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Endohelminths of marine, anadromous, and freshwater three-spined sticklebacks Gasterosteus aculeatus Linnaeus, 1758 (Perciformes: Gasterosteidae) in the White Sea

Published online by Cambridge University Press:  06 October 2025

Andrey Logvinenko Open the ORCID record for Andrey Logvinenko [Opens in a new window] ,
Ilya Gordeev Open the ORCID record for Ilya Gordeev [Opens in a new window] ,
Vyacheslav Gorbach Open the ORCID record for Vyacheslav Gorbach [Opens in a new window]  and
Sergey Sokolov Open the ORCID record for Sergey Sokolov [Opens in a new window]
Andrey Logvinenko
Affiliation:
Department of Invertebrate Zoology, Faculty of Biology, Lomonosov Moscow State University , Moscow, Russia White Sea Biological Station, Faculty of Biology, Lomonosov Moscow State University , Moscow, Russia
Ilya Gordeev*
Affiliation:
Department of Invertebrate Zoology, Faculty of Biology, Lomonosov Moscow State University , Moscow, Russia Pacific Salmon Department, Russian Federal Research Institute of Fisheries and Oceanography , Moscow, Russia
Vyacheslav Gorbach
Affiliation:
Department of Zoology and Ecology, Petrozavodsk State University, Petrozavodsk, Russia
Sergey Sokolov
Affiliation:
Center of Parasitology of the Severtsov Institute of Ecology and Evolution of RAS , Moscow, Russia
*
Corresponding author: Ilya Gordeev; Email: gordeev_ilya@bk.ru
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Abstract

This study investigates the endohelminth parasites of three-spined stickleback, Gasterosteus aculeatus, across marine, anadromous, and freshwater populations in the White Sea (Russia). A total of 241 sticklebacks were collected in Velikaya Salma Strait during 2022–2024. Thirteen helminth species were identified using morphological and molecular methods. Genetic analysis confirmed the presence of Anisakis simplex sensu stricto, Hysterothylacium aduncum, Phyllodistomum folium, Brachyphallus crenatus, and Alloopistholecithum cf. salmonis. We identified variability in parasite communities between 2022+2023 and 2024 both within and between marine, anadromous and freshwater host populations. The most striking temporal changes were observed in the parasite communities of the anadromous stickleback population, which is probably due to the different periods of time spent by the fish in fresh water in the years studied. This study highlights differences in infection of marine, anadromous, and freshwater populations of three-spined stickleback, providing insights into host-parasite dynamics across different aquatic environments in the White Sea basin.

Keywords

parasitesinfectioneuryhaline fisharctic

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Type
Research Paper
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Journal of Helminthology , Volume 99 , 2025 , e111
Copyright
© The Author(s), 2025. Published by Cambridge University Press

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References

Altukhov, KA, Mikhailovskaya, AA, Mukhomediyarov, FB, Nadezhdin, VM, Novikov, PI and Palenichko, ZG (1958) Fishes of the White Sea. Petrozavodsk: State Publishing House of the Karelian ASSR.Google Scholar
Azovsky, AI, Naumov, AD and Savchenko, ON (2023) Long-Term Dynamics of Subarctic Intertidal Macrofauna: Common Trends and the Role of Local Environment. Estuaries and Coasts 46, 740–756.CrossRefGoogle Scholar
Banister, K (1986) Gasterosteidae. In Whitehead, PJP, Bauchot, M-L, Hureau, J-C, Nielsen, J and Tortonese, E (eds) Fishes of the North-Eastern Atlantic and the Mediterranean. Vol. 2. Paris, UNESCO, pp. 640–643.Google Scholar
Bao, M, Cipriani, P, Giulietti, L, Alam, MA, Palomba, M, Mattiucci, S and Levsen, A (2022) Ascaridoid nematodes infecting commercially important marine fish and squid species from Bangladesh waters in the Bay of Bengal. Food and Waterborne Parasitology 27, e00157.CrossRefGoogle ScholarPubMed
Barskaya, YuYu, Ieshko, EP and Novohatskaya, OV (2005) Formation of the parasitofauna of pink salmon Oncorhynchus gorbuscha (Walbaum, 1792) under acclimatisation conditions. In Problems of study, rational use and protection of the White Sea resources. Materials of IX International Conference 11-14 October 2004. Petrozavodsk, pp. 39–43.Google Scholar
Bek, TA, Kosobkova, KN, Pantyulin, AN, Pertsova, NM, Semenova, NL, Sharnaud, NP and Shcherbakov, FA (1988) Complex studies of the fauna of the White Sea. Biologiya Okeana, Moscow: Nauka, pp. 6–15.8.Google Scholar
Bell, MA (2001) Lateral plate evolution in the threespine stickleback: Getting nowhere fast. In Hendry, AP, Kinnison, MT (eds) Microevolution Rate, Pattern, Process. Contemporary Issues in Genetics and Evolution. Volume 8. Dordrecht: Springer, pp. 445–461.Google Scholar
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.CrossRefGoogle Scholar
Bykhovskaya-Pavlovskaya, IE (1985) Fish Parasites: Manual. Leningrad: Nauka.CrossRefGoogle Scholar
Chappell, LH (1969) The parasites of the three-spined stickleback Gasterosteus aculeatus L. from a Yorkshire pond. II. Variation of the parasite fauna with sex and size of fish. J. Fish Biol. 1, 339–347.CrossRefGoogle Scholar
Dartnall, HJG and Walkey, M (1979) Parasites of marine sticklebacks. J. Fish Biol. 14, 471–474.CrossRefGoogle Scholar
De Lisle, SP and Bolnick, DI (2021) Male and female reproductive fitness costs of an immune response in natural populations. Evolution 75(10) 2509–2523.10.1111/evo.14266CrossRefGoogle ScholarPubMed
Dogiel, VA and Petrushevskii, GK (1935) Experience of ecological study of parasite fauna of White Sea salmon. In Voprosy ecologii I biotsenologii. Volume 2. Leningrad, pp. 137–169.Google Scholar
Frimeth, JP (1987) A survey of the parasites of nonanadromous and anadromous brook charr (Salvelinus fontinalis) in the Tabusintac River, New Brunswick, Canada. Canadian Journal of Zoology 65, 1354–1362.CrossRefGoogle Scholar
Garmash, MV (2019) Helminth fauna of the three-spine stickleback Gasterosteus aculeatus in some water bodies of the Kola Peninsula. In XVIII International Scientific Conference of Students and Postgraduates ‘Problems of the Arctic Region’ Murmansk, 15 May 2019. Conference Proceedings. Murmansk, pp. 28–32.Google Scholar
Gibson, DI (1996) Guide to the Parasites of Canadian Fishes. Ottawa: NRC Research Press, Part IV. Trematoda.Google Scholar
Gibson, DI, Jones, A and Bray, RA (2002) Keys to the Trematoda, Volume 1. Berlin: CABI Publishing.CrossRefGoogle Scholar
Grozdilova, TA (1989) Results of the study of parasite fauna of juvenile herring of the Kandalaksha Bay. Trudy Zoologitcheskogo instituta AN SSSR 203, 89–95.Google Scholar
Hanek, G and Molnar, K (1974) Parasites of freshwater and anadromous fishes from Matamek River system, Quebec. J. Fish. Res. Board Can. 31, 1135–1139.10.1139/f74-129CrossRefGoogle Scholar
Hanek, G and Threlfall, W (1970) Parasites of the threespine stickleback (Gasterosteus aculeatus) in Newfoundland and Labrador. J. Fish. Res. Board Can. 27, 901–907.10.1139/f70-096CrossRefGoogle Scholar
Hernández-Orts, JS, Scholz, T, Brabec, J, Kuzmina, T and Kuchta, R (2018) Does the number of genital organs matter? Case of the seal tapeworm Diphyllobothrium (syn. Diplogonoporus) tetrapterum (Cestoda: Diphyllobothriidea). Canadian Journal of Zoology 96, 193–204.CrossRefGoogle Scholar
Højgaard, DP, Steingrund, P and Bristow, G (2008) Parasites of three-spined stickleback, Gasterosteus aculeatus L., from Faroe Islands. Fróðskaparrit 56, 150–162.Google Scholar
Ivanova, N, Dewaard, JR and Hebert, PDN (2006a) An inexpensive, automation-friendly protocol for recovering high-quality DNA. Molecular Ecology Notes 6, 998–1002.10.1111/j.1471-8286.2006.01428.xCrossRefGoogle Scholar
Ivanova, N, Grainger, C and Hajibabaei, M (2006b) Glass fiber DNA extraction: a new inexpensive method for high throughput DNA isolation. CCDB Advances Methods Release 3. Guelph.Google Scholar
Jones, A, Bray, RA and Gibson, DI (2005) Keys to the Trematoda, Volume 2. Wallingford: CABI Publishing.Google Scholar
Josten, N, Detloff, KC and Zander, CD (2009) Analysis of a parasite supra community from the Flensburg Fjord. Parasitol. Res. 104, 449–461.10.1007/s00436-008-1218-7CrossRefGoogle ScholarPubMed
Kalbe, M, Wegner, KM and Reusch, TBH (2002) Dispersion patterns of parasites in 0+ year threespined sticklebacks: a cross population comparison. J. Fish Biol. 60, 1529–1542.Google Scholar
Klimpel, S, Kuhn, T, Münster, J, Dörge, DD, Klapper, R and Kochmann, J (2019) Parasites of Marine Fish and Cephalopods: A Practical Guide. Cham: Springer.CrossRefGoogle Scholar
Krupenko, D, Gonchar, A, Krapivin, V, Kremnev, G, Skobkina, O and Efeykin, B (2025) Complex species structure of Lecithaster salmonis (Digenea: Lecithasteridae), a fish parasite in the Arctic and Pacific Northwest. Journal of Helminthology 99, e4.CrossRefGoogle ScholarPubMed
Krupenko, D, Kremnev, G, Skobkina, O, Gonchar, A, Uryadova, A and Miroliubov, A (2022) Lecithaster (Lecithasteridae, Digenea) in the White Sea: an unnoticed guest from the Pacific? Journal of Helminthology 96, e43, 1–10.CrossRefGoogle Scholar
Kudryavtseva, VA, Belevich, TA and Zhitina, LS (2017) Diatoms in the ice of Velikaya Salma strait, the White Sea, before the spring algal bloom. Moscow University Biological Sciences Bulletin 72, 52–58.10.3103/S0096392517020080CrossRefGoogle Scholar
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, 1547–1549.10.1093/molbev/msy096CrossRefGoogle ScholarPubMed
Lajus, DL, Golovin, PV, Zelenskaia, AE, Demchuk, AS, Dorgham, AS, Ivanov, MV, Ivanova, TS, Murzina, SA, Polyakova, NV, Rybkina, EV and Yurtseva, AO (2020) Threespine stickleback of the White Sea: population characteristics and role in the ecosystem. Contemporary Problems of Ecology 13, 132–145.CrossRefGoogle Scholar
Lebedeva, DI, Zaitsev, DO, JaI, Alekseeva and Makhrov, AA (2023) Metazoan parasites of two stickleback species at the Solovetsky Archipelago (White Sea). Marine Biological Journal 8, 33–46.Google Scholar
Lester, RJG (1974) Parasites of Gasterosteus aculeatus near Vancouver, British Columbia. Syesis 7, 195–200Google Scholar
Llorens, C, Arcos, SC, Robertson, L, Ramos, R, Futami, R, Soriano, B, Ciordia, S, Careche, M, González-Muñoz, M, Jiménez-Ruiz, Y, Carballeda-Sangiao, N, Moneo, I, Albar, JP, Blaxter, M and Navas, A (2018) Functional insights into the infective larval stage of Anisakis simplex s.s., Anisakis pegreffii and their hybrids based on gene expression patterns. BMC Genomics 19, 592.10.1186/s12864-018-4970-9CrossRefGoogle ScholarPubMed
Logvinenko, AD, Gordeev, II, Ekimova, IA and Sokolov, SG (2024) Helminths of three species of White Sea fishes. Parasitology Research 123, 39.CrossRefGoogle Scholar
Logvinenko, AD, Gordeev, II and Biserova, NM (2025) The first record of Rockacestus piriei (Cestoda: Phylobothriidea) in the White Sea. In White Sea Student Scientific Session of SPbSU - 2025. Theses of reports. Saint-Petersburg: Svoyo Izdatelstvo, p. 60.Google Scholar
Malakhova, RP (1972) Parasite fauna of salmon Salmo salar L., kumzha Salmo trutta L., pink salmon Oncorhynchus gorbusha (Walb.) and whitefish Coregonus lavaretus Pidschian n. pidschianoides Pravdin in the White Sea basin. In Lososevye (Salmonidae) Karelii. No. 1. Petrozavodsk, pp. 21–26.Google Scholar
Mamayev, YuL and Oshmarin, PG (1963) Peculiarities of distribution of some helminths of Far Eastern salmonid fishes. In Parasiticheskiye chervy zhivotnyh Prymorya I Tichogo okeana. Moscow, AN USSR, pp. 114–127.Google Scholar
Mattiucci, S and Nascetti, G (2008) Advances and trends in the molecular systematics of anisakid nematodes, with implications for their evolutionary ecology and host-parasite co-evolutionary processes. Advances in Parasitology 66, 47–148.CrossRefGoogle ScholarPubMed
Mitenev, VK (1977) Fish parasite fauna of the Pyalitsa River. In Biology of commercial fishes of inland water bodies of the northern part of the European territory of the USSR. Murmansk, pp. 59–76.Google Scholar
Mitenev, VK and Shulman, BS (2005) Parasite fauna in Sticklebacks (Gasterosteidae) from water bodies of the Kola region. Parasitologiya 39, 16–24.Google ScholarPubMed
Moravec, F (1994) Parasitic nematodes of freshwater fishes of Europe. Praha, Academia.Google Scholar
Morgan, JAT and Blair, D (1995) Nuclear rDNA ITS sequence variation in the trematode genus Echinostoma: an aid to establishing relationships within the 37-collar-spine group. Parasitology 111, 609–615.10.1017/S003118200007709XCrossRefGoogle ScholarPubMed
Morozińska-Gogol, J (1999) Dynamics of select parasite infestation of the three-spined stickleback in dependence on the place of catching in the southern Baltic. Baltic Coastal Zone 3, 77–88.Google Scholar
Morozińska-Gogol, J (2006) A checklist of parasites recorded on sticklebacks (Actinopterygii: Gasterosteidae) from Poland. Parasitol. Int. 55, 69–73.CrossRefGoogle ScholarPubMed
Mozgovoy, AA (1953) Fundamentals of nematodology, Vol. II, Pt 2. Moscow, Izdatelstvo AN SSSR.Google Scholar
Muus, BJ and Nielsen, JG (1999) Sea fish. Hedehusene, Denmark, Scandinavian Fishing Year Book.Google Scholar
Nikolaev, KE, Fedorov, DD, Vinogradova, AA, Levakin, IA and Galaktionov, KV (2023) No time to relax: age-dependent infectivity of cercariae in marine coastal ecosystems. Journal of Helminthology 97, e102.10.1017/S0022149X2300086XCrossRefGoogle ScholarPubMed
Nikolaev, KE, Levakin, IA and Galaktionov, KV (2020) Seasonal dynamics of trematode infection in the first and the second intermediate hosts: A long-term study at the subarctic marine intertidal. Journal of Sea Research 164, 101931.10.1016/j.seares.2020.101931CrossRefGoogle Scholar
Nikolsky, GV (1950) Private Ichthyology. Moscow: State Publishing House ‘Sovietskaya nauka’.Google Scholar
Oksanen, J, Blanchet, FG, Friendly, M, Kindt, R, Legendre, P, McGlinn, D, Minchin, P, O’Hara, RB, Simpson, G, Solymos, P and Stevens, M (2020) Vegan community ecology package version 2.5-7 November 2020. R Project for Statistical Computing: Vienna, Austria.Google Scholar
Pertsova, NM and Kosobokova, KN (2003) Zooplankton of the White Sea: Features of the composition and structure, seasonal dynamics, and the contribution to the formation of matter fluxes. Oceanology 43, 108–122.Google Scholar
Petkevičiūtė, R, Stunžėnas, V and Stanevičiūtė, G (2004) Cytogenetic and sequence comparison of adult Phyllodistomum (Digenea: Gorgoderidae) from the three-spined stickleback with larvae from two bivalves. Parasitology 129, 771–778.10.1017/S0031182004006109CrossRefGoogle ScholarPubMed
Poulin, R, Blanar, CA, Thieltges, DW and Marcogliese, DJ (2011) The biogeography of parasitism in sticklebacks: distance habitat differences and the similarity in parasite occurrence and abundance. Ecography 34, 540–551.CrossRefGoogle Scholar
Pravdin, IF (1966) Handbook for the Study of Fishes (Primarily Freshwater). Fourth edition, revised and supplemented. Moscow, Pistchevaya promyshlennost.Google Scholar
Reimchen, TE (1992) Extended longevity in a large-bodied stickleback, Gasterosteus, population. Canadian Field Naturalist 106, 129–131.10.5962/p.356892CrossRefGoogle Scholar
Reimchen, TE and Nosil, P (2001) Ecological causes of sex-biased parasitism in threespine stickleback. Biological Journal of the Linnean Society 73(1) 51–63.Google Scholar
Rybkina, EV, Demchuk, AS, Lajus, DL, Ivanova, TS, Ivanov, MV and Galaktionov, KV (2016) Dynamics of parasite community during early ontogenesis of marine threespine stickleback, Gasterosteus aculeatus. Evolutionary Ecology Research 17, 335–354.Google Scholar
Shitikov, VK and Rosenberg, GS (2013) Randomization and bootstrap: statistical analysis in biology and ecology using R. Tol’yatti, Kassandra.Google Scholar
Shulman, SS (1956) Parasite fauna of herring, smelt and navaga of the White Sea. Trudy Karelo-Finskogo Filiala Akademii Nauk 4, 50–67.Google Scholar
Shulman, SS and Shulman-Albova, RE (1953) Parasites of Fish of the White Sea. Moscow-Leningrad: Izdatelstvo Akademii Nauk SSSR.Google Scholar
Shulman-Albova, RE (1952) Parasites of fishes of the White Sea in the area of Gridino village. Part 1. Monogenetic and digenetic suckers. Uchenye zapiski Karelo-Finskogo universiteta. Biologicheskiye nauki 4, 78–97.Google Scholar
Sokolov, SG, Atopkin, DM, Urabe, M and Gordeev, II (2019) Phylogenetic analysis of the superfamily Hemiuroidea (Platyhelminthes, Neodermata: Trematoda) based on partial 28S rDNA sequences. Parasitology 146, 596–603.10.1017/S0031182018001841CrossRefGoogle ScholarPubMed
Solonchenko, AI (1985) Development of larval stages of Bothriocephalus scorpii. Parasitology and pathology of marine organisms of the world ocean. NOAA Technical Report NMFS 25, 83–84.Google Scholar
Stunžėnas, V, Petkevičiūtė, R, Poddubnaya, LG, Stanevičiūtė, G and Zhokhov, AE (2017) Host specificity, molecular phylogeny and morphological differences of Phyllodistomum pseudofolium Nybelin, 1926 and Phyllodistomum angulatum Linstow, 1907 (Trematoda: Gorgoderidae) with notes on Eurasian ruffe as final host for Phyllodistomum spp. Parasites & Vectors 10, 286.10.1186/s13071-017-2210-9CrossRefGoogle ScholarPubMed
Terekhanova, NV, Logacheva, MD, Penin, AA, Neretina, TV, Barmintseva, AE, Bazykin, GA, Kondrashov, AS and Mugue, NS (2014) Fast evolution from precast bricks: genomics of young freshwater populations of threespine stickleback Gasterosteus aculeatus. PLoS Genetics 10, 1–13.CrossRefGoogle ScholarPubMed
Timofeeva, SV and Marasaeva, EF (1984) Parasitofauna of two forms of cod of Kandalaksha Bay of the White Sea. In Poljanskij, JI (ed) Ecological and parasitological northern seas research. Apatity, pp. 62–76.Google Scholar
Valentini, A, Mattiucci, S, Bondanelli, P, Webb, SC, Mignucci-Giannone, AA, Colom-Llavina, MM and Nascetti, G (2006) Genetic relationships among Anisakis species (Nematoda: Anisakidae) inferred from mitochondrial cox2 sequences, and comparison with allozyme data. Journal of Parasitology 92, 156–166.CrossRefGoogle ScholarPubMed
Vardić Smrzlić, I, Valić, D, Kapetanović, D, Kurtović, B and Teskeredžić, E (2012) Molecular characterisation of Anisakidae larvae from fish in Adriatic Sea. Parasitology Research 111, 2385–2391.10.1007/s00436-012-3094-4CrossRefGoogle ScholarPubMed
Usov, N, Radchenko, I, Smirnov, V and Sukhotin, A (2024) Joint seasonal dynamics of phytoplankton and zooplankton in the sub-Arctic White Sea. Marine Ecology Progress Series 732, 33–51.CrossRefGoogle Scholar
Waeschenbach, A and Littlewood, DTJ (2017) A molecular framework for the Cestoda. In Caira, J and Jensen, K (eds) Planetary Biodiversity Inventory (2008–2017): Tapeworms from the vertebrate bowels of the Earth. Lawrence: Natural History Museum, pp. 431–451.Google Scholar
Zander, CD (2007) Parasite diversity of sticklebacks from the Baltic Sea. Parasitol. Res. 100, 287–297.CrossRefGoogle ScholarPubMed