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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

Over the years, vegetation researchers have focused on which part of the distribution curve of the hourly average ozone concentrations were most important for eliciting vegetation effects. During the evolution of thinking, some very interesting hypotheses were presented. In December 1981, at an informal discussion at the US EPA research laboratory in Corvallis, Oregon, Dr. Allen Lefohn asked Dr. David Tingey about the evidence for peak concentrations of ozone being more important than the mid- and lower-level hourly average concentrations. During their discussion, it was concluded that while there was some evidence in the literature for peak ozone concentrations being more important than the lower values for affecting vegetation injury (i.e., dead areas of leaf surfaces), there was no evidence for peaks affecting growth loss to vegetation. At that time, the US EPA was discussing the possibility of proposing as a vegetation standard the seasonal average of the daily 7-h (0900-1600h) average concentration. Dr. Lefohn noted that if the peak hourly average ozone concentrations were more important than the mid- and lower-level concentrations, then the use of a seasonal 7-h average concentration would obscure the occurrence of the peak concentrations and the 7-h average concentration exposure metric would not correlate well with the biologically important peak ozone concentrations at most locations in the US. It was agreed that Dr. Lefohn would design patterns of hourly average ozone concentrations that could be applied in the US EPA's vegetation chamber studies for assessing the importance of peak concentrations (see Hogsett et al., 1985). Lefohn and Benedict (1982), who had been collaborating on the importance of peak ozone concentrations, published a paper in the peer-review literature that proposed that the higher hourly average concentrations should be given greater weight than the mid- and low-level values when assessing crop growth reduction. In 1982, at the Air Pollution Workshop held that year in Riverside, CA, Dr. Lefohn provided a short presentation of the hypothesis that the higher ozone concentrations should be weighted differently than the mid and lower values. Following his presentation, Dr. Robert Musselman introduced himself and mentioned to Dr. Lefohn that he and his research team at UC Riverside had performed an experiment that appeared to support the hypothesis about the importance of the peak concentrations. In 1983, the paper published by Musselman et al. (1983) was the first to provide experimental evidence of the importance of peak hourly average ozone concentrations in affecting vegetation growth and provided important support for the hypothesis associated with the peak values. In 1985, Hogsett et al. (1985), applying the exposure regimes designed by Dr. Lefohn, provided additional evidence of the importance of the higher hourly average ozone concentrations in affecting vegetation.

Although experimental evidence was mounting that higher hourly average concentrations should have greater weighting than lower values for assessing the potential effects of surface ozone on vegetation, in the 1990's, 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 importance of the higher hourly average ozone concentrations in eliciting a plant response. Krupa et al. (1995) suggested that only hourly average concentrations in the range of 50 to 87 ppb were important for assessing vegetation effects and concluded that concentrations > 90 ppb "appeared to be of little importance." Later, these authors 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]. While Legge et al. (1995) agreed that higher concentrations might be important given the right conditions, they concluded that concentrations near or below background levels (i.e., 35-60 ppb) were the best predictors of plant response for European crops.

Several independent analyses appeared 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]) were 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 ozone concentrations above 0.087 ppm appeared 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 ozone 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.

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 ozone injury on tobacco Bel-W3 neither appeared to be an adequate indication of the concentration of ambient ozone nor an adequate indicator for determining the risk of ozone 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 for 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 ozone 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) was 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 not optimum.

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) were difficult to substantiate primarily because the best regression model relating weekly foliar injury scores to various exposure indices was not interpretable (i.e., the coefficient of the SUM60 or N60 (i.e., sum or count of hourly concentrations > 0.06 ppm)) was 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 could be made. The apparent problem of near collinearity among the regressor variables used in stepwise regression provided problems in validating the authors' conclusions.

In view of the discussion that emerged in the scientific literature regarding the importance of high concentrations versus mid-level and lower values, the Canadian Vegetation Objective Working Group (VOWG) evaluated the work described by Krupa et al. (1994, 1995) and Legge et al. (1995). The Canadian working group (1997) concluded there was little support for using an exposure index that focused on the mid-level versus the higher concentrations. The Canadian 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 ozone monitoring sites in Canada (where losses were not observed) than those that occurred at sites which experienced much higher ozone exposures and where documented ozone effects on vegetation occurred. The exposure index used by Krupa et al. (1995) predicted much greater vegetation losses at remote northern areas of Ontario (i.e., Experimental Lakes Area), where crop effects were not 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) had pointed out that although mid-range concentrations were 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 ozone monitoring sites than those sites which experienced much higher ozone exposures where effects had been observed, the Canadian 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 for assessing vegetation effects.


The US EPA (1996a) evaluated the results reported by Tonneijck and Bugter (1991), Krupa et al. (1993, 1994, 1995), and Tonneijck (1994) when assessing the knowledge base for vegetation effects. In its 2006 Ozone Criteria Document, which summarized the effects of ozone on humans and vegetation, the EPA (1996a) concluded that the peak-weighted cumulative exposure indices were appropriate for developing exposure-response relationships to predict ozone vegetation effects (EPA 1996a, 1996b, 1997).


In 1994, research investigators focusing on the atmospheric measurement of deposition and diurnal patterns of ozone and gas exchange at a natural grassland ecosystem (see Gruenhage et al., 1994), Gruenhage and Jaeger (1994) proposed an ambient ozone exposure potential for characterizing ozone uptake. Although the micrometeorological study by the authors was not an effects study and no plant response data were reported, the results introduced the mathematical modeling concept of relating uptake (i.e., flux) with vegetation effects. Their conclusions were based on a micrometeorological study of ozone flux observations above a natural grassland in Germany. A mathematical model describing ozone flux to a meadow was developed and potential injury to the grassland ecosystem was estimated based on their observations. 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.

An observation implicit in Gruenhage and Jaeger (1994) was that the higher hourly average concentrations did not contribute as much as the mid- level values when determining the authors' cumulative atmospheric potential. This was not surprising. One would expect that the relative contribution of the low numbers of higher hourly average concentrations to any cumulative-type index (i.e., cumulative atmospheric potential, SUM06, or W126) would be minimal compared to the more numerous mid-level values. The work challenging the hypothesis of the peak concentrations was similar to the concepts described by Krupa and Legge and co-workers that the relationship between uptake and ozone concentration was solely responsible for determining the vegetation response. In other words, if uptake occurred prior to when peak ozone concentrations occur, then the mid-level and lower values would be more important than the peak values for affecting vegetation. However, a very important factor not quantitatively discussed was the importance of the detoxification of ozone in vegetation and how the detoxification related to the phasing of the uptake (i.e., flux) and the occurrence of the peak ozone concentrations.

Evidence existed, summarized by Musselman and Minnick (2000), that stomates of many plant species open at night and therefore, the potential existed for nocturnal ozone injury and damage to plants. Winner et al. (1989), Matyssek et al. (1995), and Lee and Hogsett (1999) also reported ozone uptake at night. This was an important observation in that it implied that uptake rates at night, much lower than the values observed during daylight hours, had the potential for allowing ozone doses to affect vegetation during this period. Furthermore, Musselman and Minnick (2000) suggested that plant defenses against ozone were likely lower during the night. Over the past several years, research attempted to link the relationship among uptake, ozone exposure, and detoxification with plant effects. Papers by Musselman and Massman (1999), Massman et al. (2000), and Musselman et al. (2006) summarized research efforts to develop a dose-response model that allowed for the establishment of a standard to protect vegetation from ozone. The work by Massman et al. (2000) was particularly intriguing because it developed a model that related exposure and dose and stressed the importance of defense mechanisms that varied as a function of time of day. The term "effective flux" was described as a parameter that took into consideration the detoxification of ozone within the plant. The authors believed that it was the change in the defense component as a function of time of day that perhaps explained 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) stressed that the product of the overlapping mathematical relationships of conductance, concentration, and defense mechanisms resulted 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 maximum hourly average concentrations occurred out of phase with the maximum uptake of ozone. However, as pointed out by Massman et al. (2000), it was 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, might actually define when vegetation was most sensitive to ozone and therefore, support the empirical results that the peaks should be provided greater weight than the mid- and low-level concentrations. In other words, detoxification processes might explain the biological evidence, developed under both experimental conditions and ambient conditions, that, in general, the higher hourly average concentrations were potentially more important than the mid- and low-level hourly average concentrations in eliciting an adverse effect on vegetation.

Work published by Heath et al. (2009), Temporal processes that contribute to nonlinearity in vegetation responses to ozone exposure and dose, presented important biological evidence why the higher hourly average ozone concentrations should be provided greater weight than the mid- and lower-level concentrations for assessing vegetation effects. The publication discussed the linkage of the temporal variability of apoplastic ascorbate with the diurnal variability of defense mechanisms in plants and compared this variability with daily maximum ozone concentrations and diurnal uptake and entry of ozone into the plant through stomata. The paper integrated the three processes (i.e., uptake, ozone exposure, and detoxification) and provided evidence that supported the application of nonlinearity in vegetation responses to ozone exposures and dose. One of the keys to nonlinearity, as described by Heath et al. (2009), was the out-of-phase relationship among uptake, exposure, and detoxification. More information about the Heath et al. (2009) publication and abstract can be found by clicking here.

Grantz et al. (2013), following up on the recommendation by Heath et al. (2009) to characterize diurnal patterns for detoxification, described a plant sensitivity parameter relating injury to ozone dose (uptake) for the crop species, Pima cotton (Gossypium barbadense). The authors reported a diurnal trend in the sensitivity parameter, with maximal sensitivity in mid-afternoon. Grantz et al. (2013) proposed that their sensitivity parameter might be applied as a weighting factor to improve the modeled relationships between either flux or exposure to ozone and vegetation effects. However, Grantz (2014) reported that his sensitivity parameter was not able to differentiate between flux and effective flux. Wang et al. (2015) and Dai et al. (2019) observed diurnal changes of ascorbate in the apoplast and leaf tissues. The authors concluded that detoxification is a dynamic variable that varies by time of day. Goumenaki et al. (2021) noted that their findings were consistent with a role for diel shifts in apoplast AA content and/or redox status determining the reaction of plant tissues to ozone-induced oxidative stress. Wu et al. (2021) in their analysis reported ozone detoxification should be a dynamic variable in flux-based O3 metrics.The results of Wang et al. (2015), Dai et al. (2019), Wu et al. (2021), and Goumenaki et al. (2021) appear to substantiate the discussions in Massman et al. (2000), Musselman et al. (2006), and Heath et al. (2009) that detoxification is a dynamic process that varies over the time of day and thus, supports the importance of the higher ozone concentrations in eliciting adverse effects on vegetation.

Complementing the work by Massman et al. (2000), Musselman et al. (2006), and Heath et al. (2009), results from a "natural experiment" site in the San Bernardino National Forest in California, where substantial reductions over the years in the higher hourly average ozone concentrations in the Los Angeles area occurred, provides independent confirmation of the experimental studies that showed the greater importance of the higher hourly average ozone concentrations in influencing vegetation effects. The San Bernardino site, located near Los Angeles, experienced large reductions in ambient ozone exposures between 1980 and 2000 that were related to improvements in tree conditions (EPA, 2013). The frequency of midrange hourly average ozone concentrations was little changed over this period. EPA (2013) suggested it was the reduction in the higher hourly average ozone concentrations that was responsible for the improvement in tree health.

The W126 ozone exposure index, which preferentially weights higher ozone concentrations, has been considered as the ozone standard to protect vegetation in the US. Musselman et al. (2006) concluded that 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, the US EPA's Clean Air Scientific Advisory Committee (CASAC) recommended that the W126 exposure index, as described by Lefohn and Runeckles (1987) and Lefohn et al. (1988), be adopted as the secondary ozone standard to protect vegetation. CASAC proposed that the W126 exposure index be integrated over a 3-month growing season period measured daily from 0800 to 1959 h. In June 2007, the EPA Administrator, recognizing that the primary standard for ozone did not adequately protect vegetation, proposed a separate secondary standard to protect vegetation using 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 desired to establish the W126 as the secondary ozone standard, the White House (Washington Post, April 8, 2008; Page D02; Federal Register, 2008) instructed the EPA Administrator to establish the secondary ozone standard to be the same as the primary 8-hour average standard (0.075 ppm).

In May 27, 2008, health and environmental organizations filed a lawsuit arguing that the EPA failed to protect public health and the environment when it issued in March 2008 new ozone standards. On March 10, 2009, the US EPA requested that the Court vacate the existing briefing schedule and hold the consolidated cases in abeyance. EPA requested the extension to allow time for appropriate EPA officials that were appointed by the new Administration to review the Ozone NAAQS Rule to determine whether the standards established in the Ozone NAAQS Rule should be maintained, modified, or otherwise reconsidered. EPA further requested that it be directed to notify the Court and the Parties within 180 days of the Court's order vacating the briefing schedule of the actions the Agency has taken or intends to take, if any, with regard to the Ozone NAAQS Rule, and the anticipated time frame for any such actions.

On September 16, 2009, the EPA announced it would reconsider the 2008 national ambient air quality standards (NAAQS) for ground-level ozone for both human health and environmental effects. The Agency planned to propose any needed revisions to the ozone standards by December 2009 and issue a final decision by August 2010. On January 7, 2010, the EPA announced on its website its proposal to strengthen the national ambient air quality standards for ground-level ozone. The EPA proposed decreases in the 8-hour “primary” ozone standard level, designed to protect public health, to a level within the range of 0.060-0.070 parts per million (ppm). EPA proposed to establish a distinct cumulative, seasonal “secondary” standard, referred to as the W126 index, which was designed to protect sensitive vegetation and ecosystems, including forests, parks, wildlife refuges, and wilderness areas. EPA proposed to set the level of the W126 secondary standard within the range of 7-15 ppm-hours. The proposed revisions resulted from a reconsideration of the identical primary and secondary ozone standards set at 0.075 ppm in March 2008. On August 20, the Agency announced that it would delay its final announcement to on or around the end of October. In early November, the EPA announced that it would reach a final decision on the ozone standards by December 31, 2010. On December 8, the EPA announced that it would delay its final decision on the ozone standards until July 2011. EPA announced on July 26 that it would not make a decision on the ozone standards by its previously announced deadline of July 29. On September 2, 2011, President Obama requested that the EPA withdraw its proposal for reconsidered ozone standards. The President indicated that the EPA was currently reviewing the available literature on ozone effects on human health and vegetation and would provide recommendations to him in 2013.

In August 2014, the EPA Staff recommended to the Administrator that she select the ozone primary standard at a specific level between 60-to-70-parts-per-billion. For the secondary standard, the EPA Staff recommended that the Administrator establish a 3-month, 12-h W126 secondary standard, which would have a specific value within the range of 7 to 17 ppm-h. On November 26, 2014, the EPA Administrator announced that she was proposing an ozone human health (primary) standard in the range of 65 to 70 ppb and would take comment on a standard as low as 60 ppb. For the welfare (secondary) ozone standard, she proposed that the standard be the same as the health standard if the final health standard were set in the range of 65 to 70 ppb. The Administrator believed that a health standard in this range would protect vegetation from ozone exposures of W126 values within the range of 13-17 ppm-h. She also took comment on setting a W126 value in the range of 7-13 ppm-h, which implied that she was still considering establishing a secondary standard separate in form from the human health 8-h standard. In October 2015, the Administrator concluded that protection of vegetation from adverse effects could be provided by an 8-h O3 standard of 70 ppb that restricted cumulative 3-month seasonal W126 exposures to 17 ppm-hrs or lower. Five years later, following a review of the 2015 ozone standards, the Administrator on December 23, 2020 made the decision that both the human health and vegetation ozone standards would remain at the current levels established in 2015. Following this decision, on October 29, 2021, the Agency announced it would reconsider the 2020 O3 NAAQS final action. During the reconsideration process, CASAC recommended to the Administrator that the form of the secondary standard should be changed to the cumulative W126 exposure metric, an index recommended by several previous CASAC ozone panels, as well as at times by the EPA, to protect vegetation. CASAC recommended that the Administrator consider that the level of the W126 metric be in the range of 7 to 9 ppm-hrs. Upon considering the CASAC recommendations for the human health and vegetation ozone standards as part of the reconsideration process, in August 2023 the EPA decided to initiate a new review of the ozone NAAQS, which meant that the entire ozone rulemaking process would begin once again. The current 70 ppb 8-h O3 standard promulgated in the US EPA's 2015 decision (Federal Register, 2015) serves as a surrogate to achieve O3 levels at or below a W126 value of 17 ppm-hrs, which is above the range of W126 values of 7 to 9 ppm-hrs recommended by CASAC.

Our research continues on bridging the gap between ozone exposure and ozone dose (i.e., flux). As indicated above, detoxification represents a process, which has been mostly overlooked in assessing vegetation effects. The first two processes are uptake and ozone concentration. It is the temporal relationship among these three processes that determines the resulting vegetation effects. Without including these three processes, it is impossible to apply a flux model to predict adequately vegetation effects. When considering only uptake and concentration, the flux models predict that the peaks are less important than the mid-level ozone concentrations in affecting vegetation. As indicated in Musselman et al. (2006), the use of a fixed threshold in the flux-based approach may not be an appropriate way to address detoxification processes because of changing detoxification during the day. The results reported by Wang et al. (2015), Dai et al. (2019), Wu et al. (2021), and Goumenaki et al. (2021) appear to substantiate this observation. It is anticipated that when models begin to consider the diurnal variability of detoxification, predictions will begin to agree with the controlled and ambient experimental results that illustrate the importance of the higher hourly average ozone concentrations and that the lower concentrations are not playing as important roles as the higher concentrations in eliciting an adverse effect on vegetation. If you wish to look further into this fascinating research area, please carefully read the critical review written by Musselman et al. (2006) on the subject of ozone effects on vegetation and the discussions by Massman et al. (2000), Heath et al. (2009), Wang et al. (2015), Dai et al. (2019), Wu et al. (2021), and Goumenaki et al. (2021) on the importance of the diurnal variation of ozone detoxification. The synergism provided by reading the papers is important in better understanding how to combine ozone exposure and dose so that predictive models in the future will incorporate "effective flux", which will use diurnal detoxification, to assess vegetation effects. Musselman et al. (2006) concluded that "... because there is considerable uncertainty in quantifying the various defense mechanisms, effective flux at this time is difficult to quantify. Without adequate effective flux-based models, exposure-based O3 metrics appear to be the only practical measure for use in relating ambient air quality standards to vegetation response." The conclusions reached by Musselman et al. (2006) stated in 2006 appear to be still relevant in 2024.

 

Interesting Background Reading References

Canadian Vegetation Objective Working Group (1997) Canadian 1996 NOx/VOC Science Assessment. Report of the Vegetation Objective Working Group. ISBN-1-896997-12-0. Science Assessment and Policy Integration Division, Atmospheric Environment Service, Environment Canada. Toronto, Ontario.

Dai, L., Feng, Z., Pan, X., Xu, Y., Li, P., Lefohn, A.S., Harmons, H., Kobayashi, K. 2019. The detoxification by apoplastic antioxidants is insufficient to remove the harmful effects of elevated ozone in tobacco, soybean and poplar. Environ. Pollut. 245: 380-388. DOI: https://doi.org/10.1016/j.envpol.2018.11.030

Federal Register (2008). Environmental Protection Agency. National Ambient Air Quality Standards for Ozone; Final Rule. 40 CFR Parts 50 and 58. March 27, 2008. Volume 73, No. 60. p. 16497.

Federal Register, National Ambient Air Quality Standards for Ozone (2015). 40 CFR Part 50, 51, 52, 53, and 58, pp 65292-65468.

Goumenaki, E., González-Fernández, I., and Barnes, J. D. (2021). Ozone uptake at night is more damaging to plants than equivalent day-time flux. Planta 253, 75. https://doi.org/10.1007/s00425-021-03580-w.

Grantz, D.A.; Vu, H.-B. ; Heath, R.L.; Burkey, K.O. (2013). Demonstration of a diel trend in sensitivity of Gossypium to ozone: a step toward relating O3 injury to exposure or flux. Journal of Experimental Biology. doi:10.1093/jxb/ert032.

Grantz, D.A. (2014). Diel trend in plant sensitivity to ozone: Implications for exposure- and flux-based ozone metrics. Atmospheric Environment 98:571-580.

Gruenhage, L.; Jaeger, H.-J. (1994). Influence of the atmospheric conductivity on the ozone exposure of plants under ambient conditions: Considerations for establishing ozone standards to protect vegetation. Environ. Pollut. 85:125-129.

Gruenhage, L.; Daemmgen, U.; Haenel, H.J.; Jaeger, H.-J. (1994) Response of a grassland ecosystem to air pollutants: III - The chemical climate: vertical flux densities of gaseous species in the atmosphere near the ground. Environ. Pollut. 85:43-49.

Gruenhage, L.; Jaeger, H.-J.; Haenel, J.-D.; Loepmeier, F.-J.; Hanewald, K. (1999). The European critical levels for ozone: improving their usage. Environmental Pollution. 105:163-173.

Heath, R. L.; Lefohn, A. S.; Musselman R. C. (2009). Temporal processes that contribute to nonlinearity in vegetation responses to ozone exposure and dose. Atmospheric Environment 43:2919-2928.

Hogsett, W.E.; Tingey, D.T.; Holman, S.R. (1985). A programmable exposure control system for determination of the effects of pollutant exposure regimes on plant growth. Atmos. Environ. 19:1135-1145.

Krupa, S.V.; Manning, W.J.; Nosal, M. (1993) Use of tobacco cultivars as biological indicators of ambient ozone pollution: An analysis of exposure-response relationships. Environ. Pollut. 81: 137-146.

Krupa, S.V.; Nosal, M.; Legge, A.H. (1994) Ambient ozone and crop loss: Establishing a cause-effect relationship. Environ. Pollut. 83:269-276.

Krupa, S.V., Gruenhage, L.; Jaeger, H.-J.; Nosal, M.; Manning, W.J.; Legge, A.H.; Hanewald, K. (1995) Ambient ozone (O3) and adverse crop response: A unified view of cause and effect. Environ. Pollut. 87:119-126.

Lee, E.H.; Hogsett, W.E. (1999) Role of concentration and time of day in developing ozone exposure indices for a secondary standard. J. Air & Waste Manage. Assoc. 49:669-681.

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Lefohn, A.S.; Edwards, P.J.; Adams, M.B. (1994) The characterization of ozone exposures in rural West Virginia and Virginia. J. Air Waste Manag. Assoc. 44:1276-1283.

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Lefohn A.S.; Lawrence J.A.; Kohut R.J. (1988) A comparison of indices that describe the relationship between exposure to ozone and reduction in the yield of agricultural crops. Atmospheric Environment. 22:1229-1240.

Lefohn, A.S.; Shadwick, D.S.; Somerville, M.C.; Chappelka, A.H.; Lockaby, B.G.; Meldahl, R.S. (1992) The characterization and comparison of ozone exposure indices used in assessing the response of loblolly pine to ozone. Atmos. Environ. 26A:287-298.

Legge, A.H.; Gruenhage, L.; Nosal, M.; Jaeger, H.-J.; Krupa, S.V. (1995) Ambient and adverse crop response: An evaluation of North American and European data as they relate to exposure indices and critical levels. Angew. Bot. 69:192-205.

Massman, W.J. (2004) Toward an ozone standard to protect vegetation based on effective dose: a review of deposition resistance and a possible metric. Atmos. Environ. 38: 2323-2337.

Massman, W.J.; Musselman, R.C.; Lefohn, A.S. (2000). A conceptual ozone dose-response model to develop a standard to protect vegetation. Atmospheric Environment. 34(5):745-579.

Matyssek, R.; Gunthardt, M.S.; Maurer, S.; Keller, T. (1995). Nighttime exposure to ozone reduces whole-plant production in Betula pendula. Tree Physiology 15, 159-165.

Musselman, W.J.; Massman, W.J. (1999). Ozone flux to vegetation and its relationship to plant response and ambient air quality standards. Atmospheric Environment. 33:65-73.

Musselman, R.C.; Minnick, T. (2000). Nocturnal stomatal conductances and ambient air quality standards for ozone. Atmospheric Environment. 34(5):719-733.

Musselman, R.C.; McCool, P.M.; Lefohn, A.S. (1994) Ozone descriptors for an air quality standard to protect vegetation. J. Air Waste Manag. Assoc. 44(12):1383-1390.

Musselman, R.C.; Oshima, R.J.; Gallavan, R.E. (1983). Significance of pollutant concentration distribution in the response of 'red kidney' beans to ozone. J. Am. Soc. Hortic. Sci. 108:347-351.

Musselman R. C., Lefohn A. S., Massman W. J., and Heath, R. L. (2006) A critical review and analysis of the use of exposure- and flux-based ozone indices for predicting vegetation effects. Atmospheric Environment. 40:1869-1888.

Tonneijck, A.E.G. (1994) Use of several plant species as indicators of ambient ozone: Exposure-response relationships. In: Critical Levels for Ozone - A UN- ECE Workshop Report (J. Fuhrer and B. Achermann, Editors). Proceedings of the UN-ECE Workshop on Critical Levels for Ozone, Bern, Switzerland, November 1-4, 1993. 1994, pp. 288-292. Published by the Swiss Federal Research Station for Agricultural Chemistry and Environmental Hygiene CH-3097 Liebefeld-Bern, Switzerland.

Tonneijck, A.E.G.; Bugter, R.J.F. (1991) Biological monitoring of ozone effects on indicator plants in the Netherlands: Initial research on exposure-response functions. VDI Berichte 901:613-624.

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