REDUCED BODY SIZE OF FEMALE STELLER SEA LIONS FROM A DECLINING POPULATION IN THE GULF OF ALASKA

Nutritional stress is a leading hypothesis behind the decline in numbers of Steller sea lions in the Gulf of Alaska, the Aleutian Islands, and the Bering Sea. To evaluate this hypothesis we compared body growth of female Steller sea lions 1.0–13.9 yr of age collected in the Gulf of Alaska during two time periods, 1975–1978 just prior to or early in the decline and 1985–1986 when the decline was well established. We found that growth, as measured by standard length, axillary girth, and mass, was reduced during the 1980s, supporting the undernutrition hypothesis. We also found a suggestion of reduced growth in our 1970s and 1980s samples when compared to a collection of Steller sea lions obtained from the Gulf of Alaska in 1958. However, no direct link has been demonstrated between undernutrition and the actual decline in numbers.     

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.     

RANGE-WIDE SURVEY AND ESTIMATION OF TOTAL NUMBER OF STELLER SEA LIONS IN 1989

Abstract: The first range-wide survey of Steller (northern) sea lions ( Eumetopias jubatus ) was completed in 1989 with a total of 68,094 adult and juvenile (nonpup) Steller sea lions counted. This total count includes 10,000 in Russia (15% of the range-wide count), 47,960 in Alaska (70%), 6,109 in British Columbia (9%), 2,261 in Oregon (3%), and 1,764 in California (3%). A range-wide pup count was not obtained. We estimated the 1989 world population based on a calculation for total pups and obtained a range-wide estimate of 116,000 total animals, or about 39–48% of the 240,000-300,000 estimated 30 yr ago.     

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.     

INCIDENTAL MORTALITY OF NORTHERN SEA LIONS IN SHELIKOF STRAIT, ALASKA

The incidental catch of northern sea lions ( Eumetopias jubatus ) in the walleye pollock ( Theragra chalcogramma ) joint-venture fishery in Shelikof Strait, Alaska, was studied during 1982–1984 to assess the nature and magnitude of the catch. Data were obtained by placing U.S. observers on foreign processing vessels. Dead sea lions recovered from trawl nets were counted, sexed and measured, teeth were removed for age determination by dental laminae; and stomach contents were analyzed. Although the fishery has continued to expand both in number of boats and estimated total catch (74,136 metric tons [t] in 1982 to 171,539 t in 1984), the estimated incidental catch of northern sea lions has declined (ranging from 958 to 1,436 in 1982, 216 to 324 in 1983 and 237 to 355 in 1984). Of the sea lions processed, 73 percent were caught between 2000 and 0500 h, probably during net retrieval. Most caught sea lions were females ranging in age from 1–25 yr with a mean age of 6.43 yr; 79 percent of the females were sexually mature and probably part of the reproducing population. Males had a mean age of 4.8 yr and only 12 percent were old enough to obtain and defend territories. Analysis of stomach contents showed that the sea lions consumed pollock the same size as that taken by the commercial fishery. The impact of the incidental catch on the Gulf of Alaska sea lion population is unknown.     

A CRITICAL REVIEW OF THE REGIME SHIFT-"JUNK FOOD"-NUTRITIONAL STRESS HYPOTHESIS FOR THE DECLINE OF THE WESTERN STOCK OF STELLER SEA LION

Steller sea lions ( Eumetopias jubatus ) in the central and western Gulf of Alaska, Aleutian Islands, and Bering Sea have declined by 80% in the last 30 yr. One hypothesis for the decline in this western Steller sea lion population is that a climate regime shift in 1976–1977 changed the species composition of the fish community and reduced the nutritional quality (energy density) of the sea lion prey field. This in turn led to nutritional stress and reduced individual fitness, survival, and reproduction of sea lions. Implications of this regime shift-"junk food" hypothesis are that (1) the recruitment and abundance of supposed high quality species ( e.g. , Pacific herring, Clupea pallasi ) decreased while those of supposed low quality ( e.g. , species in the family Gadidae) increased following the regime shift, (2) Steller sea lion diets shifted in response to this change in fish community structure, and (3) a diet composed principally of gadids ( e.g. , walleye pollock, Theragra chalcogramma ) is detrimental to sea lion fitness and survival. We examine data relating to each of these implications and find little support for the hypothesis that increases in the availability and consumption of gadids following the regime shift are primarily responsible for the decline of the western population of Steller sea lion.     

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.     

Predation on an upper trophic marine predator, the Steller sea lion: evaluating high juvenile mortality in a density dependent conceptual framework

The endangered western stock of the Steller sea lion (Eumetopias jubatus)--the largest of the eared seals--has declined by 80% from population levels encountered four decades ago. Current overall trends from the Gulf of Alaska to the Aleutian Islands appear neutral with strong regional heterogeneities. A published inferential model has been used to hypothesize a continuous decline in natality and depressed juvenile survival during the height of the decline in the mid-late 1980's, followed by the recent recovery of juvenile survival to pre-decline rates. However, these hypotheses have not been tested by direct means, and causes underlying past and present population trajectories remain unresolved and controversial. We determined post-weaning juvenile survival and causes of mortality using data received post-mortem via satellite from telemetry transmitters implanted into 36 juvenile Steller sea lions from 2005 through 2011. Data show high post-weaning mortality by predation in the eastern Gulf of Alaska region. To evaluate the impact of such high levels of predation, we developed a conceptual framework to integrate density dependent with density independent effects on vital rates and population trajectories. Our data and model do not support the hypothesized recent recovery of juvenile survival rates and reduced natality. Instead, our data demonstrate continued low juvenile survival in the Prince William Sound and Kenai Fjords region of the Gulf of Alaska. Our results on contemporary predation rates combined with the density dependent conceptual framework suggest predation on juvenile sea lions as the largest impediment to recovery of the species in the eastern Gulf of Alaska region. The framework also highlights the necessity for demographic models based on age-structured census data to incorporate the differential impact of predation on multiple vital rates.     

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.     

Comparing total body lipid content of young‐of‐the‐year Steller sea lions among regions of contrasting population trends

Steller sea lion (Eumetopias jubatus) young‐of‐the‐year (YOY) are nutritionally dependent upon their dam through the majority of their first year. Several indices of body condition were measured in YOY 1.5–9 mo of age captured in Southeast Alaska (n = 122), the Gulf of Alaska (n = 182), and the Aleutian Islands (n = 38) to test the hypothesis that nutritional stress impacted the ability of adult female Steller sea lions to adequately nourish their late gestation YOY in the central Aleutian Islands in the early 2000s. Body mass (kg) and percent total body lipid content (%TBL) increased with age in all three regions of Alaska that were sampled (P < 0.05). Young‐of‐the‐year 7–9 mo of age were leaner in Southeast Alaska (27.6% ± 1.0%) and Gulf of Alaska (29.5% ± 0.8%) than in the Aleutian Islands (35.7% ± 1.2%, P < 0.001). Condition indices calculated from morphometric measures did not strongly predict the %TBL measured by isotope dilution. The trend for Aleutian Island YOY to have larger body mass and larger body fat reserves are counter to what would be expected if dams were unable to adequately provision their late lactation YOY due to inadequate food availability in the central Aleutian Islands.     

SEASONAL DISTRIBUTION OF STELLER'S SEA LIONS AT ROOKERIES AND HAUL-OUT SITES IN ALASKA

The Steller's sea lion population has declined by 60%-70% over much of Alaska since the late 1970s. Overlap in species composition and sizes of fishes consumed by sea lions and harvested by commercial fisheries, particularly during winter, has led to examination of potential interaction between commercial fisheries and Steller's sea lions. Abundance and distribution data for Steller's sea lions in Alaska were derived from aerial surveys conducted during the breeding season, mid-June to early July 1992, 1994, and 1996. To study winter distribution of sea lions, we conducted aerial surveys during March 1993, November-December 1994, and March 1999. We counted about one-half as many sea lions during winter surveys compared to the breeding-season surveys. Numbers of sea lions at rookery sites dropped off considerably during winter, whereas numbers at haul-out sites did not. We found little evidence of large-scale, seasonal movement, at least for the western stock of sea lions. Rather, differences between summer and winter distribution were primarily a function of sea lions dispersing to local haul-out sites during the winter. Terrestrial sites, both rookeries and haul-outs, clearly are important to Steller's sea lions during the entire year. Individual sites may be occupied year-round or only during particular times of year.     

MASS ESTIMATES USING BODY MORPHOLOGY IN STELLER SEA LIONS

Abstract: Analytical procedures developed from studies on phocids for relating body morphometrics (length and girth) to mass were applied to 390 Steller sea lions from the Gulf of Alaska and the Bering Sea. The equations relating body volume to mass were significant and had very high correlation coefficients for animals from about 60 to over 900 kg with a standard error of ±0.6% in fitted mass. There was a significant difference in these relationships for female sea lions studied in the 1970s and those examined in the 1980s. The latter sea lions were smaller and/or leaner than those collected in the 1970s.     

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.     

KILLER WHALES, WHALING, AND SEQUENTIAL MEGAFAUNAL COLLAPSE IN THE NORTH PACIFIC: A COMPARATIVE ANALYSIS OF THE DYNAMICS OF MARINE MAMMALS IN ALASKA AND BRITISH COLUMBIA FOLLOWING COMMERCIAL WHALING

The hypothesis that commercial whaling caused a sequential megafaunal collapse in the North Pacific Ocean by forcing killer whales to eat progressively smaller species of marine mammals is not supported by what is known about the biology of large whales, the ecology of killer whales, and the patterns of ecosystem change that took place in Alaska, British Columbia, and elsewhere in the world following whaling. A comparative analysis shows that populations of seals, sea lions, and sea otters increased in British Columbia following commercial whaling, unlike the declines noted in the Gulf of Alaska and Aleutian Islands. The declines of seals and sea lions that began in western Alaska around 1977 were mirrored by increases in numbers of these species in British Columbia. A more likely explanation is that the seal and sea lion declines and other ecosystem changes in Alaska stem from a major oceanic regime shift that occurred in 1977. Killer whales are unquestionably a significant predator of seals, sea lions, and sea otters—but not because of commercial whaling.     

COUNTING STELLER SEA LION PUPS IN ALASKA: AN EVALUATION OF MEDIUMFORMAT, COLOR AERIAL PHOTOGRAPHY

Estimates of Steller sea lion ( Eumetopias jubatus ) pup production are valuable for estimating population trend and size. Currently in Alaska, pups are counted by visiting rookeries, driving older animals into the water, then walking through the rookeries and counting the pups, a highly disruptive procedure. At smaller rookeries, with good vantage points, pups are occasionally counted from the periphery of rookeries without disturbing the sea lions. We evaluated counts made from medium-format, color, aerial photographs as an alternative to drive counts and peripheral counts. Neither the peripheral counts nor the aerial photographic counts disturbed animals on the rokeries. There were strong 1:1 linear relationships between photographic counts and drive counts ( r ²= 0.966, P < 0.001) and between photographic counts and peripheral counts ( r ²= 0.999, P < 0.001). Precision was similar for all three methods of counting. We suggest that medium-format, color, aerial photographs is appropriate for routine surveys of Steller sea lion pups in Alaska because it is not disruptive to the hauled-out sea lions and provides comparable estimates with similar precision to drive and peripheral counts. Large areas canbe rapidly surveyed during periods of good weather with a minimum of manpower.     

Parasites of forage fishes in the vicinity of Steller sea lion (Eumetopias jubatus) habitat in Alaska

Fish serve as intermediate hosts for a number of larval parasites that have the potential of maturing in marine mammals such as Steller sea lions (Eumetopias jubatus). We examined the prevalence of parasites from 229 fish collected between March and July 2002 near two islands used by Steller sea lions in Southeast Alaska and island habitats in the Aleutian Islands. Sea lion populations have remained steady in Southeast Alaska but have been declining over the last 30 yr in the Aleutian Islands. Even though the fish samples near the Southeast Alaska haul-outs were composed of numerous small species of fish and the Aleutian Islands catch was dominated by juveniles of commercially harvested species, the parasite fauna was similar at all locations. Eleven of the 20 parasite taxa identified were in their larval stage in the fish hosts, several of which have been described from mammalian final hosts. Four species of parasite were more prevalent in Southeast Alaska fish samples, and seven parasite species, including several larval forms capable of infecting marine mammals, were more prevalent in fish from the Aleutian Islands. Nevertheless, parasites available to Steller sea lions from common fish prey are not likely to be a major factor in the decline of this marine mammal species.     

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.     

DISPERSAL, ROOKERY FIDELITY, AND METAPOPULATION STRUCTURE OF STELLER SEA LIONS (EUMETOPIAS JUBATUS) IN AN INCREASING AND A DECREASING POPULATION IN ALASKA

Over the past 24 yr, 8,596 Steller sea lion ( Eumetopias jubatus ) pups were branded on their natal rookeries throughout Alaska with the objectives of determining survival rates, recruitment, movements, and site fidelity. Our objectives here were to examine the extent of dispersal of Steller sea lions away from their natal rookeries, movements between stocks, and degree of natal rookery fidelity. Pups (<1 yr old) usually remained within 500 km of their natal rookery. Branded juveniles dispersed widely and were resighted at distances up to 1,785 km from their natal rookeries. Adults generally remained within 500 km of their natal rookeries. No interchange of breeding animals between the ES (eastern stock) and WS (western stock) was observed. Although natal rookery fidelity was prevalent, 33% of the 12 observations of females branded in the WS during 1987–1988 and 19% of the 29 observations of females branded in the ES during 1994–1995 were observed with newly born pups at sites other than their natal rookeries. Steller sea lions generally conformed to the metapopulation concept as depicted by Hanski and Simberloff (1997), with local breeding populations (rookeries) and movements among these local populations having the potential of affecting local dynamics.     

MAJOR DECLINE IN NUMBER OF HARBOR SEALS, PHOCA VITULINA RICHARDSI, ON TUGIDAK ISLAND, GULF OF ALASKA

Tugidak Island, located in the Gulf of Alaska, was once the site of one of largest local concentrations of harbor seals ( Phoca vitulina richardsi ) in the world. This population, which probably consisted of about 20,500 animals in the mid-1960s declined by about 85% between 1976 and 1988. The population appeared to decline more rapidly during the late 1970s than during the 1980s. Causes for the decline are not apparent. There appear to be both similarities and dissimilarities between this decline and recent declines in abundance of northern fur seals ( Callorhinus ursinus ) and Steller sea lions ( Eumetopias jubatus ) in the Bering Sea and Gulf of Alaska.     

High Natality Rates of Endangered Steller Sea Lions in Kenai Fjords,Alaska and Perceptions of Population Status in the Gulf of Alaska

Steller sea lions experienced a dramatic population collapse of more than 80% in the late 1970s through the 1990s across their western range in Alaska. One of several competing hypotheses about the cause holds that reduced female reproductive rates (natality) substantively contributed to the decline and continue to limit recovery in the Gulf of Alaska despite the fact that there have been very few attempts to directly measure natality in this species. We conducted a longitudinal study of natality among individual Steller sea lions (n = 151) at a rookery and nearby haulouts in Kenai Fjords, Gulf of Alaska during 2003–2009. Multi-state models were built and tested in Program MARK to estimate survival, resighting, and state transition probabilities dependent on whether or not a female gave birth in the previous year. The models that most closely fit the data suggested that females which gave birth had a higher probability of surviving and giving birth in the following year compared to females that did not give birth, indicating some females are more fit than others. Natality, estimated at 69%, was similar to natality for Steller sea lions in the Gulf of Alaska prior to their decline (67%) and much greater than the published estimate for the 2000s (43%) which was hypothesized from an inferential population dynamic model. Reasons for the disparity are discussed, and could be resolved by additional longitudinal estimates of natality at this and other rookeries over changing ocean climate regimes. Such estimates would provide an appropriate assessment of a key parameter of population dynamics in this endangered species which has heretofore been lacking. Without support for depressed natality as the explanation for a lack of recovery of Steller sea lions in the Gulf of Alaska, alternative hypotheses must be more seriously considered.