evidence for soil water control on carbon and water ...€¦ · evidence for soil water control on...
Post on 15-Jun-2020
0 Views
Preview:
TRANSCRIPT
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
A.
Gra
nier
eta
l./Ag
ricultu
ral
an
dF
orest
Meteo
rolo
gy
14
3(2
00
7)
12
3–
14
51
26
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
A.
Gra
nier
eta
l./Ag
ricultu
ral
an
dF
orest
Meteo
rolo
gy
14
3(2
00
7)
12
3–
14
51
30
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 carbonfluxes 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 waterdepletion, 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 bydrought than the broadleaved species.
5. D
rought impacts the annual tree growth and has alsoconsequences 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.
References
Aubinet, M., Chermanne, B., Vandenhaute, M., Longdoz, B., Yernaux,
M., Laitat, E., 2001. Long term carbon dioxide exchange above a
mixed forest in the Belgian Ardennes. Agric. For. Meteorol. 108,
293–315.
Aubinet, M., Grelle, A., Ibrom, A., Rannik, U., Moncrieff, J., Foken,
T., Kowalski, A.S., Martin, P.H., Berbigier, P., Bernhofer, C.,
Clement, R., Elbers, J., Granier, A., Grunwald, T., Morgenstern,
K., Pilegaard, K., Rebmann, C., Snijders, W., Valentini, R., Vesala,
T., 2000. Estimates of the annual net carbon and water exchange of
forests: the EUROFLUX methodology. Adv. Ecol. Res. 30, 113–
175.
Aussenac, G., Granier, A., Ibrahim, M., 1984. Influence du desseche-
ment du sol sur le fonctionnement hydrique et la croissance du
douglas (Pseudotsuga menziesii (Mirb.) Franco). Acta Oecologica
Oecol. Plant. 5, 241–253.
Badeau, V., Breda, N., 1997. La recente crise de vitalite du hetre en
plaine semble largement liee aux deficits hydriques. Les Cah-
iers du DSF 1-1997 (La sante des forets [France] en 1996), pp.
60–63.
Battaglia, M., Cherry, M.L., Beadle, C.L., Sands, P.J., Hingston, A.,
1998. Prediction of leaf area index in eucalypt plantations:
effects of water stress and temperature. Tree Physiol. 18, 521–
528.
Berbigier, P., Bonnefond, J.M., Mellmann, P., 2001. CO2 and water
vapour fluxes for 2 years above Euroflux forest site. Agric. For.
Meteorol. 108, 183–197.
Bernier, P.Y., Breda, N., Granier, A., Raulier, F., Mathieu, F., 2002.
Validation of a canopy gas exchange model and derivation of a soil
water modifier for transpiration for sugar maple (Acer saccharum
Marsh.) using sap flow density measurements. For. Ecol. Manage.
163, 185–196.
Black, T.A., 1979. Evapotranspiration of Douglas fir stands exposed to
soil water deficits. Water Res. 15, 164–170.
Bouriaud, O., Breda, N., Le Moguedec, G., Nepveu, G., 2004.
Modelling variability of wood density in beech as affected by
ring age, radial growth and climate. Trees 18, 264–276.
Breda, N., Cochard, H., Dreyer, E., Granier, A., 1993. Water
transfer in a mature oak stand (Quercus petraea): seasonal
evolution and effects of a severe drought. Can. J. For. Res. 23,
1136–1143.
Breda, N., Granier, A., Barataud, F., Moyne, C., 1995. Soil water
dynamics in an oak stand. I. Soil moisture, water potentials and
water uptake by roots. Plant Soil 172, 17–27.
Breda, N., Huc, R., Granier, A., Dreyer, E., 2006. Temperate forest
trees and stands under severe drought: a review of ecophysiolo-
gical responses, adaptation processes and long-term conse-
quences. Ann. For. Sci. 63, 625–644.
Carrara, A., Kowalski, A., Neirynck, J., Janssens, I., Yuste, J.C.,
Ceulemans, R., 2003. Net ecosystem CO2 exchange of mixed
forest in Belgium over 5 years. Agric. For. Meteorol. 119, 209–
227.
Cermak, J., Matyssek, R., Kucera, J., 1993. Rapid response of large,
drought-stressed beech trees to irrigation. Tree Physiol. 12, 281–
290.
Choisnel, E.M., Jourdain, S.V., Jacquart, C.J., 1995. Climatological
evaluation of some fluxes of the surface energy and soil water
balances over France. Ann. Geophys. 13, 666–674.
Ciais, P., Reichstein, M., Viovy, N., Granier, A., Ogee, J., Allard, V.,
Buchmann, N., Aubinet, M., Bernhofer, Ch., Carrara, A., Che-
vallier, F., De Noblet, N., Friend, A., Friedlingstein, P., Grunwald,
T., Heinesch, B., Keronen, P., Knohl, A., Krinner, G., Loustau, D.,
Manca, G., Matteucci, G., Miglietta, F., Ourcival, J.M., Pilegaard,
K., Rambal, S., Seufert, G., Soussana, J.F., Sanz, M.J., Schulze,
E.D., Vesala, T., Valentini, R., 2005. Unprecedented reduction in
A. Granier et al. / Agricultural and Forest Meteorology 143 (2007) 123–145 143
European primary productivity caused by heat and drought in
2003. Nature 437, 529–533.
Cienciala, E., Kucera, J., Ryan, M., Lindroth, A., 1998. Water flux in
boreal forest during two hydrologically contrasted years; species
specific regulation of canopy conductance and transpiration. Ann.
For. Sci. 55, 47–61.
COPA-COGECA, 2003. Assessment of the impact of the heat wave
and drought of the summer 2003 on agriculture and forestry.
Agricultural Organisations in the European Union and the General
Committee for Agricultural Cooperation in the European Union,
http://www.copa-cogeca.com/pdf.
Curiel Yuste, J., Janssens, I.A., Carrara, A., Ceulemans, R., 2004.
Annual Q10 of soil respiration reflects plant phenological patterns
as well as temperature sensitivity. Global Change Biol. 10, 1161–
1169.
Dolman, A.J., Moors, E.J., Elbers, J.A., 2002. The carbon uptake of a
mid latitude pine forest growing on sandy soil. Agric. For.
Meteorol. 111, 157–170.
Dunin, F.X., Aston, A.R., 1984. The development and proving of
models of large scale evapotranspiration: an Australian study. In:
Sharma, M.L. (Ed.), Evapotranspiration from Plant Communities.
Elsevier, Amsterdam, pp. 305–323.
Ekblad, A., Hogberg, P., 2001. Natural abundance of 13C in CO2
respired from forest soils reveals speed of link between tree
photosynthesis and root respiration. Oecologia 127, 305–308.
Epron, D., Ngao, J., Granier, A., 2004. Interannual variation of soil
respiration in a beech forest ecosystem over a 6-year study. Ann.
For. Sci. 61, 499–505.
Foken, T., Wichura, B., 1996. Tools for quality assessment of surface-
based flux measurements. Agric. For. Meteorol. 78, 83–105.
Gholz, H.L., Ewel, K.C., Teskey, R.O., 1990. Water and forest
productivity. For. Ecol. Manage. 30, 1–18.
Goldstein, A.H., Hultman, N.E., Fracheboud, J.M., Bauer, M.R.,
Panek, J.A., Xu, M., Qi, Y., Guenther, A.B., Baugh, W., 2000.
Effects of climate variability on the carbon dioxide, water, and
sensible heat fluxes above a ponderosa pine plantation in the Sierra
Navada (CA). Agric. For. Meteorol. 101, 113–129.
Granier, A., 1987. Evaluation of transpiration in a Douglas-fir stand by
means of sap flow measurements. Tree Physiol. 3, 309–320.
Granier, A., Aubinet, M., Epron, D., Falge, E., Gu@mundsson, J.,
Jensen, N.O., Kostner, B., Matteucci, G., Pilegaard, K., Schmidt,
M., Tenhunen, J., 2002. Deciduous forests: carbon and water
fluxes, balances and ecophysiological determinants. In: Valentini,
R. (Ed.), Fluxes of Carbon, Water and Energy of European Forests
Ecological Studies. Springer-Verlag, Berlin, p. 163.
Granier, A., Biron, P., Breda, N., Pontaillier, J.Y., Saugier, B., 1996.
Transpiration of trees and forest stands: short and long-term
monitoring using sapflow methods. Global Change Biol. 2,
263–274.
Granier, A., Breda, N., 1996. Modelling canopy conductance and
stand transpiration of an oak forest from sap flow measurements.
Ann. For. Sci. 53, 537–546.
Granier, A., Biron, P., Lemoine, D., 2000a. Water balance, transpira-
tion and canopy conductance in two beech stands. Agric. For.
Meteorol. 100, 291–308.
Granier, A., Breda, N., Biron, P., Villette, S., 1999. A lumped water
balance model to evaluate duration and intensity of drought
constraints in forest stands. Ecol. Model. 116, 269–283.
Granier, A., Ceschia, E., Damesin, C., Dufrene, E., Epron, D., Gross,
P., Lebaube, S., Ledantec, V., Le Goff, N., Lemoine, D., Lucot, E.,
Ottorini, J.M., Pontailler, J.Y., Saugier, B., 2000b. The carbon
balance of a young beech forest. Funct. Ecol. 14, 312–325.
Granier, A., Loustau, D., 1994. Measuring and modelling the tran-
spiration of a maritime pine canopy from sap-flow data. Agric. For.
Meteorol. 71, 61–81.
Granier, A., Loustau, D., Breda, N., 2000c. A generic model of forest
canopy conductance dependent on climate, soil water availability
and leaf area index. Ann. For. Sci. 57, 755–765.
Grassi, G., Vicinelli, E., Ponti, F., Cantoni, L., Magnani, F., 2005.
Seasonal and interannual variability of photosynthetic capacity in
relation leaf nitrogen in a deciduous forest plantation in northern
Italy. Tree Physiol. 25, 349–360.
Griffis, T.J., Black, T.A., Gaumont-Guay, D., Drewitt, G., Nesic, Z.,
Barr, A.G., Morgenstern, K., Kljun, N., 2004. Seasonal variation
and partitioning of ecosystem respiration in a southern boreal
aspen forest. Agric. For. Meteorol. 125, 207–223.
Grunwald, T., 2003. Langfristige Beobachtung von Kohlendioxid-
flussen mittels Eddy-Kovarianz-Technik uber einem Altfichtenbe-
stand im Tharandter Wald. Tharandter Klimaprotokolle 7, 146 p.
Grunzweig, J.M., Lin, T., Rotenberg, E., Schwartz, A., Yakir, D.,
2003. Carbon sequestration in arid-land forest. Global Change
Biol. 9, 791–799.
Hoff, C., Rambal, S., 2003. An examination of the interaction between
climate, soil and leaf area index in a Quercus ilex ecosystem. Ann.
For. Sci. 60, 153–161.
Hogberg, P., Nordgren, A., Buchmann, N., Taylor, A.F.S., Ekblad, A.,
Hogberg, M.N., Nyberg, G., Ottosson-Loffvenius, M., Readk,
D.J., 2001. Large-scale forest girdling shows that current photo-
synthesis drives soil respiration. Nature 411, 789–792.
Huxman, T.E., Smith, M.D., Fay, P.A., Knapp, A.K., Shaw, M.R., Loik,
M.E., Smith, S.D., Tissue, D.T., Zak, J.C., Weltin, J.F., Pockman,
W.T., Sala, O.E., Haddad, B.M., Harte, J., Koch, G.W., Scwinning,
S., Small, E.E., Williams, D.G., 2004. Convergence across biomes
to a common rain-use efficiency. Nature 419, 651–654.
IPCC, 2001. Climate change 2001: the scientific basis. http://
www.ipcc.ch/.
Innes, J.L., 1998. The impact of climatic extreme on forest: an
introduction. In: Beniston, Innes, (Eds.), The Impacts of Climate
Variability on Forests (Lecture Notes in Earth Sciences, vol. 74)
Springer, Berlin, pp. 1–18.
Irvine, J., Perks, M.P., Magnani, F., Grace, J., 1998. The response of
Pinus sylvestris to drought: stomatal control of transpiration and
hydraulic conductance. Tree Physiol. 18, 393–402.
Janssens, I.A., Lankreijer, H., Matteucci, G., Kowalski, A.S., Buch-
mann, N., Epron, D., Pilegaard, K., Kutsch, W., Longdoz, B.,
Grunwald, T., Montagnani, L., Dore, S., Rebmann, C., Moors, E.J.,
Grelle, A., Rannik, U., Morgenstern, K., Clement, R.,
Gu@mundsson, J., Minerbi, S., Berbigier, P., Ibrom, A., Moncrieff,
J., Aubinet, M., Bernhofer, C., Jensen, N.O., Vesala, T., Granier,
A., Schulze, E.D., Lindroth, A., Dolman, A.J., Jarvis, P.G., Ceule-
mans, R., Valentini, R., 2001. Productivity and disturbance over-
shadow temperature in determining soil and ecosystem respiration
across European forests. Global Change Biol. 7, 269–278.
Knohl, A., Schulze, E.D., Kolle, O., Buchmann, N., 2003. Large
carbon uptake by an unmanaged 250 year-old deciduous forest in
Central Germany. Agric. For. Meteorol. 118, 151–167.
Konopka, B., Curiel Yuste, J., Janssens, I.A., Ceulemans, R., 2005.
Comparison of fine root dynamics in Scots pine and Pedunculate
oak in sandy soil. Plant Soil 276, 33–45.
Korner, C., 2003. Carbon limitation in trees. J. Ecol. 91, 4–17.
Krishnan, P., Black, T.A., Grant, N.J., Barr, A.G., Hogg, E.H., Jassal,
R.S., Morgenstern, K., 2006. Impact of changing soil moisture
distribution on net ecosystem productivity of a boreal aspen forest
during and following drought. Agric. For. Meteorol. 139, 208–223.
A. Granier et al. / Agricultural and Forest Meteorology 143 (2007) 123–145144
Lagergren, F., Lindroth, A., 2002. Transpiration response to soil
moisture in pine and spruce trees in Sweden. Agric. For. Meteorol.
112, 67–85.
Law, B., Falge, E., Gu, L., Baldocchi, D.D., Bakwin, P., Berbigier, P.,
Davis, K.J., Dolman, A.J., Falk, M., Fuentes, J.D., Goldstein,
A.H., Granier, A., Grelle, A., Hollinger, D., Janssens, I.A., Jarvis,
P.G., Jensen, N.O., Katul, G., Mahli, Y., Matteucci, G., Meyers, T.,
Monson, R.K., Munger, J.W., Oechel, W., Olson, R., Pilegaard, K.,
Paw, U.K.T., Thorgeirsson, H., Valentini, R., Verma, S., Vesala, T.,
Wilson, K., Wofsy, S., 2002. Environmental controls over carbon
dioxide and water vapour exchange of terrestrial vegetation.
Agric. For. Meteorol. 113, 97–120.
Lawlor, D.W., 1998. Plant responses to global change: temperature
and drought stress. In: De Kok, L.J., Stulen, I. (Eds.), Responses
of Plant Metabolism to Air Pollution and Global Change. Back-
huys Publishers, Leiden, The Netherlands, pp. 193–208.
Lebourgeois, F., Breda, N., Ulrich, E., Granier, A., 2005. Climate-tree-
growth relationships of European beech (Fagus sylvatica L.) in the
French Permanent Plot Network (RENECOFOR). Trees 19, 385–
401.
Lebret, M., Nys, C., Forgeard, F., 2001. Litter production in an
Atlantic beech (Fagus sylvatica L.) time sequence. Ann. For.
Sci. 58, 755–768.
Le Dantec, V., Dufrene, E., Saugier, B., 2000. Interannual and spatial
variation in maximum leaf area index of temperate deciduous
stands. For. Ecol. Manage. 134, 71–81.
Leuschner, C., Backes, K., Hertel, D., Schipka, F., Schmitt, U.,
Tervorg, O., Runge, M., 2001. Drought responses at leaf, stem
and fine root levels of competitive Fagus sylvatica L. and Quercus
petraea (Matt.) Liebl. trees in dry and wet years. For. Ecol.
Manage. 149, 33–46.
Lieth, H., 1973. Primary production: terrestrial ecosystems. Human
Ecol. 1, 303–332.
Lindroth, A., Grelle, A., Moren, A.S., 1998. Long-term measurements
of boreal forest carbon balance reveal large temperature sensitiv-
ity. Global Change Biol. 4, 443–450.
Marcolla, B., Cescatti, A., Montagnani, L., Manca, G., Kerschbaumer,
G., Minerbi, S., 2005. Importance of advection in the atmospheric
CO2 exchanges of an alpine forest. Agric. For. Meteorol. 130, 193–
206.
Meehl, G.A., Tebaldi, C., 2004. More intense, more frequent, and
longer lasting heat waves in the 21st century. Science 305, 994–
997.
Meyers, T.P., 2001. A comparison of summertime water and CO2
fluxes over rangeland for well watered and drought conditions.
Agric. For. Meteorol. 106, 205–214.
Monteith, J.L., 1965. Evaporation and environment. In: Fogg, G.E.
(Ed.), The State and Movement of Water in Living Organisms.
Proc. XIX Symp. Soc. Exp. Biol. Cambridge University Press,
Cambridge, pp. 205–234.
Morgenstern, K., Black, T.A., Humphreys, E.R., Griffis, T.J., Drewitt,
G.B., Cai, T., Nesic, Z., Spittlehouse, D.L., Livingston, N.J., 2004.
Sensitivity and uncertainty of the carbon balance of a Pacific
Northwest Douglas-fir forest during an El Nino/La Nina cycle.
Agric. For. Meteorol. 123, 201–219.
Ngao, J., 2005. Determinism of ecosystem respiration in a beech
forest. Ph.D. Thesis, University Henri Poincare Nancy I, 147 p.
Papale, D., Reichstein, M., Canfora, E., Aubinet, M., Bernhofer, C.,
Longdoz, B., Kutsch, W., Rambal, S., Valentini, R., Vesala, T.,
Yakir, D., 2006. Towards a more harmonized processing of eddy
covariance CO2 fluxes: algorithms and uncertainty estimation.
Biogeosci. Discuss. 3, 961–992.
Pilegaard, K., Hummelshøi, P., Jensen, N.O., Chen, Z., 2001. Two
years of continuous CO2 eddy-flux measurements over a Danish
beech forest. Agric. For. Meteorol. 107, 29–41.
Rambal, S., 1984. Water balance and pattern of root water uptake by a
Quercus coccifera L. evergreen scrub. Oecologia 62, 18–25.
Rambal, S., Ourcival, J.M., Joffre, R., Mouillot, F., Nouvellon, Y.,
Reichstein, M., Rocheteau, A., 2003. Drought controls over con-
ductance and assimilation of a Mediterranean evergreen ecosystem:
scaling from leaf to canopy. Global Change Biol. 9, 1813–1824.
Rannik, U., Altimir, N., Raittila, J., Suni, T., Gaman, A., Hussein, T.,
Holtta, T., Lassila, H., Latokartano, M., Lauri, A., Natsheh, A.,
Petaja, T., Sorjamaa, R., Yla-Mella, H., Keronen, P., Berninger, F.,
Vesala, T., Hari, P., Kulmala, M., 2002. Fluxes of carbon dioxide
and water vapour over Scots pine forest and clearing. Agric. For.
Meteorol. 111, 187–202.
Rascher, U., Bobich, E.G., Lin, G.H., Walter, A., Morris, T., Naumann,
M., Nichol, C.J., Pierce, D., Bil, K., Kudeyarov, V., Berry, J.A.,
2004. Functional diversity of photosynthesis during drought in a
model tropical rainforest—the contributions of leaf area, photo-
synthetic electron transport and stomatal conductance to reduction
in net ecosystem carbon exchange. Plant Cell Environ. 27, 1239–
1256.
Rebetez, M., Mayer, H., Dupont, O., Schnindler, D., Gartner, K.,
Kropp, J., Menzel, A., 2006. Heat and drought 2003 in Europe: a
climate synthesis. Ann. For. Sci. 63, 569–577.
Reichstein, M., Ciais, P., Papale, D., Valentini, R., Running, S., Viovy,
N., Cramer, W., Granier, A., Ogee, J., Allard, V., Aubinet, M.,
Bernhofer, C., Buchmann, N., Carrara, A., Grunwald, T., Hei-
mann, M., Heinesch, B., Knohl, A., Kutsch, W., Loustau, D.,
Manca, G., Matteucci, G., Miglietta, F., Ourcival, J.M., Pilegaard,
K., Pumpanen, J., Rambal, S., Schaphoff, S., Seufert, G., Sous-
sana, J.F., Sanz, M.J., Zhao, M., 2006. Reduction of ecosystem
productivity and respiration during the European summer 2003
climate anomaly: a joint flux tower, remote sensing and modelling
analysis. Global Change Biol. 12, 1–18.
Reichstein, M., Falge, E., Baldocchi, D.D., Papale, D., Valentini, R.,
Aubinet, M., Berbigier, P., Bernhofer, C., Buchmann, N., Gilma-
nov, T., Granier, A., Grunwald, T., Havrankova, K., Janous, D.,
Knohl, A., Laurela, T., Lohila, A., Loustau, D., Matteucci, G.,
Meyers, T., Miglietta, F., Ourcival, J.M., Rambal, S., Rotenberg,
E., Sanz, M.J., Seufert, G., Vaccari, F., Vesala, T., Yakir, D., 2005.
On the separation of net ecosystem exchange into assimilation and
ecosystem respiration: review and improved algorithm. Global
Change Biol. 11, 1–16.
Reichstein, M., Rey, A., Freibauer, A., Tenhunen, J., Valentini, R.,
Banza, J., Casals, J., Cheng, Y., Grunzweig, J.M., Irvine, J., Joffre,
R., Law, B.E., Loustau, D., Miglietta, F., Oechel, W., Ourcival,
J.M., Pereira, J.S., Peressotti, A., Ponti, F., Qi, Y., Rambal, S.,
Rayment, M., Romanya, J., Rossi, F., Tedeschi, V., Tirone, G., Xu,
M., Yakir, D., 2003. Modelling temporal and large-scale spatial
variability of soil respiration from soil water availability, tem-
perature and vegetation productivity indices. Global Biogeochim.
Cycles 17 pp. 15/11-15/15, doi:10.1029/2003GB002035.
Reichstein, M., Tenhunen, J.D., Roupsard, O., Ourcival, J.M., Rambal,
S., Dore, S., Valentini, R., 2002a. Ecosystem respiration in two
Mediterranean evergreen Holm Oak forests: drought effects and
decomposition dynamics. Funct. Ecol. 16, 27–39.
Reichstein, M., Tenhunen, J.D., Roupsard, O., Ourcival, J.M., Rambal,
S., Miglietta, F., Peressotti, A., Pecchiari, M., Tirone, G., Valen-
tini, R., 2002b. Severe drought effects on ecosystem CO2 and H2O
fluxes at tree Mediterranean evergreen sites: revision of current
hypotheses? Global Change Biol. 8, 999–1017.
A. Granier et al. / Agricultural and Forest Meteorology 143 (2007) 123–145 145
Rodrigues, A., Pita, A., Mateus, J., 2005. Turbulent fluxes of carbon
dioxide and water vapour over an eucalyptus forest in Portugal.
Silva Lusitana 13, 169–180.
Saxe, H., Cannell, M.G.R., Johnsen, Ø., Ryan, M.G., Vourlitis, G.,
2001. Tree and forest functioning in response to global warming.
New Phytol. 149, 369–400.
Schar, C., Vidale, P.L., Luthi, D., Frei, C., Haberli, C., Mark, A.,
Liniger, M.A., Appenzeller, C., 2004. The role of increasing
temperature variability in European summer heatwaves. Nature
427, 332–336.
Scurlock, J.M.O., Olson, R.J., 2002. Terrestrial net primary produc-
tivity—a brief history and a new worldwide database. Environ.
Rev. 10, 91–109.
Stott, P.A., Stone, D.A., Allen, M.R., 2004. Human contribution to the
European heatwave of2004. Nature 432, 610–614.
Sturm, N., Kostner, B., Hartung, W., Tenhunen, J.D., 1998. Environ-
mental and endogenous controls on leaf- and stand-level water
conductance in a Scots pine plantation. Ann. For. Sci. 55, 237–
253.
Subke, J.A., Inglima, I., Cotrufo, M.F., 2006. Trends and methodo-
logical impacts in soil CO2 efflux partitioning: a meta-analytical
review. Global Change Biol. 12, 921–943.
Thornley, J.H.M., 1998. Dynamic model of leaf photosynthesis with
acclimation to light and nitrogen. Ann. Bot. 81, 421–430.
Tirone, G., Manca, G., Valentini, R., Seufert, G., 2003. Assorbimento
di carbonio negli ecosistemi forestali mediterranei: confronto tra
una lecceta ed una pineta. In: De Angelis, P., Macuz, A., Bucci,
G., Scarascia Mugnozza, G. (Eds.), Alberi e Foreste per il Nuovo
Millennio, Atti del III Congresso Nazionale della Societa Italiana
di Selvicoltura ed Ecologia Forestale (SISEF Atti III), IP/Office
2003. Antonini, Viterbo, pp. 99–104.
Vourlitis, G.L., Priante Filho, N., Hayashi, M.M.S., Nogueira, J.,
Caseiro, F.T., Holanda Campelo, J., 2001. Seasonal variations
in the net ecosystem CO2 exchange of a mature Amazonian
transitional tropical forest (cerradao). Funct. Ecol. 15, 388–395.
Wilson, K., Baldocchi, D.D., 2000. Seasonal and interannual varia-
bility of energy fluxes over a broadleaved temperate deciduous
forest in North America. Agric. For. Meteorol. 100, 1–18.
top related