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Growth Response to CO2 with Other Variables (Non-Ozone Air Pollutants) - Summary
Many are the studies that have examined the net effect of concomitant increases in the concentrations of atmospheric CO2 and ozone upon plant growth and development [see the several sub-headings listed under Ozone (Effects on Plants) in our Subject Index].  In this Summary, we review a few of the less numerous studies that have focused on the individual and joint effects of elevated CO2 and various non-ozone air pollutants on plant growth and development.

One non-ozone air pollutant that is particularly devastating is sulfur dioxide (SO2). As Izrael et al. (2002) describe it, SO2 "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 report that "total SO2 emission from the industrial areas of Russia comprised 5866.76 thousand tons, or 42.2% of the total emission of liquid and gaseous pollutants."  In quantifying the extent and severity of this phenomenon, they find that 1.3 million hectares of Russian forests have been adversely affected by SO2 pollution, further noting that total forest destruction occurs on 2-5% of that area, and that heavy, moderate and slight damage occur on 10-15%, 30-40% and 40-50% of it, respectively.

We report these results to indicate the seriousness of SO2 pollution for forest health and to highlight the fact that atmospheric CO2 enrichment can significantly alleviate SO2's adverse biological consequences.  Hallgren (1984), for example, demonstrated that a 300-ppm increase in the air's CO2 concentration stimulated the photosynthetic rate of Scots pines by 64% in unpolluted air, but by a larger 77% in air of abnormally high SO2 concentration, while a 600-ppm increase in the air's CO2 concentration stimulated photosynthetic rates in this important forest species by 85% in unpolluted air and by 110% in air of high SO2 concentration.  Likewise, in the case of agricultural species, Carlson (1983) found that a 900-ppm increase in the air's CO2 concentration boosted photosynthetic rates of soybeans by 87% in unpolluted air, but by whopping 715% in high-SO2 air.  Hence, there is reason to believe that the ongoing rise in the air's CO2 content may either totally counteract or significantly alleviate many of the adverse consequences of SO2 pollution, as the following more recent studies also demonstrate.

Deepak and Agrawal (2001) grew two cultivars of soybean (PK472 and Bragg) in open-top chambers maintained at atmospheric CO2 concentrations of 350 ppm (ambient) and 600 ppm (elevated) alone and in combination with ambient and elevated (with an extra 60 ppb) SO2.  They found that exposure to elevated SO2 significantly reduced every growth parameter studied, with total plant biomass and grain yield declining by approximately 18% in both cultivars.  On the other hand, elevated CO2 increased every growth parameter in both cultivars, enhancing total plant biomass and grain yield by averages of 30 and 34%, respectively.  Moreover, when the plants were simultaneously exposed to both elevated CO2 and elevated SO2, the negative effects of SO2 on the suite of growth parameters were completely ameliorated.  In fact, they were more than completely ameliorated, for the net biomass and yield responses to increased CO2 and SO2 together were not significantly different from those obtained under elevated CO2 alone.

In a similar study, but working with a different crop, Agrawal and Deepak (2003) grew two cultivars of wheat (M234 and HP1209) in open-top chambers maintained at atmospheric CO2 concentrations of 350 ppm (ambient) and 600 ppm (elevated) alone and in combination with ambient and elevated (with an extra 60 ppb) SO2.  They found that exposure to elevated CO2 increased photosynthetic rates by 58 and 48% in M234 and HP1209, respectively, while fumigation with elevated SO2 had no effect on rates of photosynthesis in either cultivar.  And when plants were grown in the combined treatment of elevated CO2 and elevated SO2, they still displayed photosynthetic rates that were 42 and 38% greater than those measured in the M234 and HP1209 control plants, respectively.

Wheat plants grown in elevated CO2 also displayed an approximate 20% reduction in stomatal conductance (which reduced transpirational water loss), while those grown in elevated SO2 exhibited an average increase of 15% (which increased transpirational water loss); and when exposed simultaneously to both gases, the plants still displayed an average 11% reduction in stomatal conductance.  This latter joint effect contributed to an approximate 32% increase in water-use efficiency, while the plants exposed to only elevated SO2 displayed an average decrease in water-use efficiency of 16%.  Last of all, exposure to elevated SO2 caused an average 13% decrease in foliar protein concentrations in both cultivars; but when they were also exposed to 600 ppm CO2, leaf protein levels dropped by only 3% in HP1209, while they actually increased by 4% in M234.

Taking advantage of a unique real-world situation, Grill et al. (2004) studied two species of oak trees (Quercus ilex and Q. pubescens) growing at double-to-triple ambient atmospheric CO2 concentrations near naturally-occurring CO2 springs in Tuscany, Italy, where the air also contained higher-than-normal concentrations of SO2 and H2S (another sulfur-based phytotoxic air pollutant, as per Schulte et al., 1999).  Specifically, they analyzed various properties of leaves and acorns growing on trees near the springs and on similar trees located some distance away in ambient-CO2 pollution-free air.  In addition, they examined several characteristics of seedlings they sprouted from acorns produced by the trees of the two environments; and they used chromosome stress tests "to investigate whether alterations in sulphur-regime have negative consequences for seedlings."

So what did they find?  The team of six scientists reported that "acorns from CO2 springs contained significantly higher sulphur concentrations than controls (0.67 vs. 0.47 mg g-1 dry weight in Q. ilex cotyledons and 1.10 vs. 0.80 in Q. pubescens)," indicative of the fact that the trees in the vicinity of the CO2-emitting springs were indeed significantly affected by the H2S- and SO2-enriched air emanating from them.  In addition, they found that Q. ilix seedlings grown from acorns produced by trees growing in the vicinity of the springs showed elevated rates of chromosomal aberrations in their root tips, suggestive of the presence of a permanent stress.  Nevertheless, as has been demonstrated by the results of several studies conducted on mature trees growing at these sites, the CO2-enriched air - even in the presence of significantly elevated concentrations of phytotoxic H2S and SO2 - tremendously enhanced the trees' photosynthetic prowess: by 26-69% (Blaschke et al., 2001), 36-77% (Stylinski et al., 2000), and a whopping 175-510% (Tognetti et al., 1998).

In another study conducted near CO2-emitting springs in central Italy, Schwanz and Polle (1998) measured still other leaf characteristics of the same oak species in order to determine the effects of elevated CO2 on their antioxidative systems.  They found that the naturally-CO2-enriched air decreased the activities of superoxide dismutase (which detoxifies highly reactive oxygen species), by 30 to 47%, compared to activities measured in leaves of trees growing some distance away from the springs.  Trees of both species growing near the springs also exhibited lower activities of catalase and other enzymes involved in the degradation of hydrogen peroxide (H2O2), which is produced during photorespiration.  They thus concluded that atmospheric CO2 enrichment generally decreases the activities of protective enzymes that reduce oxidative stress brought about by unfavorable environmental conditions, such as the presence of noxious air pollutants, because they are not needed to as great a degree by plants growing in CO2-enriched air.

To be confident of this conclusion, and to rule out the possibility that the CO2-induced decreases in the antioxidative machinery of the CO2-enriched trees might actually have increased their susceptibility to oxidative damage, Schwanz and Polle also evaluated the degree of lipid peroxidation within the trees' leaves.  This work revealed that the trees growing near the CO2-emitting springs did indeed not display increased levels of this phenomenon within their leaves; and in some cases, they actually exhibited significant reductions in lipid peroxidation.  Consequently, as the CO2 content of the air continues to rise, we can expect that these particular species of oak tree, as well as many other species of plants, will likely experience a significant amelioration of the deleterious effects of various environmental stresses, particularly those arising from air pollution, as has also been documented by the major reviews of Idso and Idso (1994) and Poorter and Perez-Soba (2001).

References
Agrawal, M. and Deepak, S.S.  2003.  Physiological and biochemical responses of two cultivars of wheat to elevated levels of CO2 and SO2, singly and in combination.  Environmental Pollution 121: 189-197.

Blaschke, L., Schulte, M., Raschi, A., Slee, N., Rennenberg, H. and Polle, A.  2001.  Photosynthesis, soluble and structural carbon compounds in two Mediterranean oak species (Quercus pubescens and Q. ilex) after lifetime growth at naturally elevated CO2 concentrations.  Plant Biology 3: 288-297.

Carlson, R.W.  1983.  The effect of SO2 on photosynthesis and leaf resistance at varying concentrations of CO2Environmental Pollution Series A 30: 309-321.

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.

Grill, D., Muller, M., Tausz, M. Strnad, B., Wonisch, A. and Raschi, A.  2004.  Effects of sulphurous gases in two CO2 springs on total sulphur and thiols in acorns and oak seedlings.  Atmospheric Environment 38: 3775-3780.

Hallgren, J.-E.  1984.  Photosynthetic gas exchange in leaves affected by air pollutants.  In: Koziol, M.J. and Whatley, F.R.  (Eds.).  Gaseous Air Pollutants and Plant Metabolism.  Butterworths, London, UK, pp. 147-159.

Idso, K.E. and Idso, S.B.  1994.  Plant responses to atmospheric CO2 enrichment in the face of environmental constraints: A review of the past 10 years' research.  Agricultural and Forest Meteorology 69: 153-203.

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.

Poorter, H. and Perez-Soba, M.  2001.  The growth response of plants to elevated CO2 under non-optimal environmental conditions.  Oecologia 129: 1-20.

Schulte, M., Raiesi, F.G., Papke, H., Butterbach-Bahl, K., van Breemen, N. and Rennenberg, H.  1999.  CO2 concentration and atmospheric trace gas mixing ratio around natural CO2 vents in different Mediterranean forests in central Italy.  In: Raschi, A., Vaccori, F.P. and Miglietta, F.  (Eds.).  Ecosystem Response to CO2: The Maple Project Results.  European Communities, Brussels, Belgium, pp. 168-188.

Schwanz, P. and Polle, A.  1998.  Antioxidative systems, pigment and protein contents in leaves of adult mediterranean oak species (Quercus pubescens and Q. ilex) with lifetime exposure to elevated CO2New Phytologist 140: 411-423.

Stylinski, C.D., Oechel, W.C., Gamon, J.A., Tissue, D.T., Miglietta, F. and Raschi, A.  2000.  Effects of lifelong [CO2] enrichment on carboxylation and light utilization of Quercus pubescens Willd. examined with gas exchange, biochemistry and optical techniques.  Plant, Cell and Environment 23: 1353-1362.

Tognetti,R., Johnson, J.D., Michelozzi, M. and Raschi, A.  1998.  Response of foliar metabolism in mature trees of Quercus pubescens and Quercus ilex to long-term elevated CO2Environmental and Experimental Botany 39: 233-245.