Production of Ceratonova shasta Myxospores from Salmon Carcasses: Carcass Removal Is Not a Viable Management Option

Abstract

Severe infection by the endemic myxozoan parasite, Ceratonova (synonym, Ceratomyxa) shasta, has been associated with declines in and impaired recovery efforts of populations of fall-run Chinook Salmon Oncorhynchus tshawytscha in the Klamath River, California. The parasite has a complex life cycle involving a polychaete worm host as well as a salmon host. Myxospore transmission of this parasite, from salmon to polychaete, is a life cycle step during which there is a potential for applied disease management. A 3-year data set on prevalence, intensity, and spore characteristics of C. shasta myxospores was obtained from adult Chinook Salmon carcasses surveyed in the main stem of the Klamath River and three of its tributaries, Bogus Creek and the Shasta and Trinity rivers. Annual prevalence of myxospore detection in salmon intestines ranged from 22% to 52%, and spore concentration values per intestinal scraping ranged from 3.94 × 10² to 1.47 × 10⁷ spores. A prevalence of 7.3% of all carcasses examined produced >5.0 × 10⁵ spores, and these carcasses with “high” spore counts accounted for 76–95% of the total spores in a given spawning season. Molecular analysis of visually negative carcasses showed that 45–87% of these samples had parasite DNA, indicating they contained either low spore numbers or presporogonic stages of the parasite. Myxospores were rarely found in carcasses of freshly spawned adults but were common in decomposed carcasses of both sexes. The date of collection or age (based indirectly on FL) did not influence detection. The longer prespawn residence time for spring-run Chinook Salmon compared with that for fall-run Chinook Salmon in the Trinity River was associated with higher spore loads. The dye exclusion method for assessing spore viability in fresh smears indicated an inverse relationship in spore integrity and initial spore concentration. A carcass-removal pilot project in Bogus Creek for 6 weeks in the fall of 2008 (907 carcasses removed) and 2009 (1,799 carcasses removed) failed to measurably influence the DNA quantity of C. shasta in targeted waters. Combined with the high numbers of carcasses that contributed myxospores, we therefore deemed that this labor-intensive approach is not a viable management option to reduce the infectivity of C. shasta in Chinook Salmon in the Klamath River.

Received January 23, 2015; accepted September 28, 2015

Acknowledgments

We sincerely thank the following individuals for collecting intestine samples: Bogus Creek collection (Yurok Fisheries): Josh Strange, Troy Fletcher Jr., and Albert Marlusser; Klamath River (Arcata Fish and Wildlife Office): Steve Gough, Ernest Chen, Tony Heacock, Aaron Johnson, Mark Magneson, Dan Menten, Amanda Piscitelli, Mandy Proudman, Ryan Slezak, and Katrina Wright. Access to carcasses was provided by Morgan Knechtle in the Shasta River and by Andy Hill in the Trinity River. Access to spawned adults was provided by the staff at the Iron Gate and Trinity River hatcheries. Ken Nichols assisted with laboratory processing and Adam Ray with water and sediment DNA sampling. Partial support for this work was derived from grants with the Pacific States Marine Fisheries Commission, U.S. Bureau of Reclamation, and National Oceanic and Atmospheric Administration. The mention of specific products does not constitute endorsement by the U.S. Fish and Wildlife Service.

Notes

¹ For many years, highly susceptible Rainbow Trout have been used to detect C. shasta in waterways. However, subsequent to our conducting the Bogus Creek sentinel fish exposures with out-of-basin Rainbow Trout, different genotypes of C. shasta were identified that are associated with different salmonid host species (Atkinson and Bartholomew 2010). For example, genotype I causes mortality in Chinook Salmon, whereas genotype II can be fatal for Coho Salmon Oncorhynchus kisutch and Rainbow Trout. Thus, sentinel trout would only detect a subset of the potential parasite population in Bogus Creek (genotype II but not genotype I). So the statement that the parasite eDNA in Bogus Creek water samples was strictly myxospore derived rather than actinospore derived is only partially supported by the negative infection response of the sentinel trout. We cannot completely rule out the presence of C. shasta genotype I actinospores without using Chinook Salmon sentinels. However, we are still confident that the majority of the eDNA is myxospore derived since we found high numbers of these spores in the local salmon (carcasses) and the habitat in that creek is regarded as unsuitable for the polychaete host that produces the actinospore stage.