Ecology Letters, (2016) 19: 249–259 doi: 10.1111/ele.

12560

LETTER Low multifunctional redundancy of soil fungal diversity at

multiple scales

Abstract
Akira S. Mori,1* Forest Isbell,2 Theory suggests that biodiversity might help sustain multiple ecosystem functions. To evaluate
Saori Fujii,1 Kobayashi Makoto,3 possible biodiversity–multifunctionality relationships in a natural setting, we considered different
Shunsuke Matsuoka4 and Takashi spatial scales of diversity metrics for soil fungi in the northern forests of Japan. We found that
Osono4 multifunctionality increased with increasing local species richness, suggesting a limited degree of
1
multifunctional redundancy. This diversity–multifunctionality relationship was independent of the
Graduate School of Environment
compositional uniqueness of each community. However, we still found the importance of commu-
and Information Sciences, Yoko-
nity composition, because there was a positive correlation between community dissimilarity and
hama National University, Yoko-
multifunctional dissimilarity across the landscape. This result suggests that functional redundancy
hama, Kanagawa 240-8501, Japan
2
can further decrease when spatial variations in identities of both species and functions are simulta-
Department of Ecology, Evolution
neously considered at larger spatial scales. We speculate that different scales of diversity could
and Behavior, University of
Minnesota, Saint Paul, MN 55108,
provide multiple levels of insurance against the loss of functioning if high-levels of local species
USA
diversity and compositional variation across locations are both maintained. Alternatively, making
3
Field Science Center for Northern
species assemblages depauperate may result in the loss of multifunctionality.
Biosphere, Hokkaido University,
Otoineppu 438, Otoineppu, Keywords
Hokkaido 098-2501, Japan Belowground processes, biodiversity-ecosystem functioning, compositional characteristics, ecosystem
4
Center for Ecological Research, multifunctionality, forest biodiversity, functional redundancy, multifunctional dissimilarity, scale
Kyoto University, Otsu, Shiga dependency, species importance.
520-2113, Japan
Ecology Letters (2016) 19: 249–259
*Correspondence: E-mail: akira.
s.mori@gmail.com

identity) can be a major determinant for overall functionality

INTRODUCTION
There are currently increasing concerns and demands for con-
serving biodiversity worldwide. These concerns primarily
result from substantial declines in biodiversity at various spa-
tial, temporal and biological scales, which have been globally
recognised for the last several decades (Butchart et al. 2010).
Concurrently, there is a growing body of scientific evidence
indicating that biodiversity is not merely a response variable
to environmental changes but also a predictor of various
ecosystem functions and services (Duffy 2009; Cardinale et al.
2012; Balvanera et al. 2013), which are essential for sustaining
human wellbeing (MA 2005). Notably, the roles of biodiver-
sity for maintaining ecosystem functioning can be more
strongly realised when multiple functions are considered
simultaneously (Hector & Bagchi 2007; Zavaleta et al. 2010;
Isbell et al. 2011; Maestre et al. 2012; Byrnes et al. 2014; Lef-
check et al. 2015). These investigations of ‘ecosystem multi-
functionality’ are of practical importance because human
society does not rely on a single function or service, but
rather, in reality, requires multiple functions and services
obtained from nature.
An important issue in considering the roles of species
assemblages for promoting multiple ecosystem functions is
that of ‘low multifunctional redundancy’ (Mori et al. 2013);
i.e. species that are functionally redundant when a single func-
tion is considered can no longer be redundant when different
functions are simultaneously considered (Gamfeldt et al. 2008;
Zavaleta et al. 2010; Isbell et al. 2011). Such low redundancy
suggests that the functional uniqueness of species (species
of ecosystems, in addition to the fundamental importance of
the level of species diversity (e.g. a-diversity). Importantly, this
functional importance of individual species to support some
functions can become particularly significant for sustaining
multifunctionality when there is species turnover across space,
time or ecosystem functions. This is because no species can
always promote all functions at different locations and time-
points (Zavaleta et al. 2010; Isbell et al. 2011). Thus, to gain
a better picture of the diversity–multifunctionality relation-
ships and to carefully assess the possible redundancy among
species (Gamfeldt et al. 2008), it is also necessary to account
for variations in species composition among communities
(compositional characteristics).
Such a perspective base on different scales of diversity could
be especially important for maintaining the multifunctionality
of natural systems, where communities often show a large
variation in species composition across space and time.
Although a recent study in a model ecosystem (Pasari et al.
2013) shed light on the importance of compositional distinct-
ness among local communities (b-diversity) to promote
ecosystem functioning, it is still unknown whether such spatial
variations in compositional characteristics affect multifunc-
tionality in natural systems. In nature, communities that are
formed through natural assembly processes might contain
complementary suites of species that are better adapted to
local conditions (Pasari et al. 2013). Furthermore, real-world
situations are characterised by a skewed distribution (i.e.
unevenness) of species abundance (McGill et al. 2007), non-
random loss of species (Bracken et al. 2008; Selmants et al.

© 2015 John Wiley & Sons Ltd/CNRS

250 A. S. Mori et al.
2012), and higher levels of biodiversity than many biodiversity
experiments. Considering this reality, it is of practical impor-
tance to simultaneously quantify the possible effects of species
identity, species diversity and compositional characteristics of
species assemblages on ecosystem multifunctionality.
Given the scale-dependency of diversity–functioning rela-
tionships (Pasari et al. 2013), which is expected to be espe-
cially the case in natural systems (Chase & Leibold 2002), a
narrow focus on diversity at a single spatial scale may be
insufficient to determine the degree of functional redun-
dancy. With this issue in mind, we focused on soil microbes
(fungi) in forested areas of the northern Japan, which have
been managed for forest diversity conservation. While many
biodiversity experiments have manipulated plant diversity,
because much of the matter and energy in an ecosystem
flows through these primary producers, it is not always pos-
sible to, in a similar manner, culture and manipulate
microorganisms that are likely equally important for regula-
tion of ecosystem processes. Microbes, as a mega-diverse
groups of organisms, have traditionally tended to be consid-
ered highly redundant for individual ecosystem functions
(Nielsen et al. 2011). However, there is a possibility of low
multifunctional redundancy according to an analysis using a
microbial genome database (Miki et al. 2014). Given the
increasing interest in understanding causes and consequences
of changes in belowground diversity (Coleman 2008; Bard-
gett & van der Putten 2014), it is necessary to assess
whether there is high or low multifunctional redundancy in
natural soil assemblages.
Here, we hypothesised that ecosystem multifunctionality
depends on soil fungal diversity, and that this relationship in
turn depends on the focal spatial scale in a natural system.
Given the large natural variation in species composition
across local communities, we expect that functional redun-
dancy will decrease at larger spatial scales. To test these
hypotheses, we used a modern high-throughput amplicon
pyrosequencing of fungal metagenomes (Osono 2014) to
determine the richness and composition of soil fungal commu-
nities. Note that the information of species richness is
important to be comparable with earlier works for the diver-
sity–multifunctionality relationship developed using plant
assemblages and is also necessary to accurately evaluate the
degree of redundancy. We suspect that approaches such as
ours, which focus on different aspects of biological organisa-
tion, will broaden our understanding of the functional roles
that soil biota play, improving our ability to help conserve
multifunctionality in natural ecosystems.
MATERIALS AND METHODS
Study site
This study was conducted in lowland coastal areas in north-
western Shiretoko National Park in Hokkaido, the northern-
most island of Japan (latitude 44°080 to 110 , longitude 145°030
to 080 , altitude 140 to 220 m). This region is subjected to the
cold Northwest Asian monsoon during winter months. The
northwestern coast experiences an annual rainfall of c.
900 mm, an average maximum temperature in August of c.
© 2015 John Wiley & Sons Ltd/CNRS
Letter
22 °C, and an average minimum temperature in February of
about 16 °C. The United Nations Educational, Scientific
and Cultural Organization (UNESCO) have classified this
area as a World Natural Heritage site because it represents
one of the richest northern temperate ecosystems in the world
and exemplifies the interaction between marine and terrestrial
ecosystems (http://whc.unesco.org/en/list/1193). Approxi-
mately, 90% of the park’s terrestrial area is covered with pris-
tine natural vegetation (mostly mixed conifer-hardwood
forests). The remaining land area was used for agriculture in
the early 20th century, but settlers abandoned these areas by
the late 1960s. Since then, numerous forest restoration efforts
have been implemented, including re-vegetation activity and
establishment of fences (3–4 m tall) to prevent overgrazing by
large herbivores. The restoration area now consists of mosaics
of different vegetation types, including monoculture planta-
tions of larch (Larix kaempferi), mixture plantations of several
tree species (mainly Picea glehnii, Abies sachalinensis, and
Betula erimani) and treeless windswept lands dominated by a
dwarf bamboo (Sasa cernua).
Census procedures
In May 2013, we established six 10 m 9 10 m study plots in
each of the above three vegetation types within the restoration
area and in adjacent natural forests (24 plots in total). In all
four types of vegetation, we established half of the plots
within large herbivore exclosure areas (i.e. within fences). In
each plot, we established three 1 m 9 1 m subplots (72 sub-
plots in total). In late May 2013, we collected topsoil from a
depth of 0–5 cm in each subplot for the following analyses.
To minimise the damage to ground vegetation, these samples
were collected adjacent to the subplot boundary. The soil
samples were used to estimate fungal diversity, belowground
ecosystem functions, and soil physicochemical properties.
Fungal diversity was measured with metagenomics (Bunge
et al. 2014; Osono 2014). Details of DNA extraction, PCR
amplification, and pyrosequencing, as well as bioinformatics,
are described in Supporting Information S1. Species were
identified based on operational taxonomic units (OTUs;
Bunge et al. 2014), leading to total of 428 fungal OTUs (here-
after, referred to as species) from soil cores collected at 72
sampling locations (38.08  0.25 fungal species per sampling
location, mean  SE). For soil physicochemical properties,
we estimated soil water content, pH and amounts of total car-
bon (C) and nitrogen (N). Total C and N were measured
using a CN analyser (JM1000CN, JScience Lab, Kyoto,
Japan). In August 2013, a vegetation survey was conducted in
all plots. Species identity and size (diameter at breast height;
DBH) were determined for all trees with DBH larger than
5.0 cm. Tree species richness, abundance and total basal area
in each plot were then calculated.
Ecosystem functions
The ecosystem functions measured here included belowground
primary production, soil carbon sequestration, decomposition
rates for plant litter, amount of plant-available nitrogen, and
reduction of nitrogen leaching losses, all of which are funda-
mental to soil biogeochemical processes (Wall et al. 2012;
Letter
Bardgett & van der Putten 2014; Bradford et al. 2014; Wagg
et al. 2014).
For litter decomposition, we used standardised materials
(tea bags) for quantifying soil stabilisation factor (S), which
could be important considering the ability of soil to sequester
carbon, in addition to the potential for initial decomposition
in a given environment (k) (Keuskamp et al. 2013). Following
the protocol of the tea-bag index (TBI; Keuskamp et al.
2013), tea-bags were retrieved after 3 months (mid-June to
mid-September), and then mass remaining was measured to
obtain k and S indices. Following earlier work (Bradford
et al. 2014), we also used materials of aboveground litter col-
lected in the sites. In late-September 2013, we initiated field
experiments for plant litter decomposition in each subplot.
Quercus crispula (QC) and Senecio cannabifolius (SC) leaves
were used as litter. QC and SC are the most dominant and
representative tree and herb species in the region, respectively.
Litterbags were placed on the surface of the ground at each
subplot (close to the localities that the above soil cores were
collected) and then retrieved after 360 and 260 days for QC
and SC respectively. The percentage of mass lost relative to
the initial dry litter mass was calculated.
The production of fine roots (diameter < 2 mm) as a proxy
for belowground primary production was estimated using an
in-growth core method that sampled mineral soil to a depth
of 10 cm. In this region, most of the fine roots are distributed
on the surface of the soil (Fukuzawa et al. 2007). The sam-
pled soils were sieved through a 2 mm mesh. A 120 g (wet
weight) sieved soil subsample was placed into the in-growth
core (4.5 cm depth, 7.5 cm diameter). Ingrowth cores were
buried (close to the localities that the soil cores were taken) in
late-May (just after snowmelt) and removed at the end of
October 2013 (just before snow cover). The dry mass of the
fine roots that were present inside the excavated cores was
measured and represented fine root production. Inorganic
nitrogen leaching was estimated using the resin core method
(Zou et al. 1992). A polyvinyl pipe was filled with ion-
exchangeable resin, buried at a depth of 10 cm in topsoil
(close to the localities the soil cores were taken) and incubated
from late May to late October 2013. The amount of nitrate
absorbed by the ion-exchange-resin was used as a proxy for
the amount of nitrogen leached from the surface soil. For cal-
culations of (multi)functionality, we used the inverse of these
values to quantify the reduction of nitrogen leaching. The
sum of ammonium and nitrate in sieved soil represented the
amount of plant-available nitrogen. Ion exchange resin and
sieved soil were extracted using 1-M KCl and 2-M KCl, respec-
tively, for the following analyses. Ammonium within extracts
was analysed by indophenol blue absorptiometry, and nitrate
within extracts was analysed by naphtyl ethylenediamine dihy-
drochloride spectrophotometry, using an auto analyser
(AACS-4, BL-TEC, Inc., Japan).
Data analyses
We used R software 3.0.2 (http://www.r-project.org/), with
‘vegan’, ‘lmerTest’, ‘multifunc’, and ‘glmmADMB’ libraries
for data analyses.
Low multifunctional redundancy of soil fungi 251
Community-level analyses
For community-level analyses, we examined effects of fungal
species richness and compositional characteristics of local fun-
gal assemblages on belowground multifunctionality. Addition-
ally, we used soil water content, soil acidity, soil C : N ratio,
tree diversity (the number of species), tree abundance and tree
basal area as possible environmental variables with which to
evaluate the diversity–functioning relationship in a natural,
unmanipulated setting (Gamfeldt et al. 2013).
First, to account for the differences in sequencing depth
between locations (116 to 912 with mean value of 437; Sup-
porting Information S1), fungal species richness (a-diversity)
was evaluated based on a rarefaction approach (Gotelli &
Colwell 2001) as often adopted elsewhere (Laliberte et al.
2014). Species richness was rarefied by randomly subsampling
116 annotated reads per sample. Second, the compositional
characteristics (b-diversity) was evaluated by Raup-Crick dis-
similarity to reduce the effects of a-diversity (Vellend et al.
2007). However, because this dissimilarity metric is not com-
pletely independent of a-diversity, we relied on a modified ver-
sion of the Raup-Crick dissimilarity metric (Chase et al.
2011). This metric is calculated using a null model, which gen-
erates species-level stochasticity by randomly drawing species
based on their observed frequency of occurrence within the
meta-community. The dissimilarity values between all pairs of
subplots were calculated with 9999 randomisations. The dis-
similarity values of this metric range between 1 and +1, with
negative and positive values indicating that species assem-
blages in two given localities share more or fewer species,
respectively, than randomly-expected from the meta-commu-
nity structure. To evaluate the compositional uniqueness of
soil fungi at each location, mean dissimilarity values were cal-
culated for each subplot. This averaged dissimilarity value
represents how a species assemblage in a given location is
compositionally unique (independent of species richness) com-
pared to the random expectation within the entire meta-com-
munity. Again, we rarefied fungal species richness in the
species 9 location matrix to correct for the disproportionate
effect of rare species on b-diversity. We excluded species that
occurred only once or twice in the meta-community from all
locations. We also confirmed that rarefaction did not substan-
tially affect our results regarding the effects of a- and b-diver-
sity on (multi)functionality (i.e. results analysed with no
rarefied dataset produced similar results).
We used several methods to evaluate the diversity–(multi)-
functionality relationship. First, we used the average multi-
functionality approach (Maestre et al. 2012), which is
straightforward and easily-understandable (Byrnes et al.
2014). Each function was standardised to common scale, and
the mean of these standardised values across all individual
functions in each location (subplot) was calculated to obtain
the average multifunctionality. We used a linear mixed effects
model (LMM) to evaluate the relationship of fungal species
richness or compositional uniqueness with average multifunc-
tionality. Plot was included as a random effect to account for
repeated measurements (three subplots) within each plot. To
consider the possibility that third variables may influence the
diversity–multifunctionality relationship in natural systems,
© 2015 John Wiley & Sons Ltd/CNRS
252 A. S. Mori et al.
we included all possible combinations of the environmental
variables and the random intercepts of vegetation types (four
categories) and fence presence/absence (two categories); conse-
quently, more than 200 candidate models were tested. The
best models were then selected using Akaike Information Cri-
terion (AIC). Following Gamfeldt et al. (2013), explanatory
variables were all centred and standardised.
Our second multifunctionality approach was a modified
average multifunctionality method. Instead of averaging the
standardised values of individual functions, we included the
identity of function (seven categories) as a random effect in
the LMM. Again, we selected the best models based on the
AIC values. In this second analysis, we also examined the
diversity–functioning relationship of each individual function.
Given the importance of quantifying responses of individual
functions in addition to evaluating the overall response of
multifunctionality to diversity changes (Bradford et al. 2014;
Byrnes et al. 2014), this approach was intuitive and enhanced
the visualisation and understanding of possible tradeoffs
between different functions. We standardised the values of the
seven functions prior to calculating correlations.
Our third multifunctionality approach was a multiple-
threshold multifunctionality method (Byrnes et al. 2014),
which explicitly incorporates tradeoffs between different func-
tions (Perkins et al. 2015) and which tests whether diverse
communities are more likely to support multiple functions at
high levels (Byrnes et al. 2014). This method evaluates the
relationships between diversity and the total number of func-
tions that have values greater than or equal to a threshold
(defined as a given percentage of the maximum observed rate
of each individual function, where the maximum was quanti-
fied as the mean of the seven highest values). We used the
threshold values between 5 and 95% at 1% intervals. To eval-
uate the effects of fungal species richness or compositional
uniqueness on multifunctionality, we used a generalised linear
mixed effects model (GLMM), with a negative binomial error
distribution and plot identity as a random effect. Again, the
best models were selected after comparing numerous candi-
date models with different combinations of environmental
variables and vegetation/fence categories. We used 20, 40, 60
and 80% of the threshold for model selection. We identified
the minimum threshold (Tmin), which is the percentage of
maximum functioning at which multifunctionality becomes
influenced by changes in diversity, and the realised maximum
effect of diversity (Rmde), which is the strength of the linear
relationships of diversity–multifunctionality (i.e. slope) where
diversity has the strongest effects.
The results of model selections for fungal species richness
and compositional uniqueness effects on multifunctionality,
which could be affected by environmental variables, are
shown in Table S1 through S6. Briefly, the best models of
diversity–multifunctionality relationships using a-diversity
(fungal species richness) consistently included soil water con-
tent and acidity as the environmental variables (Tables S1 and
S2). Models based on b-diversity (compositional uniqueness)
consistently included a random intercept of vegetation
category (Tables S3 and S4). Additionally, using the multiple-
threshold approach, we examined whether models with
different environmental or categorical variables affected
© 2015 John Wiley & Sons Ltd/CNRS
Letter
results. Excluding the selected environmental variables from
the best model of a-diversity-multifunctionality or adding
them to the best model of b-diversity-multifunctionality did
not substantially influence the results. We also confirmed that
similar results were obtained when we (1) ignored the lack of
statistical dependence between subplots and used a generalised
linear model (GLM) with a quasipoisson error and (2)
assumed a Gaussian distribution of the response variables and
used an LMM instead of GLMM. These confirmations help
compare our results with those of earlier studies (Bradford
et al. 2014; Perkins et al. 2015). We also verified that our
results were not substantially affected by the selection of
ecosystem functions (Fig. S1).
Species-level analyses
Species-level analyses are needed to determine the extent to
which same or different subsets of species are most important
for maintaining the high levels of different ecosystem func-
tions. This is because diversity effects on multifunctionality
could be significant even if species have high levels of func-
tional redundancy. For quantifying the functional importance
of species, we relied on the randomisation method of Gotelli
et al. (2011), which can be used in uncontrolled natural
assemblages. The species-specific value of functional impor-
tance is calculated as the difference between the average of
functionality where a given species is present and that where
the same species is absent. The standardised effect size (SES)
of this importance value is then quantified based on a null
model. If |SES| is higher than 1.96, then the observed value is
in the 5% tail of a normal distribution. If |SES| is lower than
1.96, the observed value is within the range expected by
chance. This standaridised metric is designed to take advan-
tage of natural variation in species composition and measure
differences in ecosystem function that are associated with this
variation (Gotelli et al. 2011).
Next, to calculate mean values of multifunctionality
required for the calculation of functional importance, we
excluded species that occurred only once or twice in the
meta-community from all locations. This rarefaction did not
substantially affect our results regarding the functional impor-
tance of each species. For the average multifunctionality
approach, we used the standardised values of multifunctiality
in each locality. We used 999 randomisations for the calcula-
tion of functional importance of each species, and repeated
the null modelling for all species. For the multiple threshold
approach, the functional importance of each species was
quantified as the difference in average number of functions
that have values greater than or equal to a threshold in locali-
ties where a target species is present and that in localities
where the same species is absent. We calculated the SES val-
ues of the functional importance for each species at each
threshold from 5 to 95% at 1% intervals. A single SES value
was individually calculated with 999 randomisations, and we
repeated the null modelling for all species at all threshold
levels.
Landscape-level analyses
To test whether and how spatial variation in species composi-
tion influences multiple functions, we analysed the relationship
Letter
between multifunctional dissimilarity and community dissimi-
larity (the modified Raup-Crick metric) across all pairs of
locations. The multifunctional dissimilarity was calculated
based on Euclidian distances using all standardised functions
that were used for the average multifunctionality approach.
The negative and positive dissimilarity values of this metric
indicate that species assemblages in two given localities simi-
larly or dissimilarly perform multiple functions, respectively.
We calculated partial Mantel correlations between community
dissimilarity and multifunctional dissimilarity, after excluding
the influences of geographical or environmental distance
between given pairs of locations (i.e. subplots). Environmental
distance was quantified using Gower distances, with
vegetation and plot identities used in the above model of
b-diversity-multifunctionality. Additionally, we included the
standardised values of water content and acidity (used in the
above model of a-diversity-multifunctionality) in environmen-
tal distances, which produced similar results.
RESULTS
Community-level analyses
After accounting for environmental covariates (Tables S1–S2),
the average multifunctionality significantly increased with
increasing fungal species richness (LMM, P < 0.05; Fig. 1a,b)
but showed no relationship with compositional uniqueness of
local assemblages (LMM, P > 0.05; Fig. 1c,d). When the
aggregated response of multifunctionality was disaggregated
to inspect the underlying individual functions, only two (herb
litter decomposition and reduction in nitrogen leaching) of
seven functions were positively affected by an increase in fun-
gal species richness (LMM, P < 0.05; Fig. 1b). The composi-
tional uniqueness was again not a significant explanatory
variable for any single function (LMM, P > 0.05; Fig. 1d). Of
21 possible combinations between individual functions, 13
showed no significant relationship (P > 0.05; Table 1). While
three pairs of functions showed a significant positive correla-
tion, five pairs showed a significant negative correlation
(P < 0.05; Table 1). When analysed with the multiple thresh-
old approach, there was a significantly positive relationship
between fungal species richness and multifunctionality
(GLMM, P < 0.05; Fig. 2a,b). Increasing species richness
started to significantly (GLMM, P < 0.05) increase multi-
functionality at a threshold of 65% of the maximum values
observed across all locations, with a peak diversity effect at a
threshold of 88% (Fig. 2b). We found an increase of 0.043
functions per addition of 1 species (Fig. 2b), indicating that
about 23 fungal species were needed to add an additional
function. Compositional uniqueness showed no relationship
with any threshold levels of local multifunctionality (GLMM,
P > 0.05; Fig. 2c,d).
Species-level analyses
The standardised functional importance (SES) based on the
average multifunctionality approach showed that, while no
species had a significantly negative effect on the multifunc-
tionality, 21 species were significantly more functionally
Low multifunctional redundancy of soil fungi 253
important than the null expectation (Fig. 3a; Supporting
information S2). Most species were not significantly more or
less functionally important than the null expectation (Fig. 3a).
The standardised functional importance (SES) based on the
multiple threshold approach similarly showed that the number
of species that were significantly more important than the null
expectation increased with increasing the threshold level of
multifunctionality (Fig. 3b; Supporting information S2),
despite the fact that most species were not significantly more
or less functionally important than the null expectation. The
mean SES values across species at each threshold significantly
increased with increasing the threshold level (ordinary least-
square regression, Slope = 0.0113, R2 = 0.49, F = 84.42,
P < 0.0001).
Landscape-level analyses
There was a positive correlation between community dissimi-
larity and multifunctional dissimilarity (Fig. 4). This positive
correlation remained significant after excluding the effects of
geographical or environmental isolation between local com-
munities (partial Mantel r = 0.071 and 0.115, respectively;
Fig. 4). That is, communities with similar compositional char-
acteristics tend to provide similar functions at similar levels,
independent of geographical proximities or similarities in envi-
ronmental conditions.
DISCUSSION
By focusing on soil fungal communities, we have tested the
scaling effects of biodiversity on ecosystem multifunctionality
and the associated multifunctional redundancy. Ours is, to
our knowledge, the first study that clearly shed light on this
issue in a natural-setting. Thus far, few studies have focused
on spatial dimensions of biodiversity–ecosystem functioning
relationships (Pasari et al. 2013). For translating the knowl-
edge of experimental diversity–multifunctionality studies into
practice, we envision that this perspective deserves to gather
further attention.
At the local scale, we found that multifunctionality signifi-
cantly increased with fungal species richness (Fig. 1a,b), sug-
gesting that maintaining local soil fungal diversity could help
sustain multifunctionality. Importantly, in spite of this posi-
tive contribution of diversity to overall ecosystem multifunc-
tionality, such positive effects of local fungal diversity was not
necessarily observed for all individual functions (Fig. 1b). This
is very likely due to potential tradeoffs among different func-
tions (Bradford et al. 2014; Byrnes et al. 2014; Lefcheck et al.
2015; Perkins et al. 2015). For example, an increase in fine-
root production for nutrient acquisition could lead to
decreased availability of inorganic nitrogen in soil (Nadelhof-
fer 2000), likely resulting in a negative correlation between the
amount of plant-available nitrogen and root productivity
(Table 1). An increase in plant-available nitrogen is often
associated with increased nitrogen leaching (MacDonald et al.
2002), likely resulting in another tradeoff (Table 1). Indeed,
consistent with a study on tree assemblages in natural systems
(Gamfeldt et al. 2013), we found positive, neutral or negative
relationships between fungal diversity and individual functions
© 2015 John Wiley & Sons Ltd/CNRS
254 A. S. Mori et al. Letter

(a) Slope: 0.0023* (b) Common slope: 0.0019*

1.00
0.7
Average multifunctionality

0.75

Functionality
0.6

0.50
●
Belowground productivity
0.5 Stabilizaiton factor (S)
0.25 Standardized decomposition (k)
Leaf litter decomposition (Tree)
Leaf litter decomposition (Herb)
Plant-available nitrogen
0.4 Reduction of nitrogen leaching
0.00
10 20 30 10 20 30
Species richness Species richness

(c) Slope: 0.0285n.s. (d) Common slope: 0.0264n.s.

1.00
0.7
Average multifunctionality

0.75
Functionality

0.6
0.50

Belowground productivity
0.5 Stabilizaiton factor (S)
0.25 Standardized decomposition (k)
Leaf litter decomposition (Tree)
Leaf litter decomposition (Herb)
Plant-available nitrogen
0.4 Reduction of nitrogen leaching
0.00
−0.6 −0.3 0.0 0.3 −0.6 −0.3 0.0 0.3
Compositional uniqueness Compositional uniqueness

Figure 1 The effects of diversity on ecosystem functioning using the averaging approach. Effects of (a) species richness and (c) compositional uniqueness on
the average multifunctionality. Red lines indicate the fits of mixed effects models. Slope values are shown with significance levels; *P < 0.05 and n.s.
P > 0.05. Effects of (b) species richness and (d) compositional uniqueness on individual functions and multifunctionality. Dots of different colors are values
of different functions. Red lines indicate the mixed effects model fit that accounts for variability across the seven functions. Slope values are shown with
significance levels; *P < 0.05 and n.s. P > 0.05. Colored lines indicate the mixed effects model fit of individual functions. (a–d) Solid thick lines and dashed
thin lines indicate significance and non-significance of the model slope, respectively. If significant, 95% confidence intervals of the model fit are shown as
shaded areas.

Table 1 Correlation matrix among seven ecosystem functions. All functions were standardised to a common scale

Belowground Tree litter Herb litter Reduction of

productivity S k decomposition decomposition nitrogen leaching

S 0.05n.s. – – – – –
K 0.03n.s. 0.18n.s. – – – –
Tree litter decomposition 0.21n.s. 0.28* 0.04n.s. – – –
Herb litter decomposition 0.37** 0.10n.s. 0.09n.s. 0.13n.s. – –
Reduction of nitrogen leaching 0.11n.s. 0.15n.s. 0.03n.s. 0.17n.s. 0.34** –
Plant-available nitrogen 0.29* 0.14n.s. 0.31* 0.27* 0.44*** 0.46****

Pearson’s correlation coefficients are shown. Significance levels; ****P < 0.0001, ***P < 0.001, **P < 0.01, *P < 0.05, n.s. P > 0.05. S and k are the stabilisa-
tion factor and initial decomposition rate estimated from the tea-bag method. The correlation coefficients for significant relationships are shown in bold letters.

© 2015 John Wiley & Sons Ltd/CNRS

Letter Low multifunctional redundancy of soil fungi 255

(a) (b) 0.075

per unit increment of species richness

6

Number of funcons ≥ Threshold

Change in number of funcons

0.050 Rmde: 0.043

0.025

2
Threshold (%)
0.000
75
50 Tmin: 65 %
0 25

10 20 30 0 25 50 75
Species richness Threshold (%)

(d)

per unit increment of composional uniqueness

(c)
1
Number of funcons ≥ Threshold

Change in number of funcons

0
4

2 Threshold (%)
−1
75
50
25

−0.8 −0.6 −0.4 −0.2 0.0 0.2 0 25 50 75

Composional uniqueness Threshold (%)

Figure 2 Diversity effects for a range of ecosystem multifunctionality thresholds. Effects of (a) species richness and (c) compositional uniqueness on the
number of functions above thresholds. Lines represent the slope between species richness and the number of functions greater than or equal to a threshold
value ranging from 5 to 95% of maximum for each function. Evaluation for (b) species richness and (d) compositional uniqueness effects on
multifunctionality. The dotted curves indicate the changes in number of functions per unit increment of diversity (slope of the relationship between
diversity and the threshold-based multifunctionality shown in (a) and (c)) with the shaded red areas indicating 95% confidence intervals. When the diversity
effects are significant (i.e. when the areas do not cover the dashed gray, zero lines), Tmin, and Rmde (see methods) are shown.

(Table 1). Our findings thus lend support for the previous tions among fungi competing for resources can even decrease
notion that, while diversity is important for ecosystem multi- the rate of biogeochemical processes (H€ attenschwiler et al.
functionality in a given locality, it would be unrealistic to sus- 2005). It is thus not surprising that some functions are inde-
tain all functions at high levels with any level of biodiversity pendent of diversity (Fig. 1b) often leading to high redun-
(Zavaleta et al. 2010; Gamfeldt et al. 2013; Byrnes et al. 2014; dancy in soil taxa. Another possibility is that the focal
Perkins et al. 2015). functions are, in reality, supported not only by fungi but also
The positive fungal diversity–multifunctionality relationship by diverse groups of organisms living belowground (Wagg
at the local scale was further supported using the multiple et al. 2014). According to a recent synthesis, ecosystem func-
threshold approach (Fig. 2a,b). Our finding that an additional tioning belowground can be threatened when soil species rich-
23 species were needed to add an additional function is higher ness is only severely reduced (Nielsen et al. 2011). In contrast,
than the reported values in previous studies for plants (Byrnes our study suggests a relatively limited degree of functional
et al. 2014) and macro-invertebrates (Perkins et al. 2015), redundancy for soil fungi when multiple functions are simulta-
indicating that many fungal species are required to increase neously considered.
multifunctionality in soil. Theory predicts positive effects of It should be noted that the above results for the relation-
microbial diversity on soil ecosystem functions, such as ships between species richness and multifunctionality may
decomposition, likely resulting from functional niche comple- not be sufficient to determine whether there is high or low
mentarity (Loreau 2001). However, results from observational multifunctional redundancy. This is because, in addition to
and experimental evidence are largely variable (H€ attenschwiler the levels of species richness in a given location, other aspects
et al. 2005). There is a possibility that antagonistic interac- of biological communities, such as the identity of constituting

© 2015 John Wiley & Sons Ltd/CNRS

256 A. S. Mori et al. Letter

(a) (b)
25 5

based on number of functions ≥ Threshold

Standardized functional importance (SES)
20 3

2
Number of species

15 1

10 –1

–2

5 –3

–4

0 –5

–4 –2 0 2 4 25 50 75
Standardized functional importance (SES) Threshold (%)
based on average multifunctionality

Figure 3 Functional importance of species to sustain multifunctionality. Standardised effect size (SES) of species’ functional importance based on (a) the
average multifunctionality approach and (b) the multiple threshold approach. (a) A histogram showing the number of functions in each SES value class.
(b) Boxplots representing species distribution at each threshold level. Black dotted lines indicate the 95% confidence intervals of the SES values. Species
with the SES values higher than the upper limits of confidence intervals are significantly (P < 0.05) more important to impact multifunctionality than
expected by chance (see Supporting Information S2 for these species identified by the two approaches).

species and that of local assemblages, may also be important
for some ecosystem functions in soil (Heemsbergen et al.
2004). At the species level, we found that some fungal species
play a disproportionally large functional role in supporting
belowground multifunctionality (Fig. 3a), especially for sus-
taining multiple functions at the higher threshold levels
(Fig. 3b). However, given our finding that the majority of
species did not significantly increase or decrease ecosystem
functioning (Fig. 3), we suggest that most particular species
do not necessarily impact ecosystem multifunctionality more
than species diversity. That is, this result again demonstrates
that, rather than the functional roles of some important spe-
cies, the number of species is fundamental for sustaining
multifunctionality. In contrast, some studies have suggested
that, rather than species richness, the identity and dominance
of particular species is of primary importance to
sustain ecosystem functioning (e.g. Winfree et al. 2015).
However, this issue has been previously discussed mainly in
the context of a single function. Although further studies are
needed, our results suggest that the importance of particular
species, rather than species diversity per se, for regulating
ecosystem functioning might depend on the number of func-
tions considered.
To further disentangle the functional roles of species
assemblages for supporting multifunctionality, we separated
the effects of species composition from those of species rich-
ness. This index of the compositional uniqueness of each
local community explained neither multifunctionality nor
individual functions at the local scale (Figs 1c,d and 2c,d).
However, it may be still important to account for composi-
tional characteristics when considering landscape-scale multi-
functionality. More specifically, although sustaining all or
most functions at high levels in a single locality may be
unrealistic in nature with any species composition or level of
biodiversity, doing so may be possible within a larger spatial
scale.
Our additional analysis at the landscape level showed a pos-
itive correlation between community dissimilarity and multi-
functional dissimilarity within the meta-community (Fig. 4).
Although a large variation was still left unexplained, our find-
ing suggests the importance of species turnover for sustaining
multifunctionality at a large spatial scale. Our other multi-
functionality approaches (Figs 1–3) ignored the identity of
individual functions, which implicitly assumes that functions
are substitutable, such that increases in some functions com-
pensate for decreases in other functions. Our cross-site results
reveal that when the identities of ecosystem functions within
each locality are considered, the functional redundancy of soil
microbes decreases to some extent. That is, shifts in fungal
community composition between locations lead to shifts in
which functions are provided, even if they do not lead to
shifts in the average level of multiple ecosystem functions.
Although it has been occasionally suggested (e.g. Heemsber-
gen et al. 2004), this is the first study to our knowledge
to clearly demonstrate the limited level of multifunctional
redundancy for soil microbes inhabiting natural ecosystems.
Consequently, as we found, diversity–multifunctionality rela-
tionships can be scale dependent. Given natural variation in
species assemblages, as well as spatial heterogeneity of envi-
ronmental factors in nature, we emphasise that the functional
roles of biodiversity need to be carefully assessed with a mul-
ti-scale and multifunctionality perspective.

© 2015 John Wiley & Sons Ltd/CNRS

Letter
Partial mantel r: 0.071* (CF: Geo)
10 Partial mantel r: 0.115** (CF: Env)
8
Multifunctional dissimilarity
6 ecological communities across locations (McKinney & Lock-
4 Importantly, recent studies have shown that soil microbes are
2
0
–1.0 –0.5 0.0 0.5
Community dissimilarity
Figure 4 Relationships of community dissimilarity and multifunctional
dissimilarity. Partial Mantel correlations with a controlling factor (CF) of
geographical (Geo) or environmental distances (Env) between two given
locations are shown with significant levels; two asterisks (**) denote
P < 0.01 and an asterisk (*) denotes P < 0.05. There was a significant
positive correlation between community dissimilarity and multifunctional
dissimilarity across locations. The red line represents the linear fit based
on standardised major axis regression, which was significant (P < 0.0001),
for visual understanding of the result. Overall, the result indicates that
species turnover is significantly positively associated with turnover of
multifunctionality between locations.
Implications
Given the rising concern that belowground biodiversity has
been seriously impacted by human activities in many parts of
the world (Pulleman et al. 2012; Bardgett & van der Putten
2014), our findings lend support to initiatives of soil biodiver-
sity conservation including those under the framework of
Convention on Biological Diversity (http://www.cbd.int/agro/-
soil.shtml). An important implication of our results is that
conserving and restoring soil microbes could likely lead to the
continued provision of ecosystem services such as carbon
sequestration and food provision (Wall et al. 2012), which are
crucial for the wellbeing of humanity. The diversity–multi-
functionality relationships we found, which were less affected
by compositional uniqueness than by local fungal diversity,
suggest a possible multifunctional insurance effect of diversity
(Yachi & Loreau 1999). Our first conclusion is that increasing
or maintaining species diversity may be one of the most
promising ways to secure overall multifunctionality.
Note that the minimal importance of compositional
uniqueness to enhance multifunctionality in no way justifies
the loss of any species, even if soil biota have some levels of
functional redundancy. Evaluating functional redundancy is
not straightforward, because its definition often varies
depending on a focal functional context (Mori et al. 2013).
Importantly, our results show that different fungal species
play different functional roles. We further demonstrated that,
Low multifunctional redundancy of soil fungi 257
as the focus shifts from local to landscape scales, multifunc-
tional redundancy can be further lowered. These findings
reveal links between species composition and multifunctional-
ity at multiple spatial scales. Our second conclusion is thus
that, spatial variation in species composition across locations
is important to maintain many functions at high levels
throughout a landscape.
There is increasing evidence that humans are homogenising
wood 1999; Olden et al. 2004). Such biotic homogenisation
has been also reported for soil biota (Mori et al. 2015).
assembled deterministically according to environmental condi-
tions, indicating that there is a natural variation in composi-
tional characteristics in environmentally heterogeneous
natural systems (Ranjard et al. 2013). The ecosystem func-
tions considered here are indeed important in practice (includ-
ing in our study system, which is undergoing forest
restoration), as these soil processes are crucial to conserve,
1.0
restore and sustain ecological dynamics by the virtue of plant-
soil feedbacks (van der Putten et al. 2013). The present study
emphasises that different scales of biodiversity could provide
multiple levels of insurance against the loss of such important
properties and feedbacks in ecological systems (Pasari et al.
2013) if both high-levels of species diversity at each location
and compositional variation across locations could be main-
tained. Alternatively, making soil assemblages depauperate or
homogeneous will likely eventually translate into the loss of
ecosystem multifunctionality and services.
ACKNOWLEDGEMENTS
This study was supported by the Mitsui & Co., Ltd. Envi-
ronment Fund and the Japanese Ministry of Education, Cul-
ture and Sports (No. 23770083). The present study was also
conducted using the Joint Usage/Research Grant of Center
for Ecological Research, Kyoto University and the Coopera-
tion Research Program of Wildlife Research Center, Kyoto
University. Logistical support for the field study was pro-
vided by the Shiretoko Foundation. We thank students at
Yokohama National University and members of the Shire-
toko Biodiversity Evaluation Project for their assistance with
field and laboratory work. Thanks are extended to editors
and three anonymous reviewers for their comments on this
paper.
AUTHORSHIP
ASM, FI, SF, MK and TO designed research. All authors col-
lected data. ASM primarily analysed data and wrote the
manuscript, with critical inputs from all authors.
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