Skip to main content
Log in

Helminths of three species of White Sea fishes

  • Research
  • Published:
Parasitology Research Aims and scope Submit manuscript

Abstract

Parasitic fauna of the White Sea cod, Gadus morhua marisalbi; the navaga, Eleginus nawaga; and the shorthorn sculpin, Myoxocephalus scorpius, in the White Sea was repeatedly studied, but no large-scale parasitological surveys have been made in the recent three decades. To fill this gap, we conducted a survey of the helminths of these three fish species at the White Sea Biological Station (Karelia, Russia) of the Lomonosov Moscow State University in August 2021. The navaga (50 specimens studied) was found to be infected with 13 species of helminths; the White Sea cod (50 specimens), with 12 species; and the shorthorn sculpin (21 specimens), with 13 species. Plerocercoids of Diphyllobothrium schistochilus and third-stage juveniles of Pseudoterranova bulbosa were recorded in the White Sea for the first time. The helminth infracommunities of the navaga and the White Sea cod were closer in structure to each other than to those of the shorthorn sculpin. In general, the levels of helminth infection of the White Sea cod, the navaga, and shorthorn sculpin have been consistently high over 85 years of observations in the White Sea, but long-term trends in the abundance of some helminth species were multidirectional.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

Data availability

Not applicable.

References

  • Arai HP (1989) Guide to the parasites of fishes of Canada. Ottawa, NRC Research Press, Part III. Acanthocephala

    Google Scholar 

  • Banzai-Umehara A, Suzuki M, Akiyama T, Ooi H-K, Kawakami Y (2016) Invalidation of Diphyllobothrium hottai (Cestoda: Diphyllobothriidae) based on morphological and molecular phylogenetic analyses. Par Int 65:459–462. https://doi.org/10.1016/j.parint.2016.06.011

    Article  Google Scholar 

  • Bao M, Cipriania P, Giuliettia L, Roiha IS, Paoletti M, Palomba M, Levsen A (2020) Air-dried stockfish of Northeast Arctic cod do not carry viable anisakid nematodes. Food Control 116:1–7. https://doi.org/10.1016/j.foodcont.2020.107322

    Article  CAS  Google Scholar 

  • Berger VJ, Galaktionov KV, Naumov AD (2001) White Sea ecology and environment. Derzavets Publisher, St. Petersburg – Tromsø

  • Bush AO, Lafferty KD, Lotz JM, Shostak AW (1997) Parasitology meets ecology on its own terms: Margolis et al. revisited. J Parasitol 83:575–583. https://doi.org/10.2307/3284227

    Article  CAS  PubMed  Google Scholar 

  • Bykhovskaya-Pavlovskaya IE (1985) Fish parasites: manual. Nauka, Moscow

    Book  Google Scholar 

  • Bykhovsky BE (1948) On the monogenetic flukes of navaga. Proc Mar Biol Station Karelo-Finnish State Univ 1:140–144

    Google Scholar 

  • Cobb NA (1888) Neue Parasitische Nematoden. Arch Naturgesch 55:149–159

    Google Scholar 

  • Cohen DM, Inada T, Iwamoto T, Scialabba N (1990) FAO species catalogue. Gadiform fishes of the world (Order Gadiformes). An annotated and illustrated catalogue of cods, hakes, grenadiers and other gadiform fishes known to date. FAO Fish Synop 125(10):442

  • Di Deco MA, Orecchia P, Paggi L, Petrarca V (1994) Morphometric stepwise discriminant analysis of three genetically identified species within Pseudoterranova decipiens (Krabbe, 1878) (Nematoda: Ascaridida). Syst Par 29:81–88

    Article  Google Scholar 

  • Druzhinin PV, Kurilo AE, Moroshkina MV (2022) Development of the White Sea coast municipalities. Probl Territory’s Dev 26:7–22. https://doi.org/10.15838/ptd.2022.2.118.2

    Article  Google Scholar 

  • Ershov PN (2010a) Changes in the diet of the coastal cod Gadus morhua marisalbi in the Kandalaksha Gulf of the White Sea under conditions of increased abundance of three-spined stickleback Gasterosteus aculeatus. J Ichth 50:84–88. https://doi.org/10.1134/S0032945210010108

    Article  Google Scholar 

  • Ershov PN (2010b) On the food composition of the European sculpin Myoxocephalus scorpius (Linnaeus, 1758) in the Kandalaksha Bay of the White Sea. Bull St Petersburg State Univ 3(2):55–62

    Google Scholar 

  • Fedorov VV (1986) Cottidae. In: Whitehead PJP, Bauchot M-L, Hureau J-C, Nielsen J, Tortonese E (eds) Fishes of the North-eastern Atlantic and the Mediterranean. UNESCO, Paris 3:1243–1260

  • Felsenstein J (1985) Confidence limits on phylogenies: an approach using bootstrap. Evol 39:783–791

    Article  Google Scholar 

  • Fraija-Fernandez N, Waeschenbach A, Briscoe AG, Hocking S, Kuchta R, Nyman T, Littlewood DTJ (2021) Evolutionary transitions in broad tapeworms (Cestoda: Diphyllobothriidea) revealed by mitogenome and nuclear ribosomal operon phylogenetics. Mol Phyl Evol 163:107262. https://doi.org/10.1016/j.ympev.2021.107262

    Article  CAS  Google Scholar 

  • Froese R, Pauly D (eds) (2023) FishBase. Gadus macrocephalus Tilesius, 1810. Accessed through: World Register of Marine Species at: https://www.marinespecies.org/aphia.php?p=taxdetails&id=254538. Accessed 2022–12–08

  • Gibson DI (1996) Guide to the parasites of Canadian fishes. Ottawa, NRC Research Press, Part IV. Trematoda

    Google Scholar 

  • Gibson DI, Jones A, Bray RA (2002) Keys to the Trematoda V. 1. CABI Publishing

  • Hammer Ø, Harper DA, Ryan PD (2001) PAST: Paleontological statistics software package for education and data analysis. Palaeont Electron 4:9

    Google Scholar 

  • Hernández-Orts JS, Scholz T, Brabec J, Kuzmina T, Kuchta R (2018) Does the number of genital organs matter? Case of the seal tapeworm Diphyllobothrium (syn. Diplogonoporus) tetrapterum (Cestoda: Diphyllobothriidea). Can J Zool 96:193–204. https://doi.org/10.1139/cjz-2017-001

    Article  Google Scholar 

  • Hrabar J, Smodlaka H, Rasouli-Dogaheh S, Petrić M, Trumbić Ž, Palmer L, Sakamaki K, Pavelin T, Mladineo I (2021) Phylogeny and pathology of anisakids parasitizing stranded California sea lions (Zalophus californianus) in Southern California. Front Mar Science 8:636626. https://doi.org/10.3389/fmars.2021.636626

    Article  Google Scholar 

  • Ieshko EP, Korosov AV (2012) Estimation of the species richness of fish parasite fauna: an ecological approach. Printsipy Ekologii 1:28–40

    Google Scholar 

  • Ivanova N, Dewaard JR, Hebert PDN (2006a) An inexpensive, automation-friendly protocol for recovering high-quality DNA. Mol Ecol Notes 6:998–1002

    Article  CAS  Google Scholar 

  • Ivanova N, Grainger C, Hajibabaei M (2006b) Glass fiber DNA extraction: a new inexpensive method for high throughput DNA isolation. CCDB Advances, Methods Release 3

  • Izvekova EI (1964) On the nutrition of cod (Gadus morhua maris-albi Der.) In the western part of the White Sea (Great Salma). Voprosy Ikhtiologii 4:354–364

    Google Scholar 

  • Jacobus K, Marigo J, Gastal SB, Taniwaki SA, Ruoppolo V, Catão-Dias JL, Tseng F (2016) Identification of respiratory and gastrointestinal parasites of three species of pinnipeds (Arctocephalus australis, Arctocephalus gazella, and Otaria flavescens) in southern Brazil. J Zoo Wildlife Medic 47:132–140. https://doi.org/10.1638/2015-0090.1

    Article  Google Scholar 

  • Jones A, Bray RA, Gibson DI (2005) Keys to the Trematoda. V. 2. CABI Publishing, Wallingford

  • Katahira H, Matsuda AT, Maeda S, Yoshida E, Banzai A, Matsuishi TF (2021) Diphyllobothrium stemmacephalum (Cestoda: Diphyllobothriidae) found from a harbor porpoise in northern Japan, with comments on a geographical gap with human infection cases in southern Japan. Par Int 87:102487. https://doi.org/10.1016/j.parint.2021.102487

    Article  CAS  Google Scholar 

  • Klimpel S, Kuhn T, Münster J, Dörge DD, Klapper R, Kochmann J (2019) Parasites of marine fish and cephalopods: a practical guide. Cham, Switzerland, Springer

  • Klinkhardt MB (1994) The karyotypic divergence between species of Gadidae (Pisces, Gadiformes). Cytobios 77:207–214

    Google Scholar 

  • Kumar S, Stecher G, Li M, Knyaz C, Tamura K (2018) MEGA X: Molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 35:1547–1549

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kutyrev IA, Mordvinov VA (2022) Population genetic structure of diphyllobothriid tapeworms (Cestoda: Diphyllobothriidea) parasitising fish in the Baikal Rift Zone. Diseas Aq Organisms 148:113–125. https://doi.org/10.3354/dao03646

    Article  CAS  Google Scholar 

  • Legendre P, Gallagher ED (2001) Ecologically meaningful transformations for ordination of species data. Oecologia 129:271–280

    Article  PubMed  ADS  Google Scholar 

  • Liu SS, Liu GH, Zhu XQ, Weng YB (2015) The complete mitochondrial genome of Pseudoterranova azarasi and comparative analysis with other anisakid nematodes. Infection, Gen Evol 33:293–298. https://doi.org/10.1016/j.meegid.2015.05.018

    Article  CAS  Google Scholar 

  • Liu GH, Nadler SA, Liu SS, Podolska M, D’Amelio S, Shao R, Gasser RB, Zhu XQ (2016) Mitochondrial phylogenomics yields strongly supported hypotheses for ascaridomorph nematodes. Sc Reports 6:1–8. https://doi.org/10.1038/srep39248

    Article  CAS  Google Scholar 

  • Logvinenko AD, Gordeev II (2022) Metazoan parasites of a few marine fish near White Sea Biological Station (Lomonosov MSU). In: Granovich AI (ed) Belomorskaya Studencheskaya Nauchnaya Sessiya SPbGUTezisy Dokladov. St Petersburg, Svoyo Izdatelstvo, pp 75

  • Logvinenko AD, Gordeev II (2021) Fish parasites of White Sea and Barents Sea: features of the fauna and retrospective analysis of the study. In: Gordeev II, Kivva KK, Vorobyova OV, Arkhipov LO, Lavrukhina EV (eds) Sovremennyye problemy i perspektivy razvitiya rybokhozyaystvennogo kompleksa: materialy IX Nauchno-prakticheskoy konferentsii molodykh uchënykh s mezhdunarodnym uchastiyem, posvyashchennoy 140-letiyu VNIRO. VNIRO, Moscow, pp 104–107 ((in Russian))

    Google Scholar 

  • Makhotin VV (2016) Embryonic and early larval development of White Sea cod Gadus morhua marisalbi (Gadidae). J Ichth 56:259–280. https://doi.org/10.1134/S0032945216020119

    Article  Google Scholar 

  • Maltsev VN (1998) On the taxonomic status of species Diphyllobothnn schistochilus (Cestoda: Pseudophyllidea) known as a parasite of bearded seal in the Arctic. In: Alimov AF, Galkin AK, Dubinina EV (eds) Problemy tsestodologii, ZIN RAN, St. Petersburg, pp 83–94

  • Marti YY (1980) Migrations of marine fishes. Picshepromisdat, Moscow

  • Mattiucci S, 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. Adv Parasitol 66:47–148

    Article  PubMed  Google Scholar 

  • Mattiucci S, Paggi L, Nascetti G, Ishikura H, Kikuchi K, Sato N, Cianchi R, Bullini L (1998) Allozyme and morphological identification of shape Anisakis, Contracaecum and Pseudoterranova from Japanese waters (Nematoda, Ascaridoidea). Syst Parasitol 40:81–92. https://doi.org/10.1023/a:1005914926720

    Article  Google Scholar 

  • Mattiucci S, Paoletti M, Webb SC (2009) Anisakis nascettii n. sp. (Nematoda: Anisakidae) from beaked whales of the southern hemisphere: morphological description, genetic relationships between congeners and ecological data. Syst Parasitol 74(3):199–217

    Article  PubMed  Google Scholar 

  • Mattiucci S, Paoletti M, Webb SC, Nascetti G (2012) Pseudoterranova and Contracaecum. USA, CRC Press Boca Raton, Molecular detection of human parasitic pathogens

    Google Scholar 

  • Moravec F (1994) Parasitic nematodes of freshwater fishes of Europe. Academia, Praha

    Google Scholar 

  • Mozgovoy AA (1953) Fundamentals of nematodology. Vol. II, Pt 2. Izdatel’stvo AN SSSR, Moscow

  • Mustafina AR, Biserova NM (2022) Excretory system ultrastructure of diphyllobothriid tapeworm Pyramicocephalus phocarum (Cestoda) with cytochemical and functional implication. Invert Zool 19:159–184. https://doi.org/10.15298/invertzool.19.2.05

    Article  Google Scholar 

  • Myers BJ (1959) Phocanema, a new genus for the anisakid nematode of seals. Can J Zool 37:459–465. https://doi.org/10.1139/z59-053

    Article  Google Scholar 

  • Nyman T, Papadopoulou E, Ylinen E, Wutke S, Michell CT, Sromek L, Sinisalo T, Andrievskaya E, Alexeev V, Kunnasranta M (2021) DNA barcoding reveals different cestode helminth species in northern European marine and freshwater ringed seals. Int J Paras: Paras and Wildlife 15:255–261. https://doi.org/10.1016/j.ijppaw.2021.06.004

    Article  Google Scholar 

  • Paggi L, Nascetti G, Cianchi R, Orecchia P, Mattiucci S, D’Amelio S et al (1991) Genetic evidence for three species within Pseudoterranova decipiens (Nematoda, Ascaridida, Ascaridoidea) in the north Atlantic and Norwegian and Barents seas. Int J Parasitol 21:195–212. https://doi.org/10.1016/0020-7519(91)90010-5

    Article  CAS  PubMed  Google Scholar 

  • Posada D (2008) jModelTest: phylogenetic model averaging. Mol Biol Evol 25:1253–1256

    Article  CAS  PubMed  Google Scholar 

  • Quiazon KMA, Santos MD, Yoshinaga T (2013) Anisakis species (Nematoda: Anisakidae) of Dwarf Sperm Whale Kogia sima (Owen, 1866) stranded off the Pacific coast of southern Philippine archipelago. Veterin Parasitol 197:221–230

    Article  Google Scholar 

  • Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatic 19:1572–1574

    Article  CAS  Google Scholar 

  • Rubilar A, Torres P, Yera H, Leyan V, Silva R (2022) First Report of Zoonotic Tapeworms, Dibothriocephalus latus (Linnaeus, 1758) and D. dendriticus (Nitzsch, 1824), and Other Endohelminth Parasites in Chinook Salmon, Oncorhynchus tshawytscha, in Chile. ComparParasitol 89:35–54. https://doi.org/10.1654/1525-2647-89.2.136

    Article  Google Scholar 

  • Sasaki M, Ishinazaka G, Nose M, Asakawa M, Nakao M (2019) Japanese “fissure” tapeworm detected from the intestinal tract of a brown bear in Shari, Hokkaido. J Japan Soc Wildlife Med 24:123–126. https://doi.org/10.5686/jjzwm.24.123

    Article  Google Scholar 

  • Schaeffner BC, Ditrich O, Kuchta R (2018) A century of taxonomic uncertainty: re-description of two species of tapeworms (Diphyllobothriidea) from Arctic seals. Polar Biol 41:2543–2559. https://doi.org/10.1007/s00300-018-2396-0

    Article  Google Scholar 

  • Scholz T, Kuchta R, Brabec J (2019) Broad tapeworms (Diphyllobothriidae), parasites of wildlife and humans: recent progress and future challenges. Int J Parasit: Par Wildlife 9:359–369. https://doi.org/10.1016/j.ijppaw.2019.02.001

    Article  Google Scholar 

  • Shulman SS (1956) Parasite fauna of herring, smelt and navaga of the White Sea. Trudy Karelo-Finskogo Filiala Akademii Nauk SSSR 4:50–67

    Google Scholar 

  • Shulman SS, Shulman-Albova RE (1953) Parasites of fish of the White Sea. Izdatel’stvo akademii nauk SSSR, Moscow-Leningrad

  • Sirenko BI (ed) (2001) List of species of free-living invertebrates of Eurasian Arctic seas and adjacent deep waters. Russian Academy of Science, Zoological Institute, Moscow

    Google Scholar 

  • Stiles CW, Hassall A (1899) Internal parasites of the fur seal. US Government Printing Office

  • Suzuki J, Murata R, Hosaka M, Araki J (2010) Risk factors for human Anisakis infection and association between the geographic origins of Scomber japonicus and anisakid nematodes. Int J Food Microb 137:88–93

    Article  Google Scholar 

  • Takano T, Iwaki T, Waki T, Murata R, Suzuki J, Kodo Y, Kobayashi K, Ogawa K (2021) Species composition and infection levels of Anisakis (Nematoda: Anisakidae) in the skipjack tuna Katsuwonus pelamis (Linnaeus) in the Northwest Pacific. Par Res 120:1605–1615

    Article  Google Scholar 

  • Tchesunov AV, Kalyakina NM, Bubnova EN (2008) A Catalogue of Biota of the White Sea Biological Station of the Moscow State University. KMK Scientific Press Ltd, Moscow, p 384

    Google Scholar 

  • Timi JT, Paoletti M, Cimmaruta R, Lanfranchi AL, Alarcos AJ, Garbin L, George-Nascimentoe M, Rodríguezf DH, Giardino GV, Mattiucci S (2014) Molecular identification, morphological characterization and new insights into the ecology of larval Pseudoterranova cattani in fishes from the Argentine coast with its differentiation from the Antarctic species, P. decipiens sp. E (Nematoda: Anisakidae). Veterin Parasitol 199:59–72

    Article  CAS  Google Scholar 

  • Timofeeva SV, Marasaeva EF (1984) Parasitofauna of two forms of cod of Kandalaksha Bay of the White Sea. In: Poljanskij JI (ed) Ecological and parasitological studies of the northern seas. Kol’skij filial AN SSSR, Apatity, pp 62–76

  • Timofeeva SV, Marasaeva EF (1988) Parasite fauna of coastal cod and navaga of the White Sea. In: Skarlato OA (ed) Sovremennyye problemy gidrobiologii Barentseva morya. Izd-vo Kol’sk. nauch. tsentra AN SSSR, Apatity, pp 55–65

  • Timofeeva SV (1990) Ecological and faunistic analysis of the parasite fauna of the Arctic Sea navaga in the White Sea. In: Dobrovolsky AA, Galaktionov KV, Strelkov AA (eds) Morfologiya i ekologiya parazitov morskikh zhivotnykh. Izd-vo Kol’sk. nauch. tsentra AN SSSR, Apatity, pp 92–103

  • Valentini A, Mattiucci S, Bondanelli P, Webb SC, Mignucci-Giannone AA, Colom-Llavina MM, Nascetti G (2006) Genetic relationships among Anisakis species (Nematoda: Anisakidae) inferred from mitochondrial cox2 sequences, and comparison with allozyme data. J Paras 92:156–166

    Article  CAS  Google Scholar 

  • Waeschenbach A, Brabec J, Scholz T, Littlewood DTJ, Kuchta R (2017) The catholic taste of broad tapeworms - multiple routes to human infection. Int J Parasitol 47:831–843. https://doi.org/10.1016/j.ijpara.2017.06.004

    Article  CAS  PubMed  Google Scholar 

  • Waeschenbach A, Littlewood DTJ (2017) A molecular framework for the Cestoda. In: Caira J, Jensen K (eds) Planetary Biodiversity Inventory (2008–2017): Tapeworms from the vertebrate bowels of the Earth. Natural History Museum, Lawrence, pp 431–451

  • Young C, Miller MA, Kuchta R, Brabec J, Newsome SD, Dailey M (2017) First report of an adult tapeworm (Cestoda: Diphyllobothriidea) in a Southern Sea Otter (Enhydra lutris nereis). J Wildlife Dis 53:934–937

    Article  Google Scholar 

Download references

Acknowledgements

We are grateful to Maxim L. Lovat, Alexander M. Kotsky, Oleg I. Malyutin, Svyatoslav Lipey, Alexander Voskoboynikov, Nikolai Melnikov, Uliana Piunova, and Galina Likhacheva for their help with the sampling. We also thank Dmitry Shchepetov, Maria Stanovova, and Darya Grishina (Lomonosov Moscow State University) for their help with the genetic studies.

Funding

This study was funded by Russian Science Foundation # 20–74-10012.

Russian Science Foundation,20-74-10012

Author information

Authors and Affiliations

Authors

Contributions

ADL obtained the samples; IIG and SGS conceptualized the study and drafted the manuscript; ADL and IAE carried out molecular studies. All authors reviewed the manuscript.

Corresponding author

Correspondence to Ilya I. Gordeev.

Ethics declarations

Consent to participate

Not applicable.

Consent for publication

Not applicable.

Competing interests

The authors declare no competing interests.

Additional information

Section Editor: Matthew Wayland.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 70 KB)

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Logvinenko, A.D., Gordeev, I.I., Ekimova, I.A. et al. Helminths of three species of White Sea fishes. Parasitol Res 123, 39 (2024). https://doi.org/10.1007/s00436-023-08017-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s00436-023-08017-9

Keywords

Navigation