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.
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