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Keywords:

  • above- and below-ground interrelationships;
  • biodiversity loss;
  • biodiversity–ecosystem functioning relationship;
  • earthworms;
  • herbivore insects;
  • Jena Experiment;
  • plant–soil (below-ground) interactions;
  • variability

Summary

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Conclusions
  8. Acknowledgements
  9. References
  10. Supporting Information

1. Recent theoretical studies suggest that the stability of ecosystem processes is not governed by diversity per se, but by multitrophic interactions in complex communities. However, experimental evidence supporting this assumption is scarce.

2. We investigated the impact of plant diversity and the presence of above- and below-ground invertebrates on the stability of plant community productivity in space and time, as well as the interrelationship between both stability measures in experimental grassland communities.

3. We sampled above-ground plant biomass on subplots with manipulated above- and below-ground invertebrate densities of a grassland biodiversity experiment (Jena Experiment) 1, 4 and 6 years after the establishment of the treatments to investigate temporal stability. Moreover, we harvested spatial replicates at the last sampling date to explore spatial stability.

4. The coefficient of variation of spatial and temporal replicates served as a proxy for ecosystem stability. Both spatial and temporal stability increased to a similar extent with plant diversity. Moreover, there was a positive correlation between spatial and temporal stability, and elevated plant density might be a crucial factor governing the stability of diverse plant communities.

5. Above-ground insects generally increased temporal stability, whereas impacts of both earthworms and above-ground insects depended on plant species richness and the presence of grasses. These results suggest that inconsistent results of previous studies on the diversity–stability relationship have in part been due to neglecting higher trophic-level interactions governing ecosystem stability.

6. Changes in plant species diversity in one trophic level are thus unlikely to mirror changes in multitrophic interrelationships. Our results suggest that both above- and below-ground invertebrates decouple the relationship between spatial and temporal stability of plant community productivity by differently affecting the homogenizing mechanisms of plants in diverse plant communities.

7.Synthesis. Species extinctions and accompanying changes in multitrophic interactions are likely to result not only in alterations in the magnitude of ecosystem functions but also in its variability complicating the assessment and prediction of consequences of current biodiversity loss.


Introduction

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Conclusions
  8. Acknowledgements
  9. References
  10. Supporting Information

Current anthropogenic global change phenomena threaten ecosystem functions and services including system properties such as productivity and stability. Biodiversity has been identified as one of the most important biotic factors driving the stability of ecosystems (Yachi & Loreau 1999; Tilman 2000; Loreau et al. 2001), and its current decline may therefore significantly impact ecosystem services (Loreau et al. 2001; Jenkins 2003). This prompted a number of studies exploring the factors affecting stability of ecosystems (McCann 2000; Otto, Rall & Brose 2007; Brose 2008). However, from early empirical and theoretical work (Odum 1953; Elton 1958; May 1973) until today (Bezemer & van der Putten 2007; Ives & Carpenter 2007; Van Ruijven & Berendse 2010), the relationship between diversity and stability has been controversial. More recently, biodiversity has been shown to govern major facets of ecosystem stability such as temporal (Tilman, Reich & Knops 2006) and spatial variability (Weigelt et al. 2008), resistance against perturbations (Mulder, Uliass & Doak 2001) and invasions (Fargione & Tilman 2005), resilience (Tilman & Downing 1994) and reliability (Naeem & Li 1997). A consensus is emerging, focusing on the varying levels of organization and interconnectance of ecosystem components (Berlow 1999; Brose, Willians & Martinez 2006; Ives & Carpenter 2007). Importantly, the strength of interactions between taxa (Berlow 1999; Berlow et al. 2009) and the non-random organization of food webs (Otto, Rall & Brose 2007; Brose 2008) have been found to stabilize ecological systems. The insurance hypothesis postulates that diversity ‘insures ecosystems against declines in their functioning since various species provide greater guarantees that some will maintain functioning even if others fail’ (Naeem & Li 1997; Yachi & Loreau 1999). Mechanisms responsible for positive diversity–stability relationships include the averaging effect (Doak et al. 1998) and the negative covariance effect (Tilman, Lehman & Bristow 1998). The former assumes smoothing of average system performance through inclusion of additional (possibly de-synchronous) components, whereas the latter suggests that the stability of functions at the community level is increased due to buffering variations in abiotic and biotic factors in space and time. In addition to diversity, certain functional groups, such as legumes and grasses in grassland, have been reported to significantly impact the stability of ecosystem functions by affecting local resource availability and by building ramified root systems, respectively (Weigelt et al. 2008).

Although different measures of ecosystem stability have been used and in part explored in one experiment (McNaughton 1985), to our knowledge temporal and spatial stability have never been investigated together in one experiment to explore their interrelationships. Weigelt et al. (2008) assumed that spatial niche complementarity renders diverse plant communities more stable in space suggesting that spatial and temporal stability might be related. Thus, spatial stability of ecosystem functions might also induce temporal stability. To further explore the interrelationship between spatial and temporal stability, we studied variation in plant community productivity by sampling spatial and temporal replicates on the same experimental plots of a large grassland biodiversity experiment (Jena Experiment; Roscher et al. 2004).

Above- and below-ground invertebrates are increasingly recognized as important agents impacting plant performance, competition and thus plant community composition in grassland (Wardle et al. 2004; Weisser & Siemann 2004; Bardgett et al. 2005). Moreover, recent reviews suggest the possibility of cascading extinctions as a consequence of declining plant diversity (Hooper et al. 2000; De Deyn & van der Putten 2005). The Jena Experiment was the first experiment to manipulate plant species richness and the composition of below- and above-ground animals simultaneously. In addition, the experimental design allows to investigate whether invertebrates impact the diversity–stability relationship of primary producers since trophic interrelationships in food webs need to be considered if we are to understand the relationship between the diversity and stability of ecological communities (Schmitz 1997; McCann 2000; Wilby & Shachak 2004; Dunne et al. 2005; Howe et al. 2006).

Earthworms and soil insects, in particular Collembola, may enhance plant community stability via increased and more constant nutrient availability, but they may also reduce it by improving the competitive strength of certain plant species and/or functional groups in space and/or time (Partsch, Milcu & Scheu 2006; Eisenhauer & Scheu 2008). For instance, Eisenhauer et al. (2008) showed that earthworms influence the resistance of plant communities against plant invaders and this effect varied with plant diversity. Similarly, above-ground insects may either stabilize plant communities by reducing the dominance of single species (Brose 2008), or destabilize them by increasing the competitive strength of certain plant species (Schädler, Brandl & Haase 2007). Moreover, as invertebrate densities vary in time and effects depend on plant community diversity and composition (Eisenhauer et al. 2008, 2009a), impacts of invertebrates are likely to vary with plant diversity as well as with time, thereby possibly altering the diversity–stability relationship.

Naturally occurring perturbations affecting ecosystem stability comprise summer drought and soil freezing during winter (see Fig. S1 in Supporting Information), while mowing of the vegetation twice a year imposes management-induced disturbances (Roscher et al. 2004). We used two measures of stability [by using the coefficient of variation (CV)], the spatial and the temporal stability of above-ground primary productivity, the most common ecosystem function measured in biodiversity–ecosystem functioning experiments (McCann 2000; Tilman, Reich & Knops 2006; Weigelt et al. 2008). We investigated the impact of above-ground and below-ground invertebrates on the spatial and temporal stability of plant community productivity and on the relationship between spatial and temporal stability in model grassland systems of varying plant species (1–60) and functional group richness (1–4). We hypothesized that plant diversity stabilizes plant community productivity in space and time. Further, we expected spatial and temporal stability to be correlated. Additionally, we explored whether invertebrates impact the spatial and temporal stability, and whether the relationship between both stability measures is affected by invertebrates.

Materials and methods

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Conclusions
  8. Acknowledgements
  9. References
  10. Supporting Information

Experimental setup

This study was conducted in the framework of the Jena Experiment, a large field experiment investigating the role of biodiversity for element cycling and trophic interactions in grassland communities (Roscher et al. 2004). The study site is located on the floodplain of the Saale River at the northern edge of Jena (Thuringia, Germany). Mean annual air temperature is 9.3 °C and annual precipitation is 587 mm (Kluge & Müller-Westermeier 2000). Prior to the establishment of the experiment in May 2002, the site had been used as an arable field for 40 years and the soil is a Eutric Fluvisol. The studied system represents Central European mesophilic grassland traditionally used as hay meadow (Arrhenatherion community). A pool of 60 native plant species was used to establish a gradient of plant species (1, 2, 4, 8, 16 and 60) and plant functional group richness (1, 2, 3 and 4) in 82 plots of 20 × 20 m (see Table S1A; Roscher et al. 2004). Using above- and below-ground morphological traits (growth form, canopy height, rooting depth and capacity for clonal growth), phenological traits (occupancy of seasonal niches, life cycle and seasonality of foliage) and N2 fixation ability, plant species were aggregated into four plant functional groups: grasses (16 species), small herbs (12 species), tall herbs (20 species) and legumes (12 species). More details on the classification of plant functional groups are given in Roscher et al. (2004). Experimental plots were mown twice a year (June and September), as is typical for hay meadows, and weeded twice a year (April and July) to maintain the target species composition. Plots were assembled into four blocks following a gradient in soil characteristics, each block containing an equal number of plots of plant species and plant functional group richness levels. Further information on the design and setup of the Jena Experiment is given in Roscher et al. (2004).

Manipulation of animal densities

Earthworms

Earthworm densities were manipulated on the 1 (16 replicates), 4 (16 replicates) and 16 plant species richness plots (14 replicates) starting in September 2003 (see Table S1A). On each plot, two randomly selected subplots of 1 × 1 m were used to initially establish ‘earthworm’ and ‘earthworm reduction’ treatments. Subplots were enclosed with PVC shields above ground (20 cm) and below ground (15 cm) to reduce colonization by earthworms. In the first 3 years of the experiment, ‘earthworm’ subplots received 25 adult individuals of Lumbricus terrestris L. (average fresh weight with gut content 4.10 ± 0.61 g) per year (15 individuals in spring and 10 in autumn) as earthworm density was low after establishment of the Jena Experiment. Earthworm addition was stopped in 2006 as colonization of the field by earthworms had reached equilibrium level, as indicated by similar earthworm densities in control and earthworm addition subplots (Eisenhauer et al. 2008). To reduce earthworm density in ‘earthworm reduction’ subplots, earthworms were extracted twice a year (spring and autumn) by electro-shocking (for details, see Eisenhauer et al. 2009a). The success of earthworm density manipulations was proven by measuring the soil surface activity of L. terrestris, which was significantly lower (−38%) in the earthworm reduction treatment than in the earthworm treatment (Eisenhauer et al. 2008). Higher earthworm densities resulted in elevated plant productivity (Eisenhauer et al. 2009a).

Below-ground insects

To manipulate soil insect densities, two subplots of 2 × 4 m within each plot were established. One subplot remained untreated (ambient density, ‘below-ground insect’ treatment), whereas the second subplot was treated with insecticide to reduce soil insect densities (‘reduced below-ground insect’ treatment). Starting in April 2003, insecticide subplots were sprayed monthly from April to November with an aqueous solution of the organothiophosphate insecticide chlorpyrifos (Hortex, Dow AgroSciences LCC, Indiapolis, IN, USA; 2% w/w; 40 g in 1 L water, 125 mL m−2; Celaflor, Dow AgroSciences LCC) using a backpack sprayer (Birchmeier Senior; operating pressure 2 × 105 Pa; Birchmeier Sprühtechnik AG, Stetten, Switzerland) to the soil surface. Whenever possible the insecticide was applied prior to precipitation events (based on weather forecasts) to increase insecticide incorporation into the soil. Chlorpyrifos is widely used in agriculture and has been shown to have negligible side effects on plants (Schädler et al. 2004).

In spring and autumn 2006, the efficiency of the insecticide treatment was explored by sampling and identifying soil animals in both subplots. Although densities of Collembola (−52%), phytophagous Coleoptera (−35%), Hemiptera (−66%), Araneida (−53%), zoophagous Coleoptera (−63%), Gamasida (−69%) and Hymenoptera (−77%) were significantly reduced in insecticide subplots, other soil animal taxa remained unaffected (Lumbricidae, Isopoda, Diptera larvae, Gastropoda and Chilopoda) or increased (Oribatida; Eisenhauer et al. 2010a). To analyse the impact of below-ground insect manipulation on plant productivity, we used two model plant species, Lolium perenne and Centaurea jacea, representing major plant functional groups of grassland communities (grasses and herbs). Both performed significantly better in control than in insecticide subplots, pointing to the prevailing importance of insect decomposers (Eisenhauer et al. 2010a).

Above-ground insects

In order to reduce above-ground insect densities, we applied an above-ground insecticide on subplots of 4 × 5 m starting in 2003 (‘reduced above-ground insect’ treatment). The ‘core area’ of 10 × 15 m (Roscher et al. 2004) remained untreated and served as a control (ambient density, ‘above-ground insect’ treatment). Insecticide subplots were sprayed with an aqueous solution of the organothiophosphate insecticide dimethoate (30 mL m−2; BASF, Ludwigshafen, Germany) at 4-week intervals between April and August using a wheeled handcart with engine (Birchmeier Senior; operating pressure 40 × 105 Pa). Dimethoate has been shown to be effective in reducing insect herbivory while having negligible direct effects on non-target organisms including plants (Hector et al. 2004; Schädler et al. 2004). To assess the success of insecticide application, insect herbivory was quantified repeatedly (Scherber et al. 2006). Above-ground herbivory decreased significantly in insecticide subplots compared with control subplots by c. −44% (Scherber et al. 2006). However, it should be noted that herbivory was only assessed for one plant species (Rumex acetosa) that had been planted into all plots of the Jena Experiment as a model species.

Sampling

Plant community biomass was harvested from all subplots [ambient and reduced earthworms (1, 4 and 16 plant species plots, = 80 subplots), ambient and reduced below-ground insects (= 152 subplots), and ambient and reduced above-ground insects (= 158 subplots)] using two metal frames of 200 × 500 mm cutting shoots 30 mm above the soil surface in May 2004, 2007 and 2009, i.e. 1, 4 and 6 years after the establishment of the treatments. In 2009, three metal frames were harvested in the above-ground insect experiment. At each sampling, we harvested above-ground biomass at different locations in the respective subplots. Subplot-specific data from single years served as temporal replicates (= 3). In 2009, plant community biomass from earthworm and below-ground insect subplots was harvested using four frames of 200 × 250 mm each and analysed separately. As described above, in above-ground insect subplots, three metal frames of 200 × 500 mm were harvested. Frames taken from the same subplot were taken as spatial replicates (earthworm and below-ground insect subplots: = 4; above-ground insect subplots: = 3). Plant community biomass per frame was stored in paper bags and dried at 70 °C to constant weight.

As an explanatory variable potentially influencing spatial and temporal stability of plant productivity, we determined the total module density in August 2005 and June 2006 by counting plant modules in two subsamples of 200 × 500 mm (see Marquard et al. 2009b for more information). Since module densities per plot in 2005 and 2006 were closely correlated (= 0.71, < 0.001), we used the mean of both years as a covariate.

Calculations

The CV is a widely used measure of stability in ecological experiments (McCann 2000). We used the CV (standard deviation divided by the mean) of above-ground primary productivity [g m−2], as the most common ecosystem function measured in biodiversity–ecosystem functioning experiments, to evaluate the plant community stability in time and space (McCann 2000; Tilman, Reich & Knops 2006; Weigelt et al. 2008). Thus, we calculated the CV from spatial and temporal replicates (R) of each experimental subplot (i) separately as follows: CVi = standard deviationi (R1i; R2i; R3i; [R4i])/meani (R1i; R2i; R3i; [R4i]). Replicates in squared brackets indicate that four replicates were only available in the case of spatial stability of the earthworm and below-ground insect experiment.

In the following, we will use the terms stability and variability as antonyms. We analysed three experiments: the earthworm experiment (spatial replicates = 4, temporal replicates = 3), the below-ground insect experiment (spatial = 4, temporal = 3) and the above-ground insect experiment (spatial = 3, temporal = 3). These experiments were analysed separately due to differences in the size of subplots, the number and size of frames used for harvesting plants, and the usage of plastic shields as surrounding of the earthworm subplots.

We did not consider invertebrate treatment effects on the diversity–plant productivity relationship in the present study as this has been done elsewhere (Eisenhauer et al. 2009a). Mean plant community biomass per subplot in each year and the number of the plots considered in the present study are given in Table S1B.

It should be noted that the results presented here are based on weeded plant communities and therefore the stability of plant productivity refers to plants remaining after weeding as is the case in previous studies (Tilman, Reich & Knops 2006; Weigelt et al. 2008).

Statistical analyses

Normal distribution and homogeneity of variance were improved by log-transformation. Split-plot GLMs (Generalized Linear Models, type I sum of squares; sas 9.2, SAS Institute Inc., Cary, NC, USA) were used to analyse the effects of Block, plant species richness (SR), plant functional group richness (FR), presence of grasses (GR), presence of legumes (LE), plot, invertebrates (IT for invertebrate treatment; EW for earthworms, BGINS for below-ground insects, AGINS for above-ground insects), and the interactions between invertebrates and SR, FR, GR and LE on the spatial and temporal variability of plant community productivity in sequential analyses (Schmid et al. 2002). Sequential analysis was chosen to account for (i) the block design of the experiment and (ii) the non-independence between SR and FR (Roscher et al. 2004).

F-values given in text and tables refer to those where the respective factor (and interaction) was fitted first (Schmid et al. 2002). Table S2 provides information of the significance of plant diversity measures when fitted second. Block was always fitted first followed by SR and FR (whose sequence was alternated). Then, the effects of presence of certain plant functional groups (whose sequence was alternated) were calculated followed by plot, invertebrates, and the respective interactions between invertebrates and plant community properties. Treatments analysed at the plot scale (Block, SR, FR, GR, LE) were tested against the variance between plots to avoid pseudoreplication, whereas treatments analysed at the subplot scale (invertebrates and interactions) were tested against the total variance (Scheiner & Gurevitch 2001). After fitting the full model, the respective models were optimized by excluding non-significant factors using Akaike’s Information Criterion (not shown; Burnham & Anderson 1998) and by testing Block, SR and FR either as categorical or as continuous factors. Plant diversity measures have been reported to exert both linear and nonlinear effects on ecosystem functioning. By analysing both categorical and continuous factors, we fitted the most adequate model for each response variable. Additionally, we performed separate GLMs for temporal variability fitting spatial variability as a covariate to investigate whether excluding the respective variance affects the significance of plant diversity measures in order to explore the interrelationship between spatial and temporal variability. To illustrate the relationship between spatial and temporal variability in the different invertebrate treatments, regressions were carried out (statistica 7.1; StatSoft, Tulsa, OK, USA). Moreover, further regressions were carried out to investigate the relationship between spatial and temporal stability and total module density. We compared the regression slopes between treatments with ambient and reduced invertebrate density using two-sided t-tests.

Results

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Conclusions
  8. Acknowledgements
  9. References
  10. Supporting Information

Spatial variability

Spatial variability of plant community productivity decreased, i.e. spatial stability increased with increasing plant diversity (plant species richness and plant functional group richness) in each of the three experiments (Table 1; Fig. 1). Spatial variability decreased from monocultures to the highest plant species richness level analysed by −58% (earthworm experiment), −38% (below-ground insect experiment) and −59% (above-ground insect experiment). Similarly, spatial variability decreased from communities containing one plant functional group to those containing four functional groups by −56% (earthworm experiment), −27% (below-ground insect experiment) and −43% (above-ground insect experiment). In contrast to the earthworm experiment and the below-ground insect experiment, spatial variability was significantly lower in the presence than in the absence of grasses in above-ground insect subplots (−42%; Table 1). The presence of legumes inconsistently impacted spatial variability; although spatial variability increased in earthworm subplots (+22%), and was not affected in below-ground insect subplots, it decreased in above-ground insect subplots in the presence of legumes (−8%; Table 1). Moreover, it decreased with increasing plant species richness in both earthworm and reduced earthworm treatments, but the decrease was more pronounced in the latter (significant Earthworm × Plant species richness interaction; Fig. 1a,b; Table 1). Similarly, the decrease in spatial variability with increasing plant diversity was more pronounced in reduced above-ground insect than in above-ground insect treatments (Fig. 1i,j; Table 1). By contrast, manipulation of below-ground insect density did not alter the diversity–stability relationship (Fig. 1e,f). Moreover, the impact of above-ground insects depended on the presence of grasses in the plant community. Although, in the reduced above-ground insect treatment, spatial variability slightly decreased in the absence of grasses (−4%), it increased in the presence of grasses (−26%; see Fig. S2b). The remaining interactions between invertebrate treatments and plant community properties did not significantly affect spatial stability.

Table 1.   Impacts of invertebrates on the stability of above-ground primary productivity
 EarthwormsBelow-ground insectsAbove-ground insects
Temporal stabilitySpatial stabilityTemporal stabilitySpatial stabilityTemporal stabilitySpatial stability
d.f.FPd.f.FPd.f.FPd.f.FPd.f.FPd.f.FP
  1. anova table of F- and P-values on the effects of block, plant species richness (SR), plant functional group richness (FR), presence of grasses (GR) and legumes (LE), plot (PL) and invertebrates (IT; earthworms, below-ground insects and above-ground insects, respectively) on the coefficient of variation of shoot biomass in time (temporal stability) and space (spatial stability). Error terms are given in italics and significant effects are given in bold. Effects of abiotic properties (block) are not highlighted. Not all plots (earthworms: = 45; below-ground insects: = 81; and above-ground insects: = 81) entered the statistical analyses due to missing values in space or time. Note that SR and FR were fitted as categorical or continuous factor.

  2. d.f., degrees of freedom; Excl., excluded from the statistical model.

Block3,305.130.00553,322.670.06413,635.810.00133,672.400.07593,724.200.00863,722.190.0968
SR2,305.670.00771,328.580.00621,634.510.03725,673.210.01181,726.870.01071,7210.550.0018
FR1,301.810.16691,329.510.00421,635.720.00691,675.810.01961,729.520.00291,729.360.0031
GR1,305.000.03301,321.960.1713Excl.Excl.Excl.Excl.Excl.Excl.Excl.Excl.Excl.1,726.160.0154
LEExcl.Excl.Excl.1,329.190.0048Excl.Excl.Excl.1,672.170.14531,725.590.02071,724.190.0444
PL30,383.330.000332,383.560.000163,752.74<0.000167,772.280.00372,773.25<0.000172,771.550.0297
IT1,381.440.23711,382.350.13361,750.90.34591,770.280.59551,775.290.02411,7710.3206
IT × SRExcl.Excl.Excl.1,384.350.0439Excl.Excl.Excl.Excl.Excl.Excl.1,770.810.37231,774.850.0306
IT × FRExcl.Excl.Excl.Excl.Excl.Excl.Excl.Excl.Excl.Excl.Excl.Excl.Excl.Excl.Excl.Excl.Excl.Excl.
IT × GR1,385.660.0225Excl.Excl.Excl.Excl.Excl.Excl.Excl.Excl.Excl.Excl.Excl.Excl.1,774.220.0433
IT × LEExcl.Excl.Excl.Excl.Excl.Excl.Excl.Excl.Excl.Excl.Excl.Excl.Excl.Excl.Excl.Excl.Excl.Excl.
Error38  38  75  77  77  77  
image

Figure 1.  Impacts of invertebrates on the diversity–stability relationship. Regressions between (a and b) spatial and (c and d) temporal variability and plant species richness in (a and c) earthworm (ambient) and (b and d) earthworm reduction treatments. Regressions between (e and f) spatial and (g and h) temporal variability and plant species richness in (e and g) below-ground insect (ambient) and (f and h) reduced below-ground insect treatments. Regressions between (i and j) spatial and (k and l) temporal variability and plant species richness in (i and k) above-ground insect (ambient) and (j and l) reduced above-ground insect treatments. Axes are given on a logarithmic scale. Lines indicate significant regressions.

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Temporal variability

Similar to spatial variability, temporal variability of plant community productivity decreased with increasing plant diversity (Table 1; Fig. 1). Temporal variability decreased from monocultures to the highest plant species richness level analysed by −29% (earthworm experiment), −43% (below-ground insect experiment) and −44% (above-ground insect experiment). Similarly, temporal variability decreased with increasing plant functional group richness by −28% (below-ground insect experiment; 1 vs. 4 plant functional groups) and −31% (above-ground insect experiment; 1 vs. 3 plant functional groups). Temporal variability decreased significantly in the presence of legumes in above-ground insect subplots (−31%) but not in earthworm and below-ground insect subplots (Table 1). Moreover, temporal variability increased significantly in the reduced above-ground insect treatment (+15%) whereas the main effects of earthworms and below-ground insects were not significant. Invertebrates did not significantly affect the relationship between plant species richness and temporal variability (Fig. 1s,d,g,h,k,l). However, temporal variability was slightly higher in the earthworm treatment than in the reduced earthworm treatment in the absence of grasses (+8%), whereas it was considerably lower in the earthworm treatment than in the reduced earthworm treatment in the presence of grasses (−24%; see Fig. S2a), resulting in an overall reduction of temporal variability in the presence of grasses. The remaining plant community properties and the interactions with invertebrate treatments did not significantly impact temporal variability.

Relationship between spatial and temporal stability

Generally, spatial variability and temporal variability were positively correlated (Fig. 2). This relationship did not differ between earthworm and earthworm reduction treatments (Fig. 2a,b). By contrast, in below- and above-ground insect treatments, the positive relationship between spatial and temporal variability was highly significant in reduced insect treatments (Fig. 2d,f), whereas there was no significant correlation between the two stability measures in below- and above-ground insect treatments (Fig. 2c,e).

image

Figure 2.  Regressions between spatial and temporal variability of plant community productivity in subplots with (a) ambient and (b) reduced earthworm density, (c) ambient and (d) reduced below-ground insect density, and (e) ambient and (f) reduced above-ground insect density. Axes are given on a logarithmic scale. Lines indicate significant regressions.

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Fitting the spatial variability as a covariate in separate sequential analyses rendered the effect of plant species richness on the temporal variability insignificant in the earthworm (F2,34 = 3.16, = 0.06), below-ground insect (F1,70 = 1.79, = 0.19) and above-ground insect experiment (F1,78 = 3.39, = 0.07). Further, spatial variability and module density were negatively correlated (= −0.32, = 0.0037), whereas temporal variability was not correlated significantly with module density (= −0.10, = 0.40). Moreover, although the regression slopes between spatial and temporal variability did not differ significantly in the earthworm treatments (= −1.31, > 0.1; Fig. 2a,b), they differed significantly between below-ground insect (= 7.14, < 0.005; Fig. 2c,d) and above-ground insect treatments (= 4.02, < 0.005; Fig. 2e,f).

Discussion

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Conclusions
  8. Acknowledgements
  9. References
  10. Supporting Information

Plant diversity and plant community stability

As found in previous studies, plant diversity stabilized plant community productivity in space and time in each of our three experiments. Weigelt et al. (2008) highlighted the importance of the functional traits rooting depth and clonal growth, and concluded that the positive effect of functional diversity on spatial stability is less pronounced than impacts on temporal stability. Our results do not support this assumption as both spatial and temporal stability responded similarly to plant diversity. Potentially, the inconsistent findings are related to the varying duration of the experiments. The study of Weigelt et al. (2008) was performed in year 3 after establishment of the Jena Experiment whereas our study was performed in year 7. In agreement with this assumption, Tilman, Reich & Knops (2006) found the impact of plant diversity on the spatial stability of grassland communities to increase with time in a decade-long grassland experiment. Further, our assumption is supported by recent findings showing that overyielding and stability of ecosystems are correlated (Tilman 1999; Tilman, Reich & Knops 2006), with the importance of overyielding increasing in time (Cardinale et al. 2007; Marquard et al. 2009a). The present study thus suggests that spatial and temporal stability of plant community productivity are affected similarly by plant diversity, and that in the long term species richness is crucial for ecosystem functioning, reinforcing the significance of the singular hypothesis (Eisenhauer et al. 2010b). Impacts of plant diversity on the stability of plant productivity were largely consistent despite the fact that the three experiments differed in the size of experimental subplots (1–20 m²), the number of frames (3–4), the area harvested (0.2–0.3 m²) and the usage of plastic shields as barriers of earthworm subplots, underlining the generality and robustness of the diversity–stability relationship.

In addition to previously proposed mechanisms governing the stability of diverse plant communities (averaging effect, Doak et al. 1998; negative covariance effect, Tilman, Lehman & Bristow 1998; increasing relevance of overyielding in time, Tilman, Reich & Knops 2006; Marquard et al. 2009a), we hypothesize that elevated plant density is crucial for community stability. Recently, the positive diversity–productivity relationship has been ascribed to increased plant module density (density of tillers and rosettes) rather than to increased module size (Marquard et al. 2009b). Interestingly, we found that module density was closely and negatively correlated with spatial variability adding to the relevance of plant density as an essential community trait not only for community productivity (Marquard et al. 2009b) but also for its stability.

Invertebrates and plant community stability

Plant community productivity and stability in temperate grassland were shown to be tightly coupled to the functional diversity of arbuscular mycorrhizal fungi (Van der Heijden et al. 1998), indicating that species interactions need to be included if we are to understand mechanisms responsible for the diversity–stability relationship of ecosystems (Schmitz 1997; McCann 2000; Wilby & Shachak 2004; Dunne et al. 2005; Howe et al. 2006). Nevertheless, experimental evidence is extremely scarce (McCann 2000). To address this deficiency, we investigated whether invertebrates impact the relationship between plant diversity and plant community stability as they function as decomposers (earthworms and below-ground insects) and herbivores (above-ground insects), both of which are known to affect plant community biomass and composition (Weisser & Siemann 2004).

Both earthworms and above-ground insects, but not below-ground insects, affected the diversity–stability relationship. Spatial variability of plant community productivity decreased more steeply with plant species richness in the reduced earthworm treatment as compared to the control with ambient density of earthworms. This might have been due to the fact that earthworms differentially affect plant species and functional groups via acceleration of nutrient cycling thereby altering below-ground plant competition (Wurst, Langel & Scheu 2005; Eisenhauer et al. 2009a), which likely differed between plant species richness levels due to varying earthworm densities (Eisenhauer et al. 2009b). Moreover, earthworms impact plant community assembly directly by influencing plant community invasibility (Eisenhauer et al. 2008); this is likely to increase the spatial variability of plant communities, in particular in more diverse plant communities where earthworm densities are elevated (Eisenhauer et al. 2009b).

In addition to spatial stability, earthworms also affected the temporal stability of plant community productivity but this varied with the presence of grasses. When grasses were absent, earthworms decreased temporal stability, whereas the opposite was true in the presence of grasses. Grasses were shown to be particularly affected by decomposer activity, which may be due to their high demand for soil nitrogen and highly branched root system (Wurst, Langel & Scheu 2005; Eisenhauer & Scheu 2008). Therefore, more continuous and elevated nutrient mobilization in the presence of earthworms (Partsch, Milcu & Scheu 2006; Eisenhauer et al. 2009a) could be responsible for the enhanced temporal stability of grass productivity, and therefore probably also causing changes in the relationship between plant species richness and temporal stability.

Above-ground insects impacted the relationship between spatial stability and plant diversity, and influenced the temporal stability of plant productivity. The increase in spatial stability with plant diversity was more pronounced in the reduced above-ground insect treatment compared with the above-ground insect treatment, which was mainly due to higher stability of diverse plant communities (16 and 60 species mixtures). Overall, temporal stability was significantly increased in above-ground insect treatments compared with the reduced above-ground insect treatment. Although above-ground insect populations vary strongly in time at the Jena Experiment field site (W. Voigt, unpubl. data), they are able to stabilize the productivity of primary producers. In a recent theoretical study on the impacts of top-down (herbivore effects) and bottom-up (nutrient effects) forces, Brose (2008) showed that herbivory predominantly reduced the biomass of dominant producer species. This resulted in a more even biomass distribution and thus in producer coexistence (stability). Moreover, Carson & Root (2000) showed that insects reduce the abundance of dominant plant species. In line with these results, experimental manipulations of herbivores (grasshoppers) at the field site of the Jena Experiment showed that selective feeding changed the functional composition and dominance structure of plant communities (Scherber et al. 2010). Therefore, herbivory might increase plant community evenness and maintain assemblages containing different life-strategies, thereby enhancing temporal stability in line with the insurance hypothesis (Naeem & Li 1997; Yachi & Loreau 1999).

Our finding that above-ground insects may significantly affect the stability of plant productivity in diverse plant communities is supported by results of another long-term grassland experiment (BioCON; Reich et al. 2001). In this experiment, plants growing in polycultures experienced a fivefold increase in damage from generalist herbivores, but 64% less damage from specialist herbivores as compared to monocultures (Lau et al. 2008). This suggests that varying impacts of above-ground insects on the stability of plant community productivity at least in part are due to shifts in the population dynamics of generalist and specialist herbivores as this might affect the dominance of certain plant species.

Impacts of above-ground insects not only depended on the diversity of plant communities but also on the presence of grasses. Although ambient densities of above-ground insects slightly decreased the spatial stability of plant community productivity in the absence of grasses, they increased the spatial stability in the presence of grasses. Generally, grasses increased the spatial stability of plant community productivity due to the fact that they build evenly distributed shoot systems by filling empty space by clonal growth and formation of new ramets (Weigelt et al. 2008). Thus, grasses might capture resources in the soil in a spatially more uniform way than other plant functional groups (Bessler et al. 2009), and this stabilizing effect may be enlarged by insect herbivores. However, the addition of insecticides possibly results in rather unspecific effects varying between herbivore species and also affecting higher trophic levels. Although the assessment of herbivory for one model plant species (R. acetosa; Scherber et al. 2006) may not adequately mirror the complexity of insecticide effects on the whole above-ground food web, these data indeed suggests reduced herbivory in insecticide plots. Overall, our results highlight that plant community properties, such as plant diversity, key plant functional groups and invertebrates impact plant community stability in space and time in an interactive way. Thus, ecosystem stability is likely governed by complex multitrophic interactions both above and below the ground.

Interrelationship between spatial and temporal stability

Although many studies have looked at effects of diversity on temporal stability, investigations analysing drivers of both temporal and spatial stability in one experiment are lacking. This may be due to the fact that investigating different stability measures and trophic levels requires large efforts in particular in field experiments (McCann 2000). Based on results from an extensive field study, McNaughton (1985) reported five of seven stability measures to be positively associated with diversity, particularly with functional diversity. In the present study, we investigated whether different stability characteristics of plant communities, i.e. spatial and temporal stability, are correlated. Interestingly, spatial and temporal stability changed to a similar extent with plant diversity and, indeed, spatial and temporal stability were positively correlated, confirming our expectations. The experimental design, however, does not allow inferring whether this correlation implies causation. Presumably, complementary resource use in diverse plant communities increases the tolerance for perturbations in both time and space (Weigelt et al. 2008; Marquard et al. 2009a). The presence of plant species with varying life-history strategies (see Roscher et al. 2004 for more information) in diverse plant communities is therefore likely to buffer both spatial and temporal variability as predicted by the insurance hypothesis (Naeem & Li 1997; Yachi & Loreau 1999). Although proposed before (Weigelt et al. 2008), we presented the first experimental indication that diversity does increase both temporal and spatial stability. However, the temporal stability of plant productivity might also be caused by the elevated spatial stability of diverse plant communities as suggested by the positive relationship between module density and overyielding (Marquard et al. 2009b). Interestingly, fitting spatial variability as a covariate in separate analyses rendered the effect of plant species richness on temporal variability insignificant in all three experiments supporting the assumption that both stability measures rely on similar mechanisms.

Further, the present results indicate that this relationship is affected by below- and above-ground invertebrates. Invertebrates differently affected stability measures resulting in highly significant correlations between temporal and spatial stability in the presence of reduced invertebrate densities, whereas the correlation disappeared in the presence of ambient below- and above-ground insects. Thus, regression slopes of treatments with ambient and reduced insect densities varied significantly. The presence of above-ground insects generally increased the temporal stability of plant productivity, but their effect on spatial stability depended on the diversity and composition of the plant community. Particularly in plant communities varying little in space, above-ground insects presumably increase temporal stability. This again suggests that herbivores dampen fluctuations in plant community productivity in time and increase plant community stability (Brose 2008). Below-ground insects neither affected temporal nor spatial stability; however, they weakened the relationship between these stability measures. Although we lack a mechanistic understanding of how below-ground insects affect the stability of plant productivity, the present study indicates that below- and above-ground insects decouple the spatial and temporal stability of grassland plant communities.

Conclusions

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Conclusions
  8. Acknowledgements
  9. References
  10. Supporting Information

This study indicates that spatial stability and temporal stability of plant productivity are correlated. Moreover, changes in species diversity in one trophic level are unlikely to mirror changes in multitrophic interrelationships, suggesting that inconsistent results of previous studies on the diversity–stability relationship in part have been due to the fact that higher trophic-level interactions governing ecosystem stability have been neglected. Our results further suggest that both above- and below-ground invertebrates decouple the relationship between spatial and temporal stability of plant community productivity by inconsistently affecting the homogenizing mechanisms of plants in diverse plant communities. Hence, species extinctions likely result not only in alterations in the magnitude of ecosystem functions but also in its variability in space and time, complicating the assessment and prediction of consequences of current biodiversity loss.

Acknowledgements

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Conclusions
  8. Acknowledgements
  9. References
  10. Supporting Information

We thank all the people who helped to establish and manage the experimental field site, particularly the former coordinator C. Roscher for managing the biomass harvest in 2004, E. Marquard for providing the data on module density, and the gardeners S. Eismann, S. Hengelhaupt, S. Junghans, U. Köber, K. Kuntze and H. Scheffler. Further, we thank U. Wehmeier, L. Clement, S. Partsch and A.C.W. Sabais for ensuring insecticide treatments and C.M. Pusch, A. Roos, D.T. Tran and T. Keil for the help during earthworm extractions. Comments of two anonymous referees helped to improve the work. The Jena Experiment is funded by the German Science Foundation (FOR 456). N.E. is grateful for a postdoctoral scholarship by the German Science Foundation (Ei 862/1-1).

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  6. Discussion
  7. Conclusions
  8. Acknowledgements
  9. References
  10. Supporting Information
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Supporting Information

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Conclusions
  8. Acknowledgements
  9. References
  10. Supporting Information

Figure S1 Temperature and precipitation from 2002 to 2009.

Figure S2 Impacts of invertebrates and presence of grasses on the stability of plant community productivity.

Table S1. Design of the Jena Experiment.

Table S2. Impacts of plant diversity measures on the stability of above-ground primary productivity

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