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1.  Using Molecular Epidemiology to Track Toxoplasma gondii from Terrestrial Carnivores to Marine Hosts: Implications for Public Health and Conservation 
Environmental transmission of the zoonotic parasite Toxoplasma gondii, which is shed only by felids, poses risks to human and animal health in temperate and tropical ecosystems. Atypical T. gondii genotypes have been linked to severe disease in people and the threatened population of California sea otters. To investigate land-to-sea parasite transmission, we screened 373 carnivores (feral domestic cats, mountain lions, bobcats, foxes, and coyotes) for T. gondii infection and examined the distribution of genotypes in 85 infected animals sampled near the sea otter range.
Methodology/Principal Findings
Nested PCR-RFLP analyses and direct DNA sequencing at six independent polymorphic genetic loci (B1, SAG1, SAG3, GRA6, L358, and Apico) were used to characterize T. gondii strains in infected animals. Strains consistent with Type X, a novel genotype previously identified in over 70% of infected sea otters and four terrestrial wild carnivores along the California coast, were detected in all sampled species, including domestic cats. However, odds of Type X infection were 14 times higher (95% CI: 1.3–148.6) for wild felids than feral domestic cats. Type X infection was also linked to undeveloped lands (OR = 22, 95% CI: 2.3–250.7). A spatial cluster of terrestrial Type II infection (P = 0.04) was identified in developed lands bordering an area of increased risk for sea otter Type II infection. Two spatial clusters of animals infected with strains consistent with Type X (P≤0.01) were detected in less developed landscapes.
Differences in T. gondii genotype prevalence among domestic and wild felids, as well as the spatial distribution of genotypes, suggest co-existing domestic and wild T. gondii transmission cycles that likely overlap at the interface of developed and undeveloped lands. Anthropogenic development driving contact between these cycles may increase atypical T. gondii genotypes in domestic cats and facilitate transmission of potentially more pathogenic genotypes to humans, domestic animals, and wildlife.
Author Summary
Toxoplasma gondii, a global parasite shed by domestic and wild felids, can cause severe disease in people and animals. In coastal California, USA, many sea otters have died due to T. gondii. Because T. gondii is shed by felids on land, otter infection suggests that this extremely hardy parasite is transported in freshwater runoff to aquatic environments, where animals and humans can become exposed. Molecular characterization of T. gondii strains infecting terrestrial and marine hosts can provide clues about parasite transmission cycles and sources of otter infection. By testing 373 and characterizing T. gondii infection in 85 terrestrial carnivores (domestic cats and wild carnivores) sharing the California coast, we found that Type X, the type previously identified in over 70% of infected sea otters tested, was more common in wild felids than domestic cats. However, discovery of Type X in domestic cats in this region suggests that they may play an important role in marine infection, as their populations are larger than those of wild felids. Differences in types of T. gondii among carnivores and in urban and agricultural vs. undeveloped areas suggest that there are separate, but overlapping domestic and wild cycles of T. gondii transmission in coastal California.
PMCID: PMC4038486  PMID: 24874796
2.  A New Pathogen Transmission Mechanism in the Ocean: The Case of Sea Otter Exposure to the Land-Parasite Toxoplasma gondii 
PLoS ONE  2013;8(12):e82477.
Toxoplasma gondii is a land-derived parasite that infects humans and marine mammals. Infections are a significant cause of mortality for endangered southern sea otters (Enhydra lutris nereis), but the transmission mechanism is poorly understood. Otter exposure to T. gondii has been linked to the consumption of marine turban snails in kelp (Macrocystis pyrifera) forests. It is unknown how turban snails acquire oocysts, as snails scrape food particles attached to surfaces, whereas T. gondii oocysts enter kelp beds as suspended particles via runoff. We hypothesized that waterborne T. gondii oocysts attach to kelp surfaces when encountering exopolymer substances (EPS) forming the sticky matrix of biofilms on kelp, and thus become available to snails. Results of a dietary composition analysis of field-collected snails and of kelp biofilm indicate that snails graze the dense kelp-biofilm assemblage composed of pennate diatoms and bacteria inserted within the EPS gel-like matrix. To test whether oocysts attach to kelp blades via EPS, we designed a laboratory experiment simulating the kelp forest canopy in tanks spiked with T. gondii surrogate microspheres and controlled for EPS and transparent exopolymer particles (TEP - the particulate form of EPS). On average, 19% and 31% of surrogates were detected attached to kelp surfaces covered with EPS in unfiltered and filtered seawater treatments, respectively. The presence of TEP in the seawater did not increase surrogate attachment. These findings support a novel transport mechanism of T. gondii oocysts: as oocysts enter the kelp forest canopy, a portion adheres to the sticky kelp biofilms. Snails grazing this biofilm encounter oocysts as ‘bycatch’ and thereby deliver the parasite to sea otters that prey upon snails. This novel mechanism can have health implications beyond T. gondii and otters, as a similar route of pathogen transmission may be implicated with other waterborne pathogens to marine wildlife and humans consuming biofilm-feeding invertebrates.
PMCID: PMC3867372  PMID: 24386100
3.  Evidence for a Novel Marine Harmful Algal Bloom: Cyanotoxin (Microcystin) Transfer from Land to Sea Otters 
PLoS ONE  2010;5(9):e12576.
“Super-blooms” of cyanobacteria that produce potent and environmentally persistent biotoxins (microcystins) are an emerging global health issue in freshwater habitats. Monitoring of the marine environment for secondary impacts has been minimal, although microcystin-contaminated freshwater is known to be entering marine ecosystems. Here we confirm deaths of marine mammals from microcystin intoxication and provide evidence implicating land-sea flow with trophic transfer through marine invertebrates as the most likely route of exposure. This hypothesis was evaluated through environmental detection of potential freshwater and marine microcystin sources, sea otter necropsy with biochemical analysis of tissues and evaluation of bioaccumulation of freshwater microcystins by marine invertebrates. Ocean discharge of freshwater microcystins was confirmed for three nutrient-impaired rivers flowing into the Monterey Bay National Marine Sanctuary, and microcystin concentrations up to 2,900 ppm (2.9 million ppb) were detected in a freshwater lake and downstream tributaries to within 1 km of the ocean. Deaths of 21 southern sea otters, a federally listed threatened species, were linked to microcystin intoxication. Finally, farmed and free-living marine clams, mussels and oysters of species that are often consumed by sea otters and humans exhibited significant biomagnification (to 107 times ambient water levels) and slow depuration of freshwater cyanotoxins, suggesting a potentially serious environmental and public health threat that extends from the lowest trophic levels of nutrient-impaired freshwater habitat to apex marine predators. Microcystin-poisoned sea otters were commonly recovered near river mouths and harbors and contaminated marine bivalves were implicated as the most likely source of this potent hepatotoxin for wild otters. This is the first report of deaths of marine mammals due to cyanotoxins and confirms the existence of a novel class of marine “harmful algal bloom” in the Pacific coastal environment; that of hepatotoxic shellfish poisoning (HSP), suggesting that animals and humans are at risk from microcystin poisoning when consuming shellfish harvested at the land-sea interface.
PMCID: PMC2936937  PMID: 20844747
4.  Effect of Estuarine Wetland Degradation on Transport of Toxoplasma gondii Surrogates from Land to Sea▿ †  
Applied and Environmental Microbiology  2010;76(20):6821-6828.
The flux of terrestrially derived pathogens to coastal waters presents a significant health risk to marine wildlife, as well as to humans who utilize the nearshore for recreation and seafood harvest. Anthropogenic changes in natural habitats may result in increased transmission of zoonotic pathogens to coastal waters. The objective of our work was to evaluate how human-caused alterations of coastal landscapes in California affect the transport of Toxoplasma gondii to estuarine waters. Toxoplasma gondii is a protozoan parasite that is excreted in the feces of infected felids and is thought to reach coastal waters in contaminated runoff. This zoonotic pathogen causes waterborne toxoplasmosis in humans and is a significant cause of death in threatened California sea otters. Surrogate particles that mimic the behavior of T. gondii oocysts in water were released in transport studies to evaluate if the loss of estuarine wetlands is contributing to an increased flux of oocysts into coastal waters. Compared to vegetated sites, more surrogates were recovered from unvegetated mudflat habitats, which represent degraded wetlands. Specifically, in Elkhorn Slough, where a large proportion of otters are infected with T. gondii, erosion of 36% of vegetated wetlands to mudflats may increase the flux of oocysts by more than 2 orders of magnitude. Total degradation of wetlands may result in increased Toxoplasma transport of 6 orders of magnitude or more. Destruction of wetland habitats along central coastal California may thus facilitate pathogen pollution in coastal waters with detrimental health impacts to wildlife and humans.
PMCID: PMC2953021  PMID: 20802072
5.  A Quantitative Ecological Risk Assessment of the Toxicological Risks from Exxon Valdez Subsurface Oil Residues to Sea Otters at Northern Knight Island, Prince William Sound, Alaska 
A comprehensive, quantitative risk assessment is presented of the toxicological risks from buried Exxon Valdez subsurface oil residues (SSOR) to a subpopulation of sea otters (Enhydra lutris) at Northern Knight Island (NKI) in Prince William Sound, Alaska, as it has been asserted that this subpopulation of sea otters may be experiencing adverse effects from the SSOR. The central questions in this study are: could the risk to NKI sea otters from exposure to polycyclic aromatic hydrocarbons (PAHs) in SSOR, as characterized in 2001–2003, result in individual health effects, and, if so, could that exposure cause subpopulation-level effects? We follow the U.S. Environmental Protection Agency (USEPA) risk paradigm by: (a) identifying potential routes of exposure to PAHs from SSOR; (b) developing a quantitative simulation model of exposures using the best available scientific information; (c) developing scenarios based on calculated probabilities of sea otter exposures to SSOR; (d) simulating exposures for 500,000 modeled sea otters and extracting the 99.9% quantile most highly exposed individuals; and (e) comparing projected exposures to chronic toxicity reference values. Results indicate that, even under conservative assumptions in the model, maximum-exposed sea otters would not receive a dose of PAHs sufficient to cause any health effects; consequently, no plausible toxicological risk exists from SSOR to the sea otter subpopulation at NKI.
PMCID: PMC2938330  PMID: 20862194
ecological risk assessment; sea otter; Enhydra lutris; Exxon Valdez oil spill; subsurface oil residues; stochastic simulation modeling; conceptual exposure modeling; polycyclic aromatic hydrocarbons
6.  Genetic Diversity and Population Parameters of Sea Otters, Enhydra lutris, before Fur Trade Extirpation from 1741–1911 
PLoS ONE  2012;7(3):e32205.
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.
PMCID: PMC3293891  PMID: 22403635
7.  Assessing Risks to Sea Otters and the Exxon Valdez Oil Spill: New Scenarios, Attributable Risk, and Recovery 
The Exxon Valdez oil spill occurred more than two decades ago, and the Prince William Sound ecosystem has essentially recovered. Nevertheless, discussion continues on whether or not localized effects persist on sea otters (Enhydra lutris) at northern Knight Island (NKI) and, if so, what are the associated attributable risks. A recent study estimated new rates of sea otter encounters with subsurface oil residues (SSOR) from the oil spill. We previously demonstrated that a potential pathway existed for exposures to polycyclic aromatic hydrocarbons (PAHs) and conducted a quantitative ecological risk assessment using an individual-based model that simulated this and other plausible exposure pathways. Here we quantitatively update the potential for this exposure pathway to constitute an ongoing risk to sea otters using the new estimates of SSOR encounters. Our conservative model predicted that the assimilated doses of PAHs to the 1-in-1000th most-exposed sea otters would remain 1–2 orders of magnitude below the chronic effects thresholds. We re-examine the baseline estimates, post-spill surveys, recovery status, and attributable risks for this subpopulation. We conclude that the new estimated frequencies of encountering SSOR do not constitute a plausible risk for sea otters at NKI and these sea otters have fully recovered from the oil spill.
PMCID: PMC3935186  PMID: 24587690
sea otter; Exxon Valdez oil spill; ecological risk assessment; Enhydra lutris; individual-based models; ecological recovery; attributable risk
8.  Limited genetic diversity among Sarcocystis neurona strains infecting southern sea otters precludes distinction between marine and terrestrial isolates 
Veterinary parasitology  2009;169(1-2):37-44.
Sarcocystis neurona is an apicomplexan parasite identified as a cause of fatal neurological disease in the threatened southern sea otter (Enhydra lutris nereis). In an effort to characterize virulent S. neurona strains circulating in the marine ecosystem, this study developed a range of markers relevant for molecular genotyping. Highly conserved sequences within the 18S ribosomal gene array, the plastid-encoded RNA polymerase (RPOb) and the cytochrome c oxidase subunit 1 mitochondrial gene (CO1) were assessed for their ability to distinguish isolates at the genus and species level. For within-species comparisons, five surface antigens (SnSAG1-SnSAG5) and one high resolution microsatellite marker (Sn9) were developed as genotyping markers to evaluate intra-strain diversity. Molecular analysis at multiple loci revealed insufficient genetic diversity to distinguish terrestrial isolates from strains infecting marine mammals. Furthermore, SnSAG specific primers applied against DNA from the closely related species, Sarcocystis falcatula, lead to the discovery of highly similar orthologs to SnSAG2, 3, and 4, calling into question the specificity of diagnostic tests based on these antigens. The results of this study suggest a population genetic structure for S. neurona similar to that reported for the related parasite, Toxoplasma gondii, dominated by a limited number of successful genotypes.
PMCID: PMC2858970  PMID: 20071081
Sarcocystis neurona; sea otter (Enhydra lutris); SnSAG; genotyping; population genetics
9.  Interactions of marine mammals and birds with offshore membrane enclosures for growing algae (OMEGA) 
Aquatic Biosystems  2014;10:3.
OMEGA is an integrated aquatic system to produce biofuels, treat and recycle wastewater, capture CO2, and expand aquaculture production. This system includes floating photobioreactors (PBRs) that will cover hundreds of hectares in marine bays. To assess the interactions of marine mammals and birds with PBRs, 9 × 1.3 m flat panel and 9.5 × 0.2 m tubular PBRs were deployed in a harbor and monitored day and night from October 10, 2011 to Janurary 22, 2012 using infrared video. To observe interactions with pinnipeds, two trained sea lions (Zalophus californianus) and one trained harbor seal (Phoca vitulina richardii) were observed and directed to interact with PBRs in tanks. To determine the forces required to puncture PBR plastic and the effects of weathering, Instron measurements were made with a sea otter (Enhydra lutris) tooth and bird beaks.
A total of 1,445 interactions of marine mammals and birds with PBRs were observed in the 2,424 hours of video recorded. The 95 marine mammal interactions, 94 by sea otters and one by a sea lion had average durations of three minutes (max 44 min) and represented about 1% of total recording time. The 1,350 bird interactions, primarily coots (Fulica americana) and gulls (Larus occidentalis and L. californicus) had average durations of six minutes (max. 170) and represented 5% of recording time. Interactive behaviors were characterized as passive (feeding, walking, resting, grooming, and social activity) or proactive (biting, pecking, investigating, and unspecified manipulating). Mammal interactions were predominantly proactive, whereas birds were passive. All interactions occurred primarily during the day. Ninety-six percent of otter interactions occurred in winter, whereas 73% of bird interactions in fall, correlating to their abundance in the harbor. Trained pinnipeds followed most commands to bite, drag, and haul-out onto PBRs, made no overt undirected interactions with the PBRs, but showed avoidance behavior to PBR tethers. Instron measurements indicated that sea-otter teeth and gull beaks can penetrate weathered plastic more easily than new plastic.
Otter and bird interactions with experimental PBRs were benign. Large-scale OMEGA systems are predicted to have both positive and negative environmental consequences.
PMCID: PMC4049508  PMID: 24955238
Biofuels; Wastewater treatment; Photobioreactors; Renewable energy; Marine mammals; Birds; Sea otter; Gulls; Monterey Bay
10.  Sea Otters Homogenize Mussel Beds and Reduce Habitat Provisioning in a Rocky Intertidal Ecosystem 
PLoS ONE  2013;8(5):e65435.
Sea otters (Enhydra lutris) are keystone predators that consume a variety of benthic invertebrates, including the intertidal mussel, Mytilus californianus. By virtue of their competitive dominance, large size, and longevity, M. californianus are ecosystem engineers that form structurally complex beds that provide habitat for diverse invertebrate communities. We investigated whether otters affect mussel bed characteristics (i.e. mussel length distributions, mussel bed depth, and biomass) and associated community structure (i.e. biomass, alpha and beta diversity) by comparing four regions that varied in their histories of sea otter occupancy on the west coast of British Columbia and northern Washington. Mussel bed depth and average mussel lengths were 1.5 times lower in regions occupied by otters for >20 years than those occupied for <5 yrs. Diversity of mussel bed associated communities did not differ between regions; however, the total biomass of species associated with mussel beds was more than three-times higher where sea otters were absent. We examined alternative explanations for differences in mussel bed community structure, including among-region variation in oceanographic conditions and abundance of the predatory sea star Pisaster ochraceus. We cannot discount multiple drivers shaping mussel beds, but our findings indicate the sea otters are an important one. We conclude that, similar to their effects on subtidal benthic invertebrates, sea otters reduce the size distributions of intertidal mussels and, thereby, habitat available to support associated communities. Our study indicates that by reducing populations of habitat-providing intertidal mussels, sea otters may have substantial indirect effects on associated communities.
PMCID: PMC3663835  PMID: 23717697
11.  Innervation patterns of sea otter (Enhydra lutris) mystacial follicle-sinus complexes 
Sea otters (Enhydra lutris) are the most recent group of mammals to return to the sea, and may exemplify divergent somatosensory tactile systems among mammals. Therefore, we quantified the mystacial vibrissal array of sea otters and histologically processed follicle-sinus complexes (F - SCs) to test the hypotheses that the number of myelinated axons per F - SC is greater than that found for terrestrial mammalian vibrissae and that their organization and microstructure converge with those of pinniped vibrissae. A mean of 120.5 vibrissae were arranged rostrally on a broad, blunt muzzle in 7–8 rows and 9–13 columns. The F-SCs of sea otters are tripartite in their organization and similar in microstructure to pinnipeds rather than terrestrial species. Each F-SC was innervated by a mean 1339 ± 408.3 axons. Innervation to the entire mystacial vibrissal array was estimated at 161,313 axons. Our data support the hypothesis that the disproportionate expansion of the coronal gyrus in somatosensory cortex of sea otters is related to the high innervation investment of the mystacial vibrissal array, and that quantifying innervation investment is a good proxy for tactile sensitivity. We predict that the tactile performance of sea otter mystacial vibrissae is comparable to that of harbor seals, sea lions and walruses.
PMCID: PMC4212681  PMID: 25400554
somatosensory system; peripheral nervous system; axon investment; vibrissae; F-SCs; comparative neurobiology; marine mammals; otters
12.  Aquatic polymers can drive pathogen transmission in coastal ecosystems 
Gelatinous polymers including extracellular polymeric substances (EPSs) are fundamental to biophysical processes in aquatic habitats, including mediating aggregation processes and functioning as the matrix of biofilms. Yet insight into the impact of these sticky molecules on the environmental transmission of pathogens in the ocean is limited. We used the zoonotic parasite Toxoplasma gondii as a model to evaluate polymer-mediated mechanisms that promote transmission of terrestrially derived pathogens to marine fauna and humans. We show that transparent exopolymer particles, a particulate form of EPS, enhance T. gondii association with marine aggregates, material consumed by organisms otherwise unable to access micrometre-sized particles. Adhesion to EPS biofilms on macroalgae also captures T. gondii from the water, enabling uptake of pathogens by invertebrates that feed on kelp surfaces. We demonstrate the acquisition, concentration and retention of T. gondii by kelp-grazing snails, which can transmit T. gondii to threatened California sea otters. Results highlight novel mechanisms whereby aquatic polymers facilitate incorporation of pathogens into food webs via association with particle aggregates and biofilms. Identifying the critical role of invisible polymers in transmission of pathogens in the ocean represents a fundamental advance in understanding and mitigating the health impacts of coastal habitat pollution with contaminated runoff.
PMCID: PMC4213613  PMID: 25297861
extracellular polymeric substances; transparent exopolymer particles; Toxoplasma gondii; zoonotic pathogen; marine transmission; sea otter
13.  Ultrastructural and molecular confirmation of the development of Sarcocystis neurona tissue cysts in the central nervous system of southern sea otters (Enhydra lutris nereis) 
International journal for parasitology  2009;39(12):1363-1372.
In 2004, three wild sea otters were diagnosed with putative Sarcocystis neurona-associated meningoencephalitis by histopathology and immunohistochemistry. Schizonts, free merozoites and tissue cysts were observed in the brains of all three infected animals. Tissue cysts from sea otter 1 (SO1) stained positively using anti-S. neurona polyclonal antiserum. However, positive staining does not preclude infection by closely related or cross-reactive tissue cyst-forming coccidian parasites. Two immature tissue cysts in the brain of SO1 were examined using transmission electron microscopy. Ultrastructural features included cyst walls with thin villous projections up to 1 μm long with tapered ends and a distinctive, electron-dense outer lining layer composed of linearly-arranged, semi-circular structures with a “hobnailed” surface contour. Small numbers of microtubules extended down through the villi into the underlying granular layer. Metrocytes were short and plump with an anterior apical complex, 22 subpellicular microtubules, numerous free ribosomes and no rhoptries. Some metrocytes appeared to be dividing, with two adjacent nuclear profiles. Collectively these ultrastructural features were compatible with developing protozoal cysts and were similar to prior descriptions of S. neurona tissue cysts. Panspecific 18S rDNA primers were utilized to identify protozoa infecting the brains of these otters and DNA amplification and additional sequencing at the ITS1 locus confirmed that all three otters were infected with S. neurona. No other Sarcocystis spp. were detected in the brains or skeletal muscles of these animals by immunohistochemistry or PCR. We believe this is the first ultrastructural and molecular confirmation of the development of S. neurona tissue cysts in the CNS of any animal.
PMCID: PMC2746246  PMID: 19527725
Sea otter; Sarcocystis neurona; Tissue cyst; Central nervous system; Brain; Ultrastructure; 18S; rDNA; ITS1
14.  Abiotic and Biotic Factors Associated with Tick Population Dynamics on a Mammalian Host: Ixodes hexagonus Infesting Otters, Lutra lutra 
PLoS ONE  2012;7(10):e47131.
The Eurasian otter, Lutra lutra, hosts several parasites with zoonotic potential. As this semiaquatic mammal has large ranges across terrestrial, freshwater and marine habitats, it has the capacity for wide dispersion of pathogens. Despite this, parasites of otters have received relatively little attention. Here, we examine their ectoparasite load and assess whether this is influenced by abiotic or biotic variables. Climatic phenomena such as the North Atlantic Oscillation (NAO) affect weather conditions in northern Europe. Consequently parasite distributions, particularly species with life stages exposed to the external environment, can be affected. We assessed the extent to which inter-annual variations in large-scale weather patterns (specifically the NAO and Central England (CE) temperatures) and host characteristics influenced tick prevalence and intensity. Ectoparasites consisted of a single species, the nidiculous tick Ixodes hexagonus (prevalence  = 24.3%; mean intensity  = 7.2; range  = 1–122; on n  = 820 otter hosts). The prevalence, but not intensity of infestation, was associated with high CE temperatures, while both prevalence and intensity were associated with positive phases of the NAO. Such associations indicate that I. hexagonus are most abundant when weather conditions are warmer and wetter. Ticks were more prevalent on juvenile than sub-adult or adult otters, which probably reflects the length of time the hosts spend in the holt where these ticks quest. High tick number was associated with poor host condition, so either poor condition hosts are more susceptible to ticks, or tick infestations negatively impact on host condition. Otters are clearly an important and common host for I. hexagonus, which has implications for vector-borne diseases. This work is the first to consider the impacts of long-term weather patterns on I. hexagonus and uses wild-animal cadavers to illustrate the importance of abiotic and biotic pressures impacting parasitic populations.
PMCID: PMC3465257  PMID: 23071736
15.  Causes and consequences of marine mammal population declines in southwest Alaska: a food-web perspective 
Populations of sea otters, seals and sea lions have collapsed across much of southwest Alaska over the past several decades. The sea otter decline set off a trophic cascade in which the coastal marine ecosystem underwent a phase shift from kelp forests to deforested sea urchin barrens. This interaction in turn affected the distribution, abundance and productivity of numerous other species. Ecological consequences of the pinniped declines are largely unknown. Increased predation by transient (marine mammal-eating) killer whales probably caused the sea otter declines and may have caused the pinniped declines as well. Springer et al. proposed that killer whales, which purportedly fed extensively on great whales, expanded their diets to include a higher percentage of sea otters and pinnipeds following a sharp reduction in great whale numbers from post World War II industrial whaling. Critics of this hypothesis claim that great whales are not now and probably never were an important nutritional resource for killer whales. We used demographic/energetic analyses to evaluate whether or not a predator–prey system involving killer whales and the smaller marine mammals would be sustainable without some nutritional contribution from the great whales. Our results indicate that while such a system is possible, it could only exist under a narrow range of extreme conditions and is therefore highly unlikely.
PMCID: PMC2685424  PMID: 19451116
killer whale; sea otter; pinniped; Bering Sea/North Pacific; trophic cascade; indirect effects
16.  Self-Mating in the Definitive Host Potentiates Clonal Outbreaks of the Apicomplexan Parasites Sarcocystis neurona and Toxoplasma gondii 
PLoS Genetics  2010;6(12):e1001261.
Tissue-encysting coccidia, including Toxoplasma gondii and Sarcocystis neurona, are heterogamous parasites with sexual and asexual life stages in definitive and intermediate hosts, respectively. During its sexual life stage, T. gondii reproduces either by genetic out-crossing or via clonal amplification of a single strain through self-mating. Out-crossing has been experimentally verified as a potent mechanism capable of producing offspring possessing a range of adaptive and virulence potentials. In contrast, selfing and other life history traits, such as asexual expansion of tissue-cysts by oral transmission among intermediate hosts, have been proposed to explain the genetic basis for the clonal population structure of T. gondii. In this study, we investigated the contributing roles self-mating and sexual recombination play in nature to maintain clonal population structures and produce or expand parasite clones capable of causing disease epidemics for two tissue encysting parasites. We applied high-resolution genotyping against strains isolated from a T. gondii waterborne outbreak that caused symptomatic disease in 155 immune-competent people in Brazil and a S. neurona outbreak that resulted in a mass mortality event in Southern sea otters. In both cases, a single, genetically distinct clone was found infecting outbreak-exposed individuals. Furthermore, the T. gondii outbreak clone was one of several apparently recombinant progeny recovered from the local environment. Since oocysts or sporocysts were the infectious form implicated in each outbreak, the expansion of the epidemic clone can be explained by self-mating. The results also show that out-crossing preceded selfing to produce the virulent T. gondii clone. For the tissue encysting coccidia, self-mating exists as a key adaptation potentiating the epidemic expansion and transmission of newly emerged parasite clones that can profoundly shape parasite population genetic structures or cause devastating disease outbreaks.
Author Summary
The parasites Toxoplasma gondii and Sarcocystis neurona have lifecycles that include a sexual stage in a definitive host and an asexual stage in intermediate hosts. For T. gondii, laboratory studies have demonstrated that the sexual stage can serve the dual purpose of producing new, virulent genotypes through recombination and promoting expansion of single clones via self-mating. Self-mating and other life history traits of T. gondii, including transmission of asexual stages among intermediate hosts, are assumed to account for the clonal population genetic structure of this organism. However, the relative contributions of sexual recombination and self-mating verses other life history traits in causing disease outbreaks or in shaping Toxoplasma's population genetic structure have not been verified in nature, nor have these traits been extensively examined in related parasites. To address this knowledge gap, we conducted population genetic analyses on T. gondii and S. neurona strains isolated from naturally occurring outbreaks affecting humans and sea otters, respectively. Our results identify self-mating as a key trait potentiating disease outbreaks through the rapid amplification of a single clone into millions of infectious units. Selfing is likely a key adaptation for enhancing transmission of recently emerged, recombinant clones and reshaping population genetic structures among the tissue-cyst coccidia.
PMCID: PMC3009688  PMID: 21203443
17.  Seroprevalence of Toxoplasma gondii in the Eurasian otter (Lutra lutra) in England and Wales 
Parasites & Vectors  2013;6:75.
Toxoplasma gondii is found on all continents and can infect all endothermic vertebrates. Toxoplasmosis is a globally important zoonosis with potentially devastating health impacts both for humans and a range of domestic and wild species. The World Health Organisation have repeatedly recommended the collection of accurate epidemiological data for T. gondii, yet despite recognised links between infection of wildlife, domestic animals and humans, seroprevalence in wild species is rarely monitored. Here, serological investigation using the Gold Standard Sabin-Feldman Dye Test was used to test for T. gondii in Eurasian otters (Lutra lutra) found dead, mainly as road-kill, in England and Wales. This is the first spatially widespread study of T. gondii in UK wildlife, and the first extensive survey of T. gondii in Eurasian otters, a sentinel species of fresh waters.
Infection was both common (39.5% prevalence, n = 271) and widespread, with significantly more infection in the east than the west of the UK. There was an increase in seroprevalence with age, but no sex bias.
The relatively high prevalence of T. gondii in a predominantly piscivorous freshwater mammal suggests widespread faecal contamination of freshwater ecosystems with oocysts. Continued surveillance of the Eurasian otter for T. gondii is valuable because of conservation concerns due to the otter’s ‘near threatened’ status on the IUCN Red List and because of the host’s role as a sentinel for freshwater health.
PMCID: PMC3622576  PMID: 23510234
Wildlife disease; Spatial distribution; Sabin Feldman; Surveillance; Zoonosis
18.  Quantifying Population-Level Risks Using an Individual-Based Model: Sea Otters, Harlequin Ducks, and the Exxon Valdez Oil Spill 
Ecological risk assessments need to advance beyond evaluating risks to individuals that are largely based on toxicity studies conducted on a few species under laboratory conditions, to assessing population-level risks to the environment, including considerations of variability and uncertainty. Two individual-based models (IBMs), recently developed to assess current risks to sea otters and seaducks in Prince William Sound more than 2 decades after the Exxon Valdez oil spill (EVOS), are used to explore population-level risks. In each case, the models had previously shown that there were essentially no remaining risks to individuals from polycyclic aromatic hydrocarbons (PAHs) derived from the EVOS. New sensitivity analyses are reported here in which hypothetical environmental exposures to PAHs were heuristically increased until assimilated doses reached toxicity reference values (TRVs) derived at the no-observed-adverse-effects and lowest-observed-adverse-effects levels (NOAEL and LOAEL, respectively). For the sea otters, this was accomplished by artificially increasing the number of sea otter pits that would intersect remaining patches of subsurface oil residues by orders of magnitude over actual estimated rates. Similarly, in the seaduck assessment, the PAH concentrations in the constituents of diet, sediments, and seawater were increased in proportion to their relative contributions to the assimilated doses by orders of magnitude over measured environmental concentrations, to reach the NOAEL and LOAEL thresholds. The stochastic IBMs simulated millions of individuals. From these outputs, frequency distributions were derived of assimilated doses for populations of 500 000 sea otters or seaducks in each of 7 or 8 classes, respectively. Doses to several selected quantiles were analyzed, ranging from the 1-in-1000th most-exposed individuals (99.9% quantile) to the median-exposed individuals (50% quantile). The resulting families of quantile curves provide the basis for characterizing the environmental thresholds below which no population-level effects could be detected and above which population-level effects would be expected to become manifest. This approach provides risk managers an enhanced understanding of the risks to populations under various conditions and assumptions, whether under hypothetically increased exposure regimes, as demonstrated here, or in situations in which actual exposures are near toxic effects levels. This study shows that individual-based models are especially amenable and appropriate for conducting population-level risk assessments, and that they can readily be used to answer questions about the risks to individuals and populations across a variety of exposure conditions. Integr Environ Assess Manag 2012; 8: 503–522. © 2012 SETAC
PMCID: PMC3465794  PMID: 22275071
Ecological risk assessment; Population-level risks; Individual-based models; Exxon Valdez oil spill; Sea otters Seaducks
19.  Risk Factors for Infection with Pathogenic and Antimicrobial-Resistant Fecal Bacteria in Northern Elephant Seals in California 
Public Health Reports  2008;123(3):360-370.
The goal of this study was to identify potential environmental and demographic factors associated with Campylobacter jejuni (C. jejuni), Salmonella enterica (Salmonella spp.), and antimicrobial-resistant Escherichia coli (E. coli) infection in northern elephant seals stranded along the California coastline.
E. coli, Salmonella spp., and C. jejuni were isolated from rectal swabs from 196 juvenile northern elephant seals, which were found stranded and alive along the California coast and brought to The Marine Mammal Center in Sausalito, California, for rehabilitation. Gender, weight, county where the animal stranded, month stranded, coastal human population density, exposure to sewage outfall or freshwater outflow (river or stream), and cumulative precipitation in the previous 24 hours, seven days, 30 days, 90 days, and 180 days were analyzed as potential risk factors for infection.
The odds of C. jejuni and antimicrobial-resistant E. coli were higher in feces of seals stranded at sites with higher levels of freshwater outflow compared with lower levels of freshwater outflow. The odds of Salmonella spp. in feces were 5.4 times greater in seals stranded in locations with lower levels of 30-day cumulative precipitation, along with substantially lower odds of Salmonella shedding for seals stranded in Monterey or Santa Cruz county compared with seals stranded in regions further north or south of this central California location.
Juvenile northern elephant seals that have entered the water are being colonized by antimicrobial-resistant and pathogenic fecal bacteria that may be acquired from terrestrial sources transmitted via river and surface waters.
PMCID: PMC2289989  PMID: 19006978
20.  High Prevalence of Proposed Müllerian Duct Remnant Cysts on the Spermatic Duct in Wild Eurasian Otters (Lutra lutra) from Sweden 
PLoS ONE  2013;8(12):e84660.
The spermatic ducts (vasa deferentia) of 235 otters (Lutra lutra) found dead between 1999 and 2012 in Sweden were examined for presence of paraductular cysts. Single or multiple elongated uni- or bilateral cysts parallel to the spermatic duct were noted in 72% of the examined males. The cysts were adjacent to, but did not communicate with the lumen of the spermatic duct, and were usually located within a few centimeters of the testis and epididymis. The cysts are proposed to be congenital Müllerian duct remnants. Other morphologic abnormalities in the reproductive organs were not noted within this study. Possible causes of the incomplete regression of the embryonic female gonadal duct are exposure to environmental contaminants such as elevated concentrations of estrogen-like compounds (endocrine disrupting chemicals), inbreeding, or a naturally occurring anatomic defect. No obvious geographical pattern was observed for otters with or without cysts. This is the first study and description of cysts on the spermatic duct in otters.
PMCID: PMC3871573  PMID: 24376831
21.  Longitudinal Poisson Regression To Evaluate the Epidemiology of Cryptosporidium, Giardia, and Fecal Indicator Bacteria in Coastal California Wetlands 
Applied and Environmental Microbiology  2012;78(10):3606-3613.
Fecal pathogen contamination of watersheds worldwide is increasingly recognized, and natural wetlands may have an important role in mitigating fecal pathogen pollution flowing downstream. Given that waterborne protozoa, such as Cryptosporidium and Giardia, are transported within surface waters, this study evaluated associations between fecal protozoa and various wetland-specific and environmental risk factors. This study focused on three distinct coastal California wetlands: (i) a tidally influenced slough bordered by urban and agricultural areas, (ii) a seasonal wetland adjacent to a dairy, and (iii) a constructed wetland that receives agricultural runoff. Wetland type, seasonality, rainfall, and various water quality parameters were evaluated using longitudinal Poisson regression to model effects on concentrations of protozoa and indicator bacteria (Escherichia coli and total coliform). Among wetland types, the dairy wetland exhibited the highest protozoal and bacterial concentrations, and despite significant reductions in microbe concentrations, the wetland could still be seen to influence water quality in the downstream tidal wetland. Additionally, recent rainfall events were associated with higher protozoal and bacterial counts in wetland water samples across all wetland types. Notably, detection of E. coli concentrations greater than a 400 most probable number (MPN) per 100 ml was associated with higher Cryptosporidium oocyst and Giardia cyst concentrations. These findings show that natural wetlands draining agricultural and livestock operation runoff into human-utilized waterways should be considered potential sources of pathogens and that wetlands can be instrumental in reducing pathogen loads to downstream waters.
PMCID: PMC3346375  PMID: 22427504
22.  A Low-Cost GPS GSM/GPRS Telemetry System: Performance in Stationary Field Tests and Preliminary Data on Wild Otters (Lutra lutra) 
PLoS ONE  2012;7(1):e29235.
Despite the increasing worldwide use of global positioning system (GPS) telemetry in wildlife research, it has never been tested on any freshwater diving animal or in the peculiar conditions of the riparian habitat, despite this latter being one of the most important habitat types for many animal taxa. Moreover, in most cases, the GPS devices used have been commercial and expensive, limiting their use in low-budget projects.
Methodology/Principal Findings
We have developed a low-cost, easily constructed GPS GSM/GPRS (Global System for Mobile Communications/General Packet Radio Service) and examined its performance in stationary tests, by assessing the influence of different habitat types, including the riparian, as well as water submersion and certain climatic and environmental variables on GPS fix-success rate and accuracy. We then tested the GPS on wild diving animals, applying it, for the first time, to an otter species (Lutra lutra). The rate of locations acquired during the stationary tests reached 63.2%, with an average location error of 8.94 m (SD = 8.55). GPS performance in riparian habitats was principally affected by water submersion and secondarily by GPS inclination and position within the riverbed. Temporal and spatial correlations of location estimates accounted for some variation in the data sets. GPS-tagged otters also provided accurate locations and an even higher GPS fix-success rate (68.2%).
Our results suggest that GPS telemetry is reliably applicable to riparian and even diving freshwater animals. They also highlight the need, in GPS wildlife studies, for performing site-specific pilot studies on GPS functioning as well as for taking into account eventual spatial and temporal correlation of location estimates. The limited price, small dimensions, and high performance of the device presented here make it a useful and cost-effective tool for studies on otters and other aquatic or terrestrial medium-to-large-sized animals.
PMCID: PMC3252312  PMID: 22242163
23.  Recovery Trends in Marine Mammal Populations 
PLoS ONE  2013;8(10):e77908.
Marine mammals have greatly benefitted from a shift from resource exploitation towards conservation. Often lauded as symbols of conservation success, some marine mammal populations have shown remarkable recoveries after severe depletions. Others have remained at low abundance levels, continued to decline, or become extinct or extirpated. Here we provide a quantitative assessment of (1) publicly available population-level abundance data for marine mammals worldwide, (2) abundance trends and recovery status, and (3) historic population decline and recent recovery. We compiled 182 population abundance time series for 47 species and identified major data gaps. In order to compare across the largest possible set of time series with varying data quality, quantity and frequency, we considered an increase in population abundance as evidence of recovery. Using robust log-linear regression over three generations, we were able to classify abundance trends for 92 spatially non-overlapping populations as Significantly Increasing (42%), Significantly Decreasing (10%), Non-Significant Change (28%) and Unknown (20%). Our results were comparable to IUCN classifications for equivalent species. Among different groupings, pinnipeds and other marine mammals (sirenians, polar bears and otters) showed the highest proportion of recovering populations, likely benefiting from relatively fast life histories and nearshore habitats that provided visibility and protective management measures. Recovery was less frequent among cetaceans, but more common in coastal than offshore populations. For marine mammals with available historical abundance estimates (n = 47), larger historical population declines were associated with low or variable recent recoveries so far. Overall, our results show that many formerly depleted marine mammal populations are recovering. However, data-deficient populations and those with decreasing and non-significant trends require attention. In particular, increased study of populations with major data gaps, including offshore small cetaceans, cryptic species, and marine mammals in low latitudes and developing nations, is needed to better understand the status of marine mammal populations worldwide.
PMCID: PMC3813518  PMID: 24205025
24.  Synergistic and Antagonistic Effects of Thermal Shock, Air Exposure, and Fishing Capture on the Physiological Stress of Squilla mantis (Stomatopoda) 
PLoS ONE  2014;9(8):e105060.
This study is aimed at assessing the effects of multiple stressors (thermal shock, fishing capture, and exposure to air) on the benthic stomatopod Squilla mantis, a burrowing crustacean quite widespread in the Mediterranean Sea. Laboratory analyses were carried out to explore the physiological impairment onset over time, based on emersion and thermal shocks, on farmed individuals. Parallel field-based studies were carried out to also investigate the role of fishing (i.e., otter trawling) in inducing physiological imbalance in different seasonal conditions. The dynamics of physiological recovery from physiological disruption were also studied. Physiological stress was assessed by analysing hemolymph metabolites (L-Lactate, D-glucose, ammonia, and H+), as well as glycogen concentration in muscle tissues. The experiments were carried out according to a factorial scheme considering the three factors (thermal shock, fishing capture, and exposure to air) at two fixed levels in order to explore possible synergistic, additive, or antagonistic effects among factors. Additive effects on physiological parameters were mainly detected when the three factors interacted together while synergistic effects were found as effect of the combination of two factors. This finding highlights that the physiological adaptive and maladaptive processes induced by the stressors result in a dynamic response that may encounter physiological limits when high stress levels are sustained. Thus, a further increase in the physiological parameters due to synergies cannot be reached. Moreover, when critical limits are encountered, mortality occurs and physiological parameters reflect the response of the last survivors. In the light of our mortality studies, thermal shock and exposure to air have the main effect on the survival of S. mantis only on trawled individuals, while lab-farmed individuals did not show any mortality during exposure to air until after 2 hours.
PMCID: PMC4136847  PMID: 25133593
25.  Phocine Distemper Virus in Northern Sea Otters in the Pacific Ocean, Alaska, USA 
Emerging Infectious Diseases  2009;15(6):925-927.
Phocine distemper virus (PDV) has caused 2 epidemics in harbor seals in the Atlantic Ocean but had never been identified in any Pacific Ocean species. We found that northern sea otters in Alaska are infected with PDV, which has created a disease threat to several sympatric and decreasing Pacific marine mammals.
PMCID: PMC2727316  PMID: 19523293
Viruses; phocine distemper virus; northern sea otters; Alaska; Pacific Ocean; dispatch

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