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, Go teborg University, Tjarno Marine Biological Laboratory, SE-452 96 Stro mstad, 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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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.

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

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TABLE 1. Functions and correlations from the ve empirical studies analyzed in the study. No. species 12 Species type plants No. functions 6 Range of pairwise function correlations 0.80 to 0.69

Study Plants (Palmborg et al. 2005, Viketoft et al. 2005)

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

Bacteria (Jiang 2007)

bacteria

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

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.

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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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. 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.

CONCEPTS & SYNTHESIS

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

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DISCUSSION 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

CONCEPTS & SYNTHESIS

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.

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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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.

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

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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-

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 hlstro Wa ms Foundation, the Colliander Foundation, the Adlerbertska Foundation, the Ebba and Sven Schwartz Foundation, and the Hasselblad Foundation. LITERATURE CITED Aarssen, L. W. 1997. High productivity in grassland ecosystems: affected by species diversity or productive species? Oikos 80:183184. Balvanera, P., A. B. Psterer, N. Buchmann, J.-S. He, T. Nakashizuka, D. Raffaelli, and B. Schmid. 2006. Quantifying the evidence for biodiversity effects on ecosystem functioning and services. Ecology Letters 9:11461156. Bellwood, D. R., A. S. Hoey, and J. H. Choat. 2003. Limited functional redundancy in high diversity systems: resilience and ecosystem function on coral reefs. Ecology Letters 6: 281285. Bracken, M. E. S., and J. J. Stachowicz. 2006. Seaweed diversity enhances nitrogen uptake via complementary use of nitrate and ammonium. Ecology 87:23972403. Bruno, J. F., K. E. Boyer, J. E. Duffy, S. C. Lee, and J. S. Kertesz. 2005. Effects of macroalgal species identity and richness on primary production in benthic marine communities. Ecology Letters 8:11651174. Cardinale, B. J., D. S. Srivastava, J. Emmett Duffy, J. P. Wright, A. L. Downing, M. Sankaran, and C. Jouseau. 2006. Effects of biodiversity on the functioning of trophic groups and ecosystems. Nature 443:989992. Chapin, F. S., III, B. H. Walker, R. J. Hobbs, D. U. Hooper, J. H. Lawton, O. E. Sala, and D. Tilman. 1997. Biotic control over the functioning of ecosystems. Science 277:500504. Downing, A. L. 2005. Relative effects of species composition and richness on ecosystem properties in ponds. Ecology 86: 701715. Duffy, J. E., K. S. MacDonald, J. M. Rhode, and J. D. Parker. 2001. Grazer diversity, functional redundancy, and productivity in seagrass beds: an experimental test. Ecology 82: 24172434. Duffy, J. E., J. P. Richardson, and E. A. Canuel. 2003. Grazer diversity effects on ecosystem functioning in seagrass beds. Ecology Letters 6:637645. Duffy, J. E., J. P. Richardson, and K. E. France. 2005. Ecosystem consequences of diversity depend on food chain length in estuarine vegetation. Ecology Letters 8:301309. Elmqvist, T., C. Folke, M. Nystro m, G. Peterson, J. Bengtsson, B. Walker, and J. Norberg. 2003. Response diversity, ecosystem change, and resilience. Frontiers in Ecology and the Environment 1:488494. Emmerson, M., M. Solan, C. Emes, D. M. Paterson, and D. Raffaelli. 2001. Consistent patterns and the idiosyncratic effects of biodiversity in marine ecosystems. Nature 411:73 77.

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Gamfeldt, L., H. Hillebrand, and P. R. Jonsson. 2005. Species richness changes across two trophic levels simultaneously affect prey and consumer biomass. Ecology Letters 8:696 703. Giller, P. S., H. Hillebrand, U.-G. Berninger, M. O. Gessner, S. Hawkins, P. Inchausti, C. Inglis, H. Leslie, B. Malmqvist, M. T. Monaghan, P. J. Morin, and G. OMullan. 2004. Biodiversity effects on ecosystem functioning: emerging issues and their experimental test in aquatic environments. Oikos 104:423436. Hector, A., and R. Bagchi. 2007. Biodiversity and ecosystem multifunctionality. Nature 448:188190. Hector, A., et al. 1999. Plant diversity and productivity experiments in European grasslands. Science 286:11231127. Heemsbergen, D. A., M. P. Berg, M. Loreau, J. R. van Hal, J. H. Faber, and H. A. Verhoef. 2004. Biodiversity effects on soil processes explained by interspecic functional dissimilarity. Science 306:10191020. Hooper, D. U., et al. 2005. Effects of biodiversity on ecosystem functioning: a consensus of current knowledge. Ecological Monographs 75:335. Huston, M. A. 1997. Hidden treatments in ecological experiments: re-evaluating the ecosystem function of biodiversity. Oecologia 110:449460. Jiang, L. 2007. Negative selection effects suppress relationships between bacterial diversity and ecosystem functioning. Ecology 88:10751085. Kareiva, P., S. Watts, R. McDonald, and T. Boucher. 2007. Domesticated nature: shaping landscapes and ecosystems for human welfare. Science 316:18661869. Loreau, M. 2004. Does functional redundancy exist? Oikos 104: 606611. Loreau, M., and A. Hector. 2001. Partitioning selection and complementarity in biodiversity experiments. Nature 412:72 75. MathWorks. 2007. MATLAB 7.4.0.287. MathWorks, Natick, Massachusetts, USA. Micheli, F., and B. S. Halpern. 2005. Low functional redundancy in coastal marine assemblages. Ecology Letters 8:391400. Naeem, S. 1998. Species redundancy and ecosystem reliability. Conservation Biology 12:3945. Norberg, J., D. P. Swaney, J. Dushoff, J. Lin, R. Casagrandi, and S. A. Levin. 2001. Phenotypic diversity and ecosystem

functioning in changing environments: a theoretical framework. Proceedings of the National Academy of Sciences (USA) 98:1137611381. Paine, R. T. 2002. Trophic control of production in a rocky intertidal community. Science 296:736739. Palmborg, C., M. Scherer-Lorenzen, A. Jumpponen, G. Carlsson, K. Huss-Danell, and P. Hogberg. 2005. Inorganic soil nitrogen under grassland plant communities of different species composition and diversity. Oikos 110:271282. Petchey, O. L., and K. J. Gaston. 2002. Functional diversity (FD), species richness and community composition. Ecology Letters 5:402411. Rosenfeld, J. S. 2002a. Logical fallacies in the assessment of functional redundancy. Conservation Biology 16:837839. Rosenfeld, J. S. 2002b. Functional redundancy in ecology and conservation. Oikos 98:156162. Solan, M., B. J. Cardinale, A. L. Downing, K. A. M. Engelhardt, J. L. Ruesink, and D. S. Srivastava. 2004. Extinction and ecosystem function in the marine benthos. Science 306:11771180. Spehn, E. M., et al. 2005. Ecosystem effects of biodiversity manipulations in European grasslands. Ecological Monographs 75:3763. Tilman, D., J. Knops, D. Wedin, P. Reich, M. Ritchie, and E. Siemann. 1997. The inuence of functional diversity and composition on ecosystem processes. Science 277:13001302. Viketoft, M., C. Palmborg, B. Sohlenius, K. Huss-Danell, and J. Bengtsson. 2005. Plant species effects on soil nematode communities in experimental grasslands. Applied Soil Ecology 30:90103. Walker, B. H. 1992. Biodiversity and ecological redundancy. Conservation Biology 6:1823. Wardle, D. A., K. I. Bonner, and K. S. Nicholson. 1997. Biodiversity and plant litter: experimental evidence which does not support the view that enhanced species richness improves ecosystem function. Oikos 79:247258. Worm, B., et al. 2006. Impacts of biodiversity loss on ocean ecosystem services. Science 314:787790. Yachi, S., and M. Loreau. 1999. Biodiversity and ecosystem productivity in a uctuating environment: the insurance hypothesis. Proceedings of the National Academy of Sciences (USA) 96:14631468.

CONCEPTS & SYNTHESIS