Herpetology Notes, volume 11: 839-841 (2018) (published online on 28 September 2018)

A new defensive behaviour for threadsnakes and the defensive repertoire of Trilepida jani (Pinto & Fernandes, 2012) (Epictinae: Leptotyphlopidae)

Angele Martins1, Gabriel M. Baptista1,2, Daniel B. Maciel1, and Rodrigo C. Gonzalez1,*

Snakes exhibit a series of defensive behaviours Trilepida jani (Pinto and Fernandes, 2012) is apparently dependant on exposure to different kinds of predators strictly fossorial (as for most leptotyphlopids), and may in the various habitats they occupy (Greene, 1988). be found in cavities under stones (Pinto and Fernandes, Antipredator mechanisms among snakes are diverse 2012). It constructs tunnels and eventually leaves these and complex, and several studies addressing defensive habitats when tunnels are flooded by intense rain (Pinto behaviour are available for neotropical snakes (e.g., and Fernandes, 2012). On 23 August 2014, during Greene, 1988; Martins, 1996; Martins et al., 2008). fieldwork in the Brazilian Cerrado in the municipality However, most studies address alethinophidian of Grão Mogol (16°33’37.9”S 42°51’03.6”W), Minas snakes, with relatively few contributions pertaining to Gerais, Brazil, an individual of T. jani (MNRJ 25148; scolecophidians (e.g., Visser, 1966; Gehlbach et al., Fig. 1) exhibited an interesting defensive repertoire 1968; Watkins II et al., 1969; Gehlbach, 1970; Webb and while being photographed. Shine, 1993; Martins, 1996; Ernst and Ernst, 2003). First, the individual showed locomotor escape Scolecophidians (sensu Vidal et al., 2010) are (Figure 1A) and balling behaviour. When manipulated, specialised burrowers that actively prey on larvae or the animal exhibited a previously undescribed adults of social insects (Greene 1997; Cundall and defensive behaviour. The snake coiled itself around Greene, 2000; Webb et al., 2000). Defensive behaviours the researcher’s finger, passing its head several times exhibited by scolecophidians include death-feigning around its body coils, and squeezing with a relatively and erratic movements, defecation, writhing, cloacal sac high amount of force. The knotting behaviour resembled discharge, silvery colouration, and vigorous semirigid an open double overhand knot (Figure 1B). In addition, serpentine behaviours (Richmond, 1955; Visser, 1966; this reaction was repeated every time the animal was Gehlbach et al., 1968; Watkins II et al., 1969; Gehlbach, manipulated. This behaviour was shortly followed by 1970). Most of these previously reported behaviours are cloacal discharge (presumably from the anal gland, with based on observations of only a few scolecophidian an intense odour) and prodding with the tail spine while species, with even fewer observations for species coiled around the manipulator’s finger. from the family Leptotyphlopidae. Knowledge of Except for this new behaviour (coiling with a double leptotyphlopid biology is still incipient (Avila et al., overhand knot), similar defensive behaviours have 2006) and warrants further investigation. already been reported for other leptotyphlopids (e.g., Rena dulcis in Watkins II et al., 1969; Rena humilis in Ernst and Ernst, 2003; Leptotyphlops scutifrons in Gehlbach et al., 1968; Epictia diaplocia in Martins, 1996). However, this is the first report of a defensive behaviour for Trilepida spp. 1 Departamento de Vertebrados, Museu Nacional, Universidade Additionally, most of the available studies on defensive Federal do Rio de Janeiro, Quinta da Boa Vista, São behaviours for leptotyphlopids are based on ant attacks Cristóvão, 20940-040, Rio de Janeiro, RJ, Brazil. 2 Universidade Estácio de Sá, Campus R9, Rua André Rocha, stimulated in captivity (Gehlbach et al.,1968; Shine 838. Taquara, 22710-560, Rio de Janeiro, RJ, Brazil. and Webb, 1990). Amongst the defensive behaviours * Corresponding author. E-mail: [email protected] exhibited by leptotyphlopids, discharge of cloacal 840 Angele Martins et al.

Figure 1. Defensive behaviour of Trilepida jani (MNRJ 25148) exhibiting erratic movements (A) and knotting behaviour, associated with prodding with the caudal spine (B). Photo by Daniel B. Maciel.

secretions is apparently used for minimising the risks of for the PostDoc fellowship provided (E-26/202.403/2017). ���� ant attacks (prey-inflicted injuries; Gehlbach et al.,1968; (processes: 142370/2014-2) and DBM thank CNPq and CAPES Shine and Webb, 1990). Olfactory cues may stimulate for the scholarships offered during PhD. erratic behaviour in other leptotyphlopids (Watkins II et al., 1969) rather than purely tactic or visual stimulation. References In this study, defensive behaviours were exhibited after Avila, R.W., Ferreira, V.L., Souza, V.B. (2006): Biology of manipulation (i.e., tactile stimulation). the blindsnake Typhlops brongersmianus (Typhlopidae) in The interpretation of the “double overhand knot” a semideciduous forest from central Brazil. Herpetological behaviour is still merely speculative and lacks Journal 16: 403–405. Cundall, D., Greene, H.W. (2000): Feeding in snakes. In: Schwenk observations in the presence of predators. However, it K. (ed.) Feeding, Form, Function, and Evolution in Tetrapod may be a protection against falls, or a way to cling to Vertebrates, p. 293–333. San Diego. some substrate to avoid being removed from a particular Durso, A. M.; Mullin, S.J. (2014): Intrinsic and Extrinsic Factors place by a predator. Additionally, the knotting behaviour Influence Expression of Defensive Behavior in Plains Hog- may prevent predators from being able to easily consume Nosed Snakes (Heterodon nasicus). Ethology, 120: 140–148. these blindsnakes as prey, especially if the spine is Ernst, C.H.,;Ernst, E.M. (2003): Snakes if the United States and pressed into sensitive areas, such as the eye. Canada. Washington DC: Smithsonian Books. Regarding the other behaviours exhibited by Trilepida Gehlbach, F.R., Watkins II, J.; Reno, H.W. (1968): Defensive behavior elicited by ant attacks. Bioscience 18: 784–785. jani mentioned above, those are widespread among Gehlbach, F.R. (1970): Death-feigning and erratic behavior in other scolecophidian snakes and terrestrial (mostly) Leptotyphlopid, Colubrid and Elapid Snakes. Herpetologica 26: alethinophidian species (Martins, 1996; Martins et al., 24–34. 2008). Despite its importance for survival, effects of Greene, H.W. (1988): Antipredator mechanisms in reptiles. In extrinsic and intrinsic factors on individual defensive Biology of the Reptilia, p. 1–152. Gans, C., Huey, R. B. (Eds)., behaviour have been neglected in most snakes and New York: Alan R. Liss, Inc. thus demand additional attention (Marques et al., 2013; Greene, H.W. (1997): Snakes: The Evolution of Mystery in Nature. Berkeley and Los Angeles, University of California Press. Durso and Mullin, 2014). This study contributes by Marques, O.A.V., Banci, K., Strussmann, C. (2013): Death- providing data on the biology of leptotyphlopid species, feigning behavior in water snakes of the genus Hydrodynastes and further studies on other species of Leptotyphlopidae (Dipsadidae) from South America. Herpetology Notes 6: 95– are recommended. 96. Martins, M. (1996): Defensive tactics in lizards and snakes: Acknowledgements. AM thanks: Coordenação de the potential contribution of the Neotropical fauna. Anais de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) for the Etologia 14: 185–199. scholarship provided during PhD, and Fundação Carlos Chagas Martins, M., Marques, O.A.V., Sazima, I. (2008): How to be Filho de Amparo à Pesquisa no Estado do Rio de Janeiro (FAPERJ) arboreal and diurnal and still stay alive: microhabitat use, time A new defensive behaviour for threadsnakes 841

of activity, and defense in Neotropical forest snakes. South Watkins II, J.F., Gehlbach, F.R., Kroll, J.C. (1969): Attractant- American Journal of Herpetology 3: 58–67. Repellent Secretions of Blind Snakes (Leptotyphlops dulcis) Pinto, R., Fernandes, R. (2012): A New Blind Snake Species of and their army ant prey (Neivamyrmex nigrescens). Ecology 50: the Genus Tricheilostoma from Espinhaço Range, Brazil and 1098–1102. Taxonomic Status of Rena dimidiata (Jan, 1861) (Serpentes: Webb, J.K., Shine, R. (1993): Prey-size selection, gape limitation Epictinae: Leptotyphlopidae). Copeia. 1: 37–38. and predator vulnerability in Australian blind snakes Richmond, N.D. (1955): The blind snakes (Typhlops) of Bimini, (Typhlopidae). Animal Behavior 45: 1117–1126. Bahama Islands, British West Indies, with description of new Webb, J.K., Shine, R., Branch, W.R., Harlow, P.S. (2000): Life- species. American Museum Novitates 1734: 1–7. history strategies in basal snakes: reproduction and dietary habits Shine, R.; Webb, J.K. (1990): Natural history of Australian of the African thread snake Leptotyphlops scutifrons (Serpentes: typhlopid snakes. Journal of Herpetology 24: 357 – 363. Leptotyphlopidae). Journal of Zoology 250: 321–327. Visser, J. (1966): Colour change in Leptotyphlops scutifrons (Peters) and notes on its defensive behavior. Zoologica Africana 2: 123–125. Vidal, N., Marin, J., Morini, M., Donnellan, S., Branch, W.R., Thomas, R., Vences, M., Wynn, A., Cruaud, C., Hedges, B. (2010): Blindsnake evolutionary tree reveals long history on Gondwana. Biology Letters 6: 558–561.

Accepted by Andrew Durso