Amphibians from southeastern state of Pará : Carajás Region , northern Brazil

are deposited in the herpetological collection of Museu Paraense Emílio Goeldi (Emílio Goeldi Museum). Valuable information on the region is also available in unpublished documents, such as environmental assessments elaborated for mining projects permits. More recently, one book chapter was published about the amphibian species of one reserve in the region (Neckel-Oliveira et al. 2012). Here we report an updated list of amphibian species from the Carajás region and its surroundings in the southeast state of Pará, together with a classification of the habitats where they were collected.


Introduction
Most of the 946 species of amphibians presently known to occur in Brazil (SBH 2012) were recorded in the last 40 years (Silvano and Segalla 2005) and approximately 250 of these species occur in the Brazilian Amazonia (Frost 2009).The description of new species in a regular basis is a strong indicator that this number may increase.However, species composition and richness data for Amazonian amphibians is still unknown for several localities (Azevedo-Ramos and Galatti 2002).
Although Amazon as a whole holds the largest diversity of amphibians in the world, the knowledge on the ecological and biogeographical factors affecting the local diversity is still limited, depending mainly on inventories with standardized collecting efforts.Most published inventories reported sampling efforts of less than two months, and were carried out on forested areas, neglecting areas of difficult access that harbor a variety of phytophysiognomies (Azevedo-Ramos and Galatti 2002).Besides, several studies as well as important data stored in collections were either not published yet or were so in nonindexed literature (Silvano and Segalla 2005).It is widely recognized that taxonomic collections are important tools to generate species lists (Shaffer et al. 1998), providing fundamental insights towards the understanding of biodiversity and biogeography that will ultimately allow the development of adequate conservation strategies (Haddad 1998).
The region of Carajás has five official reserves, holding two main kinds of vegetation, ombrophylous forest (dense or open) and metalophylous savanna (Amazonian savanna -composed mainly by herbs and shrubs restricted to iron ore outcrops).Several samplings of amphibians have been conducted in this region since 1969.Most of the vouchers and associated information produced by those inventories Abstract: The region of Carajás in the southeast of the state of Pará, Brazil, harbors five reserves, with various managing categories, distributed throughout five municipalities.A list of amphibians known to occur in this region was compiled using information on the specimens deposited in the herpetological collection of the Goeldi Museum, collected during the past four decades (1969 -2010).According to the available metadata, the species were tabulated in three environments: ombrophylous forest (rainforest), metalophic savanna (MS) and anthropic areas (AA -secondary forest -disturbed areas), resulting in 13 families and 71 species (66 anurans and 5 Gymnophiona).Ombrophylous forest has 50 species, anthropic areas has 49 species, while metalophic savanna has 38 species of anuran.south by the Carajás National Forest (05°52' -06°33' S, 49°53' -50°45' W) (Figure 1).This conservation system spreads along six municipalities (Marabá, Parauapebas, Canaã dos Carajás, Água Azul do Norte, São Félix do Xingu and Curionópolis (surrounding area), allowing effective landscape and biodiversity conservation through protection against land invasion, hunting, non-planned mining, illegal logging, and forest fire (Rolim et al. 2006).However, it is recognized that cattle raising and large-scale mining activities have been increasing the deforestation pressure in the last few years (Reis 1996;Monteiro 2005).
According to data obtained from meteorological stations located in Carajás and Tapirapé-Aquirí National Forest, the region's weather is classified as Aw -humid tropical with dry winters and average precipitation of 60 mm in the driest month (IBAMA 2004).There are two distinct seasons, a rainy season from November to April, with average precipitation of 248 mm (70% of the year's total) and a dry season, between June and September, with average precipitation of 32 mm (7% of the year's total).During the transition months (May and October) the average precipitation reaches 23% of the year's total (IBAMA 2004).The study area presents three predominant phytophysiognomies, dense and open Ombrophylous Forest (OF) and the Metalophic Savanna (MS) (known regionally as "Canga").The canga is a non-forest, open formation that grows directly from outcrops of iron ore, being restricted to the top of hills whose average plateau surface is 650 m (Silva et al. 1986).Besides these three main vegetation formations, there are large areas covered with secondary vegetation, pastures, forest fragments and other anthropic landscapes, mainly in the lowlands on the surroundings of the conservation unities, here referred to as Anthropic Areas (AA).
To describe the amphibian assemblage spatial distribution at a local scale, we tabulated each recorded species according the three main habitat types occurring in Carajás region: ombrophylous forest, metalophic savanna and anthropic areas.This categorization was made using the data extracted from the labels of the specimens deposited in MPEG and updated vegetation charts of the region.Unfortunately, it was not possible to differentiate between open and dense rain forest.Additionally, this separation was made only to facilitate comparisons with other localities of the forest and savannah.
Comparisons among different regions may raise several methodological problems, including intrinsic differences between areas, differences in the size of the areas, distances among rivers and differential sampling efforts (Duellman and Thomas 1996;Martins and Oliveira 1998).This kind of comparison is especially troubling in Carajás region since there are differences even among areas of ombrophylous vegetation (Silva et al. 1986).The present contribution represents the first step towards characterizing the amphibian species composition in different natural phytophysiognomies present in the study area, also depicting an effort to understand how the species are responding to the environmental modifications, as suggested by its presence or putative absence in anthropic areas.The extreme differences between the vegetation types encountered in the ombrophylous forest and the canga are a reflection of even more extreme abiotic differences.For example, metalophic savanna areas are located in more elevated sites, with shallow soils, suffering high levels of insolation and hydric stress (Almeida 1986).The characteristics found in each environment will be determinant in the presence or absence of amphibian species.
For amphibians, differences observed in species composition in different environments can be strongly related to variations in the microhabitat availability (Tocher 1998), hydric resources (Zimmerman and Bierregaard 1986), temperature and moisture gradients (Vonesh 2001;Haddad and Prado 2005), vegetation structural complexity (e.g.Inger and Colwell 1977;Heinen 1992;Tocher 1998;Pawar et al. 2004;Souza et al. 2008), edaphic factors (Menin et al. 2007) and altitude (Fauth et al. 1989).However, more research is necessary to understand how these environmental factors intervene in the diversity and distribution of amphibian communities.
Fifty amphibian species were recorded in the ombrophylous forest areas, nine of which were exclusive of this vegetation type.Typically, forested areas present high species richness, which could be attributed to the high environmental heterogeneity of these sites, as observed for other animals (e.g.Pianka 1967, Tews et al. 2004, Keller et al. 2009, Silva et al. 2011).This vegetation type holds more microhabitat availability, including those suitable for reproduction, allowing the occurrence of species that are more sensitive to anthropic alterations, such as those of the families Aromobatidae e Dendrobatidae.The species recorded in forested areas exhibit a variety of reproductive strategies, ranging from the use of water bodies (Ctenophryne geayi, Pipa spp., Ceratophrys cornuta, Adelphobates galactonotus, among others) to terrestrial humid environments (Ameerega spp., Phyllomedusa spp.and Leptodactylus andreae).
Thirty-eight anuran species were recorded in metalophic savanna areas.Samplings from those areas are more recent than those from ombrophylous vegetation and most of them do not show distinction between the two kinds of vegetation.Brazilian Amazonia savannas are generally poor sampled with regards to amphibians (Azevedo-Ramos and Galatti 2002).Neckel-Oliveira et al. (2000), studied the amphibian fauna in Alter do Chão, Santarém, State of Pará, which presents vegetation types similar to those encountered in Carajás, and reported eighteen anuran species which are recorded from other areas in Brazilian Amazonia as well.These species, as well as the majority or those occurring in savanna areas in Carajás, present reproductive strategies that lead to the reduction in the dependence of forested wet environments, such as to deposit eggs directly in water bodies, which decreases considerably the risk of desiccation (Lynch 1979), ecological characteristics also found in species that live in Caatinga (dry land) (Vieira et al. 2008) Forty-nine species were recorded in the anthropic areas, highlighting the importance of secondary forest maintenance, since these vegetation types are responsible for sustaining a significant component of the anuran communities in the region.Secondary forest covers more than 40% of the forested areas in the world (Wright and Muller-Landau 2006) and may represent an important alternative habitat for amphibians but its relative importance in tropical regions have been widely neglected (Heinen 1992;Neckel-Oliveira 2004;Ernst and Rödel 2005;Neckel-Oliveira and Gascon 2006).In a study conducted in two sites with preserved and altered environments, it was recorded a number of species with wide distribution, and more than 60% of the species in both sites are considered common (Caldwell and Araújo 2005).Besides that, some species can co-exist in or near disturbed areas, such as Rhinella marina, Hypsiboas geographicus, Trachycephalus typhonius, Scinax ruber and Leptodactylus hylaedactylus.Disturbances in the forest may cause several effects on amphibian populations, which can generate an over abundance of more generalist species to the detriment of other more specialized habitats, with several subsequent consequences (Caldwell and Araújo 2005).
The high environmental heterogeneity provided by the occurrence in the same region of undisturbed ombrophylous forest, anthropic areas, and a unique environment in Amazonia, the metalophylous savanna, could explain at least in part, the high diversity of amphibians in this region.Most of the species recorded in Carajás region present wide distributions across Amazonia and some of them occur even in other South American biomes.However, some of the species recorded here are more related to Central Brazilian biomes, such as Ameerega flavopicta, a species known to be endemic in Cerrado.A vicariant population of this species was already reported from Serra dos Carajás (Haddad and Martins 1994).Pseudis tocantins, recorded in this paper, from Marabá (05°23'52.3"S, 49°10'13.9"W), had its known distribution increased nearly 600 Km toward north from its nearest previous record (Palmas, State of Tocantins) (Brandão et al. 2003).
Leptodactylus syphax, found in the metalophic savanna at Carajás National Forest (50°24'27" S, 06°20'46" W), had its known distribution increased 600 Km toward north from its nearest known locality of occurrence (Ponte Alta do Tocantins/TO) (Valdujo et al. 2011;Neckel-Oliveira et al. 2012).This species is typical from open areas, being recorded from Cerrado areas in the States of Mato Grosso, Minas Gerais, Piauí and Tocantins, associated to cave environments (Cardoso and Heyer 1995; Heyer et al. 2004) which are common in the study area.Pseudopaludicola canga (Family Leiuperidae) is the solely species endemic to Carajás region, occurring only in the savanna areas in the hills of Carajás (Giaretta and Kokubum 2003).
The knowledge on the distribution of species of the family Caecilidae is still sparse.The absence of information on these animals could be assigned to several factors, including difficulties in the sampling and in the taxonomic identification.As a rule, the known distributions are punctual or even restrict to the localities type.For example, Maciel et al. (2009) described a new species of genus Brasilotyphlus, B. guarantus, previously identified as B. braziliensis.Its type locality is located in the far north of State of Mato Grosso (Guarantã do Norte municipality) but it is also recorded in the municipality of Parauapebas, state of Pará.Caecilia gracilis was recorded in Carajás (Municipality of Marabá), but only for records at Museum of Zoology University of Sao Paulo (Maciel and Hoogmoed 2011).Since information on particular habitats is normally scarce in material collection, we could not characterize these species in relation to the environment they occur.
Recently, Maciel and Hoogmoed (2011) published a list of caecilian amphibians of Brazilian Amazon with 15 species, of which five occur in Carajás region.Although it is often assumed that the species of Gymnophiona are rare, many species are well represented in scientific collections, such as Microcaecilia taylori, Caecilia gracilis Typhlonectes compressicauda, Potomotyphlus kaupii and Rhinetrema ron, suggesting that some species are not as rare as they seem to be, but it may reflect the methodology adopted (Maciel and Hoogmoed 2011).
Besides this article, Neckel-Oliveira et al. (2012) published a book this year about the species of Carajás National Forest, where 60 species were recorded.This number is relatively high and may reflect the similarity in species composition among the reserves, but this can only be demonstrated with further analysis.
The difficulty in reaching precise identifications of several taxa that probably represent complexes of multiple species is a common problem involving Amazonian species (Peloso 2010).This issue prevents us from drawing explicit comparisons between different areas and conclusions on the actual distribution of some amphibian species.Some examples of doubtful identification are Pristimantis aff.conspicillatus, P. fenestratus, Leptodactylus marmoratus species group, Allobates marchesianus species group, Dendropsophus microcephalus species group, and several other species with wide distributions in Amazonia (Peloso 2010).Further considering morphological and molecular data might reveal complexes of cryptic species studies within these groups and bring new insights into their taxonomic limits.
As a result of these taxonomic uncertainties, more precise comparisons among areas in Amazonia and, consequently, conservation measures based in the observed diversity of a given area, are threatened, reflecting severe biases regarding the actual compositional similarity among areas to be selected for conservation purposes.

Table 1 .
Species list of Carajás region found in differPeloso and Sturaro 2008;Frost 2009;hic distribNarvaes and Rodrigues 2009;Maciel and Hoogmoed 2011)0;Peloso and Sturaro 2008;Frost 2009; IUCN 2009;Narvaes and Rodrigues 2009;Maciel and Hoogmoed 2011).Habitat types = OF: Ombrophylous Forest (dense or open); MS: Metalophic Savanna; AA: Anthropic Areas.The authors wish to thank Dra. Ana Lúcia da Costa Prudente, curator of the herpetological collection of Museu Paraense Emílio Goeldi, for making specimen data available; Adriano Maciel for identifying the species of the family Caecilidae; João Fabrício de Melo Sarmento for helping in the search for data in the collection; Alexandre B. Bonaldo for helping with English version; and all the scientists who have collected in the study area along the years and others who contributed in several different ways for the elaboration of this paper.This paper was supported by CAPES (L.C.P. Masters Grant) and CNPq (Y.O.C.B Masters Grant).Alytes 13: 67-73.Caldwell, J.P. and M.C.Araújo.2005.Amphibian faunas of two eastern Amazonian rainforest sites in Pará, Brazil.Occasional Papers Sam Noble Oklahoma Museum of Natural History 16: 1-41.Duellman, W.E. and R. Thomas.1996.Anuran Amphibians from a seasonally dry forest in Southeastern Peru and comparisons of the Anurans among sites in the Upper Amazon Basin.Occasional Papers of the Museum of Natural History of the University of Kansas 180: 1-34.