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Zoologia (Curitiba)

Print version ISSN 1984-4670On-line version ISSN 1984-4689

Zoologia (Curitiba) vol.33 no.4 Curitiba  2016  Epub Sep 05, 2016

http://dx.doi.org/10.1590/S1984-4689zool-20150170 

ECOLOGY

Spider assemblage (Arachnida: Araneae) associated with canopies of Vochysia divergens (Vochysiaceae) in the northern region of the Brazilian Pantanal

Leandro D. Battirola1  * 

Daniel A. Batistella1 

Germano H. Rosado-Neto2 

Antonio D. Brescovit3 

Marinêz I. Marques4 

1Instituto de Ciências Naturais, Humanas e Sociais, Universidade Federal de Mato Grosso. Avenida Alexandre Ferronato 1200, Setor Industrial, 78557-267 Sinop, MT, Brazil.

2Departamento de Zoologia, Universidade Federal do Paraná. Caixa Postal 19020, 81531-980 Curitiba, PR, Brazil.

3Laboratório Especial de Coleções Zoológicas, Instituto Butantan. Avenida Vital Brasil 1500, Butantã, 05503-900 São Paulo, SP, Brazil.

4Instituto de Biociências, Universidade Federal de Mato Grosso. Avenida Fernando Corrêa da Costa 2367, Boa Esperança, 78060-900 Cuiabá, MT, Brazil.

ABSTRACT

This study describes the composition and temporal variation of the spider assemblage (Arachnida: Araneae) associated with canopies of Vochysia divergens Pohl. (Vochysiaceae) in the northern region of the Brazilian Pantanal. Three V. divergens plants were sampled in 2004, at each seasonal period of the northern Pantanal (high water, receding water, dry season and rising water), using thermonebulization of the canopies with insecticide, totaling 396 m2 of sampled canopies. Analysis of abundance and richness of spider families were based on Non-Metric Multidimensional Scaling (NMDS) and Variance Analysis (ANOVA and MANOVA). A total of 7,193 spiders were collected (6,330 immatures; 88.0%; 863 adults, 12.0%) distributed in 30 families. Araneidae (1,676 individuals), Anyphaenidae (1,631 individuals), Salticidae (1,542 individuals) and Pisauridae (906 individuals), were predominant, representing 80.0% of the sample. Ten different guilds were registered: aerial hunters, orb-weavers, nocturnal aerial runners and diurnal space web weavers dominated, sharing most ecological niches. The spider assemblage is affected by changes in the habitat structure, especially by the seasonal hydrological regime and variations in the phenology of V. divergens . The assemblage is composed of different groups of spiders. The dominant taxa and behavioral guilds differ in the different seasonal periods. Spiders were more abundant during the dry and rising water seasons, most likely reflecting a greater supply of potential prey, associated with new foliage and flowering at the canopy. The displacement of soil dwelling spiders to the trunks and canopies before and during the seasonal floods can change the structure and composition of the canopy assemblages. Oonopidae, Gnaphosidae and Caponiidae, were more frequent during the rising and high water seasons, which indicates that these taxa use the canopies of V. divergens as a refuge during the seasonal flooding in the Pantanal.

KEY WORDS: Invertebrates; diversity; forest canopy; seasonality; wetlands

Arthropod communities associated with canopies of typical vegetation formations of the northern region of the Pantanal have been studied in recent years (e.g., Marques et al. 2001, 2006, Battirola et al. 2005, 2007, 2014). Spiders, considered the main predators of arthropods in most biomes (Cardoso et al. 2011), are mentioned in these studies as being important components of these communities, with specific assemblages on each host plant (Santos et al. 2003, Battirola et al. 2004, Marques et al. 2007, 2011).

The different composition of spider assemblages most likely reflects the complexity of habitats in the Pantanal. The geological and geomorphological history of this biome, together with its position on the banks of large phytogeographic domains (Nunes-da-Cunha & Junk 1999, 2014), associated with water seasonality (Junk et al. 1989), results in a variety of landscapes, vegetation types (including monodominant forests) and habitats with specific characteristics (Silva et al. 2000, Nunes-da-Cunha & Junk 2011). The annual and multi-annual variations in the flood pulse affect the biota at different intensities and time scales (Nunes-da-Cunha & Junk 2004), causing terrestrial organisms to develop specific strategies to survive and adapt to the strong seasonality of this floodplain (Adis et al. 2001, Battirola et al. 2009).

Among the monodominant vegetation types in the northern region of the Pantanal of Mato Grosso, the "cambarazais" are outstanding (Silva et al. 2000). These are seasonally flooded forests with dominance of Vochysia divergens Pohl. (Vochysiaceae) (Arieira & Nunes-da-Cunha 2006). Vochysia divergens is considered invasive to native pastures, posing a problem for the local people, who rely on native grasslands for livestock (Pott & Pott 1994, Nunes-da-Cunha et al. 2000, Nunes-da-Cunha & Junk 2004). While V. divergens is characterized as a problem for landowners, it is ecologically important as a habitat and refuge for the wildlife (Pott & Pott 1994, Faßnacht 1998 , Marques et al. 2006), mainly when it is a fully grown tree (Nunes-da-Cunha & Junk 2014).

The distribution and species richness of predators like spiders may be influenced by the structural conditions of the host plants even though they do not generally have a direct relationship with these plants (Raizer & Amaral 2001, Souza & Martins 2004, 2005, Souza & Módena 2004), or by changes in environmental conditions (Wolda 1988). Spiders depend on plant structures to attach their webs and to forage. Plant phenology (flowering, fruit development and leaf fall periods), the distribution of food resources such as the presence of potential prey, often represented by herbivorous insects associated with that host, are also important to these arachnids (Costello & Daane 1995, Rinaldi & Forti 1997, Schaik et al. 1993, Arango et al. 2000).

Considering the importance of conservation and management of the specific monodominant forests of V. divergens in the Pantanal, as well as the biological diversity associated with these habitats, this study analyzed the composition and temporal variation of the spider assemblage in V. divergens canopies. Our goal was to evaluate the use of this habitat by spiders over different seasonal periods, in the northern region of the Pantanal of Mato Grosso, Brazil.

MATERIAL AND METHODS

The study area is located at the Retiro Novo Farm, Nossa Senhora do Livramento, Mato Grosso, Brazil. This area is situated on the right bank of the Cuiabá River and on the left bank of the Bento Gomes River, Pantanal of Poconé (16°15'24"-17°54'32"S, 56°36'24"-57°56'23"W) (16°15'12"S, 56°22'12"W). We studied spiders in a monodominant forest of V. divergens , known as "cambará" whose association is denominated "cambarazal" (Nascimento & Nunes-da-Cunha 1989). The study area is subjected to a rainy season from October to April and to annual flooding of 0.6-1.5 m height, generally between December and March, with four seasonal periods defined as high water (January-March), receding water (April-June), dry season (July-September), and rising water (October-December) (Heckman 1998). Data on the phenology of V. divergens correspond to those presented by Nunes-da-Cunha et al. (2000) e Nunes-da-Cunha & Junk (2004).

Twelve specimens of V. divergens were nebulized using thermonebulization of the canopies, three individuals in each seasonal period (high water, receding water, dry season and rising water in 2004). The sampled trees were selected according to the criteria proposed by Adis et al. (1998), and the methodological procedures according to Battirola et al. (2004). The entire diameter at the base of these trees was surrounded by nylon funnels (1 m in diameter each), distributed according to the shape and architecture of the canopy, bringing to a total of 396 m2 of assessed canopies (33 m2 per tree sampled). These collector funnels had a plastic collection bottle (1 L) at their base with 92% ethanol and were suspended at about 1 m from the ground by strings tied to surrounding trees. During the high water period the funnels were suspended at 2.5 m above the ground due to flooding of the forest (water depth ranging from 0.9 to 1.25 m). The nebulization was applied for 10 minutes using a Swingfog SN50 thermonebulizator, employing the non-residual synthetic pyrethroid (Lambdacialotrina at 0.5% - Icon(r)), diluted in diesel oil at a concentration of 1%, associated with the synergistic (DDVP 0.1%). This nebulization was performed at around 6:00 am, during less intense air circulation, which allows the cloud of insecticide to slowly rise through the canopy, without dispersion (Adis et al. 1998).

The collected material was transported to the Laboratório de Ecologia e Taxonomia de Artrópodes (LETA) at the Instituto de Biociências, Universidade Federal de Mato Grosso in Cuiabá, MT, and subsequently forwarded for identification to the Laboratório Especial de Coleções Zoológicas, Instituto Butantan, São Paulo, SP, where it is deposited. The behavioral guilds were determined according to Höfer & Brescovit (2001) and Dias et al. (2010).

Data from the spider assemblage were analyzed using the ordination method by Non-Metric Multidimensional Scaling (NMDS) for the abundance and presence-absence (qualitative) of families (adults + immatures), in order to reduce the dimensionality of information from multiple taxa (Clarke 1993). The dissimilarity between the sampling units was calculated using the associative matrix by means of the Bray-Curtis and Sørensen Index. Multivariate Analysis of Variance (MANOVA) was employed using the scores of NMDS dimensions with data of abundance and presence-absence, and Analysis of Variance (ANOVA) using a NMDS axes for presence-absence, associated with the a posteriori Tukey test. These analyses test the existence of average differences in the composition of the spider assemblage using categorical variables (high water, receding water, dry season and rising water). They were carried out using the free software R 2.12.1 (R Core Team 2013), Vegan package (Oksanen et al. 2014).

RESULTS

In 396 m2 of V. divergens canopies, 7,193 spiders from 30 families were sampled (18.2 ind./m2). Of this total, 6,330 individuals are immatures (88.0%, 16.0 ind./m2) and 863 adults (12.0%, 2.2 ind./m2). Araneidae (1,676 ind., 4.2 ind./m2), Anyphaenidae (1,631 ind., 4.1 ind./m2), Salticidae (1,542 ind., 3.9 ind./m2) and Pisauridae (906 ind., 2.3 ind./m2) were the most abundant families, representing 80% of the sample (Tables 1 and 2). Amaurobiidae, Ctenidae, Mimetidae, Prodidomidae, Sparassidae and Trechaleidae present only immature individuals (Table 1).

Table 1 Total abundance (number of individuals) of males, females and immatures of spiders sampled throughout the different seasonal periods in canopies of Vochysia divergens in the northern region of the Pantanal of Mato Grosso, Brazil. 

Families Adults Immatures
Males Females
Araneidae 41 87 1,548
Anyphaenidae 61 75 1,495
Salticidae 107 142 1,293
Pisauridae - - 906
Dictynidae 30 67 161
Theridiidae 9 14 241
Thomisidae 30 10 186
Oonopidae 60 39 23
Corinnidae 14 12 76
Gallieniellidae 6 10 79
Gnaphosidae 8 - 50
Titanoecidae 1 3 43
Sparassidae - - 37
Oxyopidae 1 - 27
Linyphiidae 5 5 15
Philodromidae 9 4 6
Mimetidae - - 14
Hersiliidae 2 - 6
Tetragnathidae 3 - 4
Selenopidae - 1 3
Trechaleidae - - 4
Caponiidae - 1 2
Ctenidae - - 2
Pholcidae - 1 1
Prodidomidae - - 2
Senoculidae 1 - 1
Theridiosomatidae 1 - 1
Amaurobiidae - - 1
Mysmenidae 1 - -
Uloboridae 1 - -
Indeterminated families - - 84
Total 391 472 6,330

Within the seasonal periods, receding water (2,398 ind., 33.3%, 24.2 ind./m2) and dry season (2,101 ind., 29.2%, 21.2 ind./m2) were the periods with most abundant assemblages of spiders, followed by rising water (1,663 ind., 23.1%, 16.8 ind./m2) and high water (1,031 ind., 14.3%, 10.4 ind./m2) (Table 2, Fig. 1). The coefficient of variance for the abundance of the family Araneae was 89.1% captured by ordering with two dimensions (stress 0.09), indicating that the assemblages in V. divergens canopies vary significantly throughout the seasonal periods (MANOVA: Pillai Trace = 1.27, F3,8 = 4.67, p < 0.01) (Fig. 2).

Figures 1-2 (1) Abundance of spiders and (2) ordination of assemblages of spiders in canopies of Vochysia divergens throughout the different seasonal periods in the northern region of the Pantanal of Mato Grosso, Brazil, based on a Bray-Curtis dissimilarity matrix (two axes, stress = 0.09). 

Table 2 Abundance (number of individuals), mean ± standard deviation of abundance, frequency (%) and behavioral guilds of spiders sampled in canopies of Vochysia divergens throughout the different seasonal periods in the northern region of the Pantanal of Mato Grosso, Brazil. (AH) Aerial hunters, (DAA) diurnal aerial ambushers, (DSWW) diurnal space web weavers, (GR) ground runners, (GW) ground weavers, (NAA) nocturnal aerial ambushers, (NAR) nocturnal aerial runners, (NGH) nocturnal hunters ground, (NGR) nocturnal ground runners, (OW) orb weavers. 

Taxa Seasonal periods Total Mean ± SD Frequency (%) Behavioral guild
High water Receding water Dry season Rising water
Amaurobiidae
Amaurobiidae indeterminated - 1 - - 1 0.2 ± 0.5 25 NAA
Anyphaenidae
Jessica erythrostoma (Mello-Leitão, 1939) - 4 - 4 1.0 ± 2.1 25 AH
Jessica sp. - 7 - - 7 1.7 ± 3.7 25 AH
Teudis sp. - 2 - - 2 0.5 ± 1.1 25 AH
Anyphaenidae sp. 1 12 5 - 2 19 4.7 ± 10.1 75 AH
Anyphaenidae sp. 2 7 2 - 1 10 2.5 ± 5.3 75 AH
Anyphaenidae indeterminated 179 299 596 515 1,589 397.2 ± 842.7 100 AH
Total Anyphaenidae 198 319 596 518 1,631 407.7 ± 864.9 100 AH
Araneidae
Alpaida bicornuta (Taczanowski, 1878) - 5 - - 5 1.2 ± 2.6 25 OW
Alpaida sp. - 1 - - 1 0.2 ± 0.5 25 OW
Araneus sp. - 2 - - 2 0.5 ± 1.1 25 OW
Cyclosa sp. - 1 - - 1 0.2 ± 0.5 25 OW
Eustala sp. - 7 - - 7 1.7 ± 3.7 25 OW
Hypognatha sp. - 1 - - 1 0.2 ± 0.5 25 OW
Manogea sp. - 1 - - 1 0.2 ± 0.5 25 OW
Metazygia gregalis (O.P. Cambridge, 1889) - 2 - - 2 0.5 ± 1.1 25 OW
Metazygia sp. - 7 - - 7 1.7 ± 3.7 25 OW
Araneidae sp. 1 9 25 - 4 38 9.5 ± 20.1 75 OW
Araneidae sp. 2 3 4 - 1 8 2.0 ± 4.2 75 OW
Araneidae sp. 3 - 1 - - 1 0.2 ± 0.5 25 OW
Araneidae indeterminated 256 710 263 373 1,602 400.5 ± 849.6 100 OW
Total Araneidae 268 767 263 378 1,676 419.0 ± 888.8 100 OW
Caponiidae
Caponiidae Indeterminated 3 - - - 3 0.7 ± 1.6 25 NGH
Corinnidae
Castianeira sp. - 1 - - 1 0.2 ± 0.5 25 AH
Corinnidae indeterminated 48 26 15 12 101 25.2 ± 54.1 100 AH
Total Corinnidae 48 27 15 12 102 25.5 ± 54.1 100 AH
Ctenidae
Ctenidae indeterminated - 2 - - 2 0.5 ± 1.1 25 NAA
Dictynidae
Dictyna sp. - 12 - - 12 3.0 ± 6.4 25 DSWW
Dictynidae sp. 1 - - - 1 1 0.2 ± 0.5 25 DSWW
Dictynidae sp. 2 - - - 1 1 0.2 ± 0.5 25 DSWW
Dictynidae indeterminated 15 89 123 37 264 66.0 ± 140.0 100 DSWW
Total Dictynidae 15 101 123 39 278 69.5 ± 147.4 100 DSWW
Gallieniellidae
Galianoella leucostigma (Mello-Leitão, 1941) 9 2 - 5 16 4.0 ± 8.5 75 NAR
Gallieniellidae indeterminated 16 22 38 3 79 19.7 ± 41.9 100 NAR
Total Gallieniellidae 25 24 38 8 95 23.7 ± 50.4 100 NAR
Gnaphosidae
Gnaphosidae Indeterminated 0 6 23 29 58 14.5 ± 30.7 75 GR
Hersiliidae
Hersiliidae indeterminated 3 3 - 2 8 2.0 ± 4.2 75 NAA
Linyphiidae
Sphecozone sp. - 2 - - 2 0.5 ± 1.1 25 DSWW
Linyphiidae indeterminated 17 5 - 1 23 5.7 ± 12.2 75 DSWW
Total Linyphiidae 17 7 - 1 25 6.2 ± 13.2 75 DSWW
Mimetidae
Mimetidae indeterminated - 1 9 4 14 3.5 ± 7.4 75 NAR
Mysmenidae
Mysmenidae indeterminated - 1 - - 1 0.2 ± 0.5 25 OW
Oonopidae
Gamasomorphinae sp. - 6 - - 6 1.5 ± 3.2 25 NGR
Oonopidae sp. 1 - - - 1 1 0.2 ± 0.5 25 NGR
Oonopidae sp. 2 - - - 2 2 0.5 ± 1.1 25 NGR
Oonopidae indeterminated 20 14 8 71 113 28.2 ± 59.9 100 NGR
Total Oonopidae 20 20 8 74 122 30.5 ± 64.7 100 NGR
Oxyopidae
Oxyopidae indeterminated 16 5 5 2 28 7.0 ± 14.8 100 AH
Philodromidae
Gephyrellula sp. - - - 2 2 0.5 ± 1.1 25 DAA
Philodromidae indeterminated - - 10 7 17 4.2 ± 9.0 50 DAA
Total Philodromidae - - 10 9 19 4.7 ± 10.1 50 DAA
Pholcidae
Pholcidae indeterminated 1 - - 1 2 0.5 ± 1.1 25 DSWW
Prodidomidae
Prodidomidae indeterminated - - - 2 2 0.5 ± 1.1 25 GR
Pisauridae
Pisauridae indeterminated 102 477 277 50 906 226.5 ± 480.5 100 DSWW
Salticidae
Bellota sp. - 1 - - 1 0.2 ± 0.5 25 NAR
Helvetia sp. - 1 - - 1 0.2 ± 0.5 25 NAR
Salticidae sp. 1 7 14 29 11 61 15.2 ± 32.3 100 NAR
Salticidae sp. 2 2 8 7 5 22 5.5 ± 11.7 100 NAR
Salticidae sp. 3 1 - - - 1 0.2 ± 0.5 25 NAR
Salticidae Indeterminated 169 400 554 333 1,456 364.0 ± 772.2 100 NAR
Total Salticidae 179 424 590 349 1,542 385.5 ± 817.7 100 NAR
Selenopidae
Selenopidae indeterminated 4 - - - 4 1.0 ± 2.1 25 NAA
Senoculidae NAA
Senoculus sp. - 1 - - 1 0.2 ± 0.5 25 NAA
Senoculidae indeterminated - 1 - - 1 0.2 ± 0.5 25 NAA
Total Senoculidae - 2 - - 2 0.5 ± 1.1 25 NAA
Sparassidae
Sparassidae indeterminated 2 18 3 14 37 9.2 ± 19.6 100 NAA
Tetragnathidae
Tetragnathidae indeterminated 1 5 1 - 7 1.7 ± 3.7 75 OW
Theridiidae
Anelosimus sp. - 1 - - 1 0.2 ± 0.5 25 DSWW
Argyrodes sp. - 2 - - 2 0.5 ± 1.1 25 DSWW
Theridion sp. - 1 - - 1 0.2 ± 0.5 25 DSWW
Theridiidae sp. 1 2 1 - - 3 0.7 ± 1.6 50 DSWW
Theridiidae sp. 2 1 1 - - 2 0.5 ± 1.1 50 DSWW
Theridiidae indeterminated 91 91 24 49 255 63.7 ± 135.2 100 DSWW
Total Theridiidae 94 97 24 49 264 66.0 ± 140.0 100 DSWW
Theridiosomatidae
Theridiosomatidae indeterminated
Thomisidae - 2 - - 2 0.5 ± 1.1 25 OW
Tmarus sp. - 1 - - 1 0.2 ± 0.5 25 DAA
Tobias sp. - 3 - - 3 0.7 ± 1.6 25 DAA
Thomisidae sp. 1 - - 1 - 1 0.2 ± 0.5 25 DAA
Thomisidae sp. 2 - - 1 - 1 0.2 ± 0.5 25 DAA
Thomisidae indeterminated 20 34 82 84 220 55.0 ± 116.7 100 DAA
Total Thomisidae 20 38 84 84 226 56.5 ± 119.8 100 DAA
Titanoecidae
Titanoecidae indeterminated 1 - 32 14 47 11.7 ± 24.9 75 GW
Trechaleidae
Trechaleidae indeterminated - 4 - - 4 1.0 ± 2.1 25 NAA
Uloboridae
Uloboridae indeterminated - 1 - - 1 0.2 ± 0.5 25 OW
Indeterminated Families 14 46 - 24 84
Total 1,031 2,398 2,101 1,663 7,193

Little variation was observed in the dominant groups in each seasonal period evaluated. Araneidae, Anyphaenidae, Salticidae and Pisauridae predominated in all periods evaluated, accompanied by Theridiidae (high water), Dictynidae (receding water and dry season), and Thomisidae (rising water). Individuals of some families were recorded exclusively in only one of the seasonal periods. Selenopidae and Caponiidae were sampled only during the high water season, and Prodidomidae in the rising water. During receding water, a period with the highest abundance of spiders in V. divergens canopies, the unique occurrence of Amaurobiidae, Ctenidae, Mysmenidae, Senoculidae, Theridiosomatidae, Trechaleidae and Uloboridae was observed (Table 2). The presence-absence data for families per season, show that the coefficient of variance captured by ordering with a NMDS axis was 61.2% (stress 0.27), indicating that the number of families varied significantly between seasons (ANOVA: F3.8 = 8.29, p < 0.01); differences were significant both for rising and high water (Tukey, p = 0.02), rising and receding water (Tukey, p = 0.02), respectively (Fig. 3).

Figure 3 Variation in the number of spider families based on the Sorensen index in canopies of Vochysia divergens throughout the different seasonal periods in the northern region of the Pantanal of Mato Grosso, Brazil. 

Ten behavioral guilds were found in V. divergens canopies (Table 2). Aerial hunters (1,761 ind.), orb weavers (1,687 ind.), nocturnal aerial runners (1,651 ind.) and diurnal space web weavers (1,475 ind.) predominated. Both diurnal and nocturnal aerial ambushers were represented with only 245 and 60 individuals, respectively. The guilds varied in relation to seasonal periods (ANOVA: F9.30 = 9.17, p < 0.01). Orb weavers and aerial hunters predominated over all periods, accompanied by diurnal space web weavers and nocturnal aerial runners.

A considerably differentiated pattern was observed for the clusters of soil dwelling spiders that were represented by nocturnal ground runners (122 ind.), ground runners (60 ind.), ground weavers (47 ind.) and nocturnal ground hunters (3 ind.). Ground runners (Gnaphosidae and Prodidomidae) and nocturnal ground runners (Oonopidae) were more frequent during the rising water season. Caponiidae (nocturnal ground hunters) were only sampled during the high water, while Titanoecidae (ground weavers), although they occurred during rising water and in high water season, were more abundant in the dry period (Table 2).

DISCUSSION

Variation was observed in the composition and structure of the spider assemblage in the canopies of V. divergens , with spiders groups varying throughout the seasonal periods, with significant abundance during periods of receding water and dry season, as well as the restricted occurrence of taxa in some periods. Many of these variations can be associated with habitat conditions, considering that the habitat structure is a fundamental requisite for the organization of spider assemblages (Cardoso et al. 2011).

In canopies of V. divergens , the phenology of the plant and the hydrological seasonality of the Pantanal are the two main factors in the structuring of this habitat. Due to the pronounced water seasonality in the Pantanal ecosystem, many species have developed morphological, physiological and phenological adaptations, e.g. synchronizing their stages of development to the specific seasonal periods of the region. The phenology of V. divergens is associated with seasonal flooding with renewal of foliage and flowering occurring during the receding water and dry season, respectively (Nunes-da-Cunha & Junk 2004). These periods correspond to those with more frequent occurrence of spiders associated with their canopies. This fluctuation probably reflects the greater supply of potential prey, caused by changes in canopy structure, e.g., the advent of new foliage and flowering which increase the availability of resources for herbivorous species that may be potential prey for spiders (e.g., Marques et al. 2006). The change in the canopy structure of V. divergens expands the area that can be used by spiders (immatures and adults) for fixing their webs, as well as foraging and refuge areas, mainly for immatures, representing the majority of the assemblage.

The spider assemblage in V. divergens canopies is indirectly influenced by water seasonality: 1) by its direct influence on the phenology of the host plants and 2) by inciting the displacement of soil organisms to the trunks and canopies before and during the seasonal floods. The seasonal fluctuation of taxa such as Oonopidae, Gnaphosidae and Caponiidae in V. divergens canopies shows this behavior, indicating that soil spiders move to higher layers of the habitats such as trunks and canopies, to survive during the flood periods, which was observed in ants and millipedes in the same region (Adis et al. 2001, Battirola et al. 2009).

Similarly, Adis (1981, 1992) sustained that migration from the ground to the forest canopy in the Central Amazon begins during the rising water period, already ten to eight weeks prior to forest inundation. Battirola et al. (2010) reported, for the same forest in the Pantanal, that activity density of ground dwelling spiders is higher in periods of rising water and high water than in the other periods, especially for Oonopidae and Gnaphosidae. The greater movement of spiders coincides with the flooding, which forces these arachnids and other invertebrates to move continuously, seeking refuge, in a similar manner as recorded at the Central Amazon (Adis 1981, 1997).

The dominance of four spider families in V. divergens canopies is most likely due to niche sharing and the smaller niche overlap of these spiders, since they represent a distinct behavioral guild. Differences between the dimensions of the ecological niches may reduce competition and facilitate the coexistence of species (Schoener 1974, Gilbert et al. 2008). Araneidae (orb weavers) and Pisauridae (diurnal space web weavers) represented the weavers and Anyphaenidae (aerial hunters) and Salticidae (nocturnal aerial runners) the hunters. The most important prey for spiders are arthropods. However, competition may be reduced by adopting diverse foraging methods, such as type of prey, circadian rhythm (day and night), vertical stratification (soil and canopy), and also as a result of the size of body and phenology of species (Cardoso et al. 2011). The use of different strategies to obtain resources reduces the competition between species, and allows their coexistence (Moran & Southwood 1982, Pianka 1994, Blondel 2003, Wilson 1999).

The assemblages of spiders in habitats with similar structures may be composed of different species, but have similar guild composition (Cardoso et al. 2011). This was verified in studies of spider assemblages in canopies in areas of monodominant vegetation in the northern region of the Pantanal of Mato Grosso (Santos et al. 2003, Battirola et al. 2004, Castilho et al. 2005, Marques et al. 2007). Similar dominant groups to those found in V. divergens canopies (e.g., Salticidae, Anyphaenidae, Araneidae, Corinnidae and Pisauridae), were obtained in the canopies of Calophyllum brasiliense Cambess (Gutiferae) (Marques et al. 2007). In the canopies of Attalea phalerata Mart. (Arecaceae), Salticidae, Araneidae, Oonopidae, Ctenidae and Dictynidae predominated when the water level was high (Battirola et al. 2004), and Salticidae, Gnaphosidae, Araneidae and Oonopidae during the dry season (Santos et al. 2003). Anyphaenidae and Pisauridae, which are typical of V. divergens canopies, occurred with low density on A. phalerata . One of the factors that may contribute to the different assemblages on these two host plants is the different architecture of their canopies (e.g., Farrel & Erwin 1988), which influences the presence of important microhabitats (Battirola et al. 2007, Marques et al. 2009), e.g., sites for foraging and fixing webs, presence of prey and microclimate.

The assemblage of spiders associated with V. divergens canopies is seasonally affected by variations in habitat structure, especially by the hydrological regime and by the phenology of their host plant, and it is composed of different groups of spiders with a clear distinction between behavioral guilds. Due to the flooding of the forest, the canopies are regarded as a refuge for soil dwelling spiders during rising water and high water periods.

ACKNOWLEDGEMENTS

We dedicate this work to Prof. Joachim Adis (in memoriam ) for his extensive studies of arthropods in the floodplains of the Pantanal and for his important contribution to this study. This study is in part due to scientific collaboration between the Max-Planck Institute for Limnology, Plön, Germany and the Federal University of Mato Grosso, Cuiabá, Brazil. We thank the Post-Graduate Program in Biological Sciences (Entomology), Federal University of Paraná, and the Post-Graduate Program in Ecology and Biodiversity Conservation, Institute of Biosciences UFMT for the infrastructure available for the development of this research and FAPEMAT (Fundação de Amparo à Pesquisa do Estado de Mato Grosso, Process 155864/2015). A.D. Brescovit is supported by a research grant 301776/2004-0 from CNPq.

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Received: October 17, 2015; Revised: April 03, 2016; Accepted: May 08, 2016

*Corresponding author. E-mail: ldbattirola@uol.com.br

Author Contributions:

LDB, GHRN and MIM designed the experiments; LDB and MIM conducted the experiments; LDB, DAB and ADB analyzed the data; LDB, DAB, GHRN, ADB and MIM wrote the paper.

Competing Interests:

The authors have declared that no competing interests exist.

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