Descripción morfológica de estadios larvarios infectantes de Physaloptera (Spirurida: Physalopteridae), y las lesiones histológicas en el hospedador paraténico Leptodactylus macrosternum (Anura: Leptodactylidae) en el bioma de Caatinga, Brasil

Autores/as

  • Gabriela Felix-Nascimento Universidade Federal Rural de Pernambuco
  • Fabiano M. Vieira Universidade Federal do Vale do São Francisco https://orcid.org/0000-0002-5220-7252
  • Ellen C. A. Gomes Universidade Federal do Vale do São Francisco
  • Ana Catarina L. Albinati Universidade Federal do Vale do São Francisco
  • Luís C. Muniz-Pereira Instituto Oswaldo Cruz (FIOCRUZ)
  • Geraldo J. B. Moura Universidade Federal Rural de Pernambuco
  • Leonardo B. Ribeiro Universidade Federal do Vale do São Francisco
  • Jaqueline B. Oliveira Universidade Federal Rural de Pernambuco

DOI:

https://doi.org/10.22201/ib.20078706e.2022.93.3772

Palabras clave:

Nematoda, Estómago, Anuro, Región semiárida

Resumen

El objetivo de este estudio fue describir el estadio larvario infectante de Physaloptera sp. que parasita Leptodactylus
macrosternum y los aspectos histopatológicos de esta larva en la mucosa del estómago del anuro. Se recolectaron 45
ejemplares de L. macrosternum durante la temporada de lluvias en mayo de 2018, en el municipio de Petrolina, en la
región submedia de São Francisco, en Pernambuco, Brasil. Se recolectaron 27 larvas infecantes (L3) de Physaloptera
sp., que se encontraban fijados en la mucosa del estómago de 11 (24.4%) individuos de L. macrosternum. No se
encontraron otras larvas o adultos de Physaloptera entre los huéspedes sometidos a necropsia. El sitio de fijación de
la L3 en la mucosa del estómago mostró alteraciones macroscópicas (hiperémicas y ulceradas) e histológicas (lesiones tubulares en el sitio de fijación del parásito, regiones necróticas en la túnica mucosa e infiltrado inflamatorio cerca del sitio de fijación larval). Este es el primer estudio morfológico de larvas infecciosas de Physaloptera sp. parasitando L. macrosternum, y el primer registro de Physaloptera sp. como huésped paraténico en el bioma de Caatinga. Además, es el primer estudio histopatológico de lesiones provocadas por larvas infecciosas de Physaloptera sp. en esta especie hospedera.

Biografía del autor/a

Gabriela Felix-Nascimento, Universidade Federal Rural de Pernambuco

(UFRPE), Rua Dom Manoel de Medeiros s/nº, Recife CEP 52.051-360, Brazil.Programa de Pós-graduação em Ciência Animal Tropical (PPGCAT), Universidade Federal Rural de Pernambuco (UFRPE). Rua Dom Manoel de Medeiros s/nº, Recife CEP 52.051-360, Brazil

Citas

Aguiar, A., Morais, D. H., Cicchi, P. J. P., & Da Silva, R. J. (2014). Evaluation of helminths associated with 14 amphibian species from a neotropical Island near the southeast coast of Brazil. Herpetological Review, 45, 227–236.

Alcantara, E. P., Ferreira-Silva, C., Silva, L. A. F., Lins, A. G. S., Ávila, R. W., Morais, D. H., & da Silva, R. J. (2018). Helminths of Dermatonotus muelleri (Anura: Microhylidae) from Northeastern Brazil. Journal of Parasitology, 104, 550–556. https://doi.org/10.1645/16-160

Anderson, R. C. (1988). Nematode transmission patterns. Journal of Parasitology, 74, 30–45.

Anderson, R. C. (2000). Nematode parasites of vertebrates: their development and transmission, 2nd Ed. New York: CABI Publishing.

Anderson, R. C., Chabaud, A., & Willmott, S. (2009). Keys to the nematode parasites of vertebrates: archival volume. New York: CABI Publishing.

Andrade, E. B., Lima-Júnior, T. B., Leite-Júnior, J. M. A., & Leite, J. R. S. A. (2012). Predation by native fish and feeding by crab species on Leptodactylus macrosternum Miranda-Ribeiro, 1926 (Anura: Leptodactylidae) in northeastern, Brazil. Herpetology Notes, 5, 173–175.

Andrade, E. B., Melo, S. C. A., & Cunha, J. A. S. (2013). Predation on Leptodactylus macrosternum (Anura: Leptodactylidae) by Botaurus pinnatus (Pelecaniformes: Ardeidae) in Northeastern Brazil. Herpetology Notes, 6, 201–202.

Bowman, D. D. (2010). Parasitologia veterinária de Georgis, 9th Ed. Rio de Janeiro: Saunders Elsevier.

Bush, A. O., Lafferty, K. D., Lotz, J. M., & Shostak, A. W. (1997). Parasitology meets ecology on its own terms: Margolis et al. revisited*. Journal of Parasitology, 83, 575–583. https://doi.org/10.2307/3284227

Campião, K. M., Morais, D. H., Dias, O. T., Aguiar, A., Toledo, G. M., Tavares, L. E. R. et al. (2014). Checklist of helminth parasites of amphibians from South America. Zootaxa, 3843, 1–93. https://doi.org/10.11646/zootaxa.3843.1.1

Cawthorn, R. J., & Anderson, R. C. (1976). Development of Physaloptera maxillaris (Nematoda: Physalopteroidea) in skunk (Mephitis mephitis) and the role of paratenic and other hosts in its life cycle. Canadian Journal of Zoology, 54, 13–323. https://doi.org/10.1139/z76-035

Chapman, J. M., Marcogliese, D. J., Suski, C. D., & Cooke, S. J. (2015). Variation in parasite communities and health indices of juvenile Lepomis gibbosus across a gradient of watershed land-use and habitat quality. Ecological Indicators, 57, 564–572. https://doi.org/10.1016/j.ecolind.2015.05.013

Christin, M. S., Gendron, A. D., Brousseau, P., Ménard, L., Marcogliese, D. J., Cyr, D. et al. (2003). Effects of agricultural pesticides on the immune system of Rana pipiens and on its resistance to parasitic infection. Environmental Toxicology and Chemistry, 22, 1127–1133. https://doi.org/10.1002/etc.5620220522

CONCEA (Conselho Nacional de Controle de Experimentação Animal). (2013). Resolução Normativa nº. 13, 20 de setembro de 2013. Baixa as diretrizes da prática de eutanásia do Conselho Nacional de Controle de Experimentação Animal -CONCEA. Diário Oficial da União, 5. Brazil.

Felix-Nascimento, G., Vieira, F. M., Muniz-Pereira, L. C., Moura, G. J. B., Ribeiro, L. B. & Oliveira, J. B. (2020). Two new species of Cosmocercidae (Nematoda: Cosmocercoidea) of Leptodactylus macrosternum Miranda-Ribeiro (Anura: Leptodactylidae) from Caatinga Biome, Brazil. Zootaxa, 4877, 274–290. https://doi.org/10.11646/zootaxa.4877.2.3

Ferracini, V. L., Pessoa, M. C. Y. P., Silva, A. S., & Spadotto, C. A. (2001). Análise de Risco de Contaminação das Águas Subterrâneas e Superficiais da Região de Petrolina (PE) e Juazeiro (BA). Pesticidas: Revista de Ecotoxicologia e Meio Ambiente, 11, 1–16.

Gendron, A. D., Marcogliese, D. J., Barbeau, S., Christin, M. S., Brousseau, P., Ruby, S. et al. (2003). Exposure of leopard frogs to a pesticide mixture affects life history characteristics of the lungworm Rhabdias ranae. Oecologia, 135, 469–476. https://doi.org/10.1007/s00442-003-1210-y

Goater, T. M., Goater, C. P., & Esch, G. W. (2014). Parasitism: the diversity and ecology of animal parasites, 2nd Ed. New York: Cambridge University Press.

Goldberg, S. R., Bursey, C. R., Caldwell, J. P., & Shepard, D.B. (2009). Gastrointestinal helminths of 6 sympatric species of Leptodactylus from Tocantins State, Brazil. Comparative Parasitology, 76, 258–266. https://doi.org/10.1654/4368.1

Gosling, P. J. (2005). Dictionary of Parasitology. Boca Raton: Taylor & Francis Group.

Hamann, M. I., Kehr, A. I., & González, C. E. (2013). Helminth communities in the burrowing toad, Rhinella fernandezae, from Northeastern Argentina. Biologia, 68, 1155–1162. https://doi.org/10.2478/s11756-013-0272-5

Hamann, M. I., Kehr, A. I., & González, C. E. (2014). Helminth community structure in the Argentinean bufonid Melanophryniscus klappenbachi: importance of habitat use and season. Parasitology Research, 113, 3639–3649. https://doi.org/10.1007/s00436-014-4029-z

Hernandez, A. D., Bunnell, J. F., & Sukhdeo, M. V. K. (2007). Composition and diversity patterns in metazoan parasite communities and anthropogenic disturbance in stream ecosystems. Parasitology, 134, 91–102. https://doi.org/10.1017/S0031182006001247

Heyer, R., Langone, J., La Marca, E., Azevedo-Ramos, C., di Tada, I., Baldo, D. et al. (2010). Leptodactylus latrans. The IUCN Red List of Threatened Species 2010: e.T57151A11592655. Downloaded on 30 March 2021 in https://www.iucnredlist.org/species/57151/11592655

Hobmaier, M. (1941). Extramammalian Phase of Physaloptera maxillaris Molin, 1860 (Nematoda). Journal of Parasitology, 27, 233–235. https://doi.org/10.2307/3273016

Jones, H. I. (1995). Pathology associated with physalopterid larvae (Nematoda: Spirurida) in the gastric tissues of australian reptiles. Journal of Wildlife Diseases, 31, 299–306. https://doi.org/10.7589/0090-3558-31.3.299

Kelehear, C., & Jones, H. I. (2010). Nematode larvae (Order Spirurida) in gastric tissues of australian anurans: a comparison between the introduced cane toad and sympatric native frogs. Journal of Wildlife Diseases, 46, 1126–1140. https://doi.org/10.7589/0090-3558-46.4.1126

Koprivnikar, J. (2010). Interactions of environmental stressors impact survival and development of parasitized larval amphibians. Ecological Applications, 20, 2263–2272. https://doi.org/10.1890/09-1558.1

Koprivnikar, J., Marcogliese, D. J., Rohr, J. R., Orlofske, S. A., Raffel, T. R., & Johnson, P. T. J. (2012). Macroparasite infections of amphibians: What can they tell us? Ecohealth, 9, 342–360. https://doi.org/10.1007/s10393-012-0785-3

Lafferty, K. D., & Holt, R. D. (2003). How should environmental stress affect the population dynamics of disease? Ecology Letters, 6, 654–664. https://doi.org/10.1046/j.1461-0248.2003.00480.x

Lincoln, R. C., & Anderson, R. C. (1975). Development of Physaloptera maxillaris (Nematoda) in the common field cricket (Gryllus pennsylvanicus). Canadian Journal of Zoology, 53, 385–390. https://doi.org/10.1139/z75-051

Loker, E. S., & Hofkin, B. V. (2015). Parasitology: a conceptual approach. New York: Garland Science.

Madelaire, C. B., Gomes, F. R., & Silva, R. J. (2012). Helminth parasites of Hypsiboas prasinus (Anura: Hylidae) from two Atlantic Forest fragments, São Paulo State, Brazil. Journal of Parasitology, 98, 560–564. https://doi.org/10.1645/JP-GE-2665.1

Marcogliese, D. J., King, K. C., Salo, H. M., Fournier, M., Brousseau, P., Spear, P. et al. (2009). Combined effects of agricultural activity and parasites on biomarkers in the bullfrog, Rana catasbeiana. Aquatic Toxicology, 91, 126–134. https://doi.org/10.1016/j.aquatox.2008.10.001

Martins-Sobrinho, P. M., Silva, W. G. O., Santos, E. G., Moura, G. J. B., & Oliveira, J. B. (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

McKenzie, V. J. (2007). Human land use and patterns of parasitism in tropical amphibian hosts. Biological Conservation 137, 102–116. https://doi.org/10.1016/j.biocon.2007.01.019

Mehlhorn, H. (2008) Encyclopedia of Parasitology, 3rd Edition. Heidelberg: Springer Berlin.

Oliveira, C. R., Ávila, R. W., & Morais, D. H. (2019). Helminths associated with three Physalaemus species (Anura: Leptodactylidae) from Caatinga Biome, Brazil. Acta Parasitologica, 64, 205–212. https://doi.org/10.2478/s11686-018-00022-8

Oliveira, R. H., Silva, M. C., & Ávila R. W. (2014). Predation of Leptodactylus macrosternum Miranda-Ribeiro, 1926 (Anura: Leptodactylidae) by Lygophis dilepis Cope, 1862 (Squamata: Dipsadidae). Herpetology Notes, 7, 357–358.

Pereira, J. R., & Siqueira, F. B. (1979). Alterações nas características químicas de um oxissolo sob irrigação. Pesquisa Agropecuária Brasileira, 14, 189–195.

Pergentino, H. E. S., & Ribeiro, L. B. (2017). Anurophagy by the snake Thamnodynastes phoenix (Squamata: Dipsadidae: Tachymenini) in dry forested areas of Northeastern Brazil. Herpetology Notes, 10, 597–600.

Petri, L. H. (1950). Life cycle of Physaloptera rara Hall and Wigdor, 1918 (Nematoda: Spiruroidea) with the cockroach, Blatella germanica, serving as the intermediate host. Transactions of the Kansas Academy of Science, 53, 331–337. https://doi.org/10.2307/3626145

Quadros, R. M., Marques, S. M. T., Moura, A. B., & Antonelli, M. (2014). Primeiro registro do nematoide Physaloptera praeputialis parasitando puma. Neotropical Biology and Conservation, 9, 186–189. https://doi.org/10.4013/nbc.2014.93.07

Ribeiro, L. B., & Freire, E. M. X. (2009). Tropidurus Hispidus (Ncn). Frog predation. Herpetological Review, 40, 228.

Roberts, L. S., & Janovy, J. (2009). Gerald D. Schmidt & Larry S. Roberts’ foundations of parasitology, 8th Ed. New York: McGraw-Hill.

Rohr, J. R., Raffel, T. R., Sessions, S. K., & Hudson, P. J. (2008). Understanding the net effects of pesticides on amphibian trematode infections. Ecological Applications, 18, 1743–1753. https://doi.org/10.1890/07-1429.1

Rohr, J. R., Schotthoefer, A. M., Raffel, T. R., Carrick, H. J., Halstead, N., Hoverman, J. T. et al. (2008). Agrochemicals increase trematode infections in a declining amphibian species. Nature, 455, 1235–1239. https://doi.org/10.1038/nature07281

Schell, S. C. (1952). Studies on the life cycle of Physaloptera hispida Schell (Nematoda: Spiruroidea) a parasite of the cotton rat (Sigmodon hispidus littoralis Chapman). The Journal of Parasitology, 38, 462–472. https://doi.org/10.2307/3273926

Schludermann, C., Konecny, R., Laimgruber, S., Lewis, J. W., Schiemer, F., Chovanec, A. et al. (2003). Fish macroparasites as indicators of heavy metal pollution in river sites in Austria. Parasitology, 126, 61–69. https://doi.org/10.1017/S0031182003003743

Silva, J. M. C., Barbosa, L. C. F., Leal, I. R., & Tabarelli, M. (2017). The Caatinga: understanding the challenges. In J. M. C. Silva, I. R. Leal, & M. Tabarelli (Eds.), Caatinga the largest tropical dry forest region in South America (pp. 3–19). Cham: Springer.

Sures, B., Nachev, M., Selbach, C., & Marcogliese, D. J. (2017). Parasite responses to pollution: what we know and where we go in ‘Environmental Parasitology.’ Parasites and Vectors, 10, 1–19. https://doi.org/10.1186/s13071-017-2001-3

Teles, D. A., Brito, S. V., Araujo-Filho, J. A., Ribeiro, S. C., Teixeira, A. A. M., Mesquita, D. O. et al. (2018). Nematodes of the Rhinella granulosa Spix, 1824 (Anura: Bufonidae) from the Semiarid Northeastern Caatinga Region of Brazil. Comparative Parasitology, 85, 208–211. https://doi.org/10.1654/1525-2647-85.2.208

Teles, D. A., Rodrigues, J. K., Teixeira, A. A. M., De Araujo-Filho, J. A., Sousa, J. G. G., & Ribeiro, S. C. (2018). Diet of Leptodactylus macrosternum (Miranda-Ribeiro, 1926) (Anura: Leptodactylidae) in the Caatinga domain, Northeastern Brazil, Neotropical region. Herpetology Notes, 11, 223–226.

Toledo, G. M., Morais, D. H., Silva, R. J., & Anjos, L. A. (2015). Helminth communities of Leptodactylus latrans (Anura: Leptodactylidae) from the Atlantic rainforest, south-eastern Brazil. Journal of Helminthology, 89, 250–254. https://doi.org/10.1017/S0022149X1300076X

Toledo, G. M., Schwartz, H. O., Nomura, H. A. Q., Aguiar, A., Velota, R. A. M. V., Da Silva, R. J. et al. (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

Toledo, L. F. (2005). Predation of juvenile and adult anurans by invertebrates: current knowledge and perspectives. Herpetological Review, 36, 395–400.

Velarde-Aguilar, M. G., Romero-Mayén, A. R., & León-Règagnon, V. (2014). First report of the genus Physaloptera (Nematoda: Physalopteridae) in Lithobates montezumae (Anura: Ranidae) from Mexico. Revista Mexicana de Biodiversidad, 85, 304–307. https://doi.org/10.7550/rmb.36480

Vrcibradic, D., Fusinatto, L. A., Nascimento, B. B., & Campião, K. M. (2018). Boana secedens (Barro Branco Treefrog). Endoparasites. Herpetological Review, 49, 300.

Widmer, E. A. (1970). Development of third-stage Physaloptera larvae from Crotalus viridis rafinesque, 1818 in cats with notes on pathology of the larvae in the reptile. (Nematoda, Spiruroidea). Journal of Wildlife Diseases, 6, 89–93. https://doi.org/10.7589/0090-3558-6.2.89

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Publicado

2022-09-30

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TAXONOMÍA Y SISTEMÁTICA