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The Functional Morphology of Lizard Locomotion: Integrating Biomechanics

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The Functional Morphology of Lizard Locomotion: Integrating Biomechanics 1 The Functional Morphology of Lizard Locomotion: Integrating Biomechanics, Kinematics, Morphology, and Behavior A dissertation presented to the faculty of the College of Arts and Sciences of Ohio University In partial fulfillment of the requirements for the degree Doctor of Philosophy Eric J. McElroy August 2008 2 This dissertation titled The Functional Morphology of Lizard Locomotion: Integrating Biomechanics, Kinematics, Morphology, and Behavior by ERIC J. MCELROY has been approved for the Department of Biological Sciences and the College of Arts and Sciences by Stephen M. Reilly Professor of Biological Sciences Benjamin M. Ogles Dean, College of Arts and Sciences 3 ABSTRACT MCELROY, ERIC J., Ph.D., August 2008, Biological Sciences The Functional Morphology of Lizard Locomotion: Integrating Biomechanics, Kinematics, Morphology, and Behavior (182 pp.) Director of Dissertation: Stephen M. Reilly Lizards have long served as a model system for understanding how locomotor functional morphology meets ecological demands. However, far less is known about how behavior modulates this relationship. Likewise, there is still a need for a comprehensive understanding of lizard locomotor functional morphology. This dissertation presents four studies that focus on how behavior molds locomotion and advances our understanding of lizard locomotor functional morphology. Chapter one examines variation in locomotor performance, whole-body mechanics and gaits in a phylogenetic array of lizards that use differing foraging modes. Multivariate and phylogenetic comparative analyses show that foraging mode drives the evolution of biomechanics and gaits in lizards. Sit-and-wait species used only fast speeds, trotting gaits, and running mechanics, whereas wide foraging species independently evolved slower locomotion, different walking gaits, and walking mechanics. Chapter two examines patterns of variation in the hierarchical relationship among morphology, kinematics and force during fast running in seven species of lizards. Multivariate analyses test for correlations among levels to reveal the morphological basis for kinematics and locomotor forces. The results show that limb length, support duration and float distance directly influence the nature of forces applied to the ground during the support phase of steady state locomotion and suggest that this relationship may affect locomotor energetics and endurance. 4 Chapter three examines the effects of habitat, behavior, and their interaction on undisturbed locomotor speeds in Urosaurus ornatus. Detailed video analysis of undisturbed behavior reveals that locomotor speed decreases with increasing perch height, when animals move on woody substrates, and while displaying and capturing prey. No relationship is found between speed and perch diameter or substrate incline. Finally, the interaction between perch diameter and feeding behavior results in a negative relationship between speed and perch diameter during feeding but not during other behaviors. I suggest that the relationship between habitat, behavior, and speed is affected by the level of locomotor performance (maximal vs. sub maximal) that animals routinely use during undisturbed activity. Finally, chapter four presents a detailed analysis of “foraging” behavior and field locomotor performance in a sit-and-wait (Sceloporus undulatus) and wide foraging (Aspidoscelis flagellicaudus) species. Both sit-and-wait and wide foraging species clump relatively slow locomotor behaviors just before prey attacks, a finding at odds with hypotheses from the literature. This result, along with previous studies, suggests that selection on maximum speed and endurance is not acting through the filter of foraging behavior. I suggest that “foraging mode” should be examined in light of an existing model of animal foraging (the Webb model) to direct future studies of the ecology and evolution of animal performance in relation to foraging behavior. Approved: _____________________________________________________________ Stephen M. Reilly Professor of Biological Sciences 5 ACKNOWLEDGMENTS I am especially grateful to my wife Julie and daughter Matilda for their love and support throughout this dissertation. You have made completion of this dissertation even more fulfilling than I could have imagined. We are all thankful for the support and encouragement our families have given over the past five years. Steve Reilly taught me how to think deeply and completely as a scientist. Thank you for the many quarters of research support and travel to Australia and for completely opening up your laboratory to my research endeavors. You are a great mentor, colleague, and friend. Audrone Biknevicius guided my thoughts on locomotor biomechanics and was a calming force during many frustrating hours fixing broken force plates. Audrone, thank you for all of your time, your effort, and your friendship. Don Miles provided advice and was key in sparking my interest in comparative methods and biostatistics. Thank you for this inspiration. I thank Gar Rothwell for graciously serving as the external committee member for my defense. I thank Duncan Irschick for providing advice and financial support for much of the field work presented in this dissertation. Lance McBrayer, Phil Allman, Andre Fernandez, Pat O’Connor, Nancy Stevens, Angela Horner, Dawn and Casey Holliday, Tobin Hieronomys, Susan Williams, Larry Witmer, John Bertram, Henry Streby, Duncan Irschick, Mike Jorgenson, Jen Hancock, Scarlett Tudor, Willem Roosenburg, Molly Morris, Brian Horne, Jay Meyers, Carl Hoagstrom, Scott Moody, Pete Zani and many others have engaged in many discussions in regards to this dissertation and my development as a scientist. Thank you all for your time and thoughts. 6 Jeff Willey and Bob Verb are responsible for my pursuit of a Ph. D. at Ohio University. Thank you both for guiding me to OU and to pursue a career in academics. Many people helped me accomplish the research in this dissertation. First and foremost several undergraduates helped collect and analyze hours of lizard locomotor data. For this I grateful to: Emily Bevis, Caityln Cato, Alex Fotis, Bailey Miles, Jodi Mrosko, Grant Beaman, Kris Stover, Kristen Hickey, and Andrew Parchman. Duncan Irschick, Jay Meyers, and Chloe Marien provided logistical and moral support during many hard hours filming Urosaurus and Aspidoscelis at Wet Beaver Creek. Lance McBrayer was instrumental in the collection of data from Sceloporus in Georgia. Andrew Odum and the herpetology staff at the Toledo Zoo allowed me to race Cordylus. Jens Vindum and Bob Drewes (California Academy of Sciences), Robert Espinosa (California State University at Northridge), Steve Rodgers (Carnegie Museum), Jim McGuire (University of California Museum of Vertebrate Zoology), Linda Trueb (Kansas) and Kevin De Quieroz (Smithsonian) kindly loaned lizard specimens for morphological study. Scott Moody helped me access the Ohio University reptile collection. Joe Eastman taught me how to use the x-ray machine and the finer points of developing films; he also graciously provided films and chemicals. Robbie Wilson and Mike Bennett facilitated work in Australia on Eulamprus. John Bertram, Kay Earls, Andy Lammers, and David Lee provided assistance with the force platform and virtual instrument programming. Along with undergraduates, Ohio University Animal Care (Nelson Frey and Eric Linder) ensured that all lizards received top notch care while in the lab. Arizona Game and Fish quickly processed research permits. 7 This research was funded by NSF grants (IBN 9727212; IBN 0080158; IOB 0520100), an Ohio University Research Challenge grant, and a Provost undergraduate research fund grant to Steve Reilly. Duncan Irschick’s NSF grant (IOB 0421917) provided partial support for work in Arizona. I was funded by an Ohio University Center for Ecology and Evolution Research Fellowship, a University Doctoral Fellowship, a Charles Stearns Grant-in-Aid for Herpetological Research from the California Academy of Sciences, a Phi Delta Theta scholarship, an Ohio Board of Regents Scholarship, an Ohio University Student Enhancement Award, and at Graduate Student Senate research grant. 8 TABLE OF CONTENTS Page ABSTRACT .........................................................................................................................3 ACKNOWLEDGMENTS ...................................................................................................5 LIST OF TABLES .............................................................................................................10 LIST OF FIGURES ...........................................................................................................11 GENERAL INTRODUCTION ..........................................................................................13 Synopsis of Chapters..............................................................................................14 References ..............................................................................................................17 CHAPTER 1: THE CORRELATED EVOLUTION OF BIOMECHANICS, GAIT AND FORAGING MODE IN LIZARDS ...................................................................................21 Introduction ............................................................................................................21 Materials and Methods ...........................................................................................23 Study Species .............................................................................................23
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