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Interactive Effects of CO2 and Ozone on Birch Trees -- Summary
Trees grown in CO2-enriched air nearly always exhibit increased rates of photosynthesis and biomass production, while trees grown in ozone (O3)-enriched air tend to experience the opposite effects. So what happens when both of these trace constituents of the atmosphere increase together? This question is addressed in the present summary with respect to birch trees.

At the Free-Air CO2 Enrichment (FACE) facility near Rhinelander, Wisconsin, USA, King et al. (2001) grew a mixture of paper birch and quaking aspen trees in 30-m-diameter plots that were maintained at atmospheric CO2 concentrations of 360 and 560 ppm with and without exposure to elevated O3 (1.5 times the ambient O3 concentration) for a period of two years. And in their study of the belowground environment of the trees, they found that the extra O3 had no effect on the growth of fine roots over that time period, but that elevated O3 and CO2 together increased the fine-root biomass of the mixed stand by 83%.

Simultaneously, and at the same FACE facility, Oksanen et al. (2001) observed O3-induced injuries in the thylokoid membranes of the chloroplasts of the birch trees' leaves; but the injuries were partially ameliorated in the elevated CO2 treatment. And in a study conducted two years later, Oksanen et al. (2003) say they "were able to visualize and locate ozone-induced H2O2 accumulation within leaf mesophyll cells, and relate oxidative stress with structural injuries." However, they report that "H2O2 accumulation was found only in ozone-exposed leaves and not in the presence of elevated CO2," adding that "CO2 enrichment appears to alleviate chloroplastic oxidative stress."

Across the Atlantic in Finland, Kull et al. (2003) constructed open-top chambers around two clones (V5952 and K1659) of silver birch saplings that were rooted in the ground and had been growing there for the past seven years. These chambers were fumigated with air containing 360 and 720 ppm CO2 in combination with 30 and 50 ppb O3 for two growing seasons, after which it was noted that the extra O3 had significantly decreased branching in the trees' crowns. This malady, however, was almost completely ameliorated by a doubling of the air's CO2 content. In addition, after one more year of study, Eichelmann et al. (2004) reported that, by itself, the increase in the air's CO2 content increased the average net photosynthetic rates of both clones by approximately 16%, while the increased O3 by itself caused a 10% decline in the average photosynthetic rate of clone V5952, but not of clone K1659. When both trace gases were simultaneously increased, however, the photosynthetic rate of clone V5952 once again experienced a 16% increase in net photosynthesis, as if the extra O3 had had no effect when applied in the presence of the extra CO2.

Working concurrently with the same trees, Riikonen et al. (2004) harvested them and reported finding that "the negative effects of elevated O3 were found mainly in ambient CO2, not in elevated CO2." In fact, whereas doubling the air's O3 concentration decreased total biomass production by 13% across both clones, simultaneously doubling the air's CO2 concentration increased total biomass production by 30%, thereby more than compensating for the deleterious consequences of doubling the atmospheric ozone concentration.

In commenting on this ameliorating effect of elevated CO2, the team of Finnish scientists said it "may be associated with either increased detoxification capacity as a consequence of higher carbohydrate concentrations in leaves grown in elevated CO2, or decreased stomatal conductance and thus decreasing O3 uptake in elevated CO2 conditions (e.g., Rao et al., 1995)." They also noted that "the ameliorating effect of elevated CO2 is in accordance with the results of single-season open-top chamber and growth chamber studies on small saplings of various deciduous tree species (Mortensen 1995; Dickson et al., 1998; Loats and Rebbeck, 1999) and long-term open-field and OTC studies with aspen and yellow-poplar (Percy et al., 2002; Rebbeck and Scherzer, 2002)."

In another paper to come out of the Finnish silver birch study, Peltonen et al. (2005) evaluated the impacts of doubled atmospheric CO2 and O3 concentrations on the accumulation of 27 phenolic compounds in the leaves of the trees, finding that elevated CO2 increased the concentration of phenolic acids (+25%), myricetin glycosides (+18%), catechin derivatives (+13%) and soluble condensed tannins (+19%). Elevated O3, on the other hand, increased the concentration of one glucoside by 22%, chlorogenic acid by 19%, and flavone aglycons by 4%. However, Peltonen et al. say that this latter O3-induced production of antioxidant phenolic compounds "did not seem to protect the birch leaves from detrimental O3 effects on leaf weight and area, but may have even exacerbated them." Last of all, in the combined elevated CO2 and O3 treatment, they found that "elevated CO2 did seem to protect the leaves from elevated O3 because all the O3-derived effects on the leaf phenolics and traits were prevented by elevated CO2."

Meanwhile, back at the FACE facility near Rhinelander, Wisconsin, USA, Agrell et al. (2005) had examined the effects of ambient and elevated concentrations of atmospheric CO2 and O3 on the foliar chemistry of birch and aspen trees, plus the consequences of these effects for host plant preferences of forest tent caterpillar larvae. In doing so, they had found that "the only chemical component showing a somewhat consistent co-variation with larval preferences was condensed tannins," and they discovered that "the tree becoming relatively less preferred as a result of CO2 or O3 treatment was in general also the one for which average levels of condensed tannins were most positively (or least negatively) affected by that treatment."

In this regard, it is of interest to note that the mean condensed tannin concentration of birch leaves was 18% higher in the elevated CO2 and O3 treatment. Consequently, as atmospheric concentrations of CO2 and O3 continue to rise, the increases in condensed tannin concentrations likely to occur in the foliage of birch trees should lead to their leaves becoming less preferred for consumption by the dreaded forest tent caterpillar, which according to Agrell et al. is "an eruptive generalist defoliator in North American hardwood forests, causing extensive damage during outbreak years (Fitzgerald, 1995)." Also, because the amount of methane expelled in the breath of ruminants is an inverse function of the condensed tannin concentration of the foliage they consume, the increased foliage tannin concentrations likely to exist in a high-CO2 world of the future should result in less methane being released to the atmosphere via ruminants ingesting such foliage, which phenomenon would tend to decrease the impetus for methane-induced global warming.

Concurrent with the work of Agrell et al., 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 on the growth of the Rhinelander birch trees, finding that relative to the ambient-air control treatment, elevated CO2 increased total biomass by 45% in the aspen-birch community, while elevated O3 caused a 13% reduction in total biomass relative to the control. Of most interest of all, the combination of elevated CO2 and O3 resulted in a total biomass increase of 8.4% relative to the control aspen-birch community. 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." Consequently, they 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.

Another paper to come out of the Finnish silver birch study was that of Kostiainen et al. (2006), who studied the effects of elevated CO2 and O3 on various wood properties. Their work revealed that the elevated CO2 treatment had no effect on wood structure, but that it increased annual ring width by 21%, woody biomass by 23% and trunk starch concentration by 7%. Elevated O3, on the other hand, decreased stem vessel percentage in one of the clones by 10%; but it had no effect on vessel percentage in the presence of elevated CO2.

In discussing their results, Kostiainen et al. noted that "in the xylem of angiosperms, water movement occurs principally in vessels (Kozlowski and Pallardy, 1997)," and that "the observed decrease in vessel percentage by elevated O3 may affect water transport," obviously lowering it. However, as they continued, "elevated CO2 ameliorated the O3-induced decrease in vessel percentage." In addition, they noted that "the concentration of nonstructural carbohydrates (starch and soluble sugars) in tree tissues is considered a measure of carbon shortage or surplus for growth (Korner, 2003)." Hence, they concluded that "starch accumulation observed under elevated CO2 in this study indicates a surplus of carbohydrates produced by enhanced photosynthesis of the same trees (Riikonen et al., 2004)." In addition, they reported that "during winter, starch reserves in the stem are gradually transformed to soluble carbohydrates involved in freezing tolerance (Bertrand et al., 1999; Piispanen and Saranpaa, 2001)," so that "the increase in starch concentration may improve acclimation in winter." Considering these several responses, therefore, it can be appreciated that the ongoing rise in the air's CO2 content should be a boon to silver birch (and likely many other trees) in both summer and winter in both pristine and ozone-polluted air.

Returning to the suite of Rhinelander FACE studies of paper birch, Darbah et al. (2007) found that the total number of trees that flowered increased by 139% under elevated CO2 but only 40% under elevated O3. Likewise, with respect to the quantity of flowers produced, they found that elevated CO2 led to a 262% increase, while elevated O3 led to only a 75% increase. They also determined that elevated CO2 had significant positive effects on birch catkin size, weight, and germination success rate, with elevated CO2 increasing the germination rate of birch by 110%, decreasing seedling mortality by 73%, increasing seed weight by 17% and increasing new seedling root length by 59%. On the other hand, they found that just the opposite was true of elevated O3, as it decreased the germination rate of birch by 62%, decreased seed weight by 25%, and increased new seedling root length by only 15%.

In discussing their findings, Darbah et al. additionally reported that "the seeds produced under elevated O3 had much less stored carbohydrate, lipids, and proteins for the newly developing seedlings to depend on and, hence, the slow growth rate." As a result, they concluded that "seedling recruitment will be enhanced under elevated CO2 but reduced under elevated O3," which is another important reason to hope that the atmosphere's CO2 concentration continues to climb as long as the air's O3 content is in a significantly ascending mode.

One year later, back at the Aspen FACE site near Rhinelander, Wisconsin, Riikonen et al. (2008) studied physiological consequences of increases in the atmospheric concentrations of CO2 (+36%) and O3 (+39%) - both alone and in combination - in paper birch trees during the 8th-9th years of growing-season CO2 enrichment.

And in doing so, they determined that elevated O3 decreased net photosynthesis in birch short-shoot leaves by 27%, averaged over the growing season, and in birch long-shoot leaves by 23% in the late-season, while elevated CO2 increased net photosynthesis in birch short-shoot leaves by 49% averaged over the growing season, and that in birch long-shoot leaves, measured in the late-season only, elevated CO2 enhanced net photosynthesis by 42%. In addition, they 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."

Also publishing in the same year were Darbah et al. (2008), who at various times over the 2004-2007 growing seasons collected many types of data pertaining to flowering, seed production, seed germination and new seedling growth and development of young paper birch trees. And giving results for O3 elevation first and CO2 enrichment second (as best can be determined from Darbah et al.'s graphs and text), the following percentage changes were derived for: (1) number of trees producing male flowers: (+86%, +140%) in 2006, (+70%, +70%) in 2007, (2) total number of male flowers produced (+58%, +260%) in 2006, (+68%, +82%) in 2007, (3) mean catkin or flower cluster mass (-8%, +12%) in 2004, (4) mean seed mass (-22%, +10%) in 2004, (-24%, +17%) in 2005, (-22%, -2%) in 2006, (5) mean seed germination success (-70%, +70%) in 2004, (-60%, +110%) in 2005, (-50%, +20%) in 2006, (6) mean seedling mortality, where the greatest reductions represent the greatest benefits, (-9%, -73%) in 2004, (7) mean seedling root length (+15%, +59%) in 2004, (8) mean seedling shoot length (-7%, +21%) in 2004, (9) mean seedling cotyledon length (-5%, +13%) in 2004, and (10) mean seedling dry mass after ~5 months growth in ambient air (-38%, +69%) in 2004. And in summarizing their findings, the six researchers wrote that "in this study, we found that elevated CO2 enhances and elevated O3 decreases birch reproduction and early seedling growth," while in the concluding sentence of their abstract, they wrote that "the evidence from this study indicates that elevated CO2 may have a largely positive impact on forest tree reproduction and regeneration while elevated O3 will likely have a negative impact." Yet radical environmentalists and climate alarmists continue to brand CO2 a harmful air pollutant, with many governmental agencies in nations the world over actually buying into this outrageous misrepresentation of reality.

In another study from the same year, Kostiainen et al. (2008) investigated the interactive effects of elevated concentrations of CO2 and O3 on the wood chemistry of paper birch saplings at the Aspen FACE facility in Rhinelander, Wisconsin, where the saplings had been exposed to four treatments - control, elevated CO2 (560 ppm), elevated O3 (1.5 x ambient) and their combination - for five growing seasons. And in doing so, they found that the paper birch saplings exhibited a tendency for increased stem diameter in elevated CO2, which also caused "an increase in extractives" - such as fats, waxes, triterpenoids and steroids - which have important roles to play in defense against pathogens and other biotic attacks. And as a result, the nine researchers concluded that the increased growth they observed in response to elevated CO2 "can be foreseen to shorten rotation lengths, with only moderate changes in wood properties," which is good. On the other hand, they said that "in response to elevated O3, stem wood production decreased and was accompanied by changes in vessel properties, which may indicate decreasing efficiency of water and nutrient transport," which is not good. Hence, it is indeed fortunate that the major negative effects of the elevated O3 concentration were reversed by the positive effects of the elevated CO2 concentration.

Contemporaneously, Uddling et al. (2008) studied how a 40% increase in CO2 and O3, alone and in combination, affected tree water use of mixed aspen-birch forests in the Rhinelander, Wisconsin FACE study, where sap flux and canopy leaf area index (L) were measured 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 concentration increased tree size and L by 40%, while the 40% increase in O3 concentration decreased tree size and L by 22%, in the aspen-birch stands. And thus 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 the mixed tree stands.

Also publishing in this very productive research year at the Wisconsin FACE facility 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 for all plant communities." In their analysis of subsequent data, however, they found that +O3 in combination with +CO2 increased coarse root biomass in birch/aspen communities, leading them to conclude that the amount of carbon being allocated to fine-root biomass under elevated O3 was increasing over time relative to the control, especially in the +CO2 +O3 treatment, in contrast with most shorter-term results. And in light of these findings, they concluded that "the positive effects of elevated CO2 on belowground net primary productivity may not be offset by negative effects of O3."

Back in Finland, Vapaavuori et al. (2009) grew 20 initially-seven-years-old individual trees of each of two different silver birch (Betula pendula Roth) clones -- 4 and 80 (V5952 and K1659, respectively, in the Finnish forest genetic register) -- for a period of three years (1999-2001) out-of-doors at the Suonenjoki Research Unit site of the Finnish Forest Research Institute within individual open-top chambers maintained at all combinations of (1) ambient CO2 and ambient O3, (2) ambient CO2 and double O3, (3) double CO2 and ambient O3, and (4) double CO2 and double O3, where CO2 treatments were imposed 24 hours per day, and where O3 treatments were imposed for 12, 12 and 14 hours per day in 1999, 2000 and 2001, respectively, throughout the course of which experiment they measured a variety of plant physiological responses to the four different treatments, including net photosynthesis, leaf stomatal conductance, leaf soluble proteins, leaf phenolic compounds, leaf nutrient concentrations, trunk and branch growth, physiology of the foliage and root systems, crown structure, wood properties, and interactions with folivorous insects. And when all was said and done, the twelve scientists reported that the negative effects of elevated O3 on the various growth parameters and properties of the trees "were mainly found in ambient CO2," noting that elevated CO2 typically "reversed or diminished the effects of elevated O3."

Lastly, returning to the Rhinelander (Wisconsin, USA) FACE facility, Zak et al. (2011) preface their work by noting an insufficient amount of soil nitrogen (N) and an overabundance of atmospheric ozone (O3) 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 state that the combined effects of elevated CO2 and O3 (eCO2 and eO3) "remain undocumented in the context of long-term, replicated field experiments." And to fill this void, they describe how they conducted such an experiment and what they learned from it.

The four researchers tell how in 1997 they 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. say 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 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 say "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 report 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. state that "NPP in the three plant communities responded similarly to the combined eCO2 and eO3 treatment." And they say 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 as well as projected increases in anthropogenic CO2 and climate warming (Stitch et al., 2007)."

Continuing in this vein, the four researchers ultimately conclude -- contrary to the analysis of Norby et al. (2010) -- 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 suggest 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."

In brief summation of these many positive findings, it can safely be concluded that from the tops of their crowns to the tips of their roots, earth's birch trees are generally negatively affected by rising ozone concentrations; but when the air's carbon dioxide concentration is also rising, these negative effects are often totally eliminated and replaced by positive responses.

Agrell, J., Kopper, B., McDonald, E.P. and Lindroth, R.L. 2005. CO2 and O3 effects on host plant preferences of the forest tent caterpillar (Malacosoma disstria). Global Change Biology 11: 588-599.

Bertrand, A., Robitaille, G., Nadeau, P. and Castonguay, Y. 1999. Influence of ozone on cold acclimation in sugar maple seedlings. Tree Physiology 19: 527-534.

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.

Darbah, J.N.T., Kubiske, M.E., Nelson, N., Oksanen, E., Vaapavuori, E. and Karnosky, D.F. 2007. Impacts of elevated atmospheric CO2 and O3 on paper birch (Betula papyrifera): Reproductive fitness. The Scientific World Journal 7(S1): 240-246.

Darbah, J.N.T., Kubiske, M.E., Nelson, N., Oksanen, E., Vapaavuori, E. and Karnosky, D.F. 2008. Effects of decadal exposure to interacting elevated CO2 and/or O3 on paper birch (Betula papyrifera) reproduction. Environmental Pollution 155: 446-452.

Dickson, R.E., Coleman, M.D., Riemenschneider, D.E., Isebrands, J.G., Hogan, G.D. and Karnosky, D.F. 1998. Growth of five hybrid poplar genotypes exposed to interacting elevated [CO2] and [O3]. Canadian Journal of Forest Research 28: 1706-1716.

Eichelmann, H., Oja, V., Rasulov, B., Padu, E., Bichele, I., Pettai, H., Mols, T., Kasparova, I., Vapaavuori, E. and Laisk, A. 2004. Photosynthetic parameters of birch (Betula pendula Roth) leaves growing in normal and in CO2- and O3-enriched atmospheres. Plant, Cell and Environment 27: 479-495.

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.

Fitzgerald, T.D. 1995. The Tent Caterpillars. Comstock Publishing, Ithaca, New York, USA.

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.

Korner, C. 2003. Carbon limitation in trees. Journal of Ecology 91: 4-17.

Kostiainen, K., Jalkanen, H., Kaakinen, S., Saranpaa, P. and Vapaavuori, E. 2006. Wood properties of two silver birch clones exposed to elevated CO2 and O3. Global Change Biology 12: 1230-1240.

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.

Kozlowski, T.T. and Pallardy, S.G. 1997. Physiology of Woody Plants. Academic Press, San Diego, CA, USA.

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.

Kull, O., Tulva, I. and Vapaavuori, E. 2003. Influence of elevated CO2 and O3 on Betula pendula Roth crown structure. Annals of Botany 91: 559-569.

Loats, K.V. and Rebbeck, J. 1999. Interactive effects of ozone and elevated carbon dioxide on the growth and physiology of black cherry, green ash, and yellow-poplar seedlings. Environmental Pollution 106: 237-248.

Mortensen, L.M. 1995. Effects of carbon dioxide concentration on biomass production and partitioning in Betula pubescens Ehrh. seedlings at different ozone and temperature regimes. Environmental Pollution 87: 337-343.

Norby, R.J., Warren, J.M., Iversen, C.M., Medlyn, B.E. and McMurtire, R.D. 2010. CO2 enhancement of forest productivity constrained by limited nitrogen availability. Proceedings of the National Academy of Sciences USA 107: 19,368-19,373.

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.

Peltonen, P.A., Vapaavuori, E. and Julkunen-Tiitto, R. 2005. Accumulation of phenolic compounds in birch leaves is changed by elevated carbon dioxide and ozone. Global Change Biology 11: 1305-1324.

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 enriched by CO2 and O3. Nature 420: 403-407.

Piispanen, R. and Saranpaa, P. 2001. Variation of non-structural carbohydrates in silver birch (Betula pendula Roth) wood. Trees 15: 444-451.

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.

Rao, M.V., Hale, B.A. and Ormrod, D.P. 1995. Amelioration of ozone-induced oxidative damage in wheat plants grown under high carbon dioxide. Plant Physiology 109: 421-432.

Rebbeck, J. and Scherzer, A.J. 2002. Growth responses of yellow-poplar (Liriodendron tulipifera L.) exposed to 5 years of [O3] alone or combined with elevated [CO2]. Plant, Cell and Environment 25: 1527-1537.

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.

Riikonen, J., Lindsberg, M.-M., Holopainen, T., Oksanen, E., Lappi, J., Peltonen, P. and Vapaavuori, E. 2004. Silver birch and climate change: variable growth and carbon allocation responses to elevated concentrations of carbon dioxide and ozone. Tree Physiology 24: 1227-1237.

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.

Vapaavuori, E., Holopainen, J.K., Holopainen, T., Julkunen-Titto, R., Kaakinen, S., Kasurien, A., Kontunen-Soppela, S., Kostiainen, K., Oksanen, E., Peltonen, P., Riikonen, J. and Tulva, I. 2009. Rising atmospheric CO2 concentration partially masks the negative effects of elevated O3 in silver birch (Betula pendula Roth). Ambio 38: 418-424.

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 10 April 2015