Ecosystem response persists after a prolonged marine heatwave.

Some of the longest and most comprehensive marine ecosystem monitoring programs were established in the Gulf of Alaska following the environmental disaster of the Exxon Valdez oil spill over 30 years ago. These monitoring programs have been successful in assessing recovery from oil spill impacts, and their continuation decades later has now provided an unparalleled assessment of ecosystem responses to another newly emerging global threat, marine heatwaves. The 2014-2016 northeast Pacific marine heatwave (PMH) in the Gulf of Alaska was the longest lasting heatwave globally over the past decade, with some cooling, but also continued warm conditions through 2019. Our analysis of 187 time series from primary production to commercial fisheries and nearshore intertidal to offshore oceanic domains demonstrate abrupt changes across trophic levels, with many responses persisting up to at least 5 years after the onset of the heatwave. Furthermore, our suite of metrics showed novel community-level groupings relative to at least a decade prior to the heatwave. Given anticipated increases in marine heatwaves under current climate projections, it remains uncertain when or if the Gulf of Alaska ecosystem will return to a pre-PMH state.

Assessing oxidative stress in Steller sea lions (Eumetopias jubatus): Associations with mercury and selenium concentrations.

Selenium (Se) bioavailability is required for synthesis and function of essential Se-dependent antioxidants, including the enzyme glutathione peroxidase (GPx). Strong interactions between monomethyl mercury and Se impair the critical antioxidant role of Se. Approximately 20% of Steller sea lion (Eumetopias jubatus, SSL) pups sampled in the western Aleutian Islands, Alaska, had total Hg concentrations ([THg]) measured in hair and whole blood above thresholds of concern for adverse physiologic effects in pinnipeds. Importantly, low molar ratios of TSe:THg, in some cases < 1 in several tissues (hair, liver, pelt, muscle, spleen, intestine, heart, lungs, brain) were documented for one SSL pup with [THg] above threshold of concern, which may lead to antioxidant deficiency. Our aim with this study was to evaluate the relationship between circulating [THg], [MeHg+], [TSe] and TSe:THg molar ratio status relative to oxidative stress and antioxidants measured during general anesthesia in free-ranging SSL. We captured, anesthetized and sampled newborn SSL pups at rookeries located in the Aleutian Islands or Gulf of Alaska. Biomarkers analyzed for oxidative stress included 4-hydroxynenonal and thiobarbituric acid reactive substances (4-HNE and TBARS, respectively, lipid peroxidation), protein carbonyl content (PCC, protein oxidation), and GPx activity as a key indicator for Se-dependent antioxidant defense levels. We found a negative association between TBARS and [TSe], and SSL with low [TSe] had higher concentrations of 4-HNE than those with intermediate [TSe]. These results suggest that SSL with lower [TSe] experience increased lipid peroxidation potentially associated with [THg] status.

Methyl mercury (MeHg) in vitro exposure alters mitogen-induced lymphocyte proliferation and cytokine expression in Steller sea lion (Eumetopias jubatus) pups.

Steller sea lions (Eumetopias jubatus, SSLs) are managed as two distinct population segments within U.S. waters: the endangered western distinct population segment and the recently delisted eastern distinct population segment. Recent studies reported concentrations of mercury in several tissues collected from young SSLs in the Aleutian Islands that were at or above concentrations found to negatively impact health in other fish-eating mammals. However, there are limited studies which have investigated the range of mercury concentrations that may negatively influence the SSL immune system. This study assessed relationships between methyl mercury (MeHg+) concentrations and two immune functions, lymphocyte proliferation and cytokine expression. Peripheral blood mononuclear cells (PBMCs) were isolated and cryopreserved from pups on three rookeries within the western distinct population segment: Chiswell Island, Ulak, and Agattu Islands. Lymphocyte proliferation and cytokine expression were assessed in vitro using thawed PBMCs with exposure to MeHg+ (unexposed control, 0.001, 0.01, and 0.1 µg/ml). Lymphocyte proliferation was measured without and with stimulation with a T cell mitogen (ConA) and B cell mitogen (LPS) and the concentration of cytokines was measured in the cell culture supernatant (with and without ConA or LPS). Spontaneous lymphocyte proliferation was significantly increased at 0.01 and 0.1 µg/ml. T lymphocyte proliferation was significantly increased at 0.001 µg/ml and 0.1 µg/ml, while B lymphocyte proliferation was decreased at 0.1 µg/ml. Cytokine concentrations for INFγ, IL-10, IL-6, and TNFα were reduced at 0.1 µg/ml upon either T or B cell mitogen stimulation, with the exception for IL-10, where 0.1 µg/ml reduced IL-10 concentration compared to unstimulated cells. These data suggest immune functions were affected by MeHg+ exposure requiring in vivo follow up investigations. The observed modulation of immune functions is of concern as any toxicant-induced modulation may adversely affect the health of individuals, particularly younger animals undergoing periods of critical development.

Contemporary diets of walruses in Bristol Bay, Alaska suggest temporal variability in benthic community structure.

BACKGROUND: Pacific walruses (Odobenus rosmarus divergens) are a conspicuous and important component of the Bristol Bay ecosystem and human social systems, but very little is known about walrus ecology in this region, principally their feeding ecology. The present work provides contemporary data on the diets of walruses at four haulout locations throughout Bristol Bay between 2014 and 2018. METHODS: We analyzed scat and gastrointestinal tract samples from these animals using quantitative polymerase chain reaction to amplify prey DNA, which allowed for diet estimates based on frequencies of prey item occurrence and on the relative importance of dietary items as determined from DNA threshold cycle scores. RESULTS: Diets were highly diverse at all locations, but with some variation in composition that may be related to the time of year that samples were collected (summer vs. autumn), or to spatial variability in the distribution of prey. Overall, polychaetes and tunicates had the highest frequencies of occurrence and relative abundances in 2014-15, but a major change in diet appears to have occurred by 2017-18. While some sample sizes were small, diets in these later years contrasted sharply, with a greater prevalence of sea cucumbers and mollusks, and reduced importance of decapods and fishes compared to the earlier years. Prey identified in scat samples from one collection site also contrasted sharply with those reported from the same location in 1981. The apparent temporal shifts in walrus prey may represent a changing benthic ecosystem due to warming waters in recent decades.

Spatial distribution, movements, and geographic range of Steller sea lions (Eumetopias jubatus) in Alaska.

The two stocks of Steller sea lions (Eumetopias jubatus) in Alaska include an endangered western stock, recently recovering in parts of its range following decades of decline, and an eastern stock which was removed from the U.S. Endangered Species List in 2013 following increasing numbers since the 1970s. Information on overlapping distributions of eastern and western sea lions is needed for management considerations. We analyzed >30,000 sightings collected from 2000-2014 of 2,385 sea lions that were branded as pups at 10 Alaskan rookeries to examine mesoscale (mostly <500km) spatial distribution, geographic range, and geographic population structure based on natal rookery, sex, and age during breeding and non-breeding seasons. Analyses of summary movement measures (e.g., natal rookery, sex, and age-class differences in spatial distribution and geographic range) indicate wide variation in rookery-specific movement patterns. Correlations between movement measures and population dynamics suggested movement patterns could be a function of density dependence. Animals from larger rookeries, and rookeries with slower population growth and lower survival, had wider dispersion than animals from smaller rookeries, or rookeries with high growth and survival. Sea lions from the largest rookery, Forrester Island, where survival and population trends are lowest, were the most widely distributed. Analysis of geographic population structure indicated that animals born in the eastern Aleutian Islands had the most distinct movements and had little overlap with other western sea lions. Northern Southeast Alaska, within the eastern stock, is the area of greatest overlap between stocks, and is important to western animals, especially those born in Prince William Sound. Detailed knowledge of distribution and movements of western sea lions is useful for defining recovery and population trend analysis regions that better reflect dispersion and population structure and provides valuable information to managers as critical habitat is re-evaluated and the location of the stock boundary reconsidered.

Population Trend and Elasticities of Vital Rates for Steller Sea Lions (Eumetopias jubatus) in the Eastern Gulf of Alaska: A New Life-History Table Analysis.

Steller sea lion (Eumetopias jubatus) numbers are beginning to recover across most of the western distinct population segment following catastrophic declines that began in the 1970s and ended around the turn of the century. This study makes use of contemporary vital rate estimates from a trend-site rookery in the eastern Gulf of Alaska (a sub-region of the western population) in a matrix population model to estimate the trend and strength of the recovery across this region between 2003 and 2013. The modeled population trend was projected into the future based on observed variation in vital rates and a prospective elasticity analysis was conducted to determine future trends and which vital rates pose the greatest threats to recovery. The modeled population grew at a mean rate of 3.5% per yr between 2003 and 2013 and was correlated with census count data from the local rookery and throughout the eastern Gulf of Alaska. If recent vital rate estimates continue with little change, the eastern Gulf of Alaska population could be fully recovered to pre-decline levels within 23 years. With density dependent growth, the population would need another 45 years to fully recover. Elasticity analysis showed that, as expected, population growth rate (λ) was most sensitive to changes in adult survival, less sensitive to changes in juvenile survival, and least sensitive to changes in fecundity. A population decline could be expected with only a 6% decrease in adult survival, whereas a 32% decrease in fecundity would be necessary to bring about a population decline. These results have important implications for population management and suggest current research priorities should be shifted to a greater emphasis on survival rates and causes of mortality.

The influence of year, laying date, egg fertility and incubation, individual hen, hen age and mass and clutch size on maternal immunoglobulin Y concentration in captive Steller's and spectacled eider egg yolk.

Steller's eiders and spectacled eiders are sea duck species whose populations have declined significantly and infectious diseases could influence offspring survival. Therefore, the maternal transfer of immunoglobulin Y (IgY) into yolk was investigated in captive Steller's and spectacled eiders during the 2007-2013 breeding seasons. This project had two objectives: establish baseline IgY levels in Steller's and spectacled eider yolk under controlled captive conditions and evaluate the effect of year, laying date, egg fertility, egg incubation duration, individual hen, hen age and mass, and laying order to determine which variables influenced IgY levels. Average IgY concentrations were 0.03-0.48 mg ml(-1) in Steller's eider yolk and 0.10-0.51 mg ml(-1) in spectacled eider yolk. The year and individual hen influenced IgY concentration in Steller's and spectacled eider yolk. The laying date was negatively correlated with egg IgY levels for most Steller's eider hens, but laying order was positively correlated with egg IgY concentration for spectacled eiders.

A longitudinal study of Steller sea lion natality rates in the Gulf of Alaska with comparisons to census data.

Steller sea lion (Eumetopias jubatus) numbers in the Western Distinct Population Segment are beginning to recover following the dramatic decline that began in the 1970s and ended around the turn of the century. Low female reproductive rates (natality) may have contributed to the decline and remain an issue of concern for this population. During the 2000s we found high natality among Steller sea lions in the Gulf of Alaska indicating a healthy population. This study extends these previous estimates over an additional three years and tests for interannual variations and long-term trends. We further examine the proportions of pups to adult females observed on the rookery and nearby haulouts during the birthing season to assess whether census data can be used to estimate natality. Open robust design multistate models were built and tested using Program MARK to estimate survival, resighting, and state transition probabilities in addition to other parameters dependent on whether or not a female gave birth in the previous year. Natality was estimated at 70% with some evidence of interannual variation but a long-term increasing or decreasing trend was not supported by the data. Bootstrap and regression comparisons of census data with natality estimates revealed no correlation between the two methods suggesting that census data are not an appropriate proxy for natality in this species. Longitudinal studies of individual animals are an appropriate method for estimating vital rates in species with variable detection over time such as the Steller sea lion. This work indicates that natality remains high in this region and is consistent with a population in recovery.

The effects of birth weight and maternal care on survival of juvenile Steller sea lions (Eumetopias jubatus).

Steller sea lions were listed as endangered following a collapse of the western distinct population beginning in the late 1970s. Low juvenile survival has been implicated as a factor in the decline. I conducted a multistate mark-recapture analysis to estimate juvenile survival in an area of the western population where sea lions are showing signs of recovery. Survival for males and females was 80% between 3 weeks and 1 year of age. Approximately 20% of juveniles continued to be nursed by their mothers between ages 1 and 2 and 10% between ages 2 and 3. Survival for juveniles that suckled beyond 1 year was 88.2% and 89.9% to ages 2 and 3, respectively. In contrast, survival for individuals weaned by age 1 was 40.6% for males and 64.2% for females between ages 1 and 2. Birth mass positively influenced survival for juveniles weaned at age 1 but had little effect on individuals continuing to suckle. Cumulative survival to age 4 was double that estimated during the population decline in this region. Evidence suggests that western Steller sea lions utilize a somewhat different maternal strategy than those in the eastern distinct population. Western adult females generally invest more in their pups during the first year but wean offspring by age 1 more often. This results in better survival to age 1, but greater mortality between ages 1 and 3 compared to the eastern population. Different maternal strategies may reflect density dependent pressures of populations at opposite levels of abundance.

Inter-population movements of steller sea lions in Alaska with implications for population separation.

Genetic studies and differing population trends support the separation of Steller sea lions (Eumetopias jubatus) into a western distinct population segment (WDPS) and an eastern DPS (EDPS) with the dividing line between populations at 144° W. Despite little exchange for thousands of years, the gap between the breeding ranges narrowed during the past 15-30 years with the formation of new rookeries near the DPS boundary. We analyzed >22,000 sightings of 4,172 sea lions branded as pups in each DPS from 2000-2010 to estimate probabilities of a sea lion born in one DPS being seen within the range of the other DPS (either 'West' or 'East'). Males from both populations regularly traveled across the DPS boundary; probabilities were highest at ages 2-5 and for males born in Prince William Sound and southern Southeast Alaska. The probability of WDPS females being in the East at age 5 was 0.067 but 0 for EDPS females which rarely traveled to the West. Prince William Sound-born females had high probabilities of being in the East during breeding and non-breeding seasons. We present strong evidence that WDPS females have permanently emigrated to the East, reproducing at two 'mixing zone' rookeries. We documented breeding bulls that traveled >6,500 km round trip from their natal rookery in southern Alaska to the northern Bering Sea and central Aleutian Islands and back within one year. WDPS animals began moving East in the 1990s, following steep population declines in the central Gulf of Alaska. Results of our study, and others documenting high survival and rapid population growth in northern Southeast Alaska suggest that conditions in this mixing zone region have been optimal for sea lions. It is unclear whether eastward movement across the DPS boundary is due to less-optimal conditions in the West or a reflection of favorable conditions in the East.

Body condition and endocrine profiles of Steller sea lion (Eumetopias jubatus) pups during the early postnatal period.

Body condition indices have been useful in assessing the health of domestic and free ranging populations of terrestrial mammals. Given the high energy demand and rapid growth during the postnatal period of Steller sea lion (Eumetopias jubatus) (SSL) pups, body condition was expected to be related to concentrations of a suite of hormones (cortisol, aldosterone, thyroxine, triiodothyronine, leptin) previously associated with changes in body mass and composition in developing pinnipeds. Blood samples were collected from free ranging SSL pups of known ages and sex. A body condition index (BCI) previously developed for SSL pups based on a mass and length relationship was applied to 61 SSL pups ranging in age from 5 to 38days old. BCI was not related to pup age. Overall, male pups were larger than females and older pups were larger than younger pups. Aldosterone was negatively correlated with BCI only in female pups, whereas no relationship was observed between aldosterone and BCI in males. Further, male pups had higher aldosterone concentrations than females. Concentrations of cortisol, total and free thyroxine (T4), and total triiodothyronine (T3) decreased when regressed against the elapsed time between researchers' arrival on the rookery and removal of pup from the holding corral for blood collection. While the overall variation attributed to the rookery disturbance was low (r(2)<0.293), it may be of significance for future studies on free ranging pinnipeds. This study adds to the current knowledge of the postnatal changes in free ranging SSL pups by providing ranges of the BCI and several hormone concentrations from an apparently stable population.

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.

Steller sea lion (Eumetopias jubatus) pups undergo a decrease in circulating white blood cells and the ability of T cells to proliferate during early postnatal development.

Postnatal changes in circulating immune components and peripheral blood mononuclear cell (PBMC) proliferation were assessed in Steller sea lion pups (SSL; Eumetopias jubatus). Blood samples were collected for complete blood cell counts including total and differential white blood cell (WBC) counts from 46 pups ranging in age from 5 to 38 days old. Total WBC and neutrophil counts decreased in association with increased age of the pups. The ability of PBMC to proliferate was assessed by in vitro exposure to concanavalin A (ConA) or lipopolysaccharide (LPS) in 21 pups ranging in age from 7 to 32 days old. All SSL pups responded to in vitro stimulation with ConA and LPS 055:B5 indicating peripheral T and B cells are capable of responding to an antigenic challenge. ConA-induced T cell proliferation decreased with age while there was no change in spontaneous proliferation of PBMC or B cells exposed to LPS. The decreases in total WBC, neutrophil counts and T cell proliferation indicates that SSL undergo a period of postnatal development in cell-mediated immune function which is comparatively longer than phocid pups and consistent with other otariids.

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.