Abstract

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.

Highlights

  • A large proportion of wild southern sea otters (Enhydra lutris nereis) are infected with the protozoan parasite Toxoplasma gondii, with up to 70% of live-captured animals exposed in high-risk locations such as Monterey Bay, California [1]

  • Using multi-locus sequence typing (MLST), we found 10 discrete strains in sea otters with incidental T. gondii infections (n = 83); six MLST strains in sea otters with T. gondii as a contributing cause of death (n = 21); and four MLST strains in sea otters with T. gondii as the primary cause of death (n = 12)

  • The odds of dying with toxoplasmosis as a primary cause of death were 29 times higher for sea otters infected with Type X (ToxoDB 5) than those infected with type more commonly associated with domestic cats (Type II) or a mixed Type II/X genotype

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Summary

Introduction

A large proportion of wild southern sea otters (Enhydra lutris nereis) are infected with the protozoan parasite Toxoplasma gondii, with up to 70% of live-captured animals exposed in high-risk locations such as Monterey Bay, California [1]. Among sea otter carcasses examined by pathologists between 1998 and 2001, T. gondii was determined to be the primary cause of death for 17% of otters, and the parasite contributed to mortality for an additional 12% [2]. Only wild and domestic felids serve as definitive hosts, with sexual replication of T. gondii in the gut resulting in faecal shedding of hundreds of millions of environmentally resistant oocysts [6]. Sea otters do not typically prey on warmblooded intermediate hosts of T. gondii (e.g. mammals and birds) and are likely infected via ingestion of oocysts that accumulate in coastal habitats receiving contaminated freshwater run-off [7]

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