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Michael J. Murray

Publications and source records attributed to Michael J. Murray.

15 recordsLinked to original sources

Fatal leptospirosis in southern sea otters from Central California: Pathologic findings and detection of Leptospira interrogans

Leptospira interrogans serovar Pomona infections cause periodic outbreaks in California sea lions (CSLs; Zalophus californianus ) and sporadic deaths in phocids. However, the frequency of infection and associated health impacts remain uncharacterized in sympatric threatened southern sea otters (SSOs; Enhydra lutris nereis ), which serve as important sentinels of coastal health. Given the broad impacts of L. interrogans on other marine mammals, our objective was to screen selected SSOs for infection, determine whether leptospirosis contributes to SSO mortality, and describe leptospiral-associated lesions. A retrospective review (2005–2025) identified 19 candidate cases that underwent detailed review, including Leptospira immunohistochemistry (IHC), serology, and polymerase chain reaction (PCR), with a special focus on renal and hepatic lesions. Kidney samples were PCR-positive for 74% (14/19) of suspected cases. For eight of these, DNA sequence-based serogroup typing detected L. interrogans serogroup Pomona. Seven of the 14 PCR-positive leptospirosis cases were classified as fatal based on positive renal IHC and moderate to severe tubulointerstitial nephritis. All fatal cases had anti- L. interrogans serovar Pomona antibody titers ≥1:25,600. The remaining seven PCR-positive cases were considered nonfatal leptospirosis due to minimal and/or unrelated renal lesions and negative IHC. Nonfatal Leptospira -infected cases ranged from seronegative to low positive (1:400) for serovar Pomona. Antibody titers for Leptospira PCR-negative cases were negative. In fatal cases, gross renal changes were often inapparent or characterized by miliary white cortical foci. Renal histologic lesions included tubulointerstitial nephritis, acute tubular necrosis, and suppurative tubulitis with intratubular bacteria, along with positive IHC staining for leptospiral antigen in the lesions. Gross hepatic changes were also inapparent in fatal cases, and histologic lesions were rare, characterized in one animal by hepatocellular dissociation and in two sea otters by limited leptospiral antigen detection by IHC. Most Leptospira -infected sea otters (71%, 10/14) stranded during higher rainfall months in California, suggesting possible land-to-sea transmission from terrestrial hosts. Given these findings, and because L. interrogans serovar Pomona infections have been confirmed in sympatric CSLs and terrestrial mammals from adjacent watersheds, a focused investigation of potential marine and terrestrial disease transmission dynamics could provide new information to reduce SSO mortalities.

California

Gene expression and wildlife health: Varied interpretations based on perspective

We evaluated wildlife population health from the perspective of statistical means vs. variances. We outlined the choices necessary to provide the framework for our study. These consisted of spatial and temporal boundaries (e.g., choice of sentinel species, populations, time frame), measurement techniques (molecular to population level), and appropriate statistical analyses. We chose to assess the health of 19 sea otter populations, located in the north Pacific from the Aleutian Islands, AK, to Santa Barbara, CA, and varying in population growth rates and length of occupancy. Our focal metric was gene expression (i.e., mRNA transcripts) data that we had previously generated across sea otter populations as a measure of population health. We used statistical methods with different approaches (i.e., means vs. variances) and examined the subsequent interpretive outcomes and how these influence our assessment of “health.” Interpretations based on analyses using variances versus means overlapped to some degree. In general, sea otter populations with low variation in gene expression were limited by food resources and at or near carrying capacity. In populations where the variation in gene expression was moderate or high, four out of five populations were increasing in abundance, or had been recently increasing. Where we had additional information on sources of stressors at the level of the population, we were able to draw inferences from those stressors to specific gene expression results. For example, gene expression patterns of sea otters from Western Prince William Sound were consistent with long term exposure to petroleum hydrocarbons, whereas in Kachemak Bay, patterns were consistent with exposure to algal toxins. Ultimately, determination of population or ecosystem health will be most informative when multiple metrics are examined across disciplines in the context of specific scenarios and goals.

Alaska, British Columbia, California, Oregon, Wash

Characterizing the oral and distal gut microbiota of the threatened southern sea otter (Enhydra lutris nereis) to enhance conservation practice

The southern sea otter ( Enhydra lutris nereis ) is a threatened sub-species in coastal ecosystems. To understand better the role of diet, monitor health, and enhance management of this and other marine mammal species, we characterized the oral (gingival) and distal gut (rectal and fecal) microbiota of 158 wild southern sea otters living off the coast of central California, USA, and 12 captive sea otters, some of which were included in a diet shift experiment. We found that the sea otter fecal microbiota was distinct from that of three other otter species, and that captivity does not significantly alter the community structure of the sea otter gingival or distal gut microbiota. Metagenomic analysis unexpectedly revealed that the majority of sea otter fecal DNA is derived from prey, rather than from indigenous bacteria or host cells as with most other mammals. We speculate that a reduced bacterial biomass in the sea otter gut reflects rapid gut transit time and a particular strategy for foraging and energy harvest. This study establishes a reference for the healthy sea otter microbiota, highlights how a marine lifestyle may shape the mammalian microbiota, and may inform future health assessments and conservation management of sea otter populations.

California

Sea otter population collapse in southwest Alaska: Assessing ecological covariates, consequences, and causal factors

Sea otter ( Enhydra lutris ) populations in southwest Alaska declined substantially between about 1990 and the most recent set of surveys in 2015. Here we report changes in the distribution and abundance of sea otters, and covarying patterns in reproduction, mortality, body size and condition, diet and foraging behavior, food availability, health profiles, and exposure to environmental contaminants over this 25-yr period. The population decline, which resulted in densities on the order of 5% of environmental carrying capacity, ranged from Attu Island in the west to about Castle Cape (on the south side of the Alaska Peninsula) in the east. Remaining sea otters moved closer to shore and into shallow, protected habitats. Reproductive rates appeared unchanged with the decline. Although the demographic cause of the decline was clearly elevated mortality, stranded carcasses were rare or absent. The net rate of energy gain by foraging sea otters, body length and condition, and prey biomass density, all increased after the decline and varied inversely with sea otter population density beyond the area of decline. Sea otters within the area of decline showed no increases in health anomalies, disease, contaminant exposure, or abnormal gene transcription patterns as compared to animals outside the area of decline. These collective findings are inconsistent with nutritional limitation, disease, or environmental contaminants, and consistent with predation (or possibly some other density-independent factor) as the reason for the sea otter population decline. Our approach and analyses provide a broad conceptual template for thinking about and assessing the causes of wildlife population declines.

Alaska

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.

North Pacific

Robust age estimation of southern sea otters from multiple morphometrics

Reliable age estimation is an essential tool to assess the status of wildlife populations and inform successful management. Aging methods, however, are often limited by too few data, skewed demographic representation, and by single or uncertain morphometric relationships. In this study, we synthesize age estimates in southern sea otters Enhydra lutris nereis from 761 individuals across 34 years of study, using multiple noninvasive techniques and capturing all life stages from 0 to 17 years of age. From wild, stranded, and captive individuals, we describe tooth eruptions, tooth wear, body length, nose scarring, and pelage coloration across ontogeny and fit sex‐based growth functions to the data. Dental eruption schedules provided reliable and identifiable metrics spanning 0.3–9 months. Tooth wear was the most reliable predictor of age of individuals aged 1–15 years, which when combined with total length, explained >93% of observed age. Beyond age estimation, dental attrition also indicated the maximum lifespan of adult teeth is 13‒17 years, corresponding with previous estimates of life expectancy. Von Bertalanffy growth function model simulations of length at age gave consistent estimates of asymptotic lengths (male L oo = 126.0‒126.8 cm, female L oo = 115.3‒115.7 cm), biologically realistic gestation periods ( t 0 = 115 days, SD = 10.2), and somatic growth (male k = 1.8, SD = 0.1; female k = 2.1, SD = 0.1). Though exploratory, we describe how field radiographic imaging of epiphyseal plate development or fusions may improve aging of immature sea otters. Together, our results highlight the value of integrating information from multiple and diverse datasets to help resolve conservation problems.

Ecology and Evolution

Emergence of a zoonotic pathogen in a coastal marine sentinel: Capillaria hepatica (syn. Calodium hepaticum)-associated hepatitis in southern sea otters (Enhydra lutris nereis)

Capillaria hepatica is a globally distributed zoonotic nematode parasite that most commonly infects feral and native rats. Soil contact, pica, and living in close proximity to rat populations are risk factors for human infection. Larval nematodes and eggs that were morphologically consistent with C. hepatica were observed microscopically in livers of stranded southern sea otters ( Enhydra lutris nereis ) from California. Large (90–100 × 45–55 μm), barrel-shaped non-embryonated parasite eggs with large polar prominences and a roughened or striated surface, or 105–120 μm diameter larval aphasmid nematode profiles with a prominent stichosome and hypodermal bands were observed in the livers of three otters. The liver of a fourth animal exhibited serpiginous tracts of necrosis, micro-cavitation and pleocellular inflammation, with intralesional linear eosinophilic material that resembled cuticle from degenerating metazoan parasites. Capillaria hepatica -associated hepatitis and capsular adhesions were the cause of death for one otter, and parasite-associated liver lesions were observed in all cases. All infected otters were adult females that stranded from 2006 through 2016 at multiple sites along the central California coast. All cases stranded from December through May; during and soon after peak seasonal precipitation and land-sea runoff in California. This same seasonal pattern has been reported for other land-based parasites infecting southern sea otters. Neither C. hepatica , nor any similar nematodes have been reported from marine mammals, and southern sea otters are not typical hosts for C. hepatica or any other nematode parasites. The most likely route of exposure was via freshwater runoff containing embryonated eggs liberated from predated or decomposing terrestrial hosts, especially rats. Similar to the land-based parasites Toxoplasma gondii and Sarcocystis neurona , C. hepatica eggs may be concentrated and transmitted through filter-feeding marine invertebrates that serve as southern sea otter prey, which may also pose an unrecognized public health risk for people who consume these species.

California

Spatial epidemiological patterns suggest mechanisms of land-sea transmission for Sarcocystis neurona in a coastal marine mammal

Sarcocystis neurona was recognised as an important cause of mortality in southern sea otters (Enhydra lutris nereis) after an outbreak in April 2004 and has since been detected in many marine mammal species in the Northeast Pacific Ocean. Risk of S. neurona exposure in sea otters is associated with consumption of clams and soft-sediment prey and is temporally associated with runoff events. We examined the spatial distribution of S. neurona exposure risk based on serum antibody testing and assessed risk factors for exposure in animals from California, Washington, British Columbia and Alaska. Significant spatial clustering of seropositive animals was observed in California and Washington, compared with British Columbia and Alaska. Adult males were at greatest risk for exposure to S. neurona, and there were strong associations with terrestrial features (wetlands, cropland, high human housing-unit density). In California, habitats containing soft sediment exhibited greater risk than hard substrate or kelp beds. Consuming a diet rich in clams was also associated with increased exposure risk. These findings suggest a transmission pathway analogous to that described for Toxoplasma gondii, with infectious stages traveling in freshwater runoff and being concentrated in particular locations by marine habitat features, ocean physical processes, and invertebrate bioconcentration.

California, Washington, British Columbia, Alaska

Surrogate rearing a keystone species to enhance population and ecosystem restoration

Translocation and rehabilitation programs are critical tools for wildlife conservation. These methods achieve greater impact when integrated in a combined strategy for enhancing population or ecosystem restoration. From 2002-2016, we reared 37 orphaned southern sea otter (Enhydra lutris nereis) pups, using captive sea otters as surrogate mothers, then released them into a degraded coastal estuary. As a keystone species, observed increases in the local sea otter population unsurprisingly brought many ecosystem benefits. The role that surrogate-reared otters played in this success story, however, remained uncertain. To resolve this question, we developed an individual-based model (IBM) of the local population using surveyed individual fates (survival and reproduction) of surrogate-reared and wild-captured otters, and modeled estimates of immigration. Estimates derived from a decade of population monitoring indicated that surrogate-reared and wild sea otters experienced similar reproductive and survival rates. This was true for males and females, across all ages (1-13 years) and locations evaluated. The IBM simulations indicated that reconstructed counts of the wild population are best explained by surrogate-reared otters combined with low levels of unassisted immigration. In addition, the model shows that 55% of observed population growth over this period is attributable to surrogate-reared otters and their wild progeny. Together, our results indicate that the integration of surrogacy methods and reintroduction of juvenile sea otters helped establish a biologically successful population and restore a once-impaired ecosystem.

California

Southern sea otter (Enhydra lutris nereis) population biology at Big Sur and Monterey, California --Investigating the consequences of resource abundance and anthropogenic stressors for sea otter recovery

The range of the southern sea otter ( Enhydra lutris nereis ) spans most of the central California coast from Half Moon Bay to Gaviota. Some coastal areas within this range are heavily developed and highly impacted by humans, while other areas are wild and largely pristine. Determining the relative importance of food resource abundance, environmental conditions, and anthropogenic increases in pathogens and pollutants to population change in sea otters is critical to understanding limitations to population growth. To investigate the causal links between the sluggish population growth of sea otters in central California and factors that could be driving variation in survival and reproduction, we designed a study to compare two distinct subpopulations—one in an area of low human impact (Big Sur) and one in an area of high human impact (Monterey). Between 2008 and 2011, the U.S. Geological Survey and collaborators conducted a telemetry-based study of sea otters at these two locations. The results of this study were not consistent with the hypothesis that sea otters adjacent to human population centers (Monterey) experience higher exposure to pollutants and pathogens than those in lower impacted areas (Big Sur). In fact, based on serological analysis, female sea otters from Big Sur showed higher exposure rates to Toxoplasma gondii than did female otters from Monterey, while domoic acid exposure appeared to be similar at both sites. Gene expression (specifically transcription) analysis did not indicate any consistent differences between the two populations that would have suggested a response to pathogen or toxin exposure, although there were temporal changes in gene transcription for sea otters at Big Sur following potential exposure to run-off from wildfires that occurred during the study. Together, these metrics suggest that variation in exposure to environmental stressors occurred, but patterns were not clearly attributable to differences in human population densities or land-use patterns. When compared to Monterey, sea otters in Big Sur spent more time feeding, had a higher degree of dietary specialization, were in poorer body condition, and had lower survival rates (both pups and adults). Together, these metrics suggest that otters at Big Sur had greater nutritional stress, consistent with lower per-capita resource abundance. Overall, study results indicate that density-dependent population regulation, mediated by per-capita resource abundance, is the most significant factor currently limiting population growth in the center part of the range. Additionally, spatial and temporal variation in environmental and anthropogenic stressors also can affect sea otter health, although patterns of variation are complex and are not simply a function of proximity to human populations. We also found that exposure to environmental stressors (either natural or anthropogenic in origin) often is associated with resource limitation. Finally, our results indicate that sea otter populations are structured at relatively small spatial scales, and the processes that regulate population abundance (including density-dependent resource abundance) also occur at these smaller, more local scales.

California

Defining the risk landscape in the context of pathogen pollution: Toxoplasma gondii in sea otters along the Pacific Rim

Pathogens entering the marine environment as pollutants exhibit a spatial signature driven by their transport mechanisms. The sea otter ( Enhydra lutris ), a marine animal which lives much of its life within sight of land, presents a unique opportunity to understand land–sea pathogen transmission. Using a dataset on Toxoplasma gondii prevalence across sea otter range from Alaska to California, we found that the dominant drivers of infection risk vary depending upon the spatial scale of analysis. At the population level, regions with high T. gondii prevalence had higher human population density and a greater proportion of human-dominated land uses, suggesting a strong role for population density of the felid definitive host of this parasite. This relationship persisted when a subset of data were analysed at the individual level: large-scale patterns in sea otter T. gondii infection prevalence were largely explained by individual exposure to areas of high human housing unit density, and other landscape features associated with anthropogenic land use, such as impervious surfaces and cropping land. These results contrast with the small-scale, within-region analysis, in which age, sex and prey choice accounted for most of the variation in infection risk, and terrestrial environmental features provided little variation to help in explaining observed patterns. These results underscore the importance of spatial scale in study design when quantifying both individual-level risk factors and landscape-scale variation in infection risk.

California

Gaps in kelp cover may threaten the recovery of California sea otters

Despite more than a century of federal protection, the California sea otter Enhydra lutris nereis remains threatened under the U.S. Endangered Species Act (ESA), and the population has not appreciably expanded its range in two decades. Here, we examine a novel dataset of 725 sea otter live strandings from 1984–2015 to gain insights into demographic and environmental factors underlying threats to sea otter recovery. Using multinomial logistic regression to evaluate spatiotemporal patterns of stranding causes, we demonstrate that increases in stranding rates, particularly outside the range center, are related to a substantial increase in shark bites. By contrast, trauma linked to human activities has declined dramatically, and now accounts for less than 5% of stranding cases. Within the range core, where the sea otter population seems regulated by prey availability, symptoms of energetic stress represent more than 63% of all strandings and are strongly associated with high sea otter density. Conversely, in range peripheries, the majority of strandings are caused by shark bite and neurological disease. Notably, these threats are virtually absent where nearshore habitat is characterized by at least 10% kelp canopy cover. Our analyses reveal that declining kelp cover may therefore constrain the population's spatial expansion and recovery in two key ways. Absence of kelp intensifies density‐independent threats in the range peripheries, and likely limits dispersal of reproductive females, which depend on kelp canopy for nursery habitat. These results highlight the significance of both top‐down and bottom‐up processes in population dynamics, and inform an ecosystem‐based approach to conservation planning.

California

Tagging and tracking

The number of stranding response facilities for marine mammals in the United States has increased over the past two decades, resulting in thousands of rehabilitated marine mammals released back into the wild (Geraci and Lounsbury 2005; Moore et al. 2007; Johnson and Mayer 2015; Simeone et al. 2015). All rehabilitated marine mammals released in the United States must be tagged or marked (50 CFR 216.27) and post-release monitoring is recommended, if not required, for some taxonomic groups. This depends on their release category as determined by a veterinarian in concordance with guidelines established by the National Marine Fisheries Service (NMFS) and the US Fish and Wildlife Service (USFWS; Whaley and Borkowski 2009). Monitoring the fate of released, rehabilitated marine mammals is not only necessary for the validation and refinement of veterinary procedures and treatments, but allows for the recovery of individuals that are unable to adapt to the wild (Whaley and Borkowski 2009). For cases in which rehabilitation is used to enhance small or endangered populations, monitoring the ability of individuals to forage, survive, and ultimately reproduce following release is essential for assessing the conservation value of a given program’s efforts. Post-release monitoring has also been useful in some cases for elucidating poorly understood ranges and habitat use of wild populations (Moore et al. 2007).

Book chapter

Effects of wildfire on sea otter (Enhydra lutris) gene transcript profiles

Wildfires have been shown to impact terrestrial species over a range of temporal scales. Little is known, however, about the more subtle toxicological effects of wildfires, particularly in downstream marine or downwind locations from the wildfire perimeter. These down-current effects may be just as substantial as those effects within the perimeter. We used gene transcription technology, a sensitive indicator of immunological perturbation, to study the effects of the 2008 Basin Complex Fire on the California coast on a sentinel marine species, the sea otter ( Enhydra lutris ). We captured sea otters in 2008 (3 mo after the Basin Complex Fire was controlled) and 2009 (15 mo after the Basin Complex Fire was controlled) in the adjacent nearshore environment near Big Sur, California. Gene responses were distinctly different between Big Sur temporal groups, signifying detoxification of PAHs, possible associated response to potential malignant transformation, and suppression of immune function as the primary responses of sea otters to fire in 2008 compared to those captured in 2009. In general, gene transcription patterns in the 2008 sea otters were indicative of molecular reactions to organic exposure, malignant transformation, and decreased ability to respond to pathogens that seemed to consistent with short-term hydrocarbon exposure.

California

Serologic evidence of influenza A(H1N1)pdm09 virus in northern sea otters

Sporadic epizootics of pneumonia among marine mammals have been associated with multiple animal-origin influenza A virus subtypes (1–6); seals are the only known nonhuman host for influenza B viruses (7). Recently, we reported serologic evidence of influenza A virus infection in free-ranging northern sea otters ( Enhydra lutris kenyoni ) captured off the coast of Washington, USA, in August 2011 (8). To investigate further which influenza A virus subtype infected these otters, we tested serum samples from these otters by ELISA for antibody-binding activity against 12 recombinant hemagglutinins (rHAs) from 7 influenza A hemagglutinin (HA) subtypes and 2 lineages of influenza B virus (Technical Appendix Table 1). Estimated ages for the otters were 2–19 years (Technical Appendix Table 2); we also tested archived serum samples from sea otters of similar ages collected from a study conducted during 2001–2002 along the Washington coast (9).

Washington