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The Skeletal Biology of Hibernating Woodchucks (Marmota Monax)

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The Skeletal Biology of Hibernating Woodchucks (Marmota Monax) THE SKELETAL BIOLOGY OF HIBERNATING WOODCHUCKS (MARMOTA MONAX) A dissertation submitted to Kent State University in partial fulfillment of the requirements for the degree of Doctor of Philosophy by Alison H. Doherty May, 2013 Dissertation written by Alison H. Doherty B.A., University of Wyoming, 2003 M.A., Kent State University, 2007 Ph.D., Kent State University, 2013 Approved by ________________________, Chair, Doctoral Dissertation Committee Christopher J. Vinyard ________________________, Members, Doctoral Dissertation Committee William J. Landis ________________________, Walter E. Horton, Jr. ________________________, J.G.M Thewissen ________________________, Werner J. Geldenhuys Accepted by ________________________, Chair, Department of Cell and Molecular Biology Robert V. Dorman ________________________, Dean, College of Arts and Sciences Raymond A. Craig ii TABLE OF CONTENTS LIST OF FIGURES ............................................................................................... v LIST OF TABLES ................................................................................................. ix ACKNOWLEDGEMENTS .................................................................................... xii CHAPTER Page 1 INTRODUCTION ............................................................................................. 1 Hibernation ................................................................................................ 2 An Introduction to Skeletal Physiology ..................................................... 17 2 BEHAVIORAL CHANGES IN THE LOCOMOTION OF WOODCHUCKS BEFORE AND AFTER HIBERNATION ......................................................... 27 Introduction .............................................................................................. 27 Materials and Methods............................................................................. 38 Results ..................................................................................................... 56 Discussion .............................................................................................. 70 3 HIBERNATION DOES NOT REDUCE CORTICAL BONE DENSITY, AREA OR SECOND MOMENTS OF INTERIA IN WOODCHUCKS ............. 79 Introduction ............................................................................................. 79 Materials and Methods............................................................................. 83 Results ..................................................................................................... 90 Discussion ............................................................................................. 105 4 BONE DENSITY AND CROSS-SECTIONAL PROPERTIES IN ACTIVE AND HIBERNATING ADULT WOODCHUCKS ........................................... 114 Introduction ............................................................................................ 114 Materials and Methods........................................................................... 118 Results ................................................................................................... 132 Discussion ............................................................................................ 139 iii TABLE OF CONTENTS (Continued) CHAPTER Page 5 THREE-POINT BENDING TESTS COMPARING BONE STRENGTH BEFORE AND AFTER HIBERNATION IN ADULT WOODCHUCKS .......... 146 Introduction ............................................................................................ 146 Materials and Methods .......................................................................... 149 Results ................................................................................................... 156 Discussion ............................................................................................. 163 6 ANALYSES OF SEASONAL CHANGES IN BLOOD SERUM TO ASSESS BONE MAINTENANCE IN HIBERNATING AND ACTIVE WOODCHUCKS ......................................................................................... 170 Introduction ........................................................................................... 170 Materials and Methods........................................................................... 183 Results ................................................................................................... 192 Discussion ............................................................................................ 200 7 SUMMARY AND CONCLUSIONS .............................................................. 212 Summary of the Skeletal Biology of Hibernating Woodchucks .............. 212 Bone Preservation of Hibernators and the Implications of this Work ..... 217 Future Clinical and Evolutionary Research ............................................ 220 REFERENCES ................................................................................................. 224 iv LIST OF FIGURES Figure Page 1.1 The woodchuck (Marmota monax) in its active state and hibernating. ................................................................................................ 4 1.2 Intraperitoneal temperature of a woodchuck (M8) during the hibernation season 2009-2010 ..................................................................................... 4 1.3 A sagittal view of a woodchuck in September of the prehibernation season in 2009 and again in April of the posthibernation season in 2010 ........................................................................................................... 8 1.4 Wild woodchuck (CR8) implanted with an intraperitoneal body temperature logger and maximum daily ambient temperature in 2009-2010 ................................................................................................ 11 1.5 A woodchuck burrow temperature compared to outside air temperature during the hibernation season of 2011-2012 ....................... 13 1.6 Pattern of bone loss/maintenance in non-hibernating and hibernating animals during extensive inactivity ........................................................... 15 2.1 Gait diagram of a woodchuck trotting....................................................... 29 2.2 The symmetrical and asymmetrical gaits used by woodchucks with corresponding gait diagrams .................................................................... 31 2.3 A locomotion trial and the resulting data .................................................. 42 2.4 Computed tomography scans were taken of the diaphyses of the tibia, radius, and ulna approximating 50% of the length of the bone ............................................................................................... 48 2.5 Lateral radiograph of a woodchuck’s forelimb demonstrating measurements collected for estimating stresses of the ulna at maximum vertical force ............................................................................................ 50 v LIST OF FIGURES (Continued) Figure Page 2.6 Observed frequencies of symmetrical and asymmetrical gait types used by five individual woodchucks before and after hibernation ............................................................................................... 58 2.7 The range of symmetrical and asymmetrical gaits of five woodchucks ...................................................................................... 61 2.8 Speed did not differ significantly between seasons, but was significantly different between individual woodchucks by season ............ 63 2.9 Individual woodchuck fore and hindlimb duty factors were significantly different between seasons ........................................... 63 2.10 Maximum vertical force (FV) was significantly greater only in the forelimbs in the posthibernation season................................................... 66 2.11 Average compressive stress in the radius, ulna, and tibia of woodchucks was not dependent on season ............................................ 68 2.12 Both caudal and cranial bending strains in the tibia were significantly reduced in woodchucks following hibernation .......................................... 68 2.13 Seasonal average bending strains in the forearm of woodchucks .......... 69 3.1 QµCT scan locations for the long bones and mandibles of woodchucks ............................................................................................ 85 3.2 Annual variation in cortical density and mandibular resistance to bending in woodchucks............................................................................ 92 3.3 Annual variation in metaphyseal trabecular densities and bone area fraction (B.Ar/T.Ar) in woodchucks. ......................................................... 93 3.4 Relative diaphyseal cortical area and metaphyseal cortical density tended to be larger in each bone following hibernation ............... 96 vi LIST OF FIGURES (Continued) Figure Page 3.5 Seasonal differences in diaphyseal cortical density between adult and subadult woodchucks ........................................................................ 98 4.1 Longitudinal computed tomography scoutview of the femur, tibia, and humerus .......................................................................................... 125 4.2 Cortical density of tibial diaphyses significantly increased between all three seasons in a longitudinal study of captive, adult woodchucks ...... 134 4.3 There were no significant seasonal differences in cortical area or moments of inertia in the tibial diaphyses of captive, adult woodchucks ..........................................................................................
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