Skip to main content
Log in

An annotated list of species of the Proteocephalus Weinland, 1858 aggregate sensu de Chambrier et al. (2004) (Cestoda: Proteocephalidea), parasites of fishes in the Palaearctic Region, their phylogenetic relationships and a key to their identification

  • Original Paper
  • Published:
Systematic Parasitology Aims and scope Submit manuscript

Abstract

A list and key to the identification of valid species of tapeworms of the Proteocephalus Weinland, 1858 aggregate sensu de Chambrier et al. (2004), i.e. species of the genus occurring in fresh- and brackish-water fishes in the Palaearctic Region, are provided, with data on their hosts and geographical distribution. Instead of 32 taxa listed by Schmidt (1986) and subsequent authors, only the following 14 species are considered to be valid: P. ambiguus (Dujardin, 1845) (type-species); P. cernuae (Gmelin, 1790); P. filicollis (Rudolphi, 1802); P. fluviatilis Bangham, 1925; P. gobiorum Dogiel & Bychowsky, 1939; P. longicollis (Zeder, 1800); P. macrocephalus (Creplin, 1825); P. midoriensis Shimazu, 1990; P. percae (Müller, 1780); P. plecoglossi Yamaguti, 1934; P. sagittus (Grimm, 1872); P. tetrastomus (Rudolphi, 1810); P. thymalli (Annenkova-Chlopina, 1923); and P. torulosus (Batsch, 1786). An analysis of sequences of the nuclear genes (ITS2 and V4 region of 18S rDNA) revealed the following phylogenetic relationships for these taxa: P. torulosus ((P. midoriensis, P. sagittus) (P. fluviatilis (P. filicollis, P. gobiorum, P. macrocephalus)) (P. cernuae, P. plecoglossi, P. tetrastomus ((P. longicollis, P. percae) (P. ambiguus, P. thymalli)))). P. pronini Rusinek, 2001 from grayling Thymallus arcticus nigrescens is synonymised with P. thymalli. P. esocis La Rue, 1911 is apparently invalid but its conspecificity with either P. percae or P. longicollis could not be confirmed due to the absence of the scolex in the holotype and the unavailability of other material for morphological and molecular studies. P. osculatus (Goeze, 1782) has recently been transferred to Glanitaenia de Chambrier, Mariaux, Vaucher & Zehnder, 2004. The validity of the genus is supported by the position of G. osculata within the Proteocephalidea, based on molecular data, as well as its morphology and nature of the definitive host (the European wels Silurus glanis). P. hemispherous Rahemo & Al-Niaeemi, 2001, described from S. glanis in Iraq, is transferred to Postgangesia Akhmerov, 1960 as Postgangesia hemispherous (Rahemo & Al-Niaeemi, 2001) n. comb.

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

Similar content being viewed by others

References

  • Ali, N. M., Al-Jafery, A. R., & Abdul-Ameer, K. N. (1987). Parasitic fauna of freshwater fishes in Diyala River, Iraq. Journal of Biological Sciences Research, Baghdad, 18, 163–181.

    Google Scholar 

  • Al-Kalak, S. H. N. (1992). A comparative study of the nervous system of some cestodes. MSc Thesis, Department of Biology, College of Science University of Mosul, Mosul, Iraq, 115 pp. (cited after Rahemo & Al-Niaeemi, 2001).

  • Anikieva, L. V. (1995a). Variability of a perch’s parasite Proteocephalus percae in the areal of the host. Parazitologiya, 29, 279–288. (In Russian).

    CAS  Google Scholar 

  • Anikieva, L. V. (1995b). Identity of Proteocephalus tapeworms from pike (Esox lucius) in Karelian lakes. Parazitologiya, 29, 510–515. (In Russian).

    Google Scholar 

  • Anikieva, L.V. (1998). Cestodes of the genus Proteocephalus (Cestoda: Proteocephalidea) from the European smelt Osmerus eperlanus. Parazitologiya, 32, 134–140. (In Russian).

    Google Scholar 

  • Anikieva, L. V., & Kharin, V. N. (1997). Interspecific differences of the cestodes of the genus Proteocephalus (Proteocephalidae) in freshwater fishes of the Holarctic. Parazitologiya, 31, 72–80. (In Russian).

    Google Scholar 

  • Bourque, J.-F., Dodson, J. J., Ryan, D. A. J., & Marcogliese, D. J. (2006). Cestode parasitism as a regulator of early life-history survival in an estuarine population of rainbow smelt Osmerus mordax. Marine Ecology Progress Series, 314, 295-307.

    Google Scholar 

  • de Chambrier, A., Al-Kallak, S. N. H., & Mariaux, J. (2003). A new tapeworm, Postgangesia inarmata n. sp. (Eucestoda: Proteocephalidea: Gangesiinae), parasitic in Silurus glanis (Siluriformes) from Iraq and some comments on the Gangesiinae Mola, 1929. Systematic Parasitology, 55, 199–209.

    Article  PubMed  Google Scholar 

  • de Chambrier, A., & Vaucher, C. (1999). Proteocephalidae et Monticelliidae (Eucestoda: Proteocephalidea) parasites de poissons d’eau douce au Paraguay, avec descriptions d’un genre nouveau et de dix espèces nouvelles. Revue Suisse de Zoologie, 106, 165–240.

    Google Scholar 

  • de Chambrier, A., Zehnder, M. P., Vaucher, C., & Mariaux, J. (2004). The evolution of the Proteocephalidea (Platyhelminthes, Eucestoda) based on an enlarged molecular phylogeny, with comments on their uterine development. Systematic Parasitology, 57, 159–171.

    Article  PubMed  Google Scholar 

  • Dubinina, M. N. (1952). Some remarks on the classification of tapeworm family Proteocephalidae La Rue and their distribution in the USSR. Parazitologicheskii Sbornik Zoologicheskogo Instituta AN SSSR, 14, 281–302. (In Russian).

    Google Scholar 

  • Dubinina, M. N. (1987). Class Cestoda Rudolphi, 1808. In O. N. Bauer (Ed.), Key to the parasites of freshwater fishes of the USSR (Vol. 3, pp. 5–76). Leningrad: Nauka. (In Russian).

    Google Scholar 

  • Dzhalilov, U. D., & Ashurova, M. (1971). [A new species of Proteocephalus Weinland, 1858 from fishes of the Pamir basin]. Izvestiya Akademii Nauk Tadzhik SSR, Otdelenie Biologicheskikh Nauk, 3(44), 110–111. (In Russian).

    Google Scholar 

  • Freze, V. I. (1965). [Proteocephalids – tapeworm helminths of fish, amphibians and reptiles.] Osnovy Tsestodologii (Vol. 5, 540 pp). Moscow: Nauka, (In Russian).

    Google Scholar 

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

    CAS  Google Scholar 

  • Hanzelová, V., & Scholz, T. (1992). Redescription of Proteocephalus neglectus La Rue, 1911 (Cestoda: Proteocephalidae), a trout parasite, including designation of its lectotype. Folia Parasitologica, 39, 317–323.

    Google Scholar 

  • Hanzelová, V., & Scholz, T. (1993). Systematic status of Proteocephalus tumidocollis (Cestoda: Proteocephalidae), a parasite of salmonid fishes in North America. Helminthologia, 30, 157–161.

    Google Scholar 

  • Hanzelová, V., & Scholz, T. (1999). Species of Proteocephalus Weinland, 1858 (Cestoda: Proteocephalidae), parasites of coregonid and salmonid fishes from North America: taxonomic reappraisal. Journal of Parasitology, 85, 94–101.

    Article  PubMed  Google Scholar 

  • Hanzelová, V., Scholz, T., & Fagerholm, H.-P. (1995). Synonymy of Proteocephalus neglectus La Rue, 1911 with P. exiguus La Rue, 1911, two fish cestodes from the Holarctic Region. Systematic Parasitology, 30, 173–185.

    Article  Google Scholar 

  • Hanzelová, V., Šnábel, V., Král’ová, I., Scholz, T., & D’Amelio, S. (1999). Genetic and morphological variability in cestodes of the genus Proteocephalus: geographical variation in Proteocephalus percae populations. Canadian Journal of Zoology, 77, 1450–1458.

    Article  Google Scholar 

  • Hanzelová, V., Šnábel, V., Špakulová, M., Fagerholm, H.-P., & Král’ová, I. (1995). A comparative study of the fish parasites Proteocephalus exiguus and P. percae (Cestoda: Proteocephalidae): morphology, isoenzymes, karyotype. Canadian Journal of Zoology, 73, 1191–1198.

    Article  Google Scholar 

  • Hanzelová, V., Šnábel, V., & Špakulová, M. (1996). On the host specificity of fish tapeworm Proteocephalus exiguus La Rue, 1911 (Cestoda). Parasite, 3, 253–257.

    Google Scholar 

  • Hanzelová, V., & Špakulová, M. (1992). Biometric variability of Proteocephalus neglectus (Cestoda: Proteocephalidae) in two different age groups in the rainbow trout from the Dobšiná dam (East Slovakia). Folia Parasitologica, 39, 307–316.

    Google Scholar 

  • Hoffman, G. L. (1999). Parasites of North American freshwater fishes (Second Edit., 539 pp). Ithaca & London: Comstock Publishing Associates, Cornell University Press

    Google Scholar 

  • Hypša, V., Škeříková, A., & Scholz, T. (2005). Multigene analysis and secondary structure characters in a reconstruction of phylogeny, evolution and host-parasite relationship of the order Proteocephalidea (Eucestoda). Parasitology, 130, 359–371.

    Article  PubMed  CAS  Google Scholar 

  • Ieshko, E. P., & Anikieva, L. V. (1980). Polymorphism of Proteocephalus exiguus (Cestoidea: Proteocephalidae), a common parasite of coregonid fish. Parazitologiya, 14, 422–426. (In Russian).

    Google Scholar 

  • Kataoka, N., & Momma, K. (1932). [On a cestode parasitic in Plecoglossus altivelis]. Dobutsugaku Zasshi, 44, 127–136. (In Japanese).

    Google Scholar 

  • Král’ová, I. (1996). A total DNA characterization in Proteocephalus exiguus and P. percae (Cestoda: Proteocephalidae): RAPD and hybridization techniques. Parasitology Research, 82, 668–671.

    PubMed  Google Scholar 

  • Král’ová, I., & Špakulová, M. (1996). Intraspecific variability of Proteocephalus exiguus La Rue, 1911 (Cestoda: Proteocephalidae) as studied by the random amplified polymorphic DNA method (RAPD). Parasitology Research, 82, 542–545.

    Article  PubMed  Google Scholar 

  • Král’ová, I., van de Peer, Y., Jirků, M., van Ranst, M., Scholz, T., & Lukeš, J. (1997). Phylogenetic analysis of a fish tapeworm, Proteocephalus exiguus, based on the small subunit rRNA gene. Molecular and Biochemical Parasitology, 84, 263–266.

    Article  PubMed  Google Scholar 

  • Král’ová, I., Hanzelová, V., Scholz, T., Gerdeaux, D., & Špakulová, M. (2001). A comparison of the internal transcribed spacer of the ribosomal DNA for Eubothrium crassum and Eubothrium salvelini (Cestoda: Pseudophyllidea), parasites of salmonid fish. International Journal for Parasitology, 31, 93–96.

    Article  PubMed  Google Scholar 

  • La Rue, G. R. (1914). A revision of the cestode family Proteocephalidae. Illinois Biological Monographs, 1, 3–351.

    Google Scholar 

  • Linstow, O. (1891). Über den Bau und Entwicklung von Taenia longicollis Rud. Ein Beitrag zur Kenntnis der Fischtänien. Jenische Zeitschrift für Naturwissenschaft, 25, 565–576.

    Google Scholar 

  • Margolis, L., & Arthur, J. R. (1979). Synopsis of the parasites of fishes of Canada. Bulletin of the Fisheries Research Board of Canada, 199, 269 pp.

    Google Scholar 

  • Mohamad, S. A. (1995). Studies on the cestodes parasitic in some teleost fishes in Tigris River. PhD Thesis, Department of Biology, College of Science University of Mosul, Mosul, Iraq, 126 pp. (cited after Rahemo & Al-Niaeemi, 2001).

  • Müller, O. F. (1780). Von Bandwürmen (320 pp). Leipzig: Radebeul Neumann Verlag

    Google Scholar 

  • Nelson, J. S. (1994). Fishes of the world. (3rd Edit., 600 pp). New York: John Wiley & Sons

    Google Scholar 

  • Olson, P. D., & Tkach, V. V. (2005). Advances and trends in the molecular systematics of the parasitic Platyhelminthes. Advances in Parasitology, 60, 165–243.

    Article  PubMed  Google Scholar 

  • Rahemo, Z. I. F., & Al-Niaeemi, B. H. S. (2001). A new cestode species from a freshwater catfish. Rivista di Parassitologia, 42, 71–74.

    Google Scholar 

  • Rego, A. A., de Chambrier, A., Hanzelová, V., Hoberg, E. P., Scholz, T., Weekes, P., & Zehnder, M. (1998). Preliminary phylogenetic analysis of subfamilies of the Proteocephalidea (Eucestoda). Systematic Parasitology, 40, 1–19.

    Article  Google Scholar 

  • Rødland, J. T. (1983). A redescription of the cestodes Proteocephalus filicollis (Rudolphi) from Gasterosteus aculeatus L., and P. ambiguus (Dujardin) from Pungitius pungitius (L.). Zoologica Scripta, 12, 19–23.

    Article  Google Scholar 

  • Rusinek, O. T. (1987). Zum Lebenszyklus von Proteocephalus exiguus (Cestoda), im Baikalsee. Angewandte Parasitologie, 28, 33–36.

    Google Scholar 

  • Rusinek, O. T. (2001). Description of Proteocephalus pronini sp. n. (Cestoda: Proteocephalidae) – a parasite of the Lake Hovsgol grayling. Parazitologiya, 35, 159–161. (In Russian).

    CAS  Google Scholar 

  • Rusinek, O. T., & Kuznedelov, K. T. (2002). Comparative morphological and gene systematics analysis of the Proteocephalus thymalli (Cestoda: Proteocephalidae), a parasite of graylings in lakes Hovsogol and Baikal. Parazitologiya, 36, 71–78. (In Russian).

    CAS  Google Scholar 

  • Schmidt, G. D. (1986). CRC Handbook of tapeworm identification (675 pp). Boca Raton, Florida: CRC Press

    Google Scholar 

  • Schneider, G. (1905). Die Ichthyotaenien des Finnischen Meerbusens. Festschrift für Palmén, Helsingfors, 1(8), 3–32.

    Google Scholar 

  • Scholz, T., & de Chambrier, A (2003). Taxonomy and biology of proteocephalidean cestodes: current state and perspectives. Helminthologia, 40, 65–77.

    Google Scholar 

  • Scholz, T., Drábek, R., & Hanzelová, V. (1998). Scolex morphology of Proteocephalus tapeworms (Cestoda: Proteocephalidae), parasites of freshwater fish in the Palaearctic Region. Folia Parasitologica, 45, 27–43.

    PubMed  CAS  Google Scholar 

  • Scholz, T., & Ergens, R. (1990). Cestodes of fish from Mongolia. Acta Societatis Zoologicae Bohemoslovacae, 54, 287–304.

    Google Scholar 

  • Scholz, T., & Hanzelová, V. (1994). Taxonomic study of two Proteocephalus species (Cestoda: Proteocephalidae) parasitizing coregonid fishes: the synonymy of P. fallax La Rue, 1911 with P. exiguus La Rue, 1911. Systematic Parasitology, 27, 1–12.

    Article  Google Scholar 

  • Scholz, T., & Hanzelová, V. (1998). Tapeworms of the genus Proteocephalus Weinland, 1858 (Cestoda: Proteocephalidae), parasites of fishes in Europe. Studie AV ČR. Prague: Academia, No. 2/98, 119 pp.

  • Scholz, T., & Hanzelová, V. (1999). Species of Proteocephalus Weinland, 1858 (Cestoda: Proteocephalidae) from cyprinid fishes in North America. Journal of Parasitology, 85, 150–154.

    Article  PubMed  CAS  Google Scholar 

  • Scholz, T., Hanzelová, V., Králová, I., & Griffiths, D. (1998). Synonymy of Proteocephalus pollanicola Gresson, 1952 (Cestoda: Proteocephalidae), a parasite of pollan Coregonus autumnalis pollanicola, with P. exiguus La Rue, 1911. Systematic Parasitology, 40, 35–41.

    Article  Google Scholar 

  • Scholz, T., Hanzelová, V., & Šnábel, V. (1995). The taxonomic status of Proteocephalus dubius La Rue, 1911 (Cestoda: Proteocephalidae), a puzzling parasite of perch (Perca fluviatilis L.). Parasite, 2, 231–234.

    Google Scholar 

  • Scholz, T., Marcogliese, D. J., Bourque, J.-F., Škeříková, A., & Dodson, J. J. (2004). Occurrence of Proteocephalus tetrastomus (Rudolphi, 1810) (Cestoda: Proteocephalidea) in larval rainbow smelt (Osmerus mordax) in North America: identification of an unusual pathogen confirmed. Journal of Parasitology, 90, 425–427.

    Article  PubMed  CAS  Google Scholar 

  • Scholz, T., Škeříková, A., Hanzelová, V., Koubková, B., & Baruš, V. (2003). Resurrection of Proteocephalus sagittus (Grimm, 1872) (Cestoda: Proteocephalidea) based on morphological and molecular data. Systematic Parasitology, 56, 173–181.

    Article  PubMed  Google Scholar 

  • Scholz, T., Špakulová, M., Šnábel, V., Král’ová, I., & Hanzelová, V. (1997). A multidisciplinary approach to the systematics of Proteocephalus macrocephalus (Cestoda: Proteocephalidae). Systematic Parasitology, 37, 1–12.

    Article  Google Scholar 

  • Shimazu, T. (1990). Some species of the genus Proteocephalus (Cestoidea: Proteocephalidae) from Japanese freshwater fishes, with a description of a new species. Japanese Journal of Parasitology, 39, 612–624.

    Google Scholar 

  • Shimazu, T. (1993). Redescription of Paraproteocephalus parasiluri (Yamaguti, 1934) n. comb. (Cestoidea: Proteocephalidae), with notes on four species of the genus Proteocephalus, from Japanese freshwater fishes. Journal of Nagano Prefectural College, 48, 1–9.

    Google Scholar 

  • Skryabina, E. S. (1974). [Helminths of acipenserid fishes (Acipenseridae Bonaparte, 1831)] (168 pp.). Moscow: Nauka (In Russian).

    Google Scholar 

  • Swofford, D. L. (2003). PAUP 4.0-phylogenetic analysis using parsimony (Version 4). Sunderland, Mass.: Sinauer

    Google Scholar 

  • Škeríková, A., Hypša, V., & Scholz, T. (2001). Phylogenetic analysis of European species of Proteocephalus (Cestoda: Proteocephalidea): compatibility of molecular and morphological data, and parasite-host coevolution. International Journal for Parasitology, 31, 1121–1128.

    Article  PubMed  Google Scholar 

  • Šnábel, V., Hanzelová, V., & Fagerholm, H.-P. (1994). Morphological and genetic comparison of two Proteocephalus species (Cestoda: Proteocephalidae). Parasitology Research, 80, 141–146.

    PubMed  Google Scholar 

  • Šnábel, V., Hanzelová, V., Mattiucci, S., D’Amelio, S., & Paggi, L. (1996). Genetic polymorphism in Proteocephalus exiguus shown by enzyme electropohoresis. Journal of Helminthology, 70, 345–349.

    Google Scholar 

  • Špakulová, M., & Hanzelová, V. (1992). The karyotypes of Proteocephalus percae (Cestoda: Proteocephalidae). Folia Parasitologica, 39, 324–326.

    Google Scholar 

  • Turčeková, L., & Král’ová, I. (1995). Characterization of DNA restriction profiles and rRNA gene restriction fragment length polymorphisms of Proteocephalus exiguus and P. neglectus from geographically distinct regions. Journal of Helminthology, 69, 159–163.

    Google Scholar 

  • Willemse, J. J. (1968). Proteocephalus filicollis (Rudolphi, 1802) and Proteocephalus ambiguus (Dujardin, 1845), two hitherto confused species of cestodes. Journal of Helminthology, 42, 395–410.

    Google Scholar 

  • Willemse, J. J. (1969). The genus Proteocephalus in the Netherlands. Journal of Helminthology, 43, 207–222.

    Article  PubMed  CAS  Google Scholar 

  • Yamaguti, S. (1934). Studies on the helminth fauna of Japan. Part 4. Cestodes of fishes. Japanese Journal of Zoology, 6, 1–112.

    Google Scholar 

  • Zehnder, M. P., & Mariaux, J. (1999). Molecular systematic analysis of the order Proteocephalidea (Eucestoda) based on mitochondrial and nuclear rDNA sequences. International Journal for Parasitology, 29, 1841–1852.

    Article  PubMed  CAS  Google Scholar 

  • Zeder, J. G. H. (1800). Erster Nachtrag zur Naturgeschichte der Eingeweidewürmer von Johann August Ephraim Goeze. Leipzig, 320 pp. + 6 pl.

Download references

Acknowledgements

The authors are indebted to Václav Hypša, Institute of Parasitology, for valuable suggestions and help with the phylogenetic analyses, to Alain de Chambrier, Natural History Museum, Geneva, Switzerland, for helpful remarks on an early draft of the manuscript, to Larisa V. Filimonova and Ekaterina N. Protasova, Parasitological Institute, Russian Academy of Sciences, Moscow, for lending material of P. longicollis and P. thymalli, and to Mark J. Grygier, Lake Biwa Museum, Kusatsu, Japan, for providing valuable data on P. midoriensis and P. plecoglossi specimens from Japan deposited in the Lake Biwa Museum. This study was partly supported by the Grant Agency of the Czech Republic (project No. 524/04/0342), research projects of the Institute of Parasitology (Z60220518 and LC522) and the Grant Agency of the Slovak Republic (VEGA – project No. 2/44177/04). Samples of P. plecoglossi from Lake Biwa were taken during a short stay of the senior author (TS) in Japan in 2001, supported by Cooperative Research Project K0005, directed by Mark J. Grygier of the Lake Biwa Museum. Finnish material of Proteocephalus tapeworms was taken during a short stay of TS in Finland, supported by the Finnish and Czech Academies of Sciences; fish samples and invaluable help in Finland were provided by E. Tellervo Valtonen, University of Jyväskylä, and Päivi Rintamäki-Kinnunen, University of Oulu, Finland.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Tomáš Scholz.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Scholz, T., Hanzelová, V., Škeříková, A. et al. An annotated list of species of the Proteocephalus Weinland, 1858 aggregate sensu de Chambrier et al. (2004) (Cestoda: Proteocephalidea), parasites of fishes in the Palaearctic Region, their phylogenetic relationships and a key to their identification. Syst Parasitol 67, 139–156 (2007). https://doi.org/10.1007/s11230-006-9089-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11230-006-9089-8

Keywords

Navigation