David Rosen

abstract
The increased size and enhanced compliance of the aortic bulb—the enlargement of the ascending aorta—are believed to maintain blood flow in pinnipeds during extended periods of diastole induced by diving bradycardia. The aortic bulb has been described ex vivo in several species of pinnipeds, but in vivo measurements are needed to investigate the relationship between structure and function. We obtained ultrasound images using electrocardiogramgated transesophageal echocardiography during anesthesia and after atropine administration to assess the relationship between aortic bulb anatomy and cardiac function (heart rate, stroke volume, cardiac output) in northern fur seals (Callorhinus ursinus) and Steller sea lions (Eumetopias jubatus). We observed that the aortic bulb in northern fur seals and Steller sea lions expands during systole and recoils over the entire diastolic period indicating that blood flow is maintained throughout the entire cardiac cycle as expected. The stroke volumes we measured in the fur seals and sea lions fit the values predicted based on body size in mammals and did not change with increased heart rates, suggesting that greater stroke volumes are not needed for aortic bulb function. Overall, our results suggest that peripheral vasoconstriction during diving is sufficient to modulate the volume of blood in the aortic bulb to ensure that flow lasts over the entire diastolic period. These results indicate that the shift of blood into the aortic bulb of pinnipeds is a fundamental mechanism caused by vasoconstriction while diving, highlighting the importance of this unique anatomical adaptation.

abstract
The enlarged size of the aortic bulb is thought to enhance the ability of marine mammals to remain underwater for extended periods. However, a convincing link between aortic bulb size and diving capacity has not been established. Using new and existing data, we examined the relationships between body size, maximum and routine dive duration, and aortic bulb size of pinnipeds. Comparisons among seven species of pinnipeds showed that the diameter of the aortic bulb increases allometrically with body mass (aortic bulb diameter = 0.58 x body mass0.41). We also found a linear relationship between routine dive duration and relative aortic bulb diameter (routine dive duration = 0.20 x relative aortic bulb diameter – 3.30), but no apparent relationship with maximum dive duration. Our results indicate that relative aortic bulb diameter influences diving capacity, providing further evidence that the aortic bulb is an adaptation to diving. Specifically, the relative diameter of the aortic bulb partially determines how long pinnipeds can routinely remain underwater. This has implications for the ability of different species of marine mammals to adapt to projected environmental changes and effectively forage or evade threats in altered habitats.

abstract
Growth of structural mass and energy reserves influences individual survival, reproductive success, and population and species life history. Metrics of structural growth and energy storage of individuals are often used to assess population health and reproductive potential, which can inform conservation. However, the energetic costs of tissue deposition for structural growth and energy stores and their prioritization within bioenergetic budgets are poorly documented. This is particularly true across marine mammal species as resources are accumulated at sea, limiting the ability to measure energy allocation and prioritization. We reviewed the literature on marine mammal growth to summarize growth patterns, explore their tissue compositions, assess the energetic costs of depositing these tissues, and explore the tradeoffs associated with growth. Generally, marine mammals exhibit logarithmic growth. This means that the energetic costs related to growth and tissue deposition are high for early postnatal animals, but small compared to the total energy budget as animals get older. Growth patterns can also change in response to resource availability, habitat, and other energy demands, such that they can serve as an indicator of individual and population health. Composition of tissues remained consistent with respect to protein and water content across species; however, there was a high degree of variability in the lipid content of both muscle (0.1-74.3%) and blubber (0.4-97.9%) due to the use of lipids as energy storage. We found that relatively few well-studied species dominate the literature, leaving data gaps for entire taxa, such as beaked whales. The purpose of this review was to identify such gaps, to inform future research priorities, and to improve our understanding of how marine mammals grow and the associated energetic costs.

keywords     growth, bioenergetics, body composition, northern fur seals

abstract
Between 2012 and 2022, the Vancouver Aquarium Marine Mammal Rescue Centre sedated 110 harbor seal pups for physical examinations, diagnostic procedures, or treatment. A sedation protocol of butorphanol and midazolam (0.1– 0.2 mg/kg each) was administered via a single i.v. injection in 171 procedures. Of these, 21 pups were anesthetized only with the injectables, while supplemental isoflurane inhalation anesthesia by mask was provided during 58 procedures; 92 other animals required intubation for respiratory support due to apnea or to achieve a deeper plane of anesthesia to facilitate more invasive procedures. Of the 171 sedations, five were euthanized due to poor prognosis and six failed to recover. Maximum sedation, sufficient for intended procedure or anesthesia induction, was achieved within a mean of 8.5 ± 5.8 min for i.v. injection (n = 133). Sedation duration (drug administration to full recovery) without supplemental inhalation anesthesia had a mean of 30.2 min and ranged from 14 to 52 min (n = 13). When used in stabilized young harbor seals, administration of injectable butorphanol and midazolam proved to be an effective protocol to obtain safe and reliable sedation for physical examination, minimally invasive diagnostic procedures, or as a premedication for general anesthesia.

keywords     harbour seal, seadtion, marine mammal medicine, husbandry

abstract
Bioenergetics is the study of how animals achieve energetic balance. Energetic balance results from the energetic expenditure of an individual and the energy they extract from their environment. Ingested energy depends on several extrinsic (e.g prey species, nutritional value and composition, prey density and availability) and intrinsic factors (e.g. foraging effort, success at catching prey, digestive processes and associated energy losses, and digestive capacity). While the focus in bioenergetic modelling is often on the energetic costs an animal incurs, the robust estimation of an individual’s energy intake is equally critical for producing meaningful predictions. Here, we review the components and processes that affect energy intake from ingested gross energy to biologically useful net energy (NE). The current state of knowledge of each parameter is reviewed, shedding light on research gaps to advance this field. The review highlighted that the foraging behaviour of many marine mammals is relatively well studied via biologging tags, with estimates of success rate typically assumed for most species. However, actual prey capture success rates are often only assumed, although we note studies that provide approaches for its estimation using current techniques. A comprehensive collation of the nutritional content of marine mammal prey species revealed a robust foundation from which prey quality (comprising prey species, size and energy density) can be assessed, though data remain unavailable for many prey species. Empirical information on various energy losses following ingestion of prey was unbalanced among marine mammal species, with considerably more literature available for pinnipeds. An increased understanding and accurate estimate of each of the components that comprise a species NE intake are an integral part of bioenergetics. Such models provide a key tool to investigate the effects of disturbance on marine mammals at an individual and population level and to support effective conservation and management.

keywords     marine mammals, energy intake, bioenergetics

abstract
Background: Animal movement data are regularly used to infer foraging behaviour and relationships to environmental characteristics, often to help identify critical habitat. To characterize foraging, movement models make a set of assumptions rooted in theory, for example, time spent foraging in an area increases with higher prey density. Methods: We assessed the validity of these assumptions by associating horizontal movement and diving of satellite‐ telemetered ringed seals (Pusa hispida)—an opportunistic predator—in Hudson Bay, Canada, to modelled prey data and environmental proxies. Results: Modelled prey biomass data performed better than their environmental proxies (e.g., sea surface temperature) for explaining seal movement; however movement was not related to foraging effort. Counter to theory, seals appeared to forage more in areas with relatively lower prey diversity and biomass, potentially due to reduced foraging efficiency in those areas. Conclusions: Our study highlights the need to validate movement analyses with prey data to effectively estimate the relationship between prey availability and foraging behaviour.

abstract
Sea otters (Enhydra lutris) are known ecosystem engineers that have significant impacts on their kelp forest and rocky intertidal communities due to their high levels of food intake. Quantifying sea otter food biomass and energy intake is a valuable way to understand potential ecological impacts of sea otter populations on ecosystems and for predicting future population trends and potential for expansion. While detailed, fine-scale, age-specific food intake is difficult to quantify in wild sea otters, there is a wealth of potential information available from otters under human care. This study used food and energy intake data from husbandry records of 10 sea otters collected over three decades at the Vancouver Aquarium. Within these husbandry records, daily food biomass intake and body mass measurements were recorded and converted to annual average food mass and gross energy intake (GEI). Age-, sex-, and mass-specific trends were also observed. Young sea otters had the highest relative ingested food mass, equivalent to ~26% of body mass, which decreased to ~20% in adult otters. Young otters similarly had the high- est mass-specific GEI, where measures from near birth to year 1 were ~40% higher than at year 3, the age of sexual and physical maturity. There were also key differences in trends between sexes. Captive adult male sea otters were 25 to 42% larger than females and their GEI was 23 to 58% higher, although mass-specific GEI was almost identical for male and non-reproductive female otters at all ages, plateauing at ~650 kJ kg-1 d-1. Despite high levels of ingested food mass, GEI was only 5 to 15% higher than for other captive marine mammals and was comparable to previous estimates for wild sea otters. These estimates of ingested food mass and energy intake requirements are valuable when modelling the ecological impact of sea otter populations and for considering the potential effects of future environmental changes.

keywords     sea otters, Enhydra lutris, food intake, energetics, nutrition, growth, body mass

abstract
OBJECTIVE To establish normal values for pre- and post-prandial bile acids and protein C in Pacific harbor seal (Phoca vitulina richardsi) pups. ANIMALS 45 harbor seals undergoing rehabilitation at the Vancouver Aquarium Marine Mammal Rescue Centre, 0 to 16 weeks, and deemed healthy aside from malnutrition or maternal separation. PROCEDURES Venous blood was collected from the intervertebral extradural sinus in fasted seals and again 2 hours after a fish meal. RESULTS The reference interval (90% CL, confidence limit) for pre-prandial (fasting) bile acids was 17.2 μmol/L to 25.4 μmol/L, post-prandial bile acids were 36.9 μmol/L to 46.4 μmol/L, and protein C was 72.3% to 85.4%, across ages. For comparison between developmental ages, pups were grouped into 3 age classes: < 14 days, 5 to 8 weeks, and 10 to 16 weeks. Age affected pre- and post-prandial bile acids; pups < 14 days had significantly higher pre-prandial bile acids (36.0 μmol/L ± 16.5 μmol/L; P < .0001) than other age groups and pups 5 to 8 weeks had significantly higher post-prandial bile acids (50.4 μmol/L ± 21.9 μmol/L; P < .001). Protein C was also affected by age, with seals < 14 days having significantly lower values (mean, 51.8% ± 16.7%; P < .0001). CLINICAL RELEVANCE This study established normal reference intervals for bile acids in harbor seal pups and offered a preliminary investigation into protein C in pinnipeds. The bile acid values from 0- to 16-week-old seal pups were well above established normal ranges for domestic species, highlighting the utility of age- and species-specific reference ranges. The values presented here and the differences across age classes will aid clinicians in accurately diagnosing hepatobiliary disease in harbor seal pups.

keywords     harbor seal pups, health, bile acids, Protein C

abstract
Over the past several decades, scientists have constructed bioenergetic models for marine mammals to assess potential population-level consequences following exposure to a disturbance, stressor, or environmental change, such as under the Population Consequences of Disturbance (pCOD) framework. The animal’s metabolic rate (rate of energy expenditure) is a cornerstone for these models, yet the cryptic lifestyles of marine mammals, particularly cetaceans, have limited our ability to quantify basal (BMR) and field (FMR) metabolic rates using accepted ‘gold standard’ approaches (indirect calorimeter via oxygen consumption and doubly labeled water, respectively). Thus, alternate methods have been used to quantify marine mammal metabolic rates, such as extrapolating from known allometric relationships (e.g. Kleiber’s mouse to elephant curve) and developing predictive relationships between energy expenditure and physiological or behavioral variables. To understand our current knowledge of marine mammal metabolic rates, we conducted a literature review (1900–2023) to quantify the magnitude and variation of metabolic rates across marine mammal groups. A compilation of data from studies using ‘gold standard’ methods revealed that BMR and FMR of different marine mammal species ranges from 0.2 to 3.6 and 1.1 to 6.1 x Kleiber, respectively. Mean BMR and FMR varied across taxa; for both measures odontocete levels were intermediate to higher values for otariids and lower values of phocids. Moreover, multiple intrinsic (e.g. age, sex, reproduction, molt, individual) and extrinsic (e.g. food availability, water temperature, season) factors, as well as individual behaviors (e.g. animal at water’s surface or submerged, activity level, dive effort and at-sea behaviors) impact the magnitude of these rates. This review provides scientists and managers with a range of reliable metabolic rates for several marine mammal groups as well as an understanding of the factors that influence metabolism to improve the discernment for inputs into future bioenergetic models.

abstract
Seals haul out of water for extended periods during the annual molt, when they shed and regrow their pelage. This behavior is believed to limit heat loss to the environment given increased peripheral blood flow to support tissue regeneration. The degree to which time in water, particularly during the molt, may affect thermoregulatory costs is poorly understood. We measured the resting metabolism of three spotted seals (Phoca largha), one ringed seal (Pusa hispida) and one bearded seal (Erignathus barbatus) during and outside the molting period, while resting in water and when hauled out. Metabolic rates were elevated in spotted and ringed seals during molt, but comparable in water and air for individuals of all species, regardless of molt status. Our data indicate that elevated metabolism during molt primarily reflects the cost of tissue regeneration, while increased haul out behavior is driven by the need to maintain elevated skin temperatures to support tissue regeneration.

keywords     Energetics, Thermoregulation, Molting physiology, Respirometry

abstract
Bioenergetic approaches are increasingly used to understand how marine mammal populations could be affected by a changing and disturbed aquatic environment. There remain considerable gaps in our knowledge of marine mammal bioenergetics, which hinder the application of bioenergetic studies to inform policy decisions. We conducted a priority-setting exercise to identify high-priority unanswered questions in marine mammal bioenergetics, with an emphasis on questions relevant to conservation and management. Electronic communication and a virtual workshop were used to solicit and collate potential research questions from the marine mammal bioenergetic community. From a final list of 39 questions, 11 were identified as key questions because they received votes from at least 50% of survey participants. Key questions included those related to energy intake (prey landscapes, exposure to human activities) and expenditure (field metabolic rate, exposure to human activities, lactation, time-activity budgets), energy allocation priorities, metrics of body condition and relationships with survival and reproductive success, and extrapolation of data from one species to another. Existing tools to address key questions include labeled water, animal-borne sensors, mark-resight data from long-term research programs, environmental DNA, and unmanned vehicles. Further validation of existing approaches and development of new methodologies are needed to comprehensively address some key questions, particularly for cetaceans. The identification of these key questions can provide a guiding framework to set research priorities, which ultimately may yield more accurate information to inform policies and better conserve marine mammal populations.

abstract
Estimates of prey and energy consumption are important for effective management and conservation of marine mammals and the ecosystems they inhabit. We used routinely collected husbandry data on body mass, food intake (kilo- grams), and energy intake (megajoules) from northern fur seals (Callorhinus ursinus) in zoological institutions to examine how these variables changed throughout the year, and with age, sex, and reproduction. Fur seals exhibited seasonal changes in all three variables, but the magnitude and timing of trends varied among age and sex groups. Notably, adult males exhibited rapid increases in body mass leading up to the breeding season. Fur seals were most efficient at converting energy intake to mass gain in the spring and least efficient in the fall. Intake increased into adulthood as animals grew in body mass. Sex-specific differences in intake were detectable early in development, likely related to size dimorphism. Pregnancy was energetically inexpensive compared with lactation, with food and energy intake rapidly increasing post parturition to values that were double those during early pregnancy. This study highlights the importance of accounting for different age, sex, and life history stages when estimating prey consumption of northern fur seals.

keywords     bioenergetic model, caloric intake, energetics, fatted male phenomenon, growth, lactation, otariids

abstract
Changes in Arctic ice conditions have raised concerns regarding potential impacts on energy expenditure and food requirements of walruses. Modelling the repercussions of environmental changes requires accurate species-specific measures of bioenergetic expenditures. This is particularly true for walruses, who have a unique anatomy and foraging ecology from other pinnipeds. This study measured resting metabolic rate (RMR) and subsurface swimming metabolism in two juvenile walruses over a 13-month period. The walruses had relatively low RMR compared to studies of other young pinnipeds. RMR was greater for the male than the female, as expected given his larger size; the reverse was true on a mass-specific basis. There was also considerable variability in RMR for each walrus during the year that could not be accounted for by changes in body mass. Metabolism while swimming was about twice RMR, and locomotor costs were higher than generally predicted for other marine mammals. The lower calculated swimming efficiency may reflect the fact that walruses are not “high velocity” pursuit predators. The estimates of metabolic expenditure obtained in this study for young walruses are invaluable for quantifying the energetic consequences of behavioral changes induced by environmental shifts in the wild.

keywords     bioenergetics, metabolism, swimming, walrus

abstract
This study quantified the effect of changes in prey intake on the growth of individual Steller sea lions. Data from 12 female sea lions subject to various experimental episodes of restricted food intake were used to produce an overall model predicting changes in growth rates from different levels of unpredicted reductions in energy intake. The resulting equation was robust across different types and levels of restriction, seasons, and age classes. This predictive relationship between changes in food intake and growth is invaluable for incorporating into bioenergetic models estimating the effects of environmental changes on wild Steller sea lions.

keywords     Steller sea lion, food intake, growth, body mass, energy intake, bioenergetics

abstract
Quantifying the energy needs of individual animals and understanding the relationship between food intake and physical growth are necessary to determine species-level food requirements and model potential responses to changing environmental conditions. To provide fine-scale information about developmental and seasonal patterns in the energetic requirements of Arctic phocid seals, we documented longitudinal changes in food intake, body mass, and standard length in four spotted seals (Phoca largha), three ringed seals (Pusa hispida), and two bearded seals (Erignathus barbatus). The seals were studied for up to 9 years in sub-Arctic and/or temperate climates while living under human care. Seals were fed using behavioral criteria that allowed their food intake and body mass to vary naturally. Gross energy intake (GEI) increased with age in all species, reaching a plateau as seals matured. GEI was greatest for the largest species (bearded seals) and lowest for the smallest (ringed seals). Mass-specific GEI declined with age, and was similar between spotted and ringed seals, with bearded seals consuming about half that of the smaller species. Overlaid upon long-term developmental changes were predictable seasonal cycles in food intake and body mass which became more pronounced as seals matured. Seasonal cycles in food intake and body mass did not always reflect simple cause-and-effect relationships. For example, seasonal peaks in food intake were regularly associated with simultaneous declines in body mass. The consistency of energy intake patterns, despite seals being maintained in semi-artificial conditions in different local climates, supports the hypothesis that seasonal oscillations are guided by underlying hormonal changes linked to key life history events and mediated by the physical environment. The described physiological patterns serve to highlight times of year when free-ranging Arctic seals may be more sensitive to environmental perturbations.

keywords     Phoca largha, Pusa hispida, Erignathus barbatus, food intake, caloric intake, body mass, growth, development, environmental conditions, nutrition

abstract
Pinniped hearts have been well described via dissection, but in vivo measurements of cardiac structure, function, and electrophysiology are lacking. Electrocardiograms (ECGs) were recorded under anesthesia from 8 Steller sea lions (Eumetopias jubatus), 5 northern fur seals (Callorhinus ursinus), and 1 walrus (Odobenus rosmarus) to investigate cardiac electrophysiology in pinnipeds. In addition, echocardiograms were performed on all 8 anesthetized Steller sea lions to evaluate in vivo cardiac structure and function. Measured and calculated ECG parameters included P‑wave, PQ, QRS, and QT interval durations, P‑, R‑, and T‑wave amplitudes, P‑ and T‑wave polarities, and the mean electrical axis (MEA). Measured and calculated echocardiographic parameters included left ventricular internal diameter, interventricular septum thickness, and left ventricular posterior wall thickness in systole and diastole (using M-mode), left atrium and aortic root dimensions (using 2D), and maximum aortic and pulmonary flow velocities (using pulsed wave spectral Doppler). ECG measurements were similar to those reported for other pinniped species, but there was considerable variation in the MEAs of Steller sea lions and northern fur seals. Echocardiographic measurements were similar to those reported for southern sea lions (Otaria flavenscens), including 5 out of 8 Steller sea lions having a left atrial to aortic root ratio < 1, which may indicate that they have an enlarged aortic root compared to awake terrestrial mammals. Isoflurane anesthesia likely affected some of the measurements as evidenced by the reduced fractional shortening found in Steller sea lions compared to awake terrestrial mammals. The values reported are useful reference points for assessing cardiac health in pinnipeds under human care.

abstract
Although the ability of marine mammals to lower heart rates for extended periods when diving is well documented, it is unclear whether marine mammals have electrophysiological adaptations that extend beyond overall bradycardia. We analyzed electrocardiographic data from 50 species of terrestrial mammals and 19 species of marine mammals to determine whether the electrical activity of the heart differs between these two groups of mammals. We also tested whether physiological state (i.e., anesthetized or conscious) affects electrocardiogram (ECG) parameters. Analyses of ECG waveform morphology (heart rate, P-wave duration, and PQ, PR, QRS, and QT intervals) revealed allometric relationships between body mass and all ECG intervals (as well as heart rate) for both groups of mammals and specific differences in ECG parameters between marine mammals and their terrestrial counterparts. Model outputs indicated that marine mammals had 19% longer P-waves, 24% longer QRS intervals, and 21% shorter QT intervals. In other words, marine mammals had slower atrial and ventricular depolarization, and faster ventricular repolarization than terrestrial mammals. Heart rates and PR intervals were not significantly different between marine and terrestrial mammals, and physiological state did not significantly affect any ECG parameter. On average, ECG interval durations of marine and terrestrial mammals scaled with body mass to the power of 0.21 (range: 0.19 - 0.23) rather than the expected 0.25—while heart rate scaled with body mass to the power of -0.22 and was greater than the widely accepted -0.25 derived from fractal geometry. Our findings show clear differences between the hearts of terrestrial and marine mammals in terms of cardiac timing that extend beyond diving bradycardia. They also highlight the importance of considering special adaptations (such as breath-hold diving) when analyzing allometric relationships.

keywords     ECG, electrocardiogram, marine mammal, heart rate, anesthesia, allometry, cardiac timing, comparative electrophysiology

abstract
Arctic seals, including spotted (Phoca largha), ringed (Pusa hispida), and bearded (Erignathus barbatus) seals, are directly affected by sea ice loss. These species use sea ice as a haul-out substrate for various critical functions, including their annual molt. Continued environmental warming will inevitably alter the routine behavior and overall energy budgets of Arctic seals, but it is difficult to quantify these impacts as their metabolic requirements are not well known—due in part to the difficulty of studying wild individuals. Thus, data pertaining to species-specific energy demands is urgently needed to better understand the physiological consequences of rapid environmental change. We used open-flow respirometry over a four-year period to track fine-scale, longitudinal changes in the resting metabolic rate (RMR) of four spotted, three ringed, and one bearded seal trained to participate in research. Simultaneously, we collected complementary physiological and environmental data. Species-specific metabolic demands followed expected patterns based on body size, with the largest species, the bearded seal, exhibiting the highest absolute RMR (0.48±0.04 L O2 min-1) and the lowest mass-specific RMR (4.10±0.47 ml O2 min-1 kg-1), followed by spotted (absolute: 0.33±0.07 L O2 min-1; mass-specific: 6.13±0.73 ml O2 min-1 kg-1) and ringed (absolute: 0.20±0.04 L O2 min-1; mass-specific: 7.01±1.38 ml O2 min-1 kg-1) seals. Further, we observed clear and consistent annual patterns in RMR that related to the distinct molting strategies of each species. For species that molted over relatively short intervals—spotted (33±4 days) and ringed (28±6 days) seals—metabolic demands increased markedly in association with molt. In contrast, the bearded seal exhibited a prolonged molting strategy (119±2 days), which appeared to limit the overall cost of molting as indicated by a relatively stable annual RMR. These findings highlight energetic trade-offs associated with different molting strategies and provide quantitative data that can be used to assess species-specific vulnerabilities to changing conditions.

keywords     Arctic seals, spotted seal, ringed seal, bearded seal, sea ice, molt, climate change, respirometry, resting metabolic rate, energetic trade-offs

abstract
Pinnipeds have specific macronutrient (protein, lipid) requirements to satisfy physiological functions, yet little is known about how diet characteristics affect macronutrient digestibility. We measured relative and absolute lipid and protein digestibility in six female northern fur seals (Callorhinus ursinus (Linnaeus 1758)) fed eight experimental diets composed variously of four prey species (Pacific herring (Clupea pallasii Valenciennes in Cuvier and Valenciennes 1847), walleye pollock (Gadus chalcogrammus Pallas 1814, formerly Theragra chalcogrammus (Pallas 1814)), capelin (Mallotus villosus (Müller 1776) and magister armhook squid (Berryteuthis magisterial (Berry 1913)). We quantified how digestibility was affected by proximate composition of the diet (%lipid or protein), levels of food mass and macronutrient intake, and tested for any potential benefit of multi-species diets. Overall, digestibility of both protein and lipid were high across diets, although macronutrient retention of lipids (96.0–98.4%) was significantly higher than protein (95.7–96.7%) for all but the two highest protein diets. Increased levels of protein intake resulted in increased protein retention, but decreased lipid digestibility. There was no evidence that mixed-species diets provide greater macronutrient digestibility over single-species diets. The results suggest that high to moderate lipid diets are more beneficial to northern fur seals as they lead to increased levels of lipid retention without large decreases in protein digestibility. This raises concerns that dietary factors may be contributing to the population declines of northern fur seals in the Bering Sea.

keywords     Northern fur seal, Callorhinus ursinus, diet composition, macronutrients, lipid digestibility, protein digestibility

abstract
Physiology places constraints on an animal’s ability to forage and those unable to adapt to changing conditions may face increased challenges to reproduce and survive. As the global marine environment continues to change, small, air-breathing, endothermic marine predators such as otariids (fur seals and sea lions) and particularly females and juveniles may experience increased difficulties in successfully obtaining adequate food resources. We explored whether physiological limits of female otariids may be innately related to body morphology (fur seals vs sea lions) and/or dictate foraging strategies (epipelagic vs mesopelagic or benthic). We conducted a systematic review of the increased body of literature since the original reviews of Costa et al. (2004) and Arnould and Costa (2006) on behavioural (dive duration and depth) and physiological (total body oxygen stores and diving metabolic rates) parameters. We also estimated calculated aerobic dive limit (cADL - estimated duration of aerobic dives) for species, and used simulations to predict the proportion of dives that exceeded the cADL. We then tested whether body morphology or foraging strategy were the primary predictors of these behavioural and physiological characteristics. We found that foraging strategy more than morphology was a better predictor of most parameters, including whether a species was more likely to exceed their cADL during a dive and the ratio of dive time to cADL. This suggests that benthic divers are more likely to be foraging at their physiological capacity. For species operating near their physiological capacity (regularly exceeding their cADL), the ability to switch strategies is limited as the cost of foraging deeper and longer is disproportionally high. It is proposed that some otariids may not have the ability to switch foraging strategies and so be unable adapt to a changing oceanic eco

keywords     otariid, aerobic dive limit, prey availability, meta analysis, diving

abstract
The Steller sea lion is the largest member of the Otariidae family and is found in the coastal waters of the northern Pacific Rim. Here, we present the Steller sea lion genome, determined through DNA sequencing approaches that utilized microfluidic partitioning library construction, as well as nanopore technologies. These methods constructed a highly contiguous assembly with a scaffold N50 length of over 14 megabases, a contig N50 length of over 242 kilobases and a total length of 2.404 gigabases. As a measure of completeness, 95.1% of 4104 highly conserved mammalian genes were found to be complete within the assembly. Further annotation identified 19,668 protein coding genes. The assembled genome sequence and underlying sequence data can be found at the National Center for Biotechnology Information (NCBI) under the BioProject accession number PRJNA475770.

keywords     Steller sea lion, genetics

abstract
This workshop assembled scientists and managers with technical expertise on seals, sea lions, and salmonids to identify and evaluate knowledge and uncertainties about the diets and population dynamics of pinnipeds (harbour seals, Steller sea lions, and California sea lions), as well as the impacts that pinnipeds may be having on salmonids in British Columbia and Washington State waters. The primary focal area was the Salish Sea, but included coastal Washington and British Columbia. Pinniped impacts in the Columbia River basin were not addressed. The workshop focused on what is known about predation by seals and sea lions on salmon-and how assumptions and uncertainties in the data affect the conclusions drawn to date about the effect of pinnipeds on salmon. This workshop was a first step in bringing together scientists and managers with pinniped and salmon expertise from Canada and the United States to identify and evaluate the impact that pinnipeds may be having on salmonids. It has identified the major knowledge gaps and need for focused research to address the key uncertainties that prevent drawing definitive conclusions about the role that pinnipeds play in the Salish Sea and their impact on other important ecosystem components such as salmon.

abstract
Decreased health may have lowered the birth and survival rates of Steller sea lions (Eumetopias jubatus) in the Gulf of Alaska and Aleutian Islands over the past 30 yr. Reference ranges for clinical hematology and serum chemistry parameters needed to assess the health of wild sea lion populations are limited. Here, blood parameters were serially measured in 12 captive female Steller sea lions ranging in age from 3 wk to 16 yr to establish baseline values and investigate age-related changes. Whether diving activity affects hematology parameters in animals swimming in the ocean compared with animals in a traditional aquarium setting was also examined. Almost all blood parameters measured exhibited significant changes with age. Many of the age-related changes reflected developmental life history changes, including a change in diet during weaning, an improvement of diving capacity, and the maturity of the immune system. Mean corpuscular hemoglobin and mean corpuscular volume were also higher in the ocean diving group compared with the aquarium group, likely reflecting responses to increased exercise regimes. These data provide ranges of hematology and serum chemistry values needed to evaluate and compare the health and nutritional status of captive and wild Steller sea lions.

keywords     Diving, Eumetopias jubatus, hematology, marine mammal, serum chemistry, Steller sea lion

abstract
Animal-borne instruments have become a standard tool for collecting important data from marine mammals. However, few studies have examined whether placement of these data loggers affects the behavior and energetics of individual animals, potentially leading to biasing data. We measured the effect of two types of relatively small data loggers (<1% of animals

keywords     northern fur seals, Callorhinus ursinus, telemetry, bioenergetics, biologging, diving, swimming, marine mammal

abstract
This workshop assembled scientists and managers with technical expertise on killer whales and Chinook salmon to identify and evaluate short-term management actions that might increase the immediate abundance and accessibility of Chinook salmon for southern resident killer whales, given the current size of Chinook salmon stocks. The workshop did not consider ways of producing more Chinook salmon (which will be the subject of a subsequent workshop), but rather considered ways of making more of the fish that are presently in the ocean available to southern resident killer whales (SRKW). Workshop participants presented and discussed technical information on the prey requirements of SRKW, the availability of Chinook salmon, and current protections for SRKW. Participants then split into four groups with an even distribution of expertise to evaluate three potential non- exclusive Management Actions: 1) Increase the abundance of Chinook for SRKW by reducing coast-wide fishery removals; 2) Increase the abundance of Chinook for SRKW by adjusting fishery removals at specific times and in specific areas of SRWK habitat; and 3) Increase the accessibility of Chinook by decreasing underwater noise and the physical presence of vessels where SRKW forage.

keywords     killer whales, southern resident, prey, availability, abundance, accessibility, noise, disturbance, fishing, commercial, recreational, Chinook, salmon

abstract
Direct measures of energy expenditure are difficult to obtain in marine mammals, and accelerometry may be a useful proxy. Recently its utility has been questioned as some analyses derived their measure of activity level by calculating the sum of accelerometry-based values and then comparing this summation to summed (total) energy expenditure (the so-called 'time trap'). To test this hypothesis, we measured oxygen consumption of captive fur seals and sea lions wearing accelerometers during submerged swimming and calculated total and rate of energy expenditure. We compared these values with two potential proxies of energy expenditure derived from accelerometry data: flipper strokes and dynamic body acceleration (DBA). Total number of strokes, total DBA, and submergence time all predicted total oxygen consumption (sVO2 ml kg−1). However, both total DBA and total number of strokes were correlated with submergence time. Neither stroke rate nor mean DBA could predict the rate of oxygen consumption (sV.O2 ml min−1 kg−1). The relationship of total DBA and total strokes with total oxygen consumption is apparently a result of introducing a constant (time) into both sides of the relationship. This experimental evidence supports the conclusion that proxies derived from accelerometers cannot estimate the energy expenditure of marine mammals.

keywords     energy expenditure, accelerometers, Steller sea lions

abstract
Energy expenditure of free-living fur seals and sea lions is difficult to measure directly, but may be indirectly derived from flipper stroke rate. We filmed 10 captive otariids swimming with accelerometers either attached to a harness (Daily Diary: sampling frequency 32Hz, N = 4) or taped to the fur (G6a+: 25Hz, N = 6). We used down sampling to derive four recording rates from each accelerometer (Daily Diary: 32, 16, 8, 4Hz; G6a+: 25, 20, 10, 5Hz). For each of these sampling frequencies we derived 20 combinations of two parameters (RMW - the window size used to calculate the running mean, and m – the minimum number of points smaller than the local maxima used to detect a peak), from the dynamic acceleration of x, z and x+z, to estimate stroke rate from the accelerometers. These estimates differed by up to ~20% in comparison to the actual number of foreflipper strokes counted from videos. RMW had little effect on the overall differences, nor did the choice of axis used to make the calculations (x, z or x+z), though the variability was reduced when using x+z. The best m varied depending on the axis used and the sampling frequency, where a larger m was needed for higher sampling frequencies. This study demonstrates that when parameters are appropriately tuned, accelerometers are a simple yet valid tool for estimating the stroke rates of swimming otariids.

keywords     otariid, swim mechanics, stroke rate, accelerometer, energetics, biologger

abstract
Marine mammals are characterized as having physiological specializations that maximize the use of oxygen stores to prolong time spent under water. However, it has been difficult to undertake the requisite controlled studies to determine the physiological limitations and trade-offs that marine mammals face while diving in the wild under varying environmental and nutritional conditions. For the past decade, Steller sea lions (Eumetopias jubatus) trained to swim and dive in the open ocean away from the physical confines of pools participated in studies that investigated the interactions between diving behaviour, energetic costs, physiological constraints, and prey availability. Many of these studies measured the cost of diving to understand how it varies with behaviour and environmental and physiological conditions. Collectively, these studies show that the type of diving (dive bouts or single dives), the level of underwater activity, the depth and duration of dives, and the n utritional status and physical condition of the animal affect the cost of diving and foraging. They show that dive depth, dive and surface duration, and the type of dive result in physiological adjustments (heart rate, gas exchange) that may be independent of energy expenditure. They also demonstrate that changes in prey abundance and nutritional status cause sea lions to alter the balance between time spent at the surface acquiring oxygen (and offloading CO2 and other metabolic by-products) and time spent at depth acquiring prey. These new insights into the physiological basis of diving behaviour further our understanding of the potential scope for behavioural responses of marine mammals to environmental changes, the energetic significance of these adjustments, and the consequences of approaching physiological limits.

abstract
Understanding whether northern fur seals (Callorhinus ursinus (L., 1758)) are negatively affected by changes in prey quality or diversity could provide insights into their on-going population decline in the central Bering Sea. We investigated how six captive female fur seals assimilated energy from eight different diets consisting of four prey species (walleye pollock (Gadus chalcogrammus Pallas, 1814, formerly Theragra chalcogrammus (Pallas, 1814)), Pacific herring (Clupea pallasii Valenciennes in Cuvier and Valenciennes, 1847), capelin (Mallotus villosus (Muller, 1776)), and magister armhook squid (Berryteuthis magister (Berry, 1913))) fed alone or in combination. Net energy was quantified by measuring fecal energy loss, urinary energy loss, and heat increment of feeding. Digestible energy (95.9%-96.7%) was high (reflecting low fecal energy loss) and was negatively affected by ingested mass and dietary protein content. Urinary energy loss (9.3%-26.7%) increased significantly for high-protein diets. Heat increment of feeding (4.3%-12.4%) was significantly lower for high-lipid diets. Overall, net energy gain (57.9%-83.0%) was affected by lipid content and varied significantly across diets. Mixed-species diets did not provide any energetic benefit over single-species diets. Our study demonstrates that diet quality was more important in terms of energy gain than diet diversity. These findings suggest that fur seals consuming low-quality prey in the Bering Sea would be more challenged to obtain sufficient energy to satisfy energetic and metabolic demands, independent of high prey abundance.

keywords     northern fur seal, Callorhinus ursinus, net energy, mixed-species diets, diet quality

abstract
Recent studies of stranded marine mammals indicate that exposure to underwater military sonar may induce pathophysiological responses consistent with decompression sickness (DCS). However, DCS has been difficult to diagnose in marine mammals. We investigated whether blood microparticles (MPs, measured as number/l plasma), which increase in response to decompression stress in terrestrial mammals, are a suitable biomarker for DCS in marine mammals. We obtained blood samples from trained Steller sea lions (Eumetopias jubatus, 4 adult females) wearing time-depth recorders that dove to predetermined depths (either 5 or 50 meters). We hypothesized that MPs would be positively related to decompression stress (depth and duration underwater). We also tested the effect of feeding and exercise in isolation on MPs using the same blood sampling protocol. We found that feeding and exercise had no effect on blood MP levels, but that diving caused MPs to increase. However, blood MP levels did not correlate with diving depth, relative time underwater, and presumed decompression stress, possibly indicating acclimation following repeated exposure to depth.

abstract
Previous research has presented contradictory evidence on the ability of overall dynamic body acceleration (ODBA) to predict oxygen consumption (sV̇O2) in air-breathing diving vertebrates. We investigated a potential source of these discrepancies by partitioning the ODBA: sV̇O2 relationship over 3 phases of the dive cycle (transiting to and from depth, bottom time, and post-dive surface interval). Trained Steller sea lions (Eumetopias jubatus) executed 4 types of dives to 40 m (single dives, long-duration dive bouts of 4-6 dives, short-duration dive bouts of 10 or 12 dives, and transit dives with minimal bottom duration). Partitioning single dives by dive phase showed differing patterns in the ODBA: sV̇O2 relationship among dive phases, but no significant linear relationships were observed. The proportion of the dive cycle spent transiting to and from the surface was a significant predictive factor in the ODBA: sV̇O2 relationship, while bottom duration or post-dive surface interval had no effect. ODBA only predicted sV̇O2 for dives when the proportion of time spent transiting was small. The apparent inability of ODBA to reliably predict sV̇O2 reflects differences in the inherent relationships between ODBA and sV̇O2 during different phases of the dive. These results support the growing body of evidence that ODBA on its own is not a reliable field predictor of energy expenditure at the level of the single dive or dive bout in air-breathing diving vertebrates likely because ODBA (a physical measure) cannot account for physiological changes in sV̇O2 that occur during the different phases of a dive cycle.

keywords     diving behaviour, metabolic rate, ODBA, dive phase, pinniped

abstract
Dive characteristics and dive shape are often used to infer foraging success in pinnipeds. However, these inferences have not been directly validated in the field with video, and it remains unclear if this method can be applied to benthic foraging animals. This study assessed the ability of dive characteristics from time-depth recorders (TDR) to predict attempted prey capture events (APC) that were directly observed on animal-borne video in Australian fur seals (Arctocephalus pusillus doriferus, n=11). The most parsimonious model predicting the probability of a dive with ≥1 APC on video included only descent rate as a predictor variable. The majority (94%) of the 389 total APC were successful, and the majority of the dives (68%) contained at least one successful APC. The best model predicting these successful dives included descent rate as a predictor. Comparisons of the TDR model predictions to video yielded a maximum accuracy of 77.5% in classifying dives as either APC or non-APC or 77.1% in classifying dives as successful verses unsuccessful. Foraging intensity, measured as either total APC per dive or total successful APC per dive, was best predicted by bottom duration and ascent rate. The accuracy in predicting total APC per dive varied based on the number of APC per dive with maximum accuracy occurring at 1 APC for both total (54%) and only successful APC (52%). Results from this study linking verified foraging dives to dive characteristics potentially opens the door to decades of historical TDR datasets across several otariid species.

keywords     Crittercam, Foraging behaviour, Animal-borne video, Dive profile analysis

abstract
Forces due to propulsion should approximate forces due to hydrodynamic drag for animals horizontally swimming at a constant speed with negligible buoyancy forces. Propulsive forces should also correlate with energy expenditures associated with locomotion預n important cost of foraging. As such, biologging tags containing accelerometers are being used to generate proxies for animal energy expenditures despite being unable to distinguish rotational movements from linear movements. However, recent miniaturizations of gyroscopes offer the possibility of resolving this shortcoming and obtaining better estimates of body accelerations of swimming animals. We derived accelerations using gyroscope data for swimming Steller sea lions (Eumetopias jubatus), and determined how well the measured accelerations correlated with actual swimming speeds and with theoretical drag. We also compared dive averaged dynamic body acceleration estimates that incorporate gyroscope data, with the widely used Overa ll Dynamic Body Acceleration (ODBA) metric, which does not use gyroscope data. Four Steller sea lions equipped with biologging tags were trained to swim alongside a boat cruising at steady speeds in the range of 4 to 10 kph. At each speed, and for each dive, we computed a measure called Gyro-Informed Dynamic Acceleration (GIDA) using a method incorporating gyroscope data with accelerometer data. We derived a new metric輸veraged Propulsive Body Acceleration (APBA), which is the average gain in speed per flipper stroke divided by mean stroke cycle duration. Our results show that the gyro-based measure (APBA) is a better predictor of speed than ODBA. We also found that APBA can estimate average thrust production during a single stroke-glide cycle, and can be used to estimate energy expended during swimming. The gyroscope-derived methods we describe should be generally applicable in swimming animals where propulsive accelerations can be clearly identified in the signal預nd they should also prove useful for dead-reckoning and improving estimates of energy expenditures from locomotion.

keywords     biologging, ODBA, accelerometer, gyroscope, swimming, speed, energy expenditure, drag, stroke

abstract
We tagged 82 lactating northern fur seals (Callorhinus ursinus) with tri-axial accelerometers and magnetometers on two eastern Bering Sea islands (Bogoslof and St. Paul) with contrasting population trajectories. Using depth data, accelerometer data and spectral analysis we classified time spent diving (30%), resting (~7%), shaking and grooming their pelage (9%), swimming in the prone position (~10%) and two types of previously undocumented rolling behavior (29%), with the remaining time (~15%) unspecified. The reason for the extensive rolling behavior is not known. We ground-truthed the accelerometry signals for shaking and grooming and rolling behaviors—and identified the acceleration signal for porpoising—by filming tagged northern fur seals in captivity. Speeds from GPS interpolated data indicated that animals traveled fastest while in the prone position, suggesting that this behavior is indicative of destination-based swimming. Very little difference was found in the percentages of time spent in the categorical behaviors with respect to breeding islands (Bogoslof or St. Paul Island), forager type (cathemeral or nocturnal), and the region where the animals foraged (primarily on-shelf <200m, or off-shelf > 200m). The lack of significant differences between islands, regions and forager type may indicate that behaviors summarized over a trip are somewhat hardwired even though foraging trip length and when and where animals dive are known to vary with island, forager type and region.

keywords     seals, accelerometers, animal behavior, foraging, biological locomotion, sine wave, fur seal

abstract
Seasonal changes in daily energy expenditure (DEE) and its key underlying components (costs of resting metabolic rate (RMR), thermoregulation, activity, and growth) were measured to determine seasonal energy requirements, bioenergetic priorities, and potential times of year when unpredicted episodes of nutritional stress would have their greatest effect on female northern fur seals (Callorhinus ursinus L., 1758). The DEE of 6 captive juvenile female fur seals averaged 527.8 Ä… 65.7 kJ kg-1 d-1 (Ä… SD) and fluctuated seasonally (lower during summer and winter, and up to 20% greater in spring and fall). RMR also changed significantly with season, and was higher in the fall (potentially due to moulting or anticipated migratory activity). However, changes in RMR did not follow the same seasonal trend as those of DEE. The largest component of DEE was RMR (~ 80% on average), followed by the cost of activity (which may have driven some of the seasonal variations in DEE). In contrast, the energetic costs associated with growth and thermoregulation appeared negligible within the scope of overall energy expenditures. Elevated innate costs of RMR and higher growth rates in the fall and summer, respectively, suggest that inadequate nutrition could comparatively have greater negative effects on female fur seals during these seasons

keywords     northern fur seal, Callorhinus ursinus, daily energy expenditure,resting metabolic rate, activity, growth, thermoregulation

abstract
Breath-hold divers should adjust their dive behaviors to maximize the benefits and minimize the costs of foraging on prey patches of different densities at different depths. However, few studies have quantified how animals respond to changes in prey availability (depth and density), and how this affects their foraging efficiency. We tested the effects of changes in prey availability on the foraging behavior and efficiency of Steller sea lions (Eumetopias jubatus) by measuring diving metabolic rate, dive durations, and food intake of 4 trained sea lions diving in the open ocean on controlled prey patches of different densities at different depths. Sea lions completed bouts of 5 consecutive dives on high- or low-density prey patches at two depths (10m and 40m). We found that the rate of energy expenditure did not change under any of the imposed foraging conditions (meanąSD: 0.22ą0.02 kJ min−1 kg−1), but that the proportion of time spent consuming prey increased with prey patch density due to changes in diving patterns. At both depths, sea lions spent a greater proportion of the dive bout foraging on prey patches with high prey density, which led to high rates of energy gain (4.3 ą 0.96 kJ min−1 kg−1) and high foraging efficiency (cost:benefit was 1:20). In contrast, the sea lions spent a smaller proportion of their dive bout actively feeding on prey patches with low prey density, and consequently had a lower energetic gain (0.91 ą 0.29 kJ min−1 kg−1) and foraging efficiency (1:4). The 5-fold differences in foraging efficiency between the two types of prey patches were greater than the 3-fold differences that we expected based on differences in food availability. Our results suggest that sea lions faced with reduced prey availability forage less efficiently and therefore would have greater difficulty obtaining their daily energy requirements.

keywords     Dive behavior, Diving energetics, Foraging efficiency, Optimal foraging, Steller sea lion

abstract
Feeding performance studies can address questions relevant to feeding ecology and evolution. Our current understanding of feeding mechanisms for aquatic mammals is poor. Therefore, we characterized the feeding kinematics and performance of five Steller sea lions (Eumetopias jubatus) and six northern fur seals (Callorhinus ursinus). We tested the hypotheses that both species use suction as their primary feeding mode, and that rapid jaw opening was related to suction generation. Steller sea lions used suction as their primary feeding mode, but also used a biting feeding mode. In contrast, northern fur seals only used a biting feeding mode. Kinematic profiles of Steller sea lions were all indicative of suction feeding (i.e. a small gape, small gape angle, large depression of the hyolingual apparatus and lip pursing). However, jaw opening as measured by gape angle opening velocity (GAOV) was relatively slow in Steller sea lions. In contrast to Steller sea lions, the GAOV of northern fur seals was extremely fast, but their kinematic profiles indicated a biting feeding mode (i.e. northern fur seals exhibited a greater gape, a greater gape angle and minimal depression of the hyolingual apparatus compared with Steller sea lions). Steller sea lions produced both subambient and suprambient pressures at 45 kPa. In contrast, northern fur seals produced no detectable pressure measurements. Steller sea lions have a broader feeding repertoire than northern fur seals, which likely enables them to feed on a greater variety of prey, in more diverse habitats. Based on the basal phylogenetic position of northern fur seals, craniodental morphological data of the Callorhinus lineage, and the performance data provided in this study, we suggest that northern fur seals may be exhibiting their ancestral feeding mode.

keywords     Otariidae, Callorhinus ursinus, Eumetopias jubatus,suction, biting, fossil pinnipeds

abstract
Past foraging success of diving air-breathing vertebrates can adversely affect future foraging capabilities and costs through changes in circulation or increased metabolic costs associated with digestion that are incompatible with efficient diving. This study tested the physiological interaction between digestion and diving by comparing the cost of diving in fasted and pre-fed trained Steller sea lions foraging under controlled conditions in the open ocean. Pre-dive and post-dive surface metabolism and diving metabolic rate were all higher in the pre-fed animals than the fasted animals, indicating an effect of digestion on metabolism. However, the sea lions displayed a significant reduction in the apparent additive effect of digestion during diving. The increase in rate of oxygen consumption associated with digestion was reduced by 54% during diving compared to the increase observed in pre-dive metabolism. This truncation of the additional cost of digestion rapidly disappeared following cessation of diving. The results suggest that Steller sea lions diving to depth demonstrate a partial deferment of digestion while actively foraging and that the classically held view that digestion and diving are incompatible processes may be much more variable and adaptable to specific diving conditions and behaviors than previously thought.

abstract
Gene expression profiles are increasingly being used as biomarkers to detect the physiological responses of a number of species to disease, nutrition, and other stressors. However, little attention has been given to using gene expression to assess the stressors and physiological status of marine mammals. We sought to develop and validate a nutrigenomics approach to quantify nutritional stress in Steller sea lions (Eumetopias jubatus). We subjected 4 female Steller sea lions to 3 feeding regimes over 70-day trials (unrestricted food intake, acute nutritional stress, and chronic nutritional stress), and drew blood samples from each animal at the end of each feeding regime. We then extracted the RNA of white blood cells and measured the response of 8 genes known to react to diet restriction in terrestrial mammals. Overall, we found that the genomic response of Steller sea lions experiencing nutritional stress was consistent with diet restriction regulation in terrestrial mammals. Our nutritionally stressed sea lions down-regulated some cellular processes involved in immune response and oxidative stress, and up-regulated pro-inflammatory responses and metabolic processes. Nutrigenomics appears to be a promising means to monitor nutritional status and contribute to mitigation measures needed to assist in the recovery of Steller sea lions and other at-risk species of marine mammals.

keywords     Genomics, Expression profile, q-PCR, Diet, restriction, Biomarker, Monitoring

abstract
Nutritional constraints have been proposed as a contributor to population declines in the endangered Steller sea lion Eumetopias jubatus in some regions of the North Pacific. Isotopic analysis of vibrissae (whiskers) is a potentially useful approach to resolving the nutritional ecology of this species because long-term (up to 8 yr) dietary information is sequentially recorded and metabolically inert once formed. Additionally, vibrissae are grown in utero, potentially offering indirect inference on maternal diet. However, diet reconstruction using isotopic techniques requires a priori knowledge of trophic enrichment factors (TEFs), which can vary relative to diet quality and among animal species. In this study, we provide new TEF estimates for (1) maternal relative to pup vibrissae during both gestation and nursing and (2) adult vibrissae relative to a complex diet. Further, we refine vibrissa−milk TEFs based on an additional 76 animals with an age distribution ranging from 1 to 20 mo. Mother−pup vibrissae TEF values during gestation and nursing were near zero for δ13C and averaged 0.8 and 1.6‰, respectively, for δ15N. In contrast, vibrissa− fish/invertebrate TEFs averaged 3.3 (± 0.3 SD) and 3.7‰ (±0.3) for lipid-free δ13C and δ15N, respectively. Average lipid-free δ13C and δ15N vibrissa−milk TEFs were 2.5 (±0.9) and 1.8‰ (±0.8), respectively, and did not differ among metapopulations. Empirically determined TEFs are critical for accurate retrospective diet modeling, particularly for evaluating the hypothesis of nutritional deficiency contributing to the lack of Steller sea lion population recovery in some regions of Alaska.

abstract
We tested the ability of overall dynamic body acceleration (ODBA) to predict the rate of oxygen consumption (sVO2) in freely diving Steller sea lions ( Eumetopias jubatus/) while resting at the surface and diving. The trained sea lions executed three dive types―single dives, bouts of multiple long dives with 4-6 dives per bout, or bouts of multiple short dives with 10-12 dives per bout葉o depths of 40 m, resulting in a range of activity and oxygen consumption levels. Average metabolic rate (AMR) over the dive cycle or dive bout calculated was calculated from sVO2. We found that ODBA could statistically predict AMR when data from all dive types were combined, but that dive type was a significant model factor. However, there were no significant linear relationships between AMR and ODBA when data for each dive type was analyzed separately. The potential relationships between AMR and ODBA were not improved by including dive duration, food consumed, proportion of dive cycle spent submerged or number of dives per bout. It is not clear whether the lack of predictive power within dive type was due to low statistical power, or whether it reflected a true absence of a relationship between ODBA and AMR. The average percent error for predicting AMR from ODBA was 7-11%, and standard error of the estimated AMR was 5-32%. Overall, the extensive range of dive behaviours and physiological conditions we tested indicated that ODBA was not suitable for estimating AMR in the field due to considerable error and the inconclusive effects of dive type.

keywords     Steller sea lion, oxygen consumption, overall dynamic body acceleration, activity, oxygen depletion, diving physiology

abstract
Thermoregulatory capacity may constrain the distribution of marine mammals despite having anatomical and physiological adaptations to compensate for the thermal challenges of an aquatic lifestyle. We tested whether subadult female northern fur seals (Callorhinus ursinus) experience increased thermoregulatory costs in water temperatures potentially encountered during their annual migration in the Bering Sea and North Pacific Ocean. Metabolic rates were measured seasonally in 6 captive female northern fur seals (2.75 to 3.5 yr old) in ambient air and controlled water temperatures of 2, 10, and 18 °C. Rates of oxygen consumption in ambient air (1 – 18 °C) were not related to environmental temperature except below 2.5 °C (winter only). However, metabolism was significantly higher during the fall seasonal trials (Sept – Oct) compared to other times of year, perhaps due to the costs of molting. The fur seals appeared thermally neutral in all seasons for all water temperat ures tested (2 – 18 °C) except during the summer when metabolic rates were higher in the 2 °C water. Comparing this broad thermal neutral zone to the average sea surface temperatures potentially encountered during annual migrations indicates wild fur seals can likely exploit a large geographic area without added thermal metabolic costs.

abstract
Estimates of energy expenditure for free-ranging animals are essential to answering a range of fundamental questions in animal biology, but are challenging to obtain and difficult to validate. We simultaneously employed three methods to measure the energy expenditure of 6 captive female northern fur seals (Callorhinus ursinus) during 5-day trials across 4 seasons: respirometry (oxygen consumption), doubly labeled water (DLW), and accelerometry. The DLW method estimated that the fur seals expended 13.1 ? 16.5% more energy than indicated by the more direct measures of oxygen consumption. Accelerometry failed to predict the average mass specific rate of oxygen consumption (VË™ O2DEE) within the individual seasons over entire 5- day trials. However, on a finer time scale (15 or 60 min) and adjusted for time of day, accelerometry estimated energy expenditure within an average difference of 5.4 ? 29.3% (60 min intervals) and 13.8 ? 39.5% (15 min intervals) of respirometry measured values. Our findings suggest that accelerometers have the potential to be more effective than the DLW method for measuring energy expenditure of free-ranging animals. However, rates of oxygen consumption varied with season, independent of overall activity. Seasonal effects (and time of day for accelerometry) must therefore be accounted for when estimating energy expenditure from measures of DLW and acceleration of free-swimming northern fur seals. Such corrections required for estimating energy expenditures in northern fur seals have implications for using accelerometers and DLW to estimate the energy expenditure of other species.

keywords     accelerometry, Callorhinus ursinus, daily energy expenditure, doubly labeled water, northern fur seal, respirometry

abstract
Marine mammal foraging behaviour inherently depends on diving ability. Declining populations of Steller sea lions may be facing nutritional stress that could affect their diving ability through changes in body composition or metabolism. Our objective was to determine whether nutritional stress (restricted food intake resulting in a 10% decrease in body mass) altered the calculated aerobic dive limit (cADL) of four captive sea lions diving in the open ocean, and how this related to changes in observed dive behaviour. We measured diving metabolic rate (DMR), blood O2 stores, body composition and dive behaviour prior to and while under nutritional restriction. We found that nutritionally stressed sea lions increased the duration of their single long dives, and the proportion of time they spent at the surface during a cycle of four dives. Nutritionally stressed sea lions lost both lipid and lean mass, resulting in potentially lower muscle O2 stores. However, total body O2 stores increased due to rises in blood O2 stores associated with having higher blood volumes. Nutritionally stressed sea lions also had higher mass-specific metabolic rates. The greater rise in O2 stores relative to the increase in mass-specific DMR resulted in the sea lions having a longer cADL when nutritionally stressed. We conclude that there was no negative effect of nutritional stress on the diving ability of sea lions. However, nutritional stress did lower foraging efficiency and require more foraging time to meet energy requirements due to increases in diving metabolic rates and surface recovery times.

abstract
Marine mammal foraging behavior inherently depends on diving ability. Declining populations of Steller sea lions may be facing nutritional stress that could affect their diving ability through changes in body composition or metabolism. Our objective was to determine whether nutritional stress (restricted food intake resulting in a 10% decrease in body mass) altered the calculated aerobic dive limit (cADL) of four captive sea lions diving in the open ocean, and how this related to changes in observed dive behaviour. We measured diving metabolic rate (DMR), blood O2 stores, body composition and dive behaviour prior to and while under nutritional restriction. We found that nutritionally stressed sea lions increased the duration of their single long dives, and the proportion of time they spent at the surface during a cycle of four dives. Nutritionally stressed sea lions lost both lipid and lean mass, resulting in potentially lower muscle O2 stores. However, total body O2 stores increased due to rises in blood O2 stores associated with having higher blood volumes. Nutritionally stressed sea lions also had higher mass-specific metabolic rates. The greater rise in O2 stores relative to the increase in mass-specific DMR resulted in the sea lions having a longer cADL when nutritionally stressed. We conclude that there was no negative effect of nutritional stress on the diving ability of sea lions. However, nutritional stress did lower foraging efficiency and require more foraging time to meet energy requirements due to increases in diving metabolic rates and surface recovery times.

keywords     Steller sea lion, blood volume, nutritional stress, diving metabolism, oxygen stores, dive behavior

abstract
Unexpected shortages of food may affect wildlife differently depending on the time of year it occurs. We imposed 48-hr fasts on six female northern fur seals (Callorhinus ursinus; ages 6 ? 24 months) to identify times of year when they might be particularly sensitive to interruptions in food supply. We monitored changes in their resting metabolic rates and their metabolic response to thermal challenges, and also examined potential bioenergetic causes for seasonal differences in body mass loss. Pre-fast metabolism of the fur seals while in ambient air or submerged in 4 ?C water was higher during summer (Jun-Sep) than winter (Nov-Mar), and submergence did not significantly increase metabolism indicating a lack of additional thermoregulatory costs. There was no evidence of metabolic depression following the fasting periods, nor did metabolism increase during the post-fast thermal challenge, suggesting that mass loss did not negatively impact thermoregulatory capacity. However, the fur seals lost mass at greater rates while fasting during the summer months when metabolism is normally high to facilitate faster growth rates (which would ordinarily have been supported by higher food intake levels). Our findings suggest that summer is a more critical time of year than winter for young northern fur seals to obtain adequate nutrition.

abstract
The thermoregulatory abilities of northern fur seals (Callorhinus ursinus) during their first two years in the frigid waters of the North Pacific Ocean may limit their geographic distribution and alter the costs for exploiting different species of prey. We determined the thermoneutral zone of 6 young northern fur seals by measuring their metabolism in ambient air and controlled water temperatures (0-12 °C) from ages 8 to 24 mo. We found that the ambient air temperatures within our study (overall 1.5-23.9 °C) did not affect resting metabolic rates. Calculated lower critical temperatures in water varied between 3.9 and 8.0 °C, while an upper critical temperature in water was only discernible during a single set of trials. These thermal responses provide insight into the possible physiological constraints on foraging ecology in young northern fur seals, as well as the potential energetic consequences of ocean climate change and altered prey distributions.

keywords     Northern fur seal, Callorhinus ursinus, thermoregulation, metabolism, bioenergetics

abstract
Three Steller sea lions (Eumetopias jubatus), trained to dive voluntarily to depths ranging from 10 to 50 m, were used to determine whether the relationship between activity and metabolic rate during a diving interval (MRDI, dive + surface interval) was affected by fasting (9-days) during the breeding season (spring through summer). We subsequently used the relationship between activity and MRDI to partition the metabolic costs between underwater breath-holding activity and surface breathing activities. We estimated activity from Overall Dynamic Body Acceleration (ODBA) measured using a 3-axis accelerometer, and measured MRDI using flow-through respirometry. The relationship between ODBA-based activity and MRDI was not affected by fasting period, suggesting ODBA can be used to predict energy expenditure regardless of nutritional state in the spring and summer. However, the relationship between ODBA and dive metabolic rate differs from the relationship between ODBA and the s urface metabolic rate before diving (MRSp). Partitioning MRDI into the metabolic cost of remaining at the surface (MRs) versus swimming underwater (MRUS) suggests that the metabolic cost of diving for Steller sea lions is approximately 29% lower than when breathing at the surface. ODBA appears to be a reasonable proxy to estimate metabolic rate in marine mammals, but more detailed behavioral data may be required to accurately apply the method in the field.

abstract
Management plans for North Atlantic right whales Eubalaena glacialis focus on preventing mortality from ship strikes and fishing gear entanglement. However, recovery may also be limited because individuals are under nutritional stress. We quantified the food requirements of North Atlantic right whales by age, sex and reproductive state and compared their predicted needs with field estimates of prey consumption to assess whether any demographic group of right whales might be nutritionally stressed. Energy requirements were estimated using a bioenergetics model that accounted for uncertainty in energy inputs and outputs. Consumption was estimated with prey samples taken near feeding whales in Cape Cod Bay (n = 28 net collections) and the Bay of Fundy (n = 19 optical plankton recordings). We found that calves required the least energy (~1767 MJ d-1) and that lactating females required the most (~4120 MJ d-1). Juveniles required considerably more energy than adult males and non-reproductive females. Our estimates of energy requirements for juveniles (~1906 MJ d-1), adult males (~1793 MJ d-1), and non-reproductive females (~2104 MJ d-1) compared favorably with estimates of actual consumption in Cape Cod Bay and the Bay of Fundy (i.e. they differed by ≤15%), suggesting that our model was reliable. However, lactating females appear to have obtained considerably less than their predicted energy requirements in both habitats. These findings suggest that lactating females may be experiencing an energy deficit, which may affect reproductive rates and slow population recovery. Nutritional stress may thus be limiting the recovery of North Atlantic right whales.

keywords     Bioenergetic model, Eubalaena glacialis, nutritional stress, energetic consumption, energetic requirements

abstract
The diving capacity of marine mammals is typically defined by the aerobic dive limit ^(ADL) which, in lieu of direct measurements, can be calculated ^(cADL) from total body oxygen stores (TBO) and diving metabolic rate ^(DMR). To estimate cADL, we measured blood oxygen stores, and combined this with diving oxygen consumption rates ^(VO(2) recorded from 4 trained Steller sea lions diving in the open ocean to depths of 10 or 40 m. We also examined the effect of diving exercise on O⁽²⁾ stores by comparing blood O⁽²⁾ stores of our diving animals to non-diving individuals at an aquarium. Mass-specific blood volume of the non-diving individuals was higher in the winter than in summer, but there was no overall difference in blood O⁽²⁾ stores between the diving and non-diving groups. Estimated TBO ^{(35.9 ml O(2)} kg^(-1) )was slightly lower than previously reported for Steller sea lions and other Otariids. Calculated ADL was 3.0 min (based on an average DMR of 2.24 L O⁽²⁾ min^(-1)) and was signific antly shorter than the average 4.4 min dives our study animals performed when making single long dives-but was similar to the times recorded during diving bouts (a series of 4 dives followed by a recovery period on the surface), as well as the dive times of wild animals. Our study is the first to estimate cADL based on direct measures of VO⁽²⁾ and blood oxygen stores for an Otariid and indicates they have a much shorter ADL than previously thought.

abstract
Apex predators such as Pacific white-sided dolphins (Lagenorhynchus obliquidens) have the potential to impact prey populations and to be affected by changes in prey abundance. As an abundant predator that ranges widely across the North Pacific Ocean, their interactions with prey populations may have conservation implications. We estimated the energy required by individual Pacific white-sided dolphins using a bioenergetic model that accounted for different age classes and reproductive stages (calf, juvenile, adult, pregnant and lactating). Monte Carlo simulations incorporating variability in model parameters (body mass, growth rate, costs of gestation and lactation, metabolic rate, cost of activity, and assimilation efficiencies) were used to predict ranges in energetic requirements. Mean (±SD) total energy requirements in MJ day-1 were 40.3 ± 6.2 for calves, 70.8 ± 8.2 for juveniles, 69.0 ± 3.6 for adults, 70.3 ± 3.6 for pregnant females, and 98.4 ± 20.0 for lactating femal es. Estimates of energy requirements were most sensitive to uncertainty in values used for resting metabolic rates and energetic costs of activity. Estimated mass-specific energy requirements in MJ kg-1 day-1 were elevated in calves (1.55 ± 0.23), juveniles (0.97 ± 0.11) and lactating females (1.01 ± 0.21) when compared with non-reproductive adults and pregnant females (~0.71 ± 0.04). Based on a high-energy density diet, an average sized dolphin (78 kg) would consume approximately 12.5 - 15.8 kg of fish or 15-20% of its body weight per day. These high energetic requirements may indicate a reliance of dolphins on energy rich prey, which has implications for fisheries management and conservation of marine mammals.

abstract
Like many marine mammals, Pacific white-sided dolphins (Lagenorhynchus obliquidens) consume prey that change seasonally in numbers, distribution, and energy density. However, it is not known whether these ecological factors are associated with underlying seasonal changes in energy requirements. We investigated these potential seasonal shifts in physiology by measuring resting metabolic rate (a conserved physiological trait) and recording associated daily food energy intake of three captive adult Pacific white-sided dolphins over 12 consecutive months. Two dolphins that met the criteria for measuring resting metabolism had a mean (± SE) mass-specific rate of 0.31 ± 0.0047 MJ kg-1 day- 1 (~34 MJ day-1), which was higher than that of other species of small cetaceans. Resting metabolic rates of Pacific white-sided dolphins did not vary seasonally and, hence, were not related to observed seasonal changes in water or air temperature, total energy intake, or body mass. Overall, resting metabolism accounted for ~70% of total energy intake. However, total food energy intake changed seasonally and was highest during the fall (October to December). While levels of food intake were not predicted by resting metabolic rate, body mass, or water and air temperatures, the increased intake in the fall resulted in the seasonal increase in body mass exhibited by all three dolphins. Our estimates of resting metabolic rates and relative changes in total energy intake can be used to parameterize bioenergetic models needed to estimate the ecological impacts and energetic requirements of Pacific white-sided dolphins in the wild, which will have conservation implications.

keywords     energetics, oxygen consumption, Pacific white-sided dolphins, season, food intake, metabolic rate

abstract
We conducted repeated measurements of rates of oxygen consumption on a mature (~17 yrs) male beluga whale held at the Vancouver Aquarium, and trained to rest quietly at the surface of his holding pool underneath a specially designed floating dome that completely contained the portion of his body above the water line. Each trial lasted ~20 minutes prior to the morning feed, and rates of oxygen consumption were calculated over the last 10 minutes of each trial. The average metabolic rate over 11 trials was 73,050 ± 2290 kJ d-1 (Mean ± S.E.). This translated into approximately 54.48 ± 1.71 kJ kg-1 d-1, which was approximately 1.13 ± .035 times the predicted value for a similarly-sized terrestrial mammal. This was statistically greater than 1.0, but did not approach the much higher values reported for many other small cetacean species.

abstract
Quantitative fatty acid signature analysis (QFASA) has been proposed as a technique for determining the long-term diet of animals. The method compares the fatty acid (FA) profiles of predators and potential prey items to estimate relative prey intake. We tested the assumptions of a key step in QFASA, the correction of predator FA signatures for metabolic processes through sets of calibration coefficients (CCs). We conducted long-term controlled feeding studies with captive Steller sea lions consuming herring and eulachon and northern fur seals consuming herring. We compared the results with data from harbour seals eating herring to evaluate the effects of phylogeny and prey type on individual CCs. Even within the limited extended dietary FA subset recommended for use by other researchers, we found that at least 41% of the CCs differed by family (otariid vs. phocid seals) and 58% differed by predator species (sea lion vs. fur seal), suggesting that CCs may be highly species- specific. We also found that 64% of the CCs differed by prey type (sea lions consuming herring vs. eulachon), which raises some fundamental implementation issues. We also found significant differences in diet predictions when the herring- and eulachon-derived sets of CCs were applied to an actual multi-species diet. CCs are presently used as a simple mathematical attempt to describe potentially complex biochemistry. The results of this study raise questions regarding the validity of using CCs derived from an alternative predator species, and highlight some fundamental issues regarding QFASA methodology that need to be addressed through further controlled studies.

abstract
Accurate estimates of food intake and its subsequent affect on growth are required to understand the interaction between an animals‚ physiology and its biotic environment. We determined how food intake and growth of 6 young northern fur seals (Callorhinus ursinus L., 1758) responded seasonally to changes in food availability. Animals were given unrestricted access to prey for 8 hr per day on either consecutive days or on alternate days only. We found animals offered ad libitum food on consecutive days substantially increased their food intake over normal Œtraining‚ levels. However, animals that fasted on alternative days were unable to compensate by further increasing their levels of consumption on subsequent feeding days. Absolute levels of food intake were highly consistent during winter and summer trials (2.7 ˆ 2.9 kg d-1), but seasonal differences in body mass meant that fur seals consumed more food relative to their body mass in summer (~27%) than in winter (~20%). Despite significant increases in absolute food intake during both seasons, the fur seals did not appear to efficiently convert this additional energy into mass growth, particularly in the winter. These seasonal differences in conversion efficiencies and estimates of maximum intake rates can be used to generate physiologically realistic predictions about the effect of changes in food availability on an individual fur as well as the consequences for an entire population.

abstract
Measurements of the electrophysiological auditory steady-state response (ASSR) have proven to be efficient for evaluating hearing sensitivity in odontocete cetaceans. In an effort to expand these methods to pinnipeds, ASSRs elicited by single and multiple simultaneous tones were used to measure aerial hearing thresholds in several California sea lions (Zalophus californianus) and Steller sea lions (Eumetopias jubatus). There were no significant differences between thresholds measured using the single and multiple ASSR methods, despite the more rapid nature of data collection using the multiple ASSR method. There was a high degree of variability in ASSR thresholds among subjects; thresholds covered a range of ~40dB at each tested frequency. As expected, ASSR thresholds were elevated relative to previously reported psychophysical thresholds for California and Steller sea lions. The features of high-frequency hearing limit and relative sensitivity of most ASSR audiograms were, however, similar to those of psychophysical audiograms, suggesting that ASSR methods can be used to improve understanding of hearing demographics in sea lions, especially with respect to high-frequency hearing. Thresholds for one Steller sea lion were substantially elevated relative to all other subjects, demonstrating that ASSR methods can be used to detect hearing loss in sea lions.

abstract
Ecosystem-based management (EBM) of marine resources attempts to conserve interacting species. In contrast to single-species fisheries management, EBM aims to identify and resolve conflicting objectives for different species. Such a conflict may be emerging in the northeastern Pacific for southern resident killer whales (Orcinus orca) and their primary prey, Chinook salmon (Oncorhynchus tshawytscha). Both species have at-risk conservation status and transboundary (CanadaˆUS) ranges. We modeled individual killer whale prey requirements from feeding and growth records of captive killer whales and morphometric data from historic live-capture fishery and whaling records worldwide. The models, combined with caloric value of salmon, and demographic and diet data for wild killer whales, allow us to predict salmon quantities needed to maintain and recover this killer whale population, which numbered 87 individuals in 2009. Our analyses provide new information on cost of lactation and new parameter estimates for other killer whale populations globally. Prey requirements of southern resident killer whales are difficult to reconcile with fisheries and conservation objectives for Chinook salmon, because the number of fish required is large relative to annual returns and fishery catches. For instance, a U.S. recovery goal (2.3% annual population growth of killer whales over 28 years) implies a 75% increase in energetic requirements. Reducing salmon fisheries may serve as a temporary mitigation measure to allow time for management actions to improve salmon productivity to take effect. As ecosystem-based fishery management becomes more prevalent, trade-offs between conservation objectives for predators and prey will become increasingly necessary. Our approach offers scenarios to compare relative influence of various sources of uncertainty on the resulting consumption estimates to prioritise future research efforts, and a general approach for assessing the extent of conflict between conservation objectives for threatened or protected wildlife where the interaction between affected species can be quantified.

abstract
The predictive relationship between heart rate (fH) and oxygen consumption (VO2) has been derived for several species of marine mammals swimming horizontally or diving in tanks to shallow depths. However, it is unclear how dive activity affects the fH:VO2 relationship and whether the existing equations apply to animals diving to deeper depths. We investigated these questions by simultaneously measuring the fH and VO2 of Steller sea lions (Eumetopias jubatus) under different activity states (surface resting or diving), types of dives (single dives or dive bouts), and depths (10 or 40m). We examined the relationship over dives only and also over dive cycles (dive + surface interval). We found that fH could only predict VO2 over a complete single dive cycle or dive bout cycle (i.e. surface intervals had to be included). The predictive equation derived for sea lions resting on the surface did not differ from that for single dive cycles. However, the equation derived over dive bout cycles multiple dives + surface intervals) differed from those for single dive cycles or surface resting, with similar fH for multiple dive bout equations yielding higher predicted VO2 than that for single dive bout cycles (or resting). The fH:VO2 relationships were not significantly affected by dive duration, dive depth, water temperature or cumulative food consumed under the conditions tested. Ultimately, our results demonstrate that fH can be used to predict activity-specific metabolic rates of diving Steller sea lions, but only over complete dive cycles that include a post-dive surface recovery period.

abstract
The ability to use heart rate (fh) to predict oxygen consumption rates (VO2) in Steller sea lions and other pinnipeds has been investigated in fasting animals. However, it is unknown whether established fh:VO2 relationships hold under more complex physiological situations, such as when animals are feeding or digesting. We assessed whether fh could accurately predict VO2 in trained Steller sea lions while fasting and after being fed. Using linear mixed-effects models, we derived unique equations to describe the fh:VO2 relationship for fasted sea lions resting on land and in water. Feeding did not significantly change the fh:VO2 relationship on land. However, Steller sea lions in water displayed a different fh:VO2 relationship after consuming a 4 kg meal compared to the fasting condition. Incorporating comparable published fh:VO2 data from Steller sea lions showed a distinct effect of feeding after a 6 kg meal. Ultimately, our study illustrated that both feeding and physical environment are statistically relevant when deriving VO2 from telemetered fh, but that only environment affects the practical ability to predict metabolism from fh. Updating current bioenergetic models with data gathered using these predictive fh:VO2 equations will yield more accurate estimates of metabolic rates of free-ranging Steller sea lions under a variety of physiological, behavioral, and environmental states.

abstract
Transit costs associated with commuting between resting sites ashore and foraging areas at sea are an appreciable portion of foraging expenditures in pinnipeds. We examined transit swimming in three Steller sea lions (Eumetopias jubatus) trained to follow a moving boat at different speeds and depths. We measured dive behavior (duration) and focused specifically on activity measures (fore-flipper stroking and ODBA, an overall measure of body motion), which may be proxies for metabolic expenditure. Sea lions appeared to increase efficiency while transiting at depths that approached three times their body diameters (mean depth = 151 ± 1 cm SEM, n = 87). Although the response was not uniform for all tested scenarios, all of the significant adjustments we observed to dive behavior and swimming mechanics supported an increased efficiency at this depth. An increase in transit speed (4.5 versus 3.5 knots surface speed) was associated with elevated flipper stroke frequencies (+5%) and stroke output (ODBA•stroke-1, +48%). Sea lions transiting against the flow of a tidal current had reduced dive durations (-10%), while total ODBA was consistently elevated (+8% overall). This response to tidal flow was accompanied either by elevated ODBA•stroke-1 (3.5 knots) or a parallel increase in stroking (4.5 knots). Our data demonstrate that small changes in the physical environment affect transiting in Steller sea lions, and imply that altered prey fields or changing ocean conditions can carry energetic consequences.

abstract
Muscle exercise correlates with oxygen use, tissue perfusion and heart rate (fH) in terrestrial animals, but the relationship between these physiological processes is less clear in diving animals. We found the mean heart rate of Steller sea lions trained to voluntarily dive to depths up to 40m dropped by 40% while diving, and noted that mean bradycardia was 9% greater during shallow (10m) compared to deep (40m) dives. Longer dives resulted in lower heart rates, but only when they were shallow; on the other hand, minimum instantaneous fH decreased consistently with dive duration. In general, instantaneous fH did not reflect activity over short timescales. Our data suggest that our sea lions invoked a different dive response depending on whether they dove to shallow or deep depths. During shallow (10m) dives only, the correlation between activity and fH was indicative of vascular compromise between diving and exercise. However, during deep dives (40m), there was no such correlation, suggesting that locomotory activity was uncoupled from dive bradycardia, which was possibly mediated by an absence of blood flow to active muscle. For both diving scenarios, surface fH correlated with dive activity, suggesting that some underwater locomotory costs were deferred to the post-dive surface interval. Ultimately, our data support the speculation that Steller sea lion locomotory muscles become hypoxic during diving, regardless of dive depth.

abstract
Variation in concentrations of thyroid hormones shed in feces may help to identify physiological states of animals, but the efficacy of the technique needs to be validated for each species. We determined whether a known physiological alteration to thyroid hormone production was reflected in hormone concentrations in the feces of Steller sea lions (Eumetopias jubatus). We quantified variation of triiodothyronine (T3) and thyroxine (T4) concentrations in feces following two intramuscular injections of thyrotropin (thyroid-stimulating hormone, TSH) at 24 h intervals in four captive female sea lions. We found fecal T3 concentrations increased 18-57% over concentrations measured in the baseline sample collected closest to the time of the first TSH injection (p=0.03) and 1-75% over the mean baseline concentration (p=0.12) for each animal of all samples collected prior to injections. The peak T3 response occurred 48 h post injection in three animals and 71 h in the fourth. Post-injection T4 concentrations did not differ between the baseline sample collected closest to the time of the first TSH injection (p=0.29) or the mean baseline concentration (p=0.23) for each animal. These results indicate that induced physiological alterations to circulating thyroid hormone concentrations can be adequately detected through analyses of fecal T3 concentrations and that the technique may provide a means of non-invasively detecting metabolic changes in Steller sea lions.

abstract
Fluctuations in availability of prey resources can impede acquisition of sufficient energy for maintenance and growth. By investigating the hormonal mechanisms of the somatotropic axis that link nutrition, fat metabolism, and lean tissue accretion, we can assess the physiological impact of decreased nutrient intake on growth. Further, species that undergo seasonal periods of reduced intake as a part of their normal life history may have a differential seasonal response to nutrient restriction. This experiment evaluated the influence of season and age on the response of the somatotropic axis, including growth hormone (GH), insulin-like growth factor (IGF)-I, and IGF-binding proteins (BP), to reduced nutrient intake and re-alimentation in Steller sea lions. Eight captive females (five juveniles, three sub-adults) were subject to 28-day periods of food restriction, controlled re-feeding, and ad libitum recovery in summer (long-day photoperiod) and winter (short-day photoperiod). Hormone concentrations were insensitive to type of fish fed (low fat pollock vs. high fat herring), but sensitive to energy intake. Body mass, fat, and IGF-I declined, whereas GH and IGFBP-2 increased during feed restriction. Reduced IGF-I and IGFBP with increased GH during controlled re-feeding suggest that animals did not reach positive energy balance until fed ad libitum. Increased IGF-I, IGFBP-2, IGFBP-3, and reduced GH observed in summer reflected seasonal differences in energy partitioning. There was a strong season and age effect in the response to restriction and re-alimentation, indicating that older, larger animals are better able to cope with stress associated with energy deficit, regardless of season.

abstract
Stable isotope analysis is often used to examine diet choice and tropic relationships in marine mammals. However, the technique makes a number of largely untested assumptions. For example, researchers often assume localized biopsies to be representative of the whole animal—that is, that the isotopic signal is homogenous within a tissue. Further, isotopic composition may differ across the body within the same tissue type due to differential assimilation or catabolization rates. We investigated the homogeneity of 13C and 15N values in skin and muscle across the body per individual in three pinniped species: Steller sea lions (Eumetopias jubatus, n = 5), California sea lions (Zalophus californianus, n = 6), and harbor seals (Phoca vitulina, n = 7). We also assessed if there are consistent carbon and nitrogen isotope differences between these two commonly sampled tissues. Our results show that skin tissue was significantly 13C enriched when compared to muscle tissue, and more difficult to properly process. Despite expected differences across the body in physiological processes and biochemical composition, our data indicate stable isotope signal homogeneity across the body within both muscle and skin, for both carbon and nitrogen isotopes, in all three species. These results indicate that sufficient homogeneity exists within skin and muscle tissues to suggest that point sampling can be considered representative of entire tissues, and is thus a valid technique in stable isotope studies of marine mammals.

abstract
We attached accelerometers to the head and jaw of a Steller sea lion (Eumetopias jubatus) to determine whether feeding attempts in a controlled setting could be quantified by acceleration features characteristic of head and jaw movements. Most of the 19 experimental feeding events that occurred during the 51 dives recorded resulted in specific acceleration patterns that were clearly distinguishable from swimming accelerations. The differential acceleration between the head-mounted and jaw-mounted accelerometers detected 84% of prey captures on the vertical axis and 89% on the horizontal axis. However, the jaw-mounted accelerometer alone proved to be equally effective at detecting prey capture attempts. Acceleration along the horizontal (surge)-axis appeared to be particularly efficient in detecting prey captures, and suggests that a single accelerometer placed under the jaw of a pinniped is a promising and easily implemented means of recording prey capture attempts.

abstract
Physiological responses to changes in energy balance are tightly regulated by the endocrine system through glucocorticoids, IGF-I and thyroid hormones. Changes in these hormones were studied in eight captive female Steller sea lions that experienced changes in food intake, body mass, body composition, and blood metabolites during summer and winter. During a period of energy restriction, one group of sea lions was fed reduced amounts of Pacific herring and another was fed an isocaloric diet of walleye pollock, after which both groups returned to their pre-experimental diets of herring. Cortisol was negatively and IGF-I was positively associated with changes in body mass during periods of energy restriction (mass loss associated with increase in cortisol and decrease in IGF-I) and refeeding (body mass maintenance associated with stable hormone concentrations in summer and compensatory growth linked to decrease in cortisol and increase in IGF-I in winter). Cortisol and IGF-I were also correlated with changes in lipid and lean mass, respectively. Consequently, these two hormones likely make adequate biomarkers for nutritional stress in sea lions, and when combined provide indication of the energetic strategy (lipid vs lean mass catabolism) animals adopt to cope with changes in nutrient intake. Unlike type of diet fed to the sea lions, age of the animals also impacted hormonal responses, with younger animals showing more intense hormonal changes to nutritional stress. Thyroid hormones, however, were not linked to any physiological changes observed in this study.

abstract
Two groups of female Steller sea lions (Groups H and P) were subjected to periods of energy restriction and subsequent re-feeding during winter and summer to determine changes in energy partition among principal physiological functions and the potential consequences to their fitness. Both sea lion groups consumed high-quality fish (herring) before and after the energy restrictions. During restrictions, Group H was fed a lower quantity of herring and Group P a caloric equivalent of low-quality fish (pollock). Quantitative estimates of maintenance and production energies and qualitative estimates of thermoregulation, activity and basal metabolic rate were measured. During summer, all animals compensated for the imposed energy deficit by releasing stored energy (production energy). Group H also optimized the energy allocation to seasonal conditions by increasing activity during summer when fish are naturally abundant (foraging effort) and by decreasing thermoregulation capacity when waters are warmer. During winter, both groups decreased the energy allocated to overall maintenance functions (basal metabolic rate, thermoregulation and activity together) in addition to releasing stored energy, but preserved thermoregulatory capacity. Group H also decreased activity levels in winter when foraging in the wild is less efficient, unlike Group P. Overall, sea lions fed pollock did not change energy allocation to suit environmental conditions as readily as those fed herring. This implies that low energy density diet may further reduce fitness of animals in the wild during periods of nutritional stress.

abstract
Nine Steller sea lions (Eumetopias jubatus) aged 1.756 yr were experimentally fasted for 714 d during the breeding and nonbreeding seasons to identify changes in plasma metabolites that are indicative of fasting and to determine whether the ability of sea lions to fast varies seasonally or with age. Although some animals approached the limit of their protein-sparing ability by the end of our fasting experiments, there was no sign of irreversible starvation biochemistry. Plasma blood urea nitrogen (BUN) concentrations decreased in all animals within the first week of fasting, reflecting a shift to a fasting-adapted state; however, significant increases in plasma BUN concentration at the end of the nonbreeding season fasts suggest that subadult Steller sea lions were not able to maintain a protein-sparing metabolism for a full 14 d during the nonbreeding season. In contrast, juveniles were able to enter protein sparing sooner during the nonbreeding season when they had slightly higher initial percent total body lipid stores than during the breeding season. Subadult and juvenile sea lions had low circulating ketone body concentrations compared with young sea lion pups, suggesting an age-related difference in how body reserves are utilized during fasting or how the resulting metabolites are circulated and catabolized. Our data suggest that metabolite concentrations from a single blood sample cannot be used to accurately predict the duration of fast; however, threshold metabolite concentrations may still be useful for assessing whether periods of fasting in the wild are unusually long compared with those normally experienced.

abstract
1. Numbers of Steller sea lions Eumetopias jubatus in the North Pacific have declined. According to the Nutritional Stress Hypothesis, this decline is due to reduced food availability. Data from studies conducted on pinnipeds in the laboratory are used here to test whether the Nutritional Stress Hypothesis can explain the decline of Steller sea lions. 2. Overall, there is strong evidence for biologically meaningful differences in the nutritional quality of major prey species. Steller sea lions can partly compensate for low-quality prey by increasing their food consumption. 3. There appear to be no detrimental effects of low-lipid prey on sea lion growth or body composition when sea lions can consume sufficient quantities of prey. However, the ability to increase consumption is physiologically limited, particularly in young animals. Overall, it is more difficult to maintain energy intake on a diet of low-quality prey than on a normal diet. 4. Under conditions of inadequate food intake (either due to decreased prey availability or quality, or increased energy requirements) the overall impacts of nutritional stress are complex, and are dependent upon season, prey quality, age, and the duration and intensity of the nutritional stress event. 5. Studies on pinnipeds in the laboratory have been instrumental in identifying the conditions under which changes in sea lion prey can result in nutritional stress, and the nature of the physiological impacts of nutritional stress events.

abstract
Changes in metabolic rates were measured in 3 captive female Steller sea lions (Eumetopias jubatus) that experienced fasts during summer and winter. Metabolic rates were measured (via O₂ consumption) before (MRs, surface) and after (DMR, dive + surface interval) the sea lions dove to 10–50 m depths. Measurements were obtained prior to 9-10 day fasts, and following a 14 day recovery period. The sea lions lost significantly more body mass (M_b) during the winter fast (10.6%), compared with the summer (9.5%). Mass-corrected dive metabolic rate (_cDMR = DMR • M_b^-0.714) was not affected by dive depth or duration, but increased significantly following the winter fasts (13.5 ± 8.1%), unlike the decrease during summer (-1.1 ± 3.2%). However, mass-corrected surface metabolic rate (_cMR_s) decreased significantly after both the summer (-16.4 ± 4.7%) and winter (-8.0 ± 9.0%) fasts. Consequently, the ratio between _cDMR and _cMR_c was significantly higher in winter, suggestive of an increased thermal challenge and convective heat loss while diving. Increased _cDM_s following the fast indicated that digestion began during foraging and was not deferred, implying that access to ingested energy was of higher priority than optimizing diving ability. _cDMR was elevated throughout the recovery period, independent of season, resulting in a 12% increase in foraging cost in winter and a 3% increase in summer. Our data suggest that Steller sea lions are more sensitive to changes in body condition due to food shortages in the winter compared with the summer.

abstract
The metabolic costs of foraging and the management of O₂ stores during breath-hold diving was investigated in three female Steller sea lions (Eumetopias jubatus) trained to dive between 10 and 50 m (n=1142 dives). Each trial consisted of 2 to 8 dives separated by surface intervals (SI) that were determined by the sea lion (spontaneous trials) or by the researcher (conditioned trials). During conditioned trials, SI was long enough for O₂ to return to pre-dive levels between each dive. The metabolic cost of each dive event (DMR = dive + surface interval) was measured using flow-through respirometry. The respiratory exchange ratio (VCO₂ ·VCO₂ ^-1) was significantly lower during spontaneous trials compared with conditioned trials. DMR was significantly higher during spontaneous trials and decreased exponentially with dive duration. A similar decrease in DMR was not as evident during conditioned trials. DMR could not be accurately estimated from the SI following individual dives that had short surface intervals (SI < 50 sec), but could be estimated on a dive by dive basis for longer SIs (SI > 50 sec). DMR decreased by 15%, but did not differ significantly from surface metabolic rates (MR_S) when dive duration increased from 1 to 7 min. Overall, these data suggest that DMR is almost the same as MR_S, and that Steller sea lions incur an O₂ debt during spontaneous diving that is not repaid until the end of the dive bout. This has important consequences in differentiating between the actual and ‘apparent’ metabolic rate during diving, and may explain some of the metabolic differences reported between pinniped species.

abstract
hanges in buoyancy due to seasonal or abnormal changes in body composition are thought to significantly affect the energy budget of marine mammals through changes in diving costs. We assessed how changes in body composition might alter the foraging efficiency of Steller sea lions Eumetopias jubatus by artificially adjusting the buoyancy of trained individuals. PVC tubes were attached to harnesses worn by Steller sea lions that had been trained to feed at fixed depths (10 to 30 m) and to resurface inside a metabolic dome. Buoyancy was altered to simulate the naturally occurring differences in body composition reported in adult females (~12 to 26% subcutaneous fat). Diving characteristics (transit times and time at depth) and aerobic energy expenditure (gas exchange) were measured. We found that foraging cost decreased with the duration of the dive and increased with dive depth. However, changes in body composition did not affect the diving metabolic rate of Steller sea lions for dives between 10 and 30 m. We propose that Steller sea lions may adjust their diving lung volume to compensate for changes in buoyancy to avoid additional metabolic costs.

abstract
Three Steller sea lions Eumetopias jubatus were trained to participate in free-swimming, open-ocean experiments designed to determine if activity can be used to estimate the energetic cost of finding prey at depth. Sea lions were trained to dive to fixed depths of 10 to 50 m, and to re-surface inside a floating dome to measure energy expenditure via gas exchange. A 3-axis accelerometer was attached to the sea lions during foraging. Acceleration data were used to determine the overall dynamic body acceleration (ODBA), a proxy for activity. Results showed that ODBA correlated well with the diving metabolic rate (dive + surface interval) and that the variability in the relationship (r2 = 0.47, linear regression including Sea lion as a random factor) was similar to that reported for other studies that used heart rate to estimate metabolic rate for sea lions swimming underwater in a 2 m deep water channel. A multivariate analysis suggested that both ODBA and dive duration were important for predicting diving metabolic cost, but ODBA alone predicted foraging cost to within 7% between animals. Consequently,collecting 3-dimensional acceleration data is a simple technique to estimate field metabolic rate of wild Steller sea lions and other diving mammals and birds.

abstract
Controlled feeding experiments were undertaken with captive Steller sea lions (Eumetopias jubatus) to assess seasonal (winter vs. summer) physiological responses of individual animals to reduced quantities and qualities of food that are hypothesised to occur in the wild. Eight animals were randomly divided into two experimental groups fed isocaloric diets: Group H ate Pacific herring (Clupea pallasi) throughout the experiment while Group P was switched to walleye pollock (Theragra chalcogramma) during a 28-day food restriction (after a 28-day baseline) and back to herring during a 28-day controlled re-feeding. Diet type did not impact the rates of body mass lost when food was restricted, but did influence the type of internal energy reserve (protein vs lipids) the sea lions predominantly used. In both summer and winter, Group H lost significantly more lipids and less lean mass than Group P that was fed pollock during the restriction phase. The response of Group H was consistent with the predicted pattern of nutritional stress physiology (i.e. protein sparing and utilization of lipid reserves). Group P lost a surprisingly high proportion of body protein while consuming restricted levels of pollock, which could lead to muscle impairment and vital organ failure on a long-term basis. When given increased amounts of herring during the controlled re-feeding phase, the capacity of both groups to compensate for the previous mass loss was found to depend on season and was independent of previous diet. All of the sea lions increased their rates of mass gain and returned to their pre-experimental weight during winter, but not during summer. Some intrinsic energetic plasticity related to seasonal adaptation to the environment may render winter an easier period than summer to recover from nutritional stress.

abstract
Given that many marine mammals display seasonal energetic priorities, it is important to investigate whether the impact of unexpected food restriction differs during the year. Steller sea lions (Eumetopias jubatus) fed restricted diets for up to 9 days during spring, summer, fall, and winter lost an average of 10% of their initial body mass. We tracked changes in the levels of three hormones (cortisol, total thyroxine—TT4, total triiodothyronine—TT3) and one blood metabolite (blood urea nitrogen—BUN) following a food restriction in relation to season, body mass, body composition, and metabolism. Degree of changes in cortisol, TT3, and BUN after food restriction was significantly affected by season. The greatest changes in cortisol (+231%), BUN (+11.4%), TT4 (-23.3%), and TT3 (-35.6%) occurred in the winter (November/December) when rates of body mass loss were also greatest. Changes in cortisol levels were positively related to total body mass loss, while changes in TT3 levels were negatively related. While greater increases in BUN were related to greater rates of mass loss, the use of BUN levels as an indicator of metabolic state is complicated by the type and level of food intake. The observed changes in hormone levels support morphological data suggesting Steller sea lions may be more strongly impacted by short-term, reduced energy intake during winter than at other times of the year.

abstract
Twenty-two participants from a variety of backgrounds and interests discussed how to improve the nature of research with marine mammals in the laboratory and ensure its continuation as a vital scientific resource in the future. There was agreement that captive marine mammals represent a valuable scientific asset. Many of the pressing conservation and scientific research questions pertaining to marine mammals cannot be carried out with their wild counterparts. However, studying marine mammals in the laboratory incurs specific financial, scientific, and logistical challenges. The workshop generated potential solutions to many of these issues. Participants expressed the need for greater cooperation and coordination between scientists to optimize the scientific value of research with captive marine mammals, and to minimize the costs of such research. This could be enhanced through scheduled in-person gatherings and web-based portals for listing active and proposed research. Better use must also be made of scientific resources and expertise, and novel sources of revenue have to be generated. There should also be greater sharing of documents relating to experimental design and research permitting. The effectiveness of research will benefit from greater communication between researchers and husbandry staff at institutions holding animals for research. Such efforts should raise the profile (and acceptance) of captive marine mammals science within the scientific community and for program administrators, leading to greater financial and research opportunities. Nine specific recommendations were forwarded that could be immediately implemented to enhance communication and increase the value of captive marine mammal science: 1. Produce a list of research resources (animals, specialized skills and equipment); 2. Create a list of on-going captive marine mammal studies; 3. Produce a list of publications derived from research with captive marine mammals; 4. Develop a set of guidelines for communication, responsibilities, and intellectual ownership for collaborative projects; 5. Implement means for coordination of future studies (both web-based and scheduled workshop/meetings); 6. Design a means for sharing standard Operating Procedures; 7. Hold a workshop to increase statistical rigor and standards in experimental design; 8. Introduce the use of annual survival rates into institutions holding marine mammals; and 9. Heighten the awareness of the value and prevalence of captive studies to the Us Marine Mammal Commission.

abstract
Accurate estimates of diving metabolic rate are central to assessing the energy needs of marine mammals. To circumvent some of the limitations inherent with conducting energy studies in both the wild and captivity, we measured diving oxygen consumption of two trained Steller sea lions (Eumetopias jubatus) in the open ocean. The animals dived to predetermined depths (5–30 m) for controlled periods of time (50–200 s). Rates of oxygen consumption were measured using open-circuit respirometry before and after each dive. Mean resting rates of oxygen consumption prior to the dives were 1.34 (±0.18) and 1.95 (±0.19) liter/min for individual sea lions. Mean rates of oxygen consumption during the dives were 0.71 (±0.24) and 1.10 (±0.39) liter/min, respectively. Overall, rates of oxygen consumption during dives were significantly lower (45% and 41%) than the corresponding rates measured before dives. These results provide the first estimates of diving oxygen consumption rate for Steller sea lions and show that this species can exhibit a marked decrease in oxygen consumption relative to surface rates while submerged. This has important consequences in the evaluation of physiological limitations associated with diving such as dive duration and subsequent interpretations of diving behavior in the wild.

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Nine captive Steller sea lions (Eumetopias jubatus (Schreber, 1776), 1.75–6 years of age) were fasted for 7–14 d to test the effect of short-term fasting on changes in body mass and body condition. Trials were repeated during both the summer breeding season and the nonbreeding season in seven animals to elucidate whether there was a seasonal component to the ability of Steller sea lions to adapt to limited food resources. Mean percent mass loss per day was higher during the breeding season in juveniles (1.8% ± 0.2%·d–1) than in subadults (1.2% ± 0.1%·d–1), but there were no significant age-related differences during the nonbreeding season (juveniles, 1.5% ± 0.3%·d–1; subadults, 1.7% ± 0.3%·d–1). A decrease in the rate of mass loss occurred after the first 3 d of fasting only in subadults during the breeding season. Percent total body lipid ranged from 11% to 28% of total body mass at the initiation of fasting trials. Animals with lower initial percent total body lipid exhibited higher subsequent rates of mass loss and a lower percentage of tissue catabolism derived from lipid reserves. There was no evidence of metabolic adaptation to fasting in juveniles, which suggests that juvenile sea lions would be more negatively impacted by food limitation during the breeding season than would subadults.

abstract
While foraging models of terrestrial mammals are concerned primarily with optimizing time/energy budgets, models of foraging behavior in marine mammals have been primarily concerned with physiological constraints. This has historically centered on calculations of aerobic dive limits. However, other physiological limits are key to forming foraging behavior, including digestive limitations to food intake and thermoregulation. The ability of an animal to consume sufficient prey to meet its energy requirements is partly determined by its ability to acquire prey (limited by available foraging time, diving capabilities and thermoregulatory costs) and to process that prey (limited by maximum digestion capacity and the time devoted to digestion). Failure to consume sufficient prey will have feedback effects on foraging, thermoregulation, and digestive capacity through several interacting avenues. Energy deficits will be met through catabolism of tissues, principally the hypodermal lipid layer. Depletion of this blubber layer can affect both buoyancy and gait, increasing the costs and decreasing the efficiency of subsequent foraging attempts. Depletion of the insulative blubber layer may also increase thermoregulatory costs, which will decrease foraging abilities through higher metabolic overheads. Thus, an energy deficit may lead to a downward spiral of increased tissue catabolism to pay for increased energy costs. Conversely, the heat generated through digestion and foraging activity may help to offset thermoregulatory costs. Finally, the circulatory demands of diving, thermoregulation, and digestion may be mutually incompatible. This may force animals to alter time budgets to balance these exclusive demands. Analysis of these interacting processes will lead to a greater understanding of the physiological constraints within which foraging behavior must operate.

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The costs associated with diving are a central component of a sea lions? energy budget. Accurate estimates of diving costs are needed to assess energetic and physiological constraints on foraging behavior, including the potential effects of changes in prey distribution or density. However, information on sea lion diving physiology is limited to relatively few species of pinnipeds, and there is currently no information for Steller sea lions. Information on diving energetics of pinnipeds has traditionally been gathered using either wild or captive animals. However, studies with wild animals are logistically challenging and are limited by the opportunistic nature of data collection, whilst studies in captivity have been constrained by the physical restrictions of the holding facility. To circumvent some of these limitations, we combined the best aspects of both techniques by conducting diving metabolism studies with trained Steller sea lions in an open ocean environment. Two captive-reared Steller sea lions were housed in a holding pen and transported by boat to a diving trial area. The animals were trained to dive to predetermined depths for controlled periods of time using an underwater light targeting system and a video system to monitor behavior. At the end of each dive the sea lions returned to a respirometry dome on the surface where oxygen consumption was measured to estimate diving metabolism. This paper describes the experimental setup used to evaluate diving metabolism, discusses the logistical challenges of the study and the advantages of using such an approach to carry out physiological experiments with sea lions, and provides preliminary data on the diving energetics of Steller sea lions.

abstract
Diving animals must endeavor to increase their dive depths and prolong the time they spend exploiting resources at depth. Results from captive and wild studies suggest that many diving animals extend their foraging bouts by decreasing their metabolisms while submerged. We measured metabolic rates of Steller sea lions (Eumetopias jubatus) trained to dive to depth in the open ocean to investigate the relationships between diving behaviour and the energetic costs of diving. We also constructed a general linear model to predict the oxygen consumption of sea lions diving in the wild. The resultant model suggests that mean swimming distance and depth of dives significantly influence the oxygen consumption of diving Steller sea lions. The predictive power of the model was tested using a cross-validation approach, whereby models reconstructed using data from pairs of sea lions were found to accurately predict the oxygen consumption of the third diving animal. Predict! ed oxygen consumption during dives to depth ranged from 3.37 L min-1 at 10 meters, to 1.40 L min-1 at 300 meters over a standardized swimming distance of 600 meters. This equated to an estimated metabolic rate of 97.54 and 40.52 MJ day-1, and an estimated daily feeding requirement of 18.92 and 7.96 kg day-1 for dives between 10 and 300 meters, respectively. The model thereby provides information on the potential energetic consequences that alterations in foraging strategies due to changes in prey availability could have on wild populations of sea lions.

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Steller sea lions (Eumetopias jubatus) were fed restricted iso-caloric amounts of Pacific herring (Clupea pallasi) or walleye pollock (Theragra chalcogramma) for 8-9 days, four times over the course of a year to investigate effects of season and prey composition on sea lion physiology. At these levels, the sea lions lost body mass at a significantly higher rate during winter (1.6 ± 0.14 kg d-1), and at a lower rate during summer (1.2 ± 0.32 kg d-1). Decreases in body fat mass and standard metabolic rates during the trials were similar throughout the seasons and for both diet types. The majority of the body mass that was lost when eating pollock derived from decreases in lipid mass, while a greater proportion of the mass lost when eating herring derived from decreases in lean tissue, except in the summer when the pattern was reversed. Metabolic depression was not observed during all trials despite the constant loss of body mass. Our study supports the hypothesis that restricted energy intake may be more critical to Steller sea lions in the winter months, and that the type of prey consumed (e.g., herring or pollock) may have seasonally-specific effects on body mass and composition.

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Little is known about the mechanism in which decreased nutrient intake influences the physiology of Steller sea lions. By investigating the factors that link nutrition, fat metabolism and lean tissue accretion, we can assess the impact of decreased nutrient intake on energy storage and lean tissue growth, which may have implications for survival. Captive Steller sea lion females (n = 8, 2 to 5 year of age) were used to examine changes in the somatotropic axis in response to decreased nutrient intake. Animals were placed on a normal herring maintenance diet for 1 month. After this 1 month ‘baseline’ period four animals were placed on a herring submaintenance diet and four animals were fed an isocaloric Pollock submaintenance diet for 1 month. During the 1 month submaintenance period, the animals lost 10 to 15% of their body mass. In the 1 month re-alimentation period, only three animals increased mass to their initial value. Concentrations of IGF-I followed the expected pattern paralleling changes in intake. Concentrations of GH were more variable than IGF-I. Concentrations of IGFBP generally followed the expected response based on domestic animal research. The overall concentration of IGFBP-3 declined with decreased nutrient intake. In contrast, IGFBP-2 increased with decreasing nutrient intake.

abstract
hanges in the proximate composition of prey can result in a nutritional imbalance in individual animals, regardless of total energy intake. This mechanism has been hypothesized to have contributed to the decline of Steller sea lions (Eumetopias jubatus). Yet little is known about how otariids react physiologically to short-term changes in prey quality and availability. A series of studies with young captive Steller sea lions tested several potential links between prey quality and sea lion health. Body composition (fat to total mass ratio) of animals fed constant, maintenance-level, isocaloric diets of high- or low-lipid prey changed with season, but overall was not aff ected by prey composition. The sea lions appeared to prioritize maintaining core growth rates even when energy was limited, electing to deplete lipid reserves to fulfi ll energy defi cits, resulting in changes in relative body condition. In contrast, sea lions subject to short- term, sub-maintenance diets of high- or low-lipid prey utilized a greater portion of their lipid reserves when losing body mass on low lipid prey. Experiments with diff erent ad libitum feeding regimes indicated that sea lions are readily able to alter food intake levels to compensate for diff erences in prey energy content and, to a lesser degree, prey availability. However, the results also suggest that decreases in prey quality and/or foraging opportunities can readily combine to require food intake levels that are greater than the digestive capacity of the individual. This is particularly true for young animals that may already be living ?on the edge? energetically.

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Marine mammals face distinct environmental conditions that can translate into unique physiological challenges. Studies of foraging behavior in marine (diving) mammals have primarily focused on how the physiological constraint of aerobic dive limits defines their strategies. However, there are other physiological constraints that shape foraging patterns in marine mammals that are often neglected. This paper discusses the interaction of three broad physiological processes that impose limitations on foraging patterns: the physiological demands of prey acquisition (foraging), prey processing (digestion), and thermoregulation. The theoretical framework presented allows us to review and synthesize the complex physiological interactions that shape foraging behavior at the individual level. Observed foraging behavior is an integration of a multitude of competing demands on an animal. The aim of this framework is to enhance our understanding of these processes and direct areas of future research.

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Accurate estimates of diets are vital to monitor impacts of sea lion populations on their ecosystems, their interactions with fisheries and to understand the role of food to animal nutrition and health. Approaches include using: (1) prey remnants in stomach contents, spews and scats, (2) prey DNA in scats (3) fatty acid signatures in blubber and (4) stable isotope ratios in predator's tissue. Each methodology has particular advantages and limitations, many of which can be assessed and improved through controlled captive feeding trials. Analysis of prey remnants from captive sea lion scats have shown significant variability in digestion between and within prey species, which coupled with preferential regurgitation and enumeration biases, can confound accurate diet quantification, but does not prevent spatial or temporal comparisons. Correction for partial digestion and use of additional structures besides otoliths can provide accurate prey size estimates. Prey DNA can be reliably isolated from soft remains in scats from captive sea lions and with further development this approach may allow quantification of diet. Genetic methods can be expensive and representative of only one to two days foraging (like prey remnant analysis), but may be less affected by differential digestion and can identify prey in scats that could not be identified through structural remnants. Validation of fatty acid signature analysis to quantify diet at longer temporal scales in sea lions is ongoing, but this new technique promises to be particularly useful to assess biases in traditional methods, identify the onset of weaning and to highlight what prey most contribute to lipid reserves. Stable isotope analysis of predator tissues gives only trophic level data, but can provide data on diet changes on many temporal scales. Remote video monitoring of foraging events and lavage/enema techniques can provide valuable diet information, but, like many newer techniques, animal capture is required. Ideally a suite of techniques should be used to study diet. While methods and correction factors developed for Steller sea lions can likely be applied to the other five sea lion species, they should be verified experimentally.

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Behavioral observations of lactating Steller sea lions (Eumetopias jubatus) and their offspring were recorded at 4 haulout sites in Alaska to determine: 1) whether sea lions wean during winter while they are 7-9 months old, and 2) whether sea lions using sites in the Gulf of Alaska (the declining endangered population) made longer foraging trips than sea lions in Southeast Alaska (where the population appeared larger and healthier). Longer foraging trips are commonly thought to be an indicator of nutritional stress. Eight sets of behavioral observations were made using focal and scan sampling techniques at haulouts over 4 years (1995-1998) during 3 seasons (winter, spring and summer). Counter to expectations, we found no significant differences between haulout populations in the time that lactating Steller sea lions spent at sea or on shore. This suggests that sea lions did not have more difficulty capturing prey from winter through summer in the area of decline compared to where sea lion numbers increased. However, lactating Steller sea lions in both regions made longer foraging trips in winter than they did in spring and summer. These changes in foraging patterns between seasons were consistent among all years and sites. The proportion of time that immature Steller sea lions suckled declined through the spring to early summer, suggesting that sea lions began supplementing their milk diet with solid food in the spring. We did not observe any sea lions weaning during winter. Rather, most appeared to wean at the start of the breeding season when they were 1 or 2 y old. Sea lions observed in Southeast Alaska during the late 1990s while population growth was slowing suggest that most males weaned at 2 y, and that about 50% of females weaned at 1 y and the remainder at 2 y.

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Knowing the quantity of prey that sea lions consume is a prerequisite for assessing the role of sea lions in aquatic ecosystems and the potential for competition to occur with fisheries. We reviewed the different approaches that have been used to estimate the food requirements for the six species of sea lions. We reviewed data on the quantity of food consumed by sea lions in captivity, and examined how consumption varied by species, body size, and season. We also reviewed and quantified available information on the energetics of sea lions and assessed the potential application of these data to parameterize an existing bioenergetic model that was developed to estimate the food requirements of Steller sea lions. Our study provided ranges of estimates of food consumption for sea lions that can be used in various modeling strategies to assess the impact of sea lions on prey populations, including commercially exploited fish species. The approaches reviewed in our study shared common difficulties arising from the quantity and quality of data, and the integration of data across scales and species. Our modeling exercise, in particular, identified the major uncertainties involved in estimating the food requirements of each sea lion species using an energetics approach. Our results provide direction for future research aimed at improving the accuracy and comparability of estimates of food consumption for sea lions.

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The effects of high- and low-lipid prey on the body mass, body condition, and metabolic rates of young captive Steller sea lions (Eumetopias jubatus) were examined to better understand how changes in prey composition might impact the physiology and health of wild sea lions and contribute to their population decline. Results of three feeding experiments suggest that prey lipid content did not significantly affect body mass or relative body condition (lipid mass as a percent of total mass) when sea lions could consume sufficient prey to meet their energy needs. However, when energy intake was insufficient to meet daily requirements, sea lions lost more lipid mass (9.16±1.80 kg±SE) consuming low-lipid prey compared with eating high-lipid prey (6.52±1.65 kg). Similarly, the sea lions lost 2.7±0.9 kg of lipid mass while consuming oil-supplemented pollock at maintenance energy levels but gained 5.2±2.7 kg lipid mass while consuming identical energetic levels of herring. Contrary to expectations, there was a 9.7±1.8% increase in metabolism during mass loss on submaintenance diets. Relative body condition decreased only 3.7±3.8% during periods of imposed nutritional stress, despite a 10.4±4.8% decrease in body mass. These findings raise questions regarding the efficacy of measures of relative body condition to detect such changes in nutritional status among wild animals. The results of these three experiments suggest that prey composition can have additional effects on sea lion energy stores beyond the direct effects of insufficient energy intake.

abstract
Maintaining insulative fat stores is vital for homeothermic marine mammals foraging in cold polar waters. To accomplish this, animals must balance acquisition and expenditure of energy. If this balance is shifted, body condition can decrease, challenging thermal homeostasis and further affecting energy balance. Prior studies of temperature regulation in sea lions have neither quantified basic all-inclusive heat flux values for animals swimming in cold water, nor determined whether they exhibit consistent spatial patterns of heat flux. Heat flux and skin temperature data were thus collected from four captive Steller sea lions using heat flux sensors (HFSs) with embedded thermistors. Optimal sensor placement was established using infrared thermography to locate the major areas of heat flux along the surface of the animals. Experiments were conducted on swimming animals in a large habitat tank with and without a drag harness, and on stationary animals in a temperature- and current controlled swim flume. All heat flux measurements were corrected by a previously determined correction factor of 3.42 to account for insulative effects of the HFSs and attachment mechanism. Heat flux from shoulders and hips was consistently greater than from mid-trunk and axillary areas in both swimming and stationary animals, suggesting that certain areas of the body are preferentially used to offload excess heat. Mean heat flux for animals swimming with a drag harness was significantly greater than for unencumbered animals, indicating a likely increase in heat production beyond minimum heat loss. Thus, thermal stress does not appear to constitute significant costs for Steller sea lions swimming under conditions of increased drag at speeds of approximately 1 m/s in water temperatures of approximately 8.0 °C.

abstract
The objectives of this study were to compare Resting Metabolic Rate (RMR) from animals in the eastern and western Alaskan populations to discern whether there is any evidence of nutritional stress. Oxygen consumption data were collected from captive Steller sea lions held at the Vancouver Aquarium, Vancouver, BC and from free-ranging Steller sea lions captured from western and eastern Alaskan stocks. In water, RMR ranged from 33.3 to 56.7 MJ/day for sub-adult animals (109-158 kg, 2.9-4.6 times predicted for an adult animal) and from 20.0 to 26.6 MJ/day for pups (57-59 kg, 3.3-4.3 times predicted) at 2°C. RMR, generally decreased with increasing water temperature, but the relationship was not statistically significant. Reduced body condition had a noticeable impact on RMR in juvenile sea lions at colder water temperatures. The results of the present study suggest that young sea lions would be subject to even greater thermoregulatory demands if their body condition were reduced.

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This experiment examined the response of a suite of hematologic parameters to experimentally induced nutritional stress in a group of captive Steller sea lions. The goal was to identify a suite of parameters that could be used to diagnose comparable conditions among wild Steller sea lions. Previous studies, many with ruminant mammals, have shown that there are significant changes in blood characteristics with nutritional status. However, it is equally clear that there is no overwhelming choice of blood parameter to indicate nutritional stress across different species. Therefore, species-specific empirical tests such as the one carried out in the current study are essential to place results from wild studies in a biologically meaningful context.

abstract
Foraging theory predicts that animals should proportionately increase their food intake to compensate for reduced energy content and/or prey availability. However, the theoretical intake levels will – at some point – exceed the digestive capacity of the predator. We tested the ability of Steller sea lions (Eumetopias jubatus, Schreber, 1776) to compensate for short-term changes in prey energy density and availability, and quantified the maximum amount of food a young sea lion could consume. Five 1-2 year old captive Steller sea lions were alternately offered herring (high-energy) or capelin (low-energy) each day or every second day. When prey were available on a daily basis the sea lions compensated for differences in the energy content of herring and capelin by consuming sufficient quantities of each (8.3 vs. 14.0 kg d-1, respectively) to maintain an equivalent gross energy intake. When herring was available only on alternate days, the sea lions increased their consumption by 52% to 11.5 kg d-1, which was not sufficient to maintain an average gross intake equal to when herring was available every day. When capelin was available only on alternate days, some animals increased their intake for a few days, but average intake (15.2 kg d-1) was far below levels observed during daily feeding. Generally, the sea lions appeared to reach their digestive limit at a level equivalent to 14-16% of their body mass. Our findings suggest that Steller sea lions can alter their food intake in response to short-term changes in prey quality or availability, but that these variables can quickly combine to necessitate food intake levels that exceed the physiological digestive capacities of young animals.

abstract
This experiment examined the response of a suite of hematologic parameters to experimentally induced nutritional stress in a group of captive Steller sea lions. The goal of this study was to identify a suite of parameters that could be used to diagnose comparable conditions among wild Steller sea lions. The experiments were conducted with four captive female Steller sea lions. They were alternated between isocaloric diets of Atka mackerel (4.9-6.7% lipid w.w.) and herring (10.3-13.4% lipid). The level of food intake (~35.6 kJ d-1) was set a priori at a level estimated to produce a 10-15% loss of initial body mass over the 29-day trials. Body mass was measured daily (± 0.1 kg), and body composition was determined at the start and end of each trial by deuterium dilution technique. Nine of the blood parameters measured in this study showed consistent changes over the 29-day period of induced nutritional stress. White blood cell counts, platelet counts, phosphorous levels, alkaline phosphatase levels, and serum Fe levels all showed consistent decreases, whilst red blood cell counts, hemoglobin levels, hematocrit levels, and gamma GT levels, showed consistent increases. Only one of the blood parameters showed a significantly different response in relation to diet - blood urea nitrogen (BUN) levels showed a consistent increase on the Atka mackerel diet and a consistent decrease on the herring diet (P=0.029). Sea lions on the Atka mackerel diet showed a mean percentage increase in BUN level of 9.2%, and a mean percentage decrease of 4.9% on the herring diet. Previous studies, many with ruminant mammals, have shown that there are significant changes in blood characteristics with nutritional status. However, it is equally clear that there is no overwhelming choice of blood parameter to indicate nutritional stress across different species. Therefore, species-specific empirical tests such as the one carried out in the current study are essential to place results from wild studies in a biologically meaningful context.

abstract
The validity of using heart rate to estimate energy expenditure in free-ranging Steller sea lions Eumetopias jubatus was investigated by establishing whether there is a relationship between heart rate (fH) and oxygen consumption rate (V . O·) in captive sea lions while swimming and resting. Four trained Steller sea lions (2 males and 2 females; mass 87.4–194.4·kg; age 16 months– 3 years) were each equipped with a datalogger and two dorsal subcutaneous electrodes to record electrocardiograms from which fH was calculated. V . O· (measured using open-circuit respirometry) was simultaneously recorded while the previously fasted animals were at rest within an enclosed dry metabolic chamber or while they swam in an enclosed swim mill against water currents of various speeds (0–1.5·m·s –1 ). The mean regression equation describing the relationship between fH (beats·min –1 ) and V . O· (ml·h –1 ·kg –0.60 ) for all four animals was V . O·=(71.3fH±4.3)–(1138.5±369.6) (means ± S.E.M.) (r 2 =0.69, P<0.01). The relationship demonstrated between fH and V . O· while fasting suggests that heart rate can potentially be used to monitor energy consumption in free-ranging Steller sea lions. However, a short-term feeding experiment revealed no significant increase in heart rate following a 6·kg or 12·kg meal to match the observed increase in rate of oxygen consumption. This suggests that heart rate may not accurately reflect energy consumption during digestion events. Additional research should be conducted to further elucidate how the relationship between heart rate and oxygen consumption is affected by such factors as digestive state, stress and age.

abstract
The increase in metabolism during digestion—the heat increment of feeding—is often regarded as an energetic waste product. However, it has been suggested that this energy could offset thermoregulatory costs in cold environments. We investigated this possibility by measuring the rate of oxygen consumption of four juvenile Steller sea lions (Eumetopias jubatus) before and after they ingested a meal in water temperatures of 2-8 degrees C. Rates of oxygen consumption of fasted and fed animals increased in parallel with decreasing water temperature, such that the apparent heat increment of feeding did not change with water temperature. These results suggest that Steller sea lions did not use the heat released during digestion to offset thermoregulatory costs.

abstract
We examined the digestion and passage times of bones and other hard parts from pollock, herring, salmon, and sandlance recovered from two juvenile captive Steller's sea lions (Eumetopias jubatus) subjected to varying activity levels. Key bones that could be identified to species were distributed over an average of 3.2 scats (range 1–6) following a single meal, with pollock remains occurring in significantly more scats than other species. Relying on otoliths alone to determine the presence of prey resulted in significantly fewer prey being identified than if other structures were also used (such as vertebrae, jaw bones, and teeth), particularly for salmon. Using either technique, there were significant differences in the likelihood that bones would be recovered from the series of scats produced following a meal, with pollock recovery exceeding herring (by three-fold) and sandlance (by eight-fold). Differences between species were reduced when recovery was calculated on a per scat basis rather than over multiple scats. Active animals passed greater numbers of bones, but the overall effect on prey recovery estimates was not significant. Defecation times of prey structures from a meal were variable and ranged from an initial 2–56 h to a final 28–148 h. The time interval to pass 95% of recovered structures varied by a factor of two among prey species, and was highest for pollock due to retention beyond 65 h.

abstract
The cost of swimming is a key component in the energy budgets of marine mammals. Unfortunately, data to derive predictive allometric equations are limited, and estimates exist for only one other species of otariid. Our study measured the oxygen consumption of three juvenile Steller sea lions (Eumetopias jubatus) swimming in a flume tank at velocities up to 2.2 m sec-1. Minimum measured cost of transport ranged from 3.5-5.3 J kg-1, m-1, and was reached at swimming speeds of 1.7-2.1 m s-1. These cost-of-transport values are higher than those reported for other marine mammals. However, once differences in stationary metabolic rate were accounted for, the locomotor costs (LC) for the Steller sea lions were commensurate with those of other marine mammals. Locomotor costs (LC in J m-1) appeared to be directly proportional to body mass (M in kg) such that LC = 1.651M1.01. These estimates for the cost of locomotion can be incorporated into bioenergetic models and used to determine the energetic consequences of observed swimming behavior in wild marine mammals.

abstract
Many animals lower their resting metabolism (metabolic depression) when fasting or consuming inadequate food. We sought to document this response by subjecting five Steller sea lions to periods of: (1) complete fasting; or (2) restricting them to 50% of their normal herring diet. The sea lions lost an average of 1.5% of their initial body mass per day (2.30 kg y d )during the 9 –14-day fast, and their resting metabolic rates decreased 31%, which is typical of a ‘fasting response ’. However, metabolic depression did not occur during the 28-day food restriction trials,despite the loss of 0.30% of body mass per day (0.42 kg y d). This difference in response suggests that undernutrition caused by reduced food intake may stimulate a ‘hunger response ’, which in turn might lead to increased foraging effort. The progressive changes in metabolism we observed during the fasts were related to, but were not directly caused by, changes in body mass from control levels. Combining these results with data collected from experiments when Steller sea lions were losing mass on low energy squid and pollock diets reveals a strong relationship between relative changes in body mass and relative changes in resting metabolism across experimental conditions.While metabolic depression caused by fasting or consuming large amounts of low energy food reduced the direct costs from resting metabolism, it was insufficient to completely overcome the incurred energy deficit.

abstract
Changes in the quality or quantity of food can have a dramatic effect on the population status of wild animals. Unfortunately, it is difficult to assess (or define) whether nutritional stress is a contributing factor to the decline of any particular species.The “nutritional quality ” of a diet to an animal is a complex matter to assess given the range of components that can influence its value.The effects of different diets on animal health are equally complex, and are particularly difficult to assess in large, wild animals. Research by the North Pacific Universities Marine Mammal Research Consortium with captive Steller sea lions is evaluating the possible mechanisms by which dietary changes might adversely affect the nutritional or health status of individual animals, and ultimately the population as a whole. The research investigates the three potential proximate mechanisms by which changes in diet might impact Steller sea lions:a decrease in energy intake, a decrease in the intake of some essential element, and the over-consumption of an element detrimental to sea lion health.

abstract
A generalized bioenergetic model was used to estimate the food requirements of Steller sea lions <i>Eumetopias jubatus</i> in Alaska, USA. Inputs included age and sex-specific energy require-ments by date, population size and composition, and diet composition and energy content. Error in model predictions was calculated using uncertainty in parameter values and Monte Carlo simulation methods. Our model suggests that energy requirements of individuals were generally lowest in the summer breeding season (June to August) and highest in the winter (December to February) and spring (March to May) mainly due to changes in activity budgets. Predicted relative daily food requirements were highest for young animals (12 ± 3% SD and 13 ± 3% of body mass for 1 yr old males and females respectively) and decreased with age (5 ± 1% and 6 ± 1% of body mass for 14 yr old males and 22 yr old females respectively). The mean daily food requirement of pregnant females predicted by the model was only marginally greater than the predicted mean daily food requirement of non-pregnant females of the same age. However, the model suggested that the mean daily food requirement of females nursing pups was about 70% greater than females of the same age without pups. Of the 3 sets of model parameters (diet, population, and bioenergetic), uncertainty in diet and bioenergetic parameters resulted in the largest variation in model predictions. The model provides a quantitative estimate of the Steller sea lion population’s food requirements and also suggests directions for future research.

abstract

Four Steller sea lions (Eumetopias jubatus) aged 6 weeks were fasted for 2.5 d to determine how young pups mobilize energy reserves during short periods of fasting similar to those experienced in the wild. At 6 weeks of age, the pups lost 5.1 ± 0.3% of their body mass during 2 d of fasting, with an average daily mass loss of 0.7 ± 0.1 kg·d –1 . Plasma blood urea nitrogen (BUN) concentration increased significantly from 3.0 ± 0.1 mM, after an over-night fast, to 4.8 ± 0.5 mM, after 2.5 d of fasting. It is apparent that BUN levels are quickly depressed, since after only an overnight fast, these pups showed BUN levels 2- to 4-fold lower than those measured after the same pups, when 9 months of age, had recently been fed fish. Plasma ketone body (b-HBA) concentrations of the 6-week-old pups increased significantly from 0.32 ± 0.08 to 0.42 ± 0.08 mM between 0.5 and 1.5 d of fasting. There was no significant change in mean plasma concentration beyond 1.5 d, owing to variable individual responses to extended fasting. Plasma b-HBA levels at 9 months of age ranged from 0.07 to 0.18 mM. Six-week-old Steller sea lion pups showed blood chemistry consistent with metabolic adaptation to fasting within 16 h but were unable to sustain a protein-sparing metabolism for a prolonged period. The pups appeared to revert to protein catabolism after only 2.5 d of fasting. This infers a decrease in lipid catabolism that might be due to the depletion of available lipid resources.

abstract
Dry-matter digestibility and energy digestive efficiency were measured in six juvenile Steller sea lions (Eumetopias jubatus) fed three diets each consisting of a single species: herring, pollock, and squid. Two of the animals were also fed pink salmon. Dry-matter digestibility (DMD) and digestive efficiency (DE) were measured using the energy and manganese concentration in fecal and food samples. DE values were high for all prey species (herring: 95.4 ± 0.7% (mean ± SD), pollock: 93.9 ± 1.4%, salmon: 93.4 ± 0.5%, squid: 90.4 ± 1.3%). Steller sea lions appear to digest prey of high energy density more efficiently than prey of low energy density. DMD values were also high for all prey species (herring: 90.1 ± 1.8%, pollock: 86.5 ± 3.4%, salmon: 87.3% ± 2.6, squid: 90.5 ± 1.2%). The low DMD value for pollock compared with herring and squid was due to the high proportion of bony material in pollock. There was a strong linear relationship between DE and DMD for each prey type, but the terms cannot be used interchangeably. DE measures are more meaningful than DMD in conveying the energetic benefits derived by sea lions from different types of prey. Species-specific measures of the digestible energy obtained from an array of prey items are a necessary component in understanding the bioenergetic consequences of consuming different prey species.

abstract
Dry-matter digestibility and energy digestive efficiency were measured in six juvenile Steller sea lions (Eumetopias jubatus) fed three diets each consisting of a single species: herring, pollock, and squid. Two of the animals were also fed pink salmon. Dry-matter digestibility (DMD) and digestive efficiency (DE) were measured using the energy and manganese concentration in fecal and food samples. DE values were high for all prey species (herring: 95.4 &amp;plusmn; 0.7% (mean &amp;plusmn; SD), pollock: 93.9 &amp;plusmn; 1.4%, salmon: 93.4 &amp;plusmn; 0.5%, squid: 90.4 &amp;plusmn; 1.3%). Steller sea lions appear to digest prey of high energy density more efficiently than prey of low energy density. DMD values were also high for all prey species (herring: 90.1 &amp;plusmn; 1.8%, pollock: 86.5 &amp;plusmn; 3.4%, salmon: 87.3% &amp;plusmn; 2.6, squid: 90.5 &amp;plusmn; 1.2%). The low DMD value for pollock compared with herring and squid was due to the high proportion of bony material in pollock. There was a strong linear relationship between DE and DMD for each prey type, but the terms cannot be used interchange-ably. DE measures are more meaningful than DMD in conveying the energetic benefits derived by sea lions from dif-ferent types of prey. Species-specific measures of the digestible energy obtained from an array of prey items are a necessary component in understanding the bioenergetic consequences of consuming different prey species.

abstract
The decline of Steller sea lions (Eumetopias jubatus) in the Gulf of Alaska and the Aleutian Islands may be the result of them eating too much pollock (a gadid fish) instead of a more balanced and diverse diet containing fattier fishes, such as herring or sandlance. We sought to test this junk-food hypothesis by feeding six captive Steller sea lions (ages 0.9–4.5 years) only pollock or herring. All sea lions gained mass while eating herring. However, eating only pollock for short periods (11–23 d) caused the study animals to lose an average of 6.5% of their initial body mass (0.6 kg/d) over an average feeding trial of 16 d (initial mass averaged 125 kg). The animals were allowed to eat as much pollock as they wanted but did not increase their food intake to compensate for the low energy they were receiv-ing. The sea lions showed progressive metabolic depression while losing body mass on a pollock-only diet. The loss of body mass while eating pollock was due to the lower gross energy content of pollock versus herring, the higher cost of digesting pollock, and the increased energy loss from digesting the larger quantity of fish needed to compensate for the lower energy content of pollock. Thus, our sea lions would have had to eat 35–80% more pollock than herring to maintain similar net energy intakes. Results from our captive-feeding studies are consistent with the junk-food hypothe-sis and have serious implications for Steller sea lions that have been eating primarily pollock in the Gulf of Alaska and the Aleutian Islands.

abstract
Assimilation and digestive efficiencies were measured in four juvenile Steller sea lions (Eumetopias jubatus) fed three ration sizes of herring (3%, 6%, or 9% of body mass) at three frequencies (2, 3, or 4 times daily). Assimilation efficiency (dry matter digestive efficiency) was 90.0 ± 2.0% (mean ± 1SD). Digestive efficiency (efficiency of energy digestion) was 95.5 ± 1.0%. There was a strong linear relationship between digestive and assimilation efficiency, but no significant differences in either assimilation or digestive efficiency with changes in feeding frequency or changes in daily food intake within the ranges offered.

abstract
Five juvenile Steller sea lions (Eumetopias jubatus) between the ages of 3 and 4 years were experimentally fasted for 9 to 14 d to assess changes in mass and in key plasma metabolites indicative of biochemical adaptation to fasting. The 5 sea lions lost 20.4 to 35.1 kg each, at a rate of 1 to 2% of their initial body mass per day. Two animals fasted during the natural breeding season (June) exhibited a mean daily loss of 1.6 +/- 0.1kg d-1. This was significantly lower than the mean 2.8 +/- 0.1kg d-1 lost by sea lions fasted outside the normal breeding season in April, October and November (p<0.001). The two sea lion studied in June maintained low BUN concentrations throughout the remainder of the study, while the remaining 3 animals showed significant increases after 7 d of fasting. Only the two juveniles fasted during the breeding season maintained a protein sparing metabolism, typical of the species adapted to long-term fasting. With the exception of the smallest female (after 12 d of fasting), ketone body levels ranged from 0.03 to 0.17 mM. Seasonal differences in how sea lions adapt to fasting suggests that these animals would be more severely impacted by limited food resources during the non-breeding season.

abstract
Diets of six Steller sea lions (Eumetopias jubatus) were switched between a high (herring) and a low (squid) energy density food for 14 d to determine the effects on ingested prey mass, body mass, resting metabolic rate, and the heat increment of feeding. Body mass was measured daily, and resting metabolism was measured weekly by gas respiro-metry. Ingested food mass did not differ significantly be-tween the squid diet and the control or the recovery herring diet periods. As a result of differences in energy density, gross energy intake was significantly lower during the squid diet phase than during either the control or recovery pe-riods. As a result, sea lions lost an average of 1.1 kg/d, totaling 12.2% of their initial body mass by the end of the experimental period. The heat increment of feeding for a 4-kg squid meal was significantly lower than for a similarly sized meal of herring. Decreases in both absolute (24.0 to 18.0 MJ/d, 224%) and mass-corrected (903 to 697 kJ/d/ kg 0.67 , 220%) metabolism were observed by the end of the squid feedings. This study suggests that sea lions can depress their resting metabolism in response to decreases in energy intake or body mass, regardless of satiation level.

abstract
Fasting in bears, penguins and phocid seals is accompanied by predictable changes in plasma metabolite concentrations related to alterations in the body reserves that are catabolized and illustrate a species’ ability to limit protein degradation during long-term fasting (see review in Castellini and Rea 1992, Nordoy et al. 1993, Rea 1995). Steller sea lions (Eumetopias jubatus) also undergo periods of fasting in their natural environment; adult females fast while nursing pups on the rookery, males defend breeding territories and young pups fast on the rookeries while their mothers are at sea foraging. Five juvenile Steller sea lions were fasted ‘in captivity (with free access to fresh water) for 9 to 14 days to test the hypothesis that juvenile Steller sea lions also exhibit changes in key plasma metabolites indicative of biochemical adaptation to fasting. The secondary objective of this study was to determine if blood metabolite concentrations could be used as biochemical indicators of nutritional status in free-ranging juvenile Steller sea lions.

keywords     blood chemistry, body mass, fasting, juvenile Steller sea lions, #2

abstract
When faced with decreases in energy intake, an animal has two conditions, hunger stimulates increased foraging activity, a strategy of short-term expenditure off-set by a reasonable-expectation of foraging success. However, when faced wit increased energy h periods of predictable or prolonged shortages of energy intake (although not necessarily energy availability), the animal should limit energy expenditures. The most common response to experimental undernutrition or fasting in homeotherms is metabolic depression. Invoking such physiologic responses that limitenergy expenditures limits tissue loss and delays death by starvation. Some species of marine mammals have exhibited metabolic depression, although its occurrence, scope, and triggers are still unclear. This study was designed to document the extent of metabolic depression in Steller sea lions. It investigated the role of energy and food intake on metabolic depression, and the relationship between changes in body mass and the scope of metabolic depression.

abstract
The heat increment of feeding (HIF) was measured in six captive, juvenile Steller sea lions (Eumetopias jubatus), fed meals of either 2 or 4 kg of herring. HIF was calculated as the post-prandial increase in metabolism above baseline levels, and was measured using open-circuit (gas) respirometry. It averaged 12.4 +/- 0.9% (SE) of ingested energy intake for the 4-kg meal trials, and 9.9 +/- 0.9% for the 2-kg meal size. The effect lasted 8-10 hr for the larger meal size. Metabolism peaked 3.7 hr after feeding, and was 2.13 times higher than baseline levels. For the 2-kg meal size, the effect lasted 6-8 hr, with metabolism peaking 2.8 hr after ingestion at 1.76 times baseline levels. Our estimates of HIF for Steller sea lions are at the lower end of estimates for terrestrial mammals, and are consistent with estimates for other marine mammals.

keywords     digestion, heat increment of feeding, pinnipeds, specific dynamic action, Steller sea lion