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Article history:
Received 15 April 2015
Received in revised form 5 August 2015
Accepted 11 August 2015
Available online xxx
Soil organisms are considered drivers of soil ecosystem services (primary productivity, nutrient cycling,
carbon cycling, water regulation) associated with sustainable agricultural production. Soil biodiversity
was highlighted in the soil thematic strategy as a key component of soil quality. The lack of quantitative
standardised data at a large scale has resulted in poor understanding of how soil biodiversity could be
incorporated into legislation for the protection of soil quality. In 2011, the EcoFINDERS (FP7) project
sampled 76 sites across 11 European countries, covering ve biogeographical zones (Alpine, Atlantic,
Boreal, Continental and Mediterranean) and three land-uses (arable, grass, forestry). Samples collected
from across these sites ranged in soil properties; soil organic carbon (SOC), pH and texture. To assess the
range in biodiversity and ecosystem function across the sites, fourteen biological methods were applied
as proxy indicators for these functions. These methods measured the following: microbial diversity: DNA
yields (molecular biomass), archaea, bacteria, total fungi and arbuscular mycorrhizal fungi; micro fauna
diversity: nematode trophic groups; meso fauna diversity: enchytraeids and Collembola species;
microbial function: nitrication, extracellular enzymes, multiple substrate induced respiration,
community level physiological proling and ammonia oxidiser/nitrication functional genes. Network
analysis was used to identify the key connections between organisms under the different land use
scenarios. Highest network density was found in forest soils and lowest density occurred in arable soils.
Key taxomonic units (TUs) were identied in each land-use type and in relation to SOC and pH
categorisations. Top-connected taxonomic units (i.e. displaying the most co-occurrence to other TUs)
were identied for each land use type. In arable sites this was dominated by bacteria and fungi, while in
Keywords:
Soil biodiversity
Ecosystem function
Carbon cycling and storage
Nitrogen
Phosphorus
Nutrient cycling
Network analysis
* Corresponding author.
E-mail address: rachel.creamer@teagasc.ie (R.E. Creamer).
http://dx.doi.org/10.1016/j.apsoil.2015.08.006
0929-1393/ 2015 Elsevier B.V. All rights reserved.
Please cite this article in press as: R.E. Creamer, et al., Ecological network analysis reveals the inter-connection between soil biodiversity and
ecosystem function as affected by land use across Europe, Appl. Soil Ecol. (2015), http://dx.doi.org/10.1016/j.apsoil.2015.08.006
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APSOIL 2259 No. of Pages 13
grassland sites bacteria and fungi were most connected. In forest soils archaeal, enchytraeid and fungal
TUs displayed the largest number of neighbours, reecting the greatest connectivity. Multiple regression
models were applied to assess the potential contribution of soil organisms to carbon cycling and storage
and nutrient cycling of specically nitrogen and phosphorus. Key drivers of carbon cycling were microbial
biomass, basal respiration and fungal richness; these three measures have often been associated with
carbon cycling in soils. Regression models of nutrient cycling were dependent on the model applied,
showing variation in biological indicators.
2015 Elsevier B.V. All rights reserved.
1. Introduction
Soil organisms are considered as drivers of ecosystem services,
in particular those soil ecosystem services associated with
sustainable agricultural production. These include primary production of food, bre and fuel, nutrient cycling, carbon cycling and
storage, and water inltration and purication (Hooper et al.,
2005). As such, soil biodiversity is therefore highlighted in the Soil
Thematic Strategy (EU (European Union), 2002) as a key
component of soil quality. Soil quality is dened as the capacity
of soil to function, within natural or managed ecosystem
boundaries, to sustain plant and animal production, maintain or
enhance water and air quality, and support human health and
habitation (Karlen et al., 1997). Many of these functions depend on
the diversity and activities of soil organism communities.
Increasingly we require a multi-faceted approach to land
management, with an increasing need for greater food production,
while simultaneously delivering other ecosystem services or soil
functions, such as carbon (Tardy et al., 2015) and nutrient cycling
(Fierer et al., 2012). Land management can lead to the degradation
of carbon stocks in soils, and therefore understanding the role of
soil biota in carbon cycling and storage is vital. The soil carbon pool
is 3.3 and 4.5 times the size of the atmospheric (760 Gt) and the
biotic pool (560 Gt), respectively (Lal, 2004). It is essential from a
climate change perspective that we protect carbon storage
potential in our soils, furthermore, active cycling of carbon,
combined with large amounts of organic carbon temporarily
stored in soils, increases primary productivity, stabilises soil
structure, increases nutrient retention and water ltration (Turb
et al., 2010 De Vries et al., 2013). Land management also has a
signicant impact on the capacity of the system to cycle nutrients,
providing a constant supply to crops as needed to ensure optimum
productivity. This has traditionally been a high input system, with
the addition of synthetic fertilisers to promote availability of
essential nutrient for plant growth (especially nitrogen (N) and
phosphorus (P)), however it is becoming increasingly apparent
that soil organisms have a strong role to play in the cycling of
nutrients due to their involvement in the geochemical cycles
(Lemanceau et al., 2015).
In 2012, the European Commission acknowledged the importance of soil biodiversity in the role of ecosystem functioning, stating
that these functions are worthy of protection because of their socioeconomic as well as environmental importance (Jones et al., 2012).
However, the lack of quantitative standardised data on soil
biodiversity at the European scale has resulted in poor understanding of both the role that soil organisms play in soil ecosystem services
and the need to protect soil biodiversity to ensure the future
provision of such functions. This was also highlighted in the EUs 6th
Framework programme nanced project: environmental assessment of soil for monitoring (ENVASSO) established in 2005, that
recommended pan-European indicators to assess the potential loss
of soil biodiversity (Bispo et al., 2009). This work has been followed
up by the Ecological Function and Biodiversity Indicators in
European Soils (EcoFINDERS) project, nanced under the EUs 7th
Framework programme and established in 2009, to support the
Please cite this article in press as: R.E. Creamer, et al., Ecological network analysis reveals the inter-connection between soil biodiversity and
ecosystem function as affected by land use across Europe, Appl. Soil Ecol. (2015), http://dx.doi.org/10.1016/j.apsoil.2015.08.006
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model and sampling can be found in Stone et al. (2015). In brief, soil
was sampled from each site following a pre-agreed standard
operating procedures (SOPs) within EcoFINDERS, guaranteeing
that all sites were sampled in a consistent manner. Soil was taken
from the top 5 cm of the prole using plastic cores. All cores were
packed in pre-labelled bags and posted (24 h delivery) in cooled
boxes to Teagasc Research Institute, in Ireland. On receipt, soils
were sieved to <2 mm fraction and sub-sampled following a
specied coning and quartering technique to attain homogenous
sub-samples (except the mesofaunal samples which were kept
untouched). All sub-samples for molecular analyses were frozen to
40 C and DNA extracts at 80 C. All sub-samples for microbial
functional analyses and cores for faunal analyses were kept at 4 C.
Sub-samples were posted onto the nal laboratory for analysis
within 2 weeks of receipt, using freezer packs to keep the sample
cooled. Sub-samples for the measurement of soil physical/
chemical properties were dried at 40 C (air dried).
2.2. Measurement of soil properties
Soil texture was measured using the particle size pipette
method (ISO (International Organization for Standardization),
1998), providing information on total sand (%), silt (%) and clay (%)
fractions. Total carbon (C) and nitrogen (N) were analysed
Fig. 1. Map of transect sites, based upon the biogeographical zones of Europe (EEA, 2012).
Please cite this article in press as: R.E. Creamer, et al., Ecological network analysis reveals the inter-connection between soil biodiversity and
ecosystem function as affected by land use across Europe, Appl. Soil Ecol. (2015), http://dx.doi.org/10.1016/j.apsoil.2015.08.006
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APSOIL 2259 No. of Pages 13
Please cite this article in press as: R.E. Creamer, et al., Ecological network analysis reveals the inter-connection between soil biodiversity and
ecosystem function as affected by land use across Europe, Appl. Soil Ecol. (2015), http://dx.doi.org/10.1016/j.apsoil.2015.08.006
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APSOIL 2259 No. of Pages 13
stand (15 min, room temperature). NO2 was measured spectrophotometrically (OD 540 nm) on a microplate reader. The NO2 -N
concentration was calculated using a calibration curve made with a
standard solution of NaNO2 (10 mg NO2 -N ml 1).
Quantication of the bacterial and archaeal ammonia-oxidizers
(AOA and AOB) and of the nitrous oxide reducers (nosZ1 and
nosZ2) was performed according to Tourna et al. (2008), Leininger
et al. (2006) and Jones et al. (2013), respectively. The real-time PCR
assays were carried out in a ViiA7 (Life Technologies, USA) with a
15 ml reaction volume containing the SYBR green PCR Master Mix
(Absolute Blue QPCR SYBR Green Low Rox Mix, Thermo, France),
1 mM of each primer, 250 ng of T4 gene 32 (QBiogene, France) and
0.5 ng of DNA. Standard curves were obtained with serial plasmid
dilutions of a known amount of a plasmid DNA containing
fragment of the amoA, nosZ1 and nosZ2 genes.
2.5. Statistical procedures
2.5.1. Network analysis for soil biodiversity linkages
To construct networks, TRFLP data were used for fungi, archaea
and bacteria, species numbers for Enchytraeids and Collembola,
trophic groups for nematodes, and amplicon sequence-data
grouped into family level for AMF (Table 1biodiversity). All of
the levels are further considered as taxonomic unit. Taxonomic
units (TU) that were present in only one sample per category (land
Table 1
Biological Indicators applied at 81 sites across Europe, to assess soil biodiversity or functions; C-cycling and nutrient (N&P) cycling.
Main Indicator
C storage and cycling
Extracellular enzyme activity
(EEA)
Multiple substrate induced
respiration (MicroResp)
Biolog
Measures
DNA yields
Enchytraeids
Nematodes
AMF families
Nematode
Nitrication potential
Functional Gene A
L_Arginine, L-asparagine, L-phenylalanine, L-serine, N-acetyle-D-glucosamine, L-threonine, Dglucosaminic acid, glycyl-L-glutamic acid, phenyl-ethylamine, putrescine
Amount of NO2-N released (ng/g soil dm/h)
nosZ1 (denitrier) gene, nosZ2 (denitrier) gene
Functional Gene B
AOB (Bacteria: ammonia oxidizers) gene; AOA (Archea: ammonia oxidizers) gene
Molecular microbial biomass
(ng microbial DNA g soil-1)
Fungal abundance and richness Fungal copy numbers, fungal richness
Biodiversity
Enchytraeid
Nematode
Collembola
AMF families
archaea, bacteria and fungi
Species diversity
Feeding guild richness
Species richness
Acaulosporaceae, Ambisporaceae, Archaeosporaceae, Claroideoglomeraceae, Diversisporaceae,
Gigasporaceae, Glomeraceae, Pascisporaceae, Paraglomeraceae
T-RFLP copies per ng DNA (abundance); Dikarya Richness;
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ecosystem function as affected by land use across Europe, Appl. Soil Ecol. (2015), http://dx.doi.org/10.1016/j.apsoil.2015.08.006
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All suitable biological measurements (Table 1nutrient cycling) were included in the analysis, and all non-standardized
parameters were log-transformed before inclusion in the model.
Based on amount of explained variance, and the Akaike information criterium (AIC), we selected the most parsimonious model for
predicting nutrient cycling. This procedure was also executed with
normalised N mineralisation and inversely normalised P availability as dependent variables separately, to disentangle the respective
nutrient cycles. Statistical analyses were carried out using SPSS
(20.0.0) and R (R Core Development Team, 2012).
3. Results
3.1. Review of soil properties and measurements
In total, 76 sites were analysed from the 81 sites sampled (Stone
et al., this issue), as these sites had a complete set of parameters.
Table 2 shows the range of soil properties for the 76 sites; SOC
ranged from 0.45% to 51.1% (Fig. 2a), lowest mean SOC was found in
arable sites, while the highest SOC concentrations were found in
forest sites. pH varied considerably across sites, ranging from 3.7 to
8.2, with the lowest mean pH found in forest sites and highest
mean pH in arable sites (4.99 and 7.07, respectively). Soil texture
varied across all sites and is represented in this paper by clay
content. Clay content varied from <1% to 70%.
3.2. Co-occurrence of soil organisms
To investigate the biological diversity associated with the main
drivers of biological activity described across Europe, co-occurrence patterns of TUs were created using network inference for
each land use type, SOC category and pH group (Figs. 3, 4 and 6). It
was not feasible to create co-occurrence patterns for biogeographical zones, due to the low number of sites within the Boreal and
Mediterranean zones. The size of the node represents the diversity
of a given TU. However, this information is dependent upon the
method applied to derive the diversity data. Within this study,
different methodologies were applied to derive community
assemblage information, for example the TRFLP method provides
a large number of peaks described as ngerprints providing
information on the genetic structure of the community targeted,
whereas nematode and Collembola identication are only given to
trophic groups and species, respectively. Therefore the size of the
node cannot be used as an indication of diversity of a specic TU.
The thickness of the line connecting different TUs, represents the
percentage of possible connections that are signicantly correlated
for a specic combination of TU connections. Using the percentage
of signicant correlations from possible connections instead of
absolute numbers corrects for the difference in number of TUs per
Table 2
Summary of soil properties.
Land use within
biogeographical zone
No. of
sites
SOC mean
(%)
SOC St.
dev
P mean
(mg/l)
P Std
dev
N min (mg N kg
dry soil)
Grass_Continental
Grass_Atlantic
Grass_Mediterranean
Grass_Alpine
Arable_Continental
Arable_Atlantic
Arable_Mediterranean
Arable_Alpine
Forest_Continental
Forest_Atlantic
Forest_Alpine
Forest_Boreal
11
13
2
8
10
13
2
1
5
5
2
4
6.18
4.48
1.65
6.18
1.76
2.06
1.28
3.17
9.07
4.27
12.68
32.08
4.98
2.19
0.11
2.89
0.43
1.34
0.63
0.00
6.24
1.79
4.55
15.28
64.21
68.58
69.86
105.20
156.12
137.09
17.54
27.33
46.43
39.40
54.67
121.72
49.89
52.50
30.30
101.19
130.88
109.85
19.66
0.00
51.97
50.46
51.04
62.18
435.28
361.41
133.77
488.25
168.61
159.53
97.58
207.43
383.62
288.61
637.88
540.27
N min Std
dev
pH
mean
pH Std
dev
Clay mean
(%)
Clay Std
dev
284.24
146.24
4.08
114.29
33.66
77.48
14.94
0.00
180.83
92.76
361.26
228.30
6.36
6.24
7.41
6.16
6.89
7.13
7.17
7.78
5.20
5.32
5.56
4.02
1.06
0.96
0.20
0.92
0.74
0.86
1.51
0.00
1.59
0.85
2.16
0.13
30.7
27.2
20.0
28.8
25.5
23.3
21.5
57.0
22.8
20.6
36.0
14.0
14.0
15.6
4.2
10.0
13.3
18.7
16.3
0.0
16.1
13.3
19.8
0.0
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ecosystem function as affected by land use across Europe, Appl. Soil Ecol. (2015), http://dx.doi.org/10.1016/j.apsoil.2015.08.006
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Fig. 2. (a) Soil organic carbon content by land use within biogeographical zone. The
x-axis description is provided by (b) and (c). N mineralisation potential by land use
within biogeographical zone. The x-axis description is provided by (c). P availability
summarised by land use within biogeographical zone.
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Fig. 3. (a) Network of biotic interaction based on signicant positive Spearman correlations in each land use type. The nodes are sized to the number of species included in the
analyses. The size and darkness of the connecting edges is sized to the proportion of signicant positive correlations from all possible correlations between taxonomic units in
the land-use type. For arable soils the threshold for positive interaction was Spearman correlation >0.40, for grasslands >0.35 and for forests >0.45, respectively. Land use
categories were classied on the basis of Stone et al., 2015 (this issue). (b) Top 20 connected species in the three land-use categories (i) arable, (ii) grassland and (iii) forests.
Colour legend indicates the following; fungi (pink), archeae (purple), bacteria (blue), enchytraeids (green), collembolan (orange), nematodes (light blue-turqouise) and AMF
(dark red).
Fig. 4. Network of biotic interaction based on signicant positive Spearman correlations in each organic matter (SOC%) category. The nodes are sized to the number of species
included in the analyses and their darkness is relational to the connectedness of the node to other nodes. The size and darkness of the connecting edges is sized to the
proportion of signicant positive correlations from all possible correlations between taxonomic units in each organic matter% category. For soils with organic matter% <2 the
treshold for positive interaction was Spearman correlation >0.44, for soil with org matter 215% >0.27 and for soils with organic matter >15% >0.77, respectively. Carbon
categories were classied on the basis of Stone et al., 2015 (this issue).
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ecosystem function as affected by land use across Europe, Appl. Soil Ecol. (2015), http://dx.doi.org/10.1016/j.apsoil.2015.08.006
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Fig. 5. Fungal rst degree networks in different organic matter categories. All signicant connections between fungi (red) and the other organisms are depicted here. The
darkness of the edges is scaled to the interaction strength and the size of the nodes to the average abundance of the TRFs in each organic matter category. Interactions between
fungal TRFs are not drawn. Colour legend indicates the following; fungi (pink), archeae (purple), bacteria (blue), enchytraeids (green), collembolan (orange), nematodes (light
blue-turqouise) and AMF (dark red).
Please cite this article in press as: R.E. Creamer, et al., Ecological network analysis reveals the inter-connection between soil biodiversity and
ecosystem function as affected by land use across Europe, Appl. Soil Ecol. (2015), http://dx.doi.org/10.1016/j.apsoil.2015.08.006
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Fig. 6. Network of biotic interaction based on signicant positive Spearman correlations in each pH category. The nodes are sized to the number of species included in the
analyses and their darkness is relational to the connectedness of the node to other nodes. The size and darkness of the connecting edges is sized to the proportion of signicant
positive correlations from all possible correlations between taxonomic units in the land-use type. For pH<5 the treshold for positive interaction was Spearman correlation
>0.57, for pH 57 correlation >0.31 and for pH >7 correlation >0.38, respectively. pH categories were classied on the basis of Stone et al., 2015 (this issue).
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Please cite this article in press as: R.E. Creamer, et al., Ecological network analysis reveals the inter-connection between soil biodiversity and
ecosystem function as affected by land use across Europe, Appl. Soil Ecol. (2015), http://dx.doi.org/10.1016/j.apsoil.2015.08.006