Implications of climate change for the stomatal flux of ozone: A case study for winter wheat

Environmental Pollution 146 (2007) 763e770 www.elsevier.com/locate/envpol

Implications of climate change for the stomatal flux of ozone: A case study for winter wheat Harry Harmens*, Gina Mills, Lisa D. Emberson, Mike R. Ashmore Centre for Ecology and Hydrology, Orton Building, Deiniol Road, Bangor, Gwynedd LL57 2UP, UK Received 15 December 2005; received in revised form 19 May 2006; accepted 23 May 2006

In a future climate the stomatal flux of ozone is likely to be reduced across Europe despite increasing tropospheric background ozone concentrations. Abstract Climate change factors such as elevated CO2 concentrations, warming and changes in precipitation affect the stomatal flux of ozone (O3) into leaves directly or indirectly by altering the stomatal conductance, atmospheric O3 concentrations, frequency and extent of pollution episodes and length of the growing season. Results of a case study for winter wheat indicate that in a future climate the exceedance of the flux-based critical level of O3 might be reduced across Europe, even when taking into account an increase in tropospheric background O3 concentration. In contrast, the exceedance of the concentration-based critical level of O3 will increase with the projected increase in tropospheric background O3 concentration. The influence of climate change should be considered when predicting the future effects of O3 on vegetation. There is a clear need for multi-factorial, open-air experiments to provide more realistic information for O3 flux-effect modelling in a future climate. Ó 2006 Elsevier Ltd. All rights reserved. Keywords: Ozone; Climate change; Stomatal ozone flux; AOT40; Winter wheat

1. Introduction Current levels of tropospheric ozone (O3) have been shown to cause damage to crops, trees and (semi-)natural vegetation (e.g. Bussotti et al., 2003; Harmens et al., 2004; Karlsson et al., 2003). Effects-based research has resulted in the establishment of critical levels of O3 for vegetation. Historically, these critical levels were based on the concentration of O3 in the atmosphere, but it has long been recognized that plant responses to O3 are more closely related to the absorbed O3 dose, or the instantaneous flux of O3 through the stomates (e.g. Fuhrer et al., 1992). Recently, stomatal flux-based critical levels of O3 were defined for selected crop species and provisionally for trees (LRTAP Convention, 2004). Stomatal flux-based critical levels of O3 take into account the varying influences of temperature, water

* Corresponding author. E-mail address: [email protected] (H. Harmens). 0269-7491/$ - see front matter Ó 2006 Elsevier Ltd. All rights reserved. doi:10.1016/j.envpol.2006.05.018

vapour pressure deficit (VPD), light, soil water potential (SWP), atmospheric O3 concentration and plant development (phenology) on O3 uptake. As such, they lend themselves to understanding impacts under climate change conditions since factors such as elevated CO2, temperature and changes in precipitation affect the flux of O3 into leaves. Climate change can have a direct impact on stomatal conductance ( gs) via for example elevated CO2 concentrations or indirect effects on gs via changes in climate, for example altered atmospheric and soil water deficits and temperature affecting plant physiology and phenology. In contrast to the concentration-based approach, the principles of the flux-based approach allow climate change factors to be incorporated into assessments of critical levels, although it is important to understand that such factors may not only act as ‘‘dose modifiers’’, but may also influence the detoxification capacity of the plant (e.g. Rao et al., 1995; Robinson and Sicher, 2004; Wustman et al., 2001), among other factors. Emissions scenarios applied by the Intergovernmental Panel on Climate Change project globally that by the end of

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the 21st century the mean tropospheric background O3 concentration will change by between 12% and þ62%, the mean temperature will increase between 1.4 and 5.8  C, the CO2 concentration will increase to 540e970 ppm, precipitation patterns across the globe will alter and the frequency of extreme events will increase (IPCC, 2001). Vingarzan (2004), using different IPCC scenarios, predicted global mean background tropospheric O3 concentrations ranging from about 40 to 80 ppb. The high spatial and temporal variability in O3 concentrations mean that it is difficult to identify with great confidence any long-term trends and make projections for future tropospheric O3 concentrations. There is evidence that in Europe the mean ground-level O3 concentrations are increasing and the peak concentrations are declining (Coyle et al., 2003; Simmonds et al., 2004; Vingarzan, 2004). In the future, peak concentrations of O3 will probably be reduced further with the implementation of the Gothenburg Protocol (Working Group on Effects, 2004), but this should be considered in the context of an increasing global background concentration. The overall impact of climate change on the canopy O3 flux is difficult to predict and will depend on for example geographical distribution of vegetation, severity and timing of warming, and its impacts on SWP and plant phenology (including growth period, canopy development, leaf area index). Plant species often have an optimum temperature range for gs (LRTAP Convention, 2004) and might acclimate to warming within this range depending on local environmental conditions. However, Bunce (2000) observed an exponential increase in gs with temperature over a large temperature range in eight cool and warm climate herbaceous species. Warming may encourage earlier and enhanced plant development, resulting in a forward shift of the period within the year when plants are absorbing O3. This may lead to a change in the stomatal O3 flux if peak O3 concentrations, currently associated with mid-summer, coincide with a later developmental stage of the plants. Little empirical data is available on the interactive impacts of O3 and warming on vegetation, in particular at the field scale. Many studies have shown that atmospheric CO2-enrichment reduces gs (Curtis and Wang, 1998; Drake et al., 1997; Morgan et al., 2003). Although it has been suggested that acclimation of gs to long-term exposure to elevated CO2 might occur, this is not substantiated by conclusive evidence and might not happen at all (Jarvis et al., 1999; Medlyn et al., 2001). Therefore, when plants were exposed to O3 in the presence of elevated CO2, the uptake of O3 was often reduced (Fiscus et al., 1997; Kollist et al., 2000; McKee et al., 1997). Effects of changes in precipitation patterns are likely to be mediated through (a) effects of VPD on gs, with increasing VPD causing a decrease in flux and (b) changes in SWP, with decreasing SWP resulting in decreased stomatal flux (LRTAP Convention, 2004). In this paper, we report on the impacts of climate change on stomatal O3 flux, describing the results of a flux-modelling case study for winter wheat, applying future climate scenarios. In the case study, we also compare the outcome of the fluxbased risk assessment with a concentration-based risk

assessment. The choice of wheat is driven by the fact that the stomatal O3 flux model for wheat that is employed in this study has been developed and parameterized using a large number of datasets from a number of different countries representing different climatic conditions and a range of different wheat cultivars (LRTAP Convention, 2004). Evaluations of the model indicate a good capability to predict stomatal O3 fluxes; for example, the model was able to account for 76% of the variation in gs observations made at a commercially grown wheat field in Italy (Tuovinen et al., 2004). This is one of the first studies to predict and compare the effects of climate change on the stomatal O3 flux at different locations in Europe, incorporating diverse climatic conditions in a standardized manner. 2. Materials and methods A modelling case study was conducted for winter wheat (Triticum aestivum). Annual hourly O3 concentrations at a height of 50 m and canopy height (i.e. 1 m) and meteorological data near the canopy surface were provided by EMEP/MSC-West (Co-operative programme for monitoring and evaluation of the long-range transmissions of air pollutants in Europe/Meteorological Synthesizing CentredWest) for the year 1997 for five selected EMEP grid squares (Table 1). EMEP grid squares located in each climate region (as defined in the Mapping Manual (LRTAP Convention, 2004)) were selected for use in this modelling case study. The Mapping Manual stomatal flux model, based on the stomatal component of the DO3SE model (Deposition of Ozone and Stomatal Exchange; Emberson et al., 2001; Simpson et al., 2003; Tuovinen et al., 2004), was applied to calculate the accumulated stomatal flux of O3 above a threshold of 6 nmol m2 projected leaf area (PLA) s1(AFst6), the flux threshold for the critical level for wheat (Pleijel et al., submitted for publication). The core of the leaf O3 flux model is the stomatal conductance ( gsto) multiplicative algorithm described in eq. (1):       gsto ¼ gmax  min fphen ; fO3  flight  max fmin ; ftemp  fVPD  fSWP

ð1Þ

where gsto is the actual stomatal conductance (mmol O3 m2 projected leaf area (PLA) s1), gmax is the species-specific maximum stomatal conductance (mmol O3 m2 PLA s1) and fmin is the minimum daytime gsto under field conditions. The parameters fphen, fO3, flight, ftemp, fVPD and fSWP are all expressed in relative terms (i.e. they take values between 0 and 1) as a proportion of gmax. These parameters allow for the modifying influence of phenology (phen) and O3, and four environmental variables (light (irradiance), temperature, atmospheric vapour pressure deficit (VPD) and soil water potential (SWP)) on stomatal conductance to be estimated (LRTAP Convention, 2004). For wheat, this multiplicative gsto model has been formulated and parameterized based on an extensive dataset comprising both primary and secondary data. These data incorporate information for more than 15 cultivars and 10 countries across Europe. Further details of the wheat model formulation and parameterization are given in LRTAP Convention (2004) and Pleijel et al. (submitted for publication). The model incorporates an O3 function ( fO3) which is designed to account for the premature senescence induced by O3.

Table 1 Grid references of sites in five EMEP grid squares representing the five climate zones in Europe Climate zone

Country

Latitude

Longitude

Northern Europe (NE) Atlantic Central Europe (ACE) Continental Central Europe (CCE) Eastern Mediterranean (EM) Western Mediterranean (WM)

Sweden UK

57 540 N 55 190 N

12 240 E 3 120 W

Germany

52 480 N

10 450 E

Slovenia Spain

46 70 N 40 260 N

15 60 E 3 420 W

H. Harmens et al. / Environmental Pollution 146 (2007) 763e770 A simple ‘‘water budget’’ modelling approach was employed to estimate soil moisture deficit (SMD). This method uses the multiplicative model’s estimation of canopy gsto (scaled up from leaf level gsto according to leaf area index and leaf population fractions as described in Tuovinen et al., 2004) in conjunction with the atmospheric VPD to estimate the actual canopy transpiration, where VPD provides the driving force for water moving through the soil-plant-atmosphere continuum. As such, the modelling of the accumulation of SMD, the resulting SWP and influence on gsto (determined according to the wheat fSWP relationship, soil type and rooting depth) were modelled in an internally consistent manner. For the runs presented here we assumed a medium texture soil type (consistent with the soil textures commonly found under agricultural land) and a constant rooting depth of 1 m. Leaf stomatal O3 flux (Fst) was estimated according to eq. (2), which accounts for deposition to the cuticle through the incorporation of the leaf surface resistance (rc) term: Fst ¼ cðz1 Þ  gsto 

rc rb þ rc

ð2Þ

where c(z1) is the O3 concentration (in nmol m3) at the top of the canopy (at height z1 in m), gsto is the stomatal conductance (in m s1) converted assuming normal temperature and air pressure using a factor of 41,000 according to Jones (1992); rb is the quasi-laminar resistance (estimated according to McNaughton and van der Hurk, 1995); rc is the leaf surface resistance and is assumed constant at 2500 m s1 (to be consistent with the DO3SE model). The accumulated flux above an O3 stomatal flux threshold of Y nmol m2 s1 (AFstY) is calculated as described in eq. (3), with the accumulation taking place over a defined period of time: AFst Y ¼

n X ½Fsti  Y for Fsti  Ynmol m2 PLA s1

ð3Þ

i¼1

where Fsti is the hourly O3 flux in nmol m2 PLA s1, and n is the number of hours within the accumulation period. The accumulation period is positioned around the mid-anthesis growth stage (defined as growth stage 65 according to Zadoks et al., 1974) since this is the period when wheat is most sensitive to O3 (Soja et al., 2000; Younglove et al., 1994). Mid-anthesis was estimated using a temperature sum value of 1075  C days calculated from plant emergence (defined as the first date after 1 January when the temperature exceeds 0  C, or 1 January if the temperature exceeds 0  C on that date). The stomatal DO3SE model was run with both current (1997) and climate change input O3 and meteorological data. For the climate change model runs, the current year (1997) input data were modified as described in Table 2, both with (CC þ O3) and without (CC) an increase in the O3 concentration, to understand the effects on stomatal O3 flux attributable to climate separate from changes in O3 concentration. The applied climate scenario reflects mean global changes as predicted for the end of the 21st century (IPCC, 2001). The impact of elevated CO2 on stomatal conductance was incorporated in the DO3SE model by multiplying gmax with a factor 0.65, based on the measured reduction of gmax in a Free Air Carbon dioxide Enrichment (FACE) study with spring wheat (Garcia et al., 1998), where CO2 concentrations were raised to 550 ppm. This reduction in gmax is in agreement with reported reductions in stomatal conductance between 20% and 40% by a doubling of recent atmospheric CO2 concentrations to ca. 700 ppm (Jarvis et al., 1999). For precipitation no changes or small increases (10%) in the hourly amount, depending on climate zone, were included (cf. Table 2), with no changes in the frequency. Modification to the VPD was achieved assuming a constant absolute humidity and a 3  C rise in temperature. Since the uncertainty in estimating a change in VPD is high and some model predictions suggest water vapour concentrations will increase (Stevenson et al., 2006), two model runs were performed: (i) without modifying VPD and (ii) with modification of VPD (indicated by (VPD)). It would be possible to apply more specific and localized scenarios of climate change in these simulations, but because the uncertainty in regional predictions is so great, we chose to compare the effect of the same changes at different locations in Europe. In addition to predicted changes in AFst6, the accumulated O3 concentration above a threshold of 40 ppb during daylight hours (AOT40) was estimated using the climate specific accumulation windows, which were not altered for climate change conditions, given in the Mapping Manual (LRTAP Convention,

765

Table 2 Modifications to current day (1997) meteorological and O3 concentration input data for climate change conditions Parameter

Climate change (CC)

Climate change þ O3 increase (CC þ O3)

O3 concentration (ppb)

No change in O3 concentration

Temperature (  C) CO2 effect on gs

þ3  C gmax * 0.65 (Garcia et al., 1998) If P > 0, increase P by 10% in northern and central Europe Assume absolute humidity remains constant, calculate VPD according to increase in temperature by 3  C

Increase O3 concentration by 5 ppb in all hours of the day þ 3 C gmax * 0.65 (Garcia et al., 1998) If P > 0, increase P by 10% in northern and central Europe Assume absolute humidity remains constant, calculate VPD according to increase in temperature by 3  C

Precipitation (P) (mm)a

VPD (kPa)

a Only hourly P events are altered, i.e. the magnitude and not the frequency of P events is increased.

2004). The future AOT40 at canopy height was estimated from canopy height O3 concentrations. These were derived from the 50 m height O3 concentration data either by (i) simply adding 5 ppb to the EMEP O3 concentration output at canopy height or (ii) adding 5 ppb to the 50 m height O3 concentration and then estimating the canopy O3 concentrations using the neutral stability method described in the Mapping Manual (LRTAP Convention, 2004). This method estimates the O3 concentration gradient (between the 50 m reference height and the top of the canopy) as a function of wind speed, meteorology, canopy roughness and total O3 flux (i.e. it incorporates only mechanical (not thermal) atmospheric turbulence). The dependence of this method on meteorology allowed ‘‘climate change’’ canopy gs values to be incorporated into the assessment of the O3 concentration profile and hence investigation of the effect climate change may have on AOT40 via changes in O3 deposition to vegetated surfaces.

3. Results When we describe the results below for the five climate zones in Europe, one should bear in mind that the model runs were performed for one selected EMEP grid square within each climate zone (see Table 1). Application of the climate change scenarios (‘‘CC’’) resulted in a decrease of the AFst6 for winter wheat (even with an increase in tropospheric background O3 concentration; ‘‘CC þ O3’’) for most of Europe, but not for Continental Central Europe (Fig. 1). The model predicts that an increase in VPD results in a significant decrease in the AFst6 for winter wheat. This is due to the direct limiting influence on gs (Table 3), but also related to the influence VPD has on determining SMD. SMD is the key driver limiting flux under the current and ‘‘CC þ O3(VPD)’’ model runs in Northern Europe (NE) and Western Mediterranean (WM; Fig. 2). The high SMD in NE is a result of the high VPDs (higher in comparison to other parts of Europe due to the later growing season, even with the 3  C increase in temperature; see Fig. 3) causing rapid water movement from the soil to the atmosphere through the plant, and this is not negated by the 10% increase in the amount of precipitation.

H. Harmens et al. / Environmental Pollution 146 (2007) 763e770

766

Current

4 CC

3

1.0

WM

CC+O3

CCE

CC(VPD)

NE

0.8

CC+O3(VPD)

2

fSWP

AFst6 (mmol O3 m-2 PLA)

1997

0.6 0.4

1

0.2 0 NE

ACE

CCE

EM

WM

0.0 100

Climate zone

Table 3 Influence of climate change (‘‘CC þ O3(VPD)’’ scenario, see Table 2) in comparison with the current day (1997) climate on ftemp and fVPD (described as means) over the AFst6 accumulation period for winter wheat for five different climate zones in Europe (see Fig. 1 for details) Climate zone

NE ACE CCE EM WM

Current climate

Future climate ‘‘CC þ O3(VPD)’’

ftemp

fVPD

ftemp

fVPD

0.59 0.31 0.53 0.56 0.36

0.93 0.99 0.94 0.97 0.96

0.69 0.28 0.58 0.68 0.44

0.80 0.99 0.90 0.89 0.92

200

250

Day of year

Fig. 1. Modelled accumulated stomatal flux of O3 above a threshold of 6 nmol m2 PLA s1 (AFst6) for winter wheat for five different climate zones in Europe for the reference year 1997 and for future climate using the climate change scenarios described in Table 2. The dashed line indicates the flux-based critical level of O3 for wheat (AFst6 ¼ 1 mmol m2 PLA). NE, Northern Europe; ACE, Atlantic Central Europe; CCE, Continental Central Europe; EM, Eastern Mediterranean; WM, Western Mediterranean.

CC+O3(VPD) 1.0

WM CCE NE

0.8

fSWP

For WM the higher VPDs again result in higher SMD. However, Continental Central Europe has SMD limitation under current but not under future climate conditions, which is partly a result of the increase in precipitation and, perhaps more importantly, the shifting of the growth period to earlier in the year, coinciding with heavier precipitation events (data not shown). This explains why the AFst6 for winter wheat does not decrease in Continental Central Europe under the ‘‘CC’’ scenario compared to the current year (1997) AFst6. Performing the model runs with no changes in precipitation for northern and central Europe hardly affected the outcome (data not shown). In general, the limitation of stomatal conductance caused by ftemp is decreased (but increased in Atlantic Central Europe), whilst that caused by fVPD is increased (with no change in Atlantic Central Europe; Table 3) in a future climate. The use of the thermal time method to estimate both the timing of mid-anthesis and the start and end of the growing season means that with global warming the growth and accumulation period starts and ends earlier in each location (Fig. 3). In some parts of Europe (e.g. Northern Europe, Continental Central Europe and Eastern Mediterranean) this could result in a decrease in the overlap between the O3

150

0.6 0.4 0.2 0.0 100

150

200

250

Day of year Fig. 2. Impact of climate change (‘‘CC þ O3(VPD)’’ scenario, see Table 2) in comparison with the current day (1997) climate on fSWP for winter wheat for five different climate zones in Europe (see Fig. 1 for details). Data are not shown for the climate zones with an fSWP ¼ 1 throughout the year.

accumulation period and the highest O3 concentrations at canopy level, when assuming no shift in O3 peak levels within the year. In general, the total O3 deposition in a future climate is reduced due to the reduction in stomatal flux (which also translates into reduced flux of upper canopy leaves and the lower AFst6 values reported in Fig. 1), which means that less O3 is lost from the atmosphere to the vegetation. This reduction in stomatal flux and hence total deposition will result in higher atmospheric O3 concentrations, which will likely lead to higher AOT40s. Fig. 4 shows such a situation occurring in Northern Europe, Continental Central Europe and the Western Mediterranean. However, for Atlantic Central Europe and the Eastern Mediterranean, this is not the case since the earlier AOT40 accumulation periods recommended for these climate zones coincide with periods when the deposition under climate change conditions is higher than current deposition. This is because the earlier growth period of wheat under climate change (estimated using the thermal time model) occurs under conditions less limiting to gs (i.e. lower temperatures and VPDs) (see Fig. 3). Whereas the flux-based approach predicts a reduction in the absorbed O3 dose for winter wheat under climate change conditions, resulting in reduced exceedance of the flux-based critical level across Europe (Fig. 1), the

H. Harmens et al. / Environmental Pollution 146 (2007) 763e770

Northern Europe

767

Atlantic Central Europe 120

120

60

0.4

40

0.2

20

0.0 100

125

150

175

200

225

80

0.6

60

0.4

40

0.2

20

0.0

0 250

75

100

125

Day of year

150

175

200

225

Day of year

Continental Central Europe

Eastern Mediterranean 120

120

80

0.6

60

0.4

40

0.2

20

0.0 75

100

125

150

175

200

225

0 250

100

fphen flag leaf

100

0.8

Daily max O3 (ppb)

1.0

1.0

fphen flag leaf

0 250

0.8

80

0.6

60

0.4

40

0.2

20

0.0 75

Day of year

100

125

150

175

200

225

Daily max O3 (ppb)

75

0.8

Daily max O3 (ppb)

80

0.6

100

fphen flag leaf

fphen flag leaf

100 0.8

Daily max O3 (ppb)

1.0

1.0

0 250

Day of year

Western Mediterranean

fphen flag leaf

100

0.8

80

0.6

60

0.4

40

0.2

20

0.0 75

100

125

150

175

200

225

Daily max O3 (ppb)

120 1.0

0 250

Day of year Fig. 3. Shift in the O3 accumulation period for winter wheat, as indicated by fphen of the flag leaf, with a 3  C rise in temperature (grey line) in comparison with the current day (1997) accumulation period (black line) for five different climate zones in Europe. The associated daily maximum O3 concentrations at canopy level (black dots) indicate changes in overlap with the O3 accumulation period.

concentration-based approach predicts a considerable increase in concentration-based critical level exceedance under future climate conditions (Fig. 4). 4. Discussion Based on the case study for winter wheat, two contrasting conclusions would be drawn on application of a flux-based compared to a concentration-based risk assessment methodology in a changing climate. Whereas the flux-based approach predicts a reduction in the absorbed O3 dose for winter wheat under climate change conditions in most areas of Europe, resulting in reduced exceedance of the flux-based critical level, the concentration-based approach predicts a considerable increase in concentration-based critical level exceedance under future climate conditions. These trends were generally observed for all EMEP grids included in the analysis and hence the variety of climates in Europe. It should be noted, however,

that the five selected grid squares in the case study might not be representative of the broader spatial patterns across Europe. In the case of the concentration-based approach, the simple modelling conducted here suggests that such exceedance may be exacerbated in some locations due to the effect of reduced O3 deposition to vegetated surfaces. However, enhancement of leaf area index, which might occur for some species under climate change conditions (e.g. Ainsworth and Long, 2005), has not been included and this would certainly reduce the estimated decreases in deposition to the vegetated surface. In addition, reductions of surface deposition will also increase the transport distance of O3, an effect that could be simulated with a variable deposition module within the EMEP model. Although other attempts have been made to predict the effects of climate change on AOT40 (Langner et al., 2005), they do not consider stomatal O3 flux. For the default growing season for forest trees (April to September) over which the concentration-based O3 critical level exceedances should be

H. Harmens et al. / Environmental Pollution 146 (2007) 763e770

768 12 1997

AOT40 (ppm h)

10

+O3 +O3(Dep)

8 6 4 2 0 NE

ACE

CCE

EM

WM

Climate zone Fig. 4. Accumulated O3 concentration above a threshold of 40 ppb (AOT40) for winter wheat for five different climate zones (see Fig. 1 for details) in Europe for the reference year 1997 and projected for the future assuming a rise in hourly mean O3 concentration of 5 ppb and no change in O3 deposition ( þ O3) or with a change in O3 deposition ( þ O3(Dep)), estimated according to the neutral stability method in the Mapping Manual (LRTAP Convention, 2004), and using climate change bulk canopy conditions. The dashed line indicates the concentration-based critical level of O3 for agricultural crops (AOT40 ¼ 3 ppm h).

calculated (LRTAP Convention, 2004), Langner et al. (2005) predict an increase in both AOT40 and mean daily maximum O3 concentration under climate change scenarios over southern and central Europe and a decrease in northern Europe. Coyle et al. (2005) used modelled data along with current O3 measurements to simulate changes in the UK O3 climate during the next few decades. For most applied climate change scenarios they found an increase in both AOT40 and AFst6. However, they did not take into account the influence of elevated CO2 on stomatal conductance in the flux-based approach. In contrast to the concentration-based approach, the stomatal flux-based approach lends itself much better to understanding and predicting impacts of future climate on the risk of O3 damage to vegetation, as it takes into account the influences of climate change on O3 uptake by vegetation. Our simulations in the case study are based on simple assumptions about possible changes in climate and O3 exposure in Europe over coming decades, and are not intended to be predictions of the relative effects in different regions. Nevertheless, applying the model to different locations showed important differences in response that allow us to better understand the influence of key factors in modifying stomatal O3 flux in a changing climate. There are a number of additional factors that have not been included in our case study. For example, O3 exposure patterns in a changing climate might change in several ways. Firstly, tropospheric background O3 increases will not be constant over the year, as the peaks in tropospheric background occur in spring rather than mid-summer; this may offset the benefits of an earlier start to the growing season (Coyle et al., 2003). Secondly, increased surface temperatures may lead to increased biogenic VOC emissions and hence greater regional O3 production. These, and other factors, strongly suggest the need to incorporate a deposition and flux model within atmospheric chemistry/transport models, so the combined effects of climate on

O3 formation, transport, deposition and impacts can be assessed in an integrated fashion. Thirdly, the effect of a possible increase in absolute water vapour concentration due to warming (Stevenson et al., 2006) on the stomatal O3 flux was not included in this case study. It was outside the scope of this study to incorporate changes in agricultural management practices implemented in adaptation to climate change, which may influence O3 flux. For example, alterations in precipitation and soil-atmosphere water vapour fluxes may well necessitate changes in the spatial extent and frequency of applied irrigation, which has implications on the limiting effect of drought on O3 flux. Finally, our results are for one determinate crop species, and should not be taken as predictive of the response of other species. The DO3SE model does not take into account the direct effects of O3 on stomatal behaviour and any potential consequences for stomatal responses to climatic factors. In general, longer-term exposure to O3 causes stomatal responses to become sluggish (McAinsh et al., 2002), resulting in slower and less complete stomatal closure in response to for example drought, vapour pressure deficit and photosynthetic photon flux density (Paoletti, 2005; Paoletti and Grulke, 2005). An in-depth review of the mechanisms of tree stomatal responses to elevated CO2 and O3 was conducted recently by Paoletti and Grulke (2005). Currently the DO3SE model does not take into consideration O3 detoxification mechanisms because there is considerable uncertainty in quantifying the various defence mechanisms in plants (Musselman et al., 2006). Similarly, the impacts of climate change on O3 detoxification mechanisms are uncertain. For example, contrasting effects of CO2-enrichment on the antioxidant status of leaves have been reported (Gaucher et al., 2003; McKee et al., 1997; Niewiadomska et al., 1999; Rao et al., 1995; Robinson and Sicher, 2004; Wustman et al., 2001). This case study has focused on a limited range of scenarios in Europe. However, in view of the evidence of significant impacts of O3 in south and east Asia, and the likelihood that both regional O3 concentrations and global background O3 concentrations will increase in these and other regions, improved assessments of the future impacts of O3 on food production in a global context are urgently needed (Ashmore, 2005). Our results for Europe indicate the importance of ensuring that such assessments use a flux-based approach and consider the implications of climate change in these regions. So far, O3 effects studied in isolation in single species in open-top chamber studies have been used to establish dosee response or fluxeeffect relationships. However, it is becoming increasingly important when predicting future impacts of O3 to consider O3 effects within the context of global climate change under more realistic field conditions. Only in the last decade have data emerged on the impacts of climate change and/or O3 on vegetation at the field scale under more natural conditions. Although these field studies generally substantiate predictions based on chamber studies, some inconsistencies between the results of chamber and field studies have been reported. For example, the effects of elevated O3 on an O3-sensitive plant such as soybean are substantially less in

H. Harmens et al. / Environmental Pollution 146 (2007) 763e770

a field study than predicted by chamber studies (Morgan et al., 2004). Furthermore, in the field elevated CO2 appears to reduce crop gs about one and a half times more than observed in previous chamber experiments (Kimball et al., 2002), crop yields increased far less than anticipated from prior enclosure studies with elevated CO2 (Ainsworth and Long, 2005; Morgan et al., 2005) and the responses of trees to elevated CO2 might have been underestimated in chamber studies compared with field studies (Ainsworth and Long, 2005; Karnosky et al., 2003). In addition, vegetation responses to single drivers of climate change (including changes in tropospheric O3 concentrations) cannot simply be scaled up to responses to multiple drivers due to complex interactions (Fuhrer, 2003; Shaw et al., 2002). There is a clear need for a combined approach of multi-factorial field experiments, to improve flux-based model parameterization and sophistication, and flux model application within large-scale climate and photo-oxidant models to improve predictions of the impacts of climate change-mediated effects of O3 on plant communities in the long term. 5. Conclusions In contrast to the concentration-based approach, the principles of the flux-based approach allow some key climate change factors to be incorporated into assessments of O3 critical levels for vegetation. Results of a case study for winter wheat indicate that in a future climate the exceedance of the flux-based critical level of O3 might be reduced across Europe, even when taking an increase in tropospheric O3 concentration into account. In contrast, the exceedance of the concentrationbased critical level of O3 might increase due both to anthropogenically induced increases in background tropospheric O3 concentration and alterations to the O3 mass balance resulting from reduced O3 deposition rates. Climate change factors should be fully incorporated into the O3 risk assessment methodology and the influence of climate change should be considered when predicting the future effects of O3 on vegetation. Acknowledgements The financial support of the UK Department for Environment, Food and Rural Affairs (Defra contract EPG 1/3/205 and SPU24) is gratefully acknowledged. We thank David Simpson (EMEP/MSC-West) for providing the O3 and climate data for five selected EMEP grid squares. References Ainsworth, E.A., Long, S.P., 2005. What have we learned from 15 years of free-air CO2 enrichment (FACE)? A meta-analytic review of the responses of photosynthesis, canopy properties and plant production to rising CO2. New Phytologist 165, 351e372. Ashmore, M.R., 2005. Assessing the future global impacts of ozone on vegetation. Plant, Cell and Environment 28, 949e964. Bunce, J.A., 2000. Acclimation of photosynthesis to temperature in eight cool and warm climate herbaceous C3 species: Temperature dependence of

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