An Unusual Genotype of Toxoplasma gondii from California Sea Otters (Enhydra lutris nereis): Further Evidence for Land-Sea Connectivity in the Dissemination of Marine Pathogens
IAAAM Archive
Melissa A. Miller1,2; Michael E. Grigg3; Woutrina Miller2; Chris Kreuder2; Erick R. James3; Ann C. Melli2; Haydee Dabritz2; P.R. Crosbie4; David A. Jessup1; Debbie Brownstein1; Patricia A. Conrad2
1California Department of Fish and Game, Marine Wildlife Veterinary Care and Research Center, Santa Cruz, CA, USA; 2Wildlife Health Center, School of Veterinary Medicine, Davis, CA, USA; 3Infectious Diseases, Departments of Medicine and Microbiology & Immunology, University of British Columbia, VGH, Vancouver, BC, Canada; 4Department of Biology, California State University, Fresno, Fresno, CA, USA


Toxoplasma gondii-associated meningoencephalitis is a significant cause of mortality for California sea otters (Enhydra lutris nereis). A growing body of scientific data implicates T. gondii oocysts, shed in the feces of domestic or wild cats, as the most likely environmental source of sea otter infections.12,3,4,5,7 The genus Toxoplasma is represented by a single species, T. gondii, with multiple strains, or genotypes. In terrestrial systems, three T. gondii genotypes (types I, II and III) appear to dominate worldwide. However, only limited investigation had been reported for the genotypic characterization of T. gondii isolates from sea otters and their molecular relationships to T. gondii infecting terrestrial animals and humans.2

In the present study, Toxoplasma gondii isolates were obtained from 35 necropsied California sea otters. Multi-locus PCR-RFLP (polymerase chain reaction and restriction fragment length polymorphisms) and DNA sequencing was completed for two conserved genes (18s rDNA, ITS-1) and four polymorphic genes (B1, SAG1, SAG3 and GRA6).6 No infections due to type I or III T. gondii genotypes were identified. All southern sea otter T. gondii infections were found to be grouped into two distinct genotypic clades: type II genotypes and a novel genotype, designated type x, that possessed distinct alleles at three of four polymorphic loci. At present the majority of sea otter T. gondii infections represent infections with genotype x, with the remaining due to genotype II. For subsequent risk factor studies, significant differences were identified with respect to T. gondii genotype and sea otter gender and stranding location along the California coast. Localized spatial clustering was detected for both genotype II (centered within Monterey Bay) and genotype x (centered near Morro Bay) infected otters. The Morro Bay cluster of type x-infected otters overlaps previously reported high-risk areas for sea otter infection and mortality due to T. gondii.3,5 Nine of twelve otters that had T. gondii-associated meningoencephalitis as a primary cause of death were infected with type x parasites. Genotypic comparison with terrestrial isolates of T. gondii revealed the presence of type x genotypes in wildlife and humans in the United States that on the basis of limited RFLP had been previously identified as Type II genotypes.6


The authors appreciate the assistance and support of employees and volunteers of the California Department of Fish and Game, the Monterey Bay Aquarium, the Marine Mammal Center, the University of California, Davis and the United States Geological Survey.


1.  Arkush KD, MA Miller, A Tenter, CM Leutenegger, A Packham, IA Gardner, BC Barr, PA Conrad. 2003. Molecular and bioassay-based detection of Toxoplasma gondii oocyst uptake in mussels (Mytilus galloprovincialis) following laboratory exposures and evidence of infectivity. International Journal for Parasitology. 33:1087-1097.

2.  Cole RA, DS Lindsay, CL Roderick, JP Dubey, NJ Thomas, LA Baeten. 2000. Biological and molecular characterizations of Toxoplasma gondii obtained from southern sea otters (Enhydra lutris nereis). J. Parasitol. 86:526-530.

3.  Kreuder CM, MA Miller, LJ Lowenstine, MD Harris, TE Carpenter, PA Conrad, D Jessup, JK Mazet. 2003. Recent causes of mortality in southern sea otters (Enhydra lutris nereis). Journal of Wildlife Disease. 39:495-509.

4.  Lindsay DS, KK Phelps, SA Smith, G Flick, JP Dubey. 2001 Removal of Toxoplasma gondii oocysts from sea water by Eastern Oysters (Crassostrea virginica). Journal of Eukaryotic Microbiology. 197S-198S.

5.  Miller MA, IA Gardner, A Packham, D Jessup, R Jameson, E Dodd, PA Conrad. 2002. Coastal freshwater runoff is a risk factor for Toxoplasma gondii infection in southern sea otters (Enhydra lutris nereis). International Journal for Parasitology. 32:997-1006.

6.  Miller MA, ME Grigg, C Kreuder, ER James, AC Melli, PR Crosbie, DA Jessup, JC Boothroyd, D Brownstein, PA Conrad. 2004. An unusual genotype of Toxoplasma gondii is common in California sea otters (Enhydra lutris nereis) and a source of mortality. International Journal for Parasitology. 34: 275-284.

7.  Thomas NJ, RA Cole 1996. Risk of disease and threats to wild populations. Endangered Species Update. 13:23-27.

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Melissa A. Miller

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