Hostname: page-component-65f69f4695-2qqrh Total loading time: 0 Render date: 2025-06-27T00:54:10.940Z Has data issue: false hasContentIssue false
  • English
  • Français

Species complexes and life cycles of digenetic trematodes from the family Derogenidae

Published online by Cambridge University Press:  15 August 2022

Darya Krupenko Open the ORCID record for Darya Krupenko [Opens in a new window] ,
Georgii Kremnev ,
Anna Gonchar Open the ORCID record for Anna Gonchar [Opens in a new window] ,
Alexandra Uryadova ,
Aleksei Miroliubov Open the ORCID record for Aleksei Miroliubov [Opens in a new window] ,
Vladimir Krapivin ,
Olga Skobkina ,
Arseniy Gubler  and
Olga Knyazeva
Darya Krupenko*
Affiliation:
Department of Invertebrate Zoology, Saint Petersburg University, Saint Petersburg, Russian Federation
Georgii Kremnev
Affiliation:
Department of Invertebrate Zoology, Saint Petersburg University, Saint Petersburg, Russian Federation
Anna Gonchar
Affiliation:
Department of Invertebrate Zoology, Saint Petersburg University, Saint Petersburg, Russian Federation Laboratory of Parasitic Worms and Protists, Zoological Institute, Russian Academy of Sciences, Saint Petersburg, Russia
Alexandra Uryadova
Affiliation:
Department of Invertebrate Zoology, Saint Petersburg University, Saint Petersburg, Russian Federation
Aleksei Miroliubov
Affiliation:
Department of Invertebrate Zoology, Saint Petersburg University, Saint Petersburg, Russian Federation Laboratory of Parasitic Worms and Protists, Zoological Institute, Russian Academy of Sciences, Saint Petersburg, Russia
Vladimir Krapivin
Affiliation:
Department of Invertebrate Zoology, Saint Petersburg University, Saint Petersburg, Russian Federation
Olga Skobkina
Affiliation:
Department of Invertebrate Zoology, Saint Petersburg University, Saint Petersburg, Russian Federation
Arseniy Gubler
Affiliation:
Department of Invertebrate Zoology, Saint Petersburg University, Saint Petersburg, Russian Federation
Olga Knyazeva
Affiliation:
Department of Invertebrate Zoology, Saint Petersburg University, Saint Petersburg, Russian Federation
*
Author for correspondence: Darya Krupenko, E-mail: krupenko.d@gmail.com, d.krupenko@spbu.ru
Get access Rights & Permissions [Opens in a new window]

Abstract

The best way to study digenean diversity combines molecular genetic methods, life-cycle studies and elaborate morphological descriptions. This approach has been barely used for one of the most widespread digenean taxa parasitizing fish – the superfamily Hemiuroidea. Here, we applied the integrative approach to the hemiuroideans from the family Derogenidae parasitizing fish at the White and Barents Seas. Analysis of 28S, 18S, 5.8S rDNA, ITS2 and cox1 gene sequences from sexually adult worms (maritae) showed genetic heterogeneity for 2 derogenid species known from this area: Derogenes varicus and Progonus muelleri. Thus, 2 pairs of genetic lineages were found: DV1 and DV2, PM1 and PM2, respectively. Data from other regions indicate that 2 more lineages of D. varicus probably exist. Based on previous records from the White and Barents Seas, we hypothesized that the cercariae found in the moonsnails (family Naticidae) belong to the Derogenidae and may help to differentiate these lineages as species. According to our results, Cercaria appendiculata from Cryptonatica affinis matched DV1, similar nameless cercariae from Euspira pallida and Amauropsis islandica matched DV2, and Cercaria octocauda from C. affinis matched PM1. We provide new data on the structure of these cercariae and discuss the life-cycle pattern of the studied digeneans.

Keywords

CercariaeDerogenesfish parasitesHemiuroidealife cyclesProgonusspecies recognitionTrematoda

Information

Type
Research Article
Information
Parasitology , Volume 149 , Issue 12 , October 2022 , pp. 1590 - 1606
Check for updates
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.)

Article purchase

Temporarily unavailable

References

Ahuir-Baraja, AE, Fraija-Fernández, N, Raga, JA and Montero, FE (2015) Molecular and morphological differentiation of two similar species of Accacoeliidae (Digenea): Accacladocoelium macrocotyle and A. nigroflavum from sunfish, Mola mola. The Journal of Parasitology 101, 231–235.CrossRefGoogle Scholar
Blair, D, Bray, RA and Barker, SC (1998) Molecules and morphology in phylogenetic studies of the Hemiuroidea (Digenea: Trematoda: Platyhelminthes). Molecular Phylogenetics and Evolution 9, 15–25.CrossRefGoogle ScholarPubMed
Bray, RA, Diaz, PE and Cribb, TH (2016) Knowledge of marine fish trematodes of Atlantic and Eastern Pacific Oceans. Systematic Parasitology 93, 223–235.CrossRefGoogle ScholarPubMed
Bray, RA, Cutmore, SC and Cribb, TH (2022) A paradigm for the recognition of cryptic trematode species in tropical Indo-west Pacific fishes: the problematic genus Preptetos (Trematoda: Lepocreadiidae). International Journal for Parasitology 52, 169–203.CrossRefGoogle ScholarPubMed
Chubrik, GK (1966) Fauna and ecology of trematode larvae from molluscs in the Barents and White Seas. Trudy Murmanskogo Morskogo Biologicheskogo Instituta 10, 78–166 [in Russian].Google Scholar
Cribb, TH (2016) The biodiversity of trematodes of fishes. Systematic Parasitology 93, 219–221.CrossRefGoogle ScholarPubMed
Cribb, TH, Bray, RA, Littlewood, DTJ, Pichelin, S and Herniou, EA (2001) Relationships of the Digenea – evidence from molecules and morphology. In Littlewood, DTJ and Bray, RA (eds), Interrelationships of Platyhelminthes. London, UK: Taylor & Francis, pp. 186–193.Google 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.Google ScholarPubMed
Dollfus, R (1960) Distomes des chaetognathes. Bulletin de l'Institut des Pêches Maritimes du Maroc, Casablanca 4, 19–45 [in French].Google Scholar
Dyer, WG, Williams, EH and Bunkley-Williams, L (1992) Homalometron dowgialloi sp. n. (Homalometridae) from Haemulon flavolineatum and additional records of digenetic trematodes of marine fishes in the West Indies. Journal of the Helminthological Society of Washington 59, 182–189.Google Scholar
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.CrossRefGoogle ScholarPubMed
Georgieva, S, Selbach, C, Faltýnková, A, Soldánová, M, Sures, B, Skírnisson, K and Kostadinova, A (2013) New cryptic species of the ‘revolutum’ group of Echinostoma (Digenea: Echinostomatidae) revealed by molecular and morphological data. Parasites & Vectors 6, 1–12.CrossRefGoogle ScholarPubMed
Gibson, DI and Bray, RA (1986) The Hemiuridae (Digenea) of fishes from the Northeast. Bulletin of the British Museum (Natural History) Zoology 51, 1–125.Google 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, 1–11.CrossRefGoogle Scholar
Goater, TM, Browne, CL and Esch, GW (1990) On the life history and functional morphology of Halipegus occidualis (Trematoda: Hemiuridae), with emphasis on the cystophorous cercaria stage. International Journal for Parasitology 20, 923–934.CrossRefGoogle 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
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, 833–848.CrossRefGoogle ScholarPubMed
Hunninen, AV and Cable, RM (1943) The life history of Lecithaster confusus Odhner (Trematoda: Hemiuridae). The Journal of Parasitology 29, 71–79.CrossRefGoogle Scholar
Huston, DC, Cutmore, SC, Miller, TL, Sasal, P, Smit, NJ and Cribb, TH (2021) Gorgocephalidae (Digenea: Lepocreadioidea) in the Indo-West Pacific: new species, life-cycle data and perspectives on species delineation over geographic range. Zoological Journal of the Linnean Society 193, 1416–1455.CrossRefGoogle Scholar
Issaitschikov, IM (1933) Contribution to parasitic worms of some groups of vertebrates from Russian Arctic. Transactions of the Oceanographical Institute 3, 1–44 [in Russian with partial English translation].Google 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
Køie, M (1990 a) On the morphology and life-history of Hemiurus luehei Odhner, 1905 (Digenea: Hemiuridae). Journal of Helminthology 64, 193–202.CrossRefGoogle ScholarPubMed
Køie, M (1990 b) A new cystophorous cercaria in Lunatia pallida (Broderip & Sowerby) (Naticidae): possibly the cercaria of Hemiurus levinseni Odhner, 1905 (Digenea, Hemiuridae). Ophelia 31, 77–84.CrossRefGoogle Scholar
Køie, M (1992) Life cycle and structure of the fish digenean Brachyphallus crenatus (Hemiuridae). The Journal of Parasitology 78, 338–343.CrossRefGoogle ScholarPubMed
Køie, M (1995) The life-cycle and biology of Hemiurus communis Odhner, 1905 (Digenea, Hemiuridae). Parasite 2, 195–202.Google Scholar
Køie, M (2000) Metazoan parasites of teleost fishes from Atlantic waters off the Faroe Islands. Ophelia 52, 25–44.CrossRefGoogle Scholar
Køie, M (2009) Boreogadus saida (Lepechin) (Gadidae): a review of its metazoan parasite fauna from Greenland, eastern Canada, Alaska and the Russian Arctic. Polar Biology 32, 1399–1406.CrossRefGoogle Scholar
Køie, M and Gibson, DI (1991) Aspects of the life-cycle of Magnibursatus caudofilamentosa (Reimer, 1971) Gibson and Køie, 1991 (Digenea, Hemiuroidea, Derogenidae). Ophelia 34, 117–127.CrossRefGoogle Scholar
Køie, M, Karlsbakk, E and Nylund, A (2002) A cystophorous cercaria and metacercaria in Antalis entalis (L.) (Mollusca, Scaphopoda) in Norwegian waters, the larval stage of Lecithophyllum botryophorum (Olsson, 1868) (Digenea, Lecithasteridae). Sarsia: North Atlantic Marine Science 87, 302–311.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 ScholarPubMed
Krupenko, D, Gonchar, A, Kremnev, G and Uryadova, A (2020) On the life cycle of Hemiurus levinseni Odhner, 1905 (Digenea: Hemiuridae). Invertebrate Zoology 17, 205–218.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
Kuklin, VV, Kuklina, MM and Kisova, NE (2012) Species composition and seasonal dynamics of the helminthofauna of the bullroat (Myoxocephalus scorpius, Cottidae) from Kola Bay of the Barents Sea. Russian Journal of Zoology 91, 131–137 [in Russian, with English summary].Google Scholar
Kulachkova, VG (1972) Helminths of Saggita elegans Verrill from the White Sea. Parazitologiia 16, 297–304 [in Russian, with English summary].Google 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
Kuramochi, T (2014) Digenean trematodes of deep-sea fishes from the Sea of Japan. National Museum of Nature and Science Monographs 44, 29–37.Google Scholar
Legeżyńska, J, Kędra, M and Walkusz, W (2012) When season does not matter: summer and winter trophic ecology of Arctic amphipods. Hydrobiologia 684, 189–214.CrossRefGoogle Scholar
Leigh, JW and Bryant, D (2015) POPART: full-feature software for haplotype network construction. Methods in Ecology and Evolution 6, 1110–1116.CrossRefGoogle Scholar
Leung, TL, Donald, KM, Keeney, DB, Koehler, AV, Peoples, RC and Poulin, R (2009) Trematode parasites of Otago Harbour (New Zealand) soft-sediment intertidal ecosystems: life cycles, ecological roles and DNA barcodes. New Zealand Journal of Marine and Freshwater Research 43, 857–865.CrossRefGoogle Scholar
Levinsen, GMR (1881) Bidrag til kundskap om Gronlands trematodfauna. Oversigt over det kongelige Dansk videnskadernes Selskabs Forhandlinger 23, 52–84.Google Scholar
Littlewood, DTJ and Olson, PD (2001) Small subunit rDNA and the Platyhelminthes: signal, noise, conflict and compromise. In Littlewood, DTJ and Bray, RA (eds), Interrelationships of Platyhelminthes. London, UK: Taylor & Francis, pp. 262–278.Google Scholar
Lloyd, LC (1938) Some digenetic trematodes from Puget Sound fish. The Journal of Parasitology 24, 103–133.CrossRefGoogle Scholar
Louvard, C, Cutmore, SC, Yong, RQ, Dang, C and Cribb, TH (2022) First elucidation of a didymozoid life cycle: Saccularina magnacetabula n. gen. n. sp. infecting an arcid bivalve. International Journal for Parasitology 52, 407–425.CrossRefGoogle Scholar
Madhavi, R (1978) Life history of Genarchopsis goppo Ozaki, 1925 (Trematoda: Hemiuridae) from the freshwater fish Channa punctata. Journal of Helminthology 52, 251–259.CrossRefGoogle ScholarPubMed
Manter, HW (1926) Some North American fish trematodes. Illinois Biological Monographs 10, 1–138.Google Scholar
Manter, HW (1934) Some digenetic trematodes from deep-water fish of Tortugas, Florida. Papers from Tortugas Laboratory 28, 257–345.Google Scholar
Matthews, BF (1981) Cercaria vaullegeardi Pelseneer, 1906 (Digenea: Hemiuridae); the infection mechanism. Parasitology 83, 587–593.CrossRefGoogle Scholar
McCauley, JE (1960) Some hemiurid trematodes of Oregon marine fishes. The Journal of Parasitology 46, 84–89.Google Scholar
Mitenev, VK (1993) Parasite fauna of the Barents Sea and White Sea salmon Salmo salar L. In Parasitological studies of fish in the Northern Basin. Murmansk: Izdatel’stvo PINRO, pp. 66–82 [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.Google 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 ScholarPubMed
Øresland, V (1986) Parasites of the chaetognath Sagitta setosa in the western English Channel. Marine Biology 92, 87–91.Google Scholar
Polyansky, YI (1955) Studies on the parasitology of the fish in the Northern Seas of the USSR. Parasites of fish of the Barents Sea. Trudy Zoologicheskogo Instituta 19, 5–170 [In Russian: English translation (1966) Israel Program for Scientific Translations, Cat. No. 1655, 158 pp.].Google Scholar
Rolbiecki, L and Waskusz, W (2005) Derogenes varicus (Müller, 1784) from chaetognaths (Chaetognatha) caught in Kongsfjorden, West Spitsbergen. Oceanological and Hydrobiological Studies 34, 131–134.Google Scholar
Schindelin, J, Arganda-Carreras, I, Frise, E, Kaynig, V, Longair, M, Pietzsch, T, Preibisch, S, Rueden, S, Saalfeld, S, Schmid, B, Tinevez, JY, White, DJ, Hartenstein, V, Eliceiri, K, Tomancak, P and Cardona, A (2012) Fiji: an open-source platform for biological-image analysis. Nature Methods 9, 676–682.CrossRefGoogle ScholarPubMed
Schrandt, MN, Andres, MJ, Powers, SP and Overstreet, RM (2016) Novel infection site and ecology of cryptic Didymocystis sp. (Trematoda) in the fish Scomberomorus maculatus. The Journal of Parasitology 102, 297–305.CrossRefGoogle ScholarPubMed
Shameem, U, Rao, NN and Madhavi, R (1990) Cercaria chilkaensis No. 1, a new cystophorous cercaria from the snail Stenothyra blanfordiana from Chilka lake, India. Journal of Natural History 24, 261–270.CrossRefGoogle Scholar
Shulman, S and Shulman-Albova, R (1953) Parasites of Fishes of the White Sea. Moskva-Leningrad, USSR: Izdatelstvo Akademia Nauk SSSR [In Russian].Google Scholar
Sokolov, SG, Atopkin, DM and Gordeev, II (2021) Phylogenetic position of the hemiuroid genus Paraccacladium Bray & Gibson, 1977 (Trematoda: Hemiuroidea) and the status of the subfamily Paraccacladiinae Bray & Gibson, 1977. Marine Biology Research 17, 31–40.CrossRefGoogle Scholar
Stamatakis, A (2014) RAxML version 8: a tool for phylogenetic analysis and postanalysis of large phylogenies. Bioinformatics 30, 1312–1313.CrossRefGoogle ScholarPubMed
Timofeeva, TA (1976) Morphology and biology of cystophorous cercariae from the Barents Sea. Parazitologiia 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
Tsuchida, K, Flores, V, Viozzi, G, Rauque, C and Urabe, M (2021) Hemiuroidean trematodes from freshwater Patagonian fishes: description of a new species, distribution and molecular phylogeny. Parasitology Research 120, 1219–1232.CrossRefGoogle ScholarPubMed
Tsuchida, K, Rauque, C, Viozzi, G, Flores, V and Urabe, M (2022) First report of post-cyclic transmission in trematodes: Derogenes lacustris (Digenea: Hemiuroidea) in Patagonian freshwater fishes. Parasitology 149, 234–238.Google ScholarPubMed
Urabe, M, Nishimura, T and Shimazu, T (2012) Taxonomic revision of three species of the genus Genarchopsis (Digenea: Hemiuroidea: Derogenidae) in Japan by molecular phylogenetic analyses. Parasitology International 61, 554–560.CrossRefGoogle ScholarPubMed
Wardle, WJ (1975) Cercaria anadarae sp. n. parasitizing a bivalve mollusc, Anadara brasiliana (Lamarck), from the northwest Gulf of Mexico. Journal of Parasitology 61, 1048–1049.CrossRefGoogle Scholar
Weinstein, M (1972) Studies on the Relationship between Sagitta Elegans Verrill and its Endoparasites in the Southwestern Gulf of St. Lawrence (PhD thesis). University of Montreal, Montreal, Canada.Google Scholar
WoRMS (2022) Derogenes varicus (Müller, 1784) Looss, 1901. https://www.marinespecies.org/aphia.php?p=taxdetails&id=109264 on 2022-03-20.Google Scholar
Wright, RR (1907) The plankton of eastern Nova Scotia waters. An account of floating organisms upon which young food-fishes mainly subsist. Report Department Marine Fish Canadian 39, 1–18.Google Scholar
Yamaguti, S (1938) Studies on the helminth fauna of Japan. Part 24. Trematodes of fishes, V. Japanese Journal of Zoology 8, 15–74.Google Scholar
Zelmer, DA and Esch, GW (1998) The infection mechanism of the cystophorous cercariae of Halipegus occidualis (Digenea: Hemiuridae). Invertebrate Biology 117, 281–287.CrossRefGoogle Scholar
Supplementary material: PDF

Krupenko et al. supplementary material

Krupenko et al. supplementary material 1

Download Krupenko et al. supplementary material(PDF)
PDF 94.9 KB
Supplementary material: File

Krupenko et al. supplementary material

Krupenko et al. supplementary material 2

Download Krupenko et al. supplementary material(File)
File 19.1 KB
Supplementary material: File

Krupenko et al. supplementary material

Krupenko et al. supplementary material 3

Download Krupenko et al. supplementary material(File)
File 18 KB
Supplementary material: File

Krupenko et al. supplementary material

Krupenko et al. supplementary material 4

Download Krupenko et al. supplementary material(File)
File 16.1 KB
Supplementary material: File

Krupenko et al. supplementary material

Krupenko et al. supplementary material 5

Download Krupenko et al. supplementary material(File)
File 16.5 KB