{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,5]],"date-time":"2026-10-05T21:58:15Z","timestamp":1791237495237,"version":"4.1.0"},"reference-count":59,"publisher":"American Society of Parasitologists","issue":"2","content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Journal of Parasitology"],"published-print":{"date-parts":[[2026,3,9]]},"abstract":"<jats:p>The myxozoan parasite responsible for proliferative kidney disease (PKD), Tetracapsuloides bryosalmonae, alternates between salmonid fishes and freshwater bryozoans to complete its life cycle. However, no active hosts (species that shed viable, infectious spores) for the North American (NA) strain have been identified. We used fish-to-bryozoan and bryozoan-to-fish transmission experiments to assess the active host status of steelhead trout [Oncorhynchus mykiss] and the bryozoan Fredericella borealis. Specific pathogen-free F. borealis colonies were first exposed to effluent from naturally infected O. mykiss and monitored weekly using stereomicroscopy for overt T. bryosalmonae infections. Malacospores from infected colonies were then introduced to na\u00efve O. mykiss, which were held at 16 C and sampled for polymerase chain reaction (PCR) and histology 2 and 8 wk post-exposure. Additionally, statoblasts and hatched zooids from overtly infected F. borealis colonies were screened with stereomicroscopy and quantitative real-time PCR (qPCR) to investigate transmission of T. bryosalmonae from zooids to statoblasts. Our results demonstrate that subclinically-infected O. mykiss shed viable fish malacospores of the NA strain of T. bryosalmonae, as evidenced by the development of overt infections in exposed F. borealis. Malacospores shed from the bryozoan subsequently induced clinical PKD in na\u00efve O. mykiss, which exhibited kidney swelling upon necropsy, extrasporogonic stages of the parasite in histology, and PCR detections of T. bryosalmonae DNA. We found no evidence of vertical transmission within F. borealis. Given the widespread rearing and stocking of O. mykiss across North America, these findings highlight the importance of pre-release surveillance in susceptible stocks to prevent dissemination of T. bryosalmonae in habitats where suitable host populations may overlap.<\/jats:p>","DOI":"10.1645\/25-47","type":"journal-article","created":{"date-parts":[[2026,3,16]],"date-time":"2026-03-16T10:02:58Z","timestamp":1773655378000},"page":"122-132","source":"Crossref","is-referenced-by-count":2,"title":["The Salmonid Oncorhynchus mykiss and Bryozoan Fredericella borealis Serve as Active Hosts for the North American Strain of Tetracapsuloides bryosalmonae, the Cause of Proliferative Kidney Disease"],"prefix":"10.1645","volume":"112","author":[{"given":"N.","family":"Das","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"S. D.","family":"Atkinson","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-8112-8203","authenticated-orcid":false,"given":"S. L.","family":"Hallett","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1220","reference":[{"key":"54","doi-asserted-by":"crossref","unstructured":"A. Waeschenbach, P. D. Taylor, D. T. J. Littlewood,  \"Molecular Phylogenetics and Evolution.\"  62, \"A molecular phylogeny of bryozoans.\" 718 (2012)","DOI":"10.1016\/j.ympev.2011.11.011"},{"key":"1","doi-asserted-by":"crossref","unstructured":"A. Abd-Elfattah, I. Fontes, G. Kumar, et al.  \"Parasitology.\"  141, \"Vertical transmission of Tetracapsuloides bryosalmonae (Myxozoa), the causative agent of salmonid proliferative kidney disease.\" 482 (2014a)","DOI":"10.1017\/S0031182013001650"},{"key":"2","doi-asserted-by":"crossref","unstructured":"A. Abd Elfattah, G. Kumar, H. 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Hedrick  \"Journal of Fish Biology.\"  30, \"Seasonal occurrence of the infectious stage of proliferative kidney disease (PKD) and resistance of rainbow trout, Salmo gairdneri Richardson, to reinfection.\" 477 (1987)","DOI":"10.1111\/j.1095-8649.1987.tb05771.x"},{"key":"16","doi-asserted-by":"crossref","unstructured":"B. Gorgoglione, M. H. Kotob, El-Matbouli M.,  \"Journal of Invertebrate Pathology.\"  140, \"Migrating zooids allow the dispersal of Fredericella sultana (Bryozoa) to escape from unfavourable conditions and further spreading of Tetracapsuloides bryosalmonae.\" 97 (2016)","DOI":"10.1016\/j.jip.2016.08.010"},{"key":"17","doi-asserted-by":"crossref","unstructured":"D. S. Grabner  and El-Matbouli M.  \"Diseases of Aquatic Organisms.\"  79, \"Transmission of Tetracapsuloides bryosalmonae (Myxozoa: Malacosporea) to Fredericella sultana (Bryozoa: Phylactolaemata) by various fish species.\" 133 (2008)","DOI":"10.3354\/dao01894"},{"key":"18","doi-asserted-by":"crossref","unstructured":"D. S. Grabner  and El-Matbouli M.  \"Veterinary Parasitology.\"  165, \"Comparison of the susceptibility of brown trout (Salmo trutta) and four rainbow trout (Oncorhynchus mykiss) strains to the myxozoan Tetracapsuloides bryosalmonae, the causative agent of proliferative kidney disease (PKD).\" 200 (2009)","DOI":"10.1016\/j.vetpar.2009.07.028"},{"key":"19","doi-asserted-by":"crossref","unstructured":"D. S. Grabner  and El-Matbouli M.  \"Diseases of Aquatic Organisms.\"  90, \"Tetracapsuloides bryosalmonae (Myxozoa: Malacosporea) portal of entry into the fish host.\" 197 (2010)","DOI":"10.3354\/dao02236"},{"key":"20","doi-asserted-by":"crossref","unstructured":"S. L. Hallett  and J. L. Bartholomew  \"Fish parasites: Pathobiology and protection.\"  \"Myxobolus cerebralis and Ceratomyxa shasta.\" 131 (2012)","DOI":"10.1079\/9781845938062.0131"},{"key":"21","doi-asserted-by":"crossref","unstructured":"S. L. Hallett, A. Hartigan, S. D. Atkinson,  \"Myxozoan Evolution, Ecology and Development.\"  \"Myxozoans on the move: Dispersal modes, exotic species and emerging diseases.\" 343 (2015)","DOI":"10.1007\/978-3-319-14753-6_18"},{"key":"23","doi-asserted-by":"crossref","unstructured":"H. Hartikainen, A. Waeschenbach, E. W\u00f6ss, et al.  \"Zoological Journal of the Linnean Society.\"  168, \"Divergence and species discrimination in freshwater bryozoans (Bryozoa: Phylactolaemata): diversification of freshwater bryozoans.\" 61 (2013)","DOI":"10.1111\/zoj.12025"},{"key":"24","doi-asserted-by":"crossref","unstructured":"R. P. Hedrick, D. V. Baxa, P. De Kinkelin, et al.  \"Parasitology Research.\"  92, \"Malacosporean-like spores in urine of rainbow trout react with antibody and DNA probes to Tetracapsuloides bryosalmonae.\" 81 (2004)","DOI":"10.1007\/s00436-003-0986-3"},{"key":"25","doi-asserted-by":"crossref","unstructured":"R. P. Hedrick, M. L. Kent, R. Rosemark, et al.  \"Bulletin of the European Association of Fish Pathologists (Denmark).\"  4, \"Occurrence of proliferative kidney disease (PKD) among Pacific salmon and steelhead trout.\" 3 (1984)","DOI":"10.1111\/j.1749-7345.1984.tb00166.x"},{"key":"26","unstructured":"R. P. Hedrick, M. L. Kent, C. E. Smith,  \"U.S. Fish and Wildlife Publications.\"  136, \"Proliferative kidney disease in salmonid fishes.\" (1986)"},{"key":"27","doi-asserted-by":"crossref","unstructured":"R. P. Hedrick, E. Macconnell, P. De Kinkelin,  \"Annual Review of Fish Diseases.\"  3, \"Proliferative kidney disease of salmonid fish.\" 277 (1993)","DOI":"10.1016\/0959-8030(93)90039-E"},{"key":"28","doi-asserted-by":"crossref","unstructured":"M. Henderson  and B. Okamura  \"Proceedings of the Royal Society of London. Series B: Biological Sciences.\"  271, \"The phylogeography of salmonid proliferative kidney disease in Europe and North America.\" 1729 (2004)","DOI":"10.1098\/rspb.2004.2677"},{"key":"29","doi-asserted-by":"crossref","unstructured":"S. L. Hill  and B. Okamura  \"Parasitology.\"  134, \"Endoparasitism in colonial hosts: Patterns and processes.\" 841 (2007)","DOI":"10.1017\/S0031182007002259"},{"key":"30","doi-asserted-by":"publisher","unstructured":"P. R. Hutchins, A. J. Sepulveda, H. Hartikainen, et al.  \"Ecosphere.\"  12, \"Exploration of the 2016 Yellowstone River fish kill and proliferative kidney disease in wild fish populations.\" e03436 (2021)","DOI":"10.1002\/ecs2.3436"},{"key":"31","unstructured":"M. L. Kent, L. Margolis, D. J. Whitaker, et al.  \"Folia Parasitologica.\"  41, \"Review of Myxosporea of importance in salmonid fisheries and aquaculture in British Columbia.\" 27 (1994)"},{"key":"32","doi-asserted-by":"crossref","unstructured":"M. L. Kent  and R. P. Hedrick  \"Diseases of Aquatic Organisms.\"  1, \"Development of the PKX myxosporean in rainbow trout Salmo gairdneri.\" 169 (1986)","DOI":"10.3354\/dao001169"},{"key":"33","doi-asserted-by":"crossref","unstructured":"M. L. Kent  and R. P. Hedrick  \"Journal of Protozoology.\"  32, \"PKX, the causative agent of proliferative kidney disease (PKD) in Pacific salmonid fishes and its affinities with the Myxozoa.\" 254 (1985)","DOI":"10.1111\/j.1550-7408.1985.tb03047.x"},{"key":"34","doi-asserted-by":"crossref","unstructured":"G. Kumar, Abd-Elfattah A., M. Saleh, et al.  \"Diseases of Aquatic Organisms.\"  107, \"Fate of Tetracapsuloides bryosalmonae (Myxozoa) after infection of brown trout Salmo trutta and rainbow trout Oncorhynchus mykiss.\" 9 (2013)","DOI":"10.3354\/dao02665"},{"key":"35","unstructured":"M. Longshaw, S. W. Feist, E. U. Canning, et al.  \"Bulletin of the European Association of Fish Pathologists.\"  19, \"First identification of PKX in bryozoans from the United Kingdom - molecular evidence.\" 146 (1999)"},{"key":"36","doi-asserted-by":"crossref","unstructured":"M. Longshaw, Le Deuff R. M., A. F. Harris, et al.  \"Journal of Fish Diseases.\"  25, \"Development of proliferative kidney disease in rainbow trout, Oncorhynchus mykiss (Walbaum), following short-term exposure to Tetracapsula bryosalmonae infected bryozoans.\" 443 (2002)","DOI":"10.1046\/j.1365-2761.2002.00353.x"},{"key":"37","doi-asserted-by":"crossref","unstructured":"E. Macconnell  and J. E. Peterson  \"Journal of Aquatic Animal Health.\"  4, \"Proliferative kidney disease in feral Cutthroat Trout from a remote Montana Reservoir: A first case.\" 182 (1992)","DOI":"10.1577\/1548-8667(1992)004<0182:PKDIFC>2.3.CO;2"},{"key":"38","doi-asserted-by":"crossref","unstructured":"T. G. Marsh  and T. S. Wood  \"Bryozoan Studies 2001: Proceedings of the 12th International Bryozoology Association.\"  \"Results of a freshwater bryozoan survey in the Pacific Northwestern United States.\" 207 (2002)","DOI":"10.1201\/9781003762379-29"},{"key":"39","doi-asserted-by":"crossref","unstructured":"C. McGurk, D. J. Morris, N. A. Auchinachie, et al.  \"Veterinary Parasitology.\"  135, \"Development of Tetracapsuloides bryosalmonae (Myxozoa: Malacosporea) in bryozoan hosts (as examined by light microscopy) and quantitation of infective dose to rainbow trout (Oncorhynchus mykiss).\" 249 (2006)","DOI":"10.1016\/j.vetpar.2005.07.022"},{"key":"40","doi-asserted-by":"crossref","unstructured":"D. C. Morris, D. J. Morris, A. Adams,  \"Journal of Fish Diseases.\"  25, \"Molecular evidence of release of Tetracapsula bryosalmonae, the causative organism of proliferative kidney disease from infected salmonids into the environment.\" 501 (2002)","DOI":"10.1046\/j.1365-2761.2002.00352.x"},{"key":"41","doi-asserted-by":"crossref","unstructured":"D. J. Morris  and A. Adams  \"Journal of Parasitology.\"  92, \"Proliferative, presaccular stages of Tetracapsuloides bryosalmone (Myxozoa: Malacosporea) within the invertebrate host Fredericella sultana (Bryozoa: Phylactolaemata).\" 984 (2006)","DOI":"10.1645\/GE-868R.1"},{"key":"42","doi-asserted-by":"crossref","unstructured":"D. J. Morris, A. Adams, R. H. Richards,  \"Journal of Aquatic Animal Health.\"  9, \"Studies of the PKX parasite in rainbow trout via immunohistochemistry and immunogold electron microscopy.\" 256 (1997)","DOI":"10.1577\/1548-8667(1997)009<0265:SOTPPI>2.3.CO;2"},{"key":"43","doi-asserted-by":"crossref","unstructured":"D. J. Morris, A. Adams, R. H. Richards,  \"Parasitology Research.\"  86, \"In situ hybridisation identifies the gill as a portal of entry for PKX (Phylum Myxozoa), the causative agent of proliferative kidney disease in salmonids.\" 950 (2000)","DOI":"10.1007\/PL00008525"},{"key":"44","doi-asserted-by":"publisher","unstructured":"B. Okamura, C. L. Anderson, M. Longshaw, et al.  \"Journal of Parasitology.\"  87, \"Patterns of Occurrence and 18S rDNA Sequence Variation of PKX (Tetracapsula bryosalmonae), the Causative Agent of Salmonid Proliferative Kidney Disease.\" 379 (2001)","DOI":"10.2307\/3285055"},{"key":"45","doi-asserted-by":"crossref","unstructured":"B. Okamura  and T. S. Wood  \"Journal of Fish Diseases.\"  25, \"Bryozoans as hosts for Tetracapsula bryosalmonae, the PKX organism.\" 469 (2002)","DOI":"10.1046\/j.1365-2761.2002.00376.x"},{"key":"46","doi-asserted-by":"crossref","unstructured":"T. J. Oredalen, T. A. Mo, A. Jenkins, et al.  \"Environmental DNA.\"  4, \"Use of environmental DNA to detect the myxozoan endoparasite Tetracapsuloides bryosalmonae in large Norwegian lakes.\" 1294 (2022)","DOI":"10.1002\/edn3.338"},{"key":"47","doi-asserted-by":"crossref","unstructured":"O. Palenzuela, G. Trobridge, J. L. Bartholomew,  \"Diseases of Aquatic Organisms.\"  36, \"Development of a polymerase chain reaction diagnostic assay for Ceratomyxa shasta, a myxosporean parasite of salmonid fish.\" 45 (1999)","DOI":"10.3354\/dao036045"},{"key":"48","doi-asserted-by":"crossref","unstructured":"H. Schmidt-Posthaus, K. Bettge, U. Forster, et al.  \"Diseases of Aquatic Organisms.\"  97, \"Kidney pathology and parasite intensity in rainbow trout Oncorhynchus mykiss surviving proliferative kidney disease: Time course and influence of temperature.\" 207 (2012)","DOI":"10.3354\/dao02417"},{"key":"49","doi-asserted-by":"crossref","unstructured":"C. E. Smith, J. K. Morrison, H. W. Ramsey, et al.  \"Journal of Fish Diseases.\"  7, \"Proliferative kidney disease: First reported outbreak in North America.\" 207 (1984)","DOI":"10.1111\/j.1365-2761.1984.tb00925.x"},{"key":"50","doi-asserted-by":"publisher","unstructured":"A. Sudhagar, G. Kumar, El-Matbouli M.,  \"Pathogens.\"  9, \"The Malacosporean myxozoan parasite Tetracapsuloides bryosalmonae: A threat to wild salmonids.\" 16 (2019)","DOI":"10.3390\/pathogens9010016"},{"key":"51","doi-asserted-by":"crossref","unstructured":"M. I. Taticchi, A. Gustinelli, M. L. Fioravanti, et al.  \"Italian Journal of Zoology.\"  71, \"Is the worm-like organism found in the statoblasts of Plumatella fungosa (Bryozoa, Phylactolaemata) the vermiform phase of Tetracapsuloides bryosalmonae (Myxozoa, Malacosporea)?\" 143 (2004)","DOI":"10.1080\/11250000409356565"},{"key":"52","doi-asserted-by":"crossref","unstructured":"S. Tops, H. L. Hartikainen, B. Okamura,  \"International Journal for Parasitology.\"  39, \"The effects of infection by Tetracapsuloides bryosalmonae (Myxozoa) and temperature on Fredericella sultana (Bryozoa).\" 1003 (2009)","DOI":"10.1016\/j.ijpara.2009.01.007"},{"key":"53","doi-asserted-by":"crossref","unstructured":"S. Tops, W. Lockwood, B. Okamura,  \"Diseases of Aquatic Organisms.\"  70, \"Temperature-driven proliferation of Tetracapsuloides bryosalmonae in bryozoan hosts portends salmonid declines.\" 227 (2006)","DOI":"10.3354\/dao070227"},{"key":"55","doi-asserted-by":"crossref","unstructured":"T. Wahli, D. Bernet, P. A. Steiner, et al.  \"Aquatic Sciences.\"  69, \"Geographic distribution of Tetracapsuloides bryosalmonae infected fish in Swiss rivers: An update.\" 3 (2007)","DOI":"10.1007\/s00027-006-0843-4"},{"key":"56","doi-asserted-by":"crossref","unstructured":"T. Wahli, R. Knuesel, D. Bernet, et al.  \"Journal of Fish Diseases.\"  25, \"Proliferative kidney disease in Switzerland: Current state of knowledge.\" 491 (2002)","DOI":"10.1046\/j.1365-2761.2002.00401.x"},{"key":"57","doi-asserted-by":"crossref","unstructured":"K. Waldner, T. Bechter, S. Auer, et al.  \"Ecology of Freshwater Fish.\"  29, \"A brown trout (Salmo trutta) population faces devastating consequences due to proliferative kidney disease and temperature increase: A case study from Austria.\" 465 (2020)","DOI":"10.1111\/eff.12528"},{"key":"58","doi-asserted-by":"crossref","unstructured":"T. S. Wood,  \"Zootaxa.\"  5200, \"Phylactolaemate bryozoans at the zoological survey of India and a taxonomic key to Indian phylactolaemata.\" 401 (2022)","DOI":"10.11646\/zootaxa.5200.5.1"},{"key":"59","doi-asserted-by":"crossref","unstructured":"T. S. Wood  and B. T. Backus  \"Hydrobiologia.\"  237, \"Differentiation of North American and European forms of Fredericella sultana (Blumenbach) (Ectoprocta: Phylactolaemata).\" 185 (1992)","DOI":"10.1007\/BF00005850"},{"key":"22","doi-asserted-by":"crossref","unstructured":"S. L. Hallett, R. A. Ray, C. N. Hurst, et al.  \"Applied and Environmental Microbiology.\"  78, \"Density of the waterborne parasite Ceratomyxa shasta and its biological effects on salmon.\" 3724 (2012)","DOI":"10.1128\/AEM.07801-11"},{"key":"5","doi-asserted-by":"crossref","unstructured":"J. R. Barta, D. S. Martin, P. A. Liberator, et al.  \"Journal of Parasitology.\"  83, \"Phylogenetic relationships among eight Eimeria species infecting domestic fowl inferred using complete small subunit ribosomal DNA sequences.\" 262 (1997)","DOI":"10.2307\/3284453"}],"container-title":["Journal of Parasitology"],"original-title":[],"deposited":{"date-parts":[[2026,10,5]],"date-time":"2026-10-05T21:14:54Z","timestamp":1791234894000},"score":1,"resource":{"primary":{"URL":"https:\/\/bioone.org\/journals\/journal-of-parasitology\/volume-112\/issue-2\/25-47\/The-Salmonid-Oncorhynchus-mykiss-and-Bryozoan-Fredericella-borealis-Serve-as\/10.1645\/25-47.full"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2026,3,9]]},"references-count":59,"journal-issue":{"issue":"2","published-online":{"date-parts":[[2026,3,1]]}},"URL":"https:\/\/doi.org\/10.1645\/25-47","relation":{},"ISSN":["0022-3395","1937-2345"],"issn-type":[{"value":"0022-3395","type":"print"},{"value":"1937-2345","type":"electronic"}],"subject":[],"published":{"date-parts":[[2026,3,9]]}}}