New records of spiders ( Arachnida , Araneae ) from the state of Roraima , northern Brazil

The Brazilian spider fauna comprises thousands of described species, mostly known by only one or two records, and there are large sampling gaps. The spider fauna of the state of Roraima is enigmatic in Brazil and remains largely unknown. Herein, we present a list of spider species recently collected during an expedition in Roraima. Species-level identifications were possible for 229 adult individuals of 54 species. Five species are newly recorded from Brazil, and 30 species are presented for the first time from Roraima. Most of these new records are represented by widespread species, representing the huge and historical deficiency in the spider sampling throughout Roraima.


INTRODUCTION
Brazilian spiders are suitable for the study of diversity patterns and geographical distribution owing to the existence of a large database that includes all records in taxonomic publications, among other records (i.e., Brescovit et al. 2011;Oliveira et al. 2015).As of 2013, there were 3,425 spider species recorded from Brazil, but about 40% of these species are known only by single records, while about 45% have between two and 15 records, 10% have between 16 and 60 records, and only 2% of the species are represented by more than 100 records (Oliveira et al. 2015).This heterogeneous knowledge is highly influenced by where the main national research institutions, which harbor the most significant collections, and researchers on spider systematics are located.Collections are mostly composed of species gathered nearby (Brescovit et al. 2011), significantly associated to access routes, creating larger knowledge shortfalls in localities far from the main research centers (Oliveira et al. 2016).
As a consequence of the general deficiency of sampling in Roraima, any expedition focusing on sampling arachnids in the region is expected to result in a large number of undescribed or, at least, under-recorded species (even for widespread species).Recently, we performed a short survey in four municipalities (Amajari, Boa Vista, Bonfim, and Cantá) at Roraima, and here we present a species list of these spiders and update their geographical distribution.

MATERIAL AND METHODS
The sampling was conducted in the state of Roraima in northern Brazil.The state borders Venezuela on the north and west and Guyana on the east.To the south is the state of Amazonas, and to the southeast, the state of Pará.Additionally, the region represents a large ecotone area; flanked by the Amazon Forest to the south and west, by savannas to the east, and by mountainous regions, with altitudes up to 3,000 m, to the north (Eden & McGregor 1998).The climate is characterized by three climate categories in Koppen's classification: Af (constantly humid regions with low annual variations in rainfall and temperature), Am (humid summer and short term dry winter seasons), and Aw (with four months of a real drought) (Barbosa et al. 1997;Falcão & Costa 2012).In general, lowland Roraima has annual mean temperature ranging between 26 and 27°C, which decreases considerably with elevation (Eden & McGregor 1998).The mean annual rainfall varies from 1,100-1,400 mm/year in the northeast to 2,000-2,300 mm/year in the southwest (Barbosa et al. 1997).Such heterogeneous climate and topography allow for the existence of different habitats, such as terra firme forest, seasonally flooded forest (várzea and igapó), white-sand forest (campina and campinarana), savanna, gallery, and dry forests, and various types of montane forests (Naka et al. 2006).
In July 2014, a 10-day sampling campaign was carried out in Roraima (Figure 1), in the municipalities of Amajari (Figures 2-6), Boa Vista, Bonfim (Figure 7), and Cantá.Collecting permits were issued by the Instituto Chico Mendes de Conservação da Biodiversidade (ICMBio) through the Sistema de Autorização e Informação em Biodiversidade (SISBIO #44225-1).Arachnids were collected through diurnal and nocturnal manual searches that did not follow any  standardized protocol.
Natural history: The specimen was found on the ground inside a burrow, which was lined internally with threads (as also described by Bertani & Araujo 2006).It was captured by digging out the soil.The surrounding area consisted of secondary terra firme vegetation.
All specimens were deposited in the following arachnid collections: Coleções Taxonômicas da Universidade Federal de Minas Gerais, Belo Horizonte, Minas Gerais (UFMG; curator A. J. Santos); Coleção de História Natural da Universidade Federal do Piauí, Floriano, Piauí (CHNUFPI; curator E. F. B. Lima); and Museu de Zoologia da Universidade de São Paulo, São Paulo, São Paulo (MZSP; curator R. Pinto-da-Rocha).Photographs were made using a Leica M205C stereomicroscope equipped with a Leica DFC295 digital camera.Images in different focal planes were assembled in multi-focus images using the software Leica Application Suite ver.3.3.0(Leica Inc.).The map of the sampling points was constructed in ArcMap 10.0 (ESRI), using WGS84 datum (the same used to obtain the geographical coordinates during the sampling).
The list of spiders presented herein is mainly composed by widely distributed species (50 spp.; 92% of the total), and only four species are known to have a restricted Distribution: the theraphosids Guyruita waikoshiemi (Bertani & Araújo, 2006), Psalmopoeus irminia Saager, 1994 and Theraphosa stirmi Rudloff & Weinmann, 2010, and the orb-weaver araneid Hypognatha cacau Levi, 1996.The theraphosid species are distribuited only in the Guiana shield, while H. cacau is known from the northern Amazon Forest.
Four species are recorded in Brazil for the first time: the theraphosids G. waikoshiemi and T. stirmi, the selenopid Selenops geraldinae Corronca, 1996, and the orbweaver araneid Wagneriana taboga Levi, 1991.Additionally, 30 species are recorded from Roraima for the first time.No species of medical importance was recorded.Additionally, five recorded species are widely distributed and/or can be found in synanthropic environments: Argiope argentata (Fabricius, 1775) (Araneidae), Micropholcus fauroti (Simon, 1887) (Pholcidae), Philoponella vittata (Keyserling, 1881) I-II, and divided tarsal scopula III-IV (Guadanucci et al. 2007).The females of G. waikoshiemi  can be distinguished from congeners by the incrassate tibia I (Guadanucci et al. 2007; see Figure 14) and by the spermathecae being multilobulated at the apical portion (Guadanucci et al. 2007; see Figure 15).The female specimen presented the diagnostic features for the genus (Figures 12 and 13) and species (Figures 14 and 15), but its spermathecae presented sclerotized receptacles positioned more apically than the holotype specimen drawn by Bertani & Araújo (2006).However, we consider this to be intraspecific variation.

Carvalho & M.C. Schneider leg. (UFMG 17888).
Distribution: This species is known from its type locality in northeastern Venezuela (Gran Sabana, Estado Guyana) (Saager 1994) and the municipality of Pacaraima (Roraima) near the Brazil-Venezuela border (Bertani et al. 2016).The new record extends the geographical distribution of this species by about 102 km toward the southwest.
Distribution: This species has a pantropical distribution and is introduced to Europe (Šestáková et al. 2014).It is commonly associated with human habitations throughout Central and South America (Brescovit & Rheims 2000).

Family Sparassidae Bertkau,1872
Quemedice piracuruca Rheims, Labarque & Ramírez, 2008 Quemedice piracuruca Rheims et al. (2008).Distribution: This species was previously recorded only from Colombia and Brazil (Minas Gerais and Piauí) (Rheims et al. 2008), and the new record from Roraima extends the known geographical distribution by at least 1,400 km toward the northeast.
Distribution: The distribution pattern of this species was unclear for many years.It was known only from Argentina and Paraguay (Platnick 1986), until recently found in the state of Piauí, northeastern Brazil (Carvalho et al. 2014).The new record from Boa Vista, Roraima, represents a range extension of 2,300 km toward the northwest.This species may be widely distributed over the Cerrado biome, but the scarcity of sampling in appropriate microhabitats for the species hinders the validation of this hypothesis.
Natural history: All specimens of T. gomezi were collected from under bark of Curatella americana L. (Dilleniaceae) by carefully removing pieces of bark with a forceps.These spiders usually run laterally on the tree trunks to hide in small spaces in, or under, the bark.The association between T. gomezi and C. americana was also reported in the state of Piauí by Carvalho et al. (2014).As C. americana is widely distributed from from Central America to Bolivia, and in almost all of Brazil, especially in the Cerrado biome (Sarmiento and Monasterio 1983;Vilar et al. 2009), further sampling effort from the barks of C. americana should be made.This may provide more precise information on the natural history of T. gomezi.

DISCUSSION
The data presented here were opportunistically collected and may be taxonomically, temporally, and spatially biased.That is, relatively conspicuous (widespread) species were more often collected, the sampling period was short, and sampling sites were close to main roads.Most of the species recorded, including 32 of the 36 species newly recorded from Brazil and/or Roraima, are widespread species, but the new data are not unimportant.On the contrary, these data reflect the historical paucity of spider sampling throughout Roraima.Thus, there is the need to expand spider surveys in this region.The sampling heterogeneity in Roraima is not different from the overall situation throughout Brazil (Brescovit et al. 2011: fig. 5), and corresponds to a general rule for Brazilian invertebrates, vertebrates and angiosperms (Lewinsohn et al. 2005;Oliveira et al. 2016).Even within the relatively betterstudied animal groups and biomes, such as the Atlantic and the Amazon Forests, geographic coverage is very restricted and often just a few localities have been sampled adequately (Lewinsohn et al. 2005).As a result, there is a strong spatial bias regarding the species richness, species composition and endemism knowledge in the Brazilian biodiversity (Oliveira et al. 2016).
Information from natural history collections, such these presented here, are important as they are easily usable and present a high precision in georeferencing (Graham et al. 2004).This type of data can be used in species distribution models for many purposes, such as conservation (Ferraz et al. 2012).These collection data are also crucial because they are a permanent record of a species at a given place and time (Funk & Richardson 2002).
Our sampled localities are within the areas of endemism of Roraima, supported by a relatively low number (at most 12 spp.) of synendemic spider species (Oliveira et al. 2015).However, our results suggest that these areas harbor a higher number of synendemic species than the survey by Oliveira et al. (2015), which therefore had clearly sampling bias.Additionally, the relevancy of our results relies on the use of a high number of species associated with high endemism levels for conservation purposes.The basis for environmental management and conservation policies is, at a bare minimum, the distribution and abundance of every species that requires conservation (Possingham et al. 2007).
The spider fauna of Roraima is one of the most poorly known in Brazil, with only a few published papers and mostly related to the spiders of the Maracá Island (where there are 92 recorded; number updated using the current spider nomenclature; see World Spider Catalog 2017), or individual species descriptions (Lise 1998a(Lise , 1998b;;Buckup & Marques 1989, 1991, 1992;Marques & Buckup 1992).Of these, only seven species (about 7.5% of the total) were recorded in our samples: the araneid orb-weavers Aculepeira travassosi, Amazonepeira masaka, Araneus guttatus, and Argiope argentata, the pisaurid Architis tenuis, the theridiid Dipoena atlantica, and the palpimanid Otiothops oblongus.
As observed, we expected a large number of previously unrecorded species as result of sampling anywhere in the state.However, future surveys should focus on remote and mountainous regions (e.g., Mount Roraima), or unexplored niches (e.g., soil and leaf litter).Such surveys may provide a wider overview of the whole spider fauna.Additionally, long-term or ecological studies on arachnids of Roraima have never been done.Such research would be a very interesting because the spider dynamics in the Cerrado (savanna) patches within the Amazon Forest is still completely unknown.(UFMG), Bárbara T. Faleiro (UFMG) and José Paulo Leite Guadanucci (UNESP) for assistance with species identification; and Regiane Saturnino (MPEG) and two anonymous reviewers for the revision of an early version of the manuscript.The fieldwork was supported by the project "Meiose em escorpiões (Arachnida): modelo para compreender a evolução em espécies com cromossomos aquiasmáticos", funded by Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP, Process #2011/21643-1).JCG is financially supported from FAPESP, grant #2013/20262-0.The surveys in Roraima were part of LSC's Ph.D. project.