Stress-related hormones and genetic diversity in sea otters (Enhydra lutris)

Sea otters ( Enhydra lutris ) once ranged throughout the coastal regions of the north Pacific, but were extirpated throughout their range during the fur trade of the 18th and 19th centuries, leaving only small, widely scattered, remnant populations. All extant sea otter populations are believed to have experienced a population bottleneck and thus have lost genetic variation. Populations that undergo severe population reduction and associated inbreeding may suffer from a general reduction in fitness termed inbreeding depression. Inbreeding depression may result in decreased testosterone levels in males, and reduced ability to respond to stressful stimuli associated with an increase in the stress-related adrenal glucocorticoid hormones, cortisol and corticosterone. We investigated correlations of testosterone, cortisol, and corticosterone with genetic diversity in sea otters from five populations. We found a significant negative correlation between genetic diversity and both mean population-level ( r ²= 0.27, P < 0.001) and individual-level ( r ²= 0.54, P < 0.001) corticosterone values, as well as a negative correlation between genetic diversity and cortisol at the individual level ( r ²= 0.17, P = 0.04). No relationship was found between genetic diversity and testosterone ( P = 0.57). The strength of the correlations, especially with corticosterone, suggests potential negative consequences for overall population health, particularly for populations with the lowest genetic diversity.     

Loss of genetic diversity in sea otters (Enhydra lutris) associated with the fur trade of the 18th and 19th centuries

Sea otter (Enhydra lutris) populations experienced widespread reduction and extirpation due to the fur trade of the 18th and 19th centuries. We examined genetic variation within four microsatellite markers and the mitochondrial DNA (mtDNA) d-loop in one prefur trade population and compared it to five modern populations to determine potential losses in genetic variation. While mtDNA sequence variability was low within both modern and extinct populations, analysis of microsatellite allelic data revealed that the prefur trade population had significantly more variation than all the extant sea otter populations. Reduced genetic variation may lead to inbreeding depression and we believe sea otter populations should be closely monitored for potential associated negative effects.     

Translocations maintain genetic diversity and increase connectivity in sea otters,Enhydra lutris

Sea otters, Enhydra lutris, were once abundant along the nearshore areas of the North Pacific. The international maritime fur trade that ended in 1911 left 13 small remnant populations with low genetic diversity. Subsequent translocations into previously occupied habitat resulted in several reintroduced populations along the coast of North America. We sampled sea otters between 2008 and 2011 throughout much of their current range and used 19 nuclear microsatellite markers to evaluate genetic diversity, population structure, and connectivity between remnant and reintroduced populations. Average genetic diversity within populations was similar: observed heterozygosity 0.55 and 0.53, expected heterozygosity 0.56 and 0.52, unbiased expected heterozygosity 0.57 and 0.52, for reintroduced and remnant populations, respectively. Sea otter population structure was greatest between the Northern and Southern sea otters with further structuring in Northern sea otters into Western, Central, and Southeast populations (including the reintroduced populations). Migrant analyses suggest the successful reintroductions and growth of remnant groups have enhanced connectivity and gene flow between populations throughout many of the sampled Northern populations. We recommend that future management actions for the Southern sea otter focus on future reintroductions to fill the gap between the California and Washington populations ultimately restoring gene flow to the isolated California population.     

Predicting reproduction in captive sea otters (Enhydra lutris)

The sea otter (Enhydra lutris) is a threatened species. It is also a popular exhibit animal in many zoos and aquariums worldwide. Unfortunately, sea otters reproduce successfully in only a small number of facilities. Pregnancies vary in duration, and are thought to involve a delayed implantation of about 2–3 months, followed by an implanted phase of 4–5 months. In this study we attempted to identify estrus and pregnancy states, and predict the date of birth in one female sea otter (Mali) housed at the Lisbon Oceanarium. We used different techniques to evaluate her reproductive status, including monitoring behavior to determine estrus, assessing weight changes to determine pregnancy and parturition date, and analyzing fecal hormone samples to determine estrus, pregnancy, and parturition date. During this study, Mali became pregnant four times. Her gestational length varied between 188–255 days. Weight increases >29 kg or 15% above baseline weight suggested pregnancy, and parturition was estimated to occur approximately 3 months thereafter. Fecal hormone (progestagens and estrogen) metabolite data gathered during two of her pregnancies showed that Mali's delayed implantation phase of pregnancy lasted 43–109 days (a typical duration in other sea otters is 100–110 days). Mali's implanted phase lasted a relatively long time (140–145 days compared to an average of 117 days in other sea otters). The combination of the three measurements was a powerful tool that enabled us to determine pregnancy and anticipate the arrival of a new sea otter pup. Zoo Biol 24:73–81, 2005. © 2005 Wiley‐Liss, Inc.     

Reductions in the dietary niche of southern sea otters (Enhydra lutris nereis) from the Holocene to the Anthropocene

The sea otter (Enhydra lutris) is a marine mammal hunted to near extinction during the 1800s. Despite their well‐known modern importance as a keystone species, we know little about historical sea otter ecology. Here, we characterize the ecological niche of ancient southern sea otters (E. lutris nereis) using δ¹³C analysis and δ¹⁵N analysis of bones recovered from archaeological sites spanning ~7,000 to 350 years before present (N = 112 individuals) at five regions along the coast of California. These data are compared with previously published data on modern animals (N = 165) and potential modern prey items. In addition, we analyze the δ¹⁵N of individual amino acids for 23 individuals to test for differences in sea otter trophic ecology through time. After correcting for tissue‐specific and temporal isotopic effects, we employ nonparametric statistics and Bayesian niche models to quantify differences among ancient and modern animals. We find ancient otters occupied a larger isotopic niche than nearly all modern localities; likely reflecting broader habitat and prey use in prefur trade populations. In addition, ancient sea otters at the most southerly sites occupied an isotopic niche that was more than twice as large as ancient otters from northerly regions. This likely reflects greater invertebrate prey diversity in southern California relative to northern California. Thus, we suggest the potential dietary niche of sea otters in southern California could be larger than in central and northern California. At two sites, Año Nuevo and Monterey Bay, ancient otters had significantly higher δ¹⁵N values than modern populations. Amino acid δ¹⁵N data indicated this resulted from shifting baseline isotope values, rather than a change in sea otter trophic ecology. Our results help in better understanding the contemporary ecological role of sea otters and exemplify the strength of combing zooarchaeological and biological information to provide baseline data for conservation efforts.     

Archaeological mitogenomes illuminate the historical ecology of sea otters (Enhydra lutris) and the viability of reintroduction

Genetic analyses are an important contribution to wildlife reintroductions, particularly in the modern context of extirpations and ecological destruction. To address the complex historical ecology of the sea otter (Enhydra lutris) and its failed 1970s reintroduction to coastal Oregon, we compared mitochondrial genomes of pre-extirpation Oregon sea otters to extant and historical populations across the range. We sequenced, to our knowledge, the first complete ancient mitogenomes from archaeological Oregon sea otter dentine and historical sea otter dental calculus. Archaeological Oregon sea otters (n = 20) represent 10 haplotypes, which cluster with haplotypes from Alaska, Washington and British Columbia, and exhibit a clear division from California haplotypes. Our results suggest that extant northern populations are appropriate for future reintroduction efforts. This project demonstrates the feasibility of mitogenome capture and sequencing from non-human dental calculus and the diverse applications of ancient DNA analyses to pressing ecological and conservation topics and the management of at-risk/extirpated species.     

Coastal freshwater runoff is a risk factor for Toxoplasma gondii infection of southern sea otters (Enhydra lutris nereis)

The association among anthropogenic environmental disturbance, pathogen pollution and the emergence of infectious diseases in wildlife has been postulated, but not always well supported by epidemiologic data. Specific evidence of coastal contamination of the marine ecosystem with the zoonotic protozoan parasite, Toxoplasma gondii, and extensive infection of southern sea otters (Enhydra lutris nereis) along the California coast was documented by this study. To investigate the extent of exposure and factors contributing to the apparent emergence of T. gondii in southern sea otters, we compiled environmental, demographic and serological data from 223 live and dead sea otters examined between 1997 and 2001. The T. gondii seroprevalence was 42% (49/116) for live otters, and 62% (66/107) for dead otters. Demographic and environmental data were examined for associations with T. gondii seropositivity, with the ultimate goal of identifying spatial clusters and demographic and environmental risk factors for T. gondii infection. Spatial analysis revealed clusters of T. gondii-seropositive sea otters at two locations along the coast, and one site with lower than expected T. gondii seroprevalence. Risk factors that were positively associated with T. gondii seropositivity in logistic regression analysis included male gender, older age and otters sampled from the Morro Bay region of California. Most importantly, otters sampled near areas of maximal freshwater runoff were approximately three times more likely to be seropositive to T. gondii than otters sampled in areas of low flow. No association was found between seropositivity to T. gondii and human population density or exposure to sewage. This study provides evidence implicating land-based surface runoff as a source of T. gondii infection for marine mammals, specifically sea otters, and provides a convincing illustration of pathogen pollution in the marine ecosystem.     

Lactation and resource limitation affect stress responses,thyroid hormones,immune function,and antioxidant capacity of sea otters (Enhydra lutris)

Lactation is the most energetically demanding stage of reproduction in female mammals. Increased energetic allocation toward current reproduction may result in fitness costs, although the mechanisms underlying these trade‐offs are not well understood. Trade‐offs during lactation may include reduced energetic allocation to cellular maintenance, immune response, and survival and may be influenced by resource limitation. As the smallest marine mammal, sea otters (Enhydra lutris) have the highest mass‐specific metabolic rate necessitating substantial energetic requirements for survival. To provide the increased energy needed for lactation, female sea otters significantly increase foraging effort, especially during late‐lactation. Caloric insufficiency during lactation is reflected in the high numbers of maternal deaths due to End‐Lactation Syndrome in the California subpopulation. We investigated the effects of lactation and resource limitation on maternal stress responses, metabolic regulation, immune function, and antioxidant capacity in two subspecies of wild sea otters (northern: E. l. nereis and southern: E. l. kenyoni) within the California, Washington, and Alaska subpopulations. Lactation and resource limitation were associated with reduced glucocorticoid responses to acute capture stress. Corticosterone release was lower in lactating otters. Cortisol release was lower under resource limitation and suppression during lactation was only evident under resource limitation. Lactation and resource limitation were associated with alterations in thyroid hormones. Immune responses and total antioxidant capacity were not reduced by lactation or resource limitation. Southern sea otters exhibited higher concentrations of antioxidants, immunoglobulins, and thyroid hormones than northern sea otters. These data provide evidence for allocation trade‐offs during reproduction and in response to nutrient limitation but suggest self‐maintenance of immune function and antioxidant defenses despite energetic constraints. Income‐breeding strategists may be especially vulnerable to the consequences of stress and modulation of thyroid function when food resources are insufficient to support successful reproduction and may come at a cost to survival, and thereby influence population trends.     

An unusual genotype of Toxoplasma gondii is common in California sea otters (Enhydra lutris nereis) and is a cause of mortality

Toxoplasma gondii-associated meningoencephalitis is a significant disease of California sea otters (Enhydra lutris nereis), responsible for 16% of total mortality in fresh, beachcast carcasses. Toxoplasma gondii isolates were obtained from 35 California otters necropsied between 1998 and 2002. Based on multi-locus PCR-restriction fragment length polymorphism and DNA sequencing at conserved genes (18S rDNA, ITS-1) and polymorphic genes (B1, SAG1, SAG3 and GRA6), two distinct genotypes were identified: type II and a novel genotype, here called type x, that possessed distinct alleles at three of the four polymorphic loci sequenced. The majority (60%) of sea otter T. gondii infections were of genotype x, with the remaining 40% being of genotype II. No type I or III genotypes were identified. Epidemiological methods were used to examine the relationship between isolated T. gondii genotype(s) and spatial and demographic risk factors, such as otter stranding location and sex, as well as specific outcomes related to pathogenicity, such as severity of brain inflammation on histopathology and T. gondii-associated mortality. Differences were identified with respect to T. gondii genotype and sea otter sex and stranding location along the California coast. Localised spatial clustering was detected for both type II (centred within Monterey Bay) and x (centred near Morro Bay)-infected otters. The Morro Bay cluster of type x-infected otters overlaps previously reported high-risk areas for sea otter infection and mortality due to T. gondii. Nine of the 12 otters that had T. gondii-associated meningoencephalitis as a primary cause of death were infected with type x parasites.     

Drift and beaching patterns of sea otter carcasses and car tire dummies

Enumerating and examining marine animal carcasses is important for quantifying mortality rates and determining causes of mortality. Drifter experiments are one tool for estimating at‐sea mortality and determining factors affecting carcass drift, but they require validation to confirm drifters accurately replicate the drift characteristics of the species of interest. The goal of this study was to determine whether dummies constructed from car tires were appropriate substitutes for sea otter (Enhydra lutris) carcasses. We released 33 sets of targets (carcasses and dummies) in a one‐to‐one ratio on 15 randomly chosen dates between January 1995 and December 1996. They were telemetrically tracked until they beached or were no longer detected. Beaching rates were similar between carcasses (69.7%) and dummies (66.7%). Our results indicated that there was no statistical difference in the drifting pattern, as measured by distance traveled and location, between carcasses and dummies, and that cumulative wind speed, days since release, and release month were predictors of drift patterns. We concluded that dummies constructed from car tires do imitate sea otter carcasses and could be used to estimate at‐sea mortality of sea otters, or, if released during or after an oil spill, could be used to direct search efforts for carcasses.     

AN ANALYSIS OF CALIFORNIA SEA OTTER (ENHYDRA LUTRIS) PELAGE AND INTEGUMENT

The sea otter is associated with a cold, marine habitat, has no insulating fat layer, and relies on its fur layer for insulation. Soiled pelage provides inadequate insulation and can lead to hypothermia and death. Information on sea otter pelage, the surface and bound lipids found in the pelage, and histology of the integument is thus relevant to the development of rehabilitation and management techniques for sea otters soiled with oil. We present detailed data on the sea otter pelage and integument, including hair bundle density (737–2,465 bundles per cm²), hair density per bundle (19–91.1), total hair density (26,413–164,662 hairs per cm²), guardhair length (8.2–26.9 mm), underfur length (4.6–15.8 mm), guardhair diameter (44.0–106.0 μ), underfur diameter (7.6–11.9 μ), angle of hair with respect to the skin (61.9°- 84.3°) and structure of individual hairs as seen with a scanning electron microscope. The hydrocarbon squalene was found to be the major component of the lipids associated with the pelage. Various layers of skin from eight sites on a single animal are described histologically. With the exception of density of the hair coat, sea otter integument is similar to that of domestic carnivores.     

Biological and molecular characterizations of Toxoplasma gondii strains obtained from southern sea otters (Enhydra lutris nereis)

Toxoplasma gondii was isolated from brain or heart tissue from 15 southern sea otters (Enhydra lutris nereis) in cell cultures. These strains were used to infect mice that developed antibodies to T. gondii as detected in the modified direct agglutination test and had T. gondii tissue cysts in their brains at necropsy. Mouse brains containing tissue cysts from 4 of the strains were fed to 4 cats. Two of the cats excreted T. gondii oocysts in their feces that were infectious for mice. Molecular analyses of 13 strains indicated that they were all type II strains, but that they were genetically distinct from one another.     

Ancient DNA reveals genotypic relationships among Oregon populations of the sea otter (<Emphasis Type="Italic">Enhydra lutris</Emphasis>)

The sea otter has experienced a dramatic population decline caused by intense human harvesting, followed by a century of recovery including relocation efforts to reestablish the species across its former range in the eastern Pacific. Although the otter was historically present along the coast in Oregon, there are currently no populations in this region and reintroduction efforts have failed. We examined the mtDNA genotypes of 16 pre-harvest otter samples from two Oregon locations in an attempt to determine the best genotypic match with extant populations. Our amplifications of a 222 base-pair portion of the control region from otters ranging in age from approximately 175–2000 years revealed four genotypes. The genotypic composition of pre-harvest otter populations appears to match best with those of contemporary populations from California and not from Alaska, where reintroduction stocks are typically derived.     

Assessment of clinical pathology and pathogen exposure in sea otters (Enhydra lutris) bordering the threatened population in Alaska

Northern sea otter (Enhydra lutris kenyoni) abundance has decreased dramatically over portions of southwest Alaska, USA, since the mid-1980s, and this stock is currently listed as threatened under the Endangered Species Act. In contrast, adjacent populations in south central Alaska, USA, and Russia have been stable to increasing during the same period. Sea otters bordering the area classified in the recent decline were live-captured during 2004-2006 at Bering Island, Russia, and the Kodiak Archipelago, Alaska, USA, to evaluate differences in general health and current exposure status to marine and terrestrial pathogens. Although body condition was lower in animals captured at Bering Island, Russia, than it was at Kodiak, USA, clinical pathology values did not reveal differences in general health between the two regions. Low prevalences of antibodies (<5%) were found in Kodiak, USA, and on Bering Island, Russia, to Toxoplasma gondii, Sarcocystis neurona, and Leptospira interrogans. Exposure to phocine herpesvirus-1 was found in both Kodiak, USA (15.2%), and Bering Island, Russia (2.3%). Antibodies to Brucella spp. were found in 28% of the otters tested on Bering Island, Russia, compared with only 2.7% of the samples from Kodiak, USA. Prevalence of exposure to Phocine distemper virus (PDV) was 41% in Kodiak, USA, but 0% on Bering Island, Russia. Archived sera from southwest and south-central Alaska dating back to 1989 were negative for PDV, indicating exposure occurred in sea otters in Kodiak, USA, in recent years. Because PDV can be highly pathogenic in na?ve and susceptible marine mammal populations, tissues should be examined to explore the contribution of this virus to otter deaths. Our results reveal an increase in exposure to pathogens in sea otters in Kodiak, Alaska, USA, since the 1990 s.     

STOCK STRUCTURE OF SEA OTTERS (ENHYDRA LUTRIS KENYONI) IN ALASDA

Sea otters in Alaska are recognized as a single subspecies ( Enhydra lutris kenyoni ) and currently managed as a single, interbreeding population. However, geographic and behavioral mechanisms undoubrably constrain sea otter movements on much smaller scales. This paper applies the phylogeographic method (Dizon et al . 1992) and considers distribution, population response, phenotype and genotype data to identify stocks of sea otters within Alaska. The evidence for separate stock identity is genotypic (all stocks), phenotypic (Southcentral and Southwest stocks), and geographic distribution (Southeast stock), whereas population response data are equivocal (all stocks). Differences in genotype frequencies and the presence of unique genotypes among areas indicate restricted gene flow. Genetic exchange may be limited by little or no movement across proposed stock boundaries and discontinuities in distribution at proposed stock boundaries. Skull size differences (phenotypic) between Southwest and Southcentral Alaska populations further support stock separation. Population response information was equivocal in either supporting or refuting stock identity. On the basis of this review, we suggest the following: (1) a Southeast stock extending from Dixon Entrance to Cape Yakataga; (2) a Southcentral stock extending from Cape Yakataga to Cape Douglas including Prince William Sound and Kenai peninsula coast; and (3) a Southwest stock including Alaska Peninsula coast, the Aleutians to Attu Island, Barren, Kodiak, Pribilof Islands, and Bristol Bay.     

Status,trends, and equilibrium abundance estimates of the translocated sea otter population in Washington State

Sea otters (Enhydra lutris kenyoni) historically occurred in Washington State, USA, until their local extinction in the early 1900s as a result of the maritime fur trade. Following their extirpation, 59 sea otters were translocated from Amchitka Island, Alaska, USA, to the coast of Washington, with 29 released at Point Grenville in 1969 and 30 released at La Push in 1970. The Washington Department of Fish and Wildlife has outlined 2 main objectives for sea otter recovery: a target population level and a target geographic distribution. Recovery criteria are based on estimates of population abundance, equilibrium abundance (K), and geographic distribution; therefore, estimates of these parameters have important management implications. We compiled available survey data for sea otters in Washington State since their translocation (1977–2019) and fit a Bayesian state-space model to estimate past and current abundance, and equilibrium abundance at multiple spatial scales. We then used forward projections of population dynamics to explore potential scenarios of range recolonization and as the basis of a sensitivity analysis to evaluate the relative influence of movement behavior, frontal wave speed, intrinsic growth, and equilibrium density on future population recovery potential. Our model improves upon previous analyses of sea otter population dynamics in Washington by partitioning and quantifying sources of estimation error to estimate population dynamics, by providing robust estimates of K, and by simulating long-term population growth and range expansion under a range of realistic parameter values. Our model resulted in predictions of population abundance that closely matched observed counts. At the range-wide scale, the population size in our model increased from an average of 21 independent sea otters (95% CI = 13–29) in 1977 to 2,336 independent sea otters (95% CI = 1,467–3,359) in 2019. The average estimated annual growth rate was 12.42% and varied at a sub-regional scale from 6.42–14.92%. The overall estimated mean K density of sea otters in Washington was 1.71 ± 0.90 (SD) independent sea otters/km² of habitat (1.96 ± 1.04 sea otters/km², including pups), and estimated densities within the current range correspond on average to 87% of mean sub-regional equilibrium values (range = 66–111%). The projected value of K for all of Washington was 5,287 independent sea otters (95% CI = 2,488–8,086) and 6,080 sea otters including pups (95% CI = 2,861–9,300), assuming a similar range of equilibrium densities in currently un-occupied habitats. Sensitivity analysis of simulations of sea otter population growth and range expansion suggested that mean K density estimates in currently occupied sub-regions had the largest impact on predicted future population growth (r² = 0.52), followed by the rate of southward range expansion (r² = 0.26) and the mean K density estimate of currently unoccupied sub-regions to the south of the current range (r² = 0.04). Our estimates of abundance and sensitivity analysis of simulations of future population abundance and geographic range help determine population status in relation to population recovery targets and identify the most influential parameters affecting future population growth and range expansion for sea otters in Washington State.