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Additional Defensive Behaviours of Dipsas Mikanii (Schlegel, 1837) and Taeniophallus Occipitalis (Jan, 1863) (Serpentes: Dipsadidae)

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Additional Defensive Behaviours of Dipsas Mikanii (Schlegel, 1837) and Taeniophallus Occipitalis (Jan, 1863) (Serpentes: Dipsadidae) Herpetology Notes, volume 12: 359-362 (2019) (published online on 0 April 2019) Additional defensive behaviours of Dipsas mikanii (Schlegel, 1837) and Taeniophallus occipitalis (Jan, 1863) (Serpentes: Dipsadidae) Bruno F. Fiorillo1,*, Giordano N. Rossi2, and Marcio Martins3 Snakes evolved defensive behaviours to avoid being 2015). Its diet is specialized in gastropods (Oliveira, detected, injured or killed by predators, and they possess 2001; Marques et al., 2015). an array of such behaviours (see a review in Greene, Taeniophallus occipitalis is a terrestrial, diurnal species 1988). The family Dipsadidae is widespread in the New that is found in leaf-litter (Sawaya et al., 2008; Morato et World and exhibits a high species diversity in Central al., 2011; Marques et al., 2015) of open vegetation types and South America, and the West Indies (Zaher et al., of the Cerrado (Scrocchi and Giraudo, 2005; França 2009; Vidal et al., 2010). Previous studies have reported et al., 2008; Sawaya et al., 2008). It does not seem to different defensive tactics used by several species of this persist in disturbed areas (Sawaya et al., 2008). Its diet family (e.g. Martins and Oliveira, 1998; Martins et al., is composed mainly of anurans and lizards (Yanosky et 2008; Maia-Carneiro et al., 2012; Menezes et al., 2015, al., 1996; Cechin, 1999; Marques et al., 2009). 2017; Atkinson, 2018; Fiorillo et al., 2018). However, Known defensive behaviours of D. mikanii are head there is still much to discover about defensive behavior triangulation, hiding the head, cloacal discharge, and in snakes, and the description and documentation of striking (Marques et al., 2015). For T. occipitalis, body new defensive behaviours can help us gain a better depression and cloacal discharge have been described understanding of the ecology and evolution of defensive (Marques et al., 2015). Here we report additional strategies in snakes (Martins, 1996; Martins et al., defensive behaviours for these species. On 19 July 2008). Here, we present observations of novel defensive 2018 at Santa Bárbara Ecological Station, Águas de behaviors of two species of dipsadid snakes from Brazil, Santa Bárbara Municipality, São Paulo, Brazil (22.8244 Dipsas mikanii and Taeniophallus occipitalis. S, 49.2264 W), we captured an individual D. mikanii Dipsas mikanii is widely distributed in central and (juvenile, snout-vent length ca. 20 cm) that displayed eastern Brazil, as well as in the Missiones region of hooding, flattening itself while keeping the anterior Argentina and adjacent Paraguay, and occurs in diverse portions of its body elevated (Fig. 1). This behaviour habitats, from forests to open savannas in the Brazilian was observed repeatedly every time its path was blocked Cerrado, where it is commonly found (Franco, 1994; (about four times) by the researcher during escape Cacciali, 2006; França et al., 2008; Sawaya et al., 2008; attempts. On 25 July 2018, at the same study area, we Freitas et al., 2014; Marques et al., 2015, 2017). It has captured an individual T. occipitalis (male, snout-vent terrestrial habits and is primarily nocturnal (Sazima and length ca. 25 cm). This individual was placed inside a Manzini, 1995; Sawaya et al., 2008; Marques et al., glass cup to be photographed. The glass cup containing the snake was then put upside-down on a tray filled with sand where photographs were taken. The snake fell upside-down on the sand and remained static in this position after we removed the glass cup, in a behaviour 1 Escola Superior de Agricultura Luiz de Queiroz, Universidade similar to thanatosis. After touching and moving the de São Paulo, Piracicaba, SP 13418-900, Brazil. snake a couple of times, it rotated itself upright and 2 Universidade Estadual Paulista “Júlio de Mesquita Filho”, tried to flee. We then repeated the process of turning Jaboticabal, SP 14884-900, Brazil. 3 Instituto de Biociências, Departamento de Ecologia, the snake upside-down within the glass cup three more Universidade de São Paulo, São Paulo, SP 05508-090. times without the snake presenting thanatosis, but at * Corresponding author. E-mail: [email protected] the fourth time we repeated the process the individual 360 Bruno F. Fiorillo et al. Figure 1. Different views of Dipsas mikanii, from Santa Bárbara Ecological Station, Águas de Santa Bárbara (São Paulo, Brazil), displaying hooding behaviour. Photos by Bruno Ferreto Fiorillo (A), Matheus Januário Lopes de Sousa (B) and Giordano Novak Rossi (C). displayed the behaviour again and a photograph was spp. and Aspidelaps spp.) when they are facing a threat taken (Fig. 2). (Greene, 1997; Kahn, 2011). It is well accepted that The hooding behaviour reported here for D. mikanii has hooding increases the apparent size of the individual already been recorded for its sister species D. neuwiedii and alerts the predator about a potential risk (Greene, (Martins et al., 2008), as well as other species of the 1988, 1997; Young and Kardong, 2010). family Dipsadidae (e.g. in the genera Erythrolamprus, Thanatosis has been observed in a great diversity of Hydrodynastes, Thamnodynastes, Xenodon; Greene, snakes, including colubrids, natricids, dipsadids, and 1979; Martins and Oliveira, 1998; Franco et al., 2003;elapids (Gerald, 2008; Mirza et al., 2011; Bhosale and Young and Kardong, 2010; Kahn, 2011; Menezes Thite, 2013; Marques et al., 2013; Sannolo at al., 2014). et al., 2015). This defensive behaviour is commonly However, thanatosis is rarely reported among dipsadids performed by species of Old World elapids, specifically (Marques et al., 2013; Durso and Mullin, 2014; Muscat cobras (e.g. Naja spp., Hemachatus spp., Ophiophagus et al., 2016). A number of different hypotheses have been Additional defensive behaviours of Dipsas mikanii and Taeniophallus occipitalis 361 References Atkinson, K., Smith, P., Dickens, J.K., Lee-Zuck, C. (2018): Rediscovery of the ‘lost’ snake Phalotris multipunctatus (Serpentes: Dipsadidae) in Paraguay with behavioral notes and reference to the importance of Rancho Laguna Blanca for its conservation. Current Herpetology 37 (1): 75–80. Bhosale, H.S., Thite, V. (2013): Death feigning behavior in large-eyed false cobra Pseudoxenodon macrops (Blyth, 1854) (Squamata: Colubridae). Russian Journal of Herpetology 20 (3): 190–192. Cacciali, P. (2006): Las Serpientes Caracoleras (Colubridae: Dipsadinae) de Paraguay. Revista Española de Herpetologia: 20: 71–85. Cechin, S.Z. (1999): História natural de uma comunidade de Figure 2. Taeniophallus occipitalis, from Santa Bárbara serpentes na região da depressão central (Santa Maria) Rio Ecological Station, Águas de Santa Bárbara (São Paulo, Grande do Sul, Brasil. Unpublished Ph.D. Thesis, Pontífica Brazil), displaying death feigning behaviour. Photo by Bruno Universidade Católica do Rio Grande do Sul, Rio Grande do Ferreto Fiorillo. Sul, Brazil. Durso, A.M., Mullin, S.J. (2014): Intrinsic and extrinsic factors influence the expression of defensive behaviors in Plains Hog- nosed Snakes (Colubridae: Heterodon). Ethology 120: 140– suggested to explain the exact function of this behaviour, 148. Edmunds, M. (1974): Defense in Animals. Longman Group such as the loss of interest of predators specializing Limited, First Edition. New York, USA, Longman Group in live prey (Rovee et al., 1976) or enhanced escape Limited. opportunity (Ratner and Thompson, 1960; Rovee et al., Fiorillo, B.F., Rossi, G.N., Menegucci, R. (2018): A new defensive 1976). Nevertheless, the exact mechanisms by which behaviour of the false coral snake Phalotris mertensi (Hoge, thanatosis deters predation are still unclear, particularly 1955) (Serpentes: Dipsadidae). Herpetol Notes No prelo. among vertebrates. Many snake species that invert their França, F.G.R., Mesquita, D.O., Nogueira, C.C., Araújo, A.F.B. bodies defensively expose brightly or highly-contrasting (2008): Phylogeny and Ecology Determine Mophological Structure in a Snake Assemblage in the Central Brazilian ventral patterns or coloration, and the ventral side of T. Cerrado. Copeia 1: 23–8. occipitalis is a moderately bright yellow, in contrast to Franco, F.L. (1994): O gênero Sibynomorphus Fitzinger, 1843 no its brown dorsum. This “flash coloration” may play a Brasil (Colubridae, Xenodontinae, Dipsadini). Unpublished Msc. role in startling potential predators (e.g. McCallum et Dissertation, Instituto de Biociências, Pontifícia Universidade al., 2006). Católica, Rio Grande do Sul, Porto Alegre, Brazil. The behaviours described here have in common Franco, F.L., Ferreira, T.G., Marques, O.A.V., Sazima, I. (2003): that they are secondary defences that occur during A new species of hood-displaying Thamnodynastes (Serpentes: Colubridae) from the Atlantic forest in southeast Brazil. Zootaxa the encounter with the predator (Edmunds, 1974) and 334: 1–7. are targeted to visually oriented predators (Martins et Freitas, M.A., Almeida, J.L.B., Almeida, M.S.M., Danin, al., 2008). They act through different mechanisms (to T.S., Moura, J.B. (2014): Rediscovery and First Record of intimidate and feigning death, respectively) but have Sibynomorphus mikanii septentrionalis Cunha, Nascimento & the same ultimate goal (to survive a predation attempt). Hoge, 1980 (Squamata; Serpentes) for the State of Pará. Check Moreover, both are widespread not only among the List 10 (5): 1246–1248. Dipsadidae but in several other groups of snakes, Gerald, G.W. (2008): Feign versus flight: influences of temperature, body size and locomotor abilities on death feigning in neonate suggesting convergence and relative success of these snakes. Animal Behaviour 75: 647–654. strategies. Greene, H.W. (1979): Behavioral convergence in the defensive displays of snakes. Experientia 35: 747–748. Greene, H.W. (1988): Anti-predator mechanisms in reptiles. In: Acknowledgements. The authors are grateful to São Paulo Biology of the Reptilia, p. 1–152.Gans, C., Huey, R.B., Eds., Research Foundation (FAPESP, grant # 2015/21259-8). New York, USA, Academic Press. Greene, H.W. (1997): Snakes: The Evolution of Mystery in Nature. First Edition. Berkeley CA: University of California Press. Kahn, T.R. (2011): Cobra-like hooding and mouth-gapping in an atypically monocle patterned Xenodon severus (Linnaeus, 1758): 362 Bruno F. Fiorillo et al.
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