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Research Article
Anurofauna of a remnant of Atlantic Forest in northeast Brazil
expand article infoGessica Gomes Barbosa, Camila Nascimento de Oliveira, Umberto Diego Rodrigues de Oliveira§, Gilberto Gonçalves Rodrigues
‡ Universidade Federal de Pernambuco, Recife, Brazil
§ Universidade Federal da Bahia, Salvador, Brazil
Open Access

Abstract

Studies on spatial occupation are fundamental to understand amphibian communities. The aim of this study was to record information on the spatial distribution of anurans in the Tejipió forest, state of Pernambuco, northeastern Brazil. Fieldwork was carried out weekly between October 2011 and April 2012, with daytime and night-time excursions for time-constrained active searching, in forested and open areas, military construction area and water bodies. Pitfall traps and accidental sightings were also used as alternative collection methods. Data were used to calculate richness, rarefaction curves and richness estimators. A total of 21 species were recorded, distributed in six families: Bufonidae (2 spp.); Craugastoridae (1 sp.); Hylidae (8 spp.); Leptodactylidae (8 spp.); Microhylidae (1 sp.) and Phyllomedusidae (1 sp.). Only the species Rhinella jimi was found occupying all sampled habitats in the research area. Adenomera hylaedactyla and Pristimantis ramagii deserve special care in the area because they are specialists, occupying a smaller number of habitats and microhabitats. The community of anurans of the Tejipió forest is similar to those recorded in other areas of the Atlantic Forest at the Pernambuco state, and its knowledge is essential as a basis for conservation of the area. The gradual recovery of this Atlantic Forest remnant would favor the recolonization of fauna and flora and the conservation of local biodiversity.

Keywords

abundance, amphibians, conservation, ecology, richness

Introduction

The anurans have a global richness of 8181 known species (Frost 2020), distributed in all continents, except the poles and some oceanic islands. The Neotropical region present one-third of the species known in the world (Duellman 1999). The country that holds the higher diversity of the group is Brazil, with 1137 registered species (Segalla et al. 2019). The Brazilian Atlantic Forest has 625 registered species (Rossa-Feres et al. 2017) and these numbers of species continuously increase with new studies (e.g. Malagoli et al. 2017; Guimarães et al. 2017; Roberto et al. 2017; Walker et al. 2018; Santos et al. 2019).

Originally, the Atlantic Forest biome covered 150 millions of hectares, with heterogeneous environments (Ribeiro et al. 2009). Currently, the biome is highly deforested, characterized by isolated and small fragments. Nonetheless, the Atlantic forest features a high diversity and high levels of endemism, which makes it one biodiversity hotspot (Myers et al. 2000; Ribeiro et al. 2009; Mittermeier et al. 2011). Studies that seek knowledge of ecological aspects of amphibian species serve as conservation initiatives for Atlantic Forest (e.g. Abrahão et al. 2018). Furthermore, studies about biology and distribution of the amphibians make it possible to find out new species, the degree of regional endemism, aside from enriching regional and national scientific collections (Moura et al. 2011). This type of information is very important for the elaboration of effective management and conservation measures (Pereira et al. 2015).

The recovery of vegetation provides peculiar ecological conditions, forming new landscapes and increasing the availability of microhabitats, which might be followed by the recolonization by animals and plants. Studies that aim at evaluating how this process affects biodiversity are, therefore, essential to understand the mechanisms affecting the ecological functioning of areas under regeneration. This paper contributes with the first information about the local anurans community we recorded information on the spatial distribution of anurans in the Tejipió forest, an area under regeneration at the state of Pernambuco, northeastern Brazil.

Methods

Study site

The study was conducted in the Tejipió forest (08°05'45,59"S, 34°57'04,91"W) (Fig. 1), a set of discontinued forest fragments at BR-101 Sul, in the Recife metropolitan area, state of Pernambuco, Brazil. The forest was donated by the Ministry of Agriculture to the Fourth Communications Battalion of the Brazilian army (4°BCom). The Tejipió forest occupies 172 hectares, consisting of an Atlantic Ombrophilous Dense Forest. The climate is characterized as As’ according to Köppen (Silva et al. 2014). The mean annual temperature is 25.4 °C and mean annual rainfall is 2.458 mm (World Weather Information Service 2013), with rains occurring between the months of January and August (APAC 2020). The site is located within the Tejipió river hydrographic basin (Araújo and Pires 1998).

Figure 1. 

Location of the study site (Tejipió forest), Recife, Pernambuco, northeastern Brazil. The red triangles show the location of the pitfall traps.

These fragments present low arboreal heterogeneity (Feitosa 2004), with its vegetation in progressive restoration (Guimarães et al. 2012), a process that began 50 years ago. The study site contains a forested area with a lentic water body (lake), surrounded by human communities and a military construction, with another smaller lake nearby.

Sampling

Our sampling was carried out weekly between October 2011 and April 2012 using pitfall traps, time-constrained active searches and accidental sightings. Active searches were carried out for nine hours per day, with diurnal and nocturnal searches, and totalized a sampling effort of 252 man-hours. We selected different habitats with contrasting characteristics: habitat I – open area, lightly wooded dry sites surrounded by forest; habitat II – forest area, “a minimum area of land of 0.05–1.0 hectares with tree crown cover (or equivalent stocking level) of more than 10–30 % with trees with the potential to reach a minimum height of 2–5 meter at maturity in situ”, according to Kyoto Protocol (Kant 2006); habitat III – permanent water bodies, lake 1 (8°6'35.99"S, 34°57'12.04"W), occupying 6.943 m2 surrounded by forest and lake 2, (8°5'50.03"S, 34°57'6.68"W), occupying 2.886 m2 surrounded by military construction. Both have emergent and free floating aquatic weeds; habitat IV – small temporary water bodies, occupying less than 10 m2 and dry during the dry season; and habitat V – military construction area, in the vicinity of the human habitation. In addition, we selected nine different microhabitats: 1) leaf litter (dead plant material that have fallen to the ground); 2) bare ground (soil without vegetation cover); 3) humid soil (soil with water retention); 4) buildings (e. g. walls, rooms, bathroom, among other things); 5) emergent aquatic weeds (plants that are rooted in the water body bottom, extending above the surface of the water); 6) free floating aquatic weeds (plants living on the water’s surface); 7) shrubs (small to medium sized woody plants); 8) partially immersed in water; and 9) buried in the ground (basically a hole used as a dwelling).

The pitfall traps were installed at six samplings station. Each station had four buckets, two with 60 L capacity and two with 22 L capacity, intercalated. The buckets were arranged linearly and connected by 10 m of plastic drift fences, with two plastic drift fences at the ends of the traps, totalizing 50 m. The sampling effort totalized 16,128 hours of trapping.

The specimens caught were identified and released (collecting authorization no. 31795-1 of the Chico Mendes Institute for Biodiversity Conservation). Furthermore, specimens found dead were deposited in the Herpetology Collection of the Federal Rural University of Pernambuco (CHP-UFRPE).

Data analyses

To evaluate the sampling effect, we constructed a rarefaction curve. Species richness was calculated through the richness estimators Chao 1, Jackknife 1 and Bootstrap, using 1000 random additions of the samples. The analyses were performed using EstimateS software, version 9.1 (Colwell 2013).

Results

We registered 1106 specimens, belonging to 21 species, 10 genera and 6 families: Bufonidae (2 spp.); Craugastoridae (1 sp.); Hylidae (8 spp.); Leptodactylidae (8 spp.); Microhylidae (1 sp.) and Phyllomedusidae (1 sp.) (Table 1). The Hylidae and Leptodactylidae families presented the higher richness, both with eight species each (38,1 %). The species of the family Hylidae that presented greatest specimen abundance were Dendropsophus branneri (231 individuals), Dendropsophus decipiens (63 individuals) and Scinax nebulosus (38 individuals). In turn, Adenomera hylaedactyla (273 individuals), Leptodactylus natalensis (61 individuals) and Leptodactylus macrosternum (46 individuals) showed greatest specimen abundance among Leptodactylidae species.

Table 1.

Composition and abundance of the anuran species registered during the months of October of 2011 to April 2012 in the Tejipió forest, northeastern Brazil. Habitats: I. Open area, II. Forest area, III. Permanent water bodies, IV. Temporary water bodies and V. Military construction area. Microhabitats: 1. Leaf litter, 2. Bare ground, 3. Humid soil, 4. Buildings, 5. Emergent aquatic weeds, 6. Free floating aquatic weeds, 7. Shrubs, 8. Partially immersed in water and 9. Buried in the ground. Form of register (FR): a) Pitfall traps, b) Time-constrained active searching, and c) Accidental sightings.

Taxon Habitat Microhabitat FR Abundance
Family Bufonidae
Rhinella granulosa (Spix, 1824) I 3 c 1
Rhinella jimi (Stevaux, 2002) I, II, III, IV, V 1, 2, 3, 4 a, b 24
Family Craugastoridae
Pristimantis ramagii (Boulenger, 1888) II 1 a, b 172
Family Hylidae
Boana albomarginata (Spix, 1824) III, IV 5, 7 b 33
Boana raniceps (Cope, 1862) III, IV 5, 7 b 5
Dendropsophus branneri (Cochran, 1948) III, IV 5, 6, 8 b 231
Dendropsophus decipiens (Lutz, 1925) III, IV 5, 6, 8 b 63
Dendropsophus elegans (Wied-Neuwied, 1824) III, IV 5 b 3
Dendropsophus minutus (Peters, 1872) III, IV 5, 6, 8 b 14
Scinax nebulosus (Spix, 1824) III, IV 5, 6 b 38
Scinax x-signatus (Spix, 1824) III, IV 5, 6 b 24
Family Leptodactylidae
Adenomera hylaedactyla (Cope, 1868) II 1, 2 a, b 273
Leptodactylus fuscus (Schneider, 1799) I, III 3 a, b 14
Leptodactylus macrosternum Miranda-Ribeiro, 1926 III 3, 8 b 46
Leptodactylus mystaceus (Spix, 1824) II - a 1
Leptodactylus natalensis Lutz, 1930 III 3 a, b 61
Leptodactylus troglodytes Lutz, 1926 I 2 a, b 9
Leptodactylus vastus Lutz, 1930 II, III, IV 1, 2, 3, 8 a, b 24
Physalaemus cuvieri Fitzinger, 1826 I, II, IV 1, 2, 3, 8 a, b 43
Family Microhylidae
Elachistocleis cesarii (Miranda-Ribeiro, 1920) II 1, 9 a, b 4
Family Phyllomedusidae
Pithecopus nordestinus (Caramaschi, 2006) III 5 b 23

The rarefaction curve (Fig. 2) presented a strong tendency towards stability from the 10th sample, indicating approximation to real number of species; in other words, the methods and effort used were efficient in sampling the area. The richness estimators Chao 1, Jackknife 1 and Bootstrap estimated a richness of 22, 23 and 22 species, respectively, with values of richness very close to the observed richness (Fig. 3).

Figure 2. 

Rarefaction curve representing the accumulated richness of the species of anurans in the Tejipió forest, northeastern Brazil, recorded between October 2011 and April 2012.

Figure 3. 

Richness estimators based on the abundance of anurans species recorded in the Tejipió forest, northeastern Brazil, between October 2011 and April 2012.

The time-constrained active searching method was more successful at finding different species (19 spp.) compared to the pitfall traps method (10 spp.) and accidental sightings (1 sp.) (Table 1). Only the species Leptodactylus mystaceus was recorded exclusively through the pitfall method, and Rhinella granulosa was recorded through accidental sightings, during a heavy rain event.

The highest number of species was associated with permanent water bodies (lakes) and temporary water bodies (Table 1). The hylids were recorded in association with water bodies (habitats III and IV). While leptodactylids were recorded occupying four habitats (habitats I, II, III and IV), with the species L. vastus and P. cuvieri recorded in a greater number of habitats. We recorded two species of the family Bufonidae, R. jimi and R. granulosa. Only the species Rhinella jimi was recorded occupying all the sampled habitats.

The microhabitats shared by highest number of species were the emergent aquatic weeds (B. albomarginata, B. raniceps, D. branneri, D. decipiens, D. elegans, D. minutus, S. nebulosus, S. x-signatus and P. nordestinus), humid soil (R. granulosa, R. jimi, L. fuscus, L. macrosternum, L. natalensis, L. vastus and P. cuvieri), leaf litter (R. jimi, P. ramagii, A. hylaedactyla, L. vastus, P. cuvieri and E. cesarii) and partially immersed in water (D. branneri, D. decipiens, D. minutus, L. macrosternum, L. vastus and P. cuvieri) (Table 1). Leptodactylus vastus, P. cuvieri and R. jimi used the greatest number of microenvironments, with four microhabitats each. The species L. natalensis, L. troglodytes, P. nordestinus, P. ramagii and R. granulosa were recorded only in one habitat and microhabitat.

Discussion

The 21 sampled species of anurans correspond to 24.1 % of the total species known to occur in the state of Pernambuco (Semas 2015). Atlantic Rainforest remnants in northeastern Brazil present an equal or a smaller number of species than we found in our study, such as State Park Ecotourism and Sustainable Development of Cachoeira do Urubu (21 spp.) (Barbosa et al. 2019) and Mata do Buraquinho (14 spp.) (Santana et al. 2008). Nevertheless, there are fragments with higher anuran richness, such as the integral protection area Wildlife Refuge Matas do Sistema Gurjaú (Pernambuco) with 30 spp. (Barbosa et al. 2018) and Cariri Farm (Alagoas) with 32 spp. (Palmeira and Gonçalves 2015). The species recorded are not listed as threatened (MMA 2014; Semas 2015; ICMBio 2016; IUCN 2020). The families with greatest richness were Hylidae and Leptodactylidae, which show high diversity in the Atlantic Forest (Rossa-Feres et al. 2017) and in Brazil (Segalla et al. 2019), a pattern also found in the whole Neotropical region (Duellman and Trueb 1994; IUCN 2020).

Regarding the three species registered with higher abundance in this study, A. hylaedactyla, D. branneri and P. ramagii are widely distributed in Brazil. The first A. hylaedactyla is widespread, occurring in Amazonia, Chaco, Cerrado, Caatinga and Atlantic Forest (Fouquet et al. 2013). Our study area has diverse environments for A. hylaedactyla, where this species generally is omnipresent, being abundant in leaf litter, according to Borges-Leite et al. (2015). In addition, pitfall traps are efficient in collecting these organisms with terricolous habits. The species D. branneri has a broad geographic distribution along the Brazilian coast (Haddad et al. 2013; Frost 2020), being an endemic species of the Atlantic Forest (Rossa-Feres et al. 2017). This species is found in temporary and permanent lakes (Juncá 2006; Palmeira and Gonçalves 2015) and has been registered in large groups producing advertisement calls. Pristimantis ramagii belongs to a genus comprised by typical frogs of forested areas (Pinto-Sánchez et al. 2012) and native to South America (Hedges et al. 2008). The species P. ramagii is distributed from the state of Paraíba to the north of Bahia (Haddad et al. 2013; Frost 2020) and considered an endemic species of the Atlantic Forest (Rossa-Feres et al. 2017), being exclusively found on forested areas in the present study.

The composition of the anuran assembly can vary according to local factors, environmental heterogeneity (Huston 1994), anthropic impacts (Young et al. 2001) and species phenology. Besides, anurans area generally affected by the rainfall distribution, due to an increased number of aquatic sites available for reproduction (Duellman and Trueb 1994). In the environments with anthropic alterations and high solar radiation, we found only individuals of the Bufonidae family. This can be explained because the individuals of the genus Rhinella present a higher tolerance to water loss compared to other anurans (Thorson 1955). Rhinella jimi, for example, is very generalist, occurring in secondary forest, savannah, agricultural lands, other open areas and disturbed habitats (Gilda and Carnaval 2004), being also generalist in our study. Another example, R. granulosa, is tolerant to high temperatures (Oliveira and Cassemiro 2013), we recorded a specimen in an open area.

Regarding the families that presented higher occupancy of microhabitats (Bufonidae, Hylidae and Leptodactylidae), the Bufonidae species recorded in our study are terrestrial. They were recorded in herbaceous vegetation and humid soil (Barbosa and Alves 2014). Hylidae family is recorded occupying arboreal habits, adding the possibility of vertical movement (Cardoso et al. 1989), in this case occupying shrubs, due the presence of hand adhesive discs allows them to occupy more diverse environments. The family Leptodactylidae comprises generalist organisms, which only need bodies of water to reproduce (Coelho and Oliveira 2010). These organisms occupy temporary aquatic ecosystems in open areas (Feio and Ferreira 2005), being found in the soil, margins of dams and flooded areas (Amorim et al. 2009). However, in the Tejipió forest leptodactylid species mainly occupied permanent water bodies and forest areas.

The species P. ramagii occupies forested areas under the leaf litter, which highlights the importance of conservation of forest areas for the species. However, Santana et al. (2008) observed P. ramagii occupying a variety of microhabitats, such as humid soils, leaf litter, shrubs and fallen trunks. Adenomera hylaedactyla, E. cesarii and L. mystaceus also occupying only forest areas, these highlights importance of conservation of forest areas. Despite the great abundance, P. ramagii and A. hylaedactyla were recorded in only one habitat (forest area) and few microhabitats (one and two microhabitats, respectively), indicating environmental specificity.

It is important to mention the high biological relevance of the studied area, because this highlights its scientific potential. Future studies are essential to assess how the recolonization of anurans is associated with local forest regeneration. During the study, countless impacts caused by people entering in the forest were observed, such as fire, trash release, removing soil and deforestation, among others. Thus, the presence of the Military Brigade in the area is important for its conservation (Guimarães et al. 2012), maintaining the local biodiversity. The present study aids as a first step towards the knowledge of the anuran fauna of the area, aiming to create ecological projects and public policies to preserve the area at a medium and long run.

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