Epigeic soil arthropod abundance under different agricultural land uses

The study of soil arthropods can provide valuable information how ecosystems respond to different management practices. The objective was to assess the total abundance, richness, and composition of epiedaphic arthropods in different agrosystems from southwestern Spain. Six sites with different agricultural uses were selected: olive grove, vineyards, olive grove with vineyards, wheat fields, fallows (150-300 m long), and abandoned vineyards. Crops were managed in extensive. Field margins were used as reference habitats. At the seven sites a total of 30 pitfall traps were arranged in a 10 × 3 grid. Traps were arranged to short (SD, 1 m), medium (MD, 6 m) and large (LD, 11 m) distance to the field margins in the middle of selected plots. Pitfall traps captured a total of 11,992 edaphic arthropods belonging to 11 different taxa. Soil fauna was numerically dominated by Formicidae (26.60%), Coleoptera (19.77%), and Aranae (16.76%). The higher number of soil arthropods were captured in the field margins followed by the abandoned vineyard. Significant differences were found between sites for total abundance, and zones. However, no significant differences for total abundance were found between months (April-July). Richness and diversity was highest in field margins and abandoned vineyards. Significant differences were found for these variables between sites. Our results suggest that agricultural intensification affects soil arthropods in Tierra de Barros area, a taxonomic group with an important role in the functioning of agricultural ecosystems. Additional key words: abundance; agrosystems; diversity; field margins.


Material and methods
Fieldwork was carried out in Tierra de Barros area (1.419 km²) near the city of Almendralejo (southwestern Spain, 38° 41' 26'' N / 6° 24' 43'' W, 337 m a.s.l).The climate is typically Continental-Mediterranean with relatively cold wet winters and dry hot summers (mean temperature: 16.3ºC, rainfall: 432 mm yr -1 ).Its flat to gently undulating landscape is dominated by a mosaic of dry winter cereal crops (wheat, Triticum aestivum, and barley, Hordeum vulgare), olive groves (Olea europaea), and vineyards (Vitis vinifera).Cereal crops occupied up to 2071 ha (13.72% of the total area), vineyards covered 7594 ha (50.32% of the total area) and olive groves extended over 4624 of the total area ha (30.64% of the total area).The remaining area corresponded to minor crops (mainly fruit trees), fallows of variable ages, dry pastures, river vegetation and villages.In this area natural habitats are only represented by the filed margins and some patches of riparian vegetation.
The sampling was done monthly between April and July of 2006.Six sites with different agricultural uses were selected: olive grove, vineyards, olive grove with vineyards, wheat fields, fallows (150-300 m long), and abandoned vineyards.All crops were managed in extensive.As field margins are used as reference habitats, in this study a band of 30 × 500 m located near the A6 highway was used as field margin.In this zone vegetation is composed mainly by Gramineae, Leguminoseae, Asteraceae and Rosaceae.Habitat complexity was enhanced by the presence of stones and agricultural debris.
At the seven sites a total of 30 pitfall traps (plastic jar, diameter = 30 cm, height = 15 cm) filled with a 3% formalin solution (Pekár, 2002) and detergent (~1 mL) were arranged in a 10 × 3 grid (Fig. 1).Columns were arranged to short (SD, 1 m), medium (MD, 6 m) and large (LD, 11 m) distance to the field margins in the middle of selected plots, according to Kennedy et al. (2001) and Buchholz et al. (2010).Traps were collected after 24 h.After each sampling, arthropods were sorted and preserved in ethyl alcohol (70%).

Introduction
Agricultural use covers about or ca.40% of the European land surface, with values up to 70% in some areas (Hails, 2002).Nowadays, various stakeholders request nonfood services from agricultural areas (e.g.hunting, tourism, leisure, production of renewable energy, biodiversity conservation) and, in general, society expects the agricultural landscape to be aesthetically pleasant and environmentally healthy (Brandt et al., 2000).Conversion of natural vegetation into agroecosystems and agri culture intensification, have profound impact on soil communities because they involve changes within the primary determinants of soil biodiversity, e.g.vegetation and soil microclimate (Wall et al., 2001;Decaëns & Jiménez, 2002;Gill et al., 2011).
There have been numerous reports of widespread negative impacts on local flora and fauna due to agricultural management strategies in several countries (Landis et al., 2000;Sotherton & Self, 2000;Letourneau & Goldstein, 2001;Vickery et al., 2001;Moreby et al., 2006).This reduction in biodiversity may be related both to the loss of habitats and to the degradation of remaining habitats.Semi-natural habitats within agroecosystems, such as woody hedgerows and field margins, typically support a wider variety of plants than adjacent crop fields (Boutin & Jobin, 1998;Boutin et al., 2002).In contrast to the impoverished environment of cultivated fields, marginal habitats may provide homes for several groups of arthropods by contributing to a stable structural habitat and a consistent food source (Duelli et al., 1990;Dennis & Fry, 1992).
While fostering arthropod populations in agricultural environments can be achieved by maintaining semi-natural areas adjacent to crop fields or maintaining healthy plant diversity within fields, the use of pesticides on crops may adversely affect arthropod populations (Sotherton et al., 1988).
Biodiversity in agricultural habitats is influenced by the surrounding landscape.The relationship between local species richness and the regional landscape has been addressed for several groups of plants and arthropods in Europe (e.g.Roschewitz et al., 2005;Schmidt et al., 2005).In general, more complex landscapes serve to increase the regional species pool, which translates into a higher biodiversity in crop fields and margins.
The objective of this study was to measure the effect of different agricultural soil uses on arthropod richness, abundance, and composition in a highly exploited region from an agricultural point view as is Tierra de Barros in the south-western Spain.Epigeic arthropod abundance in agrosystems months were compared by a one-way ANOVA.Post hoc comparisons of means were done using the Tukey test.The Z-test for two proportions was used to compare the abundance of arthropods between sites.This analysis was performed using SPSS 19.0 package for Windows (SPSS Inc.USA).For each group, taxa diversity and evenness were calculated following Shannon and Pielou indexes respectively.Richness index (S) was also calculated based on the number of different taxa per trap.Diversity indices among samples were compared using Shannon diversity t test (p < 0.05).All tests were performed using the statistical software PAST (Hammer et al., 2001).

Results
Pitfall traps captured a total of 11,992 edaphic arthropods belonging to 11 different taxa: Formicidae, Acari, Collembola, Coleoptera, Araneae, Hemiptera, Isopoda, Myriapoda, Blattodea, Embioptera and Dermaptera (Table 1).Besides those taxa, pitfall traps captured 178 adult individuals belonging to the taxa Diptera, Hymenoptera, Orthoptera, and Thysanoptera which are not true soil inhabitants and were not considered in the analysis.Soil fauna was numerically dominated by Formicidae (26.60%) of all organisms captured, Coleoptera (19.77%),Araneae (16.76%),Acari (12.83%),Collembola (13.40%) and Hemiptera (6.89%).Myriapoda, Blattodea, Embioptera, and Dermaptera collectively accounted for 3.74% of the total collected.The higher number of soil arthropods were captured in the field margins followed by the abandoned vineyard (Table 1).Significant differences were found between sites for total abundance (F = 2.555; df = 6; p = 0.026).Tukey's pairwise comparisons showed significant differences between field margins and fallows and wheat fields.The percentage in abundance of main groups of arthropods at different sites respect to field margin is shown in Figure 2. Significant differences for total abundance were also found between zones (F = 3.655; df = 2; p = 0.03), being the traps located nearest to the margin (SD) where more arthropods were captured (Table 2).Tukey's pairwise comparisons showed significant differences between SD and LD (p = 0.04).More arthropods were caught in July.However, no significant differences for total abundance were found between months (F = 0.522; df = 3; p = 0.669).
Richness was highest (n=11) in field margins and abandoned vineyards.Diversity was higher in field margins followed by abandoned vineyards whereas evenness was higher in field margins followed by fallow (Table 1).However, no significant differences were found for diversity between these two sites (Diversity t-test, p = 0.385).In relation to date of capture, both diversity and evenness were higher in April (Table 2), and lower in July.Finally, both diversity and evenness were higher in the line of traps located to medium distance from the margins (Table 2).Diversity was significantly higher at medium distance that at short distance from the margins (Diversity t-test, p < 0.001).

Discussion
As expected, in this study field margins supported the most abundant and diverse community of soil arthropods followed by the abandoned vineyard.The arthropod community was dominated by Formicidae, Coleoptera and Aranae in terms of abundance.The dominance of Formicidae and Coleoptera has been indicated as a general trait of ground dwelling assemblages in the Mediterranean and dessert assemblages (Doblas-Miranda et al., 2007).Even in Mediterranean agrosystems these groups dominates in the soil arthropod fauna (Morris & Campos, 1999;Santos et al., 2007).The presence of other groups is heterogeneous and may depend of the geographic situation, the management regime and the surrounding vegetation (Morris & Campos, 1999).
Plant diversity has long been recognized as an important factor determining the diversity of organisms  Hemiptera Epigeic arthropod abundance in agrosystems at higher trophic levels (Harvey et al., 2008).The intimate relationship between plant and arthropods composition is complex and beyond the scope of this study.However, in this study a clear influence of 'habitat complexity' on abundance soil arthropods has been demonstrated.Thus our results are agree with those reported by Attwood et al. (2008), that observed a general decline in arthropod richness with increasing land-use and management intensity.These authors suggested that the broad process of agricultural intensification from intact, indigenous vegetation associations, through fragmented mixed-agricultural landscapes, to highly intensive, monotypic grazing or cropping systems can lead to a reduction in biological diversity via a range of impacts and threats.There is a number of possible explanations for higher arthropod richness in systems with less intensive land uses (Attwood et al., 2008).Areas of low to moderate modification/intensification (such as native vegetation and pasture) are likely to have greater habitat complexity, due in part to less exposure to intensive and uniform management than many cropping systems.Therefore, in complex land uses, niche opportunities are likely to be numerous, whilst fewer niches may be available in structurally and compositionally less complex systems.Consequently, opportunities for coexistence through resource partitioning, are likely to be reduced in simplified systems, resulting in lowered species richness.More complex habitat composition and structure may allow greater access to a wider range of alternative food resources (Langellotto & Denno, 2004), thus supporting more omnivorous and non-obligate predatory taxa.Another potential explanation for greater richness in less disturbed habitats is that in frequently or intensely disturbed environments, community composition cannot progress beyond early pioneer stages.This frequent 'resetting of the successional clock' in areas of high disturbance results in environments that favor early successional species, while disadvantaging later successional species (Büchs et al., 2003).If the disturbance is sufficiently severe and frequent (such as in intensive cropping), it could feasibly exclude all but the most ruderal of taxa, thus potentially leading to overall lower species numbers.
Common crop management practices such as deep tillage, agro-chemical application and mechanical harvesting may all serve to increase the frequency and severity of disturbance regimes (Thorbek & Bilde, 2004).We do not have analyzed the influence of these factors in our study.However, we have studied tilled and non-tilled systems.Sharley et al. (2008) demonstrated that tillage within vineyards systems disrupted a number of beneficial invertebrate groups, including ants, centipedes, and millipedes.Ant assemblages were particularly disrupted by tillage.Santos et al. (2007) found a similar conclusion in an olive grove ecosystem: if olive grove is frequently disturbed sensitive species of ants will be progressively eliminated.
In our study traps located near the field margins captured more arthropods than those located at medium and large distances.This is according with previous studies that demonstrated that semi-natural habitats bordering crop fields provide stable shelter, food sources, and microclimate to a wide range of arthropods (e.g.Smith et al., 2008).Thus, more arthropods can be captured near the hedgerows.Seasonal conditions at the study site were not pronounced and so no significant differences in abundance and diversity between sampling periods were expected.Strong seasonality is a feature of most ecosystems, particularly in Mediterranean habitats, where the seasonal fluctuations of temperature and rainfall create marked pulses of productivity and animal activity (Blondel & Aronson, 1999).The seasonal and annual variability of the assemblage has potentially important implications on community dynamics in the study systems, since the changes in species composition and trophic structure of soil invertebrate assemblages may affect species interactions and food web dynamics over time (Doblas-Miranda et al., 2007).
Our results suggest that agricultural intensification affects soil arthropods in Tierra de Barros area.Arthropods are important drivers of ecosystem functions as nutrient cycling, pest control, pollination and maintenance of soil structure.So, strategies for addressing the conservation of arthropods in agricultural landscapes must be promoted.

Figure 1 .
Figure 1.Arrangement of thirty pitfall traps in selected sites.Columns were arranged to short (SD, 1 m), medium (MD, 6 m) and large (LD, 11 m) distance to the field margins in the middle of selected plots.

Figure 2 .
Figure 2. Comparison of captures (in percentage) by site respect to field margins for the most abundant taxa of soil arthropods captured (*: significant at p < 0.05, Z-test).

Table 1 .
Total number of specimens, richness, diversity and evenness of soil arthropods captured in the different agrosystems studied *: significant at p < 0.05, Tukey-test.

Table 2 .
Total number of specimens, richness, diversity and evenness of soil arthropods captured in the different months and by distance to the field margins SD: short distance; MD: medium distance; LD: large distance; *: significant at p < 0.05, Tukey test.