Herpetology Notes, volume 11: 831-834 (2018) (published online on 28 September 2018)

Predation attempt on crucifer (Wied-Neuwied, 1821) (Anura, Bufonidae) by Leptodactylus cf. latrans (Steffen, 1815) (Anura, Leptodactylidae) in southern Bahia,

Omar Rojas-Padilla1,*, Vinicius Queiroz Menezes2, Celso Henrique Varela Rios3, Yvonnick Le Pendu1,4, and Caio Vinícius de Mira-Mendes4

Amphibians occupy distinct ecological niches and can of their heads (Jared et al., 2015). Also, the species of feed on different organisms throughout their life stages, the genus Trachycephalus produces viscous and sticky but “practically anything will eat an ” (Poter, secretions that irritate the mucous membranes (Savage, 1972 in Duellman and Trueb, 1993, p. 244). During 2002). Similarly, the anurans of the genus Rhinella the evolution of predator-prey relations, predators have (Bufonidae) have two paratoid glands at the base of the developed strategies to become successful hunters, head that store bufogenines and bufotoxins as defensive while preys have developed defensive strategies, which compounds against predators (Jared et al., 2009). Thus, can be behavioural, morphological or involve noxious skin chemical defenses of are used with secretions, among others (Toledo et al., 2011). goal of preventing the predation attempt, in some cases The skin of amphibians is covered with glands that may lead to the death of the predator. produce secretions containing chemicals that are is distributed in areas of the Atlantic important defense against skin pathogens (e.g. Rollins- Forest in the states of Ceará, Paraíba, Pernambuco, Smith et al., 2005), as well cause various effects on contact Sergipe, Bahia, Minas Gerais, Espírito Santo and Rio whit mucosa of the mouth and eyes of predators (Toledo de Janeiro (Frost, 2018). This species can be found on and Jared, 1995). Most amphibians have been considered leaf litter of forest, but also in disturbed areas. It can poisonous, and only a few species have been found to use temporary and permanent ponds and brooks for actively inject venom: the Amazonian Rhaebo breeding (Aquino et al., 2004). guttatus squirts poison from his paratoid macroglands According to de Sá et al. (2014), the binomial (Jared et al., 2011), while the casque-headed tree Leptodactylus latrans represents a species complex and Aparasphenodon brunoi and Corythomantis greening its distinction from L. chaquensis and L. macrosternum are able to inject venom through the co-ossified spines is unclear. They assume that the only taxonomic statement that can be made is that L. latrans occurs in its type locality in Rio de Janeiro. Following de Sá et al. (2014) we prefer to keep Leptodactylus cf. latrans for populations occurring outside the type locality. This species occurs in several types of habitats, from 1 Programa de Pós-Graduação em Zoologia, Universidade Estadual de Santa Cruz, Rodovia Jorge Amado, km 16, savannas to forest, presenting a high adaptive capacity 45662-900 Ilhéus, Bahia, Brazil. to anthropogenic environments (Heyer et al., 2010). 2 Departamento de Ciências Biológicas, Universidade Estadual On march 7, 2018 around 9 PM, we found an de Santa Cruz, Rodovia Jorge Amado, km 16, 45662-900 adult individual of Rhinella crucifer (70 mm SVL, Ilhéus, Bahia, Brazil. approximately) being predated by an adult Leptodactylus 3 Hileia Consultoria Ambiental Ltda., Rua Santanésia 538, CEP cf. latrans (140 mm SVL, approximately) (Fig. 1A), 1 05580-050, São Paulo, São Paulo, Brazil. meter from a permanent pond located in the municipality 4 Programa de Pós-Graduação em Sistemas Aquáticos Tropicais, Universidade Estadual de Santa Cruz, Rodovia Jorge Amado, of Uruçuca, state of Bahia, Brazil (14.6186 °S, 39.3555 km 16, 45662-900 Ilhéus, Bahia, Brazil. °W). The R. crucifer was being ingested headfirst * Corresponding author. E-mail: [email protected] since almost the whole body of the toad was inside the 832 Omar Rojas-Padilla et al.

Figure 1. Adult of Leptodactylus cf. latrans attempting predation on an individual of Rhinella cruficer (A); individual of L. cf. latrans jumped into the marginal vegetation still with R. crucifer in the mouth (B); evidence of the toxins released by R. crucifer after being released by L. cf. latrans (C).

mouth of the L. cf. latrans, standing out just the arms secretions during the predation attempt (Fig. 1C). These and legs. The ventral position of R. crucifer could be secretions are only released after the glands undergo the consequence of thanatosis behaviour (Teles et al., mechanical pressure (Jared et al., 2008), in this case the 2017) or a defensive fight before being captured. When bite of L. cf. latrans. We cannot confirm the glandular we approached to take photos, the individual of L. cf. compounds were the cause of the release because of the latrans jumped into the marginal vegetation still with disturbance caused by our presence. R. crucifer in the mouth (Fig. 1B), however, after a A recent review by Oliveira et al. (2017) on species few seconds it released the prey and both jumped into of the genus Rhinella being preyed on by Leptodactylus the water. The paratoid glands of R. crucifer released species lists the following interactions: R. granulosa Predation attempt on Rhinella crucifer by Leptodactylus cf. latrans in Brazil 833 by L. podicipinus (Guimarães et al. 2004), R. major by 9(Special Issue 1): S1–S128. L. macrosternum (Souza et al., 2016); and a predation Duellman, W.E., Trueb, L. (1994): Biology of amphibians. 2nd attempt of R. ornate by L. latrans (Bovo et al., 2014). edn. Baltimore and London: Johns Hopkins University Press. Frost, D.R. (2018): Amphibians species of the world: an on line The records of Haddad and Bastos (1997) on the reference. Version 6.0. Eletronic database accessible at: http:// predation of R. crucifer made in São Paulo belong to R. research.amnh.org/herpetology/amphibia/index.html. American ornata (Thomé et al., 2004). Museum of Natural History, New York, USA. Accessed on 09 One of the reasons why and R. crucifer March 2018. have been reported only from predation attempts and Haddad, C.F.B., Bastos, R.P (1997): Predation on the toad Bufo not successful ingestion may be related to a large size crucifer during reproduction (Anura: Bufonidae). Amphibia- of the paratoid glands, which may hinder the predation Reptilia 18: 295-298. process. In R. granulosa and R. major the paratoid glands Heyer, R., Langone, J., La Marca, E., Azevedo-Ramos, C., di Tada, I., Baldo, D., Lavilla, E., Scott, N., Aquino, L., Hardy, J. (2010): are much less developed than in the two aforementioned Leptodactylus latrans. The IUCN Red List of Threatened species. Although Leptodactlyus cf. latrans it is Species 2010: e.T57151A11592655. http://dx.doi.org/10.2305/ considered a generalist species (Sanabria et al., 2005; IUCN.UK.2010-2.RLTS.T57151A11592655.en. Accessed on Solé et al., 2009), amphibians as food items have little 13 March 2018. representativeness in it’s diet (Pazinato et al. 2011). Guimarães, L.D., Pinto, R. M., Juliano, R. F. (2004): Bufo The record of attempted predation of Leptodactylus cf. granulosus (NCN). Predation. Herpetological Review 35: 259. latrans on Trachycephalus mesophaeus (Mira-Mendes Jared, C., Antoniazzi, M.M., Jordão, A.E.C., Silva, J.R.M.C., et al., 2012) suggests that this leptodactylid may Greven, H., Rodrigues, M.T. (2009): Parotoid macroglands in toad (): Their structure and functioning in passive be resistant to the toxins of at least some amphibian defence. Toxicon 54: 197–207. species. However, we cannot reject the hypothesis that Jared, C., Antoniazzi, M.M., Verdade, V.K., Toledo, L.F., toxins are an important factor in preventing predation, Rodrigues, M.T. (2011): The amazonian toad Rhaebo guttatus is since the predation event was not monitored until the able to voluntarily squirt poison frog the paratoid macroglands. end. We suggest that experimental studies on the Amphibia-Reptilia 32: 546–549. tolerance of anuran toxins by Leptodactylus cf. latrans Jared, C., Mailho-Fontana, P.L., Antoniazzi, M.M., Mendes, should be conducted to allow a better understanding of V.A., Barbaro, K.C., Rodrigues, M.T., Brodie Jr, E.D. (2015): the predator-prey relationships involving this species. Venomous frogs use heads as weapons. Current Biology 25(16): 2166–2170. Mira Mendes, C.V., Ruas, D.S., Solé, M. (2012): Predation attempt Acknowledgements. We thank Mirco Solé and Paulo Roberto of Trachycephalus mesophaeus (Hylidae) by Leptodactylus cf. Melo-Sampaio for English revision and their comments on the latrans (Leptodactylidae). Herpetology Notes 5: 163–164 draft of the manuscript. 2RP is supported by a MSc. scholarship Oliveira, S.R., Fachi, M.B., Silva, D.A., Morais, A.R. (2017): provided by the Programa de Alianzas para la Educación y la Predation on Rhinella mirandaribeiroi (Gallardo, 1965) (Anura; Capacitación de la Organización de Estados Americanos y Grupo Bufonidae) by a Neotropical snake, including a list with Coimbra de Universidades Brasileras (PAEC OEA-GCUB) and predation events of the genus Rhinella. Herpetology Notes 10: Coordenação de Aperfeiçoamento de Pessoal de Nível Superior 151–155. (Capes). CVMM thanks Coordenação de Aperfeiçoamento de Pazinato, D.M.L., Trindade, A.O., Oliveira, S.V., Cappellari, L.M. Pessoal de Nível Superior – CAPES for the fellowship (process (2011): Dieta de Leptodactylus latrans (Steffen, 1815) na Serra PNPD/1682788). do Sudeste, Rio Grande do Sul, Brasil. Biotemas 24: 147–151. Rollins-Smith, L. A., Reinert, L. K., O’Leary, C.J., Houston, L. 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Accepted by Javier Cortés Suárez