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 "smooth"
the occurrence of the peak concentrations and the 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). Soon after this discussion, results
published by 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. In 1982,
at the Air
Pollution Workshop held that year in
Riverside, CA, Dr. Lefohn provided a short presentation on his
hypothesis about the importance of the higher concentrations
in comparison to 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
Although it appeared that the experimental
evidence was mounting that high 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
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
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 that 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 iin 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. Their results appear to substantiate the work
of Massman et al. (2000), Musselman et al. (2006), and Heath
et al. (2009).
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.
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).
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
web site 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 will provide recommendations to him in 2013.
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 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. 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.
Follwing 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. The
current 70 ppb 8-h O3 standard as per 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.
Our research continues on bridging
the gap between ozone exposure and ozone dose (i.e., flux).
As indicated above, detoxification represents a third 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 the changing patterns associated with detoxification during
the day. The results reported by Wang et al. (2015), Dai et al.
(2019), and Wu 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) and Heath
et al. (2009) 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 2022.
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.
Federal Register, National Ambient Air Quality Standards
for Ozone (2015). 40 CFR Part 50, 51, 52, 53, and 58, pp 65292-65468.
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.
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