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Growth Response to CO2 with Other Variables (Ozone: Aspen Trees) -- Summary
Karnosky et al. (1999) described how they had grown O3-sensitive and O3-tolerant aspen clones in 30-m diameter plots at the Aspen FACE site near Rhinelander, Wisconsin, USA, where the young trees were maintained at atmospheric CO2 concentrations of either 360 or 560 ppm either with or without exposure to elevated O3 (1.5 times the ambient ozone concentration). And there, after one year of growth at ambient CO2, they determined that the elevated O3 had caused visible injury to leaves of both types of aspen, with the average percent damage in O3-sensitive clones being more than three times as great as that observed in O3-tolerant clones (55% vs. 17%, respectively). In combination with elevated CO2, however, the O3-induced damage to the leaves of these same clones was only 38% and 3%, respectively. And so they learned that elevated CO2 prevented much of the foliar damage that would otherwise have been induced by the high O3 concentrations.

King et al. (2001) studied the same young trees for a period of two years, concentrating on belowground growth, where elevated O3 alone had no effect on fine-root biomass. When the two aspen clones were simultaneously exposed to elevated CO2 and O3, however, there was an approximate 66% increase in the fine-root biomass of both of them, while back aboveground, Wustman et al. (2001) found that the aspen clones exposed to both elevated ozone and CO2 had 40% fewer visible foliar injuries than clones exposed to elevated ozone and ambient CO2.

Also working at the same experimental facility, Noormets et al. (2001) studied the interactive effects of O3 and CO2 on photosynthesis, finding that elevated CO2 increased rates of photosynthesis in both clones at all leaf positions. Maximum rates of photosynthesis were increased in the O3-tolerant clone by averages of 33 and 49% due to elevated CO2 alone and in combination with elevated O3, respectively, while in the O3-sensitive clone they were increased by 38% in both cases. Hence, CO2-induced increases in maximal rates of net photosynthesis were typically maintained, and sometimes even increased, during simultaneous exposure to elevated O3.

In another phase of the same experiment, Oksanen et al. (2001) found that after three years of treatment, ozone exposure caused significant structural injuries to thylakoid membranes and the stromal compartments within the chloroplasts of the trees' leaves; but they reported that these injuries were largely ameliorated by atmospheric CO2 enrichment. Likewise, leaf thickness, mesophyll tissue thickness, the amount of chloroplasts per unit cell area, and the amount of starch in the leaf chloroplasts were all decreased in the high ozone treatment; but simultaneous exposure of the ozone-stressed trees to elevated CO2 more than compensated for the ozone-induced reductions.

Then, after four years of growing five aspen clones with varying degrees of tolerance to ozone under the same experimental conditions, McDonald et al. (2002) developed what they termed a "competitive stress index," based on the heights of the four nearest neighbors of each tree, in order to study the influence of competition on the CO2 growth response of the various clones as modified by ozone. In general, elevated O3 reduced aspen growth independent of competitive status, while the authors noted an "apparent convergence of competitive performance responses in +CO2 +O3 conditions," which they said suggests that "stand diversity may be maintained at a higher level" in such circumstances.

Percy et al. (2002) also utilized the same experimental setting to assess a number of the aspen trees' growth characteristics, as well as the responses of one plant pathogen and two insects with different feeding strategies that typically attack the trees. Of the plant pathogen studied, they noted that "the poplar leaf rust, Melampsora medusae, is common on aspen and belongs to the most widely occurring group of foliage diseases." As for the two insects, they reported that "the forest tent caterpillar, Malacosoma disstria, is a common leaf-chewing lepidopteran in North American hardwood forests" and that "the sap-feeding aphid, Chaitophorus stevensis, infests aspen throughout its range." Hence, the rust and the two insect pests the scientists studied are widespread and have significant deleterious impacts on trembling aspen and other tree species. As but one example of this fact, Percy et al. noted that, "historically, the forest tent caterpillar has defoliated more deciduous forest than any other insect in North America" and that "outbreaks can reduce timber yield up to 90% in one year, and increase tree vulnerability to disease and environmental stress."

By itself, Percy et al. found that elevated O3 decreased tree height and trunk diameter, increased rust occurrence by nearly fourfold, improved tent caterpillar performance by increasing female pupal mass by 31%, and had a strong negative effect on the natural enemies of aphids. The addition of the extra CO2, however, completely ameliorated the negative effects of elevated O3 on tree height and trunk diameter, reduced the O3-induced enhancement of rust development from nearly fourfold to just over twofold, completely ameliorated the enhancement of female tent caterpillar pupal mass caused by elevated O3, and also completely ameliorated the reduction in the abundance of natural enemies of aphids caused by elevated O3.

One year later in another study from the Aspen FACE site, Holton et al. (2003) raised parasitized and non-parasitized forest tent caterpillars on two quaking aspen genotypes (O3-sensitive and O3-tolerant) alone and in combination for one full growing season; and they too found that elevated O3 improved tent caterpillar performance under ambient CO2 conditions, but not in CO2-enriched air. Thus, it is clear that elevated ozone concentrations have a number of significant negative impacts on the well-being of North America's most widely distributed tree species, while elevated carbon dioxide concentrations have a number of significant positive impacts that often completely eliminate the negative impacts of elevated O3. Hence, if the tropospheric O3 concentration continues to rise as expected (Percy et al. note that "damaging O3 concentrations currently occur over 29% of the world's temperate and subpolar forests but are predicted to affect fully 60% by 2100"), we had better hope that the air's CO2 content continues to rise as well, for if it doesn't rise, aspen trees will likely find themselves in a world of hurt.

Working at the same site and publishing concurrently were Oksanen et al. (2003), who reported they were able to "visualize and locate ozone-induced H2O2 [hydrogen peroxide] accumulation within leaf mesophyll cells, and relate oxidative stress with structural injuries in aspen." In addition, they discovered that "H2O2 accumulation was found only in ozone-exposed leaves and not in the presence of elevated CO2," leading them to conclude that "CO2 enrichment appears to alleviate chloroplastic oxidative stress."

Two years later, and still hard at work at the Aspen FACE site near Rhinelander, Wisconsin, King et al. (2005) evaluated the effect of CO2 enrichment alone, O3 enrichment alone, and the net effect of both CO2 and O3 enrichment together after seven full years of treatment. This work revealed that relative to the ambient-air treatment, elevated CO2 increased total biomass by 25% while elevated O3 decreased it by 23%. Of most interest of all, however, the combination of elevated CO2 and O3 resulted in a total biomass response of -7.8% relative to the control. King et al. thus concluded 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 consequently suggested that it makes sense to move forward with 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.

After one more year of data collection, Kubiske et al. (2006) found that individual tree and stand growth at the Wisconsin FACE site were significantly increased by the elevated CO2 treatment but decreased by the elevated O3 treatment, while the two effects essentially negated each other for no net change in the combined CO2 plus O3 treatment. However, they also found that "growth in elevated CO2 continued to increase each year but at a decreasing rate," such that "the annual growth increases under elevated CO2 became smaller with each successive year." And thus it was that they examined several possible explanations for this phenomenon, including N limitations and water limitations.

In conducting this investigation, the eight researchers found that "inter-annual variation in soil moisture did not modify the CO2 or O3 responses," and that "N limitations on growth did not differ among treatments." In addition, they determined that "root-specific uptake of nitrate or ammonium was not affected by elevated CO2 or O3." What they did find, however, was that the growth response to elevated CO2 "paralleled decreasing July PPF [photosynthetic photon flux] from 2001 through 2004, and decreasing previous October temperatures from 2001 to 2003." Therefore, Kubiske et al. concluded that "a several-year trend of increasingly cloudy summers and cool autumns were responsible for the decrease in CO2 growth response," explaining that "July PPF directly influences the amount of photosynthate available for stem volume growth," and that "October temperature in the north-temperate latitudes is of major importance in the photosynthetic activity of trees before leaf senescence," the stored products of which are used "to support the determinate growth phase the following year."

Reporting the results of their study of the Wisconsin aspen trees during the 8th and 9th years of growing-season CO2 enrichment, Riikonen et al. (2008) stated that elevated O3 decreased net photosynthesis in aspen clone 42E by 30% and clone 271 by 13%, averaged over the growing season, and in aspen clone 216 by 42% in the late-season, while elevated CO2 increased net photosynthesis in aspen clones 42E and 271 by 73 and 52%, respectively, averaged over the growing season, and that in aspen clone 216, measured in the late-season only, elevated CO2 enhanced net photosynthesis by 42%. They also observed that "elevated CO2 delayed, and elevated O3 tended to accelerate, leaf abscission in autumn." And when both treatments were applied together, they found that "elevated CO2 generally ameliorated the effects of elevated O3," noting that "leaf stomatal conductance was usually lowest in the combination treatment, which probably caused a reduction in O3 uptake."

Writing contemporaneously, Kostiainen et al. (2008) reported the results of their study of interactive effects of elevated concentrations of CO2 and O3 on radial growth, wood chemistry and structure of five 5-year-old trembling aspen clones at the Wisconsin FACE facility, where they had been exposed to four treatments - control, elevated CO2 (560 ppm), elevated O3 (1.5 x ambient) and their combination - for five full growing seasons. This work revealed that "elevated CO2 in the presence of ambient O3 tended to increase, and elevated O3 in the presence of ambient CO2 tended to decrease, stem radial growth," whereas "stem radial growth of trees in the combined elevated CO2 + O3 treatment did not differ from controls." In addition, they indicated that none of the structural variables of the aspen wood were affected by the elevated CO2 treatment, but that elevated O3 tended to decrease vessel lumen diameter.

Reporting on another aspect of the long-term aspen study at the Wisconsin FACE facility, Udling et al. (2008) investigated how a 40% increase above ambient values in CO2 and O3, alone and in combination, affected tree water use where "measurements of sap flux and canopy leaf area index (L) were made during two growing seasons, when steady-state L had been reached after more than 6 years of exposure to elevated CO2 and O3." This work revealed that the 40% increase in atmospheric CO2 increased tree size and L by 40%, while the 40% increase in O3 concentration decreased tree size and L by 22%. Hence, it was not surprising to learn that the combined effect of the two trace gas increases was an 18% increase in maximum stand-level sap flux. In addition, they observed that elevated O3 predisposed aspen stands to drought-induced sap flux reductions, whereas increased tree water use in response to elevated CO2 did not result in lower soil water content in the upper soil or decreasing sap flux relative to control values during dry periods.

It can thus be appreciated that the negative effects of O3 enrichment on tree growth and leaf development were more than compensated by the positive effects of an equal percentage increase in atmospheric CO2 concentration. And although the net effect on sap flux was positive (so that the trees transferred more water to the atmosphere), when the aspen stands needed moisture most (during times of drought), the water they needed was available to them, possibly because they "were growing in soil with CO2-induced increases in litter build-up and water-holding capacity of the upper soil," whereas these latter two benefits and the extra water they could supply to the trees were lacking when the trees were exposed to elevated ozone.

Also publishing new and related results in the same year were Pregitzer et al. (2008), who reported that "all root biomass sampling previous to 2002 showed that O3 exposure, alone or in combination with elevated CO2, consistently resulted in lower coarse root biomass." In analyzing more recent data, however, they found that the elevated O3 treatment significantly increased fine-root biomass in the aspen trees, and, in combination with elevated CO2, increased coarse root biomass in them as well. Hence, they concluded that "the amount of carbon being allocated to aspen fine-root biomass under elevated O3 is increasing over time relative to the control, especially in the elevated CO2 and elevated O3 treatment, in contrast with most shorter-term results, including those of King et al. (2001). And as a result, they further concluded that "the positive effects of elevated CO2 on belowground net primary productivity may not be offset by negative effects of O3."

One year later, noting that sporocarps (the reproductive structures of fungi) can be significant carbon sinks for the ectomycorrhizal fungi that develop symbiotic relationships with plants by forming sheaths around their root tips, where they are the last sinks for carbon in the long and winding pathway that begins at the source of carbon assimilation in plant leaves, Andrew and Lilleskov (2009) wrote that "it is critical to understand how ectomycorrhizal fungal sporocarps are affected by elevated CO2 and O3" because, as they continue, "sporocarps facilitate genetic recombination, permit long-distance dispersal and contribute to food webs," stressing that we need to know how these important processes will be affected by continued increases in the concentrations of these two trace constituents of the atmosphere.

In light of the importance of these considerations, the two researchers sampled aboveground sporocarps for four long years at the Aspen FACE site near Rhinelander, Wisconsin, which provided, in their words, a "unique opportunity to examine the effects of both elevated CO2 and O3 on a forested ecosystem," which examination was conducted during years 4 through 7 of the long-term study. And by so doing, they found that total mean sporocarp biomass "was generally lowest under elevated O3 with ambient CO2," and that it "was greatest under elevated CO2, regardless of O3 concentration," while in another place in their paper, they said there was "a complete elimination of O3 effects on sporocarp production when [extra] CO2 was added." And they stated that they "expect that the responses seen in the present study were conservative compared to those expected under regional to global changes in CO2 and O3."

By itself, or in combination with rising ozone concentrations, therefore, the ongoing rise in the air's CO2 content appears destined to enhance the genetic recombination and long-distance dispersal of the ectomycorrhizal fungi that form symbiotic relationships with the roots of aspen and other trees, thereby positively contributing to various food webs that will be found within earth's forests of the future.

Three years later, Zak et al. (2011) noted how both an insufficient amount of soil nitrogen (N) and an over-abundance of atmospheric ozone have often been claimed to either partially or totally repress the many positive effects of elevated atmospheric CO2 concentrations on plant growth and development, especially in the case of long-lived woody plants such as trees; but they added that the combined effects of elevated CO2 and elevated O3 (eCO2 and eO3) "remain undocumented in the context of long-term, replicated field experiments." At this point, however, they had already begun to fill this void; and they thus went on to describe how they had conducted just such an experiment and what they had learned from it.

Working at the Rhinelander (Wisconsin, USA) FACE facility, the four researchers first told how in 1997 they had planted one-half of each of 12 FACE plots with various trembling aspen (Populus tremuloides) genotypes (8, 42, 216, 259, 271) of differing CO2 and O3 sensitivities, while one-quarter of each ring was planted with a single aspen genotype (226) and paper birch (Betula papyrifera), and another quarter of each ring was planted with the same single aspen genotype and sugar maple (Acer saccharum). These treatments, each of which was replicated four times, were maintained for the following twelve years at either ambient CO2 and O3 (aCO2 and aO3), aCO2 and eO3, eCO2 and aO3, or eCO2 and eO3 - where eCO2 was 560 ppm, and where eO3 was in the range of 50-60 nmol/mol - while numerous types of pertinent data were concurrently collected.

In reference to the notorious progressive nitrogen limitation hypothesis, Zak et al. (2011) said they "found no evidence of this effect after 12 years of eCO2 exposure." In fact, they report that relative to net primary production (NPP) under aCO2, there was a 26% increase in NPP in the eCO2 treatment over the last three years of the study, which for a more standard 300-ppm increase in atmospheric CO2 concentration equates to an approximate 42% increase in NPP, which they said "was sustained by greater root exploration of soil for growth-limiting N, as well as more rapid rates of liter decomposition and microbial N release during decay."

With respect to the concomitant stress of O3 pollution, the researchers reported that "despite eO3-induced reductions in plant growth that occurred early in the experiment (i.e., after three years of exposure), eO3 had no effect on NPP during the 10th-12th years of exposure," which response, in their words, "appears to result from the compensatory growth of eO3-tolerant genotypes and species as the growth of eO3-sensitive individuals declined over time (Kubiske et al., 2007; Zak et al., 2007), thereby causing NPP to attain equivalent levels under ambient O3 and elevated O3."

In discussing various aspects of their long-term findings, Zak et al. (2011) wrote that "NPP in the three plant communities responded similarly to the combined eCO2 and eO3 treatment." And they said that "given the degree to which eO3 has been projected to decrease global NPP (Felzer et al., 2005), the compensatory growth of eO3-tolerant plants in our experiment should be considered in future simulations and, depending on the generality of this response, could dramatically diminish the negative effect of eO3 on NPP and carbon storage on land."

Continuing in this vein, the four researchers ultimately concluded that if forests of similar composition growing throughout northeastern North America respond in the same manner as those in their experiment (Cole et al., 2009), then enhanced forest NPP under eCO2 may be sustained for a longer duration than had previously been thought possible. In addition, they suggested that "the negative effect of eO3 may be diminished by compensatory growth of eO3-tolerant plants as they begin to dominate forest communities (Kubiske et al., 2007; Zak et al., 2007), suggesting that aspects of biodiversity like genetic diversity and species composition are important components of ecosystem response to this agent of global change."

And so one begins to understand that, ultimately, the good gas - CO2, which some have called the elixir of life - wins in the end because earth's trees, like much of the rest of the biosphere, are better equipped to "live long and prosper" in CO2-enriched air, even when faced with the generally negative influence of concomitant atmospheric ozone pollution.

Andrew, C. and Lilleskov, E.A. 2009. Productivity and community structure of ectomycorrhizal fungal sporocarps under increased atmospheric CO2 and O3. Ecology Letters 12: 813-822.

Cole, C.T., Anderson, J.E., Lindroth, R.L. and Waller, D.M. 2009. Rising concentrations of atmospheric CO2 have increased growth of natural stands of quaking aspen (Populous tremuloides). Global Change Biology 16: 2186-2197.

Felzer, B., Reilly, J., Melillo, J., Kicklighter, D., Sarofim, M., Wang, C., Prinn, R. and Zhuang, Q. 2005. Future effects of ozone on carbon sequestration and climate change policy using a global biogeochemical model. Climatic Change 73: 345-373.

Holton, M.K., Lindroth, R.L. and Nordheim, E.V. 2003. Foliar quality influences tree-herbivore-parasitoid interactions: effects of elevated CO2, O3, and plant genotype. Oecologia 137: 233-244.

Karnosky, D.F., Mankovska, B., Percy, K., Dickson, R.E., Podila, G.K., Sober, J., Noormets, A., Hendrey, G., Coleman, M.D., Kubiske, M., Pregitzer, K.S. and Isebrands, J.G. 1999. Effects of tropospheric O3 on trembling aspen and interaction with CO2: results from an O3-gradient and a FACE experiment. Water, Air, and Soil Pollution 116: 311-322.

King, J.S., Kubiske, M.E., Pregitzer, K.S., Hendrey, G.R., McDonald, E.P., Giardina, C.P., Quinn, V.S. and Karnosky, D.F. 2005. Tropospheric O3 compromises net primary production in young stands of trembling aspen, paper birch and sugar maple in response to elevated atmospheric CO2. New Phytologist 168: 623-636.

King, J.S., Pregitzer, K.S., Zak, D.R., Sober, J., Isebrands, J.G., Dickson, R.E., Hendrey, G.R. and Karnosky, D.F. 2001. Fine-root biomass and fluxes of soil carbon in young stands of paper birch and trembling aspen as affected by elevated atmospheric CO2 and tropospheric O3. Oecologia 128: 237-250.

Kostiainen, K., Kaakinen, S., Warsta, E., Kubiske, M.E., Nelson, N.D., Sober, J., Karnosky, D.F., Saranpaa, P. and Vapaavuori, E. 2008. Wood properties of trembling aspen and paper birch after 5 years of exposure to elevated concentrations of CO2 and O3. Tree Physiology 28: 805-813.

Kubiske, M.E., Quinn, V.S., Heilman, W.E., McDonald, E.P., Marquardt, P.E., Teclaw, R.M., Friend, A.L. and Karnosky, D.F. 2006. Interannual climatic variation mediates elevated CO2 and O3 effects on forest growth. Global Change Biology 12: 1054-1068.

Kubiske, M.E., Quinn, V.S., Marquart, P.E. and Karnosky, D.F. 2007. Effects of elevated atmospheric CO2 and/or O3 on intra- and inter-specific competitive ability of aspen. Plant Biology 9: 342-355.

McDonald, E.P., Kruger, E.L., Riemenschneider, D.E. and Isebrands, J.G. 2002. Competitive status influences tree-growth responses to elevated CO2 and O3 in aggrading aspen stands. Functional Ecology 16: 792-801.

Noormets, A., Sober, A., Pell, E.J., Dickson, R.E., Podila, G.K., Sober, J., Isebrands, J.G. and Karnosky, D.F. 2001. Stomatal and non-stomatal limitation to photosynthesis in two trembling aspen (Populus tremuloides Michx.) clones exposed to elevated CO2 and O3. Plant, Cell and Environment 24: 327-336.

Oksanen, E., Haikio, E., Sober, J. and Karnosky, D.F. 2003. Ozone-induced H2O2 accumulation in field-grown aspen and birch is linked to foliar ultrastructure and peroxisomal activity. New Phytologist 161: 791-799.

Oksanen, E., Sober, J. and Karnosky, D.F. 2001. Impacts of elevated CO2 and/or O3 on leaf ultrastructure of aspen (Populus tremuloides) and birch (Betula papyrifera) in the Aspen FACE experiment. Environmental Pollution 115: 437-446.

Percy, K.E., Awmack, C.S., Lindroth, R.L., Kubiske, M.E., Kopper, B.J., Isebrands, J.G., Pregitzer, K.S., Hendrey, G.R., Dickson, R.E., Zak, D.R., Oksanen, E., Sober, J., Harrington, R. and Karnosky, D.F. 2002. Altered performance of forest pests under atmospheres enriched by CO2 and O3. Nature 420: 403-407.

Pregitzer, K.S., Burton, A.J., King, J.S. and Zak, D.R. 2008. Soil respiration, root biomass, and root turnover following long-term exposure of northern forests to elevated atmospheric CO2 and tropospheric O3. New Phytologist 180: 153-161.

Riikonen, J., Kets, K., Darbah, J., Oksanen, E., Sober, A., Vapaavuori, E., Kubiske, M.E., Nelson, N. and Karnosky, D.F. 2008. Carbon gain and bud physiology in Populus tremuloides and Betula papyrifera grown under long-term exposure to elevated concentrations of CO2 and O3. Tree Physiology 28: 243-254.

Uddling, J., Teclaw, R.M., Kubiske, M.E., Pregitzer, K.S. and Ellsworth, D.S. 2008. Sap flux in pure aspen and mixed aspen-birch forests exposed to elevated concentrations of carbon dioxide and ozone. Tree Physiology 28: 1231-1243.

Wustman, B.A., Oksanen, E., Karnosky, D.F., Noormets, A., Isebrands, J.G., Pregitzer, K.S., Hendrey, G.R., Sober, J. and Podila, G.K. 2001. Effects of elevated CO2 and O3 on aspen clones varying in O3 sensitivity: Can CO2 ameliorate the harmful effects of O3? Environmental Pollution 115: 473-481.

Zak, D.R., Holmes, W.E., Pregitzer, K.S., King, J.S., Ellsworth, D.S. and Kubiske, M.E. 2007. Belowground competition and the response of developing forest communities to atmospheric CO2 and O3. Global Change Biology 13: 2230-2238.

Zak, D.R., Pregitzer, K.S., Kubiske, M.E. and Burton, A.J. 2011. Forest productivity under elevated CO2 and O3: positive feedbacks to soil N cycling sustain decade-long net primary productivity enhancement by CO2. Ecology Letters 14: 1220-1226.

Last updated 27 November 2013