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The Development and Improvement of Instructions FEEDING BIOMECHANICS & CRANIODENTAL MORPHOLOGY IN OTTERS (LUTRINAE) A Dissertation by LORI LYNN TIMM Submitted to the Office of Graduate Studies of Texas A&M University in partial fulfillment of the requirements for the degree of DOCTOR OF PHILOSOPHY Chair of Committee, Christopher Marshall Committee Members, Bernd Würsig Randall Davis Thomas DeWitt Head of Department, Michael Masser August 2013 Major Subject: Wildlife and Fisheries Sciences Copyright 2013 Lori Lynn Timm ABSTRACT Variation in terrestrial mammalian craniodental morphology and skull shape is known to constrain feeding performance, which in turn influences dietary habits and ultimately fitness. Otters have evolved two feeding specializations: underwater raptorial capture of prey (mouth-oriented) and capture of prey by hand (hand-oriented), which likely correspond to craniodental morphology and bite performance. However, feeding biomechanics and performance data for otters, aquatic mustelids that consume prey above water, are sparse. The first goal of the study was to investigate the relationship between feeding morphology and bite performance between two mouth-oriented piscivores (giant river otters and North American river otters) and two hand-oriented invertebrate specialists (sea otters and Asian small-clawed otters) using morphometric approaches. The second goal was to investigate fluctuating asymmetry in the cranium of otters. The third goal was to characterize feeding mechanisms (kinematics and jaw musculature) and role of bite performance in the trophic ecology of sea otters. Mouth- oriented piscivores possessed longer skulls and mandibles, with jaws designed for increased velocity at the expense of bite capability. Hand-oriented possessed more blunt skulls and mandibles designed for increased bite capability. Sea otters displayed a greater degree of fluctuating asymmetry of the skull, which is likely linked to environmental stresses. Bite performance and durophagous feeding behavior in sea otters was characterized in detail in the feeding kinematics. Estimated bite forces of sea otters were large enough to crush all size classes of butter and littleneck clams tested in ii the lab. However, sea otters are size selective predators and generally choose bivalves of small to medium size. Medium sized butter and littleneck clams required an intermediate breaking force, and are buried at a shallower depth than larger clams. Clams requiring an intermediate breaking force could decrease consumption time, thus overall handling time. iii ACKNOWLEDGMENTS I would first like to thank my committee chair, Dr. Christopher Marshall, for this opportunity and for all of his advice and support throughout this whole process. I appreciate his insight, guidance, and support throughout this research experience! I also appreciate all of his guidance in finding employment opportunities. To my committee members, Dr. Bernd Würsig, Dr. Randall Davis, and Dr. Thomas DeWitt, thank you for your continuous support and guidance. Dr. Würsig, your knowledge of otter behaviors and keystone species theory proved to be of great benefit! Dr. Davis, thank you for letting me do my kinematic study at the field camp in Simpson Bay. It was an experience I will never forget! Dr. DeWitt, thank you for all of your help and patience with the statistical analysis of traditional and geometric morphometrics. I appreciate the long hours you put in teaching me the geometric methodology with tpsDig, excel, and the statistical analysis in JMP. I also want to extend my gratitude to the kind people at the Burk Museum of Natural History (Seattle, Washington), Smithsonian National Museum of Natural History (Washington, D.C.), and the American Museum of Natural History (New York, New York) for allowing me access to all of the otter specimens for my research. Also, thank you to Nicole Hardy at the Audubon Aquarium of the Americas in New Orleans for allowing me to conduct my captive kinematics study with Buck and Emma. I want to thank the following for financial support: W.B. Davis Endowed Scholarship (Texas A&M University), Lerner-Gray Fund for Marine Research iv (American Museum of Natural History), Erma Lee and Luke Mooney Graduate Travel Grants, GGSA Micro and Mini Grants (Texas A&M University), and Marb-Mini Grants (Texas A&M University). Finally, I would like to give sincere thanks to my family and friends for their love, continuous support, and encouragement throughout this long process. Thank you Mom and Dad for all of the advice, encouraging words, and support! v TABLE OF CONTENTS Page ABSTRACT .............................................................................................................. ii ACKNOWLEDGMENTS ......................................................................................... iv TABLE OF CONTENTS .......................................................................................... vi LIST OF FIGURES ................................................................................................... viii LIST OF TABLES .................................................................................................... x CHAPTER I INTRODUCTION .......................................................................... 1 Evolution of Otters .............................................................................................. 1 Feeding Adaptations and Dietary Differences of Otters ..................................... 12 Overall Research Objectives ............................................................................... 14 CHAPTER II CRANIAL MORPHOMETRICS ................................................... 15 Introduction ........................................................................................................ 15 Objectives and Hypotheses ................................................................................. 20 Materials and Methods ........................................................................................ 21 Results…………………………………………………………………………... 31 Discussion………………………………………………………………………. 45 CHAPTER III ESTIMATED BITE FORCE OF OTTERS AND THE PHYSIOLOGY OF JAW MUSCULATURE IN SEA OTTERS ............................. 58 Introduction... ...................................................................................................... 58 Objectives and Hypotheses ................................................................................. 65 Materials and Methods ........................................................................................ 66 Results…………. ................................................................................................ 73 Discussion………………………………………………………………………. 78 CHAPTER IV FEEDING KINEMATICS ............................................................. 86 Introduction... ...................................................................................................... 86 Objectives and Hypotheses ................................................................................. 90 Materials and Methods ........................................................................................ 90 vi Results…………. ................................................................................................ 95 Discussion………………………………………………………………………. 99 CHAPTER V BREAKING FORCE OF BIVALVES AND OVERALL HANDLING TIME OF PREY IN ALASKAN SEA OTTERS (ENHYDRA LUTRIS KENYONI) IN SIMPSON BAY .................................................................. 105 Introduction.….. .................................................................................................. 105 Objectives and Hypotheses ................................................................................. 110 Materials and Methods ........................................................................................ 111 Results…………. ................................................................................................ 114 Discussion………………………………………………………………………. 125 CHAPTER VI CONCLUSION.. ........................................................................... 134 Overall Discussion .............................................................................................. 134 REFERENCES .......................................................................................................... 139 vii LIST OF FIGURES FIGURE Page 1-1 Phylogenetic relationships of otters (Koepfli et al., 2008) ......................... 8 2-1 Cranial morphometric variables. Image is of giant river otter (Pteronura Brasiliensis) ........................................................................................ 22 2-2 Cranial morphometric variables for mandible. Image is of giant river otter (Pteronura brasiliensis).............................................................. 22 2-3 Homologous landmarks for geometric morphometrics .............................. 28 2-4 Discriminant analysis with log10 transformed skull morphometric variables ............................................................................................ 32 2-5 Discriminant function analysis with occlusal surface area (OSA) of postcanine dentition on upper left jaw and condylobasal length (CBL) ................................................................................................ 33 2-6 Discriminant analysis of mandible variables ............................................. 34 2-7 Discriminant analysis with log10 transformed skull morphometric variables …. .....................................................................................
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