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Life cycle of the seabird digenean Gymnophallus minor (Gymnophallidae) in the Arctic

Part of: Helminths and their molluscan hosts: updates and remaining challenges

Published online by Cambridge University Press:  27 February 2025

K.V. Galaktionov Open the ORCID record for K.V. Galaktionov [Opens in a new window] ,
A. Gonchar Open the ORCID record for A. Gonchar [Opens in a new window] ,
K.M. Wegner Open the ORCID record for K.M. Wegner [Opens in a new window] ,
R. Wolfensberger Open the ORCID record for R. Wolfensberger [Opens in a new window] ,
C. Buschbaum Open the ORCID record for C. Buschbaum [Opens in a new window]  and
A.E. Romanovich Open the ORCID record for A.E. Romanovich [Opens in a new window]
K.V. Galaktionov
Affiliation:
Laboratory of Parasitic Worms and Protists, Zoological Institute of the Russian Academy of Sciences, Universitetskaya Emb. 1, St Petersburg 199034, Russia Department of Invertebrate Zoology, Saint Petersburg University, Universitetskaya Emb.7/9, St Petersburg 199034, Russia
A. Gonchar*
Affiliation:
Laboratory of Parasitic Worms and Protists, Zoological Institute of the Russian Academy of Sciences, Universitetskaya Emb. 1, St Petersburg 199034, Russia Department of Invertebrate Zoology, Saint Petersburg University, Universitetskaya Emb.7/9, St Petersburg 199034, Russia
K.M. Wegner
Affiliation:
Alfred Wegener Institute (AWI) – Helmholtz Centre for Polar and Marine Research, Coastal Ecology, Waddensea Station Sylt, Hafenstrasse 43, 25992 List, Germany
R. Wolfensberger
Affiliation:
Alfred Wegener Institute (AWI) – Helmholtz Centre for Polar and Marine Research, Coastal Ecology, Waddensea Station Sylt, Hafenstrasse 43, 25992 List, Germany
C. Buschbaum
Affiliation:
Alfred Wegener Institute (AWI) – Helmholtz Centre for Polar and Marine Research, Coastal Ecology, Waddensea Station Sylt, Hafenstrasse 43, 25992 List, Germany
A.E. Romanovich
Affiliation:
Research Park, Saint Petersburg University, Universitetskaya Emb.7/9, St Petersburg 199034, Russia
*
Corresponding author: A. Gonchar; Emails: [email protected]; [email protected]; [email protected]
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Abstract

Gymnophallidae is one of the digenean families featuring bivalves as first intermediate hosts. However, the exact bivalve host species remain unknown for most members of this family. Gymnophallids have been one of the targets in our continuous efforts to reveal the diversity of digeneans in the higher north. Here, we focus on Gymnophallus minor, which we found in eiders from various locations in the Arctic and sub-Arctic. Sexual adults (maritae) of G. minor can be easily identified because they have a distinctive character: the roughly equal size of the pharynx and the ventral sucker. We also matched them, using DNA markers, with the intramolluscan stages (sporocysts, cercariae, and metacercariae) from the bivalve Liocyma fluctuosa collected on Spitsbergen. Taken together, we compile the first data on the life cycle of G. minor and discuss them in the context of other gymnophallids.

Keywords

Life cycleintermediate hostbivalvemetacercariabird parasite
Type
Short Communication
Information
Journal of Helminthology , Volume 99 , 2025 , e37
Copyright
© The Author(s), 2025. Published by Cambridge University Press

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References

Achatz, TJ, Curran, SS, Patitucci, F, Fecchio, A and Tkach, VV (2019) Phylogenetic affinities of Uvulifer spp. (Digenea: Diplostomidae) in the Americas with description of two new species from Peruvian Amazon. Journal of Parasitology 105(5), 704–717.CrossRefGoogle ScholarPubMed
Ahasan, SA, De Elías-Escribano, A, Artigas, P, Alam, MZ, Mondal, MMH, Blair, D, Chowdhury, EH, Bargues, MD and Mas-Coma, S (2023) Wide variation of heterozygotic genotypes of recent fasciolid hybrids from livestock in Bangladesh assessed by rDNA internal transcribed spacer region sequencing and cloning. One Health 17, 100614.CrossRefGoogle ScholarPubMed
Bartoli, P and Gibson, DI (2007) Synopsis of the life cycles of Digenea (Platyhelminthes) from lagoons of the northern coast of the western Mediterranean. Journal of Natural History 41(25–28), 1553–1570.CrossRefGoogle Scholar
Bayssade-Dufour, C, Jouet, D, Rudolfova, J, Horák, P and Ferté, H (2006) Seasonal morphological variations in bird schistosomes. Parasite 13, 205–214.CrossRefGoogle ScholarPubMed
Benito, D, Izagirre, U, Lekube, X, Zaldibar, B, Villalba, A, De Montaudouin, X, Daffe, G, Soto, M and de Cerio, OD (2023) Molecular confirmation of pearl formation in arctic mussels (Mytilus edulis) caused by Gymnophallus bursicola (Odhner 1900) metacercariae. Parasitology 150(11), 1015–1021.CrossRefGoogle ScholarPubMed
Bishop, CA and Threlfall, W (1974) Helminth parasites of the common eider duck, Somateria mollissima (L.), in Newfoundland and Labrador. Proceedings of the Helminthological Society of Washington 7, 25–35.Google Scholar
Blasco-Costa, I, Cutmore, SC, Miller, TL and Nolan, MJ (2016) Molecular approaches to trematode systematics: ‘Best practice’ and implications for future study. Systematic Parasitology 93, 295–306.CrossRefGoogle ScholarPubMed
Cremonte, F, Gilardoni, C, Pina, S, Rodrigues, P and Ituarte, C (2015) Revision of the family Gymnophallidae Odhner, 1905 (Digenea) based on morphological and molecular data. Parasitology International 64(2), 202–210.CrossRefGoogle ScholarPubMed
Darriba, D, Posada, D, Kozlov, AM, Stamatakis, A, Morel, B and Flouri, T (2020) ModelTest-NG: A new and scalable tool for the selection of DNA and protein evolutionary models. Molecular Biology and Evolution 37(1), 291–294.CrossRefGoogle ScholarPubMed
Diaz, PE, Bray, RA, Cutmore, SC, Ward, S and Cribb, TH (2015) A complex of species related to Paradiscogaster glebulae (Digenea: Faustulidae) in chaetodontid fishes (Teleostei: Perciformes) of the Great Barrier Reef. Parasitology International 64(5), 421–428.CrossRefGoogle ScholarPubMed
Edler, D, Klein, J, Antonelli, A and Silvestro, D (2021) raxmlGUI 2.0: A graphical interface and toolkit for phylogenetic analyses using RAxML. Methods in Ecology and Evolution 12(2), 373–377.CrossRefGoogle Scholar
Feis, ME, Thieltges, DW, Olsen, JL, de Montaudouin, X, Jensen, KT, Bazaïri, H, Culloty, SC and Luttikhuizen, PC (2015) The most vagile host as the main determinant of population connectivity in marine macroparasites. Marine Ecology Progress Series 520, 85–99.CrossRefGoogle Scholar
Galaktionov, KV (2017) Patterns and processes influencing helminth parasites of Arctic coastal communities during climate change. Journal of Helminthology 91(4), 387–408.CrossRefGoogle ScholarPubMed
Galaktionov, KV, Węsławski, JM and Stempniewicz, L (2021) Food chain, parasites and climate changes in the high Arctic: A case study on trophically transmitted parasites of common eider Somateria mollissima at Franz Josef Land. Polar Biology 44, 1321–1342.CrossRefGoogle Scholar
Galaktionov, KV, Gonchar, A, Postanogova, D, Miroliubov, A and Bodrov, SY (2024) Parvatrema spp. (Digenea, Gymnophallidae) with parthenogenetic metacercariae: Diversity, distribution and host specificity in the palaearctic. International Journal for Parasitology 54(7), 333–355.Google ScholarPubMed
Golikov, AN and Scarlato, OA (1977) Composition, distribution and ecology of gastropods and bivalves off Franz Josef Land. In Scarlato, OA (ed), Biocenoses of the Shelf of Franz Josef Land and the Fauna of Adjacent Waters (Explorations of the Fauna of the Seas XIV [XXII]). Nauka, Moscow, 313–390 (in Russian).Google Scholar
Hernández-Mena, DI, García-Varela, M and de León, GPP (2017) Filling the gaps in the classification of the Digenea Carus, 1863: Systematic position of the Proterodiplostomidae Dubois, 1936 within the superfamily Diplostomoidea Poirier, 1886, inferred from nuclear and mitochondrial DNA sequences. Systematic Parasitology 94(8), 833–848.CrossRefGoogle ScholarPubMed
Kozlov, AM, Darriba, D, Flouri, T, Morel, B and Stamatakis, A (2019) RAxML-NG: A fast, scalable and user-friendly tool for maximum likelihood phylogenetic inference. Bioinformatics 35(21), 4453–4455.CrossRefGoogle ScholarPubMed
Krupenko, D, Uryadova, A, Gonchar, A, Kremnev, G and Krapivin, V (2020) New data on life cycles for three species of Fellodistomidae (Digenea) in the White Sea. Journal of Helminthology 94, e158.CrossRefGoogle ScholarPubMed
Krupenko, D, Kremnev, G, Gonchar, A, Uryadova, A, Miroliubov, A, Krapivin, V, Skobkina, O, Gubler, A and Knyazeva, O (2022) Species complexes and life cycles of digenetic trematodes from the family Derogenidae. Parasitology 149(12), 1590–1606.CrossRefGoogle ScholarPubMed
Loos-Frank, B (1969) Zur Kenntnis der gymnophalliden Trematoden des Nordseeraumes. I. Die Alternativ-Zyklen von Gymnophallus choledochus Odhner, 1900. Zeitschrift für Parasitenkunde 32, 135–156.Google ScholarPubMed
Marchiori, E, Quaglio, F, Franzo, G, Brocca, G, Aleksi, S, Cerchier, P, Cassini, R and Marcer, F (2023) Pearl formation associated with gymnophallid metacercariae in Mytilus galloprovincialis from the Northwestern Adriatic coast: preliminary observations. Journal of Invertebrate Pathology 196, 107854.CrossRefGoogle ScholarPubMed
Montenegro, D, Romero, MS and González, MT (2021) Morphological and molecular characterization of larval digenean trematodes (Parvatrema: Gymnophallidae) and their pathological effects on the clam Leukoma thaca (= Protothaca thaca) (Bivalvia: Veneridae) (Molina, 1782) from northern Chile. Parasitology International 80, 102238.CrossRefGoogle ScholarPubMed
Olson, PD, Cribb, TH, Tkach, Bray RA VV and Littlewood, DTJ (2003) Phylogeny and classification of the Digenea. International Journal for Parasitology 33, 733–755.CrossRefGoogle ScholarPubMed
Pérez-Ponce de León, G and Poulin, R (2018) An updated look at the uneven distribution of cryptic diversity among parasitic helminths. Journal of Helminthology 92(2), 197–202.CrossRefGoogle Scholar
Ronquist, F, Teslenko, M, Van Der Mark, P, Ayres, DL, Darling, A, Höhna, S, Larget, B, Liu, L, Suchard, MA and Huelsenbeck, JP (2012) MrBayes 3.2: Efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology 61(3), 539–542.CrossRefGoogle ScholarPubMed
Różycki, O and Gruszczyński, M (1991) Quantitative studies on the infauna of an Arctic estuary Nottinghambukta, Svalbard. Polish Polar Research 12(3), 433–444.Google Scholar
Ryzhikov, KM (1963) Psilostoma borealis n. sp. and Gymnophallus minor n. sp. from Anseriformes. Helminthologia 4, 424–429.Google Scholar
Shchenkov, SV, Sokolov, SG, Tsushko, KM and Denisova, SA (2022) Is Gymnophallus Odhner, 1900 (Trematoda: Gymnophallidae) polyphyletic? A new hypothesis based on phylogenetic position of Gymnophallus deliciosus (Olsson, 1893). Parasitology Research 121(7), 2157–2160.CrossRefGoogle ScholarPubMed
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
Vân Le, HL, Lecointre, G and Perasso, R (1993) A 28S rRNA-based phylogeny of the gnathostomes: First steps in the analysis of conflict and congruence with morphologically based cladograms. Molecular Phylogenetics and Evolution 2, 31–51.Google Scholar
Womble, MR, Orélis-Ribeiro, R and Bullard, SA (2015) Proterometra epholkos sp. n. (Digenea: Azygiidae) from Terrapin Creek, Alabama, USA: Molecular characterization of life cycle, redescription of Proterometra albacauda, and updated lists of host and geographic locality records for Proterometra spp. in North America. Parasitology International 64(1), 50–69.CrossRefGoogle Scholar