Steller sea lions Eumetopias jubatus and nutritional stress: evidence from captive studies

• 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 if 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.

     

Neonatal survival of Steller sea lions (Eumetopias jubatus)

Neonatal survival of Steller sea lions ( Eumetopias jubatus ) are often considered inconsequential to their population dynamics. However, observations of dead animals on rookeries and in surrounding waters suggest that early mortality is not uncommon. This study used the natural markings of adult females in a mark and resighting framework to estimate the apparent survival (φ) of pups with the Cormack–Jolly–Seber model at two sites on Lowrie Island, Alaska from birth to 3 wk old. Estimates varied greatly by site and year; 2002 Area 5:     (95% CI: 0.199, 0.684; n = 21), 2002 Area 1:     (0.437, 0.916; n = 21), 2003 Area 5:     (0.414, 0.738; n = 56), and 2003 Area 1:     (0.695, 0.997; n = 32). The mean estimate across the four area × year combinations was     (0.569, 0.772). Survival was lowest on the first day of life and then leveled off at a higher rate. None of the four environmental covariates we considered (swell height, interaction of tide and swell heights, density, or birth date) were significantly related to neonatal survival. Our results suggest that estimates of first-year survival that do not account for mortality prior to dispersal from the natal rookery may significantly overestimate survival rate.     

Characterization of eight microsatellite loci in Steller sea lions (Eumetopias jubatus)

Steller sea lions (Eumetopias jubatus) are listed as an endangered species in western Alaska and have exhibited a significant population decline throughout their range. Eight microsatellite loci were isolated from genomic DNA libraries. In addition, all these markers were found to be variable in nine individuals of the California sea lion (Zalophus californicus). This panel of markers was developed to analyse population structure in Steller sea lions throughout their range.     

Effects of research disturbance on the behavior and abundance of Steller sea lions (Eumetopias jubatus) at two rookeries in Alaska

We examined the effects of research disturbance on the behavior and abundance of Steller sea lions (Eumetopias jubatus) at rookeries on Marmot and Ugamak Islands in Alaska. During 3 of 6 yr, researchers intentionally drove all adult and juvenile sea lions off at least part of the beach in order to permanently mark and measure sea lion pups. The research disturbance occurred after the majority of females had bred and when most pups were 1 mo old. We used generalized linear models to determine the relationship between research disturbance and sea lion behavior or abundance. Research disturbance was related to changes in the proportion of sea lions exhibiting two to three of nine behavior metrics: agonistic and resting females and active males at Marmot, and active and resting males and females at Ugamak. Model results indicated that changes lasted between 3 and 20 d depending on the sex, behavior, and rookery. Inclusion of research disturbance into Marmot abundance models did not improve the fit to the data, if variability between years was permitted. Optimally timed, low‐frequency research disturbance did not appear to have long‐term effects on sea lion behavior or abundance and was largely associated with changes that were similar to natural variation.     

Poxvirus infection of Steller sea lions (Eumetopias jubatus) in Alaska

Lesions suggestive of poxvirus infection were observed in two Steller sea lions (Eumetopias jubatus) in Alaska during live capture-and-release studies during 2000 and 2001. Both of these animals, female pups in poor body condition, were from Prince William Sound; this population is part of the declining western stock. Umbilicated, typically ulcerated dermal nodules were present, primarily on the fore flippers in one case, and over most of the body in the second case. Histologically, there were discrete masses in the superficial dermis composed of epithelial cells, some of which contained eosinophilic intracytoplasmic inclusion bodies. Negative staining of skin biopsy homogenates demonstrated the presence of orthopoxvirus-like particles. Total DNA extracted from skin biopsies were analyzed by polymerase chain reaction (PCR) using primers that targeted the DNA polymerase and DNA topoisomerase genes. These primers directed the amplification of fragments 543 base pairs (bp) and 344 bp, respectively, whose deduced amino acid sequences indicated the presence of a novel poxvirus within the Chordopoxvirinae subfamily. Comparison of these amino acid sequences with homologous sequences from members of the Chordopoxvirinae indicated highest identity with orthopoxviruses.     

Field anesthesia of juvenile Steller sea lions (Eumetopias jubatus) using inhalation anesthesia

Between 1998 and 2008, 621 Steller sea lions (Eumetopias jubatus, SSL) were captured underwater by SCUBA divers and anesthetized with isoflurane (n = 602) or sevoflurane (n = 19). We found significantly faster induction time ( ± SD) for sevoflurane (11 ± 6 min) compared to isoflurane (14 ± 6 min), as well as an interaction between anesthetists using the isoflurane protocol. Severe hypothermia with temperatures <35°C were measured in 22% of all animals, and had significant associations with month, length of anesthesia, and sex. Mortality rate was low (0.33%). We conclude that both isoflurane and sevoflurane anesthesia were effective for field anesthesia to safely handle and sample SSL.     

Ontogeny of total body oxygen stores and aerobic dive potential in Steller sea lions (Eumetopias jubatus)

Two key factors influence the diving and hence foraging ability of marine mammals: increased oxygen stores prolong aerobic metabolism and decreased metabolism slows rate of fuel consumption. In young animals, foraging ability may be physiologically limited due to low total body oxygen stores and high mass specific metabolic rates. To examine the development of dive physiology in Steller sea lions, total body oxygen stores were measured in animals from 1 to 29 months of age and used to estimate aerobic dive limit (ADL). Blood oxygen stores were determined by measuring hematocrit, hemoglobin, and plasma volume, while muscle oxygen stores were determined by measuring myoglobin concentration and total muscle mass. Around 2 years of age, juveniles attained mass specific total body oxygen stores that were similar to those of adult females; however, their estimated ADL remained less than that of adults, most likely due to their smaller size and higher mass specific metabolic rates. These findings indicate that juvenile Steller sea lion oxygen stores remain immature for more than a year, and therefore may constrain dive behavior during the transition to nutritional independence.     

Temporal variability in organochlorine contamination in blood and blubber of captive Steller sea lions (Eumetopias jubatus)

Three adult captive Steller sea lions (SSL; two females, one male) housed in Alaska were longitudinally sampled for organochlorine contaminant (OC) analysis in both blubber (n= 19) and blood (n= 69) over a 2 yr period (March 2001 to March 2003). Blood OC concentrations were similar between individuals, and exhibited significant increases in summer months (July through September) relative to winter (January through March). Additionally, paired blood and blubber sample (n= 18) OC were significantly related for all animals. The relationship of blubber OC concentrations to lipid content was significant in all animals. Although limited to a small number of animals, our study results indicate that in SSLs, blood OC were both consistent among all animals and likely changed in association with physiologically driven metabolism of blubber.     

Crossing to safety: dispersal,colonization and mate choice in evolutionarily distinct populations of Steller sea lions,Eumetopias jubatus

Population growth typically involves range expansion and establishment of new breeding sites, while the opposite occurs during declines. Although density dependence is widely invoked in theoretical studies of emigration and colonization in expanding populations, few empirical studies have documented the mechanisms. Still fewer have documented the direction and mechanisms of individual transfer in declining populations. Here, we screen large numbers of pups sampled on their natal rookeries for variation in mtDNA (n = 1106) and 16 microsatellite loci (n = 588) and show that new Steller sea lion breeding sites did not follow the typical paradigm and were instead colonized by sea lions from both a declining (Endangered) population and an increasing population. Dispersing individuals colonized rookeries in the distributional hiatus between two evolutionarily distinct ( = 0.222,  = 0.053, K = 2) metapopulations recently described as separate subspecies. Hardy–Weinberg, mixed‐stock and relatedness analysis revealed levels of interbreeding on the new rookeries that exclude (i) assortative mating among eastern and western forms, and (ii) inbreeding avoidance as primary motivations for dispersal. Positive and negative density dependence is implicated in both cases of individual transfer. Migration distance limits, and conspecific attraction and performance likely influenced the sequence of rookery colonizations. This study demonstrates that resource limitation may trigger an exodus of breeding animals from declining populations, with substantial impacts on distribution and patterns of genetic variation. It also revealed that this event is rare because colonists dispersed across an evolutionary boundary, suggesting that the causative factors behind recent declines are unusual or of larger magnitude than normally occur.     

Body mass and composition responses to short-term low energy intake are seasonally dependent in Steller sea lions (Eumetopias jubatus)

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 day⁻¹), and at a lower rate during summer (1.2 ± 0.32 kg day⁻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.     

Infectious disease and the decline of Steller sea lions (Eumetopias jubatus) in Alaska, USA: insights from serologic data

Serologic data were examined to determine whether infectious disease may have played a role in the decline of Steller sea lions (Eumetopias jubatus) in the Gulf of Alaska and Aleutian Islands, USA. Available published data, unpublished data, and recent collections (1997-2000) were compared and reviewed. Data were stratified by geography to compare the declining western Alaskan population in the Aleutian Islands through eastern Prince William Sound to the increasing population in southeastern Alaska. Prevalences of antibodies from the 1970s to the early 1990s were noted for Leptospira interrogans, Chlamydophila psittaci, Brucella spp., phocid herpesvirus-1, and calciviruses. Serum samples collected from 1997-2000 were tested for antibodies to these agents as well as to marine mammal morbilliviruses, canine parvovirus, and canine adenovirus-1 and -2. Conclusions could not be drawn about changes in antibody prevalence to these agents during the decline of Steller sea lions, however, because data were incomplete or not comparable as a result of inconsistencies in testing techniques. Despite these shortcomings, results provided no convincing evidence of significant exposure of Steller sea lions to morbilliviruses, Brucella spp., canine parvovirus, or L. interrogans. Steller sea lions have been exposed to phocid herpesviruses, caliciviruses, canine adenovirus, and C. psittaci or to cross-reactive organisms in regions of both increasing and decreasing sea lion abundance. Based on similar antibody prevalence estimates from the increasing and decreasing populations, these agents are unlikely to have been the primary cause of the population decline. They may have contributed to the decline or impeded population recovery, however, because of undetected mortality and morbidity or reductions of fecundity and body condition in animals under other stresses. Systematic monitoring for disease agents and their effects is needed to determine whether infectious disease currently plays a role in the decline and lack of recovery of Steller sea lions.     

Differentiating between Steller sea lion (Eumetopias jubatus) and northern fur seal (Callorhinus ursinus) scats through analysis of faecal DNA

We describe a method to determine the species of pinniped from faeces collected from sympatric Steller sea lion (Eumetopias jubatus) and northern fur seal (Callorhinus ursinus) rookeries using newly developed species-specific primers that amplify a 667-669-base pair segment from the mitochondrial DNA (mtDNA) cytochrome B (cytB) gene region. The primers yielded the correct species in 100% of tissue samples from 10 known animals and 100% of faecal samples from 13 known animals. Species could be identified unequivocally for 87.7% of faecal samples from 122 unknown individuals. The ability to differentiate between scats of sympatrically breeding Steller sea lions and northern fur seals will contribute to the range-wide knowledge of the foraging strategies of both species as well as allow researchers to examine the niche partitioning and potential resource competition between the two predators.     

The role of Steller sea lions in a large population decline of harbor seals

We provide the first direct evidence that Steller sea lions will prey on harbor seals. Direct observations of predation on marine mammals at sea are rare, but when observed rates of predation are extrapolated, predation mortality may be found to be significant. From 1992 to 2002, harbor seals in Glacier Bay declined steeply, from 6,200 to 2,500 (∼65%). After documenting that Steller sea lions were preying on seals in Glacier Bay, we investigated increased predation by sea lions as a potential explanation for the large decline. In five independent data sets spanning 21–25 yr and including 14,308 d of observations, 13 predation events were recorded. We conducted a fine-scale analysis for an intensively studied haul-out (Spider Island) and a broader analysis of all of Glacier Bay. At Spider Island, estimated predation by sea lions increased and could account for the entirety of annual pup production in 5 of 8 yr since 1995. The predation rate, however, was not proportional to the number of predators. Predation by Steller sea lions is a new source of mortality that contributed to the seal declines; however, life history modeling indicates that it is unlikely that sea lion predation is the sole factor responsible for the large declines.     

Foraging behavior of adult female Steller sea lions during the breeding season in Southeast Alaska

During the 1990s, the Steller sea lion ( Eumetopias jubatus Schreber) Western Alaska stock (WS) suffered steep population decline while the Eastern Alaska stock (ES) steadily increased. One bottom-up forcing hypothesis explaining this decline predicted lactating adult female foraging behavior would be different between stocks. To investigate this effect, we monitored 11 ES females at two breeding rookeries using satellite dive recorders (SDR) during the early breeding seasons of 1992–1993, examined their behavior with respect to prey, physiological limitations, and habitat, and made limited comparisons to observations of WS female behavior reported in the literature. ES females were not operating at the extremes of ability, with most diving within the limits of aerobic metabolism, less than one-quarter of possible foraging time during trips spent submerged and most foraging trips requiring less than one-half the lipid store fasting ability of dependent pups. Thus, females may have some capacity to alter behavior to accommodate future changes in foraging conditions, but the extent of this plasticity is unknown. Because recent work suggests WS recovery is impeded by low natality, future studies should test differences between reproductive and non-reproductive mature females in order to properly assess the contribution of foraging ecology to SSL population dynamics.     

Postbranding Survival of Steller Sea Lion Pups at Lowrie Island in Southeast Alaska

ABSTRACT Steller sea lion (Eumetopias jubatus) pups (n = 366) were hot-branded at Lowrie Island, Southeast Alaska, USA, in June 2001 and 2002 for vital-rates studies. To assess potential mortality following branding, we estimated weekly survival to 12 weeks postbranding using mark-recapture models. Survival estimates ranged from 0.984/week to 0.988/week, or 0.868 over the 12-week period; varied little with sex, year, and capture area; and were higher for larger than smaller male pups and unexpectedly lower for larger than smaller female pups. Inclusion of resights at 1–3 years of age prevented a −4.5% bias in cumulative survival to 12 weeks postbranding by accounting for pups that survived but permanently emigrated from Lowrie Island during the 12-week survey. Data from double-marked pups (i.e., branded and flipper-tagged) indicated the low brand-misreading probability of 3.1% did not bias survival estimates. Assuming survival differences between the first 2 weeks postbranding and later weeks were due entirely to the branding event, potential postbranding mortality of branded pups attributable to the branding event was 0.5–0.7%, or one pup for every 200 marked. Weekly survival of branded pups was nearly identical to estimates from a control group of undisturbed, unbranded pups born to 10–11-year-old branded adult females in 2005 (0.987–0.988/week) and similar to pup survival estimates from other otariid studies. Available data did not indicate substantial mortality to 12 weeks postbranding resulting from the branding disturbance, suggesting branding of Steller sea lion pups can be used effectively for investigations of population declines without significantly affecting population health or study goals.     

Anthropogenic causes of the western Steller sea lion Eumetopias jubatus population decline and their threat to recovery

• 1 The western Steller sea lion Eumetopias jubatus population has experienced a chronic decline since the 1960s. The causes are likely multifactorial and a combination of anthropogenic and natural factors. A draft revised recovery plan for the Steller sea lion has been published by the US National Marine Fisheries Service, listing both anthropogenic and natural factors that may have contributed to the observed decline or which may be a threat to the recovery of the western Steller sea lion population. The purpose of this review is to consider the anthropogenic threats to this stock.
• 2 Anthropogenic sources of mortality include fisheries competition resulting in nutritional stress, mortality incidental to commercial fisheries (i.e. fisheries by‐catch), subsistence hunts, legal and illegal shooting, commercial hunts, anthropogenic‐related contamination, and research‐induced mortalities.
• 3 We present evidence that the following anthropogenic factors likely contributed to the decline of the western Steller sea lion population over the last 40 years: (i) mortality incidental to commercial fisheries (i.e. by‐catch); (ii) commercial hunting of western Steller sea lions; and (iii) legal and illegal shooting; whereas the subsistence hunts for western Steller sea lions and mortality incidental to research were not likely to be contributors to the observed decline.
• 4 Further, we present evidence that the following can be excluded as significant anthropogenic threats to the recovery of the western Steller sea lion population: (i) mortality incidental to commercial fishing; (ii) legal and illegal shooting; (iii) commercial hunts of Steller sea lions; (iv) subsistence hunting; and (v) mortality incidental to research.
• 5 Competition with fisheries resulting in nutritional stress, and the potential impacts of contaminants, are two anthropogenic factors that should continue to be a priority for the various organizations currently doing research on this population.

     

High diving metabolism results in a short aerobic dive limit for Steller sea lions (Eumetopias jubatus)

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 (VO₂) 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 O₂ stores by comparing blood O₂ 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 O₂ stores between the diving and non-diving groups. Estimated TBO (35.9 ml O₂ 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 O₂ min^?1) and was significantly 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 VO₂ and blood oxygen stores for an Otariid and indicates they have a much shorter ADL than previously thought.