Frog assemblage associated with bromeliads in a sandy coastal plain in the state of Espírito Santo, southeastern Brazil

Amphibians may use bromeliads for reproduction (i.e., bromeligenous species) or only for refuge and foraging (i.e., bromelicolous species). The partition of bromeliad resources is essential to maintain the coexistence of the associated assemblages. We sampled 913 bromeliads in a sandy coastal plain (i.e., restinga habitat) in southeastern Brazil and found 234 frogs belonging to seven species. One of the frog species was bromeligenous and the other six were facultative bromelicolous. The bromeliads of the genus Aechmea were the most frequently used by frogs. The low degree of frog occupancy of bromeliads (26%) suggests habitat segregation. Our study highlights the importance of maintenance of bromeliad species for conservation of the associated frog assemblages. Key-Words: Anura; Atlantic forest; Bromelicolous; Bromeligenous; Restinga. The Brazilian Atlantic Forest harbors more than 100 frog species that use bromeliads, which represents about 18% of the regional frog richness (Haddad et al., 2013). The degree of association between frogs and bromeliads range from obligate users (i.e., bromeligenous), which depend on these plants for breeding purposes, to facultative users (i.e., bromelicolous) that use bromeliads only as refuges and for foraging INTRODUCTION Anurans occupy many types of habitats generally related to their reproductive mode (Haddad et al., 2013). Some frog species occupy bromeliads due to these plants’ capacity to accumulate rainwater between their leaves, becoming an important microhabitat for shelter, foraging and reproduction (Peixoto, 1995). www.mz.usp.br/publicacoes www.revistas.usp.br/paz ISSN impresso: 0031-1049 ISSN 1807-0205 on-line: Museu de Zoologia da Universidade de São Paulo Papéis Avulsos de Zoologia http://dx.doi.org/10.11606/0031-1049.2017.57.34 1. Universidade Vila Velha (UVV), Programa de Pós-Graduação em Ecologia de Ecossistemas (PPGEE). Campus Boa Vista. Avenida Comissário José Dantas Mello, 21, Boa Vista II, 29102-920, Vila Velha, ES, Brasil. 2. Universidade Federal do Espírito Santo (UFES), Departamento de Gemologia. Avenida Fernando Ferrari, 514, Goiabeiras, 29075-910, Vitória, ES, Brasil. 3. ORCID: 0000-0001-7528-072X. E-mail: marcioherpetologia@gmail.com (corresponding author) 4. ORCID: 0000-0001-5185-5744. E-mail: rbfherpeto@gmail.com 5. E-mail: larissacorteletti@biologa.bio.br 6. ORCID: 0000-0003-2666-8618. E-mail: filhoprj@gmail.com 7. E-mail: pdfj@hotmail.com Volume 57(34):445-449, 2017 purposes (Peixoto, 1995; Haddad et al., 2013; Pertel et al., 2010). Because bromelicolous species breed at ponds and rivers and use bromeliads as secondary microhabitat, they may use more species of bromeliads. Many frog species in sandy coastal plains (i.e., restinga habitat) use bromeliads (Rocha et al., 2008; Schineider & Teixeira, 2001; Ferreira et  al., 2012; Mageski et  al., 2016). This association is important because of the harsh environmental conditions in restingas, such as low free water availability (because sandy soils increase water percolation), high temperature, high solar exposition and salinity (da-Silva, 1998; Scarano et al., 2001; Pereira et al., 2004). Sandy coastal plains are under severe anthropic threats such as pollution, sand extraction, increase of tourism and bromeliad collection (Brown & McLachlan, 2002; Mageski et al., 2016). Thus, understanding the bromeliad frog assemblages and the associated bromeliads is a key priority for the maintenance of the species and their ecological function in sandy coastal plains. In this work, we aimed to assess the composition and diversity of a frog assemblage that uses bromeliads in a sandy coastal plain in state of Espírito Santo, southeastern Brazil. We also present data about bromeliad species that each frog used and discuss conservation implications for the sandy coastal plains. Although our study was conducted in a sandy coastal plain, the results may have implications for other restingas in the Atlantic Forest domain. MATERIAL AND METHODS The fieldwork was carried out during five days per month from January to April 2013 in the sandy coastal plain (hereafter restinga) of Parque Estadual FIGURE 1: Location of Parque Estadual Paulo César Vinha (black dot) in the state of Espírito Santo, southeastern Brazil (A) and sampled sites: rocky outcrop (B), open shrub vegetation (C), both in the mainland, and open herbaceous vegetation in coastal island (D). States are Bahia (BA), Espírito Santo (ES), Minas Gerais (MG) and Rio de Janeiro (RJ). Mageski, M.M. et al.: Bromeliad frogs in a sandy coastal plain 446


INTRODUCTION
Anurans occupy many types of habitats generally related to their reproductive mode (Haddad et al., 2013).Some frog species occupy bromeliads due to these plants' capacity to accumulate rainwater between their leaves, becoming an important microhabitat for shelter, foraging and reproduction (Peixoto, 1995).purposes (Peixoto, 1995;Haddad et al., 2013;Pertel et al., 2010).Because bromelicolous species breed at ponds and rivers and use bromeliads as secondary microhabitat, they may use more species of bromeliads.
Many frog species in sandy coastal plains (i.e., restinga habitat) use bromeliads (Rocha et al., 2008;Schineider & Teixeira, 2001;Ferreira et al., 2012;Mageski et al., 2016).This association is important because of the harsh environmental conditions in restingas, such as low free water availability (because sandy soils increase water percolation), high temperature, high solar exposition and salinity (da-Silva, 1998;Scarano et al., 2001;Pereira et al., 2004).Sandy coastal plains are under severe anthropic threats such as pollution, sand extraction, increase of tourism and bromeliad collection (Brown & McLachlan, 2002;Mageski et al., 2016).Thus, understanding the bromeliad frog assemblages and the associated bromeliads is a key priority for the maintenance of the species and their ecological function in sandy coastal plains.
In this work, we aimed to assess the composition and diversity of a frog assemblage that uses bromeliads in a sandy coastal plain in state of Espírito Santo, southeastern Brazil.We also present data about bromeliad species that each frog used and discuss conservation implications for the sandy coastal plains.Although our study was conducted in a sandy coastal plain, the results may have implications for other restingas in the Atlantic Forest domain.

MATERIAL AND METHODS
The fieldwork was carried out during five days per month from January to April 2013 in the sandy coastal plain (hereafter restinga) of Parque Estadual Paulo César Vinha (hereafter PEPCV, 20°36'16.391"Sand 40°25'32.934"W,Fig. 1A) in Guarapari municipality, state of Espírito Santo, southeastern Brazil.The study site comprises about 1,500 ha of native restinga with rocky outcrop (Fig. 1B) and open shrub vegetation (Fig. 1C) on the mainland and open herbaceous vegetation in coastal islands (Fig. 1D).There are abundant ground bromeliads and temporary and permanent ponds.We sampled in all three vegetation types (Fig. 1B, 1C and 1D) for frogs during four hours at night (18-22 h) with a sampling method in which four researchers walked in a straight line parallel to each other searching bromeliads randomly along the trail.We identified all frog species in the field and followed Haddad et al. (2013) for classification into either bromeligenous or bromelicolous guilds (Table 1).We compared the proportions of occupied and unoccupied bromeliads to test if each bromeliad species are occupied in proportion to their local abundance, using chi-square exact test (χ2) in software R 3.3.0(R Development Core Team, 2016).We calculated diversity of frogs based on richness and abundance in the study area and in each bromeliad species by Shannon-Wiener index (H') in software Past 2.17 (Hammer et al., 2001).All frogs were released in the bromeliads where they were found after collection of data.

DISCUSSION
Our results highlight the importance of the PEPCV for conservation of bromeliad frogs.The frog richness that we found (seven) was higher than those recorded in other sandy coastal plains of Espírito Santo state.For example, six species were found by Schineider & Teixeira (2001) and six species were found by Ferreira & Mendes (2010).In addition, we recorded more species than other similar environments in the state of Espírito Santo.For example, Pertel et al. (2010) recorded three species, Mageski et al. (2014) and Pertel et al. (2006) five species, and Pertel et al. (2007) and Teixeira & Rödder (2007) six species.
Apparently, the degree of bromeliad occupancy was low in our study site.Furthermore, occupancy was not proportional to the abundance of each bromeliad species.This result may be a consequence of bromeliad selection by the frogs.In the same study site, Phyllodytes luteolus selected small plants with more leaves (Mageski et al., 2016).In addition, another study have showed that the structure of the plants influences bromeliad selection by Ololygon argyreornata (Pederassi et al., 2012).The structure of bromeliads are related to the capability to accumulate rainwater (Pontes et al., 2013).In this way, the bromeliads of the genus Aechmea seem to be the most important plants for the local frog assemblage.Aechmea blanchetiana has more leaves and harbored a higher abundance of frogs whereas Aechmea nudicaulis has a deep and wide central tank and harbored a higher diversity of bromeliad frogs (Cogliatti-Carvalho et al., 2010).
This study shows the conservation importance of bromeliads for the maintenance of frog assemblages in sandy coastal plains.These frogs are greatly affected by the dramatic reduction of the sandy coastal plain habitats that can result in the destruction of the bromeliads and in the consequent local extinction of many associated species.In addition, bromeliad collecting may transport frogs to other environments in which they can become invasive species (Salles & Silva-Soares, 2010).We recommend further studies to address information about population viability over time that improves our knowledge on the ecology of these bromeliad-associated frogs and their conservation in sandy coastal plains.

FIGURE 1 :
FIGURE 1: Location of Parque Estadual Paulo César Vinha (black dot) in the state of Espírito Santo, southeastern Brazil (A) and sampled sites: rocky outcrop (B), open shrub vegetation (C), both in the mainland, and open herbaceous vegetation in coastal island (D).States are Bahia (BA), Espírito Santo (ES), Minas Gerais (MG) and Rio de Janeiro (RJ).