Review Article
242
Direct and Indirect Climate Change Effects
on Photosynthesis and Transpiration
M. U. F. Kirschbaum1,2
1
CSIRO Forestry and Forest Products, P.O. Box 4008, Kingston ACT 2604, Australia
2
CRC for Greenhouse Accounting, P.O. Box 475, Canberra ACT 2601, Australia
Received: February 6, 2004; Accepted: March 26, 2004
Abstract: Climate change affects plants in many different ways.
Increasing CO2 concentration can increase photosynthetic rates.
This is especially pronounced for C3 plants, at high temperatures
and under water-limited conditions. Increasing temperature also affects photosynthesis, but plants have a considerable ability
to adapt to their growth conditions and can function even at extremely high temperatures, provided adequate water is available. Temperature optima differ between species and growth
conditions, and are higher in elevated atmospheric CO2. With increasing temperature, vapour pressure deficits of the air may increase, with a concomitant increase in the transpiration rate
from plant canopies. However, if stomata close in response to increasing CO2 concentration, or if there is a reduction in the diurnal temperature range, then transpiration rates may even decrease. Soil organic matter decomposition rates are likely to be
stimulated by higher temperatures, so that nutrients can be
more readily mineralised and made available to plants. This is
likely to increase photosynthetic carbon gain in nutrient-limited
systems. All the factors listed above interact strongly so that, for
different combinations of increases in temperature and CO2 concentration, and for systems in different climatic regions and primarily affected by water or nutrient limitations, photosynthesis
must be expected to respond differently to the same climatic
changes.
Key words: CO2, C3, photosynthesis, C4 photosynthesis, diurnal
temperature, Rubisco, RuBP, stomata, temperature.
Abbreviations:
RuBP:
ribulose-1,5,-bisphosphate
Rubisco: RuBP carboxylase/oxygenase
Introduction
Photosynthesis is intimately tied to climatic conditions, both
directly and indirectly. While light absorption is independent
of temperature, the subsequent steps in converting light into
chemical energy respond to temperature in complex ways. In
C3 plants, the uptake of CO2 by Rubisco is the first step in pho-
Plant Biology 6 (2004): 242 – 253
© Georg Thieme Verlag KG Stuttgart · New York
ISSN 1435-8603 · DOI 10.1055/s-2004-820883
tosynthetic CO2 assimilation, and Rubisco is not saturated with
CO2 at normal intercellular CO2 concentrations. Both CO2 and
O2 also compete for access to the active sites on Rubisco, with
increasing CO2 favouring carboxylations at the expense of oxygenations, so that an increasing proportion of reducing and
phosphorylation potentials can be channelled towards CO2 fixation.
Indirect effects of climate change may ultimately be even more
important. Plants require an aqueous medium in their cells,
and photosynthetic function is impaired when plant water status falls below critical values. Plants could maintain an aqueous internal environment by closing their stomata and minimising water loss by fully surrounding their leaves by a cuticular epidermis that allows only minor rates of water loss.
However, stomatal closure would also prevent the diffusive
entry of CO2 into photosynthesising cells. On-going water loss
is therefore an inevitable cost of the need to maintain an open
diffusion path for CO2 to enter photosynthesising leaves.
Plants photosynthesise in order to produce carbon for growth.
To grow new tissues, plants also need inorganic nutrients from
the soil, such as nitrogen and phosphorus, and plant responses
to climatic changes can be modified by the availability of these
nutrients. Nutrient availability itself can also be affected by environmental factors, especially temperature, because the rate
of soil nutrient mineralisation strongly depends on temperature.
For a detailed assessment of the overall effects of a changing
climate on photosynthesis, it is necessary to investigate the response to the simultaneous changes in several climatic variables, such as temperature, water availability, and CO2 concentration. Photosynthesis responds to all aspects of the climate.
Some of these direct and indirect ecophysiological responses
will be described below, and the various responses will then
be brought together into a fully integrated system response.
Photosynthetic Responses to CO2 Concentration
It has been shown in many experimental studies that C3 photosynthesis responds strongly to CO2 concentration, with photosynthesis typically increasing by 25 – 75 % for doubling atmospheric CO2 concentration (e.g., Kimball, 1983; Cure and
Acock, 1986; Drake, 1992; Luxmoore et al., 1993; Drake et al.,
1997; Urban, 2003). There are fewer reports for C4 plants, but
Direct and Indirect Climate Change Effects on Photosynthesis and Transpiration
Plant Biology 6 (2004)
those available suggest only minor responses to increasing CO2
concentration (e.g., Pearcy et al., 1982; Morison and Gifford,
1983; Drake, 1992; Polley et al., 1992).
Recent work has also shown sustained growth increases for
plants fumigated in “free air CO2 enrichment” (FACE) experiments. This has been observed in wheat fields (Garcia et al.,
1998) and in largely undisturbed forests (Herrick and Thomas,
2001; Gunderson et al., 2002). These responses are consistent
with theoretical understanding of the effect of CO2 concentration on photosynthesis at the leaf and stand level (McMurtrie
et al., 1992; Long et al., 1996).
In this paper, these responses have been formalised through
the photosynthesis model of Farquhar et al. (1980) and Farquhar and von Caemmerer (1982), together with assumptions
about stomatal conductance (Ball et al., 1987). The newer biochemical parameters and their temperature dependencies determined by Bernacchi et al. (2001) are used here. These
parameters suggest a greater CO2 under-saturation of Rubisco,
especially at higher temperature, than had been concluded
based on previously used parameters (e.g., McMurtrie et al.,
1992), and hence a greater responsiveness to increasing CO2
concentration.
Fig. 1 Response of C3 photosynthesis to increasing CO2 concentration. The curves compare Rubisco-limited and RuBP regeneration-limited responses at different leaf temperatures. Calculated based on the
parameters of Bernacchi et al. (2001). The response is quantified as the
percentage increase in assimilation rate (A) per percent increase in ambient CO3 concentration (pa).
Fig. 1 shows the CO2 response of photosynthesis under different photosynthetic limitations. The response is much greater
for Rubisco-limited photosynthesis and at higher temperature.
RuBP regeneration-limited photosynthesis responds to CO2
concentration only because of a changing ratio of carboxylations (that fix CO2) to oxygenations (that lose CO2), but the total rate of RuBP regeneration remains the same (Kirschbaum
and Farquhar, 1984). In the Rubisco-limited region, on the other hand, the CO2 uptake kinetics of Rubisco also become a further limitation so that, with increasing CO2 concentration,
there is not only an increasingly favourable ratio of carboxylations to oxygenations, but more RuBP molecules can be utilised as well.
This leads to the question whether plants are Rubisco or RuBP
regeneration-limited under normal environmental conditions.
There have been various surveys of leaf Rubisco activity (quantified through the maximum CO2 fixing capacity of Rubisco
with non-limiting CO2 and RuBP – Vcmax) and their capacity
for RuBP regeneration (Wullschleger, 1993; Medlyn et al.,
1999, 2002). RuBP regeneration capacity can be quantified as
Vjmax (Kirschbaum and Farquhar, 1984) for expression in units
of RuBP regeneration, or as Jmax in units of electron transport.
Units of Jmax are used more frequently in the literature, but
Vjmax has the advantage that it is numerically directly comparable with the units of assimilation rate. Rubisco activity and
the capacity for RuBP regeneration are usually strongly correlated in leaves (e.g., Fig. 2), and it would be optimal for plant
leaves to operate in such a way that Rubisco and RuBP regeneration co-limit photosynthesis (Farquhar and von Caemmerer,
1982).
With increasing atmospheric CO2 concentration, photosynthetic limitation shifts increasingly from this point of co-limitation towards limitation by RuBP regeneration, so that the response to increasing CO2 will be predominantly determined by
the CO2 responsiveness under RuBP regeneration-limited conditions. Furthermore, under light-limited conditions, photo-
Fig. 2 Vjmax plotted against Vcmax from 19 separate gas exchange
studies. All data were normalised to 25 8C and have been converted
from Jmax to Vjmax from the data given in Medlyn et al. (2002). The regression line has a slope of 0.41. Square symbols: broadleaf species; circles: conifers; triangles: crop plants.
synthesis is always RuBP regeneration-limited, so that the
CO2 response of photosynthesis under light-limited conditions
is always best described as the response of RuBP regeneration.
Hence, the overall responsiveness to increasing CO2 is probably most closely approximated by the RuBP regeneration-limited response. Responses shown below are, therefore, based on
the use of equations that describe the RuBP regeneration-limited response. However, in reality, there will also be situations
when photosynthesis is Rubisco limited, so that the overall responsiveness to increasing CO2 should be slightly more pronounced than that estimated based on RuBP regeneration limitation alone.
Fig. 3 shows rates of photosynthesis relative to rates at a preindustrial CO2 concentration of 280 μbar. At 35 8C, photosynthesis has already increased by 20 % over pre-industrial rates,
and is likely to increase by more than 90 % over pre-industrial
243
244
Plant Biology 6 (2004)
M. U. F. Kirschbaum
Fig. 3 Photosynthesis of C3 plants relative to pre-industrial photosynthetic rates. CO2 concentrations from 2000 onwards are based on the
SRES A2 scenario (IPCC, 2000). The response is based on the response
under RuBP regeneration-limited conditions (see Fig. 1). All data are expressed relative to calculated rates of photosynthesis at an assumed
pre-industrial concentration of 280 μbar. Relative rates are calculated
at four different temperatures as shown in the Figure.
rates by the end of the 21st century. The response at 5 8C is
much smaller, with increases of less than 10% to date, and anticipated increases of less than 20% by the end of the 21st century (Fig. 3). This indicates that photosynthesis at normal atmospheric CO2 concentration is already closer to saturation at
such cooler temperatures and thus responds less to increasing
CO2 than photosynthesis at higher temperatures (Long, 1991;
Kirschbaum, 1994). Consequently, plant growth responses to
increasing CO2 concentration are usually much more pronounced for plants grown at higher temperatures, with smaller increases, and sometimes even decreases, for plants grown
at lower temperatures (Kimball, 1983; Rawson, 1992).
The strong temperature × CO2 interaction is due to the competitive interaction between CO2 and O2 at the active site of
Rubisco. Rubisco can react either with CO2, in which case CO2
is productively fixed, or with O2, with CO2 being released and
captured light energy being wasted (Farquhar et al., 1980; Farquhar and von Caemmerer, 1982). The relative reaction rates
with O2 and CO2 depend on the relative concentrations of the
two gases at the enzyme sites and on temperature, with higher
temperatures favouring reactions with O2 (Long, 1991). This
causes photosynthesis to be more under-saturated with CO2
at higher temperature so that relative responses to increasing CO2 concentration increase with temperature (e.g., Kirschbaum and Farquhar, 1984).
Responses of Photosynthesis to Temperature
Photosynthesis can be strongly affected by temperature (e.g.,
Berry and Björkman, 1980; Berry and Raison, 1982; Medlyn et
al., 2002). Photosynthesis is a biochemical process and its
overall temperature response can be understood in terms of
the temperature dependencies of its component processes
and their well-known interactions (Farquhar et al., 1980; Farquhar and von Caemmerer, 1982; Kirschbaum and Farquhar,
1984; Medlyn et al., 2002).
At low to moderate temperatures, the activity of each of these
component processes increases with increasing temperature
in accordance with the Arrhenius relationship (Farquhar et al.,
1980; Berry and Raison, 1982; Medlyn et al., 2002). At higher
Fig. 4 Photosynthetic responses to temperature in four different species (redrawn from Berry and Björkman, 1980). Each panel shows the
short-term temperature response of a species grown under either high
or low temperature. Circles depict the response of low temperaturegrown, and squares that of high temperature-grown plants. Arrows
indicate the respective growth temperatures. Original data were obtained by Björkman et al. (1975), Pearcy (1977), and Mooney et al.
(1978).
temperatures, photosynthesis decreases due to conformational changes in key enzymes. This decrease is reversible at moderately high temperatures but becomes increasingly irreversible with length and intensity of high temperature exposure
(Berry and Björkman, 1980).
Photosynthesis can acclimate considerably to actual growth
conditions, but the patterns differ between species (Fig. 4).
Photosynthesis has a temperature optimum, with the sharpness of the optimum differing between species and growth,
and measurement conditions. Optimum temperatures are
higher in plants acclimated to higher growth temperatures. In
general, as in the examples in Fig. 4, optimum temperatures for
photosynthesis acclimate by about 0.5 8C per 1.0 8C change in
effective growth temperature (Berry and Björkman, 1980; Battaglia et al., 1996).
Atriplex lentiformis, Atriplex sabulosa, and Tidestromia oblongifolia are all C4 plants whereas Larrea divaricata is a C3 plant.
This indicates that both C3 and C4 species can be capable of
high photosynthetic rates up to extremely high temperatures.
While C3 plants are more typically found at cooler locations
than C4 plants (see below), the differences in distribution are
not necessarily reflected in the photosynthetic response
curves of individual species.
Photosynthetic responses to temperature are thus highly dependent on species and growth conditions. All plants appear
to be capable of a degree of adaptation to growth conditions,
and it is important to note that photosynthesis in some species
can function adequately up to 50 8C. This suggests that even
Direct and Indirect Climate Change Effects on Photosynthesis and Transpiration
Plant Biology 6 (2004)
with considerable global warming, some plants will be able to
continue to photosynthesise adequately, provided they have
sufficient water.
Some species, however, are able to acclimate more fully than
others. For example, A. sabulosa performed well when grown
in low temperatures, but photosynthetic rates were much reduced in plants grown at high temperature (Fig. 4 a). The opposite pattern was apparent in T. oblongifolia (Fig. 4 b) so that
temperature increases would be likely to favour T. oblongifolia
at the expense of A. sabulosa.
While individual species respond in unique ways, the competitive effect of increasing temperature can be generalised for
the interaction between C3 and C4 plants. C4 plants are typically found in warmer and drier habitats (Tieszen et al., 1979;
Rundel, 1980; Ehleringer et al., 1997). Warming alone is therefore likely to favour C4 species at the expense of C3 species.
However, increasing CO2 concentration benefits C3 plants, with
limited benefit for C4 species (Ehleringer et al., 1997; Collatz et
al., 1998).
Fig. 5 Critical temperature for the competition between C3 and C4
species as a function of atmospheric CO2 concentration (solid line)
and indicative changes in CO2 concentration and temperature from
1900 to 2100 (dashed line). The critical temperature curve has been redrawn from Collatz et al. (1998), and future CO2 concentrations and
temperatures are based on the SRES A2 scenario (IPCC, 2000).
Hence, the question arises whether C4 plants will gain greater
benefit from increasing temperature than C3 plants from increasing CO2 concentration. The competitive interaction between C3 and C4 plants can be modelled through the effects of
temperature and CO2 concentration on their respective quantum yields, which provides an objective measure to compare
the respective effects of temperature and CO2 concentration
on the two plant groups. Relevant equations have been developed by Collatz et al. (1998) who calculated critical temperatures as a function of atmospheric CO2 concentration for the
competitive balance of C3 and C4 species (Fig. 5).
The critical temperature for the competitive balance between
C3 and C4 species increases steeply with CO2 concentration at
low CO2 concentrations, but flattens out at higher CO2 concentrations. Over the range of possible CO2 concentrations, the
critical temperature for C3-C4 competition can range from 08
to 35 8C (Fig. 5).
If one compares that line of equal competitive strength with
past and anticipated future CO2 concentrations and temperatures, it becomes apparent that the increases in CO2 concentration will be the dominant effect in the context of C3-C4 competition. Starting from a temperature of 15.5 8C, where C3 and C4
were equally competitive at the pre-industrial CO2 concentration of 280 μbar, the dashed line in Fig. 5 shows observed and
anticipated changes in CO2 concentration and global mean
temperature. These points fall far below the critical temperature curve, indicating that the combination of anticipated climatic changes to date and over the 21st century should greatly
favour C3 species at the expense of C4 species.
There are also important interactions between the photosynthetic temperature response and other environmental factors,
such as CO2 concentration (Fig. 6). In the C3 plant Nerium oleander, much higher photosynthetic rates were observed at
higher than lower CO2 concentration. Additionally, the response curve to temperature changed, with optimum temperature increasing with increasing CO2 concentration.
Fig. 6 Photosynthetic responses to temperature in Nerium oleander at
normal (a) and elevated CO2 (b). Redrawn from Berry and Björkman
(1980). Original data were obtained by Björkman et al. (1975, 1978).
Symbols as for Fig. 4.
The experimental observations shown in Fig. 6 are consistent
with theoretical response curves based on photosynthetic
modelling (Fig. 7). At low intercellular CO2 concentration, photosynthesis is limited by Rubisco activity, which shows little
response to temperature because temperature effects on maximum catalytic capacity of Rubisco and the Michaelis–Menten
constant for CO2 largely cancel each other out (Kirschbaum
and Farquhar, 1984). At higher CO2 concentration, on the other
hand, RuBP regeneration is the principal limitation and, because of the strong increase in its activity with temperature
(Medlyn et al., 2002), assimilation rate also responds strongly
to temperature (Kirschbaum and Farquhar, 1984; Medlyn et al.,
2002).
Transpiration Rate at Different Temperatures
The driving force for transpiration from plant canopies is the
difference in vapour pressure between the inside of leaves
and the humidity of the surrounding air, with air humidity often determined by the dewpoint at the overnight minimum
245
246
Plant Biology 6 (2004)
M. U. F. Kirschbaum
Fig. 7 Interaction between leaf temperature and photosynthetic response to intercellular CO2 concentration. The families of curves give
the photosynthetic response to temperature of a Eucalyptus pauciflora
leaf at different constant intercellular CO2 concentrations. The grey
curve links the temperature optima at the respective CO2 concentrations. Simulations are based on the model of Kirschbaum and Farquhar
(1984).
temperature. With global warming, there are likely to be increases in both daytime and nighttime temperatures. If the diurnal temperature range remains constant (but see discussion
below), global warming will lead to an increase in vapour pressure deficit (VPD) because the saturated vapour pressure curve
is steeper at higher than at lower temperatures. VPD increases
by about 5 – 6 % 8C–1 over most combinations of daytime temperatures and diurnal temperature ranges (Kirschbaum,
2000 b).
These changes in VPD can be used to compute changes in transpiration rate with global warming (Fig. 8). These calculations
used the Penman–Monteith equation (Monteith, 1965; Martin
et al., 1989; McKenney and Rosenberg, 1993), with constant
radiation and canopy and aerodynamic resistances that represent typical values for the different canopy types.
Forest canopies tend to be more open than grassland canopies
so that transpiration is mostly controlled by vapour pressure
deficits and hence responds strongly to increases in VPD, with
increases for unstressed forests being between 2 – 5 % 8C–1 over
daytime temperatures between 5 and 35 8C (Fig. 8 a).
Transpiration in grass swards, on the other hand, is largely
controlled by radiation absorption and consequently less affected by increases in vapour pressure deficit (Jarvis and
McNaughton, 1986; Martin et al., 1989). Hence, in unstressed
grasslands, transpiration increases by only 1 – 4 % 8C–1.
Calculated increases in transpiration rate are greater in systems under stress, with increases in transpiration rate ranging
from 3 to 6 % 8C–1 in stressed forest systems. Stressed grasslands are calculated to respond to warming in much the same
way as unstressed forest canopies (Fig. 8 a).
However, under increased CO2 concentration, stomata of most
plants are observed to close to some extent (Saralabai et al.,
1997; Urban, 2003). The effect of such partial stomatal closure
is illustrated in Fig. 8 b for which the Penman–Monteith equation was run for a 1 8C increase in temperature and with some
stomatal closure, as indicated in the Figure. Stomatal closure
Fig. 8 Change in transpiration rate with warming (a), and with warming plus stomatal closure (b). Simulations in (b) are for an unstressed
forest. Further details of the simulations are given in Kirschbaum
(2000b).
by 10% would have the effect of more than completely negating the effect of increasing temperature by 1 8C, leading to marginally reduced transpiration rates (Fig. 8 b).
It leads to the question of the extent of stomatal closure that
can be expected in future. Morison (1985) and Allen (1990)
compiled a range of observations from the literature and
showed that stomatal conductance for both C3 and C4 species
was reduced by about 40% when CO2 concentration was doubled. Bert et al. (1997) in their review of the literature, however, found stomatal closure of only 20 % for doubling CO2 and
a constant ratio of intercellular to ambient CO2 concentration.
Medlyn et al. (2001) found a 21 % decrease in stomatal conductance in studies on European forest trees, and Curtis and Wang
(1998) found even lesser stomatal closure in their review of
studies on woody plants. Reduced stomatal conductance has
also been deduced from analysis of herbarium specimens that
has shown that the number of stomata on leaves has decreased
with historical increases in global CO2 concentration (Woodward, 1987; Rundgren and Björck, 2003; Kouwenberg et al.,
2003).
The carbon isotope discrimination between 13CO2 and 12CO2
can also be used to infer changes in the intercellular CO2 concentration, and that can be related to historical changes in atmospheric CO2 (Dawson et al., 2002). Using this approach, Arneth et al. (2002) and Duquesnay et al. (1998) reported data
that inferred some stomatal closure in response to increasing
atmospheric CO2, but Marshall and Monserud (1996) and
Monserud and Marshall (2001) found no evidence of stomatal
closure in their data sets. While there are some conflicting
Direct and Indirect Climate Change Effects on Photosynthesis and Transpiration
Plant Biology 6 (2004)
diurnal temperature range would have the effect of reducing
the expected increase in VPD, or even lead to a decrease
(Figs. 9 a, b). With a 0.8/1.2 8C (day/night) temperature increase, there would still be a slight increase in VPD, but with
an even greater disparity between daytime and nighttime
temperature increases, VPD would actually decrease.
Increases in transpiration rate are also reduced if nighttime
temperature increases exceed those during the day, and for
0.7/1.3 8C (day/night) temperature increases, there would be
almost no change in transpiration rate (Fig. 9 c). These combinations of temperature increases are similar to the combination of temperature increases observed to date (Easterling et
al., 1997). There is also evidence for a reduction in solar radiation over the past decades, probably linked to increasing atmospheric pollution (Stanhill and Cohen, 2001), which could have
further reduced transpiration rates in the recent past.
Hence, the reduction in diurnal temperature range, in addition
to any stomatal closure, all might completely negate any increase in transpiration with global warming. Therefore, for
the combination of climatic changes observed to date and anticipated into the future, there most likely would be some decrease, rather than increase, in transpiration from most plant
canopies.
Integrating Responses to Temperature, CO2,
Nutrition and Water Availability
Fig. 9 Change in VPD as absolute change (a) or relative change (b),
and transpiration rate (c) for an unstressed forest with increasing temperature for different combinations of daytime and nighttime temperature increases. Each line corresponds to a different combination of
daytime (first number) and nighttime (second number) temperature
increases. Transpiration is calculated for an unstressed forest with the
same parameters as used for the calculations in Fig. 8.
findings in some studies of the effect of CO2 on stomatal conductance, it nonetheless seems likely, on balance, that stomata
of most plants are closing to some extent in response to increasing CO2.
The analysis so far has assumed that there will be the same increases in both daily minimum and maximum temperatures.
However, observed temperature increases to date have been
mainly due to increases in nighttime temperature, with daytime temperatures having increased by only half as much as
nighttime temperatures (Karl et al., 1993; Easterling et al.,
1997). This has been largely associated with an increase in
cloudiness, which in turn is related to increasing industrial
pollution, especially over more industrialised regions (Folland
et al., 2001; Stanhill and Cohen, 2001). Simulations of future
climate generally also show a decrease in diurnal temperature
range, although by less than the trend observed to date (Cubasch et al., 2001).
If day and night temperatures increase to the same extent,
then vapour pressure deficits increase with increasing temperature. In absolute terms, the VPD increase with increasing temperature is more pronounced at higher temperature
(Fig. 9 a), although warming has a proportionately greater effect at lower base temperatures (Fig. 9 b). Any decrease in the
Photosynthesis is intimately linked to the interacting cycles of
carbon, water, and nutrients (Kirschbaum, 1999 a, b), with the
direct effects of CO2 and temperature on photosynthesis, and
the effects of temperature on transpiration rates having been
discussed above. Plants also require nutrients, especially nitrogen, which is mostly derived from the decomposition of soil
organic matter. Plant responses to increasing CO2 can be curtailed through insufficient availability of nutrients. Conversely,
increasing temperature can stimulate nitrogen mineralisation
and thus photosynthesis (Kirschbaum, 1999 b, 2000 a).
The combined effects of these processes are illustrated here
through simulations at four different locations with contrasting climates (Fig. 10). Canberra, Australia, is characterised by
low and irregular rainfall without a distinct rainy season, hot
summers, and fairly cool winters. Manila, Philippines, has very
high rainfall for half of the year but a pronounced dry season
for the other half, and high temperatures throughout the year.
Flakaliden, Sweden, has very cold winters, with snow covering
the ground for four to five months. Precipitation is not high but
more than adequate in this environment with very low evaporative demand. Alice Springs, Australia, has a typical desert climate, characterised by hot summers and very low, and severely limiting, rainfall.
For each of these sites, the comprehensive tree-growth model
CenW (Kirschbaum, 1999a) was run to simulate net primary
production (NPP) under current conditions, and for a changed
climate (Figs. 10,11). The direct effect of changing CO2 concentration was simulated as described above, but was modified in
the whole forest system through subsequent feedback effects.
Simulated responses to increasing temperature were dominated by indirect effects of temperature, while direct temperature
effects played only a minor role.
247
248
Plant Biology 6 (2004)
M. U. F. Kirschbaum
Fig. 10 Response of NPP to doubling CO2
concentration under different base conditions. Four climatically very different sites
were used to provide the base climatic conditions and, at each site, simulations were run
over a range of water and fertiliser additions.
Water loss was simulated with the Penman–Monteith equation. The diurnal temperature range was held constant in the
simulations with increasing temperature, but some degree of
stomatal closure was assumed in response to increasing CO2.
Respiration rate was simulated as being a constant fraction of
daily photosynthetic carbon gain under both increasing CO2
and temperature. The model represents a fully integrated
stand of trees in which the fluxes of carbon, water, and nitrogen are all modelled in their dependence on external factors
and through system internal feedback processes. For a full
description and testing of the model, refer to Kirschbaum
(1999a). The simulations for Flakaliden required detailed modelling of snow cover and the resultant effect on soil temperature. A description and test of these new routines is given in
the Appendix.
For all sites, the model was run for 20 years under either the
standard conditions for each site, or with added water (in daily
additions) and/or added nitrogen fertiliser (in annual additions) to emulate systems with different fertility and water
availability. The model was then run a second time under the
same conditions of water and/or fertiliser additions, and with
either CO2 concentration or temperature increased. Each point
on the 3-D plots then shows the response of the system to
increasing CO2 concentration (Fig. 10) or temperature (Fig. 11)
under contrasting initial conditions. The graphs as they are
cannot be used to infer growth rates under changing water
availability or nutrition. The following section aims to only
show the relative responsiveness of NPP to these key aspects
of climate change under contrasting initial conditions.
The CO2 response differed considerably between sites, and
across different water and fertility levels, with NPP responses
to doubling CO2 ranging between 0 – 70% (Fig. 10). When water
was limiting and nutrition adequate, which was seen especially for Canberra and Alice Springs with added fertiliser, the
growth response to doubled CO2 was almost 70%. Under those
conditions, NPP responses were dominated by water use efficiency, the condition under which increasing CO2 could potentially have its greatest impact.
On the other hand, when water was adequate, but nutrition
limiting, growth responses to doubled CO2 were only of the order of a few percent. This was the case at all sites when sufficient water but no fertiliser was added, and for Flakaliden under almost all conditions. Under those conditions, growth was
temporarily stimulated by increasing CO2, but the extra litter
produced then immobilised nutrients, lowering plant nutritional status and thus prevented sustained growth responses
(see Kirschbaum, 1999 b).
The basic interactive response pattern of increasing CO2 responsiveness with increasing fertility and decreasing water
availability was apparent at three of the four sites across the
range of water and fertiliser additions (Fig. 10). Flakaliden had
sufficient water but limited nutrition over almost all water and
fertiliser additions and showed a CO2 response only with the
highest fertiliser additions.
Direct and Indirect Climate Change Effects on Photosynthesis and Transpiration
Plant Biology 6 (2004)
Fig. 11 NPP response to increasing temperature for different base conditions. Simulations
as for Fig. 10. Note that the axes for water and
fertiliser additions are drawn in the opposite
direction from those in Fig. 10.
The differential CO2 sensitivity under different temperatures
was only apparent when neither water or nutrition were limiting. With maximum water and nutrient additions, Manila had
the highest CO2 response of about 35 %, Canberra about 25 %
and Flakaliden about 15 %. Alice Springs did not receive sufficient water and fertiliser additions to completely escape water
limitation over any of the additions used here. Under other conditions, either water use efficiency, or the negative feedbacks
from developing nutrient deficiency, became the dominant factor controlling the overall CO2 response of photosynthesis.
Under conditions when nutrition was limiting (i.e., with less
applied fertilizer, Fig. 11), the growth response to increased
temperature became more positive at all sites because of the
increasing importance of enhanced nutrient mineralisation.
That dependence on nutrient availability was most pronounced for the Canberra site, where a positive growth response of 15 % per degree warming was possible, yet the positive response to temperature disappeared with even a slight
fertiliser addition when only the negative effect of greater water loss remained, and the overall response became negative.
In response to increasing temperature (Fig. 11), the response
patterns under varying additions of water and nutrients were
fundamentally different from the responses to increasing CO2.
Increasing temperature can stimulate the rate of nitrogen mineralisation (Schimel et al., 1990; Kirschbaum, 2000 a), thereby
increasing nutrient supply and thus stimulating plant productivity, independent of any direct physiological plant responses
to increasing temperature.
Alice Springs showed a similar pattern, but with a more pronounced interaction between water and fertiliser additions as
the site remained water limited over most combinations of
water and fertiliser additions, and the response to increasing
temperature remained negative. Only with very large water
and no fertiliser additions did the response to temperature become positive.
Under conditions of limiting water and adequate nutrition,
growth responses were negative at all sites except Flakaliden
(Fig. 11). The principal reason was the increased water loss under increased temperature (see Fig. 8 – the simulations here
assumed a constant diurnal temperature range). In Flakaliden,
water limitations did not develop for a 1 8C temperature increase, so that the greater water loss at increased temperature
did not become limiting. Instead, the benefit of an extended
growing season and enhanced nitrogen mineralisation led to
a significant positive overall growth response.
These simulations have demonstrated that there is no unique
sensitivity of plant productivity to increasing CO2 concentration or temperature, but that responses are highly dependent
on circumstances. Responses to doubling CO2 are likely to
range from close to zero under nutrient-limited and well-watered conditions to increases of up to 70% under fertile but water-limited conditions (Fig. 10). Direct physiological responses,
which come into play when neither water nor nutrition are
limiting, are intermediate in their magnitude and differ with
predominant temperature. In response to increasing temperature, responses are similarly varied, with negative responses
249
250
Plant Biology 6 (2004)
M. U. F. Kirschbaum
under fertile but well-watered conditions and positive by up to
15 % per degree warming at cold sites, or sites that are strongly
nitrogen-limited (Fig. 11).
This makes it difficult to provide generalisations for the response of plants to increasing CO2 concentration or temperature. Hence, the response of individual stands of plants to increasing CO2 can only be predicted if the key limitations in
each system are understood and quantified. It is important to
quantify not only direct responses to changed external conditions but also any possible feedback effects in the system or
important controlling factors that might be independently affected by climatic changes. The overall system response will be
affected by all of these individual factors, and by their interactions.
All these factors interact strongly so that, for different combinations of temperature and CO2 increases, for systems in different parts of the world, and for systems primarily effected
by water or nutrient limitations, different overall effects on
plant photosynthesis must be expected. Responses can be negative in some circumstances and positive in others, depending
on the exact nature of changes and the factors that are initially
limiting growth and photosynthesis.
Acknowledgements
I wish to thank Sune Linder and Johan Bergh for providing the
climatic information from the Flakaliden experimental site,
and Chris Beadle and Chris Harwood for useful comments and
suggestions on the manuscript.
Appendix – Snow and Soil Temperature Calculations
The dynamics of snow cover and its effect on soil temperature
are simulated using a routine of intermediate complexity. It is
more detailed than the procedure used by McGuire et al.
(2000) but simpler than the much more detailed routines that
have been used for simulating the progression of a freezing
zone with depth into the soil and resultant effects on hydrology (e.g., Male and Granger, 1981; Stähli and Jansson, 1998; Kennedy and Sharratt, 1998; Smirnova et al., 2000).
dTs/dt = (Tm – Ts)/rT
(A3)
where rT is the soil resistance to temperature change. When
there is snow cover and the temperature is below 0 8C, snow
acts as an additional resistance to temperature change so that:
dTs/dt = (Tm – Ts)/(rT + rsS)
(A4)
where rs gives the additional resistance to soil temperature
change per mm (water equivalent) in the snow layer.
When snow is melting, the temperature at the top of the soil
cannot be greater than 0 8C. Hence, the rate of soil warming in
spring is given by the lesser of heat transfer through the insulating snow layer and the heat transfer from the top of the soil
at 0 8C. Hence, when air temperature is above 0 8C:
dTs/dt = (Tm – Ts)/(rT + rsS)
if (– Ts/rT) < [(Tm – Ts)/(rT + rsS)]
(A5a)
dTs/dt = – Ts/rT if (– Ts/rT) < [(Tm – Ts)/(rT + rsS)]
(A5b)
Model testing
The revised soil temperature routines were tested against data
from the Flakaliden site. Fig. A 1 shows observed soil and air
temperatures and predicted soil temperatures and snow packs
for one typical year out of the four years of available data.
Fig. A2 plots all observed versus predicted soil temperatures
over four years.
Soil temperatures closely followed air temperatures over the
snow-free period. The model parameter fitted to the data,
rT = 5 d–1, implies that soil temperature at 10 cm depth changed
daily by 1 ⁄ 5 of the temperature difference between air and soil
temperature, allowing the soil to follow air temperature with
only a few days delay.
Once snow fell, however, the soil became effectively isolated
from the air above it, and temperatures hardly changed (see
Goulden et al., 1998; Bergh and Linder, 1999; Strand et al.,
2002). Even though winter mean air temperatures fell to as
Precipitation is assumed to fall as snow, S, and accumulate on
the ground when daily mean temperature is below 0 8C:
dS/dt = P
if Tm < 0
(A1)
where Tm is mean air temperature and P is precipitation.
Snow is assumed to melt due to the combined effects of sensible and radiative heat transfer as:
dS/dt = –(mT Tday + mQ Qi) if (mT Tday + mQ Qi) > 0
(A2)
where Tday is mean daytime temperature, Qi is incident daily
radiation, and mT and mQ are empirical parameters that describe the dependence of the rate of snow melt on daytime
temperature and incident radiation, respectively.
Without snow, soil temperature, Ts, follows mean air temperature, with some characteristic delay term so that
Fig. A 1 Observed daily mean air and soil temperatures (at 10 cm),
predicted soil temperature (circles), and modelled snow pack (expressed in mm water) for one year of the data collected and modelled
at Flakaliden. For predicted soil temperatures, only one weekly value is
shown.
Direct and Indirect Climate Change Effects on Photosynthesis and Transpiration
Fig. A2 Observed versus predicted soil temperature (at 10 cm) at
Flakaliden (n = 1460). The line in the Figure is a 1 : 1 relationship and explains 95.6% of the observed variation.
low as – 20 8C, soil temperature remained at about 0 8C. With
regular precipitation throughout the year, snow started to fall
as soon as mean temperatures fell below 0 8C. As the soil temperature was still above 0 8C in autumn, the insulating snow
layer appeared at just the time when cold air temperatures
could have potentially pulled soil temperatures to below 0 8C
as well. The development of an insulating snow layer prevented that.
The model parameters fitted to the data suggest a rapid increase in the resistance to heat transfer by the developing
snow layer. The fitted parameter, rs = 10 mm–1 d–1, implied that
the rate of heat transfer was halved by a snow layer of as little
as 0.5 mm (water equivalent; this corresponds to about 5 mm
in depth of fresh snow). Overall, there was excellent correspondence between predicted and observed data (Fig. A2),
with 95.6 % of variation accounted for by the simple model
used here.
References
Allen, L. H. (1990) Plant responses to rising carbon dioxide and potential interactions with air pollutants. Journal of Environmental
Quality 19, 15 – 34.
Arneth, A., Lloyd, J., Santruckova, H., Bird, M., Grigoryev, S., Kalaschnikov, Y. N., Gleixner, G., and Schulze, E. D. (2002) Response of central Siberian Scots pine to soil water deficit and long-term trends
in atmospheric CO2 concentration. Global Biogeochemical Cycles
16, 1 – 13.
Ball, J. T., Woodrow, I. E., and Berry, J. A. (1987) A model predicting
stomatal conductance and its contribution to the control of photosynthesis under different environmental conditions. In Progress in
Photosynthesis Research, Vol. IV (Biggins, J., ed.), Dordrecht: Martinus Nijhoff, pp. 221 – 224.
Battaglia, M., Beadle, C., and Loughhead, S. (1996) Photosynthetic
temperature response of Eucalyptus globulus and Eucalyptus nitens. Tree Physiology 16, 81 – 89.
Bergh, J. and Linder, S. (1999) Effects of soil warming during spring
on photosynthetic recovery in boreal Norway spruce stands. Global Change Biology 5, 245 – 253.
Plant Biology 6 (2004)
Bernacchi, C. J., Singsaas, E. L., Pimentel, C., Portis, A. R., and Long, S. P.
(2001) Improved temperature response functions for models of
Rubisco-limited photosynthesis. Plant, Cell and Environment 24,
253 – 259.
Berry, J. and Björkman, O. (1980) Photosynthetic response and adaptation to temperature in higher plants. Annual Review of Plant
Physiology 31, 491 – 543.
Berry, J. A. and Raison, J. K. (1982) Responses of macrophytes to temperature. In Physiological Plant Ecology I. Responses to the Physical Environment, Encyclopedia of Plant Physiology, New Series,
Vol. 12 A (Lange, O. L., Nobel, P. S., Osmond, C. B., and Ziegler, H.,
eds.), Berlin, Heidelberg, New York: Springer-Verlag, pp. 277 – 338.
Bert, D., Leavitt, S. W., and Dupouey, J.-L. (1997) Variations in wood
δ13C and water-use efficiency of Abies alba during the last century.
Ecology 78, 1588 – 1595
Björkman, O., Badger, M., and Armond, P. A. (1978) Thermal acclimation of photosynthesis: effect of growth temperature on photosynthetic characteristics and components of the photosynthetic apparatus in Nerium oleander. Carnegie Institution Washington Yearbook 77, 262 – 282.
Björkman, O., Mooney, H. A., and Ehleringer, J. (1975) Photosynthetic
responses of plants from habitats with contrasting thermal environments: comparison of photosynthetic characteristics of intact
plants. Carnegie Institution Washington Yearbook 74, 743 – 748.
Collatz, G. J., Berry, J. A., and Clark, J. S. (1998) Effects of climate and
atmospheric CO2 partial pressure on the global distribution of C4
grasses: present, past, and future. Oecologia 114, 441 – 454.
Cubasch, U., Meehl, G. A., Boer, G. J., Stouffer, R. J., Dix, M., Noda, A.,
Senior, C. A., Raper, S., and Yap, K. S. (2001) Projections of future climate change. In Climate Change 2001: The Scientific Basis
(Houghton, J. T., Ding, Y., Griggs, D. J., Noguer, M., van der Linden,
P. J., Dai, X., Maskell, K., and Johnson, C. A., eds.), IPCC Working
Group I, Third Assessment Report. Cambridge, UK: Cambridge University Press, pp. 525 – 582.
Cure, J. D. and Acock, B. (1986) Crop responses to carbon dioxide doubling: a literature survey. Agricultural and Forest Meteorology 38,
127 – 145.
Curtis, P. S. and Wang, X. (1998) A meta-analysis of elevated CO2 effects on woody plant mass, form and physiology. Oecologia 113,
299 – 313.
Dawson, T. E., Mambelli, S., Plamboeck, A. H., Templer, P. H., and Tu, K.
P. (2002) Stable isotopes in plant ecology. Annual Review of Ecology and Systematics 33, 507 – 559.
Drake, B. G. (1992) A field study of the effects of elevated CO2 on ecosystem processes in a Chesapeake Bay wetland. Australian Journal
of Botany 40, 579 – 595.
Drake, B. G., Gonzalez-Meler, M. A., and Long, S. P. (1997) More efficient plants: a consequence of rising atmospheric CO2? Annual Review of Plant Physiology and Plant Molecular Biology 48, 609 –
639.
Duquesnay, A., Breda, N., Stievenard, M., and Dupouey, J. L. (1998)
Changes of tree-ring 13C and water-use efficiency of beech (Fagus
sylvatica L.) in north-eastern France during the past century. Plant,
Cell and Environment 21, 565 – 572.
Easterling, D. R., Horton, B., Jones, P. D., Peterson, T. C., Karl, T. R., Parker, D. E., Salinger, M. J., Razuvayev, V., Plummer, N., Jamason, P., and
Folland, C. K. (1997) Maximum and minimum temperature trends
for the globe. Science 277, 364 – 367.
Ehleringer, J. R., Cerling, T. E., and Helliker, B. R. (1997) C4 photosynthesis, atmospheric CO2 and climate. Oecologia 112, 285 – 299.
Farquhar, G. D. and von Caemmerer, S. (1982) Modelling of photosynthetic response to environmental conditions. In Physiological
Plant Ecology II. Water Relations and Carbon Assimilation, Encyclopedia of Plant Physiology, New Series, Vol. 12 B (Lange, O. L., Nobel, P. S., Osmond, C. B., and Ziegler, H., eds.), Berlin, Heidelberg,
New York: Springer-Verlag, pp. 549 – 588.
251
252
Plant Biology 6 (2004)
Farquhar, G. D., von Caemmerer, S., and Berry, J. (1980) A biochemical
model of photosynthetic CO2 assimilation in leaves of C3 species.
Planta 149, 78 – 90.
Folland, C. K., Karl, T. R., Christy, J. R., Clarke, R. A., Gruza, G. V., Jouzel,
J., Mann, M. E., Oerlemans, J., Salinger, M. J., and Wang, S.-W. (2001)
Observed climate variability and change. In Climate Change 2001:
The Scientific Basis (Houghton, J. T., Ding, Y., Griggs, D. J., Noguer,
M., van der Linden, P. J., Dai, X., Maskell, K., and Johnson, C. A.,
eds.), IPCC Working Group I, Third Assessment Report. Cambridge,
UK: Cambridge University Press, pp. 99 – 181.
Garcia, R. L., Long, S. P., Wall, G. W., Osborne, C. P., Kimball, B. A., Nie,
G. Y., Pinter, P. J., Lamorte, R. L., and Wechsung, F. (1998) Photosynthesis and conductance of spring wheat leaves: field response to
continuous free-air atmospheric CO2 enrichment. Plant, Cell and
Environment 21, 659 – 669.
Goulden, M. L., Wofsy, S. C., Harden, J. W., Trumbore, S. E., Crill, P. M.,
Gower, S. T., Fries, T., Daube, B. C., Fan, S.-M., Sutton, D. J., Bazzaz, A.,
and Munger, J. W. (1998) Sensitivity of boreal forest carbon balance to soil thaw. Science 279, 214 – 217.
Gunderson, C. A., Sholtis, J. D., Wullschleger, S. D., Tissue, D. T., Hanson, P. J., and Norby, R. J. (2002) Environmental and stomatal control of photosynthetic enhancement in the canopy of a sweetgum
(Liquidambar styraciflua L.) plantation during 3 years of CO2 enrichment. Plant, Cell and Environment 25, 379 – 393.
Herrick, J. D. and Thomas, R. B. (2001) No photosynthetic down-regulation in sweetgum trees (Liquidambar styraciflua L.) after three
years of CO2 enrichment at the Duke FACE experiment. Plant, Cell
and Environment 24, 53 – 64.
IPCC (2000) Special Report on Emissions Scenarios. A Special Report
of Working Group III of the Intergovernmental Panel on Climate
Change. Cambridge, UK: Cambridge University Press.
Jarvis, P. G. and McNaughton, K. G. (1986) Stomatal control of transpiration: scaling up from leaf to region. Advances in Ecological
Research 15, 1 – 49.
Karl, T. R., Jones, P. D., Knight, R. W., Kukla, G., Plummer, N., Razuvayev, V., Gallo, K. P., Lindseay, J., Charlson, R. J., and Peterson, T. C.
(1993) A new perspective on recent 1 global warming: asymmetric
trends of daily maximum and minimum temperature. Bulletin of
the American Meteorological Society 74, 1007 – 1023.
Kennedy, I. and Sharratt, B. (1998) Model comparisons to simulate
soil frost depth. Soil Science 163, 636 – 645.
Kimball, B. A. (1983) Carbon dioxide and agricultural yield: an assemblage and analysis of 430 prior observations. Agronomy Journal 75, 779 – 788.
Kirschbaum, M. U. F. (1994) The sensitivity of C3 photosynthesis to
increasing CO2 concentration. A theoretical analysis of its dependence on temperature and background CO2 concentration. Plant,
Cell and Environment 17, 747 – 754.
Kirschbaum, M. U. F. (1999 a) CenW, a forest growth model with
linked carbon, energy, nutrient and water cycles. Ecological Modelling 181, 17 – 59.
Kirschbaum, M. U. F. (1999 b) Modelling forest growth and carbon
storage with increasing CO2 and temperature. Tellus 51 B, 871 –
888.
Kirschbaum, M. U. F. (2000 a) Will changes in soil organic matter act
as a positive or negative feedback on global warming? Biogeochemistry 48, 21 – 51.
Kirschbaum, M. U. F. (2000 b). Forest growth and species distributions in a changing climate. Tree Physiology 20, 309 – 322.
Kirschbaum, M. U. F. and Farquhar, G. D. (1984) Temperature dependence of whole-leaf photosynthesis in Eucalyptus pauciflora Sieb. ex
Spreng. Australian Journal of Plant Physiology 11, 519 – 538.
Kouwenberg, L. L. R., McElwain, J. C., Kurschner, W. M., Wagner, F.,
Beerling, D. J., Mayle, F. E., and Visscher, H. (2003) Stomatal frequency adjustment of four conifer species to historical changes in
atmospheric CO2. American Journal of Botany 90, 610 – 619.
M. U. F. Kirschbaum
Long, S. P. (1991) Modification of the response of photosynthetic productivity to rising temperature by atmospheric CO2 concentrations: Has its importance been underestimated? Plant, Cell and
Environment 14, 729 – 739.
Long, S. P., Osborne, C. P., and Humphries, S. W. (1996) Photosynthesis, rising atmospheric carbon dioxide concentration and climate
change. In SCOPE 56 – Global Change: Effects on Coniferous Forests and Grasslands (Breymeyer, A. I., Hall, D. O., Melillo, J. M., and
Ågren, G. I., eds.), Chichester a.o.: John Wiley and Sons Ltd.,
pp.121 – 159.
Luxmoore, R. J., Wullschleger, S. D., and Hanson, P. J. (1993) Forest responses to CO2 enrichment and climate warming. Water, Air, and
Soil Pollution 70, 309 – 323.
Male, D. H. and Granger, R. J. (1981) Snow surface energy exchange.
Water Research 17, 609 – 627.
Marshall, J. D. and Monserud, R. A. (1996) Homeostatic gas-exchange
parameters inferred from 13C/12C in tree rings of conifers. Oecologia 105, 13 – 21.
Martin, P., Rosenberg, N., and McKenney, M. S. (1989) Sensitivity of
evapotranspiration in a wheat field, a forest and a grassland to
changes in climate and direct effects of carbon dioxide. Climatic
Change 14, 117 – 151.
McGuire, A. D., Melillo, J. M., Randerson, J. T., Parton, W. J., Heimann,
M., Meier, R. A., Clein, J. S., Kicklighter, D. W., and Sauf, W. (2000)
Modelling the effects of snowpack on heterotrophic respiration
across northern temperate and high latitude regions: comparisons
with measurements of atmospheric carbon dioxide in high latitudes. Biogeochemistry 48, 91 – 114.
McKenney, M. S. and Rosenberg, N. J. (1993) Sensitivity of some potential evapotranspiration estimation methods to climate change.
Agricultural and Forest Meteorology 64, 81 – 110.
McMurtrie, R. E., Comins, H. N., Kirschbaum, M. U. F., and Wang, Y.-P.
(1992) Modifying existing forest growth models to take account of
effects of elevated CO2. Australian Journal of Botany 40, 657 – 677.
Medlyn, B. E., Badeck, F. W., De Pury, D. G. G., Barton, C. V. M., Broadmeadow, M., Ceulemans, R., De Angelis, P., Forstreuter, M., Jach, M.
E., Kellomäki, S., Laitat, E., Marek, M., Philippot, S., Rey, A., Strassemeyer, J., Laitinen, K., Liozon, R., Portier, B., Roberntz, P., Wang, K.,
and Jarvis, P. G. (1999) Effects of elevated [CO2] on photosynthesis
in European forest species: a meta-analysis of model parameters.
Plant, Cell and Environment 22, 1475 – 1495.
Medlyn, B. E., Barton, C. V. M., Broadmeadow, M. S. J., Ceulemans, R.,
De Angelis, P., Forstreuter, M., Freeman, M., Jackson, S. B., Kellomäki, S., Laitat, E., Rey, A., Sigurdsson, B. D., Strassemeyer, J., Wang, K.,
Curtis, P. S., and Jarvis, P. G. (2001) Stomatal conductance of forest
species after long-term exposure to elevated CO2 concentration: a
synthesis. New Phytologist 149, 247 – 264.
Medlyn, B. E., Dreyer, E., Ellsworth, D. E., Forstreuter, M., Harley, P. C.,
Kirschbaum, M. U. F., LeRoux, X., Loustau, D., Montpied, P., Strassemeyer, J., Walcroft, A., and Wang, K. Y. (2002) Temperature response of parameters of a biochemically-based model of photosynthesis. II. A review of experimental data. Plant, Cell and Environment 25, 1167 – 1179.
Monserud, R. A. and Marshall, J. D. (2001) Time-series analysis of 13C
from tree rings. I. Time trends and autocorrelation. Tree Physiology 21, 1087 – 1102.
Monteith, J. L. (1965) Evaporation and environment. Symposium of
the Society for Experimental Biology 19, 205 – 234.
Mooney, H. A., Björkman, O., and Collatz, G. J. (1978) Photosynthetic
acclimation to temperature in the desert shrub, Larrea divaricata.
I. Carbon dioxide exchange characteristics of intact leaves. Plant
Physiology 61, 406 – 410.
Morison, J. I. L. and Gifford, R. M. (1983) Stomatal sensitivity to carbon dioxide and humidity. Plant Physiology 71, 789 – 796.
Morison, J. I. L. (1985) Sensitivity of stomata and water use efficiency
to high CO2. Plant, Cell and Environment 8, 467 – 474.
Direct and Indirect Climate Change Effects on Photosynthesis and Transpiration
Pearcy, R. W. (1977) Acclimation of photosynthetic and respiratory
CO2 exchange to growth temperature in Atriplex lentiformis (Torr.)
Wats. Plant Physiology 59, 795 – 799.
Pearcy, R. W., Osteryoung, K., and Randall, D. (1982) Carbon dioxide
exchange characteristics of C4 Hawaiian Euphorbia species native
to diverse habitats. Oecologia 55, 333 – 341.
Polley, H. W., Norman, J. M., Arkebauer, T. J., Walter-Shea, E. A., Greegor D. H. Jr., and Bramer, B. (1992) Leaf gas exchange of Andropogon
gerardii Vitman, Panicum virgatum L. and Sorghastrum nutans (L.)
Nash in a tallgrass prairie. Journal of Geophysical Research 97,
18837 – 18844.
Rawson, H. M. (1992) Plant responses to temperature under conditions of elevated CO2. Australian Journal of Botany 40, 473 – 490.
Rundel, P. W. (1980) The ecological distribution of C4 and C3 grasses
in the Hawaiian islands. Oecologia 45, 354 – 359.
Rundgren, M. and Björck, S. (2003) Late-glacial and early Holocene
variations in atmospheric CO2 concentration indicated by highresolution stomatal index data. Earth and Planetary Science Letters 213, 191 – 204.
Saralabai, V. C., Vivekanandan, M., and Babu, R. S. (1997) Plant responses to high CO2 concentration in the atmosphere. Photosynthetica 33, 7 – 37.
Schimel, D. S., Parton, W. J., Kittel, T. G. F., Ojima, D. S., and Cole,
C. V. (1990) Grassland biogeochemistry: links to atmospheric processes. Climatic Change 17, 13 – 25.
Smirnova, T. G., Brown, J. M., Benjamin, S. G., and Kim, D. (2000) Parameterization of cold-season processes in the MAPS land-surface
scheme. Journal of Geophysical Research 105, 4077 – 4086.
Stähli, M. and Jansson, P. E. (1998) Test of two SVAT snow submodels
during different winter conditions. Agricultural and Forest Meteorology 92, 29 – 41.
Stanhill, G. and Cohen, S. (2001) Global dimming: a review of the evidence for a widespread and significant reduction in global radiation with discussion of its probable causes and possible agricultural consequences. Agricultural and Forest Meteorology 107, 255 –
278.
Strand, M., Lundmark, T., Söderbergh, I., and Mellander, P.-E. (2002)
Impact of seasonal air and soil temperature on photosynthesis in
Scots pine trees. Tree Physiology 22, 839 – 847.
Tieszen, L. L., Senyimba, M. M., Imbamba, S. K., and Troughton, J. H.
(1979) The distribution of C3 and C4 grasses and carbon isotope
discrimination along an altitudinal and moisture gradient in Kenya. Oecologia 37, 337 – 350.
Urban, O. (2003) Physiological impacts of elevated CO2 concentration
ranging from molecular to whole plant responses. Photosynthetica
41, 9 – 20.
Woodward, F. I. (1987) Stomatal numbers are sensitive to increases
in CO2 from pre-industrial levels. Nature 327, 617 – 618.
Wullschleger, S. D. (1993) Biochemical limitations to carbon assimilation in C3 plants – a retrospective analysis of A/ci curves from 109
species. Journal of Experimental Botany 44, 907 – 920.
M. U. F. Kirschbaum
CSIRO Forestry and Forest Products
P.O. Box 4008
Kingston ACT 2604
Australia
E-mail: miko.kirschbaum@csiro.au
Guest Editor: F. Loreto
Plant Biology 6 (2004)
253