Received: 27 October 2021 | Revised: 28 February 2023 | Accepted: 20 March 2023

DOI: 10.1111/ele.14220

LETTER

Biodiversity mitigates trade-­offs among species functional traits

underpinning multiple ecosystem services

Emelie Waldén1 | Cibele Queiroz2,3 | Jan Plue1,4 | Regina Lindborg1,5

1
Department of Physical Geography, Abstract
Stockholm University, Stockholm, Sweden
2
Biodiversity loss and its effects on humanity is of major global concern. While
Stockholm Resilience Centre, Stockholm
University, Stockholm, Sweden
a growing body of literature confirms positive relationships between biodiversity
3
Global Resilience Partnership, Stockholm,
and multiple ecological functions, the links between biodiversity, ecological
Sweden functions and multiple ecosystem services is yet unclear. Studies of biodiversity–­
4
IVL Swedish Environmental Institute, functionality relationships are mainly based on computer simulations or controlled
Stockholm, Sweden field experiments using only few species. Here, we use a trait-­based approach to
5
The Bolin Centre for Climate Research, integrate plant functions into an ecosystem service assessment to address impacts
Stockholm University, Stockholm, Sweden
of restoration on species-­r ich grasslands over time. We found trade-­offs among
Correspondence functions and services when analysing contributions from individual species. At
Regina Lindborg, Department of Physical the community level, these trade-­offs disappeared for almost all services with
Geography, Stockholm University, SE-­106
91 Stockholm, Sweden.
time since restoration as an effect of increased species diversity and more evenly
Email: regina.lindborg@natgeo.su.se distributed species. Restoration to enhance biodiversity also in species-­ r ich
communities is therefore essential to secure higher functional redundancy towards
Editor: Akira S Mori disturbances and sustainable provision of multiple ecosystem services over time.

K EY WOR DS
grassland, long-­term in situ experiments, multifunctionality, plants, restoration, species richness

I N T RODUC T ION number of ecosystem functions even at low levels of spe-

How to protect biodiversity and manage for multiple eco-
system services provision in the Anthropocene are top
priority tasks for policies worldwide (IPBES, 2019; Maes
et al., 2014). Reports of decreasing global biodiversity
(Newbold et al., 2015) have re-­fuelled the debate on how
biodiversity loss can affect ecosystem functions and ser-
vices essential for human well-­being. The link between
biodiversity and ecosystem functioning has been debated
in the literature for decades (Cardinale et al., 2012; Mace
et al., 2012), and positive relations have been shown in
a growing number of experiments and data syntheses
(Hector & Bagchi, 2007; Hooper et al., 2012; Lefcheck
et al., 2015; Tilman et al., 2006). In contrast, other stud-
ies show species functional redundancy in a community
context (Johnson et al., 1996; Loreau, 1998; Naeem, 2002)
and many theoretical models predict saturation of the
cies richness (Flynn et al., 2009; Wardle et al., 1997). The
contribution of biodiversity to ecosystem service provi-
sion is less clear, as links between species richness, eco-
system functions and services are complex (Harrison
et al., 2014; Lavorel, 2013; Mace et al., 2012). For exam-
ple, each individual service relies on several ecosystem
functions and the degree of this dependency varies sig-
nificantly among services (Cardinale et al., 2012; de Bello
et al., 2010).
Although a wide diversity of studies have explored
the relationships between biodiversity and ecosystem
functioning (BEF), the majority are experimental in
situ studies (Balvanera et al., 2014) encompassing tar-
geted species manipulations (Fanin et al., 2018; Finn
et al., 2013; Meyer et al., 2018; Zavaleta et al., 2010), or
in silico simulations, including communities with both
low (Gamfeldt & Roger, 2017) and high species diversity

This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium,
provided the original work is properly cited.
© 2023 The Authors. Ecology Letters published by John Wiley & Sons Ltd.

Ecology Letters. 2023;26:929–941.  wileyonlinelibrary.com/journal/ele | 929


930 |    BIODIVERSITY ENHANCES ECOSYSTEM SERVICES
(Dee et al., 2017; Solan et al., 2004). Experimental in situ
and in silico studies are complementary in order to un-
derstand underlying ecological processes, and these pro-
cesses might change when studying natural dynamics
through time (Cardinale et al., 2011; Loreau et al., 2002;
Manning et al., 2019). The impact of biodiversity may
also be under-­or overestimated due to the often short-­
term and/or small-­scale nature of in situ experiments
(Cardinale et al., 2012; Duffy, 2009; Isbell et al., 2018;
Manning et al., 2018) and potential risks of missing im-
portant unknown factors in simulation (Gamfeldt &
Roger, 2017). These limitations make it difficult to apply
findings from experimental BEF studies to real-­world
ecosystem service generation, as provision of most ser-
vices are underpinned by ecological functions at larger
spatial and temporal scales (Isbell et al., 2017; Lindborg
et al., 2017), although recent work has argued that the
findings drawn from BEF experiments are generally ro-
bust (Jochum et al., 2020).
The link between biodiversity and ecosystem ser-
vices becomes even more complex when considering
multiple services. Services can interact in various ways
in form of trade-­offs and synergies, and the type and
strength of these relationships may vary over space and
time (Lindborg et al., 2017; Queiroz et al., 2015; Ross
et al., 2021). They can also form interdependent bun-
dles, that is, common sets of correlated services (Bennett
et al., 2009). Understanding these complex relationships
is important for production of multiple benefits in a par-
ticular setting and time frame. While several recent BEF
meta-­studies found a positive effect of biodiversity when
considering multiple functions (Balvanera et al., 2014;
Hector & Bagchi, 2007; Isbell et al., 2011), the link be-
tween biodiversity and multiple services is still unclear
(Cardinale et al., 2012; but see Dainese et al., 2019).
The need for customized management of multiple ser-
vices is currently recognized as a vital aspect when re-
storing degraded natural habitats (Kollmann et al., 2016;
McDonald et al., 2016). Since many biodiversity-­rich eco-
systems are degraded (Chase et al., 2020) and/or face fur-
ther degradation due to multiple environmental pressures
(Watson et al., 2016), there is an urgent need for long-­term
in situ studies that evaluate the effects of restoration
measures not only on species richness but also on the re-
covery of multiple ecosystem services in high-­diversity
systems (Balvanera et al., 2014; Fiedler et al., 2018). Here,
we use long-­term restoration data from species-­rich semi-­
natural grasslands to examine the relationships between
species diversity, functions and services in plant commu-
nities under non-­experimental conditions. To understand
different plant species' contribution to ecosystem ser-
vices, we use a trait-­based approach, that is, linking plant
functional traits (Violle et al., 2007) to specific functions
and services (Cresswell et al., 2018; Díaz et al., 2007).
According to the mass ratio theory (Grime, 1998), eco-
system functioning is primarily driven by the dominant
species in a community. Thus, increased abundance of
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species with traits contributing to particular functions,
should increase the expression of those functions, as well
as the generation of underpinned services. Species co-­
existing in high-­diversity systems often have traits that
are not equally important underpinning the various func-
tions, hence complementing each other at the community
level (Hector & Bagchi, 2007). Following habitat resto-
ration, communities usually shift in species composition,
both in terms of species identity and abundance (Carlucci
et al., 2020; Jones et al., 2018). Our selected restored sites
are subjected to passive restoration, where plant commu-
nity recovery relies on natural processes such as spatial
and temporal seed dispersal, rendering them particularly
interesting for analysing temporal relationships between
community change, biodiversity, ecosystem functions
and services.
In this article, we assess changes in biodiversity and
ecosystem services provision in semi-­natural grasslands
over a restoration period of 20 years. Such long-­term in
situ studies assessing restoration of species richness and
links to multiple ecosystem services have, to the best of
our knowledge, never been conducted. Based on theory
(Hector & Bagchi, 2007; Loreau, 1998), experimental
studies (Tilman et al., 2006) and modelling (Gamfeldt
& Roger, 2017), we expected that an increase in plant
diversity over time would increase the variety of traits
at the community level underpinning a greater variety
of ecological functions. Therefore, higher plant species
richness would, through their functional traits, increase
the possibility to generate multiple ecosystem services
(Cresswell et al., 2018). In a step-­w ise procedure, we first
identified five services for which semi-­natural grasslands
are important providers: meat production, pollination,
water retention, temperature regulation and cultural
heritage (Table 1). Second, we coupled a set of relevant
species functional traits with each of the selected ser-
vices. These different sets of traits were then used to
calculate the contribution of each species to individual
services. Finally, we paired these individual contribu-
tions with data on community change in the restored
habitats and compared to reference grassland sites (con-
tinuously grazed species-­r ich grasslands), to understand
how restoration measures have affected the distribution
of multiple services.
M AT E R I A L S A N D M ET HOD S
Study sites and field inventory
The study was conducted in restored and reference semi-­
natural grasslands situated in multiple agricultural land-
scapes in south-­c entral Sweden (Table S2). In terms of
biodiversity, traditionally managed semi-­natural grass-
lands are considered Europe's equivalent to tropical
rainforests (Wilson et al., 2012), meaning high biodiver-
sity systems at small spatial scales. To uphold grassland
 14610248, 2023, 6, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/ele.14220 by Lanzhou University, Wiley Online Library on [11/02/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
WALDÉN et al.     | 931

T A B L E 1 Ecosystem services in semi-­natural grasslands coupled to plant species functional effect traits, trait unit measured, data type and
data source (see also Tables S1, S3 and S4). Categorical values were translated to a nominal scale. All traits were then standardized into a 0–­1
scale based on the community maximum. More information regarding data source methods for collecting functional trait data can be found in
each data source reference.

Ecosystem service Functional traits Unit measured in data source Data type Data source
Meat production Leaf dry mass mg Cont. TRY
Specific Leaf Area (SLA) mm 2 mg−1 Cont. TRY
Foraging value Ranging from poisonous to best forage Ord. BiolFlor
value (scale 0–­9)
Pollination Pollination syndrome Insect pollinated or not (scale 0–­1) Bin. BiolFlor
Flowering duration No. of months Ord. Den nya nordiska floran
Nectar quantity Ranging from none to plenty (scale 0–­3) Ord. BiolFlor, Imkerbond
Zoersel
Pollen quantity Ranging from none to plenty (scale 0–­5) Ord. Imkerbond Zoersel,
BiolFlor
Temperature Height m Cont. TRY
regulation SLA mm mg2 −1
Cont. TRY
Root architecture type Tap root, adventitious, fibrous (scale 1–­3) Cat. TRY
Lifespan Annual, biennial, 2–­5 years, 5–­50 years and Ord. LEDA
>50 years (scale 1–­5)
Water retention SLA mm 2 mg−1 Cont. TRY
Height m Cont. TRY
Clonal lateral spread rate Non- ­clonal, <0.01, 0.01–­0.25 and Ord. CLO-­PLA
>0.25 m year−1 (scale 0–­3)
Root architecture type Tap root, adventitious, fibrous (scale 1–­3) Cat. TRY
Cultural heritage Grassland specialist Specialist or not (scale 0–­1) Bin. Om hävden upphör
Mentions in traditional music No. of songs Cont. Svenskt Visarkiv
and older popular songs
Abbreviations: Bin., Binary variable; Cat., Categorical value; Cont., Continuous variable; Ord., Ordinal value.

biodiversity, traditional management by grazing or
mowing, without the use of pesticides or fertilizers, is
necessary. However, as a consequence of agricultural in-
tensification, up to 90% of these habitats have been lost
during the last century (Strijker, 2005). Restoration of
semi-­natural grasslands and other degraded or damaged
habitats is highlighted as a key feature in the European
Union Biodiversity Strategy for 2030.
We used data from plant inventories of 16 restored
semi-­natural grasslands collected at two time steps;
1–­9 years (T1) and 12–­20 years (T2) post-­restoration, in
a total of 260 species. The total number of species in-
creased significantly between T1 and T2 in the restored
grasslands, from 51.6 to 62.9 species per grassland site
in average, although the average number of species
per grassland was still significantly higher in the refer-
ence grasslands (76.2 species) (Figure S1; Waldén and
Lindborg (2016)). Vascular plant species richness and
individual species abundance was inventoried using 10
plots (1 m × 1 m) equally distributed in two transects per
grassland. Abundance in its broader sense can be mea-
sured in different ways, either as the total number of an
individual species per unit area at which data are col-
lected (i.e. abundance/density), as the number of unit
areas in which the species occurred in relation to total
number of units studied (i.e. frequency), or as biomass.
In this study, we used the frequency measure based on
presence–­absence in 10 plots per grassland, scale 0–­10
(hereafter referred to as abundance).
Ecosystem services selection and trait
data collection
The number of studies addressing ecosystem services (ES)
from grasslands (natural, semi-­ natural or improved) is
generally low compared to other ecosystems like, for exam-
ple, forests (Bardgett et al., 2021). However, there are more
than 20 different services acknowledged from grasslands
related to fodder production, water, soil health, carbon
sequestration, habitat provision, pollination and biologi-
cal control (Bengtsson et al., 2019; Zhao et al., 2020). We
selected five of these: ‘meat production’, ‘pollination’,
‘temperature regulation’, ‘water retention’ and ‘cultural
heritage’ (Table 1) (for references, see Table S1), as (1) they
are the most strongly related to traditionally managed
semi-­natural grasslands in agricultural landscapes, and (2)
their underpinning of ecological functions is, through lit-
erature, linked to specific plant traits. Since these habitats
are grazed by livestock, the grassland's fodder production

932 |    BIODIVERSITY ENHANCES ECOSYSTEM SERVICES
quality is important for meat production. Grasslands are
also able to act as a food resource for crop-­pollinating in-
sects, through its diverse supply of flowering plants dur-
ing the season. Being a permanent semi-­natural habitat in
agricultural landscapes, grasslands may also sequestrate
carbon and prevent flooding in such landscapes. Finally,
through its historical origin, semi-­natural grasslands are
important carriers of cultural heritage.
The selection of plant traits is fundamental, as dif-
ferent traits play different roles in the ecological func-
tions underpinning services (Cresswell et al., 2018). In
this study, we assessed the services indirectly by assign-
ing scores to each species based on the extent to which
species-­level functional traits contribute to providing ES.
This is a commonly used approach when measuring mul-
tiple services in species-­rich systems (Díaz et al., 2007;
Zhao et al., 2020). For each ES, we selected a set of func-
tional traits (Table 1) that were identified in the literature
as being important for the ecological functions under-
pinning that specific ES (Table S1). Another important
criterion for trait selection was whether trait data were
publicly available and accessible for most species in our
study. In a few cases, other and/or additional traits would
have been preferred than those selected, but they could
not be included due to high levels of missing data. In some
cases, especially for temperature regulation and water re-
tention, many of the traits identified in the literature as
important to contribute to those particular ES were the
same. This is a consequence of the fact that some ES are
underpinned by similar ecological processes, traits and
species (Bennett et al., 2009; Rullens et al., 2019), influ-
encing the correlation among ES, found in our analysis.
All final traits were carefully selected to match the ES (for
description of trait selection and references, see Tables S1
and S4). The traits were classified so that higher values
corresponded to increased ES provision.
We calculated the mean trait values for each species
across the different databases for all continuous vari-
ables. Instead of the arithmetic mean, we used the geo-
metric mean as it is less sensitive to extreme values, and
we were interested in getting a representative value for
each species that was fairly robust to potential outliers.
The geometric mean is given by the ‘n’ root of the mul-
tiplication of all n values, where ‘n’ is the total number
of observations. Calculations were done in R 3.3.0 (R
Core Team, 2016) with the EnvStats package (function:
geoMean). To complement missing trait values, informa-
tion from alternative databases and the Swedish national
flora were added as a first measure. For the species still
lacking data for some of the traits (foraging value, nectar
and pollen quantity), missing values were at first hand
replaced by average values from species within the same
taxonomic genus present in Sweden, and secondly, by
species pool average values. For more information re-
garding percentages of missing values in primary data
sources for each of the traits and which alternative data
sources that were used, see Table S4.
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All traits were then standardized into a 0–­1 scale
(based on the community maximum), where higher
value equals higher contribution to the ES. Correlation
between traits within each ES trait group was tested in
multiple Spearman correlation tests (Table S5). Most
traits were uncorrelated, however, for example, polli-
nation syndrome and nectar/pollen quantity were cor-
related (ρSpearman > 0.5 at p < 0.001). Nevertheless, due to
the ES calculation method described below and com-
parably low correlations between other traits, all traits
were included during data preparation. For community
average trait and ES-­values, see Table S6.
Data preparation to estimate ecosystem services
from species traits
The five selected ES were treated separately in a step-­wise
procedure (Figure 1). After selecting functional traits for
each ES and collecting trait data for each species, species-­
specific ES-­values was calculated, that is, each species
received a separate ES value which reflected the species'
contribution to the provision of each service; ‘meat pro-
duction’, ‘pollination’, ‘temperature regulation’, ‘water re-
tention’ and ‘cultural heritage’. In theory, a typical plant
with high ES value for, (1) ‘meat production’ would have
a high forage value, high leaf dry mass and high SLA, (2),
‘pollination’ would be insect pollinated, have long flower
duration and plenty of nectar and pollen, (3) ‘cultural her-
itage’ would be a grassland specialist plant and be men-
tioned frequently in traditional music, (4) ‘temperature
regulation’ would be tall and long-­lived plants with high
SLA and fibrous roots, and (5) ‘water retention’ would be
tall plants with a high clonal lateral spread rate, high SLA
and fibrous roots (Table 1). Due to the resource limita-
tions and evolutionary history, these theoretical plants
might not exist in reality. Further, it is also clear that traits
are not equally important and do not scale linearly with
ES provision (Lindborg et al., 2017). Nevertheless, as no
data exist of relative trait contribution to ES generation,
we chose to treat them similarly.
For each species, the average of all trait values in the
specific ES trait group were then calculated to receive a
species-­specific ES-­value. For the ES ‘meat production’
and ‘pollination’, this was treated differently. For ‘meat
production’, species that are poisonous for cattle and
therefore cannot be used as fodder (zero as forage value)
were automatically set to an overall zero-­value for the
‘meat production’ ES. Similarly, species not pollinated by
insects were also set to a zero-­value for ‘pollination’ ES.
For each of the five ES, the species ES values was
then multiplied with the species' occurrence at each
grassland site and time step (Rest. sites T1, Rest. sites
T2, Ref. sites) resulting in species ES contribution values
for each site and time step. These species ES contribu-
tion values were calculated in two ways: (1) just based
on species presence–­absence data, and (2) each species
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WALDÉN et al.     | 933

F I G U R E 1 To estimate ecosystem service provision through species and trait data, a five-­step procedure was done for each of the five
ecosystem services (ES) separately. [1] Selecting functional traits coupled to each specific ES, according to available literature. [2] Standardizing
the traits coupled to the specific ES into a 0–­1 scale (based on the community maximum), where higher value equals higher contribution to the
ES (in this figure, we use ES 1 as an example of one of the five ES). [3] Calculating an ES value for each species in the community, by averaging
all the associated trait values for that species. [4] Multiplying the species ES value with either the species presence, or their abundance, at each
grassland site (restored and reference) and time step (T1, T2) (in this figure, we use species abundance at restored sites at T1 as an example).
[5] Using the final site-­specific species ES contribution matrix to calculate an ES community average for each ES and site to analyse the
community differences in t-­test.

contribution to a particular service weighted by its abun-
dance. This was done to disentangle how species identity
versus abundance affects ecosystem services distribu-
tion. A presence–­absence as well as an abundance-­based
species ES contribution matrix was generated for each
time step (Rest. sites T1, Rest. sites T2, Ref. sites) result-
ing in six species ES contribution matrices for every ES
(i.e. 30 matrices in total). These were used as the base
for calculating a community-­weighted mean for each ES
and site (ES community average), to be able to analyse
the community differences between T1 and T2, as well
as between restored and reference sites.
Statistical analyses
All statistical analyses were performed using R 3.3.0
(R Core Team, 2016). Relationships between the
species-­specific ES values (n = 260 × 5) were analysed in
multiple Spearman's rank correlations (function: cor.
test). The differences in community ES metrics (i.e. based
on either species presence-­absence or abundance data)
for the restored sites at T1 compared to T2 were analysed
using paired t-­tests (function: t-­test). Similarly, the dif-
ferences in community ES metrics between restored and
reference sites at T2 were analysed using Welch t-­tests
(function: t-­test). To assess the extent to which changes in
community composition are driving changes in commu-
nity ES, we ran a non-­metric multidimensional scaling
ordination (NMDS; function metaMDS, vegan package)
for each ES including both restored and reference sites.
The species abundance × site matrix underlying each
NMDS ordination was adapted per ES, using only the
species contributing to a particular ES. Each ordina-
tion solution was constrained to returning only a two-­
axes solution based on the Bray–­ Curtis dissimilarity

934 |    BIODIVERSITY ENHANCES ECOSYSTEM SERVICES
metric, which was rotated to ensure that the first NMDS
axis contained the majority of variation in the com-
munity data. Post hoc analysis to assess differences
in the positioning of the restored and reference sites
in the ordination space (using the t-­tests as described
above) was therefore restricted to the first NMDS axis.
Relationships between the different community ES met-
rics, as well as their relation to species richness, were
analysed using multiple Spearman correlations for each
category (T1, T2 and the relative change over time [∆])
respectively. Correlations between pairs of ES were used
to investigate potential trade-­offs and synergies, where
trade-­offs were given by negative correlations and syner-
gies by positive correlations between services. To ana-
lyse community evenness shift between the time steps,
we first calculated Simpson's Index of Diversity (1 − D)
for all sites (package: vegan, function: diversity), and then
analysed the result in a paired t-­test.
R E SU LT S
The contribution to the generation of selected ES dif-
fered between plant species, highlighting that one sin-
gle species cannot simultaneously have high values for
all the traits underpinning multiple ES. This resulted in
trade-­offs between ES on a species level (Figure 2). These
trade-­offs occur as groups of traits that enhance the pro-
vision of certain services, do not enhance the provision
of other services as they are underpinning different eco-
system functions. Trade-­offs were mainly found between
‘temperature regulation’ and ‘water retention’ in relation
to ‘cultural heritage’ and ‘pollination’. Different species
also contributed to ‘meat production’ and ‘cultural herit-
age’, respectively, leading to trade-­offs between the ES.
In contrast, the same species contributed to the services
‘temperature regulation’, ‘water retention’ and ‘meat
production’.
F I G U R E 2 Species-­level trade-­offs, synergies and non-­significant relationships between ecosystem services provided by plant species
occurring in the semi-­natural grasslands. Individual species ES values are calculated based on their functional traits (see calculation procedure
in Table 1 and Figure 1). Significant Spearman's rank correlations indicated by colour gradient (red is negative, blue is positive), Spearman's ρ
and p-­value (inside parenthesis).
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At the community level, plant presence/absence
data showed that community ecosystem service provi-
sion from restored grassland sites (Table S7) increased
with time towards reference levels for all five services
(Figure 3, top panel). Specifically, the generation of
‘meat production’ and ‘pollination’, in the restored hab-
itats (at T2) now resembled the reference semi-­natural
grasslands. Species richness in the restored sites also in-
creased over time (average increase of 21.9%, t = −4.50,
df = 15, p < 0.001; see also Figure S1).
Species community evenness increased over time
(Simpson's Index of Diversity 1 − D, Restored T1:
0.967 ± 0.004 vs. T2: 0.974 ± 0.003, t = −3.85, df = 15,
p-­value = 0.002, see Tables S7 and S8). However, when
species abundance was included in the calculations,
we found no increase in ecosystem service provi-
sion over time in the restored sites (Figure 3, middle
panel). We also found community changes in those
species' assemblages contributing to the respective
ecosystem services (Figure 3, bottom panel).
Positive correlations between all five services were de-
tected, both in the short-­and long-­term after restoration,
when analysed pair-­wise (Figure 4). For data of propor-
tional change for each grassland site, see Table S8. All
these individual services also became correlated with spe-
cies richness over time (compare T1 and T2 in Figure 4).
DISCUSSION
Ecosystem service trade-­offs generated at the
species level
Ecosystem service trade-­offs as an effect of land use and
management (Bennett et al., 2009; Foley et al., 2005)
have been frequently discussed in the scientific lit-
erature. These trade-­offs are often related to biodiver-
sity composition as some land uses and management
 14610248, 2023, 6, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/ele.14220 by Lanzhou University, Wiley Online Library on [11/02/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
WALDÉN et al.     | 935

F I G U R E 3 Ecosystem service (ES) provision (plant community average) for each ES; ‘meat production’, ‘pollination’, ‘temperature
regulation’, ‘water retention’ and ‘cultural heritage’. The ES community average is based on plant species traits connected to the specific
ecosystem functions and services, and the species' presence (top panel) or abundance (middle panel) in restored semi-­natural grasslands at
time 1 (T1, 1–­9 years after restoration) and time 2 (T2, 12–­20 years after restoration), as well as in intact reference semi-­natural grasslands
(Ref) at time 2. The bottom panel represent plant community change by the contributing part of the community following restoration (at T1,
T2 and Ref), represented by the position along the first axis of a non-­metric multi-­d imensional scaling ordination performed on a species
abundance × site matrix (ordinations, Figure S2). Significant differences indicated by asterisks (*p < 0.05–­0.01, **p < 0.01–­0.001, ***p < 0.001).

practices favours some species more than others
(Cardinale et al., 2012; Mace et al., 2012). This study
found clear trade-­offs among ecosystem services when
calculations were made based on the relative contribu-
tion of each plant species in the grassland community
(Figure 2). This suggests that high contribution to some
services goes along with low contribution to the provi-
sioning of others. For example, plant species that have
nectar-­r ich flowers and therefore contribute strongly to
pollination, are mostly relatively small and thick-­leaved,
with poorly developed root architecture, making them
contribute little to water retention. Some of the trade-­
offs found are relatively well-­k nown trade-­offs to occur
between provisioning services and regulating or cultural
services (Foley et al., 2005). These trade-­offs occur when
two services are underpinned by different functions, and
dependent on a distinct set of traits given by different
species (Bennett et al., 2009).
 14610248, 2023, 6, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/ele.14220 by Lanzhou University, Wiley Online Library on [11/02/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
936 |    BIODIVERSITY ENHANCES ECOSYSTEM SERVICES

F I G U R E 4 Correlations between five ecosystem services at a plant community level and in relation to species richness in restored semi-­
natural grasslands, at time 1 and 2 (T1: 1–­9 years after restoration, T2: 12–­20 years after restoration) and the relative change over time (Δ).
Provision of the ecosystem services is based on species abundance (see calculation procedure in Figure 1 and Table 1). Positive significant
relationship indicated by blue colour (reporting Spearman's ρ and p-­value in parenthesis).

In other words, trade-­offs and non-­significant rela-
tionships between service provision show that differ-
ent species, through their functions, underpin different
services. Furthermore, no single species is able to con-
tribute to high levels of all the tested services simulta-
neously. Similar to Winfree et al. (2015) and Dainese
et al. (2019), we show that individual species can have a
disproportionate large positive effect on the provision
of one service, although high levels of species richness
are needed to generate multiple services (Gamfeldt
et al., 2013). This becomes even more evident over
time, as high species richness may enhance ecosystem
functioning across temporally fluctuating and spa-
tially heterogeneous environments (Isbell et al., 2018).
Trade-­offs between groups of services could also be de-
tected in our study. For example, ‘water retention’ and
‘temperature regulation’ on the one hand, traded-­off
with ‘cultural heritage’ and ‘pollination’ on the other.
This supports the findings from previous studies on
the existence of particular ES bundles, meaning that
some ES are often positively correlated (as they are un-
derpinned by functions performed by the same species)
while others are never (Raudsepp-­Hearne et al., 2010;
Queiroz et al., 2015).
To fully understand the role of biodiversity in gener-
ating ecosystem services (Mace et al., 2012), there is a
need to identify not only trade-­offs but also synergies
among services. In our study, we found positive rela-
tionships among the services ‘temperature regulation’,
‘water retention’ and ‘meat production’. The synergies
between ‘meat production’, ‘water retention’ and ‘tem-
perature regulation’ are mostly an effect of high SLA
values, whereas the stronger synergy between ‘tempera-
ture regulation’ and ‘water retention’ relates to a plant

WALDÉN et al.
being tall, perennial and having a finer root architec-
ture. These synergies indicate that those ES are under-
pinned by functions that are given by the similar groups
of traits. The knowledge that similar traits can underpin
two different services are important to fully understand
bundles of ES and how to manage them. This highlights
the importance of traits selected for the outcome of anal-
ysis linking traits to services (de Bello et al., 2021; Mace
et al., 2012).
Ecosystem service generation changes over time
As expected, all the five services selected for this study
increased with time towards reference levels (Figure 3).
This was especially clear in the habitats 12–­20 years
after restoration (T2), where the generation of ‘meat
production’ and ‘pollination’ now resembled service
generation in reference semi-­ natural grasslands. As
species community composition often changes over
time, particularly in response to restoration, shifts in
ecosystem service provision can also be expected. In
theory, increasing numbers of co-­existing species within
a community would increase the probability of includ-
ing species with high contribution to functions and ser-
vices, due to an overall increased functional richness
(Cadotte et al., 2011). This is confirmed by our results,
where species richness in the restored sites increased
over time, simultaneously underpinning a higher num-
ber of ecosystem services (Figure 3). However, these
results should be interpreted carefully, as one of the
assumptions of this study was that all traits are equally
important for the provision of a particular ES and that
trait values scale linearly with ES provision, which is
likely not the case for all ES (Lindborg et al., 2017).
Some studies have found idiosyncratic species behav-
iour related to, for example, community composition
or temperature, partly questioning grouping species
into functional groups mainly based on their traits
(Lindborg & Eriksson, 2005). Hence, assuming traits
to be context-­independent is partly a simplification.
However, if functional groups of species are remaining
relatively constant, at least within similar systems, it is
reasonable to believe that specific groups of species will
underpin similar functions in many different environ-
ments (Díaz et al., 2007). Further investigation of the
nature and shape of these trait–­ES relationships, and
if certain traits are more important than others should
be the focus of future studies (e.g. de Bello et al., 2021).
In studies concerning restoration, it is especially im-
portant to incorporate abundance of species since that
tends to shift substantially after restoration (Waldén &
Lindborg, 2016). Since the relative abundance of spe-
cies are important to the different functions, it might
affect ecosystem service provision (Isbell et al., 2017).
To investigate the importance of species abundance, we
also included abundance (frequency) in the calculations.
14610248, 2023, 6, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/ele.14220 by Lanzhou University, Wiley Online Library on [11/02/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
    | 937
When adding species abundance, no increase in ecosys-
tem service provision over time was detected in restored
sites. This suggests that species important for the pro-
vision of multiple services may have so far remained at
low abundances compared to reference sites. Thus, not
only does a species important for a certain service need
to be present, but it also needs to be abundant enough
to actually contribute to the expression of that service in
the community. Shortly after restoration (T1), ecosystem
services' generation was mainly provided by a few abun-
dant species (illustrated in Figure S1) diverse enough in
their functional character to ensure the generation of
multiple services.
There was a clear shift in species community assem-
blage in restored sites from T1 to T2, with an increase
in community evenness. Yet, generation of ecosystem
services remained stable. This implies that service pro-
vision turned from relying on a few abundant species to
relying on more species for upholding the same provi-
sion level. By relying on a higher number of species, the
provision of each ecosystem service is likely to be more
resilient to potential future natural and non-­natural
disturbances. When several species are contributing
to the same function, some species can compensate
for the potential loss of other species (functional re-
dundancy), especially when the diversity of responses
to potential disturbances among those species is high
(response diversity) (Elmqvist et al., 2003). While this
remains a reasonable hypothesis anchored in ecologi-
cal theory, the extension of Price equation partitioning
developed by Fox and Kerr (2012) could be applied in
future research to quantify the effects on a function
of biodiversity changes (species loss/gain) and contex-
tual changes between two given communities. This
would enable a detailed exploration to understand how
ecosystem service generation remained stable in spite
of individual changes in species presences and abun-
dances. Such an approach would unveil in detail the
dominant trait-­and community-­ based mechanisms
driving shifts in ecosystem service provisioning in real-­
world high-­d iversity plant communities pressurized by
environmental changes. Finally, higher diversity also
increases the possibility for higher trait diversity that
would more efficiently counteract perturbations, al-
together reflecting the links between species diversity
and functional redundancy in the community (de Bello
et al., 2021).
Biodiversity increases provision of multiple
ecosystem services
Finding ways of increasing potential synergies and re-
ducing trade-­offs between ecosystem services is impor-
tant for future ecosystem management. When analysing
the overall contribution of the whole plant commu-
nity to the provision of ecosystem services, we found

938 |    BIODIVERSITY ENHANCES ECOSYSTEM SERVICES
strong positive correlations between all five services,
both short and long time after restoration (Figure 4).
Interestingly, all individual services became highly cor-
related with species richness over time. In comparison
with our study, increasing positive effects of biodiver-
sity have also been detected in BEF experiments over
time (Cardinale et al., 2007; Isbell et al., 2018), stressing
a clear link between traits, ecosystem functioning and
ecosystem services (Carlucci et al., 2020). Even though
the communities studied here are characterized by
very high levels of plant diversity, we show that further
increase in species richness correlated significantly
with increased provision of multiple services. This
is an important finding in relation to most previous
studies showing a positive relationship between spe-
cies richness and functional diversity which are mainly
conducted in low-­d iversity experimental communities
under controlled conditions (Manning et al., 2019).
Our results suggest that this positive relationship thus
applies even to real-­world high-­d iversity plant commu-
nities. Habitat management focusing mainly on biodi-
versity could therefore simultaneously support a range
of different services including provisioning, regulating
as well as cultural services.
Humans depend on nature and its capacity to pro-
vide multiple ecosystem services across space and time,
for their well-­being and survival (Cardinale et al., 2012;
IPBES, 2019). Achieving simultaneous provision of
multiple services is difficult, as there are fundamental
trade-­offs between functional traits underpinning these
services. Here, we show that although these trade-­offs
exist and can be mitigated by managing for increased
species richness. As shown by this study, plant diversity
can play an important role in generation of services, even
in species-­r ich real-­world ecosystems. So far, most stud-
ies have focused on biodiversity loss and the following
negative impact on functions and services. In contrast,
we highlight the multiple benefits of active manage-
ment towards increasing species richness in a commu-
nity through restoration (see also Carlucci et al., 2020).
Relying on a few key species might be sufficient when
focusing on a single service at a specific time and place
(Winfree et al., 2015). That will, however, not be enough
to ensure a long-­ term stability of ecosystem services
provision, as the environmental conditions will become
increasingly uncertain under future climate change and
other drivers of environmental change. Dade et al. (2019)
conclude that to fully understand the relation between
biodiversity and ecosystem services and manage services
over time, assessments should focus on casual drivers and
process-­based models. Our observed increase in plant
species richness, led to a higher functional redundancy
over time, indicating a more resilient service provision
with time since restoration. Still, the full implications of
our findings for ecosystem services resilience should be
further studied and also include other indicators than just
functional redundancy of plants. Nevertheless, coupling
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ecosystem service provision to biodiversity presents ad-
ditional arguments for conservation and restoration to
reach sustainability in a changing world.
AU T HOR C ON T R I BU T ION S
Emelie Waldén came up with some of the design, con-
ducted the fieldwork, compiled the data, made data anal-
ysis and compiled the statistics, and performed most of
the writing; Cibele Queiroz helped with data compiling,
analysis, design and writing; Jan Plue helped with analy-
sis and statistics; and Regina Lindborg came up with the
original idea, design and performed some of the writing.
AC K NO​W L E​D GE​M E N T S
We thank landowners and farmers for letting us col-
lect plant data on their land and two anonymous re-
viewers for their helpful comments on the article. We
are also grateful to the publicly available plant trait
databases TRY, BiolFlor, LEDA, CLO-­ PLA and
Imkerbond Zoersel, and to The Centre for Swedish
Folk Music and Jazz Research for providing access to
the online song and tune catalogue ‘Svenskt Visarkiv’.
We also acknowledge the Swedish Research Council
for Environment, Agricultural Sciences and Spatial
Planning (FORMAS, grant numbers 2009-­ 1105 and
2018-­0 0961) and the Swedish Marianne and Marcus
Wallenberg Foundation (Grant 2017.0137) for funding
of this research.
C ON F L IC T OF I N T E R E ST STAT E M E N T
None of the authors have competing interest with this
article.
PE E R R E V I E W
The peer review history for this article is available at
https://www.webof​s cien​c e.com/api/gatew​ay/wos/peer-­
revie​w/10.1111/ele.14220.
DATA AVA I L A B I L I T Y STAT E M E N T
We confirm that if the article should be accepted, the
data supporting the results will be archived in the public
repository Figshare and the data DOI will be included
at the end of the article. https://doi.org/10.6084/m9.figsh​
are.21908​964.v4
ORC I D
Jan Plue https://orcid.org/0000-0002-6999-669X
Regina Lindborg https://orcid.org/0000-0001-​7134-7974
R EF ER ENCE S
Balvanera, P., Siddique, I., Dee, L., Paquette, A., Isbell, F.,
Gonzalez, A. et al. (2014) Linking biodiversity and ecosys-
tem services: current uncertainties and the necessary next
steps. Bioscience, 64(1), 49–­ 57. Available from: https://doi.
org/10.1093/biosc​i /bit003
Bardgett, R.D., Bullock, J., Lavorel, S., Manning, P., Schaffner, U.,
Ostle, N. et al. (2021) Combating global grassland degradation.
Nature Reviews Earth & Environment, 2, 720–­735 Available from:

WALDÉN et al.
https://www.nature.com/artic​les/s4301​7- ­021- ­0 0207​-­2 [Accessed
23rd January 2022].
Bengtsson, J., Bullock, J.M., Egoh, B., Everson, C., Everson, T. &
O’Connor, T. (2019) Grasslands—­more important for ecosys-
tem services than you might think. Ecosphere. Available from:
https://doi.org/10.1002/ecs2.2582
Bennett, E.M., Peterson, G.D. & Gordon, L.J. (2009) Understanding
relationships among multiple ecosystem services. Ecology
Letters, 12(12), 1394–­ 1404. Available from: https://doi.
org/10.1111/j.1461-­0248.2009.01387.x
Cadotte, M.W., Carscadden, K. & Mirotchnick, N. (2011) Beyond spe-
cies: functional diversity and the maintenance of ecological pro-
cesses and services. Journal of Applied Ecology, 48(5), 1079–­1087.
Available from: https://doi.org/10.1111/j.1365-­2664.2011.02048.x
Cardinale, B.J., Matulich, K.L., Hooper, D.U., Byrnes, J.E., Duffy,
E., Gamfeldt, L. et al. (2011) The functional role of producer di-
versity in ecosystems. American Journal of Botany, 98(3), 572–­
592. Available from: https://doi.org/10.3732/ajb.1000364
Cardinale, B.J., Emmett Duffy, J., Gonzalez, A., Hooper, D.U.,
Perrings, C., Venail, P. et al. (2012) Biodiversity loss and its im-
pact on humanity. Nature, 486(7401), 59–­ 67. Available from:
https://doi.org/10.1038/natur​e11148
Cardinale, B.J., Wright, J.P., Cadotte, M.W., Carroll, I.T., Hector,
A., Srivastava, D.S. et al. (2007) Impacts of plant diversity on
biomass production increase through time because of spe-
­ Richers, B.T., Lin, B.B. et al. (2009) Loss of functional di-
cies complementarity. Proceedings of the National Academy of
Sciences of the United States of America, 104(46), 18123–­18128
Available from: http://www.pnas.org/conte​nt/104/46/18123.ab-
stract [Accessed 20th September 2019].
Carlucci, M.B., Brancalion, P.H.S., Rodrigues, R.R., Loyola, R. &
Cianciaruso, M.V. (2020) Functional traits and ecosystem ser-
vices in ecological restoration. Restoration Ecology, 28, 1372–­
1383. Available from: https://doi.org/10.1111/rec.13279
Chase, J.M., Blowes, S.A., Knight, T.M., Gerstner, K. & May, F.
(2020) Ecosystem decay exacerbates biodiversity loss with habi-
tat loss. Nature, 584(7820), 238–­243. Available from: https://doi.
org/10.1038/s4158​6 -­020-­2531-­2
Cresswell, C.J., Cunningham, H.M., Wilcox, A. & Randall, N.P.
(2018) What specific plant traits support ecosystem services such
as pollination, bio-­c ontrol and water quality protection in tem-
perate climates? A systematic map. Environmental Evidence, 7(1),
2. Available from: https://doi.org/10.1186/s1375​0 -­018-­0120-­8
Dade, M.C., Mitchell, M.G.E., McAlpine, C.A. & Rhodes, J.R. (2019)
Assessing ecosystem service trade-­offs and synergies: the need
for a more mechanistic approach. Ambio, 48(10), 1116–­ 1128.
Available from: https://doi.org/10.1007/s1328​0 -­018-­1127-­7
Dainese, M., Martin, E.A., Aizen, M.A., Albrecht, M., Bartomeus, I.,
Bommarco, R. et al. (2019) A global synthesis reveals biodiversity-­
mediated benefits for crop production. Science Advances, 5(10),
1–­13. Available from: https://doi.org/10.1126/sciadv.aax0121
de Bello, F., Lavorel, S., Gerhold, P., Reier, Ü. & Pärtel, M. (2010) A
biodiversity monitoring framework for practical conservation of
grasslands and shrublands. Biological Conservation, 143(1), 9–­17.
Available from: https://doi.org/10.1016/j.biocon.2009.04.022
de Bello, F., Lavorel, S., Hallett, L.M., Valencia, E., Garnier, E.,
Roscher, C. et al. (2021) Functional trait effects on ecosys-
tem stability: assembling the jigsaw puzzle. Trends in Ecology
& Evolution, 36(9), 822–­ 836. Available from: https://doi.
org/10.1016/j.tree.2021.05.001
Dee, L.E., De Lara, M., Costello, C. & Gaines, S.D. (2017) To what
extent can ecosystem services motivate protecting biodiversity?
Ecology Letters, 20(8), 935–­ 946. Available from: https://doi.
org/10.1111/ele.12790
Díaz, S., Lavorel, S., de Bello, F., Quétier, F., Grigulis, K., Matthew, T.
et al. (2007) Incorporating plant functional diversity effects in eco-
system service assessments. Proceedings of the National Academy
of Sciences of the United States of America, 104(52), 20684–­20689.
Available from: https://doi.org/10.1073/pnas.07047​16104
14610248, 2023, 6, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/ele.14220 by Lanzhou University, Wiley Online Library on [11/02/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
    | 939
Duffy, J.E. (2009) Why biodiversity is important to the functioning of
real-­world ecosystems. Frontiers in Ecology and the Environment,
7(8), 437–­4 44. Available from: https://doi.org/10.1890/070195
Elmqvist, T., Folke, C., Nyström, M., Peterson, G., Bengtsson, J.,
Walker, B. et al. (2003) Response diversity, ecosystem change,
and resilience. Frontiers in Ecology and the Environment,
1, 488–­ 494. Available from: https://doi.org/10.1890/1540-­
9295(2003)001[0488:RDECA​R]2.0.CO;2
Fanin, N., Gundale, M.J., Farrell, M., Ciobanu, M., Baldock, J.A.,
Nilsson, M.-­C. et al. (2018) Consistent effects of biodiversity loss
on multifunctionality across contrasting ecosystems. Nature
Ecology & Evolution, 2(2), 269–­278. Available from: https://doi.
org/10.1038/s4155​9-­017-­0415-­0
Fiedler, S., Perring, M.P. & Tietjen, B. (2018) Integrating trait-­based
empirical and modeling research to improve ecological resto-
ration. Ecology and Evolution, 8, 6369–­ 6380. Available from:
https://doi.org/10.1002/ece3.4043
Finn, J.A., Kirwan, L., John Connolly, M., Sebastià, T., Helgadottir,
A., Baadshaug, O.H. et al. (2013) Ecosystem function enhanced
by combining four functional types of plant species in intensively
managed grassland mixtures: a 3-­year continental-­s cale field ex-
periment. Journal of Applied Ecology, 50(2), 365–­375. Available
from: https://doi.org/10.1111/1365-­2664.12041
Flynn, D.F.B., Gogol-­ Prokurat, M., Nogeire, T., Molinari, N.,
versity under land use intensification across multiple taxa.
Ecology Letters, 12(1), 22–­ 33. Available from: https://doi.
org/10.1111/j.1461-­0248.2008.01255.x
Foley, J.A., Defries, R., Asner, G.P., Barford, C., Bonan, G., Carpenter,
S.R. et al. (2005) Global consequences of land use. Science,
309(5734), 570–­574. Available from: https://doi.org/10.1126/scien​
ce.1111772
Fox, J.W. & Kerr, B. (2012) Analyzing the effects of species gain and
loss on ecosystem function using the extended Price equation
partition. Oikos, 121(2), 290–­ 298. Available from: https://doi.
org/10.1111/j.1600-­0706.2011.19656.x
Gamfeldt, L. & Roger, F. (2017) Revisiting the biodiversity–­e cosystem
multifunctionality relationship. Nature Ecology & Evolution, 1(7),
0168. Available from: https://doi.org/10.1038/s4155​9-­017-­0168
Gamfeldt, L., Snäll, T., Bagchi, R., Jonsson, M., Gustafsson, L.,
Kjellander, P. et al. (2013) Higher levels of multiple ecosystem
services are found in forests with more tree species. Nature
Communications, 4(January), 1340. Available from: https://doi.
org/10.1038/ncomm​s2328
Grime, J.P. (1998) Benefits of plant diversity to ecosystems: immedi-
ate, filter and founder effects. Journal of Ecology, 86, 902–­910.
Available from: https://doi.org/10.2307/2648655
Harrison, P.A., Berry, P.M., Simpson, G., Haslett, J.R., Blicharska,
M., Bucur, M. et al. (2014) Linkages between biodiversity attri-
butes and ecosystem services: a systematic review. Ecosystem
Services, 9(September), 191–­ 203. Available from: https://doi.
org/10.1016/j.ecoser.2014.05.006
Hector, A. & Bagchi, R. (2007) Biodiversity and ecosystem multifunc-
tionality. Nature, 448(7150), 188–­190. Available from: https://doi.
org/10.1038/natur​e 05947
Hooper, D.U., Carol Adair, E., Cardinale, B.J., Byrnes, J.E.K.,
Hungate, B.A., Matulich, K.L. et al. (2012) A global synthe-
sis reveals biodiversity loss as a major driver of ecosystem
change. Nature, 486(7401), 105–­108. Available from: https://doi.
org/10.1038/natur​e11118
IPBES. (2019) Global assessment report on biodiversity and ecosystem
Services of the Intergovernmental Science-­Policy Platform on biodi-
versity and ecosystem services. Bonn, Germany: IPBES Secretariat.
Available from: https://doi.org/10.5281/zenodo.3831673
Isbell, F., Calcagno, V., Hector, A., John Connolly, W., Harpole, S.,
Reich, P.B. et al. (2011) High plant diversity is needed to maintain
ecosystem services. Nature, 477(7363), 199–­202. Available from:
https://doi.org/10.1038/natur​e10282

940 |    BIODIVERSITY ENHANCES ECOSYSTEM SERVICES
Isbell, F., Cowles, J., Dee, L.E., Loreau, M., Reich, P.B., Gonzalez,
A. et al. (2018) Quantifying effects of biodiversity on ecosystem
functioning across times and places. Ecology Letters, 21, 763–­
778. Available from: https://doi.org/10.1111/ele.12928
Isbell, F., Gonzalez, A., Loreau, M., Cowles, J., Díaz, S., Hector, A.
et al. (2017) Linking the influence and dependence of people on
biodiversity across scales. Nature, 546(7656), 65–­72. Available
from: https://doi.org/10.1038/natur​e22899
Jochum, M., Fischer, M., Isbell, F., Roscher, C., van der Plas, F.,
Boch, S. et al. (2020) The results of biodiversity–­e cosystem func-
tioning experiments are realistic. Nature Ecology & Evolution,
4(11), 1485–­ 1494. Available from: https://doi.org/10.1038/s4155​
9-­020-­1280-­9
Johnson, K.H., Vogt, K.A., Clark, H.J., Schmitz, O.J. & Vogt, D.J.
(1996) Biodiversity and the productivity and stability of ecosys-
tems. Trends in Ecology & Evolution, 11(9), 372–­377. Available
from: https://doi.org/10.1016/0169-­5347(96)10040​-­9
Jones, H.P., Jones, P.C., Barbier, E.B., Blackburn, R.C., Rey, J.M.,
Benayas, K.D. et al. (2018) Restoration and repair of Earth's
damaged ecosystems. Proceedings of the Biological Sciences,
285(1873), 20172577. Available from: https://doi.org/10.1098/
rspb.2017.2577
Kollmann, J., Meyer, S.T., Bateman, R., Conradi, T., Gossner, M.M.,
de Souza, M. et al. (2016) Integrating ecosystem functions into
restoration ecology-­ recent advances and future directions.
Restoration Ecology, 24(6), 722–­730. Available from: https://doi.
org/10.1111/rec.12422
Lavorel, S. (2013) Plant functional effects on ecosystem services.
Journal of Ecology, 101(1), 4–­ 8. Available from: https://doi.
org/10.1111/1365-­2745.12031
Lefcheck, J.S., Byrnes, J.E.K., Isbell, F., Gamfeldt, L., Griffin, J.N.,
Eisenhauer, N. et al. (2015) Biodiversity enhances ecosystem
multifunctionality across trophic levels and habitats. Nature
Communications, 6(April), 6936. Available from: https://doi.
org/10.1038/ncomm​s7936
Lindborg, R. & Eriksson, O. (2005) Functional response to land
use change in grasslands: comparing species and trait data.
Ecoscience, 12(2), 183–­191.
Lindborg, R., Gordon, L.J., Malinga, R., Bengtsson, J., Peterson,
G., Bommarco, R. et al. (2017) How spatial scale shapes the
generation and management of multiple ecosystem services.
Ecosphere, 8(4), e01741. Available from: https://doi.org/10.1002/
ecs2.1741
Loreau, M. (1998) Biodiversity and ecosystem functioning: a mecha-
nistic model. Proceedings of the National Academy of Sciences of
the United States of America, 95(10), 5632–­5636 Available from:
http://www.pnas.org/conte​nt/95/10/5632.abstract [Accessed 3rd
May 2019].
Loreau, M., Shahid, N. & Pablo, I. (2002) Biodiversity and ecosys-
tem functioning: synthesis and perspectives. Oxford: Oxford
University Press.
Mace, G.M., Norris, K. & Fitter, A.H. (2012) Biodiversity and eco-
system services: a multilayered relationship. Trends in Ecology
& Evolution, 27, 19–­26. Available from: https://doi.org/10.1016/j.
tree.2011.08.006
Maes, J., Teller, A., Erhard, M., Murphy, P., Paracchini, M.-­L., Cano,
J.I.B. et al. (2014) Indicators for ecosystem assessments under
action 5 of the EU biodiversity strategy to 2020. Publications
Office of the European Union. Available from: https://doi.
org/10.2779/75203
Manning, P., Loos, J., Barnes, A.D., Batáry, P., Bianchi, F.J.J.A.,
Buchmann, N. et al. (2019) Transferring biodiversity-­e cosystem
function research to the management of ‘real-­world’ ecosystems.
Advances in Ecological Research, 61(January), 323–­356. Available
from: https://doi.org/10.1016/bs.aecr.2019.06.009
Manning, P., van der Plas, F., Soliveres, S., Allan, E., Maestre, F.T.,
Mace, G. et al. (2018) Redefining ecosystem multifunctional-
ity. Nature Ecology & Evolution, 2(3), 427–­436. Available from:
https://doi.org/10.1038/s4155​9-­017-­0461-­7
14610248, 2023, 6, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/ele.14220 by Lanzhou University, Wiley Online Library on [11/02/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
McDonald, T., Gann, G.D., Jonson, J. & Dixon, K.W. (2016)
International standards for the practice of ecological resto-
ration –­including principles and key concepts. Washington,
DC. Available from: www.ser.org [Accessed 6th May 2019]:
National standards for the practice of ecological restoration
in Australia.
Meyer, S.T., Ptacnik, R., Hillebrand, H., Bessler, H., Buchmann, N.,
Ebeling, A. et al. (2018) Biodiversity–­ multifunctionality rela-
tionships depend on identity and number of measured functions.
Nature Ecology & Evolution, 2(November), 44–­ 49. Available
from: https://doi.org/10.1038/s4155​9-­017-­0391-­4
Naeem, S. (2002) Ecosystem consequences of biodiversity loss: the
evolution of a paradigm. Ecology, 83(6), 1537–­1552. Available
from: https://doi.org/10.1890/0012-­9658(2002)083[1537:ECOBL​
T]2.0.CO;2
Newbold, T., Hudson, L.N., Hill, S.L.L., Contu, S., Lysenko, I.,
Senior, R.A. et al. (2015) Global effects of land use on local ter-
restrial biodiversity. Nature, 520(7545), 45–­50. Available from:
https://doi.org/10.1038/natur​e14324
Queiroz, C., Meacham, M., Richter, K., Norström, A.V., Andersson,
E., Norberg, J. et al. (2015) Mapping bundles of ecosystem
services reveals distinct types of multifunctionality within a
Swedish landscape. Ambio, 44(S1), 89–­ 101. Available from:
https://doi.org/10.1007/s1328​0 -­014-­0601-­0
R Core Team. (2016) R: a language and environment for statistical
computing. Available from: https://www.r-­proje ​ct.org/ [Accessed
6th May 2016].
Raudsepp-Hearne, C., Peterson, G.D. & Bennett, E.M. (2010)
Ecosystem service bundles for analyzing tradeoffs in diverse
landscapes. Proceedings of the National Academy of Sciences of
the United States of America, 107, 5242–­5247.
Ross, S.R.P.-­J., Arnoldi, J.-­F., Loreau, M., White, C.D., Stout, J.C.,
Jackson, A.L. et al. (2021) Universal scaling of robustness of eco-
system services to species loss. Nature Communications, 12(1),
5167. Available from: https://doi.org/10.1038/s4146​7-­021-­25507​-­5
Rullens, V., Lohrer, A.M., Townsend, M. & Pilditch, C.A. (2019)
Ecological mechanisms underpinning ecosystem service bundles
in marine environments -­a case study for shellfish. Frontiers in
Marine Science, 6(July), 409.
Solan, M., Cardinale, B.J., Downing, A.L., Engelhardt, K.A.M.,
Ruesink, J.L. & Srivastava, D.S. (2004) Extinction and eco-
system function in the marine benthos. Science, 306(5699),
1177–­1180 Available from: http://scien​c e.scien​c emag.org/conte​
nt/306/5699/1177.abstract [Accessed 4th April 2019].
Strijker, D. (2005) Marginal lands in Europe—­c auses of decline. Basic
and Applied Ecology, 6(2), 99–­106. Available from: https://doi.
org/10.1016/j.baae.2005.01.001
Tilman, D., Reich, P.B. & Knops, J.M.H. (2006) Biodiversity and eco-
system stability in a decade-­long grassland experiment. Nature,
441(7093), 629–­632. Available from: https://doi.org/10.1038/natur​
e04742
Violle, C., Navas, M.-­ L., Vile, D., Kazakou, E., Fortunel, C.,
Hummel, I. et al. (2007) Let the concept of trait be func-
tional! Oikos, 116(5), 882–­ 892. Available from: https://doi.
org/10.1111/j.0030-­1299.2007.15559.x
Waldén, E. & Lindborg, R. (2016) Long term positive effect of grass-
land restoration on plant diversity -­success or not? PLoS One,
11(5), e0155836. Available from: https://doi.org/10.1371/journ​
al.pone.0155836
Wardle, D.A., Bonner, K.I. & Nicholson, K.S. (1997) Biodiversity
and plant litter: experimental evidence which does not sup-
port the view that enhanced species richness improves eco-
system function. Oikos, 79(2), 247. Available from: https://doi.
org/10.2307/3546010
Watson, J.E.M., Jones, K.R., Fuller, R.A., Di Marco, M., Segan, D.B.,
Butchart, S.H.M. et al. (2016) Persistent disparities between re-
cent rates of habitat conversion and protection and implications
for future global conservation targets. Conservation Letters, 9(6),
413–­421. Available from: https://doi.org/10.1111/conl.12295
 14610248, 2023, 6, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/ele.14220 by Lanzhou University, Wiley Online Library on [11/02/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
WALDÉN et al.     | 941

Wilson, J.B., Peet, R.K., Dengler, J. & Pärtel, M. (2012) Plant

species richness: the world records. Journal of Vegetation S U PP ORT I NG I N F OR M AT ION
Science, 23(4), 796–­ 802. Available from: https://doi. Additional supporting information can be found online
org/10.1111/j.1654-­1103.2012.01400.x in the Supporting Information section at the end of this
Winfree, R., Fox, J.W., Williams, N.M., Reilly, J.R. & Cariveau, article.
D.P. (2015) Abundance of common species, not species rich-
ness, drives delivery of a real-­world ecosystem service. Ecology
Letters, 18(7), 626–­635. Available from: https://doi.org/10.1111/
ele.12424
Zavaleta, E.S., Pasari, J.R., Hulvey, K.B. & David Tilman, G. (2010) How to cite this article: Waldén, E., Queiroz, C.,
Sustaining multiple ecosystem functions in grassland commu- Plue, J. & Lindborg, R. (2023) Biodiversity mitigates
nities requires higher biodiversity. Proceedings of the National trade-­offs among species functional traits
Academy of Sciences of the United States of America, 107(4), underpinning multiple ecosystem services. Ecology
1443–­1446. Available from: https://doi.org/10.1073/pnas.09068​
Letters, 26, 929–941. Available from: https://doi.
29107
Zhao, Y., Liu, Z. & Wu, J. (2020) Grassland ecosystem services: a org/10.1111/ele.14220
systematic review of research advances and future directions.
Landscape Ecology, 35(1), 793–­814. Available from: https://doi.
org/10.1007/s1098​0 -­020-­0 0980​-­3