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Herpetology Notes, volume 7: 123-126 (2014) (published online on 11 April 2014) Predation of six anuran species by the banded cat-eyed snake, Leptodeira annulata (Serpentes: Dipsadidae), in the Caatinga scrub of northeastern Bahia, Brazil Carlos R. Santos-Silva1*, Igor S. Andrade 2, Maria L. N. Araújo 2, Lívia Claudia S. Barros2, Lidiane Gomes 2 and Stephen F. Ferrari3 Introduction Material and methods Snakes are the main predators of anurans in habitats surrounding bodies of water (Sazima and Haddad, 1992; Wells, 2007; Bernarde and Abe, 2010). Some snake species prey almost exclusively on amphibians, which contribute up to 90% of their diets (Mushinsky et al., 1982). However, detailed observations of predation events are rare due to the difficulties of monitoring these animals in the wild (Malkmus, 2000; Lima and Colombo, 2008). The banded cat-eyed snake, Leptodeira annulata, is widely distributed in Neotropical wetlands between Mexico and Argentina (Carvalho et al., 2005). The snakes of this genus are typically batracophagous, feeding on adult amphibians in shrubs or trees near the water’s edge, or on their egg clutches or tadpoles (Duellman, 1978; Martins and Oliveira, 1998; Jungfer and Weygoldt, 1999; Bernarde and Abe 2010; Sales et al., 2013). These snakes are opistoglyphic and have a relatively simple form of venom, in comparison with other snakes (Mebs, 1968; Nascimento et al., 2013). The present study describes the behavior of L. annulata during the predation of six anuran species in the Raso da Catarina Ecological Station in the semi-arid zone of northeastern Bahia, Brazil. The events described here were recorded between March 2010, and February 2011. The study site was a temporary pond within the palm-dominated, shrubby-arboreal Caatinga scrub in Jeremoabo, Bahia (9.916944°S, 38.698611°W, datum SAD-69; elev. 444 m a.s.l.). Nocturnal observations were conducted at the site between 18:00 h and 01:00 h. Snake length was estimated based on photographs taken of each event (see Costa-Pereira et al., 2010), with the snake being compared with nearby objects (leaves, rocks, branches and so on), which were measured in the field. Behavioral data were collected ad libitum through continuous observation (Del-Claro, 2004), focusing on the aspects of the event considered to be most relevant in terms of the predatory behavior. Photographs were taken of each event, and have been deposited in the herpetological collection of the Federal University of Sergipe (UFS) in São Cristóvão, Sergipe, Brazil. The anuran species were identified based on direct observation in the field and comparisons with specimens deposited in the herpetological collections at UFS and the Bahia State University at Feira de Santana (UEFS). Graduate Program in Ecology and Conservation, Universidade Federal de Sergipe, 49100-000 São Cristóvão – SE, Brazil; 2 Department of Education, Universidade do Estado da Bahia, Campus VIII, Paulo Afonso – BA, Brazil; 3 Department of Ecology, Universidade Federal de Sergipe, São Cristóvão – SE, Brazil. * Corresponding author: e-mail: [email protected] 1 Results Six predation events involving Leptodeira annulata were recorded, each involving a distinct anuran species. The predation of Hypsiboas crepitans (Figure 1-a) was observed on October 22nd, 2010, between 19:25 h and 19:52 h. This event involved the largest L. annulata specimen (total length, TL = 850 mm) recorded in the present study. The strike was not observed. The prey was already dead and the ingestion process had begun when the animals were sighted. The predation on Phyllomedusa bahiana (Figure 1-b) occurred on December 17th, 2010, between 22:22 h and 124 Carlos R. Santos-Silva et al. Figure 1. Anurans captured by Leptodeira annulata in the Raso da Catarina Ecological Station, Bahia, Brazil, between March, 2010, and February, 2011: (a) Hypsiboas crepitans; (b) Phyllomedusa bahiana; (c) Rhinella granulosa; (d) Leptodactylus troglodytes; (e) Scinax x-signatus; (f) Physalaemus kroyeri (Photos: Santos-Silva, C.R.). 00:15 h. This was the longest event recorded here. An adult male P. bahiana was initially observed calling, perched on dry branches at the water’s edge. A large L. annulata (TL = 765 mm) attacked the frog, striking at the mid region of the body, close to the hindlimbs. The frog emitted distress calls and moved its forelimbs in an effort to free itself by pulling on dry twigs while grasping the neck of the snake with its left foot. The bitten area of the frog’s body and the snake’s head became covered with the peptide secretion produced by the glands of P. bahiana. After approximately 29 minutes, the frog succumbed to the attack and the snake pulled it into a shrub (Capparis yco) and began swallowing it. The predation of Rhinella granulosa (Figure 1-c) was observed on January 21st, 2011, between 19:16 h and 20:51 h. A medium-sized L. annulata (approximate TL= 650 mm) was observed head-down in a vertical position in the dry branches of a shrub (Croton sp.) Predation of six anuran species by the banded cat-eyed snake, Leptodeira annulata around 15 cm above the ground, when it attacked and held on to a calling male R. granulosa by the middle of its body. The toad emitted distress calls intensely and moved its limbs during the first 5 min in an attempt to free itself from the snake. Another 16 minutes passed before the toad became completely motionless and was presumably dead. It was then swallowed head-first. The duration of the event, from the strike until the complete ingestion of the prey, lasted 1 h and 35 min. The predation on Leptodactylus troglodytes (Figure 1-d) occurred on February 23rd, 2011, between 19:48 h and 20:23 h. An adult female L. troglodytes was observed at the water’s edge, close to a calling male when it was captured by a large Leptodeira annulata (TL = 740 mm) that was foraging actively in the dry vegetation. The anuran was captured by a rapid strike to the middle of its body, slightly closer to the forelimbs. During the first six minutes, the anuran moved its limbs vigorously in an attempt to escape the attack. The snake then began to ingest the anuran by the head, together with the left front limb, swallowing the animal as far as the scapular girdle, when it stopped for five minutes, until the prey had become completely motionless. The snake swallowed the rest of the frog using rhythmic movements of its mandible. During this process, the snake’s fangs ruptured the inguinal tissue of the frog’s body, causing its mature eggs to spill out. The predation of Scinax x-signatus (Figure 1-e) was observed on February 25th, 2011, between 22:16 h and 22:32 h. A medium-sized L. annulata (TL = 600 mm) was observed foraging on the branches of a small bush (Croton sp.) with its head pointing downwards approximately 80 cm above the ground. It then seized by the head a calling male S. x-signatus perched approximately 10 cm away. Following the attack, the frog inflated its body and moved its limbs rapidly in an attempt to free itself during the next three minutes. The snake held the prey by the head for another two minutes until its movements had ceased completely, and then it began to ingest the frog. The whole event lasted 16 minutes. The predation on Physalaemus kroyeri (Figure 1-f) occurred onFebruary 25th, 2011, between 22:23 h and 22:29 h. This event involved the smallest L. annulata (TL = 480 mm) recorded here. The strike was not observed, although the frog was still alive when the animals were first encountered. The snake had the hindlimbs of the frog in its mouth as far as the median portion of the animal’s body, which was inflated. The frog was drawn into the digestive tract of the snake while still moving its 125 eyes and forelimbs, through movements of the mandible and then accommodated with lateral undulations and peristaltic movements. Discussion The predation events recorded in this study were consistent with those observed in other ecosystems, in particular the relative vulnerability of anurans during the reproductive season (Duellman and Trueb, 1986; Pough et al., 1998; Haddad et al., 2008). In fact, all but one event were recorded between December and February, coinciding with the rainy season (Sick et al. 1987). Furthermore, only one of the events involved an adult female (L. troglodytes), which is consistent with the preference of predators for calling males (Pough et al. 1992; Toledo, 2003). This is the second study to report the predation of adult Phyllomedusa tree frogs by L. annulata. Nascimento et al. (2013) recorded the predation of three phyllomedusine species (Phyllomedusa vaillanti, Phyllomedusa tomopterna, and Phyllomedusa tetraploidea) in Brazil, Peru, and Ecuador. These records reinforce the conclusion that the toxins secreted by these anurans are insufficient to protect them from predation by L. annulata, although the exact mechanism through which the snake counteracts this chemical defense is unknown. While L. annulata is known to prey on a wide range of anuran species (Nascimento et al., 2013), only R. granulosa had been previously recorded in its diet (Vitt, 1996; Ávila and Morais, 2007). This reinforces the importance of our results, given that the impact of predation by this snake on anuran communities is poorly known, as for other predators (Toledo, 2005). Acknowledgements. We thank CEMAVE (Kleber Oliveira and Antônio E. 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