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University of California Santa Cruz Fur Versus Blubber: A UNIVERSITY OF CALIFORNIA SANTA CRUZ FUR VERSUS BLUBBER: A COMPARATIVE LOOK AT MARINE MAMMAL INSULATION AND ITS METABOLIC AND BEHAVIORAL CONSEQUENCES A dissertation submitted in partial satisfaction of the requirements for the degree of DOCTOR OF PHILOSOPHY in ECOLOGY AND EVOLUTIONARY BIOLOGY by Heather Elizabeth Mostman Liwanag December 2008 The dissertation of Heather Elizabeth Mostman Liwanag is approved: _________________________________ Professor Terrie M. Williams, Chair _________________________________ Professor Daniel P. Costa _________________________________ Professor Annalisa Berta _________________________________ Lisa C. Sloan Vice Provost and Dean of Graduate Studies Copyright © by Heather Elizabeth Mostman Liwanag 2008 TABLE OF CONTENTS page LIST OF FIGURES………………………………………………………………….vii LIST OF TABLES…………………………………………………………………….x ABSTRACT……………………………………………………………………….....xi ACKNOWLEDGEMENTS………………………………………………………….xv INTRODUCTION Introduction……………………………………………………………………1 References……………………………………………………………………..7 CHAPTER 1. Morphological and thermal properties of mammalian insulation: implications for the evolutionary transition to an aquatic lifestyle. Abstract………………………………………………………………………11 Introduction…………………………………………………………………..12 Materials and Methods……………………………………………………….14 Fur and Blubber Sampling…………………………………………...14 Fur Characteristics…………………………………………………...15 Blubber Characteristics………………………………………………20 Thermal Conductivity………………………………………………..23 Statistical Analyses…………………………………………………..25 Results………………………………………………………………………..26 Fur Characteristics…………………………………………………...26 Blubber Characteristics………………………………………………32 iii Total insulation………………………………………………………36 Discussion……………………………………………………………………37 Modification of fur for aquatic living………………………………..37 The evolutionary transition to blubber……………………………….41 Ecological and evolutionary implications……………………………46 Tables and Figures…………………………………………………………...51 References…………………………………………………………………..102 Appendix……………………………………………………………………112 CHAPTER 2. The effects of water temperature on the energetic costs of juvenile and adult California sea lions (Zalophus californianus): The importance of recycling endogenous heat during activity. Abstract……………………………………………………………………..121 Introduction…………………………………………………………………122 Materials and Methods……………………………………………………...125 Animals……………………………………………………………..125 Experimental protocol……………………………………………...126 Oxygen consumption……………………………………………….127 Core temperature……………………………………………………129 Statistical analyses and calculations………………………………..130 Results………………………………………………………………………132 Resting Metabolism and Thermal Neutral Zone……………………132 Core Temperature…………………………………………………..133 Activity Thermogenesis…………………………………………….134 iv Discussion…………………………………………………………………..136 Thermal capabilities of the California sea lion……………………..136 Thermal limitations in juvenile sea lions…………………………...138 The effect of locomotor activity on thermal responses……………..140 Tables and Figures………………………………………………………….145 References…………………………………………………………………..157 CHAPTER 3. Energetic costs and thermoregulation in northern fur seal (Callorhinus ursinus) pups: The importance of behavioral strategies for thermal balance in furred marine mammals. Abstract……………………………………………………………………..162 Introduction…………………………………………………………………163 Materials and Methods……………………………………………………...167 Animals……………………………………………………………..167 Protocol……………………………………………………………..167 Oxygen consumption……………………………………………….168 Determination of the thermal neutral zone…………………………169 Behavioral analyses………………………………………………...170 Statistical analyses………………………………………………….171 Results………………………………………………………………………172 Resting Metabolism and Thermal Neutral Zone……………………172 Jughandling Metabolism……………………………………………173 Grooming Metabolism……………………………………………...175 v Effects of water temperature on behavior…………………………..175 Effects of feeding on behavior……………………………………...176 Discussion…………………………………………………………………..177 Thermal capabilities of northern fur seal pups……………………..177 The effects of behavioral strategies on thermal responses.................180 The effects of ingested prey items on thermal responses…………..183 Conclusions…………………………………………………………185 Tables and Figures………………………………………………………….187 References…………………………………………………………………..203 vi LIST OF FIGURES page CHAPTER 1 FIGURE 1. Conductivity chamber, showing placement of thermocouples relative to the sample and standard material…………………………………………….56 FIGURE 2. Carnivore phylogeny used for evolutionary comparisons……………...58 FIGURE 3. Scanning electron micrographs of representative hairs from terrestrial and marine carnivores, showing the cuticular scale patterns………………...60 FIGURE 4. Elongation (maximum length / maximum width) of the cuticular scales of carnivore guard hairs and underhairs……………………………………...71 FIGURE 5. Circularity (minimum diameter / maximum diameter) of carnivore guard hairs and underhairs………………………………………………………….73 FIGURE 6. Lengths of carnivore guard hairs and underhairs………………………75 FIGURE 7. Fur density and blubber thickness among carnivores…………………..77 FIGURE 8. Fur densities among otariid species, with a cladogram illustrating the evolutionary relationships among the species………………………………..79 FIGURE 9. Character evolution of guard hair circularity among pinniped species, with the polar bear as an outgroup…………………………………………...81 FIGURE 10. Character evolution of guard hair length and underhair length among pinniped species, with the polar bear as an outgroup………………………..83 FIGURE 11. Character evolution of fur density among pinniped species, with the polar bear as an outgroup…………………………………………………….86 FIGURE 12. Amount of air trapped in the fur and lost during diving for the pelts of eight pinniped species………………………………………………………..88 FIGURE 13. Height of guard hairs and underhairs for pinniped pelts when dry, immersed, and under hydrostatic pressure…………………………………...90 FIGURE 14. Percent lipid content (by weight) of pinniped blubber………………..92 vii FIGURE 15. Change in thermal conductivity with lipid content of blubber for phocids, sea lions, and fur seals……………………………………………...94 FIGURE 16. Percent composition of fatty acid types in pinniped blubber…………96 FIGURE 17. Thermal resistance of the total insulation (in m2·°C·W-1) in relation to body mass (in kg) for carnivores………………………………………….....98 FIGURE 18. Schematic comparing relative body size and insulating layers of fur seals and sea lions…………………………………………………………..100 CHAPTER 2 FIGURE 1. Resting metabolism and core body temperature in relation to water temperatures for mature and immature California sea lions………………..147 FIGURE 2. Metabolic rate in relation to temperature for juvenile California sea lions at rest and while swimming at 1 m/s………………………………………..149 FIGURE 3. Metabolic heat production in relation to calculated swim velocity for four juvenile California sea lions…………………………………………...151 FIGURE 4. The effects of body mass on swimming metabolic rates for four juvenile California sea lions…………………………………………………………153 FIGURE 5. Comparison of predicted and measured metabolic heat production in relation to calculated swim velocity for juvenile sea lions…………………155 viii CHAPTER 3 FIGURE 1. Northern fur seal pup in the jughandle position, with one foreflipper held between both hind flippers above the water………………………………..191 FIGURE 2. Representative metabolic trace for a northern fur seal exhibiting the jughandling posture, illustrating the characteristic changes in metabolic rate associated with this behavior……………………………………………….193 FIGURE 3. Resting metabolic rate in relation to water temperature for three northern fur seal pups………………………………………………………………...195 FIGURE 4. Metabolic rate according to behavior for northern fur seal pups……..197 FIGURE 5. Percent time spent grooming in relation to water temperature for three northern fur seal pups……………………………………………………….199 FIGURE 6. Comparison of thermal liability of sea otter and pinniped species…...201 ix LIST OF TABLES page INTRODUCTION TABLE 1. Fur vs. Blubber……………………………………………………………5 CHAPTER 1 TABLE 1. Hair, pelt, and full sculp samples analyzed in the present study………..51 TABLE 2. Thermal conductivities of pelts and blubber layers……………………..54 TABLE A1. Species means ± 1SD for hair circularity from the present study……112 TABLE A2. Species means for hair length from the present study and published sources………………………………………………………………………113 TABLE A3. Species means ± 1 SD for fur density from the present study and published sources…………………………………………………………...115 TABLE A4. Species means ± 1 SD (by age class) for blubber thickness, from the present study and published sources………………………………………..117 TABLE A5. Species means ± 1 SD for blubber and subcutaneous fat lipid content, from the present study and published sources……………………………...120 CHAPTER 2 TABLE 1. Body mass, resting metabolic rate, and lower critical temperatures of the California sea lions used in this study………………………………………145 CHAPTER 3 TABLE 1. Body mass, lower critical temperatures, and metabolic rates for northern fur seal pups………………………………………………………………...187 TABLE 2. Lower critical temperatures (TLC) for sea otters and pinnipeds resting in water………………………………………………………………………...189 x FUR VERSUS BLUBBER: A COMPARATIVE LOOK AT MARINE MAMMAL INSULATION AND ITS METABOLIC AND BEHAVIORAL CONSEQUENCES Heather Elizabeth Mostman Liwanag ABSTRACT This research compares the use of fur and blubber as insulation in mammals, with a focus on the otariids (fur seals and sea lions) and the transition of mammals to aquatic living. The otariids represent the only mammalian family to include both types
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