Land use influences the abundance and diversity of soil arthropods. The evaluation of the impact of different management strategies on soil quality is increasingly sought, and the determination of community structures of edaphic fauna can represent an efficient tool. In the area of Langhe (Piedmont, Italy), eight vineyards characterized for physical and chemical properties (soil texture, soil pH, total organic carbon, total nitrogen, calcium carbonate) were selected. We evaluated the effect of two types of crop management, organic and integrated pest management (IPM), on abundance and biodiversity of microarthropods living at the soil surface. Soil sampling was carried out in winter 2011 and spring 2012. All specimens were counted and determined up to the order level. The biodiversity analysis was performed using ecological indexes (taxa richness, dominance, Shannon–Wiener, Buzas and Gibson's evenness, Margalef, equitability, Berger–Parker), and the biological soil quality was assessed with the BSQ-ar index.
The mesofauna abundance was affected by both the type of management and
sampling time. On the whole, a higher abundance was in organic vineyards
(
The functioning of terrestrial ecosystems depends on the relationships between above- and belowground food webs. In particular, the transfer of biotic components of the decomposer subsystem highly affects the relationship between the two components (Kardol et al., 2011; Wardle et al., 2004).
Soil quality characteristics such as stability, resilience to disturbance or stress and biodiversity (van Bruggen and Semenov, 2000) are directly influenced by land use and management practices (DeFries et al., 2004). Assessment of soil quality is a complex issue that depends on the combination of all physical, chemical and biological properties.
The capability of a soil to sustain biological productivity while at the same time maintaining environmental equilibrium cannot be directly measured; however, it can be assessed through indicators based on biological components of soil that need standardization and suitable databases. Compared with forestry, there is generally less agreement about how the relationship between biodiversity and agriculture should be measured. Much of the emphasis – where it occurs at all – is focused on measuring detrimental impacts of agriculture on surrounding habitats (for instance through soil erosion or pollution run-off) rather than looking at biodiversity within agricultural systems (Dudley et al., 2005). The development of agroecological technologies and systems which emphasize the conservation/regeneration of biodiversity, soil, water and other resources is urgently needed to meet the growing array of socioeconomic and environmental challenges (Altieri, 1999; Lavelle, 2000). European policies for sustainable agronomic management have been implemented, but these need to be evaluated for their efficiency (Chikoski et al., 2006; Herzog, 2005).
Several studies have documented the importance of the soil biota for soil quality and vitality (Lavelle et al., 2006), as well as its potential for reflecting anthropogenic disturbances (Paoletti et al., 1991; Van Straalen, 1998). In an agricultural context, the combination of productive goals and sustainable land uses protecting both soil and biodiversity is essential in order to prevent the decline of soil fauna communities (Menta et al., 2011). Enhancing biodiversity in agroecosystems is a key ecological strategy to make sustainable productions.
Farming practices such as ploughing, chemical fertilization and pesticide application can affect soil quality by modifying soil characteristics (Mazzoncini et al., 2010). Therefore, soil quality can be assessed by physical, chemical and microbiological properties of soil together with the abundance and diversity of edaphic fauna (nematodes, Acari, Collembola, Symphyla, Chilopoda, Pauropoda, enchytraeids, earthworms); furthermore, the determination of community structure adds significant information on the soil status (Cole et al., 2006; De Goede and Brussard, 2002; Duelli and Obrist, 2003; Menta et al., 2008; van Straalen, 1998; Yan et al., 2012). In a well-balanced soil, mesofauna is highly biodiversified and occupies all trophic levels within the soil food webs (Ruf et al., 2006). Therefore, the loss of mesofauna diversity is a negative consequence on soil biota, since it is involved in fundamental ecosystem services such as nutrient cyclings (Gardi et al., 2008; Narula et al., 1996). The knowledge of interactions between the different groups of organisms and of mechanisms regulating the soil food web is crucial for assessing the sustainability of land use; however there is a need for further studies (Maraun and Scheu, 2000).
Soil microarthropods, as litter transformers, improve soil quality and affect the soil structural properties (porosity, aeration, infiltration and distribution of organic matter in soil horizons) (Bird et al., 2004; Culliney, 2013). They are concentrated in the litter layers and upper horizons of the soil, and their abundance and distribution are highly dependent on individual tolerance limits to environmental conditions (Chikoski et al., 2006; Faber and Verhoef, 1991). Microarthopods are useful models as they are both taxonomically and ecologically highly diversified; particularly, euedaphic forms are unable to survive abrupt variations due to the disturbances caused, for example, by agricultural cultivation and trampling (Parisi et al., 2005; Menta, 2012).
The literature suggests that organically managed fields contain a greater abundance and diversity of arthropods than conventionally managed fields (Berry et al., 1996; Hole et al., 2005; Pimentel et al., 2005; Reddersen, 1997) and that changing from conventional to organic farming leads to a gradual increase in biodiversity (van Diepeningen et al., 2006).
The aim of this study was to determine the effect of management practices in experimental vineyards, by comparing organic and integrated pest management (IPM), on soil microarthropod community structure and composition before and after treatments. In particular, we hypothesized that organic management may positively affect the abundance (total numbers of individuals), richness (total numbers of taxa (ecomorphological group), diversity and quality indexes of all soil microarthropods as evidenced in the cited studies where organic and conventional managements were compared.
The study was carried out in the north-west of Italy, in Piedmont, in the central Tanaro River area (Table 1a). This hilly area is characterized by marls, clays and sands, and is almost entirely devoted to the production of high-quality wines, in particular Barbera. The sampled vineyards are located in a triangle area with 20 km maximum distance between the vineyards' locations.
According to the georeferenced soil database for Europe, the climatic
classification of this area is Mediterranean suboceanic to subcontinental
(TM3) (Costantini et al., 2013): this is characterized by a degree of
continentality – a rather high temperature difference between summer and
winter and a quite regular precipitation pattern – typifying the Po Plain
and adjacent low hills as relatively warmer than the other climates of
northern Italy. On the whole, although the various microclimates determined
by the hills and valleys of the Langhe are influenced by the continental
climate of the entire area, the values of average annual temperature of all
places lowland (below 300 m above sea level) are similar (see Table 1b), in
the 12–14
Soil physical and chemical parameters of the investigated vineyard sites (March 2011).
IPM were treated with anti-downy mildew
fungicides such as metiram (three times), metiram
Soil samples for the study of microarthropods were carried out in late winter
2011 and spring 2012. In each site, one plot (10 m
The samples collected for determination of abiotic parameters were
homogenized for each vineyard. Soil texture was determined by the X-ray
attenuation method according to the procedure described by Andrenelli et
al. (2013), using a Micromeritics SediGraph apparatus. The procedure provides
pipette-equivalent results. Soil pH was determined potentiometrically in a
1 : 2.5 soil : water suspension. Soil total organic carbon (TOC) and
total nitrogen (TN) were determined by dry combustion, using a Thermo Flash
2000 CN analyser. Each soil sample was analysed two times separately:
60–70 mg of soil was weighed into Sn capsules and analysed for total C
(organic
The influence of management and soil sampling was evaluated on the density of
mesofauna by means of analysis of variance (ANOVA). In the present study, the
biological soil quality was defined through qualitative and quantitative
indices. The ecological quali-quantitative indices, calculated for each
management in spring and autumn samples, were the following (see Harper,
1999; Krebs, 1989): taxa richness (
Biological quality of soil was evaluated by the BSQ-ar index (Parisi, 2001). The BSQ-ar index is based on direct correlation between the quality of soil and the number of microarthropods adapted to the soil habitat. It uses the biological form approach to separate the mesofauna specimens into morphological classes according to their levels of adaptation to the soil environment. Each form is ecomorphologically scored (EMI: eco-morphological index), ranging from 1 to 20, on the basis of its edaphic adaptation level. The sum of EMIs gives the global value of BSQ-ar index. The biological soil quality was characterized on the basis of D'Avino (2002) classification and the values were compared by the Mann–Whitney test.
The statistics concerning the calculation and comparisons of the biodiversity indexes were obtained using the program PAST (2013) (Hammer et al., 2001). All other statistical analyses were performed using the statistical program SPSS 13.0 (SPSS, 2004).
The climate data for air temperature and rainfall registered in the three
locations for 120 days before the samplings are reported in Fig. 1. During
the considered periods, the daily mean temperatures were quite similar in the
different localities with values around 3
Temperature (lines) and rainfall (bars) measured in the three
vineyard sites (CSA, CSB, CSF) for 120 days before the soil samplings in
2010–2011
The soil characteristics of studied sites are reported in Table 2. The
different vineyard soils had quite homogeneous texture, ranging from medium
(loam) to moderately fine (clay loam and silty clay loam). Soil TOC content
was generally medium, scarce in CSB_i2 and CSF_i3, and high in CSA_o3.
TN content was the highest in CSA_o3. Soil pH ranged from slightly to
moderately alkaline. Total CaCO
Community structure of the soil microarthropods (
On the whole, the abundance of microarthropods was higher in the organic
vineyards than in IPM ones, with a ratio of about 2 : 1, and the mesofauna
density was considerably affected by both sampling time
(
Figure 2 shows the total soil microarthropod density registered in the
different samplings. In 2011, a higher density was registered in the organic
vineyards (
Density of soil microarthropods measured as means (
The community structure of the soil microarthropods in the different seasons is reported in Table 3. The distribution of the three main animal groups (Acari, Collembola, other arthropods) did not show any substantial difference depending on management. The mites represented about 50 % of the total arthropodofauna recorded, collembolans about 30 %, and other microarthropods about 20 %. The group of the other arthropods was represented by epiedaphic (Rincota, Thysanoptera, Diptera, Psocoptera, Blattodea), hemiedaphic (Hymenoptera, holometabolous larvae, Diptera larvae, Geophilomorpha, Julida, Isopoda, Homoptera) and euedaphic forms (Symphyla, Pauropoda, Pseudoscorpionida, Coleoptera, Protura, Diplura).
The biodiversity indexes and their comparisons are reported in Table 4. In
March 2011, the taxa richness was higher in the organically managed
vineyards; the Margalef index denoted a higher variation in soil samples from
the organic vineyards, while a higher evenness (
The BSQ-ar index was higher in the organic than in the IPM vineyards
in March 2011 (Mann–Whitney,
On the whole, several studies report about comparison in biodiversity between organic and conventional fields/crops by indicating a greater abundance and diversity of arthropods in organic ones (e.g. Hole et al., 2005; Kromp, 1990; Liebig and Doran, 1999; Reddersen, 1997). Less data and evidence are available in the evaluation of the artropod biodiversity to compare organic and IPM managements (Landi et al., 2014; Todd et al., 2015). The organic and integrated systems showed higher soil quality and potentially lower negative environmental impact than the conventional system (Mazzoncini et al., 2010; Reganold et al., 2001).
Taxa richness (
Soil microarthropods taxa, eco-morphological index (EMI) and QBS-ar
values for each sampling time and management. Values with different letters
within each row are different (Mann–Whitney
In the present study case, in vineyards, the effect of organic and IPM managements on soil quality was evaluated through the characterization of the entire microarthropod community living on soil surface. The total abundance and biodiversity of microarthropods were higher in the organically managed vineyards than the IPM ones only in March 2011. Some factors may have contributed to this evidence. Compared to the organic management, which was based on no-tillage, allowing natural grass to cover the vineyard floor over the whole year, IPM may have resulted in higher soil disturbance due to the tillage treatment performed at the beginning of winter, which can explain the lower collembolan population (Heisler, 1991).
The treatments applied on vine plants in the different managed vineyards did not seem to affect the soil mesofauna as registered by Scalercio et al. (2009) on olive groves. Conversely, the suppression of the herbicide (glyphosate formulations) application, in IPM fields in 2012, appeared to benefit the organisms living in the topsoil; this was observed by Gomez and Sagardoy (1985) and by Renaud et al. (2004) on springtails.
In addition, the difference registered in 2011 and 2012 in the total abundance could be affected by climatic data registered in the previous sampling periods and natural seasonal fluctuations in soil microarthropods (Culliney, 2013; Narula et al., 1996). In accordance with other studies, the number of springtails, in 2012, increased after rainfall, finding an optimal habitat (Badejo et al., 1998; Costantini et al., 2015; Schaefer, 1995).
In the first half of February 2012, Piedmont was affected by an exceptional cold spell, while an average deficit of 8 % rainfall was observed (ARPA Piemonte, 2012).
Concerning the biodiversity analysis, the higher dominance in May 2012 in organic vineyards than IPM ones was due to mite and springtail populations: these groups represented 91 % of the total microarthropods collected. On the whole, within Acari, the oribatid mites were the most represented with a ratio of about 2 : 1 (oribatids in organic vs. oribatids in IPM). This evidence seems to be in agreement with those registered by several authors that consider the oribatid mites as a good bioindicator as their community structure can be significantly affected by several levels of disturbance (Behan-Pelletier, 1999; Caruso and Migliorini, 2006).
The biodiversity indexes registered in 2011, in particular the Margalef index, were affected by the difference in taxa richness. In organic vineyards, conspicuous presence of euedaphic groups was registered such as pseudoscorpions, Protura, Diplura, springtails, mites and small myriapods (Pauropoda and Symphyla). In 2012, the same number of taxa richness values was measured in the different management. However, the relative frequency in each taxon determined higher values in Shannon–Wiener and equitability indexes in IPM vineyards.
The BSQ-ar values were consistent with the total microarthropod abundance.
The biological quality of the soil was very high in the organic vineyards of Costigliole d'Asti area. These soils can be ascribed to high biological classes (VI), similar to those registered in undisturbed and forestal soils (Parisi et al., 2005). Miani et al. (2005) found similar evidence, with BSQ-ar values higher (about 20 %) in organic vineyards than the values registered in conventionally managed ones.
In this case study, on the yearly basis, the IPM strategy seemed to affect the soil biota; however, on a short timescale, high BSQ-ar values were registered by denoting that these soils are still resilient and show quick microarthropod recolonization. Biodiversity plays a fundamental role in the capacity of the soil to recover its initial situation after a natural or human perturbation (Spratt, 1997). The presence of some euedaphic groups (Protura, Diplura and Pauropoda), even if less affecting the soil processes (Eisenbeis and Wichard, 1987), is highly responsive to stress conditions and can be relevant for the purpose of biomonitoring (Parisi et al., 2005).
The BSQ-ar allowed for different situations to be compared and for guidance to be provided for the interpretation of the impact management. At the same time, it must be emphasized that, if a study aim is qualitatively focused on highlighting the presence of key species (i.e. sensitive to agricultural processing/works) well adapted to soil habitat, it is highly advisable to evaluate the euedaphic forms present in a deeper sampling range or to study the vertical migration of microarthropods.
By perspective, attention should be moved from the monitoring method to evaluate to which extent the processes determined by microarthropods can affect a plant's physiological and productive status. The effects of soil biodiversity on vegetation dynamics operate through a variety of biotic interactions, among which are the changing interactions between plants and their below- and above-ground multitrophic communities (Bardgett and van der Putten, 2014).
This kind of evidence can be integrated in the microarthropod studies addressing spatial and temporal partitioning, population dynamics, and taxon-specific or functional groups. As soil arthropods include a wide range of taxa with diverse patterns of response to different kinds of anthropogenic perturbations (Decaëns et al., 2006), may provide a wider view of soil quality if they are combined with other parameters (e.g. soil physico-chemical conditions, bioavailability).
Further research is needed to establish more quantitative relationships between specific groups, especially among arthropods, to better understand the roles of soil fauna in C and N cycles and crucially developing such ecological–economic links to assess the effects of agricultural systems on specific, measurable properties that are important indicators of sustainability.
The authors would like to thank the following vineyard farms for their receptiveness and kindness: Az. Agr. Corino Lorenzo, Costigliole d'Asti (Asti); Az. Agr. Piana Antonio, Castelboglione (Asti); and Tenuta Vitivinicola Bricco Boschis, Cavallotto, Castiglione Falletto (Cuneo). Edited by: S. Mocali