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Death-Feigning Behaviour in Micrurus Ortonii (Schmidt, 1953) (Elapidae) in Northern Brazil

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Death-Feigning Behaviour in Micrurus Ortonii (Schmidt, 1953) (Elapidae) in Northern Brazil Herpetology Notes, volume 13: 603-606 (2020) (published online on 05 August 2020) Death-feigning behaviour in Micrurus ortonii (Schmidt, 1953) (Elapidae) in northern Brazil Rodrigo Castellari Gonzalez1,* and Uécson Suendel Costa de Oliveira2 Micrurus ortonii (Schmidt, 1953) (Serpentes, unknown, especially regarding its defensive repertoire Elapidae) is a coral snake in the M. hemprichii (Almeida et al., 2016; Rojas-Morales et al., 2018). complex, traditionally classified as a subspecies of M. Death-feigning is classified as a “late” defensive tactic hemprichii (Silva-Jr. et al., 2016). Recently, Valencia (Honma et al., 2006; Humpreys and Ruxton, 2018), et al. (2016) proposed elevating it to specific status, a since it is triggered after physical contact with a predator recommendation that was followed by Bernarde et al. (Gehlbach, 1970; Honma et al., 2006), and typically (2018) but which has not yet been rigorously evaluated. involves a stereotyped set of behaviours such as tonic The species’ diagnostic characters include a single immobility, stiffness, turning belly up, mouth gaping cloacal plate and the colour pattern (triads with long and tongue protrusion (McDonald, 1974; Greene, 1988; black rings intercalated by yellow-orange and white Humphreys and Ruxton, 2018). rings) (Schmidt 1936, 1953, 1955; Campbell and Lamar These complex behaviours could increase the chances 1989, 2004; Fraga et al., 2013; Silva-Jr et al., 2016; of survival whether the predator loses interest, and gets Valencia et al., 2016; Bernarde et al., 2018). Micrurus distracted to permit a quick escape (Honma et al., 2006; ortonii is both diurnal and nocturnal, and feeds on Humphreys and Ruxton, 2018) or even by hampering lizards, other snakes and onychophorans (Beebe, 1946; the possibility of being swallowed due to stiffness and Dixon and Soini, 1986; Chippaux, 1986; Silva-Jr., 1993; body shape (Honma et al., 2006). However, the exact Silva, 1994; Roze, 1996; Martins and Oliveira, 1998; mechanisms by which it is effective as a defensive tactic Bernarde and Abe, 2006; Fraga et al., 2013; Santos- are unclear (Gehlbach, 1970; McDonald, 1974; Greene, Costa et al., 2015; Rojas-Morales et al., 2018). It can be 1988; Honma et al., 2006) and likely depend on the found in primary and secondary forests in the Amazon predator’s foraging mode (i.e. death feigning should lowlands (Martins and Oliveira, 1998; Bernarde and only work against visually-oriented predators which Abe, 2006; Ribeiro-Jr et al., 2008; Santos-Costa et al., do not eat dead prey or save prey for later consumption 2015), east of the Andes in Colombia, Ecuador, Peru, (Ratner and Thompson, 1960; Gehlbach, 1970; Rovee Bolivia and Brazil (Schmidt, 1953; Roze, 1967, 1996; et al., 1976; Greene, 1988). Hoge and Romano, 1971; Dixon and Soini, 1986; Here we describe the death-feigning behaviour of an Campbell and Lamar, 1989, 2004; Silva-Jr et al., 2016). individual Micrurus ortonii found on a forest path in Due to its cryptic habits, often being found underground Rondônia, northern Brazil, the first such record for this or within the leaf litter (Dixon and Soini, 1986; Martins species (or for M. hemprichii, if subspecies designation and Oliveira, 1998), most of its biology remains largely is ultimately retained). On 13 March 2014, at 10:00 h, during fieldwork in Mutum Paraná, district of Porto Velho, Rondônia, Brazil (09°34’30.16”S, 64°50’55.14”W; datum SAD69,121 m a.s.l.), we found an adult male Micrurus ortonii moving in the leaf litter on a forest path. Immediately after being 1 Museu de História Natural do Ceará Prof. Dias da Rocha, manipulated, it started to behave lethargically (Fig. 1A). Centro de Ciências da Saúde, Universidade Estadual do Ceará, It then consecutively turned belly up, opened its mouth Fortaleza, 60741-000, Ceará, Brazil. (Fig. 1B) and stopped showing responses to external 2 Programa de Pós-Graduação em Biotecnologia e Biodiversidade/ PPG Bionorte, Universidade Federal do Acre, Rio Branco, stimuli as it was touched with a snake hook. This 69915-900, Acre, Brazil. behaviour lasted for approximately 4 minutes, during * Corresponding author: E-mail: [email protected] which the animal’s body remained stiff and its mouth 604 Rodrigo Castellari Gonzalez & Uécson Suendel Costa de Oliveira Figure 1. Death-feigning by Micrurus ortonii (Schmidt, 1953), still in normal position A), after turning itself belly-up B) in Amazon, Brazil. Photographs by Uécson S.C. de Oliveira; also published in Almeida et al., 2016, without description. slightly open, but with the tongue withdrawn. The least occasionally employ thanatosis as a defensive animal only started behaving normally after it was left mechanism, although they might easily resort to using alone, as we moved about 5 m away from it. No other venom (e.g. Bothrops erythromelas; Santos and Muniz, defensive behaviour could be observed afterwards, nor 2012; B. jararacussu; Muscat and Entiauspe-Neto, did we try to re-induce this behaviour, as the animal was 2016; Hemachatus haemachatus, Naja haje, Naja left in the wild. nigricollis; Gehlbach, 1970; Vogel and Han-Yuen, Even though death-feigning is widespread (Vogel and 2010). Because snakebite envenoming does not result in Han-Yuen, 2010; Humphreys and Ruxton, 2018), it is the rapid onset of severe pain in predators, antipredator believed to be underreported (Humphreys and Ruxton, defence is probably not the primary function of venom, 2018), since it is rarely seen in the field and difficult although there may be some exceptions (Ward-Smith et to test in controlled environments. Death-feigning also al., 2020). seems to be widespread amongst snakes (Mutoh, 1983; Finally, many snake species invert their positions Vogel and Han-Yuen, 2010), being reported for numerous defensively to expose brightly or highly-contrasting taxa (see Vogel and Han-Yuen, 2010 for a larger list). ventral patterns, and although both the dorsal and Other Micrurus (including Micrurus frontalis, M. tener, ventral sides of M. ortonii are brightly coloured with M. paraensis, M. remotus, and M. spixii; Azevedo, contrasting patterns, they do differ (Fig. 1), with brighter 1960, Gehlbach, 1970; Almeida et al., 2016) are known orange-yellow and white spots on the venter. This “flash to exhibit thanatosis. Micrurus also employ a variety of colouration” might also play a role in startling potential other defensive tactics, such as aposematic colouration, predators (e.g. McCallum et al., 2006). immobility, fleeing, dorso-ventral flattening, hiding In general, Micrurus have secretive habits, usually the head in the body-coils, tail displays, hemipenal or being found underground or in the leaf litter (Martins cloacal eversion, body thrashing, and biting (Martins, and Oliveira, 1998; Fraga et al., 2013, Almeida et al., 1996; Martins and Oliveira, 1998; Fraga et al., 2013; 2016). Since their behaviour is difficult to observe Vitt and Caldwell, 2013; Santos-Costa et al., 2015; (Gehlbach, 1970; Humpreys and Ruxton, 2018) it is Almeida et al., 2016). Puzzlingly, both aposematism usually not recorded by general collectors. We highlight and thanatosis seem to be most successfully employed the importance of observing and documenting snake against visually-oriented predators, and it is not clear behaviour before collecting them. under what circumstances one or the other may be relied upon. Acknowledgments. We thank Ana Carolina Calijorne Lourenço, Besides Micrurus, several other medically-important Moises Barbosa de Souza and Andrew M. Durso for valuable venomous snakes that lack aposematic colouration at suggestions in the text and lab support. Death-feigning behaviour in Micrurus ortonii in northern Brazil 605 References of Heterodon platyrhinos Latreille (Serpentes). Journal of Herpetology 8: 157–164. Almeida, P.C.R., Prudente, A.D.C., Curcio, F.F., Rodrigues, Mutoh, A. (1983): Death-feigning behavior of the Japanese colubrid M.T.U. (2016): Biologia e história natural das cobras-corais. snake Rhabdophis tigrinus. Herpetologica 39: 78–80. In As Cobras-Corais do Brasil: Biologia, Taxonomia e Muscat, E., Rotenberg, E.L., Machado, I.F. (2016): Death-feigning Envenenamentos, p. 168–215. Silva-Jr, N.S., Org., Ed., Goiania, behaviour in an Erythrolamprus miliaris (Linnaeus 1758) water Brazil, PUC Goiás. snake in Ubatuba, São Paulo, southeastern Brazil (Dipsadidae). Azevedo, A.C.P. (1960): Notes on coral snakes (Serpentes, Herpetology Notes 9: 95–97. Elapidae). I. About the eggs of coral snakes. II. A new Muscat, E., Entiauspe-Neto, O.M. (2016): Bothrops jararacussu observation of the behavior of Micrurus frontalis multicinctus (Atlantic forest Jararacussu) - defensive behavior. Herpetological and its relationship with folklore. Iheringia, Zoologia 14: 1–13. Review 47: 474. Beebe, W. (1946): Field notes on the snakes of Kartabo, British Ratner, S.C., Thompson, R.W. (1960): Immobility reactions (fear) Guiana and Caripito, Venezuela. Zoologíca, Chicago 31: 11– of domestic fowl as a function of age and prior experience. 52. Animal Behaviour 8: 186-191. Bernarde, P.S., Abe, A.S. (2006): A snake community at Espigão Ribeiro-Júnior, M.A., Gardner, T.A., Ávila-Pires, T.C. (2008): do Oeste, Rondônia, Southwestern Amazon, Brazil. South Evaluating the effectiveness of herpetofaunal sampling American Journal of Herpetology 1: 102–113. techniques across a gradient of habitat change in a tropical forest Bernarde, P.S., Turci, L.C.B., Abegg, A.D., Franco, F.L. (2018): A landscape. Journal of Herpetology 42: 733–750. remarkable new species of coralsnake of the Micrurus hemprichii Rojas-Morales, J.A., Cabrera-Vargas, F.A., Ruiz-Valderrama, D.H. species group from the Brazilian Amazon. Salamandra 54: 249– (2018): Ninia hudsoni (Serpentes: Dipsadidae) as prey of the 258. coral snake Micrurus hemprichii ortonii (Serpentes: Elapidae) Campbell, J.A., Lamar, W.W. (1989): The venomous Reptiles of in northwestern Amazonia. Boletín Científico del Centro de Latin America. Ithaca, USA, Cornell University Press. Museos of the Universidad de Caldas 22: 102–105. Campbell, J.A., Lamar, W.W. (2004): The venomous reptiles of Roze, J.A.
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