Hostname: page-component-78c5997874-s2hrs Total loading time: 0 Render date: 2024-11-17T10:13:42.233Z Has data issue: false hasContentIssue false
  • English
  • Français

Ceratonova shasta: a cnidarian parasite of annelids and salmonids

Published online by Cambridge University Press:  09 September 2022

Jerri L. Bartholomew Open the ORCID record for Jerri L. Bartholomew [Opens in a new window] ,
Julie D. Alexander ,
Sascha L. Hallett ,
Gema Alama-Bermejo  and
Stephen D. Atkinson
Jerri L. Bartholomew*
Affiliation:
Department of Microbiology, Oregon State University, Nash Hall 226, Corvallis, Oregon 97331, USA
Julie D. Alexander
Affiliation:
Department of Microbiology, Oregon State University, Nash Hall 226, Corvallis, Oregon 97331, USA
Sascha L. Hallett
Affiliation:
Department of Microbiology, Oregon State University, Nash Hall 226, Corvallis, Oregon 97331, USA
Gema Alama-Bermejo
Affiliation:
Institute of Parasitology, Biology Center of the Czech Academy of Sciences, Branisovska 31, 37005 Ceske Budejovice, Czech Republic Division of Fish Health, University of Veterinary Medicine, Veterinärplatz 1, 1210 Vienna, Austria
Stephen D. Atkinson
Affiliation:
Department of Microbiology, Oregon State University, Nash Hall 226, Corvallis, Oregon 97331, USA
*
Author for correspondence: Jerri L. Bartholomew, E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

The myxozoan Ceratonova shasta was described from hatchery rainbow trout over 70 years ago. The parasite continues to cause severe disease in salmon and trout, and is recognized as a barrier to salmon recovery in some rivers. This review incorporates changes in our knowledge of the parasite's life cycle, taxonomy and biology and examines how this information has expanded our understanding of the interactions between C. shasta and its salmonid and annelid hosts, and how overarching environmental factors affect this host–parasite system. Development of molecular diagnostic techniques has allowed discrimination of differences in parasite genotypes, which have differing host affinities, and enabled the measurement of the spatio-temporal abundance of these different genotypes. Establishment of the C. shasta life cycle in the laboratory has enabled studies on host–parasite interactions and the availability of transcriptomic data has informed our understanding of parasite virulence factors and host defences. Together, these advances have informed the development of models and management actions to mitigate disease.

Keywords

Actinosporediseaseenteronecrosisenvironmental factorsepidemiologyfish immunityintra-specific parasite diversitymanagementmonitoringmyxosporeMyxozoa
Type
Review Article
Information
Parasitology , Volume 149 , Special Issue 14: Fish Parasitology , December 2022 , pp. 1862 - 1875
Check for updates
Copyright
Copyright © The Author(s), 2022. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Ahmad, F, Debes, PV, Pukk, L, Kahar, S, Hartikainen, H, Gross, R and Vasemägi, A (2021) Know your enemy – transcriptome of myxozoan Tetracapsuloides bryosalmonae reveals potential drug targets against proliferative kidney disease in salmonids. Parasitology 148, 726–739.CrossRefGoogle ScholarPubMed
Alama-Bermejo, G, Holzer, AS and Bartholomew, JL (2019) Myxozoan adhesion and virulence: Ceratonova shasta on the move. Microorganisms 7, 397.CrossRefGoogle ScholarPubMed
Alama-Bermejo, G, Meyer, E, Atkinson, SD, Holzer, AS, Wiśniewska, MM, Kolísko, M and Bartholomew, JL (2020) Transcriptome-wide comparisons and virulence gene polymorphisms of host-associated genotypes of the cnidarian parasite Ceratonova shasta in Salmonids. Genome Biology and Evolution 12, 1258–1276.CrossRefGoogle ScholarPubMed
Alama-Bermejo, G, Bartošová-Sojková, P, Atkinson, SD, Holzer, AS and Bartholomew, JL (2022) Proteases as therapeutic targets against the parasitic cnidarian Ceratonova shasta: characterization of molecules key to parasite virulence in salmonid hosts. Frontiers in Cellular and Infection Microbiology 11, 804864.CrossRefGoogle ScholarPubMed
Alcorn, SW, Murra, AL and Pascho, RJ (2002) Effects of rearing temperature on immune functions in sockeye salmon (Oncorhynchus nerka). Fish and Shellfish Immunology 12, 303–334.CrossRefGoogle ScholarPubMed
Alexander, JD, Kerans, BL, Koel, TM and Rasmussen, C (2011) Context-specific parasitism in Tubifex in geothermally influenced stream reaches in Yellowstone National Park. Journal of the North American Benthological Society 30, 853–867.CrossRefGoogle Scholar
Alexander, JD, Hallett, SL, Stocking, R, Xue, L and Bartholomew, JL (2014) Host and parasite populations after a flood. Northwest Science 88, 219–233.CrossRefGoogle Scholar
Alexander, JD, Kerans, B, Hallett, SL and Stevens, L (2015) Part III: host-parasite interactions: chapter 11: invertebrate hosts: annelid obligate hosts. In Okamura, B, Gruhl, A and Bartholomew, JL (eds), Myxozoan Evolution, Ecology and Development. London: Springer, pp. 217–234.CrossRefGoogle Scholar
Alexander, JD, Wright, KA, Som, NA, Hetrick, NJ and Bartholomew, JL (2016) Integrating models to predict the distribution of the invertebrate host of myxosporean parasites. Freshwater Science 35, 1263–1275.CrossRefGoogle Scholar
Americus, B, Hams, N, Klompen, A, Alama-Bermejo, G, Lotan, T, Bartholomew, JL and Atkinson, SD (2021) The cnidarian parasite Ceratonova shasta utilizes inherited and recruited venom-like compounds during infection. PeerJ 9, e12606.CrossRefGoogle ScholarPubMed
Atkinson, SD and Bartholomew, JL (2010 a) Disparate infection patterns of Ceratomyxa shasta (Myxozoa) in rainbow trout Oncorhynchus mykiss and Chinook salmon Oncorhynchus tshawytscha correlate with ITS-1 sequence variation in the parasite. International Journal for Parasitology 40, 599–604.CrossRefGoogle ScholarPubMed
Atkinson, SD and Bartholomew, JL (2010 b) Spatial, temporal and host factors structure the Ceratomyxa shasta (Myxozoa) population in the Klamath River Basin. Infection, Genetics and Evolution 10, 1019–1026.CrossRefGoogle ScholarPubMed
Atkinson, SD, Foott, JS and Bartholomew, JL (2014) Erection of Ceratonova n. gen. (Myxosporea: Ceratomyxidae) to encompass freshwater species C. gasterostea n. sp. from threespine stickleback (Gasterosteus aculeatus) and C. shasta n. comb. from salmonid fishes. Journal of Parasitology 100, 640–645.CrossRefGoogle Scholar
Atkinson, SD, Hallett, SL and Bartholomew, JL (2018) Genotyping of individual Ceratonova shasta (Cnidaria: Myxosporea) myxospores reveals intra-spore ITS-1 variation and invalidates the distinction of genotypes II and III. Parasitology 145, 1588–1593.CrossRefGoogle ScholarPubMed
Atkinson, SD, Bartholomew, JL and Rouse, GW (2020) The invertebrate host of salmonid fish parasites Ceratonova shasta and Parvicapsula minibicornis (Cnidaria), is a novel fabriciid annelid, Manayunkia occidentalis sp. nov. (Sabellida: Fabriciidae). Zootaxa 4751, 310–320.CrossRefGoogle ScholarPubMed
Barrett, DE (2020) What Makes a Fish Resistant? Comparative Genomics and Transcriptomics of Oncorhynchus mykiss with Differential Resistance to the Parasite Ceratonova shasta (PhD thesis). Oregon State University, Corvallis, OR, USA.Google Scholar
Barrett, DE and Bartholomew, JL (2021) A tale of two fish: comparative transcriptomics of resistant and susceptible steelhead following exposure to Ceratonova shasta highlights differences in parasite recognition. PLoS ONE 16, e0234837.CrossRefGoogle ScholarPubMed
Barrett, DE, Estensoro, I, Sitjà-Bobadilla, A and Bartholomew, JL (2021) Intestinal transcriptomic and histologic profiling reveals tissue repair mechanisms underlying resistance to the parasite Ceratonova shasta. Pathogens 10, 1179.CrossRefGoogle Scholar
Bartholomew, JL (1998) Host resistance to infection by the myxosporean parasite Ceratomyxa shasta: a review. Journal of Aquatic Animal Health 10, 112–120.2.0.CO;2>CrossRefGoogle Scholar
Bartholomew, JL, Smith, CE, Rohovec, JS and Fryer, JL (1989) Characterization of the host response to the myxosporean parasite, Ceratomyxa shasta (Noble), by histology, scanning electron microscopy, and immunological techniques. Journal of Fish Diseases 12, 509–522.CrossRefGoogle Scholar
Bartholomew, JL, Whipple, MJ, Stevens, DG and Fryer, JL (1997) The life cycle of Ceratomyxa shasta, a myxosporean parasite of salmonids, requires a freshwater polychaete as an alternate host. Journal of Parasitology 83, 859–868.CrossRefGoogle ScholarPubMed
Bartholomew, JL, Whipple, MJ and Campton, D (2001) Inheritance of resistance to Ceratomyxa shasta in progeny from crosses between high- and low-susceptibility strains of rainbow trout (Oncorhynchus mykiss). Bulletin of the National Research Institute of Aquaculture (suppl. 5), 71–75.Google Scholar
Bartholomew, JL, Ray, E, Torell, B, Whipple, MJ and Heidel, JR (2004) Monitoring Ceratomyxa shasta infection during a hatchery rearing cycle: comparison of molecular, serological and histological methods. Diseases of Aquatic Organisms 62, 85–92.CrossRefGoogle ScholarPubMed
Bartholomew, JL, Atkinson, SD and Hallett, SL (2006) Involvement of Manayunkia speciosa (Annelida: Polychaeta: Sabellidae) in the life cycle of Parvicapsula minibicornis, a myxozoan parasite of pacific salmon. Journal of Parasitology 92, 742–748.CrossRefGoogle ScholarPubMed
Bartošová-Sojková, P, Kyslík, J, Alama-Bermejo, G, Hartigan, A, Atkinson, SD, Bartholomew, JL, Picard-Sánchez, A, Palenzuela, O, Faber, MN, Holland, JW and Holzer, AS (2021) Evolutionary analysis of cystatins of early-emerging metazoans reveals a novel subtype in parasitic cnidarians. Biology 10, 110.CrossRefGoogle ScholarPubMed
Bird, PI, Trapani, JA and Villadangos, JA (2009) Endolysosomal proteases and their inhibitors in immunity. Nature Reviews Immunology 9, 871–882.CrossRefGoogle ScholarPubMed
Bjork, SJ (2010) Factors Affecting the Ceratomyxa shasta Infectious Cycle and Transmission between Polychaete and Salmonid Hosts (PhD thesis). Oregon State University, Corvallis, OR, USA.Google Scholar
Bjork, SJ and Bartholomew, JL (2009 a) Effects of Ceratomyxa shasta dose on a susceptible strain of rainbow trout and comparatively resistant Chinook and coho salmon. Diseases of Aquatic Organisms 86, 29–37.CrossRefGoogle ScholarPubMed
Bjork, SJ and Bartholomew, JL (2009 b) The effects of water velocity on the Ceratomyxa shasta infectious cycle. Journal of Fish Disease 32, 131–142.CrossRefGoogle ScholarPubMed
Bjork, SJ and Bartholomew, JL (2010) Invasion of Ceratomyxa shasta (Myxozoa) and comparison of migration to the intestine between susceptible and resistant fish hosts. International Journal for Parasitology 40, 1087–1095.CrossRefGoogle Scholar
Bjork, SJ, Zhang, Y, Hurst, CN, Alonso-Naveiro, ME, Alexander, JD, Sunyer, JO and Bartholomew, J (2014) Defenses of susceptible and resistant Chinook salmon (Oncorhynchus tshawytscha) against the myxozoan parasite Ceratomyxa shasta. Journal of Fish and Shellfish Immunology 37, 87–95.CrossRefGoogle ScholarPubMed
Bower, SM and Margolis, L (1985) Microfiltration and ultraviolet irradiation to eliminate Ceratomyxa shasta (Myxozoa: Myxosporea), a salmonid pathogen, from Fraser River water, British Columbia. Canadian Technical Report of Fisheries and Aquatic Sciences 1364, 11.Google Scholar
Brekhman, V, Ofek-Lalzar, M, Atkinson, SD, Alama-Bermejo, G, Maor-Landaw, K, Malik, A, Bartholomew, JL and Lotan, T (2021) Proteomic analysis of the parasitic cnidarian Ceratonova shasta (Cnidaria: Myxozoa) reveals diverse roles of actin in motility and spore formation. Frontiers in Marine Science 8, 632700.CrossRefGoogle Scholar
Breyta, R, Atkinson, SD and Bartholomew, JL (2019) Evolutionary dynamics of Ceratonova species in the Klamath River basin reveals different host adaptation strategies. Infection, Genetics and Evolution 78, 104081.CrossRefGoogle ScholarPubMed
Buchanan, DV, Sanders, JE, Zinn, JL and Fryer, JL (1983) Relative susceptibility of four strains of summer steelhead to infection by Ceratomyxa shasta. Transactions of the American Fisheries Society 112, 541–543.2.0.CO;2>CrossRefGoogle Scholar
Cassone, A, Vecchiarelli, A and Hube, B (2016) Aspartyl proteinases of eukaryotic microbial pathogens: from eating to heating. PLoS Pathogens 12, e1005992.CrossRefGoogle ScholarPubMed
Chapman, PF (1986) Occurrence of the noninfective stage of Ceratomyxa shasta in mature summer chinook salmon in the south fork Salmon River, Idaho. Progressive Fish-Culturist 48, 304–306.2.0.CO;2>CrossRefGoogle Scholar
Chiaramonte, LV, Ray, RA, Corum, RA, Soto, T, Hallett, SL and Bartholomew, JL (2016) Klamath River thermal refuge provides juvenile salmon reduced exposure to the parasite Ceratonova shasta. Transactions of the American Fisheries Society 145, 810–820.CrossRefGoogle Scholar
Crête-Lafrenière, A, Weir, LK and Bernatchez, L (2012) Framing the Salmonidae family phylogenetic portrait: a more complete picture from increased taxon sampling. PLoS ONE 7, e46662.CrossRefGoogle ScholarPubMed
Curtis, J, Poitras, T, Bond, S and Byrd, K (2021) Sediment Mobility and River Corridor Assessment for a 140-Kilometer Segment of the Main-Stem Klamath River below Iron Gate Dam CA. Washington D.C.: U.S. Geological Survey Open-File Report 2020–1141, 38p. Available at https://doi.org/10.3133/ofr2020114.CrossRefGoogle Scholar
DuBey, R and Caldwell, C (2004) Distribution of Tubifex tubifex lineages and Myxobolus cerebralis infection in the tailwater of the San Juan River, New Mexico. Journal of Aquatic Animal Health 16, 179–185.CrossRefGoogle Scholar
Eszterbauer, E, Atkinson, S, Diamant, A, Morris, D, El-Matbouli, M and Hartikainen, H (2015) Myxozoan life cycles: practical approaches and insights. In Okamura, B, Gruhl, A and Bartholomew, J (eds), Myxozoan Evolution, Ecology and Development. London: Springer, pp. 175–198. Available at doi: 10.1007/978-3-319-14753-6_10.CrossRefGoogle Scholar
Foott, JS, Stone, R and True, K (2007) Relationship between Ceratomyxa Shasta and Parvicapsula minibicornis Actinospore Exposure in the Klamath River and Infection in Juvenile Chinook Salmon. FY 2006 Investigational Report. Anderson, CA: US Fish and Wildlife Service, CA-NV Fish Health Center.Google Scholar
Foott, JS, Stone, R, Fogerty, R, True, K, Bolick, A, Bartholomew, JL, Hallett, SL, Buckles, GR and Alexander, JD (2016) Production of Ceratonova shasta myxospores from salmon carcasses: carcass removal is not a viable management option. Journal of Aquatic Animal Health 28, 75–84.CrossRefGoogle Scholar
Fujiwara, M, Mohr, MS, Greenberg, A, Foott, JS and Bartholomew, JL (2011) Effects of ceratomyxosis on population dynamics of Klamath fall-run Chinook salmon. Transactions of the American Fisheries Society 140, 1380–1391.CrossRefGoogle Scholar
Gras, S, Byzia, A, Gilbert, FB, McGowan, S, Drag, M, Silvestre, A, Niepceron, A, Lecaille, F, Lalmanach, G and Brossier, F (2014) Aminopeptidase N1 (EtAPN1), an M1 metalloprotease of the apicomplexan parasite Eimeria tenella, participates in parasite development. Eukaryotic Cell 13, 884–895.CrossRefGoogle ScholarPubMed
Hallett, SL and Bartholomew, JL (2006) Application of a real-time PCR assay to detect and quantify the myxozoan parasite Ceratomyxa shasta in river water samples. Diseases of Aquatic Organisms 71, 109–118.CrossRefGoogle ScholarPubMed
Hallett, SL and Bartholomew, JL (2012) Chapter 8: Myxobolus cerebralis and Ceratomyxa shasta. In Woo, PTK and Buchmann, K (eds), Fish Parasites: Pathobiology and Protection. Oxfordshire, UK: CABI, pp. 131–162.CrossRefGoogle Scholar
Hallett, SL, Erséus, C, O'Donoghue, PJ and Lester, RJG (2001) Parasite fauna of Australian marine oligochaetes. Memoirs of the Queensland Museum 46, 555–576.Google Scholar
Hallett, SL, Ray, RA, Hurst, CN, Holt, RA, Buckles, GR, Atkinson, SD and Bartholomew, JL (2012) Density of the waterborne parasite Ceratomyxa shasta and its biological effects on salmon. Applied and Environmental Microbiology 78, 3724–3731.CrossRefGoogle ScholarPubMed
Hamilton, JB, Rondorf, DW, Tinniswood, WR, Leary, RJ, Mayer, T, Gavette, C and Casal, LA (2016) The persistence and characteristics of Chinook salmon migrations to the Upper Klamath River prior to exclusion by dams. Oregon Historical Quarterly 117, 326–377.CrossRefGoogle Scholar
Hillemeier, D, Belchik, M, Soto, T, Tucker, SC and Ledwin, S (2017) Measures to Reduce Ceratonova shasta Infection of Klamath River Salmonids. A Guidance Document. CA: Disease Technical Advisory Team.https://www.waterboards.ca.gov/waterrights/water_issues/programs/bay_delta/california_waterfix/exhibits/docs/PCFFA&IGFR/part2/pcffa_154.pdf.Google Scholar
Holzer, AS, Sommerville, C and Wootten, R (2004) Molecular relationships and phylogeny in a community of myxosporeans and actinosporeans based on their 18S rDNA sequences. International Journal of Parasitology 34, 1099–1111.CrossRefGoogle Scholar
Holzer, AS, Piazzon, MC, Barrett, D, Bartholomew, JL and Sitjà-Bobadilla, A (2021) To react or not to react: the dilemma of fish immune systems facing myxozoan infections. Frontiers in Immunology 12, 734238.CrossRefGoogle ScholarPubMed
Hurst, CN and Bartholomew, JL (2012) Ceratomyxa shasta genotypes cause differential mortality in their salmonid hosts. Journal of Fish Diseases 35, 725–732.CrossRefGoogle ScholarPubMed
Hurst, CN, Holt, RA and Bartholomew, JL (2012) Ceratomyxa shasta in the Williamson River, Oregon: implications for reintroduced salmon. North American Journal of Fisheries Management 32, 14–23.CrossRefGoogle Scholar
Hurst, CN, Wong, P, Hallett, SL, Ray, RA and Bartholomew, JL (2014) Transmission and persistence of Ceratomyxa shasta genotypes in chinook salmon. Journal of Parasitology 100, 773–777.CrossRefGoogle Scholar
Hurst, CN, Alexander, JD, Dolan, BP, Jia, L and Bartholomew, JL (2019) Outcome of within-host competition demonstrates that parasite virulence doesn't equal success in a myxozoan model system. International Journal for Parasitology: Parasites and Wildlife 9, 25–35.Google Scholar
Ibarra, AM, Gall, GAE and Hedrick, RP (1991) Susceptibility of two strains of rainbow trout Oncorhynchus mykiss to experimentally induced infections with the myxosporean Ceratomyxa shasta. Diseases of Aquatic Organisms 10, 191–194.CrossRefGoogle Scholar
Ibarra, AM, Hedrick, RP and Gall, GAE (1992) Inheritance of susceptibility to Ceratomyxa shasta (Myxozoa) in rainbow trout and the effect of length of exposure on the liability to develop ceratomyxosis. Aquaculture 104, 217–229.CrossRefGoogle Scholar
Ibarra, AM, Hedrick, RP and Gall, GAE (1994) Genetic analysis of rainbow trout susceptibility to the myxosporean, Ceratomyxa shasta. Aquaculture 120, 239–262.CrossRefGoogle Scholar
Johnson, KA, Sanders, JE and Fryer, JL (1979) Ceratomyxa shasta in Salmonids. Washington D.C.: U.S. Fish and Wildlife Service, Fish Disease Leaflet 58.Google Scholar
Jones, SRM, Bartholomew, JL and Zhang, JY (2015) Mitigating myxozoan disease impacts on wild fish populations. In Okamura, B, Gruhl, A and Bartholomew, JL (eds), Myxozoan Evolution, Ecology and Development. London: Springer, pp. 397–413. Available at https://doi.org/10.1007/978-3-319-14753-6_21.CrossRefGoogle Scholar
Kent, ML, Soderlund, K, Thomann, E, Schreck, CB and Sharpton, TJ (2014) Post-mortem sporulation of Ceratomyxa shasta (Myxozoa) after death in adult Chinook salmon. Journal of Parasitology 100, 679–683.CrossRefGoogle ScholarPubMed
Krueger, RC, Kerans, BL, Vincent, E and Rasmussen, C (2006) Risk of Myxobolus cerebralis infection to rainbow trout in the Madison River, Montana, USA. Ecological Applications 16, 770–783.CrossRefGoogle ScholarPubMed
Lee, JY, Song, SM, Moon, EK, Lee, YR, Jha, BK, Danne, DB, Cha, HJ, Yu, HS, Kong, HH, Chung, DI and Hong, Y (2013) Cysteine protease inhibitor (Acstefin) is required for complete cyst formation of Acanthamoeba. Eukaryotic Cell 12, 567–574.CrossRefGoogle ScholarPubMed
Lehman, BM, Johnson, RC, Adkison, M, Burgess, OT, Connon, RE, Fangue, NA, Foott, JS, Hallett, SL, Martinez–López, B, Miller, KM, Purcell, MK, Som, NA, Valdes–Donoso, P and Collins, AL (2020) Disease in Central Valley Salmon: status and lessons from other systems. San Francisco Estuary and Watershed Science 18, 1–31.CrossRefGoogle Scholar
Lodh, N, Stevens, L and Kerans, B (2011) Prevalence of Myxobolus cerebralis infections among genetic lineages of Tubifex tubifex at three locations in the Madison River, Montana. Journal of Parasitology 97, 531–534.CrossRefGoogle ScholarPubMed
Margolis, L, McDonald, TE and Whitaker, DJ (1992) Assessment of the impact of the myxosporean parasite Ceratomyxa shasta on survival of seaward migrating juvenile chinook salmon, Oncorhynchus tshawytscha, from the Fraser River, British Columbia. Canadian Journal of Fisheries and Aquatic Sciences 49, 1883–1889.CrossRefGoogle Scholar
Meaders, MD and Hendrickson, GL (2009) Chronological development of Ceratomyxa shasta in the polychaete host, Manayunkia speciosa. Journal of Parasitology 95, 1397–1408.CrossRefGoogle ScholarPubMed
Nichols, KM, Young, WP, Danzmann, RG, Robison, BD, Rexroad, C, Noakes, M, Phillips, RB, Bentzen, P, Spies, I, Knudsen, K, Allendorf, FW, Cunningham, BM, Brunelli, J, Zhang, H, Ristow, S, Drew, R, Brown, KH, Wheeler, PA and Thorgaard, GH (2003 a) A consolidated linkage map for rainbow trout (Oncorhynchus mykiss). Animal Genetics 34, 102–115.CrossRefGoogle ScholarPubMed
Nichols, KM, Bartholomew, JL and Thorgaard, GH (2003 b) Mapping multiple genetic loci associated with Ceratomyxa shasta resistance in Oncorhynchus mykiss. Diseases of Aquatic Organisms 56, 145–154.CrossRefGoogle ScholarPubMed
Noble, ER (1950) On a myxosporidian (protozoan) parasite of California trout. Journal of Parasitology 36, 457–460.CrossRefGoogle ScholarPubMed
Palenzuela, O, Trobridge, G and Bartholomew, JL (1999) Development of a polymerase chain reaction diagnostic assay for Ceratomyxa shasta, a myxosporean parasite of salmonid fish. Diseases of Aquatic Organisms 36, 45–51.CrossRefGoogle ScholarPubMed
Palti, Y, Genet, C, Gao, G, Hu, Y, You, FM, Boussaha, M, Rexroad, CE and Luo, MC (2011) A second generation integrated map of the rainbow trout (Oncorhynchus mykiss) genome: analysis of conserved synteny with model fish genomes. Marine Biotechnology 14, 343–357.CrossRefGoogle ScholarPubMed
Piriatinskiy, G, Atkinson, SD, Park, S, Morgenstern, D, Brekhman, V, Yossifon, G, Bartholomew, JL and Lotan, T (2017) Functional and proteomic analysis of Ceratonova shasta (Cnidaria: Myxozoa) polar capsules reveals adaptations to parasitism. Scientific Reports 7, 9010.CrossRefGoogle ScholarPubMed
Quinn, TP (2018) The Behavior and Ecology of Pacific Salmon and Trout. Seattle: University of Washington Press.Google Scholar
Ratliff, DE (1981) Ceratomyxa shasta: epizootiology in Chinook salmon of central Oregon. Transactions of the American Fisheries Society 110, 507–513.2.0.CO;2>CrossRefGoogle Scholar
Ratliff, DE (1983) Ceratomyxa shasta: Longevity, distribution, timing, and abundance of the infective stage in Central Oregon. Canadian Journal of Fisheries and Aquatic Sciences 40, 1622–1632.CrossRefGoogle Scholar
Ray, RA and Bartholomew, JL (2013) Estimation of transmission dynamics of the Ceratomyxa shasta actinospore to the salmonid host. Parasitology 140, 907–916.CrossRefGoogle Scholar
Ray, RA, Rossignol, PA and Bartholomew, JL (2010) Mortality threshold for juvenile Chinook salmon Oncorhynchus tshawytscha in an epidemiological model of Ceratomyxa shasta. Diseases of Aquatic Organisms 93, 63–70.CrossRefGoogle Scholar
Ray, RA, Holt, RA and Bartholomew, JL (2012) Relationship between temperature and Ceratomyxa shasta-induced mortality in Klamath River salmonids. Journal of Parasitology 98, 520–526.CrossRefGoogle ScholarPubMed
Ray, RA, Perry, RW, Som, NA and Bartholomew, JL (2014) Using cure models for analyzing the influence of pathogens on salmon survival. Transactions of the American Fisheries Society 143, 387–398.CrossRefGoogle Scholar
Ray, RA, Alexander, JD, De Leenheer, P and Bartholomew, JL (2015) Modeling the effects of climate change on disease severity: a case study of Ceratonova (syn Ceratomyxa) shasta in the Klamath River. In Okamura, B, Gruhl, A and Bartholomew, JL (eds), Myxozoan Evolution, Ecology and Development. London: Springer, pp. 363–378.Google Scholar
Richey, CA, Kenelty, KV, Hopkins, KVS, Stevens, BN, Martínez-López, B, Hallett, SL, Atkinson, SD, Bartholomew, JL and Soto, E (2020) Validation of environmental DNA sampling for determination of Ceratonova shasta (Noble, 1950) (Cnidaria: Myxozoa) distribution in Plumas National Forest, CA. Parasitology Research 119, 859–870.CrossRefGoogle Scholar
Robinson, HE, Alexander, JD, Hallett, SL and Som, NA (2020) Management brief: prevalence of infection in hatchery-origin Chinook salmon correlates with abundance of Ceratonova shasta spores: implications for management and disease risk. North American Journal of Fisheries Management 40, 959–972.CrossRefGoogle Scholar
Robinson, HE, Alexander, JD, Bartholomew, JL, Hallett, SL, Hetrick, N, Perry, R and Som, NA (2022) Using a mechanistic framework to model the density of an aquatic parasite Ceratonova shasta. PeerJ 10, e13183.CrossRefGoogle ScholarPubMed
Schafer, WE (1968) Studies on the epizootiology of the myxosporidan Ceratomyxa shasta Noble. California Fish and Game 54, 90–99.Google Scholar
Scharsack, JP and Franke, F (2022) Temperature effects on teleost immunity in the light of climate change. Journal of Fish Biology 2022, 1–17. doi: 10.1111/jfb.15163Google Scholar
Stinson, MET and Bartholomew, JL (2012) Predicted redistribution of Ceratomyxa shasta genotypes with salmonid passage in the Deschutes River, Oregon. Journal of Aquatic Animal Health 24, 274–280.CrossRefGoogle ScholarPubMed
Stinson, MET, Atkinson, SD and Bartholomew, JL (2018) Widespread distribution of Ceratonova shasta (Cnidaria: Myxosporea) genotypes indicates evolutionary adaptation to its salmonid fish hosts. Journal of Parasitology 104, 645–650.CrossRefGoogle ScholarPubMed
Stocking, RW and Bartholomew, JL (2007) Distribution and habitat characteristics of Manayunkia speciosa and infection prevalence with the parasite Ceratomyxa shasta in the Klamath River, Oregon-California. Journal of Parasitology 93, 78–88.CrossRefGoogle ScholarPubMed
Taggart-Murphy, L, Alama-Bermejo, G, Dolan, B, Takizawa, F and Bartholomew, J (2021) Differences in inflammatory responses of rainbow trout infected by two genotypes of the myxozoan parasite Ceratonova shasta. Developmental and Comparative Immunology 114, 103829.CrossRefGoogle ScholarPubMed
Taghon, GL, Nowell, A and Jumars, P (1980) Induction of suspension feeding in spionid polychaetes by high particulate fluxes. Science 210, 562–564.CrossRefGoogle ScholarPubMed
Thompson, TQ, Bellinger, MR, O'Rourke, SM, Prince, DJ, Stevenson, AE, Rodrigues, AT, Sloat, MR, Speller, CF, Yang, DY, Butler, VL, Banks, MA and Miller, MR (2019) Anthropogenic habitat alteration leads to rapid loss of adaptive variation and restoration potential in wild salmon populations. Proceedings of the National Academy of Sciences 116, 177–186.CrossRefGoogle ScholarPubMed
Thompson, NF, Anderson, EA, Clemento, AJ, Campbell, MA, Pearse, DA, Hearsey, JW, Kinziger, AP and Garza, JC (2020) A complex phenotype in salmon controlled by a simple change in migratory timing. Science 370, 609–613.CrossRefGoogle ScholarPubMed
Vaughn, CC, Spooner, D and Galbraith, HS (2007) Context-dependent species identity effects within a functional group of filter-feeding bivalves. Ecology 88, 1654–1662.CrossRefGoogle ScholarPubMed
Voss, A, Benson, C and Freund, S (2022) Myxosporean Parasite (Ceratonova shasta and Parvicapsula minibicornis) Prevalence of Infection in Klamath River Basin Juvenile Chinook Salmon, March–July 2021. Anderson, CA: U.S. Fish & Wildlife Service. California – Nevada Fish Health Center.Google Scholar
Xiao, C and Desser, SS (1998) The oligochaetes and their actinosporean parasites in Lake Sasajewun, Algonquin Park, Ontario. Journal of Parasitology 84, 1020–1026.CrossRefGoogle ScholarPubMed
Yamamoto, T and Sanders, JE (1979) Light and electron microscopic observations of sporogenesis in the myxosporida, Ceratomyxa shasta (Noble, 1950). Journal of Fish Diseases 2, 411–428.CrossRefGoogle Scholar
Yokoyama, H, Ogawa, K and Wakabayashi, H (1993) Some biological characteristics of actinosporeans from the oligochaete Branchiura sowerbyi. Diseases of Aquatic Organisms 17, 223–228.CrossRefGoogle Scholar
Zhang, YA, Salinas, I, Li, J, Parra, D, Bjork, S, Xu, Z, LaPatra, SE, Bartholomew, J and Sunyer, JO (2010) IgT, a primitive immunoglobulin class specialized in mucosal immunity. Nature Immunology 11, 827–835.CrossRefGoogle ScholarPubMed