Gyrodactylid parasites were observed on non-native populations of North-American freshwater catfishes, Ameiurus nebulosus and Ameiurus melas (Siluriformes: Ictaluridae), at several sites in the Elbe River basin, Czech Republic, Europe. Using a combination of morphological and genetic analyses, the parasites infecting A. nebulosus were determined to be Gyrodactylus nebulosus, a North American parasite co-introduced to Europe along with its Ameiurus fish hosts. Subtle morphometrical differences, as well as seasonal variations, were observed among parasites collected from A. nebulosus and A. melas. The host-related variation was further supported through genetic analysis of the partial 18S rDNA, ITS1-5.8S-ITS2 and COI, showing 0.2, 3.0 and 4.8% divergence, respectively. Consistent genetic differences indicated there were two distinct genotypes. Subtle morphological differences associated with the shape of sickle toe, anchor root and ventral bar membrane, according to host species, also supported the description of a new cryptic species, Gyrodactylus melas n. sp., infecting A. melas. Multivariate morphometrical analysis of haptoral hard parts showed significant differences between the anchor lengths of G. nebulosus and G. melas n. sp. However, the measurements of the haptoral hard structures partially overlapped between species, limiting the usage of these parameters for species delineation.

Czech Academy of Sciences Institute of Vertebrate Biology Květná 8 60365Brno Czech Republic

Department of Botany and Zoology Masaryk University Faculty of Science Kotlářská 2 61137Brno Czech Republic

Faculty of Agronomy Mendel University Zemědělská 1 1665 603 65Brno Czech Republic

U S Fish and Wildlife Service La Crosse Fish Health Center Midwest Fisheries Center Onalaska Wisconsin USA

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Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W and Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Research 25, 3389–3402. PubMed PMC

Béres B, Kánainé SD, Muller T, Staszny A, Farkas M, Baks K, Orbán L, Urbányi B and Kovács B (2017) Species-specific markers provide molecular genetic evidence for natral introgression of bullhead catfishes in Hungary. PeerJ 5, e2804. PubMed PMC

Bueno-Silva M, Boeger WA and Pie MR (2011) Choice matters: incipient speciation in Gyrodactylus Corydori (Monogenoidea: Gyrodactylidae). International Journal for Parasitology 41, 657–667. 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

Cunningham C (1997) Species variation within the internal transcribed space (ITS) region of Gyrodactylus (Monogenea: Gyrodactylidae) ribosomal RNA genes. Journal of Parasitology 83, 215–219. PubMed

Dávidová M, Jarkovský J, Matějusová I and Gelnar M (2005) Seasonal occurrence andmetrical variability of Gyrodactylus Rhodei Žitňan 1964 (monogenea. Gyrodactylidae). Parasitology Research 95, 398–405. PubMed

Galli P, Pugachev ON and Kritsky D (2010) Guide to Monogenoidea of Freshwater Fish of Palaearctic and Amur Regions. Milan, Italy: Ledizioni-Ledi Publishing.

García-Vásquez A, Hansen H, Christison KW, Bron JE and Shinn AP (2011) Description of free new species of Gyrodactylus von Nordmann, 1832 (Monogenea) parasitising Oreochromis niloticus niloticus (L.) and O. mossambicus (Peters) Cichlidae. Acta Parasitologica 56, 20–33.

García-Vásquez A, Razo-Mendivil U and Rubio-Godoy M (2015) Morphological and molecular description of eight new species of Gyrodactylus von Nordmann, 1832 (Platyhelminthes: Monogena) from Poecilid fishes, collected in thein natural distribution range in the Gulf of Mexico slope, Mexico. Parasitology Research 114, 3337–3355. PubMed

Gilmore SR, Cone DK, Lowe G, King SK, Jones SRM and Abbott CL (2012) Molecular phylogeny of Gyrodactylus (Monogenea) parasitizing fishes in fresh water, estuarine and marine habitats in Canada. Canadian Journal of Zoology 90, 776–786.

Hanel L and Lusk S (2005) Fishes and Lampreys of the Czech Republic: Distribution and Conservation. Vlašim, Czech Republic: ZO ČSOP Vlašim (in Czech with English summary).

Hansen H, Bakke TA and Bachmann L (2007) DNA Taxonomy and barcoding of monogenean parasites: lessons from Gyrodactylus. Trends in Parasitology 23, 363–367. PubMed

Hoffman GL (1999) Parasites of North American Freshwater Fishes. Ithaca and London, UK: Comstock Publishing Associates.

Huyse T and Volckaert FAM (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. PubMed

Kennedy CR (1994) The ecology of introductions. In Pike AW and Lewis JW (eds), Parasitic Diseases of Fish. Tresaith, Wales: Samara Publishing Ltd., pp. 189–208.

Kritsky DC and Mizelle JD (1968) Studies on monogenetic trematodes. XXXV. Some new and previously described North American species of Gyrodactylus. American Midland Naturalist 79, 205–215. 10.2307/2423166. DOI

Kumar S, Stecher G, Li M, Knyaz C and Tamura K (2018) MEGA X: molecular evolutionary Genetics analysis across computing platforms. Molecular Biology and Evolution 35, 1547–1549. PubMed PMC

Kuusela J, Ziętara MS 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.

Kvach Y, Ondračková M, Janáč M and 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, Seifertová M and Hulak B (2019) Gyrodactylus ginestrae n. sp. (Monogenea: Gyrodactylidae), a parasite of the big-scale sand smelt, Atherina boyeri Risso, 1810 (Actinopterygii: Atherinidae) from the Black Sea. Parasitology Research 118, 3315–3325. PubMed

Leis E, Easy R and Cone D (2018) Supplemental diagnosis of Gyrodactylus fairporti Van Cleave, 1921 (Monogenea) from 1 month old black bullhead (Ameirus melas) in riverside pools in Wisconsin. Parasitology Research 117, 1265–1269. PubMed

Leis E, Leblanc R, Easy R, Dort H and Cone D (2020) Supplemental diagnosis of Gyrodactylus nebulosus Kritsky and Mizelle, 1968 (Monogenea) on 0+ age Ameirus nebulosus (Siluriformes) considered for commercial grow-out in Southwestern Nova Scotia, Canada. Parasitology Research 119, 1149–1153. PubMed

Littlewood DTJ, Rohde K and Clough KA (1997) Parasite speciation within or between host species? Phylogenetic evidence from site-specific polystome monogeneans. International Journal for Parasitology 27, 1289–1297. PubMed

Lusk S, Lusková V and Hanel L (2011) Alien fish species in the Czech Republic and their impact on the native fish fauna. Folia Zoologica 59, 57–72.

Lymbery AJ, Morine M, Kanani HG, Beatty SJ and 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

MacLeod CJ, Paterson AM, Tompkins DM and Duncan RP (2010) Parasite lost – do invaders miss the boat or drown on arrival? Ecology Letters 13, 516–527. PubMed

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.

Matějusová I, Gelnar M, McBeath AJA, Collins CM and Cunningham CO (2001) Molecular markers for gyrodactylids (Gyrodactylidae: Monogenea) from five fish families (Teleostei). International Journal for Parasitology 31, 738–745. PubMed

Mo TA (1991) Variations of opisthaptoral hard parts of Gyrodactylus salaris Malmberg 1957 Monogenea Gyrodactylidae on parr of Atlantic salmon Salmo salar L. in laboratory experiments. Systematic Parasitology 20, 11–19.

Mo TA (1993) Seasonal variations of the opisthaptoral hard parts of Gyrodactylus derjavini Mikailov, 1975 (Monogenea: Gyrodactylidae) on brown trout Salmo trutta L. parr and Atlantic salmon S. salar L. parr in the River Sandvikselva, Norway. Systematic Parasitology 26, 225–231.

Musil J, Jurajda P, Adámek Z, Horký P and Slavík O (2010) Non-native fish introductions in the Czech Republic – species inventory, facts and future perspectives. Journal of Applied Ichthyology 26, 38–45.

Muzzal PM and Whelan G (2011) Parasites of fish from the Great Lakes: a synopsis and review of the literature, 1871–2010. Great Lakes Fishery Commission Miscellaneous Publication 2011-01.

Nitta M and Nagasawa K (2015) An alien monogenean, Ligictaluridus pricei (Platyhelminthes: Ancyrocephalidae), parasitic on the channel catfish Ictalurus punctatus (Actinopterygii: Siluriformes: Ictaluridae) in Japan. Species Diversity 20, 95–102.

Paladini G, Huyse T and Shinn AP (2011) Gyrodactylus salinae n.sp. (Platyhelminthes: Monogenea) infecting the south European toothcarp Aphanius fasciatus (Valenciennes) (Teleostei, Cyprinodontidae) from a hypersaline environment in Italy. Parasites & Vectors 4, 100. PubMed PMC

Plaisance L, Rousset V, Morand S and Littlewood DTJ (2008) Colonization of Pacific islands by parasites of low dispersal ability: phylogeography of two monogenean species parasitizing butterflyfishes in the South Pacific Ocean. Journal of Biogeography 35, 76–87.

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.

Razo-Mendivil U, García-Vásquez A and Rubio-Godoy M (2016) Spot the difference: two cryptic species of Gyrodactylus von Nodrmann, 1832 (Platyhelminthes: Monogenea) infecting Astyanax aeneus (Actinopterygii, Characidae) in Mexico. Parasitology International 65, 389–400. PubMed

Rokicka M, Lumme J and Ziętara MS (2007) Identification of Gyrodactylus ectoparasites in Polish salmonid farms by PCR-RFLPof the nuclear ITS segment of ribosomal DNA (Monogenea: Gyrodactylidae). Acta Parasitologica 52, 185–195.

Rutkayová J, Biskup R, Harant R, Šlechta V and Koščo J (2013) Ameiurus melas (black bullhead): morphological characteristics of new introduced species and its comparison with Ameiurus nebulosus (brown bullhead). Reviews in Fish Biology and Fisheries 23, 51–68.

Shinn AP, Hansen H, Olstad K, Bachmann L and 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 and Bron JE (2010) GyroDb. World Wide Web electronic publication. http://www.gyrodb.net, version (06/2010).

Spillman CJ (1961) Faune de France. No. 65, Poissons d'Eau Douce. Paris, France: Éditions Paul Lechevalier.

Vancheva N, Bobeva A, Pehlivanov L, Stefanov T and 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 first record of Gyrodactylus nebulosus in the Palaearctic. Parasitology Research 119, 2105–2112. PubMed

Vanhove MPM, Tessens B, Shoelinck C, Jondelius U, Littlewood DTJ, Artois T and Huyse T (2013) Problematic barcoding in flatworms: a case-study on monogeneans and rhabdocoels (Platyhelminthes). ZooKeys 365, 355–379. PubMed PMC

Walter RP, Gnyra ES, Söderberg LI and Heath DD (2014) Rapid genetic identification of brown bullhead (Ameiurus nebulosus), black bullhead (Ameiurus melas) and their hybrids. Conservation Genetics Resources 6, 507–509.

Xavier R, Faria PJ, Pladini G, van Oosterhout C, Johnson M and Cable J (2015) Evidence for cryptic speciation in directly transmitted gyrodactylid parasites of Trinidadian guppies. PLoS ONE 10, e0117096. PubMed PMC

Ziętara MS and Lumme J (2002) Speciation by host switch and adaptive radiation in a fish parasite genus Gyrodactylus (Monogenea, Gyrodactylidae). Evolution 56, 2445–2458. PubMed

Ziętara MS 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. 10.1023/A:1023938415148. PubMed DOI

Intraspecific variation in Gyrodactylus mediotorus and G. crysoleucas (Gyrodactylidae) from Nearctic shiners (Leuciscidae): evidence for ongoing speciation, host-switching, and parasite translocation

Comparative Analysis of Parasite Load on Recently Established Invasive Pumpkinseed Lepomis gibbosus (Actinopterygii: Centrarchidae) in Europe

First data on parasites of the invasive brown bullhead Ameiurus nebulosus (Siluriformes: Ictaluridae) in Ukraine

Revealing the hidden diversity of Gyrodactylus communities (Monogenea, Gyrodactylidae) from Nearctic Catostomidae and Leuciscidae fish hosts (Teleostei, Cypriniformes), with descriptions of ten new species

The parasites of a successful invader: monogeneans of the Asian topmouth gudgeon Pseudorasbora parva, with description of a new species of Gyrodactylus