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Herpetology Notes, volume 13: 863-865 (2020) (published online on 16 October 2020)

New defensive behaviour for neuwiedii Günther, 1863 (, Dipsadidae) in a fragment of Atlantic Forest

Mariana Pedrozo¹, Matheus de Toledo Moroti¹, and Edélcio Muscat¹,*

Knowledge about anti-predatory strategies for space, and sometimes shows a triangular occipital spot different is increasing continuously with (Günther, 1863). Recent fieldwork has provided an the descriptions of new defensive behaviours over the opportunity to observe previously unknown aspects of years (e.g. Alves et al., 2013; Fiorillo et al., 2019; Assis the natural history of X. neuwiedii. Thus, the objective et al., 2020). The varied anti-predatory strategies present of this study is to describe a new defensive behaviour in this group, such as aposematism, cryptic colouration, for Xenodon neuwiedii, in a fragment of Atlantic Forest mimicry, head triangulation, and biting (Pough et in the Mantiqueira Mountains in south-eastern . al., 2004) are directly associated with survivorship On 19 April 2020 at 4:00 p.m. we found an adult (Lima and Dill, 1990; Guimarães and Sawaya, 2011; individual of Xenodon neuwiedii moving in a grassy area Dell’Aglio et al., 2012). (Fig. 1A) of the Projeto Dacnis private reserve in the São Cryptic colouration is a good example of primary Francisco Xavier sub-district, municipality of São José strategy (independent on the predator’s presence) to dos Campos, São Paulo state, Brazil (-22.889194°N, avoid being detected by visually-oriented predators -45.937500°E, WGS 84). When we approached it, it Edmunds (1974), while head triangulation and biting started to perform a display by elevating the tail: it was are important secondary strategies (triggered by the tightly coiled and only showing its dorsal surface (Fig. predator’s presence) to intimidate the predator and, 1B). The snake swung it from side to side before trying thus, avoid . Some primary anti-predatory to escape. When manipulated, it started to press the tail strategies, like polymorphism and mimicry are known spine against the researcher’s arm (E. Muscat), causing to some Bothrops Wagler, 1824 and Micrurus Wagler, a little discomfort but not breaking the skin. The spine- 1824 species, and secondary defences, like biting press happened quickly, making it impracticable for us and false strikes, are well documented for the to make a visual record of the behaviour. We filmed the Xenodon Boie, 1827 (e.g. Lavilla et al., 1979; Dirksen tail display and deposited it in Fonoteca Neotropical and Duarte, 1998; Martins et al., 2008; Mesquita et al., Jacques Vielliard (ZUEC-VID 795, also available on the 2013). YouTube platform (https://youtu.be/yjToAdyE6dM). Xenodon neuwiedii belongs to the Dipsadidae family Body compression or depression, head elevation (Costa and Bérnils, 2018) and is widely distributed in or triangulation are examples of behaviours that are (Nogueira et al., 2019). The species reported for X. neuwiedii (see Table 1) and are considered is terrestrial, with diurnal habits, usually associated common in phylogenetically related species (Martins et with open areas in forests, disturbed environments, al., 2008; Tozetti et al., 2009; Alves et al., 2013). Those and forest edges (Nogueira et al., 2019). This species behaviours can be considered warning displays (Sazima, has a greenish or brownish olive colouration, with 1992). They create an illusion of a larger body size brown cross bands on the trunk, snout and interorbital (Tozetti et al., 2009), which may discourage predators from striking at the snake. The tail display mimics the head and aims to misdirect predators’ attacks while the real head searches for refuge (Greene, 1973). The spine- pressing behaviour, performed by X. neuwiedii, is widely ¹ Projeto Dacnis, Estrada do Rio Escuro 4754, Sertão das known for Scolecophids, but also for some Dipsadids, Cotias, Ubatuba, São Paulo, Brazil. e.g. Atractus trilineatus Wagler, 1828 in Beebe (1946); * Corresponding author. E-mail: [email protected] Taeniophallus brevirostris (Peters, 1863) in Martins and 864 Mariana Pedrozo et al.

Figure 1. (A) Individual of Xenodon neuwiedii recorded in the São Francisco Xavier sub-district, São José dos Campos, São Paulo state, Brazil, (B) tail display in detail.

Oliveira (1998); Psomophis joberti (Sauvage, 1884) in species of the genera Bothrops and Micrurus, due to Lima et al. (2010) and may be related to an attempt to visual similarity and some defensive displays (e.g. head cause injuries to the predator. Nevertheless, we found triangulation, false strikes, and tail display — exhibiting not reports on this behaviour for Xenodon species. red ventral scales; Yanosky and Chani, 1988; Sazima Within the genus Xenodon, tail display is known for and Abe, 1991; Sawaya et al., 2008). Although mimicry X. dorbignyi (Bibron, 1854), X. histricus (Jan, 1863), hypotheses are largely cited in literature (e.g. Tozetti et X. nattereri (Steindachner, 1867), X. matogrossensis al., 2009; Oliveira et al., 2010; Alves et al., 2013; Banci (Scrocchi and Cruz, 1993), X. guentheri Boulenger, et al., 2020), being mostly accepted, further studies are 1894 and X. merremii (Wagler, 1824) (Tozetti et al., needed to provide compelling evidence these similarities 2009; Alves et al., 2013; Marques et al., 2015, 2019; enhance mimic’s survivorship (Banci et al., 2020). Abegg et al., 2018). Species of Xenodon have also been Furthermore, we cannot reject the role of evolutionary reported as mimicry to some sympatric and syntopic factors in the selection of ’ defensive repertoire (Greene, 1988), considering these similarities might represent behavioural convergences. Thus, studies that document behaviours are important to fill in the gaps Table 1. Types of defensive behaviour reported for Xenodon in the knowledge of species’ natural history, as well as neuwiediiTable. 1. Types of defensive behaviour reported for Xenodonproviding neuwiedii data for. future studies.

Defensive behaviour Xenodon neuwiedii Acknowledgements. We thank Projeto Dacnis for institutional support and Elsie Laura Rotenberg for the English revision. We Body depression Martins et al., 2008 also thank the editorial team and the reviewers that helped us Body inflation Martins et al., 2008 improve the quality of the manuscript. Crypsis Martins et al., 2008 References Head triangulation Martins et al., 2008 Abegg, A.D., Ceron, K., Lhanos, F.H. (2018): Xenodon Head elevation Martins et al., 2008 guentheri (Günther’s False Fer-de-lance). Defensive behavior. Mimicry Martins et al., 2008 Herpetological Review 49: 141–142. Alves, S. da S., Bolzan, M.R, Santos, T.G. do, Gressler, D.T., Neck S-coil Martins et al., 2008 Cechin, S.Z. (2013): Rediscovery, distribution extension Polymorphism Martins et al., 2008 and defensive behaviour of Xenodon histricus (Squamata: Serpentes) in the state of Rio Grande do Sul, Brazil. Salamandra Tail display Present study 49: 219–222. Spine-press Present study Assis, C.L. de, Guedes, J.J.M., Jesus, L.M.G., Feio, R.N. (2020): New defensive behaviour of the false Oxyrhopus

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rhombifer Duméril, Bibron & Duméril, 1854 (Serpentes, de Caatinga no nordeste brasileiro. Papéis Avulsos de Zoologia Dipsadidae) in south-eastern Brazil. Neotropical Biology and 53: 99–113. Conservation 15: 71–76. Nogueira C.C., Argôlo A.J.S., Arzamendia V., Azevedo J.A., Beebe, W. (1946): Field notes on the snakes of Kartabo, British Barbo F.E., Bérnils R.S., et al. (2019): Atlas of Brazilian snakes: Guiana, and Caripito, . Zoologica 31: 11–52. verified point-locality maps to mitigate the Wallacean shortfall Banci, K.R.S., Eterovic, A., Marinho, P.S., Marques, O.A.V. in a megadiverse snake fauna. South American Journal of (2020): Being a bright snake: testing aposematism and mimicry 14: 1–274. in a neotropical forest. Biotropica 1–13. Oliveira, T.O., Machado, F.C., Costa, H.C. (2010): Exchanging Costa, H.C., Bérnils, R.S. (2018): Répteis do Brasil e suas Unidades carrion for fresh meat: the vulture Cathartes burrovianus (Aves, Federativas: lista de espécies. Herpetologia Brasileira 7: 11–57. Cathartidae) preys on the snake (Serpentes, Dell’Aglio, D.D., Toma, T.S.P., Muelbert, A.E., Sacco, A.G., Dipsadidae) in southeastern Brazil. Biotemas 23: 177–180. Tozetti, A.M. (2012): Head triangulation as anti-predatory Pough, F.H., Andrews, R.M., Cadle, J.E., Crump, M.L., Savitsky, mechanism in snakes. Biota Neotropica 12: 315–318. A.H., Wells, K.D. (2004): Herpetology. Pearson Prentice Hall, Dirksen, L., Duarte, M.R. (1998): Polymorphismus in Waglerophis Upper Saddle River, New Jersey. merremii (Wagler, 1824) mit 1 Abbildung von M. R. Duarte. Sawaya, R.J., Augusto, O., Marques, V., Martins, M. (2008): Herpetofauna 20: 115–120. Composition and natural history of a Cerrado snake assemblage Edmunds, M. (1974): Defence in : a survey of anti-predator at Itirapina, São Paulo state, southeastern Brazil. Biota defences. New York: Longman. Neotropica 8: 127–149. Fiorillo, B.F., Rossi, G.N., Martins, M. (2019): Additional Sazima, I. (1992): Natural history of the jararaca pitviper, Bothrops defensive behaviours of Dipsas mikanii (Schlegel, 1837) and jararaca, in Southeastern Brazil. Campbell, J.A., Brodie Jr, E.D. Taeniophallus occipitalis (Jan, 1863) (Serpentes: Dipsadidae). (Eds) Biology of the Pitvipers. Texas, Selva Tyler. pp. 199–216. Herpetology Notes 12: 359–362. Sazima, I., Abe, A.S. (1991): Studies on Neotropical fauna and Greene, H.W. (1973): Defensive tail display by Snakes and environment habits of five Brazilian snakes with coral-snake Amphisbaenians. Society for the Study of Amphibians and pattern, including a summary of defensive tactics. Studies on 7: 143–161. Neotropical Fauna and Environment 26: 159–164. Greene, H.W. (1988): Antipredator mechanisms in reptiles. In Tozetti, A.M., Oliveira, R.B., Pontes, G.M.F. (2009): Defensive Biology of the Reptilia. Alan R. Liss, New York, 16: 1–152. repertoire of Xenodon dorbignyi (Serpentes, Dipsadidae). Biota Guimarães, M., Sawaya, R.J. (2011): Pretending to be venomous: is Neotropica 9: 157–163. a snake’s head shape a trustworthy signal to a predator? Journal Yanosky, A.A., Chani, J.M. (1988): Possible dual mimicry of of Tropical Ecology 27: 437–439. Bothrops and Micrurus by the Colubrid, dorbignyi. Günther, A. (1863): XXXV- Third account of new species of snakes Society for the Study of Amphibians and Reptiles 22: 222–224. in the collection of the British Museum. Annals and Magazine of Natural History 12: 348–365. Lavilla, E.O., Scrocchi, G.J., Terán, E.M.T. (1979): Sobre algunos aspectos del comportamiento en cautiverio de Xenodon merremii (Wagler) (Ophidia: ). Acta Zoológica Lilloana 35: 289–293 Lima, S.L., Dill, L.M. (1990): Behavioral decisions made under the risk of predation: a review and prospectus. Canadian Journal of Zoology 68: 619–640. Lima, D.C., Borges-Nojosa, D.M., Borges-Leite, M.J., Passos, D.C. (2010): Psomophis joberti (sand snake) defensive behavior. Herpetological Review 41: 96–97. Marques, O.A.V., Eterovic, A., Nogueira, C.C., Sazima, I. (2015): Serpentes do Cerrado: guia ilustrado. First edition. Ribeirão Preto, São Paulo, Brazil, Holos Editora. Marques, O.A.V., Eterovic, A., Sazima, I. (2019): Serpentes da Mata Atlântica: guia ilustrado para as florestas costeiras do Brasil. Second edition. Cotia, São Paulo, Brazil, Ponto A Editora. Martins, M., Oliveira, M.E. (1998): Natural history of snakes in forests of the Manaus region, Central Amazonia, Brazil. Herpetological Natural History 6: 78–150. Martins, M., Marques, O.A.V., Sazima, I. (2008): How to be arboreal and diurnal and still stay alive: microhabitat use, time of activity, and defense in Neotropical forest snakes. South American Journal of Herpetology 3: 58–67. Accepted by Rodrigo Gonzalez Mesquita, P.C., Passos, D.C., Borges-Nojosa, D.M., Cechin, S.Z. (2013): Ecologia e história natural das serpentes de uma área