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Growth Response to CO2 with Other Variables (Ozone: Miscellaneous Trees) -- Summary
Ozone (O3) is the primary air pollutant responsible for visible foliar injury and reduced growth in trees the world over. Most studies of the subject suggest it gains entrance to leaves through their stomata, whereupon it interferes with the process of photosynthesis and thereby reduces plant productivity. The global significance of the phenomenon was described in some detail by Fowler et al. (1999), who estimated O3 to have been negatively impacting a full quarter of earth's forests at the close of the 20th century, and who calculated it to have the potential to negatively impact fully one-half of the planet's forests by 2100.

So what effect has this phenomenon had on earth's trees since the inception of the Industrial Revolution? And what will its likely impact be over the course of the current century?

In one of the earlier studies of the subject, Kainulainen et al. (1998) constructed open-top chambers around Scots pine (Pinus sylvestris L.) trees that were about 20 years old and fumigated them with combinations of ambient or CO2-enriched air (645 ppm) and ambient or twice-ambient (20 to 40 ppb) ozone-enriched air for three growing seasons, in order to study the interactive effects of these two vastly different gases on starch and secondary metabolite production. In doing so, they discovered that elevated CO2 and O3 (ozone) had no significant impact on the trees' starch production, even after two years of treatment exposure. However, near the end of the third year, elevated CO2 alone significantly enhanced starch production in current-year needles. But neither elevated CO2 nor O3, acting alone or together, had any significant effects on the concentrations of the secondary metabolites they investigated.

This paper thus showed the need for long-term studies when investigating tree responses to atmospheric CO2 enrichment. Whereas no effects of elevated CO2 on starch production were found after two years of treatment exposure, starch concentrations in needles ultimately increased significantly in the CO2-enriched trees late into the third year of the study. Thus, long-lived perennial plants, such as trees, clearly require long-term CO2-enrichment studies to reveal how they will respond to the rising concentration of atmospheric CO2. With respect to Scots pine trees, this study thus suggests that the species may indeed display long-term increases in starch concentration in response to the rising CO2 content of the air, which can be mobilized to provide carbohydrates for active plant sinks to increase total tree size and biomass. In addition, if ozone continues to accumulate in the lower atmosphere, Scots pine may still not display any adverse response to it, as atmospheric CO2 enrichment seems to be able to protect against O3-induced harm.

Also prior to the turn of the century, Broadmeadow et al. (1999) performed several experiments on young trees, including sessile oak (Quercus petraea), European beech (Fagus sylvatica), and sweet chestnut (Castanea sativa), in order to determine how their responses to ozone exposure are affected by elevated CO2 and other environmental variables. This work revealed that elevated CO2 generally reduced the amount of ozone damage done to plants by inducing various degrees of stomatal closure, which thereby decreased the incidental uptake of this harmful air pollutant. Thus, this study also suggested that as the air's CO2 concentration continues to rise, many different tree species will likely exhibit reductions in stomatal conductance, which should reduce the negative effects of tropospheric ozone on their growth and development.

A couple years later, Herman et al. (2001) noted that air pollution by SO2, Pb, NOx and NH3 had been significantly reduced in central Europe over the prior two decades, but that ozone concentrations there were still on the rise, based on trends derived from European databases that included ozone measurements from about 100 stations in Austria and Germany. The parameter Herman et al. used to express the significance of these ozone trends was the AOT40 Critical Level set by the UN-ECE (1994), which had a value of 10 ppm.h and which was defined as accumulated ozone exposure above a threshold of 40 ppb 24 hours per day over the six-month growing season of April-September, which in controlled experiments had been documented to cause approximate 10% reductions in tree biomass production.

So just how bad had the ozone pollution become in central Europe? In most of the grid plots of the Austrian Forest Inventory Grid, and based on 1993 ozone data, Herman et al. reported that "the Critical Level of 10 ppm.h had been exceeded up to sevenfold," which led them to state that "where standards had been exceeded to such an alarming extent, serious damage of forest trees should be expected."

So what did the trees in these highly-ozone-polluted grid plots look like? Were they absolutely devastated? Or maybe even dead? In the words of Herman et al., "the results of the Austrian monitoring surveys did not reflect such damage." They noted, for example, that "neither the general evaluation of the foliage losses in the context of the crown condition inventories nor the development of the growing stock reflect a dramatic situation." In fact, they stated that not only were there no "dramatic" reductions in tree health and productivity, there were typically none at all; and in many areas there were actually improvements, such as crown conditions in Austria looking slightly better and the growing stock increasing.

Continuing, Herman et al. acknowledged that although ozone-related losses of biomass could not be confirmed on old trees, under the ozone levels of that day they did show some reductions in photosynthetic CO2 uptake. This phenomenon was particularly evident in old trees at high altitudes, where AOT40 values were much more extreme, and in trees that were experiencing "additional climatic stress." But the researchers were careful to add that "the reductions of the CO2 uptake were in no proportion to the massive excess of the AOT40."

What is one to conclude from these dichotomous observations? Ozone exposures more than sevenfold greater than the Critical Level (which Critical Level alone should have decreased tree productivity by 10%) were occurring all across the Austrian Forest Inventory Grid; and such conditions could well have been expected to reduce the growth rates of the exposed trees by fully 70% or more. Yet there was no evidence of any widespread damage or productivity reduction. In fact, growth conditions seemed to have improved almost everywhere, except at high altitudes and under conditions of more-than-usual climatic stress.

Herman et al. thus suggested that these observations implied that the once-adequate Critical Level of ozone exposure was no longer suitable for application. And why? They provided the answer by correctly stating that "the significant parameter for the assessment of the risk" is not the atmospheric concentration of ozone, but "the absorbed dose." Hence, they advised the creation of a new Critical Level that "takes into account leaf conductance and the environmental parameters influencing it."

This latter statement is a reasonable rendering of what should be the proper approach to the issue, for there are many concurrent and ongoing changes in earth's atmosphere, and the net result of all of them acting in unison must be considered in predicting the consequences of changes in any individual factor. In the case of earth's climate, for example, the surface air temperature consequences of an increase in the air's CO2 content cannot be adequately evaluated without considering the effects of concurrent changes in atmospheric aerosol quantities and properties. Likewise, in the case of forest health, the biological consequences of rising tropospheric ozone concentrations cannot be adequately evaluated without considering the effects of the concurrent and ongoing rise in the air's CO2 content, which is known to have a significant impact on leaf conductance and, hence, largely determines a tree's critical "absorbed dose" of ozone. And when this more rational approach has been followed, it has been shown in numerous laboratory and field experiments that realistically-scaled concurrent increases in atmospheric CO2 and ozone concentrations typically lead to very little change in plant net productivity. And, therefore, it is logical to conclude that the lack of substantial negative ozone-induced impacts on the forests of central Europe, as described by Herman et al., may well have been the result of the compensatory beneficial impacts of the historical and still-ongoing rise in the air's CO2 content.

Four years later, King et al. (2005) noted that pre-industrial concentrations of tropospheric O3 were estimated to have been less than 10 ppb, but to have subsequently risen to the 30-40 ppb background levels of their day, referencing Levy et al. (1997). In addition, they indicated that the rising boundary-layer O3 concentration caused by increasing industrialization around the globe had had negative continent-scale implications for carbon sequestration for some time (Felzer et al., 2004). Hence, they felt a need to evaluate the net effect of the positive CO2 and negative O3 impacts of possible future increases in these trace atmospheric gases on the productivity of the most widespread tree species found in North America, i.e., trembling aspen (Populus tremuloides Michx.), as well as two-member mixed communities of trembling aspen-paper birch (Betula papyrifera Marsh.) and trembling aspen-sugar maple (Acer saccharum Marsh.).

This work was carried out at the Aspen FACE site (Dickson et al., 2000) near Rhinelander, Wisconsin, USA, where pure stands of aspen and mixed stands of aspen-birch and aspen-maple were allowed to grow for seven years in either ambient air or air enriched with an extra 200 ppm of CO2 or air enriched with an extra 50% O3 or air thus enriched by both CO2 and O3, after which the eight researchers evaluated the effects of CO2 enrichment alone, O3 enrichment alone, and the net effect of both CO2 and O3 enrichment together on the growth of the trees. And in so doing, they found that relative to the ambient-air control treatment, elevated CO2 "increased total biomass 25, 45 and 60% in the aspen, aspen-birch and aspen-maple communities, respectively, while elevated O3 caused 23, 13 and 14% reductions in total biomass relative to the control in the respective communities. Of most interest of all, however, the combination of elevated CO2 and O3 "resulted in total biomass responses of -7.8, +8.4 and +24.3% relative to the control in the aspen, aspen-birch and aspen-sugar maple communities, respectively."

King et al. thus concluded from the results of their study that "exposure to even moderate levels of O3 significantly reduces the capacity of net primary productivity to respond to elevated CO2 in some forests." And they therefore suggested that it makes sense to develop technologies that reduce anthropogenic precursors to photochemical O3 formation, because the implementation of such a policy would decrease an important constraint on the degree to which forest ecosystems can positively respond to the ongoing rise in the air's CO2 concentration.

Working concurrently, Gardner et al. (2005) grew pre-flushed hardwood stem cuttings of the inter-American (Populus trichocarpa Torr. & Gray ex Hook. x P. deltoides Bartr. ex Marsh) hybrid poplar clone 'Boelare' out-of-doors in eight open-top chambers for two growing seasons of 132 and 186 days (first and second years, respectively), during which time they measured a number of plant properties and physiological processes. Two of the eight chambers were maintained at ambient carbon dioxide (350 ppm) and ozone concentrations (A), two at ambient CO2 with daily O3 episodes rising to a mid-day peak of 100 ppb (AO), two at elevated CO2 (700 ppm) and ambient O3 (E), and two at elevated CO2 and O3 (EO) throughout the first year of the study, while only CO2 was elevated during the second year.

With respect to the effect of CO2 alone, Gardner et al. found that mainstem dry weight "was increased by 38% in 700-ppm CO2 compared with that in 350-ppm CO2 at the end of the first growing season," and that "during year 2 mainstem dry weight increased by about 5-fold and the relative effect of elevated CO2 remained similar in magnitude (32%) to that seen in the first year." They also report that during the first season of exposure, mainstem dry mass was decreased by 45% in the O3-episode treatment in 350-ppm CO2, but by only 34% in the O3-episode treatment in 700-ppm CO2; and because of the strong growth-promoting effect of the extra CO2, the O3-induced change in growth when going from the ambient-CO2-ambient-O3 treatment to the elevated-CO2-elevated-O3 treatment was only a reduction of 10%, as compared to the O3-induced reduction of 45% when CO2 was not increased concurrently. And in light of these findings, the British researchers concluded that "elevated levels of CO2 can play a key role in ameliorating the worst effects of severe ozone episodes on a relatively sensitive tree species," and that "O3 episodes are less likely to be detrimental to P. trichocarpa x P. deltoides in the CO2 concentrations of the future."

Noting that the "detrimental effects of ozone on plants are well known" and that "CO2 generally affects trees in opposite ways to ozone," Valkama et al. (2007) conducted a literature review that they described as "the first quantitative analysis of the interactive effects of elevated O3 and elevated CO2 on tree chemistry and herbivore performance," based on the results of 63 studies conducted on 22 tree species and 10 insect herbivore species that were published between 1990 and 2005. This detective work revealed that with respect to the ways by which elevated O3 may benefit insect herbivores that tend to damage trees, Valkama et al. determined that "elevated O3 significantly shortened development time of insect herbivores [when they are exposed and vulnerable to attack by various enemies] and increased their pupal mass in the overall dataset." In addition, they found that the "relative growth rate of chewers was significantly increased by 3.5% under elevated O3." However, they discovered that "these effects were counteracted by elevated CO2," such that "elevated O3 in combination with CO2 had no effect on herbivore performance," with the exception that when elevated CO2 was added to the O3-enriched air, it not only counteracted the O3-induced increase in pupal biomass, it actually reduced it below what it was in ambient air by 7%. And this analysis of the vast majority of pertinent experimental data obtained prior to 2006 suggests that in the never-ending battle between insect herbivores and the trees on whose foliage they feast, the ongoing rise in the air's CO2 content likely plays an extremely important role in negating, and in some cases even more than negating, the damage otherwise capable of being done to earth's forests by voracious insect pests.

Also publishing an important paper about this same time were Wittig et al. (2007), who calculated that the increase in the atmosphere's O3 concentration since the start of the Industrial Revolution had caused a mean decrease of 11% in the leaf photosynthetic CO2 uptake of earth's temperate and boreal forests. In addition, based on projections derived from the A2 storyline of the Special Report on Emissions Scenarios included in IPCC Assessment Report Four (which indicate that atmospheric O3 concentrations could rise 20-25% between 2015 and 2050, and that they could further increase by 40-60% by 2100 if current emission trends continue), they calculated that temperate and boreal forest photosynthetic rates could decline by an additional 8-16% by the end of the century.

Fortunately, the stomatal-aperture-constricting effect of concomitant past increases and anticipated future increases in the air's CO2 content tend to counter the negative influence of rising O3 concentrations by retarding O3 entry into plant leaves. In addition, the CO2-induced increase in leaf photosynthesis (its "aerial fertilization effect") has been shown to often more than compensate for the negative influence of ozone on leaf photosynthesis rates. Furthermore, these welcome findings comprise only half of the good news about rising CO2 concentrations and their impact on the ozone problem, as is described in what follows.

First of all, it is a well-established fact that vegetative isoprene emissions are responsible for the production of vast amounts of tropospheric ozone (Chameides et al., 1988; Harley et al., 1999). In fact, it has been calculated by Poisson et al. (2000) that current levels of non-methane hydrocarbon (NMHC) emissions (the vast majority of which are isoprene, accounting for more than twice as much as all other NMHCs combined) likely increase surface ozone concentrations from what they would be in their absence by up to 50-60% over land. In addition, although little appreciated, it has been known for some time that atmospheric CO2 enrichment typically leads to large reductions in isoprene emissions from plants; yet this phenomenon has typically not been factored into projections of future atmospheric O3 concentrations.

This glaring omission was addressed by Arneth et al. (2007), who noted that future vegetative isoprene emissions had typically been modeled to rise in tandem with projected increases in vegetative biomass and productivity (driven by projected changes in various environmental factors), which protocol, in an anticipated warmer and CO2-enriched world of the future, had generally led to predictions of significant increases in isoprene emissions and, therefore, significant increases in future atmospheric O3 concentrations, as had been anticipated to occur by Wittig et al. However, Arneth et al. convincingly demonstrated that "a quite different result is obtained when the direct CO2 effect on isoprene emissions is included," noting that in this more realistic situation a properly-forced model "maintains global isoprene emissions within 15% of present values."

In light of these important findings, the team of seven Swedish and UK researchers correctly concluded that "predictions of high future tropospheric O3 concentrations partly driven by isoprene emissions may need to be revised." And for a no-net-change in vegetative isoprene emissions between now and the end of the current century, the fears of Wittig et al. should fail to materialize. In fact, just the opposite should occur.

Most recently, Xu et al. (2012) have noted that "levels of atmospheric CO2 and O3 have increased rapidly in the last five decades," and they say that "it is predicted that at the end of this century, the average levels of CO2 and O3 in the Earth's atmosphere are going to reach 700 ppm and 80 ppb, respectively (IPCC, 2007)." Thus, in an experiment designed to evaluate the opposing effects of these two atmospheric trace gases on Chinese pine (Pinus tabulaeformis) trees at the year AD 2100, they grew four-year-old trees in loamy soil with no extra fertilizer within twelve open-top chambers in May 2006 within the populated central area of Shenyang city in northeastern China, where the trees were exposed to either current ambient air of about 400 ppm CO2 and 40 ppb O3 or 700 ppm CO2 and 80 ppm O3, plus all combinations thereof.

This study revealed that elevated CO2 by itself "did not significantly affect net photosynthetic rate, stomatal conductance, chlorophyll content, the maximum quantum yield of photosystem II, or the effective quantum yield of photosystem II electron transport after 90 days of gas exposure." However, it increased growth. Elevated O3 by itself, on the other hand, "decreased growth, net photosynthetic rate and stomatal conductance after 90 days of exposure," but Xu et al. say that "its negative effects were alleviated by elevated CO2." And these findings suggest a huge win for CO2 in its battle with O3 to impact the growth and development of Chinese pine trees.

In summation, therefore, it would appear from the host of discoveries described above that the positive effects of atmospheric CO2 enrichment more than compensate for whatever negative effects concomitant elevated ozone concentrations may have on the growth of earth's many tree species.

References
Arneth, A., Miller, P.A., Scholze, M., Hickler, T., Schurgers, G., Smith, B. and Prentice, I.C. 2007. CO2 inhibition of global terrestrial isoprene emissions: Potential implications for atmospheric chemistry. Geophysical Research Letters 34: 10.1029/2007GL030615.

Broadmeadow, M.S.J., Heath, J. and Randle, T.J. 1999. Environmental limitations to O3 uptake - Some key results from young trees growing at elevated CO2 concentrations. Water, Air, and Soil Pollution 116: 299-310.

Chameides, W.L., Lindsay, R.W., Richardson, J. and Kiang, C.S. 1988. The role of biogenic hydrocarbons in urban photochemical smog: Atlanta as a case study. Science 241: 1473-1475.

Dickson, R.E., Lewin, K.F., Isebrands, J.G., Coleman, M.D., Heilman, W.E., Riemenschneider, D.E., Sober, J, Host, G.E., Zak, D.R., Hendrey, G.R., Pregitzer, K.S. and Karnosky, D.F. 2000. Forest Atmosphere Carbon Transfer and Storage (FACTS-II): The Aspen Free-Air CO2 and O3 Enrichment (FACE) Project: An Overview. USDA Forest Service NCRS, St. Paul, Minnesota, USA.

Felzer, B., Kicklighter, D., Mellilo, J., Wang, C., Zhuang, Q. and Prinn, R. 2004. Effects of ozone on net primary production and carbon sequestration in the conterminous United States using a biogeochemistry model. Tellus 56B: 230-248.

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Wittig, V.E., Ainsworth, E.A. and Long, S.P. 2007. To what extent do current and projected increases in surface ozone affect photosynthesis and stomatal conductance of trees? A meta-analytic review of the last 3 decades of experiments. Plant, Cell and Environment 30: 1150-1162.

Xu, S., Chen, W., Huang, Y. and He, X. 2012. Responses of growth, photosynthesis and VOC emissions of Pinus tabulaeformis Carr. exposure to elevated CO2 and/or elevated O3 in an urban area. Bulletin of Environmental Contamination and Toxicology 88: 443-448.

Last updated 6 November 2013