New Records of Predation Interactions Between Birds and Amphisbaenians, and a Report of Bites by Amphisbaena Vermicularis Wagler, 1824 (Squamata: Amphisbaenidae)
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Herpetology Notes, volume 14: 1117-1122 (2021) (published online on 20 Aug 2021) New records of predation interactions between birds and amphisbaenians, and a report of bites by Amphisbaena vermicularis Wagler, 1824 (Squamata: Amphisbaenidae) Lucas de Souza Almeida1,* and Lucas Lima Bezerra2 Amphisbaenids are limbless reptiles with worm-like to display defensive tactics such as erratic movements, appearance, reduced eyes, and fossorial habits (Barros- fleeing, caudal luring, gaping the mouth, caudal autotomy, Filho et al., 2008). Their range covers the African and and biting (Greene, 1973; Navega-Gonçalves and Benites, American continents and, up to now, 182 species have 2019; Guedes et al., 2020). Here we present two records been described, of which 82 are reported to occur in of interactions between amphisbaenians and birds, one Brazil (Costa and Bérnils, 2018; Uetz et al., 2020). with a Roadside Hawk, Rupornis magnirostris (Gmelin, These animals are adapted for living most of their lives 1788), and another with a Rufous Hornero, Furnarius in underground galleries (Gans, 1978; Kearney and rufus (Gmelin, 1788). We also report a defensive Stuart, 2004; Bernarde, 2012; Vitt and Caldwell, 2013), behaviour for Amphisbaena vermicularis Wagler, 1824. using their heads with highly specialized and resistant The first interaction occurred on 30 September 2017 bones to excavate (Gans, 1978). Since they inhabit at 11:42 h, after a rainy morning, in a fragment of dense underground galleries, amphisbaenians are difficult to ombrophilous rainforest located in an urban area in the find and, therefore, their natural history,in situ behaviour, coastal city of Peruíbe, São Paulo State, southeastern predators, and prey are rarely documented (Gans, 1971; Brazil (24.3636°S, 47.0213°W; Datum WGS-84; Marques and Sazima, 1997; Filogonio et al., 2009). elevation 12 m). We observed a Roadside Hawk as Based on a molecular analysis, Mott and Vieites (2009) it grabbed an amphisbaenian, probably Leposternon synonymized all South American amphisbaenid genera microcephalum Wagler, 1824, with its claws. The with Amphisbaena, except for the genus Mesobaena. hawk then landed on a tree branch and repeatedly beat Although the work of Mott and Vieites (2009) was the amphisbaenian against the trunk of the tree. The important for a better understanding of the evolutionary hawk also stomped on the amphisbaenian and pecked history of this complex group, we here follow Ribeiro et at it three times. While pecking at its prey, the hawk al. (2011) in treating Leposternon as a valid genus. used abrupt movements of its wings and feet to try and Unlike fishes, birds, and mammals, reptiles were lacerate the amphisbaenian’s body. The amphisbaenian once considered behaviourally less complex animals merely writhed in response. As soon as the hawk ended (Brattstrom, 1974). However, we now know that reptiles the attacks, it looked around and repeated the pulling have a wide behavioural repertoire (Vitt and Caldwell, movements helped by its wings. The amphisbaenian 2013). Some of these behaviours may be induced by then lifted its anterior body portion (Fig. 1A), making the action of predators or the stress generated during it possible to discern its “shovel-shaped” head (Gans, predation events, and they can be more vigorous in 1971; Porto et al., 2000; Perez and Ribeiro, 2008). After cases of subjugation (Greene, 1973; Edmunds, 1974). that, the hawk flew off with the amphisbaenian in its When threatened by a predator, amphisbaenians are able claws. The interaction lasted about 35 s. The second interaction occurred on the campus of the Universidade Estadual Paulista, Rio Claro Municipality, São Paulo State, southeastern Brazil (22.3972°S, 1 Laboratório de Herpetologia, Departamento de Biodiversidade, Instituto de Biociências, Universidade Estadual Paulista ‘Júlio 47.5438°W; Datum WGS-84; elevation 611 m), on 13 de Mesquita Filho’, Rio Claro, São Paulo 13506-900, Brazil. November 2017 at 17:53 h, during a warm and sunny 2 Universidade Estadual do Ceará, Fortaleza, Ceará 60714-903, afternoon after hours of torrential rain. A Rufous Hornero Brazil. started a series of long and low flights before landing on * Corresponding author. E-mail: [email protected] dry leaves of fern and Cecropia hololeuca Miq. After © 2021 by Herpetology Notes. Open Access by CC BY-NC-ND 4.0. landing, the bird pecked four times at the same spot, and 1118 Lucas de Souza Almeida & Lucas Lima Bezerra Figure 1. (A) A Roadside Hawk, Rupornis magnirostris, subduing an amphisbaenian of the genus Leposternon (probably L. microcephalum) in Peruíbe Municipality, São Paulo State, southeastern Brazil. The yellow arrow indicates the head of the amphisbaenian. (B) Amphisbaena dubia dropped on the asphalt by Furnarius rufus in Rio Claro Municipality, São Paulo State, southeastern Brazil. on the last peck, it pulled an individual of Amphisbaena biological specimens found dead can be deposited in a dubia Müller, 1924 out of the ground by its posterior body scientific collection without the need for a collection portion. The hornero then flew a brief and low flight to permit. reposition itself next to the amphisbaenian, which tried to With regard to amphisbaenians, predation records by hide under the dry leaves. Quickly searching through the birds are the most common and were briefly reviewed leaves with two side movements of its beak, the hornero previously (Zamprogno and Sazima, 1993; Rajão et al., found the amphisbaenian, which showed no defensive 2013; Hayes et al., 2015). Hayes et al. (2015) included a behaviour. With two additional pecks, combined with Whistling Heron, Syrigma sibilatrix (Temminck, 1824), short and quick wing strokes, the hornero subjugated the on the list of amphisbaenians predators. Folly et al. (2015) amphisbaenian and kept it restrained using its beak. The published about a fortuitous predation event between a bird seemed to have difficulty keeping the amphisbaenian Red-legged Seriema, Cariama cristata (Linnaeus, 1766), in its beak, even though it writhed only very slowly. and Leposternon microcephalum. Smaniotto et al. (2017) With the amphisbaenian still in its beak, the hornero reported the interaction between a Guira Cuckoo, Guira flew a brief and low flight, moving to a location about guira (Gmelin, 1766), and Amphisbaena vermicularis in 3 m away from the observers. Suddenly, a Pale-breasted the state of Mato Grosso, central Brazil. Tanaka et al. Thrush, Turdus leucomelas Vieillot, 1818, arrived and (2019) published a short note reporting three events of attacked the hornero, which dropped the amphisbaenian. unidentified amphisbaenids being attacked by White- The hornero then picked up the amphisbaenian again necked Hawks, Amadonastur lacernulatus (Temminck, in its beak and carried it along the ground for 1 m. The 1827), an endemic and uncommon species occurring in hornero then released the still-moving amphisbaenian, the denser vegetation of the Brazilian Atlantic Forest. pecked at it twice, and succeeded in killing it. The hornero Recently, Nolasco et al. (2020) found a Burrowing tried to carry the amphisbaenian in its beak once more, Owl, Athene cunicularia (Molina, 1782), preying on an but the flight was low and, after 5 m, the amphisbaenian Amphisbaena vermicularis. Besides these birds, other fell onto the asphalt. The hornero then abandoned its vertebrates prey on amphisbaenians, including semi- prey. The observed interaction lasted for 2:23 min. The fossorial coralsnakes, genus Micrurus (Sazima and Abe, Amphisbaena dubia specimen (Fig. 1B) was a female 1991; Marques and Sazima, 1997; Gomes et al., 2005; with 210 mm snout–vent length (measured with a 1 mm Da Silva Banci et al., 2017), as well as the colubrids precision measuring tape) and was identified using the Apostolepis cearensis Gomes, 1915 (Silveira et al., 2014) information in Gans (1964), Vanzolini (2002), and Zaher and members of the genus Elapomorphus (Zamprogno et al. (2011). Unfortunately, we discarded the A. dubia and Sazima, 1993). Maschio et al. (2010) evaluated the because at that time, we were unaware that in Brazil dietary composition of Anilius scytale (Linnaeus, 1758), Predation Interactions Between Birds and Amphisbaenians 1119 and reported that this fossorial snake preys on several records and the occurrence of rain. All the interactions species of amphisbaenians, such as Amphisbaena described in this work occurred during the rain or one day anomala (Barbour, 1914), A. fuliginosa Linnaeus, 1758, after a rainy day. These data corroborate the observation A. mitchelli Procter, 1923, and Leposternon polystegum by Zamprogno and Sazima (1993) that amphisbaenians (Duméril, 1851). There is a curious record of predation probably go to the surface more frequently after rainy by Drymarchon corais (Boie, 1827) on Amphisbaena periods due to flooding of their tunnels, exposing alba Linnaeus, 1758 (Campos et al., 2010). There is themselves and becoming potential prey. also one record of attempted predation by the lizard Some amphisbaenians display defensive behaviours Ameiva ameiva (Linnaeus, 1758) (Ubaid et al., 2009). when facing predators or other kinds of threats (Greene, A Pepper Frog, Leptodactylus labyrinthicus (Spix, 1973). Some species, such as Amphisbaena alba and 1824), was found with an A. vermicularis in its stomach A. fuliginosa, perform defensive tail displays, possibly content (Vaz-Silva et al., 2003). After analyses of the as a distraction for potential predators (Beebe, 1945; stomach content of a dead Crab-eating Fox, Cerdocyon Gans, 1962; Greene, 1973; Zamprogno and Sazima, thous (Linnaeus, 1766), Zamprogno and Sazima (1993) 1993). Several species are able to autotomize their tails reported that this animal may prey on individuals of to escape from predators, as Vanzolini (1951) noticed Leposternon wuchereri (Peters, 1879). for A. fuliginosa and Zamprogno and Sazima (1993) The knowledge about the diet of birds of prey, as well reported for A. vermicularis and A. mertensii Strauch, as their foraging and hunting behaviours are incomplete 1881. Guedes et al. (2020) presented a review of A. (Panasci and Withacre, 2000). Birds of prey, such as vermicularis with autotomized tails. Other defensive R.