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Diversity and host specificity of monogenean gill parasites (Platyhelminthes) of cichlid fishes in the Bangweulu-Mweru ecoregion

Published online by Cambridge University Press:  22 August 2017

M.W.P. Jorissen ,
A. Pariselle ,
T. Huyse ,
E.J. Vreven ,
J. Snoeks ,
F.A.M. Volckaert ,
A. Chocha Manda ,
G. Kapepula Kasembele ,
T. Artois  and
M.P.M. Vanhove
M.W.P. Jorissen*
Affiliation:
Department of Biology, Royal Museum for Central Africa, Leuvensesteenweg 13, BE-3080 Tervuren, Belgium Research Group Zoology: Biodiversity & Toxicology, Centre for Environmental Sciences, Hasselt University, BE-3590 Diepenbeek, Belgium
A. Pariselle
Affiliation:
Institut des Sciences de l'Evolution, IRD, B.P. 1857, Yaoundé, Cameroon
T. Huyse
Affiliation:
Department of Biology, Royal Museum for Central Africa, Leuvensesteenweg 13, BE-3080 Tervuren, Belgium Laboratory of Biodiversity and Evolutionary Genomics, Department of Biology, University of Leuven, Ch. Deberiotstraat 32, BE-3000 Leuven, Belgium
E.J. Vreven
Affiliation:
Department of Biology, Royal Museum for Central Africa, Leuvensesteenweg 13, BE-3080 Tervuren, Belgium
J. Snoeks
Affiliation:
Department of Biology, Royal Museum for Central Africa, Leuvensesteenweg 13, BE-3080 Tervuren, Belgium Laboratory of Biodiversity and Evolutionary Genomics, Department of Biology, University of Leuven, Ch. Deberiotstraat 32, BE-3000 Leuven, Belgium
F.A.M. Volckaert
Affiliation:
Laboratory of Biodiversity and Evolutionary Genomics, Department of Biology, University of Leuven, Ch. Deberiotstraat 32, BE-3000 Leuven, Belgium
A. Chocha Manda
Affiliation:
Unité de recherche en Biodiversité et Exploitation durable des Zones Humides (BEZHU), Faculté des Sciences Agronomiques, Université de Lubumbashi, Haut-Katanga, R.D. Congo
G. Kapepula Kasembele
Affiliation:
Unité de recherche en Biodiversité et Exploitation durable des Zones Humides (BEZHU), Faculté des Sciences Agronomiques, Université de Lubumbashi, Haut-Katanga, R.D. Congo
T. Artois
Affiliation:
Research Group Zoology: Biodiversity & Toxicology, Centre for Environmental Sciences, Hasselt University, BE-3590 Diepenbeek, Belgium
M.P.M. Vanhove
Affiliation:
Department of Biology, Royal Museum for Central Africa, Leuvensesteenweg 13, BE-3080 Tervuren, Belgium Research Group Zoology: Biodiversity & Toxicology, Centre for Environmental Sciences, Hasselt University, BE-3590 Diepenbeek, Belgium Laboratory of Biodiversity and Evolutionary Genomics, Department of Biology, University of Leuven, Ch. Deberiotstraat 32, BE-3000 Leuven, Belgium Capacities for Biodiversity and Sustainable Development, Operational Directorate Natural Environment, Royal Belgian Institute of Natural Sciences, Vautierstraat 29, 1000 Brussels, Belgium Department of Botany and Zoology, Faculty of Science, Masaryk University, Kotlářská 2, CZ-611 37 Brno, Czech Republic
*
*E-mail: michiel.jorissen@uhasselt.be
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Abstract

This study represents the first exploration of the parasite fauna of cichlid fishes in the Mweru-Luapula subregion (Central Africa). Twelve species of cichlids and 14 species of Monogenea from three genera (Cichlidogyrus, Gyrodactylus and Scutogyrus) were collected. We present a first record of the gill parasite fauna of eight host species, Oreochromis mweruensis, Orthochromis sp. ‘Mambilima’, Sargochromis mellandi, Serranochromis angusticeps, S. stappersi, S. thumbergi and Tylochromis mylodon. The host range of ten parasite species was expanded. The study further includes the description of Cichlidogyrus consobrini sp. n. from S. mellandi and Orthochromis sp. ‘Mambilima’. A new morphotype of C. halli is characterized, and three species – C. papernastrema, C. quaestio and C. zambezensis – are redescribed. Furthermore, the biodiversity and host specificity of these parasites is compared with that of cichlid parasites from Lake Kariba and Cameroon. Two species, including C. consobrini sp. n. and a new morphotype of C. halli, are putative endemics. The parasite fauna in Bangweulu-Mweru is highly similar in species composition to Lake Kariba, but in Bangweulu-Mweru the same parasite species are more host-specific, probably because of hydrogeographical differences between the two regions.

Type
Research Paper
Information
Journal of Helminthology , Volume 92 , Issue 4 , July 2018 , pp. 417 - 437
Copyright
Copyright © Cambridge University Press 2017 

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References

Bakke, T.A., Cable, J. & Harris, P.D. (2007) The biology of gyrodactylid monogeneans: the ‘Russian doll killers’. Advances in Parasitology 64, 161–376.CrossRefGoogle ScholarPubMed
Barson, M., Přikrylová, I., Vanhove, M.P.M. & Huyse, T. (2010) Parasite hybridization in African Macrogyrodactylus spp. (Monogenea, Platyhelminthes) signals historical host distribution. Parasitology 137, 1585–1595.CrossRefGoogle ScholarPubMed
Bates, J.W. (1997) The slide sealing compound ‘Glyceel’. Journal of Nematology 29, 565.Google Scholar
Beletew, M., Getahun, A. & Vanhove, M.P.M. (2016) First report of monogenean flatworms from Lake Tana, Ethiopia: gill parasites of the commercially important Clarias gariepinus (Teleostei: Clariidae) and Oreochromis niloticus tana (Teleostei: Cichlidae). Parasites & Vectors 9, 410. doi: 10.1186/s13071-016-1691-2.Google Scholar
Combes, C. (1990) Rencontre, identification, installation dans le cycle des métazoaires parasites. Bulletin de la Société Zoologique de France 115, 99–105.Google Scholar
Cribb, T.H., Chisholm, L.A. & Bray, A.R. (2002) Diversity in the Monogenea and Digenea: does lifestyle matter? International Journal for Parasitology 32, 321–328.Google Scholar
De Vos, L., Snoeks, J. & Thys Van Den Audenaerde, D.F.E. (2001) An annotated checklist of the fishes of Rwanda (East Central Africa)., with historical data on introductions of commercially important species. Journal of East African Natural History 90, 41–68.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. Systematic Parasitology 50, 159–186.Google Scholar
Dunz, A.R. & Schliewen, U.K. (2012) Molecular phylogeny and revised classification of the haplotilapiine cichlid fishes formerly referred to as ‘Tilapia’. Molecular Phylogenetics and Evolution 68, 64–80.Google Scholar
Fannes, W., Vanhove, M.P.M, & Huyse, T. (2017) Redescription of Cichlidogyrus tiberianus Paperna, 1960 and C. dossoui Douëllou, 1993 (Monogenea: Ancyrocephalidae), with special reference to the male copulatory organ. Systematic Parasitology 94, 133–144.Google Scholar
FEOW (Freshwater Ecoregions Of the World). (2016) Available at www.feow.org (accessed 28 October 2016).Google Scholar
Friedman, M., Keck, B.P., Dornburg, A., Eytan, R.I., Martin, C.H., Hulsey, C.D., Wainwright, P.C. & Near, T.J. (2013) Molecular and fossil evidence place the origin of cichlid fishes long after Gondwanan rifting. Proceedings of the Royal Society for Biological Sciences. doi: 10.1098/rspb.2013.1733.Google Scholar
Froese, R. & Pauly, D. (Eds) (2015) FishBase. World Wide Web electronic publication. Available at http://www.fishbase.org (accessed 1 November 2016).Google Scholar
Gillardin, C., Vanhove, M.P.M., Pariselle, A., Huyse, T. & Volckaert, F.A.M. (2012) Ancyrocephalidae (Monogenea) of Lake Tanganyika: II: description of the first Cichlidogyrus spp. parasites from tropheine fish hosts (Teleostei, Cichlidae). Parasitology Research 110, 305–313.Google Scholar
ICZN (International Commission on Zoological Nomenclature). (1999) International Code of Zoological Nomenclature. Available at http://www.nhm.ac.uk/hosted-sites/iczn/code/ (accessed 3 February 2017).Google Scholar
Joyce, D.A., Lunt, D.H., Bills, R., Turner, G.F., Katongo, C., Duftner, N., Sturmbauer, C. & Seehausen, O. (2005) An extant cichlid fish radiation emerged in an extinct Pleistocene lake. Nature 435, 90–95.Google Scholar
Katongo, C., Koblmüller, S., Duftner, N., Mumba, L. & Sturmbauer, C. (2007) Evolutionary history and biogeographic affinities of the serranochromine cichlids in Zambian rivers. Molecular Phylogenetics and Evolution 45, 326–338.Google Scholar
Key, R.M., De Wasele, B. & Liyngu, A.K. (2004) A multi-element baseline geochemical database from the western extension of the Central Africa Copperbelt in northwestern Zambia. Applied Earth Sciences (Transactions of the Institution for Mining and Metallurgy) 113, 205–226.Google Scholar
Kmentová, N., Gelnar, M., Koblmüller, S. & Vanhove, M.P.M. (2016a) First insights into the diversity of gill monogeneans of ‘Gnathochromis’ and Limnochromis (Teleostei: Cichlidae) in Burundi: do the parasites mirror host ecology and phylogenetic history? PeerJ 4, e1629. https://doi.org/10.7717/peerj.1629.Google Scholar
Kmentová, N., Gelnar, M., Mendlová, M., Van Steenberge, M., Koblmüller, S. & Vanhove, M.P. (2016b) Reduced host-specificity in a parasite infecting non-littoral Lake Tanganyika cichlids evidenced by intraspecific morphological and genetic diversity. Scientific Reports 6, 39605. doi:10.1038/srep39605.CrossRefGoogle Scholar
Koblmüller, S., Schlieuwen, U.K., Duftner, N., Sefc, K.N., Katongo, C. & Sturmbauer, C. (2008) Age and spread of Haplochromine cichlid fishes in Africa. Molecular Phylogenetics and Evolution 49, 153–169.Google Scholar
Korallo-Vinarskaya, N.P., Krasnov, B.R., Vinarski, M.V., Shenbrot, G.I., Mouillot, D. & Poulin, R. (2009) Stability in abundance and niche breadth of gamasid mites across environmental conditions, parasite identity and host pools. Evolutionary Ecology 23, 329–345.Google Scholar
Krasnov, B.R., Mouillot, D., Shenbrot, G.I., Khoklova, I.S. & Poulin, R. (2004) Geographical variation in host specificity of fleas (Siphonaptera): the influence of phylogeny and local environmental conditions. Ecography 27, 787–797.Google Scholar
Lévêque, C. (1997) Biodiversity dynamics and conservation: the freshwater fish of tropical Africa. 1st edn. 438 pp. Cambridge, Cambridge University Press.Google Scholar
Lim, S.-Y., Ooi, A-L. & Wong, W.-L. (2016) Gill monogeneans of Nile tilapia (Oreochromis niloticus) and red hybrid tilapia (Oreochromis spp.) from the wild and fish farms in Perak, Malaysia: infection dynamics and spatial distribution. Springerplus 5, 1609.Google Scholar
Madanire-Moyo, G.N., Luus-Powell, W.J. & Olivier, P.A. (2012) Diversity of metazoan parasites of the Mozambique tilapia, Oreochromis mossambicus (Peters, 1852), as indicators of pollution in the Limpopo and Olifants River systems. Onderstepoort Journal of Veterinary Research. doi: 10.4102/ojvr.v79i1.362.Google Scholar
Mendlová, M. & Šimková, A. (2014) Evolution of host specificity in monogeneans parasitizing African cichlid fish. Parasites & Vectors 7, 69. doi: 10.1186/1756-3305-7-69.Google Scholar
Mendlová, M., Pariselle, A., Vyskočilová, M. & Šimková, A. (2010) Molecular phylogeny of monogeneans parasitizing African freshwater Cichlidae inferred from LSU rDNA sequences. Parasitology Research 107, 1405–1413.Google Scholar
Messu Mandeng, F.D.M., Bilong Bilong, C.F., Pariselle, A., Vanhove, M.P.M., Bitja Nyom, A.R. & Agnèse, J.F. (2015) A phylogeny of Cichlidogyrus spp. (Monogenea, Dactylogyridae) clarifies a host-switch between fish families and reveals an adaptive component to attachment organ morphology of this parasite genus. Parasites & Vectors 8, 852. doi: 10.1186/s13071-015-1181-y.CrossRefGoogle Scholar
Mogoi Rindoria, N., Kamau Mungai, L., Wamalwa Yasindi, A. & Onjango Otachi, E. (2016) Gill monogeneans of Oreochromis niloticus (Linnaeus, 1758) and Oreochromis leucostictus (Trewavas, 1933) in Lake Naivasha, Kenya. Parasitology Research 115, 1501–1508.Google Scholar
Moore, A.E. & Larkin, P.A. (2001) Drainage evolution in south central-Africa since the breakup of Gondwana. South African Journal of Geology 200, 47–68.Google Scholar
Murray, A.M. (2001) The fossil record and biogeography of the Cichlidae (Actinopterygii: Labroidei). Biological Journal of the Linnean Society 74, 517–532.Google Scholar
Muterezi Bukinga, F., Vanhove, M.P.M., Van Steenberge, M. & Pariselle, A. (2012) Ancyrocephalidae (Monogenea) of Lake Tanganyika: III: Cichlidogyrus infecting the world's biggest cichlid and the non-endemic tribes Haplochromini, Oreochromini and Tylochromini (Teleostei, Cichlidae). Parasitology Research 111, 2049–2061.CrossRefGoogle ScholarPubMed
Nack, J., Bitja Nyom, A.R., Pariselle, A. & Bilong Bilong, C.F. (2015) New evidence of a lateral transfer of monogenean parasite between distant fish hosts in Lake Ossa, South Cameroon: the case of Quadriacanthus euzeti n. sp. Journal of Helminthology. doi:10.1017/S0022149X15000577.Google Scholar
Paperna, I. (1973) New species of Monogenea from African freshwater fish. A preliminary report. Revue de Zoologie et Botanique Africaines 87, 505–518.Google Scholar
Paperna, I. (1979) Monogenea of inland water fish in Africa. Annales du Musée Royale d'Afrique Centrale sér in-8° (Zool.) 226, 1–131.Google Scholar
Pariselle, A. & Euzet, L. (1996) Cichlidogyrus Paperna, 1960 (Monogenea: Ancyrocephalidae): gill parasites from West African Cichlidae of the subgenus Coptodon Regan, 1920 (Pisces), with descriptions of six new species. Systematic Parasitology 34, 109–124.CrossRefGoogle 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 Parasitologica 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, 849–898.CrossRefGoogle Scholar
Pariselle, A., Boeger, W.A., Snoeks, J., Bilong Bilong, C.F., Morand, S. & Vanhove, M.P.M. (2011) The monogenean parasite fauna of of cichlids: A potential tool for host biogeography. International Journal for Evolutionary Biology. doi:10.4061/2011/471480.Google Scholar
Pariselle, A., Bitja Nyam, A.R. & Bilong Bilong, C.F. (2013) Checklist of the ancyrocephalids (Monogenea) parasitizing Tilapia species in Cameroon, with the description of three new species. Zootaxa 3599, 78–86.Google Scholar
Pariselle, A., Bitja Nyom, A.R. & Bilong Bilong, C.F. (2014) Four new species of Cichlidogyrus (Monogenea, Ancyrocephalidae) from Sarotherodon mvogoi and Tylochromis sudanensis (Teleostei, Cichlidae) in Cameroon. Zootaxa 3881, 258–266.Google Scholar
Pérez-Ponce de Léon, G. & Choudhury, A. (2005) Biogeography of helminth parasites of freshwater fishes in Mexico: the search for patterns and processes. Journal of Biogeography 32, 645–659.Google Scholar
Poulin, R. & Morand, S. (2004) Parasite biodiversity. Washington, DC, USA, Smithsonian Institution Press.Google Scholar
Pouyaud, L., Desmarais, E., Deveny, M. & Pariselle, A. (2006) Phylogenetic relationships among monogenean gill parasites (Dactylogyridae, Ancyrocephalidae) infesting tilapiine hosts (Cichlidae): systematic and evolutionary implications. Molecular Phylogenetics and Evolution 38, 241–249.CrossRefGoogle Scholar
Price, C.E. & Kirk, R.G. (1967) First description of a monogenetic trematode from Malawi. Revue de Zoologie et Botanique Africaines 76, 137–143.Google Scholar
Price, C.E., Peebles, H.E. & Bamford, T. (1969) The Monogenean parasites of African fishes – IV. Two new species from South African hosts. Revue de Zoologie et de Botanique Africaines LXXIX, 117–124.Google Scholar
Schedel, F.D.B., Friel, J.P. & Schlieuwen, U.K. (2014) Haplochromis vanheusdeni a new haplochromine cichlid species from the Great Ruaha River drainage, Rufiji Basin, Tanzania. Spixiana 37, 135–149.Google Scholar
Schwanck, E. (1994) Behaviour and colour differences between O. macrochir and O. mweruensis (Teleostei: Cichlidae). Ichthyological Exploration of Freshwaters 5, 267–280.Google Scholar
Schwarzer, J., Misof, B., Tautz, D. & Schliewen, U.K. (2009) The root of the East African cichlid radiations. BMC Evolutionary Biology 9, 186.CrossRefGoogle ScholarPubMed
Shinn, A.P., Paladini, G., Rubio-Godoy, M., Domingues, M.V., Whittington, I.D. & Bron, J.E. (2011) MonoDb. A webhost for Monogenea. World Wide Web electronic publication. Available at http://www.monodb.org (accessed 12 October 2016).Google Scholar
Skelton, P.H. (2001) A complete guide to the freshwater fishes of southern Africa. 388 pp. Capetown, Struik Publishers.Google Scholar
Sparks, J.S. & Smith, W.L. (2005) Freshwater fishes, dispersal ability, and nonevidence: ‘Gondwana Life Rafts’ to the rescue. Systematic Biology 54, 158–165.Google Scholar
Thieme, M.L., Abell, R., Stiassny, M.L.J., Skelton, P., Lehner, B., Teugels, B.B., Dinerstein, E., Kamdem-Toham, A., Burgess, N. & Olson, D. (2005) Freshwater ecoregions of Africa and Madagascar: A conservation assessment. 483 pp. Washington DC, Island Press.Google Scholar
Thys Van Den Audenaerde, D.F.E. (1964) Revision systematique des especes congolaises du genre Tilapia (Pisces, Cichlidae). Annales du Musee Royal de l'Afrique Centrale, Sciences Zoologiques 124, 1–155.Google Scholar
Thys Van Den Audenaerde, D.F.E. (1988) Natural distribution of tilapias and its consequences for the possible protection of genetic resources. pp. 1–12 in Pullin, R.S.V. (Ed.) Tilapia genetic resources for aquaculture. ICLARM Conference Proceedings 16.Google Scholar
Trewavas, E. (1983) Tilapiine fishes of the genera Sarotherodon, Oreochromis and Danakilia. 1st edn. 583 pp. London, British Museum of Natural History.Google Scholar
Valois, A.E. & Poulin, R. (2015) Global drivers of parasitism in freshwater plankton communities. Limnology and Oceanography 60, 1707–1718.Google Scholar
Vanhove, M.P.M., Van Steenberge, M., Dessein, S., Volckaert, F.A.M., Snoeks, J., Huyse, T. & Pariselle, A. (2013) Biogeographical implications of Zambezian Cichlidogyrus species (Platyhelminthes: Monogenea: Ancyrocephalidae) parasitizing Congolian cichlids. Zootaxa 3608, 398–400.Google Scholar
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 biogeography. Trends in Parasitology 1536, 820–832.CrossRefGoogle Scholar
Van Steenberge, M., Vreven, E. & Snoeks, J. (2014) The fishes of the Upper Luapula area (Congo Basin): a fauna of mixed origin. Ichthyological Exploration of Freshwaters 24, 329–345.Google Scholar
Vignon, M., Pariselle, A. & Vanhove, M.P.M. (2011) Modularity in attachment organs of African Cichlidogyrus (Platyhelminthes: Monogenea: Ancyrocephalidae) reflects phylogeny rather than host specificity or geographic distribution. Biological Journal of the Linnean Society 102, 694–706.Google Scholar
Whittington, I.D., Cribb, B.W., Hamwoord, T.E. & Halliday, J.A. (2000) Host-specificity of monogenean (platyhelminth) parasites: a role for anterior adhesive areas? International Journal for Parasitology 30, 305–320.Google Scholar
Wu, X.Y., Zhu, X.Q., Xie, M.Q. & Li, A.X. (2007) The evaluation for generic-level monophyly of Ancyrocephalinae (Monogenea, Dactylogyridae) using ribosomal DNA sequence data. Molecular Phylogenetics and Evolution 44, 530–544.Google Scholar
Zago, A.C., Franceschini, L., Garcia, F., Schalch, S.H.C., Gozi, K.S. & da Silva, R.J. (2014) Ectoparasites of Nile tilapia (Oreochromis niloticus) in cage farming in a hydroelectric reservoir in Brazil. Revista Brasilieira de Parasitologica Veterinária 23. doi: 10.1590/S1984-29612014041.Google Scholar
Zahradníčková, P., Barson, M., Luus-Powell, W.J. & Přikrylová, I. (2016) Species of Gyrodactylus Von Nordmann, 1832 (Platyhelminthes: Monogenea) from cichlids from Zambezi and Limpopo river basins in Zimbabwe and South Africa: evidence for unexplored species richness. Systematic Parasitology 93, 679–700.Google Scholar
Zengeya, T.A., Booth, A.J., Bastos, A.D.S. & Chimimba, C.T. (2011) Trophic interrelationships between the exotic Nile tilapia, Oreochromis niloticus and indigenous tilapiine cichlids in a subtropical African river system (Limpopo River, South Africa). Environmental Biology of Fishes 92, 479–489.Google Scholar