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Infection dynamics of two renal myxozoans in hatchery reared fry and juvenile Atlantic cod Gadus morhua L.

Published online by Cambridge University Press:  26 May 2010

A. S. HOLZER ,
S. STEWART ,
A. TILDESLEY ,
R. WOOTTEN  and
C. SOMMERVILLE
A. S. HOLZER*
Affiliation:
Institute of Aquaculture, University of Stirling, Stirling FK9 4LA, Scotland, UK Cavanilles Institute of Biodiversity and Evolutionary Biology, University of Valencia, P.O. Box 22085, 46071Valencia, Spain
S. STEWART
Affiliation:
Institute of Aquaculture, University of Stirling, Stirling FK9 4LA, Scotland, UK
A. TILDESLEY
Affiliation:
Institute of Aquaculture, University of Stirling, Stirling FK9 4LA, Scotland, UK
R. WOOTTEN
Affiliation:
Institute of Aquaculture, University of Stirling, Stirling FK9 4LA, Scotland, UK
C. SOMMERVILLE
Affiliation:
Institute of Aquaculture, University of Stirling, Stirling FK9 4LA, Scotland, UK
*
*Corresponding author: Holzer, Cavanilles Institute of Biodiversity and Evolutionary Biology, University of Valencia, P.O. Box 22085, 46071Valencia, Spain. Tel: +34 9635 43685. Fax: +34 9635 43733. E-mail: astrid.holzer@uv.es
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Summary

In order to study the infection dynamics of 2 renal myxozoans, Zschokkella hildae Auerbach, 1910 and Gadimyxa atlanticaKøie, Karlsbakk and Nylund, 2007 in cultured Atlantic cod, Gadus morhua L. aged 3–19 months, a specific single-round PCR assay and a double-label in situ hybridization protocol were developed. The results demonstrated that the 2 myxozoans show spatial separation of their development with regard to spore formation inside the renal tubules versus the collecting ducts and ureters, as well as temporal separation with Z. hildae proliferating and developing spores only once the G. atlantica infection decreases, despite the presence of both myxozoans in the smallest fry studied. These results strongly suggest within-host competition of the 2 myxozoans with potential suppression of Z. hildae by G. atlantica until G. morhua acquires immunity against G. atlantica. The quantification of the G. atlantica infection inside the renal tubules before and after a 29-day experimental growth performance study using fry from hatcheries with differing filtration systems showed that the intensity of infection with G. atlantica seems to be controlled if prolonged exposure to the myxozoan transmission stages takes place from hatching onwards. Surprisingly, growth rates in the trial were inversely affected suggesting that G. atlantica does not negatively influence cod fry growth performance.

Keywords

MyxozoaGadimyxa atlanticaZschokkella hildaemixed infectionhatchery reareddynamicscompetitioninnate and acquired immunitydouble-label in situ hybridizationPCR
Type
Research Article
Information
Parasitology , Volume 137 , Issue 10 , September 2010 , pp. 1501 - 1513
Copyright
Copyright © Cambridge University Press 2010

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References

REFERENCES

Arthur, J. R. (1984). A survey of the parasites of walleye pollock (Theragara chalcogramma) from the northeastern Pacific Ocean off Canada and a zoogeographical analysis of the parasite fauna of this fish throughout its range. Canadian Journal of Zoology 62, 675–684.CrossRefGoogle Scholar
Aseeva, N. L. (2002). Myxosporidian fauna from the Gadidae in Far Eastern seas. Parazitologiya 36, 167–174.Google Scholar
Bakay, Y. I. and Zubchenko, A. V. (1981). Parasites of roundnose grenadier (Coryphaenoides rupestris) in two areas of the north Atlantic in 1981. Annales Biologiques 38, 200–201.Google Scholar
Bartholomew, J. L., Smith, C. E., Rohover, J. S. and Fryer, J. L. (1989). Characterisation of a host response to the myxosporean parasite Ceratomyxa shasta (Noble), by histology, scanning electron microscopy and immunological techniques. Journal of Fish Diseases 12, 509–522. doi: 10.1111/j.1365-2761.1989.tb00561.x.CrossRefGoogle Scholar
Beamish, F. W. H., Sitja-Bobadilla, A., Jebbink, J. A. and Woo, P. T. K. (1996). Bioenergetic cost of cryptobiosis in fish: rainbow trout Oncorhynchus mykiss infected with Cryptobia salmositica and with an attenuated live vaccine. Diseases of Aquatic Organisms 25, 1–8. doi: 10.3354/dao025001.CrossRefGoogle Scholar
Bruce, M. C., Donnelly, C. A., Alpers, M. P., Galinski, M. R., Barnwell, J. W., Walliker, D. and Day, K. P. (2000). Cross-species interactions between malaria parasites in humans. Science 287, 845–848. doi: 10.1126/science.287.5454.845.CrossRefGoogle ScholarPubMed
Csaba, S. (1976). An unidentifiable extracellular sporozoan parasite from the blood of the carp. Parasitologia Hungarica 9, 21–24.Google Scholar
Feist, S. W., Peeler, E. J., Gardiner, R., Smith, E. and Longshaw, M. (2002). Proliferative kidney disease and renal myxosporidiosis in juvenile salmonids from rivers in England and Wales. Journal of Fish Diseases 25, 451–458. doi: 10.1046/j.1365-2761.2002.00361.x.CrossRefGoogle Scholar
Ferguson, H. W. (1981). The effects of water temperature on the development of proliferative kidney disease in rainbow trout, Salmo gairdneri Richardson. Journal of Fish Diseases 4, 175–177. doi: 10.1017/S0031182009005800.CrossRefGoogle Scholar
Foott, J. S., Harmon, R. and Stone, R. (2004). Effect of water temperature on non-specific immune function and ceratomyxosis in juvenile chinook salmon and steelhead from the Klamath River. California Fish and Game 90, 71–84.Google Scholar
Foott, J. S. and Hedrick, R. P. (1987). Seasonal occurrence of the infectious stage of proliferative kidney disease (PKD) and resistance of rainbow trout, Salmo gairdneri Richardson, to reinfection. Journal of Fish Biology 30, 477–483. doi: 10.1111/j.1095-8649.1987.tb05771.x.CrossRefGoogle Scholar
Freitak, D., Ots, I., Vanatoa, A. and Horak, P. (2003). Immune response is energetically costly in white cabbbage butterfly pupae. Proceedings of the Royal Society of London, B 270 (Suppl.) S220–S222. doi: 10.1098/rsbl.2003.0069.CrossRefGoogle Scholar
Furuta, T., Ogawa, K. and Wakabayashi, H. (1993). Humoral immune response of carp Cyprinus carpio to Myxobolus artus (Myxozoa, Myxobolidae) infection. Journal of Fish Biology 43, 441–450. doi: 10.1111/j.1095-8649.1993.tb00579.x.CrossRefGoogle Scholar
Gaevskaya, A. V. and Kovaleva, A. A. (1979). New and rarely occurring myxosporidia species from the Celtic Sea fishes. Parazitologiya 13, 159–165.Google Scholar
Hedrick, R. P., El Matbouli, M., Adkison, M. A. and MacConnell, E. (1998). Whirling disease: re-emergence among wild trout. Immunological Reviews 166, 365–376. doi: 10.1111/j.1600-065X.1998.tb01276.x.CrossRefGoogle ScholarPubMed
Holzer, A. S., Sommerville, C. and Wootten, R. (2003). Tracing the route of Sphaerospora truttae from the entry locus to the target organ of the host, Salmo salar L., using an optimized and specific in situ hybridization technique. Journal of Fish Diseases 26, 647–655. doi: 10.1046/j.1365-2761.2003.00501.x.CrossRefGoogle Scholar
Holzer, A. S., 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 for Parasitology 34, 1099–1111. doi: 10.1016/j.ijpara.2004.06.002.CrossRefGoogle Scholar
Holzer, A. S., Sommerville, C. and Wootten, R. (2006). Molecular studies on the seasonal occurrence and development of five myxozoans in farmed Salmo trutta L. Parasitology 132, 193–205. doi: 10.1017/S0031182005008917.CrossRefGoogle ScholarPubMed
Holzer, A. S., Wootten, R. and Sommerville, C. (2010). Zschokkella hildae Auerbach, 1910: Phylogenetic position, morphology, and location in cultured Atlantic cod. Parasitology International (in the Press) doi:10.1016/j.parint.2009.12.004.CrossRefGoogle ScholarPubMed
Jones, S. R. M., Prosperi-Porta, G., Dawe, S. C. and Barnes, D. P. (2003). Distribution, prevalence and severity of Parvicapsula minibicornis infections among anadromous salmonids in the Fraser River, British Columbia, Canada. Diseases of Aquatic Organisms 54, 49–54. doi: 10.3354/dao054049.CrossRefGoogle ScholarPubMed
Karvonen, A. (2006 a). Intestinal distribution and fecundity of two species of Diplostomum parasites in definitve hosts. Parasitology 132, 357–362. doi: 10.1017/S0031182005009091.CrossRefGoogle Scholar
Karvonen, A. (2006 b). Ecological divergence of closely related Diplostomum (Trematoda) parasites. Parasitology 133, 229–235. doi: 10.1017/S0031182006000242.CrossRefGoogle ScholarPubMed
Kent, M. L. and Lom, J. (1986). Development of the PKX myxosporean in rainbow trout Salmo gairdneri. Diseases of Aquatic Organisms 1, 159–182.Google Scholar
Køie, M. (2002). Spirorchid and serpulid polychaetes are candidates as invertebrate hosts for myxozoa. Folia Parasitologica 49, 160–162.CrossRefGoogle ScholarPubMed
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, 1456–1467. doi: 10.1645/GE-1256.1.CrossRefGoogle ScholarPubMed
Køie, M., Steffensen, J. F., Moller, P. R. and Christiansen, J. S. (2008). The parasite fauna of Arctogadus glacialis (Peters) (Gadidae) from western and eastern Greenland. Polar Biology 31, 1017–1021. doi: 10.1007/s00300-008-0440-1.CrossRefGoogle Scholar
Lochmiller, R. L. and Deerenberg, C. (2000). Trade-offs in evolutionary immunology: just what is the cost of immunity? Oikos 88, 87–98. doi: 10.1034/j.1600-0706.2000.880110.x.CrossRefGoogle Scholar
Lom, J. and Dyková, I. (1992). Myxosporidia (Phylum Myxozoa). In Protozoan Parasites of Fishes (ed. Lom, J. and Dyková, I.), pp. 159–315. Elsevier Science Publishers B.V.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.CrossRefGoogle ScholarPubMed
MacKenzie, K. (1979). Some parasites and diseases of blue whiting Micromesistius poutassou to the north and west of Scotland and at the Faroe Islands UK. Scottish Fisheries Research Report 1–14.Google Scholar
Magnadóttir, B. (2006). Innate immunity of fish (overview). Fish & Shellfish Immunology 20, 137–151. doi: 10.1016/j.fsi.2004.09.006.CrossRefGoogle ScholarPubMed
Magnadóttir, B., Jonsdottir, H., Helgason, S., Bjornsson, B., Jorgensen, T. O. and Pilstrom, L. (1999). Humoral immune parameters in Atlantic cod (Gadus morhua L.) – I. The effects of environmental temperature. Comparative Biochemistry and Physiology B – Biochemistry & Molecular Biology 122, 173–180. doi: 10.1016/S0305-0491(98)10156-6.CrossRefGoogle Scholar
Magnadóttir, B., Lange, S., Gudmundsdottir, S., Bogwald, J. and Dalmo, R. A. (2005). Ontogeny of humoral immune parameters in fish. Fish & Shellfish Immunology 19, 429–439.CrossRefGoogle ScholarPubMed
Magnadóttir, B., Lange, S., Steinarsson, A. and Gudmundsdottir, S. (2004). The ontogenic development of innate immune parameters of cod (Gadus morhua L.). Comparative Biochemistry and Physiology B – Biochemistry & Molecular Biology 139, 217–224.CrossRefGoogle ScholarPubMed
Martin, L. B., Scheuerlein, A. and Wikelski, M. (2003). Immune activity elevates energy expenditure of house sparrows: a link between direct and indirect costs? Proceedings of the Royal Society of London, B 270, 153–158. doi: 10.1098/rspb.2002.2185.CrossRefGoogle ScholarPubMed
Mayxay, M., Pukrittayakamee, S., Chotivanich, K., Imwong, M., Looareesuwan, S. and White, N. J. (2001). Identification of cryptic co-infection with Plasmodium falciparum in patients presenting with vivax malaria. American Journal of Tropical Medicine and Hygiene 65, 588–592.CrossRefGoogle ScholarPubMed
McGeorge, J., Sommerville, C. and Wootten, R. (1994). Light and electron-microscope observations on extrasporogonic and sporogonic stages of a myxosporean parasite of the genus Sphaerospora Thelohan, 1892 from Atlantic salmon, Salmo salar L. in Scotland. Journal of Fish Diseases 17, 227–238. doi: 10.1111/j.1365-2761.1994.tb00218.x.CrossRefGoogle Scholar
Mideo, N. (2009). Parasite adaptations to within-host competition. Trends in Parasitology 25, 261–268. doi: 10.1016/j.pt.2009.03.001.CrossRefGoogle ScholarPubMed
Munoz, P., Cuesta, A., Athanassopoulou, F., Golomazou, H., Crespo, S., Padros, F., Sitja-Bobadilla, A., Albinana, G., Esteban, M. A., Alvarez-Pellitero, P. and Meseguer, J. (2007). Sharpsnout sea bream (Diplodus puntazzo) humoral immune response against the parasite Enteromyxum leei (Myxozoa). Fish & Shellfish Immunology 23, 636–645. doi: 10.1016/j.fsi.2007.01.014.CrossRefGoogle ScholarPubMed
Munoz, P., Sitja-Bobadilla, A. and Alvarez-Pellitero, P. (2000). Cellular and humoral immune response of European sea bass (Dicentrarchus labrax L.) (Teleostei: Serranidae) immunized with Sphaerospora dicentrarchi (Myxosporea: Bivalvulida). Parasitology 120, 465–477.CrossRefGoogle ScholarPubMed
Nagao, Y., Kimura-Sato, M., Chavalitshewinkoon-Petmitr, P., Thongrungkiat, S., Wilairatana, P., Ishida, T., Tan-Ariya, P., de Souza, J. B., Krudsood, S. and Looareesuwan, S. (2008). Suppression of Plasmodium falciparum by serum collected from a case of Plasmodium vivax infection. Malaria Journal 7, 113. doi: 10.1186/1475-2875-7-113.CrossRefGoogle ScholarPubMed
Pedersen, B. S. and Mills, N. J. (2004). Single vs. multiple introduction in biological control: the roles of parasitoid efficiency, antagonism and niche overlap. Journal of Applied Ecology 41, 973–984. doi: 10.1111/j.0021-8901.2004.00953.x.CrossRefGoogle Scholar
Redondo, M. J., Palenzuela, O., Riaza, A., Macias, A. and Alvarez-Pellitero, P. (2002). Experimental transmission of Enteromyxum scophthalmi (Myxozoa), an enteric parasite of turbot Scophthalmus maximus. Journal of Parasitology 88, 482–488. doi: 10.1645/0022-3395(2002)088[0482:ETOESM]2.0.CO;2.CrossRefGoogle ScholarPubMed
Richie, T. L. (1988). Interactions between malaria parasites infecting the same vertebrate host. Parasitology 96, 607–639.CrossRefGoogle ScholarPubMed
Saulnier, D. and de Kinkelin, P. (1996). Antigenic and biochemical study of PKX, the myxosporean causative agent of proliferative kidney disease of salmonid fish. Diseases of Aquatic Organisms 27, 103–114.CrossRefGoogle Scholar
Schrøder, M. B., Villena, A. J. and Jorgensen, T. O. (1998). Ontogeny of lymphoid organs and immunoglobulin producing cells in Atlantic cod (Gadus morhua L.). Developmental and Comparative Immunology 22, 507–517. doi: 10.1016/S0145-305X(98)00030-5.CrossRefGoogle ScholarPubMed
Sitja-Bobadilla, A. (2008). Living off a fish: A trade-off between parasites and the immune system. Fish & Shellfish Immunology 25, 358–372. doi: 10.1016/j.fsi.2008.03.018.CrossRefGoogle Scholar
Sitja-Bobadilla, A., Palenzuela, O., Riaza, A., Macias, M. A. and Alvarez-Pellitero, P. (2007). Protective acquired immunity to Enteromyxum scophthalmi (myxozoa) is related to specific antibodies in Psetta maxima (L.) (teleostei). Scandinavian Journal of Immunology 66, 26–34. doi: 10.1111/j.1365-3083.2007.01942.x.CrossRefGoogle ScholarPubMed
Sitja-Bobadilla, A., Redondo, M. J., Bermudez, R., Palenzuela, O., Ferreiro, I., Riaza, A., Quiroga, I., Nieto, J. M. and Alvarez-Pellitero, P. (2006). Innate and adaptive immune responses of turbot, Scophthalmus maximus (L.), following experimental infection with Enteromyxum scophthalmi (Myxosporea: Myxozoa). Fish & Shellfish Immunology 21, 485–500.CrossRefGoogle ScholarPubMed
Sitja-Bobadilla, A., Redondo, M. J., Macias, M. A., Ferreiro, I., Riaza, A. and Alvarez-Pellitero, P. (2004). Development of immunohistochemistry and enzyme-linked immunosorbent assays for the detection of circulating antibodies against Enteromyxum scophthalmi (Myxozoa) in turbot (Scophthalmus maximus L.). Fish & Shellfish Immunology 17, 335–345.CrossRefGoogle ScholarPubMed
St Hilaire, S., Boichuk, M., Barnes, D., Higgins, M., Devlin, R., Withler, R., Khattra, J., Jones, S. and Kieser, D. (2002). Epizootiology of Parvicapsula minibicornis in Fraser River sockeye salmon, Oncorhynchus nerka (Walbaum). Journal of Fish Diseases 25, 107–120.CrossRefGoogle Scholar
Tops, S., Lockwood, W. and Okamura, B. (2006). Temperature-driven proliferation of Tetracapsuloides bryosalmonae in bryozoan hosts portends salmonid declines. Diseases of Aquatic Organisms 70, 227–236. doi: 10.3354/dao070227.CrossRefGoogle ScholarPubMed
Wahli, T., Knuesel, R., Bernet, D., Segner, H., Pugovkin, D., Burkhardt-Holm, P., Escher, M. and Schmidt-Posthaus, H. (2002). Proliferative kidney disease in Switzerland: current state of knowledge. Journal of Fish Diseases 25, 491–500. doi: 10.1046/j.1365-2761.2002.00401.x.CrossRefGoogle 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.CrossRefGoogle Scholar