The herpetofauna of Parque Nacional da Serra das Confusões , state of Piauí , Brazil , with a regional species list from an ecotonal area of Cerrado and Caatinga

Different physiognomies at Parque Nacional da Serra das Confusões (PNSCo) were intensively sampled aiming to access the distribution pattern of its herpetofauna. Sixty six species were found in the park (47 reptiles and 19 amphibians); the rarefaction curve for lizards, although not fully stabilized in an asymptote, indicates that the sampling effort was enough to reveal most lizard species occurring in the area; and richness estimators recovered values close to observed. For amphibians, the curve shows a weak tendency to stabilization with richness estimators indicating that additional records could be done. Field work carried out at PNSCo has highlighted an unique herpetofauna: five new species were described and there are three candidates as new species. The regional list including Cerrados’s units Estação Ecológica Serra Geral do Tocantins (EESGT) and Estação Ecológica de Uruçuí-Una (EEUU) with Caatinga’s ones PNSCo and Parque Nacional da Serra da Capivara (PNSCa), shows a high herpetofaunal diversity (191 species) to the region. The cluster analysis recovered the Cerrados’s units and Caatinga’s ones, in separate clusters evidencing a species turnover between domains, despite its geographical proximity. Thus, although there is widespread fauna throughout region shared by the units, each reserve holds its own faunal identity, harboring a singular assemblage of species.

Both Cerrado and Caatinga biomes lost extensive areas of original vegetation, mostly due to fast expansion of agricultural enterprises (Myers et al. 2000, Cavalcanti & Joly 2002, Klink & Machado 2005, Silva et al. 2006).With this continuous process of habitat loss, it seems imperative to prioritize faunal inventories within both biomes in order to fill the geographical gaps in our knowledge, allowing more accurate decisions when defining areas for conservation (Brooks et al. 1992;Greene 1994;Silva & Bates 2002).According to Castro (2000), the state of Piauí harbors an important center of biodiversity, mainly for its highly diversified vegetation that accounts for a large ecotonal zone that includes Cerrado, Dry Forest, Caatinga and pre-Amazon elements.
Here, we present a taxonomic list of the local herpetofauna present at the Parque Nacional da Serra das Confusões (PNSCo), located in southwestern Piauí, one of the least studied areas of the Cerrado-Caatinga ecotone.We also provide a regional list of the herpetofauna that includes three intensively sampled conservation units that are geographically closer to PNSCo, as follows: Parque Nacional da Serra da Capivara (PNSCa), Estação Ecológica de Uruçuí-Una (EEUU) and Estação Ecológica Serra Geral do Tocantins (EESGT).Finally, we compare the herpetofaunal composition of PNSCo with other local lists from the Caatinga and neighboring biomes.

Study area
The Parque Nacional da Serra das Confusões (PNSCo) (approximate coordinates: 08°32' -09°16'S, 43°15' -43°51'W, Figures 1, 2) was created in October 1998, and preserves an area of approximately 500.000ha in southwestern Piauí, close to the border of the state of Bahia.The park is placed in an ecotonal area of Tropical Dry Forest and Caatinga (Olson et al. 2001), with a predominance of deciduous forest and arboreal Caatinga.Climate is considered to be tropical semiarid.The park is situated within the Parnaíba drainage, in a sandstone plateau with altitudes ranging from about 450 to 700 m above the sea level [a.s.l.]) (Rodrigues et al. 2001;Bour & Zaher 2005).The plateau is locally known as "Chapada da Serra Grande," contains most of the area belonging to the park, and is dissected on its southwestern portion by the intermittent Santana River drainage (Rodrigues et al., 2001;Bour and Zaher, 2005).The top of the plateau, averages 550 m a.s.l., being covered by a tall arboreal caatinga that grows on sandy soil and produces an abundant leaf litter.The plateau is dissected by the intermitent Itaueira River in its central portion and by the "Lagoa do Jacu" depression created by erosive processes in its northern portion.The southern and western borders of the park are deeply dissected, with scattered rocky outcrops over sandy soil originated from the erosion of the Chapada da Serra Grande plateau.Lowland areas are characterized by dense rocky outcrops with low arboreal Caatinga growing over a sandy soil.This vegetation is widespread on the open lowlands.Several canyons, dissected by intermittent rivers with an evergreen forest and a dense leaf litter, are also present, but account for only a minor portion of the area.

Sampling method
Sampling was carried out in two campaigns in the years 2000 and 2002, one at the end of the dry season (September 26 th to October 10 th 2000) and other during the rainy season (January 10 th to 26 th 2002).The main physiognomic subunits present in the region were sampled using pitfall traps with drift fences, complemented by active visual searches.Twelve lines of pitfall traps were installed, each composed of 10 sampling units that consisted of four 30 liters buckets arranged in Y-shape, with a central one connecting to three peripherals by 4 m long plastic fences.Habitat types, geographic coordinates, campaigns and the total sampling effort are summarized in Table 1   It remains constantly in the shade, and accumulates large layers of leaf litter over sandy soil.6. High arboreal Caatinga (Lowland) -Lines 11 and 12. High arboreal elements, with canopy at 10 m above sandy soil rich in organic matter and closed understory.This type of vegetation predominates in the valleys.A representative sample of specimens was collected and housed at the herpetological collection of the Museu de Zoologia, Universidade de São Paulo, São Paulo, Brazil (MZUSP).Voucher specimens were fixed in 10% formalin and preserved in 70% alcohol.The remaining individuals were marked by toe clipping and released near the capture site.

Data Analysis
The effectiveness of the sampling effort was estimated based on rarefaction curves, through 10.000 randomizations without replacement, of a matrix containing the number of individuals per species at each sampling day, including data from both pitfall traps and active search, for lizards and anurans.This analysis was performed using EstimateS v.8.0.0 (Colwell 2006).We also estimated species richness with the Chao2 and Jacknife1 estimators.Snakes were excluded from this analysis because capture rates were low, and the resulting list for the group may be underestimated, which could compromise the behavior of the rarefaction curves.
EESGT and EEUU are mostly within the Cerrado (with EEUU having some Caatinga's elements) while PNSCo and PNSCa are mostly within a Caatinga physiognomy (with PNSCo including Cerrado elements).

Results
Sixty six species of reptiles and amphibians were found at PNSCo: 47 reptiles (21 lizards, 20 Snakes, 2 turtles and 4 amphisbaenids) and 19 amphibians (18 anurans and one caecilian) (Table 2, Figures 3, 4, 5).For lizards, the rarefaction curve showed a tendency to asymptote, with decreasing standard deviation after 34 sampling days (two campaigns together) (Figure 6A), same pattern found in each campaign separately (Figure 6B).The richness estimators Chao2 and Jacknife1 recovered 19 and 20 species, respectively.For amphibians, the rarefaction curve for the two campaigns together showed only a weak tendency towards stabilization (Figure 7A), differently from the results attained for each campaign separately (Figure 7B).The richness estimators Chao2 and Jacknife1 recovered 17 and 18 species, respectively.
Sixteen species occured in all four units while 17 species were shared among three of them, 32 species were shared only between EEUU and EESGT, 8 species between PNSCo and PNSCa, 5 species between PNSCo and EEUU, and 4 between PNSCo and EESGT.Only one species was shared between PNSCa and EEUU and none were exclusive of PNSCa and EESGT together.Seven species occurred exclusively in PNSCa, 17 in PNSCo, 20 in EEUU, and 64 in EESGT (Table 3).The cluster analysis recovered PNSCo and PNSCa within the Caatinga group, and EEUU and EESGT within the Cerrado group, indicating a strong species turnover in the contact region between Caatinga and Cerrado in southern Piauí (Figure 8).The same pattern was recovered for lizards and amphibians when analyzed separately (Data not shown).

Discussion
The herpetofauna of PNSCo is one of the most diverse of the Caatinga biome, except for the fauna from the isolated forest patches of northeastern Brazil, usually referred as "Brejos Nordestinos".A total of 66 species were recorded (74 species when taking together PNSCo and PNSCa), equating in diversity with previously well sampled areas like Exu in Pernambuco, Valença in Piauí, and Xingó in Alagoas (with 53, 42 and 41 species, respectively) (Rodrigues, 2003a).
Part of the high diversity found in the PNSCo and PNSCa taken together can be explained by landscape heterogeneity, which, in turn, also characterizes the Cerrado units and strongly differs from Caatinga (sensu stricto) areas where the landscape physiognomy is far more homogeneus.However, since the PNSCo and PNSCa are situated in an ecotonal area between these two biomes, they harbor a mix of Caatinga and Cerrado elements, forming an heterogeneous landscape.This results in high species diversity, with species typical from Cerrado (e.g.Hoplocercus spinosus, Coleodactylus brachystoma, Colobosaura modesta) and Caatinga (e.g.Epicrates assisi, Dermatonotus mulleri, Physalaemus albifrons, Corythomantis greeningi, Rhinella jimi, Proceratophrys cristiceps) coexisting in the area.Adding to phytogeomorphological features, historical events also could be acting to increase the local diversity in the southwestern Piauí, as the historical contacts now lost between sandy soils from this region and those from the São Francisco dunes (Rodrigues et al. 2001).
The observed richness of lizards and amphibians might be close to the real diversity in PNSCo since species rarefaction curves for both groups tend toward an asymptote after 34 sampling days (stronger for lizards) and richness estimators recover close values to those obtained.However, some new species records are expected in the future since arboreal, aquatic, fossorial species and ones with explosive reproduction are always more difficult to sample and tend to be underestimated even in long-term and/or large-scale inventories.
Indeed, the most diverse lists of local herpetofauna are those based on intensive field work with long periods of sampling along different climatic seasons and/or mega infrastructure projects with extensive devastation of natural habitats, such as hydroelectric power plants (Pavan & Dixo 2004, Vaz-Silva et al. 2007, Silva Junior et al. 2005, Loebmann & Haddad 2010, Nogueira et al. 2010, Silveira et al. 2010, Recoder et al. 2011, Valdujo et al. 2011, Dal Vechio et al. 2013, present work).In addition, long-term surveys provide necessary material to understand the basic biology of the species (Vitt 1982;Cruz 1994;Mesquita & Colli 2003;Werneck et al. 2009;Dal Vechio et al. 2014, 2015).
Sampling efforts at PNSCo resulted in the discovery and description of five new species: Calyptommatus confusionibus (Rodrigues et al. 2001), Mesoclemmys perplexa (Bour & Zaher 2005), Stenocercus squarrosus (Nogueira & Rodrigues 2006), Ameivula confusioniba and Glaucomastix venetacauda (Arias et al. 2011a).Another three are candidates to new species.Adenomera sp., was detected as a possible new species in a recent molecular study (Fouquet et al. 2014).This species also occurs at EEUU, being probably distributed along the northern Cerrado and ecotonal areas between this domain and the neighbors.Leptodactylus aff.syphax has recently been recognized as an undescribed new species (Loebmann & Haddad 2010;Andrade et al. 2011;Ribeiro et al. 2012;Cavalcanti et al. 2014).Ameivula sp.seems to be a hybrid between A. confusioniba and G. venetacauda (Arias pers. comun).
Five additional species are worthy of comment.The five specimens of Trilepida sampled in the PNSCo have scale counts that are intermediate between T. koppesi and T. fuliginosa.Although quantitatively more similar to T. koppesi, they present qualitative characters that resemble T. fuliginosa (Passos et al. 2006).Trilepida koppesi is distributed throughout the southern Cerrado region (São Paulo, eastern Mato Grosso do Sul and southern Goiás states), while T. fuliginosa is distributed in the northern part of the Cerrado, with the nearest record in Palmas (Tocantins basin), about 520 km in straight line far from PNSCo (Passos et al. 2006).Sampled specimens in PNSCo could either be an undescribed species or represent a large distribution extension for Trilepida fuliginosa and the first record of the species for the Caatinga domain.
Other interesting species is Siphonops paulensis, which is widely distributed in Brazil, with only a few records for the Caatinga biome  (Taylor 1968(Taylor , 1970;;Santana et al. 2015).The specimen of S. paulensis represents the first record for the state of Piauí and fills an important distribution gap for the group in northwestern Brazil.However, it is likely that S. paulensis represents a complex of cryptic species (Wilkinson, pers. comm.).Indeed, Loebmann and Haddad (2010) already pointed out the complex taxonomic nature of this species when they registered Siphonops for the "Brejo Nordestino" Planalto de Ibiapaba and considered their record as possibly representing an undescribed species related to S. paulensis.Here we treat the population in PNSCo as S. paulensis, pending further studies that could clarify the taxonomic status of populations considered to belong to this widely distributed species.
A recent phylogenic work of Tropidurus semitaeniatus showed the complexity of the the species, with several lineages candidates to fully species, inclusive, there are two distinct of these lineages that occur in PNSCo, being one of them exclusive to the park; and there is another exclusive lineage to EEUU (Werneck et al. 2015).Here, we maintain T. semitaeniatus as just one species until further taxonomic approach.
Amphisbaena frontalis is until now known only from the type locality at the left bank of middle São Francisco River in Alagoado, Bahia state.The record in PNSCo expands its distribution on approximately 270 km northwest of the type locality (Vanzolini 1991); and highlights an historical event of sand contact with southwestern Piauí and São Francisco Dunes as mentioned above.Finally, Hoplocercus spinosus is a typical Cerrado species that also occurs in contact areas with forested biomes.In PNSCo, H. spinosus was found in a forested Caatinga, representing the easternmost record and first for the species within the Caatinga domain (Torres-Carvajal et al. 2011).
The PNSCo together with other regional conservation units of similar latitude (i.e.EESGT, EEUU and PNSCa) protect an area of ca.200.000Km 2 in northern Cerrado and western Caatinga.There is a widespread herpetofaunal species throughout this landscape, occuring in all these four units, however, the fauna is more similar between Cerrado's units (EESGT + EEUU) and Caatinga's ones (PNSCo and PNSCa) but not so much between them.Despite the geographical proximity between these Cerrado and Caatinga parks, there is a turnover of congeneric species that seems to be related to the shift of domains (e.g.Tropirurus oreadicus X Tropirurus hispidus; Stenocercus quinarius X Stenocercus squarrosus; Ameivula mumbuca X Ameivula confusioniba; Procellosaurinus erythrocercus X Vanzosaura savanicola; Epicrates crassus X Epicrates assisi; Phyllomedusa azurea X Phyllomedusa nordestina; Leptodactylus syphax X Leptodactylus aff.syphax; Physalaemus centralis X Physalaemus albifrons; Rhinella mirandaribeiroi X Rhinella granulosa; Rhinella schneideri X Rhinella jimi; Proceratophrys goyana X Proceratophrys cristiceps).This shift on is also recovered in the similarity analysis, with PNSCo and PNSCa included within the "Caatinga" group while EESGT and EEUU units cluster within the "Cerrado" group, indicating that the units harbor a typical faunal of each biome.
Our results show that the PNSCo harbors one of the most diverse herpetofauna among the inventoried localities within the Caatinga domain, conferring to the park a strategic role for the conservation of the remaining regions of this vanishing domain.Our results also indicate that, despite geographical proximity, the northeastern Cerrado and Caatinga units studied still retain high levels of diversity and uniqueness with low faunal similarities between domains, evidencing a high species turnover.

Figure 2 .
Figure 2. View of plateau with rock outcrop and arboreal caatinga in its base.

Figure 6 .
Figure 6.Rarefaction curve for lizards.A -after 34 sampling days (two campaign together); B -for each campaign separately.

Figure 7 .
Figure 7. Rarefaction curve for amphibians.A -after 34 sampling days (two campaign together); B -for each campaign separately.

Table 1 .
All pitfall lines with its accurate coordinate and the effort spent in each campaign.