Genetic diversity and population parameters of sea otters, Enhydra lutris, before fur trade extirpation from 1741-1911

All existing sea otter, Enhydra lutris, populations have suffered at least one historic population bottleneck stemming from the fur trade extirpations of the eighteenth and nineteenth centuries. We examined genetic variation, gene flow, and population structure at five microsatellite loci in samples from five pre-fur trade populations throughout the sea otter's historical range: California, Oregon, Washington, Alaska, and Russia. We then compared those values to genetic diversity and population structure found within five modern sea otter populations throughout their current range: California, Prince William Sound, Amchitka Island, Southeast Alaska and Washington. We found twice the genetic diversity in the pre-fur trade populations when compared to modern sea otters, a level of diversity that was similar to levels that are found in other mammal populations that have not experienced population bottlenecks. Even with the significant loss in genetic diversity modern sea otters have retained historical structure. There was greater gene flow before extirpation than that found among modern sea otter populations but the difference was not statistically significant. The most dramatic effect of pre fur trade population extirpation was the loss of genetic diversity. For long term conservation of these populations increasing gene flow and the maintenance of remnant genetic diversity should be encouraged.     

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.     

Applied zooarchaeology and Oregon Coast sea otters (Enhydra lutris)

The sea otter (Enhydra lutris) was nearly driven to extinction on the Pacific Coast in the 19th century due to intensive commercial hunting and the maritime fur trade. Despite successful reintroduction efforts elsewhere in North America, the Oregon sea otter population remains locally extirpated and listed as endangered. Prior study addressed precontact sea otter teeth from Oregon and found they were not significantly different in absolute size from modern California sea otter (Enhydra lutris nereis) teeth, and smaller than modern Alaska sea otter (Enhydra lutris lutris) teeth. These geographic groupings were later confirmed by an ancient DNA study. The conclusion that distinct geographic populations exist based on tooth size was founded on small samples. Larger samples of teeth, as well as new data on humeri and femora, indicate dimensions vary significantly along a latitudinal cline from California to Alaska. Morphometric analyses of ancient animal remains can be used to examine spatial relationships of phenotypic features and inform conservation biology decisions.     

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.     

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.     

Evaluation of an indirect fluorescent antibody test (IFAT) for demonstration of antibodies to Toxoplasma gondii in the sea otter (Enhydra lutris)

An indirect fluorescent antibody test (IFAT) for detection of Toxoplasma gondii infection was validated using serum from 77 necropsied southern sea otters (Enhydra lutris nereis) whose T. gondii infection status was determined through immunohistochemistry and parasite isolation in cell culture. Twenty-eight otters (36%) were positive for T. gondii by immunohistochemistry or parasite isolation or both, whereas 49 (64%) were negative by both tests. At a cutoff of 1:320, combined values for IFAT sensitivity and specificity were maximized at 96.4 and 67.3%, respectively. The area under the receiver-operating characteristic curve for the IFAT was 0.84. A titer of 1:320 was used as cutoff when screening serum collected from live-sampled sea otters from California (n = 80), Washington (n = 21), and Alaska (n = 65) for T. gondii infection. Thirty-six percent (29 out of 80) of California sea otters (E. lutris nereis) and 38% (8 out of 21) of Washington sea otters (E. lutris kenyoni) were seropositive for T. gondii, compared with 0% (0 out of 65) of Alaskan sea otters (E. lutris kenyoni).     

AN ESTIMATION OF CARRYING CAPACITY FOR SEA OTTERS ALONG THE CALIFORNIA COAST

Carrying capacity (K) for the California sea otter ( Enhydra lutris nereis ) was estimated as a product of the density of sea otters at equilibrium within a portion of their existing range and the total area of available habitat. Equilibrium densities were determined using the number of sea otters observed during spring surveys in 1994, 1995, and 1996 in each of three habitat types where sea otters currently exist. Potential sea otter habitat was defined as from the California coastline to the 40-m isobath and classified as rocky, sandy, or mixed habitat according to the amount of kelp and rocky substrate in the area. The amount of habitat available to sea otters in California was estimated using a Geographic Information Systems (GIS) program. The estimated mean number of sea otters that could be supported by the marine environment to a depth of 40 m in California was 15,941 (95% CI 13,538–18,577). The GIS-based approach incorporated detailed bathymetric contours, produced repeatable and accurate estimates, and served as an innovative method of measuring sea otter habitat. We believe the approach described in this paper represents the best available information on how a sea otter population at equilibrium would be distributed along the California coast.     

Sarcomas in three free-ranging northern sea otters (Enhydra lutris kenyoni) in Alaska

Three sarcomas were diagnosed in wild northern sea otters (Enhydra lutris kenyoni) during the mid- to late 1990s. Histologically, the tumors were a chondrosarcoma and two low-grade fibrosarcomas with myofibroblastic cell differentiation. The three sea otters were surviving in the wild and were killed by hunters.     

Clinical pathology and assessment of pathogen exposure in southern and Alaskan sea otters

The southern sea otter (Enhydra lutris nereis) population in California (USA) and the Alaskan sea otter (E. lutris kenyoni) population in the Aleutian Islands (USA) chain have recently declined. In order to evaluate disease as a contributing factor to the declines, health assessments of these two sea otter populations were conducted by evaluating hematologic and/or serum biochemical values and exposure to six marine and terrestrial pathogens using blood collected during ongoing studies from 1995 through 2000. Samples from 72 free-ranging Alaskan, 78 free-ranging southern, and (for pathogen exposure only) 41 debilitated southern sea otters in rehabilitation facilities were evaluated and compared to investigate regional differences. Serum chemistry and hematology values did not indicate a specific disease process as a cause for the declines. Statistically significant differences were found between free-ranging adult southern and Alaskan population mean serum levels of creatinine kinase, alkaline phosphatase, alanine aminotransferase, aspartate aminotransferase, calcium, cholesterol, creatinine, glucose, phosphorous, total bilirubin, blood urea nitrogen, and sodium. These were likely due to varying parasite loads, contaminant exposures, and physiologic or nutrition statuses. No free-ranging sea otters had signs of disease at capture, and prevalences of exposure to calicivirus, Brucella spp., and Leptospira spp. were low. The high prevalence (35%) of antibodies to Toxoplasma gondii in free-ranging southern sea otters, lack of antibodies to this parasite in Alaskan sea otters, and the pathogen's propensity to cause mortality in southern sea otters suggests that this parasite may be important to sea otter population dynamics in California but not in Alaska. The evidence for exposure to pathogens of public health importance (e.g., Leptospira spp., T. gondii) in the southern sea otter population, and the na?veté of both populations to other pathogens (e.g., morbillivirus and Coccidiodes immitis) may have important implications for their management and recovery.     

Evaluating the current condition of a threatened marine mammal population: Estimating northern sea otter (Enhydra lutris kenyoni) abundance in southwest Alaska

We estimated density and abundance of the threatened southwest Alaska distinct population segment of northern sea otters (Enhydra lutris kenyoni) in two management units. We conducted aerial surveys in Bristol Bay and South Alaska Peninsula management units in 2016, and modeled sea otter density and abundance with Bayesian hierarchical distance sampling models and spatial environmental covariates (depth, distance to shore, depth × distance to shore). Spatial environmental covariates substantially impacted sea otter group density in both management units, but effects sizes differed between the two management units. Abundance (9,733 otters, 95% CrI 6,412–17,819) and density (0.82 otters/km², 95% CrI 0.54–1.49) estimates for Bristol Bay indicated a moderate population size. In contrast, abundance (546 otters, 95% CrI 322–879) and density (0.06 otters/km², 95% CrI 0.03–0.09) estimates indicated a relatively low population size in South Alaska Peninsula. Overall, our results highlight the importance of accounting for the detection process in monitoring at-risk species to reduce the uncertainty associated with making conclusions about population declines.     

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.     

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.     

Archaeological and Contemporary Evidence Indicates Low Sea Otter Prevalence on the Pacific Northwest Coast During the Late Holocene

Ecosystems - The historic extirpation and subsequent recovery of sea otters (Enhydra lutris) have profoundly changed coastal social-ecological systems across the northeastern Pacific. Today, the...     

Patterns of mortality in southern sea otters (Enhydra lutris nereis) from 1998-2001

Detailed postmortem examination of southern sea otters (Enhydra lutris nereis) found along the California (USA) coast has provided an exceptional opportunity to understand factors influencing survival in this threatened marine mammal species. In order to evaluate recent trends in causes of mortality, the demographic and geographic distribution of causes of death in freshly deceased beachcast sea otters necropsied from 1998-2001 were evaluated. Protozoal encephalitis, acanthocephalan-related disease, shark attack, and cardiac disease were identified as common causes of death in sea otters examined. While infection with acanthocephalan parasites was more likely to cause death in juvenile otters, Toxoplasma gondii encephalitis, shark attack, and cardiac disease were more common in prime-aged adult otters. Cardiac disease is a newly recognized cause of mortality in sea otters and T. gondii encephalitis was significantly associated with this condition. Otters with fatal shark bites were over three times more likely to have pre-existing T. gondii encephalitis suggesting that shark attack, which is a long-recognized source of mortality in otters, may be coupled with a recently recognized disease in otters. Spatial clusters of cause-specific mortality were detected for T. gondii encephalitis (in Estero Bay), acanthocephalan peritonitis (in southern Monterey Bay), and shark attack (from Santa Cruz to Point A?o Nuevo). Diseases caused by parasites, bacteria, or fungi and diseases without a specified etiology were the primary cause of death in 63.8% of otters examined. Parasitic disease alone caused death in 38.1% of otters examined. This pattern of mortality, observed predominantly in juvenile and prime-aged adult southern sea otters, has negative implications for the overall health and recovery of this population.     

Transmission of Toxoplasma: clues from the study of sea otters as sentinels of Toxoplasma gondii flow into the marine environment

Toxoplasma gondii affects a wide variety of hosts including threatened southern sea otters (Enhydra lutris nereis) which serve as sentinels for the detection of the parasite's transmission into marine ecosystems. Toxoplasmosis is a major cause of mortality and contributor to the slow rate of population recovery for southern sea otters in California. An updated seroprevalence analysis showed that 52% of 305 freshly dead, beachcast sea otters and 38% of 257 live sea otters sampled along the California coast from 1998 to 2004 were infected with T. gondii. Areas with high T. gondii exposure were predominantly sandy bays near urban centres with freshwater runoff. Genotypic characterisation of 15 new T. gondii isolates obtained from otters in 2004 identified only X alleles at B1 and SAG1. A total of 38/50 or 72% of all otter isolates so far examined have been infected with a Type X strain. Type X isolates were also obtained from a Pacific harbor seal (Phoca vitulina) and California sea lion (Zalophus californianus). Molecular analysis using the C8 RAPD marker showed that the X isolates were more genetically heterogeneous than archetypal Type I, II and III genotypes of T. gondii. The origin and transmission of the Type X T. gondii genotype are not yet clear. Sea otters do not prey on known intermediate hosts for T. gondii and vertical transmission appears to play a minor role in maintaining infection in the populations. Therefore, the most likely source of infection is by infectious, environmentally resistant oocysts that are shed in the feces of felids and transported via freshwater runoff into the marine ecosystem. As nearshore predators, otters serve as sentinels of protozoal pathogen flow into the marine environment since they share the same environment and consume some of the same foods as humans. Investigation into the processes promoting T. gondii infections in sea otters will provide a better understanding of terrestrial parasite flow and the emergence of disease at the interface between wildlife, domestic animals and humans.     

SEA OTTER DIETS IN A DECLINING POPULATION IN ALASKA

Diet of sea otters ( Enhydra lutris ) using a haulout site on the north side of the Alaska Peninsula was determined from 50 scats. Dominant prey species were mussels ( Mytilus edulis ), followed by three species of clams ( Siliqua spp., Spisula polynyma , and Tellina lutea ), sand dollars ( Echinarachnius parma ), and helmet crabs ( Telmessus cheiragonus ). Our results support preliminary findings by Cim-berg et al. (1984) that this sea otter population preys heavily on mussels and that the presence of low caloric value sand dollars in their diet is significant. Coupled with population estimates, our results also provide evidence that this population of sea otters may be declining due, in part, to overdepletion of food resources.     

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.     

Lymphosarcoma in a sea otter (Enhydra lutris)

Lymphoblastic lymphosarcoma involving the mesenteric lymph node and thymus was discovered in a 4 yr old male sea otter (Enhydra lutris). Diagnosis was based on gross and light microscopic studies. The cause of this neoplasm was not determined. This is the first case of lymphosarcoma reported in sea otters.     

Influence of occupation history and habitat on Washington sea otter diet

Habitat characteristics are primary determinants of nearshore marine communities. However, biological drivers like predation can also be important for community composition. Sea otters (Enhydra lutris ssp.) are a salient example of a keystone species exerting top‐down control on ecosystem community structure. The translocation and subsequent population growth and range expansion of the northern sea otter (Enhydra lutris kenyoni) in Washington State over the last five decades has created a spatio‐temporal gradient in sea otter occupation time and density, and acts as a natural experiment to quantify how sea otter population status and habitat type influence sea otter diet. We collected focal observations of sea otters foraging at sites across the gradient in varying habitat types between 2010 and 2017. We quantified sea otter diet composition and diversity, and long‐term rates of energy gain across the gradient. We found that sea otter diet diversity was positively correlated with cumulative sea otter density, while rate of energy gain was negatively correlated with cumulative density. Additionally, we found that habitat type explained 1.77 times more variance in sea otter diet composition than sea otter cumulative density. Long‐term diet studies can provide a broader picture of sea otter population status in Washington State.