SEARCH

SEARCH BY CITATION

Keywords:

  • Biodiversity;
  • Coleoptera;
  • forest regeneration;
  • insect conservation;
  • Mata Atlântica;
  • old-growth forest;
  • secondary forest;
  • soil type;
  • species density;
  • species richness

Abstract

  1. Top of page
  2. Abstract
  3. Introduction
  4. Methods
  5. Results
  6. Discussion
  7. Conclusions
  8. Acknowledgements
  9. References
  10. Appendix

Abstract.  1. As mature tropical forests disappear, secondary forests with their potential to conserve mature tropical forest species are increasingly of interest in a conservation context.

2. We investigated the recovery of litter inhabiting beetle diversity and composition during natural forest regeneration in the coastal submontane forest of Southern Brazil, using chronosequences on two different soil types: cambisol and gleysol. Secondary forests, ranging in ages from 5 to 50 years, as well as old-growth forests were studied. Beetles were sifted from leaf litter and extracted using the Winkler technique.

3. Young secondary forests had a very low species density and a significantly different and heterogeneous species composition compared to old-growth forests. During forest regeneration, species density greatly increased and the species composition of older secondary forests was similar to that of old-growth forests. The recovery pattern of species density and composition differed between soil types; nonetheless, they showed the same tendencies generally. Thus, mature secondary forests of about 35–50 years can be assumed to contribute substantially to the maintenance of forest beetle species.

4. Litter quantity was not only significantly correlated with species density; but, even reflected the density pattern of both soil types. Thus, litter quantity is an important factor for maintaining or recovering high beetle densities. The composition of beetle assemblages was strongly affected by soil type. Thus, soil type should be considered in regional biodiversity monitoring and conservation actions.


Introduction

  1. Top of page
  2. Abstract
  3. Introduction
  4. Methods
  5. Results
  6. Discussion
  7. Conclusions
  8. Acknowledgements
  9. References
  10. Appendix

A major threat to global biodiversity is the ongoing destruction of mature tropical forests (Dirzo & Raven, 2003). Although future deforestation rates and their consequence for species extinction is scientifically debated (Brook et al., 2006; Wright & Muller-Landau, 2006a,b; Gardner et al., 2007b; Laurance, 2007), it is widely agreed that the proportion of secondary forests to total forest area will further increase (Perz & Skole, 2003; Aide & Grau, 2004; FAO 2009). This trend makes it important to evaluate the potential of secondary forests to act as refuges for forest species (Lawton et al., 1998; Wright, 2005). However, data on the recovery of faunal assemblages during forest regrowth are still sparse and mostly confined to a few popular groups, such as birds and ants (e.g. Dunn, 2004; Sodhi et al., 2005; Silva et al., 2007; Bihn et al., 2008; but, see Basset et al., 2008). Prediction of changes in species richness, among faunal groups using indicator taxa, often fails (Prendergast, 1997; Lawton et al., 1998; Wolters et al., 2006; Barlow et al., 2007a; Basset et al., 2008); therefore, it is crucial to increase the database of faunal inventories and their response patterns (Schulze et al., 2004). This is especially true for tropical insect communities of highly specific microhabitats, such as leaf litter (Lewinsohn et al., 2005).

Beetles affect many important ecosystem processes in forests including litter decomposition, nutrient flow and food web regulation. They modulate their environment at different trophic levels being predators as well as decomposers. In tropical forests, beetles are particularly species rich and abundant (Hammond, 1990; Nadkarni & Longino, 1990; Didham et al., 1998; Stork & Grimbacher, 2006) and reflect the richness of insect communities (Moeed & Meads, 1985). However, litter inhabiting beetles of tropical forests have rarely been studied owing to their diminutive size and poor taxonomical description. Most available studies that examined the effect of habitat loss and modification on ground related beetles in neotropical regions, were conducted in the Amazonian rainforest and focused on dung beetles (Klein, 1989; Andresen, 2003; Spector & Ayzama, 2003; Feer & Hingrat, 2005; Gardner et al., 2008; but, see Didham et al., 1998; Uehara-Prado et al., 2009).

Forest succession is accompanied with an increase in litter fall (Ewel, 1976) and tree diversity (Liebsch et al., 2008), which accelerates the amount and complexity of leaf litter (Burghouts et al., 1992). An increase in quantity (Jonsson & Jonsell, 1999; Barberena-Arias & Aide, 2003) and complexity (Tews et al., 2004; Lassau et al., 2005) of inhabited substrate often positively affects beetle diversity and composition. It is frequently traced back to increased resource availability (Gotelli & Colwell, 2001) and an extensive number of habitable niches (Klopfer & MacArthur, 1960). Furthermore, macro-fauna in or on soils is dependent upon microclimatic conditions (Martius et al., 2004). In particular, soil moisture has a strong effect on species diversity and composition (Lassau et al., 2005).

We investigated the recovery pattern of litter inhabiting beetles during natural forest regeneration, in soils differing markedly in moisture content in the Mata Atlântica (Atlantic Forest) of Brazil. To the best of our knowledge no comparable study, examining the effect of forest succession and soil type on litter beetles, has been conducted in the Brazilian Atlantic Forest, one of the most threatened tropical forest biomes in the world. Migration, industrialisation and urban expansion have resulted in only 11–16% of the original forest area remaining in small fragments of mostly secondary forests (Ribeiro et al., 2009). Nevertheless, the Atlantic Forest biome still exhibits an enormous biodiversity, and its conservation is of extreme importance (Laurance, 2009). We addressed and tested the following hypotheses related to the response of litter inhabiting beetles to forest regeneration: (i) species density increases and species composition changes with forest age. (ii) Litter volume influences significantly species density and composition. (iii) Different soil types have different species composition and affect species density.

Methods

  1. Top of page
  2. Abstract
  3. Introduction
  4. Methods
  5. Results
  6. Discussion
  7. Conclusions
  8. Acknowledgements
  9. References
  10. Appendix

Study area and sites

The study was conducted in the coastal mountain range in Paraná, Southern Brazil, within the municipality of Antonina. The regional climate is classified according to Köppen as Cfa (humid subtropical, Peel et al., 2007), with an annual rainfall of 2000–3000 mm, a wet season from September to April and a dry season from May to August. The average annual temperature is 20° C. The study sites were located in the Cachoeira Nature Reserve, owned by the Brazilian NGO Society for Wildlife Research and Environmental Education (SPVS) (Fig. 1). The reserve is located in the submontane forest zone (0–600 m above sea level). The natural vegetation is classified as humid submontane forest (IBGE 1992). Forest disturbances were caused mainly by buffalo grazing, cash crop plantations and selective logging. This has led to a mosaic landscape of mature and different-aged secondary forests embedded in a matrix of small settlements, farms and pastures.

image

Figure 1.  Map of the study region, indicating the location of the study sites in the Rio do Cachoeira Reserve. Numbers indicate successional stages 1–4 (white circles: sites on cambisol, black circles: sites on gleysol).

Download figure to PowerPoint

We used a chronosequence approach to investigate the recovery of litter inhabiting beetles during forest regeneration. A chronosequence comprises three stages of secondary forest: Stage 1 (very young: ∼5 years after abandonment), Stage 2 (young: 12–15 years), Stage 3 (old: 35–50 years) and Stage 4 as a reference (old-growth forests: at least 100 years without anthropogenic impact). To investigate the influence of soil type on recovery patterns, chronosequences were studied on two contrasting soil types: cambisol and gleysol. Gleysols, unlike cambisols, are influenced by groundwater and have a seasonally high water level. Because the flat plains of the reserve were intensively anthropogenically used, old-growth forests are not found on the gleysol; therefore, they could not be included in the study design. Three replicate sites per forest stage/soil type combination were established and scattered throughout the reserve. The age after abandonment was estimated from information provided by long-time residents and from satellite photos taken in 1952, 1980 and 2002. Sites were located using local vegetation and soil data provided by the SPVS.

Sampling methods and beetle identification

Beetles were collected from June to July 2003 from 20 1-m2 leaf litter samples taken at each site using a 1-m2 frame. Samples were taken every 5 m along two parallel 50 m transects installed at least 50 m from the forest edge to minimise edge effects. The leaf litter was sieved through a 10-mm mesh. Beetles were extracted from the samples using the Winkler method (Besuchet et al., 1987); Winkler bags were suspended for 3 days, which was suitable for a comparative survey of litter inhabiting beetles (Krell et al., 2005). Leaf litter volume was measured by filling the coarse leaf litter in a graduated bucket, slightly compressing the foliage using a standard weight and then measuring the depth of the litter. Beetles were identified to the family level using the keys from Lawrence et al. (1999). Nine beetle families [Carabidae, Curculionidae (with the exception of Scolytinae), Staphylinidae, Leiodidae, Endomychidae, Hydrophilidae, Cerylonidae, Eucinetidae, and Tenebrionidae] were further sorted into morphospecies (Oliver & Beattie, 1996; Barrat et al., 2003) or species when possible. We refer to morphospecies as species. We chose these beetle families because: (i) they were sampled in high numbers. (ii) They are typical inhabitants of leaf litter. (iii) Taxonomists were able to study our material. We also differentiated between predators (Staphylinidae, Carabidae) and decomposers (Curculionidae, remaining five families). As we lacked data on the feeding behaviour of focal species, we determined trophic groups using data listed in Lawrence et al. (1999) and in the literature cited in Hanagarth and Brändle (2001). Accordingly, the decomposer group includes fungivorous, phytophagous, and saprophagous species. Voucher specimens were deposited in the Department of Zoology, University of Curitiba (UFPR).

Data analyses

Species data for all 20 sub-samples per site were pooled because individual catches were too small for reliable analyses. We compared species density rather than species richness between forest stages. This was due to the low species counts at several sites, which we considered a meaningful part of the response pattern. We standardised the observed species numbers by estimating total species numbers using an abundance-based non-parametric estimator (Jack 1) (EstimateS 8.0, Colwell, 2006). Patterns in species density were analysed conjointly for all beetle families and separately for Staphylinidae, Carabidae, Curculionidae and the remaining families using one-way analysis of variance (one-way anova) and Fisher’s LSD post hoc tests (SPSS 17.0.2, Chicago, IL, USA). Pearson correlations between species density of Staphylinidae, Carabidae, and Curculionidae were conducted to test for possible indicator groups reflecting overall species density. We examined the effect of litter volume, successional stage and soil type on species density with two-way anova (SPSS 17.0.2). The effect of litter volume on species density was examined in analyses with and without litter volume as covariate. Additionally, we compared species richness between old-growth forest and old secondary forest using sample based rarefaction curves (EstimateS 8.0). We calculated relative evenness of abundance and counted the number of species unique to each forest stage/soil type combination. Unique species are defined here as those species represented by at least two specimens in a successional stage/soil type combination and no specimens in other combinations. We tested for differences in species composition among forest stages on both soil types using the multiresponse permutation procedure (MRPP) and visualised pattern of similarity in beetle assemblage composition with non-metric multidimensional scaling (NMDS) ordination. This was based on square root transformed data and the Bray-Curtis distance measure (PCOrd version 4.01, McCune & Mefford, 1999). We used a permutational multivariate analysis of variance (PERMancova, Anderson, 2005) to examine the effect of successional stage (Stages 1–3), soil type and litter volume as covariate on an assemblage composition with 999 permutations of residuals in the full model, using square root transformed data and Bray-Curtis distances.

Results

  1. Top of page
  2. Abstract
  3. Introduction
  4. Methods
  5. Results
  6. Discussion
  7. Conclusions
  8. Acknowledgements
  9. References
  10. Appendix

Beetle fauna

A total of 3683 beetles, representing 35 families (Appendix 1), were collected from 420 m2 leaf litter. Dominant beetle families were staphylinids (52.5%), curculionids (13%), scydmaenids (9%) and carabids (9%) together representing 83.5% of total counts. Fifteen families were represented only as singletons or doubletons; 2181 specimens of nine beetle families were determined to 256 species. The most species rich families were staphylinids (159 species), curculionids (39), and carabids (23). Fifty-seven per cent of all species were recorded as singletons or doubletons. Species accumulation curves did not reach an asymptote. The estimate of total species number (34–77%) indicated a moderate level of completeness (Table 1).

Table 1.   Diversity and abundance of leaf litter beetles along successional stages in the Atlantic Forest of Southern Brazil.
ParameterSoil type and successional stage*
CambisolGleysol
Stage 1Stage 2Stage 3Stage 4Stage 1Stage 2Stage 3
  1. *Numbers represent different-aged forest stages comprising secondary forests of ∼5 years (stage 1), 12–15 years (stage 2), 35–50 years (stage 3), and old-growth forest (stage 4).

  2. †Means of three replicate sites (= 3). Sub-samples of each site were pooled. Number of species observed on 20 1-m2 plots of forest floor.

  3. ‡Estimated total number of species (on 20 1-m2 plots of forest floor) using the Jack 1 richness estimator with 100 randomisations without replacement.

  4. §Percentage of Jack 1 estimate compared to observed number of species. Completeness is stated for every replicate site.

Number of families†9.0 ± 2.69.7 ± 1.214.3 ± 4.215.3 ± 2.18.0 ± 29.3 ± 0.69.0 ± 1.0
Abundance (families)†60.3 ± 25.5106.0 ± 64.1348.0 ± 238.5390.3 ± 107.933.7 ± 8.1172.3 ± 37.1131.3 ± 77.2
Observed number of species†16.7 ± 3.220.3 ± 3.557.0 ± 16.662.0 ± 9.28.3 ± 0.633.3 ± 5.929.7 ± 11.8
Abundance (species)†38.7 ± 22.438.7 ± 16.5237.0 ± 182.3236.7 ± 101.212.3 ± 4.093.3 ± 26.670.3 ± 48.8
Estimated number of species‡25.8 ± 3.034.6 ± 4.585.5 ± 20.289.5 ± 9.414.0 ± 2.250.4 ± 12.747.4 ± 18.5
Unique species326 131 8 0
Completeness (%)§34/52/57 47/62/6156/64/56 66/75/7772/65/67 57/68/75 63/63/61
Evenness (J’)0.86 ± 0.130.92 ± 0.050.86 ± 0.040.87 ± 0.040.96 ± 0.030.88 ± 0.020.92 ± 0.06

Species density and richness

Species density increased with forest age (cambisol: = 0.001; gleysol: = 0.01; = 3; Fig. 2a). On cambisol, Stage 1 (very young) and Stage 2 (young secondary forest) did not differ significantly from each other (Fig. 2a). However, the total species density was convincingly lower than that of older forest stages (Fig. 2a). The species density of old secondary forest did not differ significantly from that of old-growth forest (Fig. 2a). The species density of Stage 1 was notably lower than that of Stages 2 and 3 on gleysol; on the other hand, the species density did not increase between Stage 2 and Stage 3 (Fig. 2). Predators (Fig. 2b, c) and decomposers (Fig. 2d, e) showed a similar pattern. We found meaningful effects of successional stage and soil type on total species density (Table 2a). When litter volume was added as covariate to the model, soil type no longer significantly affected total species density (Table 2b). Sample based rarefaction curves of species richness showed no notable difference between old-growth forest and Stage 3 (old secondary forest, Fig. 2f). Evennesses between successional stages were similar and ranged from 0.86 to 0.96 (anova, = 0.76, = 3; Table 1). The staphylinid density pattern showed the best correlation to overall species density (r = 0.93, < 0.001).

image

Figure 2.  Patterns of species density (a–e) and species richness (f) of secondary and old-growth forests. The mean estimated species density of different-aged secondary forests (stages 1–3) and old-growth forest (stage 4) were compared for all species combined (a) and for only staphylinids (b), carabids (c), curculionids (d), and for less-abundant beetle families belonging to the decomposer group (hydrophilids, tenebrionids, eucinetids, endomychids, leiodids, cerylonids) in a joint plot (e). Stages on cambisol (•) and gleysol (Δ) were analysed separately. Stages (= 3) were tested among each other for statistical significance (LSD tests, ≤ 0.05). In a–e, different letters indicate different means. (f) Sample based rarefaction curves of mature secondary forest (stage 3) and old-growth forest on cambisol, calculated for all three sites combined.

Download figure to PowerPoint

Table 2.   Results of two-way anova on the effect of soil type and successional stage on species density. The effect of litter quantity was evaluated by calculating the effects of soil type and successional stage without considering litter quantity in the model (b) and by adding litter volume as covariate (a).
Source of variationSS (type I)d.f.MSFP
(a)
Soil type4168.014168.018.80.001
Successional stage8843.532947.813.3<0.001
Soil type × successional stage2165.321082.64.90.026
Error2883.413221.8  
(b)
Litter volume14702.7114202.7115.1<0.001
Soil type9.319.30.10.970
Successional stage1343.43447.73.50.010
Soil type × successional stage471.32235.61.80.020
Error1533.612127.8  

Litter volume

The mean leaf litter volume per site between samples and within replicates was highly variable. Litter volume changed significantly during forest regeneration (= 0.04, = 3; Fig. 3). The mean leaf litter volume of young secondary forests was lower than that of old secondary forests and old-growth forest. Litter volume was lower at gleysol sites than at cambisol sites, except for Stage 2. The increasing litter volume and increasing species density patterns were highly consistent with regard to successional stage and soil type.

image

Figure 3.  Box plots of leaf litter volume per m2 in different successional stage/soil type combinations in the Atlantic Forest of Brazil. The central horizontal line in the box marks the median of the values; the box edges the first and third quartile. The inter-quartile range within the box includes the central 50% of the values. The whiskers show the range of observed values that are not within the first and third quartile but not further away than 1.5 times the inter-quartile range from the hinges. Crosses are the arithmetic mean. Each box contains 20 values of three replicate sites, making a total of 60 values.

Download figure to PowerPoint

Beetle assemblage composition

The species composition of litter inhabiting beetle assemblages differed among successional stages (MRPP, cambisol: = 0.015; gleysol: = 0.01; Fig. 3). Multidimensional scaling ordination grouped sites on gleysol separately from sites on cambisol (Fig. 4). Young forests (Stages 1 and 2) showed high heterogeneity. On cambisol, the assemblage composition of Stages 1 and 2 differed significantly from that of Stage 3 and old-growth forest (Stage 4; MRPP, = 0.03). The assemblage composition of Stages 3 and 4 was less variable among sites and did not differ from each other (MRPP, = 0.89). On gleysol, the assemblage composition of Stage 1 differed from that of Stages 2 and 3 (MRPP, = 0.02). The assemblage composition was significantly affected by soil type (= 0.004), successional stage (= 0.035), as well as litter volume (= 0.001).

image

Figure 4.  Non-metric multidimensional scaling (NMDS) ordination of the leaf litter beetle assemblages, according to successional stage and soil type. Species are indicated with crosses. Successional stage/soil type combinations grouped closer together are more similar in species composition.

Download figure to PowerPoint

Discussion

  1. Top of page
  2. Abstract
  3. Introduction
  4. Methods
  5. Results
  6. Discussion
  7. Conclusions
  8. Acknowledgements
  9. References
  10. Appendix

Patterns of species density and richness

The species density of leaf litter beetles in old-growth forests was much higher than that of secondary forests, 5–15 years after abandonment. This reveals a clear negative effect of deforestation on the diversity of the selected beetle families, as reported for many other taxa (e.g. Lawton et al., 1998; Nichols et al. 2007; Bihn et al., 2008). Moreover, the very low number of species in young forests, mostly found as singletons, demonstrates the unsuitability of these habitats for beetles inhabiting this niche in mature forests as well as for species well adapted to open habitats. Larger open habitats are not a natural component of the landscape; therefore, the invasion of open habitat species in deforested sites probably influences the recolonisation of leaf litter beetles very little in the area studied.

Old secondary forests of about 35–50 years already had species densities and richness similar to that of old-growth forest, indicating a rapid recovery during further forest regeneration. This result supports the conclusion of Dunn (2004) and Grimbacher et al. (2007) that species richness is the component of diversity with the highest recovery ability.

The recovery patterns of predators and decomposers did not differ significantly (Fig. 2b–e) with an almost linear relationship between their densities (see Gaston et al., 1992). A direct predator/prey interaction seems insufficient to explain this pattern, as the abundance of predators clearly exceeds that of decomposers. The pattern can best be explained by a general cascading effect of lower trophic levels on the diversity of higher trophic levels driven by litter quantity (Barberena-Arias & Aide, 2003).

We found Staphylinidae to be the most abundant and species rich beetle family by far in our study sites, which is also found in nearby temperate forests (Marinoni & Ganho, 2003) and the Amazonian region (Didham et al., 1998; Hanagarth & Brändle, 2001). The pattern of staphylinid density observed was strongly correlated with the pattern of overall beetle density. Thus, although their taxonomy is notoriously difficult, staphylinids may be a good biodiversity indicator of beetle assemblages in tropical forests.

Recovery of assemblage composition

Patterns of significant changes in species composition during forest regeneration were comparable to those of species density (Figs 2 and 3). Compared to the assemblages of mature forests, the assemblages of young forests were more similar to each other; however, the initial post-disturbance assemblages of the young forests still varied greatly. We suggest that this heterogeneity is caused by variable recolonisation scenarios, which are affected by differing vegetation structures. These in turn influence microclimatic conditions and litter quantity (Liebsch et al., 2007), by proximity of native habitats (Pawson et al., 2008) and by disturbance history (Saint-Germain et al., 2005). Old secondary forests varied less in composition and were not distinguishable from old-growth forests. Grimbacher et al. (2007) found similar results; possible reasons for these observations were given as a longer time for beetle accumulation, a greater structural habitat complexity (Lassau et al., 2005) and larger plant species richness (Haddad et al., 2001). However, comparable studies still found large differences between old secondary forests and old-growth forests, emphasising a much longer time span for the recovery of ant (Dunn, 2004; Bihn et al., 2008), amphibian/lizard (Gardner et al., 2007a) and bird assemblages (Dunn, 2004; Barlow et al., 2007b). We suggest four explanations for the fast recovery of leaf litter beetle assemblages, observed in our study. First, many litter inhabiting beetles are volant or have a high surface mobility, allowing them to disperse well. Second, the short generation time of beetles promotes rapid recolonisation of suitable habitats. Third, a quantity of leaf litter comparable to that of old-growth forest offers adequate microhabitats for most forest species. Fourth, large old-growth forest patches, which still exist in our study area, could serve as species sources for secondary forests, which feature conditions already suitable for forest species.

Sample adequacy and rare species

Rare species are an integral part of tropical insect assemblages (Novotny & Basset, 2000) as shown in many beetle studies in tropical forests (e.g. see Didham et al., 1998; Grimbacher et al., 2007). We only reached a moderate degree of sample completeness with many singletons, making it difficult to distinguish between random catches and distribution patterns of rare species. However, the reliability of our findings is supported by an almost identical pattern of additional chronosequences in a nearby reserve (only on cambisol), despite seasonal and spatial differences in sampling. Nevertheless, we found at least 13 ‘unique’ species in old-growth forests that could not be statistically confirmed as indicators of old-growth forests. We suggest that probably more rare beetle species will be lost through deforestation than short-term studies are able to detect. Therefore, we stress the importance of maintaining old-growth forests to protect forest biodiversity.

Effect of soil type on the recovery pattern

The soil type strongly influenced the recovery pattern of species density and composition. Lower species densities in old secondary forests on gleysol compared to cambisol indicate that the harsh conditions on gleysol may restrict species establishment. Other studies have shown that high soil moisture negatively affects beetle diversity by influencing adult habitat selection and reproduction (Doube, 1983; Vessby & Wiktelius, 2003). However, the surprisingly similar pattern of species density and litter volume indicates that the amount of litter may be far more important for explaining the species density pattern than soil moisture. This assumption is supported by the observation that little additional variance is explained when leaf litter is added to the model (Table 2). Thus, soil type seems to affect species density indirectly by affecting litter quantity. Seasonal flooding that occurs on the gleysol sites may restrict the development of deep and complex litter layers; thereby, reducing the number of species, as reported for spiders (Uetz, 1976). However, soil type significantly affected assemblage composition even when litter volume was added to the model (Fig. 3). This indicated that the composition of assemblages contains information not reflected in species diversity metrics. A convergence towards more similar assemblages in older stages suggests that the major difference in assemblage composition could be confined to the recolonisation process. This signifies that pioneers on gleysol and cambisol differ and fewer mature forest species occur on gleysol than on cambisol.

Conclusions

  1. Top of page
  2. Abstract
  3. Introduction
  4. Methods
  5. Results
  6. Discussion
  7. Conclusions
  8. Acknowledgements
  9. References
  10. Appendix

The study established that beetle species density increases and assemblage composition changes during forest regeneration. However, only mature secondary forests of 35–50 years seem to be suitable habitats for most litter inhabiting beetle species. These mature secondary forests can be considered to contribute substantially to the maintenance of forest species, at least when old-growth forests remain nearby. Younger forests, up to 15 years after abandonment, showed low species densities even though they are situated in the immediate vicinity of an old-growth forest and feature an almost forest like structure.

Litter quantity was strongly correlated with species density and seems to reflect species density on both gleysol and cambisol soils. Thus, litter volume may be an important aspect of priority sites for conservation if the goal is to maintain a high density of beetle species. It is likely that insects will rarely be the primary target of future regional conservation strategies; thereby, causing litter quantity to be a valuable interface between the preservation of biotopes and the conservation of insects. However, it is debatable whether or not the addition of leaf litter, in initial regeneration stages, is an efficient tool for accelerating the recovery of leaf litter beetles. Nakamura et al. (2009) mentioned positive effects of mulching for the recolonisation of ants and points out the necessity of a fully closed canopy to suppress the invasion by pastoral species. In our study region a competition with pastoral species does not seem to limit the recolonisation of forest species; therefore, addition of leaf litter could be efficient even in the initial stages, when the canopy is not yet closed. However, the quantity of habitable substrate was not in itself sufficient to predict the structure of litter inhabiting beetle assemblages. Conditions related to soil type, especially if the soils differ dramatically, must be considered if highly diverse soil-related insect communities, such as beetles, are to be integrated into conservation strategies.

Acknowledgements

  1. Top of page
  2. Abstract
  3. Introduction
  4. Methods
  5. Results
  6. Discussion
  7. Conclusions
  8. Acknowledgements
  9. References
  10. Appendix

We thank the SPVS for access to the study sites and for field work assistance. Special thank goes to Volker Brachat, Martin Baehr, Germano Rosado-Neto, Roland Grimm, Alexander Riedel, Ulrich Irmler, and Volker Puthz for support in beetle identification. The study was embedded in the Project Solobioma, funded by the German Ministry of Education and Research (01LB0201) and the Brazilian Conselho Nacional de Desenvolvimento Científico e Tecnológico (160611/IBAMA reg.: 1920414). We are indebted to Yves Basset, Owen Lewis and two anonymous reviewers for constructive comments that greatly improved an earlier version of this manuscript.

References

  1. Top of page
  2. Abstract
  3. Introduction
  4. Methods
  5. Results
  6. Discussion
  7. Conclusions
  8. Acknowledgements
  9. References
  10. Appendix
  • Aide, T.M. & Grau, H.R. (2004) Globalization, migration and Latin American ecosystems. Science, 30, 5191551916.
  • Anderson, M.J. (2005) PERMANOVA: A FORTRAN Computer Program for Permutational Multivariate Analysis of Variance. Department of Statistics, University of Auckland, New Zealand.
  • Andresen, E. (2003) Effect of forest fragmentation on dung beetle communities and functional consequences for plant regeneration. Ecography, 26, 8797.
  • Barberena-Arias, M.F. & Aide, T.M. (2003) Species diversity and trophic composition of litter insects during plant secondary succession. Caribbean Journal of Science, 2, 161169.
  • Barlow, J., Gardner, T.A., Araujo, T.S., Avila-Pires, T.C., Bonaldo, A.B., Costa, J.E., Esposito, M.C., Ferreira, L.V., Hawes, J., Hernandez, M.I.M., Hoogmoed, M.S., Leite, R.N., Lo-Man-Hung, R.F., Malcolm, J.R., Martins, M.B., Mestre, L.A.M., Miranda-Santos, R., Nunes-Gutjahr, A.L., Overal, W.L., Parry, L., Peters, S.L., Ribeiro-Junior, M.A., Da Silva, M.N.F., Da Silva-Motta, C. & Peres, C.A. (2007a) Quantifying the biodiversity value of tropical primary, secondary and plantation forests. Proceedings of the National Academy of Science of the United States of America, 104, 1855518560.
  • Barlow, J., Mestre, L.A.M., Gardner, T.A. & Peres, C.A. (2007b) The value of primary, secondary and plantation forests for Amazonian birds. Biological Conservation, 136, 212231.
  • Barrat, B.I.P., Deraik, J.G.B., Rufaut, G.B., Goodman, A.J. & Dickinson, K.J.M. (2003) Morphospecies as a substitute for Coleoptera species identification, and the value of experience in improving accuracy. Journal of the Royal Society of New Zealand, 33, 583590.
  • Basset, Y., Missa, O., Alonso, A., Miller, S.E., Curletti, G., DeMeyer, M., Eardley, C., Lewis, O.T., Mansell, M.W., Novotny, V. & Wagner, T. (2008) Changes in arthropod assemblages along a wide gradient of disturbance in Gabon. Conservation Biology, 22, 15521563.
  • Besuchet, C., Burckhardt, D.H. & Löbl, I. (1987) The ‘Winkler/Moczarski’ eclector as efficient extractor for fungus and litter Coleoptera. The Coleopterists Bulletin, 41, 392394.
  • Bihn, J., Verhaagh, M. & Brändle, M. (2008) Do secondary forests act as refuges for old-growth forest animals? Recovery of ant diversity in the Atlantic forest of Brazil. Biological Conservation, 141, 733743.
  • Brook, B.W., Bradshaw, J.A., Koh, L.P. & Sodhi, N.S. (2006) Momentum drives the crash: mass extinction in the tropics. Biotropica, 38, 302305.
  • Burghouts, T., Ernsting, G., Korthals, G. & DeVries, T. (1992) Litterfall, leaf litter decomposition and litter invertebrates in primary and selectively logged dipterocarp forest in Sabah, Malaysia. Philosophical Transactions: Biological Sciences, 335, 407416.
  • Colwell, R.K. (2006) EstimateS: statistical estimation of species richness and shared species from samples. version 8. persistent Available from URL: http://purl.oclc.org/estimates.
  • Didham, R.K., Hammond, P.M., Lawton, J.H., Eggleton, P. & Stork, N.E. (1998) Beetle species responses to tropical forest fragmentation. Ecological Monographs, 68, 295323.
  • Dirzo, R. & Raven, P.H. (2003) Global state of biodiversity and loss. Annual Review of Environment and Resources, 28, 137167.
  • Doube, B.M. (1983) The habitat preference of some bovine dung beetles (Coleoptera: Scarabaeidae) in Hluhluwe Game Reserve, South Africa. Bulletin of Entomological Research, 73, 357371.
  • Dunn, R.R. (2004) Recovery of faunal communities during tropical forest regeneration. Conservation Biology, 18, 302309.
  • Ewel, J.J. (1976) Litterfall and leaf decomposition in a tropical forest succession in Eastern Guatemala. Journal of Ecology, 64, 293308.
  • FAO (2009) State of the World’s Forests. Food and Agriculture Organisation, United Nations, Rome.
  • Feer, F. & Hingrat, Y. (2005) Effects of forest fragmentation on a dung beetle community in French Guiana. Conservation Biology, 19, 11031112.
  • Gardner, T.A., Barlow, J. & Parry, L.W. (2007b) Predicting the uncertain future of tropical forest species in a data vacuum. Biotropica, 39, 2530.
  • Gardner, T.A., Malva, I.M., Hernández, M.I.M., Barlow, J. & Peres, C.A. (2008) Understanding the biodiversity consequences of habitat change: the value of secondary and plantation forests for neotropical dung beetles. Journal of Applied Ecology, 45, 883893.
  • Gardner, T.A., Ribeiro-Junior, M.A., Barlow, J., Avila-Pires, T.C.S., Hoogmoed, M.S. & Peres, C.A. (2007a) The value of primary, secondary, and plantation forests for a neotropical herpetofauna. Conservation Biology, 21, 775785.
  • Gaston, K.J., Warren, P.H. & Hammond, P.M. (1992) Predator: non-predator ratios in beetle assemblages. Oecologia, 90, 417421.
  • Gotelli, N.J. & Colwell, R.K. (2001) Quantifying biodiversity: procedures and pitfalls in the measurement and comparison of species richness. Ecology Letters, 4, 379391.
  • Grimbacher, P.S., Caterall, C.P., Kanowski, J. & Proctor, H.C. (2007) Responses of ground-active beetle assemblages to different styles of reforestation on cleared rainforest land. Biodiversity and Conservation, 16, 21672184.
  • Haddad, N.M., Tilman, D., Haarstadt, J., Ritchie, M. & Knops, J.M.A. (2001) Contrasting effects of plant richness and competition on insect communities: a field experiment. American Naturalist, 158, 1735.
  • Hammond, P.M. (1990) Insect abundance and diversity in the Dumoga-Bone National Park, N. Sulawesi, with special reference to the beetle fauna of lowland rain forests in the Toraut region. Insects and the Rain Forest of South-East Asia (Wallacea) (ed. by W.J.Knight and J.D.Holloway), pp. 197254. Royal Entomological Society of London, London, UK.
  • Hanagarth, W. & Brändle, M. (2001) Soil beetles (Coleoptera) of a primary forest, secondary forest and two mixed polyculture systems in central Amazonia. Andrias, 15, 155162.
  • Instituto Brasileiro de Geografia e Estatística IBGE (1992) Manual Técnico da Vegetação Brasileira. Série Manuais Técnicos em Geosciencias. Centro de Documentação e Disseminação de Informações (CDDI), Rio de Janeiro, Brazil.
  • Jonsson, B.G. & Jonsell, M. (1999) Exploring potential biodiversity indicators in boreal forests. Biodiversity and Conservation, 8, 14171433.
  • Klein, B.C. (1989) Effects of forest fragmentation on dung and carrion beetle communities in central Amazonia. Ecology, 70, 17151725.
  • Klopfer, P.H. & MacArthur, R. (1960) Niche size and faunal diversity. American Naturalist, 94, 293300.
  • Krell, F.T., Chung, A., DeBoise, E., Eggleton, P., Giusti, A., Inward, K. & Krell-Westerwalbesloh, S. (2005) Quantitative extraction of macro-invertebrates from temperate and tropical leaf-litter and soil: efficiency and time-dependent taxonomic biases of the Winkler extraction. Pedobiologia, 49, 175186.
  • Lassau, S.A., Hochuli, D.F., Cassis, G. & Reid, C.A.M. (2005) Effects of habitat complexity on forest beetle diversity: do functional groups respond consistently? Diversity and Distribution, 11, 7382.
  • Laurance, W.F. (2007) Have we overstated the tropical biodiversity crisis? Trends in Ecology and Evolution, 22, 6570.
  • Laurance, W.F. (2009) Conserving the hottest of the hotspots. Biological Conservation, 142, 1137.
  • Lawrence, J.F., Hastings, A.M., Dallwitz, M.J., Paine, T.A. & Zurcher, E.J. (1999) Beetles of the World, IntKey. version 5.09. Division of Entomology, CSIRO, Canberra, Australia.
  • Lawton, J.H., Bignell, D.E., Bolton, B., Bloemers, G.F., Eggleton, P., Hammond, P.M., Hodda, M., Holt, R.D., Larson, T.B., Mawdsley, N.A., Stork, N.E., Srivastava, D.S. & Watt, A.D. (1998) Biodiversity inventories, indicator taxa and effects of habitat modification in tropical forest. Nature, 391, 7276.
  • Lewinsohn, T.M., Freitas, A.V.L. & Prado, P.I. (2005) Conservation of terrestrial invertebrates and their habitats in Brazil. Conservation Biology, 19, 640645.
  • Liebsch, D., Goldenberg, R. & Marques, M.C.M. (2007) Florística estrutura de comunidades vegetais em uma cronoseqűência de Floresta Atlântica no estado do Paraná, Brasil. Acta Botanica Brasilica, 21, 983992.
  • Liebsch, D., Marques, M.C.M. & Goldenberg, R. (2008) How long does the Atlantic rain forest take to recover after a disturbance? Changes in species composition and ecological features during secondary succession Biological Conservation, 141, 17171725.
  • Marinoni, R.C. & Ganho, N.G. (2003) Fauna de coleopterano Parque estadual de Vila Velha, Ponta Grossa, Paraná, Brasil Abundância e riqueza das familias capturadas atraves de armadilhas de solo. Revista Brasileira de Zoologia, 20, 737744.
  • Martius, M., Höfer, H., Garcia, M.V.B., Römbke, J. & Hanagarth, H. (2004) Litter fall, litter stocks and decomposition rates in rainforest and agroforestry sites in central Amazonia. Nutrient Cycling in Agroecosystems, 68, 137154.
  • McCune, B. & Mefford, M.J. (1999) Multivariate Analyses of Ecological Data, version 4.01. MJM software, Gleneden Beach, Oregon.
  • Moeed, A. & Meads, M.J. (1985) Seasonality of pitfall trapped invertebrates in three types of native forest, Orongorongo Valley, New Zealand. New Zealand Journal of Zoology, 12, 1753.
  • Nadkarni, N.M. & Longino, T. (1990) Invertebrates in canopy and ground organic matter in a neotropical montane forest, Costa Rica. Biotropica, 22, 286289.
  • Nakamura, A., Caterall, C.P., Burwell, C.J., Kitching, R.L. & House, A.P.N. (2009) Effects of shading and mulch depth on the colonization of habitat patches by arthropods of rainforest soil and litter. Insect Conservation and Diversity, 2, 121131.
  • Nichols, E., Larsen, T., Spector, S., Davis, A.L., Escobar, F., Favila, M., Vulinec, K. & The Scarabaeinae Research Network (2007) Global dung beetle response to tropical forest modification and fragmentation: a quantitative literature review and meta-analysis. Biological Conservation, 137, 119.
  • Novotny, V. & Basset, Y. (2000) Rare species in communities of tropical insect herbivores: pondering the mystery of singletons. Oikos, 89, 564572.
  • Oliver, I. & Beattie, A.J. (1996) Designing a cost effective invertebrate survey: a test of methods for rapid biodiversity assessment. Ecological Application, 6, 594607.
  • Pawson, S.M., Brockerhoff, E.G., Meenken, E.D. & Didham, R.K. (2008) Non-native plantation forests as alternative habitat for native forest beetles in a heavily modified landscape. Biodiversity and Conservation, 17, 11271148.
  • Peel, M.C., Finlayson, B.L. & McMahon, T.A. (2007) Updated world map of the Köppen-Geiger climate classification. Hydrology and Earth System Sciences, 11, 163316.
  • Perz, S.G. & Skole, D.L. (2003) Secondary forest expansion in the Brazilian Amazon and the refinement of forest transition theory. Society and Natural Resources, 16, 277294.
  • Prendergast, J.R. (1997) Species richness covariance in higher taxa: empirical tests of the biodiversity indicator concept. Ecography, 20, 210216.
  • Ribeiro, M.C., Metzger, J.P., Martensen, A.C., Ponzoni, F.J. & Hirota, M.M. (2009) The Brazilian Atlantic Forest: how much is left, and how is the remaining forest distributed? Implications for conservation Biological Conservation, 142, 11411153.
  • Saint-Germain, M., Larrivee, M., Drapeau, P., Fahrig, L. & Buddle, C.M. (2005) Short-term response of ground beetles (Coleoptera: Carabidae) to fire and logging in a spruce-dominated boreal landscape. Forest Ecology and Management, 212, 118126.
  • Schulze, C.H., Waltert, M., Kessler, P.J.A., Pitopang, R., Shahabuddin, Veddeler, D., Mühlenberg, M., Gradstein, S.R., Leuschner, C., Steffan-Dewenter, I. & Tscharntke, T. (2004) Biodiversity indicator groups of tropical land-use systems: comparing plants, birds and insects. Ecological Application, 14, 13211333.
  • Silva, R.R., Machado Feitosa, R.S. & Eberhardt, F. (2007) Reduced ant diversity along a habitat regeneration gradient in the southern Brazilian Atlantic Forest. Forest Ecology and Management, 240, 6169.
  • Sodhi, N.S., Koh, L.P., Prawiradilaga, D.M.DarjonoTinulele, I.Putra, D.D. & Tan, T.H.T. (2005) Land use and conservation value for forest birds in Central Sulawesi (Indonesia). Biological Conservation, 122, 547558.
  • Spector, S. & Ayzama, S. (2003) Rapid turnover and edge effects in dung beetle assemblages (Scarabaeidae) at a Bolivian neotropical forest-savanna ecotone. Biotropica, 35, 394404.
  • Stork, N.E. & Grimbacher, P.S. (2006) Beetle assemblages from an Australian tropical rainforest show that the canopy and the ground strata contribute equally to biodiversity. Proceedings of the Royal Society of London, Series B, 273, 19691975.
  • Tews, J., Brose, U., Grimm, V., Tielbörger, K., Wichmann, M.C., Schwager, M. & Jeltsch, F. (2004) Animal species diversity driven by habitat heterogeneity/diversity: the importance of keystone structures. Journal of Biogeography, 31, 7992.
  • Uehara-Prado, M., Fernandes, J.O., Bello, A.M., Machado, G., Santos, A.J., Vaz-de-Melo, F.Z. & Freitas, A.V.L. (2009) Selecting terrestrial arthropods as indicators of small-scale disturbance: a first approach in the Brazilian Atlantic forest. Biological Conservation, 142, 12201228.
  • Uetz, G.W. (1976) Gradient analysis of spider communities in a streamside forest. Oecologia, 22, 373385.
  • Vessby, K. & Wiktelius, S. (2003) The influence of slope aspect and soil type on immigration and emergence of some northern temperate dung beetles. Pedobiologia, 47, 3951.
  • Wolters, V., Bengtsson, J. & Zaitsev, A.S. (2006) Relationship among the species richness of different taxa. Ecology, 87, 18861895.
  • Wright, S.J. (2005) Tropical forests in changing environment. Trends in Ecology and Evolution, 20, 553560.
  • Wright, S.J. & Muller-Landau, H.C. (2006a) The future of tropical forest species. Biotropica, 38, 287301.
  • Wright, S.J. & Muller-Landau, H.C. (2006b) The uncertain future of tropical forest species. Biotropica, 38, 443445.

Appendix

  1. Top of page
  2. Abstract
  3. Introduction
  4. Methods
  5. Results
  6. Discussion
  7. Conclusions
  8. Acknowledgements
  9. References
  10. Appendix

Appendix 1

Beetle families and their abundances found in different successional stages (stage 1: ∼5 years; stage 2: 12–15 years; stage 3: 35–50 years after abandonment and stage 4: old-growth forest) in the Rio do Cachoeira Reserve, Paraná, Brazil.

Beetle familySoil type and successional stage
CambisolGleysol
Stage 1Stage 2Stage 3Stage 4Stage 1Stage 2Stage 3
Staphylinidae6919655256267287220
Curculionidae391813214567367
Scydmaenidae13109914872640
Carabidae15913612413023
Ptiliidae124517543526
Hydrophilidae31332843117
Eucinetidae16191813
Chrysomelidae131371252
Tenebrionidae62915162
Cerylonidae215127
Leiodidae11314111
Nitidulidae2221321
Endomychidae118
Coccinellidae1261
Hydraenidae314
Scarabaeidae22
Corylophidae12
Zopheridae21
Elateridae111
Melandryidae12
Anthicidae11
Scirtidae11
Cerambycidae11
Ptilodactylidae11
Lagriidae2
Languridae1
Limnichidae1
Laemophloidae1
Erotylidae1
Trogossitidae1
Cneoglossidae1
Clambidae1
Dytiscidae1
Lycidae1
Lampyridae1
Families15152023151414
Abundance17930810451169101487394