Ambient Ozone Impacts on Specialty Crops
NE-1013/1030 CSREES project, F. Booker, Chair
USDA-ARS Plant Science Research Unit
Department of Crop Science, Box 7631, NC State University
Raleigh, NC 27695
October 3, 2007
There are at least 12 major crop species within the U.S. that are considered ozone-sensitive,
many of which are classified as specialty crops (Krupa et al., 1998b). These include alfalfa,
barley, bean, clover and other forages, grape, oat, peanut, potato, rice, tomato and watermelon
(Benton et al., 2000; Burkey et al., 2007; Heagle, 1989; Kats et al., 1985; Kobayashi et al., 1995;
Krupa et al., 1998b; Synder et al., 1991). In addition, a commercial sugarcane clone in
California may be ozone-sensitive (D. Grantz, personal communication). Ornamental plants
such as petunia and buddleia, fruit bushes (blueberry), and landscape shrubs can also be damaged
by ambient ozone (Cathey and Heggestad, 1982; Chappelka, 2002; Findley et al., 1997a; Findley
et al., 1997b). Ozone-sensitive plants frequently exhibit visible foliar injury, and chronic ozone
exposures can reduce yields and biomass. Nutritional quality also declines in some crops and
forages. Agronomic crop yield loss due to ambient ozone in the U.S. is estimated to range from
5 to 15% (Heagle, 1989), worth $3-5 billion annually (EPA, 2006; Fiscus et al., 2005).
However, the database for these estimates is inadequate, especially for specialty crops. In
addition, wide variability in ozone-sensitivity among various crop cultivars is common.
Variation in sensitivity within species may be as great as differences among species (EPA,
2006).
There continues to be a critical need to obtain quantitative data on ozone exposure-plant response
relationships under ambient conditions and in a changing climate. According to the US EPA’s
Clean Air Science Advisory Committee (CASAC), the quantitative evidence linking specific
ozone concentrations to specific vegetation effects - especially at the complex ecosystem level must continue to be characterized as having high uncertainties due to the lack of data for
verification of those relationships (CASAC, 2006, http://www.epa.gov/sab/pdf/casac-07001.pdf). Similarly, studies are needed to explain the mechanisms of when and why plants are
susceptible or tolerant to ozone stress. These efforts can assist in better defining the geographic
extent, magnitude and economic consequences of the adverse effects of tropospheric ozone on
crops and other vegetation.
Tropospheric ozone, both an air pollutant and a greenhouse (re-radiative) gas, is detrimental to
plants and human health, and contributes to global warming (EPA, 2006; Prather et al., 2001).
While ozone is a normal component of the troposphere, background levels of ozone have been
increasing for more than 100 years. They have doubled since pre-industrial times, and are
continuing to increase, with average annual concentrations ranging from 20 to 45 ppb. Despite
national air quality regulations aimed at controlling ground level ozone pollution, it continues to
be a major concern for crop production and forest health (EPA, 2006). As of 2005, there were
455 counties in the U.S., mainly along the eastern seaboard, the Midwest and the south central
regions, and California that were in violation of the current National Air Quality Standard (EPA,
2006). Moreover, every region of the U.S. except for the Pacific Northwest and much of the
2
Great Plains experiences phytotoxic ambient ozone concentrations periodically during the
growing season. East Asian countries, India, Pakistan, many countries around the
Mediterranean, parts of Mexico and Brazil are currently experiencing reductions in crop
production due to ambient ozone (Emberson et al., 2001; Wang and Mauzerall, 2004). Climate
model projections forecast that the largest rice and peanut producing regions in the world,
located mainly in China, Japan, India, central Africa, the southern U.S., and Indonesia, may
experience significantly higher levels of tropospheric ozone in the coming 50 years (Emberson et
al. 2001; Wang and Mauzerall, 2004). Rising levels of atmospheric CO2 will likely moderate the
influence of increasing ground-level ozone concentrations in these regions, but eventual impacts
on yield in concert with other changing environmental factors are unclear.
While peak ozone concentrations in the U.S. may be lower on average recently, chronic exposure
in the range that can affect plants interspersed with episodes of higher concentrations continue to
occur (EPA, 2006). In fact, intermediate concentrations of ambient ozone may have the largest
impact on crop yields (Krupa et al., 1995). Ozone uptake is highest during mid-day and early
afternoon when high rates of leaf gas-exchange coincide with rising ozone concentrations. There
appears to be a tipping point around seasonal average ozone concentrations of 50 ppb or greater
that results in yield suppression in ozone-sensitive crops (Krupa et al., 1994; Krupa et al.,
1998a). However, environmental factors such as temperature, saturation vapor pressure deficit,
soil moisture content, and solar radiation intensity modulate ozone uptake by plants and thus
influence spatial and temporal variability in concentration-response relationships. For example,
ambient ozone injury to crops is widespread across Europe, and countries that have low ozone
concentrations but high ozone stomatal fluxes have frequent records of visible injury attributed
to ozone (Harmens et al., 2007). Understanding how environmental factors affect ozone flux is
critical for predicting ambient ozone impacts on vegetation. Genotype and developmental stage
also play major roles in determining plant sensitivity to ozone.
Research on plant responses to ozone has included various experimental approaches. Most
ozone experiments have used controlled environment, greenhouse, field chambers and free-air
systems (EPA, 2006). The USDA National Crop Loss Assessment Network (NCLAN) program
utilized regression modeling approaches based on concentration-response experiments conducted
in open-top field chambers to estimate ambient ozone effects on various crop species (Rawlings
et al., 1988). Free-air systems use ambient level and greater ozone concentrations for predictive
purposes. We have relatively limited direct evidence about how plants respond to ambient levels
of ozone versus clean air environments (Heagle, 1989; Olszyk et al., 1993). However, the
evidence that is available suggests that chambers do not fundamentally alter plant responses to
ozone, and chambers remain a useful tool for testing species sensitivity and developing ozoneresponse relationships (EPA, 2006). In general, soybean responses to ozone in free-air systems
have supported results from open-top chamber experiments (Morgan et al., 2006).
Most ozone studies, however, have been single factor or two-way interaction experiments. The
effects of ambient ozone in combination with two or more other environmental factors have been
little explored. But, it has been shown in rice that the magnitude of the ozone and elevated
carbon dioxide responses and interactions can be influenced by high temperature episodes,
nutritional status and intra-plant competition (Reid and Fiscus, 2008). Such experiments are
3
complicated and expensive to conduct. However, plant responses to ozone are highly influenced
by site conditions, and comprehensive assessment of their relative influences needs attention.
One way to obtain insight about the effects of ambient ozone on plants is to compare the growth
and productivity of plant cultivars and clones that are known to differ from each other in
response to ozone as detected by ozone injury symptom expression and/or changes in biomass
and yield. This has been done with clonal clover and selected bean lines. In experiments
utilizing ambient air exposures in New York, North Carolina, and California, ambient ozone
concentrations were sufficient to cause respectively a 25%, 39% and >50% biomass reduction in
sensitive versus tolerant clones of white clover (Heagle et al., 1995). Similarly, in North
Carolina, a 50% yield reduction was observed in sensitive versus tolerant cultivars of snap bean
grown in ambient air (Burkey et al., 2005). On Long Island, NY, snap bean pod yield of the
sensitive line was reduced by as much as 43%. When ozone concentrations were much lower
during the late-season crop (August), compared with the previous two crops (June and July),
ozone injury was less, and the sensitive and tolerant lines yielded similarly. The similar yields at
low ambient ozone concentrations further demonstrated that these lines were a suitable biological
tool for assessing the impact of ambient ozone.
Results obtained with sensitive and tolerant crop lines, however, have been qualified by the
discovery that pairs of ozone sensitive-tolerant plants can differ in growth rate, size, and
performance although the differentially-sensitive snapbean lines S156 and R123 are similar in
size and productivity in low ozone air (Burkey et al. 2005; Flowers et al. 2007). Another
drawback is the lack of an effective control treatment when comparing two plants. One way to
create such a control is to use only the sensitive plant and treat half of the plants with the ozoneinjury suppressing chemical l-ethylenediurea (EDU) and not the other half. There is ample
precedent for this type of experiment and generally good results using clover, peanut and snap
bean (Ensing et al., 1986; Manning and Krupa, 1992; Miller et al., 1994). However,
uncertainties continue to exist regarding the influence of EDU treatment regimes, concurrent
environmental conditions, and relative species/cultivar sensitivity to ambient ozone when using
EDU to assess ambient ozone damage to vegetation.
In addition to reductions in biomass or crop yield, many studies indicate that there may be
economically important effects of ambient ozone on the quality of crop and forage species (EPA,
1996). Visible symptoms on marketable portions of crops and ornamental plants can occur with
seasonal 7-h mean ozone exposures of 40 to 100 ppb (EPA, 2006). Several examples of changes
in crop quality due to ambient ozone are presented below.
In a UK study, potato exposed to an AOT (Accumulated exposure Over a Threshold) 40 value of
12.5 ppm.h in open-top chambers resulted in the paste from tubers being more viscous (Donnelly
et al., 2001). In this study, an AOT40 exposure of 27.11 ppm.h caused starch granules to be less
resistant to swelling, and total glycoalkaloid content was increased. Such increases in
glycoalkaloid content have been observed previously in potato (Pell and Pearson, 1984) and may
be important because glycoalkaloids cause bitter flavors and, at higher concentrations, toxicity.
In the CHanging climate and potential Impacts on Potato yield and quality (CHIP) program, the
effects of ozone were studied using open-top chambers at six sites in northern Europe. The
reducing sugar and starch content of tubers decreased linearly due to ozone exposure, while the
4
ascorbic acid concentration increased (Vorne et al., 2002). Compared to the control, exposure to
an AOT40 value of 14 ppm.h decreased starch concentrations by 2%, decreased reducing sugar
concentration by 30%, and increased ascorbic acid concentration by 20%. While the changes in
reducing sugars and ascorbic acid increased tuber quality, the reduction in starch concentration
decreased tuber quality.
Ozone has been found to reduce the oil, protein, and carbohydrate contents of Eurol rape seed in
a free-air exposure system in the UK (Bosac et al., 1998; Ollerenshaw et al., 1999). Yield
quality measured as crude protein and oil content was decreased significantly. Because the price
of the product is reduced in direct proportion to the oil content, such a decrease represents a
substantial loss to growers.
Watermelon (cv. Sugar Baby) grown as an autumn crop in open-top chambers in Indiana and
treated with either charcoal-filtered or non-filtered air showed a significant decrease in
marketable yield by weight and number (21%) for plants grown in non-filtered air compared
with those grown in clean air (Synder et al., 1991). In two studies using open-top chambers in
commercial fields in Spain, the soluble solids content of watermelon was decreased 4 to 8% due
to seasonal ambient ozone levels (Gimeno et al., 1999).
One of the most common effects of ozone is to promote leaf senescence. Thus, in pastures or
other types of grasslands exposed to ozone the fraction of senescing tissue may be increased.
Studies also indicate that ambient ozone can reduce forage nutritive quality as well as biomass.
For example, in grass-clover forage, white clover leaf in vitro dry matter disappearance and N
were decreased, and neutral detergent fiber increased by ambient ozone (50 ppb) compared with
charcoal-filtered air (Burns et al., 1997). In another study, exposure to elevated O3 under free-air
conditions caused reductions in the digestibility and nutritive quality of clover, and these were
not ameliorated by co-exposure to elevated CO2 as has been observed for physiological
processes reflected in plant growth and biomass production (Fuhrer 2003). Decreased yield and
quality of ozone-exposed bahiagrass (Paspalum notatum) (Muntifering et al., 2000) and sericea
lespedeza (Lespedeza cuneata) (Powell et al., 2003) were of sufficient magnitude to have
nutritional implications in their utilization by mammalian herbivores (Krupa et al., 2004).
Results from a long-term experiment in a species-rich, extensively managed Swiss pasture
revealed that forage nutritive quality was altered by ozone as a result of shifts in proportions of
grasses, legumes and forbs (Lin et al., 2007). Likewise, a decline in relative feed value of highyielding alfalfa in Alberta, Canada was strongly linked to ambient ozone concentrations (Lin et
al., 2007). Decreased nutritive quality of forages can lead to lower milk and meat production
from grazing animals, thus linking air quality with impacts on animal production systems.
Because loss of nutritive quality due to O3 injury has been observed to approach the same order
of magnitude as that observed for biomass yield depression, total loss of consumable food value
(fractional reduction in yield × fractional reduction in nutritive quality could possibly be much
more significant than biomass yield reductions alone in the assessment of the true economic
impact of O3 on herbaceous vegetation under current and future global-climate scenarios.
Lastly, parasites and pests might also affect ozone dose-yield response relationships. Ozone can
decrease severity of disease caused by obligate parasites such as rusts and powdery mildew of
small grain crops and increase severity of disease caused by facultative parasites such as Botrytis
on onion and potato (Heagle, 1989). The Mexican bean leaf beetle, Epilachna varivestis,
5
consumes more foliage of soybean plants exposed to ozone than foliage of nonexposed plants.
However, virtually nothing is known about interactive effects between parasites, pests, and
seasonal exposure to ozone on crop yield (Heagle, 1989).
Understanding the impact of ambient ozone under open field conditions is especially relevant to
current agricultural practices where new crop cultivars, many of which are genetically-modified,
are being placed into production without specific consideration of their sensitivity to ambient
ozone. Crop breeding programs need to incorporate selection of traits for improved plant
tolerance to ambient ozone to maintain and increase crop yields and nutritive quality. In
addition, there has been very little consideration of how rising atmospheric carbon dioxide and
nitrogen deposition levels could alter plant responses to ozone and vice-versa. This issue is
important to air quality regulators, crop producers, ecosystem managers, and climate modelers.
As has been shown recently for elevated carbon dioxide, this is a major uncertainty in projecting
future national and global food supply (Long et al., 2006).
A full assessment of ambient ozone impacts on crop performance is likely to be complex. In
addition, growers may not perceive the yield losses due to ozone because there is no clean-air
reference for comparison. Also, environmental conditions influence ambient ozone effects and
inter-annual variability in weather conditions complicates the picture. It is impossible to assess
yield loss in the field or to positively diagnose ozone symptoms without comparisons at a range
of ozone concentrations. This can be accomplished through studies using a variety of
approaches. These include outdoor controlled-environment chambers, open-top field chambers,
free-air exposure systems, open air experiments with sensitive/tolerant cultivars, ozoneprotectants, and multivariate modeling of plant responses to ambient ozone using multiple study
locations and similar experimental protocols. These protocols can be used in various
combinations, augmented by modern molecular biology techniques such as quantitative trait loci
(QTL) analyses with available recombinant inbred lines (e.g., rice, peanut and tomato), to screen
crops for ozone sensitivity. Studies are needed to: a) define crop responses to ozone under a
range of controlled environmental conditions; b) identify molecular markers for ozone
sensitivity; c) assess plant responses to ambient ozone in natural settings; and, d) construct
predictive models of crop performance in a changing climate. These are costly studies to
conduct and have not been performed for currently relevant cultivars. In general, it is important
to remember that elevated ozone is toxic to all living things. Our current understanding of crop
responses to ozone indicates that measurable yield losses due to ozone toxicity are likely
occurring in many regions of the U.S. and elsewhere in the world. However, to refine the range
of likely losses will require updating and expanding previous studies using modern cultivars
grown under current production conditions of fertility and water management. Potential gains
achieved by screening modern cultivars for ozone sensitivity utilizing marker-assisted selection
is an unexplored arena although preliminary studies are underway (Kim et al., 2004).
Research issues
1. Assess the impact of ambient ozone pollution on specialty crop production and nutritional
quality, both nationally and internationally.
2. Determine the influence of other growth-regulating environmental factors on plant
responses to ozone.
3. Determine the influence of ambient ozone in plant pest and pathogen relationships.
6
4. Quantify the contributions of ambient ozone from those of the other factors to crop
productivity and chemistry.
5. Determine the potential of modern genetic screening techniques, e.g., QTL analysis and
marker-assisted selection, for assessing ozone-sensitivity of new crop cultivars.
6. Convey to the public the nature and degree of the impact.
7
References
Benton, J., J. Fuhrer, B.S. Gimeno, L. Skarby, D. Palmer-Brown, G. Ball, C. Roadknight, and G.
Mills. 2000. An international cooperative programme indicates the widespread
occurrence of ozone injury on crops. Agriculture Ecosystems and Environment 78:19-30.
Bosac, C., V.J. Black, J.A. Roberts, and C.R. Black. 1998. Impact of ozone on seed yield and
quality and seedling vigour in oilseed rape (Brassica napus L.). Journal of Plant
Physiology 153:127-134.
Burkey, K.O., J.E. Miller, and E.L. Fiscus. 2005. Assessment of ambient ozone effects on
vegetation using snap bean as a bioindicator species. Journal of Environmental Quality
34:1081-1086.
Burkey, K.O., F.L. Booker, W.A. Pursley, and A.S. Heagle. 2007. Elevated carbon dioxide and
ozone effects on peanut. II. Seed yield and quality. Crop Science 47:1488-1497.
Burns, J.C., A.S. Heagle, and D.S. Fisher. 1997. Nutritive value of ozone sensitive and resistant
Ladino white clover clones after chronic ozone and carbon dioxide exposure, p. 153-167,
In L. H. Allen, Jr., et al., eds. Advances in carbon dioxide effects research. Proceedings
of a symposium. American Society of Agronomy, Madison.
Cathey, H.M., and H.E. Heggestad. 1982. Ozone sensitivity of herbaceous plants: Modification
by ethylenediurea. Journal of the American Society of Horticultural Science 107:10351042.
Chappelka, A. 2002. Reproductive development of blackberry (Rubus cuneifolius), as influenced
by ozone. New Phytologist 155:249-255.
Donnelly, A., J. Craigon, C.R. Black, J.J. Colls, and G. Landon. 2001. Elevated CO2 increases
biomass and tuber yield in potato even at high ozone concentrations. New Phytologist
149:265-274.
Emberson, L.D., M.R. Ashmore, F. Murray, J.C.I. Kuylenstierna, K.E. Percy, T. Izuta, Y. Zheng,
H. Shimizu, B.H. Sheu, C.P. Liu, M. Agrawal, A. Wahid, N.M. Abdel-Latif, M. van
Tienhoven, L.I. de Bauer, and M. Domingos. 2001. Impacts of air pollutants on
vegetation in developing countries. Water, Air, and Soil Pollution 130:107-118.
Ensing, J., G. Hofstra, and E.J. Adomait. 1986. The use of cultivar yield data to estimate losses
due to ozone in peanut (Arachis hypogeae). Canadian Journal of Plant Science 66:511520.
Findley, D.A., G.J. Keever, A.H. Chappelka, D.J. Eakes, and C.H. Gilliam. 1997a. Differential
response of buddleia (Buddleia davidii Franch.) to ozone. Environmental Pollution
98:105.
8
Findley, D.A., G.J. Keever, A. Chappelka, C.H. Gilliam, and D.J. Eakes. 1997b. Ozone
sensitivity of selected southeastern landscape plants. Journal of Environmental
Horticulture 15:51.
Fiscus, E.L., F.L. Booker, and K.O. Burkey. 2005. Crop responses to ozone: uptake, modes of
action, carbon assimilation and partitioning. Plant, Cell and Environment 28:997-1011.
Flowers, MD, EL Fiscus, KO Burkey, FL Booker and J-J Dubois. 2007. Photosynthesis,
chlorophyll fluorescence, and yield of snap bean (Phaseolus vulgaris L.) genotypes
differing in sensitivity to ozone. Environmental and Experimental Botany 61:190-198.
Gimeno, B.S., V. Bermejo, R.A. Reinert, Y. Zheng, and J.D. Barnes. 1999. Adverse effects of
ambient ozone on watermelon yield and physiology at a rural site in eastern Spain. New
Phytologist 144:245-260.
Harmens, H., G. Mills, F. Hayes, L. Jones, D. Norris, and J. Fuhrer. 2007. Air Pollution and
Vegetation: ICP Vegetation Annual Report 2006/2007 ISBN 987 1 85531 233 3. Centre
for Ecology and Hydrology, Bangor, UK.
Heagle, A.S. 1989. Ozone and crop yield. Annual Review of Phytopathology 27:397-423.
Heagle, A.S., J.E. Miller, B.I. Chevone, T.W. Dreschel, W.J. Manning, P.M. McCool, C.L.
Morrison, G.E. Neely, and J. Rebbeck. 1995. Response of a white clover indicator system
to tropospheric ozone at eight locations in the United States. Water, Air and Soil
Pollution 85:1373-1378.
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 Environment 14:103.
Kim, K.M., Y.S. Kwon, J.J. Lee, M.Y. Eun, and J.K. Sohn. 2004. QTL mapping and molecular
marker analysis for the resistance of rice to ozone. Molecules and Cells 17:151.
Kobayashi, K., M. Okada, and I. Nouchi. 1995. Effects of ozone on dry matter partitioning and
yield of Japanese cultivars of rice (Oryza sativa L.). Agriculture, Ecosystems &
Environment 53:109-122.
Krupa, S., R. Muntifering, and A. Chappelka. 2004. Effects of ozone on plant nutritive quality
characteristics for ruminant animals. The Botanica 54:1-12.
Krupa, S.V., M. Nosal, and A.H. Legge. 1994. Ambient ozone and crop loss: Establishing a
cause-effect relationship. Environmental Pollution 83:269-276.
Krupa, S.V., M. Nosal, and A.H. Legge. 1998a. A numerical analysis of the combined open-top
chamber data from the USA and Europe on ambient ozone and negative crop responses.
Environmental Pollution 101:157-160.
9
Krupa, S.V., A.E.G. Tonneijck, and W.J. Manning. 1998b. Ozone, p. 2-1 - 2-28., In R. B.
Flagler, ed. Recognition of Air Pollution Injury to Vegetation:A pictorial atlas. Air &
Waste Management Association, Pittsburgh.
Krupa, S.V., L. Grunhage, H.-J. Jager, M. Nosal, W.J. Manning, A.H. Legge, and K. Hanewald.
1995. Ambient ozone (O3) and adverse crop response: A unified view of cause and effect.
Environmental Pollution 87:119-126.
Lin, J.C., M. Nosal, R.B. Muntifering, and S.V. Krupa. 2007. Alfalfa nutritive quality for
ruminant livestock as influenced by ambient air quality in west-central Alberta.
Environmental Pollution 149:99-103.
Lin, J.C., K. Nadarajah, M. Volk, R.B. Muntifering and J. Fuhrer. 2007. Nutritive quality of a
species-rich, extensively managed pasture exposed to elevated ozone in a free-air
fumigation system. J. Anim. Sci. 90 (Suppl. 1): 36.
Long, S.P., E.A. Ainsworth, A.D.B. Leakey, J. Nosberger, and D.R. Ort. 2006. Food for thought:
Lower-than-expected crop yield stimulation with rising CO2 concentrations. Science
312:1918-1921.
Manning, W.J., and S.V. Krupa. 1992. Experimental methodology for studying the effects of
ozone on crops and trees, p. 93-156, In A. S. Lefohn, ed. Surface Level Ozone Exposures
and Their Effects on Vegetation. Lewis Publishers, Inc., Chelsea.
Miller, J.E., W.A. Pursley, and A.S. Heagle. 1994. Effects of ethylenediurea on snap bean at a
range of ozone concentrations. Journal of Environmental Quality 23:1082-1089.
Morgan, P.B., T.A. Mies, G.A. Bollero, R.L. Nelson, and S.P. Long. 2006. Season-long
elevation of ozone concentration to projected 2050 levels under fully open-air conditions
substantially decreases the growth and production of soybean. New Phytologist 170:333343.
Muntifering, R.B., D.D. Crosby, M.C. Powell, and A.H. Chappelka. 2000. Yield and quality
characteristics of bahiagrass (Paspalum notatum) exposed to ground-level ozone. Animal
Feed Science Technology 84:243-256.
Muntifering, R.B., A.H. Chappelka, J.C. Lin, D.F. Karnosky and G.L. Somers. 2006. Chemical
composition and digestibility of Trifolium exposed to elevated ozone and carbon dioxide
in a free-air (FACE) fumigation system. Functional Ecology 20:269.
Ollerenshaw, J.H., T. Lyons, and J.D. Barnes. 1999. Impacts of ozone on the growth and yield of
field-grown winter oilseed rape. Environmental Pollution 104:53-59.
Olszyk, D.M., A. Bytnerowicz, G. Kats, C. Reagan, S. Hake, T. Kerby, D. Millhouse, B.
Roberts, C. Anderson, and H. Lee. 1993. Plant and environment interactions - cotton
10
yield losses and ambient ozone concentrations in California San-Joaquin Valley. Journal
of Environmental Quality 22:602-611.
Pell, E.J., and N.S. Pearson. 1984. Ozone-induced reduction in quantity and quality of two potato
cultivars. Environmental Pollution 35:345-352.
Powell, M.C., R.B. Muntifering, J.C. Lin and A.H. Chappelka. 2003. Yield and quality of sericea
lespedeza (Lespedeza cuneata) and little bluestem (Schizachyrium scoparium) exposed to
ground-level ozone. Environ. Pollution 122: 313.
Prather, M., D. Ehhalt, F. Dentener, R. Derwent, E. Dlugokencky, E.A. Holland, I. Isaksen, J.
Katima, V. Kirchhoff, P. Matson, P. Midgley, and M. Wang. 2001. Atmospheric
chemistry and greenhouse gases, p. 239-287, In J. T. Houghton, et al., eds. Climate
Change 2001: The Scientific Basis. Contribution of Working Group I to the Third
Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge
University Press, Cambridge, UK.
Rawlings, J.O., V.M. Lesser, A.S. Heagle, and W.W. Heck. 1988. Alternative ozone dose
metrics to characterize ozone impact on crop yield loss. Journal of Environmental Quality
17:285-291.
Reid, C.D. and E.L. Fiscus. 2008. Elevated CO2 and O3 effects on rice. Global Change Biology
14: 60-76.
Synder, R.G., J.E. Simon, R.A. Reinert, M. Simini, and G.E. Wilcox. 1991. Effects of air quality
on growth, yield and quality of watermelon. HortScience 26:1045.
U.S., E.P.A. 1996. Air Quality Criteria for Ozone and Other Photochemical Oxidants. U.S. EPA
report no. EPA/600/P-93/004bF ed. U.S. Environmental Protection Agency, Office of Air
Quality Planning and Standards, Research Triangle Park, NC., Research Triangle Park.
U.S. EPA. 2006. Air Quality Criteria for Ozone and Related Photochemical Oxidants
EPA/600/R-05/004aF-cF. U.S. Environmental Protection Agency, Washington, D.C.
Vorne, V., K. Ojanperä, L. De Temmerman, M. Bindi, P. Högy, M.B. Jones, T. Lawson, and K.
Persson. 2002. Effects of elevated carbon dioxide and ozone on potato tuber quality in the
European multiple-site experiment 'CHIP-project'. European Journal of Agronomy
17:369-381.
Wang, X., and D.L. Mauzerall. 2004. Characterizing distributions of surface ozone and its
impact on grain production in China, Japan and South Korea: 1990 and 2020.
Atmospheric Environment 38:4383-4402.