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Vertical transmission of Tetracapsuloides bryosalmonae (Myxozoa), the causative agent of salmonid proliferative kidney disease

Published online by Cambridge University Press:  07 November 2013

AHMED ABD-ELFATTAH ,
INÊS FONTES ,
GOKHLESH KUMAR ,
HATEM SOLIMAN ,
HANNA HARTIKAINEN ,
BETH OKAMURA  and
MANSOUR EL-MATBOULI
AHMED ABD-ELFATTAH
Affiliation:
Clinical Division of Fish Medicine, University of Veterinary Medicine, Vienna, Austria
INÊS FONTES
Affiliation:
Life Sciences Department, Natural History Museum, London, UK
GOKHLESH KUMAR
Affiliation:
Clinical Division of Fish Medicine, University of Veterinary Medicine, Vienna, Austria
HATEM SOLIMAN
Affiliation:
Clinical Division of Fish Medicine, University of Veterinary Medicine, Vienna, Austria Fish Medicine and Managements, Faculty of Veterinary Medicine, University of Assuit, 71515 Assuit, Egypt
HANNA HARTIKAINEN
Affiliation:
Life Sciences Department, Natural History Museum, London, UK
BETH OKAMURA
Affiliation:
Life Sciences Department, Natural History Museum, London, UK
MANSOUR EL-MATBOULI*
Affiliation:
Clinical Division of Fish Medicine, University of Veterinary Medicine, Vienna, Austria
*
* Corresponding author: Clinical Division of Fish Medicine, University of Veterinary Medicine, Veterinärplatz 1, 1210 Vienna, Austria. E-mail: Mansour.El-Matbouli@vetmeduni.ac.at
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Summary

The freshwater bryozoan, Fredericella sultana, is the main primary host of the myxozoan endoparasite, Tetracapsuloides bryosalmonae which causes proliferative kidney disease (PKD) of salmonid fish. Because spores that develop in bryozoan colonies are infectious to fish, bryozoans represent the ultimate source of PKD. Bryozoans produce numerous seed-like dormant stages called statoblasts that enable persistence during unfavourable conditions and achieve long-distance dispersal. The possibility that T. bryosalmonae may undergo vertical transmission via infection of statoblasts has been the subject of much speculation since this is observed in close relatives. This study provides the first evidence that such vertical transmission of T. bryosalmonae is extensive by examining the proportions of infected statoblasts in populations of F. sultana on two different rivers systems and confirms its effectiveness by demonstrating transmission from material derived from infected statoblasts to fish hosts. Vertical transmission in statoblasts is likely to play an important role in the infection dynamics of both bryozoan and fish hosts and may substantially contribute to the widespread distribution of PKD.

Keywords

BryozoaFredericella sultanastatoblastsmaternal coloniesTetracapsuloides bryosalmonaepersistent infectiondispersal
Type
Research Article
Information
Parasitology , Volume 141 , Issue 4 , April 2014 , pp. 482 - 490
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Copyright
Copyright © Cambridge University Press 2013 

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References

REFERENCES

Anderson, C. L., Canning, E. U. and Okamura, B. (1999). Molecular data implicate bryozoans as hosts for PKX (phylum Myxozoa) and identify a clade of bryozoan parasites within the Myxozoa. Parasitology 119, 555–561.CrossRefGoogle ScholarPubMed
Borsuk, M. E., Reichert, P., Peter, A., Schager, E. and Burkhardt-Holm, P. (2006). Assessing the decline of brown trout (Salmo trutta) in Swiss rivers using a Bayesian probability network. Ecological Modelling 192, 224–244.Google Scholar
Briski, E., Cristescu, M. E., Bailey, S. A. and MacIsaac, H. J. (2011). Use of DNA barcoding to detect invertebrate invasive species from diapausing eggs. Biological Invasions 13, 1325–1340.Google Scholar
Bull, J. J., Molinieux, I. J. and Rice, W. R. (1991). Selection of benevolence in a host–parasite system. Evolution 45, 875–882.Google Scholar
Canning, E. U., Curry, A., Feist, S. W., Longshaw, M. and Okamura, B. (1999). Tetracapsula bryosalmonae n.sp. for PKX organism, the cause of PKD in salmonid fish. Bulletin of the European Association of Fish Pathologists 19, 203–206.Google Scholar
Canning, E. U., Curry, A., Feist, S. W., Longshaw, M. and Okamura, B. (2000). A new class and order of myxozoans to accommodate parasites of bryozoans with ultrastructural observations on Tetracapsula bryosalmonae (PKX organism). Journal of Eukaryotic Microbiology 47, 456–468.CrossRefGoogle ScholarPubMed
Canning, E. U., Tops, S., Curry, A., Wood, T. S. and Okamura, B. (2002). Ecology, development and pathogenicity of Buddenbrockia plumatellae Schröder, 1910 (Myxozoa, Malacosporea) (syn. Tetracapsula bryozoides) and establishment of Tetracapsuloides n. gen. for Tetracapsula bryosalmonae . Journal of Eukaryotic Microbiology 49, 280–295.Google Scholar
Charalambidou, I., Santamarıa, L. and Figuerola, J. (2003). How far can the freshwater bryozoan Cristatella mucedo disperse in duck guts? Archiv für Hydrobiologie 157, 547–554.Google Scholar
Clifton-Hadley, R. S., Bucke, D. and Richards, R. H. (1986). Economic importance of proliferative kidney disease in salmonid fish in England and Wales. Veterinary Record 119, 305–306.Google Scholar
De Kinkelin, P., Gay, M. and Forman, S. (2002). The persistence of infectivity of Tetracapsula bryosalmonae-infected water for rainbow trout, Oncorhynchus mykiss (Walbaum). Journal of Fish Diseases 25, 477–482.Google Scholar
El-Matbouli, M. and Hoffmann, R. W. (2002). Influence of water quality on the outbreak of proliferative kidney disease field studies and exposure experiments. Journal of Fish Diseases 25, 459–467.Google Scholar
Feist, S. W. and Longshaw, M. (2006). The Phylum Myxozoa. In Fish Diseases and Disorders, Vol. 1. (ed. Woo, P. T. K.), pp. 230–296. CABI, Wallingford, UK.Google Scholar
Feist, S. W., Longshaw, M., Canning, E. U. and Okamura, B. (2001). Induction of proliferative kidney disease (PKD) in rainbow trout Oncorhynchus mykiss via the bryozoan Fredericella sultana infected with Tetracapsula bryosalmonae . Diseases of Aquatic Organisms 45, 61–68.Google Scholar
Ferguson, H. W. and Ball, H. J. (1979). Epidemiological aspects of proliferative kidney disease in rainbow trout, Salmo gairdneri Richardson in Northern Ireland. Journal of Fish Diseases 2, 219–225.Google Scholar
Figuerola, J., Green, A. J., Black, K. and Okamura, B. (2004). Influence of gut morphology on passive transport of freshwater bryozoans by waterfowl in Donana (southwestern Spain). Canadian Journal of Zoology 82, 835–840.Google Scholar
Figuerola, J., Green, A. J. and Michot, T. C. (2005). Invertebrate eggs can fly: evidence of waterfowl-mediated gene flow in aquatic invertebrates. American Naturalist 165, 274–280.Google Scholar
Freeland, J. R., Noble, L. R. and Okamura, B. (2000). Genetic consequences of the metapopulation biology of a facultatively sexual freshwater invertebrate. Journal of Evolutionary Biology 13, 383–395.Google Scholar
Grabner, D. S. and El-Matbouli, M. (2008). Transmission of Tetracapsuloides bryosalmonae (Myxozoa: Malacosporea) to Fredericella sultana (Bryozoa: Phylactolaemata) by various fish species. Diseases of Aquatic Organisms 79, 133–139.Google Scholar
Grabner, D. S. and El-Matbouli, M. (2009). 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). Veterinary Parasitology 165, 200–206.Google Scholar
Green, A. J., Jenkins, K. M., Bell, D., Morris, P. J. and Kingsford, R. T. (2008). The potential role of waterbirds in dispersing invertebrates and plants in arid Australia. Freshwater Biology 53, 380–392.Google Scholar
Hartikainen, H. and Okamura, B. (2012). Castrating parasites and colonial hosts. Parasitology 139, 547–556.CrossRefGoogle ScholarPubMed
Hartikainen, H., Fontes, I. and Okamura, B. (2013). Parasitism and phenotypic change in colonial hosts. Parasitology 140, 1403–1412.Google Scholar
Henderson, M. W. and Okamura, B. (2004). The phylogeography of salmonid proliferative kidney disease in Europe and North America. Proceedings of the Royal Society B 1549, 1729–1736.Google Scholar
Hengherr, S. and Schill, R. O. (2011). Dormant stages in freshwater bryozoans – an adaptation to transcend environmental constraints. Journal of Insect Physiology 57, 595–601.Google Scholar
Hill, S. L. L. and Okamura, B. (2007). Endoparasitism in colonial hosts: pattern and processes. Parasitology 134, 841–852.Google Scholar
Kent, M. L., Khattra, J., Hervio, D. M. L. and Devlin, R. H. (1998). Ribosomal DNA sequence analysis of isolates of the PKX myxosporean and their relationship to members of the genus Sphaerospora . Journal of Aquatic Animal Health 10, 12–21.Google Scholar
Kipp, R., Bailey, S. A., MacIsaac, H. J. and Ricciardi, A. (2010). Transoceanic ships as vectors for nonindigenous freshwater bryozoans. Diversity and Distributions 16, 77–83.Google Scholar
Kumar, G., Abd-Elfattah, A., Soliman, H. and El-Matbouli, M. (2013). Establishment of medium for laboratory cultivation and maintenance of Fredericella sultana for in vivo experiments with Tetracapsuloides bryosalmonae (Myxozoa). Journal of Fish Diseases 36, 81–88.Google Scholar
Marković, G., Karin-Žnidaršić, T. and Simonović, P. (2009). Bryozoan species Hyalinella punctata Hancock in the gut content of chub Leuciscus cephalus L. Polish Journal of Ecology 57, 201–205.Google Scholar
Massard, J. A. and Geimer, G. (2008). Global diversity of bryozoans (Bryozoa or Ectoprocta) in fresh water. Hydrobiologia 595, 93–99.Google Scholar
Morris, D. J. and Adams, A. (2006 a). Proliferative, presaccular stages of Tetracapsuloides bryosalmonae (Myxozoa: Malacosporea) within the invertebrate host Fredericella sultana (Bryozoa: Phylactolaemata). Journal of Parasitology 92, 984–989.Google Scholar
Morris, D. J. and Adams, A. (2006 b). Transmission of freshwater myxozoans during the asexual propagation of invertebrate hosts. International Journal for Parasitology 36, 371–377.Google Scholar
Mouranval, J. P., Guillemain, M., Canny, A. and Poirier, F. (2007). Diet of non-breeding wildfowl Anatidae and Coot Fulica atra on the Perthois gravel pits, northeast France. Wildfowl 57, 68–97.Google Scholar
Okamura, B., Hartikainen, H., Schmidt-Posthaus, H. and Wahli, T. (2011). Proliferative kidney disease as an emerging disease: the importance of life cycle complexity and environmental change. Freshwater Biology 56, 735–753.CrossRefGoogle Scholar
Sterud, E., Forseth, T., Ugedal, O., Poppe, T. T., Jørgensen, A., Bruheim, T., Fjeldstad, H. P. and Mo, T. A. (2007). Severe mortality in wild Atlantic salmon Salmo salar due to proliferative kidney disease (PKD) caused by Tetracapsuloides bryosalmonae (Myxozoa). Diseases of Aquatic Organisms 77, 191–198.Google Scholar
Taticchi, M. I., Gustinelli, A., Fioravanti, M. L., Caffara, M., Pieroni, G. and Prearo, M. (2004). Is the worm-like organism found in the statoblasts of Plumatella fungosa (Bryozoa, Phylactolaemata) the vermiform phase of Tetracapsuloides bryosalmonae (Myxozoa, Malacosporea)? Italian Journal of Zoology 71, 143–146.Google Scholar
Tops, S. (2004). Ecology, life history and diversity of malacosporeans. Ph.D. thesis. University of Reading.Google Scholar
Tops, S. and Okamura, B. (2003). Infection of bryozoans by Tetracapsuloides bryosalmonae at sites endemic for salmonid proliferative kidney disease. Diseases of Aquatic Organisms 57, 221–226.Google Scholar
Tops, S., Baxa, D. V., McDowell, T. S., Hedrick, R. P. and Okamura, B. (2004). Evaluation of malacosporean life cycles through transmission studies. Diseases of Aquatic Organisms 60, 109–121.Google 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.Google Scholar
Tops, S., Hartikainen, H. and Okamura, B. (2009). The effects of infection by Tetracapsuloides bryosalmonae (Myxozoa) and temperature on Fredericella sultana (Bryozoa). International Journal for Parasitology 39, 1003–1010.Google Scholar
Wood, T. S. and Okamura, B. (2005). A New Key to the Freshwater Bryozoans of Britain, Ireland and Continental Europe, with Notes on their Ecology. Freshwater Biological Association, The Ferry House, Far Sawrey, Ambleside, Cumbria, UK.Google Scholar