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University of California Santa Cruz UNIVERSITY OF CALIFORNIA SANTA CRUZ Bioenergetics of marine mammals: the influence of body size, reproductive status, locomotion and phylogeny on metabolism A dissertation submitted in partial satisfaction of the requirements for the degree of DOCTOR OF PHILOSOPHY in ECOLOGY AND EVOLUTIONARY BIOLOGY by Jennifer L. Maresh June 2014 The Dissertation of Jennifer L. Maresh is approved: Professor Terrie M. Williams, Chair Professor Daniel P. Costa Professor Daniel E. Crocker Tyrus Miller Vice Provost and Dean of Graduate Studies Copyright © by Jennifer L. Maresh 2014 Table of Contents List of Figures . vi List of Tables . xiii Abstract . xvi Acknowledgements . xviii 1 Introduction 1 1.1 Broad context . 1 1.2 Dissertation outline . 3 2 Free-swimming northern elephant seals have low field metabolic 6 rates that are sensitive to an increased cost of transport 2.1 Introduction . 8 2.2 Methods . 12 2.2.1 Experimental design and animal handling . 12 2.2.2 Data collection and processing: behavior . 13 2.2.3 Data collection and processing: energetics . 15 2.2.4 Data analysis . 18 2.3 Results . 21 2.3.1 Effects of increased transport costs on metabolism, diving behavior and swimming mechanics . 21 2.3.2 Predicting costs during standard locomotion . 23 2.4 Discussion . 27 2.4.1 Ecological implications: field metabolic rates and locomotion . 28 iii 2.4.2 Basal metabolic rates: marine mammals and juveniles . 30 2.4.3 Altered behavior at sea . 32 2.4.4 Predicting the energy requirements of free-ranging animals . 34 2.4.5 Conclusions . 35 3 Summing the strokes: extreme energy economy in a large marine 50 carnivore 3.1 Introduction . 53 3.2 Methods . 56 3.2.1 Flipper stroking data . 56 3.2.2 Energetics data . 58 3.2.3 Statistical analysis . 61 3.3 Results . 62 3.3.1 Energy expenditure . 62 3.3.2 Foraging success and energy budgets . 65 3.3.3 Seals with added drag . 67 3.4 Discussion . 68 3.4.1 Energy economy and the effects of pregnancy . 68 3.4.2 Energy budgets . 73 3.4.3 Prey requirements . 75 3.4.4 Disruption of routine swimming behaviors . 77 3.4.5 Conclusions . 78 4 One marine mammal is not like the other: sampling bias inflates 93 perceptions of metabolic energy demand in aquatic carnivores 4.1 Marine mammal energetics . 94 iv 4.1.1 Sampling bias . 100 4.1.2 Extrapolated estimates . 101 4.2 The case for carnivory: Are marine mammals really that different? . 102 4.2.1 “Basal” metabolic rate . 105 4.2.2 Field metabolic rate . 107 4.3 Predicting metabolic energy demand for the average marine mammal . 109 4.4 Predicting metabolic energy demand for the individual marine mammal . 110 4.5 Conclusions . 112 4.6 Datasets & methods . 114 5 Synthesis 124 5.1 Elephant seals and disturbance . 124 5.2 Marine mammals and paradigms . 126 5.3 New questions . 127 Appendices 130 A.1 Basal metabolic rate: eutherian mammals . 130 A.1.1 BMR determinations . 131 A.1.2 Data sources . 170 A.2 Field metabolic rate: eutherian mammals . 198 A.2.1 FMR determinations . 199 A.2.2 Data sources . 205 Bibliography 216 v List of Figures 2.1 Haul-out (Año Nuevo) and release (Hopkins) sites of translocated seals are approximately 50 km apart across the Monterey Bay. Surface tracks of one homing seal during both trips are shown as an example. For this seal, Trip 1 was under the control treatment, while Trip 2 was under the added drag treatment. Only portions of the tracks representing transit across the bay (hatched) were used in comparisons of diving behavior and transit rates. 37 2.2 A comparison of dive types shows putative (A) foraging and (B) transit behaviors during similar timeframes for two different translocations. The top figure was taken from the dive record of seal #6 during her second trip, which included a large proportion of foraging dives (24%) compared to all other translocations (mean = 1.5 ± 0.02%). The bottom figure shows a more typical translocation dive record, with relatively deep u- and v-shaped transiting dives over the canyon flanked by shallow, benthic dives where the seal is following the bottom topography of the Monterey Bay. 38 2.3 Total number of flipper strokes increased linearly with total time spent at sea (entire measurement period). This relationship was similar for seals regardless of treatment and can be described by the equation y = 38629x – 10331 (r2 = .97, F = 330.3, p < 1,7 .0001). 39 2.4 Total at-sea mass-specific energy expenditure increased linearly with total number of flipper strokes for seals swimming normally and for seals swimming with added drag. This relationship differed between treatments so the regression line is vi for control seals only and can be described by the equation y = 0.0039x – 87.62 ( r2 = .98, F = 342.1, p < .001). 40 1,6 2.5 Total (A) and net (B) stroking costs had a tendency to decrease linearly with mass, although these relationships were not statistically significant. This relationship differed between treatments so the regression lines are shown for control seals only. 41 2.6 Total at-sea mass-specific energy expenditure increased linearly with time spent at sea. This relationship was similar for seals regardless of treatment and can be described by the equation y = 163.0x – 142.4 ( r2 = .98, F = 2741, p < .0001). 42 1,6 3.1 Northern elephant seal mother with (A) young pup (1-2 d) and (B) pup just before weaning (25-28 d). Photo credits: D. Costa, M. Fowler. 80 3.2 Mass-specific field metabolic rates of northern elephant seals based on total number of flipper strokes executed during their foraging migrations, as a function of mass. Filled circles indicate seals carrying added drag during their short migrations. See text for equations. 81 3.3 Field metabolic rates of northern elephant seals compared to Kleiber (1975) predictions of mammalian basal metabolic rate (BMR) (dashed red line) and Boyd (2002) predictions of marine mammal field metabolic rate (FMR) (dashed grey line), as a function of mass. Compared to seals during their short migration, vii seals of similar average body mass had 23% lower FMRs during the long migration according to the equation FMR = 19.5M + 14389. 82 LT 3.4 Flipper stroke rates were higher for seals swimming normally during the short foraging trip (N = 13) than during the long foraging trip (N = 7). In comparison, seals swimming with added drag during their short trips (N = 3) stroked consistently faster than normally swimming seals during the same time (Welch two- sample t-test, t = -9.7674, df = 7.471, p < 0.001). Dark horizontal bars represent median (50 th percentile) values while the lower and upper limits of the boxes represent the 25 th and 75 th percentiles, respectively. Whiskers correspond to the 1.5 interquartile range, and points represent outliers. 83 3.5 Partitioning of ingested energy among work (grey tones) and production (warm tones) costs in foraging elephant seals. Absolute costs for each seal are shown in the white panels (A), while proportions of total costs are averaged across the three groups in the grey panel (B), where ST = seals during the short foraging trip, LT = seals during the long foraging trip, and DG = seals with added drag during the short trip. Within each group, seals are listed from left to right in order of increasing body size. If locomotion costs in LT seals are similar to those of ST seals, basal metabolism would have to be suppressed by approximately 21% in pregnant seals (see text). 84 3.6 Average prey requirements of adult female northern elephant seals across an entire foraging migration as a function of prey item’s energetic density, assuming an average mass for each prey species. From left to right, prey items include squid (Octopoteuthis deletron , 0.20 kg, 3.08 MJ kg -1), Pacific hake viii (Merluccius productus , 0.32 kg, 3.43 MJ kg -1), Pacific herring (Clupea pallasii , 0.55 kg, 5.44 MJ kg -1) and lantern fish (F. myctophidae, 0.02 kg, 11.88 MJ kg -1). Numbers above bars indicate the number of that particular prey item that would need to be captured per foraging dive in order to support at-sea energy expenditure, assuming a simple, monophagous diet. The diet of elephant seals, while unknown, likely includes a mix of these and other species of different sizes, and therefore true prey capture numbers and rates will vary from this idealized depiction. Sources: (Beamish & McFarlane 1985; Clarke et al. 1985; Ohizumi et al. 2003; NOAA-OPR 2008). 86 3.7 Flipper stroking follows a predictable pattern along the course of each dive. The top panel shows one foraging dive during the short migration of seal X851, where depth is shown with.
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