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A new species of hemiuroidean trematode from Hatcheria macraei (Siluriformes, Trichomycteridae) and Heleobia hatcheri (Gastropoda, Cochliopidae) in a Patagonian River

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Abstract

A new hemiuroidean species, Genarchella pichileufuensis n. sp. (Derogenidae: Halipeginae), was found in the stomach of the siluriform freshwater fish, Hatcheria macraei (Girard, 1855), in the Pichileufu River, Patagonia, Argentina. Its rediae with immature cystophorous cercariae were found in the snail Heleobia hatcheri (Pilsbry, 1911) in the same site. The present new species is morphologically featured by having a cyclocoel in the hindbody unlike the other species of the genus. The characteristics of this species allowed us to amend the diagnosis of the genus Genarchella as follows: cyclocoel present or absent; testes symmetrical to tandem; ootype pouch present. In the phylogenetic analysis, G. pichileufuensis forms a well-supported clade with Genarchella spp. recovered from Mexican freshwater fishes. This clade is included in the cluster of representatives of the subfamily Halipeginae. So far, three hemiuroidean species, Thometrema patagonica (Szidat, 1956), Derogenes lacustris Tsuchida, Flores, Viozzi, Rauque et Urabe, 2021 and G. pichileufuensis n. sp., have been reported from freshwater fishes in Argentinean Patagonia.

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Data availability

Specimens used in this study were deposited in the Museo Argentino de Ciencias Naturales Bernardino Rivadavia (Buenos Aires, Argentina), and the sequence data are available in the INSD.

Code availability

This study is not a code-related work.

References

  • Brooks DR, Mayes MA, Thorson TB (1979) Paravitellotrema overstreeti sp. n. (Digenea: Hemiuridae) from the Colombian freshwater stingray Potamotrygon magdalenae Dumeril. Proc Helminthol Soc Wash 46:52–54

    Google Scholar 

  • Calhoun DM, Curran SS, Pulis EE, Provaznik JM, Franks JS (2013) Hirudinella ventricosa (Pallas, 1774) Baird, 1853 represents a species complex based on ribosomal DNA. Syst Parasitol 86:197–208

    Article  PubMed  Google Scholar 

  • Ditrich O, Scholz T, Aguirre-Macedo L, Vargas-Vázquez J (1997) Larval stages of trematodes from freshwater molluscs of the Yucatan Peninsula, Mexico. Folia Parasitol 44:109–127

    Google Scholar 

  • Gibson DI, Bray RA (1979) The Hemiuroidea: terminology, systematics and evolution. Bull Br Mus (Nat Hist) Zool 36:35–146

    Article  Google Scholar 

  • Gibson DI (2002) Family Derogenidae Nicoll, 1910 In: Gibson DI, Jones A, Bray RA (eds) Keys to the Trematoda. Vol. 1. CABI Publishing, Wallingford, UK, and The Natural History Museum, London xvi, pp 351–368

  • Hasegawa M, Kishino H, Yano T (1985) Dating the human-ape split by a molecular clock of mitochondrial DNA. J Mol Evol 22:160–174

    Article  CAS  PubMed  Google Scholar 

  • Hoffman GL (1999) Parasites of North American freshwater fishes. Cornell University Press, USA, 539 pp

  • Kimura M (1980) A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120

    Article  CAS  PubMed  Google Scholar 

  • Kohn A, Fernandes BMM, Gibson DI, Fróes OM (1990) On the Brazilian species of halipegine genera (Trematoda: Derogenidae) from fishes, with new morphological data, hosts and synonyms. Syst Parasitol 16:201–211

    Article  Google Scholar 

  • Kohn A, Fernandes BMM, Cohen SC (2007) South American trematodes parasites of fishes. CNPq and FIOCRUZ, 318 pp

  • Kumar S, Stecher G, Tamura K (2016) MEGA 7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lunaschi LI, Drago FB (2000) Thometrema patagonica (Szidat, 1956) n. comb. para Derogenes patagonicus (Szidat) Yamaguti, 1971 (Trematoda Derogenidae). Physis Buenos Aires Secc B 58(134–135):43–46

    Google Scholar 

  • Madhavi R (1978) Life history of Genarchopsis goppo Ozaki, 1925 (Trematoda: Hemiuridae) from the freshwater fish Channa punctata. J Helminthol 52:251–259

    Article  CAS  PubMed  Google Scholar 

  • Martín PR (2002) Evidence for parthenogenesis and natural imposex in the Patagonian freshwater snail Heleobia hatcheri (Gastropoda: Hydrobiidae). J Molluscan Stud 68:291–295

    Article  Google Scholar 

  • Martorelli SR (1989) Estudios parasitológicos en biotopos lénticos de la República Argentina y desarrollo del ciclo biológico monoxeno de la metacercaria progenética de Genarchella genarchella Travassos, 1928 (Digenea, Hemiuridae) parásita Littoridina parchappei (Mollusca, Hidrobiidae). Rev Mus La Plata 14:109–117

    Google Scholar 

  • Miura O, Kuris AM, Torchin ME, Hechinger RF, Dunham EJ, Chiba S (2005) Molecular-genetic analysis reveal cryptic species of trematodes in the intertidal gastropod, Batillaria cumingi (Crosse). Int J Parasitol 35:793–801

    Article  CAS  PubMed  Google Scholar 

  • Mladineo I, Bott NJ, Nowak BF, Block BA (2010) Multilocus phylogenetic analyses reveal that habitat selection drives the speciation of Didymozoidae (Digenea) parasitizing Pacific and Atlantic bluefin tunas. Parasitology 137:1013–1025

    Article  CAS  PubMed  Google Scholar 

  • Olson PD, Cribb TH, Tkach VV, Bray RA, Littlewood DTJ (2003) Phylogeny and classification of the Digenea (Platyhelminthes: Trematoda). Int J Parasitol 33:733–755

    Article  CAS  PubMed  Google Scholar 

  • Ostrowski de Núñez M, Arredondo NJ, Gil de Pertierra AA (2017) Adult trematodes (Platyhelminthes) of freshwater fishes from Argentina: a checklist. Rev Suisse Zool 124:91–113

    Google Scholar 

  • Pérez-Ponce de León G, Hernández-Mena DI (2019) Testing the higher-level phylogenetic classification of Digenea (Platyhelminthes, Trematoda) based on nuclear rDNA sequences before entering the age of the ‘next-generation’ Tree of Life. J Helminthol 93:260–276

    Article  PubMed  Google Scholar 

  • Rumi A, Gregoric DEG, Núñez V, Darrigran GA (2008) Malacología Latinoamericana. Moluscos de agua dulce de Argentina. Rev Biol Trop 56:77–111

    PubMed  Google Scholar 

  • Scholz T, Salgado-Maldonado G (1994) On Genarchella isabellae (Digenea: Derogenidae) from cichlid and pimelodid fishes in Mexico. J Parasitol 80:1013–1017

    Article  CAS  PubMed  Google Scholar 

  • Scholz T, Vargas-Vazquez J, Salgado-Maldonado G (1995) Revision of Genarchella species (Digenea: Derogenidae) parasitizing freshwater fishes in Mexico and Central America. J Nat Hist 29:1403–1417

    Article  Google Scholar 

  • Schrandt MN, Andres MJ, Powers SP, Overstreet RM (2016) Novel infection site and ecology of cryptic Didymocystis sp. (Trematoda) in the fish Scomberomorus maculatus. J Parasitol 102:297–305

    Article  PubMed  Google Scholar 

  • Shimazu T (1995) Trematodes of the genus Genarchopsis (Digenea, Derogenidae, Halipeginae) from freshwater fishes of Japan. Proc Jap Soc Syst Zool 54:1–18

    Google Scholar 

  • Shimazu T (2015) Digeneans parasitic in freshwater fishes (Osteichthyes) of Japan. IV. Derogenidae. Bull Br Mus (Nat Hist) Zool 41:77–103

    Google Scholar 

  • Shimazu T, Urawa S, Coria CO (2000) Four species of digeneans, including Allocreadium patagonicum sp. n. (Allocreadiidae), from freshwater fishes of Patagonia, Argentina. Folia Parasitol 47:111–117

    Article  CAS  Google Scholar 

  • Sokolov SG, Gordeev II, Atopkin DM (2016) Redescription of trematode Gonocerca muraenolepisi Paruchin et Ljadov, 1979 (Hemiuroidea: Derogenidae), a body cavity parasite of Antarctic fishes, with a discussion of its phylogenetic position. Invert Zool 13:191–202

    Article  Google Scholar 

  • Sokolov SG, Atopkin DM, Urabe M, Gordeev II (2019) Phylogenetic analysis of the superfamily Hemiuroidea (Platyhelminthes, Neodermata: Trematoda) based on partial 28S rDNA sequences. Parasitology 146:596–603

    Article  PubMed  Google Scholar 

  • Sokolov SG, Atopkin DM, 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. Mar Biol Res. https://doi.org/10.1080/17451000.2021.1891252

    Article  Google Scholar 

  • Szidat L (1956a) Über die Parasitenfauna von Percichthys trucha (Cuv. & Val.) Girard der patagonischen Gewässer und die Beziehungen des Wirtsfisches und seiner Parasiten zur paläarktischen Region. Arch Hydrobiol 51:542–577

    Google Scholar 

  • Szidat L (1956b) Über den Entwicklungszyklus mit progenetischen Larvenstadien (Cercariaeen) von Genarchella genarchella Travassos, 1928 (Trematoda: Hemiuridae) und die Möglichkeit einer hormonalen Beeinflussung der Parasiten durch ihle Wirtstierre. Z Tropenmed Parasitol 7:132–153

    CAS  PubMed  Google Scholar 

  • Tkach VV, Littlewood DTJ, Olson PD, Kinsella JM, Swiderski Z (2003) Molecular phylogenetic analysis of the Microphalloidea Ward, 1901 (Trematoda: Digenea). Syst Parasitol 56:1–15

    Article  PubMed  Google Scholar 

  • Travassos L, Artigas P, Pereira C (1928) Fauna helminthologica dos peixes de água doce do Brasil. Arch Inst Biol 1:5–68

    Google Scholar 

  • Tsuchida K, Flores V, Viozzi G, Rauque C, Urabe M (2021) Hemiuroidean trematodes from freshwater Patagonian fishes: description of a new species, distribution and molecular phylogeny. Parasitol Res 120:1219–1232

    Article  PubMed  Google Scholar 

  • Urabe M, Shimazu T (2013) Allogenarchopsis gen. nov. (Digenea, Derogenidae, Halipeginae) parasitic in the intestine of freshwater fishes: a molecular and morphological study of adult and cercarial forms. Bull Natl Mus Nat Sci Ser A 39:119–130

    Google Scholar 

  • Urabe M, Nishimura T, Shimazu T (2012) Taxonomic revision of three species of the genus Genarchopsis (Digenea:Hemiuroidea: Derogenidae) in Japan by molecular phylogenetic analyses. Parasitol Int 61:554–560

    Article  PubMed  Google Scholar 

  • Watson DE (1976) Digenea of fishes from Lake Nicaragua. Invest Ichthyofauna Nicaraguan Lakes 15:251–260

    Google Scholar 

  • Wu Y, Gao J, Cheng X, Xie M, Yuan X, Liu D, Song R (2020) Characterization and comparative analysis of the complete mitochondrial genome of Azygia hwangtsiyui Tsin, 1933 (Digenea), the first for a member of the family Azygiidae. Zookeys 945:1–16

    Article  PubMed  PubMed Central  Google Scholar 

  • Yamaguti S (1958) Systema Helminthum I. The digenetic trematodes of vertebrates. Part I. Interscience Publishers Inc., New York, 1575 pp

  • Yamaguti S (1971) Synopsis of digenetic trematodes of vertebrates. Keigaku Publishing Co., Tokyo, Vol. 1 and 2, 1074 pp

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Acknowledgements

We thank S. Marquez from INIBIOMA (CONICET—UNCo) for helping us with the DNA extraction. We are grateful to Dr. G. Pérez-Ponce de León for providing us with information on Mexican Genarchella species through personal communication. We are also grateful to Drs. S. G. Sokolov and D. M. Atopkin for helping us with their sequence data. Samples were taken with the permission of National Park authorities (Permission No. 935). Financial support was provided by CONICET PIP 11220150100477 and a grant from Universidad Nacional del Comahue (B–225). We also thank the anonymous reviewers and editor whose comments improved our manuscript.

Funding

This study was funded by CONICET PIP 11220150100477 and a grant from Universidad Nacional del Comahue (B-225).

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Correspondence to Karin Tsuchida.

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This is a taxonomical study for fish parasites, and no ethical approval is required.

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Tsuchida, K., Urabe, M., Viozzi, G. et al. A new species of hemiuroidean trematode from Hatcheria macraei (Siluriformes, Trichomycteridae) and Heleobia hatcheri (Gastropoda, Cochliopidae) in a Patagonian River. Parasitol Res 120, 2523–2532 (2021). https://doi.org/10.1007/s00436-021-07210-y

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