CONCEPTS & SYNTHESIS

EMPHASIZING NEW IDEAS TO STIMULATE RESEARCH IN ECOLOGY

Ecology, 89(5), 2008, pp. 12231231

2008 by the Ecological Society of America

MULTIPLE FUNCTIONS INCREASE THE IMPORTANCE OF BIODIVERSITY

FOR OVERALL ECOSYSTEM FUNCTIONING
LARS GAMFELDT,1,2,3 HELMUT HILLEBRAND,2
1

AND

PER R. JONSSON1

Department of Marine Ecology, Goteborg University, Tjarno Marine Biological Laboratory, SE-452 96 Stromstad, Sweden
2
Institute for Botany, Aquatic Ecology, University of Cologne, Gyrhofstrasse 15, D-50931 Koln, Germany

Abstract. Biodiversity is proposed to be important for the rate of ecosystem functions.

Most biodiversityecosystem function studies, however, consider only one response variable at
a time, and even when multiple variables are examined they are analyzed separately. This
means that a very important aspect of biodiversity is overlooked: the possibility for different
species to carry out different functions at any one time. We propose a conceptual model to
explore the effects of species loss on overall ecosystem functioning, where overall functioning
is dened as the joint effect of many ecosystem functions. We show that, due to
multifunctional complementarity among species, overall functioning is more susceptible to
species loss than are single functions. Modeled relationships between species richness and
overall ecosystem functioning using ve empirical data sets on monocultures reected the
range of effects of species loss on multiple functions predicted by the model. Furthermore, an
exploration of the correlations across functions and the degree of redundancy within functions
revealed that multifunctional redundancy was generally lower than single-function redundancy in these empirical data sets. We suggest that by shifting the focus to the variety of
functions maintained by a diversity of species, the full importance of biodiversity for the
functioning of ecosystems can be uncovered. Our results are thus important for conservation
and management of biota and ecosystem services.
Key words: bacteria; biodiversity; ecosystem functioning; multifunctionality; multiple functions; plants;
redundancy; seagrass.

INTRODUCTION
The richness of species, functional groups, or genotypes is an important aspect of biodiversity that governs
the magnitude and efciency of ecosystem processes and
properties (Chapin et al. 1997). Additionally, biodiversity is essential for providing goods and services to
human society and thus also has economic values.
Process rates in ecosystems, properties of ecosystems,
and goods and services derived from ecosystems have
often been summarized as ecosystem functions. The
hypothesis that biodiversity is important for ecosystem
functions seems to have good general support (Hooper
et al. 2005, Balvanera et al. 2006). Many studies,
however, conclude that individual species are as efcient
performers of certain ecosystem processes as a more
diverse mix of species (e.g., Aarssen 1997, Huston 1997,
Manuscript received 18 December 2006; revised 22 August
2007; accepted 11 September 2007. Corresponding Editor: J. B.
Yavitt.
3
E-mail: lars.gamfeldt@marecol.gu.se

Wardle et al. 1997, Bruno et al. 2005, Hooper et al. 2005,

Cardinale et al. 2006). In fact, empirical studies show
that one or a few key species can dominate individual
ecosystem processes (e.g., Paine 2002, Bellwood et al.
2003, Solan et al. 2004). In addition, a small range of
species can often carry out the same individual
ecological process, resulting in a high degree of
ecological redundancy in natural and experimental
species assemblages (Walker 1992, Naeem 1998, but
see Loreau 2004).
Conceptually, as species richness increases, so does
the lowest possible level of any single ecosystem
function (Fig. 1a). Depending on the redundancy across
species for the function of interest, this increase can be
steep at high redundancy (solid curve) or at at low
redundancy (gray curve). It is possible, however, that
high-performing species are present at all levels of
species richness, and hence system states above the solid
curve are hypothetically possible (gray area).
Within the extensive biodiversityecosystem function
(BEF) research over the past decade, the majority of

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FIG. 1. (a) The effects of species loss for hypothetical communities. The black line represents maximum loss in function if each
species lost is the most efcient species of the ones remaining in the community (as we move from high to low species richness). The
darker gray area above this line represents all possible scenarios of species loss. The arrow and the gray line indicate that the impact
of species loss on ecosystem function changes with changing redundancy. (b) The graph shows conceptually how the probability of
sustaining overall functioning depends on both the number of functions and the degree of multifunctional redundancy across
species. With some functional specialization, multiple functions will always be more susceptible to species loss than single functions
(dashed line). This susceptibility will increase with decreasing redundancy. At the extreme case where all species can carry out only
one function, the probability of sustaining overall functioning will be zero until S n, where the probability will instantaneously
rise to a certain level. If all species play the exact same role for all functions, functioning will equal the response of one function.

studies has used a single-function perspective, i.e.,

addressed the consequence of species loss on single
process rates or properties. The use of single response
variables as proxies for ecosystem functioning may
ignore other important ecosystem processes (Rosenfeld
2002a). Equating single functions with overall functioning can be highly misleading, especially if BEF research
ultimately aims to provide knowledge and advice to
management and conservation. Rather, individual functions and processes may be better viewed as components
of ecosystem functioning writ large. In this paper we
therefore propose that overall ecosystem functioning is
the joint effect of multiple ecosystem functions. We
believe that this is a valuable denition, which will aid in
the interpretation of the ecological consequences of
biodiversity loss.
The role of altered biodiversity for multifunctional
ecosystem functioning has so far only been considered in
a quantitative way in the recent study by Hector and
Bagchi (2007). They found that ecosystem multifunctionality in experimental grasslands does require greater
numbers of species than do single functions. Otherwise,
when multiple functions have been examined (e.g.,
Tilman et al. 1997, Duffy et al. 2001, Downing 2005,
Spehn et al. 2005), they have not been considered
collectively. Duffy et al. (2003) discussed qualitatively
the role of individual species for different functions in
seagrass beds, and concluded that even when single
grazer species are most important for individual
ecosystem responses (i.e., there are sampling rather than
complementarity effects, see Loreau and Hector [2001]),
only mixtures of these grazers maximize multiple
ecosystem responses simultaneously. Furthermore, dif-

ferent species of marine macroalgae appear to differ in

their efciency in using limiting resources, so that total
nitrogen use is higher in diverse assemblages than
predicted based on the uptake rates of the component
species (Bracken and Stachowicz 2006). As stated by
Rosenfeld (2002b), species are more likely to show
nonoverlapping functions in a multi-dimensional than in
a one-dimensional functional space. Accordingly, Petchey and Gaston (2002) showed that species become
increasingly unique when many functions are added to a
multivariate index of functional diversity.
To examine the importance of diversity for the overall
functioning of ecosystems, it is important to analyze
quantitatively the effect of species loss on multiple
functions. We hypothesized that as several functions are
considered jointly, the importance of biodiversity will
become apparent, even though single functions do not
depend on a mixture of different species or groups. This
should hold true for different ecosystem types, sets of
organisms (or genotypes, functional groups, etc.), and
functions. To explore the importance of biodiversity for
multiple ecosystem functioning, we rst present a simple
conceptual model. We then compare the outcome of this
model with independent empirical data sets, for which
we derive estimates for the consequences of species loss
on single and multiple ecosystem functions.
CONCEPTUAL MODEL
Overall functioning is the joint effect of multiple
constituent functions considered in any one system, and
cannot be expressed as the average of those functions.
Our conceptual model rests on the logical but important
premise that a decline in one function cannot be

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BIODIVERSITY AND MULTIPLE FUNCTIONS

1b). The arrows in Fig. 1b indicate how both the degree

of redundancy and the number of functions interact to
inuence the probability of sustaining overall ecosystem
functioning in the face of biodiversity loss. We tested
this conceptual model using empirical data sets to (1)
test how the perceived effects of species loss might
change if more than one function is considered at the
same time, and (2) show how redundancy levels within
and across functions may be distributed for different
types of organisms and functions. Note that the
empirical data sets, although they already measure a
variety of functions, all cover only a subset of the
important processes and properties in ecosystems.
Accordingly, this subset of functions can be dened as
joint ecosystem functioning.
ANALYSIS

OF

EMPIRICAL DATA

Data sets
A survey of the literature revealed only a few studies
with information on multiple functions for a range of
monocultures. There are indeed more published studies
that investigate multiple functions (e.g., Tilman et al.
1997, Spehn et al. 2005). It is, however, not possible
from those papers to extract information on speciesspecic data for the functional performances of individual monocultures. Other studies (e.g., Gamfeldt et al.
2005) consider only low levels (23) of species richness
and functions. To examine our conceptual model, we
used ve empirical data sets (referred to as the Plant
study, the Bacteria study, and Seagrass studies IIII; for
details see Table 1). From the two plant studies by
Palmborg et al. (2005) and Viketoft et al. (2005), which
are based on the same experiment, we collected
information on three functions from each study on the
same 12 plant species (Plants). In Jiang (2007) we found
three functions for four bacteria species (Bacteria).
From Duffy et al. (2001) we extracted information on
three grazer species and three functions (Seagrass I), and
from Duffy et al. (2005) on four grazers and four
functions. Duffy et al. (2005) included two different
scenarios for the effects of grazers (with and without a
predatory crab), which we refer to as separate experiments in our study (without crabs [Seagrass II] and with
crabs [Seagrass III]). All three seagrass studies actually
presented more functions and response variables, but
some variables did not t the broad denition of the
word function, and some were indirect effects of other
functions. All functions examined in our analyses t well
within the listed denitions of ecosystem functions and
processes in Giller et al. (2004).
Rationale
We based our analyses on monoculture data only and
provide a simple analysis of consequences of species loss,
which can be viewed as a best-case scenario, as we did
not include a variety of factors that might deteriorate
consequences of biodiversity loss. First, we constructed
mixtures from the monocultures in each data set and

CONCEPTS & SYNTHESIS

compensated by an increase in another function. For

example, decreased primary productivity cannot be
compensated by an increase in nutrient uptake. We
therefore must dene some level of each function that we
nd acceptable. When one function drops beneath this
level, overall ecosystem functioning is no longer
sustained.
As an example, let us consider a system with S
number of species and N number of functions, and look
at the probability of this system of sustaining overall
functioning in the face of random species loss. For any
one function, the probability of sustaining this function
increases with species richness due to sampling effects
(Aarsen 1997, Cardinale et al. 2006), and will asymptotically approach a maximum value, which we set as 1
(cf. Fig. 1a). The sampling effect means that the
probability of sampling functionally important species
increases with increasing number of species. At low
species richness, the probability of sustaining a function
will lie somewhere between 0 and 1 because there is a
certain probability of sampling those species that are
efcient for the function.
For multiple functions the probability also approaches 1 at high species richness, where enough species are
included that together perform all necessary functions,
i.e., ensure overall ecosystem functioning. As for single
functions, the response of overall functioning to species
loss depends on the level of redundancy (Fig. 1b).
However, multifunctional redundancy implies a positive
covariance of species traits across functions, i.e., the
ability of species to perform different functions has to be
positively correlated. In one extreme scenario, each
species is equally important for each function, in which
case functions will be perfectly correlated across species,
and the effect of species loss on overall ecosystem
functioning is then the same as for each single function
(Fig. 1b). At the other end, specialization among species
results in uncorrelated results or even negative correlations. An extreme case is when each species can carry
out only one function and contributes nothing to the
other functions. Under such conditions fewer than n
number of species will have zero probability of
sustaining overall ecosystem functioning (Fig. 1b). This
scenario leads to little redundancy across functions,
which is potentially unrelated to redundancy within
functions.
For real-world species assemblages, levels of redundancy across multiple functions will fall somewhere
between these two extreme scenarios. Even if different
species may be equally important for one function,
redundancy across functions can be low, as different
species may sustain different functions. Therefore, the
important message from this conceptual model is that a
system is more likely to lose overall ecosystem functioning if species traits do not covary and different functions
reside on different species. At the same time, the
probability of losing ecosystem functioning increases
with the number of different functions considered (Fig.

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TABLE 1. Functions and correlations from the ve empirical studies analyzed in the study.

Study

CONCEPTS & SYNTHESIS

Plants (Palmborg et al. 2005,

Viketoft et al. 2005)

No.
species
12

Species
type

No.
functions

plants

Bacteria (Jiang 2007)

bacteria

Seagrass I (Duffy et al. 2001)

grazers

Seagrass II and III

(Duffy et al. 2005)

grazers

equalled the level of any function in a mixture with the

level of the best constituent species in monoculture.
Using data from monocultures to address multispecies
performance is conservative, since it completely disregards complementarity effects (enhanced performance in
mixes of species due to niche partitioning or facilitation),
and suggests that only selection effects are driving BEF.
We thus adopt the view that multispecies assemblages
outperform the average but not the best monoculture,
which emerged from a recent study comprising metaanalysis across systems, trophic levels, and functions
(Cardinale et al. 2006).
Second, we use a 0.5 threshold for assessing a single
ecosystem function to be performed sufciently within
an ecosystem. Thus, if the mixture contained a species
performing an ecosystem function at half the maximum
strength, we considered this to be sufcient for the
community to sustain that particular function. In the
absence of a general criterion for when ecologists
consider an ecosystem function at risk, we used a rather
low threshold, which in its analogy to EC50 (concentration giving 50% of maximum effect in ecotoxicology)
reects another important outcome of the Cardinale et
al. (2006) meta-analysis: they found that for any single
function, on average one species was needed to keep a
certain process at ;60% of its maximum rate. Using 0.5
as a threshold thus maximizes the probability that in our
calculations, only one species will be needed for a single
function, and that calculated effects of species loss will
appear only on the level of joint ecosystem functioning.
The consequences of species loss on joint ecosystem
functioning would appear much more dramatic if a
threshold of 0.75 or 0.9 had been used.
Third, we do not consider temporal changes in the
environment. The number of species needed to sustain a
single function (and consequently joint ecosystem
functioning) will be much higher in temporally uctuating or unstable ecosystems, as different species might
perform a single function at different times.

Functions
biomass production
NO3 extraction
NH4 extraction
nematode plant feeder production
nematode fungal feeder production
nematode bacterial feeder production
biomass production
consumer biomass production
decomposition
biomass production
algae grazing
eelgrass grazing
biomass production
macroalgae grazing
sediment algae grazing
epiphyte production

Range of pairwise
function correlations
0.80 to 0.69

0.07 to 0.63
0.84 to 0.87
no crabs: 0.62 to 0.95
with crabs: 0.55 to 0.94

Finally, the model further assumes that simply the

presence of a species performing an ecosystem function
at half the maximum strength is sufcient for the
community to sustain that particular function. Thus, we
make no assumptions on minimum densities required to
sustain ecosystem processes. Different extinction scenarios and types of density dependence may further
inuence the exact relationship between diversity and
multiple ecosystem functioning, but probably less so
than for single functions (e.g., Solan et al. 2004). The
most common species may be least susceptible to
extinction and most important for one of the functions.
But other functions may be strongly affected by less
common species, and some processes may in fact be only
weakly coupled to overall density (e.g., predation and
pollination). By not making any specic assumptions
about density dependence we emphasize the general
effect of biodiversity when considering multiple functions collectively.
Calculation of consequences of species loss
We analyzed the effect of species on multiple
ecosystem functions by randomly deleting 1 to S  1
species from the species pool and calculating the
probability that the reduced community was still able
to perform all single functions considered at the 0.5
threshold. These calculations were based on the speciesspecic information from the monocultures within the
ve data sets. For all mixtures of species, each function
was assigned the function value of the best-performing
monoculture (as described in Rationale). For each data
set we performed three calculation steps.
The rst step was to transform the multiple target
functions to a common scale. For each single function
we dened the proposed effect of diversity when
diversity enhances the function (e.g., grazer richness
increases grazer productivity and decreases algal biomass [Cardinale et al. 2006]). For each function we
identied the best-performing monoculture and assigned

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BIODIVERSITY AND MULTIPLE FUNCTIONS

Calculation of redundancy
We also calculated relative estimates of redundancy
for each data set, both within functions and across
functions. We used pairwise correlations for all functions across all species to calculate across-function
(multifunctional) redundancy for each data set. A
correlation for any two functions across all species tells
us something about how much two functions covary,
i.e., how the relative species contributions are distributed. These values range from 1 to 1, where 1 means that
the functions correlate perfectly, 0 means that there is no
correlation, and 1 means that there is a perfect negative
correlation between functions. Low or inversely correlated functions imply that species are functionally
complementary, i.e., several species are important for
ecosystem functioning, and that species might have
trade-offs for different functions. The mean of the
correlation coefcients between all possible combinations of functions is employed as the redundancy (for
this study) across functions. The correlation coefcients
do not, however, tell us anything about the magnitude of
the function values for each function. We therefore also
calculated a measure of redundancy within each

FIG. 2. The probability of sustaining joint functioning with

changing species richness for (a) plants with 12 species and N
16 functions, and for (b) bacteria with 4 species and N 13
functions.

function by taking the mean performance of all species

when the best species was removed. This redundancy
varies between 0 and 1, where 1 depicts perfect
replacement (i.e., the absence of the best-performing
species can be fully compensated), and 0 the absence of
redundancy (i.e., only the best species is able to perform
this function). Then we compared estimates of redundancy across and within functions for all data sets to
explore whether redundancy across functions is less
probable than within functions.
EMPIRICAL DATA: RESULTS
The analyses of the empirical data sets captured the
range of patterns found in the conceptual model (Fig.
1b). Plants showed quite low multifunctional redundancy among the 12 plant species, and considering all six
functions, made joint ecosystem functioning highly
susceptible to species loss (Fig. 2a). Bacteria showed
higher multifunctional redundancy, as there was an
effect of the number of functions only at low species
richness (Fig. 2b).
The analyses of the grazerseagrass data sets also
revealed a range in susceptibility of joint ecosystem
functioning to species loss. The importance of diversity
increased with the number of functions considered in the
three data sets (Fig. 3). All three data sets showed high
risk of losing joint functioning if only one or two species
were removed.
The redundancy within functions ranged from 0.19 to
0.71, indicating a wide spread in the ability to sustain
single functions when species are lost (Fig. 4: x axis).
However, across functions, much lower levels of

CONCEPTS & SYNTHESIS

the process rate of this function a value of 1. The other

monoculture values were then expressed as ratios to the
best-performing species. If this ratio was negative we
assigned it a value of zero. The truncation at zero for
negative values prevented the articial increase of low
function values when normalizing to the maximum
function value.
In a second step, we randomly deleted species from
the assemblage and calculated the effects of species loss
on each single function, by analyzing if there was at least
one species remaining with a performance value .0.5,
which we had dened as a sufcient function level (see
Rationale).
In a nal, third step, we considered whether joint
ecosystem functioning was sustained in the reduced
community for any combination of 1 to N functions. We
considered this maintenance of joint ecosystem functioning to be achieved when for each ecosystem function
at least one species was present in the remaining
community performing above the threshold of 0.5. The
probability of sustaining joint ecosystem functioning
was then calculated for each combination of remaining
species richness and number of functions considered.
We simulated random species loss for one to several
ecosystem functions using a simple computer sampling
routine. Sampling of each combination of species
richness and number of ecosystem functions was
repeated 10 000 times (the maximum number of
combinations was 18 480). From the repeated samples
we calculated the probability of sustaining joint
ecosystem functioning for each combination of species
loss and number of ecosystem functions. All simulations
were performed with MATLAB 7 (MathWorks 2007)
for the Apple Mac OS X.

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CONCEPTS & SYNTHESIS

DISCUSSION

FIG. 3. The probability of sustaining joint functioning with

changing species richness for (a) Seagrass I, (b) Seagrass II,
and (c) Seagrass III grazer studies (Duffy et al. 2001, 2005).
The number of functions (N) ranges from 3 to 4. The pattern
is identical for scenarios with one and two functions in
Seagrass I.

redundancy were observed, as the means of the pairwise

correlation coefcients between functions were close to 0
for most data sets (Fig. 4: y axis). Thus, there was a
higher probability that species extinctions affected joint
ecosystem functioning if more than one function was
considered.

Our calculations on empirical results showed clearly

that joint ecosystem functioning (i.e., the sustaining of
multiple functions) is more sensitive to species loss than
are single functions. An important message from these
analyses is that even though the performance of
individual functions can often be explained by the
presence of one or a few functionally dominant species
and is relatively insensitive to initial species loss, joint
functioning proved to be generally susceptible to the loss
of species. This denes a new type of complementarity
for species: complementarity across multiple functions.
To ensure overall functioning in the face of biodiversity
loss, it is thus important to consider the degree of
multifunctional redundancy.
Interestingly, the patterns in the empirical data sets
spanned the ranges of species lossfunctioning relationships covered in the conceptual model (Fig. 1b). The
results from Plants (Fig. 2a) mirrored the patterns of a
multifunctionally nonredundant community (species are
complementary in terms of which functions they are
important for), and the results from Bacteria (Fig. 2b)
mirrored those of a multifunctionally redundant assemblage (most species are important for all functions). The
Seagrass data also revealed that considering multiple
functions made the species assemblages more susceptible
to diversity loss (Fig. 3).
This general pattern was also shown by the comparison of redundancy within and across functions, where
redundancy across functions was generally low regardless of the degree of redundancy for single functions
(Fig. 4). Our simple approach to measuring redundancy
does not intend to give a general absolute measure for
the consequences of species loss, but it allows a
standardized comparison of relative redundancy across
data sets. We consider it a strength of our analysis that
we used different data sets, which had not initially been
collected to quantitatively test predictions on multifunctional effects of diversity loss. Across the organisms and
ecosystems used in these data sets, we arrived at a
general conclusion about the importance of biodiversity

FIG. 4. The means of the redundancy values

within single functions plotted against the means
of the correlation coefcients across multiple
functions. Error bars are 61 variance. Studies in
the graph are from left to right: Seagrass III,
Plants, Seagrass I, Seagrass II, and Bacteria. See
Analysis of empirical data: Calculation of redundancy.

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BIODIVERSITY AND MULTIPLE FUNCTIONS

Additionally, the width of single functions addressed in

BEF studies tends to be very narrow, often based on
production within one trophic level and consumption of
the next lower level (Cardinale et al. 2006). Giller et al.
(2004) strongly advocate that additional important
process rates in ecosystems should be analyzed within
the BEF framework.
None of the published BEF studies that have to date
measured multiple functions have looked at natural
ecosystems and nonrandom species loss. Future experiments should aim at lling this gap so that the results of
our analyses can be compared to alternative scenarios.
The fact that published studies have used experimentally
constructed communities does not mean, however, that
their studies on random species loss does not have any
relevance to natural systems. Researchers have often
chosen common species from the natural systems that
their assembled communities are supposed to mimic,
and the results from marine BEF experiments (e.g.,
Duffy et al 2003) appear to scale up to patterns found at
regional and global scales (Worm et al. 2006). We
believe that the results of our simple model, and the fact
that it is supported by the analyses of independent
empirical data, are robust in terms of different types of
extinction scenarios and types of density dependence,
since it includes no assumptions about these factors.
Within the eld of BEF, the terms ecosystem function
and functioning are often used as synonyms; the result is
some confusion regarding the meaning of these terms.
With an attempt to explicitly dene ecosystem functions
as single processes that together constitute overall
ecosystem functioning we believe that our interpretation
of the effects of biodiversity change will be facilitated.
Even though touched upon in earlier studies (Rosenfeld
2002a, b, Duffy 2003, Bracken and Stachowicz 2006),
the explicit and quantitative point that joint functioning
is more sensitive to species loss than are single ecosystem
functions, has only been brought forward twice (Hector
and Bagchi 2007, the present study). Turning to a
multifunctional perspective can move us away from the
traditional focus on sampling effects of dominant
species. In terms of resilience (the ability of a system
to return to its original state following a perturbation), a
multifunctional perspective provides new insights into
the way species can buffer for environmental uctuations and changes, as well as for perturbations and
stresses. Earlier work has pointed out the importance of
biodiversity for single functions in uctuating environments (Yachi and Loreau 1999), the role of phenotypic
trade-offs for the dynamics of functional group properties (Norberg et al. 2001), and the concept of response
diversity (Elmqvist et al. 2003). However, a focus on
multiple functions calls for further concerns. In the face
of external pressure on many ecosystems, ensuring
resilience requires management of a broader range of
species and traits than previously acknowledged.
Our results are also relevant to the discussion about
the goods and services derived by humans from

CONCEPTS & SYNTHESIS

in sustaining overall ecosystem functioning. Our model

and analyses conrmed the observation in Duffy et al.
(2003) that even where sampling can explain individual
ecosystem responses, only more diverse assemblages
maximized multiple ecosystem responses simultaneously. If our observed patterns should prove to be general,
they have important consequences for how the effects of
biodiversity should be interpreted.
The rst attempts to quantify the importance of
biodiversity for multiple functions (Hector and Bagchi
2007, and the present study) reach the same conclusion:
plant species richness is more important for multifunctionality than for single functions. Hector and
Bagchi (2007) analyzed a data set from the BIODEPTH
project (Hector et al. 1999). Similar to our study, they
based their analyses on presence/absence, but Hector
and Bagchi (2007) used backward-deletion multiple
regressions and the Akaike Information Criterion to
nd the most parsimonious set of species that inuences
each function. They thus used information on species
mixtures to predict the number of species required as
number of ecosystem functions increase (based on set
theory). Our model is based on the simpler, but more
general, concept of how combinations of monocultures
may sustain an increasing number of functions, and our
empirical analyses included a broader set of organisms
and functions. The combined results of both studies
suggest that effects of diversity on multiple ecosystem
functioning may be general.
The lack of a multifunctional perspective on BEF has
skewed the debate about the importance of species
richness and species identity. Many studies show
idiosyncratic effects of diversity on ecosystem functions
(Wardle et al. 1997, Emmerson et al. 2001), whereas
others show that diverse assemblages do not perform
signicantly better than the best monoculture (Cardinale
et al. 2006). Our results suggest that focusing on
individual functions can often be highly misleading,
because a high level of a single function does not equal
overall ecosystem functioning. In contrast, it is possible
that the mixture performs worse than the best monoculture for each individual function (unifunctional
underyielding), but still experiences multifunctional
overyielding because the identity of the best monoculture species switches between functions. Redundancy is
thus less likely to be present when multiple functions are
considered. As pointed out by Kareiva et al. (2007),
important ecosystem services may often be subject to
trade-offs, i.e., an increase in one service (e.g., biomass
production) may be accompanied by a decrease in
another (e.g., resistance to disease). Indeed, low
functional redundancy is conrmed in natural marine
systems (Micheli and Halpern 2005), suggesting that the
functioning of ecosystems can be tightly linked to
changes in biodiversity. Likewise, Heemsbergen et al.
(2004) show that between-species functional differences
over four traits explain positive net diversity effects for
two individual ecosystem processes in soil microcosms.

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ecosystems. Naeem (1998) discussed the concepts of

ecosystem failure and reliability and proposed: From
an ecosystem perspective, an ecosystem fails when it
ceases to provide the services and goods demanded of
it. If, from a management perspective, we dene a
range of functions (or services) that we intend to
preserve, any amount of species loss resulting in a
signicant lowering of any one of those functions could
be considered an ecosystem failure. Therefore, we
propose that ensuring multiple functions could be equal
to sustaining ecosystem integrity. By dening a range
and level of functions that are essential from the
perspective of ecosystem services and environmental
management, we can start to evaluate the effects of
biodiversity loss for real systems. Even though arbitrarily chosen, a 50% decrease in functioning could be
viewed as a level at which the ecosystem can no longer
provide the necessary ecosystem functions. There is little
discussion in the literature about what effect levels of
reduced ecosystem function could be viewed as ecologically signicant, and hence we had not much information to base our threshold levels on. In addition to the
EC50 index analogue, decreases in ecosystem function in
the range of 50% in the lowest compared to the highest
diversity treatments seem to be quite common in the
literature on biodiversity effects on ecosystem functioning (BEF). Average diversity effect sizes for both
terrestrial and aquatic ecosystems are ;0.5 (measured as
loge[response ratios]), which corresponds to ;40%
reduction in process rates for biomass production and
resource use (see Cardinale et al. 2006: Fig. 1).
Our model and analyses are only a small step to show
that species richness may affect the overall functioning
of ecosystems. For future analyses, several issues need to
be addressed when deciding how to jointly analyze
multiple functions, and there is a need for more studies
that look explicitly at multiple functions for realistic
ranges of diversity. Moreover, the potential consequences for ecosystem management have to be fully developed. We propose four emergent research tasks. First,
functions have to be dened more properly. Some
functions may be viewed as subparts of other functions;
for example, nutrient cycling is one part of the many
processes that determine primary productivity. A second
task related to ecosystem management is the weighting
of functions. Should the degradation of specic chemicals be viewed on a par with primary productivity, and
is pollination more, less, or equally important as
herbivory? Third, from a management perspective,
how many functions constitute ecosystem functioning?
Cardinale et al. (2006) consider biomass production at
the focal trophic level and resource use efciency, but
this denition neglects indirect effects (e.g., nutrient
regeneration by consumers) or rates of mutualism (N2
xation, pollination). Finally, we need theoretical and
empirical studies on how different extinction scenarios
and types of density dependence affect the relationship
between biodiversity and multiple functions. An effec-

Ecology, Vol. 89, No. 5

tive analytical framework should be able to address all

of these issues. By moving from a unifunctional to a
multifunctional approach, there will be a shift in the way
the effects of biodiversity loss will be interpreted, and
this will aid management and conservation of biological
values, as well as increase the understanding of the
benets of protecting biodiversity for our future.
ACKNOWLEDGMENTS
We thank J. Havenhand, B. Matthiessen, J. Bengtsson, and
M. Gamfeldt for stimulating discussions and valuable comments. Three anonymous reviewers provided comments that
strengthened the synthesis and discussion. We are grateful for
support from the Swedish Environmental Protection Agency
through the MARBIPP program (to L. Gamfeldt), FORMAS
through contract 215/2006-2096 (to P. R. Jonsson), the Swedish
Research Council through contract 621-2002-4770 (to P. R.
Jonsson), the Helge and Ax:son Johnson Foundation, the
Wahlstroms Foundation, the Colliander Foundation, the
Adlerbertska Foundation, the Ebba and Sven Schwartz
Foundation, and the Hasselblad Foundation.
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