Herpetofauna in Two Habitat Types (Tabuleiros and Stational Semidecidual Forest) in the Reserva Biológica Guaribas, Northeastern Brazil

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Herpetology Notes, volume 11: 455-474 (2018) (published online on 28 May 2018)

Herpetofauna in two habitat types (tabuleiros and Stational Semidecidual Forest) in the Reserva Biológica Guaribas, northeastern Brazil

Daniel O. Mesquita1,*, Brygida C.F. Alves2, Carmem K.B. Pedro1, Daniel O. Laranjeiras1, Francis L.S. Caldas3, Isabella M.M.C. Pedrosa1, Jefter B. Rodrigues1, Leandro O. Drummond4, Lucas B.Q. Cavalcanti1, Milena Wachlevski5, Paulo Nogueira-Costa6, Rafaela C. França7 and Frederico G.R. França2

Abstract. We present a detailed list of the reptiles and amphibians occurring in two habitat types (tabuleiros and Stational Semidecidual Forest) in the Reserva Biológica Guaribas (REBIO Guaribas), Paraíba State, northeastern Brazil. We sampled species using pitfall traps, transects, and during active searches. We recorded a total of 106 species, including 20 lizards, seven amphisbaenians, 42 snakes, one turtle, two crocodilians, and 34 frogs. Of these, five lizards, six snakes, 14 frogs, seven amphisbaenians, and the turtle were new records for REBIO Guaribas. The frog and snake rarefaction curves reached the asymptote, indicating that we achieved a good estimate of species richness for those taxa. The herpetofauna in REBIO Guaribas is composed of species typical for both forested biomes and open areas. The open areas in REBIO Guaribas occur within an Atlantic Forest matrix and are locally known as tabuleiros, which present typical elements of cerrado savannahs, reinforcing the importance of the open areas in species composition and maintenance of regional fauna. We outline the importance of long-term inventories, such as in REBIO Guaribas, especially due to the higher number of rare species found, which provides essential information for species and habitat management.

Keywords: Herpetofauna, Reserva Biológica Guaribas, tabuleiros, savannahs, endemism, new records, Brazil

Introduction Amphibians and reptiles represent an important component of an area’s biodiversity because they have essential ecological functions in natural assemblages 1 Centro de Ciências Exatas e da Natureza, Departamento de (e.g., Colli et al., 2002; Costa et al., 2007; Brites et al., Sistemática e Ecologia Universidade Federal da Paraíba, 2009). Due to their abundance and the relative ease with João Pessoa, PB 58051-900, Brazil which they can generally be located, identified, and 2 Centro de Ciências Aplicadas e Educação, Campus IV, Litoral studied, amphibians and reptiles are commonly used Norte, Universidade Federal da Paraíba, Rio Tinto, PB to identify areas and priorities for conservation (Diniz- 58297-000, Brazil 3 Filho et al., 2004; Vitt et al., 2007). In addition, the Faculdades Integradas de Sergipe, Largo Glicério Cerqueira number of undescribed species remains high in many 387, Centro, Tobias Barreto, SE 35690-000, Brazil 4 Departamento de Ecologia, Laboratório de Vertebrados, CP places and examples of such discoveries are plentiful 68020, Universidade Federal do Rio de Janeiro, Ilha do (e.g., Brandão, 2002; Colli et al., 2003a,b; Giugliano et Fundão, Rio de Janeiro, RJ 21941-901, Brazil al., 2013). The neotropical region harbours enormous 5 Centro de Ciências Biológicas e da Saúde, Universidade biodiversity, and a significant centre of endemism in Federal Rural do Semi-Árido, Mossoró, RN 59625-900, eastern Brazil is Atlantic Forest (e.g., Rocha et al., 2003; Brazil 6 Mittermeier et al., 2005; Ribeiro et al., 2009). Departamento de Ecologia, IBRAG, Universidade do Estado Originally, Atlantic Forest covered an area of do Rio de Janeiro, Rua São Francisco Xavier 524, Maracanã, Rio de Janeiro, RJ 20550-019, Brazil approximately 1,500,000 km2 along the east coast 7 Programa de Pós-graduação em Ecologia e Conservação da of Brazil and ranging into the interior of the country Biodiversidade, Universidade Estadual de Santa Cruz, CEP (Ab’Saber, 1977), but since the arrival of European 45662-900 – Salobrinho, BA, Brazil colonists deforestation has devastated the area * Corresponding author. E-mail: [email protected] 456 Daniel O. Mesquita et al.

Figure 1. SEMAs and sampling sites in the Reserva Biológica Guaribas, Mamanguape and Rio Tinto Municipalities, Paraíba State, Brazil. Circles indicate pitfall traps (red), transects (green), Visual Encounter Surveys (VES, orange), and VES coupled with pitfall traps (blue).

(PROBIO, 2002). Currently, only 8% of original Tabuleiros are poorly known savannahs that comprise Atlantic Forest remains, with undisturbed areas almost sandy soils in more elevated landscapes without marine completely absent (PROBIO, 2002). Due to the high influence; they are a distinct part of the Atlantic Forest level of diversity and intense pressure from human biome. Structurally, they are similar to coastal restingas, development, the Atlantic Forest is considered a despite the absence of marine influence (Oliveira Filho hotspot for global biodiversity conservation (Myers et and Carvalho, 1993). They are dominated by typical al., 2000). It harbours more than 20,000 vascular plant cerrado species of herbaceous, shrubby, and arboreal species (8000 endemics), 250 mammal species (55 strata, and mainly exist as patches of savannahs endemics, of which 35 are endangered), and 1020 bird (Oliveira Filho and Carvalho, 1993; Barbosa et al., species (188 endemic, 104 endangered) (Tabarelli et al., 2011). They occur in continuous areas between Natal 2005). Considering the herpetofauna, approximately and Touros, Rio Grande do Norte State, and form 457 amphibian species (90 endemics, 27 endangered) mosaics along the coast of Paraíba State, where forest and 197 reptile species (90 endemics, 35 endangered) tends to occupy depressions while tabuleiros occupy have been documented (Marques et al., 2001; Silvano the more elevated areas. In addition, several plant and and Pimenta, 2003; Ribeiro et al., 2009; Haddad et animal species are shared with cerrado, and despite of al., 2013). Due its great extent, Atlantic Forest is an the fact that the biogeographical relationship between extremely heterogeneous biome, dominated by tropical these two environments have not yet been elucidated, pluvial forests that are more seasonal when more distant tabuleiros are considered isolated cerrado-like areas from the coast. Many distinct ecosystems are associated within an Atlantic Forest matrix (Oliveira Filho and with this environment, such as the araucarias forests Carvalho, 1993). in the south, mangroves, coastal restingas, the isolated The cerrado is a large and diverse ecoregion in central forest patches in northeast called brejos, and the isolated and southern Brazil that covers an area of approximately tabuleiros (Tabarelli and Santos, 2004; Tabarelli et al., 2,000,000 km2, nearly 25% of the country. Cerrado 2005, 2006). includes forests, where arboreal species dominate; Herpetofauna in two habitat types in the Reserva Biológica Guaribas, Brazil 457 savannahs, with trees and shrubs dispersed on an 1995), and the tabuleiros in Paraíba State, which are herbaceous stratum; and grasslands, with herbaceous protected in REBIO Guaribas, which also includes part species and some shrubs (Ribeiro and Walter, 1998; of the Atlantic Forest known as Stational Semidecidual Oliveira and Marquis, 2002). Isolated patches of Forest (SSF; Oliveira Filho and Carvalho, 1993). There cerrado occur in northern and northeastern Brazil as is very little known about the amphibian and reptile scattered islands inside the Amazon Forest (Pires, 1973) assemblages in tabuleiros, with most information where they are known as tabuleiros (Oliveira Filho and only available in the unpublished management plan Carvalho, 1993). As is the case with plants, amphibians of the reserve; in general, these landscapes are poorly and reptiles also congregate with lower diversity than protected and highly threatened by human activity. Thus, in core cerrado areas, despite the relatively higher conducting inventories in these locations is imperative endemism rates (Ávila-Pires, 1995; Colli, 1996; to determine conservation priorities. Our objective was Mesquita et al., 2007). to perform a long-term herpetological inventory in the Tabuleiros are highly endangered by agricultural REBIO Guaribas and to compare the species richness of expansion, mining, cattle breeding, and human-caused tabuleiros and SSF sites. fire (Faleiro et al., 2008). Another problem is the near absence of conservation units covering these isolated Material and methods areas. Among the few isolated protected areas, we Study area.—We performed the study in REBIO highlight the Amapá State savannahs, even though Guaribas, located in the Mamanguape and Rio Tinto only 2% of its area is effectively protected (Cavalcanti, Municipalities, Paraíba State, northeastern Brazil (Fig. 1). The climate of this region is hot and humid according to the Köppen Classification, with an annual average temperature of approximately 24–26°C (Nimer, 1989). The area receives approximately 1750–2000 mm of rainfall per year, with rains starting in February and reaching their highest levels in April–July (MMA/ IBAMA, 2003). The dry season lasts two or three months, from October–December (Barbosa et al., 2011). According to its management plan, REBIO Guaribas is an integral protection conservation unit, with an area of approximately 4321 ha, comprising three disjunct areas known as SEMAs. SEMAs 1–3 comprise areas of 616.4 ha, 3378.2 ha, and 327.0 ha, respectively (Fig. 1). SEMA 1 and 2 comprise a mix of SSF and tabuleiros, while SEMA 3 includes only SSF. The landscape of REBIO Guaribas is predominantly flat, with an elevation below 100 m. Aside from savannah patches, the region also includes Atlantic Forest, which presents complex vegetation formations throughout its range (Oliveira Filho and Carvalho, 1993; Barbosa et al., 2011). Among the phytophysiognomies present in REBIO Guaribas, we highlight the tabuleiros and SSFs (Figs. 1, 2), savannahs that occur dispersed within forested areas and show high similarity with cerrado (Oliveira Filho and Carvalho, 1993). Figure 2. (Top) Typical vegetation types of Reserva Biológica Guaribas, showing the tabuleiros habitat with Stational The term “SEMA” does not appear to be an acronym, as no Semidecidual Forest (SSF) in the background. (Bottom) explanation for the word is given in the REBIO’s manage- Pitfall traps located in an SSF. Photos by Daniel O. Mesquita ment plan. It is simply a word to refer to the disjunct areas (tabuleiros), Daniel O. Laranjeiras (SSF). that comprise the REBIO. 458 Daniel O. Mesquita et al.

Data collection (Reptiles).—We installed 50 Y-shaped IUCN) were taken. The specimen preparation process pitfall trap arrays (25 in SSFs and 25 in tabuleiros) followed standard ethical guidelines (ASIH, 2004), and the Society for the Study of Amphibians and Reptiles using one 60-l bucket in the centre and one each at the and Conselho Brasileiro de Biologia (CFBio). All end of the three arms (each separated by an angle of animals were deposited in the herpetological collections 120°). Bucket locations were connected by three 5-m of the Universidade Federal da Paraíba (CHUFPB), the drift fences built from galvanized iron, for a total of 200 Universidade Federal da Paraíba in Rio Tinto (RT), the buckets (Fig. 2). Traps were checked twice per week for Universidade Federal Rural do Semi-Árido (UFERSA), five years (2008–2012). We also randomly performed the Coleção Herpetológica do Semiárido da Universidade visual encounter searches using rubber bands to collect Federal Rural do Semi-Árido (CHSA), the Fonoteca da animals, 3 days per month, from 0800–1700 h, during Universidade Federal do Semi-Árido (FNUFERSA), or 2008–2009. When the number of specimens reached the Museu Nacional at the Universidade Federal do Rio the maximum authorized by collecting permits, animals de Janeiro (UFRJ). were individually marked by toe clipping all lizards and Species were identified using the information in frogs and released in the same area (Heyer et al., 1994; Bokermann (1966), Peters and Orejas-Miranda Cechin and Martins, 2000; Ferner, 2007). All snakes (1986a,b), Vanzolini et al. (1980), Rodrigues (1987), and amphisbaenians were collected, since they never Ávila-Pires (1995), Colli et al. (2002), Vanzolini reached the maximum number authorized by collecting (2004), and Magalhães et al. (2015). We adopted the permits. nomenclature used in the Brazilian list of Amphibians Data collection (Amphibians).—Amphibians were and Reptiles (SBH, 2017a,b). Furthermore, we compared sampled in two different time periods during 2013, specimens with the animals housed at CHUFPB and using Visual Encounter Surveys and auditory searches UFRJ. in breeding and shelter sites (Crump and Scott, 1994; To evaluate the quality of the sampling effort, we Heyer et al., 1994). The first sampling took place constructed rarefaction curves for lizards, frogs, and during two 15-day field trips in the dry (January) and all the herpetofauna combined, based on individuals wet (June) seasons. The second sampling took place (Gotelli and Colwell, 2001), and used the Chao2P during a five-day field trip each month in the dry (May– species estimator (Lopez et al., 2012) in EstimateS 9.1 August) and wet (November–December) seasons. We (Colwell, 2013) and R (R Development Core Team, performed searches from 1800–0000 h, with at least 2015). We choose the Chao 2P species estimator three people, totalling 9720 person-hours of effort. because it produces very good estimates of species Additionally, we installed six pitfall trap arrays (three at richness using information from either well-sampled or each sampling site, pond, and or/stream) with four 30-l poorly-sampled areas (Lopez et al., 2012). The curves buckets arranged in the same pattern as described above, were obtained through 1000 resamplings of the original totalling 20 buckets (Cechin and Martins, 2000). data, with no reposition. We did not build chelonian or In addition, in the wet seasons of 2014 and 2015 crocodilian curves because these taxa were only rarely (18–24 July 2014 and 09–17 July 2015), we sampled present in a sample. amphibians in all three SEMAs using active search in straight transects restricted by time (20 min per transect Results with five observers) for ten consecutive nights each year. We documented 72 reptile species (20 lizards, seven In this case, the total sampling effort was 7100 person- amphisbaenians, 42 snakes, one turtle, two crocodilians) hours, with 2700 person-hours spent in the tabuleiros and 34 species of frogs (Table 1; Figs. 3–6). Twenty-five and 4400 person-hours in SSFs. species were recorded exclusively in open areas and 11 Specimens were collected according to permits species were reported exclusively in forested areas, granted by the appropriate agencies: FLSC (SISBIO while only six species were observed in both areas (Table # 36095-8) and MW (SISBIO # 41748-1). Specimens 1). Considering lizards, the REBIO Guaribas harbours captured were killed on the same day using a lethal similar proportions of species in open (15) and forested injection of lidocaine and preserved in a 10% solution areas (13), with only nine species shared between both of formalin. They were subsequently transferred to 70% areas (Table 1) and one exclusively in human habitations alcohol for long-term storage. No globally or locally (Hemidactylus mabouia). Considering snakes, most endangered species (e.g., listed as threatened by the species were typically found in open areas: 33 species Herpetofauna in two habitat types in the Reserva Biológica Guaribas, Brazil 459

Table 1. List of the herpetofauna observed at REBIO Guaribas during a long-term study (2008–2013). New records are indicated with an asterisk (*). Occurrences in boundary habitats, along the dirt roads delimiting the reserve, are reported separately, since sometimes we conducted active searches in these areas, which comprise a different set of environmental characteristics distinct from either tabuleiros or SSFs. Table 1.

Species Occurrence Voucher number Number of specimens Tabuleiros SSF Boundaries FROGS (34) Bufonidae (2) Rhinella crucifer* - x - CHUFPB 04362 8 Rhinella jimi x x x CHUFPB 07889 54 Craugastoridae (1) - - Pristimantis ramagii x x - CHUFPB 00472 378 Eleutherodactylidae (1) Adelophryne sp.* - x - CHSA.A 274 21 Hylidae (16) Dendropsophus branneri x - x CHUFPB 09027 146 Dendropsophus elegans x - x CHUFPB 10252 3 Dendropsophus minutus x - x CHUFPB 02189 266 Dendropsophus nanus x - x CHUFPB 09048 25 Dendropsophus oliveirai* x - x CHUFPB 00487 43 Hypsiboas albomarginatus x - x CHUFPB 07890 39 Hypsiboas faber x - - CHUFPB 07896 24 Hypsiboas raniceps x - x CHUFPB 10262 13 Phyllomedusa nordestina x - x CHUFPB 11217 32 Scinax auratus* x - - CHUFPB 09047 98 Scinax cretatus* x - - CHUFPB 01799 27 Scinax eurydice* x x - CHUFPB 07957 12 Scinax fuscomarginatus* x - x CHUFPB 13251 45 Scinax melanodactylus* x x - MNRJ 91050 121 Scinax nebulosus* - - x CHUFPB 12940 73 Scinax x-signatus x - x CHUFPB 11536 30 Leptodactylidae (11) Adenomera sp. x x x CHUFPB 12911 9 Leptodactylus fuscus - x x CHUFPB 12715 5 Leptodactylus macrosternum* x - x CHUFPB 11480 86 1 Leptodactylus natalensis - x x CHUFPB 07620 84 Leptodactylus troglodytes x - x CHUFPB 07632 15 Leptodactylus vastus x - x CHUFPB 09089 77 Physalaemus albifrons* - - x MNRJ 91054 5 Physalaemus cuvieri x - x CHUFPB 07909 30 Pleurodema diplolister* x - x CHUFPB 12717 39 Pseudopaludicola jaredi* - - x CHUFPB 11235 28 Pseudopaludicola mystacalis - - x FNUFERSA 054 1 Microhylidae (2) Dermatonotus muelleri x - x CHUFPB 07614 5 Elachistocleis cesarii* - x - CHUFPB 07888 3 Ranidae (1) Lithobates palmipes x x x CHUFPB 07959 138 CROCODILES Alligatoridae (2) Caiman latirostris - - x Visual Record* - Paleosuchus palpebrosus - x - Visual Record* - LIZARDS (27) Amphisbaenidae (7) Amphisbaena alba* x - - CHUFPB 05476 23 Amphisbaena lumbricaris* - - - RT 0267 4 Amphisbaena pretrei* - - - RT 0039 4 Amphisbaena vermicularis* - - - RT 0267 8 Amphisbaena sp. 1* - - - RT 0864 1 Amphisbaena sp. 2* - - - RT 0235 2 Leposternum polystegum* - - - RT 0220 2

ʹ Adenomera sp. x x x CHUFPB 12911 9 Leptodactylus fuscus - x x CHUFPB 12715 5 Leptodactylus macrosternum* x - x CHUFPB 11480 86 Leptodactylus natalensis - x x CHUFPB 07620 84 Leptodactylus troglodytes x - x CHUFPB 07632 15 Leptodactylus vastus x - x CHUFPB 09089 77 Physalaemus albifrons* - - x MNRJ 91054 5 Physalaemus cuvieri x - x CHUFPB 07909 30 Pleurodema diplolister* x - x CHUFPB 12717 39 Pseudopaludicola jaredi* - - x CHUFPB 11235 28 Pseudopaludicola mystacalis - - x FNUFERSA 054 1 Microhylidae (2) Dermatonotus muelleri x - x CHUFPB 07614 5 Elachistocleis cesarii* - x - CHUFPB 07888 3 Daniel O. Mesquita et al. 460 Ranidae (1) Lithobates palmipes x x x CHUFPB 07959 138 Table 4. CROCODILESContinued. Table 1. Alligatoridae (2) Species Caiman latirostris - Occurrence- x Vo Visualucher Record* number Number of- specimens Paleosuchus palpebrosus Tabuleiros- SSFx Boundaries - Visual Record* - FROGSLIZARDS (34) (27) BufonidaeAmphisbaenidae (2) (7) RhinellaAmphisbaena crucifer alba* * x- x- - CHUFPB 0547604362 238 RhinellaAmphisbaena jimi lumbricaris* x- x- x - CHUFPBRT 0267 07889 544 CraugastoridaeAmphisbaena (1) pretrei * - - - RT 0039 4 PristimantisAmphisbaena ramagii vermicularis * x- x- - CHUFPBRT 0267 00472 3878 EleutherodactylidaeAmphisbaena sp. (1) 1* - - - RT 0864 1 AdelophryneAmphisbaena sp. sp.* 2* - x- - CHSA.ART 0235 274 212 HylidaeLeposternum (16) polystegum* - - - RT 0220 2 DactyloidaeDendropsophus (2) branneri x - x CHUFPB 09027 146 DendropsophusDactyloa punctata elegans* x- x- x - CHUFPB 0366910252 373 DendropsophusNorops ortonii* minutus x- x- x - CHUFPB 1024402189 26610 ʹ GekkonidaeDendropsophus (1) nanus x - x CHUFPB 09048 25 DendropsophusHemidactylus mabouia oliveirai * x- - x CHUFPB 0088200487 438 GymnophthalmidaeHypsiboas albomarginatus (3) x - x CHUFPB 07890 39 HypsiboasCercosaura faber ocellata x - - CHUFPB 1101707896 243 HypsiboasDryadosaura raniceps nordestina x x- x- CHUFPB 0356110262 8131 PhyllomedusaMicrablepharus nordestina maximiliani x x- x- CHUFPB 0041911217 13291 * IguanidaeScinax (1) auratus x - - CHUFPB 09047 98 ScinaxIguana cretatusiguana * x x- x - CHUFPB 0312801799 276 * LeiosauridaeScinax eurydice (1) x x - CHUFPB 07957 12 ScinaxEnyalius fuscomarginatus catenatus* * x Data from CHUFPB- x C CHUFPBHUFPB 0264013251 451 * PhyllodactylidaeScinax melanodactylus (1) x x - MNRJ 91050 121 ScinaxGymnodactylus nebulosus geckoides* x- - x - CHUFPB 0746012940 6773 PolychrotidaeScinax x-signatus (2) x - x CHUFPB 11536 30 LeptodactylidaePolychrus acutirostris (11) * Data from CHUFPB CHUFPB 02595 1 Polychrus marmoratus* - x - CHUFPB 02591 4 Scincidae (3) Mabuya heathi x - - CHUFPB 03978 54 1 Mabuya macroryncha x x - CHUFPB 03959 39 Mabuya nigropunctata - x - CHUFPB 11014 8 Sphaerodactylidae (1) Coleodactylus meridionalis x x - CHUFPB 03248 99 Teiidae (4) Ameiva ameiva x x - CHUFPB 02650 116 Ameivulla ocellifera x - - CHUFPB 03745 671 Kentropyx calcarata x x - CHUFPB 02517 441 Salvator merianae x x x CHUFPB 11015 5 Tropiduridae (1) Tropidurus hispidus x x x CHUFPB 07284 156 SNAKES (42) 3 Boidae (2) Boa constrictor x - x CHUFPB 04930 5 Epicrates assisi x - x CHUFPB 13174 38 Colubridae (9) Chironius exoletus x - - CHUFPB 12276 3 Chironius flavolineatus x - x CHUFPB 12278 9 Drymarchon corais - x x RT 0005 3 Drymoluber dichrous x x x CHUFPB 12282 9 Leptophis ahaetulla* - x x CHUFPB 12308 11 Oxybelis aeneus x - x CHUFPB 12323 6 Spilotes pullatus x x x RT 0507 7 Spilotes sulphureus x - x RT 0132 4 Tantilla melanocephala x x x CHUFPB 04595 42 Dipsadidae (26) Apostolepis cearensis x x x RT 0596 8 Apostolepis longicauda - x - RT 0308 5 Boiruna sertaneja x - x RT1042 2 Erythrolamprus almadensis - x x RT 0176 2 Erythrolamprus poecilogyrus x - x CHUFPB 12311 14 Erythrolamprus taeniogaster* - - x CHUFPB 12317 8 Helicops angulatus* - - x CHUFPB 12286 41 Imantodes cenchoa - x - CHUFPB 12306 12 Lygophis dilepis x - x CHUFPB 12312 6 Oxyrhopus guibei x - - RT 0130 1 Oxyrhopus petolarius* x - x CHUFPB 12326 7 Oxyrhopus trigeminus x - x CHUFPB 04769 36

Ͷ Tropiduridae (1) Tropidurus hispidus x x x CHUFPB 07284 156 SNAKES (42) Boidae (2) Boa constrictor x - x CHUFPB 04930 5 Epicrates assisi x - x CHUFPB 13174 38 Colubridae (9) Herpetofauna in two habitat types in the Reserva Biológica Guaribas, Brazil Chironius exoletus x - - CHUFPB 12276 3 461 Chironius flavolineatus x - x CHUFPB 12278 9 Table 4. Continued.Drymarchon corais - x x RT 0005 3 Table 1. Drymoluber dichrous x x x CHUFPB 12282 9 Species Leptophis ahaetulla* - Occurrencex x Vo CHUFPBucher number 12308 Number of11 specimens Oxybelis aeneus Tabuleirosx SSF- Boundaries x CHUFPB 12323 6 FROGS Spilotes(34) pullatus x x x RT 0507 7 BufonidaeSpilotes (2) sulphureus x - x RT 0132 4 RhinellaTantilla melanocephalacrucifer* x- x x - CHUFPB 0459504362 482 DipsadidaeRhinella (26) jimi x x x CHUFPB 07889 5 4 CraugastoridaeApostolepis (1)cearensis x- x x- RT 0596 8 PristimantisApostolepis longicaudaramagii x- x - CHUFPBRT 0308 00472 3578 EleutherodactylidaeBoiruna sertaneja (1) x - x RT1042 2 AdelophryneErythrolamprus sp. *almadensis - x x - CHSA.ART 0176 274 212 HylidaeErythrolamprus (16) poecilogyrus x - x CHUFPB 12311 14 DendropsophusErythrolamprus branneritaeniogaster * x- - x CHUFPB 1231709027 1468 DendropsophusHelicops angulatus elegans* x- - x CHUFPB 1228610252 413 DendropsophusImantodes cenchoa minutus x- x- x - CHUFPB 1230602189 26612 DendropsophusLygophis dilepis nanus x - x CHUFPB 1231209048 256 DendropsophusOxyrhopus guibei oliveirai * x - x- CHUFPBRT 0130 00487 431 HypsiboasOxyrhopus albomarginatuspetolarius* x - x CHUFPB 1232607890 397 HypsiboasOxyrhopusPhilodryas fabertrigeminusnattereri x - x - CHUFPB CHUFPB 047690789607670 362412 HypsiboasPhilodryas ranicepsolfersii x - x x CHUFPB CHUFPB 1026212334 1322 PhyllomedusaPhilodryas patagoniensis nordestina x - x x CHUFPB CHUFPB 1121712251 3221 ScinaxPhimophis auratus guerini* x - - - CHUFPBRT 0114 09047 981 Ͷ ScinaxPseudoboa cretatus nigra* x - x- CHUFPB CHUFPB 0179912345 2713 ScinaxPsomophis eurydice joberti* * x- x- x- CHUFPB 0795712348 142 ScinaxSibon nebulatus fuscomarginatus * x x- x CHUFPB 1325112349 459 ScinaxSibynomorphus melanodactylus mikanii* x x- x- CHUFPBMNRJ 91050 12351 12116 ScinaxSibynomorphus nebulosus neuwiedi* x- - x x CHUFPBRT 0127 12940 732 ScinaxSiphlophis x-signatus compressus x - x x CHUFPBRT 0264 11536 304 LeptodactylidaeTaeniophallus (11) affinis x x - CHUFPB 12355 3 Taeniophallus occipitalis x - x RT 1015 12 Thamnodynastes pallidus x - - CHUFPB 12361 2 Xenodon merremii CHUFPB 12384 13 1 Elapidae (2) Micrurus ibiboboca x x x CHUFPB 13216 64 Micrurus potyguara* x - x CHUFPB 06947 17 Typhlopidae Amerotyphlops brongersmianus x x - CHUFPB 00731 50 Amerotyphlops paucisquamus x x - CHUFPB 00727 70 Viperidae (1) Bothrops leucurus x x x CHUFPB 12231 60 TURTLES Chelidae (1) Phrynops geoffroanus* - - x Visual Record* -

occurred in open areas and 15 in forested environments, the large sample size, the rarefaction curve for lizard with 10 species shared between environments (Table species was still rising at the end of the sampling 1). effort, probably due to the presence of two singletons 5 (Polychrus acutirostris, Enyalius catenatus). The curve The rarefaction curves of snakes and amphibians (Fig. for the combined herpetofaunal data slowly increased to 7) reached an asymptote, indicating that the probability the asymptote, nearly reaching the Chao 2P estimator of an increase in the number of species is low. Despite curve. The reason for this increase is the presence of the 462 Daniel O. Mesquita et al.

Figure 3. Examples of frogs from Reserva Biológica Guaribas. (A) Hypsiboas albomarginatus. (B) Hypsiboas faber. (C) Dendropsophus nanus. (D) Dendropsophus oliveirai. (E) Dendropsophus elegans. (F) Dendropsophus branneri. (G) Scinax fuscomarginatus. (H) Scinax eurydice. (I) Scinax nebulosus. (J) Scinax auratus. (K) Scinax melanodactylus. (L) Scinax x-signatus. (M) Adelophryne sp. (N) Leptodactylus fuscus. (O) Leptodactylus macrosternum. (P) Leptodactylus troglodytes. Photos by Daniel O. Mesquita (A–C, P) and Leandro O. Drummond (D–O).

two lizard singletons mentioned above, coupled with Discussion crocodilians and the chelonian, also singletons. Of the 72 reptile species documented herein, five lizards, six snakes, 14 frogs, seven amphisbaenas, and the turtle were new records for REBIO Guaribas, Herpetofauna in two habitat types in the Reserva Biológica Guaribas, Brazil 463

Figure 3. Continued.

based on the latest accessible herpetofauna species list Forest sites in southeastern Brazil and Bahia State, for the study site, the management plan of the reserve, the richness was smaller, varying from 29–47 species, and a previous snake inventory (MMA/IBAMA, 2003; but reaching impressive numbers, with more than 100 França et al., 2012). Considering the rarefaction curves, species (Lucas and Fortes, 2008; Serafim et al., 2008; the amphibian richness in the REBIO Guaribas reaches Condez et al., 2009; Almeida et al., 2011). However, values near the richness estimator, indicating that the the inventories in Atlantic Forest sites in northeastern sampled richness represents a proper approximation of Brazil, north of the São Francisco River, present a similar the real richness. When compared with other Atlantic richness to Guaribas, from 22–30 species (Borges- 464 Daniel O. Mesquita et al.

Figure 4. Additional frogs from Reserva Biológica Guaribas. (A) Leptodactylus vastus. (B) Lithobates palmipes. (C) Physalaemus albifrons. (D) Adenomera sp. (E) Dermatonotus muelleri. (F) Elachistocleis cesarii. (G) Rhinella crucifer. (H) Rhinella jimi. Photos by Daniel O. Mesquita (A, C, E), Daniel O. Laranjeiras (H), and Leandro O. Drummond (B, D, F, G).

Nojosa and Caramaschi, 2005; Borges-Nojosa and Camurugi et al., 2010; Morato et al., 2011). Considering Cascon, 2005; Loebmann and Haddad, 2010; Moura et open areas, like restingas, caatinga, and cerrado, the al., 2011). In sites south of the São Francisco River, the richness of the REBIO Guaribas is higher than that of results were contradictory, with sites having mixtures restingas, which vary from 2–30 species (Van Sluys of low and high richness, varying from 17–48 species et al., 2004; Bastazini et al., 2007; Rocha et al., 2008; (Árzabe et al., 1998; Oliveira and Lirio-Junior, 2000; Silva et al., 2008; Narvaes et al., 2009; Wachlevski and Herpetofauna in two habitat types in the Reserva Biológica Guaribas, Brazil 465

Figure 5. Examples of lizards from Reserva Biológica Guaribas. (A) Norops ortonii. (B) Dactyloa punctata. (C) Polychrus acutirostris. (D) Polychrus marmoratus. (E) Coleodactylus meridionalis. (F) Mabuya macroryncha. (G) Mabuya heathi. (H) Mabuya nigropunctata. (I) Dryadosaura nordestina. (J) Micrablepharus maximiliani. (K) Ameivulla ocellifera. (L) Kentropyx calcarata. (M) Salvator merianae. (N) Tropidurus hispidus. (O) Iguana iguana. Photos by Daniel O. Laranjeiras (A, B, F, H, O), Daniel O. Mesquita (C–E, I–M), and Leandro O. Drummond (G, N).

Rocha, 2010; Telles et al., 2012) or caatinga (15–21 et al., 2011; Gambale et al., 2014). species; Vieira et al., 2007; Garda et al., 2013; Pedrosa Considering the herpetofaunal species composition, et al., 2013; Protázio et al., 2015), and similar to cerrado the REBIO Guaribas shares approximately 17% of (21–39 species; Silveira, 2006; Oda et al., 2009; Maffei species with the Atlantic Forest areas south of the São 466 Daniel O. Mesquita et al.

Figure 5. Continued.

Francisco River and 58% with sites located north of the REBIO Guaribas and cerrado is 23%, higher than for São Francisco River (Árzabe et al., 1998; Oliveira and meridional Atlantic Forest sites (Silveira, 2006; Oda Lirio-Junior, 2000; Borges-Nojosa and Caramaschi, et al., 2009; Maffei et al., 2011; Gambale et al., 2014), 2005; Borges-Nojosa and Cascon, 2005; Camurugi suggesting a strong relationship with cerrado (Oliveira et al., 2010; Loebmann and Haddad, 2010; Morato Filho and Carvalho, 1993; Barbosa et al., 2011). et al., 2011; Moura et al., 2011), suggesting that the However, most species are widely distributed, such as river may be barrier for these animals (Prance, 1982). Dendropsophus minutus, D. nanus, Hypsiboas faber, H. The average proportion of shared species among the raniceps, Leptodactylus fuscus, L. troglodytes, Scinax Herpetofauna in two habitat types in the Reserva Biológica Guaribas, Brazil 467

Figure 6. Examples of snakes from Reserva Biológica Guaribas. (A) Amerotyphlops brongersmianus. (B) Drymoluber dichrous. (C) Chironius exoletus. (D) Chironius flavolineatus. (E) Apostolepis cearensis. (F) Helicops angulatus. (G) Imantodes cenchoa. (H) Oxyrhopus trigeminus. (I) Philodryas patagoniensis. (J) Psomophis joberti. (K) Sibon nebulatus. (L) Sibynomorphus mikanii. (M) Taeniophallus occipitalis. (N) Thamnodynastes pallidus. (O) Micrurus ibiboboca. (P) Bothrops leucurus. Photos by Daniel O. Laranjeiras (A), Leandro O. Drummond (C, D, F, G, N, P), Frederico G.R. França (B, E, F, H–J, L, M, O) and Daniel O. Mesquita (K).

fuscomarginatus, S. nebulosus, and S. x-signatus (Frost, et al., 2011), they are embedded in an Atlantic Forest 2017). Additionally, although the tabuleiros are part of matrix, which could be favourable for the establishment the cerrado (Oliveira Filho and Carvalho, 1993; Barbosa of typical open area anurans, such as the 15 new 468 Daniel O. Mesquita et al.

Figure 6. Continued.

records found in the REBIO Guaribas (Adelophryne sampling were conducted because the rarefaction curve sp., Dermatonotus muelleri, Elachistocleis cesarii, continued increasing and did not reach the asymptote, Leptodactylus macrosternum, Physalaemus albifrons, probably due to the presence of two singletons (Lopez Pleurodema diplolister, Pseudopaludicola mystacalis, et al., 2012), Polychrus acutirostris and Enyalius P. jaredi, Rhinella crucifer, Scinax auratus, S. cretatus, catenatus. Another possibility is the presence of other S. melanodactylus, S. eurydice, S. fuscomarginatus, and species that could promote an increase in richness, such S. nebulosus (MMA/IBAMA, 2003). as Strobilurus torquatus, which was found in areas close Considering lizards, our list could increase if additional to the Atlantic Forest, such as the Permanent Preservation Herpetofauna in two habitat types in the Reserva Biológica Guaribas, Brazil 469

stricto (13–25 species; Vitt, 1995; Garda et al., 2013; Pedrosa et al., 2013; Cavalcanti et al., 2014). Compared with forested habitats, the richness was similar to dry forest fragments within cerrado (18 species; Werneck et al., 2009), smaller than Amazon Forest sites (22–28 species; Vitt and Zani, 1996; Macedo et al., 2008), and bigger than gallery forest within cerrado (11 species; Brandão and Araujo, 2001), and other Atlantic Forest sites (10–17 species; Santana et al., 2008; Forlani et al., 2010; Lira Filho et al., 2011; Morato et al., 2011). Considering the herpetofauna species composition, the REBIO Guaribas shares approximately 30% of its species with other SSF sites from south of the São Francisco River and 70% with sites north of the São Francisco River, indicating the importance of the “Centro de Endemismo Pernambuco,” an area of Atlantic forest north of the São Francisco River with a high level of endemism relative to areas south of the river (Prance, 1982). In addition, the average proportion of shared species among REBIO Guaribas and cerrado is 43%, greater than meridional (south of the São Francisco River) Atlantic Forest sites (Feio and Caramaschi, 2002; Condez et al., 2009; Forlani et al., 2010). However, it is similar to septentrional (north of the São Francisco River) Atlantic Forest sites, reaching 70% similarity. Moreover, although the tabuleiros are related to the cerrado (Oliveira Filho and Carvalho, 1993; Barbosa et al., 2011), they harbour widely distributed species, including Ameiva ameiva, Cercosaura ocellata, Cnemidophorus ocellifer, Mabuya heathi, Micrablepharus maximiliani, and Polychrus Figure 7. Rarefaction curves for amphibians, lizards, acutirostris. Since tabuleiros are embedded within an snakes, and pooled herpetofauna coupled with a species Atlantic Forest matrix, they could be favourable for richness estimator (Chao2P). Black lines represent collected the establishment of typical lizards from open areas. individuals, and circles are the total species estimates based on We recorded five new species of lizards in REBIO Chao2P (Lopez et al., 2012). Guaribas, Dactyloa punctata, Enyalius catenatus, Mabuya nigropunctata, Norops ortonii, and Polychrus acutirostris (MMA/IBAMA, 2003). The rarefaction curves for snakes reach the asymptote Area Jardim Botânico Benjamim Maranhão and Reserva and overlap with the richness estimator Chao2P, de Patrimônio Particular Natural Gargaú (Rodrigues et indicating that the probability to add new species al., 2013), which were previously connected to REBIO to the area is low. Snakes are usually difficult to Guaribas before human activities in the region (Santana collect (Martins, 1998; Cechin and Martins, 2000); et al., 2008). Compared with other open areas, the lizard consequently, short-term studies tend to not generate richness (20 species) was higher than at restinga sites, sufficient information about their diversity (Dorcas which vary from 8–13 species (Freire, 1996; Teixeira, and Willson, 2011; Bernarde, 2012) and long-term 2001; Carvalho et al., 2007), cerrado (9–16 species; studies are preferred. Thus, in contrast to lizards and Vitt, 1991; Gainsbury and Colli, 2003; Vitt et al., amphibians, little information is available about snake 2005; Mesquita et al., 2006a), and Amazon savannahs assemblages, making further comparisons difficult. The (2–11 species; Vitt and Carvalho, 1995; Mesquita et richness of the snake fauna in REBIO Guaribas, with al., 2006b; 2007), but similar to that of caatinga sensu 43 species, is similar to other open areas, like cerrado, 470 Daniel O. Mesquita et al. which vary from 36–61 species (França et al., 2008; our numerous undergraduate students for their participation in the Sawaya et al., 2008; França and Braz, 2013), and it is fieldwork. higher than at caatinga sites (19–22 species; Vitt and Vangilder, 1983; Mesquita et al., 2013). Compared References with forested areas, the richness of snakes from REBIO Ab’Saber, A.N. (1977): Os domínios morfoclimáticos da América Guaribas was higher than other Atlantic Forest areas do Sul. Primeira aproximação. Geomorfologia 52: 1–21. (24–32 species; Marques and Sazima, 2004; Pontes et Ab’Sáber, A.N. (1982): The paleoclimate and paleoecology of al., 2008; Costa et al., 2010), and smaller than Amazon Brazilian Amazonia. In: Biological Diversification in the Forest sites (53–66 species; Martins, 1998; Bernarde Tropics, p. 41–59. Prance, G.T., Ed., New York, Columbia University Press. and Abe, 2006; Santos-Costa et al., 2015). The variation Almeida, A.P., Gasparini, J.L., Peloso, P.L.V. (2011): Frogs of the in the number of snake species is usually due to the state of Espírito Santo – the need for looking at the ‘coldspots’. differences in the size of the areas, sampling effort, and Check List 7 (4): 542–560. habitat structure (França et al., 2008). The richness of Árzabe, C., De Carvalho, C.X., Costa, M.A.G. (1998): snakes in REBIO Guaribas reflects the presence of both Anuran assemblages in Crasto forest fonds (Sergipe State, a high sampling effort and the presence of both open Brazil): comparative structure and calling activity patterns. and forested environments (Rodrigues et al., 2015). Herpetological Journal 8 (2): 111–113. Ávila-Pires, T.C.S. (1995): Lizards of Brazilian Amazonia (Reptilia: The present study reinforces the importance of the Squamata). Zoologische Verhandelingen 299: 3–706. REBIO Guaribas for the conservation of tabuleiros; Barbosa, M.R.V., Thomas, W.M., Zárate, E.L.P., Lima, R.B., Agra, most species from the area are typical from open areas, M.F., Lima, I.B., Pessoa, M.C.R., Lourenço, A.R.L., Delgado, with some being exclusive to these isolated open areas. G.C.J., Pontes, R.A.S., Chagas, E.C.O., Viana, J.L., Gadelha, One theory that explains the formation of these isolated P.C.N., Araújo, C.M.L.R., Araújo, A.A.M., Freita, G.B., Lima, areas is the Pleistocene refuge hypothesis, which states J.R., Silva, F.O., Vieira, L.A.F., Pereira, L.A., Costa, R.M.T., that during glacial periods, with reduced precipitation, Duré, R.C., V. de Sá, M.G. (2011): Checklist of the vascular plants of the Guaribas Biological Reserve, Paraíba, Brazil. large areas of the Neotropics were covered by savannahs, Revista Nordestina de Biologia 20 (2): 79–106. restricting forests to isolated patches (Eden, 1974; Bastazini, C.V., Munduruca, J.F.V., Rocha, P.L.B., Napoli, M.F. Ab’Sáber, 1982; Bigarella and Andrade-Lima, 1982; (2007): Which environmental variables better explain changes Huber, 1982). Thus, isolated savannah patches nowadays in anuran community composition? A case study in the Restinga are the vestiges of a extensive savannah that extended of Mata de São João, Bahia, Brazil. Herpetologica 63 (4): 459– from central Brazil to the Guianas, crossing northeastern 471. Brazil (Prance, 1978). Currently, these patches occur Bernarde, P.S. (2012): Anfíbios e Répteis: Introdução ao Estudo da Herpetofauna Brasileira. Curitiba, Puerto Rico, USA, Anolis as dispersed islands embedded in the Amazon Forest, Books. and isolated patches in northeastern Brazil, covering Bernarde, P.S., Abe, A.S. (2006): A snake community at Espigão 2 approximately 150,000 km , 2% of Brazilian territory do Oeste, Rondônia, southwestern Amazon, Brazil. South (Pires, 1973). Their isolation promotes speciation and American Journal of Herpetology 1 (2): 102–113. produces endemic fauna, typically in open areas. In Bigarella, J.J., Andrade-Lima, D. (1982): Paleoenvironmental addition, some species were identified only at the genus changes in Brazil. In: Biological Diversification in the Tropics, level and may represent undescribed species. p. 27–40. Prance, G.T., Ed., New York, Columbia University Press. We conducted a long-term inventory of REBIO Bokermann, W.C.A. (1966): Notas sobre três espécies de Guaribas, reinforcing the importance of the tabuleiros Physalaemus de Maracás, Bahia (Amphibia, Leptodactylidae). in species composition and maintenance of regional Revista Brasileira de Biologia 26 (3): 253–259. fauna. According to the rarefaction curves, amphibian Borges-Nojosa, D.M., Caramaschi, U. (2005): Composição e análise and snake samples are very broad, and the probability of comparativa da diversidade e das afinidades biogeográficas dos discovering unreported species is small. However, due lagartos e anfisbenídeos (Squamata) dos brejos nordestinos. In: the presence of two singletons, other lizard species may Ecologia e Conservação da Caatinga, p. 463–512. Leal, I.R., Tabarelli, M., Silva, J.M.C., Eds., Recife, Pernambuco, Brazil, be added when more animals are captured. Universidade Federal de Pernambuco�. Borges-Nojosa, D.M., Cascon, P. (2005): Herpetofauna da área Acknowledgements. We thank the Conselho Nacional de Reserva da Serra das Almas, Ceará. In: Análise das Variações Desenvolvimento Científico e Tecnológico and the Fundação de da Biodiversidade do Bioma Caatinga: Suporte a Estratégias Apoio à Pesquisa da Paraíba for financial support, and the Instituto Regionais de Conservação, p. 243–273. 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Accepted by Hinrich Kaiser