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Anurans exhibit several defensive behaviors, including sound emission (e.g. release calls and agonistic calls) and visual displays, such as thanatosis and stiff-legged (Duellman and Trueb 1986, Toledo et al. 2011). The last one is characterized by a posture with the legs stiff and back extended, remaining the individual static in this position for a few minutes after the disturbance caused by a potential predator (Sazima 1978, Schlüter and Salas 1991, Bertoluci et al. 2007).
This behavior is mainly known for groups that inhabit forests: species of the genera Proceratophrys, Macrogenioglottus, Odontophrynus (Odontophrynidae), Scythrophrys (Leptodactylidae), Arcovomer, and Ctenophryne (Microhyliade) (Toledo and Zina 2004, Menin and Rodrigues 2007, Giaretta and Martins 2009, Maffei and Ubaid 2016, Mira-Mendes et al. 2016, Rolim 2017, Borteiro et al. 2018). However, the stiff-legged behavior was also recorded for species that are typical of non-forested environments, such as the toads Rhinella granulosa (Spix, 1824) and R. pygmaea (Myers and Carvalho, 1952) (Mângia and Santana 2013, Figueiredo-de-Andrade and Silveira 2018), both from the R. granulosa species group (Narvaes and Rodrigues 2009). In this note, we report two cases of stiff-legged behavior in additional species of the R. granulosa species group.
On 23 November 2017, we observed a male individual of Rhinella bergi (Céspedez, 2000) in a Chacoan area, in the Porto Murtinho municipality (21°41 South, 57°44 West), Mato Grosso do Sul state, Brazil. When we handled the specimen, at approximately 21:00h, it exhibited the stiff-legged defensive behavior (Fig. 1a). Right after we placed the individual on the floor, it continued exhibiting the behavior, keeping the hind limbs stretched and back extended, with the body flattened dorso-ventrally. The second record was registered on 19 December 2018, in the São Gonçalo do Pará municipality (19°59 South, 44°51West), Minas Gerais state, Brazil. We collected a male individual of R. mirandaribeiroi (Gallardo, 1965), which exhibited the same stiff-legged behavior, while being handled (Fig. 1b). We collected both specimens and housed at the Zoological Collection of the Federal University of Mato Grosso do Sul (ZUFMS-AMP13336; ZUFMS-AMP13283; collection permits: SISBio 45889-1).
Figure 1 Specimens of Rhinella displaying stiff-legged behavior. a Adult male of Rhinella bergi (MAP4018), captured in Porto Murtinho municipality, Mato Grosso do Sul state, Brazil. b Adult male of Rhinella mirandaribeiroi (MAP5768), captured in São Gonçalo do Pará municipality, Minas Gerais state, Brazil.
The defensive stiff-legged behavior is usually combined with the anuran cryptic coloration resembling dead leaves (Toledo et al. 2011). Nevertheless, both species recorded in the present study have terrestrial habits and inhabit open areas (Narvaes and Rodrigues 2009). Rhinella bergi occurs in Chaco regions of Paraguay, northwestern Argentina and Mato Grosso do Sul in Brazil (Céspedez 2000), while R. mirandaribeiroi occurs in Cerrado areas of Brazil, in the Noel Kempff National Park, Bolivia, and in Cerrado enclaves within the Amazon Forest (Narvaes and Rodrigues 2009, Melo et al. 2013).
Table 1 Records of stiff-legged behavior for Brazilian anuran species from forest environments and open areas.
| Taxon | Habitat | References |
|---|---|---|
| Bufonidae | ||
| Dendrophryniscus berthalutzae Izecksohn, 1994 | Forest-floor | Toledo et al. 2011 |
| Dendrophryniscus brevipollicatus Jiménez de la Espada, 1870 | Forest-floor | Bertoluci et al. 2007 |
| Dendrophryniscus carvalhoi Izecksohn, 1994 | Forest-floor | Cassimiro et al. 2010 |
| Dendrophryniscus leucomystax Izecksohn, 1968 | Forest-floor | Bertoluci et al. 2007 |
| Rhinella bergi (Céspedez, 2000) | Open areas | Present study |
| Rhinella granulosa (Spix, 1824) | Forest-floor | Mângia and Santana 2013 |
| Rhinella marina (Linnaeus, 1758) | Open areas | Ferrante et al. 2020 |
| Rhinella mirandaribeiroi (Gallardo, 1965) | Open areas | Present study |
| Rhinella pygmaea (Myers and Carvalho, 1952) | Open areas | Figueiredo-de-Andrade and Silveira 2018 |
| Craugastoridae | ||
| Euparkerella cochranae Izecksohn, 1988 | Forest-floor | Toledo et al. 2011 |
| Cycloramphidae | ||
| Cycloramphus parvulus (Girard, 1853) | Forest-floor | Rocha et al. 1998 |
| Leptodactylidae | ||
| Paratelmatobius poecilogaster Giaretta and Castanho, 1990 | Forest-floor | Toledo et al. 2011 |
| Physalaemus gracilis (Boulenger, 1883) | Forest-floor | Rocha and Martins 2013 |
| Pleurodema bibroni Tschudi, 1838 | Forest-floor | Kolenc et al. 2009 |
| Scythrophrys sawayae (Cochran, 1953) | Forest-floor | Garcia 1999 |
| Microhylidae | ||
| Arcovomer passarellii Carvalho, 1954 | Forest-floor | Giaretta and Martins 2009 |
| Chiasmocleis ventrimaculata (Andersson, 1945) | Forest-floor | Schlüter and Salas 1991 |
| Ctenophryne geayi Mocquard, 1904 | Forest-floor | Schlüter and Salas 1991, Menin and Rodrigues 2007 |
| Microhyla berdmorei (Blyth, 1856) | Forest-floor | Shahrudin 2014 |
| Stereocyclops incrassatus Cope, 1870 | Forest-floor | Tonini et al. 2011 |
| Stereocyclops parkeri (Wettstein, 1934) | Forest floor | Sazima 1978 |
| Odontophrynidae | ||
| Macrogenioglottus alipioi Carvalho, 1946 | Forest floor | Mira-Mendes et al. 2016 |
| Odontophrynus americanus (Duméril and Bibron, 1841) | Open areas | Maffei and Ubaid 2016, Rolim 2017, Borteiro et al. 2018 |
| Proceratophrys appendiculata (Günther, 1873) | Forest floor | Sazima 1978 |
| Proceratophrys boiei (Wied-Neuwied, 1824) | Forest-floor | Toledo and Zina 2004, Costa et al. 2009 |
| Proceratophrys mantiqueira Mângia, Santana, Cruz and Feio, 2014 | Forest-floor | Moura et al. 2010 (cited as P. melanopogon) |
| Proceratophrys melanopogon (Miranda-Ribeiro, 1926) | Forest-floor | Toledo et al. 2011 |
| Proceratophrys moehringi Weygoldt and Peixoto, 1985 | Forest-floor | Weygoldt 1986 |
| Proceratophrys renalis (Miranda-Ribeiro, 1920) | Forest-floor | de Amorim Peixoto-M et al. 2013, Peixoto et al. 2013 |
Our records add up to five species of open areas exhibiting this defensive strategy (Maffei and Ubaid 2016, Rolim 2017, Borteiro et al. 2018, Figueiredo-de-Andrade and Silveira 2018, Ferrante et al. 2020) (Table 1). Mira-Mendes et al. (2016)) demonstrated the occurrence of this behavior for 23 forest-floor species. Although Pleurodema bibroni Tschudi, 1838 is categorized as a species from the forest-floor in the Mira-Mendes et al. (2016) study, Kolenc et al. (2009) showed that this species also inhabits non-forested environments, suggesting that P. bibroni exhibit the stiff-legged behavior as death feigning function, rather than camouflage.
In total, 29 anuran species from six families show the stiff-legged behavior, with the family Bufonidae having the largest number of species that exhibit this defensive strategy (n=9), from which four species are from open areas (Table 1). Forest species that exhibit the stiff-legged behavior use this strategy to camouflage themselves among the leaves, once they present cryptic coloration, thus avoiding predation (Sazima 1978). With this, we can assume that the species of open areas perform stiff-legged behavior to look like dead body on the ground (death feigning).
