Plant, Cell and Environment (1998) 21, 565–572
ORIGINAL ARTICLE
OA
220
EN
Changes of tree-ring δ 13C and water-use efficiency of beech
(Fagus sylvatica L.) in north-eastern France during the past
century
A. DUQUESNAY, 1 N. BRÉDA, 1 M. STIEVENARD 2 & J. L. DUPOUEY 1
1
Ecophysiology Unit, INRA-Nancy, 54280 Champenoux, France, and 2LMCE, CEA Saclay, 91191 Gif-sur-Yvette, France
ABSTRACT
We investigated variation in intrinsic water-use efficiency
during the past century by analysing δ 13C in tree rings of
beech growing in north-eastern France. Two different
silvicultural systems were studied: high forest and coppicewith-standards. We studied separately effects related to the
age of the tree at the time the ring was formed and effects
attributable to environmental changes. At young ages, δ 13C
shows an increase of more than 1‰. However, age-related
trends differ in high forest and coppice-with-standards.
Changes in microenvironmental variables during stand
maturation, and physiological changes related to structural
development of the trees with ageing, could explain these
results. During the past century, δ 13C in tree rings shows a
pattern of decline that is not paralleled by air δ 13C
changes. Isotopic discrimination has significantly
decreased from 18·1 to 16·4‰ in high forest and varied
insignificantly between 17·4 and 16·9‰ in coppice-withstandards. As a consequence, intrinsic water-use efficiency
has increased by 44% in high forest and 23% in coppicewith-standards during the past century. These results
accord with the increased water-use efficiency observed in
controlled experiments under a CO2-enriched atmosphere.
However, other environmental changes, such as nitrogen
deposition, may be responsible for such trends.
Key-words: Fagus sylvatica L., age; 13C/12C ratio; isotopic
discrimination; long-term trends; north-eastern France; silviculture; water-use efficiency.
INTRODUCTION
Elevated atmospheric CO2 concentration affects the gasexchange metabolism of trees in several ways. In controlled
experiments, CO2 assimilation is generally stimulated and
stomatal conductance reduced. As a consequence, wateruse efficiency (WUE), the ratio of carbon assimilated to
water transpired, increases markedly (Eamus & Jarvis
1989; Ceulemans & Mousseau 1994). If these results, usually obtained from young trees in short-term experiments,
Correspondence: J. L. Dupouey. Fax: 33 3 83 39 40 22; e-mail:
[email protected]
© 1998 Blackwell Science Ltd
can be extrapolated to the long term and to adult trees in
forest ecosystems, they could have important implications
for the global carbon cycle and the geographical range of
trees (Amthor 1995) and for the hydrological cycle
(Farquhar 1997).
This extrapolation is still a matter of speculation, partly
because of the lack of long-term field experiments to
examine tree responses to elevated atmospheric CO2.
However, the response to atmospheric CO2 increase during
the past century can be indirectly assessed using tree-rings
and herbarium samples.
Leaf stomatal density controls maximal values of stomatal conductance and therefore influences WUE. Herbarium
leaves of many tree species show an average reduction in
stomatal density over the past century (see Woodward &
Kelly 1995). For beech (Fagus sylvatica L.), different
trends have been observed, ranging from an increase of
6·3% to a decrease of 43% during the past 200 years
(Paoletti & Gellini 1993; Woodward & Kelly 1995).
The 13C/12C ratio also gives information about past
WUE variations. This ratio is expressed as δ13C, the proportional deviation from the international Peedee belemnite (PDB) carbonate standard (Craig 1957):
13 12
C/ Csample
δ13C (‰) = –––––––––––
– 1 × 1000 .
13 12
C/ CPDB
(
)
(1)
During carbon fixation, fractionation associated with physical and enzymatic processes causes plant matter to be 13Cdepleted in comparison with the air. This carbon isotopic
discrimination is expressed as
(δair – δplant)
∆ (‰) = ––––––––––– × 1000 .
(1000 + δplant)
(2)
The relative rates of carbon fixation and stomatal conductance are the primary factors determining ∆. According to
the model proposed by Farquhar, O’Leary & Berry (1982),
∆ (‰) = a + (b – a)(Ci/Ca)
(3)
13
where a is the discrimination against CO2 during CO2 diffusion through the stomata (a = 4·4‰, O’Leary 1981), b is
the discrimination associated with carboxylation (b = 27‰,
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A. Duquesnay et al.
566
Farquhar & Richards 1984) and Ci and Ca are intercellular
and ambient CO2 concentrations.
Given Fick’s law:
A = gCO (Ca – Ci),
(4)
2
where A is the net photosynthesis, measured as CO2
uptake, and gCO2 is the leaf conductance to CO2, and given
that gH2O, the leaf conductance to water vapour is 1·6gCO2,
∆ can be related to the ratio A/gH2O by
1.6 A
∆ (‰) = a + (b – a) (1 – ––– –––– ) .
Ca gH O
(5)
2
A/gH O is called intrinsic WUE (Osmond, Bjorkman &
Anderson 1980). It is a component of plant transpiration
efficiency, the long-term expression of biomass gain with
respect to water loss at the level of the whole plant.
Peñuelas & Azcón-Bieto (1992) observed that isotopic
discrimination ∆ of herbarium leaves of Mediterranean trees
has decreased by 1‰ and thus intrinsic WUE has increased
during the past four decades. Woodward (1993), also using
herbarium leaves, showed that the intrinsic WUE of eight
temperate tree species has increased by 30% since 1930.
A few results have been obtained by investigating δ13C in
tree rings. Feng & Epstein (1995) showed a significant intrinsic WUE increase for four species over the past century.
Likewise, Bert, Leavitt & Dupouey (1997) observed a 30%
increase in the intrinsic WUE of Abies alba Mill. between
1930 and 1980. Conversely Marshall & Monserud (1996)
showed homoeostasis for WUE in several species of conifer
between the beginning and the end of the century. Almost all
such observations have been made in coniferous species.
In the present study, we investigated intrinsic WUE
changes during the past century in a deciduous species,
beech, growing in the Lorrain plain. A previous dendrochronological study (Badeau et al. 1995) had shown an
increasing long-term growth trend during this period.
Furthermore, growth trends depend on silvicultural system
and stand density. Therefore in our study we took separate
samples from high forest and coppice-with-standards.
Finally, key factors in such long-term studies are the confounding effects of environmental changes and tree or stand
ageing. Wood formed during the first years of tree life is generally depleted in 13C in comparison with wood formed later
(Francey & Farquhar 1982; Bert, Leavitt & Dupouey 1997),
a phenomenon called ‘age effect’ or ‘juvenile effect’. The
corresponding δ13C increase varies around 1·5‰. However,
the reported time span of this increase is highly variable:
from the first 20 years of tree life (Freyer 1979) to 215 years
(Mazany, Lerman & Long 1980). In our study, we devised a
sampling scheme to study separately this age effect and longterm trends attributable to external environmental factors.
2
MATERIALS AND METHODS
Sampling strategy
The study was carried out in the calcareous plateaux of
Lorrain (north-eastern France), where the climate is
intermediate between continental and atlantic. The average
annual rainfall is 730 mm and the average annual temperature 9·7 °C.
We sampled separately two types of silvicultural system:
high stands and coppice-with-standards (Fig. 1). In the first
system, stands are of even age and trees experience a high
level of competition during their life. The second system is
characterized by two different strata that develop differently: the coppice, growing from stumps, which is clearcut every 25–30 years, and a few high trees, the standards,
which grow from seeds, initially within the coppice, then
above the coppice, at low density. The standards are harvested after several rotations of the coppice, roughly every
150 years.
Cores used in the present study were selected from a
larger set of cores previously collected for a dendroecological study (Badeau et al. 1995). In this previous study,
102 sites with similar ecological characteristics (topography, soil, vegetation, microclimate) and free from any fertilization had been sampled. Ten trees, selected among the
dominants in high stands and the standards in coppicewith-standards, had been cored to the pith at breast height
in each site (one core per tree). A total of 1025 trees had
been sampled.
Tree-age effect on isotopic discrimination
To avoid any effect of long-term environmental changes,
we chose tree rings formed between 1965 and 1974 but by
trees of different cambial ages (the age of the tree when the
ring was formed). Eleven 10-year age classes were studied:
Figure 1. Stand-structure changes along a silvicultural rotation in
(a) high stands and (b) coppice-with-standards. In high stands,
trees pass through a juvenile stage (1) and an adult stage (2). In
coppice-with-standards two strata initially coexist: the coppice
(cross-hatching) and the standards (1); then, every 25–30 years, the
coppice is clear cut (2).
© 1998 Blackwell Science Ltd, Plant, Cell and Environment, 21, 565–572
Water-use efficiency of beech over the past century
5–14 years, 15–24 years, etc. Ten-ring sequences were
pooled and analysed together to limit the influence of particular climatic events. The 1965–1974 decade was chosen
for two reasons: a large number of rings were available for
this decade, and it was characterized by a low water stress
level (Fig. 2). Drought reduces beech isotopic discrimination (Dupouey et al. 1993; Saurer, Siegenthaler &
Schweingruber 1995) and we wanted to limit possible
interactions between age and drought effects.
Long-term changes of isotopic discrimination
In this part of the work, we analysed tree rings formed
between 1850 and 1990, pooled by 10-year sequences.
Only tree-rings formed at 38–47 years of age in high stands
and 43–52 years of age in coppice-with-standards were
studied to avoid the age effect. We selected these age
classes because a large number of rings were available and
because a juvenile effect has been observed on radial
growth curves below 40 years of age (Picard 1995).
For each of the previously chosen age and date classes,
10 trees were selected according to their history: by looking at individual radial growth curves, we discarded trees
in which growth had been supressed at any time. Site
effects were limited by choosing the 10 trees from different
locations. For each selected tree, the chosen tree-ring
sequence was set by counting from the pith, then excised
from the core with a razor blade.
Stable carbon isotope analysis
The holocellulose fraction was extracted from the tree-ring
samples before carbon isotope analysis to avoid the effects
of radial translocation of carbon (Tans, de Jong & Mook
1978) or varying proportions of wood compounds (Park &
Epstein 1961; Wilson & Grinsted 1977; Benner et al. 1987).
Ten-ring sequences were ground in a mill, and subsequently boiled for 10 h in a soxhlet with 2:1 toluene:ethanol,
567
then with 100% ethanol for the same time. The treated
wood was then boiled in deionized water and bleached in
acetic acid solution at 70 °C to which sodium hypochlorite (NaClO2) was added to decompose the lignin
(Leavitt & Danzer 1993). Holocellulose was obtained by
soaking samples in sodium hydroxide (17%, 1 h) then in
acetic acid (10%, 10 min) following Da Silveira &
Sternberg (1989).
Holocellulose was combusted to CO2 at 500 °C in sealed
evacuated Pyrex tubes containing precombusted copper
oxide as the oxygen source (Sofer 1980). The CO2 was
separated from other combustion products by cryogenic
distillation. The 13C/12C ratio was measured with a
Finnigan Mat 252 mass spectrometer.
Calculation of ∆, Ci and WUE — error estimation
∆, Ci and A/gH2O were calculated using Eqns 2, 3 and 5,
respectively.
For Eqn 2, we collected published values for air δ13C
from ice-core measurements (Friedli et al. 1986), direct
atmospheric measurements (Keeling, Mook & Tans 1979;
Keeling, Carter & Mook 1984; Keeling et al. 1989; Leavitt
& Long 1989) and inferred from C4 plants (Marino &
McElroy 1991).
For Eqns (3) and (5), we used atmospheric CO2 concentrations collected from ice-core data (Neftel et al. 1985;
Raynaud & Barnola 1985; Friedli et al. 1986; Pearman
et al. 1986; Staffelbach, Stauffer & Sigg 1991) and direct
atmospheric measurements (Keeling et al. 1979; Mook
et al. 1983; Keeling et al. 1984; Fraser, Elliot & Waterman
1986; Friedli et al. 1987; Keeling et al. 1989; Leavitt &
Long 1989; Keeling & Whorf 1991).
For the study of tree-age effects, we used air δ13C and Ca
values of the 1970 decade (average of values between 1964
and 1975) for the calculation of ∆, Ci and A/g.
Meteorological data from the Nancy station were used
for the calculation of potential evapotranspiration (PET),
according to the Penman equation.
Two types of error were estimated: (1) the error associated with holocellulose combustion and mass-spectrometer
measurements, which was assessed by repeated analysis of
a laboratory standard extracted from a beech-wood sample
from Lorrain; (2) the error associated with our sampling
design. For the latter purpose, in one case (1970 decade),
the 10 tree-ring sequences of one batch were separately
analysed. This error term, which also includes the type (1)
error, was used to assess the significance of long-term δ13C
variations.
RESULTS
Error estimation
Figure 2. Annual cumulated soil water deficit indices calculated
for a typical beech stand of the Lorrain plateau, cumulated by
decades. Indices have been calculated using a daily water balance
model (Bréda 1994), with climatic data from the meteorological
station of Nancy-Tomblaine (Météo France).
© 1998 Blackwell Science Ltd, Plant, Cell and Environment, 21, 565–572
Repeated combustion and analysis of the reference cellulose gave a confidence interval of ± 0·09‰ (P < 0·05,
n = 24). Within the 1970 decade, the standard deviation of
the 10 samples was 0·48‰ for high stands (SEM ± 0·15‰,
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A. Duquesnay et al.
n = 10) and 1·11‰ for coppice-with-standards (SEM ±
0·35‰, n = 10). The corresponding SEMs of ∆, Ci and A/g
for high stands and coppice-with-standards were, respectively: ± 0·16‰ and ± 0·36‰; ± 2·3 cm3 m−3 and
± 5·2 cm3 m−3; and ± 1·4 µmol mol-1 and ± 3·3 µmol mol–1.
Age effect
δ13C variations according to age for high stands and coppice-with-standards are shown in Fig. 3. There is a clear
difference between the two silvicultural systems: for
high stands, δ13C increases from – 24·5‰ to – 23·25‰
from 10 to 50 years of age and then up to 140 years gradually decreases to its initial value. For coppice-withstandards, δ13C values increase from – 24·75‰ to
– 23·5‰ from 20 to 80 years of age and then remain relatively constant up to 140 years. Thus, the increase of
δ13C in the first stage of life shows a lag of 30 years
between high forest and coppice-with-standards.
Furthermore, δ13C variations in high stands are larger
than the confidence interval, whereas δ13C variations in
coppice-with-standards are smaller than the confidence
interval.
Variations during the past century
Variations of air δ13C and tree δ13C values during the
past century are shown in Fig. 4(a). δ13C values vary
between – 23·2 and – 24·3‰. Both long-term, low-frequency variations and short-term, interdecade variations
are observed.
Simple or multiple regression of these latter high-frequency variations upon climatic variables (temperature,
precipitation and potential evapotranspiration) gave only
loose relationships (r = 0·38, n = 10, not significant, for
the correlation between ∆ and precipitation minus potential evapotranspiration averaged by decades). The waterstress effect on δ13C variations is therefore probably
smoothed at the decade level and was not factored out in
subsequent analyses.
Figure 3. Variations in δ13C according to age for high forest (l)
and coppice-with-standards (¡). Corresponding A/g-values are
shown on the right-hand y-axis.
In addition to these variations at the decade level, longterm trends were apparent. Tree-ring δ13C values did not
follow the decreasing atmospheric δ13C trend during the
past century. They even increased in high forest between
1880 and 1920.
Consequently, isotopic discrimination ∆ significantly
decreased in high forest with time (r = 0·74, P < 0·05,
n = 12), from 18·1 to 16·4‰ (Fig. 4b). In coppice-withstandards, there was no clear trend with time and values
varied insignificantly between 16·6 and 17·9‰. The Ci/Ca
ratio, which is a linear function of ∆, followed the same
patterns.
In both silvicultural systems, Ci has significantly
increased, by 20 cm3 m−3, since the beginning of the century (Fig. 4c). Variations of intrinsic WUE are shown in
Fig. 4(d). Intrinsic WUE shows a strong positive trend during the study period. A/g has increased by 44% in high
stands and 23% in coppice-with-standards. This increase is
statistically significant in both type of stand.
DISCUSSION
Age effect
Our results confirm the existence of an age effect on δ13C,
often also called the juvenile effect. Values increase by 1‰
during the first stage of life in both high forest and coppicewith-standards, but the timing of this age effect differs
between the two systems. This age effect may be attributed
to two different causes: changes in microenvironmental
variables during stand maturation, and physiological
changes linked to tree structural development.
During stand maturation, canopy height, leaf area and
tree density change. At the young stage, small trees may
assimilate more soil-respired, and therefore isotopically
lighter, CO2 (Vogel 1978; Sternberg et al. 1989). It has also
been shown that δ13C increases with an increase in vapour
pressure difference (Farquhar, Ehleringer & Hubick 1989)
or irradiance (Francey & Farquhar 1982; Collet et al. 1993;
Zimmerman & Ehleringer 1990), two factors that change
as trees grow.
The above mechanisms could explain the observed
increase of δ13C with age in our stands. The 30-year lag
between the increase in high-stands δ13C values and the
increase in coppice-with-standards values could be
explained by the fact that, in coppice-with-standards, trees
destined to become standards are sheltered by the existing
standards and compete with the dense coppice for
25–30 years. Thus, during the first stage of their life, coppice-with-standards trees grow in a more humid and probably CO2-enriched environment, and at a lower irradiance
level. For older trees, a reverse situation is observed: in
coppice-with-standards, old trees grow isolated in an open
stand, whereas the tree density in high stands is high and
the canopy closed. Indeed Buchmann, Kao & Ehleringer
(1997) observed a stronger vertical gradient of air CO2 and
δ13C in more closed broadleaved canopy compared with
more open stands, leading to more negative leaf δ13C
© 1998 Blackwell Science Ltd, Plant, Cell and Environment, 21, 565–572
Water-use efficiency of beech over the past century
569
Figure 4. Changes during the past century in (a) δ13C, (b) isotopic discrimination ∆, (c) Ci and (d) A/g for high forest (l) and coppicewith-standards (¡). Air δ13C values and atmospheric CO2 concentrations are shown, respectively, on the right y-axis of graphs (a) and (c).
Standard errors of the means associated with the 1970 decade are shown for high forest and coppice-with-standards by the solid and
dotted lines, respectively.
© 1998 Blackwell Science Ltd, Plant, Cell and Environment, 21, 565–572
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A. Duquesnay et al.
values. Leavitt (1993) observed that wood δ13C was higher
in open-canopy stands than in closed-canopy stands.
However, the decrease of δ13C in old high stands remains
to be explained.
Variations of hydraulic conductance linked with tree
ageing and branch elongation have also been shown to
modify leaf gas exchanges and thus plant δ13C. Younger
trees have shorter branches and therefore more negative
tree-ring or leaf δ13C values (Waring & Silvester 1994;
Yoder et al. 1994; Panek & Waring 1995; Panek 1996).
However, these relationships were obtained only with
coniferous species. Fagus sylvatica has a more complex
structure, characterized by a balance between short and
long internodes, and this balance is the key factor in
hydraulic conductance variability in ring-porous species
such as Fraxinus excelsior L. or Fagus sylvatica (Cochard
et al. 1997). The relationships in these species between the
variations of internode length and δ13C changes with age
warrant further investigation.
Polley et al. (1993, 1996) gave experimental evidence of the
existence of a large positive effect on WUE of CO2 increase
from subambient level. In addition to these short-term gasexchange adjustments to elevated CO2, slow adaptative processes could also have enhanced WUE. The decrease during
the past century in leaf stomatal density observed on herbarium leaves could by itself explain the concomitant WUE
increase (Woodward 1993; Kürschner 1996).
Other environmental factors, such as nitrogen supply,
could also play a part in the observed trends. Nitrogen
deposition has increased markedly in the studied area during the past decades (Ulrich & Williot 1993). Guehl, Fort &
Ferhi (1995) observed that WUE assessed by gas-exchange
measurements increases when nitrogen supply is optimum
for maritime pine. Högberg, Johannisson & Hällgren
(1993) observed a 1·4‰ decrease in ∆ in pine needles after
nitrogen fertilization. However, Mitchell & Hinckley
(1993), in Douglas fir, found no difference in instantaneous
WUE with high and low levels of nitrogen supply.
Long-term changes
CONCLUSION
Our results are in agreement with those of Peñuelas &
Azcón-Bieto (1992), Woodward (1993), Ehleringer &
Cerling (1995), Feng & Epstein (1995) and Bert et al.
(1997), who reported similar decreases of isotopic discrimination ∆ or increases of WUE during the same period,
using historical records in leaves or wood. Our results also
accord with predicted values of WUE increase obtained
from a gas-exchange model of the effect of current environnemental changes (Beerling 1994). In all previous studies, the Ci/Ca ratio remained constant or decreased during
the past century. Our results do not support the hypothesis
of a regulation of either Ci or Ci/Ca, at least in the long
term. However, Marshall & Monserud (1996) observed an
increase of Ci/Ca since the beginning of the century for
three coniferous species in the western USA, and hence
homoeostasis in WUE. Marshall & Monserud compared
two groups of 10-ring sequences, one at the beginning of
the century, and one at the end of the century. Our study has
shown a large interdecade variability of δ13C, which could
hide long-term trends.
Results obtained in controlled experiments suggest that
the trend of increasing WUE that we observed could be
attributable to the increase in atmospheric CO2 concentration. This effect has been well documented for many woody
plant species (see Ceulemans & Mousseau 1994) and is one
of the most pronounced responses to elevated CO2. For
Fagus sylvatica, Overdieck & Forstreuter (1994) demonstrated improved WUE in saplings growing at elevated CO2
concentration. Using branch-bags, Dufrêne, Pontailler &
Saugier (1993) also observed an increase in WUE in
branches of 20-year-old beech trees. This effect is generally
the result of an increase in assimilation rate and a decrease in
stomatal conductance (but see Heath & Kerstiens 1997).
These experimental results were obtained at ambient and
twice-ambient CO2 concentration, whereas the trees we
studied grew at CO2 concentrations of 290–360 cm3 cm−3.
The aim of the present study was to examine variations of
δ13C and intrinsic WUE during the past century. Our
results show that isotopic discrimination ∆ has decreased
significantly. Intrinsic WUE has increased by 44% in high
stands over the past century. These results, obtained from a
sample of adult forest trees, are consistent with observations on the consequences for young plants in controlled
conditions of an increase in atmospheric CO2 concentration. However, the observed changes cannot be atributed to
this single cause, because of the many other factors
involved. Moreover, complex patterns in the variation of
δ13C with tree age show that isotopic values cannot be
simply compared at different tree ages.
Few in situ studies of δ13C long-term trends have been
carried out in forest ecosystems, and trends in isotopic discrimination (∆) and WUE over the past century observed
by different authors do not all correspond. Further studies
are needed, with other species and in other biomes.
ACKNOWLEDGMENTS
We thank P. Behr for technical assistance during the field
work, and V. Lenoble for valuable suggestions during the
preparation of isotope samples. We are also grateful to V.
Badeau and J. M. Guehl for helpful discussions and
comments, and to C. Powell for correcting the English of
the manuscript.
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Received 26 September 1997; received in revised form 18 February
1998; accepted for publication 18 February 1998
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