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It is marine: distinguishing a new species of Catatropis (Digenea: Notocotylidae) from its freshwater twin

Published online by Cambridge University Press:  22 September 2020

Anna Gonchar Open the ORCID record for Anna Gonchar [Opens in a new window]  and
Kirill V. Galaktionov
Anna Gonchar*
Affiliation:
Department of Invertebrate Zoology, Saint Petersburg State University, Universitetskaya emb., 7–9, Saint Petersburg199034, Russia Laboratory of Parasitic Worms and Protists, Zoological Institute RAS, Universitetskaya emb., 1, Saint Petersburg199034, Russia
Kirill V. Galaktionov
Affiliation:
Department of Invertebrate Zoology, Saint Petersburg State University, Universitetskaya emb., 7–9, Saint Petersburg199034, Russia Laboratory of Parasitic Worms and Protists, Zoological Institute RAS, Universitetskaya emb., 1, Saint Petersburg199034, Russia
*
Author for correspondence: Anna Gonchar, E-mail: [email protected], [email protected]
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Abstract

The morphology of sexual adults is the cornerstone of digenean systematics. In addition, life cycle data have always been significant. The integration of these approaches, supplemented with molecular data, has allowed us to detect a new species that many researchers may have previously seen, but not recognized. Sexual adults from common eiders that we found in northern European seas were extremely similar to other notocotylids, but the discovery of their intermediate host, a marine snail, revealed the true nature of this material. Here we describe sexual adults, rediae and cercariae of Catatropis onobae sp. nov. We discuss how ‘Catatropis verrucosa’ should be regarded, justify designation of the new species C. onobae for our material and explain why it can be considered a cryptic species. The phylogenetic position of C. onobae within Notocotylidae, along with other evidence, highlights the challenges for the taxonomy of the family, for which two major genera appear to be polyphyletic and life cycle data likely undervalued.

Keywords

Catatropiscercariaecryptic speciesDigenealife cycleNotocotylidaeOnoba aculeusSomateria mollissima
Type
Research Article
Information
Parasitology , Volume 148 , Issue 1 , January 2021 , pp. 74 - 83
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Copyright
Copyright © The Author(s), 2020. Published by Cambridge University Press

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References

Assis, JCA, Lopez-Hernández, D, Pulido-Murillo, EA, Melo, AL and Pinto, HA (2019) A morphological, molecular and life cycle study of the capybara parasite Hippocrepis hippocrepis (Trematoda: Notocotylidae). PLoS ONE 14, 9–12.CrossRefGoogle Scholar
Barton, DP and Blair, D (2002) Superfamily Pronocephaloidea Looss, 1899. In Gibson, D, Jones, A and Bray, RA (eds), Keys to Trematoda, Vol. 2. London: CABI, pp. 383–396.Google Scholar
Bayssade-Dufour, C, Albaret, J-L, Fermet-Quinet, H and Farhati, K (1996) Catatropis lagunae n. sp., Trematoda, Notocotylidae, parasite d'oiseaux de mer. The Canadian Field-Naturalist 110, 392–402.Google Scholar
Bayssade-Dufour, C, Jouet, D, Rudolfova, J, Horák, P and Ferté, H (2000) Seasonal morphological variations in bird schistosomes. Parasite 13, 205–214.CrossRefGoogle Scholar
Belopolskaia, MM (1952) Parasite fauna of marine waterfowl. Uchenie Zapiski Leningradskogo Universiteta 141, 127–180.Google Scholar
Besprozvannykh, VV (2006) Life cycle of the trematode Catatropis Hisikui (Notocotylidae) in conditions of Primorsky region. Vestnik Zoologii 40, 267–270.Google Scholar
Besprozvannykh, VV, Ngo, HD, Ha, NV, Hung, NM, Rozhkovan, KV, Ermolenko, AV and Resources, B (2013) Descriptions of digenean parasites from three snail species, Bithynia fuchsiana (Morelet), Parafossarulus Striatulus Benson and Melanoides tuberculata Müller, in North Vietnam. Helminthologia 50, 190–204.CrossRefGoogle Scholar
Blasco-Costa, I, Cutmore, S, Miller, TL and Nolan, MJ (2016) Molecular approaches to trematode systematics: “best practice” and implications for future study. Systematic Parasitology 93, 295–306.CrossRefGoogle Scholar
Boyce, K, Hide, G, Craig, PS, Harris, PD, Reynolds, C, Pickles, A and Rogan, MT (2012) Identification of a new species of digenean Notocotylus Malhamensis n. sp. (Digenea: Notocotylidae) from the bank vole (Myodes Glareolus) and the field vole (Microtus agrestis). Parasitology 139, 1630–1639.CrossRefGoogle Scholar
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.Google Scholar
Cribb, TH (1991) Notocotylidae (Digenea) from the Australian water rat Hydromys chrysogaster Geoffroy, 1804 (Muridae). Systematic Parasitology 18, 227–237.CrossRefGoogle Scholar
Cribb, TH, Bray, RA, Olson, PD and Littlewood, DTJ (2003) Life cycle evolution in the Digenea: a new perspective from phylogeny. Advances in Parasitology 54, 197–254.CrossRefGoogle ScholarPubMed
Darriba, D, Taboada, GL, Doallo, R and Posada, D (2012) Jmodeltest 2: more models, new heuristics and parallel computing. Nature Methods 9, 772.CrossRefGoogle ScholarPubMed
Diaz, JI, Gilardoni, C, Lorenti, E and Cremonte, F (2020) Notocotylus Primulus n. sp. (Trematoda: Notocotylidae) from the crested duck Lophonetta specularioides (Aves, Anatidae) from Patagonian coast, southwestern Atlantic Ocean. Parasitology International 74, 101976.CrossRefGoogle ScholarPubMed
Dubois, G (1951) Etude des trématodes Nord-Américains de la collection E.L. Schiller et révision du genre Notocotylus Diesing, 1839. Bulletin de la Société Neuchâteloise des Sciences Naturelles 74, 41–76.Google Scholar
Dvoryadkin, V (1987) Morphology and life cycle of Catatropis morosovi. Helminth and Diseases Caused by Them. Vladivostok: DVNC USSR Ac. Sci. Publ., pp. 29–33.Google Scholar
Erkina, NA (1953) The life cycle of Catatropis verrucosa (Frölich, 1789). In Skrjabin, KI (ed.), Trematodes of Animals and Man. Principles of Trematodology, Vol. 8. Moscow: Publishing House of the USSR Academy of Sciences, pp. 106–117.Google Scholar
Filimonova, LV (1985) Tremarodes of the USSR Fauna. Notocotylids. Moscow: Nauka.Google Scholar
Flores, V and Brugni, N (2003) Catatropis Chilinae n. sp. (Digenea: Notocotylidae) from Chilina Dombeiana (Gastropoda: Pulmonata) and notes on its life-cycle in Patagonia, Argentina. Systematic Parasitology 54, 89–96.CrossRefGoogle ScholarPubMed
Flores, V and Brugni, N (2006) Catatropis hatcheri n. sp. (Digenea: Notocotylidae) from Heleobia hatcheri (Prosobranchia: Hydrobiidae) and notes on its life-cycle in Patagonia, Argentina. Systematic Parasitology 63, 111–118.CrossRefGoogle ScholarPubMed
Fraija-Fernandez, N, Olson, PD, Crespo, EA, Raga, JA, Aznar, FJ and Fernandez, M (2015) Independent host switching events by digenean parasites of cetaceans inferred from ribosomal DNA. International Journal for Parasitology 45, 167–173.CrossRefGoogle ScholarPubMed
Frölich, JA (1789) Beschreibungen einiger neuer Eingeweidewürmer. Naturforscher 24, 10–162.Google Scholar
Galaktionov, KV and Blasco-Costa, I (2018) Microphallus ochotensis sp. nov. (Digenea, Microphallidae) and relative merits of two-host microphallid life cycles. Parasitology Research 117, 1051–1068.CrossRefGoogle ScholarPubMed
Galaktionov, K and Skirnisson, K (2000) Digeneans from intertidal molluscs of SW Iceland. Systematic Parasitology 47, 87–101.CrossRefGoogle ScholarPubMed
Georgieva, S, Faltýnková, A, Brown, R, Blasco-Costa, I, Soldánová, M, Sitko, J, Scholz, T and Kostadinova, A (2014) Echinostoma “Revolutum” (Digenea: Echinostomatidae) species complex revisited: species delimitation based on novel molecular and morphological data gathered in Europe. Parasites and Vectors 7, 1–18.Google ScholarPubMed
Gonchar, A and Galaktionov, KV (2017) Life cycle and biology of Tristriata anatis (Digenea: Notocotylidae): morphological and molecular approaches. Parasitology Research 116, 45–59.CrossRefGoogle ScholarPubMed
Gonchar, A and Galaktionov, KV (2020) New data support phylogeographic patterns in a marine parasite Tristriata anatis Digenea: Notocotylidae. Journal of Helminthology 94, e79. doi: 10.1017/S0022149X19000786.CrossRefGoogle Scholar
Gonchar, A, Jouet, D, Skírnisson, K, Krupenko, D and Galaktionov, KV (2019) Transatlantic discovery of Notocotylus atlanticus (Digenea: Notocotylidae) thanks to life cycle data. Parasitology Research 118, 1445–1456.CrossRefGoogle Scholar
Gorbushin, AM and Levakin, IA (1999) The effect of trematode parthenitae on the growth of Onoba Aculeus, Littorina saxatilis and L. obtusata (Gastropoda: Prosobranchia). Journal of the Marine Biological Association of the UK 79, 273–280.CrossRefGoogle Scholar
Guindon, S and Gascuel, O (2003) A simple, fast and accurate method to estimate large phylogenies by maximum-likelihood. Systematic Biology 52, 696–704.CrossRefGoogle ScholarPubMed
Guindon, S, Dufayard, J-F, Lefort, V, Anisimova, M, Hordijk, W and Gascuel, O (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Systematic Biology 59, 307–321.CrossRefGoogle ScholarPubMed
Guryanova, E and Ushakov, P (1928) On the fauna of Chernaya Inlet of Novaya Zemlya. In Derjugin, K (ed.), Studies of the Seas of the USSR. Leningrad: Leningrad Hydrological Institute, pp. 3–72.Google Scholar
Hanelt, AB (2009) Hyperparasitism by Paragordius varius (Nematomorpha: Gordiida) Larva of Monostome Redia (Trematoda: Digenea). Journal of Parasitology 95, 242–243.CrossRefGoogle Scholar
Hernández-Mena, DI, Pinacho-Pinacho, CD, García-Varela, M, Mendoza-Garfias, B and Pérez-Ponce de León, G (2019) Description of two new species of allocreadiid trematodes (Digenea: Allocreadiidae) in middle American freshwater fishes using an integrative taxonomy approach. Parasitology Research 118, 421–432.CrossRefGoogle ScholarPubMed
Izrailskaia, A, Besprozvannykh, V, Tatonova, Y, Nguyen, H and Ngo, H (2019) Developmental stages of Notocotylus Magniovatus Yamaguti, 1934, Catatropis vietnamensis n. sp., Pseudocatatropis Dvoryadkini n. sp., and phylogenetic relationships of Notocotylidae Lühe, 1909. Parasitology Research 118, 469–481.CrossRefGoogle ScholarPubMed
Joyeux, C (1922) Recherches sur les Notocotyles. Bulletins de la Société de Pathologie Exotique 15, 331–343.Google Scholar
Kanev, I and Vasiliev, I (1986) Identification of Catatropis verrucosa (Frölich, 1789) (=pro parte to Pseudocatatropis joyeaxi gen. and sp. nov comb.). Proceedings of the 5th International Helminthological Symposium Organised by Helminthological Institute of the Czechoslovak Academy of Sciences in Kosice, 22– 24 October 1986, High Tatra, pp. 5–6.Google Scholar
Kanev, I, Vassilev, I, Dimitrov, V and Radev, V (1994) Life-cycle, delimitation and redescription of Catatropis verrucosa (Frölich, 1789) Odhner, 1905 (Trematoda: Notocotylidae). Systematic Parasitology 29, 133–148.CrossRefGoogle Scholar
Kinsella, JM and Tkach, VV (2005) Notocotylus fosteri sp. nov. (Trematoda, Notocotylidae) from the rice rat, Oryzomys palustris in Florida. Acta Parasitologica 50, 194–198.Google Scholar
Koch, M (2002) First record and description of Catatropis indicus Srivastava 1935 (Digenea: Notocotylidae) in Australia. Memoirs-Queensland Museum 48, 147–154.Google Scholar
Krupenko, D and Gonchar, A (2017) Ventral concavity and musculature arrangement in notocotylid maritae (Digenea: Notocotylidae). Parasitology International 66, 660–665.CrossRefGoogle Scholar
Kulachkova, VG (1966) Trematodes of the long-tailed duck (Clangula hyemalis L.) in Kandalaksha Bay of the White Sea. Trudy GELAN 17, 82–87.Google Scholar
Luton, K, Walker, D and Blair, D (1992) Comparisons of ribosomal internal transcribed spacers from two congeneric species of flukes (Platyhelminthes: Trematoda: Digenea). Molecular and Biochemical Parasitology 56, 323–327.CrossRefGoogle Scholar
Miller, MA, Schwartz, T, Pickett, BE, He, S, Klem, EB, Scheuermann, RH, Passarotti, M, Kaufman, S and Oleary, MA (2015) A RESTful API for access to phylogenetic tools Via the CIPRES science gateway. Evolutionary Bioinformatics 11, 43–48.CrossRefGoogle ScholarPubMed
Odening, K (1966) Physidae und Planorbidae als Wirte in den Lebenszyklen einheimischer Notocotylidae (Trematoda: Paramphistomida). Zeitschrift für Parasitenkunde 27, 210–239.CrossRefGoogle Scholar
Odhner, T (1905) Die Trematoden des arktischen Gebietes. Jena: Gustav Fischer.Google Scholar
Olson, PD, Cribb, TH, Tkach, VV, Bray, RA and Littlewood, DTJ (2003) Phylogeny and classification of the Digenea. International Journal for Parasitology 33, 733–755.CrossRefGoogle ScholarPubMed
Rohde, K and Onn, LF (1967) Life cycle of Catatropis indica Srivastava, 1935 (Trematoda: Notocotylidae). Zeitschrift für Parasitenkunde 29, 137–148.CrossRefGoogle Scholar
Ronquist, F and Huelsenbeck, JP (2003) Mrbayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics Applications Note 19, 1572–1574.CrossRefGoogle ScholarPubMed
Rothschild, M (1938) Notes on the classification of cercariae of the superfamily Notocotyloidea (Trematoda), with special reference to the excretory system. Novitates Zoologicae 16, 75–83.Google Scholar
Schneider, CA, Rasband, WS and Eliceiri, KW (2012) NIH Image to ImageJ: 25 years of image analysis. Nature Methods 9, 671–675.CrossRefGoogle ScholarPubMed
Schuster, RK and Wibbelt, G (2012) Catatropis pakistanensis n. sp. (Trematoda: Notocotylidae) from Northern shovelers, Anas clypeata (Anatidae: Aves) from Pakistan with some remarks on the history of Catatropis species. Helminthologia 49, 43–48.CrossRefGoogle Scholar
Skirnisson, K and Galaktionov, KV (2002) Life cycles and transmission patterns of seabird digeneans in SW Iceland. Sarsia 87, 144–151.CrossRefGoogle Scholar
Soldánová, M, Georgieva, S, Roháčová, J, Knudsen, R, Kuhn, JA, Henriksen, EH, Siwertsson, A, Shaw, JC, Kuris, AM, Amundsen, PA, Scholz, T, Lafferty, KD and Kostadinova, A (2017) Molecular analyses reveal high species diversity of trematodes in a sub-Arctic lake. International Journal for Parasitology 47, 327–345.CrossRefGoogle 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
Tkach, VV, Pawlowski, J, Mariaux, J, Swiderski, Z, Litlewood, DTJ and Bray, RA (2001) Molecular phylogeny of the suborder Plagiorchiata and its position in the system of Digenea. In Littlewood DTJ and Bray RA (eds). Interreleationships of the Platyhelminthes. London, UK: CRC Press, pp. 186–193.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
Waltho, C and Coulson, J (2015) The Common Eider. London: T & AD Poyser.Google Scholar
WoRMS Editorial Board (2020) World Register of Marine Species. doi: 10.14284/170.CrossRefGoogle Scholar
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