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Diversity and Host Specificity of Monogenean Gill Parasites (Platyhelminthes) of Cichlid Fishes in the Bangweulu-Mweru Ecoregion

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Diversity and Host Specificity of Monogenean Gill Parasites (Platyhelminthes) of Cichlid Fishes in the Bangweulu-Mweru Ecoregion Journal of Helminthology (2018) 92, 417–437 doi:10.1017/S0022149X17000712 © Cambridge University Press 2017 Diversity and host specificity of monogenean gill parasites (Platyhelminthes) of cichlid fishes in the Bangweulu-Mweru ecoregion M.W.P. Jorissen1,2*, A. Pariselle3,T.Huyse1,4, E.J. Vreven1, J. Snoeks1,4, F.A.M. Volckaert4, A. Chocha Manda5, G. Kapepula Kasembele5, T. Artois2 and M.P.M. Vanhove1,2,4,6,7 1Department of Biology, Royal Museum for Central Africa, Leuvensesteenweg 13, BE-3080 Tervuren, Belgium: 2Research Group Zoology: Biodiversity & Toxicology, Centre for Environmental Sciences, Hasselt University, BE-3590 Diepenbeek, Belgium: 3Institut des Sciences de l’Evolution, IRD, B.P. 1857, Yaoundé, Cameroon: 4Laboratory of Biodiversity and Evolutionary Genomics, Department of Biology, University of Leuven, Ch. Deberiotstraat 32, BE-3000 Leuven, Belgium: 5Unité de recherche en Biodiversité et Exploitation durable des Zones Humides (BEZHU), Faculté des Sciences Agronomiques, Université de Lubumbashi, Haut-Katanga, R.D. Congo: 6Capacities for Biodiversity and Sustainable Development, Operational Directorate Natural Environment, Royal Belgian Institute of Natural Sciences, Vautierstraat 29, 1000 Brussels, Belgium: 7Department of Botany and Zoology, Faculty of Science, Masaryk University, Kotlářská 2, CZ-611 37 Brno, Czech Republic (Received 11 April 2017; Accepted 16 July 2017; First published online 22 August 2017) 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 char- acterized, 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 pu- tative 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 differ- ences between the two regions. *E-mail: [email protected] Downloaded from https://www.cambridge.org/core. KU Leuven Libraries, on 22 May 2019 at 13:07:48, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1017/S0022149X17000712 418 M.W.P. Jorissen et al. Introduction from the Congo Basin to palaeolake Makgadikgadi, where they experienced an explosive radiation (Joyce The Bangweulu-Mweru ecoregion is part of the Congo et al., 2005). When the lake dried up, several species per- basin and covers the south-eastern part of the Democratic sisted in the southern African rivers and dispersed from Republic of Congo (DRC) and the north-eastern part of there (Joyce et al., 2005) into the Congo Basin (Katongo Zambia (Thieme et al., 2005; FEOW, 2016). It lies just et al., 2007) through a recent link between the basins north of the Zambezi–Congo watershed, but parts of the (Lévêque, 1997;Keyet al., 2004). ecoregion drained into the Zambezi Basin from the late In complex biogeographical situations, e.g. the disper- Tertiary (Moore & Larkin, 2001) up to the Holocene sal of serranochromine cichlids across the Zambezi– (Lévêque, 1997; Key et al., 2004; Katongo et al., 2007; Congo watershed, hydrology and molecular markers are Koblmüller et al., 2008). These historical connections are used as biogeographical tools (Joyce et al., 2005; Katongo also reflected in the freshwater fish fauna, which is highly et al., 2007; Koblmüller et al., 2008). Additionally, fossil similar in both basins (Van Steenberge et al., 2014). The evidence is used for studies on a larger geographical freshwater fish fauna has the highest similarity with scale and on higher taxonomical levels (Murray, 2001; the Upper Congo, to which it currently drains (Van Sparks & Smith, 2005; Friedman et al., 2013). Parasites Steenberge et al., 2014). The Bangweulu-Mweru region is can also function as biogeographical tools for freshwater relatively speciose and exhibits a high degree of endem- fish biogeography (Pérez-Ponce de Léon & Choudhury, icity relative to other freshwater ecoregions (Thieme 2005; Barson et al., 2010; Pariselle et al., 2011). Although et al., 2005). The Biological Distinctiveness Index of the not often used in biogeographical research, monogeneans ecoregion is globally outstanding and the Conservation are an ideal choice as taxonomic markers. They have lim- Status Index lists it as a first priority area (Thieme et al., ited dispersal capability because they are aquatic, strictly 2005; FEOW, 2016). Bangwuelu-Mweru harbours 138 parasitic and have a direct life cycle, thus linking them fish species belonging to 58 genera and 18 families (Van strongly to the host species. Furthermore, monogeneans Steenberge et al., 2014). Within the ecoregion, the are the most host-specific of fish parasites and very Mweru-Luapula subregion is the most diverse, harbour- host-specific in general (Whittington et al., 2000; Cribb ing 135 freshwater fish species of which 35 are endemic, et al. 2002). Consequently, host species are often infected with Lake Mweru and the Lower Luapula being the by a characteristic set of monogenean species, thus pro- most speciose (Van Steenberge et al., 2014). In contrast, viding a distinguishable feature between them. the Bangweulu-Chambeshi subregion is species-poor rela- The most speciose monogenean genus on African ci- tive to Mweru-Luapula, with 93 species and a single en- chlids is Cichlidogyrus Paperna, 1960 (Dactylogyridae), demic species (Van Steenberge et al., 2014). with over 100 valid species described. It occurs solely on The Cichlidae (Teleostei: Cichliformes) have the highest the gills of African and Levantine cichlids, with the excep- number of endemic species (Thieme et al., 2005) and, after tion of C. nandidae Birgi & Lambert, 1986, C. inconsultans the Cyprinidae, constitute the second most speciose fam- Birgi & Lambert, 1986 and C. amieti Birgi & Euzet, 1983 ily (Lévêque, 1997) within Bangweulu-Mweru. A typical (Pariselle & Euzet, 2009). The former two are found on species for the Mweru-Luapula subregion is Oreochromis Polycentropsis abreviata Boulenger, 1901 (Nandidae) and mweruensis Trewavas, 1983, occurring in the Lualaba, the latter on representatives of Nothobranchidae. Species Luvua, Lake Mweru and the Lower Luapula (Schwanck, of Scutogyrus Pariselle & Euzet, 1995, a closely related 1994). It is closely related and morphologically similar genus, co-occur with representatives of Cichlidogyrus on to O. macrochir (Boulenger, 1912) (Trewavas, 1983; the gills of African cichlids, and comprise seven described Schwanck, 1994). Both species have an allopatric distribu- species (Pariselle & Euzet, 2009; Pariselle et al., 2013). tion, with O. macrochir occurring in the Upper Luapula, Representatives of both genera differ in haptor morph- Lake Bangwuelu, Chambeshi, Kafue, Kalomo, Upper ology. Representatives of Scutogyrus have a winged Zambezi, Okavango, Cunene, Buzi and Luembe rivers dorsal transversal bar with two very long auricles. They (Schwanck 1994). In 1945, a few pairs of O. mweruensis also have a thin oval-shaped plate associated with the from Mweru-Luapula were introduced in the vicinity of ventral transverse bar (Pariselle & Euzet, 2003, 2009; Lubumbashi for farming purposes (Thys van den Pariselle et al., 2013). In representatives of Cichlidogyrus Audenaerde, 1988). Also O. macrochir was introduced in the plate and wings are absent and the auricles are Bangweulu-Mweru (Kipopo) (De Vos et al. 2001). Both shorter (Pariselle & Euzet, 2009). A single exception to species hybridize, as discovered by Thys van den this is an undescribed Cichlidogyrus representative from Audenaerde (1964), but were classified as subspecies at Limnochromis auritus (Boulenger, 1901) collected in the the time. Burundese part of Lake Tanganyika; it has even longer Other common species in the region, such as Tilapia auricles than those found on Scutogyrus representatives sparrmanii Smith, 1840 and Coptodon rendalli (Boulenger, (Kmentová et al., 2016a). Phylogenetically, Scutogyrus 1857), have a wider distribution. They occur in both the forms a monophyletic clade within Cichlidogyrus, making Congo and Zambezi basins, and as far south as the the latter paraphyletic, but a formal reclassification has Limpopo Basin (Skelton, 2001; Schwarzer et al., 2009; not been carried out (Pouyaud et al., 2006;Wuet al., Zengeya et al., 2011). The serranochromine cichlids have 2007; Mendlová et al., 2010; Mendlová & Šimková, several representatives in Bangweulu-Mweru and are spe- 2014). The host range of species of Scutogyrus was limited ciose throughout southern Africa (Van Steenberge et al., to mouth-brooding cichlids, specifically Oreochromini, 2014). They also have a complex evolutionary history but one recently
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