Forest growth and species distribution in a changing climate

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1 Tree Physiology 20, 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 CO 2 concentration can increase photosynthetic rates, with the greatest increases likely to be in C 3 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 CO 2 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 CO 2 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: CO 2, 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 CO 2 from the atmosphere to the sites of photosynthesis within leaves. To take up CO 2, plants must open their stomata, which results in the outward diffusion of water. Increases in atmospheric CO 2 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 CO 2 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. 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 How is the climate changing? The atmospheric CO 2 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-

2 310 KIRSCHBAUM 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 CO 2 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 CO 2 concentration may reach 700 µmol mol 1 before the end of the 21st century (Schimel et al. 1996). These increases in CO 2 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 CO 2 concentration Of the projected aspects of atmospheric and climate change, the increase in atmospheric CO 2 concentration is the most certain. It has been shown in many experimental studies that photosynthesis in C 3 plants, including trees, responds strongly to CO 2 concentration, with photosynthesis typically increasing 25 75% for a doubling in CO 2 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 CO 2 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 CO 2 concentration at different temperatures (Kirschbaum 1994). Figure 2 shows rates of photosynthesis at elevated atmospheric CO 2 concentrations relative to rates at preindustrial atmospheric CO 2 concentration (here defined as 281 µmol mol 1 ). These simulations show that the photosynthetic rate in Figure 1. Mean global CO 2 concentration (top panel) and global temperature anomaly (bottom panel). The insert in the top panel gives annual rates of increase over recent years. The CO 2 data have been redrawn from IPCC (1996) and updated with data from Keeling and Whorf available from the Web: loa-co2/maunaloa.co2. Temperature data are from Jones (1994) and updated with more recent data from the Web: ornl.gov/ftp/trends/temp/jonescru/global.dat. C 3 plants, especially at higher temperatures, is not saturated with CO 2, 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 CO 2 concentrations projected for the end of the 21st century, the photosynthetic rate is still not saturated with CO 2 and the rate of photosynthesis will continue to increase with further increases in CO 2 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 CO 2 saturation at those temperatures (Kimball 1983, Figure 2. Response of C 3 photosynthesis to increasing CO 2 concentration. The response up to 1997 is shown in (a), based on the observed CO 2 concentrations shown in Figure 1. The response up to the year 2100 is shown in (b), based on predicted increases in CO 2 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 CO 2 concentration without additional feedback effects or interaction with water use. TREE PHYSIOLOGY VOLUME 20, 2000

3 EFFECTS OF CLIMATE CHANGE ON FOREST GROWTH AND COMPOSITION 311 Rawson 1992). There are fewer reports with C 4 plants, but the available evidence suggests only minor responses to CO 2 concentration (e.g., Pearcy et al. 1982, Morison and Gifford 1983, Drake 1992, Polley et al. 1992). The strong enhancement of C 3 photosynthesis is mainly a result of the competitive interaction between CO 2 and oxygen at the active site of Rubisco. Rubisco reacts either with CO 2,in which case CO 2 is productively fixed, or with oxygen, with CO 2 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 CO 2 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 CO 2 at higher temperatures, so that relative responses to increasing CO 2 concentration are more pronounced with increasing temperature (e.g., Kirschbaum and Farquhar 1984). Many plants exposed to elevated CO 2 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 CO 2 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. 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 C 4 plant native to hot Californian deserts, whereas A. sabulosa isac 4 plant native to cooler habitats. Although C 4 plants are more typically found in warmer and drier habitats than C 3 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 CO 2 concentration, those in panel (d) at elevated CO 2. Original data from Björkman et al. (1975, 1978). 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4 312 KIRSCHBAUM (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 CO 2 concentration in the C 3 plant, N. oleander. At higher CO 2 concentration, much higher photosynthetic rates were possible (as in Figure 2). Additionally, the response curve to temperature changed, with optimum temperature increasing with increasing CO 2 concentration (Kirschbaum and Farquhar 1984, McMurtrie et al. 1992). In C 3 species at low CO 2 concentration, photosynthesis is limited by Rubisco activity, which shows little response to temperature because effects on maximum capacity and the Michaelis-Menten constant for CO 2 largely cancel each other out (Kirschbaum and Farquhar 1984). At high CO 2 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 CO 2 concentration (see below). Temperature and CO 2 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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5 EFFECTS OF CLIMATE CHANGE ON FOREST GROWTH AND COMPOSITION 313 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 CO 2 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 CO 2 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 CO 2 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). 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 CO 2 concentration. For instance, plant tissue grown in high CO 2 concentrations usually has a lower nitrogen concentration than tissue grown at low CO 2 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 CO 2 concentration or an indirect response to lowered tissue nitrogen concentration. Gifford (1995) studied the response of respiration to changes in temperature and CO 2 concentration, and expressed his findings as the ratio of respiration rate to photosynthetic rate over 24 h. Because there was no consistent effect of CO 2 concentration on the ratio, Gifford (1995) concluded that, for assessing the impacts of changing CO 2 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 TREE PHYSIOLOGY ON-LINE at

6 314 KIRSCHBAUM 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) = exp[ T / (T )] 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 CO 2 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, r c, 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 at5ºcto 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 CO 2 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 CO 2 concentration (Woodward 1987a). Morison (1985) compiled a range of observations from the literature, and showed that stomatal conductance for C 3 and C 4 species was reduced by about 40% when CO 2 concentration was doubled. Several observations of tree species (Eamus and TREE PHYSIOLOGY VOLUME 20, 2000

7 EFFECTS OF CLIMATE CHANGE ON FOREST GROWTH AND COMPOSITION 315 Jarvis 1989) suggest, however, that stomatal adjustment did not occur or was minimal with increasing CO 2, especially in conifers (e.g., Marshall and Monserud 1996, Pataki et al. 1998). Marshall and Monserud (1996) studied trends in δ 13 C observed in growth rings of three conifer species over this century, and concluded that the difference between ambient and intercellular CO 2 concentration (c a c i ) had remained constant, whereas the ratio of c i /c a has changed. This implies either that there were no changes in assimilation rate and stomatal conductance despite the increasing atmospheric CO 2 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 ºCincrease 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 CO 2 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 CO 2 concentration will lead to smaller increases, or a reduction, in transpiration. Similarly, species in which stomata are more sensitive to CO 2 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 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% ( o C) 1, calculated as P = 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). TREE PHYSIOLOGY ON-LINE at

8 316 KIRSCHBAUM crease more than precipitation with global warming, or that the difference will only be slight (Figures 8 and 9). Integrating responses to temperature, CO 2, 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 CO 2 from the atmosphere, but in the diffusive uptake of CO 2, 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 CO 2 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 CO 2 concentration, which affects the rate of photosynthesis (Figure 2). With increasing temperature, more water is lost per unit carbon gained, and with increasing CO 2 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, CO 2 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 CO 2 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 CO 2 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). These two processes restrict the possible positive response of plant productivity to increasing CO 2 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 CO 2 concentration or increasing temperature by 2 C are shown in Figure 12. These con- 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). 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( T)]. The relative decomposition rate, D, was calculated as: D = exp[5.19 (T 25)/(T )]. Parameters were adjusted so that relationships were normalized to 1 at 25 ºC. TREE PHYSIOLOGY VOLUME 20, 2000

9 EFFECTS OF CLIMATE CHANGE ON FOREST GROWTH AND COMPOSITION 317 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 CO 2 concentration or temperature. In response to doubling CO 2 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 CO 2 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 CO 2 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 CO 2 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 CO 2 concentration or increasing ambient temperature by 2 o C 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). 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 CO 2 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 CO 2 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 CO 2 concentration. In response to doubled CO 2 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 CO 2 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 CO 2 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 CO 2 conditions. In wet years, when water availability was not limiting growth, the response to CO 2 was more modest because only the direct photosynthetic response to CO 2 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 CO 2 concentration and temperature were both increased, growth responses were similar to the sum of the responses to temperature and CO 2 concentration individually (Figure 13). Combined responses were dominated by the response to increasing CO 2 concentration, with peak responses being similar to responses to CO 2 concentration alone, but in years when responses to CO 2 concentration were only weak, additional TREE PHYSIOLOGY ON-LINE at

10 318 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 CO 2 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 CO 2 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 CO 2 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 CO 2 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