Coastal freshwater runoff is a risk factor for Toxoplasma gondii infection of southern sea otters (Enhydra lutris nereis)

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Abstract

The association among anthropogenic environmental disturbance, pathogen pollution and the emergence of infectious diseases in wildlife has been postulated, but not always well supported by epidemiologic data. Specific evidence of coastal contamination of the marine ecosystem with the zoonotic protozoan parasite, Toxoplasma gondii, and extensive infection of southern sea otters (Enhydra lutris nereis) along the California coast was documented by this study. To investigate the extent of exposure and factors contributing to the apparent emergence of T. gondii in southern sea otters, we compiled environmental, demographic and serological data from 223 live and dead sea otters examined between 1997 and 2001. The T. gondii seroprevalence was 42% (49/116) for live otters, and 62% (66/107) for dead otters. Demographic and environmental data were examined for associations with T. gondii seropositivity, with the ultimate goal of identifying spatial clusters and demographic and environmental risk factors for T. gondii infection. Spatial analysis revealed clusters of T. gondii-seropositive sea otters at two locations along the coast, and one site with lower than expected T. gondii seroprevalence. Risk factors that were positively associated with T. gondii seropositivity in logistic regression analysis included male gender, older age and otters sampled from the Morro Bay region of California. Most importantly, otters sampled near areas of maximal freshwater runoff were approximately three times more likely to be seropositive to T. gondii than otters sampled in areas of low flow. No association was found between seropositivity to T. gondii and human population density or exposure to sewage. This study provides evidence implicating land-based surface runoff as a source of T. gondii infection for marine mammals, specifically sea otters, and provides a convincing illustration of pathogen pollution in the marine ecosystem.

Introduction

Growing evidence supports the link between human environmental disturbance and emerging infectious diseases of wildlife populations (Daszak et al., 2001). More than any other animal species, humans impact the environment locally, regionally and globally, inducing atmospheric, hydrological and biochemical changes that can be detected in the most remote regions of the planet. Anthropogenic environmental changes may promote the emergence of pathogens through the transportation and introduction of infectious agents or hosts to new environments, through manipulation of local ecosystems to favour the proliferation or prolonged survival of infectious agents, or by facilitating new host–pathogen interactions. These emerging infectious diseases in turn pose threats to ecosystem biodiversity and human health.

The protozoan parasite Toxoplasma gondii is a recognised pathogen of humans and terrestrial animals. This parasite has a two-host life cycle, with many animals, including mice, birds, domestic livestock and humans serving as potential intermediate hosts (Frenkel and Dubey, 1972). In the intermediate host, invasive stages of T. gondii may spread throughout the muscles, nervous system and other tissues, forming long-lived tissue cysts. However, the only animals known to shed oocysts in their faeces are felids, most importantly domestic cats. These oocyst-shedding definitive hosts are infected through oocyst exposure, or by consumption of infected intermediate hosts.

The most common routes of T. gondii infection for humans are through exposure to oocysts in contaminated soil, transplacental transmission or by consumption of uncooked or undercooked meat containing encysted parasites (Frenkel and Dubey, 1972). However, recent evidence indicates that waterborne T. gondii exposure is more common than previously recognised, and may represent an important source of human infection (Bowie et al., 1997, Aramini et al., 1999, Tenter et al., 2000). These waterborne infections probably result from exposure to infective oocysts in polluted water, but it is also possible that aquatic species serve as intermediate or paratenic hosts.

Increasing recognition of T. gondii infection in diverse species of marine mammals, including cetaceans (Cruickshank et al., 1990, Inskeep et al., 1990, Migaki et al., 1990, Mikelian et al., 2000), pinnipeds (Van Pelt and Dietrich, 1973, Migaki et al., 1977, Holshuh et al., 1985, Miller et al., 2001) and sirenians (Buergelt and Bonde, 1983) provides compelling evidence for marine dispersal of this terrestrial pathogen. Until recently, most reports consisted of case studies on individual T. gondii-infected animals. However, the recent recognition of numerous fatal T. gondii brain infections in southern sea otters (Enhydra lutris nereis) from California (Thomas and Cole, 1996, Cole et al., 2000) prompted concerns about the emergence of T. gondii as a significant marine pathogen. Whether the emergence of T. gondii infection in sea otters is attributable to increasing prevalence, increased surveillance, or both, is unknown. For California otters examined between 1992 and 1995, Thomas and Cole (1996) attributed 8.5% of total sea otter mortality to protozoal meningoencephalitis. Using parasite isolation in cell culture and brain immunohistochemistry, we recently discovered that 36% (28/77) of freshly dead sea otters were infected with T. gondii at the time of postmortem examination (Miller et al., 2002), suggesting that T. gondii infection is common in southern sea otters.

Sea otters are a unique marine mammal species because they live, reproduce and feed almost exclusively in the nearshore marine environment, often within 0.5 km of the shoreline (Riedman and Estes, 1990). As a federally listed threatened species with evidence of recent population declines, the high prevalence of T. gondii infection in southern sea otters is of concern. To investigate the apparent emergence of T. gondii as a pathogen of southern sea otters, we determined seroprevalence in live and dead sea otters examined between 1997 and 2001 using an indirect fluorescent antibody test (IFAT) which was recently validated for sea otters (Miller et al., 2002). Additional coastal environmental data, including location and volumes of river and stream runoff, municipal sewage outfall and human coastal population density were assembled from federal and state sources. The compiled demographic and environmental data were examined for statistical associations with T. gondii seropositivity in sea otters. Our working hypotheses were that T. gondii exposure in sea otters would be positively correlated with age class, total length, body weight, nutritional condition, coastal human population density and areas of maximal sewage and freshwater outflow. Because we focussed on T. gondii seropositivity, not T. gondii-induced disease for the present study, we expected to find no relationship between seropositivity and dead versus live status at time of sampling. Through spatial analysis we hoped to detect high and low risk areas for T. gondii seroprevalence that could provide optimal sampling locations for future research on routes and mechanisms of T. gondii exposure in sea otters.

Section snippets

Study population

Data from 223 live- and dead-sampled otters were included in the study (Table 1). Throughout the study period, yearly rangewide counts identified <2,300 sea otters along the central coast of California (United Sates Geological Survey unpublished technical report). Southern sea otters currently range from Half Moon Bay south to Santa Barbara, California, a distance of approximately 661 km. Data on each otter's gender, age class, stranding or sampling location and other factors, as defined below,

Seroprevalence

The T. gondii seroprevalence was 42% (49/116) for live otters and 62% (66/107) for dead otters using an IFAT cutoff titre of ≥1:320 as positive. Reciprocal IFAT titres ranged from 80 to 20,480 for both live and dead otters. Gender and age distributions differed between the live and dead otters (Table 1). Live-sampled otters had a higher proportion of females (P=0.013) and young age classes (P=0.068) compared with dead otters. These differences between the two groups were accounted for in the

Discussion

The overall goal of the present study was to investigate the apparent emergence of T. gondii infections in southern sea otters from California. Between 1997 and 2001, we collected serum from 223 live and dead sea otters. The current California sea otter population is approximately 2,300 animals. Using a T. gondii IFAT that was previously validated for sea otters, we determined that 42% (49/116) of live otters, and 62% (66/107) of fresh dead California otters were seropositive for T. gondii at

Acknowledgements

This research was supported in part through funding from the National Sea Grant Program (NA06RG0142 R/CZ-169), PKD Trust, the Morris Animal Foundation, the San Francisco Foundation, UC Davis Wildlife Health Center, the Lindbergh Foundation, Friends of the Sea Otter, the Marine Mammal Center and the California Department of Fish and Game. The authors wish to acknowledge the excellent assistance of staff and volunteers from the California Department of Fish and Game, the Marine Mammal Center, the

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