Systematic Parasitology

, Volume 93, Issue 7, pp 679–700 | Cite as

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

  • Petra Zahradníčková
  • Maxwell Barson
  • Wilmien J. Luus-Powell
  • Iva Přikrylová
Article

Abstract

New findings on Gyrodactylus spp. parasitising African cichlids in southern Africa are presented, comprising data from Zimbabwe and South Africa. Morphometry of opisthaptoral hard parts in combination with nuclear ribosomal DNA sequences confirmed the presence of six species of Gyrodactylus von Nordmann, 1832. Three new species are described from fishes in Zimbabwe: Gyrodactylus chitandiri n. sp. from the gill arches of Coptodon rendalli (Boulenger) and Pseudocrenilabrus philander (Weber); Gyrodactylus occupatus n. sp. from the fins of Oreochromis niloticus (L.), Pharyngochromis acuticeps (Steindachner) and P. philander; and Gyrodactylus parisellei n. sp. from the fins of O. niloticus, P. philander and Tilapia sp. Gyrodactylus nyanzae Paperna, 1973 was also identified from the gills of O. niloticus and C. rendalli collected from two localities in Zimbabwe; these findings represent new host and locality records for this parasite. Gyrodactylus sturmbaueri Vanhove, Snoeks, Volckaert & Huyse, 2011 was identified from P. philander collected in South Africa and Zimbabwe thereby providing new host and locality records for this parasite. Finally, Gyrodactylus yacatli García-Vásquez, Hansen, Christison, Bron & Shinn, 2011 was collected from the fins of O. niloticus and P. philander studied in Zimbabwe; this represents the first record of this species from the continent of Africa. Notably, this study improves upon the knowledge of Gyrodactylus spp. parasitising cichlids from these southern African regions. All species studied were recorded from at least two different cichlid host species indicating trend for a wide range of Gyrodactylus hosts in Africa. Accordingly, this supports the idea of intensive host switching in the course of their evolution.

References

  1. Bakke, T. A., Cable, J., & Harris, P. D. (2007). The biology of gyrodactylid monogeneans: The “Russian-doll killers”. Advances in Parasitology, 64, 161–376.CrossRefPubMedGoogle Scholar
  2. Barson, M., Mulonga, A., & Nhiwatiwa, T. (2008). Investigation of a parasitic outbreak of Lernaea cyprinacea Linnaeus (Crustacea: Copepoda) in fish from Zimbabwe. African Zoology, 43, 175–183.CrossRefGoogle Scholar
  3. Boeger, W. A., Kritsky, D. C., & Pie, M. R. (2003). Context of diversification of the viviparous Gyrodactylidae (Platyhelminthes, Monogenoidea). Zoologica Scripta, 32, 437–448.CrossRefGoogle Scholar
  4. Bukinga, F. M., Vanhove, M. P. M., Van Steenberge, M., & Pariselle, A. (2012). Ancyrocephalidae (Monogenea) of Lake Tangynyika: III: Cichlidogyrus infecting the world´s biggest cichlid and the non-endemic tribea Haplochromi, Oreochromini and Tylochromini (Teleostei, Cichlidae). Parasitology Research, 111, 2049–2061.CrossRefGoogle Scholar
  5. Cable, J., Scott, E. C. G., Tinsley, R. C., & Harris, P. D. (2002). Behavior favoring transmission in the viviparous monogenean Gyrodactylus turnbulli. Journal of Parasitology, 88, 183–184.CrossRefPubMedGoogle Scholar
  6. Cambray, J., & Swart, E. (2007). Oreochromis mossambicus In: IUCN 2007. 2007 IUCN Red List of Threatened Species. Online at: http://www.iucnredlist.org. Accessed 5 August 2015.
  7. Capella-Gutierrez, S., Silla-Martinez, J. M., & Gabaldon, T. (2009). trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics, 25, 1972–1973.CrossRefPubMedPubMedCentralGoogle Scholar
  8. Christison, K. W., Shinn, A. P., & Van As, J. G. (2005). Gyrodactylus thlapi n. sp. (Monogenea) from Pseudocrenilabrus philander philander (Weber) (Cichlidae) in the Okavango Delta. Botswana. Systematic Parasitology, 60, 165–173.CrossRefPubMedGoogle Scholar
  9. Cone, D. K., Arthur, R., & Bondad-Reantaso, M. G. (1995). Description of two new species of Gyrodactylus von Nordmann, 1832 (Monogenea) from cultured Nile tilapia, Tilapia nilotica (Cichlidae), in the Philippines. Journal of the Helminthological Society of Washington, 62, 6–9.Google Scholar
  10. Dunz, A. R., & Schliewen, U. K. (2013). Molecular phylogeny and revised classification of the haplotilapiine cichlid fishes formerly referred to as “Tilapia”. Molecular Phylogenetics and Evolution, 68, 64–80.CrossRefPubMedGoogle Scholar
  11. Duponchelle, F., Paradis, E., Ribbink, A. J., & Turner, G. F. (2008). Parallel life history evolution in mouthbrooding cichlids from the African Great Lakes. Proceedings of the National Academy of Sciences of the United States of America, 105, 15475–15480.CrossRefPubMedPubMedCentralGoogle Scholar
  12. El-Abbassy, S. (2005). Studies of the anatomical features, histochemical components and pathological impacts of gyrodactylid monogenean parasites infesting the catfish Clarias gariepinus inhabiting Nile Delta Waters. PhD Thesis, Faculty of Sciences, Mansoura University, Mansoura, Egypt.Google Scholar
  13. Ellender, B. R., & Weyl, O. L. F. (2014). A review of current knowledge, risk and ecological impacts associated with non-native freshwater fish introductions in South Africa. Aquatic Invasions, 9, 117–132.CrossRefGoogle Scholar
  14. El-Naggar, A. M. (2007). Mode of attachment and local histopathological impacts of the viviparous monogeneans Gyrodactylus rysavyi and M. congolensis from the skin and fins of the Nile catfish Clarias gariepinus. Egyptian Journal of Zoology, 49, 293–308.Google Scholar
  15. El-Naggar, A. M., & El-Abbassy, S. (2003). Anatomical observations on the viviparous monogenean Gyrodactylus rysavyi Ergens, 1973 from the Nile catfish Clarias gariepinus in Egypt. Egyptian Journal of Zoology, 40, 225–249.Google Scholar
  16. El-Naggar, A. M., & El-Tantawy, S. A. (2003). The dynamics of gill monogenean communities on cichlid fish hosts inhabiting Damietta Branch of the River Nile: long-term changes in species richness and community structure. Journal of the Egyptian German Society of Zoology, 41D, 187–220.Google Scholar
  17. Ergens, R. (1973). Two new species of Gyrodactylus from Clarias lazera. Revue de Zoologie et de Botanique africaines, 87, 77–80.Google Scholar
  18. Froese, R., & Pauly, D. (Eds) (2015). FishBase. World Wide Web electronic publication, version 04/2015. http://www.fishbase.org. Accessed 7 June 2015.
  19. García-Vásquez, A., Hansen, H., Christison, K. W., Bron, J. E., & Shinn, A. P. (2011). Description of three new species of Gyrodactylus von Nordmann, 1832 (Monogenea) parasitising Oreochromis niloticus niloticus (L.) and O. mossambicus (Peters) (Cichlidae). Acta Parasitologica, 52, 20–33.Google Scholar
  20. García-Vásquez, A., Hansen, H., Christison, K. W., Rubio-Godoy, M., Bron, J. E., & Shinn, A. P. (2010). Gyrodactylids (Gyrodactylidae, Monogenea) infecting Oreochromis niloticus niloticus (L.) and O. mossambicus (Peters) (Cichlidae): A pan-global survey. Acta Parasitologica, 55, 215–229.CrossRefGoogle Scholar
  21. García-Vásquez, A., Hansen, H., & Shinn, A. P. (2007). A revised description of Gyrodactylus cichlidarum Paperna, 1968 (Gyrodactylidae) from the Nile tilapia, Oreochromis niloticus niloticus (Cichlidae), and its synonymy with G. niloticus Cone, Arthur et Bondad-Reantaso, 1995. Folia Parasitologica, 54, 129–140.CrossRefPubMedGoogle Scholar
  22. Genner, M. J., Seehausen, O., Lunt, D. H., Joyce, D. A., Shaw, P. W., Carvalho, G. R., & Turner, G. F. (2007). Age of cichlids: New dates for ancient lake fish radiations. Molecular Biology and Evolution, 24, 1269–1282.CrossRefPubMedGoogle Scholar
  23. Gilmore, S. R., Cone, D. K., Lowe, G., King, S. K., Jones, S. R. M., & Abbott, C. L. (2012). Molecular phylogeny of Gyrodactylus (Monogenea) parasitizing fishes in fresh water, estuarine, and marine habitats in Canada. Canadian Journal of Zoology, 90, 776–786.CrossRefGoogle Scholar
  24. Glez-Peña, D., Gómez-Blanco, D., Reboiro-Jato, M., Fdez-Riverola, F., & Posada, D. (2010). ALTER: program-oriented conversion of DNA and protein alignments. Nucleic Acids Research, 38, W14–W18.CrossRefPubMedPubMedCentralGoogle Scholar
  25. Guindon, S., & Gascuel, O. (2003). A simple, fast and accurate method to estimate large phylogenies by maximum-likelihood. Systematic Biology, 52, 696–704.CrossRefPubMedGoogle Scholar
  26. Hammer, Ø., Harper, D. A. T., & Ryan, P. D. (2001). PAST: Paleontological Statistics Software Package for Education and Data Analysis. Palaeontological Electronic, 4.Google Scholar
  27. Harris, P. D., Shinn, A. P., Cable, J., & Bakke, T. A. (2004). Nominal species of the genus Gyrodactylus von Nordmann 1832 (Monogenea:Gyrodactylidae), with a list of principal host species. Systematic Parasitology, 59, 1–27.CrossRefPubMedGoogle Scholar
  28. Hecht, T., & Endemann, F. (1998). The impact of parasites, infections and diseases on the development of aquaculture in sub-Saharan Africa. Journal of Applied Ichthyology-Zeitschrift Fur Angewandte Ichthyologie, 14, 213–221.CrossRefGoogle Scholar
  29. Huelsenbeck, J. P., & Ronquist, F. (2001). MrBayes: Bayesian inference of phylogenetic trees. Bioinformatics, 17, 754–755.CrossRefPubMedGoogle Scholar
  30. Hurvich, C. M., & Tsai, C. L. (1989). Regression and time series model selection in small samples. Biometrika, 76, 297–307.CrossRefGoogle Scholar
  31. Joyce, D. A., Lunt, D. H., Genner, M. J., Turner, G. F., Bills, R., & Seehausen, O. (2011). Repeated colonization and hybridization in Lake Malawi cichlids. Current Biology, 21, 526–526.CrossRefGoogle Scholar
  32. Kazembe, J., Marshall, B., Moelants, T., & Tweddle, D. (2010). Tilapia sparrmanii. The IUCN Red List of Threatened Species. http://www.iucnredlist.org. Accessed 03 Feb 2015.
  33. Keenleyside, M. H. (1991). Cichlid fishes: behaviour, ecology and evolution. London: Chapman and Hall.Google Scholar
  34. Koblmüller, S., Schliewen, U. K., Duftner, N., Sefc, K. M., Katongo, C., & Sturmbauer, C. (2008). Age and spread of the haplochromine cichlid fishes in Africa. Molecular Phylogenetics and Evolution, 49, 153–169.CrossRefPubMedGoogle Scholar
  35. Malmberg, G. (1970). The excretory systems and marginal hooks as basis for the systematics of Gyrodactylus (Trematoda, Monogenea). Arkiv för Zoologi, 2, 1–235.Google Scholar
  36. Matějusová, I., Gelnar, M., McBeath, A. J. A., Collins, C. M., & Cunningham, C. O. (2001). Molecular markers for gyrodactylids (Gyrodactylidae : Monogenea) from five fish families (Teleostei). International Journal for Parasitology, 31, 738–745.CrossRefPubMedGoogle Scholar
  37. Mittermeier, R. A., Turner, W. R., Larsen, F., Brooks, T. M., & Gascon, C. (2011). Biodiversity Hotspots: Distribution and Protection of Conservation Priority Areas. In: Zachos, F.E. & Habel, J. C. (Eds.), Biodiversity Hotspots (pp. 3–22). Berlin Heidelberg: Springer.Google Scholar
  38. Murray, A. M. (2001). The oldest fossil cichlids (Teleostei: Perciformes): indication of a 45 million-year-old species flock. Proceedings of the Royal Society of London B: Biological Sciences, 268, 679–684.CrossRefGoogle Scholar
  39. Nack, J., Bilong, B. C., & Euzet, L. (2005). Monogenean parasites from Clariidae (Teleostei, siluriformes) in Cameroon: I. Description of two new species of Gyrodactylus from the Nyong Bassin. Parasite, 12, 213–220.CrossRefPubMedGoogle Scholar
  40. Paetow, L., Cone, D. K., Huyse, T., McLaughlin, J. D., & Marcogliese, D. J. (2009). Morphology and molecular taxonomy of Gyrodactylus jennyae n. sp (Monogenea) from tadpoles of captive Rana catesbeiana Shaw (Anura), with a review of the species of Gyrodactylus Nordmann, 1832 parasitising amphibians. Systematic Parasitology, 73, 219–227.CrossRefPubMedGoogle Scholar
  41. Paperna, I. (1968). Monogenetic trematodes collected from fresh water fish in Ghana. Second report. Bamidgeh, 20, 88–99.Google Scholar
  42. Paperna, I. (1973). New species of Monogenea (Vermes) from African freshwater fish. A preliminary report. Revue de Zoologie et de Botanique Africaines, 87, 505–518.Google Scholar
  43. Paperna, I. (1979). Monogenea of inland water fish in Africa. Annales des Museé Royal de l’Afrique Centrale, Science Zoologique, 226, (Ser. 8), 1–131.Google Scholar
  44. Paperna, I. (1996). Parasites, infections and diseases of fishes in Africa. An update. CIFA Technical Paper 31, Food and Agriculture Organization, Rome.Google Scholar
  45. Pariselle, A., Van Steenberge, M., Snoeaks, J., Volckaert, F. A. M., Huyse, T., & Vanhove, M. P. M. (2015). Ancyrocephalidae (Monogenea) of Lake Tanganyika: Does the Cichlidogyrus parasite fauna of Interochromis loocki (Teleostei, Cichlidae) reflect its host´s phylogenetic affinities? Contribution to Zoology, 84, 25–38.Google Scholar
  46. Posada, D. (2003). Using Modeltest and PAUP* to select a model of nucleotide substitution. In: Baxevanis, A. D., Davison, D. B., Page, R. D. M., Petsko, G. A., Stein, L. D. & Stormo, G. D. (Eds.), Current Protocols in Bioinformatics (pp. 6.5.1–6.5.14). New York: Wiley.Google Scholar
  47. Price, C., & Gery, J. (1968). Parasites de poissons du Gabon. Généralités sur les trematodes monogénétiques, et description de six nouvelles espéces parasites du genre Barbus. Biologia Gabonica, 4, 83–103.Google Scholar
  48. Přikrylová, I., Blažek, R., & Gelnar, M. (2012a). Gyrodactylus malalai sp. nov. (Monogenea, Gyrodactylidae) from Nile tilapia, Oreochromis niloticus (L.) and Redbelly tilapia, Tilapia zillii (Gervais)(Teleostei, Cichlidae) in the Lake Turkana. Kenya. Acta Parasitologica, 57, 122–130.PubMedGoogle Scholar
  49. Přikrylová, I., Blažek, R., & Vanhove, M. P. M. (2012b). An overview of the Gyrodactylus (Monogenea: Gyrodactylidae) species parasitizing African catfishes, and their morphological and molecular diversity. Parasitology Research, 110(3), 1185–1200.CrossRefPubMedGoogle Scholar
  50. Přikrylová, I., Matějusová, I., Jarkovský, J., & Gelnar, M. (2008). Morphometric comparison of three members of the Gyrodactylus nemachili-like species group (Monogenea: Gyrodactylidae) on Barbatula barbatula L. in the Czech Republic, with a reinstatement of G. papernai Ergens & Bychowsky, 1967. Systematic Parasitology, 69, 33–44.CrossRefPubMedGoogle Scholar
  51. Přikrylová, I., Matějusová, I., Musilová, N., & Gelnar, M. (2009). Gyrodactylus species (Monogenea: Gyrodactylidae) on the cichlid fishes of Senegal, with the description of Gyrodactylus ergensi n. sp from Mango tilapia, Sarotherodon galilaeus L. (Teleostei: Cichilidae). Parasitology Research, 106, 1–6.CrossRefPubMedGoogle Scholar
  52. Přikrylová, I., Vanhove, M. P. M., Janssens, S. B., Billeter, P. A., & Huyse, T. (2013). Tiny worms from a mighty continent: High diversity and new phylogenetic lineages of African monogeneans. Molecular Phylogenetics and Evolution, 67, 43–52.CrossRefPubMedGoogle Scholar
  53. Prudhoe, S., & Hussey, C. G. (1977). Some parasitic worms in freshwater fishes and fish-predators from the Transvaal, South Africa. African Zoology, 12, 113–147.CrossRefGoogle Scholar
  54. Rambaut, A. (2008). Molecular evolution, phylogenetics and epidemiology, FigTree v. 1.3. 1.Google Scholar
  55. Rokicka, M., Lumme, J., & Zietara, M. S. (2007). Identification of Gyrodactylus ectoparasites in Polish salmonid farms by PCR-RFLP of the nuclear ITS segment of ribosomal DNA (Monogenea, Gyrodactylidae). Acta Parasitologica, 52, 185–195.CrossRefGoogle Scholar
  56. Ronquist, F., & Huelsenbeck, J. P. (2003). MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics, 19, 1572–1574.CrossRefPubMedGoogle Scholar
  57. 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 Evolutionary Biology, 5, 17.CrossRefPubMedPubMedCentralGoogle Scholar
  58. Schwarzer, J., Misof, B., Tautz, D., & Schliewen, U. K. (2009). The root of the East African cichlid radiations. Bmc Evolutionary Biology, 9, 181.CrossRefGoogle Scholar
  59. Shinn, A. P., Paladini, G., Rubio-Godoy, M., Domingues, M. V., Whittington, I. D., Bron, J. E. (2011). MonoDb. A web-host for Monogenea. World Wide Web electronic publication. http://www.monodb.org. Accessed 2 September 2015.
  60. Skelton, P. H. (2001). A complete guide to the freshwater fishes of Southern Africa (New ed.). Cape Town: Struik.Google Scholar
  61. Snoeks, J. (2000). How well known is the ichthyodiversity of the large East African lakes? Advances in Ecological Research, 31, 17–38.CrossRefGoogle Scholar
  62. Sturmbauer, C. (1998). Explosive speciation in cichlid fishes of the African Great Lakes: a dynamic model of adaptive radiation. Journal of Fish Biology, 53, 18–36.CrossRefGoogle Scholar
  63. Sturmbauer, C., Husemann, M., & Danley, P. D. (2011). Explosive speciation and adaptive radiation of East African cichlid fishes Biodiversity Hotspots. Springer, p 333–362.Google Scholar
  64. Tamura, K., Stecher, G., Peterson, D., Filipski, A., & Kumar, S. (2013). MEGA6: Molecular Evolutionary Genetics Analysis Version 6.0. Molecular Biology and Evolution, 30, 2725–2729.CrossRefPubMedPubMedCentralGoogle Scholar
  65. Thompson, J. D., Higgins, D. G., & Gibson, T. J. (1994). Clustal-W - Improving the Sensitivity of Progressive Multiple Sequence Alignment through Sequence Weighting, Position-Specific Gap Penalties and Weight Matrix Choice. Nucleic Acids Research, 22, 4673–4680.CrossRefPubMedPubMedCentralGoogle Scholar
  66. Turner, G. F., Seehausen, O., Knight, M. E., Allender, C. J., & Robinson, R. L. (2001). How many species of cichlid fishes are there in African lakes? Molecular Ecology, 10, 793–806.CrossRefPubMedGoogle Scholar
  67. Van As, J. G., & Basson, L. (1984). Checklist of freshwater fish parasites from southern Africa. South African Journla of Wildlife Research, 14, 49–61.Google Scholar
  68. Vanhove, M. P. M., Snoeks, J., Volckaert, F. A. M., & Huyse, T. (2011). 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, 364–380.CrossRefPubMedGoogle Scholar
  69. Ziętara, M. S., & Lumme, J. (2002). Speciation by host switch and adaptive radiation in a fish parasite genus Gyrodactylus (Monogenea, Gyrodactylidae). Evolution, 56, 2445–2458.CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2016

Authors and Affiliations

  • Petra Zahradníčková
    • 1
  • Maxwell Barson
    • 2
  • Wilmien J. Luus-Powell
    • 3
  • Iva Přikrylová
    • 1
    • 3
    • 4
  1. 1.Department of Botany and Zoology, Faculty of ScienceMasaryk UniversityBrnoCzech Republic
  2. 2.Department of Biological SciencesUniversity of ZimbabweHarareZimbabwe
  3. 3.Department of BiodiversityUniversity of LimpopoSovengaSouth Africa
  4. 4.Water Research Group, School of for Environmental Sciences and DevelopmentNorth West UniversityPotchefstroomSouth Africa

Personalised recommendations