Community structure and composition of litter spiders ( Arachnida : Araneae ) and influence of macro-climatic factors on Parque Ecológico Jatobá Centenário , Morrinhos , Goiás , Brazil

Acknowledgements: I am grateful to my graduation supervisor, Professor Marcos Antonio Pesquero, Universidade Estatual de Goiás, and my colleagues, Adagmar Vaz Ferreira and Diggenes de Souza Oliveira, for help in the collection and sorting of the samples. Professor Kleber Del Claro, Universidade Federal de Uberlândia, also provided valued comments on the project design and report. Dr Antonio Brescovit, Instituto Butantan, is very gratefully acknowledged for identifying over 100 morphospecies sample to family, genus and species levels, where possible. I am also most grateful to Drs. Tracey Churchill and Robert Raven, Queensland Museum, for reading the manuscript and providing valued criticisms of content. Abstract: Spiders are a diverse group and are considered to be good bioindicators due to their sensitivity to variation in biotic and abiotic factors. Despite this the taxonomy of the Araneae is poorly known, particularly in the tropical and subtropical regions. The use of spider guilds can improve our understanding of the dynamics of spider communities, and in this paper we analyse the influence of climatic factors on guilds and species dominance of spiders within the leaf litter layer of a semi-deciduous forest in the tropical savanna Cerrado, Brazil. The study site was Parque Ecológico Jatobá Centenário, a fragment of 90ha, in Morrinhos, Goiás, Brazil. Spiders were sampled from November 2006 to August 2007 using pitfall traps that remained open for seven days on each of four occasions. Overall 4139 spiders from 35 families and 118 species were collected. The main families were Salticidae (28%), Linyphiidae (27%), Lycosidae (12%) and Theridiidae (11%). In terms of richness the main families were: Theridiidae, Salticidae, Corinnidae and Araneidae, with 18, 16, 15 and 13 species respectively. The overall Shannon-Wiener (H’) diversity was 3.6. The rainy season showed higher values than the dry season for abundance (2,868 and 1,271 respectively), richness (100 and 71) and diversity (3,296 and 3,237). The families Theridiidae, Corinnidae and Salticidae presented more species in both dry and wet seasons. Observed climatic variation (rainfall, humidity and temperature) between seasons influenced the community structure of ground-dwelling spiders.


INTRODUCTION
Spiders, Order Araneae, are a group of megadiverse arthropods with 3,960 genera and 45,674 species currently described worldwide (Platnick 2015).As in most invertebrate groups the taxonomy of the Araneae is poorly known, mainly due to the limited number of specialists (Lewinsohn & Prado 2002).Coddington & Levi (1991) estimate that the true diversity of spiders is over 100,000 species, with most occurring in the tropical and subtropical regions.Studies on spiders are of ecological interest because they are abundant generalist predators in terrestrial ecosystems, effecting population control of other arthropods, notably of phytophagous insects (Roth 1993).Sensitive to environmental heterogeneity (Hatley & MacMahon 1980;Gunnarsson 1990;Baur et al. 1996;Raizer 2004), spider communities are utilised as bio-indicators in studies assessing the condition of terrestrial biomes (Baert et al. 1991).
Patterns of species richness in spiders can vary spatially and temporally (Uetz 1977).Temporal changes in the composition of spider communities can be influenced by changes in soil moisture, temperature, rainfall, flooding regime, prey availability, competitors and predators (Uetz 1977;Schaefer 1987;Battirola et al. 2004).The spatial stratification (horizontal or vertical) of spider fauna is strongly influenced by the physical structure of the environment (Uetz 1991;Raizer & Amaral 2001).
The Cerrado (Brazilian Savannah) is one of 25 global hotspots for biota with high conservation priority (Myers et al. 2000).The richness of this biome can represent up to 33% of the Brazilian biota (Aguiar et al. 2004).Strategies for the conservation and sustainable use of remnant vegetation are urgently required due to the rapid rate of destruction of these tropical forests and the associated species extinctions (Espírito-Santo et al. 2002).
This study aimed to characterize the spider community of the leaf litter in a semi-deciduous tropical forest remnant inside the Brazilian Cerrado, and identify the correlated climatic factors.

Study Area
The study was undertaken at the Parque Ecológico Jatobá Centenário, hereafter referred to as PEJC (Fig. 1).With an area of 90ha, PEJC is located north of the city of Morrinhos in the microregion of the Meia-Ponte basin, which lies in the southern part of the state of Goiás, Brazil (17 0 43'36"S & 49 0 07'55"W), at an altitude of 790m.The study area lies within the Plateau Demoted of Goiânia that includes convex landforms dominated by tabular quartzite and the mica group Araxá, and situated between 600 and 850 metres elevation (Nascimento 1992).
The climate is defined as AW according to the classification of Köppen (Lohmann et al. 1993), characterized by two well defined seasons, one dry and cold and the other hot and rainy.
Originally, various categories of vegetation called "cerrado" sensu lato covered the entire region (Eiten 1993).The PEJC aims to preserve the native vegetation as well as the spring and the Açude stream.The vegetation is a semi-deciduous stationary forest (Veloso et al. 1991) and is represented by trees up to 25m high.In the southern region of the park, several water holes join forming the Açude stream, where characteristics of the soil support ferns, palms and trees with tabular and air roots.

Collection procedure
Pitfall traps were used for the collection of spiders in the leaf litter in PEJC.This method is widely employed in the study of dwelling active arthropods (Barreiros et al. 2003;Candiani et al. 2005;Rocha-Dias et al. 2005;Lopes et al. 2006;Brito et al. 2007;Oliveira et al. 2007;Podgaiski et al. 2007).
Sampling was restricted in 12 quadrats, number of traps and distance between the trap is as follows (Figs.
Pitfall traps were made of plastic cups (500ml, 13cm tall and 8.5cm in diameter) buried with the lip close to the soil surface and containing 200ml of preservative solution (4% formalin with 4 drops of detergent liquid).The study was conducted from November 2006 to August 2007: with two collections during the rainy season and two during the dry season.The pitfall traps were left open for seven days on each occasion.

Identification of spiders collected
Spiders were collected and preserved in 70% ethanol and then transported to the Laboratory of Ecology, State University of Goiás, for identification to family and morphospecies level using the identification keys of Pikelin & Schiapelli (1963) and Brescovit et al. (2002).Upon completion of this study, the specimens were deposited in the collection of the Laboratory of Arthropods of the Butantan Institute in São Paulo, SP, Brazil.

Climate Data
The abiotic data relating to mean temperature, mean rainfall and relative humidity were obtained from the Meteorological station of the Department of Geography, State University of Goiás -Unit University of Morrinhos, GO, Brazil.

Data Analysis
The Shannon-Wiener (H') diversity was calculated for the entire sample and for each season was sampled (wet and dry) by using the PAST version 1.36 (Hammer et al. 2001).
The normality analysis of data on "abiotic" variables (relative humidity, mean temperature and average monthly rainfall) and "biotic" spider variables (species richness, abundance and diversity) was performed using the Lilliefors test.
The difference between the relative humidity, mean temperature, mean rainfall, abundance, richness, adults and juveniles in the dry and rainy seasons and the difference between male and female of each family were analyzed using the Mann-Whitney U test, because of the non-parametric distribution of the sampled data.All data were processed using the programs BioEstat 5.0 (Ayres et al. 2007) and Microsoft® Office Excel 2007 Species accumulation curve was estimated using EstimateS 9.1.0(Colwell 2013).
To analyze the interference of climatic factors on community structure permutation MANOVA on R package Vegan 2.3-0 (Oksanen et al. 2015) was used.

Diversity of spider fauna
A total of 4,139 spiders were captured belonging to 118 morphospecies and 35 families (Table 1).Adults represented 52% of all spiders: 1,275 males and 877 females.All families sampled had mature individuals.Only adults were subjected to data analysis, as the reliable identification of spiders to family level relies on mature reproductive structures.The species accumulation curve reached 135 and 137 species with Chao1 and Chao2 respectively (Fig. 3).
The Shannon-Wiener diversity index H' was 3.519.

Seasonality of the spider fauna
In the rainy season (April to September) a total of 2,868 spiders were captured, including 1,419 adults and 100 morphospecies.The number of adult males and females was even (50%), whereas in the dry season 1271 spiders were sampled, with 733 adults grouped into 71 morphospecies.About 58% of all spiders collected were adults representing 77% male and 23% female only (Fig. 7).
The Theridiidae was the most species rich family followed by Salticidae and then Corinnidae in both wet season (16, 14 and 13 morphospecies, respectively) and dry season (12, 12 and 08 morphospecies, respectively).Araneidae was the fourth richest in the rainy season with 12 morphospecies, while in the dry season the fourth was Lycosidae with four morphospecies (Fig. 8).
The families that represented the greatest numbers of spiders collected in the rainy season were the Salticidae, with 987 individuals; Lycosidae, with 309; Linyphiidae with 276 and Theridiidae with 242 (Fig. 9).These families represented 63% of total spiders collected during this period, and 54% of adults collected.Members of the family Mysmenidae were not encountered during this season.The Deinopidae, Titanoecidae and Zodariidae were represented by two specimens each, while only one individual of the Oxyopidae and Uloboridae were  The diversity of the dry period was H' = 3.237, while the rainy season was H' = 3.296.

Comparison between wet and dry season related araneofauna
The relative humidity averaged 71.1% ± 13.26 in the first wet season collection (November 2006), with a minimum of 41% and a maximum of 98%.In the month of the second wet season collection (February 2007) the average relative humidity was 77% ± 7.69, with minimum 51% and maximum of 93%. In
The temperature in the month of first sample showed a mean of 23.93 0 C ± 1.76, with a minimum of 14.3 0 C and maximum of 34.3 0 C; in the following sampled month the mean was 24.07 0 C ± 0.81, with a minimum of 16.5 0 C and maximum of 32.1 0 C; in the third month of sampling the mean was 20,93 0 C ± 2.03, with minimum of 6.8 0 C and maximum of 31.7 0 C, and the last sampling the average was 21,09 0 C ± 1.78, with a minimum of 9.6 0 C and maximum of 34.8 0 C (Fig. 11).
The accumulated rainfall in the months of collections was 137.9mm in the first, the second 148.4mm, 5.4mm in the third and fourth 0mm.Significant differences were observed between the relative humidity (U = 161, P<0.0001), the temperature (U = 354, P<0.0001) and precipitation (U = 831, P<0.0001) between the two seasons.However, a high correlation between the climatic factors was found (Table 2).
The mean annual temperature of approximately 22 0 C and relative humidity and high rainfall during the warm months and very low in the cold months is typical feature of tropical savanna climate (Lohmann et al. 1993).

Diversity of spiders
Of spider inventories in Brazil, few have surpassed the total abundance, abundance of adults and number of families observed in this study.Of those few, Rocha-Dias et al. ( 2005  results were found in several studies with soil spiders except family Araneidae which usually is only sampled with high richness in studies using tree and shrub collections (Candiani et al. 2005;Rocha-Dias et al. 2005;Rodrigues 2005;Podgaiski et al. 2007).This phenomenon can be explained by males seeking females, dispersal of newly matured females and/or juveniles, noting that the vast majority of individuals collected were adults and 64% of individuals belonging to this family were obtained in the first collection in rainy season, a period where most species starts mating (Lopes et al. 2006).The Alpaida sp.represented the majority of individuals of this family, being a genus typically represented by tree species, found in abundance in the inventories of the Amazon and the African Savanna (Hofer & Brescovit 1991;Whitmore et al. 2002).The high capture rate of this spider may be related with the precipitation, when arboreal species could drop from the trees because of heavy rain.Salticidae had the largest number of individuals, with the predominance of juveniles in the rainy season.Gasnier et al. (1995), Green (1999) and Toti et al. (2000) reported high abundance of this family on bushes and trees, which may be an indication that the rainy season is the period of dispersal of immature individuals.Agreeing with Jocqué (1984), jumping spiders are common in tropical soil, since the high temperatures benefit wandering spiders.A more detailed study would show which hypothesis is true about the immature specimens found in this study, dispersion of bush and tree jumping spiders or high levels of juveniles of soil salticids.
The abundance of the family Lycosidae reflects anthropic action in the sampled area, because they are more frequent in open environments and are considered good biological indicators (Costa et al. 1991), besides having a strategy of predation active hunting, moving through wide area.Linyphiidae is a family abundant in several studies, as noted by Indicatti et al. (2005) wherein 60% of their specimens belonged to this family.These spiders are typically present in litter.They are also species that nest in the upper strata of vegetation (Lopes et al. 2006).The family Theridiidae features a high phenotypic plasticity, being found in many environments and strata, also urban areas (Lopes et al. 2006).Another factor that would justify its abundance is the fact that they show a negative correlation between the number of specimens and size of the fragment, i.e., they are less sensitive to the size of the fragment (Miyashita et al. 1998).
Species of Linyphiidae and Hahnidae are more abundant in forest fragments, while Ochyrocera spp.are also abundant in the forest environment (Rock-Dias 2005).Mineo (2009) noted that one species of Tenedos (Zodariidae) was the most abundant in samples in the savannah, but in this study a species of the same  Zodariidae and Linyphiidae species are the most common in open vegetation of Cerrado, while species of the family Zodariidae and the genus Lycosinae (Lycosidae) are the most abundant in cerrado sensu stricto.Mineo (2009) showed that one species of Tenedos, one of Lycosinae and a Euryopis (Theridiidae) are the most represented in dense woodland environment.The genus Tenedos and the most abundant families present in previous studies were sample in this research, with the exception of family Zodariidae.
The family Actinopodidae, despite having several species in Brazil is rarely present on inventories (Mineo 2009;Platnick 2015;Podgaiski et al. 2007;Raizer et al. 2005), probably present species that use the "Stakeout on soil" as foraging strategy (Souza 2007).Despite being a family Amaurobiidae quite common in studies of spiders in a recent survey conducted on different vegetation of the cerrado biome that family was not recorded (Mineo 2009).
Mysmenidae and Nemesiidae families are poorly sampled, Rock-Dias et al. (2005) found specimens related to these two families in forest fragments of Atlantic Forest in southern Bahia, while Barreiros (2004) sampled only family Mysmenidae in an ecological station in Amazon.As both mentioned above and this study collected in dense forest, it can be an indication that these families have a preference to dense forest habitats.
The genus Ariadna (Segestriidae) is distributed on all continents except Antarctica, being found by Barreiros (2004) in the Amazon.The records of these taxa in this study may be the first for Brazilian savannah.

Frequency of spiders
In this study was observed marginally greater amount of spiders (U=87; P=0.06) in the rainy season compared to the dry season, as well as greater amount of females (U=6654, P<0.0001).Candiani et al. (2005), Lopes et al. (2006) andPodgaiski et al. (2007) found similar pattern, observing greater richness in spring and lowest richness in autumn.Spring and autumn coincide with the onset of the rainy season and dry season respectively in the study region.Rodrigues (2005) in a study of the sandbank vegetation of southern Brazil found a different pattern in the distribution of young, males and females.Their samples resulted in 70% of young, while in adults sex ratio was 36% males and 64% females.The difference in diversity between seasons may be related to the high richness and abundance observed in the rainy season, unlike the study reported by Podgaiski et al. (2007) that found greater diversity in the autumn, which was justified by the lack of uniformity presented by the spring, which presented many singletons.

Comparison between wet and dry season related with fauna of spiders
The interference of relative humidity, rainfall and temperature with the structure of the spider community in the study area is expected, because spiders are sensitive to environmental changes.However, the abiotic variables tested in this study explain just 20% of all variation together.The remaining 80% are influenced by other various factors, including microclimatic changes.An example is the residual soil moisture, which negatively influenced litter spider community, i.e., the higher the soil humidity, the lower is the abundance and richness of spiders (Rodrigues 2004).Miglio (2004) did not observe differences in abundances between the dry and rainy season in the Amazon region, with the exception of wetland area.Mineo (2009) showed that in cerrado soil spiders are influenced by climatic factors, the relative humidity influences the total abundance, richness is influenced by several factors depending on the physiognomy, the number of males is influenced by the minimum temperature, relative humidity and the maximum rainfall in 24 hours, number of females is influenced mainly by the high rainfall in 24 hours, and the representation of young are changed by various climatic factors such as among the main maximum temperature and relative humidity.Uetz (1991) states that the structure of the vegetation being together with the heterogeneity of habitats is one of the factors that mostly influence of spider fauna because they are extremely sensitive to small changes in habitat, including the complexity, depth of litter and microclimate (Uetz 1991;Hurd & Fagon 1992).These factors may be responsible for 80% seasonal variation of litter spider community not explained by this study.

Figure 6 .
Figure 6.Spider abundance of males and females from 17 families with the highest number of adults collected in the Ecological Park Centennial Jatoba.(U=102; P=0.07) Figure 9.Total abundance of major spider families according to the season of collection in the Ecological Park Centennial Jatoba.(U=87; P=0.06) Figure 11.Comparison of humidity, temperature and rainfall between stations dry and rainy in the Parque Ecológico Jatobá Centenário

Table 2 . Correlation of climatic factors. genus
was found only in the first collection of the rainy season, being represented only by two males, this may indicate the preference of the species of this genus for open vegetation environments, but more extensive research is neede to prove this hypothesis.