Eumetopias Research Articles

Where do sea lions live? Interspecific interactions and abiotic factors predict Steller sea lion habitat.

Habitat selection by species is dependent on both abiotic factors and species interaction. With regards to species interaction, competition and facilitation can play a critical role regarding how a species selects its habitat. Previous work has suggested that Steller sea lions (Eumetopias jubatus) have been displaced from their haulout sites due to competition with California sea lions (Zalophus californianus). The purpose of our study is to understand what factors determine the number of Steller sea lion present at a haul out site in the Barkley Sound area in Bamfield, BC. We tested this by asking if the number of Steller sea lions at a haulout site at a certain time is related to the presence of California sea lions (as a proxy for interspecific interaction), time of day, and tide height or a combination of two or three of these variables. After running a generalized mixed effect model and competing our models using Akaike Information Criteria, our results indicated that tide height was the best predictor for explaining the number of Steller sea lions present at a haulout site. However, our results also indicated that the presence of California sea lions and time of day may play a role in determining Steller sea lion haulout sites as well. We found from this study that both species interaction and abiotic factors need to be collectively considered when predicting the mechanisms underlying species habitat choice in marine ecosystems.

Winter movements and long-term dispersal of Steller sea lions in the Glacier Bay region of Southeast Alaska

Winter movements and long-term dispersal of Steller sea lions in the Glacier Bay region of Southeast Alaska

Chemical and Mechanical Characteristics of Steller Sea Lion Meat Caught in Hokkaido

Chemical and Mechanical Characteristics of Steller Sea Lion Meat Caught in Hokkaido

REGIONAL AND AGE-RELATED VARIATIONS IN HAPTOGLOBIN CONCENTRATIONS IN STELLER SEA LIONS (EUMETOPIAS JUBATUS) FROM ALASKA, USA

Varying concentrations of the highly conserved acute phase response protein, haptoglobin, can indicate changes to the health and disease status of mammals, including the Steller sea lion (SSL; Eumetopias jubatus). To better understand factors relating to acute phase response in SSLs, circulating haptoglobin concentrations (Hp) were quantified in plasma collected from 1,272 individuals sampled near rookeries and haulouts off the coast of Alaska, US. We compared Hp in SSLs between sexes and among different age classes (young pups, young-of-the-year, yearlings, subadults, and adults) sampled within distinct regions in Alaska (Aleutian Islands, Gulf of Alaska, Southeast Alaska). Regional and age-related differences were observed, particularly in younger SSLs. No sex-related differences were detected. We identified weakly significant relationships between Hp and hematology measurements including white blood cell counts and hematocrit in young pups from the Aleutian Islands and Southeast Alaska. No relationship between Hp and body condition was found. Lastly, a nonlinear relationship of plasma Hp and whole blood total mercury concentrations (THg) was observed in SSLs from the endangered western distinct population segment in Alaska. These results demonstrated that regional variation in Hp, especially in younger SSLs, may reflect regional differences in health and circulating THg.

Enhanced quantification of serum immunoglobulin G from a non-model wildlife species, the Steller sea lion (Eumetopias jubatus), using a protein A ELISA

Immunoglobulins (Ig) are proteins that preserve immune homeostasis and are quantified to infer changes to the acquired humoral immune response in mammals. Measuring Ig in non-model wildlife for immune surveillance often requires ingenuity, and rigorous standardization of methodologies to provide reliable results especially when lacking species-specific reagents. We modified and optimized existing ELISA methodology utilizing the binding properties of Staphylococcus-derived Protein A (PrtA) to immunoglobulin G (IgG). We enhanced the assay for quantifying IgG in Steller sea lion (SSL) serum using critical quality control measures including dilution linearity, spike and percent recoveries, and internal controls. Of the modifications made, heat treatment of SSL serum enhanced accuracy and precision of IgG measurements by improving linearity and percent recovery in parallel dilutions and serum spikes. Purified canine IgG standard was not affected by heat inactivation. These results support that confounding serum proteins interfere with binding of PrtA with IgG demonstrating the need for heat treatment of serum to optimize IgG quantification using the PrtA-ELISA. Further, essential validation measures ensure proper assay performance. Consequently, the improved PrtA-ELISA provides species-independent IgG detection with validation criteria to enhance accuracy and precision for addressing future immunological questions in non-model wildlife in clinical, ecological, and conservation contexts.

Characterizing estrus by trans-abdominal ultrasounds, fecal estrone-3-glucuronide, and vaginal cytology in the Steller sea lion (Eumetopias jubatus)

The ability to monitor the estrus cycle in wild and captive marine species is important for identifying reproductive failures, ensuring a successful breeding program, and monitoring animal welfare. Minimally invasive sampling methods to monitor estrus in captive populations have been developed, but results suggest these tools can be species-specific in their precision and accuracy. Therefore, the minimally invasive sampling methods of trans-abdominal ultrasounds, a fecal steroid analysis (estrone-3-glucuronide, E1G), and vaginal cytology, were evaluated for their efficacy to characterize and monitor estrus in a captive breeding population of Steller sea lions (Eumetopias jubatus). Three adult females were sampled over five breeding seasons, resulting in six estrus profiles characterized by trans-abdominal ultrasounds, five by fecal E1G, and four by vaginal cytology. Animals were trained to allow trans-abdominal ultrasounds, fecal samples, and vaginal swabs to be collected approximately daily. Of the 76 trans-abdominal ultrasound sessions attempted, 8 successfully visualized both ovaries. From these scans, the chronology of ovarian changes during proestrus and estrus was estimated. The time from the detection of developing follicles to the identification of a dominate follicle occurred in 2–5 days and a corpus hemorrhagicum formed approximately 4 days later. However, because visualization of the ovaries was prevented by the gastrointestinal system in 88% of scans, this tool was overall unreliable for monitoring changes associated with estrus. To detect fine scale physiological changes associated with estrus, we analyzed changes in fecal E1G (n = 62) and vaginal cytology (n = 157) 15 days before and after each female's single copulation event (Day = 0). Changes in fecal E1G had the highest accuracy at detecting Day = 0. Fecal E1G increased leading up to estrus, peaked at Day = 0, and then declined. Although we did observe the characteristic increase in superficial cells associated with impending estrus, the type of cell which peaked closest to Day = 0 was intermediate. The uncertainty around the peak in intermediate cells, indicating estrus, was greater than the uncertainty associated with detecting estrus from fecal E1G. Collectively, these results suggest that changes in fecal E1G and vaginal cytology are viable tools to detect estrus in Steller sea lions, but require daily sampling to detect gradual changes, limiting their applicability to studies of wild populations.

Temporal records of diet diversity dynamics in individual adult female Steller sea lion (Eumetopias jubatus) vibrissae

Detailed information on the nutrition of free-ranging mammals contributes to the understanding of life history requirements, yet is often quite limited temporally for most species. Reliable dietary inferences can be made by analyzing the stable carbon (C) and nitrogen (N) isotopic values (δ13C and δ15N) of some consumer tissues; exactly which tissue is utilized dictates the inferential scope. Steller sea lion (SSL) vibrissae are grown continuously without shedding and thus provide a continuous multi-year record of dietary consumption. We applied a novel kernel density approach to compare the δ13C and δ15N values along the length of SSL vibrissae with δ13C and δ15N distributions of potential prey species. This resulted in time-series of proportion estimates of dietary consumption for individual SSL. Substantial overlap in δ13C and δ15N distributions for prey species prevented a discrete species-scale assessment of SSL diets; however, a post hoc correlational analysis of dietproportion estimates revealed grouping by trophic level. Our findings suggest that adult female SSL diets in the western and central Aleutian Islands shift significantly according to season: diets contain a higher proportion of lower trophic level species (Pacific Ocean perch, northern rockfish, Atka mackerel and walleye pollock) in the summer, whereas in the winter SSL consume a much more diverse diet which includes a greater proportion of higher trophic level species (arrowtooth flounder, Kamchatka flounder, darkfin sculpin, Pacific cod, Pacific octopus, rock sole, snailfish, and yellow Irish lord).

Present-Day Assemblage of Birds and Mammals in the Islands of Four Mountains, Eastern Aleutians, Alaska

AbstractWe compiled present-day observations and survey data of the avian and mammal fauna in the Islands of Four Mountains, Alaska, which primarily consist of marine-adapted species, to provide insight into the prehistoric fauna found in the archaeological record. We documented 63 bird species, mainly seabirds (67%). The majority (71%) of the estimated number of breeding birds are ledge nesters, predominately murres, and most (68%) spend the majority of their lives in the offshore environment. We lack good estimates for burrow and crevice nesters, which were impacted by and are still recovering from a period of arctic fox farming in the twentieth century. Marine mammals, predominately Steller sea lion, harbor seal, and sea otter, primarily use accessible land as haul-outs and are found in low numbers compared with the rest of the Aleutians. Red fox, the only land mammal, presently only reside on Chuginadak Island. While the present-day fauna is similar to the fauna recorded in the archaeological record, we found no indication of nesting by ancient murrelets and northern fulmars in the Island of Four Mountains, whereas both species were present in midden sites on Carlisle and Chuginadak Islands, with the possibility of prehistoric breeding colonies on Carlisle Island.

Juvenile Steller sea lion (Eumetopias jubatus) utilization distributions in the Gulf of Alaska

BackgroundA utilization distribution quantifies the temporal and spatial probability of space use for individuals or populations. These patterns in movement arise from individuals’ internal state and from their response to the external environment, and thus can provide insights for assessing factors associated with the management of threatened populations. The Western Distinct Population Segment of the Steller sea lion (Eumetopias jubatus) has declined to approximately 20% of levels encountered 40 years ago. At the height of the decline, juvenile survival appeared to be depressed and currently there is evidence that juvenile mortality due to predation may be constraining recovery in some regions. Therefore, our objectives were to identify what spaces are biologically important to juvenile Steller sea lions in the Kenai Fjords and Prince William Sound regions of the Gulf of Alaska.MethodsWe examined geospatial location data from juvenile sea lions tagged between 2000 and 2014 (n = 84) and derived individual and pooled-population utilization distributions (UDs) from their movements. Core areas were defined from the UDs using an individual-based approach; this quantitatively confirmed that all individuals in our sample exhibited concentrated use within their home range (95% UD). Finally, we explored if variation in UD characteristics were associated with sex, season, age, or region.ResultsWe found evidence that individual juvenile home ranges were region and sex-specific, with males having larger home ranges on average. Core space characteristics were also sex-specific, and exhibited seasonal patterns of reduced size, increased proximity to haulouts, and increased intensity of use in the summer, but only in the Kenai Fjords-Gulf of Alaska region.ConclusionsThis study highlights the areas of biological importance during this vulnerable life history stage, and the demographic, seasonal, and spatial factors associated with variation in movement patterns for a marine mesopredator. This can be useful information for promoting species recovery, and for future efforts to understand ecological patterns such as predator-prey interactions.

Obstacles and Opportunities of Using a Mobile App for Marine Mammal Research

This study investigates the use of a mobile application, Whale mAPP, as a citizen science tool for collecting marine mammal sighting data. In just over three months, 1261 marine mammal sightings were observed and recorded by 39 citizen scientists in Southeast Alaska. The resulting data, along with a preliminary and post-Whale mAPP questionnaires, were used to evaluate the tool’s scientific, educational, and engagement feasibility. A comparison of Whale mAPP Steller sea lion distribution data to a scientific dataset were comparable (91% overlap) given a high enough sample size (n = 73) and dense spatial coverage. In addition, after using Whale mAPP for two weeks, citizen scientists improved their marine mammal identification skills and self-initiated further learning, representing preliminary steps in developing an engaging citizen science project. While the app experienced high initial enthusiasm, maintaining prolonged commitment represents one of the fundamental challenges for this project. Increasing participation with targeted recruitment and sustained communication will help combat the limitations of sample size and spatial coverage. Overall, this study emphasizes the importance of early evaluation of the educational and scientific outcomes of a citizen science project, so that limitations are recognized and reduced.

Validation of a Protein A-based ELISA for quantifying Immunoglobulin G in a non-traditional wildlife species, the Steller sea lion (Eumatopias jubatus)

Abstract Immunoglobulins are key proteins that function to preserve immune homeostasis and are quantified to infer changes to the acquired humoral immune response in mammals. Measuring immunoglobulins in non-traditional wildlife for immune surveillance often requires ingenuity, and rigorous standardization of methodologies to provide consistent and reliable results especially for species lacking species-specific reagents. We modified and optimized existing ELISA methodology that utilizes the binding properties of Staphylococcus derived Protein A (Prt A) with immunoglobulin G (IgG). We validated the assay for accurately quantifying IgG in Steller sea lion (SSL) serum using critical measures of validation including parallelism, spike and percent recoveries, and internal controls. Of the modifications made, heat inactivation of SSL serum proved pivotal to enhance accuracy and precision of IgG detection by improving linearity and percent recovery in parallelism dilutions and serum spikes. Purified canine IgG standard was not affected by the heat inactivation protocol. These results support that confounding serum proteins likely interfere with the binding of Prt A with IgG, and demonstrate the need for heat inactivation of serum to ensure optimal IgG quantification using the PrtA-ELISA. Further, incorporation of spike and recovery are essential validation measures to ensure proper standardization of this assay. Consequently, the improved and validated PrtA-ELISA guarantees a species-independent IgG detection with validation criteria to enhance accuracy, and precision for addressing future immunological questions concerning SSLs and other non-traditional wildlife in a clinical, ecological, and conservation context.

Correction: Natal and breeding philopatry of female Steller sea lions in southeastern Alaska.

[This corrects the article DOI: 10.1371/journal.pone.0176840.].

Maternal and offspring effects on the timing of parturition in western Steller sea lions (Eumetopias jubatus)

Identifying factors that affect the timing of parturition among annual breeders is important to aid our understanding of how variations may adversely affect population trends over both short and long temporal scales. We investigated the effect of several parameters on the timing of parturition among individual Steller sea lions (Eumetopias jubatus (Schreber, 1776)) over 6 years between 2005 and 2016 using an information–theoretic approach. In addition to the random effect of year, birth and care of a pup in the previous year had the largest effect on parturition, causing a 2.4 day delay. Maternal age was negatively correlated with timing of parturition and male pups were born nearly a day earlier than female pups, on average. There was limited support for effects of sex and mass, with heavier pups born marginally earlier than lighter ones. This study illustrates some of the complexity of variables that can influence the timing of birth in this species and which should be considered in models that attempt to identify long-term trends in changing marine ecosystems.

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.

Milk fatty acid composition of perinatal and foraging Steller sea lions (Eumetopiasjubatus): examination from pup stomachs

To investigate the milk fatty acid composition of female Steller sea lions (Eumetopias jubatus (Schreber, 1776)) between and within maternal states (i.e., perinatal or foraging), milk samples were collected in 2010 and 2011 via gastric intubation from Steller sea lion pups on a small rookery in the central Gulf of Alaska. Maternal states of lactating females were determined upon reuniting with their sampled pups via remotely operated video cameras on the rookery. Milk fatty acid composition between Steller sea lion maternal states was significantly different, and thus can be utilized to distinguish between perinatal and foraging Steller sea lions of the same geographic region in the absence of direct observation. However, milk fatty acid composition remained relatively constant within perinatal Steller sea lions, suggesting steady mobilization of fatty acids from blubber to milk, and within foraging Steller sea lions, implying females forage on similar prey species within several days after their perinatal period. Differences in milk fatty acid composition between maternal states, including differences in the relative percentages of polyunsaturated fatty acids, may have important implications for growth and development of offspring.

Overwintering Steller sea lion (Eumetopias jubatus) pup growth and behavior prior to weaning

We measured individual growth, looked for evidence of weaning, and examined the interaction of these changes with diving behavior in young-of-year Steller sea lion (Eumetopias jubatus (Schreber, 1776)) pups in Alaska, USA, during their first winter. Steller sea lions employ an income breeding strategy, in which females provision their young over an individually variable period of months to years. Thus, we set out to identify whether these young sea lions showed evidence of weaning during the challenging winter months, describe the nature of their growth during this time, and examine their behaviors in light of these changes. Between 2005 and 2008, we captured 71 pups during early winter and recaptured 33 of these pups in early spring. Mark–resight and stable nitrogen isotope ratios in vibrissae indicated most pups remained nutritionally dependent on adult females throughout the winter. All pups increased both mass and lipid mass, with half of growth contributed by lipid mass. Changes in behavior were not correlated with growth excepting a weak but significant effect on rate of vertical travel. This study demonstrated that capture–recapture of Steller sea lion pups is possible, provided seasonal timing, locations, and age classes are carefully considered for their likelihood of capture success.

Brucella Antibodies in Alaskan True Seals and Eared Seals—Two Different Stories

Brucella pinnipedialis was first isolated from true seals in 1994 and from eared seals in 2008. Although few pathological findings have been associated with infection in true seals, reproductive pathology including abortions, and the isolation of the zoonotic strain type 27 have been documented in eared seals. In this study, a Brucella enzyme-linked immunosorbent assay (ELISA) and the Rose Bengal test (RBT) were initially compared for 206 serum samples and a discrepancy between the tests was found. Following removal of lipids from the serum samples, ELISA results were unaltered while the agreement between the tests was improved, indicating that serum lipids affected the initial RBT outcome. For the remaining screening, we used ELISA to investigate the presence of Brucella antibodies in sera of 231 eared and 1,412 true seals from Alaskan waters sampled between 1975 and 2011. In eared seals, Brucella antibodies were found in two Steller sea lions (Eumetopias jubatus) (2%) and none of the 107 Northern fur seals (Callorhinus ursinus). The low seroprevalence in eared seals indicate a low level of exposure or lack of susceptibility to infection. Alternatively, mortality due to the Brucella infection may remove seropositive animals from the population. Brucella antibodies were detected in all true seal species investigated; harbor seals (Phoca vitulina) (25%), spotted seals (Phoca largha) (19%), ribbon seals (Histriophoca fasciata) (16%), and ringed seals (Pusa hispida hispida) (14%). There was a low seroprevalence among pups, a higher seroprevalence among juveniles, and a subsequent decreasing probability of seropositivity with age in harbor seals. Similar patterns were present for the other true seal species; however, solid conclusions could not be made due to sample size. This pattern is in accordance with previous reports on B. pinnipedialis infections in true seals and may suggest environmental exposure to B. pinnipedialis at the juvenile stage, with a following clearance of infection. Furthermore, analyses by region showed minor differences in the probability of being seropositive for harbor seals from different regions regardless of the local seal population trend, signifying that the Brucella infection may not cause significant mortality in these populations. In conclusion, the Brucella infection pattern is very different for eared and true seals.

Estimating animal utilization densities using continuous‐time Markov chain models

Abstract A long‐standing goal in ecology is to describe an animal's home range or utilization density (UD) without complete knowledge of the animal's movement. There are a number of methods available to calculate a UD from telemetry data, but the most common methods limit the UD to cover areas where the animal was observed during tracking, and do not account for preferential use of different habitats (resource selection). The limiting distribution of a continuous‐time Markov chain (CTMC) matches the intuitive understanding of a UD for an animal following a CTMC movement model. By modelling continuous‐time movement through discrete‐gridded space we can infer environmental effects on animal movement and then predict a UD over the desired spatial area that captures preferential use of space. The r packages crawl and ctmcmove allow ecologists to use telemetry data to predict the UD of an animal using the limiting distribution of a CTMC movement model. We used data collected from Steller sea lions in Alaska to illustrate use of this method for investigating range‐wide space use. Our findings show how these packages, and this method, can aid our understanding of space‐use by predicting use outside the areas where animals were observed, avoiding barriers to movement, including environmental covariates and removing the release effect of telemetry studies. These results will be important for both conservation and management, particularly when determining critical habitat designation.

Exploring local fishery management through cooperative acoustic surveys in the Aleutian Islands

An alternate management system is introduced which uses seasonal and spatially explicit multi-species quotas generated from small-scale cooperative fishery acoustic surveys to manage the Aleutian Islands walleye pollock (Gadus chalcogrammus) fishery while limiting impacts on the endangered Western stock of Steller sea lions (Eumetopias jubatus). This is a novel collaboration among scientists, industry, and Alaska Natives considering a cooperative management approach. The proposed system integrates the catch monitoring and accounting systems already in place in the federal groundfish fisheries off Alaska with cooperative acoustic survey biomass estimates to facilitate more refined spatial and temporal fishery management decisions. Conditions were examined under which such a system could operate successfully and results from field work conducted to assess technical requirements were discussed. During field trials biomass estimates from each survey were produced within 24-h of survey completion. This suggests spatial abundance estimates can be available in a timely manner for managing local fisheries. The proposed management system was found feasible and relatively easy to initiate because of highly motivated and cooperative industry partners, a well-established mechanism for setting allowable catch limits, and a robust catch accounting system already in place. In addition, high quality commercial echosounders required for this system are currently used by industry and, with proper controls on calibration and survey design, produce biomass estimates of sufficient quality. The application of this approach beyond this case study is also discussed for managing fisheries worldwide where fine temporal and spatial scale management could benefit the conservation of other protected species.

Survival of adult Steller sea lions in Alaska: senescence, annual variation and covariation with male reproductive success.

Population dynamics of long-lived vertebrates depend critically on adult survival, yet factors affecting survival and covariation between survival and other vital rates in adults remain poorly examined for many taxonomic groups of long-lived mammals (e.g. actuarial senescence has been examined for only 9 of 34 extant pinniped species using longitudinal data). We used mark–recapture models and data from 2795 Steller sea lion (Eumetopias jubatus) pups individually marked at four of five rookeries in southeastern Alaska (SEAK) and resighted for 21 years to examine senescence, annual variability and covariation among life-history traits in this long-lived, sexually dimorphic pinniped. Sexes differed in age of onset (approx. 16–17 and approx. 8–9 years for females and males, respectively), but not rate (−0.047 and −0.046/year of age for females and males) of senescence. Survival of adult males from northern SEAK had greatest annual variability (approx. ±0.30 among years), whereas survival of adult females ranged approximately ±0.10 annually. Positive covariation between male survival and reproductive success was observed. Survival of territorial males was 0.20 higher than that of non-territorial males, resulting in the majority of males alive at oldest ages being territorial.