Systematic Parasitology

, Volume 56, Issue 3, pp 163–168

Use of ITS rDNA for discrimination of European green- and brown-banded sporocysts within the genus Leucochloridium Carus, 1835 (Digenea: Leucochloriidae)

  • S.P. Casey
  • T.A. Bakke
  • P.D. Harris
  • J. Cable
Article

Abstract

Transmission of Leucochloridium species to their definitive avian hosts may be facilitated by the rhythmic movement of coloured sporocyst broodsacs in the ocular tentacles of infected snails. These broodsacs resemble caterpillars and by enticement increase the probability of predation by birds. Broodsac banding pattern and colour (green, yellow to red/brown) have traditionally formed part of the taxonomic criteria for the genus. In this study, sequence divergence of the 5.8S rDNA gene and associated internal transcribed spacers (ITS1 and ITS2) in two of the most frequently observed Leucochloridium taxa from Europe is related to broodsac type based on colour and banding pattern. The present green-banded broodsac (L. paradoxum Carus, 1835) and brown-banded broodsac forms (L. variae McIntosh, 1932) differ in ITS sequence by 6.8%, confirming their distinctness. No intraspecific differences were noted within each colour morph in specimens collected from Poland, Denmark or Norway, indicating that a single taxon of each type occurs in Europe. The significance of these findings to our understanding of metapopulation dynamics and evolutionary ecology of Leucochloridium is discussed.

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References

  1. Baer, J.G. (1971) Animal parasites. London: World Wide Laboratory, 256 pp.Google Scholar
  2. Bakke, T.A. (1972a) Studies of the helminth fauna of Norway. XXII. The common gull, Larus canus L., as final host for Digenea (Platyhelminthes). I. The ecology of the common gull and the infestation in relation to season and the gulls' habitat, together with the distribution of the parasites in the intestine. Norwegian Journal of Zoology, 20, 165–188.Google Scholar
  3. Bakke, T.A. (1972b) Studies of the helminth fauna of Norway. XXIII. The common gull, Larus canus L., as final host for Digenea (Platyhelminthes). II. The relationship between infection and sex, age and weight of the common gull. Norwegian Journal of Zoology, 20, 189–204.Google Scholar
  4. Bakke, T.A. (1978a) Intraspecific variation of adult Leucochloridium sp. (Digenea) from natural and experimental infections. Canadian Journal of Zoology, 56, 94–102.Google Scholar
  5. Bakke, T.A. (1978b) Taxonomy of Leucochloridium sp. (Digenea) infecting Succinea pfeifferi Rossmässler, 1835. Zeitschrift für Parasitenkunde, 55, 153–164.Google Scholar
  6. Bakke, T.A. (1978c) Urogonimus macrostomus (Rudolphi, 1803) (Digenea): its taxonomy andmorphology as revealed by light and scanning morphology. Canadian Journal of Zoology, 56, 2280–2291.Google Scholar
  7. Bakke, T.A. (1978d) Reproductive system of the type specimens of Urogonimus macrostomus (Rudolphi, 1803) Monticelli, 1888 (Digenea). Zoologica Scripta, 7, 19–23.Google Scholar
  8. Bakke, T.A. (1980) A revision of the family Leucochloridiidae Poche (Digenea) and studies on the morphology of Leucochloridium paradoxum Carus, 1835. Systematic Parasitology, 1, 189–202.Google Scholar
  9. Bakke, T.A. (1982) The morphology and taxonomy of Leucochloridium (L.) variae McIntosh (Digenea, Leucochloridiidae) from the Nearctic as revealed by light and scanning electron microscopy. Zoologica Scripta, 11, 87–100.Google Scholar
  10. Cable, J., Harris, P.D., Tinsley, R.C. & Lazarus, C.M. (1999) Phylogenetic analysis of Gyrodactylus spp. (Platyhelminthes: Monogenea) using ribosomal DNA sequences. Canadian Journal of Zoology, 77, 1439–1449.Google Scholar
  11. Carus, C.G. (1835) Beobachtung über einen merkwürdingen schöngefärbten Eingeweidewurm, Leucochloridium paradoxum mihi, und dessen parasitische Erzeugung in einer Landschnecke, Succinea amphibia Drap. Helix putris Linn. Nova Acta Physico-Medica Academiae Caesareae Leopoldino-Carolinae Germanicum Naturae Curiosorum, 17, 87–100.Google Scholar
  12. Chilton, N.B., Gasser, R.B. & Beveridge, I. (1995) Differences in a ribosomal DNA sequence of morphologically indistinguishable species within the Hypodontus macropi complex (Nematoda: Strongyloidea). International Journal for Parasitology, 25, 647–651.Google Scholar
  13. Cunningham, C.O., Mo, T.A., Collins, C.M., Buchmann, K., Thiery, R., Blanc, G. & Lautraite, A. (2001) Redescription of Gyrodactylus teuchis, Blanc, Thiery, Daniel & Vigneulle, 1999 (Monogenea: Gyrodactylidae): a species identified by ribosomal RNA sequence. Systematic Parasitology, 48, 141–150.Google Scholar
  14. Elder, J.F. & Turner, B.J. (1995) Concerted evolution of repetitive DNA sequences in eukaryotes. The Quarterly Review of Biology, 70, 297–320.Google Scholar
  15. Heckert, G.A. (1889) Leucochloridium paradoxum. Monographische darstellung der entwicklungs-und Lebensgeschichte des Distomum macrostomum. Bibliotheca Zoologica, 4, 1–66.Google Scholar
  16. Hohorst, W. (1937) Die 'Fühler-made' (Leucochloridium sp.) der Bernsteinschnecke, ein für die Umgebung von Frankfurt a. M. neurer Saugwurm. Natur und Volk, 67, 122–132.Google Scholar
  17. Hsü, H.F. (1936) Studien zur Systematik und Entwicklungsgeschichte der Gattung Leucochloridium Carus. II. Über zwei Leuchocloridium-arten der Kurischen Nehrung sowie über Fütterungsversuche mit Grünen Sporocysten dieser Gattung. Zeitschrift für Parasitenkunde, 8, 714–728.Google Scholar
  18. Kocher, T.D., Thomas, W.K., Meyer, A., Edwards, S.V., Pääbo, S., Villablanca, F.X. & Wilson, A.C. (1989) Dynamics of mitochondrial DNA evolution in animals: Amplification and sequencing with conserved primers. Proceedings of the National Academy of Sciences of the USA, 86, 6196–6200.Google Scholar
  19. Lewis, P.D. Jr (1974) Helminths of terrestrial molluscs in Nebraska. II. Life cycle of Leucochloridium variae McIntosh, 1932 (Digenea: Leucochloridae). Journal of Parasitology, 60, 251–255.Google Scholar
  20. Lewis, P.D. Jr (1977) Adaptations for the transmission of species of Leucochloridium from molluscan to avian hosts. Proceedings of the Montana Academy of Sciences, 37, 70–81.Google Scholar
  21. Lo, C.T. & Chen, C.P. (1973) Studies on Leucochloridium passeri Wu from Taiwan (Digenea: Leucochloridiidae). Bulletin of the Institute of Zoology, Academia Sinica (Taipei), 12, 71–77.Google Scholar
  22. Mönnig, H.O. (1922) Über Leucochloridium macrostomum (Leucochloridium paradoxum Carus), ein Beitrag zur Histologie der Trematoden. Jena: Gustav Fischer, 61 pp.Google Scholar
  23. Pojma?ska, T. (1962) On sporocysts of the genus Leucochloridium in Poland. Acta Parasitologica Polonica, 10, 369–376.Google Scholar
  24. Pojma?ska, T. (1963) Experimental development of Leucochloridium sp. (Trematoda, Brachylaemidae). Acta Parasitologica Polonica, 11, 153–159.Google Scholar
  25. Pojma?ska, T. (1967) Variability of Leucochloridium paradoxum Carus (= L. heckerti Kagan, 1952) (Trematoda: Brachylaemidae) in natural and experimental conditions. Acta Parasitologica Polonica, 14, 381–398.Google Scholar
  26. Pojma?ska, T. (1969a) Leucochloridium perturbatum sp. n. (Trematoda: Brachylaemidae), morphology, individual variability and life cycle. Acta Parasitologica Polonica, 16, 153–175.Google Scholar
  27. Pojma?ska, T. (1969b) Specific criteria in the genus Leucochloridium Carus 1835, emend. Kagan, 1952. Acta Parasitologica Polonica, 16, 185–192.Google Scholar
  28. Pojma?ska, T. (1969c) Life cycle and morphology of the adult Leucochloridium subtilis sp. n. (Trematoda: Brachylaemidae). Acta Parasitologica Polonica, 16, 176–184.Google Scholar
  29. Pojma?ska, T. (1969d) European species of Leucochloridium Carus. Acta Parasitologica Polonica, 16, 193–205.Google Scholar
  30. Pojma?ska, T. (1978) Life cycle of Leucochloridium vogtianum Baudon, 1881 (=L. phragmitophila Bykovskaja-Pavlovskaja et Dubinina, 1951 in parte) (Trematoda, Leucochloridae). Acta Parasitologica Polonica, 25, 11–20.Google Scholar
  31. Rietschel, G. (1970) Das Auftreten von 'Fühlermaden' (Leucochloridium) in Hessen. Natur und Museum, 100, 57–64.Google Scholar
  32. Rietschel, G. (1972) Untersuchungen über Farbmuster-Typen bei Leucochloridium-Sporocysten (Trematoda, Brachylaemidae) und deren Zugehörigkeit zu bestimmten Arten. Zeitschrift für Parasitenkunde, 40, 61–68.Google Scholar
  33. Rietschel, G. (1979) Vorkommen larvaler Trematoden in Bernsteinschnecken (Succineidae) Hessens. Zeitschrift für Parasitenkunde, 58, 265–274.Google Scholar
  34. Rozen, S. & Skaletsky, H.J. (1998) Primer3. http://www. genome.wi.mit.edu/genome software/other/primer3.html.Google Scholar
  35. Tkach, V.V., Pawlowski, J., Mariaux, J. & Swiderski, Z. (2001) Molecular phylogeny of the suborder Plagiorchiata and its position in the system of Digenea. In: Littlewood, D.T.J. & Bray, R. A. (Eds) Interrelationships of Platyhelminthes. London: Taylor and Francis, pp. 186–193.Google Scholar
  36. Thompson, J.D., Gibson, T.J., Plewniak, F., Jeanmougin, F. & Higgins, D.G. (1997) The ClustalX windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Research, 24, 4876–4882.Google Scholar
  37. Wesenberg-Lund, C. (1931) Contribution to the development of the trematoda Digenea. Part I. The biology of Leucochloridium paradoxum. Konglige Danske Videnskapernes Selskabs Skrifter, Naturvidenskabelig og Matematisk Afdeling, 9, 94–142.Google Scholar
  38. Zeller, E. (1874) Ueber Leucochloridium paradoxum Carus und die weitere Entwicklung seiner Distomenbrut. Zeitschrift für Wissenschafliche Zoologie, 24, 564–578.Google Scholar

Copyright information

© Kluwer Academic Publishers 2003

Authors and Affiliations

  • S.P. Casey
    • 1
  • T.A. Bakke
    • 2
  • P.D. Harris
    • 3
  • J. Cable
    • 1
  1. 1.School of BiosciencesCardiff UniversityCardiffUK
  2. 2.Zoological MuseumUniversity of OsloNorway
  3. 3.School of Continuing Education and School of Life and Environmental SciencesUniversity of NottinghamNottinghamUK

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