Advertisement

Systematic Parasitology

, Volume 90, Issue 2, pp 177–190 | Cite as

Morphological polymorphism in tapeworms: redescription of Caryophyllaeus laticeps (Pallas, 1781) (Cestoda: Caryophyllidea) and characterisation of its morphotypes from different fish hosts

  • Vladimíra Hanzelová
  • Mikuláš Oros
  • Daniel Barčák
  • Dana Miklisová
  • Diana Kirin
  • Tomáš ScholzEmail author
Article

Abstract

Recent morphological and molecular data have shown that one of the most common parasites of freshwater fish in the Palaearctic Region, the cestode Caryophyllaeus laticeps (Pallas, 1781) (Eucestoda: Caryophyllidea), is highly polymorphic. Five distinct morphotypes of C. laticeps, largely corresponding to different fish hosts and representing separate, yet closely related genetic lineages, have been recognised and they are characterised in the present paper. Morphotype 1 from breams, Abramis brama (L.) (type-host) and Ballerus spp., corresponds to the original Taenia laticeps Pallas, 1781 and its neotype (paragenophore ex A. brama in Russia) is designated. This morphotype is characterised by a slender body and flabellate scolex. Morphotype 2 was found in the Macedonian vimba Vimba melanops (Heckel) and the vimba bream V. vimba (L.); it is typified by a more robust body, with most anterior extent of the vitelline follicles near the scolex and the cirrus-sac situated more anteriorly than in other morphotypes. Morphotype 3 is represented by worms from the common carp Cyprinus carpio L. that possess a cuneicrispitate scolex (having the form of a wedge with shallow indentations on anterior margin). Morphotype 4 from the common nase Chondrostoma nasus (L.) has a large, robust body and a wide scolex with numerous superficial grooves (wrinkles) in its anterior part. Morphotype 5 is represented by worms from the white-eye bream Ballerus sapa (Pallas); its typical characteristics are a festoon-like anterior margin of the scolex, the absence of vitelline follicles posterior to the cirrus-sac and the absence of a well-developed internal seminal vesicle. Discriminant analysis of 15 morphometric variables readily separated Morphotypes 3, 4 and 5 and confirmed the key discriminating power of traits related to the reproductive system, especially the terminal reproductive organs. Morphological polymorphism and the genetic divergence of different morphotypes of C. laticeps correspond to its wide spectrum of fish definitive hosts and a large distribution area that includes Europe, most of Palaearctic Asia and northern Africa.

Keywords

Anterior Margin Fish Host Anterior Extremity Vitelline Follicle Abramis Brama 
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.

Notes

Acknowledgements

The authors are grateful to Aneta Kostadinova and two anonymous reviewers for their helpful suggestions, Viera Kurimaiová, Institute of Parasitology, SAS, Košice, Slovakia, for help with the preparation of line drawings, Larisa G. Poddubnaya, Institute of Inland Waters, Borok, Russia and Franz Jirsa for organising collecting trips to the River Volga in Russia during 2008 and 2009 and the Drau River in Austria during 2009, respectively. Thanks are also due to Ali Aydoğdu, Turkey, for providing specimens from Vimba vimba, Anirban Ash, India, Sonya Shukerova and Stefan Hristov, Bulgaria, Marta Špakulová and Ľudmila Turčeková, Slovakia for help with fish dissections, and Stanislav Géci and Rudolf Halmi from Slovak Fishing Union for help in obtaining fish. Curators of the following collections kindly provided specimens for the present study: Sven Boström (SMNH), Alain de Chambrier and Jean Mariaux (MHNG-PLAT), Eileen Harris (BMNH), Patricia Pilitt and Eric P. Hoberg (USNPC), Oksana Greben (ZIK), Alex Galkin (ZIRAS), Kennet Lundin (GNM), Birger Neuhaus (ZMB) and Helmut Sattmann (ZMW). This study was supported by the Slovak Research and Development Agency (projects APVV-0653-11 and LPP 0171-09), Grant Agency VEGA (project 2/0129/12), National Science Foundation, USA (PBI awards 0818696 and 0818823), and Czech Science Foundation (project P505/12/G112). The study was undertaken within the framework of a project of the Research & Development Operational Programme funded by the ERDF (code ITMS: 26220120022) (0.5). Access to old literature at the ZMB was enabled by the EU SYNTHESYS project (DE-TAF-3080) to T.S.; the help of Birger Neuhaus and staff of the ZMW library is also much appreciated.

Supplementary material

11230_2014_9536_MOESM1_ESM.doc (47 kb)
Supplementary material 1 (DOC 47 kb)
11230_2014_9536_MOESM2_ESM.xls (40 kb)
Supplementary material 2 (XLS 40 kb)

References

  1. Akhmerov, A. Kh. (1960). [Tapeworms of fish of the Amur River.] Trudy Gelminthologicheskoi Laboratorii, 10, 15–31 (In Russian).Google Scholar
  2. Anderson, R. M. (1974). Population dynamics of the cestode Caryophyllaeus laticeps (Pallas, 1781) in the bream (Abramis brama L.). Journal of Animal Ecology, 43, 305–321.CrossRefGoogle Scholar
  3. Anderson, R. M. (1976). Seasonal variation in the population dynamics of Caryophyllaeus laticeps. Parasitology, 72, 281–305.PubMedCrossRefGoogle Scholar
  4. Astrin, J. J., Zhou, X., & Misof, B. (2013). The importance of biobanking in molecular taxonomy, with proposed definitions for vouchers in a molecular context. ZooKeys, 365, 67–70.PubMedCrossRefGoogle Scholar
  5. Barčák, D., Oros, M., Hanzelová, V., & Scholz, T. (2014). Phenotypic plasticity in Caryophyllaeus brachycollis Janiszewska, 1953 (Cestoda: Caryophyllidea): does fish host play a role? Systematic Parasitology, 88, 153–166.PubMedCrossRefGoogle Scholar
  6. Batsch, A. J. G. C. (1786). Naturgeschichte der Bandwurmgattung überhaupt und ihrer Urten insbesondere, nach den neuern Beobachtungen in einem systematischen Auszuge. Halle: J. J. Gebauer, 299 pp.Google Scholar
  7. Bazsalovicsová, E., Kráľová-Hromadová, I., Brabec, J., Hanzelová, V., Oros, M., & Scholz, T. (2014). Conflict between morphology and molecular data: a case of the genus Caryophyllaeus (Cestoda, Caryophyllidea), monozoic tapeworm of cyprinid fishes. Folia Parasitologica, 61, 347–354.Google Scholar
  8. Bloch, M. E. (1782). Abhandlung von der Erzeugung der Eingeweidewürmer und den Mitteln wieder dieselben. Berlin: G. F. Hesse, 54 pp.Google Scholar
  9. Brabec, J., Scholz, T., Kráľová-Hromadová, I., Bazsalovicsová, E., & Olson, P. D. (2012). Substitution saturation and multiple copies of standard nuclear and mitochondrial phylogenetic markers in an unusual group of unsegmented tapeworms (Platyhelminthes). International Journal for Parasitology, 42, 259–267.Google Scholar
  10. Bremser, J. G. (1824). Icones Helminthum Systema Rudolphii Entozoologicum illustrantes. Vienna: A. Strauus, 12 pp.Google Scholar
  11. Bremser, J. G. (1837). Traité zoologique et physiologique sur les vers intestinaux de l’home. Nouvel Atlas. Paris: Méquignon/Marvis, 70 pp.Google Scholar
  12. Chervy, L. (2009). Unified terminology for cestode microtriches: a proposal from the International Workshops on Cestode Systematics in 2002–2008. Folia Parasitologica, 56, 199–230.PubMedCrossRefGoogle Scholar
  13. Davydov, V. G., & Poddubnaya, L. G. (1988). Functional morphology of frontal and uterine glands in cestodes of the order Caryophyllidea. Parazitologiya, 22, 449–457 (In Russian).Google Scholar
  14. Dubinina, M. N. (1971). [Tapeworms of the Amur River basin.] Parazitologicheskii Sbornik AN SSSR, 25, 77–119 (In Russian).Google Scholar
  15. Dubinina, M. N. (1987). [Class tapeworms – Cestoda Rudolphi, 1808.] In: Bauer, O. N. (Ed.) Key to the parasites of freshwater fishes of the USSR. Leningrad: Nauka, pp. 5–76 (In Russian).Google Scholar
  16. Froese, R., & Pauly, D. (2014). Fishbase. World Wide Web electronic publication. http://www.fishbase.org.
  17. Fuhrmann, O. (1930). Dritte Klasse des Cladus Plathelminthes, Cestoidea. Kükenthal’s Handbuch der Zoologie, 2, 141–416.Google Scholar
  18. Gibson, D. I., Bray, R. A., & Harris, E. A. (Compilers) (2005). Host-Parasite Database of the Natural History Museum, London. http://www.nhm.ac.uk/research-curation/scientific-resources/taxonomy-systematics/host-parasites/.
  19. Goeze, J. A. E. (1782). Versuch einer Naturgeschichte der Eingeweidewürmer thierischer Körper. Blankenburg: Ph. U. Pape, 472 pp.Google Scholar
  20. Kennedy, C. R. (1969). Seasonal incidence and development of the cestode Caryophyllaeus laticeps (Pallas) in the River Avon. Parasitology, 59, 783–794.PubMedGoogle Scholar
  21. Kennedy, C. R., & Walker, P. J. (1969). Evidence for an immune response by dace, Leuciscus leuciscus, to infections by the cestode Caryophyllaeus laticeps. Journal of Parasitology, 55, 579–582.PubMedCrossRefGoogle Scholar
  22. Khalil, L. F., Jones, A., & Bray, R. A. (1994). Keys to the cestode parasites of vertebrates. Wallingford, UK: CAB International, 751 pp.Google Scholar
  23. Kulakovskaya, O. P. (1961). [On the fauna of the Caryophyllaeidae (Cestoda, Pseudophyllidea) of the USSR.] Parasitologicheskii Sbornik, 20, 339–354 (In Russian).Google Scholar
  24. Mackiewicz, J. S. (1974). The genus Caryophyllaeus Gmelin (Cestoidea: Caryophyllidea) in the Nearctic. Proceedings of the Helminthological Society of Washington, 41, 184–191.Google Scholar
  25. Mackiewicz, J. S. (1994). Order Caryophyllidea van Beneden in Carus, 1863. In: Khalil, L. F., Jones, A. & Bray, R. A. (Eds) Keys to the cestode parasites of vertebrates. Wallingford, UK: CAB International, pp. 21–43.Google Scholar
  26. Macko, J. K., Ryšavý, B., Špakulová, M., & Kráľová, I. (1993). Synopsis of cestodes in Slovakia I. Cestodaria, Cestoidea: Caryophyllidea, Spathebothriidea, Pseudophyllidea, Proteocephalidea. Helminthologia, 30, 85–91.Google Scholar
  27. Moravec, F. (2001). Checklist of the metazoan parasites of fishes of the Czech Republic and the Slovak Republic (1873–2000). Praha: Academia, 169 pp.Google Scholar
  28. Mrázek, A. (1901). Ueber die Larve von Caryophyllaeus mutabilis Rud. Centralblatt für Bakteriologie, Parasitenkunde und Infektionskrankheiten, 29, 485–491.Google Scholar
  29. Nybelin, O. (1922). Anatomisch-systematische Studien über Pseudophyllidien. Göteborgs Kungl. Vetenskaps och Vitterhets Samhälles Handlingar, 26, 1–228.Google Scholar
  30. Oros, M., Scholz, T., Hanzelová, V., & Mackiewicz, J. S. (2010). Scolex morphology of monozoic cestodes (Caryophyllidea) from the Palaearctic Region: a useful tool for species identification. Folia Parasitologica, 57, 37–46.PubMedCrossRefGoogle Scholar
  31. Pallas, P. S. (1781). Bemerkungen über die Bandwürmer in Menschen und Tieren. Neu Nordische Beytrage zur physikalischen und geographischen Erd- und Völker Beschreibung, Naturgeschichte und Ökonomie. Erster Band. St. Peterburg and Leipzig: J. Z. Logan, pp. 39–112.Google Scholar
  32. Poddubnaya, L. G. (1995). [Peculiarities of the integument genesis in procercoids of caryophyllidean cestodes.] Parazitologiya, 29, 13–18 (In Russian).Google Scholar
  33. Protasova, E., Kuperman, B., Roytman, V., & Poddubnaya, L. G. (1990). [Caryophyllidea of the fauna of the USSR.] Moscow: Nauka, 240 pp (In Russian).Google Scholar
  34. Rudolphi, C. A. (1802). II. Fortschung der Beobachtungen über die Eingeweidewürmer. Archiv für Zoologie und Zootomie, 3, 61–125.Google Scholar
  35. Rudolphi, C. A. (1809). Entozoorum sive vermium intestinalium historia naturalis. Volumen II, Part I. Amstelaedami: Sumtibus Tabernae Librariae et Artium, 458 pp.Google Scholar
  36. Scholz, T. (1989). Amphilinida and Cestoda, parasites of fish in Czechoslovakia. Praha: Academia, 56 pp.Google Scholar
  37. Scholz, T., Brabec, J., Kral’ová-Hromadová, I., Oros, M., Bazsalovicsová, E., Ermolenko, A., & Hanzelová, V. (2011). Revision of Khawia spp. (Cestoda: Caryophyllidea), parasites of cyprinid fish, including a key to their identification and molecular phylogeny. Folia Parasitologica, 58, 197–223.PubMedCrossRefGoogle Scholar
  38. Scholz, T., Oros, M., Choudhury, A., Brabec, J., & Waeschenbach, A. (2015). New circumscription of freshwater fish parasites Monobothrium Diesing, 1863 and Promonobothrium Mackiewicz, 1968 (Cestoda: Caryophyllidea) using morphological and molecular evidence. Journal of Parasitology, 101 (in press).Google Scholar
  39. Sekutowicz, S. (1934). Etudes sur le développement et la biologie de Caryophyllaeus laticeps (Pall.). Mémoires de l’Academie Polonaise des Sciences et des Lettres, Classe Sciences Mathematiques et Naturelles, 6, 1–15.Google Scholar
  40. van Beneden, P. J. (1858) Mémoire sur les vers intestinaux. Supplément aux Comptes Rendus des Séances de l’Académie des Sciences, Vol. 2, 376 pp.Google Scholar
  41. van Lidth de Jeude, T. G. (1829). Recueil de figures des vers intestinaux, ouvrage, présentant une distribution méthodique de ces animaux, les caractères généraux et particuliers de leurs familles et de leurs genres, principalement suivant le système de Mr. le professeur C. A. Rudolphi et la description de quelques espèces les plus remarquables. Leide: S. et J. Luchtmans, 15 pp.Google Scholar
  42. Will, H. (1893). Anatomie von Caryophyllaeus Rud. Ein Beitrag zur Kenntnis der Cestoden. Zeitschrift für Wissenschaftliche Zoologie, 56, 1–39.Google Scholar
  43. Žitňan, R. (1968). Cestoidea der Fische im Flusse Hron (ČSSR). Studia Helminthologica, 10, 11–20.Google Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2014

Authors and Affiliations

  • Vladimíra Hanzelová
    • 1
  • Mikuláš Oros
    • 1
  • Daniel Barčák
    • 1
  • Dana Miklisová
    • 1
  • Diana Kirin
    • 2
  • Tomáš Scholz
    • 3
    Email author
  1. 1.Institute of ParasitologySlovak Academy of SciencesKošiceSlovakia
  2. 2.Agricultural University of PlovdivPlovdivBulgaria
  3. 3.Institute of ParasitologyBiology Centre of the Czech Academy of SciencesČeské BudějoviceCzech Republic

Personalised recommendations