LETTERS
PUBLISHED ONLINE: 29 JANUARY 2012 | DOI: 10.1038/NCLIMATE1368
Land use alters the resistance and resilience of
soil food webs to drought
Franciska T. de Vries1 *, Mira E. Liiri2 , Lisa Bjørnlund3 , Matthew A. Bowker4 , Søren Christensen3 ,
Heikki M. Setälä2 and Richard D. Bardgett1
Soils deliver several ecosystem services including carbon
sequestration and nutrient cycling, which are of central importance to climate mitigation and sustainable food production1–3 .
Soil biota play an important role in carbon and nitrogen
cycling, and, although the effects of land use on soil food
webs are well documented4–6 , the consequences for their resistance and resilience to climate change are not known. We
compared the resistance and resilience to drought—which is
predicted to increase under climate change2,7 —of soil food
webs of two common land-use systems: intensively managed
wheat with a bacterial-based soil food web and extensively
managed grassland with a fungal-based soil food web. We
found that the fungal-based food web, and the processes of
C and N loss it governs, of grassland soil was more resistant,
although not resilient, and better able to adapt to drought
than the bacterial-based food web of wheat soil. Structural
equation modelling revealed that fungal-based soil food webs
and greater microbial evenness mitigated C and N loss. Our
findings show that land use strongly affects the resistance
and resilience of soil food webs to climate change, and that
extensively managed grassland promotes more resistant, and
adaptable, fungal-based soil food webs.
Soils deliver a range of ecosystem services. They not only provide
nutrients for crop growth, but also store significant quantities of
C and N, which contributes to climate mitigation8 and sustainable
food production1–3 . The soil organisms that drive processes of C and
N cycling are significantly affected by land use and the intensity of
agricultural management9 : not only can agricultural intensification
reduce the diversity of soil biota4,6 , but it can also induce shifts in the
composition of soil communities from fungal- to bacterial-based
food webs4–6 . It has been suggested that fungal-based soil food webs,
which are common in extensively managed farming systems9,10 ,
are better able to withstand climate change-related disturbances
than are bacterial-based soil food webs11,12 . Moreover, because
fungal-based soil food webs are linked to increased soil C and N
retention5,13–17 , it is likely that they will also better retain C and
N under climate-change-related disturbances than bacterial-based
soil food webs. However, it has also been suggested that fungalbased soil food webs would recover slowly after climate changerelated disturbances, because slow-growing organisms, including
fungi and fungal-feeding fauna, tend to be more resistant (that
is, have greater ability to withstand a disturbance)18 , but less
resilient (that is, have lower rate of recovery after a disturbance)18 ,
than fast-growing organisms such as bacteria and bacterial-feeding
fauna11,18–20 . So far these ideas remain untested, and therefore
the consequences of land use for the resistance and resilience of
soil food webs and processes of C and N loss to climate-induced
disturbances, such as drought, are not known.
Here, we tested how contrasting agricultural land use affects the
resistance and resilience of soil food webs and soil C and N loss
to drought, which is predicted to increase under climate change2,7 .
Specifically, we tested the hypothesis that fungal-based soil food
webs, and the processes of C and N loss that they govern, are
more resistant to drought than their bacterial-based counterparts.
To test this hypothesis, we used two land use systems, namely
extensively managed grassland with a fungal-based food web and
an intensively managed wheat system with a bacterial-based food
web. Effects of prolonged drought on soil food webs, including
the microbial community, protozoa, nematodes, enchytraeids and
microarthropods, were first tested in the field in both land-use
systems (Methods and Supplementary Methods). Subsequently,
the resistance and resilience of these soil food webs to simulated
drought was tested using a laboratory assay on soils taken from
the field experiment (Methods). Here, soil-food-web responses
were measured at the end of the laboratory-based drought,
and 1, 3, 10 and 77 days after rewetting. We constructed a
soil-food-web model (Supplementary Fig. S1) to calculate total
biomasses of the fungal and bacterial energy channels21 , and we
used evenness of microbial phospholipid fatty acids (PLFAs) as
a measure of changes in microbial communities (Supplementary
Methods). We also measured key processes that are carried out
by the soil food web and represent C and N loss pathways: CO2
and N2 O production, and N leaching in drainage waters. To
quantify the immediate effect of drought on the soil food web
and C and N losses, and their rate of recovery after rewetting,
resistance and resilience indices were calculated22 . The resistance
index calculates the absolute amount of change relative to the
control at the end of the disturbance, and ranges from −1 to
+1, with +1 indicating maximum resistance (that is, no effect of
drought). The resilience index calculates the absolute difference
that exists between drought and control treatments relative to the
initial absolute effect of the disturbance, and ranges from −1 to
+1, with +1 indicating maximum resilience (that is, complete
recovery after rewetting).
The grassland and wheat soils had more fungal-based and
bacterial-based food webs, respectively (Supplementary Table S1).
Field drought reduced bacterial-channel biomass (that is, bacteria
and bacterial-feeding fauna) in both soils, but had contrasting
effects on fungal-channel biomass (fungi and fungal-feeding fauna).
In particular, field drought reduced fungal-energy-channel biomass
1 Soil
and Ecosystem Ecology, Lancaster Environment Centre, Lancaster University, Lancaster LA1 3EX, UK, 2 University of Helsinki, Department of
Environmental Sciences, Niemenkatu 73, FIN-15140, Lahti, Finland, 3 Biologisk Institut, Terrestrisk Økologi, Øster Farimagsgade 2D, 1353 København K,
Denmark, 4 Southwest Biological Science Center, US Geological Survey, PO Box 5614, Building 56 No 150, Flagstaff, Arizona 86011, USA.
*e-mail: [email protected].
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NATURE CLIMATE CHANGE DOI: 10.1038/NCLIMATE1368
LETTERS
Resistance index
a
Fungal-channel biomass
Wheat
field
Bacterial-channel biomass
1.00
PLFA evenness
0.98
0.96
0.94
0.92
0.90
0.88
Grassland
Wheat
field
0.86
Grassland
Wheat
field
0.9
0.8
0.7
0.6
0.5
0.4
0.3
0.2
0.1
0
Microarthropod richness
Grassland
Wheat
field
Control
Field drought
Resilience index
Grassland
1.0
0.9
0.8
0.7
0.6
0.5
0.4
0.3
0.2
0.1
0
1.0
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0
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0.2
0
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0
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1.0
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0.6
0.4
0.2
0
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Grassland
Resilience index
b
1.0
0.9
0.8
0.7
0.6
0.5
0.4
0.3
0.2
0.1
0
1.0
0.8
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0
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0
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1.0
0.8
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0.2
0
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1.0
0.8
0.6
0.4
0.2
0
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¬1.0
Wheat
field
1
3
10
77
Time after rewetting (days)
1
3
10
77
Time after rewetting (days)
1
3
10
77
Time after rewetting (days)
1
3
10
77
Time after rewetting (days)
Figure 1 | Resistance and resilience of soil food webs to a laboratory drought as affected by a previous field drought. a, Soil-food-web resistance to a
laboratory-based drought as affected by a previous field drought. Field drought increased resistance of fungal-channel biomass and evenness of
microbial PLFAs in grassland soil (field × drought interaction F1,12 = 9.1, P = 0.011, and F1,12 = 17.7, P = 0.001, respectively). Resistance of microarthropod
richness was higher in grassland than in wheat-field soil (F1,12 = 10.9, P = 0.006). Resistance of fungal-channel biomass to drought was greater than
resistance of bacterial-channel biomass (paired-samples T-test, t15 = 4.51, P < 0.001). b, Soil-food-web resilience following a laboratory-based drought as
affected by a previous field drought. Field drought reduced resilience of the soil food web in grassland, but not in wheat-field soil (field × drought
interactions for fungal-channel biomass F1,48 = 73.9, P < 0.001, bacterial-channel biomass F1,48 = 26.6, P < 0.001, evenness of microbial PLFAs
F1,48 = 39.7, P < 0.001). Resilience of microarthropod richness was higher in wheat-field soil than in grassland soil (F1,48 = 29.4, P < 0.001). Resilience of
fungal-channel biomass was lower than resilience of bacterial-channel biomass (paired-sample T-test, t63 = −6.42, P < 0.001). Markers denote treatment
means ± 1 s.e.m. (n = 4).
under wheat, but increased this measure, and the diversity
and richness of microarthropods, in grassland (Supplementary
Table S1). The response of microarthropods to field drought
might have been caused by increased dissolved organic C and
fungal biomass (Supplementary Table S1), as changes in resource
availability are known to be key drivers of microarthropod
community structure in grassland23 . In the laboratory, the fungal
energy channel was more resistant (Fig. 1a), but less resilient
(Fig. 1b), to drought than the bacterial energy channel, regardless
of from which land use the soil originated. Also, after rewetting,
bacterial, but not fungal, PLFAs decreased, indicating that bacteria
are less resistant to rewetting than fungi (Supplementary Fig. S4).
In addition, microarthropod richness had a greater resistance to
the laboratory-based drought in grassland than wheat soil (Fig. 1a).
Moreover, drought in the field significantly increased the resistance
of the fungal energy channel and the evenness of microbial PLFAs
to the second laboratory-based drought in grassland soil, but
not in wheat soil. This increase in resistance after field drought
suggests adaptation of the fungal-based food web of grassland
soil to drought, but it was traded off by a decreased resilience
to the laboratory-based drought (Fig. 1b). In general, our results
indicate a trade-off between resistance and resilience in soil food
webs, which is consistent with theoretical publications on resistance
and resilience11,18,19 .
2
Losses of C (CO2 production) and N (leaching in drainage
waters) were also more resistant to laboratory-based drought
in grassland than in wheat soil (Fig. 2a). Grassland soil had
greater amounts of readily available C and a higher absolute
respiration in the field and at the start of the incubation experiment
(Supplementary Fig. S2 and Table S1), and resistance of CO2
production to laboratory-based drought was higher in grassland
than in wheat soil. The positive relationship between respiration
and microbial growth (Supplementary Fig. S3), and the rapid
increase of fungal and bacterial PLFAs after rewetting in grassland
soil (Supplementary Fig. S4), indicate that the grassland microbial
community more efficiently incorporated the flush of readily
available C caused by drought15 . Adding to this, resilience of
CO2 production was highest in the grassland field-control soil
(Fig. 2b). Not only was N leaching from grassland soil more
resistant to drought, but it was also lower during the whole
experiment (including field-based measurements) than from wheat
soil (Supplementary Fig. S5 and Table S1). This corresponds
with the notion that N leaching is less from fungal-based than
bacterial-based soils5,14 . Field drought decreased the resistance of N
leaching to laboratory drought; this was traded off by an increased
resilience (Fig. 2b). We were unable to calculate a resistance index
of N2 O production owing to negative values in the control,
which indicates N2 O consumption in some treatments24 . However,
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NATURE CLIMATE CHANGE DOI: 10.1038/NCLIMATE1368
Wheat
field
3
10
77
Time after rewetting (days)
1.0
0.8
0.6
0.4
0.2
0
¬0.2
¬0.4
¬0.6
¬0.8
¬1.0
1.0
0.8
0.6
0.4
0.2
0
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¬1.0
N leaching
Control
Field drought
Grassland
Wheat
field
3
10
77
Time after rewetting (days)
Resilience index
Resistance index
Grassland
1.0
0.9
0.8
0.7
0.6
0.5
0.4
0.3
0.2
0.1
0
1.0
0.8
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0
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Resilience index
1.0
0.8
0.6
0.4
0.2
0
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CO2
Resilience index
Resilience index
1.0
0.8
0.6
0.4
0.2
0
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Resilience index
b
0
¬0.1
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¬1.0
Resilience index
Resistance index
a
LETTERS
1.0
0.8
0.6
0.4
0.2
0
¬0.2
¬0.4
¬0.6
¬0.8
¬1.0
N2O
Grassland
Wheat
field
3
10
77
Time after rewetting (days)
Figure 2 | Resistance and resilience of C and N losses to a laboratory drought as affected by a previous field drought. a, Resistance of CO2 production
and N leaching to a laboratory-based drought as affected by a previous field drought. Resistance of both respiration and N leaching was higher in grassland
than in wheat-field soil (F1,12 = 9.1, P = 0.011, and F1,12 = 33.7, P < 0.001, respectively). Resistance of N leaching was reduced by field drought (F1,12 = 26.7,
P < 0.001), but more so in grassland soil (field × field-drought interaction F1,12 = 4.0, P = 0.069). b, Resilience of CO2 production, N leaching and N2 O
production following a laboratory-based drought as affected by a previous field drought. Resilience of respiration at the end of the experiment was highest
in grassland soil control (field × field-drought × sampling-date interaction F2,36 = 6.4, P = 0.004). Field drought increased resilience of N leaching
(field × field-drought interaction F1,36 = 6.3, P = 0.017), but reduced resilience of N2 O production in grassland soil (field × field-drought interaction
F1,36 = 6.3 and F1,36 = 4.2, P = 0.049, respectively). Markers denote treatment means ±1 s.e.m. (n = 4).
laboratory drought significantly increased N2 O production in
grassland (Supplementary Fig. S6), but not in wheat soil. This, and
the higher N2 O production rates in grassland soil throughout the
experiment, was probably a consequence of higher C availability.
However, differences in soil structure and availability of anaerobic
microsites, which is probably greater in grassland soil, might
also have contributed25 . Still, rates of N2 O production recovered
faster in grassland field-control soil than in wheat field-control
soil following rewetting (Fig. 2b), which further points to more
efficient incorporation of excess C in the fungal-based soil food
web of grassland.
We constructed a structural equation model to test the
hypothesis that soil-food-web characteristics exerted a direct
influence over soil C and N losses in the laboratory experiment
(Supplementary Fig. S7). Because we wanted to focus on the
interactions of soil biota and their relative influence on C and N
losses across all treatments, we used residuals of the full-factorial
analysis of variance model for the modelling (Supplementary
Methods). Because of this step, variation in the data caused by
treatment effects or biophysical differences among wheat fields
and grasslands (for example soil nutrient and C availability)
cannot influence the outcome of our model. After these treatment
effects had been removed, the residual variance in soil-food-web
characteristics and C and N fluxes (ranging from 10.9 to 64.7%,
Fig. 3) fed into the structural equation model. A significant
proportion of this variance in C and N fluxes was explained
by variance in soil-food-web characteristics (Fig. 3). Throughout
the laboratory experiment, a high fungal/bacterial channel ratio
was associated with lower amounts of C lost through respiration
(Fig. 3a–d), which is consistent with our observation that the more
fungal-based grassland microbial community incorporated C more
efficiently. Greater evenness of microbial PLFAs was associated with
reduced loss of N through leaching, and after 10 days (Fig. 3c)
increased microarthropod richness. Increased microarthropod
richness can stimulate N mineralization26 , which here—in the
absence of plant N uptake—led to increased N leaching from
soil (Fig. 3d). In addition, respiration—a measure of heterotrophic
microbial activity—strongly controlled N cycling. Respiration
positively influenced N2 O production at the first sampling
date, suggesting that C availability controlled denitrification.
It also exerted a negative control on N leaching across all
sampling dates (Fig. 3).
In conclusion, our data show that differences in soil food webs
resulting from agricultural land use have significant implications
for their resistance and resilience under drought, and that this has
consequences for the loss of C and N from soil. Specifically, we show
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NATURE CLIMATE CHANGE DOI: 10.1038/NCLIMATE1368
5
F/B channel
ratio
¬0.29P < 0.001
¬0.08
0.0
5
.08
¬0
¬0
.0
3
R2 = 0.02
¬0.14P = 0.04
Respiration
PLFA
evenness
¬0.10P = 0.03
5
2
0.0
0.0
8
0.0
R2 = 0.12
Total N
leached
¬0.06
0.0
0
¬0.39P < 0.001
0.08
R2 = 0.04
N2O
production
0.17
P=
0
R2 = 0.01
Microarthropod
richness
R2 = 0.14
Total N
leached
¬0.16P = 0.03
3
0.4
¬0.16P = 0.03
5
0.0
PLFA
evenness
2
.01
¬0
0.1
2
R2 = 0.07
Respiration
1
0.0
0.1
Respiration
¬0.27P < 0.001
¬0.25P = 0.04
77 days
R2 = 0.05
¬0.20P = 0.04
0
¬0
.06
¬0.05
0..0
5
0.08P = 0.006
.08
¬0
.05
PLFA
evenness
d
.08
¬0
¬0
¬0.08
7
0.0
¬0.13
0
0.08
R2 = 0.03
N2O
production
0.17
R2 = 0.04
N2O
production
0.17
5
0.0
R2 = 0.01
R2 = 0.01
Microarthropod
richness
F/B channel
ratio
R2 = 0.25
Total N
leached
¬0.26P = 0.03
Microarthropod
richness
F/B channel
ratio
4
0.0
.01
¬0
0.1
1
3 days
R2 = 0.02
Respiration
PLFA
evenness
10 days
¬0
.03
b
0.10
.06
¬0
¬0.14P = 0.04
F/B channel
ratio
c
R2 = 0.32
N2O
production
¬0.17
0.51P < 0.001
R2 = 0.02
Microarthropod
richness
¬0.24P < 0.001
1 day
0.08
a
¬0.07
LETTERS
R2 = 0.30
Total N
leached
Figure 3 | Relationships between remaining variance in soil-food-web characteristics and C and N fluxes, after variance accounted for by experimental
treatments has been removed, 1, 3, 10 and 77 days after rewetting. Residual variances that fed into the structural equation model were as follows:
microarthropod richness 42.2%, F/B channel ratio 52.2%, PLFA evenness 19.9%, respiration 21.3%, N2 O 64.7%, total N leached 10.9%. The weight of the
arrows indicates the strength of the causal relationship, supplemented by a path coefficient. R2 values denote the amount of variance explained by the
model for the response variables. Our overall model fit was satisfactory (χ 2 = 64.1, P = 0.24; RMSEA = 0.033, P = 0.754).
that fungal-based food webs of grassland soil, and the processes of
C and N loss that they govern, are more resistant to drought than
are bacterial-based food webs of more intensively managed wheat
soil. Importantly, the resistance of the grassland soil food web was
increased after the field drought, which suggests that it adapts to
a changing climate. Moreover, we show that, across both land-use
systems, more fungal-based soil food webs and a greater evenness
of microbial PLFAs mitigated the effects of drought on processes of
C and N loss from soil. Collectively, our findings show that land use
alters the stability of soil food webs and the ecosystem services that
they deliver under climate change.
were calculated as RS(t0 ) = 1 − (2|D0 |)/(C0 + |D0 |), with C0 the value of the
control at the end of the disturbance and |D0 | the absolute difference between
the control and the disturbed soil22 . Resilience indices were calculated as
RL(tx ) = (2|D0 |)/(|D0 | + |Dx |) − 1, with |Dx | the absolute difference between
the control and the disturbed soil at time x (ref. 22). Resistance indices were
analysed using two-way analysis of variance with factors land use and field drought;
resilience indices were analysed using three-way analysis of variance with factors
land use, field drought and sampling time, using PASW Statistics 17.0 (2009
SPSS). We constructed our structural equation model in Amos 18.0 (2009 SPSS),
using the multigroup modelling approach to track changes in the strength of the
pathways in the model. We confirmed adequate model fit with the χ 2 test and
the RMSEA index. A full description of the modelling procedure is available in
Supplementary Methods.
Methods
Received 28 February 2011; accepted 6 December 2011;
published online 29 January 2012
The field experiment was located in the south of England (51◦ 320 55.2000 N,
1◦ 040 37.4400 W) and consisted of grassland and wheat field on the same slope
and the same soil type. Field drought was simulated by randomly placing three
transparent roofs (1.6 m × 1.6 m) in each field for three months (April–July
2009). After this, soil was collected from droughted and control plots. Soil
from each treatment was transferred into 1 l pots, rewetted to 60% water
holding capacity (WHC), and used for the full-factorial drought experiment
(field × field drought × laboratory drought × 5 sampling dates, each treatment
replicated four times, resulting in 160 pots) in the greenhouse (20 ◦ C, day/night
16 h/8 h, randomized block design). During two weeks, drought pots were dried
to, and kept at, 20% WHC versus control pots that were kept at 60% WHC.
Successively, all pots were rewetted and kept at 60% WHC for 2.5 months.
A full description of the set-up of the field and the laboratory experiment, N
and C loss measurements, and soil microbial and faunal analyses and biomass
calculations is available in the Supplementary Methods. Resistance indices
4
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Acknowledgements
This project was part of the EU Seventh Framework funded SOILSERVICE project, led
by K. Hedlund. We thank all project partners for contributing to this manuscript through
discussions. We thank S. Mortimer and D. Carpenter for setting up the field experiment,
and G. Hildred for allowing us into his fields. H. Quirk, L. Trimnell, V. van Velzen,
A. Spangenberg, L. F. Petersen, I. Dodd, G. Mies, F. Willeboordse, B. v/d Waterbeemd,
C. Siderius, E. Wilson and K. Wilson helped with field and laboratory work. We thank
K. Orwin and W. van der Putten for commenting on the manuscript.
Author contributions
R.D.B., H.M.S., S.C., F.T.d.V., M.E.L. and L.B. had the original idea for the experiment.
F.T.d.V. set up the experiment, and laboratory work was conducted by F.T.d.V., M.E.L.
and L.B. M.A.B. carried out the structural equation modelling. The manuscript was
written principally by F.T.d.V. and R.D.B., with extensive input from H.M.S., S.C.,
M.E.L., L.B. and M.A.B.
Additional information
The authors declare no competing financial interests. Supplementary information
accompanies this paper on www.nature.com/natureclimatechange. Reprints and
permissions information is available online at http://www.nature.com/reprints.
Correspondence and requests for materials should be addressed to F.T.d.V.
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