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

. 2023 Dec ; 60 (4) : 357-369. [epub] 20231231

Status PubMed-not-MEDLINE Jazyk angličtina Země Německo Médium electronic-ecollection

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid38222490

This study describes the parasite community of non-native brown bullhead, Ameiurus nebulosus (Actinopterygii: Ictaluridae), collected at three sites in the river Vistula Basin (Lake Svitiaz, Lake Pisochne, and Lake on Plastova) and one site in the river Diester Basin (Lake Stryiska), in Ukraine. Our data represent the first comprehensive study of parasite community in this fish species in Europe. Sixteen parasite taxa were found, including species co-introduced from North America and species acquired in the European range. Maximum parasite richness (13 spp.) was recorded in Lake Svitiaz situated in a Natural Protected Area, while lowest species richness (3 spp.) was observed at Lake on Plastova, an artificial pond in the city of Lviv. Three co-introduced monogenean species, Gyrodactylus nebulosus, Ligictaluridus pricei and Ligictaluridus monticellii, are recorded in Ukraine for the first time, widening the knowledge of the European distribution of these North American parasites. Metric features for hard parts of invasive and native monogeneans showed overlap in ligictalurid parasites, but slightly smaller metrics in Ukrainian G. nebulosus, possibly reflecting water temperature during fish sampling. Though prevalence and abundance of acquired parasites was relatively low, infection parameters for metacercariae of Diplostomum spp. were relatively high at Lake Svitiaz and the natural Lake Stryiska in Lviv. In two lakes in the Vistula basin, we found high prevalence and abundance of Anguillicola crassus, an Asian nematode infecting eels, possibly supporting the invasional meltdown hypothesis. Our study confirms both further spread of non-native parasites in Europe and use of non-native fish as competent hosts for local native and introduced parasites.

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Adamczyk L.H.. Contribution to the knowledge of the parasitofauna of Ictalurus nebulosus (Le Sueur, 1819) Przegląd Zool. 1973;17:358–363.

Anderson R.M., May R.M.. Regulation and stability of host-parasite population interactions: I. Regulatory processes. J Anim Ecol. 1978;47:219–247. doi: 10.2307/3933. DOI

Anderson R.M., May R.M.. Population biology of infectious diseases: Part I. Nature. 1979;280:361–367. doi: 10.1038/280361a0. PubMed DOI

Anderson R.M., May R.M.. Coevolution of hosts and parasites. Parasitology. 1982;85:411–426. doi: 10.1017/S0031182000055360. PubMed DOI

Bănăduc D., Marić S., Cianfaglione K., Afanasyev S., Somogyi D., Nyeste K., Antal L., Koščo J., Ćaleta M., Wanzenböck J., Curtean-Bănăduc A.. Stepping stone wetlands, last sanctuaries for European mudminnow: how can the human impact, climate change, and non-native species drive a fish to the edge of extinction? Sustainability. 2022;14(20):13493. doi: 10.3390/su142013493. DOI

Brooks D.R., Hoberg E.P.. How will global climate change affect parasite–host assemblages? Trends Parasitol. 2007;23:571–574. doi: 10.1016/j.pt.2007.08.016. PubMed DOI

Catford J.A., Vesk P.A., Richardson D.M., Pyšek P.. Quantifying levels of biological invasion: towards the objective classification of invaded and invasible ecosystems. Glob Change Biol. 2012;18(1):44–62. doi: 10.1111/j.1365-2486.2011.02549.x. DOI

Chechyna A.S., Malevytska M.A., Kononova N.E.. Vliyanie akklimatizatsii karlikovogo somika na yego parazitofaunu [Influence of acclimatization of brown bullhead on its parasite fauna] Reports of the Academy of Sciences of the USSR. 1953;88(1):173–175. (In Russian with English summary) PubMed

Cognetti D. E., Maktiis L.. Nuovo gyrodactylide parassita nella cavità olfattiva di Ameiurus catus L. Boll. Soc. Nat. Napoli. 1924;36:76–81.

Cribb T.H., Bray R.A.. Gut wash, body soak, blender and heat-fixation: approaches to the effective collection, fixation and preservation of trematodes of fishes. Syst Parasitol. 2010;76:1–7. doi: 10.1007/s11230-010-9229-z. PubMed DOI

de León G.P.P., Rosas-Valdez R., Aguilar-Aguilar R., Mendoza-Garfias B., Mendoza-Palmero C., García-Prieto L., Rojas-Sánchez A., Briosio-Aguilar R., Pérez-Rodríguez R., Domínguez-Domínguez O.. Helminth parasites of freshwater fishes, Nazas River basin, northern Mexico. Check List. 2010;6(1):26–35. doi: 10.15560/6.1.026. DOI

Đikanović V., Simonović P., Cakić P., Nikolić V.. Parasitofauna of allochthonous fish species in the open waters of the Danube River Basin (Serbian part) – impact on the native fish fauna. Appl Ecol Environ Res. 2018;16:6129–6142. doi: 10.15666/aeer/1605_61296142. DOI

Emde S., Rueckert S., Kochmann J., Knopf K., Sures B., Klimpel S.. Nematode eel parasite found inside acanthocephalan cysts - a “Trojan horse” strategy? Parasite Vectors. 2014;7:504. doi: 10.1186/s13071-014-0504-8. PubMed DOI PMC

Fehér E., Doszpoly A., Horváth B., Marton S., Forró B., Farkas S.L., Bányai K., Juhász T.. Whole genome sequencing and phylogenetic characterization of brown bullhead (Ameiurus nebulosus) origin ranavirus strains from independent disease outbreaks. Infect Genet Evol. 2016;45:402–407. doi: 10.1016/j.meegid.2016.10.001. PubMed DOI

Gallardo B., Clavero M., Sánchez M.I., Vilà M.. Global ecological impacts of invasive species in aquatic ecosystems. Glob Change Biol. 2016;22:151–163. doi: 10.1111/gcb.13004. PubMed DOI

Galli P., Pugachev O., Kritsky D. Guide to Monogenoidea of freshwater fish of Palaearctic and Amur regions. Milano: Ledizioni-Ledipublishing; 2010. p. 300.

Galli P., Stefani F., Benzoni F., Crosa G., Zullini A.. New records of alien monogeneans from Lepomis gibbosus and Silurus glanis in Italy. Parassitologia. 2003;45:147–149. PubMed

Georgiev B., Biserkov V., Genov T.. In toto staining method for cestodes with iron acetocarmine. Helminthologia. 1986;23:279–281.

Goedknegt M.A., Feis M.E., Wegner K.M., Luttikhuizen P.C., Buschbaum C., Camphuysen K. (C.J.), van der Meer J., Thieltges D.W.. Parasites and marine invasions: Ecological and evolutionary perspectives. J Sea Res. 2016;113:11–27. doi: 10.1016/j.seares.2015.12.003. DOI

Gozlan R.E., Britton J.R., Cowx I., Copp G.H.. Current knowledge on non-native freshwater fish introductions. J Fish Biol. 2010;76(4):751–786. doi: 10.1111/j.1095-8649.2010.02566.x. DOI

Gómez-Arreaza A., Haenni A.-L., Dunia I., Avilán L.. Viruses of parasites as actors in the parasite-host relationship: A “ménage à trois.”. Acta Trop. 2017;166:126–132. doi: 10.1016/j.actatropica.2016.11.028. PubMed DOI

Hanek G., Fernando C.H.. Monogenetic trematodes from the Bay of Quinte area, Ontario. II. Genus Gyrodactylus Nordmann, 1832. Can J Zool. 1971;49:1331–1341. doi: 10.1139/z71-199. PubMed DOI

Hermoso V., Clavero M., Blanco-Garrido F., Prenda J.. Invasive species and habitat degradation in Iberian streams: an analysis of their role in freshwater fish diversity loss. Ecol Appl. 2011;21(1):175–188. doi: 10.1890/09-2011.1. PubMed DOI

Hohenadler M.A.A., Honka K.I., Emde S., Klimpel S., Sures B.. First evidence for a possible invasional meltdown among invasive fish parasites. Sci Rep. 2018;8:15085. doi: 10.1038/s41598-018-33445-4. PubMed DOI PMC

Ivlev V.S., Protasov A.A.. Amerikanskiy som v ozeroakh Volynskoy oblasti [American catfish in the lakes of Volyn region] Priroda. 1948;8:67–68. (In Russian)

Kennerley J.A., Somveille M., Hauber M.E., Richardson N.M., Manica A., Feeney W.E.. The overlooked complexity of avian brood parasite-host relationships. Ecol Lett. 2022;25:1889–1904. doi: 10.1111/ele.14062. PubMed DOI PMC

Klassen G.J., Beverley-Burton M.. Ligictaluridus Beverley-Burton, 1984 (Monogenea: Ancyrocephalidae) from catfishes (Siluriformes: Ictaluridae) in North America with redescriptions of the type species, Ligictaluridus pricei (Mueller, 1936), and three others. Can J Zool. 1985;63:715–727. doi: 10.1139/z85-101. DOI

Kmentová N., Van Steenberge M., Thys van den Audenaerde D.F.E., Nhiwatiwa T., Muterezi Bukinga F., Mulimbwa N’sibula T., Masilya Mulungula P., Gelnar M., Vanhove M.P.M.. Co-introduction success of monogeneans infecting the fisheries target Limnothrissa miodon differs between two non-native areas: the potential of parasites as a tag for introduction pathway. Biol Invasions. 2019;21:757–773. doi: 10.1007/s10530-018-1856-3. DOI

Koinova I.B., Chorna A.K.. Lviv reservoirs: Current geo-ecological status and opportunities for its improvement. Man Environ Issues Neoecology. 2019;32:6–15. doi: 10.26565/1992-4224-2019-32-01. DOI

Kutsokon I., Kvach Y., Dykyy I., Dzyziuk N.. The first report of the brown bullhead Ameiurus nebulosus (Le Sueur, 1819) in the Dniester River drainage, Ukraine. BioInvasions Rec. 2018;7:319–324. doi: 10.3391/bir.2018.7.3.14. DOI

Kvach Y., Kutsokon Y., Janáč M., Dykyy I., Dzyziuk N., Dudliv I., Nazaruk K.. Parasites of the invasive Chinese sleeper Percсottus glenii (Actinopterygii: Odontobutidae) in the region of the first introduction of the Carpathian population. Oceanol Hydrobiol Stud. 2022;51:1–9. doi: 10.26881/oahs-2022.1.01. DOI

Kvach Y., Ondračková M., Janáč M., Jurajda P.. Methodological issues affecting the study of fish parasites. I. Duration of live fish storage prior to dissection. Dis Aquat Organ. 2016;119(2):107–115. doi: 10.3354/dao02990. PubMed DOI

Kvach Y., Ondračková M., Janáč M., Jurajda P.. Methodological issues affecting the study of fish parasites. III. Effect of fish preservation method. Dis Aquat Organ. 2018;127(3):213–224. doi: 10.3354/dao03197. PubMed DOI

Kvach Y., Ondračková M., Janáč M., Krasnovyd V., Seifertová M., Jurajda P.. Parasites of round goby, Neogobius melanostomus, currently invading the Elbe River. Oceanol Hydrobiol Stud. 2019;48:56–65. doi: 10.1515/ohs-2019-0006. DOI

Leis E., Leblanc R., Easy R., Dort H., Cone D.. Supplemental diagnosis of Gyrodactylus nebulosus Kritsky and Mizelle, 1968 (Monogenea) on 0+ age Ameiurus nebulosus (Siluriformes) considered for commercial grow-out in Southwestern Nova Scotia, Canada. Parasitol Res. 2020;119:1149–1153. doi: 10.1007/s00436-019-06598-y. PubMed DOI

Lymbery A.J., Morine M., Kanani H.G., Beatty S.J., Morgan D.L.. Co-invaders: The effects of alien parasites on native hosts. Int J Parasitol Parasites Wildl. 2014;3:171–177. doi: 10.1016/j.ijppaw.2014.04.002. PubMed DOI PMC

Malmberg G.. The excretory systems and the marginal hooks as a basis for the systematics of Gyrodactylus (Trematoda, Monogenea) Ark Zool. 1970;23:1–235.

Marcogliese D.J., Compagna S.. Diplostomatid eye flukes in young-of-the-year and forage fishes in the St. Lawrence River, Quebec. J Aquat Anim Health. 1999;11:275–282. doi: 10.1577/1548-8667(1999)011<0275:DEFIYO>2.0.CO;2. DOI

Mo T.. 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. Syst Parasitol. 1993;26:225–231. doi: 10.1007/BF00009730. DOI

Moravec F. Checklist of the metazoan parasites of fishes of the Czech Republic and the Slovak Republic (1873–2000) Prague: Academia; 2001. p. 168.

Moravec F. Parasitic nematodes of freshwater fishes of Europe. 2nd edition. Academia; Prague: 2013. p. 601.

Nedić Z., Simonović P., Nikolić V.. A note on the occurrence of Pallisentis ussuriensis (Kostylev, 1941) (Acanthocephala) from the brown bullhead (Ameiurus nebulosus) in Bosnia and Herzegovina; Book of Abstracts from 13th European Multicolloquium of Parasitology; Belgrade, Serbia. 2021. pp. 206–207. In.

Nitta M., Nagasawa K.. An alien monogenean, Ligictaluridus pricei (Platyhelminthes: Ancyrocephalidae), parasitic on the Channel catfish Ictalurus punctatus (Actinopterygii: Siluriformes: Ictaluridae) in Japan. Species Divers. 2015;20:95–102. doi: 10.12782/sd.20.1.095. DOI

Nowak M., Szczerbik P., Tatoj K., Popek W.. Non-native freshwater fishes in Poland: an overview. AACL Bioflux. 2008;1:173–191.

Ondračková M., Bartáková V., Kvach Y.. Ophiotaenia europaea Odening, 1963 (Cestoda: Onchoproteocephalidea) adopts a North American brown bullhead catfish Ameiurus nebulosus Lesueur, 1819 as intermediate/paratenic host in Europe. BioInvasions Rec. 2021;10(4):948–959. doi: 10.3391/bir.2021.10.4.19. DOI

Ondračková M., Seifertová M., Bryjová A., Leis E., Jurajda P.. Morphometric and genetic evidence for cryptic diversity in Gyrodactylus (Monogenea) infecting non-native European populations of Ameiurus nebulosus and A. melas. Parasitology. 2020;147:1700–1711. doi: 10.1017/S0031182020001195. PubMed DOI PMC

Page L.M., Burr B.M. A field guide to freshwater fishes: North America, north of Mexico (Peterson field guide) Boston: Houghton Mifflin; 1991. p. 448.

Prost M.. Fish Monogenoidea of Poland. II. Parasites of Ictalurus nebulosus (Le Sueur). Revision of genera Cleidodiscus Mueller, 1934, and Urocleidus Mueller, 1934. Acta Parasitol Pol. 1973;21:315–326.

Rechulicz J., Plaska W.. The invasive Ameiurus nebulosus (Lesueur, 1819) as a permanent part of the fish fauna in selected reservoirs in Central Europe: long-term study of three shallow lakes. Turk J Zool. 2018;42:464–474. doi: 10.3906/zoo-1710-16. DOI

Ricciardi A. Thorp J.H., Rogers D.C. Thorp and Covich’s freshwater invertebrates. 4th edition. Boston: Academic Press; 2015. Chapter 5 – Ecology of invasive alien invertebrates; pp. 83–91. (Eds.) DOI

Roman-Chiriac E. Fauna Republicii Populare Romîne, Plathelminthes, Volumul II, Fascicula 1: Clasa Monogenoidea. București: Editura Academiei Republicii Socialiste România; 1960. p. 147.

Rutkayová J., Biskup R., Harant R., Šlechta V., Koščo J.. Ameiurus melas (black bullhead): morphological characteristics of new introduced species and its comparison with Ameiurus nebulosus (brown bullhead) Rev Fish Biol Fish. 2013;23:51–68. doi: 10.1007/s11160-012-9274-6. DOI

Sarabeev V., Balbuena J.A., Desdevises Y., Morand S.. Host-parasite relationships in invasive species: macroecological framework. Biol Invasions. 2022;24:2649–2664. doi: 10.1007/s10530-022-02821-7. DOI

Schindler O. Freshwater fishes (English translation) London: Thames & Hudson; 1957. p. 243.

Simberloff D., Martin J.-L., Genovesi P., Maris V., Wardle D.A., Aronson J., Courchamp F., Galil B., García-Berthou E., Pascal M., Pyšek P., Sousa R., Tabacchi E., Vilà M.. Impacts of biological invasions: what’s what and the way forward. Trends Ecol Evol. 2013;28:58–66. doi: 10.1016/j.tree.2012.07.013. PubMed DOI

Šimková A., Plaisance L., Matějusová I., Morand S., Verneau O.. Phylogenetic relationships of the Dactylogyridae Bychowsky, 1933 (Monogenea: Dactylogyridea): the need for the systematic revision of the Ancyrocephalinae Bychowsky, 1937. Syst Parasitol. 2003;54:1–11. doi: 10.1023/A:1022133608662. PubMed DOI

Taraschewski H.. Hosts and parasites as aliens. J Helminthol. 2006;80:99–128. doi: 10.1079/JOH2006364. PubMed DOI

Torchin M., Lafferty K., Dobson A., McKenzie V.J., Kuris A.M.. Introduced species and their missing parasites. Nature. 2003;421:628–630. doi: 10.1038/nature01346. PubMed DOI

Tsaryk J., Gorban I., Holovachov O., Shydlovskyy I., Gorban L., Dykyy I., Lesnik V., Matejchyk V., Pudlyk J., Senyk M.. Ecological factors influencing biodiversity preservation in the Shatsk National Park. Acta Agrophysica. 2002:275–285.

Ulikowski D., Traczuk P., Kalinowska K.. Abundance and size structure of invasive brown bullhead, Ameiurus nebulosus (Lesueur, 1819), in a mesotrophic lake (north-eastern Poland) BioInvasions Rec. 2022;11:267–277. doi: 10.3391/bir.2022.11.1.27. DOI

Vancheva N., Bobeva A., Pehlivanov L., Stefanov T., Georgiev B.B.. 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. Parasitol Res. 2020;119:2105–2112. doi: 10.1007/s00436-020-06699-z. PubMed DOI

Vasenko O.G., Starko M.V.. Vuhor yevropeiskyi v Ukrayini: analiz mozhlyvostey zbilshennia yoho populiatsii z vrakhuvanniam vymoh mizhnarodnoyi rady z doslidzhen morya (ICES) [European eel in Ukraine: Analysis of the possibilities of its population increase taking into account the requirements of the International Council for the Exploration of the Sea (ICES)]; Zbirnyk naukovykh statei XVIII Mizhnarodnoi naukovo-praktychnoi konferentsii “Ekologichna bezpeka: problemy i shliakhy vyrishennia” [Proceedings of 18th International Scientific Conference ‘Environmental safety: problems and solutions’]; Kharkiv. September 15–16, 2022; Kharkiv: UkrNDIEP; 2022. pp. 74–81. (In Ukrainian)

Zenni R.D., Nuñez M.A.. The elephant in the room: the role of failed invasions in understanding invasion biology. Oikos. 2013;122(6):801–815. doi: 10.1111/j.1600-0706.2012.00254.x. DOI

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