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.
Lefohn A.S.; Benedict H.M. (1982)
Development of a mathematical index that describes ozone concentration,
frequency, and duration. Atmospheric Environment. 16:2529-2532.
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.
Lefohn A.S.; Runeckles V.C. (1987)
Establishing standards to protect vegetation - Ozone exposure/dose
considerations. Atmospheric Environment. 21:561-568.
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.
U.S. Environmental Protection Agency (1996a) Air Quality
Criteria for Ozone and Related Photochemical Oxidants. Environmental
Protection Agency, Office of Research and Development, Research
Triangle Park, NC. U.S. EPA report no. EPA/600/P-93/004bF.
U.S. Environmental Protection Agency (1996b) Review of
National Ambient Air Quality Standards for Ozone-Assessment of
Scientific and Technical Information. Office of Air Quality Planning
and Standards, Research Triangle Park, NC. EPA-452/R-96-007.
U.S. Environmental Protection Agency (1997) National Ambient
Air Quality Standards for Ozone: Final Rule. Federal Register
62, Number 138, 38855-38896. July 18, 1997.
U.S. Environmental Protection Agency (2006) Review of National
Ambient Air Quality Standards for Ozone-Assessment of Scientific
and Technical Information. Office of Air Quality Planning and
Standards, Research Triangle Park, NC. EPA/600/R-05/004af.
US Environmental Protection Agency
(2013). Integrated Science Assessment of Ozone and Related Photochemical
Oxidants (Final Report). EPA/600/R-10/076F. Research Triangle
Park, NC: Environmental Protection Agency. Available at: http://www.epa.gov/ttn/naaqs/standards/ozone/s_o3_2008_isa.html.
Wang, L., Pang, J., Feng, Z., Zhu,
J., Kazuhiko, K. (2015) Diurnal variation of apoplastic ascorbate
in winter wheat leaves in relation to ozone detoxification. Environmental
Pollutution. 207:413-419.
Washington Post (2008) It's Not a
Backroom Deal If the Call Is Made in the Oval Office by Cindy
Skrzycki. Tuesday, April 8, 2008; Page D02.
Winner, W.E.; Lefohn, A.S.; Cotter, I.S.; Greitner, C.S.;
Nellessen, J.; McEvoy, L.R. Jr.; Olson, R.L.; Atkinson, C.J.;
Moore, L.D. (1989) Plant Responses to Elevational Gradients of
O3 Exposures in Virginia. Proc. Natl. Acad. Sci. USA 86:8828-8832.
Wu, R., Agathokleous, E., Feng, Z. (2021). Novel ozone
flux metrics incorporating the detoxification process in the
apoplast: An application to Chinese winter wheat. Science of
the Total Environment 767 (2021) 144588.
Yun, S-C., Laurence, J.A. (1999). The response of sensitive
and tolerant clones of Populus tremuloides to dynamic ozone exposure
under controlled environmental conditions. New. Phytol. 143:303-313.
