Microsoft Word - 15-Bio_13450.doc 445 Original Article Biosci. J., Uberlândia, v. 28, n. 3, p. 445-455, May/June. 2012 EFFECTS OF EUCALYPTUS PLANTATIONS ON SOIL ARTHROPOD COMMUNITIES IN A BRAZILIAN ATLANTIC FOREST CONSERVATION UNIT EFEITOS DE PLANTIOS DE EUCALIPTO SOBRE A COMUNIDADE DE ARTRÓPODES DO SOLO EM UMA UNIDADE DE CONSERVAÇÃO DA MATA ATLÂNTICA Rodrigo CAMARA 1 ; Maria Elizabeth Fernandes CORREIA 2 ; Dora Maria VILLELA 3 1. Engenheiro Agrônomo, doutorando no Programa de Pós Graduação em Ecologia e Recursos Naturais da Universidade Estadual do Norte Fluminense - UENF, Campos dos Goytacazes, RJ, Brasil. rcamara73@gmail.com; 2. Pesquisadora da Empresa Brasileira de Pesquisa Agropecuária - EMBRAPA - Agrobiologia, Seropédica, RJ, Brasil. ecorreia@cnpab.embrapa.br; 3. Professora Associada da UENF, Campos dos Goytacazes, RJ, Brasil. dora@uenf.br ABSTRACT: The Atlantic Forest is a conservation hotspot due to its elevated level of biodiversity and current state of degradation. Some areas of Atlantic Forest have been replaced by eucalyptus monocultures in Brazil. Soil arthropods can be important indicators for assessing the recomposition of native forests after disturbs. This study aimed to test the hypothesis that exist differences in the composition and structure of soil arthropod communities among two plantations of eucalyptus (Corymbia citriodora) in different stages of natural regeneration of Atlantic forest (YP = Young Plantation and MP = Mature Plantation, in less and more advanced stage of regeneration, respectively) and a fragment of Atlantic forest (FOREST), in wet and dry seasons, in União Biological Reserve, Brazil, using pitfalls. Archaeognatha, Diplura, Opilionida, and Thysanura were restricted to the FOREST, while Diptera, Isoptera, and Orthoptera were favored by the microclimatic conditions in eucalyptus plantations. Soil arthropod community in FOREST was more complex than those in eucalyptus plantations. In general, soil arthropod communities showed higher total abundance and richness of groups, while equability decreased, as regeneration of Atlantic forest advanced in eucalyptus plantations, making this community more similar to that observed in the FOREST. The average total abundance, average richness, and total richness of soil arthropods were higher in the wet season in all areas, but the opposite occurred for the equability. Soil arthropod community improved with the regeneration of native forest species under the eucalyptus plantations. KEYWORDS: Corymbia citriodora. Ecological indicators. Edaphic fauna. Regeneration. INTRODUCTION The largest portion of biological diversity in all habitats is represented by arthropods (DUELLI et al., 1999). Nevertheless, studies that measure loss of habitat quality commonly focus on vegetation and forest fauna. Less emphasis has been given to the arthropods that inhabit soil permanently or in at least one of their stages of development (DORAN; ZEISS, 2000), despite their essential role in the decomposition and mineralization of the organic matter found in soil, which are vital processes for the sustainability of natural and unmanaged ecosystems (LAVELLE, 1996). Soil arthropods can be efficient ecological indicators because they respond to human pressure on forests through alterations in their community (RAINIO; NIEMELÄ, 2003), with a reduction in the abundance and/or richness of their community as a whole and/or of the diverse groups which compose it (DUARTE, 2004; BARETTA et al., 2008; COPATTI; DAUDT, 2009). The employment, however, of these organisms as bioindicators of ecosystem quality is still incipient (LEWINSOHN et al., 2005), since the importance of the relation between the dynamics of soil degradation and the decline of soil fauna activities has not been fully appreciated (LAVELLE et al., 1994). The potential for arthropods as indicators is especially promising in the case of the Atlantic Forest, for which scarce available data exist (DUARTE, 2004; BARETTA et al., 2008; COPATTI; DAUDT, 2009; FERREIRA; MARQUES, 1998; MOÇO et al., 2003; SOUZA et al., 2008), despite this biome’s status as a conservation hotspot (MYERS et al., 2000) and the important pressure to the expansion of agro-forestry systems, which includes the replacement of native forests by eucalypt plantations for industrial use (LIMA, 1996). Thus, studies aimed at addressing this aspect can contribute substantially to the monitoring of the functioning and conservation of ecosystems that were submitted to the impacts of anthropic activities and belong to this important biome. In this context, the present study aimed to test the hypotheses that exist differences in the composition and structure of soil arthropod Received: 05/08/11 Accepted: 05/11/11 446 Effects of eucalyptus... CAMARA, R.; CORREIA, M. E. F.; VILLELA, D. M. Biosci. J., Uberlândia, v. 28, n. 3, p. 445-455, May/June. 2012 communities: (a) between two plantations of eucalyptus (Corymbia citriodora) in different stages of natural regeneration of Atlantic Forest species in Brazilian biological reserve; (b) between these plantations and a fragment of Atlantic Forest in this biological reserve; and (c) between different climate seasons within these same areas. MATERIAL AND METHODS Study site This study was performed in the União Biological Reserve (22º 27’ 30”S e 42º 02’ 15”W), located in Rio de Janeiro State, Brazil, whose total area is 3,12 ha of which 2,22 ha are covered by Atlantic Forest (LAPENTA et al., 2003). The other part of the area is occupied by abandoned eucalyptus plantations of different ages (220 ha), as well as fields and pastures, roads, and an industrial area (506 ha) (IBAMA, 2007). Part of the forest of the study area was logged in the 1930s for wood to be used in steam locomotives and later plantations of Eucalyptus grandis W. Hill ex Maiden were established for the same purpose in the 1960s and, subsequently, of Corymbia citriodora (Hook.) K. D. Hill & L. A. S. Johnson, other eucalyptus species, in the 1970s to produce railroad ties (EVARISTO et al., 2011). In 1998 the União Biological Reserve was created as a conservation area that would help preserve the habitat of Leontopithecus rosalia (golden lion tamarin), an endemic species of primate threatened with extinction (EVARISTO et al., 2011). According to Köppen’s classification, the predominant climate in the region is humid tropical with a dry winter (Aw), with an average annual temperature of 22 ºC and an average rainfall of 2.337 mm year-1, with 89% concentrated between October and April, in 2009 (Figure 1). The forest growths in Inceptisol and the eucalyptus stands were planted in Ultisol (MIRANDA et al., 2007). 0,0 5,0 10,0 15,0 20,0 25,0 30,0 0 100 200 300 400 500 600 ja n /0 9 fe b/ 0 9 m ar /0 9 ap r/ 09 m ay /0 9 ju n/ 0 9 ju l/0 9 au g/ 0 9 se p/ 09 oc t/ 09 n ov /0 9 d ec /0 9 ja n /1 0 fe b/ 0 9 m ar /1 0 ap r/ 10 m ay /1 0 Te m pe ra tu re ( ° C ) P re ci p it at io n (m m ) Precipitation Temperature Figure 1. Monthly average temperature and rainfall at União Biological Reserve, Brazil. Collected by Golden Lion Tamarin Association. The soil arthropods community was studied in two Corymbia citriodora plantations of different ages that have been unmanaged since 1996: Young Plantation (YP) and Mature Plantation (MP), which were established in 1991 and 1968, respectively (IBAMA, 2007), and in a fragment of the native Atlantic Rainforest (FOREST) located approximately 400 m apart from both the Corymbia citriodora plantations (EVARISTO et al., 2011). The MP has a plantation spacing of 3.0 m x 3.0 m and an area of 11.4 ha, while the YP has a 7.2 ha area and spacing of 1.5 m x 3.0 m (IBAMA, 2007). The tree species community of the Atlantic Forest in natural regeneration in the MP understory presents a more developed structure, higher density of live adult individuals, denser canopy, and higher diversity than that of YP, with Xylopia sericea being the most important species in the regeneration of 447 Effects of eucalyptus... CAMARA, R.; CORREIA, M. E. F.; VILLELA, D. M. Biosci. J., Uberlândia, v. 28, n. 3, p. 445-455, May/June. 2012 MP and Myrsine coriacea in the YP (EVARISTO et al., 2011). Experimental design Evaluations of the natural regeneration of Atlantic Rainforest native tree species were carried out in five plots (5 m x 20 m) installed in each of the two eucalyptus plantations: YP and MP (EVARISTO et al., 2011). The sampling of soil arthropods community was performed by means of two pitfalls traps installed randomly in each one of these plots, obtaining ten pitfalls in each plantation. In the FOREST, a 50-meter transect was settled starting 100 m from the edge, and pitfalls were installed at five meters apart each one, obtaining ten pitfalls in this area. Each trap was considered an experimental unit. These traps, which allow the indirect evaluation of the abundance of taxonomic groups that reflects “activity-density”, which can be affected by habitat (APIGIAN et al., 2006), were employed in the wet season (January) and dry season (August) of 2010. The arthropods collected were identified by the use of pertinent literature (COSTA et al., 1988; VAN ACHTERBERG, 1991). Formicidae was considered a taxonomic group apart from Hymenoptera, because of the facility of identification. Collembola was subdivided in three taxonomic groups: Entomobryomorpha, Poduromorpha and Symphypleona. This study estimated average total abundance for each group was estimated, expressed in number of individuals per trap per day, average richness, considering the average of the number of taxonomic groups within the experimental units in each area, total richness or the total number of taxonomic groups in each area, the relative participation (%) of the taxonomic groups and the equability (Pielou Index). The equability index varies between zero and one, and the distribution of individuals within taxonomic groups became more equal as the value of this index became closer to one (ODUM, 1988). The comparisons among the different areas within the same climate season were performed by the non-parametric statistical Kruskal-Wallis Test. In order to compare the results between different seasons within the same area, the non-parametric statistical Mann-Whitney Test was employed (ZAR, 1984). Statistical analyses were carried out with Statistica 7.0 program. The Sorensen index was used to calculate the similarity between the areas in relation to the taxonomic groups’ composition. RESULTS Thirty-three soil fauna taxonomic groups were found in the União Biological Reserve. More than half of the total taxons (61%) were common to the two plantations and the FOREST. Archaeognatha and Thysanura, both saprophage groups, and the predators Diplura and Opilionida were restricted to the FOREST, while Isoptera occurred only in the two eucalyptus plantations. Pseudoscorpionida (predators) were absent in the MP, though they were found both in the YP and the FOREST in the wet season. In the dry season, this group was only encountered in the FOREST. Diplopoda (saprophages), Mantodea and Trichoptera’s larvae were only sampled in the MP. However, Coleoptera (adult individuals and larva), which involve predators and another functional groups, Heteroptera (herbivorous) and Isopoda (saprophages) were equally present in the MP and the FOREST, but were not observed in the YP (Table 1). The FOREST presented an abundance of Araneae (predators) and Entomobryomorpha (microphage or saprophage) significantly higher than in the plantations during the wet season. The abundance of Coleoptera and Hymenoptera (predators) was significantly higher in the FOREST than in the MP in the wet season. The abundance of Coleoptera was significantly higher in the FOREST than in the YP in the dry season. The opposite occurred for Orthoptera in wet season and for Auchenorrhyncha in the dry season. The YP showed significantly higher abundance of Diptera when compared to other locations in the wet season. This pattern was also observed in the MP for Acari, also in the wet season (Table 1). Formicidae was one of the most abundant groups in all of three study areas, in both climactic seasons, although there were differences with respect to the participation of the most abundant taxonomic groups (Table 1). Entomobryomorpha represented the highest contribution in total abundance of the soil arthropod community in FOREST - more than 60% - in both climate seasons (Table 1). The contribution of Entomobryomorpha increased as the natural regeneration developed in eucalyptus plantations: from 5% in YP to 30% in MP, in the wet season, and from 8% in YP to 65% in MP, in the dry season (Table 1). The opposite was observed in relation to Diptera’s participation: the contribution of this taxonomic group decreased from 28% in YP to 6% in MP, in the wet season, and from almost 29% in YP to almost 12% in MP, in the dry season (Table 1). 448 Effects of eucalyptus... CAMARA, R.; CORREIA, M. E. F.; VILLELA, D. M. Biosci. J., Uberlândia, v. 28, n. 3, p. 445-455, May/June. 2012 Table 1. Average abundance (number of individuals pitfall-1 day-1 ± standard error) of soil arthropods in Corymbia citriodora (eucalyptus) and in Atlantic Rainforest at União Biological Reserve, Brazil1 Taxonomic groups Eucalyptus Atlantic Rainforest Young plantation Mature plantation Abundance % Abundance % Abundance % Wet season (January 2010) Acari 1.00 ± 0.31 B 4.76 3.61 ± 1.02 A 15.33 1.04 ± 0.34 B 3.00 Araneae 0.40 ± 0.08 B 1.90 0.43 ± 0.10 B 1.83 0.96 ± 0.14 A 2.77 Archaeognatha - - - - 0.07 ± 0.03 A 0.20 Auchenorryncha 0.41 ± 0.16 A 1.95 0.34 ± 0.13 A 1.44 0.40 ± 0.06 A 1.16 Blattodea 0.16 ± 0.05 A 0.96 0.10 ± 0.06 A 0.42 0.03 ± 0.02 A 0.09 Coleoptera - - 0.13 ± 0.03 B 0.55 0.81 ± 0.07 A 2.34 Coleoptera’s larvae - - 0.17 ± 0.05 A 0.72 0.11 ± 0.05 B 0.32 Diplopoda - - 0.01 ± 0.01 A 0.04 - - Diplura - - - - 0.03 ± 0.02 A 0.09 Diptera 5.89 ± 0.89 A 28.05 1.49 ± 0.24 B 6.33 2.29 ± 0.44 B 6.61 Diptera’s larvae 0.01 ± 0.01 A 0.05 0.04 ± 0.02 A 0.17 0.04 ± 0.02 A 0.12 Entomobryomorpha 1.09 ± 0.11 B 5.19 7.00 ± 1.28 B 29.75 21.69 ± 2.81 A 62.63 Poduromorpha 0.03 ± 0.03 A 0.14 - - - - Symphypleona 5.66 ± 2.25 A 26.95 0.27 ± 0.12 B 1.15 0.37 ± 0.15 AB 1.07 Formicidae 3.17 ± 0.47 B 15.10 7.39 ± 1.64 A 31.41 5.03 ± 0.65 AB 14.52 Formicidae’s larvae - - 0.01 ± 0.01 A 0.04 - - Heteroptera - - 0,01 ± 0,01 A 0.04 0.01 ± 0.01 A 0,03 Hymenoptera 0.74 ± 0.20 AB 3.52 0.20 ± 0.06 B 0.85 0.90 ± 0.22 A 2.60 Isopoda 0.01 ± 0.01 A 0.05 0.13 ± 0.08 A 0.55 0.01 ± 0.01 A 0.03 Isoptera 0.01 ± 0.01 A 0.05 0.13 ± 0.09 A 0.55 - - Lepidoptera’s larvae 0.01 ± 0.01 A 0.05 0.04 ± 0.02 A 0.17 0.03 ± 0.02 A 0.09 Mantodea - - 0.04 ± 0.04 A 0.17 - - Opilionida - - - - 0.09 ± 0.07 A 0.26 Orthoptera 1.90 ± 0.56 A 9.05 1.80 ± 0.71 A 7.65 0.40 ± 0.12 B 1.16 Pseudoscorpionida 0.01 ± 0.01 A 0.05 - - 0.01 ± 0.01 A 0.03 Psocoptera 0.04 ± 0.03 A 0.19 0.13 ± 0.05 A 0.55 0.03 ± 0.03 A 0.09 Sternorryncha 0.37 ± 0.13 A 1.76 0.01 ± 0.01 A 0,04 0.04 ± 0.02 A 0.12 Thysanoptera 0.06 ± 0.03A 0.29 - - 0.10 ± 0.05 A 0.29 Thysanura - - - - 0.13 ± 0.11 A 0.38 Trichoptera’s larvae - - 0.03 ± 0.02 A 0.13 - - Dry season (July 2010) Acari 0.35 ± 0.11 A 5.86 0.63 ± 0.18 A 3.56 1.02 ± 0.23 A 6.20 Araneae 0.25 ± 0.05 A 4.19 0.25 ± 0.09 A 1.41 0.48 ± 0.07 A 2.92 Auchenorryncha 0.49 ± 0.11 A 8.21 0.48 ± 0.12 A 2.71 0.13 ± 0.04 B 0.79 Coleoptera 0.05 ± 0.02 B 0.84 0.27 ± 0.08 AB 1.53 0.73 ± 0.22 A 4.44 Coleoptera’s larvae 0.02 ± 0.02 A 0.34 0.06 ± 0.03 A 0.34 0.06 ± 0.03 A 0.36 Diptera 1.70 ± 0.43 A 28.48 2.08 ± 0.49 A 11.75 1.24 ± 0.28 A 7.54 Diptera’s larvae - - 0.06 ± 0.03 A 0.34 0.11 ± 0.04 A 0.67 Earthworm’s cocoon - - - - 0.02 ± 0.02 A 0.12 Entomobryomorpha 0.49 ± 0.27 B 8.21 11.44 ± 2.24 A 64.63 10.48 ± 1.26 A 63.75 Poduromorpha - - - - 0.11 ± 0.08 A 0.67 Symphypleona 0.05 ± 0.02 A 0.84 0.08 ± 0.03 A 0.45 0.21 ± 0.09 A 1.28 449 Effects of eucalyptus... CAMARA, R.; CORREIA, M. E. F.; VILLELA, D. M. Biosci. J., Uberlândia, v. 28, n. 3, p. 445-455, May/June. 2012 Formicidae 2.02 ± 0.47 A 33.84 1.38 ± 0.34 A 7.80 1.00 ± 0.17 A 6.08 Formicidae’s larvae - - - - 0.02 ± 0.02 A 0.12 Heteroptera 0.17 ± 0.07 A 2.85 0.03 ± 0.02 A 0.17 0.08 ± 0.05 A 0.49 Hymenoptera 0.11 ± 0.05 A 1.84 0.16 ± 0.05 A 0.90 0.33 ± 0.09 A 2.01 Isopoda - - 0.02 ± 0.02 A 0.11 0.05 ± 0.03 A 0.30 Isoptera 0.02 ± 0.02 A 0.34 0.03 ± 0.02 A 0.17 0.02 ± 0.02 A 0.12 Lepidoptera 0.02 ± 0.02 A 0.34 - - - - Orthoptera 0.17 ± 0.06 A 2.85 0.16 ± 0.06 A 0.90 0.22 ± 0.09 A 1.34 Pseudoscorpionida - - - - 0.02 ± 0.02 A 0.12 Psocoptera 0.02 ± 0.02 A 0.34 0.05 ± 0.02 A 0.28 0.03 ± 0.02 A 0.18 Sternorryncha 0.02 ± 0.02 A 0.34 - - - - Thysanoptera 0.03 ± 0.02 A 0.50 0.51 ± 0.23 A 2.88 0.10 ± 0.04 A 0.61 Thysanura - - - - 0.02 ± 0.02 A 0.12 1Values with significant difference in the same line, are followed by different letters (Kruskal-Wallis Test, p<0.05). The total abundance and average richness of soil arthropods increased according to the natural trees native regeneration in the understory of the eucalyptus plantations (Table 2). The total richness presented the same pattern in the wet season, while a higher distinction between the plantations and the FOREST was observed in the dry season. The equability index value in the MP was close to that verified in the FOREST and lower than that found in the YP in the wet and in the dry seasons (Table 3). Table 2. Total average abundance (number of individuals pitfall-1 day-1 ± standard error) and average richness of taxonomic groups (number of taxonomic groups) of soil arthropods in Young Plantation (YP) and Mature Plantation (MP) of Corymbia citriodora (eucalyptus) and Atlantic Rainforest (FOREST) at União Biological Reserve, Brazil1 Area Total Average Abundance Average Richness Wet Season Dry Season Wet Season Dry Season YP 21.03 ± 3.05 Ba 5.97 ± 1.01 Bb 11 Aa 8 Bb MP 23.53 ± 3.27 ABa 17.70 ± 2.23 Aa 12 Aa 10 ABa FOREST 34.63 ± 3.70 Aa 16.44 ± 1.94 Ab 13 Aa 12 Aa 1Values followed by different capital letters in the same column means significant difference among areas at the same season (Kruskal- Wallis Test, p<0.05). Values followed by different minuscule letters in the same line means significant difference between seasons at same area (Mann-Whitney Test, p<0.05). Table 3. Total richness (total number of taxons) and Pielou’s index (equability) of soil arthropods in Young Plantation (YP) and Mature Plantation (MP) of Corymbia citriodora (eucalyptus) and Atlantic Rainforest (FOREST) at União Biological Reserve, Brazil Area Total Richness Equability Wet Season Dry Season Wet Season Dry Season YP 20 17 0,53 0,67 MP 23 17 0,49 0,49 FOREST 24 22 0,44 0,49 Comparing the two climate seasons, the values for total average abundance, average richness, and total richness of soil arthropods were generally higher in the wet season than in the dry season in all three areas studied, while the opposite occurred with the equability value, which was higher in the dry season than in the wet season (Table 3). The three study areas presented higher Sorensen index values, because all of them was higher than 0.5 (ANDRADE et al., 2002), but this index showed that the arthropods community composition in YP was more similar to MP than to the FOREST, and that the FOREST had higher similarity with MP, than with YP (Table 4). 450 Effects of eucalyptus... CAMARA, R.; CORREIA, M. E. F.; VILLELA, D. M. Biosci. J., Uberlândia, v. 28, n. 3, p. 445-455, May/June. 2012 Table 4. Sorensen index (similarity) of soil arthropods in Young Plantation (YP) and Mature Plantion (MP) of Corymbia citriodora (eucalyptus) and Atlantic Rainforest (FOREST) at União Biological Reserve, Brazil Area Wet season Dry season YP MP FOREST YP MP FOREST YP 1 0.76 0.70 1 0.88 0.77 MP 0.76 1 0.77 0.88 1 0.87 FOREST 0.70 0.77 1 0.77 0.87 1 DISCUSSION The conversion of natural forests by humans into other types of ecosystems results in modifications in the structure and fertility of the soil environment (MOÇO et al., 2003) which are reflected in the soil fauna community (LAVELLE et al., 2006), whose response presents variations depending on which group the organisms belong to (CIVIDANES, 2002; COIMBRA et al., 2007; COPATTI; DAUDT, 2009). This results from the manner in which each group exploits the available resources. Thus, soil arthropods are grouped in three functional categories: predators, saprophages, and ecosystem engineers (LAVELLE, 1996). In the present study, results showed that the establishment of eucalyptus plantations was responsible for the exclusion and/or reduction in abundance of certain groups of soil arthropods, notably those that contain predators and saprophages, as well as favoring other groups, in comparison with native forest. Therefore, these organisms, which tended to be eliminated from the system, were those most sensitive to environmental impacts (MOÇO et al., 2003), which suggests that, within the soil arthropod community, the predators and saprophages can be considered the most appropriate functional groups for the monitoring of ecosystem functioning and of the impacts caused by the establishment of eucalyptus plantations in the Atlantic forests and probably humid tropical forests. The unfavorable conditions caused to these groups could trigger disruptions in distinct aspects of soil functions (KNOEPP et al., 2000). The increase in plant community diversity, in terms of species richness and functional groups, may favor the increase in soil arthropod density (EISENHAUER et al., 2011), likely due to the production of more diverse litter in decomposition (LAVELLE et al., 1994; COIMBRA et al., 2007), which can offer the soil improved nutritional conditions in terms of both quality and quantity, such as N, P, and K, compared with more homogenous forest litter (WANG et al., 2008). This effect may be produced by the complementariety of species, when species that occupy different ecological niches coexist in the same environment (LOREAU et al., 2001). It is believed that this process occurred in União Biological Reserve, where the tree community in the MP presented more diversity than the YP (EVARISTO et al., 2011) and thus the plant litter decomposition in the first plantation is more heterogeneous than that of YP (TESCH, 2005). A previous study registered the presence of a litter layer with a higher nutritional quality in the soil surface of the MP (N total = 7.4 g kg-1; C/N ratio = 74) compared with the YP (N total = 4.2 g kg-1; C/N = 114) (VILLELA et al., 2004), which influenced the higher total content of N (3.1 g kg-1) and lower C/N (8.85) in MP soil compared with the YP (N total = 1.3 g kg-1; C/N = 18) (VILLELA et al., 2001). The total N content in the soil may present a positive correlation to the soil biota composition in eucalyptus forests, as has been verified in Australia (CATTERALL et al., 2001). In addition, as a consequence of a closer canopy in the MP than in the YP, the solar radiation above the soil is probably more intense in the YP, condition that may result in cooler soil temperatures and higher humidity levels in the MP than the YP soil. Thus areas in a more advanced stage of natural regeneration of native tree species can be colonized by a soil arthropod community with higher species richness and/or groups with different survival strategies and a more complex structure than those in a more initial stage (OLIVEIRA et al., 1995; WARREN & ZOU, 2002; LAN et al., 2006; NEGRETE-YANKELEVICH et al., 2006; MAHARNING et al., 2009), due to increased support capacity caused by a higher diversity of niches available in the former (LAVELLE, 1996). The incidence of solar radiation in the MP may be probably closer to that verified in the FOREST and may therefore also allow the soil temperature and humidity level in the MP to be in line with conditions in the FOREST when compared with the YP. This would justify the increased similarities between the soil arthropod communities in the MP and the FOREST compared to the YP. 451 Effects of eucalyptus... CAMARA, R.; CORREIA, M. E. F.; VILLELA, D. M. Biosci. J., Uberlândia, v. 28, n. 3, p. 445-455, May/June. 2012 Nevertheless, the soil arthropod community in the FOREST presented a higher level of complexity than both eucalyptus plantations. This suggests that, despite the more advanced stage of natural regeneration in the MP in relation to the YP (EVARISTO et al., 2011), the negative impacts on soil arthropods associated with the substitution of the FOREST for the establishment of eucalyptus plantations can still be noticed. Some species of Opilionida and Pseudoscorpionida are important biological indicators due to their rarity or endemism (MMA, 2003; SOUZA et al., 2008). Opilionida were only observed in a fragment of the Atlantic Forest when compared with a plantation of eucalyptus (Eucalyptus sp.) established in a conservation unit located in the Southeast of Brazil (LEWINSOHN et al., 2005), as in the present study. In forests of Araucaria angustifolia (Bertoloni) O. Kuntze (Araucariaceae), which are ecosystems associated to the Atlantic Forest biome, the abundance of Araneae and Coleoptera fell sharply with the reduction of the size of fragments, with Pseudoscorpionida pratically disappearing in the smaller fragments, probably due to higher levels of alteration of the vegetation structure and to reduced quantities of litter on the soil surface in these fragments when compared to other larger fragments studied (DUARTE, 2004). Pseudoscorpionida was observed in a preserved FOREST and also in an 18-year-old plantation of Corymbia citriodora in the state of Rio de Janeiro (MOÇO et al., 2003). However, this group was not observed in other ecosystems studied: a natural unpreserved forest, a shrubland in regeneration, and a five-year-old pasture. A reduction of the primary resources of food chains can cause a decline in abundance of predators, those organisms that occupy the top of such chains, which suggests that bottom-up control of ecosystems may be negatively affected by disturbance, as was observed in tropical forests in Mexico subjected to selective logging of native vegetation (NEGRETE-YANKELEVICH et al., 2007). It is believed that this process may explain the loss of predator groups in eucalyptus plantations compared with the native FOREST in the União Biological Reserve. Nevertheless, besides predators, saprophages were also negatively affected by the plantations in the study area and thus may signal a loss of edaphic environment quality as a whole. Soil arthropod communities in disturbed environments can become increasingly dominated over time by groups of opportunistic organisms that are able to adapt and tolerate the disturbances (LAURANCE et al., 2002). It is possible the case for Orthoptera and Auchenorryncha, as both groups increased their population in the eucalyptus plantations in the present study, in contrast to what happened in the FOREST. The same may be concluded for Diptera, a group composed of adult individuals that don’t exploit forest litter soil resources in this stage of life, and whose average abundance was significantly greater in the YP in the wet season, compared with the other study areas. The importance of Diptera in the YP was highlighted by its elevated relative participation, which was the highest among all groups in the wet season and the second highest in the dry season. Orthoptera is a group capable to colonize simplified environments, replacing other groups. This trait contributes to a higher average abundance of this opportunistic group in newer and disturbed environments (ASSAD, 1997). Within the different taxons of soil arthropods, Orthoptera was the only order whose abundance increased significantly in forest areas of the Brazilian Amazon that were subjected to repeated burnings, compared with others that were not burned, during one year (SILVEIRA et al., 2010). The elevated total average abundance of soil fauna in the FOREST and MP in relation to the YP, in both climate seasons, was probably influenced by the important contribution of Entomobryomorpha, which ranked in the two most abundant groups in the MP and FOREST in both seasons. In the YP, however, this group occupied the fifth and fourth positions in the wet and in the dry seasons, respectively. One of the reasons for the increase in Entomobryomorpha populations in less disturbed ecosystems is the higher organic material levels in the soil compared with environments subjected to negative impacts (MUSSURY et al., 2002). In addition, when environmental conditions are more stable, a dominance of a small number of groups is observed, groups which become strong competitors for resources (30). The climate season can influence soil arthropod community because of the rainfall seasonality. Total average abundance, average richness, and total richness of soil arthropods were higher in all three study areas in the wet season, in comparison with the dry season. The higher pluviometry can stimulate the vegetal growth and litter production in wet season, which may increase resources to soil arthropods, in comparison to the dry season (KNOEPP et al., 2000). So, the dry season can prejudice the soil arthropod community. The results obtained in this study corroborated the hypothesis that exist differences in the composition and structure of soil arthropod 452 Effects of eucalyptus... CAMARA, R.; CORREIA, M. E. F.; VILLELA, D. M. Biosci. J., Uberlândia, v. 28, n. 3, p. 445-455, May/June. 2012 communities between two plantations of eucalyptus (Corymbia citriodora) in different stages of natural regeneration of Atlantic Forest tree species in the União Biological Reserve. The soil under the native forest hosted a more complex community of arthropods than the plantations of Corymbia citriodora, thus indicating that the replacement of Atlantic Forest by monocultures of this species of eucalyptus can comprise the functioning of the ecosystem. The climate seasons considerable influenced the soil arthropod communities. In the general, the wet season favoured total average abundance, average richness, and total richness of soil arthropods in all three study areas, in comparison with the dry season. ACKNOWLEDGMENTS We thank the FAPERJ - Fundação Carlos Chagas Filho de Amparo à Pesquisa do Estado do Rio de Janeiro for financial support (APQ1E- 26/110.400/2010) and to the scholarship of the first author; the União Biological Reserve - Instituto Chico Mendes de Conservação da Biodiversidade (ICMBio) and the Graduation Program of Ecology and Natural Resources (PPGERN) at UENF for logistic support. We also thank Marcelo Trindade Nascimento for the support during the project, Vinícius Duncan, Gerson Purificação e Helmo Carvalho for their help in field work and Roberto Silva for his help in arthropods identifications. RESUMO: A Mata Atlântica é um hotspot para a conservação pela elevada biodiversidade e estado atual de degradação. Algumas de suas áreas têm sido substituídas por monoculturas de eucaliptos no Brasil. Os artrópodes do solo podem ser importantes indicadores da recomposição de florestas nativas pós-distúrbio. O presente estudo objetivou testar a hipótese de que existem diferenças na composição e estrutura da comunidade de artrópodes do solo entre dois plantios de eucalipto (Corymbia citriodora) em diferentes estágios de regeneração natural de Mata Atlântica (PJ = Plantio Jovem e PM = Plantio Maduro, em estágio de regeneração menos e mais avançado, respectivamente) e um fragmento de Mata Atlântica (FLORESTA), nas estações chuvosa e seca, na Reserva Biológica União, Brasil, usando armadilhas de queda. Archaeognatha, Diplura, Opilionida, e Thysanura restringiram-se à FLORESTA, enquanto Diptera, Isoptera, e Orthoptera foram favorecidos pelas condições microclimáticas nos eucaliptais. A complexidade da comunidade de artrópodes do solo foi maior na FLORESTA do que nos eucaliptais. Em geral, a comunidade de artrópodes do solo apresentou maior abundância total e riqueza de grupos, enquanto a equitabilidade diminuiu, conforme a regeneração da Mata Atlântica avançou nos eucaliptais, formando uma comunidade mais semelhante àquela observada na FLORESTA. A abundância media total, a riqueza média e a riqueza total de artrópodes do solo foram maiores na estação chuvosa em todas as áreas, mas o oposto ocorreu para a equitabilidade. A comunidade de artrópodes do solo se tornou mais complexa com o avanço da regeneração de espécies nativas de Mata Atlântica no sub-bosque dos eucaliptais. PALAVRAS-CHAVE: Corymbia citriodora. Fauna edáfica. Indicadores ecológicos. Regeneração. REFERENCES ANDRADE, L. A. Z.; FELFILI, J. M.; VIOLATTI, L. Fitossociologia de uma área de Cerrado denso na RECOR-IBGE, Brasília-DF. Acta Botanica Brasilica, São Paulo, v. 16, n. 2, p. 225-240, abr. 2002. APIGIAN, K. O.; DAHLSTEN, D. L.; STEPHENS, S. L. Biodiversity of Coleoptera and the importance of habitat structural features in a Sierra Nevada mixed-conifer forest. Environmental Entomology, Lanham, v. 35, n. 4, p. 964-975, aug. 2006. ASSAD, M. L. L. Fauna do solo. In: VARGAS, M.A.T. & HUNGRIA, M. (Org.). Biologia dos solos dos Cerrados. Planaltina, DF: Embrapa-Cpac, 1997. p. 363-443. BARETTA, D.; FERREIRA, C. S.; SOUSA, J. P. S.; CARDOSO, E. J. B. N. Colêmbolos (Hexapoda: Collembola) como bioindicadores da qualidade do solo em áreas de Araucaria angustifolia. Revista Brasileira de Ciência do Solo, Viçosa, v. 32, n. especial, p. 2693-2699, out./dez. 2008. CATTERALL, C. P.; PIPER, S. D.; BUNN, S. E.; ARTHUR, J. M. Flora and fauna assemblages vary with local topography in a subtropical eucalypt forest. Austral Ecology, Hoboken, v. 26, n. 1, p. 56–69, feb. 2001. 453 Effects of eucalyptus... CAMARA, R.; CORREIA, M. E. F.; VILLELA, D. M. Biosci. J., Uberlândia, v. 28, n. 3, p. 445-455, May/June. 2012 CIVIDANES, F. J. Efeitos do sistema de plantio e da consorciação soja-milho sobre artrópodes capturados no solo. Pesquisa Agropecuária Brasileira, Brasília, v. 37, n. 1, p. 15-23, jan. 2002. COIMBRA, J. L. M.; SANTOS, J. C. P.; ALVES, M. V.; BARZOTTO, I. Técnicas multivariadas aplicadas ao estudo da fauna do solo: contrastes multivariados e análise canônica discriminante. Revista Ceres, Viçosa, v. 54, n. 313, p. 270-276, mai/jun. 2007. COPATTI, C. E.; DAUDT, C. R. Diversidade de artrópodes na serapilheira em fragmentos de mata nativa e Pinus elliottii (Engelm. var elliottii). Ciência e Natura, Santa Maria, v. 31, n. 1, p. 95–113, jun. 2009. COSTA, C.; VANIN, S. A.; CASARI-CHEN, A. S. Larvas de Coleoptera do Brasil. São Paulo: FAPESP, 1988. 165 p. DORAN, J. W.; ZEISS, M. R. Soil health and sustainability: managing the biotic component of soil quality. Applied Soil Ecology, Amsterdam, v. 15, n. 1, p. 3-11, aug. 2000. DUARTE, M. M. Abundância de microartrópodes do solo em fragmentos de mata com araucária no sul do Brasil. Iheringia, Porto Alegre, v. 94, n. 2, p. 163-169, jun. 2004. DUELLI, P.; OBRIST, M. K.; SCHMATZ, D. R. Biodiversity evaluation in agricultural landscapes: above- ground insects. Agriculture, Ecosystems and Environment, Amsterdam, v. 74, n. 1, p. 33–64, jun. 1999. EISENHAUER, N.; MILCU, A.; SABAIS, A. C.; BESSLER, H.; BRENNER, J.; ENGELS, C.; KLARNER, B.; MARAUN, M.; PARTSCH, S.; ROSCHER, C.; SCHONERT, F.; TEMPERTON, V.M.; THOMISCH, K.; WEIGELT, A.; WEISSER, W.W.; SCHEU, S. Plant diversity surpasses plant functional groups and plant productivity as driver of soil biota in the long term. PLoS One, v. 6, n. 1, 2011. doi:http://www.plosone.org/article/info:doi%2F10.1371%2Fjournal.pone.0016055. Accessed April 30th, 2011. EVARISTO, V. T.; BRAGA, J. M. A.; NASCIMENTO, M. T. Atlantic Forest regeneration in abandoned plantations of eucalypt (Corymbia citriodora (Hook.) KD Hill and LAS Johnson) in Rio de Janeiro, Brazil. Interciencia, Caracas, v. 36, n. 6, p. 431-436, jun. 2011. FERREIRA R. L.; MARQUES, M. M. G. S. M. A fauna de artrópodes de serrapilheira de áreas de monocultura com Eucalyptus sp. e mata secundária heterogênea. Anais da Sociedade Entomológica do Brasil, Londrina, n. 3, v. 27, p. 395-403, set. 1998. IBAMA. Plano de recuperação dos eucaliptais da Reserva Biológica União. Rio das Ostras: Reserva Biológica União, Associação Mico-leão Dourado, Critical Ecosystem Partnership Fund, 2007. 141 p. KNOEPP, J. D.; COLEMAN, D. C.; CROSSLEY JR, D. A.; CLARK, J. S. Biological indices of soil quality: an ecosystem case study of their use. Forest Ecology and Management, Amsterdam, v. 138, p. 357-368, nov. 2000. LAN, Y.; WENHUI, Y.; YONGCHANG, S. Soil animal communities at five succession stages in the litter of the evergreen broad-leaved forest in Tiantong, China. Frontiers of Biology in China, Berlin, v. 1, n. 2, p. 142−150, jun. 2006. LAPENTA, M. J.; PROCÓPIO-DE-OLIVEIRA, P.; KIERULFF, M. C. M.; MOTTA-JR, J. C. Fruit exploitation by golden lion tamarins (Leontopithecus rosalia) in the União Biological Reserve, Rio das Ostras, RJ - Brazil. Mammalia, Paris, v. 67, n. 1, p. 41–46, jan. 2003. LAURANCE, W. F.; LOVEJOY, T. E.; VASCONCELOS, H. L.; BRUNA, E. M.; DIDHAM, R. K.; STOUFFER, P. C.; GASCON, C.; BIERREGAARD, R. O.; LAURANCE, S. G.; SAMPAIO, E. Ecosystem decay of Amazonian forest fragments: a 22-year investigation. Conservation Biology, Malden, v. 16, n. 3, p. 605–618, jun. 2002. 454 Effects of eucalyptus... CAMARA, R.; CORREIA, M. E. F.; VILLELA, D. M. Biosci. J., Uberlândia, v. 28, n. 3, p. 445-455, May/June. 2012 LAVELLE, P. Diversity of soil fauna and ecosystem function. Biology International, Paris, v. 33, p. 3-16, jul. 1996. LAVELLE, P.; DANGERFIELD, M.; FRAGOSO, C.; ESCHNEBRENNER, V.; LOPEZ-HERNANDEZ, D.; PASHANARI, B.; BRUSSARD, L. The relationship between soil macrofauna and tropical soil fertility. In WOOMER, P.L. & SWIFT, M.J. (Ed.). The biological management of tropical soil fertility. Londres: Wiley- Sayce, 1994. p. 136-169. LAVELLE, P.; DECAËNS, T.; AUBERT, M.; BAROTA, S.; BLOUINA, M.; BUREAU, F.; MARGERIE, P.; MORAA, P.; ROSSIC, JP. Soil invertebrates and ecosystem services. European Journal of Soil Biology, Amsterdam, v. 42, p. S3–S15, oct. 2006. LEWINSOHN, T. M.; FREITAS, A. V. L.; PRADO, P. I. Conservation of terrestrial invertebrates and their habitats in Brazil. Conservation Biology, Malden, v. 19, n. 3, p. 640-645, jun. 2005. LIMA, W. P. Impacto ambiental do eucalipto. 2ª ed. São Paulo: Universidade de São Paulo, 1996. 301 p. LOREAU, M.; NAEEM, S.; INCHAUSTI, P.; BENGTSSON, J.; GRIME, J. P.; HECTOR, A.; HOOPER, D. U.; HUSTON, M. A.; RAFFAELLI, D.; SCHMID, B.; TILMAN, D.; WARDLE, D. A. Ecology – biodiversity and ecosystem functioning: Current knowledge and future challenges. Science, Washington, v. 294, p. 804– 808, oct. 2001. MAHARNING, A. R.; MILLS, A. A. S.; ADL, S. M. Soil community changes during secondary succession to naturalized grasslands. Applied Soil Ecology, Amsterdam, v. 41, n. 2, p. 137–147, feb. 2009. MIRANDA, C. C.; CANELLAS, I. P.; NASCIMENTO, M. T. Caracterização da matéria orgânica do solo em fragmentos de Mata Atlântica e plantios abandonados de eucalipto, Reserva Biológica União, RJ. Revista Brasileira de Ciência do Solo, Viçosa, v. 31, p. 905-916, oct. 2007. MMA (Ministério do Meio Ambiente). Anexo à Instrução Normativa n° 3, de 27 de maio de 2003, do Ministério do Meio Ambiente. Lista das espécies da fauna brasileira ameaçadas de extinção. Ministério do Meio Ambiente (MMA), Brasília. Available at http://www.ibama.gov.br/fauna/downloads/lista%20spp.pdf. Accessed April 30th, 2011. MOÇO, M. K. S.; GAMA-RODRIGUES, E. F.; GAMA-RODRIGUES, A. C. G.; CORREIA, M. E. F. Caracterização da fauna edáfica em diferentes coberturas vegetais na região Norte-Fluminense. Revista Brasileira de Ciência do Solo, Viçosa, v. 29, p. 555-564, jul. 2003. MUSSURY, R. M.; SCALON, S. P. Q.; SILVA, S. V.; SOLIGO, F. R. Study of Acari and Collembola populations in four cultivation systems in Dourados – MS. Brazilian Archives of Biology and Technology, Curitiba, v. 45, n. 3, p. 257-264, sep. 2002. MYERS, N.; MITTERMEIER, R.A.; MITTERMEIER, C.G.; FONSECA, G.A.B.; KENT, J. Biodiversity hotspots for conservation priorities. Nature, Washington, v. 403, p. 853-858, feb. 2000. NEGRETE-YANKELEVICH, S.; FRAGOSO, C.; NEWTON, A. C.; HEAL, O. W. Successional changes in soil, litter and macroinvertebrate parameters following selective logging in a Mexican Cloud Forest. Applied Soil Ecology, Amsterdam, v. 35, n. 2, p. 340–355, feb. 2007. NEGRETE-YANKELEVICH, S.; FRAGOSO, C.; NEWTON, A.C.; RUSSELL, G.; HEAL, O.W. Spatial patchiness of litter, nutrients and macroinvertebrates during secondary succession in a Tropical Montane Cloud Forest in Mexico. Plant and Soil, Berlin, v. 286, p. 123-139, jul. 2006. ODUM, E. P. Ecologia. Rio de Janeiro, RJ: Guanabara Koogan, 1988. 434p. 455 Effects of eucalyptus... CAMARA, R.; CORREIA, M. E. F.; VILLELA, D. M. Biosci. J., Uberlândia, v. 28, n. 3, p. 445-455, May/June. 2012 OLIVEIRA, M. A.; DELLA LUCIA, T. M. C.; ARAUJO, M. S.; CRUZ, A.P. A fauna de formigas em povoamento de eucalipto e mata nativa no estado do Amapá. Acta Amazonica, Manaus, v. 25, n. 1/2, p. 117- 126, mai. 1995. RAINIO, J.; NIEMELÄ, J. Ground beetles (Coleoptera: Carabidae) as bioindicators. Biodiversity and Conservation, Berlin, v. 12, n. 3, p. 487–506, mar. 2003. SILVEIRA, J. M.; BARLOW, J.; LOUZADA, J.; MOUTINHO, P. Factors affecting the abundance of leaf- litter arthropods in unburned and thrice-burned seasonally-dry Amazonian Forests. PlosONE,v.5,n.9,2010.doi:http:/www.plosone.org/article/info%3Adoi%2F10.1371%2Fjournal.pone.0012877. Accessed April 30th, 2011. SOUZA, R. C.; CORREIA, M. E. F.; PEREIRA, M. G.; SILVA, E. M. R.; PAULA, R. R.; MENEZES, L. F. T. Estrutura da comunidade da fauna edáfica em fragmentos florestais na Restinga da Marambaia, RJ. Revista Brasileira de Ciências Agrárias, Recife, v. 3, n. 1, p. 49-57, jan./mar. 2008. TESCH, E. R. Produção de serapilheira em três plantios de eucalipto (Corymbia citriodora (Hook) LAS Johnson & KD Hill), de diferentes idades, com sub-bosque de mata nativa em regeneração, na Reserva biológica União, RJ. 2005. 33 f. Graduation Conclusion Work. Universidade Estadual do Norte Fluminense Darcy Ribeiro, Campos dos Goytacazes, RJ. 2005. VAN ACHTERBERG, K. (Ed.) The insects of Australia. 2ed. New York: Cornell University Press, 1991. v. 1 e 2. VILLELA, D. M.; NASCIMENTO, M. T.; MAZUREC, A. P.; GONÇALVES, G. M.; REZENDE, C. E. Soil chemical properties under Eucalyptus citriodora plantations of different ages after 9-year period of abandonment in União Biological Reserve, Rio de Janeiro State, Brazil. In: 3rd INTERNATIONAL CONFERENCE ON LAND DEGRADATION AND MEETING OF THE IUSS SUBCOMISSION C-SOIL AND WATER CONSERVATION, 2001, Rio de Janeiro. Anais… Rio de Janeiro: EMBRAPA, 2001. CD- ROM. VILLELA, D. M.; NASCIMENTO, M. T.; REZENDE, C. E.; NASCIMENTO, A. C.; MAZUREC, A. P.; TESCH, E. Effects of regeneration of native species under Eucalyptus plantations, after 6-yrs of abandonment, on nutrients concentrations and quantities of litter layer in União Biological Reserve, Rio de Janeiro State, Brazil. In: 4th INTERNATIONAL SYMPOSIUM ENVIRONMENTAL GEOCHEMISTRY IN TROPICAL COUNTRIES, 2004, Búzios. Anais… Niterói: UFF/Programa de Geoquímica, 2004. p. 202-205. WANG, Q.; WANG, S.; HUANG, Y. Comparisons of litterfall, litter decomposition and nutrient return in a monoculture Cunninghamia lanceolata and a mixed stand in southern China. Forest Ecology and Management, Amsterdam, v. 255, n. 3/4, p. 1210–1218, mar. 2008. WARREN, M. W.; ZOU, X. Soil macrofauna and litter nutrients in three tropical tree plantations on a disturbed site in Puerto Rico. Forest Ecology and Management, Amsterdam, v. 170, p. 161–171, oct. 2002. ZAR, J. H. Biostatistical Analysis. 3ed. New Jersey: Prentice Hall, 1984. 662 p.