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New Record of Physaloptera Sp. (Nematoda: Physalopteridae) Parasitizing Philodryas Nattereri (Ophidia: Dipsadidae) in Brazil

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New Record of Physaloptera Sp. (Nematoda: Physalopteridae) Parasitizing Philodryas Nattereri (Ophidia: Dipsadidae) in Brazil Herpetology Notes, volume 12: 1031-1034 (2019) (published online on 27 October 2019) New record of Physaloptera sp. (Nematoda: Physalopteridae) parasitizing Philodryas nattereri (Ophidia: Dipsadidae) in Brazil Monique Celião de Oliveira1,*, Vandeberg Ferreira Lima1, Cicero Leonardo de Morais Pinto1, Érica Gomes da Silva1, Diêgo Alves Teles2, Cristiana Ferreira-Silva3, and Waltécio de Oliveira Almeida4 Parasites are important regulators of animal to infection by opportunistic bacteria (Barbosa et al., populations, affecting fertility (Dunlap and Schall, 2006). 1995), feeding behaviour (Roca et al., 2005), habitat Philodryas nattereri Steindachner, 1870 (Fig. 1) is a use (Comas and Ribas, 2013; Hamann et al., 2013), member of the family Dipsadidae, (Ferrarezzi, 1994; phylogeny (Muñoz et al., 2006; Brito et al., 2014b), Zaher et al., 2009; Vidal et al., 2010; Uetz et al., 2017) and body size and mass (Korallo et al., 2007; Campião and one of the most common snake species northeastern et al., 2015) of their hosts. Snakes are parasitized by a Brazil (Mesquita et al., 2013). It is a medium-sized wide variety of endoparasites (e.g., Silva et al., 2001), snake (maximum snout–vent length recorded in and the majority of those occurring in the digestive tract males 1260 mm; Mesquita et al., 2011) with a wide are nematodes. This type of parasite is known to cause distribution in arid and semi-arid regions of Brazil and tissue and organ damage and may even lead to the local Paraguay (Calixto and Morato, 2017; Uetz et al., 2017). extinction of their host population (e.g., Farrell et al., An active forager, P. nattereri has a generalist diet that 2015). includes lizards, birds, mammals, and amphibians (Vitt The nematode genus most commonly found in snakes and Vangilder, 1983; França et al., 2008; Mesquita et is Physaloptera Rudolphi, 1819 (see Barbosa et al., al., 2011). 2006). This nematode has a filarial body with a caudal region that includes two thin “lips” that are possibly Material and Methods used for locomotion. Adults can reach a maximum On 3 May 2015 a female P. nattereri (snout–vent length length of 48 mm (Barbosa et al., 2006). Infections by 825 mm, tail length 319 mm, weight 257 g) was found Physaloptera can cause ulcerations, haemorrhages, and dead on a road in the municipality of Farias Brito, Ceará excessive digestive secretions (Araújo, 1999), leading 1 Laboratório de Zoologia, Universidade Regional do Cariri, Rua Coronel Antônio Luiz, 1161, Campus do Pimenta, Crato, Ceará 63105-000, Brazil. 2 Laboratório de Herpetologia, Universidade Federal da Paraíba, Cidade Universitária, Campus I, João Pessoa, Paraíba 58059- 900, Brazil. 3 Departamento de Parasitologia, Instituto de Biociências, Universidade Estadual Paulista Avenida Bento Lopes s/n, Distrito de Rubião Junior, Botucatu, São Paulo 18080-970, Brazil. 4 Departamento de Química Biológica, Universidade Regional do Cariri, Rua Coronel Antônio Luiz, 1161, Campus do Figure 1. Adult Philodryas nattereri from Farias Brito Pimenta, Crato, Ceará 63105-000, Brazil. Municipality, Ceará State, northeastern Brazil. Photo by * Corresponding author. E-mail: [email protected] Herivelto F. Oliveira. 1032 Monique Celião de Oliveira et al. Figure 2. (A) Cephalic and (B) caudal extremities of Physaloptera sp. recovered from a specimen of Philodryas nattereri in northeastern Brazil. Photos by Érica G. Silva. State, northeastern Brazil (ca. 6.7833°S, 39.5332°W), to the knowledge of the helminth parasite fauna in apparently the victim of an accident. The specimen was snakes. In the literature there are few studies that have collected and taken to the Laboratory of Zoology at the investigated the helminths associated with snakes in Regional University of Cariri, where it was measured, the Caatinga biome in northeastern Brazil (Almeida et fixed in 10% formalin and preserved in 70% ethanol, al., 2006, 2007, 2008; Araujo-Filho et al., 2013, 2018; then deposited in the herpetological collection of the Oliveira et al., 2018). Universidade Regional do Cariri (specimen number In the Caatinga biome, infection with Physaloptera sp. URCA H13.5200). The gastrointestinal tract was has been reported previously in both amphibians (Teles removed for dissection and endoparasite analysis using et al., 2017) and reptiles (Silva et al., 2017; Teles et al., a stereomicroscope. 2017; Oliveira et al., 2015). Nematodes of the genus Physaloptera have a life cycle that includes insects Results and Discussion (e.g., crickets, grasshoppers, cockroaches, beetles) as intermediate hosts (e.g., Gray and Anderson, 1982), and One of the parasite specimens found in the stomach of P. these are important items in the diets of lizards (Pontes nattereri was identified as a larval stage of Physaloptera et al., 2009; Ribeiro et al., 2011; Albuquerque et al., sp. (parasitological collection of Universidade Regional 2018) and amphibians (Oliveira et al., 2014; Teles et al., do Cariri, specimen number URCA P1210; Fig. 2). 2018). In turn, lizards and amphibians are prey items for Infection with nematodes of the genus Physaloptera snakes of the genus Philodryas (Mesquita et al., 2013; has already been reported in the snakes Philodryas Menezes et al., 2013). sp. (Dipsadidae), Xenodon merremii (Dipsadidae), Boa constrictor (Boidae), Micrurus surinamensis Acknowledgments. The authors thank the Conselho Nacional (Elapinae), and Crotalus viridis (Viperidae) (Travassos de Desenvolvimento Científico e Tecnológico (CNPq) for and Freitas, 1943; Widmer, 1967, 1970; Barbosa et al., scholarships granted to EGS, CLMP, DAT, and WOA. 2006; Ávila et al., 2013; Tavares et al., 2017). Previous reports of parasite infection for P. nattereri include References only pentastomid worms, namely Cephalobaena Albuquerque, R.L., Protázio, A.S., Cavalcanti, L.B.Q., Lopez, tetrapoda and Raillietiella furcocerca (Almeida et al., L.C.S., Mesquita, D.O. (2018): Geographical ecology 2007, 2008), and, most recently, the acanthocephalan of Tropidurus hispidus (Squamata: Tropiduridae) and Oligacanthorhynchus sp. (Araujo-Filho et al., 2018). Cnemidophorus ocellifer (Squamata: Teiidae) in a neotropical Our study presents the first record of the nematode region: a comparison among Atlantic Forest, Caatinga, and Physaloptera sp. parasitizing P. nattereri, contributing coastal populations. Journal of Herpetology 52 (2): 145–155. New record of Physaloptera sp. parasitizing Philodryas nattereri in Brazil 1033 Almeida, W.O., Brito, S.V., Ferreira, F.S., Christoffersen, M.L. Diseases 11 (1): 41–44. (2006): First record of Cephalobaena tetrapoda (Pentastomida: Dunlap, K.D., Schall, J.J. (1995): Hormonal alteration and Cephalobaenidae) as a parasite on Liophis lineatus (Ophidia: reproductive inhibition in male fence lizards (Sceloporus Colubridae) in Northeast Brazil. Brazilian Journal of Biology occidentalis) infected with the malarial parasite Plasmodium 66 (2A): 559–564. mexicanum. Physiological Zoology 68: 608–621. Almeida, W.O., Guedes, T.B., Freire, E.M.X., Vasconcellos, Farrell, M.J., Stephens, P.R., Berrang-Ford, L., Gittleman, J.L., A. (2008): Pentastomid infection in Philodryas nattereri Davies, T.J. (2015): The path to host extinction can lead to loss Steindachner, 1870 and Oxybelis aeneus (Wagler, 1824) of generalist parasites. Journal of Animal Ecology 84: 978–984. (Squamata: Colubridae) in a caatinga of northeastern Brazil. Ferrarezzi, H. (1994): Uma sinopse dos gêneros e classificação das Brazilian Journal of Biology 68 (1): 193–197. serpentes (Squamata) II. Familia Colubridae. In: Herpetologia Almeida, W.O., Vasconcellos, A., Lopes, S.G., Freire, E.M.X. no Brasil I, p. 81–91. Nascimento, L. B., Bernardes, A. T., Cotta, (2007): Prevalence and intensity of pentastomid infection in two G. A., Eds., Belo Horizonte, Brazil, Fundação Biodiversitas & species of snakes from Northeastern Brazil. Brazilian Journal of Fundação Ezequiel Dias. Biology 67 (4): 759–763. França, F.G.R., Mesquita, D.O., Nogueira, C.C., Araújo, A.F.B. Araujo Filho, J.A., Oliveira, C.R., Ávila, R.W., Roberto, I.J., (2008): Phylogeny and ecology determine morphological Almeida, W.O. (2013): Natural history notes. Lachesis structure in a snake assemblage in the central Brazilian Cerrado. muta (Surucucu, Atlantic Forest Bushmaster). Parasitism. Copeia 2008 (1): 23–38. Herpetological Review 44: 43. Gray, J.B., Anderson, R.C. (1982): Development of Turgida Araujo Filho, J.A., Teles, D.A. Teixeira., A.A.M., Sakamoto, turgida (Rudolphi, 1819) in the common field cricket (Acheta A.C.F.L., Pinto, C.L.M., Silva, É.G., Almeida, W.O. (2018): pennsylvanicus Burmeister). Canadian Journal of Zoology 60 Natural history notes. Philodryas nattereri (Run-Snake). (9): 2134–2142. Endoparasites. Herpetological Review 49(1): 138. Hamann, M.I., Kehr, A.I., Gonzalez, C.E. (2013): Biodiversity of Araujo, T., Moro, L., Lúcia, M., Golloubeff, B., Vasconcelos, A.C. trematodes associated with amphibians from a variety of habitats (1999): Occurrence of some endo- and ectoparasites in the in Corrientes Province, Argentina. Journal of Helminthology 87: serpentarium of UNIFENAS. Brazilian Journal of Veterinary 286–300. Research and Animal Science 36 (1): 1–10. Korallo, N.P., Vinarski, M.V., Krasnov, B.R., Shenbrot, G.I., Ávila, R.W., Morais, D.H., Anjos, L.A., Almeida, W.O., Silva, R.J. Mouillot, D., Poulin, R. (2007): Are there general rules governing (2013): Endoparasites infecting the semiaquatic coral snake parasite diversity? Small mammalian hosts and gamasid mite Micrurus surinamensis (Squamata: Elapidae) in the southern
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