Parasitology Research

, Volume 95, Issue 2, pp 79–89 | Cite as

Validity reassessment of Trichobilharzia species using Lymnaea stagnalis as the intermediate host

  • J. RudolfováEmail author
  • V. Hampl
  • C. Bayssade-Dufour
  • A. E. Lockyer
  • D. T. J. Littlewood
  • P. Horák
Original Paper


The systematics within the genus Trichobilharzia is complicated. After the description of the type species Trichobilharzia ocellata, the name was routinely used for nearly all European findings of ocellate furcocercariae. T. ocellata was also described from North America and Japan. However, the identity of T. ocellata remains questionable. Comparison of data from the literature showed differences among various T. ocellata isolates and led us to the conclusion that the North American and the Japanese findings are not identical with European T. ocellata. In addition, the description of T. szidati corresponds with the recently reported European T. ocellata isolates. Sequence analysis of the ITS region confirmed that they are identical.


Internal Transcribe Spacer Intermediate Host Seminal Receptacle Snail Species Species Determination 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



We wish to thank Prof. W. Haas from the University of Erlangen (Germany) and Dr. M. de Jong-Brink from the Vrije Universiteit (The Netherlands) for providing us with T. ocellata cercariae and Dr. E. Źbikowska from Nicholas Copernicus University (Poland) for providing us with cercariae from naturally infected snails. This work was supported by the Czech Ministry of Education (grant no. J13/981131-4), by the Czech Ministry of Health (grant no. NJ7545-3/2003) and by The Wellcome Trust (grant no. 072255). The experiments comply with the current laws of the Czech Republic and the United Kingdom.


  1. Blair D, Islam KS (1983) The life cycle and morphology of Trichobilharzia australis n. sp. (Digenea: Schistosomatidae) from the nasal blood vessels of the black duck (Anas superciliosa) in Australia, with a review of the genus Trichobilharzia. Syst Parasitol 5:89–117CrossRefGoogle Scholar
  2. Brumpt E (1931) Cercaria ocellata, déterminant la dermatite des nageurs, provient d’une bilharzie des canards. CR Hebd Acad Sci 192:612–614Google Scholar
  3. Charlesworth B, Sniegowski P, Stephan W (1994) The evolutionary dynamics of repetitive DNA in eukaryotes. Nature 371:215–220CrossRefPubMedGoogle Scholar
  4. Chikami A (1961) Studies on Trichobilharzia ocellata (La Vallete, 1855) in Japan. Jpn J Parasitol 10:106–118Google Scholar
  5. Cort WW, Talbot SB (1936) Studies on schistosomes dermatitis. III. Observation on the behavior of the dermatitis producing schistosome cercariae. Am J Parasitol 4:385–396Google Scholar
  6. Dvořák J, Vanáčová Š, Hampl V, Flegr J, Horák P (2002) Comparison of European Trichobilharzia species based on ITS1 and ITS2 sequences. Parasitology 124:307–313CrossRefPubMedGoogle Scholar
  7. Eklu-Natey DT, Al-Khudri M, Gauthey D, Dubois JP, Wüest J, Vaucher C, Huggel H (1985) Epidémiologie de la dermatite des baigneurs et morphologie de Trichobilharzia cf. ocellata dans le lac Léman. Rev Suisse Zool 92:939–953Google Scholar
  8. Fain A (1956) Les schistosomes ďoiseaux du genre Trichobilharzia Skrjabin et Zakharow, 1920 au Ruanda Urundi. Rev Zool Bot Afr 54:147–178Google Scholar
  9. Farley J (1971) A review of the family Schistosomatidae: excluding the genus Schistosoma from mammals. J Helminthol 45:290–320Google Scholar
  10. Gay P, Bayssade-Dufour C, Grenouillet F, Bourezane Y, Dubois JP (1999) Étude expérimentale de dermatites cercariennes provoquées par Trichobilharzia en France. Med Mal Infect 29:629–637Google Scholar
  11. Hertel J, Hamburger J, Haberl B, Haas W (2002) Detection of bird schistosomes in lakes by PCR and filter-hybridization. Exp Parasitol 101:57–63CrossRefPubMedGoogle Scholar
  12. Horák P, Kolářová L, Dvořák J (1998) Trichobilharzia regenti n. sp. (Schistosomatidae, Bilharziellinae), a new nasal schistosome from Europe. Parasite 5:349–357PubMedGoogle Scholar
  13. Horák P, Kolářová L, Adema CM (2002) Biology of the schistosome genus Trichobilharzia. Adv Parasitol 52:155–233CrossRefPubMedGoogle Scholar
  14. Huelsenbeck JP, Ronquist F (2001) MrBayes: Bayesian inference of phylogenetic trees. Bioinformatics 17:754–755CrossRefPubMedGoogle Scholar
  15. Islam KS, Copeman DB (1986) The morphology and life cycle of Trichobilharzia parocellata (Johnston and Simpson, 1939) Islam and Copeman, 1980 from the visceral blood vessels of Australian anatids. Syst Parasitol 8:39–49Google Scholar
  16. Kalbe M, Haberl B, Haas W (1997) Miracidial host-finding in Fasciola hepatica and Trichobilharzia ocellata is stimulated by species-specific glycoconjugates released from the host snails. Parasitol Res 83:806–812CrossRefPubMedGoogle Scholar
  17. Kalbe M, Haberl B, Haas W (2000) Snail host finding by Fasciola hepatica and Trichobilharzia ocellata: compound analysis of “miracidia-attracting glycoproteins”. Exp Parasitol 96:231–242CrossRefPubMedGoogle Scholar
  18. Kane RA, Rollinson D (1994) Repetitive sequences in the ribosomal DNA internal transcribed spacer of Schistosoma haematobium, Schistosoma intercalatum and Schistosoma mattheei. Mol Biochem Parasitol 63:153–156CrossRefPubMedGoogle Scholar
  19. Khalil LF (2002) Family Schistosomatidae Stiles and Hassall, 1898. In: Gibson DI, Jones A, Bray RA (eds) Keys to the Trematoda, vol 1. CAB International, WallingfordGoogle Scholar
  20. Kilias R, Frick W (1964) Die Zwischenwirtsschnecken wichtiger einheimischer Haus- und Nutztier-Helminthen. Angew Parasitol 5:13–45Google Scholar
  21. Kock S (2000) Evaluation of the importance of different characters for the systematic classification of European Trichobilharzia species. PhD dissertation, Christian Albrechts University, KielGoogle Scholar
  22. Kock S (2001) Investigation of intermediate host specificity help to elucidate the taxonomic status of Trichobilharzia ocellata (Digenea: Schistosomatidae). Parasitology 123:67–70CrossRefPubMedGoogle Scholar
  23. Kock S, Böckeler W (1998) Observations on cercarial chaetotaxy as a means for the identification of European species of Trichobilharzia Skrjabin et Zakharow, 1920 (Digenea: Schistosomatidae). Syst Parasitol 43:159–166CrossRefGoogle Scholar
  24. Kolářová L, Horák P (1996) Morphology and chaetotaxy of Trichobilharzia szidati Neuhaus, 1952 cercariae (Trematoda: Schistosomatidae: Bilharziellinae). Helminthologia 33:7–9Google Scholar
  25. La Valette de St. George A (1855) Symbolae ad trematodum evolutionis historiam. Dissertation, BeroliusGoogle Scholar
  26. Lockyer AE, Olson PD, Ostergaard P, Rollinson D, Johnston DA, Attwood SW, Southgate VR, Horak P, Snyder SD, Le TH, Agatsuma T, McManus DP, Carmichael AC, Naem S, Littlewood DTJ (2003)The phylogeny of the Schistosomatidae based on three genes with emphasis on the interrelationships of Schistosoma Weinland, 1858. Parasitology 126:203–224CrossRefPubMedGoogle Scholar
  27. McMullen DB, Beaver PC (1945) Studies on schistosome dermatitis. IX. The life cycle of three dermatitis-producing schistosomes from birds and a discussion of the subfamily Bilharziellinae (Trematoda: Schistosomatidae). Am J Hyg 42:128–154Google Scholar
  28. Meyer PO, Dubois G (1954) Dermatite humaine causée par des furcocercaires ocellées dans les bains publics de Zurich. Bull Soc Neuchatel Sci Nat 77:81–108Google Scholar
  29. Müller V, Kimmig P (1994) Trichobilharzia franki n. sp.—die Ursache für Badendermatitiden in südwestdeutschen Baggerseen. Appl Parasitol 35:12–31PubMedGoogle Scholar
  30. Neuhaus W (1952) Biologie und Entwicklung von Trichobilharzia szidati n. sp. (Trematoda, Schistosomatidae), einem Erreger von Dermatitis beim Menschen. Z Parasitenkd 15:203–266CrossRefPubMedGoogle Scholar
  31. Odening K (1996) What Cercaria ocellata actually is. Acta Parasitol Turc 20 [Suppl 1]:387–397Google Scholar
  32. Picard D, Jousson O (2001) Genetic variability among cercariae of the Schistosomatidae (Trematoda: Digenea) causing swimmer’s itch in Europe. Parasite 8:237–242PubMedGoogle Scholar
  33. Posada D, Crandall KA (1998) Modeltest: testing the model of DNA substitution. Bioinformatics 14:817–817CrossRefPubMedGoogle Scholar
  34. Richard J (1971) La chétotaxie des cercaires. Valeur systématique et phylétique. Mém Mus Natl Hist Nat, Ser A, Zool 67:1–179Google Scholar
  35. Simon-Martin F, Simon-Vicente F (1999) The life cycle of Trichobilharzia salmanticensis n. sp. (Digenea: Schistosomatidae), related to cases of human dermatitis. Res Rev Parasitol 59:13–18Google Scholar
  36. Skrjabin KI, Zakharov NP (1920) Zwei neue Trematodengattungen aus den Blutgefässen der Vögel. (Beitrag zur Kenntnis der Helminthenfauna der Vögel Russlands) (in Russian). Izv Donskovo Vet Inst 2:1–6Google Scholar
  37. Sluiters JF (1983) Observations on the identity of the avian schistosome Trichobilharzia ocellata (La Valette, 1855) Brumpt, 1931. Acta Leiden 51:53–60PubMedGoogle Scholar
  38. Swofford, DL (2002) PAUP*. Phylogenetic analysis using parsimony *and other methods. Sinauer, Sunderland, Mass.Google Scholar
  39. Szidat L (1942) Was ist Cercaria ocellata La Valette? Morphologische und entwicklungsgeschichtliche Untersuchungen über den Erreger der europäischen Cercarien-Dermatitis des Menschen. Dtsch Tropenmed Z, 46:481–497, 509–524Google Scholar
  40. Szidat L, Wigand R (1934) Leitfaden der Einheimischen Wurmkrankheiten des Menschen. Thieme, LeipzigGoogle Scholar
  41. Talbot SB (1936) Studies on schistosome dermatitis. II. Morphological and life history studies on three dermatitis-producing schistosome cercariae, C. elvae Miller, 1923, C. stagnicolae n. sp., and C. physellae n. sp. Am J Hyg 23:372–384Google Scholar
  42. Voronin MV, Beer SA, Dobrovolskij AA (2002) Schistosomatidnyje cerkarii gruppy Trichobilharzia cf. ocellata iz populjacij megapolisov Moskvy i Sankt-Peterburga. Teoretičeskije i prikladnyje problemy parazitologii. Ross Akad Nauk, Inst Parazit Google Scholar
  43. Źbikowska E (2004) Infection of snails with bird schistosomes and the threat of swimmer’s itch in selected Polish lakes. Parasitol Res 92:30–35Google Scholar

Copyright information

© Springer-Verlag 2004

Authors and Affiliations

  • J. Rudolfová
    • 1
    Email author
  • V. Hampl
    • 1
  • C. Bayssade-Dufour
    • 2
  • A. E. Lockyer
    • 3
  • D. T. J. Littlewood
    • 3
  • P. Horák
    • 1
  1. 1.Department of ParasitologyCharles UniversityPrague 2Czech Republic
  2. 2.Biologie ParasitaireMuseum National Paris cedex 05France
  3. 3.Department of ZoologyThe Natural History MuseumLondon UK

Personalised recommendations