Skip to main content
Log in

Histological and molecular studies of species of Myxobolus Bütschli, 1882 (Myxozoa: Myxosporea) in the gills of Abramis, Blicca and Vimba spp. (Cyprinidae), with the redescription of M. macrocapsularis Reuss, 1906 and M. bliccae Donec & Tozyyakova, 1984

  • Published:
Systematic Parasitology Aims and scope Submit manuscript

Abstract

Although Myxobolus spp. from cyprinid fishes are generally characterised by a strict host-specificity, this study has found that the breams Abramis brama (L.), Blicca bjoerkna (L.) and Vimba vimba (L.) may be infected by the same Myxobolus spp. It is demonstrated that M. macrocapsularis Reuss, 1906, a parasite of the gill filaments of B. bjoerkna, can also infect A. brama. In the same way, M. bliccae Donec & Tozyyakova, 1984, also a parasite of B. bjoerkna, can also occur in V. vimba. The molecular sequences of M. macrocapsularis spores from B. bjoerkna and A. brama were 100% identical. Two of the 18S rDNA sequences of three replicate samples of M. bliccae from B. bjoerkna were 100% identical, whereas the third sequence exhibited a 99.7% similarity with sequences from V. vimba. M. bliccae sequences of spores collected from V. vimba showed a 99.8% similarity to the first two isolates and 99.6% to the third. Data obtained by morphological, histological and molecular biological methods all suggest that Myxobolus spp., known for their strict host-specificity, may sometimes infect several closely related cyprinids.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Figs. 4–5
Fig. 6
Figs. 7–8
Fig. 9

Similar content being viewed by others

References

  • Andree, K. B., Székely, Cs., Molnár, K., Gresoviac, S. J., & Hedrick, R. P. (1999). Relationships among members of the genus Myxobolus (Myxozoa: Bivalvidae) based on small subunit ribosomal RNA sequences. Journal of Parasitology, 85, 68–74.

    Article  PubMed  CAS  Google Scholar 

  • Blazer, V. S., Densmore, C. L., Schill, W. B., Cartwright, D. D., & Page, S. J. (2004). Comparative susceptibility of Atlantic salmon, lake trout and rainbow trout to Myxobolus cerebralis in controlled laboratory exposures. Diseases of Aquatic Organisms, 58, 27–34.

    Article  PubMed  CAS  Google Scholar 

  • Bogutskaya, N. G. (1986). A contribution to the question of taxonomic relations of species from the genera Abramis, Blicca and Vimba (Cyprinidae). Voprosy Ikhtiologii, 26, 576–584. [In Russian.].

    Google Scholar 

  • Briolay, J., Galtier, N., Brito, R. M., & Bouvet, Y. (1998). Molecular phylogeny of Cyprinidae inferred from cytochrome b DNA sequences. Molecular Phylogenetics and Evolution, 9, 100–108.

    Article  PubMed  CAS  Google Scholar 

  • Chevenet, F., Brun, C., Banuls, A. L., Jacq, B., & Christen, R. (2006). TreeDyn: towards dynamic graphics and annotations for analyses of trees. BMC Bioinformatics, 10, 439.

    Article  Google Scholar 

  • Cone, D. K., & Overstreet, R. M. (1998). Species of Myxobolus (Myxozoa) from the bulbus arteriosus of centrarchid fishes in North America, with a description of two new species. Journal of Parasitology, 84, 371–374.

    Article  PubMed  CAS  Google Scholar 

  • Dereeper, A., Guignon, V., Blanc, G., Audic, S., Buffet, S., Chevenet, F., Dufayard, J. F., Guindon, S., Lefort, V., Lescot, M., Claverie, J. M., & Gascuel, O. (2008). Phylogeny.fr: robust phylogenetic analysis for the non-specialist. Nucleic Acids Research, 1, 36 (Web Server issue): W465–9. Epub 2008 Apr 19.

  • Dogiel, V. A. (1948). Parasitic protozoa of fishes in the Bay of Peter the Great. Bulletin of the Institute of Freshwater Fisheries, Leningrad, 27, 17–66. [In Russian.]

    Google Scholar 

  • Donec, Z. S. (1964). Myxosporidians (Myxosporidia) of freshwater fishes of Ukrainian SSR. Candidate of Sciences Dissertation. Autoreferation of the Allunion Scientific Research Institute of Lake and River Fisheries, 17 pp. (In Russian)

  • Donec, Z. S., & Shulman, S. S. (1984). Cnidosporidia. In: Bauer, O. N. (Ed.) Key to the parasites of freshwater fishes of the USSR. Leningrad: Nauka, Vol. 1. pp. 88–251. [In Russian.]

  • Dyková, I., & Lom, J. (2007). Histopathology of protistan and myxozoan infections in fishes. Prague: Academia, 219 pp.

  • Eiras, J. C., Molnár, K., & Lu, Y. S. (2005). Synopsis of the genus Myxobolus Bütschli, 1882 (Myxozoa: Myxosporea). Systematic Parasitology, 61, 1–46.

    Article  PubMed  CAS  Google Scholar 

  • Eszterbauer, E. (2004). Genetic relationship among gill-infecting Myxobolus species (Myxosporea) of cyprinids: molecular evidence of importance of tissue-specificity. Diseases of Aquatic Organisms, 58, 35–40.

    Article  PubMed  Google Scholar 

  • Eszterbauer, E., & Székely, Cs. (2004). Molecular phylogeny of the kidney-parasitic Sphaerospora renicola from common carp (Cyprinus carpio) and Sphaerospora sp. from goldfish (Carassius auratus auratus). Acta Veterinaria Hungarica, 52, 469–478.

    Article  PubMed  CAS  Google Scholar 

  • Eszterbauer, E., Székely, Cs., Molnár, K., & Baska, F. (2000). Development of Myxobolus bramae (Myxosporea: Myxobolidae) in oligochaete alternate host, Tubifex tubifex. Journal of Fish Diseases, 23, 19–25.

    Article  Google Scholar 

  • Ferguson, J. A., Atkinson, S. D., Whipps, C. M., & Kent, M. L. (2008). Molecular and morphological analysis of Myxobolus spp. of Salmonid fishes with the description of a new Myxobolus species. J. Parasitol., 94, 1322–1334.

    Article  PubMed  Google Scholar 

  • Guindon, S., & Gascuel, O. (2003). A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Systematic Biology, 52, 696–704.

    Article  PubMed  Google Scholar 

  • Hall, T. A. (1999). BioEdit: A user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series, 41, 95–98.

    CAS  Google Scholar 

  • Hedrick, R. P., McDowell, T. S., Mukkatira, K., Georgiadis, M. P., & MacConnell, E. (2001). Susceptibility of three species of anadromous salmonids to experimentally induced infectious with Myxobolus cerebralis, the causative agent of whirling disease. Journal of Aquatic Animal Health, 13, 43–50.

    Article  Google Scholar 

  • Higgins, D., Thompson, J., Gibson, T., Thompson, J. D., Higgins, D. G., & Gibson, T. J. (1994). CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Research, 22, 4673–4680.

    Article  PubMed  Google Scholar 

  • Hillis, D. M., & Dixon, T. (1991). Ribosomal DNA: Molecular evolution and phylogenetic inference. The Quarterly Review of Biology, 66, 411–453.

    Article  PubMed  CAS  Google Scholar 

  • Huelsenbeck, J. P., & Ronquist, F. (2001). MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics, 17, 754–755.

    Article  PubMed  CAS  Google Scholar 

  • Lom, J., & Dyková, I. (1992). Protozoan parasites of fishes. Developments in aquaculture and fisheries science. Amsterdam: Elsevier, Vol. 26, 315 pp.

  • Lom, J., & Dyková, I. (2006). Myxozoan genera: definition and notes on taxonomy, life-cycle terminology and pathogenic species. Folia Parasitologica, 53, 1–36.

    PubMed  Google Scholar 

  • Longshaw, M., Frear, P., & Feist, S. W. (2005). Description, development and pathogenicity of myxozoan (Myxozoa: Myxosporea) parasites of juvenile cyprinids (Pisces: Cyprinidae). Journal of Fish Diseases, 28, 489–508.

    Article  PubMed  CAS  Google Scholar 

  • Masoumian, M., Baska, F., & Molnár, K. (1996). Myxobolus nodulointestinalis sp. n. (Myxosporea, Myxobolidae), a parasite of the intestine of Barbus sharpeyi. Diseases of Aquatic Organisms, 24, 35–39.

    Article  Google Scholar 

  • Molnár, K. (1994). Comments on the host, organ and tissue specificity of fish myxosporeans and on the types of their intrapiscine development. Parasitologica Hungarica, 27, 5–20.

    Google Scholar 

  • Molnár, K., Cech, G., & Székely, C. (2008). Infection of the heart of the common bream, Abramis brama (L.) with Myxobolus s.l. dogieli (Myxozoa, Myxobolidae). Journal of Fish Diseases, 31, 613–620.

    Article  PubMed  Google Scholar 

  • Molnár, K., Eszterbauer, E., Székely, Cs., Dán, Á., & Harrach, B. (2002). Morphological and molecular biological studies on intramuscular Myxobolus spp. of cyprinid fish. Journal of Fish Diseases, 25, 643–652.

    Article  Google Scholar 

  • Molnár, K., Marton, Sz., Eszterbauer, E., & Székely, Cs. (2006). Comparative morphological and molecular studies on Myxobolus spp. infecting chub from the River Danube, Hungary, and description of M. muellericus sp. n. Diseases of Aquatic Organisms, 73, 49–61.

    Article  PubMed  Google Scholar 

  • Molnár, K., Marton, Sz., Eszterbauer, E., & Székely, Cs. (2007). Description of Myxobolus gayerae n. sp. and redescription of Myxobolus leuciscinae infecting the European chub from the Hungarian stretch of the river Danube. Diseases of Aquatic Organisms, 78, 147–153.

    Article  PubMed  Google Scholar 

  • Molnár, K., Székely, C., Hallett, S. L., & Atkinson, S. D. (2009). Some remarks on the occurrence, host specificity and validity of Myxobolus rotundus Nemeczek, 1911 (Myxozoa: Myxosporea). Systematic Parasitology, 72, 71–79.

    Article  PubMed  Google Scholar 

  • Reuss, H. (1906). Neue Myxosporidien von Süsswasserfischen. Bulletin de l’Académie Impériale des Sciences de St-Petersbourg, Ser. T, 25, 199–205.

    Google Scholar 

  • Shulman, S. S. (1966). [Myxosporidia of the fauna of the USSR.] Moscow: Nauka, 504 pp. [In Russian.]

  • Székely, Cs., Hallett, S. L., Atkinson, S. D., & Molnár, K. (2009). Complete life cycle of Myxobolus rotundus (Myxosporea: Myxobolidae), a gill myxozoan of common bream Abramis brama. Diseases of Aquatic Organisms, 85, 147–155.

    Article  PubMed  Google Scholar 

  • Székely, Cs., Rácz, O., Molnár, K., & Eszterbauer, E. (2002). Development of Myxobolus macrocapsularis (Myxosporea: Myxobolidae) in an oligochaete alternate host, Tubifex tubifex. Diseases of Aquatic Organisms, 48, 117–123.

    Article  PubMed  Google Scholar 

  • Tamura, K., Dudley, J., Nei, M., & Kumar, S. (2007). MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Molecular Biology and Evolution, 24, 1596–1599.

    Article  PubMed  CAS  Google Scholar 

  • Zardoya, R., & Doadrio, I. (1999). Molecular evidence on the evolutionary and biogeographical patterns of European cyprinids. Journal of Molecular Evolution, 9, 227–237.

    Article  Google Scholar 

  • Zardoya, R., Economidis, P. S., & Doadrio, I. (1999). Phylogenetic relationships of Greek Cyprinidae: Molecular evidence for at least two origins of the Greek cyprinid fauna. Molecular Phylogenetics and Evolution, 13, 122–131.

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

This study was supported by the Hungarian Scientific Research Fund (OTKA, project K 71837). The authors thank Ms Györgyi Pataki for preparing the drawings and the histological slides.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Kálmán Molnár.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Molnár, K., Cech, G. & Székely, C. Histological and molecular studies of species of Myxobolus Bütschli, 1882 (Myxozoa: Myxosporea) in the gills of Abramis, Blicca and Vimba spp. (Cyprinidae), with the redescription of M. macrocapsularis Reuss, 1906 and M. bliccae Donec & Tozyyakova, 1984. Syst Parasitol 79, 109–121 (2011). https://doi.org/10.1007/s11230-011-9292-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11230-011-9292-0

Keywords

Navigation