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Bridging the Gap Between Ozone Exposure and Ozone Dose: The Importance of High Hourly Average Concentrations for Affecting Vegetation

Copyright by A.S. Lefohn

Lefohn and Benedict (1982) proposed that the higher hourly average concentrations should be given greater weight than the mid- and low-level values when assessing crop growth reduction. The experimental results reported by Musselman et al. (1983) and Hogsett et al. (1985) illustrated the importance of these higher hourly average ozone concentrations in affecting vegetation. Confirming the results reported by Musselman et al. (1983) and Hogsett et al. (1985), using the identical SUM06 exposure index values, Yun and Laurence (1999) reported that the exposure regime that contained the higher hourly average concentrations resulted in greater vegetation effects than the regime that experienced the lower hourly average concentrations.

An important question was raised in the 1990s regarding whether the high hourly average concentrations should have greater weighting than lower values for assessing the potential effects of surface ozone on vegetation. Tonneijck and Bugter (1991), Krupa et al. (1993, 1994, 1995), Gruenhage and Jaeger (1994), Tonneijck (1994), and Legge et al. (1995) published papers questioning the current understanding of the peer-review literature that higher hourly average ozone concentrations are more important than the mid- and lower-level values in eliciting a plant response. Krupa et al. (1995) suggest that only hourly average concentrations in the range of 50 to 87 ppb are important for assessing vegetation effects and conclude that concentrations > 90 ppb "appeared to be of little importance." These authors have modified their previous statement by explaining "While this overall conclusion does not negate the importance of peak hourly O3 concentrations if they occur at the right time of the day, it is important to note that as ambient hourly O3 concentrations reach peak concentrations, their frequency of occurrences decline and so do the properties of atmospheric (O3 flux) and plant (uptake) conductance" [Legge et al., 1995]. However, while Legge et al. (1995) agree that higher concentrations might be important given the right conditions, they conclude that concentrations near or below background levels (i.e., 35-60 ppb) are the best predictors of plant response for European crops.

Several independent analyses appear to contradict the conclusion reached by Krupa et al. (1994) and Legge et al. (1995) that mid-level concentrations (values between 0.050 ppm and 0.087 ppm [Krupa et al., 1994, 1995] or between 0.035 ppm and 0.060 ppm for European crops [Legge et al., 1995]) are more important than the higher hourly average concentrations (e.g., values greater than 0.060 for European crops and 0.087 ppm for U.S. crops). Using the EPA's National Crop Loss Assessment Network (NCLAN) data, Musselman et al. (1994) reported that hourly average O3 concentrations above 0.087 ppm appear to be more important contributors to crop losses than hourly average concentrations below 0.087 ppm. Similar to these findings, Lefohn et al. (1994), using the results of an Auburn University intensive field research study assessing the effects of O3 on two loblolly pine half-sibling families (Lefohn et al., 1992), pointed out that the hourly average concentrations above 0.087 ppm appeared to play a more important role in determining growth reductions than mid-level values. Similarly, Lefohn et al. (1994) commented on the inconsistency in applying the Krupa et al. hypothesis when actual ambient data were applied.

With conflicting results, who is correct? In order to answer this question, one has to carefully critique the series of papers that challenge the current thinking that higher hourly average concentrations are more important than the mid and lower values. The works by Tonneijck and Bugter (1991) and Tonneijck (1994) were not designed to test the importance of peak versus mid or low levels of ozone. Tonneijck and Bugter (1991) concluded that O3 injury on tobacco Bel-W3 neither appeared to be an adequate indication of the concentration of ambient O3 nor an adequate indicator for determining the risk of O3 injury to other plant species or to vegetation as a whole. After reporting a poor relationship between ambient ozone and tobacco response, Tonneijck (1994) used data obtained from the Dutch monitoring network in the period 1979-1983 to explain injury response in tobacco Bel-W3 and bean. The author concluded that the results did not support the overall concept that higher concentrations of O3 were more important than lower values in eliciting a response because the higher concentrations did not necessarily cause the greater effects. The work reported by Tonneijck (1994) is difficult to substantiate because (1) latent variables, particularly climate, were important and were excluded in their analysis of unplanned data and (2) the power of their statistical approach was weak.

Krupa et al. (1993) concluded that the best predictors of foliar injury on tobacco Bel-W3 were exposure indices that focused on the mid levels of ozone. The conclusions reached by Krupa et al. (1993) are difficult to substantiate primarily because the best regression model relating weekly foliar injury scores to various exposure indices is not interpretable, i.e., the coefficient of the SUM60 or N60 (i.e., sum or count of hourly concentrations > 0.06 ppm) is negative and not directionally correct, a clear indication of problems of near linear dependency among indices such that little or no distinction of the relative influence of the exposure indices on injury response can be made. The apparent problem of near collinearity among the regressor variables used in stepwise regression provide problems in validating the authors' conclusions.

In view of the discussion that had emerged in the scientific literature regarding the importance of high concentrations versus mid-level and lower values, the Canadian Vegetation Objective Working Group (VOWG) thoroughly evaluated the work described by Krupa et al. (1994, 1995) and Legge et al. (1995). The Canadian working group (1997) concluded that there was little support for using an exposure index that focused on the mid-level versus the higher concentrations. The findings were based on the following:

  • Cumulative exposure indices that focused on the higher hourly average concentration performed considerably better in exposure-response models than the index proposed by Krupa et al. (1995), which focused on the mid-level values.
  • Inaccurate use by Krupa et al. (1994, 1995) of some of the NCLAN data were identified.
  • The exposure index that focused on the mid-level concentrations predicted greater losses to vegetation at remote ambient O3 monitoring sites in Canada (where losses were not observed) than those that occurred at sites which experienced much higher O3 exposures and where documented O3 effects on vegetation have occurred. The exposure index predicted much greater vegetation losses at remote northern areas of Ontario (i.e., Experimental Lakes Area), where crop effects have not been documented. Similarly, high losses were predicted for remote areas in Cormack, Newfoundland, and Vegreville, Alberta.

In continuing its review, the Working Group noted that Legge et al. (1995) have pointed out that although mid-range concentrations are important, if high concentrations were to occur during the time of day when plants were most sensitive, then the higher concentrations would also be important. However, based on its observation that the exposure index that focused on the mid-level concentrations predicted greater losses at remote ambient O3 monitoring sites than those sites which experienced much higher O3 exposures where effects had been observed, the Working Group concluded that the results reported by Legge et al. (1995) were difficult to rationalize. The Working Group (1997) concluded that there was sufficient evidence that cumulative exposure indices that weight the higher hourly average concentrations more than the mid levels should be used for developing exposure-response relationships.


EPA (1996a) has evaluated the results reported by Tonneijck and Bugter (1991), Krupa et al. (1993, 1994, 1995), and Tonneijck (1994). In the Ozone Criteria Document, which summarizes the effects of ozone on humans and vegetation, the EPA (1996a) reviewed the statistical procedures reported by Krupa et al. (1994 and 1995) and concluded that the peak-weighted cumulative exposure indices were appropriate for developing exposure-response relationships to predict O3 vegetation effects (EPA 1996a, 1996b, 1997).


Based on atmospheric measurement of deposition and diurnal patterns of O3 and gas exchange at a natural grassland ecosystem (see Gruenhage et al., 1994), Gruenhage and Jaeger (1994) proposed an ambient O3 exposure potential for characterizing O3 uptake. The micrometeorological study by the authors is not an effects study and no plant response data were reported. Their conclusions were based on a micrometeorological study of O3 flux observations above a natural grassland in Germany. A mathematical model describing O3 flux to a meadow was developed and potential injury to the grassland ecosystem was estimated based on their observations. Effects data were not used by Gruenhage and Jaeger (1994) in their model. Gruenhage and Jaeger (1994), using their atmospheric exposure potential approach, concluded that mid-level hourly average concentrations (0.05-0.09 ppm) were more important than the higher concentrations (> 0.09 ppm) for the grassland vegetation grown, in 1990 and 1991, at their site. Gruenhage and Jaeger have since combined their work with others in the application of their observations (Krupa et al., 1994, 1995) and Legge et al. (1995).

It is inappropriate to use the meteorological observations made at the German grassland site for the purpose of deriving a model that predicts the potential effect on vegetation for every hourly average ozone concentration anywhere in the world at any time. Not every plant species behaves in the same manner as the German grassland ecosystem did in 1991 and 1992. In addition, every model has sets of key assumptions that may or not be correct on a universal basis. Similarly, not every agricultural rural site in the world has the same exposure characteristics as those found for the site in Germany. As noted by Musselman et al. (1994), hourly average concentrations greater than or equal to 0.10 ppm occur frequently at many rural agricultural and forested sites in the United States, in contrast with that observed at the grassland research site in Germany. Second, unlike the O3 exposure dynamics reported by Gruenhage and Jaeger (1994), Musselman et al. (1994) found that for most rural agricultural and forested sites in the United States the higher hourly average concentrations occurred during the 0900-1559h daylight window. The authors pointed out that more than 50% of the hourly average concentrations greater than or equal to 0.10 ppm occurred during this potentially biologically important period.

Another observation implicit in Gruenhage and Jaeger (1994) was that the higher hourly average concentrations did not contribute as much as the mid- level ones when determining the cumulative atmospheric potential. This is not surprising. One would expect that the contribution of higher hourly average concentrations to any cumulative-type index (i.e., cumulative atmospheric potential, SUM06, or W126) would be minimal in relation to the mid-level values when the number of higher hourly average concentrations is small. However, this observation should not be generalized because the relative role of hourly average concentrations in the final summation of the atmospheric exposure potential is dependent upon the distribution of the hourly average concentrations, which will vary from site to site and from year to year. Hourly average concentrations greater than or equal to 0.10 ppm will have a greater contribution to the cumulative sum of the atmospheric exposure potential values at many rural sites in the United States than at the rural grassland ecosystem site in Germany. It is inappropriate to use the relative roles of the high- and mid-level hourly average concentrations in a cumulative sum of either (1) an atmospheric exposure potential or (2) exposure indices, such as the W126 or SUM06, to examine the concept that the highest hourly average concentrations have a greater potential to elicit an adverse effect on vegetation than the lower values. The concept of higher concentrations being more important than the mid and lower levels is biologically based and is invariant to the mathematical distribution of the hourly average concentrations or the time of day of occurrence at a specific site.

The papers by Krupa et al. (1993, 1994, 1995), Tonneijck and Bugter (1991), and Tonneijck (1994), Gruenhage and Jaeger (1994), and Legge et al. (1995) have raised some interesting questions about relating ozone exposure and dose for the purpose of predicting effects on vegetation. In my own papers, I have stated that exposure is not a perfect surrogate for dose and have cited examples where field studies have confirmed inconsistent relationships. There always will be examples when the exposure is high, but the uptake is low, and the vegetation effects are minimal. However, while a set of physical observations obtained at a grassland ecosystem for two years can be used in a model for the purposes of developing a concept, one should not assume that the collected meteorological and carbon dioxide uptake data are representative of all physical sites and plant species. For example, Gruenhage et al. (1994) found that the maximum deposition velocity for ozone occurring at their site in Germany was around 1100h in the morning. The maximum hourly average concentration of ozone occurred near 1600h. Thus, as observed by Gruenhage et al. (1994), the maximum hourly average concentrations occurred out of phase with the maximum uptake of ozone and thus, they concluded that the higher highly average concentrations are not that important for affecting vegetation. However, for

maize and beech,

alfalfa,

and

ponderosa pine

grown elsewhere, periods of uptake during the day are quite different than the observations of Gruenhage et al. (1994). Note that unlike the findings reported by Gruenhage and Jaeger (1994), some plants appear to be sensitive to ozone exposure during the part of the day when high hourly average concentrations occur at many sites in the United States (e.g., 0900-1600h). In addition, work by Musselman and Minnick (2000) report that stomates can be open at night and therefore, the potential exists for noctural ozone injury and damage to plants, which has been reported by Winner et al. (1989), Matyssek et al. (1995), and Lee and Hogsett (1999).

To perform the experiment correctly, the following data are needed from the same site: (1) micrometeorological information, (2) uptake rates unique to vegetation species, (3) quantified defense estimates as a function of time of day, and (4) documented vegetation effects. By performing a series of experiments across many geographical areas under different conditions, one may be able to develop a generalized approach that incorporates hourly average concentrations with atmospheric conditions and biological uptake for predicting vegetation effects. At this time, when one takes a closer look at the set of papers that hypothesize that midrange hourly average ozone concentrations (e.g., 50 to 90 ppb) are more important than the high range for vegetation effects purposes, the evidence simply is not there. Lee and Hogsett (1999), after reviewing the analyses by Krupa and co-workers, concluded that "evidence suggesting that plants show greater response to mid-range hourly average O3 concentrations (0.05-0.09 ppm) than to high concentrations (>0.09 ppm) cannot be justified because of flaws in the statistical approaches or limitations in design and inference due to data sets with few exceedances of 0.10 ppm."

The data are not available to extrapolate the grassland findings in Germany to other sites as the authors have done in the papers with Krupa et al. (1994, 1995) and Legge et al. (1995). It is desirable to develop a linkage between O3 exposure and actual O3 uptake by vegetation so that a dependable standard or critical level can be established to protect vegetation. However, given the variation in a plant's daily and developmental sensitivity, it appears, at this time, that models that link O3 exposure with vegetation uptake, quantifiable defense mechanisms, and effects are not yet dependable enough to be useful for the standard-setting process. The current flux models that are linked with effects, ignore defense mechanisms and assume that plants have no immune systems. This assumption is incorrect.

Based on the research results published in the peer-review literature, the U.S. EPA (2006) currently concludes that higher hourly average concentrations have greater potential than the mid-level concentrations to elicit an adverse vegetation effect. This does not mean that mid- and lower hourly average concentrations are not important, but rather that a disproportionate weighting should be given to the higher values. Gruenhage et al. (1999) note that "at the present time, for plants other than wheat, the data base is too small to derive meaningful and reliable effective dose-response relationships."

Over the next several years, research will continue to attempt to develop dose uptake models that predict vegetation effects. However, just as important, will be the attempts to link the more numerous measurements of ozone exposure in the ambient air with dose uptake, quantifiable defense mechanisms, and plant effects. Research is progressing nicely in this evolving field. Papers by Musselman and Massman (1999), Massman et al. (2000), and Musselman et al. (2006) summarize current efforts to develop a dose-response model that would allow for the establishment of a standard to protect vegetation from ozone. The work by Massman et al. (2000) is particularly intriguing because it develops a model that relates exposure and dose and stresses the importance of defense mechanisms that vary as a function of time of day. It is the change in the defense component as a function of time of day that may explain the biologically based observation that the higher hourly average concentrations should be weighted greater than the mid- and lower- values in predicting vegetation damage from ozone. Massman et al. (2000) and Massman (2004) stress that the product of the overlapping mathematical relationships of conductance, concentration, and defense mechanisms results in a much different picture of potential impact to vegetation than just the use of conductance and concentration in predicting vegetation effects.

As indicated above, Gruenhage et al. (1994) found that the the maximum hourly average concentrations occurred out of phase with the maximum uptake of ozone. However, as pointed out by Massman et al. (2000), it is important to quantify the relationship among concentration exposure, ozone uptake, and the ability of defense mechanisms to neutralize some of the ozone update as a function of time of day. Thus, although the maximum hourly average concentrations occurred out of phase with the maximum uptake of ozone as reported by Gruenhage et al. (1994), the defense mechanisms or repair mechanisms, varying as a function of time of day, may actually define when vegetation is most sensitive to ozone. As indicated above, biological evidence developed under both experimental conditions and ambient conditions indicate that, in general, the higher hourly average concentrations are potentially more important than the mid- and low-level hourly average concentrations in eliciting an adverse effect on vegetation. As indicated above, actual results in the field collected under ambient conditions support these findings.

We are continuing our collaboration with researchers from around the world in developing flux-based ozone models, which include the quantification of defense mechanisms, to describe the relationship between exposure, dose, vegetation effects, and the standard-setting process. However, until research results are readily available that explore the "neutralizing capacity" that defense mechanisms may have on ozone update, any attempt to ozone establish standards or critical levels based on flux, without including defense mechanisms in flux-based models, will result in serious inconsistent predictions that are therefore not reliable.

As indicated in Musselman et al. (2006), at this time, the exposure-based indices appear to be to be the only practicable measure for use in relating ambient air quality to vegetation response. At its August 24-25, 2006 meeting in Durham, North Carolina, EPA's Clean Air Scientific Advisory Committee (CASAC) recommended that the W126 exposure index, as described by Lefohn and Runeckles (1987), become the secondary ozone standard to protect vegetation. CASAC proposed that the W126 exposure index would be integrated over a 3-month growing season period measured daily from 0800 to 1959 hr. In June 2007, the EPA Administrator proposed the W126 exposure index as the secondary ozone standard. On March 12, 2008, the EPA Administrator made the final decision on the human health and vegetation ozone standards. EPA revised the 8-hour "primary" ozone standard, designed to protect public health, to a level of 0.075 parts per million (ppm). The previous standard, set in 1997, was 0.08 ppm. Although the EPA Administrator recommended the W126 as the secondary ozone standard, based on advice from the White House (Washington Post, April 8, 2008; Page D02; Federal Register, 2008), the EPA Administrator made the secondary ozone standard the same as the primary 8-hour average standard (0.075 ppm).

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