K. Vandermeiren, H. Harmens, G. Mills and L. De Temmerman
Ozone (O3) is a naturally occurring chemical present in both the stratosphere (the 'ozone layer', 10-40km above the earth) and in the troposphere (0-10km above the earth). While stratospheric O3 protects the Earth's surface from solar UV radiation, tropospheric O3 is the third most important greenhouse gas (after CO2 and CH4) (Denman et al. 2007; Solomon et al. 2007). It contributes to greenhouse radiative forcing, causing a change in the balance between incoming solar radiation and outgoing infrared radiation within the atmosphere that controls the Earth's surface temperature. Besides its role as a direct greenhouse gas, O3 has been identified as one of the major phytotoxic air pollutants. The adverse effects of O3 on plants were first identified in the 1950s (Hill et al. 1961), and it is now recognized as the most important rural air pollutant, affecting human health and materials, as well as vegetation (WGE 2004).
Comparisons of the mean global tropospheric O3 concentrations with those measured over a century ago indicate that current levels have increased by approximately two times due to enhanced emissions associated with fossil fuel and biomass burning (Gauss et al. 2006; Denman et al. 2007). Long-distance and even intercontinental transport has resulted in a steady increase in O3 concentration in rural areas hundreds and thousands of kilometers from the original sources of pollution (Prather et al. 2003). Nearly one-quarter of the Earth's surface is currently at risk from the mean tropospheric O3 in excess of 60nll-1 during mid-summer with even greater local concentrations occurring (Fowler et al. 1999a, b). This is well above the mean concentration of 40nll-1 that has been determined for damage to sensitive plant species (Fuhrer et al. 1997; Mills et al. 2000; LRTAP Convention 2007). Several scenarios indicate that concentrations of tropospheric O3 might further increase throughout the 21st century (Gauss et al. 2003); simulations for the period 2015 through 2050, project increases in tropospheric O3 of 20-25% (Meehl et al. 2007).
K. Vandermeiren (b)
Veterinary and Agrochemical Research Centre, Leuvensesteenweg 17, B-3080 Tervuren, Belgium e-mail: [email protected]
S.N. Singh (ed.), Climate Change and Crops, Environmental Science and Engineering, DOI 10.1007/978-3-540-88246-6.10, © Springer-Verlag Berlin Heidelberg 2009
The global patterns of exposure of vegetation to O3 are also changing. A prediction of the differences in annual global mean surface O3 concentrations from the 1990s to 2020s has recently been modelled by Dentener et al. (2005), showing increases in all major agricultural areas of the northern hemisphere with large spatial variation. Control measures on emissions of nitrogen oxides (NOx) and volatile organic compounds (VOCs) applied in North America and western Europe, where the impacts of O3 on crop production and forest vitality have been well established, are expected to lead to reductions in peak O3 concentrations (Gardner and Dor-ling 2000). However, the effect of these changes may be offset by the predicted increases in global background tropospheric concentrations, in particular as a result of increased global emissions of NOx (NEGTAP 2001). Furthermore, in parts of Asia, Latin America and Africa, these increases in background concentrations are combined with trends of increased emissions of O3 precursors, suggesting that current and future impacts of O3 on crops and forests in these areas may be very significant.
Climate change can further affect tropospheric O3 e.g. by modifying emissions of precursors (European Commission 2003), such as biogenic VOC emissions (e.g. isoprene) that may be highly sensitive to climate change. Although these emissions increase with increasing temperature, certain studies concur that climate-driven changes in vegetation types unfavourable to isoprene emissions (notably the recession of tropical forests) would partly compensate for the effect of warming in terms of O3 generation (Lathiere et al. 2005). Of course, changes in temperature, humidity, UV radiation intensity and atmospheric circulation brought about by climate change could affect production, transport and removal of O3 significantly and increases in regional O3 pollution are expected due to higher temperatures and weaker circulation. Other, more indirect effects of climate change may cause either an increase or a decrease in background tropospheric O3, due to competing effects of higher water vapour and higher stratospheric input (Denman et al. 2007).
Many studies have been conducted on the impacts of O3 pollution on vegetation, ranging from effects at the cellular level to predicting impacts on a regional and international scale (EPA 1996). O3 damage to plant tissues includes visible leaf injury, decreased photosynthesis and increased senescence, which has significant repercussions on the yield of major agricultural crops, biodiversity and forest health. There is no doubt that predicted increases in tropospheric O3 will impact on future agro-ecosystems and their management. Nevertheless, the major current projections of global food production under atmospheric change scenarios do not account for the damaging effect of rising O3 and current risk assessment tools do not sufficiently consider its interaction with other climatic changes (Long et al. 2005; Easterling et al. 2007). In addition, many coupled climate-carbon models have currently neglected the impacts of changing ground-level O3 concentrations on carbon cycling (Sitch et al. 2007). The aim of this chapter is to provide an overview of the impacts of O3 on crops in a changing climate.
10.2 Ground Level Ozone as a Component of Climate Change
The level of O3 in the troposphere is controlled by a complex set of photochemical reactions involving NOx, carbon monoxide and VOCs (Penkett 1991; United Kingdom Photochemical Oxidants Review Group 1993; Crutzen et al. 1999). Natural sources of NOx (e.g. from soils, lightning and transport from the stratosphere) and VOCs (e.g. from soils and vegetation) ensure that there is always a background concentration of O3 in the troposphere. There is also a contribution from incursions of O3 from the stratosphere, although this is of minor importance in the global budget (Denman et al. 2007). Anthropogenic emissions of large quantities of O3 precursors due to fossil fuel combustion and biomass burning, have substantially increased the amount of O3 since the pre-industrial era. Recent evaluations of surface measurements in the 19th and early 20th century in Europe (Volz and Kley 1988; Harris et al. 1997) clearly indicate much lower O3 concentrations than today. Since O3 is relatively short-lived, lasting for a few days to weeks in the atmosphere, ground-level distributions are highly variable and tied to the abundance of its forerunner compounds, water vapour and sunlight. Trends in anthropogenic emissions of O3 precursors (1990-2000) show reductions in industrialised regions like the USA and Organisation for Economic Co-operation and Development (OECD) Europe, while regions dominated by developing countries show significant growth in emissions (Forster et al. 2007) which has repercussions on the global O3 distribution. The boundary layer O3 concentrations show strong diurnal and seasonal cycles with daytime and summertime maxima. O3 episodes are associated with hot sunny weather and occur over wide areas; peak concentrations occur mainly during the afternoon, when photochemical O3 production is most active. At night time, however, in the absence of significant O3 formation, the O3 concentration may fall due to reactions with NO and through deposition to the surface, which is the major sink for O3 at rural sites. Moreover, sites that experience the same regional O3 distribution, may have different exposure levels due to different local features, such as elevation, wind speed, roughness of the earth's surface (Derwent and Kay 1988).
As global O3 exposures increase over this century, direct and indirect interactions with climate change and elevated CO2 will modify plant dynamics (Fiscus et al. 2005) and as such, it is vital to evaluate the impact of O3 on vegetation within a framework of future climatic conditions (Ashmore and Bell 1991). Continued emissions of the most important greenhouse gases, carbon dioxide (CO2), nitrous oxide (N2O) and methane (CH4) at or above current rates will cause further warming and induce many changes in the global climate system during the 21st century that would very likely be larger than those observed during the 20th century (Meehl et al. 2007). For the next two decades, a warming of about 0.2°C per decade is projected for a range of emission scenarios. Even if the concentrations of all greenhouse gases and aerosols had been kept constant at year 2000 levels, a further warming of about 0.1 °C per decade would be expected (IPCC 2007). However, there is unanimous agreement among the models that future climate change will reduce the efficiency of the land and ocean carbon cycle to absorb anthropogenic CO2, essentially owing to a reduction in land carbon uptake. The latter is driven by a combination of reduced net primary productivity and increased soil respiration of CO2 under a warmer climate. This positive feedback will lead to atmospheric CO2 concentrations between 730 and 1020 ppm by 2100 and an additional warming of between 0.1 and 1.5°C (Meehl et al. 2007). Globally averaged mean water vapour and evaporation are projected to increase. Increases in the amount of precipitation are very likely in high latitudes, while decreases are predicted in most subtropical land regions. A warmer future climate will also imply fewer frost days and increased summer dryness with greater risk of drought especially in the mid-continental areas. These projected climatic changes will have an impact on the response of plants to O3 (Tausz et al. 2007). But the opposite also applies: O3 itself can modify the response of plants to a range of naturally occurring environmental stresses, such as drought (Bell 1987; Heggestad et al. 1985). Other important interactions may arise from the fact that O3 alters the performance of herbivorous insect pests and plant pathogens, which will themselves be influenced by the climate change, e.g. as a result of greater survival under milder winter conditions.
O3 is one of the most powerful, highly reactive oxidants and its potential to damage vegetation has been known for over 30 years. One of the first confirmed reports of widespread foliar injury which could be attributed to O3 was the so-called "weather fleck" of tobacco in the eastern United States (Heggestad and Middleton 1959). Leaves were damaged by straw-coloured flecks making the tobacco unusable. In the early 1960s, another economically important disorder of potatoes called "speckle leaf" was observed in USA (Hooker et al. 1973), which was later associated with the concomitant occurrence of elevated tropospheric O3 concentrations. Research in recent years has advanced our understanding of the mechanisms underlying O3 effects on agricultural crops, trees and native plant species and detailed compendia have been produced to illustrate the range of symptoms produced on different species (Krupa et al. 1998).
The key process in relating O3 exposure to biochemical, physiological and final yield responses is the ease with which O3 gets access into the stomata. This depends firstly on atmospheric processes above the plant canopy that control the transfer of ambient O3 towards the vicinity of the leaf surface (Fig. 10.1). This transfer is mainly governed by wind turbulence and the roughness of the terrestrial landscape, including altitude and type of vegetation. At the leaf surface, the thickness and resistance of the boundary layer depend primarily on the wind speed and leaf characteristics, such as orientation, size, shape and hairiness. The actual diffusion of gasses through the stomata, expressed by the stomatal conductance (gs), is proportional to the atmospheric concentration of O3, but is also strongly controlled by the
Fig. 10.1 Simplified scheme of O3 transfer, plant uptake and cell response. For details: see text
Fig. 10.1 Simplified scheme of O3 transfer, plant uptake and cell response. For details: see text
stomatal aperture. The importance of these successive resistance factors is not to be ignored. High O3 concentrations often tend to coincide with the weather conditions that limit the dose of O3 absorbed by the plant: stagnant weather situations limit the O3 transfer across the atmospheric boundary layer to the vegetation and high vapour pressure deficits (VPD) (= low relative air humidity) lead to low values of stomatal conductance (Grunhage et al. 1997).
As illustrated in Fig. 10.1, once O3 has penetrated the leaf via the stomata and substomatal air space, the majority will be absorbed into the aqueous phase of the mesophyllic cell wall matrix where it reacts with water and solutes to form free radicals, such as hydroperoxide (-O2H), superoxide (-O2-) and the hydroxyl radical (■OH), which can further lead to the formation of hydrogen peroxide (H2O2) (Long and Naidu 2002). There is now an increasing evidence that these short lived, highly reactive oxygen species (ROS) are involved in O3-mediated injury (Polle 1998). Although ascorbate and other scavenging systems will partly remove O3 and ROS, a fraction may still reach and damage the outer proteins and lipids of the plasmalemma, causing cell leakage and loss of solutes. In response to O3 stress, reactive radicals are also generated inside the cell. Although ROS are considered deleterious and harmful, recent studies indicate that such an "oxidative burst" may be important to stimulate signal transduction pathways that promote plant defence responses and programmed cell death to a wide variety of stimuli, such as high light, heavy metals, mechanical and physical stresses, drought, UV radiation and pathogens (Sandermann et al. 1998; Rao et al. 2000; Van Breusegem et al. 2001). Whether the defence responses are successful or not depends on the concentration of O3, the duration of the exposure, the plant age, genotype and pre-conditioning.
Loss of photosynthetic capacity is an early phenomenon of O3 exposure and sometimes the only physiological symptom of damage during chronic exposure. This may be also attributed partly to a decrease in the amount and activity of the CO2 fixating enzyme, ribulosebiphosphate carboxylase (Rubisco) (Lehnherr et al. 1988; McKee et al. 1995) and partly due to accelerated senescence, with a down-regulation of photosynthetic genes and an up-regulation of genes involved in programmed cell death and/or tissue senescence. Inhibition of CO2 assimilation can also result from direct or indirect inhibition of stomatal opening that reduces uptake (Saurer et al. 1991; Torsethaugen et al. 1999). These biochemical and physiological changes determine the final effect on plant vitality and productivity, although all the processes by which O3 leads to reductions in agricultural yield are complex and not always fully understood. For example, the same O3 episode may have different effects on crop yield depending on when it occurs (Vandermeiren et al. 1995; Soja et al. 2000). This is related to the relative sink and source strength and hence, on partitioning priorities at the time of exposure.
Due to changes in pool size of metabolites, the effects on crop quality can be significant. Importantly, the altered biochemical state, including increases in antiox-idant scavenging systems within the tissue, may change the response of the plant to existing environmental conditions and other stresses. This "cross-induction" suggests that distinct stresses may activate the same, or at least overlapping, signal transduction pathways (Sharma and Davis 1994). Rao et al. (2000) indeed showed that pre-exposure to O3 induced resistance to subsequent pathogen infection.
As such, there are two modes of O3-induced injury patterns currently categorized by Long and Naidu (2002):
1) Acute injury due to exposure to high concentrations, 120-500 nl l-1, for hours, may occur at the most polluted sites. Distinct visible injury like water-logging is detected on the leaves in several hours, the area of which then turns into typical O3 symptoms (necrotic stippling, bronzing or chlorosis) within a few days. Under these exposure conditions, toxic reactions of O3 with cellular components exceed the tolerance level of the cells, resulting in cell death.
2) Chronic injury is a consequence of exposure to an elevated background concentration with peak daily concentrations in the range of 40-120 nl l-1 over several days in the growing season. This type of injury is more subtle and, depending on plant species, may include symptoms such as chlorosis and premature senescence, resulting in earlier leaf abscission and flowering (Pell et al. 1997). Often no visible injury is observed, but lower rates of photosynthesis do indicate adverse effects on plant vitality. Decreased photosynthetic capacity and accelerated loss of leaf area will depress plant productivity, leading to losses in crop yield.
10.4 Impacts of Ozone on Crop Production and Quality
Whilst extreme acute O3 exposure damages the plasmalemma to the extent that the cell is unable to maintain its ionic balance and cell death follows, less acute and chronic exposure diminishes whole plant productivity which may affect the final marketable yield prior to the occurrence, if any, of lesion formation (Heagle 1989; Heath and Taylor 1997). Acute injury can cause obvious and immediate loss of economic value, if the market value of the species depends on its visible appearance, such as many horticultural crops. Severe damage has been observed on irrigated crops in the Mediterranean region (Fumigalli et al. 2001). For example, an O3 episode north of Athens in 1998 caused severe reddening and necrosis on lettuce (Lactuca sativa) and chicory (Chicorium indybus L. and endivia L.) with 100% loss of the commercial value of the products (Velissariou 1999). There have also been several reports of visible O3 injury in North America and Europe (Emberson et al. 2003), and also in a range of horticultural crops in Taiwan (Sheu and Liu 2003).
It is well established that there are pronounced differences in O3 sensitivity between species, but also between varieties within species. Many of the published lists of sensitive species are based on visible injury induced by acute O3 exposure (Mills et al. 2000; Table 10.1), but these rankings may not be related to relative sensitivity in terms of yield or physiology responses to longer-term exposures (Ashmore 2002). When crops were ranked in sensitivity to O3 by determining the AOT401 associated with a 5% reduction in yield, wheat, pulses, cotton and soybean were the most sensitive of the agricultural crops (Mills et al. 2007; Table 10.2). Several horticultural crops, such as tomato and lettuce were of comparable sensitivity. Crops, such as potato and sugar beet, that have green foliage throughout the summer
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