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Redescription of Cichlidogyrus tiberianus Paperna, 1960 and C. dossoui Douëllou, 1993 (Monogenea: Ancyrocephalidae), with special reference to the male copulatory organ

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Abstract

The flatworms of the genus Cichlidogyrus Paperna, 1960 (Monogenea: Ancyrocephalidae) are gill parasites of freshwater fish, affecting predominantly the family Cichlidae. Cichlidogyrus tiberianus Paperna, 1960 and Cichlidogyrus dossoui Douëllou, 1993 are among the most widely distributed species of the genus, occurring in several African river basins and infecting many different host species, including the economically important Nile tilapia Oreochromis niloticus (Linnaeus) and redbreast tilapia Coptodon rendalli (Boulenger). Despite their wide distribution, C. tiberianus and C. dossoui have so far been studied only by light microscopy. In this paper they are redescribed on the basis of scanning electron microscopy of newly-collected material. The new material was obtained from redbreast tilapia caught in the Luapula River (D. R. Congo). The haptoral sclerites and genitalia are redescribed and illustrated in detail. Special attention is given to the complex morphology of the male copulatory organ.

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References

  • Aguirre-Fey, D., Benítez-Villa, G. E., Pérez-Ponce de León, G., & Rubio-Godoy, M. (2015). Population dynamics of Cichlidogyrus spp. and Scutogyrus sp. (Monogenea) infecting farmed tilapia in Veracruz, México. Aquaculture, 443, 11–15.

    Article  Google Scholar 

  • Bondad-Reantaso, M. G., & Arthur, J. R. (1990). The parasites of Nile tilapia (Oreochromis niloticus (L.)) in the Philippines, including an analysis of the changes in the parasite fauna of cultured tilapia from fry to marketable size. In: Hirano, R. & Hanyo, I. (Eds), Proceedings of the 2nd Asian fisheries forum. Manila: Asian Fisheries Society, pp. 729–734.

    Google Scholar 

  • Dossou, C. (1982). Parasites de poissons d’eau douce du Bénin III. Espèces nouvelles du genre Cichlidogyrus (Monogenea) parasites de Cichlidae. Bulletin de l’Institut Fondamental d’Afrique Noire, 44, 295–322.

    Google Scholar 

  • Dotta, G., Brum, A., Jeronimo, G. T., Maraschin, M., & Martins, M. L. (2015). Effect of dietary supplementation with propolis and Aloe barbadensis extracts on hematological parameters and parasitism in Nile tilapia. Revista Brasileira de Parasitologia Veterinária, 24, 66–71.

    Article  CAS  PubMed  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, 25, 159–186.

    Article  Google Scholar 

  • Ergens, R. (1981). Nine species of the genus Cichlidogyrus Paperna, 1960 (Monogenea: Ancyrocephalinae) from Egyptian fishes. Folia Parasitologica, 28, 205–214.

    Google Scholar 

  • Eschmeyer, W. N., & Fricke, R. (2015). Catalog of fishes: genera, species, references. Retrieved November 27, 2015, from http://researcharchive.calacademy.org/research/ichthyology/catalog/fishcatmain.asp.

  • Fannes, W., Vanhove, M. P. M., Huyse, T., & Paladini, G. (2015). A scanning electron microscope technique for studying the sclerites of Cichlidogyrus. Parasitology Research, 114, 2031–2034.

    Article  PubMed  Google Scholar 

  • Hagras, A. E., El-Naggar, M. M., Ogawa, K., Hussien, A. B., & El-Naggar, A. M. (2000). Effect of some ecological parameters of the monogenean gill parasites on the cichlid fish Oreochromis niloticus and Tilapia zilli from Manzala Lake and Mansouria Canal at east northern delta - Egypt. Journal of the Egyptian-German Society of Zoology (Series D, Invertebrate Zoology & Parasitology), 32, 205–221.

    Google Scholar 

  • Ibrahim, M. M. (2012). Variation in parasite infracommunies of Tilapia zillii in relation to some biotic and abiotic factors. International Journal of Zoological Research, 8, 59–70.

    Article  Google Scholar 

  • Ibrahim, M. M., & Soliman, M. F. (2011). Parasite community of wild and cultured Oreochromis niloticus from Lake Manzalah, Egypt. Journal of the Egyptian Society of Parasitology, 41, 685–697.

    PubMed  Google Scholar 

  • Jiménez-García, M. I., Vidal-Martínez, V. M., & López-Jiménez, S. (2001). Monogeneans in introduced and native cichlids in Mexico: evidence for transfer. Journal of Parasitology, 87, 907–909.

    PubMed  Google Scholar 

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

    Google Scholar 

  • Lizama, M. A. P., Takemoto, R. M., Ranzani-Paiva, M. J. T., Ayroza, L. M. S., & Pavanelli, G. C. (2007). Relação parasito-hospedeiro em peixes de pisciculturas da região de Assis, Estado de São Paulo, Brasil. 1. Oreochromis niloticus (Linnaeus, 1757). Acta Scientiarum, 29, 223–231.

    Google Scholar 

  • Lopez, N. C. (1991). Metazoan ectoparasites of some cultured fishes from Laguna Lake and vicinities. Transactions of the National Academy of Science and Technology (Philippines), 13, 499–516.

    Google Scholar 

  • López-Jiménez, S. (2001). Estudio parasitológico de los peces de aguas dulces del estado de Tabasco. Gaceta Sigolfo: Sistema de Investigación del Golfo de México, 3, 8–10.

    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, 79, 362.

    Article  Google Scholar 

  • Madanire-Moyo, G. N., Matla, M. M., Olivier, P. A. S., & Luus-Powell, W. J. (2011). Population dynamics and spatial distribution of monogeneans on the gills of Oreochromis mossambicus (Peters, 1852) from two lakes of the Limpopo River System, South Africa. Journal of Helminthology, 85, 146–152.

    Article  CAS  PubMed  Google Scholar 

  • Maneepitaksanti, W., & Nagasawa, K. (2012). Monogeneans of Cichlidogyrus Paperna, 1960 (Dactylogyridae), gill parasites on tilapias, from Okinawa Prefecture, Japan. Biogeography, 14, 111–119.

    Google Scholar 

  • Mendlová, M., Desdevises, Y., Civáňová, K., Pariselle, A., & Šimková, A. (2012). Monogeneans of West African cichlid fish: evolution and cophylogenetic interactions. PLoS ONE, 7, e37268.

    Article  PubMed  PubMed Central  Google Scholar 

  • Messu Mandeng, F. D., Bilong Bilong, C. F., Pariselle, A., Vanhove, M. P. M., Bitja Nyom, A. R., & Agnèse, J. F. (2015). A phylogeny of Cichlidogyrus spp. (Monogenea, Dactylogyridea) clarifies a host-switch between fish families and reveals an adaptive component to attachment organ morphology of this parasite genus. Parasites & Vectors, 8, 582.

    Article  Google Scholar 

  • Natividad, J. M., Bondad-Reantaso, M. G., & Arthur, J. R. (1986). Parasites of Nile tilapia (Oreochromis niloticus) in the Philippines. In J. L. Maclean, L. B. Dizon, & L. V. Hosillos (Eds), Proceedings of the 1st Asian fisheries forum. Manila: Asian Fisheries Society, pp. 255–259.

    Google Scholar 

  • N’Douba, V., Thys van den Audenaerde, D. F. E., & Pariselle, A. (1997). Description d’une espèce nouvelle de monogène ectoparasite branchial de Tilapia guineensis (Bleeker, 1862) (Cichlidae) en Côte-d’Ivoire. Journal of African Zoology, 111, 429–433.

    Google Scholar 

  • Palmer, A. R. (1996). From symmetry to asymmetry: phylogenetic patterns of asymmetry variation in animals and their evolutionary significance. Proceedings of the National Academy of Sciences USA, 93, 14279–14286.

    Article  CAS  Google Scholar 

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

    Google Scholar 

  • Paperna, I. (1964). The metazoan parasite fauna of Israel inland water fishes. Bamidgeh, Bulletin of Fish Culture in Israel, 16, 3–66.

    Google Scholar 

  • Paperna, I. (1965). Monogenetic trematodes collected from fresh water fish in southern Ghana. Bamidgeh, Bulletin of Fish Culture in Israel, 17, 107–111.

    Google Scholar 

  • Paperna, I. (1969). Monogenetic trematodes of the fish of the Volta basin and South Ghana. Bulletin de l’Institut Fondamental d’Afrique Noire, 31, 840–880.

    Google Scholar 

  • Paperna, I. (1979). Monogenea of inland water fish in Africa. Annales du Musée Royal de l’Afrique Centrale (série Zoologie), 226, 1–131.

    Google Scholar 

  • Paperna, I., & Thurston, J. P. (1969). Monogenetic trematodes collected from cichlid fish in Uganda; including the description of five new species of Cichlidogyrus. Revue de Zoologie et de Botanique Africaines, 79, 15–33.

    Google Scholar 

  • Paredes-Trujillo, A., Velázquez-Abunader, I., Torres-Irineo, E., Romero, D., & Vidal-Martínez, V. M. (2016). Geographical distribution of protozoan and metazoan parasites of farmed Nile tilapia Oreochromis niloticus (L.) (Perciformes: Cichlidae) in Yucatán, México. Parasites & Vectors, 9, 66.

    Article  Google Scholar 

  • Pariselle, A., & Euzet, L. (1994). Three new species of Cichlidogyrus Paperna, 1960 (Monogenea, Ancyrocephalidae) parasitic on Tylochromis jentinki (Steindachner, 1895) (Pisces, Cichlidae) in West Africa. Systematic Parasitology, 29, 229–234.

    Article  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. Systematic Parasitology, 30, 187–198.

    Article  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.

    Article  Google Scholar 

  • Pariselle, A., & Euzet, L. (1997). New species of Cichlidogyrus Paperna, 1960 (Monogenea, Ancyrocephalidae) from the gills of Sarotherodon occidentalis (Daget) (Osteichthyes, Cichlidae) in Guinea and Sierra Leone (West Africa). Systematic Parasitology, 38, 221–230.

    Article  Google Scholar 

  • Pariselle, A., & Euzet, L. (1998). Five new species of Cichlidogyrus (Monogenea: Ancyrocephalidae) from Tilapia brevimanus, T. buttikoferi and T. cessiana from Guinea, Ivory Coast and Sierra Leone (West Africa). Folia Parasitologica, 45, 275–282.

    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 Parasitologica, 50, 195–201.

    Article  PubMed  Google Scholar 

  • Pariselle, A., & Euzet, L. (2004). Two new species of Cichlidogyrus Paperna, 1960 (Monogenea, Ancyrocephalidae) gill parasites on Hemichromis fasciatus (Pisces, Cichlidae) in Africa, with remarks on parasite geographical distribution. Parasite, 11, 359–364.

    Article  CAS  PubMed  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.

    Article  Google Scholar 

  • Pariselle, A., Bilong Bilong, C., & Euzet, L. (2003). 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. Systematic Parasitology, 56, 201–210.

    Article  PubMed  Google Scholar 

  • Pariselle, A., Bitja Nyom, 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.

    Article  PubMed  Google Scholar 

  • Pouyaud, L., Desmarais, E., Deveney, M., & Pariselle, A. (2006). Phylogenetic relationships among monogenean gill parasites (Dactylogyridea, Ancyrocephalidae) infesting tilapiine hosts (Cichlidae): systematic and evolutionary implications. Molecular Phylogenetics and Evolution, 38, 241–249.

    Article  CAS  PubMed  Google Scholar 

  • Řehulková, E., Mendlová, M., & Šimková, A. (2013). Two new species of Cichlidogyrus (Monogenea: Dactylogyridae) parasitizing the gills of African cichlid fishes (Perciformes) from Senegal: morphometric and molecular characterization. Parasitology Research, 12, 1399–1410.

    Article  Google Scholar 

  • Roberts, R. J., & Sommerville, C. (1982). Diseases of tilapias. In: Pullin, R. S. V. & Lowe-McConnell, R. H. (Eds), The biology and culture of tilapias. ICLARM Conference Proceedings 7. Manila: International Center for Living Aquatic Resources Management, pp. 247–263.

  • Roche, D. G., Leung, B., Mendoza Franco, E. F., & Torchin, M. E. (2010). Higher parasite richness, abundance and impact in native versus introduced cichlid fishes. International Journal for Parasitology, 40, 1525–1530.

    Article  PubMed  Google Scholar 

  • Rohlf, F. J. (2013). tpsDig version 2.17. Department of Ecology and Evolution, State University of New York at Stony Brook, New York.

  • Salgado-Maldonado, G., & Rubio-Godoy, M. (2014). Helmintos parásitos de peces de agua dulce introducidos. In R. E. Mendoza Alfaro & P. Koleff Osorio (Eds), Especies acuáticas invasoras en México. Mexico: Comisión Nacional para el Conocimiento y Uso de la Biodiversidad, pp. 269–285.

    Google Scholar 

  • Schilthuizen, M. (2013). Something gone awry: unsolved mysteries in the evolution of asymmetric animal genitalia. Animal Biology, 63, 1–20.

    Article  Google Scholar 

  • Shaharom-Harrison, F. (1987). The effect of hydrocortisone on Cichlidogyrus infection on Tilapia under controlled conditions. Tropical Biomedicine, 4, 196–198.

    Google Scholar 

  • Šimková, A., Ondračková, M., Gelnar, M., & Morand, S. (2002). Morphology and coexistence of congeneric ectoparasite species: reinforcement of reproductive isolation? Biological Journal of the Linnean Society, 76, 125–135.

    Google Scholar 

  • Soliman, M. F. M., & Ibrahim, M. M. (2011). Monogenean community structure of Oreochromis niloticus in relation to heavy metal pollution and host reproductive cycle. Journal of the Egyptian Society of Parasitology, 42, 11–24.

    Article  Google Scholar 

  • Thurston, J. P. (1970). The incidence of Monogenea and parasitic Crustacea on the gills of fish in Uganda. Revue de Zoologie et de Botanique Africaines, 82, 111–130.

    Google Scholar 

  • Vanhove, M. P. M., Pariselle, A., Van Steenberge, M., Raeymaekers, J. A. M., Hablützel, P. I., Gillardin, C., et al. (2015). Hidden biodiversity in an ancient lake: phylogenetic congruence between Lake Tanganyika tropheine cichlids and their monogenean flatworm parasites. Scientific Reports, 5, 13669.

    Article  PubMed  PubMed Central  Google Scholar 

  • Vanhove, M. P. M., Van Steenberge, M., Dessein, S., Volckaert, F. A. M., Snoeks, J., Huyse, T., et al. (2013). Biogeographical implications of Zambezian Cichlidogyrus species (Platyhelminthes: Monogenea: Ancyrocephalidae) parasitizing Congolian cichlids. Zootaxa, 3608, 398–400.

    Article  PubMed  Google Scholar 

  • Vanhove, M. P. M., Volckaert, F. A. M., & Pariselle, A. (2011). 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, 28, 253–263.

    Article  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.

    Article  Google Scholar 

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Acknowledgements

The authors wish to thank A. Reygel for executing the drawings, E. Harris, D. Gibson (Natural History Museum, London) and A. Ghoneim (Damietta University, Egypt) for help in obtaining literature, A. Pariselle (Institut de Recherche pour le Développement, France/Cameroon), S. Rothman (Tel Aviv University, Israel) and M. Jorissen (RMCA/Hasselt University) for discussions on Cichlidogyrus taxonomy, E. Vreven (RMCA/KU Leuven), A. Chocha Manda, E. Abwe, B. Katemo Manda, G. Kapepula Kasembele, M. Kasongo Ilunga Kayaba, C. Kalombo Kabalika and C. Mukweze Mulelenu (Université de Lubumbashi, D.R. Congo) for their contributions to this research, and C. Allard, M. Parrent, J. Snoeks and D. Van den Spiegel for assistance with RMCA collections. Moise Katumbi Chapwe, the last governor of the ex-province of Katanga, is cordially thanked for his kind hospitality and support. Two anonymous reviewers provided helpful comments and suggestions.

Funding

The authors wish to thank the Belgian Federal Science Policy Office (BRAIN-be Pioneer Project BR/132/PI/TILAPIA) for financial support. M.P.M.V. is partly supported by Czech Science Foundation project no. P505/12/G112 (ECIP). The fieldwork was partly financed by a travel grant from the Research Foundation - Flanders (FWO-Vlaanderen) to MPMV, by the South Initiative Renforcement des capacités locales pour une meilleure évaluation biologique des impacts miniers au Katanga (RD Congo) sur les poissons et leurs milieux aquatiques (ZRDC2014MP084) of the University Development Cooperation of the Flemish Interuniversity Council (VLIR-UOS), and by the Mbisa Congo project, a framework agreement project of the RMCA and the Belgian Development Cooperation.

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Correspondence to Wouter Fannes.

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All applicable institutional, national and international guidelines for the care and use of animals were followed. Sampling was carried out under attestation de recherche no. 863/2014 from the Faculté des Sciences Agronomiques of the Université de Lubumbashi.

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Fannes, W., Vanhove, M.P.M. & 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 94, 133–144 (2017). https://doi.org/10.1007/s11230-016-9685-1

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