Skip to main content
SpringerLink
Log in

Hemiuroidean trematodes from freshwater Patagonian fishes: description of a new species, distribution and molecular phylogeny

  • Fish Parasitology - Original Paper
  • Published:
Parasitology Research Aims and scope Submit manuscript

Abstract

A new trematode species, Derogenes lacustris Tsuchida, Flores, Viozzi, Rauque et Urabe n. sp. (Derogenidae: Derogeninae), from freshwater fishes is described using morphological and molecular approaches in Argentinean Patagonia. D. lacustris is the most common hemiuroidean species in the Limay River basin and parasitizes almost all the native and introduced Patagonian freshwater fish. This new species could be considered as the unique freshwater species in the genus Derogenes Nicoll, 1910. Another hemiuroidean species, Thometrema patagonica Szidat (Archiev Hydrobiol 51: 542–577, 1956) Lunaschi et Drago 2000 (Derogenidae: Halipeginae), is found from Percichthys trucha (Perciformes) in the Neuquén River basin. Its diagnosis and molecular data are provided by the present study. In the molecular analysis of the Patagonian hemiuroideans, T. patagonica composes a group with halipeginean species in the phylogenetic tree of 28S rDNA sequences, while D. lacustris is not included in the same group. D. lacustris also shows low intraspecific variation in COI sequences regardless of the localities or host species.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2-4
Fig. 5-8
Fig. 9
Fig. 10
Fig. 11

Similar content being viewed by others

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.

References

  • Bartoli P, Gibson DI (1991) On Podocotyle scorpaenae, Poracanthium furcatum and Derogenes latus, three poorly known digenean parasites of western Mediterranean teleosts. Syst Parasitol 20:29–46

    Article  Google Scholar 

  • Bray RA, Cribb TH, Barker SC (1993) The Hemiuroidea (Digenea) of pomacentrid fishes (Perciformes) from Heron Island, Queensland, Australia. Syst Parasitol 24:159–184

    Article  Google Scholar 

  • Brinkmann AJ (1967) Some trematodes from marine fishes in the water of Rhodes. Arbok Univ Bergen Mat -Nat Sene 10:2–13

    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  Google Scholar 

  • Curran SS, Overstreet RM, Font W (2002) Thometrema lotzi sp nov (Digenea, Derogenidae) from freshwater and brackish water fishes of Louisiana and Mississippi (USA). Acta Parasitol 47:14–19

    Google Scholar 

  • Detwiler JT, Bos DH, Minchella DJ (2010) Revealing the secret lives of cryptic species: Examining the phylogenetic relationships of echinostome parasites in North America. Mol Phylogenet Evol 55:611–620

    Article  Google Scholar 

  • Gibson DI (2001) Digenea. In: Costello MJ, Emblow C, White RJ (eds) European register of marine species: a check-list of the marine species in Europe and a bibliography of guides to their identification, Collection Patrimoines Naturels, vol 50, pp 136–142

    Google Scholar 

  • Gibson DI (2002) Family Derogenidae Nicoll, 1910. In: Gibson DI, Bray RA, Jones A (eds) Keys to the Trematoda 1. CAB Int Nat Hist Mus, London, pp 351–368

    Chapter  Google Scholar 

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

    Google Scholar 

  • 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  Google Scholar 

  • Jaiswal GP (1967) Investigations on the trematode fauna of the common food fishes of Hyderabad, A. P. Part I. A new species of Derogenes Lühe, 1900, from a freshwater fish, Channa (Ophiocephalus) punctatus. Indian J Helminthol 18:36–44

  • 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  Google Scholar 

  • 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  Google Scholar 

  • Linton E (1940) Trematodes from fishes mainly from the Woods Hole region, Massachusetts. Proc U S Natl Mus 88:1–172

    Article  Google Scholar 

  • Locke SA, Caffara M, Marcogliese DJ, Fioravanti ML (2015) A large-scale molecular survey of Clinostomum (Digenea, Clinostomidae). Zool Scr 44:203–217

    Article  Google Scholar 

  • Looss A (1899) Weitere Beiträge zur Kenntniss der Trematoden-Fauna Aegyptens, zugleich Versuch einer natürlichen Gliederung des Genus Distomum Retzius. Zool Jahrb Syst 12:521–784

    Google Scholar 

  • Looss A (1901) Über einige Distomen der Labriden des Triester Hafens. Centralbl Bakteriol, Parasitenkunde und Infektionskrankheiten. Abt 1, 29: 437–442

  • Lühe M (1900) Über Distomen aus der Gallenblase von Mittelmeerfischen. Zool Anz 23:504–509

    Google Scholar 

  • Lunaschi L (1988) Helmintos Parasitos de Peces de Agua Dulce de la Argentina X. Tres nuevas especies del genero Thometrema Amato, 1968 (Trematoda-Derogenidae). Neotropica 34:23–32

    Google Scholar 

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

    Google Scholar 

  • Manter HW (1934) Some digenetic trematodes from deer-water fish of Tortugas, Florida. Publ Carnegie Instit Wash 435:257–345

    Google Scholar 

  • Manter HW (1954) Some digenetic trematodes from fishes of New Zealand. Trans Roy Soc N Z 82:457–568

    Google Scholar 

  • Melo FTV, Silva JP, Gonçalves EC, Furtado AP, Giese EG, Santos CP, Santos JN (2013) Taxonomic status and redescription of the genus Brasicystis Thatcher, 1979 (Digenea: Didymozoidae). Parasitol Int 62:208–214

    Article  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

  • 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. Parasitol 137:1013–1025

    Article  CAS  Google Scholar 

  • Monticelli FS (1893) Studii sui trematodi endoparassiti: Primo contributo di osservazioni sui distomidi. Zool Jahrb Supplementheft 3, Jena G. Fischer, pp 180-184, 224-225

  • 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  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  Google Scholar 

  • Posada D, Crandall KA (1998) Modeltest: testing the model of DNA substitution. Bioinfomatics 14:817–8818

    Article  CAS  Google Scholar 

  • Rambaut A, Suchard MA, Drummond AJ (2013) Tracer 1.6.0. http://beast.bio.ed.ac.uk. Accessed 16 Sept 2020

  • Rauque CA, Viozzi G, Flores V, Vega R, Waicheim A, Salgado-Maldonado G (2018) Helminth parasites of alien freshwater fishes in Patagonia (Argentina). Int J Parasitol Parasites Wildl 7:369–379

    Article  Google Scholar 

  • Ronquist F, Teslenko M, Mark PVD, Ayres DL, Darling A, Höhna S, Larget B, Liu L, Suchard MA, Huelsenbeck JP (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol 61:539–542

    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  Google Scholar 

  • Shen JW (1989) Studies on the digenetic trematodes of fishes from Jiaozhou Bay. Stud Mar Sin 30:153–162

    Google Scholar 

  • Shen JW (1990a) Description of four new species (Lepocreadiidae and Hemiuridae) and a list of digenetic trematodes of fishes from Yellow Sea. Mar Sci Bull 9:54–63

    Google Scholar 

  • Shen JW (1990b) Digenetic trematodes of fishes from the Changjiang River estuary. Stud Mar Sin 31:115–120

    Google Scholar 

  • Shen JW, Qiu Z (1995) Studies on the trematodes of fishes from the Yellow Sea and the Bo Hai Sea. Sci Press Beijing China, pp 120-121, 174-175

  • 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. Zool Bespozvon 13:191–202

    Google Scholar 

  • Sokolov SG, Atopkin DM, Gordeev II, Shedko MB (2018) Phylogenetic position of the genus Gonocerca Manter, 1925 (Trematoda, Hemiuroidea), based on partial sequences of 28S rRNA gene and a reconsideration of taxonomic status of Gonocercinae Skrjabin et Guschanskaja, 1955. Parasitol Int 67:74–78

    Article  CAS  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. Parasitol 146:596–603

    Article  Google Scholar 

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

    Google Scholar 

  • Tanabe AS (2011) Kakusan4 and Aminosan: two programs for comparing nonpartitioned, proportional and separate models for combined molecular phylogenetic analyses of multilocus sequence data. Mol Ecol Resour 11:914–921

    Article  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  Google Scholar 

  • Wang P (1991) Report on 1 new genus and 6 new species of digenetic trematodes from marine fishes in Pingtan, Fujian Province. Wuyi Sci J 8:131–138

    Google Scholar 

  • WoRMS (2020) Derogenes Lühe, 1900. http://www.marinespecies.org/aphia.php?p=taxdetails&id=108722. Accessed 28 Mar 2020

  • Yamaguti S (1971) Synopsis of digenetic trematodes of vertebrates. Keigaku Publishing Co Tokyo, Vol. 1, pp 285-286, 299-300, 1074.; Vol. 2, pls 349

Download references

Acknowledgements

We thank T. Nakano, Kyoto University, for his kind advice on the Zoological Nomenclature, S. Marquez from INIBIOMA (CONICET - UNCo) for helping us with the DNA extraction and P. Moreno for giving us the material of D. lacustris corresponding to Lake Huechulafquén and Moquehué (Neuquén Province). Samples were taken with the permission of the National Park authorities (Permission No. 935).

Funding

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

Author information

Authors and Affiliations

  1. Division of Environmental Dynamics, Graduate School of Environmental Science, The University of Shiga Prefecture, 2500 Hassaka, Hikone, Shiga, 522–8533, Japan

    Karin Tsuchida

  2. Laboratorio de Parasitología, INIBIOMA (CONICET–Univ. Nac. del Comahue), Quintral 1250, (8400), San Carlos de Bariloche, Río Negro, Argentina

    Verónica Flores, Gustavo Viozzi & Carlos Rauque

  3. Department of Ecosystem Studies, School of Environmental Sciences, The University of Shiga Prefecture, 2500 Hassaka, Hikone, Shiga, 522–8533, Japan

    Misako Urabe

Authors
  1. Karin Tsuchida
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Verónica Flores
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Gustavo Viozzi
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Carlos Rauque
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Misako Urabe
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Karin Tsuchida or Verónica Flores.

Ethics declarations

Conflicts of interest

The authors declare that they have no conflict of interest.

Ethics approval

This is a taxonomic study about fish parasites, and no ethical approval is required.

Consent to participate

This study includes no human cases, and no consent is needed.

Consent for publication

This study includes no human cases, and no consent is needed.

Code availability

This study is not a code-related work.

Additional information

Section Editor: Christoph G. Grevelding

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Karin Tsuchida and Verónica Flores are first co-authors of this paper

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Tsuchida, K., Flores, V., Viozzi, G. et al. Hemiuroidean trematodes from freshwater Patagonian fishes: description of a new species, distribution and molecular phylogeny. Parasitol Res 120, 1219–1232 (2021). https://doi.org/10.1007/s00436-020-06939-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00436-020-06939-2

Keywords

Search

Navigation