Hostname: page-component-586b7cd67f-l7hp2 Total loading time: 0 Render date: 2024-11-29T22:19:20.988Z Has data issue: false hasContentIssue false
  • English
  • Français

Characterization of a Gyrodactylus salaris variant: infection biology, morphology and molecular genetics

Published online by Cambridge University Press:  09 October 2003

T. LINDENSTRØM ,
C. M. COLLINS ,
J. BRESCIANI ,
C. O. CUNNINGHAM  and
K. BUCHMANN
T. LINDENSTRØM
Affiliation:
Department of Veterinary Microbiology, Laboratory of Fish Diseases, Royal Veterinary and Agricultural University (RVAU), Stigbøjlen 4, DK-1870 Frederiksberg C., Denmark
C. M. COLLINS
Affiliation:
FRS Marine Laboratory, P.O. Box 101, Victoria Road, Aberdeen AB11 9DB, Scotland, UK
J. BRESCIANI
Affiliation:
Department of Ecology, Zoology Section, RVAU, Thorvaldsensvej 40, DK-1871 Frederiksberg C., Denmark
C. O. CUNNINGHAM
Affiliation:
FRS Marine Laboratory, P.O. Box 101, Victoria Road, Aberdeen AB11 9DB, Scotland, UK
K. BUCHMANN
Affiliation:
Department of Veterinary Microbiology, Laboratory of Fish Diseases, Royal Veterinary and Agricultural University (RVAU), Stigbøjlen 4, DK-1870 Frederiksberg C., Denmark
Get access Rights & Permissions [Opens in a new window]

Abstract

A laboratory population of a Danish Gyrodactylus salaris variant founded by 1 single specimen was established and infection studies performed. Rainbow trout as well as Atlantic salmon of 3 different stocks were infected both in cohabitation systems and as single-parasite infections on isolated hosts. Both infection systems revealed that this particular morphotype exhibits low virulence towards Atlantic salmon. Thus, in isolated hosts, the parasites could either not establish or only reproduce to a limited degree on salmon. Rainbow trout, in contrast, proved to be rather susceptible to infection with this G. salaris variant and abundances on this host species always attained significantly higher values in cohabitation systems compared to salmon. Detailed morphological examination confirmed the very high resemblance to G. salaris (sensu stricto), as the range of variation in sclerite characters of the morphotype is almost fully covered by the total range of variation reported for reference G. salaris. Morphological similarities to the closely related congeneric species G. bohemicus were noted. Molecular studies, however, showed that the morphotype most likely represents a G. salaris variant, as it differed only slightly from G. salaris sensu Malmberg, 1957, which is also known to inhabit Danish watercourses. The genomic target region investigated does not allow us to rule out the possibility that it represents a variant form of G. thymalli. Sequences of the ribosomal RNA internal transcribed spacer (ITS) revealed that single individuals contained 2 different ITS sequences, one identical to reference sequence of G. salaris while the other differed at 3 positions. This can be interpreted as an example of a hybrid or, more likely, as intra-individual variation of ITS within single individuals. As one of the nucleotide changes in the variant ITS affects an Hae III restriction site, the current G. salaris variant can be distinguished from G. salaris sensu Malmberg by RFLP diagnosis.

Keywords

Gyrodactylus salaris variantsusceptibilityOncorhynchus mykissSalmo salarITS polymorphism
Type
Research Article
Information
Parasitology , Volume 127 , Issue 2 , August 2003 , pp. 165 - 177
Copyright
2003 Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

AGATSUMA, T., ARAKAWA, Y., IWAGAMI, M., HONZAKO, Y., CAHYANINGSIH, U., KANG, SHIN-YONG & HONG, SUNG-JONG (2000). Molecular evidence of natural hybridisation between Fasciola hepatica and F. gigantica. Parasitology International 49, 231–238.CrossRefGoogle Scholar
ALLENDORF, F. W., RYMAN, N. & UTTER, F. M. (1987). Genetics and the fishery management. In Population Genetics and Fishery Management (ed. Ryman, N. & Utter, F.), pp. 1–19. University of Washington Press, Seattle.
APPLEBY, C. & MO, T. A. (1997). Population dynamics of Gyrodactylus salaris (Monogenea) infecting Atlantic salmon, Salmo salar, parr in the River Batnfjordselva, Norway. Journal of Parasitology 83, 23–30.CrossRefGoogle Scholar
BAKKE, T. A., HARRIS, P. D. & CABLE, J. (2002). Host specificity dynamics: observation on gyrodactylid monogeneans. International Journal for Parasitology 32, 281–308.CrossRefGoogle Scholar
BAKKE, T. A., HARRIS, P. D., JANSEN, P. A. & HANSEN, L. P. (1992 a). Host specificity and dispersal in gyrodactylid monogeneans, with particular reference to Gyrodactylus salaris (Platyhelminthes, Monogenea). Diseases of Aquatic Organisms 13, 63–74.Google Scholar
BAKKE, T. A., HARRIS, P. D. & JANSEN, P. A. (1992 b). The susceptibility of Salvelinus fontinalis (Mitchill) to Gyrodactylus salaris Malmberg (Platyhelminthes; Monogenea) under experimental conditions. Journal of Fish Biology 41, 499–507.Google Scholar
BAKKE, T. A., JANSEN, P. A. & HANSEN, L. P. (1990). Differences in the host resistance of Atlantic salmon, Salmo salar L., stocks to the monogenean Gyrodactylus salaris Malmber, 1957. Journal of Fish Biology 37, 577–587.Google Scholar
BAKKE, T. A., JANSEN, P. A. & HANSEN, L. P. (1991 b). Experimental transmission of Gyrodactylus salaris Malmberg (Platyhelminthes, Monogenea) from the Atlantic salmon (Salmo salar) to the European eel (Anguilla anguilla). Canadian Journal of Zoology 69, 733–737.Google Scholar
BAKKE, T. A., JANSEN, P. A. & KENNEDY, C. R. (1991 a). The host specificity of Gyrodactylus salaris Malmberg (Platyhelminthes, Monogenea): susceptibility of Oncorhynchus mykiss (Walbaum) under experimental conditions. Journal of Fish Biology 39, 45–57.Google Scholar
BAKKE, T. A., JANSEN, P. A. & HARRIS, P. D. (1996). Differences in susceptibility of anadromous and resident stocks of Arctic char to infections of Gyrodactylus salaris under experimental conditions. Journal of Fish Biology 49, 341–351.Google Scholar
BAKKE, T. A. & MacKENZIE, K. (1993). Comparative susceptibility of native Scottish and Norwegian stocks of Atlantic salmon, Salmo salar L., to Gyrodactylus salaris Malmberg: Laboratory experiments. Fisheries Research 17, 69–85.Google Scholar
BAKKE, T. A., SOLENG, A. & HARRIS, P. D. (1999). The susceptibility of Atlantic salmon (Salmo salar L.)×brown trout (Salmo trutta L.) hybrids to Gyrodactylus salaris Malmberg and Gyrodactylus derjavini Mikailov. Parasitology 119, 467–481.Google Scholar
BUCHMANN, K. & BRESCIANI, J. (1997). Parasitic diseases in pond-reared rainbow trout. Diseases of Aquatic Organisms 28, 125–138.CrossRefGoogle Scholar
BUCHMANN, K. & BRESCIANI, J. (1998). Microenvironment of Gyrodactylus derjavini on rainbow trout Oncorhynchus mykiss: association between mucous cells density in skin and site selection. Parasitology Research 84, 17–24.Google Scholar
BUCHMANN, K., LINDENSTRØM, T., NIELSEN, M. E. & BRESCIANI, J. (2000). Diagnosis and occurrence of ectoparasite infections (Gyrodactylus spp.) in Danish salmonids. Dansk Veterinœr Tidsskrift (in Danish) 83, 15–19.Google Scholar
BUCHMANN, K. & ULDAL, A. (1997). Gyrodactylus derjavini infections in four salmonids: comparative host susceptibility and site selection of parasites. Diseases of Aquatic Organisms 28, 13–22.Google Scholar
BUSH, A. O., LAFFERTY, K. D., LOTZ, J. M. & SHOSTAK, A. W. (1997). Parasitology meets ecology on its own terms: Margolis et al. revisited. Journal of Parasitology 83, 575–583.CrossRefGoogle Scholar
CUNNINGHAM, C. O. (1997). Species variation within the internal transcribed spacer (ITS) region of Gyrodactylus (Monogenea) ribosomal RNA genes. Journal of Parasitology 83, 215–219.CrossRefGoogle Scholar
CUNNINGHAM, C. O., ALIESKY, H. & COLLINS, C. M. (2000). Sequence and secondary structure variation in the Gyrodactylus (Platyhelminthes: Monogenea) ribosomal RNA gene array. Journal of Parasitology 86, 567–576.CrossRefGoogle Scholar
CUNNINGHAM, C. O., McGILLIVRAY, D. M., MacKENZIE, K. & MELVIN, W. T. (1995). Discrimination between Gyrodactylus salaris, G. derjavini, and G. truttae (Platyhelminthes: Monogenea) using restriction fragment length polymorphisms and an oligonucleotide probe within the small subunit ribosomal RNA gene. Parasitology 111, 87–94.Google Scholar
CUNNINGHAM, C. O., MO, T. A., COLLINS, C. M., BUCHMANN, K., THIERY, R., BLANC, G. & 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
ERGENS, R. (1992). Gyrodactylus bohemicus sp. n. (Monogenea: Gyrodactylidae) from Oncorhynchus mykiss (Walbaum) and Salvelinus fontinalis (Mitchill) (Clupeiformes: Salmonidae) in Czechoslovakia. Folia Parasitologica 39, 391–394.Google Scholar
HARRIS, P. D., CABLE, J., TINSLEY, R. C. & 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., JANSEN, P. A. & BAKKE, T. A. (1994). The population age structure and reproductive biology of Gyrodactylus salaris Malmberg (Monogenea). Parasitology 108, 167–173.CrossRefGoogle Scholar
HUDSON, E. B. & HILL, B. J. (1993). EC Directive 91/67/EEC and its relevance to diseases in wild salmonids. Fisheries Research 17, 229–236.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). Parasitology 102, 105–112.CrossRefGoogle Scholar
JANSEN, P. A. & BAKKE, T. A. (1995). Susceptibility of brown trout to Gyrodactylus salaris (Monogenea) under experimental conditions. Journal of Fish Biology 46, 415–422.CrossRefGoogle Scholar
JENSEN, A. & JOHNSEN, B. O. (1992). Site specificity of Gyrodactylus salaris Malmberg, 1957 (Monogenea) on Atlantic salmon (Salmo salar L.) in the River Lakselva, northern Norway. Canadian Journal of Zoology 70, 264–267.Google Scholar
JOHNSEN, B. O. & JENSEN, A. (1991). The Gyrodactylus story in Norway. Aquaculture 98, 289–302.CrossRefGoogle Scholar
KAY, J. W., SHINN, A. P. & SOMMERVILLE, C. (1999). Towards an automated system for the identification of notifiable pathogens: Using Gyrodactylus salaris as an example. Parasitology Today 15, 201–206.CrossRefGoogle Scholar
LINDENSTRØM, T., NIELSEN, M. E. & BUCHMANN, K. (1999). Gyrodactylids on salmonids from Danish streams. Proceedings of the Symposium Dedicated to the 90th Anniversary of the Birthday of Academician B. E. Bychowsky. Systematics and Phylogeny of Plathyhelminthes, St. Petersburg, Russia, pp. 62–64.
MALMBERG, G. (1970). The excretory systems and the marginal hooks as a basis for the systematics of Gyrodactylus (Trematoda, Monogenea). Archiv för Zoologie 23, 1–235.Google Scholar
MALMBERG, G. (1987). Increased intraspecific divergence in Gyrodactylus salaris resulting from genetic drift in fish farm populations. Information, Åbo Akademi 19, 33.Google Scholar
MATEJUSOVÁ, I., GELNAR, M., McBEATH, A. J. A., COLLINS, C. M. & CUNNINGHAM, C. O. (2001). Molecular markers for gyrodactylids (Gyrodactylidae: Monogenea) from five fish families (Teleostei). International Journal for Parasitology 31, 738–745.CrossRefGoogle Scholar
McHUGH, E. S., SHINN, A. P. & KAY, J. W. (2000). Discrimination of the notifiable pathogen Gyrodactylus salaris (Monogenea) using statistical classifiers applied to morphometric data. Parasitology 121, 315–323.CrossRefGoogle Scholar
MO, T. A. (1991). Variations of opisthaptoral hard 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.CrossRefGoogle Scholar
MO, T. A. (1992). Seasonal variations in the prevalence and infection intensity of Gyrodactylus salaris Malmberg, 1957 (Monogenea, Gyrodactylidae) on Atlantic salmon parr, Salmo salar L., in the River Batnfjordselva, Norway. Journal of Fish Biology 41, 697–707.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. and Atlantic salmon S. salar L. parr in the River Sandvikselva, Norway. Systematic Parasitology 26, 225–231.Google Scholar
NIELSEN, C. V. & BUCHMANN, K. (2001). Occurrence of Gyrodactylus parasites in Danish fish farms. Bulletin of the European Association of Fish Pathologists 21, 19–25.Google Scholar
SÁNCHEZ, J. G., SPEARE, D. J., MARKHAM, R. J. F. & JONES, S. R. M. (2001). Isolation of a Loma salmonae variant: biological characteristics and host range. Journal of Fish Biology 59, 427–441.CrossRefGoogle Scholar
SHINN, A. P., GIBSON, D. I. & SOMMERVILLE, C. (1997). Argentophillic structures as a diagnostic criterion for the discrimination of species of the genus Gyrodactylus von Nordmann (Monogenea). Systematic Parasitology 37, 47–57.CrossRefGoogle Scholar
SOLENG, A. & BAKKE, T. A. (2001). The susceptibility of grayling (Thymallus thymallus) to experimental infections with the monogenean Gyrodactylus salaris. International Journal for Parasitology 31, 793–797.CrossRefGoogle Scholar
SOLENG, A., BAKKE, T. A. & HANSEN, L. P. (1998). Potential for dispersal of Gyrodactylus salaris (Platyhelminthes, Monogenea) by sea-running stages of the Atlantic salmon (Salmo salar): field and laboratory studies. Canadian Journal of Fisheries and Aquatic Sciences 55, 507–514.CrossRefGoogle Scholar
SOLENG, A., JANSEN, P. A. & BAKKE, T. A. (1999). Transmission of the monogenean Gyrodactylus salaris. Folia Parasitologica 46, 179–184.Google Scholar
STERUD, E., MO, T. A., COLLINS, C. M. & CUNNINGHAM, C. O. (2002). The use of host specificity, pathogenicity and molecular markers to differentiate between Gyrodactylus salaris Malmberg, 1957 and G. thymalli Žitňan, 1960 (Monogenea, Gyrodactylidae). Parasitology 124, 203–214.Google Scholar
STÅHL, G. (1983). Differences in the amount and distribution of genetic variation between natural populations and hatchery stocks of the Atlantic salmon. Aquaculture 33, 23–32.CrossRefGoogle Scholar
VAN HERWERDEN, L., BLAIR, D. & AGATSUMA, T. (1999). Intra- and interindividual variation in ITS1 of Paragonimus westermani (Trematoda: Digenea) and related species: Implications for phylogenetic studies. Molecular Phylogenetics and Evolution 12, 67–73.CrossRefGoogle Scholar
ZIĘTARA, M. S., HUYSE, T., LUMME, J. & VOLCKAERT, F. A. (2002). Deep divergence among subgenera of Gyrodactylus inferred from rDNA ITS region. Parasitology 124, 39–52.CrossRefGoogle Scholar