LOCOMOTION, MORPHOLOGY, AND HABITAT USE IN ARBOREAL SQUIRRELS (RODENTIA: SCIURIDAE) 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 Richard L. Essner, Jr. June 2003 This dissertation entitled LOCOMOTION, MORPHOLOGY, AND HABITAT USE IN ARBOREAL SQUIRRELS (RODENTIA: SCIURIDAE) BY RICHARD L. ESSNER, JR. 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 ESSNER, JR., RICHARD L. Ph.D. June 2003. Biological Sciences Locomotion, Morphology, and Habitat Use in Arboreal Squirrels (Rodentia: Sciuridae) (135pp.) Director of Dissertation: Stephen M. Reilly Arboreal locomotion has not been well studied in mammals outside of primates and mammalian gliding has received even less attention. While numerous studies have examined morphological variation in these forms, there is currently a lack of detailed kinematic, behavioral, and ecological data to assist in explaining the patterns. Here, I present three studies that focus on differing aspects of locomotion in arboreal squirrels. These range from 3-D kinematics (Chapters 1 & 2) to morphology, locomotor behavior, and habitat use (Chapter 3). First, kinematics were quantified and compared among leaping, parachuting, and gliding squirrels to test for differences during the launch phase. Only six out of 23 variables were found to differ significantly among the three species investigated. The six significant variables were partitioned into morphological, behavioral, and performance based differences. Remarkably, there were no differences attributable to hindlimb kinematics indicating that propulsion is the same in leaping, parachuting, and gliding squirrels. Next, the initial airborne phase was investigated. Following the launch nongliding squirrels initiated gradual and symmetrical movements of the limbs. Flying squirrels initiated highly stereotyped fluttering movements characterized by a series of rapid asymmetrical rotations of the fore and hindlimbs. This behavior is hypothesized to provide control over angular momentum and disrupt detrimental fluid dynamic effects. The kinematics of the landing phase were also investigated in flying squirrels. Landing was characterized by limb adduction, tail dorsiflexion, and billowing of the patagium which acted to increase angle of attack and slow descent. Flying squirrels reached maximum extension of their limbs and maximal flexion of the vertebral column as they contacted the landing platform. This was hypothesized as a mechanism for increasing deceleration time and reducing peak landing forces. Finally, in order to determine which aspects of morphology, behavior, and ecology define evolutionary transitions from arboreality to semiarboreality/terrestriality or gliding in squirrels I investigated each of the levels using ordination (principal components analysis and correspondence analysis) and multivariate analysis of variance. In addition, I examined causal linkages across levels by testing a number of biomechanical predictions. Flying squirrels and chipmunks occupied extreme regions of morphospace, ethospace, and ecospace, while red squirrels were generally located in intermediate positions consistent with the idea that they exhibit the ancestral condition. Biomechanical predictions were supported in some instances but not in others, reinforcing the need for further study. Approved: Stephen M. Reilly Associate Professor of Biological Sciences 5 Acknowledgments I extend my sincere gratitude to my advisor Steve Reilly. Steve initially inspired me through the book he co-edited entitled Ecological Morphology. The ragged pages of that book have provided me with a roadmap throughout my graduate career. Steve has continued to inspire me through his passion for science and his quest for “the nanosecond of discovery.” I am also deeply indebted to Clay Corbin, Pete Larson, and Lance McBrayer. I have learned more from them than they will ever know. Clay in particular made the long commutes from Lancaster bearable. I will truly miss our conversations on that long and winding road. I thank Audrone Biknevicius, Ron Heinrich, and Larry Witmer for being excellent mentors. Their guidance and encouragement through the years have been a valuable asset. In addition, Sue Bullard and Brigitte Demes were extremely helpful with their comments. I sincerely appreciate their efforts on my behalf. These outstanding individuals comprised my dissertation committee and I thank them all for their support and dedication. I thank John Scheibe for giving me the “spark” of scientific curiosity. John was the first person to introduce me to the field of ecology and evolutionary biology. In addition, he did me the great service of passing along his enthusiasm for ecomorphology and gliding locomotion. I am forever in his debt. I am also indebted to Jim Robins and A. J. Hendershott for the times spent discussing gliders ad infinitum over the years. I thank the Reilly Lab past & present especially Jason Elias, Andy Parchman, and Kristen Hickey for their help with many aspects of my research. I also thank the OU 6 Evomorph group, most notably Kay Earls and Nancy Stevens, for their welcome advice. I have never been associated with a finer group of individuals. I sincerely thank the army of undergraduates who helped with much of this research. Special thanks go to Jeremy Caudill, Tara Chapman, Kim Huber, Brian Mussio, Colin Shelton, and Jonathan Vega. Their hard work made this project possible. I thank Robert Dudley, Steve Edinger, Cliff Frohlich, Ted Goslow, Robert Hikida, and Robert Srygley for helpful comments. I thank Jerry Svendsen for expanding my background in the fields of ecology, mammalogy, and statistics and for generously allowing me to borrow traps for an extended period of time. Dave Elliott was extremely generous with his time and materials on many occasions during my time at OU. Scott Carpenter and the Lab Animal Resources Staff took excellent care of the animals used in this study. Their expertise and dedication are truly impressive. I sincerely thank my family for their construction skills, but more importantly for their love and support over all of these years. They have gone above and beyond the call of duty on countless occasions and are in large part responsible for getting me to this point. Most of all I extend my deepest gratitude to my wife Jill for her inexhaustible love and patience. I cannot count the number of weekends she gave up to assist me with data collection. She has been a partner in everything I have done. This research was supported by NSF Dissertation Improvement Grant (IBN 0076342), an Ohio University Student Enhancement Award, grants-in-aid from the Society for Integrative and Comparative Biology and the American Society of Mammalogists, and several Ohio University John Houk Memorial Research Grants. 7 Table of Contents Abstract................................................................................................................................3 Acknowledgments................................................................................................................5 List of Tables .......................................................................................................................8 List of Figures......................................................................................................................9 General Introduction ..........................................................................................................11 References................................................................................................................15 Chapter 1 Three-Dimensional Launch Kinematics in Leaping, Parachuting, and Gliding Squirrels ........................................................................................................................17 Materials and Methods ............................................................................................20 Results .....................................................................................................................25 Discussion ...............................................................................................................28 References ...............................................................................................................36 Chapter 2 Three-Dimensional Aerial Kinematics in Arboreal Squirrels..........................46 Materials and Methods ............................................................................................52 Results .....................................................................................................................57 Discussion ...............................................................................................................64 References ...............................................................................................................73 Chapter 3 Morphology, Locomotor Behavior, and Habitat Use in Arboreal Squirrels....93 Materials and Methods ............................................................................................98 Results ...................................................................................................................102 Discussion .............................................................................................................105