SEARCH

SEARCH BY CITATION

Keywords:

  • air pollution;
  • atmospheric change;
  • cumulative ozone uptake;
  • forests;
  • global change;
  • stomata

ABSTRACT

  1. Top of page
  2. ABSTRACT
  3. INTRODUCTION
  4. MATERIALS AND METHODS
  5. RESULTS
  6. DISCUSSION
  7. ACKNOWLEDGMENTS
  8. REFERENCES
  9. Supporting Information

The surface concentration of ozone ([O3]) has risen from less than 10 ppb prior to the industrial revolution to a day-time mean concentration of approximately 40 ppb over much of the northern temperate zone. If current global emission trends continue, surface [O3] is projected to rise a further 50% over this century, with larger increases in many locations including Northern Hemisphere forests. This review uses statistical meta-analysis to determine mean effects, and their confidence limits, of both the current and projected elevations of [O3] on light-saturated photosynthetic CO2 uptake (Asat) and stomatal conductance (gs) in trees. In total, 348 measurements of Asat from 61 studies and 266 measures of gs from 55 studies were reviewed. Results suggested that the elevation of [O3] that has occurred since the industrial revolution is depressing Asat and gs by 11% (CI 9–13%) and 13% (CI 11–15%), respectively, where CI is the 95% confidence interval. In contrast to angiosperms, gymnosperms were not significantly affected. Both drought and elevated [CO2] significantly decreased the effect of ambient [O3]. Younger trees (<4 years) were affected less than older trees. Elevation of [O3] above current levels caused progressively larger losses of Asat and gs, including gymnosperms. Results are consistent with the expectation that damage to photosynthesis depends on the cumulative uptake of ozone (O3) into the leaf. Thus, factors that lower gs lessen damage. Where both gs and [O3] were recorded, an overall decline in Asat of 0.21% per mmol m−2 of estimated cumulative O3 uptake was calculated. These findings suggest that rising [O3], an often overlooked aspect of global atmospheric change, is progressively depressing the ability of temperate and boreal forests to assimilate carbon and transfer water vapour to the atmosphere, with significant potential effects on terrestrial carbon sinks and regional hydrologies.


INTRODUCTION

  1. Top of page
  2. ABSTRACT
  3. INTRODUCTION
  4. MATERIALS AND METHODS
  5. RESULTS
  6. DISCUSSION
  7. ACKNOWLEDGMENTS
  8. REFERENCES
  9. Supporting Information

Although altered precipitation, temperature and CO2 concentrations ([CO2]) have received the most attention with respect to the impacts of global change on terrestrial ecosystems (Geider, Delucia & Falkowski 2001; Prentice et al. 2001; Denman et al. 2007), tropospheric ozone (O3) is also rising (Ehhalt et al. 2001; Forster et al. 2007; Meehl et al. 2007) and is now considered to be the most important air pollutant affecting vegetation in both rural and urban areas (Ashmore 2005; EPA 2006; Karnosky et al. 2007; Matyssek et al. 2007; Paoletti et al. 2007). O3 is a secondary pollutant formed from the action of sunlight on nitrogen oxides (NOx), produced mainly from automobiles and biomass burning, in the presence of volatile organic compounds (VOCs) of both natural and industrial origin (Fowler et al. 1999b; Denman et al. 2007; Forster et al. 2007). Limited measurements from the nineteenth century suggest that pre-industrial ground-level O3 concentration ([O3]) was less than 10 ppb (Volz & Kley 1988). Over the last century, surface ambient background [O3] over forested land in the Northern Hemisphere has increased to levels that are damaging to vegetation (Chappelka & Samuelson 1998; Skarby et al. 1998; Fowler et al. 1999a; Akimoto 2003; EPA 2006; Forster et al. 2007; Karnosky et al. 2007; Matyssek et al. 2007). Although [O3] varies across these regions depending on proximity to sources of pollutants and time of day and year, 40 ppb is representative of the mean day-time ambient background [O3] during spring and summer months (Fowler et al. 1999a; Appendix S1). Furthermore, projections based on the A2 storyline of the Special Report on Emissions Scenarios (SRES) and included in the Intergovernmental Panel on Climate Change (IPCC) Assessment Report Four (AR4) indicate that [O3] could rise 20–25% between 2015 and 2050, and further increase by 40–60% by 2100 if current emission trends continue (Meehl et al. 2007). The largest increases are projected for the NorthernHemisphere (Karnosky et al. 2005) because of both increasing precursor concentrations and climatic conditions more favourable to O3 formation (Meehl et al. 2007).

O3 has been suspected of causing visible foliar injury and reduced growth in vegetation since the 1950s (Middleton 1956; Darley & Middleton 1966). Mounting evidence compiled over the past several decades in the peer-reviewed literature and government criteria documents has confirmed that O3 is the major pollutant responsible for visible foliar injury and reduced growth in trees (Reich 1987; Broadmeadow 1998; Chappelka & Samuelson 1998; Skarby et al. 1998; Fowler et al. 1999a; EPA 2006; Forster et al. 2007; Karnosky et al. 2007; Matyssek et al. 2007). For example, assuming that hourly O3 above 60 ppb is most damaging to trees, Fowler et al. (1999a) projected that nearly a quarter of the earth's forests are currently at risk of damage and reduced productivity, and by 2100 this will expand to half of the world's forests. Although the molecular mechanisms leading to O3 damage have not been fully elucidated (Kangasjarvi, Jaspers & Kollist 2005), physiological studies suggest that chronic elevation of [O3] decreases productivity primarily by lowering photosynthesis (Heath 1994; Farage & Long 1995; Dizengremel 2001; Long & Naidu 2002). Photosynthesis or gross primary productivity (GPP) is the driving step of the global carbon cycle, with more than 50% of total terrestrial GPP and net primary productivity (NPP) (i.e. GPP–autotrophic respiration) accounted for by forests (Geider et al. 2001; Grace 2004). Rising [O3] is therefore likely to decrease the capacity of the terrestrial biosphere to take up CO2 and offset rising global [CO2]. Recent reviews have documented responses of trees to O3 on a case-by-case basis (EPA 2006; Karnosky et al. 2007; Matyssek et al. 2007), but without a comprehensive quantitative summary of known observations, it is difficult to quantify the current overall trend and future change in photosynthetic productivity.

O3 is a strong oxidant, and significant damage to photosynthesis occurs when O3 enters the leaf through the stomata. This leads to a progressive loss of ribulose 1.5-bisphosphate carboxylase/oxygenase (Rubisco) activity (Farage et al. 1991; Farage & Long 1995; Pell, Schlagnhaufer & Arteca 1997; Dizengremel 2001), and is evident in a decline in light-saturated rate of leaf CO2 uptake (Asat) (Farage et al. 1991; Farage & Long 1995; Farage 1996). Reich (1987) proposed a ‘unifying theory’ of the impacts of O3 on conifers, broadleaved trees and crops, and showed that the amount of damage to photosynthesis was linearly related to the rate of O3 flux (FO3) through the leaf stomata, rather than O3 dose, i.e. the product of [O3] and hours of exposure. This ‘unifying theory’ marked the shift towards estimating cumulative O3 uptake (CU) rather than dose as a means to project O3 impact (Ollinger, Aber & Reich 1997; Felzer et al. 2004). This approach was recently promoted for the level II assessment of O3 impacts (Matyssek et al. 2007) and was shown to be superior to accumulated dose above a threshold of 40 ppb (Karlsson et al. 2007). The most recent reviews also suggest the approach would be further improved by including species-specific detoxification and repair processes. However, species-specific information regarding these processes is limited at present, and thus unavailable for incorporation into a comprehensive quantitative analysis of O3 impacts observed in the literature (Matyssek et al. 2007; Wieser & Matyssek 2007).

Although O3 may directly decrease stomatal conductance (gs) (Reich & Lassoie 1984), other analyses suggest that decreased gs follows a decline in photosynthetic carboxylation capacity and that decreased gs is likely a symptom rather than a cause of decline in Asat (Farage et al. 1991; Farage & Long 1995; Martin et al. 2001). Any environmental stress that reduces gs and therefore O3 uptake, such as drought, elevated [CO2] or nutrient deficiency, might be expected to lessen damage caused by O3 (Long & Naidu 2002). If O3 causes a large-scale decrease in gs in forests, there are major implications for regional hydrology, surface temperatures and the global climate system (Sellers et al. 1996). Conversely, any environmental condition that causes a decoupling of Asat to gs, such as the heterogeneous light environment low in a forest canopy, which results in a higher conductance than is needed to support CO2 uptake, is likely to exacerbate damage by O3 uptake (Fredericksen et al. 1996). However, the response of trees is also likely to vary with age (Samuelson & Kelly 2001; Nunn et al. 2006; Karnosky et al. 2007) and capacity of the tree to detoxify O3 (Matyssek et al. 2007). This complicates scaling to forests comprised of trees of various age classes (Samuelson & Kelly 2001; Karnosky et al. 2005), because scaling factors used in modelling analyses are based largely on juvenile trees in chambers (Reich 1987; Ollinger et al. 1997; Felzer et al. 2004). It has been suggested that conifers are less sensitive to O3 compared to broadleaved trees, possibly because of their lower average conductance (Reich 1987; Chappelka & Samuelson 1998; Samuelson & Kelly 2001; Nunn et al. 2006). This is consistent with the view that O3 damage is directly proportional to CU, which in any environment will be less for plants with lower gs. Martin et al. (2001) showed that a decline in the rate of damage to Asat with time in a leaf exposed to a constant elevation of [O3] may be explained by a decline in gs.

With the exception of free-air concentration enrichment (FACE) (Oksanen 2003; Karnosky et al. 2005; Low et al. 2006), all published experiments with trees grown at elevated [O3] involve chambers of various designs. By nature of their design, chambers alter the soil–plant–atmosphere continuum and place restrictions on tree growth, which might modify the observed response to O3 fumigation. Experiments also differ in many other respects including tree age, taxa, soils and fumigation techniques such as exposure duration and treatment [O3] (Reich 1987; Chappelka & Samuelson 1998; Skarby et al. 1998; Matyssek & Innes 1999; Ashmore 2005; Karnosky et al. 2007). This variability complicates any assessment of the overall effect of rising [O3] on tree Asat and gs.

From the wealth of individual studies, can we statistically determine the mean responses of Asat and gs to both current and projected elevations of [O3]? A meta-analysis allows estimation of a mean relative response and its confidence limits from disparate experiments investigating the effect of the same treatment, but administered in different ways and with different experimental designs. The technique has been widely used in ecology to analyse suites of observations from many varied independent sources (Hedges, Gurevitch & Curtis 1999; Rosenberg, Adams & Gurevitch 2000). Recent application of meta-analytic techniques to ecological and environmental studies has determined the magnitude and significance of the effect of elevated [CO2] on soybeans(Ainsworth et al. 2002) and trees (Curtis & Wang 1998), and the effect of elevated [O3] on soybean (Morgan, Ainsworth & Long 2003). The method is therefore suitable for a post-hoc analysis of the O3 effects literature.

For this review, we compiled peer-reviewed studies published since the late 1960s, and from observations found in this literature we conducted a meta-analysis to determine the direction, magnitude and significance of O3 impacts on Asat and gs of trees. This review includes observations from 73 primary research articles reporting over 1900 observations of Asat and gs of trees exposed to ambient and elevated [O3] relative to control conditions. This quantitative meta-analytic review of the literature addresses the following questions: (1) what is the impact of observed ambient background [O3] on Asat and gs relative to pre-industrial [O3]; (2) how will future elevated [O3] affect Asat and gs relative to pre-industrial [O3]; (3) what are the expected changes in Asat and gs with future [O3] relative to observed ambient background [O3]; (4) in all cases, how do other factors modify this response; and (5) is there a linear decline in Asat with CU when all studies of trees are pooled together? Quantitative answers to these questions should provide the best currently available estimates of how rising [O3] will affect Asat and gs, two key parameters in global and regional carbon cycle and hydrological models.

MATERIALS AND METHODS

  1. Top of page
  2. ABSTRACT
  3. INTRODUCTION
  4. MATERIALS AND METHODS
  5. RESULTS
  6. DISCUSSION
  7. ACKNOWLEDGMENTS
  8. REFERENCES
  9. Supporting Information

Database

A database of the effects of O3 on Asat and gs was compiled by surveying the peer-reviewed literature with the Web of Science (Thompson-ISI, Philadelphia, PA, USA) and SilverPlatter (Ovid Technologies, New York, NY, USA). Key-word searches were made for as far back as the search engines would allow, covering the period 1970 through October 2006. To avoid missing relevant references because of inadequate key-words or those published prior to 1970, reference lists of articles identified from the key-word searches were checked against the database to identify missing references. In total, 133 articles that reported [O3] effects on Asat and 110 articles that reported gs were found. Within these articles, individual measurements were considered independent if they were made on different species or distinct genotypes within a species, or if the measurements were made on different dates. Articles and measurements were excluded if: (1) the standard deviation (SD) could not be determined or there was no replication; (2) an exact measure of either Asat or gs, with their units, could not be extracted; (3) the description of experimental design was insufficient to allow objective assignment to the categories of Table 1; (4) the data were previously or more completely reported in another article; and (5) the leaf exposure period was less than 7 d and therefore not representative of chronic exposure. After evaluating articles based on these exclusion criteria, 65 articles measuring Asat and 51 articles measuring gs were used for the meta-analysis, most exclusions having resulted from the first criterion (Appendix S1).

Table 1.  Categories and levels describing the experimental conditions in studies of ozone (O3) effects on light-saturated photosynthesis (Asat) and stomatal conductance (gs) of trees
CategoryCategorical level
Tree classificationAngiospermGymnosperm       
Tree age (years)<4>4       
Leaf age (years)0 > 11–2≥2      
Rooting environmentPot grownRooted in the ground       
MethodGrowth chamberGreenhouseOpen-top chamberBranch chamberFree-air enrichment    
Experiment duration (d)7–2930–5960–8990–119120–149150–365≥365≥730≥1095
Mean [O3] (ppb)0–2930–5960–8990–119≥120    
Additional treatmentNo additional treatmentElevated [CO2]DroughtLow nutrientLower canopy    

For each observation of Asat or gs, the value in the control and elevated [O3] treatment (XC and XE), the SDs (SDC and SDE) and replication (NC and NE) were entered into the database together with categorical information, including [O3] concentration and duration (Table 1). Values of Asat and gs were extracted from tables, text and/or figures of each primary article, and then compiled into spreadsheets specific to both Asat and gs. Values given only in the figures of publications were digitized using data extraction software (GRAFULA 3 v.2.10, Wesik SoftHaus, St. Petersburg, Russia). If measurements of A or gs were made over the diurnal course, only values for light- saturating conditions were recorded in the database. Three databases were compiled: (1) trees grown in charcoal-filtered (CF) control were compared to trees grown in ambient background [O3]; (2) trees grown in CF control were compared to trees grown in elevated [O3] treatments; and (3) trees grown in ambient background [O3] were compared to trees grown in elevated [O3] treatments.

Sources of variation

Eight categories were identified as important potential sources of variation that could alter the response of Asat and/or gs to [O3] (Table 1). Each observation of Asat and gs was objectively coded into the appropriate levels of each category shown in Table 1: (1) angiosperm versus gymnosperm; (2) tree age; (3) leaf age; (4) rooting environment; (5) fumigation method (e.g. FACE versus open-top chamber); (6) duration of leaf fumigation; (7) mean [O3]; and (8) additional treatments (e.g. elevated [CO2] or drought) (Table 1). The mean [O3] in the control and in the treatment is defined as the average concentration for the leaf exposure period which varied from 4 to 24 h d−1. Duration of leaf fumigation varied from 7 d to more than a year. In addition to these categories, the different tree genera in each database were examined.

Meta-analyses

To calculate the effect of O3 on trees as a proportionate change in Asat or gs, the natural log of the response ratio, r, was used, where r is the ratio of the mean in the experimental treatment (XE) divided by the mean in the control (XC). Based on the assumption of random variation in effect sizes between studies, we used a weighted mixed-model analysis where each individual response was weighted by the reciprocal of the mixed-model variance (Gurevitch & Hedges 1999; Hedges et al. 1999). In the first analysis, XC was the measure in CF air, and XE was ambient background [O3]. In the second analysis, XC was the measure in CF air, and XE was the measure from elevated [O3] treatments. In the third analysis, XC was the measure in ambient background [O3], and XE was the measure in elevated [O3] treatments.

Effect sizes are reported as the unlogged r converted to the mean percentage change from the control [(r – 1) × 100] as in previous analyses (Curtis & Wang 1998; Ainsworth et al. 2002; Morgan et al. 2003; Ainsworth & Long 2005). Trees unaffected by [O3] have an r = 1, and therefore a 0% change from control. A negative percentage change indicates a decrease in Asat or gs in response to [O3], while positive values indicate an increase. If the 95% confidence interval (CI) did not overlap zero, response to O3 treatment is considered significant (Curtis & Wang 1998). A meta-analytic software package was used to calculate all effect sizes and their 95% CIs (MetaWin 2.1.3.4, Sinauer Associates, Sunderland, MA, USA) (Rosenberg et al. 2000).

The eight categories described earlier were analysed to test differences in the response of different genera of trees grown under different experimental and environmental conditions. The analysis proceeded by partitioning the variance in two steps following the methods previously described by Curtis & Wang (1998). Firstly, between-group heterogeneity (QB) for each category was examined, then data were subdivided according to levels of those categorical variables with significant QB. If 95% CIs did not overlap, means were considered to be significantly different from one another (Curtis & Wang 1998; Gurevitch & Hedges 1999). Levels of each category were included in the analysis if there were at least 10 observations. If less than 10 observations were available, results were only discussed if they originated from at least three independent articles.

Cumulative O3 uptake analysis

In addition to the mean [O3] (ppb) calculated over the leaf exposure period, the duration of leaf fumigation reported in days (d) and the number of hours (h) that fumigation was applied each day were recorded. Assuming that [O3] inside the leaf is zero (Laisk, Kull & Moldau 1989), then FO3 into the leaf was calculated as:

  • image(1)

where gz (mmol m−2 s−1) is gs to O3 calculated from gs (mmol m−2 s−1) divided by 1.67, the ratio of the diffusion constants for water vapour and O3 (Laisk et al. 1989). Finally, CU (mmol m−2) was calculated by summing FO3 over the time interval between consecutive observations of gs:

  • image(2)

following Reich (1987) and Nunn et al. (2006). Asat expressed as the percent reduction in leaves in elevated [O3] treatments relative to those in CF air was linearly regressed against CU. Studies were excluded from this analysis based on three criteria: (1) rates of Asat were not reported in conjunction with gs; (2) there was insufficient information to convert the reported units of gs to mmol m−2 or to convert units of Asat into µmol m−2 s−1; and (3) cumulative uptake was less than 10 mmol m−2; these studies were excluded because either conductance was low and thus difficult to measure with any accuracy, or the exposure period was brief. Thirty-eight independent studies investigating 28 different species provided a sample size of 292 for the regression analysis.

RESULTS

  1. Top of page
  2. ABSTRACT
  3. INTRODUCTION
  4. MATERIALS AND METHODS
  5. RESULTS
  6. DISCUSSION
  7. ACKNOWLEDGMENTS
  8. REFERENCES
  9. Supporting Information

CF air versus ambient background O3

Across all studies, the ambient background [O3] caused an 11% decrease in Asat (n = 348) and a 13% decrease in gs (n = 266) compared to leaves in CF air. The average ambient [O3] in the experiments in which Asat was measured was 47 ppb, with a range of 26–100 ppb, and was slightly higher than the average across the studies reporting effects on gs, 42 ppb which ranged between 26 and 69 ppb (Fig. 1). This average however hides a marked difference between gymnosperms which showed no response in Asat or gs when exposed at ambient background [O3] (QB = 26.97, P < 0.001 for Asat; QB = 29.86, P < 0.001 for gs) (Fig. 1) versus angiosperms which showed a highly significant decrease of 14 and 16%, respectively (Fig. 1). These were also significant differences between genera. Asat and gs were significantly reduced in Fraxinus, Populus, Prunus and Viburnum species grown in ambient background O3 relative to CF controls, while there was no change in either parameter in Picea, Pinus or Quercus species (Table 2). The Asat of Fagus species was not affected by background O3, while gs was reduced by 16% on average (Table 2). One limitation in the comparison of genera is that [O3] differed between studies of different genera, and may confound the comparisons (Table 2).

image

Figure 1. The percent change in light-saturated photosynthesis (Asat) and stomatal conductance (gs) for trees grown in ambient background ozone (O3) relative to charcoal-filtered (CF) air including the difference between angiosperms and gymnosperms. Degrees of freedom (d.f.) and average ambient background [O3] are given on the y-axis.

Download figure to PowerPoint

Table 2.  Percent change (% change), 95% confidence intervals (95% CI), degrees of freedom (d.f.) and mean ozone concentrations ([O3]) for the estimate of the mean response of light-saturated photosynthesis (Asat) and stomatal conductance (gs) across all studies (cumulative effect size), and for angiosperms, gymnosperms and different genera grown in charcoal-filtered (CF) air versus ambient background ozone (O3)
GenusAsatgs
% Change95% CId.f.[O3]% Change95% CId.f.[O3]
Cumulative effect size−11−13 to −934747−13−15 to −1126542
Gymnosperms−2−6 to 383452−4 to 95744
Picea4−4 to 122333122–242339
Pinus−3−7 to 25849−6−14 to 33348
Angiosperms−14−16 to −1226348−16−18 to −1320742
Fagus−5−11 to 21433−16−27 to −3836
Fraxinus−17−22 to −123842−9−16 to −23542
Populus−24−28 to −216057−27−31 to −223641
Prunus−5−9 to −15954−12−19 to −41944
Quercus0−8 to 92242−1−5 to 63643
Viburnum−20−23 to −153641−27−32 to −223641

Angiosperms growing under different growth environments or stress conditions showed different responses to ambient background [O3] (Table 3; Fig. 2). Asat and gs were not reduced significantly in drought-stressed trees exposed to ambient O3. No significant interaction of elevated [CO2] and [O3] or of nutrient deficiency with [O3] could be detected for trees grown in ambient [O3] relative to CF air. The reduction in both Asat and gs caused by current ambient elevation of [O3] was about 30% greater in lower canopy versus upper canopy leaves (Fig. 2). However, all of the measurements of lower canopy leaves came from a single study on three species (Novak et al. 2005), so results should be interpreted cautiously. When studies which imposed no additional treatments were separated out, then Asat (n = 194) and gs (n = 136) were reduced by 9 and 12%, respectively, by the current ambient [O3] (Fig. 2). Tree age significantly altered the mean response of Asat and gs to ambient background [O3] (Table 3; Appendix S2). In young trees age <4 years, Asat was reduced by 10% while the reduction in Asat was more than double (22%) for trees >4 years (Appendix S1). Ambient [O3] reduced gs in trees <4 years by 5%, while gs of trees >4 years was reduced by 23% compared to CF controls (Appendix S2).

Table 3.  Between-group heterogeneity (QB) for ozone (O3) effect size, comparing angiosperms grown in charcoal-filtered (CF) air versus ambient background ozone concentration ([O3])
CategoryAsatgs
QBPQBP
  1. Asat, light-saturated photosynthesis; gs, stomatal conductance.

Genus136.91<0.001112.93<0.001
Tree age16.75<0.00160.67<0.001
Method0.320.6270.470.531
Rooting environment0.220.90119.010.001
Duration11.430.1676.470.385
Additional treatment66.72<0.00141.04<0.001
image

Figure 2. The effect of additional treatments on the response of light-saturated photosynthesis (Asat) and stomatal conductance (gs) of angiosperms to ambient background ozone (O3) relative to charcoal-filtered (CF) controls. Degrees of freedom (d.f.) and average ambient background [O3] are given on the y-axis.

Download figure to PowerPoint

Neither duration nor method of exposure significantly altered the mean response of Asat or gs of angiosperms to ambient background [O3] (Table 3). Ambient [O3] reduced gs in trees grown in pots, while there was no effect on gs in trees grown in the ground (Appendix S2).

CF air versus elevated O3 treatments

Examination of all studies which compared trees grown in CF air with those grown in elevated [O3] treatments showed an average decrease in Asat of 19% (n = 460) at a mean [O3] of 85 ppb and reduction in gs of 10% (n = 277) (Fig. 3) at a mean [O3] of 91 ppb. The reduction in Asat was progressively greater as the treatment [O3] increased, with a similar trend in gs (Table 4; Fig. 3), except for treatments above 120 ppb where the small sample size and restriction to a few genera limit interpretation.

image

Figure 3. The percent change in light-saturated photosynthesis (Asat) and stomatal conductance (gs) for trees grown in elevated ozone (O3) treatments relative to charcoal-filtered (CF) air, and the impact of different elevated ozone concentrations ([O3]) on the response. Degrees of freedom (d.f.) and average treatment [O3] are given on the y-axis.

Download figure to PowerPoint

Table 4.  Between-group heterogeneity (QB) for ozone (O3) effect size across descriptive categories, comparing trees grown in charcoal-filtered (CF) air versus elevated O3 treatments
CategoryAsatgs
QBPQBP
  1. Asat, light-saturated photosynthesis; gs, stomatal conductance; [O3], O3 concentration.

Angiosperms versus gymnosperms0.880.3872.520.157
Genus26.770.04138.530.006
Tree age11.930.0020.00010.992
Leaf age2.300.3786.710.073
Rooting environment1.040.3588.620.014
Method1.660.6952.010.457
Duration18.750.05621.350.027
[O3]24.170.00113.210.018
Additional treatment26.400.00217.070.012

When comparing Asat in trees grown in CF air versus elevated O3 treatments, gymnosperms did not significantly differ from angiosperms; however, genera showed different responses for both parameters that were not explained by differences in the mean treatment [O3] (Table 5). Elevated O3 treatments significantly reduced both Asat and gs for Fagus, Pinus and Populus, while only Asat was reduced for Prunus species (Table 5). There was no response of Asat or gs to elevated O3 treatments for Picea or Liriodendron species relative to CF controls (Table 5), and no response of gs for Abies species. Further analysis revealed that the gs studies with [O3] greater than 120 ppb were made with Abies, Betula, Picea and Pinus species, which do not show a general decrease in gs with elevated [O3].

Table 5.  Percent change (% change), 95% confidence intervals (95% CI), degrees of freedom (d.f.) and mean ozone concentrations ([O3]) for the estimate of the mean response of light-saturated photosynthesis (Asat) and stomatal conductance (gs) across all studies (cumulative effect size), and for angiosperms, gymnosperms and different genera grown in charcoal-filtered (CF) air versus elevated ozone (O3) treatments
GenusAsatgs
% Change95% CId.f.[O3]% Change95% CId.f.[O3]
Cumulative effect size−19−21 to −1645586−10−13 to −627691
Gymnosperms−17−21 to −1216092−6−12 to 010996
Abies    2−19 to 289110
Picea−8−17 to 254765−4 to 164590
Pinus−21−27 to −159397−17−24 to −953100
Angiosperms−20−23 to −1629482−12−16 to −716688
Betula−15−23 to −848861−8 to 103898
Fagus−21−32 to −81749−23−35 to −81157
Liriodendron−10−29 to 151258−10−35 to 241060
Populus−21−26 to −1612079−19−28 to −940104
Prunus−28−34 to −2152106−100   
Quercus−3−17 to 142277−15−24 to −63680

Additional treatments affected the mean response of both Asat and gs (Table 4; Fig. 4). Both drought and elevated [CO2] ameliorated the effect of elevated [O3] on Asat and gs, while nutrient deficiency and lower canopy did not significantly affect the response (Fig. 4). Excluding studies with additional treatments, elevated [O3] reduced Asat by 20% (n = 374) and gs by 12% (n = 230). This was more than double the reduction of Asat by ambient air relative to CF controls, while the reduction in gs was of similar magnitude in both analyses in the absence of additional stress or changes to growth environment (Figs 2 & 4). Neither fumigation method nor leaf age significantly altered the mean response of either Asat or gs (Table 4). The mean response of Asat to elevated [O3] was affected by tree age, while the mean response of gs to elevated [O3] was affected by duration of exposure and rooting environment (Table 4; Appendix S3). The response of gs to elevated [O3] treatments relative to CF air was greater for trees grown in the ground compared with pot-grown trees, but this might be explained by the higher mean [O3] associated with experiments in which trees were grown in the ground, rather than in pots (Appendix S3).

image

Figure 4. The effect of additional treatments on the response of light-saturated photosynthesis (Asat) and stomatal conductance (gs) to elevated ozone (O3) treatments relative to charcoal-filtered (CF) controls. Degrees of freedom (d.f.) and average treatment [O3] are given on the y-axis.

Download figure to PowerPoint

Ambient background O3 versus elevated O3 treatments

In a third analysis, we compared trees grown at ambient background [O3], which averaged to 44 ppb for Asat and 36 ppb for gs, with trees grown under elevated O3 treatments which averaged 81 ppb for Asat and 71 ppb for gs. Across all studies, elevated O3 treatments decreased Asat by 18% (n = 349) and decreased gs by 6% (n = 253) (Fig. 5). There was a progressive decrease in Asat and gs with an increase in treatment [O3], but again no effect on gs at [O3] > 120 ppb (Table 6; Fig. 5). In this comparison, neither gymnosperm versus angiosperm nor leaf age significantly altered the magnitude of the decrease because of elevation of [O3] (Table 6). Duration of exposure altered the mean response, but the trends were not easily explained (Appendix S4). The Asat of trees <4 years old was reduced by 21%, which was significantly different from trees >4 years old for which Asat was reduced by 10% (Appendix S4). Asat was reduced more for trees grown in the ground compared to pot-grown trees, despite lower average [O3], while gs was unaffected by elevated [O3] relative to ambient [O3] (Appendix S4). Neither branch chamber nor FACE significantly affected the response of gs to elevated [O3] relative to ambient background controls; however, gs was significantly reduced by elevated O3 treatments in open-top chambers (Appendix S4). There was no significant effect of additional treatment (Table 6). Acer, Betula, Fagus, Picea, Pinus, Populus and Prunus species showed significant decreases in Asat at elevated [O3] but not Quercus, while only Pinus and Quercus species showed a decrease in gs (Table 7).

image

Figure 5. The percent change in light-saturated photosynthesis (Asat) and stomatal conductance (gs) for trees grown in elevated ozone (O3) treatments relative to ambient background O3, and the impact of different elevated O3 treatments on the response of both parameters. Degrees of freedom (d.f.) and average treatment [O3] are given on the y-axis.

Download figure to PowerPoint

Table 6.  Between-group heterogeneity (QB) for ozone (O3) effect size across descriptive categories, comparing trees grown in ambient background ozone concentration ([O3]) versus elevated O3 treatments
CategoryAsatgs
QBPQBP
  1. Asat, light-saturated photosynthesis; gs, stomatal conductance.

Angiosperms versus gymnosperms1.980.2562.300.178
Genus24.670.08319.520.103
Tree age4.380.0763.30.148
Leaf age3.390.3364.550.183
Rooting environment5.700.0500.190.697
Method3.310.70315.670.015
Duration20.270.04420.570.015
[O3]34.310.00114.180.030
Additional treatment5.920.5635.230.535
Table 7.  Percent changes (% change), 95% confidence intervals (95% CI), degrees of freedom (d.f.) and mean ozone concentrations ([O3]) for the estimate of the mean response of light-saturated photosynthesis (Asat) and stomatal conductance (gs) across all studies (cumulative effect size), and for angiosperms, gymnosperms and different genera grown in ambient background ozone (O3) versus elevated O3 treatments
GenusAsatgs
% Change95% CId.f.[O3]% Change95% CId.f.[O3]
Cumulative effect size−18−20 to −1534881−6−10 to −325271
Gymnosperms−16−19 to −1213487−10−15 to −410182
Picea−16−22 to −105573−7−15 to 16077
Pinus−16−21 to −107694−13−22 to −34090
Angiosperms−19−22 to −1621377−4−9 to 115063
Acer−20−31 to −814674−12 to 221268
Betula−14−22 to −643458−2 to 185240
Fagus−11−20 to −21953−12−26 to 51157
Liriodendron    −6−41 to 50768
Populus−26−32 to −204089    
Prunus−24−30 to −1950108    
Quercus−7−17 to 52277−11−19 to −23880

Cumulative O3 uptake analysis of CF versus elevated O3 treatments

When observations of Asat for trees grown in elevated [O3] relative to CF air were combined, there was a significant negative correlation between percent change in Asat from CF air and CU (Fig. 6) (r2 = 0.25; P < 0.01). Linear regression analysis showed a significant and linear loss of photosynthetic capacity, as measured by Asat, of 22% for every 100 mmol m−2 of CU per unit of leaf area (Fig. 6)

image

Figure 6. The relationship between cumulative ozone (O3) uptake (mmol m−2) and the percent change in light-saturated photosynthesis (Asat) for trees grown in elevated O3 treatments relative to charcoal-filtered (CF) air. The solid line shows the linear regression, and dashed lines show 95% confidence intervals (CIs). Twenty-eight species were included in this analysis: Acer saccharum, Betula pendula, Ceratonia siliqua, Fagus sylvatica, Fraxinus pennsylvanica, Liriodendron tulipifera, Malus pumila, Olea europa, Picea abies, Pinus echinata, Pinus halepensis, Pinus ponderosa, Pinus taeda, Populus maximowizii × trichocarpa, Populus tremuloides, Populus tristis × balsamifera, Prunus armeniaca, Prunus avium, Prunus domestica, Prunus dulcis, Prunus persica, Prunus salicina, Prunus serotina, Pyrus pyrafolia, Quercus ilex, Quercus ilex ilex, Quercus ilex rotundifolia and Quercus rubra.

Download figure to PowerPoint

DISCUSSION

  1. Top of page
  2. ABSTRACT
  3. INTRODUCTION
  4. MATERIALS AND METHODS
  5. RESULTS
  6. DISCUSSION
  7. ACKNOWLEDGMENTS
  8. REFERENCES
  9. Supporting Information

Are current background levels of O3 affecting photosynthesis and gs in trees?

This meta-analytic review of the peer-reviewed literature suggests that the elevation of surface level [O3] that has occurred since the industrial revolution is depressing leaf photosynthetic CO2 uptake in trees by 11%, with a 95% CI of 9–13% (Table 2). This is based on 348 measurements, almost exclusively from studies representing trees from the temperate and boreal forest biomes of the Northern Hemisphere, the region of the globe that has seen the largest increase in surface level [O3] (Ehhalt et al. 2001). Temperate and boreal forests account for approximately 17% of terrestrial NPP and 29% of the estimated total carbon sink of terrestrial ecosystems (0.82 Gt C year−1) (Grace (2004). Assuming that photosynthesis or GPP is proportional to NPP, our findings suggest that these regions could be an even larger current carbon sink in the absence of O3 effects.

This review also suggests that the rise in [O3] since the industrial revolution has also caused a 13% decrease in average gs with a 95% CI of 11–15% (Table 2; Fig. 1). Because the response of Asat to intercellular CO2 concentration (ci) is non-linear, this would be insufficient to explain the 9–13% decrease in Asat. However, such a large decrease in gs across forest landscapes could have impacts on regional and continental hydrology. Sellers et al. (1996) showed via coupled plant physiology and global circulation models that a decrease in gs of similar magnitude because of rising [CO2] affected regional climate, by both decreasing transfer of water to the atmosphere so lowering precipitation and increasing surface temperature. In soy bean fields growing under FACE, a 10% decrease in average gs across three complete growing seasons resulted in an 8.6% decrease in system evapo-transpiration and 0.4 °C increase in day-time surface temperature (Bernacchi et al. 2007). As the third strongest greenhouse gas, O3 directly contributes to global warming (Denman et al. 2007); this analysis also suggests that in its role as the most important secondary pollutant impacting trees, current [O3] has potential to indirectly alter regional climate change through reduced gs leading to increased surface temperature and decreased atmospheric humidity.

O3 effects are not uniform across taxa: gymnosperms are apparently unaffected by the current increase in ambient background [O3], while Asat and gs are generally decreased in angiosperms. Gymnosperms consistently have lower average gs compared to angiosperms and therefore lower uptake of [O3]. Samuelson & Kelly (2001) reported gs for a range of gymnosperm and angiosperm temperate trees grown at different life stages and grown under the same conditions. From this broad sample, we calculated a mean gs of 100 mmol m−2 s−1 for gymnosperms and 185 mmol m−2 s−1 for angiosperms. At these conductances, O3 uptake in the gymnosperms would be 0.54 or roughly half that of the angiosperms.

In the absence of additional treatments such as drought or nutrient deficiency, Asat was 10% lower for angiosperms in ambient background O3 compared to CF air (Fig. 2). Relative to pre-industrial conditions, elevated [CO2] projected for the middle of this century ameliorates the impact of ambient background [O3] on angiosperms (Fig. 2). This implies that the impact of the current ambient [O3] will lessen with time. This is consistent with the fact that gs decreases with rising [CO2] (Long et al. 2004) and will therefore decrease CU. However, current projections suggest that [O3] will rise at a similar rate to [CO2], and more in some regions of the temperate Northern Hemisphere (Ehhalt et al. 2001; Denman et al. 2007). So, any decrease in gs caused by rising [CO2] is likely to be offset by a rise in [O3]. Further, Karnosky et al. (2003) reported that despite decreased gs in some trees, damage remains the same for a given [O3] treatment, implying that decreased O3 uptake may be offset by decreased capacity for detoxification in trees grown in elevated [CO2].

The current meta-analysis shows that the detrimental effect of ambient [O3] is less in droughted trees, again a situation where gs and therefore O3 uptake will be decreased (Fig. 2). However, individual studies have suggested that high [O3] exposure may result in increased transpiration and exacerbate drought effects (Maier-Maercker & Koch 1991; McLaughlin et al. 2007), although these studies examined natural variation in [O3] where effects may be confounded with other environmental variables. Grulke et al. (2004) observed night-time opening of stomata in ponderosa pine exposed to elevated [O3]. However, gs was 5–10 times lower than during the day and also less in older trees and at the end of the growing season. Given the diurnal variation in water vapour pressure deficit, this nocturnal opening would likely have a minimal effect on water use. Grulke et al. (2002) noted a sluggish response of the stomata of ponderosa pine exposed to elevated [O3]. However, predicted gs for these plants based on light and water potential was not statistically different from control. Despite these effects of [O3], our analysis shows that on average gs is significantly reduced, suggesting that loss of control may be isolated to certain species and does not appear to reflect the average trend.

Less easily predicted was the finding that lower canopy leaves are more affected than upper canopy leaves. However, this result came from a single study that investigated three species (Novak et al. 2005), so the generality of the result is unknown. It is possible that low or dynamic light conditions cause a decoupling of Asat and gs in shaded leaves of seedlings and saplings, and thus create greater potential for O3 uptake per unit of net photosynthesis (Fredericksen et al. 1996). It is also possible that the shaded leaves are older, and therefore might have a higher CU.

How will future levels of tropospheric O3 impact photosynthesis and gs in trees?

The average current day-time background [O3] in the studies reviewed in this analysis was 40 ppb. Given current emission trends, tropospheric [O3] is projected to rise globally by 20–25% between 2015 and 2050, and 40–60% by 2100 (Meehl et al. 2007). Based on the mean ambient [O3] calculated from data in this analysis, the IPCC projections imply an increase in [O3] from 40 to 48–50 ppb by 2050 and to 56–64 ppb by 2100 for the sites in which the data for this analysis were obtained. Based on the current meta-analysis, this could drive a further 8–16% decrease in Asat caused by rising [O3] (Appendix S4). However, O3 is not the only element of global change, and increasing [CO2], temperature and drought stress will interact with O3 stress.

Surprisingly, angiosperms and gymnosperms showed a similar reduction in Asat under elevated [O3]. One interpretation of this finding is that while current elevations have been insufficient to affect gymnosperms, the increase projected for later in this century will be sufficient not only to further reduce Asat in angiosperms, but also reduce Asat of gymnosperms. This suggests greater sensitivity of Northern Hemisphere forest carbon sinks in the future compared with present conditions (Karnosky et al. 2007; McLaughlin et al. 2007).

Because of the difficulty of studying large and mature trees, young trees and often seedlings and saplings have formed the larger part of most studies of O3 impacts. Older trees were under-represented in the data so preventing a comprehensive analysis of age effects. There were sufficient data to separate effects on trees under and over 4 years. Trees over 4 years showed a greater reduction in Asat and gs because of current background than did trees under 4 years, suggesting greater sensitivity with age (Appendix S3). This is of concern because it suggests by focusing on younger trees, the effect of ambient [O3] on photosynthesis and productivity may be underestimated. The finding is consistent with the observation that during the first 2 years of growth under free-air [O3] enrichment, there were no observed effects on productivity at elevated [O3] for some Populus tremuloides clones, but highly significant effects were apparent in later years (Karnosky et al. 2005). However, this meta-analysis suggests that when [O3] was elevated to 83–84 ppb, damage to Asat appeared greater in the younger trees. This lack of consensus highlights the need for experiments which examine impact of future [O3] on trees from planting through to maturation, as is being conducted in the FACE experiment in Rhinelander, WI, USA (Karnosky et al. 2007).

In the absence of additional environmental modifications, such as elevated [CO2], Asat was reduced by 20% in elevated [O3] of 87 ppb compared to CF air. This reduction was ameliorated when elevated [O3] was combined with elevated [CO2]. Similarly, the detrimental effect of elevated [O3] was ameliorated by drought, likely because gs and therefore [O3] uptake were lower in drought treatments (Fig. 4). Results from aspen FACE suggest that elevated [O3] is sufficient to offset the enhancement in NPP by [CO2] elevated to 550 ppm, and that in some species elevated [O3] will reduce NPP despite a higher [CO2] (King et al. 2005). In all cases in this analysis, the Asat of Populus species was significantly and negatively impacted by [O3], often appearing most sensitive angiosperm. This is significant because Populus trees are major components of forests across the northern temperate and boreal zone and also include important candidate bioenergy crops (Isebrands et al. 2001; Karnosky et al. 2007).

Is there a linear decline in Asat with increasing CU?

The analysis has been limited to the effects based on day-time [O3]. However, CU has been shown to be a more effective predictor of O3 damage (Reich 1987; Nunn et al. 2006; Karlsson et al. 2007; Karnosky et al. 2007; Matyssek et al. 2007). This measure is theoretically more satisfactory, but more difficult to estimate because it requires a simultaneous record of both gs and Asat under various [O3]. Reich (1987) in a review of the limited observations of O3 impacts on tree productivity that had been made at this date showed linear relationships between reduction of Asat and CU. Here, there were sufficient data to undertake this analysis with 28 tree species (Fig. 6). With the variability of species and genotypes within species, coupled with a wide range of locations and experimental conditions, far less of the variability is accounted for by CU, but a significant negative correlation was found (Fig. 6). Some of this variability may also be accounted for by differing capacities for detoxification (Matyssek et al. 2007; Wieser & Matyssek 2007). This suggests that the concept of CU as a predictor of O3 damage (Karnosky et al. 2007; Matyssek et al. 2007) is robust and supports the ‘unifying theory’ proposed by Reich (1987). Our estimated slope predicts a 0.21% decrease in Asat for every mmol m−2 of uptake. This is substantially less than the 0.64% per mmol m−2 averaged across the values given by Reich (1987) for pines and hardwoods, but this may result from the larger database now available and still represents a significant loss of photosynthetic capacity. Our estimate matches annual biomass reduction for less sensitive species predicted by Karlsson et al. (2007) of 0.28% per mmol m−2. Because we use all known data in the peer-reviewed literature to date, 0.21% per mmol m−2 represents the current literature average for loss of photosynthetic capacity with CU. If we assume an average of 14 h daylight over a 150 d growing season, at a mean [O3] of 40 ppb and a mean gs of 185 mmol m−2 s−1, CU would be 48 mmol m−2 which would cause an 11% decline in Asat based on the relationship of Fig. 6. If [O3] rises to 60 ppb by the end of the century, then uptake would rise to 72 mmol m−2 and the decline in Asat would reach 17%, with even larger losses for forests in more polluted areas.

While the effects shown here are not new, we have quantified the current state of knowledge providing the averages and their error limits for two important forest parameters for both terrestrial carbon cycle and regional hydrology models. The significant decreases in both Asat and gs, and the projected further declines, indicate that rising [O3] is negatively affecting both carbon sequestration and water vapour transfer to the atmosphere. Rising surface [O3] and its interaction with forests are an often overlooked aspect of global change. The statistically significant evidence for deleterious impacts on photosynthetic potential averaged across over 350 measurements demonstrates the need to fully incorporate this into future projections of how atmospheric change and forest biomes will interact in effecting future climatic change.

ACKNOWLEDGMENTS

  1. Top of page
  2. ABSTRACT
  3. INTRODUCTION
  4. MATERIALS AND METHODS
  5. RESULTS
  6. DISCUSSION
  7. ACKNOWLEDGMENTS
  8. REFERENCES
  9. Supporting Information

The authors thank Joseph Castro, Charles Chen, Frank Dohleman, Mark Harrison, Fernando Miguez, Shawna Naidu and Xinguang Zhu for useful discussions during the preparation of the databases and manuscript. V.E.W. is supported by a Graduate Research for the Environment Fellowship (GREF), part of the US Department of Energy's Global Change Education Program.

REFERENCES

  1. Top of page
  2. ABSTRACT
  3. INTRODUCTION
  4. MATERIALS AND METHODS
  5. RESULTS
  6. DISCUSSION
  7. ACKNOWLEDGMENTS
  8. REFERENCES
  9. Supporting Information

Supporting Information

  1. Top of page
  2. ABSTRACT
  3. INTRODUCTION
  4. MATERIALS AND METHODS
  5. RESULTS
  6. DISCUSSION
  7. ACKNOWLEDGMENTS
  8. REFERENCES
  9. Supporting Information

Appendix S1. References included in the database for meta-analysis and cumulative ozone uptake analysis. Appendix S2. Effect Sizes (E) 95% Confidence Intervals (CI), degrees of freedom (df) and mean ozone concentrations ([O3]) for categories with significant between-group heterogeneity for trees grown in charcoal-filtered air relative to ambient background ozone concentrations. Appendix S3. Effect Sizes (E) 95% Confidence Intervals (CI), degrees of freedom (df) and mean ozone concentrations ([O3]) for categories with significant between-group heterogeneity for trees grown in charcoal-filtered air relative to elevated ozone treatments. Appendix S4. Effect Sizes (E) 95% Confidence Intervals (CI), degrees of freedom (df) and mean ozone concentrations ([O3]) for categories with significant between-group heterogeneity for trees grown in ambient background ozone relative to elevated ozone treatments.

FilenameFormatSizeDescription
PCE1717_AppendixS1.doc55KSupporting info item
PCE1717_AppendixS2.doc44KSupporting info item
PCE1717_AppendixS3.doc71KSupporting info item
PCE1717_AppendixS4.doc60KSupporting info item

Please note: Wiley Blackwell is not responsible for the content or functionality of any supporting information supplied by the authors. Any queries (other than missing content) should be directed to the corresponding author for the article.