Research Article |
Corresponding author: Zsolt Tóth ( toth.zsolt@univet.hu ) Academic editor: Davy McCracken
© 2018 Zsolt Tóth, Elisabeth Hornung, András Báldi.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Tóth Z, Hornung E, Báldi A (2018) Effects of set-aside management on certain elements of soil biota and early stage organic matter decomposition in a High Nature Value Area, Hungary. Nature Conservation 29: 1-26. https://doi.org/10.3897/natureconservation.29.24856
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Agricultural intensification is one of the greatest threats to soil biota and function. In contrast, set-aside still remains a management practice in certain agri-environmental schemes. In Hungary, the establishment of sown set-aside fields is a requirement of agri-environmental schemes in High Nature Value Areas. We tested the effects of set-aside management on soil biota (bacteria, microarthropods, woodlice and millipedes), soil properties and organic matter decomposition after an initial establishment period of two years. Cereal – set-aside field pairs, semi-natural grasslands and cereal fields were sampled in the Heves Plain High Nature Value Area in Eastern Hungary, in May 2014. Topsoil samples were taken from each site for physical, chemical, microbial analyses and for extraction of soil microarthropods. Macrodecomposers were sampled by pitfall traps for two weeks. The biological quality of soil was estimated by the integrated QBS index (‘‘Qualità Biologica del Suolo’’, meaning ‘‘Biological Quality of Soil’’) based on diversity of soil microarthropods. To follow early stage organic matter decomposition, we used tea bags filled with a site-independent, universal plant material (Aspalathus linearis, average mass 1.26 ± 0.03 g). Tea bags were retrieved after 1 month to estimate the rate of mass loss. We found significant differences between habitat types regarding several soil physical and chemical parameters (soil pH, K and Na content). The study showed positive effects of set-aside management on soil biodiversity, especially for microarthropods and isopods. However, we did not experience similar trends in relation to soil bacteria and millipedes. There was higher intensity of organic matter decomposition in soils of set-aside fields and semi-natural grasslands (remaining mass on average: 74.17% and 76.6%, respectively) compared to cereal fields (average remaining mass: 81.3%). Out of the biotic components, only the biological quality of soil significantly influenced (even if marginally) plant tissue decomposition. Our results highlight the importance of set-aside fields as shelter habitats for soil biota, especially for arthropods. Set-aside fields that are out of a crop rotation for 2 years could be a valuable option for maintaining soil biodiversity, as these fields may simultaneously conserve elements of above- and below-ground diversity.
agri-environmental schemes, agrobiodiversity, detritivores, soil biological quality, tea bag method
The European Union (EU) is one of the most intensive agricultural regions per unit of surface area in the world (
Agroecosystems and agricultural landscapes provide important soil related ecosystem services, i.e. the maintenance of soil fertility and structural properties, filtering and providing reservoir for water, nutrient cycling and climate regulation (
Numerous studies have shown that agricultural intensification represents a major threat to soil biodiversity and to the provision of ecosystem services (e.g.
The establishment of semi-natural habitats (grassy strips, sown or naturally regenerated set-aside fields, hedgerows, treelines etc.) in agricultural landscapes is a common practice to enrich habitat diversity or to connect isolated habitats (e.g.
European agricultural policy has long relied on agri-environmental schemes (AES) to alleviate the negative environmental impacts of agricultural intensification (
Insight in conservation management in Central and Eastern European countries could be particularly valuable, as their agrobiodiversity is still high compared to Western Europe (
The present study aimed to test the following hypotheses:
(i) set-aside management has profound effects on soil physical and chemical properties,
(ii) set-aside fields and semi-natural grasslands provide more favourable conditions for studied soil organisms compared to cereal fields,
(iii) plant tissue decomposition is higher in set-aside fields and semi-natural grasslands
(iv) decomposition rate is positively correlated with measures of soil biodiversity.
The study was conducted in the region of North-eastern Hungary (Heves County) in 2014 (see map in Suppl. material
Within the study area, two-year-old set-aside fields (Sa) were chosen, each with an adjacent cereal field (CSa) with seven replicates (Figure
Soil was sampled randomly by taking five soil cores from 0–15 cm depth in May 2014. Before soil analyses, soil cores corresponding to each site were pooled to obtain a composite sample. Physical and chemical analyses of soils were carried out on air-dried samples from which crop residues, root fragments and rocks larger than 2 mm had been removed (
To determine the effects of set-aside management on the bacterial community structure, composite soil samples were taken from each field in May 2014. Soil sampling locations (five subsamples per field) were randomly chosen from the upper surface (0–5 cm). DNA was isolated from samples with NucleoSpin Soil kit (Macherey-Nagel, Düren, Germany). The quality of nucleic acids was assessed with 1% agarose gel electrophoresis stained with ethidium bromide. Nucleic acid quantification was undertaken with a Qubit 2.0 Fluorometer (Thermo Fischer Scientific, Waltham, MA, USA) throughout the study.
For bacterial community fingerprinting with the terminal restriction fragment length polymorphism (T-RFLP) method, 16S rDNA fragments were amplified with a 5’ VIC-labelled 27F primer (VIC-5’-AGAGTTTGATCMTGGCTCAG-3’) and a 518R primer (5’-ATTACCGCGGCTGCTGG-3’). Polymerase chain reactions (PCRs) were undertaken with 5 µl of DreamTaq PCR buffer, 0.3 µM of each primer, 0.2 mM of each dNTP, 30 ng DNA sample, 1 U DreamTaq DNA Polymerase (Thermo Fischer Scientific) and nuclease-free water up to the final reaction volume of 50 µl. Amplification conditions were as follows: 95 °C for 3 minutes, then 32 cycles of 94 °C for 30 s, 52 °C for 30 s and 72 °C for 30 s, then a final extension at 72 °C for 7 minutes. To obtain molecular fingerprints after the amplification, 16S rDNA amplicons were digested with the restriction enzyme, AluI (AG↓CT) (Thermo Fischer Scientific) as described by
Soil microarthropods were collected by taking undisturbed soil cores (8 cm in diameter, 400 cm3, six per plot) to a depth of 15 cm at 0, 10 and 20 m from the field edge along a transect. In semi-natural grasslands, soil samples were taken at a distance of 10 m from each other and 2–300 m from the field edge.
Soil fauna was extracted using the Berlese-Tullgren funnel method. During a 12-day extraction period, microarthropods were collected and stored in vials containing 70% ethanol. All animals were counted under a dissecting microscope. Then they were classified into taxonomic groups and the QBS index (‘‘Qualità Biologica del Suolo’’, meaning ‘‘Biological Quality of Soil’’) was calculated according to
Macrodecomposers were sampled by pitfall traps for two weeks in May 2014. Traps were set along a 20 m transect 0, 5, 10 and 20 m from the field edge. In semi-natural grasslands, traps were placed at a distance of 10 m from each other and 2–300 m from the field edge. We applied funnel traps filled with ethylene glycol. They were sunk directly into the soil and covered with plastic roofs to shield from rain. Pitfall traps were returned to the laboratory and, after sorting for subsequent species identification, the samples were preserved in 70% ethanol. Millipedes (Diplopoda) and isopods (Isopoda: Oniscidea) were identified to species level. For identification of millipedes, the keys of
To follow microbial degradation of organic matter, the novel litter quality independent tea bag method was used (
All statistical analyses were performed in R 3.3.1 (
Outliers were identified and removed prior to data analysis. After fitting the full models for each dependent variable, we used Akaike Information Criterion (AIC) to select the most parsimonious model. The lack of spatial independence of the paired set-aside and cereal fields was treated by application of a random factor (‘location’). Since there was significant intercorrelation between soil characteristics and habitat type, their effects were tested in separate models. Assumptions of normality and homoscedasticity of the residuals were verified visually using diagnostic plots. Statistical significance was determined at the level: α = 0.05.
The effects of land use on soil physical and chemical properties were tested by linear mixed-effects model (LMM), with ‘habitat type’ as explanatory variable and ‘location’ as random factor.
Alpha diversity metrics (Shannon diversity [H'] and Evenness [J'] indices based on T-RFLP abundance data) were calculated to estimate the diversity of bacterial communities. We used LMMs to determine the effects of habitat type, soil physical and chemical properties on bacterial alpha diversity. A PERMANOVA (Bray-Curtis index, permutation = 999) was conducted to assess differences in the bacterial communities by habitat type.
To characterise soil arthropod communities, QBS index, species richness (number of species in the sample) and abundance (number of individuals in the sample) were used. The LMMs were used to examine the effects of abiotic soil properties and habitat type on faunal richness and abundance. The influence of abiotic soil properties and habitat types on the species composition of isopod and millipede assemblages was tested by generalised linear mixed models (GLMMs) with the multivariate approach. As our data showed a negative binomial distribution, we thus used the ‘manyglm’ method (family = negative binomial). Then we conducted NMDS ordinations using the Bray-Curtis dissimilarity index to visualise patterns of species composition of macrodetritivore assemblages. In the latter case, species with low relative abundance (Trachelipus nodulosus: 0.43%, Porcellionides pruinosus: 0.58%) were excluded from the analysis.
Rates of decomposition were estimated with a single exponential decay model (
Mt / M0 = e−kt, (1)
where M0 is the initial dry mass, Mt is the residual dry mass at time t and k is the decay constant.
The effects of habitat type and abiotic soil properties were tested by a LMM.
A soil biodiversity index was calculated from the average of all standardised soil community characteristics (bacterial diversity, QBS index, macrofauna species richness and abundance) and used as a general indicator (
We experienced significant differences in soil pH, K2O and sodium (Na) content amongst habitat types. Soil pH ranged from 4.42 to 6.86 in the different habitat types. It had the lowest value in semi-natural grasslands (G) followed by set-aside (Sa) and cereal fields (C and CSa) (Table
Basic properties of soil samples taken from the 0–15 cm depth (mean ± SE). Letters indicate significant differences amongst the means at p < 0.05. Abbreviations – SOM: soil organic matter, C: cereal fields, CSa: cereal fields adjacent to set-asides, Sa: set-aside fields, G: semi-natural grasslands.
Habitat types | ||||
---|---|---|---|---|
C | CSa | Sa | G | |
pH | 6.09±0.22 (a) | 5.54±0.22 (ab) | 5.29±0.20 (bc) | 4.92±0.13 (c) |
KA | 44.83±1.23 (a) | 47.14±2.77 (a) | 43.57±0.94 (a) | 47.17±1.44 (a) |
Salt (m/m %) | 0.04±0.01 (a) | 0.03±0.00 (a) | 0.04±0.01 (a) | 0.05±0.01 (a) |
CaCO3 (m/m %) | 0.32±0.29 (a) | 0.19±0.17 (a) | 0 (a) | 0 (a) |
SOM (m/m %) | 3.57±0.43 (a) | 3.29±0.21 (a) | 3.52±0.28 (a) | 4.02±0.29 (a) |
NO2-NO3 N (mg kg-1) | 13.04±6.67 (a) | 7.88±1.04 (a) | 23.27±5.39 (a) | 35.67±16.49 (a) |
P2O5 (mg kg-1) | 300±57.79 (a) | 165.71±23.61 (a) | 136.86±43.21 (a) | 233.75±119.06 (a) |
K2O (mg kg-1) | 682±99.12 (a) | 677.14±71.93 (a) | 461±65.2 (b) | 378±32.76 (b) |
Na (mg kg-1) | 182.92±66.35 (b) | 97.37±13.77 (b) | 72.14±13.35 (b) | 500.5±96.61 (a) |
Mg (mg kg-1) | 565.33±81.85 (a) | 542.14±70.63 (a) | 605.57±68.48 (a) | 775.17±118.34 (a) |
SO4-S (mg kg-1) | 41.5±6.64 (a) | 38.79±4.36 (a) | 42.39±4.40 (a) | 58.2±7.84 (a) |
Soil bacteria
The Shannon and Evennes indices showed relatively high variability amongst habitat types, with values ranging from 1.37 to 3.03 and from 0.28 to 0.71, respectively. Only Evennes index was significantly influenced by the studied environmental variables: it decreased with the SOM% (t = -2.47, p = 0.05), whereas increased with soil Na content (t = 3.28, p = 0.022) (Table
Soil microarthropods
In total, 14385 specimens belonging to 19 taxa of microarthropods were sampled (Suppl. materials
Diversity (expressed in species richness and QBS index) and abundance of microarthropods (A–B), isopods (C–D) and millipedes (E–F) in different habitat types. Error bars represent means and SE. Please note the different scaling for the Y axes. Letters indicate significant differences amongst the means. Abbreviations – C: cereal fields, CSa: cereal fields adjacent to set-asides, Sa: set-aside fields, G: semi-natural grasslands.
Effects of habitat type and soil physicochemical properties on microarthropods and macrodetritivores. CaCO3 and Mg variables are not included in the table, since they had significant effects on none of the dependent variables. Abbreviations – QBS: soil biological quality index, SR: species richness, SOM%: soil organic matter %, KA: soil plasticity index according to Arany; +: positive effect, −: negative effect, NS: not significant, ***: p ≤ 0.001, **: p ≤ 0.01, *: p ≤ 0.05, ˙: p ≤ 0.1
Microarthropods | Macrodetritivores | |||||||
---|---|---|---|---|---|---|---|---|
Isopoda | Diplopoda | |||||||
diversity (QBS) | abundance | composition | diversity (SR) | abundance | diversity (SR) | abundance | composition | |
habitat | ** | * | NS | * | ** | NS | * | ** |
pH | − *** | + *** | NS | − * | NS | NS | NS | NS |
SOM % | + * | NS | ˙ | NS | NS | NS | NS | NS |
KA | + ** | NS | NS | NS | NS | NS | NS | * |
salt | NS | − *** | NS | NS | NS | NS | NS | ˙ |
K2O | NS | − *** | NS | NS | − ˙ | NS | NS | NS |
NO2-NO3 N | NS | + *** | NS | NS | − * | NS | NS | NS |
SO4-S | + ** | NS | NS | NS | NS | NS | NS | NS |
Na | − * | − ** | NS | NS | NS | NS | NS | NS |
Soil macrodetritivores
In total, 1391 individuals of 8 macrodecomposer species were identified from samples collected by the pitfall traps, including 783 individuals of four isopod species (Armadillidium vulgare, Latreille, 1804; Porcellionides pruinosus, Brandt, 1833; Trachelipus rathkii, Brandt, 1833; Trachelipus nodulosus, C. Koch, 1838) and 608 individuals of four millipede species (Brachydesmus superus, Latzel, 1884; Brachyiulus bagnalli, Brölemann, 1924; Iulus terrestris, Linnaeus, 1758; Megaphyllum unilineatum, C. Koch, 1838) (Suppl. materials
In the present study, species richness was significantly affected by the studied environmental variables only in the case of isopods. We experienced significant effects of habitat type and soil pH on isopod species number increasing with soil acidity (z = -2.236, p = 0.022) (Table
Species composition of iso- and diplopod assemblages was affected by habitat type, salt concentration and soil plasticity (Table
On average, 22.41% of organic matter was decayed during a month. Mass loss was significantly different between habitat types (F = 10.8618, p < 0.001). We experienced the highest decomposition in set-asides (remaining mass: 74.17%, on average) while the lowest in cereal fields (remaining mass: 81.3%, on average). The decomposition rate was negatively influenced by SOM content (F= 12.3966, p= 0.002). However, soil pH had positive effects on the intensity of mass loss (F = 5.3119, p = 0.033). Organic matter decomposition did not change with soil biodiversity (t = 1.2589, p = 0.255). Nevertheless, we found marginally significant QBS index – decay rate relationship (t = 2.1076, p = 0.08) (Figure
The general consensus in literature is that agricultural practices, particularly soil cultivation and manuring, can lead to drastic changes in soil physical and chemical properties (e.g.
Soil bacteria
Contrary to our expectations, we found no significant differences amongst habitat types regarding bacterial alpha diversity and community composition. The majority of studies showed that microbial species richness increases both with plant diversity and reduction of anthropogenic disturbances (e.g.
Out of the α diversity indices, the evenness of the bacterial communities was significantly influenced by SOM and sodium contents of soils. This corresponds with findings in which significant effects of soil pH, organic matter content, moisture and nutrient availability on microbial community structure have been reported (e.g.
Soil microarthropods
The more diverse and complex vegetation creates more favourable microclimatic conditions for soil microarthropods (
The higher microarthropod diversity and abundance in cereal fields adjacent to set-asides compared to cereals without set-aside fields are probably attributable to the spillover effect of set-aside fields: several studies have proved the positive role of semi-natural habitat patches as propagule sources, affecting favourably the adjacent areas as well (e.g.
Soil macrodetritivores
Species richness of isopods and millipedes reflected the regional species pool. All millipede and isopod species found in the sampling sites are rather common in the Hungarian Great Plain (Korsós and Hornung, unpublished results). In human modified habitats, such as agroecosystems, a wide range of millipede species generally occurs in relatively low species richness, but in high density (
We identified that habitat type, salt concentration and soil plasticity (expressed in KA) were the main factors influencing the species composition of the macrodecomposer assemblages (Figure
Plant tissue decomposition was the highest in set-aside fields and semi-natural grasslands during the studied period. There was also a significant difference in mass loss of organic matter between cereal fields with and without set-asides. We experienced the lowest degree of decomposition in the latter habitats.
It has long been proven that characteristics of ecosystems (e.g. physical, chemical and biological properties) basically determine their functionalities (
In addition to the habitat type, two abiotic soil properties (soil pH and SOM%) also significantly affected the decomposition rates. The greater biodegradation observed in the more alkaline soils is probably attributed to the fact that the acidic soil pH is not favourable to the majority of soil organisms, which can lead to reduced organic matter decomposition. The negative relationship between SOM content and decay rates could infer less intensive mineralisation and immobilisation than humification, resulting in a higher SOM level due to the gradual accumulation of soil organic matter.
There was no significant correlation between soil biodiversity and organic matter decomposition in our research, despite the positive trend between the two variables. Reasons for the lack of significance may be related to one-off sampling, short period of the organic matter decomposition test, forced skip of key groups of decomposer organisms (fungi, earthworms) etc. In the case of microbes, we could estimate the diversity only of soil bacteria, although it is possible that habitats with acidic soils were dominated by fungi. This is also supported by the fact that soils with low pH and higher organic matter content – such as semi-natural grasslands and set-aside fields in our study – generally have a fungal-dominated food web (
Out of the biotic components, only soil biological quality (expressed in the QBS index) significantly influenced (even if marginally) plant tissue decomposition. The positive effects of microarthropods on decay of organic matter have already been demonstrated in a number of studies (e.g.
Our results indicate that set-aside management under agri-environment schemes has profound effects not only on certain soil physical and chemical properties, but on soil biodiversity and function as well. The present study highlights the importance of set-aside fields particularly for the conservation to surface dwelling invertebrates. Set-aside fields function as semi-natural habitats providing favourable conditions especially for micro- and macroarthropods, supporting the regeneration of soil biological resources. Set-aside fields that are not part of a crop rotation for at least 2 years could be a valuable option for establishing ecological focus areas under the Common Agricultural Policy (CAP) in the EU, as these fields may help to conserve soil biodiversity.
However further research is required to look for the optimum management regimes for all soil-related organisms supporting the most abundant and diverse soil biota, particularly in relation to the establishment methods of set-aside or other semi-natural habitat types in agricultural landscapes.
Finally, we emphasise that evaluation of agri-environmental schemes, regarding soil biodiversity and function, is of high practical and theoretical importance. For example, data on soil biota, plant tissue decomposition and/or their relationship are essential to better understand mechanisms influencing biogeochemical cycles. Therefore, the biological and functional aspects of soil need to be better taken into account in a national or/and European soil monitoring scheme.
The authors thank the Bükk National Park Directorate and the landowners for permission to work on their fields. We are grateful to András Táncsics and Balázs Kriszt (Szent István University) for their contribution in microbial analyses. We would like to thank Zoltán Elek and Gergely Boros (MTA Centre for Ecological Research) for their assistance in field works and for advice. This research was financially supported by the LIBERATION EU FP7 project [FP7 KBBE 311781] and the 12190-4/2017/FEKUTSTRAT grant of the Hungarian Ministry of Human Capacities.
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