MORPHOLOGICAL AND BEHAVIORAL DEVELOPMENT IN A TOP NORTH AMERICAN CARNIVORE, THE COYOTE By Suzanne La Croix A DISSERTATION Submitted to Michigan State University in partial fulfillment of the requirements for the degree of DOCTOR OF PHILOSOPHY Zoology 2011 ABSTRACT MORPHOLOGICAL AND BEHAVIORAL DEVELOPMENT IN A TOP NORTH AMERICAN CARNIVORE, THE COYOTE By Suzanne La Croix Young animals must resolve the conflicting demands of survival and growth, ensuring that they can function while developing towards their adult form. The ontogenetic relationship between cranium and mandible is of special interest because these two parts of the feeding apparatus must function in concert while both change along steep growth trajectories. Further, phenotypic plasticity in the feeding apparatus warrants investigation because variation in the emergent phenotype of the food processing apparatus has obvious implications for form and function, and important consequences for survival. This dissertation investigated morphological and behavioral development of coyotes. First, I examined ontogenetic changes in skull shape and the relationship between cranium and mandible, relative to key life-history events. In coyotes, there was synchrony of growth between cranium and mandible, and asynchrony of mandibular development; these patterns were also characteristic of spotted hyenas. However, coyotes had a much less protracted development than that in hyenas, and coyotes were handicapped relative to adults for a much shorter time. Morphological development did not predict life-history events in these two carnivores as it has in rodents. Second, I investigated the ontogeny of feeding performance and feeding biomechanics in coyotes. The results showed that the development of feeding performance was asynchronous with that of both feeding biomechanics and skull morphology and that this pattern was also characteristic of spotted hyenas. This developmental asynchrony suggests that a certain minimum threshold of physical growth and development, together with the associated development of biomechanics, are required to produce effective mastication. Third, I examined developmental plasticity in feeding behavior and feeding apparatus morphology by documenting variation in adult phenotypes due to experimental manipulation of diet. Variation in early bone processing opportunities lead to differences in adult skull shape, size and mastication musculature and this variation in morphology mediated the relationship between early diet and adult feeding performance. Fourth, I examined phenotypic plasticity in feeding apparatus morphology and feeding biomechanics through a comparison of captive and wild coyote skulls drawn from the same geographical area. Skull shape, skull size and length, and feeding biomechanics exhibited phenotypic plasticity in response to captivity. I demonstrated environmental effects on adult form, and such differences in form have implications for function. Collectively, the chapters in this dissertation provide a great deal of insight into developmental relationships between skull morphology and feeding behavior in Canis . Our results support the idea that developmental processes exhibit phenotypic plasticity, being sensitive to environmental effects. This results in variation in ontogenetic outcomes and has implications for both adult form and function. Copyright by SUZANNE LA CROIX 2011 ACKNOWLEDGEMENTS My doctoral research follows from my life-long fascination with canids and my undergraduate regret of never having taken a course in zoology. In 1992, I remedied the regret and was set upon a new life path - a scientific career that featured ethological research on canids. To start at the beginning, then, I must thank Dr. Nancy Seefelt, my graduate student colleague at both Central Michigan University and Michigan State University (MSU), who made my introduction to Dr. Kay Holekamp in 2001. Having found a synergy with Kay, I soon moved to East Lansing with my entourage of seven dogs and set to work. For this opportunity and for all her support throughout my doctoral research, I thank Kay Holekamp. Kay is an outstanding mentor who generously shares her vision while providing us with the tools to develop our own. She is a rigorous, passionate, and intelligent scientist who leads by example. Her scholarly achievements and professional demeanor inspire us to develop complex research questions and to network across academic disciplines. She is also understanding, encouraging and loyal; her faith in our abilities to reach our prescribed goals never wavers and she is first at the finish line to offer her sincerest congratulations. Kay has impacted me in so many ways, personally and professionally, that words are inadequate to express what a privilege it is to count her among my confidents and my colleagues. For all this, I am appreciative and grateful. My other committee members, Drs. Laura Smale, Barbara Lundrigan and Joseph Vorro, have also generously offered me their support and insights at every v critical stage of my doctoral program. Without their encouragement and wisdom, this dissertation would surely be a different product. Laura Smale gave scientific basis to my interests in development periods and all things ontogenetic. Barb Lundrigan encouraged my efforts to create a one-of-a-kind ontogenetic series of known-age coyote skulls and set me on the path of geometric morphometrics. And Joe Vorro brought fresh perspectives and anatomical expertise to my research while offering great life advice at no extra charge. During my time at MSU, I have had the opportunity to share a lab with Sarah Benson-Amram, Pat Bills, Andy Booms, Katy Califf, Leslie Curren, Stephanie Dloniak, Anne Engh, Andy Flies, David Green, Julia Greenberg, Sarah Jones, Joe Kolowski, Sarah Lansing, Eva-Maria Muecke, Wiline Pangle, Kate Shaw, Jennifer Smith, Greg Stricker, Eli Swanson, Jaime Tanner, Kevin Theis, Russ Van Horn, Page Van Meter, Aaron Wagner, Sofi Wahaj, Heather Watts, and Marc Wiseman. Our extended lab family included Terri McElhinny and the members of the McAdam’s lab. I have enjoyed their camaraderie, insight and encouragement and thank them for all their suggestions and assistance along the way. In addition, I would like to thank Casey Leonard and Gwen Webster, MSU undergraduates, and Andrea Beaudet, a promising high school student, for their personal assistance in collecting data. This work could never have been accomplished without the assistance and direct support of the USDA APHIS Wildlife Services National Wildlife Research Center Logan Field Station in Millville, Utah. I am grateful for their interest in this project and for their tireless efforts. Dr. John Shivik, Doris Zemlicka, Jeff Schultz, vi Stacey Brummer, Patrick Darrow, and many other staff members at the Logan Field Station provided unparalleled support in facilitating my access to research animals and in managing animal care during my study. Further, I would like to thank the Utah State University community for welcoming me to their canid luncheons, especially Drs. Fred Knowlton, Mike Jaeger, Eric Gese and Lynne Gilbert-Norton. Their camaraderie and insights into coyotes were most valuable to me. The success of this project has relied greatly on collaborative input. I am especially indebted to Dr. Miriam Zelditch of the University of Michigan. Her knowledge of geometric morphometrics provided the foundation for my analyses of skull growth, development and plasticity. Further, Miriam’s insights and mentoring have molded my critical thinking skills and made me a better scientist. I would also like to thank Laura Abraszinskas and Paula Hildebrandt, of MSU Museum, who provided the technical expertise and manpower for creating a world class ontogenetic collection of coyote skulls. In addition, Drs. David Long and Matthew Parsons of MSU’s Department of Geological Sciences provided equipment and supervision for the lyophilization of mastication muscles. Finally, I would like to thank the entire staff of the MSU Zoology Department; it is their administrative support and daily doses of cheer that permit us to successfully navigate the hurdles to degree completion. I thank MSU for their generous support during all phases of my dissertation work. The College of Natural Science awarded me Graduate Summer Research and Dissertation Completion Fellowships. I received Research Enhancement and Travel Fellowships from the Graduate School. The Department of Zoology provided me vii with a John R. Shaver Award and Research Grants. This work was also made possible by National Science Foundation grants awarded to Kay Holekamp (IOB0618022 and IOS-0819437). Without this financial support, none of this research would have been possible. Finally, I would like to express my gratitude to my family. The unwavering support of my husband, Geoff Barker, and our daughter, Brooke, have permitted me to pursue and complete this research. My parents, too, have assisted whenever possible to help me attain my personal goals. And of course, our dogs were my loyal companions throughout. viii TABLE OF CONTENTS LIST OF TABLES……………………………………………...…………………...……….x LIST OF FIGURES…………………………………………………………………..……xiv CHAPTER 1: GENERAL INTRODUCTION…………………………………..…………………...…..…1 CHAPTER 2: ONTOGENETIC RELATIONSHIPS BETWEEN CRANIUM AND MANDIBLE IN COYOTES AND HYENAS………………...………………………………………..…….13 Introduction………………………………………………………….…….………..14 Methods…………………………………………………………………..………...18 Results…………………………………………………………………..………….28 Discussion……………………………………………………………..………...…42