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Soil fauna changes across Atlantic Forest succession

The soil fauna can be used as a bioindicator of soil quality and ecosystem functioning. The present study aimed to assess the effect of the Atlantic Forest secondary succession on the structure and composition of the soil fauna community in Itaboraí, Rio de Janeiro. We selected five areas along a gradient of forest succession: pasture (PA) and four forest fragments (FF1, FF2, FF3, FF4), which are in a toposequence. Thus, we divided the areas in upper, middle and lower thirds and delimitated a transect (20 m) in each third. In the dry season 2010, a metalic square (0.25 m x 0.25 m) was released in five points spaced 5 m apart, in each transect. The soil fauna was manually captured on samples of the litter standing stock and blocks of the topsoil (0.000.10 m), circumscribed to the square, in the forest fragments. In PA, we colected only the topsoil blocks. The complexity of the structure and composition of the soil fauna community increased in the topsoil and litter standing stock, along the successional gradient. However, the similarity among the areas was much greater in the litter standing stock, in comparison to the topsoil.


Introduction
The Atlantic Forest is known internationally because of its high levels of richness and endemism of plant species (Murray-Smith et al., 2009). However, currently, there are only a few small and isolated forest fragments of this biome, which are in different stages of secondary succession (Ribeiro et al., 2009). Thus, several species have become endangered due to the loss and fragmentation of habitat (Biodiversitas, 2016), and studies focused on ecosystem functioning, structure, and composition of animal and plant communities may contribute to the recovery and preservation of the forest remnants.
The structure and species composition of the plant communities change along the forest succession (Marín-Spiotta et al., 2007;Menezes et al., 2009), as the microclimate conditions change (Negrete-Yankelevich et al., 2007). As a result, ecosystem functioning so as litterfall, litter standing stock and decomposition also change, during the forest development (Ostertag et al., 2008;Pinto et al., 2008;Mateus et al., 2013). In terms of litter decomposition, the role of the soil fauna is prominent (Mayer, 2008).
The soil fauna community responds to variations within the forest succession (Younger et al., 2005;Negrete-Yankelevich et al., 2007;Menezes et al. 2009;Camara et al., 2012;Rousseau et al., 2014;Machado et al., Com. Sci., Bom Jesus, v.9, n.2, p.162-174, Apr./Jun. 2018 2015). Therefore, the soil fauna may function as a bioindicator of soil quality and ecosystem functioning along this process. If negative impact is observed in the community of such organisms, the human intervention is needed to facilitate the forest succession. However, it is necessary to conduct more studies with this approach, to identify consistent patterns of the response of the soil organisms to different stages of the forest succession (Sylvain & Wall, 2011).
The present study aimed to assess the effect of the Atlantic Forest secondary succession on the structure and composition of the soil fauna community in Itaboraí, Rio de Janeiro.

Material e methods
The study area is located between latitudes 22º 40' 30 "S and 22º 38 '42" S, and longitudes 42 48'.54 "W and 42 47' 42" W, in the municipality of Itaboraí, state of Rio de Janeiro.
The area is at an altitude of 27 m . According Köppen (1948), the climate is tropical Aw, that is, with rainy summers and dry winters. The annual average temperature is 21.4 °C and higher values occur from January to March, while the smaller from June to August, according to   (Figura 1). This author also pointed that the total annual rainfall is 1,461 mm, the rainiest months are December and January, while June and July are the months with less precipitation. The predominant soil type in the region is Oxisoil (Gomes et al., 2014).
Most of the original vegetation of the region, which is Dense Ombrophilous Forest of lowland and lower montane (Veloso et al., 1991), was eliminated primarily for installation of pastures and crops, as well as logging and extraction of sand and clay. Thus, the matrix area corresponds to abandoned pastures, among which are observed some small fragments of secondary forest (<5 ha) on the top of the slopes. For the present study, we selected an abandoned pasture area (PA) and four forest fragments, which are in an increasing gradient of natural regeneration: FF1, FF2, FF3 and FF4 (Uhlmann et al., 2014). The forest fragments vary in size: FF3 presents the higher area (21 ha), followed by FF1 (10 ha), FF2 (7,5 ha), and FF4 (3 ha) (Scoriza, 2012). According to Uhlmann et al. (2014) Biological and Fertility program (TSBF), described by Anderson and Ingram (1993). In PA, only the topsoil blocks were collected. Thus, we obtained a total of 15 samples of the litter standing stock and blocks of the topsoil in each forest fragment, and 15 samples of the topsoil in PA. Each sample was considered an experimental unit.
The samples were individually packed in plastic bags previously identified. In the field, these materials were transferred into a tray where the organisms were manually extracted, with the aid of tweezers. The organisms were individually stored in vials with 70% alcohol. Subsequently, in the laboratory, the organisms were identified by naked or under binocular magnifying lens, if necessary, and quantified in large taxonomic groups (order, class, family). Formicidae and Enchytraeidae were both considered a taxon apart of Hymenoptera and Oligochaeta, respectively. The adults were separated from juvenile forms (pupa) and larval forms even when they belonged to the same taxonomic group, due to the differences between these vital stages in terms of their ecological role in the soil environment (Odum, 1988). Taxonomic groups were further categorized according to their trophic guilds (Menezes et al., 2009;Camara et al., 2012;Silva et al., 2013;Rousseau et al., 2014). Thus, some of them were categorized in: predators, saprophagous, and herbivorous (Table 2). In contrast, some taxonomic groups included edaphic organisms with belonged to more than one trophic guild. In these cases, they were categorized as: predators/saprophagous, saprophagous/herbivorous, or saprophagous/ microphagous.
We estimated the values of the structural attributes of the soil community: total density (D) and density of the taxonomic groups (m -2 individuals), total richness or number of the taxonomic groups (S), equability (U, Pielou index) and diversity (H', Shannon index) (Odum, 1988).
The community composition was evaluated according to the following criteria: absence/ presence of the taxonomic groups; relative contribution (%) of the taxonomic groups; density of the taxonomic groups; density of the trophic guilds. The relative contribution was calculated as the ratio between the density of each group and the density of the community. The taxonomic groups with a low relative contribution (< 1%) in both litter standing stock and topsoil, were reunited as the group "Other".
The mean values of abundance According to this author, leaves predominated in the litter standing stock (47,5% of the total) at the forest fragments. Both of these multivariate analyses were performed by PAST software, version 2.17c (Hammer et al., 2001).

Results and Discussion
The effect of the Atlantic Forest succession on the structure of the soil fauna community We extracted a total of 8,173 organisms which were distributed in 34 taxonomic groups.
All of these groups occurred in at least one of the forest fragments. In the topsoil, the number  Table 1. Structural attributes of the soil fauna community structure within litter standing stock and topsoil in the upper, middle and lower thirds (UT, MT and LT, respectively) at a pasture area (PA) and four forest fragments in an increasing gradient of natural regeneration (FF1, FF2, FF3, and FF4), Itaboraí, RJ*.
As the successional gradient progresses, the plant community undergoes an increasing in its structure (Marín-Spiotta et al., 2007), which is reflected in an increased litterfall (Pinto et al., 2008) and, consequently, in largest litter standing stock (Mateus et al., 2013). Such conditions, combined with a more closed canopy in forests with more advanced sucessional stage (Menezes et al., 2009)    Pseudoscorpionida and Diplura were both absent in a pasture area, but they occurred in forest fragments in four and three different stages of succession, respectively, in the Brazilian Amazon (Rousseau et al., 2014). Archaeognatha, Diplura, and Thysanura were restricted to a preserved native forest, and they were not found in two abandoned eucalyptus plantations with different stages of natural regeneration of Atlantic Forest (Camara et al., 2012).
According to Camara et al. (2012), the relative contribution of Entomobryomorpha increased from 5% to 30% in the dry season and from 8% to 65% in the rainy season, According to the average of all of the forest fragments, most of the individuals (> 50%) that belonged to 29 taxonomic groups were extracted from the litter standing stock (Figure 3). Oligochaeta's cocoons (Figure 3). The latter group refers to the egg stage of Oligochaeta, which do not feed, and therefore do not belong     (Camara et al., 2012), and in areas within less advanced stages of succession, in the Brazilian Amazon (Morais et al., 2010). These guilds are sensitive to human impacts, which can decrease the primary resources for the trophic chains (Negrete-Yankelevich et al., 2007), and are important for the nutrient cycling (Correia & Andrade, 2008). Thus, taxonomic groups of the soil fauna that belong to the guilds of predators and saprophagous should be considered indicators of soil quality (Menezes et al., 2009).
The cluster analysis based on the average abundance of the soil fauna taxonomic groups within the topsoil showed the low similarity that all areas presented to each other ( Figure   4A). Thus, the complexity of both the structure and composition of the soil fauna community was lower in PA and FF1, but increased along the successional gradient ( Figure 4). In fact, the community in FF3 showed higher similarity to  The Figure 5 indicated that FF1 was more correlated by the C/N ratio of the leaf litter lying on the soil surface, which was significantly higher in this area in comparison to FF2, FF3, and FF4 (Scoriza, 2012). On the other hand, the concentrations of K and Mg were best correlated to FF3, due to the higher values of both leaf litter chemical attributes (Scoriza, 2012). These results agreed to Boeger et al. (2005), which observed that the concentrations of N and K are higher in leaves of tree species that occurs in areas with more advanced stage of Atlantic forest. Thus, the lower concentration of nitrogen, associated with the highest concentration of carbon, would result in the increase of C/N ration in leaves of the litter standing stock in FF1.
The increase of N and K concentrations in the leaves probable occurred as a consequence of the higher depth of the litter standing stock in advanced stages fo forest natural regeneration (Boeger et al., 2005). This patter was also verified in the areas studied, because the litter standing stock was significantly lower in FF1, in comparison to FF2, FF3, and FF4 (Scoriza, 2012). This is a reflection of the higher litterfall, which increases by the higher tree community structure, in more advanced stages of forest regeneration (Chazdon, 2012).
FF2 presented higher correlations to both equability and diversity in the topsoil, because of the higher values of these attributes, in comparison to the other forest fragments (Table   1). However, most of the structural attributes of the edaphic fauna within the topsoil (density and richness) and the litter standing stock (equability and diversity) presented higher correlation to the FF4. This pattern corroborated the fact that the complexity of the edaphic community increased as the natural regeneration of the Atlantic Forest advanced, in the area of study.

Conclusions
The complexity of the structure and composition of the edaphic fauna community increased in the topsoil and litter standing stock, along the successional gradient. However, the similarity among the areas was much greater in the litter standing stock, in comparison to the topsoil.