Hostname: page-component-586b7cd67f-l7hp2 Total loading time: 0 Render date: 2024-11-30T04:07:30.896Z Has data issue: false hasContentIssue false
  • English
  • Français

Lecithaster (Lecithasteridae, Digenea) in the White Sea: an unnoticed guest from the Pacific?

Published online by Cambridge University Press:  21 June 2022

D. Krupenko Open the ORCID record for D. Krupenko [Opens in a new window] ,
G. Kremnev Open the ORCID record for G. Kremnev [Opens in a new window] ,
O. Skobkina ,
A. Gonchar Open the ORCID record for A. Gonchar [Opens in a new window] ,
A. Uryadova  and
A. Miroliubov Open the ORCID record for A. Miroliubov [Opens in a new window]
D. Krupenko*
Affiliation:
Department of Invertebrate Zoology, St Petersburg University, Universitetskayia nab. 7–9, 199034, St Petersburg, Russia
G. Kremnev
Affiliation:
Department of Invertebrate Zoology, St Petersburg University, Universitetskayia nab. 7–9, 199034, St Petersburg, Russia
O. Skobkina
Affiliation:
Department of Invertebrate Zoology, St Petersburg University, Universitetskayia nab. 7–9, 199034, St Petersburg, Russia
A. Gonchar
Affiliation:
Department of Invertebrate Zoology, St Petersburg University, Universitetskayia nab. 7–9, 199034, St Petersburg, Russia Laboratory of Parasitic Worms and Protists, Zoological Institute, Russian Academy of Sciences, Universitetskaya nab. 1, 199034, St Petersburg, Russia
A. Uryadova
Affiliation:
Department of Invertebrate Zoology, St Petersburg University, Universitetskayia nab. 7–9, 199034, St Petersburg, Russia
A. Miroliubov
Affiliation:
Department of Invertebrate Zoology, St Petersburg University, Universitetskayia nab. 7–9, 199034, St Petersburg, Russia Laboratory of Parasitic Worms and Protists, Zoological Institute, Russian Academy of Sciences, Universitetskaya nab. 1, 199034, St Petersburg, Russia
*
Author for correspondence: D. Krupenko, E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Morphological discrimination of species is problematic in many digenean taxa. Parasites of marine fish from the genus Lecithaster Lühe, 1901 are a good example of this. Our goal was to understand which species of Lecithaster infect fish in the White Sea, and reveal their life cycles. We collected specimens of maritae from nine fish species, analysed their morphology and sequenced 28S ribosomal DNA and internal transcribed spacer 2 (ITS2). Contrary to previous accounts, all of them belong to a single species, Lecithaster salmonis Yamaguti, 1934, which was previously only recorded from the Pacific. Morphologically, our maritae specimens were highly variable, sharing characters of L. salmonis, Lecithaster confusus Odhner, 1905 and Lecithaster gibbosus (Rudolphi, 1802) Lühe, 1901. This variability did not correlate with the moderate differences in ITS2 among the specimens, and neither did the fish host species. Members of the subfamily Salmoninae appear to be the best suited definitive hosts, judging from the intensity rates. The intermediate hosts were also discovered: the first is Cryptonatica affinis (Gmelin, 1791) and the second are planktonic copepods. These lifecycle data from the White Sea are consistent with L. salmonis species identification and with the distribution of this species in the North Pacific. The geographical range of L. salmonis seems to be interrupted, and we discuss possible ways of L. salmonis expansion.

Keywords

DigeneaHemiuroideaLecithasteridaefish parasiteslife cyclesmorphological variability28SITS2cercariaeWhite Sea
Type
Research Paper
Information
Journal of Helminthology , Volume 96 , 2022 , e43
Copyright
Copyright © The Author(s), 2022. 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.)

References

Alekseev, MY, Tkachenko, AV, Zubchenko, AV, Shkatelov, AP and Nikolaev, AM (2019) Distribution, spawning and the possibility of fishery of introduced pink salmon (Oncorhynchus gorbuscha Walbaum) in rivers of Murmansk Oblast]. Russian Journal of Biological Invasions 10, 109–117 (in Russian).CrossRefGoogle Scholar
Anderson, GR and Barker, SC (1998) Inference of phylogeny and taxonomy within the Didymozoidae (Digenea) from the second internal transcribed spacer (ITS2) of ribosomal DNA. Systematic Parasitology 41, 87–94.CrossRefGoogle Scholar
Atopkin, DM, Nakao, M, Besprozvannykh, VV, Ha, ND, Nguyen, HV and Sasaki, M (2020) Morphological and molecular data for species of Lecithaster Lühe, 1901 and Hysterolecithoides Yamaguti, 1934 (Digenea: Lecithasteridae) from fish of East Asia and phylogenetic relationships within the Hemiuroidea Looss, 1899. Journal of Helminthology 94, E14.CrossRefGoogle Scholar
Barskaya, YY, Ieshko, EP and Novokhatskaya, OV (2005) Formation of parasite fauna of pink salmon Oncorhynchus gorbuscha (Walbaum, 1792) under acclimatization. pp. 39–43 in Alimov, AF, Berger, VY, Ieshko, EP and Nemova, NN (Eds) The study, sustainable use and conservation of natural resources of the White Sea. Proceedings of the IXth International Conference, October, 11–14, 2004. Petrozavodsk, Karelia, Russia (in Russian).Google Scholar
Besprozvannykh, VV, Atopkin, DM, Ngo, HD, Ermolenko, AV, Van Ha, N, Van Tang, N and Beloded, AY (2017) Morphometric and molecular analyses of two digenean species in mugilid fish: Lecithaster mugilis Yamaguti, 1970 from Vietnam and L. sudzuhensis n. sp. from southern Russian Far East. Journal of Helminthology 91, 326–331.CrossRefGoogle Scholar
Blasco-Costa, I and Poulin, R (2013) Host traits explain the genetic structure of parasites: a meta-analysis. Parasitology 140, 1316–1322.CrossRefGoogle ScholarPubMed
Carreras-Aubets, M, Repullés-Albelda, A, Kostadinova, A and Carrassón, M (2011) A new cryptic species of Aponurus Looss, 1907 (Digenea: Lecithasteridae) from Mediterranean goatfish (Teleostei: Mullidae). Systematic Parasitology 79, 145–159.CrossRefGoogle Scholar
Chen, C and Nomaki, H (2021) Noteworthy observations and records of rare bathyal gastropods from unusual habitats in Sagami Bay, Japan. Marine Biodiversity 51, 1–8.CrossRefGoogle Scholar
Chubrik, GK (1966) Fauna and ecology of trematode larvae from molluscs in the Barents and White seas. Trudy Murmanskii Morskoi Biologicheskii Institute 10, 78–166 (in Russian).Google Scholar
Crawford, SS and Muir, AM (2008) Global introductions of salmon and trout in the genus Oncorhynchus: 1870–2007. Reviews in Fish Biology and Fisheries 18, 313–344.CrossRefGoogle Scholar
Darriba, D, Taboada, GL, Doallo, R and Posada, D (2012) JModelTest 2: more models, new heuristics and parallel computing. Nature Methods 9, 772–772.CrossRefGoogle ScholarPubMed
Esch, GW, Kennedy, CR, Bush, AO and Aho, JM (1988) Patterns in helminth communities in freshwater fish in Great Britain: alternative strategies for colonization. Parasitology 96, 519–532.CrossRefGoogle ScholarPubMed
Gibson, DI (2002) Family Lecithasteridae Odhner, 1905. pp. 381–396 in Gibson, DI, Jones, A and Bray, RA (Eds) Keys to the Trematoda, Vol. 1. London, The Natural History Museum.CrossRefGoogle Scholar
Gilardoni, C, Etchegoin, J, Cribb, T, Pina, S, Rodrigues, P, Diez, ME and Cremonte, F (2020) Cryptic speciation of the zoogonid digenean Diphterostomum flavum n. sp. demonstrated by morphological and molecular data. Parasite 27, 44.CrossRefGoogle Scholar
Golikov, AN (1987) Class Gastropoda. pp. 41–148 in Starobogatov, YI and Naumov, AD (Eds) Molluscs of the White Sea. Leningrad, Nauka (in Russian).Google Scholar
Gonchar, A and Galaktionov, KV (2021) It is marine: distinguishing a new species of Catatropis (Digenea: Notocotylidae) from its freshwater twin. Parasitology 148, 74–83.CrossRefGoogle ScholarPubMed
Hunninen, AV and Cable, RM (1943) The life history of Lecithaster confusus Odhner (Trematoda: Hemiuridae). Journal of Parasitology 29, 71–79.CrossRefGoogle Scholar
Kantor, II and Sysoev, AV (2006) Marine and brackish water Gastropoda of Russia and adjacent countries: an illustrated catalogue. Moscow, KMK Scientific Press Ltd, p. 373.Google Scholar
Klemetsen, A, Amundsen, PA, Dempson, JB, Jonsson, B, Jonsson, N, O'Connell, MF and Mortensen, E (2003) Atlantic salmon Salmo salar L., brown trout Salmo trutta L. and Arctic charr Salvelinus alpinus (L.): a review of aspects of their life histories. Ecology of Freshwater Fish 12, 1–59.CrossRefGoogle Scholar
Køie, M (1979) On the morphology and life-history of Derogenes varicus (Müller, 1784) Looss, 1901 (Trematoda, Hemiuridae). Zeitschrift für Parasitenkunde 59, 67–78.CrossRefGoogle Scholar
Køie, M (1989) On the morphology and life history of Lecithaster gibbosus (Rudolphi, 1802) Lühe, 1901 (Digenea, Hemiuroidea). Parasitology Research 75, 361–367.CrossRefGoogle Scholar
Kremnev, G, Gonchar, A, Krapivin, V, Knyazeva, O and Krupenko, D (2020) First elucidation of the life cycle in the family Brachycladiidae (Digenea), parasites of marine mammals. International Journal for Parasitology 50, 997–1009.CrossRefGoogle Scholar
Kumar, S, Stecher, G and Tamura, K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Molecular Biology and Evolution 33, 1870–1874.CrossRefGoogle ScholarPubMed
Linton, E (1940) Trematodes from fishes mainly from the Woods Hole region, Massachusetts. Proceedings of the United States National Museum 88, 1–172.CrossRefGoogle Scholar
Makhrov, AA and Lajus, DL (2018) Postglacial colonization of the North European seas by Pacific fishes and lamprey. Contemporary Problems of Ecology 11, 247–258.CrossRefGoogle Scholar
Manter, HW (1926) Some North American fish trematodes. Illinois Biological Monographs 10, 1–138.Google Scholar
Martin, WE and Multani, S (1970) Some helminths of the mudsucker fish, Gillichthys mirabilis cooper. Bulletin Southern-California Academy of Sciences 69, 161–168.Google Scholar
Mitenev, VK and Karasev, AB (2005) Ecological characteristics of the parasite fauna of the Atlantic salmon Salmo salar L. from the Barents and White seas watersheds. Salmonid fishes of Eastern Fennoscandia. Petrozavodsk, KarRC RAS, pp. 81–89 (in Russian).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.CrossRefGoogle ScholarPubMed
Odhner, T (1905) Die Trematoden des arktischen Gebietes. Fauna Arctica 4, 289–372 (in German).Google Scholar
Olson, PD, Cribb, TH, Tkach, VV, Bray, RA and Littlewood, DTJ (2003) Phylogeny and classification of the Digenea (Platyhelminthes: Trematoda). International Journal for Parasitology 33, 733–755.CrossRefGoogle Scholar
Orecchia, P, Paggi, L and Radujkovir, BM (1988) Digeneans of fishes from the Adriatic Sea with a description of Lecithaster atherinae n. sp. From Atherina (hepsetia) boyeri. Parassitologia 30, 225–229.Google Scholar
Schindelin, J, Arganda-Carreras, I, Frise, E, et al. (2012) Fiji: an open-source platform for biological-image analysis. Nature Methods 9, 676–682.CrossRefGoogle ScholarPubMed
Shimazu, T (2018) Adult digeneans (Trematoda) parasitic in Hypomesus nipponensis (Osteichthyes, Osmeridae) from brackish-water lakes of Japan. Bulletin of the National Museum of Natural Sciences, Series A 44, 57–68.Google Scholar
Shulman, S and Shulman-Albova, R (1953) Parasites of fishes of the white Sea. Moskva-Leningrad, Izdatelstvo Akademia Nauk SSSR, p. 201 (in Russian).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.CrossRefGoogle ScholarPubMed
Srivastava, LP (1966) The morphology of Lecithaster musteli sp. nov. (Digenea: Hemiuridae) from the intestine of Onos mustelus (L.) and a review of the genus Lecithaster Lühe, 1901. Parasitology 56, 543–554.CrossRefGoogle Scholar
Stamatakis, A (2014) RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30, 1312–1313.CrossRefGoogle ScholarPubMed
Timofeeva, TA (1976) Morphology and biology of cystophorous cercariae from the Barents Sea. Parasitologiia 10, 488–496 (in Russian, with English summary).Google Scholar
Tkach, V, Grabda-Kazubska, B, Pawlowski, J and Swiderski, Z (1999) Molecular and morphological evidence for close phylogenetic affinities of the genera Macrodera, Leptophallus, Metaleptophallus and Paralepoderma [Digenea, Plagiorchiata]. Acta Parasitologica 44, 170–179.Google Scholar
WoRMS. (2022a) Lecithaster Lühe, 1901. Available at https://www.marinespecies.org/aphia.php?p=taxdetails&id=108771 (accessed 4 March 2022).Google Scholar
WoRMS. (2022b) Cryptonatica affinis (Gmelin, 1791). Available at https://www.marinespecies.org/aphia.php?p=taxdetails&id=140525 (accessed 20 April 2022).Google Scholar
Yamaguti, S (1934) Studies on the helminth fauna of Japan. Part 2, Trematodes of fishes, I. Japanese Journal of Zoology 5, 249–541.Google Scholar
Yamaguti, S (1940) Studies on the helminth fauna of Japan Part 31. Trematodes of fishes, VII. Japanese Journal of Zoology 9, 35–108.Google Scholar
Zhukov, EV (1960) Endoparasitic worms of the fishes in the Sea of Japan and South-Kuril shallow-waters. Trudy Zoologicheskogo Lnstituta 28, 3–146 (in Russian).Google Scholar
Supplementary material: PDF

Krupenko et al. supplementary material

Tables S1 and S2

Download Krupenko et al. supplementary material(PDF)
PDF 465.7 KB