An annotated list and molecular data on larvae of gryporhynchid tapeworms (Cestoda: Cyclophyllidea) from freshwater fishes in Africa

  • Tomáš Scholz
  • Sareh Tavakol
  • Lucie Uhrová
  • Jan Brabec
  • Iva Přikrylová
  • Šárka Mašová
  • Andrea Šimková
  • Ali Halajian
  • Wilmien J. Luus-Powell
Article
Part of the following topical collections:
  1. Cestoda

Abstract

An annotated list of larvae (metacestodes) of gryporhynchid tapeworms (Cestoda: Cyclophyllidea) from freshwater fishes in Africa is provided with numerous new host and geographical records. Newly collected materials from Burundi, Democratic Republic of the Congo, Kenya, Madagascar, Namibia, Senegal, South Africa, Sudan and Zimbabwe practically double the total number of species reported from African fish so far. We confirm the occurrence of 16 species (five unidentified to the species level and most likely representing new taxa) belonging to the genera Amirthalingamia Bray, 1974 (1 species), Cyclustera Fuhrmann, 1901 (2 species), Dendrouterina Fuhrmann, 1912 (1 species), Neogryporhynchus Baer & Bona, 1960 (1 species), Paradilepis Hsü, 1935 (4 species), Parvitaenia Burt, 1940 (5 species), and Valipora Linton, 1927 (2 species). Additionally, metacestodes of four unidentified species of Paradilepis and Parvitaenia are reported from fish for the first time. Rostellar hooks of all species are illustrated and their measurements are provided together with a host-parasite list. The molecular phylogenetic analysis based on partial LSU rDNA sequences offers the first insight into the internal phylogenetic relationships within the family. Together with the morphological observations, the present study provides a taxonomic baseline for future studies on this largely neglected, but widely distributed and relatively frequent, group of parasites of African fishes, including economically important cichlids like tilapias and cyprinids.

Notes

Acknowledgements

Two anonymous reviewers and the Editor provided helpful suggestions that helped improve the quality of the manuscript. The authors are also indebted to Miloslav Jirků (Institute of Parasitology, BC CAS, České Budějovice, Czech Republic), Božena Koubková (Faculty of Science, Masaryk University, Brno, Czech Republic) and Olena Kudlai (North-West University, Potchefstroom, South Africa) who generously provided us with specimens of gryporhynchids from Kenya, Senegal and South Africa, respectively, Eva Řehulková and Maarten P. M. Vanhove (Faculty of Science, Masaryk University, Brno, Czech Republic; Royal Belgian Institute of Natural Sciences, Brussels, Belgium; KU Leuven, Leuven, Belgium; Hasselt University, Diepenbeek, Belgium) and J. Rasamy Razanabolana (University of Antananarivo, Madagascar), J. R. Rasoloariniaina (Centre National de Recherche sur l’Environnement, Antananarivo) for their assistance with fish dissection and parasite collection from cichlid fish in Madagascar, and Marliese Truter (North-West University, Potchefstroom, South Africa) for her assistance with dissecting P. philander in North-West Province. TS is obliged to staff of the Royal Museum of Central Africa, especially Tine Huyse and Christophe Allard, for help during his short stay in Tervuren.

Funding

This study was supported by the Czech Science Foundation (project No. P505/12/G112) and Institute of Parasitology (institutional support RVO 60077344). Some of the results formed part of the BSc thesis of L. Uhrová. Stay of TS in the Royal Museum of Central Africa in Tervuren, Belgium, in February 2016 was funded by the EU-SYNTHESYS Project BE-TAF-5671. This work is also based on the research supported by the South African Research Chairs Initiative (SARChI) of the Department of Science and Technology and National Research Foundation of South Africa (Grant no. 101054). Any opinion, finding and conclusion or recommendation expressed in this material is that of the authors and the funding agencies do not accept any liability in this regard.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All applicable institutional, national and international guidelines for the care and use of animals were followed.

Supplementary material

11230_2018_9796_MOESM1_ESM.pdf (190 kb)
Supplementary material 1 (PDF 191 kb)

References

  1. Aloo, P. A. (2002). A comparative study of helminth parasites from the fish Tilapia zillii and Oreochromis leucostictus in Lake Naivasha and Oloidien Bay, Kenya. Journal of Helminthology, 76, 95–102.CrossRefPubMedGoogle Scholar
  2. Baer, J. G. (1959). Exploration des Parcs Nationaux du Congo Belge. Fasc. 1. Helminthes parasites. Brussels, Belgium: Instituts des Parcs Nationals, Congo Belge, 163 pp.Google Scholar
  3. Baer, J. G., & Bona, F. V. (1960). Révision des Cestodes Dilepididae Fuhrm., 1907 des Ardéiformes. Note préliminaire. Bolletino dell’Istituto e Museo di Zoologia della Università di Torino, 6, 91–143.Google Scholar
  4. Batra, V. (1984). Prevalence of helminth parasites in three species of cichlids from a man-made lake Zambia. Zoological Journal of the Linnean Society, London, 82, 319–333.CrossRefGoogle Scholar
  5. Bona, F. V. (1975). Étude critique et taxonomique des Dilepididae Fuhrmann, 1907 (Cestoda) parasites des Ciconiiformes. Roma, Italy: Consiglio Nazionale delle Ricerche, 750 pp.Google Scholar
  6. Bona, F. V. (1994). Family Dilepididae Railliet & Henry, 1909. In: Khalil, L. F., Jones, A. & Bray, R. A. (Eds) Keys to the Cestode Parasites of Vertebrates. Wallingford, UK: CAB International, pp. 445–554.Google Scholar
  7. Brabec, J., Scholz, T., Králová-Hromadová, I., Bazsalovicsová, E., & Olson, P. D. (2012). Substitution saturation and nuclear paralogs of commonly employed phylogenetic markers in the Caryophyllidea, an unusual group of non-segmented tapeworms (Platyhelminthes). International Journal for Parasitology, 42, 259–267.CrossRefPubMedGoogle Scholar
  8. Bray, R. A. (1974). A new genus of dilepidid cestode in Tilapia nilotica (L., 1758) and Phalacrocorax carbo (L., 1758) in Sudan. Journal of Natural History, 8, 589–596.CrossRefGoogle Scholar
  9. Caira, J. N., & Jensen, K. (Editors) (2017). Planetary Biodiversity Inventory (2008–2017): Tapeworms from Vertebrate Bowels of the Earth. Lawrence, USA: University of Kansas, Natural History Museum, Special Publication No. 25, 463 pp.Google Scholar
  10. Ergens, R. (1969). The suitability of ammonium picrate-glycerin in preparing slides of lower Monogenoidea. Folia Parasitologica, 16, 320.Google Scholar
  11. Froese, R., & Pauly, D. (Editors) (2017) FishBase. World Wide Web electronic publication. www.fishbase.org (Accessed July 2017).
  12. Fuhrmann, O. (1909). Die Cestoden der Vögel des weissen Nils. In: Jägerskiöld, L. A. (Ed.). Results of the Swedish zoological expedition to Egypt and the White Nile, 1901, 3, 1–53.Google Scholar
  13. Fuhrmann, O. (1912). Ergebnisse der mit Subvention ans der Erbschaft Treitl unternommenen zoologischen Forschungsreise Dr. Franz Werner’s nach dem ägyptischen Sudan u. Nord Uganda. XXI. Vogelcestoden. Sitzungsberichte der Kaiserlichen Akademie der Wissenschaften, Mathematisch-Naturwissenschaftliche Klasse, 121, 181–192.Google Scholar
  14. Gibson, D. I., Bray, R. A., & Harris, E. A. (Compilers) (2005). Host-Parasite Database of the Natural History Museum, London. World Wide Web electronic publication. http://www.nhm.ac.uk/research-curation/scientific-resources/taxonomy-systematics/host-parasites/
  15. Guindon, S., Dufayard, J.-F., Lefort, V., Anisimova, M., Hordijk, W., & Gascuel, O. (2010). New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Systematic Biology, 59, 307–321.CrossRefPubMedGoogle Scholar
  16. del Hoyo, J., Elliott, A., & Sargatal, J. (Eds) (1992). Handbook of the birds of the world. Vol. 1. Barcelona: Lynx Edicions, 696 pp.Google Scholar
  17. Joyeux, C., & Baer, J. G. (1935). Notices helminthologiques. Bulletin de la Société Zoologique de, France, 60, 482–501.Google Scholar
  18. Katoh, K., & Standley, D. M. (2013). MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Molecular Biology and Evolution, 30, 772–780.CrossRefPubMedPubMedCentralGoogle Scholar
  19. Kearse, M., Moir, R., Wilson, A., Stones-Havas, S., Cheung, M., Sturrock, S., et al. (2012). Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics, 28, 1647–1649.CrossRefPubMedPubMedCentralGoogle Scholar
  20. Khalil, L. F. (1961). On a new cestode, Paradilepis maleki sp. nov. (Dilepididae), from a sacred ibis in the Sudan. Journal of Helminthology, 35, 255–258.CrossRefPubMedGoogle Scholar
  21. Khalil, L. F., & Polling, L. (1997). Check list of the helminth parasites of African freshwater fish. Pietersburg, South Africa: University of the North, Republic of South Africa, 161 pp.Google Scholar
  22. Malmberg, G. (1957). [On the occurrence of Gyrodactylus on Swedish fish.] Skrifter utgivna av Södra Sveriges Fiskeriföreningen 1956, pp. 19–76 (In Swedish).Google Scholar
  23. Mariaux, J., Tkach, V. V., Vasileva, G. P., Waeschenbach, A., Beveridge, I., Dimitrova Y. D., et al. (2017). Cyclophyllidea van Beneden in Braun, 1900. In: Caira, J. N. & Jensen, K. (Eds) Planetary Biodiversity Inventory (2008–2017): Tapeworms from Vertebrate Bowels of the Earth. Lawrence, USA: University of Kansas, Natural History Museum, Special Publication No. 25, pp. 77–148.Google Scholar
  24. Mettrick, D. F. (1967). Some cestodes from Ardeiformes and Charadriiformes in Central Africa. Revue de Zoologie et Botanique Africaine, 75, 333–362.Google Scholar
  25. Moravec, F., & Scholz, T. (2016). Helminth parasites of the lesser great cormorant Phalacrocorax carbo sinensis from two nesting regions in the Czech Republic. Folia Parasitologica, 63, 022.CrossRefGoogle Scholar
  26. Ortega-Olivares, M. P., Barrera-Guzmán, A., Haasová, I., Salgado-Maldonado, G., Guillén-Fernández, S., & Scholz, T. (2008). Tapeworms (Cestoda: Gryporhynchidae) of herons (Ciconiiformes: Ardeidae) from Mexico: new host and geographical records. Comparative Parasitology, 75, 182–195.CrossRefGoogle Scholar
  27. Ortega-Olivares, M. P., García-Prieto, L., & García-Varela, M. (2014). Gryporhynchidae (Cestoda: Cyclophyllidea) in Mexico: species list, hosts, distribution and new records. Zootaxa, 3795, 101–125.CrossRefPubMedGoogle Scholar
  28. Rudolphi, K. A. (1819). Entozoorum Synopsis cui accedunt mantissa duplex et indices locupletissimi. Berlin, Germany, X + 811 pp. & 3 plts.Google Scholar
  29. Schmidt, G. D. (1986). Handbook of tapeworm identification. Boca Raton, USA: CRC Press, 675 pp.Google Scholar
  30. Scholz, T., Boane, C., & Saraiva, A. (2008). New metacestodes of gryporhynchid tapeworms (Cestoda: Cyclophyllidea) from carp (Cyprinus carpio Linnaeus, 1758) from Mozambique, Africa. Comparative Parasitology, 75, 315–320.CrossRefGoogle Scholar
  31. Scholz, T., Bray, R. A., Kuchta, R., & Řepová, R. (2004). Larvae of gryporhynchid cestodes (Cyclophyllidea) from fish: a review. Folia Parasitologica, 51, 131–152.CrossRefPubMedGoogle Scholar
  32. Scholz, T., Kuchta, R., & Salgado-Maldonado, G. (2002). Cestodes of the family Dilepididae (Cestoda: Cyclophyllidea) from fish-eating birds in Mexico: a survey of species. Systematic Parasitology, 52, 171–182.CrossRefPubMedGoogle Scholar
  33. Scholz, T., & Salgado-Maldonado, G. (2001). Metacestodes of the family Dilepididae (Cestoda: Cyclophyllidea) parasitising fishes in Mexico. Systematic Parasitology, 49, 23–40.CrossRefPubMedGoogle Scholar
  34. Sokolov, S. G., Protasova, E. N., & Reshetnikov, A. N. (2015). First data on parasites of the rotan, Perccottus glenii Dybowski, 1877 (Perciformes: Odontobutidae), from Germany, with a detection of the previously unknown merocercoid of the gryporhynchid cestode Mashonalepis macrosphincter (Fuhrmann, 1909). Acta Zoologica Bulgarica, 67, 557–560.Google Scholar
  35. Truter, M., Přikrylová, I., Malherbe, W., & Smit, N. J. (2016). First report of metazoan parasites from the cichlid Pseudocrenilabrus philander and the cyprinid Enteromius paludinosus in a South African Ramsar wetland. African Journal of Aquatic Science, 41, 499–503.CrossRefGoogle Scholar
  36. Vanhove, M. P. M., Hablützel, P. I., Pariselle, A., Šimková, A., Huyse, T., & Raeymaekers, J. A. M. (2016). Cichlids: a host of opportunities for evolutionary parasitology. Trends in Parasitology, 32, 820–832.CrossRefPubMedGoogle Scholar
  37. Wedl, C. (1855). Characteristik mehrerer gröstenteils neuer Taenien. Sitzungsberichte der kaiserlichen Akademie der Wissenschaften, Mathematisch-Naturwissenschaftliche Classe, 18 (1), 5–27.Google Scholar

Copyright information

© Springer Science+Business Media B.V., part of Springer Nature 2018

Authors and Affiliations

  1. 1.Institute of Parasitology, Biology CentreCzech Academy of SciencesČeské BudějoviceCzech Republic
  2. 2.Department of ParasitologyUniversity of South Bohemia in České BudějoviceČeské BudějoviceCzech Republic
  3. 3.Department of BiodiversityUniversity of LimpopoSovengaSouth Africa
  4. 4.Department of Botany and Zoology, Faculty of ScienceMasaryk UniversityBrnoCzech Republic
  5. 5.Water Research Group, Unit for Environmental Sciences and ManagementNorth-West UniversityPotchefstroomSouth Africa

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