Herpetology Notes, volume 13: 283-289 (2020) (published online on 27 March 2020)

Two new records of predation by fulgidus (: ) in the northern region of

Lucas de Souza Almeida1,*, Antonio Waldeir Oliveira da Silva2, and Vivian C. Trevine3

Oxybelis Wagler, 1830 is a monophyletic of such as frogs, , birds and even small mammals Neotropical Colubridae (Montingelli et al., 2019) (Köhler, 2008). Despite this large range of prey groups, represented by four , O. aeneus (Wagler, 1824), O. fulgidus diet consists primarily of birds and lizards O. fulgidus (Daudin, 1803), O. brevirostris (Cope, (Scartozzoni et al., 2009). In the present work, we 1861), and O. wilsoni Villa and Mccranie, 1995, the first report two new predatory interactions. The first one two occurring in Brazil (Wallach et al., 2014). All of involving O. fulgidus and Cnemidophorus cryptus Cole them share diagnostic morphological characters, such as and Dessauer, 1993 (Whiptal ) and the second one the evident elongated snout, large eyes, binocular vision O. fulgidus and Forpus xanthopterygius (Spix, 1824) and slender body (Henderson and Binder, 1980). Their (Blue-winged parrotlet), three species that occur in the life habitats are very similar: species of this genus are North region of Brazil. We also provide a brief review predominantly arboreal, spending most of their time of O. fulgidus diet. in trees or shrubs, with diurnal habits and ambushing The first observation occurred on June 11, 2018 at forage strategy (Henderson, 1982; Shine et al., 1996). 13:06 in a farm, in the municipality of Primavera, Pará, (green vine ) is a large tree snake north region of Brazil (-0.981111, -47.144166, WGS- distributed from northern to 84). This area is a private property consisting of an (Peters and Orejas-Miranda, 1970; Wallach et al., open area with degraded vegetation, where the intent 2014). According to Martins and Oliveira (1998), these is to create an area of agroforestry. Some alien species are more associated with forest environments of plants are common, like Mangifera indica Linnaeus, and, even though arboreal, they can occasionally move 1753 and Urochloa decumbens (Stapf, 1919), but also on the ground when active (Martins and Oliveira, 1998). native species are present, such as Byrsonima crassifolia Like other oviparous species, O. fulgidus females are (Linnaeus, 1753) and Chrysobalanus icaco Linnaeus, larger in snout-vent length and heavier than males 1753. It is common to observe wandering at (Henderson, 1982; Scartozzoni et al., 2009), and an the farm, which also neighbours a preserved forest adult female can reach up to 2063 mm of total length fragment. (Beebe, 1946). Its size and opisthoglyphous fangs, used During our observation, we found two individuals of to subdue their prey, allow this species to consume larger C. cryptus walking and thermoregulating on the ground. and more diversified preys (Scartozzoni et al., 2009), The whiptail lizards were getting closer to a shrub of C. icaco. An adult specimen of O. fulgidus was pendant in that shrub, about 40 cm above the ground. The posterior portion of the snake’s body was suspended in a branch and the other half was on the ground, when O. fulgidus attacked one of the lizards. After capturing the lizard 1 Universidade Estadual Paulista “Júlio de Mesquita Filho”, with a massive strike, the snake grasped the lizard’s Departamento de Biodiversidade, Instituto de Biociências, body, making two loops with it is own body while 13506-900, Rio Claro, Brazil. holding up the prey in its mouth (Fig. 1). The lizard 2 Rua Professor Firmino, 262, Centro, 68707-000, Primavera, showed some resistance for about 9min after being bitten Pará, Brazil. and moved its limbs and tail, attracting the attention of 3 Laboratório Especial de Coleções Zoológicas, Instituto Butantan, Av. Vital Brasil, 1500, 05503-900, São Paulo, São a domestic chicken (Gallus gallus Linnaeus, 1758). Paulo, Brazil. When the chicken got closer to the snake, it responded * Corresponding author. E-mail: [email protected] undoing the loops around the lizard’s body and carrying 284 Lucas de Souza Almeida et al.

Figure 1. Documentation of the predation event between Oxybelis fulgidus and Cnemidophorus cryptus. A: Detail of O. fulgidus holding the whiptail lizard (C. cryptus) with its rear fangs. At this point the prey showed some resistance and movement of its limbs; B: A second individual of C. cryptus, which escaped the snake strike and fled into a burrow in the sandy soil; C: The position of O. fulgidus and its prey in the shrub (red circle); D: Oxybelis fulgidus holding C. cryptus, which presented no more muscular responses after 14 minutes of observation.

it 55cm higher of the initial point in the shrub. We were et al., 2012). This species is composed by unisexual able to see the snake moving its jaws and pressing the diploid and geographic discontinuous populations, lizard repeatedly, which may indicate contractions and all individuals are females, due to parthenogenetic in the region of the Duvernoy’s glands triggered by reproduction (Cole and Dessauer, 1993). The adductor muscles (Johnston, 2014). After 14min of discontinuous populations classified as C. cryptus occur observation, the whiptail lizard did not demonstrate any in , and Brazil (Cole and Dessauer, signs of reaction, presumably paralyzed by the effects 1993; Ribeiro-Júnior and Amaral, 2016). Brazilian of the snake’s venom (Fig. 1D). The green vine snake populations are distributed in eastern Amazonia, in the started to handle the lizard, swallowing head first, while states of Amazonas, Rondônia, Amapá, Maranhão and still suspended above ground. The whole observation Pará (Ribeiro-Júnior and Amaral, 2016). Cnemidophorus lasted about 32min. At the end of the predatory event, cryptus are terrestrial and diurnal , dwelling on O. fulgidus came down of the shrub and got away. We open vegetation with sandy soil (Mesquita and Colli, maintained a distance of 4 m from the interaction at all 2003), as observed in this study. times, aiming not to interrupt or disturb the animals. The second observation was made on May 16, 2019 at Cnemidophorus cryptus is a lizard from the C. 12:39 in a secondary forest fragment, in an urban area lemniscatus complex (Markezich et al., 1997; Harvey of Manaus, Amazonas, Brazil (-3.016944, -60.023055, Two new records of predation by Oxybelis fulgidus in the northern region of Brazil 285

Figure 2. Sequential photos of the predation event on Forpus xanthopterygius by Oxybelis fulgidus. A: F. xanthopterygius trying to defend itself from O. fulgidus grasp, while the snake holds the bird; B: O. fulgidus starting to handle the prey moving its jaws and going for the head; C: O. fulgidus using a thicker branch to elevate the bird; D: O. fulgidus finally engulfs F. xanthopterygius. (Photos by: Clodoaldo Costa Junior)

WGS-84). On the border of the fragment, an individual 2C). Finally, after 51min of observation, O. fulgidus of O. fulgidus was spotted with a male of Forpus was able to fully ingest the prey (Fig. 2D). xanthopterygius (blue-winged parrotlet) in its mouth. The blue-winged parrotlet is the smallest Psittacidae Both animals were found on a branch around 1.8 m that occurs in Brazil (Cubas et al., 2014), and a common above the ground. At first, the Blue-winged parrotlet species, distributed from the Amazon basin to northern did some agonistic vocalizations, and was trying to Argentina (Bocalini and Silveira, 2015). These birds use its feet to push the snake away, while it grabbed may exhibit gregarious behaviour, foraging alone or the parrotlet’s neck (Fig. 2A). After 7min containing in groups with up to ten individuals (Sazima, 2008). In the prey, the Green vine snake overcame the parrotlet’s our observations, this F. xanthopterygius was foraging resistance, and it stopped moving. The snake began to alone. This was the first predation record of a Psittacidae handle and swallow the motionless bird headfirst (Fig. by O. fulgidus. 2B). About 22min passed before the snake swallowed Several studies have documented the green vine snake the bird’s head. While O. fulgidus was handling F. dietary preference, as shown in Table 1. The majority xanthopterygius, it retracted part of its body upwards of O. fulgidus prey items reported in the literature are to a thicker branch, getting a better support and a diurnal and terrestrial, such as the lizards Ameiva ameiva, horizontal position in relation to the ground, which festivus, Manciola guaporicola, Tropidurus apparently facilitated the consumption of the bird (Fig. oreadicus (Faria and Araujo, 2004; Scartozzoni et al., 286 Lucas de Souza Almeida et al.

Table 1. List of prey items documented for Oxybelis fulgidus in the literature, ordered by year of publication. Table 1. List of prey items documented for Oxybelis fulgidus in the literature, ordered by year of publication.

Prey items References Birds Unidentified bird Beebe (1946); Martins and Oliveira (1988); Scartozzoni et al., (2009) Unidentified Passeriforme Henderson & Binder (1980); Henderson (1982); Scartozzoni (2009) Spinus notata (Du Bus de Gisignies, 1847) Stuart (1948) Parulidae Wetmore et al., 1947 Henderson and Binder (1980); Henderson (1982) Volatina jacarina (Linnaeus, 1766) Nascimento et al., (1988) Tangara episcopus (Linnaeus, 1766) Martins and Oliveira (1998) Pipra sp. Linnaeus, 1764 Martins and Oliveira (1998) Rufirallus viridis (Müller, 1776) Bringsøe (2002) Tyrannus melancholicus satrapa (Cabani and Heine, 1860) Hayes (2002) Dendrocincla homochroa (Sclater, 1860) Leenders and Colwell (2003) Elaenia sp. Sundevall, 1836 Rodrigues et al., (2005) Monasa nigrifrons (Spix, 1824) Endo et al. (2007) Tyrannidae Vigors, 1825 Scartozzoni et al., (2009) Bucconidae Horsfield, 1821 Scartozzoni et al., (2009) Muscicapidae Fleming, 1822 Scartozzoni et al., (2009) Amazilia tzacalt (De la Llave, 1833) Van Dort (2011) Turdus grayi Bonaparte, 1838 Figueroa and Valerio, (2011) Sturnella militaris (Linnaeus, 1758) Capurucho and Costa (2012) Columbina passerina (Linnaeus, 1758) Fraga et al., (2012) Columbina squammata (Lesson, 1831) Miranda et al., (2013) Turdus leucomelas Rafinesque, 1815 Viana et al., (2014) Pitangus sulphuratus (Linnaeus, 1766) Viana et al., (2014) Troglodytes aedon Vieillot, 1809 Sosa-Bartuano and Rodríguez-Beitía (2015) Xiphorhynchus flavigaster Swainson, 1827 Díaz-Gamboa (2017) Eumomota superciliosus (Sandbach, 1837) Cherry-Jr et al., (2017) Chelidoptera tenebrosa (Pallas, 1782) Gama et al., (2018) Ramphocelus carbo (Pallas, 1764) May et al., (2018); Hernández-Ruz (2019) Paroaria nigrogensis (Lafresnaye, 1846) Sánchez-Ojeda and Cortés-Suárez (2019) Catharus occidentalis Sclater, 1859 Rodríguez-Pérez and Mata-Silva (2019) Forpus xanthopterygius (Spix, 1824) This study Lizards Unidentified lizard Beebe (1946); Henderson and Binder (1980); Henderson (1982); Martins and Oliveira (1998); Scartozzoni et al., (2009) Norops chrysolepis (Duméril and Bibron, 1837) Beebe (1946) Basiliscus vittatus Wiegmann, 1828 Henderson and Binder (1980); Henderson (1982) Ctenosaura similis (Gray, 1831) Henderson and Binder (1980); Henderson (1982) Sceloropus chrysostictus Cope, 1866 Henderson and Binder (1980); Henderson (1982) Anolis sp. Sparrman, 1784 Henderson and Binder (1980); Henderson (1982); Bernarde and Abe (2010) (Wiegmann, 1834) Henderson and Binder (1980); Henderson (1982) Ameiva ameiva (Linnaeus, 1758) Nascimento et al., (1988) Holcosus festivus (Lichtenstein and Martens, 1856) Norris and Burtt-Jr (1998) Ameiva sp. Linnaeus, 1758 Martins and Oliveira (1998) Polychrus marmoratus (Linnaeus, 1758) Scartozzoni et al., (2009) Norops ortonii (Cope, 1868) Scartozzoni et al., (2009)

Two new records of predation by Oxybelis fulgidus in the northern region of Brazil 287

Table 1. Continued.

Prey items References Tropidurus oreadicus Rodrigues, 1987 Scartozzoni et al., (2009) Manciola guaporicola (Dunn, 1935) Scartozzoni et al., (2009) Tropiduridae Bell, 1843 Scartozzoni et al., (2009) Hemidactylus mabouia (Moreau de Jonnès, 1818) Santos-Jr et al., (2011) Iguana iguana (Linnaeus, 1758) Costa-Campos et al., (2014) Cnemidophorus cryptus Cole and Dessauer, 1993 This study

2009; Ribeiro-Júnior and Amaral, 2016) and C. cryptus. were observed immobilizing a lizard after 14 min and To reach and strike terrestrial lizards, the green vine snake a parrotlet within 7 min of manipulation. Moreover, could chase them on the ground or behave as reported in there are few cases of human accidents with this this study, which was also registered by Norris and Burtt opisthoglyphous genus. Silva et al. (2019) described a (1998). Both studies have demonstrated that O. fulgidus symptomatic envenomation with an O. fulgidus from strikes its terrestrial targets while perching partially Pará, Brazil, with symptoms such as tachycardia, suspended on low branches of trees. Although classified dizziness, local bleeding, moderate pain with erythema, as mainly living on rocks or open areas, where they local oedema and ecchymosis. bask at the hottest hours of the day, T. oreadicus and A. This study is the first record of predation by O. fulgidus ameiva can be found in some perches or on fallen tree on the genus Cnemidophorus, as well as on a Psittacidae trunks, above the ground (Meira et al., 2007; Ribeiro- bird, aggregating more information on this species Júnior and Amaral, 2016). In that situation, it is possible behaviour in natural conditions. It is crucial that further that the green vine snake gets those preys without studies continue to point out the importance of studying descending to the floor. However, the record presented the natural history of Neotropical fauna, especially for by Miranda et al. (2013), where O. fulgidus preyed a species that can represent new sources of information on Columbina squammata, a bird that often forages on the new pharmacological compounds, such as Colubridae ground (Sick, 1997), was completely observed on the and Dipsadidae snakes. Additional studies are needed ground. Smith et al. (2018) observed a predation on to elucidate the hunting strategies and behaviour of the Holcosus undulatus and they mention that the green green vine snake. vine snake descended completely to the ground during the seizure. Therefore, those interactions with terrestrial Acknowledgments. We are thankful to Clodoaldo Costa Junior for providing us with those records of predation on Forpus species show some plasticity of O. fulgidus foraging xanthopterygius by Oxybelis fulgidus. We are grateful to Gabriele habitats, as reported by Martins and Oliveira (1998). Santana de Farias for English revision and Paula Eveline Ribeiro The green vine possesses a three-finger Anunciação for manuscript revision, and for providing valuable toxin (3FTx), a protein group commonly found in comments. We are thankful to Marcelia Basto da Silva for snake’s venom (Hedge et al., 2010). That toxin was confirming the identification of Cnemidophorus cryptus. isolated from O. fulgidus venom, and described as fulgimotoxin, a potent compound that may be lethal References to lizards. Furthermore, other 3FTx proteins such as Beebe, W. (1946): Field notes on the snakes of Kartabo, British denmotoxin, which is responsible for the toxicity to birds, Guiana, and Caripito, Venezuela. Zoologica 31(1): 11–52. were also recorded in this snake venom (Heyborne and Bernarde, P.S., Abe, A.S. (2010): Hábitos alimentares de serpentes Mackessy, 2013). These authors clarified the biological em Espigão do Oeste, Rondônia, Brasil. Biota Neotropica 10(1): role of fulgimotoxin, evidencing a neurotoxin structural 167–173. conformation, allowing the predator to intervene on Bocalini, F., Silveira, L.F. (2015): Morphological variability and of the Blue-winged parrtolet Forpus xanthopterygius the lizard’s ion channel blocking (Hedge et al., 2010; (Psittacidae). Revista Brasileira de Ornitologia 23(1): 64–75. Heyborne and Mackessy, 2013). These findings can Bringsøe, H. (2002): Herpetology in 5. Green explain the observations made in the field, including vine snake, Oxybelis fulgidus, feeding on water rail. Nordisk the ones reported in this study, where two O. fulgidus Herpetologisk Forening 45: 95–96. 288 Lucas de Souza Almeida et al.

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Accepted by Mirco Solé