Climate extremes initiate ecosystem‐regulating functions while maintaining productivity

Abstract

Summary1. Studying the effects of climate or weather extremes such as drought and heat waves on biodiversity and ecosystem functions is one of the most important facets of climate change research. In particular, primary production is amounting to the common currency in field experiments world-wide. Rarely, however, are multiple ecosystem functions measured in a single study in order to address general patterns across different categories of responses and to analyse effects of climate extremes on various ecosystem functions.2. We set up a long-term field experiment, where we applied recurrent severe drought events annually for five consecutive years to constructed grassland communities in central Europe. The 32 response parameters studied were closely related to ecosystem functions such as primary production, nutrient cycling, carbon fixation, water regulation and community stability.3. Surprisingly, in the face of severe drought, above- and below-ground primary production of plants remained stable across all years of the drought manipulation.4. Yet, severe drought significantly reduced below-ground performance of microbes in soil indicated by reduced soil respiration, microbial biomass and cellulose decomposition rates as well as mycorrhization rates. Furthermore, drought reduced leaf water potential, leaf gas exchange and leaf protein content, while increasing maximum uptake capacity, leaf carbon isotope signature and leaf carbohydrate content. With regard to community stability, drought induced complementary plant–plant interactions and shifts in flower phenology, and decreased invasibility of plant communities and primary consumer abundance.5. Synthesis. Our results provide the first field-based experimental evidence that climate extremes initiate plant physiological processes, which may serve to regulate ecosystem productivity. A potential reason for different dynamics in various ecosystem services facing extreme climatic events may lie in the temporal hierarchy of patterns of fast versus slow response. Such data on multiple response parameters within climate change experiments foster the understanding of mechanisms of resilience, of synergisms or decoupling of biogeochemical processes, and of fundamental response dynamics to drought at the ecosystem level including potential tipping points and thresholds of regime shift. Future work is needed to elucidate the role of biodiversity and of biotic interactions in modulating ecosystem response to climate extremes.

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SPECIAL FEATURE
ECOLOGICAL CONSEQUENCES OF CLIMATE EXTREMES
Climate extremes initiate ecosystem-regulating
functions while maintaining productivity
Anke Jentsch1*, Juergen Kreyling2, Michael Elmer3, Ellen Gellesch2, Bruno Glaser4,
Kerstin Grant2, Roman Hein2, Marco Lara4, Heydar Mirzae5, Stefanie E. Nadler2,
Laura Nagy1, Denis Otieno5, Karin Pritsch6, Uwe Rascher7, Martin Scha ¨ dler8,
Michael Schloter6, Brajesh K. Singh9, Jutta Stadler9, Julia Walter10, Camilla Wellstein2,
Jens Wo ¨ llecke3and Carl Beierkuhnlein2
1Disturbance Ecology, University of Bayreuth, D-95440 Bayreuth, Germany;2Biogeography, University of Bayreuth,
95440 Bayreuth, Germany;3Soil Protection and Recultivation, BTU Cottbus, Konrad-Wachsmann-Allee 6, 03046
Cottbus, Germany;4Soil Biogeochemistry, Martin-Luther University of Halle-Wittenberg, von Seckendorfplatz 3, 06120
Halle, Germany;5Plant Ecology, University of Bayreuth, 95440 Bayreuth, Germany;6Terrestrial Ecogenetics, Helmholtz
Zentrum Muenchen, German Research Center for Environmental Health, Ingolstaedter Landstrabe 1, 85764 Neuher-
berg, Germany;7Institute of Chemistry and Dynamics of the Geosphere, ICG-3, Phytosphere, Research Centre Ju ¨lich,
Leo-Brandt-Str., D-52425 Ju ¨lich, Germany;8Community Ecology, Helmholtz-Centre for Environmental Research – UFZ,
Theodor-Lieser-Str. 4, 06110 Halle, Germany;9Centre for Plants and Environment, University of Western Sydney,
Penrith South DC, NSW, Australia; and10Conservation Biology, UFZ-Helmholtz, Centre fu ¨r Environmental Research,
Permoserstr. 15, 04318 Leipzig, Germany
Summary
1. Studying the effects of climate or weather extremes such as drought and heat waves on biodiver-
sity and ecosystem functions is one of the most important facets of climate change research. In par-
ticular, primary production is amounting to the common currency in field experiments world-wide.
Rarely, however, are multiple ecosystem functions measured in a single study in order to address
general patterns across different categories of responses and to analyse effects of climate extremes
onvariousecosystemfunctions.
2. We set up a long-term field experiment, where we applied recurrent severe drought events annu-
ally for five consecutive years to constructed grassland communities in central Europe. The 32
response parameters studied were closely related to ecosystem functions such as primary produc-
tion,nutrientcycling,carbonfixation,waterregulationandcommunitystability.
3. Surprisingly, in the face of severe drought, above- and below-ground primary production of
plantsremainedstableacrossallyearsofthedroughtmanipulation.
4. Yet, severe drought significantly reduced below-ground performance of microbes in soil indi-
cated by reduced soil respiration, microbial biomass and cellulose decomposition rates as well as
mycorrhizationrates.Furthermore,droughtreducedleafwaterpotential,leafgasexchangeandleaf
protein content, while increasing maximum uptake capacity, leaf carbon isotope signature and leaf
carbohydratecontent.Withregardtocommunitystability,droughtinducedcomplementaryplant–
plant interactions and shifts in flower phenology, and decreased invasibility of plant communities
andprimaryconsumerabundance.
5. Synthesis. Our results provide the first field-based experimental evidence that climate extremes
initiate plantphysiological processes, whichmay serve toregulateecosystem productivity.A poten-
tial reason for different dynamics in various ecosystem services facing extreme climatic events may
lieinthetemporalhierarchyofpatternsoffastversusslowresponse.Suchdataonmultipleresponse
parameterswithinclimatechangeexperimentsfostertheunderstandingofmechanismsofresilience,
*Correspondence author. E-mail: anke.jentsch@uni-landau.de
? 2011 The Authors. Journal of Ecology ? 2011 British Ecological Society
Journal of Ecology 2011, 99, 689–702doi: 10.1111/j.1365-2745.2011.01817.x

Page 2

of synergisms or decoupling of biogeochemical processes, and of fundamental response dynamics
to drought at the ecosystem level including potential tipping points and thresholds of regime shift.
Future work is needed to elucidate the role of biodiversity and of biotic interactions in modulating
ecosystemresponsetoclimateextremes.
Key-words: below-ground, competition, decomposition, invasion, leaf chemistry, microbial,
phenology, plant–climate interactions, precipitation change, productivity
Introduction
Currently, knowledge about ecological responses to climate
change is based largely on effects of climatic trends such as
gradual warming, precipitation change and CO2enrichment.
However, the magnitude and frequency of climate or weather
extremes such as severe drought, heat waves, heavy rain and
late frost events are expected to increase in the near future
(IPCC 2007; O’Gorman & Schneider 2009). Thus, predictions
ofeffectsofclimate extremes on species,communitiesand eco-
systemshavebecomecriticaltoscienceandsociety.Yet,conse-
quences of future climate extremes for ecosystem functions
and services are largely unknown and have only recently been
addressed by ecological research (Gutschick & BassiriRad
2003; Schro ¨ ter et al. 2005; Jentsch 2006; Jentsch, Kreyling &
Beierkuhnlein 2007; Suttle, Thomsen & Power 2007; Knapp
et al. 2008; Fisher, Turner & Morling 2009; Jentsch & Bei-
erkuhnlein2010).
There is growing concern that climatic extremes such as
severe drought could negatively affect ecosystem functioning
and stability. A review of the literature revealed that the focus
over the last decade has been primarily on primary productiv-
ity (Figure S1a–d and Table S1 in Supporting Information),
one of the major common currencies in global ecology. The
findings from existing climate change studies on drought
effects are highly controversial. While some field experiments
showed that natural and simulated drought led to decreases of
primary productivity (Olesen & Bindi 2002; Morecroft et al.
2004;Penuelaset al.2004;Ciaiset al.2005),othersdidnotfind
any significant effects of locally severe drought manipulations
(Fay et al. 2000; Kreyling et al. 2008c). Generally, evidence
suggests that an elongation of inter-rainfall intervals as well as
changesin seasonaltiming are more likely to cause areduction
of above-ground net primary productivity (ANPP) than
reduced total rainfall quantity per se (Fay et al. 2000; Swem-
mer,Knapp&Snyman2007).
However,furtheraspectsconfound thedebateon ecosystem
functioninginthelightofclimatechange.First,theroleofbio-
diversityinensuringtheperformanceofecosystemfunctioning
(Balvanera et al. 2006; Worm et al. 2006; Hector & Bagchi
2007; Suttle, Thomsen & Power 2007) and in enhancing resis-
tanceorresiliencetodroughthasbeenproventobefundamen-
tal (Pfisterer & Schmid 2002; Kahmen, Perner & Buchmann
2005; De Boeck et al. 2008; van Ruijven & Berendse 2010).
Secondly, multiple ecosystem functions in the face of climate
extremes have rarely been addressed simultaneously in experi-
ments(Jentsch,Kreyling&Beierkuhnlein2007;Jentsch&Bei-
erkuhnlein 2008, 2010). Prevailing response parameters in
climate change experiments are above-ground production, soil
C:N ratio and soil respiration (Figure S1d, Table S2). How-
ever, the interrelationships between above-ground primary
production and below-ground nutrient cycling, carbon fixa-
tionorwaterregulationarerarelyaddressed.
Here, we analyse the effects of recurrent severe drought
(local 100-year or1000-year extreme events) on multiple eco-
systempropertiesofaplantedgrasslandinCentralEuropeina
long-term field experiment (EVENT-I) located in Bayreuth,
Germany. Semi-natural European grasslands are widespread,
of economic value, provide many ecological services and are
important for nature conservation. They have been managed
either as hay meadows or pastures in Europe for thousands of
years.
Our goal was to assess whether there are general patterns
across these different categories of important ecosystem func-
tions including primary productivity, water regulation, carbon
fixation,nutrientcyclingandcompositionalstabilitytoclimate
extremes.
We expected the grassland ecosystem to react sensitively to
extreme recurrent drought events, and specifically hypothe-
sized that (i) above-ground productivity would be decreased;
and (ii) other ecosystem functions, such as water regulation,
carbon fixation, nutrient cycling and compositional stability,
wouldbenegativelyimpacted.
Materials and methods
EXPERIMENTAL DESIGN
The EVENT-I experiment (Jentsch, Kreyling & Beierkuhnlein 2007)
is established in the Ecological Botanical Garden of the University
of Bayreuth, Germany (49?55¢19¢¢N, 11?34¢55¢¢E, 365 m a.s.l.) with
a mean annual temperature of 8.2 ?C and a mean annual precipita-
tion of 724 mm (1971–2000). Precipitation is distributed bi-modally
with a major peak in June⁄July and a second peak in Decem-
ber⁄January (data: German Weather Service). The experiment was
carried out with two fully crossed factors: (i) climate extremes
(severe drought, ambient control); (ii) community diversity (two
species of one functional group, four species of two functional
groups, and four species of three functional groups, monocultures
of particular species), representing key species combinations of
grassland. The total setup consisted of five replicates of each facto-
rial combination, 60 plots in total of 2 · 2 m in size. The factors
were applied in a split-plot design with the vegetation types and
diversity levels blocked and randomly assigned within each drought
manipulation (Jentsch, Kreyling & Beierkuhnlein 2007). The origi-
nally installed species composition was maintained by periodical
weeding. The texture of the previously homogenized and constantly
drained soil consisted of loamy sand (82% sand, 13% silt, 5% clay)
690A. Jentsch et al.
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with pH = 4.5 in the upper and pH = 6.2 in the lower soil layer
(measured in 1 m KCl). Data acquisition was carried out in the cen-
tral square metre of each plot only, in order to circumvent edge
effects.
CLIMATIC EXTREMES
Theclimatemanipulationsconsistedofextremedroughtandambient
conditions for control. Extremeness of drought events was deter-
mined by statistical extremity with respect to a historical reference
period (extreme value theory) independent of its effects on organisms
(Jentsch2006). Inparticular, intensityof the treatmentswas basedon
the local 100-year extreme event in 2005, 2006 and 2007, and on the
local 1000-year extreme event for 2008 and 2009. Vegetation periods
(March–September) of 1961–2000 were used as the reference period
(data: German Weather Service). Gumbel I distributions were fitted
totheannualextremes,and100-yearand1000-yearrecurrenceevents
werecalculated.
Drought was defined as the number of consecutive days with less
than 1 mm daily precipitation. Accordingly, a drought period of
32 days (2005–2007) and of 42 days (2008 and 2009) was applied in
the experiment during the peak growing season in June. Maximum
valuesinthehistoricaldatasetwere33 dayswithout rainduringJune
and July 1976. Drought was induced with the support of rain-out
shelters that permitted nearly 90% penetration of photosynthetically
activeradiation.
Unwanted greenhouse effects were avoided by starting the roof
from a height of 80 cm, allowing for near-surface air exchange. After
the experimental drought period, the roofs were removed. A lateral
surface flow was avoided by plastic sheet pilings around treated plots
reachingdowntoadepthof10 cm.
The ambient control plots (C) remained without manipulation
throughout the entire period. A roof artefact control with five repli-
cates of the rain-out shelters was in place in 2006. Adding the same
amountofwaterasoccurrednaturallyindailyresolutionbelowintact
shelters during the drought manipulation period did not result in any
significant differences in response parameters, indicating no signifi-
canteffectfromthe slightly increased temperaturecausedbythe rain-
outshelters.
EXPERIMENTAL PLANT COMMUNITIES
Overall, grasslands are spatially important ecosystems in Central
Europe. Five widespread plant species were chosen from the regional
flora, i.e. Arrhenatherum elatius (L.) P. Beauv. ex J. Presl & C. Presl,
Holcus lanatus L., Geranium pratense L., Lotus corniculatus L. and
Plantago lanceolata L. Species were selected with respect to their
affiliation to defined functional groups (grasses, forbs, leguminous
forbs), to life span (perennials), to overall importance in nearby and
Central European grassland systems, and to the fact that they do
naturally grow on substrate similar to the one used in this experi-
ment. One hundred plant individuals per plot in defined quantitative
composition were planted in a systematic hexagonal grid with 20 cm
distance between individuals in early April 2005. Grass and forb indi-
viduals used in the experiment were grown from seeds in a green-
house in the preceding fall. Thus, all plants were in a juvenile stage
during manipulation and data acquisition. All plants had been accli-
mated on site since February 2005, reaching growth heights of
c. 15 cm. Biomass at planting amounted to 0.1–0.6 g dry wt per indi-
vidual. These experimental communities represent naturally occur-
ring species combinations. The grassland plots were established at
two levels of species diversity (2 and 4 species) and three levels of
functional diversity (1, 2, 3 functional groups), resulting in three spe-
cies combinations or communities in total (Table 1) plus monocul-
tures of selected species.
RESPONSE PARAMETER
The 32 parameters measured are categorized into five key ecosystem
functions (Fig. 1) and are described below in order of their appear-
ance, except for soil moisture, whichis presented first. Since complete
time series data are not available for all parameters, it is indicated in
Table S3 whether data from five consecutive years or from particular
years were sampled. All data presented in Fig. 1 are derived from
yearsofmaximumdroughteffects.
SOIL MOISTURE
Soilmoisturewasrecordedbytimedomainreflectancemeasurements
(Diviner 2000; Sentek Sensor Technologies, Stepney, SA, Australia)
at )10 cm in 2005–2007. In 2008–2009, soil moisture was recorded
between 2 and 7 cm in one grassland plot per treatment block in 1-h
intervals by FD-sensors (Echo.EC-5⁄k; Decagon Devices, Pullman,
WA,USA).
Primary production
ABOVE-GROUND NET PRIMARY PRODUCTION
Above-ground biomass harvests (ANPP) of all standing plant mate-
rial (dead and alive) in all communities were conducted twice a year
(early in July and mid September) in 2005–2009, resembling local
Table 1. Experimental plant communities in the EVENT-I experiment (Jentsch, Kreyling & Beierkuhnlein 2007) representing grassland
vegetationincentralEurope:threefunctionaldiversitylevelsvariedbynumberofspecies,growthformandpresence⁄absenceoflegume
Abbreviation
Vegetation
type
Diversity
levelDescriptionSpecies
G2)
GrasslandATwo species, one functional group
(grass)
Arrhenatherum elatius, Holcus lanatus
G4)
GrasslandBFour species, two functional groups
(grass, forb)
Arrhenatherum elatius, Holcus lanatus,
Plantago lanceolata, Geranium pratense
G4+
GrasslandCFour species, three functional groups
(grass, forb, leguminous forb)
Arrhenatherum elatius, Holcus lanatus,
Plantago lanceolata, Lotus corniculatus
G, grassland; 2⁄4, number of species; ), without legume; +, with legume
Drought effect on multiple ecosystem services691
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agricultural routines. All biomass was taken out of the central
square metre of each grassland plot in order to circumvent edge
effects. The harvested biomass was sorted to species and dried to
constant weight at 75 ?C and weighed (Ohaus NavigatorTM, Ohaus
Corporation, Parsippany, NJ, USA; accuracy±0.01 g).
NITROGEN-FIXING LEGUMES
According to the above-mentioned routines, harvested biomass of
the legume species L. corniculatus was used to determine the perfor-
manceofnitrogen-fixingplants.
PLANT COVER
Species-specific above-ground cover was quantified using a pin-point
method, by recording the presence of plant organs in general and the
presence of each species separately at 100 vertically inserted steel nee-
dles. These values were then treated as the percentage of cover. The
measurement was repeated three times in each vegetation period
(May, July and September).
BELOW-GROUND BIOMASS
Root length was used as proxy for below-ground productivity.
Root length was acquired by the minirhizotron technique three
times a year. One clear plastic tube (5 cm diameter) was installed at
a 45? angle in each plot prior to planting. Tubes were installed to a
depth of 45 cm. Portions of the tubes exposed at the surface were
covered with adhesive aluminium foil and the ends were capped to
prevent entry of water, light and heat. Images of 4 cm2were col-
lected in the main rooting zone at 15 cm in each tube by a digital
camera mounted on an endoscope. Images were analysed for root
length using the line intersection method (Tennant 1975) within a
systematic grid (10 · 10, with a grid unit of 0.2 · 0.2 cm). Five rep-
licates per sampling date were analysed.
SHOOT-TO-ROOT RATIO
Shoot-to-root ratio was evaluated using the ratio between above-
groundcoverandbelow-groundrootlengthat5 cmsoildepth(Krey-
ling et al. 2008b). Both parameters were a priori standardized to the
samemeanandstandarddeviation.
Water regulation
LEAF WATER POTENTIAL
Predawn (wpd) and midday (wl) leaf water potential (wpd) were mea-
sured on one leaf of H. lanatus per plot using a portable pressure
chamber (PMS Instruments Co., Corvallis, OR, USA). During mea-
surements, the leaves were cut while enclosed in a plastic bag to
reduce further moisture loss during transfer and fixing into the cham-
ber. Moist tissue paper was introduced into the chamber to reduce
water loss during the measurements. Measurements were confined to
theperiodbetween04:00and05:00 hours
LEAF CARBON ISOTOPE SIGNAL
At the end of drought, a set of three fully matured leaves of A. elatius
from every plot was selected. In each plot, two sun-exposed leaves of
five individual plants were sampled and combined. The samples were
oven-dried for 48 h at 80 ?C. The dry leaves were ball-milled and
subsamples of 1 mg analysed for d13C with an elemental analyser
attached to an isotope-ratio mass spectrometer using ConFlo III
interface (Thermo Electron, Bremen, Germany). The carbon isotope
composition (d13C) of a sample was calculated as: d13C = [(Rsample⁄
Rstandard) ) 1] · 1000, expressed in units of per thousand (&).
13C:12C ratios were calculated against the P.D. Belemite Standard
(precision of 0.2 &). The results were compared with other measure-
ments to determine changes associated with shifts in13C. Every mea-
surementwas replicatedtwice andthe accuracy in d-values was better
than0.1&.
Carbon fixation
EFFICIENCY OF PHOTOSYNTHETIC LIGHT
CONVERSION
Chlorophyll a fluorescence in the grass species H. lanatus was
recorded using a pulse-amplitude-modulated photosynthesis yield
analyser (PAM 2000 and Mini-PAM; WALZ, Effeltrich, Germany)
with a leaf clip holder. The second or third fully expanded leaves
were measured on four different tillers of one individual. Four mea-
surements per plant were averaged for further analysis. We
obtained predawn fluorescence values at the end of the first
drought treatment in May⁄June and throughout the early recovery
period after the second drought. The maximum quantum efficiency
of photosystem II was calculated as Fv⁄Fm. Variable fluorescence
(Fv) and maximum fluorescence (Fm) were measured before dawn.
Variable fluorescence was calculated as Fm) F0, Fmbeing the max-
imum fluorescence of the dark-adapted leaf after applying a satu-
rating light pulse and F0being the steady-state fluorescence yield of
the dark-adapted leaf (Maxwell & Johnson 2000). To enable a
comparison between absolute fluorescence values, a fluorescence
standard material was measured before dawn and calculated as
Fv⁄Fm (Fv= Fm) F0) (Maxwell & Johnson 2000). Absolute F0
and Fmvalues were taken to separate the effects of photodamage,
becoming apparent with an increase of F0, from the effects of
photoprotection related to enhanced non-photochemical quench-
ing, becoming apparent with a decrease in Fm(Walter et al. 2011).
LEAF GAS EXCHANGE
Carbon dioxide assimilation (A) at the leaf was monitored in A. ela-
tius in all the grassland communities. (No data could be obtained
from H. lanatus in the particular year of data mining due to its leave
status.) A series of weekly measurements were carried out using a
portable gas-exchange system (LI-6400; LI-Cor, Lincoln, NE,
USA). A set of three grass tufts on each plot were identified and
marked for measurements. On any measurement day, 2–3 suitable
leaf blades selected from each of the tufts per plot were set parallel
in the cuvette, with their upper surfaces well exposed so that they
were fully illuminated during measurements. Every turn of measure-
ments lasted 1–2 min, when a steady state was attained and a set of
10 readings per measurement logged at 10-s intervals. The selected
leaves were marked and similar leaves were monitored either during
midday (12:00 to 14:00 hours) or throughout the day (from sunrise
to sunset), when diurnal course measurements were conducted. The
measured leaves were then excised at the end of the measurement
period and the leaf area (LA) of the section of leaf enclosed in the
cuvette determined using LA meter. (CI-202 CID; Camas, WA,
USA). Leaf area information was then used to standardize the leaf
gas-exchange data.
692A. Jentsch et al.
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SOIL RESPIRATION
In situ rates of soil respiration were measured using a portable CO2
infrared gas analyser (EGM-4; PP Systems, Amesbury, USA) linked
to a soil respiration chamber (SRC-1; PP Systems). At the beginning
of the vegetation period, permanent PVC collars (10 cm diameter,
5 cmheight,lightgreycolour)wereinstalledineveryplotwitha1-cm
edge above soil surface to realize a closed system when the soil respi-
ration chamber was placed on the collar during measurement. The
day before each measurement, all above-ground vegetation was
removed from the collar using scissors. During the timeframe of
8:00–12:00 hours, the soil respiration chamber was placed for 240 s
on the collar of every plot. An internal fan realized the even distribu-
tion of air and the infrared gas analyser monitored the build-up of
CO2within the system. The rates of soil respiration were determined
fromthisbyfittingaquadraticequationtothechangeinCO2concen-
trationwithtime.Forthisstudy,weanalysedthesoilrespirationrates
at second 240 of each high-diversity grassland plot including A. ela-
tius, H. lanatus, P. lanceolata and G. pratense on the last day of
droughtmanipulation.
MAXIMUM LEAF AND CANOPY UPTAKE RATES
Net ecosystem CO2exchange (NEE) was measured with chambers
on 40 · 40 cm frames established on each of the treatment plots.
Daily course of NEE was measured using manually operated,
closed gas-exchange canopy chambers. Light–response curves
depicting the net photosynthetic CO2uptake rate (A) of plants at
any measuring time were obtained from leaf-level gas-exchange
measurements by fitting an empirical rectangular hyperbola model
(Gilmanov et al. 2005): NEE = (a + Q⁄aQ ) b) ) c, where a is
the initial slope of the light–response curve and an approximation
of the canopy light utilization efficiency (mol CO2per mol PAR), b
is the maximum CO2 uptake capacity (lmol m)2s)1), Q is the
photosynthetically active radiation (PAR, in lmol m)2s)1), and c
is an approximation of the average daytime ecosystem respiration
(lmol m)2s)1). An approximation of maximum canopy uptake
capacity was extrapolated from leaf-level measurements. Canopy
NEE rate was estimated from leaf photosynthetic rate at saturating
light intensities (it was shown that A at PAR = 2000 lmol m)2s)1
correlates well with canopy NEE). Maximum gross primary pro-
ductivity (GPPmax) was calculated as: GPPmax= NEE2000) Reco,
where A2000is the maximum leaf photosynthetic rate at a saturating
level of light intensity and Recois the corrected respiration term (c)
obtained from the model.
Nutrient cycling
IN SITU DECOMPOSITION RATE OF CELLULOSE
Biological activityof soilfauna and micro-organisms was determined
indirectly from the decay of cellulose using mini-container tubes
(Kreyling et al. 2008a). In total, 864 mini-containers were filled with
0.2 g of cellulose (poor in phosphorus, Schleicher & Schu ¨ ll, Dassel,
Germany) each, closed with a 2-mm mesh, and put into container
tubes, consisting of 12 mini-containers each. Two tubes were buried
horizontally 1 cm below soil surface in each grassland plot. After
94 days, one tube per plot was harvested, whereas the others were
harvestedafter 186 days. After careful cleaningand drying, the decay
of cellulose was determined by subtracting final ashes-free dry mass
frominitialdrymass(105 ?C).
MYCORRHIZAL COLONIZATION
One complete plant individual of P.lanceolata was taken from each
plot on the last day of drought using a soil core sampler with 5 cm
diameter (Eijkelkamp, Giesbeek, the Netherlands). This particular
species was chosen, because pre-analysis revealed higher effects of
drought on mycorrhizaal colonization of P. lanceolata than on that
of other species tested. Roots were cut off and fixed in formalin-alco-
holic-acid (50% Ethanol, 40% H2O, 7.5% formalin, 2.5% acidic
acid), and stained with 5% blue ink vinegar solution after boiling in
10% KOH. Afterwards, mycorrhization ratios were determined by
scanning15 cm fine roots of each sample for arbuscules and vesicules
under a microscope (400·) using the ‘magnified intersection method’
(McGonigleet al.1990).
SOIL MICROBIAL NITROGEN POOL
Soil microbial nitrogen was extracted from fresh soil according to a
modified chloroform fumigation–extraction method (Brookes et al.
1985). After chloroform fumigation (24 h at room temperature), dis-
solved organic and microbial N was extracted with 50 mL 0.5 m
K2SO4and quantified(DIMA TOC-100; Dimatec,Essen,Germany).
Microbial biomass and relative abundance of microbial groups were
measured using phospholipid fatty acid analysis as described (Singh
et al.2006).
POTENTIAL SOIL ENZYME ACTIVITIES
For soil enzyme activity measurements, enzymes involved in carbon,
nitrogen and phosphorus cycling were selected (Mirzaei et al. 2008),
thus addressing important microbial soil functions (Waldrop & Fire-
stone 2006). The enzyme activities tested were acid phosphatase
cleaving organically bound phosphate, cellobiohydrolase, b-xylosi-
dase and b-glucosidase related to the degradation of plant cell wall
components and N-acetylglucosaminidase representing chitinases
that degrade chitin from fungal or arthropod origin. Soil samples for
determining soil enzyme activities were collected immediately after
finishing the drought manipulations (Kreyling et al. 2008a). Four
samples per plot (depth 0–5 cm) were combined, mixed and kept at
4 ?C until further processing within 4 weeks after sampling. Soil sus-
pensions (0.4 g fresh soil in 40 mL H2O) were prepared from each
sample. The assay is based on the enzymatic cleavage of the below-
detailedmethylumbelliferone(MU)coupledsubstratesandthesubse-
quent detection of MU released during incubation. In brief, 50 lL
per well of soil suspensions (three replicates each sample) were dis-
persed in microplates and 100 lL of substrate solutions were added
to start the reactions. After stopping the reaction with 100 lL of
2.5 m Tris buffer and centrifugation, MU concentrations were deter-
mined on a fluorescence spectrometer at excitation⁄emission wave-
lengths of 365⁄450 nm respectively. The following enzyme substrates
were used with the incubation times given: MUF-phosphate, 20 min;
MUF-xyloside, 1 h; MUF-cellobiohydrofurane, 1 h; MUF-N-ace-
tyl-b-glucosaminide, 40 min; MUF-b-glucoside, 1 h. Substrate con-
centrations in the incubation mix were 500 lM except for MUF-
cellobiohydrofurane with 400 lM. To account for quenching and to
calculate the amount of MUF released, calibration curves were
included with 50 lL of soil samples as in the incubation wells and
MUF-solutions to give a final amount of 0–500 pmol per well. Nega-
tive controls for autofluorescence of substrates were also included.
Enzyme activities are expressed as MUF-release per gram soil dry
weightperhour.
Drought effect on multiple ecosystem services693
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PLANT-AVAILABLE SOIL NITRATE AND AMMONIUM
Plant-available nitrogen was extracted from four homogenized,
sieved (<2 mm), mixed samples of the upper soil layer (0–10 cm) of
each plot sampled in July using a 1 m KCl solution after filtration
(Typ 15 A Blauband; Roth, Karlsruhe, Germany) (Kreyling, Bei-
erkuhnlein & Jentsch 2010). Nitrate and ammonium were quantified
usingflowinjectionanalysis(FIA-LAB;MLE,Dresden,Germany).
LEAF CARBON-TO-NITROGEN RATIO
Leaf carbon (C), leaf nitrogen (N) and C:N ratios were measured
from mixed samples of two sun-exposed leaves of five individual
plants per species and plot, sampled in July (Kreyling, Beierkuhnlein
& Jentsch 2010). The samples were oven-dried for 48 h at 75 ?C. The
dry leaves were ball-milled and subsamples of 1 mg analysed with an
elemental analyser in a massspectrometerusing ConFloIII interface.
Plant-available nitrogen was extracted from four homogenized,
sieved (2 mm) and filtered (Roth, Germany, Typ 15A Blauband)
mixed samples of the upper soil layer (0–10 cm) of each plot using a
1 mKClsolution.
LEAF PROTEIN CONTENT
Total protein content in lg per mg fresh weight was determined as a
proxy for nutritive value of the legume key species H. lanatus, which
was growing in all plots. One leaf sample per plot was taken on the
last day of drought treatment, frozen in liquid nitrogen and freeze-
dried to determine protein-bound amino acids. Amino acids of the
protein fraction were extracted. Amino acid concentrations were
measured with an ion exchange chromatograph (amino acid analyser
LC 3000; Biotronik SE & Co. KG, Berlin, Germany) and protein
content was calculated by pooling the content of each amino acid in
theproteinfraction.
LEAF NITROGEN ISOTOPE SIGNAL
Equally aged, south-facing leaves of A. elatius were collected and oven-
dried at 60 ?C for 48 h, and then fine-milled. Natural abundance of
d15N and total nitrogen concentration were analysed using an elemen-
tal analyser (EA 3000; EuroVector, Italy) coupled online to a ConFlo
III interface connected to an isotope-ratio mass spectrometer (MAT
253; Thermo Electron). The d15N values were calculated as: d15N
[&] =(Rsample⁄Rstandard) ) 1 · 1000,whereRrepresentstheratio
of15N:14Nisotopes.Asstandard,(nitrogenin)airwasused.
Community responses
INVASIBILITY
Invasibility of the experimental communities was recorded three
times per year: before and after the drought manipulations in early
summer,andinfall(Kreylinget al.2008c).Invadingplantindividuals
were collected from the inner square metre of each plot and subse-
quently separated by species. Removal took place only after the first
true leaves (after the cotyledons) emerged, but most specimens were
considerably older than this and clearly established in the stand. At
this point in development, we expected that number of individuals
give a measure of established invaders rather than chance germina-
tions. For each plot, the number of individuals was determined. The
planted target species of the experiment were removed from the sub-
sequent analysis. Tests confirmed that germination from the soil seed
bank was negligible after 1 year. Thus, invasibility was only based on
speciesinvadingfromthematrixvegetation.
PLANT COMPOSITIONAL CHANGE
The measurementsofabove-groundspecies-specific cover(seeabove)
were used to evaluate shifts in the species abundance distributions of
the artificial plant assemblages. Compositional change of each indi-
vidual plot was evaluated by comparing the species abundance distri-
bution at each time step to the initial species abundance distribution
(5 weeksafterplanting)bytheBray–Curtisindex.
COMPETITIVE EFFECT ⁄ FACILITATIVE EFFECT
The relative neighbour effect (RNE) calculates the effect of neigh-
bours relative to the plant with the greatest performance:
RNE = Pcontr) Pmix⁄x with x = Pcontr if Pcontr> Pmix and
x = Pmixif Pmix> Pcontr, where RNE = Relative neighbour effect
()1 £ RNE £ + 1), Pcontr= performance per plant for a plant
growing alone, Pmix= performance per plant for a plant growing in
mixture. Negative values indicate facilitation, and positive values
indicatecompetition(Markham&Chanway1996).
SENESCENCE
Tissue die-back was quantified by cover measurements of standing-
dead plant organs (Kreyling et al. 2008d). A pin-point method was
applied, recording the presence of plant organs in general and the
presenceforeachspeciesseparatelyat100verticallyinsertedsteelnee-
dles.Thesevaluesweretreatedaspercentagecover.Themeasurement
wasrepeatedfourtimesoverthecourseofthevegetationperiod.
VARIABILITY IN LENGTH OF FLOWERING
For each species, weekly observations of the flowering status of
four individuals per plot and species were carried out (Jentsch
et al. 2009). Individuals were counted as ‘flowering’ when the
anthers were visible in at least one flower. Flowering length was
calculated as the difference between the dates of the 25th and
75th percentiles of the flowering curve over time. Variability in
length of flowering was obtained as the standard deviation
between all species for each treatment (drought and control) sepa-
rately. Statistical significance of difference in variability was evalu-
ated by the Levene test.
VARIABILITY IN FLOWER PHENOLOGY
Flowerphenologywasobtainedfromthesamedataaslengthofflow-
ering (see above). As a surrogate, the mid-flowering date was calcu-
lated for each species and plot, i.e. the date of the 50th percentile of
the flowering curve over time. Variability in flower phenology was
expressed asthe standard deviation between all species for eachtreat-
ment (drought and control) separately. Statistical significance of dif-
ferenceinvariabilitywasevaluatedbytheLevenetest.
RESISTANCE TO HERBIVORY (PHENOL CONTENT)
For analysis of total soluble carbohydrates and total phenolics, three
mixed samples of at least two plants per plot were taken at the end of
the drought period, immediately frozenin liquid nitrogenand lyophi-
lized (n = 15). Thirty milligrams were extracted in 50% methanol.
Total soluble carbohydrates were analysed using the anthrone
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method with glucose as a standard. Extinction was measured at
620 nm. Total phenols were analysed using Folin Ciocalteu’s reagent
andcatechinasastandardandmeasuringextinctionat750 nm.
PRIMARY CONSUMER ABUNDANCE
Richness was sampled in June in one circular area (40 cm diameter)
in each grassland plot using a D-Vac suction sampler (ecotech
GmbH, Bonn, Germany). For each plot, the sampling bag was
removed and all sampled material was stored in ethanol. Arthropod
samples were quantified as the total number of individuals and iden-
tified at least to order level. However, some taxa were identified to
the family level (families within the Coleoptera, Hemiptera, most
Hymenoptera) and in one case to genus level (Psylliodes Chrysomeli-
dae). The use of higher taxonomic levels has been shown to produce
a good approximation of total species richness (Biaggini et al.
2007).
STATISTICAL ANALYSES
Linear Models combined with anova were applied to test for signifi-
cant differences between groups at single points of time, while tak-
ing the split-plot design into account. Homogeneous groups of
factor combinations (drought manipulation, vegetation type, diver-
sity level) were identified by Tukey’s HSD post hoc comparisons.
Level of significance was set to P < 0.05. Statistical significance of
difference in variability of length in flowering was evaluated by the
Levene test.
For time series, Linear Mixed-Effects Models were employed to
test for effects of drought manipulation and diversity and their
respective interactions while taking the split-plot design and the
repeated measures into account (time used as random factor). When
no significant interaction was found, the model was simplified by
using onlythe drought manipulationsasfixedeffects and timeasran-
dom effect. Significance of differences (P < 0.05) was evaluated by
Markov Chain Monte Carlo sampling of 1000 permutations. Linear
Mixed-EffectsModelswereconductedwiththefunction‘lmer’(Bates
&Sarkar2007).
Prior to statistical analysis, data was log- or square-root-trans-
formed,ifconditionsofnormalitywerenotmet,ortoimprovehomo-
geneity of variances. Both characteristics were tested by examining
the residuals versus fitted plots and the normal qq-plots of the linear
models.AllstatisticalanalyseswereperformedusingR.
Results
The effects of drought on all measured ecosystem properties
are summarized in Fig. 1 using response ratios to standardize
theeffectsizeoftheseveredroughttreatment.
WATER REGULATION
Severe drought significantly reduced soil moisture during the
manipulation periods in all years (Figs 1 and 2). A high vari-
ability both within years and between years is evident due to
inter-annual variability of precipitation (Table 2). Even
though absolute minima in soil moisture were similar for
droughtandcontrolinmostyears,soilmoistureofthedrought
plots remained considerably longer below the approximate
permanent wilting point (pF = 4.2) for the soil substrate. The
manipulation effect vanished within days for all years except
2009, where a lag phase of about 2 months until August
occurred. Further, drought decreased leaf water potential,
while increasing leaf carbon isotope signal in some species
(Fig. 2).
PRIMARY PRODUCTION
At the level of the grassland community or ecosystem, respec-
tively, local, annually recurrent 100-year and 1000-year
extreme drought events had no significant effect on various
processes that contribute to primary production in any of the
5 years from 2005 to 2009 (Figs 1 and 3). Surprisingly, neither
ANPP,norgreencoverofvegetationorbelow-groundproduc-
tion recorded as root length in the main rooting horizon were
affected by drought (Figs 1 and 3). Further, there was no sig-
nificant drought effect on biomass production of the nitrogen-
fixingplantL.corniculatus(Fig. 1).
CARBON FIXATION
Drought increased the maximum uptake capacity (GPPmax)
in grassland by 36% (Fig. 1). The soil respiration rate (Reco
calculated by the model was lower under drought than under
ambientconditions.Soilrespirationwasslightlybutnotsignif-
icantlydecreasedattheendofthedrought.
NUTRIENT CYCLING
Nutrient cycling in soil was clearly affected by drought
(Fig. 1). The annually recurrent drought events increased
ammonium content in soil, whereas soil microbial N was
decreased. Overall turnover rates were reduced, indicated by
decreased decomposition rate of cellulose and potential
enzymaticactivities.Therelativeabundanceofdifferentmicro-
bial groups except for arbuscular mycorrhiza remained
unchanged.
Remarkably, despite stability in biomass production,
drought decreased leaf protein content and the leaf nitrogen
isotope signature and increased C:N ratio and carbohydrate
contentinleaves,thusdecreasingfeedvalueofplanttissue.
COMMUNITY RESPONSES
Some ecosystem properties associated with community stabil-
ity were positively affected by drought. For example, annually
recurrent droughtevents reduced the invasibility of plantcom-
munities and, thus, increased community stability. Remark-
ably, recurrent severe drought did not cause any shift in the
absolute abundance of species, thus, it did not cause any com-
positional change within 5 years (Fig. 4), although it induced
complementary,species-specific
resulting in shifts in species-specific biomass contribution to
overall community production. For example, the competitive
effect of neighbouring plants on L. corniculatus was increased
by drought as well as the facilitative effect of neighbouring
plants on A. elatius. Still, a significant difference between
plant–plantinteractions
Drought effect on multiple ecosystem services695
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Page 8

drought and control was found in community composition
when comparing the species abundance distribution at each
timesteptotheinitialspeciesabundancedistributionbyasimi-
larity index. Further, drought increased leaf senescence and
caused shifts in flower phenology with regards to variability in
lengthoffloweringandmid-floweringdayofparticularspecies
in some years (for detailed results on shifts in phenology see
Jentsch et al. 2009). According to the decreased feed value of
plant tissue, primary consumer abundance was decreased by
drought.
Discussion
Our experimental approach has the ambitious goal to search
forasynthesisofthewiderangeofdroughtresponsescollected
in a single study. Our goal is to see whether general patterns
about different categories of responses can be drawn within a
single temperate grassland study system. In the following, we
first discuss particular drought responses, and then suggest
potential reasons why the responses may differ among the five
majorecosystemfunctions.
WATER REGULATION
Soil moisture dynamics and other soil-related parameters
integrate how biological systems respond to climate change
(Emmett et al. 2004). Soil water content was significantly
reduced by drought in our experiment, but there were strong
differences between years (Fig. 2). Natural precipitation dur-
ing the manipulation periods is of importance here, as the
years 2005–2008 all included some natural dry spells and
effect size of the drought manipulation therefore was bigger
in 2009 when no such natural event occurred. Still, it is not
completely clear how precipitation regimes translate into vari-
ation of the soil moisture regime (Weltzin et al. 2003; Potts
et al. 2006; Dermody et al. 2007). There is a growing number
Fig. 2. (a) Above-ground NetPrimaryProduction(ANPP),(b)cover
of green biomass, and (c) root length over five growing seasons
(mean±SE over all species compositions in grassland, n = 15 per
datapoint).
Fig. 1. Effects of recurrent severe drought
events on 32 response parameters organized
into ecosystem functions. All data were col-
lected at the EVENT-I experimental site
(Jentsch, Kreyling & Beierkuhnlein 2007) in
Central Europe during the years 2005–2009.
A parameter is marked as significant (filled
black bar) if data of at least 1 year showed
significant differences between drought and
ambient conditions (anova). Data shown
represent maximum effects from years with
highest drought effects, averaged over all
three experimental grassland communities.
For references of published details please
refertoMaterialsandmethodssection.
696 A. Jentsch et al.
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Page 9

of studies explicitly addressing time lags between precipitation
manipulation and the soil moisture regime (Dermody et al.
2007; Sherry et al. 2007), soil moisture storage (Potts et al.
2006) or soil hydrological properties as affected by interacting
climatic drivers (Bell, Sherry & Luo 2010). However, re-wet-
ting dynamics (Xiang et al. 2008), soil drying (St Clair et al.
2009) and potential carry-over effects between recurrent
heavy rainfall or drought events have not been analysed in
much detail. The transformation of precipitation pulses to
increased soil water contents available to plant roots and soil
biota for uptake can be complex: soil depth, soil texture, par-
ent material, organic matter content, vegetation type, pres-
ence of plant functional types, LA index and soil surface
characteristics all affect the partitioning between interception,
run-off, infiltration and subsequent hydraulic re-distribution,
soil evaporation, plant water uptake and seepage (Loik et al.
2004; Bell, Sherry & Luo 2010).
Amount, frequency and seasonal timing of soil water
available for plants, soil fauna and soil microbes will basically
determine much of the ecosystem response to more extreme
precipitation regimes. While in this experiment we only mani-
pulated the amount of soil water available to plants, seasonali-
ty issues appear to be an emerging research frontier. Yet, the
majorremainingchallengeistoassesshowfutureprecipitation
regimes with more extreme precipitation events affect – due to
alterations in soil moisture – biogeochemical cycles, biotic
interactionsandecosystemfunctions.
PRIMARY PRODUCTION
We found that drought has resulted in pronounced effects in
the functional performance such as carbon fixation and nutri-
ent cycling of plant communities and of individual species as
well as in fluxes and pools. However, all ecosystem properties
related to primary production remained stable throughout all
5 years of the experiment, despite recurrent severe drought
events and despite different pre-experimental soil water status
between years. In temperate grasslands, experimental drought
events tend to reduce biomass productivity (Sternberg et al.
1999; Grime et al. 2000; Kahmen, Perner & Buchmann 2005).
Fay et al. (2003), however, showed that the magnitude of
reduction in ANPP is the same if rainfall quantity is reduced
by30%orifinter-rainfall-intervalsareincreasedby50%with-
out a change in the annual amount of precipitation. Presum-
ably, complementary responses
contributedtobufferingprimaryproductionatthecommunity
level without changing community composition in our experi-
ment (Wang, Yu & Wang 2007; Kreyling et al. 2008a,b,c,d).
For example, the competitive effect of neighbouring plants on
L. corniculatus was increased by drought as well as the facilita-
tiveeffectofneighbouringplantsonA.elatius.Thisisinaccor-
dance with a long-term study of 207 grassland plots, which
demonstrated that biodiversity stabilizes community and eco-
inspeciesinteractions
200520062007
Year
20082009
0
100
200
300
400
ANPP (g m–2 a–1)
0
6
20
40
60
80
100
Green cover (%)
Ambient
Drought
Root length (cm 4 cm–2)
NS
NS
0
1
2
3
4
5
NS
(a)
(b)
(c)
Fig. 3. Soil moisture in the EVENT experiment at )2 to )7 cm dur-
ing manipulation (light grey boxes) and recovery after extreme
drought for control (black line) and drought (grey line). MJJA =
May, June, July, August. Plant-available water is shown between the
dashed lines: permanent wilting point (pF = 4.2) and field capacity
(pF = 1.8).SeeMaterialsandmethodsfortechnicaldetails.
Table 2. Temperature and precipitation sums (added daily amount) for each year until the start of the drought manipulation and the respective
alterationfromthelong-termmean(1971–2000,data:GermanWeatherServicestationBayreuth)
Year
Temperature sum
(1 January to start
of manipulation)
Relative change of
temperature sum compared
to long-term mean (%)
Precipitation sum
(1 January to start
of manipulation)
Relative change of
precipitation sum compared to
long-term mean (%)
2005
2006
2007
2008
2009
824.7
394.7
978.7
757.6
574.9
)3
)38
+77
+40
+4
259.7
208.3
258.6
282.2
246.4
)9
+10
+9
+19
+4
Drought effect on multiple ecosystem services697
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Page 10

system processes, but not population processes (Tilman 1996).
Here, primary production was one of the key parameters stud-
ied. The persistence of this general ecosystem function was
strongerthanexpected.Concerningbelow-groundproduction,
several studies (Trillo & Fernandez 2005; Newman, Arthur &
Muller 2006) report increased root biomass in response to
chronically decreased water supply, while a complete water
withdrawal over defined periods of time result in stable or
decreasedbelow-groundbiomass(Kreylinget al.2008a).
CARBON FIXATION
Results from ecosystem CO2measurements showed a 36%
increase in GPP during drought in the grassland, but a
reduction in the assimilatory capacity of the leaves (Fig. 1).
During water stress, there was an increase in tillering, leading
to increased photosynthetic area of particular species, yet not
an increasein absolute cover or green cover of the community.
Thus, even though CO2assimilation was reduced at leaf level
asaresultofwaterstress,theoveralleffectofthelargeLApre-
sented by the tillers lead to an increase in the contribution of
particular species to ecosystem productivity, compensating for
reduced photosynthetic rates at leaf level. Declining stomatal
conductance asa result ofstomatalclosure wasresponsible for
the observed low leaf-level CO2 assimilation rates during
stress. Zavalloni et al. (2009) reported a reduction in leaf
assimilation, but increased biomass production in grassland
subjected to extreme drought. In contrast, Stitt & Schulze
(1994)pointoutthatchangesinphotosynthesisnotnecessarily
leadtochangesingrowthorbiomass.
NUTRIENT CYCLING
Nutrient cycling was clearly affected by drought. The annually
recurrent drought events increased leaf C:N and plant-avail-
able soil ammonium, whereas they decreased the decomposi-
tion rate and mycorrhization rate. Obviously, water stress has
animpactontheactivityandabundanceofammoniumoxidiz-
ing prokaryotes, resulting in increased ammonium in the soil,
which, however, can hardly be taken up by plants (Gleeson
et al. 2010). The microbial community seems generally irre-
sponsive to drought treatment where the onlysignificant effect
was an increase in microbial biomass, however the relative
abundance of different microbial groups remained unchanged
except for arbuscular mycorrhizal fungi. This is in accordance
with other findings showing that drought changes community
structure in arbuscular mycorrhizal fungi including their car-
bohydrate and nitrogen storage bodies, so that they take up
less nitrogen (Shi et al. 2002). Our results suggested that com-
position of microbial groups in soils is generally resistant to
drought treatment. This observation is in agreement with pre-
vious reports (Williams 2007, Williams & Xia 2009; Andresen
et al. 2010).Both leafC:N ratio(s?) and microbial data suggest
that there was an increase in C:N ratio which may explain
lowersoilrespiration under droughtconditions. Thismay sug-
gest lower activity of microbial communities which is reflected
by the decreased rate of decomposition. In this study, leaf and
microbial C:N ratio and litter decomposition responded to
drought treatment, but biological and geochemical responses
of climate treatment are complex (Andresen et al. 2010), and
future work should include multi-factorial experiments taking
into accountenvironmentalfactorssuchassoiltype,soilwater
andlanduse(Singhet al.2010).
Additionally,ourresultsshowthatclimateextremes further
affect the abundance of herbivores associated with the plant
community. For instance, we suggest that the reduction of
abundances of athropods by drought events may translate to
changes in the top–down control of vegetation by herbivores
and slowed decomposition dynamics due to a lower activity of
decomposers.
–20
–10
0
10
20
–20
–10
0
10
–20
–10
0
10
0
10
A. elatius
H. lanatus
G. pratense
–20
–10
–20
–10
0
10
L. corniculatus
2005200620072008 2009
Abundance shifts (%)
P. lanceolata
Fig. 4. Abundance shift (%) of the grassland species Arrhenatherum
elatius, Holcus lanatus, Plantago lanceolata, Geranium pratense and
Lotus corniculatus for the years 2005–2009 (mean±SE of the abso-
lute deviation of species cover under drought from the mean of con-
trol, n = 15 for A. elatius & H. lanatus, n = 10 for P. lanceolata,
n = 5forG.pratense&L.corniculatusperdatapoint).Nosignificant
drought effects on species cover (anova for each year and Linear
Mixed-EffectModelforlong-termtrends:P < 0.05).
698A. Jentsch et al.
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COMMUNITY RESPONSES
Relative importance of each species in a community context
was affected by the drought treatments as measured by the
similarity of species abundances to the starting conditions for
eachplot.Theeffectsize,however,wascomparablysmall,pre-
sumably because speciescompositionswere held constant over
the course of the experiment by weeding out non-target spe-
cies. Furthermore, competitive balance, based on species-spe-
cific biomass production, was altered and variability in
flowering was affected. Particularly, averaged over all species,
drought advanced the mid-flowering day within the season
and expanded the length of the flowering period. On the other
hand, no significant shifts in relative abundance of single spe-
cies were observed (Fig. 4). Generally, however, shifts in spe-
cies composition might require substantial lag phases (Grime
et al. 2000; Buckland et al. 2001), especially as non-target spe-
cieswerenotallowedtoimmigrateintoourplots.
LIMITATIONS OF THE EVENT EXPERIMENT
All the results discussed above stem from one site, i.e. one par-
ticular climate, one soil type, one form of experimental manip-
ulations and a limited set of species. Certainly, an array of
factors such as the investigated ecosystem type, time scales,
level of nutrient availability, water holding capacity of soils,
level of biodiversity or particular design and execution of the
experimental treatments will modify the effects of drought on
ecosystem properties. Therefore, similar approaches from
other sites and climatic conditions are clearly needed in order
to test the generality of the observed findings. In particular,
experiments with strongly controlled species compositions
need to be compared to natural or semi-natural communities.
Another importantgap of knowledge thatcannot be answered
by our experiment is the importance of interactions between
the climatic drivers, as there is clear evidence that effects
of drivers such as warming, drought, N-deposition and
CO2-increase are not additive (Shaw et al. 2002; Andresen
et al.2010).
Generally, manipulation artefacts or hidden treatments are
a concern for global change field experiments. Rain-out shel-
ters are the usual device to simulate drought even though they
are known to cause artefacts in the microclimate (Fay et al.
2000). Our artefact control treatment showed that the slight
temperature increase and the alterations in irradiance or wind
speed due to our shelters caused no effect on the measured
response parameters, presumably because the shelters were
active only during the short manipulation periods. Other arte-
facts, however, might be more important, yet less investigated,
such as preferential site selection by animals due to the close
proximity of different climatic conditions between the treat-
ments blocks (Moise & Henry 2010). Such spatial patterns at
small distances clearly differ strongly from drought effects at
landscapelevels.
Wesetthemagnitudeofthedroughtmanipulationbasedon
statistical recurrence of dry spells in the local climate data
series (1961–2000). Recurrence of extreme events itself,
however, is subject to climate change, leading to an amplifica-
tion of precipitation extremes with ongoing climate change
(Allan & Soden 2008). For the ambient conditions in our
experiment, though, the statistical recurrence of the different
manipulationyearsfellwellwithinthoseofthelong-termaver-
ages for air temperature, precipitation sum or length of rain-
freeperiods(datanotshown).Thismaybeamongthereasons,
whywedidnotobservelargeeffectsonbiomassproduction.
Conclusion
Our experimental data demonstrate that climate extremes
initiate ecosystem-regulating functions such as water and
nutrient cycling, gas exchange and compositional dynamics
while maintaining primary production. They indicate an
importantcontributionofecologicalcomplexitytothemainte-
nance of productivity in the face of increased temporal climate
variability and extraordinary weather events. However, single
species reactions can not be translated directly to the commu-
nity and ecosystem level. A potential reason for different
drought impacts on various ecosystem properties may lie in
the temporal hierarchy of fast versus slow response patterns.
In our temperate grassland, we observed the following
response dynamics within half a decade of recurrent drought
events: very fast alteration of soil moisture status, subsequent
fast change in nutrient cycling and gas exchange, slow species-
specific response in primary production, inertia in community
productivity.
Such data on multiple response parameters within climate
change experiments foster the understanding of mechanisms
of resilience, of synergisms or decoupling in biogeochemical
processes, and of fundamental response dynamics to drought
attheecosystemlevel.
As it was the case with the open questions on the conse-
quences of the crisis of biodiversity, we see this complexity in
studying impacts of climate extremes as a new chance for a
boost in ecological theory. Additionally, comprehensive stud-
ies on the complex responses will help developing coping strat-
egiesfortheadaptedmanagementoftheseecosystems.
Future challenges consist of analysing responses for multi-
ple ecosystem functions and at multiple levels of organization
with the goal of assessing how they interact to influence emer-
gent ecosystem properties, such as ecosystem function and
stability. The observed stability in primary production in the
face of recurrent severe drought does not mean that
the responses at the ecosystem level are null. On the contrary,
the observed changes in ecosystem-regulating functions in
terms of gas exchange, nutrient cycling, water regulation and
community stability suggest a prominent role of climate
extremes in ecosystem response to climate change. However,
modelling the behaviour of ecosystems during and after
climate extremes at larger spatial scales and over longer peri-
ods of time requires more in-depth knowledge on possible
response mechanisms at the level of plant communities.
Potential epigenetic, physiological or trophic responses need
to be rigorously further explored experimentally. Laboratory
studies on molecular mechanisms have to be related to stud-
Drought effect on multiple ecosystem services699
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Page 12

ies with the same species in the field. Field studies must inte-
grate various levels of functional diversity (Beierkuhnlein
et al. in press). Phenotypical diversity of populations has to
be considered. Life cycles of plant species and cohorts can be
of crucial importance. Gradients in soil types have to be inte-
grated. Then, we can reach a better understanding of the
mechanisms that are initiated in plant communities by
extreme events.
Future work is needed to elucidate the role of biodiversity
and of biotic interactions in modulating ecosystem response to
extreme weather events. Further, we need more data on
impacts of climate extremes on multiple ecosystem properties
from various ecosystems and biomes, in order to foster the
search for generality across different categories of response.
Here, a major challenge is to assess the speed of response
across various parameters, including long-term feedbacks, i.e.
caused by a nitrogen-dependent feedback on productivity
(Haddad,Tilman&Knops2002).
Generally,scientistsarechallengedbyrelatingtheecosystem
properties measured (here: net ecosystem exchange, biomass
above- and below-ground, carbon fixation by photosynthesis,
nutrient ratios) to ecosystem functions and services, such as
productivity, carbon fixation, nutrient cycling, decomposition
and water regulation. Measuring ecosystem services is a fast-
developing research area with many debates on how to assess
theservicesadequately.
Acknowledgements
The contribution of various working groups to the measurements in the
EVENT experiment gives us a unique opportunity to bring bits and pieces
together. We thank J. Bo ¨ ttcher-Treschkow, M. Ewald, N. Herold, Z. Hussein
Y. Li, M. Mederer, C. Mu ¨ ller, L. Mueller, S. Neugebauer, D. Pfab, K. Simmn-
acher, H. Skiba, S. Walther, M. Wenigmann, D. Wulf and many student help-
ers for assistance with data mining in the field and fruitful discussions.
Research funding was provided by the German Science Foundation (DFG)
andbyFORKAST.
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Received15August2010;accepted1February2011
HandlingEditor:MelindaSmith
Supporting Information
Additional supporting information may be found in the online ver-
sionofthisarticle:
Table S1. Search items for searching the ISI Web of Science?Data
base for publications on weather events and climate extremes. Aster-
isksareplaceholderswithinthesearchstring.
Drought effect on multiple ecosystem services701
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Table S2. Links for searching the ISI Web of Science?Data base for
publicationsonweathereventsandclimateextremes.
TableS3. Samplingyears ofallresponseparameterspresented in Fig-
ure1.Givenaredatafromyearswithmaximumdroughteffect.
Figure S1. Research on ecological effects of climate extremes and
weathereventsbased onpublicationsfound inthe ISI WebofScience
(for search details see Table 2). (a) Temporal development of the
number ofpublications onclimate extremes (n = 380)in the last two
decade (shown is only the last decade); total yield 1134 peer-reviewed
papers. (b) Studied extreme weather events (n = 464 including dou-
ble or triple assignments) of the relevant peer-reviewed papers
(n = 380) yielded by the literature study. Twenty four publications
did not specify the event. (c) Research activity in the three main
biomes by proportion of publications based on 380 peer-reviewed
papers particularly studying effects of climate extremes on ecosystem
functions. Grassland includes deserts, peat and wetlands. Shrubland
includes tundra. Any one paper may have been assigned to multiple
subject areas.(d) Studied effects ofextreme weather eventsonecosys-
tem properties arranged by ecosystem services and functions based
on 380 peer-reviewed papers particularly studying effects of climate
extremesonecosystemfunctions.
Asaservicetoourauthorsandreaders,thisjournalprovidessupport-
ing 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
thanmissingfiles)shouldbeaddressedtotheauthors.
702 A. Jentsch et al.
? 2011 The Authors. Journal of Ecology ? 2011 British Ecological Society, Journal of Ecology, 99, 689–702