Assessing Ozone Damage To Cutleaf Coneflower in An

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Journal of the Franklin Institute 355 (2018) 6152–6168

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Education Article
Assessing ozone damage to cutleaf coneflower in an
ozone bioindicator garden
Joshua Pringle a,∗, Celine Yu b, Miriam Sachs c, Raluca Ellis d
a The Franklin Institute, Philadelphia, PA, USA
b New York University, New York, NY, USA
c Drexel University Antoinette Westphal College of Media Arts and Design, Philadelphia, PA, USA
d University of Toronto, Toronto, ON, Canada
Received 19 April 2017; received in revised form 20 February 2018; accepted 3 May 2018
Available online 30 May 2018
Abstract
To collect data on ozone pollution and foliar damage, we established the first Philadelphia Ozone
Bioindicator Garden at The Franklin Institute Science Museum. In this paper, we examine the relation-
ship between ozone concentrations in an urban environment and changes in foliar damage in cutleaf
coneflower (Rudbeckia laciniata) plants. Higher ozone concentrations were observed during Summer
2015 than during Summer 2014 at our site. Diurnal analysis reveals a nightly diminishment of ozone’s
rate of dissipation around 4am, which we attributed to intrusions of air from the residual layer (the
layer of air above the boundary layer). We saw that visible foliar injury starts relatively slowly and ac-
celerates beginning in late July for stippling and early August for chlorosis and necrosis. We found that
injury ratings on ozone-damaged leaves progress faster later in the season despite lower ambient ozone
concentrations; we hypothesized that this is evidence of a “latency period” in the cutleaf coneflower’s
foliar injury response to ozone. Cutleaf coneflowers may serve as engaging tools to alert and inform
Philadelphians about air quality issues. Our results suggest that these plants are good candidates for
future work in developing bioindicators of ozone where direct monitoring is not feasible.
© 2018 The Franklin Institute. Published by Elsevier Ltd. All rights reserved.
∗ Corresponding author.
E-mail address: Jxp5328@gmail.com (J. Pringle).
https://doi.org/10.1016/j.jfranklin.2018.05.015
0016-0032/© 2018 The Franklin Institute. Published by Elsevier Ltd. All rights reserved.
J. Pringle et al. / Journal of the Franklin Institute 355 (2018) 6152–6168 6153
Editor’s Note:
The mission of The Franklin Institute is to inspire a passion for learning about science
and technology. One effort in support of that mission is the engagement of high school
students in hands-on science research activities. As this article shows, these young scientists
can become quite knowledgeable. As part of their experience, they learned how to write
scientific articles and about the peer review process. The publication of this educational
article serves as a testament to their good efforts and as inspiration for other young scholars.
Karen Elinich, Directing Editor
1. Introduction
Ozone (O3 ) is an important gas that has diverse beneficial and harmful effects in our at-
mosphere. Ninety percent of Earth’s ozone is found in the stratosphere (15–50 km from the
surface), where it provides protection from UV radiation that is 200 nm to 310 nm in wave-
length [9]. Ozone is also an important greenhouse gas in the mid-troposphere, comprising an
increasing percentage (currently ∼15%) of total anthropogenic radiative forcing [21]. Ozone
and its by-product via photochemical oxidation, the hydroxyl radical (OH), “clean” the atmo-
sphere through reactions with organic compounds, such as methane [19]. However, ozone at
ground level is toxic to humans, animals, and plants as it oxidizes biological tissues [2]. In the
troposphere (surface to 10–15 km), ozone has more than doubled since the industrial revolu-
tion, producing concentrations that are poisonous for living things [15]. In the United States,
ozone is responsible for $500 million in reduced crop production each year [33]. Ground-level
ozone has far-reaching effects on biodiversity and ecosystem services, impacting some species
more than others and affecting how nutrients cycle through the ecosystem [18].
Commonly found at heightened levels in urban regions, ozone is often monitored by local
and state agencies and is regulated by the U.S. Environmental Protection Agency (EPA)
under the National Ambient Air Quality Standards (NAAQS). The standard for ozone is
70 parts per billion (ppb), defined as the 3-year-average of the fourth-highest 8-h-average
concentration for a particular location [36]. Heightened ozone levels aggravate lung diseases
such as asthma, emphysema, and chronic bronchitis in sensitive populations and induce
respiratory problems, including coughing, throat or chest pain, wheezing, and shortness
of breath [32]. Long-term ozone exposure is likely to be one of many causes of asthma
development [32]. Children are particularly affected, given their immature respiratory systems
and their time spent outdoors being physically active. In extreme cases, emergency room
visits may be required and even death can result [37].
Natural sources of ozone in the troposphere include reactions involving gases produced
through lightning and intrusions from the ozone layer in the stratosphere. These, in addition
to pollution transported from overseas, account for northeastern US “background” ozone con-
centrations of around 15–25 ppb during the summertime [41]. Anthropogenic sources of ozone
often push summertime concentrations in excess of 40 ppb, which is the threshold past which
many plants (including crops and trees) exhibit physiological damage and yield reductions [8].
The main mechanism for ground-level ozone formation is the photolysis of nitrogen diox-
ide (NO2 ). The main source of NO2 in cities is the oxidation of nitric oxide (NO), which is a
product of high-temperature fossil-fuel combustion. The intense heat in these combustion re-
actions breaks apart a small fraction of oxygen molecules. The amount of oxygen broken apart
6154 J. Pringle et al. / Journal of the Franklin Institute 355 (2018) 6152–6168
increases with temperature, and around 2700 °C, oxygen is significantly dissociated [12]. The
oxygen atoms can then react with otherwise inert nitrogen (N2 ) according to these reactions:
O2 + heat ↔ O + O (R1)
O + N2 ↔ NO + N (R2)
N + O2 ↔ NO + O (R3)
Overall: 2O2 + N2 + heat ↔ 2O + 2NO (R4)
Next, there are 2 cycles NO may use to manufacture O3 molecules. One is a null cycle,
in which NO and NO2 rapidly convert back and forth on a timescale of minutes, producing
and consuming O3 :
NO + O3 → NO2 + O2 (R5)
NO2 + UV radiation → NO + O (R6)
O + O2 + M → O3 + M (R7)
This cycle results in no net gain of ozone. However, reactions with volatile organic com-
pounds (VOCs) allow for an ozone-production cycle, wherein NO is converted to NO2 without
consuming O3 . In the US, while having declined an estimated 46% since 1990, anthropogenic
VOCs, such as benzene and toluene from gasoline, paints, and industrial processes, are emit-
ted at 11.2 Tg/year, whereas biogenic VOCs, such as isoprene from vegetation, are emitted at
31.8 Tg/year [34]. In this ozone-production cycle, a hydroxyl radical (OH) takes a hydrogen
atom from the volatile organic compound to produce the peroxy radical and water:
VOC + OH + O2 → RO2 + H2 O (R8)
[Where R denotes an organic group]
RO2 + NO → NO2 + RO (R9)
RO + O2 → HO2 + oxidized VOC (R10)
HO2 + NO → NO2 + OH (R11)
[Followed by photolysis of the new NO2 molecules to form O3 (R6) and (R7)]
Overall: VOC + 4O2 → 2O3 + oxidized VOC (NO, NO2 , and OH act as catalysts)
Ozone concentrations are correlated with temperature. Higher temperatures are correlated
with more sunlight, which increases the rate of photolysis of NO2 . In addition, at higher
temperatures, the slowest (and thus, limiting) reactions speed up, leading to a slight enhance-
ment in O3 production [28]. The highest ozone concentrations usually occur on warm and
sunny days, with light winds minimizing dispersal of pollution-laden air.
Many plants are sensitive to ozone exposure. Ozone enters leaves by diffusion through
their stomata. It then reacts with cell components including fats, proteins, nucleic acids,
and carbohydrates, [11] and decomposes to organic radicals and various reactive forms of
oxygen [13]. These may cause many forms of damage, such as reduced fluidity of cell
membranes when free radicals strip electrons from lipids [27]. Damage that is not repaired
or compensated for may become visible as foliar injury or may stunt growth, yield, etc. [31].
Not all O3 exposures cause growth or yield reductions. Ozone only stunts growth or yield
if it affects the limiting factor in plant growth (e.g. nutrient uptake) [31]. However, plants
stressed by ozone may be more susceptible to infections [3]. Stress from ozone damage
causes a response similar to the reaction of plants to pathogen attacks: rapid release of
reactive oxygen species by cells, called oxidative burst [10,40]. Markings from ozone-related
plant damage are most visible in the summertime when concentrations are at their highest,
but ozone can damage plants year-round. For example, chronic ozone exposures affect the
resilience of red spruce (Picea rubins) during winter [7].
Ozone damage is cumulative, increasing with the age of the plant based on the frequency,
concentration, and duration of O3 exposures (even across multiple years for perennials).
Morgan et al. [20] found significant decrease in biomass and seed production in soybeans,
where impact of ozone increased with developmental stage. McKee et al. [17] showed that
ozone causes escalating damage to the photosynthetic capacity of wheat flag leaves over the
growing season. This enhanced response with time may be due to the compounding of the
effects of ozone over the lifespans of the plants.
Plants may minimize ozone damage in two general ways: avoidance (i.e. reducing expo-
sure by stomatal closure), and tolerance [30]. Stomata close in response to several factors,
including drought, humidity, and light intensity [6]. Ozone only causes damage if a sufficient
amount reaches sensitive cellular locations [31]. Ozone injury will not occur if the rate of O3
uptake is low enough that the plant can remove or process the incoming O3 , or if the plant
is able to repair or compensate for the injury [31]. Antioxidants and antioxidant enzymes
play key roles in ozone tolerance. For example, increasing the amount of ascorbic acid, the
most abundant antioxidant in plants, provides greater protection against oxidative damage [4].
In ozone-tolerant species, either oxidative burst is suppressed or damage is confined, which
minimizes visible injury [13]. The cutleaf coneflower (Rudbeckia laciniata) plants monitored
in this study are not ozone-tolerant, as demonstrated in various experiments. For example,
Neufeld et al. [23] reported that the cutleaf coneflower was extremely sensitive to ozone,
while Szantoi et al. [29] found that elevated O3 resulted in significant decreases in cutleaf
coneflower biomass and nutritive quality.
Ozone negatively affects many plant processes including photosynthesis, CO2 photoassimi-
lation, and rate of senescence. These alterations result in dysfunction of transpiration and water
use efficiency, reduction of dry matter production, and yield losses [11]. These ozone-induced
effects at the individual plant level can result in considerable changes in biodiversity because
ozone affects individual species in various ways and intensities. Experimental O3 exposures
reduced growth and flowering of the butterfly bush (Buddleia davidii), and reduced flowers
and fruits in spreading dogbane (Apocynum androsaemifolium) [13]. On the other hand, broad
beans (Vicia faba) infected by rust fungus (Uromyces fabae) gained protection against ozone
[16]. O3 can even impact broad ecosystem services such as carbon storage, water cycling,
and nutrient cycling through downstream effects of individual plant and species damage [18].
Some plant species display visible effects of ozone damage, such as stippling (small dark
spots on the top of the leaf), chlorosis (yellowing, breakdown of chlorophyll), and necrosis
(thorough tissue death). Both acute and chronic exposures to ozone levels above 40 ppb
may result in symptoms of foliar injury on sensitive plants [11]. Visible injury is not always
Fig. 1. Aerial view of the location of The Franklin Institute Ozone Garden.
related to yield loss. Bioindicator systems, which involve plants known to show certain yield
or visual damage sensitivity to ozone levels, are used to show where ozone levels may
affect yield or otherwise disturb plant health [26]. Bioindicator systems may also be valuable
where instrument-based monitoring of ozone is not feasible. In this study, we examine the
response of the cutleaf coneflower bioindicator system to ambient ozone exposure over the
course of a growing season and examine seasonal trends in ozone concentrations in an urban
environment.
2. Methods
2.1. Site description
Meteorological data, ozone concentrations, and plant health measurements were collected
at the Ozone Bioindicator Garden, an educational exhibit located at The Franklin Institute
Science Museum in Philadelphia, Pennsylvania (39°57 30.12 N 75°10 26.01 W; Fig. 1). The
museum is located in Center City, with major roads and highways lying within blocks of the
garden. Pollution from local traffic is thought to influence data collected in the Bioindicator
Garden. The museum building shades the garden in the mornings and, along with nearby
skyscrapers, influences local wind patterns. The garden is situated behind the museum, near
the garage entrance and loading dock.
2.2. Data collection
Leaf Injury Rating training was used in preparation for data collection and is avail-
able online from the National Park Service [22]. The training develops estimation skills
Table 1
The table shows the six rating classes used to assess ozone-induced foliar injury. The classes apply to stippling,
chlorosis, and necrosis.
Class Description
Class 1 = 0% No ozone-induced injury
Class 2 = 1–6% Light ozone-induced injury
Class 3 = 7–25% Moderate ozone-induced injury
Class 4 = 26–50% Moderately severe ozone-induced injury
Class 5 = 51–75% Severe ozone-induced injury
Class 6 = 76–100% Extremely severe ozone-induced injury
Fig. 2. Examples of ozone damage on coneflower bioindicator plants at the Franklin Institute Ozone Garden. Both im-
ages show prominent examples of chlorosis (toward the bottoms of both images). Stippling appears most pronounced
in the upper half of image (b) and necrosis is displayed near the bottom of image (a).
via species-specific online modules. Table 1 shows the six rating classes used to assess
ozone-induced foliar injury.
In addition to measuring height and counting leaves, data collection involved monitoring
three types of visible foliar injury on the bioindicator plants: stippling, chlorosis, and necrosis.
Stippling is a dark spotting that appears only on the upper side of a leaf and does not cross
the veins of the leaf. Chlorosis is the yellowing of a leaf due to a lack of chlorophyll. Necrosis
is the death of leaf tissue, visible as browning and wilting of the leaf (Fig. 2). Chlorosis
and necrosis are more advanced damage types that will, in general, follow the appearance of
stippling [14]. While several trained individuals collected data using visual inspection, one
individual collected the vast majority of the data after the first week, to maximize consistency.
Weekly observations were conducted on the cutleaf coneflower to assess ambient ozone
damage because it is a well-known bioindicator for ozone [26]. Coneflowers are grown from
early spring to late fall, though above or below-average temperatures can lengthen or shorten
the season. Foliar damage data were collected once the plants developed fully-grown leaves
(in June) and collection stopped in September. Leaves were labeled and data were collected
according to visual techniques described in Ladd’s et al. Ozone-Induced Foliar Injury Field
Guide (available to the public at http:// science-edu.larc.nasa.gov/ ozonegarden/ materials-guide.

php), which provides detailed instructions for planting a bioindicator garden.
The garden is equipped with instruments to provide real-time measurements of ozone con-
centrations as well as meteorological data year-round. Ozone concentration was recorded every
five minutes by a model 106-L ozone monitor [1]. The monitor was located in a weatherproof
box attached to an exterior wall of The Franklin Institute. The inlet, located near the bioindi-
cator plants, was connected to the monitor via a 20-foot length line of tubing. The monitor
measures the transmission of UV light, generated by an internal mercury lamp, through a
sample of air using a photodiode [1]. Ozone absorbs ultraviolet (UV) light that is 200 nm to
310 nm in wavelength. The instrument calculates the amount of ozone in the air in parts per
billion by volume (ppbv), using the Beer-Lambert Law. A Vantage VUE weather station from
Davis Instruments is used to measure the temperature, relative humidity, wind direction, wind
speed, and amount of rainfall. The weather monitor is located at the northwest corner of the
garden. Weather and ozone data are transmitted every 5 min automatically to the GO3 Project
website at http://go3project.com, and are available for graphing and download to the public.
2.3. Data analysis
Foliar damage observations were compiled and processed in Igor Pro 6.0 (Wavemetrics,
Lake Oswego, OR), an advanced data processing and analysis software package. The data
were filtered for inconsistencies that were due to human error. For example, stippling, chloro-
sis, and necrosis ratings on leaves should never decrease over time. Out of 1800 total ratings
recorded, there were only three ratings (0.17%) that were lower than prior ratings and in each
instance, the difference was one or two classes (see Table 1 for rating classes). Thus, we expect
no significant positive bias in our data due to the filtering. Ozone and weather data were also
imported into Igor Pro and filtered for spikes (short-lived enhancements of operational param-
eters) due to instrument errors. For example, the temperature jumping from 30 °C to 1000° for
one data point, then returning to 30°, or ozone dropping well below 0 ppb for one data point
and then rebounding were considered errors. The data were initially downloaded from the GO3
project website in 5 min intervals, later averaged to hourly intervals in Igor, then separated into
monthly and seasonal groupings. From the seasonal groupings, diurnal plots were produced
to depict changes in ozone and temperature over the course of an average day in each season.
In our foliar injury analysis, we do not present data sorted by plant, as doing this would add
extraneous information about the setup/geography of our garden. Each plant’s foliar damage
depends to an extent on its sun exposure [5]. Instead, the data were averaged across individual
plants, thus eliminating “noise” that would be merely indicative of our garden layout. Here-
after, hours during which the average ozone concentration was 40 ppb or higher (see Introduc-
tion for the significance of this level in assessing ozone damage) are referred to as “H40”s.
H40 is different from the metric “AOT40” in that H40 only measures the number of hours dur-
ing which 40 ppb is surpassed; it does not measure the extent of exceedance in any given hour.
3. Results and discussion
3.1. Ozone concentration analysis
Fig. 3 shows near-continuous ozone and meteorological data from June 2014 to November
2014. During this time, ozone varied from below the detection limit (4 ppb) to 93.16 ppb,
Fig. 3. Time series of ozone (bottom) and temperature (top) from 2014. Ozone concentrations 40 ppb or greater are
highlighted in purple. (For interpretation of the references to color in this figure legend, the reader is referred to the
web version of this article.)
Fig. 4. Time series of ozone (bottom) and temperature (top) from 2015. Ozone concentrations 40 ppb or greater are
highlighted in purple. (For interpretation of the references to color in this figure legend, the reader is referred to the
web version of this article.)
with higher values occurring during the summer months (meteorological summer, or the
months of June, July, and August). Fig. 4 shows analyzed data from March 2015 to Septem-
ber 2015, with ozone varying from below the detection limit to 136.05 ppb. The largest
concentrations were again observed during the summer months.
Higher ozone levels were observed during Summer 2015 than during Summer 2014 at
our site; the seasonal hourly averages were 38.4 ppb for Summer 2015 and 31.4 ppb for
Summer 2014. Fig. 5 shows a histogram of Summer 2014 ozone and Summer 2015 ozone,
with a line indicating where 40 ppb lies. In 2015, there were 813 H40s, up from 454 in
Fig. 5. Histogram of Summer (June, July, August) 2014 (front, orange) and Summer 2015 (behind, blue) ozone.
(For interpretation of the references to color in this figure legend, the reader is referred to the web version of this
article.)
2014. Furthermore, 80.4% of summer days in 2015 and 54.3% in 2014 had daily maximum
ozone concentrations above 40 ppb. Our data is in agreement with measurements from the
United States Environmental Protection Agency (EPA); 2 out of their 3 sites in the Greater
Philadelphia Area showed an increase in ozone during the summer months from 2014 to 2015
[35]. Ozone concentrations being so distinctly higher in Summer 2015 than Summer 2014 at
our site may be at least partly due to meteorological dynamics. Additionally, in Spring 2015,
the ozone monitor (including its inlet) was moved to be co-located with the garden, which is
closer to the street. However, upon relocation a new line was installed. We hypothesized that
line loss of ozone influenced some of our Summer 2015 data, so ozone data from July 14
to August 31, 2015 was corrected based on data from an identical ozone monitor at Central
High School (40°02 14.7 N 75°09 01.2 W). Apart from July 14 to August 31, 2015, data
was not adjusted because it was comparable to measurements from Central and the EPA.
We display the daily maximum-8-h-averaged ozone data for 2014 and 2015 in Figs. 6 and
7 because this metric is what the EPA uses to determine compliance with its public health pro-
tection standards (see Introduction) [36]. These data were computed based on our time series
data from 2014 and 2015, and similar analysis as we used for the time series may be used here.
As one of six criteria pollutants, ozone is regulated by standards set by the EPA called National
Ambient Air Quality Standards, as required by the Clean Air Act [36]. On April 30, 2012,
based on the 2008 standard, the EPA designated Philadelphia as a “nonattainment” area, with
a classification of “marginal”, meaning Philadelphia exceeded the 2008 standard of 75 ppb by
less than 11 ppb [25,38,39]. “Marginal” is the least severe classification of nonattainment [38].
Fig. 6. Daily maximum-8-h-averaged ozone from 2014.
Fig. 7. Daily maximum-8-h-averaged ozone data for 2015.
Using the latest (2015) NAAQS, according to our data, Philadelphia appears to have ex-
ceeded the ozone concentration standard on 2 days in 2014 and on 18 days in 2015. However,
since we only present 2 years of data while the standard requires 3 years of measurements,
we cannot report on compliance/noncompliance. According to data provided by the EPA
from 4 monitors in the Philadelphia area over the past 3 years (2013–2015), Philadelphia
does appear to have complied with the standard that was in place over those years [35].
Fig. 8. Diurnal ozone (smooth lines) and temperature (lines with plus symbols) from Fall 2014 (blue), Spring 2015
(green), and Summer 2015 (red). (For interpretation of the references to color in this figure legend, the reader is
referred to the web version of this article.)
3.2. Seasonal diurnal behavior
Fig. 8 shows average diurnal ozone and temperature data for Fall 2014, Spring 2015, and
Summer 2015. Examining the temperature plots, we see absolute minima around 7–8 a.m.
This is due to radiational cooling that has occurred throughout the night due to a lack
of sunshine. We see the change in ozone follows the change in temperature, as expected
(see Introduction), indicating the “ozone-production cycle” revving up in the morning and
shutting down in the afternoon. Both temperature and ozone production are primarily driven
by sunlight, however ozone production also receives a slight enhancement from increased
temperatures (see Introduction).
The ozone plots all have either a local maximum or a slowed decrease around 4 a.m. This
could be due to intrusions of air from the residual layer. We know there is no significant new
production of ozone overnight because there is no photolysis of NO2 (R6–R7 in introduction)
in the absence of sunlight. The temperature plots show a much less pronounced “hump”
around the same time, possibly in response to the reduced atmospheric volume and increased
pressure overnight to the diurnal patterns of atmospheric pressure and volume.
Overall, ozone is lower in fall and spring than in summer, as expected due to seasonal
changes in sunlight. Ozone rises more sharply in the afternoon during summer days in
response to intense sunlight. Therefore, we expect to find more substantial visible symptoms
of ozone damage to our coneflowers in the summertime.
Fig. 9. Average progression of stippling (green), chlorosis (yellow), and necrosis (purple) injury ratings from every
observed leaf. (For interpretation of the references to color in this figure legend, the reader is referred to the web
version of this article.)
3.3. Foliar damage analysis
Fig. 9 shows average stippling, chlorosis, and necrosis during our observation period
according to the six rating classes (see Table 1). From this display, we can evaluate which
form of damage is most suitable for monitoring ozone’s effects on the plants. Stippling
increases steadily throughout the season, compared to the more abrupt surges in injury
observed for chlorosis and necrosis in August and again in September. Furthermore, stippling
is only caused by ozone exposure, while there may be other causes of observed chlorosis and
necrosis, including normal senescence. Thus, we rely on stippling to monitor ozone damage
rather than chlorosis or necrosis.
Ozone damage starts relatively slowly and accelerates beginning in late July for stippling,
and early August for chlorosis and necrosis. This shift is more visually pronounced in the
observations than it appears in the time series. Due to the nature of the rating system,
damage ratings 2 (1–6%) and 3 (7–25%) combined comprise the same total percentage of
leaf coverage as do each of the following ratings (4, 26–50%; 5, 51−75%; 6, 76−100%).
Therefore, if the rating system were uniform, categories 2 and 3 would be condensed into
one category, making the earlier slopes of the graphs even flatter, and the later, more vertical
Fig. 10. Average stippling injury ratings by leaf age (top 5 graphs) and the corresponding section of our ozone time
series (bottom). “Leaf 1” is the average “Leaf 1” from every coneflower plant (CF1–CF8). The data are divided
into two periods: the “inception” period (from measurement initiation until the first instance of average Leaf Injury
Rating of 2 or higher) (shaded underneath), and the “expansion” period (from that point until measurement cessation)
(unshaded).
slopes even more dramatic in comparison. One of the results of using this rating system is
that early damage is magnified.
Along with the corresponding section of our ozone time series, Fig. 10 presents the average
stippling injury ratings of our plants by leaf age. “Leaf 1”, for example, is the average “Leaf
1” from every coneflower plant (CF1–CF8). Since it was the first leaf to emerge, Leaf 1 is
at the bottom. Preserving the difference in ages of the leaves (e.g. separating younger leaves
Fig. 11. Linear fit slopes (converted into a “per 10 weeks” unit for better comprehension) for the inception (blue)
and expansion (red) periods in Fig. 10. The linear fits were determined in order to improve understanding of the
rates of ozone damage before and after the injury threshold 2 was recorded. (For interpretation of the references to
color in this figure legend, the reader is referred to the web version of this article.)
from older leaves) shows an undamped look at the progression of stippling. The foliar injury
plots are divided into two periods: the “inception” period (from measurement initiation until
the first instance of average Leaf Injury Rating of 2+), and the “expansion” period (from
that point until measurement cessation). Inception period analysis gives a sense of how long
it took for ozone exposure to start inflicting damage. Expansion period observations help our
understanding of the progression of damage after it was established in the plants.
The lower, older leaves received damage earlier, as expected (see Introduction). The oldest
leaves (Leaf 1) also fell more frequently. When a leaf fell or otherwise disappeared, we
stopped recording data for it. The average leaf that fell had a Leaf Injury Rating of 4.3 for
stippling, 4.4 for chlorosis, and 4.0 for necrosis. Two leaves (out of 40) fell off before the late
July spike in injury ratings, and they each did so with a stippling rating of 2. The remaining
leaves (at the first measurement after the 2 early losses) had an average stippling rating of 1.5.
Thus, early leaf loss does not sufficiently account for the early-season flatness of the slopes.
Later in the season, it became common for leaves to show high amounts of damage. Leaf
loss adds uncertainty to our data, as we do not know how the damage would have progressed
on fallen leaves or how that progression would compare with that of the remaining leaves.
By comparing our time series to our stippling data, we calculate that the average number
of H40s during inception periods was 577, equaling 37% of the hours in the interval. For
expansion periods, the average number of H40s was 317, or 32% of the interval. Fig. 11
examines the linear fit slopes (converted into a “per 10 weeks” unit for better comprehension)
for the inception and expansion periods in Fig. 10. The linear fits were determined in order to
improve understanding of the rates of ozone damage before and after the injury threshold 2
was recorded. The linear fit slopes are higher during the expansion periods, indicating faster
damage progression despite the lower amounts and percentages of H40s late in the season.
Our ozone-weakened leaves undergo a faster rate of damage despite lower concentrations
later in the season and we hypothesize that this is evidence of a “latency period” in the
cutleaf coneflower’s foliar injury response to ozone. If such a latency period is indeed present,
cutleaf coneflowers might not be a good ozone bioindicator system, because visual evidence
of enhanced ozone concentrations does not appear until after the ozone event. However, the
plants can still give visual information about heightened ozone concentrations at a particular
location over the course of a growing season, even if visual damage is delayed. Further
research using controlled studies can quantify the dynamics of this possible latency period.
Researchers may also study the damage displayed by these plants in subsequent years and
compare the patterns of foliar injury response.
4. Conclusion
We presented data on ozone pollution and changes in foliar damage in cutleaf coneflower
(Rudbeckia laciniata) plants in an urban environment from the years 2014 and 2015. Buildings
and pollution from local traffic patterns (including a highway) in Center City Philadelphia in-
fluenced our ozone and foliar injury data. Time series data showed an overall increase in ozone
concentration from 2014 to 2015 at our site. Our diurnal plots of ozone and temperature all
have either a local maximum or a slowed decrease around 4 a.m., which we attributed to intru-
sions of air from the residual layer. Our foliar injury ratings show that injury starts relatively
slowly and accelerates beginning in late July for stippling, and early August for chlorosis
and necrosis. In addition, ozone-damaged leaves appear to receive injury faster despite lower
concentrations later in the season; we hypothesized that this is evidence of a “latency period”
in the cutleaf coneflower’s foliar injury response to ozone. We contribute these data to the
body of knowledge regarding “chamberless” effects of ambient O3 levels on plant health [13].
The cutleaf coneflower may serve as an engaging tool to alert and inform Philadelphians
about air quality issues. Allowing public access to the ozone garden or opening an interactive
exhibit area containing cutleaf coneflower plants may provide good feedback on whether they
are particularly effective engagement tools. Significant foliar damage is a good proxy for high
ozone concentrations; in areas where electronic monitoring of ozone is unfeasible, the plants
may serve as hardy [24] bioindicators, alerting the public of unhealthy air. People could have
their own living pollution monitors; although not responsive to daily fluctuations in ozone, they
would display longer-term trends. As our ozone garden grows, we will continue to explore
original ways we can involve our community in air quality and climate change issues.
Acknowledgments
This research did not receive any specific grant from funding agencies in the public,
commercial, or not-for-profit sectors.
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Assessing Ozone Damage To Cutleaf Coneflower in An

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Journal of the Franklin Institute 355 (2018) 6152–6168

Overall: 2O2 + N2 + heat ↔ 2O + 2NO (R4)

NO2 + UV radiation → NO + O (R6)

VOC + OH + O2 → RO2 + H2 O (R8)

[Where R denotes an organic group]

RO2 + NO → NO2 + RO (R9)

RO + O2 → HO2 + oxidized VOC (R10)

HO2 + NO → NO2 + OH (R11)

2.1. Site description

2.2. Data collection

Guide (available to the public at http:// science-edu.larc.nasa.gov/ ozonegarden/ materials-guide.

2.3. Data analysis

3. Results and discussion

3.1. Ozone concentration analysis

Fig. 6. Daily maximum-8-h-averaged ozone from 2014.

Fig. 7. Daily maximum-8-h-averaged ozone data for 2015.

3.2. Seasonal diurnal behavior

3.3. Foliar damage analysis

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