Anuran species in a remnant of the Atlantic rainforest in an urban area

Abstract

Forest fragments in urban areas have many habitat resources that frogs use for refuge, reproduction and growth. Knowledge of an anuran assembly is the first step towards understanding the importance of these forest fragments in areas highly threatened by anthropogenic actions. We sampled anurans during the day and night from November 2012 to August 2013 through visual and acoustic surveys. We found 333 individuals belonging to 19 species. The highest richness and abundance were recorded in January whereas the lowest richness and abundance were recorded in June. Most species were found in open areas. Our results highlight the importance of well-studied urban fragments for the anuran community. The conservation of these habitats may ensure the viability of the ecological functions of this anuran community for the future.

Key-Words.
Amphibian; Community; Habitat loss; Refuge; Conservation

INTRODUCTION

The Atlantic Forest is under severe fragmentation and loss due to human colonization, which poses several threats to native biodiversity (Ribeiro et al., 2009; Tabarelli et al., 2010). Fragmentation and habitat loss change the forest structure and local climate, and as a consequence the temperature and humidity are also modified (Felix et al., 2004; Gandinetti & Jacobi, 2005; Cushman, 2006). Nevertheless, some of the remaining fragments play an important role as refuge for many species in some regions of the Atlantic Forest domain (Rocha et al., 2004; Martins et al., 2014).

Urban forest fragments may provide survival conditions for several organisms including plants, invertebrates and vertebrates (Rodrigues et al., 1993; Miyashita et al., 1998; Azevedo et al., 2002; Brown & Freitas, 2002; Estrada & Coates-Estrada, 2002; Pontes & Soares, 2005; Tsuji-Nishikido, 2011; Diamond & Heinen, 2016). Anurans have specific requirements for habitat occupancy that are usually related to their reproductive mode (Duellman & Trueb, 1994; Almeida-Gomes & Rocha, 2015). Species are either specialists that require a specific habitat for reproduction (e.g., bromeliads) or opportunistic that are able to reproduce in different types of habitats (e.g., ponds, streams and rivers) (Duellman & Trueb, 1994; Haddad et al., 2013).

In this study, we assessed the composition, spatial distribution, and diversity of anuran community inhabitants in urban forest fragment in southeastern Brazil.

MATERIAL AND METHODS

We studied the amphibian community at Parque Estadual da Fonte Grande (hereafter PEFG), in the municipality of Vitória, in the state of Espírito Santo, southeastern Brazil (20°18’S and 40°20’W, 300 m asl., Fig. 1). PEFG comprises ca. 218 ha of Atlantic Forest, mostly of secondary vegetation (Griffo & Silva, 2013). The climate is monsoon (Am) according to the revised Köppen-Geiger’s climate classification (Alvares et al., 2013).

Anurans were recorded monthly during the day (08:00-12:00 h) and night (18:00-23:00 h), from November 2012 to August 2013 through visual and acoustic surveys in permanent ponds, temporary and permanent streams, forest leaf-litter, and bromeliads, because these were the sites in PEFG in which anurans were most likely to be found. The individuals were hand captured and maintained in plastic bags for identification. Afterwards, all individuals were released in the same site where they were captured. Some specimens (ca. five individuals per species) were collected and euthanized with topical lidocaine (CEBEA, 2013), fixed in 10% formalin and preserved in 70% alcohol (Auricchio & Salomão, 2002). Vouchers specimens were deposited in the Museu Nacional at Universidade Federal do Rio de Janeiro (MN/UFRJ) and Eugenio Izecksohn at Universidade Federal Rural do Rio de Janeiro (EI/UFRRJ). In order to evaluate sampling effectiveness, we ran a species rarefaction curve with 1,000 randomizations of the original dataset using Biodiversity R package (Kindt, 2016) in R 3.3.0 (R Development Core Team, 2016). For each species, we obtained data of conservation status and population trends from the Red List of the International Union for Conservation of Nature (IUCN, 2017). We categorized the habitat requirements of the species: “forest dependent”, “open landscapes” and “habitat generalist” (when they occupy both forest and open landscapes) (Teixeira et al., 2008; Haddad et al., 2013).

Figure 1
Map of the study location in the state of Espírito Santo, southeastern Brazil. In detail, Vitória municipality with delimitations of Parque Estadual da Fonte Grande (yellow contour).

RESULTS

We recorded 333 individuals belonging to 19 species and seven families (Table 1). The species rarefaction curve stabilized in 20 species (Fig. 2), indicating that our sampling was sufficient to record all potential species in PEFG. All recorded species were classified as “Least Concern”. Three species (15%) have decreasing population trends (IUCN, 2017). The highest richness (N = 9) and abundance (N = 84) were recorded in January (rainy season) whereas the lowest richness (N = 4) and abundance (N = 9) were recorded in June (dry season).

Figure 2
Species rarefaction curve of the anuran recorded at Parque Estadual da Fonte Grande, municipality of Vitória, state of Espírito Santo, southeastern Brazil. Vertical bars indicate the upper and lower limits of the confidence interval (95%).

Table 1
Anuran composition of the Parque Estadual da Fonte Grande, municipality of Vitória, state of Espírito Santo, southeastern Brazil. Habitat requirements: F = Forest-dependent, O = Open-landscape dependent, and G = habitat generalist. *Endemic to Atlantic Forest. Conservation status of all species is Least Concern. ^Dspecies found during the day, ^Nspecies found during the night.

Family Species	Population trends	Habitat
Bufonidae
Rhinella crucifer (Wied-Neuwied, 1821)*,N	decreasing	G
Craugastoridae
Haddadus binotatus (Spix, 1824)*,D	stable	F
Cycloramphidae
Thoropa miliaris (Spix, 1824)*,D,N	stable	G
Hylidae
Boana albomarginata (Spix, 1824)*,N	stable	O
Boana faber (Wied-Neuwied, 1821)*,N	stable	G
Dendropsophus bipunctatus (Spix, 1824)*,N	stable	O
Dendropsophus branneri (Cochran, 1948)N	stable	O
Dendropsophus decipiens (Lutz, 1925)N	stable	G
Dendropsophus haddadi (Bastos & Pombal, 1996)*,N	stable	O
Scinax alter (Lutz, 1973)*,N	stable	O
Scinax cuspidatus (Lutz, 1925)*,N	stable	O
Scinax gr. ruber N	No data	O
Ololygon argyreornata (Miranda-Ribeiro, 1926)*,N	stable	G
Ololygon gr. perpusilla sp. nov.*,D,N	No data	O
Trachycephalus nigromaculatus Tschudi, 1838,N	stable	F
Leptodactylidae
Leptodactylus latrans (Steffen, 1815)N	stable	G
Physalaemus crombiei Heyer & Wolf, 1989*,D,N	decreasing	F
Odontophrynidae
Proceratophrys schirchi (Miranda-Ribeiro, 1937)*,D,N	decreasing	F
Pipidae
Pipa carvalhoi (Miranda-Ribeiro, 1937)D,N	stable	O

DISCUSSION

The number of species recorded at PEFG correspond to about 56% of the 34 species known to the Vitória municipality (Ferreira et al., 2010) and 68% of the recorded species (N = 13) are endemic to the Atlantic Forest (Table 1). Regarding habitat requirements, the majority of the species in PEFG are open-landscape dependent (48%), followed by generalist (31%) and forest dependent (21%). In a more preserved Atlantic Forest fragment situated in an inland mountainous region (about 80 km away), most of the recorded species were also classified as open-landscapes dependent (58%), followed by forest dependent (29%) and generalist (13%) (Silva-Soares & Scherrer, 2013). However, in a cabruca agrosystem (i.e., mixed of forest and cacao plantation) in Atlantic Forest (about 90 km away), the majority of the species recorded are forest dependent (49%), followed by open landscapes (35%) and habitat generalists (16%) (Teixeira et al., 2015). Variations in the habitat preferences of anurans across sites are perhaps a consequence of the different habitat types available to occupy and the degree of forest conservation. We detected a high proportion of open-landscape dependent species that include a new bromeliad frog (TSS; MMM; & Hélio R. da Silva, unpubl. data), which increases the value of PEFG for anuran conservation.

Our results highlight the importance of well-studied urban fragments of the Atlantic Forest for anuran assembly. Although surrounded by urban landscapes, this forest refuge harbors 19 species of anurans, three of which (Rhinella crucifer, Physalaemus crombiei and Proceratophrys schirchi) with population decline (IUCN, 2017) and one new species that we found during this work (Silva-Soares et al. under description). This richness was probably related to the variety of habitat types in PEFG (permanent ponds, temporary and permanent streams, bromeliads, and forest leaf-litter) in which anurans have been reproducing. Thus, the conservation of these habitats may ensure the continuous viability and ecological functions of this anuran assembly in the present and into the future.

ACKNOWLEDGMENTS

We are grateful to Elaine Campinhos, Eliane Giori, Suzana Carvalho, Leonardo Zortéa, Maria Carolina Stein, Paulo Victor Scherrer and Sulamita Marques for their assistance in the field. Rodrigo Barbosa Ferreira and Cora Jennings for English review. The Prefeitura Municipal de Vitória (PMV) especially Breno Platais, Camila Ramos, Felipe Fraga and security guards for logistical support. Instituto Chico Mendes de Conservação da Biodiversidade (ICMBio, SISBIO) and PMV for issued permits (processes 34836-4/2012 and 3764161/2012, respectively). TSS received funds from Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq; PCI-DA). MMM received scholarships from Fundação de Amparo à Pesquisa e Inovação do Espírito Santo (FAPES) and Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES). RBGC research was sponsored by FAPES (#0611/2015).

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• 1
  Edited by: Marcelo Duarte
• Published with the financial support of the "Programa de Apoio às Publicações Científicas Periódicas da USP"
• 3
  Seção de Publicações - Museu de Zoologia da Universidade de São Paulo

Publication Dates

• Publication in this collection
  2018

History

• Received
  19 Oct 2017
• Accepted
  18 Dec 2017