The summarised information presented in the previous paragraphs assumes that the predicted changes are occurring in isolation. However, the situation is far more complex as the various changes associated with climate change will act together to influence stomatal uptake. Some examples are provided to illustrate the complexity of the interactions.
Whilst a rise in CO2 levels would be expected to reduce stomatal opening and thus reduce uptake, the reduced gs will increase leaf temperature due to a reduction in leaf evapotranspiration, which adds to an enhanced effect of temperature on gs. In free-air concentration enrichment (FACE4) systems, rises in canopy temperatures between 0.6 and 1.1 °C have been reported at elevated CO2 concentrations and such increases should be added to those predicted for global warming (Kimball et al. 2002). The resultant increase in leaf temperature would either increase or decrease conductance depending on whether the optimum temperature for gs has been reached. Potentially, the effects of elevated CO2 and temperature on the gs of leaves could cancel out each other.
In general, decreases in gs with elevated CO2 are exacerbated by drought stress which also tends to close stomata (Kang et al. 2002). Partial closure of stomata results in increased WUE, indicating that plants may be able to withstand more moderate water stress. However, improved WUE detected at the leaf level may not cause the expected reduction in whole plant water consumption as whole canopies may still consume equal amounts or even more water due to an elevated CO2-induced increase in total leaf area and leaf temperature (Riedo et al. 1999; Hui et al. 2001; Kimball et al. 2002). Elevated CO2 tends to increase soil moisture by reducing plant water uptake (Owensby et al. 1999; Kimball et al. 2002), which could potentially result in a lower reduction in both gs and uptake of O3. In general, elevated CO2 will reduce the leaf uptake of O3, but the impact of CO2 enrichment on O3 uptake at
4 FACE = a circular or octagonal system of pipes that release treatment gas, or air enriched with the treatment gas, just above the crop canopy.
the canopy level will also be affected by elevated CO2-induced changes in leaf area index and soil moisture.
Interactions between O3 stress and WUE are important due to the co-occurrence of high O3 levels, combined with reduced soil moisture during warm weather. Reduced leaf WUE in response to O3 was found in wheat (Saurer et al. 1991) and soybean (Vozzo et al. 1995). This effect may be linked to direct negative effects of O3 on stomatal functioning (Leipner et al. 2001; McAinsh et al. 2002) or the stronger sensitivity of photosynthetic CO2 fixation relative to the gs of water vapour (Saurer et al. 1991). But because of a concurrent reduction in crop biomass, O3 is not likely to be having an effect on total crop water consumption.
The complexity of the interactions between the factors involved in climate change is well illustrated by consideration of the impacts of global warming on the canopy uptake of O3. When considered as a single factor, increased temperature is likely to increase stomatal uptake of O3, provided the optimum for gs has not been reached (Fig. 10.3). However, the response to warming will also be affected by the following indirect effects:
• Providing the precursors are present, an increase in warming would increase the rate of tropospheric O3 formation with a consequent increase in O3 concentration surrounding the leaves and available for stomatal uptake;
• Warming will result in a increase in VPD and decrease in SWP (soils will dry out faster due to enhanced soil evaporation and enhanced canopy evapotranspiration), which will generally result in a decrease in the stomatal flux of O3 into leaves due to a reduction in gs (Emberson et al. 2000). Semi-arid regions are likely to be most sensitive to warming as the potential evapotranspiration increases by about 2-3% for each 1°C rise in temperature (Fuhrer and Booker 2003);
• Warming will enhance plant development, which will reduce the stomatal flux of O3 into leaves at a later stage of development (Emberson et al. 2000).
Thus, the overall impact of warming on the canopy flux of O3 is difficult to predict and will depend on the severity and timing (e.g. summer or winter) of warming, future changes in SWP and the phenological stage of the vegetation, as well as any changes in seasonal pattern in the occurrence of peak episodes of O3. In a first simple modelling approach for winter wheat, Harmens et al. (2007) showed that in a future climate (including increases in background O3 concentration, temperature and CO2, changes in VPD and precipitation), the exceedance of the flux-based critical level of O3 might be reduced over Europe. In contrast, under the same scenario, the exceedance of the concentration-based critical level would increase. Izrael (2002), on the other hand, predicts that the projected warming accompanied by a 30% increase in tropospheric O3 and 20% decline in humidity would decrease the grain and fodder productions by 26 and 9%, respectively in North Asia.
10.8 Detoxification of Ozone in Plants in a Changing Climate
Of all factors involved in global climate change, the influence of elevated CO2 on O3 sensitivity has been the subject of the majority of experimental studies involving O3 impacts on plants. In contrast with the general reduction of uptake of O3 by plants due to a reduction in gs at elevated compared to ambient CO2, impacts of CO2-enrichment on the antioxidant status of leaves are not consistent. In barley, primary leaves developed early senescence at elevated compared to ambient CO2, which was associated with a decline in antioxidant capacity, resulting in oxidative stress in this otherwise O3-insensitive species (Robinson and Sicher 2004). These results suggest that protection of aging leaves from O3 damage might be reduced at elevated CO2. In a FACE experiment with deciduous trees, it was found that although elevated CO2 decreased gs, the relative decrease in dry matter production and photosynthesis caused by elevated O3 was the same at ambient and elevated CO2, suggesting that elevated CO2 grown tissue was metabolically less tolerant of O3 (Karnosky et al. 2005). A study on wheat has also suggested that CO2 enrichment will render plants more susceptible to O3 at the cellular level (Barnes et al. 1995). In contrast, Rao et al. (1995) indicated that elevated CO2 might protect wheat leaves against O3-induced oxidative stress by prolonged enhancement of the antioxidant status, whereas McKee et al. (1997b) concluded that stomatal exclusion rather than the antioxidant status plays a major role in the protective effect of elevated CO2 against O3 damage in wheat. Recent results showed that leaf antioxidant enzyme activity (e.g. superoxide dismutase) was involved in conferring CO2-induced tolerance to O3 stress in soybean (Lee 2000). Both high light and elevated carbohydrate levels favoured the maintenance of high total ascorbic acid in leaves, which often correlates with O3 tolerance. For the same crops, Booker and Fiscus (2005) found that equivalent O3 fluxes, that suppressed net photosynthesis, growth and yield at ambient concentrations of CO2, were generally much less detrimental to plants treated concurrently with elevated CO2.
In summary, a general ameliorating effect of CO2-enrichment on O3-induced oxidative stress via changes in the antioxidant status of leaves has not been proven as experimental data are inconclusive. Predictions cannot yet be made for impacts of small increases in temperature on the antioxidant status of leaves, since temperature effects have mainly been reported in relation to chilling or heat stress rather than the effects of a few degrees rise in temperature.
10.9 Impact of Elevated O3 and CO2 on Visible Injury, Crop Yield and Quality
Since both O3 and CO2 have strong effects on photosynthesis and crop production, knowledge of crop responses to a combination of elevated 'greenhouse' concentrations of both gases is one of the most important issues in view of future climate changes. While elevated CO2 generally has a growth stimulating effect due to an increase in photosynthesis, O3 tends to have the opposite effect. Moreover, both components can directly affect biochemical and physiological processes, such as plant senescence, that might influence plant response to other biotic or abiotic stresses (Barnes and Davison 1988).
To date, studies that have examined the interactive effects of CO2 and O3 have shown a variety of plant responses (Polle and Pell 1999; Olszyk et al. 2000). The nature of the interaction may be influenced by the characteristics of the O3 exposure pattern (timing in relation to phenological development, chronic or acute exposure), plant species, water availability, and other climatic parameters, but it will also depend upon the kind of effect that is considered i.e. total biomass or economic yield, photosynthesis, visible injury etc. In general, elevated CO2 reduces O3-induced leaf damage and yield losses, primarily through O3 exclusion via a reduction in gs, but also to a certain extent due to an increased detoxification capacity.
In a number of crop species, O3 injury to leaves was reduced substantially by elevated CO2, e.g. tobacco (Heck and Dunning 1967), spring wheat (Mortensen 1990; McKee et al. 1995; Rao et al. 1995; Fangmeier et al. 1996; Mulholland et al. 1997; Cardoso-Vilhena et al. 1998), radish (Barnes and Pfirrmann 1992), barley (Fangmeier et al. 1996), snap bean (Cardoso-Vilhena et al. 1998) and potato (De Tem-merman et al. 2002). For wheat, CO2 exposure influenced the severity of visible leaf damage and protected against O3 induced premature senescence during early vegetative growth (Mulholland et al. 1997). However, elevated CO2 had only a limited protective effect (reduced foliar injury) for a sensitive clone of white clover (Heagle et al. 1993) and had no effect on O3 injury to leaves of Phaseolus vulgaris (Heck and Dunning 1967). Exposure of C3 and C4 grass species to O3 increased leaf dark respiration and decreased photosynthesis (Volin et al. 1998), which was not the case in an elevated CO2 environment. As repair processes on the cellular level depend primarily on the dark respiration, the cost of repair is lower in the elevated CO2 environment. The length of the dark period is also very important for the plant to recover from the O3 exposure during the day. As De Temmerman et al. (2002) pointed out, crops, such as potato, show visible symptoms at much lower O3 concentrations during the long days in summer, when the dark period becomes too short for repair.
The relative yield stimulation by elevated CO2 tends to be larger in an atmosphere with elevated levels of O3, or vice versa, in a CO2-enriched atmosphere, negative effects of O3 are less than at ambient CO2. In determinate crops, such as cereals, grain yield not only depends on photosynthesis, but also on the length of the active phase of leaf photosynthesis and the sink capacity of the grains. In wheat, elevated CO2 fully protects against the detrimental effects of O3 on biomass, but not yield (McKee et al. 1997a). Similar results have been reported with soybean (Fiscus et al. 1997), cotton (Heagle 1989) and tomato (Reinert et al. 1997). On the other hand, Pleijel et al. (2000) found that the grain yield in wheat was negatively affected by O3 at ambient CO2 but unaffected by O3 at elevated CO2. Responses of wheat to elevated O3 and CO2 appear to be cultivar-dependant, as some cultivars do not respond significantly to elevated O3 levels and for those cultivars, no significant interactions between O3 and CO2 were observed (Bender et al. 1999). Although elevated CO2 did not prevent O3 induced yield losses in potato, the yield increases in response to CO2 fertilisation far exceeded O3-induced losses (Craigon et al. 2002). In potato, significant interactions between O3 and CO2 were observed regarding the glucose and reducing sugar content in tubers (Vorne et al. 2002). Despite the beneficial impact of CO2 enrichment on growth and yield of C3 cereal crops, declines in flour quality due to reduced N content are likely in a CO2-enriched world (Fangmeier et al. 1999), thereby counteracting the positive effect of O3 on flour quality (Vandermeiren et al. 1992; Pleijel et al. 1999).
It has been indicated that the maximum benefits for wheat production in response to CO2 enrichment will not be accomplished under concomitant increases in tropo-spheric O3 concentration (Rudorff et al. 1996). This implies that predictive models based simply on the impacts of elevated CO2 will result in an overestimation of the likely effects of atmospheric change on plant productivity (Barnes and Wellburn 1998). Importantly, Long et al. (2005) pointed out that chamber studies, which have been the main mechanistic basis for crop yield models, overestimate the yield gain by elevated CO2 compared to what was observed under fully open-air conditions in the field, as provided by FACE systems. Based on chamber experiments, average yield stimulation for C3 crops with a doubling of CO2 has been estimated at 30%, whilst estimates based on results from field-scale experiments under more realistic conditions (including varying water availability) were lower. According to a review by Kimball et al. (2002) on responses of agricultural crops in FACE systems, elevated CO2 stimulates biomass in C3 grasses by an average of 12%, grain yield in wheat and rice (Oryza sativa L.) by 10-15%, and tuber yield in potato by 28%. Yield stimulation in C4 crops is much lower. Some environmental differences between chamber and open air micro-climate also have an influence on the plant interaction with O3 uptake and detoxification (Morgan et al. 2003). Morgan et al. (2006) observed in an open-air study that the effects of season-long elevation of O3 induced substantially greater grain losses in soybean compared to chamber experiments. If this is representative of other major crops and growing areas, then yield losses due to rising O3 will even outweigh any gains due to rising CO2 (Long et al. 2005).
While leaf-level responses to elevated CO2 and O3 are well documented, a few studies have addressed canopy level responses to increases in these pollutants. In SoyFACE, the results show a decrease in evapotranspiration of soybean for all three treatments (+CO2, +O3, +CO2 and O3), with the largest decrease observed for growth in elevated O3 (Bernacchi et al. 2006). When integrated over the season, plants grown in elevated CO2 and O3 used 10 and 18% less water, respectively.
While the directional response of soybean exposed to increases in CO2 and in O3 were similar, the mechanisms for these responses differ. Growth in elevated O3 resulted in a decrease in leaf area compared with the control. It is likely that the O3-induced damage to the plant canopy, responsible for the lower biomass and leaf area, is responsible for the lower evapotranspiration in soybean. On the other hand, soybean grown in elevated CO2 demonstrated higher leaf area while showing a reduction in evapotranspiration suggesting that a decrease in gs was sufficient to more than offset the increase in leaf area (Bernacchi et al. 2007). These results imply that future atmospheric change may influence soybean response to drought conditions and may have feedback effects on atmospheric moisture, potentially altering regional precipitation patterns.
10.10 Impacts of Increased Ground-Level Ozone on Weeds, Pests and Diseases
The occurrence of plant pests (weeds, insects or microbial pathogens) is an important constraint with global average yield losses estimated at about 40% (Oerke et al. 1994), and production costs significantly dependent on the extent of measures necessary for plant protection. Consequently, changes in the occurrence of pests due to increased O3 and its interaction with other climatic changes are of economical importance. Because insect and plant species show individual responses to climate change, it is expected that climate change will affect the temporal and spatial association between species interacting at different trophic levels (Harrington et al. 1999). Changes in foliar chemistry and surface characteristics by O3 may have an effect on the incidence of viral and fungal diseases and the impacts of insect pests, although not much experimental information is available on this subject in relation to crops because these are mostly grown under conditions which prevent the occurrence of pests and diseases.
Virtually nothing is known about effects of elevated O3 on crop-weed interactions (Fuhrer and Booker 2003), but O3 may potentially affect the ability of weeds and crops to compete for common resources. In the case of aggressive weed species of tropical or subtropical origin, future climatic conditions may lead to their expansion into temperate regions. The generalized prediction that in a CO2-rich world, major crops will compete more successfully with the worst agricultural weeds, which are mostly C4 species (Dukes and Mooney 1999), may not be accurate due to regional differences. For instance, in US, 9 out of 15 worst weeds in the most important crops are C3, and a substantial fraction of crops are C4 (Bunce and Ziska 2000). The interactions between weeds and crops or grassland species in relation to climate change are complex and further experiments with different crop-weed systems under a range of atmospheric and edaphic conditions, are needed for accurate predictions.
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