Ozone occurs naturally in the stratosphere and forms a protective layer that shields the Earth from harmful radiation. However, at ground level this gas is an air pollutant that can exacerbate human respiratory problems and negatively affect vegetation.
Ground-level ozone is produced from sunlight-driven reactions between gases such as carbon monoxide (CO), nitrogen oxides (NOx), methane (CH4) and non-methane volatile organic compounds (nmVOCs). These precursor gases can originate from natural sources, including wildfires and lightning, but additional ozone is formed as a result of human activities, particularly emissions from vehicles and industry, including fossil fuel burning.
“ozone is an air pollutant that can exacerbate human respiratory problems and negatively affect vegetation”
Warm and sunny weather conditions can lead to ozone ‘episodes’, when concentrations of the gas in the atmosphere can peak for several days at a time. Ground-level ozone concentrations vary around the world, depending on the time of year, geographical location and proximity to sources of emissions. However, as a transboundary pollutant, the gases that react together to form ozone (precursors) can travel thousands of kilometres from their sources, and ozone concentrations can be particularly high in rural areas downwind of cities.
Ozone pollution increased greatly between the end of the 19th and 20th centuries, with a reported doubling of concentrations between the 1950s and 1990s at sites in Europe. In recent years, ozone levels have become more stable in Europe and declined in North America due to the implementation of policies to improve air quality. However, ozone in rapidly developing regions continues to rise, and the scale of the problem in many crop-growing areas of Africa, for example, is not well understood because monitoring stations are often located in urban rather than rural areas. Additionally, the patterns of pollution in Europe are changing. While the peaks in concentrations during the summer have been declining, background levels are gradually increasing due to the transport of ozone precursors from other regions.
How does ozone affect plants?
Ozone enters plants through pores on the leaf surface (stomata). It is a very reactive gas and quickly leads to cell wall and membrane damage and the disruption of photosynthetic processes. When the antioxidative ability of a cell is overwhelmed, cell death can occur, resulting in visible damage to the leaf. While visible symptoms can vary between species, there are several features that tend to be commonly found in ozone-damaged plants:
- Small, pale yellow, cream or bronze coloured pin-head sized blotches, known as stipples, occur between the leaf veins. These spots can join up to cover large areas of the leaf when ozone concentrations are high.
- Damage appears on the upper surface of the leaves, spreading to the underside in severe cases.
- Older leaves towards the base of the stem and branches tend to be more affected than younger leaves as damage is determined by the accumulated uptake of ozone over time. Even low ozone concentrations can lead to visible injury. This happens when conditions are very favourable for ozone intake into the leaf, for example, when nutrient, light and moisture levels are high, and stomata are open.
“differences in ozone sensitivity can lead to long-term changes in species evenness”
Over the longer term, plant growth can be affected by ozone from a combination of reduced photosynthesis following damage, and reduced leaf area as ozone-damaged leaves fall early from the plant. Ozone negatively affects many different types of vegetation. Impacts on trees include visible injury on leaves, an increase in the rate of ageing of leaves and loss of leaves from the tree crown, as well as a reduction in growth and therefore carbon sequestration. For some species, the number of flowers can be reduced by ozone. In diverse plant communities, differences in ozone sensitivity between species can lead to long-term changes in species evenness or richness. Grassland and wetland habitats are important for biodiversity conservation, and in some habitats in milder climates, species are exposed to ozone over long growing seasons.
Ozone threat to food security
Research has shown that ozone exposure can affect the yield of sensitive species of crops including soybean, common bean, pulses, wheat, and to a lesser extent rice, potato and maize. As these crops are staple food sources around the world, ozone pollution has the potential to impact food security. Visible damage to ozone sensitive leafy crops can also negatively affect crop quality and therefore market value.
Global modelling1 led by the UK Centre for Ecology & Hydrology (UKCEH) has estimated the impacts of ozone on wheat, maize, soybean and rice yield. Crops varied in sensitivity to ozone, with global yield losses greatest for soybean (12.4%), then wheat (7.1%), rice (6.1%) and maize (4.4%). The impact of ozone on yield was found to compare in importance with other key pressures including heat stress, aridity, and soil nutrient availability.
Our analysis of the impacts of ozone pollution on global wheat production2 showed that estimated yield losses were high in humid rain-fed and irrigated areas of major wheat-producing countries (e.g. United States, France, India, China and Russia). Total production losses in developing countries receiving Official Development Assistance (ODA) were found to be 50% higher than those in developed countries. This is important as it suggests that ozone pollution has the potential to reduce the possibility of meeting UN food security targets. Recently, UKCEH has been investigating the ozone impact on African crops3. Our results show the negative effect of increased ozone on the yield of African wheat and common bean cultivars, which are varieties that have been cultivated by selective breeding.
Different cultivars of the same crop can show varying sensitivity to ozone. These differences are thought to be influenced by characteristics of each cultivar including rate of ozone uptake through the leaf pores or antioxidant capacity. Studies have indicated that ozone sensitivity of crop cultivars could vary between continents. For example wheat and rice cultivars grown in Asia have been found to be more sensitive to ozone than those grown in North America. Ozone can also impact quality of crop grains, for example, a study of the effect of current ozone concentrations using filtered air found a reduction in grain protein yield, which has further potential consequences for human nutrition.
Pioneering research facilities
Scientists across the world, including experts at UKCEH, have been investigating the effects of ozone on crops for many years, using a variety of exposure methods, including closed and open-top chambers, solardomes and field release systems. Each method has pros and cons. Field release systems allow plants to be grown in their natural environment, but can be very expensive to set up and run. Open-top chambers allow plants to be grown under controlled conditions. However, the chamber enclosures can have an impact on the plant environment, for example, elevating temperature and reducing light, potentially leading to unnatural growing conditions.
The UKCEH field site in Bangor in North Wales, is currently the only place in the world where both solardomes and Free-Air Ozone Exposure (FAOE) field release rings are in operation together. There, UKCEH scientists carry out experiments on the impacts of ozone on crops using eight solardomes (glasshouses) with ozone concentrations set at different levels by computer, allowing a simulation of ozone episodes. Three of the domes also have a heating system to allow tropical crops to be grown in more natural conditions. Crops grown in the solardomes include wheat, beans, millets and sweet potato as well as specific African crops.
In addition to investigating the impact of elevated ozone on crop yield, other physiological measurements can be taken, including chlorophyll content of the leaves, gas exchange through the stomata, and rate of photosynthesis. Using measurements on the rate of gas exchange and other environmental factors, including light level and temperature, it is possible to calculate how much ozone the plants are taking in (ozone flux).
Data on how yield varies with increasing ozone uptake from different cultivars of the same crop can be combined to establish dose-response relationships, which can be used to set critical levels and improve risk assessment of ozone pollution for crops. Using an approach based on concentration alone, high levels of damage are predicted to be present simply where ozone concentration is highest. However, as local meteorological conditions may affect stomatal opening and ozone uptake, the flux-based approach, which is a measure of how much ozone the plant is taking in, is the preferred method for risk assessments.
To predict impacts on crop yield at a larger scale, modelling studies are used. This method is particularly useful for providing estimates of crop yield loss for regions lacking ozone measurements or where it is difficult to carry out field experiments.
Our research shows that ozone pollution is reducing production of staple food crops in areas of the world that are already challenged by other stresses. It is therefore important to consider methods of mitigating against the negative effects of ozone, which would lead to benefits in terms of crop yield.
In the long term, international efforts are required to reduce the emissions of the gases that can join to form ozone, which can damage crops grown locally and in other countries. There are, however, short-term solutions that can reduce ozone damage.
“timing irrigation when there are low levels of ozone could minimise the impact on crop yield”
Irrigation can increase ozone uptake by the plant as leaf stomata are opening to allow water intake, thereby increasing damage to the plant. Therefore, timing irrigation when there are low levels of ozone could minimise the impact on crop yield. A UKCEH study4 involving wheat in Kenya also found that reduced irrigation stimulated grain weight, which compensated for ozone-induced reductions in well-watered plants. In rice-growing countries, the process of alternate wetting and drying irrigation (AWD), where fields are allowed to dry for a few days before re-irrigation, rather than maintaining continuous standing water, can be used to reduce water usage and methane emissions. This approach may be useful to reduce the ozone impact on rice yield.
There is also potential to reduce the yield loss by growing ozone-tolerant crop cultivars, either using traditional breeding approaches such as pedigree selection (though this can be time consuming and costly) or molecular methods such as marker assisted selection (MAS). Possible targets for breeding of ozone tolerance include reducing the stomatal uptake of ozone into the leaf and increasing its detoxification once inside the leaf. However, tolerance to ozone needs to be balanced with other favourable characteristics, such as fast growth, high yield and drought tolerance.
Science informs global action
The International Cooperative Programme on Effects of Air Pollution on Natural Vegetation and Crops (ICP Vegetation) was established in 1987 to consider the underlying science for quantifying damage to plants caused by air pollutants, particularly ozone. Now, more than 300 scientists from around 60 countries participate in the programme, which is part of the activities of a working group under the UN’s Convention on Long-range Transboundary Air Pollution (LRTAP).
ICP Vegetation is led by UKCEH in Bangor, and the chair is Dr Felicity Hayes, who has been involved in its work for more than 20 years. The programme:
- Collates evidence of ozone impacts on vegetation (for example from field surveys, biomonitoring and ozone exposure experiments)
- Develops ozone dose-response/flux-effect relationships to establish safe thresholds (critical levels) for ozone impacts on vegetation
- Models and maps impacts of ozone on vegetation from local to global scale
- Studies interactive impacts between ozone pollution and climate change, and interactive impacts between ozone and other air pollutants such as nitrogen on vegetation
Task Force meetings are held for ICP Vegetation participants from around the world every year, giving the opportunity for the latest research and achievements over the last year to be presented, and future plans to be discussed.
The results of the scientific work of the ICP Vegetation support policy including the development of LRTAP protocols, which commit countries to reducing pollutant emissions by specific target years. The ICP Vegetation also produces reports which include policy recommendations, with recent topics including the impacts of ozone on carbon sequestration, ecosystem services and biodiversity, and food security.
Support for farmers
ICP Vegetation has also been involved in outreach work to spread the message about the damage that ozone pollution can cause to crops. An online course has been developed, introducing the problem of ozone pollution and its effects on tropical crops. Additional resources include a YouTube video, webinars and leaflets/brochures on ozone impacts. Lastly, in collaboration with the Centre for Agriculture and Bioscience International (CABI), information on the symptoms of ozone damage on crops has been included in the Plantwise Knowledge Bank. Led by CABI, Plantwise is a global programme, which aims to help farmers reduce yield losses caused by plant health problems. A network of plant health clinics has been set up, providing farmers with practical plant health advice.
UKCEH has also developed the Ozone Injury smartphone app5 to allow users to submit records of incidences of visible ozone injury on vegetation. The identification of visible injury is a low-cost method of determining if a species is being negatively affected by ozone pollution. This is particularly useful in countries where it may be difficult or impractical to perform field experiments on the impact of ozone. Collection of field-based evidence on the occurrence of ozone-induced leaf injury enables the verification of predictions from experiments and models and helps to demonstrate the impact of current ambient ozone levels.
ICP Vegetation will continue researching the impacts of ozone on vegetation and gathering evidence of ozone damage. Activities on the agenda for the next couple of years include a state of knowledge report on the genetics of crop resilience to ozone and potential for improved crop breeding, and further modelling work using ozone risk assessment for vegetation under various air pollution scenarios, focusing on the contribution of methane as a precursor. There is also some ongoing collaboration with modellers to include ozone effects in crop growth models, which would improve understanding of the role ozone will play in limiting food supply in the future.
Overall, research suggests that ozone pollution could be one reason for unexplained agricultural yield gaps and slowing down of yield improvement seen in many areas of the world. Therefore, international cooperation to reduce ozone pollution and increased research into solutions for mitigation would provide benefits for agriculture and other types of vegetation.