Utah State University DigitalCommons@USU All Graduate Theses and Dissertations Graduate Studies 5-2016 Stable Isotopes and the Ecology and Physiology of Reptiles Andrew M. Durso Utah State University Follow this and additional works at: https://digitalcommons.usu.edu/etd Part of the Biology Commons Recommended Citation Durso, Andrew M., "Stable Isotopes and the Ecology and Physiology of Reptiles" (2016). All Graduate Theses and Dissertations. 5064. https://digitalcommons.usu.edu/etd/5064 This Dissertation is brought to you for free and open access by the Graduate Studies at DigitalCommons@USU. It has been accepted for inclusion in All Graduate Theses and Dissertations by an authorized administrator of DigitalCommons@USU. For more information, please contact [email protected]. STABLE ISOTOPES AND THE ECOLOGY AND PHYSIOLOGY OF REPTILES by Andrew M. Durso A dissertation submitted in partial fulfillment of the requirements for the degree of DOCTOR OF PHILOSOPHY in Biology Approved: ______________________ ______________________ Susannah S. French Alan H. Savitzky Major Professor Committee Member ______________________ ______________________ Edmund D. Brodie Lise M. Aubry Committee Member Committee Member ______________________ ______________________ Daniel A. Warner Mark McLellan Committee Member Vice President for Research and Dean of the School of Graduate Studies UTAH STATE UNIVERSITY Logan, Utah 2016 ii Copyright © Andrew M. Durso 2016 All Rights Reserved iii ABSTRACT Stable Isotopes and the Ecology and Physiology of Reptiles by Andrew M. Durso, Doctor of Philosophy Utah State University, 2016 Major Professor: Dr. Susannah S. French Department: Biology Animals trade-off limited resources among competing demands. Trade-offs are difficult to quantify because it is challenging to measure investment into disparate physiological systems using a common scale. Additionally, biologists desire methods to more precisely measure energy status in wild animals. I used stable isotopes to help solve both of these problems. I examined natural spatial and temporal variation in stable isotope signatures of wild lizards and found significant variation. In the lab, I was able to demonstrate the utility of nitrogen stable isotope ratios of uric acid pellets for measuring nutritional stress. By tracing labeled amino acids through the bodies of gravid female lizards, I demonstrated that vitellogenesis and wound healing compete for amino acids and quantified the direction and magnitude of the trade-offs. I showed that reproductive-immune trade-offs vary based on reproductive stage and energy availability, have effects on metabolism and immune function, and are influenced by hormonal mechanisms. My findings shed light on the interconnectedness of stable isotope endpoints and key physiological systems in animals. I showed that isotopic signatures of physiological stress can be reflected at a large scale in natural populations, and I made novel measurements of the size and direction of trade-offs, which were formerly limited to physiological and performance outcomes. (160 pages) iv PUBLIC ABSTRACT Stable Isotopes and the Ecology and Physiology of Reptiles Andrew M. Durso When animals don’t have enough food, they have to “choose” between “spending” their limited energy on themselves or on their offspring. Biologists think that reptiles can make this choice quickly in response to different environments. But, it can be hard to study these choices because it is hard to convert between, for example, the number of eggs laid and the speed of healing a wound. By using stable isotope chemistry, we can collect more detailed and comparable information about how lizards and other animals spend their limited resources than with any other method. For example, lizards in the wild have similar stable isotope signatures to nearby plants and insects, because their bodies are built out of these foods. In the lab, the stable isotope signatures of lizard “pee” (uric acid) change in predictable ways when they are hungry. We could essentially measure how hungry a wild lizard is by looking at the stable isotope signatures of its uric acid. We can also use a stable isotope “spike” to track where resources go within a lizard’s body. Because protein from food is used for both healing wounds and creating egg yolk, we can measure which of these is a greater priority for lizards by examining the amount of our stable isotope spike that ends up in both places. I found that lizards make different choices under different circumstances; in particular, their stage of pregnancy had a strong effect on how much protein they put into their eggs. This technique could be used on any animal, isn’t very expensive, and could help us learn a lot more about exactly how our bodies, and those of other animals, work. v ACKNOWLEDGMENTS During the course of this dissertation, I received funding, directly or indirectly, from the National Science Foundation, USDA Agricultural Research Service, USU College of Science, USU Department of Biology, USU Ecology Center, and Utah Public Radio. Wild lizards were collected under the authority of Utah State Department of Wildlife Resources COR #1COLL8382 and handled in accordance with USU IACUC protocol #2068. I received generous technical and logistical support with mass spectrometry from John Stark, Kendal Morris, Katrina Slabaugh, and Tom Maddox. Michael Angilletta and Dale DeNardo provided support to Geoff Smith as he collected respirometry data at Arizona State University. Michael Piep and Carlee Coleman helped me with plant identification, and James Pitts helped me with insect identification. Susan Durham advised me on statistics. I had the privilege of working with several wonderful lab assistants, especially Sydney Greenfield and Cheyne Warren, but also Sabrina Anderson, Tyler Hansen, Heather Jones, Kati Mattinson, Sarah Mueller, and Taylor Pettit. I also enjoyed the company and help of numerous field assistants, including Alex Berryman, Jennica Blasi, Trevor Brown, Naomi Clements, Holly Flann, Dacia Hunter, Jenny Kordosky, Georgia Kosmala, Nick Kiriazis, John Pettit, Austin Spence, Marilize van der Walt, Richard Walker, Eleanor Watson, and Julianne Wood. I wish to thank my advisor, Susannah French, and my committee members, Al Savitzky, Butch Brodie, Lise Aubry, and Dan Warner, for their mentorship and support. Their graduate students and my friends, Lori Neuman-Lee, Geoff Smith, Alison Webb, Spencer Hudson, Shab Mohammadi, and Gareth Hopkins, were indispensable companions in the field and lab. USU Biology faculty Marty Crump and Nancy Huntly mentored me in numerous ways. Finally, I wish to thank my partner, Kendal Morris, and my family, especially my mother Sandy Durso, father Paul Durso, and brother Kevin Durso, for their love and support in all things. vi CONTENTS Page ABSTRACT ......................................................................................................................... iii PUBLIC ABSTRACT............................................................................................................ iv ACKNOWLEDGMENTS ....................................................................................................... v LIST OF TABLES ...............................................................................................................viii LIST OF FIGURES ............................................................................................................... ix CHAPTER 1. INTRODUCTION ...................................................................................................... 1 A Stable Isotope Primer .............................................................................................. 1 Stable Isotopes and Animal Physiology........................................................................ 2 Trade-offs in Animal Physiology ................................................................................. 4 Natural Abundance Variation in Stable Isotope Ratios .................................................. 5 Stable Isotope Tracer Experiments ............................................................................... 7 Reptiles...................................................................................................................... 7 Dissertation Overview................................................................................................. 9 References ............................................................................................................... 12 2. STOICHIOMETRIC AND STABLE ISOTOPE RATIOS SUPPORT STRESS PHYSIOLOGY OF WILD LIZARDS IN AN URBAN LANDSCAPE ........................ 22 Introduction ............................................................................................................. 22 Methods ................................................................................................................... 25 Results ..................................................................................................................... 28 Tables and Figures.................................................................................................... 29 Discussion................................................................................................................ 40 References ............................................................................................................... 44 3. STABLE ISOTOPE RATIOS OUTPERFORM OTHER PHYSIOLOGICAL ENDPOINTS OF NUTRITIONAL STRESS .............................................................