Abstract
Parapharyngodon spp. are nematodes parasites of amphibian and reptiles worldwide distributed. Of 55 valid species, only 11 are known for the Neotropical realm, and six were found parasitizing hylid frogs in the world. In the present work, we describe a new species of Parapharyngodon from the large intestine of Osteocephalus taurinus from Reserva de Desenvolvimento Mamirauá, Amazonas, Brazil, using light and scanning electron microscopy. Parapharyngodon curupira n. sp. is allocated to the group of species with three pairs of cloacal papillae. However, it shows a set of different morphological characters compared to its congeners. In the new species, males have gubernaculum and smooth cloacal lip, females have pre-bulbar ovaries, and we also observed some morphometric differences. Among Parapharyngodon spp. from the Neotropical realm, the new taxon resembles P. alverangai and P. politoedi. The last species was described from the same host and biome (Amazon); however, they can be easily distinguished from new species by the presence of gubernaculum and v-shape structure at the lower caudal lip. Thus, we characterize and propose a new species of Parapharyngodon from the western amazon.
Similar content being viewed by others
Code availability
Not applicable.
References
Abdel-Ghafar, F., Varjabedian, K. G., Quraishy, S. A., Abdel-Gaber, R., Fol M., & Talal, N. (2020). Morphological description and phylogenetic assessment of 28S rRNA for Thelandros chalcidiae sp. nov. from Chalcides ocellatus. Molecular Biology Reports, 47(37), 05–3718. https://doi.org/10.1007/s11033-020-05412-8
Adamson, M. L. (1981). Parapharyngodon osteopili n. sp. (Pharyngodonidae: Oxyuroidea) and a revision Parapharyngodon and Thelandros. Systematic Parasitology, 10, 105-117. https://doi.org/https://doi.org/10.1007/BF00012216
Agosta, S. J., Janz, N., & Brooks. (2010). How specialists can be generalists: resolving the “parasite paradox” and implications for emerging infectious disease. Zoologia, 27(2), 151-162. https://doi.org/10.1590/S1984-46702010000200001
Araújo-Filho, J. A., Brito, S. V., Almeida, W. O., Morais, D. H., & Ávila, R. W. (2015). A new species of Parapharyngodon (Nematoda: Pharyngodonidae) infecting Dermatonotus muelleri (Anura: Microhylidae) from Caatinga, Northeastern Brazil. Zootaxa, 4012(2), 386–390. https://doi.org/10.11646/zootaxa.4012.2.10
Baylis, H. A. (1936). Nematoda. 1. Ascaridoidea and Strongyloidea. The Fauna of British India. London: Taylor & Francis, 408.
Bursey, C. R., & Brooks, D. R. (2004). Parapharyngodon duniae n. sp. (Nematoda: Pharyngodonidae) in Phrynohyas venulosa (Anura: Hylidae) from the Area de Conservation Guanacaste, Guanacaste, Costa Rica. Journal of Parasitology, 90(2), 137-139.
Bursey, C. R., Drake, M., Cole, R., Sterner, M. , Pinckney, R., & Zieger, U. (2013). New species of Parapharyngodon (Nematoda: Pharyngodonidae) in Rhinella marina (Anura: Bufonidae) from Granada, West Indies. Journal of Parasitology, 99(3), 475–479. https://doi.org/10.1645/GE-3235.1
Bursey, C. R & Goldberg, S. R. (2015). Description of a new species of Parapharyngodon (Nematoda: Pharyngodonidae) from Mexico with a list of current species and key to species from the Panamanian Region. Journal of Parasitology, 101(3), 374–381. https://doi.org/10.1645/13-460.1
Bursey, C. R., & Telford Jr, S. R. (2002). Parapharyngodon ocalaensis n. sp. (nematoda: pharyngodonidae) from the sand Skink, Neoseps reynoldsi (Scincidae), of Florida. Journal of Parasitology, 88(5), 929-931. https://doi.org/10.1645/0022-3395(2002)088[0929:PONSNP]2.0.CO;2
Chabaud, A. G. (1965). Ordre des Ascaridida. In Traité de zoologie. Systématique de nématodes, P. P. Grassé (ed.). Masson et Cie, Paris, France, 932–1180.
Ferreira, L. F. (1973). O fenômeno Parasitismo. Revista da Sociedade Brasileira de Medicina Tropical, VII(4), 261-277.
Ferreira, A. C. S., Vieira, F. M., da Silva, D. C. N., Ribeiro, L. B., Ferreira, J. A., & Muniz-Pereira, L. C. (2021). Parapharyngodon hispidus n. sp. (Nematoda: Pharyngodonidae) in Tropidurus hispidus (Spix) (Squamata: Tropiduridae) from Caatinga Biome of the Vale do São Francisco, state of Pernambuco, Brazil with a key for the Neotropical species of the genus Parapharyngodon Chatterji. Zootaxa, 4980, 1-3. https://doi.org/10.11646/zootaxa.4980.1.12
Freitas, J. P. T. (1957). Sôbre os gêneros Thelandros Wedl, 1962 e Parapharyngodon Chatterji, 1933, com descrição de Parapharyngodon alvarengai sp. n. (Nematoda, Oxyuroidea). Memórias do lnstituto Oswaldo Cruz, 55, 2145. https://doi.org/10.1590/S0074-02761957000100003
García-Calvente, I. (1948). Revisión del género Pharyngodon y descripción de especies nuevas. Revista Ibérica de Parasitología, 8, 367–410.
Holt, B. G., Lessard J. P., Borregaard, M. K., Fritz, S. A., Araújo, M. B., Dimitrov, D., Fabre, P-H., Graham, C. H., Graves, G. R., Jønsson, K. A., et al. (2013). An update of Wallace’s zoogeographic regions of the world. Science, 339, 74–78. https://doi.org/10.1126/science.1228282
Hoorn, C., & Wesselingh, F. P. (2010). Amazonia: landscape and species evolution: a look into the past. Blackwell Publishing, 1-6.
Jiménez, A. F., León-Règagnon, V., & Pérez-Ramos, E. (2008). Two new species of Parapharyngodon (Oxyuroidea: Pharyngodonidae) from theenigmatic Bipes canaliculatus and Bipes tridactylus (Squamata: Bipedidae). Revista Mexicana de Biodiversidad, 79, 113S- 120S.
Karve, J. N. (1938). Some nematode parasites of lizards. In Livro Jubilar do Prof. Lauro Travassos, Editado para commemorar o 25 anniversário de suas actividades scientificas (1913–1938), B. Silva (ed.). Instituto Oswaldo Cruz, Rio de Janeiro, Brazil, 251–258.
Pereira, F. B., Campião, K. M., Luque, J. L., Tavares, L. E. R. (2017). Parapharyngodon hugoi n. sp., a new nematode (Oxyuroidea: Pharyngodonidae) of the tree frog Trachycephalus typhonius (Linnaeus) from the Brazilian Pantanal, including a key to the congeners from amphibians of the American continent. Systematic Parasitology, 94, 599–607. https://doi.org/10.1007/s11230-017-9725-5
Pereira, F. B., Luque, J. L., & Tavares, L. E. R. (2018). Integrative approach on Pharyngodonidae (Nematoda: Oxyuroidea) parasitic in reptiles: Relationship among its genera, importance of their diagnostic features, and new data on Parapharyngodon bainae. PLoS ONE, 13(7), e0200494. https://doi.org/10.1371/journal.pone.0200494
Petter, A. J. & Quentin, J. C. (1976). Key to the genera of the Oxyuroidea. CIH Keys to the Nematode Parasites of Vertebrates. No. 4. Anderson, R. C., Chabaud, A. G. & Willmott, S. (Editors). Farnham Royal, Slough, UK: Commonwealth Agricultural Bureaux, 30.
Rahimian, H., Pazoki, S., & Habashi, S. A. (2014). Gastrointestinal Nematodes of Laudakia nupta nupta (Sauria: Agamidae) from Iran with descriptions of two new species (Oxyuridea: Pharyngodonidae) and comments on the diagnostic features of Parapharyngodon and Thelandros. Zootaxa, 3852(1), 051–082. https://doi.org/10.11646/zootaxa.3852.1.2
Ramallo, G., Bursey, C., Castillo, G & Acosta J. C.(2016). New species of Parapharyngodon (Nematoda: Pharyngodonidae) in Phymaturus spp. (Iguania: Liolaemidae) from Argentina. Acta Parasitologica, 61, 461–465. https://doi.org/10.1515/ap-2016-0062
Santos, T. A. P., Argôlo, E. G. G., Santos, A. N., Rodrigues, A. R. O., González, C. E., Santos, J. N., & Melo, F. T. V. (2018). A new species of Parapharyngodon Chatterji, 1933 (Oxyuroidea: Pharyngodonidae), parasitic in Osteocephalus taurinus (Anura: Hylidae) from Brazil. Journal of Helminthology, 93(2), 1-6. https://doi.org/10.1017/S0022149X18000093
Skrjabin, K. I., Shikhobalova, N. P., & Mozgovoi, A. A. (1951). Key to parasitic nematodes. Vol. 2. Oxyurata and Ascaridata. Izdatel’stvo Akademii Nauk S.S.S.R., Moscow, Russia, 703.
Sobral-Souza, T., & Lima-Ribeiro, M. S. (2017). De volta ao passado: Revisitando a História Biogeográfica das Florestas Neotropicais Úmidas. Oecologia Australis, 21(2), 93-107. https://doi.org/10.4257/oeco.2017.2102.01
Velarde-Aguilar, M. G., Mata-López, R., Guillén-Hernández, S., León-Règagnon, V. (2015). Parapharyngon n. spp. (Nematoda: Pharyngodonidae) parasites of Hylid Frogs from Mexico and review of species included in the genus. Journal of Parasitology, 101(2), 212-230. https://doi.org/10.1645/13-328.1
Acknowledgments
We are grateful to the crew of the “Laboratório Multiusuário de Biologia Estrutural Celular, ICB-UFPA” and Yuri Willkens for technical support in SEM analysis.
Funding
This work was supported by CAPES/PPGBAIP/UFPA the National Council for Scientific and Technological Development (CNPq) (Grant Number 431809/2018-6 Universal); CNPq Research grant productivity to MELO, F. T. V. (Process No. 304955/2018-3) and SANTOS, J. N. (Process No. 305552/2019-8); FAPESPA/CNPQ PRONEM 01/2021 process 794027/2013. This study is part of the first author’s monograph and A.N.S Ph.D dissertation from the Postgraduate Program in Biology of Infectious and Parasitic Agents/ICB-UFPA.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Ethics approval
We followed all applicable institutional, national, and international guidelines for animal care and use.
Consent to participate
Not applicable.
Consent for publication
Not applicable.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Santos, A.N., Jesus, R.F., Macedo, L.C. et al. New species of Parapharyngodon (Nematoda: Pharyngodonidae) parasite of Osteocephalus taurinus (Anura: Hylidae) from Northern Brazilian Amazon Region. Syst Parasitol 99, 437–445 (2022). https://doi.org/10.1007/s11230-022-10037-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11230-022-10037-5