Herpetology Notes, volume 11: 869-871 (2018) (published online on 15 October 2018)

New defensive behaviours of the false coral Phalotris mertensi (Hoge, 1955) (Serpentes: Dipsadidae)

Bruno F. Fiorillo1,*, Giordano N. Rossi2, and Rafael Menegucci3

Although repertories of defensive tactics have been amphisbaenians, caecilians, and other (Duarte, described for a variety of snake taxa (e.g., Sazima and 2006; Marques et al., 2009, 2015). Abe, 1991; Natera-Mumaw et al., 2008; Tozetti et al., Probably due to the fossorial lifestyle of P. mertensi 2009; Alves et al., 2013; Alcântara-Menezes et al., and difficulty to observe it in nature, the only known 2015, 2017; Guedes et al., 2017; Atkinson, 2018), there defensive behaviours for this are erratic are still many gaps in our knowledge, even for the best- movements and stinging with the tail (Marques et al., known species (e.g., Martins et al., 2008; Marques et al., 2015). Here we present defensive behaviours that have 2015; Alcântara- Menezes et al., 2015). Most species not been previously described for this species. The of false coral snakes, particularly those in the genera first observation was made on 28 June 2017 at Bonfim Apostolepis and Phalotris are fossorial (Marques et al., Paulista, Ribeirão Preto Municipality, São Paulo, Brazil 2015), which allows for observations only rarely and (21.3052°S, 47.8074°W). While being photographed, thus increases the difficulty in obtaining basic natural an adult female P. mertensi, snout–vent length (SVL) history information such as diet, reproduction, diary ca. 60 cm, shook its head from side to side and gaped activity, or behaviour. as the camera or handler’s hand approached it, ceasing Phalotris mertensi is one of those rarely encountered to present this behaviour as the handler moved away. species (Marques et al., 2015). It occurs primarily in As manipulation continued, the individual behaved seasonal and ombrophilous forests in Cerrado areas as described five more times. On 28 July 2018, at of the southernmost part of Brazil (Ferrarezzi, 1993; Santa Bárbara Ecological Station, Águas de Santa Costa et al., 2007; Sawaya et al., 2008; Condez et al., Bárbara Municipality, São Paulo, Brazil (22.8244°S, 2009; Bérnils, 2009). However, it has also been found in 49.2264°W), we captured an individual (male, SVL altered areas in the vicinities of the Itirapina Ecological ca. 60 cm) that displayed the same behaviour once and Station, which includes agricultural lands, cattle raising, also tried to bury itself (forcing the head against the leaf pine and eucalyptus plantations, and a dam (Sawaya litter) (Fig. 1B). et al., 2008). This species has fossorial habits and has Phalotris mertensi is a species that spends most of its been observed in activity during both day and night life in crevices, holes or underground (Sawaya et al., (Sawaya et al., 2008; Condez et al., 2009; Marques et 2008; Marques et al., 2015). However, even fossorial al., 2015). Its diet includes elongated vertebrates such as may explore the terrestrial stratum (e.g., forced by soil saturation after heavy rains; see Almeida et al., 2016). Burying itself is a primary defence and may operate before predators initiate prey-catching interaction (e.g., Robinson, 1969). However, non- aggressive defences such as withdrawing itself from the 1 Escola Superior de Agricultura Luiz de Queiroz, Universidade surface environment are never perfect since it’s possible de São Paulo, Piracicaba, São Paulo 13418-900, Brazil. for a predator to discover prey by chance or during a 2 Universidade Estadual Paulista “Júlio de Mesquita Filho”, systematic search for food (Edmunds, 1974). Hence, Jaboticabal, São Paulo 14884-900, Brazil. 3 Projeto Dacnis, Estrada Monte Valério 4754, Sertão das such prey is sometimes forced to resort to aggressive Cotias, Ubatuba, São Paulo 11680-000, Brazil. tactics, known as secondary defences (Edmunds, 1974). * Corresponding author. E-mail: [email protected] Once knowing it has been detected, the prey may signal 870 Bruno F. Fiorillo et al.

based arboreal and/or terrestrial species (Martins and Oliveira, 1998; Marques et al., 2001, 2005, 2015, 2017; Martins et al., 2008; Sawaya et a., 2008), and although gaping behaviour is common between other fossorial squamates (e.g. amphisbaenians; see Greene, 1973), this is, to our knowledge, the first time gaping behaviour is described for a fossorial snake species. This type of behaviour may be rare in fossorial snakes because they choose to escape and bury themselves most of the time (as evidenced in one of the individuals; Fig. 1B) or because they are difficult to observe and consequently their behaviour is not well documented. Alternatively, gaping behaviour could be considered as a deimatic strategy if there is contrast of colourations between the mouth and the body surface of the individual (e.g., Oxybelis aeneus, see Martins and Oliveira, 1998). This is not the case in P. mertensi since this species does not present such colour contrast. Thus, we must conclude that it is only a threat of injury through a bite to the potential predator. In addition, P. mertensi presents aposematic coloration and possibly potent toxins like other species of the (e.g., P. trilineatus; Valls- Moraes and Lema, 1997) that could favour secondary Figure 1. Phalotris mertensi, from: (A) Bonfim Paulista, defence behaviours. Ribeirão Preto (São Paulo, Brazil), displaying gaping as a defensive behaviour; (B) Santa Bárbara Ecological Station, Águas de Santa Bárbara (São Paulo, Brazil), burying itself Acknowledgements. The authors are grateful to Marcio Borges Martins, for valuable suggestions on the manuscript. B.F. Fiorillo in the leaf litter. Photos by Rafael Menegucci (A) and Bruno thanks the São Paulo Research Foundation (FAPESP, grant # Ferreto Fiorillo (B). 2015/21259-8) and Marcio Roberto Costa Martins.

References to predators and transmit behavioural warnings about Alcântara-Menezes, F.A, Fiorillo, B.F., Gonzalez, R.C. (2015): the dangers of contact, or signal that it has been sighted Hooding behavior in Erythrolamprus miliaris Linnaeus, 1758 but will not easily let the predator succeed, which may (Serpentes: Dipsadidae). Notes 8: 291–293. prevent the predator to attack (Dugatkin, 2013). Alcântara-Menezes, F., Fiorillo, B.F., Franco, F.L., Feio, R.N. As described in previous studies, defence behaviour (2017): Repertoire of antipredator displays in the poorly known seems to be less conserved than other acting pattern snake Gomesophis brasiliensis (Gomes, 1918) from the Atlantic Forest. Herpetology Notes 10: 245–247. traits in Neotropical snakes (e.g., feeding habits, habitat Almeida, P.C.R., Prudente, A.L.C., Curcio, F.F., Rodrigues, use, and reproduction; Martins and Oliveira, 1998; M.T.U. (2016): Biologia e história natural das cobras-corais. Martins et al., 2002, 2008). Alcântara-Menezes et al. In: As Cobras-corais do Brasil: Biologia, Taxonomia, Venenos (2017) suggested that some defensive behaviours may Envenenamentos, p. 168–215. Goiânia, Goiás, Brazil, Ed. be used simply because they have low energy costs PUC. and/or are well established among snakes in their Alves, S.S., Bolzan, A.M.R., Santos, T.G., Gressler, D.T., Cechin, evolutionary history. Since gaping probably has low S.Z. (2013): Rediscovery, distribution extension and defensive energy cost and is exhibited in several snake genera and behavior of Xenodon histricus (: Serpentes) in the state of Rio Grande do Sul, Brazil. Salamandra 49(4): 219–222. families (e.g., Boa, Chironius, Gomesophis, Leptophis, Atkinson, K., Smith, P., Dickens, J.K., Lee-Zuck, C. (2018): Xenodon; Martins et al., 2008, Marques et al., 2015, Rediscovery of the ‘lost’ snake Phalotris multipunctatus Alcântara-Menezes et al., 2017), such behaviour could (Serpentes: Dipsadidae) in Paraguay with behavioral notes and increase chances of survival during encounters with reference to the importance of Rancho Laguna Blanca for its predators. On the other hand, most of these are visual conservation. Current Herpetology 37(1): 75–80. A new defensive behaviour of the false coral snake Phalotris mertensi 871

Bérnils, R.S. (2009): Composição e Padrões de Distribuição de Marques, O.A.V., Eterovic, A., Nogueira, C.C., Sazima, I. (2015): Caenophidia (Squamata, Serpentes) das Serras Atlânticas e Serpentes do Cerrado: Guia Ilustrado, First Edition. Ribeirão Planaltos do Sudeste da América do Sul. Unpublished Ph.D. Preto, São Paulo, Brazil, Holos Press. Thesis, Universidade Federal do Rio de Janeiro, Rio de Janeiro, Marques, O.A.V., Eterovic, A., Guedes, T.B., Sazima, I. (2017): Brazil. Serpentes da Caatinga: Guia Ilustrado, First Edition. Ribeirão Condez, T.H, Sawaya, R.J., Dixo, M. (2009): Herpetofauna of Preto, São Paulo, Brazil, Holos Press. the Atlantic Forest remnants of Tapiraí and Piedade region, Martins, M., Oliveira, M.E. (1998): Natural history of snakes São Paulo state, southeastern Brazil. Biota Neotropica 9(1): in forests of the Manaus region, Central Amazonia, Brazil. 57–185. Herpetological Natural History 6: 78–150. Costa, G.C., Nogueira, C., Machado, R.B., Colli, G.R. (2007): Martins, M., Marques, O.A.V., Sazima, I. (2002): Ecological and Squamate richness in the Brazilian Cerrado and its environmental- phylogenetic correlates of feeding habits in neotropical pitvipers climatic associations. Diversity and Distributions 13: 714–724. of the genus Bothrops. In: Biology of the Vipers, p. 307–328. Duarte, M.R. (2006): Natural history notes. Phalotris mertensi Schuett, G.W., Hoggren, M., Douglas, M.E., Eds., Utah, USA, (false coral snake) and Amphisbaena mertensi (NCN). Predation. Eagle Mountain Press. Herpetological Review 37(2): 234. Martins, M., Marques, O.A.V., Sazima, I. (2008): How to be Dugatkin, L.A. (2013): Principles of Behavior. In: arboreal and diurnal and still stay alive: microhabitat use, time Antipredator behaviour, p. 382–412. New York, USA, W. W. of activity, and defense in Neotropical forest snakes. South Norton & Company Press. American Journal of Herpetology 3: 58–67. Edmunds, M. (1974): Defense in Animals, First Edition. Burnt Natera-Mumaw, M., Diasparra, J.P., Novoa, J., Jiménez, D. (2008): Mill, England, Longman Group Limited Press. Defensive behavior in Philodryas viridissima (Linnaeus, 1758). Ferrarezzi, H. (1993): Nota sobre o gênero Phalotris com revisão Herpetotropicos 4(1): 40. do grupo Nasutus e descrição de três novas espécies (Serpentes, Robinson, M.H. (1969): The defensive behavior of some , ). Memórias do Instituto Butantan 55: orthopterigoid insects from Panama. Transactions of the Royal 21–38. Entomological Society of London 121: 281–303. Guedes, J.J.M., Assis, C.L., Silva, D.H., Feio, R.N. (2017): New Sawaya, R.J., Marques, O.A.V., Martins, M. (2008): Composição e records and notes on defensive behavior of Thamnodynastes história natural das serpentes de Itirapina, São Paulo, sudeste do rutilus (Prado 1942). Neotropical Biology and Conservation Brasil. Biota Neotropica 8(2): 127–149. 12(2): 154–158. Sazima, I., Abe, A.S. (1991): Habits of five Brazilian snakes with Greene, H.W. (1973): Defensive Tail Display by Snakes and coral-snake pattern, including a summary of defensive tactics. Amphisbaenians. Journal of Herpetology 7(3): 143–161. Studies on Neotropical Fauna and Environment 26(3): 159– Marques, O.A.V., Eterovic, A., Sazima, I. (2001): Serpentes da 164. Mata Atlântica: guia ilustrado para a Serra do Mar, First Edition. Tozetti, A.M., Oliveira, R.B., Pontes, G.M.F. (2009): Defensive Ribeirão Preto, São Paulo, Brazil, Holos Press. repertoire of Xenodon dorbignyi (Serpentes, Dipsadidae). Biota Marques, O.A.V., Eterovic, A., Strüssmann, C., Sazima, I. (2005): Neotropica 9(3): 157–163. Serpentes do Pantanal: guia ilustrado, First Edition. Ribeirão Valls-Moraes, F., Lema, T. (1997): Envenomation by Phalotris Preto, São Paulo, Brazil, Holos Press. trilineatus in Rio Grande do Sul State, Brazil: a case report. Marques, O.A.V., Pereira, D.N., Barbo, F.E., Germano, V.J., Journal of Venomous Animals and Toxins 3(1): 106. Sawaya, R.J. (2009): in São Paulo municipality: diversity and ecology of the past and present fauna. Biota Neotropica 9(2): 139–150.

Accepted by Andre Bruinjé