Skip to main content

Ancyrocephalidae (Monogenea) of Lake Tanganyika: II: description of the first Cichlidogyrus spp. parasites from Tropheini fish hosts (Teleostei, Cichlidae)

Parasitology Research volume 110, pages 305–313 (2012)Cite this article

Abstract

Although Lake Tanganyika hosts the most diverse endemic cichlid fish assemblage, its monogenean parasite fauna has hardly been documented. The cichlid tribe Tropheini has generated great interest because of its systematic position within the Haplochromini s.l. and its diversity in trophic morphology, reproductive behaviour and population structure. It has the potential to host a diverse Monogenea fauna. Here, we describe the first Cichlidogyrus spp.: Cichlidogyrus steenbergei sp. n., Cichlidogyrus irenae sp. n. and Cichlidogyrus gistelincki sp. n. The three host species, Limnotilapia dardennii, Ctenochromis horei and Gnathochromis pfefferi, are all infected by a single unique Cichlidogyrus sp. The genital and haptoral structure of the new species suggests a close relationship, which might mirror the close affinities between the hosts within the Tropheini. Based on haptoral configuration, the new species belong to a morphological group within the genus containing parasites both of West African cichlids and of Haplochromini, and hence, do not represent a new organisation of the attachment organ (as has recently been described of congeners infecting the ectodine cichlid Ophthalmotilapia).

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

43,34 €

Price includes VAT (Finland)
Tax calculation will be finalised during checkout.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

References

  • Blais J, Rico C, van Oosterhout C, Cable J, Turner GF, Bernatchez L (2007) MHC adaptive divergence between closely related and sympatric African cichlids. PLoS ONE 2:8

    Article  Google Scholar 

  • Cohen AS, Lezzar KE, Tiercelin JJ, Soreghan M (1997) New palaeogeographic and lake-level reconstructions of Lake Tanganyika: implications for tectonic, climatic and biological evolution in a rift lake. Basin Res 9:107–132

    Article  Google Scholar 

  • Douëllou L (1993) Monogeneans of the genus Cichlidogyrus Paperna, 1960 (Dactylogyridae: Ancyrocephalinae) from cichlid fishes of Lake Kariba (Zimbabwe) with descriptions of five new species. Syst Parasitol 25:159–186

    Article  Google Scholar 

  • Eschmeyer WN, Fricke R (eds) (2011). Catalog of Fishes electronic version. http://research.calacademy.org/ichthyology/catalog/fishcatmain.asp. Accessed 10 February 2011

  • Euzet L, Prost M (1981) Report of the meeting on Monogenea: problems of systematics, biology and ecology. In: Slusarski W (ed) Review of advances in parasitology. P.W.N. Polish Scientific Publishers, Warsaw, pp 1003–1004

    Google Scholar 

  • Gregory RD (1990) Parasites and host geographic range as illustrated by waterfowl. Funct Ecol 4:645–654

    Article  Google Scholar 

  • Gussev AV (1962, 1964) Order Dactylogyridea. In: Bychovskaya-Pavlovskaya IE, Gussev AV, Dubinina MN, Izymova NA, Smirnova TS, Sokolovskaya IL, Shtein GA, Shul’man SS, Epsthein VM (eds) Key to the parasites of freshwater fish of the USSR. Israel Program for Scientific Translations, Jerusalem, pp 204–342 [Russian original: Opredelitel’ parazitov presnovohnyh ryb SSSR. Moscow-Leningrad: Izadtel’stovo Akademii Nauk SSSR]

  • Harris PD, Cable J (2000) Gyrodactylus poeciliae n. sp. and G. milleri n. sp. (Monogenea: Gyrodactylidae) from Poecilia caucana (Steindachner) in Venezuela. Syst Parasitol 47:79–85

    PubMed  Article  CAS  Google Scholar 

  • Huyse T, Malmberg G (2004) Molecular and morphological comparisons between Gyrodactylus ostendicus n. sp. (Monogenea: Gyrodactylidae) on Pomatoschistus microps (Krøyer) and G. harengi Malmberg, 1957 on Clupea harengus membras L. Syst Parasitol 58:105–113

    PubMed  Article  Google Scholar 

  • Kabata Z (1985) Parasites and diseases of fish cultured in the tropics. Taylor & Francis, London and Philadelphia

    Google Scholar 

  • Koblmüller S, Sefc KM, Sturmbauer C (2008) The Lake Tanganyika cichlid species assemblage: recent advances in molecular phylogenetics. Hydrobiologia 615:5–20

    Article  Google Scholar 

  • Koblmüller S, Egger B, Sturmbauer C, Sefc KM (2010) Rapid radiation, ancient incomplete lineage sorting and ancient hybridization in the endemic Lake Tanganyika cichlid tribe Tropheini. Mol Phylogenet Evol 55:318–334

    PubMed  Article  Google Scholar 

  • Konings A (1998) Tanganyika cichlids in their natural habitat. Cichlid Press, El Paso

    Google Scholar 

  • Kornfield I, Smith PF (2000) African cichlid fishes: model systems for evolutionary biology. Annu Rev Ecol Syst 31:163–196

    Article  Google Scholar 

  • Maan M, Van Rooijen AMC, Van Alphen JJM, Seehausen O (2008) Parasite-mediated sexual selection and species divergence in Lake Victoria cichlid fish. Biol J Linn Soc 94:53–60

    Article  Google Scholar 

  • Malmberg G (1957) On the occurence of Gyrodactylus on Swedish fishes. Skr Söd Sver Fiskför Asskr 1956:19–76 [in Swedish]

    Google Scholar 

  • Meyer A, Knowles LL, Verheyen E (1996) Widespread geographical distribution of mitochondrial haplotypes in rock-dwelling cichlid fishes from Lake Tanganyika. Mol Ecol 5:341–350

    PubMed  CAS  Google Scholar 

  • Mwita C, Nkwengulila G (2008) Determinants of the parasite community of clariid fishes from Lake Victoria, Tanzania. J Helminthol 82:7–16

    PubMed  Article  Google Scholar 

  • Nieberding CM, Olivieri I (2007) Parasites: proxies for host genealogy and ecology? Trends Ecol Evol 22(3):156–165

    PubMed  Article  Google Scholar 

  • Page RDM, Holmes EC (1998) Molecular evolution: a phylogenetic approach. Blackwell, Malden, Oxford and Carlton

    Google Scholar 

  • Paperna I (1960) Studies on monogenetic trematodes in Israel. 2. Monogenetic trematodes of cichlids. Bamidgeh 12:20–33

    Google Scholar 

  • Paperna I (1979) Monogenea of inland water fish in Africa. Annalen Koninklijk Museum voor Midden-Afrika Zoologische Wetenschappen 226, Tervuren

  • Paperna I (1996) Parasites, infections and diseases of fishes in Africa. An update. CIFA Technical Paper 31. Food and Agriculture Organization, Rome

    Google Scholar 

  • Pariselle A, Euzet L (1995) Gill parasites of the genus Cichlidogyrus Paperna, 1960 (Monogenea, Ancyrocephalidae) from Tilapia guineensis (Bleeker, 1862), with descriptions of six new species. Syst Parasitol 30:187–198

    Article  Google Scholar 

  • Pariselle A, Euzet L (2003) Four new species of Cichlidogyrus (Monogenea: Ancyrocephalidae), gill parasites of Tilapia cabrae (Teleostei: Cichlidae), with discussion on relative length of haptoral sclerites. Folia Parasit 50:195–201

    Google Scholar 

  • Pariselle A, Euzet L (2009) Systematic revision of dactylogyridean parasites (Monogenea) from cichlid fishes in Africa, the Levant and Madagascar. Zoosystema 31(4):849–898

    Article  Google Scholar 

  • Pariselle A, Bilong Bilong C, Euzet L (2003a) Four new species of Cichlidogyrus Paperna, 1960 (Monogenea, Ancyrocephalidae), all gill parasites from African mouthbreeder tilapias of the genera Sarotherodon and Oreochromis (Pisces, Cichlidae), with a re-description of C. thurstonae Ergens, 1981. Syst Parasitol 56:201–210

    PubMed  Article  Google Scholar 

  • Pariselle A, Morand S, Deveney M, Pouyaud L (2003b) Parasite species richness of closely related hosts: historical scenario and “genetic” hypothesis. In: Combes C, Jourdan J (eds) Hommage à Louis Euzet—taxonomie, écologie et évolution des métazoaires parasites. Taxonomy, ecology and evolution of metazoan parasites. Presses Universitaires de Perpignan, Perpignan, pp 147–166

    Google Scholar 

  • Poll M (1986) Classification des Cichlidae du lac Tanganika. Tribus, genres et espèces. Mémoires de la Classe des Sciences XLV, 2nd edn. Académie Royale de Belgique, Brussels

    Google Scholar 

  • Pouyaud L, Desmarais E, Deveney M, Pariselle A (2006) Phylogenetic relationships among monogenean gill parasites (Dactylogyridae, Ancyrocephalidae) infesting tilapiine hosts (Cichlidae): systematic and evolutionary implications. Mol Phylogenet Evol 38:241–249

    PubMed  Article  CAS  Google Scholar 

  • Salzburger W, Mack T, Verheyen E, Meyer A (2005) Out of Tanganyika: genesis, explosive speciation, key-innovations and phylogeography of the haplochromine cichlid fishes. BMC Evol Biol 5:17

    PubMed  Article  Google Scholar 

  • Snoeks J (2000) How well known is the ichthyodiversity of the large East African lakes? Adv Ecol Res 31:17–38

    Article  Google Scholar 

  • Sturmbauer C, Hainz U, Baric S, Verheyen E, Salzburger W (2003) Evolution of the tribe Tropheini from Lake Tanganyika: synchronized explosive speciation producing multiple evolutionary parallelism. Hydrobiologia 500:51–64

    Article  Google Scholar 

  • Vanhove MPM, Snoeks J, Volckaert FAM, Huyse T (2011a) First description of monogenean parasites in Lake Tanganyika: the cichlid Simochromis diagramma (Teleostei, Cichlidae) harbours a high diversity of Gyrodactylus species (Platyhelminthes, Monogenea). Parasitology 138(3):364–380

    PubMed  Article  CAS  Google Scholar 

  • Vanhove MPM, Volckaert FAM, Pariselle A (2011b) Ancyrocephalidae (Monogenea) of Lake Tanganyika: I: Four new species of Cichlidogyrus from Ophthalmotilapia ventralis (Teleostei, Cichlidae), the first record of this family in the basin. Zoologia (Curitiba, Impr) 28(2):253–263

  • Vignon M, Pariselle A, Vanhove MPM (2011) Modularity in attachment organs of African Cichlidogyrus (Platyhelminthes, Monogenea, Ancyrocephalidae) reflects phylogeny rather than host specificity or geographic distribution. Biol J Linn Soc 102(3):694–706

    Article  Google Scholar 

  • Wagner CE, McCune AR (2009) Contrasting patterns of spatial genetic structure in sympatric rock-dwelling cichlid fishes. Evolution 63:1312–1326

    PubMed  Article  Google Scholar 

  • Yuma M, Narita T, Hori M, Kondo T (1998) Food resources of shrimp-eating cichlid fishes in Lake Tanganyika. Env Biol Fish 52(1–3):371–378

    Article  Google Scholar 

  • Ziętara MS, Lumme J (2003) The crossroads of molecular, typological and biological species concepts: two new species of Gyrodactylus Nordmann, 1832 (Monogenea: Gyrodactylidae). Syst Parasitol 55:39–52

    PubMed  Article  Google Scholar 

Download references

Acknowledgements

Prof. J. Snoeks (RMCA/K.U.Leuven) is gratefully acknowledged for his input and for commenting on an earlier version of the manuscript; Prof. C. Sturmbauer (Karl-Franzens University of Graz) for organizing the expedition to Zambia and Tanzania, and for host identification; M. Van Steenberge (K.U.Leuven/RMCA), J. Raeymaekers (K.U.Leuven), J.K. Zimba, L. Makasa (Lake Tanganyika Research Station, Mpulungu, Zambia), T. Veall, O.R. Mangwangwa (Rift Valley Tropicals, Zambia/Tanzania), M. Nshombo, N. Mulimbwa, R. Muzumani, B. Muterezi, N. Mbirize, L. Kapepula (Centre de Recherche en Hydrobiologie, Uvira, DRC), C. Katongo (University of Zambia, Lusaka) and their technical staff, for scientific, logistical and administrative contributions to the fieldwork; the Tanzania Commission for Science and Technology (COSTECH) for research permit no. 2007-258-CC-2006-151 to M.P.M.V. and T.H., respectively, are PhD and post-doctoral fellows of the Research Foundation–Flanders (FWO–Vlaanderen). Fieldwork was funded by two travel grants from the Research Foundation–Flanders and one from the King Leopold III Fund for Nature Conservation and Exploration to M.P.M.V.

Author information

Author notes

  1. Céline Gillardin

    Present address: ZAVO, Hoogstraat 3 and Groenstraat 13, 1930, Zaventem, Belgium

Affiliations

  1. Laboratory of Animal Diversity and Systematics, Biology Department, Katholieke Universiteit Leuven, Charles Deberiotstraat 32, 3000, Leuven, Belgium

    Céline Gillardin, Maarten P. M. Vanhove, Tine Huyse & Filip A. M. Volckaert

  2. Ichthyology Unit, African Zoology Department, Royal Museum for Central Africa, Leuvensesteenweg 13, 3080, Tervuren, Belgium

    Maarten P. M. Vanhove

  3. IRD (ex-ORSTOM)/ISE-M, UR226/UMR5554, Université Montpellier II - CC 063, 34095, Montpellier Cedex 5, France

    Antoine Pariselle

Authors
  1. Céline Gillardin
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Maarten P. M. Vanhove
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Antoine Pariselle
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Tine Huyse
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Filip A. M. Volckaert
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Maarten P. M. Vanhove.

Additional information

Céline Gillardin and Maarten P.M. Vanhove contributed equally to this paper.

Tine Huyse and Filip A. M. Volckaert are joint senior authors.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Gillardin, C., Vanhove, M.P.M., Pariselle, A. et al. Ancyrocephalidae (Monogenea) of Lake Tanganyika: II: description of the first Cichlidogyrus spp. parasites from Tropheini fish hosts (Teleostei, Cichlidae). Parasitol Res 110, 305–313 (2012). https://doi.org/10.1007/s00436-011-2490-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00436-011-2490-5

Keywords

  • Africa
  • Cichlid parasites
  • Ctenochromis horei
  • Gnathochromis pfefferi
  • Limnotilapia dardennii
  • Platyhelminthes