Linking seasonal distribution patterns with prey availability in a central-place forager, the Steller sea lion

Aim We used a novel approach to infer foraging areas of a central‐place forager, the Steller sea lion (Eumetopias jubatus), by assessing changes in the temporal and spatial distribution patterns of sea lions at terrestrial sites. Specifically, our objectives were (1) to classify seasonal distribution patterns of Steller sea lions and (2) to determine to what extent the seasonal distribution of Steller sea lions is explained by seasonal concentrations of prey. Location Southeast Alaska, USA. Methods Steller sea lions of all age classes were counted monthly (2001–04) by aerial surveys at 28 terrestrial sites. Hierarchical cluster analysis and principal components analysis were used to classify seasonal distribution patterns of Steller sea lions at these terrestrial sites. We estimated the proportion of sea lions in the study area that were associated with each seasonal distribution pattern. Results Multivariate ordination techniques revealed four distinct seasonal distributional patterns. During December, 55% of the sea lions in the study area were found at Type 1 sites, located near over‐wintering herring aggregations. During May, 56% of sea lions were found at Type 2 sites, near aggregations of spring‐spawning forage fish. In July, 78% of sea lions were found at Type 3 sites, near summer migratory corridors of salmon. During September, 44% of sea lions were found at Type 4 sites, near autumn migratory corridors of salmon. Main conclusions Seasonal attendance patterns of sea lions were commonly associated with the seasonal availability of prey species near terrestrial sites and reflected seasonal foraging patterns of Steller sea lions in Southeast Alaska. A reasonable annual foraging strategy for Steller sea lions is to forage on herring (Clupea pallasii) aggregations in winter, spawning aggregations of forage fish in spring, salmon (Oncorhynchus spp.) in summer and autumn, and pollock (Theragra chalcogramma) and Pacific hake (Merluccius productus) throughout the year. The seasonal use of haulouts by sea lions and ultimately haulout‐specific foraging patterns of Steller sea lions depend in part upon seasonally available prey species in each region.     

Steller sea lion spatial‐use patterns derived from a Bayesian model of opportunistic observations

Despite acquisition of a substantial catalog of telemetry data from Steller sea lions (Eumetopias jubatus) over the past two decades, scientists still lack comprehensive regionally explicit knowledge about Steller sea lion habitat use. The Platforms of Opportunity data contain records of Steller sea lion sightings throughout the species’ entire range and have potential to fill gaps in knowledge about their spatial use; however, the data have not previously been used because effort (e.g., time spent surveying or area sampled) was not recorded when sightings were obtained. For this study a novel approach was used to overcome the lack of effort data through development of an effort index and a Bayesian negative binomial model. The model quantified Steller sea lion encounter rates and associated uncertainty within 15 × 15 km² grid cells across the species’ entire range. Year‐round, as well as breeding and nonbreeding season encounter rates were estimated. The results of this analysis identify several previously undocumented areas of high use by Steller sea lions, indicate that only 37% of Steller sea lion high‐use areas fall within designated critical habitat, and demonstrate that use of depth and distance from shore as indicators of Steller sea lion habitat is contraindicated.     

Organochlorine exposure and health effects in stranded Steller sea lions (Eumetopias jubatus) and Pacific harbor seals (Phoca vitulina richardii) from Oregon and southern Washington coasts

Organochlorine (OC) pesticides and polychlorinated biphenyls (PCBs) have been detected in a variety of marine mammal species at levels associated with adverse health effects. Little is known about OC levels and impacts on health in pinnipeds with different life histories. We determined the health and levels of 18 OC pesticides and 16 PCB congeners in blubber samples from 20 Steller sea lions and 39 Pacific harbor seals stranded from Oregon and Southern Washington. The most commonly detected OC at the highest concentration was p,p′- dichlorodiphenyldichloroethylene (DDE). PCBs were detected in all samples as well. Hypothesis testing indicated that diseased Steller sea lions (males and females combined) had higher contaminant concentrations than healthy Steller sea lions, and diseased Pacific harbor seals had higher concentrations of total OCs than healthy animals. Differences were also noted between diseased and healthy animals when looking at individual sexes of each species. Diseased Steller sea lions had higher mean contaminant levels than diseased harbor seals and healthy Steller sea lions had higher mean contaminant concentrations than healthy Pacific harbor seals. These results show that species differences exist in both contaminant loads and sensitivity to contaminants, which may be due to differences in life histories and physiology.     

Mercury Concentrations in Hair from Neonatal and Juvenile Steller Sea Lions (Eumetopias jubatus): Implications Based on Age and Region in this Northern Pacific Marine Sentinel Piscivore

Mercury is a global contaminant of concern for the fetus and the neonate of piscivores. Methylmercury, produced within marine ecosystems, is of particular concern as a readily absorbed neurotoxicant transported across the blood brain barrier and transplacentally. In the North Pacific Ocean, Steller sea lions are broadly distributed apex predators and, as such, integrate complex food webs and the associated exposure and possible adverse effects of toxic and infectious agents. Hair, including lanugo, was examined using regional and age groupings to assess mercury concentrations in young Alaskan Steller sea lions. The highest concentrations of mercury occurred in the youngest animals, likely via in utero exposure. Based on the adverse developmental outcomes of methylmercury toxicity this specific cohort is of concern. Regionally, higher concentrations of mercury were observed in the endangered western population of Steller sea lions and mirrored patterns observed in human biomonitoring studies of Alaskan coastal communities. These data have broader implications with respect to human and ecosystem health as Steller sea lions rely on similar prey species and foraging areas as those targeted by commercial fisheries and subsistence users and are therefore valuable sentinels of marine ecosystem health.     

ASSESSING KILLER WHALE PREDATION ON STELLER SEA LIONS FROM FIELD OBSERVATIONS IN KENAI FJORDS, ALASKA

The behavioral and predatory patterns of Gulf of Alaska (GOA) transient killer whales ( Orcinus orca ) were studied between 2000 and 2005 using remote video and vessel-based observations near the Chiswell Island Steller sea lion ( Eumetopias jubatus ) rookery and in the broader Kenai Fjords (KF) region of the northern GOA. GOA transient killer whales were observed on 118 d over the 6-yr period; the median group size was two (range: 1–9). Nine predation events were observed from vessels and an additional sixteen were inferred from remote video studies; all involved Steller sea lions. Estimates from field observations suggest that fifty-nine sea lions were consumed over the summer seasons of 2002–2005; whereas estimates based on published caloric requirements of transient killer whales would suggest a loss of 103 sea lions over the same time period. GOA transients spent a large proportion (43%) of their time resting which may be a strategy for conserving energy. Predation on sea lion pups at the Chiswell Island rookery was greatest during years when a single killer whale was foraging alone and when a 1.5-yr-old calf was evidently being trained to handle prey. Predation on pups was low during years when killer whales were foraging in groups and were observed and presumed to be taking mostly juvenile sea lions. Our study suggests that GOA transients are having a minor effect on the recovery of Steller sea lions in the GOA.     

Assessment of Competition between Fisheries and Steller Sea Lions in Alaska Based on Estimated Prey Biomass,Fisheries Removals and Predator Foraging Behaviour

A leading hypothesis to explain the dramatic decline of Steller sea lions (Eumetopias jubatus) in western Alaska during the latter part of the 20th century is a change in prey availability due to commercial fisheries. We tested this hypothesis by exploring the relationships between sea lion population trends, fishery catches, and the prey biomass accessible to sea lions around 33 rookeries between 2000 and 2008. We focused on three commercially important species that have dominated the sea lion diet during the population decline: walleye pollock, Pacific cod and Atka mackerel. We estimated available prey biomass by removing fishery catches from predicted prey biomass distributions in the Aleutian Islands, Bering Sea and Gulf of Alaska; and modelled the likelihood of sea lions foraging at different distances from rookeries (accessibility) using satellite telemetry locations of tracked animals. We combined this accessibility model with the prey distributions to estimate the prey biomass accessible to sea lions by rookery. For each rookery, we compared sea lion population change to accessible prey biomass. Of 304 comparisons, we found 3 statistically significant relationships, all suggesting that sea lion populations increased with increasing prey accessibility. Given that the majority of comparisons showed no significant effect, it seems unlikely that the availability of pollock, cod or Atka mackerel was limiting sea lion populations in the 2000s.     

Interactions between killer whales (<Emphasis Type="Italic">Orcinus orca</Emphasis>) and Steller sea lions (<Emphasis Type="Italic">Eumetopias jubatus</Emphasis>) in the vicinity of Brat Chirpoev Island,Kuril Islands

The behaviors of breeding Steller sea lions in response to encounters with killer whales near the shore were observed on Brat Chirpoev Island, Kuril Islands between May and July 2002–2007. Approaches by killer whales and sea lion behavior was observed visually and recorded. Killer whales approached the rookery 104 times during the entire period of observations (289 days). In most cases (n = 95), beached sea lions did not show any apparent reactions to the presence of killer whales, and there were no observed interactions. Sea lions showed agitation during nine of the approaches; five of these events were considered to be predation attempts. The killer whales attacked the sea lions three times, however all the attacks were unsuccessful. We recorded two different types of responses towards the killer whales: (1) beaching on the shore (three times) and (2) mass exodus from the rookery with subsequent formation of a tight, actively swimming and vocalizing group (six times). The latter is the first recorded observation of this behavior for Steller sea lions. The observation suggests a low degree of interactions between these two species near the studied rookery. Despite the numerous observations of killer whales near the rookery, there were no observations of direct predation on sea lions. It is likely the killer whale predation has little or no direct impact on the Steller sea lion population on Brat Chirpoev Islands during the breeding period.     

Surface temperature patterns in seals and sea lions: A validation of temporal and spatial consistency

We assessed infrared thermography (IRT) as a tool for evaluating spatial and temporal surface temperature patterns in juvenile female harbor seals (Phoca vitulina, n=6) and adult female Steller sea lions (Eumetopias jubatus, n=2). Following a technical assessment of the influence of environmental parameters on the specific camera to be used, we identified regional and seasonal variability of surface temperatures. Variation was observed in several seasonal transitions (winter, reproductive, molt) in ten monitored body regions. Spatially and temporally consistent thermal patterns in the shoulder, axillae, foreflipper and hindflipper suggest thermal windows in both species.     

The decline of Steller sea lions Eumetopias jubatus in Alaska: a review of the nutritional stress hypothesis

1. The decline of Steller sea lions Eumetopias jubatus in the Gulf of Alaska and Aleutian Islands between the late 1970s and 1990s may have been related to reduced availability of suitable prey. Many studies have shown that pinnipeds and other mammals suffering from nutritional stress typically exhibit reduced body size, reduced productivity, high mortality of pups and juveniles, altered blood chemistry and specific behavioural modifications. 2. Morphometric measurements of Steller sea lions through the 1970s and 1980s in Alaska indicate reduced body size. Reduced numbers of pups born and an apparent increase in juvenile mortality rates also appear to be nutritionally based. Blood chemistry analyses have further shown that Steller sea lions in the Gulf of Alaska and Aleutian Islands area exhibited signs of an acute phase reaction, or immune reaction, in response to unidentified physical and/or environmental stress. Behavioural studies during the 1990s have not noted any changes that are indicative of an overall shortage in the quantity of prey available to lactating female sea lions. 3. The data collected in Alaska are consistent with the hypothesis that Steller sea lions in the declining regions were nutritionally compromised because of the relative quality of prey available to them (chronic nutritional stress), rather than because of the overall quantity of fish per se (acute nutritional stress). This is further supported by captive studies that indicate the overall quality of prey that has been available to Steller sea lions in the declining population could compromise the health of Steller sea lions and hinder their recovery.     

No Evidence of Metabolic Depression in Western Alaskan Juvenile Steller Sea Lions (Eumetopias jubatus)

Steller sea lion (Eumetopias jubatus) populations have undergone precipitous declines through their western Alaskan range over the last four decades with the leading hypothesis to explain this decline centering around changing prey quality, quantity, or availability for this species (i.e., nutritional stress hypothesis). Under chronic conditions of reduced food intake sea lions would conserve energy by limiting energy expenditures through lowering of metabolic rate known as metabolic depression. To examine the potential for nutritional stress, resting metabolic rate (RMR) and body composition were measured in free-ranging juvenile Steller sea lions (N = 91) at three distinct geographical locations (Southeast Alaska, Prince William Sound, Central Aleutian Islands) using open-flow respirometry and deuterium isotope dilution, respectively. Average sea lion RMR ranged from 6.7 to 36.2 MJ d⁻¹ and was influenced by body mass, total body lipid, and to a lesser extent, ambient air temperature and age. Sea lion pups captured in the Aleutian Islands (region of decline) had significantly greater body mass and total body lipid stores when compared to pups from Prince William Sound (region of decline) and Southeast Alaska (stable region). Along with evidence of robust body condition in Aleutian Island pups, no definitive differences were detected in RMR between sea lions sampled between eastern and western populations that could not be accounted for by higher percent total body lipid content, suggesting that that at the time of this study, Steller sea lions were not experiencing metabolic depression in the locations studied.     

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.     

STELLER SEA LION STATUS AND TREND IN SOUTHEAST ALASKA: 1979–1997

Steller sea lion (Eumetopias jubatus) numbers in the United States declined by about 75% over the past 20+ yr. They are classified, under the U. S. Endangered Species Act, as “threatened” in the eastern portion of their range and as “endangered” in the western portion. We analyzed trends in numbers of pup and non-pup Steller sea lions counted in Southeast Alaska between 1979 and 1997. Sea lion numbers, based on counts of pups on rookeries, increased by an average of 5.9% per year between 1979 and 1997. However, numbers of pups increased at a much slower rate (+ 1.7% per year) between 1989 and 1997. For counts of non-pup Steller sea lions we used models that controlled for the effects of date, time, and tide at the time of the survey to analyze trends. This technique reduced bias and increased precision of the resulting trend estimates. Numbers of sea lions were stable (+0.5%) between 1989 and 1996, based on counts of non-pups. We estimated the Southeast Alaska breeding population of Steller sea lions at about 19,000 animals of all ages in 1997, a level that is probably near the highest in recorded history.     

Population growth and colonization of Steller sea lions in the Glacier Bay region of southeastern Alaska: 1970s–2009

We estimated trends in numbers of Steller sea lions in the Glacier Bay region of the eastern population from the 1970s to 2009. We documented the colonization of several new haul‐outs and the transition of one haul‐out (Graves Rocks) to a rookery, assessed seasonal patterns in distribution, and compared counts from different observation platforms. Sea lions increased in the region by 8.2%/yr (95%CI = 6.4%–10.0%), with the most growth at South Marble Island in Glacier Bay (16.6%/yr, 1991–2009) and rapid growth in Cross Sound. Seasonal patterns in the distribution of sea lions were likely influenced by new breeding opportunities and the seasonal availability of prey. Factors that likely contributed to the exceptional growth include availability of new habitat following deglaciation, immigration, redistribution, decreases in mortality, and ecosystem‐level changes. The rapid increase in sea lion numbers in this region is of particular interest in light of dramatic declines in the western population and evidence that Steller sea lions from both the eastern and western populations colonized the Graves Rocks rookery. The colonization and rookery development in this dynamic area may signal the reversal of the reproductive isolation of the two populations.     

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.     

Impact of changing diet regimes on Steller sea lion body condition

A leading theory for the cause of the decline of Steller sea lions is nutritional stress, which led to chronic high juvenile mortality and possibly episodic adult mortality. Nutritional stress may have resulted from either poor quality or low abundance of prey. The objective of this study was to determine whether we could predict shifts in body condition (i.e., body mass or body fat content) over different seasons associated with a change in diet (i.e., toward lower quality prey). Captive Steller sea lions (n= 3) were fed three different diet regimes, where Diet 1 approximated the diet in the Kodiak area in the 1970s prior to the documented decline in that area, Diet 2 approximated the species composition in the Kodiak area after the decline had begun, and Diet 3 approximated the diet in southeast Alaska where the Steller sea lion population has been increasing for over 25 yr. All the animals used in this study were still growing and gained mass regardless of diet. Body fat (%) varied between 13% and 28%, but was not consistently high or low for any diet regime or season. Mean intake (in kg) of Diet 2 was significantly greater for all sea lions during all seasons. All animals did, however, tend to gain less body mass on Diets 2 and 3, as well as during the breeding and postbreeding seasons. They also tended to gain more mass during the winter and on Diet 1, though these differences were not statistically significant. Thus, changing seasonal physiology of Steller sea lions appears to have more impact on body condition than quality of prey, provided sufficient quantity of prey is available. Steller sea lions are opportunistic predators and are evidently able to thrive on a variety of prey. Our results indicate that Steller sea lions are capable of compensating for prey of low quality.     

RETROSPECTIVE ISOTOPIC ANALYSES OF STELLER SEA LION TOOTH ANNULI AND SEABIRD FEATHERS: A CROSS-TAXA APPROACH TO INVESTIGATING REGIME AND DIETARY SHIFTS IN THE GULF OF ALASKA

Stable isotope (δ¹⁵N and δ¹³C) values of individual tooth annuli of female Steller sea lions ( n = 120) collected from the 1960s through the 1980s were used for retrospective analyses of temporal changes in food webs in the Gulf of Alaska and North Pacific Ocean. We also examined isotopically contour feathers of tufted puffins ( n = 135) and crested auklets ( n = 37) through this period to test for broader isotopic patterns indicative of whole food web changes. Steller sea lions decreased slightly in δ¹³C and increased in δ¹⁵N values, suggesting an increasing trophic level and change in foraging location or oceanographic isotopic signature. Steller sea lion first and second tooth annuli were enriched in ¹⁵N and depleted in ¹³C compared with subsequent annuli, indicating the effects of maternal influence through weaning. The general pattern of increasing δ¹⁵N values among Steller sea lions supports previous conclusions regarding a reduction or redistribution of forage fishes and an increase of demersal and semi-demersal species in the North Pacific ecosystem. There were no significant changes in δ¹⁵N values for either bird species. However, δ¹³C values in both bird species again suggested changes in foraging location or a shift in oceanographic currents.     

DEVELOPMENT OF DISPERSAL, MOVEMENT PATTERNS, AND HAUL-OUT USE BY PUP AND JUVENILE STELLER SEA LIONS (EUMETOPIAS JUBATUS) IN ALASKA

Population declines of Steller sea lions ( Eumetopias juhatus ) in western Alaska (west of 144°W) may be a result of reduced juvenile survival. We used satellite telemetry to study the at-sea distribution and movement patterns of pup (1.6–11.9 mo) and juvenile (12.0–35.1 mo) Steller sea lions. We studied trip distance, duration, and interhaul-out movements of sea lions in relation to age, sex, and month of year in the decreasing western population (WP; Prince William Sound, Kodiak, Aleutian Islands, Alaska) and the increasing eastern population (EP; Southeast Alaska). We deployed 103 satellite transmitters (29 WP; 74 EP) on sea lions between 1998 and 2001. Round trip distance and duration increased with age, trip distance was greater in the WP than the EP, trip duration was greater for females than males, and haul-out use was clustered. Changes in round trip distance and duration occurred from April to June for all age classes studied indicating that the annual timing of weaning may be less variable than the age of weaning. Overall, 90% of round trips were ≤ 15 km from haul-outs and 84% were <20 h, indicating nearshore areas adjacent to haulouts are critical to the developing juvenile.     

QUANTIFICATION OF TERRESTRIAL HAUL-OUT AND ROOKERY CHARACTERISTICS OF STELLER SEA LIONS

Steller sea lions ( Eumetopias jubatus ) are known to have occupied the same terrestrial haul-out and rookery sites across the North Pacific Rim for centuries, but it is not known why they choose and stay at these locations, or what defines their preferred habitat. Classifying and comparing the shoreline type of haul-outs and rookeries against sites not used by Steller sea lions showed that they preferentially locate their haul-outs and rookeries on exposed rocky shorelines and wave-cut platforms. However, no preference was found for selecting rookeries on sheltered shore types. Shoreline types used less frequently by sea lions included fine-to-medium-grained sand beaches, mixed sand and gravel beaches, gravel beaches, and sheltered rocky shores. Quantifying the shoreline types used by sea lions confirms anecdotal reports of habitat preferences and may prove useful in identifying and protecting sea lion terrestrial habitat, or in forecasting how climate change might affect the distribution of sea lions.     

The use of fractal image statistics in the estimation of lateral spatial extent

It has been argued that the characteristics of many commonly occurring surface textures are such that the resulting luminance distributions have the statistical properties of fractals, over a wide range of spatial scales. We show that, when fractal luminance distributions are spatially filtered, the spatial density of zero-crossings obtained is inversely proportional to the scale of filtering, and is not strongly dependent on the fractal dimension of the pattern used. We propose that this predictable property of natural images could provide a basis for the estimation of lateral spatial extent by counting zero-crossings within an interval at a variety of spatial scales, and averaging over spatial scale. We carried out experiments to compare the relative apparent lateral extents of fractal patterns and patterns of equally spaced bars, as a function of the number of bars. The results are in good agreement with theory.