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Bromelicolous Habit of Three Species of Rhinella Fitzinger, 1826 (Anura: Bufonidae) in Northeastern Brazil’S Atlantic Forest

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Bromelicolous Habit of Three Species of Rhinella Fitzinger, 1826 (Anura: Bufonidae) in Northeastern Brazil’S Atlantic Forest Herpetology Notes, volume 14: 903-906 (2021) (published online on 24 June 2021) Bromelicolous habit of three species of Rhinella Fitzinger, 1826 (Anura: Bufonidae) in Northeastern Brazil’s Atlantic Forest Ubiratã Ferreira Souza1,*, Alan Pedro de Araújo2,3, Alcina Gabriela Maria Medeiros da Fonsêca Santos1, and Marcos Jorge Matias Dubeux4 Understanding habitat types and how organisms bromeliads for breeding can still use them as shelter (i.e., make use of them, is crucial for identifying factors bromelicolous; sensu Peixoto, 1995). Bromelicolous that determine species distribution and community habit can be recurrent (e.g., Scinax pachycrus [Araújo composition (Kopp and Eterovick, 2006; Pittman et et al., 2020], Nyctimantis brunoi [Peixoto, 1995]) or al., 2014). The phytotelmata are plant structures that opportunistic – when the anuran uses this phytotelm accumulate rainwater (e.g., bromeliad tanks, tree holes, occasionally (Peixoto, 1995; Andrade et al., 2009). bamboo internodes, axils and floral bracts; see Kitching, Among the four genera of bufonids occurring in 2000). Such structures provide microhabitats for fungi, the Brazilian Atlantic Forest (Segalla et al., 2019), microalgae, and both invertebrate and vertebrate Dendrophryniscus Jiménez-de-la-Espada, 1870, animals (Maguire, 1971; Ramos et al., 2018, 2019). The Frostius Cannatella, 1986 and Melanophryniscus plants of the Bromeliaceae family are the most common Gallardo, 1961 have strong association with phytotelm phytotelm across the Neotropical region (Ulloa-Ulloa environments, including bromeligenous species (Cruz et al., 2017), being used for shelter, foraging and/or and Peixoto, 1982; Haddad and Prado, 2005; Kwet et reproduction (Pugliese et al., 2009; Nunes et al., 2012). al., 2005; Wells, 2007; Langone et al., 2008; Dias et al., Among Neotropical anurans, more than 168 known 2016; Sabagh et al., 2017). However, for more than 90 species use bromeliad phytotelm habitats (Peixoto, Rhinella species, information about the use of specific 1995; Tonini et al., 2020), of which >100 depend on habitats is still scarce, and in most cases, they are bromeliads for reproduction (i.e., bromeligenous; regarded as habitat generalists (Duellman and Trueb, Tonini et al., 2020). This number is increasing following 1994; Sabagh and Carvalho-e-Silva, 2008). Some species recent descriptions of new species (Sabagh et al., 2017; have terrestrial habits, whereas others demonstrate Vörös et al., 2017; Orrico et al., 2018; Folly et al., 2018; semiarboreal habits and are found in human-altered Dias et al., 2020). Nevertheless, species that do not use habitats, open areas, as well as in the interior and edges of forest remnants (Roberto et al., 2011; Dubeux et al., 2019; Frost, 2020). Herein, we report the bromelicolous habit of three species of Rhinella from the northern region of the Atlantic Forest, Brazil. 1 Laboratório de Estudos Herpetológicos e Paleoherpetológicos, Departamento de Biologia, Universidade Federal Rural de In the Estação Ecológica de Tapacurá (8.0368ºS, Pernambuco, Rua Dom Manoel de Medeiros s/n, Recife, 35.2018ºW; WGS84, 200 m elevation), municipality 52171-900 Pernambuco, Brazil. of São Lourenço da Mata, Pernambuco state, Brazil, 2 Departamento de Ecologia, Laboratório de Herpetologia e we found a Rhinella granulosa (Spix, 1824) adult Comportamento Animal, Universidade Federal de Goiás, Av. on 4 February 2018 (dry season) at 18:00 h; and two Esperança s/n, Goiânia, 74690-900 Goiás, Brazil. Rhinella jimi (Stevaux, 2002) adults on 15 June 2018 3 Projeto Bromeligenous, Instituto de Pesquisa, Ensino e (rainy season) at 20:00 h (Fig. 1A–B). These frogs were Preservação Ambiental Marcos Daniel, Rua Fortunato Ramos in the basal axils of an Aechmea leptantha (Harms) 123, Santa Lúcia, Vitória, 29056-020 Espírito Santo, Brazil. 4 Laboratório de Herpetologia, Departamento de Zoologia, Leme & amp; J.A. Siqueira on a rocky outcrop. In the Universidade Federal de Pernambuco, Av. Prof. Moraes Rego Jardim Botânico do Recife (8.0748ºS, 34.9616ºW; 1 m 1235, Recife, 50670-901 Pernambuco, Brazil. elevation), municipality of Recife, Pernambuco state, * Corresponding author. E-mail: Brazil, we found two R. granulosa adults sharing the [email protected] same basal axil of Aechmea aquilega (Salisb) Griseb © 2021 by Herpetology Notes. Open Access by CC BY-NC-ND 4.0. (Fig. 1C) on 24 November 2018 (dry season) at 11:00 h. 904 Ubiratã Ferreira Souza et al. The bromeliad was in the sandy soil next to a bromeliad municipality of Quebrangulo, Alagoas state, Brazil, we cluster of the same species. In the Estação Ecológica found a R. crucifer adult in a basal axil of A. leptantha de Murici (9.2263ºS, 35.8978ºW; 387 m elevation), (Fig. 1E) on 21 April 2019 (dry season) at 17:30 h. The municipality of Murici, Alagoas state, Brazil, we found nearest bromeliad was two meters away and was part of a Rhinella crucifer (Wied-Neuwied, 1821) adult in A. leptantha cluster. a basal axil of A. leptantha (Fig. 1D, F) on 15 March In general, Rhinella species have reproductive mode 2019 (dry season) at 14:26 h. This bromeliad was found “type 1”, where eggs are deposited directly in the water in a cluster (~2 m diameter) on a rocky outcrop near and tadpoles develop in lentic environments, such a grassland area. In the Reserva Biológica de Pedra as permanent and temporary ponds (sensu Haddad Talhada (9.2550ºS, 36.4269ºW; 771 m elevation), and Prado, 2005). Nevertheless, there are records of Figure 1. Bromelicolous habit of Rhinella species in the northern region of the Atlantic Forest. (A) and (B) = R. diptycha; (C) = R. granulosa; (D) and (E) = R. crucifer; (F) = cluster of the bromeliad Aechmea leptantha. Photos by Alan Araújo (A and B), Alcina Santos (C) and Marcos Dubeux (D, E, F). Bromelicolous habit of three species of Rhinella, Atlantic Forest, Brazil 905 bromelicolous habits in Rhinella species from Restinga C., Recoder, R.S, et al. (2020): A new large canopy-dwelling habitats of the Atlantic forest (R. pygmaea [Peixoto, species of Phyllodytes Wagler, 1930 (Anura, Hylidae) from the 1995] and R. crucifer [Ferreira and Teixeira, 2009; Atlantic Forest of the state of Bahia, Northeastern Brazil. PeerJ 8: e8642. Mageski et al., 2017]) and from the semiarid ecoregion Dubeux, M.J.M., Palmeira, C.N.S., Gonçalves, U., Vieira, R.T.A., of the Caatinga (R. granulosa and R. diptycha [Ribeiro Araújo, L.W.L. (2019): Rhinella jimi (Cururu Frog). Arboreality. et al., 2012, Protázio et al., 2013]). Thus, it is likely Herpetological Review 50(4): 764. that the use of bromeliads by Rhinella is related Duellman, W.E., Trueb, L. (1994): Biology of Amphibians. The to the availability of humid shelter and/or feeding John Hopkins University Press, Baltimore, USA, 670 pp. environments. Ferreira, R.B., Teixeira, R.L. (2009): Feeding pattern and use of reproductive habitat of the Striped toad Rhinella crucifer (Anura: According to the records presented here, the Bufonidae) from Southeastern Brazil. Acta Herpetologica 4(2): bromelicolous habit in Rhinella is more common during 125–34. the dry season, which in the northern region of the Finlay, B.J., Frank, J.H., Lounibos, L.P. (1984): Phytotelmata: Atlantic Forest corresponds to the months of October Terrestrial Plants as Hosts for Aquatic Insect Communities. to March (Hijmans et al., 2005; Alvarez et al., 2013). Journal of Animal Ecology 53(2): 698–699. It follows the pattern already found for opportunistic Folly, M., Hepp, F., Carvalho-e-Silva, S.P. (2018): A New bromelicolous species, where individuals tend to use Bromeligenous Species of Fritziana Mello-Leitão, 1937 (Amphibia: Anura: Hemiphractidae) from High Elevations in these more humid environments during the dry season the Serra Dos Órgãos, Rio de Janeiro, Brazil. Herpetologica to avoid desiccation and for protection against possible 74(1): 58–72. predators (Peixoto, 1995; Ferreira and Teixeira, 2009; Frost, D.R. (2020): Amphibian Species of the World: Online Protázio et al., 2013). These new records reinforce that Reference. Version 6.0. http://research.amnh.org/herpetology/ the bromelicolous habit of Rhinella may be an alternative amphibia/index.php. Accessed on 30 July 2020. strategy to avoid dehydration in environments with dry Gilbert, K.J., Bittleston, L.S., Naive, M.A.K., Kiszewski, A.E., Buenavente, P.A.C., Lohman, D.J., Pierce, N.E. (2020): season (Andrade et al., 2009; Alvarez et al., 2013). Investigation of an elevational gradient reveals strong differences between bacterial and eukaryotic communities coinhabiting Acknowledgements. The authors thank the Instituto Chico nepenthes phytotelmata. Microbial Ecology 80: 334–349. Mendes de Conservação da Biodiversidade – REBIO de Pedra Haddad, C.F.B., Prado, C.P.A. (2005): Reproductive modes in Talhada and ESEC de Murici for logistical support; Dr. Jefferson frogs and their unexpected diversity in the Atlantic Forest of Pimentel from Jardim Botânico do Recife for identifying the Brazil. BioScience 55: 207–217. bromeliad species; Dr. Ralph Lacerda de Albuquerque and Dr. Hijmans, R.J., Cameron, S.E., Parra, J.L., Jones, P.G., Jarvis, A. Marcelo Nogueira de Carvalho Kokubum for reviewing the text; (2005): Very high resolution interpolated climate surfaces for Ms. Rebecca Umeed for English editing; ICMBio for sampling global land areas. International Journal of Climatology, 25(15): permits (ICMBio/SISBio 57241-1 and 66127). MJMD thanks 1965–1978. FACEPE (IBPG-1117-2.04/19) for financial support. Kitching, R.L. (2000): Food webs and container habitats: the natural history and ecology of phytotelmata. Cambridge University References Press, Cambridge, UK, 432 pp. Kopp, K., Eterovick, P.C. (2006): Factors influencing spatial and Alvares, C.A., Stape, J.L., Sentelhas, P.C., Gonçalves, J.L.M., temporal structure of frog assemblages at ponds in southeastern Sparovek, G. (2013): Köppen’s climate classification map for Brazil. Journal of Natural History 40(29–31): 1813–1830. Brazil. Meteorologische Zeitschrift 22(6): 711–728. Kwet, A., Maneyro, R., Zillikens, A., Mebs, D. (2005): Andrade, E.V.E., Albertin, M., Moura, G.J.B (2009): Primeiro Advertisement calls of Melanophryniscus dorsalis (Mertens, registro do uso de Bromeliaceae por Elachistocleis ovalis 1933) and M.
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