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ICPEP-3 (2005) Souvenir

How Air Pollution Can Change the Response of

Plants to Other Environmental Stresses

J N B Bell

Professor of Environmental Pollution,

Centre for Environmental Policy/Division of Biology

Imperial College London, Silwood Park campus, Ascot

Berkshire, SL5 7PY, UK.


It has been known since the 17th century that air pollution can cause serious damage to vegetation, causing both visible blemishes on foliage and/or reductions in growth and crop yield. Research into this topic started in the late 19th century, initially in Germany, but followed rapidly by the UK, USA, Canada and elsewhere. Initially interest was centred on the traditional pollutants in the form of coal smoke and SO2, later it was realised that there were other phytotoxic pollutants present in the atmosphere. Thus in the period after World War II interest shifted to photochemical oxidants, particularly O3, formed as secondary pollutants resulting from complex atmospheric chemical reactions involving nitrogen oxides and volatile organic compounds under conditions of high temperature and sunlight. The recognition of O3 as a widespread pollutant, particularly in rural areas, occurred first in California, then elsewhere in North America, followed by Europe and Japan in the 1970s and much more recently in some parts of the developing world, although in the latter case the severity of the problem is largely unrecognised. Subsequently other pollutants became recognised as of major importance, notably NO2 and NH3 and their products. Widespread problems are not restricted to O3, because acid rain and total nitrogen deposition are known to cause large scale problems of acidification and eutrophication, respectively.

The best example of an attempt to estimate the economic impacts of air pollution on crops was the National Crop Loss Assessment Network (NCLAN) carried out in the USA in the 1980s, followed by a similar programme in Europe. This concentrated mainly on O3 and predicted a loss of $3 billion per annum for the 10 principal widely grown crops in the USA. It should be noted that this programme concentrated on the impacts of pollution on crop yield. However, there are a numerous other stresses, both abiotic and biotic, which cause enormous losses to agriculture, up to an order of magnitude higher than the estimates of NCLAN. Thus if the response of plants to these other stresses could be modified by air pollution, then the economic consequences could be substantial, including both negative and positive effects. In this article a brief overview will be given of the evidence for air pollutants impacting on these other stresses.

Abiotic stresses

There are a wide range of abiotic stresses which impact vegetation, including frost/low temperature, high temperature, drought, salinity, wind and mineral deficiency/toxicity. The best researched areas of interactions of abiotic stresses with air pollution are for frost and drought, with, to a much lesser extent, salinity.


There is abundant evidence that air pollutants can sensitise plants to frost damage, particularly in the case of SO2 and O3. Numerous controlled experiments have demonstrated that fumigated plants which are subsequently exposed to low temperatures show much greater frost injury than those that were previously exposed to charcoal- filtered clean air. Much interest in this issue was shown in both eastern North American and Europe during the 1980s, when major research programmes examined the possible role of O3 in .forest decline.. This followed observations that tree health showed particularly severe deterioration following harsh winters. It was demonstrated conclusively that a summertime fumigation with O3 resulted in increased sensitivity to subsequent frost stress, including visible injury and delayed hardening in a number of tree species. Likewise it is now well known that heather in European heathlands, impacted by high levels of N deposition is sensitive to frost damage, leading to gaps in the canopy which permit the invasion of nitrophilous grasses and deterioration of these habitats of high conservation value.

Similar effects have also been demonstrated for herbaceous species, including grasses, cereals and clovers. In the UK the potential for SO2 to exacerbate frost injury has been shown in both laboratory and field studies. In the latter case, of particular interest are observations at two open-air fumigation systems, where cereals were subjected to SO2 in fields where different plots received different concentrations of SO2 from computer controlled arrays of pipes. In such a situation the crop is subjected to all the local natural stresses, both abiotic and biotic. It was recorded in both systems that following periods of cold weather injury was significantly greater in the plots which had been fumigated with SO2, with an indication of a dose/response relationship. My own research group has demonstrated a similar phenomenon, but this time caused by ambient pollution. In February 1986 we were carrying out an overwinter experiment in which four cultivars of red clover were grown in open-top chambers, ventilated with ambient or clean charcoal- filtered air, or else in outside chamberless plots. This month was exceptionally severe for the south of England, as the temperature fell below zero for four weeks. At the end of this period severe low temperature injury was seen on all the experimental plants, this being similar in the outside plots and the ambient air chambers, but significantly reduced in all cultivars in the charcoal-filtered chambers. Thus ambient air pollution had sensitised the clovers to frost injury. The pollutant(s) involved could not be identified unequivocally. O3 can be dismissed as it is not elevated under winter conditions, but it is known that large areas of Western Europe, including the UK were blanketed in a cloud of high SO2 concentrations at the time, although the role of NO2 cannot be precluded.


It is generally held that drought reduces air pollution injury by reducing stomatal conductance, thereby inhibiting the uptake of pollutant gases into the leaf. However, this appears to be a complex situation, about which it is difficult to generalise, not the least because air pollutants have been demonstrated both to open and close stomata, depending on species, pollutant concentration and prevailing environmental conditions. In the case of soya beans in the USA and trees in the UK it has been shown that the nature of the O3/drought interaction reverses, depending on pollutant concentration. of particular interest is a study in the UK, which showed that pretreatment with a SO2+NO2 mixture predisposed a grass species to drought stress. The grass was fumigated with a range of pollutant concentrations or else kept in clean air, before all plants being transferred to the latter treatment, with half being kept well-watered and the other half droughted. The watered plants showed no effect of pollution pretreatment, but the droughted plants showed a concentration-dependant reduction in growth, when pretreated with SO2+NO2. As in the case of frost injury, there has been considerable interest in the role of O3/drought interactions in contribution to forest decline, in view of the latter apparently becoming worse following very dry summers. However, it is difficult to elucidate the respective roles of these two stresses in view of the fact that very dry summers always coincide with particularly high O3 levels.

Biotic stresses

As in the case of abiotic stresses, their biotic equivalents are responsible for massive crop losses worldwide. These can take many forms, the principal being fungal pathogens, herbivorous insect pests, viruses, bacteria and nematodes. The interactions of air pollutants on all of these have been investigated, with emphasis on fungal interactions.

Fungal Pathogens

Observations have been made for many years that the incidence of a range of fungal pathogens appear to be related, either positively or negatively, to elevated levels of air pollutants, most of these being in the vicinity of point sources. In general it appears that biotrophs (fungi not readily cultured in the absence of the host) were reduced in pathogenicity, while non-biotrophs showed a more mixed response. It was postulated that the former was a reflection of the intimate connection between the metabolism of the pathogen and the host, with pollutant-induced impairment of the latter resulting in damage to the fungus. In the case of stimulation it was suggested that injury to the host's surface provided courts of infection for the pathogen. Many studies have been carried out on pathogen/pollutant interactions, although only a relatively small number of the vast range of potential combinations have been investigated. Thus only a selection will be given here, concentrating on the results of my own research group. One particularly interesting study of ours involved investigation of the natural infection of barley, growing in one of the open-air SO2 fumigation systems mentioned earlier. This showed that in three successive growing seasons infection by powdery mildew was stimulated by SO2, but the reverse occurred for leaf blotch. A controlled fumigation with the same concentrations of SO2 in chambers confirmed the causal nature of the field system observations. The use of economic models for infection/crop yield reduction of these host/pathogen systems indicated that the combined net effect of them would be negative at all concentrations employed. Of particular interest here is the fact that powdery mildew is classed as a biotroph, indicating that the suggestion that biotrophs are reduced in infection by air pollution is certainly not a universal phenomenon.

There are two interesting cases where fungal pathogen incidence has been related to air pollution levels to the extent that they are considered to be (and in one case has been) employed as biomonitors. Both of these have been investigated by my group. The first of these is black spot of roses a ubiquitous disease of rose leaves. In the past when SO2 levels were very high in many parts of the UK, this disease was reported as absent from the more polluted areas. A study in the mid-1960s showed that its incidence was negatively related to the prevailing SO2 concentration in a study of nurseries nationwide. The causality of this relationship was confirmed by controlled fumigation experiments.

Subsequently with the massive fall in concentrations, anecdotal evidence indicated that it had reinvaded locations where it was formerly absent. A study by a member of my group involved revisiting the locations of the 1960s survey and showed clearly that reinvasion had occurred everywhere and that there was no indication of any relationship with the residual SO2 levels. The second disease was rather more controversial and studies have produced intriguing results. This was the tarspot of sycamore, which takes the form of large black lesions on the tree's leaves. A field study in cities of northern England in the mid-1970s showed a negative relationship between a calculated tarspot index (TSI: number of spots per leaf unit area) and SO2 concentrations, which showed a similar cut- off level for total elimination as in the earlier black spot research. Thus it was postulated that TSI was a good bioindication of prevailing SO2 concentrations and it was incorporated into lichen biomonitor surveys in parts of northern England in the 1970s. However, a survey in the mid-1980s in Edinburgh failed to find the same relationship, and it was suggested that the earlier findings were an artefact viz. that in the more polluted areas towards the centre of cities the activities of street cleaners and park keepers increasingly removed the only source of inoculum in the form of spores over wintering on dead leaves on the ground. I used this example some years ago in a lecture I gave on a short course on environmental science for lawyers, as an exemplary lesson in the dangers of attributing causality to observed relationships. It was entitled .Correlation and Causality: Park Keepers or Pollution.! However, I had to eat my words! In the late 1980s some of the last controls on SO2 emissions from domestic coal-burning were imposed around colliery villages in north-east England. A colleague from the local University of Newcastle upon Tyne observed that with falling SO2 concentrations, not only did black spot of roses show reinvasion, but so also did tarspot of sycamore! Intrigued by this we studied the relationship between TSI and air pollution in the London area and a region of northern England (around the city of Sheffield). In the case of the Sheffield area tarspot had been recorded as absent in the mid-1970s in the more polluted places, in a biomonitoring study. When we resurveyed the area in 1999 the disease was prevalent in effectively all sites, and showed no relationship to the contemporary (much lower) SO2 concentrations. Interestingly there was one site where it was absent: in the very middle of Sheffield, where a single tree was surrounded by concrete paving and there was no possibility of spores surviving over winter to reinfect. Thus there was overwhelming evidence that SO2 and TSI were negatively related and that the latter was potentially a good biomonitor. However, as part of the same study, the TSI of sycamore trees was measured along a transect of 50 km from a rural area into central London. It was found that the disease disappeared within London. Initially it was postulated that its relative short spore dispersal distance might have delayed reinvasion. However, this was refuted by a field study where saplings from a clean area were exposed along the same transect, together with inoculum in the form of infected dead leaves placed alongside. Again the fungus failed to reinfect within London. There would appear to be only two possible explanations: differences in climate along the transect and/or increasing NO2 concentrations towards central London. The former can be dismissed as the changes in climatic parameters between the rural area and central London are far less than those around the UK, where the disease is ubiquitous (including Edinburgh). The most likely explanation is that the fungus is sensitive to NO2, a pollutant which has its highest levels in the UK in London. This would suggest the potential for TSI to be used as a biomonitor for NO2.


As in the case of fungal pathogens, for many years there have been field observations of changes in herbivorous pest (both sucking and chewing) infestation of vegetation in polluted areas. These have largely shown increases in incidence, but there are some opposite cases, particularly at very high pollutant concentrations. These observations have been made around point, diffuse and line scources (in the form of busy roads). Various studies have examined the causality and underlying mechanisms of these effects, employing field, filtration, fumigation and survey techniques. Some of the work of my research group on this topic will now be summarised.

Our initial work started as a result of discussions between myself and a colleague. The latter was an entomologist, interested in the relationship between host plant chemistry and herbivorous insect performance. My colleague was well aware that subtle changes in the amino acid composition of a plant could have major impacts on the performance of insects feeding on it. I was aware (from the literature) that air pollution could influence plant amino acid composition. Thus, ipso facto, we established the hypothesis that air pollution could alter pest infestations via changes in plant chemistry. We had no funding to test this hypothesis, but then in 1982 a gift arrived from Germany in the form of a student who wanted to carry out his Diplom Arbeit with us, and we suggested this topic. Probably one of the best decisions we ever made! As in other work, we developed a programme to verify the causality of field observations. For many years colleagues had worked on models to predict the outbreak of the serious sucking pest, black bean aphid, on crops in summer, by studying the number of eggs on its over winter host in different parts of the country. Consistently these models under predicted the outbreaks in areas impacted by the pollution plume downwind to the east of London. Thus we decided to investigate the impacts of SO2 and NO2 on this aphid. We fumigated the bean for short periods withSO2 and NO2 and then put the plants in clean air. Weighed aphids were caged on the leaves of fumigated plants and then reweighed three days later. It was demonstrated that the growth rate of aphids feeding on previously fumigated plants was increased above that of those on clean air controls. A parallel study examined the growth rate of aphids feeding on artificial diets, mimicking bean phloem sap, and showed no effect. Thus our hypothesis was confirmed that air pollution could change pest performance via effects on the host plant and most of our subsequent research has suggested that this is mediated via plant chemistry, particularly shifts in amino acid composition. Subsequently we have shown that this phenomenon is widely distributed across a wide range of pest/host plant systems. More confirmation of the relationship was determined by three further parts of the same investigation: a filtration study in central London showed the same effects, as did a transect exercise in which plants were exposed along a declining gradient of air pollution out from central London; finally an examination of aphid trap data around the UK showed that most species occurred at greater levels in areas with higher SO2 pollution. The magnitude of the response of these insects which have a very short life cycle, indicates that they could readily escape the control of their natural enemies in the form of predators and parasites. Subsequent research has confirmed this, including measurements of infestation by aphids on barley  in one of the field SO2 fumigation systems discussed earlier. Ozone has also been shown to affect aphid performance, mediated via the host plant. Our own work has shown in chamber filtration experiments in a rural area that the pollution climate of a relatively low O3 summer produced a substantial increase in colony size of black bean aphids feeding on beans. Other work has shown that O3 levels only just above the natural background can produce substantial increases in aphid growth rates. In the case of O3 there is evidence that there may be complex interactions with duration and temperature of exposure.


The subject of air pollution impacts on plant response to natural stresses remains relatively little studied. Yet it has potentially very significant implications for crop production not least in developing countries. It has so far been totally ignored in the establishment of air quality standards and guidelines, with the single exception of the United Nations Economic Commission for Europe's incorporation of extreme low temperatures into the critical levels for forests and natural vegetation, which are lowered by 25% in such circumstances. My conclusion is that the world is missing the opportunity to address a really serious threat to food security, notably in developing countries. Everybody understands the importance of frost, drought, insect pests and pathogens. Few understand the direct impacts of air pollution on crops. And fewer still understand the potential for the first of these to be impacted by the second!


Davison, A.W. & Barnes, J.D. (2002) Air pollutant-biotic stress interactions. In: Bell, J.N.B. & Treshow, M. (eds.) . 2nd  edition. John Wiley & son, Chichester. Pp 359-377.

Flückiger, W., Braun, S. & Hiltbrunner, E. (2002) Effects of air pollutants on biotic stresses. In: Bell, J.N.B. & Treshow, M. (eds.) . 2nd  edition. John Wiley & son, Chichester. Pp 379-406.

This article has been reproduced from the Souvenir released during the Third International Conference

on Plants & Environmental Pollution (ICPEP-3) held at Lucknow from  28 November to 2 December 2005.

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