Effect of estuarine wetland degradation on transport of Toxoplasma gondii surrogates from land to sea.
ABSTRACT: 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.
Project description:Why some Toxoplasma gondii-infected southern sea otters (Enhydra lutris nereis) develop fatal toxoplasmosis while others have incidental or mild chronic infections has long puzzled the scientific community. We assessed robust datasets on T. gondii molecular characterization in relation to detailed necropsy and histopathology results to evaluate whether parasite genotype influences pathological outcomes in sea otters that stranded along the central California coast. Genotypes isolated from sea otters were also compared with T. gondii strains circulating in felids from nearby coastal regions to assess land-to-sea parasite transmission. The predominant T. gondii genotypes isolated from 135 necropsied sea otters were atypical Type X and Type X variants (79%), with the remainder (21%) belonging to Type II or Type II/X recombinants. All sea otters that died due to T. gondii as a primary cause of death were infected with Type X or X-variant T. gondii strains. The same atypical T. gondii strains were detected in sea otters with fatal toxoplasmosis and terrestrial felids from watersheds bordering the sea otter range. Our results confirm a land-sea connection for virulent T. gondii genotypes and highlight how faecal contamination can deliver lethal pathogens to coastal waters, leading to detrimental impacts on marine wildlife.
Project description:The increase in human population and domestic pets, such as cats, are generating important consequences in terms of habitat loss and pathogen pollution of coastal ecosystems with potential to generate negative impacts in marine biodiversity. Toxoplasma gondii is the etiological agent of zoonotic disease toxoplasmosis, and is associated with cat abundance and anthropogenic disturbance. The presence of T. gondii oocysts in the ocean has negatively affected the health status of the threatened Southern sea otter (Enhydra lutris nereis) populations. The present study analyzed seroprevalence and presence of T. gondii DNA in American mink (Neovison vison), Southern river otters (Lontra provocax) and domestic cats (Felis silvestris catus) in four different areas in Southern Chile comprising studies in rivers and lakes in Andean foothills and mountains, marine habitat and island coastal ecosystems. Mean seroprevalence of T. gondii in the study was 64% of 151 total animals sampled: 59% of 73 American mink, 77% of 13 Southern river otters, 68% of 65 domestic cats and in two of two kodkods (Leopardus guigna). Toxoplasma gondii DNA was detected in tissues from one American mink and one Southern river otter. The present study confirms the widespread distribution of T. gondii in Southern Chile, and shows a high exposure of semiaquatic mustelids and domestic cats to the parasite. Cats and anthropogenic disturbance have a role in the maintenance of T. gondii infection in ecosystems of southern Chile.
Project description: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.
Project description:The processes promoting disease in wild animal populations are highly complex, yet identifying these processes is critically important for conservation when disease is limiting a population. By combining field studies with epidemiologic tools, we evaluated the relationship between key factors impeding southern sea otter (Enhydra lutris nereis) population growth: disease and resource limitation. This threatened population has struggled to recover despite protection, so we followed radio-tagged sea otters and evaluated infection with 2 disease-causing protozoal pathogens, Toxoplasma gondii and Sarcocystis neurona, to reveal risks that increased the likelihood of pathogen exposure. We identified patterns of pathogen infection that are linked to individual animal behavior, prey choice, and habitat use. We detected a high-risk spatial cluster of S. neurona infections in otters with home ranges in southern Monterey Bay and a coastal segment near San Simeon and Cambria where otters had high levels of infection with T. gondii. We found that otters feeding on abalone, which is the preferred prey in a resource-abundant marine ecosystem, had a very low risk of infection with either pathogen, whereas otters consuming small marine snails were more likely to be infected with T. gondii. Individual dietary specialization in sea otters is an adaptive mechanism for coping with limited food resources along central coastal California. High levels of infection with protozoal pathogens may be an adverse consequence of dietary specialization in this threatened species, with both depleted resources and disease working synergistically to limit recovery.
Project description: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.
Project description:Recovering species are often limited to much smaller areas than they historically occupied. Conservation planning for the recovering species is often based on this limited range, which may simply be an artifact of where the surviving population persisted. Southern sea otters (<i>Enhydra lutris nereis</i>) were hunted nearly to extinction but recovered from a small remnant population on a remote stretch of the California outer coast, where most of their recovery has occurred. However, studies of recently-recolonized estuaries have revealed that estuaries can provide southern sea otters with high quality habitats featuring shallow waters, high production and ample food, limited predators, and protected haul-out opportunities. Moreover, sea otters can have strong effects on estuarine ecosystems, fostering seagrass resilience through their consumption of invertebrate prey. Using a combination of literature reviews, population modeling, and prey surveys we explored the former estuarine habitats outside the current southern sea otter range to determine if these estuarine habitats can support healthy sea otter populations. We found the majority of studies and conservation efforts have focused on populations in exposed, rocky coastal habitats. Yet historical evidence indicates that sea otters were also formerly ubiquitous in estuaries. Our habitat-specific population growth model for California's largest estuary-San Francisco Bay-determined that it alone can support about 6,600 sea otters, more than double the 2018 California population. Prey surveys in estuaries currently with (Elkhorn Slough and Morro Bay) and without (San Francisco Bay and Drakes Estero) sea otters indicated that the availability of prey, especially crabs, is sufficient to support healthy sea otter populations. Combining historical evidence with our results, we show that conservation practitioners could consider former estuarine habitats as targets for sea otter and ecosystem restoration. This study reveals the importance of understanding how recovering species interact with all the ecosystems they historically occupied, both for improved conservation of the recovering species and for successful restoration of ecosystem functions and processes.
Project description:Rapidly developing coastal regions face consequences of land use and climate change including flooding and increased sediment, nutrient, and chemical runoff, but these forces may also enhance pathogen runoff, which threatens human, animal, and ecosystem health. Using the zoonotic parasite Toxoplasma gondii in California, USA as a model for coastal pathogen pollution, we examine the spatial distribution of parasite runoff and the impacts of precipitation and development on projected pathogen delivery to the ocean. Oocysts, the extremely hardy free-living environmental stage of T. gondii shed in faeces of domestic and wild felids, are carried to the ocean by freshwater runoff. Linking spatial pathogen loading and transport models, we show that watersheds with the highest levels of oocyst runoff align closely with regions of increased sentinel marine mammal T. gondii infection. These watersheds are characterized by higher levels of coastal development and larger domestic cat populations. Increases in coastal development and precipitation independently raised oocyst delivery to the ocean (average increases of 44% and 79%, respectively), but dramatically increased parasite runoff when combined (175% average increase). Anthropogenic changes in landscapes and climate can accelerate runoff of diverse pathogens from terrestrial to aquatic environments, influencing transmission to people, domestic animals, and wildlife.
Project description: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.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.
Project description:Effective conservation and restoration of estuarine wetlands require accurate maps of their historical and current extent, as well as estimated losses of these valued habitats. Existing coast-wide tidal wetland mapping does not explicitly map historical tidal wetlands that are now disconnected from the tides, which represent restoration opportunities; nor does it use water level models or high-resolution elevation data (e.g. lidar) to accurately identify current tidal wetlands. To better inform estuarine conservation and restoration, we generated new maps of current and historical tidal wetlands for the entire contiguous U.S. West Coast (Washington, Oregon, and California). The new maps are based on an Elevation-Based Estuary Extent Model (EBEEM) that combines lidar digital elevation models (DEMs) and water level models to establish the maximum historical extent of tidal wetlands, representing a major step forward in mapping accuracy for restoration planning and analysis of wetland loss. Building from this new base, we also developed an indirect method for mapping tidal wetland losses, and created maps of these losses for 55 estuaries on the West Coast (representing about 97% of historical West Coast vegetated tidal wetland area). Based on these new maps, we estimated that total historical estuary area for the West Coast is approximately 735,000 hectares (including vegetated and nonvegetated areas), and that about 85% of vegetated tidal wetlands have been lost from West Coast estuaries. Losses were highest for major river deltas. The new maps will help interested groups improve action plans for estuarine wetland habitat restoration and conservation, and will also provide a better baseline for understanding and predicting future changes with projected sea level rise.
Project description:Toxoplasma gondii oocyst wall protein 1 (TgOWP1) integrates a family of seven proteins, consensually assumed as specific antigens of Toxoplasma gondii oocyst stage, located in the outer layer of the oocyst wall. Herein, we notice the expression of a recombinant antigen, rTgOWP1-f, derived from a fragment selected on basis of its structural homology with Plasmodium MSP1-19. Rabbit polyclonal antibodies anti-rTgOWP1-f evidence ability for specific identification of environmental T. gondii oocysts. We assume, rTgOWP1-f, as a possible biomarker of oocysts. In addition, we present findings supporting this vision, including the development of an immunodetection method for T. gondii oocysts identification.