Hostname: page-component-848d4c4894-4hhp2 Total loading time: 0 Render date: 2024-05-14T16:15:02.448Z Has data issue: false hasContentIssue false
  • English
  • Français

Oswaldocruzia franciscoensis n. sp. (Nematoda: Molineidae) in Leptodactylus macrosternum Miranda-Ribeiro, 1926 (Anura: Leptodactylidae) from Caatinga morphoclimatic domain, Brazil: morphological and molecular characterisation

Published online by Cambridge University Press:  27 December 2023

F.M. Vieira Open the ORCID record for F.M. Vieira [Opens in a new window] ,
F.B. Pereira Open the ORCID record for F.B. Pereira [Opens in a new window] ,
L.B. Ribeiro Open the ORCID record for L.B. Ribeiro [Opens in a new window] ,
J.B. Oliveira Open the ORCID record for J.B. Oliveira [Opens in a new window] ,
D.C.N. Silva ,
L.C. Muniz-Pereira Open the ORCID record for L.C. Muniz-Pereira [Opens in a new window]  and
G. Felix-Nascimento Open the ORCID record for G. Felix-Nascimento [Opens in a new window]
F.M. Vieira*
Affiliation:
Campus de Ciências Agrárias, Universidade Federal do Vale do São Francisco (UNIVASF), Rodovia BR-407, KM 12 Lote 543 S/n Projeto de Irrigação Nilo Coelho, Petrolina, 56300-000, Brazil
F.B. Pereira
Affiliation:
Departamento de Parasitologia, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, Bloco L4 sala 252, Av. Antônio Carlos, 6627, Pampulha, Belo Horizonte, MG 31270-901, Brazil
L.B. Ribeiro
Affiliation:
Campus de Ciências Agrárias, Universidade Federal do Vale do São Francisco (UNIVASF), Rodovia BR-407, KM 12 Lote 543 S/n Projeto de Irrigação Nilo Coelho, Petrolina, 56300-000, Brazil
J.B. Oliveira
Affiliation:
Laboratório de Parasitologia, Universidade Federal Rural de Pernambuco (UFRPE), Rua Dom Manoel de Medeiros s/nº, Recife CEP 52051-360, Brazil
D.C.N. Silva
Affiliation:
Campus de Ciências Agrárias, Universidade Federal do Vale do São Francisco (UNIVASF), Rodovia BR-407, KM 12 Lote 543 S/n Projeto de Irrigação Nilo Coelho, Petrolina, 56300-000, Brazil
L.C. Muniz-Pereira
Affiliation:
Laboratório de Helmintos Parasitos de Vertebrados, Instituto Oswaldo Cruz, FIOCRUZ. Av. Brasil 4365, Rio de Janeiro CEP 21040-900, Brazil
G. Felix-Nascimento
Affiliation:
Campus de Ciências Agrárias, Universidade Federal do Vale do São Francisco (UNIVASF), Rodovia BR-407, KM 12 Lote 543 S/n Projeto de Irrigação Nilo Coelho, Petrolina, 56300-000, Brazil Laboratório de Anatomia dos Animais Domésticos e Silvestres (LAADS), Universidade Federal do Vale do São Francisco (UNIVASF), Rodovia BR-407, Km. 12 Lote 543 s/n Projeto de Irrigação Nilo Coelho, Petrolina, Pernambuco 56300-000, Brazil
*
Corresponding author: F.M. Vieira; Email: fmatosvieira@gmail.com
Get access Rights & Permissions [Opens in a new window]

Abstract

A new species of Oswaldocruzia Travassos, 1917 (Nematoda, Molineidae), parasite of Leptodactylus macrosternum Miranda-Ribeiro, 1926 (Anura: Leptodactylidae), from Caatinga morphoclimatic domain, Brazil, is described based on morphological and molecular data. Oswaldocruzia franciscoensis n. sp. is characterised by an anterior extremity with a cephalic vesicle divided into two portions, a body covered by cuticular longitudinal ridges, and cervical alae. Males of the new species have caudal bursa of type I with a 2-1-2 pattern, spicules divided into a shoe, bifurcated fork, and blade with two unequal branches, in which the longer branch bifurcates at its distal portion end and the smaller branch with three distal processes, each with distal bifurcations. Females have didelphic and amphidelphic uteri, an ovijector divided into vestibule, anterior and posterior sphincters, and anterior and posterior infundibula. The new species differs from its Neotropical congeners that have caudal bursa of type I, based on the presence of cervical alae and by having a spicular blade distally divided into two unequal branches, with the longer branch bifurcating at its distal portion and smaller branch with three distal processes, each distally bifurcated. The partial 18S rDNA sequence generated for Oswaldocruzia franciscoensis n. sp. is the first of a representative belonging to this genus in the Neotropical region.

Keywords

TaxonomywildlifeMolineidaeLeptodactylidaeBrazilian semi-arid
Type
Research Paper
Information
Journal of Helminthology , Volume 97 , 2023 , e104
Copyright
© The Author(s), 2023. Published by Cambridge University Press

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

Ávila, RW and Silva, RJ (2010) Checklist of helminths from lizards and amphisbaenians (Reptilia, Squamata) of South America. Journal of Venomous Animals and Toxins including Tropical Diseases 16, 543–572. doi:10.1590/S1678-91992010000400005.CrossRefGoogle Scholar
Ben Slimane, B and Durette-Dessett, MC (1993) Quatre nouvelles espèces du genre Oswaldocruzia Travassos, 1917 (Nematoda: Trichostrongyloidea) parasites d’amphibiens d’Equateur. Revue Suisse de Zoologie 100, 113–136. doi: 10.5962/bhl.part.82503CrossRefGoogle Scholar
Ben Slimane, B and Durette-Desset, MC (1995) Oswaldocruzia (Nematoda, Trichostrongylina, Molineoidea) parasites d’Amphibiens du Brésil et de l’Equateur, avec redéfinition de l’espèce-type O. subauricularis (Rudolphi, 1819) et d’O. mazzai Travassos, 1935. Revue Suisse de Zoologie 102, 635–653. doi: 10.5962/bhl.part.82503Google Scholar
Ben Slimane, B, Chabaud, AG and Durette-Desset, MC (1996) Les nemàtodes Trichostrongylina parasites d’amphibiens et de reptiles: Problémes taxonomiques, phylètiques et biogèographiques. Systematic Parasitology 35, 179–206. doi: 10.1007/BF00009639.CrossRefGoogle Scholar
Benício, RA, Santos, RS, Freire, SM, Ávila, RW, Silva, RJ and Fonseca, MG (2022) Diversity of helminth parasites in amphibians from northeastern Brazil. Biologia 77, 2571–2579. doi: 10.1007/s11756-022-01132-5.CrossRefGoogle Scholar
Blaxter, ML, De Ley, P, Garey, JR, Liu, LX, Scheldeman, P, Vierstraete, A, Vanfleteren, JR, Mackey, LY, Dorris, M, Frisse, LM, Vida, JT and Thomas, WK (1998) A molecular evolutionary framework for the phylum Nematoda. Nature 392, 71–75. doi: 10.1038/32160.CrossRefGoogle ScholarPubMed
Bouckaert, R, Vaughan, TG, Barido-Sottani, J, Duchêne, S, Fourment, M, Gavryushkina, A, Heled, J, Jones, G, Kühnert, D, De Maio, N, Matschiner, M, Mendes, FK, Müller, NF, Ogilvie, HA, Du Plessis, L, Popinga, A, Rambaut, A, Rasmussen, D, Siveroni, I, Suchard, MA, Wu, CH, Xie, D, Zhang, C, Stadler, T and Drummond, AJ (2019) BEAST 2.5: An advanced software platform for Bayesian evolutionary analysis. PLoS Computational Biology 15, 1–28. doi: 10.1371/journal.pcbi.1006650.CrossRefGoogle ScholarPubMed
Bouckaert, RR and Drummond, AJ (2017) bModelTest: Bayesian phylogenetic site model averaging and model comparison. BMC Evolutionary Biology 17, 1–11. doi:10.1007/10.1186/s12862-017-0890-6.CrossRefGoogle ScholarPubMed
Bursey, CR and Goldberg, SR (2004) Cosmocerca vrcibradici n. sp. (Ascaridida: Cosmocercidae), Oswaldocruzia vitti n. sp. (Strongylida: Molineoidae), and other helminths from Prionodactylus eigenmanni and Prionodactylus oshaughnessyi (Sauria: Gymnophthalmidae) from Brazil and Ecuador. Journal of Parasitology 90, 140–145. doi:10.1645/GE-3234.CrossRefGoogle Scholar
Bursey, CR and Goldberg, SR (2011) New species of Oswaldocruzia (Nematoda: Molineidae) and other helminths in Bolitoglossa subpalmata (Caudata: Plethodontidae) from Costa Rica. Journal of Parasitology 97, 286–292. doi:10.1645/GE-2622.1.CrossRefGoogle ScholarPubMed
Bush, AO, Lafferty, KD, Lotz, JM and Shostak, AW (1997) Parasitology meets ecology on its own terms: Margolis et al. revisited*. Journal of Parasitology 83, 575–583. doi:10.7939/R3J38KV04.CrossRefGoogle Scholar
Campião, KM, Morais, DH, Dias, OT, Aguiar, A, Toledo, GM, Tavares, LER and Silva, RJ (2014) Checklist of helminth parasites of amphibians from South America. Zootaxa 3843, 1–93. doi:10.11646/zootaxa.3843.1.1.CrossRefGoogle ScholarPubMed
Carreno, RA and Nadler, SA (2022) Phylogenetic analysis of the lungworms (Nematoda: Metastrongyloidea) inferred using nuclear ribosomal and mitochondrial DNA sequences. Journal of Parasitology 108, 441–452. doi:10.1645/21-124.CrossRefGoogle ScholarPubMed
Chilton, NB, Huby-Chilton, F, Gasser, RB and Beveridge, I (2006) The evolutionary origins of nematodes within the order Strongylida are related to predilection sites within hosts. Molecular Phylogenetics and Evolution 40, 118–128. doi:10.1016/j.ympev.2006.01.003.CrossRefGoogle ScholarPubMed
Conselho Nacional de Controle de Experimentação Animal (2018) Resolução Normativa CONCEA nº. 37, de 15 de fevereiro de 2018. Baixa a Diretriz da Prática de Eutanásia do Conselho Nacional de Controle de Experimentação Animal—Concea. Diário Oficial da União 1, 5. https://www.gov.br/mcti/pt-br/acompanhe-o-mcti/concea/arquivos/pdf/legislacao/resolucao-normativa-no-37-de-15-de-fevereiro-de-2018.pdf/view.Google Scholar
De Bellocq, JG, Ferté, H, Depaquit, J, Justine, JL, Tillier, A and Durette-Desset, MC (2001) Phylogeny of the Trichostrongylina (Nematoda) inferred from 28S rDNA sequences. Molecular Phylogenetics and Evolution 19, 430–442. doi:10.1006/mpev.2001.0925.CrossRefGoogle Scholar
De Ley, P, De Ley, IT, Morris, K, Abebe, E, Mundo-Ocampo, M, Yoder, M, Heras, J, Waumann, D, Rocha-Olivares, A, Burr, AHJ, Baldwin, JG and Thomas, WK (2005) An integrated approach to fast and informative morphological vouchering of nematodes for applications in molecular barcoding. Philosophical Transactions of the Royal Society B 360, 1945–1958. doi:10.1098/rstb.2005.1726.CrossRefGoogle ScholarPubMed
Durette-Desset, MC (1985) Trichostrongyloid nematodes and their vertebrate hosts: Reconstruction of the phylogeny of a parasitic group. Advances in Parasitology 24, 239–306. doi:10.1016/S0065-308X(08)60564-3.CrossRefGoogle ScholarPubMed
Durette-Desset, MC, Anjos, LA and Vrcibradic, D (2006) Three new species of the genus Oswaldocruzia Travassos, 1917 (Nematoda: Trichostrongylina, Molineoidea) parasites of Enyalius spp. (Iguanidae) from Brazil. Parasite 13, 115–125. doi:10.1051/parasite/2006132115.CrossRefGoogle ScholarPubMed
Floyd, RM, Rogers, AD, Lambshead, PJD and Smith, CR (2005) Nematode-specific PCR primers for the 18S small subunit rRNA gene. Molecular Ecology Notes 5, 611–612. doi:10.1111/j.1471-8286.2005.01009.x.CrossRefGoogle Scholar
Folmer, O, Black, M, Hoeh, W, Lutz, R and Vrijenhoek, R (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology 3, 294–299. https://www.mbari.org/wp-content/uploads/2016/01/Folmer_94MMBB.pdf.Google ScholarPubMed
Fontanilla, IK and Wade, CM (2008) The small subunit (SSU) ribosomal (r) RNA gene as a genetic marker for identifying infective 3rd juvenile stage Angiostrongylus cantonensis. Acta Tropica 105, 181–186. doi:10.1016/j.actatropica.2007.10.007.CrossRefGoogle ScholarPubMed
Freitas, JFT and Lent, H (1938) Novo nematódeo parasito de rã sul-americana. Memórias do Instituto Oswaldo Cruz 33, 477–479. doi:10.1590/S0074-02761938000400004.CrossRefGoogle Scholar
Guerrero, R (2013) Two new species of Oswaldocruzia (Nematoda: Trichostrongylina: Molineoidea) parasites of the cane toad Rhinella marina (Amphibia: Anura) from Peru. Acta Parasitologica 58, 30–36. doi:10.2478/s11686-013-0103-4.CrossRefGoogle ScholarPubMed
Hoglund, J, Morrison, DA, Divina, BP, Wilhelmson, E and Mattsson, JG (2003) Phylogeny of Dictyocaulus (lungworm) from eight species of ruminants based on analyses of ribosomal RNA data. Parasitology 127, 179–187. doi:10.1017/s0031182003003366.CrossRefGoogle ScholarPubMed
Kambayashi, C, Kakehashi, R, Sato, Y, Mizuno, H, Tanabe, H, Rakotoarison, A, Kunzel, S, Furuno, N, Ohshima, K, Kumazawa, Y, Nagy, ZT, Mori, A, Allison, A, Donnellan, SC, Ota, H, Hoso, M, Yanagida, T, Sato, H, Vences, M and Kurabayashi, A (2022) Geography-dependent horizontal gene transfer from vertebrate predators to their prey. Molecular Biology and Evolution 39, msac052. doi:10.1093/molbev/msac052.CrossRefGoogle ScholarPubMed
Kirillova, NY, Kirillov, AA, Shchenkov, SV and Chikhlyaev, IV (2020) Oswaldocruzia filiformis sensu lato (Nematoda: Molineidae) from amphibians and reptiles in European Russia: Morphological and molecular data. Nature Conservation Research 5, 41–56. doi:10.24189/ncr.2020.041.CrossRefGoogle Scholar
Kirillova, NY, Kirillov, AA and Chikhlyaev, IV (2021) Morphological variability of Oswaldocruzia filiformis (Nematoda: Molineidae) in amphibians from European Russia. IOP Conference Series: Earth and Environmental Science 818, 012018. doi:10.1088/1755-1315/818/1/012018.Google Scholar
Kirillova, NY, Kirillov, AA, Shchenkov, SV and Chikhlyaev, IV (2023) Oswaldocruzia ukrainae (Nematoda: Molineidae) - A parasite of European green toad Bufotes viridis: Morphological and molecular data. Biology 12, 772. doi:10.3390/biology12060772.CrossRefGoogle ScholarPubMed
Lacerda, GMC, Santana, JA, Araujo Filho, JA and Ribeiro, SC (2023) Checklist of parasites associated with ʻreptiles’ in Northeast Brazil. Journal of Helminthology 97, e3. doi:10.1017/S0022149X22000785.CrossRefGoogle ScholarPubMed
Larrat, YM, Melo, FTV, Gomes, TFF, Wilkens, Y and Santos, JN (2018) Oswaldocruzia lanfrediae n. sp. (Strongylida: Molineidae), a parasite of Leptodactylus paraensis Heyer (Anura: Leptodactylidae) in Brazil. Systematic Parasitology 95, 871–879. doi:10.1007/s11230-018-9814-0.CrossRefGoogle Scholar
Lent, H and Freitas, JFT (1935) Sobre uma nova espécie do gênero Oswaldocruzia Travassos, 1917. Memórias do Instituto Oswaldo Cruz 30, 379–386. doi:10.1590/S0074-02761935000900004.CrossRefGoogle Scholar
Magalhães, FM, Lyra, ML, Carvalho, TR, Baldo, D, Brusquetti, F, Burella, P, Colli, GR, Gehara, MC, Giaretta, AA, Haddad, CFB, Langone, JA, López, JA, Napoli, MF, Santana, DJ, Sá, RO and Garda, AA (2020) Taxonomic review of South American butter frogs: Phylogeny, geographic patterns, and species delimitation in the Leptodactylus latrans species group (Anura: Leptodactylidae). Herpetological Monographs 34, 131–177. doi:10.1655/0733-1347-31.4.131.CrossRefGoogle Scholar
Notredame, C, Higgins, DG and Heringa, J (2000) T-Coffee: A novel method for fast and accurate multiple sequence alignment. Journal of Molecular Biology 302, 205–217. doi:10.1006/jmbi.2000.4042.CrossRefGoogle ScholarPubMed
Pereira, FB, Ferreira, VL, Tomas, WM, Elisei, C, Paiva, F and Tavares, LER (2019) Diaphanocephalus galeatus (Nematoda: Diaphanocephalidae), a poorly known parasite of lizards: Redescription, first genetic characterization and a revision of its congeners from Brazil. Journal of Helminthology 93, 629–635. doi:10.1017/S0022149X18000597.CrossRefGoogle Scholar
Prado, DE (2003) As Caatingas da América do Sul. In: Leal, IR, Tabareli, M and Silva, JMC (eds), Ecologia e conservação da Caatinga. Recife: Editora Universitária da UFPE, 3–73.Google Scholar
Puga, S (1981) Oswaldocruzia neghmei nov. sp. (Trichostrongylidae) un nuevo nemátodo parásito del anuro chileno Hylorina sylvatica (Leptodactylidae). Studies on Neotropical Fauna and Environment 16, 107–111. doi:10.1080/01650528109360585.CrossRefGoogle Scholar
Rambaudt, A, Drummond, AJ, Xie, D, Baele, G and Suchard, MA (2018) Posterior summarization in Bayesian phylogenetics using Tracer 1.7. Systematic Biology 67, 901–904. doi:10.1093/sysbio/syy032.CrossRefGoogle Scholar
Ruiz-Torres, N, Garía-Prieto, L, Osorio-Sarabia, D and Violante-González, J (2013) A new species of nematode (Molineidae) from Rhinella marina (Amphibia: Bufonidae) in Guerrero, México. Journal of Parasitology 99, 509–512. doi:10.1645/GE-3244.1.CrossRefGoogle Scholar
Russel, PM, Brewer, BJ, Klaere, S and Bouckaert, RR (2019) Model selection and parameter inference in phylogenetics using nested sampling. Systematic Biology 68, 219–233. doi:10.1093/sysbio/syy050.CrossRefGoogle ScholarPubMed
Santos, JN, Giese, EG, Maldonado Junior, A and Lanfredi, RM (2008) A new species of Oswaldocruzia (Molineidae: Nematoda) in Chaunus marinus (Amphibian: Bufonidae) (Linnaeus, 1758) from Brazil. Journal of Parasitology 94, 264–268. doi:10.1645/GE-1336.1.CrossRefGoogle Scholar
Simões, RO, Fraga-Neto, S, Vilar, EM, Maldonado Júnior, A and Vilela, RV (2019). A new species of Bidigiticauda (Nematoda: Strongyida) from the bat Artibeus planirostris (Chiroptera: Phyllostomidae) in the Atlantic Forest and a molecular phylogeny of the molineid bat parasites. Journal of Parasitology 105, 783–792. doi:10.1645/18-191.CrossRefGoogle Scholar
Svitin, R (2017) Two new species of Oswaldocruzia (Nematoda, Molineidae) parasitising lizards in Ukraine. Zootaxa 4263, 358–368. doi:10.11646/zootaxa.4263.2.9.CrossRefGoogle ScholarPubMed
Willkens, Y, Maldonado, A, Santos, JN, Maschio, GF and Melo, FTV (2016) Redescription of Oswaldocruzia chambrieri (Strongylida: Molineidae) from Rhinella margaritifera (Anura: Bufonidae) in Caxiuanã National Forest, Brazil. Acta Parasitologica 61, 567–575. doi:10.1515/ap-2016-0076.CrossRefGoogle ScholarPubMed
Willkens, Y, Furtado, AP, Santos, JN and Melo, FTV (2021) Do host habitat use and cospeciation matter in the evolution of Oswaldocruzia (Nematoda, Molineidae) from neotropical amphibians? Journal of Helminthology 95, e33. doi:10.1017/S0022149X21000250.CrossRefGoogle ScholarPubMed
Zarlenga, DS, Lichtenfels, JR and Stringfellow, F (1994) Cloning and sequence analysis of the small subunit ribosomal RNA gene from Nematodirus battus. Journal of Parasitology 80, 342–344. doi:10.2307/3283773.CrossRefGoogle ScholarPubMed