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A new species of Rhabdias (Nematoda: Rhabdiasidae), a lung parasite of Pseudopaludicola pocoto (Anura: Leptodactylidae) from north-eastern Brazil: description and phylogenetic analyses

Published online by Cambridge University Press:  03 November 2020

D.H. Morais Open the ORCID record for D.H. Morais [Opens in a new window] ,
M.I. Müller Open the ORCID record for M.I. Müller [Opens in a new window] ,
F.T.V. Melo Open the ORCID record for F.T.V. Melo [Opens in a new window] ,
A. Aguiar Open the ORCID record for A. Aguiar [Opens in a new window] ,
Y. Willkens Open the ORCID record for Y. Willkens [Opens in a new window] ,
C. de Sousa Silva Open the ORCID record for C. de Sousa Silva [Opens in a new window] ,
E.G. Giese Open the ORCID record for E.G. Giese [Opens in a new window] ,
R.W. Ávila Open the ORCID record for R.W. Ávila [Opens in a new window]  and
Reinaldo José da Silva Open the ORCID record for Reinaldo José da Silva [Opens in a new window]
D.H. Morais*
Affiliation:
Universidade Federal de Uberlândia – UFU, Instituto de Ciências Agrárias, LMG-746, Km 1, Monte Carmelo38500-000, MG, Brazil
M.I. Müller
Affiliation:
UNESP – Univ. Estadual Paulista, Campus de Botucatu, Instituto de Biociências, Setor de Parasitologia, Av. Bento Lopes s/n Distrito de Rubião Junior CEP 18080-970, Botucatu, SP, Brazil Departamento de Ciências Biológicas, Universidade Federal de São Paulo (UNIFESP), Diadema, São Paulo, Brazil
F.T.V. Melo
Affiliation:
Laboratório de Biologia Celular e Helmintologia, Instituto de Ciências Biológicas, Universidade Federal do Pará, Belém, PA, Brazil
A. Aguiar
Affiliation:
Laboratório de Herpetologia, Departamento de Zoologia, Instituto de Biociências de Rio Claro, Universidade Estadual Paulista – UNESP
Y. Willkens
Affiliation:
Laboratório de Biologia Celular e Helmintologia, Instituto de Ciências Biológicas, Universidade Federal do Pará, Belém, PA, Brazil
C. de Sousa Silva
Affiliation:
Departamento de Biologia, Universidade Regional do Cariri – URCA, Rua Cel. Antônio Luis, 1161, CEP 63105-000, Pimenta, Crato, CE, Brazil
E.G. Giese
Affiliation:
Laboratório de Histologia e Embriologia Animal, Instituto da Saúde e Produção Animal, Universidade Federal Rural da Amazônia, Belém, Pará, Brazil;
R.W. Ávila
Affiliation:
Núcleo Regional de Ofiologia, Centro de Ciências, Universidade Federal do Ceará, Av. Humberto Monte, Pici, 60455-970, Bloco 902, Fortaleza, CE, Brazil
Reinaldo José da Silva
Affiliation:
UNESP – Univ. Estadual Paulista, Campus de Botucatu, Instituto de Biociências, Setor de Parasitologia, Av. Bento Lopes s/n Distrito de Rubião Junior CEP 18080-970, Botucatu, SP, Brazil
*
Author for correspondence: D.H. Morais, E-mail: drmoraisvt@ufu.br
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Abstract

Rhabdias pocoto n. sp. is herein described from the lungs of the swamp frog Pseudopaludicola pocoto Magalhães, Loebmann, Nogueira, Kokubum, Baptista, Haddad & Garda, 2014, from the Caatinga biome in the state of Ceará, in north-eastern Brazil. The new species is characterized by a body that dilates posteriorly, six small lips (protuberances) and two rounded lateral expansions of cuticular inflation on the anterior end, each containing an amorphous gland-like structure inside and a short and conical tail. Additionally, molecular analysis and comparison of the partial mitochondrial cytochrome c oxidase I sequence of R. pocoto n. sp. revealed genetic divergence between the new species and the sequences of Rhabdias spp. previously deposited in GenBank. Phylogenetic analysis grouped the new taxon into the R. pseudosphaerocephala species complex + R. glaurungi clade. The new discovery represents the 19th species of Rhabdias spp. described in the Neotropical region, the ninth in Brazil and the first species of Rhabdias found parasitizing South American frogs of the genus Pseudopaludicola, as well as the first Caatinga biome species of Rhabdias.

Keywords

Caatinga biomenematodesRhabdias phylogenyCOI gene
Type
Review Article
Information
Journal of Helminthology , Volume 94 , 2020 , e209
Copyright
Copyright © The Author(s), 2020. Published by Cambridge University Press

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References

Alcantara, EP, Ferreira-Silva, C, Silva, LAF, Lins, AGS, Ávila, RW, Morais, DH and Silva, RJ (2018) Helminths of Dermatonotus muelleri (Anura: Microhylidae) from northeastern Brazil. Journal of Parasitology 104, 550–556.CrossRefGoogle ScholarPubMed
Amorim, DM, Olivera, RH, Dyna, C, Sousa, DM, Santos, MEP, Lima, LS, Pinto, LC and Ávila, RW (2019) Nematodes parasites of Rhinella jimi (Stevaux, 2002) (Anura: Bufonidae) in areas of Caatinga, northeastern Brazil. Neotropical Helminthology 13, 265–271.Google Scholar
Andrade, IS, Barros, LCS, Oliveira, AFS, Juncá, FA and Magalhaes, FM (2015) Distribution extension of Pseudopaludicola pocoto Magalhães, Loebmann, Kokubum, Haddad & Garda, 2014 (Anura: Leptodactylidae: Leiuperinae) in state of Minas Gerais, Brazil. Herpetology Notes 8, 227–229.Google Scholar
Araujo-Filho, JA, Brito, SV, Almeida, WO, Morais, DH and Ávila, RW (2015) A new species of Parapharyngodon (Nematoda: Pharyngodonidae) infecting Dermatonotus muelleri (Anura: Microhylidae) from Caatinga, northeastern Brazil. Zootaxa 4012, 386–390.CrossRefGoogle ScholarPubMed
Campião, KM, Morais, DH, Dias, OT, Aguiar, A, Toledo, G, Tavares, LER and Silva, RJ (2014) Checklist of helminth parasites of amphibians from South America. Zootaxa 3843, 1–93.CrossRefGoogle ScholarPubMed
CFMV (2013) Conselho Federal de Medicina Veterinária. Métodos de eutanásia. pp. 28–29 in Guia brasileiro de boas práticas de eutanásia em animais. Comissão de ética, Bioética e bem-estar animal. CFMV. Brasília, Distrito Federal.Google Scholar
Cipriani, P, Mattiucci, S, Paoletti, M, Santoro, M and Nascetti, G (2012) Rhabdias esculentarum n. sp. (Nematoda: Rhabdiasidae) from green frogs of the Rana esculenta species complex in Italy: Molecular evidence, morphological description and genetic differentiation from its congeners in frogs and toads. Systematic Parasitology 82, 131–146.CrossRefGoogle ScholarPubMed
Frost, DR (2020) Amphibian Species of the World: an Online Reference. Version 6.0. New York, NY, USA, American Museum of Natural History. Available at http://research.amnh.org/herpetology/amphibia/index.html (accessed 4 May 2020).Google Scholar
Garda, AA, Stein, MG, Machado, RB, Lion, MB, Juncá, FA and Napoli, MF (2017) Ecology, Biogeography, and Conservation of Amphibians of the Caatinga. pp. 133–149 in Silva, JMC, Leal, IR, Tabarelli, M (Eds) Caatinga. Cham, Springer.CrossRefGoogle Scholar
Guindon, S and Gascuel, O (2003) A Simple, Fast, and Accurate Algorithm to Estimate Large Phylogenies by Maximum Likelihood. Systematic Biology 52, 696–704.CrossRefGoogle ScholarPubMed
Gutiérrez, RO (1945) Contribución al conocimiento de los nemátodos parásitos de anfibios argentinos. B.S. thesis. Museo de la Plata, Argentina, 37 p.Google Scholar
Johnson, PTJ, Calhoun, DM, Stokes, AN, Susbilla, CB, McDevitt-Galles, T, Briggs, CJ, Hoverman, JT, Tkach VV, and de Roode, JC (2018) Of poisons and parasites-the defensive role of tetrodotoxin against infections in newts. Journal of Animal Ecology 87(4), 1192–1204.CrossRefGoogle ScholarPubMed
Jorge, F and Poulin, R (2018) Poor geographical match between the distributions of host diversity and parasite discovery effort. Proceedings of the Royal Society B: Biological Sciences 285, 20180072.CrossRefGoogle ScholarPubMed
Junker, K, Lhermitte-Vallarino, N, Barbuto, M, Ineich, I, Wanji, S and Bain, O (2010) New species of Rhabdias (Nematoda:Rhabdiasidae) from Afrotropical anurans, including molecular evidence and notes on biology. Folia Parasitologica 57(1), 47–61.CrossRefGoogle ScholarPubMed
Kearse, M, Moir, R, Wilson, A, Stones-Havas, S, Cheung, M, Sturrock, S and Drummond, A (2012) Geneious Basic: An integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28, 1647–1649.CrossRefGoogle ScholarPubMed
Kimura, M (1980) A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. Journal of Molecular Evolution 16, 111–120.CrossRefGoogle ScholarPubMed
Kloss, GR (1971) Alguns Rhabdias (Nematoda) de Bufo no Brasil. Papeis Avulsos de Zoologia 24, 1–52.Google Scholar
Kloss, GR (1974) Rhabdias (Nematoda, Rhabditoidea) from the marinus group of Bufo. A study of sibling species. Arquivos de Zoologia (São Paulo) 25, 61–120.CrossRefGoogle Scholar
Kuzmin, Y (2013) Review of Rhabdiasidae (Nematoda) from the Holarctic. Zootaxa 3639, 1–76.CrossRefGoogle ScholarPubMed
Kuzmin, Y and Tkach, VV (2020) Rhabdias. Kyiv, Ukraine, World Wide Web electronic publication. http://izan.kiev.ua/ppages/rhabdias.Google Scholar
Kuzmin, Y, Tkach, VV and Snyder, SD (2003) The nematode genus Rhabdias (Nematoda: Rhabdiasidae) from amphibians and reptiles of the Nearctic. Comparative Parasitology 70, 101–114.CrossRefGoogle Scholar
Kuzmin, Y, Du Preez, LH and Junker, K (2015) Some nematodes of the genus Rhabdias Stiles et Hassall, 1905 (Nematoda: Rhabdiasidae) parasitizing amphibians in French Guiana. Folia Parasitologica 62, 031.CrossRefGoogle Scholar
Kuzmin, Y, Melo, FTV, Silva Filho, HF and Santos, JN (2016) Two new species of Rhabdias Stiles et Hassall, 1905 (Nematoda: Rhabdiasidae) from anuran amphibians in Para. Brazil. Folia Parasitologica 63, 015. doi: 10.14411/fp.2016.015.Google ScholarPubMed
Kuzmin, Y, Halajian, A, Tavakol, S, Luus-Powell, WJ and Tkach, VV (2017) Description and phylogenetic position of a new species of Rhabdias Stiles et Hassall, 1905 (Nematoda: Rhabdiasidae) from the banded rubber frog, Phrynomantis bifasciatus (Smith) (Amphibia: Microhylidae), in South Africa. Folia Parasitologica 64, 35, 1–8.CrossRefGoogle ScholarPubMed
Langford, GJ Jr and Janovy, J (2013) Host specificity of the North American Rabdias spp. (Nematoda: Rhabdiasidae): combined field data and experimental infections with a molecular phylogeny. Journal of Parasitology 99, 277–286.CrossRefGoogle Scholar
Lhermitte-Vallarino, N, Junker, K and Bain, O (2009) Reappraisal of the specific status of Rhabdias (Nematoda: Rhabdiasoidea) from Malagasy chameleons in the Paris Museum collection. Parasite 16, 111–123.CrossRefGoogle ScholarPubMed
Lhermitte-Vallarino, N, Barbuto, M, Ineich, I, Wanji, S, Lebreton, M, Chirio, L and Bain, O (2008) First report of Rhabdias (Nematoda: Rhabdiasoidea) from lungs of montane chameleons in Cameroon: Description of two new species and notes on biology. Journal Parasite 15(4), 553–564.CrossRefGoogle ScholarPubMed
Lins, AGS, Aguiar, A, Morais, DH, Silva, LAF, Ávila, RW and Silva, RJ (2017) Helminth fauna of Leptodactylus syphax (Anura: Leptodactylidae) from Caatinga biome, northeastern Brazil. Revista Brasileira de Parasitologia Veterinária (impresso) 26, 74–80.CrossRefGoogle ScholarPubMed
Madelaire, CB, Franceschini, L, Morais, DH, Gomes, FR and Silva, RJ (2020) Helminth parasites of three anuran species during reproduction and drought in the Brazilian semiarid Caatinga region. Journal of Parasitology 106, 334–340.CrossRefGoogle ScholarPubMed
Magalhães, FM, Loebmann, D, Kokubum, MNC, Haddad, CFB and Garda, A (2014) A new species of Pseudopaludicola (Anura: Leptodactylidae: Leiuperinae) from northeastern Brazil. Herpetologica 70, 77–88.CrossRefGoogle Scholar
Martínez-Salazar, EA (2008) A new rhabdiasid species from Craugastor occidentalis (Anura: Brachycephalidae) from Sierra de Manantlán, Jalisco.CrossRefGoogle Scholar
Miller, MA, Pfeiffer, W and Schwartz, T (2010) Creating the CIPRES Science Gateway for inference of large phylogenetic trees, SC10 Workshop on Gateway Computing Environments (GCE10), New Orleans, November 14, 1–8.CrossRefGoogle Scholar
Morais, DH, Aguiar, A, Müller, MI, Narciso, RB, da Silva, LAF and Silva, RJ (2017) Morphometric and phylogenetic analyses of Serpentirhabdias viperidicus n. sp. (Nematoda: Rhabdiasidae) from the lancehead snake Bothrops moojeni Hoge. Journal of Helminthology 91(3), 360–370.CrossRefGoogle ScholarPubMed
Müller, MI, Morais, DH, Costa-Silva, GJ, Aguiar, A, Ávila, RW and Silva, RJ (2018) Diversity in the genus Rhabdias (Nematoda, Rhabdiasidae): Evidence for cryptic speciation. Zoologica Scripta 47, 595–607. DOI: 10.1111/zsc.12304.CrossRefGoogle Scholar
Nascimento, LC, Gonçalves, EC, Melo, FT, Giese, EG, Furtado, AP and Santos, JN (2013) Description of Rhabdias breviensis n. sp. (Rhabditoidea: Rhabdiasidae) in two Neotropical frog species. Systematic Parasitology 86, 69–75.CrossRefGoogle Scholar
Oliveira, CR, Ávila, RW and Morais, DH (2019) Helminths associated with three Physalaemus species (Anura: Leptodactylidae) from Caatinga Biome, Brazil. Acta Parasitologica 64, 205–212.CrossRefGoogle ScholarPubMed
Posada, D (2008) jModelTest: phylogenetic model averaging. Molecular Biology and Evolution 25, 1253–1256.CrossRefGoogle ScholarPubMed
Poulin, R (2007) Evolutionary ecology of parasites. 2nd edn. 332 pp. Princeton, New Jersey, University Press.CrossRefGoogle Scholar
Poulin, R, Hay, E and Jorge, F (2019) Taxonomic and geographic bias in the genetic study of helminth parasites. International Journal for Parasitology 49, 429–435.CrossRefGoogle ScholarPubMed
Prosser, SWJ, Velarde-Aguilar, MG, Leon-Regagnon, V and Henert, PDN (2013) Advancing nematode barcoding: A primer cocktail for the cytochrome c oxidase subunit I gene from vertebrate parasitic nematodes. Molecular Ecology 13, 1108–1115.Google ScholarPubMed
Pyron, AR and Wiens, JJ (2011) A large-scale phylogeny of Amphibia including over 2800 species, and a revised classification of extant frogs, salamanders, and caecilians. Molecular Phylogenetics and Evolution 61, 543–583.CrossRefGoogle Scholar
Rambaut, A (2009) Molecular Evolution, phylogenetics and epidemiology: Fig-Tree. URL: http://tree.bio.ed.ac.uk/software/figtree/ (accessed 10 November 2015).Google Scholar
Ronquist, F and Huelsenbeck, JP (2003) MRBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19, 1572–1574.CrossRefGoogle ScholarPubMed
Schuurmans-Stekhoven, JH (1952) Nematodos parasitarios de anfibios, pajaros y mamiferos de la Republica Argentina. Acta Zoologica Lilloana 10, 315–400.Google Scholar
Segalla, MV, Caramaschi, U, Cruz, CAG, Garcia, PCA, Grant, T, Haddad, CFB, Santana, DJ, Toledo, LF and Langone, JA (2019) Brazilian amphibians: list of species. Herpetologia Brasileira 08, 65–96.Google Scholar
Silva, IC, Lima, MSCS, Santos, MCO, Souza, PS and Pederassi, J (2015) Geographic distribution: Pseudopaludicola pocoto. Herpetological Review 46, 213.Google Scholar
Silva, CS, Roberto, IJ, Ávila, RW and Morais, DH (2017) New records and geographic distribution map of Pseudopaludicola pocoto (Anura: Leptodactylidae: Leiuperinae) in northeastern Brazil. Pesquisa Ensino Ciências Exatas & Natureza 2, 131–135.CrossRefGoogle Scholar
Silva, CS, Ávila, RW and Morais, DH (2018) Helminth community dynamics in a population of Pseudopaludicola pocoto (Leptodactylidae: Leiuperinae) from northeast-Brazilian. Helminthologia 55, 292–305.CrossRefGoogle Scholar
Tamura, K, Peterson, D, Peterson, N, Stecher, G, Nei, M and Kumar, S (2011) MEGA5: Molecular Evolutionary Genetics Analysis using Maximum Likelihood, Evolutionary Distance, and Maximum Parsimony Methods. Molecular Biology and Evolution 28, 2731–2739.CrossRefGoogle ScholarPubMed
Teles, DA, Araujo-Filho, JA, Ávila, RW and Almeida, WO (2014) Helminths of Leptodactylus vastus (Anura: Leptodactylidae) in area of Caatinga, Brazil. Herpetology Notes 7, 355–356.Google Scholar
Teles, DA, Sousa, JGG, Teixeira, AAM, Silva, MC, Oliveira, RH, Silva, MRM and Ávila, RW (2015) Helminths of the frog Pleurodema diplolister (Anura, Leiuperidae) from the Caatinga in Pernambuco State, northeast Brazil. Brazilian Journal of Biology 75, 251–253.CrossRefGoogle Scholar
Teles, DA, Pinto, CLM, Teixeira, AAM and Araujo-Filho, JA (2018a) First report of Rhabdias sp. infecting Leptodactylus macrosternum from the Caatinga domain, Neotropical region. Cuadernos de Herpetologia 32 (2) 01–02.Google Scholar
Teles, DA, Brito, SV, Araujo-Filho, JA, Ribeiro, SC, Teixeira, AAM, Mesquita, DO and Almeida, WO (2018b) Nematodes of the Rhinella granulosa Spix, 1824 (Anura: Bufonidae) from the semiarid northeastern Caatinga Region of Brazil. Comparative parasitology 85, 208–211.CrossRefGoogle Scholar
Tkach, VV, Kuzmin, Y and Snyder, SD (2014) Molecular insight into systematics, host associations, life cycles and geographic distribution of the nematode family Rhabdiasidae. International Journal for Parasitology 44, 273–284.CrossRefGoogle ScholarPubMed
Willkens, Y, Rebêlo, GL, Santos, JN, Furtado, AP, Vilela, RV, Tkach, VV, Kuzmin, Y and Melo, FTV (2019) Rhabdias glaurungi n. sp. (Nematoda: Rhabdiasidae), parasite of Scinax gr. ruber (Laurenti, 1768) (Anura: Hylidae), from the Brazilian Amazon. Journal of Helminthology 94, 1–9.Google Scholar
Xia, X (2013) DAMBE. A comprehensive software package for data analysis in molecular biology and evolution. Molecular Biology and Evolution 30, 1720–1728.CrossRefGoogle ScholarPubMed
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