Bromelicolous habit of three species of Rhinella Fitzinger ...

Understanding habitat types and how organisms make use of them, is crucial for identifying factors that determine species distribution and community composition (Kopp and Eterovick, 2006; Pittman et al., 2014). The phytotelmata are plant structures that accumulate rainwater (e.g., bromeliad tanks, tree holes, bamboo internodes, axils and floral bracts; see Kitching, 2000). Such structures provide microhabitats for fungi, microalgae, and both invertebrate and vertebrate animals (Maguire, 1971; Ramos et al., 2018, 2019). The plants of the Bromeliaceae family are the most common phytotelm across the Neotropical region (Ulloa-Ulloa et al., 2017), being used for shelter, foraging and/or reproduction (Pugliese et al., 2009; Nunes et al., 2012).

Among Neotropical anurans, more than 168 known species use bromeliad phytotelm habitats (Peixoto, 1995; Tonini et al., 2020), of which >100 depend on bromeliads for reproduction (i.e., bromeligenous; Tonini et al., 2020). This number is increasing following recent descriptions of new species (Sabagh et al., 2017; Vörös et al., 2017; Orrico et al., 2018; Folly et al., 2018; Dias et al., 2020). Nevertheless, species that do not use

bromeliads for breeding can still use them as shelter (i.e., bromelicolous; sensu Peixoto, 1995). Bromelicolous habit can be recurrent (e.g., Scinax pachycrus [Araújo et al., 2020], Nyctimantis brunoi [Peixoto, 1995]) or opportunistic – when the anuran uses this phytotelm occasionally (Peixoto, 1995; Andrade et al., 2009).

Among the four genera of bufonids occurring in the Brazilian Atlantic Forest (Segalla et al., 2019), Dendrophryniscus Jiménez-de-la-Espada, 1870, Frostius Cannatella, 1986 and Melanophryniscus Gallardo, 1961 have strong association with phytotelm environments, including bromeligenous species (Cruz and Peixoto, 1982; Haddad and Prado, 2005; Kwet et al., 2005; Wells, 2007; Langone et al., 2008; Dias et al., 2016; Sabagh et al., 2017). However, for more than 90 Rhinella species, information about the use of specific habitats is still scarce, and in most cases, they are regarded as habitat generalists (Duellman and Trueb, 1994; Sabagh and Carvalho-e-Silva, 2008). Some species have terrestrial habits, whereas others demonstrate semiarboreal habits and are found in human-altered 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.

In the Estação Ecológica de Tapacurá (8.0368ºS, 35.2018ºW; WGS84, 200 m elevation), municipality of São Lourenço da Mata, Pernambuco state, Brazil, we found a Rhinella granulosa (Spix, 1824) adult on 4 February 2018 (dry season) at 18:00 h; and two Rhinella jimi (Stevaux, 2002) adults on 15 June 2018 (rainy season) at 20:00 h (Fig. 1A–B). These frogs were in the basal axils of an Aechmea leptantha (Harms) Leme & amp; J.A. Siqueira on a rocky outcrop. In the Jardim Botânico do Recife (8.0748ºS, 34.9616ºW; 1 m elevation), municipality of Recife, Pernambuco state, Brazil, we found two R. granulosa adults sharing the same basal axil of Aechmea aquilega (Salisb) Griseb (Fig. 1C) on 24 November 2018 (dry season) at 11:00 h.

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

1 Laboratório de Estudos Herpetológicos e Paleoherpetológicos, Departamento de Biologia, Universidade Federal Rural de Pernambuco, Rua Dom Manoel de Medeiros s/n, Recife, 52171-900 Pernambuco, Brazil.

2 Departamento de Ecologia, Laboratório de Herpetologia e Comportamento Animal, Universidade Federal de Goiás, Av. Esperança s/n, Goiânia, 74690-900 Goiás, Brazil.

3 Projeto Bromeligenous, Instituto de Pesquisa, Ensino e Preservação Ambiental Marcos Daniel, Rua Fortunato Ramos 123, Santa Lúcia, Vitória, 29056-020 Espírito Santo, Brazil.

4 Laboratório de Herpetologia, Departamento de Zoologia, Universidade Federal de Pernambuco, Av. Prof. Moraes Rego 1235, Recife, 50670-901 Pernambuco, Brazil.

* Corresponding author. E-mail: [email protected]

© 2021 by Herpetology Notes. Open Access by CC BY-NC-ND 4.0.

Ubiratã Ferreira Souza et al.904

The bromeliad was in the sandy soil next to a bromeliad cluster of the same species. In the Estação Ecológica de Murici (9.2263ºS, 35.8978ºW; 387 m elevation), municipality of Murici, Alagoas state, Brazil, we found a Rhinella crucifer (Wied-Neuwied, 1821) adult in a basal axil of A. leptantha (Fig. 1D, F) on 15 March 2019 (dry season) at 14:26 h. This bromeliad was found in a cluster (~2 m diameter) on a rocky outcrop near a grassland area. In the Reserva Biológica de Pedra Talhada (9.2550ºS, 36.4269ºW; 771 m elevation),

municipality of Quebrangulo, Alagoas state, Brazil, we found a R. crucifer adult in a basal axil of A. leptantha (Fig. 1E) on 21 April 2019 (dry season) at 17:30 h. The nearest bromeliad was two meters away and was part of A. leptantha cluster.

In general, Rhinella species have reproductive mode “type 1”, where eggs are deposited directly in the water and tadpoles develop in lentic environments, such as permanent and temporary ponds (sensu Haddad 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 habits in Rhinella species from Restinga habitats of the Atlantic forest (R. pygmaea [Peixoto, 1995] and R. crucifer [Ferreira and Teixeira, 2009; Mageski et al., 2017]) and from the semiarid ecoregion of the Caatinga (R. granulosa and R. diptycha [Ribeiro et al., 2012, Protázio et al., 2013]). Thus, it is likely that the use of bromeliads by Rhinella is related to the availability of humid shelter and/or feeding environments.

According to the records presented here, the bromelicolous habit in Rhinella is more common during the dry season, which in the northern region of the Atlantic Forest corresponds to the months of October to March (Hijmans et al., 2005; Alvarez et al., 2013). It follows the pattern already found for opportunistic bromelicolous species, where individuals tend to use these more humid environments during the dry season to avoid desiccation and for protection against possible predators (Peixoto, 1995; Ferreira and Teixeira, 2009; Protázio et al., 2013). These new records reinforce that the bromelicolous habit of Rhinella may be an alternative strategy to avoid dehydration in environments with dry season (Andrade et al., 2009; Alvarez et al., 2013).

Acknowledgements. The authors thank the Instituto Chico Mendes de Conservação da Biodiversidade – REBIO de Pedra Talhada and ESEC de Murici for logistical support; Dr. Jefferson Pimentel from Jardim Botânico do Recife for identifying the bromeliad species; Dr. Ralph Lacerda de Albuquerque and Dr. Marcelo Nogueira de Carvalho Kokubum for reviewing the text; Ms. Rebecca Umeed for English editing; ICMBio for sampling permits (ICMBio/SISBio 57241-1 and 66127). MJMD thanks FACEPE (IBPG-1117-2.04/19) for financial support.

References

Alvares, C.A., Stape, J.L., Sentelhas, P.C., Gonçalves, J.L.M., Sparovek, G. (2013): Köppen’s climate classification map for Brazil. Meteorologische Zeitschrift 22(6): 711–728.

Andrade, E.V.E., Albertin, M., Moura, G.J.B (2009): Primeiro registro do uso de Bromeliaceae por Elachistocleis ovalis (Schneider, 1799) (Anura: Microhylidae). Biota Neotropica 9(4): 257–259.

Araújo, A.P., Marques, A.H.C., Dantas, A.P., Junior, M.M., Moura, G.J.B., Tinoco, M.S. (2020): Assisted phoresy of invertebrates by anurans in tank bromeliads: interspecific relationship. Aquatic Sciences 82: 1–11.

Cruz, C.A.G., Peixoto, O.L. (1982): Sobre a biologia de Atelopus pernambucensis Bokermann, 1962 (Amphibia, Anura, Bufonidae). Revista Brasileira de Biologia 42: 627–629.

Dias, E.G., Silva, P.S., Pereira, E.N., Santos, E.M. (2016): Frostius pernambucensis (Frost’s Toad). Parental care. Herpetological Review 47: 277–278.

Dias, I.R., Novaes-e-Fagundes, G., Mollo-Neto, A., Zina, J., Garcia,

C., Recoder, R.S, et al. (2020): A new large canopy-dwelling species of Phyllodytes Wagler, 1930 (Anura, Hylidae) from the Atlantic Forest of the state of Bahia, Northeastern Brazil. PeerJ 8: e8642.

Dubeux, M.J.M., Palmeira, C.N.S., Gonçalves, U., Vieira, R.T.A., Araújo, L.W.L. (2019): Rhinella jimi (Cururu Frog). Arboreality. Herpetological Review 50(4): 764.

Duellman, W.E., Trueb, L. (1994): Biology of Amphibians. The John Hopkins University Press, Baltimore, USA, 670 pp.

Ferreira, R.B., Teixeira, R.L. (2009): Feeding pattern and use of reproductive habitat of the Striped toad Rhinella crucifer (Anura: Bufonidae) from Southeastern Brazil. Acta Herpetologica 4(2): 125–34.

Finlay, B.J., Frank, J.H., Lounibos, L.P. (1984): Phytotelmata: Terrestrial Plants as Hosts for Aquatic Insect Communities. Journal of Animal Ecology 53(2): 698–699.

Folly, M., Hepp, F., Carvalho-e-Silva, S.P. (2018): A New Bromeligenous Species of Fritziana Mello-Leitão, 1937 (Amphibia: Anura: Hemiphractidae) from High Elevations in the Serra Dos Órgãos, Rio de Janeiro, Brazil. Herpetologica 74(1): 58–72.

Frost, D.R. (2020): Amphibian Species of the World: Online Reference. Version 6.0. http://research.amnh.org/herpetology/amphibia/index.php. Accessed on 30 July 2020.

Gilbert, K.J., Bittleston, L.S., Naive, M.A.K., Kiszewski, A.E., Buenavente, P.A.C., Lohman, D.J., Pierce, N.E. (2020): Investigation of an elevational gradient reveals strong differences between bacterial and eukaryotic communities coinhabiting nepenthes phytotelmata. Microbial Ecology 80: 334–349.

Haddad, C.F.B., Prado, C.P.A. (2005): Reproductive modes in frogs and their unexpected diversity in the Atlantic Forest of Brazil. BioScience 55: 207–217.

Hijmans, R.J., Cameron, S.E., Parra, J.L., Jones, P.G., Jarvis, A. (2005): Very high resolution interpolated climate surfaces for global land areas. International Journal of Climatology, 25(15): 1965–1978.

Kitching, R.L. (2000): Food webs and container habitats: the natural history and ecology of phytotelmata. Cambridge University Press, Cambridge, UK, 432 pp.

Kopp, K., Eterovick, P.C. (2006): Factors influencing spatial and temporal structure of frog assemblages at ponds in southeastern Brazil. Journal of Natural History 40(29–31): 1813–1830.

Kwet, A., Maneyro, R., Zillikens, A., Mebs, D. (2005): Advertisement calls of Melanophryniscus dorsalis (Mertens, 1933) and M. montevidensis (Philippi, 1902), two parapatric species from southern Brazil and Uruguay, with comments on morphological variation in the Melanophryniscus stelzneri group (Anura: Bufonidae). Salamandra 41: 3–20.

Langone, J.A., Segalla, M.V., Bornschein, M.R., de-Sá, R.O. (2008): A new reproductive mode in the genus Melanophryniscus Gallardo, 1961 (Anura: Bufonidae) with description of a new species from state of Paraná, Brazil. South American Journal of Herpetology 3: 1–9.

Lopez, L.C.S., Alves, R.R.D.N., Rios, R.I. (2009): Micro-environmental factors and the endemism of bromeliad aquatic Fauna. Hydrobiologia 625: 151–156.

Mageski, M., Ferreira, R.B., Costa, L.C.D., Jesus, P.R., Ferreira, P.D. (2017): Frog assemblage associated with bromeliads in a

Bromelicolous habit of three species of Rhinella, Atlantic Forest, Brazil 905

Accepted by Clarissa Canedo

sandy coastal plain in the state of Espírito Santo, southeastern Brazil. Papéis Avulsos de Zoologia 57(34): 445–449.

Maguire, B. (1971): Phytotelmata biota and community structure determination in plant-held waters. Annual Review of Ecology, Evolution, and Systematics 2: 439–464.

Nunes, I., Kwet, A. Pombal-Jr, J.P. (2012): Taxonomic revision of the Scinax alter species complex (Anura: Hylidae). Copeia 3: 554–569.

Orrico, V.G D., Dias, I.R., Marciano-Jr, E. (2018): Another new species of Phyllodytes (Anura: Hylidae) from the Atlantic Forest of northeastern Brazil. Zootaxa 4407(1): 101–110.

Peixoto, O.L. (1995): Associação de anuros a bromeliáceas na Mata Atlântica. Revista da Universidade Rural, Série Ciências da Vida 17: 75–83.

Pittman, S.E., Osbourn, M.S., Semlitsch, R.D. (2014): Movement ecology of amphibians: a missing component for understanding population declines. Biological Conservation 169: 44–53.

Protázio, A.S., Protázio, A.S., Ribeiro, E.S., Nogueira, E.M.S., Moura, G.J.B. (2013): The role of bromeliad architecture and abiotic factors in occupation by anurans. Neotropical Biology and Conservation 8(2): 88–95.

Pugliese, A., Baêta, D., Pombal-Jr., J.P. (2009): A new species of Scinax (Anura: Hylidae) from rocky montane fields in southeastern and central Brazil. Zootaxa 2269: 53–64.

Ramos, G.J.P., Moura, C.W.N. (2019): Algae and cyanobacteria in phytotelmata: diversity, ecological aspects, and conservation. Biodiversity and conservation 28(7): 1667–1697.

Ramos, G.J.P., Santana, L.M., Medina, A.M., Bicudo, C.E.D.M., Branco, L.H.Z., Moura, C.W.D.N. (2018): Unraveling algae and cyanobacteria biodiversity in bromeliad phytotelmata in different vegetation formations in Bahia State, Northeastern Brazil. Acta Botanica Brasilica 32(4): 567–577.

Ribeiro, E.S., Moura, G.J.B., Protázio, A.S., Protázio, A.S., Nogueira, E.M.S. (2012): Associação entre anfíbios anuros e Aechmea aquilega (Salisb) Griseb, (Bromeliaceae) na Ilha do Urubu, Paulo Afonso, Bahia. In: Biodiversidade da Caatinga do submédio e baixo São Francisco, Salvador, p. 65–79. Santos, C.A.B., Nogueira, E.M.S. (Org.). EDUNEB, Bahia.

Roberto, I.J., Brito, L., Cascon, P. (2011): Temporal and spatial patterns of reproductive activity in Rhinella hoogmoedi (Anura: Bufonidae) from a tropical rainforest in northeastern brazil, with the description of its advertisement call. South American Journal of Herpetology 6(2): 87–97.

Sabagh, L.T., Carvalho-e-Silva, A.M.P.T. (2008): Feeding overlap in two sympatric species of Rhinella (Anura: Bufonidae) of the Atlantic Rain Forest. Revista Brasileira de Zoologia 25: 247–253.

Sabagh, L.T., Ferreira, R.B., Rocha, C.F.D. (2017): Host bromeliads and their associated frog species: further considerations on the importance of species interactions for conservation. Symbiosis 73(3): 201–211.

Steinbach-Padilha, G. (2008): A new species of Melanophryniscus (Anura, Bufonidae) from the Campos Gerais region of Southern Brazil. Phyllomedusa 7: 99–108.

Ulloa-Ulloa, C., Acevedo-Rodríguez, P., Beck, S., Belgrano, M.J., Bernal, R., Berry, P.E., et al. (2017): An integrated assessment of the vascular plant species of the Americas. Science 358: 1614–1617.

Vörös, J., Dias, I. R., Solé, M. (2017): A new species of Phyllodytes (Anura: Hylidae) from the Atlantic Rainforest of southern Bahia, Brazil. Zootaxa 4337(4): 584–594.

Wells, K.D. (2007): The Ecology and Behavior of Amphibians. The University of Chicago Press, Chicago, 1148 pp.

Ubiratã Ferreira Souza et al.906