BACKGROUND: Monogenea van Beneden, 1858 is a group of parasitic flatworms, commonly found infecting bony fish. Several genera, such as Cichlidogyrus Paperna, 1960, are reported to include potential pathogenic species that can negatively impact aquaculture fish stocks. They can switch from introduced to native fish and vice versa. In Africa (and all over the world), fish species belonging to Cichlidae are often kept in aquaculture and represent a major source of food. Thus, research on the biodiversity and occurrence of monogenean species on these fish is of importance for aquaculture and conservation. The present study is a survey of the diversity of species of Cichlidogyrus in the south of the Democratic Republic of the Congo (DRC) on three cichlid species: Orthochromis sp. 'Lomami', Serranochromis cf. macrocephalus, and Tilapia sparrmanii Smith, 1840. METHODS: Specimens of Cichlidogyrus were isolated from the gills and mounted on glass slides with Hoyer's medium. The genital and haptoral hard parts were measured and drawn using interference contrast. RESULTS: In total, six species of Cichlidogyrus were found, all new to science: C. bulbophallus n. sp. and C. pseudozambezensis n. sp. on S. cf. macrocephalus, C. flagellum n. sp. and C. lobus n. sp. on T. sparrmanii, C. ranula n. sp. on S. cf. macrocephalus and Orthochromis sp. 'Lomami', and C. maeander n. sp. found on Orthochromis sp. 'Lomami' and T. sparrmanii. The first four species are considered to be strict specialists, C. ranula n. sp. an intermediate generalist and C. maeander n. sp. a generalist. These parasite species show morphological similarities to species found in the Lower Guinea and Zambezi ichthyofaunal provinces, which might be explained by past river capture events between river systems of the Congo Province and both these regions. CONCLUSIONS: Serranochromis cf. macrocephalus and Orthochromis sp. 'Lomami' can harbour respectively three and two species of Cichlidogyrus, all described in this study. Tilapia sparrmanii can harbour seven species, of which three are described in the present study. These results highlight the species diversity of this parasite genus in the Congo Basin.

Department of Biology Royal Museum of Central Africa Tervuren Belgium

Department of Botany and Zoology Faculty of Science Masaryk University Brno Czech Republic

Ichthyology Section Zoology Department Royal Museum of Central Africa Tervuren Belgium

ISEM Université de Montpellier CNRS IRD EPHE CIRAD INRAP Montpellier France

Laboratory Biodiversity Ecology and Genome Research Centre Plant and Microbial Biotechnology Biodiversity and Environment Faculty of Sciences Mohammed 5 University Rabat Morocco

Laboratory of Biodiversity and Evolutionary Genomics Department of Biology University of Leuven Leuven Belgium

Research Group Zoology Biodiversity and Toxicology Centre for Environmental Sciences Hasselt University Diepenbeek Belgium

Section de Parasitologie Département de Biologie Centre de Recherche en Hydrobiologie Uvira Democratic Republic of the Congo

Unité de recherche en Biodiversité et Exploitation durable des Zones Humides Faculté des Sciences Agronomiques Université de Lubumbashi Lubumbashi Democratic Republic of the Congo

Zoology Unit Finnish Museum of Natural History University of Helsinki Helsinki Finland

Zobrazit více v PubMed

Gibson DI, Timofeeva TA, Gerasev PI. A catalogue of the nominal species of the monogenean genus Dactylogyrus Diesing, 1850 and their host genera. Syst Parasitol. 1996;35:3–48. doi: 10.1007/BF00012180. DOI

Cribb TH, Chisholm LA, Bray RA. Diversity in the Monogenea and Digenea: does lifestyle matter? Int J Parasitol. 2002;32:321–328. doi: 10.1016/S0020-7519(01)00333-2. PubMed DOI

Pugachev ON, Gerasev PI, Gussev AV, Ergens R, Khotenowsky I. Guide to Monogenoidea of freshwater fish of Palaearctic and Amur regions. 1. Milan, Italy: Ledizioni; 2010.

Paladini G, Longshaw M, Gustinelli A, Shinn AP. Parasitic diseases in aquaculture: their biology, diagnosis and control. In: Austin B, Newaj-Fyzul A, editors. Diagnosis and Control of Diseases of Fish and Shellfish. Hoboken: Wiley; 2017. pp. 37–107.

Bakke TA, Harris PD, Cable J. Host specificity dynamics: observations on gyrodactylid monogeneans. Int J Parasitol. 2002;32:281–308. doi: 10.1016/S0020-7519(01)00331-9. PubMed DOI

Bauer ON. Spread of parasites and diseases of aquatic organisms by acclimatization: a short review. J Fish Biol. 1991;39:679–686. doi: 10.1111/j.1095-8649.1991.tb04398.x. DOI

Šimková A, Řehulková E, Rasoloariniaina JR, Jorissen MWP, Scholz T, Faltýnková A, et al. Transmission of parasites from introduced tilapias: a new threat to endemic Malagasy ichthyofauna. Biol Invasions. 2019;21:803–819. doi: 10.1007/s10530-018-1859-0. DOI

Jiménez-García MI, Vidal-Martínez VM, López-Jiménez S. Monogeneans in introduced and native cichlids in Mexico: evidence for transfer. J Parasitol. 2001;87:907–909. PubMed

FAO . The state of world fisheries and aquaculture 2014. Rome: Food and Agriculture Organization of the United Nations; 2014.

Kullander SO. A phylogeny and classification of the South American Cichlidae (Teleostei: Perciformes) In: Malabarba LR, Reis RE, Vari RP, Lucena CAS, editors. Phylogeny and classification of Neotropical fishes. Brasil: Edipucrs; 1998. pp. 461–498.

Froese R, Pauly D, editors. FishBase. World Wide Web electronic publication. http://www.fishbase.org/search.php. Version 06/2018. Accessed 1 Jan 2018.

Snoeks J, Harrison IJ, Stiassny MLJ. The status and distribution of freshwater fishes. In: Darwall WRT, Smith KG, Allen DJ, Holland RA, Harrison IJ, Brooks EGE, editors. The diversity of life in African freshwaters: underwater, under threat. Gland, Switzerland and Cambridge, UK: IUCN; 2011. pp. 42–73.

Pariselle A, Boeger WA, Snoeks J, Bilong Bilong CF, Morand S, Vanhove MPM. The monogenean parasite fauna of cichlids: a potential tool for host biogeography. Int J Evol Biol. 2011;2011:471480. doi: 10.4061/2011/471480. PubMed DOI PMC

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

Paperna I. Onchobdella n. gen. New genus of monogenetic trematodes (Dactylogyridae, Bychowski, 1933 from cichlid fish from West Africa. Proc Helminthol Soc Wash. 1968;1968(35):200–206.

Pariselle A, Euzet L. Scutogyrus gen. n. (Monogenea, Ancyrocephalidae) for Cichlidogyrus longicornis minus Dossou, 1982, C. l. longicornis, and C. l. gravivaginus Paperna and Thurston, 1969 with description of three new species parasitic on African cichlids. J Helminthol Soc Wash. 1995;1995(62):157–173.

Christison KW, Shinn AP, van As JG. Gyrodactylus thlapi n. sp. (Monogenea) from Pseudocrenilabrus philander philander (Weber) (Cichlidae) in the Okavango Delta, Botwana. Syst Parasitol. 2005;60:165–173. doi: 10.1007/s11230-004-6342-x. PubMed DOI

Scholz T, Vanhove MPM, Smit N, Jayasundera Z, Gelnar M. A guide to the parasites of African freshwater fishes. Brussels: Royal Belgian Institute of Natural Sciences; 2018.

Rahmouni C, Vanhove MPM, Šimková A. Seven new species of Cichlidogyrus Paperna, 1960 (Monogenea: Dactylogyridae) parasitizing the gills of Congolese cichlids from northern Lake Tanganyika. PeerJ. 2018;6:e5604. doi: 10.7717/peerj.5604. PubMed DOI PMC

Jorissen MWP, Pariselle A, Huyse T, Vreven EJ, Snoeks J, Decru E, et al. Six new dactylogyrid species (Platyhelminthes, Monogenea) from the gills of cichlids (Teleostei, Cichliformes) from the Lower Congo Basin. Parasite. 2018;25:64. doi: 10.1051/parasite/2018059. PubMed DOI PMC

Pariselle A, Euzet L. Systematic revision of dactylogyridean parasites (Monogenea) from cichlid fishes in Africa, the Levant and Madagascar. Zoosystema. 2009;31:849–898. doi: 10.5252/z2009n4a6. DOI

Vignon M, Pariselle A, Vanhove MPM. Modularity in attachment organs of African Cichlidogyrus (Platyhelminthes: Monogenea: Ancyrocephalidae) reflects phylogeny rather than host specificity or geographic distribution. Biol J Linn Soc Lond. 2011;102:694–706. doi: 10.1111/j.1095-8312.2010.01607.x. DOI

Salzburger W, Mack T, Verheyen E, Meyer A. Out of Tanganyika: genesis, explosive speciation, key-innovations and phylogeography of the haplochromine cichlid fishes. BMC Evol Biol. 2005;5:17. doi: 10.1186/1471-2148-5-17. PubMed DOI PMC

Dunz AR, Schliewen UK. Molecular phylogeny and revised classification of the haplotilapiine cichlid fishes formerly referred to as “Tilapia”. Mol Phylogenet Evol. 2013;68:64–80. doi: 10.1016/j.ympev.2013.03.015. PubMed DOI

Meyer BS, Matschiner M, Salzburger W. A tribal level phylogeny of Lake Tanganyika cichlid fishes based on a genomic multi-marker approach. Mol Phylogenet Evol. 2015;83:56–71. doi: 10.1016/j.ympev.2014.10.009. PubMed DOI PMC

Abell R, Thieme ML, Revenga C, Bryer M, Kottelat M, Bogutskaya N, et al. Freshwater ecoregions of the world: a new map of biogeographic units for freshwater biodiversity conservation. Bioscience. 2008;58:403–414. doi: 10.1641/B580507. DOI

Stiassny MLJ, Brummett RE, Harrison IJ, Monsembula R, Mamonekene V. The status and distribution of freshwater fishes in central Africa. In: Brooks EGE, Allen DJ, Darwall WRT, editors. The status and distribution of freshwater biodiversity in central Africa. Gland, Switzerland: IUCN; 2011. pp. 27–46.

Douëllou L. Monogeneans of the genus Cichlidogyrus Paperna, 1960 (Dactylogyridae: Ancyrocephalinae) from cichlid fishes of Lake Kariba (Zimbabwe) with descriptions of five new species. Syst Parasitol. 1993;25:159–186. doi: 10.1007/BF00007007. DOI

Jorissen MWP, Pariselle A, Huyse T, Vreven EJ, Snoeks J, Volckaert FAM, et al. Diversity and host specificity of monogenean gill parasites (Platyhelminthes) of cichlid fishes in the Bangweulu-Mweru ecoregion. J Helminthol. 2018;92:417–437. doi: 10.1017/S0022149X17000712. PubMed DOI

Vanhove MPM, Van Steenberge M, Dessein S, Volckaert FAM, Snoeks J, Huyse T, et al. Biogeographical implications of Zambezian Cichlidogyrus species (Platyhelminthes: Monogenea: Ancyrocephalidae) parasitizing Congolian cichlids. Zootaxa. 2013;3608:398–400. doi: 10.11646/zootaxa.3608.5.8. PubMed DOI

Price CE, Peebles HE, Bamford T. The monogenean parasites of African fishes. IV. Two new species from South African hosts. Rev Zool Bot Afr. 1969;79:117–124.

Pariselle A, Euzet L. Four new species of Cichlidogyrus (Monogenea: Ancyrocephalidae), gill parasites of Tilapia cabrae (Teleostei: Cichlidae), with discussion on relative length of haptoral sclerites. Folia Parasitol. 2003;50:195–201. doi: 10.14411/fp.2003.035. PubMed DOI

Hyman LH. The invertebrates: Platyhelminthes and Rhynchocoela, the acoelomate Bilateria. New York: McGraw-Hill; 1951.

Fannes W, Vanhove MPM, Huyse T. Redescription of Cichlidogyrus tiberianus Paperna, 1960 and C. dossoui Douëllou, 1993 (Monogenea: Ancyrocephalidae), with special reference to the male copulatory organ. Syst Parasitol. 2017;2017(94):133–144. doi: 10.1007/s11230-016-9685-1. PubMed DOI

Wägele J. Foundations of phylogenetic systematics. 2. München: Verlag Dr. Friedrich Pfeil; 2005.

Davis JI, Nixon KC. Populations, genetic variation, and the delimitation of phylogenetic species. Syst Biol. 1992;41:421–435. doi: 10.1093/sysbio/41.4.421. DOI

International Commission on Zoological Nomenclature et al. Article 50: Authors of names and nomenclatural acts. In: Ride WDL, Cogger HG, Dupuis C, Kraus O, Minelli A, Thompson FC, et al., editors. International code of zoological nomenclature. 4. London: The International Trust for Zoological Nomenclature; 1999. p. 2015.

ICZN International Commission on Zoological Nomenclature: Amendment of articles 8, 9, 10, 21 and 78 of the International Code of Zoological Nomenclature to expand and refine methods of publication. Bull Zool Nomencl. 2012;69:161–169. doi: 10.21805/bzn.v69i3.a8.161. PubMed DOI

Birgi E, Lambert A. Présence chez un Nandidae (Téléostéen), Polycentropsis abbreviata Boulenger, 1901, du genre Cichlidogyrus (Monogenea, Monopisthocotylea, Ancyrocephalidae) - Description de Cichlidogyrus nandidae n. sp. et de Cichlidogyrus euzeti n. sp. Ann Parasitol Hum Comp. 1986;61:521–528. doi: 10.1051/parasite/1986615521. DOI

Birgi E, Lambert A. A propos de Cichlidogyrus euzeti Birgi et Lambert, 1986 décrit au Cameroun chez un Nandidae, Polycentropsis abbreviata. Ann Parasitol Hum Comp. 1987;62:103. doi: 10.1051/parasite/1987621103. DOI

Vanhove MPM, Volckaert FAM, Pariselle A. Ancyrocephalidae (Monogenea) of Lake Tanganyika: I: Four new species of Cichlidogyrus from Ophthalmotilapia ventralis (Teleostei: Cichlidae), the first record of this parasite family in the basin. Zoologia. 2011;28:253–263. doi: 10.1590/S1984-46702011000200016. DOI

Pariselle A, Bilong Bilong CF, Euzet L. 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 redescription of C. thurstonae Ergens, 1981. Syst Parasitol. 2003;56:201–210. doi: 10.1023/B:SYPA.0000003807.27452.bd. PubMed DOI

Schedel FDB, Vreven E, Manda BK, Abwe E, Manda AC, Schliewen UK. Description of five new rheophilic Orthochromis species (Teleostei: Cichlidae) from the Upper Congo drainage in Zambia and the Democratic Republic of the Congo. Zootaxa. 2018;4461:301–349. doi: 10.11646/zootaxa.4464.3.1. PubMed DOI

Pariselle A, Euzet L. Cichlidogyrus Paperna, 1960 (Monogenea, Ancyrocephalidae): gill parasites from West African Cichlidae of the subgenus Coptodon Regan, 1920 (Pisces), with descriptions of six new species. Syst Parasitol. 1996;34:109–124. doi: 10.1007/BF00009685. DOI

Pariselle A, Euzet L. New species of Cichlidogyrus Paperna, 1960 (Monogenea, Ancyrocephalidae) from the gills of Sarotherodon occidentalis (Daget) (Osteichthyes, Cichlidae) in Guinea and Sierra Leone (West Africa) Syst Parasitol. 1997;38:221–230. doi: 10.1023/A:1005803202543. DOI

Van Steenberge M, Vreven E, Snoeks J. The fishes of the Upper Luapula area (Congo basin): a fauna of mixed origin. Ichthyol Explor Freshwaters. 2014;24:329–345.

Mendlová M, Šimková A. Evolution of host specificity in monogeneans parasitizing African cichlid fish. Parasit Vectors. 2014;7:69. doi: 10.1186/1756-3305-7-69. PubMed DOI PMC

Pouyaud L, Desmarais E, Deveney M, Pariselle A. Phylogenetic relationships among monogenean gill parasites (Dactylogyridea, Ancyrocephalidae) infesting tilapiine hosts (Cichlidae): systematic and evolutionary implications. Mol Phylogenet Evol. 2006;38:241–249. doi: 10.1016/j.ympev.2005.08.013. PubMed DOI

Poulin R, Krasnov BR, Mouillot D. Host specificity in phylogenetic and geographic space. Trends Parasitol. 2011;27:355–361. doi: 10.1016/j.pt.2011.05.003. PubMed DOI

Krasnov BR, Poulin R. Ecological properties of a parasite: species-specific stability and geographical variation. In: Morand S, Krasnov BR, editors. The biogeography of host-parasite interactions. New York: Oxford University Press; 2010. pp. 99–114.

Rahmouni C, Vanhove MPM, Šimková A. Underexplored diversity of gill monogeneans in cichlids from Lake Tanganyika: eight new species of Cichlidogyrus Paperna, 1960 (Monogenea: Dactylogyridae) from the northern basin of the lake, with remarks on the vagina and the heel of the male copulatory organ. Parasit Vectors. 2017;10:591. doi: 10.1186/s13071-017-2460-6. PubMed DOI PMC

Kmentová N, Gelnar M, Mendlová M, Van Steenberge M, Koblmüller S, Vanhove MPM. Reduced host-specificity in a parasite infecting non-littoral Lake Tanganyika cichlids evidenced by intraspecific morphological and genetic diversity. Sci Rep. 2016;6:39605. doi: 10.1038/srep39605. PubMed DOI PMC

Messu Mandeng FDM, Bilong Bilong CF, Pariselle A, Vanhove MPM, Bitja Nyom AR, Agnèse J-F. 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. Parasit Vectors. 2015;8:582. doi: 10.1186/s13071-015-1181-y. PubMed DOI PMC