Dias Mira-Mendes Solé 2014 APA Da Lagoa Encantada

Introduction

Amphibians and reptiles are among the most endangered groups of animals worldwide. The main cause of their decline is associated to the loss and fragmentation of the environment, especially in the Neotropics (Gibbons et al., 2000; Young et al., 2004; Stuart et al., 2004; Todd et al., 2009).

The APA (Environmental Protection Area) of Lagoa Encantada, located in the municipality of Ilhéus, Bahia state, was established in June 14, 1993 (Bahia, 1993), with the main goal to protect the environmental heritage. In 2003, the environmental protection area was renamed the APA of Lagoa Encantada and Rio Almada, covering the cities of Ilhéus, Uruçuca, Itajuípe, Coaraci and Almadina, with an estimated total area of 157,745 ha, represented by remnants of the Atlantic Forest (Bahia, 2003). This region shelters one of the largest remnants of Atlantic Forest in northeastern Brazil (Araújo et al., 1998), and is characterized by a high level of species

richness and endemism (Haffer, 1974; Mori et al., 1981; Brown, 1991; Martini et al., 2007).

According to Carnaval et al. (2009), the southern Bahia region acted as a bioclimatic refugium during the last glaciation, playing an important role regarding the diversification of amphibian species. However, the herpetofauna of the region is poorly known and new species of amphibians and reptiles are still frequently described from this region (Recoder et al., 2010; Napoli et al., 2011; Curcio et al., 2012; Lourenço-de-Moraes et al., 2012; Caramaschi et al., 2013; Teixeira Jr. et al., 2013; Rodrigues et al., 2013).

In this study we present a rapid inventory of herpetofauna of four different sites located inside the “APA of Lagoa Encantada and Rio Almada”.

Methodology

The present inventory was undertaken in the region of the watershed of the Almada River and the APA (Environmental Protection Area) of the Lagoa Encantada and Rio Almada, within the Central Corridor of the Atlantic Forest - a biodiversisty hotspot in southern Bahia state, northeast Brazil.

Field work was done in four different areas, represented by three points in each area (Figure 1; Table 1). The selected areas were: Serra dos Sete Paus at the boundary of the municipalities of Floresta Azul and Almadina;

Herpetology Notes, volume 7: 627-637 (2014) (published online on 12 November 2014)

Rapid inventory of herpetofauna at the APA (Environmental Protection Area) of the Lagoa Encantada

and Rio Almada, Southern Bahia, Brazil

Iuri Ribeiro Dias1*, Caio Vinicius de Mira-Mendes1 and Mirco Solé1

1 Universidade Estadual de Santa Cruz, Departamento de Ciências Biológicas, Rodovia Ilhéus-Itabuna, km 16, 45662-000 Ilhéus, Bahia, Brazil

* Corresponding author e-mail: [email protected]

Abstract. Southern Bahia has one of the largest remnants of Atlantic Forest in northeastern Brazil, sheltering high levels of species richness and endemisms. In the present study, we report the results of a rapid inventory comprehending 12 days of samplings at the APA of the Lagoa Encantada and Rio Almada. We recorded 76 species belonging to the herpetofauna, being 59 anurans and 17 reptiles. This high species richness recorded in just a few days reveals the biological importance of this area, and probably a larger effort would lead to recording more species.

Keywords. Atlantic Forest, conservation, endemism, Anura, Squamata

Iuri Ribeiro Dias et al.628

Serra do Corcovado in Almadina municipality; Lagoa Encantada and Serra da Temerosa both in Ilhéus municipality .

The main forest types found during the study were the Tropical Montane Rainforest and the Tropical Submontane Rainforest, except in the Lagoa Encantada

area, where the predominant vegetation type was the Tropical Lowland Rainforest. In general, the sampled forest fragments were located in hilly environments (except the points of Lagoa Encantada area, located in lowlands), in a good conservation condition and usually surrounded by cocoa plantations and / or pasture. The points sampled in the Lagoa Encantada area were located between two protected areas, the Parque Estadual da Serra do Conduru and the Private Natural Heritage Reserve (RPPN) Salto Apepique.

According to Köppen (1936), the climate of the region is Af (Tropical rainforest climate), characterized as hot and humid without a defined dry season. The mean monthly temperature ranges from 19.3-29ºC with an annual average around 23.2ºC, the relative humidity varies from 82.2-87.4% and precipitation is 1722 mm annually (Mendonça et al., 1996).

Fieldwork was carried out between 11 and 22 February 2011. Each area was sampled during three consecutive days (16:00h – 00:00h) by two researchers, each point being sampled only once. As the aim was to make a rapid inventory, we used visual surveys (Fitch 1987) in order to maximize sampling effort. For anurans we also used the method of visual and acoustic encounter

Figure 1. Map showing the limits of the APA of the Lagoa Encantada and Rio Almada, Bahia State, Northeastern Brazil and sampling points. Green spots are forest remnants of the Atlantic Forest in the region.

Sites Latitude Longitude Elevation-14.753981º -39.691841º 676 m -14.762575º -39.649557º 482 m Serra do Sete Paus -14.777635º -39.614061º 502 m -14.700045º -39.610872º 534 m -14.700156º -39.596010º 712 m Serra do Corcovado-14.698954º -39.602816º 881 m -14.473733º -39.447763º 509 m -14.487317º -39.450760º 559 m Serra da Temerosa -14.475027º -39.437438º 415 m -14.563973º -39.105011º 101 m -14.534158º -39.115587º 112 m Lagoa Encantada -14.582963º -39.117962º 94 m

Table 1. Geographical coordinates in decimal degrees (Datum = WGS84) of the sampled points inside the APA Lagoa Encantada and Rio Almada.

Rapid inventory of herpetofauna at environmental protection areas in Brazil 629

surveys (Rödel and Ernst, 2004) and accidental sightings (species found during displacement between sampling points). We used trails within the forest fragments, where we inspected every potential microenvironment for the occurrence of amphibians and reptiles (e.g. leaf litter, under trunks, rocks, bromeliads, streams). We also inspected the permanent and temporary ponds located at the study site. Species were identified in the field and photographed, when possible.

The rarefaction curve for amphibians was generated based on the Mao Tau estimator (after 1000 randomizations) (Colwell and Coddington, 1994). For the extrapolation of species richness, five different estimators were used: Jacknife 1, Chao 1, ACE, ICE and Bootstrap. Each sampling day was considered as a sampling unit. The program EstimateS 9.1 (Cowell, 2013) was used for the calculations.

Results and Discussion

During the period of the study we recorded 76 species belonging to the herpetofauna, being 59 anurans and 17 reptiles (Table 2; Figure 2, 3 and 4). The number of recorded species is very high, considering that only 12 days were spent to sample the study area. According to IUCN (2013), 36 of the recorded anuran species are not threatened (LC), 9 are listed as data deficient (DD) and the conservation status of twelve have not been classified yet. Allobates olfersioides is considered vulnerable to extinction and Aplastodiscus cf. weygoldi is classified as near threatened by the IUCN. Of the 17 reptile species, only two have been evaluated by IUCN (Salvator merianae and Tropidurus torquatus), which are classified as not threatened (LC).

The rarefaction curve for amphibian species indicated a slight tendency towards stabilization from the ninth day of sampling, being that only two species were added towards the end of samplings (Figure 5). Although the sampling effort employed in the study area was relatively small, it was possible to record a considerable number of species, between 90-96% of the species richness indicated by the estimators (Jacknife 1 = 65.4; Bootstrap = 62.8; ICE = 62.6; ACE = 61.9; Chao 1 = 61.1 species), revealing that sampling was qualitatively satisfactory during the study period.

Compared with other studies from the southern Bahia region, the APA of the Lagoa Encantada and Rio Almada shows a high herpetofauna species richness (59 anurans and 17 reptiles) (Table 3). The high species richness can be attributed to the large extent of the study area. Although the sampling sites are all located within the

APA of Lagoa Encantada and Rio Almada, points can be located up to 50 km away from each other, covering both lowland areas as hilly environments, which gives the study area a structural, climatic and geological heterogeneity.

Most studies published from southern Bahia were made with a sampling effort of a few days in the field and still recorded a high richness (Table 3). However, the region still lacks systematic long-term studies which would allow a better understanding of the local amphibian and reptile diversity, especially for the group of reptiles (Table 3) for which only one long-term study (12 years) addressing the snakes of the cocoa region of southern Bahia (Argôlo, 2004) has been performed until today. In this study, we made a rapid inventory lasting 12 days, and probably a larger effort would lead to the record of more species at this region and probably to the discovery of species new to science.

The amphibian species found can be considered as typical of the Atlantic forest, with 75% of the species being endemic of this domain, and six species endemic of Bahia (Haddad et al., 2013; Table 2). In this study, 48% of the anuran species were found only in forest environments.

Figure 5. Rarefaction curve of observed species richness of anuran amphibians sampled in from APA Lagoa Encantada and Rio Almada, based on the number of sampling days. Dashed lines denote the threshold of the 95% confidence intervals.

Family / Species A1 A2 A3 A4 IUCN

AMPHIBIAANURA

AromobatidaeAllobates olfersioides (Lutz, 1925) # - - - X VU

BufonidaeRhinella crucifer (Wied-Neuwied, 1821) # X X - X LC

Rhinella granulosa (Spix, 1824) - - X X LC

Rhinella hoogmoedi Caramaschi & Pombal, 2006 # X - X X LC

Rhinella jimi (Stevaux, 2002) X X - X LC

CentrolenidaeVitreorana eurygnatha (A. Lutz, 1925) # - X - - LC

Craugastoridae"Eleutherodactylus" bilineatus (Bokermann, 1975) † - X - - LC

Haddadus binotatus (Spix, 1824) # X X X X LC

Pristimantis paulodutrai (Bokermann, 1975) # X X X X LC

Pristimantis sp. X X X X -

Pristimantis vinhai (Bokermann, 1975) # X X X X LC

HemiphractidaeGastrotheca pulchra Caramaschi & Rodrigues, 2007 # X X - X DD

EleutherodactylidaeAdelophryne sp. 1 - - - X -

Adelophryne sp. 2 X - X - -

HylidaeAgalychnis aspera (Peters, 1873) † - - X - LC

Aplastodiscus ibirapitanga (Cruz, Pimenta & Silvano, 2003) # X X - X LC

Aplastodiscus sibilatus (Cruz, Pimenta & Silvano, 2003) # - - X - DD

Aplastodiscus cf. weygoldti * X X - - NT

Bokermannohyla capra Napoli & Pimenta, 2009 † - X X - -

Dendropsophus bipunctatus (Spix, 1824) # - - X - LC

Dendropsophus branneri (Cochran, 1948) X X X X LC

Dendropsophus cf. oliverai (Bokermann, 1963) X X X LC

Dendropsophus elegans (Wied-Neuwied, 1824) # X X X X LC

Table 2. List of sampled amphibians and reptiles from APA Lagoa Encantada and Rio Almada. Legend: A1 = Serra dos Sete Paus; A2 = Serra do Corcovado; A3 = Lagoa Encantada; A4 = Serra da Temerosa; # Endemic of biome Atlantic Rain Forest; † = endemic of Atlantic Rain Forest in state of Bahia; * = only acoustic record.

Dendropsophus haddadi (Bastos & Pombal, 1996) # - - - X LC

Dendropsophus minutus (Peters, 1872) - - X - LC

Dendropsophus novaisi (Bokermann, 1968) - X - X DD

Hypsiboas albomarginatus (Spix, 1824) # X X X X LC

Hypsiboas atlanticus (Caramaschi & Velosa, 1996) # - - X X LC

Hypsiboas crepitans (Wied-Neuwied, 1824) X X - X LC

Hypsiboas exastis (Caramaschi & Rodrigues, 2003) # X X X X DD

Hypsiboas faber (Wied-Neuwied, 1821) # X X X X LC

Hypsiboas pombali (Caramaschi, Pimenta & Feio, 2004) # X X X - LC

Hypsiboas semilineatus (Spix, 1824) # - - X - LC

Phasmahyla spectabilis Cruz, Feio & Nascimento, 2008 # X X - - DD

Phyllodytes cf. maculosus Cruz, Feio, and Cardoso, 2007 * X X - X DD

Phyllodytes melanomystax Caramaschi, Da Silva & Britto-Pereira, 1992 #* X - X X LC

Phyllodytes sp. 1* X X X X -

Phyllodytes sp. 2* X X - - -

Phyllodytes sp. 3* - X - X -

Phyllodytes sp. 4* - - X - -

Phyllodytes sp. 5* X X X X -


Family / Species A1 A2 A3 A4 IUCN

AMPHIBIA

ANURAHylidaePhyllomedusa burmeisteri Boulenger, 1882 # X X X X LC

Phyllomedusa nordestina Caramaschi, 2006 X X X X DD

Phyllomedusa rohdei Mertens, 1926 # - - X - LC

Scinax alter (Lutz, 1973) * # - - X - LC

Scinax argyreornatus (Miranda-Ribeiro, 1926) # - X X - LC

Scinax cf. x-signatus X X X X LC

Scinax eurydice (Bokermann, 1968) # - X X X LC

Scinax juncae Nunes & Pombal, 2010 # X X - X -

Scinax strigilatus (Spix, 1824) † - X - X DD

Scinax sp. - - - X -

Sphaenorhynchus prasinus Bokermann, 1973 # X - X X LC

LeptodactylidaeLeptodactylus fuscus (Schneider, 1799) X X X X LC

Leptodactylus cf. latrans (Steffen, 1815) X X X X LC

Leptodactylus mystaceus (Spix, 1824) - - - X LC

Physalaemus camacan Pimenta, Cruz & Silvano, 2005 † X - X X DD

Physalaemus erikae Cruz & Pimenta, 2004 † - X X X LC

OdontophrynidaeProceratophrys renalis (Miranda-Ribeiro, 1920) # - - X X -

Proceratophrys schirchi (Miranda-Ribeiro, 1937) #* - X - - LC

REPTILIA

SQUAMATA LIZARDS

DactyloidaeAnolis fuscoauratus D'Orbigny, 1837 X X - X -Gymnophthalmidae Leposoma cf. scincoides Spix, 1825 X X - - -Leiosauridae Enyalius cf. catenatus (Wied, 1821) X X X X -

Table 2. Continued.

y ( , )

SphaerodactylidaeColeodactylus meridionalis (Boulenger, 1888) - - X X -

TeiidaeAmeiva ameiva (Linnaeus, 1758) - - X - -Tupinambis merianae (Duméril & Bibron, 1839) - - X - -TropiduridaeTropidurus torquatus (Wied-Neuwied, 1820) - - - X -

SNAKESColubridaeChironius fuscus (Linnaeus, 1758) - X - - -Oxybelis aeneus (Wagler, 1824) X - - - -DipsadidaeErythrolamprus taeniogaster (Jan, 1866) - - X - -Oxyrhopus formosus (Wied, 1820) - X - - -Oxyrhopus petolarius (Linnaeus, 1758) - - - X -Sibynomorphus neuwiedi (Ihering, 1911) - X - X -ViperidaeBothrops bilineata (Wied, 1825) X - - X -Bothrops jararaca (Wied, 1824) X X - - -Bothrops leucurus Wagler, 1824 - - - X -

Total species of anurans 33 38 38 40 -Total species of reptiles 6 7 5 8


Salvator

We also expand the geographic distribution of Aplastodiscus sibilatus (Figure 2.H) from Igrapiúna municipality (Camurugi et al. 2010) to the “Lagoa

Encantada” (near 80 km south). Thus, the nearby areas of Lagoa Encantada now constitute the southern limit of distribution of this species.

Figure 2. Some amphibian species from APA Lagoa Encantada and Rio Almada, Bahia State, Northeastern Brazil. a) Rhinella granulosa; b) R. hoogmoedi; c) Vitreorana eurygnatha; d) Haddadus binotatus; e) Gastrotheca pulchra; f) Adelophryne sp.; g) Aplastodiscus ibirapitanga; h) A. sibilatus; i) Bokermannohyla capra; j) Dendropsophus bipunctatus; l) D. elegans; m) D. minutus; n) Agalychnis aspera; o) Hypsiboas exastis and p) H. faber. Photos by I. R. Dias.


Figure 3. Some amphibian species from APA Lagoa Encantada and Rio Almada, Bahia State, Northeastern Brazil. a) Hypsiboas semilineatus; b) Phasmahyla spectabilis; c) Phyllomedusa nordestina; d) P. rohdei; e) Scinax sp.; f) S. strigilatus; g) Leptodactylus cf. latrans; h) L. mystaceus; i) Physalaemus camacan and j) Proceratophrys renalis. Photos by I. R. Dias.


The species Phasmahyla spectabilis, Aplastodiscus cf. weygoldti and Vitreorana eurygnatha have a restricted distribution to Bahia state, and are known from less than five locations (Freitas et al., 2004; Pimenta et al., 2005; Freitas et al., 2007; Cruz et al., 2008; Tinoco et al., 2008; Dias et al., 2011; Silva et al., 2012). During this study, we added new points of occurrence of these species.

Currently 11 species are recognized within the genus Phyllodytes (Frost, 2014). Species of this genus are intimately associated with bromeliads, performing all

their life cycles within these plants (Peixoto, 1995; Caramaschi et al., 2004). Due to this feature, many species occur in bromeliads in the canopy, hampering the study and collection of specimens for a better understanding of the diversity of the genus. Through the advertisement call we identified seven species of this genus in the study area, being five of them probably unknown to science. In other fieldworks, three of these species were collected and are in the process of taxonomic description. Thus, the diversity of this genus

Figure 4. Some reptiles species from APA Lagoa Encantada and Rio Almada, Bahia State, Northeastern Brazil. a) Anolis fuscoauratus; b) Enyalius cf. catenatus; c) Coleodactylus meridionalis; d) Oxybelis aeneus; e) Erythrolamprus taeniogaster; f) Oxyrhopus formosus; g) O. petolarius; h) Sibynomorphus neuwiedi; i) Bothrops bilineata (adult); j) B. bilineata (juvenile); l) B. jararaca and m) B. leucurus. Photos by I. R. Dias.


is underestimated, and probably southern Bahia is a hotspot for species of the genus Phyllodytes.

Among the reptiles, the records of Bothrops bilineatus and Oxyrhopus formosus need to be highlighted. Both species are considered uncommon in their occurrence areas and show disjunct distributions with populations in the Atlantic Forest and the Amazon (Dixon and Soini, 1986; Bailey, 1986; Cunha and Nascimento, 1993; Argôlo, 2004; Frota et al., 2005; Bernarde and Abe, 2006; Tonini et al., 2010). In a study conducted in southern Bahia during 14 years, 4680 snakes were

obtained, of which approximately 1% (63 individuals) belonged to the species B. bilineatus and only two to O. formosus (Argôlo, 2004). B. bilineatus was one of the viperids less abundant in the study area. Probably arboreal habits of this snake contribute to the difficulty of detection of this species in their area of distribution. Currently Oxyrhopus formosus is known only from four municipalities within the Atlantic forest domain: Mucuri - type locality (Bailey, 1986), Almadina and Coaraci in Bahia (Argôlo et al., 2012.); and Duas Barras in the state of Espírito Santo (Tonini et al., 2010).

Richness Localities

Anurans ReptilesTime

sampled Methodology References

APA of Lagoa Encantada and Rio Almada 59 17 12 days Active search This study

Porto Sul - Aritaguá -Ilhéus 50 24 24 days (2 months )

Active search and pitfall

Hydros/Orienta/Derba (2011)

Reserva Ecológica da Michelin - Igrapiúna 48 - 52 days

(13 months ) Active search

and pitfall Camurugi et al. 2010

Terminal Portuário da Ponta da Tulha - Ilhéus 47 26 59 days


and pitfall Biodinâmica/ Bamin,

2009

Parque Estadual da Serra do Conduru - Uruçuca, Itacaré e Ilhéus 45 17 13 days Active search

and pitfall Pimenta et al. 2005 ; Argolo et al. 2005

RPPN Estação Veracruz - Porto Seguro 39 - 4 days Active search Silvano & Pimenta,

2003

Projeto de Assentamento Zumbi dos Palmares - Camamu 32 - 4 days Active search Silvano & Pimenta,

2003

Reserva Sapiranga - Mata de São João 30 - 21 days


and pitfall Bastazini et al. 2007

Reserva Sapiranga - Mata de São João 25 - 15 days

(5 months ) Active search Juncá, 2006

RPPN Serra do Teimoso - Jussari 24 - 4 days Active search Silvano & Pimenta, 2003

Serra da Jiboia - Santa Terezinha e Elísio Medrado 22 - 12 days

(4 months ) Active search Juncá, 2006

Reserva Biológica de Una - Una 19 - 4 days Active search Silvano & Pimenta, 2003

Ecoparque de Una - Una 18 - 4 days Active search Silvano & Pimenta, 2003

Fazenda Caititu - Uruçuca 17 - 4 days Active search Silvano & Pimenta, 2003

Faz. Orion e Boa Sorte- Arataca 16 - 4 days Active search Silvano & Pimenta, 2003

Table 3. Number of anuran and reptile species found in areas within the Atlantic forest in southern Bahia with respective sampling effort and methods used in each study.


Final Remarks

Although the “APA of Lagoa Encantada and Rio Almada” represents a valuable local environmental heritage, several projects are being planned and / or implemented at the site (e.g. a new airport; the shipping terminal Porto Sul; and the West-East Integration railway). Thus, it is essential that these projects should be implemented with caution, aiming at an efficient environmental management that minimizes negative impacts on the fauna and flora of the region. Although still relatively little known, this reserve is of global importance due to its high biodiversity.

Acknowledgment. We are thankful to ECONAMFI Projetos & Pesquisas for supporting the research and Fábio Falcão and Tadeu T. Medeiros for the field assistance; IRD and CVMM are grateful to CAPES and FAPESB for grants. MS thanks CNPq for a research grant.

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Accepted by Miguel Vences


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