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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 ,

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

Abstract. Southern Bahia has one of the largest remnants of Atlantic Forest in northeastern Brazil, sheltering high levels of 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 . 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,

Introduction richness and endemism (Haffer, 1974; Mori et al., 1981; Brown, 1991; Martini et al., 2007). and reptiles are among the most According to Carnaval et al. (2009), the southern endangered groups of worldwide. The main Bahia region acted as a bioclimatic refugium during cause of their decline is associated to the loss and the last glaciation, playing an important role regarding fragmentation of the environment, especially in the the diversification of species. However, the Neotropics (Gibbons et al., 2000; Young et al., 2004; herpetofauna of the region is poorly known and new Stuart et al., 2004; Todd et al., 2009). species of amphibians and reptiles are still frequently The APA (Environmental Protection Area) of Lagoa described from this region (Recoder et al., 2010; Napoli Encantada, located in the municipality of Ilhéus, Bahia et al., 2011; Curcio et al., 2012; Lourenço-de-Moraes state, was established in June 14, 1993 (Bahia, 1993), et al., 2012; Caramaschi et al., 2013; Teixeira Jr. et al., with the main goal to protect the environmental heritage. 2013; Rodrigues et al., 2013). In 2003, the environmental protection area was renamed In this study we present a rapid inventory of the APA of Lagoa Encantada and Rio Almada, covering herpetofauna of four different sites located inside the the cities of Ilhéus, Uruçuca, Itajuípe, and “APA of Lagoa Encantada and Rio Almada”. Almadina, with an estimated total area of 157,745 ha, represented by remnants of the Atlantic Forest (Bahia, Methodology 2003). This region shelters one of the largest remnants of Atlantic Forest in northeastern Brazil (Araújo et al., The present inventory was undertaken in the region 1998), and is characterized by a high level of species of the watershed of the 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.

1 Universidade Estadual de Santa Cruz, Departamento de Field work was done in four different areas, represented Ciências Biológicas, Rodovia Ilhéus-, km 16, by three points in each area (Figure 1; Table 1). The 45662-000 Ilhéus, Bahia, Brazil selected areas were: Serra dos Sete Paus at the boundary * Corresponding author e-mail: [email protected] of the municipalities of and Almadina; 628 Iuri Ribeiro Dias et al.

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.

Serra do Corcovado in Almadina municipality; Lagoa area, where the predominant vegetation type was the Encantada and Serra da Temerosa both in Ilhéus Tropical Lowland Rainforest. In general, the sampled municipality . forest fragments were located in hilly environments The main forest types found during the study were (except the points of Lagoa Encantada area, located in the Tropical Montane Rainforest and the Tropical lowlands), in a good conservation condition and usually Submontane Rainforest, except in the Lagoa Encantada 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. Table 1. Geographical coordinates in decimal degrees According to Köppen (1936), the climate of the region (Datum = WGS84) of the sampled points inside the APA is Af (Tropical rainforest climate), characterized as hot Lagoa Encantada and Rio Almada. and humid without a defined dry season. The mean monthly temperature ranges from 19.3-29ºC with an Sites Latitude Longitude Elevation -14.753981º -39.691841º 676 m annual average around 23.2ºC, the relative humidity Serra do Sete Paus -14.762575º -39.649557º 482 m varies from 82.2-87.4% and precipitation is 1722 mm -14.777635º -39.614061º 502 m annually (Mendonça et al., 1996). -14.700045º -39.610872º 534 m Fieldwork was carried out between 11 and 22 February Serra do Corcovado -14.700156º -39.596010º 712 m -14.698954º -39.602816º 881 m 2011. Each area was sampled during three consecutive -14.473733º -39.447763º 509 m days (16:00h – 00:00h) by two researchers, each point Serra da Temerosa -14.487317º -39.450760º 559 m being sampled only once. As the aim was to make a -14.475027º -39.437438º 415 m -14.563973º -39.105011º 101 m rapid inventory, we used visual surveys (Fitch 1987) Lagoa Encantada -14.534158º -39.115587º 112 m in order to maximize sampling effort. For anurans we -14.582963º -39.117962º 94 m also used the method of visual and acoustic encounter Rapid inventory of herpetofauna at environmental protection areas in Brazil 629 surveys (Rödel and Ernst, 2004) and accidental sightings APA of Lagoa Encantada and Rio Almada, points can (species found during displacement between sampling be located up to 50 km away from each other, covering points). We used trails within the forest fragments, both lowland areas as hilly environments, which gives where we inspected every potential microenvironment the study area a structural, climatic and geological for the occurrence of amphibians and reptiles (e.g. leaf heterogeneity. litter, under trunks, rocks, bromeliads, streams). We also Most studies published from southern Bahia were inspected the permanent and temporary located made with a sampling effort of a few days in the field at the study site. Species were identified in the field and and still recorded a high richness (Table 3). However, photographed, when possible. the region still lacks systematic long-term studies The rarefaction curve for amphibians was generated which would allow a better understanding of the local based on the Mao Tau estimator (after 1000 amphibian and diversity, especially for the group randomizations) (Colwell and Coddington, 1994). For of reptiles (Table 3) for which only one long-term study the extrapolation of species richness, five different (12 years) addressing the of the cocoa region of estimators were used: Jacknife 1, Chao 1, ACE, ICE southern Bahia (Argôlo, 2004) has been performed until and Bootstrap. Each sampling day was considered as today. In this study, we made a rapid inventory lasting a sampling unit. The program EstimateS 9.1 (Cowell, 12 days, and probably a larger effort would lead to the 2013) was used for the calculations. record of more species at this region and probably to the discovery of species new to science. Results and Discussion The amphibian species found can be considered as During the period of the study we recorded 76 species typical of the Atlantic forest, with 75% of the species belonging to the herpetofauna, being 59 anurans and being endemic of this domain, and six species endemic 17 reptiles (Table 2; Figure 2, 3 and 4). The number of Bahia (Haddad et al., 2013; Table 2). In this study, of recorded species is very high, considering that only 48% of the anuran species were found only in forest 12 days were spent to sample the study area. According environments. 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 Figure 5. Rarefaction curve of observed species richness of shows a high herpetofauna species richness (59 anurans anuran amphibians sampled in from APA Lagoa Encantada and 17 reptiles) (Table 3). The high species richness and Rio Almada, based on the number of sampling days. can be attributed to the large extent of the study area. Dashed lines denote the threshold of the 95% confidence Although the sampling sites are all located within the intervals. 630 Iuri Ribeiro Dias et al.

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.

Family / Species A1 A2 A3 A4 IUCN AMPHIBIA ANURA Aromobatidae Allobates olfersioides (Lutz, 1925) # - - - X VU Bufonidae Rhinella 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 Centrolenidae Vitreorana eurygnatha (A. Lutz, 1925) # - X - - LC "Eleutherodactylus" bilineatus (Bokermann, 1975) † - X - - LC 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 Hemiphractidae Gastrotheca pulchra Caramaschi & Rodrigues, 2007 # X X - X DD Adelophryne sp. 1 - - - X - Adelophryne sp. 2 X - X - - Agalychnis aspera (Peters, 1873) † - - X - LC Aplastodiscus (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

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 - Rapid inventory of herpetofauna at environmental protection areas in Brazil 631

Table 2. Continued.

Family / Species A1 A2 A3 A4 IUCN AMPHIBIA ANURA Hylidae Phyllomedusa burmeisteri Boulenger, 1882 # X X X X LC Phyllomedusa Caramaschi, 2006 X X X X DD Phyllomedusa rohdei Mertens, 1926 # - - X - LC 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 Leptodactylidae Leptodactylus 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 Pimenta, Cruz & Silvano, 2005 † X - X X DD Physalaemus erikae Cruz & Pimenta, 2004 † - X X X LC Odontophrynidae Proceratophrys renalis (Miranda-Ribeiro, 1920) # - - X X - Proceratophrys schirchi (Miranda-Ribeiro, 1937) #* - X - - LC REPTILIA SQUAMATA Anolis fuscoauratus D'Orbigny, 1837 X X - X - Gymnophthalmidae Leposoma cf. scincoides Spix, 1825 X X - - - Leiosauridae Enyaliusy cf. catenatus (,)(Wied, 1821) X X X X - Sphaerodactylidae Coleodactylus meridionalis (Boulenger, 1888) - - X X - Teiidae Ameiva ameiva (Linnaeus, 1758) - - X - - TupinambisSalvator merianae (Duméril & Bibron, 1839) - - X - - Tropiduridae Tropidurus torquatus (Wied-Neuwied, 1820) - - - X - SNAKES Chironius fuscus (Linnaeus, 1758) - X - - - Oxybelis aeneus (Wagler, 1824) X - - - - Dipsadidae Erythrolamprus taeniogaster (Jan, 1866) - - X - - formosus (Wied, 1820) - X - - - (Linnaeus, 1758) - - - X - Sibynomorphus neuwiedi (Ihering, 1911) - X - X - Viperidae Bothrops 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 8 632 Iuri Ribeiro Dias et al.

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.

We also expand the geographic distribution of Encantada” (near 80 km south). Thus, the nearby areas Aplastodiscus sibilatus (Figure 2.H) from Igrapiúna of Lagoa Encantada now constitute the southern limit of municipality (Camurugi et al. 2010) to the “Lagoa distribution of this species. Rapid inventory of herpetofauna at environmental protection areas in Brazil 633

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. 634 Iuri Ribeiro Dias et al.

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) ; 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.

The species Phasmahyla spectabilis, Aplastodiscus cf. their life cycles within these plants (Peixoto, 1995; weygoldti and Vitreorana eurygnatha have a restricted Caramaschi et al., 2004). Due to this feature, many distribution to Bahia state, and are known from less than species occur in bromeliads in the canopy, hampering five locations (Freitas et al., 2004; Pimenta et al., 2005; the study and collection of specimens for a better Freitas et al., 2007; Cruz et al., 2008; Tinoco et al., 2008; understanding of the diversity of the . Through the Dias et al., 2011; Silva et al., 2012). During this study, advertisement call we identified seven species of this we added new points of occurrence of these species. genus in the study area, being five of them probably Currently 11 species are recognized within the genus unknown to science. In other fieldworks, three of Phyllodytes (Frost, 2014). Species of this genus are these species were collected and are in the process of intimately associated with bromeliads, performing all taxonomic description. Thus, the diversity of this genus Rapid inventory of herpetofauna at environmental protection areas in Brazil 635

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.

Richness Time Localities Methodology References Anurans Reptiles sampled APA of Lagoa Encantada and Rio 59 17 12 days Active search This study Almada

24 days Active search Hydros/Orienta/Derba Porto Sul - Aritaguá -Ilhéus 50 24 (2 months ) and pitfall (2011)

Reserva Ecológica da Michelin - 52 days Active search 48 - Camurugi et al. 2010 Igrapiúna (13 months ) and pitfall

Terminal Portuário da Ponta da 59 days Active search Biodinâmica/ Bamin, 47 26 Tulha - Ilhéus (5 months ) and pitfall 2009

Parque Estadual da Serra do Active search Pimenta et al. 2005 ; 45 17 13 days Conduru - Uruçuca, Itacaré e Ilhéus and pitfall Argolo et al. 2005

RPPN Estação Veracruz - Porto Silvano & Pimenta, 39 - 4 days Active search Seguro 2003

Projeto de Assentamento Zumbi dos Silvano & Pimenta, 32 - 4 days Active search Palmares - 2003

Reserva Sapiranga - Mata de São 21 days Active search 30 - Bastazini et al. 2007 João (3 months ) and pitfall

Reserva Sapiranga - Mata de São 15 days 25 - Active search Juncá, 2006 João (5 months )

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

Serra da Jiboia - Santa Terezinha 12 days 22 - Active search Juncá, 2006 e Elísio Medrado (4 months )

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

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

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

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

is underestimated, and probably southern Bahia is a obtained, of which approximately 1% (63 individuals) hotspot for species of the genus Phyllodytes. belonged to the species B. bilineatus and only two to Among the reptiles, the records of Bothrops bilineatus O. formosus (Argôlo, 2004). B. bilineatus was one of and Oxyrhopus formosus need to be highlighted. Both the viperids less abundant in the study area. Probably species are considered uncommon in their occurrence arboreal habits of this contribute to the difficulty areas and show disjunct distributions with populations of detection of this species in their area of distribution. in the Atlantic Forest and the Amazon (Dixon and Currently Oxyrhopus formosus is known only from four Soini, 1986; Bailey, 1986; Cunha and Nascimento, municipalities within the Atlantic forest domain: 1993; Argôlo, 2004; Frota et al., 2005; Bernarde and - type locality (Bailey, 1986), Almadina and Coaraci in Abe, 2006; Tonini et al., 2010). In a study conducted Bahia (Argôlo et al., 2012.); and Duas Barras in the state in southern Bahia during 14 years, 4680 snakes were of Espírito Santo (Tonini et al., 2010). 636 Iuri Ribeiro Dias et al.

Final Remarks Camurugi, F. Lima, T.M., Mercês, E.A., Juncá, F.A. (2010): Anuros da Reserva Ecológica da Michelin, Município de Igrapiúna, Although the “APA of Lagoa Encantada and Rio Estado da Bahia, Brasil. Biota Neotropica 10(2): 305–312. Almada” represents a valuable local environmental Caramaschi U., Orrico, V.G.D., Faivovich, J., Dias I.R., Solé, M. heritage, several projects are being planned and / or (2013): A new species of Allophryne (Anura: Allophrynidae) implemented at the site (e.g. a new airport; the shipping from the Atlantic Rain Forest Biome of eastern Brazil. terminal Porto Sul; and the West-East Integration Herpetologica 69: 480–491. railway). Thus, it is essential that these projects should Caramaschi, U., Peixoto, O.L., Rodrigues, M.T. (2004): be implemented with caution, aiming at an efficient Revalidation and redescription of Phyllodytes wuchereri (Peters, 1873) (Amphibia, Anura, Hylidae). 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