Skip to main content
Log in

First description of the adult stage of Clinostomum cutaneum Paperna, 1964 (Digenea: Clinostomidae) from grey herons Ardea cinerea L. and a redescription of the metacercaria from the Nile tilapia Oreochromis niloticus niloticus (L.) in Kenya

  • Published:
Systematic Parasitology Aims and scope Submit manuscript

Abstract

The combined use of morphological and molecular studies allowed for the first time the recognition and description of the adult stage of Clinostomum cutaneum Paperna, 1964 from the grey heron Ardea cinerea L. in Kenya. A redescription of the metacercaria that infect Nile tilapia Oreochromis niloticus niloticus (L.) from the same aquatic environment is also presented. C. cutaneum differs from all other species of Clinostomum Leidy, 1856 in the shape of its uterus. Sequencing the rRNA confirmed the morphological similarity between adults from the grey heron and the metacercarial stage from tilapia, and a level of genetic similarity with the other previously sequenced Clinostomum spp. was observed. The need for a reorganisation of Clinostomum using both morphological and molecular methods is highlighted.

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
Figs. 2–5
Fig. 6
Figs. 7-10

Similar content being viewed by others

References

  • Altschul, S. F., Gish, W., Miller, W., Myers, E. W., & Lipman, D. J. (1990). Basic local alignment search tool. Journal of Molecular Biology, 215, 403–410.

    CAS  PubMed  Google Scholar 

  • Bullard, S. A., & Overstreet, R. M. (2008). Digeneans as enemies of fishes. In J. C. Eiras, H. Segner, T. Wahli, & B. G. Kapoor (Eds.), Fish diseases. Vol. 2. Enfield, NH: Science Publishers, pp. 817–976.

    Google Scholar 

  • Coleman, A. W. (2003). ITS2 is a double-edged tool for eukaryote evolutionary comparisons. Trends in Genetics, 19, 370–375.

    Article  CAS  PubMed  Google Scholar 

  • Cribb, T. H., Anderson, G. R., Adlard, R. D., & Bray, R. A. (1998). A DNA-based demonstration of a three-host life-cycle for the Bivesiculidae (Platyhelminthes: Digenea). International Journal for Parasitology, 28, 1791–1795.

    Article  CAS  PubMed  Google Scholar 

  • Dubois, G. (1930). Trematoda. Matériaux de la mission scientifique Suisse en Angola. Bulletin Société Neuchâteloise des Sciences Naturelles, 54, 61–72.

    Google Scholar 

  • Dvořák, J., Vanácová, Š., Hampl, V., Flegr, J., & Horák, P. (2002). Comparison of European Trichobilharzia species based on ITS1 and ITS2 sequences. Parasitology, 124, 307–313.

    PubMed  Google Scholar 

  • Dzikowski, R., Levy, M. G., Poore, M. F., Flowers, J. R., & Paperna, I. (2004). Clinostomum complanatum and Clinostomum marginatum (Rudolphi, 1819) (Digenea: Clinostomidae) are separate species based on differences in ribosomal DNA. Journal of Parasitology, 90, 413–414.

    Article  CAS  PubMed  Google Scholar 

  • Feizullaev, N. A., & Mirzoeva, S. S. (1983). Revision of the Superfamily Clinostomoidea and analysis of its system. Parazitologiya, 17, 3–11 (in Russian).

    Google Scholar 

  • Finkelman, S. (1988). Infections of Clinostomatidea in the Sea of Galilee fish. MSc Thesis, Hebrew University of Jerusalem, 62 pp. (in Hebrew, English summary).

  • Galazzo, D. E., Dayanandan, S., Marcogliese, D. J., & McLaughlin, J. D. (2002). Molecular systematics of some North American species of Diplostomum (Digenea) based on rDNA-sequence data and comparisons with European congeners. Canadian Journal of Zoology, 80, 2207–2217.

    Article  CAS  Google Scholar 

  • Hershkovitz, M. A., & Lewis, L. A. (1996). Deep-level diagnostic value of the rDNA-ITS region. Molecular Biology and Evolution, 13, 1276–1295.

    CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Jousson, O., & Bartoli, P. (2002). Species diversity among the genus Monorchis (Digenea: Monorchiidae) parasitic in marine teleosts: Molecular, morphological and morphometrical studies with a description of Monorchis blennii n. sp. Parasitology Research, 88, 230–241.

    Article  CAS  PubMed  Google Scholar 

  • Kane, R. A., Ridgers, I. L., Johnston, D. A., & Rollinson, D. (1996). Repetitive sequences within the first internal transcribed spacer of ribosomal DNA in schistosomes contain a Chi-like site. Molecular and Biochemical Parasitology, 75, 265–269.

    Article  CAS  PubMed  Google Scholar 

  • Kane, R. A., & Rollinson, D. (1994). Repetitive sequences in the ribosomal DNA internal transcribed spacer of Schistosoma haematobium, Schistosoma intercalatum and Schistosoma mattheei. Molecular and Biochemical Parasitology, 63, 153–156.

    Article  CAS  PubMed  Google Scholar 

  • Kanev, I., Radev, V., & Fried, B. (2002). Family Clinostomidae Lühe, 1901. In: D. I. Gibson, A. Jones, & R. A. Bray (Eds.), Keys to the Trematoda (Vol. 1). Wallingford, UK: CAB International and the Natural History Museum, pp. 113–120.

    Google Scholar 

  • Lockyer, A. E., Olson, P. D., Ostergaard, P., Rollinson, D., Johnston, D. A., Attwood, S. W., et al. (2003). The phylogeny of the Schistosomatidae based on three genes with emphasis on the interrelationships of Schistosoma Weinland, 1858. Parasitology, 126, 203–224.

    Article  CAS  PubMed  Google Scholar 

  • Luton, K., Walker, D., & Blair, D. (1992). Comparisons of ribosomal internal transcribed spacers from two congeneric species of flukes (Platyhelminthes: Trematoda: Digenea). Molecular and Biochemical Parasitology, 56, 323–328.

    Article  CAS  PubMed  Google Scholar 

  • Mariaux, J. (1998). A molecular phylogeny of the Eucestoda. The Journal of Parasitology, 84, 114–124.

    Article  CAS  PubMed  Google Scholar 

  • Matthews, D., & Cribb, T. H. (1998). Digenetic trematodes of the genus Clinostomum Leidy, 1856 (Digenea: Clinostomidae) from birds of Queensland, Australia, including C. wilsoni n. sp. from Egretta intermedia. Systematic Parasitology, 39, 199–208.

    Article  Google Scholar 

  • Morgan, J. A. T., & Blair, D. (1995). Nuclear rDNA ITS sequence variation in the trematode genus Echinostoma: An aid to establishing relationships within the 37-collar-spine group. Parasitology, 111, 609–615.

    Article  CAS  PubMed  Google Scholar 

  • Nolan, M. J., & Cribb, T. H. (2004). The life cycle of Paracardicoloides yamagutii Martin, 1974 (Digenea: Sanguinicolidae). Folia Parasitologica, 51, 320–326.

    PubMed  Google Scholar 

  • Nolan, M. J., & Cribb, T. H. (2005). The use and implications of ribosomal DNA sequencing for the discrimination of digenean species. Advances in Parasitology, 60, 101–163.

    Article  PubMed  Google Scholar 

  • Olsen, W. O. (1974). Animal parasites: Their life cycles and ecology. Baltimore: University Park Press, 562 pp.

    Google Scholar 

  • Olson, P. D., Cribb, T. H., Tkach, V. V., Bray, R. A., & Littlewood, D. T. J. (2003). Phylogeny and classification of the Digenea (Platyhelminthes: Trematoda). International Journal for Parasitology, 33, 733–755.

    Article  CAS  PubMed  Google Scholar 

  • Paperna, I. (1964a). Parasitic helminths of inland-water fishes in Israel. Israel Journal of Zoology, 13, 1–26.

    Google Scholar 

  • Paperna, I. (1964b). The metazoan parasite fauna of Israel inland water fishes. Bamidgeh, 16, 3–66.

    Google Scholar 

  • Pritchard, M. H., & Kruse, G. (1982). The collection and preservation of animal parasites. Lincoln, NE: University of Nebraska Press, 147 pp.

    Google Scholar 

  • Suh, Y., Thien, L. B., & Zimmer, E. A. (1992). Nucleotide sequences of the internal transcribed spacers and 5.8s rRNA gene in Canella winterana (Magnoliales; Canellaceae). Nucleic Acids Research, 20, 6101–6102.

    Article  CAS  PubMed  Google Scholar 

  • 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  CAS  PubMed  Google Scholar 

  • Troitsky, A. V., & Bobrova, V. K. (1986). 23s rRNA-derived small ribosomal RNAs: Their structure and evolution with references to plant phylogeny. In S. K. Dutta (Ed.), DNA systematics. Vol 2. Plants. Boca Raton, FL: CRC Press, pp. 137–170.

    Google Scholar 

  • Troitsky, A. V., Melekhovets, Y. E., Rakhimova, G. M., Bobrova, V. K., Valiejo-Roman, K. M., & Antonov, A. S. (1991). Angiosperm origins and early stages of seed plant evolution deduced from rRNA sequences. Journal of Molecular Evolution, 32, 253–261.

    Article  CAS  PubMed  Google Scholar 

  • Ukoli, F. M. A. (1966). On Clinostomum tilapiae n. sp., and C. phalacrocoracis Dubois, 1931 from Ghana, and a discussion of the systematics of the genus Clinostomum Leidy, 1856. Journal of Helminthology, 40, 187–214.

    Article  CAS  PubMed  Google Scholar 

  • Van Herwerden, L., Blair, D., & Agatsuma, T. (1998). Intra- and interspecific variation in nuclear ribosomal internal transcribed spacer 1 of the Schistosoma japonicum species complex. Parasitology, 116, 311–317.

    Article  PubMed  Google Scholar 

  • Yamaguti, S. (1971). Synopsis of digenetic trematodes of vertebrates. Vol. 1. Tokyo: Keigaku Publishing Co., 1074 pp.

    Google Scholar 

Download references

Acknowledgements

The authors gratefully acknowledge funding from the European Community under the sixth Framework Programme for Specific Targeted Research Project for the Integrated Project BOMOSA, INCO-CT-2006-032103. Disclaimer: the views expressed in this publication are the sole responsibility of the authors and do not necessarily reflect the views of the European Commission. Neither the European Commission nor any person acting on behalf of the Commission is responsible for the use which might be made of the information contained herein.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Andrea Gustinelli.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Gustinelli, A., Caffara, M., Florio, D. et al. First description of the adult stage of Clinostomum cutaneum Paperna, 1964 (Digenea: Clinostomidae) from grey herons Ardea cinerea L. and a redescription of the metacercaria from the Nile tilapia Oreochromis niloticus niloticus (L.) in Kenya. Syst Parasitol 76, 39–51 (2010). https://doi.org/10.1007/s11230-010-9231-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11230-010-9231-5

Keywords

Navigation