Ozone :: Arable and horticultural

Ecosystems: 

Effects and implications

  • Visible leaf injury can reduce the value of horticultural crops;
  • Visible leaf injury and/or premature leaf die-back can result in reduced growth during a growing season;
  • Reduced growth and yield (both quantity and quality) of sensitive species;
  • Potential alterations in numbers and timing of flowering and seed production;
  • Alterations of response to other environmental stresses such as drought stress;
  • Potential enhanced susceptibility to pests and diseases.

For crop species, visible injury to leaves and reduction to crop yield can occur. Crops that are sensitive to ozone (in terms of yield) include wheat, ‘peas and beans’ and onion. Moderately sensitive crops include potato, barley and maize, whereas oats are less sensitive (Mills and Harmens, 2011).

For mixed sown grasslands, habitat structure could be altered via changes in growth of component species, particularly as the extent of growth reduction would vary between species. In addition, habitat function could be impacted via changes in timing of flowering and leaf-fall.

Overview: evidence, processes and main impacts

Ozone is very reactive; the reactive oxygen (molecular) species that form as ozone enters a leaf can cause damage to cell components, e.g. cell membranes. Reactive oxygen species are also produced by plant cells in many processes involved in growth and development and from abiotic stresses, e.g. high light intensity and drought. This is one of the reasons that some symptoms of ozone pollution are not specific to ozone.

Ozone exposure studies have shown that ozone-specific visible leaf injury symptoms can occur for some horticultural crops e.g. parsley and coriander, some arable crops e.g. potato and maize (Hayes et al., 2007) and some grassland species of pastures, e.g. Trifolium repens (e.g. Bungener et al., 1999; Wilbourn et al., 1995). Many crops show reductions in yield with elevated ozone concentrations, but the magnitude of the effect varies between species and can also vary between cultivars (Mills and Harmens, 2011).

It has been demonstrated that ozone can impair the functioning of leaf pores (stomata) responsible for gas exchange (e.g. water, carbon dioxide, ozone) between the plant and the atmosphere. Although not yet shown for crop species, a reduced response to drought has been shown for Leontodon hispidus (Mills et al., 2009) and Ranunculus acris and Dactylis glomerata (Wagg et al., 2013), implying that soil drying during a prolonged drought would be further exacerbated by ozone pollution. 

Concentration-based critical levels have been established for the protection of crop yield and the vitality of pasture and fodder quality in productive perennial grasslands. These are based on the accumulated ozone concentration over a threshold of 40 ppb during daylight hours (AOT40), accumulated over a stated time period. Concentration-based critical levels have been defined for agricultural (based on wheat) and horticultural crops (based on tomato), and for pasture dominated by annuals or perennials (see critical levels table). Ozone concentrations are measured or calculated for the top of the plant canopy (LRTAP Convention, 2011). 

More recently it has been shown that the impacts of ozone depend on the amount of the pollutant reaching the sites of damage within the leaf (Phytotoxic Ozone Dose = POD) and stomatal (leaf pore) flux-based critical levels were developed to address this. The flux-based critical levels for effects on crops are based on flux to the upper canopy leaves, and have been derived for wheat, potato and tomato (LRTAP Convention, 2011; Mills et al., 2011b). For pasture the critical level is based on Trifolium. Species of the genus Trifolium (clovers) were selected from the many species considered because: i) effects of ozone in ambient air on these species are widespread across Europe; ii) ozone exposure experiments have confirmed that these species are amongst the most sensitive to ozone of those tested in Europe (e.g. Hayes et al., 2007); and iii) Trifolium species have an important role as nitrogen fixers within grassland ecosystems. The critical level was determined for a 10% reduction in biomass of Trifolium species, the lowest percentage biomass reduction that was statistically significant (see critical levels table).

Pollutant type and risk

Ozone is a naturally occurring chemical in the lowermost layer of the Earth’s atmosphere. Natural sources of the precursors of ozone such as oxides of nitrogen and non-methane volatile organic compounds ensure that there is always a background concentration of ozone.  Additional ozone is formed from complex photochemical reactions of precursors, which include NOx, carbon monoxide and non-methane volatile organic compounds, released due to anthropogenic emissions. Ozone concentrations are usually highest in rural and upland areas downwind of major conurbations. However, some regions with more moderate ozone concentrations also have high risk of effects where climatic conditions favour ozone uptake by the plants.

In the UK large areas of arable land coincide with areas where the ozone exposure is generally highest. In particular, ozone concentrations and fluxes to wheat tend to be highest in central and southern England, including East Anglia, so that predicted economic losses for ozone effects on wheat are generally highest in this region (Mills and Harmens, 2011). However, variations occur between years due to variation in climate and ozone concentrations (Mills et al., 2011a)  

Indicators of ozone impacts

These can be difficult to identify in ‘field’ conditions. Often the symptoms of ozone injury are those of a general stress response, and in addition a rapid turnover of damaged leaves can make attribution to ozone pollution difficult. Some species exhibit ozone-specific visible leaf injury symptoms in controlled studies and these ‘typical’ symptoms of visible leaf injury attributed to ozone have occasionally been observed in natural conditions. Legumes are one of the species groups on which these symptoms are most likely to be observed.

Examples of species specific responses

Some examples of specific responses are given in the table below. This does not represent a comprehensive review of all species impacts. Crops that are sensitive to ozone (in terms of yield) include wheat, ‘peas and beans’ and onion. Moderately sensitive crops include potato, barley and maize, whereas oats are less sensitive to ozone (Mills and Harmens, 2011).

Species

Response

Reference

Wheat

Reduced yield

Many examples, including Pleijel et al., 2006

Tomato

Reduced yield

e.g. Calvo et al., 2007

Potato

Reduced yield

e.g. Vandermeiren et al., 2005

Lettuce

Visible leaf injury

Goumenaki et al., 2007

Trifolium repens

Reduced biomass

Hayes et al., 2009

What factors modify ozone impacts?

Climatic (e.g. temperature, humidity) and soil factors (e.g. water content) that influence uptake of ozone via the leaf pores (stomata) can influence ozone impacts in some species (see above section on stomatal fluxes).

Critical levels:

Flux-based critical levels (Mills et al., 2011b, LRTAP Convention, 2011)

                        Receptor

Effect

(per cent reduction)

Parameter1

 

Critical level

(mmol m-2 PLA3)

Wheat

Grain yield (5%)

POD6

1

Wheat

1000 grain weight (5%)

POD6

2

Wheat

Protein yield (5%)

POD6

2

Potato

Tuber yield (5%)

POD6

5

Tomato

Fruit yield (5%)

POD6

2

Productive grassland (based on clover)

Biomass (10%)

POD1

2

Concentration-based critical levels (LRTAP Convention, 2011)

                        Receptor

Effect

 

Parameter2

 

Critical level

(ppm h)

Agricultural crops (based on wheat)

Yield reduction

AOT40

3

Horticultural crops (based on tomato)

Yield reduction

AOT40

6

(Semi-)natural vegetation communities dominated by annuals (including annuals in pasture)

Growth reduction and/or seed production

AOT40

3

(Semi-)natural vegetation communities dominated by perennials (including perennials in pasture)

Growth reduction

AOT40

5

1 PODY = Phytotoxic Ozone Dose above a flux threshold of Y nmol m-2 PLA s-1.

2 AOT40 = Accumulated ozone above a threshold of 40 ppb during daylight hours.

3 PLA = Projected leaf area.

References: 
Bungener, P. ; Balls, G.R. ; Nussbaum, S. ; Geissmann, M. ; Grub, A. ; Fuhrer, J. 1999 Leaf injury characteristics of grassland species exposed to ozone in relation to soil moisture condition and vapour pressure deficit. New Phytologist 142 271-282
Calvo, E. ; Martin, C. ; Sanz, M.J. 2007 Ozone sensitivity differences in five tomato cultivars: visible injury and effects on biomass and fruits. Water Air and Soil Pollution 186 167-181
Goumenaki, E. ; Fernandez, I. G.; Papanikolaou, A. ; Papadopoulou, D. ; Askianakis, C. ; Kouvarakis, G. ; Barnes, J. 2007 Derivation of ozone flux-yield relationships for lettuce: a key horticultural crop. Environmental Pollution 146 699-706
Hayes, F.; Jones, M.L.M.; Mills, G.; Ashmore, M. 2007 Meta-analysis of the relative sensitivity of semi-natural vegetation species to ozone. Environmental Pollution 146 754-762
Hayes, F.; Mills, G.; Harmens, H. ; Norris, D. 2007 Evidence of widespread ozone damage to vegetation in Europe (1990-2006).
Mills, G.; Hayes, F.; Wilkinson, S. ; Davies, W.J. 2009 Chronic exposure to increasing background ozone impairs stomatal functioning in grassland species. Global Change Biology 15 1522-1533
Mills, G.; Pleijel, H.; Braun, S.; Buker, P.; Bermejo, V. ; Calvo, E. ; Danielsson, H. ; Emberson, L. ; Fernandez, Gonzalez ; Grunhage, L.; Harmens, H. ; Hayes, F.; Karlsson, P.E.; Simpson, D. 2011 New stomatal flux-based critical levels for ozone effects on vegetation. Atmospheric Environment 45 5064-5068
Pleijel, H.; Eriksen, A.B. ; Danielsson, H. ; Bondesson, N. ; Sellden, G. 2006 Differential ozone sensitivity in an old and a modern Swedish wheat cultivar – grain yield and quality, leaf chlorophyll and stomatal conductance. Environmental and Experimental Botany 56 63-71
Vandermeiren, K. ; Black, C. ; Pleijel, H.; De Temmerman, L. 2005 Impact of rising tropospheric ozone on potato: effects on photosynthesis, growth, productivity and yield quality. Plant Cell and Environment 28 982-996
Wagg, S. ; Mills, G.; Hayes, F.; Wilkinson, S. ; Davies, W.J. 2013 Stomata are less responsive to environmental stimuli in high background ozone in Dactylis glomerata and Ranunculus acris. Environmental Pollution 175 82-91
Wilbourn, S. ; Davison, A.W.; Ollerenshaw, J.H. 1995 The use of an unenclosed field fumigation system to determine the effects of elevated ozone on a grass clover mixture. New Phytologist 129 23-32