Directory UMM :Data Elmu:jurnal:T:Tree Physiology:Vol16.1996:
Tree Physiology 16, 389--396
© 1996 Heron Publishing----Victoria, Canada
Ecophysiological responses of woody plants to past CO 2 concentrations
DAVID J. BEERLING
Department of Animal and Plant Sciences, University of Sheffield, Sheffield S10 2TN, U.K.
Received May 10, 1995
Summary An approach is detailed for calculating historical
rates of CO2 uptake and water loss of leaves from measurements of leaf δ13C composition and climatic information. This
approach was applied to investigate leaf gas exchange metabolism of woody taxa during the past 200 years of atmospheric
CO2 increase and in response to the longer-term atmospheric
CO2 increases plants experienced over the Pleistocene. Reconstructed net assimilation rates and water use efficiencies increased in response to increasing atmospheric CO2
concentrations in both sets of material, whereas stomatal conductance, showing the combined responses of changes in stomatal density and leaf assimilation rates, was generally less
responsive. Woody temperate taxa maintained a nearly constant ci /ca ratio in response to the increase in atmospheric CO2
concentrations over both timescales, in part, as a result of
changes in stomatal density. The reconstructed leaf-scale
physiological responses to past global climatic and atmospheric change corroborated those anticipated from experimental work indicating the adequate capacity of experiments, at
least at the scale of individual leaves, to predict plant responses
to future environmental change.
Keywords: assimilation rate, climate change, CO2 uptake, leaf
δ13C composition, Pinus flexilis, Salix herbacea stomatal conductance, water use efficiency.
Introduction
The possible impact of predicted future atmospheric CO2 increases on plants and ecosystems is being investigated by the
coordinated development of global vegetation modeling and
ecophysiological experimental research programs (Steffen et
al. 1992). Equally important, however, is an understanding of
how leaf photosynthesis and transpiration have responded to
past CO2 increases (Beerling and Woodward 1993). This objective is being pursued through paleoecophysiology. The paleoecophysiological approach investigates changes in leaf
morphology, especially stomatal density (Woodward 1987,
Beerling et al. 1993b, Van de Water et al. 1994), and water use
efficiency, based on stable carbon isotope composition (δ13C)
(Peñuelas and Azcón-Bieto 1992, Beerling et al. 1993a, Beerling and Woodward 1993, Woodward 1993, Ehleringer and
Cerling 1995) from historical collections of leaves.
Paleoecophysiology can now be extended further to investigate leaf-scale fluxes of CO2 and water vapor in the past. There
is a sound theoretical basis for relating leaf gas exchange
processes to leaf δ13C composition (Farquhar et al. 1982,
Farquhar et al. 1989). After accounting for the isotopic fractionations associated with diffusion and enzymatic reactions,
leaf δ13C composition is determined principally by the ratio of
intercellular (ci ) to ambient CO2 concentrations (ca), representing a time-integrated measure of CO2 uptake and water
loss (Ehleringer 1993). Changes in the concentration of atmospheric CO2 and 13C/12C ratio have been reported from ice core
studies (Friedli et al. 1986, Neftel et al. 1988, Leuenberger et
al. 1992), and the isotope fractionation associated with diffusion and enzymatic reactions has been determined experimentally (see Farquhar and Lloyd 1993). Consequently, it is now
possible to extract values of ci directly from historical sequences of leaves analyzed for δ13C. To reconstruct CO2 uptake
rates of leaves growing in the past requires δ13C-derived ci
values to be fed into a mechanistic biochemical model of
photosynthesis (Farquhar et al. 1980) that can be used, in
conjunction with appropriate climatic information, to drive an
empirical model of leaf stomatal conductance to water vapor
(Ball et al. 1987). This new approach differs from that of
Beerling (1994) in that rates of CO2 uptake and water loss from
leaves are constrained by δ13C composition and are not entirely
dependent on climate (see Schemes A and B, Figure 1). The
central aim of the present work is to understand the effects of
long-term changes in global climate and atmospheric composition on the exchange of CO2 and water vapor by leaves.
The new approach has been applied to two historical sequences of leaves (Beerling et al. 1993a, 1993b, Van de Water
et al. 1994). The first set is a collection of herbarium leaves of
the woody dwarf shrub Salix herbacea L. (dwarf willow) that
spans the past two centuries during which a rapid increase in
atmospheric CO2 concentration occurred (Friedli et al. 1986).
The second set covers a longer time sequence, 30,000 years,
and provides a history of leaf metabolism of Pinus flexilis
James. (limber pine) during the Pleistocene (Van de Water et
al. 1994). During this period, ice core studies have revealed
major changes in the concentration of atmospheric CO2 (Neftel
et al. 1988, Leuenberger et al. 1992) with low glacial concentrations of about 200 ppm and higher concentrations of about
280 ppm in the early Holocene.
390
BEERLING
Materials and methods
Wj =
Theory
Leaf stable carbon isotope composition, δ13Cp, is controlled by
gas exchange according to (Farquhar et al. 1982):
δ 13 Cp = δ 13 ca − a − (b − a)(ci/ca),
(1)
where a and b are fractionation constants due to diffusion
through the stomata (4.4) and net CO2 fixation by Rubisco
(29), respectively, δ13ca is the 13C/12C ratio of atmospheric CO2
concentration, ca is the ambient CO2 partial pressure, and ci is
the intercellular CO2 partial pressure. When δ13ca and ca are
both known, Equation 1 can be solved for ci as:
ci =
−(δ13 cp − δ 13 ca + a)
.
b/ca − a/ca
(2)
The isotopically derived value of ci is next fed into the
Farquhar et al. (1980) biochemical model of leaf photosynthesis. According to the model, leaf photosynthesis is described
by:
Jci
.
O
4ci +
τ
Light dependency of the model is achieved through its effects
on electron transport according to:
J=
αI
0.5O
min(W c,W j) − Rd ,
τci
Vmax ci
,
O
c i + K c 1 +
Ko
,
(6)
where Jmax is the maximum rate of electron transport, α is the
efficiency of light conversion on an incident light basis (mol
electrons per mol photons) (0.24), and I is the photosynthetically active radiation (PAR) (µmol m −2 s −1). The temperature
responses of Kc, Ko, τ, Vmax and Jmax described by Harley et al.
(1992) have been used.
Equations 1--6 provide a theoretical framework for estimating leaf net assimilation rates from δ13C composition. From the
CO2 uptake rate (A, µmol m −2 s −1), the response of stomatal
conductance is predicted, after modification by environmental
conditions (Ball et al. 1987, Leuning 1990, Aphalo and Jarvis
1993), as follows:
glAH
,
(ca − Γ)
(7)
(3)
where A is net leaf photosynthetic rate (µmol CO2 m −2 s −1), ci
and O are the partial pressures of CO2 and O2 in the intercellular leaf space, respectively, Wc and Wj are the rates of carboxylation-limited Rubisco (ribulose-1,5-bisphosphate (RuBP)
carboxylase/oxygenase) activity and RuBP regeneration by
electron transport, respectively, Rd is the rate of CO2 release in
the light resulting from processes other than photorespiration,
and τ is the specificity of Rubisco.
Because it is uncertain whether Rubisco activity or electron
transport is limiting photosynthesis when dealing with historical values of δ13C-ci, two leaf photosynthetic rates are calculated, one limited by Rubisco activity and the other limited by
RuBP regeneration through electron transport, and according
to Equation 3, the minimum of the two is chosen.
Rubisco activity limits the carboxylation rate according to:
Wc =
0.5
α 2 I2
1 +
Jmax 2
g s = go +
A = 1 −
(5)
where gs is the stomatal conductance to water vapor (mmol
m −2 s −1), go is the stomatal conductance when A is zero at the
light compensation point, g1 is an empirical sensitivity coefficient, H is the relative humidity (%) of the air surrounding the
leaf, ca is the atmospheric CO2 concentration (Pa), and Γ is the
CO2 compensation point (Pa). Both go and g1 have the temperature responses and constraints reported by Woodward et al.
(1995), and Γ has a temperature response general to plants with
a C3 photosynthetic pathway (Leuning 1990). The term (ca −
Γ), in the denominator of Equation 7, improves the responses
of stomatal conductance to low CO2 concentrations (Leuning
1990), appropriate for simulations under low glacial CO2 concentrations; however, there remain problems with some of the
responses of Equation 7, particularly to relative humidity
(Aphalo and Jarvis 1993). Note that a known value of ci
permits the calculation of the gas exchange rates of the plants
directly rather than requiring the iterative procedure adopted
when the value of ci is unknown (Scheme A versus Scheme B,
Figure 1).
(4)
where Vmax is the maximum rate of carboxylation, and Kc and
Ko are the Michaelis-Menten constants for carboxylation and
oxygenation, respectively.
The rate of carboxylation when limited solely by the rate of
RuBP regeneration in the Calvin cycle, Wj, is mediated through
the rate of electron transport (J):
Historical collections of leaf material
Two sets of species-specific material were used to reconstruct
the historical gas exchange responses of plants to past CO2
variations. The first set, of the woody dwarf shrub S. herbacea,
was collected from similar altitudes in southern Sweden over
the past 200 years and stored in the herbarium of the Swedish
Natural History Museum, Stockholm. Leaf δ13C values and
stomatal density have been reported by Beerling et al. (1993a,
1993b, respectively). Leaves were sampled from flowering
ECOPHYSIOLOGICAL RESPONSES OF WOODY PLANTS TO CO2
391
Figure 1. Schematic representation of
two approaches for reconstructing the
past gas exchange characteristic of vegetation. In Scheme A, the approach is dependent on climate and is essentially an
unconstrained modeling approach requiring iterative calculations of gas exchange parameters (see Beerling 1994
for details). The second approach
(Scheme B), and the one employed in
the present work, extracts a value of ci
from leaf δ13C measurements.
shoots on the assumption that they had developed in saturating
irradiance, consequently the PAR value (I, Equation 6) was set
at 1500 µmol m −2 s −1. The maximum rates of Rubisco activity,
Vmax (Equation 4), and electron transport, Jmax (Equation 5),
for S. herbacea were assigned after Beerling and Quick (1995)
for tundra vegetation. Records of atmospheric CO2 and δ13ca
were taken from ice core studies (Friedli et al. 1986) and from
the continuous monitoring record at Mauna Loa, Hawaii
(Keeling and Whorf 1994). Climate inputs (temperature and
humidity) used in the model (Figure 1B) were the 30-year
averages reported for the site nearest the collection locality
(Müller 1982).
The continuous Pleistocene sequence of leaf δ13C composition for the conifer P. flexilis reported by Van de Water et al.
(1994) provides the second set of material investigated for gas
exchange reconstructions. Assigned values of Vmax and Jmax
were typical of cool/cold conifer forests (Beerling and Quick
1995). Because the irradiance each needle was exposed to over
its lifetime is unknown and dependent on its position within
the canopy, the value of I (Equation 6) was set at 1500 µmol
m −2 s −1. Site selection was made by Van de Water et al. (1994)
to minimize changes in vapor pressure deficit, temperature and
water availability over the past 30,000 years, and to focus
attention only on the effects of changing CO2 concentrations.
This was achieved by developing the Holocene section of the
30,000-year chronology from needles recovered in middens at
sites in southern Idaho, near the lower limits of P. flexilis. The
modern floras and temperatures of these sites closely approximate the glacial floras and temperatures of the more southerly
sites, as determined from packrat midden studies (Betancourt
et al. 1990). This rationale parallels that frequently used in
palaeoecology where the modern climate of one site approximates the palaeoclimate of the glacial sites. On this basis, Van
de Water et al. (1994) considered that variations in precipitation and average annual temperatures were minimized. Estimates of present-day temperatures and humidity needed for the
model were based on the present climate of the region (Müller
1982), and I used the ice core records of CO2 and δ13ca de-
scribed by Beerling (1994).
Results
Leaf-scale photosynthetic rates, reconstructed from δ13C
measurements, for the dwarf shrub S. herbacea showed a
gradual increase over the past two centuries (Figure 2A),
whereas stomatal conductance declined over this time. Overall, the changes in CO2 and water vapor fluxes led to a steady
increase in water use efficiency (Figure 2C).
Solving Equation 2 with the detailed Siple Station ice core
record (Friedli et al. 1986) showed that the increase in photosynthetic rates of S. herbacea leaves was brought about by an
increase in the average concentration of CO2 inside the leaf (ci)
(Figure 3A). The increase in ci was proportional to the atmospheric CO2 increases recorded at Mauna Loa, such that the ci /ca
ratio increased only slightly (Figure 3B).
Longer-term historical gas exchange reconstructions based
on fossil δ13C measurements and Equations 1--7 indicated
increasing photosynthetic rates of needles of P. flexilis over the
past 30,000 years (Figure 4A). Fluxes of water vapor showed
a more ambiguous trend and large variations particularly between 15,000--20,000 years BP (Figure 4B), a time when the
ice cores record the major CO2 increase from glacial to interglacial concentrations (Leuenberger et al. 1992). As with
S. herbacea, the responses of photosynthesis and stomatal
conductance at the leaf-scale led to a steady and marked
increase in water use efficiency (Figure 4C), driven primarily
by the intercellular CO2 concentration of the leaf tracking
atmospheric concentrations (Figure 5A) in a nearly proportional manner (Figure 5B).
Discussion
Experiments in which woody plants and C3 annuals were
grown in the pre-industrial CO2 concentration (280 ppm) demonstrated lower leaf photosynthetic rates and higher leaf stomatal conductances (Woodward 1987, 1993, Overdieck 1989,
392
BEERLING
Figure 3. Calculated (A) intercellular CO2 concentrations (ci) (r =
0.79, P < 0.01) and (B) ratio of intercellular to ambient CO2 concentration (ci /ca) (r = 0.48, P < 0.05) of leaves of Salix herbacea over the
past 200 years.
Figure 2. Reconstructed trends in (A) photosynthetic rates (r = 0.81,
P < 0.01), (B) stomatal conductance (r = 0.41, P < 0.05) and (C) water
use efficiency (r = 0.97, P < 0.05) of leaves of the woody dwarf shrub
Salix herbacea growing in southern Sweden over the past 200 years of
CO2 increase. The reconstructions are based on δ13C-derived ci values
used in a biochemical model of leaf photosynthesis and an empirical
model of stomatal conductance.
Polley et al. 1992a, 1992b, Tissue et al. 1995) compared with
plants growing at the present CO2 concentration of 350 ppm.
The historical reconstructions of leaf gas exchange responses
for the woody shrub S. herbacea are in accordance with these
experimental data, i.e., they showed an overall increase in leaf
photosynthetic rates of 23% (Figure 2A), a decrease in stomatal conductance of about 6%, and a steady increase in leaf
water use efficiency over the past two centuries (Figure 2C).
Whether this photosynthetic stimulation will be sustained by
S. herbacea as the CO2 concentration continues to rise appears
to depend on an increase in air temperatures enhancing nutrient supply rates from the soil (Oechel et al. 1994).
Ehleringer and Cerling (1995) suggested that the ci /ca ratio
has remained nearly constant with increasing CO2 concentration over the past 200 years, because ci tracks atmospheric
concentrations. The 200-year time series of δ13C measurements of S. herbacea support this idea (Figure 3A), although a
small increase in the value of ci /ca from 0.59 to 0.65 was
evident (Figure 3B). This contrasts with the pattern obtained
from an analysis of a 100-year sequence of Prosopis alba
leaves collected from the Atacama desert in northern Chile
(Ehleringer et al. 1992, Ehleringer and Cerling 1995). In this
system, leaves growing in an increasing atmospheric CO2
concentration over the 100-year period had a constant ci /ca
ratio but a decreasing ci value, suggesting constant photosynthetic rates but an increasing water use efficiency (Ehleringer
and Cerling 1995). These contrasting sets of results may reflect
the different climates in which the plants grew (boreal versus
desert), or differences in the sensitivity of stomatal conductance and stomatal density to CO2 increases, or both.
One possible mechanism operating to maintain a constant
ci /ca ratio in leaves in response to increasing CO2 concentrations is a decrease in stomatal density (Ehleringer and Cerling
1995). In the case of S. herbacea, the small increase in ci /ca
(Figure 3) can be considered against a 60% decrease in leaf
stomatal density over the past two centuries (Beerling et al.
1993b). Woodward (1987) reported that the stomatal density
of temperate arboreal species decreased by 40% in response to
CO2 increases over the same time leading to the expectation
that these temperate species would show a rising value of ci and
ECOPHYSIOLOGICAL RESPONSES OF WOODY PLANTS TO CO2
393
Figure 5. Calculated (A) intercellular CO2 concentrations (ci ) and (B)
ratio of intercellular to ambient CO2 concentration (ci /ca) of needles
of Pinus flexilis over the past 30,000 years.
Figure 4. Reconstructed trends in (A) photosynthetic rates, (B) stomatal conductance and (C) water use efficiency of leaves of Pinus
flexilis growing in southern USA during the last deglaciation. The
reconstructions are based on δ13C-derived ci values extracted from the
data of Van de Water et al. (1994).
a constant ci/ca ratio over this time. Extracting values of ci
(Equation 2) and ci /ca from reported δ13C measurements of the
same material showed a rising value of ci and a constant ci /ca
ratio over time (Figures 6A and 6B). However, despite these
two sets of supporting evidence, it is clear that a decrease in
stomatal density is not a prerequisite for regulating a nearly
constant ci /ca ratio. Malone et al. (1993) reported no significant
decrease in stomatal density of C3 crop plants over a CO2
concentration gradient of 200--350 ppm, yet the isotopically
derived gas exchange responses revealed a near-constant ci /ca
ratio (Polley et al. 1993a).
Measurements of the stable carbon isotope composition of
fossilized needles of P. flexilis from the Pleistocene permit an
investigation of the fluxes of CO2 and water vapor, regulated
by stomata, over a wider CO2 range than the increase plants
have experienced since the pre-industrial era and over a considerably longer timescale (Neftel et al. 1988, Leuenberger et
al. 1992). In agreement with experimental data obtained from
studies in which annual plants were grown at glacial and
present CO2 concentrations (Polley et al. 1993a, 1993b, Tissue
et al. 1995, Dippery et al. 1995), reconstructed photosynthetic
rates of P. flexilis needles were lower during glacial times
relative to the present day (Figure 5A). Similar observations
have been reported for ponderosa pine growing across an
altitudinal gradient (Callaway et al. 1994), indicating that
P. flexilis may have responded similarly during the last glaciation. However, leaf stomatal conductance to water vapor
showed no major decrease in response to the CO2 increase
from 180 to 290 ppm (Figure 5B), in agreement with a previous modeling study (Beerling 1994), as a result of the combined effect of changes in stomatal density and photosynthetic
rates over the past 30,000 years. The relative responses of
photosynthesis, stomatal conductance and stomatal density all
contribute to a linear increase in water use efficiency with
increasing CO2 concentration, as has been observed in experimental studies (Polley et al. 1993a, 1993b, Tissue et al. 1995).
Values of ci gradually increased over the past 30,000 years so
that ci /ca was maintained at a near-constant value (Figure 6A
and 6B). Accompanying this response, the stomatal density of
P. flexilis needles from the same sites and of the same ages
decreased (Van de Water et al. 1994). Collectively these data
provide evidence that stomatal density has had a regulatory
role in maintaining a near-constant ci /ca ratio over a much
longer timescale than previously reported (Ehleringer and Cer-
394
BEERLING
Figure 6. Calculated (A) intercellular CO2 concentrations (ci ) (r =
0.49, P < 0.05) and (B) ratio of intercellular to ambient CO2 concentration (ci /ca) (r = 0.37, P < 0.05) of leaves of the woody species
Carpinus betulus, Fagus sylvatica, Populus nigra, Quercus petraea,
Quercus robur, Tilia cordata and Alnus glutinosa growing in Cambridge over the past 200 years (recalculated from the original data of
Woodward 1993).
ling 1995).
Global atmospheric CO2 concentrations rose rapidly during
the deglaciation and apparently induced oscillatory gas exchange behavior in P. flexilis needles (Figures 4 and 5). Stability seems to have been achieved when the atmospheric CO2
concentration reached values of about 290 ppm in the early
Holocene. Fluctuations in leaf gas exchange 15,000--20,000
years BP are not readily explained by an increased number of
sampling localities at this time (see Table 1 in Van de Water et
al. 1994), and the extent of the oscillations is greater than the
background noise in the samples. Therefore, it is possible that
either the metabolism of the P. flexilis needles took some time
to achieve homeostatic adjustment to the increase in atmospheric CO2 concentration, or that the effect was associated
with the switch in the global climate system from a glacial to
an interglacial state (Lautenschlager and Herterich 1990). If
the latter explanation is true, then these low-frequency oscillations show the coupling of cool, dry conifer forests in the
western USA with changing regional atmospheric circulation
patterns, representing a previously unreported phenomenon of
plant responses to environmental change during the deglaciation.
The historical gas exchange reconstructions described here
are presented with two important caveats. First, because ci was
derived from leaf δ13C composition, it represents an average
value over the lifetime of the leaf (Ehleringer 1993). This
leads, in turn, to the reconstruction of average photosynthetic
rates, rather than maximum values under optimum conditions.
Furthermore, the reconstructed absolute photosynthetic rates
depend on the chosen values of Vmax and Jmax , and both values
can be influenced by CO2 and temperature. Temperature dependence of the values was included in the model and predicted on the basis of the polynomial responses given by
McMurtrie and Wang (1993), whereas the direct influence of
CO2 on Vmax and Jmax was not explicitly modeled. The values
of Vmax and Jmax used in the calculations were determined at
the present ambient CO2 concentration of 350 ppm (Beerling
and Quick 1995). Tissue et al. (1995) found that growth of the
C3 annual Abutilon theophrasti Medic. at low glacial CO2
concentrations resulted in a measurable reduction in Vmax and
Jmax relative to plants grown at the present ambient CO2 concentration. However, studies on trees grown in elevated CO2
concentrations generally show a decrease in Vmax and Jmax ,
although a variety of responses have been reported (Gunderson
and Wullschleger 1994). Further observations are needed to
provide the detail required to model the influence of CO2 on
Vmax and Jmax accurately.
The second caveat is that experiments designed to simulate
plant growth at low glacial CO2 concentrations can never fully
represent how plants grew under glacial conditions because
modern genotypes are unlikely to be representative of those
prevailing during the last, or previous, glaciations (Beerling
and Woodward 1993). However, the approach outlined here
offers a basis for reconstructing the gas exchange responses of
plants utilizing the genotypes that existed at that time and
allows comparison with the responses of modern genotypes in
current experiments.
An approach has been presented for reconstructing past rates
of leaf CO2 uptake and water loss of leaves from leaf δ13C
composition and climate. The approach has been applied to
leaf collections of the dwarf shrub S. herbacea spanning the
past 200 years of CO2 increase and to Pleistocene sequences of
fossilized needles of P. flexilis. Both taxa showed historical gas
exchange responses to CO2 increases similar to those anticipated on the basis of experimental results. The maintenance of
a near-constant ci /ca ratio in response to increasing CO2 concentrations on both time scales was achieved, at least in part,
by a decrease in stomatal density. I conclude that leaf-level
plant responses to future global change can be reasonably
predicted in an experimental context.
Acknowledgments
I thank Ian Woodward for comments and discussion on the manuscript
and gratefully acknowledge funding of this work through the Royal
Society.
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© 1996 Heron Publishing----Victoria, Canada
Ecophysiological responses of woody plants to past CO 2 concentrations
DAVID J. BEERLING
Department of Animal and Plant Sciences, University of Sheffield, Sheffield S10 2TN, U.K.
Received May 10, 1995
Summary An approach is detailed for calculating historical
rates of CO2 uptake and water loss of leaves from measurements of leaf δ13C composition and climatic information. This
approach was applied to investigate leaf gas exchange metabolism of woody taxa during the past 200 years of atmospheric
CO2 increase and in response to the longer-term atmospheric
CO2 increases plants experienced over the Pleistocene. Reconstructed net assimilation rates and water use efficiencies increased in response to increasing atmospheric CO2
concentrations in both sets of material, whereas stomatal conductance, showing the combined responses of changes in stomatal density and leaf assimilation rates, was generally less
responsive. Woody temperate taxa maintained a nearly constant ci /ca ratio in response to the increase in atmospheric CO2
concentrations over both timescales, in part, as a result of
changes in stomatal density. The reconstructed leaf-scale
physiological responses to past global climatic and atmospheric change corroborated those anticipated from experimental work indicating the adequate capacity of experiments, at
least at the scale of individual leaves, to predict plant responses
to future environmental change.
Keywords: assimilation rate, climate change, CO2 uptake, leaf
δ13C composition, Pinus flexilis, Salix herbacea stomatal conductance, water use efficiency.
Introduction
The possible impact of predicted future atmospheric CO2 increases on plants and ecosystems is being investigated by the
coordinated development of global vegetation modeling and
ecophysiological experimental research programs (Steffen et
al. 1992). Equally important, however, is an understanding of
how leaf photosynthesis and transpiration have responded to
past CO2 increases (Beerling and Woodward 1993). This objective is being pursued through paleoecophysiology. The paleoecophysiological approach investigates changes in leaf
morphology, especially stomatal density (Woodward 1987,
Beerling et al. 1993b, Van de Water et al. 1994), and water use
efficiency, based on stable carbon isotope composition (δ13C)
(Peñuelas and Azcón-Bieto 1992, Beerling et al. 1993a, Beerling and Woodward 1993, Woodward 1993, Ehleringer and
Cerling 1995) from historical collections of leaves.
Paleoecophysiology can now be extended further to investigate leaf-scale fluxes of CO2 and water vapor in the past. There
is a sound theoretical basis for relating leaf gas exchange
processes to leaf δ13C composition (Farquhar et al. 1982,
Farquhar et al. 1989). After accounting for the isotopic fractionations associated with diffusion and enzymatic reactions,
leaf δ13C composition is determined principally by the ratio of
intercellular (ci ) to ambient CO2 concentrations (ca), representing a time-integrated measure of CO2 uptake and water
loss (Ehleringer 1993). Changes in the concentration of atmospheric CO2 and 13C/12C ratio have been reported from ice core
studies (Friedli et al. 1986, Neftel et al. 1988, Leuenberger et
al. 1992), and the isotope fractionation associated with diffusion and enzymatic reactions has been determined experimentally (see Farquhar and Lloyd 1993). Consequently, it is now
possible to extract values of ci directly from historical sequences of leaves analyzed for δ13C. To reconstruct CO2 uptake
rates of leaves growing in the past requires δ13C-derived ci
values to be fed into a mechanistic biochemical model of
photosynthesis (Farquhar et al. 1980) that can be used, in
conjunction with appropriate climatic information, to drive an
empirical model of leaf stomatal conductance to water vapor
(Ball et al. 1987). This new approach differs from that of
Beerling (1994) in that rates of CO2 uptake and water loss from
leaves are constrained by δ13C composition and are not entirely
dependent on climate (see Schemes A and B, Figure 1). The
central aim of the present work is to understand the effects of
long-term changes in global climate and atmospheric composition on the exchange of CO2 and water vapor by leaves.
The new approach has been applied to two historical sequences of leaves (Beerling et al. 1993a, 1993b, Van de Water
et al. 1994). The first set is a collection of herbarium leaves of
the woody dwarf shrub Salix herbacea L. (dwarf willow) that
spans the past two centuries during which a rapid increase in
atmospheric CO2 concentration occurred (Friedli et al. 1986).
The second set covers a longer time sequence, 30,000 years,
and provides a history of leaf metabolism of Pinus flexilis
James. (limber pine) during the Pleistocene (Van de Water et
al. 1994). During this period, ice core studies have revealed
major changes in the concentration of atmospheric CO2 (Neftel
et al. 1988, Leuenberger et al. 1992) with low glacial concentrations of about 200 ppm and higher concentrations of about
280 ppm in the early Holocene.
390
BEERLING
Materials and methods
Wj =
Theory
Leaf stable carbon isotope composition, δ13Cp, is controlled by
gas exchange according to (Farquhar et al. 1982):
δ 13 Cp = δ 13 ca − a − (b − a)(ci/ca),
(1)
where a and b are fractionation constants due to diffusion
through the stomata (4.4) and net CO2 fixation by Rubisco
(29), respectively, δ13ca is the 13C/12C ratio of atmospheric CO2
concentration, ca is the ambient CO2 partial pressure, and ci is
the intercellular CO2 partial pressure. When δ13ca and ca are
both known, Equation 1 can be solved for ci as:
ci =
−(δ13 cp − δ 13 ca + a)
.
b/ca − a/ca
(2)
The isotopically derived value of ci is next fed into the
Farquhar et al. (1980) biochemical model of leaf photosynthesis. According to the model, leaf photosynthesis is described
by:
Jci
.
O
4ci +
τ
Light dependency of the model is achieved through its effects
on electron transport according to:
J=
αI
0.5O
min(W c,W j) − Rd ,
τci
Vmax ci
,
O
c i + K c 1 +
Ko
,
(6)
where Jmax is the maximum rate of electron transport, α is the
efficiency of light conversion on an incident light basis (mol
electrons per mol photons) (0.24), and I is the photosynthetically active radiation (PAR) (µmol m −2 s −1). The temperature
responses of Kc, Ko, τ, Vmax and Jmax described by Harley et al.
(1992) have been used.
Equations 1--6 provide a theoretical framework for estimating leaf net assimilation rates from δ13C composition. From the
CO2 uptake rate (A, µmol m −2 s −1), the response of stomatal
conductance is predicted, after modification by environmental
conditions (Ball et al. 1987, Leuning 1990, Aphalo and Jarvis
1993), as follows:
glAH
,
(ca − Γ)
(7)
(3)
where A is net leaf photosynthetic rate (µmol CO2 m −2 s −1), ci
and O are the partial pressures of CO2 and O2 in the intercellular leaf space, respectively, Wc and Wj are the rates of carboxylation-limited Rubisco (ribulose-1,5-bisphosphate (RuBP)
carboxylase/oxygenase) activity and RuBP regeneration by
electron transport, respectively, Rd is the rate of CO2 release in
the light resulting from processes other than photorespiration,
and τ is the specificity of Rubisco.
Because it is uncertain whether Rubisco activity or electron
transport is limiting photosynthesis when dealing with historical values of δ13C-ci, two leaf photosynthetic rates are calculated, one limited by Rubisco activity and the other limited by
RuBP regeneration through electron transport, and according
to Equation 3, the minimum of the two is chosen.
Rubisco activity limits the carboxylation rate according to:
Wc =
0.5
α 2 I2
1 +
Jmax 2
g s = go +
A = 1 −
(5)
where gs is the stomatal conductance to water vapor (mmol
m −2 s −1), go is the stomatal conductance when A is zero at the
light compensation point, g1 is an empirical sensitivity coefficient, H is the relative humidity (%) of the air surrounding the
leaf, ca is the atmospheric CO2 concentration (Pa), and Γ is the
CO2 compensation point (Pa). Both go and g1 have the temperature responses and constraints reported by Woodward et al.
(1995), and Γ has a temperature response general to plants with
a C3 photosynthetic pathway (Leuning 1990). The term (ca −
Γ), in the denominator of Equation 7, improves the responses
of stomatal conductance to low CO2 concentrations (Leuning
1990), appropriate for simulations under low glacial CO2 concentrations; however, there remain problems with some of the
responses of Equation 7, particularly to relative humidity
(Aphalo and Jarvis 1993). Note that a known value of ci
permits the calculation of the gas exchange rates of the plants
directly rather than requiring the iterative procedure adopted
when the value of ci is unknown (Scheme A versus Scheme B,
Figure 1).
(4)
where Vmax is the maximum rate of carboxylation, and Kc and
Ko are the Michaelis-Menten constants for carboxylation and
oxygenation, respectively.
The rate of carboxylation when limited solely by the rate of
RuBP regeneration in the Calvin cycle, Wj, is mediated through
the rate of electron transport (J):
Historical collections of leaf material
Two sets of species-specific material were used to reconstruct
the historical gas exchange responses of plants to past CO2
variations. The first set, of the woody dwarf shrub S. herbacea,
was collected from similar altitudes in southern Sweden over
the past 200 years and stored in the herbarium of the Swedish
Natural History Museum, Stockholm. Leaf δ13C values and
stomatal density have been reported by Beerling et al. (1993a,
1993b, respectively). Leaves were sampled from flowering
ECOPHYSIOLOGICAL RESPONSES OF WOODY PLANTS TO CO2
391
Figure 1. Schematic representation of
two approaches for reconstructing the
past gas exchange characteristic of vegetation. In Scheme A, the approach is dependent on climate and is essentially an
unconstrained modeling approach requiring iterative calculations of gas exchange parameters (see Beerling 1994
for details). The second approach
(Scheme B), and the one employed in
the present work, extracts a value of ci
from leaf δ13C measurements.
shoots on the assumption that they had developed in saturating
irradiance, consequently the PAR value (I, Equation 6) was set
at 1500 µmol m −2 s −1. The maximum rates of Rubisco activity,
Vmax (Equation 4), and electron transport, Jmax (Equation 5),
for S. herbacea were assigned after Beerling and Quick (1995)
for tundra vegetation. Records of atmospheric CO2 and δ13ca
were taken from ice core studies (Friedli et al. 1986) and from
the continuous monitoring record at Mauna Loa, Hawaii
(Keeling and Whorf 1994). Climate inputs (temperature and
humidity) used in the model (Figure 1B) were the 30-year
averages reported for the site nearest the collection locality
(Müller 1982).
The continuous Pleistocene sequence of leaf δ13C composition for the conifer P. flexilis reported by Van de Water et al.
(1994) provides the second set of material investigated for gas
exchange reconstructions. Assigned values of Vmax and Jmax
were typical of cool/cold conifer forests (Beerling and Quick
1995). Because the irradiance each needle was exposed to over
its lifetime is unknown and dependent on its position within
the canopy, the value of I (Equation 6) was set at 1500 µmol
m −2 s −1. Site selection was made by Van de Water et al. (1994)
to minimize changes in vapor pressure deficit, temperature and
water availability over the past 30,000 years, and to focus
attention only on the effects of changing CO2 concentrations.
This was achieved by developing the Holocene section of the
30,000-year chronology from needles recovered in middens at
sites in southern Idaho, near the lower limits of P. flexilis. The
modern floras and temperatures of these sites closely approximate the glacial floras and temperatures of the more southerly
sites, as determined from packrat midden studies (Betancourt
et al. 1990). This rationale parallels that frequently used in
palaeoecology where the modern climate of one site approximates the palaeoclimate of the glacial sites. On this basis, Van
de Water et al. (1994) considered that variations in precipitation and average annual temperatures were minimized. Estimates of present-day temperatures and humidity needed for the
model were based on the present climate of the region (Müller
1982), and I used the ice core records of CO2 and δ13ca de-
scribed by Beerling (1994).
Results
Leaf-scale photosynthetic rates, reconstructed from δ13C
measurements, for the dwarf shrub S. herbacea showed a
gradual increase over the past two centuries (Figure 2A),
whereas stomatal conductance declined over this time. Overall, the changes in CO2 and water vapor fluxes led to a steady
increase in water use efficiency (Figure 2C).
Solving Equation 2 with the detailed Siple Station ice core
record (Friedli et al. 1986) showed that the increase in photosynthetic rates of S. herbacea leaves was brought about by an
increase in the average concentration of CO2 inside the leaf (ci)
(Figure 3A). The increase in ci was proportional to the atmospheric CO2 increases recorded at Mauna Loa, such that the ci /ca
ratio increased only slightly (Figure 3B).
Longer-term historical gas exchange reconstructions based
on fossil δ13C measurements and Equations 1--7 indicated
increasing photosynthetic rates of needles of P. flexilis over the
past 30,000 years (Figure 4A). Fluxes of water vapor showed
a more ambiguous trend and large variations particularly between 15,000--20,000 years BP (Figure 4B), a time when the
ice cores record the major CO2 increase from glacial to interglacial concentrations (Leuenberger et al. 1992). As with
S. herbacea, the responses of photosynthesis and stomatal
conductance at the leaf-scale led to a steady and marked
increase in water use efficiency (Figure 4C), driven primarily
by the intercellular CO2 concentration of the leaf tracking
atmospheric concentrations (Figure 5A) in a nearly proportional manner (Figure 5B).
Discussion
Experiments in which woody plants and C3 annuals were
grown in the pre-industrial CO2 concentration (280 ppm) demonstrated lower leaf photosynthetic rates and higher leaf stomatal conductances (Woodward 1987, 1993, Overdieck 1989,
392
BEERLING
Figure 3. Calculated (A) intercellular CO2 concentrations (ci) (r =
0.79, P < 0.01) and (B) ratio of intercellular to ambient CO2 concentration (ci /ca) (r = 0.48, P < 0.05) of leaves of Salix herbacea over the
past 200 years.
Figure 2. Reconstructed trends in (A) photosynthetic rates (r = 0.81,
P < 0.01), (B) stomatal conductance (r = 0.41, P < 0.05) and (C) water
use efficiency (r = 0.97, P < 0.05) of leaves of the woody dwarf shrub
Salix herbacea growing in southern Sweden over the past 200 years of
CO2 increase. The reconstructions are based on δ13C-derived ci values
used in a biochemical model of leaf photosynthesis and an empirical
model of stomatal conductance.
Polley et al. 1992a, 1992b, Tissue et al. 1995) compared with
plants growing at the present CO2 concentration of 350 ppm.
The historical reconstructions of leaf gas exchange responses
for the woody shrub S. herbacea are in accordance with these
experimental data, i.e., they showed an overall increase in leaf
photosynthetic rates of 23% (Figure 2A), a decrease in stomatal conductance of about 6%, and a steady increase in leaf
water use efficiency over the past two centuries (Figure 2C).
Whether this photosynthetic stimulation will be sustained by
S. herbacea as the CO2 concentration continues to rise appears
to depend on an increase in air temperatures enhancing nutrient supply rates from the soil (Oechel et al. 1994).
Ehleringer and Cerling (1995) suggested that the ci /ca ratio
has remained nearly constant with increasing CO2 concentration over the past 200 years, because ci tracks atmospheric
concentrations. The 200-year time series of δ13C measurements of S. herbacea support this idea (Figure 3A), although a
small increase in the value of ci /ca from 0.59 to 0.65 was
evident (Figure 3B). This contrasts with the pattern obtained
from an analysis of a 100-year sequence of Prosopis alba
leaves collected from the Atacama desert in northern Chile
(Ehleringer et al. 1992, Ehleringer and Cerling 1995). In this
system, leaves growing in an increasing atmospheric CO2
concentration over the 100-year period had a constant ci /ca
ratio but a decreasing ci value, suggesting constant photosynthetic rates but an increasing water use efficiency (Ehleringer
and Cerling 1995). These contrasting sets of results may reflect
the different climates in which the plants grew (boreal versus
desert), or differences in the sensitivity of stomatal conductance and stomatal density to CO2 increases, or both.
One possible mechanism operating to maintain a constant
ci /ca ratio in leaves in response to increasing CO2 concentrations is a decrease in stomatal density (Ehleringer and Cerling
1995). In the case of S. herbacea, the small increase in ci /ca
(Figure 3) can be considered against a 60% decrease in leaf
stomatal density over the past two centuries (Beerling et al.
1993b). Woodward (1987) reported that the stomatal density
of temperate arboreal species decreased by 40% in response to
CO2 increases over the same time leading to the expectation
that these temperate species would show a rising value of ci and
ECOPHYSIOLOGICAL RESPONSES OF WOODY PLANTS TO CO2
393
Figure 5. Calculated (A) intercellular CO2 concentrations (ci ) and (B)
ratio of intercellular to ambient CO2 concentration (ci /ca) of needles
of Pinus flexilis over the past 30,000 years.
Figure 4. Reconstructed trends in (A) photosynthetic rates, (B) stomatal conductance and (C) water use efficiency of leaves of Pinus
flexilis growing in southern USA during the last deglaciation. The
reconstructions are based on δ13C-derived ci values extracted from the
data of Van de Water et al. (1994).
a constant ci/ca ratio over this time. Extracting values of ci
(Equation 2) and ci /ca from reported δ13C measurements of the
same material showed a rising value of ci and a constant ci /ca
ratio over time (Figures 6A and 6B). However, despite these
two sets of supporting evidence, it is clear that a decrease in
stomatal density is not a prerequisite for regulating a nearly
constant ci /ca ratio. Malone et al. (1993) reported no significant
decrease in stomatal density of C3 crop plants over a CO2
concentration gradient of 200--350 ppm, yet the isotopically
derived gas exchange responses revealed a near-constant ci /ca
ratio (Polley et al. 1993a).
Measurements of the stable carbon isotope composition of
fossilized needles of P. flexilis from the Pleistocene permit an
investigation of the fluxes of CO2 and water vapor, regulated
by stomata, over a wider CO2 range than the increase plants
have experienced since the pre-industrial era and over a considerably longer timescale (Neftel et al. 1988, Leuenberger et
al. 1992). In agreement with experimental data obtained from
studies in which annual plants were grown at glacial and
present CO2 concentrations (Polley et al. 1993a, 1993b, Tissue
et al. 1995, Dippery et al. 1995), reconstructed photosynthetic
rates of P. flexilis needles were lower during glacial times
relative to the present day (Figure 5A). Similar observations
have been reported for ponderosa pine growing across an
altitudinal gradient (Callaway et al. 1994), indicating that
P. flexilis may have responded similarly during the last glaciation. However, leaf stomatal conductance to water vapor
showed no major decrease in response to the CO2 increase
from 180 to 290 ppm (Figure 5B), in agreement with a previous modeling study (Beerling 1994), as a result of the combined effect of changes in stomatal density and photosynthetic
rates over the past 30,000 years. The relative responses of
photosynthesis, stomatal conductance and stomatal density all
contribute to a linear increase in water use efficiency with
increasing CO2 concentration, as has been observed in experimental studies (Polley et al. 1993a, 1993b, Tissue et al. 1995).
Values of ci gradually increased over the past 30,000 years so
that ci /ca was maintained at a near-constant value (Figure 6A
and 6B). Accompanying this response, the stomatal density of
P. flexilis needles from the same sites and of the same ages
decreased (Van de Water et al. 1994). Collectively these data
provide evidence that stomatal density has had a regulatory
role in maintaining a near-constant ci /ca ratio over a much
longer timescale than previously reported (Ehleringer and Cer-
394
BEERLING
Figure 6. Calculated (A) intercellular CO2 concentrations (ci ) (r =
0.49, P < 0.05) and (B) ratio of intercellular to ambient CO2 concentration (ci /ca) (r = 0.37, P < 0.05) of leaves of the woody species
Carpinus betulus, Fagus sylvatica, Populus nigra, Quercus petraea,
Quercus robur, Tilia cordata and Alnus glutinosa growing in Cambridge over the past 200 years (recalculated from the original data of
Woodward 1993).
ling 1995).
Global atmospheric CO2 concentrations rose rapidly during
the deglaciation and apparently induced oscillatory gas exchange behavior in P. flexilis needles (Figures 4 and 5). Stability seems to have been achieved when the atmospheric CO2
concentration reached values of about 290 ppm in the early
Holocene. Fluctuations in leaf gas exchange 15,000--20,000
years BP are not readily explained by an increased number of
sampling localities at this time (see Table 1 in Van de Water et
al. 1994), and the extent of the oscillations is greater than the
background noise in the samples. Therefore, it is possible that
either the metabolism of the P. flexilis needles took some time
to achieve homeostatic adjustment to the increase in atmospheric CO2 concentration, or that the effect was associated
with the switch in the global climate system from a glacial to
an interglacial state (Lautenschlager and Herterich 1990). If
the latter explanation is true, then these low-frequency oscillations show the coupling of cool, dry conifer forests in the
western USA with changing regional atmospheric circulation
patterns, representing a previously unreported phenomenon of
plant responses to environmental change during the deglaciation.
The historical gas exchange reconstructions described here
are presented with two important caveats. First, because ci was
derived from leaf δ13C composition, it represents an average
value over the lifetime of the leaf (Ehleringer 1993). This
leads, in turn, to the reconstruction of average photosynthetic
rates, rather than maximum values under optimum conditions.
Furthermore, the reconstructed absolute photosynthetic rates
depend on the chosen values of Vmax and Jmax , and both values
can be influenced by CO2 and temperature. Temperature dependence of the values was included in the model and predicted on the basis of the polynomial responses given by
McMurtrie and Wang (1993), whereas the direct influence of
CO2 on Vmax and Jmax was not explicitly modeled. The values
of Vmax and Jmax used in the calculations were determined at
the present ambient CO2 concentration of 350 ppm (Beerling
and Quick 1995). Tissue et al. (1995) found that growth of the
C3 annual Abutilon theophrasti Medic. at low glacial CO2
concentrations resulted in a measurable reduction in Vmax and
Jmax relative to plants grown at the present ambient CO2 concentration. However, studies on trees grown in elevated CO2
concentrations generally show a decrease in Vmax and Jmax ,
although a variety of responses have been reported (Gunderson
and Wullschleger 1994). Further observations are needed to
provide the detail required to model the influence of CO2 on
Vmax and Jmax accurately.
The second caveat is that experiments designed to simulate
plant growth at low glacial CO2 concentrations can never fully
represent how plants grew under glacial conditions because
modern genotypes are unlikely to be representative of those
prevailing during the last, or previous, glaciations (Beerling
and Woodward 1993). However, the approach outlined here
offers a basis for reconstructing the gas exchange responses of
plants utilizing the genotypes that existed at that time and
allows comparison with the responses of modern genotypes in
current experiments.
An approach has been presented for reconstructing past rates
of leaf CO2 uptake and water loss of leaves from leaf δ13C
composition and climate. The approach has been applied to
leaf collections of the dwarf shrub S. herbacea spanning the
past 200 years of CO2 increase and to Pleistocene sequences of
fossilized needles of P. flexilis. Both taxa showed historical gas
exchange responses to CO2 increases similar to those anticipated on the basis of experimental results. The maintenance of
a near-constant ci /ca ratio in response to increasing CO2 concentrations on both time scales was achieved, at least in part,
by a decrease in stomatal density. I conclude that leaf-level
plant responses to future global change can be reasonably
predicted in an experimental context.
Acknowledgments
I thank Ian Woodward for comments and discussion on the manuscript
and gratefully acknowledge funding of this work through the Royal
Society.
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