Journal of Ecology 2011, 99, 572–582
doi: 10.1111/j.1365-2745.2010.01783.x
Impact of above- and below-ground invertebrates on
temporal and spatial stability of grassland of different
diversity
Nico Eisenhauer1*†, Alexandru Milcu2, Eric Allan3, Norma Nitschke3, Christoph Scherber4,
Vicky Temperton5, Alexandra Weigelt6, Wolfgang W. Weisser3 and Stefan Scheu1
1
Georg-August-University Goettingen, J.F. Blumenbach Institute of Zoology and Anthropology, Berliner Str. 28, 37073
Goettingen, Germany; 2NERC Centre for Population Biology, Division of Biology, Imperial College London, Silwood
Park Campus, Ascot SL5 7PY, UK; 3Friedrich-Schiller-University, Institute of Ecology, Dornburger Str. 159, 07743
Jena, Germany; 4Georg-August-University Goettingen, Institute of Agroecology, Waldweg 26, 37073 Goettingen, Germany; 5IBG-2 Plant Sciences, Forschungszentrum Juelich, 52425 Juelich, Germany; 6University of Leipzig, Institute of
Biology, Johannisallee 21-23, 04103 Leipzig, Germany
Summary
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 belowground 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.
Key-words: above- and below-ground interrelationships, biodiversity loss, biodiversity–
ecosystem functioning relationship, earthworms, herbivore insects, Jena Experiment, plant–
soil (below-ground) interactions, variability
Introduction
*Correspondence author. E-mail: [email protected]
†Present address: Department of Forest Resources, University of
Minnesota, 1530 Cleveland Ave. N., St Paul, MN 55108, USA.
Current anthropogenic global change phenomena threaten
ecosystem functions and services including system properties
such as productivity and stability. Biodiversity has been
2011 The Authors. Journal of Ecology 2011 British Ecological Society
Spatial and temporal stability 573
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 perfor-
mance, 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 managementinduced 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.
2011 The Authors. Journal of Ecology 2011 British Ecological Society, Journal of Ecology, 99, 572–582
574 N. Eisenhauer et al.
Materials and methods
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).
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
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).
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, n = 80 subplots), ambient and reduced below-ground insects (n = 152 subplots), and ambient and reduced above-ground insects (n = 158
2011 The Authors. Journal of Ecology 2011 British Ecological Society, Journal of Ecology, 99, 572–582
Spatial and temporal stability 575
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 (n = 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: n = 4; above-ground insect subplots:
n = 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 (r = 0.71, P < 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 n = 4, temporal replicates n = 3), the
below-ground insect experiment (spatial n = 4, temporal n = 3) and
the above-ground insect experiment (spatial n = 3, temporal n = 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
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% (aboveground 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
2011 The Authors. Journal of Ecology 2011 British Ecological Society, Journal of Ecology, 99, 572–582
3,30
2,30
1,30
1,30
Excl.
30,38
1,38
Excl.
Excl.
1,38
Excl.
38
5.13
5.67
1.81
5.00
Excl.
3.33
1.44
Excl.
Excl.
5.66
Excl.
0.0055
0.0077
0.1669
0.0330
Excl.
0.0003
0.2371
Excl.
Excl.
0.0225
Excl.
3,32
1,32
1,32
1,32
1,32
32,38
1,38
1,38
Excl.
Excl.
Excl.
38
2.67
8.58
9.51
1.96
9.19
3.56
2.35
4.35
Excl.
Excl.
Excl.
0.0641
0.0062
0.0042
0.1713
0.0048
0.0001
0.1336
0.0439
Excl.
Excl.
Excl.
P
3,63
1,63
1,63
Excl.
Excl.
63,75
1,75
Excl.
Excl.
Excl.
Excl.
75
d.f.
5.81
4.51
5.72
Excl.
Excl.
2.74
0.9
Excl.
Excl.
Excl.
Excl.
F
0.0013
0.0372
0.0069
Excl.
Excl.
<0.0001
0.3459
Excl.
Excl.
Excl.
Excl.
P
3,67
5,67
1,67
Excl.
1,67
67,77
1,77
Excl.
Excl.
Excl.
Excl.
77
d.f.
2.40
3.21
5.81
Excl.
2.17
2.28
0.28
Excl.
Excl.
Excl.
Excl.
F
Spatial stability
0.0759
0.0118
0.0196
Excl.
0.1453
0.003
0.5955
Excl.
Excl.
Excl.
Excl.
P
3,72
1,72
1,72
Excl.
1,72
72,77
1,77
1,77
Excl.
Excl.
Excl.
77
d.f.
4.20
6.87
9.52
Excl.
5.59
3.25
5.29
0.81
Excl.
Excl.
Excl.
F
Temporal stability
0.0086
0.0107
0.0029
Excl.
0.0207
<0.0001
0.0241
0.3723
Excl.
Excl.
Excl.
P
Above-ground insects
3,72
1,72
1,72
1,72
1,72
72,77
1,77
1,77
Excl.
1,77
Excl.
77
d.f.
2.19
10.55
9.36
6.16
4.19
1.55
1
4.85
Excl.
4.22
Excl.
F
Spatial stability
0.0968
0.0018
0.0031
0.0154
0.0444
0.0297
0.3206
0.0306
Excl.
0.0433
Excl.
P
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: n = 45; below-ground insects: n = 81; and aboveground insects: n = 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.
d.f., degrees of freedom; Excl., excluded from the statistical model.
Block
SR
FR
GR
LE
PL
IT
IT · SR
IT · FR
IT · GR
IT · LE
Error
F
d.f.
d.f.
P
Temporal stability
Spatial stability
Temporal stability
F
Below-ground insects
Earthworms
Table 1. Impacts of invertebrates on the stability of above-ground primary productivity
576 N. Eisenhauer et al.
2011 The Authors. Journal of Ecology 2011 British Ecological Society, Journal of Ecology, 99, 572–582
Spatial and temporal stability 577
(a)
(b)
(c)
(d)
(e)
(f)
(g)
(h)
(i)
(j)
(k)
(l)
Fig. 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.
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.
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% (belowground insect experiment) and )44% (above-ground insect
experiment). Similarly, temporal variability decreased with
increasing plant functional group richness by )28% (belowground 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.
2011 The Authors. Journal of Ecology 2011 British Ecological Society, Journal of Ecology, 99, 572–582
578 N. Eisenhauer et al.
RELATIONSHIP BETWEEN SPATIAL AND TEMPORAL
Discussion
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 aboveground insect treatments (Fig. 2c,e).
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, P = 0.06), below-ground insect (F1,70 = 1.79,
P = 0.19) and above-ground insect experiment (F1,78 = 3.39,
P = 0.07). Further, spatial variability and module density
were negatively correlated (r = )0.32, P = 0.0037), whereas
temporal variability was not correlated significantly with module density (r = )0.10, P = 0.40). Moreover, although the
regression slopes between spatial and temporal variability did
not differ significantly in the earthworm treatments
(t = )1.31, P > 0.1; Fig. 2a,b), they differed significantly
between below-ground insect (t = 7.14, P < 0.005; Fig. 2c,d)
and above-ground insect treatments (t = 4.02, P < 0.005;
Fig. 2e,f).
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
(a)
(b)
(c)
(d)
(e)
(f)
Fig. 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.
2011 The Authors. Journal of Ecology 2011 British Ecological Society, Journal of Ecology, 99, 572–582
Spatial and temporal stability 579
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 belowground 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 aboveground 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
2011 The Authors. Journal of Ecology 2011 British Ecological Society, Journal of Ecology, 99, 572–582
580 N. Eisenhauer et al.
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). Belowground 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 aboveground insects decouple the spatial and temporal stability of
grassland plant communities.
Conclusions
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
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).
2011 The Authors. Journal of Ecology 2011 British Ecological Society, Journal of Ecology, 99, 572–582
Spatial and temporal stability 581
N.E. is grateful for a postdoctoral scholarship by the German Science Foundation (Ei 862 ⁄ 1-1).
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Supporting Information
Additional Supporting Information may be found in the online version of this article:
Fig. S1. Temperature and precipitation from 2002 to 2009.
Fig. 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.
As a service to our authors and readers, this journal provides supporting information supplied by the authors. Such materials may be
re-organized for online delivery, but are not copy-edited or typeset.
Technical support issues arising from supporting information (other
than missing files) should be addressed to the authors.
Received 15 July 2010; accepted 1 December 2010
Handling Editor: Richard Bardgett
2011 The Authors. Journal of Ecology 2011 British Ecological Society, Journal of Ecology, 99, 572–582