Download Forest growth and species distribution in a changing climate

Tree Physiology 20, 309–322
© 2000 Heron Publishing—Victoria, Canada
Forest growth and species distribution in a changing climate
MIKO U. F. KIRSCHBAUM
CSIRO Forestry and Forest Products, PO Box E4008, Kingston ACT 2604, Australia
Received March 24, 1998
Summary Climate change has many potential effects on
plants, some detrimental to growth, others beneficial. Increasing CO2 concentration can increase photosynthetic rates, with
the greatest increases likely to be in C3 plants growing in warm
dry conditions. Increasing temperature directly affects plant
growth through effects on photosynthetic and respiration rates.
However, plants have a considerable ability to adapt to changing conditions and can tolerate extremely high temperatures,
provided that adequate water is available. Increasing temperature may increase vapor pressure deficits of the air, and thereby
increase transpiration rates from most plant canopies. Effects
are likely to vary among plant communities, with forests generally experiencing greater increases in transpiration rates than
grasslands. These increases in transpiration are likely to be reduced by stomatal closure in response to increasing CO2 concentration. In many areas, precipitation will probably increase
with global warming; however, these increases may be insufficient to meet the increased transpirational demand by plant
canopies. Increasing temperature is likely to increase soil organic matter decomposition rates so that nutrients may be more
readily mineralized and made available to plants. In highly fertile systems, this could lead to nutrient losses through leaching.
For different combinations of increases in temperature and
CO2 concentration, and for systems primarily affected by water or nutrient limitations, different overall effects on plant
productivity can be expected. Responses will be negative in
some circumstances and positive in others, but on the whole,
catastrophic changes to forest growth seem unlikely under
most conditions.
In contrast, ecological consequences of climate change are
potentially more serious. The distribution of many species
tends to be limited to a narrow range of environmental conditions. Climate conditions over much of a species’ current natural range may therefore become unsuitable, leading to
significant decline of forests or of particular species within
forests.
Keywords: CO2, global warming, greenhouse gases, mineralization, photosynthesis, transpiration.
belowground terrestrial organic carbon (Melillo et al. 1990).
Forests can become carbon sources when they are cut or degraded or carbon sinks when newly established or when
growth rates are enhanced. Forests also harbor the majority of
the world’s biodiversity. As such, they represent indispensable repositories of genetic resources.
Climate critically influences the structure and function of
forests. All forest organisms ultimately depend directly or indirectly on photosynthesis for their energy requirements. Photosynthesis depends on the absorption of light and the diffusion of
CO2 from the atmosphere to the sites of photosynthesis within
leaves. To take up CO2, plants must open their stomata, which results in the outward diffusion of water. Increases in atmospheric
CO2 concentration can increase photosynthetic carbon gain of
most plants by improving the ratio between carbon assimilation
and transpirational water loss. Conversely, increased temperatures will reduce the ratio of carbon gain to water loss.
The responses of plants to climatic changes can be modified by
climatic effects on mineral nutrient availability. For a detailed
assessment of the effects of changing climate on forest
ecosystems, it is necessary to investigate the response to simultaneous changes in several climatic variables, such as temperature, water availability, and ambient CO2 concentrations.
Forest growth can respond to climate change directly, e.g.,
changes in rates of photosynthesis and respiration in response
to changes in temperature, and indirectly, e.g., through
changed water relations, which impact photosynthesis through
changes in stomatal conductance. Some of these ecophysiological responses will be described below and integrated
into a simulated system response.
In considering the effect of climate change on forest ecosystems, it is necessary to consider not only the direct ecophysiological effects, but also the ways in which these effects are
modified by biological interactions between organisms. Some
species will remain unaffected by climate change, whereas
others will become more or less competitive. These ecological
interactions may ultimately have the greatest consequence for
the future functioning of forest ecosystems.
How is the climate changing?
Introduction
Forests cover about one quarter of the Earth’s land surface
area. They play a major role in the global carbon budget, because they contain about 80% of all aboveground and 40% of
The atmospheric CO2 concentration has increased from its
preindustrial concentration of about 280 µmol mol –1 to almost
370 µmol mol –1 in 1998, and is increasing further by about
1.5 µmol mol –1 each year (Figure 1). The annual rate of in-
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crease shows some intriguing interannual variations, with
1992 and 1993 showing rates of increase of less than 1 µmol
mol –1 year –1 (Figure 1). These low rates of increase followed
the 1991 eruption of Mt. Pinotubo and may be related to the
temporary global cooling that followed the eruption. In more
recent years, the atmospheric CO2 concentration has been increasing at rates of 1.5 to 2 µmol mol –1 year –1. Unless emissions of fossil fuels can be significantly curtailed in the future,
atmospheric CO2 concentration may reach 700 µmol mol –1 before the end of the 21st century (Schimel et al. 1996).
These increases in CO2 concentration, together with the increase in other greenhouse gases, are widely believed to be responsible for increased global mean temperatures (Nicholls et
al. 1996). Temperatures in the late 1990s have been more than
half a degree warmer than those at the end of the last century
(Figure 1). Temperatures in 1998 were the warmest observed
within the instrumental record, exceeding the previous record
in 1997 by about 0.15 ºC (Figure 1). If the concentration of
greenhouse gases continues to increase, temperatures are
likely to increase by a further 1 to 4.5 °C by 2100, depending
on future rates of greenhouse gas emission, the countervailing
effects of pollution haze, and climatic sensitivity to greenhouse gas concentrations (Kattenberg et al. 1996). Some regions are likely to experience significantly more or less
warming than the global mean, and land temperatures are
likely to increase more than ocean temperatures because of the
greater heat capacity of the oceans. Increased temperature may
lead to additional changes in precipitation, cloudiness, frequency and intensity of extreme events and sea level rise
(Kattenberg et al. 1996).
Responses of photosynthesis to CO2 concentration
Of the projected aspects of atmospheric and climate change,
the increase in atmospheric CO2 concentration is the most certain. It has been shown in many experimental studies that photosynthesis in C3 plants, including trees, responds strongly to
CO2 concentration, with photosynthesis typically increasing
25–75% for a doubling in CO2 concentration (e.g., Kimball
1983, Cure and Acock 1986, Drake 1992, Luxmoore et al.
1993). These responses persist after inclusion of the effects of
photosynthetic down-regulation (Gunderson and Wullschleger 1994). Such 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).
For the present work, these responses have been formalized
through the photosynthesis model of Farquhar et al. (1980)
and Farquhar and von Caemmerer (1982). Based on assumptions about stomatal conductance (Ball et al. 1987) and the relative limitations by Rubisco activity and RuBP regeneration, it
is possible to model the dependence of photosynthesis on CO2
concentration at different temperatures (Kirschbaum 1994).
Figure 2 shows rates of photosynthesis at elevated atmospheric CO2 concentrations relative to rates at preindustrial atmospheric CO2 concentration (here defined as 281 µmol
mol –1).
These simulations show that the photosynthetic rate in
Figure 1. Mean global CO2 concentration (top panel) and global temperature anomaly (bottom panel). The insert in the top panel gives annual rates of increase over recent years. The CO2 data have been
redrawn from IPCC (1996) and updated with data from Keeling and
Whorf available from the Web: http://cdiac.esd.ornl.gov/ftp/mauna
loa-co2/maunaloa.co2. Temperature data are from Jones (1994) and
updated with more recent data from the Web: http://cdiac.esd.
ornl.gov/ftp/trends/temp/jonescru/global.dat.
C3 plants, especially at higher temperatures, is not saturated
with CO2, and that the overall rate of photosynthesis is likely
to have increased over this century, and will continue to increase into the next century. Even at the CO2 concentrations
projected for the end of the 21st century, the photosynthetic
rate is still not saturated with CO2 and the rate of photosynthesis will continue to increase with further increases in CO2
concentration. At 35 °C, photosynthetic rates have already increased by 5% over preindustrial rates, and are likely to increase by about 20% over preindustrial rates by the end of the
20th century. The response at lower temperatures, on the other
hand, is much smaller, indicating that photosynthetic rates are
closer to CO2 saturation at those temperatures (Kimball 1983,
Figure 2. Response of C3 photosynthesis to increasing CO2 concentration. The response up to 1997 is shown in (a), based on the observed CO2 concentrations shown in Figure 1. The response up to the
year 2100 is shown in (b), based on predicted increases in CO2 concentration into the next century following the IPCC 92a scenario
(Schimel et al. 1996). Data are expressed relative to calculated rates
of photosynthesis at an assumed preindustrial concentration of 281
µmol mol –1. Relative rates are calculated at four temperatures as
shown in the Figure. Calculations follow the equations given by
Kirschbaum (1994) and only describe the direct response of photosynthesis to CO2 concentration without additional feedback effects or
interaction with water use.
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Rawson 1992). There are fewer reports with C4 plants, but the
available evidence suggests only minor responses to CO2 concentration (e.g., Pearcy et al. 1982, Morison and Gifford 1983,
Drake 1992, Polley et al. 1992).
The strong enhancement of C3 photosynthesis is mainly a
result of the competitive interaction between CO2 and oxygen
at the active site of Rubisco. Rubisco reacts either with CO2, in
which case CO2 is productively fixed, or with oxygen, with
CO2 being released and captured light energy being wasted
(Farquhar et al. 1980, Farquhar and von Caemmerer 1982).
The relative reaction rates of Rubisco with oxygen and CO2
depend on the relative concentrations of the two gases and on
temperature, with higher temperatures favoring reactions with
oxygen. This causes photosynthesis to be less saturated with
CO2 at higher temperatures, so that relative responses to increasing CO2 concentration are more pronounced with increasing temperature (e.g., Kirschbaum and Farquhar 1984).
Many plants exposed to elevated CO2 concentrations exhibit photosynthetic down-regulation over exposure times of
weeks or longer (e.g., Gunderson and Wullschleger 1994,
Long et al. 1996, Wolfe et al. 1998). Partly, this has been explained as an experimental artifact, because downward acclimation tends to be more pronounced if plants are grown in
smaller pots (Arp 1991, Thomas and Strain 1991). However,
even under natural conditions, a degree of downward acclimation is expected if increased photosynthetic carbon gain is not
matched by a similarly increased nutrient supply, with the result that foliar nutrient concentrations and inherent
photosynthetic rates are reduced (e.g., Rastetter et al. 1992,
1997, Kirschbaum et al. 1994, 1998, Wolfe et al. 1998).
The responses depicted in Figure 2 point to significant potential increases in productivity in response to increasing CO2
concentration. However, plant growth is ultimately affected
not only by photosynthetic carbon gain, but also by nutritional
requirements and water relations. Calculated changes in photosynthesis are only part of the suite of effects that together
will determine plant productivity under changed conditions.
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changing temperature (Slatyer and Morrow 1977, Battaglia et
al. 1996). The acclimation potential of plants is illustrated in
Figure 3. Four different response patterns are shown. In all
cases, plants of the same species were grown under two contrasting growth conditions, as indicated by arrows in Figure 3,
and short-term photosynthetic responses were observed over a
range of temperatures.
Photosynthesis in all cases reached a maximum at some intermediate temperature. The sharpness of the peak at which
maximum photosynthesis occurred differed between species,
and between growth and measurement conditions. All species
displayed considerable potential for adaptation, with higher
optimum temperatures observed for plants acclimated to
higher growth temperatures. In general, it appears that optimum temperatures acclimate by about 0.5 ºC per 1.0 ºC
change in effective growth temperature (Berry and Björkman
1980, Battaglia et al. 1996).
In Nerium oleander L., photosynthetic rates at optimum
temperatures were similar at high and low growth temperatures, but in Atriplex sabulosa Rouy, maximum photosynthetic rates were higher in low-temperature grown plants, and
in Tidestromia oblongifolia (S. Watson) Standley maximum
photosynthetic rates were much higher in high-temperature
grown plants. This corresponded with the respective growth
habits of the different species: T. oblongifolia is a C4 plant native to hot Californian deserts, whereas A. sabulosa is a C4
plant native to cooler habitats. Although C4 plants are more
typically found in warmer and drier habitats than C3 plants
Responses of photosynthesis to temperature
Photosynthetic carbon gain can be strongly affected by temperature (e.g., Berry and Björkman 1980, Berry and Raison
1982). Photosynthesis is a biochemical process, and its overall
temperature dependence can be understood in terms of the
temperature dependencies of its component processes and
their interaction (Farquhar et al. 1980, Farquhar and von
Caemmerer 1982, Kirschbaum and Farquhar 1984). At low
temperatures, photosynthesis increases with increasing temperature, which is well described by the Arrhenius relationship (Nolan and Smillie 1976, Farquhar et al. 1980, Berry and
Raison 1982). At higher temperatures, photosynthesis decreases as a result of conformational changes in key enzymes
(Berry and Björkman 1980).
Plants have a considerable ability to adapt to their environments. Different species have evolved adaptations to their
thermal habitats (e.g., Björkman et al. 1974) and can display
considerable acclimation to actual growth conditions. For
long-lived foliage, this can involve acclimation to seasonally
Figure 3. Representative photosynthetic response patterns to temperature in three species (redrawn from Berry and Björkman 1980). Each
panel depicts the response of a species grown in contrasting temperatures. Circles depict the response of low-temperature grown plants,
and squares depict the response of high-temperature grown plants.
Arrows indicate the respective growth temperatures. Data in panels
(a)–(c) were obtained at ambient CO2 concentration, those in panel
(d) at elevated CO2. Original data from Björkman et al. (1975, 1978).
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(Tieszen et al. 1979, Rundel 1980), both groups are capable of
adaptation to a wide range of temperatures.
Figures 3c and 3d show the interaction between the temperature response of photosynthesis and CO2 concentration in the
C3 plant, N. oleander. At higher CO2 concentration, much
higher photosynthetic rates were possible (as in Figure 2). Additionally, the response curve to temperature changed, with
optimum temperature increasing with increasing CO2 concentration (Kirschbaum and Farquhar 1984, McMurtrie et al.
1992).
In C3 species at low CO2 concentration, photosynthesis is
limited by Rubisco activity, which shows little response to
temperature because effects on maximum capacity and the
Michaelis-Menten constant for CO2 largely cancel each other
out (Kirschbaum and Farquhar 1984). At high CO2 concentration, on the other hand, RuBP regeneration is the principal limitation to photosynthetic rate, and, because of the increase in
RuBP regeneration with increasing temperature (Nolan and
Smillie 1976), assimilation rate also increases with temperature (Kirschbaum and Farquhar 1984).
Photosynthetic responses to temperature are thus highly dependent on species and growth conditions as well as the external environment during measurements. However, all plants
appear to be capable of a high degree of adaptation to growth
conditions. It is also noteworthy that photosynthesis, at least in
the experimental plants shown here, could function adequately
up to nearly 50 °C provided that water supply was sufficient.
This finding suggests that even with considerable global
warming, photosynthesis is not likely to be significantly impaired; however, some species are able to acclimate more fully
than others. For example, A. sabulosa performed well when
grown at low temperatures, but photosynthetic rates were
much reduced for plants grown at high temperatures (Figure 3a). The opposite was true for T. oblongifolia (Figure 3b),
indicating that increased temperature is likely to favor
T. oblongifolia at the expense of A. sabulosa. Although some
species may function adequately at high temperatures, the differential response of species may alter competitive relationships between co-occurring species.
Effects on photosynthesis are likely to translate into effects
on net primary productivity. In a study of net primary production in different ecosystems of the world, Lieth (1973) expressed net primary production (NPP) as a function of mean
annual temperature (Figure 4). The relationship between temperature and NPP has also been the subject of a more recent
comprehensive model intercomparison (Cramer et al. 1999).
The strong effect of temperature is associated with the
length of the growing season, and to a lesser extent with increasing radiation at different latitudes. The data suggested
that NPP could increase substantially with increasing temperature, especially in systems that currently experience low mean
annual temperatures. The correlation between temperature
and radiation, however, is unlikely to hold in the future so that
somewhat smaller increases must be expected.
Forest growth in cool regions has been shown to increase
markedly with increasing temperature (Kauppi and Posch
1985, Beuker 1994, Proe et al. 1996), and it has been postulated that there could be significant growth enhancement with
Figure 4. Net primary production expressed as a function of temperature (redrawn from Lieth 1973). The compiled observations of NPP
are shown in (a) together with a curve fitted to the data. The relative
slope of the line, which gives the relative increase in NPP with temperature increase, is shown in (b).
global warming in forests in Finland (Kellomäki et al. 1997)
and Scotland (Proe et al. 1996). Where temperatures are already moderate to warm and productivity is limited by water
availability, however, productivity might decrease in response
to global warming as was found in simulations of loblolly pine
growth in the USA (McNulty et al. 1996). The effects of increasing temperature must be viewed not in isolation, but in
combination with effects of changing humidity, water availability and CO2 concentration (see below).
Temperature and CO2 effects on respiration rate
The carbon assimilated during photosynthesis is partly used
for maintenance respiration, and the remainder is used for
growth. Respiration rates increase in response to short-term
increases in temperature (Forward 1960). If these higher respiration rates were maintained for plants exposed to higher temperatures for longer periods, it would follow that, at higher
temperatures, a greater fraction of fixed carbon would be lost
in respiration, with less available for growth so that growth
rates would decrease with increasing temperature (Fitter and
Hay 1987, Woodwell 1987, Melillo et al. 1990).
However, studies have shown that the control of respiration
rate follows a more intricate pattern. Körner and Larcher
(1988), for example, grew the alpine plant, Vaccinum
myrtillus L. at 10 and 20 °C. When plants experienced a
short-term increase in temperature from 10 to 20 °C,
respiration rates approximately doubled (Figure 5). However,
respiration rate in plants grown and measured at 20 °C was
similar to the rate of plants grown and measured at 10 °C. The
observed short-term doubling in respiration rate with increased temperature was not observed when plants were able
to acclimate to the higher temperature.
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The acclimation response of plant respiration to temperature was more fully investigated by Gifford (1995) in an
experiment with Triticum aestivum L. He expressed his observations as the ratio of respiration rate to photosynthesis measured over 24 h (Figure 6).
When Gifford (1995) grew plants at 15 °C, he observed that
about 36% of carbon gained in photosynthesis was lost in respiration. When he transferred plants to 25 °C, there was an initial increase in the ratio of respiration rate to photosynthetic
rate over the first day, but that ratio decreased over subsequent
days. After 6 days, the ratio was similar to that observed at
15 °C. When plants were transferred back to 15 °C, there was
again an initial response to the new temperature. After another
4 days, however, the ratio was again similar to that at the
outset (Figure 6a).
When the ratio of respiration rate to photosynthetic rate was
expressed as a function of growth temperature in acclimated
plants (Figure 6b), there was a slight increase in the ratio with
increasing temperature (from 0.39 to 0.43 between 15 and
30 °C). Similar results were obtained with other species, including the tree species Pinus radiata D. Don and Eucalyptus
camaldulensis Dehnh. (Gifford 1994, R.M. Gifford, CSIRO
Plant Industry, pers. comm.). Hence, Gifford (1994, 1995) and
others (e.g., Körner 1996, Waring et al. 1998) concluded that
the ratio of respiration to photosynthesis does not deviate significantly from constancy over a range of temperatures, and
that increases in global temperature are not likely to lead to
significantly increased carbon losses in respiration.
There has also been much recent interest in the direct effect
of CO2 concentration on plant respiration rates (e.g., Amthor
1991, Gonzalez-Meler et al. 1996). Several studies have
shown a short-term reduction in respiration rate following
moderate increases in CO2 concentration (see Gonzalez-Meler
et al. 1996). However, it is not clear whether these short-term
responses lead to similar longer-term responses.
In longer-term experiments, respiration rates generally decrease with increasing CO2 concentration, but such findings
are not universal (Amthor 1991, Gonzalez-Meler et al. 1996,
Drake et al. 1999). Analysis is complicated because respiration rate responds to various plant internal factors, which are
Figure 5. Short-term response of respiration rate to temperature in
Vaccinum myrtillus plants grown at either 10 °C or 20 °C (redrawn
from Körner and Larcher 1988).
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Figure 6. Changes in the ratio of respiration rate to photosynthetic rate
in response to changes in temperature: (a) over time following a
change in temperature; and (b) as a function of temperature in fully
acclimated plants. Data redrawn from Gifford (1995). Plants in (a)
were initially grown at 15 ºC. Arrows indicate times when plants were
transferred first to 25 ºC and then back to 15 ºC.
usually altered by changes in ambient CO2 concentration. For
instance, plant tissue grown in high CO2 concentrations
usually has a lower nitrogen concentration than tissue grown
at low CO2 concentrations. Because respiration rate usually increases with increases in tissue nitrogen concentration, it is not
clear whether decreased respiration rate is a direct response to
increased CO2 concentration or an indirect response to lowered tissue nitrogen concentration.
Gifford (1995) studied the response of respiration to
changes in temperature and CO2 concentration, and expressed
his findings as the ratio of respiration rate to photosynthetic
rate over 24 h. Because there was no consistent effect of CO2
concentration on the ratio, Gifford (1995) concluded that, for
assessing the impacts of changing CO2 concentration and temperature, it would be best to assume that the ratio of respiration
rate to photosynthetic rate does not change.
Transpiration rate at different temperatures
Figure 7 shows saturated vapor pressure as a function of temperature. As a generalized approximation, the absolute humidity in the air can be defined as the vapor pressure that was at
equilibrium with the previous night’s diurnal minimum temperature (Running et al. 1987, Glassy and Running 1994). The
vapor pressure at equilibrium with daytime temperatures determines the humidity of the air inside leaves. The difference
between those two vapor pressures gives the vapor pressure
deficit (VPD) of the air, which is the principal driving force for
transpiration from plant canopies (Monteith 1965).
At arid sites, overnight cooling is often insufficient for dew
formation so that the absolute vapor pressure at these sites may
be determined at some other cooler location (Kimball et al.
1997). Similarly, in maritime locations, the humidity of the air
may be determined by air–sea exchange. However, the basic
principle embodied in Figure 7 is not affected by these additional considerations. The effective minimum temperature
must be understood to be the minimum temperature wherever
the absolute humidity of the air was last determined by condensation.
With global warming, both overnight minimum and daytime temperatures are likely to increase. If the diurnal temperature range does not change (but see discussion below) it will
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Figure 7. Saturated vapor pressure shown as a function of temperature, together with diurnal minimum and daytime temperatures. The
humidities at those temperatures determines the vapor pressure deficit
of the air. Saturated humidity in Pa is calculated as: e(T) = 610.78
exp[17.269 T / (T + 237.3)] where T is air temperature in ºC.
lead to an increase in vapor pressure deficit because the saturated vapor pressure curve is steeper at higher temperatures
than at lower temperatures (Figure 7).
Figure 8a shows the increase in vapor pressure deficit of the
air with global warming if there is no change in diurnal temperature range. The increase in vapor pressure deficit with increasing temperature is only marginally different for different
diurnal temperature ranges or daytime temperatures, with increases in VPD being between 5 and 6% °C – 1 over most temperature combinations. Only at very low temperatures does the
increase in VPD exceed 6% °C – 1; similarly, only at very high
base temperatures does the VPD increase fall below 5% °C – 1
(Figure 8a).
These changes in VPD can be used to compute increases in
transpiration rate with global warming. The calculations were
done with the Penman-Monteith equation (Monteith 1965,
Martin et al. 1989). Canopy and aerodynamic resistances,
given in the legend of Figure 8, were taken to represent typical
values for different canopy types.
Canopies differ in the way transpiration rates respond to environmental drivers. Forest canopies tend to be relatively open
so that transpiration rates often vary primarily as a function of
changes in vapor pressure deficit. Transpiration in grass
swards, on the other hand, is largely controlled by radiation interception, and transpiration rates are consequently less affected by variations in vapor pressure deficit (Jarvis and
McNaughton 1986). These differential effects are formalized
through canopy and aerodynamic resistances included in the
Penman-Monteith equation.
The simulations suggest only slight increases in transpiration rate with increasing VPD for grassland systems because
of the greater control of transpiration by net radiation rather
than by vapor pressure deficit. Calculated increases in transpiration rate range from 1% °C – 1 for canopies at 40 °C to about
4% °C – 1 at 5 °C (Figure 8b).
There is likely to be a greater increase in transpiration rate in
Figure 8. Change in vapor pressure deficit, VPD (a), and transpiration
rate with warming (b) and with warming plus stomatal closure in response to increased CO2 concentration (c). Change in vapor pressure
was calculated as a function of daytime temperature and for several
temperature ranges between daytime and overnight minimum
temperature. Transpiration rate was calculated with the Penman-Monteith equation, with an assumed diurnal temperature range
of 10 °C, net radiation = 400 W m –2, and parameters for aerodynamic
and canopy resistance representative for grasslands (100; 50 s m –1),
unstressed forests (25; 50 s m –1) and forests with reduced conductance because of some kind of stress (25; 200 s m –1). For calculations
in (c), canopy resistance, rc, was increased by 0, 5, 10 or 15% as indicated in the Figure.
forest systems (Figure 8b), because transpiration rate of forests is more strongly controlled by VPD than by absorbed net
radiation. Calculated increases ranged from 5% °C – 1 at 5 ºC to
2% °C – 1 at 40 °C. Calculated increases in transpiration were
even greater for forest systems under stress, with increases in
transpiration rate ranging from 3 to 6% °C – 1, because transpiration rate in stressed forests is even more strongly controlled
by VPD. These calculations imply that, under warmer conditions in the future, systems limited by the availability of water
are likely to use their available water more quickly, thereby
limiting plant growth.
Increased atmospheric CO2 concentration causes the
stomata of most plants to close to some extent (Eamus and
Jarvis 1989, Eamus 1991), and analysis of herbarium specimens has shown that the number of stomata has decreased
with increasing global CO2 concentration (Woodward 1987a).
Morison (1985) compiled a range of observations from the literature, and showed that stomatal conductance for C3 and C4
species was reduced by about 40% when CO2 concentration
was doubled. Several observations of tree species (Eamus and
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EFFECTS OF CLIMATE CHANGE ON FOREST GROWTH AND COMPOSITION
Jarvis 1989) suggest, however, that stomatal adjustment did
not occur or was minimal with increasing CO2, especially in
conifers (e.g., Marshall and Monserud 1996, Pataki et al.
1998). Marshall and Monserud (1996) studied trends in δ13C
observed in growth rings of three conifer species over this century, and concluded that the difference between ambient and
intercellular CO2 concentration (ca – ci) had remained constant, whereas the ratio of ci/ca has changed. This implies either that there were no changes in assimilation rate and
stomatal conductance despite the increasing atmospheric CO2
concentration, or that assimilation rate and stomatal conductance both increased. Such an implied increase in conductance
is the opposite of that observed in most other studies.
Any decrease in stomatal conductance would reduce transpiration rates. The effect of such partial stomatal closure was
determined by the Penman-Monteith equation, with a 1 °C increase in temperature plus some degree of stomatal closure
(Figure 8c). Stomatal closure by 10% almost completely negates the effect on transpiration of a 1 ºC increase in temperature. Stomatal closure by more than 10% leads to net
reductions of transpiration rates, whereas stomatal closure by
less than 10% leads to increased transpiration rates, but of
lesser magnitude than would occur without adjustments in
stomatal conductance (Figure 8c).
This example only indicates the sensitivity of plant systems
to the indicated changes, but ultimate outcomes will depend
largely on the relative rates of increase in CO2 concentration
and temperature, and the extent of physiological adjustment.
Greater relative temperature increases will lead to greater increases in transpiration rate, whereas greater relative increases
in CO2 concentration will lead to smaller increases, or a reduction, in transpiration. Similarly, species in which stomata are
more sensitive to CO2 concentration will experience less increase in transpiration rate than species with less sensitive
stomata.
These considerations all assume that there will be similar increases in minimum and maximum temperatures. However, it
is not clear whether the diurnal temperature range will remain
the same. The observed temperature increases to date have
been mainly caused by increases in nighttime temperature,
with only small increases in daytime temperatures in most regions (Karl et al. 1993, Nicholls et al. 1996). These patterns
are partly associated with an increase in cloudiness (Nicholls
et al. 1996).
Climate change simulations generally show slight decreases
in the diurnal temperature range, but there are several complex
feedback processes that can increase or counteract the relationship between greenhouse gases and the diurnal temperature range (Kattenberg et al. 1996). Although there will
probably be some decrease in diurnal temperature range in the
future, it is not possible to predict its extent (Kattenberg et al.
1996). A decrease in the temperature range would have the effect of reducing VPD and transpiration rates.
Under greenhouse conditions, all aspects of the hydrologic
cycle are likely to intensify so that rainfall will increase. The
outputs of 19 global circulation models were summarized for
the 1990 IPCC report (Cubasch and Cess 1990), and the modeled increases in temperature and precipitation are shown in
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Figure 9. The models differed in various aspects of their structure and parameterization, resulting in a range of temperature
sensitivities and associated increases in precipitation. Simulations that showed greater temperature increases generally also
predicted increases in global precipitation (Figure 9).
To derive a relationship between simulated changes in precipitation and temperature, a curve was fitted to the observations in Figure 9. This shows a mean increase in predicted
precipitation of 2.2% °C – 1 (see also Rind et al. 1997). Thus the
expected increases in precipitation may be insufficient to meet
the increased transpirational demand of many ecosystems unless stomatal closure significantly reduces transpiration rates,
with forests being more vulnerable than grasslands (Figure 8).
Although these data suggest that many forests will experience greater water limitations in the future, there will also be
great variability, with water status improving productivity in
some regions and worsening it in others. Increases in productivity in one region and decreases in another may partly cancel
each other out in terms of global productivity; however, ecological changes may occur in either case as the conditions to
which ecosystems had previously adapted are changed.
Potential evapotranspiration rates can be estimated by a variety
of equations based on varying physical rationales (cf. McKenney
and Rosenberg 1993). Some workers have used the Thornthwaite
method, which is based on the observed correlation between
evapotranspiration and temperature in the current climate
(Thornthwaite 1948). The method gives adequate estimates of
current transpiraiton rates, because the two basic drivers of
transpiration, radiation and vapor pressure deficit, tend to be
correlated with each other. However, that correlation is unlikely to persist in the future because temperature increases are
unlikely to be matched by corresponding increases in radiation.
Workers who have used the Thornthwaite method have concluded that water may become much more limiting with temperature increases in the future (e.g., Gleick 1987, Rind et al. 1990,
1997, Leichenko 1993). However, results based on the Penman-Monteith equation, which represent the relevant physical
processes more effectively, indicate that transpiration may not in-
Figure 9. Changes in temperature and precipitation simulated by 19
global circulation models. The fitted curve corresponds to a calculated increase in transpiration of 2.2% (oC) –1, calculated as ∆P =
1.022∆T (r 2 = 0.69) where ∆P is the percentage change in global modeled precipitation and ∆T is the modeled change in temperature. Data
were compiled by Cubasch and Cess (1990).
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KIRSCHBAUM
crease more than precipitation with global warming, or that the
difference will only be slight (Figures 8 and 9).
Integrating responses to temperature, CO2, and nutrient
and water availability.
Forest growth is ultimately determined by the interacting cycles of carbon, water and nutrients as shown in Figure 10
(Kirschbaum 1999a). Plants grow by fixing CO2 from the atmosphere, but in the diffusive uptake of CO2, trees inevitably
lose water. Water can be replenished from the soil as long as
adequate soil water is available. Otherwise, further water loss
must be prevented by stomatal closure, which also prevents
CO2 fixation.
The relationships between water loss and carbon gain are affected by temperature, which affects the vapor pressure deficit
and transpiration rate (Figure 8), and CO2 concentration,
which affects the rate of photosynthesis (Figure 2). With increasing temperature, more water is lost per unit carbon
gained, and with increasing CO2 concentration, more carbon
can be gained per unit water lost.
Plants also require nutrients, especially nitrogen. Most nitrogen is derived from the decomposition of soil organic matter. In the decomposition of soil organic matter, CO2 is
released to the atmosphere and any excess nitrogen is mineralized and becomes available for plant uptake. If plants are able
to fix more carbon through increased CO2 concentration but
nutrient uptake is limited, then plant internal nutrient status declines (e.g., Drake 1992, Tissue et al. 1993). This constitutes a
negative feedback effect of increasing CO2 concentration on
plant productivity. Plants that fix more carbon also produce
more litter, which adds to soil organic matter and immobilizes
nutrients. This reduces the nutrients available for plant uptake
and results in a second negative feedback effect (Rastetter et
al. 1992, 1997, Comins and McMurtrie 1993, Kirschbaum et
al. 1994, 1998).
Figure 10. Diagrammatic representation of the interrelationships between carbon, water and nutrient cycles. The diagram shows only nitrogen as representative of nutrients in the cycling system. Redrawn
from Kirschbaum (1999a).
These two processes restrict the possible positive response
of plant productivity to increasing CO2 concentration. However, temperature increases can also play a role. There are
likely to be only slight direct effects of increasing temperature
on plant function (Figures 4 and 6), but high temperatures can
increase the rate of organic matter decomposition and mineralization of nitrogen (Kirschbaum 2000). With increasing
temperature, more nutrients become available for plant uptake, stimulating plant productivity independently of any direct physiological plant responses to increasing temperature
(Schimel et al. 1990).
Figure 11 shows the relative temperature response of organic matter decomposition rate (after Kirschbaum 2000) and
net primary production (after Lieth 1973). Kirschbaum (2000)
reviewed the methods used to assess the temperature sensitivity of organic matter decomposition rate, and derived a relationship that best described the experimental values. Lieth’s
data compilation is presented in Figure 4.
Figure 11 shows that, with increasing temperature, the rate
of organic matter decomposition will be stimulated much
more than net primary production, so that nutrients will become more readily available in most circumstances. If it occurs, it will come at the expense of a decrease in soil organic
matter (Schimel et al. 1990, Kirschbaum 2000).
The combined growth response to these interacting factors
was investigated with the generic forest growth model, CenW
(Kirschbaum 1999a). Initial conditions for the model were obtained at a site near Canberra, Australia (Kirschbaum 1999b).
The base climate in Canberra is hot in summer and cool with frequent mild frosts in winter. Rainfall is extremely variable, but
generally insufficient to meet transpirational demand by trees.
Soil fertility is low (Kirschbaum 1999b). The model was run either under control conditions as observed (C), with fertilization
but no additional irrigation (F), with irrigation but no fertilizer
addition (I), or with both irrigation and fertilizer applied (IF). The
modeled growth responses to doubling CO2 concentration or increasing temperature by 2 °C are shown in Figure 12. These con-
Figure 11. Relative temperature response of net primary production
(NPP) (after Lieth 1973; see also Figure 4) and organic matter decomposition after Kirschbaum (2000). Net primary productivity was calculated as: NPP = 1.19/[1 + exp(1.315 – 0.119 T)]. The relative
decomposition rate, D, was calculated as: D = exp[5.19 (T – 25)/(T +
38.8)]. Parameters were adjusted so that relationships were normalized to 1 at 25 ºC.
TREE PHYSIOLOGY VOLUME 20, 2000
EFFECTS OF CLIMATE CHANGE ON FOREST GROWTH AND COMPOSITION
ditions were chosen to simulate growth responses under naturally
dry or wet and naturally fertile or infertile conditions.
With irrigation and fertilization (IF), responses were dominated by the direct physiological effects of either increasing
CO2 concentration or temperature. In response to doubling
CO2 concentration, there was an approximately 15–20% increase in productivity. The magnitude of that increase was
consistent with the magnitude of the direct photosynthetic response to doubled CO2 concentration (see Figure 2). There
was little consistent response to increasing temperature by
2 °C. The positive response to increasing temperature in some
years was caused by the alleviation of frost damage (assumed
to occur at nighttime temperatures below 0 °C) in years when
it was particularly severe. However, temperature increases
also led to increased heat damage (assumed to occur at daytime temperatures above 35 °C), which reduced productivity
in years that were already relatively warm. Simulated responses of productivity to temperature became more negative
with larger temperature increases (Kirschbaum 1999b).
With irrigation only (I), in response to doubling CO2 concentration, there was an initial increase in productivity by
about 10%, but the response was transient and within a few
years productivity was the same, or even less than, that of
plants grown at normal CO2 concentrations. In response to increasing temperature, on the other hand, there was a 10–20%
growth enhancement that continued to increase over time, but
with considerable year-to-year variation. The greatest positive
response was in Year 9, when an exceptionally cold winter
Figure 12. Growth response to a doubling of CO2 concentration or increasing ambient temperature by 2 oC under four different experimental conditions. Climatic conditions and initial values for soil organic
matter were those observed at an experimental site near Canberra,
Australia. The model was run with irrigation and fertilization applied
every five years (IF), with irrigation but no fertilization (I), with fertilizer but only natural rainfall (F) or with no additions at all (C). Climate change was imposed from Year 2, and stem wood production is
expressed relative to that of stands exposed to the current climate. Redrawn from Kirschbaum (1999b).
317
caused frost damage that could be prevented by a 2 ºC
temperature increase (as in the IF treatment).
In the irrigation treatment (I), there was little response to increasing CO2 concentration because water-use efficiency was
unimportant in this treatment. Furthermore, a transient increase in productivity led to increased litter production. Increased litter carbon then immobilized nitrogen in the soil and
reduced its subsequent availability to trees. Trees with lower
internal nutrient concentration also allocated a greater relative
proportion of biomass below ground that further reduced
aboveground growth to less than that of trees grown at normal
CO2 concentration. Conversely, with increased temperature
and the resultant increase in nutrient availability, a greater
fraction of carbon was allocated above ground so that
stemwood production was increased by an even greater proportion than total net primary production.
Under increased temperature, on the other hand, more nitrogen was mineralized and became available to plants. This
overcame the most critical growth limitation and considerably
enhanced growth. Increasing transpirational demand with increasing temperature played no role under irrigation. Other
negative effects of increasing temperature, such as growth under supra-optimal temperature, did affect plant growth, but the
consequences of the positive factors predominated.
In fertilized plants without irrigation (F), the simulated response was fundamentally different. There was little response
to temperature but a large growth increase in response to increased CO2 concentration. In response to doubled CO2 concentration, growth was increased by over 80% in the driest
year, and was enhanced by about 60% on average over all
years. Under these simulated conditions, growth was essentially limited by water availability and hence determined by
the efficiency with which a limited amount of water could be
used. Under doubled CO2 concentration, transpiration efficiency could be substantially increased, which greatly stimulated growth.
In the control (C), as in the fertilizer treatment (F), there was
little response to temperature, with a slight decrease in growth
in some seasons and a slight increase in others. In contrast,
there was a large response to increasing CO2 concentration,
with growth enhanced by up to 80% in the driest year and 40%
overall. In wet years, the growth response was smaller. In dry
years, growth was essentially limited by water use, and water-use efficiency was much enhanced under the higher CO2
conditions. In wet years, when water availability was not limiting growth, the response to CO2 was more modest because
only the direct photosynthetic response to CO2 gave a benefit.
This benefit was further reduced by some nitrogen being immobilized by the higher previous carbon production and subsequently increased litter fall.
When CO2 concentration and temperature were both increased, growth responses were similar to the sum of the responses to temperature and CO2 concentration individually
(Figure 13). Combined responses were dominated by the response to increasing CO2 concentration, with peak responses being similar to responses to CO2 concentration alone, but in years
when responses to CO2 concentration were only weak, additional
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318
KIRSCHBAUM
increases in temperature maintained the combined response at a
higher overall level.
These simulations showed that there is not one unique sensitivity of plant productivity to increasing CO2 concentration and
temperature, but that responses are highly dependent on circumstances. Responses are likely to range from negative under some
circumstances to increases of at least 50% in response to doubling CO2 concentration under conditions where plants are
strongly water limited, but where other limitations are slight.
Where growth is limited by nitrogen nutrition, time becomes a further complicating factor. Forest stands might be
currently limited by nitrogen availability, but systems with nitrogen-fixing plants can increase their nitrogen stocks over
time if other potentially growth-limiting factors become more
favorable. Nitrogen limitations that might prevent full use of
more favorable climatic conditions in the short term could thus
diminish over time. However, growth increases in response to
enhanced nitrogen mineralization resulting from increased
temperature could also be lost over longer periods, because excess nitrogen is eventually lost from the system, and the system then attains a new equilibrium with lower nitrogen status
and growth rate when inputs and outputs are again balanced.
These simulations show that it is difficult to generalize the response of forests to increasing temperature and CO2 concentration. Changes in rainfall patterns will further complicate the
overall assessment. Hence, the response of individual forest
stands to any or all of these environmental changes can only be
predicted if the key limitations in each system have been studied
thoroughly so that the magnitude of various responses can be
assessed, and feedbacks in the system taken into account when
predicting overall responses.
The complexity of these interactions has been recognized
by forest growth modelers in recent years, and attempts have
been made to devise models that adequately describe the
growth response of whole ecosystems (e.g., Kellomäki et al.
1997, King et al. 1997, Valentine et al. 1998). The model comparison of Ryan et al. (1996) was particularly interesting, because it compared the responses predicted by a range of forest
Figure 13. Growth response to a doubling of CO2 concentration, a
2 °C increase in ambient temperature, or both together under control
conditions. The modeling conditions are described in Figure 12.
growth models for the same sites and under the same climate
change scenarios. The models available at that time gave a
range of diverging predictions, illustrating that the understanding of ecosystem processes was not yet sufficient to
make future predictions, even if all ecosystem parameters
were fully known or prescribed.
Species distributions
In addition to its effect on the ecophysiology of forests, climate change can affect the suitability of various locations for
different species (Kirschbaum et al. 1996). In trying to assess
the probable impact of climate change, an important distinction must be made between a species’ fundamental niche and
its realized niche (Hutchinson 1957, Austin 1992, Malanson et
al. 1992). The fundamental niche encompasses the set of environmental conditions in which a species could potentially
grow and reproduce if there were no competition from other
species. Its realized niche is the range of conditions under
which it actually occurs while subject to competition (e.g.,
Booth et al. 1988, Malanson et al. 1992).
In some cases, fundamental and realized niches coincide,
such as for species limited by extreme environmental stresses
(Woodward 1987b). For example, plants can only tolerate extreme temperatures (e.g., –60 ºC) if they have special adaptive
features. Tolerance to milder limits (like 0 ºC), on the other
hand, is attainable by many species through subtle shifts in
membrane composition or other minor adjustments. Hence, it
is more likely that realized and fundamental niches coincide at
a –60 ºC boundary than a 0 ºC degree boundary.
It is more typical for a species’ fundamental niche to be
wider than its realized niche (Austin 1992). Competitive interactions with other species usually restrict species’ actual distributions to subsets of their fundamental niche. A species’
realized niche may also be restricted for historical reasons. For
example, an area may be currently suitable for a species, but
the species may have become extinct in that location during
the last ice age and its re-invasion prevented by slow dispersal
or physical barriers, e.g., waterways between islands.
One can use the observed distribution of species as an initial
guide to the likely impact of climate change. Figure 14 shows the
observed distribution of Eucalyptus fastigata H. Deane &
Maiden as a function of temperature in its natural habitat in
southeastern Australia. These observations define the realized
niche of this species.
Most species have even narrower niches than that of
E. fastigata. Hughes et al. (1996a, 1996b) mapped the distribution of 819 eucalypt species in Australia, and related their
observed occurrence to mean annual temperature and rainfall
over that range (Figure 15). Eucalyptus fastigata (Figure 14),
for example, was recorded to occur over a range of 6–7ºC.
Of all species analyzed by Hughes et al. (1996a, 1996b),
one quarter had distributions that ranged over only 1 ºC or less,
and over 50% of all species had distributions of 3 ºC or less.
Only a small number of species were generalists, with about
5% of species distributed over a range of temperatures greater
than 10 ºC (Figure 15).
The observations of Hughes et al. (1996a, 1996b) provide
TREE PHYSIOLOGY VOLUME 20, 2000
EFFECTS OF CLIMATE CHANGE ON FOREST GROWTH AND COMPOSITION
Figure 14. Observed probability of occurrence of Eucalyptus
fastigata in southeastern Australia as a function of mean annual temperature (redrawn from Austin 1992).
an initial assessment of potential impacts, but such an analysis
is by necessity restricted to the observed distribution of species. For rarer species, the observations will sometimes be incomplete. Consideration of this factor would shift the actual
frequency distribution to the right in Figure 15.
In some instances, the narrow distribution of a species may
not be related to the climate, but to soil type or other non-climatic aspects of the environment. That species might continue
to be highly competitive in its current habitat even with considerable warming. On the other hand, it may also be particularly vulnerable to climate change, because it may not be able
to migrate to a different region if it were outcompeted in its
current habitat in a warmer climate.
The observed correlation of species distributions with climate factors may sometimes reflect causal relationships between species distributions and some other factor, such as fire
frequency, that in the past has been correlated with temperature. As an approximation, one can assume that such correlations will persist in the future. It may also be possible to
initiate management changes and break the correlation with
the climate to protect some vulnerable species.
Nonetheless, despite various caveats, the information in
Figure 15 reveals the ecological vulnerability of many species
319
to climate change. With climate change, the distribution of
suitable habitats for a given species will change. If there is any
change in temperature, water availability or climate attributes
that are indirectly linked to climate, such as fire frequency, individuals at particular locations may find themselves outside
their realized or fundamental niche. Predictions of future
trends in species distributions would be easy if realized and
fundamental niches coincided. However, the ultimate success
of many species will be determined by interactions between
species and these outcomes are notoriously difficult to predict
(e.g., Landsberg and Stafford Smith 1992, Davis et al. 1998).
It has been argued that predictions of catastrophic species
decline may be overly pessimistic because they are based on
analyses relying on observed realized niches of species
(Malanson et al. 1992, Loehle 1996). On the other hand, pressure from climate changes will add to other pressures that ecosystems already endure, such as habitat destruction and
fragmentation and invasion by exotic species, so that the ultimate ecological effects on many species could be severe
(Skole and Tucker 1993, Fearnside 1995, Phillips 1997,
Bazzaz 1998).
Although the differences between fundamental and realized
niches cause difficulties in predicting change over time, the direction of change can be anticipated based on observation of
the realized niches. For many species with narrow temperature
niches (Figures 14 and 15), a temperature increase of only 2 °C
could change the environment from being suitable to totally
unsuitable. This could occur either because some tolerance
thresholds are exceeded or because competing species are
better able to make use of the altered growing conditions. Additionally, there are aspects of the emerging climate, such as
higher CO2 concentration, that have no recent historic parallels. Future species interactions may also be different from
current interactions because they depend partly on historical
factors, and interactions may be modified by the loss of some
species that were unable to adapt to changing conditions.
Finally, there is the problem that the future climate is not likely
to stabilize at some new level but will continue to change for
as long as the concentration of greenhouse gases continues to
increase.
Some species will be favored and others adversely affected
by changed conditions. This will change the competitive interactions between species and lead to changes in the species
composition of forests. Species with narrow temperature tolerances, that grow slowly or have poor dispersal mechanisms
are likely to be lost, whereas species with broader tolerances
or which complete their life cycle more quickly, such as early
successional trees and shrubs, and those with greater dispersal
mechanisms will succeed. For many forests, this could lead to
the loss of many species with currently narrow distributions,
whereas species that can tolerate the new conditions or that
have the potential to invade newly suitable habitats will persist.
Acknowledgments
Figure 15. Environmental niches for 819 Australian eucalypt species.
Redrawn from Hughes et al. (1996b).
This work contributes to CSIRO’s Climate Change Research Program. I thank the organizers of the Conference “Process-Based
Models for Forest Management” for supporting my conference atten-
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KIRSCHBAUM
dance in Finland, and Michael Battaglia, Roger Gifford and John Raison for many helpful comments on the manuscript.
References
Amthor, J.S. 1991. Respiration in a future, higher-CO2 world. Plant
Cell Environ. 14:13–20.
Arp, W.J. 1991. Effects of source-sink relations on photosynthetic acclimation to elevated CO2. Plant Cell Environ. 14:869–875.
Austin, M.P. 1992. Modelling the environmental niche of plants: implications for plant community response to elevated CO2 levels.
Aust. J. Bot. 40:615–630.
Ball, J.T., I.E. Woodrow and J.A. Berry. 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. Ed. J. Biggins. Martinus Nijhoff,
Dordrecht, pp 221–224.
Battaglia, M., C. Beadle and S. Loughhead. 1996. Photosynthetic
temperature response of Eucalyptus globulus and Eucalyptus
nitens. Tree Physiol. 16:81–89.
Bazzaz, F.A. 1998. Tropical forests in a future climate: changes in biological diversity and impact on the global carbon cycle. Clim.
Change 39:317–336.
Berry, J. and O. Björkman. 1980. Photosynthetic response and adaptation to temperature in higher plants. Annu. Rev. Plant Physiol.
31:491–543.
Berry, J.A. and J.K. Raison. 1982. Responses of macrophytes to temperature. In Physiological Plant Ecology I. Responses to the
Physical Environment, Encyclopedia of Plant Physiology, New
Series Vol. 12A. Eds. O.L. Lange, P.S. Nobel, C.B. Osmond and
H. Ziegler. Springer-Verlag, Berlin, pp 277–338.
Beuker, E. 1994. Long-term effects of temperature on the wood production of Pinus sylvestris L. and Picea abies (L.) Karst. in old
provenance experiments. Scand. J. For. Res. 9:34–45.
Björkman, O., M. Nobs, H.A. Mooney, J. Troughton, J. Berry,
F. Nicholson and W. Ward. 1974. Growth responses of plants from
habitats with contrasting thermal environments: transplant studies
in the Death Valley and the Bodega Head experimental gardens.
Carnegie Inst. Wash. Year Book 73:748–757.
Björkman, O., H.A. Mooney and J. Ehleringer. 1975. Photosynthetic
responses of plants from habitats with contrasting thermal environments: comparison of photosynthetic characteristics of intact
plants. Carnegie Inst. Wash. Year Book 74:743–748.
Björkman, O., M. Badger and P.A. Armond. 1978. Thermal acclimation of photosynthesis: effect of growth temperature on photosynthetic characteristics and components of the photosynthetic
apparatus in Nerium oleander. Carnegie Inst. Wash. Year Book
77:262–282.
Booth, T.H., H.A. Nix, M.F. Hutchinson and T. Jovanovic. 1988.
Niche analysis and tree species introduction. For. Ecol. Manage.
23:47–59.
Comins, H.N. and R.E. McMurtrie. 1993. Long-term biotic response
of nutrient-limited forest ecosystems to CO2-enrichment; equilibrium behaviour of integrated plant-soil models. Ecol. Appl.
3:666–681.
Cramer, W.P., D.W. Kicklighter, A. Bondeau, B. Moore, III,
G. Churkina, B. Nemry, A. Ruimy and A.L. Schloss. 1999. Comparing global models of terrestrial net primary productivity (NPP):
overview and key results. Global Change Biol. 5:1–15.
Cubasch, U. and R.D. Cess. 1990. Processes and modelling. In Climate Change. The IPCC Scientific Assessment. Eds. J.T. Houghton, G.J. Jenkins and J.J. Ephraums. Cambridge University Press,
Cambridge, pp 69–91.
Cure, J.D. and B. Acock. 1986. Crop responses to carbon dioxide
doubling: a literature survey. Agric. For. Meteorol. 38:127–145.
Davis, A.J., L.S. Jenkinson, J.H. Lawton, B. Shorrocks and S. Wood.
1998. Making mistakes when predicting shifts in species range in
response to global warming. Nature 39:783–786.
Drake, B.G. 1992. A field study of the effects of elevated CO2 on ecosystem processes in a Chesapeake Bay wetland. Aust. J. Bot.
40:579–595.
Drake, B.G., J. Azcon-Bieto, J. Berry, J. Bunce, P. Dijkstra, J. Farra,
R.M. Gifford, M.A. Gonzalez-Meler, G. Koch, H. Lambers,
J. Siedow and S. Wullschleger. 1999. Does elevated atmospheric
CO2 concentration inhibit mitochondrial respiration in green
plants? Plant Cell Environ. 22:649–647.
Eamus, D. 1991. The interaction of rising CO2 and temperature with
water use efficiency. Plant Cell Environ. 14:843–852.
Eamus, D. and P.G. Jarvis. 1989. The direct effects of increase in the
global atmospheric CO2 concentration on natural and commercial
temperate trees and forests. Adv. Ecol. Res. 19:1–55.
Farquhar, G.D. and S. von Caemmerer. 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. 12B. Eds. O.L.
Lange, P.S. Nobel, C.B. Osmond and H. Ziegler. Springer-Verlag,
Berlin, pp 549–588.
Farquhar, G.D., S. von Caemmerer and J. Berry. 1980. A biochemical
model of photosynthetic CO2 assimilation in leaves of C3 species.
Planta 149:78–90.
Fearnside, P.M. 1995. Potential impacts of climatic change on natural
forests and forestry in Brazilian Amazonia. For. Ecol. Manage.
78:51–70.
Fitter, A.H. and R.K.M. Hay. 1987. Environmental physiology of
plants, 2nd Edn. Academic Press, San Diego, California, 421 p.
Forward, D.F. 1960. Effect of temperature on respiration. In Encyclopedia of plant physiology Vol. 12, No. 2. Ed. W. Ruhland.
Springer-Verlag, Berlin, pp 234–258.
Gifford, R.M. 1994. The global carbon cycle: a viewpoint on the
missing sink. Aust. J. Plant Physiol. 21:1–15.
Gifford, R.M. 1995. Whole plant respiration and photosynthesis of
wheat under increased CO2 concentration and temperature:
long-term vs. short-term distinctions for modelling. Global
Change Biol. 1:385–396.
Glassy, J.M. and S.W. Running. 1994. Validating diurnal climatological logic of the MT-CLIM model across a climatic gradient in Oregon. Ecol. Appl. 4:248–257.
Gleick, P. 1987. Regional hydrologic consequences of increases in
atmospheric CO2 and other trace gases. Clim. Change 10:137–161.
Gonzalez-Meler, M.A., B.G. Drake and J. Azcon-Bieto. 1996. Rising
atmospheric carbon dioxide and plant respiration. In SCOPE
56—Global Change: Effects on Coniferous Forests and
Grasslands. Eds. A.I. Breymeyer, D.O. Hall, J.M. Melillo and G.I.
Ågren. John Wiley & Sons Ltd., Chichester, pp 161–181.
Gunderson, C.A. and S.D. Wullschleger. 1994. Photosynthetic acclimation in trees to rising atmospheric CO2: a broader perspective.
Photosynth. Res. 39:369–388.
Hughes, L., E.M. Cawsey and M. Westoby. 1996a. Geographic and
climatic range sizes of Australian eucalypts and a test of
Rapoport’s rule. Glob. Ecol. Biogeog. Lett. 5:128–142.
Hughes, L., E.M. Cawsey and M. Westoby. 1996b. Climatic range
sizes of Eucalyptus species in relation to future climate change.
Glob. Ecol. Biog. Lett. 5:23–29.
Hutchinson, G.E. 1957. Concluding remarks. Cold Spring Harbor
Symp. Quant. Biol. 22:415–427.
TREE PHYSIOLOGY VOLUME 20, 2000
EFFECTS OF CLIMATE CHANGE ON FOREST GROWTH AND COMPOSITION
IPCC, 1996. Technical summary. In Climate Change 1995. The
Science of Climate Change. Eds. J.T. Houghton, L.G. Meira Filho,
B.A. Callander, N. Harris, A. Kattenberg and K. Maskell. Cambridge University Press, Cambridge, pp 9–49.
Jarvis, P.G. and K.G. McNaughton. 1986. Stomatal control of transpiration: scaling up from leaf to region. Adv. Ecol. Res. 15:1–49.
Jones, P.D. 1994. Hemispheric surface air temperature variations: a
reanalysis and an update to 1993. J. Climatol. 7:1794–1802.
Karl, T.R., P.D. Jones, R.W. Knight, G. Kukla, N. Plummer,
V. Razuvayev, K.P. Gallo, J. Lindseay, R.J. Charlson and T.C. Peterson. 1993. A new perspective on recent global warming: asymmetric trends of daily maximum and minimum temperature. Bull.
Am. Meteorol. Soc. 74:1007–1023.
Kattenberg, A., F. Giorgi, H. Grassl, G.A. Meehl, J.F.B. Mitchell,
R.J. Stouffer, T. Tokioka, A.J. Weaver and T.M.L. Wigley. 1996.
Climate models—projections of future climate. In Climate Change
1995. The Science of Climate Change. Eds. J.T. Houghton, L.G.
Meira Filho, B.A. Callander, N. Harris, A. Kattenberg and
K. Maskell. Cambridge University Press, Cambridge, pp 285–357.
Kauppi, P. and M. Posch. 1985. Sensitivity of boreal forests to possible climatic warming. Clim. Change 7:45–54.
Kellomäki, S., T. Karjalainen and H. Väisänen. 1997. More timber
from boreal forests under changing climate? For. Ecol. Manage.
94:195–208.
Kimball, B.A. 1983. Carbon dioxide and agricultural yield: an
assemblage and analysis of 430 prior observations. Agron.
J. 75:779–788.
Kimball, J.S., S.W. Running and R. Nemani. 1997. An improved
method for estimating surface humidity from daily minimum temperature. Agric. For. Meteorol. 85:87–98.
King, A.W., W.M. Post and S.D. Wullschleger. 1997. The potential
response of terrestrial carbon storage to changes in climate and atmospheric CO2. Clim. Change 35:199–227.
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
Environ. 17:747–754.
Kirschbaum, M.U.F. 1999a. CenW, a forest growth model with
linked carbon, energy, nutrient and water cycles. Ecol.
Model.181:17–59.
Kirschbaum, M.U.F. 1999b. Modelling forest growth and carbon
storage under changed climatic conditions. Tellus 51B:871–888.
Kirschbaum, M.U.F. 2000. Will changes in soil organic matter act as
a positive or negative feedback on global warming? Biogeochemistry 48:21–51.
Kirschbaum, M.U.F. and G.D. Farquhar. 1984. Temperature dependence of whole-leaf photosynthesis in Eucalyptus pauciflora Sieb.
ex Spreng. Aust. J. Plant Physiol. 11:519–538.
Kirschbaum, M.U.F., D.A. King, H.N. Comins, R.E. McMurtrie, B.E.
Medlyn, S. Pongracic, D. Murty, H. Keith, R.J. Raison, P.K.
Khanna and D.W. Sheriff. 1994. Modelling forest response to increasing CO2 concentration under nutrient-limited conditions.
Plant Cell Environ. 17:1081–1099.
Kirschbaum, M.U.F., A. Fischlin, M.G.R. Cannell, R.V. Cruz,
W. Galinski and W.A. Cramer. 1996. Climate change impacts on
forests. In Climate Change 1995: Impacts, Adaptations and
Mitigation of Climate Change: Scientific-Technical Analyses.
Contribution of Working Group II to the Second Assessment
Report of the Intergovernmental Panel on Climate Change. Eds.
R.T. Watson, M.C. Zinyowera and R.H. Moss. Cambridge University Press, Cambridge and New York, pp 131–158.
321
Kirschbaum, M.U.F., B. Medlyn, D.A. King, S. Pongracic, D. Murty,
H. Keith, P.K. Khanna, P. Snowdon and J.R. Raison. 1998.
Modelling forest-growth response to increasing CO2 concentration
in relation to various factors affecting nutrient supply. Global
Change Biol. 4:23–42.
Körner, C. 1996. The response of complex multispecies systems to elevated CO2. In Global Change and Terrestrial Ecosystems. Eds.
B.H. Walker and W.L. Steffen. Cambridge University Press, pp
20–43.
Körner, C. and W. Larcher. 1988. Plant life in cold climates. In Plants
and Temperature. Eds. S.F. Long, and F.I. Woodward. Symp. Soc.
Exp. Biol. 42, The Company of Biol. Ltd., Cambridge, pp 25–57.
Landsberg, J. and M. Stafford Smith. 1992. A functional scheme for
predicting the outbreak potential of herbivorous insects under
global climate change. Aust. J. Bot. 40:565–577.
Leichenko, R.M. 1993. Climate change and water resource availability: an impact assessment for Bombay and Madras, India. Water
Intern. 18:147–156.
Lieth, H. 1973. Primary production: terrestrial ecosystems. Hum.
Ecol. 1:303–332.
Loehle, C. 1996. Forest response to climate change: do simulations
predict unrealistic dieback? J. For. 94:13–15.
Long, S.P., C.P. Osborne and S.W. Humphries. 1996. Photosynthesis,
rising atmospheric carbon dioxide concentration and climate
change. In SCOPE 56—Global Change: Effects on Coniferous
Forests and Grasslands. Eds. A.I. Breymeyer, D.O. Hall, J.M.
Melillo and G.I. Ågren. John Wiley & Sons Ltd., Chichester, pp
121–159.
Luxmoore, R.J., S.D. Wullschleger and P.J. Hanson. 1993. Forest responses to CO2 enrichment and climate warming. Water Air Soil
Pollut. 70:309–323.
Malanson, G.P., W.E. Westman and Y.-L. Yan. 1992. Realized versus fundamental niche functions in a model of chaparral response
to climatic change. Ecol. Model. 64:261–277.
Marshall, J.D. and R.A. Monserud. 1996. Homeostatic gas-exchange
parameters inferred from 13C/12C in tree rings of conifers.
Oecologia 105:13–21.
Martin, P., N. Rosenberg and M.S. McKenney. 1989. Sensitivity of
evapotranspiration in a wheat field, a forest and a grassland to
changes in climate and direct effects of carbon dioxide. Clim.
Change 14:117–151.
McKenney, M.S. and N.J. Rosenberg. 1993. Sensitivity of some potential evapotranspiration estimation methods to climate change.
Agric. For. Meteorol. 64:81–110.
McMurtrie, R.E., H.N. Comins, M.U.F. Kirschbaum and Y.-P. Wang.
1992. Modifying existing forest growth models to take account of
effects of elevated CO2. Aust. J. Bot. 40:657–677.
McNulty, S.G., J.M. Vose and W.T. Swank. 1996. Potential climate
change effects on loblolly pine forest productivity and drainage
across the southern United States. Ambio 25:449–453.
Melillo, J.M., T.V. Callaghan, F.I. Woodward, E. Salati and S.K.
Sinha. 1990. Effects on ecosystems. In Climate Change: the IPCC
Scientific Assessment. Eds. J.T. Houghton, G.J. Jenkins and J.J.
Ephraums. Cambridge University Press, Cambridge, pp 283–310.
Monteith, J.L. 1965. Evaporation and environment. Symp. Soc. Exp.
Biol. 19:205–234.
Morison, J.I.L. and R.M. Gifford.1983. Stomatal sensitivity to carbon
dioxide and humidity. Plant Physiol. 71:789–796.
Morison, J.I.L. 1985. Sensitivity of stomata and water use efficiency
to high CO2. Plant Cell Environ. 8:467–474.
TREE PHYSIOLOGY ON-LINE at http://www.heronpublishing.com
322
KIRSCHBAUM
Nicholls, N., G.V. Gruza, J. Jouzel, T.R. Karl, L.A. Ogallo and D.E.
Parker. 1996. Observed climate variability and change. In Climate
Change 1995. The Science of Climate Change. Eds: J.T. Houghton,
L.G. Meira Filho, B.A. Callander, N. Harris, A. Kattenberg and
K. Maskell. Cambridge University Press, Cambridge, pp 133–192.
Nolan, W.G. and R.M. Smillie. 1976. Multi-temperature effects on
Hill reaction activity of barley chloroplasts. Biochim. Biophys.
Acta 440:461–475.
Pataki, D.E., R. Oren and D.T. Tissue. 1998. Elevated carbon dioxide
does not affect average canopy stomatal conductance of Pinus
taeda L. Oecologia 117:47–52.
Pearcy, R.W., K. Osteryoung and D. Randall. 1982. Carbon dioxide
exchange characteristics of C4 Hawaiian Euphorbia species native
to diverse habitats. Oecologia 55:333–341.
Phillips, O.L. 1997. The changing ecology of tropical forests. Biodivers. Conserv. 6:291–311.
Polley, H.W., J.M. Norman, T.J. Arkebauer, E.A. Walter-Shea, D.H.
Greegor, Jr. and B. Bramer. 1992. Leaf gas exchange of Andropogon gerardii Vitman, Panicum virgatum L. and Sorghastrum
nutans (L.) Nash in a tallgrass prairie. J. Geophys. Res. 97:
18837–18844.
Proe, M.F., S.M. Allison and K.B. Matthews. 1996. Assessment of
the impact of climate change on the growth of Sitka spruce in Scotland. Can. J. For. Res. 26:1914–1921.
Rastetter, E.B., R.B. McKane, G.R. Shaver and J.M. Melillo. 1992.
Changes in C storage by terrestrial ecosystems: how C–N interactions restrict responses to CO2 and temperature. Water Air Soil
Pollut. 64:327–344.
Rastetter, E.B., G.I. Ågren and G.R. Shaver. 1997. Responses of
N-limited ecosystems to increased CO2: a balanced-nutrition, coupled-element-cycles model. Ecol. Appl. 7:444–460.
Rawson, H.M. 1992. Plant responses to temperature under conditions
of elevated CO2. Aust. J. Bot. 40:473–490.
Rind, D., R. Goldberg, J. Hansen, C. Rosenzweig and R. Ruedy.
1990. Potential evapotranspiration and the likelihood of future
drought. J. Geophys. Res. 95:9983–10004.
Rind, D., C. Rosenzweig and M. Stieglitz. 1997. The role of moisture
transport between ground and atmosphere in global change. Annu.
Rev. Energy Environ. 22:47–74.
Rundel, P.W. 1980. The ecological distribution of C4 and C3 grasses
in the Hawaiian islands. Oecologia 45:354–359.
Running, S.W., R.R. Nemani and R.D. Hungerford. 1987. Extrapolation of synoptic meteorological data in mountainous terrain, and its
use for simulating forest evapotranspiration. Can. J. For. Res.
17:472–483.
Ryan, M.G., R.E. McMurtrie, G.I. Ågren, E.R. Hunt, Jr., J.D. Aber,
A.D. Friend, E.B. Rastetter and W.M. Pulliam. 1996. Comparing
models of ecosystem function for temperate conifer forests. II.
Simulations of the effect of climate change. In SCOPE 56—Global
Change: Effects on Coniferous Forests and Grasslands. Eds. A.I.
Breymeyer, D.O. Hall, J.M. Melillo and G.I. Ågren. John Wiley
and Sons Ltd., Chichester, pp 363–387.
Schimel, D., D. Alves, I. Enting, M. Heimann, F. Joos, D. Raynaud,
T. Wigley, M. Prather, R. Derwent, D. Ehhalt, P. Fraser,
E. Sanhueza, X. Zhou, P. Jonas, R. Charlson, H. Rohde,
S. Sadasivan, K.P. Shine, Y. Fouquart, V. Ramaswamy, S. Solomon, J. Srinivasan, D. Albritton, R. Derwent, I. Isaksen, M. Lal and
D. Wuebbles. 1996. Radiative forcing of climate change. In The
Science of Climate Change. Eds. J.T. Houghton, L.G. Meira Filho,
B.A. Callander, N. Harris, A. Kattenberg and K. Maskell. Climate
Change 1995, Cambridge University Press, Cambridge, pp
65–131.
Schimel, D.S., W.J. Parton, T.G.F. Kittel, D.S. Ojima and C.V. Cole.
1990. Grassland biogeochemistry: links to atmospheric processes.
Clim. Change 17:13–25.
Skole, D. and C. Tucker. 1993. Tropical deforestation and habitat
fragmentation in the Amazon: satellite data from 1978 to 1988.
Science 260:1905–1910.
Slatyer, R.O. and P.A. Morrow. 1977. Altitudinal variation in the
photosynthetic characteristics of snow gum, Eucalyptus pauciflora
Sieb. ex Spreng. Seasonal changes under field conditions in the
Snowy Mountains of south-eastern Australia. Aust. J. Bot.
25:1–20.
Thomas, R.B. and B.R. Strain. 1991. Root restriction as a factor in
photosynthetic acclimation of cotton seedlings grown in elevated
carbon dioxide. Plant Physiol. 96:627–634.
Thornthwaite, C.W. 1948. An approach towards a rational classification of climate. Geograph. Rev. 38:55–94.
Tieszen, L.L., M.M. Senyimba, S.K. Imbamba and J.H. Troughton.
1979. The distribution of C3 and C4 grasses and carbon isotope discrimination along an altitudinal and moisture gradient in Kenya.
Oecologia 37:337–350.
Tissue, D.L., R.B. Thomas and B.R. Strain. 1993. Long-term effects
of elevated CO2 and nutrients on photosynthesis and Rubisco in
Loblolly pine seedlings. Plant Cell Environ. 16:859–865.
Valentine, H.T., T.G. Gregoire, H.E. Burkhart and D.Y. Hollinger.
1998. Projections of growth of loblolly pine stands under elevated
temperature and carbon dioxide. In The Productivity and
Sustainability of Southern Forest Ecosystems in a Changing
Environment. Eds. R.A. Mickler and S. Fox. Springer-Verlag,
New York, pp 341–352.
Waring, R.H., J.J. Landsberg and M. Williams. 1998. Net primary
production of forests—a constant fraction of gross primary production. Tree Physiol. 18:129–134.
Wolfe, D.W., R.M. Gifford, D. Hilbert and Y.Q. Luo. 1998. Integration of photosynthetic acclimation to CO2 at the whole-plant level.
Global Change Biol. 4:879–893.
Woodward, F.I. 1987a. Stomatal numbers are sensitive to increases in
CO2 from pre-industrial levels. Nature 327:617–618.
Woodward, F.I. 1987b. Climate and plant distribution. Cambridge
University Press, Cambridge, 174 p.
Woodwell, G.M. 1987. Forests and climate: surprises in store.
Oceanus 29:71–75.
TREE PHYSIOLOGY VOLUME 20, 2000