Maintaining control: metabolism of molting Arctic seals in water and when hauled out.

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.

CARDIAC EXAMINATIONS OF ANESTHETIZED STELLER SEA LIONS (EUMETOPIAS JUBATUS), NORTHERN FUR SEALS (CALLORHINUS URSINUS), AND A WALRUS (ODOBENUS ROSMARUS).

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 eight Steller sea lions (Eumetopias jubatus), five northern fur seals (Callorhinus ursinus), and one walrus (Odobenus rosmarus) to investigate cardiac electrophysiology in pinnipeds. In addition, echocardiograms were performed on all eight 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 five out of eight 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.

REFERENCE RANGES AND AGE-RELATED AND DIVING EXERCISE EFFECTS ON HEMATOLOGY AND SERUM CHEMISTRY OF FEMALE STELLER SEA LIONS ( EUMETOPIAS JUBATUS).

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.

Dive, food, and exercise effects on blood microparticles in Steller sea lions (Eumetopias jubatus): exploring a biomarker for decompression sickness.

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/µl 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.

Feeding kinematics and performance of basal otariid pinnipeds, Steller sea lions and northern fur seals: implications for the evolution of mammalian feeding.

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.

A nutrigenomic approach to detect nutritional stress from gene expression in blood samples drawn from Steller sea lions.

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 nutrigenomic 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 how terrestrial mammals respond to dietary restrictions. 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.

Steller sea lions (Eumetopias jubatus) have greater blood volumes, higher diving metabolic rates and a longer aerobic dive limit when nutritionally stressed.

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.

Ultrasound images of the ascending aorta of anesthetized northern fur seals and Steller sea lions confirm that the aortic bulb maintains continuous blood flow.

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 electrocardiogram-gated 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.

What are the Metabolic Rates of Marine Mammals and What Factors Impact this Value: A review.

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.

Normal pre- and post-prandial bile acids and protein C values vary by age in harbor seal pups (Phoca vitulina richardsi) undergoing rehabilitation.

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.

Linking movement and dive data to prey distribution models: new insights in foraging behaviour and potential pitfalls of movement analyses.

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.

Key questions in marine mammal bioenergetics.

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 labelled 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.

Aerial audiograms of several California sea lions (Zalophus californianus) and Steller sea lions (Eumetopias jubatus) measured using single and multiple simultaneous auditory steady-state response methods.

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 ∼40 dB 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.

Dive behaviour impacts the ability of heart rate to predict oxygen consumption in Steller sea lions (Eumetopias jubatus) foraging at depth.

The predictive relationship between heart rate (f(H)) 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 f(H):VO2 relationship and whether the existing equations apply to animals diving to deeper depths. We investigated these questions by simultaneously measuring the f(H) 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 40 m). We examined the relationship over dives only and also over dive cycles (dive + surface interval). We found that f(H) 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 f(H) for multiple dive bout equations yielding higher predicted VO2 than that for single dive bout cycles (or resting). The f(H):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 f(H) 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.

Electrocardiographic Scaling Reveals Differences in Electrocardiogram Interval Durations Between Marine and Terrestrial Mammals.

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.

Molting strategies of Arctic seals drive annual patterns in metabolism.

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 are 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 seals, three ringed seals 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.

Changes in glucocorticoids, IGF-I and thyroid hormones as indicators of nutritional stress and subsequent refeeding in Steller sea lions (Eumetopias jubatus).

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.

The Genome of the Steller Sea Lion (Eumetopias jubatus).

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.

Proxies of energy expenditure for marine mammals: an experimental test of "the time trap".

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 [Formula: see text] 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 ([Formula: see text] 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.

Physiological constraints and energetic costs of diving behaviour in marine mammals: a review of studies using trained Steller sea lions diving in the open ocean.

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 nutritional 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.