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Death-Feigning Behaviour (Thanatosis) in Chilean Green Racer, Philodryas Chamissonis (Wiegmann, 1835) (Serpentes: Dipsadidae)

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Death-Feigning Behaviour (Thanatosis) in Chilean Green Racer, Philodryas Chamissonis (Wiegmann, 1835) (Serpentes: Dipsadidae) Herpetology Notes, volume 13: 731-732 (2020) (published online on 25 August 2020) Death-feigning behaviour (thanatosis) in Chilean green racer, Philodryas chamissonis (Wiegmann, 1835) (Serpentes: Dipsadidae) Nicolás Zañartu1 and Félix A. Urra1,2,* Thanatosis is an anti-predatory behaviour that (Abegg et al., 2018), and P. viridissima (Marques, 1999; involves death-feigning (immobilisation reflex) as a Natera-Mumaw et al., 2008), which contrasts with the “last resort” by prey that have been detected or seized scarce information available for the species of trans- by a predator (Ushakov, 2007; Mendoza, 2009), thereby Andean group P. amaru, P. chamissonis, P. simonsii, presumably reducing the perceived need of the predator and P. tachymenoides (Zaher et al., 2014). to further subdue its prey or causing the predator to Philodryas chamissonis (Wiegmann, 1835) is a rear- cease paying attention (Humphreys and Ruxton, 2018). fanged snake endemic to Chile that preys on frogs, In snakes, death-feigning is influenced by body size, lizards, birds, and small mammals (Greene and Jaksic, sex, and temperature (Mutoh, 1983; Gerald, 2008; 1992; Torres, 2017; Riquelme and Catchpole, 2019). Gregory, 2008; Durso and Mullin, 2014). In fact, this Although it is one of the most common snake species behaviour may occur more frequently in snakes with in Chile, aspects of the composition of the venom (Urra small body sizes such as neonates or juveniles (Gerald, et al., 2015), human envenomation (Urra et al., 2019), 2008), in females than males (Durso and Mullin, reproductive biology (Cabeza et al., 2019), and natural 2014), or when environmental temperature conditions history (Cañas and Urra, 2019) have been recently are unfavourable for crawling (Mutoh, 1983; Gregory, described and defensive strategies remain extensively 2008). The execution and duration of this behaviour are unknown. In line with this, the only defensive behaviour also determined by the ability of the snake species to reported for this species is the hooding in adults from visually and chemically receive and interpret various the Metropolitan Region of Chile (Jara and Pincheira- signals such as predator type, escape opportunities, and Donoso, 2015). In this study, we describe the first distance and direction of the predator (Burghardt and Greene, 1988; Durso and Mullin, 2014). The genus Philodryas (Wagler 1830) is currently composed of 23 rear-fanged snake species widely distributed in South America and divided into cis- Andean and trans-Andean species (Zaher et al., 2014). Detailed defensive behaviours have been described for cis-Andean species such as P. patagoniensis (Tozetti et al., 2012), P. aestiva (Banci et al., 2018), P. olfersii 1 Network for snake venom research and drug discovery, Santiago, Chile. 2 Programa de Farmacología Molecular y Clínica, Instituto de Ciencias Biomédicas (ICBM), Facultad de Medicina, Figure 1. Thanatosis behaviour by a juvenile of Philodryas Universidad de Chile, Chile. chamissonis (Wiegmann, 1835) at Quebrada El Frances, * Corresponding author. E-mail: [email protected] Valparaiso Region, Chile. 732 Nicolás Zañartu & Félix A. Urra observation of death-feigning behaviour in a juvenile of Greene, H.W., Jaksic, F.M. (1992): The feeding behavior and P. chamissonis. natural history of two Chilean snakes, Philodryas chamissonis In September 2018, during fieldwork at Quebrada and Tachymenis chilensis (Colubridae). Revista Chilena de Historia Natural 65: 485–493. El Francés (32.8667°S, 71.7333°W; WGS 84, 160 m Gregory, P.T. (2008): Bluffing and waiting: handling effects and a.s.l.), Papudo, Valparaiso Region, Chile, a juvenile of post-release immobility in a death-feigning snake (Natrix P. chamissonis was found under rocks in a sclerophyll natrix). Ethology 114: 768–774. forest. When the snake was exposed, it tried to escape Humphreys, R.K., Ruxton, G.D. (2018): A review of thanatosis between adjacent rocks, and when confronted, the snake (death feigning) as an anti-predator behavior. Behavioral flipped over and remained immobile for approximately Ecology and Sociobiology 72: 22. four minutes, exposing its yellow ventral side (Fig. 1). Jara, M., Pincheira-Donoso, D. (2015): The neck flattening defensive behaviour in snakes: First record of hooding in the Unlike some snake species that use death-feigning as South American colubrid genus Philodryas. Animal Biology defensive behaviour, the snake did not open its mouth 65: 73–79. and extrude its tongue. When handled, the specimen Marques, O.A.V. (1999): Defensive behavior of the green snake showed no additional changes in the death-feigning Philodryas viridissimus (Linnaeus) (Colubridae, Reptilia) from behaviour. After five minutes without manipulation and the Atlantic Forest in Northeastern Brazil. Revista Brasileira de at 1 m from the researchers, the snake began tongue- Zoologia 16(1): 266. flicking, raised its head, and slowly crawled away. Mendoza, I. (2009): Defensive behavior in Leptodeira annulata ashmeadii (Hallowell, 1845). Herpetotropicos 5(1): 67. The species of the genus Philodryas are known Mutoh, A. (1983): Death-feigning behavior of the Japanese colubrid to escape quickly when released or attempt to bite snake Rhabdophis tigrinus. Herpetologica 39(1): 78–80. vigorously. Thanatosis has been only described for an Natera-Mumaw, M., Diasparra, J.P., Jiménez, D. (2008): adult male of Philodryas patagoniensis during handling; Defensive behavior in Philodryas viridissima (Linnaeus, 1758). in this case, the behaviour continued even after the snake Herpetotropicos 4(1): 40. was released (Tozetti et al., 2012). Our observation is Riquelme, M., Catchpole, S. (2019): Philodryas chamissonis the first evidence of thanatosis for the poorly known (Wiegmann 1835) (Squamata, Dipsadidae) depredando sobre Phyllotis darwini (Waterhouse 1837) (Rodentia, Cricetidae). trans-Andean group of Philodryas. Further studies are Boletín Chileno de Herpetología 6: 71. required to increase the knowledge about the defensive Torres, F. (2017): Observación de culebra de cola larga, Philodryas behaviour repertoire of these snakes. chamissonis (Wiegmann, 1835) (Squamata: Dipsadidae) depredando sobre un polluelo de yal (Phrygilus fruticeti). Acknowledgements. This work was supported by CONICYT Boletín Chileno de Herpetología 4: 21. PCI-Biotechnology #Redbio0027 (FAU). Tozetti, A.M., Oliveira R.B., Pontes, G.M.F. (2012): Philodryas patagoniensis. Defensive behavior/Thanatosis. Herpetological References Review 43(4): 661. Urra, F.A., Miranda-Calle, A.B., Araya-Maturana, R. (2019): Abegg, A.D., Mario-Darosa, C., Maises, C.A. (2018): Philodryas Philodryas (Serpentes: Dipsadidae) envenomation, a neglected olfersii (Lichtenstein’s Green Racer) Defensive behavior. issue in Chile. Toxins 11(12): 697. Herpetological Review 49(2): 349–350. Urra, F.A., Pulgar, R., Gutiérrez, R., Hodar, C., Cambiazo, V., Labra, Banci, K.R.S., Cunha, A.L.S., Marques, O.A.V. (2018): Philodryas A. (2015): Identification and molecular characterization of five aestiva (Brazilian Green Racer) Habitat use and defensive putative toxins from the venom gland of the snake Philodryas behavior. Herpetological Review 49(1): 137–138. chamissonis (Serpentes: Dipsadidae). Toxicon 108: 19–31. Burghardt, G.M., Greene, H.W. (1988): Predator stimulation and Ushakov, M.V. (2007): On the defensive behavior of the Grass duration of death feigning in neonate hognose snakes. Animal Snake Natrix natrix (Linnaeus, 1758). Russian Journal of Behaviour 36(6): 1842–1844. Ecology 38(2): 124–127. Cabeza, O., Vargas, E., Ibarra, C., Urra, F.A. (2019): Observations Zaher, H., Arredondo, J.C., Valencia, J.H., Arbelaez, E., Rodrigues, on reproduction in captivity of the endemic long-tailed snake M.T., Altamirano-Benavides, M. (2014): A new Andean species Philodryas chamissonis (Wiegmann, 1835) (Reptilia, Squamata, of Philodryas (Dipsadidae, Xenodontinae) from Ecuador. Dipsadidae) from Chile. Herpetozoa 32: 203–209. Zootaxa 3785: 469–480. Cañas, J., Urra, F.A. (2019): Philodryas chamissonis (Chilean Green Racer). Nocturnal activity Herpetological Review 50(3): 600. Durso, A.M., Mullin, S.J. (2014): Intrinsic and extrinsic factors influence expression of defensive behavior in plains hog-nosed snakes (Heterodon nasicus). Ethology 120: 140–148. Gerald, G.W. (2008): Feign versus flight: influences of temperature, Accepted by Fábio Hepp body size and locomotor abilities on death feigning in neonate snakes. Animal Behavior 75(2): 647–654..
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