Hostname: page-component-cd9895bd7-lnqnp Total loading time: 0 Render date: 2024-12-26T21:03:22.115Z Has data issue: false hasContentIssue false

The ultrastructure of hypersymbionts on the monogenean Gyrodactylus salaris infecting Atlantic salmon Salmo salar

Published online by Cambridge University Press:  12 April 2024

T.A. Bakke*
Affiliation:
Natural History Museum, Department of Zoology, University of Oslo, PO Box 1172, Blindern, NO-0318 Oslo, Norway
J. Cable
Affiliation:
School of Biosciences, Cardiff University, Cardiff, CF10 3TL, UK
M. Østbø
Affiliation:
Natural History Museum, Department of Zoology, University of Oslo, PO Box 1172, Blindern, NO-0318 Oslo, Norway
*
*Corresponding author: Fax: 47 22851837, Email: [email protected]
Rights & Permissions [Opens in a new window]

Abstract

Core share and HTML view are not available for this content. However, as you have access to this content, a full PDF is available via the ‘Save PDF’ action button.

There is increasing pressure to develop alternative control strategies against the pathogen Gyrodactylus salaris, which has devastated wild Atlantic salmon Salmo salar in Norway. Hyperparasitism is one option for biological control and electron microscopy has revealed two ectosymbionts associated with G. salaris: unidentified rod-shaped bacteria, and the protist, Ichthyobodo necator. No endosymbionts were detected. The flagellate I. necator occurred only occasionally on fish suffering costiosis, whereas bacterial infections on the tegument of G. salaris were observed throughout the year, but at variable densities. Bacteria were seldom observed attached to fish epidermis, even when individuals of G. salaris on the same host were heavily infected. Wounds on salmon epidermis caused by the feeding activity of bacteria-infected G. salaris did not appear to be infected with bacteria. On heavily infected gyrodactylids, bacteria were most abundant anteriorly on the cephalic lobes, including the sensory structures, but no damaged tissue was detected by transmission electron microscopy in the region of bacterial adherence. Furthermore, transmission and survival of infected G. salaris on wild salmon did not appear to be influenced by the bacterial infection. The lack of structural damage and impact on G. salaris biology indicates that these bacteria are not a potential agent for control of gyrodactylosis. However, this may not be the case for all gyrodactylid–bacterial interactions and a review of bacterial infections of platyhelminths is presented.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2006

References

Aho, J.M., Uglem, G.L., Moore, J.P. & Larsen, O.R. (1991) Bacteria associated with the tegument of Clinostomum marginatum (Digenea). Journal of Parasitology 77, 784786.CrossRefGoogle ScholarPubMed
Bakke, T.A. & Harris, P.D. (1998) Diseases and parasites in wild Atlantic salmon ( Salmo salar ) populations. Canadian Journal of Fisheries and Aquatic Sciences 55, 247266.CrossRefGoogle Scholar
Brown, E.E. & Gratzek, J.B. (1980) Fish farming handbook. Food, bait, tropicals and goldfish. 390 pp. Westport, Connecticut Avi Publishing Co., Inc.Google Scholar
Bruno, D.W. & Poppe, T. (1996) A colour atlas of salmonid diseases. 194 pp. London, Academic Press.Google Scholar
Cable, J. & Harris, P.D. (2002) Gyrodactylid developmental biology: historical review, current status and future trends. International Journal for Parasitology 32, 255280.CrossRefGoogle ScholarPubMed
Cable, J. & Tinsley, R.C. (1992) Microsporidian hyperparasites and bacteria associated with Pseudodiplorchis americanus (Monogenea: Polystomatidae). Canadian Journal of Zoology 70, 523529.CrossRefGoogle Scholar
Cable, J., Harris, P.D. & Bakke, T.A. (2000) Population growth of Gyrodactylus salaris (Monogenea) on Norwegian and Baltic Atlantic salmon ( Salmo salar ) stocks. Parasitology 121, 621629.CrossRefGoogle ScholarPubMed
Canning, E.U. (1975) The microsporidean parasites of Platyhelminthes: their morphology, development, transmission and pathogenicity. Commonwealth Institute of Helminthology Miscellaneous Publications 2, 132.Google Scholar
Cone, D.K. & Cusack, R. (1988) A study of Gyrodactylus colemanensis Mizelle and Kritsky, 1967 and Gyrodactylus salmonis (Yin and Sproston, 1948) (Monogenea) parasitizing captive salmonids in Nova Scotia. Canadian Journal of Zoology 66, 409415.CrossRefGoogle Scholar
Cone, D.K. & Odense, P.H. (1984) Pathology of five species of Gyrodactylus Nordmann, 1832 (Monogenea). Canadian Journal of Zoology 62, 10841088.CrossRefGoogle Scholar
Crouse-Eisnor, R.A., Cone, D.K. & Odense, P.H. (1985) Studies on relations of bacteria with skin surface of Carassius auratus L. and Poecilia reticulata. Journal of Fish Biology 27, 395402.CrossRefGoogle Scholar
Cusack, R. & Cone, D.K. (1985) A report of bacterial microcolonies on the surface of Gyrodactylus (Monogenea). Journal of Fish Diseases 8, 125127.CrossRefGoogle Scholar
Cusack, R., Rand, T. & Cone, D. (1988) A study of bacterial microcolonies associated with the body surface of Gyrodactylus colemanensis Mizelle and Kritsky, 1967 (Monogenea), parasitizing Salmo gairdneri Richardson. Journal of Fish Diseases 11, 271274.CrossRefGoogle Scholar
Dollfus, R.P. (1946) Parasites (animaux et vegetaux) des helminthes. Hyperparasites ennemis et prédateurs des helminthes parasites et des helminthes libre. Encyclopedie Biologique 27, 1482.Google Scholar
El-Naggar, M.M. & Kearn, G.C. (1989) Haptor glands in the gill-parasitic, ancyrocephaline monogenean Cichlidogyrus halli typicus and the report of a possible prokaryotic symbiont. International Journal for Parasitology 19, 401408.CrossRefGoogle Scholar
Heggberget, T.G. & Johnsen, B.O. (1982) Infestations by Gyrodactylus sp. of Atlantic salmon, Salmo salar L., in Norwegian rivers. Journal of Fish Biology 21, 1526.CrossRefGoogle Scholar
Hughes-Stamm, S., Cribb, T.H. & Jones, M.K. (1999) Structure of the tegument and ectocommensal microorgansims of Gyliauchen nahaensis (Digenea: Gyliauchenidae), an inhabitant of herbivorous fish of the Great Barrier Reef, Australia. Journal of Parasitology 85, 10471052.CrossRefGoogle Scholar
Jansen, P.A. & Bakke, T.A. (1991) Temperature-dependent reproduction and survival of Gyrodactylus salaris Malmberg, 1957 (Platyhelminthes: Monogenea) on Atlantic salmon ( Salmo salar L.). Parasitology 102, 105112.CrossRefGoogle ScholarPubMed
Jansen, P.A. & Bakke, T.A. (1993a) Regulatory processes in the monogenean Gyrodactylus salaris Malmberg – Atlantic salmon ( Salmo salar L.) association. II. Experimental studies. Fisheries Research 17, 103114.CrossRefGoogle Scholar
Jansen, P.A. & Bakke, T.A. (1993b) Regulatory processes in the monogenean Gyrodactylus salaris Malmberg – Atlantic salmon ( Salmo salar L.) association I. Field studies in south-east Norway. Fisheries Research 17, 87101.CrossRefGoogle Scholar
Johnsen, B.O. (1978) The effect of an attack by the parasite Gyrodactylus salaris on the population of salmon parr in the river Lakselva, Misvær in Northern Norway. Astarte 11, 79.Google Scholar
Johnsen, B.O., Møkkelgjerd, P.I. & Jensen, A.J. (1999) The parasite Gyrodactylus salaris on salmon parr in Norwegian rivers, status report at the beginning of year 2000. NINA Oppdargsmelding 617, 1129 (in Norwegian with English summary).Google Scholar
Kritsky, D.C. (1978) The cephalic glands and associated structures in Gyrodactylus eucaliae Ikezaki and Hoffman, 1957 (Monogenea: Gyrodactylidae). Proceedings of the Helminthological Society of Washington 45, 3749.Google Scholar
Lasee, B.A. & Sutherland, D.R. (1993) Bacterial colonization of tegumental surfaces of Culaeatrema inconstans Lasee et al., 1988 (Digenea) from the brook stickleback, Culaea inconstans. Journal of Fish Diseases 16, 8385.CrossRefGoogle Scholar
Lindblom, G.-B. & Nilsson, L.-Å. (1994) Interaction between Campylobacter jejuni / coli and Schistosoma mansoni, a helminth parasite. Bulletin of the Scandinavian Society of Parasitology 4, 18.Google Scholar
Lom, J. & Dykovaá, I. (1992) Protozoan parasites of fishes. 315 pp. Amsterdam, Elsevier.Google Scholar
Lo Verde, P.T., Amento, C. & Higashi, G.I. (1980) Parasite–parasite interaction of Salmonella typhimurium and Schistosoma. Journal of Infectious Diseases 141, 177185.CrossRefGoogle ScholarPubMed
Lundin, K. (1998) Symbiotic bacteria on the epidermis of species of the Nemertodermatida (Platyhelminthes Acoelomorpha). Acta Zoologica 79, 187191.CrossRefGoogle Scholar
Lyons, K.M. (1969a) Sense organs of monogeneans ending in a typical cilium. Parasitology 59, 431443.CrossRefGoogle Scholar
Lyons, K.M. (1969b) Compound sensilla in monogenean skin parasites. Parasitology 59, 444455.CrossRefGoogle Scholar
Lyons, K.M. (1970) Fine structure of the outer epidermis of the viviparous monogenean Gyrodactylus sp. from the skin of Gasterosteus aculeatus. Journal of Parasitology 56, 11101117.CrossRefGoogle Scholar
Morris, G.P. (1973) The morphology of associations between a trematode ( Megalodiscus temperatus ) and bacteria. Canadian Journal of Zoology 51, 13131314.CrossRefGoogle Scholar
Morris, G.P. & Halton, D.W. (1975) The occurrence of bacteria and mycoplasma-like organisms in a monogenean parasite, Diclidophora merlangi. International Journal for Parasitology 5, 495498.CrossRefGoogle Scholar
Poléo, A.B.S., Schjolden, J., Hansen, H., Bakke, T.A., Mo, T.A., Rosseland, B.O. & Lydersen, E. (2003) The effect of various metals on Gyrodactylus salaris (Platyhelminthes, Monogenea) infections in Atlantic salmon ( Salmo salar ). Parasitology 128, 19.Google Scholar
Rego, A.A. & Gibson, D.I. (1989) Hyperparasitism by helminths: new records of cestodes and nematodes in protocephalid cestodes from South American siluriform fishes. Memorias do Instituto Oswaldo Cruz 84, 371376.CrossRefGoogle Scholar
Rohde, K. (1986) Ultrastructure of the pharynx and some parenchyma cells of Zeuxapta seriolae and Paramicrocotyloides reticularis (Monogenea: Polyopisthocotylea: Microcotylidae). Australian Journal of Zoology 34, 473484.CrossRefGoogle Scholar
Salte, R. & Bentsen, H.B. (2004) Avl for økt motstand mot Gyrodactylus salaris -infeksjon. Norsk Veterinærtidsskrift 3, 186189 (in Norwegian).Google Scholar
Snieszko, S.F. and Bullock, G.L. (1968) Freshwater fish diseases caused by bacteria belonging to the genera Aeromonas and Pseudomonas. US Department of International Fisheries and Wildlife Services, Fish Diseases Leaflet, 11.Google Scholar
Soleng, A., Poleéo, A.B.S., Alstad, N.E.W. & Bakke, T.A. (1999a) Aqueous aluminium eliminates Gyrodactylus salaris (Platyhelminthes, Monogenea) infections in Atlantic salmon. Parasitology 119, 1925.CrossRefGoogle ScholarPubMed
Soleng, A., Jansen, P.A. & Bakke, T.A. (1999b) Transmission of the monogenean Gyrodactylus salaris. Folia Parasitologica 46, 179184.Google Scholar
Soleng, A., Poléo, A.B.S. & Bakke, T.A. (2005) Toxicity of aqueous aluminium to the ectoparasitic monogenean Gyrodactylus salaris. Aquaculture 250, 616620.CrossRefGoogle Scholar
Tuazon, C.U., Nash, T., Cheever, A. & Neva, F. (1985) Interaction of Schistosoma japonicum with Salmonella and other gram-negative bacteria. Journal of Infectious Diseases 152, 722726.CrossRefGoogle ScholarPubMed
Veltkamp, C.J., Chubb, J.C., Birch, S.P. & Eaton, J.W. (1994) A simple freeze dehydration method for studying epiphytic and epizoic communities using the scanning electron microscope. Hydrobiologica 288, 3338.CrossRefGoogle Scholar
Veltkamp, C.J., Richards, G.R. & Chubb, J.C. (1996) Freeze fixation-dehydration as a method of preparation of Gyrodactylus (Monogenea) for scanning electron microscopy. Journal of Helminthology 70, 8589.CrossRefGoogle Scholar
Vickerman, K. (1972) The host–parasite interface of parasitic protozoa. Some problems posed by ultrastructural studies. Symposia of the British Society for Parasitology 10, 7191.Google Scholar
Whittington, I.D., Cribb, B.W., Hamwood, T.E. & Halliday, J. (2000) Host specificity of monogenean (Platyhelminth) parasites: a role for anterior adhesive areas? International Journal for Parasitology 30, 305320.CrossRefGoogle ScholarPubMed
Williams, J.B. (1991) Rickettsiae and giant lysosomes in the testes of Temnocephala novaezealandiae (Platyhelminthes: Temnocephaloidea). Journal of Submicroscopical Cytology and Pathology 23, 447455.Google ScholarPubMed
Williams, J.B. (1992) Ultrastructure of the intestinal epithelium and prey microorganisms of Troglocaridicola mrazeki (Platyhelminthes: Scutaiellidae). Journal of Submicroscopical Cytology and Pathology 24, 473481.Google Scholar