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Impacts of Air Pollution on Agriculture in North America WALTER W. HECK Agricultural Research Service U.S. Department of Agriculture This chapter highlights our current understanding of the effects of anthropogenic air pollutants on agriculture in the United States and assesses their impact on crop productivity. Information from a cross section of crop-oriented review articles has been used to help define the problem (Altshuller and Linthurst, 1984; Dochinger and Seliga, 1976; Evans, 1984; Guderian, 1985; Heck 1984; Heck and Brandt, 1977; Heck et al., 1977, 1982a, 1982b, 1983a, 1984a, 1984b, 1984c, 1986; Irving, 1987; Jager and Klein, 1980; National Academy Sciences, 1977; Roberts, 1984; Shupe et al., 1983; Shriner et al., 1980; Reshow, 1984; Unsworth and Ormrod, 1982; U.S. EPA, 1978, 1982a, 1982b, 1986; and Winner et al., 1986~. Air pollution effects from point sources were first recognized in the early 1900s. Research was directed at recognizing injury symptoms and assessing losses in productivity in accordance with the severity of symptom development. Since that time, many chemicals have been identified as atmospheric contaminants that can injure or damage crops at some range of exposure concentration and time Able 1~. Sulfur dio~de (SO2) and fluoride (generally as hydrogen fluoride or HF) gases from point sources caused injury to vegetation around the turn of the century. Ducktown (Copper Hill), Tennessee in the United States, and SudbuIy, Ontario in Canada still show marked effects from SO2 releases from early smelter operations. Today, the installation of emission control systems and the use of high stacks has generally eliminated extensive injury to vegetation near sources of SO2. However, high-capacity power stations with tall stacks have increased the distribution of lower SO2 concentrations over larger areas. Thus, SO2 is now considered a regional problem, although direct effects on agricultural production are poorly defined. 171
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172 TABS F 1 Phytoto~cic air pollutants, in order of importance to crop systems.a ECOLOGICAL RISKS Primary or Pollutant Secondary Form Major Source(s) . . o so2 NO2 HF PAN-Oxid.C NO C12 HO Toxic elements NH3 SO4 NO3- H2S co2 UV-B! Secondary Primary Primary and secondary Primary Primary Secondary Primary Primary Primary Primary Primary Secondary Secondary Primary Primary Primary Gas (;as Gas Gas - particulate Gas Gas Gas Gas Gas Particulate Gas Aerosol Aerosol Gas Gas Radiation Atmospheric transformation (associated with automotive emissions, NO2, hydrocarbons) Power generation, smelter operations From direct release and atmospheric transformation ~igh-temperature com- bustion, from NO); fertilizer production Superphosphate, aluminium smelters Combustion, natural Atmospheric transformation (automotive emissions, NO2, hydrocarbons) Combustion, natural Spills, manufacture Buming of plastics Smelters, combustion processes Feedlots, natural Atmospheric transformation (SO2) Atmospheric transformation (;N02) Paper production, natural, geothermal Combustion, natural Natural, stratospheric O3 depletion a This list is not meant to be complete but represents the most unportant air pollutants with respect to terrestrial plant systems. Several of dose low on the list have been poorly studied and may be more important than currently thought. b Ethylene c Peroxyace~1 nitrate~xidant SOURCE: Heck, 1982. Fluoride (as HF) injury to vegetation was described by the turn of the century, but did not become a major problem until aluminum smelting and super-phosphate production increased in the 1940s. Fluoride symptoms are well characterized and a spectrum of sensitivities both between and within species is known. Foliar analysis is an acceptable diagnostic tool since fluo- ride accumulates in plant tissues. However, natural distribution of fluoride complicates the diagnosis. Shupe et al. (1983) present a comprehensive treatment of fluoride research. Photochemical air pollution injury was first described in the Los Ange- les area in 1944 and was evident over large segments of California by 1950. Components of photochemical oxidants (primarily ozone or 03) injure and damage crops in many areas of North America. Ozone, peroxyacetyl ni- trate (PAN), and nitrogen dioxide (NO2) are phytotoxic components of the photochemical complex. Ethylene is a major petrochemical and a by-product of combustion and of plant metabolism. It is a phytotoxic hydrocarbon gas and contributes
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HUMAN EFFECTS ON THE TE~ST~ E~RONME~ 173 to the formation of photochemical oxidants. Ethylene from anthropogenic sources probably contributes to crop losses. EFFECTS OF AIR POLLUTANTS OTlIER THAN OZONE ON AGRICULTURAL PRODUCTIVITY Many phytotoxic air pollutants have caused serious damage around point sources. Others are ubiquitous across the continent of North Amer- ica and are perceived as major problems. Fluoride is one of the most phytotoxic of the first group, while hydrogen chloride and hydrogen sulfide are less toxic. PAN is more phytotoxic than O3 and is widespread (in low concentrations) around metropolitan areas. Nitrogen dioxide has been studied principally in combination with O3 and SO2 because alone it is not particularly phytotoxic at current ambient concentrations. However, it is a primary actor in ozone formation. The air pollutants currently of greatest national concern are O3, SO2, NO2, and the transformed products of SO2 and NO2 (SO42- and NO3-) that are largely responsible for acidic precipitation. In North America, O3 has the greatest effect on agricultural productivity because it is found in damaging concentrations in most sections of the continent. Sulfur dioxide is released from point sources and may, over weeks or months, injure sensitive vegetation. Its primary impact may occur when it is associated with O3 or NO2. The importance of NO2 in terrestrial ecosystems is as an ingredient in photochemical reactions (forming 03) and when present in association with SO2 or O3. These three pollutants (03, SO2, and NO2) are critical components in the formation of acidic precipitation. Space does not permit a discussion of the many air pollutants that have damaged plants due to accidental releases or on a fairly local basis. However, a brief discussion of NO2, acidic deposition, and SO2 are included in this section. The importance of ozone is recognized and treated in a separate section along with assessment methods. Nitrogen Dioxide (NO2) Nitrogen dioxide can be used as a nitrogen source by plants. The first published study using ambient levels of i5NO2 (0.097, 0.152, or 0.325 ppm NO: for three hours) reported a linear relation between exposure concentration and uptake for snapbean; essentially all the nitrogen was metabolized (Rogers et al., 1979~. Although several studies have reported greater NO2 uptake at night, Yoneyama et al. (1979) found that night absorption was only about 14% of that absorbed during the day. Both nitrogen oxide (NO) and NO2, which are associated with the production of high levels of greenhouse CO2, substantially decreased growth
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174 ECOLOGICAL RISKS and productivity of greenhouse crops (Mansfield et al., 1982~. This raises serious concern for greenhouse operators who add CO2 in the greenhouse. Acidic Deposition The effects on crops of acidic precipitation (often incorrectly called "acid rain," but encompassing all forms of precipitation) was highlighted in the United States in an international symposium (Dochinger and Seliga, 1976~. Acidic deposition includes both wet and dry deposition of acidifying substances such as SO2 and NO2. Acidic precipitation is used to separate the transformed products (SO42- and NO3-) from gaseous SO2 and NO2; the term "acid rain" denotes only that specific form of acidic precipitation. Vegetation growing where acidic fogs or clouds are common may also be affected. The pollution control strategy of using tall stacks to reduce ground- level concentrations of sulfur and nitrogen oxides near fossil fuel combus- tion sources is a contributing factor to the long-range transport of acidic substances. The transformed products may be deposited hundreds of kilo- meters downwind in precipitation. Acidic precipitation may affect the growth, reproduction, quality, and/or yield of agricultural crops (Heck et al., 1984a). Direct effects include changes in leaf surface morphology, foliar nutrient leaching, up- take of additional sulfur or nitrogen, or changes in metabolic function or reproductive processes; with perennial plants, the effect may be cumulative across growing seasons. Indirect effects include altered physicochemical characteristics of soils (e.g., water-holding capacity), nutrient availability, availability of toxic elements, and susceptibility of plants to biotic and other stresses. Research efforts in the early 1980s developed around field studies utilizing rain exclusion systems to permit growth of plants under field conditions. Evans et al. (1986) reported significant acidic rain effects on 'Amsoy 71' over five consecutive growing periods; but no effects on other soybean cultivars were reported. DuBay and Heagle (1987) reported no effects on growth or yield from rain acidities as low as pH 2.7 (using similar field protocol) for the cultivar 'Forrest.' Banwart et al. (1987) found no effect on two field corn cultivars at present acidity levels, although a significant reduction in yield was found in one cultivar at a pH of 3.0. Fell et al. (1987) detected no effects on two potato cultivars at pH treatments as low as 2.8. Acidic precipitation may affect plant systems, but the evidence is lim- ited. It seems safe to suggest that we have not succeeded in developing an experimental approach that will permit the identification of small impacts.
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HUAf 4N EFFECTS ON THE TERRESTRIAL ENVIRONMENT 175 Likewise, the presence of increasing nitrogen and sulfur with decreasing pH (increasing H+) probably confounds experimental results. Sulfur Dioxide (SO2) Sulfur dioxide was extensively studied in the first half of the century (Heck and Brandt, 1977~. Interest was renewed by the increase in power generation and the subsequent increase in SO2 emissions. In addition, results of long-term assessments around point sources convinced scientists that earlier perceptions of SO2 thresholds needed to be reexamined. The effects of SO2 may be visible or subtle. Acute injury results in cell plasmolysis with foliar lesions, often bleached white; chlorosis may occur. Chronic injury may initially disrupt cellular activity, followed by chlorosis or other pigment changes that may lead to cell death. Chronic injury patterns are generally not characteristic of SO2 and may be confused with symptoms caused by diseases, insects. other stresses, as well as normal leaf senescence. The mechanism of crop response to SO2 has been studied in several ways. Sensitivity differences in four cultivars of cucumber were related to SO2 uptake (stomata! activity), but leaves of different sensitivity on the same plant involved a biochemical or developmental resistance mechanism related to the formation and loss of hydrogen sulfide (H2S) (Bressan et al., 1978; Sekiya et al., 1982~. Evidence for the photodetoxification of SO2 was associated with increased injury to plants on which stomata remained open during dark exposures to SO2; a strong case was presented for sulfite as the primary phytotoxicant for acute plant injury (Olszyk and Tingey, 1984~. Plant physiological and biochemical processes are probably more important controllers of plant resistance to SO2 (tolerance) than is control of gas entry via the stomata (avoidance). Many biological and physical factors affect the response of plants to SO2, including genetic, biological, environmental, and chemical. Research of a genetic nature has concentrated on the determination of relative sen- sitivities of species and their genotypes, and on the effects on pollen and pollen germination (Heck et al., 1986~. Mexican bean beetle larva fed preferentially on soybean foliage exposed to chronic concentrations of SO2 (Hughes et al., 1983~. Environmental factors include light, temperature, humidity, CO2, freezing, soil moisture, and soil nutrition. Several of these have been studied in combination. Plants are generally more sensitive to SO2 as light intensity, wind speed, temperature, and humidity increase; ele- vated CO2 levels protect plants; and freezing may increase plant sensitivity, while low soil moisture tends to make plants more resistant. The effect on plants of mixtures of pollutants (i.e., SO2 and 03) is due primarily to the O2 component and is discussed below. Research has shown that mixtures of SO2 and NO2 can cause interactive effects
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176 ECOLOGICAL RISgS TABLE 2 Growth and yield of selected crop species in response to sulfur dioxide exposures. Test Sulfur Dioxide Plant Exposure Characteristics Results Six species Constant and stochastic concentration, 0-0.20 ppm (Greenhouse) Barley Barley Rice (3cvs) L~liw?~ Constant SO2 concentration underestimated effects compared to the time series treat- ments; excellent discussion of time series concept; interpretation of results difficult. 0.010, 0.023, 0.038 and 0.058 ppm mean over growing season (Field, open release system) 0.04 to 0.20 ppm mean concentration across growing season; a two year field study; open release of SO2 0.05 to 0.20 ppm, 24 hr per day, 5 da per week, 15 weeks; in pots in open-top chambers 0.012 to 0.029 ppm perenne winter mean at 4 selected sites with differing SO2 concentrations (field-correlational) Controls not defied but three lowest SO2 concentrations gave about 5, 20, and 12% yield increase respectively; the high SO2 reduced yield about 18% (McLeod et al., 1986). Yield reduction found in both years; when average SO2 during fumigation was used in regression analysis found a 2.2% loss per 0.01 ppm of SO2 (Baker et al., 1986). Yield at highest SO2 compared to lowest was reduced from 11 to 29% in the three cultivars (Kats et al., 1985~. Two sites with lowest mean SO2 showed same total dry wt yields; two highest sites showed a -19 and -54% reduction respectively. Me site with highest SO2 also suffered winter injury (Ashenden, 1987). SOURCE: Heck et al., 1986. Individual references, not included here, are found in the original table. On sensitive plant types. An interesting biochemical explanation for the synergistic action of SO2 and NO2 on several grass species involves the inability of the plant to detoxify nitrite in the presence of SO2 (Wellburn et al., 1981~. Examples of the effects of SO2 on carbon translocation and partitioning and on plant growth and yield are shown in Able 2. Generally, assimilates move to developing leaves rather than to roots under low SO2 stress. Root growth is generally reduced more than shoot growth and occurs at relatively low SO2 concentrations. The results support the contention that plants are sensitive to low SO2 concentrations (< 0.10 ppm), when exposed continuously. Dose/response studies using an open-air SO2 release system have sim- ulated exposures of soybean to SO2 near point sources. Soybean yield was decreased by periodic SO2 exposures after flowering to doses of approx- imately 10 to 15 ppm-hours (Sprugel et al., 1980~. These dose statistics
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HUAL4N EFFECTS ON THE TERRESTRIAL ENVIRONMENT J 120 o at 0 1 tO o ~ 100 90 ~ -80 o o 177 CULTIVAR YEAR ~ WELLS 1977 O WELLS 1978 ~K- S 1492 1980 K-S 1492 1981 ' ~ WILLIAMS Iseo ~ ~ CORSOY 1980 - ° an on ~ 0 . · ~ so ~ I I l o 5 10 ~ 65 20 2S 50 :55 SULFUR Dl OX I DE DO SE ( ~ pm - H R ) FIGURE 1 Effects of periodic SO2 exposures in open air on the yield of soybeans (Heck et al., 1986~. were products of mean exposure durations of 2.5 to 4.2 hours, mean con- centrations of 0.12 to 0.31 ppm, and 19 to 25 exposures. Doses in the 5 ppm-hour range were either stimulators or inhibitory. Maximum peak-to- mean SO2-concentration ratios were about 2.5. Figure 1 shows results of these studies. Daily four- or seven-hour exposures of cotton and tomato (Heck et al., 1983b) or soybeans (Heagle et al., 1983) in open-top field chambers demonstrated that SO2 concentrations, which are likely to occur regionally in the United States, probably do not cause decreased yield. A similar conclusion was reached in a review by Roberts (1984) on the effects of SO2 on plant productivity, which included results from open-air studies. However, emissions of SO2 near point sources can cause decreased yield . . . . in sensitive crop species. EFFECTS OF OZONE ON AGRICULTURAL PRODUCTIVITY This section presents summary information on the effects of O3 on crop growth and productivity. It also provides background information on plant response, including some review of field research that supports efforts to assess O3 dose, and crop yield responses for assessment purposes.
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178 ECOLOGICAL RISKS Symptomatology The effects of O3 on crops are either visible (i.e., morphological, pigmented, chlorotic, or necrotic foliar patterns resulting from major phys- iological disturbances in plant cells) or subtle (i.e., measurable growth or physiological changes Without visible injury that may affect yield, or re- productive or genetic crop systems). Ozone injury often appears as flecks (small, bleached necrotic areas) or stipple (small pigmented areas) on up- per foliar surfaces. Chlorosis may be associated with acute exposure to O3. Chronic injury may cause chlorosis or other color or pigment changes that may eventually lead to cell death; early senescence with or without leaf abscission may occur. Chronic injury patterns are easily confused with symptoms caused by diseases, insects, other stresses, and normal leaf senescence. From a practical standpoint, visible foliar injury is the only conclusive way to identify O3 injury in the field. Research has shown relationships between visible injury and growth and yield for many plant species (Heck et al., 1977~. Physiological and Biochemical Effects Ozone enters leaves through stomata. Any stress causing stomata! closure reduces O3 uptake and thus protects the plant by avoidance. The fate of O3 after entry into plant leaves is not known. Some fraction of O3 may pass through the cell membrane (Mudd et al., 1984~; O3 may react with protein or lipid membrane components (Heath, 1980~; or free, radical products of O3 activity within the substomatal cavity may react with membrane components (Grimes et al., 1983~. Regardless of the exact mechanism of action, the cell membrane is probably the site of initial O3 reaction. Factors Affecting Plant Response Many biological and physical factors are known to affect the response of plants to 03, including genetic (e.g., cultivar and species differences, effects on reproductive structures, inheritance of sensitivity); biological (e.g., plant diseases, insects); environmental (e.g., climatic [temperature, light, humidity] and edaphic [nutrition, soil moistures; and chemical (e.g., herbicides, insecticides, special additives), as well as other factors. Genetic Research of a genetic nature has concentrated on the determination of relative sensitivities of species and their genotypes, and on the effects on
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HUMAN EFFECTS ON THE TERRESTRIAL ENVIRONMENT 179 pollen and pollen germination. Studies on the heritability of O3 resistance suggest that O3 resistance is heritable. Results of cultivar screening suggest that, when dealing with extremes of sensitivity, cultivars maintain the same relative separations when longer-term exposures are performed under both field and controlled conditions (Heck et al., 1988c). Biological Interrelationships between biological stresses (e.g., insects and dis- eases) and plant response to O3 must be understood as part of a crop-loss assessment effort. Available information regarding effects of O3 on plant parasites suggest that obligate fungal parasitism is generally inhibited and that some facultative parasites may benefit; these effects are probably indi- rect through the host. Foliar parasites may provide localized protection of the host from O3 injury. Review articles by Heagle (1982) and Lawrence (1981) cover much of the research on plant/parasite interactions. Environmental Relationships between climatic or edaphic factors and plant response to pollutant exposure are discussed in several O3 reviews (Heck et al., 1977; U.S. EPA' 1986~. Generalizations on the modifications of plant response to O3 by climatic factors are difficult because of the known exceptions. Evidence suggests that lower light intensity during growth, higher light intensity during exposure, higher growth temperatures, and higher growth and exposure humidities increase the sensitivity of many species to O3. Information suggests that increased O3 sensitivity, although related to stomata! conductance, reflects changed physiological conditions within the plant. Environmental conditions in the field can affect stomata! control of plant response the same day, and physiological control of plant response will start the following day. A two- to four-day period is usually necessary before physiological conditions that affect plant response to 0 will completely reflect the changed environmental conditions. Tingey et al. (1982), using a uniform water stress, reported that O3 sensitivity in bean decreased with increasing plant water stress; protection occurred in one day at the highest stress, and recovery occurred within six days. Beans treated with a chemical to induce stomata! opening in water-stressed plants were as sensitive to O3 as non-water-stressed plants (Tingey and Hogsett, 1985~. Results suggest that O3 protection in water- stressed plants is caused by stomata! control and not biochemical control. Heggestad et al. (1985) found that soybean growing in open-top chambers were more sensitive to ambient concentrations of O3 under a small soil- moisture stress than when adequate moisture was available. Because of the
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180 TABLE 3 Plant response to O3 and -SO2 mixtures. ECOLOGICAL RISKS Test Exposure Plant Information Plant Response to the Mixture Bean, snap Bean, field 0.20 ppm each gas; 7 hours/ day, 4 days; varied . . sa Duty 0.05-0.30 ppm O3; 0.04 ppm SO2; 4 hours Tomato 0.005 to 0.468 pprn SO2; 0.015 pprn or 0.056 ppm O3; 5 hr/ day, 5 da/wk, 57 days; field study with open top chambers Lettuce, 0.4 ppm O3, 0.8 radish ppm SO2; 6 hours Potato Soybean Four O3 concentrations filter- ing of ambient O3; 0.1 ppm SO2; for 6 hours/day, 255 hours 0.06 or 0.08 ppm O3, 0.06 or 0.11 ppm SO2; 5 hours/day, days; in open field facility Soybean 0.04 to 0.08 mean ppm 03, 0.00 to 0.11 mean ppm SO2; 5 hr/day, 16 days, during pod fill, linear gradient system in field. Stomatal conductance: synergistic (variable); foliar injury: antagonistic; growth: additive; effect changed with salinity. Net photosynthesis: additive or antag- onistic, depending on O3 concentration. Ripe fruit decreased 16% by O3 Cow SO2 treatment), 18% by SO2 (low O3 treatment); 32% in high O3 - high SO2 treatment; additive response (Heggestad et al., 1986).- Use of covariates increased precision for lettuce and radish; lettuce growth and injury effects antagonistic; radish was additive. Reductions in various growth and yield parameters were additive. Both O3 and SO2 caused decreases in a number of yield measures; mixture responses were additive. Ozone caused 26% seed yield reduction, SO2 a 6% reduction . . a. . . Wit n no slgnlIlcant interactions (Reich and Amundson, 1984). SOURCE: Heck et al., 1986. Individual references, not included here, are found in the onginal table. importance of soil water stress in agricultural areas, it is imperative that we try to understand this interaction and include it in any assessment effort. Pollutant Interactions Plants are often more severely affected by mixtures of O3 with other pollutants than by O3 alone (Lefohn and Ormrod, 1984; Reinert, 1984~. In general, mixtures tend to give a greater-than-additive (synergistic) response when the concentrations are below those causing visible effects from pol- lutants singly; concentrations around the injury threshold tend to produce an additive response; and concentrations above threshold tend to cause a less-than-additive (antagonistic) response. The term synergistic, although statistically appropriate, is not necessarily biologically appropriate since response functions may not be linearly related to pollutant concentration. Table 3 is a summary of results from selected studies using O3 with SO2.
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HUMAN EFFECTS ON THE TERRESTRIAL ENVIRONMENT TABLE 4 Growth and yield of selected crop species in response to ozone exposure. 181 Test Ozone Exposure Plant Characteristics Results Bean, lima Comparison of charcoal filtered (8 genotypes) (< 0.02 ppm mean daily max) and non-filtered (< 0.06 ppm mean daily max) greenhouses. Yield reductions of 3.4 to 68.5% were found across the 8 geno- types (Meredith et al., 1986). Bean, snap 0.30, 0.60 ppm; 1.5 hour, 2 Reduced relative and absolute times; 6 growth stages; growth rates, pod production, harvest 7 days after exposure modulation, and fixed nitrogen; or at fresh harvest (con- magnitude varied with O3 concentra- trolled) lion and growth stage. Tomato, 0.08-0.10 ppm; 5 hours/day, 5 86% reduction in fruit number, Tusy Ton days/week, 5 weeks (green- 91% reduction in fruit weight. house) Soybean 0.02 to 0.097 ppm; 341 hours, Yield was +15%, -34%, and -40% at intermittent over 113 days; 0.046, 0.070 and 0.097 ppm in com- greenhouse parison to 0.02 ppm. The increase at 0.046 ppm was not significant (Endress and Greenwald, 1985). Cotton, 0.20 ppm; 6 hours, 2 times/ Vegetative biomass and boll production Acala SJ-2 week, 1 group started at 8 day, reduced; greatest reduction in boll 1 at 42 days from seed and root weights; 48% reduction in (greenhouse) boll number. Clover, 0.03, 0.05, 0.08 ppm; 7 hours/ Total forage and forage regrowth Ladino day, 6 months Field: pots) reduced for clover and clover- fescue mixture in relation to O3 concentration; fescue unaffected. Rice (3 cvs) 0.05 to 0.20 ppm, 5 hr per Yield at highest O3 lowest day, compared to 5 da per wk. was reduced front 12 to 29% 15 wks; in pots in open in the three cultivars top chambers (Kats et al., 1985). SOURCE: Heck et al., 1986. Individual references, not included here, are found in the original table. Growth, Biomass, and Yield Effects Greenhouse and controlled-environment research were used in early assessments of O3 effects. These studies underestimated the effects of O3 found in later field studies, but the estimates were reasonable. The effects of O3 on growth and yield are briefly summarized in Able 4. Research results have generally shown that: · O3 affects crop growth and productivity; · cultivar differences are usually observed; · root growth is affected more than shoot growth;
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HUAI4N EFFECTS ON THE TERRESTRIAL ENVIRONMENT 1.0 08 en ~ 0.S e_ - ~ 0.4 - o ~0.2 185 —Corn Wheot , Cot ton Soybeans Peats 'Ng ~ ., O~ 1 1 1 1 1 =: 0 0.02 0.04 0 06 - _~ —_~_ \ - - _ ~ 0.08 0. Ozore Concentration (ppn`) FIGURE 2 Effects of chronic O3 exposures on the proportional yield loss of five crop species as predicted by the Weibull model, using results Mom open-top chambers. The O3 concentration is the seasonal 7-hr/day mean (Heck et al., 1986~. Ozone Functions for Use in Crop Loss Assessments The N CLAN program determined that the Weibull function had a number of redeeming features and accepted its relative response portion for use in assessment efforts. The Weibull permitted the assessment either to utilize a homogeneous response function for a species (i.e., a single or several cultivars) developed from experimental designs across years or sites, or to use a heterogeneous response function if such a function showed no apparent inconsistencies. In the assessment of yield effects Cable 6, Figure 2), many of the combined data sets were homogeneous; in the 1988 economic assessment, however, heterogeneous data sets were used where necessary to describe the effects on a single species (Adams et al., 1988~. Ozone dose/crop yield response functions can take on a variety of forms depending upon the dose statistic used. There is no preferred function,
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186 110 _ o Im c o - y .* 60 50 90 80 70 ECOLOGICAL RISKS _ Of . \ O iA ~ - ·~Q ·\ ~ or ~ Cordon Argo~,11 t980 · toys. aweigh, NC 1981 G Hods -Ithaca, NY 19 81 · Dovi. Ro~h,NC 1982 O Ems Bet? - lie, - 1982 OWiIIi~ -8~1~'vilb, Ad 1982 · Isis—Raleigh, NC 1983 C4ttivor Locotbn '9 · \ O 002 0.~ 0." 0.~ 0~ 0.12 0 ~ O.K Ozone C4=entraton- Seasonal 7 How/Doy Meon (pen) FIGURE 3 Effects of chronic O3 exposures in open-top field chambers on yield of soybeans. The seasonal O3 concentrations for the control treatment ranged from 0.02 to 0.03 ppm, depending on the year and location (Heck et al., 1986~. but it should utilize an exposure statistic that adequately describes the biological response to O3. The N CLAN program used 7-hr/day and 12- hr/day seasonal mean O3 values because they adequately described the yield responses of the crops tested. These functions were used by Adams et al. (1988) in their final economic assessment for NCLAN. Interpolations of Ozone Data to a County Level The NCLAN program utilized data from the U.S. Environmental Pro- tection Agency (EPA) Storage and Retrieval of Aerometric Data (SAROAD) system for interpolation processes. In the SAROAD system most monitor- ing sites are urban, with few in rural crop-growing areas, and many areas of the United States have only a few monitoring sites. Several factors enhanced our ability to interpolate O3 data across broad areas. First, O3 precursors are transported over great distances. Second, O3 is more stable as air masses move into rural areas because concentrations of reactive chemical species are reduced (Heck et al., 1984b). NCLAN used the krig- ing spatial interpolation process to develop county-level seasonal (7-hr/day,
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HUAL41V EFFECTS ON THE TERRESTRIAL ENVIRONMENT BOO - 1 .00 300 > o t00 o 187 SOt LEVEL · ·.000 o ·.C;26 · · .O~ 5 O · .367 1 to . . , , . , . o o ~ o 0 02 0.0. 0.06 0.08 0.10 0.12 O. 1. B 7H d~' SEASONAL - CAN 0. CONCE~rRAT'oN (ppm ) FIGURE 4 Yield response of 'Davis' soybean to combinations of O3 and SO2 at Raleigh, NC in 1982. Curve was estimated by polynomial analysis using combined SO2 data (Heagle et al., 1988~. 12-hr/day) mean O3 concentrations for use in crop-loss assessment (Heck et al., 1983b, 1984b). This technique was fully reviewed by an outside group and found to be a reasonable approach to estimate county-level O3 concentrations (Heck et al., 1985; Lefohn et al., 1987~. However, it should be noted that this technique does not handle mountainous terrain well, and it is weak where monitoring points are too far apart, as in much of the western United States. Crop Census The Census of Agriculture, conducted by the U.S. Department of Agriculture, provides a county-level yield statistic for crops of interest (Heck et al., 1982b; Shriner et al., 1984; Adams et al., 1988~. It involves an extensive national inventory of crops (not broken down by cultivars) and acreage grown. Data are obtained by analyzing responses to questionnaires mailed out approximately every five years. County estimates are adjusted for nonrespondents. Analysis of Crop Yield Reductions Ozone dose/crop yield response functions, crop yields at the county level, and seasonal 7-hr/day mean O3 concentrations at the county level are
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188 ECOLOGICAL RISKS Z I.0 ~ - Ve ~ o.a \ `N ~ o.e \ ° of o 0 0.2 _ ~ B o.o . 1 . I I , , , 002 004 0C>6 008 0 10 012 014 12 ~ 6~' SŁaSONa~ - ~~N as cot~cE~TR^rio~ I Pam ) FIGURE 5 Proportional yield response to O3 of cotton grown with intermittent periods of soil-moisture stress (WS) or grown with well-watered conditions (WOO) for 'McNair 235' at Raleigh, NC in 1985. Curves were derived using Weibull analyses with the a value set at 100 (Heagle et al., 1988~. used to calculate crop losses related to reductions in yield. The impacts of O3 are reflected in the yield data found in the Census of Agriculture. Using the county-level O3 values and the response function for the crop of interest, the expected percent yield reduction of the crop in the county is calculated. The yield reduction is based on comparing the yield found at the observed county-level O3 values with the expected yield at an 0.025 ppm O3 concentration (seasonal 7-hr/day mean O3 concentration in clean air). Increases in yield with different percentage improvements in air quality can then be calculated. Values for each crop and each county where a given crop is grown are then used to calculate national yield losses for each crop of interest. This approach was first used for an analysis with four species (i.e., corn, peanut, soybean, and wheat) by Heck et al. (1982b) as part of a larger assessment by Shriner et al. (1984~. The assessment was done to show the value of the selected approach in documenting regional and national losses of crops due to O3. Nine NCLAN type data sets (i.e., 1 corn, 1 peanut, 3 soybean, and 4 wheat) obtained from two N CLAN and seven pre-NCLAN studies at North Carolina State University were utilized in the assessment effort. County O3 and crop inventory data for 1978 were used. Kriging of the 1978 O3 data was first attempted and used
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HUAf4N EFFECTS ON THE TERRESTRIAL ENVIRONMENT 189 on a national basis by James Reagan (EPA) to predict county-wide yield losses (Heck et al., 1983a). The data sets were used with the 7-hr/day seasonal mean O3 statistic in calculating yield reductions using a linear response function. Results were calculated for county units, and tables and maps were developed to summarize and show patterns of the O3 effects on soybean, corn, wheat, and peanuts. The assessment estimated that an approximate $3 billion of productivity in the four crops would be gained if current maximum 7-hr/day seasonal O3 concentrations were reduced to 0.025 ppm. Soybean represented 64% of the impact, corn 17%, wheat 12%, and peanut 7%. The methodology is sound but the assessment of dollar losses cannot be considered an economic analysis. The same basic approach was utilized by Adams et al. in develop- ing yield reduction/increase estimates for their interim (1984) and final (1988) NCLAN economic assessment efforts. In the interim assessment, the Weibull model was used for the response function. Into O3 data sets were utilized: the kriged 1980 O3 data on a county basis and the 1978-82 five-year average O3 data base kriged to the county level. Crop inventory data were used and losses were based on 1980 dollars. Six crops (i.e., barley, corn, cotton, sorghum, soybean, and wheat) were used in this as- sessment. The final assessment utilized a similar approach, incorporated three additional crops (i.e., alfalfa, hay, and rice) and used 1982 as the base year for O3. The Economic Erects of Ozone on Agriculture Based on crop response data from many experimental designs, a num- ber of regional and national economic assessments have been made since 1980 (Table 7~. Regional estimates ranged from about $30 million (Min- nesota) to about $670 million (Corn Belt). National estimates were based on different groups of crops but ranged from $1.2 to 3.0 billion; corn and soybean were included in all estimates. The national economic assessments by NCLAN (Adams et al., 1988) was in good agreement, showing about $2.7 billion surplus with a 40% reduction in seasonal O3 concentrations (Table 8~. A summary of economic estimates suggests that current seasonal O3 concentrations are causing in excess of $3 billion annual loss in crop productivity (Adams et al., 1988~. CONCLUSIONS The information presented here supports the thesis that O3 has a major impact on crop production in North America. Assessment methodologies are developed along with results of field research that are critical to the prediction of O3 effects on crop productivity.
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190 ECOLOGICAL RISKS TABLE 7 Summary results of several regional and national economic assessment using NCLAN data.a Assumptions of Region O3 Concentration Crops Benefits ($ tic 106) California Reduce to 0.04 18 $ 45 ppm (seasons) Com Belt Reduce NAAQS from Coin, Soybean $ 668 0.12 to 0.08 ppm Wheat Illinois logo reduciion Com, Soybean $ 226 U.S. Reduce to 0.04 ppm Com, Soybean $ 2,400 Cotton, Wheat U.S. Reduce to 0.04 ppm Sene + Peanut $ 1,300 a Reports from 1984/1985; results in 1980 U.S. dollars. SOURCE: Adams et al., 1988. TABLE 8 National economic assessment from NCLAN.a Total Surplus O3 Assumption (millions in 1982 dollars) 1984 Model 25% increase 109to reduciion 25% reduciion 4~o reduciion 1988 Model 25% increase logo reduciion 25% reduciion 40% reduciion -2,165 699 1,828 2,637 -2,053 808 1,890 2,780 a Reports from 1984 and 1988; results in 1982 dollars. SOURCE: Adams et al., 1988 Summary of Current Knowledge on the Effects of Ozone (and Other Air Pollutants) · Ozone is responsible for most of the crop-yield losses from air pollutants on both a regional and national scale within North America. · Losses from other pollutants are minimal, relative to O3, and primarily source related or related to joint effects with O3. · Pollutant dose/crop yield response functions are essential for pre- dicting yield losses; non-linear models give the best fit to available field data for O3. · Based on available technology, the open-top chamber system is the best approach for the development of predictive models for O3, but open release systems may function well for other pollutants.
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HUMAN EFFECTS ON THE TERRESTRL4L ENVIRONMENT 191 · The extrapolation of O3 data on a regional basis, using the interpo- lation technique of kriging, is a useful and necessary part of an assessment effort. However, the technique is not suitable with SO2 or other point source related pollutants. Foliar symptoms on crops under field conditions often appear as early senescence and -may be difficult to assess. · Although the mechanism of plant response to air pollutants is not understood, the cell membrane is probably the site of initial impact for O3. · Ozone and SO2 affect photosynthesis and carbon allocation in plants; reduced allocation to roots and reproductive structures is usually found. Similar effects may be true for other pollutants. Differences in both species and cultivars within species response to air pollutants is found in all crops. Interactions between air pollutants (02, S02, and HF) and both biotic and abiotic factors on plant responses are documented. · The response of many crop species to O3 iS affected by the presence of other pollutants (specifically SO2 and NOT. · Most crops show growth, biomass and yield reduction when grown under current ambient air concentrations of O3. These responses may be true for SO2 and acidic precipitation, but the data are equivocal. · The NCLAN data base has permitted a reasonable first estimate of crop yield losses associated with O3 as an air pollutant of national and international importance. Areas of Uncertainty in Assessing the Effects of Air Pollutants on Crop Production · The available data base is small and thus is not fully representative of North America. For 03, only 10 field crops were studied in the N CLAN program; five had four or more experimental designs. Data for other pollutants is not as strong. · Potential effects of field methodology have not been fully addressed for any pollutant. · Ozone dose/crop yield response models are empirical and not based on mechanistic considerations. Models for other pollutants are weak. · The effect of soil moisture on crop yield response to air pollutants has been studied for O3 and SO2, but the results are not definitive. · The effects of other biotic or abiotic stresses on crop response to air pollutants are not understood and are not included in predictive models. · The importance of exposure dynamics (i.e., peak O3 values) occur- ring throughout the growing season is not well understood.
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192 ECOLOGICAL RISKS · There are insufficient rural monitoring sites to corroborate the knging interpolative process for 03; interpolation for other pollutants is not feasible. · The estimates of economic loss from O3 would probably range from $1-7 billion or more if all crops were considered; losses will vary from year to year depending on both O3 concentrations and meteorological conditions. REFERENCES Adams, R.M., J.D. Glyer, and B.A. McCarl. 1988. The NCLAN economic assessment: Approach, findings and implications. In Assessment of Crop Loss from Air Pollutants, W.W. Heck, D.T. Tingey, and O.C. Taylor, eds. London: Elsevier Science Publishers. Adams, R.M., S.A. Hamilton, and B.A. McCarl. 1984. The Economic Effects of Ozone on Agriculture. EPA. Environ. Res. Lab., Corvallis, OR. EPA~00/3 84-090. September 1984. Altshuller, A.P., and R.~ Linthurst, eds. 1984. The acidic deposition phenomenon and its effects: Critical assessment review papem, Vol. II: Effects Sciences, EPA-60018-83- 016B, EPA, Office of Research and Development, Washington, DC. Ashenden. 1987. Effects of ambient levels of air pollution on grass swards subjected to different defoliation regimes. Environmental Pollution 45:29-47. Baker, C.K., JJ. Colls, AK. Fullwood, and G.G.R. Seaton. 1986. Depression of growth and yield in winter barley exposed to sulphur dioxide in the field. New Phytologist 104:233-241. Banwart, W.L., P.M. Porter, J.J. Hassett, and W.M. Walker. 1987. Simulated acid rain effects on yield response of two corn cultivam. Agricultural Journal 79:497-501. Bressan, R.A., L.G. W~lson, and P. Filner. 1978. Mechanisms of resistance to SO2 in the cucurbitaceae. Plant Physiolology 61:761-767. Dochinger, LS. and T.A. Seliga, eds. 1976. Proceedings of the F~rst International Symposium on Acid Precipitation and the Forest Ecosystem. U.S.D.A. Forest Service, General Technical Report NE-23. Upper Darby, PA. DuBay, D.T., and AS. Heagle. 1987. The effects of simulated acid rain with and without ambient rain on the growth and yield of field-grown soybeans. Environmental and Experimental Botany 27:395-401. Endress, A.G., and C. Grunwald. 1985. Impact of chronic ozone on soybean growth and biomass partitioning. Agriculture, Ecosystems and the Environment 13:9-23. Evans, LS., K.F. Lewin, and G.R. Hend~y. 1986. Yields of field-grown soybean exposed to simulated acidic rainfalls. BNL 52009. Dept. Applied Science. Brookhaven National Laborato~y, Upton, NY. Grimes, H.D., KK Perkins, and W.F. Boss. 1983. Ozone degrades into hydroxyl radical under physiological conditions. Plant Physiology 72:1016-1020. Guderian, R., ed. 1985. Photochemical oxidants-formation, distribution, control and effects on vegetation. Berlin and New York: Springer-Verlag. Heagle, AS. 1982. Interactions between air pollutants and parasitic diseases. Pp. 333-348 in Effects of Gaseous Air Pollution in Agriculture and Horticulture, M.H. Unsworth and D.P. Ormrod, eds. London: Buttersworth Scientific. Heagle, A S., W.W. Heck, J.O. Rawlings, and R.B. Philbeck. 1983. Effects of chronic doses of ozone and sulfur dioxide on injury and yield of soybeans in open-top chambers. Crop Science 23:1184-1191. Heagle, S.S., L~! Kress, PJ. Temple, R.J. Kohut, J.E. Miller, and H.E. Heggestad. 1988. Factors inDuencing ozone doselyield response relationships in open-top field chamber studies. In Assessment of Crop Loss from Air Pollutants, W.W. Heck, D.T. Tingey, and O.C. Taylor, eds. London: Elsevier Science Publishers.
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HUMAN EFFECTS ON THE TERRESTRIAL ENVIRONMENT 193 Heath, R.L. 1980. Initial events in injury to plants by air pollutants. Annual Review of Plant Physiology 31:395-431. Heck, W.W. 1984. Defining gaseous pollution problems in North Amenca. Pp. 35-48 in Gaseous Air Pollutants and Plant Metabolism, M.J. Koziol, and F.R. Whatley, eds. London: Butte~worth. Heck, W.W., and C S. Brandt. 1977. Effects on vegetation: Native crops, Forest. Pp. 157-229 in Air Pollution, A.C. Stern, eds. 3rd Edition, Vol. 2b. New York: Academic Press. Heck, W.W., A.S. Heagle, and D.S. Shriner. 1986. Effects on vegetation: Native crops, forest. Pp. 247-350 in Air Pollution, A.C. Stern, ed. 3rd Edition, Vol. 6. New York: Academic Press. Heck, W.W., J.B. Mudd, and P.R. Miller. 1977. Plants and microorganisms. Chapter 11 in Ozone and Other Photochemical Oxidants. National Academy of Sciences, Washington, DC. Heck, W.W., D.T. Tingey, and O.C Taylor, eds. 1988a. Assessment of crop loss from air pollutants. London: Elsevier Science Publishers. . 1988b. Assessment of crop loss from air pollutants. Environmental Pollution. Special Issue 53. Heck, W.W., U. Blum, R.A. Reinert, and AS. Heagle. 1982a. Effects of air pollution on crop production. Pp. 333-350 in Strategies of Plant Reproduction, YUJ. Meudt, ed. BARC Symposium No. 6. Totowa, NJ: Allanheld, Osman & Co. Publisher, Inc. Heck, W.W., J.A. Dunning, R.A. Reinert, S.A. Prior, M. Rangappa, and P.S. Benepal. 1988c. Differential response of four bean cultivars to chronic doses of ozone. Journal of the American Society of Horticultural Sciences 113:46-51. Heck, W.W., R.M. Adams, W.W. Cure, A.S. Heagle, H.E. Heggestad, R.J. Kohut, L.W. Kress, J.O. Rawlings, and O.C. Taylor. 1983a. A reassessment of crop loss from ozone. Environmental Science and Technology 17:573-580A. Heck, W.W, O.C Taylor, R. Adams, G. gingham, J. Miller, E. Preston, and L~ Weinstein. 1982b. Assessment of crop loss from ozone. Journal of the Air Pollution Control Association 32 35~362. Heck, W.W., U. Blum, W.F. Boss, A.S. Heagle, R.A. Linthurst, R.A. Reinert, J.F. Reynolds, and H.H. Rogem. 1984a. Pe~spectives of air pollution research on plants. Pp. 17~249 in Reviews in Environmental Toxicology I, Ernest Hodgson, ed. Amsterdam: Elsevier Scientific Publishing Co. Heck, W.W., W.W. Cure, J.O. Rawlings, IJ. Zaragoza, AS. Heagle, H.E. Heggestad, R.J. Kohut, L^W. Kress, and P.J. Temple. 1984b. Assessing impacts of ozone on agricultural crops. I. Overview. Journal of the Air Pollution Control Association 34:729-735. . 1984c. Assessing impacts of ozone on agricultural crops: II. Crop yield functions and alternative exposure statistics. Journal of the Air Pollution Control Association 34:810-817. Heck, W.W., O.C. Taylor, R.M. Adams, G. gingham, J.E. Miller, E.M. Preston, UH. Weinstein, R.G. Amundson, RJ. Kohut, J.A. Laurence, W.C. Cure, A S. Heagle, J.T. Gish, H.E. Heggestad, L.W. Kress, G.E. Neely, J.O. Rawlings, and P. Temple. 1983b. National Crop Loss Assessment Network (NCLAN) 1982 Annual Report. EPA 600/3-84-049. EPA, Corvallis, OR. Heck, W.W., O.C. Taylor, R.M. Adams, J.E. Miller, D.T. Tingey, L.H. Weinstein, R.G. Admundson, NS. Heagle, D.N King, R.G. Kohut, L~W. Kress, J.A. Laurence, AS. Lefohn, V.M. Lesser, J.R. Miller, G.E. Neely, PJ. Temple, and J.O. Rawlings. 1985. National Crop Loss Assessment Network (NC~ 1984 Annual Report. EPAJ600/3- 86/041, Environ. Res. Lab., Office of Res. and Develop., EPA, Corvallis, OR. Heggestad, H.E., J.H. Bennett, E.H. Lee, and L^W. Douglass. 1986. Effects of increasing doses of sulfur dioxide and ambient ozone on tomatoes: plant growth, leaf injuty, elemental composition, fruit yield and quality. Phytopathology 76:1338-1344. Heggestad, H.E., T.J. Gish, E.H. Lee, J.H. Bennett, and bW. Douglass. 1985. Interac- tion of soil moisture stress and ambient ozone on growth and yields of soybeans. Phytopathology 75:472~77.
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194 ECOLOGICAL RISKS Hughes, P.R., A.I. Dickie, and M.^ Penton. 1983. Increased success of the Mexican bean beetle on field grown soybeans exposed to sulfur dioxide. Journal of Environmental Quality 12:565-568. Irving, P.M. 1987. Effects on agricultural crops. Chapter 6 in Interim Assessment: The Causes and Effects of Acidic Deposition. Vol. IV. The National Acid Precipitation Assessment Program. Washington, D.C. Jager, H.J., and H. Klein. 1980. Biochemical and physiological effects of sulfur dioxide on plants. Angewandte Botanik 54:337-348. Kats, G., P.J. Dawson, A. Bytnerowicz, J.W. Wolf, C.R. Thompson, and D.M. Olszyk. 1985. Effects of ozone or sulfur dioxide on growth and yield of rice. Agriculture, Ecosystems and the Environment 14:103-117. Laurence, J.A. 1981. Effects of air pollutants on plant pathogen interactions. Zeitschrift fur Pflanzenkrankheiten und Pflanzenschutz 88:156-172. Lefohn, A S. and D.P. Ormrod, eds. 1984. A review and assessment of the effects of pollutant mixtures on vegetation- Research recommendations. EPA~00/3-84-037. Corvallis Environmental Research Lab., Office of Research and Development, EPA, Cowallis, OR. Lefohn, A.S., H.P. Knudsen, J. Logan, J. Simpson, and C. Bhumralkar. 1987. An evaluation of the Kriging method, as applied by NCLAN, to predict 7-fur seasonal ozone concentrations. Journal of the Air Pollution Control Association 37:595 60Z Mansfield, T.N, M.E. Whitmore, and R.M. Law. 1982. Effects of nitrogen oxides on plants: two case studies. Pp. 511-520 in Air Pollution by Nitrogen Oxides, T. Schneider and L" Grant, eds. Amsterdam: Elsevier Scientific Publ. Co. McLeod, A.R., K. Alexander, and D.M. Cribb. 1986. Effects of open-air fumigation with sulfur dioxide on the growth of cereals. I. Grain Yield of Winter Barley (Hordeum vulgare) cv Sonja 1982-83. Report No. TPRD/L/3071/R86 Central Electricity Research I~ bora tories, Lea therhea d, Surry, U.K. Meredith, F.I., C.A. Thomas, and H.E. Heggestad. 1986. Effect of the pollutant ozone in ambient air on lima bean. Journal of Agriculture and Food Chemistry 34:179-185. Mudd, J.B., S.K. Banerjee, M.M. Pooley, and KL~ Knight. 1984. Pollutants and plant cells: effects on membranes. Chapter 8 in Gaseous Air Pollutants and Plant Metabolism. M.J. Koziol, and F.R. Whatley, eds. London: ButteIworth. National Academy of Sciences. 1977. Nitrogen Oxides. Chapter 9. National Academy Press, Washington, D.C. Olsyk, D.M., and D.T. Tingey. 1984. Phytotoxicity of air pollutants. Plant Physiolology 74:999-1005. Ormrod, D.P., 1978. Pollution in Horticulture. Amsterdam and New York: Elsevier Scientific Publishing Company. Pell, E.J., CJ. Arny, and N.S. Pearson. 1987. Impact of simulated acidic precipitation on quantity and quality of a field grown potato crop. Environmental and Experimental Botany 27:7-14. Rawlings, J.O., and W.W. Cure. 1985. The Weibull function as a dose/response model for studying air pollution effects on crop yields. Crop Science 25:807-814. Reich, P.B., and R.G. Amundson. 1984. Low level O3 and/or SO2 exposure causes a linear decline in soybean yield. Environmental Pollution (Series A) 34:345-355. Reinert, R.A. 1984. Plant response to air pollutant mixtures. Annual Review of Phytopathol- ogy 22:421-442. Roberts, T.M. 1984. Effects of air pollution on agriculture and forestry. Atmospheric Environment 18:629-652. Rogers, H.H., J.C. Campbell, and R.J. yolk. 1979. Nitrogen-15 dioxide uptake and incorporation by Pnaseolus vulgans L Science 206:33~335. Sekiya, J., LG. Wilson, and P. Filner. 1982. Resistance to injury by sulfur dioxide. Plant Physiology 70:437-441. Shriner, D.S., C.R. Richmond, and S. E. Lindberg, eds. 1 980. Atmospheric sulfur deposition , environmental impact and health effects. Ann Arbor: Ann Arbor Science Publishers, Inc.
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HUMAN EFFECTS ON THE TERRESTRIAL ENVIRONMENT 195 Shriner, D.S., W.W. Cure, A.S. Heagle, W.W. Heck, D.W. Johnson, R.J.Olson, and J.M. Skelly. 1984. An analysis of potential agriculture and forest impacts of long range transport air pollutants. ORNL-5910. Oak Ridge National Laboratory, Oak Ridge, TN. Shupe, J.L., H.B. Peterson, and N.C. Leone, eds. 1983. Fluorides: Effects on vegetation, animals, and humans. Proceedings of the International Fluoride Symposium, Paragon Press, Inc., Salt Lake City, UT. Sprugel, D.G., J.E. Miller, R.N. Muller, HJ. Smith, and P.B. Xerikos. 1980. Sulfur dioxide effects on yield and seed quality in field-grown soybeans. Phytopathology 70:1129-1133. Temple, PA., and O.C. Taylor. 1983. Worldwide ambient measurements of peroxyacetyl nitrate (PAN) and implications for plant injury. Atmospheric Environment 17:1583-1587. Tingey, D.T., and W.E. Hogsett. 1985. Water stress reduces ozone injury via a stomata! mechanism. Plant Physiology 77:944-947. Tingey, D.T., G.L~ Thutt, M.I~ Gumpertz, and W.E. Hogsett. 1982. Plant water status influences ozone sensitivity of bean plants. Agriculture and the Environment 7:243- 254. Reshow, M., ed. 1984. Air Pollution and Plant Life. Chichester, England: John Wiley & Sons Limited. Unsworth, M.H., and D.P. Ormrod, eds. 1982. Effects of gaseous air pollution in agriculture and horticulture. Butterworth, London. U.S. Environmental Protection Agency (EPA). 1978. Air Quality Criteria for Ozone and Other Photochemical Oxidants. Chapters 10/11, EPA 60018-79 004. Office of Research and Development, Washington, D.C. U.S. EPA. 1982a. Air Quality Criteria for Oxides of Nitrogen. Chapter 12, EPA-600/8-82-026. Office of Research and Development, Environmental Criteria and Assessment Office, Research Triangle Park, NC. U.S. EPA. 1982b. Air Quality Criteria for Particulate Matter and Sulfur Oxides. Vol. III, Chapter 8, EPA 600/8 82-029C. Office of Research and Development, Environmental Criteria and Assessment Office. Research Triangle Park, NC. U.S. EPIC 1986. Air Quality Criteria for Ozone and Other Photochemical Oxidants. Vol III, Chapter 6, EPA 600/8-84~20CF. Environmental Criteria and Assessment Office, Research Triangle Park, NC Wellburn, JAR., C. Higginson, D. Robinson, and C Walmsley. 1981. Biochemical explanations of more than additive inhibitory effects of low atmospheric levels of sulfur dioxide plus nitrogen dioxide upon plants. New Phytologist 88:223-237. Winner, W.E., H.N Mooney, and R.A. Goldstein, eds. 1986. Sulfur dioxide and vegetation: Ecology, physiology and policy Issues. Stanford Univ. Press, Pala Alto, CA. Yoneyama, T., H. Sasakawa, S. Ishizuka, and T. Tatsuka. 1979. Absorption of atmospheric NO2 by plants and soils. Soil Science and Plant Nutrition 25:267-Z75.
Representative terms from entire chapter:
primary primary primary