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First description of monogenean parasites in Lake Tanganyika: the cichlid Simochromis diagramma (Teleostei, Cichlidae) harbours a high diversity of Gyrodactylus species (Platyhelminthes, Monogenea)

Published online by Cambridge University Press:  15 October 2010

MAARTEN P. M. VANHOVE ,
JOS SNOEKS ,
FILIP A. M. VOLCKAERT  and
TINE HUYSE
MAARTEN P. M. VANHOVE*
Affiliation:
Laboratory of Animal Diversity and Systematics, Katholieke Universiteit Leuven, Deberiotstraat 32, B-3000 Leuven, Belgium Department of African Zoology, Royal Museum for Central Africa, Leuvensesteenweg 13, B-3080 Tervuren, Belgium
JOS SNOEKS
Affiliation:
Laboratory of Animal Diversity and Systematics, Katholieke Universiteit Leuven, Deberiotstraat 32, B-3000 Leuven, Belgium Department of African Zoology, Royal Museum for Central Africa, Leuvensesteenweg 13, B-3080 Tervuren, Belgium
FILIP A. M. VOLCKAERT
Affiliation:
Laboratory of Animal Diversity and Systematics, Katholieke Universiteit Leuven, Deberiotstraat 32, B-3000 Leuven, Belgium
TINE HUYSE
Affiliation:
Laboratory of Animal Diversity and Systematics, Katholieke Universiteit Leuven, Deberiotstraat 32, B-3000 Leuven, Belgium
*
*Corresponding author: Laboratory of Animal Diversity and Systematics, Katholieke Universiteit Leuven, Charles Deberiotstraat 32, B-3000 Leuven, Belgium. Tel: +32 16 32 39 18. Fax: +32 16 32 45 75. E-mail: maarten.vanhove@bio.kuleuven.be
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Summary

Lake Tanganyika harbours the most diverse endemic cichlid fish assemblage of Africa, but its monogenean fish parasites have not been investigated. Here we report, for the first time, on the Gyrodactylus parasites in this hotspot of fish biodiversity. Haptor morphometrics and nuclear ribosomal DNA sequences revealed 3 new species on Zambian Simochromis diagramma: Gyrodactylus sturmbaueri n. sp., G. thysi n. sp. and G. zimbae n. sp. Their distinct morphology and strong genetic differentiation suggest that they belong to distant lineages within the genus Gyrodactylus, and phylogenetic reconstructions suggest affinities with other genera of gyrodactylids. Additional U-shaped haptoral plates in G. thysi n. sp. and a second large spine-like structure in the male copulatory organ of G. zimbae seem to represent new features for the genus. Such large diversity on a single host species can probably be explained by host-switching events during the course of evolution, in agreement with the generally accepted concept that ecological transfer is an important aspect of gyrodactylid speciation. Additional parasitological surveys on other host species, covering a broader phylogenetic and geographical range, should clarify the evolutionary history of Gyrodactylidae on cichlids in the African Great Lake and other parts of Africa.

Keywords

AfricacichlidsGyrodactylidaeLake TanganyikaMonogeneaSimochromis diagrammaspeciationspecies descriptionspecies flockTropheini
Type
Research Article
Information
Parasitology , Volume 138 , Issue 3 , March 2011 , pp. 364 - 380
Copyright
Copyright © Cambridge University Press 2010

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References

REFERENCES

Bakke, T. A., Cable, J. and Harris, P. D.. (2007). The biology of gyrodactylid monogeneans: the “Russian-doll killers”. Advances in Parasitology 64, 161–376, 459–460.CrossRefGoogle Scholar
Bakke, T. A., Harris, P. D. and Cable, J. (2002). Host specificity dynamics: observations on gyrodactylid monogeneans. International Journal for Parasitology 32, 281–308.CrossRefGoogle ScholarPubMed
Barson, M., Přikrylová, I., Vanhove, M. P. M. and Huyse, T. (2010). Parasite hybridization in African Macrogyrodactylus spp. (Monogenea, Platyhelminthes) signals historical host distribution. Parasitology 137, 1585–1595.CrossRefGoogle ScholarPubMed
Blais, J., Rico, C., van Oosterhout, C., Cable, J., Turner, G. F. and Bernatchez, L. (2007). MHC adaptive divergence between closely related and sympatric African cichlids. PLoS ONE 2(8), e734. doi: 10.1371/journal.pone.0000734CrossRefGoogle ScholarPubMed
Boeger, W. A., Kritsky, D. C. and Pie, M. R. (2003). Context of diversification of the viviparous Gyrodactylidae (Platyhelminthes, Monogenoidea). Zoologica Scripta 32, 437–448.CrossRefGoogle ScholarPubMed
Brichard, P. (1978). Fishes of Lake Tanganyika. TFH Publications, Neptune City, NJ, USA.Google Scholar
Bruno, D. W., Collins, C. M., Cunningham, C. O. and MacKenzie, K. (2001). Gyrodactyloides bychowskii (Monogenea: Gyrodactylidae) from sea-caged Atlantic salmon Salmo salar in Scotland: occurrence and ribosomal RNA sequence analysis. Diseases of Aquatic Organisms 45, 191–196.CrossRefGoogle ScholarPubMed
Cable, J., Harris, P. D., Tinsley, R. C. and Lazarus, C. M. (1999). Phylogenetic analysis of Gyrodactylus spp. (Platyhelminthes: Monogenea) using rDNA sequences. Canadian Journal of Zoology 77, 1439–1449.CrossRefGoogle Scholar
Cable, J., Scott, E. C. G., Tinsley, R. C. and Harris, P. D. (2002). Behavior favoring transmission in the viviparous Monogenean Gyrodactylus turnbulli. Journal of Parasitology 88, 183–184.CrossRefGoogle ScholarPubMed
Calendini, F. and Martin, J. F. (2005). PaupUp v1.0.3.1. A Free Graphical Frontend for Paup* Dos Software. [WWW document]. URL http://www.agromontpellier.fr/sppe/Recherche/JFM/Paupllp/Google Scholar
Capella-Gutiérrez, S., Silla-Martínez, J. M. and Gabaldón, T. (2009). trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics 25, 1972–1973.CrossRefGoogle ScholarPubMed
Christison, K. W., Shinn, A. P. and 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.CrossRefGoogle Scholar
Cohen, A. S., Lezzar, K. E., Tiercelin, J. J. and Soreghan, M. (1997). New palaeogeographic and lake-level reconstructions of Lake Tanganyika: implications for tectonic, climatic and biological evolution in a rift lake. Basin Research 9, 107–132.CrossRefGoogle Scholar
Cone, D. K., Arthur, J. R. and Bondad-Reantaso, M. G. (1995). Description of 2 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
Coulter, G. W. (1991 a). Composition of the flora and fauna. In Lake Tanganyika and its Life (ed. Coulter, G. W.), pp. 200–274. Oxford University Press, Oxford, UK.CrossRefGoogle Scholar
Coulter, G. W. (1991 b). Zoogeography, affinities and evolution, with special regard to the fish. In Lake Tanganyika and its Life (ed. Coulter, G. W.), pp. 275–305. Oxford University Press, Oxford, UK.CrossRefGoogle Scholar
Eschmeyer, W. N. and Fricke, R. (eds.) (2009). Catalog of Fishes electronic version, http://research.calacademy.org/ichthyology/catalog/fishcatmain.asp, version 09/2009.Google Scholar
Edgar, R. C. (2004). MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research 32, 1792–1797.CrossRefGoogle ScholarPubMed
Felsenstein, J. (2005). PHYLIP (Phylogeny Inference Package) Version 3.6. Distributed by the author. Department of Genome Sciences, University of Washington, Seattle, USA.Google Scholar
Galis, F. and Metz, J. A. J. (1998). Why are there so many cichlid species? Trends in Ecology and Evolution 13, 1–2.CrossRefGoogle ScholarPubMed
García-Vásquez, A., Hansen, H. and 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.CrossRefGoogle Scholar
Geets, A., Appleby, C. and Ollevier, F. (1999). Host-dependent and seasonal variation in opisthaptoral hard parts of Gyrodactylus cf. arcuatus from three Pomatoschistus spp. and G. arcuatus from Gasterosteus aculeatus: a multivariate approach. Parasitology 119, 27–40.CrossRefGoogle Scholar
Gelman, A. and Rubin, D. B. (1992). Inference from iterative simulation using multiple sequences. Statistical Science 7, 457–472.CrossRefGoogle Scholar
Glez-Peña, D., Gómez-Blanco, D., Reboiro-Jato, M., Fdez-Riverola, F. and Posada, D. (2010). ALTER: program-oriented format conversion of DNA and protein alignments. Nucleic Acids Research. Web Server issue, 1–5. doi: 10.1093/nar/gkq321.CrossRefGoogle ScholarPubMed
Gregory, R. D. (1990). Parasites and host geographic range as illustrated by waterfowl. Functional Ecology 4, 645–654.CrossRefGoogle Scholar
Greenwood, P. H. (1983). The zoogeography of African freshwater fishes: bioaccountancy or biogeography? In Evolution, Time and Space: The Emergence of the Biosphere Vol. 23 (ed. Sims, R. W., Price, J. H. and Whalley, P. E. S.), pp. 179–199. Academic Press, London, UK.Google Scholar
Guindon, S. and Gascuel, O. (2003). A simple, fast and accurate method to estimate large phylogenies by maximum-likelihood. Systematic Biology 52, 696–704.CrossRefGoogle ScholarPubMed
Harris, P. D. (1993). Interactions between reproduction and population biology in Gyrodactylid monogeneans – a review. Bulletin Français de la Pêche et de la Pisciculture 328, 47–65.CrossRefGoogle Scholar
Harris, P. D. and Cable, J. (2000). Gyrodactylus poeciliae n. sp. and G. milleri n. sp. (Monogenea: Gyrodactylidae) from Poecilia caucana (Steindachner) in Venezuela. Systematic Parasitology 47, 79–85.CrossRefGoogle Scholar
Harris, P. D., Shinn, A. P., Cable, J. and 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.CrossRefGoogle ScholarPubMed
Hayward, C. J., Iwashita, M., Ogawa, K. and Ernst, I. (2001). Global spread of the eel parasite Gyrodactylus anguillae (Monogenea). Biological Invasions 3, 417–424.CrossRefGoogle Scholar
Hillis, D. M., Mable, B. K., and Moritz, C. (1996). An overview of applications of molecular systematics. In Molecular Systematics, 2nd Edn (ed. Hillis, D. M., Moritz, C. and Mable, B. K.), pp. 515–534. Sinauer, Massachusetts, USA.Google Scholar
Huelsenbeck, J. P. and Ronquist, F. (2001). MrBayes: Bayesian inference of phylogenetic trees. Bioinformatics 17, 754–755.CrossRefGoogle ScholarPubMed
Hurvich, C. M. and Tsai, C.-L. (1989). Regression and time series model selection in small samples. Biometrika 76, 297–307.CrossRefGoogle Scholar
Huyse, T., Audenaert, V. and Volckaert, F. A. M. (2003). Speciation and host-parasite relationships in the parasite genus Gyrodactylus (Monogenea, Platyhelminthes) infecting gobies of the genus Pomatoschistus (Gobiidae, Teleostei). International Journal for Parasitology 33, 1679–1689.CrossRefGoogle ScholarPubMed
Huyse, T. and Malmberg, G. (2004). Molecular and morphological comparisons between Gyrodactylus ostendicus n. sp. (Monogenea: Gyrodactylidae) on Pomatoschistus microps (Krøyer) and G. harengi Malmberg, 1957 on Clupea harengus membras L. Systematic Parasitology 58, 105–113.CrossRefGoogle Scholar
Huyse, T., Malmberg, G. and Volckaert, F. A. M. (2004). Four new species of Gyrodactylus Von Nordmann, 1832 (Monogenea, Gyrodactylidae) on gobiid fishes: combined DNA and morphological analyses. Systematic Parasitology 59, 103–120.CrossRefGoogle ScholarPubMed
Huyse, T. and Volckaert, F. A. M. (2002). Identification of a host-associated species complex using molecular and morphometric analyses, with the description of Gyrodactylus rugiensoides n. sp. (Gyrodactylidae, Monogenea). International Journal for Parasitology 32, 907–919.CrossRefGoogle Scholar
Koblmüller, S., Egger, B., Sturmbauer, C. and Sefc, K. M. (2010). Rapid radiation, ancient incomplete lineage sorting and ancient hybridization in the endemic Lake Tanganyika cichlid tribe Tropheini. Molecular Phylogenetics and Evolution 55, 318–334.CrossRefGoogle ScholarPubMed
Konings, A. (1998). Tanganyika Cichlids in their Natural Habitat. Cichlid Press, El Paso, Texas, USA.Google Scholar
Kritsky, D. C. and Boeger, W. A. (2003). Phylogeny of the Gyrodactylidae and the phylogenetic status of Gyrodactylus Nordmann, 1832 (Platyhelminthes: Monogenoidea). In Taxonomie, Ecologie et Evolution des Métazoaires Parasites. Taxonomy, Ecology and Evolution of Metazoan Parasites (Livre hommage à Louis Euzet). Vol. II, (ed. Combes, C. and Jourdane, J.), pp. 37–58. Presses Universitaires de Perpignan, Perpignan, France.Google Scholar
Kuusela, J., Ziętara, M. S. and Lumme, J. (2008). Description of three new European cryptic species of Gyrodactylus Nordmann, 1832 supported by nuclear and mitochondrial phylogenetic characterization. Acta Parasitologica 53, 120–126.CrossRefGoogle Scholar
Luus-Powell, W. J., Mashego, S. N. and Khalil, L. F. (2003). Mormyrogyrodactylus gemini gen. et sp. n. (Monogenea: Gyrodactylidae), a new gyrodactylid from Marcusenius macrolepidotus (Mormyridae) from South Africa. Folia Parasitologica 50, 49–55.CrossRefGoogle Scholar
Malmberg, G. (1970). The excretory systems and the marginal hooks as basis for the systematics of Gyrodactylus (Trematoda, Monogenea). Arkiv för Zoologi 2, 1–235.Google Scholar
Matĕjusová, I., Gelnar, M., McBeath, A. J. A., Collins, C. M. and Cunningham, C. O. (2001). Molecular markers for gyrodactylids (Gyrodactylidae: Monogenea) from five fish families (Teleostei). International Journal for Parasitology 31, 738–745.CrossRefGoogle ScholarPubMed
Matĕjusová, I., Gelnar, M., Verneau, O., Cunningham, C. O. and Littlewood, D. T. J. (2003). Molecular phylogenetic analysis of the genus Gyrodactylus (Platyhelminthes: Monogenea) inferred from rDNA ITS region: subgenera versus species groups. Parasitology 127, 603–611.CrossRefGoogle ScholarPubMed
Meinilä, M., Kuusela, J., Ziętara, M. S. and Lumme, J. (2002). Primers for amplifying ∼820 bp of highly polymorphic mitochondrial COI gene of Gyrodactylus salaris. Hereditas 137, 72–74.CrossRefGoogle ScholarPubMed
Meyer, A., Knowles, L. L. and Verheyen, E. (1996). Widespread geographical distribution of mitochondrial haplotypes in rock-dwelling cichlid fishes from Lake Tanganyika. Molecular Ecology 5, 341–350.CrossRefGoogle ScholarPubMed
Mwita, C. and Nkwengulila, G. (2008). Determinants of the parasite community of clariid fishes from Lake Victoria, Tanzania. Journal of Helminthology 82, 7–16.CrossRefGoogle Scholar
Nishida, M. (1991). Lake Tanganyika as an evolutionary reservoir of old lineages of East African cichlid fishes: inferences from allozyme data. Cellular and Molecular Life Sciences 47, 974–979.CrossRefGoogle Scholar
Paperna, I. (1996). Parasites, Infections and Diseases of Fishes in Africa. An Update. CIFA Technical Paper 31. Food and Agriculture Organization, Rome, Italy.Google Scholar
Paperna, I. (1979). Monogenea of Inland Water Fish in Africa. Annalen Koninklijk Museum voor Midden-Afrika Zoologische Wetenschappen, Tervuren, Belgium.Google Scholar
Pariselle, A. and Euzet, L. (2009). Systematic revision of dactylogyridean parasites (Monogenea) from cichlid fishes in Africa, the Levant and Madagascar. Zoosystema 31, 849–898.CrossRefGoogle Scholar
Poll, M. (1986). Classification des Cichlidae du lac Tanganika. Tribus, Genres et Espèces. Mémoires de la Classe des Sciences. Académie Royale de Belgique, Brussels.Google Scholar
Posada, D. (2003). Using Modeltest and PAUP* to select a model of nucleotide substitution. In Current Protocols in Bioinformatics (ed. Baxevanis, A. D., Davison, D. B., Page, R. D. M., Petsko, G. A., Stein, L. D. and Stormo, G. D.), pp. 6.5.1–6.5.14. John Wiley & Sons, Inc., New York, USA.Google Scholar
Posada, D. (2008). jModelTest: phylogenetic model averaging. Molecular Biology and Evolution 25, 1253–1256.CrossRefGoogle ScholarPubMed
Přikrylová, I., Matĕjusová, I., Musilová, N. and Gelnar, M. (2009 a). 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: Cichlidae). Parasitology Research 106, 1–6.CrossRefGoogle Scholar
Přikrylová, I., Matĕjusová, I., Musilová, N., Gelnar, M. and Harris, P. D. (2009 b). A new gyrodactylid (Monogenea) genus on gray bichir, Polypterus senegalus (Polypteridae) from Senegal (West Africa). Journal of Parasitology 95, 555–560.CrossRefGoogle ScholarPubMed
Prudhoe, S. (1951). Trematoda, Cestoda and Acanthocephala. In Exploration Hydrobiologique du Lac Tanganyika (1946–1947) – Résultats Scientifiques. Vol. III(2). Royal Belgian Institute of Natural Sciences, Brussels.Google Scholar
Pugachev, O. N., Gerasev, P. I., Gussev, A. V., Ergens, R., Khotenowsky, I. (2009). Guide to Monogenoidea of Freshwater Fish of Palaearctic and Amur Regions. Ledizione-LediPublishing, Milan, Italy.Google Scholar
Raeymaekers, J. A. M., Huyse, T., Maelfait, H., Hellemans, B. and Volckaert, F. A. M. (2008). Community structure, population structure and topographical specialisation of Gyrodactylus (Monogenea) ectoparasites living on sympatric stickleback species. Folia Parasitologica 55, 187–196.CrossRefGoogle ScholarPubMed
Rodriguez, F., Oliver, J. L., Marin, A. and Medina, J. R. (1990). The general stochastic model of nucleotide substitution. Journal of Theoretical Biology 142, 485–501.CrossRefGoogle ScholarPubMed
Ronquist, F. and Huelsenbeck, J. P. (2003). MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19, 1572–1574.CrossRefGoogle ScholarPubMed
Salzburger, W., Meyer, A., Baric, S., Verheyen, E. and Sturmbauer, C. (2002). Phylogeny of the Lake Tanganyika cichlid species flock and its relationship to the Central and East African haplochromine cichlid fish faunas. Systematic Biology 51, 113–135.CrossRefGoogle Scholar
Salzburger, W., Mack, T., Verheyen, E. and Meyer, A. (2005) Out of Tanganyika: genesis, explosive speciation, key-innovations and phylogeography of the haplochromine cichlid fishes. BMC Evolutionary Biology 5, 17. doi: 10.1186/1471-2148-5-17CrossRefGoogle ScholarPubMed
Shinn, A. P., Bron, J. E., Sommerville, C. and Gibson, D. I. (2003). Comments on the mechanism of attachment in species of the monogenean genus Gyrodactylus. Invertebrate Biology 122, 1–11.CrossRefGoogle Scholar
Shinn, A. P., Hansen, H., Olstad, K., Bachmann, L. and Bakke, T. A. (2004). The use of morphometric characters to discriminate specimens of laboratory-reared and wild populations of Gyrodactylus salaris and G. thymalli (Monogenea). Folia Parasitologica 51, 239–252.Google Scholar
Snoeks, J. (2000). How well known is the ichthyodiversity of the large East African lakes? Advances in Ecological Research 31, 17–38.CrossRefGoogle Scholar
StatSoft, Inc. (2008). STATISTICA (Data Analysis Software System), Version 8.0. www.statsoft.com.Google Scholar
Sturmbauer, C., Hainz, U., Baric, S., Verheyen, E. and Salzburger, W. (2003). Evolution of the tribe Tropheini from Lake Tanganyika: synchronized explosive speciation producing multiple evolutionary parallelism. Hydrobiologia 500, 51–64.CrossRefGoogle Scholar
Swofford, D. L. (2001). PAUP*: Phylogenetic Analysis Using Parsimony (*and Other Methods), Version 4.0b10. Sinauer Associates, Sunderland, MA, USA.Google Scholar
Tavaré, S. (1986). Some probabilistic and statistical problems in the analysis of DNA sequences. In Some Mathematical Questions in Biology – DNA Sequence Analysis (ed. Miura, R. M.), pp. 57–86. American Mathematical Society, Providence, Rhode Island, USA.Google Scholar
Trewavas, E. (1983). Tilapiine Fishes of the Genera Sarotherodon, Oreochromis and Danakilia. British Museum (Natural History), London, UK.CrossRefGoogle Scholar
Vaughan, D. B., Christison, K. W., Hansen, H. and Shinn, A. P. (2010). Gyrodactylus eyipayipi sp. n. (Monogenea: Gyrodactylidae) from Syngnathus acus (Syngnathidae) from South Africa. Folia Parasitologica 57, 11–15.CrossRefGoogle Scholar
Vianna, R. T., Boeger, W. A. and Dove, A. D. M. (2007). Neotropical Monogenoidea. 51. Scutalatus magniancoratus gen. et sp. n. (Gyrodactylidae) from the South-American electric eel, Electrophorus electricus (Gymnotidae, Gymnotiformes), and redescription of Mormyrogyrodactylus gemini from the African bulldog, Marcusenius macrolepidotus (Mormyridae, Osteoglossiformes). Acta Zoologica (Stockholm) 88, 89–94.CrossRefGoogle Scholar
Whittington, I. D. (1998). Diversity “down under”: monogeneans in the Antipodes (Australia) with a prediction of monogenean biodiversity worldwide. International Journal for Parasitology 28, 1481–1493.CrossRefGoogle ScholarPubMed
Wilson, A. B., Glaubrecht, M. and Meyer, A. (2004). Ancient lakes as evolutionary reservoirs: evidence from the thalassoid gastropods of Lake Tanganyika. Proceedings of the Royal Society of London, B 271, 529–536.CrossRefGoogle ScholarPubMed
Ziętara, M. S., Huyse, T., Lumme, J. and Volckaert, F. A. M. (2002). Deep divergence among subgenera of Gyrodactylus inferred from rDNA ITS region. Parasitology 124, 39–52.CrossRefGoogle ScholarPubMed
Ziętara, M. S. and Lumme, J. (2002). Speciation by host-switching and adaptive radiation in a fish parasite genus Gyrodactylus (Monogenea, Gyrodactylidae). Evolution 56, 2445–2458.Google Scholar
Ziętara, M. S. and Lumme, J. (2003). The crossroads of molecular, typological and biological species concepts: two new species of Gyrodactylus Nordmann, 1832 (Monogenea: Gyrodactylidae). Systematic Parasitology 55, 39–52.CrossRefGoogle ScholarPubMed
Ziętara, M. S. and Lumme, J. (2004). Comparison of molecular phylogeny and morphological systematics in fish parasite genus Gyrodactylus Nordmann, 1832 (Monogenea, Gyrodactylidae). Zoologica Poloniae 49, 5–28.Google Scholar