Ground-dwelling spiders (Arachnida, Araneae) in different vegetational formations in a Neotropical floodplain

1 Universidade Federal de Mato Grosso, Programa de Pósgraduação em Ecologia e Conservação da Biodiversidade, Instituto de Biociências. Av. Fernando Correa da Costa, s/n, Boa Esperança, 78060-900, Cuiabá, MT, Brazil. 2 Instituto Butantan, Laboratório Especial de Coleções Zoológicas. Av. Vital Brasil, 1500, Butantã, 05503-900, São Paulo, SP, Brazil. 3 Universidade Federal de Mato Grosso, Instituto de Ciências Naturais, Humanas e Sociais. Campus Universitário de Sinop, Av. Alexandre Ferronato, 1200, Setor Industrial, 78557-267, Sinop, MT, Brazil. 4 Universidade Federal de Mato Grosso, Departamento de Biologia e Zoologia, Instituto de Biociências. Av. Fernando Corrêa da Costa, s/n, Boa Esperança, 78060-900, Cuiabá, MT, Brazil. Kellie Cristhina dos Anjos1 kellieanjos@gmail.com


Introduction
Wetlands are composed of a complex of aquatic habitats, marsh land, and in the case of floodplains, rivers, such as in the Pantanal of Mato Grosso, Brazil. In addition to these habitats, large transition zones between aquatic and terrestrial environments are common (Junk et al., 2006). The Pantanal occupies approximately 140,000 km 2 of the Upper Paraguay River Basin and its tributaries (Harris et al., 2005), and is characterised by seasonal variations in the hydrological regime with alternating wet and dry periods (Heckman, 1998). Due to the low drainage capacity during the aquatic phase, the plains are flooded by overflowing rivers. During the terrestrial phase, they become completely dry (Junk and Nunes-da-Cunha, 2005;Junk et al., 2006).
The geological and geomorphological history of the Pantanal, its location along the margins of three major phytogeographical areas, and the influence of its main tributaries, together results in a high diversity of vegetation types and habitats (Nunes-da-Cunha and Junk, 1999). These features give the Pantanal a highly heterogeneous landscape, consisting of a mosaic of forests, savannahs and grasslands (Silva et al., 2000) which provide habitat for a wide variety of plant and animal species, particularly invertebrates (Adis and Junk, 2002;Battirola et al., 2009Battirola et al., , 2010Marques et al., 2011;Nunes-da-Cunha and Junk, 2014).
Spiders comprise a significant proportion of species diversity in terrestrial environments (Coddington and Levi, 1991;Totti et al., 2000;Dias et al., 2010), and represent one of the most diverse and abundant groups of organisms on the planet with approximately 46,000 species described (World Spider Catalog, 2016). They are generalist predators and perform important functions within natural ecosystems as regulators of insect and other invertebrate populations (Foelix, 1996). The richness and dominance of this taxon in these environments is associated with spatial heterogeneity and habitat structure, determined by plant community composition of different strata (Raizer and Amaral, 2001;Castilho et al., 2005), amount and structure of undergrowth and litter (Souza, 2007), and environmental conditions such as seasonality (Battirola et al., , 2016. Despite the large number of studies carried out in Brazil, research related to spider assemblages in wet areas such as the Pantanal are still scarce (Battirola et al., 2004(Battirola et al., , 2016Castilho et al., 2005;Raizer et al., 2005;Marques et al., 2007). Considering the importance of biodiversity studies involving groups such as Araneae, this study contributes to the knowledge of ground-dwelling spider richness at northern region of the Pantanal of Mato Grosso, and evaluated the distribution of composition, abundance and richness of this assemblage in a vegetation mosaic in a floodplain during the dry season, including murundu fields, pastures and forested areas.  (Figure 1). The climate in this region is Tropical Savannah, Köppen climate classification category Aw, characterised by dry summers and wet winters, with temperatures ranging between 22 o C and 32 o C (Hasenack et al., 2003). Annual rainfall varies between 1,000 and 1,500 mm (Junk et al., 2006). The regional seasonality is determined by four periods, dry season, rising water, high water and receding water, which define the alternation between terrestrial and aquatic phases in this region (Heckman, 1998).

Study area
The wetland vegetation is characterised by a mosaic of forests, savannahs and grasslands, with the occurrence of homogeneous groups or monodominance (Nunes-da-Cunha and Junk, 2014), incorporating the compositional floristic elements of adjacent phytogeographic provinces such as the Cerrado, Amazon and the Gran Chaco (Adámoli, 1982;Silva et al., 2000;Junk et al., 2006). The sampling area covered a range of habitats classified according to Veloso et al. (1991), PCBAP (1997, and Santos et al. (2004), and involved five major vegetation types locally known as landizal, cambarazal and cordilheira, murundu fields and pastures, described below. Landizal, cambarazal and cordilheira were grouped as one landscape unit called "forested areas".
Landizal areas are characterised by low, continuous canopy ranging between 3-7.5 m in height, usually associated with watercourses . This stratum is dominated by Licania parvifolia Huber (Chrysobalanaceae), Calophyllum brasiliense Cambess (Gutiferae), Calypthranthes eugenioides Camb. (Myrtaceae) and Mabea sp. (Euphorbiaceae). Cambarazal areas constitute a homogeneous and dense formation dominated by Vochysia divergens Pohl (Vochysiaceae), the height of which ranges from 5-18 m (Silva et al., 2000), being considered a colonising species of natural wetlands in the Pantanal of Poconé (Prance and Schaller, 1982;Nascimento and Nunes-da-Cunha, 1989). The areas named cordilheiras are characterised by ground elevations of one to two meters above field level, being covered by savannah or forest vegetation that does not directly suffer the effects of periodic inundation (Nunes-da-Cunha and Junk, 1999;Guarim et al., 2000).
Murundu fields are natural fields with portions of higher ground and micro elevations regionally called murundus (Ponce and Nunes-da-Cunha, 1993). These areas are apparently the result of Isoptera (Hexapoda) activity in the construction of termite mounds (Heckman, 1998).
Pastures are natural areas characterised by the predominance of mimoso grass, Axonopus purpusii (Mez) Chase (Gramineae), perennial vegetation resistant to temporary submersion for six months (Nunes-da-Cunha and Junk, 2014). It has a wide distribution, occurring in savannahs, along the margins of bays (permanent and temporary) and mainly in seasonal grassland areas in sandy areas of the Pantanal. Introduced pasture in this region primarily consists of Brachiaria humidicola (Rendle) Schweick (Poaceae), forming pastures not renewed periodically (Nunes-da-Cunha and Junk, 2014).

Methods
Ground-dwelling spider assemblages were sampled using pitfall traps (Adis, 2002). These traps consisted of a polyeth-ylene bottle, 20 cm in height with a 5-6 cm circular aperture that was buried in the soil to intercept organisms traversing the ground. The traps were protected by plastic covers (20 x 20 cm) supported upon four metal rods to prevent interference from leaves, branches and rain. Traps, containing 250 ml of alcohol solution, detergent and 4% formalin, were installed within a 5 x 5 km area containing 30 transects, each 250 m in length, spaced 1 km apart in accordance with the RAPELD methodology. This method, according to Magnusson et al. (2005), allows unbiased estimates of the distribution, abundance, biomass and biogeography of species between sites ( Figure 1). Each sample point was characterised by a 250 m long transect, along which five traps were distributed and remained installed for eight days, totalling 150 samples. Among the 30 sample units, 10 were located within forested areas, 11 in murundu fields, and nine in pasture areas. Samples were transported to the Laboratório de Ecologia e Taxonomia de Artrópodes Terrestres (LETA), Instituto de Biociências, Universidade Federal de Mato Grosso. Spiders were separated from other arthropods and identified to the taxonomic level of family, following the classification proposed by Brescovit et al. (2002). Adult individuals were identified to genus and/or species level at the Laboratório Especial de Coleções Zoológicas, Instituto Butantan -SP, where the reference material is deposited. Behavioural guilds were determined according to Höfer and Brescovit (2001) and Dias et al. (2010).

Data analysis
The ground-dwelling spider composition was evaluated based on the data ordering of the assemblage abundance (quantitative) and occurrence (presence-absence) (qualitative) by Non-Metric Multidimensional Scaling (NMDS), to reduce the dimensionality of data from multiple species (Clarke, 1993). Dissimilarity between the sampling units was calculated using the association matrix through the Bray-Curtis and Sørensen index. Multivariate Analyses of Variance (MANOVA) were used to test for average differences in Araneae assemblage composition, with the two axes of NMDS in relation to the variable vegetation types (forested areas, murundu fields and pastures). Analyses of Variance (ANOVA) were used to compare, individually, abundance and richness of Araneae between vegetation types. The normality of the data was tested by Shapiro-Wilk. For the evaluation of species richness nonparametric estimate methods Jackknife 1 and Bootstrap were adopted. MANOVA and ANOVA analyses were performed using the free software R 2.12.1 (R Core Team, 2013), Vegan package (Oksanen et al., 2014).

Discussion
Despite the specific structural conditions of each vegetation formation (e. g. Junk et al., 1989Junk et al., , 2006Tissiani et al., 2015), abundance, species richness and composition of ground-dwelling spider assemblages did not show any differences between forested areas, pasture, and murundu fields. In addition to the similar distribution between vegetation types, the spider assemblage composition is also comparable to those obtained in surveys conducted in the same region of the Pantanal (Castilho et al., 2005;Raizer et al., 2005;Battirola et al., 2010;Marques et al., 2010Marques et al., , 2011, except for the dominance of Lycosidae and Gnaphosidae. The groups in behavioural guilds, although have not been statically evaluated, show heterogeneous distribution between weavers and hunting spiders, and high prevalence of hunting spiders in all vegetational formations, as registered in other habitats of the Pantanal of Poconé (Castilho et al., 2005;Battirola et al., 2010).
The structural variation between habitats can affect the distribution of resources to the fauna, considering that it offers a three-dimensional array of substrates, physical and chemical, wet and dry, exposed or not, which directly receive the sun's energy (Erwin, 2013). Areas with high complexity in the vegetation can present a larger variety of prey or more diversified sites for spiders to build traps and shelters (Cardoso et al., 2011). However, the similarity between the patterns of ground-dwelling spiders assemblages may be associated to the fact that the landscape formation of the Pantanal's flood plains occurs in a mosaic arrangement (Silva et al., 2000;Nunes-da-Cunha and Junk, 2014), where abrupt changes between vegetation types allows units of different vegetation types to exist within close proximity to one another. Therefore these vegetation types are subject to the same variations and influences from floods, soil type, moisture and temperature, allowing the occurrence of spider assemblages with similar structure, due to the proximity with these habitats.
The occurrence of many grassed areas within the assessed mosaic landscape, especially murundus and pastures, is one of the factors responsible for the dominance of Lycosidae and Gnaphosidae in the assemblage composition. Weeks and Holtzer (2000) found these same families within habitats formed by this type of vegetation. The Lycosidae are cosmopolitan and vary greatly in size (Foelix, 1996); they are characterised as typical ground-dwelling spiders. Jocqué and Alderweireldt (2005) showed that Lycosidae co-evolved with the formation of grass/fields and dispersed concurrently with the expansion of this vegetation type, as evidenced by the high abundance of these spiders in open habitats with low vegetation, as well as low frequency in dense forests, agreeing with the results observed in this study, where a high abundance of these spiders was found in open habitats.
For Jocqué and Dippenaar-Schoeman (2007), Gnaphosidae behaviour is similar to the Lycosidae, occurring in a wide variety of habitats. The Gnaphosidae are engaged in nocturnal activity, and their foraging tactics resemble those used by Lycosidae (Weeks and Holtzer, 2000), facilitating colonisation of open areas such as fields and pastures (Jocqué and Dippenaar-Schoeman, 2007 select their microhabitats according to available moisture, litter and presence of herbaceous vegetation (Cady, 1984). Studies conducted in forested areas in the same region of the Pantanal showed lower activity and species richness of these families compared to pasture and murundu fields evaluated in this study, further demonstrating the interaction between these spiders with open vegetation areas (Castilho et al., 2005;Battirola et al., 2010). The total sampled species in our study conducted in a mosaic of vegetation formation is higher than species richness recorded in surveys conducted in monodominant forest in the same Pantanal region, such as areas with Attalea phalerata Mart. (Arecaceae) (Castilho et al., 2005;Marques et al., 2011) and Vochysia divergens Pohl. (Vochysiaceae) . This high species richness is probably related to the variation in vegetation types occurring in the study area. The Salticidae, Linyphiidae and Lycosidae families showed higher species richness in this study. In addition to the large representation of these families in numbers of species, it was possible to identify and make the first record of Aillutticus raizeri (Salticidae) in the northern region of the Pantanal of Mato Grosso. This species was previously recorded only in the Pantanal of Mato Grosso do Sul (Ruiz and Brescovit, 2006), and is possibly endemic to the Pantanal, since there are no records in any other regions of Brazil. Other Salticidae also recorded for the first time in this region were Freya chapare Galiano, 2001, previously known only to Bolívia and Goiás State (Brazil) (Galiano, 2001), and Tullgrenella guayapae Galiano, 1970, previously recorded only in Argentina (Platnick, 2014. Due to seasonal structural alterations in the system caused by flood pulse in flood-prone areas such as the Amazon and Pantanal, ground-dwelling species may behave differently in response to environmental conditions, such as by using of trunks and canopies in vertical migration behaviour, or in horizontal movement along the ground following the flood line (Adis, 1981(Adis, , 1997Höfer, 1997). These movements cause assemblages that occupy seasonally flooded areas to come into contact with those who occupy non-floodable habitats. Although this study was conducted in the Pantanal during the dry season, it is possible to infer that the murundu fields and forested areas mountain ranges act as places of refuge for edaphic organisms, since these areas are not directly affected by seasonal flooding (e. g. Nunes da Battirola et al., 2009;De Morais et al., 2013). This movement would allow the occurrence of species from both wetland habitats and non-floodable habitats in one place, increasing the similarity between assemblages, even in different habitats and seasonal periods.
In general, abundance, species richness and composition of ground-dwelling spider assemblages did not present differences between forested areas, pasture, and mu-rundu fields. However ground-dwelling spider assemblage showed relatively high species richness in the three analysed vegetation types and high similarity between them. In this study Lycosidae and Gnaphosidae dominance was associated with grassed areas, characterising this assemblage and indicating the importance of this kind of habitat in the region of the Pantanal to the maintenance requirement of the vegetational mosaic and for the conservation of Pantanal biodiversity.