Hostname: page-component-7bb8b95d7b-5mhkq Total loading time: 0 Render date: 2024-09-20T00:48:34.631Z Has data issue: true hasContentIssue false
  • English
  • Français

A new species of lungworm from the Atlantic Forest: Rhabdias megacephala n. sp. parasite of the endemic anuran Proceratophrys boiei

Published online by Cambridge University Press:  18 September 2024

R. Euclydes Open the ORCID record for R. Euclydes [Opens in a new window] ,
F.T. de Vasconcelos Melo ,
H.C. da Justa Open the ORCID record for H.C. da Justa [Opens in a new window] ,
R.F. Jesus Open the ORCID record for R.F. Jesus [Opens in a new window] ,
L.H. Gremski Open the ORCID record for L.H. Gremski [Opens in a new window] ,
S.S. Veiga Open the ORCID record for S.S. Veiga [Opens in a new window]  and
K.M. Campião Open the ORCID record for K.M. Campião [Opens in a new window]
R. Euclydes*
Affiliation:
Biological Interactions, Faculty of Biological Sciences, Federal University of Paraná, Curitiba, Paraná 81531-980, Brazil
F.T. de Vasconcelos Melo
Affiliation:
Laboratory of Cell Biology and Helminthology ‘Prof. Dr. Reinalda Marisa Lanfredi’, Institute of Biological Sciences, Federal University of Pará, Belém, Pará 66075-110, Brazil
H.C. da Justa
Affiliation:
Department of Cell Biology, Federal University of Paraná (UFPR), Curitiba, Paraná 81531-980, Brazil
R.F. Jesus
Affiliation:
Laboratory of Cell Biology and Helminthology ‘Prof. Dr. Reinalda Marisa Lanfredi’, Institute of Biological Sciences, Federal University of Pará, Belém, Pará 66075-110, Brazil
L.H. Gremski
Affiliation:
Department of Cell Biology, Federal University of Paraná (UFPR), Curitiba, Paraná 81531-980, Brazil
S.S. Veiga
Affiliation:
UFPR: Universidade Federal do Parana
K.M. Campião
Affiliation:
Biological Interactions, Faculty of Biological Sciences, Federal University of Paraná, Curitiba, Paraná 81531-980, Brazil
*
Corresponding author: R. Euclydes; Email: rafael.euclydes@gmail.com
Get access Rights & Permissions [Opens in a new window]

Abstract

Rhabdias are lung-dwelling parasites of anurans and some reptiles. Currently, 93 species are known to exist worldwide. The identification of Rhabdias species is based mainly on morphological traits of hermaphroditic females that generally have a very conserved morphology. However, different approaches, such as the combination of morphological, molecular, and ecological data, have provided advances in identifying and delimiting rhabdiasid species. Here, we describe a new species of Rhabdias from the south of Brazil, with morphological and molecular data. The new species is distinguished from its congeners by having an elongated body, evident cephalic dilation, larger buccal capsule, and large esophagus. In addition to morphological characteristics, we observed significant genetic divergence among the cytochrome oxidase subunit I (COI) sequence of the new species and the closest available sequence, Rhabdias fuelleborni (10.24%–10.87%). Furthermore, phylogenetic reconstructions based on the COI gene indicated that the new species represents a different lineage, constituting an outgroup of the species complexes Rhabdias cf. stenocephala and Rhabdias fuelleborni with Rhabdias sp. 4. Thus, Rhabdias megacephala is the 24th nominal species of the Neotropical region, the 14th Brazilian, and the fourth species described from south of Brazil.

Keywords

Species diversitytaxonomymolecularparasitismAtlantic Forest
Type
Research Paper
Information
Journal of Helminthology , Volume 98 , 2024 , e51
Copyright
© The Author(s), 2024. 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

Aguiar, A, Anjos, LA, Nomura, HAQ, Schwartz, HO, Toledo, GM, Velota, RAMV and da Silva, RJ (2018). Helminth community structure of 13 species of anurans from Atlantic rainforest remnants, Brazil. Journal of Helminthology 92, 438–444. https://doi.org/10.1017/S0022149X17000608.Google Scholar
Alcantara, EP, Müller, MI, Úngari, LP, Ferreira-Silva, C, Emmerich, E, Giese, EG, Morais, DH, Santos, ALQ, O’Dwyer, LH and Silva, RJ (2023). Integrative taxonomy in the genus Rhabdias Stiles et Hassall, 1905 from anuran in Brazil, description of two new species and phylogenetic analyses. Parasitology International 93, 102714. https://doi.org/10.1016/j.parint.2022.102714.Google Scholar
Almeida-Santos, M (2017). Ecological aspects of the horned leaf-frog Proceratophrys mantiqueira (Odontophrynidae) in an Atlantic Rainforest area of southeastern Brazil. Salamandra 53, 413–422.Google Scholar
Bergamini, M and Thomas, C (2011). Arboreal diversity of the Atlantic forest of southern Brazil: From the beach ridges to the Paraná River. In Grillo O (ed), The Dynamical Processes of Biodiversity - Case Studies of Evolution and Spatial Distribution. InTech. https://doi.org/10.5772/24129.Google Scholar
Boquimpani-Freitas, L, Vrcibradic, D, Vicente, JJ, Bursey, CR and Rocha, CFD (2001). Helminths of the horned leaf frog, Proceratophrys appendiculata, from southeastern Brazil. Journal of Helminthology 75, 233–236.Google Scholar
Bursey, CR and Goldberg, SR (2005). New species of Oswaldocruzia (Nematoda: Molineoidae), new species of Rhabdias (Nematoda: Rhabdiasidae), and other helminths in Rana cf. forreri (Anura: Ranidae) from Costa Rica. Journal of Parasitology 91, 600–605. https://doi.org/10.1645/GE-3440.Google Scholar
Campião, KM, Morais, DH, Dias, OT, Aguiar, A, Toledo, G, Tavares, LER and Da Silva, RJ (2014). Checklist of helminth parasites of amphibians from South America. Zootaxa 3843, 1–93. https://doi.org/10.11646/zootaxa.3843.1.1.Google Scholar
D’Bastiani, E, Campião, KM, Boeger, WA and Araújo, SBL (2020). The role of ecological opportunity in shaping host–parasite networks. Parasitology 147, 1452–1460. https://doi.org/10.1017/S003118202000133X.Google Scholar
de Cássia Silva do Nascimento, L, Gonçalves, EC, de Vasconcelos Melo, FT, Giese, EG, Furtado, AP and dos Santos, JN (2013). Description of Rhabdias breviensis n. sp. (Rhabditoidea: Rhabdiasidae) in two Neotropical frog species. Systematic Parasitology 86, 69–75. https://doi.org/10.1007/s11230-013-9432-9.Google Scholar
Euclydes, L, Dudczak, AC and Campião, KM (2021). Anuran’s habitat use drives the functional diversity of nematode parasite communities. Parasitology Research 120, 993–1001. https://doi.org/10.1007/s00436-020-06994-9.Google Scholar
Euclydes, L, De La Torre, GM, Dudczak, AC, Melo FT de, V and Campião, KM (2022). Ecological specificity explains infection parameters of anuran parasites at different scales. Parasitology 149, 646–653. https://doi.org/10.1017/S0031182022000087.Google Scholar
Fecchio, A, Wells, K, Bell, JA, Tkach, VV, Lutz, HL, Weckstein, JD, Clegg, SM and Clark, NJ (2019). Climate variation influences host specificity in avian malaria parasites. Ecology Letters 22, 547–557. https://doi.org/10.1111/ele.13215.Google Scholar
Frost, DR (2024). Amphibian species of the world: An online reference. Version 6.2 American Museum of Natural History. Available at https://amphibiansoftheworld.amnh.org/index.php (accessed 13 January 2024).Google Scholar
Haddad, CFB and Sazima, I (1992). Anfíbios anuros da Serrado Japi. In Morellato, LPC (ed.). História natural da Serra do Japi: Ecologia e preservação de uma área florestal no sudeste do Brasil. Campinas: Editora Unicamp e FAPESP, 188–211.Google Scholar
Hoorn, C, Wesselingh, FP, Ter Steege, H, Bermudez, MA, Mora, A, Sevink, J, Sanmartín, I, Sanchez-Meseguer, A, Anderson, CL, Figueiredo, JP, Jaramillo, C, Riff, D, Negri, FR, Hooghiemstra, H, Lundberg, J, Stadler, T, Särkinen, T and Antonelli, A (2010). Amazonia through time: Andean uplift, climate change, landscape evolution, and biodiversity. Science 330, 927–931. https://doi.org/10.1126/science.1194585.Google Scholar
Kamiya, T, O’Dwyer, K, Nakagawa, S and Poulin, R (2014). What determines species richness of parasitic organisms? A meta-analysis across animal, plant and fungal hosts: Determinants of parasite species richness. Biological Reviews 89, 123–134. https://doi.org/10.1111/brv.12046.Google Scholar
Katoh, K and Standley, DM (2013). MAFFT Multiple Sequence Alignment Software Version 7: Improvements in performance and usability. Molecular Biology and Evolution 30, 772–780. https://doi.org/10.1093/molbev/mst010.Google Scholar
Kimura, M (1980). A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. Journal of Molecular Evolution 16, 111–120. https://doi.org/10.1007/BF01731581.Google Scholar
Klaion, T, Almeida-gomes, M, Tavares, LER, Rocha, CFD and Sluys, MV (2011). Diet and nematode infection in Proceratoprhys boiei (Anura: Cycloramphidae) from two Atlantic rainforest remnants in southeastern Brazil. Anais Da Academia Brasileira de Ciências 83, 1303–1312. https://doi.org/10.1590/S0001-37652011000400017.Google Scholar
Kloss, GR (1971). Alguns Rhabdias (Nematoda) de Bufo no Brasil. Papéis Avulsos do Zoologia 24, 1–52. https://doi.org/10.11606/0031-1049.1971.24.p1-52Google Scholar
Kuzmin, Y (2013). Review of Rhabdiasidae (Nematoda) from the Holarctic. Zootaxa 3639, 1–76. https://doi.org/10.11646/zootaxa.3639.1.1.Google Scholar
Kuzmin, Y, du Preez, L, Nel, T and Svitin, R (2022). Three new species of Rhabdias Stiles et Hassall, 1905 (Nematoda: Rhabdiasidae) parasitic in Ptychadena spp. (Amphibia: Anura: Ptychadenidae) and an identification key to Rhabdias spp. from Afrotropical anurans. Parasitology International 91, 102649. https://doi.org/10.1016/j.parint.2022.102649.Google Scholar
Kuzmin, Y, Du Preez, LH and Junker, K (2015). Some nematodes of the genus Rhabdias Stiles et Hassall, 1905 (Nematoda: Rhabdiasidae) parasitising amphibians in French Guiana. Folia Parasitologica 62, article 2015.031. https://doi.org/10.14411/fp.2015.031.Google Scholar
Kuzmin, Y, Tkach, VVand Brooks, DR (2007). Two new species of Rhabdiasids from the marine toad, Bufo marinus (l.) (Lissamphibia: Anura: Bufonidae), in Central America. Journal of Parasitology 93, 159–165. https://doi.org/10.1645/GE-858R.1.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. https://doi.org/10.1654/4075.Google Scholar
Kuzmin, Y, Vasconcelos Melo, FT de, Filho HF da, S and Nascimento dos Santos, J (2016). Two new species of Rhabdias Stiles et Hassall, 1905 (Nematoda: Rhabdiasidae) from anuran amphibians in Para, Brazil. Folia Parasitologica 63, article 2015.016. https://doi.org/10.14411/fp.2016.015.Google Scholar
Langford, GJ and Janovy, J (2013). Host specificity of North American Rhabdias spp. (Nematoda: Rhabdiasidae): Combining field data and experimental infections with a molecular phylogeny. Journal of Parasitology 99, 277–286. https://doi.org/10.1645/GE-3217.1.Google Scholar
Marcaida, AJB, Nakao, M, Fukutani, K, Nishikawa, K and Urabe, M (2022). Phylogeography of Rhabdias spp. (Nematoda: Rhabdiasidae) collected from Bufo species in Honshu, Shikoku, and Kyushu, Japan including possible cryptic species. Parasitology International 90, 102612. https://doi.org/10.1016/j.parint.2022.102612.Google Scholar
Martínez-Salazar, EA (2006). A new Rhabdiasid species from Norops megapholidotus (Sauria: Polychrotidae) from Mexico. Journal of Parasitology 92, 1325–1329. https://doi.org/10.1645/GE-872R1.1.Google Scholar
Martins-Sobrinho, PM, Silva, WGDO, Santos, EGD, Moura, GJBD and Oliveira, JBD (2017). Helminths of some tree frogs of the families Hylidae and Phyllomedusidae in an Atlantic rainforest fragment, Brazil. Journal of Natural History 51, 1639–1648. https://doi.org/10.1080/00222933.2017.1337945.Google Scholar
Minh, BQ, Schmidt, HA, Chernomor, O, Schrempf, D, Woodhams, MD, von Haeseler, A and Lanfear, R (2020). IQ-TREE 2: New models and efficient methods for phylogenetic inference in the genomic era. Molecular Biology and Evolution 37, 1530–1534. https://doi.org/10.1093/molbev/msaa015.Google Scholar
Morais, DH, Müller, MI, Melo, FTV, Aguiar, A, Willkens, Y, de Sousa Silva, C, Giese, EG, Ávila, RW and da Silva, RJ (2020). A new species of Rhabdias (Nematoda: Rhabdiasidae), a lung parasite of Pseudopaludicola pocoto (Anura: Leptodactylidae) from north-eastern Brazil: Description and phylogenetic analyses. Journal of Helminthology 94, e209. https://doi.org/10.1017/S0022149X20000929.Google Scholar
Müller, MI, Morais, DH, Costa-Silva, GJ, Aguiar, A, Ávila, RW and da Silva, RJ (2018). Diversity in the genus Rhabdias (Nematoda, Rhabdiasidae): Evidence for cryptic speciation. Zoologica Scripta 47, 595–607. https://doi.org/10.1111/zsc.12304.Google Scholar
Müller, MI, Morais, DH, da Costa, LFST, de Vasconcelos Melo, FT, Giese, EG, Ávila, RW and da Silva, RJ (2023). Revisiting the taxonomy of Rhabdias fuelleborni Travassos, 1928 (Nematoda, Rhabdiasidae) with approaches to delimitation of species and notes on molecular phylogeny. Parasitology International 92, 102692. https://doi.org/10.1016/j.parint.2022.102692.Google Scholar
Pleijel, F, Jondelius, U, Norlinder, E, Nygren, A, Oxelman, B, Schander, C, Sundberg, P and Thollesson, M (2008). Phylogenies without roots? A plea for the use of vouchers in molecular phylogenetic studies. Molecular Phylogenetics and Evolution 48, 369–371. https://doi.org/10.1016/j.ympev.2008.03.024.Google Scholar
Posada, D (2008). jModelTest: Phylogenetic model averaging. Molecular Biology and Evolution 25, 1253–1256. https://doi.org/10.1093/molbev/msn083.Google Scholar
Poulin, R (2011). Host specificity in phylogenetic and geographic space. Trends in Parasitology 27, 355–361. https://doi.org/10.1016/j.pt.2011.05.003.Google Scholar
Prado, GM and Pombal, JP Jr. (2008). Espécies de Proceratophrys Miranda-Ribeiro, 1920 com apêndices palpebrais (Anura; Cycloramphidae). Arquivos de Zoologia 39, 1–85. https://doi.org/10.11606/issn.2176-7793.v39i1p1-85.Google Scholar
Rambaut, A (2009). FigTree v1.3.1. Institute of Evolutionary Biology, University of Edinburgh. Available at http://tree.bio.ed.ac.uk/software/figtree/ (accessed 09 January 2024).Google Scholar
Reginato, M and Goldenberg, R (2007). Análise florística, estrutural e fitogeográfica da vegetação em região de transição entre as Florestas Ombrófilas Mista e Densa Montana, Piraquara, Paraná, Brasil. Hoehnea 34, 349–360. https://doi.org/10.1590/S2236-89062007000300006.Google Scholar
Ronquist, F, Huelsenbeck, JP, Teslenko, M, Zhang, C and Nylander, JAA (2003). MrBayes version 3.2 Manual: Tutorials and Model Summaries. Available at https://nbisweden.github.io/MrBayes/download.html (accessed 30 December 2023).Google Scholar
Santos-Pereira, M, Pombal, JP Jr. and Rocha, CFD (2018). Anuran amphibians in state of Paraná, southern Brazil. Biota Neotropica 18, e20170322. https://doi.org/10.1590/1676-0611-bn-2017-0322.Google Scholar
Sobral-Souza, T, Lima-Ribeiro, MS and Solferini, VN (2015). Biogeography of Neotropical rainforests: Past connections between Amazon and Atlantic Forest detected by ecological niche modeling. Evolutionary Ecology 29, 643–655. https://doi.org/10.1007/s10682-015-9780-9.Google Scholar
Tamura, K, Stecher, G and Kumar, S (2021). MEGA11: Molecular Evolutionary Genetics Analysis Version 11. Molecular Biology and Evolution 38, 3022–3027. https://doi.org/10.1093/molbev/msab120.Google Scholar
Tavares-Costa, LFS, Rebêlo, GL, Müller, MI, Jesus, RF, Nandyara, B, Silva, LMO, Costa-Campos, CE, dos Santos, JN and Melo FT de, V (2022). A new species of Rhabdias (Nematoda: Rhabdiasidae), a lung parasite of Pristimantis chiastonotus (Anura: Strabomantidae) from the Brazilian Amazon: Description and phylogenetic analyses. Parasitology Research 121, 155–166. https://doi.org/10.1007/s00436-021-07396-1.Google Scholar
Teles, DA, Brito, SV, Filho, JAA, Dias, DQ, Ávila, RW and Almeida, WO (2017). Nematode parasites of Proceratophrys aridus (Anura: Odontophrynidae), endemic frog of the Caatinga domain of the Neotropical Region, Brazil. Herpetology Notes, 10, 525–527.Google 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. https://doi.org/10.1016/j.ijpara.2013.12.005.Google Scholar
Travassos, L (1930). Pesquizas helminthologicas realisadas em Hamburgo: VII. Notas sobre os Rhabdiasoidea Railliet, 1916: (Nematoda). Memórias Do Instituto Oswaldo Cruz, 24, 161–181. https://doi.org/10.1590/S0074-02761930000800003.Google Scholar
Willkens, Y, Rebêlo, GL, Santos, JN, Furtado, AP, Vilela, RV, Tkach, VV, Kuzmin, Y and Melo, FTV (2020). Rhabdias glaurungi sp. nov. (Nematoda: Rhabdiasidae), parasite of Scinax gr. ruber (Laurenti, 1768) (Anura: Hylidae), from the Brazilian Amazon. Journal of Helminthology 94, e54. https://doi.org/10.1017/S0022149X19000476.Google Scholar
Xia, X (2018). DAMBE7: New and improved tools for data analysis in molecular biology and evolution. Molecular Biology and Evolution 35, 1550–1552. https://doi.org/10.1093/molbev/msy073.Google Scholar
Supplementary material: File

Euclydes et al. supplementary material

Euclydes et al. supplementary material
Download Euclydes et al. supplementary material(File)
File 800.1 KB