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Myxosporean parasites of marine fishes: their distribution in the world's oceans

Published online by Cambridge University Press:  12 September 2014

K. MACKENZIE  and
C. KALAVATI
K. MACKENZIE*
Affiliation:
School of Biological Sciences (Zoology), University of Aberdeen, Tillydrone Avenue, Aberdeen AB24 2TZ, Scotland, UK
C. KALAVATI
Affiliation:
Marine Biology Laboratory, Opp. A.U. Post Office, Andhra University, Visakhapatnam 530 003, Andhra Pradesh, India
*
* Corresponding author: School of Biological Sciences (Zoology), University of Aberdeen, Tillydrone Avenue, Aberdeen AB24 2TZ, Scotland, UK. E-mail: k.mackenzie@abdn.ac.uk
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Summary

Myxosporeans are among the most common parasites of marine fish. Their economic importance is mainly as pathogens of both wild and farmed fish, but they have also been used as biological tags in population studies of their fish hosts. Here we review the literature and show the distribution of different families of Myxosporea infecting marine fishes in the world's oceans – the North Atlantic, South Atlantic, North Pacific, South Pacific and Indian. We also analyse their distribution in different orders of marine fishes. New families, genera and species of marine Myxosporea are continually being described and many more await description. Some regions, in particular the North Atlantic, have been more thoroughly investigated than others, so the analyses we present may not reflect the true distributions and we acknowledge that these may change considerably as other regions are investigated more fully. The distribution of myxosporean families in different taxonomic groups of marine fishes can indicate phylogenetic relationships between parasite and host and suggest the origins of different myxosporean taxa. We present some examples, while recognizing that new molecular information on phylogenetic relationships within the Myxozoa will lead to major changes in classification.

Keywords

Myxosporeansmarine fishesdistributionoceans

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Type
Review Article
Information
Parasitology , Volume 141 , Issue 13 , November 2014 , pp. 1709 - 1717
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Copyright © Cambridge University Press 2014 

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References

REFERENCES

Alama-Bermejo, G., Cuadrado, M., Raga, J. A. and Holzer, A. S. (2009). Morphological and molecular redescription of the myxozoan Unicapsula pflugfelderi Schubert, Sprague & Reinboth 1975 from two teleost hosts in the Mediterranean. A review of the genus Unicapsula Davis 1924. Journal of Fish Diseases 32, 335–350.CrossRefGoogle ScholarPubMed
Álvarez-Pelliterro, P. and Sitjá-Bobadilla, A. (1993). Pathology of Myxosporea in marine fish culture. Diseases of Aquatic Organisms 17, 229–238.Google Scholar
Bartošova, P., Freeman, M. A., Yokoyama, H., Caffara, M. and Fiala, I. (2011). Phylogenetic position of Sphaerospora testicularis and Latyspora scomberomori n. gen. n. sp. (Myxozoa) within the marine urinary clade. Parasitology 138, 381–393.Google Scholar
Burger, M. A. A. and Adlard, R. D. (2010). Four new species of Kudoa meglitsch, 1947 (Myxosporea: Multivalvulida) from Australia with recommendations for species descriptions in the Kudoidae). Parasitology 137, 793–814.Google Scholar
Campbell, N. (2005). The myxosporean parasitofauna of the Atlantic horse mackerel, Trachurus trachurus L. in the North-East Atlantic Ocean and Mediterranean Sea. Acta Parasitologica 50, 97–101.Google Scholar
Diamant, A. (1997). Fish-to-fish transmission of a marine myxosporean. Diseases of Aquatic Organisms 30, 99–105.CrossRefGoogle Scholar
Eiras, J. C. (2002). Synopsis of the species of the genus Henneguya Thélohan, 1892 (Myxozoa: Myxosporea: Myxobolidae). Systematic Parasitology 52, 43–54.CrossRefGoogle ScholarPubMed
Eiras, J. C. (2006). Synopsis of the species of Ceratomyxa Thélohan, 1892 (Myxozoa: Myxosporea: Ceratomyxidae). Systematic Parasitology 65, 49–71.CrossRefGoogle ScholarPubMed
Eiras, J. C., Molnár, K. and Lu, Y. S. (2005). Synopsis of the species of the genus Myxobolus Bütschli, 1882 (Myxozoa: Myxosporea: Myxobolidae). Systematic Parasitology 61, 1–46.CrossRefGoogle Scholar
Eiras, J. C., Saraiva, A., Cruz, C. F., Santos, M. J. and Fiala, I. (2011). Synopsis of the species of Myxidium Bütschli, 1882 (Myxozoa: Myxosporea: Bivalvulida). Systematic Parasitology 80, 81–116.Google Scholar
Eiras, J. C., Lu, Y. S., Gibson, D. I., Fiala, I., Saraiva, A., Cruz, C. and Santos, M. J. (2012). Synopsis of the species of Chloromyxum Mingazinni, 1890 (Myxozoa: Myxosporea: Chloromyxidae). Systematic Parasitology 83, 203–225.Google Scholar
Eiras, J. C., Saraiva, A. and Cruz, C. (2014 a). Synopsis of the species of Kudoa Meglitsch, 1947 (Myxozoa: Myxosporea: Multivalvulida). Systematic Parasitology 87, 153–180.CrossRefGoogle ScholarPubMed
Eiras, J. C., Zhang, J. and Molnar, K. (2114 b). Synopsis of the species of Myxobolus Bütschli, 1882 (Myxozoa: Myxosporea: Myxobolidae). Systematic Parasitology 88, 11–36.CrossRefGoogle Scholar
Feist, S. W. (1997). Pathogenicity of renal myxosporeans of fish. Bulletin of the European Association of Fish Pathologists 17, 209–214.Google Scholar
Fiala, I. (2006). The phylogeny of Myxosporea (Myxozoa) based on small subunit ribosomal RNA gene analysis. International Journal for Parasitology 36, 1521–1534.Google Scholar
Fiala, I. and Bartošová, P. (2010). History of myxozoan character evolution on the basis of rDNA and EF-2 data. BMC Evolutionary Biology 10, article no. 228, 13.CrossRefGoogle ScholarPubMed
Gleeson, R. J. and Adlard, R. D. (2011). Morphological and genetic analysis of three new species of Ceratomyxa Thélohan, 1892 (Myxozoa: Myxosporea) from carcharhinid sharks off Australia. Systematic Parasitology 80, 117–124.CrossRefGoogle ScholarPubMed
Gleeson, R. J. and Adlard, R. D. (2012). Phylogenetic relationships amongst Chloromyxum Mingazinni, 1890 (Myxozoa: Myxosporea), and the description of six novel species from Australian elasmobranchs. Parasitology International 61, 267–274.CrossRefGoogle Scholar
Gleeson, R. J., Bennett, M. B. and Adlard, R. D. (2010). First taxonomic description of multivalvulidan parasites from elasmobranchs: Kudoa hemiscylli n. sp. and Kudoa carcharhini n. sp (Myxosporea: Multivalvulida). Parasitology 137, 1885–1898.Google Scholar
Gunter, N. L. and Adlard, R. D. (2008). Bivalvulidan (Myxozoa: Myxosporea) parasites of damselfishes with description of twelve novel species from Australia's Great Barrier Reef. Parasitology 135, 1165–1178.Google Scholar
Gunter, N. L. and Adlard, R. D. (2009). Seven new species of Ceratomyxa from the gall bladders of serranids from the Great Barrier Reef, Australia. Systematic Parasitology 73, 1–11.CrossRefGoogle ScholarPubMed
Gunter, N. L. and Adlard, R. (2010). The demise of Leptotheca Thélohan, 1895 (Myxozoa: Myxosporea: Ceratomyxidae) and assignment of its species to Ceratomyxa Thélohan, 1892 (Myxosporea: Ceratomyxidae) Ellipsomyxa Køie, 2003 (Myxosporea: Ceratomyxidae), Myxobolus Bütschli, 1882 and Sphaerospora Thélohan, 1892 (Myxosporea: Sphaerosporidae). Systematic Parasitology 75, 81–104.CrossRefGoogle ScholarPubMed
Gunter, N. L., Whipps, C. M. and Adlard, R. D. (2009). Ceratomyxa (Myxozoa: Bivalvulida): robust taxon or genus of convenience? International Journal for Parasitology 39, 1395–1405.CrossRefGoogle ScholarPubMed
Gunter, N. L., Burger, M. A. A. and Adlard, R. D. (2010). Morphometric and molecular characterization of four new Ceratomyxa species (Myxosporea: Bivalvulida: Ceratomyxidae) from fishes off Lizard Island, Australia. Folia Parasitologica 57, 1–10.CrossRefGoogle ScholarPubMed
Heiniger, H. and Adlard, R. D. (2013 a). Molecular identification of cryptic species of Ceratomyxa Thélohan, 1892 (Myxosporea: Multivalvulida) including the description of eight novel species from apogonid fishes (Perciformes: Apogonidae) from Australian waters. Acta Parasitologica 58, 342–360.CrossRefGoogle Scholar
Heiniger, H. and Adlard, R. D. (2013 b). Host specificity and local infection dynamics of Kudoa leptacanthae n. sp. (Multivalvulida: Kudoidae) from the pericardial cavity of two Zoramia spp. (Perciformes: Apogonidae) at Lizard Island Lagoon, Queensland, Australia. Parasitology International 61, 697–706.Google Scholar
Heiniger, H. and Adlard, R. D. (2014). Relatedness of novel species of Myxidium Bütschli, 1882, Zschokkella Auerbach, 1910 and Ellipsomyxa Køie, 2003 (Myxosporea: Bivalvulida) from the gall bladders of marine fishes (Teleostei) from Australian waters. Systematic Parasitology 87, 47–72.Google Scholar
Heiniger, H., Gunter, N. L. and Adlard, R. D. (2008). Relationships between four novel ceratomyxid parasites from the gall bladders of labrid fishes from Heron Island, Queensland, Australia. Parasitology International 57, 158–165.Google Scholar
Heiniger, H., Gunter, N. L. and Adlard, R. D. (2011). Re-establishment of the family Coccomyxidae and description of five novel species of Auerbachia and Coccomyxa (Myxosporea: Bivalvulida) parasites from Australian fishes. Parasitology 138, 501–515.Google Scholar
Heiniger, H., Cribb, T. H. and Adlard, R. D. (2013). Intra-specific variation of Kudoa spp. (Myxosporea: Multivalvulida) from apogonid fishes (Perciformes), including the description of two new species, K. cheilodipteri n. sp.and K. cookie n. sp. from Australian waters. Systematic Parasitology 84, 193–215.Google Scholar
Henning, S. S., Hoffman, L. C. and Manley, M. (2013). A review of Kudoa-induced myoliquefaction of marine fish species in South Africa and other countries. South African Journal of Science 109, 1–5.Google Scholar
Kabata, Z. (1967). Whiting Stocks and their Gall-bladder Parasites in British Waters. Marine Research  No. 2, 11pp.Google Scholar
Kabata, Z. and Whitaker, D. J. (1985). Parasites as a limiting factor in exploitation of Pacific whiting, Merluccius productus . Marine Fisheries Review 47, 55–59.Google Scholar
Karlsbakk, E. and Køie, M. (2012). The marine myxosporean Sigmomyxa sphaerica (Thélohan, 1895) gen. n., comb. n. (syn. Myxidium sphaericum) from garfish (Belone belone (L.)) uses the polychaete Nereis pelagica as invertebrate host. Parasitology Research 110, 211–218.Google Scholar
Kaur, H. and Singh, R. (2012). A synopsis of the species of Myxobolus Bütschli, 1882 (Myxozoa: Bivalvulida) parasitizing Indian fishes and a revised dichotomous key to myxosporean genera. Systematic Parasitology 81, 17–37.Google Scholar
Kent, M. L., Margolis, L. and Corliss, J. O. (1994). The demise of a class of protists: taxonomic and nomenclatural revisions proposed for the protest phylum Myxozoa Grassé, 1970. Canadian Journal of Zoology 72, 932–937.CrossRefGoogle Scholar
Kent, M. L., Andree, K. B., Bartholomew, J. L., El-Matbouli, M., Desser, S. S., Devlin, R. H., Feist, S. W., Hedrick, R. P., Hoffmann, R. W., Khattra, J., Hallett, S. L., Lester, R. J. G., Longshaw, M., Palenzuela, O., Siddall, M. E. and Xiao, C. (2001). Recent advances in our knowledge of the Myxozoa. Journal of Eukaryotic Microbiology 48, 395–413.CrossRefGoogle ScholarPubMed
Khan, R. A. and Tuck, C. (1995). Parasites as biological indicators of stocks of Atlantic cod (Gadus morhua) off Newfoundland, Canada. Canadian Journal of Fisheries and Aquatic Sciences 52(Suppl. 1), 195–201.CrossRefGoogle Scholar
Køie, M. (2003 a). Ellipsomyxa gobii gen. et sp. n. (Myxozpa: Ceratomyxidae) in the common goby Pomatoschistus microps (Teleostei: Gobiidae) from Denmark. Folia Parasitologica 50, 269–271.Google Scholar
Køie, M., Whipps, C. M. and Kent, M. L. (2004). Ellipsomyxa gobii (Myxozoa: Ceratomyxidae) in the common goby Pomatoschistus microps (Teleostei: Gobiidae) uses Nereis spp. (Annelida: Polychaeta) as invertebrate host. Folia Parasitologia 51, 14–18.CrossRefGoogle Scholar
Køie, M., Karlsbakk, E. and Nylund, A. (2007). A new genus Gadimyxa with three new species (Myxozoa: Parvicapsulidae) parasitic in marine fish (Gadidae) and the two-host life cycle of Gadimyxa atlantica n. sp. Journal of Parasitology 93, 1459–1467.Google Scholar
Køie, M., Karlsbakk, E. and Nylund, A. (2008). The marine herring myxozoan Ceratomyxa auerbachii (Myxozoa: Ceratomyxidae) uses Chone infundibuliformis (Annelida: Polychaeta: Sabellidae) as invertebrate host. Folia Parasitologica 55, 100–104.Google Scholar
Køie, M., Karlsbakk, E., Einen, A.-C. B. and Nylund, A. (2013). A parvicapsulid (Myxozoa) infecting Sprattus sprattus and Clupea harengus (Clupeidae) in the Northeast Atlantic uses Hydroides norvegicus (Serpulidae) as invertebrate host. Folia Parasitologica 60, 149–154.Google Scholar
Kovaleva, A. A. (1988). Suborder Sphaeromyxina (Myxosporea, Bivalvulida), its structure and position in myxosporidian system. Zoologicheskii Zhurnal 67, 1616–1620.Google Scholar
Lom, J. and Dyková, I. (1992). Protozoan Parasites of Fishes. Developments in Aquaculture and Fisheries Science, vol. 26. Elsevier, Amsterdam.Google Scholar
Lom, J. and Dyková, I. (2006). Myxozoan genera: definition and notes on taxonomy, life-cycle terminology and pathogenic species. Folia Parasitologica 53, 1–36.Google Scholar
Larsen, G., Hemmingsen, W., MacKenzie, K. and Lysne, D. A. (1997). A population study of cod, Gadus morhua L., in northern Norway using otolith structure and parasite tags. Fisheries Research 32, 13–20.CrossRefGoogle Scholar
MacKenzie, K., Kalavati, C., Gaard, M. and Hemmingsen, W. (2005). Myxosporean gall bladder parasites of gadid fishes in the North Atlantic: their geographical distributions and an assessment of their economic importance in fisheries and mariculture. Fisheries Research 76, 454–465.Google Scholar
Maeno, Y. and Sorimachi, M. (1992). Skeletal abnormalities of fishes caused by parasitism of Myxosporea. In Control of Disease in Mariculture (ed. Svrjcek, R. S.), pp. 113–118. NOAA Technical Report NMFS 111. National Oceanic and Atmospheric Administration, USA.Google Scholar
Markiv, M. E. and Wolf, K. (1983). Myxosoma cerebralis (Myxozoa: Myxosporea) etiologic agent of salmonid whirling disease requires tubificid worms (Annelida: Oligochaeta) in its life cycle. Journal of Protozoology 30, 561–564.Google Scholar
Miller, T. L. and Adlard, R. D. (2013). Unicapsula species (Myxosporea: Trilosporidae) of Australian marine fishes, including the description of Unicapsula andersenae n. sp. in five teleost families off Queensland, Australia. Parasitology Research 112, 2945–2957.Google Scholar
Moran, J. D. W., Whitaker, D. J. and Kent, M. L. (1999). A review of the myxosporean genus Kudoa Meglitsch, 1947, and its impact on the international aquaculture industry and commercial fisheries. Aquaculture 172, 163–196.Google Scholar
Nesnidal, M. P., Maximilian, P., Helmkampf, M., Bruchhaus, I., El-Matbouli, M. and Hausdorf, B. (2013). Agent of whirling disease meets orphan worm: phylogenetic analyses firmly place Myxozoa in Cnidaria. PLoS ONE 8, article no. e54576.Google Scholar
Palenzuela, O. (2006). Mixozoan infections in Mediterranean mariculture. Parassitologia 48, 27–29.Google ScholarPubMed
Rangel, L. F., Santos, M. J., Cech, G. and Székely, C. (2009). Morphology, molecular data, and development of Zschokkella mugilis (Myxosporea: Bivalvulida) in a polychaete alternate host. Journal of Parasitology 95, 561–569.Google Scholar
Rangel, L. F., Gibson, D. I. and Santos, M. J. (2014). Synopsis of the species of the genus Myxobilatus Davis, 1944 (Myxozoa: Myxosporea: Myxobilatidae). Systematic Parasitology 87, 187–198.Google Scholar
Redondo, M. J., Palenzuela, O., Riaza, A., Macías, Á. and Álvarez-Pelliterro, P. (2002). Experimental transmission of Enteromyxum scophthalmi (Myxozoa), an enteric parasite of turbot Scophthalmus maximus . Journal of Parasitology 88, 482–488.Google Scholar
Siddall, M. E., Martin, D. S., Bridge, D., Desser, S. S. and Cone, D. K. (1995). The demise of a phylum of protists: phylogeny of the Myxozoa and other parasitic cnidaria. Journal of Parasitology 81, 961–967.Google Scholar
Sindermann, C. J. (1957). Diseases of fishes of the western North Atlantic. VI. Geographic discontinuity of myxosporidiosis in immature herring from the Gulf of Maine. Maine Department of Sea and Shore Fisheries Research Bulletin No. 29, 1–20.Google Scholar
Smothers, J. F., von Dohlen, C. D., Smith, L. H. Jr. and Spall, R. D. (1994). Molecular evidence that the myxozoan protists are metazoans. Science 265, 1719–1721.Google Scholar
Whipps, C. M. (2011). Interrenal disease in bluegills (Lepomis macrochirus) caused by a new genus and species of myxozoan. Journal of Parasitology 97, 1159–1165.Google Scholar
Whipps, C. M., Grossel, G., Adlard, R. D., Yokoyama, H., Bryant, M. S., Munday, B. L. and Kent, M. L. (2004). Phylogeny of the multivalvulidae (Myxozoa: Myxosporea) based on comparative ribosomal DNA sequence analysis. Journal of Parasitology 90, 618–622.Google Scholar
Yasuda, H., Ooyama, T., Iwata, K., Tun, T., Yokoyama, H. and Ogawa, K. (2002). Fish-to-fish transmission of Myxidium spp. (Myxozoa) in cultured tiger puffer suffering from emaciation disease. Fish Pathology 37, 29–33.Google Scholar
Zhao, Y., Zhou, Y., Kent, M. L. and Whipps, C. M. (2008). Replacement of the preoccupied name Davisia Laird, 1953 and description of a new myxozoan species (Myxosporea: Sinuolineidae) from Sebastiscus marmoratus (Cuvier, 1829) in the East China Sea. Journal of Parasitology 94, 269–279.Google Scholar