Atmospheric ozone: Formation and effects on vegetation

Environmental Pollution 50 (1988) 101-137

Atmospheric Ozone: Formation and Effects on Vegetation

Sagar V. Krupa Department of Plant Pathology, University of Minnesota, St Paul, MN 55108, USA

& William J. Manning Department of Plant Pathology, University of Massachusetts, Amherst, MA 01003, USA

ABSTRACT Ozone ( 0 3 ) is present both & the troposphere and the stratosphere. Tropospheric 03 is predominantly produced by photochemical reactions involving precursors generated by natural processes and to a much larger extent by man's activities. There is evidence for a trend towards increasing tropospheric 0 3 concentrations. However, tropospheric 0 3 is known to account for only 10% of the vertical 0 3 column above the earth's surface. The stratosphere accounts for an additional 90% of the 03 column. There is evidence to suggest that there are losses in the stratospheric 0 3 due to the updraft of 0 3 destroying pollutants generated by both natural processes and by human activity. Such a loss in stratospheric 03 can result in alterations of incidence in the ultraviolet ( UV ) radiation to the earth's surface. Tropospheric 0 3 is known to be highly phytotoxic. Appropriate exposures to 0 3 can result in both acute (symptomatic) and chronic (changes in growth, yield or productivity and quality) effects. Chronic effects are of great concern in terms of both crops and forests. A number of experimental techniques are available to evaluate the chronic effects of O 3 on plants. There are limitations attached to the use of these techniques. However, results obtained with such techniques are valuable if interpreied in the appropriate context. Among all field evaluation techniques, open-top chambers are the most frequently used method for evaluating the chronic effects of O 3 on crops. The National Crop Loss Assessment Program ( N C L A N ) of the United States is the largest such effort. However, given the limitations of the open-top 101 Environ. Pollut. 0269-7491/88/$03.50 © Elsevier Applied Science Publishers Ltd, England, 1988. Printed in Great Britain

102

Sagar 1I. Krupa, William J. Manning

chambers and the experimental aspects of NCLAN, its results must be interpreted with caution. On the other hand, acute effects can be evaluated with less complexity through the use of biological indicator plants. The numerical modelling of such effects are also far less complicated than establishing numerical cause and effects relationships for chronic effects. Confounding the acute or chronic responses of plants to 03, is the presence of other kinds and forms of pollutants in the ambient atmosphere and the incidence of pathogens and pests. The resulting complex interactions andjoint effects on plants are poorly understood. Future research must address these issues. In the final analysis we have re-emphasized the fact that plant health is the product of its interaction with the physical and chemical climatology and pathogens and pests. What we have described in this context is the importance of tropospheric 03 within the chemical climatology ofour environment and its effects on vegetation.

ATMOSPHERIC OZONE The occurrence of regional scale photochemical smog in areas downwind from urban centres in many parts of the world is of much concern. According to Haagen-Smit (1952) many of the characteristics of the tropospheric photochemical smog could be explained by the presence of ozone (03) and other photochemical oxidants. These substances, he believed, were formed in the troposphere as a result of chemical reactions involving the oxides of nitrogen (NOx) and hydrocarbons (HC) present in the automobile exhaust. Significant quantities of NOx are also emitted during the combustion of fossil fuels. In addition to these observations of HaagenSmit, 03 is also known to occur in the stratosphere. The characteristics and mechanisms of formation of both the tropospheric and stratospheric 03 are discussed in greater detail in the following sections. Consult Table 1 for definitions of key terms used in these discussions.

O Z O N E IN T H E T R O P O S P H E R E The tropospheric concentrations of 0 3 across the earth's surface are governed by natural processes and by man's influence. Background concentrations of 0 3 observed in a number of locations around the world typically show average daily 1 h maxima of ~ 20-60 ppb (Singh et al., 1978). An area being classified as remote does not rule out the possibility of long range transport of pollutants to these sites. Nevertheless, long term data at

Atmospheric ozone: formation and effects on vegetation

103

TABLE 1

Definitions of Terms Used in Discussions of the Characteristics of 03 and Mechanisms of Formation Term Ekman layer

Free troposphere Photochemical oxidants Photochemical smog

Planetary boundary layer (PBL)

Stratosphere Sur['ace boundary layer

Troposphere

Definition

The layer of transition between the surface boundary, where the shearing stress is constant, and the free atmosphere where the atmosphere is treated as an ideal fluid in approximate geostrophic equilibrium. The troposphere above the mixed layer. Those substances which oxidise I- in the KI measurement method (2H + + 2I- + oxidant--*I 2 + O 2 + H 2 O ). A combination of smoke and fog consisting of pollutants produced through chemical reactions driven by radiant energy (sunlight). Also known as atmospheric boundary layer. That layer of the atmosphere from the earth's surface to the geostrophic wind level including, therefore, the surface boundary layer and the Ekman layer. Above this layer lies the free atmosphere. Earth's atmosphere between altitudes of 10 and 50 km where temperature increases with altitude. That thin layer of air adjacent to the earth's surface extending up to the so-called anemometer level (the base of the Ekman layer). Within this layer the wind distribution is determined largely by the vertical temperature gradient and the nature and contours of the underlying surface. Earth's atmosphere for approximately the first l0 km where temperature decreases with altitude (ignoring localised radiation or subsidence inversions).

such sites typically show a yearly cycle with a m a x i m u m in the late winter or early spring. Altshuller (1986) reviewed the processes t h a t can contribute to the surface O3 c o n c e n t r a t i o n s m e a s u r e d at n o n - u r b a n locations. These processes consist of" (a) t r a n s p o r t o f O a f o r m e d in the stratosphere into the free t r o p o s p h e r e a n d subsequent t r a n s p o r t d o w n into the p l a n e t a r y b o u n d a r y layer (PBL); (b) p h o t o c h e m i c a l 0 3 f o r m a t i o n within the free troposphere a n d the clean P B L ; (c) p h o t o c h e m i c a l O3 f o r m a t i o n within the polluted PBL, especially d u r i n g the passage o f w a r m high pressure systems, a n d (d) O3 f o r m a t i o n within single or superimposed plumes. The d a t a on m e a n a n d m a x i m u m h o u r l y O3, nitric oxide (NO) a n d nitrogen dioxide (NO:) c o n c e n t r a t i o n s at some n o n - u r b a n m o n i t o r i n g locations in the U n i t e d States, C a n a d a a n d U n i t e d K i n g d o m are s u m m a r i s e d in Table 2.

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Demerjian (1986), Finlayson-Pitts & Pitts (1986), and Wayne (1987) have summarised information relevant to the chemistry of the clean troposphere. According to Demerjian (1986) the photochemistry of the unpolluted troposphere develops around a chain reaction sequence involving NO, methane (CH4), carbon monoxide (CO) and 03. This reaction sequence is initiated by hydroxyl radicals (HO) formed from the interaction of O (XD), the product of photolysis of 03 in the short-end portion of the solar spectrum, with water. 0 3 ~- hv (2 < 310nm)-~O (1D) + 0 2

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107

Atmospheric ozone: formation and effects on vegetation

losses at the earth's surface. The reaction sequence for 0 3 production involves converting N O to NO2 at a rate sufficiently high to maintain a N O 2 / N O ratio to sustain the observed background levels of 03.

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Sagar V. Krupa, William J. Manning

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Atmospheric ozone: formation and effects on vegetation

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To explain the behaviour o f O 3 in remote locations, Singh et al. (1977, 1978) developed a schematic representation of variations in 0 3 concentration by season (Fig. 1). Natural 03 effects (Curve A) are expected to be at a maximum during early spring. The changes in 0 3 concentrations due to local 0 3 production and transport from urban centres, both processes resulting from the photochemical phenomena, are represented by Curves B and C. Similarly, Fig. 2 shows variations in the 03 concentrations at the surface and in the free troposphere. This Figure shows a large 03 reservoir with no average diurnal variation, except near the earth's surface where the 03 concentrations are regulated by the surface destruction and mixed layer dynamics. Alterations introduced as a result of human activity on the photochemical oxidation cycle within the atmosphere are predominantly due to two classes of compounds, volatile organic carbon (VOC) and NO, (Fig. 3). Free radical reaction on VOC is initiated by a select group of compounds which, for the most part, are activated by sunlight. Formaldehyde (HCHO) and nitrous Free Radical Initiators

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acid (HONO), in particular, show high potential as free radical initiators during the early morning sunrise period. After the initial free radical attack, the VOCs decompose through paths resulting in the production of peroxy radicals (HO z, RO2, R102, etc.), and partially oxidised products which in themselves may be photoactive radical producing compounds. The peroxy radicals react with NO converting it to NO2 and in the process produce hydroxy and alkoxy radicals (OH, RO, RIO, etc.). The alkoxy radicals can be further oxidised, forming additional peroxy radicals and partially oxidised products, thereby completing the inner loop reaction chain shown in Fig. 3, or they may attack, as would be the major path for hydroxyl radical, the VOC pool present in the polluted atmosphere, thereby completing the outer loop of the reaction chain. The data on 03 formation within some urban plumes are summarised in Table 3.

OZONE IN THE STRATOSPHERE In the stratosphere, a series of photochemical reactions involving 0 3 and molecular 02 occur. Ozone strongly absorbs solar radiation in the region from ,,~210 to 290nm, whereas 0 2 absorbs at < ~200nm. The absorption of light primarily by O 3 is a major factor causing the increase in temperature with altitude in the stratosphere. Excited 02 and O3 photodissociate, initiating a series of reactions in which O3 is both formed and destroyed leading to a steady state concentration ofO3 (Finlayson-Pitts & Pitts, 1986). This O3 serves as a shield against biologically harmful solar ultraviolet (UV) radiation, initiates key stratospheric chemical reactions, and transforms solar radiation into the mechanical energy of atmospheric winds and heat. Also, downwind intrusions of stratospheric air supply the troposphere with the 0 3 necessary to initiate photochemical processes in the lower atmosphere and the flux of photochemically active UV photons (wavelength, 2 < 315nm) into the troposphere is limited by the amount of stratospheric O 3 (Cicerone, 1987). Ozone concentrations vary with altitude above the earth's surface; peak fractions of about 10-s by volume are found between 25 and 35 km. The vertical column of 0 3 is distributed roughly as follows: 0-10km (troposphere), 10%; 10-35km, 80%; and above 35km, 10% (Cicerone, 1987). Ever since the publications of Johnston (1971) and Molina & Rowland (1974) human activities have been projected to substantially deplete the stratospheric O 3 through anthropogenic increases in the global concentrations of key atmospheric chemicals. Cicerone (1987) has provided an excellent treatment of this question. Of concern is the flow into the

1i 2

Sagar 11".Krupa, William J. Manning

stratosphere of CH4, nitrous oxide (N20), methyl chloride (CH3C1), synthetic chlorofluoro carbons (CFCs), chlorocarbons (CCs) and organobromine (OB) compounds. Many possible stimuli have been proposed for the destruction of stratospheric O3: NO X from nuclear explosions, hypothetical fleet of supersonic aircraft, solar proton events, increased atmospheric N 2 0 and chlorine from the continued use of CFCs and CCs, volcanoes, and space shuttle rocket exhaust. Also increases in atmospheric CH4 can lead to changes in the O3 layer through interactions with NO x and C1Ox cycles and through production of H O r Of all these possibilities, the most definitive experiment to date concerns solar proton events. Observations that followed the large event of August 1972 showed that O 3 concentrations were reduced by about as much as theory predicted, at least in the upper stratosphere (Heath et al., 1977). Figure 4 (Cicerone, 1987) shows examples of large scale processes that produce and transfer source gases, which undergo irreversible photooxidation to yield important gaseous radicals, to the stratosphere. The N 2 0 from soil and oceanic microbial activity enters the lower atmosphere and, through large scale motions (principally in the tropics), is transported upward to the stratosphere. Subsequently, most N 2 0 is decomposed through: N 2 0 + hv-oN2 + O (1D)

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(2)

Similarly, the synthetic CC12F 2 and CClaF are swept upward into the middle stratosphere, where UV photolysis dissociates them to yield chlorine atoms. As with N 2 0 , there are no known tropospheric sinks for CC12F 2 and CClaF, so that nearly 100% of the molecules released at the earth's surface reach the stratosphere. On the other hand, methane is not as inert in the atmosphere as N 2 0 and CFCs. Perhaps 85% to 90% of the CH4 released at the earth's surface is consumed in the troposphere. The remaining 10% to 15% reaches the stratosphere. Stratospheric oxidation of CH4 gives rise to water vapour and OH and HO 2 radicals. The upper boxes in Fig. 4 show some of the important reactions that control stratospheric O 3 concentrations. Attempts to predict the future effects of continued increases in stratospheric source gases (e.g. CFCs) have given rise to various mathematical models. Simulated CFC releases lead to O3 column decreases at all latitudes (Isaksen & Stordal, 1986). Larger decreases in the O a column were calculated for high latitudes (> 40 °) than for low latitudes.

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No clear trend in the total column of stratospheric 0 3 has been reported to date except for over Antarctica (refer to Atmospheric Ozone, 1985, World Meteorological Organization, Geneva, Switzerland). There does not appear to be an accepted explanation for the large decreases in 0 3 reported over Antarctica. Reduced amounts of atmospheric 03 permit disproportionately large amounts of UV radiation to penetrate through the atmosphere. For example, with overhead sun and typical 0 3 amounts, a 10% decrease in 0 3 will result in a 20% increase in UV penetration at 305 nm, a 250% increase at 290nm, and 500% increase in 287nm (Cutchis, 1974). It should also be noted that decreases in the total 03 column due to decreases in stratospheric 0 3 may partially be compensated by increases in tropospheric 0 3. Logan (1985) estimated that approximately 20-30% of the decrease in stratospheric 0 3 over middle and high latitudes of the northern hemisphere could be compensated for by what appears to be a trend toward increasing 0 3 in the troposphere in these geographic areas. The consequences of such a trend must be considered in the context of vegetation effects.

O Z O N E E F F E C T S ON V E G E T A T I O N By 1944, new types of foliar injury were noticed on vegetation in the Los Angeles area. Middleton et al. (1950) reported that this injury was caused by smog or air pollution. Weather fleck of cigar-wrapper tobacco was reported in Connecticut as a disease of unknown cause in 1952 (Rich et al., 1969). Ozone (03) was shown to be the cause of grape leaf stipple in 1958 (Richards et al., 1958) and weather fleck of tobacco in 1959 (Heggestad & Middleton, 1959). Activated charcoal filters were first used to protect plants in Los Angeles in 1961 (Darley & Middleton, 1961) and to prevent 0 3 fleck and premature senescence of tobacco leaves in 1966 (Menser et al., 1966). While investigating weather fleck, it was observed that there was considerable variation in cigar-wrapper tobacco cultivar responses to 03. One commonly grown cultivar (C) was so sensitive to 03 that it became obsolete and could no longer be grown commercially in the Connecticut Valley. Cultivar B, however, was quite tolerant to 03. A new super-sensitive strain (Bel-W3) was selected from the sensitive cultivar CCC-W3 (Heggestad & Menser, 1962). Bel-W3 tobacco has since become the world's most commonly used bioindicator for ambient 0 3 (Manning & Feder, 1980). Since those early investigations with tobacco, it has become evident that 03 is the most important phytotoxic air pollutant in the United States. Increasing numbers of reports of 03 injury on sensitive or indicator plants

Atmospheric ozone: formation and effects on vegetation

115

from countries such as Australia, Canada, Japan, India, Israel, Mexico, the Netherlands, the United Kingdom and West Germany indicate that O3 is also of increasing concern on a world-wide scale, especially in relation to the possible role of 03 in forest decline problems (Krause et al., 1983; Ashmore et al., 1985; deBauer et al., 1985; Prinz, 1987; Krause, 1988). During the last 30 years, hundreds of reports have been published on the effects of 0 3 on vegetation (National Academy of Sciences, 1977; Laurence & Weinstein, 1981; Jacobson, 1982; Taylor, 1984; Heggestad & Bennett, 1984; Guderian, 1985; Prinz & Brandt, 1985; Legge & Krupa, 1986; Prinz, 1987; Heck, et al., 1988). Our purpose here is to provide an overview of plant responses to 03, with an emphasis on effects on yields.

P R I M A R Y EFFECTS OF OZONE

Symptoms of ozone injury enters plant leaves via open stomates during the normal process of gas exchange between a leaf and its normal environment (Rich et al., 1970). Once inside the leaf 0 3, or some intermediate like an OH radical, changes the integrity of cells, probably due to changes in membrane permeabilities (Fong, in: Lee, 1985). If cells collapse and die, then symptoms occur on leaf surfaces. For broad-leaved plants with palisade mesophyll cells (Fig. 5), symptoms will appear first on upper leaf surfaces, as palisade cells are 0 3

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116

Sagar V. Krupa, William J. Manning TABLE 4

Common Symptoms of Foliar Ozone Injury Acute injury

Chronic injury

Flecking: small necrotic areas due to death of palisade cells, metallic or brown, fading to tan, grey or white Stippling: tiny punctate spots where a few palisade cells are dead or injured, may be white, black, red or red-purple

Pigmentation (bronzing): leaves turn red-brown to brown as phenolic pigments accumulate Chlorosis: may result from pigmentation or may occur alone as chlorophyll breaks down Premature senescence: early loss of leaves or fruit

especially susceptible to 0 3. Conifers, and plants with undifferentiated mesophyll cells, can have symptoms on either leaf surface as only cells near stomata are affected by 03 (Lacasse & Treshow, 1976). On m a n y plants, 0 3 injury is confined to the tips of younger leaves, becoming more extensive as the leaf matures. Leaves that are still expanding, or have just achieved full size, are the most susceptible to 03 (Lacasse & Treshow, 1976). Depending on the type and variety of plant, the concentration and duration of 03 exposure, and other interacting factors, 03 can cause a wide array o f symptoms on plants. Examples of c o m m o n 03 injury symptoms for broad-leaved plants are summarised in Table 4. Conifers may exhibit r e d - b r o w n tipburn of current season's needles or chlorotic mottle of older needles. Examples of s y m p t o m expression for sensitive crop plants and deciduous and coniferous trees are given in Tables 5, 6 and 7. Symptom TABLE 5

Crop Plants Commonly Affected by Ozone and Typical Symptoms Expressed Plant

Bean (Phaseolus) Cucumber (Cucumis) Grape (Vitis) Morning glory (lpomoea) Onion (Allium) Potato (Solanum) Soybean (Glycine) Spinach (Spinacea) Tobacco (Nicotiana) Watermelon (Citrullus)

Foliar symptoms

Bronzing and chlorosis White stipple Red to black stipple Chlorosis White flecks and tip dieback Grey fleck and chlorosis Red-bronzing and chlorosis Grey to white fleck Metallic to white fleck Grey fleck

Atmospheric ozone: formation and effects on vegetation

117

TABLE 6

Deciduous Trees Commonly Affected by Ozone and Typical Symptoms Expressed

Tree

Foliar symptoms

Black cherry (Prunus serotina)

Red-black stipple, reddening and leaf chlorosis, premature defoliation Red-purple stipple and bronzing

Green ash (Fraxinus pennsylvatica var. lanceolata) Quaking aspen (Populus tremuloides)

Black stipple, chlorosis, premature defoliation Chlorosis, early senescence and defoliation Dark stipple

Sycamore (Platanus occidentalis) Tulip poplar (Liriodendron

tulipifera

expression for 03 injury for many plants has been extensively reviewed (Heggestad & Heck, 1971; Hill et al., 1961, 1970; Lacasse & Treshow, 1976; Manning & Feder, 1980; Taylor, 1984). 03 may cause acute injury, chronic injury, or it may affect growth and yield, with or without visual symptoms. Acute injury involves cell death and occurs on plants exposed to high concentrations of O 3 for a short time period. Chronic injury results from long-term exposure of plants to low concentrations o f O 3 (Table 4). In nature, both types of symptoms may occur on the same plant, but at different times in the life cycle, due to the fluctuating nature of ambient concentrations of O a.

Factors affecting ozone injury Growing plants are exposed to many interacting biotic and abiotic factors that affect their performance and success and responses to 0 3. Some of these TABLE 7

Conifers Commonly Affected by Ozone and Typical Symptoms Expressed

Tree Eastern white pine (Pinus strobus)

Jeffrey pine (Pinus jeffreyii) Ponderosa pine (Pinus ponderosa)

White fir (Abies concolor)

Foliar symptoms Chlorotic fleck or mottle on older needles, Red-brown tipburn of current needles Chlorotic mottle of older needles Chiorotic fleck or mottle on older needles, followed by needle dieback from tips Chlorotic mottle on older needles

118

Sagar V. Krupa, WiOiamJ. Manning FACTORS INFLUENCING PLANT RESPONSE TO OZONE

BIOTIC FACTORS

PHYSIOLOGICAL FACTORS

PATHOGENS TEMPERATURE HUMIDITY CARBON DIOXIDE (COa) WIND SPEED RADIATION (LIGHT)

INSECTS

INSECTS PATHOGENS MYCORRHIZAE NEMATODES N2-FIXATION COMPETITION WITH PLANTS

TEMPERATURE MOISTURE NUTRITION 02-C02 TENSIONS COMPACTION (SOIL) TYPE (SOIL)

Fig. 6. Factors influencingplant response to ozone. are summarised in Fig. 6. In addition, genetic variability within and between species and cultivars greatly affects plant responses to O3. This is well-known for plants like alfalfa, bean, cotton, petunia, potato, soybean, tobacco, and tomato (Rich & Hawkins, 1970; Heggestad, 1973; Lacasse & Treshow, 1976; de Vos et al., 1982). Warm temperatures, sunlight, high relative humidity, good nutrition, adequate soil moisture and other factors are necessary for O3 injury to occur (Heck, 1968; Heggestad & Heck, 1971; Heggestad et al., 1985, 1988; Lacasse & Treshow, 1976; Tingey et al., 1982). Sensitive plants that are not suffering from other stresses are usually injured by O 3. Runeckles & Palmer (1987) have recently reported that plant growth inhibition by O 3 is significantly increased by prior plant exposure to nitrogen dioxide (NO2). Mehlhorn & Wellburn (1987) demonstrated that stress ethylene increased visible O 3 injury in peas. N O 2 also enhanced O3 injury by increasing stress ethylene production. Dose-response relationships In determining the effects of 0 3 o n plants, attempts have been made to quantitate the magnitude of plant responses to known concentrations of 03

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over fixed periods of time, under defined environmental conditions. The amount ofO 3 available during the response period is often termed the 'dose'. It can be expressed either as 0 3 concentration times duration of exposure or as an average 0 3 concentration times duration of exposure (Menser & Hodges, 1968; Krupa & Kickert, 1987). A more useful concept for air pollution researchers, however, is the concept of threshold dose. This is the lowest 03 dose that will produce a measurable effect. Bel-W3 tobacco, for example, will show visible 03 injury if exposed to 0.05 ppm 03 for 3 h (Menser et al., 1966). Sensitive clones of Eastern white pine will be injured by 03 at 0.07 ppm for 4 h (Costonis & Sinclair, 1969). Ponderosa pine needles can be injured by 03 at 0.05-0.06 ppm for 24 h (Miller, 1983). It has been demonstrated that plants usually have different thresholds for foliar 03 injury and yield losses (Jacobson, 1982). Heagle et al. (1979a) found that concentrations of 03 that caused foliar injury on field corn hybrids were different than thresholds required for yield losses. Reich & Amundson (1985) reported yield losses and growth reductions in the absence of foliar symptoms. Using dose/responses, Reich (1987) has developed a conceptual model to explain differences in different types of plant responses to ambient 03 . Using this model, which involves relation of plant responses to an equivalent 03 dose during one growing season, he concludes that herbaceous crop plants are the most sensitive to 03 , deciduous trees are intermediate and conifers the least sensitive.

Biomonitoring ozone with plants Certain plants that respond to 03 in predictable and reliable ways can be used to biologically determine that 03 is present in ambient air. These plants indicate that 03 is present at concentrations that will cause injury. If there is good dose/response data available, then bioindicator plants can also be used to biomonitor 03. Bel-W3 tobacco is the most frequently used plant to detect 03 in ambient air. There is a positive correlation between degree of leaf injury and ambient 03. Comparison of injury severity on Bel-W3 and BeI-B plants can provide a measure of air quality (Manning & Feder, 1980). Other plants that can be used as 03 bioindicators are listed in Table 8.

Ozone effects on plant growth and yields After it was established that O3 could cause a wide array of symptoms on many plants, the next logical question was whether O a had any effects on

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growth and yields of crops and forest trees. This prompted many investigations and the development of several different methods to determine growth and yield effects (Laurence & Weinstein, 1981; Heck et al., 1982, 1984a,b; Jacobson, 1982; Heggestad & Bennett, 1984; Taylor, 1984; Lee, 1985; Prinz, 1987; Krupa & Kickert, 1987; Manning, 1988). Answering the key question of whether or not 0 3 significantly affects plant growth and yield has proven extraordinarily difficult. This is due to the TABLE 8

Plants That Can be Used as Bioindicators or Biomonitors of Ambient Ozone Common name

Latin name

Bean Grape

Phaseolus vulgaris Vitis labrusca

Spinach Tobacco

Spinacea oleracea Nieotiana tabaeum

White pine

Pinus strobus

Useful cultivars

Pinto 111, Tempo Ives (sensitive) VanBuren (tolerant) Most are sensitive BeI-B (tolerant) Bel-W3 (sensitive) Grafted sensitive and tolerant trees

Adapted from: Manning & Feder (1980).

nature of the pollutant and its distribution in ambient air. During the growing season, 0 3 is an all-pervasive pollutant, making it difficult to exclude it and still have conditions that are relevant to those that occur in nature. Side-by-side comparisons of the effects of ambient 03 on plants are impossible, unless some way can be devised to exclude 03 from the control treatment. Development of a universally accepted method of accomplishing this, under normal conditions, has not been accomplished. This means that all experimental determinations of the effects of ambient 03 on plant growth and yield must be qualified by the inherent limitation of whatever method was used to achieve them. Plants also respond differently to 03 at different stages of their life cycles. Since ambient 0 3 concentrations fluctuate, as do other environmental conditions, there will be periods when less sensitive growth stages will be exposed to potentially damaging concentrations of 03, with little adverse effects or there will be periods when 03 concentrations will be too low for plants to respond or periods when environmental conditions prevent or reduce 0 3 uptake by plants. During these periods, compensatory growth may occur which may reduce or eliminate 0 3 effects on yields. These factors are seldom considered when experiments are designed to determine the effects of 0 3 on plant yields under ambient conditions.

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Methods for studying ozone effects on plant growth and yields The methods used to study 0 3 effects on plants range from controlled environments to field exposure systems to field plots in ambient air. These are summarised in Table 9, and reviewed elsewhere (Heagle & Philbeck, 1979; Heagle e t al., 1979b; and Krupa, in: Lee, 1985). They will be discussed below and examples of results will be given for some of the methods.

Controlled environments Environment variables that affect 0 3 uptake and plant sensitivity are most easily manipulated in modified greenhouses, growth chambers or experimental chambers, used in greenhouses or growth chambers. The individual

TABLE 9 Summary of Methods Used to Determine the Effects of Ozone on Plants Methods

References

Controlled environments

Modified greenhouses Modified growth chambers Experimental chambers (used in greenhouses or growth chambers) rectangular chambers round chambers e.g. Continuous Stirred Tank Rectors (CSTRs)

Darley & Middleton (1961) Menser et al. (1966) Wood et al. (1973)

Heagle & Philbeck (1979) Heck et al. (1978)

Field exposure systems

Open-air chamberless systems Linear gradient systems Zonal air pollution systems (ZAPS) Field chamber systems closed chambers, greenhouses open-top chambers, up-draft chambers down-draft chambers

Laurence et al. (1982) Lee & Lewis (1978) Thompson & Taylor (1969) Heagle et al. (1973, 1979b), Lee (1985) Runeckles et al. (1978)

Field plots in ambient air

Natural ozone concentration gradients Cultivar comparisons Protective chemicals Long-term growth reduction measurements

Oshima et aL (1976) Heggestad (1973), Manning, et al. (1974), Rich & Hawkins (1970) Carnahan et al. (1978) Manning et al. (1974) Miller (1983), Peterson et aL (1987), Skelly et al. (1983)

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effects o f O 3 are determined here with greatest precision, but results obtained are usually relevant only to the conditions of the experiment. Extrapolation of data to ambient conditions may not be possible. Darley & Middleton (1961) used activated charcoal filters on greenhouses to protect floricultural crops from air pollution injury in Los Angeles. Menser et al. (1966) used charcoal filters to prevent 0 3 fleck on BeI-W3 tobacco in Beltsville. Heggestad (1973) grew 12 potato cultivars in charcoalfiltered and non-filtered air in greenhouses in Beltsville and determined yield differences (Table 10). The cultivars most affected by 0 3 had all been developed in parts of the country where 0 3 concentrations are normally quite low. More recently, Endress & Grunwald (1985) investigated the long-term effects of low concentrations of 0 3 on greenhouse-grown soybeans. Concentrations of 0-07 and 0.097 p p m 0 3 decreased plant growth and yields. An 03 concentration of 0-046 ppm, however, resulted in an increase in yield. Commercially available growth chambers can also be modified and used as 0 3 fumigation chambers. W o o d et al. (1973) were among the first to successfully develop this method. Experimental chambers of various kinds are placed as units either in modified greenhouses or growth chambers. Pass-through, non-recirculating TABLE 10

Yields of Potato Cultivars Grown in Charcoal-filtered or Non-filtered Air in Greenhouses, Beltsville, MD, 1971 Cultivars

Yields (g)

100 CF

NF ×

Charcoal-filtered (CF)

Non-filtered (NF)

218 251 282 251 318 369 273 466 380 410 295 401

279 269 287 252 304 339 218 346 276 272 187 199

Katahdin Penn 71 Pungo Norgold Russett Superior Kennebec Wauseon Norchip La Chipper Alamo Haig Norland

LSD, 0'05 = 71 g for cultivars within an air regime, 81 g between air regimes. Adapted from: Heggestad (1973).

128 107 102 100 96 92 80 74 73 66 63 50

Atmospheric ozone: formation and effects on vegetation

123

air flow systems are preferred. Rectangular chambers may have regions where 03 concentrations are not uniform (Heagle & Philbeck, 1979). Heck et aL (1978), developed cylindrical continuous stirred tank reactors (CSTRs). Continuous uniform air mixing in the cylindrical chambers is provided by an impeller in the top and baffles along the sides. There are no 'dead spots' as might be found in the corners of rectangular chambers. CSTRs are widely used, particularly in studying the effects of 0 3 on physiological and biochemical processes. Field exposure systems Controlled environment facilities are often small in size and are good for relatively short-term experiments with small numbers of plants. Field exposure systems have been developed to determine the effects of ambient 03 on large numbers of plants under field conditions. In an effort to develop as natural a system as possible, zonal air pollution systems (ZAPS) and linear gradient systems have been developed (Lee & Lewis, 1978; Laurence et al., 1982). A network of perforated pipes is placed in the field among growing plants. 03 at a high concentration is introduced at one end of the pipes and either allowed to diffuse down the pipes or is driven along with a blower. Concentration gradients form along the pipes and the effects of 0 3 at different concentrations can be determined. Control plots are not possible and changes in wind turbulence can affect 03 concentrations. Early versions of field exposure chambers consisted of placing small closed carbon-filtered or non-filtered greenhouses over trees or crops in the field. T h o m p s o n & Taylor (1969) placed chambers with closed tops over 16year-old citrus trees in California. Ambient air reduced orange and lemon yields up to 50%, due to premature leaf and fruit drop. Results from these closed chambers are strongly affected by chamber conditions and do not relate well to ambient conditions. Heagle et al. (1973) and others developed a standardised large cylindrical open-top plastic-covered field chamber. Incoming air is either charcoalfiltered or not or may be amended with any concentration of 0 3. Incoming air inflates the double wall of the lower half of the chamber and moves outward through perforations all around the inner wall, moving under and over the plants inside and then upward and out of the chamber. The use of directional baffles or truncated cones or collars of various diameters helps to reduce down-draft intrusion of ambient air (Krupa, In: Lee, 1985). This updraft, open-top chamber is the most widely used device for studying 03 effects on plants in the field. Runeckles et al. (1978), however, recognised that plants are usually exposed to 03 when ambient air sweeps over the top of

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Sagar V. Krupa, William J. Manning

them, rather than from underneath them, and developed the down-draft chamber as an alternative system. The environment in an open-top chamber can be different than that in open ambient air. Air flow and 0 3 concentrations are usually constant and may be more or less than normal. Changes can occur in light, humidity and soil moisture levels. Absence of dew formatiofl may prevent normal incidence of foliar diseases. Insects are usually excluded from open-top chambers. Because of these possible chamber effects, non-chamber, open-air ambient plots are usually included for the sake of comparisons (Heagle et al., 1979b; Krupa, in Lee, 1985). The world's largest air pollution research programme on vegetation effects was begun in 1980, when the National Crop Loss Assessment Network N C L A N was established by the US Department of Agriculture and the US Environmental Protection Agency. The primary purpose of N C L A N was to assess the effects o f O 3 on yields of economically important crop species and to use the information to make predictive models and to aid in establishing national air quality standards (Heck et al., 1982, 1984a,b). Large numbers of open-top chambers were set up at sites in Raleigh, NC, Beltsville, MD, Argonne, IL, Ithaca, NY, and Shafter and Tracey, CA. Crops such as soybeans, wheat, field corn, tobacco and snapbeans were exposed to carbon-filtered air, using 0.025 p p m 03 as the estimate of 03 in the CF chambers. This concentration also corresponds to an estimate of natural background Oa concentrations. In addition, 4 to 6 03 treatments were established by adding 03 in constant or proportional amounts to ambient air O3 concentrations for 7 h per day (10:00 to 17:00 h). Ambient air chamber-less plots were used for comparisons. O 3 monitoring data are summarised and presented as a seasonal mean of the daily 7 h mean 0 3 treatment (Heck et al., 1984a,b). By adding O3 at 4 to 6 concentrations, it was possible to establish 0 3 concentrations higher than those found in ambient air in the particular field plot area. The purpose of this was to develop dose-response data for major crop plants and seasonal mean O 3 data. Use of this data with the Weibull model allowed the development of models for prediction of yield losses due to O3 (Heck et al., 1984b). Many publications have emerged from the N C L A N programme. A recent example is a paper on the effects of O3 on yields of winter wheat in Ithaca, NY (Kohut et al., 1987) (Table 11). When compared to filtered air, every treatment resulted in a loss in terms of seed weight and 100-seed weight. A m u n d s o n et al. (1987) reported that O3-caused yield reductions in winter wheat, 'Vona' were caused by reductions in net photosynthesis. Reductions in field corn yields were determined by Kress & Miller (1985). There are many other papers that relate to N C L A N studies.

Atmospheric ozone: formation and effects on vegetation

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T A B L E 11 Effects o f O z o n e o n Yields of V o n a W i n t e r W h e a t in O p e n - t o p C h a m b e r s , Ithaca, N Y

Treatments

Filtered air A m b i e n t air Non-filtered Non-filtered Non-filtered Non-filtered

air +0'03 ppm 0 3 + 0'06 p p m 0 3 + 0"09 p p m 0 3

Seed weight

lO0-seed weight

kg ha- 1

% loss

weight (g)

% loss

5 331"0 4 049-8 3 552-1 2 322'3 1 698'8 1 430"0

-24 33 56 68 73

3"26 2'32 2'47 1'77 1.41 1.30

-29 24 46 57 69

AdaptedJrom: K o h u t et al. (1987).

The NCLAN programme has been very successful and productive. Models for prediction of O3-caused losses for major crops have been developed. The results and the models, however, have been criticised and they are not universally accepted. The open-top chamber regimes used to generate the data base for NCLAN do not account for the episodicity ofO3 in ambient air and for the effects that changes in other environmental factors would have on yields. Heggestad et al. (1985) have shown that soil moisture stress and 0 3 have effects on soybean yields and soybean shoots and roots (Heggestad et al., 1988). Krupa & Kickert (1987) point out that long-term averaging of air pollutants, such as 03, create artefacts due to the non-normal distribution of ambient 03 concentrations. The use of constant concentrations of 0 3 may not be the best exposure regime. Musselman et al. (1983) showed that bean plants exposed to constant concentrations of 03 showed the same types of response to O3 as did plants exposed to variable 0 3 concentrations, at equivalent doses. The effect of variable concentrations of 03 on beans, however, was greater than that caused by constant concentrations of 03. This problem could be avoided in the N C L A N programme by the use of a programmable computer-based 0 3 exposure control system, using experimentally developed fluctuating 03 regimes (Hogsett et al., 1985). Heagle et al. (1987) report that the 7-h day used by N C L A N may be missing the effects of late afternoon 03 on yields. Tobacco exposed to proportional 0 3 additions for 12 h per day (10:00 to 22:00) yielded 10% less (three treatment levels combined) than those exposed for only 7 h per day (10:00 to 17:00). Using the protectant chemical EDU, Smith et al. (1987) determined that ambient O 3 in open field plots in New Jersey had no effects on yields of

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Sagar V. Krupa, William J. Manning

Williams and Cutler soybeans over a three-year period. Their 7-h seasonal mean for one year, however, was 0-062 ppm 03. If the predictive NCLAN model for soybeans was used, this mean 03 concentration should have resulted in a yield loss (Heck et al., 1984b). Field plots in ambient air Open-air field plots, with no interfering chambers or apparatus, are the best place to investigate the effects of ambient 03 on plant growth and yields. It would be ideal to compare the growth and yield of plants in an area with high 03 concentrations with that of those in a nearby area with low O a concentrations. Given the all pervasive nature of ambient 03, however, this is usually impossible to accomplish. Due to specific geographic features and air flow patterns, there is a wellknown natural 0 3 concentration gradient in the Los Angeles Basin. 03 concentrations near the ocean are low and much higher in the adjacent mountains above the area. Oshima et al. (1976) placed alfalfa plants, in containers ofa standardised soil mix, at sites along the 0 3 gradients between the ocean and the mountains. Using regression analysis, they calculated that alfalfa yields were reduced by 53% when results from the mountains and the ocean were compared. A similar situation has been described where 03 injury on pines increases with altitude around Mexico City (de Bauer et al., 1985). Where plant materials are carefully defined, growth and yield responses can be compared when closely related cultivars, differing in sensitivity to 03, are grown in the same location. This can be done with potatoes, tobacco, beans, and grafted or selected white pine clones (Rich & Hawkins, 1970; Manning et al., 1974; Manning & Feder, 1980). It has been known for many years that a number of chemicals will suppress 03 injury to one degree or another if they are applied to plants before they are exposed to 03. This approach is very simple and shows great promise. It has received much criticism, however, because it is claimed that the chemicals themselves may affect plant growth and yield and that realistic analysis of different 03 exposure regimes under uniform conditions is not possible (Heagle et al., 1979b; Krupa, in Lee, 1985). Manning et al. (1974) demonstrated that foliar spray applications of the fungicide benomyl (methyl 1-(butylcarbamoyl)-2-benzimidazole-carbamate) reduced 03 injury and increased yields for an O3-sensitive snapbean but had no effects on performance of an O3-tolerant cultivar (Table 12). Foliar sprays or drenches of E D U (ethylenediurea) (N-[2-oxo-1imidazolidinyl)ethyl]-Nl-phenylurea) prevented or decreased 03 injury on bean plants and was more effective than benomyl (Carnahan et al., 1978).

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Atmospheric ozone: formation and effects on vegetation

TABLE 12 Influence of Benomyl Foliar Sprays on Yield of the Ozone-sensitive Snapbean Cultivar 'Tempo' and the Ozone-tolerant Cultivar 'Slender White', in the Field at Waltham, Massachusetts Cultivars and treatments

Average yields by weeks a 3

4

5

Average total yields

1

2

77.3 91.0

213'2" 151.7"

504-3 417.3

326.3 234.0

180.6 226"0

712.3" 433"0*

1 589-7 1 457'2

1 225'1 831"8

1 035"8* 411-0"

96.8 115.0

335'7 330'0

264.7 249.7

373.5 330-7

181.5 116.3

1 252.2 1 141.7

354"3 428-3

1 166"0 1 529'5

1 011'6 977"6

1 700'0 1 435'1

647"6 465"1

4879"5 4835"6

Tempo a

Number of pods: sprayed b

non-sprayed

226'8** 127.3"*

1 347'9** 1 021-3"*

Wt of pods (g):

sprayed non-sprayed

4 743.5** 3 359"0**

Slender White c

Number of pods: sprayed

non-sprayed Wt. of pods (g): sprayed

non-sprayed

a First harvest made 54 days after planting. b Weekly foliar sprays of benomyl at 2-4 glitre 1 c First harvest made 61 days after planting. a Average per four replications, twenty plants each. * Significantly different values (P = 0.05). ** Significantly different values ( P = 0.01). From: Manning et al. (1974).

Clarke et al. (1983) used E D U in the field to determine the extent of foliar 0 3 injury on three potato cultivars and yield losses. Reductions in tomato yields (Table 13) were demonstrated when plants were treated with E D U in Ontario (Legassicke & Ormrod, 1981). Smith et al. (1987) were unable to use E D U to demonstrate yield losses for soybeans due to ambient 0 3. Chemical protectants require several applications, usually at two-week intervals. Plants must be protected during stages when they are most sensitive to 0 3. For many plants, those stages and concentrations of chemicals needed for protection would have to be determined experimentally in advance. Trees have both primary and secondary growth and long-term growth reductions can be determined by means of physical measurements and interpretation of tree rings from cores taken from tree trunks. These results represent long-term growth trends and suggest changes that may be due to Oa and other factors.

Sagar V. Krupa, William J. Manning

128

T A B L E 13 Examples o f the Effects of E D U Applications o n Yield o f Ozone-sensitive 'Tiny Tim' T o m a t o e s in the Field at Harrow, O n t a r i o

EDU treatment

Number of fruit per plant

Control 1.0 g litre- 1, foliar spray 0"5 g per plant soil drench

317 a* 413 b 369 a'b

Avg. fruit wt (g)

% ripe fruit

5"85 a 5'89 a 6.26 a

67 a 67 a

61 a'h

Yield per plant (g) 1 856 ~ 2 431 b 2 312 ~'b

* M e a n separation by D u n c a n ' s multiple range test, P = 0.05.

Adapted from: Legassicke & O r m r o d (1981).

The classic example of long-term growth reduction analysis of a forest ecosystem is the San Bernadino mountain forests east of Los Angeles. Ponderosa and Jeffrey pines are weakened by 03, foliar injury causing premature needle drop, resulting in reduced radial growth of branches and trunks (Miller, 1983). This same unfortunate pattern has recently been reported for Jeffrey pines in Sequoia and King's Canyon national parks, north of Los Angeles, and east of San Francisco (Peterson et al., 1987). Decline of growth of Eastern white pines in the Blue Ridge mountains of Virginia has also been documented by Skelly et al. (1983). European investigators are beginning to suspect that 03 may affect the growth of spruce, fir and beech. 03 may be weakening trees, reducing their radial growth and making them more susceptible to other stress factors, resulting in widespread forest decline ('Neuartige Waldschaden') (Ashmore et al., 1985; Krause et al., 1983; Krause, 1988). Ozone effects on yield quality

A great deal of attention has been paid to determining the effects of 0 3 o n the quantity or size of plant yields. Considerably less is known about 03 effects on the quality of plant yields. Most of the information that is available relates to changes in quality or mineral content of potatoes and leguminous plants, most of which are used for forage (Blum et al., 1981; Skarby, 1984; Tingey et al., 1986). There is a great need for information on 03 effects on the quality as well as the quantity of plant yields.

SECONDARY EFFECTS OF OZONE In addition to causing visible symptoms on leaves and reducing the growth and yield of plants, 03 can have other secondary effects, which may be many,

Atmospheric ozone:formation and effects on vegetation

129

subtle and interactive. If these are not considered when assessing 0 3 effects on plant yields, then misleading or incomplete results will be obtained. Long-term exposure to low concentrations of 0 3 affects photosynthesis and results in reduced translocation of photosynthate from shoots to roots (Cooley & Manning, 1987). This may adversely affect mycorrhizae (Keana & Manning, 1987), and enhance root senescence (Manning et al., 1971), which will affect yields due to reduced uptake of water and minerals. Insects and pathogens associated with plants are known to be affected by 0 3. Sometimes the effect on the insect or pathogen is a direct and obvious one, but usually it is an indirect one that is expressed through a change in the physical or chemical nature of the plant. Additional information is provided in the following reviews: Alstad et al. (1982); Hughes (1988); Hughes & Laurence (1984); Huttunen (1984); Manning & Keane (1988). Effects on insects

affect the nutritional status of host plants for insects or change their morphology, making them more or less palatable or suitable as habitats and sites of reproduction (Hughes, 1988). Chappelka et al. (1987) reported that Mexican bean beetles preferred to feed on ozonated soybean foliage, even though they are only marginally adopted to feeding on soybean leaves. Larvae appeared to prosper when fed ozonated foliage. Tomato pinworms developed faster and survived longer on tomato plants injured by 0 3 (Trumble et al., 1987). O3-weakened pines in California, Virginia and Mexico become more susceptible to invasion by bark beetles (deBauer, et al., 1985; Miller, 1983; Skelly et al., 1983). 0 3 can

Effects on pathogens

There are many more reports of O3-plant-pathogen interactions than there are O3-plant-insect interactions. It is well established that O3 can directly or indirectly affect the course of development of plant diseases and there are many reports in the literature. 03 generally increases the incidence of diseases caused by non-obligate fungi, particularly necrotrophic fungi, like Botrytis. Manning et al. (1969), demonstrated that infection of potato leaves was increased when they were injured by 0 3. Fehrman et al. (1986), found that perinoculative exposures to O3 generally increased incidence of cereal leaf pathogens, such as Ascochyta, Gerlachia, and Drechslera. 0 3 generally decreases the incidence of diseases caused by obligate fungi, such as rusts and powdery mildews (Heagle, 1975). Dohmen (1987), has recently shown that preinoculative exposures of young wheat plants to 0 3 reduced the effectiveness of inoculum of brown rust.

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Sagar V. Krupa, William J. Manning

03-weakened pines in California and Virginia may also become more susceptible to root rots caused by Heterobasidion annosum and Verticicladiella procera (Miller, 1983; Skelly et al., 1983).

CONCLUSIONS (1)

(2)

(3)

03 concentrations in the troposphere are increasing and becoming more pervasive. 0 3 is the most important phytotoxic air pollutant in the USA, and is becoming a major concern on a world-wide scale. There are several methods that can be used to demonstrate the effects of 0 3 on plant growth and yields. Results from N C L A N , however, may not truly reflect the real situation and caution should be exercised in interpreting results from the programme. Experiments need to be designed to investigate the long-term effects of O3-plant-insect and/or pathogen interactions in relation to crop yields.

REFERENCES Alstad, D. N., Edmunds, G. F., Jr & Weinstein, L. H. (1982). Effects of air pollutants on insect populations. Ann. Rev. Entomol., 27, 369-84. Altshuller, A. P. (1986). The role of nitrogen oxides in non-urban ozone formation in the planetary boundary layer over North America, Western Europe and adjacent areas of ocean. Atmos. Environ., 20, 245 68. Amundson, R. G., Kohut, R. J., Schoettle, A. W., Raba, R. M. & Reich, P. B. (1987). Correlative reductions in whole-plant photosynthesis and yield of winter wheat caused by ozone. Phytopathology, 77, 75-9. Ashmore, M., Bell, N. & Rutter, J. (1985). The role of ozone in forest damage in West Germany, Ambio, 14, 81-7. Blum, U., Smith, G. R. & Fites, R. C. (1981). Effects of multiple 03 exposures on carbohydrate and mineral contents of ladino clover. Environ. and Exptl. Botany, 22, 143-54. Carnahan, J. E., Jenner, E. L. & Wats, E. K. W. (1978). Prevention of ozone injury to plants by a new protectant chemical. Phytopathology, 68, 1225-9. Chappelka, A. H., Kraemer, M. E., Mebrahtu, T., Rangappa, M. & Benepal, P. S. (1987). Effects of ozone on soybean resistance to the Mexican bean beatle (Epilachna varivestis)i Environ. and Exptl. Botany. (In press.) Cicerone, R. J. (1987). Changes in stratospheric ozone. Science, 237, 3542. Clark, T. L. & Clarke, J. F. (1984). A Lagrangian study of the boundary layer transport of pollutants in the northeastern United States, Atmos. Environ., 18, 287-97. Clarke, B., Henninger, M. & Brennan, E. (1983). An assessment of potato losses caused by oxidant air pollution in New Jersey. Phytopathology, 73, 104-8.

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ADDENDUM Since this review was completed, the following paper was published: Altshuler, A. P. (1987). Estimation of natural background of ozone present at surface rural locations. J. Air Pollut. Control Assoc., 26, 1409-17.