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Endoparasites infecting the semiaquatic coral snake Micrurus surinamensis (Squamata: Elapidae) in the southern amazonian region, Mato Grosso state, Brazil

Endoparasitas infectando a coral semiaquática Micrurus surinamensis (Squamata: Elapidae) no sul da Amazônia, Mato Grosso, Brasil

Abstracts

A parasitological survey was conducted in specimens of the semiaquatic coral snake Micrurus surinamensis, a poorly known South American elapid. Four specimens collected at the southern Amazon region in the Brazilian state of Mato Grosso were analyzed for endoparasites. Three parasite species were recovered from the snake hosts: the pentastomid Sebekia oxycephala, the nematode Physaloptera sp. and the trematode Opisthogonimus lecithonotus. This represents new locality and host record for S. oxycephala and O. lecithonotus.

parasitism; Pentastomida; Nematoda; Trematoda; snakes


Um estudo parasitológico foi conduzido em espécimes da cobra coral semiaquática Micrurus surinamensis, espécie de elapídeo sulamericano pouco conhecida. Quatro exemplares coletados na região sul da Amazônia, no norte do estado de Mato Grosso foram analisados quanto a presença de endoparasitas. Três espécies de parasitas foram encontradas: o pentastomídeo Sebekia oxycephala, o nematódeo Physaloptera sp. e o trematódeo Opisthogonimus lecithonotus. Isso representa novo registro de localidade e hospedeiro para S. oxycephala e O. lecithonotus.

parasitismo; Pentastomida; Nematoda; Trematoda; serpentes


1. Introduction

The coral snake genus Micrurus Wagler 1824 comprises 76 species restricted to the Western hemisphere, occupying almost all of the major biomes of the Neotropics (Roze, 1996ROZE, JA., 1996. Coral Snakes of the Americas: Biology, Identification, and Venoms. Malabar, Florida, USA: Krieger Publishing Company. 328 p.; Campbell and Lamar, 2004CAMPBELL, JA. and LAMAR, WW., 2004. The Venomous Reptiles of the Western Hemisphere. New York: Comstock, Ithaca & London. 810 p.). Many studies on natural history of this genus have been recently published (Marques, 2002MARQUES, OAV., 2002. Natural history of the coral snake Micrurus decoratus (Elapidae) from the Atlantic forest in southeast Brazil, with comments on possible mimicry. Amphibia-Reptilia, vol. 23, p. 228-232.; Aguiar and Di-Bernardo, 2007AGUIAR, LFS. and DI-BERNARDO, M., 2007. Micrurus altirostris. Herpetological Review, vol. 38, no. 2, p. 209.; Ávila et al., 2010ÁVILA, RW., KAWASHITA-RIBEIRO, RA., FERREIRA, VL., and STRÜSSMANN, C., 2010. Natural history of the coral snake Micrurus pyrrhocryptus Cope 1862 (Elapidae) from semideciduous forests of western Brazil. South American Journal of Herpetology, vol. 5, no. 2, p. 97-101.), including those dealing with parasites associated with these snakes (Pizzato and Madi, 2002; Silva and Barrella, 2002; 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, vol. 67, no. 4, p. 759-763.; Santos et al., 2008SANTOS, KR., BARRELLA, TH., ZICA, EOP. and SILVA, RJ., 2008. New reports on parasitism by Haplometroides buccicola (Digenea, Plagiorchiidae) in Brazilian snake. Journal of Venomous Animals and Toxins Including Tropical Diseases (Online), vol. 14, no. 3, p. 527-532.; MacAllister et al., 2010).

The semiaquatic coral snake Micrurus surinamensis is widely distributed in equatorial forests in six countries of South America, feeding mainly on bony fishes and eels (Roze, 1966; Morais et al., 2011MORAIS, DH., ÁVILA, RW., KAWASHITA-RIBEIRO, RA. and CARVALHO, MA., 2011. Squamata, Elapidae, Micrurus surinamensis (Cuvier, 1817): New records and distribution map in the state of Mato Grosso, Brazil, with notes on diet and activity period. Checklist, vol. 7, p. 350-351.). In Brazil, this snake has been reported in the states of Acre, Amazonas, Roraima, Rondônia, Pará, Maranhão, Tocantins, Goiás and Mato Grosso (Passos and Fernandes, 2005PASSOS, P. and FERNANDES, DS., 2005. Variation and taxonomic status of the coral snake Micrurus surinamensis (Cuvier, 1817) (Serpentes: Elapidae). Zootaxa, vol. 953, p. 1-14.; Silva Jr. et al., 2008; Morais et al., 2011MORAIS, DH., ÁVILA, RW., KAWASHITA-RIBEIRO, RA. and CARVALHO, MA., 2011. Squamata, Elapidae, Micrurus surinamensis (Cuvier, 1817): New records and distribution map in the state of Mato Grosso, Brazil, with notes on diet and activity period. Checklist, vol. 7, p. 350-351.). Despite this huge distribution, many biological aspects of M. surinamensis have been poorly studied, especially regarding parasitism. The purpose of this note is to report the occurrence of nematode, trematode and pentastomid parasites in M. surinamensis.

2. Material and Methods

Four specimens of Micrurus surinamensis previously fixed and housed in the “Coleção Zoológica de Vertebrados da Universidade Federal de Mato Grosso,” Cuiabá, Brazil (UFMT) were analyzed for parasites. The snakes were collected at three municipalities from Mato Grosso State, all of them in small streams inside alluvial forest in the Amazonian region: one specimen from Juara municipality, a region characterized by the transition of Cerrado-Amazon areas (UFMT 5950; adult female, 968 mm SVL), one from Cotriguaçu municipality, also a region of Cerrado-Amazon transition (UFMT 9270, adult female, 640 mm SVL), and two from Colniza municipality (UFMT 7164, adult female, 782 mm SVL; UFMT 7170, adult male, 678 mm SVL), a region characterized by Alluvial forest. The snakes were initially preserved in 10% formalin and then stored in 70% ethanol. A midventral incision was made in the body wall, and organ surfaces were visually checked for parasites. Subsequently, the lungs and digestive tract were examined under a stereomicroscope for parasites. For identification, nematodes were cleared in phenol, pentastomids were cleared in a drop of Hoyer's medium and trematodes were stained with carmine and cleared in creosote. All parasites were counted and deposited in the Coleção Helmintológica do Instituto de Biociências (CHIBB) at Universidade Estadual Paulista Júlio de Mesquita Filho, São Paulo State, Brazil.

3. Results and Discussion

We recovered 73 specimens of three parasite species (Table 1): 50 larvae of the nematode Physaloptera sp. from the stomach of one snake host (CHIBB 6743); 20 adults of the trematode Opisthogonimus lecithonotus from the mouth and esophagus of one snake host (CHIBB 5068); and 3 nymphs of the pentastomid Sebekia oxycephala in the body cavity of two snake hosts, infected with 1 or 2 nymphs (CHIBB 6744).

Table 1
Epidemiological data for four Micrurus surinamensis and their nematode parasites at the southern Amazonian region, Mato Grosso State, Brazil. For each nematode the prevalence, intensity of infection (mean ± one standard deviation), mean abundance and the sites of infection are given. Abbreviations are: BC = Body cavity and MO = Mouth.

Currently, four species of Physaloptera have been reported infecting reptiles from South America (Physaloptera liophis, P. obtusissima, P. lutzi, and P. retusa), and identification is based on male caudal morphology and length of spicules (Vicente et al., 1993VICENTE, JJ., RODRIGUES, HO., GOMES, DC. and PINTO, RM., 1993. Nematóides do Brasil. Parte III: Nematóides de répteis. Revista Brasileira de Zoologia, vol. 10, no. 1, p. 19-168.). Our specimen could not be identified due to their immature condition. Usually these nematodes use amphibians, lizards and snakes as intermediate hosts (Anderson, 2000).

The pentastomid Sebekia oxycephala is widely distributed, occurring from the southern part of the United States to southern South America (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, vol. 70, no. 2, p. 457-458.). In Brazil, nymphs of S. oxycephala have been reported parasitizing four freshwater fish species: Serrasalmus nattereri, Pseudoplatystoma corruscans and Phallocerus harpagus (see 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, vol. 70, no. 2, p. 457-458.) and Serrasalmus marginatus (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.). Adults of this pentastomid have been reported infecting crocodilian species (Junker and Boomker, 2006JUNKER, K. and BOOMKER, J., 2006. A check-list of the pentastomid parasites of crocodilians and freshwater chelonians. Onderstepoort Journal of Veterinary Research, vol. 73, p. 27-36.). The life cycle of S. oxycephala is well known and involves several freshwater fish species as intermediate hosts (Venard and Bangham, 1941VENARD, CE., and BANGHAM, RV., 1941. Sebekia oxycephala (Pentastomida) from Florida Fishes and Some Notes on the Morphology of the Larvae. 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.; 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, vol. 70, no. 2, p. 457-458.). Heymons (1935)HEYMONS, R., 1935. Bronn's Klassen und Ordnungen des Tierreichs: Pentastomida. Leipzig: Akademische Verlagsgesellschaft MBH. vol. 5, seção 4, livro 1. suggested that nymphs of this pentastomid may also infect lizards and snakes, but Riley (1986)RILEY, J., 1986. The biology of pentastomids. Advances in Parasitology, vol. 25, p. 45-128. considered the source of this information vague and pointed out the need for confirmation. However, nymphs of Sebekia have been reported to infect other Neotropical snakes, such as Helicops leopardinus (Rego and Vicente, 1988REGO, AA. and VICENTE, JJ., 1988. Excursão científica à Zona do Pantanal, Estado de Mato Grosso, para coletas de helmintos. Ciência e Cultura, vol. 40, p. 65-68.), Nerodia spp. (Overstreet et al., 1985OVERSTREET, RM., SELF, JT. and VLIET, KA., 1985. The pentastomid Sebekia mississippiensis sp. n. in the American alligator and other hosts. Proceedings of the Helminthological Society of Washington, vol. 52, p. 266-277.), and Micrurus surinamensis (this work). The infection of these snakes with nymphs of Sebekia, could be related to their semiaquatic habitats (Ávila et al., 2006ÁVILA, RW., FERREIRA, VL. and ARRUDA, JAO., 2006. Natural history of the South American water snake Helicops leopardinus (Serpentes: Colubridae) in the Pantanal, Brazil. Journal of Herpetology, vol. 40, no. 2, p. 274-279.; Morais et al., 2011MORAIS, DH., ÁVILA, RW., KAWASHITA-RIBEIRO, RA. and CARVALHO, MA., 2011. Squamata, Elapidae, Micrurus surinamensis (Cuvier, 1817): New records and distribution map in the state of Mato Grosso, Brazil, with notes on diet and activity period. Checklist, vol. 7, p. 350-351.; Mushinsky et al., 1982MUSHINSKY, HR., HEBRARD, JJ. and VODOPICH, S., 1982. Ontogeny of water snake foraging ecology. Ecology, vol. 63, p.1624-1629.), since nymphs of Sebekia actively infect their intermediate hosts (Junker et al., 1998JUNKER, K., BOOMKER, J. and BOOYSE, DG., 1998. Experimental studies on the life-cycle of Sebekia wedli (Pentastomida: Sebekidae). Onderstepoort Journal of Veterinary Research, vol. 65, p.233-237.). Moreover, the reports of Sebekia infecting the terrestrial coral snake Micrurus alleni (Goldberg and Bursey, 2004GOLDBERG, 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.) could be explained by their piscivorous diet (Roze, 1996ROZE, JA., 1996. Coral Snakes of the Americas: Biology, Identification, and Venoms. Malabar, Florida, USA: Krieger Publishing Company. 328 p.; Cunha and Nascimento, 1978CUNHA, OR. and NASCIMENTO, FP., 1978. Ofídios da Amazônia. X - As cobras da região leste do Pará. Publicações Avulsas do Museu Paraense Emílio Goeldi, vol. 31, p. 1-218.).

Opistogonimus lecithonotus were reported from the oral cavity and esophagus of 22 Neotropical snake species, including one coral snake, Micrurus pyrrhocryptus (Lunaschi and Drago, 2007LUNASCHI, LI. and DRAGO, FB., 2007. Checklist of digenean parasites of amphibians and reptiles from Argentina. Zootaxa, vol. 1476, p. 51-68.). Snakes infected by O. lecithonotus show a high phylogenetic distance and belong to several genera and families (e.g., Dipsadidae, Colubridade, Viperidae and Elapidae; see Lunaschi and Drago, 2007LUNASCHI, LI. and DRAGO, FB., 2007. Checklist of digenean parasites of amphibians and reptiles from Argentina. Zootaxa, vol. 1476, p. 51-68.), with a wide variety of habits (e.g., terrestrial, aquatic, semifossorial) and prey types (e.g., anurans, fishes, snakes, mammals, etc), thus making it difficult to provide general predictions about which ecological aspects of the hosts make them susceptible to infection by this trematode.

In conclusion, despite of our small sample size, the present study makes an important contribution to our knowledge of parasitism in snakes of South America, since M. surinamensis represents a new host record for these three parasite species. Moreover, the state of Mato Grosso is a new locality record for S. oxycephala and O. lecithonotus. Hence, we strongly suggest more studies dealing with parasitism in Neotropical snakes, especially regarding elapids, for a better understanding of ecological processes, such as infracommunity structure and infection patterns.

To Marcos André de Carvalho for allowing access to material under his care at the “Coleção Zoológica de Vertebrados da Universidade Federal de Mato Grosso” (UFMT). We are grateful to the to Conselho Nacional de Desenvolvimento Científico e Tecnológico – CNPq for the research grant awarded to W.O. Almeida (PQ-311713/2012-2); to Fundação Cearense de Apoio ao Desenvolvimento Científico e Tecnológico – FUNCAP for the research grant awarded to R.W. Ávila (BPI-0067-00006.01.00/12).

References

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  • 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, vol. 70, no. 2, p. 457-458.
  • 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, vol. 67, no. 4, p. 759-763.
  • ÁVILA, RW., FERREIRA, VL. and ARRUDA, JAO., 2006. Natural history of the South American water snake Helicops leopardinus (Serpentes: Colubridae) in the Pantanal, Brazil. Journal of Herpetology, vol. 40, no. 2, p. 274-279.
  • ÁVILA, RW., KAWASHITA-RIBEIRO, RA., FERREIRA, VL., and STRÜSSMANN, C., 2010. Natural history of the coral snake Micrurus pyrrhocryptus Cope 1862 (Elapidae) from semideciduous forests of western Brazil. South American Journal of Herpetology, vol. 5, no. 2, p. 97-101.
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  • 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.
  • HEYMONS, R., 1935. Bronn's Klassen und Ordnungen des Tierreichs: Pentastomida. Leipzig: Akademische Verlagsgesellschaft MBH. vol. 5, seção 4, livro 1.
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  • JUNKER, K., BOOMKER, J. and BOOYSE, DG., 1998. Experimental studies on the life-cycle of Sebekia wedli (Pentastomida: Sebekidae). Onderstepoort Journal of Veterinary Research, vol. 65, p.233-237.
  • LUNASCHI, LI. and DRAGO, FB., 2007. Checklist of digenean parasites of amphibians and reptiles from Argentina. Zootaxa, vol. 1476, p. 51-68.
  • MARQUES, OAV., 2002. Natural history of the coral snake Micrurus decoratus (Elapidae) from the Atlantic forest in southeast Brazil, with comments on possible mimicry. Amphibia-Reptilia, vol. 23, p. 228-232.
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  • MUSHINSKY, HR., HEBRARD, JJ. and VODOPICH, S., 1982. Ontogeny of water snake foraging ecology. Ecology, vol. 63, p.1624-1629.
  • OVERSTREET, RM., SELF, JT. and VLIET, KA., 1985. The pentastomid Sebekia mississippiensis sp. n. in the American alligator and other hosts. Proceedings of the Helminthological Society of Washington, vol. 52, p. 266-277.
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  • VICENTE, JJ., RODRIGUES, HO., GOMES, DC. and PINTO, RM., 1993. Nematóides do Brasil. Parte III: Nematóides de répteis. Revista Brasileira de Zoologia, vol. 10, no. 1, p. 19-168.
  • 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.

Publication Dates

  • Publication in this collection
    Aug 2013

History

  • Received
    12 Apr 2012
  • Accepted
    28 Aug 2012
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