Herpetofauna of protected areas in the Caatinga V : Seridó Ecological Station ( Rio Grande do Norte , Brazil )

We provide a list of lizards, snakes, chelonians, and amphibians collected during a 30-day expedition to the Seridó Ecological Station (ESEC Seridó), Rio Grande do Norte state, Brazil. We sampled species using thirty-seven pitfall trap stations composed of four buckets each, along with glue traps and active searches. We recorded 13 species of lizards, eight snakes, 19 amphibians, and one chelonian. Rarefaction curves suggest local biodiversity is still underestimated. Sampling during rainy season was crucial to stabilize rarefaction curve for amphibians. Comparisons of our results with data from literature show we did not capture some arboreal and semifossorial lizards known for the area. Seridó Ecological Station fauna is characterized mainly by generalist species common to lowland Caatinga sites. Still, several Caatinga endemics species are found, which underscore the importance of this small but representative protected area.


INTRODUCTION
The Caatinga is an exclusively Brazilian biome (Tabarelli and Silva 2005) located at northeastern portion of the country and occupying about 800,000 km².It is limited to east and northwest by Atlantic and Amazon forests, respectively, and to southwest and south by the Cerrado savannas (Andrade et al. 2005;Leal et al. 2005a;Prado 2005).Caatinga is located in a semiarid region characterized by low and irregular rainfall, high temperatures and high light intensity that causes high evaporation rates and soil desiccation, culminating in a water deficit throughout most of the year (Prado 2005;Trovão et al. 2007).The vegetation is deciduous, represented by semiarid xerophytic formations consisting in many cases of trees, low shrubs, cacti and bromeliads (Trovão et al. 2004;Prado 2005;Queiroz et al. 2006).However, other vegetation types are also present and high floristic richness can be found, with some areas having medium-sized to large trees with high canopies, a feature that characterizes Caatinga also as seasonally dry tropical forest (STDF; sensu Pennington et al. 2009;Werneck 2011).
For a long time Caatinga has been considered poorly studied and under poorly protected (less than 2% of its area) (Leal et al. 2005a).This scarce knowledge and low levels of protection come from the long-held historical view that arid regions have low productivity and diversity (Albuquerque and Andrade 2002).This view has been reversed in recent years with the increase in inventories and long-term research (Albuquerque et al. 2012;Barbosa et al. 2013) and in the number of protected areas, now about 7.5% of Caatinga territory (MMA 2016).However, the biome continued to suffer same old problems, such as intense deforestation and expansion of irrigated crops, factors which have gradually promoted soil salinization, increasing water evaporation (Drumond et al. 2000).Replacement of natural areas with agriculture and wild fires have acted together with livestock to speed up desertification (Casteleti et al. 2003).Goats have been released into natural areas and consume large amounts of plants, which may cause long-term changes in the landscape (Leal et al. 2005b).
The suggestion that the Caatinga herpetofauna had low endemism and hence did not harbour its own fauna was common sense up to the early 1980s (Vanzolini et al. 1980).This scenario has changed with newly described  Caldas et al. | Herpetofauna of Seridó Ecological Station 1996;Delfim and Freire 2007;Freire et al. 2009;Magalhães et al. 2013).Over 90% of the area of Rio Grande do Norte state is covered by the Caatinga biome.

Study site
Seridó Ecological Station (ESEC Seridó; Figure 1) is located in Serra Negra do Norte municipality in the southwestern region of Rio Grande do Norte state (06°35ʹ to 06°40ʹ S, 037°20ʹ to 037°39ʹ W) and encompasses an area of ca.1,166 ha (ICMBIO 2016).Its location is at "Depressão Sertaneja Setentrional", one of the eight ecoregions recognized for Caatinga biome (Velloso et al. 2002), whose average annual rainfall is around 500-800 mm.Open Caatinga vegetation characterizes it, with shallow soils distributed in a wide plain interspersed by residual higher elevation areas over landscape (Velloso et al. 2002).
Vegetation is composed mostly by herbs and shrubs, with predominant genera as Amburana Schwacke & Taub.(Fabaceae), Ximenia Plum.ex L. (Olacaceae), Luet zelburgia Harms (Fabaceae), Mimosa L. (Fabaceae) among others, and a endemic species, Gossypium mustelinum Miers ex G.Watt (Malvaceae) (Velloso et al. 2002).The region known as "Seridó" located in Rio Grande do Norte suffer remarkable human disturbances, which combined with the delicate nature of local environment species and moderate to high levels of endemism being reported for some groups (Rodrigues 1991a(Rodrigues , 1991b(Rodrigues , 2000;;Heyer and Juncá 2003;Magalhães et al. 2014).In fact, diversity of reptiles and amphibians in Caatinga is remarkable given its severe environmental conditions (Navas et al. 2002;Rodrigues 2005).Knowledge for the area is still growing as new areas are being inventoried (Ribeiro et al. 2012;Garda et al. 2013;Cavalcanti et al. 2014;Pedrosa et al. 2014;Magalhães et al. 2015;Pereira et al. 2015).However, it is still undersampled, with just a few areas currently sampled in entire states in the Northeastern region.Information on diversity and endemism can only be obtained with implementation and publication of field surveys, which are the key for development of more efficient conservation strategies (Silveira et al. 2010).
We present a list of amphibians and reptiles collected during a 30-day field expedition to Seridó Ecological Station (ESEC Seridó) located in Serra Negra municipality, Rio Grande do Norte state, Brazil.Our methodology is similar to other four inventories recently published for the biome (Garda et al. 2013;Cavalcanti et al. 2014;Pedrosa et al. 2014;Magalhães et al. 2015).Rio Grande do Norte state has a total area of 52,797 km 2 (roughly the size of West Virginia,United States, or the Netherlands).Still, only a single amphibian inventory and some lists for squamates have been published for the state (Freire  Denser vegetation, presence of herbaceous and shrubby with leaf litter, without rock formations (presence of glue traps).

Caldas et al. | Herpetofauna of Seridó Ecological Station
drift fences) distributed in five different habitats.In each habitat, stations were at least 20m apart; 3. Glue traps, four squares of 20 cm 2 , two on ground and two on branches or tree trunks, distributed in each pitfall trap station (Figures 6 and 7).
The four pitfall trap arrays were set in different habitats of ESEC (Figures 2-7): 2. Denser vegetation with herbaceous plants and shrubs with leaf litter and rock outcrops; 3. Open vegetation with herbaceous plants and shrubs without leaf litter; 4. A temporary stream bank with arboreal formation and soil covered by leaf litter; 5. "Massapê" soil, consisting of a compact clay soil with low permeability (as described in Andrade 2005; Oliveira Andrade 2007); 6-7.Denser vegetation with herbaceous plants and shrubs with leaf litter but lacking rock outcrops.

Data analysis
To evaluate the quality of sampling effort we constructed rarefaction curves for lizards, amphibians and all herpetofauna combined, based on individuals (Gotelli and Colwell 2001), using Chao2P species estimator (Lopez et al. 2012), in EstimateS 8.2.0 (Collwell 2005) and R (R Development Core Team 2009).The curves were obtained through 1,000 resampling of original data, with no reposition.

DISCUSSION
All lizards and seven snakes had already been collected in a previous study that recorded 16 lizards, 14 snakes, and two amphisbaenids from Seridó Ecological Station (Freire et al. 2009).In addition, the snake Epictia borapeliotes (Vanzolini, 1996), also collected in this inventory, was recorded in a later study (Guedes et al. 2014).Although those previous studies presented all our recorded species of lizards, snakes and amphisbaenids, those authors did not use richness estimators coupled with rarefaction curves to confirm inventory efficiency.We also collected one chelonian and 19 frogs not previously recorded from the study area.
Lizard species richness at ESEC Seridó (16 species) is regionally significant when compared to other Caatinga areas: Exu/Pernambuco (14 species; Vitt 1995), Floresta Nacional de Negreiros (14 species; Pereira et al. 2015), PARNA Serra da Capivara (17 species; Cavalcanti et al. 2014), PARNA do Catimbau (15 species; Pedrosa et al. 2014) and PARNA da Chapada Diamantina (25 species; Magalhães et al. 2015).The lizard families Gekkonidae, Phyllodactylidae, Teiidae and Tropiduridae have similar species compositions in other Caatinga areas (Vitt 1995;Garda et al. 2013;Pedrosa et al. 2014), which is expected because many of their representatives are common in open areas and can use a variety of microhabitats found in various xerophytic formations (Vitt 1995).In contrast, Gymnophthalmidae, which is frequently found on leaf litter, has a low richness even at Exu/Pernambuco, where only V. multiscutata is found (Vitt 1995).A greater richness of gymnophthalmids can be observed for "sand dunes in the middle São Francisco River" and this particularity is related to speciation factors exclusive of this region (Rodrigues 1996;Rodrigues 2005).Rodrigues (2005) and Freitas and Silva (2007) and are as follows: Habitat = A -arboreal, AQ -aquatic, L -leaf litter, F -fossorial, S -saxicolous, T -terrestrial.Distribution = WO -wide occurrence in the biome, R -relictual distribution, DS -dependent drainage system, ?-unknown or preliminary data.Low number of snake species results from sampling difficulties related to the group and the reduced sampling period (30 days) for snakes.Low abundances, cryptic habits and microhabitat specificity demand more efficient and specific capture methods as well as greater sampling efforts (Dorcas and Willson 2011;Bernarde 2012).Indeed, if we compare the present study species richness (eight species) to one described by Freire et al. (2009) (14 species) which was conducted over a much larger timeframe (2002)(2003)(2004), our list still presents half of the species previously recorded, even though our sampling effort was much less.
Frog species richness at ESEC Seridó is average for the Caatinga domain.Previous studies have recorded from 12 to 26 species of frogs (Arzabe 1999;Vieira et al. 2007;Campos and Santos 2011;Silva and Santos 2011;Pedrosa et al. 2014).We collected frogs typically found in open areas, with a dominance of Leptodactylidae and Hylidae species; these are the most representative families in several Brazilian biomes (Bertoluci 1998;Bernarde 2007;Vieira et al. 2007).Although hylids are usually more abundant than leptodactylids, they had fewer species in ESEC Seridó.Such a trend is not common in Brazil, but it has been commonly reported for open environments (Cardoso et al. 1989;Arzabe 1999;Vieira et al. 2007).Herbaceous and shrub formations predominate in our study site, which in general presents a lower vertical stratification, possibly accounting for a lower richness of hylid species (Rossa-Feres and Jim 2001).Alternatively, the water deficit in the Caatinga could favor burrowing species, which are very common among leptodactylids.Accordingly, some recently studied Caatinga areas showing higher rates of hylids compared to leptodactylids (e.g., ESEC Raso da Catarina and PARNA Catimbau) presented mesic habitats with marked influences of Atlantic rainforest sites (Garda et al. 2013;Pedrosa et al. 2014).
Despite the important contributions of this inventory, additional sampling seems necessary at ESEC Seridó to provide a complete list of local diversity herpetofauna diversity.Our inventory, for example, failed to find lizard species identified in other inventories (Hemi dactylus brasilianus [Amaral, 1935], Polychrus acutirostris Spix, 1825, and Micrablepharus maximiliani [Reinhardt & Lütken, 1862]; Freire et al. 2009).This is somewhat puzzling, given that our methods have efficiently captured those species in other Caatinga sites studied (Garda et al. 2013;Cavalcanti et al. 2014;Pedrosa et al. 2014;Magalhães et al. 2015).ESEC Seridó is within one of the major centres of desertification in Brazil (Sampaio  ), and is one of the smallest strict protection areas in the country.Farms surround it, and hunters and livestock are frequently found inside the area.Because the local richness of the herpetofauna is not yet completely known for the "Seridó region", and because no data are available on species abundances over time, population trends, and hence, conservation of local biodiversity are hard to evaluate.The region's small size makes it easy to monitor and, as such, an ideal place to evaluate the impacts of human activity.There is a need for prolonged inventory and monitoring using reproducible methods to help with comparisons with other biomes and to show population trends over time.

Figure 1 .
Figure 1.Map of South America showing Brazil (thick line) and Rio Grande do Norte State (grey inset).Right side shows Seridó Ecological Station (ESEC Seridó), its map and the ten sampled points.Points 1-5 refer to pitfall trap arrays.Point 10 refers to dam and remaining areas surveyed through active searches.

Figure 46 .
Figure 46.Species accumulation curves (circles) and rarefaction curves (lines) for lizards, amphibians and all herpetofauna based on number of individual specimens recorded at Seridó Ecological Station (ESEC-Seridó).

Table 1 .
Caldas et al. | Herpetofauna of Seridó Ecological Station List of squamates, chelonians and anuran amphibians known for Seridó Ecological Station (ESEC Seridó), Rio Grande do Norte, Brazil.Abbreviations of habitat and distribution categories were adapted from Caldas et al. | Herpetofauna of Seridó Ecological Station