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Defensive Behaviours in the Bahia Forest Frog Macrogenioglottus Alipioi Carvalho, 1946 (Anura: Odontophrynidae), with a Review of the Stiff-Legged Posture

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Defensive Behaviours in the Bahia Forest Frog Macrogenioglottus Alipioi Carvalho, 1946 (Anura: Odontophrynidae), with a Review of the Stiff-Legged Posture Herpetology Notes, volume 9: 91-94 (2016) (published online on 25 March 2016) Defensive behaviours in the Bahia forest frog Macrogenioglottus alipioi Carvalho, 1946 (Anura: Odontophrynidae), with a review of the stiff-legged posture Caio Vinícius de Mira-Mendes1,*, Danilo Silva Ruas1, Indira Castro2, Mirco Solé3 and Julio Ernesto Baumgarten3 Macrogenioglottus alipioi Carvalho, 1946 is a large W, approximately 90–400 m a.s.l.), located in the odontophrynid toad that occurs in the Atlantic Forest municipality of Igrapiúna, southern Bahia, Brazil, we domain from the state of São Paulo to Alagoas (Frost found an adult male of M. alipioi calling in a temporary 2015; Bourgeois 2010). It inhabits the leaf litter of pond inside a forest fragment. We captured the individual preserved forests and can be found calling in temporary to take some photographs and the toad immediately ponds formed on the forest floor after extremely heavy reacted by inflating its body (Figure 1A). After placing rains during explosive breeding events (Abravaya and it back on the forest floor it kept this posture (Figure Jackson 1978). 1B), and when touched, directed its back towards the Amphibians serve as prey for a great variety of animals hand, performing a body-tilting posture (Figure 1C). including vertebrates, as well as some arthropods (Wells Then the toad tried to escape and reacted to our attempt 2007). To avoid being preyed upon, they have evolved to recapture it by flattening its body on the floor and several defensive strategies, which provide protection stretching out its legs (Figure 1D), adopting the posture from potential predators (Duellman and Trueb 1986). called stiff-legged behaviour (sensu Toledo et al. 2011). Among anurans, 31 defensive behaviours were The toad remained in this position for about 10 minutes, recognized by Toledo et al. (2011), mostly associated to and then tried to flee again. remaining motionless or fleeing (Jared et al. 2011). We Puffing-up-the-body is a common behaviour report a sequence of defensive behaviours performed by performed by anurans. It consists of enlarging the body Macrogenioglottus alipioi in an Atlantic forest fragment size by filling the lungs with air (Toledo et al. 2011). in Northeastern Brazil. This increase in size may discourage the predator to On June 06, 2015, at 22.30 h, during fieldwork in the capture it (Williams et al. 2000; Toledo et al. 2011). In Michelin Ecological Reserve (13°49’35” S, 39°08’32” some cases, puffing-up-the-body may be accompanied by other defensive postures, such as body-tilting. This defensive behaviour consists of directing the dorsal part of the body towards the predator (Toledo et al. 2011). In toads with dorsal macroglands, such as M. alipioi, by 1 Graduate Program in Ecology and Biodiversity Conservation, adopting a body-tilting posture the glands would most Universidade Estadual de Santa Cruz, Rodovia Jorge Amado, likely be the first part of the toad’s body that the predator km 16, 45662-900 Ilhéus, Bahia, Brazil would bite. Thus, noxious secretions could come into 2 Graduate Program in Zoology, Universidade Estadual de Santa contact with the mouth of the predator, allowing the Cruz, Rodovia Jorge Amado, km 16, 45662-900 Ilhéus, escape of the toad (Toledo et al. 2011). Bahia, Brazil Stiff-legged behaviour has been reported for forest- 3 Department of Biological Sciences, Universidade Estadual de Santa Cruz, Rodovia Jorge Amado, km 16, 45662-900 floor toads that have cryptic colouration (Toledo et al. Ilhéus, Bahia, Brazil 2011). According to Sazima (1978), this behaviour may * Corresponding author e-mail: [email protected] protect the toad against visually oriented predators, 92 Caio Vinícius de Mira-Mendes et1 al. Table 1. Records of stiff-legged behaviour of amphibian anurans from �������������� 1 Table 1. Records of stiff-legged behaviour of amphibian anurans from forest-floor. Species Family Reference Dendrophryniscus berthalutzae Izecksohn, 1994 Bufonidae Toledo et al. 2011 Dendrophryniscus brevipollicatus Jiménez de la Espada, Bufonidae Bertoluci et al. 2007 1870 Dendrophryniscus leucomystax Izecksohn, 1968 Bufonidae Bertoluci et al. 2007 Dendrophryniscus carvalhoi Izecksohn, 1994 Bufonidae Cassimiro et al. 2010 Rhinella granulosa (Spix, 1824) Bufonidae Mângia and Santana 2013 Euparkerella cochranae Izecksohn, 1988 Craugastoridae Toledo et al. 2011 Zachaenus parvulus (Girard, 1853) Cycloramphidae Rocha et al. 1998 Paratelmatobius poecilogaster Giaretta and Castanho, 1990 Leptodactylidae Toledo et al. 2011 Pleurodema bibroni Tschudi, 1838 Leptodactylidae Kolenc et al. 2009 Scythrophrys sawayae (Cochran, 1953) Leptodactylidae Garcia 1999 Physalaemus gracilis (Boulenger, 1883) Leptodactylidae Rocha and Martins 2013 Arcovomer passarellii Carvalho, 1954 Microhylidae Giaretta and Martins 2009 Chiasmocleis ventrimaculata (Andersson, 1945) Microhylidae Schlüter and Salas 1991 Ctenophryne geayi Mocquard, 1904 Microhylidae Schlüter and Salas 1991; Menin and Rodrigues 2007 Microhyla berdmorei (Blyth, 1856) Microhylidae Shahrudin 2014 Stereocyclops parkeri (Wettstein, 1934) Microhylidae Sazima 1978 Stereocyclops incrassatus Cope, 1870 Microhylidae Tonini et al. 2011 Proceratophrys melanopogon Heyer, Rand, Cruz, Peixoto, Odontophrynidae Moura et al. 2010; Toledo et al. and Nelson, 1990 2011 Proceratophrys boiei (Wied-Neuwied, 1824) Odontophrynidae Toledo and Zina 2004; Costa et al. 2009 Proceratophrys appendiculata (Günther, 1873) Odontophrynidae Sazima 1978 Proceratophrys renalis (Miranda-Ribeiro, 1920) Odontophrynidae Peixoto et al. 2013 Proceratophrys moehringi Weygoldt and Peixoto, 1985 Odontophrynidae Weygoldt, 1986 Macrogenioglottus alipioi Carvalho, 1946 Odontophrynidae Present study 2 such as birds, snakes and mammals that feed on prey In the present study, we described a sequence of which lives in the leaf litter (Bertoluci et al. 2007). defensive behaviours displayed by the Bahia forest The immobility, which in some cases can last up to 30 frog Macrogenioglottus alipioi. Puffing-up-the-body minutes, could favour camouflage of the toad among and body-tilting had been described for M. allipioi by fallen leaves. With our new record for M. alipioi, stiff- Toledo et al. (2011), however, this is the first record legged behaviour has now been recorded in 23 species of stiff-legged behaviour for this species. According of forest-floor toads belonging to six different families to Toledo et al. (2011), the combination of different (Table 1), corroborating that this posture may have defensive strategies could result in higher chances of the evolved convergently among unrelated frog groups, as toad avoiding or escaping a potential predator. suggested by Sazima (1978). Defensive behaviours in the Bahia forest frog 93 Figure 1. Sequence of defensive behaviours displayed by Macrogenioglottus alipioi in northeastern Brazil. A) Puffing-up-the- body after handling. B) Puffing-up-the-body in frontal view. C) Body-tilting behaviour. D) Stiff-legged behaviour. Acknowledgements. We thank the Center for Biodiversity Macrogenioglottus alipioi Carvalho, 1946: Distribution Studies of the Michelin Ecological Reserve for logistical and extension, state of Alagoas, northeastern Brazil. Check list 6: financial support; Fabio Falcão, Francisco F.R. Oliveira and 187–188. Amanda S. F. Lantyer Silva for comments on the manuscript; Cassimiro, J., Verdade, V.K., Rodrigues, M.T. (2010): C.V.M.M. thanks Fernanda Tonolli for her patience, affection Dendrophryniscus carvalhoi (Carvalho’s Tree Toad). Defensive and eternal loving support. behavior. Herpetological Review 41: 472. Costa, P.N., Silva-Soares, T., Bernstein, L.B. (2009): Defensive References behaviour of Proceratophrys boiei (Wied-Neuwied, 1824) (Amphibia, Anura, Cycloramphidae). petology Notes 2: Abravaya, P., J. F. Jackson. (1978): Reproduction in 227-229. Macrogenioglottus alipioi Carvalho (Anura, Leptodactylidae). Duellman, W. E., Trueb, L. (1994): Biology of amphibians. Second Contributions in Science, Natural History Museum of Los edition. Baltimore, John Hopkins University. Angeles County 298: 1–9. Frost, D. R. (2015): Amphibian Species of the World: an Online Bertoluci, J., Brassaloti, R. A., Sawakuchi, H. O., Ribeiro JR., Reference. Version 6.0 (Date of access). Electronic Database J. W. & Woehl JR., G. (2007): Defensive behavior with stiff- accessible at http://research.amnh.org/herpetology/ amphibia/ legged posture in the Brazilian tree toads Dendrophryniscus index.html. American Museum of Natural History, New York, brevipollicatus and D. leucomystax (Anura, Bufonidae). Alytes. USA. 25:1-2. Garcia, P. C. A. (1999): Scythrophrys sawayae. (NCN). Defensive Bourgeois, P.A. (2010): Amphibia, Anura, Cycloramphidae, behavior. Herpetological Review 30: 224. 94 Caio Vinícius de Mira-Mendes et al. Giaretta, A., Martins, L. (2009): Notes on the call and behavior Shahrudin, S. (2014): Defensive Behaviour of Microhyla berdmorei of Arcovomer passarellii (Anura: Microhylidae). Herpetology (Blyth, 1856) (Anura: Microhylidae) from Peninsular Malaysia. Notes 2: 91-93. Herpetology Notes 7: 787-789. Jared, C., Antoniazzi, M.M., Verdade, V.K., Sciani, J.M., Pimenta, Toledo, L.F., Sazima, I., Haddad, C.F.B. (2011): Behavioural D.C., Toledo, L.F., Rodrigues, M.T. (2011): The Amazonian defences of anurans: an overview. Ethology Ecology & toad Rhaebo guttatus is able to voluntarily squirt poison from Evolution 23: 1-25. the paratoid macroglands. Amphibia-Reptilia 32: 546–549. Toledo, L.F., Zina, J.P. (2004): Proceratophrys boiei (Smooth Kolenc,
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