www.elsevier.com/locate/agrformet

Agricultural and Forest Meteorology 143 (2007) 123–145

Evidence for soil water control on carbon and water dynamics

in European forests during the extremely dry year: 2003

A. Granier a,*, M. Reichstein b,c, N. Breda a, I.A. Janssens d, E. Falge e, P. Ciais f,T. Grunwald g, M. Aubinet h, P. Berbigier i, C. Bernhofer g, N. Buchmann j,

O. Facini k, G. Grassi l, B. Heinesch h, H. Ilvesniemi m, P. Keronen n,A. Knohl c,o, B. Kostner g, F. Lagergren p, A. Lindroth p, B. Longdoz a,

D. Loustau i, J. Mateus q, L. Montagnani r,s, C. Nys t, E. Moors u, D. Papale b,M. Peiffer a, K. Pilegaard v, G. Pita q, J. Pumpanen w, S. Rambal x,

C. Rebmann c, A. Rodrigues y, G. Seufert l, J. Tenhunen e, T. Vesala n, Q. Wang e

a UMR INRA-UHP Forest Ecology and Ecophysiology, 54820 Champenoux, Franceb Department of Forest Environment Science and Resource, DISAFRI, University of Tuscia, Via Camillo de Lellis, 01100 Viterbo, Italy

c Max Planck Institute for Biogeochemistry, Postfach 10 01 64, 07701 Jena, Germanyd Department of Biology, University of Antwerp, Universiteitsplein 1, 2610 Wilrijk, Belgium

e Pflanzenokologie, Universitat Bayreuth, 95440 Bayreuth, Germanyf LSCE, CE Orme des Merisiers, Bat 701, 91191 Gif sur Yvette Cedex, France

g Department of Meteorology, Institute of Hydrology and Meteorology, Technische Universitat Dresden, 010062 Dresden, Germanyh Faculte des Sciences Agronomiques de Gembloux, Unite de Physique, B-5030 Gembloux, Belgium

i UR EPHYSE-INRA Bordeaux, 69 route d’Arcachon, 33612 Gazinet, Francej Institute of Plant Sciences, Swiss Federal Institute of Technology (ETH), Zurich, Switzerland

k Istituto di Biometeorologia CNR Via Gobetti, 101, 40129 Bologna, Italyl Environment Institute, JRC-Ispra, 21020 Ispra, Italy

m Vantaa Research Centre, Finnish Forest Research Institute, P.O. Box 18, 01301, Finlandn Department of Physical Sciences, P.O. Box 64, University of Helsinki, 00014, Finland

o Department of Environmental Science, Policy and Management, Ecosystem Science Division, University of California, Berkeley, USAp Lund University, Department of Physical Geography and Ecosystem Analysis,

Soelvegatan 12, Solvegatan 12, S-223 62 Lund, Swedenq Instituto Superior Tecnico, Departamento de Engenharia Mecanica, Av. Rovisco Pais, 1049-001 Lisboa, Portugal

r Agenzia Provinciale per l’Ambiente, Via Amba-Alagi 5, 39100 Bolzano, Italys Ripartizione Foreste di Bolzano, Via Brennero 6, 39100 Bolzano, Italy

t INRA Biogeochemistry of Forest Ecosystems, 54280 Champenoux, Franceu Alterra, Postbus 47, 6700 AA Wageningen, The Netherlands

v Plant Research Department, Risø National Laboratory, P.O. Box 49, 4000 Roskilde, Denmarkw Department of Forest Ecology, P.O. Box 27, University of Helsinki, 00014, Finland

x CEFE/CNRS 1919 Route Mende BP 5051 Montpellier, 34033, Francey Estacao Florestal Nacional, Departamento de Silvicultura e Produtos Florestais,

Av. da Republica, Quinta do Marques, 2780-149 Oeiras, Portugal

Received 17 May 2006; received in revised form 12 December 2006; accepted 15 December 2006

* Corresponding author. Tel.: +33 3 83 39 40 38; fax: +33 3 83 39 40 69.

E-mail address: agranier@nancy.inra.fr (A. Granier).

0168-1923/$ – see front matter # 2007 Elsevier B.V. All rights reserved.

doi:10.1016/j.agrformet.2006.12.004

A. Granier et al. / Agricultural and Forest Meteorology 143 (2007) 123–145124

Abstract

The drought of 2003 was exceptionally severe in many regions of Europe, both in duration and in intensity. In some areas,

especially in Germany and France, it was the strongest drought for the last 50 years, lasting for more than 6 months.

We used continuous carbon and water flux measurements at 12 European monitoring sites covering various forest ecosystem

types and a large climatic range in order to characterise the consequences of this drought on ecosystems functioning.

As soil water content in the root zone was only monitored in a few sites, a daily water balance model was implemented at each

stand to estimate the water balance terms: trees and understorey transpiration, rainfall interception, throughfall, drainage in the

different soil layers and soil water content. This model calculated the onset date, duration and intensity of the soil water shortage

(called water stress) using measured climate and site properties: leaf area index and phenology that both determine tree transpiration

and rainfall interception, soil characteristics and root distribution, both influencing water absorption and drainage. At sites where

soil water content was measured, we observed a good agreement between measured and modelled soil water content.

Our analysis showed a wide spatial distribution of drought stress over Europe, with a maximum intensity within a large band

extending from Portugal to NE Germany.

Vapour fluxes in all the investigated sites were reduced by drought, due to stomatal closure, when the relative extractable water in

soil (REW) dropped below ca. 0.4. Rainfall events during the drought, however, typically induced rapid restoration of vapour fluxes.

Similar to the water vapour fluxes, the net ecosystem production decreased with increasing water stress at all the sites. Both gross

primary production (GPP) and total ecosystem respiration (TER) also decreased when REW dropped below 0.4 and 0.2, for GPP

and TER, respectively.

A higher sensitivity to drought was found in the beech, and surprisingly, in the broadleaved Mediterranean forests; the coniferous

stands (spruce and pine) appeared to be less drought-sensitive.

The effect of drought on tree growth was also large at the three sites where the annual tree growth was measured. Especially in

beech, this growth reduction was more pronounced in the year following the drought (2004). Such lag effects on tree growth should

be considered an important feature in forest ecosystems, which may enhance vulnerability to more frequent climate extremes.

# 2007 Elsevier B.V. All rights reserved.

Keywords: Drought; Europe; Carbon and water fluxes; Forest; Modelling; Water balance

1. Introduction

Water and carbon fluxes and, as a consequence,

productivity of terrestrial ecosystems are strongly

influenced by drought. This is true among sites, when

considering the relationship between average climate

and forest productivity (Lieth, 1973; Gholz et al., 1990;

Scurlock and Olson, 2002; Huxman et al., 2004), and

also for the interannual variations within one site

(grasslands: Meyers, 2001, forests: Granier et al.,

2000b). Repeated droughts induce a reduction in leaf

area index (Battaglia et al., 1998; Le Dantec et al., 2000)

that in turn decreases GPP (Law et al., 2002; Hoff and

Rambal, 2003). Due to recurrent severe droughts, the

Mediterranean and dry-tropical vegetation show adap-

tations: species composition, increased root to shoot

ratio and leaf thickness, drought-adapted physiology as

enhanced osmotical adjustments, decreased vulnerabil-

ity to cavitation (see a recent review on drought effects

and adaptations by Breda et al., 2006). However, even

drought-adapted ecosystems are influenced by drought

(coniferous: Goldstein et al., 2000, evergreen: Rambal

et al., 2003; Reichstein et al., 2002b). In tropical

rainforests, the dry season may have a strong influence

on carbon fluxes (Vourlitis et al., 2001; Rascher et al.,

2004). In boreal forests, Cienciala et al. (1998) pointed

out a strong reduction in transpiration during dry years,

while Krishnan et al. (2006) reported in a boreal aspen

stand submitted to a 3-year long drought a decline in

both growth and leaf area index that continued even

after 2 years following the drought.

Due to global change, more frequent and severe

droughts are expected in some regions of the globe,

mainly in the Northern hemisphere (Lawlor, 1998; Saxe

et al., 2001; Meehl and Tebaldi, 2004; Schar et al., 2004

and International Panel on Climate Change, IPCC,

2001). The effects of such extreme events are, however,

poorly documented because of their limited occurrence

under past and actual climate (Innes, 1998).

At the stand level, studies on the effect of drought on

tree transpiration estimated from sap flow measure-

ments are quite numerous (e.g., Breda et al., 1993;

Irvine et al., 1998). Granier et al. (2000c) derived

responses of canopy conductance to drought for several

temperate tree species. A strong reduction in tree and

both canopy conductance for water vapour and stand-

scale transpiration when soil water content decreases is

generally found in most of the tree species.

Under natural conditions, the impact of drought on

carbon fluxes has been less frequently investigated than

A. Granier et al. / Agricultural and Forest Meteorology 143 (2007) 123–145 125

that on water flux regulation. A network of eddy-

covariance flux towers revealed a pronounced relation-

ship between NEE and annual rainfall (Grunzweig

et al., 2003), and a decline in GPP with annual water

balance calculated from integrated ET minus precipita-

tion (Law et al., 2002).

The drought and heat wave that occurred in summer

2003 in Europe was exceptional, both in duration and in

its large distribution across Europe (Stott et al., 2004;

Ciais et al., 2005) and provoked a dramatic reduction of

the crop yield in France, Italy and South Germany

(COPA-COGECA, 2003).

The 2003 drought thus provided a good opportunity

to examine the response of a wide range of terrestrial

ecosystems to extreme climatic conditions, and thus to

gain insights how the future climate, with potentially

more intense and more frequent extreme climatic

conditions, will alter ecosystem functioning (Schar

et al., 2004). Especially, the Central European tree

species like beech, which are typically not exposed to

extreme summer drought, were expected exhibit a

strong reaction during 2003.

We analysed water and carbon fluxes data from 12

forest sites, covering oceanic to continental, and

Mediterranean to boreal climates. The reader should

bear in mind that, although we focused on drought, this

drought was accompanied by a heat wave; at some

places in Western Europe, air temperature was higher

than 40 8C for several days during August, the monthly

average was 5–6 8C higher than normal (Rebetez et al.,

2006) in France and in Germany.

The objectives of this work were: (i) to quantify the

drought intensity and duration during 2003 in the 12

forest sites, plus 4 additional ones where above-canopy

fluxes were not measured, (ii) to relate the measured

carbon fluxes to the modelled soil water content and

compare the response of the different species, (iii) to

estimate the reduction in the annual 2003 net ecosystem

exchange (NEE), the gross primary production (GPP)

and the total ecosystem respiration (TER) as compared

to a typical year.

2. Material and methods

Most of the studied sites belong to the Carboeurope

network aiming at measuring energy, carbon and water

fluxes above different European vegetation types (http://

www.bgc-jena.mpg.de/public/carboeur/). Climate and

site data from four additional sites were also used for

drought quantification.

The main characteristics of the sites and references

providing each site description are given in Table 1.

Those sites belong to the most important European

forest ecosystem types: temperate deciduous (Hesse,

Sorø, Hainich, Vielsalm, Fougeres, Nonantola), tempe-

rate coniferous (Tharandt, Loobos, Brasschaat), boreal

coniferous (Norunda, Hyytiala), mountain coniferous

(Renon), Atlantic (Le Bray) and Mediterranean (San

Rossore, Espirra, Puechabon). They are even-aged

stands, except Vielsalm (beech and Douglas-fir),

Nonantola (mix of ash, oak, maple, willow plus other

minor species), and Renon (spruce and pine). About

half of the sites are plantations; most of them are mature

or old stands.

2.1. Flux measurements and data processing

CO2 fluxes were estimated using the eddy covariance

technique (see in Table 2 the main set up and sensor

characteristics) and following the EUROFLUX meth-

odology (Aubinet et al., 2000). Air temperature, CO2

and water vapour concentration as well as the three

components of the wind velocity were sampled at a

20 Hz frequency. Covariance of the vertical velocity

component and of the CO2 concentration was computed

every half hour. Classical averaging, rotation and

correction procedures (Aubinet et al., 2000) and quality

tests (Foken and Wichura, 1996) were applied; we

assumed that NEP � NEE.

The same procedure of gap filling was applied in all

sites. Moreover, the same method for calculating

ecosystem respiration (TER) and gross photosynthesis

(GPP) from net CO2 fluxes (NEE) was used (Reichstein

et al., 2005). The partitioning of the observed NEE

into gross primary production (GPP) and ecosystem

respiration (TER) was achieved through an algorithm

that first establishes a short-term temperature depen-

dence of ecosystem respiration on air temperature from

turbulent nighttime data and then uses this relationship

for extrapolating respiration from nighttime to daytime.

Day-to-day varying base rates of respiration were

derived from the u*-filtered nighttime fluxes, where the

u* threshold was derived specifically for each site-year

according to Reichstein et al. (2005). By using short

periods for deriving the temperature dependence, the

algorithm avoids the confounding effect of covariance

between general biological activity and temperature

occurring at seasonal time-scales (cf. detailed discus-

sion in paper cited above). Uncertainties of the changes

of GPP and TER between the years were estimated as a

combination of the uncertainties that arise from the

eddy covariance measurements themselves, u*-filtering,

the gap filling and the flux partitioning according to

the following reasoning. We assume that potential

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Table 1

Main characteristics of the investigated sites: location, elevation, tree species, tree age, mean annual temperature (Ta), annual rainfall (R): mean, 2003 rainfall and 2003 difference to the mean

Site Country Species Latitude (8N) Longitude (8E) Age (year) Elevation (m) Ta (8C) R (mm) Citation

Mean 2003 Difference

Fougeresa,b,c,d France European beech 48.38 �1.18 32 190 11.2 1083 781 �302 Lebret et al. (2001)

Hainichd Germany European beech 51.07 10.45 0–253 445 7.0 800 544 �256 Knohl et al. (2003)

Hessed France European beech 48.67 7.07 36 300 9.2 885 661 �224 Granier et al. (2000b)

Sorød Denmark European beech 55.49 11.65 83 40 8.1 510 532 22 Pilegaard et al. (2001)

Vielsalm Belgium Beech/Douglas-fir 50.30 6.00 63–93 450 7.5 1000 846 �154 Aubinet et al. (2001)

Nonantolac,e Italy Mixed deciduous 44.68 11.03 11 25 14.5 754 535 �219 Grassi et al. (2005)

Espirrae Portugal Eucalyptus 38.63 �8.60 12 96 15.9 709 628 �81 Rodrigues et al. (2005)

Puechabonc France Mediterrannean oaks 43.74 3.60 61 270 13.4 883 1199 316 Rambal et al. (2003)

Le Bray France Maritime pine 44.70 �0.77 33 60 13.5 950 847 �103 Berbigier et al. (2001)

San Rossore Italy Maritime pine 43.73 10.29 43 4 14.2 920 743 �177 Tirone et al. (2003)

Brasschaatb,c Belgium Scots pine 51.32 4.52 74 16 10.0 750 668 �82 Carrara et al. (2003)

Loobosc,e Netherlands Scots pine 52.17 5.74 96 52 9.8 786 710 �76 Dolman et al. (2002)

Hyytialad Finland Scots pine 61.85 24.28 42 170 3.5 640 438 �202 Rannik et al. (2002)

Tharandtd Germany Spruce 50.96 13.57 111 380 7.5 820 495 �325 Grunwald (2003)

Norunda Sweden Spruce/pine 60.08 17.47 100 45 5.5 545 521 �24 Lindroth et al. (1998)

Renon Italy Mixed coniferous 46.58 11.43 0 to180 1730 3.8 790 683 �107 Marcolla et al. (2005)

The mean rainfall is calculated for the last 15–50 years according to sites.a Not included in Carboeurope, no flux data.b No flux data in 2003.c Soil temperature not available.d Available soil water measurements.e More than 20% of missing eddy-flux data in 2003.

A. Granier et al. / Agricultural and Forest Meteorology 143 (2007) 123–145 127

Table 2

Main characteristics of the eddy-covariance systems and set-up: measurement height, sensors and u* threshold (see text)

Site EC measurement height (m) EC sensors u* threshold

Hainich 44 Li6262 (Licor) + Solent R2 (Gill) 0.4

Hesse 23.5 Li6262 (Licor) + Solent R2 (Gill) 0.2

Sorø 43 Li6262 (Licor) + Solent R2 (Gill) 0.25

Vielsalm 40 Li6262 (Licor) + Solent R2 (Gill) 0.5

Nonantola 13 Li6262 (Licor) + Solent R2 (Gill)

Espirra 33 Li7500 (Licor) + Solent R2 (Gill) 0.2

Puechabon 12.2 Li6262 (Licor) + Solent R3A (Gill) 0.35

Le Bray 41 Li7500 (Licor) + Solent R2 (Gill) 0.4

San Rossore 24 Li6262 (Licor) + Solent R2 (Gill)

Brasschaat 41 Li6262 (Licor) + Solent R2 (Gill) 0.2

Loobos 27 Li6262 (Licor) and after 2001 DOY 158

Li7500 (Licor) + Windmaster Pro (Gill)

0

Hyytiala 23.3 Li6262 (Licor) + Solent R2 (Gill) 0.2

Tharandt 42 Li6262 (Licor) + Solent R2 (Gill) 0.3

Norunda 35, 70 and 100 Li6262 (Licor) + Solent R2 (Gill) 0.4

Renon 32 Li7500 (Licor) + Solent R3HS (Gill) 0.3

systematic errors that affect the absolute magnitude

of the fluxes, as well as uncertainties by the u*-filtering

do not affect estimates of between-year variability,

since fluxes in different years should be affected

similarly (see Morgenstern et al., 2004). Random errors

of up to 50% for the half-hourly flux diminish by

integration over a month or a year. For a more

detailed uncertainty analysis the reader is referred to

Papale et al. (2006). The uncertainty of the flux

partitioning is largely determined by the uncertainty in

the temperature sensitivity of the base respiration

(E0) when extrapolating from night to day. This

uncertainty was estimated as the standard deviation

of all E0 estimates for 1 year (cf. Reichstein et al., 2005),

assuming that the expected value of E0 is constant over

the year and all variability can be attributed to the

estimation error. Clearly, since E0 can vary through the

year, this is a very conservative estimate of error. Errors

for each year were summed for the difference between

years, assuming that they are independent between

years. These uncertainties remained between 4 and

17 g C m�2 month�1 for the summer months and

between 25 and 95 g C m�2 year�1 for the whole year,

but they do not include measurement uncertainties due

to unfavorable conditions, even after u*-correction (e.g.

advection at high u*).

Water vapour flux measurements were analysed here

at six sites: Hesse, Hainich, Sorø, Tharandt, Hyytiala

and Loobos. At Hesse, additional measurements of sap

flow in 10 trees of various diameters were performed

(Granier et al., 2000a), allowing at estimating stand

scaled tree transpiration (T) and deriving canopy

conductance for water vapour (gc) following the

approach of Granier and Breda (1996).

Meteorological conditions were measured half-

hourly above all stands including global, net and PPFD

radiation, air temperature and humidity, rainfall, wind

speed and direction. At some sites, soil water content

was automatically monitored using the TDR technique,

mostly in the upper soil layers: Hesse: �30 and

�55 cm, Hainich: �30 cm, Sorø: 0 to �16 cm,

Tharandt: �10 cm, Hyytiala: �4 to �30 cm and �30

to �68 cm, Fougeres: �30 and �55 cm.

2.2. Water balance modelling

As soil water content was not measured in all the

investigated sites (see Table 1), the water balance model

BILJOU (‘‘BILan hydrique JOUrnalier’’, Granier et al.,

1999) was applied at the 16 sites using the above-

canopy measurements of daily climate (rainfall, global

radiation, air temperature and humidity, wind speed).

The model calculates daily: water fluxes (tree tran-

spiration, understorey evapotranspiration, rainfall inter-

ception, and drainage) and soil water content at

different depths. Tree transpiration (T) is calculated

from the Penman–Monteith equation (Monteith, 1965),

under the big-leaf approximation. Stomatal regulation

during water stress and leaf area index variation (the

latter only in the broadleaved stands) is modelled

according to Granier et al. (1999, 2000c).

Soil water deficit (so called water stress later on)

was assumed to occur in forests when the relative

extractable soil water (REW) dropped below the

threshold of 0.4 (Granier et al., 1999; Bernier et al.,

2002) inducing stomatal regulation in forest trees

(Lagergren and Lindroth, 2002, reported a or slightly

lower threshold value).

A. Granier et al. / Agricultural and Forest Meteorology 143 (2007) 123–145128

REWt on day t is calculated from soil water content

as follows:

REWt ¼EWt

EW(1)

in which EWt and EW are the actual (day t) and the

maximum extractable soil water, respectively. EW is

defined as the difference in soil water content between

field capacity (soil water matric potential of

�0.03 MPa) and wilting point (soil water matric poten-

tial of �1.6 MPa) in the entire root zone, which varies

between 0.9 and 1.8 m according to the sites. We used

soil water retention curves obtained at different depths

in the soil to get field capacity and wilting point water

content.

Three variables are calculated to characterise water

stress: start (i.e. the day of year when REW drops below

0.4), duration (i.e. the number of days when

REW < 0.4) and intensity (i.e. Is = SUM (t = 1–365)

max[0, (0.4 � REWt)/0.4], which is dimensionless and

Fig. 1. Time-course in 2003 of relative extractable water, calculated from bu

REW (full lines) at six European sites. Depths of measurements were: He

(circles), Sorø (c) 2 probes from 0 to �16 cm (circles and crosses), Tharandt

�68 cm (crosses), Fougeres (f) �30 and �55 cm.

ranges between 0 (no stress) and 365 (soil water reserve

totally depleted during 1 year). Is reaches ca. 90–120 in

the most severe observed water stress condition.

Calculation of both stress duration and intensity were

performed over the vegetation period: from budburst to

leaf fall in the deciduous stands, or over the whole year

in the coniferous and the evergreen Mediterranean

stands.

The site-related parameters of the model describe:

(1) the stand structure and the tree phenology:

maximum LAI (June–July); for deciduous forests the

dates of budburst and of complete leaf fall, and (2) soil

properties according to a 1D multilayer sub-model (for

each soil layer: the maximum extractable water, the root

proportion, the bulk density, the soil water content at

�1.6 MPa and the porosity). When data on the root

distribution in the soil was lacking, an exponential

decrease was assumed from soil surface to the

maximum root depth, as defined by the bedrock depth,

at the sites where this information was available.

lk soil water measurements using the TDR technique and of modelled

sse (a) �30 cm (circles) and �55 cm (crosses), Hainich (b) �30 cm

(d) �10 cm (circles), Hyytiala (e) �4 to �30 cm (circles) and �30 to

A. Granier et al. / Agricultural and Forest Meteorology 143 (2007) 123–145 129

In all simulations (years 2002 and 2003), the model

was initialised assuming that soils were saturated (at

field capacity) on 1 January 2002.

In sites where soil water content was monitored by

TDR probes, the agreement between measured and

modelled REW was good (Fig. 1), except at Tharandt

(Fig. 1d) where measurements were only performed in

the superficial soil layer (0–10 cm), while roots extend

far below. At Hesse, where 6 soils layers were equipped

with TDR probes from�10 to�160 cm, the comparison

of REW (0–10 cm) to REW (0–160 cm), showed a

discrepancy similar to that observed at Tharandt (data not

shown). At Hyytiala, the discrepancy between measure-

ments and model for the first third of the year 2003 can be

explained by the snow accumulation in winter and its

melting in spring, phenomena that are not taken into

account in the water balance model BILJOU. During the

vegetation period (DOY 120–280), measured and

modelled REW agreed well.

2.3. Climatic conditions

There is a large variation in the annual rainfall (long-

term average for the last 30 years synoptic weather

station data) in the Carboeurope sites we investigated,

ranging from 510 to 1083 mm year�1. In most places,

the annual rainfall in 2003 was lower than the long term

mean; this reduction was �15% on average. Never-

theless, the difference in annual rainfall between the

long-term average and the year 2003 was not larger than

325 mm. At Sorø and Puechabon, the 2003 rainfall was

higher than average. The rainfall deficit mainly took

place during summer and autumn. The year 2003 was

the driest for the last half century in some places (Hesse

and Tharandt); at most of the other sites, 2003 was

exceptionally dry, but some previous years were drier

(1959, 1973, 1976).

2.4. Tree growth

Tree growth was measured in 2003 at only three sites

(Hesse: beech, Tharandt: spruce, Norunda: spruce and

Scots pine) from circumference measurements at breast

height (1.3 m), manually (100 to 300 trees in the foot-

print of the towers) and at Hesse with automatic

dendrometer bands. At Tharandt and Hesse, biomass

increment was estimated from allometric relationships

relating total tree biomass to circumference and tree

height (J.M. Ottorini and N. Le Goff, personal

communication). When used, dendrometer bands

allowed estimating seasonal growth pattern and

especially the date at which of radial growth stopped.

2.5. Plant area index

At Hesse, in order to relate the day-to-day variation

of transpiration and of the canopy conductance to water

vapour to leaf development, we calculated the plant area

index (PAI), from the measurement of intercepted

radiation by the canopy. Although this method does not

allow at calculating leaf area index because trunks and

branches intercept radiation, especially during the non-

leafed period, the rapid PAI variation during spring and

fall are tightly due to leaf expansion and to leaf fall. PAI

calculation was made under high diffuse-to-total

radiation ratio (>0.5), with an extinction coefficient

of 0.395, i.e. the mean value derived from the Beer-

Lambert Law and maximum LAI as measured in the

litter traps.

2.6. Modelling TER and GPP variation

Both daily TER and GPP were fitted (software

Statgraphics plus1 4.1) using non-linear regressions in

which the independent variables were climatic factors

and REW.

At all the 12 sites where CO2 flux data were available

and with less than 20% of missing data (see Table 3), air

temperature and REW significantly explained the

variation in TER (g C m�2 day�1). Unfortunately, soil

temperature, which is often considered as the major

driving variable of TER fluxes, could not be included in

a general model of TER, since it was not measured at

the same depth at all the sites (at �0.05 or �0.10 m);

moreover, in some sites, this data was missing in the

data base (Table 1). We therefore use the air

temperature, which is well correlated to soil tempera-

ture (average r2 = 0.85 where both were measured).

The following model was fitted on the daily data for

both years 2002 and 2003:

TER ¼ ½1þ a LnðREWÞ�½b expðcTaÞ� (2)

where Ta is the air temperature (8C), and a, b, c are the

fitted parameters.

As for TER, REW and Ta explained the variation of

GPP; global radiation was included in the model. In the

deciduous stands, data were filtered by removing the

periods when leaf area index was not at maximum, i.e.

before DOY 140 or after DOY 280. The following

multiplicative non-linear model of GPP was applied at

the 12 sites, in which the first function of f1 of REW is a

non-rectangular hyperbola, which is often used to fit the

leaf photosynthesis response (Thornley, 1998). The

curvature coefficient was set to 1.4, from preliminary

tests, as the best fit obtained on sites experiencing a

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Table 3

Leaf area index in 2003 (LAI), maximum extractable water (EW), water stress duration (in days), beginning date of drought onset (day of year), drought intensity estimated with the water balance

model, NEE, GPP and TER in 2002 and 2003

Site Tree

density

(n ha�1)

Average

tree height

(m)

LAI

(m2 m�2)

Soil type Soil depth

(cm)

EW

(mm)

Stress

duration

in 2003

Date

beginning

stress in 2003

Stress

intensity

in 2003

Stress

intensity

in 2002

NEE GPP TER

2002 2003 2002 2003 2002 2003

Fougeres 4260 14 7.0 Alocrisol luvisol 160 180 51 229 14.1 0.0

Hainich 334 23.1 6.2 Cambisol 57 170 102 178 53.5 0.0 �582 �475 1670 1326 1088 851

Hesse 3348 18 7.2 Luvisol/stagnic

luvisol

145 175 111 178 57.8 0.0 �593 �498 1663 1382 1070 884

Sorø 326 28 4.8 Mollisol 137 85 211 21.6 1.3 �176 �239 1432 1440 1256 1201

Vielsalm 205 29.9 5.1 Cambisol 150 186 28 216 4.6 0.0 �562 �672 1580 1484 1017 812

Nonantola 1100 8 2.7 Eutric Vertisol 150 135 159 103.8 12.4

Espirra 983 20 2.8 Dystric Cambisol 65 101 148 143 121.6 100.3

Puechabon 7150 5.5 2.9 Rhado chromic

luvisol

50 150 114 157 80.7 47.8 �458 �351 1204 1006 746 655

Le Bray 455 20.8 3.0 Hydromorphic

podzol

120 120 128 166 57.5 50.4 102 �181 1186 1342 1288 1161

San Rossore 567 18 4.2 140 138 161 94.4 2.3 �430 �359 1878 1517 1448 1158

Brasschaat 375 21 3.0 Umbric regosol 40 123 110 183 50.1 0.0

Loobos 360 16 2.3 Podzolic 135 66 214 28.6 0.0

Hyytiala 2500 13.5 4.0 Haplic podzol 125 75 205 24.8 11.5 �305 �200 782 729 478 528

Tharandt 477 26.5 7.6 Loamy skeleton

podzol

150 172 172 161 94.3 0.2 �649 �479 1837 1614 1188 1135

Norunda 895 25 4.0 Dystric regosol >100 125 51 206 10.5 23.7 43 44 1325 1438 1368 1482

Renon 280 29 4.0 Haplic podzol 30 110 63 162 34.4 0.0 �669 �782 1277 1126 608 344

The grey boxes indicate sites that where submitted to significant or severe water stress in 2002.

A. Granier et al. / Agricultural and Forest Meteorology 143 (2007) 123–145 131

large range of REW variations. The second function

( f2) is a rectangular hyperbola depending on global

radiation, while the third function ( f3) is a parabola

describing the canopy photosynthesis limitation by

temperature:

GPP ¼ f 1ðREWÞ f 2ðRgÞ f 3ðTaÞ (3)

f 1ðREWÞ

¼ fd þ eREW � ½ðd þ eREWÞ2 � 2:8deREW�0:5g1:4

(3a)

f 2ðRgÞ ¼ fRg

ðgþ hRgÞ(3b)

f 3ðTaÞ ¼ iþ jTa þ kT2a (3c)

where GPP is expressed in g C m�2 day�1, Rg is the

global radiation (W m�2) and [d. . .k] are the fitted

parameters.

Fig. 2. Top: variation of evapotranspiration (E, eddy covariance measu

evapotranspiration (ETM, Penman–Monteith formula) and of plant area ind

in 2003 at Hesse. The two horizontal grey lines indicate the PAI reduction

conductance for water vapour, as calculated from the Penman–Monteith form

and precipitation (Pi, left Y-axis).

3. Results and discussion

3.1. Seasonal variation of water vapour and carbon

fluxes

An example (Hesse beech forest) of the time-course

of water fluxes during 2003 for water vapour flux (E,

evapotranspiration), as measured with eddy covariance,

and stand-scaled sap flow (T) is presented in Fig. 2. Both

E and T behaved similarly. Deviations from daily

maximum evapotranspiration (ETM), as calculated with

the Penman–Monteith equation with calibrated max-

imum canopy conductance for water vapour for beech

(Granier et al., 2000a), were observed starting DOY 178

and lasted until complete leaf fall around DOY 300. A

parallel sharp decrease of both REW and canopy

conductance for water vapour (gc) was clearly visible,

gc reaching very low values, less than 0.05 cm s�1,

whereas it was comprised between 0.4 and 0.6 cm s�1

in 2002. The small rainfall events (DOY 183, 208, 228,

243) provoked an immediate, but temporary increase in

gc and hence in tree transpiration, lasting for 4–5 days.

rements), tree transpiration (T, stand-scaled sap flow), maximum

ex (PAI, from radiation interception under diffuse radiation, see text)

due to the abnormal leaf fall in August 2003. Bottom: daily canopy

ula inversion (squares) and the variation of modelled REW (grey line)

A. Granier et al. / Agricultural and Forest Meteorology 143 (2007) 123–145132

Fig. 3. Variation of NEE (daily data) and that of modelled relative extractable water (REW) during 2003 in: (a) beech, (b) coniferous, and (c)

Mediterranean stands. For more clarity, not all the sites are included in this figure.

On the same graph, variation in the plant area index is

also shown: an exceptional decrease of ca. 1 m2 m�2

was observed during August (DOY 213–243) that was

due to abnormal premature leaf fall of green leaves,

probably with embolized petioles.

The 2003 time-course of daily-averaged NEE and

modelled REW differed for beech, temperate conifer-

ous, and Mediterranean (plus Le Bray) forests (Fig. 3).

The three beech forests (Hesse, Sorø and Hainich,

Fig. 3a) showed very similar seasonal time-courses and

values of NEE. A rapid increase in carbon uptake

occurred in spring starting around DOY 110 following

bud break, and reached a maximum carbon fixation

around DOY 170. At this date, NEE reached ca.

�10 g C m�2 day�1. Then, carbon uptake declined to

almost zero on DOY 220. Intermittent rainfall events

that occurred after this date temporary stimulated the

carbon uptake.

In the coniferous stands (Fig. 3b), the pattern of

variation in daily NEE was less comparable among

sites, probably partly because of species differences

(Pinus sylvestris and Picea abies). Nevertheless, the

maximum carbon uptake occurred around DOY 180,

followed by a decrease afterwards, to a minimum

around DOY 240, thus similar to, but slightly later than

the beech stands. Thereafter, NEE increased (i.e.

absolute values of NEE decreased) towards zero, as

for beech, and less fluctuated around zero. Note the

abrupt increase in REW at Hyytiala after DOY 280

resulting from heavy rains (84 mm in 5 days).

Mediterranean sites also showed very similar

seasonal variation in NEE, despite their different

species composition: evergreen oak at Puechabon and

maritime pine at San Rossore and Le Bray (Fig. 3c). The

main difference was observed in August, when sites

typically became carbon sources.

Generally, the highest CO2 uptake was observed in

the deciduous forests (ca. �10 g C m�2 day�1), while

the coniferous forests showed medium values

(NEE = �6 to �7 g C m�2 day�1). The lowest rates

were measured in the Mediterranean stands (ca.

�4 g C m�2 day�1), which also exhibited the lowest

seasonal variation in NEE. In most of the investigated

sites, there was a clear decrease in the CO2 uptake after

DOY 180–200, much sharper than in 2002 (Fig. 4)

accompanying an increasing water stress severity

(Fig. 3). After this period, NEE even became positive

(i.e. source of CO2 to the atmosphere) for some days at

most of the sites. At Puechabon and Le Bray, NEE was

positive for more than 40 days, indicating that total

ecosystem respiration exceeded gross photosynthesis.

The seasonal variation in total ecosystem respiration

(TER) and gross primary production (GPP) exhibited at

all sites a sharp increase in spring, with maximum rates

between May and August during wet years (e.g. in

Fig. 4 at Hesse and Tharandt, the year 2002 during

A. Granier et al. / Agricultural and Forest Meteorology 143 (2007) 123–145 133

Fig. 4. Variation of 24-h daily evapotranspiration (E, a and b), of gross primary production (GPP, c and d) and of total ecosystem respiration (TER, e

and f) at Hesse (left panels) for beech and at Tharandt (right panels) for spruce in 2002 (closed circles) and 2003 (open circles). Also shown is the

temporal variation of REW in 2002 and 2003 at the two sites (Hesse: panel g, Tharandt: panel h). The horizontal line indicates the REW value of 0.4.

which REW remained above 0.4), corresponding to the

period of high photosynthesis and warm temperatures.

During 2003, TER showed a maximum around DOY

150 (4–8 g C m�2 day�1), which was more pronounced

in the beech stands. Maximum GPP was also reached

around DOY 150 at Hesse (15 g C m�2 day�1) and

Tharandt (13 g C m�2 day�1). In 2003, TER and GPP

were clearly reduced by drought thereafter. During the

driest period, between DOY 210 and 250, TER was

reduced by 30–32% in 2003 as compared to 2002; GPP

was decreased in a larger proportion, by 36–50% and E

by 35%.

3.2. 2003 versus 2002 annual carbon and water

balances

Variation in the annual NEE from 2002 to 2003 are

compared in Fig. 5. At Le Bray, where 2002 reached the

same drought intensity as 2003 (Table 3), the value of

2001 was used instead of 2002. The drought effect on

A. Granier et al. / Agricultural and Forest Meteorology 143 (2007) 123–145134

Fig. 5. Variation in the annual NEE between 2003 and 2002 in 12

forest stands. The positive values indicate a decreased carbon fixation

in 2003 compared to 2002. Top: variation among the sites. Bottom: the

NEE 2002–2003 variation as a function of water stress intensity

(ISTRESS, dimensionless). At Le Bray, the reference (wet) year

was 2001 because 2002 was a dry year. Renon is not shown due to

incomplete data set in 2003.

NEE was variable from site to site, most of them

exhibiting a lower NEE in 2003 as compared to 2002.

An increase (i.e. higher carbon uptake) in NEE from

2002 to 2003 was observed at Renon (113 g C m�2

year�1), Vielsalm (110 g C m�2 year�1) and Sorø

(+63 g C m�2 year�1), a moderate decrease (i.e. a

lower carbon uptake) of 50–100 g C m�2 year�1 at

Loobos, San Rossore, Hainich, Hyytiala, Hesse and

Puechabon, and a stronger decrease of 150–300 g

C m�2 year�1 at Tharandt and Le Bray. The three sites

where an increase in NEE was observed were submitted

to a moderate drought intensity in 2003 that did not

reduce stomatal conductance to a large extend and for a

limited period, while the generally observed higher

radiation in summer 2003 enhanced photosynthesis.

Besides stomatal closure caused by water stress (Fig. 2),

the annual E was not reduced to a large extent in 2003

compared to 2002 (�5 to�10% at the driest sites versus

�15 to�25% for both GPP and TER), due to the higher

evaporative demand in 2003: the potential evapotran-

spiration (Penman formula) was on average 20% higher

in 2003 than in 2002.

3.3. Drought distribution in Europe

Water stress duration in 2002 and 2003, and the date of

onset and the drought intensity (ISTRESS) in 2003 are

shown in Table 3. In 2002, ISTRESS was null or low,

except at the south-western sites (Le Bray, Puechabon

and Espirra) and the Nordic sites (Norunda and Hyytiala),

where the year 2002 was also relatively dry and even

slightly drier than 2003. The largest values of ISTRESS

in 2003 were reached at Hainich, Le Bray, Hesse,

Tharandt, Puechabon, Espirra, Nonantola and San

Rossore, where water stress lasted for 3–4 months,

while at Vielsalm, Fougeres, Sorø, Hyytiala, Norunda,

Renon and Loobos it lasted for only 1–2 months.

ISTRESS, onset and duration were well correlated to

each other (r2 = 0.80). The distribution of the ISTRESS

indices in Europe is shown in the map of Fig. 6. The most

severe drought was observed over a large southwest to

northeast transect in Europe. The northwestern coast of

France, the North Sea and the Baltic Sea area were less

affected by drought. Over the investigated stands, the

2003 reduction in NEE was related to drought intensity

(r2 = 0.60, p = 0.003, Fig. 5).

3.4. Relating fluxes to water stress intensity

Although sites differed in the magnitude of soil water

depletion, due to large differences in climate, soil and

canopy properties, the time-courses of simulated REW

in 2003 were very similar because the main rainfall

events occurred quite simultaneously across the sites

(around DOY 182, 208, 250 and 275, see Fig. 3). At all

sites, extractable soil water dropped for a variable

duration during the growing season below REW = 0.4,

corresponding to the soil water depletion below the

threshold inducing stomatal closure. In 2002 (data not

shown), this threshold was either not reached or

exceeded for only a few days, except at Le Bray,

Espirra and Puechabon where drought was severe.

Large differences among sites were observed during the

autumn and winter soil rewetting, mainly because of

large differences in rainfall and also in physical soil

properties; moreover in some sites (Tharandt, Sorø,

Hesse) complete soil recharge did not occur before the

end of 2003 or was not even achieved by then. This

pattern was also exceptional, as in normal years

complete soil recharge is achieved in October or

November.

A. Granier et al. / Agricultural and Forest Meteorology 143 (2007) 123–145 135

Fig. 6. Distribution of water stress intensity in 2003 over the 16 investigated forest sites of Carboeurope.

Modelling the stand water balances allowed estima-

tion of the temporal variation in soil water content at

each site and hence the opportunity to relate water

vapour and carbon fluxes to REW (Fig. 7). We remind

that we used here the modelled REW because, except at

few sites, there are no routine soil water content

measurement in the whole root zone. The maximum

water vapour and carbon fluxes (at high soil water

content) varied among sites, as reported above (Fig. 3).

Daily E, GPP and TER followed comparable patterns:

they were reduced when REW decreased below

threshold values (REW0). Under declining REW, there

was a more gradual and earlier decrease in GPP and E

(REW0 � 0.4) than in TER (REW0 � 0.2). The large

scatter of E was due to varying day-to-day weather

condition (mainly radiation and VPD). In the six forest

stands where vapour fluxes were studied, the decrease in

REW from 1 to 0.4 did also not lead to significant

change in E (Fig. 7). Below this REW threshold, there

was a marked decrease in E in all the sites. One may also

note that, for REW ranging from 0.8 to 1.0 (spring

periods), the daily water vapour flux remained low as

the result of non-complete leaf maturity and/or of

temperature limitation for stomatal opening. As for E

variability, the scatter in TER and GPP is well related to

weather condition: for GPP, the values tending to zero

correspond to low radiation and/or rainfall condition.

Remarkably large TER fluxes are noticed at Norunda,

which have on average an annual carbon balance close

to zero (Lindroth et al., 1998).

3.5. Carbon fluxes

At the 12 sites where carbon flux data were available,

we tested the influence of the major environmental

variables (radiation, air temperature, vapour pressure

deficit, modelled REW) on the daily values of TER and

GPP, the latter during the growing season for the

deciduous stands, using the models (2) and (3).

For TER, fitted parameters and coefficients of

determination are given in Table 4. All the coefficients

of determination where higher than 0.5, except at

Renon. The complexity of processes underlying TER

probably explains these quite low coefficients of

regression. In the site of Vielsalm where drought was

very mild, the effect of REW on TER variation was not

A. Granier et al. / Agricultural and Forest Meteorology 143 (2007) 123–145136

Fig. 7. Variation of daily (24-h sums) evapotranspiration (E, top), total ecosystem respiration (TER, middle) and gross primary production (GPP,

bottom) as a function of modelled relative extractable water in the soil (REW) in 2003. Evapotranspiration was measured in only 6 sites, carbon

fluxes (GPP and TER) in 12 sites. Data of Vielsalm, where REW remained high during summer 2003, are not shown. For better clarity, data are

restricted to the period between DOY 140 and 280. The sites Norunda and Renon, exhibiting extreme TER values are distinguished. Symbols are

explained in Table 1.

Table 4

Coefficients of the non-linear regression between TER, REW and air temperature (see Eq. (2))

Hainich Hesse Sorø Vielsalm Puecha bon Le Bray San Rossore Loobos Hyytiala Tharandt Norunda Renon

a 0.243 0.193 0.159 0.109 0.218 0.040 0.147 0.167 0.018 0.105 0.080 0.172

b 1.598 1.466 1.877 1.526 0.940 1.422 1.542 2.397 1.038 1.623 2.314 0.814

c 0.0633 0.0629 0.0691 0.0576 0.0668 0.0588 0.0588 0.0493 0.0532 0.0693 0.0721 0.0781

r2 0.73 0.67 0.66 0.51 0.52 0.66 0.55 0.64 0.57 0.73 0.73 0.40

A. Granier et al. / Agricultural and Forest Meteorology 143 (2007) 123–145 137

Table 5

Coefficients of the non-linear regression between GPP, REW, global radiation and temperature (see Eq. (3))

Hainich Hesse Sorø Vielsalm Puechabon Le Bray San Rossore Loobos Hyytiala Tharandt Norunda Renon

d 0.155 0.0819 0.0818 0.255 0.0439 0.0216 0.104 0.0513 0.0612 0.0415 0.0681 0.135

e 1.286 0.367 0.366 2.5E+06 0.209 0.424 1.45 0.443 0.885 0.714 2.028 2.864

f 0.228 0.145 �0.065 �0.404 0.129 0.152 0.122 0.275 0.160 0.161 0.166 0.133

g 124.9 38.2 125.2 259.6 66.5 58.1 152.9 52.3 45.2 38.04 73.8 19.0

h 0.139 0.075 0.067 0.275 0.041 0.028 0.056 0.271 0.039 0.026 0.056 0.168

i �9.45 74.6 �55.5 12.2 37.7 15.3 41.8 87.9 1.88 19.3 24.5 31.5

j 9.36 6.11 �35.0 2.45 3.85 10.2 4.21 6.93 4.89 6.05 4.27 7.16

k �0.261 �0.219 1.052 �0.0822 �0.0977 �0.274 �0.127 �0.0812 �0.156 �0.200 �0.104 �0.197

r2 0.76 0.77 0.82 0.77 0.77 0.73 0.84 0.59 0.81 0.83 0.87 0.73

significant. The coefficient c, that describes the rate at

which TER increases with temperature, is quite constant

within individual tree species: 0.063–0.069 in the 3

beech stands, 0.059 in the 2 maritime pine stands,

0.049–0.053 in the 2 Scots pine stands.

Fits of GPP were generally better than that of TER.

The regression parameters and coefficient of determi-

nation are given in Table 5. The fit was quite poor for

Fig. 8. Modelled ecosystem respiration (TER, top) and gross primary produ

extractable water (REW) in 12 forest sites. Air temperature was set at 20 8C, g

cannot be distinguished.

Loobos (r2 = 0.59), but coefficients of determination

were higher than 0.70 at all the other sites, reaching 0.87

at Norunda. At Vielsalm, as for TER, the effect of REW

on GPP variation was not significant. At some sites, the

model could be improved to some extent when

introducing the negative effects of increasing air vapour

pressure deficit and/or the direct to diffuse radiation

ratio on the GPP variation. Nevertheless, as the

ction (GPP, bottom) from Eqs. (2) and (3), of as a function of relative

lobal radiation at 20 MJ m�2 day�1. Note that GPP for Hesse and Sorø

A. Granier et al. / Agricultural and Forest Meteorology 143 (2007) 123–145138

additional explained variance was limited and, more-

over, only improved the fit at some sites, we preferred to

use the simplest model (3).

The variation of modelled TER and GPP as a

function of REW is shown in Fig. 8 in the 12 sites. The

maximum assimilation rates (GPPmax) under wet

condition varied from 5.4 (Puechabon) to 12.8 g

C m�2 day�1 (Hesse and Sorø). A general trend of

increasing GPPmax with LAI was found among sites

(data not shown). Norunda exhibited very high rates of

TER: under unlimited soil water and warm temperature,

TERmax reached 9.8 g C m�2 day�1. In the 11 other

Fig. 9. Plots of modelled versus measured GPP (left panels) and TER (righ

beech stands (top), Mediterranean stands (middle) and temperate coniferou

sites, TERmax ranged between 3.0 and 7.5 g C m�2

day�1. Both GPP and TER decreased with REW.

However, GPP was more responsive to increasing

drought than TER; therefore NEE was reduced to a

lesser extent than GPP. The three beech and the

Mediterranean stands clearly exhibited a higher

sensitivity of GPP to water stress than the temperate

coniferous forests. The two models capture satisfacto-

rily the GPP and TER variation (Fig. 9). However,

modelled GPP was generally better correlated with

observed data than TER. We can partly explain it by the

use of air temperature instead of soil temperature in the

t panels), daily values for 2002 and 2003. Sites are pooled as follow:

s stands (bottom). The 1:1 line is drawn.

A. Granier et al. / Agricultural and Forest Meteorology 143 (2007) 123–145 139

Fig. 10. Effect of drought on the reduction of gross primary produc-

tion (GPP) and on ecosystem respiration (TER), daily estimates, when

relative extractable water drops from 1.0 to 0.1, as calculated from

models (2) and (3), with air temperature = 20 8C and global

radiation = 20 MJ m�2 day�1. Letter B refers to broadleaved, M to

broadleaved Mediterranean and C to coniferous stands.

model. Moreover, because ecosystem respiration

involves more processes than photosynthesis, each

responding to specific and numerous drivers and thus

may not be captured by an as simple approach as GPP.

Moreover, the correlations between measured and

modelled values were higher in the beech stands than

in the other ecosystems types.

From Eqs. (2) and (3) we calculated the theoretical

daily reduction in TER and GPP for a drop of REW

from 1.0 (i.e. at field capacity) to 0.1 (severe water

stress), other factors (radiation, temperature) being set

at optimum; the resulting decreases in GPP and TER are

presented in Fig. 10. The broadleaved temperate and

Mediterranean sites clearly exhibited stronger GPP

reductions with drought (45–60%) than coniferous sites

(16–38%). The drought-induced decrease in TER also

showed, albeit less clearly, a difference among

ecosystem types, i.e. a smaller reduction in TER in

coniferous than in deciduous and Mediterranean forest

ecosystems. At Le Bray and Hyytiala, TER was more

sensitive than GPP to drought TER; at Renon, it was the

opposite.

3.6. Reductions in tree growth following the

drought

Tree growth measurements were performed at Hesse

(beech) and Tharandt (spruce), both experiencing a

severe and comparable water stress intensity in 2003,

and at Norunda (spruce and Scots pine), under medium

stress intensity (see Table 3). The seasonal increase in

tree circumference at Hesse from dendrometer band

measurements (data not shown) started earlier in 2003

than in 2002 as a consequence of hot spring and

therefore earlier budburst. The circumference growth

was substantially declined on DOY 180 and continued

slowly until DOY 190, date of growth cessation, which

is exceptionally early. REW reached 0.4 on DOY 178.

When comparing 2003–2002, annual NEE was reduced

by 18% (�106 g C m�2 year�1) and 24% (�151 g

C m�2 year�1) at Hesse and Tharandt, respectively,

while the annual biomass increment was reduced in

different proportions, i.e. by 22% and 44%, respec-

tively. At Norunda, the 2003 growth reached only 64%

of the mean 2004 and 2005 growth (two humid years,

while 2002 was dry), pine trees being more affected by

drought than spruces.

Quantification of drought should be based on

biological variables such as predawn leaf water potential

(Cp), a measure of the water constraint that is actually

experienced by the vegetation. At Hesse, Cp dropped to

�2.2 MPa in beech and in the accompanying hornbeam

trees, indicating a severe water stress. This Cp was lower

than the theoretical value of soil water potential at the

wilting point (�1.6 MPa), indicating that these adult

trees may extract water from very small soil micro pores,

more actively than low vegetation, as was previously

observed in Douglas fir (Aussenac et al., 1984), Scots

pine (Sturm et al., 1998), Mediterranean oaks (Rambal,

1984) or sessile oaks (Breda et al., 1995). Unfortunately,

measurements of leaf water potential could not be

routinely performed at all sites, let alone repeatedly.

Therefore, our approach was to estimate soil water

content in the root zone by modelling the water balance.

The water balance model used here agreed well with soil

water content measurements in the sites where those

measurements were performed. In 2006, the duration of

the water shortage period varied from 28 to 148 days

among the sites, depending on stand LAI and soil

extractable water. Both drought intensity and duration

depended locally on the amount of rainfall during the

June to August period. Rainfall events, even small ones,

provoked a rapid increase in both evapotranspiration and

carbon uptake due to stomata re-opening with free water

becoming available for the superficial roots, even if the

underlying bulk soil remained dry (Choisnel et al., 1995).

Nevertheless, we observed here that small rain events

during the summer of 2003 lead to only partial recovery

of water vapour fluxes could indicate damages in the soil-

to-leaf conductivity, probably due to the fine root dying

and/or xylem embolism in the most apical part of the

trees. In autumn or winter, at some sites, the complete soil

water recharge was not even achieved by the end of

December.

Maximum water fluxes mainly depend on the

evaporative demand and on LAI, as previously reported

for European beech (Granier et al., 2002) and for a wide

A. Granier et al. / Agricultural and Forest Meteorology 143 (2007) 123–145140

range of tree species under contrasted climates (Granier

et al., 1996, 2000c). In our study, water vapour fluxes

were dramatically reduced during the drought when

REW dropped below a threshold comprised between

0.35 and 0.4 according to the sites. In agreement with

our results, a REW threshold of 0.4 was reported in

different tree species under various soil types (Black,

1979; Dunin and Aston, 1984; Granier, 1987; Granier

and Loustau, 1994; Granier et al., 1999; Wilson and

Baldocchi, 2000; Rambal et al., 2003). However, our

approach of the drought quantification by modelling

REW was partly limited at some of the investigated sites

by: (i) the relatively poor knowledge of soil-root

properties, and to a lesser extent by; (ii) the stand and

understorey LAI and their temporal variation. There is

therefore some uncertainty in the actual water stress

intensity that forest ecosystems experienced in summer

2003. For a more in-depth modelling, actual site

parameters, especially for soil (physical soil properties,

extractable soil water, root distribution) would be

necessary. This is a challenge for future drought studies

at the eddy flux sites.

Decreasing soil water content induced a decrease in

GPP and, at lower REW, also in TER. The decrease in

photosynthesis of the beech and the Mediterranean

species appeared to be more pronounced than that for

coniferous stands. Cermak et al. (1993) and Granier

et al. (2000a) also showed the high sensitivity to water

stress in beech. Rambal et al. (2003) highlighted the

importance of water stress, even in Mediterranean-type

ecosystems, that experience frequent and pronounced

summer water deficits and therefore presumably exhibit

constitutive adaptations to drought (phenology, photo-

protection, leaf anatomy or rooting depth). Hence, the

high sensitivity to water stress of Mediterranean forests

was rather surprising. However, this response could also

constitute an adaptation under increasing frequency of

severe summer droughts.

During drought, daily E and GPP decreased

simultaneously and the ratio between them was

maintained quite constant even at low REW values,

indicating not significant increase in the canopy water-

use efficiency (data not shown, cf. also Reichstein et al.,

2006), calculated as the ratio GPP/E. Hence, stomatal

closure seemed to explain most of the limitation in GPP.

Drought also decreased TER in summer 2003 at all

sites, but to a lesser extent than GPP. Thus, during the

drought period the ratio of TER/GPP increased.

However, at an annual time scale TER/GPP did not

significantly differ between 2002 and 2003, remaining

on average close to 0.70. Even if the eddy-covariance

method is not suitable for separating the two main

components of ecosystem respiration, i.e. autotrophic

and heterotrophic respiration, both terms were probably

simultaneously reduced. Griffis et al. (2004) showed

during drought in a boreal deciduous forest a strong

reduction in the respiratory fluxes: ecosystem, soil and

bole respiration, their decrease being well-related to soil

water content measured in the superficial layers. As

both GPP and tree growth were limited by drought, also

autotrophic respiration most likely decreased during

summer 2003. From a trenched plot study, a strong

reduction in autotrophic respiration was observed at

Hesse in 2004 (Ngao, 2005), also a dry year in this area

(data not shown). In forest ecosystems, autotrophic

respiration consumes about 40–75% of the net

photosynthetic production (Saxe et al., 2001) and has

been shown to strongly depend on the availability of

recent assimilates (Hogberg et al., 2001; Ekblad and

Hogberg, 2001). Dealing with differences in the

respiration response to drought among forest types,

Curiel Yuste et al. (2004) observed within a mixed

temperate forest that deciduous canopies, which have

larger seasonal amplitude in GPP than evergreen

canopies, also exhibit larger seasonal changes in

respiration. In our study, we also showed in coniferous

forests that TER, as GPP, was generally less reduced by

drought than in the deciduous stands, although this

observation must be confirmed in future studies on a

broader range of tree species. The strong dependence of

autotrophic respiration on the availability of recent

assimilates may therefore explain why in this study

TER the beech forests were more responsive to

temperature than in the other forest types.

Also heterotrophic respiration is drought sensitive,

as was clearly shown at Hesse during the 2004 drought

(Ngao, 2005). A recent meta-analysis on the contribu-

tion of heterotrophic respiration to soil CO2 efflux

suggested that in coniferous forests, TER appeared to be

less reduced under warmer climate; from 60 to 70% in

Boreal forests, to less than 50% in tropical forests

(Subke et al., 2006). We have, however, no information

on the separate effects of extreme drought on the

autotrophic and heterotrophic respiratory components

of soil CO2 efflux or TER. TER can also be separated in

the above and below ground components. The major

contribution originates from below ground compart-

ments, which represents 50–80% of TER, with an

average value of 63% in undisturbed ecosystems

(Janssens et al., 2001). Besides soil temperature,

drought explains a large part of the intra and inter-

annual variability of soil respiration (Reichstein et al.,

2003; Epron et al., 2004). Therefore, as the decrease in

TER observed here probably originated mostly in the

A. Granier et al. / Agricultural and Forest Meteorology 143 (2007) 123–145 141

decrease of soil respiration, ecosystem respiration

models must take into account both temperature and

soil water content (Reichstein et al., 2002a).

As both GPP and TER fluxes were reduced by

drought, the absolute decrease in NEE was smaller than

that in GPP; this was also confirmed by recent large-

scale modelling approaches developed at the European

scale (Ciais et al., 2005). In sites where drought was

most severe, NEE became positive for 1–2 weeks in

August. Similar results were found on a pasture in the

central USA (Meyers, 2001), which under normal

precipitation was a carbon sink (NEE = �120 g

C m�2 year�1), but turned into a source (NEE = +155 g

C m�2 year�1) during a dry year.

Unfortunately, in the investigated sites for the

studied period, there were few observations on tree

growth, nor early leaf fall, branch fall or tree mortality.

At most sites, the maximum leaf area index observed in

2003 was not lower than in 2002. However, early leaf

yellowing and leaf fall was observed in some stands

where drought was the most severe. For example at

Hesse, important leaf fall in mid-August was observed,

estimated as 1.7 m2 m�2 (Breda et al., 2006); at

Brasschaat, the pine stand also showed a decrease in

LAI of 0.8 m2 m�2, and drought reduced live root

biomass by about 40% (Konopka et al., 2005). At the

Tharandt site, needle-litter fall was abnormally

increased from mid-September to November 2003,

equalling a decrease in LAI of 0.9 m2 m�2, while

normally the maximum litter fall occurred between

November and March; further, about 20 spruce trees had

to be felled within the source area of the tower due to

bark-beetle attack.

In both deciduous and coniferous stands, the 2003

tree growth was significantly reduced. A higher

reduction in spruce tree growth as compared to beech

was observed. This can be explained by an earlier

drought onset date (DOY 161 at Tharandt, 178 at Hesse)

and to the timing of radial growth in both species: on

average 66% of the annual growth takes place before 1

July (DOY 182) in beech (Bouriaud et al., 2004), while

in spruce it is only of 56% at the same date. At Hesse,

due to the high soil water reserve, drought, even

exceptional, never takes place before July. In the

following year, 2004, the growth rate during the rapid

radial increment period (DOY 140–180), was lower

than for all the previous years (1999–2003):

0.20 mm day�1 in 2004 versus 0.27 mm day�1 in

2003. The annual circumference growth in 2004 was

27% lower than in 2003 (i.e. only 62% of the 2002

annual growth), indicating in beech lasting drought

effects on the radial growth. Coupling soil water deficit

calculation using the same water balance model, we

previously reported such time lag effects of droughts

occurring during the previous summer on beech crown

condition (Badeau and Breda, 1997), leaf area index

(Breda, personal communication) or radial growth

(Granier et al., 1996; Lebourgeois et al., 2005). We

interpret these differed effects, i.e. both reduced growth

rate in spring and maximum growth, as a consequence

of reduced carbohydrate, lipids and protein reserves at

the end of 2003 (see Breda et al., 2006). Analysing

mature trees from various climate zones from tropical to

temperate and alpine tree-line systems, Korner (2003)

found that in periods of reduced or zero growth, the

source activity (carbon assimilation) still exceeds the

demand (respiration). Even during the dry midsummer

in the Mediterranean area, photosynthesis is less

depressed than structural growth. Thus, depletion of

non-structural carbohydrate pools, only, cannot explain

the reduced growth in 2004. Other factors, e.g., damage

to the rooting system or irreversible xylem embolism,

affecting sink activity must have restricted the biomass

production of trees. Leuschner et al. (2001) showed a

stimulated fine-root growth of beech during dry

summer, thus compensating for root biomass losses

due to high root mortality during drought. This

behaviour would increase the carbon sink of the root

compartment and may contribute to the disproportional

reduced stem growth rate. More long-term observations

are, however, needed to determine whether drought

extremes such as in 2003 result in tree dieback (with

long-term effects on the carbon balance) or in complete

recovery. Long-term consequences of an extreme

drought event are still poorly known. Smaller reserves

in trees organs and/or damages in the root systems or

xylem dysfunction could probably weaken the trees for

extended periods during which they may be more

sensitive to stress.

We did not deconvolute the effect of high

temperature from that of the extreme drought, so the

reader should be aware that in some European places,

forests could experience more than a drought stress. The

highest temperatures (>40 8C in Central, East France

and in Western Germany) occurred when water stress

was the highest during August 2003. As a consequence,

canopy temperature rose up to 3–4 8C above air

temperature, probably inducing damage to leaf pig-

ments. Nevertheless, our investigated stands were not

submitted to as high temperatures: the peak tempera-

tures were 39 8C at Le Bray and 37 8C at Hesse and San

Rossore.

Analysis of extreme climatic events such as the 2003

heat and drought wave can improve our knowledge of the

A. Granier et al. / Agricultural and Forest Meteorology 143 (2007) 123–145142

possible effects of climate change on the functioning of

the ecosystems. We showed that forest ecosystems

responded quickly and sharply to drought. If summer

droughts would become more frequent, carbon uptake by

the vegetation would probably decrease, with some sites

even switching from a sink to a source of carbon.

Accounting for the effects of extreme events is definitely

essential to make accurate climate and carbon cycle

predictions for the coming decades. Except perhaps at

high elevation, more frequent heat and drought events

may counteract the smooth trends of warmer tempera-

tures and longer growing seasons, implying a long-term

decrease in productivity, reversing sinks to sources, and

inducing positive carbon-climate feedbacks.

4. Conclusion

In this work we pointed out the following points:

1. D

rought is a major driver of the water and carbon

fluxes in the forest ecosystems, whatever tree species

and climatic zone. Therefore, more effort should be

devoted in the future to soil water measurements over

the root zone at the eddy-flux sites.

2. B

oth transpiration, gross photosynthesis and respira-

tion are sharply decreased when the relative

extractable soil water drops below ca. 0.4.

3. N

et ecosystem exchange is reduced with soil water

depletion, but to a lesser extend than gross ecosystem

production, due to the compensating effect of the

decreased ecosystem respiration.

4. T

he coniferous species appear to be less affected by

drought than the broadleaved species.

5. D

rought impacts the annual tree growth and has also

consequences in the following years.

Acknowledgements

We thank all the technicians, students and post-docs

who helped collect data at all sites.

Most of the research in the 16 sites investigated here

is supported by the CARBOEUROPE No. GOCE-CT-

2003-505572 European programme.

We also thank Riccardo Valentini (University of

Tuscia, Italy) who played a major role in stimulating the

scientific cooperation between the teams to conduct

such common works.

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