That the findings of Wang and Mauzerall are indeed "conservative," is demonstrated by the work of Wahid et al. (2001), who in a study of the effects of ozone pollution in the Punjab region of Pakistan periodically applied a powerful ozone protectant to soybeans growing in three different locations in the general vicinity of the city of Lahore - a suburban site, a remote rural site, and a rural roadside site - throughout two different growing seasons (one immediately post-monsoon and one the following spring or pre-monsoon).  The results of this treatment were truly astounding.  At the suburban site, application of the ozone protectant increased the weight of soybean seeds produced per plant by 47% in the post-monsoon season and by 113% in the pre-monsoon season.  At the remote rural site, the corresponding yield increases were 94% and 182%, while at the rural roadside site, they were 170% and 285%.  Averaged across all three sites and both seasons of the year, the mean increase in yield caused by countering the deleterious effects of this major air pollutant was nearly 150%; and due to their finding that "the impacts of ozone on the yield of soybean are larger in the rural areas around Lahore than in suburban areas of the city," they concluded "there may be substantial impacts of oxidants on crop yield across large areas of the Punjab."

In light of the observations of Wahid et al. and those of Wang and Mauzerall, it is clear that whatever could be done to reduce these massive O3-induced crop losses - or, ideally, eliminate them altogether - would be a godsend to the people of nearly all parts of the planet.  So the next thing to ask is What can rising atmospheric CO2 concentrations do to alleviate the problem?  We here briefly summarize the findings of a number of studies we have reviewed on our website that have addressed this question.

Miller et al. (1998) grew soybeans for one season in pots within open-top chambers maintained at atmospheric CO2 concentrations of 370, 482, 599 and 713 ppm in combination with atmospheric O3 concentrations of 20, 50 and 79 ppb.  By harvest time (113 days after planting), elevated CO2 had significantly increased all biomass and growth variables measured, with the greatest percentage enhancements occurring at the highest CO2 and O3 concentrations.  Plants grown at 20 ppb O3 and 713 ppm CO2, for example, displayed total dry weights that were 48% greater than their ambient-air-grown counterparts, while plants grown at 79 ppb O3 and 713 ppm CO2 exhibited dry weights that were 53% greater than their ambient-air counterparts.  Likewise, in the same experiment, Heagle et al. (1998) found that plants grown at 20 ppb O3 and 713 ppm CO2 displayed seed dry weights that were 20% greater than their ambient-air-grown counterparts, while plants grown at 79 ppb O3 and 713 ppm CO2 exhibited seed dry weights that were 74% greater than their ambient-air counterparts.

In a similar study, Reid et al. (1998) grew soybeans in open-top chambers maintained at atmospheric CO2 concentrations of 371 and 708 ppm and O3 concentrations of 24 and 81 ppb.  In the ambient-CO2 air, elevated O3 exposure reduced the amount and activity of rubisco per unit leaf area, as well as leaf starch content.  In the elevated-CO2 air, on the other hand, elevated O3 exposure had no effect on these three leaf parameters, demonstrating a total amelioration of potential O3-induced damage by atmospheric CO2 enrichment.

In another such study, Reid and Fiscus (1998) grew soybeans for a single season in pots placed within open-top chambers maintained at either ambient (365 ppm) or elevated (727 ppm) concentrations of atmospheric CO2 and below-ambient (20 ppb) or 1.5 times ambient (74 ppb) levels of ozone.  In doing so, they found that elevated CO2 enhanced rates of photosynthesis in the presence or absence of ozone and typically ameliorated the negative effects of ozone on carbon assimilation.

In a literature review of O3 and CO2 effects on soybean photosynthesis, growth and yield, Morgan et al. (2003) state that "meta-analytic techniques were used to quantitatively summarize the response of soybean to an average, chronic ozone exposure of 70 ppb, from 53 peer-reviewed studies," after which the net effect of concurrently elevated O3 and CO2 (to unspecified concentrations described as being "above 400 ppm") was similarly derived.  They report finding that "when both O3 and CO2 are elevated, the mean decrease in photosynthesis is 7%," which "compares to a 20% loss for plants grown at elevated O3 and the current ambient CO2."  They also report that "at maturity, the average shoot biomass was decreased 34% and seed yield was 24% lower" in response to elevated O3 alone; but they note that "seed yield decreases for plants grown in elevated O3 and elevated CO2 are only half of those for plants grown in current ambient CO2 and elevated O3."  Last of all, they note "there were significant ozone responses in several plant parameters at low daily average concentrations (less than 60 ppb)," which is less than current concentrations in many locations.  In fact, they report that in studies where the O3 treatment average was less than 60 ppb, "seed yield, shoot and root dry weight were all significantly decreased by about 10%," which suggests that in these circumstances the degree of atmospheric CO2 enrichment employed in the joint O3/CO2 experiments likely would have completely eradicated the O3-induced losses in plant production.

That this conclusion is indeed robust is suggested by the findings of Booker et al. (2005a), who grew well watered and fertilized soybeans from seeds that were sown either directly in the ground or in 15-liter pots out-of-doors in open-top chambers maintained at all combinations of low (24 ppb) or high (75 ppb) O3 concentrations and ambient (373 ppm) or elevated (699 ppm) CO2 concentrations in 1999, and in 21-liter pots maintained at all combinations of low (24 ppb) or high (75 ppb) O3 concentrations and ambient (369 ppm) or elevated (717 ppm) CO2 concentrations in 2000.  In 1999, in the pot-grown plants, the 212% increase in atmospheric O3 concentration decreased net photosynthesis by approximately 21%; but when the air's CO2 concentration was simultaneously boosted by 87%, the negative impact of the O3 increase was more than ameliorated, with the result that the plants exposed to elevated concentrations of both trace gases exhibited net photosynthesis rates that were 26% greater than those exhibited by the plants growing in low O3 and CO2 air.  Likewise, in the ground-grown plants, the 212% increase in atmospheric O3 concentration decreased net photosynthesis by approximately 14%; but when the air's CO2 concentration was simultaneously boosted by 87%, the negative impact of the O3 increase was again more than ameliorated, with the result that the plants exposed to elevated concentrations of both trace gases exhibited net photosynthesis rates that were 40% greater than those exhibited by the plants growing in low O3 and CO2 air.

With respect to seed yield in 1999, in the pot-grown plants the 212% increase in atmospheric O3 concentration decreased total seed biomass by approximately 27%; but when the air's CO2 concentration was simultaneously boosted by 87%, the negative impact of the O3 increase was also more than ameliorated, with the result that the plants exposed to elevated concentrations of both trace gases produced 15% more total seed biomass than the plants growing in low O3 and CO2 air.  Likewise, in the ground-grown plants, the 212% increase in atmospheric O3 concentration decreased total seed biomass by approximately 24%; but when the air's CO2 concentration was simultaneously boosted by 87%, the negative impact of the O3 increase was once again more than ameliorated, with the result that the plants exposed to elevated concentrations of both trace gases produced 15% more total seed biomass than the plants growing in low O3 and CO2 air.

Last of all, with respect to seed yield in 2000, in the pot-grown plants the 212% increase in atmospheric O3 concentration decreased total seed biomass by approximately 41%; but when the air's CO2 concentration was simultaneously boosted by 94%, the negative impact of the O3 increase was yet again more than ameliorated, with the result that the plants exposed to elevated concentrations of both trace gases produced 18% more total seed biomass than the plants growing in low O3 and CO2 air.  Likewise, in the ground-grown plants, the 212% increase in atmospheric O3 concentration decreased total seed biomass by approximately 39%; but when the air's CO2 concentration was simultaneously boosted by 94%, the negative impact of the O3 increase was also yet again more than ameliorated, with the result that the plants exposed to elevated concentrations of both trace gases produced 9% more total seed biomass than the plants growing in low O3 and CO2 air.  Consequently, in all of the many situations investigated in this comprehensive study, slightly less than a doubling of the air's CO2 concentration more than compensated for the deleterious effects of slightly more than a tripling of the air's O3 concentration on both leaf net photosynthesis and total seed biomass production in soybeans.

In a similar two-year open-top chamber study of aboveground postharvest reside, Booker et al. (2005b) grew soybeans in reciprocal combinations of low and high atmospheric concentrations of O3 (21 and 74 ppb, respectively) and CO2 (370 and 714 ppm, respectively), finding that residue mass input "is increased by elevated CO2 and suppressed by O3."  More specifically, they report that elevated O3 decreased aboveground postharvest residue by 15-46%, while elevated CO2 increased it by 28-56%; and in combination, the CO2 effect always predominated.  In the case of leaves, for example, elevating the air's O3 concentration dropped dry mass residue to only 54% of what it was under ambient conditions, while concurrently elevating the air's CO2 concentration boosted it to 124% of what it was in ambient air.  Corresponding results of 85% and 123% were obtained for petioles, 60% and 121% for stems, and 72% and 122% for husks.  Consequently, as in the cases of net photosynthesis and seed yield investigated by Booker et al. (2005a), the results of this study demonstrated that slightly less than a doubling of the air's CO2 concentration more than compensated for the deleterious effects of slightly more than a tripling of the air's O3 concentration on the production of aboveground postharvest residue in soybeans.

Rounding out our review of O3 effects on soybeans, we report the results of Booker and Fiscus (2005), who grew well watered and fertilized plants for two years (1998 and 1999) out-of-doors in 21-liter pots in open-top chambers from emergence to maturity while they were exposed to either charcoal-filtered air, or charcoal-filtered air plus an extra 336 ppm CO2, or charcoal-filtered air plus 1.5 times normal ambient O3, or charcoal-filtered air plus an extra 336 ppm CO2 and 1.5 times normal ambient O3.  Using this protocol, they determined that the imposition of elevated CO2 alone increased soybean pod biomass by 23.0%, the imposition of elevated O3 alone decreased pod biomass by 13.3%, while the imposition of elevated CO2 and O3 together increased pod biomass by 23.0%.  In thinking about these results, if one first considers the negative effect of elevated ozone, adding extra CO2 is seen to more than completely ameliorate ozone's negative effect on pod biomass.  If, on the other hand, one first considers the positive effect of elevated CO2, adding ozone is seen to have absolutely no effect on CO2's positive effect.  Consequently, it can be appreciated that the positive effect of elevated CO2 in this study was vastly superior to the negative effect of elevated ozone.  In fact, it totally dominated.

Finally, we come to a consideration of sulfur dioxide (SO2), which in the words of Izrael et al. (2002) "causes widespread damage to plants, because it can spread through large distances, and its emissions into the atmosphere are large."  In 1996, for example, they say that "total SO2 emission from the industrial areas of Russia comprised ... 42.2% of the total emission of liquid and gaseous pollutants," and in quantifying the extent and severity of this phenomenon, they found that 1.3 million hectares of Russian forest land have been adversely affected by SO2 pollution, noting that total forest destruction occurs on 2-5% of this area, and that heavy, moderate and slight damage occur on 10-15%, 30-40% and 40-50% of it, respectively.  As for the ability of atmospheric CO2 enrichment to counter the huge negative impact of SO2 pollution, we note that in the case of soybeans, Carlson (1983) found that a 900-ppm increase in the air's CO2 concentration boosted photosynthetic rates by 87% in unpolluted air but by a whopping 715% in high-SO2 air, suggesting that as with ozone, the ongoing rise in the air's CO2 content can do much to either totally prevent or significantly alleviate the adverse consequences of SO2 pollution.

In a more recent study that directly demonstrates this fact, Deepak and Agrawal (2001) grew two soybean cultivars in open-top chambers maintained at atmospheric CO2 concentrations of 350 and 600 ppm alone and in combination with elevated (to 60 ppb) SO2.  In doing so, they found that exposure to elevated SO2 significantly reduced every growth parameter studied, with total plant biomass and grain yield being reduced by approximately 18% in both cultivars.  In contrast, elevated CO2 significantly increased every growth parameter in both cultivars, with total plant biomass and grain yield being increased by 30 and 34%, respectively.  Moreover, when the plants were exposed simultaneously to elevated CO2 and SO2, the negative effects of SO2 on these growth parameters were completely ameliorated.  In fact, their observed values were not significantly different from those obtained under CO2-enriched conditions alone.

In conclusion, the high ozone and sulfur dioxide concentrations of today, as well as the even higher concentrations that will exist in many parts of the world in years to come, have and will have severe negative consequences for soybean production, all else being equal.  However, the atmosphere's current high CO2 concentration, plus the higher concentration it will have in the future, has and will have an important ameliorative effect on the adverse impacts of these two major air pollutants.  In fact, current and anticipated concentrations of CO2 may well compensate, or even more than compensate, for the full extent of the potential negative consequences of both elevated O3 and SO2.

References
Booker, F.L. and Fiscus, E.L.  2005.  The role of ozone flux and antioxidants in the suppression of ozone injury by elevated CO2 in soybean.  Journal of Experimental Botany 56: 2139-2151.

Booker, F.L., Miller, J.E., Fiscus, E.L., Pursley, W.A. and Stefanski, L.A.  2005a.  Comparative responses of container- versus ground-grown soybean to elevated carbon dioxide and ozone.  Crop Science 45: 883-895.

Booker, F.L., Prior, S.A., Torbert, H.A., Fiscus, E.L., Pursley, W.A. and Hu, S.  2005b.  Decomposition of soybean grown under elevated concentrations of CO2 and O3.  Global Change Biology 11: 685-698.

Deepak, S.S. and Agrawal, M.  2001.  Influence of elevated CO2 on the sensitivity of two soybean cultivars to sulphur dioxide.  Environmental and Experimental Botany 46: 81-91.

Heagle, A.S., Miller, J.E. and Pursley, W.A.  1998.  Influence of ozone stress on soybean response to carbon dioxide enrichment: III. Yield and seed quality.  Crop Science 38: 128-134.

Izrael, Yu.A., Gytarsky, M.L., Karaban, R.T., Lelyakin, A.L. and Nazarov, I.M.  2002.  Consequences of climate change for forestry and carbon dioxide sink in Russian forests.  Isvestiya, Atmospheric and Oceanic Physics 38: S84-S98.

Miller, J.E., Heagle, A.S. and Pursley, W.A.  1998.  Influence of ozone stress on soybean response to carbon dioxide enrichment: II. Biomass and development.  Crop Science 38: 122-128.

Morgan, P.B., Ainsworth, E.A. and Long, S.P.  2003.  How does elevated ozone impact soybean? A meta-analysis of photosynthesis, growth and yield.  Plant, Cell and Environment 26: 1317-1328.

Reid, C.D. and Fiscus, E.L.  1998.  Effects of elevated [CO2] and/or ozone on limitations to CO2 assimilation in soybean (Glycine max).  Journal of Experimental Botany 18: 885-895.

Reid, C.D., Fiscus, E.L. and Burkey, K.O.  1998.  Combined effects of chronic ozone and elevated CO2 on rubisco activity and leaf components in soybean (Glycine max).  Journal of Experimental Botany 49: 1999-2011.

Wahid, A., Milne, E., Shamsi, S.R.A., Ashmore, M.R., and Marshall, F.M.  2001.  Effects of oxidants on soybean growth and yield in the Pakistan Punjab.  Environmental Pollution 113: 271-280.

Wang, X. and Mauzerall, D.L.  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.