THE BIODYNAMICS OF ARBOREAL LOCOMOTION IN THE GRAY SHORT- TAILED OPOSSUM (MONODELPHIS DOMESTICA) 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 Andrew R. Lammers August 2004 This dissertation entitled THE BIODYNAMICS OF ARBOREAL LOCOMOTION IN THE GRAY SHORT- TAILED OPOSSUM (MONODELPHIS DOMESTICA) BY ANDREW R. LAMMERS has been approved for the Department of Biological Sciences and the College of Arts and Sciences by Audrone R. Biknevicius Associate Professor of Biomedical Sciences Leslie A. Flemming Dean, College of Arts and Sciences LAMMERS, ANDREW R. Ph.D. August 2004. Biological Sciences The biodynamics of arboreal locomotion in the gray short-tailed opossum (Monodelphis domestica). (147 pp.) Director of Dissertation: Audrone R. Biknevicius Most studies of animal locomotor biomechanics examine movement on a level, flat trackway. However, small animals must negotiate heterogenerous terrain that includes changes in orientation and diameter. Furthermore, animals which are specialized for arboreal locomotion may solve the biomechanical problems that are inherent in substrates that are sloped and/or narrow differently from animals which are considered terrestrial. Thus I studied the effects of substrate orientation and diameter on locomotor kinetics and kinematics in the gray short-tailed opossum (Monodelphis domestica). The genus Monodelphis is considered the most terrestrially adapted member of the family Didelphidae, but nevertheless these opossums are reasonably skilled at climbing. The first study (Chapter 2) examines the biomechanics of moving up a 30° incline and down a 30° decline. Substrate reaction forces (SRFs), limb kinematics, and required coefficient of friction were measured. On sloped substrates, M. domestica moved more slowly with a higher duty factor, used more statically stable gaits (decline), and required a greater coefficient of friction to avoid slipping. These data suggest that a 30° slope is enough to perturb the opossums’ normal mode of locomotion, and they must therefore adjust their locomotor patterns to remain stable. On inclines, both limb pairs supported body weight equally, and the craniocaudal limb excursion increased; however, the forelimbs exerted greater propulsive impulse than hindlimbs. On the decline, the forelimbs were brought to bear far more body weight and braking effort than the hindlimbs; perhaps the greater forelimb protraction (at touchdown) was a way of accommodating a more substantial load during downhill locomotion. The second and third studies (Chapters 3 & 4) tested the effects of substrate diameter on locomotor kinetics and kinematics. On the arboreal substrate, many kinetic patterns were similar to those observed on the terrestrial. Forelimbs exhibited higher vertical impulse and peak vertical force than hindlimbs, and both limb pairs exerted a braking force followed by a propulsive force during each stride. However, the forelimbs exerted more than twice the braking and propulsive impulses than hindlimbs. The manus was placed higher around the circumference of the branch than the pes. The shifts in forces and limb placement resulted in a lower required coefficient of friction in the forelimb. Thus, the forelimbs are probably more stable than the hindlimbs, and this may explain why forelimbs have such a dominant role on the branch. Although vertical impulses were lower on the terrestrial substrate than on the arboreal support, this was most likely due to speed effects because the opossums refused to move as quickly on the arboreal trackway. Vertical impulse decreased significantly faster with speed on the arboreal substrate because most of these trials were relatively slow, and stance duration decreased with speed more rapidly at these lower speeds. A decrease in speed is a common behavioral adaptation to maintain stability. Stride length, frequency, and duration were well-correlated with speed, but spatial variables were not. Thus it is possible that timing variables were affected by speed, while substrate affected mostly spatial variables (joint angles and limb placement). The distal elements of the forelimb were significantly more adducted on the arboreal substrate, but otherwise there were few substrate effects on the forelimb. It is possible that the relatively stable placement of the manus permits the forelimb to make few kinematic adjustments for arboreal locomotion. In contrast, substrate had many significant effects on hindlimb kinematics. Like the forelimb, the distal elements of the hindlimb were significantly adducted on the arboreal trackway. On the arboreal trackway, the hindlimb was more protracted at touchdown and time of peak vertical force, and hip height was greater. The pelvic girdle of the opossums underwent lateral undulation regardless of substrate. The lack of crouching behavior on the branch may suggest that crouching behavior is not a universal adaptation to treacherous substrates. Finally, the posterior shift in weight support observed in Chapter 3 may be the result of relatively protracted hindlimbs on the arboreal trackway. Approved: Audrone R. Biknevicius Associate Professor of Biomedical Sciences ACKNOWLEDGMENTS I would like to thank my dissertation committee members: my advisor, Audrone Biknevicius, and committee members Steve Reilly, Nancy Stevens, Nancy Taterek, and Larry Witmer for their support during the completion of this dissertation. To Audrone, thank you for giving me this chance to work in your lab, for giving me a second chance when I needed it, and for your constant support, enthusiasm, and friendship. To Steve, thank you for sharing your excitement of science and of my research. To Nancy Stevens for many fruitful discussions about the biomechanical challenges of arboreal locomotion, and also for the possum poetry. To Larry, for showing me that anatomy is incredibly interesting – not only has it been enjoyable to teach human gross anatomy over the last three years, that knowledge and experience was in no small way responsible for landing my new job. To Nancy Taterek, thanks for your last-minute help and agreeing to serve on my committee on such short notice. I would also like to acknowledge my indebtedness to Kay Earls, who taught me everything I know about designing and building force transducers and programming Labview virtual instruments. I also thank former and current members of the Biknevicius lab, including Jen Hancock, Elicia Thompson, and Jeff Willey for their friendship and scientific discussion. Thanks also to all of the graduate students and faculty in the Ecology and Evolutionary Biology program at Ohio University who have helped make the past five years a truly enjoyable experience, both professionally and personally. I thank many undergraduates who spent tireless hours helping me collect data: Julie Abbuhl, Amy Back, Emily Bevis, Trish Chalfant, Jessica Demidovich, Kevin Funk, Josh Hill, Andy Parchman, ChiChi Peng, and Jen Tat. I thank Eric Lindner for his expert care of the opossums, and Randy Mulford of the physics metal shop for building many versions of the arboreal force transducers. Funding for this dissertation was provided by the Department of Biological Sciences, Ohio University, and a Sigma Xi Grant in Aid of Research. Finally, I thank my parents, Kenneth and Dorothy Lammers, and my brother Ben, for their never-ending support, and for providing a place to escape when I needed a break. Finally, thanks to my girlfriend, Darcy, whose love and support was essential to completing my dissertation and getting a job. Table of Contents List of Tables .................................................................................................................... 10 List of Figures................................................................................................................... 11 Chapter 1: The biomechanical challenges of arboreal locomotion ............................ 15 1.1. Terrestrial locomotion............................................................................................ 15 1.2. Arboreal substrates................................................................................................. 16 Incline and decline.................................................................................................... 16 Diameter ................................................................................................................... 18 1.3. Relevance............................................................................................................... 20 1.4. References.............................................................................................................. 21 Chapter 2: Locomotor kinetics and kinematics on inclines and declines in the gray short-tailed opossum (Monodelphis domestica) ............................................................ 29 2.1. Summary................................................................................................................ 29 2.2. Introduction............................................................................................................ 30 2.3. Materials and Methods........................................................................................... 34 Animals ..................................................................................................................... 34 Force data acquisition .............................................................................................