SNAKES AS HOSTS FOR Centrorhynchus (ACANTHOCEPHALA) CYSTACANTHS IN THE BRAZILIAN PAMPA

Julia Veiga Pereira; Carolina Silveira Mascarenhas; Gertrud Müller

doi:10.22201/fc.25942158e.2025.1.1045

Authors

Julia Veiga Pereira
Carolina Silveira Mascarenhas Instituto Federal Sul-rio-grandense
Gertrud Müller

DOI:

https://doi.org/10.22201/fc.25942158e.2025.1.1045

Keywords:

Dipsadidae, infection indices, paratenic host, Viperidae

Abstract

Snakes may act as paratenic hosts for Centrorhynchus species, but there are few records in Brazil. Therefore, this study aimed to record Centrorhynchus cystacanths and their infection indices in different snake species from the Pampa biome in southern Brazil. Forty-two individuals belonging to eleven species were examined. Twenty-seven (64.29%) snakes were parasitized by Centrorhynchus cystacanths. Mean intensities of infection ranged from 5.50 to 139.33 helminths/host. Pseudablabes patagoniensis, Philodryas olfersii and Erythrolamprus poecilogyrus were the species with the highest intensities of infection: 836, 248 and 235 cystacanths, respectively. Atractus reticulatus, Phalotris lemniscatus and Dipsas ventrimaculatus were not parasitized. Thamnodynastes strigatus, Philodryas aestiva, Erythrolamprus jaegeri, Helicops infrataeniatus and Bothrops alternatus were recorded for the first time as hosts for Centrorhynchus cystacanths. Snakes represent a trophic bridge for the parasite to reach the final host and develop into an adult to complete its life cycle.

References

Abegg, A.D., O.M. Entiauspe-Neto, H.C. Costa & O.S. Santos. 2015. Erythrolamprus poecilogyrus sspp. (Serpentes: Dipsadidae): predação. Herpetologia Brasileira 4:60-63.

Achaval, F. & A. Olmos. 2003. Anfibios y Reptiles del Uruguay. Graphis, Montevideo. Uruguay.

Aguiar, L.F.S. & M. Di-Bernardo. 2004. Diet and Feeding Behavior of Helicops infrataeniatus (Serpentes: Colubridae: Xenodontinae) in Southern Brazil. Studies on Neotropical Fauna and Environment 39:7-14.

Amato J.F.R., W.A. Boeger & S.B. Amato. 1991. Coleta e Processamento de Parasitos do Pescado. Imprensa Universitária, UFRRJ, Rio de Janeiro, Brazil.

Amato, J.F., S.B. Amato, P.B. Araújo & A.F. Quadros. 2003. First report of pigmentation dystrophy in terrestrial isopods, Atlantoscia floridana (van Name) (Isopoda, Oniscidea), induced by larval acanthocephalans. Revista Brasileira de Zoologia 20:711-716.

Andrade, B.O., W. Dröse, C.A. Aguiar, E.T. Aires, D.J. Alvares, R.L. Barbieri, et al. 2023. 12,500+ and counting: biodiversity of the Brazilian Pampa. Frontiers of Biogeography 15:e59288.

Balestrin, R.L., M. Di-Bernardo & A.G. Moreno. 2007. Feeding ecology of the neotropical worm snake Atractus reticulatus in southern Brazil. Herpetological Journal 17:62-64.

Bellini, G.P., A.R. Giraudo, V. Arzamendia & E.G. Etchepare. 2015. Temperate snake community in South America: is diet determined by phylogeny or ecology? PloS ONE 10:e0123237.

Bencke, G.A., L. Chomenko & D.M. Sant’Anna. 2016. O que é o Pampa? In: Chomenko L. & G.A. Bencke (Org.) Nosso Pampa Desconhecido. Fundacão Zoobotânica do Rio Grande do Sul, Porto Alegre, pp 17-27. https://sema.rs.gov.br/projeto-rs-biodiversidade. [Accessed in April 2024].

Bernarde, O.S. 2012. Anfíbios e Répteis: Introdução ao Estudo da Herpetofauna Brasileira. Anolis Books, São Paulo, Brazil.

Bernarde, O.S., J.C. Moura-Leite, R.A. Machado & M.N. Kokobum. 2000. Diet of the colubrid snake, Thamnodynastes strigatus (Günther, 1858) from Paraná state, Brazil, with field notes on anuran predation. Revista Brasileira de Biologia 60:695-699.

Bush, A.O., K.D. Lafferty, J.M. Lotz & A.W. Shostak. 1997. Parasitology meets ecology on its own terms: Margolis et al. revisited. Journal of Parasitology 83:575-583.

Cordero, E.H. 1933. Sur quelques acanthocéphales de L’Amerique Méridionale, I. Annales de Parasitologie Humaine et Comparée 11:271-279.

Coimbra, M.A.A., C.S. Mascarenhas, A.B.D. Henzel, J.H. Wolter, R.R.C. da Silva, F.L. da Silveira & G. Müller. 2023. Parasite-host relations and new reports of helminths for Rhinella dorbignyi (Duméril & Bibron, 1841) (Anura: Bufonidae) from Neotropical region. Parasitology International 96:102766.

Corrêa, D.N., F.M. Quintela & D. Loebmann. 2016. Feeding ecology of Erythrolamprus jaegeri jaegeri (Günter, 1858) and Erythrolamprus poecilogyrus sublineatus (Cope, 1860) in the coastal zone of Subtropical Brazil (Serpentes, Dipsadidae). Anais da Academia Brasileira de Ciências 88:293-308.

Chomenko, L. & G.A. Bencke. 2016. Nosso Pampa Desconhecido. Fundacão Zoobotânica do Rio Grande do Sul, Porto Alegre. https://sema.rs.gov.br/projeto-rs-biodiversidade. [Accessed in April 2024].

Farias, F.M., C.A.R. Melo, D.C.P. Pellegrini, H. Hasenack & M.F. Scherer 2023. O cerne do Pampa: Conhecendo o mais austral dos biomas brasileiros. Ciência & Cultura 75, https://revistacienciaecultura.org.br/?artigos=o-cerne-do-pampa [Accessed in April 2024].

Frota, A.V.B. da, B.D.Vitorino, J.R. da S. Nunes & C.J. da Silva. 2021. An overview of the diet of the Great Black Hawk Urubitinga urubitinga (Accipitriformes: Accipitridae) and report of new prey species. Ornithology Research 29:29-37.

Guedes, T.B., O.M. Entiauspe-Neto & H.C. Costa. 2023. Lista de répteis do Brasil: atualização de 2022. Herpetologia Brasileira 12:56-131.

Hartmann, P.A. & O.A.V. Marques. 2005. Diet and habitat use of two sympatric species of Philodryas (Colubridae), in south Brazil. Amphibia-Reptilia 26:25-31.

IBGE. 2019. Biomas e sistema costeiro-marinho do Brasil: compatível com a escala 1:250 000. IBGE, Rio de Janeiro. https://biblioteca.ibge.gov.br/visualizacao/livros/liv101676.pdf [Accessed in April 2024].

Kennedy, C.R. 2006. Ecology of the Acanthocephala. Cambridge University Press, United Kingdom.

Lamas, M.F. & L.I. Lunaschi. 2009. Primer registro de Centrorhynchus sp. (Acanthocephala: Centrorhynchidae) en Leptophis ahaetulla marginatus (Colubridae) de Argentina. Cuadernos de Herpetología 23:45-49.

MapBiomas Project – Mapeamento anual de cobertura e uso da terra no Brasil entre 1985 a 2022 – Coleção 8. https://brasil.mapbiomas.org/wp-content/uploads/sites/4/2023/08/FACT_MapBiomas_Mapeamento-Anual-Cobertura_Colecao8_31.pdf [Accessed in April 2024].

Marcogliese, D.J. 2005. Parasites of the superorganism: are they indicators of ecosystem health? International Journal for Parasitology 35:705-716.

Marques, O.A.V., A. Eterovic & I. Sazima. 2001. Serpentes da Mata Atlântica: Guia Ilustrado para a Serra do Mar. Holos, Ribeirão Preto, Brazil.

Mascarenhas, C.S., B.M. Chaviel, F.F. Bernardon, J.H. Wolter, M.A.A. Coimbra & G. Müller. 2022. Gastrointestinal helminths associated with three species of freshwater turtles in the Pampa biome, southern Brazil. Parasitology Research 121:225-233.

Oliveira, R.J., C.S. Mascarenhas & G. Müller. 2024. Centrorhynchus spp. (Acanthocephala) in South America: new anuran record and checklist of vertebrate hosts. Brazilian Journal of Veterinary Parasitology 33:e015823.

Panasci, T. & D. Whitacr. 2000. Diet and foraging behavior of nesting roadside hawks in Petén, Guatemala. The Wilson Bulletin 112:555-558.

Petrochenko, V.I. 1971. Acanthocephala of domestic and wild animals. Academy os Sciences of the USSR. Israel Program for Scientific Translations, Jerusalem, Israel.

Porto, L.M.V. & A.M. Rui. 2019. Diet and habitat use by two sympatric canids in the Pampas of South America. Neotropical Biology and Conservation 14:1-12.

Quintela, F.M. & D. Loebmann. 2009. Guia ilustrado: os répteis da região costeira do extremo sul do Brasil. USEB, Pelotas, Brazil.

Quintela, F.M. & D. Loebmann. 2019. Diet, sexual dimorphism and reproduction of sympatric racers Philodryas aestiva and Philodryas patagoniensis from the coastal Brazilian Pampa. Anais da Academia Brasileira de Ciências 91:e20180296.

Ribeiro, S., L.F.B. Moreira, G.E. Overbeck & L. Maltchik. 2021. Protected areas of the Pampa biome presented land use incompatible with conservation purposes. Journal of Land Use Science, 16:260-272.

Ruas, J.L., G. Müller, N.A.R. Farias, T. Gallina, A.S. Lucas, F.G. Pappen, A.L. Sinkoc & J.G.W. Brum. 2008. Helmintos do cachorro do campo, Pseudalopex gymnocercus (Fischer, 1814) e do cachorro do mato, Cerdocyon thous (Linnaeus, 1766) no sul do estado do Rio Grande do Sul, Brasil. Revista Brasileria de Parasitologia Veterinária 17:87-92.

Santos, V.G.T. & S.B. Amato. 2010. Rhinella fernandezae (Anura, Bufonidae) paratenic host of Centrorhynchus sp. (Acanthocephala, Centrorhynchidae). Revista Mexicana de Biodiversidade 81:53-56.

Silva, D.S. & G. Müller. 2012. Primeiro registro de Opisthogonimus lecithonotus (Trematoda: Plagiorchiidae) em Philodryas olfersii (Serpentes: Dipsadidae) e primeiro registro de P. olfersii como hospedeiro paratênico de Centrorhynchus sp. (Acanthocephala: Centrorhynchidae). The Biologist 10:95.

Silva, J.Á. & S.A. Talamoni. 2003. Diet adjustments of maned wolves, Chrysocyon brachyurus (Illiger) (Mammalia, Canidae), subjected to supplemental feeding in a private natural reserve, Southeastern Brazil. Revista Brasileira de Zoologia 20:339-345.

Silveira, E.C., C.S. Mascarenhas, S. Huckembeck, G. Müller & D. Loebmann. 2022. Parasitic helminths in Boana pulchella (Duméril & Bibron, 1841) (Anura: Hylidae) and their relation with host diet, body size, and habitat. Cuadernos de Herpetología 36:155-167.

Smales, L.R. 2007. Acanthocephala in amphibians (Anura) and reptiles (Squamata) from Brazil and Paraguay with description of a new species. Journal of Parasitology 93:392-398.

Soave, G.E., C.A. Darrieu, M.E. Aribalzaga, A.R. Camperi, M. Lucía, J. Williams & M. Juares. 2008. Dieta del Pirincho (Guira guira) en el nordeste de la provincia de Buenos Aires, Argentina (Cuculiformes: cuculidae). Revista de Biologia Tropical 56:1883-1892.

Souza Jr., C.M., J.Z. Shimbo, M.R. Rosa, L.L. Parente, A.A. Alencar, B.F.T. Rudorff, H. Hasenack, M. Matsumoto, L.G. Ferreira, P.W.M. Souza-Filho, S.W. de Oliveira, W.F. Rocha, A.V. Fonseca, C.B. Marques, C.G. Diniz, D. Costa, D. Monteiro, E.R. Rosa, E. Vélez-Martin, E.J. Weber, F.E.B. Lenti, F.F. Paternost, F.G.C. Pareyn, J.V. Siqueira, J.L. Viera, L.C. Ferreira Neto, M.M. Saraiva, M.H. Sales, M.P.G. Salgado, R.Vasconcelos, S. Galano, V.V. Mesquita & T. Azevedo. 2020. Reconstructing three decades of land use and land cover changes in Brazilian biomes with Landsat archive and Earth engine. Remote Sensing 12:2735.

Tanasov V.S., M.F.D. Furtado & M.G. Salomão. 2003. Avaliação dos impactos causados pelos procedimentos de permuta de serpentes no Brasil em cem anos de existência do Instituto Butantan. Publicações Avulsas do Instituto Pau Brasil 6:1-48.

Thaler R., H. Folly, C. Galvão & L.A. da Silva. 2018. First predation report of Leptodactylus chaquensis (Anura, Leptodactylidae) by Helicops infrataeniatus (Squamata, Dipsadidae) and new records for this water snake. Herpetology Notes 11:539-541.

Travassos, L. 1926. Contribuições para o conhecimento da fauna helminthologica brasileira. XX. Memórias do Instituto Oswaldo Cruz 19:31-125.

Uetz, P., P. Freed, R. Aguilar, F. Reyes, J. Kudera & J. Hošek (Eds.). 2024. The Reptile Database. http://www.reptile-database.org. [Accessed in October 2024].

Varela, O., A. Cormenzana-Méndez, L. Krapovickas & E.H. Bucher. 2008. Seasonal Diet of the Pampas Fox (Lycalopex gymnocercus) in the Chaco Dry Woodland, Northwestern Argentina. Journal of Mammalogy 89:1012-1019.

Vidal-Martinez, V.M., D. Pech, B. Sures, S.T. Purucker & R. Poulin. 2010. Can parasites really reveal environmental impact? Trends in Parasitology 26:44-51.

Vieira, L.A. & R.L. Teixeira. 2008. Diet of Athene cunicularia (Molina, 1782) from a sandy coastal plain in southeast Brazil. Boletim do Museo de Biologia Mello Leitão 23:5-14.

Vizcaíno, S.I. 1993. Presencia del género Centrorhynchus Lühe, 1911 (Acanthocephala: Centrorhynchidae) en la República Argentina. Neotropica 39:77-78.