The parasites of a successful invader: monogeneans of the Asian topmouth gudgeon Pseudorasbora parva, with description of a new species of Gyrodactylus
Jazyk angličtina Země Francie Médium print-electronic
Typ dokumentu časopisecké články
Grantová podpora
20-29111S
Czech Science Foundation
PubMed
37326471
PubMed Central
PMC10274305
DOI
10.1051/parasite/2023024
PII: parasite230035
Knihovny.cz E-zdroje
- Klíčová slova
- Bivaginogyrus, Monogenea, New species, Parasite loss, Phylogeny, Species invasion,
- MeSH
- Cyprinidae * parazitologie MeSH
- fylogeneze MeSH
- máloostní * MeSH
- nemoci ryb * epidemiologie parazitologie MeSH
- paraziti * MeSH
- Trematoda * genetika MeSH
- zvířata MeSH
- Check Tag
- mužské pohlaví MeSH
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
Monogenean parasites are often co-introduced with their fish hosts into novel areas. This study confirmed co-introduction of two dactylogyrids, Dactylogyrus squameus Gusev, 1955 and Bivaginogyrus obscurus (Gusev, 1955), and a newly described gyrodactylid species, Gyrodactylus pseudorasborae n. sp. into Europe along with their fish host, the invasive topmouth gudgeon Pseudorasbora parva (Temminck & Schlegel) from East Asia. All three species were observed in the lower Dnieper and middle Danube basin regions and had slightly larger haptoral hard parts than the same parasites in their native range. While dactylogyrids occurred sporadically, we recorded regular infection by G. pseudorasborae n. sp. at relatively high prevalence and abundance. This latter species was observed in both the native and non-native range of topmouth gudgeon, and resembles Gyrodactylus parvae You et al., 2008 recently described from P. parva in China. Both species were distinguished based on genetic analysis of their ITS rDNA sequence (6.6% difference), and morphometric differences in the marginal hooks and male copulatory organ. Phylogenetic analysis of dactylogyrid monogeneans showed that B. obscurus clustered with Dactylogyrus species parasitising Gobionidae and Xenocyprididae, including D. squameus, supporting recent suggestions of a paraphyletic origin of the Dactylogyrus genus. In addition to co-introduced parasites, topmouth gudgeon was infected with a local generalist, G. prostae Ergens, 1964, increasing the number of monogeneans acquired in Europe to three species. Nevertheless, monogenean infections were generally lower in non-native host populations, potentially giving an advantage to invading topmouth gudgeon.
TITLE: Les parasites d’un envahisseur à succès : les monogènes du goujon asiatique Pseudorasbora parva, avec description d’une nouvelle espèce de Gyrodactylus. ABSTRACT: Les parasites monogènes sont souvent co-introduits avec leurs hôtes poissons dans de nouvelles zones. Cette étude a confirmé la co-introduction de deux Dactylogyridae, Dactylogyrus squameus Gusev, 1955 et Bivaginogyrus obscurus (Gusev, 1955), et d’une espèce de Gyrodactylidae nouvellement décrite, Gyrodactylus pseudorasborae n. sp. en Europe, en même temps que leur hôte poisson, le goujon envahissant Pseudorasbora parva (Temminck & Schlegel) qui vient d’Asie de l’Est. Les trois espèces ont été observées dans les régions du bas Dniepr et du bassin moyen du Danube et avaient des parties sclérifiées haptorales légèrement plus grandes que les mêmes parasites dans leur aire de répartition d’origine. Alors que les Dactylogyridae étaient rares, nous avons enregistré une infection régulière par G. pseudorasborae n. sp. à une prévalence et une abondance relativement élevées. Cette dernière espèce a été observée à la fois dans l’aire de répartition indigène et non indigène du goujon asiatique et ressemble à Gyrodactylus parvae You et al., 2008 récemment décrit chez P. parva en Chine. Les deux espèces ont été distinguées sur la base de l’analyse génétique de leur séquence ITS de l’ADNr (différence de 6,6 %) et des différences morphométriques dans les crochets marginaux et l’organe copulateur mâle. L’analyse phylogénétique des monogènes Dactylogyridae a montré que B. obscurus se regroupait avec des espèces de Dactylogyrus parasitant les Gobionidae et les Xenocyprididae, y compris D. squameus, soutenant les suggestions récentes d’une origine paraphylétique du genre Dactylogyrus. En plus des parasites co-introduits, le goujon asiatique était infecté par un généraliste local, G. prostae Ergens, 1964, portant le nombre de monogènes acquis en Europe à trois espèces. Néanmoins, les infections par les monogènes étaient généralement plus faibles dans les populations d’hôtes non indigènes, donnant potentiellement un avantage à l’invasion du goujon asiatique.
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Aguiar JC, Maia AAM, Silva MRM, Ceccarelli PS, Domingues MV, Adriano EA. 2017. An integrative taxonomic study of Pavanelliella spp. (Monogenoidea, Dactylogyridae) with the description of a new species from the nasal cavities of an Amazon pimelodid catfish. Parasitology International, 66, 777–788. PubMed
Ahne W, Thomsen I. 1986. Isolation of pike fry rhabdovirus from Pseudorasbora parva (Temminck and Schlegel). Journal of Fish Diseases, 9, 555–556.
Azuma M, Motomura Y. 1998. Feeding habits of largemouth bass in a non-native environments: the case of a small lake with bluegill in Japan. Environmental Biology of Fishes, 52, 379–389.
Bakke TA, Cable J, Harris PD. 2007. The biology of gyrodactylid monogeneans: the “Russian-doll killers”. Advanced in Parasitology, 64, 161–376. PubMed
Bănărescu P. 1964. Fauna Republicii Populare Române. 13. Pisces - Osteichthyes (peşti ganoizi şi osoşi), vol 13, Academiei Republicii Populare Române: Bucuresti.
Behrmann-Godel J, Roch S, Brinker A. 2014. Gill worm Ancyrocephalus percae (Ergens 1966) outbreak negatively impacts the Eurasian perch Perca fluviatilis L. stock of Lake Constance, Germany. Journal of Fish Diseases, 37(10), 925–930. PubMed
Belova SV. 1988. Variability of chitinoid structures of Dactylogyrus hypophtalmichthys (Monogenoidea) in relation to host size and season, in Investigations of Monogeneans in the USSR. Skarlato OA, Editor. Balkema: Rotterdam. p. 38–43.
Benovics M, Kičinjaová ML, Šimková A. 2017. The phylogenetic position of the enigmatic Balkan Aulopyge huegelii (Teleostei: Cyprinidae) from the perspective of host-specific Dactylogyrus parasites (Monogenea), with a description of Dactylogyrus omenti n. sp. Parasites & Vectors, 10, 547. PubMed PMC
Benovics M, Desdevises Y, Vukic J, Sanda R, Simkova A. 2018. The phylogenetic relationships and species richness of host-specific Dactylogyrus parasites shaped by the biogeography of Balkan cyprinids. Scientific Reports, 8(1), 13006. PubMed PMC
Benovics M, Desdevises Y, Šanda R, Vukić J, Scheifler M, Doadrio I, Sousa-Santos C, Šimková A. 2020. High diversity of fish ectoparasitic monogeneans (Dactylogyrus) in the Iberian Peninsula: a case of adaptive radiation? Parasitology, 147, 418–430. PubMed PMC
Benovics M, Nejat F, Abdoli A, Simkova A. 2021. Molecular and morphological phylogeny of host-specific Dactylogyrus parasites (Monogenea) sheds new light on the puzzling Middle Eastern origin of European and African lineages. Parasites & Vectors, 14(1), 372. PubMed PMC
Beyer K. 2004. Escapees of potentially invasive fishes from an ornamental aquaculture facility: the case of topmouth gudgeon Pseudorasbora parva. Journal of Fish Biology, 65(Suppl. A), 326–327.
Blasco-Costa MI, Míguez-Lozano R, Sarabeev V, Balbuena JA. 2012. Molecular phylogeny of species of Ligophorus (Monogenea: Dactylogyridae) and their affinities within the Dactylogyridae. Parasitology International, 61, 619–627. PubMed
Bruno DW, Collins CM, Cunningham CO, 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. PubMed
Bush AO, Lafferty KD, Lotz JM, Shostak AW. 1997. Parasitology meets ecology on its own terms: Margolis et al. Revisited. Journal of Parasitology, 83, 575–583. PubMed
Cable J, Harris PD, Tinsley RC, Lazarus CM. 1999. Phylogenetic analysis of Gyrodactylus spp. (Platyhelminthes: Monogenea) using ribosomal DNA sequences. Canadian Journal of Zoology, 77(9), 1439–1449.
Cakic P, Lenhardt M, Kolarevic J, Mickovic B, Hegedis A. 2004. Distribution of the Asiatic cyprinid Pseudorasbora parva in Serbia and Montenegro. Journal of Fish Biology, 65, 1431–1434.
Cheng J, Zou H, Li M, Wang J, Wang G, Li W. 2023. Morphological and Molecular Identification of Dactylogyrus gobiocypris (Monogenea: Dactylogyridae) on Gills of a Model Fish, Gobiocypris rarus (Cypriniformes: Gobionidae). Pathogens, 12(2), 206. PubMed PMC
Copp GH, Fox MG. 2007. Growth and life history traits of introduced pumpkinseed (Lepomis gibbosus) in Europe, and the relevance to its potential invasiveness, in Biological invaders in inland waters: Profiles, distribution, and threats. Gherardi F, Editor. Springer: Dordrecht. p. 289–306.
Cunningham CO. 1997. Species variation within the internal transcribed spacer (ITS) region of Gyrodactylus (Monogenea: Gyrodactylidae) ribosomal RNA genes. Journal of Parasitology, 83(2), 215–219. PubMed
Dávidová M, Jarkovský J, Matějusová I, Gelnar M. 2005. Seasonal occurrence and metrical variability of Gyrodactylus rhodei Žitňan 1964 (Monogenea, Gyrodactylidae). Parasitology Research, 95, 398–405. PubMed
Fazio G, Sasal P, Mouahid G, Lecomte-Finiger R, Moné H. 2012. Swim bladder nematodes (Anguillicoloides crassus) disturb silvering in european eels (Anguilla anguilla). Journal of Parasitology, 98(4), 695–705. PubMed
Galli P, Strona G, Benzoni F, Crosa G, Stefani F. 2007. Monogenoids from freshwater fish in Italy, with comments on alien species. Comparative Parasitology, 74, 264–272.
Galli P, Pugachev ON, Kritsky D. 2010. Guide to Monogenoidea of freshwater fish of Palaearctic and Amur regions. Ledizioni-Ledi Publishing: Milan.
Gilmore SR, Cone DK, Lowe G, King SK, Jones SRM, Abbott CL. 2012. Molecular phylogeny of Gyrodactylus (Monogenea) parasitizing fishes in fresh water, estuarine, and marine habitats in Canada. Canadian Journal of Zoology, 90(6), 776–786.
Gozlan RE, Andreou D, Asaeda T, Beyer K, Bouhadad R, Burnard D, Caiola N, Cakic P, Djikanovic V, Esmaeili HR, Falka I, Golicher D, Harka A, Jeney G, Kováč V, Musil J, Nocita A, Povz M, Poulet N, Virbickas T, Wolter C, Tarkan AS, Tricarico E, Trichkova T, Verreycken H, Witkowski A, Zhang CG, Zweimueller I, Britton JR. 2010. Pan-continental invasion of Pseudorasbora parva: towards a better understanding of freshwater fish invasions. Fish & Fisheries, 11, 315–340.
Gussev AV. 1955. Monogenetic trematodes of the fishes of Amur River system. Trudy Zoologicheskogo Instituta Academii Nauk USSR, 19, 171–400.
Gussev AV, Gerasev PI. 1985. Rod Bivaginogyrus Gussev et Gerasev 1985, in Opredelitel’ Parazitov Presnovodnykh Ryb Fauny SSSR, Tom 2. Bauer ON, Editor. Nauka: Leningrad. p. 192–194 [In Russian].
Gusev AV, Dubinina MN, Raikova EV, Khotenkovskiy IA, Pugachev ON, Ergens R. 1985. Paraziticheskiye mnogokletochnye. Part 1. Monogenea, in Opredelitel’ Parazitov Presnovodnykh Ryb Fauny SSSR, Tom 2. Bauer ON, Editor. Nauka: Leningrad. p. 10–268 [In Russian].
Hall TA. 1999. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series, 41, 95–98.
Hardouin EA, Andreou D, Zhao Y, Chevret P, Fletcher DH, Britton JR, Gozlan RE. 2018. Reconciling the biogeography of an invader through recent and historic genetic patterns: the case of topmouth gudgeon Pseudorasbora parva. Biological Invasions, 20, 2157–2171.
Harris PD, Shinn AP, Cable J, Bakke TA. 2004. Nominal species of the genus Gyrodactylus von Nordmann 1832 (Monogenea: Gyrodactylidae), with a list of principal host species. Systematic Parasitology, 59, 1–27. PubMed
Hassouna N, Michot B, Bachellerie JP. 1984. The complete nucleotide sequence of mouse 28S rRNA gene. Implications for the process of size increase of the large subunit rRNA in higher eukaryotes. Nucleic Acids Research, 12(8), 3563–3583. PubMed PMC
ICZN. 1999. International Code of Zoological Nomenclature. The International Trust for Zoological Nomenclature: London. http://www.nhm.ac.uk/hosted-sites/iczn/code/.
Kalyaanamoorthy S, Minh B, Wong T, von Haeseler A, Jermiin LS. 2017. ModelFinder: fast model selection for accurate phylogenetic estimates. Nature Methods, 14(6), 587–589. PubMed PMC
Katoh K, Rozewicki J, Yamada KD. 2019. MAFFT online service: multiple sequence alignment, interactive sequence choice and visualization. Briefings in Bioinformatics, 20(4), 1160–1166. PubMed PMC
Kirk RS. 2003. The impact of Anguillicola crassus on European eels. Fisheries Management and Ecology, 10, 385–394.
Kmentová N, Cruz-Laufer AJ, Pariselle A, Smeets K, Artois T, Vanhove MPM. 2022. Dactylogyridae 2022: a meta-analysis of phylogenetic studies and generic diagnoses of parasitic flatworms using published genetic and morphological data. International Journal for Parasitology, 52, 427–457. PubMed
Kottelat M, Freyhof J. 2007. Handbook of European freshwater fishes. Publications Kottelat, Cornol and Freyhof: Berlin.
Kumar S, Stecher G, Li M, Knyaz C, Tamura K. 2018. MEGA X: Molecular evolutionary genetics analysis across computing platforms. Molecular Biology and Evolution, 35(6), 1547–1549. PubMed PMC
Kuusela J, Zietara MS, Lumme J. 2008. Description of three European cryptic species of Gyrodactylus Nordmann, 1832 supported by nuclear and mitochondrial phylogenetic characterisation. Acta Parasitologica, 53(2), 120–126.
Kvach Y, Ondračková M, Janáč M, Jurajda P. 2016. Methodological issues affecting the study of fish parasites. I. Duration of live fish storage prior to dissection. Diseases of Aquatic Organisms, 119, 107–115. PubMed
Kvach Y, Ondračková M, Bryjová A, Jurajda P. 2017. Parasites as biological tags of divergence in Central European gudgeon populations (Actinopterygii: Cyprinidae: Gobioninae). Biologia, 72, 671–679.
Kvach Y, Ondračková M, Kutsokon Y, Dzyziuk N. 2018. New record of monogenean parasites on non-indigenous fishes in the Ukrainian Danube delta. BioInvasions Records, 7, 65–72.
Li RR, Li WX, Wu XD, Wang GT. 2014. Identification of Gyrodactylus species in goldfish (Carassius auratus) through morphological study and the analysis of rDNA ITS sequence. Acta Hydrobiologica Sinica, 38, 903–909.
Lymbery AJ, Morine M, Kanani HG, Beatty SJ, Morgan DL. 2014. Co-invaders: the effects of alien parasites on native hosts. International Journal for Parasitology: Parasites and Wildlife, 3, 171–177. PubMed PMC
Malmberg G. 1970. The excretory systems and the marginal hooks as a basis for the systematics of Gyrodactylus (Trematoda, Monogenea). Arkiv für Zoology, 23, 1–235.
Margaritov NM, Kiritsis SG. 2011. Parasites of topmouth gudgeon Psudorasbora parva (Schlegel) in fish farms in Bulgaria. Acta Zoologica Bulgarica, 63, 187–193.
Matějusová I, Gelnar M, McBeath AJA, Collins CM, Cunningham CO. 2001. Molecular markers for gyrodactylids (Gyrodactylidae: Monogenea) from five fish families (Teleostei). International Journal for Parasitology, 31, 738–745. PubMed
Matejusová I, Gelnar M, Verneau O, Cunningham CO, Littlewood DTJ. 2003. Molecular phylogenetic analysis of the genus Gyrodactylus (Platyhelminthes: Monogenea) inferred from rDNA ITS region: subgenera versus species groups. Parasitology, 127(6), 603–611. PubMed
Mendlová M, Šimková A. 2014. Evolution of host specificity in monogeneans parasitizing African cichlid fish. Parasites & Vectors, 7, 69. PubMed PMC
Minh BQ, Nguyen MAT, von Haeseler A. 2013. Ultrafast approximation for phylogenetic bootstrap. Molecular Biology and Evolution, 30(5), 1188–1195. PubMed PMC
Mo TA. 1991. Variation of opisthaptoral hard parts of Gyrodactylus salaris Malmberg, 1957 (Monogenea: Gyrodactylidae) on rainbow trout Oncorhynchus mykiss (Walbaum, 1792) in a fish farm, with comments on the spreading of the parasite in south-eastern Norway. Systematic Parasitology, 20, 1–10.
Moravec F. 2001. Checklist of metazoan parasites of fishes of the Czech Republic and the Slovak Republic (1873–2000). Akademia: Praha.
Nagasawa K, Kim Y-G, Hirose H. 1994. Anguillicola crassus and A. globiceps (Nematoda: Dracunculoidea) parasitic in the swimbladder of eels (Anguilla japonica and A. anguilla) in East Asia: a review. Folia Parasitologica, 41, 127–137.
Nguyen L-T, Schmidt HA, von Haeseler A, Minh BQ, Notes A. 2015. IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Molecular Biology and Evolution, 32(1), 268–274. PubMed PMC
Nitta M, Nagasawa K. 2014. Bivaginogyrus obscurus (Monogenea: Dactylogyridae), a gill parasite of two cyprinids Pseudorasbora pumila pumila and Pseudorasbora parva, new to Japan. Species Diversity, 19, 167–171.
Nitta M, Nagasawa K. 2016. New geographical records of three gill monogeneans (Platyhelminthes) parasitic on Pseudorasbora parva (Cypriniformes: Cyprinidae) in Japan. Species Diversity, 21, 1–7.
Nitta M, Nagasawa K. 2016. A new species of Dactylogyrus (Monogenea: Dactylogyridae) parasitic on an endangered freshwater fish, Rhodeus atremius atremius, endemic to Japan. Parasitology International, 65, 483–487. PubMed
Nitta M, Nagasawa K. 2020. Gobioecetes longibasais n. sp. (Monogenea: Dactylogyridae) from Rhinogobius similis Gill (Perciformes: Gobiidae) from Okinawa-jima Island, the Ryukyu Archipelago, Southern Japan, with a new host record for Gobioecetes biwaensis Ogawa and Itoh, 2017. Systematic Parasitology, 97(2), 193–200. PubMed
Nitta M, Nagasawa K. 2023. Gill monogeneans (Platyhelminthes) parasitic on Gnathopogon elongatus elongatus and G. caerulescens (Cypriniformes: Gobionidae) from Japan, with descriptions of one new species of Dactylogyrus and three new species of Bivaginogyrus (Dactylogyridae). Species Diversity, 28, 69–97.
Ondračková M, Matějusová I, Šimková A, Gelnar M. 2004. New reports of dactylogyridean species (Monogenea) for Central Europe. Helminthologia, 41, 139–145.
Ondračková M, Dávidová M, Přikrylová I, Pečínková M. 2011. Monogenean parasites of introduced pumpkinseed Lepomis gibbosus (Centrarchidae) in the Danube River basin. Journal of Helminthology, 85, 435–441. PubMed
Ondračková M, Seifertová M, Bryjová A, Leis E, Jurajda P. 2020. Morphometric and genetic evidence for cryptic diversity in Gyrodactylus (Monogenea) infecting non-native European populations of Ameiurus nebulosus and A. melas. Parasitology, 147, 1700–1711. PubMed PMC
Ondračková M, Bartáková V, Kvach Y, Bryjová A, Trichkova T, Ribeiro F, Carassou L, Martens A, Masson G, Zechmeister T, Jurajda P. 2021. Parasite infection reflects host genetic diversity in the pumpkinseeds non-native range. Hydrobiologia, 848, 2169–2187.
Paladini G, Hansen H, Fioravanti ML, Shinn AP. 2011. Gyrodactylus longipes n. sp. (Monogenea: Gyrodactylidae) from farmed gilthead seabream (Sparus aurata L.) from the Mediterranean. Parasitology International, 60, 410–418. PubMed
Parker JD, Torchin ME, Hufbauer RA, Lemoine NP, Alba C, Blumenthal DM, Bossdorf O, Byers JE, Dunn AM, Heckman RW, Mn Hejda, Jarošík V, Kanarek AR, Martin LB, Perkins SE, Pyšek P, Schierenbeck K, Schlöder C, van Klinken R, Vaughn KJ, Williams W, Wolfe LM. 2013. Do invasive species perform better in their new ranges? Ecology, 94, 985–994. PubMed
Poulin R, Mouillot D. 2003. Host introductions and the geography of parasite taxonomic diversity. Journal of Biogeography, 30, 837–845.
Prenter J, MacNeil C, Dick JTA, Dunn AM. 2004. Roles of parasites in animal invasions. Trends in Ecology and Evolution, 19, 385–390. PubMed
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 and Bychowsky, 1967. Systematic Parasitology, 69, 33–44. PubMed
Prost M. 1973. Fish Monogenoidea of Poland. II. Parasites of Ictalurus nebulosus (Le Sueur). Revision of genera Cleidodiscus Mueller, 1934 and Urocleidus Mueller, 1934. Acta Parasitologica Polonica, 21, 315–326.
Rambaut A. 2017. FigTree (version 1.4.3). Available at: http://tree.bio.ed.ac.uk/software/figtree/.
Rambaut A, Drummond AJ, Xie D, Baele G, Suchard MA. 2018. Posterior summarization in Bayesian phylogenetics using Tracer 1.7. Systematic Biology, 67(5), 901–904. PubMed PMC
Rokicka M, Lumme J, Ziętara MS. 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(3), 185–195.
Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, Höhna S, Larget B, Liu L, Suchard MA, Huelsenbeck JP. 2012. MrBayes 3.2: Efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology, 61(3), 539–542. PubMed PMC
Shinn AP, Hansen H, Olstad K, Bachmann L, Bakke TA. 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. PubMed
Shinn AP, Harris PD, Cable J, Bakke TA, Paladini G, Bron JE. 2010. GyroDb. World Wide Web electronic publication. www.gyrodb.net, version (06/2022).
Šimková A, Morand S, Jobet E, Gelnar M, Verneau O. 2004. Molecular phylogeny of congeneric monogenean parasites (Dactylogyrus): a case of intrahost speciation. Evolution, 58, 1001–1018. PubMed
Šimková A, Verneau O, Gelnar M, Morand S. 2006. Specificity and specialization of congeneric monogeneans parasitizing cyprinid fish. Evolution, 60, 1023–1037. PubMed
Šimková A, Navrátilová P, Dávidová M, Ondračková M, Sinama M, Chappaz R, Gilles A, Costedoat C. 2012. Does invasive Chondrostoma nasus shift the parasite community structure of endemic Parachondrostoma toxostoma in sympatric zones? Parasites & Vectors, 5, 200. PubMed PMC
Šimková A, Benovics M, Rahmouni I, Vukić J. 2017. Host-specific Dactylogyrus parasites revealing new insights on the historical biogeography of Northwest African and Iberian cyprinid fish. Parasites & Vectors, 10, 589. PubMed PMC
Simon A, Gozlan RE, Robert Britton J, van Oosterhout C, Hänfling B. 2015. Human induced stepping-stone colonisation of an admixed founder population: the spread of topmouth gudgeon (Pseudorasbora parva) in Europe. Aquatic Sciences, 77, 17–25.
Sinnappah ND, Lim SL-H, Rohde K, Tinsley R, Combes C, Verneau O. 2001. A paedomorphic parasite associated with a neotenic amphibian host: phylogenetic evidence suggests a revised systematic position for Sphyranuridae within anuran and turtle polystomatoineans. Molecular Phylogenetics and Evolution, 18(2), 189–201. PubMed
Škoríková B, Scholz T, Moravec F. 1996. Spreading of introduced monogeneans Pseudodactylogyrus anguillae and P. bini among eel populations in the Czech Republic. Folia Parasitologica, 43, 155–156. PubMed
StatSoft. 2022. STATISTICA (Data Analysis Software System), Version 14.1.
Taraschewski H. 2006. Hosts and parasites as aliens. Journal of Helminthology, 80, 99–128. PubMed
Torchin ME, Lafferty KD, Dobson AP, McKenzie VJ, Kuris AM. 2003. Introduced species and their missing parasites. Nature, 421, 628–629. PubMed
Trifinopoulos J, Nguyen L-T, von Haeseler A, Minh BQ. 2016. W-IQ-TREE: a fast, online phylogenetic tool for maximum likelihood analysis. Nucleic Acids Research, 44(W1), W232–W235. PubMed PMC
Tu X, Ling F, Huang A, Wang G. 2015. An infection of Gyrodactylus kobayashii Hukuda, 1940 (monogenea) associated with the mortality of goldfish (Carassius auratus) from central China. Parasitology Research, 114, 737–745. PubMed
Vancheva N, Bobeva A, Pehlivanov L, Stefanov T, Georgiev BB. 2020. Alien parasites on an alien fish species: monogeneans from the black bullhead Ameiurus melas (Siluriformes) in the Lake Srebarna Biosphere Reserve, Bulgaria, with the fist record of Gyrodactylus nebulosus in the Palaearctic. Parasitology Research, 119, 2105–2112. PubMed
Whittington ID, Cribb BW, Hamwood TE, Halliday J. 2000. Host-specificity of monogenean (platyhelminth) parasites: a role for anterior adhesive areas? International Journal for Parasitology, 30, 305–320. PubMed
Winger AC, Hansen H, Bachmann L, Bakke TA. 2008. Gyrodactylus species (Monogenea) infecting alpine bullhead (Cottus poecilopus Heckel, 1837) in Norway and Slovakia, including the description of Gyrodactylus mariannae sp. nov. Acta Parasitology, 53(3), 240–250.
You P, Easy R, Cone DK. 2008. Gyrodactylus parvae n. sp. (Monogenea) from the fins and body surface of Pseudorasbora parva (Cyprinidae) in central China. Comparative Parasitology, 75, 28–32.
Yuryshynets V, Zaichenko N. 2015. Comparative analysis of the parasite fauna of Pseudorasbora parva (Cyprinidae) in the native and non-native areas of its distribution. Hydrobiological Journal, 51, 101–109.
Ziętara MS, Lumme J. 2002. Speciation by host switch and adaptive radiation in a fish parasite genus Gyrodactylus (Monogenea, Gyrodactylidae). Evolution, 56, 2445–2458. PubMed
Ziętara M, Lumme J. 2004. Comparison of molecular phylogeny and morphological systematics in fish parasite genus Gyrodactylus Nordmann, 1832 (Monogenea, Gyrodactylidae). Zoologica Poloniae, 49(1–4), 5–28.
Zietara MS, Huyse T, Lumme J, Volckaert FA. 2002. Deep divergence among subgenera of Gyrodactylus inferred from rDNA ITS region. Parasitology, 124(1), 39–52. PubMed