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University of California Riverside and San Diego UNIVERSITY OF CALIFORNIA RIVERSIDE AND SAN DIEGO STATE UNIVERSITY Factors That Influence the Performance of Complex Behaviors in a Terrestrial Vertebrate: Variability in the Kangaroo Rat Evasive Leap A Dissertation submitted in partial satisfaction of the requirements for the degree of Doctor of Philosophy in Evolutionary Biology by Grace Freymiller June 2021 Dissertation Committee: Dr. Rulon Clark, Co-Chairperson Dr. Timothy Higham, Co-Chairperson Dr. Christopher Clark Dr. Marshal Hedin Copyright by Grace Freymiller 2021 The Dissertation of Grace Freymiller is approved: ________________________________________________________ ________________________________________________________ ________________________________________________________ Committee Co-Chairperson ________________________________________________________ Committee Co-Chairperson University of California, Riverside San Diego State University ACKNOWLEDGEMENTS This research would not be possible without the help of many research assistants who each helped collect data in the field, stuck through difficult working conditions, and provided great company during long field seasons: Jessica Ryan, Drew Steele, Katherine Phillips, Colin Goodman, Regina Spranger, Frank Accardo, Corrina Tapia, Timothy Garvey, Devin Murphy, Arturo Barrett, Delaney Curran, Emily Zart, Antonio Ruvalcaba, Kaleb Hill, Dayna Levine, and Sara Friemuth. I am thankful for the staff of the Chiricahua Desert Museum, the Rancho Jamul Ecological Reserve, Sweeney Granite Mountains Desert Research Center, and the CSU Desert Studies Center for logistical support during field data collection, as well as the Marine Corps Air Station, Yuma and Abigail Rosenberg for providing us with access to the Barry M. Goldwater Range. I thank my committee members and collaborators for their insight and assistance during the development and structuring of my research: Timothy Higham, Christopher Clark, Marshal Hedin, Kevin Burns, and Craig McGowan. I would like to thank Rulon Clark, who has been an incredible mentor and friend. I’m honored to have had the privilege to work with you and address so many interesting questions about such an amazing system. iv I thank Earl, Lucy, and Christina Freymiller for their encouragement and inspiration. Thank you for fostering my love of science, fascination with animals, and motivation to push myself beyond what I ever thought was possible. And of course, I would like to thank Malachi Whitford for providing endless support during all aspects of this journey—I couldn’t imagine sharing these unforgettable memories with anyone else but you. This research was funded by the National Science Foundation, the American Society of Mammalogists, the Animal Behavior Society, the American Philosophical Society, and San Diego State University. The text of this dissertation, in part, is a reprint of the material as it appears in “Recent Interactions With Snakes Enhance Escape Performance of Desert Kangaroo Rats (Rodentia: Heteromyidae)” (2017) and “Escape Dynamics of Free-Ranging Desert Kangaroo Rats (Rodentia: Heteromyidae) Evading Rattlesnake Strikes” (2019). The co- author Rulon Clark listed in these publications directed and supervised the research which forms the basis for this dissertation. The co-author Timothy Higham listed in these publications provided technical expertise and feedback on the manuscripts. The co-author Malachi Whitford listed in these publications aided in data collection/analysis and provided feedback on the manuscripts. v ABSTRACT OF THE DISSERTATION Factors That Influence the Performance of Complex Behaviors in a Terrestrial Vertebrate: Variability in the Kangaroo Rat Evasive Leap by Grace Freymiller Doctor of Philosophy, Graduate Program in Evolutionary Biology University of California, Riverside and San Diego State University, June 2021 Dr. Rulon Clark and Dr. Timothy Higham, Co-Chairpersons Physical performance inextricably ties variation in physiology, morphology, and behavior to fitness. By studying how morphology is linked to performance, and the consequences of performance ability on survival and reproduction, evolutionary biologists can understand the selection pressures driving the evolution of particular morphological characteristics. However, many studies of performance are conducted in the lab in order to control external factors, allowing for detailed analyses of a few potentially influential variables but reducing the overall ecological realism of the results. The capacity for field studies to capture natural levels of variability helps to elucidate important ecological factors that influence locomotor performance and therefore drive individual fitness. This dissertation explores the evolution of bipedalism in rodents and the factors that affect their jump performance using a field- based approach. To do this, I investigated (1) the natural jump performance of kangaroo rats (Dipodomys) by filming their escapes from rattlesnake strikes, (2) the conditions under vi which they utilize these impressive jump escapes, (3) the relationship between hindlimb morphology and jump performance, and (4) how jump performance compares between bipedal and quadrupedal rodents. From these studies, I was able to determine their natural levels of performance, the ecological contexts that place selective pressure on jump performance, how those pressures on performance have shaped the evolution of their hindlimb morphology, and whether bipedality indeed confers improved jump performance when compared to quadrupedal rodents. vii TABLE OF CONTENTS Introduction ....................................................................................................................... 1 References ....................................................................................................................... 4 Chapter 1: Escape dynamics of free-ranging desert kangaroo rats (Rodentia: Heteromyidae) evading rattlesnake strikes Abstract ........................................................................................................................... 7 Introduction ..................................................................................................................... 8 Methods ......................................................................................................................... 11 Results ........................................................................................................................... 15 Discussion ..................................................................................................................... 17 References ..................................................................................................................... 24 Figures & Tables ........................................................................................................... 28 Chapter 2: Recent interactions with snakes enhance escape performance of desert kangaroo rats (Rodentia: Heteromyidae) during simulated attacks Abstract ......................................................................................................................... 31 Introduction ................................................................................................................... 32 Methods ......................................................................................................................... 35 Results ........................................................................................................................... 43 Discussion ..................................................................................................................... 46 References ..................................................................................................................... 54 Figures and Tables ........................................................................................................ 58 viii Chapter 3: Comparative analysis of Dipodomys species indicates that kangaroo rat hindlimb anatomy is adapted for rapid evasive leaping Abstract ......................................................................................................................... 60 Introduction ................................................................................................................... 61 Methods ......................................................................................................................... 66 Results ........................................................................................................................... 71 Discussion ..................................................................................................................... 72 References ..................................................................................................................... 77 Figures and Tables ........................................................................................................ 81 Chapter 4: Springing into action: comparing jump performance between bipedal and quadrupedal rodents Abstract ......................................................................................................................... 87 Introduction ................................................................................................................... 88 Methods ......................................................................................................................... 91 Results ..........................................................................................................................
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