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First record of Sebekia oxycephala (Pentastomida: Sebekidae) infecting Helicops infrataeniatus (Reptilia: Colubridae), São Paulo State, Brazil

The genus Helicops comprises 15 species that are widely distributed throughout South America and such species are well adapted to aquatic environments (Ávila et al., 2006Ávila, RW.,Ferreira, VL. and ARRUDA, JAO., 2006. Natural history of the South American water snake (Serpentes: Colubridae) in the Pantanal, Brazil. Helicops leopardinusJournal of Herpetology, vol. 40, no. 2, p. 274-279. http://dx.doi.org/10.1670/113-05N.1.
http://dx.doi.org/10.1670/113-05N.1...
). These snakes are active during daytime, feed on fishes and amphibians, and forage in every layer of the water column and surface (Aguiar and Di-Bernardo, 2004Aguiar, LFS. and Di-Bernardo, M., 2004. Diet and feeding behavior of . Helicops infrataeniatus (Serpentes: Colubridae: Xenodontinae) in southern BrazilStudies on Neotropical Fauna and Environment, vol. 39, no. 1, p. 7-14. http://dx.doi.org/10.1080/01650520412331270927.
http://dx.doi.org/10.1080/01650520412331...
).

Pentastomida is a group of parasites with a complex morphology showing “five mouths”. Even though Pentastomida is in the Crustacea group, they also present characteristics of onychoforans (Abele et al., 1989Abele, LG., Kim, W. and FELGENHAUER, BE.,1989. Molecular evidence for inclusion of the phylum Pentastomida in the Crustacea. Molecular Biology and Evolution, vol. 6, p. 685-691.). Pentastomida species are parasites of the respiratory tract of vertebrates, and most of the records and new species are associated with reptiles (Almeida and Christoffersen, 2002ALMEIDA, WO. and CHRISTOFFERSEN, ML. 2002. Pentastomida. In: MORRONE, J. and LLORENTE-BOUSQUETS, J. (Eds.). Biodiversidad, taxonomía y biogeografía de artrópodos de México: hacia uma síntesis de su conocimiento. Vol. 3. México: Universidad Nacional Autónoma de México. p. 187-202.). In Brazil, five pentastomid species associated with snakes have already been recorded: Cephalobaena tetrapoda Heymons, 1922 associated with Crotalus durissus terrificus Laurenti, 1768 and Liophis lineatus Linnaeus, 1758; Raillitiella furcocerca Diesing, 1863 associated with Boa constrictor Linnaeus, 1758, Coluber lichtensteinii Wiedneuwied, 1824, Drymarchon corais Stejneger 1899, Crotalus durissus terrificus, Xenodon merremii Wagler, 1824 and Lachesis sp.; Kiricephalus coarctatus Sambon, 1910 associated with Dryadophis bifossatus Raddi, 1820, Aporophislineatus Boulenger, 1894, Herpetodryas carinatus Linnaeus, 1758 and Coluber corais Boulenger, 1894; Porocephalus crotali Humboldt, 1808 associated with Crotalusdurissus terrificus; and Sebekia oxycephala Diesing, 1835 (Almeida et al., 2007Almeida, WO.,Vasconcellos, A., Lopes, SG. and Freire, EMX., 2007. Prevalence and intensity of pentastomid infection in two species of snakes from northeastern Brazil. Brazilian Journal of Biology = RevistaBrasileira de Biologia, vol. 67, no. 4, p. 759-763. http://dx.doi.org/10.1590/S1519-69842007000400025. PMid:18278332
http://dx.doi.org/10.1590/S1519-69842007...
) associated with Micrurus surinamensis Cuvier, 1817 (Ávila et al., 2013Ávila, RW.,Morais, DH., Anjos, LA., Almeida, WO. and Silva, RJ., 2013. Endoparasites infecting the semiaquatic coral snake Micrurussurinamensis (Squamata: Elapidae) in the southern Amazonian region, Mato Grosso state, Brazil. Brazilian Journal of Biology = RevistaBrasileira de Biologia, vol. 73, no. 3, p. 645-647. http://dx.doi.org/10.1590/S1519-69842013000300024. PMid:24212707
http://dx.doi.org/10.1590/S1519-69842013...
).

Sebekia is a pentastomids genus generally associated with crocodilians, and the species of this genus use fishes as intermediate host. However, the biological cycle of Sebekia oxycephala is still not clear regarding lizards and snakes infections (Venard and Bangham, 1941Venard, CE., and BANGHAM, RV., 1941. (Pentastomida) from Florida Fishes and Some Notes on the Morphology of the Larvae. Sebekia oxycephalaThe Ohio Journal of Science, vol. 41, p. 23-28.; Riley, 1986Riley, J., 1986. The biology of pentastomids. Advances in Parasitology, vol. 25, p. 45-128. http://dx.doi.org/10.1016/S0065-308X(08)60342-5. PMid:3535437
http://dx.doi.org/10.1016/S0065-308X(08)...
; Junker and Boomker, 2006Junker, K. and Boomker, J., 2006. Check-list of the pentastomid parasites crocodilians and freshwater chelonians. The Onderstepoort Journal of Veterinary Research, vol. 73, no. 1, p. 27-36. http://dx.doi.org/10.4102/ojvr.v73i1.167. PMid:16715876
http://dx.doi.org/10.4102/ojvr.v73i1.167...
).

Studies in Brazil have shown that S. oxycephala seems to be a generalist species with a behavior similar to other pentastomids already studied (Rego and Eiras, 1989Rego, AA.and Eiras, J., 1989. Identificação das larvas de Sebekia e (Pentastomida). Histopatologia em peixes de rios. LeiperiaBrazilian Journal of Biology = RevistaBrasileira de Biologia, vol. 49, no. 2, p. 591-595.; Almeida et al., 2010Almeida, WO.,Silva-Souza, AT. and Sales, DL., 2010. Parasitism of Phalloceros harpagos (Cyprinodontiformes: Poeciliidae) by Sebekia oxycephala (Pentastomida: Sebekidae) in the headwaters of the Cambé River, Paraná State, Brazil. Brazilian Journal of Biology = Revista Brasileira de Biologia, vol. 70, no. 2, p. 457-458. http://dx.doi.org/10.1590/S1519-69842010005000004. PMid:20552150
http://dx.doi.org/10.1590/S1519-69842010...
). Sebekia oxycephala presents geographical distribution from the southern United States to the southern South America. In Brazil, pentastomid nymphs were reported parasitizing the fishes Serrasalmus nattereri Günther, 1864, Pseudoplatystoma corruscans Spix & Agassiz, 1829, Phalloceros harpagos Lucinda, 2008 (Almeida et al., 2010Almeida, WO.,Silva-Souza, AT. and Sales, DL., 2010. Parasitism of Phalloceros harpagos (Cyprinodontiformes: Poeciliidae) by Sebekia oxycephala (Pentastomida: Sebekidae) in the headwaters of the Cambé River, Paraná State, Brazil. Brazilian Journal of Biology = Revista Brasileira de Biologia, vol. 70, no. 2, p. 457-458. http://dx.doi.org/10.1590/S1519-69842010005000004. PMid:20552150
http://dx.doi.org/10.1590/S1519-69842010...
) and Serrasalmus marginatus Valenciennes, 1837 (Vicentin et al., 2011Vicentin, W., Vieira, KRI.,Costa, FES., Takemoto, RM., Tavares, LER. and Paiva, F., 2011. Metazoan endoparasites of Serrasalmus marginatus (Characiformes: Serrasalminae) in the Negro River, Pantanal, Brazil. Revista Brasileira de Parasitologia Veterinária, vol. 20, no. 1, p. 61-63. http://dx.doi.org/10.1590/S1984-29612011000100012. PMid:21439234
http://dx.doi.org/10.1590/S1984-29612011...
), and also the snakes Helicops leopardinus (Schlegel, 1837) (Rego and Vicente, 1988Rego, AA.and VICENTE, JJ., 1988. Excursão científica à Zona do Pantanal, Estado de Mato Grosso, para coletas de helmintos. Ciencia e Cultura, vol. 40, p. 65-68.), Nerodia spp. (Overstreet et al., 1985Overstreet, RM., Self, JT. and VLIET, KA.,1985. The pentastomid sp. n. in the American alligator and other hosts. Sebekia mississippiensisProceedings of the Helminthological Society of Washington, vol. 52, no. 2, p. 266-277.) and Micrurus surinamensis (Ávila et al., 2013Ávila, RW.,Morais, DH., Anjos, LA., Almeida, WO. and Silva, RJ., 2013. Endoparasites infecting the semiaquatic coral snake Micrurussurinamensis (Squamata: Elapidae) in the southern Amazonian region, Mato Grosso state, Brazil. Brazilian Journal of Biology = RevistaBrasileira de Biologia, vol. 73, no. 3, p. 645-647. http://dx.doi.org/10.1590/S1519-69842013000300024. PMid:24212707
http://dx.doi.org/10.1590/S1519-69842013...
).

In July 2012 and February 2013, two snakes Helicops infrataeniatus (Jan, 1865) were sampled in a Conservation Unit (Private Reserve of the Natural Patrimony ‘Aguapeí River Mouth’) in Castilho municipality, São Paulo State, Brazilian southeast. The snakes were necropsied, however only one was infected with parasites. Three immature pentastomids were found, one in the body cavity and two in the lungs. The parasites were collected, fixed with alcohol 70º and examined as permanent slides with Hoyer. The pentastomid identification was based on the dimensions of the hooks, copulatoryspiculae of the males (measured with the aid of a microscope fitted with a micrometer eyepiece), number of body rings and oral cavity (Venard and Bangham, 1941Venard, CE., and BANGHAM, RV., 1941. (Pentastomida) from Florida Fishes and Some Notes on the Morphology of the Larvae. Sebekia oxycephalaThe Ohio Journal of Science, vol. 41, p. 23-28.; Self and Rego, 1985Self, JT. and REGO, AA., 1985. Reassessments and revisions of certain genera and species of the family Sebekidae (Pentastomida) including description of . Sebekia microhamus n. spSystematic Parasitology, vol. 7, no. 1, p. 33-41. http://dx.doi.org/10.1007/BF00010159.
http://dx.doi.org/10.1007/BF00010159...
). The morphological analyses of the pentastomids enabled to identify the species as Sebekia oxycephala (Figure 1). Voucher parasite specimens were deposited at the Coleção Helmintológica do Instituto de Biociências, São Paulo State University, Botucatu, São Paulo State, Brazil, under the numbers CHIBB 7175 and 7176.

Figure 1
Anterior end of Sebekia oxycephala collected in the body cavity of Helicops infrataeniatus from the municipality of Castilho, São Paulo State, Brazil.

The infection of H. infrataeniatus with S. oxycephala may be related to the semi-aquatic habit and piscivorous diet of this host, since nymphs directly infect the aquatic intermediate hosts, like fishes (Junker et al., 1998Junker, K., Boomker, J. and Booyse, DG.,1998. Experimental studies on the life-cycle of Sebekia wedli (Pentastomida: Sebekidae). The Onderstepoort Journal of Veterinary Research, vol. 65, no. 4, p. 233-237. PMid:10192834.; Ávila et al., 2006Ávila, RW.,Ferreira, VL. and ARRUDA, JAO., 2006. Natural history of the South American water snake (Serpentes: Colubridae) in the Pantanal, Brazil. Helicops leopardinusJournal of Herpetology, vol. 40, no. 2, p. 274-279. http://dx.doi.org/10.1670/113-05N.1.
http://dx.doi.org/10.1670/113-05N.1...
; Morais et al., 2011Morais, DH.,Avila, RW., Kawashita, RA.and CARVALHO, MA., 2011. Squamata, Elapidae, (Cuvier, 1817): new records and distribution map in the state of Mato Grosso, Brazil, with notes on diet and activity period. Micrurus surinamensisCheck List = Journal of Species Lists and Distribution, vol. 07, no. 03, p. 350-351.). Such affirmation was previously confirmed by Goldberg and Bursey (2004)Goldberg, SR. and BURSEY, CR., 2004. Coelomic metazoan endoparasites of 15 colubrid and two elapid snake species from Costa Rica. Caribbean Journal of Science, vol. 40, no. 1, p. 62-69. that found Sebekia sp. infecting Micrurusalleni Schmidt, 1936, which shows terrestrial habit but piscivorous diet. Rego and Vicente (1988)Rego, AA.and VICENTE, JJ., 1988. Excursão científica à Zona do Pantanal, Estado de Mato Grosso, para coletas de helmintos. Ciencia e Cultura, vol. 40, p. 65-68. also recorded this parasite associated with the congeneric species H. leopardinus from Mato Grosso State, Brazil.

These findings corroborate the fact that S. oxycephala shows low specificity for intermediate hosts. This study reports for the first time S. oxycephala infecting H. infrataeniatus, adding this snake species to the host list of this pentastomid in Brazil and also recording São Paulo State as a new locality for geographic distribution.

Acknowledgements

The authors are grateful to the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq – productivity fellowship process 311713/2012-2), the Fundação de Amparo à Pesquisa do São Paulo (FAPESP – process 2011/20186-6) and the Companhia Energética do Estado de São Paulo (CESP).

References

  • Abele, LG., Kim, W. and FELGENHAUER, BE.,1989. Molecular evidence for inclusion of the phylum Pentastomida in the Crustacea. Molecular Biology and Evolution, vol. 6, p. 685-691.
  • Aguiar, LFS. and Di-Bernardo, M., 2004. Diet and feeding behavior of . Helicops infrataeniatus (Serpentes: Colubridae: Xenodontinae) in southern BrazilStudies on Neotropical Fauna and Environment, vol. 39, no. 1, p. 7-14. http://dx.doi.org/10.1080/01650520412331270927.
    » http://dx.doi.org/10.1080/01650520412331270927
  • Almeida, WO.,Silva-Souza, AT. and Sales, DL., 2010. Parasitism of Phalloceros harpagos (Cyprinodontiformes: Poeciliidae) by Sebekia oxycephala (Pentastomida: Sebekidae) in the headwaters of the Cambé River, Paraná State, Brazil. Brazilian Journal of Biology = Revista Brasileira de Biologia, vol. 70, no. 2, p. 457-458. http://dx.doi.org/10.1590/S1519-69842010005000004. PMid:20552150
    » http://dx.doi.org/10.1590/S1519-69842010005000004
  • Almeida, WO.,Vasconcellos, A., Lopes, SG. and Freire, EMX., 2007. Prevalence and intensity of pentastomid infection in two species of snakes from northeastern Brazil. Brazilian Journal of Biology = RevistaBrasileira de Biologia, vol. 67, no. 4, p. 759-763. http://dx.doi.org/10.1590/S1519-69842007000400025. PMid:18278332
    » http://dx.doi.org/10.1590/S1519-69842007000400025
  • ALMEIDA, WO. and CHRISTOFFERSEN, ML. 2002. Pentastomida. In: MORRONE, J. and LLORENTE-BOUSQUETS, J. (Eds.). Biodiversidad, taxonomía y biogeografía de artrópodos de México: hacia uma síntesis de su conocimiento. Vol. 3. México: Universidad Nacional Autónoma de México. p. 187-202.
  • Ávila, RW.,Ferreira, VL. and ARRUDA, JAO., 2006. Natural history of the South American water snake (Serpentes: Colubridae) in the Pantanal, Brazil. Helicops leopardinusJournal of Herpetology, vol. 40, no. 2, p. 274-279. http://dx.doi.org/10.1670/113-05N.1.
    » http://dx.doi.org/10.1670/113-05N.1
  • Ávila, RW.,Morais, DH., Anjos, LA., Almeida, WO. and Silva, RJ., 2013. Endoparasites infecting the semiaquatic coral snake Micrurussurinamensis (Squamata: Elapidae) in the southern Amazonian region, Mato Grosso state, Brazil. Brazilian Journal of Biology = RevistaBrasileira de Biologia, vol. 73, no. 3, p. 645-647. http://dx.doi.org/10.1590/S1519-69842013000300024. PMid:24212707
    » http://dx.doi.org/10.1590/S1519-69842013000300024
  • Goldberg, SR. and BURSEY, CR., 2004. Coelomic metazoan endoparasites of 15 colubrid and two elapid snake species from Costa Rica. Caribbean Journal of Science, vol. 40, no. 1, p. 62-69.
  • Junker, K. and Boomker, J., 2006. Check-list of the pentastomid parasites crocodilians and freshwater chelonians. The Onderstepoort Journal of Veterinary Research, vol. 73, no. 1, p. 27-36. http://dx.doi.org/10.4102/ojvr.v73i1.167. PMid:16715876
    » http://dx.doi.org/10.4102/ojvr.v73i1.167
  • Junker, K., Boomker, J. and Booyse, DG.,1998. Experimental studies on the life-cycle of Sebekia wedli (Pentastomida: Sebekidae). The Onderstepoort Journal of Veterinary Research, vol. 65, no. 4, p. 233-237. PMid:10192834.
  • Morais, DH.,Avila, RW., Kawashita, RA.and CARVALHO, MA., 2011. Squamata, Elapidae, (Cuvier, 1817): new records and distribution map in the state of Mato Grosso, Brazil, with notes on diet and activity period. Micrurus surinamensisCheck List = Journal of Species Lists and Distribution, vol. 07, no. 03, p. 350-351.
  • Overstreet, RM., Self, JT. and VLIET, KA.,1985. The pentastomid sp. n. in the American alligator and other hosts. Sebekia mississippiensisProceedings of the Helminthological Society of Washington, vol. 52, no. 2, p. 266-277.
  • Rego, AA.and Eiras, J., 1989. Identificação das larvas de Sebekia e (Pentastomida). Histopatologia em peixes de rios. LeiperiaBrazilian Journal of Biology = RevistaBrasileira de Biologia, vol. 49, no. 2, p. 591-595.
  • Rego, AA.and VICENTE, JJ., 1988. Excursão científica à Zona do Pantanal, Estado de Mato Grosso, para coletas de helmintos. Ciencia e Cultura, vol. 40, p. 65-68.
  • Riley, J., 1986. The biology of pentastomids. Advances in Parasitology, vol. 25, p. 45-128. http://dx.doi.org/10.1016/S0065-308X(08)60342-5. PMid:3535437
    » http://dx.doi.org/10.1016/S0065-308X(08)60342-5
  • Self, JT. and REGO, AA., 1985. Reassessments and revisions of certain genera and species of the family Sebekidae (Pentastomida) including description of . Sebekia microhamus n. spSystematic Parasitology, vol. 7, no. 1, p. 33-41. http://dx.doi.org/10.1007/BF00010159.
    » http://dx.doi.org/10.1007/BF00010159
  • Venard, CE., and BANGHAM, RV., 1941. (Pentastomida) from Florida Fishes and Some Notes on the Morphology of the Larvae. Sebekia oxycephalaThe Ohio Journal of Science, vol. 41, p. 23-28.
  • Vicentin, W., Vieira, KRI.,Costa, FES., Takemoto, RM., Tavares, LER. and Paiva, F., 2011. Metazoan endoparasites of Serrasalmus marginatus (Characiformes: Serrasalminae) in the Negro River, Pantanal, Brazil. Revista Brasileira de Parasitologia Veterinária, vol. 20, no. 1, p. 61-63. http://dx.doi.org/10.1590/S1984-29612011000100012. PMid:21439234
    » http://dx.doi.org/10.1590/S1984-29612011000100012
  • (With 1 figure)

Publication Dates

  • Publication in this collection
    May 2015

History

  • Received
    10 Dec 2013
  • Accepted
    31 Jan 2014
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