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Arctic charr (Salvelinus alpinus) is a suitable host for Gyrodactylus salaris (Monogenea, Gyrodactylidae) in Norway

Published online by Cambridge University Press:  23 October 2006

G. ROBERTSEN ,
H. HANSEN ,
L. BACHMANN  and
T. A. BAKKE
H. HANSEN
Affiliation:
Natural History Museum, Department of Zoology, University of Oslo, P.O. Box 1172, N-0318 Oslo, Norway
L. BACHMANN
Affiliation:
Natural History Museum, Department of Zoology, University of Oslo, P.O. Box 1172, N-0318 Oslo, Norway
T. A. BAKKE
Affiliation:
Natural History Museum, Department of Zoology, University of Oslo, P.O. Box 1172, N-0318 Oslo, Norway
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Abstract

Gyrodactylus specimens infecting both anadromous Arctic charr (Salvelinus alpinus) from River Signaldalselva (northern Norway) and resident Arctic charr from Lake Pålsbufjorden (southern Norway) were identified as G. salaris using molecular markers and morphometrics. The infection in Pålsbufjorden represents the first record of a viable G. salaris population infecting a host in the wild in the absence of salmon (Salmo salar). G. salaris on charr from Signaldalselva and Pålsbufjorden bear different mitochondrial haplotypes. While parasites infecting charr in Signaldalselva carry the same mitochondrial haplotype as parasites from sympatric Atlantic salmon, G. salaris from charr in Pålsbufjorden bear a haplotype that has previously been found in parasites infecting rainbow trout (Oncorhynchus mykiss) and Atlantic salmon, and an IGS repeat arrangement that is very similar to those observed earlier in parasites infecting rainbow trout. Accordingly, the infection may result from 2 subsequent host-switches (from salmon via rainbow trout to charr). Morphometric analyses revealed significant differences between G. salaris infecting charr in the 2 localities, and between those on sympatric charr and salmon within Signaldalselva. These differences may reflect adaptations to a new host species, different environmental conditions, and/or inherited differences between the G. salaris strains. The discovery of G. salaris on populations of both anadromous and resident charr may have severe implications for Atlantic salmon stock-management as charr may represent a reservoir for infection of salmon.

Keywords

Arctic charrAtlantic salmonGyrodactylus salarishost-switchmolecular markersmorphometryrainbow trout
Type
Research Article
Information
Parasitology , Volume 134 , Issue 2 , February 2007 , pp. 257 - 267
Copyright
2006 Cambridge University Press

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References

REFERENCES

Aass, P. ( 1970). The winter migrations of charr, Salvelinus alpinus L., in the hydroelectric reservoirs Tunhovdfjord and Pålsbufjord, Norway. Report of the Institute of Freshwater Research Drottningholm 50, 5–44.Google Scholar
Altschul, S. F. ( 1991). Amino acid substitution matrices from an information theoretic perspective. Journal of Molecular Biology 219, 555–565.CrossRefGoogle Scholar
Appleby, C. ( 1996). Variability of the opisthaptoral hard parts of Gyrodactylus callariatis Malmberg, 1957 (Monogenea: Gyrodactylidae) from Atlantic cod Gadus morhua L. in the Oslo Fjord, Norway. Systematic Parasitology 33, 199–207.CrossRefGoogle Scholar
Bakke, T. A., Harris, P. D. and Cable, J. ( 2002). Host specificity dynamics: observations on gyrodactylid monogeneans. International Journal for Parasitology 32, 281–308. DOI:10.1016/S0020-7519(01)00331-9.CrossRefGoogle Scholar
Bakke, T. A., Harris, P. D., Jansen, P. A. and Hansen, L. P. ( 1992). Host specificity and dispersal strategy in gyrodactylid monogeneans, with particular reference to Gyrodactylus salaris Malmberg (Platyhelminthes, Monogenea). Diseases of Aquatic Organisms 13, 63–74.CrossRefGoogle Scholar
Bakke, T. A., Jansen P. A. and Harris, P. D. ( 1996). Differences in susceptibility of anadromous and resident stocks of Arctic charr to infections of Gyrodactylus salaris under experimental conditions. Journal of Fish Biology 49, 341–351.CrossRefGoogle Scholar
Boeger, W. A. and Kritsky, D. C. ( 1997). Coevolution of the Monogenoidea (Platyhelminthes) based on a revised hypothesis of parasite phylogeny. International Journal for Parasitology 27, 1495–1511.CrossRefGoogle Scholar
Boeger, W. A., Kritsky, D. C. and Pie, M. R. ( 2003). Context of diversification of the viviparous Gyrodactylidae (Platyhelminthes, Monogenoidea). Zoologica Scripta 32, 437–448.CrossRefGoogle Scholar
Brooks, D. R. and McLennan, D. A. ( 1993). Parascript: Parasites and the Language of Evolution. Smithsonian Institution Press, Washington, DC.
Brunner, P. C., Douglas, M. R., Osinov, A., Wilson, C. C. and Bernatchez, L. ( 2001). Holarctic phylogeography of Arctic charr (Salvelinus alpinus L.) inferred from mitochondrial DNA sequences. Evolution 55, 573–586.Google Scholar
Buchmann, K. and Lindenstrøm, T. ( 2002). Interactions between monogenean parasites and their fish hosts. International Journal for Parasitology 32, 309–319.CrossRefGoogle Scholar
Cable, J. and Harris, P. D. ( 2002). Gyrodactylid developmental biology: historical review, current status and future trends. International Journal for Parasitology 32, 255–280.CrossRefGoogle Scholar
Collins, C. M. and Cunningham, C. O. ( 2000). Characterization of the Gyrodactylus salaris Malmberg, 1957 (Platyhelminthes: Monogenea) ribosomal intergenic spacer (IGS) DNA. Parasitology 121, 555–563. DOI:10.1017/S0031182099006770.CrossRefGoogle Scholar
Cribb, T. H., Chisholm, L. A. and Bray, R. A. ( 2002). Diversity in the Monogenea and Digenea: does lifestyle matter? International Journal for Parasitology 32, 321–328.Google Scholar
Cunningham, C. O., Mo, T. A., Collins, C. M., Buchmann, K., Thiery, R., Blanc, G. and Lautraite, A. ( 2001). Redescription of Gyrodactylus teuchis Lautraite, Blanc, Thiery, Daniel & Vigneulle, 1999 (Monogenea: Gyrodactylidae); a species identified by ribosomal RNA sequence. Systematic Parasitology 48, 141–150.CrossRefGoogle Scholar
Cunningham, C. O., Collins, C. M., Malmberg, G. and Mo, T. A. ( 2003). Analysis of ribosomal RNA intergenic spacer (IGS) sequences in species and populations of Gyrodactylus (Platyhelminthes: Monogenea) from salmonid fish in northern Europe. Diseases of Aquatic Organisms 57, 237–246.CrossRefGoogle Scholar
Dávidova, M., Jarkoský, J., Matějusová, I. and Gelnar, M. ( 2005). Seasonal occurrence and metrical variability of Gyrodactylus rhodei Žitnaň, 1964 (Monogenea, Gyrodactylidae). Parasitology Research 95, 398–405.CrossRefGoogle Scholar
Ergens, R. ( 1976). Variability of hard parts of opisthaptor of two species of Gyrodactylus Nordmann, 1832 (Monogenoidea) from Phoxinus phoxinus (L.). Folia Parasitologica 23, 111–126.Google Scholar
Ergens, R. ( 1981). Variability of hard parts of opisthaptor in Gyrodactylus truttae Gläser, 1974 (Gyrodactylidae: Monogenea). Folia Parasitologica 28, 37–42.Google Scholar
Ergens, R. and Gelnar, M. ( 1985). Experimental verification of the effect of temperature on the size of hard parts of opisthaptor of Gyrodactylus katharineri Malmberg, 1964 (Monogenea). Folia Parasitologica 32, 377–380.Google Scholar
Geets, A., Appleby, C. and Ollevier, F. ( 1999). Host-dependent and seasonal variation in opisthaptoral hard parts of Gyrodactylus cf. arcuatus from three Pomatoschistus spp. and G. arcuatus from Gasterosteus aculeatus: a multivariate approach. Parasitology 119, 27–40.Google Scholar
Hammer, Ø., Harper, D. A. T. and Ryan, P. D. ( 2001). PAST: paleontological statistics software package for education and data analysis. Palaeontologia Electronica 4, 1–9.Google Scholar
Hansen, H., Bachmann, L. and Bakke, T. A. ( 2003). Mitochondrial DNA variation of Gyrodactylus spp. (Monogenea, Gyrodactylidae) populations infecting Atlantic salmon, grayling and rainbow trout in Norway and Sweden. International Journal for Parasitology 33, 1471–1478. DOI:10.1016/S0020-7519(03)00200-5.CrossRefGoogle Scholar
Hansen, H., Martinsen, L., Bakke, T. A. and Bachmann, L. ( 2006). The incongruence of nuclear and mitochondrial DNA variation supports conspecificity of the monogenean parasites Gyrodactylus salaris and G. thymalli. Parasitology doi: 10.1017//5003//82006000655 (in the Press).CrossRefGoogle Scholar
Harris, P. D., Cable, J., Tinsley, R. C. and Lazarus, C. M. ( 1999). Combined ribosomal DNA and morphological analysis of individual gyrodactylid monogeneans. Journal of Parasitology 85, 188–191.CrossRefGoogle Scholar
Harris, P. D., Shinn, A., Cable, J. and Bakke, T. A. ( 2004). Nominal species of the genus Gyrodactylus von Nordmann 1832 (Monogenea: Gyrodactylidae), with a list of principal host species. Systematic Parasitology 59, 1–27.CrossRefGoogle Scholar
Heggberget, T. G. ( 1984). Habitat selection and segregation of parr of Arctic charr (Salvelinus alpinus), brown trout (Salmo trutta) and Atlantic salmon (Salmo salar L.) in two streams in North Norway. In Biology of the Arctic Charr (ed. Johnson, L. and Burns, B. L.), pp. 217–231. Proceedings of the International Symposium on Arctic charr, Winnipeg, Manitoba, University of Manitoba Press.
Huyse, T. and Volckaert, F. A. M. ( 2002). Identification of a host-associated species complex using molecular and morphometric analyses, with the description of Gyrodactylus rugiensoides n. sp. (Gyrodactylidae, Monogenea). International Journal for Parasitology 32, 907–919.CrossRefGoogle Scholar
Huyse, T. and Volckaert, F. A. M. ( 2005). Comparing host and parasite phylogenies: Gyrodactylus flatworms jumping from goby to goby. Systematic Biology 54, 710–718. DOI:10.1080/10635150500221036.CrossRefGoogle Scholar
Johnsen, B. O., Møkkelgjerd, P. I. and Jensen, A. J. ( 1999). The parasite Gyrodactylus salaris on salmon parr in Norwegian rivers, status report at the beginning of year 2000. NINA Oppdragsmelding 617, 1–129 (in Norwegian, English summary).Google Scholar
Klemetsen, A., Amundsen, P.-A., Dempson, J. B., Jonsson, N., O'Connell, M. F. and Mortensen, E. ( 2003). Atlantic salmon Salmo salar L., brown trout Salmo trutta L. and Arctic charr Salvelinus alpinus (L.): a review of aspects of their life histories. Ecology of Freshwater Fish 12, 1–59.Google Scholar
Knudsen, R., Rikardsen, A. H., Kristoffersen, R., Sandring, S. and Siikavoupio, S. ( 2004). Registrations of Gyrodactylus spp. in the fish community in Signaldalselva and Kitdalselva in Troms county 2003. NINA oppdragsmelding 817, 1–23 (in Norwegian, English summary).Google Scholar
Knudsen, R., Adolfsen, P., Sandring, S., Kristoffersen, R., Rikardsen, A. and Siikavuoppio, A. ( 2006). The suitability of anadromous Arctic charr as host and vector of the monogenean Gyrodactylus salaris. Ecology of Freshwater Fish. (in the Press.)Google Scholar
Kristoffersen, R., Richardsen, A., Winger, A. C., Adolfsen, P. and Knudsen, R. ( 2005). Arctic charr as a long-term host of Gyrodactylus salaris in River Skibotnelva, northern Norway. NINA Rapport 36, 1–27 (in Norwegian, English summary).Google Scholar
Malmberg, G. ( 1970). The excretory system and the marginal hooks as a basis for the systematics of Gyrodactylus (Trematoda, Monogenea). Arkiv für Zoologi 23, 1–235.Google Scholar
Matějusová, I., Gelnar, M., McBeath, A. J. A., Collins, C. M. and Cunningham, C. O. ( 2001). Molecular markers for gyrodactylids (Gyrodactylidae: Monogenea) from five fish families (Teleostei). International Journal for Parasitology 31, 738–745. DOI:10.1016/S0020-7519(01)00176-X.CrossRefGoogle Scholar
Meinilä, M., Kuusela, J., Ziętara, M. S. and Lumme, J. ( 2004). Initial steps of speciation by geographic isolation and host switch in salmonid pathogen Gyrodactylus salaris (Monogenea: Gyrodactylidae). International Journal for Parasitology 34, 515–526. DOI:10.1016/j.ijpara.2003.12.002.CrossRefGoogle Scholar
Mo, T. A. ( 1988). Gyrodactylusundersøkelser av fisk i forbindelse med rotenonbehandlingen av Skibotnelva i august 1988. Gyrodactylusundersøkelsene ved Zoologisk Museum, Universitetet i Oslo 1–14. (In Norwegian.)
Mo, T. A. ( 1991 a). Seasonal variations of opisthaptoral hard parts of Gyrodactylus salaris Malmberg, 1957 (Monogenea: Gyrodactylidae) on parr of Atlantic salmon Salmo salar L. in River Batnfjordselva, Norway. Systematic Parasitology 19, 231–240.Google Scholar
Mo, T. A. ( 1991 b). Variations of opisthaptoral hard parts of Gyrodactylus salaris Malmberg, 1957 (Monogenea: Gyrodactylidae) on parr of Atlantic salmon Salmo salar L. in laboratory experiments. Systematic Parasitology 20, 11–20.Google Scholar
Mo, T. A. ( 1991 c). Variations of opisthaptoral parts of Gyrodactylus salaris Malmberg, 1957 (Monogenea: Gyrodactylidae) on rainbow trout Oncorhynchus mykiss (Walbaum, 1792) in a fish farm, with comments on the spreading of the parasite in south-eastern Norway. Systematic Parasitology 20, 1–9.Google Scholar
Mo, T. A. ( 1993). Seasonal variations of the opisthaptoral hard parts of Gyrodactylus derjavini Mikailov, 1975 (Monogenea: Gyrodactylidae) on brown trout Salmo trutta L. parr and Atlantic salmon S. salar L. parr in the River Sandvikselva, Norway. Systematic Parasitology 26, 225–231.Google Scholar
Olstad, K., Cable, J., Robertsen, G. and Bakke, T. A. ( 2006). Unpredicted transmission strategy of Gyrodactylus salaris (Monogenea: Gyrodactylidae): survival and infectivity of parasites on dead hosts. Parasitology 133, 33–41. doi: 10.1017/5003118200600966.CrossRefGoogle Scholar
Poulin, R. ( 2002). The evolution of monogenean diversity. International Journal for Parasitology 32, 245–254.CrossRefGoogle Scholar
Robertsen, G. ( 2005). Taxonomy and systematics of Gyrodactylus salaris (Monogenea, Gyrodactylidae) infecting wild populations of Arctic charr (Salvelinus alpinus) in Norway. Cand. scient. thesis in Zoology, University of Oslo pp. 1–41.
Shinn, A. P., Gibson, D. I. and Sommerville, C. ( 2001). Morphometric discrimination of Gyrodactylus salaris Malmberg (Monogenea) from species of Gyrodactylus parasitizing British salmonids using novel parameters. Journal of Fish Diseases 24, 83–97.CrossRefGoogle Scholar
Shinn, A. P., Hansen, H., Olstad, K., Bachmann, L. and Bakke, T. A. ( 2004). The use of morphometric characters to discriminate specimens of laboratory-reared and wild populations of Gyrodactylus salaris and G. thymalli (Monogenea). Folia Parasitologica 51, 239–252.CrossRefGoogle Scholar
Soleng, A., Jansen, P. and Bakke, T. A. ( 1999). Transmission of the monogenean Gyrodactylus salaris. Folia Parasitologica 46, 179–184.Google Scholar
Sterud, E. ( 1999). Parasitter hos norske ferskvannsfisk. Norsk Zoologisk Forening. 7, 1–22. (In Norwegian.)Google Scholar
Sterud, E., Mo, T. A., Collins, C. M. and Cunningham, C. O. ( 2002). The use of host specificity, pathogenicity, and molecular markers to differentiate between Gyrodactylus salaris Malmberg, 1957 and G. thymalli Zitnan, 1960 (Monogenea: Gyrodactylidae). Parasitology 124, 203–213. DOI: 10.1017/S0031182001001044.CrossRefGoogle Scholar
Ziętara, M. S. and Lumme, J. ( 2002). Speciation by host switch and adaptive radiation in a fish parasite genus Gyrodactylus (Monogenea: Gyrodactylidae). Evolution 56, 2445–2458. DOI:10.1554/0014-3820(2002)056[2445:SBHSAA]2.0.CO;2.CrossRefGoogle Scholar
Ziętara, M. S. and Lumme, J. ( 2003). The crossroads of molecular, typological and biological species concepts: two new species of Gyrodactylus Nordmann, 1832 (Monogenea: Gyrodactylidae). Systematic Parasitology 55, 39–52.CrossRefGoogle Scholar