Hostname: page-component-cb9f654ff-5jtmz Total loading time: 0 Render date: 2025-09-03T18:25:40.154Z Has data issue: false hasContentIssue false
  • English
  • Français

Metacercariae of Diplostomum spp. from eyes of the Bullhead Cottus koshewnikowi Gratzianov, 1907 from the northern European watershed

Published online by Cambridge University Press:  24 July 2025

D. Lebedeva Open the ORCID record for D. Lebedeva [Opens in a new window] ,
S.V. Bugmyrin Open the ORCID record for S.V. Bugmyrin [Opens in a new window] ,
D. Zaitsev Open the ORCID record for D. Zaitsev [Opens in a new window]  and
E.P. Ieshko Open the ORCID record for E.P. Ieshko [Opens in a new window]
D. Lebedeva*
Affiliation:
Institute of Biology, https://ror.org/035y1ap70 Karelian Research Centre , RAS, 11 Pushkinskaya St., 185910, Petrozavodsk, Russia
S.V. Bugmyrin
Affiliation:
Institute of Biology, https://ror.org/035y1ap70 Karelian Research Centre , RAS, 11 Pushkinskaya St., 185910, Petrozavodsk, Russia
D. Zaitsev
Affiliation:
https://ror.org/0176aa147 Petrozavodsk State University , Lenin Prospect, 185910, Petrozavodsk, Russia
E.P. Ieshko
Affiliation:
Institute of Biology, https://ror.org/035y1ap70 Karelian Research Centre , RAS, 11 Pushkinskaya St., 185910, Petrozavodsk, Russia
*
Corresponding author: D. Lebedeva; Email: daryal78@gmail.com
Get access Rights & Permissions [Opens in a new window]

Abstract

Metacercariae of Diplostomum spp. are widespread fish parasites. In this study we obtained the first data on infection of Bullhead Cottus koshewnikowi with these larvae in five rivers of northern Europe (Finland and Russia) using molecular and morphological description. Three Diplostomum spp. were revealed in the eyes of bullheads. Diplostomum spathaceum and D. mergi Lineage 3 sensu Georgieva et al. (2013) were found in the lens, while Diplostomum sp. Lineage 6 sensu Blasco-Costa et al. (2014) was found in the retina. We obtained molecular data on these three species and provided morphological characteristics of the latter two species. Partial sequences of the cytochrome c oxidase subunit 1 (cox1) and ITS1-5.8S-ITS2 were amplified for 20 isolates. Using molecular data, we ascertained the species identification and obtained new information on the life cycles of D. mergi Lineage 3 and Diplostomum sp. Lineage 6. Partial cox1 sequences were used to assess the haplotype diversity of D. mergi Lineage 3 and Diplostomum sp. Lineage 6 in the study area. Discriminant analysis showed that D. mergi Lineage 3 was morphometrically close both to the species of the lens complex (D. mergi Lineage 2, D. mergi, D. nordmanni, and D. parviventosum) and to the species from the retina (D. pungiti, D. volvens). Dimensions of Diplostomum gobiorum lay far outside the confidence interval of D. mergi Lineage 3. Our molecular and morphological data and the new information about the hosts and the distribution of these parasites are a crucial step towards elucidating the diversity and life cycles of these important parasites. The data on the infection of bullheads in the River Utsjoki (a tributary of the River Teno, Finland) with metacercariae of Diplostomum spp. offer some insights into the relationships between the introduced host and the native parasites. Infection of bullheads, which are considered invasive in the Teno River system, with metacercariae of Diplostomum spp. may lead to increased infection levels in resident fish.

Keywords

DiplostomidaeCottidaelensretinacox1ITS1-5.8S-ITS2

Information

Type
Research Paper
Information
Journal of Helminthology , Volume 99 , 2025 , e81
Copyright
© The Author(s), 2025. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Article purchase

Temporarily unavailable

References

Achatz, TJ, Martens, JR, Kostadinova, A, Pulis, EE, Orlofske, SA, Bell, JA, Fecchio, A, Oyarzún-Ruiz, P, Syrota, YY and Tkach, VV (2022) Molecular phylogeny of Diplostomum, Tylodelphys, Austrodiplostomum and Paralaria (Digenea: diplostomidae) necessitates systematic changes and reveals a history of evolutionary host switching events. International Journal of Parasitology 52, 47–63. https://doi.org/10.1016/j.ijpara.2021.06.002.CrossRefGoogle ScholarPubMed
Barskaya, YY, Ieshko, EP and Lebedeva, DI (2008) Parasites of Salmonidae Fish of Fennoscandia: Practical Guide. Petrozavodsk, KRC RAS.Google Scholar
Behrmann-Godel, J (2013) Parasite identification, succession and infection pathways in perch fry (Perca fluviatilis): New insights through a combined morphological and genetic approach. Parasitology 140, 509–520. https://doi.org/10.1017/S0031182012001989.CrossRefGoogle ScholarPubMed
Blasco-Costa, I, Faltýnková, A, Georgieva, S, Skírnisson, K, Scholz, T and Kostadinova, A (2014) Fish pathogens near the Arctic Circle: Molecular, morphological and ecological evidence for unexpected diversity of Diplostomum (Digenea: Diplostomidae) in Iceland. International Journal for Parasitology 44, 703–715. https://doi.org/10.1016/j.ijpara.2014.04.009.CrossRefGoogle ScholarPubMed
Bush, AO, Lafferty, KD, Lotz, JM and Shostak, AW (1997) Parasitology meets ecology on its own terms: Margolis et al. revisited. Journal of Parasitology 83, 575–583. https://doi.org/10.2307/3284227.CrossRefGoogle Scholar
Darriba, D, Taboada, GL, Doallo, R and Posada, D (2012) jModelTest 2: More models, new heuristics and parallel computing. Natural Methods 9, 772–772. https://doi.org/10.1038/nmeth.2109.CrossRefGoogle ScholarPubMed
Dorovskih, GN (1997) Results of the study of fishes’ parasites in river basins of the North-east of the European part of Russia. Trematodes (Trematoda). Parasitologiya 31, 550–564.Google Scholar
Ellendt, S (2016) Environmental and Genetic Determinants of Bacterial Microbiota and Parasites Associated with Cottus Across Natural Hybrid Zones. Dissertation “Dr. rer. nat.”. Christian Albrechts University of Kiel. 125 pp.Google Scholar
Evseeva, NV (2001) Parasite diversity in stone loach (Nemachilus barbatulus L.) and bullhead (Cottus gobio L.) in the urbanized ecosystem of the Lososinka River. In Ecological and parasitological studies of animals and plants of the European North. Petrozavodsk: Karelian Scientific Center of the Russian Academy of Sciences, 30–35.Google Scholar
Faltýnková, A, Georgieva, S, Kostadinova, A, Blasco-Costa, I, Scholz, T and Skírnisson, K (2014) Diplostomum von Nordmann, 1832 (Digenea: Diplostomidae) in the sub-Arctic: descriptions of the larval stages of six species discovered recently in Iceland. Systematic Parasitology 89, 195–213. https://doi.org/10.1007/s11230-014-9517-0.CrossRefGoogle ScholarPubMed
Faltýnková, A, Kudlai, O, Pantoja, C, Yakovleva, G and Lebedeva, D (2022) Another plea for ‘best practice’ in molecular approaches to trematode systematics: Diplostomum sp. clade Q identified as Diplostomum baeri Dubois, 1937 in Europe. Parasitology 149, 503–518. https://doi.org/10.1017/S0031182021002092.CrossRefGoogle ScholarPubMed
Freyhof, J, Kottelat, M and Nolte, A (2005) Taxonomic diversity of European Cottus with description of eight new species (Teleostei: Cottidae). Ichthyological Exploration of Freshwaters 16(2), 107–172.Google Scholar
Galazzo, DE, Dayanandan, S, Marcogliese, DJ and McLaughlin, JD (2002) Molecular systematics of some North American species of Diplostomum (Digenea) based on rDNA sequence data and comparisons with European congeners. Canadian Journal of Zoology 80, 2207–2217. https://doi.org/10.1139/z02-198.CrossRefGoogle Scholar
Georgieva, S, Soldánová, M, Pérez-Del-Olmo, A, Dangel, DR, Sitko, J, Sures, B and Kostadinova, A (2013) Molecular prospecting for European Diplostomum (Digenea: Diplostomidae) reveals cryptic diversity. International Journal for Parasitology 43, 57–72. https://doi.org/10.1016/j.ijpara.2012.10.019.CrossRefGoogle ScholarPubMed
Gordy, MA and Hanington, PC (2019) A fine-scale phylogenetic assessment of digenean trematodes in central Alberta reveals we have yet to uncover their total diversity. Ecology and Evolution 9, 3153–3238. https://doi.org/10.1002/ece3.4939.CrossRefGoogle ScholarPubMed
Haarder, S, Jørgensen, K, Kania, PW, Skovgaard, A and Buchmann, K (2013) Occurrence of Diplostomum pseudospathaceum Niewiadomska, 1984 and D. mergi Dubois, 1932 (Digenea: Diplostomidae) in Danish freshwater snails: ecological and molecular data, Folia Parasitologica 60, 177–180. https://doi.org/10.14411/fp.2013.020.CrossRefGoogle Scholar
Hammer, Ø, Harper, DAT and Ryan, PD (2001) PAST: Paleontological Statistics Software Package for Education and Data Analysis. Palaeontologia Electronica 4, 9. http://palaeo-electronica.org/2001_1/past/issue1_01.htm.Google Scholar
Hoogendoorn, C, Smit, NJ and Kudlai, O (2020). Resolution of the identity of three species of Diplostomum (Digenea: Diplostomidae) parasitising freshwater fishes in South Africa, combining molecular and morphological evidence. International Journal for Parasitology Parasites and Wildlife 11, 50–61. https://doi.org/10.1016/j.ijppaw.2019.12.003.CrossRefGoogle ScholarPubMed
Ieshko, EP and Shulman, BS (2001) Peculiarities of parasitofauna of young Atlantic salmon (Salmo salar L.) of the rivers of the Teno River system (Northern Finland). Parasitologiya 35, 344–352.Google Scholar
Ieshko, EP, Lebedeva, DI, Barskaya, YY, Shul’man, BS and Niemela, E (2013) Bullhead (Cottus gobio L.) invasion in the Utsjoki River (Northern Finland): Parasitological aspects. Russian Journal of Biological Invasions 4, 17–23. https://doi.org/10.1134/S2075111713010049.CrossRefGoogle Scholar
Jørgensen, L, Avundsen, PA, Gabler, HM, Halvorsen, M, Erkinaro, J and Niemela, E (1999) Spatial distribution of Atlantic salmon parr (Salmo salar L.) and bullhead (Cottus gobio L.) in lotic and lentic habitats of a diversified watercourse in Northern Fennoscandia. Fisheries Research 41, 201–211.10.1016/S0165-7836(99)00014-4CrossRefGoogle Scholar
Karvonen, A and Marcogliese, DJ (2020) Diplostomiasis (Diplostomum spathaceum and related species). In Woo PTK Leong, J-A and Buchmann, K (eds), Climate Change and Infectious Fish Diseases. Wallingford: CABI, 434–456.Google Scholar
Kirjušina, M and Vismanis, K (2007) Checklist of the parasites of fishes of Latvia. FAO Fisheries Technical Paper No. 369/3, FAO, Rome.Google Scholar
Kontula, T and Väinölä, R (2001) Postglacial colonization of Northern Europe by distinct phylogeographic lineages of the bullhead, Cottus gobio. Molecular Ecology 10(8), 1983–2002. https://10.1046/j.1365-294x.2001.01328.x.CrossRefGoogle ScholarPubMed
Kontula, T and Väinölä, R (2004) Molecular and morphological analysis of secondary contact zones of Cottus gobio in Fennoscandia: Geographical discordance of character transitions. Biological Journal of the Linnean Society 81, 535–552. https://doi.org/10.1111/j.1095-8312.2003.00298.x.CrossRefGoogle Scholar
Kottelat, M (1997) European freshwater fishes. An heuristic checklist of the freshwater fishes of Europe (exclusive of former USSR), with an introduction for non-systematists and comments on nomenclature and conservation. Biologia, Bratislava 52(Suppl. 5), 1–271.Google Scholar
Kudlai, O, Oros, M, Kostadinova, A and Georgieva, S (2017) Exploring the diversity of Diplostomum (Digenea: Diplostomidae) in fishes from the river Danube using DNA mitochondrial barcodes. Parasites & Vectors 10, 592. https://doi.org/10.1186/s13071-017-2518-5.CrossRefGoogle Scholar
Kuhn, JA, Kristoffersen, R, Knudsen, R, Jakobsen, J, Marcogliese, DJ, Locke, SA, Primicerio, R and Amundsen, P-A (2015) Parasite communities of two three-spined stickleback populations in subarctic Norway—effects of a small spatial-scale host introduction. Parasitology Research 114, 1327–1339. https://doi.org/10.1007/s00436-015-4309-2.CrossRefGoogle ScholarPubMed
Kumar, S, Stecher, G, Suleski, M, Sanderford, M, Sharma, S and and Tamura, K (2024) MEGA12: Molecular Evolutionary Genetics Analysis version 12 for adaptive and green computing Molecular Biology and Evolution 41, 1–9. https://doi.org/10.1093/molbev/msae263.CrossRefGoogle ScholarPubMed
Kvach, Y, Boldyrev, V, Lohner, R and Stepien, CA (2015) The parasite community of gobiid fishes (Actinopterygii: Gobiidae) from the Lower Volga River region. Biologia 70, 948–957. https://doi.org/10.1515/biolog-2015-0108.CrossRefGoogle Scholar
Lebedeva, DI, Chrisanfova, GG, Ieshko, EP, Guliaev, AS, Yakovleva, GA, Mendsaikhan, B and Semyenova, SK (2021) Morphological and molecular differentiation of Diplostomum spp. metacercariae from brain of minnows (Phoxinus phoxinus L.) in four populations of northern Europe and East Asia. Infection, Genetics and Evolution 92, 104911. https://doi.org/10.1016/j.meegid.2021.104911.CrossRefGoogle ScholarPubMed
Leigh, JW and Bryant, D (2015) PopART: Full-feature software for haplotype network construction. Methods in Ecology and Evolution 6, 1110–1116. https://doi.org/10.1111/2041-210X.12410.CrossRefGoogle Scholar
Lebedeva, DI, Popov, IY, Yakovleva, GA, Zaicev, DO, Bugmyrin, SV and Makhrov, AA (2022) No strict host specificity: Brain metacercariae Diplostomum petromyzifluviatilis Müller (Diesing, 1850) are conspecific with Diplostomum sp. Lineage 4 of Blasco-Costa et al. (2014). Parasitology International 91, 102654. https://doi.org/10.1016/j.parint.2022.10265.CrossRefGoogle ScholarPubMed
Locke, SA, McLaughlin, JD and Marcogliese, DJ (2010a) DNA barcodes show cryptic diversity and a potential physiological basis for host specificity among Diplostomoidea (Platyhelminthes: Digenea) parasitizing freshwater fishes in the St. Lawrence River, Canada. Molecular Ecology 19, 2813–2827. https://doi.org/10.1111/j.1365-294X.2010.04713.x.CrossRefGoogle Scholar
Locke, SA, McLaughlin, JD, Dayanandan, S and Marcogliese, DJ (2010b) Diversity, specificity and evidence of hybridization in Diplostomum spp. metacercariae in freshwater fishes is revealed by DNA barcodes and ITS sequences. International Journal for Parasitology 40, 333–343. https://doi.org/10.1016/j.ijpara.2015.07.001.CrossRefGoogle Scholar
Locke, SA, Al-Nasiri, FS, Caffara, M, Drago, F, Kalbe, M, Lapierre, AR, McLaughlin, JD, Nie, P, Overstreet, RM, Souza, GTR, Takemoto, RM and Marcogliese, DJ (2015) Diversity, specificity and speciation in larval Diplostomidae (Platyhelminthes: Digenea) in the eyes of freshwater fish, as revealed by DNA barcodes. International Journal for Parasitology 45, 841–855. https://doi.org/10.1016/j.ijpara.2015.07.001.CrossRefGoogle ScholarPubMed
Locke, SA, Drago, FB, Núñez, V, Souza, GTRE and Takemoto, RM (2020) Phylogenetic position of Diplostomum spp. from New World herons based on complete mitogenomes, rDNA operons, and DNA barcodes, including a new species with partially elucidated life cycle. Parasitology Research 119, 2129–2137. https://doi.org/10.1007/s00436-020-06713-4.CrossRefGoogle ScholarPubMed
Marcogliese, DJ and Locke, SA (2021) Infection of Diplostomum spp. in invasive round gobies in the St Lawrence River, Canada. Journal of Helminthology 95, e64. https://doi.org/10.1017/S0022149X21000559.CrossRefGoogle Scholar
Martinek, I and Hernández-Orts, JS (2023) Helminth fauna of the black goby Gobius niger L. (Gobiiformes: Gobiidae) from the Finnish Archipelago, Baltic Sea: Molecular and morphological data. Current Research in Parasitology and Vector Borne Diseases 5, 100169. https://doi.org/10.1016/j.crpvbd.2023.100169.CrossRefGoogle ScholarPubMed
Moszczynska, A, Locke, SA, McLaughlin, JD, Marcogliese, DJ and Crease, TJ (2009) Development of primers for the mitochondrial cytochrome c oxidase I gene in digenetic trematodes illustrates the challenge of barcoding parasitic helminths. Molecular Ecology Resources 9, 75–82. https://doi.org/10.1111/j.1755-0998.2009.02634.x.CrossRefGoogle ScholarPubMed
Niewiadomska, K (1987) Diplostomum paracaudum (Iles 1959), Shigin 1977 (Digenea, Diplostomidae) and its larval stages: A new record from Poland. Acta Parasitologica Polonica 31, 199– 210.Google Scholar
Niewiadomska, K (2010) Fauna słodkowodna Polski. 34A. Przywry (Trematoda).Część ogólna; Część systematyczna – Aspidogastrea, Digenea: Strigeida. Wydawnictwo Uniwersytetu Łódzkiego, Łódź.CrossRefGoogle Scholar
Niewiadomska, K and Szymański, S (1991) Host-induced variability of Diplostomum paracaudum (Iles, 1959) metacercariae (Digenea). Acta Parasitologica Polonica 36, 11– 17.Google Scholar
Niewiadomska, K and Szymański, S (1992) Host-induced variability of Diplostomum pseudospathaceum Niewiadomska, 1984 metacercariae (Digenea). Acta Parasitologica Polonica 37, 11– 17.Google Scholar
Ondračková, M, Valigurová, A, Hodová, I, Bartáková, V, Tkachenko, MY, Janáč, M and Vetešník, L (2025) Diplostomum-induced sac formation in lenses of Ameiurus Bullheads: A host defence response? Journal of Fish Diseases, e14137. https://doi.org/10.1111/jfd.14137.CrossRefGoogle ScholarPubMed
Pérez-del-Olmo, A, Georgieva, S, Pula, HJ and Kostadinova, A (2014) Molecular and morphological evidence for three species of Diplostomum (Digenea: Diplostomidae), parasites of fishes and fish-eating birds in Spain. Parasites & Vectors 7, 502. https://doi.org/10.1186/s13071-014-0502-x.CrossRefGoogle ScholarPubMed
Petrushevsky, GK (1940) Materials on parasitology of fishes of Karelia. II Parasites of fish of Lake Onega. Scientific Notes of the Leningrad State Pedagogical Institute 30, 133–186.Google Scholar
Pihlaja, O, Julkunen, M, Niemela, E and Erkinaro, J (2003) Changes in the density of introduced bullhead, Cottus gobio L., and its impact on juvenile Atlantic salmon, Salmo salar L., densities in a sub-Arctic salmon river in northern Finland. Fisheries Management and Ecology 5, 189–199. https://doi.org/10.1046/j.1365-2400.1998.00083.xCrossRefGoogle Scholar
Rahn, AK, Krassmann, J, Tsobanidis, K, MacColl, ADC and Bakker, TCM (2016) Strong neutral genetic differentiation in a host, but not in its parasite. Infection, Genetics and Evolution 44, 261–271. https://doi.org/10.1016/j.meegid.2016.07.011.CrossRefGoogle Scholar
Rambaut, A (2012) FigTree v1. 4. Molecular evolution, phylogenetics and epidemiology. Available at: https://github.com/rambaut/figtree/releases (accessed 1 January 2025).Google Scholar
Ronquist, F, Teslenko, M, Van Der Mark, P, Ayres, DL, Darling, A, Höhna, S and Huelsenbeck, JP (2012) MrBayes 3.2: Efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology 61, 539–542. https://doi.org/10.1093/sysbio/sys029.CrossRefGoogle ScholarPubMed
Rumyantsev, EA, Ieshko, EP and Shulman, BS (2003) Development of parasitofauna in freshwater sculpin (Cottus gobio L.) (Pisces: Cottidae). Parazitologiya 37, 140–144.Google Scholar
Rumyantsev, EA (2007) Fish Parasites in Lakes of the European North (Fauna, Ecology, Evolution). Petrozavodsk: KRC RAS.Google Scholar
Schwelm, J, Georgieva, S, Grabner, D, Kostadinova, A and Sures, B (2021) Molecular and morphological characterisation of Diplostomum phoxini (Faust, 1918) with a revised classification and an updated nomenclature of the species-level lineages of Diplostomum (Digenea: Diplostomidae) sequenced worldwide. Parasitology 148, 1648–1664, https://doi.org/10.1017/S0031182021001372.CrossRefGoogle Scholar
Shorthouse, DP (2010) SimpleMappr, an online tool to produce publication-quality point maps. Available at https://www.simplemappr.net (accessed 12 February 2025).Google Scholar
Selbach, C, Soldánová, M, Georgieva, S, Kostadinova, A and Sures, B (2015) Integrative taxonomic approach to the cryptic diversity of Diplostomum spp. in lymnaeid snails from Europe with a focus on the ‘Diplostomum mergi’ species complex. Parasitу & Vectors 8, 300. https://doi.org/10.1186/s13071-015-0904-4.CrossRefGoogle Scholar
Seppala, T, Chubb, JC, Niemela, E and Valtonen, ET (2007). Introduced Bullheads Cottus gobio and Infection with Plerocercoids of Schistocephalus cotti in the Utsjoki, an Arctic River in Finland. Journal of Fish Biology 70, 1865–1876. https://doi.org/10.1111/j.1095-8649.2007.01462.x.CrossRefGoogle Scholar
Shigin, AA (1969) On the life cycle and species independence of Diplostomum gobiorum Shigin, 1965 (Trematoda, Diplostomum). Trudy Gel’mintologicheskoi Lab. Akad. Nauk SSSR 20, 176–190.Google Scholar
Shigin, AA (1986) Trematodes in the Fauna of the USSSR: The Genus Diplostomum. Metacercariae. Moscow: Nauka.Google Scholar
Shigin, AA (1993) Trematodes of the fauna of Russia and neighbouring regions. Genus Diplostomum, Adults. Nauka, Moscow.Google Scholar
Shigin, AA, Chupilko, SV and Klochkova, EA (1985) Towards knowledge of the life cycle of Diplostomum parviventosum (Trematoda, Diplostomidae) – parasites of fish-eating birds. Trudy Gel’mintologicheskoi Lab. Akad. Nauk SSSR 33, 157–180.Google Scholar
Shulman, BS, Ieshko, EP, Shchurov, IL, Yonsen, BO and Yensen, AJ (2004) Peculiarities of the parasite fauna of the landlocked Atlantic Salmon Salmo salar in the basin of Namsen River. Parasitologiya 38, 94–97.Google Scholar
Shulman, SS (1962) Parasite fauna of fish of Syamozero lakes group. Proceedings of Syamozero complex expedition 2, 173–244.Google Scholar
Shulman, SS, Malakhova, RP and Rybak, VF (1974) Comparative-Ecological Analysis of Fish Parasites of Lakes of Karelia. Leningrad: Nauka.Google Scholar
Shulman, BS, Ieshko, EP, Shchurov, IL, Yonsen, BO and Yensen, AJ (2005) Peculiarities of the parasite fauna of the landlocked Atlantic Salmon Salmo salar of the Vefsna River (Northern Norway). Salmonid Fishes of Eastern Fennoscandia 191–194.Google Scholar
Sideleva, VG, Naseka, AM, Nowak, M and Palandačić, A (2019) The finding of holotype and redescription of Cottus microstomus Heckel 1837 (Cottidae). Ichthyological Research 66, 249–257. https://doi.org/10.1007/s10228-018-00676-4.CrossRefGoogle Scholar
Sideleva, V, Kesminas, V and Zhidkov, Z (2022) A new species of genus Cottus (Scorpaeniformes, Cottidae) from the Baltic Sea Basin and its phylogenetic placement. European Journal of Taxonomy 834, 38–57. https://doi.org/10.5852/ejt.2022.834.1897.CrossRefGoogle Scholar
Sokolov, SG, Ieshko, EP and Lebedeva, DI (2023) Resurrection of Diplostomum numericum Niewiadomska, 1988 (Digenea, Diplostomatoidea: Diplostomidae) based on novel molecular data from the type-host. Diversity 15, 840. https://doi.org/10.3390/d15070840.CrossRefGoogle Scholar
Soldánová, M, Georgieva, S, Rohacova, J, Knudsen, R, Kuhn, JA, Henriksen, EH, Siwertsson, A, Shaw, JC, Kuris, AM, Amundsen, PA, Scholz, T, Lafferty, KD and Kostadinova, A (2017) Molecular analyses reveal high species diversity of trematodes in a sub-Arctic lake. International Journal for Parasitology 47, 327–345. https://doi.org/10.1016/j.ijpara.2016.12.008.CrossRefGoogle Scholar
Sudarikov, VE and Shigin, AA (1965) On the methods for working with metacercariae of the Strigeidida. Trudy Gel’mintologicheskoi Lab. Akad. Nauk SSSR 15, 158–166.Google Scholar
Valtonen, ET, Hakalahti-Sirén, T, Karvonen, A and Pulkkinen, K (2012) Suomen kalojen loiset. Tampere: Gaudeamus Oy.Google Scholar
Villesen, P (2007) FaBox: An online toolbox for fasta sequences. Molecular Ecology Notes 7, 965–968. https://doi.org/10.1111/j.1471-8286.2007.01821.x. https://laji.fi/en; https://laji.fi/en/taxon/MX.5090558; Cottus koshewnikowi | Overview | Finnish Biodiversity Info Facility (assessed 14 May 2025)CrossRefGoogle Scholar
Yushkov, VF and Ivashevsky, GA (1999). Parasites of vertebrate animals of the European North-East of Russia. Catalogue. Ural Branch. Komi Scientific Center. Syktyvkar.Google Scholar
Supplementary material: File

Lebedeva et al. supplementary material

Lebedeva et al. supplementary material
Download Lebedeva et al. supplementary material(File)
File 49.3 KB