Herpetology Notes, volume 13: 171-173 (2020) (published online on 26 February 2020)

Predation of Tropidurus hispidus (, Tropiduridae) by aeneus (Squamata, ) in two biomes in the state of Pernambuco, Northeast of Brazil

Juliana D. de Sousa¹, José Henrique de A. Lima¹,*, and Marcelo N. de C. Kokubum¹

The in Brazil have been studied through several such as rocks, tree trunks, and even urban environments approaches, including diet (e.g. Pinto and Lema, 2002; (Rodrigues, 1987). In this study, are presented two Pizzatto et al., 2009), predation and other behaviour data predation events involving O. aeneus and T. hispidus in (Bernarde and Abe, 2010; Guedes et al., 2014). Most two distinct biomes (Caatinga and Atlantic Rainforest) of this information refers to predation events involving in northeastern Brazil. None of the specimens were as preys (e.g. Kokubum and Lemos, 2004; Sales collected, and the records were based on our observations et al., 2010; Costa-Campos and Souza, 2013; Robbins and photographs. et al., 2013; Passos et al., 2016; Pergentino et al., 2017), The first record occurred on the 7th of September 2018, demonstrating the importance of this group at 0900 h, in a Caatinga area at Sítio Fechado (7.2992°S, for the diet of many . However, more 37.2978°W; Datum WSG84; 737 m elevation), naturalistic observations are needed to understand the Municipality of Brejinho, State of Pernambuco, Brazil. predator-prey relation, since there are many unusual One adult individual of O. aeneus was seen above a or unprecedented behaviours in the outcome of this shrub’s branches, with its head close to the ground (~8cm) interaction. and suspended on the branches (vertical position), with Oxybelis aeneus (Wagler, 1824) is an arboreal snake, an adult individual of T. hispidus, immobilized by the widely distributed on the American continent, occurring head, in its mouth. After 20 minutes, the snake begun from the south of North America, Central America, to execute several jaw movements to swallow the and most of the South American continent (Savage, and, 3 minutes later, the snake had ingested up to part of 2002). Its foraging strategy is the sit-and-wait type, the prey´s forelimbs (Fig. 1A). Subsequently, the snake with a diverse diet, which includes , small arboreal tried to lift its head above the branches (like the rest of mammals, insects (e.g. Campbell, 1998) and fishes its body) and, in this moment, the prey almost fell on the (e.g. Hetherington, 2006), although with a preference ground, but the snake was able to hold the lizard (Fig. for lizards (Henderson, 1982; Campbell, 1998; Savage, 1B). After 13 minutes, the prey was completely ingested 2002; Grant and Lewis, 2010). by the snake still suspended on the branches and, finally, The lizard Tropidurus hispidus (Spix, 1825) is widely the snake went away. The whole observation and distributed in the Northeast of Brazil (Días-Uriarte, photography event lasted approximately 40 minutes. 1999; Abreu et al., 2002), being an abundant and The second event occurred on the 14th of June 2019, generalist species. Regarding its habitat, T. hispidus at 1015 h, in an Atlantic Rainforest area at Refúgio de can be sighted in the most variable types of substrates, Vida Silvestre Matas do Siriji (7.6159°S, 35.5050°W; Datum WSG84; 570 m elevation), Municipality of São Vicente Férrer, State of Pernambuco, Brazil. As well as the previously described event, an adult individual of O. aeneus, suspended over the shrub vegetation (~190 cm high), captured by the head (Fig. 2) an adult ¹ Laboratório de Herpetologia, Unidade Acadêmica de Ciências individual of T. hispidus which was on the ground. After Biológicas, Centro de Saúde e Tecnologia Rural, Universidade Federal de Campina Grande, Jatobá, Patos, Paraíba 58708- 10 minutes trying to swallow the prey, the snake, still 110, Brazil. suspended on the branches, gave up, released the dead * Corresponding author. E-mail: [email protected] lizard and went away. 172 Juliana D. de Sousa et al.

Figure 1. Frontal (A) and lateral (B) views of Oxybelis aeneus on attempted predation on Tropidurus hispidus at Sítio Fechado, a Caatinga area in the Municipality of Brejinho, State of Pernambuco, Brazil.

There are several records of saurophagy regarding O. aeneus, most of which are based on the analysis of the stomach contents of the snakes, being found the species Ameivula ocellifera (Spix, 1825), Tropiduris hispidus, Brasiliscincus heathi (Schmidt and Inger, 1951), and Hemidactylus mabouia (Moreau de Jonnès, 1818) (Mesquita et al., 2012), and only a few are based on observations in nature: Tropidurus semitaeniatus (Spix, 1825), Ameivula ocellifera, and Lygodactylus klugei (Smith, Martin and Swain, 1977) (Vitt and Vangilder, 1983), Tropidurus hygomi Reinhardt and Lutken, 1862 (Santos et al., 2012), Basiliscus plumifrons Cope, 1875 (Grant and Lewis, 2010), and Hemidactylus mabouia (Lissa et al., 2018). Despite the fact that Mesquita et al (2012) had already recorded T. hispidus as a prey item for O. aeneus based on the analysis of stomach contents, here we describe processes of capturing and ingesting the prey. We draw attention to the fact that, in both cases, the snakes were suspended over vegetation, perpendicular to the soil, when they captured and ingested (or tried to ingest) the prey. This strategy, despite making it more difficult to the immobilization and intake of prey Figure 2. Oxybelis aeneus on attempted predation on (especially those larger), seems to be common to the Tropidurus hispidus at Refúgio de Vida Silvestre Matas do species. Moreover, the fact that the snakes did not go Siriji, an Atlantic Rainforest area in the Municipality of São down to the ground to better immobilize the prey, risking Vicente Férrer, State of Pernambuco, Brazil. losing it, demonstrates its extremely arboreal habit. Also, Predation of Tropidurus hispidus by Oxybelis aeneus in two biomes, Brazil 173 we emphasize that T. hispidus is a species with a sit-and- a vine snake Oxybelis aeneus (Serpentes: Colubridae) in an wait foraging behaviour (Schoener, 1971), becoming Atlantic Forest fragment, Northeastern Brazil. Pesquisa e Ensino an easy prey for the O. aeneus, considering this lower em Ciências Exatas e da Natureza 2: 67–70. Maia-Carneiro, T., Goyannes-Araújo, P., Rocha, C.F.D. (2016): mobility aspect. On the other hand, according to Greene Predation of Tropidurus hispidus (Squamata, Tropiduridae) by (1976), the position in which the prey is captured can leucocephalus (Squamata, Dipsadidae). Neotropical facilitate or complicate the deglutition, and when the Biology and Conservation 11: 47–50. prey is caught by the head, the predation is more efficient Mesquita P.C.M.D., Borges-Nojosa D.M., Passos D.C., Bezerra because it reduces the resistance caused by the prey’s C.H. (2012): Activity patterns of the Brown Vine snake Oxybelis body surface, so the predator spend less time and energy. aeneus (Wagler, 1824) (Serpentes, Colubridae) in the Brazilian This strategy is even more necessary for lizards such as semiarid. Animal Biology 62: 289–299. Passos, D.C., Monteiro, F.A.C., Nogueira, C.H.O. (2016): T. hispidus, that has mucronate scales (Maia-Carneiro Dangerous neighborhood: saurophagy between syntopic et al., 2016), which complicates the manipulation and Tropidurus lizards. Biota Neotropica 16: 1–5. ingestion. Another element that can prevent this process Pergentino, H.E.S., Nicola, P.A., Pereira, L.C.M., Novelli, I.A., is the prey size, the reason, we believe, that determined Ribeiro, L.B. (2017): A new case of predation on a lizard by the outcoming of the second event described herein. Tropidurus hispidus (Squamata, Tropiduridae), including a list Eventually, predators give up very large prey, which of saurophagy events with lizards from this as predators could lead to a high energy expenditure or even death in Brazil. Herpetology Notes 10: 225–228. Pinto, C.D.C., Lema, T. De. (2002): Comportamento alimentar by obstruction of the respiratory tract, even for snakes, e dieta de serpentes, gêneros Boiruna e Clelia (Serpentes, that have highly kinetic skulls. Colubridae). Iheringia, Série Zoologia 92: 9–19. Pizzatto, L., Marques, O.A.V., Facure, K. (2009): Food habits of References Brazilian boid snakes: overview and new data, with special reference to Corallus hortulanus. Amphibia-Reptilia 30: 533– Abreu, M.L.S., Frota, J.G., Yuki, R.N. (2002): Geographic 544. distribution, Tropidurus hispidus. Herpetology Review 33: 66. Robbins, T.R., Schrey, A., McGinley, S., Jacobs, A. (2013): On Bernarde, P.S., Abe, A.S. (2010): Hábitos alimentares de serpentes the incidences of cannibalism in the lizard genus Sceloporus: em Espigão do Oeste, Rondônia, Brasil. Biota Neotropica 10: updates, hypotheses, and the first case of siblicide. Herpetology 167–173. Notes 6: 523–528. Campbell, J.A. (1998): The amphibian and of northern Rodrigues, M.T. (1987): Sistemática, Ecologia e zoogeografia dos Guatemala, the Yucatán, and Belize. Norman, USA, University Tropidurus do grupo torquatus ao sul do Rio Amazonas (Sauria, of Oklahoma Press. Iguanidae). Arquivos de Zoologia de São Paulo 31: 105–230. Costa-Campos, C.E., Souza, N.S. (2013): Tropidurus hispidus Sales, R.F.D., Ribeiro, L.B., Almeida, H.W.B., Freire, E.M.X. (Peters’ Lava Lizard). Saurophagy. Herpetological Review 44: (2010): Ameiva ameiva (Giant Ameiva). Saurophagy. 515–516. Herpetological Review 44: 72–73. Díaz-Uriarte, R. (1999): Anti-predator behaviour changes Santos, R.A., Santana, D.O., Caldas, F.L.S., Faria, R.G. (2012): following an aggressive encounter in the lizard Tropidurus Tropidurus hygomi (reinhardt’s lava lizard). Predation. hispidus. Proceedings Royal Society London Biological 266: Herpetological Review 43(3): 490-491. 2457–2464. Savage, J.M. (2002): The amphibians and reptiles of Costa Rica. Grant, P.B.C., Lewis T.R. (2010): Predation attempt by Oxybelis Chicago, USA, University of Chicago Press. aeneus (Wagler) (Mexican Vinesnake) on Basiliscus plumifrons Schoener, T.W. (1971): Theory of feeding strategies. Annual (Cope). Acta Herpetologica 5: 19–22. Review Ecology Systematics 2: 369–404. Greene, H.W. (1976): Scale overlap, a directional sign stimulus Vitt, L.J., Vangilder, L.D. (1983): Ecology of a snake community in for prey ingestionby ophiophagous snakes. Zeitschrift northeastern Brazil. Amphibia-Reptilia 4: 273–296. Tierpsychologie 41: 113–120. Guedes, T.B., Nogueira, C., Marques, O.A.V. (2014) Diversity, natural history, and geographic distribution of snakes in the Caatinga, Northeastern Brazil. Zootaxa, 3863(1): 1–93. Henderson, R.W. (1982): Trophic relationships and foraging strategies of some new world tree snakes (Leptophis, Oxybelis, Uromacer). Amphibia-Reptilia 3: 71–80. Hetherington, T.E. (2006): Oxybelis aeneus. Diet. Herpetological Review 37: 94–95. Kokubum, M.N.C., Lemos, F.G. (2004): Tropidurus torquatus (calango). saurophagy. Herpetological review 35: 270–271. Lissa, D.F., Carmem, K.B.P., Lucas, B.Q.C., Daniel, O.M. (2018): Accepted by Pedro Pinna Predation of Hemidactylus mabouia (Sauria: Gekkonidae) by