Abstract
During a parasitological survey, specimens belonging to the genus Hedruris (Nematoda: Hedruridae) were found in the stomach of Synbranchus marmoratus Bloch from the Paraná Guazú River, Paraná River basin (Argentina). Comparative morphological studies with its congeners showed that these nematodes belonged to a new species, herein described as Hedruris anguila sp. nov. The new species can be distinguished from remaining Hedruris species by the pseudolabia size, the morphology and size of spicules, the length of female caudal hook, the shape and size of eggs and the particular morphology of the male tail. Hedruris anguila sp. nov. closely resembles Hedruris bifida Rossin & Timi, 2016 and H. suttonae Brugni & Viozzi, 2010, both also described from fish hosts, in the arrangement of caudal papillae and morphology of eggs, but differ in the size of female hook and spicules, and the number of caudal papillae in males. The main morphological features, host range and geographical distribution of all species in the genus Hedruris species are analyzed and discussed. This is the first report of a representative of the family Hedruridae parasitizing a species of Synbranchidae and the eleventh report of the genus Hedruris for a fish host. The number of valid species of Hedruris described was increased to 26, including the new species; 11 for the Neotropical Region and represent the third species found in fish host from Argentina. Based on morphological analysis, the speciation process probably occurred first in Gondwana and the non-mammillated eggs could be an ancestral morphological character. The diet of Synbranchus marmoratus and values of prevalence and mean intensity could indicate that this host species is a true definitive host for this nematode.
References
- Acosta, A.A., Caffara, M., Fioravanti, M.L., Utsunomia, R., Zago, A.C., Franceschini, L. & da Silva, R.J. (2016) Morphological and molecular characterization of Clinostomum detruncatum (Trematoda: Clinostomidae) metacercariae infecting Synbranchus marmoratus. Journal of Parasitology, 102, 151–156. https://doi.org/10.1645/15-773 DOI: https://doi.org/10.1645/15-773
- Anderson, R., Chabaud, A. & Willmott, S. (2009) Keys to the nematode parasites of vertebrates: archival volume. CABI Publising. Wallingford, 463 pp. https://doi.org/10.1079/9781845935726.0000 DOI: https://doi.org/10.1079/9781845935726.0000
- Andrews, J.R.H. (1974) A new species of Hedruris (Nematoda: Spirurida) from the skink Leiolopsima smithi. New Zealand Journal of Zoology, 1, 329–332. https://doi.org/10.1080/03014223.1974.9517837 DOI: https://doi.org/10.1080/03014223.1974.9517837
- Arredondo, N.J., Vieira Alves, P. & Gil de Pertierra, A.A. (2017) A new genus of proteocephalid tapeworm (Cestoda) from the marbled swamp eel Synbranchus marmoratus Bloch (Synbranchiformes: Synbranchidae) in the River Paraná basin, Argentina. Folia Parasitologica, 64, 015. https://doi.org/10.14411/fp.2017.015 DOI: https://doi.org/10.14411/fp.2017.015
- Baker, M.R. (1982) Systematics and zoogeography of three new nematode parasites of the frog Breviceps sylvestris Fitz Simons from South Africa. Canadian Journal of Zoology, 60, 3134–3142. https://doi.org/10.1139/z82-398 DOI: https://doi.org/10.1139/z82-398
- Baker, M.R. (1986) Revision of Hedruris Nitzsch (Nematoda: Habronematoidea) from aquatic vertebrates of North America. Canadian Journal of Zoology, 64, 1567–1572. https://doi.org/10.1139/z86-234 DOI: https://doi.org/10.1139/z86-234
- Baylis, H.A. (1931) VIII.—A species of the Nematode genus Hedruris occurring in the trout in New Zealand. Annals and Magazine of Natural History, 7, 105–114. https://doi.org/10.1080/00222933108673285 DOI: https://doi.org/10.1080/00222933108673285
- Baird, W. (1858) Description of two new species of Entozoa. Proceedings of the Zoological Society of London, 26, 224–225. https://doi.org/10.1111/j.1469-7998.1858.tb06366.x DOI: https://doi.org/10.1111/j.1469-7998.1858.tb06366.x
- Bendezú, L.S. (1974) Nueva especie del género Hedruris Nitzsch, 1821 Nematode Parásito de Batrachophrynus brachydactylus Peters, 1873. Revista Ciencias Universidad Nacional Mayor de San Marcos, 70, 45–51.
- Brugni, N.L. & Viozzi, G.P. (2010) A new hedrurid species (Nematoda) from galaxiid fishes in Patagonia (Argentina), and infection of amphipods as intermediate host. Journal of Parasitology, 96, 109–115. https://doi.org/10.1645/GE-2251.1 DOI: https://doi.org/10.1645/GE-2251.1
- Bursey, C.R. & Goldberg, S.R. (2000) Hedruris hanleyae n. sp. (Nematoda: Hedruridae) from Hemidactylus garnotii (Sauria: Gekkonidae) from the Cook Islands. Oceania. Journal of Parasitology, 86, 556–559. https://doi.org/10.1645/0022-3395(2000)086[0556:HHNSNH]2.0.CO;2 DOI: https://doi.org/10.1645/0022-3395(2000)086[0556:HHNSNH]2.0.CO;2
- Bursey, C.R. & Goldberg, S.R. (2007) New species of Hedruris (Nematoda: Hedruridae), Anuracanthorhynchus lutzi (Hamann, 1891) n. comb. and other helminths in Lithobates warszewitschii (Anura: Ranidae) from Costa Rica. Caribbean Journal of Science, 43, 1–10. https://doi.org/10.18475/cjos.v43i1.a2 DOI: https://doi.org/10.18475/cjos.v43i1.a2
- Chandler, A.C. (1919) On a species of Hedruris occurring commonly in the western newt, Notophthalmus torosus. Journal of Parasitology, 5, 116–122. https://doi.org/10.2307/3271163 DOI: https://doi.org/10.2307/3271163
- Chatin, M.J. (1876) Etudes helminthologiques. Deuxième serie. Comptes Rendus de l’Association Francaise pour l’Avancement des Sciences, Paris, 4, 801–805.
- Fernández, E.M., Ferriz, R.A., Bentos, C.A. & López, G.R. (2012) Dieta y ecomorfología de la ictiofauna del arroyo Manantiales, provincia de Buenos Aires, Argentina. Revista del Museo Argentino de Ciencias Naturales, 14, 1–13. https://doi.org/10.22179/REVMACN.14.206 DOI: https://doi.org/10.22179/REVMACN.14.206
- Fernandez, R.V., Tourne, M.L. & Guerrero, D.C. (2019) Parvaprostatum synbranchi n. gen. n. sp. (Trematoda: Diplostomida), parásitos de la anguila Synbranchus marmoratus Bloch, 1795 en Uruguay. Neotropical Helminthology, 13, 151–160. https://doi.org/10.24039/rnh2019132636 DOI: https://doi.org/10.24039/rnh2019132636
- Freitas, J.F.T. & Lent, H. (1941) Contribuicao ao estudo do genero Hedruris Nitzsch, 1821 (Nematoda). Papeis Avulsos de Zoologia Universidade de Sao Paulo, Museu de Zoologia, 1, 121–142.
- Froese, R. & Pauly, D. (Eds.) (2022) FishBase. World Wide Web electronic publication. http://www.fishbase.org (accessed 30 August 2022)
- Graham, J.T. (1981) Burrowing and amphibious life of the swamp eel Synbranchus marmoratus. American Zoologist, 21, 995.
- Hasegawa, H. (1989) Neoentomelas asatoi gen. et sp. n. (Nematoda: Rhabdiasidae) and Hedruris miyakoensis sp. n. (Nematoda: Hedruridae) from skinks of the Ryukyu Archipelago, Japan. Proceedings of the Helminthological Society of Washington, 56, 145–150.
- Huyse, T., Poulin, R. & Theron, A. (2005) Speciation in parasites: a population genetics approach. Trends in Parasitology, 21, 469–475. https://doi.org/10.1016/j.pt.2005.08.009 DOI: https://doi.org/10.1016/j.pt.2005.08.009
- Ibañez, H.N. & Córdova, B.E. (1976) Cuatro especies nuevas de nematodos del sur del Perú y redescripción de Hedruris orestiae Moniez, 1889. Memorias do Instituto Oswaldo Cruz, 74 (3–4), 231–254. https://doi.org/10.1590/S0074-02761976000300004 DOI: https://doi.org/10.1590/S0074-02761976000300004
- Johnston, T.H. & Mawson, P.M. (1941) Some nematodes from Kangaroo Island, South Australia. Records of the South Australian Museum, 7, 145–148.
- Jones, H.I. (2013) Gastrointestinal nematodes from three species of leaf-tailed geckos (Reptilia: Saltuarius spp.), with descriptions of new species of Skrjabinodon (Oxyuroidea: Pharyngodonidae) and Hedruris (Habronematoidea: Hedruridae). Comparative Parasitology, 80, 47–59. https://doi.org/10.1654/4590.1 DOI: https://doi.org/10.1654/4590.1
- Jones, H.I. & Resasco, J. (2016) A new species of Hedruris (Nematoda: Hedruridae) from the Australian Skink Lampropholis guichenoti (Reptilia: Scincidae). Comparative Parasitology, 83, 173–177. https://doi.org/10.1654/4806i.1 DOI: https://doi.org/10.1654/4806i.1
- Junges, C.M., Lajmanovich, R.C., Peltzer, P.M., Attademo, A.M. & Bassó, A. (2010) Predator–prey interactions between Synbranchus marmoratus (Teleostei: Synbranchidae) and Hypsiboas pulchellus tadpoles (Amphibia: Hylidae): Importance of lateral line in nocturnal predation and effects of fenitrothion exposure. Chemosphere, 81, 1233–1238. https://doi.org/10.1016/j.chemosphere.2010.09.035 DOI: https://doi.org/10.1016/j.chemosphere.2010.09.035
- Kurochkin, Y. . & Korotaeva, V.D. (1974) A new nematode, Hedruris marinus (Hedruridae, Spirurata) from the stomach of marine fish. Izvestiya Tikhookeanskogo Nauchno Issledovatel’ skogo Instituta Rybnogo Khozyaistva i Okeanografii TINRO Parazity morskikh zhivotnykh, 88, 69–71.
- Linstow, O. (1909) Hedruris squamata n. sp. Arch. Naturgesch, 75, 63–66.
- Lo Nostro, F.L. & Guerrero, G.A. (1996) Presence of primary and secondary males in a population of the protogynous Synbranchus marmoratus. Journal of Fish Biology, 49, 788–800. https://doi.org/10.1111/j.1095-8649.1996.tb00079.x DOI: https://doi.org/10.1111/j.1095-8649.1996.tb00079.x
- Luque, J.L., Vieira, F.M., Herrmann, K., King, T.M., Poulin, R. & Lagrue, C. (2010) New evidence on a cold case: trophic transmission, distribution and host-specificity in Hedruris spinigera (Nematoda: Hedruridae). Folia Parasitologica, 57, 223–231. https://doi.org/10.14411/fp.2010.029 DOI: https://doi.org/10.14411/fp.2010.029
- Mateo, E. (1971) Nematodes de peces del Lago Titicaca. II. Hedruris basilichtensis, nueva especie de la familia Hedruridae Railliet, 1916. Revista Villareal, 1, 81–84.
- Moniez, R. (1889) Recherches sur le Genre Hedruris: À propos d’une espèce nouvelle, Hedruris orestiae. Revue Biologique du Nord de la France, 1, 361–385.
- Moravec, F. (1998) Nematodes of freshwater fishes of the Neotropical region. Academia, Praha, 464 pp.
- Morishita, K. (1926) Studies on some nematode parasites of frogs and toads in Japan, with notes on their distribution and frequency. Journal of the Faculty of Science, Imperial University of Tokyo, 4, 1–32.
- Nitzsch, C.L. (1821) Ascaris. Allgemeine Encyclopadie der Wissenschaften und Kunste, 6, 44–49.
- Olson, D.M., Dinerstein, E., Wikramanayake, E.D., Burgess, N.D., Powell, G.V.N., Underwood, E.C., D’Amico, J.A., Itoua, I., Strand, H.E., Morrison, J.C., Loucks, C.J., Allnutt, T.F., Ricketts, T.H., Kura, Y., Lamoreux, J.F., Wettengel, W.W., Hedao, P. & Kassem, K.R. (2001) Terrestrial ecoregions of the world: A New Map of Life on Earth. A new global map of terrestrial ecoregions provides an innovative tool for conserving biodiversity. BioScience, 51, 933–938. https://doi.org/10.1641/0006-3568(2001)051[0933:TEOTWA]2.0.CO;2 DOI: https://doi.org/10.1641/0006-3568(2001)051[0933:TEOTWA]2.0.CO;2
- Palumbo, E., Servian, A., Sánchez, R. & Diaz, J. I. (2020) A new species of Hedruris (Nematoda: Hedruridae) from freshwater turtles, its life cycle and biogeographic distribution of the genus. Journal of Helminthology, 94 (e93), 1–11. https://doi.org/10.1017/S0022149X19000877 DOI: https://doi.org/10.1017/S0022149X19000877
- Pereira, C. & Vaz, Z. (1933) Nematoides parasitos de Cynolebias bellotti (Pisces: Cyprinodonta). Revista de Biologia e Hygiene, 4, 59–61.
- Perrier, E. (1871) Sur l’organisation d’une espèce nouvelle de Nématoide appartenant au genre Hedruris. C. R. Academie des Sciences, 72, 337–339.
- Petter, A. J. (1971) Redescription d’Hedruris androphora Nitzsch, 1821 (Nematoda: Hedruridae) et étude de son développement chez l’hôte intermédiare. Annales de Parasitologie Humaine et Comparée, 46, 479–495. https://doi.org/10.1051/parasite/1971464479 DOI: https://doi.org/10.1051/parasite/1971464479
- Railliet, A. (1916) La famille des Thelaziidae. The Journal of Parasitology, 2 (3), 99–105. https://doi.org/10.2307/3271191 DOI: https://doi.org/10.2307/3271191
- Ramadan, M.M., Awad, E.R. & Taha, R.G. (2014) Anatomical and Surface morphology of Hedruris lutjanenses sp. n. (Nematoda: Hedruridae) from the common marine water fish Lutjanus synagris in Damietta, Egypt. Journal of Egyptian Society of Parasitology, 44, 309–320. https://doi.org/10.21608/jesp.2014.90381 DOI: https://doi.org/10.12816/0006469
- Ramallo, G., Bursey, C. & Goldberg, S. (2018) Redescription of Hedruris mucronifer (Nematoda: Hedruridae) parasite of Telmatobius schreiteri (Anura, Telmatobiidae) from Tucumán, Argentina. Parasitology Research, 117, 3903–3907. https://doi.org/10.1007/s00436-018-6097-y DOI: https://doi.org/10.1007/s00436-018-6097-y
- Ravaglia, M. & Maggese, M.C. (1995) Melano-macrophages centres in gonads of the swamp eel Synbranchus marmoratus. Histological and histochemical characterization. Journal of Fish Diseases, 18, 117–125. https://doi.org/10.1111/j.1365-2761.1995.tb00269.x DOI: https://doi.org/10.1111/j.1365-2761.1995.tb00269.x
- Rosen, D.E. & Greenwood, P.H. (1976) A fourth neotropical species of synbranchid eel and the phylogeny and systematics of synbranchiform fishes. Bulletin of American Museum of Natural History, 257, 1–69.
- Rossin, M.A. & Timi, J.M. (2016) A new species of Hedruris Nitzsch, 1821 (Nematoda: Hedruridae) parasitic in the freshwater fish Oligosarcus jenynsii (Gunther, 1864) (Characidae) from Argentina. Systematic Parasitology, 93, 899–904. https://doi.org/10.1007/s11230-016-9675-3 DOI: https://doi.org/10.1007/s11230-016-9675-3
- Sarmiento, L., Tantaleán, M. & Huiza, A. (1999) Nematodos parásitos del hombre y de los animales en el Perú. Revista Peruana de Parasitología, 14, 9–65.
- Schuurmans Stekhoven, Jr. J.H. (1952) Nematodos parasitarios de anfibios, pájaros y mamíferos de la República Argentina. Acta Zoológica Lilloana, 10, 315–400.
- Thomas, P.M. (1959) Some nematode parasites from Australian hosts. Transactions of the Royal Society of South Australia, 82, 151–162.
- Yamaguti, S. (1935) Studies on the helminth fauna of Japan. Part 9. Nematodes of fishes, 1. Japanese Journal of Zoology, 6, 338–386.
- Yamaguti, S. (1941) Studies on the helminth fauna of Japan. Part 33. Nematodes of fishes, II. Japanese Journal of Zoology, 9, 343–396.