COMPARATIVE STUDIES IN THE FUNCTIONAL MORPHOLOGY OF LIZARD FEEDING: KINEMATICS, BEHAVIOR, AND BIOMECHANICS 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 Lance D. McBrayer August 2002 This dissertation entitled COMPARATIVE STUDIES IN THE FUNCTIONAL MORPHOLOGY OF LIZARD FEEDING: KINEMATICS, BEHAVIOR, AND BIOMECHANICS BY LANCE D. MCBRAYER has been approved for the Department of Biological Sciences and the College of Arts and Sciences by Stephen M. Reilly Associate Professor of Biological Sciences Leslie A. Flemming Dean, College of Arts and Sciences McBrayer, Lance D. Ph.D. August 2002. Biological Sciences Comparative Studies in the Functional Morphology of Lizard Feeding: Kinematics, Behavior, and Biomechanics (148pp.) Director of Dissertation: Stephen M. Reilly In fish, mammals, and birds the functional morphology of the feeding apparatus has been well studied. However in lizards (non-ophidian squamates), much less is known about the functional variation that may result from their diverse cranial morphologies. Here, I present four functional studies of the lizard feeding apparatus. Initially, the feeding kinematics of lizards were quantified and used to test two existing models of prey transport for all amniotes. To do so, I devised a method to quantitatively test for differences in kinematic phases of mouth opening. This method, slope analysis, demonstrated that feeding kinematics were highly variable intra- and interspecifically and that one model accurately characterized prey transport in lizards. Next, variation in feeding behavior was quantified to understand how members of two clades (Iguania, Autarchoglossa) process their prey. Iguanian lizards processed their prey using mostly a palatal crushing behavior while autarchoglossans used puncture crushing. Iguanians also engaged in significantly fewer processing behaviors per feeding bout. Autarchoglossans processed prey extensively and interspersed processing behaviors with transport behaviors. In fact, three behaviors, puncture crushing, prey transport and the total number of behaviors, are coevolving based on independent contrasts analysis. Interestingly, patterns in feeding behavior closely paralleled the dichotomy seen in foraging mode between these clades. Because feeding behavior and foraging mode are likely related, I investigated how feeding morphology and foraging mode evolve in a group of closely related species. I tested the hypothesis that feeding biomechanics and performance coevolve with foraging mode in Kalahari lacertids. The head length and width variables supported this hypothesis; however, the remaining variables and biting performance did not. Given the extreme dependence of all Kalahari lizards on termites, it is likely that this dietary constraint prevents morphological specialization. Finally, the tradeoffs between lizard skull form and biting performance are explored. Lizards exceeded predictions regarding the position of the most posterior tooth and muscle resultant. Head width and depth were highly correlated with biting performance within species, however among species, lever mechanics were better predictors. Consequently further studies of functional tradeoffs are required to understand how they might influence lizard ecology and evolution. Approved: Stephen M. Reilly Associate Professor of Biological Sciences 5 Acknowledgments My deepest appreciation is extended to my wife, Juliann, and my family for their unwavering emotional and financial support. Without them, the completion of this dissertation would have little meaning. Also, I am forever indebted to my advisor, Steve Reilly, for taking me on as a student and teaching me the skills required to be successful as a scientist. Thanks, Steve, for being a great mentor, teacher, and friend. Clay Corbin, Rick Essner, and Peter Larson were subjected to ridiculously long and tedious discussions of all things biological, political, and philosophical. Without these people or these therapeutic sessions, I would know and understand very little about biology or life. I will be forever grateful to have known and learned from all of the above mentioned people and will cherish their friendships forever. I greatly appreciate the advice and assistance of Audrone Biknevicius, Don Miles, and Scott Moody. Thank you for providing sound guidance and support. I hope I can reciprocate someday. I sincerely thank Roger Anderson and Tom White for their loan of lizards, equipment and time. You each taught me a great deal and I look forward to our continued personal and professional relationships. I was very fortunate to have met John Steffen during fieldwork and am grateful for his hard work, support, and friendship. Martin Price was extremely helpful during fieldwork in South Africa, and I consider myself very lucky to have worked with him. Also during fieldwork in South Africa and Namibia, Mike Griffin, Henke Picard, Fricki Picard, Henne Molle, Sorel Burger, John, and Callo, provided tremendous assistance and support. Thank you all. Finally and most importantly, the advice and logistical knowledge of Aaron Bauer, Alexander Flemming, and Mike Griffin made the whole trip possible. 6 I thank Dr. Winfried Just and Dr. Willem Roosenburg for ideas and discussion regarding methods to quantify and compare gape profiles. The Ecolunch and Evomorph discussion groups at Ohio University provided many helpful discussions, ideas, and criticisms of this and other research related to lizard feeding. I thank Larry Witmer, Kevin de Queiroz, Molly Morris, Kurt Schwenk, Anthony Herrel, Gad Perry, Bill Cooper, Ray Huey, and Ron Heinrich for comments and discussion on various aspects of this work. I would like to thank the following undergraduate students for their tremendous effort, dedication, and assistance with data collection, digitization, and lizard husbandry: Kristin Hickey, Andrew Parchman, Jason Elias, Andrew Clifford, Paul Bedocs, Jill Radnov, Adrienne Fuhr, Lori Gill, Julia Keith, Bethany Suchowiecki, Mike Mullins, Stephanie Poduska, and Chris Akers. The personnel at the Animal Holding facilities at Ohio University helped tremendously with the care and maintenance of lizards. This research was supported by a Claude Kantner Fellowship, an Ohio University Student Enhancement Award, a Sigma Xi Grant-in-Aid of Research, several Ohio University Department Biological Sciences Travel Awards, and several John Houk Memorial Research Grants. 7 Table of Contents Abstract................................................................................................................................3 Acknowledgements...............................................................................................................5 List of Tables ........................................................................................................................8 List of Figures.......................................................................................................................9 General Introduction ..........................................................................................................10 Literature Cited.......................................................................................................13 Chapter 1 Testing amniote models of prey transport kinematics: a quantitative analysis of mouth opening patterns in lizards...................................................................................14 Materials and Methods............................................................................................17 Results....................................................................................................................22 Discussion...............................................................................................................24 Literature Cited.......................................................................................................32 Chapter 2 Prey processing in lizards: Behavioral variation in sit-and-wait and wide foraging taxa.................................................................................................................................43 Materials and Methods............................................................................................45 Results....................................................................................................................48 Discussion...............................................................................................................52 Conclusions.............................................................................................................56 Literature Cited.......................................................................................................59 Chapter 3 The relationship between skull morphology, biting performance and foraging mode in Kalahari lacertid lizards..................................................................................74 Materials and Methods............................................................................................77 Results....................................................................................................................84 Discussion...............................................................................................................88 Literature Cited.......................................................................................................95