Squamate Reptiles from Parque Nacional das Emas and surroundings , Cerrado of Central Brazil

We present a list of squamate reptiles from Parque Nacional da Emas (PNE), ten neighbor private properties and Parque Estadual Nascentes do Rio Taquari, states of Goiás, Mato Grosso, and Mato Grosso do Sul. The study area encompasses the headwaters of Araguaia and Taquari river basins and part of Paranaíba River Basin, resulting in significant habitat heterogeneity. Inside PNE, we recorded 74 squamate species: 47 snakes, 21 lizards and six amphisbaenians. If we consider also the neighboring areas, richness value raises to 87 species: 54 snakes, 27 lizards and six amphisbaenians. From these, 52 % of the lizards, 19 % of the snakes and 33 % of the amphisbaenians are Cerrado endemics. Forest-specialist species are more common outside than inside PNE. Additional species are expected to occur in the PNE region, in view of their known geographical ranges. Introduction The first comprehensive published research on Cerrado herpetofauna recorded 47 lizards, 107 snakes and 15 amphisbaenians for the biome (Colli et al. 2002). Recently, more detailed studies based on systematized data revealed that at least 237 Squamate species are found in the region, including at least 68 lizards, 145 snakes and 24 amphisbaenians (Costa et al. 2007). Nevertheless, despite the high potential local richness values (Costa et al. 2007), Cerrado herpetofauna is still considered poorly sampled because studies are mostly located in few restricted areas. In a local scale, lizard assemblages are better characterized in literature than snakes or amphisbaenians, and richness varies greatly among areas, ranging from 15 species in Parque Nacional da Bodoquena region (20o32' S, 56o42' W), state of Mato Grosso do Sul (Uetanabaro et al. 2007), to 26 lizard species, in Jalapão region (10o38' S, 46o48' W), state of Tocantins (Vitt et al. Check List 5(3): 405–417, 2009. ISSN: 1809-127X


Introduction
The first comprehensive published research on Cerrado herpetofauna recorded 47 lizards, 107 snakes and 15 amphisbaenians for the biome (Colli et al. 2002).Recently, more detailed studies based on systematized data revealed that at least 237 Squamate species are found in the region, including at least 68 lizards, 145 snakes and 24 amphisbaenians (Costa et al. 2007).
Nevertheless, despite the high potential local richness values (Costa et al. 2007), Cerrado herpetofauna is still considered poorly sampled because studies are mostly located in few restricted areas.
Apart from biogeographical importance and lack of scientific knowledge, zoological studies on the Cerrado are highly relevant, as this region has been recognized as the one of the 25 global biodiversity hotspots, representing a priority target area for conservation actions (Myers et al. 2000).Over the past 35 years, more than half of the Cerrado's original area has been transformed for agriculture, while only 2.2 % of it is area are under strict legal protection (Klink and Machado, 2005).The surroundings of the Parque Nacional das Emas (PNE) have suffered a severe loss of habitat due to the development of the agriculture in the last decades, and this region has been considered a priority area for conservation of Cerrado biodiversity, based on species richness and the occurrence of endemic, rare, and threatened species (MMA 2007).
Here we provide a checklist of the snake, lizard and amphisbaenian species found during a long term study on squamate reptiles in the PNE region, including Nascentes do Parque Estadual do Rio Taquari and ten neighbor private properties.We also provide comparisons among sampling sites, comments on Cerrado endemic species, and conservation issues.

Material and Methods
Parque Nacional das Emas (18°20' S, 53°00' W, 760-880 m a.s.l.; Figures 1, 2 and 3) is a large (ca.130,000 ha) preserved area of Cerrado, localized on a plateau dominated by interfluvial grassy scrubland (campo sujo) and cerrado grassland (campo limpo), although arboreal savannas are also present in smaller proportions (see detailed descriptions of Cerrado physiognomies in Ribeiro and Walter 1998).This plateau, classified as Savanna Parque (Figure 2 b) according to IBGE (2003) vegetation physiognomies, degrades to lower areas (600-700 m; Figure 1b) on the eastern border as well as outside the park, to the north (Araguaia River Basin), east (Jacuba-Correntes system, Paraná River Basin) and west (Taquari River Basin, Pantanal complex; Figure 2  Riparian habitats, such as wet grasslands (campo úmido) and gallery forests (mata de galeria) are present along water courses both inside and outside the park, as well as isolated patches of mesophytic forests.
The PNE encompasses areas belonging to the Paranaíba (Formoso, Jacuba and Correntes rivers) River Basin (Figure 2 b).We also sampled habitats not widespread inside PNE, such as typical cerrado, cerradão (woodlands) and wider gallery forests, mostly located in Taquari and Araguaia River Basins, not farther than 50 km from PNE (Figure 2).Sites outside PNE located in Araguaia River Basin are Assentamento Nascentes do Araguaia, Babilônia Farm and Jaboticaba Farm, in Mineiros, state of Goiás; Granada Farm, in Alto Taquari, and Sapo River region, in Alto Araguaia, both in the state of Mato Grosso.Sites located at Taquari River Basin are: Mutum Farm, Vista Bonita Farm and Planalto Farm in      (Fitch 1987) inside PNE, and not quantified outside, 20,388 pitfall traps-day (Corn 1994) inside PNE and 10,196 outside, and opportunistic encounters (all the snakes found in situations other than searching or sampling activities, including specimens collected by other researchers during their fieldwork, as in Jácomo and Silveira 1988).Lizards and amphisbaenians were found mostly through pitfall traps and opportunistic encounters.All collected specimens were deposited in the herpetological collections of Instituto Butantan (IB), Museu de Zoologia da Universidade de São Paulo (MZUSP), and Coleção Herpetológica da Universidade de Brasília (CHUNB).We also include specimens already available in these collections, as well as those deposited in Museu de Zoologia da Universidade Estadual de Campinas (ZUEC) or the herpetological collection of Universidade Católica de Goiás (CEPB), from former and unpublished studies.Taxonomic arrangements is based on SBH (2009), Zaher et al. 2009 andCurcio et al. (2009).

Results and Discussion
We found 74 squamate reptile species inside PNE (Table 1, Figure 4 and 5, Appendix 1): 47 snakes, 21 lizards and six amphisbaenians.Other seven snake and six lizard species were found in areas sampled outside PNE, resulting in a regional richness of 87 squamate species.These 13 species were only found in PNE neighboring areas, located in Paranaíba, Taquari and Araguaia river basins, probably as an effect of differences in habitat structure inside and outside the park.
The number of species found in PNE represents 31 % of lizards, 25 % of amphisbaenians and 33 % of snakes known to occur in Cerrado, according to the list presented by Costa et al. (2007).If we include data obtained in PNE neighboring areas, values are raised to 40 % of lizards and 38 % of snakes.Eleven lizards (52 % of the total number of species in this group, at PNE), two amphisbaenians (33 %) and nine snakes (19 %) found inside PNE are Cerrado endemics.Therefore, we found higher proportions of Cerrado endemics than described in literature: according to Colli et al. (2002) 25 % of lizards, 10 % of snakes and 50 % of amphisbaenians occurring at Cerrado are endemic species.These differences may be explained by two main factors: knowledge on squamate reptiles' taxonomy and distribution has improved during the past six years, and we included previously undescribed, restricted range species, not included in Colli et al. (2002) results.
Many additional species are still expected to occur in the PNE and surroundings, in view of their geographical ranges.Recently Vaz-Silva et listed 45 snakes, 18 lizards and five amphisbaenians for the Espora Hidroeletrical Power Plant, in Aporé region, close to PNE.Among these, two amphisbaenians and seven snakes, five of them forest specialists or aquatic species, were registered for Aporé, but not for PNE region.Due to the short distance between sites and the general similarity between the two assemblages the nine above mentioned species are also expected to occur in PNE surroundings.

Conservation Implications:
least 79 out of 88 sampled squamate species.The PNE protects a rich reptilian fauna, highly representative of the herpetofauna of the Upper Paraná River Basin, in the southern portion of the Cerrado, one of the most disturbed regions in the domain (Machado et al. 2004;Redford 1985).Also, because of its more than 130,000 ha, PNE can protect significant populations of Cerrado Squamates, including some grassland-specialist species, which have lost most of their habitats outside the park, such as the lizards Kentropyx paulensis, Anolis meridionalis, Tupinambis duseni and the snakes Philodryas livida, and Rhachidelus brazili.However, 18.6 % of the lizard species found in PNE surroundings may be regionally unprotected: three of them (C.brachystoma, M. bistriata and S. sinesaccus) are mostly forests inhabitants, although M. bistriata can also be found in open areas in other localities at Mato Grosso state (C. Strussmann, pers. com.).Two other species (M.maximiliani and V. rubricauda) are regionally restricted to sandy soil savannas, and are both among the most common species at Vista Bonita and Saramandaia farms, Taquari basin.Although M. atticolus and C. aff.ocellifer are also sandy soil areas inhabitants, this habitat is extremely restricted inside PNE, and are much more common at both Araguaia and Taquari basins.We expect to find other species (mainly snakes and/or forest-specialist species) outside PNE, and it is possible that a greater proportion of the regional fauna will be found after new studies in Cerrado remnants outside the protected sites, as we spent the great majority of our collecting efforts inside PNE.
Natural landscapes around PNE are highly threatened by the expansion of mechanized agriculture, and many species may be lost if not protected by public or private reserves.We suggest that new conservation units must be planned for the region, aiming to protect lowland habitats at Araguaia and Taquari river basins and act as a complement on regional conservation efforts.
Our results indicate that snake assemblages in Cerrado show higher richness levels than previously suspected, corroborating recent conclusions regarding Squamate diversity in Central Brazil (Costa et al. 2007;Recoder and Nogueira 2007;Vaz-Silva et al. 2007).We suggest that long-term studies are necessary to properly evaluate species richness and composition of Cerrado squamate fauna, especially with regard to snakes and amphisbaenians.
a), in areas dominated by typical cerrado (cerrado sensu stricto), belonging to other five different vegetation physiognomies of Savanna vegetation class (IBGE 2003; Figure 2 b).

Figure 1 .
Figure 1.Map showing location of Parque Nacional da Emas (PNE) and Parque Estadual Nascentes do Rio Taquari (PENRT) in Brazil.Cerrado domain is represented in light green.

Figure 3 .
Figure 3.Some of the sample sites at Parque Nacional da Emas (PNE) and Parque Estadual Nascentes do Rio Taquari (PENRT), and in other locations in Araguaia and Taquari river basins.A. Overview of different Cerrado formations at PNE; B. Grassland, PNE; C. Aerial view, PNE; D. Marsh and typical cerrado at Sapo river region; E. Garrote Farm, PENRT; F. Gallery forest at Garrote Farm, PENRT; G. Marsh and typical cerrado at Vista Bonita Farm, Taquari River Basin; H. Dense cerrado at Saramandaia Farm, Taquari River Basin.Photos A-C, E-H: P. H. Valdujo; D: Carlos E. R. Cândido.

Table 1 .
-Lizards, amphisbaenians, and snakes registered at Parque Nacional das Emas (PNE) and surroundings areas in Taquari (TA) and Araguaia (AR) river basins.Endemic species are marked with " e ".Site names and their geographic coordinates are listed in Appendix 2.