Aspects of Applied Biology 115, 2012

Restoring diverse grassland: What can be achieved where, and what will it do for us?

Resilience of diverse grassland communities
By T HOCHSTRASSER1, G MOSER2, C KAMMANN2 and C MUELLER1,2
School of Biology and Environmental Science, University College Dublin, Ireland
2
Department of Plant Ecology, Justus-Liebig University, Giessen, Germany

1

Summary
Elevated CO2 effects (a press perturbation) on plants communities may alter community
dynamics and as such the response to extreme climatic events (pulse perturbation). The
ongoing Giessen FACE experiment (GiFACE) in Germany in a high diversity permanent
grassland presents a unique opportunity to study the combined effects of a press
perturbation with a pulse perturbation. The experiment was set up in 1998, and in 2003
the area was subject to a severe drought that significantly reduced biomass production.
The objective of this study was to elucidate the role of species diversity in the recovery
of primary productivity after drought under elevated CO2. It can be shown that due to
the high diversity in this grassland, biomass production had recovered one year after
drought to at least pre-drought levels. However, the community effects of the drought
were much longer lasting, with increased effective diversity, as expressed through species
turnover and variation in species abundances, for three years after the drought. While the
recovery of primary productivity in 2004 was related to species richness, species richness
tended to be negatively associated with variation in biomass production in subsequent
years, and a variation in primary productivity was better explained by effective diversity.
In conclusion, while there were small effects of elevated CO2 on community structure
observed over the course of the experiment, these effects did not influence the recovery
of primary productivity in elevated CO2 plots after the drought.
Key words: FACE, stability, press perturbation, pulse perturbation, diversity effect
Introduction
The ability of ecosystems to withstand extreme climatic events is an important issue, with the
frequency of such events increasing with climate change (Smith, 2011). Furthermore, ecosystems
are under a number of anthropogenic pressures such as increased nitrogen deposition, elevated
CO2, and changes in land use. The change in the dynamics of ecosystems under the latter is often
subtle, potentially leading to surprise outcomes in the longer term (Ives & Carpenter, 2007). The
study of the combined effects of pulse perturbations (as in the occurrence of extreme climatic
events) and press perturbations will help identify similarities and differences in the mechanisms
that lead to stability in ecosystem functioning under multiple perturbations.
FACE (Free Air Carbondioxide Enrichment) experiments offer a unique opportunity to study
the combined effects of a constant anthropogenic change in the environment, a press perturbation
(sensu Ives & Carpenter, 2007), and extreme climatic events (pulse perturbations). Unfortunately,
not all FACE experiments also allow the study of diversity effects as such systems often host
low numbers of species. The Giessen FACE experiment in Germany, however, was set-up in
1998 in a diverse temperate grassland system without initial disturbance as the experimental
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area was not ploughed and had been under the same management regime for around 100 years
(Jäger et al., 2003; Kammann et al., 2005). In 2003, 5 years after the initiation of the experiment,
Europe experienced an extreme climatic event (drought with heat-wave) that significantly reduced
primary productivity all over Europe (Ciais et al., 2005). This system thus presents us with the
unique opportunity of studying the interactions of a press perturbation with a pulse perturbation.
The overall objective of this paper was to investigate if and how species diversity contributed to
the recovery of primary productivity after drought and what the effect of the CO2 treatment (press
disturbance) had on this recovery. In particular, we asked the following questions:
1)
Did primary productivity decline in 2003 and how long did it take to recover?
2)
Does species diversity have an effect on the recovery of primary productivity after drought?
3)
Does elevated CO2 have an effect on species diversity and community dynamics?
4)
And thus, does elevated CO2 have an effect on the recovery of primary productivity after
drought?
It is hypothesised that the recovery after drought (pulse perturbation) is dependent on species
diversity effects due to species complementarity (Hector et al., 2010).
Methods
Study site
The Giessen FACE experiment (GiFACE) was set-up at a grassland research site near Giessen,
Germany (50°32’N, 8°41.3’E, 172 m a.s.l.). The vegetation at this site is a diverse hay meadow
typical of extensively managed temperate grasslands. Monitoring of the site started in 1993 and
elevated CO2 treatment (20% above ambient concentration during the day) was initiated in three
replicates in 1998 and is ongoing since then. For a detailed description of the site and the treatment
consult Jäger et al. (2003).
Sampling
Sampling of the vegetation occurs twice a year, once in spring (late May – early June) and once in
late summer (late August – early September) (Grüters et al., 2006). The community composition
of the vegetation is assessed in two 4.5 m2 sampling quadrats in each plot (ring) by estimating
%-cover for each species using a semi-categorical system, whereby Braun-Blanquet cover
categories1 were used except when cover was in-between categories and directly noted. One week
after the vegetation survey the aboveground biomass is harvested in 14 small sampling units
scattered throughout the plot (ring).
Analyses
A comparison of within plot to between plot variation showed that there is spatial autocorrelation
for sampling units within plots. It was therefore decided that the results from sampling units
within plot should be averaged for further analyses. All analyses were conducted separately for
the two seasons of sampling (spring and summer), except for primary productivity, which was
compared on a yearly basis to answer the first question. Primary productivity was defined as the
oven-dried harvested biomass per season. The recovery of primary productivity after the drought
was defined as follows:
Degree of recovery = biomass2004 – average(biomass98-02)
Species diversity was defined by the number of species per plot (species richness) and by
Simpson’s dominance index (D) (Simpson, 1949). Furthermore, it was considered that not only
r=0.1%, +=0.5%, 2m=1%, 2a=10%, 2b=20%, 3=37.5%, 4=62.5% and 5=87.5% (% cover is the mid-point
of the cover class).
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species number, but also the effective diversity as expressed by the variation in abundance of
species from year to year was important in explaining diversity effects. Therefore, an index of
‘effective diversity’ (EFFDIV) was calculated, which provided a combined measure of species
turnover and changes in species abundance:
EFFDIV = Σi abs(Log10(abupi+1) – Log10(abuci+1))
where abs is the absolute value, abup is the abundance of the species in the previous year and
abuc is the abundance of the species in the current year, i is an index ranging from 1 to the
total number of species. The log10 transformation of the abundances of species was undertaken
because of the multiplicative nature of cover data and because it improved the normality of the
data (LepšŠmilauer, 2003). Furthermore, years were classified according to the occurrence of the
drought in 2003. A pre-drought period was defined as 1998−2002, the drought year was treated
separately, and a post-drought period was defined (2004−2008). Based on preliminary analyses it
was found that while this classification of years into categories corresponds well to the dynamics
of primary productivity, the same classification could not be applied to effective diversity, which
continued to be high after the drought until 2006. Therefore, years were classified differently as
follows: 1998−2002: pre-drought period, 2003−2006: drought and recovery, and 2007−2008 postdrought
Stepwise, backward selection of explanatory variables was conducted using multiple linear
regression (proc glm) in SAS version 9.1. Only significant explanatory variables were retained.
For correlations between species richness or effective diversity and recovery Pearson’s correlation
coefficient (r) was used and correlations expressed as percentages (r2 * 100).
Results
Effect of drought on primary productivity
Primary productivity in 2003 was significantly different from other years of the experiment (Fig.
1). There was no difference between ambient and elevated CO2 in terms of how much productivity
declined and primary productivity recovered to pre-drought levels in both treatments in 2004.
2003 drought 

Fig. 1. Harvested biomass by year (A = ambient CO2, E = elevated CO2). Error bars represent standard
deviations. Treatments are not significantly different. Differences in mean are observed between the
drought (2003) year and all other years.

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Effect of species diversity on recovery after drought
Inspection of effective diversity (EFFDIV) over time shows that starting in 2003 the plots are
characterised by increased variability in species number and abundance until about 2006 (Fig.
2). These relatively large changes in community composition for an extended period after the
drought show that even though the system is stable and recovering ecosystem function (primary
productivity) within one year, the repercussions of the extreme climatic event on community
dynamics are much longer lasting and dynamics only return to normal boundaries of variation
four years after the drought. In 2004, a much higher percentage of primary productivity than usual
was due to the growth of subdominant forbs, including legumes (not shown).
a) Spring releve

b) Summer releve

Fig. 2. Effective diversity (EFFDIV) by year (A = ambient CO2, E = elevated CO2)
a) Spring releve; b) Summer releve. Error bars represent standard deviations. Ambient plots have
significantly higher EFFDIV in spring releves, treatments are not significantly different in summer releves.
Differences in mean are observed between pre-drought (1998−2002), drought and recovery (2003−2006)
and post-drought (2007−08) years (cf. text for details).

The variation of the recovery of biomass in 2004 was correlated to species richness with about
44 % of the variation in the spring biomass harvest explained by species richness (36% for the
late summer harvest). Interestingly, the variation in production from 2005 onwards was inversely
correlated to species richness and started to be positively correlated to effective diversity.
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Effect of elevated CO2 on species diversity and community dynamics
The effects of elevated CO2 on species diversity are insignificant in many cases. However, it
was found that elevated CO2 reduced species richness of the plots in late summer (P = 0.04). It
also increased species dominance (as expressed by Simpson’s dominance index), thus reducing
species evenness. In spring, dominance in CO2 plots increased over the duration of the experiment,
whereas dominance was higher in CO2 treatment plots throughout the experiment in late summer.
In spring, effective diversity (EFFDIV) was generally higher in control plots under ambient
CO2 than in elevated CO2 treatment plots (Fig. 2), whereas in summer there was no significant
difference between ambient and elevated CO2 plots in terms of effective diversity.
Effect of CO2 on recovery after 2003 drought
Overall, elevated CO2 did not affect the recovery of primary productivity after drought. Similar
to ambient plots, primary productivity was recovered within one year (Fig. 1).
Discussion
This study shows that elevated CO2 (press perturbation) does not have a strong effect on the
recovery of primary productivity of this diverse grassland after the drought and heat-wave of 2003.
The recovery was mostly due to a diversity effect, produced by differences in species abundance
and species richness. The effect of the extreme event (pulse perturbation) was long lasting in
terms of community dynamics, whereas primary productivity recovered within one year.
Some effects of elevated CO2 on the diversity of species could be observed. It seems likely
that elevated CO2 is enhancing the dominance of the vegetation. This supports the idea that
successively species that can take advantages of elevated CO2 to increase growth come to dominate
the vegetation. Interestingly, this increased dominance within the vegetation was also associated
with lower community dynamics (called effective diversity (EFFDIV) in this study) in the spring.
The spring sampling period is presumably the sampling period when abiotic conditions have the
most influence on community dynamics. In particular water and nitrogen shortages during this
early growth period may open up niches for species turnover. Under elevated CO2, however,
water use efficiency is improved and nitrogen cycling may be enhanced and thus fluctuation in the
abiotic environment may be dampened allowing less opportunities for subdominants to explore
temporary niches. This is different in late summer when competitive effects are more important.
Overall, it was shown that diversity is important in the recovery of this diverse grassland after
drought. In order to fully study the effect of higher [CO2] on community dynamics, it would
be necessary to allow diversity effects of the press perturbation to occur. This is not currently
possible as the study is set-up, as propagules are readily available on site and can disperse freely
between plots irrespective of treatment.
Acknowledgements
We thank the German Science Foundation (DFG) and the Hessian Agency for the Environment
(HLUG) for financial support. The vegetation data were gathered and prepared for analysis by
Anita Seifert and Sybille Janzen. The GiFACE is supported by technical staff and students at
the Justus Liebig University in Giessen all of whom we thank very much for their contributions.
T Hochstrasser was supported by University College Dublin seed funding to present at the AAB
conference.
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References
Ciais P, Reichstein M, Viovy N, Granier A, Ogee J, Allard V, Aubinet M, Buchmann N,
Bernhofer C, Carrara A, Chevallier F, De Noblet N, Friend A D, Friedlingstein P, Grunwald
T, Heinesch B, Keronen P, Knohl A, Krinner G, Loustau D, Manca G, Matteucci G, Miglietta
F, Ourcival J M, Papale D, Pilegaard K, Rambal S, Seufert G, Soussana J F, Sanz M J,
Schulze E D, Vesala T, Valentini R. 2005. Europe-wide reduction in primary productivity caused
by the heat and drought in 2003. Nature 437:529−533.
Grüters U, Janze S, Kammann C, Jäger H-J. 2006. Plant functional types and elevated CO2:
A method of scanning for causes of community alteration. Journal of Applied Botany and Food
Quality 80:116−128.
Hector A, Hautier Y, Saner P, Wacker L, Bagchi R, Joshi J, Scherer-Lorenzen M, Spehn
E M, Bazeley-White E, Weilenmann M, Caldeira M C, Dimitrakopoulos P G, Finn J A,
Huss-Danell K, Jumpponen A, Mulder C P H, Palmborg C, Pereira J S, Siamantziouras A
S D, Terry A C, Troumbis A Y, Schmid B, Loreau M. 2010. General stabilizing effects of plant
diversity on grassland productivity through population asynchrony and overyielding. Ecology
91:2213−2220.
Ives A R, Carpenter S R. 2007. Stability and diversity of ecosystems. Science 317:58−62.
Jäger H J, Schmidt S W, Kammann C, Grünhage L, Müller C, Hanewald K. 2003. The
university of Giessen Free-Air Carbon Dioxide Enrichment study: description of the experimental
site and of a new enrichment system. Journal of Applied Botany 77:117−127.
Kammann C, Grünhage L, Grüters U, Janze S, Jäger H J. 2005. Response of aboveground
grassland biomass and soil moisture to moderate long-term CO2 enrichment. Basic and Applied
Ecology 6:351−365.
Lepš J, Šmilauer P. 2003. Multivariate analysis of ecological data using CANOCO. Cambridge,
UK: Cambridge University Press.
Simpson E H. 1949. Measurement of diversity. Nature 163:688.
Smith M D. 2011. The ecological role of climate extremes: current understanding and future
prospects. Journal of Ecology 99:651−655.

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