Herpetology Notes, volume 12: 1193-1195 (2019) (published online on 08 December 2019)

Note on an event of double : Leptodeira annulata (Linnaeus, 1758) (Serpentes: Dipsadidae) being predated by Drymarchon corais Boie, 1827 (Serpentes: Colubridae), being predated in turn by atrox (Linnaeus, 1758) (Serpentes: Viperidae)

Sóstenes José Souza Pelegrini¹,*, Nathocley Mendes Venâncio², and Adriana Akemi Kuniy¹

Ophiophagy, or the habit of feeding on , is a in the neotropics, and has a generalist diet, feeding behavior known for various animals in different parts of on anurans, , snakes, eggs and the world (Nogueira et al., 2003; Jackson, 2004; Martínez- (Duellman, 1990; Stevenson et al., 2009; Bernarde and Freiria et al., 2006; Dorward, 2014). In the Neotropical Abe, 2010; Prudente et al., 2014). It is worth mentioning region, well-known ophiophagous snakes belong to the that one of the prey items recorded for D. corais is a genera Boiruna Zaher, 1996; Clelia Fitzinger, 1826; Bothrops (Prudente et al., 2014), the speckled Erythrolamprus Boie, 1826; Micrurus Wagler, 1824; forest pit-viper Bothrops taeniatus Wagler, 1824. and Phalotris Cope, 1861 (Abalos and Nader, 1968; Greene, 1983; Lema et al., 1983; Mushinsky, 1987; Results and Discussion Pinto and Lema, 2002). However, ophiophagy has also This note reports an unprecedented event of double been recorded for the common lancehead, Bothrops predation involving snakes. The event was recorded athrox (Gonçalves, 2016), and the yellow-tail cribo, by chance in a road near an area cleared for livestock Drymarchon corais (Duellman, 1990; Stevenson et al., farming and native forest fragments in the rural area 2009; Bernarde and Abe, 2010). Bothrops atrox is a snake of the municipality of Novo Repartimento, in the state from the family Viperidae. Assessments in the wild of of Pará, (coordinates -4.5010° S, -50.7663° W, the activity period of species within the genus Bothrops DATUM WGS 84, 167 m elev.). On the 23rd of January (sensu lato) indicate a tendency toward nocturnal and 2018, at approximately 23:30h, we observed in the crepuscular patterns widespread throughout the Amazon field an event of predation of a Drymarchon corais by (Hartmann et al., 2003). Studies on its feeding behavior a Bothrops atrox (Fig. 1A). The recorded individual of indicate ontogenetic differences, with smaller, younger B. atrox had already started the process of ingesting its individuals feeding on ectothermic prey, while larger, prey but, soon after we met it, it started regurgitating. adult individuals indicates a tendency for endotherms After the individual of D. corais was fully expelled, we prey (Gonçalves, 2016). The species’ diet includes observed that it had also started the ingestion of another amphibians, marsupials, rodents and lizards, besides snake (Fig. 1B), having probably been interrupted by other snakes (Silva et al., 2010). Drymarchon corais is the B. atrox attack. The snake predated by the D. corais a diurnal and terrestrial Colubridae snake widespread specimen was a banded cat-eyed snake, Leptodeira annulata (Fig. 1C–F) The publication of notes like the present one is important to help mitigate the current lack of field studies on snake ecology. These studies are hard to 1 JGP Consultoria e Participações Ltda., R. Américo Brasiliense perform due to the relatively scarcity of field records 615, Alto da Boa Vista, São Paulo, São Paulo 04715-000, of these animals, in large part as a result of their cryptic Brazil. 2 Faculdade Meta (FAMETA), Estrada Alberto Torres 947, Rio coloration, the nocturnal behaviour of many species, Branco, Acre 69919-230, Brazil. and their low displacement capacity (Fraga et al., 2013). * Corresponding author. E-mail: [email protected] This note is also relevant because, while ophiophagy 1194 Sóstenes José Souza Pelegrini et al.

Figure 1. (A) Bothrops atrox swallowing an Drymarchon corais. (B) Moment when the Drymarchon corais was fully regurgitated. (C) Leptodeira annulata predated by the registered Drymarchon corais. (D) Detail showing the venter of the Leptodeira annulata predated by Drymarchon corais. (E) Detail showing the dorsum of the Leptodeira annulata predated by Drymarchon corais. (F) Leptodeira annulata after full removal from the digestive tract of the Drymarchon corais.

is known for smaller, younger individuals of B. atrox, MZUSP 22843 and Leptodeira annulata: MZUSP the specimen recorded predating an specimen of D. 22844). The B. atrox specimen was released near the corais was an adult, measuring approximately 76 cm. site where the snakes were sighted. It is important to Although B. atrox is considered a generalist feeder, mention that the head of the individual of Drymarchon its diet, and especially its ophiophagous behaviour, corais shows a snout-vent length (SVL) measurement are poorly studied (Gonçalves, 2016). This is, in fact, of 627 mm and the TL of 134 mm, since Leptodeira the first record of D. corais predation by B. atrox. As annulata shows the SVL of 481 mm and the TL of 174 mentioned above, D. corais is also known to display mm, but the tail was fragmented, which makes those ophiophagous behaviour. However, this is also the first inaccurate measures. record of the species predating L. annulata. Acknowledgments. We thank BMTE (Belo Monte Transmissora The individuals of D. corais and L. annulata were de Energia) and JGP Consultoria e Participações for supporting collected and deposited in the Museu de Zoologia da and organizing field logistics. We also thank IBAMA (Instituto Universidade de São Paulo (MZUSP), as they were Brasileiro do Meio Ambiente e dos Recursos Naturais Renováveis already dead when registered (Drymarchon corais: – “Brazilian Institute for the Environment and Renewable Natural Note on an event of double predation 1195

Resources”) for issuing the necessary collection and capture Lema, T., Araujo, M.L., Azevedo, A.C.P. (1983): Contribuição ao permit (IBAMA 651/2015). conhecimento da alimentação e do modo alimentar de serpentes do Brasil. Comunicação do Museu de Ciências da PUCRS, References Série Zoologia 26: 41–121. Martínez-Freiria, F., Brito, J.C., Lizana Avia, M. (2006): Abalos, J., Nader, R. (1968): Los habitos de Pseudoboa cloelia y Ophiophagy and in Vipera latastei Bosca, 1878 Pseudoboa maculata. Revista da Faculdade de Ciências Médicas (Reptilia, Viperidae). Herpetological Bulletin 96: 26–28. da Universidade Nacional de Córdoba 60: 5–12. Mushinsky, H.R. (1987): Foraging ecology. In: Snakes: Ecology Bernarde, P.S., Abe, A.S. (2010): Hábitos alimentares de serpentes and Evolutionary Biology, pp. 302–334. Seigel, R.A., Collins, em Espigão do Oeste, Rondônia, Brasil. Biota Neotropica 10 J.T., Novak, S.S., Eds., New York, USA, McMillan Press. (1): 167–173. Nogueira, C., Sawaya, R.J., Martins, M. (2003): Ecology of the Dorward, L. (2014): Predation of Elaphe dione (Pallas, 1773) by pitviper, Bothrops moojeni, in the Brazilian Cerrado. Journal of Dolichophis caspius (Gmelin, 1789) (Squamata: Colubridae). Herpetology 37: 653–659. Herpetology Notes 7: 165–166. Pinto, C.C., Lema, T. (2002): Comportamento alimentar e dieta de Duellman, W.E. (1990): Herpetofaunas in neotropical rainforests: serpentes, gêneros Boiruna e Clelia (Serpentes, Colubridae). comparative composition, history, and resource use. In: Four Iheringia Série Zoologia 92: 9–19. Neotropical Rainforest, pp. 455–487. Gentry, A.H., Ed., Prudente, A.L.C., Menks, A.C., Silva, F.M., Maschio, G.F. (2014): Connecticut, USA, Yale University Press. Diet and reproduction of the Western Indigo Snake Drymarchon Fraga, R., Lima, A.P., Prudente, A.L., Magnusson, W.E. (2013): corais (Serpentes: Colubridae) from the Brazilian Amazon. Guia de cobras da região de Manaus – Amazônia Central. Herpetology Notes 7: 99–108. Manaus, Brazil, INPA. Silva, M.V., Souza, M.B., Bernarde, P.S. (2010): Riqueza e dieta Greene, H.W. (1983): Dietary correlates of the origin and radiation de serpentes do Estado do Acre, Brasil. Revista Brasileira de of snakes. American Zoologist 23: 431–442. Zoociências 12: 165–176. Gonçalves, P.F.B. (2016): Biologia reprodutiva e alimentar de Stevenson, D.J., Enge, K.M., Carlile, L.D., Dyer, K.J., Norton, Bothrops atrox (Serpentes, Viperidae) nas regiões central T.M., Hyslop, N.L., Kiltie, R.A. (2009): An e sudoeste da Amazônia. Unpublished MSc dissertation, (Drymarchon couperi) mark-recapture study in southeastern Universidade Federal do Amazonas, Amazonas, Brazil.. Georgia. Herpetological Conservation Biology 4: 30–42. Hartmann, P.A., Teresinha, M, Olímpio, L, Giasson, M. (2003). Uso do e alimentação em juvenis de Bothrops jararaca (Serpentes: Viperidae) na Mata Atlântica do Sudeste do Brasil. Phyllomedusa 2: 35–41. Jackson, K., Kley, N.J., Brainerd, E.L. (2004): How snakes eat snakes: the biomechanical challenges of ophiophagy for the California , Lampropeltis getula californiae (Serpentes: Colubridae). Zoology 107: 191–200.

Accepted by Clarissa Canedo