Hostname: page-component-76fb5796d-dfsvx Total loading time: 0 Render date: 2024-04-25T11:33:40.972Z Has data issue: false hasContentIssue false
  • English
  • Français

Morphological and molecular characterization of cucullanid nematodes including Cucullanus opisthoporus n. sp. in freshwater fish from the Brazilian Amazon

Published online by Cambridge University Press:  25 October 2016

F.B. Pereira  and
J.L. Luque
F.B. Pereira
Affiliation:
Departamento de Parasitologia Animal, Universidade Federal Rural do Rio de Janeiro (UFRRJ), Caixa Postal 74540, Seropédica, RJ, 23851-970, Brazil
J.L. Luque*
Affiliation:
Departamento de Parasitologia Animal, Universidade Federal Rural do Rio de Janeiro (UFRRJ), Caixa Postal 74540, Seropédica, RJ, 23851-970, Brazil
*
*E-mail: luqueufrrj@gmail.com
Get access Rights & Permissions [Opens in a new window]

Abstract

Molecular and morphological characterization of two species of Cucullanidae from freshwater fish in Brazil are provided, one of which represented an undescribed taxon. Cucullanus opisthoporus n. sp. was collected in Cichla melaniae from River Xingu, State of Pará, and in C. pinima from River Jamarí, State of Rondônia. Nematodes referable to Cucullanus grandistomis were collected in Oxydoras niger from River Xingu. The new species has an appendage in the tail tip, ventrally covered by small spines, which is an exclusive feature of Cucullanus tucunarensis. However, C. tucunarensis differs from C. opisthoporus n. sp. based upon the relative position of deirids and the excretory pore, which are more posterior from the oesophageal end in the new species. Observations of C. tucunarensis type specimens also revealed features that were wrongly or not reported in the original description. Type specimens of C. grandistomis were observed, although they were poorly preserved. After evaluation of newly collected specimens of C. grandistomis, features unreported in the original description were observed for the first time, including the presence of an intestinal caecum. Thus, C. grandistomis was transferred to Dichelyne. Sequences of the 18S and 28S rRNA genes revealed high genetic similarity between the specimens of C. opisthoporus n. sp. from the two different hosts as well as their genetic distance from Dichelyne grandistomis n. comb. Phylogenetic reconstructions using representatives of Cucullanidae suggested the artificiality of the current morphological system adopted to separate the genera, since most genera were not monophyletic, although the availability of genetic data is still fragmented.

Type
Research Papers
Information
Journal of Helminthology , Volume 91 , Issue 6 , November 2017 , pp. 739 - 751
Copyright
Copyright © Cambridge University Press 2016 

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.)

References

Anderson, R.C., Chabaud, A.G. & Willmott, S. (2009) Keys to the nematode parasites of vertebrates: Archival volume. 480 pp. Wallingford, CABI Publishing.Google Scholar
Astrin, J.J., Zhoun, X. & Misof, B. (2013) The importance of biobanking in molecular taxonomy, with proposed definitions for vouchers in a molecular context. Zookeys 365, 67–70.Google Scholar
Berland, B. (1970) On the morphology of the head in four species of the Cucullanidae (Nematoda). Sarsia 43, 15–64.Google Scholar
Černotíková, E., Horák, A. & Moravec, F. (2011) Phylogenetic relationships of some spirurine nematodes (Nematoda: Chromadorea: Rhabditida: Spirurina) parasitic in fishes inferred from SSU rRNA gene sequences. Folia Parasitologica 58, 135–148.Google Scholar
Choudhury, A. & Nadler, S.A. (2016) Phylogenetic relationships of Cucullanidae (Nematoda) with observations on Seuratoidea and the monophyly of Cucullanus, Dichelyne and Truttaedacnitis . Journal of Parasitology 102, 87–93.CrossRefGoogle ScholarPubMed
Darriba, D., Taboada, G.L., Doallo, R. & Posada, D. (2012) jModelTest 2: more models, new heuristics and parallel computing. Nature Methods 9, 772.CrossRefGoogle ScholarPubMed
Ferraz, E. & Thatcher, V.E. (1988) Bacudacnitis grandistomis gen. et sp. nov. (Nematoda: Cucullanidae) parasita intestinal de um bagre, Pseudodoras niger (Valenciennes) da Amazonia brasileira. Amazoniana. 10, 249–253.Google Scholar
Froese, R. & Pauly, D. (Eds) (2016) FishBase. World Wide Web electronic publication. Available at http//www.fishbase.org, version 06/2014 (accessed 28 June 2016).Google Scholar
Gibbons, L.M. (2010) Keys to the nematode parasites of vertebrates: Supplementary volume. 416 pp. Wallingford, CABI Publishing.Google Scholar
Guindon, S. & Gascuel, O. (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Systematic Biology 52, 696–704.CrossRefGoogle ScholarPubMed
Huelsenbeck, J.P. & Ronquist, F. (2001) MrBayes: Bayesian inference of phylogenetic trees. Bioinformatics 17, 754–755.CrossRefGoogle ScholarPubMed
Isbert, W., Montero, F.E., Carrasón, M. & González-Solís, D. (2015) Dichelyne (Cucullanelus) romani n. sp. (Nematoda: Cucullanidae) in notacanthid fishes from the Northeast Atlantic and Western Mediterranean. Systematic Parasitology 91, 35–47.CrossRefGoogle Scholar
Katoh, K., Misawa, K., Kuma, K. & Myiata, T. (2002) MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Research 30, 3059–3066.Google Scholar
Lacerda, A.C.F., Takemoto, R.M., Marchiori, M.C., Martins, M.L. & Pavanelli, G.C. (2013) New species of Cucullanus (Nematoda: Cucullanidae) an intestinal parasite of the peacock bass Cichla piquiti (Perciformes: Cichlidae) from the Tocantins River, Brazil. Journal of Helminthology 89, 9–12.Google Scholar
Laetsch, D.R., Heitlinger, E.G., Taraschewski, H., Nadler, S.A. & Blaxter, M.L. (2012) The phylogenetics of Anguillicolidae (Nematoda: Anguillicoloidea), swimbladder parasites of eels. BMC Evolutionary Biology 12, 1–16.CrossRefGoogle ScholarPubMed
Li, L., Du, L.-Q., Xu, Z., Guo, Y.-N., Wang, S.-X. & Zhang, L.-P. (2014) Morphological variability and molecular characterization of Dichelyne (Cucullanelus) pleuronectidis (Yamaguti, 1935) (Ascaridida: Cucullanidae) from the flatfish Pleuronichthys cornutus (Temminck & Schlegel) (Pleuronectiformes: Pleuronectidae) in the East China Sea. Systematic Parasitology 87, 87–98.CrossRefGoogle Scholar
Mejía-Madrid, H.H. & Aguirre-Macedo, M.L. (2011) Redescription and genetic characterization of Cucullanus dodsworthi (Nematoda: Cucullanidae) from the checkered puffer Sphoedoirdes testudineus (Pisces: Tetraodontiformes). Journal of Parasitology 97, 695–706.CrossRefGoogle ScholarPubMed
Moravec, F. (1979) Observations on the development of Cucullanus (Truttaedacnitis) truttae (Fabricius, 1794) (Nematoda: Cucullanidae). Folia Parasitologica 26, 295–307.Google Scholar
Moravec, F. (1998) Nematodes of freshwater fishes of the Neotropical region. 464 pp. Prague, Academia.Google Scholar
Moravec, F. & Justine, J.L. (2011) Cucullanid nematodes (Nematoda: Cucullanidae) from the deep sea marine fishes off New Caledonia, including Dichelyne etelidis n. sp. Systematic Parasitology 78, 95–104.Google Scholar
Moravec, F., Kohn, A. & Fernandes, B.M.M. (1993) Nematode parasites of fishes of the Paraná River, Brazil. Part 2. Seuratoidea, Ascaridoidea, Habronematoidea and Acuarioidea. Folia Parasitologica 40, 115–134.Google Scholar
Moravec, F., Wolter, J. & Körting, W. (1999) Some nematodes and acanthocephalans from exotic ornamental freshwater fishes imported into Germany. Folia Parasitologica 46, 296–310.Google Scholar
Moravec, F., Sasal, R., Würtz, J. & Taraschewski, H. (2005) Cucullanus oceanensis (Nematoda: Cucullanidae) from Pacific eels (Anguilla spp.). Systematic Parasitology 52, 342–348.Google Scholar
Moravec, F., Khosheghbal, M. & Pazooki, J. (2014) Dichelyne (Dichelyne) spinigerus sp. nov. (Nematoda: Cucullanidae) from the marine fish Otolithes ruber (Sciaenidae) off Iran and first description of the male of Philometra otolithi Moravec et Manoharan, 2013 (Nematoda: Philometridae). Acta Parasitologica 59, 229–237.Google Scholar
Nadler, S.A., Carreno, R.A., Mejía-Madrid, H., Ullberg, J., Pagan, C., Houston, R. & Hugot, J.P. (2007) Molecular phylogeny of clade III nematodes reveals multiple origins of tissues parasitism. Parasitology 134, 1421–1442.Google Scholar
Nunn, G.B. (1992). Nematode molecular evolution . PhD Dissertation. University of Nottingham, UK, 187 pp.Google Scholar
Pereira, F.B., Vieira, F.M. & Luque, J.L. (2014) A new species of Cucullanus Nematoda: Cucullanidae) from the grey triggerfish Balistes capriscus Gmelin (Osteichthyes: Balistidae) off Rio de Janeiro, Brazil. Systematic Parasitology 87, 283–291.Google Scholar
Pereira, F.B., Tavares, L.E.R., Scholz, T. & Luque, J.L. (2015a) A morphological and molecular study of two species of Raphidascaroides Yamaguti, 1941 (Nematoda: Anisakidae), parasites of doradid catfish (Siluriformes) in South America, with a description of R. moraveci n. sp. Systematic Parasitology 91, 49–61.Google Scholar
Pereira, F.B., Vieira, F.M. & Luque, J.L. (2015b) New morphological data and first description of gravid female of Cucullanus bagre Petter, 1974 (Nematoda: Cucullanidae) from Bagre bagre (Linnaeus, 1766) (Siluriformes: Ariidae) off Brazil. Acta Parasitologica 68, 138–145.Google Scholar
Petter, A.J. (1974) Deux nouvelles espèces de Cucullanidae parasites des poissons em Guyane. Bulletin du Museum National d'Histoire Naturelle de Paris, Série 3, no. 255, Zoologie 177, 1459–1467.Google Scholar
Santos, R.B. & Tavares-Dias, M. (2010) Células sanguíneas e resposta hematológica de Oxydoras niger (Pisces, Doradidae) oriundos da bacia do Médio Rio Solimões, estado do Amazonas (Brasil), naturalmente parasitados. Boletim do Instituto de Pesca 36, 283–292.Google Scholar
Silva, A.M.O., Tavares-Dias, M., Gerônimo, G.T. & Martins, M.L. (2011) Parasite diversity in Oxydoras niger (Osteichthyes: Doradidae) from the basin of Solimões River, Amazonas state, Brazil, and the relationship between monogeneoideans and condition factor. Brazilian Journal of Biology 71, 791–796.Google Scholar
Vieira, F.M., Pereira, F.B., Pantoja, C., Soares, I.A., Pereira, A.N., Timi, J.T., Scholz, T. & Luque, J.L. (2015) A survey of nematodes of the genus Cucullanus Müller, 1777 (Nematoda, Seuratoidea) parasitic in marine fishes off Brazil, including description of three new species. Zootaxa 4039, 289–311.CrossRefGoogle ScholarPubMed
Yooyen, T., Moravec, F. & Wongsawad, C. (2011) Two new species of Cucullanus Müller, 1777 (Nematoda: Cucullanidae) from marine fishes off Thailand. Systematic Parasitology 78, 139–149.CrossRefGoogle ScholarPubMed
Werle, E., Schneider, C., Renner, M., Völker, M. & Fiehn, W. (1994) Convenient single-step, one tube purification of PCR products for direct sequencing. Nucleic Acids Research 22, 4354–4355.CrossRefGoogle ScholarPubMed