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1EDGE
EFFECT ON STRUCTURE AND COMPOSITION OF SOIL FAUNA IN
ATLANTIC FOREST, RJ, BRAZIL
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SUMMARY
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Forest fragmentation may influence soil fauna community. This work analyzed the
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structure and composition of soil fauna in different sizes of Atlantic Rain Forest fragments
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(SF: small fragment; MF: medium and LF: large), within four seasons, by means of stratified
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installation of pitfall traps. The organisms were identified as taxonomic groups (order,
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family). There were observed stronger effects of fragment size and seasonality on the
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composition of groups rather than on structure of the community. The smallest forest
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fragment showed higher total abundance; the intermediate fragment, the greatest uniformity
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and diversity; and the larger fragment, the greatest richness. The highest values of total
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abundance and richness occurred in rainy season, but no clear effects of seasonality on
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uniformity and diversity were identified.
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Index terms: biodiversity, forest fragmentation, soil organisms.
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RESUMO: EFEITO DE BORDA SOBRE A ESTRUTURA E COMPOSIÇÃO DA
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FAUNA DO SOLO EM MATA ATLÂNTICA, RJ, BRASIL
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A fragmentação florestal pode influenciar a comunidade da fauna do solo. Este
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trabalho analisou a estrutura e composição da fauna do solo em fragmentos de Mata
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Atlântica de diferentes tamanhos (FP: fragmento pequeno; FM: médio; FG: grande), nas
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quatro estações do ano, com a instalação estratificada de pitfall traps em parcelas. Os
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organismos foram identificados em grupos taxonômicos (ordem, família). O efeito do
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tamanho do fragmento e da estação climática sobre a fauna do solo foram mais
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importantes do ponto de vista da composição de grupos do que da estrutura da
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comunidade. O menor fragmento florestal apresentou maior abundância total; o
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fragmento intermediário, as maiores uniformidade e diversidade; e o maior fragmento, a
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maior riqueza. Os maiores valores de abundância total e riqueza da comunidade da fauna
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do solo ocorreram na estação chuvosa, mas não foram identificados efeitos claros da
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sazonalidade sobre a uniformidade e diversidade.
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Termos de indexação: biodiversidade, fragmentação florestal, organismos do solo.
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INTRODUÇÃO
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The original forest cover is removed in order to attend different land uses, thus
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converting landscape into a set of small forest fragments with different shapes and degrees
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of isolation and degradation (Didham et al., 1996). Edges are created around all these
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remnants, where solar radiation and winds are more intense, which results in increments of
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air and soil temperatures and decreases soil moisture, as compared with the interior of the
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forest fragments (Siqueira et al., 2004). This phenomenon is called edge effect and it is
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responsible for decreasing richness of the understory plants in Atlantic Rain Forest
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(Paciencia & Prado, 2004; Gomes et al., 2009) up to more than 50 m from the edge to the
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interior of the fragments (Fontoura et al., 2006). Edge effects in Atlantic Rain Forest is also
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responsible for high mortality of trees (Malchow et al., 2006) and the establishment of a
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tree community with a high density of small individuals predominantly composed of
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pioneer species (Bernacci et al., 2006; Carvalho et al., 2008) and deciduous species that
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shed their leaves to minimize water loss in dry season (Holanda et al., 2010).
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The limited information about nutrient cycling in Atlantic Rain Forest suggest that
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some aspects of this process may be changed by the edge effect. Litterfall may be lower at
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the edge of fragments due to the massive presence of smaller trees, in comparison to the
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fragments interior (Nascimento, 2005; Vidal et al., 2007). In other situations, there were no
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differences between the edge and the interior, in relation to the litterfall and thickness of
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the litter layer disposed on the soil surface (Portela & Santos, 2007) and input of nutrients
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through litterfall (Nascimento, 2005). Litter decomposition may be slower at the edge,
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where the community of soil fauna involved in the process had lower diversity and was
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represented mainly by microphages organisms compared to the interior, where
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predominated saprophagous-predators organisms (Pereira et al., 2013).
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When comparing Atlantic Rain Forest fragments with different sizes, there were no
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differences in the thickness of the litter layer, but litterfall was higher in the larger
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fragment (Portela & Santos, 2007). However, in another area was observed that highest
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litterfall occurred in the smallest fragment (Vidal et al., 2007), while in another area there
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were no difference among small, medium and large fragments in terms of litterfall and
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concentration and input of P, but concentrations and input of K and Mg were higher in
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intermediate fragment, while Ca were higher in the smaller fragment (Gomes et al., 2010).
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Understanding the edge effects on the soil fauna community is important as indication of
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biological diversity loss due to the forest fragmentation, which contributes to taking
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measures aimed at proper management of the remaining fragments (Didham et al., 1996;
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Davies & Margules, 1998). This study evaluated the structure and composition of the soil
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fauna community in forest fragments of different sizes and degrees of isolation in
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Teresópolis, Rio de Janeiro, Brazil.
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MATERIAL AND METHODS
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Study area
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This study was conducted in the rural municipality of Teresópolis (22º17'61 "S and
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42º52'58''W) in the State of Rio de Janeiro, Brazil. The climate is classified as hot and
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humid tropical, with average annual rainfall ranging between 1250 and 1500 mm
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(RadamBrasil, 1983). The region has a dry season (May-August) with average monthly
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rainfall of 100 mm, and a rainy season (September to April) with average monthly rainfall
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exceeding 200 mm, while the average monthly temperature of 19.5 °C shows little
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variation throughout the year (Gomes et al., 2010). The undulating relief has steep
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escarpments, the original vegetation is Montane Ombrophilous Dense Forest and the
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predominant class of soils is dystrophic Red-Yellow Podzolic (RadamBrasil, 1983), whose
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current classification is Red-Yellow Paleudult (Embrapa, 2006). Forest fragments of three
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different sizes, Small Forest Fragment (SP: approximately 3.2 ha), Medium Forest
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Fragment (MF: 23 ha) and Large Forest Fragment (LF: 62 ha), were selected. SF and LF
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are inserted into an environmental matrix formed by agricultural crops, pasture, or rocky
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outcrops and they are insolated to at least 500 m from other forest fragments. MF is
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connected to other forest fragments of less than 200 m of distance (Gomes et al., 2010).
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Sampling of the soil fauna community
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In each forest fragment were demarcated three plots (10 m x 100 m) located at a
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distance of 0-10 m (first parcel), 60-70 m (second parcel) and 160-170 m (third parcel), the
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from the edge. The soil fauna community was sampled by means of five pitfall traps
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distant 20 m apart from each other in each plot (N = 15 traps / forest fragment). The traps
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consisted of plastic containers (7 cm tall, 5 cm diameter) filled with 100 mL of
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acetylsalicylic acid 3 % solution and were buried in the soil with the opening close to the
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interface with the litter standing stock. This method allows sampling meso and macrofauna
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that participates directly in the fragmentation of litter and in the redistribution of the
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organic residues (Correia & Oliveira, 2000). The contents of the traps were stored in
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plastic vials with a solution of ethyl alcohol 70 % until the analysis.
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The traps remained in the field for a period of 10 consecutive days, and were
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installed in the seasons: spring (October/2004) and summer (December/2004),
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corresponding to the rainy season, autumn (April/2005) and winter (July/2005),
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corresponding to the dry season. This procedure aimed to evaluate the influence of the
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seasons on the structure and composition of the soil fauna community, as this was
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previously found in different studies (Corrêa Neto et al., 2001; Moço et al., 2005; Menezes
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et al., 2009; Silva et al., 2009; Calvi et al., 2010; Camara et al., 2012; Cunha Neto et al.,
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2012). The organisms were identified and quantified in taxonomic groups (order or family)
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(Moço et al., 2005; Souza et al., 2008; Menezes et al., 2009; Calvi et al., 2010; Camara et
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al., 2012; Cunha Neto et al., 2012; Pereira et al., 2013; Silva et al., 2013). Abundance
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(number of individuals trap-1 day-1), richness (R, total number of groups), evenness (U,
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Pielou index) and diversity (H', Shannon index) were calculated. The results obtained were
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subjected to analysis of variance. The averages for forest fragments and seasons were
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compared by Kruskal-Wallis non-parametric test at 5 % significance, with BioEstat
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statistical software version 5.3.
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RESULTS
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Edge effects on soil fauna community
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A total of 31708 individuals were sampled in Atlantic Rain Forest fragments, which
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corresponded to the total mean abundance of 214.8 individuals trap-1 day-1. The highest
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average abundance of soil fauna community occurred in FP (27.54), which was
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approximately 2 and 3 times higher than that observed in FG (16.15) and FM (10.00),
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respectively. According to the analysis by climate station, the highest values of total
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abundance were observed in FP and the lower in FM, while the intermediate values
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occurred in FG, that did not differ from the other fragments, in both rainy and dry seasons
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(Table 1).
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Table 1. Average total abundance and indix of richness, uniformity and diversity of soil fauna in
Atlantic Rain Forest fragments, in four climate seasons, Teresópolis, RJ
SF
Ab*
R
MF
U
H’
Ab*
R
LF
U
H’
Ab*
R
U
H’
Spring
30.19±3.38ABa 22 0.57 2.56 25.08±2.94Ba 19 0.58 2.47 47.85±12.75Aa 21 0.52 2.27
Summer
73.57±33.90Aa 18 0.16 0.67 12.16±1.18Aa 20 0.62 2.70
12.15±2.72Aa
21 0.52 2.30
Rainy season (spring and summer)
51.88±17.22Aa 23 0.36 1.62 18.62±1.96Ba 22 0.59 2.65 30.00±7.21ABa 24 0.50 2.28
Autumn
4.93±1.08Ab
14 0.45 1.72
1.60±0.21Bb
13 0.77 2.85
3.21±0.69ABb
17 0.64 2.60
1.39±0.23Ab
10 0.83 2.76
2.30±0.56ABb
17 0.67 2.76
Winter
1.47±0.23Ab
11 0.55 1.89
1.15±0.17Ab
10 0.75 2.50
Dry season (autumn and winter)
3.20±0.89Ab
14 0.48 1.81
1.38±0.20Bb
SF
27.54±9.11A
23 0.36 1.65
16 0.69 2.78
MF
10.00±1.49B
22 0.60 2.69
LF
16.15±4.01AB
24 0.51 2.35
*Average of 15 replicates. Values followed by different capital letters indicate significant differences
among forest fragments within the same season, according Kruskal-Wallis test at 5 %. Values followed
by lowercase letters indicate significant differences between climate seasons within the same forest
fragment, according Kruskal-Wallis test at 5 %. SF: small fragment; MF: medium fragment; LF: large
fragment. Ab: total abundance (individuals trap-1 day-1 ± standard error); R: richness; U: Pielou evenness
index; H': Shannon diversity index.
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Forest fragments presented almost the same average values of richness, with a
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tendency to higher values in LF (24), intermediate in SF (23) and lower in FM (22). This
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pattern was observed in the rainy season, but was slightly modified in the dry season,
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where the descending order of the fragments was: LF> MF> SF. In terms of the indexes of
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evenness and diversity, the highest mean values were observed in MF, followed by LF and
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SF. In general, this pattern was a reflection of the results obtained for the rainy and dry
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seasons (Table 1).
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A total of 26 groups of soil fauna were observed in the Atlantic Rain Forest
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fragments, eight of them (31 % of the total) presented restricted occurrence. Hymenoptera
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were not sampled in SF; Symphyla and Thysanoptera were not sampled in LF; Lepidoptera
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larvae, Scorpionida and Thysanura not occurred in MF; Chilopoda and Enchytraeidae were
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not sampled in FP and FM (Table 2).
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Formicidae and Collembola were the groups with the highest relative contribution
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in total abundance in SF and LF. But the values of their participation changed between
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those areas, since the relative contribution of Formicidae was almost two times higher SP
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(70 %) than in LF (45 %), and the opposite was observed for Collembola (SF: 12 %, LF:
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21 %). Collembola was the dominant group in MF (33 %), followed by Diptera and
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Formicidae, which showed virtually the same relative participation (20 % and 19 %,
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respectively). Significant influence of forest fragment size on the abundance of taxonomic
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groups only occurred for Formicidae and Heteroptera, whose values decreased, and for
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Coleoptera and Orthoptera, which increased, as increased the size of the fragments (Table
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2).
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Effects of climate season on soil fauna community
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Practically all sampled individuals were observed in the rainy season (93.5 %),
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equally distributed in spring (47.2 %) and summer (46.3 %), while the rest of the
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individuals that were sampled in the dry season (6.5 %) concentrated in fall (4.6 %) than in
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winter (1.9 %). The average values of total abundance and richness were higher in rainy
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season compared to dry season, in all forest fragments. The opposite pattern was observed
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for the mean values of evenness and diversity, that were higher in dry season compared to
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rainy season, in all forest fragments (Table 1).
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Table 2. Average abundance of soil fauna taxonomic groups (individuals trap-1 day-1 ± standard error) in Atlantic Rain Forest fragments, in four climate
seasons, Teresópolis, RJ
Spring
Taxonomic groups
Summer
Autumn
Winter
SF
MF
LF
SF
MF
LF
SF
MF
LF
SF
MF
LF
Araneae
0.71±0.20Aa
0.53±0.09Aa
0.87±0.21Aa
0.25±0.05Aa
0.19±0.03Aab
0.21±0.03Aab
0.04±0.02Ab
0.07±0.02Abc
0.05±0.02Ab
-
0.01±0.01c
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Blattodea
0.01±0.01Aa
0.01±0.01Aa
0.01±0.01Aa
0.04±0.02Aa
0.01±0.01Aa
-
0.01±0.01Aa
0.03±0.02Aa
0.01±0.01Aa
0.01±0.01Aa
0.01±0.01Aa
0.07±0.05Aa
Chilopoda
-
-
0.01±0.01a
-
-
0.12±0.12a
-
-
-
-
-
-
Collembola
10.44±1.55Aa
10.99±1.96Aa
11.37±2.81Aa
1.89±0.55Ab
2.19±0.40Aa
1.85±0.24Aa
0.32±0.09Ab
0.27±0.01Ab
0.25±0.07Ab
0.07±0.03Ab
0.10±0.03Ab
0.03±0.02Ab
Coleoptera
5.13±0.76Aa
2.48±0.38Aa
3.85±1.12Aa
1.35±0.32Aab
1.73±0.43Aa
1.16±0.29Aab
0.19±0.06ABbc
0.07±0.02Bb
0.65±0.29Ab
0.09±0.03Ac
0.15±0.08Ab
0.41±0.13Ab
Diplopoda
0.15±0.04Aa
0.16±0.05Aa
0.21±0.05Aa
0.02±0.01Ab
0.04±0.02Aab
0.01±0.01Ab
-
0.02±0.01b
-
-
-
-
Diptera
6.07±1.30Aa
5.62±1.24Aa
7.51±2.02Aa
1.52±0.29Aab
1.84±0.32Aa
1.89±0.52Aab
0.13±0.04Abc
0.29±0.09Ab
0.25±0.09Abc
0.07±0.03Ab
0.16±0.04Ab
0.17±0.08Ac
Enchytraeidae
-
-
0.01±0.01
-
-
-
-
-
-
-
-
-
Formicidae
5.31±0.77Aa
2.35±0.42Ba
21.17±13.97ABa
67.07±34.46Aa
4.11±0.47Aa
5.99±2.23Aa
3.37±1.13Aab
0.51±0.14Bb
1.43±0.41ABab
0.97±0.21Ab
0.47±0.12ABb
0.35±0.12Bb
Heteroptera
0.14±0,06Aa
0.13±0.04Aa
0.06±0.03Ba
0.04±0.02Aa
0.11±0.10Aab
0.01±0.01Ab
0.02±0.01Aa
0.01±0.01Ab
0.02±0.01Ab
0.06±0.03Aa
-
0.02±0.02Ab
Homoptera
0.08±0.02Aa
0.17±0.06Aa
0.13±0.05Aa
0.18±0.06Aa
0.04±0.02Aab
0.02±0.01Aa
0.01±0.01Aa
0.01±0.01Ab
0.03±0.01Aa
0.05±0.04Aa
-
0.05±0.02Aa
-
0.03±0.02Aa
0.18±0.14Aa
-
0.01±0.01Aa
0.01±0.01Aa
-
-
-
-
-
-
Isopoda
0.33±0.05Aa
0.48±0.15Aa
0.51±0.12Aa
0.31±0.13ABab
0.62±0.20Aa
0.07±0.03Bab
0.27±0.16Aab
0.23±0.07Aa
0.09±0.04Aab
0.12±0.11Ab
0.18±0.06Aa
0.13±0.08Ab
Isoptera
0.13±0.04Aa
-
0.04±0.02Ba
0.01±0.01Aa
0.06±0.02Aa
0.05±0.02Aa
0.01±0.01Aa
0.01±0.01Aa
0.09±0.06Aa
0.01±0.01Aa
0.04±0.04Aa
0.13±0.07Aa
Coleoptera’s larvae
0.78±0.25Aa
0.44±0.12Aa
0.63±0.19Aa
0.22±0.06Aa
0.14±0.05Aab
0.29±0.11Aa
0.01±0.01Ab
0.02±0.01Ab
0.03±0.02Aa
0.01±0.01b
-
-
Diptera’s larvae
0.16±0.04Aa
0.11±0.06Aa
0.10±0.05Aa
0.01±0.01Aa
0.01±0.01Aa
0.05±0.04Aa
0.01±0.01Aa
0.01±0.01Aa
0.03±0.02Aa
-
0.02±0.02
-
Lepidoptera’s larvae
Hymenoptera
0.01±0.01Aa
-
0.01±0.01Aa
0.01±0.01Aa
-
0.01±0.01Aa
0.01±0.01Aa
-
0.01±0.01Aa
-
-
-
Lepidoptera
0.02±0.01a
-
-
0.01±0.01Aa
0.01±0.01A
0.01±0.01A
-
-
-
-
-
-
Oligochaeta
-
0.05±0.02Aa
0.08±0.03Aa
0.04±0.02A
0.03±0.01Aa
0.01±0.01Aa
-
-
-
-
-
-
Opilionida
0.09±0.08A
0.01±0.01Aa
0.01±0.01Aa
-
0.03±0.02Aa
0.03±0.02Aa
-
0.01±0.01Aa
0.03±0.02Aa
-
-
-
Orthoptera
0.41±0.13Ba
1.36±0.33Aa
1.14±0.19Aa
0.61±0.24Ba
1.01±0.11Aa
0.35±0.11Bab
-
0.04±0.01Bb
0.24±0.14Ab
0.01±0.01Ab
0.01±0.01Ab
0.03±0.03Abc
Pseudoscorpionida
0.01±0.01A
0.01±0.01Aa
-
-
0.01±0.01Aa
0.01±0.01A
-
-
-
-
-
-
Scorpionida
0.10±0.01A
-
0.02±0.02Aa
-
-
-
-
-
0.01±0.01a
-
-
-
Symphyla
0.01±0.01A
0.15±0.07Aa
-
-
-
-
-
0.01±0.01a
-
-
-
-
Thysanoptera
0.21±0.09a
-
-
0.01±0.01Aa
0.01±0.01A
-
-
-
-
-
-
-
Thysanura
0.01±0.01
-
-
-
-
0.01±0.01a
-
-
0.01±0.01a
-
-
-
*Values followed by different capital letters indicate significant differences among forest fragments within the same season, according Kruskal-Wallis test at 5 %. Values followed by lowercase letters indicate
significant differences between climate seasons within the same forest fragment, according Kruskal-Wallis test at 5 %. SF: small fragment; MF: medium fragment; LF: large fragment.
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Only Collembola, Coleoptera, Diptera, Formicidae and Isopoda were sampled in all of the
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four seasons, regardless of the forest fragmente size. The influence of the weather season in the
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presence/absence occurred for 21 groups (81 % of the total). Chilopoda, Enchytraeidae,
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Hymenoptera, Lepidoptera, Oligochaeta, Pseudoscorpionida and Thysanoptera were sampled only
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during the rainy season (spring and/or summer). Lepidoptera larvae, Opilionida, Scorpionida and
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Symphyla were not sampled only in winter, which is the driest period of the year in the region. No
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group was sampled only in the dry season (fall and/or winter) (Table 2).
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Formicidae predominated in all of the forest fragments, in both rainy and dry seasons.
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However, the relative participation of this group was different among the fragments, in the rainy
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season (SF: 70 %, MF: 19 %, LF: 45 %) and dry season (SF: 67 %, MF: 36 %, LF: 39 %). The
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second group with higher participation in rainy season was Collembola, whose dominance was also
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different among forest fragments (SF: 12 %, MF: 34 %, LF: 22 %). In dry season, there was
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variation among the forest fragments in terms of the second dominant group: Orthoptera in SF (9
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%), Diptera in MF (16 %) and Coleoptera in LF (23 %) (Table 2).
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There were differences between climate seasons in terms of the influence in abundance of
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some taxa in forest fragments. The abundance of Araneae, Collembola, Coleoptera, Diptera,
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Formicidae, Isopoda, Orthoptera and Coleoptera’s larvae were higher in rainy season compared to
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dry season. Neither group presented greater abundance in dry season than in rainy season (Table 2).
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DISCUSSION
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Edge effects on soil fauna community
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The complexity of soil fauna community is a reflection of the plant community. Therefore,
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in general where the vegetation cover showed higher structure and diversity the same pattern was
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observed for soil fauna (Duarte, 2004; Moço et al., 2005; Menezes et al., 2009; Camara et al., 2012;
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Cunha Neto et al., 2012; Pereira et al., 2013). In an Atlantic Forest area with Araucaria angustifolia
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(Bertoloni) O. Kuntze in the state of Rio Grande do Sul, the total average density of soil fauna
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community was higher in larger forest fragments (4.00, 6.00, 18.00 and 35.00 ha) compared to the
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smaller ones (0.25, 0.40 and 0.80 ha) (Duarte, 2004). Abundance, richness, evenness and diversity
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of soil fauna were higher in preserved and not preserved fragments of Atlantic Forest than at a
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Corymbia citriodora (Hook.) KD Hill & L.A.S. Johnson plantation and pasture, both in rainy and
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dry seasons in the North Fluminense region (Moço et al., 2005). The values of total density,
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richness and uniformity of soil macrofauna in the rainy and dry seasons increased with the advance
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of the stage of natural regeneration of Atlantic Forest in abandoned pastures and crop coffee, also in
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the state of Rio de Janeiro (Menezes et al., 2009).
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However, although the total abundance and total richness of soil fauna were higher in native
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forest, followed by abandoned plantation Corymbia citriodora in a gradient of natural regeneration
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of Atlantic Rain Forest, the opposite was found for evenness which was higher in the eualyptus
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plantation within the initial stage of natural regeneration than in the others ecosystems, in the State
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of Rio de Janeiro, in both rainy and dry seasons (Camara et al., 2012).
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In an area of secondary Semidecidual Seasonal Forest in the State of Minas Gerais, the
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values of evenness and diversity in the rainy season, and the total abundance and richness of soil
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fauna in the rainy and dry seasons, were higher than in a plantation of Eucalyptus grandis x
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Eucalyptus urophylla hybrid, but the opposite occurred in the case of evenness and diversity in the
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dry season, which were higher at the eucalyptus plantation (Cunha Neto et al., 2012). In a fragment
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of secondary Atlantic Forest in the State of Rio de Janeiro, the highest values of evenness and
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diversity were found in the interior, where the plant community had more advanced stage of natural
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regeneration, although the highest values of total abundance of soil fauna and richness occurred at
215
the edge, which showed characteristics of early stages of natural regeneration (Pereira et al., 2013).
216
According to data available from seed rain to the forest fragments studied, although the total
217
number of sampled seeds was directly proportional to the size of the fragment (SF: 2394 seeds, MF:
218
4095, LF: 7667) and the richness of the vegetation cover was greater in MF (49 species),
219
intermediate in SF (44) and lowest in LF (31), the diversity was higher in SF (H: 0.96), followed by
220
MF (0.86) and much lower in LF (0:33) (Gondim, 2005). Thus, the author of the work previously
221
mentioned concluded that this was due to the significant relative participation of few species in the
222
seed rain, as more than 75% of the total seeds collected was due to five, three and one species in SF,
223
MF and LF, respectively, and also to the high similarity between MF and LF with respect to the
224
composition and abundance of plant species.
225
Litterfall, which reflect de structure of plant comunnity (Pinto & Marques, 2003; Martin et
226
al., 2004), did not presented differences between these forest fragments (SF: 4.74 t ha, MF: 4.96 and
227
LF: 4.40) (Gomes et al., 2010). So, in the present work the structure of the soil fauna community
228
did not reflect the complexity of the plant community structure, because there were no clear pattern
229
for the first one, as the highest total average abundance was observed in SF and the smallest in MF;
230
the richness values were similar among the forest fragments, with a tendency to be higher in LF and
231
lower in MF; and evenness and diversity were higher in MF and smaller in SF.
232
The absence of a clear pattern of the structure of the soil fauna communities at different
233
plant community occurred in the comparison between two forest fragments in different stages of
10
234
natural regeneration, where richness was higher and evenness were smaller in the fragment with
235
initial stage of regeneration, in the rainy and dry seasons (Calvi et al., 2010). However, the authors
236
of the work earlier cited verified that the values of total abundance and diversity presented
237
conflicting trends from one season to another, because the diversity was lower in the rainy and
238
higher in the dry season, while the abundance was higher in the rainy and lowest in dry season in
239
the fragment with the initial stage of natural regeneration, when compared to the fragment at an
240
advanced stage of natural regeneration.
241
The higher abundance of soil fauna community in SF may be explained by the sampling of a
242
elevated number of individuals of Formicidae, which was the most abundant group in the summer
243
and autumn seasons. In fact, these values in SF were, respectively, 16 times and 11 times higher
244
than in MF and LF in summer, and seven times and two times higher than in MF and LF in autumn.
245
This was probably a response of this group to the prevailing climatic conditions in the smallest
246
forest fragment, which presented the highest degree of disturbance when compared with other forest
247
fragments. The striking abundance of Formicidae in SF (summer: 91 % of total individuals of soil
248
fauna community; autumn: 68 %) was reflected in the lower value for the eveness index in this
249
fragment than in the other ones. This low value for evenness influenced the lowest diversity in SF
250
when compared with the fragments of intermediate and large size.
251
In some situations, the dominance of Formicidae, a group that involves saprophagous and
252
predator species, diminish gradually as advanced the stage of natural regeneration of Atlantic Rain
253
Forest in areas impacted by different anthropogenic activities (Menezes et al., 2009; Calvi et al.,
254
2010; Camara et al., 2012). The relative participation of Formicidae was higher at the edge than in
255
the interior of a fragment of Atlantic Forest in the State of Rio de Janeiro (Pereira et al., 2013).
256
Formicidae presents high participation in the soil fauna community in different forest ecosystems
257
(Moço et al., 2005; Souza et al., 2008; Cunha Neto et al., 2012).
258
Besides Formicidae, the size of the forest fragments influenced the presence/absence in
259
samples, the participation and relative abundance of other groups of soil fauna, which may be
260
considered as indicators of forest fragmentation in Atlantic Forest areas with similar characteristics
261
to those found in this study. Chilopoda, group of predators, and Enchytraeidae, saprophages
262
organisms, occurred only in the larger forest fragment. Hymenoptera, group of predators, was found
263
only in fragments of intermediate and large size. With the size increasing of the fragments,
264
increased the abundance of Coleoptera, group that involves predator or saprophagous species, and
265
Orthoptera, group of herbivorous, and increased the relative participation of Collembola, which
266
belongs to the guild of microphagous-saprophagous.
11
267
Formicidae, Coleoptera and Collembola are soil organisms indicators of ecological changes
268
in the Atlantic Forest, according to a review which considered data from 56 studies conducted in
269
tropical forest areas in different countries, since their diversity responds to changes in the diversity
270
of plant community and/or litter (Junior Brown, 1997). The occurrence of different groups of
271
predators demonstrates a more complex structure of the community characterized by higher
272
functional redundancy and redistribution of energy along the trophic chain (Begon et al., 2005). In
273
the Atlantic Forest with Araucaria angustifolia, the relative participation of Coleoptera was
274
considerably higher in larger fragments than in the smaller ones (Duarte, 2004). The abundance of
275
Coleoptera and Hymenoptera increased as advanced the stage of natural regeneration of secondary
276
areas of Atlantic Forest in the state of Espírito Santo (Calvi et al., 2010).
277
Comparing the edge and interior of an Atlantic Forest fragment, the relative participation of
278
Hymenoptera was almost the same in both environments, but the relative participation of
279
Coleoptera was higher in the interior than the edge, where Chilopoda and Enchytraeidae were
280
restricted (Pereira et al., 2013). Coleoptera (larvae and adults) was not sampled on an abandoned
281
eucalyptus plantation in the early stage of natural regeneration of Atlantic Forest, but was verified
282
in native forest and in an abandoned eucalyptus plantation in advanced stage of natural
283
regeneration, where the abundance of Hymenoptera was lower compared to the the native forest
284
(Camara et al., 2012). Certain predator species of Formicidae were sampled only in a preserved
285
secondary forest fragment and in an abandoned pasture with natural regeneration of Atlantic Forest,
286
and did not occur on a plantation of Acacia mearnsii (De Wild) and na area cultivated with different
287
crop species (Schmidt & Diehl, 2008). Thus, refining the scale of identifying Formicidae key-
288
species as bioindicators of environmental disturbance in the Atlantic Rain Forest ecosystems is an
289
important issue in future works.
290
The abundance of Orthoptera was lower in a forest fragment in advanced stage of natural
291
regeneration of Atlantic Forest (old secondary forest) than in other in early stage (secondary forest)
292
(Calvi et al., 2010). The relative participation of this group in the soil fauna community was lower
293
in native forest than in abandoned eucalypt plantations in different stages of natural regeneration of
294
Atlantic Forest (Camara et al., 2012). Orthoptera, which was sampled only in one of two forest
295
fragments temporarily flooded and preserved in Restinga da Marambaia (Souza et al., 2008), was
296
the only taxonomic group whose abundance was higher in areas of the Amazon-Cerrado transitional
297
forest submitted to repeated burnings, both in the rainy and dry season, when compared with control
298
areas where this management was not performed (Silveira et al., 2010). Orthoptera is a group that
299
colonizes usually with high abundance disturbed environments, where plant community complexity
300
is simplified (Assad, 1997). In the present study, as forest fragments increased its size, the
12
301
abundance of this group also increased. This result suggests that medium and large fragments are
302
likely to receiving a strong influence of the edge effect.
303
Although the relative contribution of Collembola decreased along a gradient of increasing
304
natural regeneration of Atlantic Forest in Espírito Santo (Calvi et al., 2010), the dominance of this
305
group, represented by Entomobryomorpha, increased by an increasing gradient of natural
306
regeneration Atlantic Forest in abandoned plantations of eucalyptus in Rio de Janeiro (Camara et
307
al., 2012). The relative participation of Chilopoda, Coleoptera, Hymenoptera and Collembola, this
308
one represented by Entomobryomorpha, Poduromorpha and Symphypleona groups, were higher in
309
an area of Atlantic Forest than in a plantation of hybrid eucalyptus (Cunha Neto et al., 2012). The
310
relative participation of Collembola (Entomobryomorpha, Poduromorpha and Symphypleona) was
311
higher at the edge than in the interior of a fragment of Atlantic Forest (Pereira et al., 2013).
312
As previously reported, although the richness of soil fauna community were similar between
313
forest fragments, the changes in the composition of groups indicated more clearly the ecological
314
differences between the studied environments. This pattern also occurred for the community of
315
Formicidae, when comparing an area of preserved native forest, abandoned pasture with initial
316
natural regeneration of Atlantic Forest, an area of planting of acacia and an area of agriculture crops
317
(Schmidt & Diehl, 2008). The composition of the soil fauna and the presence of certain functional
318
groups have great potential to assess the quality of soil, the level of degradation caused by
319
anthropogenic abundances (Stork & Eggleton, 1992; Paoletti, 1999) and demonstrate the
320
effectiveness of biological measures employed in environmental recovery processes (Parr &
321
Chown, 2001).
322
Effects of climate season on soil fauna community
323
The values of total abundance and richness were higher in the rainy season. Overall, these
324
results also occurred in areas of native forest and abandoned eucalypt plantations with natural
325
regeneration of Atlantic Forest (Camara et al., 2012). However, density and richness of the fauna
326
collected in litter were higher in dry than in rainy season in an area of initial secondary regeneration
327
(capoeira), and there were no differences between seasons for the fauna community sampled
328
directly in the soil (Moço et al., 2005). In an area in the initial stage of natural regeneration of
329
Atlantic Forest, total abundance of soil fauna was higher in the rainy season, but in the area in an
330
advanced stage of regeneration this variable was higher in the dry season, and there were no
331
differences between the seasons in relation to the total richness in these areas (Calvi et al., 2010).
332
There were no differences between rainy and dry seasons in terms of total density and
333
richness of soil fauna, in three forest fragments in different stages of natural regeneration of Atlantic
334
Forest (Menezes et al., 2009). However, in the work previously cited, the effect of seasonality was
13
335
observed through the variability of total density among the sampling points that increased the
336
standard error in dry season, when compared with rainy season. The same effect occurred in
337
monospecific plantations of Acacia mangium Wild, Mimosa artemisiana Heringer & Paula, hybrid
338
eucalyptus plantation and a pasture area (Cunha Neto et al., 2012).
339
In some areas of Atlantic Rain Forest, litterfall is lower in the dry season (Pinto & Marques,
340
2003; Pereira et al., 2008; Calvi et al., 2009). Consequently, in this period occurs decreasing in the
341
availability of food resources for soil fauna (Correia & Oliveira, 2000) and moisture in the litter,
342
which causes the migration of this organisms from litter to soil layers, reducing the abundance in
343
litter during dry season (Silva et al., 2009). The opposite migration from soil to litter may occur in
344
rainy season (Corrêa Neto et al., 2001). Thus, organisms of soil fauna tends to cluster in high
345
abundance within microsites where there is greater accumulation of water and/or litter in dry
346
season, avoiding most sampling points where environmental conditions are less favorable. In the
347
rainy season, the availability of resources is likely to have more homogeneous distribution, which
348
results in less environmental heterogeneity and, consequently, there is less variability in soil
349
organisms abundance among the microsites (Menezes et al., 2009; Cunha Neto et al., 2012).
350
There was not a well defined pattern about the influence of climate season on the evenness
351
and diversity in the forest fragments studied. In contrast, higher values of evenness and diversity
352
generally in dry than in rainy season have been reported in various tropical forest ecosystems
353
(Moço et al., 2005; Menezes et al., 2009; Calvi et al., 2010; Camara et al., 2012; Cunha Neto et al.,
354
2012).
355
In relation to the presence/absence in sampling, the number of soil fauna groups affected by
356
climate season was nearly three times higher than that affected by the size of forest fragments.
357
Chilopoda, Diplopoda, Enchytraeidae, Hymenoptera, Lepidoptera (larvae and adults), Oligochaeta,
358
Opilionida, Pseudoscorpionida, Scorpionida, Symphyla and Thysanoptera were only sampled in the
359
rainy season, whereas no group was sampled only in the dry season. In the dry season, Coleoptera’s
360
larvae did not occur in soil and litter of an eucalyptus plantation and the same result was observed
361
to Isoptera in the soil compartiment from an area of preserved Atlantic Forest (Moço et al., 2005).
362
Chilopoda was sampled in plantations of Acacia mangium, Mimosa artemisiana, hybrid of
363
Eucalyptus grandis x Eucalyptus urophylla and a pasture area only in the rainy season (Cunha Neto
364
et al., 2012).
365
The abundance of Araneae, Collembola, Coleoptera (larvae and adults), Diplopoda, Diptera,
366
Formicidae, Heteroptera, Homoptera, Isopoda and Orthoptera were higher in rainy season. By other
367
hand, none group presented higher abundance in dry than in rainy season. This suggests that the
368
edge effect was more pronounced in the dry season, probably resulting in edaphoclimatic conditions
14
369
less favorable to soil fauna, as higher air and soil temperature and lower humidity, regardless of size
370
of the forest fragment. Even when there are no differences between climate stations with relation to
371
the total richness of soil fauna community, differences may be observed between them in terms of
372
the composition of soil fauna groups. This occurred in fragments of Atlantic Rain Forest in different
373
stages of natural regeneration, where there were no differences between climate season in relation
374
to the richness, although some groups were only sampled or presented higher abundance in the
375
rainy season, while others were restricted or presented higher abundance in the dry season (Calvi et
376
al., 2010).
377
378
CONCLUSIONS
379
380
1. In relation to the structure of the soil fauna community, the small forest fragment
381
presented higher total abundance; the intermediate-sized forest fragment, the greatest evenness and
382
diversity; and the larger fragment, the greatest richness.
383
384
2. The highest values of total abundance and richness of soil fauna community occurred in
the rainy season, but no clear effects of seasonality were identified on the evenness and diversity.
385
3. The influence of fragment size and seasonality were clearly noted in relation to the
386
composition of soil fauna, due to the diferences between them in terms of presence/absence and/or
387
abundance of some taxonomic groups.
388
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