Recovery rates of bottlenose dolphin (Tursiops truncatus) carcasses estimated from stranding and survival rate data

Recovery of cetacean carcasses provides data on levels of human‐caused mortality, but represents only a minimum count of impacts. Counts of stranded carcasses are negatively biased by factors that include at‐sea scavenging, sinking, drift away from land, stranding in locations where detection is unlikely, and natural removal from beaches due to wave and tidal action prior to detection. We estimate the fraction of carcasses recovered for a population of coastal bottlenose dolphins (Tursiops truncatus), using abundance and survival rate data to estimate annual deaths in the population. Observed stranding numbers are compared to expected deaths to estimate the fraction of carcasses recovered. For the California coastal population of bottlenose dolphins, we estimate the fraction of carcasses recovered to be 0.25 (95% CI = 0.20–0.33). During a 12 yr period, 327 animals (95% CI = 253–413) were expected to have died and been available for recovery, but only 83 carcasses attributed to this population were documented. Given the coastal habits of California coastal bottlenose dolphins, it is likely that carcass recovery rates of this population greatly exceed recovery rates of more pelagic dolphin species in the region.     

POTENTIAL IMPACT OF OIL SPILLS ON CALIFORNIA SEA OTTERS: IMPLICATIONS OF THE EXXON VALDEZ SPILL IN ALASKA

Based on the survival of sea otters held at rehabilitation centers during the 1989 Exxon Valdez oil spill in Alaska, we built two models of otter mortality. One was based on the relationship between mortality and distance from spill origin, the other was based on the relationship between mortality and time from the spill origin. These models are simplistic and are meant as first steps in arriving at realistic risk estimates and in providing a conceptual framework for relating oil spills and sea otter mortality. Using the distance model, we simulated the impact of an Exxon Valdez event occurring at different locations along the California coast. A spill at the Monterey Peninsula had the greatest impact, exposing 90% of the California sea otter population to oil and killing at least 50% of the individuals. The time model was used to predict the mortality of otters exposed to oil of various ages and for various periods of time. It suggested that efforts to rehabilitate otters should be discontinued 20-30 d after a spill. The limitations of the data available from the Exxon Valdez spill emphasize the importance of being prepared to conduct appropriate research during the next oil spill in sea otter habitat.     

AGE- AND SEX-SPECIFIC MORTALITY AND POPULATION STRUCTURE IN SEA OTTERS

We used 742 beach-cast carcasses to characterize age- and sex-specific sea otter mortality during the winter of 1990-1991 at Bering Island, Russia. We also examined 363 carcasses recovered after the 1989 grounding of the T/V Exxon Valdez , to characterize age and sex composition in the living western Prince William Sound (WPWS) sea otter population. At Bering Island, mortality was male-biased (81%), and 75% were adults. The WPWS population was female-biased (59%) and most animals were subadult (79% of the males and 45% of the females). In the decade prior to 1990-1991 we found increasing sea otter densities (particularly among males), declining prey resources, and declining weights in adult male sea otters at Bering Island. Our findings suggest the increased mortality at Bering Island in 1990-1991 was a density-dependent population response. We propose male-maintained breeding territories and exclusion of juvenile females by adult females, providing a mechanism for maintaining densities in female areas below densities in male areas and for potentially moderating the effects of prey reductions on the female population. Increased adult male mortality at Bering Island in 1990-1991 likely modified the sex and age class structure there toward that observed in Prince William Sound.     

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.     

Temporal association between land-based runoff events and California sea otter (Enhydra lutris nereis) protozoal mortalities

Toxoplasma gondii and Sarcocystis neurona have caused significant morbidity and mortality in threatened Southern sea otters (Enhydra lutris nereis) along the central California coast. Because only terrestrial animals are known to serve as definitive hosts for T. gondii and S. neurona, infections in otters suggest a land to sea flow of these protozoan pathogens. To better characterize the role of overland runoff in delivery of terrestrially derived fecal pathogens to the near shore, we assessed the temporal association between indicators of runoff and the timing of sea otter deaths due to T. gondii and S. neurona. Sea otter stranding records 1998-2004, from Monterey and Estero bays were reviewed and cases identified for which T. gondii or S. neurona were determined to be a primary or contributing cause of death. Precipitation and stream flow data from both study sites were used as indicators of land-based runoff. Logistic regression was applied to determine if a temporal association could be detected between protozoal mortalities and runoff indicators that occur in the 2 mo preceding mortality events. A significant association was found between S. neurona otter deaths at Estero Bay and increased stream flow that occurred 30-60 days prior to mortality events. At this site, the cause of otter mortality following increased river flows was 12 times more likely to be S. neurona infection compared with nonprotozoal causes of death. There were no significant associations between the timing of T. gondii otter deaths and indicators of overland runoff. Our results indicate that the association between overland runoff and otter mortalities is affected by geography as well as parasite type, and highlight the complex mechanisms that influence transmission of terrestrially derived pathogens to marine wildlife. Policy and management practices that aim to mitigate discharges of contaminated overland runoff can aid conservation efforts by reducing pathogen pollution of coastal waters, which impacts the health of threatened marine wildlife and humans.     

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.     

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.     

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.     

Helminth parasites of the southern sea otter Enhydra lutris nereis in central California: abundance,distribution and pathology

From October 1997 to May 2001, the gastrointestinal tracts from 162 beach-cast southern sea otters Enhydra lutris nereis were examined for helminth parasites and associated lesions. Carcasses were collected opportunistically in central California between Pt. San Pedro and Pt. Arguello. The primary goals of this study were to examine spatial and temporal variability in mortality due to parasite infection, identify factors associated with increased risk of infection, and illustrate the process of intestinal perforation by Profilicollis spp. Two genera and 4 species of acanthocephalans (Profilicollis altmani, P. kenti, P. major, Corynosoma enhydri) were found in 46.3% (Profilicollis spp.) and 94.4% (C. enhydri) of the carcasses examined. Three species of Digenea (Microphallus pirum, M. nicolli, Plenosoma minimum) were found in 47% of carcasses, at times in massive numbers (> 3000 per cm2). This is the first report of the latter 2 species from the sea otter. Mortality resulting from infection by Profilicollis spp. occurred in 13.0% (n = 21) of sampled carcasses, either directly, due to perforation of the intestinal wall and peritonitis (9.9%, n = 16), or indirectly, due to inhibition of host nutrient uptake or depletion of host energy reserves to fight chronic infections (3.1%, n = 5). The most massive infections (< 8760 parasites), and all cases of intestinal perforation occurred in carcasses infected by P. altmani and/or P. kenti. Mortality due to infection by Profilicollis spp. occurred more frequently among juvenile and old-adult females (chi2 = 17.479, df = 9, p = 0.045) from sand and mixed habitats in Monterey and Santa Cruz in the north of the sea otter range (chi2 = 9.84, df = 4, p = 0.045). Spatial differences in sea otter mortality coincided with the relative distributions of Profilicollis altmani, P. kenti, and P. major, and may reflect differences in sea otter diet, or differences in intensity of infection in intermediate hosts. Mortality rate due to infection by Profilicollis spp. decreased between 1998 and 2001, though differences were not significant (chi2 = 3.983, df = 3, p = 0.40), and may vary on multi-year cycles due to environmental factors such as density of definitive hosts (e.g. the surf scoter Melanitta perspicillata), or El Ni?o. Corynosoma enhydri did not cause significant damage to the intestine of the host, even when present in great numbers.     

SEA OTTERS AND BENTHIC PREY COMMUNITIES IN WASHINGTON STATE

An August 1987 benthic survey of otter-free and otter-occupied areas along the outer coast of Washington State's Olympic Peninsula confirms that this area has been as profoundly influenced by sea otters as other rocky, nearshore communities studied in California, Canada, and Alaska. Prey density, size, and biomass were found to be negatively correlated with sea otter abundance, suggesting that the re-introduction of sea otters to this area in 1969–1970 has profoundly affected invertebrate prey abundance and distribution, particularly that of the red sea urchin, Strongylocentrotus franciscanus. Red urchin distribution appears to influence algal groups differently and in a manner consistent with current otter/urchin/kelp theory. Foliose red algal abundance was negatively related to urchin numbers and coralline crusts were positively correlated. Aerial photographs of Macrocystis integrifolia cover at Cape Alava suggest an increase since the introduction of sea otters. Given the present distribution of prey along the Olympic Peninsula coast, we conclude that as the sea otter population continues to grow, range expansion is more likely to occur to the north, which may also lead to possible conflicts with an increasing sea urchin fishery and Native American set net activity.     

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.     

SEX DETERMINATION OF THE CALIFORNIA SEA LION (ZALOPHUS CALIFORNIANUS CALIFORNIANUS) FROM CANINE TEETH

Size of canine teeth from California sea lion ( Zalophus californianus californianus ) carcasses is shown to be useful in determining the sex of animals which have missing genitalia or which are otherwise of unknown sex. A total of 267 canine teeth from carcasses of 68 males and 43 females were measured along five axes. Of root and crown measurements of upper and lower canines, males and females overlapped only in root thickness of upper canines. A multivariate ANOVA showed a significant difference in the size of canines between upper and lower canines, and between males and females. Stepwise discriminant analysis produced discriminant functions for upper and lower canines for determining sex of unknown-sexed California sea lions. A separate set of canine teeth from 39 male and 49 female California sea lions was correctly classified without prior knowledge of sex by visual inspection and by the two discriminant functions.     

SPERM WHALES IN THE GULF OF CALIFORNIA: RESIDENCY, MOVEMENTS, BEHAVIOR, AND THE POSSIBLE INFLUENCE OF VARIATION IN FOOD SUPPLY

Sperm whale movements, residency, population structure, and behavior were investigated in the Gulf of California in 1998 and 1999. Variations in sperm whale movement patterns and behavior were related to changes in prey abundance (jumbo squid, Dosidicus gigas ) determined by fishery statistics. Photo-identification data revealed that seven female sperm whales moved into the Gulf of California from the Galapagos Islands, traveling up to 3,803 km. These are among the longest documented movements for female sperm whales. There were significant differences in speed and distance traveled during a dive cycle between 1998 and 1999 (low and high squid abundance). In 1999 there were also significant differences in small-scale movements and behavior between the northern and the southern part of the study area (high and low prey abundance). These results suggest that when food resources are low, sperm whales travel in straighter lines, dive for longer periods, travel larger distances during dive cycles, and at higher speed. In 1999 there were significant differences in time spent socializing in areas of high prey abundance versus areas of low abundance. All of these changes in behavior were consistent with increased foraging effort when squid abundance was low. A high proportion of mature males and first-year calves were observed in the Gulf of California, suggesting that it is an important sperm whale breeding ground.     

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.     

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.     

Southern Sea Otter as a Sentinel of Marine Ecosystem Health

The southern sea otter (Enhydra lutris nereis) is listed as threatened under the Endangered Species Act (ESA) and is a keystone species, strongly influencing the abundance and diversity of the other species within its kelp forest ecosystem. This is accomplished primarily by preying upon urchins that eat the kelp stipe and holdfast, which can reduce a kelp forest to an urchin barren. Sea otters are very susceptible to marine pollutants such as petroleum, which may be directly toxic and/or alter their furs insulating properties. Sea otters are an excellent sentinel species. They eat approximately 25% of their body weight per day in shellfish and other invertebrates, and can concentrate and integrate chemical contaminants. In addition, they appear to be susceptible to a number of diseases and parasites that may have anthropogenic origins, and shellfish may serve as an intermediary for some of these infections. Many of the shellfish the otters eat are also harvested for human food. In their role as sentinels, sea otter health has implications for human health, economic sustainability of shellfisheries, as well as overall marine ecosystem health. The recent southern sea otter decline has been viewed with some alarm by conservationists and, indeed, recovery seems a long way off. High mortality rather than depressed recruitment appears to underlie the decline. A good deal of debate has centered on the role of infectious diseases and parasites, exposure to contaminants, nutrition and prey availability, net and pot fishery interactions, and other sources of mortality. Current research is being done related to major classes of mortality, various types of pollutants and some specific organisms causing southern sea otter mortality, and their implications for marine ecosystem health and sustainability.     

中国水獭保护现状及珠江口水獭种群重建探讨

顶级捕食者在生态系统中发挥着重要作用，受到研究者们的广泛关注。水獭作为很多淡水生态系统的顶级捕食者，在我国却长期处于被忽视的状态。我国分布有3种水獭--欧亚水獭、亚洲小爪水獭和江獭，曾经遍布我国中东部和东北地区，包括珠江口地区。但在20世纪，3种水獭均经历了大规模的种群下降，甚至区域性灭绝。在全球13种水獭中，已有3种（海獭、北美水獭和欧亚水獭）通过种群复壮和重引入实现了种群重建，这为其它水獭物种的种群重建提供了重要参考和建议。同国内其它地区类似，珠江口地区的水獭种群在20世纪后期大量减少，目前只在少数几个地点还有确切的欧亚水獭分布记录，亚洲小爪水獭和江獭已无近期记录。在珠江口重建水獭种群具有重要的生态意义和社会价值。本文对重建珠江口水獭种群的相关问题进行了分析。     

Dramatic increase in sea otter mortality from white sharks in California

Although southern sea otters (Enhydra lutris nereis) are not considered prey for white sharks (Carcharodon carcharias), sharks do nonetheless bite sea otters. We analyzed spatial and temporal trends in shark bites on sea otters in California, assessing the frequency of shark bite wounds in 1,870 carcasses collected since 1985. The proportion of stranded sea otters having shark bites has increased sharply since 2003, and white shark bites now account for >50% of recovered carcasses. The trend was most pronounced in the southern part of the range, from Estero Bay to Point Conception, where shark bite frequency has increased eightfold. Seasonal trends were also evident: most shark‐bitten carcasses are recovered in late summer and fall; however, the period of elevated shark bite frequency has lengthened. The causes of these trends are unclear, but possible contributing factors include increased white shark abundance and/or changes in white shark behavior and distribution. In particular, the spatiotemporal patterns of shark‐bitten sea otters match increases in pinniped populations, and the increased availability of marine mammal prey for white sharks may have led to more sharks spending more time in nearshore waters utilized by both sea otters and pinnipeds.     

Demographics and spatio‐temporal signature of the biotoxin domoic acid in California sea lion (Zalophus californianus) stranding records

California sea lions (Zalophus californianus) in otherwise good nutritional condition have been consistently affected by the marine biotoxin domoic acid since the late 1990s. In this study we evaluated the temporal and spatial stranding patterns of suspected and confirmed cases of domoic acid intoxicated sea lions from 1998 to 2006, using records of strandings along the California coast obtained from members of the California Marine Mammal Stranding Network. The majority of domoic acid cases were adult females (47%–82% of the total annual domoic acid cases), a contrast to strandings that were not related to domoic acid, which were generally dominated by juveniles and pups. Exposure to this biotoxin led to a 6.67‐fold increase in adult female strandings in 2000, and a 5.44‐fold increase in adult female deaths in 2006, relative to strandings and deaths of adult female not affected by domoic acid. Domoic acid cases have occurred annually since 1998 (except for 1999) between April and August, with clusters centered primarily at Pismo Beach (San Luis Obispo County), as well as at other beaches in San Luis Obispo, Monterey, Santa Cruz, Santa Barbara, Orange, and San Diego counties. The larger ecological and population level implications of increased domoic acid strandings and deaths, particularly among adult female sea lions, warrant further attention and need to be investigated.     

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.