EPA-600/1-76-027b
August 1976 Environmental Health Eilects Research Series
OZONE AND OTHER PHOTOCHEMICAL OXIDANTS
Volume 2 (Chapters 8-15.)
.{*»
"Health Effects Research Laboratory
. , n . . n ,
ice of Research and Development
U.S. Environmental Protection Agency
Research Triangle Park, North Carolina 27711
-------
Ozone
and Other
Photochemical
Oxidants
Volume 2 of 2 Volumes
Subcommittee on Ozone and Other Photochemical Oxidants
Committee on Medical and Biologic
Effects of Environmental Pollutants
National Research Council
NATIONAL ACADEMY OF SCIENCES \J,
Washington, D. C. 1976
-------
NOTICE
The project reported on here was approved by the
Governing Board of the National Research Council, whose
members are drawn from the Councils of the National
Academy of Sciences, the National Academy of Engineering,
and the Institute of Medicine. The members of the comrait'-
tee responsible for the report were chosen for their
special competences and with regard for appropriate repre-
sentation of experience and disciplines. The findings and
conclusions presented are entirely those of that committee.
This report has been critically reviewed according to
procedures approved by a Report Review Committee consisting
of members of the National Academy of Sciences, the National
Academy of Engineering, and the Institute of Medicine. Only
after completion of the review process has it been released
for publication.
The work on which this publication is based was performed
pursuant to Contract No. 68-02-1226 with the Environmental
Protection Agency.
-------
CHAPTER 8
TOXICOLOGY*
The toxicologic aspects of oxidant air pollution have most often
been examined through laboratory studies of individual constituents of
the complex mixture of air contaminants that characterizes the ambient
air environment. Photochemical air pollution (with automobile exhaust
as the primary emission source) can be chemically characterized as
oxidizing in reaction, and the chemical species that contribute to this
oxidizing property are varied. Among the strongest of the photochemically
formed oxidants that are present in "oxidant smog" and are stable enough to
be identified and measured is ozone. Because ozone is also known to be
among the most toxic of gases, it is logical that most toxicologic
research related to the potential health effects of photochemical air
pollution has focused on it. It has become almost a reflex to think of
ozone toxicity when "oxidant toxicity" is mentioned. Nitrogen dioxide
is another toxic gas present in "oxidant smog," but, by most conventional
indexes, it is less toxic than ozone, especially when compared in the
same proportions as their concentrations in ambient air. Indeed, ozone
and nitrogen dioxide share many common toxicologic properties. Nitrogen
dioxide will be discussed in another monograph in this series, so its
toxicology will not be reviewed here, except for specific comparisons.
Other chemical species—e.g., the peroxyacylnitrates and hydroxyl free
*Most experimental toxicology studies of inhaled vapors and gases report
concentrations as parts per million. That convention is used in this
chapter. See Chapter 6 for relations of various measurement units.
-------
radicals, which undoubtedly contribute to the oxidizing properties of the
total mixture of oxidant air pollution—may also contribute to the total
biologic activity of this mixture. However, there have been too few
controlled toxicologic studies to permit an evaluation of their contrib-
ution to the toxicologic actions of photochemical oxidant mixtures. For
example, the single toxicologic study on PAN that has been reported
indicated that it. is much less acutely toxic than ozone (Campbell et al.,
27
1967).
The review of the experimental toxicology of photochemical oxidants
in this chapter is therefore primarily a review of the toxicology of
ozone. The reader should bear in mind that what is said about ozone may
not apply in every case to the broader term "photochemical oxidants",
but, given the current state of knowledge, ozone toxicology is the best
approximation of the toxicology of the class. With this in mind, it is
of value to review briefly the experimental toxicology of complex
mixtures of ambient or laboratory simulated photochemical smog.
Investigations of the potential biologic actions of a complex photo-
chemical reaction mixture, produced by irradiating mixtures of air and
auto exhaust under laboratory conditions that simulated real driving
patterns and solar irradiation, were first conducted in the laboratories
of the Division of Air Pollution, U.S. Department of Health, Education,
105,106,109,147,150
and Welfare (DHEW). The effects of both nonirradiated
and irradiated exhaust mixtures were studied. Clearly, irradiation of the
air-exhaust mixture led to the formation of photochemical reaction products
that were biologically more active. The changes in chemical qualities of
the mixture
8-2
-------
that accompanied the increased biologic activity were an increase in the
concentration of total oxidant and an increase in the formation of irritant
aldehydes. The relative proportions of the suspect biologically active
chemical species varied with the total concentration of exhaust gases in
147,150
the irradiated mixture and with the duration of irradiation.
Single-inhalation exposure studies lasting a few hours demonstrated in
laboratory animals that irradiation of exhaust mixtures led to greater
effects on respiratory mechanics in guinea pigs, greater reduction in
voluntary running activity of mice, and slightly greater carboxyhemoglobin
formation in rats, compared with animals exposed to the same total con-
centration of exhaust gases that were not irradiated. The concentration
of total oxidant in these experiments ranged between 0.33 and 0.80 ppm
in the irradiated-exhaust mixtures; only a trace or no oxidant was detected
in the unirradiated exhaust. The irritant aldehydes, formaldehyde and
acrolein, were also present in higher concentrations in the irradiated
atmospheres. The effects that were noted during the period of exposure
(usually 4-6 h) were reversible within a few hours when the animals were
returned to clean air. The effects in animals exposed to the irradiated-
exhaust mixture are not necessarily uniquely characteristic of ozone,
but most of them could have been produced by ozone.
The nature of changes in respiratory mechanics in guinea pigs exposed
to irradiated exhaust varied somewhat according to the ratio of oxidant
to aldehyde concentrations (formaldehyde and acrolein were measured), and
this ratio in turn varied with the duration of irradiation of the air-
147
exhaust mixture. Thus, when the oxidant:aldehyde ratio was low, the
8-3
-------
pattern of effects on guinea pig respiration resembled that produced by
6,149,152
such upper airway irritants as formaldehyde and acrolein and was
characterized by increased pulmonary flow resistance, increased tidal
volume, and decreased frequency of breathing. Increasing the ratio
resulted in a shift in the pattern of respiration toward that produced by
153
deep-lung irritants (e.g., ozone and nitrogen dioxide) —namely, de-
creased tidal volume and increased frequency—although the increased flow
resistance typical of the aldehyde effect persisted. This interactive
effect of an oxidant-aldehyde mixture could be reproduced by a simple
147
mixture of ozone and acrolein. Concentration-response relationships
of these effects and other actions in laboratory animals exposed to mixed
or single components of oxidant air pollution are summarized in Table 8-1.
From the data in Table 8-1, the conclusion could be drawn that all
the functional effects observed in short-duration experiments with lab-
oratory-produced photochemical smog mixtures could have been due to ozone
alone if one considers total oxidant concentration of the mixture equiv-
alent to ozone concentration. A possible exception is the increase in
respiratory flow resistance in guinea pigs, which is more characteristic
of and probably due, at least in part, to the irritant aldehydes in the
exhaust mixtures. The increase in respiratory frequency in guinea pigs
is most probably due to the oxidant (or ozone) content of the mixture.
Comparison of the concentrations for equal effectiveness in decreasing
the spontaneous running activity in mice also suggests that this action
of the mixture may be largely due to ozone; and the oxidant content of
irradiated auto exhaust appears to explain adequately the increase in
8-4
-------
$
CM
in
> ro
in
r- p«
^* ^-H
rH ,_(
(N
in
ro ro
in in
ro
in
O O O O O
in m m Lfi ^">
rH rH rH rH rH
^ ^ ^ ^ ^
r» r^ r-- r^ r^
oo
en
4-1
CO §
S^
$3
i s
SB
O iH
•rH (tj
-P P "3
B 'Q ra
rH -H 0)
rH > H
PLI '^ tn
g
s
8
•d
fi
s
Q
d
8
a
CTi
en
-------
8
-H
$
I
-P
3
OD >*
ro in
00 CO
ro n
•H
tr
oo
O IO
o m
• 10
O (N
2
Oz
Ni
0)
£s
I
ss
Jll
. a
ui w
4J
%
U-)
19
8-6
-------
susceptibility to respiratory infection in mice exposed to the mixture.
These conclusions must, of course, be qualified by the possibility that
other chemical species, such as hydroxyl free radicals, that were not
measured or reported might also have produced the same effects and led
to the same conclusions. Nevertheless, it is reasonable to conclude that
many of the functional effects produced by short-duration exposures to
complex photochemical oxidant mixtures are due to ozone.
109
Hueter et al. exposed animals to irradiated automobile exhaust
(simulated photochemical smog) for periods up to 23 months. The concen-
trations were cycled, to simulate daily peak and trough pollution concen-
trations in urban centers. Peak daily concentrations of carbon monoxide
were 20, 50, 60, and 100 ppm in four sets of exposure chambers. There
was considerable loss of ozone and nitrogen dioxide on chamber walls,
cages, and animal fur, so the concentrations of chemically reactive gases
to which the animals were exposed probably ranged from about 0.04 to 0.2
ppm for ozone and about 0.15 to 0.5 ppm for nitrogen dioxide. Pulmonary
flow resistances, tidal volumes, and respiratory frequencies of guinea
pigs were measured (while the animals were breathing clean air for brief
test periods) at 16-week intervals during the experiments and were not
affected by the chronic exhaust exposures. Exhaust-exposed mice showed
a decrease in running activity for the first few weeks of exposure, but
then recovered to control activity. A decrease in mouse fertility rate
and a decrease in infant survival rate occurred in the exhaust chambers,
and there was an increase in the rate of spontaneous pulmonary infection
in exhaust-exposed animals. There were no significant effects of exhaust
8-7
-------
exposures on mortality, histopathology, growth rate, or hematologic
indexes. Interpretation of these studies is difficult, because of surface
loss of contaminants in the chambers. The decrease in mouse fertility
125
(duplicated in a second experiment ), the decrease in mouse physical
activity, and the increase in susceptibility to infections suggest that
some functional measurements were more sensitive for detecting effects
than conventional histologic, hematologic, or growth measurements. It is
doubtful, however, whether any of the observed changes could be considered
chronic effects, i.e., irreversible or progressive in the absence of
continued exposure.
216
Wayne and Chambers reviewed the findings of studies on experimental
animals exposed throughout their lifetimes to ambient Los Angeles atmosphere.
The control animals were kept in rooms that were ventilated with special
filters that removed most of the ambient air pollutants. No clear evi-
dence of chronic injury from the ambient air pollution was observed.
There was sane suggestion from pulmonary function tests, electron-microscopic
examinations, and pulmonary adenoma incidence that aged animals were
adversely affected by ambient smog; and some reversible changes in pul-
monary function of guinea pigs were noted during peak periods of air
pollution. Increased 17-ketosteroid excretions suggested that breathing
polluted ambient air was stressful for guinea pigs. Not only were the
reported effects marginal, but some of them may have been due to variations
in temperature and humidity. Although the information obtained is of
little value in the quantitative assessment of the health hazards of air
pollution, some subjects for possible future consideration were revealed:
8-8
-------
the effects of air pollutants on aged animals in which physiologic repair
processes are less active and the effects of other stressful stimuli on
the response to air pollutants.
55
Qnik and Plata reported on studies of the effect of breathing
ambient oxidant-polluted air in Riverside, California, on spontaneous
running activity of mice, as recorded over a 1-year period. The controls
were mice that were exposed to highly filtered air. Monthly peak oxidant
concentrations in the unfiltered ambient air were 0.05-0.24 ppm; peak
nitrogen dioxide concentrations, 0.04-0.07 ppm; and peak total hydrocarbon
concentrations, 2.7-4.4 ppm. The daily activity of mice breathing filtered
air was consistently higher than that of those breathing ambient air, and
the differences between the two groups were greatest during the months
when peak oxidant concentrations were highest. Other environmental vari-
ables, especially temperature, may also have contributed to the magnitude
of differences between the groups.
160
Nakajima et al. studied histopathologic changes in the lungs of
mice that were exposed to irradiated auto exhaust and oxidant-fortified
exhaust-gas mixtures for 2-3 h/day on 5 days/week for a month. Histopa-
thologic changes resembling tracheitis and bronchial pneumonia were observed
in mice exposed to atmospheres containing oxidant at 0.1-0.5 ppm, but not
in those exposed to atmospheres containing 0.1-0.15 ppm. The changes were
minimal in the latter group; the main finding reported was irregular
arrangement of the epithelial cells of the relatively thick bronchioles.
As will be shown in greater detail, ozone alone can produce many of
the effects of complex mixtures of photochemical oxidant air pollution
8-9
-------
that have been reported from studies on experimental animals. Studies of
the response of animals to these complex mixtures have the advantage that
they should detect the gamut of potential toxicity of photochemical oxi-
dant smog. However, the study of complex mixtures has limited value for
mechanism studies, the most useful type of research for laboratory animal
experimentation. The mere demonstration of similarity in quality of
response to complex mixtures and selected individual constituents does
not ensure that the constituents studied are the only or even the primary
biologically active ones. At the same time, lack of similarity, both
qualitative and quantitative, between effects of a mixture and effects
of individual constituents may reflect interactive effects, both synergistic
and antagonistic. The prime disadvantage of attempting to study the complex
mixture of photochemical smog—either ambient smog or a realistic laboratory
simulation—is the difficulty of obtaining reproducible, controlled
atmospheres.
EFFECTS IN THE LUNGS
Disposition and Uptake
There is little information on the exact disposition and sites of
uptake of ozone. However, because it is relatively insoluble in water,
it can reach the periphery of the lung and hence has the opportunity to
exert damage to both the central airways and terminal lung units. Ozone
is highly reactive, and, given the concentrations found in ambient air, it
is highly unlikely to be exhaled as ozone under conditions of normal breathing.
70,222
Frank and colleagues have attempted to define the amount and
site of uptake of ozone in the lung, by two methods: direct measurement
8-10
-------
of the drop in concentration of the gas across the upper airway (nose and
pharynx) or the remainder of the airways, and predictions based on a
computer model. In their animal experiments, they used anesthetized,
paralyzed, mechanically ventilated beagles. The upper airways were
surgically isolated, and ozone at two concentrations (0.7-0.85 and 0.2-
0.4 ppm) was administered by nose or mouth. Flow rates were either high
(35-45 liters/min) or low (3.5-6.5 liters/min). Each exposure lasted
20-30 min; but, because of the slow response of the mast ozone meter,
measurements of respiratory uptake were useful only during the last 4-5
min of exposure. The following observations were made: nasal uptake
exceeded oral uptake at both high and low flow rates (p<0.01); uptake of
ozone, both nasally and orally, was inversely related to flow rate (p_<0.01),
except when the gas was directed through the mouth at the high flow rate;
and a decrease or increase in nasal resistance induced by drugs did not
significantly change the uptake. The same investigators have developed
a computer model for predicting uptake of ozone, with some assumptions
related to solubility coefficient, an idealized version of the morphometry
217
of the lungs and a fixed set of ventilatory parameters. Computer
analysis has shown that the dosage of ozone is greater to the peripheral
70
airways than to the alveolar structures.
Effects of Short-Term Exposure to Ozone
Morphologic Effects. Gross autopsy findings of puJinonary edema and
hemorrage after acute exposure to ozone have been known for some time.
Several studies have shown that edema and an acute inflammatory response
occur in several species after brief exposures to ozone. The minimal
8-11
-------
concentration of ozone that causes the responses that have been demon-
strated depends very much on the methods used for the detection of edema.
191
Scheel et al. provided histopathologic evidence of injury caused
by a single acute exposure to ozone at 1.0 or 3.2 ppm for 4 h in mice and
by repeated intermittent exposures (8-45 ppm for 1 h) in rabbits. No
gross pulmonary edema was observed in mice killed immediately after
exposure to 1 ppm, but moderately engorged blood vessels and capillaries
containing an excess of leukocytes were found. Mice killed 20 h after
exposure showed mild edema and migration of the leukocytes into the
alveolar spaces. Inhalation of 3.2 ppm produced grossly visible edema
during or shortly after exposure. The perivascular lymphatic vessels
were distended and filled with edematous precipitate. Hyperemia (excess
blood), mobilization of leukocytes, and various degrees of extravasation
of red cells accompanied the edema. Damage to the respiratory tract
consisted of loss of epithelium from the bronchioles; sheets of desquamated
epithelial cells were seen in the lumen. The technique for measuring the
gross edema produced (wet and dry lung weights) that was used in earlier
studies was not sufficiently sensitive to detect a mild edematous reaction.
More refined methods, based on the recovery of radiolabeled blood albumin
in pulmonary lavage fluid, indicate that the ozone-exposure threshold
5
for edema formation in rats is 0.25-0.5 ppm for 6 h.
The use of sophisticated techniques of light and electron microscopy
have enabled several investigators to describe in detail the nature of
16
the inflammatory response. Boatman et al. observed a desquamation of
the ciliated epithelium throughout the airways of cats exposed to ozone
8-12
-------
at 0.25, 0.5, and 1.0 ppm for 4-6 h. The intensity of the response
appeared to be dose-related. Ultrastructural changes in the airways
consisted of cytoplasmic vacuolization of ciliated cells and condensed
mitochondria with abnormal cristae configuration. The latter occurred
most often in the medium-sized airways, 0.8-1.2 mm in diameter. Alveolar
ultrastructural changes included swelling and denudation of the cytoplasm
of Type I cells, swelling or breakage of capillary endothelium, and lysis
of red blood cells. Type II pneumocytes appeared normal. There was a
considerable variation in the degree of response, both within a single
lung and from animal to animal.
197
Stephens et al. have shown that, in rats, the degenerative changes
in Type I alveolar cells occur after exposure to ozone at concentrations
as low as 0.2 ppm for 3 h and that the cells are replaced by Type II
alveolar cells beginning a day after the exposure. By electron microscopy,
11
Bils noted that the swelling of the epithelial alveolar lining cells of
mice occurred after exposure to ozone at 0.6-1.3 ppm for 4 h. These changes
were not accompanied by fluid accumulation in the alveolar space. There
was also a focal swelling of the endothelial cells and an occasional
break in the basement membrane.
Electron microscopy has also shown that, in rats exposed to ozone at
3 ppm for 4 h and in mice exposed to 4 ppm for 3 h, acute inflaninatory
174,220
bronchiolar lesions occur. These concentrations were high enough
to produce alveolar edema, and the observed changes were similar to those
found in earlier studies that used standard histologic techniques.
8-13
-------
Effects on Pulmonary Function. Changes in pulmonary function have
been observed in a variety of species after short-term exposure to ozone,
including alterations in the elastic behavior of the lungs, increased
resistance to flow, and decreased carbon monoxide diffusion capacity.
191
Scheel et al. exposed 75 rats to ozone at 2 ppm for 3 h and
measured pulmonary function immediately after removal of the animals
from the exposure chamber. Decreases in minute ventilation, tidal
volume, and oxygen uptake occurred immediately after exposure and reached
minimal recorded values after 8 h. At 20 h after exposure, all measure-
ments had returned to normal. Pulmonary edema may have been responsible
for the observations reported.
153
Murphy et al. exposed guinea pigs to ozone at 0.34-1.35 ppm for
2 h. Respiratory rates increased and tidal volumes decreased during
exposure to all concentrations. The maximal changes were significantly
different (p_ <0.05) frcm preexposure control values for every concentration
used. Once a maximal response was reached, the effects tended to remain
constant for the remainder of the test period. Respiratory rates and
tidal volumes tended to return to preexposure: control values when the
animals were returned to clean air. Total respiratory flow resistances
were not significantly altered during inhalation of ozone at 0.34 and
0.68 ppm, but increased by 47% during exposure to 1.08 ppm.
52
Easton and Morphy observed up to a threefold increase in flow
resistance within an hour in guinea pigs during exposure to ozone at 5-7
ppm0 There was a 50% increase in frequency of breathing and a small
increase in tidal volume. Lung compliance decreased by 50%. After
8-14
-------
exposure, all measurements returned to preexposure values within 3 h.
These responses did not result in an increase in the work of breathing,
in contrast with the response of guinea pigs to other irritants (formal-
dehyde and sulfur dioxide), in which the observed changes in pulmonary
7
function resulted in an increase in the work of breathing.
215
Recently, Watanabe et al. observed changes in respiratory
mechanics and single-breath diffusing capacity in cats exposed to ozone
at 0.26-1.0 ppm for an average of 4-6 h. The animals were anesthetized,
paralyzed, and mechanically ventilated through a tracheal cannula.
Increased pulmonary flow resistance was the most sensitive index of ozone
exposure in this species and occurred in almost all the animals exposed
to 1.0 and 0.5 ppm and in two cats exposed to 0.25 ppm. Although the
magnitude of the change was dose-related, it appeared that the concen-
tration of ozone was more critical than the duration of the exposure.
The mechanism of the response to ozone at 1.0 ppm appeared to differ
from that to the lower concentrations in that there was a pulsatile
increase in resistance that was superimposed on a more progressive change.
The underlying increase in resistance was approximately exponential with
respect to time. Changes in dynamic compliance and capacity for diffusing
carbon monoxide were less frequent and less marked than the change in
resistance. Vital capacity did not change. The shape of the volume-
pressure curve during deflation did not change, and that suggests that
alveolar stability was not affected. In cats, therefore, exposure to
ozone affects airway caliber at concentrations lower than those which
affect transfer of carbon monoxide across the alveolar-capillary membrane
8-15
-------
or alveolar surface forces in the absence of pulmonary edema. Unlike
the increase in pulmonary flow resistance that results from exposure to
sulfur dioxide, the response to ozone is not mediated entirely via reflex
bronchoconstriction, inasmuch as it was only partially reversed by atropine
in these experiments. About half the response persisted after the admin-
istration of the drug. Thus, the small airways are implicated in the
persistent increases in pulmonary flow resistance in response to ozone.
This implication is further supported by the following observations:
vagal innervation ends short of the peripheral airways, ozone can pene-
trate to the periphery of the lung, and postmortem studies show that
inflammatory changes occur in the peripheral airways.
Unilateral exposure of the lung may be achieved in rabbits, because
they have an intact mediastinum, which permits the unexposed lung to
serve as a control for the exposed lung. The control lung may be collapsed,
and ozone inhaled in a normal fashion by the noncollapsed lung; or, by
selective catheterization, one lung can be made to breathe ozone through
an airtight system while the other breathes ambient air. Rabbits so
exposed to ozone at 12 ppm had increases in respiratory rate and minute
4
volume and bilateral decreases in tidal volume and dynamic compliance.
Pulmonary function measurements were not significantly different in the
ozone-exposed lung until edema developed, as determined by an increase in
the wet weight of that lung. After edema formation, tidal and minute
volumes, inspiratory and expiratory flow rates, and dynamic compliance
decreased and pulmonary flow resistance increased in the lung exposed
to ozone, relative to the unexposed lung.
8-16
-------
Studies have been performed on the effects of ozone exposure on
69
excised dog lungs. This preparation offers the advantages of providing
information on changes in pulmonary function in the absence of intra-
alveolar edema and vagal innervation. High concentrations of ozone were
used (6.8-10.3 ppm for 2.5 h and 5-10 ppm for 3 h). The changes in static-
deflation volume-pressure relationships were barely detectable, whether
measured in air or saline. The data suggest that exposure to ozone does
not produce significant depletion or degradation of either surface-active
material or tissue elastic elements in the absence of edema. Thus, it
seems that the changes in elastic behavior, as determined by changes in
dynamic lung compliance, are secondary to the formation of edema, unevenly
distributed changes in flow resistance or compliance, and a change in
tidal volume or end-expiratory lung volume.
There is evidence that ozone has a delayed effect on elastic behavior.
Excised lungs of rabbits that were unilaterally exposed to ozone at 1.0
ppm for 3 h and then allowed to breathe ambient air for up to 2 weeks
showed a depression in the volume-pressure curves. This change was present
during most of the postexposure test period. The mechanism underlying
70
this response was not determined.
71,72
Frank et al. exposed the right lung of rabbits to ozone at 2.2-
12.1 ppm for 3 h, the left lung having been collapsed before exposure.
When edema occurred in the right lung, changes in surfactant behavior
(as determined by in vitro measurements of the surface tension of washings
from the left lung) were observed in some animals. No such changes were
observed in the absence of edema in the right lung. These results suggest
8-17
-------
not only that ozone can induce chemical changes in exposed lungs, but
that the products of such changes can cause deleterious effects in non-
exposed lungs.
Effects of Prolonged Exposures to Ozone
199
According to Stokinger, at least three effects of long-term
exposure to ozone have been recognized: effects on morphology and
function of the lung, lung-tumor acceleration, and aging. An additional
effect, the development of tolerance after exposure to low concentrations
of ozone, may also be related to chronic toxicity.
204
Stokinger e_t al. reported that chronic bronchitis, bronchiolitis,
and emphysematous and fibrotic changes in the lung tissues occur in mice,
hamsters, and guinea pigs exposed daily to ozone at a concentration
slightly above 1 ppm. These irreversible changes also develop in animals
that have developed tolerance to acute inflammatory effects.
75
Freeman et al. used tissue fixation and electron microscopy and
reported on the morphologic changes that occurred in the lungs of dogs
exposed to ozone at 1-3 ppm for 5-24 h/day for up to 18 months. In general,
the effects reported tended to increase in severity with the concen-
tration used, rather than with the duration of the exposure. There was
no evidence of pulmonary edema. The most noticeable change was a
thickening of the bronchioles and respiratory bronchioles. This change
was barely noticeable at the lowest concentrations used, but at the
highest concentrations it was accompanied by infiltration of lymphocytes,
plasma cells, and fibroblasts that formed peribronchiolar collars, thus
reducing the caliber of the small airways. Bronchiolar changes included
an increase in the proportion of mucus-forming cells and squamous metaplasia
8-18
-------
of columnar and cuboidal cells. In addition, there was an increase in the
average number of macrophages per field along the peripheral airways.
In developing rats exposed to ozone at 0.54 or 0.88 ppm for up to
3 weeks, morphologic changes were seen in the respiratory bronchioles
and distal portions of the terminal bronchiolar epithelium, the entire
alveolar duct, and the associated alveoli. These changes started to
occur after 24 h of exposure; but, after several days of exposure, the
hypertrophic bronchiolar epithelium tended to recede and was replaced by
cuboidal or squamous cells. The lungs of growing rats exposed to ozone
at 0.9 ppm were approximately 38% heavier than those of normal animals
74
of the same age; within 3 weeks, 50% had died with grossly inflated lungs.
Mice exposed to ozone at 2.5 ppm for 120 days showed progressive
metaplasia along the tracheal bronchial tree. Return of these animals
to clear air resulted in a reversal of these changes after a further 120
170
days.
10
Bartlett et al. exposed 194 young rats (3-4 weeks old) continuously
to ozone at 0.2 ppm for 28-32 days and observed that there was no effect
on respiratory frequency, weight gain, tail-length increase, and external
appearance in the ozone-exposed group and that, although both ozone-
exposed and control groups looked healthy, 12 ozone-exposed and 11 control
animals had pneumonitis at the end of the exposure period. The results
with the latter animals were discarded in the later data analysis. The
lung volumes of the ozone-exposed group were 16% greater than those of
the control group. Air or saline static volume-pressure deflation curves
at 95% or 100% of total lung capacity showed that transpulmonary pressure
8-19
-------
was significantly lower in the ozone-exposed group, thus confirming that
exposed lungs were over distended at high transpulmonary pressures. The
fact that this occurred in both air- and saline-filled lungs suggested
a small change in tissue elasticity, rather than abnormal surface tension.
There were no apparent morphologic differences between the two groups
detected by conventional staining techniques, but more sensitive electron-
microscopic techniques might have revealed some differences.
Acceleration of lung tumorigenesis (adenoma) in a lung-tumor-
susceptible strain of mice occurred after daily exposures to ozone at
about 1 ppm. At 15 months, an incidence of 85% was seen in the ozone-
exposed animals, compared with 38% in the controls; the average number
199
of tumors per mouse was 1.9, compared with 1.5 in the controls.
There is some suggestive evidence that exposure to ozone accelerates
12 13
the aging process (es). Bjorksten and Bjorksten and Andrews have
presented evidence that aging is due to irreversible cross-linking
between macromolecules, principally proteins and nucleic acids. Aldehydes
were included in the list of cross-linking agents, and these can be
26
produced in the lung as a result of ozone exposure.
Tolerance
One feature of the response to oxidants (in particular, ozone) that
has stimulated considerable interest is the apparent development of
tolerance to the acute effects of short-term exposure to these agents
59
in laboratory animals. Fairchild reviewed possible mechanisms of this
phenomenon. Tolerance has been defined as the increased capacity of an
organism that has been preexposed to oxidant to resist the effects of
8-20
-------
later exposures to ordinarily lethal (or otherwise injurious) doses of
the same agent or of different agents (cross-tolerance) with similar
toxicologic properties.
Development of tolerance to the acute toxicity of ozone in experi-
mental animals has been demonstrated after a single, brief (1 h or less)
exposure to low concentrations (0.3-3 ppm). Rats can develop a tolerance
that lasts for a month or longer. In mice, a tolerance lasting up to
14 weeks has been observed. Ozone is not the only lung edematogenic
agent that can produce tolerance. This phenomenon is also observed with
nitrogen dioxide, phosgene, and phenylthiourea. The tolerance evoked by
one agent can provide cross-protection against other irritants. For
example, a single exposure of rats or mice to ozone (0.5-5 ppm for 1-5 h)
will induce protection against the acute pulmonary effects of nitrogen
dioxide, hydrogen peroxide, ketene, phosgene, hydrogen sulfide, and
59
nitrosyl chloride. The development of pulmonary edema is the toxic
effect of all these compounds. Although pretreatment by injection of
phenylthiourate will provide tolerance to inhalation of an ordinarily lethal
dose of ozone, the reverse is not true. Inhalation of ozone will not
provide cross-tolerance to the lung edema produced by injection of
thiourate.
104
Studies by Henschler et al. on the development of tolerance to
nitrogen dioxide in mice provided some insight into the significance of
this phenomenon. They found that mice that had been exposed only once
to nitrogen dioxide were almost totally protected from effects of later
exposures to high, usually fatal concentrations, whereas those which were
8-21
-------
repeatedly exposed were only partially protected. It was concluded that
the first exposure protected from the effects of the following exposures,
thus inhibiting increased tolerance buildup. It is significant that, in
another experiment, mice tolerant to nitrogen dioxide were exposed to a
concentration high enough to cause lethality, but none of the mice died
with pulmonary edema. The predominant gross finding was massive
hemorrhage.
In animals made tolerant to ozone and later exposed to ordinarily
injurious concentrations, the usual increase in lung water and other
pathologic changes associated with edema were either reduced or absent,
and the usual ozone-induced changes in activity of serum alkaline
phosphatase and adrenal succinic dehydrogenase were absent or slight.
In addition, there was significantly less oxidation of lung reduced
59
glutathione in the tolerant animals. It should be pointed out that
there may be species differences in tolerance development. Quilligan
182
et al. used several different conditions of exposure and challenge
and were unable to demonstrate tolerance to ozone in baby chicks; and
it is not known whether humans develop tolerance to ozone.
Tolerance appears to be a local phenomenon, in that experiments
with unilateral exposure showed that a lung is not protected from pulmonary
edema unless it has been exposed itself. Thus, no tolerance was produced
in the contralateral, unexposed lung; this suggested that there is no
77
evidence of a circulating humoral agent that confers tolerance. The
same investigators also attempted to show whether induction of tolerance
affected the cytotoxic effects of ozone on alveolar macrophages (discussed
8-22
-------
in the next section). They used unilateral exposure and lavage and
observed no differences in the cytotoxicity of ozone between tolerant
and nontolerant lungs. A twofold increase in the number of polymor-
phonuclear neutrophilic leukocytes occurred in the tolerant lung. Alveolar-
macrophage enzyme activities were equally depressed in both tolerant and
nontolerant lungs. This study suggested, therefore, that tolerance does not
protect the antibacterial defense mechanisms of the lung from the effects of
153
ozone. In addition, Murphy et al. found that exposure to ozone, which
produced tolerance in guinea pigs to the edema produced by later exposure
to high concentrations, failed to produce tolerance to the effects of low
concentrations of ozone on respiratory frequency and tidal volume.
It appears that the development of tolerance is a useful tool to
determine the mechanism of ozone-induced pulmonary edema. However, in
the light of the findings that repeated intermittent exposures of mice
to nitrogen dioxide produced less protection from the effects of a lethal
dose than a single preexposure and the failure to produce tolerance to
the effects of ozone on antibacterial defense mechanisms or on the
respiratory patterns of guinea pigs, it is unlikely that tolerance
development provides significant protection in human populations con-
tinuously exposed to low concentrations of oxidants.
Defense Mechanisms
It has been observed that animals challenged with aerosols of
infectious organisms suffer a higher incidence of infection if they have
been previously exposed to ozone, irradiated auto exhaust, or other
common pollutants. The suggested explanation for this is that the various
8-23
-------
polutants inhibit, inactivate, or otherwise impair two distinct functions:
raucociliary streaming, the action of cilia in the nasal and upper respi-
ratory passages that clears particles and thus prevents them from entering
the lungs; and phagocytosis by alveolar macrophages.
139
Miller and Ehrlich determined the effect of exposure to ozone on
the susceptibility of mice and hamsters to respiratory infection caused
by inhalation of Klebsiella pneumoniae aerosol. The ozone exposures
used were 1.3-4.4 ppm for 3 h and 0.84 ppm for 4 h per day, 5 days/week
for 2 weeks. The observation period for this experiment was 2 weeks.
Mortality and survival time were measured. The mortality due to K._
pneumoniae infection was significantly greater (p< 0.05) for every
exposure regimen in which animals were exposed to ozone than in their
paired controls. No deaths were caused by ozone exposure alone. Autopsy
of the animals exposed to K._ pneumoniae that died within the 14-day
holding period showed the infectious organism in the lungs and heart.
K._ pneumoniae was absent in animals that survived the 14-day holding
period. It was concluded that exposure to ozone significantly reduced
the resistance of mice and hamsters to later respiratory infection due
to K^ pneumoniae. Statistical evaluation of the data indicated higher
mortality, shorter survival time, and a lower LD (for K. pneumoniae)
50 — _———
in animals exposed to ozone than in controls.
181
In a similar series of experiments conducted by Purvis et al.,
mice were exposed to ozone at 3.8-4.1 ppm for 3 h, 1-27 h before and
3-27 h after challenge with K._ pneumoniae aerosol. Within 19 h after
exposure to ozone, the resistance of mice to respiratory infection
8-24
-------
ijnitiated by challenge with the. aerosol was significantly reduced. The
same effect was observed in infected animals exposed to ozone up to 27 h
after challenge with the aerosol.
36
Coffin and Blorrmer have shown that mice exhibit increased mortality
from Streptococcus aerosol after exposure to ozone at 0.08 ppm for 3 h.
This concentration of ozone also produced a decrease in the rate of kill
of bacteria deposited in the lungs and hence an increase in their later
35
multiplication. This effect was noted 4 days after exposure, but not
4 h after exposure.
95
Goldstein et al. studied the effect of ozone on the in vivo rate
of bacterial killing in the mouse lung. They used male Swiss mice infected
with aerosols of Staphylococcus aureus labeled with phosphorus-32. The
animals were sacrificed immediately or after exposure to ozone at 0.62-
4.25 ppm for 4 h, and the radioisotope concentration in the lungs was
determined. Increased numbers of bacteria were consistently cultured
from the lungs of animals exposed to ozone, compared with controls, and
the magnitude of the effect was dose-related up to 2.58 ppm. Some mice
exposed to 2.2 ppm or greater yielded more staphylococci than were inhaled
initially; thus, intrapulmonary bacterial multiplication had occurred.
The difference between control and infected animals was significant
(p< 0.05) at 1.10 ppm, when individual aerosol experiments were compared.
When the data from all the experiments were pooled, there were significant
differences in bacterial activity between control and treated mice for
each ozone exposure (p< 0.05). Inasmuch as the ozone-exposed mice vrere
able to remove the same number of bacteria as control mice via mucociliary
8-25
-------
streaming, the investigators concluded that the inhibition of bactericidal
activity resulted from the toxic effect of ozone on the alveolar macrophages.
3
Alpert and Lewis used unilateral exposure to study the effect of
ozone on the defense mechanisms of the lungs. Rabbits were exposed unilat-
erally to ozone at 0.5, 0.75, and 3 ppm for 3 h. The alveolar macrophages
were harvested by pulmonary lavage. Although there was a statistically
significant reduction in the viability of the cells from the ozone-exposed
lung, compared with the air-exposed lung, the differences were small.
There was also a dose-related inhibition of the intracellular hydrolytic
enzymes acid phosphatase, lysosyme, and 6-glucuronidase. The fraction
of total cells present as polymorphonuclear neutrophilic leukocytes in
the lavage fluid from the exposed lung increased in a dose-related fashion
from approximately 2% at 0 ppm to approximately 28% at 3 ppm. Associated
with the increase in the fraction of polymorphonuclear neutrophilic
leukocytes was a reciprocal decrease in the fraction of alveolar macro-
phages, although the total number of macrophages per gram (dry wt) remained
unchanged. The authors suggested that the depression of the intracellular
hydrolytic enzymatic activity by ozone may contribute to the ozone-caused
impairment of lung defense mechanisms.
Interactions with Bronchoactive Agents
The lung is relatively rich in Mstsinine-containing mast cells, so
it is not surprising that a number of investigators have assessed the
role of histamine in the pulmonary toxicity observed after ozone exposure.
Among the many effects of histamine are edematogenic alterations
in vascular endothelium and bronchoconstriction. The latter may be
8-26
-------
particularly pertinent, in view of its being a central manifestation of
asthma attacks and of the reported association of asthma attacks with
photochemical air pollution. Bronchoconstriction has also been observed
in animals and man experimentally exposed to ozone or photochemical air
pollution.
49
Dixon and Mountain reported that exposure of mice to ozone at
1 ppm for 5 h resulted in a depletion of lung histamine content to as
low as 75% of the control value 5 days later. They also observed that
pretreatment with promethazine, an antihistaminic agent, resulted in a
decrease in the amount of pulmonary edema produced by a sublethal dose of
ozone. However, promethazine, in addition to being a potent antihistaminic
agent, is a phenothiozine derivative and thus might act as a free-radical-
trapping or membrane-stabilizing agent.
Other investigators have been unable to demonstrate lung histamine
41
depletion in rats exposed to ozone at 4 ppm for 4 h or guinea pigs
52
exposed to ozone at 1-5 ppm for 3 h. In the latter study, it was
observed that exposure to ozone at 5 ppm for 2 h followed by challenge
with histamine at 0.9-1.4 mgAg (injected 1.5-2.0 h after the end of
exposure) resulted in increased mortality, compared with that in an air-
exposed control group. The increased susceptibility to histamine was
detectable for 120 h after the end of exposure to ozone at as low as 0.8
ppm. This concentration is about one-twentieth of that required to
produce death from pulmonary edema due to ozone alone. It was found that
the increased susceptibility occurred only when exposure to ozone took
place before challenge with histamine. There was no increase in suscepti-
bility in guinea pigs that received histamine before exposure.
8-27
-------
Potentiation of the action of acetylcholine, another bronchoconstrictive
agent implicated as a mediator in asthma, has also been reported in guinea
pigs exposed to ozone at at least 2 ppm for 30 min before inhalation of
128
acetylcholine; the effect was observed intermittently for up to 23 h
after ozone exposure.
The reported potentiation by ozone of the membrane damage produced
88
by the indirect pathway of complement might also play a role if it
occurs in vivo, inasmuch as this complement pathway apparently mediates
127
the allergin-reagin-induced release of histamine. In view of the
fact that asthma attacks usually occur at night, whereas ozone peaks in
ambient air occur late in the morning, it might be more reasonable to
ascribe the epidemiologic association of photochemical oxidants with
asthma (if such exists—see Chapter 10) to an ozone-induced alteration
of the respiratory tract, either potentiating an otherwise subclinical
effect of an allergen or increasing the reactivity of smooth muscle to
bronchoactive compounds.
The vasoactive compound serotonin has also been suggested to be
196
responsible for ozone-induced pulmonary edema by Skillen et al., who
noted a decrease in lung serotonin after ozone exposure. Prostaglandins
may also be involved in ozone toxicity, in view of a report that aspirin,
49
a prostaglandin inhibitor, protects from ozone toxicity. Prostaglandins
173
are released from injured lungs, possibly as a result of membrane damage.
206
Recently, Tan et al. demonstrated that injection of hydroperoxides,
39
which results in lung damage similar to that caused by injected ozonides,
appeared to interfere with lung prostaglandin synthesis.
In a study of the mechanism whereby Bordetella pertussis vaccine
60,209 208
increased acute ozone toxicity in rate, Thompson ascribed the
effects to g-adrenergic blockade, and not to an immune-mediated response.
It was further noted that both atropine and reserpine reduced mortality,
8-28
-------
which suggested that the acute lethal effects of ozone were due to shock
and circulatory collapse, rather than pulmonary edema.
The release of bronchoactive compounds may result from immune
reactions. A possible role for the immune system in chronic ozone
191 203
toxicity was suggested by Scheel et al. and by Stokinger and Scheel,
who hypothesized that ozone altered lung protein, making it immunogenic
to the host. Presumably, the resulting antibody would cross-react with
normal lung tissue and produce damage. Although some indirect evidence
25
to support this hypothesis was presented, it has been questioned.
In addition, the suggestion that neonatal thymectomy altered ozone
98 209
toxicity has not been confirmed.
BIOCHEMICAL ACTIONS AND MECHANISMS
Molecular Reactions
Free-Radical Effects of Ozone: The idea that ozone toxicity is
expressed through the formation of reactive free-radical intermediates
was originally derived from studies that noted the similarity of the
effects of ozone to those of radiation. Earlier studies included the
observation of a similar and generally additive effect of ozone and
64
x irradiation in producing chromosomal aberrations in Vicia fava seeds;
radiation-like effects on the deoxygenation of hemoglobin in the occluded
20
digits of humans breathing ozone at 1 ppm for 10 min; the protective
62
effects of thiol radioprotective agents in ozone toxicity; the ability
of ozone to produce mutations and chromosomal damage; and an increase in
the radiation-induced sphering of human and animal red cells in vitro
21
after ozone inhalation. These studies and the idea of free-radical
201 213 134
effects of ozone have been reviewed by Stokinger, Veninga, Menzel,
223
Zelac et al. and others. As discussed in more detail later, Zelac
223,224
et al. have also demonstrated a nearly additive effect of ozone
8-29
-------
and x irradiation in producing lyrrphocytic chromosomal breaks in Chinese
hamsters. Furthermore, other antioxidant and radical-trapping agents—
including various quinones, ascorbic acid, and a-tocopherol—have been
87,89,129,135,164,184
reported to protect from ozone toxicity.
The exact radicals produced by ozone in vivo are not fully under-
1
stood. Alder and Hill proposed that the aqueous decomposition of ozone
produced both hydrogen and hydroxyl free radicals and that the reaction
64
was catalyzed by base. Fetner suggested that hydroxyl and peroxyl
radicals were responsible for the observed radiomimetic effects. It
should be noted that the peroxyl radical dissociates to form the superoxide
157
anion radical at physiologic pH. Recently, Mustafa et al. noted an
increase in lung superoxide dismutase after ozone exposure, which indirectly
201
suggested the presence of the superoxide anion radical. Stokinger,
noting the lability of sulfhydryl groups in the presence of ozone and
radiation, hypothesized that free radicals might be derived from the
interaction of ozone with sulfhydryls. A similar reaction pathway has
45
been proposed by DeLucia et al. That ozone-induced free radicals are
derived from the oxidative decomposition of unsaturated fatty acids has
84 134 185
been suggested by B. Goldstein and Balchum, Menzel, and Roehm et al.
86
B. Goldstein et al. used electron paramagnetic resonance to demonstrate
free-radical signals in ozonized linoleic acid. It is also conceivable
that singlet oxygen is derived directly from ozone or via the decomposition
of an ozonide. Furthermore, hydrogen peroxide, which may be formed in
aqueous solution by ozone or these intermediates, has been indirectly
82
identified in the red cells of animals that inhaled ozone.
8-30
-------
All these rapidly reacting intermediates are potentially harmful to
the cell and might play a role in ozone toxicity. Furthermore, the
potential for ozone-induced free-radical chain reactions exists. It
appears likely that more than one radical is formed, either directly
from ozone or as a result of the interaction of ozone with normal cellular
constituents.
The implications of various oxidative free-radical reactions for
biologic processes are being studied. Many of these reactions appear to
play a role in normal cellular processes and may be of pathologic signif-
icance only if not contained by normal defense mechanisms. It is of
194
interest that Shoaf et al. have suggested on the basis of energetics
that ozone might be derived from superoxide anion radical. Inasmuch as
superoxide is formed during some intracellular processes, ozone might be
a normal transient intermediate in vivo. Ozonides have also been produced
in the absence of ozone by the photooxidation of diazo compounds in the
155
presence of aldehydes. Further information concerning the inter-
relationships of ozone, free radicals, peroxides, ozonides, and singlet
oxygen in biologic systems would be useful.
Sulfhydryl Compounds and Pyridine Nucleotides; In view of the
oxidant nature of ozone, a number of investigators have evaluated its
effects on intracellular compounds that are normally active in cellular
redox reactions. Attention has focused particularly on reduced pyridine
nucleotides—reduced nicotinamide adenine dinucleotide (NADH) and reduced
nicotinamide ademine dinucleotide phosphate (NADPH)—and on sulfhydryl
compounds, specifically reduced glutathione (GSH).
8-31
-------
143 145 133 161
Mudd, Mudd et al., Menzel, and Nasr et al. have reported
that ozonization of aqueous solutions of NADH or NADPH results in their
oxidation. However, there is a difference in their findings as to whether
the resulting product is a biologically active oxidized pyridine nucleotide
133
(NAD or NADP), as suggested by Menzel, or is molecularly disrupted to
the extent that it is unable to participate in enzymatic processes.
Inasmuch as more drastic effects are likely to be observed in vitro, it
is more likely that oxidation of intracellular reduced pyridine nucleotides
proceeds mainly to NAD or NADP after ozone inhalation, but further
resolution of this question would be of value.
161
Nasr et al. failed to observe a change in the ratio of NADPH to
NADP in the tracheal epithelium of rats exposed to ozone at 33 ppm for an
hour. This apparently negative in vivo finding is not surprising, inasmuch
as NADP will be rapidly reduced back to NADPH if ozone does not disrupt
the structural integrity of pyridine nucleotides. In addition, de_ novo
synthesis of pyridine nucleotides may also occur. The intracellular ratio
of reduced to oxidized pyridine nucleotides is under fine cellular control,
in that the oxidation of NADPH or NADH results in the stimulation of
enzymatic activity, which restores the initial ratio. In the case of
NADPH, its oxidation increases the activity of the hexose monophosphate
shunt; this also occurs after the oxidation of glutathione. The relevant
enzymatic steps are depicted in Figure 8-1. The direct interrelationship
of glutathione and NADPH occurs in the reduction of oxidized glutathione
to reduced glutathione by glutathione reductase. NADPH is required in
this step and is itself oxidized to NADP. Accordingly, the oxidation of
8-32
-------
2GSH + [0] G. peroxidase GSSG +
GSSG + 2NADPH G. reductase 2GSH + 2NADP
G-6-P + NADP G-6-PD 6-P-G + NADPH
(HMP shunt)>
GSH=reduced glutathione
GSSG=oxidized glutathione
G. peroxidase=glutathione perioxidase
G. reductase=glutathione reductase
G-6-PD=glucose-6-phosphate dehydrogenase
6-PG=6-phosphogluconate
G-6-P=glucose-6-phosphate
[0]=oxidizing moiety, e.g., hydrogen peroxide, free radical, lipid peroxide
HMP shunt=hexose monophosphate shunt
NADP=nicotinamide adenine dinucleotide phosphate
NADPH= reduced nicotinamide adenine dinucleotide phosphate
Figure 8-1. Some enzyme processes active in defending against oxidant stress,
8-33
-------
either NADPH or GSH conceivably accounts for the apparent increase in
hexose monophosphate shunt enzymes after repeated ozone exposure.
44
de Koning and Jegier also measured pyridine nucleotides in a study
in which exposure of Euglena gracilis to ozone at 0.8 ppm for an hour in
the presence of light produced a 9-12% decrease in NADH formation.
Histochemical studies have demonstrated an alteration in NADPH- and NADH-
diaphorase activity in the lungs of rats exposed to 0.8-ppm ozone for 7
30
days.
A possible interaction of ozone with sulfhydryl groups in vivo was
58,62
originally suggested by Fairchild et al., who noted that protection
from lethal concentrations of ozone was conferred by the injection or
inhalation of sulfhydryl or disulfide compounds. Other investigators have
20,73,110,133
also noted protection from ozone toxicity by sulfhydryl compounds.
142
Mountain observed a decrease in lung glutathione and in the activity
of the sulfhydryl-containing enzyme succinic dehydrogenase after ozone
exposure. The possible toxicologic implications of the reaction of ozone
201
with sulfhydryl compounds were discussed in detail by Stokinger.
Exposure of aqueous solutions of GSH to ozone results in the formation
not only of GSSG, but also of higher oxidation states, including the
133
sulfoxide. This is important, in that, although the enzymes shown in
Figure 8-1 are capable of recycling GSSG back to GSH, the production of
the sulf oxide or the sulf one may lead to irreversible loss of glutathione.
By analogy, a similar oxidation of protein sulfhydryl groups to the
sulfoxide would also presumably prevent reduction by a disulfide-
exchange mechanism with glutathione and therefore lead to irreversible
8-34
-------
inactivation. However, the ozone-induced production of sulfoxides or
sulfones has not been reported in vivo.
45
DeLucia et al. reported that exposure of rats to 2-ppm ozone for
4-8 h resulted in a statistically significant decrease in both protein
and nonprotein lung sulfhydryl groups. Bu1^ rats exposed to 0.8-ppm ozone
for 10 days showed no change in lung sulfhydryl concentrations. As
pointed out by the authors, this finding suggests lung adaptation and is
consistent with their observation that chronic ozone exposure resulted
in an increase in glucose-6-phosphate dehydrogenase (G-6-PD) concentration,
despite a decrease in its activity after acute exposure. Glutathione
reductase, and NADH and succinate cytochrcme c reductase concentrations
were also decreased after acute ozone exposure; this was ascribed to an
effect on protein sulfhydryl groups. However, there is no firm evidence
that free sulfhydryl groups are involved in the active sites of any of
these enzymes in the lung. The cytochrome c reductases and glutathione
reductases both contain flavins, which are relatively readily oxidized
intermediates. Further studies on the sensitivity of flavin compounds
to ozone appear warranted. In addition, there is evidence of an effect
of ozone on cytochrome heme compounds, which might explain the decrease
45
in cytochrome c reductase observed by DeLucia et al.
46
More recently, DeLucia et al. reported that the bulk of the
glutathione oxidized in rat lung after exposure to 4-ppm ozone for 6 h
was in the form of mixed disulfides with lung protein sulfhydryl groups.
No increase in the concentration of oxidized glutathione was noted. Peak
oxidation of nonprotein sulfhydryl groups did not occur until about 24 h
8-35
-------
after exposure, and recovery was evident at 48 h. Effects of exposure
to lower concentrations (0.8 ppm for 24 h and 1.5 ppm for 8 h) were not
observed.
Further detailed studies of the effect of ozone on enzymes active
in the defense against intracellular oxidation were performed by Chow and
31-33
co-workers. Chronic ozone exposure resulted in an increase in the
activity of G-6-PD and 6-phosphogluconic dehydrogenase, two constituents
of the hexose monophosphate shunt, and an increase in glutathione
peroxidase and glutathione reductase concentrations (see Figure 8-1).
Of particular note is a study in which groups of rats were exposed to
ozone at 0.2, 0.5, or 0.8 ppm continuously for 8 days. The increases in
G-6-PD, glutathione peroxidase, and glutathione reductase were linearly
related to dose. Statistically significant differences were present
after exposure to ozone at 0.2 ppm. In an additional study, exposure of
rats to ozone at 0.75 ppm resulted initially in a decrease in the activity
32
of these enzymes and then an increase, as exposure continued. As
discussed below, the authors related their findings to the action of
glutathione peroxidase in detoxifying lipid peroxides, rather than to an
ozone-induced intracellular aqueous radical or hydrogen peroxide. However,
if the latter processes do occur, a similar increase in these enzymes
after chronic exposure might be expected.
Lipids. Unsaturated fatty acids (UFA) are readily oxidized cellular
macromolecules whose oxidative breakdown has been observed in a number of
situations analogous to ozone toxicity, including radiation, exposure to
132 210
hyperbaric oxygen, and inhalation of nitrogen dioxide. The classic
8-36
-------
mechanism by which free radicals and oxidative states interact with the
carbon-carbon double bonds of UFA is the formation of peroxides. Their
decomposition may result in further free-radical production capable of
initiating peroxidation of additional UFA. The resulting breakdown of
the UFA molecule results in various addition and decomposition products,
including peroxides and carbonyl compounds, which may themselves be
toxic to the cell. Ozonization of UFA appears in many ways similar to
lipid peroxidation in the resulting products and biologic implications.
However, the initial attack on the double bond proceeds by a different
mechanism. This has been studied in ozonized fatty-acid methyl ester
184,185
emulsions and thin films by Roehm et al., whose findings support
40
the general mechanism originally proposed by Criegee (Figure 8-2).
In this scheme, ozone directly attacks carbon-carbon double bonds; this
results, after decomposition of the double bond, in the formation of a
zwitterion and aldehyde. These recombine to produce the ozonide. As
184
pointed out by Roehm et al., in the presence of water the zwitterion
may form peroxides that can then catalyze the peroxidation of additional
molecules of UFA. The ozone-induced oxidative decomposition of UFA in
135
model membranes and emulsions has also been evaluated by Menzel et al.
207 134
and Teige et al., and the subject has been reviewed by Menzel.
It is not clear from cellular and in vivo experiments whether the
observed ozone-induced breakdown of UFA proceeds through the direct
attack of ozone on UFA, through the effects of an ozone-induced free
radical that result in lipid peroxidation, or through a combination of
these processes. Inasmuch as phenolic antioxidants are not as effective
8-37
-------
0-0-0
o / \
R-CH = CH-fT - i-> R-CH - CH-R'
o-o-o o-o
, ff \ multiple
R-CH . + R - CH - R-CH XH-R - ^> deconposition
products
(A) (B) (C)
Figure 8-2. Mechanism of ozonolysis. A, Criegee zwitterion; B, aldehyde;
C, ozonide.
8-38
-------
in protecting against the direct attack of ozone on double bonds as they
185
are in the autocatalytic lipid peroxidation process, the finding that
vitamin E protects against ozone toxicity might indirectly indicate that
136,137
ozone-induced lipid peroxidation does occur. However, Menzel et al.,
in a series of studies with preformed fatty-acid ozonides, have concluded
that such compounds may be responsible for a significant proportion of
ozone toxicity. Because "lipid peroxidation" is the term commonly used
in the literature and the biologic implications of lipid ozonization and
lipid peroxidation appear to be relatively similar, we will use the latter
term in discussing the effects of ozone on UFA.
Evidence of a role of lipid peroxidation in the cellular toxicity of
ozone has been obtained in in vitro studies in which human red cells were
exposed to this oxidant gas. The possibility that lipid peroxidation
is responsible for altered permeability of bacterial cell walls after
193
ozone exposure was proposed by Scott and Lesher and has since been
207
confirmed by others. Of note is the study of Teige et al. in which
red cells were lysed more readily by incubation with ozonized liposomes
137
than they were by ozone itself. Similarly, Menzel et al, noted that
incubation of red cells in ozonized serum produced more toxicity than did
direct ozonization of the red cells in the absence of serum. Menzel
137
et al. also demonstrated that incubation of human or mouse cells with
fatty-acid ozonides produced Heinz bcdies, methemoglobin formation,
oxidation of thiol groups, and formation of mixed disulfides with hemoglobin.
Oral administration of vitamin E protected against Heinz-body formation
in vitro. Heinz bodies were also observed in the red cells of mice
8-39
-------
exposed to ozone at 0.85 ppm for 48 h. Lung toxicity that mimicked that
39
observed after ozone exposure has been seen by Cortesi and Privett
in rats that received intravenous injections of fatty-acid hydroperoxides
or ozonides.
Lung lipid peroxidation during ozone inhalation was suggested by
the finding of conjugated diene bonds in an extract of the lungs of mice
90
exposed to ozone at 0.4-0.7 ppm for 4 h. The presence of thiobarbituric
acid reactants, predominantly malonaldehyde (another index of lipid
peroxidation), has been observed in the lungs of rats exposed to ozone at
33
0.7-0.8 ppm continuously for 5-7 days. The malonaldehyde concentration
was linearly related to the concentration of glutathione peroxidase, and
animals given a-tocopherol supplements did not have as great an increase
in either malonaldehyde or glutathione peroxidase. The authors suggested
that the increase in glutathione peroxidase concentration reflected the
activity of this enzyme in detoxifying lipid peroxides, rather than a
more direct ozone-induced intracellular radical or oxidizing species.
This is a crucial point, particularly because in later studies there was
31
no apparent threshold for the increase in glutathione peroxidases.
Lipid peroxidation is primarily a cell-membrane event, whereas GSH and
its related enzymes are intracellular. Therefore, although an increase
in these enzymes would presumably protect intracellular constituents
against oxidation that is secondary to lipid peroxidation, direct protection
of the cell membrane might not be expected. Accordingly, a lack of
threshold for a lipid peroxidation-induced increase in glutathione
peroxidase implies that any concentration of ozone produces lung lipid
8-40
-------
peroxidation. However, such an interpretation must be viewed with caution,
for at least two reasons: the assumption of linearity in the enzyme data
is open to question, particularly because the findings are not inconsistent
31
with a curvilinear function; and lung lipid peroxidation at low con-
centrations of ozone (e.g., 0.2 ppm) has still not been documented, and
it is possible that the observed enzyme increases, rather than reflecting
lipid peroxidation, are in response to other intracellular ozone effects.
If the latter is true, then the increase in glutathione peroxidase could
be considered an adaptive response with no pathologic consequences to
the lung, although this is open to debate. In this respect, it is of
180
interest that Prinsloo has reported an increase in lung hexose
monophosphate shunt enzymes after inhalation of quartz dust4
Further indirect evidence of a role of lipid peroxidation in ozone
toxicity has been obtained in studies in which animals deficient in
vitamin E were found to be more susceptible to lethal concentrations of
ozone and sublethal concentrations led to a more rapid utilization of
87,135
this antioxidant vitamin. Although vitamin E deficiency potentiates
the effects of ozone, it is not completely clear whether supranormal
concentrations of vitamin E protect against ozone toxicity. Mice given
tocopherol supplements were not protected against lethal concentrations
164
of ozone, and the specific activity of lung hydrolases was found to
48
be unrelated to dietary vitamin E concentration. However, other
investigators have reported that additional supplementation with vitamin E
above usual dietary concentrations lessens the extent of toxicity in
31,33,159
animals that inhale ozone.
8-41
-------
158
Mustafa et al. were unable to detect lung lipid peroxides after
short-term or subacute ozone exposures (0.8-2.0 ppm), but noted their
presence after in vitro exposures of mitochondrial preparations. Dowell
51
et al. saw no evidence of lipid peroxidation in an alveolar macrophage
preparation obtained from rabbits acutely exposed to ozone at up to 10 ppm.
The implications of an ozone-induced breakdown of UFA extend beyond
the destruction of these integral components of cellular membranes. Lipid
peroxides can produce hydrogen peroxide and oxidize sulfhydryl groups and
other amino acid constituents, and this results in enzyme inactivation.
In addition, lipid peroxidation has been implicated in one of the many
theories that attempt to explain the aging process—that based in part
on the apparent similarity of "normal" age pigments to the products of
the reaction of lipid peroxides with proteins. In particular, proteins
cross-linked by the dicarbonyl lipid peroxide breakdown product malonaldehyde
47
have fluorescent spectra similar to that of lipofuchsin age pigment.
22
Bruch and SchlipkOter noted lipofuchsin granules in the lungs of mice
exposed to ozone at 0.86 ppm for up to 10 months. Inasmuch as acceleration
191
of aging has been reported after chronic ozone exposure, it is con-
ceivable that this is mediated through lipid peroxidation. In addition
to free radicals and peroxides, the end products of the oxidative decom-
position of UFA include carbonyl compounds that may also have toxic effects.
26
Buell et al. reported the presence of carbonyl compounds in the lungs of
rabbits exposed to ozone at 1 ppm for 1 h and suggested that these compounds
can cross-link collagen or elastin and so lead to altered lung function.
Increased cross-linking of collagen has also been suggested as a mechanism
8-42
-------
of the deterioration of lung function with age. Recently, Sugihara and
205
Martin reported simulation of lung aging after exposure to formaldehyde,
a cross-linking agent.
Proteins. As described above, sulfhydryl groups are relatively
susceptible to oxidation by ozone, and a decrease in lung-protein
sulfhydryl groups has been reported as a consequence of ozone exposure.
Free sulfhydryl groups are important constituents of many enzymes, and
oxidation results in a loss in activity. In addition, cell-membrane
sulfhydryl groups play an important role in the transport of water and
ions, and it is conceivable that their oxidation in the lung is a factor
in ozone-induced pulmonary edema.
The oxidation of cysteine, as well as other amino acids, was studied
144
by Mudd et al. Individual amino acids in aqueous solution were exposed
to ozone; the reported order of susceptibility was cysteine, methionine,
tryptophan, tyrosine, histidine, cystine, and phenylalanine. Other amino
acids were not affected. This order is similar to that for the relative
susceptibility of amino acids to radiation and to lipid peroxides.
Evaluation of the ozonization products revealed that cysteine was con-
verted to cysteic acid, as well as cystine; methionine to methionine
sulfoxide; tryptophan to a variety of products, including kynurenine and
N-formylkynurenine; tyrosine also to a variety of products, including
dihydroxyphenylalanine; histidine to ammonia, proline, and other compounds;
and cystine in part to cysteic acid. In sane cases, the rate and end
products depended on the pH of the solution.
8-43
-------
Somewhat different oxidation products were observed by Previero
178,179
et al., who performed the ozonization in anhydrous formic acid,
rather than aqueous solution. This raises the possibility that in vivo
effects on protein may depend on the relative hydrophobicity of the
location of the susceptible amino acid, particularly in cell-membrane
lipoproteins.
A number of investigators have studied the effect of ozone on the
ultraviolet absorption spectra of proteins and amino acids. A decrease
in the absorption of 280-nm light in a number of proteins was originally
79
reported by Giese et al. to be a consequence of ozone exposure; they
suggested that this was due to an interaction of ozone with the ring
structures of tyrosine and tryptophan. Exposure of a solution of
tryptophan to ozone resulted in a decrease in 280-nm absorption, whereas
the extinction coefficient of tyrosine increased. Similar results with
191
tyrosine were reported by Scheel et al., who also noted alterations
in the ultraviolet spectra of egg albumen, perhaps representing dena-
turation by ozone.
91
MDre recently, B. Goldstein and McDonagh demonstrated that the
native protein fluorescence (280-nm excitation, 330-nm emission) of red-
cell membranes exposed in vitro to ozone at 1 ppm was a somewhat more
sensitive indicator of ozone effect than other characteristics measured
in the same system, including oxidation of cell-membrane sulfhydryl
groups, loss of acetylcholinesterase activity, and formation of lipid
peroxide breakdown products.
8-44
-------
Among the specific enzymes whose activity has been reported to be
decreased after in vitro ozone exposure are papain, glyceraldehyde-3-
133 107 144
phosphate dehydrogenase, lysozyme, ribonuclease, and acetyl-
83,167
cholinesterase. The latter enzyme appears to be particularly
susceptible to free-radical and oxidative states. A loss in acetyl-
23
cholinesterase activity has been reported in the red cells of humans
92
and mice that inhaled ozone. However, there are only minimal amounts
of this enzyme in lung tissue, and, although it has been suggested that
26
acetylcholinesterase is important in bronchial tract ciliary activity,
there is no direct evidence to support this conjecture.
As described elsewhere in this chapter, alterations in the activity
of a number of lung enzymes have been described after acute and chronic
ozone exposure. With the possible exceptions of the sulfhydryl-containing
enzyme succinic dehydrogenase and the cytochrome P-450 enzyme benzopyrene
hydroxylase, it is difficult to determine whether these findings are due
to a direct oxidative effect of ozone or are secondary to changes in
protein synthesis, concentrations of intermediates, or destruction of
cells or organelles.
Nucleic acids. Less is known about the interaction of ozone with
other macromolecules. Alterations of nucleic acids in solution have
34
been reported by Christensen and Giese, and in Escherichia coli by
177
Prat et al. in studies with relatively high concentrations of ozone.
Both purines and pyrimidines are attacked by ozone. However, the detailed
chemistry of the reaction, including the intermediates and end products,
has not been fully elucidated. This may be important, in view of the
8-45
-------
chronosonal effects of ozone, although such effects are most likely
due to the interaction of an ozone-induced intermediate with DNA, rather
than to ozone itself.
Studies of DNA synthesis in lung after ozone exposure have yielded
191
varied results. Scheel et al. exposed rats to ozone at 9.2 ppm for
45 min and reported an initial decrease in lung DNA content, which
returned to normal in 6 h. In contrast, lung RNA content was found to
increase sharply (as fraction of body weight) an hour after exposure.
41
Cronin and Giri found no change in DNA content per lung in rats exposed
56
to ozone at 4 ppm for 4 h. Evans et al. used a more sensitive auto-
radiographic procedure and reported a decrease in the fraction of mouse
lung cells that synthesized DNA immediately after exposure to ozone at
0.5-3.5 ppm for 6 h. DNA synthesis had returned to normal or above
219
normal within 72 h after exposure. More recently, Werthamer et al.
studied the uptake of tritiated thymidine, uridine, and leucine in lung
homogenates obtained from mice exposed to ozone at 2.5 ppm for 2 h/day
for up to 120 consecutive days. Both DNA and RNA synthesis initially
declined, but protein synthesis was greatly increased. By 30 days of
exposure, DNA synthesis was above normal, but RNA synthesis remained low.
Carbohydrates. Even less is known about the effects of ozone on
~26
carbohydrates. Buell et al. observed a decrease in the depolymerization
of hyaluronic acid after treatment of the lungs of ozone-exposed rabbits
88
(1 ppm for 1 h) with hyaluronidase. B. Goldstein et al. reported a
loss in membrane neuraminic acid of red cells exposed in vitro to high
concentrations of ozone. It would be important to study the effects of
8-46
-------
ozone on respiratory tract mucus, which is rich in carbohydrates, including
neuraminic acid. This could include determination of the extent to which
ozone is able to penetrate mucus that is unreacted, whether the reaction
of ozone with mucus results in the formation of cytotoxic intermediates,
and evaluation of the interaction in mucus of ozone with other air
pollutants, particularly sulfur dioxide. Of possible pertinence is a
63
study by Falk et al., who observed that ozone produced a loss in the
viral hemagglutinating ability of snail mucus.
Subcellular Components
Current approaches to understanding the biochemistry of organ
systems depend heavily on fractionation procedures designed to separate
various cellular and subcellular components. The lung is a very complex
organ, which contains many cell types that presumably function in dif-
ferent ways and may well have different key biochemical processes.
Unfortunately, the lung is difficult to homogenize and fractionate, and
this, along with the multiplicity of cell types, has greatly retarded
understanding of normal lung biochemistry.
Many studies have evaluated the biochemical effects of ozone and
other pollutants with whole-lung homogenates. This is a somewhat
unsatisfactory approach, inasmuch as a toxic effect at a specific target
site may be obscured by reciprocal adaptive changes in other pulmonary
cells or organelles, as well as by an influx of leukocytes and the
presence of edema. Of interest in this regard is the observation of an
22,170
ozone-induced increase in the number of lung Clara cells and a
shift from type 1 to type 2 pneumocytes, which has been hypothesized
8-47
-------
42
to be related to antioxidant defense. The biochemical concomitants
of these morphologic alterations are unknown and are unlikely to be
ascertained by using whole-lung homogenates. For a full understanding
of the effects of ozone in the lung, and in particular for a determination
of the lowest ozone concentrations that affect specific important indexes
of toxicity, more information on normal lung biochemistry is necessary.
In general, the lung has been considered to be the major site of
ozone toxicity, if for no other reason than because it is the first organ
to come into contact with inhaled ozone. It is therefore of interest
39
that, in a study by Cortesi and Privett/ intravenous injection of a fatty-
acid ozonide in rats resulted in lung, edema and hemorrhage and that on
gross examination the lung was the only organ noted to be affected.
206
Similar results were observed after injection of a fatty-acid hydroperoxide.
Other systemic agents that are relatively specific to the lung and whose
118
toxicity is perhaps mediated by free-radical reactions include paraquat
28
and 3-methylindole. These findings raise the possibility that there
is some unknown biochemical aspect of the normal lung that, in comparison
with other organs, makes it relatively susceptible to oxidative free-
radical-including agents like ozone.
Membranes. The possibility that pulmonary membranes are a primary
site of ozone toxicity is suggested by a number of lines of evidence,
most of which are indirect. These include observations that the membrane
171 193
is the major site of ozone toxicity in plants and bacteria;
morphologic evidence of pulmonary membrane damage after ozone exposure
in a number of studies; and in vitro experiments with human red cells
and artificial lipid membranes.
8-48
-------
As discussed above, UFA which are present primarily in cellular
membranes, appear to be particularly susceptible to oxidative degradation
by ozone. Various studies of membrane lipid peroxidation have implicated
this process in damage to organelles, including mitochondria, microscmes,
and lysosomes, as well as to the cell membrane itself. By analogy, it
is conceivable that many of the findings in cells and subcellular
components described in other sections of this chapter are secondary to
ozone-induced lipid peroxidation. However, this remains conjectural.
Furthermore, the effects of ozone on the cell membrane do not appear to
be limited to UFA. Protein is also affected, particularly cell-membrane
sulfhydryl groups and aromatic amino acids. Whether these protein
effects are secondary to cell-membrane lipid peroxidation or arise as a
direct result of ozone is not clear.
No studies of the effect of ozone on a lung plasma membrane fraction
have been reported. However, a few studies have evaluated the activity
in whole-lung homogenates of enzymes that are believed to be associated
191
with membranes. Scheel et al. reported a decrease in both 51-
nucleotidase and alkaline phosphatase concentrations (expressed as
amount per milligram of tissue) in rats exposed to ozone at 16.9 ppm
219
for 1 h or 6 ppm for 4 h. Werthamer et al. exposed mice to ozone at
2.5 ppm for 2 h/day on consecutive days. No effect on the concentration
of alkaline phosphatase in lung homogenates was observed after the first
day of exposure, and enzyme activity rose after 3 days of exposure. This
was followed by a precipitous decrease in alkaline phosphatase activity
(expressed as amount per milligram of lung protein) to about 50% of
8-49
-------
control values, which persisted for 30 consecutive days of exposure.
41
Cronin and Girl reported a decrease in lung adenosine triphosphatase
(ATPase) concentration (expressed as fraction of total lung weight) in
rats exposed to ozone at 4 ppm for 4 h. However, this appeared to be
due to the edema, inasmuch as recalculating the data in relation to
total DNA revealed no difference between control and ozone-exposed lung
ATPase concentrations.
Microsomes. An effect of ozone on lung microsomes has been suggested
by morphologic studies that indicated alterations in the endoplasmic
11,75,108
reticulum. Biochemical evidence of an effect on microsomal
166
enzymes was originally obtained in the studies of Palmer et al.,
who demonstrated that ozone exposure (0.75-LO ppm for 3 h) resulted in a
decrease in activity of Syrian hamster lung benzopyrene hydroxylase, a
mixed-function oxidase that depends on cytochrome P-450. No change in
hepatic activities of this enzyme were observed, and the results were
similar in animals in which high activities of benzopyrene hydroxylase
had been induced. The maximal effect was not observed until a few days
165
after the single ozone exposure. Palmer et al. also reported a decrease
in rabbit tracheobronchial mucosal benzopyrene hydroxylase activity after
exposure to similar ozone concentrations.
93
Recently, B. Goldstein et al. observed a decrease in microsomal
cytochrome P-450 concentrations in the lungs of rabbits exposed to ozone
at 1 ppm for 90 min. Again, the nadir of the cytochrome P-450 was not
85
reached until a few days after ozone exposure. B. Goldstein and Balchum
had previously obtained indirect evidence that microsomal cytochrome P-450
8-50
-------
played a role in the expression of ozone toxicity. Rats given inducing
regimens of phenobarbital, which are reported to increase cytochrane
P-450, were more susceptible to lethal concentrations of ozone; but
injection of allylisopropylacetamide, which destroys cytochrome P-450,
resulted in protection. The finding that mixed-function oxidase
119
inhibitors protect plants against ozone injury may be analogous.
Other known free-radical-trapping agents shown to protect against ozone
toxicity have often been given in multiple daily doses before acute
ozone exposure and may also be active through alteration of microsomal
intermediates. However, lung cytochrome P-450 concentrations have not
been measured in conjunction with any of these agents.
Liver cytochrome P-450 has been shown to be destroyed by lipid
190
peroxides, and in vitro exposure of lung microsomes to ozone is
93
accompanied by a loss in cytochrome p-450 and the formation of malonaldehyde.
Evidence of a possible effect of inhaled ozone on hepatic microsomes has
76
been obtained by Gardner et al., who demonstrated that mice exposed
to ozone at 1 ppm for 3 h on 2 or 3 successive days developed a prolongation
of pentobarbital sleeping time. No effect was observed immediately after
exposure on the first day, nor was there any significant difference from
the control after 4-7 days of exposure. The latter finding appeared to
be due to tolerance, inasmuch as increasing the dose to 5 ppm after 7
days at 1 ppm again resulted in a prolongation of pentobarbital sleeping
time. The authors suggested that their findings reflect a decrease in
hepatic microsomal metabolism of pentobarbital, perhaps due to an oxidizing
circulating intermediate.
8-51
-------
Mitochondria. Numerous ultrastructural studies have noted lung
11,15,
mitochondrial swelling and degenerative changes after ozone exposure.
16,170,174-176,192,197,198
Mitochondrial swelling occurs in vitro in
association with lipid peroxidation of the mitochondrial membrane.
However, the biochemical concomitants of ozone-induced damage to lung
mitochondria have not been extensively studied.
73
Freebairn noted a decrease in oxygen uptake of plant and bovine
liver mitochondria that was reversible by glutathione and ascorbic acid.
The activity of some mitochondrial enzymes, including succinic dehydrogenase
and cytochrome oxidase, has been found to be susceptible to ozone.
Mustafa and colleagues have performed a series of studies on the
effect of ozone on rat lung mitochondrial oxygen consumption. Acute-
exposure studies (2 ppm for 8 h and 3 ppm for 4 h) revealed that an initial
decrease in succinate dependent oxygen consumption was followed by a
rebound in which increase in the utilization of succinate, as well as
156,158
other substrates, was noted. This increase persisted for at least
3 weeks. No difference in the yield of mitochondria between control and
exposed lungs was noted immediately after ozone exposure, but there was
a definite increase in the number of mitochondria in the exposed lungs
within 48 h of recovery. The authors concluded that increased lung
mitochondrial oxygen consumption during recovery from ozone was due to
both enzyme activation and mitochondrial proliferation, but primarily
the latter. Continuous exposure to ozone at 0.8 ppm for 10 or 20 days
resulted in a significant increase in lung-homogenate oxygen consumption.
In a further experiment, rats were exposed continuously for 7 days to
8-52
-------
158
ozone at 0.2, 0.5, or 0.8 ppm. The observed increase in oxygen con-
sumption was statistically significant at all concentrations of ozone
and varied directly with dose.
159
More recently, Mustafa studied succinate-dependent mitochondrial
oxygen consumption in rats fed either a diet containing vitamin E at
approximately the normal American dietary intake or one with 6 times as
much vitamin E. A statistically significant increase in oxygen consumption
was observed in rats that received the diet lower in vitamin E when
exposed to ozone at either 0.1 or 0.2 ppm for 7 days. In rats on the
diet higher in vitamin E, ozone at 0.2 ppm for 7 days also produced a
significant increase, but ozone at 0.1 pprn was without effect. Unfortunately,
serum vitamin E concentrations were not given.
Lysosomes. The effect of ozone on lysosomal enzymes has been
studied by a number of investigators0 Ozone has been clearly shown to
inactivate lysozyme in vitro, but the effects of inhaled ozone on the
activity of lysozyme appear to depend on the pulmonary fraction under
107
study. Holzman et ajl. reported that exposure of rabbits or mice to
ozone resulted in a decrease in the lysozyme activity of bronchopulmonary
lavage samples. The effect was linearly related to the product of ozone
concentration and duration of exposure, although relatively high concen-
trations of ozone (2.0-5.5 ppm) were used in this acute-exposure experiment
(1-4 h). The authors also reported that alveolar cells present in the
bronchial lavage of rabbits exposed to ozone at 10 ppm for 3 h had a
decrease in the rate of lysosomal release when incubated in vitro. The
inference that this is due to in vivo oxidation of intracellular lysozyme
8-53
-------
is questionable, in view of the different cell populations present in
the ozone-exposed and control bronchial lavage specimens. Of interest,
however, is a reported decrease in the release of lysozyme from a peritoneal
polymorphonuclear leukocyte sample obtained from the ozone-exposed rabbits.
4,111
In further studies by the same group, depression in the activity
of lysosomal enzymes—acid phosphatase, g-glucuronidase, and lysozyme—
was observed in alveolar macrophages obtained from rabbits exposed to
ozone at as low as 0.25 ppm for 3 h. Enzyme concentrations returned
toward normal 24 h after exposure. An ozone-induced redistribution of
lysosomal enzyme into the cytosol was suggested by a fractionation study
that demonstrated a smaller fraction of enzyme activity in the alveolar
macrophage lysosomal pellet, compared with the supernatant, with increasing
110
doses of ozone. In vitro studies of rabbit alveolar macrophages in
tissue culture revealed an ozone-induced decrease in lysosomal acid
hydrolase activity, which was prevented when sulfhydryl compounds or
serum were added to the tissue-culture medium. A decrease in lysozyme
has also been reported in the tears of humans reacting to photochemical
189
smog.
In contradistinction to the decrease in lysosomal enzyme activity
observed in alveolar macrophages and bronchial lavage fluid, Dillard
48
et al. reported that continuous ozone exposure (0.70-0.79 ppm for 5-7
days) resulted in an increase in the activity of some lysosomal hydrolases
in rat whole-lung hcmogenates and lung fractions, including the soluble
supernatant. The tocopherol concentrations of the diet had no effect
on the findings.
8-54
-------
31
Similarly, Chow et al. observed an increase in the lysozyme
activity of a soluble lung fraction and of plasma after continuous
exposure of rats to ozone at 0.8 ppm for 8 days. However, no difference
in lung or plasma lysozyme activity from control values was present in
rats continuously exposed to 0.2 or 0.5 ppm or intermittently exposed
(0.2-0.8 ppm, 8 h/day for 7 days). Histochemical evidence of an increase
29
in lung acid phosphatase, a lysosomal enzyme, has also been reported.
The apparently conflicting data on lysozyme may perhaps be explainable
by considering three distinct effects of ozone: an irritative response
that produces an influx into the lung of leukocytes, including the
alveolar macrophage, which contain lysozyme at relatively high concen-
trations, thereby leading to an increase in whole-lung lysozyme concen-
tration; a disruption of lung lysosomal membranes, resulting in the
release of acid hydrolases; and oxidation of lysosonal protein, producing
enzyme inactivation. Evidence to support each of these processes is
available, and it appears that the net observed effects will depend on
the ozone dose and the lung fraction that is evaluated.
48 141
As discussed in detail by Dillard et al. and by Mittman et al.,
the possible relationship of lysosomal proteases to chronic lung disease
has been inferred from the finding of an increased incidence of emphysema
in subjects deficient in serum a -antitrypsin factor, an a -globulin
1 1
that can inhibit lysosomal proteases. (No effect of ozone on serum
a -antitrypsin inhibitor was noted in rabbits chronically exposed to
1 168
ozone. ) Thus, an ozone-induced increase in concentrations of such
enzymes in the lung might produce excess proteolysis and result in
eventual chronic lung disease. However, the available evidence is
inadequate to support the belief that such a process
8-55
-------
occurs in humans intermittently exposed to ozone that results from photo-
chemical smog formation. Further studies of this potential hazard would
be of value.
Connective Tissue. Despite physiologic evidence that chronic ozone
10
exposure may affect lung elasticity, there is very little information
concerning the biochemical effects of ozone on lung collagen. Buell
26
et al. obtained a collagen-containing fraction from the lungs of
rabbits exposed to ozone at 1 ppm for 1 h. A number of dinitrophenylhydrazine-
reacting carbonyl compounds were obtained after digestion with collagenase
or elastase. The authors suggested that such carbonyls might result in
intramolecular or intermolecular cross-linking of collagen with an
attendant decline in lung function. On the basis of present information,
these carbonyl compounds are most likely derived from lipdLd.
112
In a recent abstract, Hussain et al. presented evidence that
exposure of rats to ozone at 0.8 ppm for up to a week resulted in an
increased rate of collagen synthesis. Such a finding might be relevant
to ozone-induced fibrosis. Obviously, further study of the biochemical
effects of ozone on lung collagen and elastin are in order, particularly
in conjunction with chronic-exposure experiments.
Alveolar Macrophages
Alveolar macrophages represent a major line of pulmonary defense
against exogenous material, including infectious agents and particles.
Although the origin of these phagocytic cells is still not completely
clear, recent information suggests that they are derived from the bone
24
marrow, but are capable of further division and replenishment in the
8-56
-------
81
lung. As discussed below, a number of investigators have reported
alterations in alveolar macrophage function and biochemistry after ozone
exposure. Before a description of their observations, one potential
difficulty in interpreting the effect of ozone inhalation on alveolar
macrophages should be mentioned. Inhalation of ozone or other irritants
results in an alteration of the number of alveolar macrophages obtained
in a bronchial lavage. Presumably, this is due to a combination of cell
destruction and an influx of younger alveolar macrophages in response
to the irritant stress. It is well known that immature human granulocytes
have functional capacities and concentrations of biochemical intermediates
different from those of mature polymorphonuclear leukocytes. Unfortunately,
there is no readily available morphologic indicator of alveolar macrophage
maturity, as there is for granulocytes. Accordingly, observed differences
between alveolar macrophages obtained after ozone exposure and those
present in normal lungs may simply reflect relative immaturity secondary
to pulmonary irritation, rather than a direct effect of ozone on bio-
chemistry or function.
Interest in the effects of ozone on alveolar macrophages has been
spurred by the observation that relatively low concentrations of ozone
potentiate respiratory infections in animals and perhaps man. Coffin
37
et al. observed a decrease in the number of bacteria phagocytized by
alveolar macrophages obtained from rabbits exposed to various concen-
trations of ozone as low as 0.3 ppm. Some suggestion of a lack of
threshold is present, but it is not clear whether the difference from
the controls at lower ozone concentrations is statistically significant.
8-57
-------
These findings in rabbits are similar to those of E. Goldstein
94-97
et al_., who have related increased bacterial infectivity in mice to
an ozone-induced impairment in the bactericidal capabilities of alveolar
macrophages. They used radioactively labeled bacteria and observed a
decrease in mouse lung bactericidal activity after a 4-h exposure to
ozone at about 0.3-0.4 ppm. With this technique the effects of ozone
97
and nitrogen dioxide are roughly additive, and silicotic mice are no
94
more susceptible to ozone than are control mice.
51
Dowell et al. reported an increase in the osmotic fragility of
alveolar macrophage preparations obtained from rabbits acutely exposed
to ozone at 10 ppm for 3 h or intermittently exposed to ozone at 2 ppm
for 8 h/d for 7 days. Similar intermittent exposure to ozone at 0.5 ppm
was without effect. A test for malonaldehyde formation was negative,
but this lipid peroxide breakdown product may have been lost during the
preparatory procedure.
Additional studies related to the alveolar macrophage include that
218
of Weissbecker et al., who demonstrated that in vitro exposure to
ozone at as low as 0.06 ppm resulted in alveolar macrophage cell death.
183
However, Richmond observed only a slight decrease in bacterial
phagocytosis during in vitro incubation of alveolar macrophages with an
initial ozone concentration of 0.8 ppm. Inasmuch as ozone was not
administered continuously, the dose to the cells may have been minimal.
78
Gardner et al. noted the ozone-induced loss of an alveolar
macrophage protective component in lung lavage fluid after acute ozone
exposure (10 ppm). This factor appears to stabilize alveolar macrophages
8-58
-------
in lung fluid, and its loss would result in a decrease in cell viability.
As pointed out by the authors, this finding might indicate that the
reported effects of ozone on alveolar macrophages are, at least in part,
due indirectly to an action on an alveolar fluid component, rather than
on the macrophage itself. The substantial decrease in recoverable
alveolar macrophages after ozone inhalation does suggest that ozone has
a direct effect on alveolar macrophages, as does the study of Huber
108
et al., who noted nonspecific ultrastructural alterations in rabbit
alveolar macrophages after exposure to ozone at 5 ppm for 3 h. However,
other investigators have failed to observe morphologic abnormalities in
16,176
alveolar macrophages after inhalation of ozone.
Mechanisms by which ozone might interfere with bactericidal function
include an alteration in cell-membrane function that produces a loss in
116
phagocytic ability and is perhaps mediated by lipid peroxides and a
decrease in the ability of alveolar macrophages to kill phagocytized
bacteria. Leukocytes in general appear to have a multiplicity of
mechanisms for destroying ingested bacteria.
Ozone might interfere with the intracellular bactericidal capabilities
of alveolar macrophages by inactivating lysosomal hydrolases, or perhaps
through the destruction of heme-containing enzymes that are apparently
involved in producing superoxide anion radical. Further evaluation of
the process by which relatively low concentrations of ozone potentiate
bacterial infection would be of value.
8-59
-------
Extrapulmonary Effects
An appreciable body of evidence has accumulated to indicate that
ozone has extrapulmonary effects. Although some of the reported effects
may be secondary to the reaction of ozone with intrapulmonary neural
receptors or to release of humoral substances from the lung, other
findings appear to be more directly related to an oxidizing effect of
ozone. The biochemical basis for the latter is unclear, particularly
because the reactivity of ozone and its short-lived intermediates would
make it unlikely for them to penetrate the pulmonary parenchyma. Earlier
studies on the subject of extrapulmonary effects have been reviewed by
201
Stokinger.
Industrial and epidemiologic evidence associating ozone exposure
with headache and drowsiness are relatively nonspecific and do not clearly
124
indicate extrapulmonary effects. Lagerwerff noted changes in a number
of indexes of vision at ozone concentrations of 0.2-0.5 ppm during short-
20
term exposures. In addition, Brinkman and Lamberts reported a 50%
decrease in the rate of desaturation of oxyhemoglobin in the skin
capillaries of a tied-off finger during inhalation of ozone at 1 ppm
(the experimental procedure was not given in detail). Neither of these
studies, which have been in the literature for some time, has been
replicated.
23
Recently, Buckley et al. have described statistically significant
changes in a number of constituents and properties of red cells and serum
in human volunteers experimentally exposed to ozone at 0.5 ppm for 165
min. Their findings included an increase in red-cell osmotic fragility
8-60
-------
and a decrease in red-cell acetylcholinesterase and glutathione, all of
which were consistent with previous in vitro or animal studies. They
also observed an increase in serum thiobarbituric acid reactants con-
sistent with lipid peroxidation and an increase in serum vitamin E that
they attributed to its mobilization. The thiobarbituric acid assay is
predominantly a measure of malonaldehyde. Increased serum malonaldehyde
concentrations have usually been reported in man only in association
with significant red-cell lipid peroxidation, such as occurs in hemolytic
vitamin E deficiency, presumably because malonaldehyde is rapidly
metabolized and cleared from the serum. Also consistent with acute
hemolysis is the observation by Buckley et al. in the same subjects of
increases in serum lactic dehydrogenase and in red-cell G-6-PD. In
contrast with those in the lung, G-6-PD increases in the anucleate red
cell are thought to represent solely a decrease in mean red-cell age
consistent with reticulocytosis, which (to explain the extent of the
G-6-PD increase in this study) would be consistent with a relatively
significant acute hemolysis. Data necessary to interpret this possibility
99
were not fully presented. A more recent report from this group
evaluating dose-response data for human 2-h exposures to ozone at 0.25,
0.37, and 0.50 ppm showed a no-effect concentration of 0.25 ppm for mean
change in red-cell acetylcholinesterase activity and osmotic fragility
and a linear dose-related effect on these two characteristics at the
higher ozone concentrations.
A number of animal studies have revealed extrapulmonary effects.
Again, there is some question as to which of these may represent an effect
8-61
-------
of ozone, or a direct ozone-induced intermediate, rather than a more
indirect response to pulmonary toxicity, perhaps mediated by neurohumoral
factors. Thus, for instance, the observations of altered hepatic nucleic
191 50
acid concentrations, shifts in the content of metals in the liver,
102
alterations in urinary pH, increases in liver weight and alkaline
148
phosphatase activities, and variations in the circulating white-cell
17
count in ozone-exposed animals conceivably represent nonspecific
responses to lung injury.
Of interest is the experimental approach whereby ozone is delivered
solely to one lung. The observation of pulmonary effects in the unexposed
71
lung indicates that there are extrapulmonary effects of ozone at
edematogenic concentrations. However, only the exposed lung appears to
develop tolerance to later ozone exposure and to exhibit impairment of
2,3,72
bacterial defense mechanisms.
Evidence of a direct oxidizing effect on the blood of mice and rats
inhaling ozone was obtained in a study in which an increase in an in vivo
B7
red-cell catalase-reacting compound, presumably hydrogen peroxide, was
noted. Although this was observed only at ozone concentrations of 5 ppm
or greater, the indirect assay for red-cell hydrogen peroxide used in
this study is relatively insensitive and would not detect smaller degrees
of ozone-induced oxidant stress. A significant decrease in the activity
of red-cell acetylcholinesterase, a membrane constituent known to be
sensitive to lipid peroxides, has been reported in mice exposed for 4 h
92
to ozone at 8 ppm. However, only a slight decrease in red-cell
acetylcholinesterase was noted in rabbits chronically exposed to ozone
8-62
-------
114 21
at 0.4 ppm. An earlier study by Brinkman et al. noted that 30-60
min of inhalation of ozone at 0.2 ppm potentiated the sphering of animal
and human red cells irradiated in vitro. The contention that this
intriguing effect is related to an increase in aging by ozone is open to
question. Ozone effects in blood also include chromosal aberrations in
223,224
the circulating lymphocytes of hamsters, an increase in plasma
31 169
lysozyme, higher serum concentrations of trypsin protein esterase,
136,137
and Heinz bodies in circulating red cells. Earlier studies by
140
Mittler et al. failed to reveal any change in the hemoglobin or
hematocrit of young rats chronically exposed to ozone at 2.4 ppm.
Biochemical changes in animal central nervous systems have been
195
reported by Skillen et al., who noted a decrease in brain 5-hydrox-
ytryptamine (serotonin) in rats exposed to ozone at 6 ppm for 4 h, and
211
by Trams et al., who observed decreases in catecholamines and catechol-
0-methyltransferase in dogs chronically exposed to ozone at 1, 2, or 3
ppm. Electroencephalographic (EEC) measurements in the same dogs were
115
recently presented by Johnson et al., who noted alterations in EEC
patterns at 9 months of ozone exposure, but not after 18 months of
221
exposure. Previously, Xintaras et al. had observed alterations in
the visual evoked electric response in rats acutely exposed to 0.5-1.0
115
ppm. As pointed out by Johnson ejt al., it is not clear whether these
findings indicate a direct neurotoxic action of ozone or are secondary
to damage in other organs.
Other reported systemic effects of ozone include histologic changes
8
in the parathyroid glands of rats exposed to ozone at 0.75 ppm for 4-8 h,
8-63
-------
variations in rat thyroid function that depend on the concentration and
61
duration of ozone exposure, alterations in myocardial histology in
21
mice exposed to 0.2 ppm 5 h/day for 3 weeks, ECG changes in dogs
chronically exposed to irradiated auto exhaust (containing oxidants at
14
0.4-0.8 ppm), inhibition of gastric motility in rats exposed to ozone at
186
0.5 ppm for 2 h, and a decrease in the release of lysozyme frcm
107
peritoneal granulocytes in ozone-exposed rabbits.
169
An interesting report by P'an and Jegier noted an increase in
serum trypsin protein esterase in association with pulmonary vascular
lesions in rabbits chronically exposed to ozone at 0.4 ppm. This serum
a-2-macroglobulin, which is synthesized in the liver, has been reported
to be increased in human vascular disorders, but its physiologic
significance is unknown.
In summary, the current evidence appears to support the contention
that ozone or an oxidizing derivative is able to penetrate the alveolar
basement membrane into the pulmonary circulation. Recent evidence,
which requires replication, suggests that red-cell changes consistent
with an oxidizing effect can be detected in the blood of humans exposed
to ozone at ambient concentrations. There is also evidence that ozone
affects other extrapulmonary organ systems, but it is not clear whether
this is due to oxidizing intermediates—such as ozonides, peroxides, and
the resulting carbonyl compounds carried in the circulation—or whether
it is secondary to reflex arcs or to humoral processes initiated in the
lung.
8-64
-------
MJTAGENIC AND CARCINOGENIC ACTIONS
The supposition that ozone is mutagenic or carcinogenic in man is
based primarily on information on the biochemical mechanism of ozone
toxicity and to a lesser extent on in vitro and animal studies. The
biochemical evidence is for the most part indirect and depends on an
analogy between the free-radical nature of ozone toxicity and of radiation
and other carcinogenic agents.
The production of chromosomal abnormalities by ozone was first
64
observed in plants by Fetner, who noted abnormal anaphases in the root
tips of Vicia fava seeds exposed to ozone. Bacterial mutagenesis by
43,214
ozone has been reported by a number of investigators. Hamelin and
100,101
Chung noted an increased mutation rate in Escherichia coli
exposed to ozone at as low as 0.05 ppm for 5 min and observed that the
mutants were sensitive to ozone and x irradiation. They suggested that
ozone might interact in DNA repair processes. Other studies indicating
ozone-induced chromosomal effects include the observation of mitotic
66
inhibition in grasshopper neuroblasts and abnormalities in the eggs of
126
oysters treated with ozonized seawater.
65
Fetner has also demonstrated chromatid breaks in a human tissue-
culture cell line exposed to ozone at 8 ppm for 5 min. Other tissue-
187
culture studies include that of Sachsenmaier et al., who noted
tetraploidy and other chromosomal abnormalities in embryonic chick
fibroblasts exposed to ozone and a decrease in transplantability of
163
mouse ascites tumor cells. In addition, Pace et al. demonstrated an
interference by ozone with mitotic activity in two tissue-culture cell
8-65
-------
19
lines. More recently, Booher et al. reported that lung cells exposed
in culture to ozone concentrations as low as 0.3 ppm demonstrated an
inhibition in growth that was proportional to the ozone concentration.
223,224
Of particular interest are the studies of Zelac et al. in
which Chinese hamsters exposed to ozone at 0.2 ppm for 5 h had an increased
number of chromosomal breaks in their circulating lymphocytes. Blood
samples for study were obtained inmediately after exposure and 6 and 15.5
days later. The highest break frequency was observed after the longest
delay. The authors compared the effects of x irradiation and ozone
singly and combined, in their system. The combined effects were less
than additive; this suggested some protective mechanism, perhaps analogous
103
to that observed by Hattori et al. When the authors extrapolated their
data to acceptable industrial-hygiene exposures to ozone and radiation,
ozone was found to be much more likely than x irradiation to produce
chromosomal breaks in such exposures.
138
More recently, Mertz et al. has studied the circulating lymphocytes
of humans experimentally exposed to ozone at 0.5 ppm for 6-10 h. A
statistically significant increase in the number of minor chromosomal
abnormalities (not breaks) was observed; it reached a peak about 2 weeks
after exposure and later returned to normal. This delay in the development
of chromosomal abnormalities observed after ozone exposure in both hamsters
and humans differs from that observed in human radiation studies, in
which aberrations tend to remain roughly constant over 3-4 weeks. This
raises the possibility that the ozone-induced abnormality is related to
a postreplication repair process.
8-66
-------
Carcinogenic or mutagenic effects of ozone have also been suggested
199
by a number of other animal studies. Stokinger noted that ozone
exposure resulted in an increased incidence of pulmonary adenomas in a
strain of mice prone to develop these benign neoplasms. Howerver, the
experimental findings were not reported in detail. A combination of
ozone and gasoline has also been shown to cause an increased incidence
121,122
of lung tumor in two strains of mice, only one of which is prone
to develop pulmonary adenomas.
A mutagenic effect of ozone on germ cells was suggested by the study
21
of Brinkman et al., in which female mice exposed to ozone at 0.1-0.2
ppm 7 h/day 5 days/week for 3 weeks before birth, demonstrated a fourfold
increase in neonatal mortality. A further report of this study noted
213
increased blepharophimosis and jaw anomalies and a decrease in litter size.
An artificial oxidant smog mixture derived from irradiated auto exhaust
has also been reported to cause an increase in neonatal mortality in
109,125
mice.
The toxicologic evidence indicating a possible role of ozone in
human cancer may be summarized as follows:
• The biochemical mechanism of ozone toxicity appears to have many
similarities with those of other agents, particularly ionizing
radiation, that are known human carcinogens.
• In vitro studies with tissue-culture cell .lines and bacteria have
demonstrated ozone-induced chromosomal effects.
• Some animal studies with ozone or synthetic photochemical smog
have shown chromosomal defects in circulating lymphocytes, a
8-67
-------
more rapid appearance of benign pulmonary tumors, and an increase
in neonatal mortality consistent with a mutagenic effect.
• One study of humans experimentally exposed to ozone showed
transient development of minor chromosomal abnormalities in
circulating lymphocytes.
The toxicologic studies must be considered in the perspective of an
absence of epidemiologic evidence that links photochemical air pollution
with human cancer. Despite the presence of significant concentrations of
ozone in southern California for three decades, no associated increase in
cancer has been observed. However, the relatively recent arrival and the
peripatetic nature of Los Angelenos might obscure, for the present, a
carcinogenic or mutagenic effect of ozone. Furthermore, it is necessary
to consider the possible toxicologic interaction between ozone and other
airborne carcinogens. The reported ozone-induced decrease in lung
benzopyrene hydroxylase and cytochrome P-450 concentrations could be
interpreted as protecting against aromatic hydrocarbon carcinogerisis in
which in vivo activation appears necessary. Alternatively, it could be
hypothesized that ozone would directly activate aromatic hydrocarbon
carcinogens (e.g., by conversion to epoxides or other free-radical
intermediates) and therefore promote the presumed carcinogenic process.
This speculative discussion is presently solely to illustrate the potential
complexities of the problem of ozone-induced carcinogenesis. Obviously,
far more information is needed on the biochemical action of ozone and
the interaction of ozone with other potential carcinogens. This would
allow more confident assessment of the possible role of ozone in human
carcinogenesis until definitive epidemiologic information is available.
8-68
-------
EFFECTS ON REPRODUCTION
As noted previously, exposure of mice to simulated photochemical
smog produced by irradiating diluted auto-exhaust mixtures resulted in
109
reduced fertility and fecundity and decreased infant survival. Lewis
125
et al. pursued this observation in greater depth and showed that the
nonpregnancy rate was significantly (p< 0.02) greater (20 of 153) in
female mice that were mated with male mice that had been exposed for 46
days to irradiated auto exhaust than in females that were mated with
males that were in clean-air chambers (nine of 159). No differences in
the groups with respect to the presence of copulatory plugs and absence
of implantation scars in the nonpregnant females supported the authors
conclusion that the differences in pregnancy rates were due to reduced
fertility. In pregnant females that had been mated with irradiated-
exhaust males, there were fewer uterine implantation scars and fewer
pups per litter (p_< 0.05) than in females mated with clean-air males.
In addition, offspring viability was reduced in litters that were kept
in irradiated-exhaust chambers. The concentration of oxidant (ozone)
varied during each day of exposure, with peaks as high as 1.0 ppm.
Daily nitrogen dioxide and carbon monoxide concentration peaks were about
1.5 ppm and 100 ppm, respectively. The results of these experiments
suggested a possible mutagenic effect in male germ cells resulting from
exposure to the oxidant mixture.
In an earlier study of a simpler oxidant smog mixture made by reacting
ozone with gasoline vapors (oxidant concentration, 1.25 ppm in the mixture
123
by neutral potassium iodide method), Kotin and Thomas exposed male and
8-69
-------
female mice to the synthetic oxidant mixture, to Los Angeles air, and to
washed air. Significant differences from controls in reproduction effects
were noted only in mating pairs in the synthetic smog mixture. These
consisted of reduced conception rates, litter size, and survival of
newborn (that were held in the exposure chambers until weaning). These
authors also alluded to possible mutagenic effects associated with organic
peroxides that would be expected in the synthetic mixture; however, they
felt that their data on fecundity reflected an effect primarily on the
females.
21 213
Brinkman et al. and Veninga exposed mated pairs of their
laboratory's inbred gray mice and CSV black mice to ozone at 0.1 or 0.2
ppm 7 h/day 5 days/week for 3 weeks. There was little or not effect on
litter size, compared with air-exposed controls; however, there was a
greater incidence of neonatal mortality during the first 3 weeks of life
in the litters of ozone-exposed parents. Offspring (C57 blacks exposed,
in addition, for 3 weeks postnatally) from the 0.2-ppm-ozone groups had
increased incidence of blepharophimosis and increased incidence of jaw
abnormalities. The authors concluded that this was further evidence of
a similar action of ozone and ionizing radiation (which produced the same
effects at a dosage of 20 r/day).
These studies, although few, suggest that exposure to photochemical
oxidants can influence fertility and fecundity in animals and that the
general health of newborn animals is much more likely to be impaired by
exposure to oxidants than that of their parents. Whether the changes
observed in reproduction variables can be related to mutagenic actions of
8-70
-------
ozone, discussed earlier, remains to be determined. In any event, it
seems logical that effects of low concentrations of ozone and other
photochemical oxidants on reproduction must be indirect and may be
mediated by endocrine or ozone-biologic reaction products.
CENTRAL NERVOUS SYSTEM AND BEHAVIORAL EFFECTS
It is somewhat surprising that possible central nervous system (CNS)
or behavioral responses to ozone exposure have not been subjected to
greater investigation, in view of the reports of headache and drowsiness
in humans exposed to ozone and the apparent CNS depression that occurs
200,201
as an early sign of ozone interaction in animals. Xintaras
221
et al., in an application of the evoked-response technique, found a
depression in the specific visual cortex and in the superior colliculus
53
of rats exposed to ozone at 0.5-1.0 ppm for 1 h. However, Eglite found
no change in rat behavior or chronaxial muscle ratios after 93 days of
124
exposure to ozone at 0.6 ppm. Lagerwerff demonstrated in human
volunteers that repeated exposure to ozone at concentrations of 0.02-0.05
ppm resulted in psychophysiologic or sensoriphysiologic changes, including
decreased visual acuity, increased peripheral vision, altered extraocular
muscle balance, lethargy, and difficulty in concentrating.
As mentioned previously, decreased voluntary running activity of
mice was one of the most sensitive indexes of an effect of ambient photo-
55
chemical oxidant air pollution or simulated oxidant smog that was
109,147
produced in the laboratory by irradiating diluted auto-exhaust gasses.
Whether this effect of the mixtures was due to only ozone or other oxidant
is not certain. It is plausible to conclude that ozone was the effective
8-71
-------
153
agent, in view of the fact that Murphy et al. shaved that ozone at as
low as 0.20 ppn (during a single 6-h exposure) reduced voluntary running
activity of mice by 50%.. The 6-h exposure used in those studies coincided
with the maximaL activity period of the animals (i.e., darkness, in
adapted mice), so it seems that the effect of ozone overcame strong
natural motivation for running activity. Furthermore, Konigsberg and
120
Bochman noted a concentration-related reduction in the gross motor
activity of rats exposed to ozone at 0.1-1.0 ppm. As reported for oxidant
109
mixtures, mice exposed continuously to ozone at 0.3 ppm adapted and
153
returned to normal activity in about a week. However, the same mice
were still susceptible to the activity-reducing effect of higher concen-
trations (0.6-0.8 ppm), and adaptation to control activity did not occur
153 68
for at least 7 days of continuous exposure. Fletcher and Tapell
reported that the voluntary running activity of rats was reduced by 84%
during continuous exposure to ozone at 1 ppm for a week. Boche and
18
Quilligan also demonstrated that the oxidant mixture produced by
ozonizing gasoline vapors (ozone content, 0.4 ppm or greater) caused a
decrease in running activity in mice.
These studies, although demonstrating that reduction of voluntary
running activity in mice is a very sensitive biologic indicator of oxidant
and ozone, did not reveal the mechanism of the effect. It is possible
that this effect represents only a precautionary reaction of the organism
to avoid moving about when its senses detect (by odor or irritation) a
strange and unpleasant stimulus. This would be consistent with the
observation of avoidance, by mice, of a cage ventilated with ozone at
3-72
-------
172
0.6-1.1 ppm in preference for a clean-air cage. Reduction of voluntary
running activity might also be secondary to lung irritation or inflaimation;
however, the concentrations for activity reduction are below those
generally associated with edema or other signs of local injury in the
lung. Finally, one could evoke a systemic mechanism of action as a direct
effect of circulating ozone (which seems unlikely) or of a CNS-depressant
oxidant-biologic reaction product formed locally in the lung. Further
studies would be required to determine whether these or other mechanisms
are involved.
SUMMARY OF DOSE-RESPONSE RELATIONSHIPS
The acute lethal action of ozone is due to its capacity to produce
pulmonary edema. The LC for rats and mice exposed for a single 4-h
period is approximately 6 ppm, and cats, rabbits, guinea pigs, and dogs
199
(in that order) are decreasingly susceptible to the lethal action.
Numerous reviews have considered the toxicity of ozone at lethal and
113,146,162,199-202,212
lower concentrations.
In the foregoing discussion and in Table 8-2, attention has focused
on studies in laboratory animals that have been exposed to ozone concen-
trations of about 1 ppm or less, because results of studies conducted
with such concentrations are thought to be more directly relevant to
ambient oxidant air pollution, which is the source of exposure for large
human populations. In Table 8-2, no attempt has been made to list all
studies; more comprehensive summaries can be found in some of the mono-
graphs cited. Instead, the table cites studies thought to be most useful
for evaluating the health implications of exposure to low concentrations
8-73
-------
of ozone, and the concentrations listed are the lowest at which the
described effects have been observed. Unfortunately, many studies have
not included a sufficient range of experimental concentrations to permit
construction of reliable dose-response curves or to determine what, if
any, would be a "no-observed-effect" concentration for the experimental
conditions used. Although it is understandable that research scientists
find little stimulation in conducting exposure experiments at concen-
trations that fail to produce changes in the biologic system in which
they are interested, the conduct (and reporting) of such experiments is
extremely important for a pragmatic evaluation of the implications of
positive findings for human health.
The table illustrates the wide variety of biologic effects produced
in laboratory animals exposed to relatively low concentrations of ozone.
Obviously, some effects have more serious health implications than others.
3-74
-------
00
r-i
CM
^
in
CM
ro
CN
CO
in
ro
,-H
CM
0)
tn
(U
to
QJ
3
CN
CO
ro
in o
I
Ti
oo
(N
•w
Is
i -H
oo
o
CM
3-75
-------
i
CM
CM
co
CM
CM
in
rH
CM
ro
in
CTl
o
CTi
CM
CXI
XI
in
CO
CM
X!
CM
in
CM
•
o
m
CN
•
o
CN
in
CN
O
in
CM
o
ro
•
o
in
•
o
r-
ro
o
8-76
-------
oo
m
CM
CM
r-
ro
in
LO
ro
in
-P
a
CN
OO
e
13
8
4-1
4-1
W
•3
5
a
I
0)
D
•H W
M-l -H
U
-H
o
V
CN
in
o
in
oo
oo
o
oo
vo
o
r-
•
o
3-77
-------
8
S
id
O rH CNJ
co n ro n
CN
oo
co
w tn
•H co
-P
d r-l
0 O
in
-P
S
O
IT)
t^
•
o
00
•
O
co
8-78
-------
CTi CN
(N
00
n
a-
0 rt
N u
o -0
u
oo
o
8-79
-------
RED3MMENDATIONS FOR RESEARCH
Enhanced susceptibility to respiratory exposure to infectious agents
is of considerable potential public health significance. This has been
reported to occur in mice exposed to ozone at as low as 0.08 ppm, the
lowest reported "effect" concentration in laboratory animal studies.
It seems essential, therefore, to continue and expand research on the
effect of ozone and other photochemical oxidants on physiologic protective
mechanisms of the lung. Appropriate dose-response studies should be
included to confirm or establish the exposure concentration-time rela-
tionships that result in increased susceptibility to inhaled microorganisms,
and studies of the cellular responses and mechanisms should be conducted
with a view to providing methods that are applicable to epidemiologic
studies in oxidant-exposed human populations.
Research designed to elucidate the pathophysiologic implications of
reversible changes in lung function, histology, and biochemistry that
have been observed at concentrations of 0.2-0.5 ppm would be especially
valuable in evaluating the significance of these changes for health. In
particular, it would be useful to determine what, if any, causal or
correlative relationships exist between different effects detected by
various experimental assay systems and between reversible changes and
more chronic effects, such as reduced lung elasticity, fibrosis, and
adencma formation. Studies on laboratory animals are particularly
suited to this type of mechanism-correlative research; but, with appropriate
experimental designs, such research should be very useful in determining
which methods or biologic changes can be usefully applied to clinical or
8-80
-------
epidemiologic studies. At the same time, such research could determine
whether sane of the changes (e.g., increased activity of enzymes involved
in cell redox systems) are indicative of injury or are homeostatic
adaptive responses. This information will have value in predicting
potential injury in the "average" population and possible help to identify
people who are hypersusceptible by virtue of some deficiency in adaptive
protective mechanisms. Related to these research efforts, further
investigation of the influence of oxidant exposure on enzymes that bio-
transform other inhaled chemicals (e.g., aromatic hydrocarbons) and the
interaction effect of dietary antioxidants (e.g., vitamin E) should be
pursued, particularly in relation to oxidant-induced oxidation of membrane
lipids and free-radical formation.
There are several scattered reports of extrapulmonary effects of
ozone exposure in laboratory animals. Some (e.g., chromasomal aber-
rations in hamster lymphocytes) occur at or near concentrations that
cause local effects in the lung and portend serious and long-term health
implications. Others(e.g., reduction of voluntary activity) may be
transient or reversible, but nevertheless contribute to decrements in
performance or well-being. It is particularly important that further
research be conducted to confirm (or refute) these reported extrapulmonary
actions of ozone and the exposure concentrations at which they occur.
If confirmation of their occurrence is obtained at or below the currently
reported effective exposure concentrations, useful research efforts could
be directed toward determining whether they are direct or secondary
effects and toward identifying the chemical species responsible. More
8-81
-------
importantly, confirmation of an isolated effect on cell genetic material
would demand a thorough expert evaluation of its significance on the
basis of existing knowledge of the long-term implication of the effect
and, accordingly, intensified laboratory and epidemiologic research.
DISCUSSION
During the last decade, toxicologic research on the effects of ozone
in laboratory animals has demonstrated that exposure for a few hours to
airborne concentrations of less than 1 ppm produces numerous changes in
cell and organ structure and function. The limiting concentrations
required to produce these changes appear to differ somewhat among different
species of laboratory animals and with the particular type of effect under
investigation. However, there seems to be little doubt that several
functional and morphologic indexes of response to ozone are altered with
exposures to ozone concentrations of about 0.2-0.5 ppm. Many of the
functional and morphologic changes produced in experimental animals
exposed to ozone as a single contaminant gas have also been demonstrated
to occur with exposure to complex mixtures of laboratory-produced or
ambient photochemical oxidant air pollution.
Most research has focused on the effects of ozone on lung function,
morphology, and biochemistry. Altered lung function, observed in studies
of the mechanical behavior of lungs of several species, has been noted
as the result of a few hours of exposure to ozone at 0.2-0.3 ppm.
Improved techniques for detecting minimal pulmonary edema and for examining
the microstructure of cells of the respiratory tract indicate that structural
alterations also occur with short exposures to this range of concentrations.
8-82
-------
Furthermore, altered activities of various lung enzymes or enzyme systems,
particularly those involved in defending against oxidant stress, have
been noted by several investigators to occur at concentrations of 0.2
ppm. Although all these effects appear to be accentuated by higher con-
centrations of ozone, indicating a dose-response relationship, most
investigations have not determined (or have failed to report) whether
lower concentrations fail to produce such changes. In spite of the fact
that biochemical, functional, and morphologic effects have all been
detected at about the same low exposure concentrations, there has been
little systematic investigation to determine whether these effects are
causally related. Some effects noted in these experiments might be
considered adaptive, rather than injurious. For example, the increased
activities of lung glutathione peroxidase and glutathione reductase that
have been demonstrated after exposure to 0.2 ppm may represent an adaptation
or compensation to an injurious effect, such as lipid peroxidation, which,
although detected only at exposures to 0.4 ppm and above, may go undetected
at lower exposure concentrations because of the insensitivity of current
assay methods. In spite of these unknowns, it is noteworthy that, in the
one case in which it is possible to make direct comparisons of the effects
of ozone in laboratory animals ard in humans in controlled experiments—
i.e., lung-function studies—the minimally effective concentrations are
nearly identical, around 0.3 ppm. It is tempting, therefore, to speculate
that humans might also sustain the biochemical and morphologic changes
observed in laboratory animals exposed to this concentration; but such
a conclusion must await mechanistic information concerning the relationships
8-83
-------
between the different types of effects or independent demonstration of
these effects in man.
Recent studies involving repeated or prolonged exposures of
laboratory animals to ozone suggest that changes that are indicative of
chronic lung diseases (such as decreased elasticity of the lungs, hyper-
trophy of bronchiolar epithelium, and deposition of connective tissue)
also require concentrations of 0.2-0.5 ppm. At slightly higher concen-
trations, fibrotic changes in the lungs have been observed histologically;
this is consistent with a reported increased rate of collagen synthesis
in the lung. It appears, therefore, that the changes observed with short-
duration exposures, although generally reversible on cessation of exposure,
are as sensitive in evaluating the injury potential of exposure to ozone
as are long-term exposure studies. There have been, however, very few
truly chronic exposure studies (i.e., covering a major part of the life-
time of the species) on which to base conclusions.
Another subject of active investigation concerning the effects of
ozone is related to the mechanisms of defense against inhaled micro-
organisms. It has been shown that exposure of a few hours results in a
marked increase in the susceptibility of animals to controlled doses of
infectious organisms introduced into the lung. In fact, this criterion
of an effect is the most sensitive of any that nave been reported, with
significantly increased susceptibility of mice to one microorganism
occurring after exposure to an ozone concentration as low as 0.08 ppm.
Other reports referring to different microorganisms or different species
suggest that somewhat higher concentrations are required, but clearly
this effect is noted at less than 1.0 ppm. Research in the mechanism of
8-84
-------
ozone's effectiveness in decreasing resistance to infectious agents
suggests an action on the numbers and viability of lung macrophages.
Aside from the obvious practical implication of these findings for
carefully planned epidemiologic studies on the incidence of lung
infection in human populations exposed to oxidant air pollution, they
have stimulated more basic research in the physiology and biochemistry
of lung macrophages that may have implications beyond the question of
oxidant toxicity.
Earlier toxicity studies had suggested that the hazard from repeated
ozone exposure might be reduced, inasmuch as animals became tolerant to
the acute pulmonary edematogenic action of ozone. However, more recent
studies, which demonstrate that tolerance to the ordinarily ozone-induced
increase in susceptibility to infectious microorganisms or to the effects
on respiratory mechanics does not develop, suggest that the tolerance
phenomenon would have little protective value with respect to repeated
exposure to ambient oxidant smog.
There are several reports of noteworthy extrapulmonary effects in
laboratory animals with concentrations of about 0.2 ppm. These include
reduced voluntary activity, chromosomal aberrations in circulating
lymphocytes of hamsters, increased neonatal mortality, and greater
incidence of jaw abnormalities in offspring of ozone-exposed mice. The
mechanisms of these reported effects and whether they are due to direct
actions of absorbed ozone, some secondary reaction product, or secondary
responses to the stress of local actions in the lung are largely unknown.
However, reported analogous effects in humans exposed to ozone, such as
8-85
-------
changes in visual acuity and headache (possibly related to the reduced
activity in animals) and minor chromosomal abnormalities in circulating
lymphocytes, require that these extrapulmonary effects be considered in
the evaluation of the hazard of ozone exposure. Furthermore, the
chromosomal aberrations in hamsters and the reports of mutagenic activity
of ozone in a variety of microorganisms, tissue cultures, plants, and
insects raise the questions of the possibility of a genetic or carci-
nogenic hazard of this gas. Indeed, earlier studies at higher concen-
trations of ozone or mixtures of ozone with hydrocarbons have suggested
a tumorigenic action in the lungs of mice. Although present evidence
does not justify a definitive conclusion that exposure to ozone implies
a mutagenic or carcinogenic hazard, prudence requires that this possibility
should not be dismissed until it has been definitively tested experimentally
and epidemiologically.
The possibility of interactions of ozone with other environmental
stresses has received relatively little recent attention. Two exceptions
are noteworthy, however: reports of increased susceptibility to some of
the actions of ozone in animals that are deficient in vitamin E or the
converse (protection conferred by administration of vitamin E) and
observations that exposure to ozone at less than 1.0 ppm reduces activity
of the cytochrome P-450 mixed-function oxidase activity of lungs.
Although the implications of these observations are not yet clear, they
remind us that nutritional variations or exposure to foreign chemicals
that are metabolized by lung mixed-function oxidases may provide bases
for unanticipated qualitative or quantitative effects associated with
oxidant exposures.
8-86
-------
On the basis of the foregoing discussion, it appears that, if
traditional criteria for hazard evaluation are applied to the toxicologic
data on experimental animals, there is little room for complacency re-
garding current ambient concentrations of ozone. Functional, biochemical,
and structural effects in both pulmonary and extrapulmonary systems have
been reported by numerous investigators at or near concentrations that
are at least occasionally achieved in some polluted urban centers.
Unfortunately, there are no adequate methods for extrapolating data to
obtain reliable quantitative estimates of population risk at environmental
concentrations near the standard, and there is no assurance that the risk
is zero.
8-87
-------
REFERENCES
1- Alder, M. G., and G. R. Hill. The kinetics and mechanism of hydroxide ion
catalyzed ozone decomposition in aqueous solution. J. Amer. Chem. Soc
72:1884-1886, 1950.
2. Alpert, S. M., D. E. Gardner, D. J. Hurst, T. R. Lewis, and D. L. Coffin.
Effects of exposure to ozone on defensive mechanisms of the lung. J.
Appl. Physiol. 31:247-252, 1971.
i -1
3. Alpert, S. M., and T. R. lewis. Ozone tolerance studies utilizing unilater
lung exposure. J. Appl. Physiol. 31:243-246, 1971.
4. Alpert, S. M., and T. R. lewis. Unilateral pulmonary functions study of
ozone toxicity in rabbits. Arch. Environ. Health 23:451-458, 1971.
5. Alpert, S. M., 8. B. Schwartz, S. D. lee, and T. R. lewis. Alveolar
protein accumulation: A sensitive indicator of low level oxidant
toxicity. Arch. Environ. Med. 128:69-73, 1971. (UNVERIFIED)
6. Amdur, M. 0. The effect of aerosols on the response to irritant gases, pp.
281-292. In C. N. Davies, Ed. Inhaled Particles and Vapours. Proceed
ings of an International Symposium organized by the British Occupation*
Hygiene Society, I960. New York: Pergamon Press, 1961.
7. Amdur, M. 0. The physiological response of guinea pigs to atmospheric
pollutants. Int. J. Air Water Pollut. 1:170-183, 1959.
. • ~ • f .- ,. ,••' ' .,--..
8. Atwal, 0. S., and T. Wilson. Parathyroid gland changes following ozone
inhalation. A morphologic study. Arch. Environ. Health 28:91-100,
1974.
9. Balchum, 0. J., J. S. O'Brien, and B. D. Goldstein. Ozone and unsatur-
ated fatty acids. Arch. Environ. Health 22:32-34, 1971.
8-88
-------
10. Bartlett, D., Jr., C. S. Faulkner, II, and K. Cook. Effect of chronic
ozone exposure on lung elasticity in young rats. J. Appl. Physiol.
37:92-96, 1974.
11. Bils, R. F. Ultrastructural alterations of alveolar tissue of mice. III.
^
Ozone. Arch. Environ. Health 20:468-480, 1970.
12. Bjorksten, J. Aging, primary mechanism. Gerontologia S:179-192, 1963.
13. Bjorksten, J., and F. Andrews. Chemical mechanisms underlying the
biological mechanisms of the aging process. J. Amer. Geriatr.
Soc. 12:627-631, 1964.
14. Bloch, W. N., Jr., T. R. Lewis, K. A. Busch, J. G. Orthoefer, and J. F.
Stara. Cardiovascular status of femal beagles exposed to air pollu-
tants. Arch. Environ. Health 24:342-353, 1972.
r f i
15. Boatman, E. S., and R. Frank. Morphologic and ultrastructural changes in
the lungs of animals during acute exposure to ozon$. Chest 65(Suppl.)
9S-18S, 1974.
16. Boatman, E. S., S. Sato, and R. Frank. Acute effects of ozone on cat
lungs. II. Structural. Amer. Rev. Resp. Dis. 110:157-169, 1974.
17. Bobb, G. A., and E. J. Fairchild. Neutrophil-to-lymphocyte ratio as
indicator of ozone exposure. Toxicol. Appl. Pharmacol. 11:558-564,
1967.
18. Boche, R. D., and J? J. Quilligan, Jr. Effect o£ synthetic smog on spontaneous
activity of mice. Science 131:1733-1734, 1960.
19. Booher, J., D. E. Rounds, C. Spier, and L. Wightman. A tissue culture model
for studying environmental pollutants. In Vitro 10:342, 1974. (abstract)
8-89
-------
20. Brinkman, R., and H. B. Lamberts. Ozone as & possible radiomimetic gas.
Nature 181:1202-1203, 1958.
21. Brinkman, R., H. B. Lamberts, and T. S. Veninga. Radiomimetic toxiclty
of ozonised air. Lancet 1:133-136, 1964.
22. Bruch, J., and H.-W. Schlipkoter. Veranderungen der Lungenalveolen bei
der Maus nach chronischer Exposition mit Ozon in niedriger Konzentra-
tion. Virchows. Arch. Abt. A Path. Anat. 358:355-368, 1973.
23. Buckley, R. D., J. D. Hackney, K. Clark, and C. POsin. Ozone and human
blood. Arch. Environ. Health 30:40-43, 1975.
24. Brunstetter, M.-A., J. A. Bardie, R. Sehiff, J. P. Lewis, and C. E. Cross.
The origin of pulmonary alveolar macrophages. Studies of stem cells
using the Es-2 marker of mice. Arch. Intern. Med. 127:1064-1068, 1971.
25. Buell, G. C. Summary of Immunochemical Studies of Ozone. AlHL - Report
No. 15. Berkeley: State of California Department of Public Health,
Division of Laboratories, Air and Industrial Hygiene Laboratory, 1961.
9 pp.
~ ~~ i i J J '
26. Buell, G. C., Y. Tokiwa, and P. K. Mueller. Potential crosslinking agents
in lung tissue. Formation ^ind isolation after in vivo exposure to
ozone. Arch. Environ. Health 10:213-219, 1965.
27. Campbell, Rf I., G." L".~ Clarke, L." 0." Emik, and R." Li' Plata. The atmospheti.
contaminant peroxyacetyl nitrate. Acute inhalation toxicity in mice.
Arch. Environ. Health 15:739-744, 1967. . .
28 c*,!.*. ;•' i.'. H.' T.' VoUoyama, and *.' 0.' Dickinson. Induction of pul.on-
ary edema and emphysema in cattle and goats with 3-tnethylindole.
Science 176:298-299, 1972.
8-90
-------
29. Castleman, W. L., D. L. Dungworth, and W. S. Tyler. Cytochemically detected
alterations of lung acid phosphatase reactivity following ozone exposure.
Lab. Invest. 29:310-319, 1973.
30. Castleman, W. L., D. L. Dungworth, and W. S. Tyler. Histochemically detected
enzymatic alterations in rat lung exposed to ozone. Exp. Mol,
Path. 19:402-421, 1973.
31. Chow, C. K., C. J. Dillard, and A. 1. Tappel. Glutathione peroxidase
system and lysozyme in rats exposed to ozone or nitrogen dioxide.
Environ. Res. 7:311-319, 1974.
32. Chow, C. K., and A. L. Tappel. Activities o£ pentose shunt and glycolytic
enzymes in lungs of ozone-exposed rats. Arch. Environ. Health 26:205-
208, 1973.
33. Chow, C. K., and A. L. Tappel. An enzymatic protective mechanism against
lipid peroxidation damage to lungs of ozone-exposed rats. Lipids
7:518-524, 1972. *
34. Christensen, E., and A. C. Giese. Changes in absorption spectra of nucleic
acids and their derivatives following exposure to ozone and ultraviolet
radiations. Arch. Biochem. Biophys. 51:208-216, 1954.
35. Coffin, D. L., and D. E. Gardner. Interaction of biological agents and
chemical air pollutants. Ann. Occup. Hyg. 15:219-234, 1972.
35. Coffin, D. 1., and E. J. Blommer. Alteration of the pathogenic role of strep-
tococci group C in mice conferred by previous exposure to ozone, pp. 54-
61. In I. H. Silver, Ed. Aerobiology. Proceedings of the Third Inter-
national Symposium held at the University of Sussex, England, 1969.
New York: Academic Press, 1970.
37_ Coffin, D. L., D. E. Gardner, R. S. Holzman, and F. J. Wolock. Influence
of ozone on pulmonary cells. Arch. Environ. Health 16:633-636, 1968.
3-91
-------
38. Coffin, D. L., E. J. Blommer, D. E. Gardner, and R. S. Holzman. Effect of
air pollution on alteration of susceptibility to pulmonary infections,
pp. 75-80. In Proceedings of the 3rd Annual Conference on Atmospheric
Contaminants in Confined Spaces. Dayton, Ohio: Wright-Patterson Air
Force Base, Aerospace Medical Research Laboratories, 1968.
39. Cortesi, R., and 0. S. Privett. Toxicity of fatty ozonides and peroxides.
Lipids 7:715-721, 1972.
40. Criegee, R. Course of ozonization of unsaturated compounds. Record Chem.
Progm. 18:111-120, 1957.
41. Cronin, S. R., and S. N. Giri. Effects of pulmonary irritants on DNA,
ATPase activity, and histamine on rat lung. Proc. Soc. Exp. Biol.
Med. 146:120-125, 1974.
42. Cross, C. E. The granular type II pneumonocyte and lung antioxidant defense.
Ann. Intern. Med. 80:409-411, 1974. (
43. Davis, I. Microbiologic Studies with Ozone. Mutagenesis of Ozone for
Escherichia coli. Brooks Air Force Base, Texas: School of Aerospace
Medicine. USAF Aerospace Medical Center (ATC), June 1961. 9 pp.
44. de Koning, H., and Z. Jegier. Effect of ozone on pyridine nucleotide
reduction and phosphorylation of Euglena gracilis. Arch. Environ.
Health 18:913-916, 1969.
45. DeLucia, A. J., P. M. Ho^ue, M. G. Mustafa, and C. E. Cross. Ozone inter-
action with rodent lung: Effect on sulfhydryls and sulfhydryl-containir
enzyme activities. J. Lab. Clin. Med. 80:559-566, 1972.
46. DeLucia, A. J. , M. G. Mustafa, M. 2. Hussain, and C. E. Cross. Ozone inter-
action with rodent lung. III. Oxidation of reduced glutathione and
formation of mixed disulfides between protein and nonprotein sulfhydryls
J. Clin. Invest. 55:794-802, 1975.
8-92
-------
47. Dillard, C. J., and A. L. Tappel. Fluorescent products from reaction o£
peroxidizing polyunsaturated fatty acids with phosphatidyl ethanolamine
and phenylalanine. Lipids 8:183-189, 1973.
48. Dillard, C. J., M. Urribarri, K. Reddy, B. Fletcher, S. Taylor, B. de Lumen,
S. Langberg, and A. L. Tappel. Increased lysosomal enzymes in lungs
of ozone-exposed rats. Arch. Environ. Health 25:426-431, 1972.
49_ Dixon, J. R., and J. T. Mountain. Role of histamine and related substances
in development of tolerance to edemagenic gases. Toxicol. Appl. Pharmacol.
7:756-766, 1965.
50. Dixon, J. R., W. D. Wagner, T. D. Martin, R. G. Keenan, and H. E. Stokinger.
Metal shifts as early indicators of response from low-grade pulmonary
irriation. Toxicol. Appl. Pharmacol. 9:225-233, 1966.
51. Dowell, A. R., L. A. Lohrbauer, D. Hurst, and S. D. Lee. Rabbit alveolar
macrophage damage caused by in vivo ozone inhalation. Arch. Environ.
Health 21:121-128, 1970.
52. Easton, R. E. and S. D. Murphy. Experimental ozone preexposure and
histamine. Effect on the acute toxicity and respiratory function
effects of histamine in guinea pigs. Arch. Environ. Health 15:160-166,
1967.
53. Eglite, M. A contribution to the hygienic assessment of atmospheric ozone.
Hyg. Sanit. 33(1-3):18-23, 1968.
54, Ehrlich, R. Effect of nitrogen dioxide on resistance to respiratory
infection. Bact. Rev. 30:604-614, 1966.
55. Emik, 0., and R. L. Plata. Depression of running activity in mice by
exposure to polluted air. Arch. Environ. Health 18:574-579, 1969.
8-93
-------
56. Evans, M. J. , W. Mayr, R. F. Bils, and C. G. Loosli. Effects of ozone
on cell renewal in pulmonary alveoli of aging mice. Arch. Environ.
Health 22:450-453, 1971.
57. Fairchild, E. J., II. Neurohumoral factors in injury from inhaled irritants
Arch. Environ. Health 6:79-86, 1963.
Delete 58--same as 57.
59. Fairchild, E. J., II. Tolerance mechanisms. Determinants of lung responses
to injurious agents. Arch. Environ. Health 14:111-125, 1967.
60. Fairchild, E. J., G. A. Bobb, and G. E. Thompson. Enhanced toxicity of
a respiratory irritant (ozone) by pertussis sensitization. Fed.
Proc. 25:692, 1966. (abstract)
61. Fairchild, E. J., II, S. L. Graham, M. Kite, R. Killens, and L. D. Scheel.
I 0-1 f
Changes in thyroid Iiji activity in ozone-tolerant and ozone-susceptible
rats. Toxicol. Appl. Pharmacol. 6:607-613, 1964.
62. Fairchild, E. J., S. D. Murphy, and H. E. Stokinger. Protection by sulfur
compounds against the air pollutants ozone and nitrogen dioxide.
Science 130:861-862, 1959.
63. Falk, H. L., P. Kotin, W. Rowlette. The response of mucus-sec ret ing
epithelium and mucus to irritants. Ann. N. Y. Acad. Sci. 106:583-
608, 1963.
••>-»-• f t f t r • / r > t , . * » • ^
64. Fetner, R. H. Chromosome breakage in Vicia faba by ozone. Nature 181:
504-505, 1958.
65. Fetner, R. H. Ozone-induced chromosome breakage in human cell cultures.
Nature 194:793-794, 1962.
8-94
-------
66. Fetner, R. H. Mitotic Inhibition Induced in Grasshopper Neuroblasts
by Exposure to Ozone. Technical Documentary Report SAM-TDR 63-39.
Brooks Air Force Base, Texas: USAF School of Aerospace Medicine,
Aerospace Medical Division (AFSC), June 1963.
Delete 67 (omitted)
68. Fletcher, B. L., and A. L. Tappel. Protective effects of dietary alpha-
tocopherol in rats exposed to toxic levels of ozone and nitrogen
dioxide. Environ. Res. 6:165-175, 1973.
69 0 Frank, R., J. P. Flesch, and J. D. Brain. Effect of ozone on elastic
behavior of excised lungs of dogs. Environ. Res. 4:343-354, 1971.
70. Frank, N. R. Pulmonary functional changes: Animal studies, pp. 185-204.
In National Research Council of Canada. NRC Associate Committee on
Scientific Criteria for Environmental Quality. Report No. 12.
Subcommittee on Air. Photochemical Air Pollution:* Formation, Trans-
port and Effects. Ottawa: National Research Council of Canada, 1975.
71. Frank, N. R., J. D. Brain, and D. E. Sherry. Unilateral lung exposure to
ozone. Fed. Proc. 27:279, 1968. (abstract)
72. Frank, N. R., J. D. Brain, and D. E. Sherry. Unilateral tolerance and
altered elastic behavior in rabbits. Araer. Ind. Hyg. Assoc. J.
(Abstracts) 31:31, 1970.
73. Freebaim, H. T. Reversal of inhibitatory effects of ozone on oxygen
uptake of mitochondria. Science 126:303-304, 1957.
74. Freeman, G., L. T. Juhos, N. J. Furiosi, R. Mussendett, R. J. Stephens,
and M. J. Evans. Pathology of pulmonary disease from exposure to
interdependent ambient gases (nitrogen dioxide and ozone). Arch.
Environ. Health 29:203-210, 1974.
8-95
-------
75. Freeman, G., R. J. Stephens, D. I. Coffin, and J. F. Stara. Changes in
dogs' lungs after long-term exposure to ozone. Light and electron
microscopy. Arch. Environ. Health 26:209-216, 1973.
76. Gardner, D. E., J. w. Illing, F. J. Miller, and D. L. Coffin. The effect
of ozone on pentobarbital sleeping time in mice. Res. Commun. Chem.
Path. Pharmacol. 9:689-699, 1974.
77. Gardner, D. E., T. R. Lewis, S. M. Alperfc, D. J. Hurst, and D. L. Coffin.
The role of tolerance in pulmonary defense mechanisms. Arch. Environ.
Health 25:432-438, 1972.
78. Gardner, D. E., E. A. Pfitzer, R. T. Christian, and D. L. Coffin. Loss
of protective factor for alveolar macrophages when exposed to ozone.
Arch. Intern. Med. 127:1078-1084, 1971.
79. Giese, A. C., H. L. Leighton, and R. Bailey. Changes in the absorption
spectra of proteins and representative amino acids induced by
ultraviolet radiations and ozone. Arch. Biochem.(Biophys. 40:71-
84, 1952.
80. Glende, E. A., Jr. Carbon tetrachloride-induced protection against carbon
tetrachloride toxicity. The role of the liver microsomal drug-
metabolizing system. Biochem. Pharmacol. 21:1697-1702, 1972.
81- Golde, D. W., T. N. Finley, and M. J. Cline. The pulmonary macrophage in
acute leukemia. N. Engl. J. Med. 290:875-878, 1974.
82. Goldstein, B. D. Hydrogen peroxide in erythrocytes. Detection in rats
and mice inhaling ozone. Arch. Environ. Health 26:279-280, 1973.
83. Goldstein, B. D. Production of paroxysmal nocturnal haemoglobinuria-
like red cells by reducing the oxidizing agents. Brit. J. Haematol.
26:49-58, 1974.
84. Goldstein, B. D., and 0. J. Balchum. Effect of ozone on lipid peroxidation
in the red blood cell. Proc. Soc. Exp. Biol. Med. 126:356-358, 1967.
8-96
-------
85. Goldstein, B. D., and 0. J. Balchum. Modification of the response of
rats to lethal levels of ozone by enzyme-indueing agents. Toxicol.
Appl. Pharmacol. 27:330-335, 1974.
86. Goldstein, B. D., 0. J. Balchum, H. B. Demopoulos, and P. S. Duke.
Electron paramagnetic resonance spectroscopy. Arch. Environ. Health
17:46-49, 1968.
87. Goldstein, B. D., R. D. Buckley, R. Cardenas, and 0. J. Balchum.
Ozone and vitamin E. Science 169:605-606, 1970.
88. Goldstein, B. D., L. Y. Lai, and R. Cuzzi-Spada. Potentiation of comple-
ment-dependent membrane damage by ozone. Arch. Environ. Health 28:
40-41, 1974.
89. Goldstein, B. D., M. R. Levine, R. Cuzzi-Spada, R. Cardenas, R. D. Buckley,
and 0. J. Balchum. £-Aminobenzoic acid as a protective agent in ozone
toxicity. Arch. Environ. Health 24:243-247, 1972.
-/
90. Goldstein, B. D. , C. Lodi, C. Collinson, and 0. J. Balqhum. Ozone and
lipid peroxidation. Arch. Environ. Health 18:631-635, 1969.
91. Goldstein, B. D., And E. M. McDonagh. Effect of ozone on cell membra,ne
protein fluorescence. 1. In vitro studies utilizing the red cell
membrane. Environ. Res. 9:179-186, 1975.
92. Goldstein, B. D., B. Pearson, C. Lodi, R. D. Buckley, and 0. J. Balchum.
The effect of ozone on mouse blood in vivo. Arch. Environ. Health
16:648-650, 1968.
93. Goldstein, B. D., S. Solomon, B. S. Pasternack, and D. R. Bickers.
Decrease in rabbit lung microsomal cytochrome P-450 levels following
ozone exposure. Res. Commun. Chem. Path. Pharmacol. 10:759-762, 1975.
94. Goldstein, E., M. C. Eagle, and P. D. Hoeprich. Influence of ozone on
pulmonary defense mechanisms of silicotic mice. Arch. Environ.
Health 24:444-448, 1972.
i
8-97
-------
95. Goldstein, E., W. S. Tyler, P. D. Hoeprich, and C. Eagle. Adverse influen(
of ozone on pulmonary bactericidal activity of lung. Nature 229:262-
263, 1971.
96. Goldstein, E., W. S. Tyler, P. D. Hoeprich- and C. Eagle. Ozone and
the antibacterial defence mechanisms of the murine lung. Arch.
Intern. Med. 127:1099-1102, 1971.
97. Goldstein, E., D. Warshauer, W. Lippert, and B. Tarkington. Ozone and
nitrogen dioxide exposure. Murine pulmonary defense mechanisms.
Arch. Environ. Health 28:85-90, 1974.
if - - •
98. Gregory, A. R., L. A. Ripperton, and B. Miller. Effect of neonatal
thymectomy on the development of ozone tolerance in mice. Amer.
Ind. Hyg. Assoc. J. 28:278-282, 1967.
99. Hackney, J. D., W. S. Linn, D. C. Law, S. K. Karuza, H. Greenberg, R. D.
Buckley, and E. E. Pedersen. Experimental studies on human health
effects of air pollutants. III. Two-hour exposure to ozone alone and
\
in combination with other pollutant gases. Arch. Environ. Health
30:385-390, 1975.
100. Hamelin, C., and Y. S, Chung. Characterization of mucoid mutants of
Escherichia coli K-12 isolated after exposure to ozone. J. Bacteriol.
122:19-24, 1975.
101. Hamelin, C., and Y. S. Chung. Resistance Tl'ozone ehez Escherichia coll
II. Relations avec certains mecanismes de reparation de 1'ADN.
Molec. Gen. Genet. 129:177-184, 1974.
102. Hathaway, J. A., and R. E. Terrill. Metabolic effects of chronic ozone
exposure on rats. Ind. Hyg. J. 23:392-394, 1962.
103. Hattori, K., N. Kato, M. Kinoshita, S. Kinoshita, and T. Sunada. Protective
effect of ozone in mice against whole-body x-irradiation. Nature 198:
1220, 1963.
8-98
-------
104. Henschler, D., E. Hahn, H. Heymann, and H. Wunder. Mechanismus einer
Toleranzsteigerung bei wiederholter Einatmung von Lungenodem erzeugenden
Gasen. Nauny Schmiedegerg Arch. Exp. Path. 249:343-356, 1964.
105. Hinners, R. G. Engineering the chronic exposure of animals to laboratory pro-
duced automobile exhaust. J7 Air Pollut. Contr. Assoc. 12:527-530, 1962.
106. Hinners, R. G. Laboratory produced automobile exhaust facility. Biomed.
Sci. Instrum. 1:53-58, 1963.
107. Holzman, R. S., D. E. Gardner, and D. L. Coffin. In vivo inactivation of
lysozyme by ozone. J. Bacteriol. 96:1562-1566, 1968.
108. Huber, G. 1., R. J. Mason, M. LaForce, 1. J. Spencer, D. E. Gardner, and
D. L. Coffin. Alterations in the lung following administration of
ozone. Arch. Intern. Med. 128:81-87, 1971.
109. Hueter, F. G., G. L. Contner, K. A. Busch, and R. G. Hinners. Biological
effects of atmospheres contaminated by auto exhaust. Arch. Environ.
Health 12:553-560, 1966. '
110. Hurst, D. J., and D. L. Coffin. Ozone effect on lysosomal hydrolases of
alveolar macrophages in vitro. Arch. Intern. Med. 127:1059-1063, 1971.
111. Hurst, D. J., D. E. Gardner, and D. 1. Coffin. Effect of ozone on acid
hydolysis of the pulmonary alveolar macrophage. J. • Reticuloendothel.
Soc. 8:288-300, 1970.
112. Hussain, M. Z., M. G. Mustafa, R. B. Rucker, and C. E. Cross. Lung
collagen synthesis as stimulated by low level ozone exposure.
Clin. Res. 23:138A, 1975. (abstract)
113. Jaffe, L. S. Photochemical ait pollutants and their effects on men and
animals. II. Adverse effects. Arch. Environ. Health 16:241-255, 1968.
114. Jegier, 2. L'ozone en tant que polluant atmospherique. Can. J. Public
Health 64:161-166, 1973.
8-99
-------
115. Johnson, B. L. , J. G. Orthoefer, T. R. Lewis, and C. Xintaras. The effect
of ozone on brain function. Presented at the American Medical Associ-
ation Air Pollution Medical Research Conference, December 5-6, 1974.
San Francisco, California.
116. Khandwala, A., and J. B. L. Gee. Linoleic acid hydroperoxide: Impaired
bacterial uptake by alveolar macrophages, a mechanism of oxidant
lung injury. Science 182:1364-1365, 1973.
117. Deleted
118. Kimbrough, R. D., and T. B. Gaines. Toxicity of paraquat to rats and its
effect on rat lung. Toxicol. Appl. Pharmacol. 17:679-690, 1970.
119. Koiwai, A., and T. Kisaki. Mixed function oxidase inhibitors protect
plants from ozone injury. Agric. Biol. Chem. 37:2449-2450, 1973.
(
120. Konigsberg, A. S., and C. H. Bachman. Ozonized atmospheric and gross
motor activity of rats. Int. J. Biometeorol. 14:261-266, 1970.
121. Kotin, P., and H. I. Falk. II. The experimental induction of pulmonary
tumors in strain-A mice after their exposure to atmosphere of ozonized
gasoline. Cancer 9:910-917, 1956.
122. Kotin, P., H. L. Falk, and C. J. MeCammOrt. III. The experimental induction
of pulmonary tumors and changes in respiratory epithelium in C57BL mice
following exposure to ozonized gasoline. Cancer 11:473-481, 1958.
123. Kotin, P., and M. Thomas. Effect of air contaminants on reproduction and
offspring survival in mice. A.M.A. Arch. Ind. Health 16:411-413, 1957.
124. Lagerwerff, J. J. Prolonged ozone inhalation and its erfects on visual
parameters. Aerospace Med. 34:479-486, 1963.
8-100
-------
125. Lewis, T. R., P. G. Hueter, and K. A. Busch. Irradiated automobile exhaust:
Its effects on the reproduction of mice. Arch. Environ. Health 15:26-
35, 1967.
126. MacLean, S. A., A. C. Longwell, and W. J. Blogoslawski. Effects of
ozone-treated sea water on the spawned, fertilized, meiotic, and
cleaving eggs of the commercial American oyster. Mutat. Res.
21:283-285, 1973.
127. Malley, A., 1. Baecher, G. Crossley, and D. Burger. Allergen-reagin-mediated
histamine release reactions. Int. Arch. Allergy Appl. Immunol. 44:122-
139, 1973.
128. Matsumura., Y., K. Mizuno, T. Miyamoto, T. Suzuki, and Y. Oshima. The
effects of ozone, nitrogen dioxide, and sulfur dioxide on experi-
mentally induced allergic respiratory disorder in guinea pigs. IV.
Effects on respiratory sensitivity to inhaled acetylcholine. Amer.
\
Rev. Resp. Dis. 105:262-267, 1972.
129- Matzen, R. N. Effect of vitamin C and hydrocortisone on the pulmonary
edema produced by ozone in mice. J. Appl. Physiol. 11:105-109, 1957.
i '
130. Mendenhall, R. M., and H. E. Stokinger. Films from lung washings as a
mechanism model for lung injury by ozone. J. Appl. Physiol. 17:28-
32, 1962.
131. Mendenhall, R. M., and H. E. Stokinger. Tolerance and cross-tolerance
development to atmospheric pollutants ketene and ozone. J. Appl.
Physiol. 14:923-926, 1959.
132. Mengel, C. E., H. E. Kann, Jr., A. M. Lewis, and B. Horton. Mechanisms of j.n
vivo hemolysis induced by hyperoxia. Aerospace Med. 35:857-860, 1964.
8-101
-------
133. Menzel, D. B. Oxidation of biologically active reducing substances by
ozone. Arch. Environ. Health 23:149-153, 1971.
134. Menzel, D. B. Toxicity of ozone, oxygen, and radiation. Ann. Rev. Pharmacoi.
10:379-394, 1970.
135. Menzel, D. B., J. N. Roehm, and S. D. Lee. Vitamin E: The biological and
environmental antioxidant. Agric. Food Chem. 20:481-486, 1972.
136. Menzel, D. B., R. J. Slaughter, A. M. Bryant, and H. 0. Jauregui. Prevention ol
ozonide-induced Heinz bodies in human erythrocytes by vitamin E. Arch.
Environ. Health 30:234-236, 1975.
137. Menzel, D. B., R. J. Slaughter, A. M. Bryant, and H.~ 0. Jauregui. Heinz bodies
formed in erythrocytes by fatty acid ozonides and ozone. Arch. Environ.
Health 30:296-301, 1975.
138. Metfz, T. , H. A. Bender, H. D. Kerr, and T. J. Kulle. Observations of
aberrations in chromosomes of lymphocytes from human subjects exposed
to ozone at a concentration of 0.5 ppm for 6 and 10 hours. Mutat.
Res. 31:299-302, 1975.
139. Miller, S., and R. Ehrlieh. Susceptibility to respiratory infections of
animals exposed to ozone. Susceptibility to Klebsulla pneumoniae.
J. Infect. Dis. 103:145-149, 1958.
140. Mittler, S., M. King, and B. Burkhardt. Toxicity of ozone. III. Chronic
toxicity. Arch. Ind. Health 15:191-197, 1957.
141. Mittman, C., T. Barbela, and J. Lieberman. Antitrypsin deficiency and abnormal
protease inhibitor phenotypes. Arch. Environ. Health 27:201-207, 1973.
142. Mountain, J. T. Detecting hypersusceptibility to toxic substances. An
appraisal of simple blood tests. Arch. Environ. Health 6:357-365, 1963.
8-102
-------
143. Mudd, J. B. Responses of enzyme systems to air pollutants. Arch. Environ.
Health 10:201-206, 1965.
144. Mudd, J. R., R. Leavitt, A. Ongun, and T. T. McManus. Reaction of ozone with
amino acids and proteins. Atmos. Environ. 3:669-681, 1969.
145, Mudd, J. B., P. Leh, and T. T. McManus. Reaction of ozone with nicotinamide
and its derivatives. Arch. Biochem. Biophys. 161:408-419, 1974.
146. Mueller, P. K. , and M. Hitchcock. Air quality criteria—toxicological
appraisal for oxidants, nitrogen oxides and hydrocarbons. J. Air
Pollut. Control Assoc. 19:670-676, 1969.
147. Murphy, S. D. A review of effects on animals of exposure to auto exhaust and
some of its components, jf Air Pollut. Contr. Assoc. 14:303-308, 1964.
148. Murphy, S. D., H. V. Davis, and V. L. Zaratzian. Biochemical effects in
rats from irritation air contaminants. Toxicol. Appl. Pharmacol.
6:520-528, 1964.
149. Murphy, S."t>r, D." A." Klingshirn, and C.' E." Ulrich. Respiratory response of
guinea pigs during acrolein inhalation and its modification by drugs.
J. Pharmacol. Exp. Therap. 141:79-83, 1963.
150. Murphy, S. D. , J. ft. Leng, C. E. Ulrich, and H. V. Davis. Effects on animals
of exposure to auto exhaut. Arch. Environ. Health 7:60-70, 1963.
151. Murphy, S. D., and R. Prindle. Effects of automotive exhaust on pulmonary
function of guinea pigs. Presented a A.M.A. Symposium on Air Pollution
and Pulmonary Disease, Los Angeles, Calif., November 25, 1962.
Murphy, S. D. , and C. E. Ulrich. Multi-animal test system for measuring
effects of irritant gases and vapors on respiratory function of guinea
pigs. Amer. Ind. Hyg. Assoc. J. 25:2.8-36, 1964.
8-103
-------
153. Murphy, S. D. , C. R. Ulrich, S. H. Frankowitz, and C. Xintaris. Altered
function in animals inhaling low concentrations of ozone and nitrogen
dioxide. Amer. Ind. Hyg. Assoc. J. 25:246-253, 1964.
154. Deleted
155. Murray, R. V., and D. P. Higley. Ozonides from the photoxidation of
diazo compounds in the presence of 180 labeled aldehydes and 18Q .
J. Amer. Chem. Soc. 95:7886-7888; 1973.
156. Mustafa, M. G. Augmentation of mitochrondial oxidative metabolism in
lung tissue during recovery of animals from acute ozone exposure.
Arch. Biochem. Biophys. 165:531-538, 1974.
157. Mustafa, M. G. , S. M. Macres, B. K. Tarkington, C. K. Chow, and M. Z.
(
Hussein. Lung superoxide dismutase (SOD): Stimulation by low-
level ozone exposure. Clin. Res. 23:138A, 1975. (abstract)
158. Mustafa, M. G. , A. J. DeLucia, G. K. York, C. Arth, and C. E. Cross.
Ozone interaction with rodent lung. II. Effects on oxygen con-
sumption of mitochondria. J. Lab. Clin. Med. 82:357-365, 1973.
159. Mustafa, M. G. Influence of dietary vitamin E on lung cellular sensitivity
to ozone in rats. Nutr. Rep. Int. 11:473-476, 1975.
160. Nakajima, T. , S. KusumOto, Y. Tstlbota, E. YonekaWa, R. Yoshida, K. Motomiya,
K. Ito, G. Ide, and H. Otsu. Histopathological changes in the respir-
atory organs of mice exposure to photochemical oxidants and automobile
exhaust gas. Osaka Prefectural Public Health Research Institute,
Research Reports, Labor Hygiene Series, No. 10, September 1972, pp.
35-42. (in Japanese)
8-104
-------
161. Nasr, A. N. M., B. D. Dinman, and I. A. Bernstein. II. Effect o£ ozone
inhalation on nadide phosphate levels in tracheal mucosa. Arch.
Environ. Health 22:545-550, 1971.
162. North Atlantic Treaty Organization. Committee on the Challenges of Modern
Society. Air Quality Criteria for Photochemical Oxidants and Related
Hydrocarbons. Brussels, Belgium: North Atlantic Treaty Organization,
1974.
163. Pace, D. M., P. A. Landolt, and B. T. Aftonomos. Effects of ozone on cells
in vitro. Arch. Environ. Health 18:165-170, 1969.
164. Pagnotto, L. D., and S. S. Epstein. Protection by antioxidants against
ozone toxicity in mice. Experientia 25:703, 1969.
165. Palmer, M. S., R. W. Exley, and D. L. Coffin. Influence of pollutant
gases on benzpyrene hydroxylase activity. Arch. Environ. Health
25:439-442, 1972.
i
166. Palmer, M. S., D. H. Swanson, and D. L. Coffin. Effect of ozone on
benzpyrene hydroxylase activity in the Syrian golden hamster.
Cancer Res. 31:730-733, 1971.
167. P'an, A. Y. S., and 2. Jegier. The effect of sulfur dioxide and ozone
on acetylcholinesterase. Arch. Environ. Health 21:498-501, 1970.
168. p'an, A. Y. S., and 2. Jegier. The setum trypsin inhibitor capacity during
ozone exposure. Arch. Environ. Health 23:215-219, 1971.
169. P'an, A. Y. S., and 2. Jegier. Trypsin protein esterase in relation to
ozone-induced vascular damage. Arch. Environ. Health 24:233-236, 1972.
170. Penha, P. D., and S. Werthamer. Pulmonary lesions induced by long-term
exposure to ozone. II. Ultrastructure observations of proliferative
and regressive lesions. Arch. Environ. Health 29:282-289, 1974.
8-105
-------
171. Perchorowicz, J. T., and I. P. Ting. Ozone effects on plant cell permea-
bility. Amer. J. Bot. 61:787-793, 1974.
172. Peterson, D. C., and H. L. Andrews. The role of 03 in radiation avoidance
in the mouse. Radiat. Res. 19:331-336, 1963.
173. Piper, P., and J. Vane. The release of prostaglandins from lung and
other tissues. Ann. N. Y. Acad. Sci. 180:363-385, 1971.
!74. Plopper, C. G., D. L. Dungworth, and W. S. Tyler. Morphometric evaluation
of pulmonary lesions in rats exposed to ozone. Amer. J. Path. 71:
395-408, 1973.
175. Plopper, C. G., D. 1. Dungworth, and W. S. Tyler. Pulmonary lesions in
rats exposed to ozone. A correlated light and electron microscopic
study. Amer. J. Path. 71:375-394, 1973.
176. Plopper, C. G., D. L. Dungworth, and W. S. Tyler. Ultrastructure of pul-
monary alveolar macrophages in situ in lungs from rats exposed to
ozone. Amer. Rev. Resp. Dis. 108:632-638, 1973.
177. Prat, R., Cl. Nofre, and A. Cier. Effets de 1'hypochlorite de sodium,
de 1'ozone et des radiations ionisantes sur les constituants
pyrimidiques d'escherichia coli. Ann. Inst. Pasteur 114:595-607,
1968.
178. Previero, A., E. Scoffone, P. Pajetta, and C. A. Benassi. Comportamento
degli amminoacidi di fronte all1 ozono. Gazz. Chim. Ital. 93:841-848,
1963.
179. Previero, A., A. Signor, and S. Bezzi. Tryptophan modification in polypeptide
chains. Nature 204:687-688, 1964.
180. Prinsloo, H. Effect of exposure to quartz dust rn vivo on pentose cycle
activity in guinea pig lung. Environ. Res. 6:68-76, 1973.
8-106
-------
181. Purvis, M. R., S. Milter, and R. Ehrlich. Effect of atmospheric pollutants
on susceptibility to respiratory infection. I, Effect of ozone.
J. Infect. Dis. 109:238-242, 1961.
182. Quilligan, Jf J., Jr., R.~ D? Boehe, H." L7 Falk, and p? Kotin. The toxicity of
ozone for young chicks. A7M7A7 Arch. Ind. Health 18:16-22, 1958.
183. Richmond, V. L. In vitro hydrolas and phagocytic activities of alveolar
macrophages. J. Lab. Clin. Med. 83:757-767, 1974.
184. Roehm, J. H., J. G. Hadley, and D. 6. Menzel. Antioxidants vs lung disease.
Arch. Intern. Hed. 128:88-93, 1971.
185. Roehm, J. N., J. G. Hadley, and D. B. Menzel. Oxidation of unsaturated
fatty acids by ozone and nitrogen dioxide. A common mechanism of
action. Arch. Environ. Health 23:142-148, 1971.
186. Roth, R. P., and M. F. Tansy. Effects of gaseous air pollutants on gastric
secreto-motor activities in the rat. J. Air Pollut. Control Assoc.
22:706-709, 1972. '
187. Sachsemnaier, W., W. Siebs, and T.-A. Tan. Wirkung von Ozon auf
Mauseaseites-tumorzellen und auf Huhnerfibroblasten in der
Gewebekultur. Z. Krebsforsch. 67:113-126, 1965.
188. Said, S. I. The lung in relation, to vasoactive hormones. Fed. £roc. 32":
1972-1976, 1973.
189. Sapse, A. T., B. Bonavida, w. Stone, Jr., and E. E. Sercarz. Human
tear lysozyme. III. Preliminary study on lysozyme levels in
subjects with somg eye irritation. Amer. J. Ophthalmol. 66:76-
80, 1968.
190. Schacter, B. A., H. S. Marver, and U. A. Meyer. Hemoprotein catabolism
during stimulation of microsomal lipid peroxidation. Biochim. Biophys.
Acta 279:221-227, 1972.
8-107
-------
191. Scheel, L. D., 0. J. Dobrogorski, J. T. Mountain, J. L. Svirbely, and
H. E. Stokinger. Physiologic, biochemical, immunologic and pathologic
changes following ozone exposure. J. Appl. Physiol. 14:67-80, 1959.
192 Schlipkoter, H.-W., and J. Bruch. Funktionelle und morphologisehe
Veranderung bei Ozonexposition. Zbl. Bakt. Hyg., I. Abt. Orig. B
156:486-499, 1973.
193. Scott, D. B. M., and E. C. Lesher. Effect of ozone on survival and
permeability of Escherichia coll. J. Bacteriol. 85:567-576, 1963.
194. Shoaf, A. R., R. C. Allen, and R. H. Steele. Electronic excitation state
generation in mammalian systems: Mechanism-role-pathology. Second Annual
Meeting, American Society for Photobiology, July 22-26, 1974. University
of British Columbia, Vancouver, B.C.
195. Skillen, R. G., C. H. Thiertes, J. Cangelosi, and L. Strain. Brain
5-hydroxytryptamine in ozone-exposed rats. Proc. Soc. Exp. Biol.
Med. 108:121-122, 1961.
196. Skillen, R. G., C. H. Thienes, J. Cangelosi, and 1. Strain. Lung 5-
hydroxy-tryptamine and ozone induced pulmonary edema in rats.
Proc. Soc. Exp. Biol. Med. 107:178-180, 1961.
197. Stephens, R. J., M. F. Sloan, M. J. Evans, and G. Freeman. Alveolar
type 1 cell response to exposure to 0.5 ppm Cv, for short periods.
Exp. Molec. Path. 20:11-23, 1974.
- ,,- - ,- - ----- , •
198. Stephens, R. J., M. F. SloAn, M. J. Evans, and G. Freeman. Early response
of lung to low levels of ozone. Amer. J. Path. 74:31-58, 1974.
199. Stokinger, H. E. Effects of air pollution on animal, pp. 282-334. In
A. C. Stern, Ed. Air Pollution. Vol. 1. New York: Academic Press,
1962.
200. Stokinger, H. E. Ozone toxicity. A. M. A. Arch. Ind. Hyg. Occup. Med. 9:
366-383, 1954.
8-108
-------
201. Stokinger, H. E. Ozone toxicology. A review of research and industrial
experience: 1954-1964. Arch. Environ. Health 10:719-731, 1965.
202. Stokinger, H. E., and D. 1. Coffin. Biologic effects of air pollutants, pp.
445-544. In A. C. Stern, Ed. Air Pollution. Vol. 1. Air Pollution
and Its Effects. (2nd ed.) New York: Academic Press, 1968.
203. Stokinger, H. E., and I. D. Scheel. Ozone toxicity. Immunoehemical and
tolerance-producing aspects. Arch. Environ. Health 4:327-334, 1962.
204. Stokinger, H," ET, W? D? Wagner, and 0? J.~ Dobrogorski. Ozone toxicity studies.
IIl7 Chronic injury to lungs of animals following exposure at a low level.
A."fo.A. Arch. Ind. Health 16;514-522, 1957.
205. Sugihara, T., and C. J. Martin. Simulation of lung tissue properties in
•
age and irreversible obstructive syndromes using an aldehyde. J. Clin.
Invest. 56:23-29, 1975.
206. Tan, W. C., R. Cortesi, and 0. S. Privett. Lipid peroxide and lung
prostaglandins. Arch. Environ. Health 28:82-84, 1974.
207. Teige, B., T. T. McManus, and J. B. Mudd. Reaction of ozone with phosphathyl-
choline kiposomes and the lytic effect of products on red blood cells.
Chem. Phys. Lipids 12:153-171, 1974.
208. Thompson, G. E. Cardiovascular considerations of rat pulmonary edema.
Milit. Med. 136:50-56, 1971. ^
209. Thompson, G. E. Experimental acute pulmonary edema in the rat. Effect
of Bordetella pertussis vaccine on ozone mortality. Arch. Environ.
Health 23:154-160, 1971.
210. Thomas, H. V., P. K. Mueller, and R. L. Lyman. Lipoperoxidation of lung lipids
in rats exposed to nitrogen dioxide. Science 159:533-534, 1968.
8-109
-------
211. Trams, E. G., C. J. Lauter, E. A. B. Brown, and 0. Young. Cerebral
cortical metabolism after chronic exposure to ozone. Arch. Environ.
Health 24:153-159, 1972.
212. U. S. Department o£ Health, Education, and Welfare. Public Health Service.
Environmental Health Service. Toxicological Appraisal of photochemical
oxidants, pp. 8-1--8-44. In Air Quality Criteria for Photochemical
Oxidants. National Air Pollution Control Administration Publication
No. AP-63. Washington, D. C.: U. S. Government Printing Office, 1970.
213. Veninga, T. S. Toxicity of ozone in comparison with ionizing radiation.
Strahlentherapie 134:469-477, 1967.
214. Vrochinskii, K* K. E. coli variability in water under the effect of ozone.
»
Zh. Mikrobiol. Epidemiol. Immunobiol. 41:79-84, Mar. 1964. (in Russian)
215. Watanabe, S., R.' Prank, and E. Yokoyama. Acute effects of ozone on lungs of
i
cats. I? Functional. Amer. Rev. Resp. Dis. 108:1141-1151, 1973.
216. Wayne, L. G., and L. A. Chambers. Biological effects of urban air
pollution. V. A study of effects of Los Angeles atmospher on
Laboratory rodents. Arch. Environ. Health 16:871-885, 1968.
217. Weibel, E. R. Morphometry of the Human Lung. Mew York: Academic Press, Inc.,
1963. 151 pp.
218.Weissbecker, L., R. D. Carpenter, P. C. Luchsinger, and T. S.'Osdene. In vitro
alveolar macrophage viability. Effect of gases. Arch. Environ. Health
18:756-759, 1969.
219. werthamer, S., P. D. Penha, and 1. Amaral. Pulmonary lesions induced by
chronic exposure to ozone. I. Biochemical alterations. Arch.
Environ. Health 29:164-166, 1974.
8-110
-------
220. Werthamer, S., L." H." Schwartz, J," J^ Carr, and L." Suskind. Ozone-induced
pulmonary lesions: Severe epithelial changes following sublethal doses.
Arch. Environ. Health 20:16-21, 1970.
221. Xintaras, C., B. L. Johnson, C. E. Ulrich, R. E. Terrill, and M. F. Sosecki.
Application of the evoked response techniques in air pollution
toxicology. Toxicol. Appl. Pharmacol. 8:77-87, 1966.
222. Yokoyamo, E., and R. Frank. Respiratory uptake o£ ozone in dogs. Arch.
Environ. Health 25:132-138, 1972.
223 Zelac, R. E., H. L. Cromroy, W. E. Bolch, Jr., B. G. Dunavant, and H. A.
Bevis. Inhaled ozone as a mutagen. I. Chromosome aberrations
induced in Chinese hamster lymphocytes. Environ. Res. 4:262-282, 1971.
224 Zelac, R. E. , H. L. Cromroy, W. E. Bolch, Jr., B. G. Dunavant, and H. A.
Bevis. Inhaled ozone as a mutagen. II. Effect on the frequency of
chromosome aberrations observed in irradiated Chinese hamsters.
Environ. Res. 4:325-342, 1971.
-------
CHAPTER 9
CONTROLLED STUDIES ON HUMANS
Most standards for safe concentrations of oxidants and other photo-
chemical pollutants are based on information about their effect on human
health. Such information is acquired through the interplay of different
fields of scientific endeavor, including epidemiologic investigation of
pollutant-exposed human groups and controlled experimental study of
animals or volunteer human subjects. Epidemiologic studies of humans can
be used to obtain dose-response information on polluted ambient air, but
they are limited by cost factors, dose-range availability, the presence of
interfering pollutant substances, and the problems caused by the presence
of many uncontrolled variables. Most controlled experimental investigations
have been conducted with animals. However, there is no rigorous way of
extrapolating animal dose-response data to humans. There is a need, then,
for comprehensive human experimental studies that are carefully controlled
and documented to ensure reproducibility and to withstand challenge by
proponents of other standards of safe concentrations. Such studies can
establish the presence and importance of acute health responses in normal
and hyperreactive people. Dose-response information, including minimal-
measurable-effects concentrations, can be determined. Hypotheses can be
developed and then subjected to animal or epidemiologic investigation. Typi-
cally, controlled human studies on the health effects of specific pollutants
use fixed concentrations, an absence of interfering pollutants, controlled
environmental conditions, and well-characterized volunteer subjects. Risk
is inherent in any research involving humans, and it is axiomatic that
reasonable and proper care should be taken. Prudence in the design of
-------
controlled human experiments requires that, when available, information from
animal and epidemiologic work be used to delineate ways in which critical
human studies are likely to be most useful.
The purposes of this chapter are to review available test methods
and protocol designs for controlled human studies, to review and discuss
published data, and to make recommendations for future studies.
EXPERIMENTAL METHODS
The basic design of studies on effects of pollutants should seek
to maximize information relevant to public health. Tests must be reliable
and sensitive, the experimental air environment must be rigorously controlled,
and the manner in which subjects are exposed to this environment must simu-
late ambient exposure. These constraints impose complications and necessi-
tate a focus on environmental control and monitoring, physiologic testing,
and evaluation of symptoms and clinical observations.
Controlled-Enviromnent Chambers
Construction and Monitoring Equipment. A survey of the environmental control
1 7 8 9 32
and monitoring technology used in several experimental studies
indicated significant limitations in experimental control capability. There
are seven controlled-environment chambers or clean-room facilities in the United
States for human exposure (community air pollution inhalation) from which studies
have been reported. Another is under construction at the University of North
Carolina in association with the EPA at Chapel Hill. There are three chambers
in Canada of similar design.
Table 9-1 lists design features of the exposure chambers in the
United States that have air-cleaning equipment. The facility at the
9-2
-------
TABLE 9-1
Controlled-Environment Chambers or Clean-Room Facilities for
Community Air Pollution Short- Or Long-Term Human Exposure,
United States"" Facility—
c
Item or Condition H.S.C. U. Md. U. Pa. R.L.A. St. V St. B~ N.Y.U.
Temperature Control + + + + + + +
Humidity Control + + + + + + +
Pressure Control + - + - - - -
Sound Control + - + + - + -
High-Efficiency Particle
Filter
Laminar Flow-
Charcoal Filter
Catalytic Filter—
+
-
+
+
+
+
+
+
-
+
_
+
e
+
+
+
-
+
_
+
+
+
_
Scrubber^
Purafil filter- - - - +
Active— - + - + - +
— Based in part on information from an EPA - sponsored workshop on controlled-
environment-chambers, April 26-27, 1971, Research Triangle Park, N.C.
b
— H.S.C. = Hospital for Sick Children, Washington, B.C.
U. Md. = University of Maryland Hospital, Baltimore,
U. Pa. = University of Pennsylvania Hospital, Philadelphia.
R.L.A. = Rancho Los Amigos Hospital, Bowney, Ca.
St. V. = St. Vincent's Hospital, New York, N.Y.
St. B. = University of California, Santa Barbara.
N.Y.U. = New York University, New York, N.Y. (Clean-room facility has
been dismantled).
r»
- More than one chamber available. This describes the plexiglass chamber used
for ozone and peroxyacetylnitrate studies.
~L Refers to use of an intake plenum to ensure fairly uniform air flow and
negligible gas concentration gradients within the region of the exposure
chamber occupied by subjects.
— Can be operated with intake flow either through or bypassing the plenum.
— Heated or nonheated bed designed to oxidize carbon nonoxide and light
hydrocarbons (not removed by activated charcoal) to carbon dioxide and water.
9-3
-------
g
The liquid acid gas scrubber is packed with, polypropylene and uses sodium
carbonate solution.
•L
— Aluminum oxide pellets impregnated with potassium permanganate.
— As judged by personal communication or recent publication.
9-4
-------
University of Maryland Hospital, Baltimore, has a chamber with activated-
charcoal and high-efficiency particle filters and controlled temperature
and humidity. St. Vincent's Hospital and New York University, New York
City, each have a clean-room facility. The University of Pennsylvania Hospital,
25
Philadelphia, has a self-contained, reinforced-concrete climate-controlled
chamber, with pressure controls from 28 to 32 in. Hg (about 710 to 810 mm
Hg, or 95 to 108 kilopascals). Rancho Los Amigos Hospital, Downey, California,
has a totally enclosed steel chamber. Inlet air is heated and passed through
a Hopcalite catalyst bed, filtered by high-efficiency particle filters,
activated charcoal, Purafil (aluminum oxide pellets impregnated with potassium
28a
permanganate), and a Mine Safety Appliance catalytic adsorbent bed. The
controlled-environment facility at the Hospital for Sick Children, Washington,
B.C., is a self-contained, reinforced-concrete structure that can provide
clean or specifically polluted air of monitored composition along with con-
trolled temperature, pressure, and humidity. The living area for the
subjects is a two-room apartment with bath and minimal kitchen facilities
2 7 53
(600 ft , or 56 m ). The University of California at Santa Barbara
has two chambers for temperature - and humidity-controlled environmental
studies. A third chamber is used for altitude simulation, and a fourth
for ozone and peroxyacetylnitrate (PAN) studies. The latter chamber is
6.5 ft (2m) wide, 10 ft (3m) long, and 19 ft (5.8m) high and is constructed
of plexiglass. A chamber complex at the University of Wisconsin in Madison
55
is designed primarily for studies of occupational inhalation toxicology.
A description of the environmental-control chamber for human
experimental studies at McGill University, Montreal, exemplifies the other
two Canadian facilities — at the Gage Research Institute, Toronto, and
9-5
-------
McMaster University, Hamilton, Ontario. It is a transparent chamber, 12 ft
(3.7 m) long, 8 ft (2.4 m) wide, and 6 ft (1.8 m) high constructed of 14 6x4-
ft (1.8 x 1.2-m) panels of plexiglass held together with angled metal.
The chamber is built within an ordinary air-conditioned working labora-
tory, with a door in the middle of one of the 12-ft (3.7-m) sides. Near
the bottom of the chamber a hole has been cut to accommodate a 9-in.
window fan, which gives the desired incoming atmosphere. Air from the
laboratory is not purified before entering the chamber. At the end of
the chamber opposite the fan, two outlet pipes, 6.5 and 3.75 in. (16.5
and 9.5 cm) in diameter, run from the chamber ceiling to a fume hood.
3 3
Air passes through the chamber at approximately 12,000 ft /h (336 m /h) ,
resulting in about 20 volume changes hourly. The temperature and humidity
controls are those for the building in which the chaff,', er is housed.
For the most reliable results, chamber environment should be
monitored continuously with instruments and techniques equivalent to
those used in ambient-air monitoring networks. Calibration of instruments
should follow recommendations by appropriate agencies and be checked by
cross comparisons with those in other analytic laboratories.
Ideally, two monitoring instruments, each operating on a different
principle, should be used for each gaseous pollutant under study. Ozone and
nitrogen oxides can be monitored with chemiluminescence analyzers, which
provide fast response and freedom from interference by other pollutants.
Total oxidants can also be monitored by the neutral potassium iodide solution
and Saltzman reagent methods with continuous-flow colorimetric analyzers.
A nondispersive infrared analyzer and an oxidative electrochemical analyzer
9-6
-------
can be used for monitoring carbon monoxide, and light-scattering counters
for monitoring particles.
Environmental Variables. In human experimental studies, variables to be
considered and controlled include pollutant gas concentration, humidity,
temperature, light intensity, noise, particles, and the presence of other
gases.
The relative humidity, air temperature, noise, and artificial
lighting must be controlled in environmental exposure chambers, because
they can influence a subject's response directly or indirectly. At high
temperature, heat stress can dominate the symptomatic and physiologic
responses of human subjects. The rates of some chemical reactions of
exposure gases depend heavily on temperature, so temperature should be
controlled. This can be done with refrigerated cooling coils in the
air-conditioning section of air supply systems, heaters, and thermo-
couple sensors. Extremes of relative humidity are known to cause dis-
comfort in humans. The equilibrium size of hygroscopic aerosol parti-
cles, the degree of conversion of sulfur dioxide to sulfurous acid in
41
sodium chloride droplets, and the extent and rate of chemical reaction
of mixtures of such pollutant gases as sulfur dioxide, ozone, and ammonia
depend on the relative humidity of the chamber air. Cooling coils in air-
conditioning units, and the injection of purified steam can be used to
regulate relative humidity. Artificial lighting within human-exposure
chambers should be designed to ensure proper illumination, but to avoid
potential experimental complications. If the intensity is too high, the
air may overheat. Ultraviolet irradiation should be avoided to prevent
photochemical reactions from forming uncontrolled and unknown reaction
9-7
-------
products in the chamber. If ultraviolet irradiation of gases is desired
to form specific oxidant compounds for human exposures, it should be carried
out in separate chambers to avoid contamination of the human-exposure chamber
with intermediate products and to prevent the subjects from being directly
exposed to harmful radiation. Conventional tungsten and fluorescent lighting
meet the illumination requirements of human-exposure chambers.
High levels of noise known to cause discomfort to humans are
unacceptable. Moderate noise also becomes undesirable in some experimental
situations, if it is distracting or interferes with speech communication.
During controlled exposures of human subjects to specific compounds
like ozone, the concentrations of suspended particles and trace gases must
be known and minimized to ensure that health effects can be attributed solely
to ozone. The air purification units for the environmental chambers are
designed to remove most of the particles and pollutant gases from the ambient
air. Prefilters and efficient absolute filters are used to remove 99% of
the particles with diameters of 0.3 jm or more. Catalytic beds, adsorption
beds, and activated-carbon and chemical filters are used to convert carbon
monoxide to carbon dioxide and to remove most of the other gaseous hydro-
carbons, sulfur dioxide, nitrogen dioxide, nitric oxide, and ammonia.
Condensation nuclei counters, which are commercially available, can be used
to monitor the total number of particles with diameters greater than 20A.
Light-scattering nephelometers can approximate the total number concentration
of particles with diameters of 0.1 - 1/im. Single-particle optical counters
with multichannel analyzers can be used to monitor the number of particles
in finite size intervals between 0.2 and 10 >mi. Alternatively, cascade
impactors and particle filters can be used to monitor the total mass
9-8
-------
concentration and the size distribution of the aerosol in the chamber.
Gas monitors are commercially available for sulfur dioxide, nitrogen
dioxide, nitric oxide, carbon monoxide, and ozone. Ammonia and these
other gases can also be collected by bubblers and analyzed by wet chemical
methods if proper precautions are taken to account for interferences.
Trace hydrocarbons can be monitored by taking bag samples and analyzing
them by gas chromatography, mass spectrometry, or infrared spectropho-
tometry.
In the design of controlled exposures to gases and particles,
separately or in combination, extreme care is needed to avoid formation
of interfering species. For example, in a study of the effect of a
39
mixture of nitrogen dioxide and ferric oxide aerosol in dogs, signifi-
cant quantities of ammonium and nitrate ions were found in particles
filtered from the air of the exposure chamber. Ammonia and trace hydro-
carbon gases also emanate from sedentary and exercising humans. To
prevent these contaminant gases from building up in the chamber, a continuous
flow of fresh air through the chamber must be maintained.
In exposures of humans to artificially generated aerosols, where
the information is to be relevant to ambient aerosols, several factors are
important: the particle diameter distribution must be fairly constant and
fall within size ranges typical for the given compound in the ambient air,
the chemical composition of the aerosol must be stable and predictable, and
the electric charge distribution of the aerosol must simulate that of
normal atmospheric aerosols.
Selection and Characterization of Subjects
A minimal group size is difficult to specify. Studies on similar
subjects could be expected to give the least variability in results; thus,
9-9
-------
dose-response information on relatively small groups of medically characterized
subjects could provide a basis for extrapolating to essentially similar
population groups. Useful results have been obtained with as few as eight
31
subjects. Healthy, young males probably should be studied initially because
some variations are known to accompany aging and some problems are peculiar
to females (e.g., the estrus cycle and pregnancy). Later studies of older
males and females will, however, be required for complete information.
Volunteers with disease who can give informed consent and for
whom some expected benefit balances the expected risk can be considered
as potential subjects. If those selected for the study are smokers, this
information and an estimate of the degree of smoking are needed, because
32,38
systematic differences between smokers and nonsmokers have been found.
People with known or suspected cardiopulmonary disease who are
referred by a physician for diagnostic environmental stress-testing may
also serve as subjects. Testing under environmental stress of persons
who are suspected hyperreactors to pollutants is analogous in concept to
exercise stress-testing of suspected cardiac patients. However, in
contrast with the general availability of exercise stress-testing laborato-
ries, the expense involved in an operational facility for environmental
stress-testing limits its availability to research centers. Accordingly,
a person who is referred for clinical testing by his physician may well
become part of investigative programs and be asked to volunteer for
additional procedures.
In selection of subjects, ethical considerations are dominant
and limit the deliberate exposure of minors or of others who are unable
legally to be volunteer subjects.
9-10
-------
Among the criteria for selecting subjects with close similarities,
socioeconomic status cannot be ignored any more than nutritional status
or genetic background. Finally, place of residence and prior occupational
pollution exposure may be important.
Measurement of Human Response
In addition to the visual monitoring of subjects during testing,
clinical assessment can be accomplished by having the project physician
interview each subject concerning symptoms, with a standard questionnaire
immediately after exposure. Also, subjects can keep a record, on a standard
form, of symptoms experienced during and after exposure. It is well to
note here that caution should be exercised in interpreting symptoms, because
these are unlikely to be "blind" studies.
Much progress has been made in recent years in the measurement and
understanding of lung physiology. Usually, several methods are available
for the measurement of each characteristic of lung function of interest.
Comprehensive descriptions of the various pulmonary function tests are
6 12 20 29
readily available, ' ' ' so a complete review will not be attempted
here.
Because the respiratory tract is an initial target of any air
pollutant challenge, it usually receives primary attention in tests to
determine irritant effects of exposure. Other aspects of interest include
hematology, blood enzyme biochemistry, eye irritation, and psychomotor
performance. Constriction of the large airways, maldistribution of ventila-
tion due to narrowing in some small airways, constriction of peripheral
lung units, and mechanical or gas diffusion impairment due to edema
9-11
-------
are possible effects of insult by pollutants. A variety of pulmonary tests
are required to examine the possibilities.
13
Flow-volume curves: The characteristics measured by the maximal
expiration are forced vital capacity (FVC), 1-s forced expiratory volume
c
(FEV..), peak expiratory flow rate (Vmax), and flow rates at 50% and 25%
• *
of the remaining FVC (V , V ) for partial and maximal flow-volume curves.
These measurements give an easily obtained, relatively reproducible
evaluation of overall pulmonary mechanical performance, but provide little
information on the mechanisms responsible for any observed changes.
22 23
Airway resistance (R ) and thoracic gas volume (TGV): ' The
measurement of R is probably more sensitive than maximal flow measurements
for constriction of large airways, but it is also more difficult to perform
and is less stable. These problems similarly affect the measurement of
TGV, which, however, may be useful for detecting gas trapped as a consequence
of airway dysfunction (in combination with a gas-dilution lung-volume
determination).
24,26,29
Total respiratory resistance(R ): Resistance can be measured
at pressure perturbation frequencies of 3, 6, 9, and 12 Hz. Unfortunately,
this measurement is affected by changes in upper-airway configuration, which may
complicate the detection of changes in pulmonary airways per se. As predicted
43
by Otis, the method is believed capable of detecting asynchronous mechanical
behavior (unequal regional ventilatory time constants), which otherwise can
be documented only by the considerably more difficult measurement of dynamic
lung compliance.
3»16 i6
Closing volume (CV): Buist and Ross measured the lung volume
at which closure of a significant number of small airways presumably occurs,
9-12
-------
as well as estimating of residual volume (RV) and total lung capacity (TLC)
through the expired nitrogen concentration. In another study, they presented
a method to estimate the uniformity of ventilation distribution by measuring
the slope of the alveolar nitrogen plateau.
40
Static lung compliance (C ) and dynamic lung compliance (C^ )
are measured from recordings of transpulmonary pressure and respiratory flow
and volume. Dynamic compliance in the tidal range is measured in a series
of breaths each at normal frequency and at other frequencies — such as 20,
40, 60, 80, and 100 breaths/min — with total volume monitored and kept constant.
Static compliance is measured by interrupting airflow intermittently during
an inspiration from functional residual capacity (FRC) to TLC, followed by
an expiration to RV. Each determination is preceded by an inspiration to
TLC to give a consistent volume history. Compliance measurements are indis-
pensable for documentation of changes in the mechanical characteristics of
the lung, particularly the development of unequal time constants. Unfortunate-
ly, the measurements are somewhat unstable and require considerable effort on
the part of subjects and investigators. In some studies, these tests are
performed only on a subgroup of subjects selected for motivation and performance.
Pulmonary diffusing capacity (Dj ) can be determined by the single-
JL(U
breath carbon monoxide method according to a technique developed by Ogilvie
42
e_t a\^. For example, a test gas containing 0.15% carbon monoxide and 10% helium in
air can be used. In calculating D^ , correction is made for backpressure of
carbon monoxide due to significant concentrations of blood carboxyhemoglobin.
Helium is measured with a thermal conductivity meter, and carbon monoxide with
an infrared detector or an electrochemical analyzer. Reproducibility of this
test may be poor under some conditions and it is affected by changes in ventila-
9-13
-------
tion diffusing capacity ratios, but the test offers the potential of detecting
changes in the blood-air interface (such as alveolar edema) that might
otherwise go undetected.
Oxygen consumption can be measured at rest and during exercise on
a constant-load bicycle ergometer or a treadmill at a level producing a
4
specified percentage of predicted maximal oxygen consumption. Expired
air is collected and measured with a spirometer to determine total expired
volume, and samples are analyzed for oxygen and carbon dioxide.
Carboxyhemoglobin concentration [COHb] can be estimated with the
method of Jones and co-workers. The subject holds a deep breath for 20 s
to allow equilibration of carbon monoxide between alveolar air and blood and
then expires a sample of that air into a container. The air carbon monoxide
concentration may be directly related to [COHb]. The test can be performed
before exposure in an environmental chamber to help to verify that the subject
has not received inordinate ambient pollutant exposure.
Biochemical studies on human blood samples have been used to measure
15
response by Buckley e_t al. , who reported changes in red cells and serum
of men after a single acute exposure to ozone at 0.50 ppm for 2.75 h. Red-
cell membrane fragility and glucose-6-phosphate dehydrogenase and lactate
dehydrogenase activities were increased, and red-cell acetylcholinesterase
activity and reduced gluathione were decreased. Red-cell glutathione reduc-
tase (GSSRase) activity was not significantly altered; however, serum GSSRase
activity was significantly decreased, and serum vitamin E content and lipid
peroxidation were significantly increased.
11 46 48
A number of investigators ' ' have argued that behavioral
changes are more prevalent than frank physiologic or clinical changes as
9-14
-------
effects of air pollutants. If the ability to perform routine tasks, such
as operating an automobile or a complex piece of machinery, is compromised
by pollutant exposure, the setting of air pollution standards should take
such effects into consideration.
28
In one study, human subjects were tested in a controlled-
environment chamber with a high (summer) temperature and with ozone, nitrogen
dioxide, and carbon monoxide as pollutants. Performance on a divided-atten-
tion task given at the end of the exposure period and the subjects' heart-
rate variability (as a potential psychophysiologic measure of attention) were
evaluated. The subjects displayed a significant decrement in peripheral
attention associated with increased ambient temperature. Effects attributable
to pollutant gases were variable.
Subjects exposed to ambient oxidant pollution or to controlled
oxidant pollution in a test chamber express their response by symptoms, as
well as by physiologic changes. Because of their subjective nature, little
attention has been given to symptoms in overall assessments of effects;
however, with systematic collection, these experimental data lend themselves
to semiquantitation.
28a
In the study by Hackney et al, the investigators proposed a
method for consistent gathering of symptom data by means of a checklist,
wherein symptoms are scored (according to predetermined criteria of severity)
for three different periods during and after exposure. The sum of the
scores for all symptoms from all periods gives a total symptom score, or
discomfort index, for the 24-h period after the start of exposure. In their
study, symptom scores for 42 subjects exposed to ozone at 0.25, 0.37, and
9-15
-------
0.5 ppm revealed a dose-response relationship for higher doses that approxi-
mated the relationship demonstrated by objective pulmonary function. These
results suggest that semiquantitation of symptoms is feasible in controlled
pollution-exposure studies and may be a useful clinical investigative tool.
Experimental Design Considerations
Multiple stresses may be important in assessing functional and adaptive
capabilities or people. An exposure protocol can be designed to simulate
as closely as possible the ambient exposure of a group likely to have signifi-
cant exposure, such as people working outdoors on a smoggy summer day. A
2-h exposure period is realistic, in that high ambient pollutant concentra-
tions usually persist about that long. Other exposure periods should be
chosen to simulate different pollutant episodes. Specified amounts of
exercise can serve as a tool in experimental design to provide additional
stress. Intermittent light exercise (sufficient to approximate a doubling
of minute volume) during exposure produces a realistic degree, of ventila-
tion (to which pollutant dose is approximately proportional) during typical
work. Increased temperature is another stress factor that is often present
during oxidant air pollution episodes and so can be introduced into the
experimental situation. The design can provide for successive days' exposures,
in that deleterious effects of exposure may be cumulative. These require-
ments can be incorporated into a protocol in a cost-effective manner that
tests several subjects on a given day. However, with a single chamber of
limited size, this requires staggered exposure and testing periods, precluding
"blind" studies or control measurements on the same day. Thus, sham control
runs (identical protocols with exposure to purified air) precede the pollutant
exposure, so that reliable baseline values of the measured characteristics
can be obtained.
9-16
-------
"Blind" studies with chemical substances that have a characteristic
odor or irritant effect are difficult to manage. If, as with ozone, the odor
sense tends to diminish, then "odor sham" protocols are possible. However,
keeping the subjects and the investigators (other than the safety officer)
truly uninformed about the nature of a particular experiment is not a trivial
problem.
37
Cyclic variations in measurements are potentially important.
Adequate information is not available, for example, on normal variation
over time in tests of human physiologic function. This presents a problem
in designing not only short-term experiments, but especially longer-term
studies. Detailed data on stability of a given measurement over periods of
minutes, hours, days, weeks, months, and even years would improve rational
experimental designs. Variations in measurements with changing seasons,
especially summer versus winter, might be expected, because of the effect
of large temperature differences on physiology and life style. Interactions
may be important in design and data interpretation. The likelihood of
recent prior exposure to high oxidant concentration is clearly a function
of the summer season and geographic location.
There is a definite need for dose-response information on specified
groups of people, if frequency distributions of responses are to be estimated.
Obtaining and using such information present numerous problems, such as
selection of appropriate groups and their size; the need to include persons
with disease, as well as the very young and very old; and extrapolation of
the data to the total population. With separate dose-response information
on representative samples of major population groups, a frequency distribution
of responses at each pollutant concentration might be determined by weighting
9-17
-------
the mean change for each group according to the general populations they
represent. Information on frequency distribution of responses is necessary
for any cost-benefit analysis that will require quantitative estimates of
effects in terms of dollars.
With due regard to the factors just discussed, a test series may
reasonably be designed to support or reject the hypothesis that no effects
of realistic pollutant exposure will be detected in volunteer subjects.
Results supporting the hypothesis would be useful to regulatory agencies in
setting air pollution standards. If minimal effects are found in a group
of "normal" subjects, an effective experimental strategy is to test a group
of specified "hyperreactive" subjects, characterized by a prestudy history
of cough, chest discomfort, or wheezing associated with allergy or exposure
to air pollution.
Experimental data can be subjected to repeated one-way variance analyses.
CO
Post hoc comparisons with the Newman-Kuels test are made when significant
differences among test conditions are found. A few significant differences
due to random variation may be found, because of the number of statistical
comparisons usually being made; therefore, all observed, statistically
significant changes must be examined critically for physiologic significance.
Ambient-Air Studies
Experiments can be conducted with well-specified ambient air, if
a suitable chamber is in a highly polluted area and if ambient air can be
introduced into the chamber without significant pollutant losses. Other runs
with clean air and matched temperature and humidity serve as controls. Alter-
natively, mobile health-testing laboratories with air monitoring capabilities
can go to polluted areas of interest.
9-18
-------
Detection of short-term cardiopulmonary effects of ambient oxidant
pollutant exposure is complicated by several factors. The physiologic
measures of such effects exhibit significant inherent variability, which may
mask the relatively small changes expected. The atmosphere contains many
potentially hazardous materials, both natural and man-made, in continuously
varying concentrations. Not all these substances have been identified,
and many that have been identified cannot be adequately monitored. Other
environmental factors, such as temperature and humidity, may influence
physiologic function independently and thus complicate the detection and
interpretation of pollutant effects. Variations in concentration of any
given pollutant are usually closely linked to variations in concentrations
of other pollutants., and this makes it difficult to assess the toxicity
of a single component of the ambient mixture. These problems have led
to the assertion that ambient-exposure study results cannot be interpreted
reliably, owing to the incompleteness of both the atmospheric and the
biologic information and the inability to control or allow for all inter-
fering variables. This assertion is correct in principle, but neglects the
possibility of obtaining valuable partial answers to health-effects questions
through ambient studies. Such improved understanding of the effects of
ambient oxidants should be attainable through improved atmospheric monitoring;
improved physiologic, biochemical, and clinical evaluation of exposed subjects;
application of findings from concurrent controlled-exposure studies; and
combination of ambient- and controlled-exposure studies.
REVIEW AND DISCUSSION OF PUBLISHED DATA
The data base on health effects of photochemical oxidants and ozone
was reviewed by the Subcommittee on Ozone and Other Photochemical Oxidants
9-19
-------
in a report prepared in September 1974 for the Committee on Public Works,
2
U.S. Senate. The following discussion repeats some of the material in
that report, to exemplify the need for further work, including controlled
human studies.
The federal primary ambient air quality standard for photochemical
3
oxidants is 160 ug/m (0.08 ppm), a maximal 1-h average concentration not
to be exceeded more than once per year. Air Quality Criteria for Photo-
chemical Qxidants catalogs and describes the overall data base for present
standards. In information received by the Subcommittee (February 23-24, 1974),
the following evidence was cited as the basis on which the EPA set the
standards:
• When high-shcool cross-country runners were exposed for 1 h to
photochemical oxidants at 0.03 - 0.3 ppm, their performance
decreased with increasing concentration. A statistical test
for threshold values (regression using "hockey stick" functions)
applied to these data gives a threshold estimate of 0.12 ppm, with
a 95% confidence interval of 0.067 - 0.163 ppm.1'5'30'44'57
3
• At short-term maximal peak oxidant concentration of 490 >ig/m
(0.25 ppm), subjects with asthma begin to experience significantly
more attacks. These maximal daily peaks may occur with a maximal
o
hourly average concentration as low as 300 jig/m (0.15 ppm). Eight
people sensitive to smog experienced increased attacks at oxidant
concentrations corresponding to those at which plant damage occurs
3 1,49
(8-h average, 200 ug/m , or 0.10 ppm).
o
• At short-term peak oxidant concentration of 196 >ug/m (0-10 ppm)
and above, humans begin to experience eye irritation. These
9-20
-------
peaks would be expected to occur with maximal hourly average
3 45,47
concentrations of 50-100 jug/m (0.025-0.05 ppm).
• At short-term ozone concentration of 160 ;ug/m3 (0.08 ppm) for
3 h, experimental animals (mice) exhibited increased susceptibility
to laboratory-induced bacterial infections. A firm dose-response
relationship was established for this effect.
14
• Brinkman j|t^ .al- found that, at short-term ozone concentration
3
of 392 Aig/m (0.20 ppm) for 1-2 h, experimental animals had
increased sphering of red blood cells. Similarly, humans had
o
increased sphering after 30 min of exposure to 490 >ig/m (0.25 ppm).
14
• Brinkman et al. also found that, at long-term ozone concentra-
3
tion of 392 jug/m (0.20 ppm) for 5 h/day for 3 weeks, structural
changes in the nuclei of heart muscle fibers were produced in
adult rabbits and mice. The fibers reverted to normal a month after
exposure.
The EPA used the data from the first three studies listed to obtain
3
the value of 200 ug/m (0.1 ppm) for a maximal 1-h concentration—the lowest
concentration at which measurable human effects are generally observed. No
formal methodology was used in making this selection; it was derived as a best
judgment by EPA officials.
Similarly, no published record exists to describe the procedure used
in selecting 0.08 ppm as the national primary standard for photochemical
oxidants. It is the recollection of EPA officials that the standard was
set midway between the highest average background concentration of ozone
(0.06 ppm) and 0.1 ppm, giving a 20% "margin of safety."
9-21
-------
There are obvious Inadequacies in the established values. First,
it was assumed that the oxidant standard is a surrogate standard for
photochemical oxidants, with ozone as the indicator. However, it is clear
that very low concentrations of specific irritants, such as peroxyacetyl-
nitrate (PAN), are sufficient to cause eye irritation. Second, some of the
statistical techniques used to determine the lowest concentration at which
effects are observed were inconsistent and undocumented. A "hockey stick"
5 44
function ' was sometimes used to find an effect threshold.
The inadequacy of the technical data base on photochemical
5
oxidants was realized from the start by EPA officials; Earth &t^ aJ.. , describing
the situation in 1971, stated that "many bits of information required to
place the present National Ambient Air Quality Standards on an irrefutable
and unassailable scientific basis are not yet available."
Exposure to Ozone
Studies before 1970 are reviewed in Air Quality Criteria for Photo-
chemical Oxidants. Details of selected controlled human studies repeated
later are given below.
lOa
Bates and Hazucha measured significant changes in lung function
(decrease in maximal flow rate at 50% of the vital capacity, maximal transpul-
monary pressure, and increase in total pulmonary resistance) in 10 normal
male subjects aged 23-35 years Concluding two smokers) exposed to pure ozone
at 0.75 ppm for 2 h. Two of the three subjects who exercised intermittently
at twice the resting volume showed accentuated effects. In a separate study
32
by Hazucha et ad. on effects of short-term exposure, significant changes in
lung function (decreases in forced vital capacity, forced expired volume at 1 s,
9-22
-------
maximal flow rate at 50% of vital capacity, and maximal midexpiratory
flow rate; and increases in closing capacity and residual volume) were
found in 12 normal males aged 23.6 + 0.7 years (including six smokers)
exposed to pure ozone at 0.75 and 0.37 ppm for 2 h during alternating rest
and exercise periods. The higher concentration affected smokers more than
nonsmokers, whereas the lower concentration affected smokers and nonsmokers
similarly. In these two studies, most subjects complained of cough, chest
tightness, and substernal soreness. A few also had pharyngitis, dyspnea,
and wheezing.
31
Hazucha also measured small decreases in the same lung functions
as above in three normal male subjects of mean age 20 years (nonsmokers)
exposed to pure ozone at 0.25 and 0.56 ppm for 2 h during alternating
15-min periods of rest and exercise. Although these decreases were not
statistically significant, in view of the small number of subjects involved,
they were consistent and in general agreed in value with dose-response
curves drawn from data at 0.75 and 0.37 ppm (Figure 9-1). The subjects
coughed and complained of chest tightness, substernal soreness, increased
9 31 32
salivation, and expectoration of mucus. The studies just described
were conducted in the Montreal chamber facility with general conditions
of: temperature, 21-23 C; humidity, 42-49% inside background air; and
two or more Mast coulombic meters for oxidant monitoring.
28a, 28b, 28c
Studies by Hackney et al. used a protocol designed to
simulate summer exposure in the Los Angeles southern coastal air basin and
included the additional stresses of heat, intermittent exercise, and
repeated exposures. Careful attention was given to environmental control,
pollutant monitoring and generation, and subject selection. Four male
9-23
-------
subjects aged 36-49 years (including one cigarette smoker) judged by subject-
ive criteria to have normally reactive airways completed this protocol.
No obvious effects — as assessed by clinical response and measures of
respiratory, cardiac, and metabolic functional change — were noted after
exposure for 4-5 h to 0.5-ppm ozone, 0.5-ppm ozone and 0.3-ppm nitrogen
dioxide, or 0.5-ppm ozone, 0.3-ppm nitrogen dioxide, and 30-ppm carbon
monoxide. A second group of four, aged 29-41 years (including two cigarette-
smokers) , who had previously experienced clinical bronchospasm and were
judged by subjective criteria to have hyperreactive airways (history of
developing symptoms during light activity in smog or history of asthma)
developed clinical discomfort and were unable to complete the protocol.
Exposed to ozone at 0.5 ppm for 4-5 h, this group developed marked changes
in pulmonary mechanics and gas distribution. Some effects were later
found after exposure to ozone at 0.37 ppm, but not at 0.25 ppm. In light
of the marked clinical effects, the protocol was modified, and a third
group of seven subjects, aged 22-36 years (including two smokers), judged to
have normally reactive airways, were studied. This group, exposed to ozone
at 0.5 ppm for 2 h, showed only minimal effects on the first day of exposure;
however, five of the seven showed significant effects on a second exposure
day. A fourth group of seven subjects, aged 22-41 years (including three
cigarette-smokers), exposed for 2 h to 0.25-ppm ozone, 0.25-ppm ozone and
0.3-ppm nitrogen dioxide, or 0.25-ppm ozone, 0.3-ppm nitrogen dioxide, and
30-ppm carbon monoxide showed no obvious effects. Of seven subjects, three
were judged on the basis of subjective criteria to have hyperreactive airways
and four were deemed to have normally reactive airways. A fifth group of
five subjects, aged 27—41 years (including one cigarette-smoker), was exposured to
0.37-ppm ozone for 2 h. Important changes with exposure were found in most phy-
siologic measures. However, one subject showed substantial changes in measures of
9-24
-------
lung mechanical function, which became worse on the second day of exposure.
Findings from this series of studies indicate that there is a wide range of
sensitivity to photochemical pollutants and that more sensitive people
develop significant symptoms, biochemical changes, and respiratory function
decrease under exposure conditions similar to those experienced during
i 0 ft /-»
pollution episodes. The studies just described ' ' were conducted
in the Rancho Los Amigos Hospital chamber facility with general conditions of:
temperature, 31C; humidity, 35%; purified background air; and chemilumine-
scence and neutral potassium iodide mentoring for oxidants.
Comparison of health effects of exposure to ozone ' ' '
suggests that Canadians are more reactive than southern Calif ornians. These
results are summarized in Figure 9—1. Experimental methods and subject
responses were compared further in a cooperative investigation of this
apparent reactivity difference. In studies conducted in California, four
Canadians and four Calif ornians were exposed to ozone at 0.37 ppm in purified
air at 21 C and 50% relative humidity for 2 h with intermittent light exer-
27a
cise. Exposures to purified air alone served as controls. Methodologic
differences sufficient to explain different results of previous studies were
not found. Subject responses were similar to those observed previously —
Canadians on the average showed greater clinical and physiologic reactivity
to exposure than did Calif ornians, who were no more than minimally reactive.
Canadians also showed larger increases in red-cell fragility after exposure.
These results support the existence of a real difference in reactivity between
the Calif ornians and Canadians studied to date. Although the number of
subjects tested in the cooperative study is small, the good agreement between
these results and previous results in the separate laboratories allows
considerably increased confidence in direct comparison of the previous results
9-25
-------
from Los Angeles and Canada, providing a considerably larger data base
from which to judge relative reactivity.
If the difference in response to ozone between Canadians and
southern Californians studied is accepted as real, a hypothesis of
adaptation in southern Californians is supported. Further support of the
hypothesis requires demonstration that the subjects tested are truly
representative of larger population groups residing in the same areas and
that identifiable factors other than adaptation are not sufficient to
explain the observations.
38
In studies by Kerr et al., 20 healthy adults — nine males and
one female, aged 21-60 years (including 10 smokers and 10 nonsmokers) —
were exposed to ozone at 0.5 ppm for 6 h in an environmental chamber.
During this period, they engaged in two 15-min medium exercise sessions
(100 W at 60 rpm) on a bicycle ergometer. Symptoms of dry cough and
chest discomfort, after ozone exposure, were more commonly noted in
nonsmokers. They also had a significant decrease in dynamic compliance
after exposure. Subjects who experienced symptoms, in general, were the ones
who developed objective evidence of decreased pulmonary function. Chest
discomfort ranged from tightness on full inspiration to generalized chest pain
accentuated by exercise, cough, and irritation of the nose and throat.
Significant changes from control values for the group as a whole after ozone
exposure were observed for several pulmonary function tests: specific
airway conductance (SGaw), pulmonary resistance (RL), FVC, and FEVo. No
significant change was observed with respect to diffusing capacity (D^ ),
CO
static lung compliance (Cgt), or the various tests derived from the nitrogen
elimination rate. When the smokers were considered as a separate group,
no significant decrease in pulmonary function was observed, although some
9-26
-------
38
individual smokers had decreases in pulmonary function. These studies
were conducted in the Baltimore chamber facility with general conditions of:
temperature, 24 C; humidity, 45%; purified background air; and two Mast
coulombic meters for oxidant monitoring.
64
Folinsbee et al. tested the response of 28 subjects after ozone
exposure to three stages of ergometer exercise with loads adjusted to 45,
60, and 75% of maximal aerobic power. The subjects were exposed to ozone
at 0.37, 0.40, or 0.75 ppm for 2 h, at rest or while exercising inter-
mittently — 15 min of rest alternated with 15 min of exercise at a
workload sufficient to increase ventilation by a factor of 2.5. These
studies were conducted in a plexiglass chamber (Toronto). Oxidant monitoring
was with a coulombmetric analyzer (Mast), which was checked periodically
against neutral buffered potassium iodide. Neither submaximal exercise
oxygen consumption nor minute ventilation was significantly altered after
ozone exposure at any concentration. The primary response was an alteration
of exercise ventilatory pattern. An increase in breathing rate (r=0.98)
and a decrease in tidal volume (r=0.91) were correlated with the dose of
ozone, calculated as the volume of ozone inspired during exposure. It was
concluded that through its irritant properties, ozone modified normal
ventilatory response to exercise and that this effect was dose-dependent.
48a
Rummo et al. exposed 22 male volunteers, aged 19-27, for up
to 4 h to ozone at 0.4 ppm in relatively clean ambient air or to ambient
air alone. Subjects were seated during exposure, except for two 15-min
exercise periods on a bicycle ergometer at 700 kg-m-min exercise that about
doubled the heart rate and quadrupled the ventilation volume. After 2 h of
ozone exposure, there was a significant change (_p_ < 0.05) in FVC, MMF, and
airway resistance (Raw). Several other measures (FEV-p VCQ, and ^25) were
lower after 2 h of exposure, but the statistical significance was borderline.
9-27
-------
However, after 4 h of exposure, all flow measures were significantly decreased,
compared with controls. After 4 h, Raw increased, FVC decreased further,
and FEV, decreased significantly. Residual volume, functional residual
capacity, and total lung volume did not change as a result of the ozone
exposure.
Kagawa and Toyama have reported on the results of limited studies
involving four normal male subjects exercising while exposed to ozone at 0.9
ppm for 5 min. A significant decrease in SGaw was found during exposure
and after 5 min of recovery.
9,28a,b,c,31,32,38,48a,64 . .
In all reported studies, an association
between symptoms and changes in lung function was usually found. In general,
people who noticed cough and substantial tightness first were the ones who
developed the greatest defect in function. Ozone-induced defects in function
were not usually found in the absence of definite symptoms of ozone-induced
respiratory irritation.
It would be desirable at this point to discuss mechanistic interpreta-
tion of the lung function measures — such as FEB-^, delta nitrogen, and airway
resistance — that have been reported to change with ozone challenge. Unfortu-
nately, although such measurements as FEV.. give an easily obtained, relatively
reproducible evaluation of overall lung mechanical performance, they provide
little information on the mechanisms responsible for any observed change.
Also, the measurement of the slope of the alveolar nitrogen plateau (delta
nitrogen) cannot be interpreted beyond saying that it reflects the uniformity
of ventilation distribution. Airway resistance and specific airway conductance
are thought to be sensitive measures of constriction of large airways. Results
of animal experiments provide additional information about mechanisms of action
of oxidant pollutants on the respiratory system. These are discussed in Chapter 8.
9-28
-------
In interpreting the results of human experimental studies with pure
ozone in relation to the oxidant standard, it must be remembered that the
other oxidants ordinarily present in smog were absent. Conceivably, a larger
difference may be necessary between the lowest concentration of pure ozone
at which an observed effect occurred and the air quality standard than between
the lowest concentration of oxidant mixtures and the standard.
„. . , _ ,. , ., , , 10,28a,28b,28c,31,32,36,38,
The newer experimental studies described above
48a,64
show that significant adverse health effects occur in humans at ozone
concentrations of 0.37 ppm and higher. Some limited studies show evidence
of human health effects of exposure to pure ozone at concentrations as low as
0.25 ppm (see Figure 9-1). The uncertainties of extrapolating ozone effects
to oxidant effects, of dose estimation, of measurement, and of subject
sensitivity must be kept in mind when comparing the new data with the standard.
Exposure to Ozone and Other Pollutants
Hazucha and Bates and Hazucha reported an enhanced effect between
ozone and sulfur dioxide in controlled-exposure studies of airway responses
in humans. Hazucha studied subjects only in the resting state; Bates and Hazucha
during rest and exercise. With various tests of ventilatory function—including
FEV,, midmaximal flow rate, and maximal expiratory flow rate at 50% of vital
capacity — the investigators showed that healthy male college students
experienced no effect of sulfur dioxide at 0.37 ppm, a 10% decline in function
with ozone at 0.37 ppm, and a 20-40% decline in function with a combination
of sulfur dioxide at 0.37 ppm and ozone at 0.37 ppm. The effect of ozone
alone on human function was not clearly mainifested until subjects had been
exposed for 2 h; the effect of the combination of ozone and sulfur dioxide was
apparent within 0.5 h. The maximal effect was observed in the first 30 min
9-29
-------
Figure 9-1. Behavior of FEV in response to ozone expressed as percentage
change from the appropriate control (SHAM) experiment. Smokers
and nonsmokers combined. Exposures 2 h, with intermittent light
exercise, except some Los Angeles exposures at 0.5 ppm for 4 h
with intermittent exercise. Points of error bars represent mean
response (AFEV postexposure vs. control) +1 standard error.
Curves represent best second-order polynominal fit to mean points.
Numbers adjacent to points represent sample sizes: L.A., 7 at
0.25 ppm, 13 at 0.37 ppm, 15 at 0.5 ppm; Montreal, 3 at 0.25 ppm
and 0.56 ppm (error bars not given, because of small sample
size), 12 at 0.37 ppm and 0.75 ppm. Mean values for L.A. and
Montreal 0.37 ppm x 2 h exposures are significantly different.
t = 4.15. 2. < 0.01. Equations for dose-response curves:
L.A., second-order fit to 3 data points, (AFEV %) = -7.524 +
2
46.546 (ppm 03) - 81.795 (ppm 03)"; Montreal, second-order
fit to 4 data points, (AFEV^) = 2.147 - 13.229 (ppm 03) -
2
35.383 (ppm 0.,) . NOTE: These equations are only for the
concentration ranges of the data.
9-30
-------
FIGURE 9-1
OWtGE IN FEVj
10,0
-10.0
r-20,0
,-30.0
PPM 03 ( BY NEUTRAL BUFFERED KI PETHQD )
-6 ,8
9-31
-------
after cessation of exposure. Care was taken to use scrubbers on the instru-
ments that were used to measure each gas concentration. The effect of the
combined gases was greater than the sum of the effects of the two gases
administered separately.
AJ n. i i A .*> A • 28a,28b,28c
Adult male volunteers were exposed to purified air,
to ozone alone, or to ozone in combination with nitrogen dioxide and carbon
monoxide. No additional effects were detected when nitrogen dioxide at
0.3 ppm was added to ozone. The addition of carbon monoxide at 30 ppm to
the ozone-nitrogen dioxide mixture produced no additional effects, other
than a slight increase in blood carboxyhemoglobin content and small decreases
in psychomotor performance, which were not consistent in different subject
groups.
Exposure to Peroxyacetylnitrate
52
In 1965, Smith reported increased oxygen uptake during exercise
in college students exposed to PAN at 0.3 ppm. The average increase was
21 62
2.3%. More recently, Drinkwater et al. and Ravin et al. found no
significant physiologic change attributed to PAN exposure. They tested 20
young men (smokers and nonsmokers) for maximal aerobic power (treadmill walk)
in a 35 C environment under four ambient air conditions: filtered air,
carbon monoxide at 50 ppm, PAN at 0.27 ppm, and carbon monoxide and PAN.
No significant physiologic effects were noted during the PAN exposure for
smokers or nonsmokers. Maximal aerobic power was not affected by any
pollutant condition. Heat stress was more effective than any pollutant
condition in reducing work capacity, and a 4.3% decrease in maximal aerobic
power in a 35 C environment, compared with a 25 C environment, was greater
than the differences in aerobic power found between filtered air and any of
the pollutant conditions.
9-32
-------
Other Experimental Studies
34
Holland et^ a]^. studied 14 subjects under conditions of short-term
exposures to irradiated automobile exhaust. The environmental conditions
simulated the "moderate" smog episodes in the Los Angeles air basin. Oxidant
concentrations were reported as 0.22-0.27 ppm (on the basis of the alkaline
potassum iodide method). No significant changes attributed to exposure were
found in reaction time, vital capacity, work performance, or oxygen consump-
tion.
60
Henschler reported that the characteristic pungent odor of ozone
was detected instantaneously at low concentrations (less than 0.02 ppm),
depending on individual sensory perception acuity, and perceived at higher
concentrations (0.05 ppm) for an average of 5 min. At higher concentrations,
the odor was perceived as stronger and persisted for an average of 13 min.
Eye irritation has been a common complaint of people exposed to
33
photochemical air pollution. Attempts to investigate this experimentally
have encountered problems, because of the subjective nature of the human
response and the multiphasic photochemical reactions involved. Human studies
conducted until 1970 on eye irritation are cataloged and discussed in National
Air Pollution Control Administration Publication AP-64, Air Quality Criteria
for Hydrocarbons.
Several studies indicate that the major photochemical products that
cause eye irritation are acrolein, PAN, and peroxybenzoylnitrate (PBzN). ' '
Ozone, the principal contributor to ambient oxidant concentrations, is not an
eye irritant. This is an important observation, because it might have been
assumed that lacrimation would correlate with respiratory effects. In fact,
however, ozone concentrations can be high enough to cause considerable respira-
tory effects without any irritation of the eyes having been noted. Heuss
and Glasson state that the potency of PBzN as an eye irritant is 200 times
9-33
-------
33
that of formaldehyde. In studies by Heuss et al, PBzN was formed in
parts-per-million amounts by irradiating automobile exhaust in laboratory
apparatus. When some aromatics were added to a low-aromatic gasoline,
PBzN and greatly increased eye irritation resulted.
63
Wilson et al. measured irradiated automobile exhaust and pure
organic compounds and found that the addition of sulfur dioxide, although
it increased aerosol formation, decreased eye irritation in many of the
hydrocarbon - NOx systems studied.
A number of components of ambient oxidant mixtures are discussed
in Chapter 3. Further detailed characterization studies of ambient particulate
pollution may suggest that some of these compounds are present in the organic
fraction in quantities likely to be detrimental to human health. Further
controlled health-effects studies might be accomplished with irradiated and
diluted automobile exhaust or exposure to pure specific compounds.
Limitations of Controlled Human Studies
It is apparent that controlled human experimental studies are
needed, but are cumbersome and costly. Other limitations include restrict-
ions as to the number of measurable responses and the fact that individual
pollutants are usually studied, rather than ambient mixtures. In addition,
healthy subjects are usually studied, rather than sensitive population
groups. The results of these studies are applicable to acute effects; but
their relation, if any, to chronic effects is not known.
Ethical considerations impose design requirements that increase
the cost and complexity of controlled human studies. For example, prudent
operational guidelines for such studies could include:
9-34
-------
• The Investigators serving as the first subjects for each series
of exposure studies.
• Pollutant exposure concentrations selected so as not to exceed
documented ambient concentrations.
• The exposure environment constantly monitored by the technician
who is operating the pollutant generating equipment.
• The presence of a physician.
• Monitoring of subjects electrocardiograpaically from outside
the chamber.
• Direct observation of subjects at all times by viewport or
closed-circuit television.
• Frequent checks by the attending physician and the chamber
engineer for hazardous conditions and, if they encounter any,
application of corrective measures or halting of the study.
• Physician screening of prospective volunteers.
• Obtaining of informed consent after the subject is given a
full explanation of the experimental procedures, including
known risks and discomforts. The form would describe the
procedures and risks fully and specify that the subject may
withdraw from the study at any time.
SUMMARY
Convincing new information on the health effects of oxidant
exposure has emerged from controlled studies on humans, from which tentative
dose-response curves have been constructed. The new data show statistically
significant reduced pulmonary function in healthy smokers and nonsmokers
at ozone concentrations at and above 0.37 ppm for 2-h exposures. Other gases
9-35
-------
and aerosols found in an urban atmosphere were not present in these experiments.
Some studies suggest that mixtures of sulfur dioxide and ozone at a
concentration of 0.37 ppm are more active physiologically than would be
expected from the behavior of the gases acting separately.
Wide variation in response among different individuals is a general
finding in studies of oxidants, as well as other pollutants.
Undesirable health effects of oxidant air pollution exposure are
increased by exercise, and many people apparently limit strenuous exercise
voluntarily when oxidant pollution is high.
Safety, ethical, and legal considerations require that the utmost
care be exercised in human experimentation. The risk inherent in this work
can be minimized by taking reasonable precautions while ensuring the satis-
factory performance of the study.
RECOMMENDATIONS
Further studies are needed to give better dose-response information
and to provide a frequency distribution of the population response to oxidants
alone and in combination with other pollutants at various concentrations.
Such studies should include the effects of mixed pollutants over ranges
corresponding to the ambient atmosphere. With combinations of ozone and
sulfur dioxide, the mixture should be carefully characterized to be sure
of the effects of trace pollutants on sulfate aerosol formation. The design
of such studies should consider the need to use the information for cost-
benefit analysis and for extrapolation from animals to humans and from small
groups of humans to populations. Recent research has indicated the possibility
of human adaptation to chronic exposure to oxidants. Further study is
desirable.
9-36
-------
Studies are needed to clarify the importance of age, sex, ethnicity,
familial elements, nutritional factors, and pharmacologic agents in determining
response to oxidants. Because people with lung disease are thought to be more
susceptible to oxidant pollutants, exposure studies are needed to quantify this.
Better methods for measuring or estimating the actual dose of oxidants absorbed
by each subject are needed. The usual time variation in measures of human
response should be evaluated per se, because this information is needed to
optimize experimental design.
More information is needed before rational guidance can be given about
limiting exercise during periods of high oxidant pollution.
Standards for the exposures of humans to controlled atmospheres
should be discussed by national groups and agencies, such as the National
Academy of Sciences, the American Medical Association, and the National
Institutes of Health.
9-37
-------
REFERENCES
la. U. S. Department of Health, Education, and Welfare. Public Health Service.
National Air Pollution Control Administration. Epidcmiological appraisal
of photochemical oxidants, pp. 9-1--9-33. In Air Quality Criteria for
Photochemical Oxidants. NAPCAPubl. No. AP-63. Washington, D. C. :
U. S. Government Printing Office, 1970.
lb. u. S. Department of Health, Education, and Welfare. Public Health Service.
National Air Pollution Control Administration. Natural sources of
ozone, pp. 4-1--4-4. In Air Quality Criteria for Photochemical Oxidants.
NAPCAPubl. No. AP-63. Washington, D. C.: U. S. Government Printing
Office, 1970.
2«. National Academy of Sciences. National Academy of Engineering. Coordinating
Committee on Air Quality Studies. Air Quality and Automobile Emission
Control. Vol. 1. Summary Report. U. S. Senate Committee Print Serial
No. 93-24. Washington, D. C.: U. S. Government Printing Office, 1974.
129 pp.
2b. National Academy of Sciences. National Academy of Engineering. Coordinating
Committee on Air Quality Studies. Air Quality and Automobile Emission
Control. Vol. 2. Health Effects of Air Pollutants. U. S. Senate
Committee No. 93-24. Washington, D. C.: U. S. Government Printing
Office, 1974. 511 pp.
2c. National Academy of Sciences. National Academy of Engineering. Coordinating
Committee on Air Quality Studies. Air Quality and Automobile Emission
Control. Vol. 3. The Relationship of Emissions to Ambient Air Quality.
U. S. Senate Committee Print Serial No. 93-24. Washington, D. C.:
U. S. Government Printing Office, 1974. 137 pp.
9-38
-------
2d. National Academy of Sciences. National Academy of Engineering. Coordinating
Committee on Air Quality Studies. Air Quality and Automobile Emission
Control. Vol. 4. The Costs and Benefits of Automobile Emission Control.
U. S. Senate Committee Print Serial No. 93-24. Washington, D. C.:
U. S. Government Printing Office, 1974. 470 pp.
3. Anthonisen, N. R., J. Danson, p. C. Robertson, and W. R. D. Ross. Airway
closure as a function of age. Respir. Physiol. 8:58-65, 1970.
4. Astrand, P. 0., and I. Rhyming. A nomogram for calculation of aerobic capacity
(physical fitness) from pulse rate during submaximal work. J. Appl.
Physiol. 7:218-221, 1954.
5. Barth, Dt S., J. C. Romanovsky, J.'M. Rnelson, A. P4 Altshuller, and R. J. M."
Horton. Discussion /_of national ambient air quality standards/. J. Air
Pollut. Control Assoc. 21;544-548, 1971.
6. Bates, D. V., P. T. Macklem, and R. V. Christie. Respiratory Function in
Disease. An Introduction to the Integrated Study of the Lung. (2nd ed.)
Philadelphia: W7 B7 Saunders, Co., 1971. 584 pp.
7. Bates, D. V., G. Bell, C. Burnham, M. Hazucha, J. Mantha, 1. D. Pengelly,
and F. Silverman. Problems in studies of human exposure to air
pollutants. Can. Med. Assoc. J. 103:833-837, 1970.
8. Bates, D. V. Air pollutants and the human lung. The James Waring Memorial
Lecture. Amer. Rev. Respir. Dis. 105:1-13, 1972.
9o Bates, D. V., G[ H. Bell, CT D; Burnham, M. Hazucha, J. Mantha, L/ D. Pengelly,
and P." Silver-man. Short-term effects of ozone on the lung. J. Appl.
Physiol. 32:176-181, 1972.
9-39
-------
lOa. Bates, D., and M. Hazucha. The short-term effects of ozone on the human
lung, pp. 507-540. In National Research Council.. Assembly of Life
Sciences. Proceedings of the Conference on Health Effects of Air
Pollutants, October 3-5, 1973. Senate Committee on Public Works Print
Serial No. 93-15. Washington, D. C.: U. S. Government Printing
Office, 1973.
10b. Hazucha, M. , and D. V. Bates. Combined effect of ozone and sulphur dioxide
on human pulmonary function. Nature 257:50-51, 1975.
11. Behavioral toxicology looks at air pollutants. /Interview with C. Xintaras^/
Environ. Sci. Technol. 2:731-733, 1968.
12. Bouhuys, A. Breathing: Physiology, Environment and Lung Disease. New York;
Grune and Stratton, 1974. 511 pp.
13. Bouhuys, A., V. R. Hunt, B. M. Kim, and A. Zapletal. Maximum expiratory flow
rates in induced bronchoconstriction in man. J. Clin. Invest. 48:1159-
1168, 1969.
14. Brinkman, R., H. B. Lamberts, and T. S. Veninga. Radiomimetic toxicity
of ozonised air. Lancet 1:133-136, 1964.
15 Buckley, R. D., J. D. Hackney, K. Clark, and C. Posin. Ozone and human
blood. Arch. Environ. Health 30:40-43, 1975.
16^ Buist, A. S., and B. B. Ross. Predicted values for closing volumes using a
modified single breath nitrogen test. Amer. Rev. Respir. Dis. 107:744-
752, 1973.
17. Buist, A. s., and B. B. Ross. Quantitative analysis of the alveolar plateau
in the diagnosis of early airway obstruction. Amer. Rev. Respir. Dis.
108:1078-1087, 1973.
9-40
-------
18. Coffin, D. 1., E. J. Blommer, D. E. Gardner, and R. S. Holzman. Effect of
air pollution on alteration of susceptibility to pulmonary infections,
pp. 75-80. In Proceedings of the 3rd Annual Conference on Atmospheric
Contaminants in Confined Spaces. Dayton, Ohio: Wright-Patterson Air
Force Base, Aerospace Medical Research Laboratories, 1968.
19^ Coffin, D. L., and D. E. Gardner. Interaction of biological agents and chem-
ical air pollutants. Ann. Occup. Hyg. 15:219-234, 1972.
20. Comroe, J. H., R. E. Forster, A. B. Dubois, W. A. Btiscoe, and E. Carlsen.
The Lung: Clinical Physiology and Pulmonary Function Tests. (2nd ed.)
Chicago: Year Book Medical Publishers, Inc., 1962. 390 pp.
21. Drinkwater, B. L., P. B. Raven, S. M. Horvath, J. A. Gliner, R. 0. Ruhling,
N. W. Bolduan, and S. Taguchi. Air pollution, exercise, and heat stress.
Arch. Environ. Health 28:177-181, 1974.
22. Du Bois, A. B., S. Y. Botelho, G. N. Bedell, R. Marshall, and J. H. Comroe.
A rapid plethysmographic method for measuring thoracic gas volume: A
comparison with a nitrogen washout method for measuring functional resid-
ual capacity in normal subjects. J. Clin. Invest. 35:322-326, 1956.
23. Du Bois, A. B., S. Y. Botelho, and J. H. Comroe. A new method for measuring
airway resistance in man using a body plethysmograph: Valves in normal
subjects and in patients with respiratory disease. J. Clin. Invest. 35:
__ 327-335, 1956.
24. Du Bois, A. B., A, W. Brody, D, H. Lewis, and B. F. Burgess, Jr. Oscillation
mechanics of lungs and chest in man. J.'Appl. Physiol. 8:587-594, 1955.
25. Everetts, J., Jr. Design of climate-control chamber. Trans. N. Y. Acad. Sci,
24:173-176, 1961.
9-41
-------
26. Goldman, M. D., R. J. Knudson, J. Mead, N. Peterson, J. S. Schwaber, and
M. E. Wohl. A simplified measurement of respiratory resistance by
forced oscillation. J. Appl. Physiol. 28:113-116, 1970.
27a> Hackney, J. D., W. S. Linn, S. K. Karuza, R. D. Buckley, D. C. Law, D. V.
Bates, M. Hazucha, L. D. Pengelly, and F. Silverman. Health effects
of ozone exposure in Canadians versus Southern Californians. Amer.
Rev. Respir. Dis. 111:902, 1975. (abstract)
2ga< Hackney, J. D., W. S. Linn, R. D. Buckley, E. E. Pedersen, S. K. Karuza,
D. C. Law, and A. Fischer. Experimental studies on human health effects
of air pollutants. I. Design considerations. Arch. Environ. Health
30:373-378, 1975.
28b. Hackney, J. D., W. S. Linn, J. G. Mohler, E. E. Pedersen, P. Breisacher,
and A. Russo. Experimental studies on human health effects of air
pollutants. II. Four-hour exposure to ozone alone and in combination
with other pollutant gases. Arch. Environ. Health 30:379-384, 1975.
28c. Hackney, J. D., W. S. Linn, D. C. Law, S. K. Karuza, H. Greenberg, R. D.
Buckley, and E. E. Pedersen. Experimental studies on human health
effects of air pollutants. III. Two-hour exposure to ozone alone and
in combination with other pollutant gases. Arch. Environ. Health
30:385-390, 1975.
29. Fenn, W. 0., and H. Rahn, Eds. Handbook of Physiology. Section 3. Respira-
tion. Vols. 1 & 2. Washington, D. C.: American Physiological Society,
1965. 1,696 pp.
30. Hasselblad, V., G. Lowrimore, W. C. Nelson, J. Creason, and C. J. Nelson.
Regression Using "Hockey Stick" Functions. Durham, N. C.: U. S. Depart-
ment of Health, Education and Welfare. Public Health Service. Environ-
mental Health Service. National Air Pollution Control Administration.
(in house report, 1970.)
9-42
-------
31. Hazucha, M. Effects of Ozone and Sulfur Dioxide on Pulmonary Function in Man.
Ph.D. Thesis. McGill University, Montreal, Canada, 1973. 233 pp.
32. Hazucha, M., F. Silverman, C. Parent, S. Field, and D. Bates. Pulmony func-
tion in man after short-term exposure to ozone. Arch. Environ. Health
27:183-188, 1973.
33. Heuss, J. M., G. T. Nebel, and B. A. D'Alleva. Effects of gasoline aromatic
and lead content on exhaust hydrocarbon reactivity. Environ. Sci.
Technol. 8:641-647, 1974.
34. Holland, G. J., D. Benson, A. Bush, G. Q. Rich, and R. P. Holland. Air
pollution simulation and human performance. Amer. J. Public Health
_ 58:1684-1690, 1968.
35< Jones, R.'H., M. F. Ellicott, J. B. Cadigan, and E. A. Gaensler. The relation-
ship between alveolar and blood carbon monoxide concentrations during
breathholding. Simple estimation of COHb saturation. J. Lab. din. Med.
51:553-564, 1958.
36^ Kagawa, J., and T. Toyama. Effects of ozone and brief exercise on specific
airway conductance in man. Arch. Environ. Health 30:36-39, 1975.
36a. Kennedy, H. W. Legal aspects of human exposure to atmospheric pollutants.
Arch. Environ. Health 6:785-798, 1963.
37. Kerr, H. D. Diurnal variation of respiratory function independent of air
quality. Experience with an environmentally controlled exposure cham-
ber for human subjects. Arch. Environ. Health 26:144-152, 1973.
38. Kerr, H. D., T. J. Kulle, M. L. Mcllhany, and P. Swidersky. Effects of
ozone on pulmonary function in normal subjects. An environmental-
chamber study. Amer. Rev. Respir. Dis. 111:763-773, 1975.
9-43
-------
39. Knott, M. J., and M. Malanchuk. Analysis of foreign aerosol produced in
N02-rich atmospheres of aerosol exposure chambers. Amer. Ind. Hyg.
Assoc. J. 30:147-152, 1969.
40. Milic-Emili, J., J.'Mead, J. M. Turner, and L, M, Glauser. Improved technique
for estimating pleural pressure from esophogeal balloons. J. Appl.
Physiol. 19:207-211, 1964.
41. McJilton, C., R. Frank, and R. Charlson. Role of relative humidity in the
synergistic effect of a sulfur dioxide-aerosol mixture on the lung.
Science 182:503-504, 1973.
42. Ogilvie, C. M., R. E. Forster, W. S. Biakemore, and J. W. Morton. A stand-
ardized breathholding technique for the clinical measurement of the
diffusing capacity of the lung for carbon monoxide. J. Clin. Invest.
36:1-17, 1957.
43. Otis, A. B., C. B. McKerrow, P. A. Bartlett, J. Mead, N. McTlroy, N. J.
Selverstone, and E. P. Radford. Mechanical factors in distribution
of pulmonary ventilation. J. Appl. Physiol. 8:427-443, 1958.
44. Quandt, R. E. The estimation of the parameters of a linear regression system
obeying two separate regimes. J. Amer. Stat. Assoc. 53:873-880, 1958.
45. Renzetti, N. A., and V. Gobran. Studies of Eye Irritation Due to Los Angeles
Smog, 1954-1956. Air Pollution Foundation MR-4. San Marino, Calif.:
Air Pollution Foundation, 1959.
46. Reynolds, R. U. Project Clean Air Research Reports. Task Force Assessments.
Vol. 3. Psychological and Behavioral Effects. Riverside: University
of California, 1970. (UNVERIFIED)
47. Richardson, N. A., and W. C. Middleton. Evaluation of Filters for Removing
Irritants From Polluted Air. University of California. Department
of Engineering Report No. 57-43. Los Angeles: University of California,
1957. 31 pp.
9-44
-------
48. Ruffin, J. B. Functional testing for behavioral toxicity: A missing dimen-
sion in experimental environmental toxicology. J. Occup. Med. 5:117-
121, 1963.
48a. Rumrno, N. J., J. H. Knelson, S. Lassiter, and J. Cam. Effects of ozone on
pulmonary function in healthy young men. Personal Communication, 1975.
49. Schoettlin, C. E., and E. Landau. Air pollution and asthmatic attacks in
the Los Angeles area. Public Health Rep. 76:545-548, 1961.
50. Schuck, E. A., and G. J. Doyle. Photooxidation of Hydrocarbons in Mixtures
Containing Oxides of Nitrogen and Sulfur Dioxide. Report No. 29. San
Marino, Calif.: Air Pollution Foundation, 1959. _/ 126 pp._/
51. Shy, C. M., Y. Alarie, D. V. Bates, R. Frank, J. D. Hackney, S. M. Horvath,
and J. A. Nadel. Synergism or antagonism of pollutants in producing
health effects, pp. 483-499. In National Academy of Sciences. National
Academy of Engineering. Coordinating Committee on Air Quality Studies.
Air Quality and Automobile Emission Control. Vol. 2. Health Effects
of Air Pollutants. U. S. Senate Committee No. 93-24. Washington, D. C.:
U. S. Government Printing Office, 1974.
52. Smith, L. E. Peroxyacetyl nitrate inhalation. Cardiorespiratory effects.
Arch. Environ. Health 10:161-164, 1965.
53. Snell, R. E., and P. C. Luchsinger. Effects of sulfur dioxide on expiratory
flow rates and total respiratory resistance in normal human subjects.
Arch. Environ. Health 18:693-698, 1969.
54. Stephens, E. R., E. F. Darley, 0. C. Taylor, and W. E. Scott. Photochemical
reaction products in air pollution. Int. J. Air Water Pollut. 4:79-
100, 1961.
9-45
-------
55a. Stewart, R. D. , C. L. Hake, A. J. Lebrurt, J. H. Kalbfleisch, P. E. Newton,
J. E. Peterson, H. H. Cohen, R. Struble, and K. A. Busch. Effects of
trichloroethylene on behavioral performance capabilities, pp. 96-129.
In C. Xintaras, B. L. Johnson and I. de Grott, Eds. Behavioral Toxicol-
ogy. Early Detection of Occupational Hazards. HEW Publ. No. (NIOSI!)
74-126. Washington, D. C.: U. S. Government Printing Office, 1974.
55b. Medical College of Wisconsin. Measurement of physiological and behavioral
responses in a controlled-environment chamber, pp. 361-375. In C.
Xintaras, B. L. Johnson and I. de Groot, Eds. Behavioral Toxicology.
Early Detection of Occupational Hazards. HEW Publ. No. (NIOSH)74-126.
Washington, D. C.: U. S. Government Printing Office, 1974.
56. U. S. Environmental Protection Agency. Part 410--National primary and secon-
dary ambient air quality standards. Fed. Reg. 36:8186-8201, 1971.
57. Wayne, W. S. , and P. F. Wehrle. Oxidant air pollution and school absenteeism.
Arch. Environ. Health 19:315-322, 1969.
58. Winer, B\ J. Statistical Principles in Experimental Design. (2nd ed.) New
York: McGraw-Hill Book Company, 1971. 907 pp.
59. Yamashiro, S. M., S. K. Karuza, and J. D. Hackney. Phase compensation of
Fleisch pneumotachographs. J. Appl. Physiol. 36:493-495, 1974.
60. Henschler, D.", A. Stier, H, Beck, and W. Neumann. Geruchsschwellen einiger
wichtiger Reizgase (Schwefeldioxyd, Ozon, Stickstoffdioxyd) und
Erscheinungen bei der Einwirkung Geringer Konzentrationen auf den Menschen,
Arch. Gewerbepathol. Gewerbehyg. 17:547-570, 1960.
61. Heuss, J/M., and W. A. Glasson. Hydrocarbon reactivity and eye irritation.
Environ. Sci. Technol. 2:1109-1116, 1968.
9-46
-------
62. Raven, P. B. , B. L. Drinkwater, R. 0. Ruhling, N. Bolduan, S. Taguchi, J.
Gliner, and S. M. Horvath. Effect of carbon monoxide and peroxyacetyl
nitrate on man's maximum aerobic capacity. J. Appl. Physio1. 36:288-
293, 1974.
63. Wilson, W. E., Jr., A. Levy, and E. H. McDonald. Role of S02 and photochem-
ical aerosol in eye irriation from photochemical smog. Environ. Sci.
Technol. 6:423-427, 1972.
64. Folinsbee, 1. J., F. Silverman, and R. J. Shephard. Exercise responses follow-
ing ozone exposure. J. Appl. Physiol. 38:996-1001, 1975.
9-47
-------
Chapter 10
EPIDEMIOLOGIC STUDIES
A variety of epidemiologic studies attempting to associate various
characteristics of human health and functioning with daily concentrations of
photochemical oxidants have been carried out during the last two decades,
primarily in the Los Angeles air basin. A few of these have shown clear-cut
associations involving large segments of the population. Other studies related
to both the same and different health indicators have failed to demonstrate any
consistent association. Failure to establish clear-cut associations may well be
inherent in some aspects of the epidemiologic method. Epidemiologic studies
have the advantage of being focused on the real -world, using human populations
in their normal setting. This permits identification of both long-term and
short-term variations in health and function that can be correlated with pol-
lutant exposures. It also permits identification of susceptible groups within
the general population that may be at greater risk. Epidemiologic studies,
however, have two main disadvantages: the health indexes used must inevitably
be relatively crude, as opposed to controlled laboratory conditions; and it is
extremely difficult in the real world to isolate the effect of one environmental
factor in the presence of numerous other independent and dependent variables,
•which may be synergistic with or antagonistic to the environmental factor under
study--e. g. , other air pollutants, meteorologic factors, socioeconomic status,
occupational exposures, personal health habits, and cigarette-smoking. Within
these limits, some definite conclusions can be drawn as to the association (or
lack of it) of some health indicators with photochemical oxidant pollution.
Because of the lack of epidemiologic information in some critical areas, use
-------
must be made of clinical and toxicologic studies on photochemical oxidants,
both in setting ambient air standards and in planning future epidemiologic
studies.
MORTALITY
Death is obviously the most clear-cut and significant end point for
determining the effect of an environmental challenge on health. It rarely has
a single, isolated cause, however, even in apparently simple events like
automobile accidents, homicide, and suicide. Careful investigation -will
usually reveal a constellation of factors that contributed to the final event.
Documented episodes of deliberate or inadvertent exposure of a sizable pop-
ulation to a high concentration of a known toxic substance are extremely rare,
and all attempts to link death with ambient air pollution at normal concen-
trations must consider a multitude of factors. Furthermore, these factors
often vary from person to person and from situation to situation. Among the
factors that must be considered are the age and state of health of the person
affected, the presence of coexisting disease states (likely for many
people), the activity being pursued by the person at the time of and just
before death, and individual biologic variation in response to different
types of stress. Other factors that must be considered in relation to the
specific challenge are the type of pollutant, the presence of other pollutants
(always a factor in epidemiologic studies of populations in natural envi-
ronments), the duration of exposure at various concentrations, the frequency
and degree of previous exposures to similar pollutants that may initiate either
tolerance or hypersensitivity to the offending agent, and the meteorologic
conditions under which exposure may take place. The last factor is often shown
to play an overwhelming role in determining the outcome of the challenge.
10-2
-------
Several mortality studies on different population groups have been
conducted, principally in the Los Angeles area. Studies by the California
Department of Public Health (reported in 1955, 1956, and 1957) showed a
marked increase in daily mortality among Los Angeles County residents aged
65 and older during a period of high photochemical oxidant concentrations in
a 2-week period in September 1955. An examination of temperatures during
this period showed that the increase in deaths occurred immediately after a
marked increase in temperature; mortality returned to normal before oxidant
concentrations had returned to those prevailing before the episode. Although
the photochemical oxidant concentrations were high immediately before,
during, and after the heat wave, the daily mortality decreased when temper-
atures dropped. During other periods when daily mortality in citizens over
65 was compared with both temperature and oxidant concentrations, no con-
sistent pattern could be discerned, nor could a pattern be seen at other times
when oxidants rose to medium and high concentrations without an accompanying
increase in temperature. It must be concluded that heat rather than photo-
chemical oxidant exposure, precipitated the increase in fatalities in the
population studied. Nevertheless, the possibility cannot be dismissed that
the concomitant high oxidant concentrations increased the death toll. Such
2
synergistic actions between air pollutants and weather are well known.
Heat has long been known to be one of the greatest stresses to which
an elderly person can be subjected, and heat waves in New York, as well
as Los Angeles, have been regularly shown to be followed by a tripling
or quadrupling of daily deaths among persons over 65, especially before
air conditioning became prevalent. Unfortunately, high temperatures are
often associated with high oxidant concentrations in the Los Angeles basin.
10-3
-------
In an attempt to isolate the effects of these two environmenta character -
3
istics Oechsli and Buechley studied the mortality associated -with three
Los Angeles heatwaves, in 1939, 1955, and 1963. It was assumed that
less photochemical oxidant pollution was present in 1939 (although no
measurements were made at that time), and yet there was an equally high
mortality among elderly persons in 1939 and 1955. Temperatures were
similar in each of the three heat waves. A lessened mortality was
observed during the 1963 heat wave, perhaps because of the increasing
use of air conditioning between 1955 and 1963. The authors concluded
that the high photochemical oxidant concentrations did not augment the
mortality effect of high temperatures.
Residents of nursing homes were a special group included in the
1
California Department of Public Health study. They were considered of
special interest because of the assumed presence of chronic illness in most
of them and their possible greater susceptibility to photochemical oxidant
pollution. All nursing homes in Los Angeles County containing 25 or more
beds were included, and daily mortality, transfer to a hospital because of
worsening disease, maximal daily temperatures, and the occurrence of smog-
3
alert days with ozone concentrations of 590 yg/m (0. 3 ppm) or higher were
considered. Again, the striking effect on mortality during heat waves was
noticed, but no correlation with smog-alert days could be demonstrated.
4
Massey, Landau, and Deane conducted a study on two synthetic
communities within the Los Angeles air basin. These communities, -with a
combined population of 944, 391 persons, -were divided into high-pollution
and low-pollution areas. The two areas had similar temperatures. The
mean number of daily deaths in the low-pollution area was subtracted from
10-4
-------
the mean number in the high-pollution area, and the difference was examined
by correlation and regression analyses with respect to differences in pollution.
The observers were unable to detect any significant correlation between
mortality and difference in oxidant, sulfur dioxide, or carbon monoxide content
in the ambient air.
Studying specifically the effect of pollutant concentrations on cardiac
5
and respiratory diseases in Los Angeles County, Hechter and Goldsmith
compared daily mortality from these causes with fluctuations in oxidant and
carbon monoxide concentrations and temperature. The authors removed the
statistical effect of season by fitting Fourier curves to the data, which were
presumed to be independent of season. When residua from the fitted curves
were analyzed, no significant correlations between pollutants and mortality
from cardiorespiratory diseases could be found. The authors also applied
lags of 1-4 days, but again were unable to demonstrate any significant cor-
relations. It is possible that some additive effect of pollutants on mortality
occurred but -would not be detected by this analysis.
Another attempt to compare cardiorespiratory deaths with photo-
6
chemical oxidant pollution was carried out by Mills, who compared seasonally
adjusted nursing-home deaths in Los Angeles with measures of photochemical
oxidant pollution. He found a suggestive positive association between photo-
chemical oxidant concentration and excess deaths when pollution rose
3
above 390 ug/m (0. 2 ppm). Although heat and. seasonal variability
were considered, the statistical analyses used make it questionable
whether their effect could be suppressed.
A variety of methods have been used to assess a relationship between
mortality from chronic illness and photochemical oxidant pollution, but none
has been able to demonstrate a clear-cut relationship. The possibility of a
10-5
-------
synergistic effect has not been ruled out, although the experience of
areas other than the Los Angeles basin with lower concentrations of
photochemical oxidant pollution suggests that temperature is an over-
whelming factor in these deaths.
Further studies on mortality in relation to photochemical oxidant
pollution are needed to delineate differences in susceptibility (especially
in children and the elderly), to assess the additive effects of various
weather conditions, to examine geographic variations in mortality in
relation to pollution, and to determine whether excess mortality is
attributable to specific diseases (e. g. , emphysema), which may have
been overlooked in examinations of total mortality. Populations should
also be more carefully categorized to determine whether specific sub-
samples are at greater risk.
HOSPITAL ADMISSIONS
Several studies have attempted to correlate increased numbers of
hospital admissions with variations in photochemical oxidant pollution.
1
The California Department of Public Health study of excess mortality
also investigated hospital admissions as a possible health indicator of
oxidant pollution. Admissions to Los Angeles County General Hospital in
September through December 1954 for childhood asthma, tuberculosis,
other respiratory diseases, and all other causes were examined. No
significant association with oxidant concentrations was found.
Two other investigators have attempted to relate hospital admis-
7, 8
sions to increased photochemical oxidant pollutants. Sterling et al.
studied admissions to Los Angeles hospitals for a 7-month period in
10-6
-------
1961. They grouped diseases into "highly relevant," "relevant," and
"irrelevant" categories. The "highly relevant" -were allergic disorders,
inflammatory diseases of the eye, acute upper respiratory infections,
influenza, and bronchitis. "Relevant" disorders included diseases of
the heart, rheumatic fever, vascular diseases, and all other respiratory
diseases. All other diseases were considered "irrelevant. " Because
both hospital admissions and photochemical oxidant concentrations
varied by day of -week, corrections for both-were introduced into the
analysis. Although there was a statistically significant correlation
coefficient between hospital admissions for "highly relevant" and
"relevant" conditions and photochemical oxidant pollution, the differences
were extremely smallT
Both "highly relevant" and "relevant" diseases showed some correlation
with carbon monoxide and ozone, and nitrogen oxides and particles
correlated with "highly relevant" diseases. Even if the relationships
claimed by this study are valid, they are small, and confirmation by
studies over a long period is needed.
9, 10
Brant and Hill also examined the number of patients who had
respiratory and cardiovascular diseases and were admitted to Los
Angeles County General Hospital for a 4. 5-month period in 1954.
These months--generally regarded as the "smog season"--included the
highest photochemical oxidant concentrations of the year. Because he
accepted into his study group only persons who had resided for at
least 3 years within 13 km of downtown Los Angeles and excluded
the extremely old and children under 9, the numbers he dealt with
were rather small for this brief period. Complex statistical analyses
10-7
-------
were used to compare admissions with photochemical oxidant pollution,
as measured at a monitoring station not quite 6 km from the hospital.
The methods used have been questioned by many competent statis-
ticians, and the claims of a significant correlation between periods
of photochemical oxidant pollution and hospital admissions are dif-
ficult to accept. Even more difficult to accept is the claim of a positive
correlation bet-ween high concentrations of photochemical oxidants and
hospital admissions 4 weeks later. No reasonable medical explanation
can be given for the latter correlation.
Studies to date have demonstrated an extremely weak correlation
(if any) between photochemical oxidant pollution and hospital admissions.
If such correlations do exist, observations must be carried out over
considerably longer periods with adequate provisions for controlling
confounding variables, such as meteorologic factors.
ACUTE RESPIRATORY INFECTION
The possibility that chronic exposure to photochemical oxidant
pollution alters host resistance and thus increases susceptibility to
acute respiratory infection is a challenging one. An opportunity to
examine this thesis occurred in 1968 and 1969, when an epidemic of
A2/Hong Kong influenza occurred in southern California. Pearlman
11
et al. had the opportunity to observe five southern California
communities that varied from high to low oxidant concentrations during
this period. Because other pollutants, especially oxides of nitrogen
and particles, have shown associations with influenza attack rates, an
association with photochemical oxidant pollution was carefully inves-
tigated. Pearlman ^t al. examined the morbidity among 3, 500
10-8
-------
elementary-school children in five communities. Although these
communities showed a definite gradient in chronic oxidant exposure,
there -was no significant difference in oxidant concentrations imme-
diately before or during the epidemic. Questionnaires to parents of
the children followed between November 1968 and January 1969 asked
about the presence of influenza-like illness or symptoms. Blood
specimens were later obtained from the children whose parents reported
upper respiratory symptoms. Titration was performed by hemagglu-
tination inhibition and complement fixation against A 2 influenza antigen.
Although more children reported illness in low-pollution cities, no
statistically significant difference in illness rates could be correlated
with exposure to chronic oxidant air pollution. Inasmuch as acute oxidant
concentrations were roughly similar in all five communities, it may be
that the children did not receive an oxidant dose sufficient to impair host
defense mechanisms immediately before or during their exposure to the
virus. In statistical manipulation, the investigators were able to minimize
other significant covariants, but concluded that "oxidant exposure. . . .did
not alter host defense mechanisms enough to cause morbidity differences. "
School absenteeism is known to be due in large part to acute
12
respiratory illness, so Wayne and Wehrle followed daily absenteeism
rates in schoolchildren in Los Angeles, but were unable to detect any
relationship between variations in ambient photochemical oxidant con-
centrations and school absenteeism.
In a long-term study, Hammer etal. recorded daily symptoms
in healthy young student nurses for a period of nearly 3 years (October
13
1961-June 1964). An average of 61 student nurses in two nursing
10-9
-------
schools in Los Angeles completed a daily dairy for 868 days on the
incidence of cough, chest discomfort, eye discomfort, and headache--
all symptoms that might be expected to accompany an acute respiratory
infection. Other recorded information included incidence of gastroin-
testinal symptoms, physician visits, restricted activity, and menses.
Daily maximal hourly concentrations of photochemical oxidants, carbon
monoxide, and nitrogen dioxide and daily temperatures were also measured
at monitoring stations within 2 miles of the schools. As expected, eye
discomfort showed the strongest correlation with photochemical oxidant
concentrations, with one-third of the total population reporting the symptom
when oxidant concentration reached 0. 5 ppm. However, cough and chest
discomfort also increased with maximalhourls oxidant concentration.
Headache showed a positive association with photochemical oxidant con-
centration, but the increase in the number reporting the symptom (3-8%)
was considerably less than for other symptoms. Temperature and carbon
monoxide and nitrogen dioxide concentrations could not explain the
associations found. Cigarette-smoking history, allergies, and bias in
reporting were supressed as variables in the analysis. It is of particular
interest that the authors were able to compute the thresholds of which the
prevalence of the symptoms began to increase and found them close to the
present U.S. national primary standard for photochemical oxidant, indicating
little or no margin of safety. The eye irritation threshold was calculated
3
at approximately 294 Mg/m (0. 15 ppm). Because these were all young
healthy adults, relatively free from chronic disease, the same effects in
elderly persons or in those with chronic heart or lung diseases could be
expected to result in greater physiologic embarrassment.
10-10
-------
Although the observed threshold for eye discomfort is comparable
•with reported results of human experimental exposure-chamber studies,
it is recognized that current methods for measuring photochemical
oxidants primarily measure ozone, •which is not known to be an eye
irritant. The authors therefore assumed that the measured concen-
trations of ozone reflected the concentrations of such known eye irritants
as peroxyacylnitrate, peroxybenzoylnitrate, formaldehyde, and acrolein--
all of which have been shown to be present in Los Angeles basin air.
However, the symptoms of cough, chest discomfort, and headache have
all been associated -with occupational exposure to ozone, so it is possible
that ozone itself is the offending agent for these symptoms. It is interesting
that the observed daily maximal hourly carbon monoxide concentrations
in this study -were below those which have been reported to cause headache
experimentally. Nevertheless, inasmuch as a significant number of
student nurses did report headache associated -with increased oxidant
concentration, an interaction between carbon monoxide and oxidants
cannot be excluded.
10-11
-------
AGGRAVATION OF PREEXISTING DISEASE
The best-documented health effect of general urban air pollution
is the aggravation of preexisting disease. In the notorious Donora
episode and in the many we 11-documented episodes of excess mortality
in London's "smogs," most of those who died had had marked impairment
of cardiac or pulmonary reserve. Similarly, the majority of epidemiologic
studies demonstrating an association of health impairment with increased
air pollution were carried out in areas where the atmosphere was
characterized by a particulate-sulfate (and preponderantly chemically
reducing) type of pollution. Several investigators have attempted to
determine whether similar health effects are produced by exposure to
atmospheres that have photochemical oxidants as the characteristic
pollutants.
14
Studies by Motley ^t al_. on 66 volunteers, 46 of whom had
pulmonary emphysema, were conducted in a "filtered room" from which
oxidants •were removed by activated-char coal filters. Pulmonary
function studies demonstrated improvement in emphysematous patients
who remained in the room for 40 h or more, if they had entered it on
a day when the ambient air in Los Angeles was considered "smoggy"
by the investigators and the Los Angeles Air Pollution Control District.
Normal subjects showed no change in pulmonary function in the filter ed-
air chamber, compared with measurements taken when they were
breathing ambient "smoggy" air. Emphysematous patients also showed
no improvement if they entered the room on a "nonsmoggy" day. The
study, although widely cited, is difficult to evaluate, because the
number of patients was relatively small. Some improvement was noted
10-12
-------
in the emphysematous patients who entered on "smoggy days" in vital
capacity, FEV , and maximal breathing capacity. The most marked
3
change, however, was a decrease in residual lung volume.
15
Remmers and Balchum used a specially constructed room at
Los Angeles County Hospital with an air-conditioning filter system
and filters that could be used at the discretion of the investigator to
remove photochemical oxidants and nitrogen oxides from ambient air.
Particulate matter could also be partially removed. They carried
out studies during September and October 1964 and from March to
November 1965. Pulmonary function studies were performed one or
more times a day during the approximately 1 week that each patient
spent in the room with no filtration and again for a week with
filtration. Temperature and humidity were kept constant in both cases.
Airway resistance, diffusing capacity, other pulmonary functions, blood
oxygen tension, and oxygen consumption were measured when the subjects
•were at rest and exercising. Examination of the data indicated that
airway resistance was affected by increased oxidant concentration over
3
a range of 100 - 450 ug/m (0.05 - 0. 23 ppm). Unfortunately, the
data are difficult to interpret, because many of the subjects were
cigarette-smokers, the subjects were exposed to ambient air con-
taining many substances in addition to oxidant, and the observed
improvement with filtered air may have been caused by the removal
of other pollutants, such as aerosols, aldehydes, and particles.
A more elaborate analysis of these data was carried out by Ury and
16
Hexter. It demonstrated that oxygen consumption, in most cases,
increased with oxidant concentration. Unfortunately,
10-13
-------
the oxidant concentration was measured only twice a day at a station
some distance from the site of the subjects' exposure. Oxidant was
also measured as ozone, so the concentrations of other irritant oxidant
compounds could not be determined.
17
A much larger group of men was followed by Shoettlin in an
attempt to study the long-term effects of community air pollution on
persons with and without symptoms of pulmonary disease. These two
groups were veterans who lived in the domiciliary unit and in the
chronic-disease annex of the Los Angeles Veterans' Administration
Center. A group of 528 veterans in the domiciliary unit who had no
symptoms of respiratory disease were used as the control population.
A group of 326 men -were selected on the basis of at least two symptoms
of respiratory disease for 2 years or longer. The symptoms included
cough, sputum production , shortness of breath, wheezing, and abnormal
breath sounds. The two groups were matched by age and smoking history,
and the resulting pairs were studied weekly by repeated pulmonary
function tests and response to a standardized respiratory-symptom
questionnaire. An analysis of variants showed no statistically significant
effects of air pollution on incidence or prevalence of respiratory symptoms
or on tests of pulmonary function. Nevertheless, the maximal oxidant
and oxidant precursor concentrations consistently accounted for more of
the variation in frequency of symptoms and clinical signs in the group
with pulmonary disease than in the control group. Up to 30% of the
variation in symptoms in the group with pulmonary symptoms appeared
to be correlated with the maximal oxidant precxirsor concentrations,
•whereas no association could be demonstrated in the control group.
10-14
-------
ASTHMA
Asthma, a. disease featuring sudden and dramatic variations
in respiratory symptoms and pulmonary function, is •well known to be
related to environmental factors in many cases. Many other factors,
however, may play a significant role in the precipitation of asthmatic
attacks, including meteorologic factors, emotional factors, infection,
allergy, and physical activity. It has also been demonstrated that
there is a significant ethnic variation in factors associated with acute
18
asthmatic attacks. Nevertheless, between 2 and 5% of the popu-
lation is subject to asthmatic attacks, so it has been examined as an
indicator of health effects of photochemical oxidant pollution.
19
Schoettlin and Landau carried out one of the earliest studies to
determine whether aggravation of asthma could be related to increases
in oxidant concentrations. They followed 137 asthmatics in Pasadena
with known asthma for at least 5 years. Over at least a 3-month
period in late 1956--the usual peak oxidant period of the year--
weekly reports were obtained from each patient as to the number of
attacks. Of the 3,435 attacks reported by these patients, less than
5% were spontaneously associated by the patient with "smog."
Although most reported attacks on days with high enough oxidant
concentrations to cause eye irritation and plant damage, the majority
of attacks occurred between midnight and 6:00 a.m., whereas peak
oxidant concentrations occurred between 10:00 a.m. and 4:00 p.m.
This lag, however, would not necessarily rule out a causative role of
oxidants in asthmatic attacks. The conclusion of the authors was that
only 8 of the 137 patients could be characterized as "smog reactors."
10-15
-------
20
The oxidant concentrations later reported by Renzetti and Marcus
•were a peak of 0. 25 ppm and, for the same period and same station,
a maximal hourly concentration of about 0. 02 ppm. It is of interest
that one-third of the attacks spontaneously associated with "smog" were
reported by a single patient. However, in spite of the small number
of people who spontaneously associated their attacks with "smog, "
this study suggests that there are probably some people who do
experience asthmatic attacks related to increased concentrations of
photochemical oxidants. Further studies to confirm this, sponsored
by the EPA, are underway in the Los Angeles air basin.
EFFECTS OF PHOTOCHEMICAL OXIDANTS ON HEALTHY POPULATIONS
Athletic Performance
21
Wayne ei^ al. related athletic performance of high-school
cross-country runners over a 5-year period from 1959 to 1964 to oxidant
measurements for the hour of the race and 1, 2, and 3 h before the
race. Temperature, relative humidity, wind velocity and direction,
and oxides of nitrogen were also considered, but showed no relation
to the running times. A "training effect" that might be expected to
improve performance on each succeeding race was also considered.
A significant relationship, however, was observed between high
oxidant concentrations and the percentage of runners whose performance
decreased, compared with their performances in the previous home
meet. It is of interest that the deterioration in performance of these
3
21 runners was noted beginning at 130 ug/m . With increasing oxidant
concentration, there was a manifest deterioration in team performance
10-16
-------
3
over a range of 60 - 590 Mg/m . This deterioration
in performance began well below the national photochemical oxidant
3
standard of 160 yg/m (0.08 ppm). The authors readily admitted
that "the observed effects may be more related to the lack of maximal
effort due to the increasing discomfort than to decreased physiologic
capability." Nevertheless, although they discussed the possibility
that decreasing performance might be due to the detrimental effect
of discomfort from eye irritation, the data provide convincing
evidence that some components of the air that were measured as
oxidant had an effect on team performance.
Although no threshold effect was specified by Wayne et al.
22
a later analysis by Hasselblad et al. suggested a threshold estimate
3
of 235 yg/m (0. 012 ppm). A similar study was carried out over a
23
shorter period by Koontz in Seattle, where oxidant concentrations
were approximately one-third those in Los Angeles. A decrease in
performance of long-distance runners was noted with increasing
oxidant concentrations, but these were also associated with marked
temperature increases, and it was impossible to separate their
relative contributions.
Automobile Accidents
Another association of oxidant concentrations with potentially
serious implications is the increase in automobile accidents noted by
24
Ury. He recorded accidents in each daylight hour of each weekday
in the "high-smog" 3-month period between August and November for
2 years and found a statistically significant relationship between oxidant
10-17
-------
concentrations and the number of automobile accidents. He was
unable to demonstrate a similar relationship with nitrogen dioxide.
Because the study compared hours -with presumably similar traffic
density, the likelihood that traffic density accounted for the association
is probably small. The data suggest that photochemical oxidant pol-
lution impairs driving performance, either directly by interfering with
oxygen transport or utilization or indirectly by causing eye discomfort
or respiratory irritation. It is also possible that other pollutants,
such as carbon monoxide emitted from the automobile tailpipe,
account for some or all of the excess accidents.
Discomfort
Additional evidence of an association of discomfort or more
severe health effects with increased oxidant concentrations was
published by the Committee on Air Pollution of the Los Angeles
25
County Medical Association. The organization circulated a
questionnaire to a sample of every sixteenth physician registered to
practice in the County. Although air pollution was not specifically
mentioned in the questionnaire, the fact that it was sponsored by an
air pollution committee probably suggested to the physicians that air
pollution was the principal environmental concern. The physicians
were asked how many patients they had advised to move from Los
Angeles County for health reasons before December I960. By
extrapolation from these questionnaires, it was estimated that over
10, 000 persons had been advised by their physicians to move from the
County for health reasons and, for two-thirds of these, air pollution
was given as the reason. Because this was a study of attitudes,it
cannot be categorically cited as indicative of a definite health effect.
10-18
-------
Pulmonary Function
Children have often been considered to be particularly sensitive
indicators of environmental challenge and therefore to constitute a group
in -which adverse health effects of air pollution might be detected at lower
concentrations than in adults. Two groups of elementary-school children
living in the Los Angeles basin were assessed twice a week by McMillan
26
et al. with a Wright peak-flow meter to measure ventilatory performance.
One group of 50 children lived in an area exposed to high oxidant concen-
trations, and the other group of 28 children lived in a less polluted area.
During 11 months of the study, no correlation could be found between acute
changes in oxidant concentration and ventilatory performance in either
group. Unfortunately, there were significant differences between the two
groups, in that the group in the more highly polluted area was ethnically
mixed and had an incidence of upper respiratory tract infection 3 times
greater than that reported in the other group. Pulmonary function studies,
as part of the Community Health Effects Surveillance Studies (CHESS)
program, are underway in seven communities with graduated concentrations
of photochemical oxidants in the Los Angeles basin. It is hoped that these
will yield more definitive results.
A similar study on the relations between pulmonary function and
27
exposure to photochemical oxidant pollution was carried out by Cohen et al.
To eliminate the effects of smoking, the study was confined to Seventh Day
Adventists who abstain from tobacco. They were divided into two groups:
one living in the San Gabriel Valley (a high-oxidant-pollution area), the
second living in San Diego, which was then considered to represent a
relatively low-pollution area. Each participant was
10-19
-------
interviewed by a physician, underwent a battery of pulmonary function
tests, and completed a standardized respiratory-disease questionnaire.
Daily maximal hourly average oxidant concentrations in the San Gabriel
Valley -were twice those in San Diego during the time of the study (San
3 3
Gabriel, about 274 \ig/m , or 0. 14 ppm; and San Diego, 137yg/m ,
or 0. 07 ppm). In spite of the marked difference between the oxidant
concentrations in the two areas, no significant differences could be
found in pulmonary function studies, the prevalence of chronic
bronchitis, or the occurrence of respiratory-disease symptoms, as
determined by the questionnaire. In this study, the differences may
have been due to the absence of cigarette-smoking in both groups;
some investigators have suggested that smoking is an additive factor
28
in the effects of ambient air pollution. It must also be noted that,
although the peak values of oxidant pollution in the more polluted
area were twice those in the less polluted area, the mean yearly
averages were essentially the same.
29
Kagawa and Toyama in Tokyo followed 20 normal 11-year-
old schoolchildren once a week from June to December 1972 with a
battery of pulmonary function tests. Environmental factors studied
included oxidant, ozone, hydrocarbon, nitric oxide, nitrogen dioxide,
sulfur dioxide, particles, temperature, and relative humidity.
Temperature was found to be the most important environmental
factor affecting respiratory tests. The observers noted that pulmonary
function tests of the upper airway were more susceptible to increased
temperature than those of the lower airway. Although the effect of
temperature was the most marked, ozone concentration -was significantly
10-20
-------
associated with air-way resistance and specific airway conductance.
Increased ozone concentrations usually occur at the same time as
increased temperature, so their relative contributions could not be
determined.
Eye Irritation and Lacrimation
Eye irritation and lacrimation are by far the most widespread
and common symptoms clearly associated with increased photochemical
oxidant pollution. Although photochemical oxidant is customarily
measured as ozone, ozone itself is not a primary eye irritant. Thus,
the eye irritation associated with increased photochemical oxidants
is probably due to some or many of the complex organic oxidants
31, 32
produced in photochemical "smog." Richardson and Middleton
noted nearly 20 years ago that eye irritation could be expected in a
considerable portion of the population when the oxidant concentration
3
reached 200yg/m
33
Renzetti and Gobran carried out a controlled study on two
groups of 20 female telephone-company employees working in adjacent
rooms for a period of 120 days. Filters to remove eye irritants were
switched periodically between the rooms, so that the two groups were
alternately exposed to test and control conditions. Subjects were
unaware of whether air was filtered or unfiltered at any given time,
but they consistently reported eye irritation when the oxidant concen-
3
tration exceeded 200 yg/m . Eye irritation has also
been previously cited as the most commonly reported symptom in the
13
student-nurse study of Hammer et al.
10-21
-------
That the problem of eye irritation in urban environments is not
34,35
confined to Los Angeles is indicated by the studies of McCarroll et al.
36
and Mountain et_ al_. on a population in the lower east side of Manhattan.
This population of approximately 2, 000 persons of all ages representing
the major ethnic groups of New York City was followed for a period of 3
years with weekly interviews. Participants were queried about the
occurrence of many different diseases, disease symptoms, aggravation
of preexisting diseases, and a variety of other health factors. Frequency
of reports of new eye irritation increased concomitantly with increases
in oxidant concentrations in the neighborhood. Exact oxidant concen-
trations could not be measured in the study, because of the presence
of high concentrations of interfering substances, including sulfur
oxides, particles, and carbon monoxide. Substances other than oxidants
might have contributed to the eye irritation reported by this population.
For the two most prevalent symptoms related to photochemical
oxidant exposure — eye irritation and lacrimation--no method of
quantification has been developed. Eye irritation, although undoubtedly
real, is a purely subjective response of the subject, and no measurement,
other than the complaint itself, has yet been developed. Similarly, a
routine objective measure of lacrimation remains to be developed.
However, studies on tears have demonstrated that, when a person
is experiencing eye irritation, the lysozyme content of the tears is
37
lower than normal. Measuring lysozyme content of tears or the
related pH variation appears promising, but more feasibility studies
are necessary before the usefulness of the method is known.
10-22
-------
A survey of the state of knowledge of eye irritation and
lacrimation in response to photochemical oxidant pollution was carried
out by Wilson of the Copley International Corporation for the Coordinating
38
Research Council. After reviewing the studies cited above and related
toxicologic work, the report concludes: "In many ways, the under-
standing of eye irritation produced by photochemical smog has not kept
pace with the understanding of other smog manifestations. Part of this
is no doubt due to the fact that air pollution control agencies are not
set up to collect data from human panels but rely exclusively on
instruments. If an objective measure were available for measuring
eye irritation, and if this measure were sensitive enough to be
useful below the threshold of most humans, then a straightforward
study could be done on natural smog."
Nevertheless, in spite of the many gaps in our knowledge of
the components that produce eye irritation, there is remarkable
uniformity in the findings of several epidemiologic studies cited, in
the prevalence of the symptoms as oxidant concentrations increase,
in the distress that oxidants cause the affected subjects, and in the
threshold concentration at which the symptoms appear (0. 15-0. 2 ppm).
PHOTOCHEMICAL OXIDANT POLLUTION AS A CAUSE OF CHRONIC
DISEASE
Several studies attempting to relate aggravation of preexisting
chronic disease to increases in photochemical oxidant pollution have been
discussed. The possibility has also been raised that photochemical oxidant
pollution plays a role in the initiation of some chronic diseases. In part,
this possibility was suggested by laboratory studies demonstrating some
10-23
-------
radi.omim.etic properties of ozone. Although ozone may mimic ionizing
radiation in some respects, it carries by no means all the carcinogenic
implications. Nevertheless, experiments have indicated chromosomal
39
damage to living cells by ozone and to human cells in vitro by organic
40 41
peroxides. Work of Palmer and colleagues has suggested that
ozone is a potential cocarcinogen--a finding that carries great impli-
cations during a time of increasing rates of human lung cancer.
To assess the possible contribution of photooxidant pollution
42
to lung-cancer mortality, Buell je_t a_l. carried out a prospective
study of lung cancer among 69, 160 members of the American Legion--
residents of Los Angeles County, the San Francisco Bay area, San
Diego County, and all other California counties. This study was
carefully adjusted for cigarette-smoking habits, occupation, and
duration of residence in the same county. Death certificates for the
first 5-year period were checked for mortality from cancer of the
lung and from other chronic lung conditions for a total of 336, 571
man-years of observation. As would be expected, residents of the
urban counties of Los Angeles, the San Francisco Bay area, and San
Diego had considerably higher mortality, both from lung cancer and
from other cronic pulmonary disease. Even when adjusted for
cigarette-smoking, these differences persisted, but they are compatible
with other observations on the well-known "urban factor" in increased
death rates from lung cancer, other cancers, and other chronic pulmonary
disease. When heavy smokers (more than one pack a day) were examined,
the relative risk of lung cancer was found to be greater in Los Angeles
County than in other areas of California. For nonsmokers, however,
10-24
-------
the rate in the San Francisco Bay area and San Diego County was
slightly higher than the rate in Los Angeles County. From these
data, it was not possible to demonstrate any effect of oxidant pollution
on lung-cancer mortality, if one assumes that in the years of observation
(i958-1963) oxilant concentrations were higher in Los Angeles. However,
because it is well known that the development of overt lung cancer
is an indolent process that takes many years, the period of observation
may not have been long enough to detect an environmental effect.
When the same observers examined mortality from chronic
respiratory diseases other than cancer of the lung, the death rates
were found to be somewhat higher in Los Angeles than in the San
Francisco Bay area and San Diego County, particularly among persons
•who had lived for 10 or more years in the same area. It is well
known, however, that socioeconomic class is an important factor
43
in mortality from chronic respiratory disease, and no data are
available to show such differences among the groups examined in this
study.
44
With standardized respiratory-survey techniques, Deane et al.
examined a. group of West Coast outdoor telephone-company employees
whose work and medical and social status were comparable with those
of similar groups examined on the East Coast, in the United Kingdom,
and in Japan. They noted that, in the group over 50 years old, respiratory
symptoms were more frequent in the Los Angeles and in the San
Francisco population than in the other areas studied. Twice as many
telephone-company workers in Los Angeles complained of persistent
cough and phlegm as in San Francisco. The groups were controlled
for smoking habits. Surprisingly,
10-25
-------
in spite of the difference in reporting of symptoms, there were no
important differences in the results of pulmonary function tests
between residents of the two areas in this occupational group.
50
These findings are at variance with those of Hackney, •who noted
seasonal differences, which were greater in San Francisco than in
Los Angeles.
DISCUSSION
The EPA is conducting a major study in the Los Angeles basin
on the effects of photochemical oxidants on health. It is a survey
of schoolchildren in seven communities representing a gradient of oxidant
exposure. In addition to comprehensive environmental monitoring data,
specific health characteristics will be followed, including chronic
respiratory disease in adults, lower respiratory disease in children,
acute respiratory disease in both children and adults, pulmonary function
in children, aggravation of asthma, irritation of mucous membranes,
and tissue residues of trace metals. Complete data from this study
will not be available for another 3 years, but data from the first 2
years may become available sooner.
A second study by the EPA will attempt to correlate the effects
of photochemical oxidants and cigarette-smoking in promoting chronic
respiratory signs and symptoms in cohorts of adolescents and their
families. Pulmonary function tests will be included, and this study
should do much to answer the vexing questions of the relationship of
chronic pulmonary disease and photochemical air pollution.
10-26
-------
The abovementioned studies are being carried out by the EPA
as part of the CHESS program. Although some of these studies have
produced useful information, others are apparently not fulfilling their
objectives. Specifically, these studies are designed entirely in-house
by full-time employees of the EPA at Research Triangle Park, North
Carolina. The studies -would have benefited by the presentation of
experimental design and proposals to knowledgeable and experienced
scientists outside the federal establishment for comment and criticism.
Furthermore, some of the information collected in past studies
and much that is now being collected is retained by the EPA to be
used ultimately in standard-setting, without first being subjected to the
scrutiny of the scientific community outside the federal government.
To date, there has been relatively little publication in the usual
scientific journals, and most data have been issued by the EPA in
the form of monographs; hence, external scientific input, although
sought, had little effect on the published scientific product. Because
most of these studies have been related to disease or symptom
prevalence, before-and-after studies of the effects of approved air
quality have been impossible to carry out. This criticism applies not
only to the CHESS studies, but to virtually all epidemiologic studies
cited in this chapter, inasmuch as adequate environmental monitoring
was rarely carried out in studies before the last decade. The
epidemiologists and statisticians undertaking the CHESS studies are
extremely competent and are supported by well-trained engineers,
chemists, and meteorologists. Personnel turnover, however, has
inevitably affected the continuity of direction of the program.
10-27
-------
In addition to these much-needed studies, others should be
designed to seek information on human populations on points already
raised by important toxicologic and clinical studies. Although
epidemiologists have been unsuccessful in relating infectious diseases
45
to oxidant pollution, Coffin and Garner showed that ozone exposure
before or after exposure to pathogenic bacteria strikingly increases
mortality in mice. They found that ozone not only affected host
resistance by inhibiting clearance rates, but also permitted uncontrolled
growth of streptococci. This and much other toxicologic evidence
that ozone interferes with host defense mechanisms in animals suggest
that a similar phenomenon may go unrecognized in humans.
41
The evidence that ozone is a potential cocarcinogen has grave
implications. If the radiomimetic properties of ozone are confirmed,
we may well be dealing with a nonthreshold dose-response situation in
which no standard can be considered to represent a completely innocuous
46,47
concentration of pollutant. The recent work of Bates and Hazucha
showing a synergistic effect of ozone and sulfur dioxide encourages the
belief that pollutants cannot be considered separately when standards
are promulgated and that the complex interrelationships among them
must be considered. It is important to know -whether other phenomena
48
well demonstrated in animals, such as tolerance, also occur in humans.
And there are suggestions that some type of cross-protection may occur,
whereby exposure to ozone provides some protection against other irritant
49
oxidants. Analogues for all these phenomena should be sought in human
populations, and methods should be devised for assessing their significance
for human health.
10-28
-------
RECOMMENDATIONS
Modification of the method in which the CHESS studies are
designed and in -which the data are displayed would add considerably
to their value. The scientific data collected in all the CHESS studies
should be made available through accepted scientific publications
to the scientific community as a whole.
The continuation of epidemiologic studies, including those of
the CHESS program, is vital to our understanding of the effects of air
pollution on health. There is no other way to determine the needed
dose-response (exposure-response) relationships between the complex
urban atmospheres and specific health effects. No animal or clinical
experiment can duplicate the full range of variables to be found in
ambient urban air. For this reason, all necessary support should
be given to qualified scientists to conduct epidemiologic studies
designed to answer these questions. Although such studies are
expensive and time-consuming, the data they produce can be produced
in no other way and are essential in the development of useful air
quality standards.
It is important to know whether such phenomena as tolerance
and cross-protection, well demonstrated or suggested in animals,
occur in man. Analogues for all these phenomena should be sought
in human populations, and methods should be devised for assessing
their significance for human health.
10-29
-------
REFERENCES
la. California Department of Public Health. Clean Air for California. Initial
Report of the Air Pollution Study Project. Berkeley: California
Department of Public Health, March 1955. 57 pp.
lb. California Department of Public Health. Clean Air for California. Second
Report of the California Department of Public Health. Berkeley: Califo
nia Department of Public Health, March 1956. 23 pp.
lc. California Department of public Health. Report III ... A Progress Report od
California Department of Public Health. Berkeley: California Depart-
ment of Public Health, Feb. 1957. 32 pp.
2. McCarroll, JT, and W7 Bradley. Excess mortality as an indicator of health
effects of air pollution. Amer. J? Public Health 56:1933-1942, 1966.
3. Oechsli, P. W. , and R. W. Buechley. Mortality During Hot Spells in Los
Angeles and Orange Counties, 1939-1963. Public Health Service Con-
tract 85-65-20, 1965. (UNVERIFIED)
/t. Massey, F. J., E. Landau, and M. Deane. Air pollution and mortality in
two areas of Los Angeles County. Biometrics 18:263, 1962. (abstract)
5- Hechter, H^H., and J." R." Goldsmith. Air pollution and daily mortality. Ame:
J?Med. Sci. 241:581-588, 1961.
f Mills, C. A. Respiratory and cardiac deaths in Los Angelas smogs. Amer.
J. Med. Sci. 233:379-386, 1957.
7. Sterling, T." 1)7, JT J. Phair, s. V? Pollack, D» A. Schumsky, and I. DeGroot.
Urban morbidity and air pollution. A first report. Arch. Enviroi*. Heall
13:158-170, 1966.
8. Sterling, Tf Df, ST Cf Pollack, and J." J." Phair. Urban hospital morbidity and
air pollution: A second report. Arch. Environ. Health 15:362-374, 1967
10-30
-------
9 Brant, J." W.'A. Human cardiovascular diseases and atmospheric air pollution ii,
Los Angeles, California. Int. J. Air Water Pollut. 9:219-231, 1965.
I0. Brant, J." Wf A.", and S." R? C'f HiU. Human respiratory diseases and atmospheric
air pollution in Los Angeles, California. Int. J? Air Water Pollut. 8:
259-277, 1964.
n Pearlman, M. E., J. P. Finklea, C. M. Shy, J. Van Bruggen, and V. A. Mewill.
Chronic oxidant exposure and epidemic influenza. Environ. Res. 4:129-
140, 1971.
12 Wayne, W." S.", and P.' Pf Weh'rle. Oxidant air pollution and school absenteeism.
Arch. Environ. Health 19:315-322, 1969.
j. Hammer, D.~ I., V." tlasselblad, fi." Portrtoy, and r.'ttehrle. Los Angeles student
nurse study. Daily symptom re-porting and photochemical oxidants. Arch.
Environ. Health 28:255-260, 1974.
]/t Motley, H.""!.", R." H." Smart, and C.~ T." Leftwich. Effect of polluted Los Angeles
air (smog) on lung volume measurements. J.A7K.A. 171:1469-1477, 1959.
15. Remmers, J. E., and 0. J. Balchum. Effects of Los Angeles Urban Air Pollu-
tion Upon Respiratory Function of Emphysematous Patients. The Effect
of the Microenvironment of Patients with Respiratory Disease. Paper
No. 65-43 Presented at the 58th Annual Meeting of the Air Pollution
Control Association, Toronto, Canada, June 1965. 17 pp.
16. Uty» H* K-» artd AT C." Hexter. Relating photochemical pollution to human physio-
logical reactions under controlled conditions. Statistical procedures.
Arch. Environ. Health 18:473-480, 1969.
17- Schoettlin, C. The health effect of air pollution on elderly males. Amer. Rev,
Resp. Dis. 86:878-897, 1962. ' .. .
18. Earnest, M., R." Bernal, S. Greenbaum, T. Logio, 2. Pollard, B. "Weisz, and J.
McCarroll. Emergency clinic visits for asthma. Public Health Rep. 81:
911-918, 1966.
10-31
-------
19. Schoettlin, C.' E.', and E. Landau. Air pollution and asthmatic attacks in the
Los Angeles area. Public Health Rep. 76:545-548, 1961.
20. Renzetti, N. A., Ed. An Aerometric Survey of the Los Angeles Basin,
August-November, 1954. Air Pollution Foundation Technical Report No. 9.
San Marino, Calif.: Air Pollution Foundation, 1955. 334 pp.
21. Wayne, W. S. , P. F. Wehrle, and R. E. Carroll. Oxidant air pollution and
athletic performance. J.A.M.A. 199:901-904, 1967.
22. Hasselblad, V., G. Lowriraore, W. C. Nelson, J. Creason, and C. J. Nelson.
Regression Using "Hockey Stick" Functions. Durham, N. C.: U. S. Depart-
ment of Health, Education and Welfare. Public Health Service. En\iron-
mental Health Service. National Air Pollution Control Administration.
(in-house report, 1970.)
23. Koontz, C. H. Oxidant air pollution and athletic performance: A study in
Seattle. Submitted to Department of Preventive Medicine, University
of Washington, September 26, 1968.
2/j Ury, H. K. Photochemical air pollution and automobile accidents in Los
Angeles. An investigation of oxidant and accidents, 1963 and 1965.
Arch. Environ. Health 17:334-342, 1968.
25. Physician Environmental Health Survey: A Poll of Medical Opinion. Los
Angeles County Medical Association and Tuberculosis and Health Associa-
tion. Los Angeles, May, 1961.
26. McMillan, R." ST, D." HT Wiseman, B. Hanes, and P." FT Wehrle. Effect of oxidanfc
air pollution on peak expiratory flow rates in Los Angeles school children.
Arch. Environ. Health 18:941-949, 1969.
27- Cohen, C. AT, AT RT Hudson, J.' L.' Clausen, and J.~ H.' Knelson. Respiratory symp-
toms, spirometry, and oxidant air pollution in nonsmoking adults. Atner.
Rev. Resp. Dis. 105:251-261, 1972.
10-32
-------
28. Freeman, G., L. T. Juhos, N. J. Furiosi, R. Mussenden, R. J. Stephens,
and M. J. Evans. Pathology of pulmonary disease from exposure to
interdependent ambient gases (nitrogen dioxide and ozone). Arch.
Environ. Health 29:203-210, 1974.
29. Kagawa, J., and T. Toyama. Photochemical air pollution. Its effects Ort reS-
piratory function of elementary school children. Arch. Environ. Health
30:117-122, 1975.
30. Pearlman, M. E., J. F. Finklea, C. M. Shy, J. Van Bruggen, and V. A. Netfill.
Chronic oxidant exposure and epidemic influenza. Environ. Res. 4:129-
140, 1971.
3]- Richardson, M. A., and W. C. Middleton. Evaluation o£ Filters for Removing
Irritants From Polluted Air. University of California. Department
of Engineering Report No. 57-43. Los Angeles: University of California,
1957. 31 pp.
32. Richardson, N. A., and W. C. Middleton. Evaluation of filters for Removing
irritants from polluted air. Heat. Pip. Air Condition. 30(11):147-154,
1958.
33- Renzetti, N. A., and V. Gobran. Studies of Eye Irritation Due to Los Angeles
Smog, 1954-1956. Air Pollution Foundation MR-4. San Marino, Calif.:
Air Pollution Foundation, 1959.
- • • I * i - - ~ " ' " "
3^. McCarroll, J. R., E. J. Cassell, W. Ingram, and D. Wolter. Health and the
urban environment. Air pollution and family illness: I. Design for
study. Arch. Environ. Health 10:357-363, 1965.
35- McCarfoll, J., Ek~ J," Cassell, D." Vt. Wolter, J." D. Mountain, J." RT Diamond, and
17 M7 Mountain. Health and the urban environment. V. Air pollution and
illness in a normal urban population. Arch. Environ. Health 14:178-184,
1967.
10-33
-------
36. Mountain, I/M., E. J. Cassell, D.~ W." Walter, J." D. Mountain, J." R." Diamond, si
J. R. McCarroll. Health and the urban environment. VII. Air pollution <
disease symptoms in a "normal" population. Arch. Environ. Health 17:
343-352, 1968.
37. Sapse, A. T. , B. Bonavida, W. Stone, Jr., and" E. E. Sercarz. Human
tear lysozyme. III. Preliminary study on lysozyme levels in
subjects with somg eye irritation. Amer. J. Ophthalmol. 66:76-
80, 1968.
og^ Wilson, K. W. Survey of Eye Irritation and Lachrymation in Relation to Air
Pollution. Final Report. La Jolla, Calif.: Copley International
Corporation, 1974. 62 pp.
, ft f
39 _ Petner, R. 11. Chromosome breakage in Vicia faba by ozone. Nature 181:
504-505, 1958.
LO Fetner, R. H. Ozone-induced chromosome breakage in human cell cultures.
Nature 194:793-794, 1962.
/H. Palmer, M. S., R. W. Exley, and D. I. Coffin. Influence of pollutant
gases on benzpyrene hydroxylase activity. Arch. Environ. Health
25:439-442, 1972.
j,2. Bueli, P., J," ET Dunn, Jr., and L." Breslow. Cancer of the lung and Los Angeles
type air pollution. Prospective study. Cancer 20:2139-2147, 1967.
i\J>. Winkelstein, W., Jr., S^'Kantot, E.~ W." Davis, CT S." Maneri, and tj." ET MosKet.
The relationship of air pollution and economic status to total mortality
selected respiratory system mortality in men. I. Suspended particulates
Arch. Environ. Health 14:162-171, 1967.
kb. Deane, M., JT RT Goldsmith, and D." Tuma. Respiratory conditions in outside
workers. Report on outside plant telephone workers in San Francisco and
Los Angeles. Arch. Environ. Health 10:323-331, 1965.
10-34
-------
45. Coffin, D. L., and D. E. Gardner. Interaction o£ biological agents and chem-
ical air pollutants. Ann. Occup. Hyg. 15:219-234, 1972.
46. Bates, D., and M. Hazucha. The short-term effects of ozone on the human
lung, pp. 507-540. In National Research Council.. Assembly of Life
Sciences. Proceedings of the Conference on Health Effects of Air
Pollutants, October 3-5, 1973. Senate Committee on Public Works Print
Serial No. 93-15. Washington, D. C. : U. S. Government Printing
Office, 1973.
i ( • . .
47. Hazucha, M., and D. V. Bates. Combined effect of ozone and sulphur dioxide
on human pulmonary function. Nature 257:50-51, 1975.
48. Stokinger, H. E., and L. D. Scheel. Ozone toxicity. Immunochemical and
tolerance-producing aspects. Arch. Environ. Health 4:327-334, 1962.
49. Stokinger, H. E., W. D. Wagner, and 0. J. Dobrogorski. Ozone toxicity
studies. III. Chronic injury to lungs of animals following exposure
at a low level. A.M.A. Arch. Ind. Health 16:514-522, 1957.
50. Hackney, J. Final Report to California State Air Resources Board on Contract
No. N01-HR3-2901. Smoking and Chronic Airways Obstruction., 1975.
(UNVERIFIED)
10-35
-------
Chapter 11
PLANTS AND MICROORGANISMS
The intent of this chapter is to give a critical review of all research
related to the effects of photochemical oxidants, including ozone and the
peroxyacylnitrates, on plants and microorganisms.
Injury to vegetation -was one of the earliest indicators of photochemical
369
air pollution. Injury was first observed in the Los Angeles area in 1944.
Since then, there has been a slow but steady increase in research efforts to
understand the effects of these pollutants on vegetation. In the late 1960's
and early 1970's, there has been a flood of published information.
In attempting to understand the effects of pollutant-pathogen interactions,
investigators looked at the effects of oxidant pollutants on individual micro-
organisms and on these organisms as they infected host plants. Ozone has been
tried as a fumigant to protect stored plants and plant parts against infection
by parasitic and saprophytic fungi and bacteria. Research on ozone as a
sterilant for water supplies and sewage systems is also related to effects on
bacteria. Some studies have simply used bacteria as models for the action of
ozone in biologic systems.
The chemical composition of the photochemical oxidant complex is dis-
cussed in Chapter 2. The major phytotoxic components are ozone, nitrogen
dioxide, and the peroxyacylnitrates. The latter homologous series of compounds
includes peroxyacetylnitrate (PAN), peroxypropionylnitrate (PPN), peroxybutyryl-
nitrate (PBN), peroxyisobutyrylnitrate (PisoBN), and peroxybenzoylnitrate
(PBzN). The first four of these are known to be toxic to plants, but only PAN
and PPN have been reported in sufficient quantities in ambient air to cause visible
-------
506
symptoms. The effects of the nitrogen oxides (NO ) are included in
80 x
another NAS report. Discussion of the quantitative effects of ozone
and PAN will be limited to laboratory and controlled field exposures,
because, under ambient conditions, the effects of these compounds are
difficult to differentiate. Although ozone is, quantitatively, the primary
oxidant component of photochemical air pollution, the term "oxidant" is used
to include ozone and PAN in discussing biologic effects under ambient conditions.
However, some studies suggest that phytotoxicants in addition to ozone and
209
PAN are present in the photochemical complex. Regardless of the number
of phytotoxicants present, ozone is the most important, it has received the
greatest amount of study, and its effects are better understood. The major
thrust of this chapter covers research with ozone.
225,461 496
Before ozone and PAN were identified as specific phytotoxic
components of the photochemical complex, researchers used a number of
artificial chemical reaction systems to simulate the ambient photochemical
oxidant situation. These efforts involved a number of irradiated and non-
irradiated reaction systems (unsaturated hydrocarbon-ozone mixtures,
unsaturated hydrocarbon-NO mixtures, and dilute auto exhaust). Most
x
research before I960 involved one or more of these reaction systems. This
102, 103, 132, 209,210, 215, 365, 368,401, 505,
research has been well reviewed
515,553
and thus is not extensively covered here. Although the work is dif-
ficult to correlate with research on individual pollutants or combinations of
pollutants, many of our present concepts were first enunciated on the basis
of these photochemical oxidant simulation systems. Any researcher con-
cerned with the effects of oxidant pollutants on vegetation or microorganisms
should be familiar -with this early work.
11-2
-------
A number of reviews of varied quality cover general or special
515
effects of photochemical oxidants on vegetation (Table 11-1). Thomas
fairly comprehensively covered the available information on the effects of
365
photochemical oxidants on plants. Middleton gave the first comprehensive
coverage of the phytotoxic effects of photochemical oxidants in 1961. A
453
number of excellent reviews have appeared since 1961. Rich presented
131, 132
an early review of ozone effects. Dugger and associates presented
210
the physiologic and biochemical effects of oxidants on plants. Heck
196
covered factors that influenced the expression of oxidant damage. Heagle
discussed oxidant problems with respect to interactions between air pol-
lutants and plant parasites. Three chapters in the air pollution atlas
215,235, 510
(Recognition of Air Pollution Injury to Vegetation; A Pictorial Atlas)
stressed components of the photochemical oxidant complex in terms of symptom
447
development and relative susceptibility of plants. Reinert et aj.. presented
an excellent treatment of interactions between several of the photochemical
oxidant pollutants and sulfur dioxide. The American Phytopathological Society
12
published a glossary of terms that should be useful to any research worker.
In addition, several recent review articles have discussed the effects of
211,223, 505,567
photochemical oxidants or ozone on vegetation. Three
recent books on air pollution effects on vegetation cover subjects of concern
128a,390, 398
to anyone interested in the photochemical oxidants. There
are two criteria documents: one for the Canadian Ministry of the Environ-
318
ment in 1975 and the other for the former U. S. National Air Pollution
401
Control Administration in 1970. Both focus on the development of criteria
useful for the setting of ambient air quality standards. These two reviews
pertain primarily to dose-response effects and attempt to define threshold
11-3
-------
Table 11-1
Selected Review Articles - A Subject Listing
Subject
References
General
Criteria documents
Symptoms and susceptibility
Photochemical oxidants
Ozone
PAN
Physiologic and biochemical
Effects of various factors
Plants as monitors
Glossary of terms
51, 101, 103, 128a, 175, 211, 222,
223, 251, 317, 351a, 364, 365, 367,
368, 390, 398, 505, 515, 516, 517,
565, 566, 571, 584
318, 401
215, 235, 475, 510, 515
103, 215
235, 390, 453, 567
79, 390, 510
128a, 131, 132, 390
196, 210, 447
28, 209
12
11-4
-------
dose or specific concentration and time combinations that produce specific
response measures. Neither document contains sufficient information on
microorganisms to enable the development of useful dose-response information.
318
The Canadian review is generally more comprehensive than the U. S.
401
document, in that it presents a threshold dose-response curve for
use with ozone and, by implication, with ambient oxidant measurements.
RESPONSES OF VASCULAR PLANTS
Injury to vegetation from photochemical oxidants was first characterized
369
in 1944 as a glazing, silvering, or bronzing of the lower leaf surfaces
of broadleaved plants. These symptoms were first identified in the Los
Angeles area, but were soon recognized over a large segment of southern
367
California and in the San Francisco Bay area.. Photochemical oxidants
are known to injure plants in most, if not all, major metropolitan areas
of the United States, Canada, and Mexico and probably affect vegetation in
major metropolitan areas throughout the world.
Ozone is generally recognized as the most important phytotoxicant
300
in the oxidant complex. Early studies were reported in 1864, The
285a
phytotoxicity was firmly established in 1914, and this was confirmed
246
in laboratory studies in 1937. It was first shown as a phytotoxic component
461
(causing grape stipple) of the oxidant complex in 1958 and later as the
225
cause of weather fleck of tobacco. Ozone is now known to cause
injury to a multitude of broadleaved plants and to explain several types of
needle injury in both eastern and -western conifer species.
11-5
-------
496
The peroxyacylnitrates were first identified in 1961 as the primary
cause of the undersurface glazing and bronzing on some broadleaved plants.
PAN has since been implicated in numerous pollution episodes in southern
California. Its importance in other metropolitan and rural areas in the
United States and throughout the world is uncertain, although symptoms have
428
been reported elsewhere. This is because oxidant concentrations in
other parts of the world are much lower than those reported in California,
and monitoring networks have not looked for PAN or its homologues.
436
The report by Penkett £t al_. is the first to come from Europe.
Research on photochemical oxidants including ozone was confined
primarily to California during the 1950's. By 1959, ozone was known to
be an important pollutant in the eastern United States and southern Canada.
It is now known as a ubiquitous pollutant and has been widely studied through-
out the United States and Canada. By 1972, several other countries had
recognized the potential effects of photochemical oxidants on vegetation and
initiated research.
We shall stress three areas of methodology that are of special concern
for the study of air pollution effects on vegetation: growth of the test organisms,
exposure facilities, and instrumentation. First, to determine the effects of
air pollutants on many plant species, one must have a good understanding of
the best cultural conditions for a given test crop; some results reflect the
use of poor test specimens. Second, dynamic air-flow designs are required
in chamber construction and exposure conditions must be similar to those
•which occur in the field. The method of preference would be a dynamic,
218
single-pass system, to avoid reactions of reactive oxidants with materials
of chamber construction or emanations from the plants. Several useful chamber
11-6
-------
24,204,232,332, 592
designs have been reported in the literature.
For routine experiments, temperature, light, and relative humidity should
approach ambient conditions, and nutrient status should be conducive to
good growth. Third, one should not assume instrument accuracy without
adequate calibration, either initially or later. Most plant scientists have
used the Mast oxidant instrument to measure ozone and ambient oxidants.
One should be aware of the inherent variability among instruments and
routinely calibrate them. Calibration of all instruments should be with the
EPA standard 1% neutral potassium iodide method, and the values should
be so reported. When this is not done, the actual values may be 50-100%
greater than the reported values. Most papers do not state the calibra-
tion procedure, if any, and some do not mention the monitoring instrument.
Investigators who use the Mast instrument over long periods without an
adequate maintenance program may also report erroneous values. Cali-
bration and instrumentation problems are reviewed in Chapter 6. For
3
comparison, ozone at 1 ppm is equivalent to ozone at about 1, 960 yg/m .
The foliar response of plants is discussed in terms of the visible
or subtle effects on individual plants. Visible effects may be defined as
identifiable, pigmented, chlorotic, or necrotic foliar patterns
that result from major physiologic disturbances. Subtle effects do not produce
visible injury, but may include transitory metabolic disturbances, such as
changes in rates of respiration, photosynthesis, transpiration, and enzymatic
processes. Subtle effects may be measurable in terms of growth or long-term
biochemical changes. Both visible and subtle effects are induced by physiologic
and biochemical changes in the plant. Subtle changes may also affect repro-
ductive or genetic systems. If cumulative changes occur within individual
11-7
-------
plants as a result of visible or subtle effects, these changes may affect plant
populations and communities, and this could have adverse effects on eco-
194,568
systems. Community and ecosystem responses are discussed and
quantified in Chapter 12.
In general, the direct response of plants to all oxidant pollutants
has been in the foliage. In several cases of long-term exposure (grape-
fruit after several months of exposure to ambient oxidants) or high ozone
371 490
concentration over a shorter period (apple, peach ), injury has
been reported on fruit itself.
Visible Symptoms
Visible symptoms are useful in characterizing the response of vegeta-
565
tion to a variety of stresses, including air pollution. Similar symptoms,
induced by different stresses, have been well described and may confuse the
60,227,235
diagnosis. On the basis of studies to date, diagnostic techniques
that use indicators other than visible injury (e.g., respiration) are less
reliable than the subjective judgment of an experienced observer. Thus,
it is important that researchers become familiar -with injury symptoms
caused by oxidants and those caused by other stresses. This section briefly
describes the injury symptoms used for diagnostic purposes.
The terms "acute injury" and "chronic injury" are often confused with
"acute exposure" and "chronic exposure. " Their historical use and the need
for brief descriptive terminology suggest that they are still useful terms.
Acute injury may affect only a small part of a given leaf. It is a result of
destruction of cell contents and always causes cell death. The necrotic
patterns in acute injury may be characteristic of a given oxidant. These
11-8
-------
patterns at least demonstrate the presence of a chemical toxicant. Acute
injury is usually associated -with short exposures (hours) to specific oxidants
or pollutant mixtures at concentrations that cause acute injury and usually
appears within 24 h after exposure. Chronic injury, whether mild or severe,
is usually associated with long-term or intermittent exposures to low con-
centrations of oxidants that do not produce acute injury. Normal cellular
activity is disrupted, and the chlorosis or other color or pigment change that
follows may eventually cause cell death. Chronic oxidant injury patterns are
generally not characteristic and may be confused with symptoms caused by
normal senescence, biotic diseases, insects, nutritional disorders, or other
environmental stresses. These patterns may appear as early leaf senescence
with or without leaf abscission. Repeated short-term exposures to ozone
may cause physiologic changes that are responsible for chronic symptoms.
However, such exposures may produce small but additive amounts of acute
injury that are mistakenly referred to as chronic injury.
Before the identification of ozone and PAN as two major phytotoxic
oxidants in photochemical air pollution, simulated "smog" (a variety of chemical
mixtures) and ambient pollution were the test atmospheres used. The most
complete morphologic and developmental studies were conducted during
35-38, 60, 179
this time by Bobrov (Glater) and associates. These were
classic studies that covered a range of plant species, including table beet,
annual bluegrass, oat, and tobacco. From these early studies has come our
basic understanding of microscopic changes and developmental patterns.
These workers first suggested that membrane injury may have led to the
initial effects on the chloroplasts. They also defined developmental patterns
and showed that leaves near maximal expansion were more sensitive than
11-9
-------
young leaves (or leaf tissue) or older leaves. They suggested that maximal
sensitivity -was related to stomatal function, volume of intercellular spaces,
and the extent of suberization of mesophyll cells. Other work has since
148,361, 524, 529, 542
substantiated their studies.
60
Bystrum _et al. first described morphologic changes in leaf surface
waxes of table beet exposed to photochemical oxidants; these changes were
different from those associated with aphid feeding. Comparison of oxidant
injury with that produced by insects has since received attention from
227
Hibben, who found that ozone injury to the leaves of four tree species
produced smaller flecks, randomly spaced and darker than fleck injury
along veins induced by a mesophyll-feeding leafhopper.
Although ozone and PAN are considered the two primary phytotoxic
oxidants in the photochemical complex, the specific response of plants to
many simulated atmospheres suggests the existence of other phytotoxic
209
oxidants. The symptoms associated with many of these reactant mixtures
208,215
are closely related to those caused by ozone and PAN. In some tests,
the mixtures used would not have produced either ozone or PAN. In other
cases, leaf age or the pattern of injury on sensitive test plants suggested
one or more pollutants other than ozone or PAN. Field injury symptoms
often resemble those reported for ozone or PAN, but the response pattern
is sufficiently different that accurate diagnosis is difficult. Brennan
50
et al. correlated development of oxidant symptoms with aldehyde con-
centrations in New Jersey and suggested that aldehyde may be a major
phytotoxic component of the photochemical oxidant complex. The symptoms
were probably not responses to the aldehyde, but rather to some compound
237a
or group of compounds present under the same conditions as the aldehyde.
11-10
-------
The most complete description of ozone injury symptoms is found
235
in the Atlas. However, several of the review articles, including the
318,401
two criteria documents, have injury descriptions. A concise
211
description is found in Heck and Brandt.
The classic ozone symptoms on angiosperms are the upper surface
225 461
fleck of tobacco and stipple of grape. These classic symptoms were
described in plants with differentiated mesophyll and are especially significant,
because they were identified with palisade cells, and not with spongy cells.
The two classic symptoms are still more widely associated with the
response of dicotyledonous plants to ozone than are other symptoms. Many
plants (e. g. , pinto bean, cucumber, tomato, soybean, and sycamore) may have
the entire upper surface covered with a bleached appearance as a result of
ozone exposure, with no observable injury on the lower surface. On closer
examination, the bleached area is seen to be made up of many small groups
of palisade cells that are dead and contain no pigment. In other plants or
under different conditions, the palisade cells may accumulate dark alkaloid
pigments (stipple) coincidentally with cell death. After exposure to higher
ozone concentrations or after longer periods of exposure, injury extends
to the spongy cells, producing bifacial necrosis. Plants exposed to a high
concentration of ozone or to a high concentration of ambient pollution during
a pollution episode usually develop dark watersoaked areas in the leaf within
a few hours. Leaves may show partial recovery, or these areas may form
light-tan bifacial necrotic lesions within 24-48 h. Individual lesions may
be small, but groups of them can extend and affect a considerable portion
of the leaf.
11-11
-------
In monocotyledonous plants (grasses and cereals) and some others,
there is no division of mesophyll tissue, and injury normally appears as a
35
bifacial fleck. Some plants, after extended exposure to low concentrations
of pollution (either continuously or intermittently), produce chlorotic patterns
that may be distinctive of oxidant pollution or similar to symptoms of normal
senescence. The early senescence seen in some plants may be a result of
long-term exposure to ambient oxidants.
The foregoing discussion is not descriptive of effects noted in con-
iferous trees, such as pine. It is -worth discussing two classic oxidant (ozone)
syndromes of pine--one eastern, the other •western. Ozone is the probable
23
cause of emergence tipburn in -white pine (white pine needle dieback). The
injury is characterized as a tip dieback of newly elongating needles and occurs
throughout the range of eastern white pine. Affected trees are found at random
in a stand, and symptoms develop in discrete episodes in successive years.
Primary roots of affected trees often die after repeated needle injury.
85
Costonis and Sinclair reported silvery or chlorotic flecks,
chlorotic mottling, and tip necrosis of needles as results of ozone exposure.
314
Ozone may be associated with semimature-tissue needle blight (SNB), but
315
Linzon found that both SNB-sensitive and SNB-tolerant-white pine were first
injured -with ozone at about 0. 6 ppm for 2 h, and the symptoms were not like
315
SNB. Linzon found that ozone injury began in young tissue -with newly functional
313
stomates, whereas in SNB the necrosis begins in semimature leaf tissue
and then spreads through the older needle tissue toward the tip. Needle
injury resulting in a disease called "chlorotic decline" of ponderosa pine
426
was first noticed in 1953 and was related to oxidant air pollution by 1961.
The chlorotic decline was characterized by a progressive reduction in terminal
11-12
-------
and diameter growth, retention of only the current season's needles, reduc-
tion in number and size of these needles, yellow mottling of the needles,
deterioration of the primary roots, and eventual death of the tree. The
425
chlorotic decline was not associated with stresses other than ozone.
These symptoms were reproduced by exposing ponderosa pine to ozone at
380
0. 5 ppm for 9 h/day for 9-18 days. Similar symptoms were noted by
462
Richards £t al_. , who called the disease "ozone needle mottle of pine."
149,150,151 374
Evans and Miller and Miller and Evans have conducted
histologic investigations on injury development in ponderosa pine. They found
that chlorotic needle mottle caused by ozone or ambient oxidants was easily
374
distinguished from "winter fleck. " A comparison of needle anatomy in four
pines of differing sensitivity suggested that sensitivity was related to the
150
number of mesophyll cells per stomate. They also reported an accumulation
of chloroplasts and carbohydrate stain in peripheral portions of mesophyll
cells of ponderosa needles before development of visible injury that was
149
not related to stomatal presence. These changes were not shown sufficiently
151
to be specific for ozone effects.
Injury from PAN was first described as smog injury by Middleton
369
ei^ al_. on spinach, garden beet, romaine lettuce, and chard. They
reported a collapse of spongy mesophyll tissue with the development of large
air pockets, especially near the stomates. The air spaces gave the leaf the
appearance of a glaze and were responsible for this classic PAN symptom.
35-38,60, 179
Most of the descriptive work reported by Bobrov and associates
from simulated atmospheres and ambient exposures resulted from PAN
injury. The classic injury pattern for PAN is glaze followed by a bronzing
of the lower leaf surface. Young expanding leaves are normally more
11-13
-------
sensitive to PAN than more mature leaves. Physiologic maturity is
important, as shown by the banding appearance on many susceptible leaves
that do not mature uniformly. If the -whole leaf has a similar physiologic
age, it may be uniformly injured (e. g. , pinto bean). In case of severe
injury, bifacial necrosis can occur. Early senescence and leaf abscission
are often associated with PAN injury. The most complete description of
510
injury is that by Taylor and MacLean. Symptoms associated with PPN
and PEN are similar to those for PAN.
79, 506, 566
In several cases, symptoms have been associated with dose.
At a high dose (0. 5 - 1.0 ppm for 0. 5 h), sensitive plants show complete
collapse. As the dose is reduced, the plants may show necrotic banding,
then bronzing and glazing with slight collapse. At 0. 1 ppm, chlorosis is the
79
major symptom. In some unpublished work, an upper-surface light-yellow
to white stippling has been described on alfalfa after exposure to PAN
at 0. 02 - 0. 1 ppm for 2-6 h. The injury was intercostal on the tip of young
128
leaves and on the base of old leaves. Drummond reported a necrotic
fleck and an upper-s\irface stipple on petunia after a 1-h exposure to PAN
at 0. 15 ppm.
Physiologic and Biochemical Effects; Mechanism of Action
Many reports on the effects of ozone and PAN on physiologic processes
(net photosynthesis, stomatal response, and water relations) and on metabolic
activity (including in vivo and in vitro studies of individual enzymes, enzyme
systems, metabolic pathways, metabolic pool relationships, cell organelles,
and plant tissue studies) have appeared since 1964.
11-14
-------
Stomata are the principal entry sites for ozone and PAN into plant
347
leaves, and stomatal closure effectively protects the plant from injury.
259,289,
Several studies suggest that oxidants may cause stomatal closure.
326,457
Stomatal closure was associated with a genetic factor in onion
142
wherein the stomata of sensitive plants did not close. The effect of ozone
and PAN on stomatal opening depends on many interacting factors; those
116
representing water stress appear to be the most important. Dean related
stomatal density to the difference in sensitivity between two tobacco cultivars.
153
Evans and Ting found that maximal sensitivity of b«an primary leaves
was not associated with changes in stomatal number o>r leaf resistance.
Ozone exposure caused a decrease in relative water content, but no change
in resistance. Bean leaf sensitivity seemed more a function of internal
activities.
Isolated enzymes and enzyme systems are affected by exposure to PAN
and ozone. It is now recognized that strong oxidants interfere with various
oxidative reactions within plant systems. Metabolic pools, including nitrogen
and carbohydrate, appear to have some controlling influence on the response
of plants to these pollutants. Sulfhydryl groups are primary targets of oxidant
pollutants and may be a key to understanding the mechanism of action.
Unsaturated lipid components of some membranes are sites of early action of
both ozone and PAN.
Ozone. Ozone is the most nearly ubiquitous of the photochemical
oxidants, at least in concentrations that cause measureable effects. It has
been studied more extensively than the other oxidants.
• Physiologic effects: The physiologic effects of ozone depend on
its entry into the internal leaf spaces through the stomata. If the plant
11-15
-------
is resistant to ozone even when stomata remain open, mechanisms of
resistance, other than stomatal closure, must be operative. The
physiologic effects measureable with the intact tissue include effects
on respiration and photosynthesis.
551
Todd reported that the respiration of pinto bean leaves was
stimulated by exposure to ozone (at 4 ppm for 40 min) . The first
measurements were 4 h after the ozone exposure. The respiration rate
later declined to the control value. In all cases, increased respiration
321
correlated well with visible injury. Macdowall confirmed these
results, but made an additional observation: during the first hour after
ozone exposure (at 0. 7 ppm for 1 h), and before visible symptoms
appeared, respiration was inhibited. The increase in respiration took
129
place only later, when visible symptoms appeared. Dugger and Palmer
reported an increase in respiration in lemon leaf tissue after 5 days
of exposure to ozone at 0. 15-0. 25 ppm for 8 h/day. They reported no
11
morphologic changes at that time. Anderson and Taylor found that
ozone induced carbon dioxide evolution in tobacco callus tissue. The
threshold for evolution was about 0. 1 ppm for 2 h in the sensitive Bel W .
3
The ozone concentration required for maximal carbon dioxide evolution
was about twice as much in the more resistant cultivar. Formation of
roots decreased sensitivity.
551 554
Todd and Todd and Probst also measured the effects of
ozone (at 4 ppm for 40 min) on photosynthesis and found that development
of symptoms was associated with inhibition of carbon dioxide fixation.
321
This effect was also confirmed by Macdowall, who reported that the
inhibition of photosynthesis was greater than that which could be accounted
11-16
-------
234
for by chlorophyll destruction. Hill and Littlefield associated decreased
net photosynthesis caused by ozone (at 0. 06 ppm for 1 h) with both stomatal
opening and rates of transpiration. These studies have generally shown
that net photosynthesis can decrease without visible injury.
431
Pell and Brennan found an initial decrease in net photosynthesis
and an increase in total adenylate concentration after a 3-h exposure to an
injurious concentration of ozone. Net photosynthesis returned to normal
within 24 h. Respiration was usually not immediately stimulated, but it
was within 24 h. The authors concluded that the stimulation of respiration
was a consequence of cellular injury, whereas the changes in photosynthesis
and adenylate content -were early events leading to the appearance of ozone
injury.
The photosynthetic rate is an important indicator of vigor in
ponderosa pine. A reduction in this rate may occur at the threshold dose
379
of ozone without visible symptoms. Miller ei^ aL found that a daily
9-h exposure to ozone at 0. 15 ppm reduced apparent photosynthetic rates
40
by 10% after 30 days, without typical ozone symptoms. Botkin et al.
found that a threshold ozone dose for suppression of net photosynthesis in
eastern white pine was a 4-h exposure to 0. 50 ppm.
Ozone causes both quantitative and qualitative changes in carbon
590
dioxide fixation patterns. Wilkinson and Barnes, using carbon
14
dioxide- C, found a reduction in radioactivity in soluble sugars and
increases in free amino acids and sugar phosphates in white pine after a
372
10-min exposure to ozone at 0. 10 ppm. Miller observed a decrease
14
in carbon dioxide- C fixation in ponderosa pines that correlated with
loss of chlorophyll, after exposure to ozone at 0. 30 - 0. 35 ppm. The
Hill reaction rates of chloroplasts isolated from healthy and ozone-injured
11-17
-------
ponderosa pine indicated that both light and dark reactions of the chloroplasts
15
from ozone-injured plants -were depressed. Barnes found depressed
photosynthesis and stimulated respiration in seedlings of four pine species
of the southeastern United States after exposure to ozone at 0. 15 ppm.
It is commonly observed that leaves exposed to ozone develop dark
green areas--sometimes referred to as a "•waterlogging" effect. If
symptoms develop, they will be in these "waterlogged" areas, but
symptoms are not always a consequence of the "waterlogging." In other
words, there is sometimes recovery from this initial effect. The effect
is due to leakage of cell contents into the intercellular spaces and, to
some extent, is reversible. Many experiments with radioactive inorganic
ions and organic substances have confirmed that plant cell permeability is
154 437
affected by exposure to ozone. Perchorowicz and Ting found that,
immediately after ozone exposure (at 0.4 ppm for 1 h), there was no uptake
14
of glucose- C, but the uptake slowly increased for a period of hours.
However, the metabolism of the glucose into various products (organic
acids, lipids, carbon dioxide) was not changed by the ozone exposure.
Although it is widely believed that the effects of ozone on cell perme-
533
ability are the basis of ozone toxicity, the chemical basis of the effects
on membranes is still arguable. It is still not clear whether the first
effect of ozone is on the protein or lipid components of the cell.
133
Dugger
-------
Susceptibility was regained by supplying sucrose through the petiole.
However, susceptible leaves could be made resistant by supplying more
sucrose through the petiole. They concluded that the leaf was resistant
when the soluble-sugar content was either above or below the range of
302
1. 0 - 4. 0 mg/g of fresh weight. These results were confirmed by Lee,
who concluded that the protective action of high sugar content could be
partly, but not completely, explained by causing closure of stomata (ozone
16
at 0. 8 ppm for 5 h). Barnes and Berry reported seasonal changes in
the soluble sugars of white pine that may relate low sugar contents to a
189
prolonged sensitivity to ozone. Hanson and Stewart found that several
species exposed to noninjurious concentrations of ozone retained higher
starch concentrations in their tissue after 12-36 h of darkness.
320
Macdowall found that tobacco leaves were most susceptible to
injury by ozone (at 0. 035 ppm for 5 h) just after full leaf expansion. This
point corresponded to the beginning of the decline in protein content.
303
Lee modified the nitrogen content of tobacco leaves by supplying urea
and found a positive correlation of injury caused by ozone (at 1 ppm for 5 h)
with nonprotein nitrogen, but not with protein. This result is in contrast
531
with that of Ting and Mukerji, who found that, in cotton leaves (in which
the period of maximal susceptibility was at about 75% of full leaf expansion),
the amino acid pool was low at the time of maximal susceptibility. However,
ozone treatment (0. 7 ppm for 1 h) increased the free amino acid pool.
At the moment, it is impossible to give a rational explanation of the
relationship between ozone injury and carbohydrate and nitrogen composition
of the leaf. The compounds measured (protein and carbohydrate) may be
only distantly related to metabolites that confer resistance or susceptibility.
11-19
-------
It seems reasonable that susceptibility and resistance of different
plant species and different varieties -within a species should depend on con-
centrations of endogenous antioxidants. The results of such studies do
191
not give a clear picture: Hanson et^aL concluded that the range of
susceptibility in petunia varieties depended on the ascorbic acid concen-
353
tration, but Menser found that the ascorbic acid content of tobacco
varieties -was not related to ozone susceptibility. Ozone resistance of
plants can be conferred by application of antioxidants. In the case of
•white bean, ascorbic acid, cysteine, glutathione, and nickel N-dibutyldithio-
105, 170
carbamate were effective. Field studies -with tomato and tobacco
showed that a number of antioxidants were effective protectors: manganous
1, 2-naphthoquinone-2-oxime, cobaltous 8-quinolate, nickel di-N-butyldithio-
454
carbamate, N-isopropyl-N-phenyl-p_-phenylenediamine. These pre-
ventives do not yet present an economically feasible practice for agriculture.
• Biochemical effects: It is usual to find some changes in the
chemical composition of plant tissue after exposure to ozone. One cannot
be certain whether the changes are associated with early reactions to
ozone or are merely delayed consequences of cell injury.
A number of histologic and histochemical changes in current-year
needles of ponderosa pine were detected after five to seven daily exposures
149
to ozone at 0.45 ppm for 12 h each day. Chloroplasts and carbohydrate
stain accumulated in the peripheral portions of mesophyll cells; con-
currently, the homogenous distribution of proteins and nucleic acids was
disrupted, and acid phosphatase activity increased. Cell wall destruction
occurred in mesophyll cells after appreciable intracellular damage.
11-20
-------
251a, 252 255
Howell and Howell and Kremer found phenol
accumulation associated with the exposure of plants to ozone. Menser
356
and Chaplin also reported an increase in the phenol content of tobacco
243
leaves injured by ambient oxidants. Hoffman reported as much as an
80% increase in nicotine in leaves exposed to ozone at 0. 24 ppm for 4 h.
No increase was found after exposure to 0. 06 or 0. 12 ppm. Keen and
271
Taylor found accumulation of several isoflavonoid compounds in soybean
(Harosay 63) exposed to ozone. The presence of these compounds suggests
a defense mechanism against ozone that is similar to that for disease
resistance.
556
Tomlinson and Rich reported an increase in y-aminobutyric
acid in bean leaves after exposure to ozone (at 1 ppm for 30 min). In a
531
more comprehensive study, Ting and Mukerji repeated this finding
in cotton leaves, but found increases in many other amino acids. The only
decreases found were in phosphoserine, phosphoethanolamine, ethanolamine,
phenylalanine, and alanine. There are discrepancies in the literature
regarding the time after ozone treatment before detection of changes in
531
amino acid composition. Ting and Mukerji found the increase only
543
after 24 h, whereas Tingey et al. reported the change to be immediate.
543
Similar differences concern soluble protein: Tingey ^t^l_. noted a rise
92,94
after 24 h, whereas Craker found a decline in protein content. As
543
far as specific proteins are concerned, both Tingey ei_ al. and Leffler
305 ~~ 595
and Cherry found a decrease in nitrate reductase; Yamaga et al.
106
reported a decrease in carbohydrase. Dass and Weaver found significant
increases in peroxidase and cellulase, but no change in lactate dehydrogenase;
97
Curtis and Howell reported an increase in peroxidase isoenzyme activity.
534
Tingey has also reported an increase in the G-6-PD activity. It is
11-21
-------
possible to fit the latter change into a rational scheme for the effects of
ozone, but "rational" is not synonymous with "right." Chang and
72
Heggestad found that ozone at 0. 35 ppm for 50-80 min impaired the
activity of photosystem II in spinach and reduced the 8-carotene of the
87
chloroplasts. Coulson and Heath, using isolated chloroplasts, found
an inhibition of both photosystems and no penetration of the grana. They
suggested that in the intact plant ozone affects only the first membrane
contacted.
69,70,71
Chang has made observations on the polysomes of pinto
bean leaves exposed to ozone (at 0. 35 ppm for 20-50 min). He found that
the chloroplast polysomes -were more susceptible to degradation than were
the cytoplasmic ribosomes. The sulfhydryl content of the chloroplast
ribosomes was also much more susceptible to oxidation than was that of
the cytoplasmic ribosomes. Finally, it was found that the effects of ozone,
on ribosome composition could be reproduced by p_-mercuricbenzoate.
Chang's results imply that either ozone itself or a product of ozone
oxidation passes from the cytoplasmic membrane to the interior of the
chloroplast before having its effect. These results connect with a number
of papers on the oxidation of sulfhydryl compounds by ozone. Tomlinson
557
and Rich have reported decreases in leaf sulfhydryl groups after ozone
exposure (at 1 ppm for 30-60 min). A number of investigators have found
that reagents that react with sulfhydryl groups can reproduce the symptoms
105
of ozone damage. Dass and Weaver reported this effect in white
557
bean. Tomlinson and Rich reported the same effect in tobacco, and
455
Rich and Tomlinson found that conidiophores of Alternaria solani
became more susceptible to ozone if they were pretreated with iodoacetamide.
11-22
-------
It appears that effects on sulfhydryl content may be quite early events
in the toxic reactions initiated by ozone. One should remember, however,
that symptoms of ozone and PAN injury are quite different, and one cannot
explain the effects of both pollutants as sulfhydryl oxidizers.
558,559
Tomlinson and Rich have also considered the reaction of
ozone (at 1 ppm for 30 min) •with lipid components of the leaves. They
found that a change in the fatty acid composition as a result of ozone
treatment was an increase in the saturated fatty acid content. It was
concluded that malonaldehyde (an index of lipid peroxidation) was formed
168
only in the later stages of ozone damage. Frederick and Heath reported
that the production of malonaldehyde is correlated with loss of viability of
Chlorella sorokiana exposed to ozone (at 1. 8 ppm for 5-20 min), but with
499
a lag after the initiation of ozone exposure. Swans on et al. , in
agreement with Tomlinson and Rich, found only small changes in the fatty
acid composition of tissue exposed to ozone (at 0.3 ppm for 2 h) . It is not
possible to conclude from the available data that oxidation of lipid is the
560
primary effect of ozone exposure. Tomlinson and Rich have examined
the effects of ozone on the complex lipids of plants. Plants were exposed
to ozone at 0. 25 ppm until the first symptoms were seen (2. 5-3 h), and
leaf solubles were extracted. It was found that there were a decrease in
free sterol and increases in both sterol glucoside and acylated sterol
glucoside.
543
Tingey et_a±. found an increase in reducing sugars soon after
the exposure of soybean plants to ozone. In experiments with ponderosa
379
pine, Miller e± aj. found that the polysaccharide content of both current
and 1-year needles, treated for 33 days with ozone at 0. 30 ppm, was lowered
11-23
-------
by 40%, but there -was a slight increase of soluble sugars. No
14
relationship -with ascorbic acid was found. Barnes reported studies
•with five pine species exposed to ozone at 0. 05 pprn for 5-22 weeks.
There were significant increases in total soluble carbohydrates, re-
ducing sugars, and ascorbic acid. At 0. 15 ppm, the effect on ascorbic
acid was not observed. These results do not lead one to believe that
ascorbic acid plays an important role in ozone resistance.
405
Nobel and Wang reported that the permeability of the outer mem-
branes of chloroplasts was increased by exposure to ozone (at 30 ppm for
169
5 min). They hypothesized that the effect was lipid oxidation. Freebairn
showed that ozone inhibited respiratory activities of isolated mitochondria,
304
and Lee found that the effect of ozone on oxidative phosphorylation was
395
greater than on oxygen uptake. Mudd ei_aL reported that the metabolism
of UDP-galactose by isolated chloroplasts was inhibited by ozone (at 1, 000
ppm for 2 min). There were differential affects on the synthesis of various
galactolipids, the synthesis of monogalactosyldiglyceride being relatively
resistant. This differential effect of ozone could be reproduced by chemicals
that react-with sulfhydryl groups.
There is some information concerning the reaction of ozone with
chemicals under aqueous conditions. The information available suggests
that double-bond cleavage takes place, just as it does under nonaqueous
conditions, except that ozonides are not formed. Instead, the zwitterionic
intermediate reacts with water, producing an aldehyde and hydrogen peroxide.
In addition to double-bond cleavage, a number of other oxidations are
394
possible. Mudd je_t al_. showed that the susceptibility of amino acids
is in the order cysteine, tryptophan, methionine, histidine, tyrosine,
11-24
-------
phenylalanine, and cystine (ozone at 2,000 ppm for 2-10 min). All
550
other amino acids are resistant. Todd tested the susceptibility of
catalase, peroxidase, urease, and papain to ozone. Papain -was the
most susceptible; this result is consistent with the knowledge that a
sulfhydryl group is necessary for its activity. The inactivation of
394 307
avidin and lysozyme can be attributed to the oxidation of
tryptophan residues, although, in the case of lysozyme, methionine is
also partially oxidized. Enzyme inactivation caused by ozone reaction
394
with histidine has been indicated in the case of pancreatic ribonuclease.
The reaction of nicotinamide derivatives with ozone has been studied by
392
Mudd j3jt al. (ozone at 0. 4 - 800 ppm for 1-100 min). The reduced
forms are quite susceptible, and the oxidized forms quite resistant. The
adenine moiety is quite resistant. When NADH is oxidized by ozone, the
5, 6 double bond is broken, so the coenzyme is no longer biologically useful.
Studies of the reaction of ozone -with simplified lipid systems have
393
shown that malonaldehyde can be produced by direct ozonolysis. The
use of malonaldehyde assay as an index of lipid peroxidation is therefore
invalid in ozone studies. Liposom.es formed from egg lecithin and pre-
pared in aqueous media were quite resistant to ozone, but the contribution
395
of polyconcentric spheres to this resistance has not been fully assessed.
However, the bilayer configuration, with the susceptible unsaturated fatty
acids shielded from ozone by the hydrophilic areas of the molecule, may
be resistant. In hexane, where the fatty acid moieties are exposed, ozone
reacts stoichiometrically with the double bonds. The experiments with
aqueous suspensions of phosphatidylcholine gave no evidence of the for-
528
mation of lipid peroxides, nor did experiments with films of fatty
465
acids exposed to ozone.
11-25
-------
• Chemical basis of toxicity: There is only one comprehensive
theory for the action of ozone on biologic organisms--the theory of Chow
73
and Tappel that the initial event is the formation of lipid peroxide and
that successive events are an attempt to detoxify this product. The theory
was developed from experiments with animals that show that exposure to
ozone increases malonaldehyde, glutathione peroxidase, glutathione
reductase, and G-6-PD.
O
3
lipid £ lipid peroxide (ROOH),
GSH peroxidase
ROOH + 2GSH ^ROH + GSSG,
+ GSSG reductase +
GSSG + NADPH + H > 2GSH + NADP ,
+ G6P dehydrogenase +
NADP + G-6-P . ^ 6PG + NADPH + H .
This theory is questionable on a number of points: there is no
direct evidence of formation of lipid peroxide, GSH can be oxidized
directly by ozone or used to reduce hydrogen peroxide produced from ozone
reactions, and the increased activity of G£»P <^eh
-------
• Physiologic effects: Leaf age and illumination have been studied
as physiologic and physical factors that affect the response of plants to
135
PAN. Leaves of most plants are most susceptible when very young.
In primary leaves of pinto bean, the period of maximal susceptibility to
PAN precedes that for ozone by several days (about 5-7 days from seed
for PAN, as opposed to 9-13 days for ozone). The example of tomato
is particularly striking, inasmuch as the terminal leaflet of the compound
leaf is the oldest tissue. Thus, the youngest susceptible leaf is affected
in the terminal leaflet; but, as the leaves become older, the terminal
510
leaflet is resistant and the lateral leaflets are injured.
There is no reason to believe that stomatal opening is different
in leaves of different ages, so the entry of PAN into the intercellular
spaces of the leaf is probably the same as the entry of ozone. One can
hypothesize that the chemical composition of the leaf is such that re-
sistance is conferred at particular physiologic states. Such a hypothesis
would lead to a search for compounds that combat the oxidizing and
acylating properties of PAN.
There appears to be an absolute requirement for illumination
before, during, and after fumigation with PAN (1 ppm for 30 min), if
513
symptoms are to be observed. If the prefumigation light period is
followed by 15 min of darkness before a 30-min exposure to PAN in the
light, no symptoms are observed. Thus, at this time, a short dark
period before PAN exposure prevents damage. However, the dark period
after fumigation must be 1-2 h long, if damage is to be avoided. The light
506
period after fumigation must be 3 h long, if damage is to be maximal.
These effects of illumination are not understood.
11-27
-------
134
The action spectrum for the light requirement shows maximal
quantum responsivity at 420 and 480 nm and low responsivity at wavelengths
134
characteristic of chlorophyll (PAN at 4 ppm for 15 min). The action
spectrum suggests participation of either carotenoids or flavins. It should
be emphasized that the action spectrum for illumination was determined
only during fumigation. It is possible that a different photoreceptor is
involved in the periods before and after exposure. Photosynthesis of
intact cells of Chlamydomonas reinhard/ was inhibited by PAN (at 125
180
ppm for 5 min). Photosynthesis recovered after the exposure, but
the recovery varied with the light quality used during the exposure.
Recovery was less when the irradiation was at 450 nm; this is roughly
134
consistent with the work on the action spectrum in pinto bean leaves.
Although the quantum responsivity is low at 660-700 nm, effects
of irradiance at these wavelengths are noticeable. In a comparison of the
effects of light at 660 and 700 nm, injury was greatest when plants were
irradiated at 660 nm during exposure and lowest when they -were exposed
130
either in darkness or at 700 nm (PAN at 1 ppm for 15 min). The most
striking observation was that simultaneous exposure to light at 660 and 700
nm resulted in little injury. These results v/ere interpreted as effects on
photo synthetic systems I (activated at 700 nm) and II (activated at 660 nm),
but effects of these wavelengths on phytochrome transformation should not
be overlooked:
660 nm
P -; ^ p
700 nm
where P is the red form of phytochrome and P is the far-red form.
r fr
11-28
-------
It is noticeable that the action spectrum for the PAN effect is similar to
that for phytochrome and for some physiologic responses mediated by
59,383
phytochrome. Interaction of PAN with the phytochrome system
seems worthy of systematic study. The light effects may also be related
to the sulfhydryl content of plants, inasmuch as illumination increases
130
and exposure to PAN (at 1 ppm for 15 min) lowers the sulfhydryl content.
It has been suggested that sulfhydryl compounds are susceptible to
reaction with PAN (by oxidation or acetylation), and thus that conditions that
increase the sulfhydryl content will increase susceptibility. This explanation
for PAN injury is consistent -with the finding that inhibition of photo-
phosphorylation by N-ethylmaleimide, a reagent that reacts with sulfhydryl
350a
radicals, is most effective when chloroplasts are treated in the light.
In the Calvin and Hatch-Slack pathways of carbon dioxide fixation in photo-
synthesis, some enzymes are activated by light (e. g. , ribulose phosphate
59
kinase), and some are inactivated by light (e. g. , glucose-6-phosphate
9
dehydrogenase or G-6-PD). In both cases, the effect of light can be
replicated with sulfhydryl compounds, such as dithiothreitol. The reaction
of PAN with the sulfhydryl forms of these enzymes can easily be visualized
as upsetting the regulation of carbon dioxide fixation. These considerations
are consistent with the effects of PAN on various aspects of photosynthesis
(adenosine triphosphate, ATP, formation; nicotinamide adenine dinucleotide
phosphate, NADP, reduction; and carbon dioxide fixation) and with the fact
that the earliest injury found by the electron microscope was in the stroma
525
of the chloroplasts (PAN at 1 ppm for 30 min).
• Biochemical effects: Several enzymes that use nicotinamide co-
387
factors were found to be inhibited by PAN (at 125 ppm for 1 min) in
11-29
-------
in vitro studies. These enzymes were most susceptible in the absence of
substrates. In some cases, an enzyme was protected by the nicotinamide
cofactor (e.g., G-6-PD plus NADP), and in other cases, by the cosub-
strate (e. g. , isocitrate dehydrogenase plus isocitrate). Precisely the
same protection could be obtained when compounds that react with
sulfhydryl compounds (e.g. , p_-mercuricbenzoate) were used instead of
PAN. Thus, the evidence indicated that PAN reacted with sulfhydryl
groups.
Direct evidence of the reaction of PAN with sulfhydryl compounds
306, 388, 391
has since been obtained (PAN at 115 ppm for 1-10 min). In the
reaction with glutathione, the major products are oxidized glutathione
(disulfide) and S-acetylglutathione. Other sulfhydryl compounds (e. g. , co-
enzyme A, lipoic acid, and cysteine) yield only oxidation products, with no
evidence of S-acetylation. However, acetylation reactions have been observed
403 583
with alcohols and amines. Sulfur compounds other than thiols can
undergo oxidation by PAN: methionine is converted to methionine sulfoxide,
and oxidized lipoic acid (disulfide) is converted to sulfoxide.
Papain is readily inactivated by PAN (at 115 ppm for 40 min), provided
391
that it is in the sulfhydryl form. The reaction of sulfhydryl groups of
hemoglobin with PAN is very similar to the reaction with p_-mercuricbenzoate:
there is more reaction at a pH of 4. 5 than at a pH of 7. However, there
is one striking difference between PAN and classic compounds that react
391
with sulfhydryl groups: egg albumen is resistant to reaction with PAN.
Thus, enzymes that have no free sulfhydryl groups should be quite resistant
to PAN. This is the case with pancreatic ribonuclease: the native enzyme
was not affected by a 300-fold molar excess of PAN.
11-30
-------
There is some difficulty in correlating results of PAN exposure
in vivo with the above types of in vitro studies. For example, UDP-glu-
pyrophosphorylase is very susceptible to PAN in vitro, but in vivo there
186
is a stimulation of enzymatic activity (at 112 ppm for 6 min). It is
also anomalous that, whereas phosphoglucomutase of oat seedlings is sensitive
186
to PAN both in vivo and in vitro (at 50 ppm for 4 h), it is generally
considered that the active site is serine, rather than cysteine. Results of
enzyme analysis after in vivo exposure to tissues to PAN are complicated,
because direct effects on the enzyme may be overshadowed by effects on
protein synthesis, and these effects in turn may be directly on the protein
synthesizing machinery or on the regulatory mechanisms that depress or
stimulate protein synthesis. A schematic representation of this dynamic
system shows that PAN could affect the synthetic process (site 1), the
enzyme itself (site 2), or the degradation process (site 3). If the site of
attack were site 2, the synthetic process might compensate for degradation
of the enzyme by producing more.
synthesis enzyme X degradation degradation
precursors _____\ _ _ _ _ ^ products
t T t
site 1 site 2 site 3
If the enzyme activity were measured as a function of time after exposure,
there would be first a decrease and then recovery of activity. (Such a
response has been observed for the effect of ozone on respiration. ) Effects
at site 3 -would show first an increase in activity and then, if the system
were regulated, a decline to normal, as the synthetic process slowed down.
Effects at site 1 would cause a decrease in activity commensurate with the
rate of enzyme degradation.
11-31
-------
Experiments with chloroplasts showed an apparent inhibition of fatty
389
acid synthesis by PAN (at 72 ppm for 10 min). The result is difficult
to interpret: the inhibition could be attributed to inactivation of one of the
enzymes of the multistep system or to oxidation of the reductant (reduced
NADP, or NADPH) required in the chain elongation process.
In addition to the protein and low -molecular -weight thiols that
react with PAN, there are several other reactive biochemicals. Reduced
nicotinamide derivatives are susceptible to oxidation by PAN (at 72 ppm
389
for 1-5 min), whereas the oxidized forms are resistant. The capability
of PAN to oxidize these compounds rapidly dissipates in aqueous solution,
with a half-life of 4-10 min, depending on pH. The oxidation products appear
to be the biologically active forms of the nicotinamide derivatives. Purines
427
and pyrimidines react with PAN (at 1, 000 ppm for 30-120 min). The
order of sensitivity is thymine, guanine, uracil, cytosine, and adenine.
Their reactions were studied at relatively low pH and at high PAN concen-
tration and are probably not of biologic significance.
Various olefins and amines (undiluted) react with solutions of PAN
104, 583
in CdCl:
z
.0
PAN + R C = CR - ^R C - C R + MeONO + MeNO ;
2222 2
PAN + RNH - ^CH CONHR+O + HNO .
23 22
These oxidation and acetylation reactions have not yet been examined in a
biologic context.
• Chemical basis of toxicity; The toxicity of the peroxyacylnitrates
to plants can be the result of several different processes. Any chemical
11-32
-------
explanation of the toxicity will have to explain the increasing toxicity of
the series PAN, PPN, PEN, and PBzN. Three hypotheses have been
390
tested: the more toxic homologues are more readily taken up by the
plant; all homologues are taken up equally well, but the plant is able to
reverse the actions of the lower homologues; and all homologues are
taken up equally-well, but the higher homologues have longer half-lives.
In testing the first hypothesis, it was found that PAN and PPN were taken
up equallly well by plants; so that hypothesis is probably incorrect. The
ability of the plant to hydrolyze thioesters of glutathione was tested; the
second hypothesis predicted that the higher homologues would be hydrolyzed
591
more slowly; but the opposite was found. Thus, the second hypothesis,
although not fully tested (in that the thioesters measured may not be the
ones formed in the cell), does not look promising. The third hypothesis
was tested by determining the half-lives of the oxidizing power of each com-
pound in aqueous medium. PBN had the longest half-life, as predicted, but
390
the half-lives of PAN and PPN were about the same. It seems probable
that half-life influences the toxicity of the peroxyacylnitrates, although
definitive results have not yet been obtained.
Discussion. The acute responses of plants to ozone and PAN result
from disruption of normal cellular mechanisms. The initial response causes
disorganization, prehaps through an attack on sulfhydryl linkages or unsaturated
lipid linkages. Cellular water and salts are lost, with cell plasmolysis re-
sulting. Cell death normally will occur; however, depending on dose and
environmental conditions, membrane permeability may be restored and cell
recovery take place. The extent of recovery depends on the severity of the
external stresses and probably on the ability of the cells to initiate repair
11-33
-------
mechanisms. A sigmoid response has been observed in many plants
exposed to ozone and probably reflects physical resistance to gase move-
544
ment within the tissues. Tingey ^jt aL determined activity changes
in selected enzymes from soybean leaves and found that the reactions
were similar to those produced by other stresses, and not to the process
of senescence.
Chronic injury results primarily from secondary reactions involving
membrane injury. The oxidants could cause the formation of free radicals
or other, more stable oxidants (such as hydrogen peroxide), -which in turn
could cause secondary reactions. These secondary reactions could stimulate
1,89,539
the production of cellular ethylene, with tissue senescence resulting.
These secondary reactions may predispose plants to increased injury from
later acute exposures by limiting their repair capability. This predisposition
concept has been noted in several reports.
Reproductive Systems and Life Cycles
Ozone and PAN are both strong oxidizing agents. Some work has
suggested that ozone is a radiomimetic gas. It is known to cause chromosomal
breakage in both plants and animals at high concentrations. Although the
potential of ozone's mutagenic effects on vegetation at ambient concentrations
491
is not understood, Sparrow and Schairer reported that ozone appeared
to be a weak mutagen in causing an increase in the pink somatic mutation
rates in petals of Tradescantia.
155
Feder showed an effect of ozone on tobacco pollen germination
and postulated effects on reproductive capacity of tobacco. This work was
488
not substantiated by Sinclair, but the exposure techniques used were
177
questionable. Gentile £t al_. showed that germination of pollen from
11-34
-------
sensitive ascessions of Lycopersicon Pimpinellifolium were reduced by as
155
much as 40% with techniques described by Feder. However, reciprocal
cross-pollinations between ozone-exposed and -unexposed populations led
193
to normal fruit development and viable seeds. Harrison and Feder
found a migration of cell organelles from the outer layer of cytoplasm in
pollen grain of sensitive petunia exposed to ozone. They used 0. 50 ppm for
397
3 h and found an 80% reduction in germination. Mumford et a_l. found
that 0. 03-0. 06 ppm was the threshold for an effect on germination of corn
pollen. They did extensive biochemical studies of the pollen and suggested
that ozone induces autolysis of structural glycoproteins and stimulates amino
62, 63
acid synthesis. Cameron and associates found major reductions in
yield of some corn varieties after high-ambient-oxidant episodes occurred
during tasseling. These reductions appeared to result from poor fertilization.
Although preliminary, those studies point to the importance of understanding
the direct effects of oxidant pollutants on reproductive processes within plant
species.
A study was undertaken to determine the potential mutagenic effects
57
of ozone on Arabidopsis thaliana. This plant completes its life cycle in
about 35 days and is an excellent test species for determining effects of ozone
across life cycles. Plants were exposed to acute doses for 6 h/day, 3 days/
•week, through 4 weeks of the life cycle. Seeds were collected from control
and exposed plants and planted over seven generations. Seed production and
biomass were reduced within generations, but no factors studied were carried
over into later generations. The results showed that, for this particular
species and the concentrations used, no mutagenic effects were carried via
seed to later generations. This was a preliminary study that also reported
11-35
-------
problems with variability in plant response. The author suggested that
similar studies be initiated to verify these results.
Biomass and Yield
Photochemical oxidants, including ozone and PAN, reduce plant
biomass and yields in many plant species. Although yield and growth reduc-
tions are normally associated with visible injury, the oxidants can cause
growth reductions with little or no injury. This relationship is not understood
for the oxidant pollutants and probably varies with species and cultivars,
as well as with conditions of growth and exposure, including dose. Todd
552
and Arnold compared injury with biomass and chlorophyll content for
pinto bean exposed to a synthetic oxidant (ozone plus hexene). They found
a logarithmic relationship between injury and the two physiologic measure-
ments and suggested that injury was not a reliable index of growth effects.
Their data were from acute exposures and suggest effects on growth at low
4,5
injury values. A group of Canadian workers have used physiologic
measures exclusively for acute exposures. Many investigators are using
physiologic measures, instead of injury, because they are more objective.
Although physiologic responses are often better measures of chronic effects,
their variability is usually at least as great as that of a subjective injury
measure, and they are sometimes not as sensitive in indicating acute effects.
470
Runeckles and Resh reported on a reflectance measure of chronic effects
that was much less variable than chlorophyll extraction. They did not com-
pare this with a visual injury estimate. This technique should be studied
further.
Considerable information is available on growth and yield effects.
However, because it comes from scattered sources and much of it is
11-36
-------
subjective, no one has developed the data for predictive use (relating
dose or injury to yield reductions). This section is divided into a discussion
of effects under ambient conditions and a discussion of effects with controlled
additions of oxidants, primarily ozone. The ambient oxidant section includes
observational information and chamber studies comparing plant response in
filtered versus unfiltered ambient air.
Ambient oxidant studies. Since the first observations of oxidant
injury, there have been continual reports of effects of oxidants on
vegetation. This section does not attempt to cover all those reports, but
does give several descriptive examples. The closing sections of this
chapter (on plants as monitors and on economics) have additional examples.
144
Engle elb al_. first identified ozone as the cause of onion tip burn. They
associated the development of this condition with severe •weather fronts and
suggested that ozone, produced in thunderstorms, may be the culprit.
They identified both resistant and sensitive cultivars where resistance was
580
genetically controlled. Weaver and Jackson first described bronzing
in white bean and associated this with oxidant (ozone) episodes. They found
that ozone produced similar symptoms and that 0. 16-ppm ozone for 0. 5 h
was the threshold for effects in their studies. This disease is known to cause
184
reductions in bean yields. Haas did a growth analysis in field plot studies.
He selected 5 plots based on severity of bronzing symptoms and showed a
relationship between severity of bronzing and growth. He found that the
rate of growth influenced symptom severity and that the stage of growth
determined the dose at which bronzing occurred. He showed that physical
42
conditions within a field could cause a variable response. Brasher et al.
reported 10 - 95% injury to 3 cultivars and 16 seedling lines of potato
11-37
-------
after 3 days of ambient oxidant that reached a maximum of 0. 15 ppm. No
459
yield data were reported for this study. Rich ^t al_. reported crop
damage from oxidants to many plants in Connecticut when oxidant concen-
tration was above 0. 05 ppm. There were 83 of these high-oxidant days in
451
355 days monitored over 4 growing seasons. Reinert ei_ al. found similar
effects around Cincinnati, Ohio, when oxidant concentrations were high. In
this study, a group of plants was set out to monitor effects. Generally,
422
these studies have not included quantitative yield data. Oshima et al.
reported a severe episode in California where injury was greater than
expected on the basis of total-oxidant measurements. The presence of PPN
was suspected. This is indicative of the episodic potential in high-pollution
areas throughout the country. Several studies have reported on the severe
77,375
effects of oxidants on ponderosa pine in the San Bernardino Mountains,
and quantitative work (including growth-ring analyses) is reported elsewhere
32, 571
in this document. Several subjective observations have come from Europe
588
and Australia, but little quantitative work has come from outside the
United States and Canada.
Several excellent studies have reported yield data obtained by use
of filtered and nonfiltered greenhouse or field chambers. Selected summary
data are shown in Table 11-2. The first field-chamber work was reported
521
on citrus by Thompson and Taylor. Their report summarized several
years of detailed work on lemon and orange and considered many combinations
of pollutants. Reductions in fruit size, number, and total yields were
reported in these studies and are the basis for the projected 50% reductions
520
in citrus yields from the Los Angeles basin. Thompson and Kats showed
that some of these effects on citrus were probably related to concentrations
11-38
-------
cu
o
C
0)
(N
CN
CN
rH
CN
o
csi
CN
,— 1
rH
CU
rH
43
rt
H
A
13
rH
CU
•H
*t
43
IS CO
O 4-1
M C
O rt
rH
Q
rrj
/•^ cu
CU 4J
c o
o cu
N rH
O CU
v-x c/3
CO C
4-1 -H
rt r*i
13 J-l
•H 3
X i-l
1— 1
4->
(3 M
cu rt
•rl -rl
rP 1 — 1
I °
^3 P^t
MH 13
0 (3
rt
ca
4-J
a
cu
>4H
MH
Ci3
rH
o
S-l
4-1
a
S-S O
O
•i
cu g
co o
C rJ
O MH
P,
co c
cu o
PS -H
4J
4-1 0
a 3
rt 13
rH CU
PM r4
13 13
rH rH
cu cu
•H -H
* ft
CN CN
ro in
cu
Jj
H
a)
rl
3
CO
o
p.
w
a
o
ca
rt
cu
CO
(3
•H
o
60
cu
Q
S
P
P
p3 *
0 S3
O 0
•H
4-1 4->
13 rt
rt rl
13 4-1
•rl (3
S3
0
I— 1
•
o
A
^
CO
4J
G
CU
M-l
cu
^_)
cu
43
4-1
o
13
C
rt
p.
o
13
MH
rt
cu
H
N—''
yi-Nt
T3
(3
o
M-)
CO
G
o
•H
4-1
a
13
13 CU
rH rJ
a)
1-1 (L|
r*. CU
•> 4J
<• o
m •— '
C
•H -v.
,r|
•
cu >
rH
0
r™3
pi
•H
•
cu
>
rt
rG •
4J *J
o a)
0 co
x— ^
—v !-i
M cd
rt cu
cu >.
f^
4-1 Pi
CO O
!-( G
•H CU
MH co
S™ S NM*'
*T3 *T3
rH rH
cu cu
•H -H
M «V
CN rH
rH \O
4-1
p.
cu
C/3
1
^> pi
rt o
rt
M cu
CU CO
^
O 00
P!
Pi -H
CU ^
4J 0
<4H SJ
O 00
LO
cs
•
o
Al
^*l
4-1
fi
cu
4-1
O rJ
o rt
cu
cd
00 13
3 M
CO -H
r!
T3 4-1
0) ^x
CO
rt ^c3
CU rH
t-l CU
O >H
Pi r**!
•H
^-^ *
r^
«J-
•> /*^
CO CO x-v
M rJ CO
rt rt v-i
> > fl)
•H -H >
4J 4J -H
rH rH 4J
3 3 rH
0 03
x-N 0
O CU ro
rH i— 1 r- < i— 1
^^ rP ^^ r-l
rt ^-^
r*^ 4-1 r*%
S-l 0) rJ >^
3 ."^ 3 M
•!-> rJ T-l 3
C1 rt 13 -i-i
•H S -H (3
M *rl
9^ 3 •*
r^. oo •>
vo in » — i i — i
S-l
0
M-l
cu
Q r4
3 0
Q 1J I
.g o3
^ r**^
cd
g CO
^
^> ci3 ^
H nd M
M S
j3 *>d" *r~)
0 1 (3
5C ro -H
m
m
•
o
1
^5
CM
•
o
cu
, — 1
P,
^
4J
CO
a
•H
4J
o
^1
a
CU
C
A
rl
o
rH
o
a
cu
N
(3
o
r4
M
V— «•*
J.J
cr>
00
o
0
A
x—s
C
0
•H
CO
co
•H
G
co
o
«
cu
}_4
3
4-1
rt
0
dJ
J_4
a
ca
4J
S
rH
p.
cu
^
•H
4-1
•H
CO
C
cu
CO
rl
0
M-l
13
rH
o
43
CO
cu
M
,£]
H
N^ /
1
1
t-Q
t_f"j
1
a
p.
p.
o
CN
t
o
rt
^-^
^*>
M
3
•n
(3
•H
*T3
t-H
o
r!
CO
(1)
J_l
43
4-1
rH
cd
S
•H
C
•H
S
N»-^
1^2
00
1
vO
m
o
o
CN
o
o
V-l
rt
ca
CU
4-1 -H
C G
rH P^
PM tti
pi
o
§
cu
00
§
rt
•H
4-1
« Pi
cu rt
P.M-1
rt ti
O NI
cu
S
CO
o
O
cu
pq
G
o
H
3
O
o cu
H pq
4-1
P4 O
o o
4J M
4-1 4-1
43 43
CO CO
cu cu
H (-1
M-I MH
CN r-
CN CN
00
•rl
S
O
VJ
60
C §
cu co
4J rt
<4H CU
O CO
m
o
o
A
rt
G
o
G
G !S
rt
o cu
H PH
11-39
-------
O C
cfl
CD
4J
O
01
0)
CJ
cu
cu
IH
0)
co
CM
CM
CM
/^s
•
4J
O
O
N-^
CM
|
i-l
i— 1
CU
rH
Cfl
H
ft
T3
a)
•H
bH
ft
J
W ^
j» W
o -u
O cfl
1
r^
CJ PM
O
13
/-* 0)
01 4-1
C 0
O 0)
N t-l
O O)
^ CO
co (3
4-1 -rl
a
cO >-.
•H 3
X "*"")
O Pi
r-l
4J
0 M
CU Cfl
•H -rl
6 o
•^ pn
M-t T3
i™H
0
4-1
C
&•« 0
0
n
cu e
co o
0 M
O M-I
ft
CO 0
0) O
PH *rH
4->
4-1 CJ
0 3
cfl 13
r-l 0)
PM l-i
*"O
H
0)
•H
jx,
•«
^^^
0
I
VO
I— 1
V— '
00
CM
0)
£3
•H
H
CU
H
^
CO
o
ft
X
W
60
0
•H
[j
O
J-|
60
60
jj
•H
M
3
^ 0
|LfJ Q
CO
in co
vO CU
13
0)
0>
CO
•f.
s-^
4-1 CM
0 r^
•H CTi
rH i-H
A
O
CN
1
C
o
CO
cfl
0)
CO
60
C
•H
[5
O
60
V-J
cu
^
o
co
0
O
•H
4J
Ctf
a
o
1-1
CO
13
01
cu
CO
.!•
/«-x
4-1 CO
0 r~
•rl CT*
pH ^H
ft
O>
CM
1
m
CM
CM
}_l
0 M
4-1 O
n |
CO
M M
cfl cfl
cu >
*"O *H 'O *H
iH 4-1 H -U
0) i-t s O >> O
•t A
^3 vO
LO CM
| |
"«3" O
CO (N
y— N
CO
J_J
cfl
0)
CM
v — '
43
CO
CO
1
CM
CO
s~\
13
0)
J_(
01
^
O
o
CO
CU
cfl
<4-4
cfl
0)
rH
s-'
^^
J-l
3
*i ;
•H
•\
lO
ON
CO
^*>
C^J
*T3
CU
^
•rH
4-1
3
CJ
CU
ca
0
O
O
CO
I
ft
0 «
O 0
O O
•H
4-1 4-1
0 Cfl
cfl M
3 £
>.
0
W
CO
CO
^
•H
4-1
r-l
3
O
p
•H
4-J
rH
CJ
A
0
O
4-J
4J
O
CJ
Cfl
rH
3
O
4-1 -H
rd 4-1
4J H
O 3
PH O
•H
4-J
i-l
3
O
ft
O
4-1
Cfl 60
4-1 -H
O cfl
PM HI
0
o
4-1
Ol
13 (3co
T3 0 1^5
•H f
g cflcn
4JLO
O) cfl.3-
O T3 •>
•H cum
CD >J-
•H ••
0) 4->cM
S-l CflCNl
3 4-iJ-
cfl 4-id-
H 0co
0) Cfl r— t
4-13"
•H CT'J"
4J--H
0) 3 •>
J3 O
t> O O oo
cfl S -HcM
J3 4->csl
ft «
(3 • -HI— i
O Cfl M I~H
•rH -H CJcsl
4-1 0 TO •
n) H o) co
4J O 13 &
o) IH oi
60 -H 01 -H
01 .H > >
> cfl -H 0)
O 60 J-4
O
4-1 0 T3 rH
•H C cfl
>^ cfl Vi
M co o)
3 4-1 CD >
•n 0 4-1 CU
C oi o co
•H "4-4 0)
IH M-i 0
IH oi IH -H
O Ol
ca oi 4-1 oi
0 4-1 [3 >
O Vt cfl -H
•r-l O rH 60
4J ft ft
cfl 01 01
£> H H H
M 0 cfl
01 4J
CO CO Ol CD
,J2 5-1 CD 0)
O -rl O -H
IH 13 M
13 cfl
i— |cn 4-> g
Ol <-£> dp
•H co cfl 3
IH • 4J CD
i— 1 1 3
?•> Cfl 1 1 — I *T3
C .H O
CO 4-J O O
S Ol| ftO
•
CU
0
•H
1 |
X
(3
•H
OJ
^
4J
a
01
u
C
O
O
II
01
co
o
-
O
•s
cu
oi
11-40
-------
518, 519, 522
of PAN in the ambient air. Thompson and co-workers used
the same chambers to determine effects of oxidants on grape over 2 years.
They found nominal effects in the first year and 50-60% reductions in the
next 2 years. The differences were attributed to the effects of oxidants
on floral initiation in the year before the first study year. This concept
could hold for any plants when floral structures are initiated in the prior
season. They also reported a 41-62% reduction in leaf chlorophyll and
a 13-17% reduction in sugars. A wax emulsion spray gave a 20% increase
in yield over unsprayed plants; this suggests that selected protectants may
be useful in protecting grapes grown in areas of high oxidant concentration.
These chambers were also used in the San Joaquin Valley in California to
53
determine effects of oxidants on cotton. Yield reductions of 5-29% in the
lint and seed were reported at three locations over 2 years, but no effects
221
on lint quality or seed grade were found. Heggestad reported reduced
yields in four potato cultivars grown in filtered versus nonfiltered green-
houses. The results cover a 3-year study and show up to a 50% loss in
yield from sensitive cultivars. He also presented an excellent description
204
of oxidant and ozone symptoms on potato. Heagle et aj_. reported
preliminary results on yield reduction in tobacco grown as part of a test
of an open-top field-chamber design. They found significant reductions in
both top and root fresh weight that compared closely with injury ratings
253
(Table 11-3). Howell and Koch reported yield reductions of 16-40%
in four soybean cultivars with these open-top chambers. They found no
changes in the protein or oil of seed.
11-41
-------
Table 11-3
Injury versus Growth Reduction in Selected Plants Exposed to Ozone
Ozone Con-
Plant Growth Foliar Injury
Response, % Response, %
Plant centration, Exposure reduction increase over
Species ppm Time, h from control control Reference
Bean,
cultiva r
Pinto
Corn,
sweet
Soybean,
cultiva r
Dare
Tobacco,
cultiva r
Bel W
3
Soybean (2
cultivars)
0. 30
0. 30
0. 30
0. 30
0.05
0. 10
0.05
0. 10
0. 1 (+
SO at
2
0. 1)
> 0.05a
0. 05
0. 10
0. 5/day,
14 days
1. 0/day,
14 days
2/day,
14 days
3/day,
14 days
6/day,
64 days
6/day,
64 days
6/day,
133 days
6/day,
133 days
6/day,
133 days
(Often
over
growing
season)
8/day, 5
days/wk,
3 wk
8/day, 5
days/wk,
3 wk
1 1, leaf dry wt
40, leaf dry wt
70, leaf dry wt
76, leaf dry wt
12, ave. 4 yield
responses
35, ave. 4 yield
responses
22, plant fresh wt
65, plant fresh wt
75, plant fresh wt
22, top fresh wt
2, top fresh wt
21, top fresh wt
9
46
69
78
14
25
19
37
46
17
8
19
319
206
205
204
548
a A study in field chambers with ambient photochemical
oxidant (ozone) concentrations.
11-42
-------
Controlled chamber studies. Many workers have used controlled
additions of ozone in acute or chronic studies to determine effects on a
variety of growth measures. These studies suggest results attributable to
ambient oxidants in field plantings. However, in the field, there are
probably combinations of acute, chronic, and predisposition effects of
oxidants on the susceptible species and cultivars. Most of these studies are
from greenhouse and controlled-chamber exposures, but several have used
chambers placed over field plantings. Several studies have shown correlations
between injury and yield or biomass reductions (Table 11-3). These suggest
that injury may be a good criterion of yield reductions. However, it is
known that yield reductions occur with little or no visible injury and that
injury may cause no measurable yield reductions. These studies have been
divided according to whether they used short- or long-term exposures.
413
• Growth effects of short ozone exposures: Ordin and Propst
used high concentrations of either ozone or PAN and reported a 50% inhibition
in indoleacetic acid-stimulated growth in Avena coleoptile. This suggested
that the oxidant may have a direct effect on hormonal production. Adedipe
and associates reported reduced biomass and floral production in four bedding
5 4
plants and in 2 radish cultivars from acute ozone exposures (Table 11-4).
They reported no effects on marigold, celosia, impatiens, and salvia, even
at the high concentration of 0. 80 ppm for a 2-h exposure. The radish study
included effects of exposure temperatures on growth. One cultivar re-
acted the same across temperatures, but the response of the second was
540
conditioned by temperature. Tingey et ah exposed radish at 7, 14, or
21 days and all combinations of these ages to ozone at 0. 40 ppm for 1. 5 h.
They found the greatest effect on root growth at 14 days for the single
11-43
-------
HI
o
CU
U1
cd
H
CO
4J
c
cd
rH
PH
O
cu
rH
01
C/)
M-4
O
T)
rH
cu
•H
(H
1
O
r-l
O
CO
o
p.
C
6s?
cu"
CO
a
o
ex
ca
cu
erf
4-1
C
rrl
TO
rH
PH
CU
M
J3
ca
0
3
rH
O
H
4J
C
o
a
o
4-1
d
o
•H
4-1
o
cu
M
rC
*
cu
4J
0
o
CO
CO
a)
ca
13
O
Pu
CO
CU
V4
J3
4-1
&
0
00
CO
M-l
O
•
cu
cd
A
m
CN
•
O
(3
l-i
CU
Z
0
M-l
A
4J
J5
^.i
CU
O
U-l
co
CU
ca
C
o
P.
ca
cu
n
CU
!
CO
M-l
0
•
cu
Cfl
cT
*—*
CM
CO
cu
co
13
o
ex
CO
cu
^
cu
6
cd
CO
14-1
0
•
£
cd
ON
""""
CN
CO
cu
ca
C
o
ex
ca
cu
cu
CO
M-l
O
•
cu
>
Cfl
oo
CO
CM
ca
cu
CO
C
o
P.
CO
cu
^
1
cd
ca
<4-l
o
•
cu
cfl
*
ON
CN
ca
cu
co
0
ex
co
cu
cu
1
CO
M-l
o
•
cu
cd
r— 1
iH
CN
CO
CU
CO
o
ex
ca
cu
M
cu
H
CO
M-l
0
•
cu
cd
i— i
CM
CN
CO
CU
CO
O
ex
CO
0)
r-4
cu
co
M-l
o
•
CU
cd
F— 1
CO
CN
ca
cu
ca
C
o
ex
CO
cu
M
g
cd
ca
<4-l
O
•
CU
cd
„
CM
CM
co
cu
co
13
o
a
CO
cu
cu
1
co
MH
o
•
cu
cd
,^r
1~H
CN
CO
CU
co
(3
O
ex
CO
a>
cu
1
CO
M-l
o
•
CU
cd
^
CM
CN
CO
CU
CO
(3
o
ex
CO
cu
cu
ca
M-l
o
•
cu
>
cd
oT
CO
CN
CO
CU
CO
C
o
p<
co
a>
^
0)
e
cd
CO
M-l
O
•
CU
>
„
o
CN
ca
a)
CO
C
O
ex
CO
CU
^1
cu
cd
ca
M-l
O
•
a)
£
„
^0
CM
CO
CU
CO
(3
O
ex
CO
cu
r-<
CU
cd
CO
M-l
O
•
cu
Cfl
„
OO
CM
CO
CU
CO
p!
o
p.
ca
cu
M
cu
co
M-l
O
•
CU
>
vfT
i— 1
CN
^-^
M
CU
•H
rH
cfl
>
cd
o
^
£j
^"»
t-l
*"CJ
o
4-1
vO
CO
CO
CU
rH
rH
CU
PQ
r*.
M
^|
cu
t-C
o
**^
4J
^"»
j^
t)
4-1
O
o
oo
CO
4-1
r^
V4
4J
O
0
r~-
CO
rC^rS
rH~
^^
LO
•
i-H
-P 4->
^ ^»
W M
'"U *T3
4-1 4-1
O O
O O
co m
^o r-.
Wi^
CN CO
**** s^
in m
« •
rH rH
>> M
rJ 3
3 i-)
•r-l (3
C -H
•H
&*s
6^9 OO
i— I ^-i
***S N— ^
•M 4J
& J}
J>^ ^*,
i-l r-l
rO t3
o o
ON i —
rH CO
r— 1 •*
cu
C
0
N
O
CU
4-1
3
O
^
M-l
O
CO
4-1
O
cu
i
13
CU
a
C
o
u
cu
o
N
0
Q
P
P,
*i
(3
O
•H
cfl
M
4-1
w
CO
cu
4J -H
(3 O
cd cu
rH P.
PM en
o o o
CN o
•H ^a
rH -H
O K
3 ""I
S b
O O O O
r-l CM -* OO
0 0 O 0
cu
t-l
a n
O r™
bOO
1|
C r^
m
CN
o
o-
o o
o o
•H CU
4-1 ^3
rH O
rj »
1
>
3
15
•H
4-1
rH
O O
n
cu
1
11-44
-------
CU
o
S3
QJ
ri
CU
MH
CU
O
oo
CM
O
00
CM
G C
O
&
ected Plants
rH
CU
C/3
MH
O
-d
rH
cu
•rl
r*~*
*^
rj
cd
f*j
4-1
[5
O
rl
O
&
O
CU
rl
^J
CO
0
P.
?
gxO
A
cu
co
G
O
p.
CO
cu
oi
4-1
c
cd
rH
PX*
CU
J_l
3
CO
o
p.
rH
O
rl
4J
C
o
a
0
O
M-l
C
0
•rl
4-1
a
rj
13
CU
rl
3
•n
•S
O
_£_
4-1
^
^>
^)
rrj
^J
CU
,£>
3
4J
•t
O
,J
<~|
«
CU
0
«^-
CU
rl
CU
CU
CO
3
't?
•H
v^/
4-1
IS
^
rl
13
^(
cu
3
A
0
CO
5
CO
v^/
-3"
•rl
O
ca
4-1
ca
•H
i
G
•H
O
S-l
00
^^s
4J
£j
^
rl
13
4-1
G
cd
rH
P.
«\
in
i — i
rH
•H
0
CO
4J
CO
•rl
i
3
o
S-l
00
^•^
4J
[5
K*">
rl
13
4-1
G
cd
rH
p.
A
o
CM
i— I
O
or
4-1
TJ
4-1
G
cd
rH
P.
G
•rl
^^
CU rH
CO -H
cd o
cu ca
^
o ^
(•4 W
•rl T3
•t
m
rH
i-H
O
rl
Jj
4-1
G
cd
rH
P,
C
•H
s^
CU rH
CO -rl
cd o
CU CO
^
a t^.
G rl
•rl 'rj
•\
m
CM
i-H
4-1
O
cu
MH
MH
CU
A
O
o-
CM
rl
3
•H
O
G
N— '
4-1 4J
& [5
^ ^
^•4 r4
TrJ rj^
4-1 4-1
C C
cd m
rH rH
a P.
*l A
ON CJN
i— i <^~
«— i -d"
4J
a
(U
4-1
G
O
a
rH
rH
^»
r\
P.
O
O
rH
rG
O
^
oo
CM
cu
G
O
N
O
CU
4-)
3
O
o
co
o
cu
w
4
p
G
cS G
O
CU -H
C 4J
O cd
N S-l
O 4J
o o
o o
o o
m o
O rH
o
m
o
o
CO
cu
4J iH
fi a
cd cu
rH &
AH CO
rl
Cti
•H
4J
O
•••a
0 C
4J Cd
Cd rH
4-1 ^1
O O
Q, £^
cd
•H
4-1
rH
O
rH
»rH
o cd
4-1 rP
cd cu
0 r4
O -H
H PM
ca
•H
rH
O
rH
o cd
4-1 ~Q
cd cu
0 r4
O -H
EH fi,
o o o
CM o o
O <—I i—I
o
CO
s
4-> cd
3 W
O
G
« cd
G -t-1
O rl
•H cd
C P,
O c/)
3
O
O
o cr
O 12
cd
o cu
L_j pp
ca
cu
CO
4-1
CU
M
cd
P.
T3
cu
IJ
0
G
CU
ca
•H
cu
4-1
o
ca
ca
cu
rH
fi
ED
G
•rl
CO
CU
M
3
CO
o
cu
<4H
O
S-l
cu
"0
3
11-45
-------
exposure and at 7 and 14 days for the double exposure. The greatest effect
•was found in the root growth from the triple exposure (7, 14, and 21 days).
The root reductions for the multiple exposures •were equal to the additive
reductions for single exposures. It was concluded that reductions were
a result of photosynthate going preferentially to top growth. Reduced root
growth rate was still found in the second week after exposure.
The studies of acute effects resulted in interesting growth phenomena
542
that require further study. Tingey e_t al. related foliar sensitivity in
the first trifoliate leaf of soybean to leaf growth, stomatal resistance, and
several metabolites. Maximal sensitivity occurred during the end of the
period of rapid leaf expansion, when stomatal resistance was low. However,
reduced sensitivity •was shown in older leaves when stomatal resistance •was
still low. They found no relationship between sensitivity and concentrations
of protein, amino acids, or various carbohydrates. This suggested that
metabolic pools •were not directly related to foliar response. Tingey and
536
Blum reported a consistent reduction in root growth that was related to
reduced nodule number in soybean. The ozone did not affect nodular activity
147
or size. Evans exposed pinto bean to acute ozone doses and found a
reduction in leaf expansion within 12 h (10%) and a 33% maximal reduction on
the day after a 0. 20-ppm exposure. Growth rate continued to slow 3 days
after exposure. He used the terminal leaflet of the first trifoliate for these
studies. A stimulation of stem elongation in tomato within 3 days after a
402
2-h exposure to 0. 30-ppm ozone and a predisposition to increased
sensitivity from acute ozone exposure after exposure to low ozone concen-
467
trations have also been reported. These are only some of the effects
seen. Similar results are reported elsewhere in this chapter.
11-46
-------
512
• Growth effects of long-term ozone exposures: Taylor gt al.
first reported a 52% reduction in the fresh weight of avocado seedlings
548
exposed to a synthetic "smog" (ozone plus hexene) for 280 h. Tingey et al.
found reduced growth in 2 soybean cultivars (Hood and Dare) after intermettent
exposure to ozone at 0. 10 ppm over 3 weeks. They found that root and top
growth were equally affected, but that roots were most affected when soybean
was exposed to a mixture of ozone and sulfur dioxide. They found similar
545
results with radish. Little injury was reported in either paper.
171
Frey reported a 55% reduction in seed yield of soybean with a 5% de-
crease in seed lipids and a 21% increase in free amino acids. This is one
of the few reports on quality changes in seed as a result of ozone exposure.
A 30% reduction in -wheat yield occurred when wheat was exposed at anthesis
481 423
to ozone at 0. 2 ppm, 4h/day for 7 days. Oshima reported a reduc-
tion in tomato yield at 0. 35 ppm over a long exposure period, whereas injury
effects were significant at both 0. 20 and 0. 35 ppm. He suggested an injury-
tolerance threshold for tomato below which one would find no yield reduction.
He also reported a decrease in kernel weight of sweet corn exposed to ozone
418
at 0. 20 or 0. 35 ppm. The reduced weight was associated with a shrivel
ear condition (kernels) that might relate to the effects of ozone on pollen
development.
91
Craker reported a reduction in petunia flower weight after a 53-day
93
exposure to ozone at 0. 05-0. 07 ppm, but an increase in petunia flower weight
was found in a 7-day exposure to 3 different concentrations. Carnations
continuously exposed to 0. 07-0.08 ppm produced a single deformed flower,
157
but the controls had 24 normal flowers. Poinsettia bract area was de-
creased by 39% after a 50-day exposure (6 h/day) to ozone at 0. 10-0. 12 ppm.
11-47
-------
22a
Bennett e_t aL make a case for stimulation of growth at low
concentrations of ozone. They exposed bean (cultivar Pure Gold Wax),
barley (cultivar Brock), and smartweed to ozone at 0. 03 ppm over some
growth stage and found instances of significant growth increases. The
concept needs further study in light of the current concern over "normal"
background ozone concentrations.
206
Heagle and associates found a reduction in yield of sweet corn
205
and soybean after exposure to ozone at 0. 10 ppm for 6 h/day over
much of the growing season. These exposures were carried out in field
chambers set over soybean plots in the field. They suggested that a threshold
for measurable effects on these crops would lie between ozone (oxidant) con-
centrations of 0. 05 and 0. 10 ppm for 6 h/day. These values are realistic
in terms of growing-season averages in the eastern United States. More
of these studies could help to clarify dose-response relationships for
economically important crops.
Table 11-5 summarizes these long-term, chronic studies.
194
Harwood and Treshow exposed 15 species, representative of the
aspen plant community, to ozone at 0, 0. 05, 0. 15, and 0. 30 ppm and ambient
air during the growing season and reported effects in all species at the highest
pollution concentration (Table 11-6). There was considerable plant variability,
and only 6 species reproduced. However, vigor was reduced and most species
441
were sensitive. Price and Treshow found major biomass reductions in
6 grass and 2 tree species exposed for 4 h/day to ozone at 0.15-0.33 ppm
over a growing season. They also found a reduction in or loss of some re-
productive components. These effects could result in subtle shifts in com-
munity composition after several years of ozone exposure.
11-48
-------
CU
o
CU
r4
CU
4-1
0)
tX
58
56
56
CO
m
CU !-i
rH 3
i~H *i"~)
o c
M H
4J
O cd
O iH
rH
60 cd
0-rf1
hJ rH
(U
4H -H
O ^
03 ••
4J J3
O 4-1
Q) &
4H O
4H 'H
fd CJ3
^5
•»
cu
03
C
O
P.
03
cu
4-1
P!
rH
P-l
rH
O
^4
4-1
P!
O
CJ
e
o
4H
pj
o
•H
4J
0
3
CU
60
P!
•H
VJ
CU
IS
0
rH
4H
A
VO
ro
• A
60
P!
•H
^
0)
O
rH
M-l
A
o
O
r- 1
s-^
13
CU
4J
cu
rH
P-
e
0
CJ
cu
M
3
03
O
PX
cu
^J
0)
4-1
4H
cd
V,
^
1 — 1
^-^
cu
4-1
cd
60
e
•H
H
3
O
''O
PI
o
4H
•V
o
J3
4J
>
O
M
60
CU
>
•H
4-1
cd
4J
CU
60
cu
>
T3
cu
o
3
T)
CU
M
^/
60
P!
•H
^1
cu
o
rH
4H
t\
O
m
60
Pi
•H
4-1
CO
cd
rH
!-<
01
S
0
rH
4H
M
CU
4J
M
O
A3
CO
^— '
s*~*
J3
4->
u
0
M
60
CU
>
•H
4-1
cd
4-1
CU
60
CU
>
13
0>
CJ
rj
4-1
^
A3
03
01
6013 M
P!
•H
M
cu
£3
o
rH
4H
A
O
m
CU
}_l
•I
01
6
•H
4-1
4H
}_l
0)
£j
O
rH
4H
•V
O
ro
CU
N
•H
03
4-J
CJ
cd
}-l
jjs
•S
O^
rO
cu
3
CO •
o cu
e
&
a g
CU P
o 3
o «
U P!
O
0) -rl
o cd
N V-l
O 4J
cd co
•^ cd
in ^
o
^H
O
cd
13 03
-* cd
CN T3
o
m
o
in
• cd
m
cd
03 13 CO
o
I
o
o
m •>
cd co
T) >>
-». cd ,
^*D ^
CO CO
cu cu
S-l J-i
4H 4H
4-1 4H
o cd
O 01
m
m
cd co
oo -a
CO 03
01 CU
J-l M
4H 4H
4J 4H
O Cd
O 0)
en CN
v£> CN
in
CO O 0)
O «w p<
o
o
m
o
o
o
m
o
m
o
CO
0)
4-1 -H
a o
cd cu
rH P
P-i CO
CU
(U
a
13
cd
I
Carnation
Geranium
Petunia
Poinsetti;
03
•H
T3
11-49
-------
CU
o
c
0)
JH
0)
CM
co
co
~,
CU $H
rH 3
rH -n
o a
rl M
4-1
rt ^
o cd
O -rl
rH
go
PH
CU
VI
60 cd
C •>
O rO
1-4 rH
cu
MH -H
O £H
CO •>
4-1 ,£
a 4J
cu £
IH o
i_|.-j l_|
w o
rH
O
rl
4J
sponse, %
n from cor
cu o
Pi -rl
4-1
4-1 O
C 3
Cu • O
rH CD
p_j ^_j
cu
!-! ,fl
CO «
fti
as
1
C B
CU p.
0 ft
rt
o •<
U PS
0
CU iH
C 4-1
O cd
N rl
O 4J
4-1 4J
4J
4-14-1 4J J5
O O &
4J O 0 ,C
& }H >-l ,C CO
CO CU
>-. CU CO CU M
M 60 3 JH MH 4J
13 Cd O 14H ,£
i-l M 4-1 60
ft O fi ft O -H
O 4J -H O O CU
4J CO i+H 4J SH f\
o o r~ o> co o
in ^J" ^o r*^ r*^ r^
oo oo
CO CM
>-! !>•!
cfl co cd co
rO r** ""O ^*
*-» cd ^ cd
CO T3 00 13
O CO
CM rH
• •
O O
:e (chlorosis)
> in lateral bud
U W
p! co
cu cd
CJ CU
CO \-t
CU CJ
Cj (5
0) -H ,-N
co C
id o
<4H rH -rl
Cfl 04-1
CU >4H cfl
rH 0) 60
. -H §
•* n cj
O 14-1 rH
in ^ cu
in
I
co in
* hT
cd cd
13 CD 13 CO
CM 13 CM 13
m in
o o
• •
o o
4-1
13
CO
cu
4H
O
vD
4J
rl
13
4J
C
cd
H
ft
CO
CO
CO
vO
>>
cd co
'O K^
CM 13
in
rH
•
O
4-1
& &
rC CO
co cu
4H
13
rCJ O
0 ft
ft
•• o
c^ o
C^ *-H
4J 4-1
rl M
13 13
4-1 4-1
C G
Cd Cfl
rH H
& ft
in r^
CTv C^
CO co
\^5 vO
>> >,
cd co cd co
^-^ cd -^ cd
CM 13 CM 13
m in
CM CO
• •
o o
(Data available on
whole plants, roots
leaves, injury, and
4-1 4-1 |5
* * r?
M rl 13
13 t3
•4H
14H HH Cfl
Cfl Cfl CU
CU 0) rH
rH rH
« ^ CO
00 CO CM
*3" *J" *^"
rH t— 1 1— 1
>%>••>•>
cd co cd cfl cfl co
*^^ cd ^- cd "^ cd
CM 13 co i3 <)• T3
in m in
rH rH rH
• • •
O O O
3 levels of soil
moisture stress)
i
4J 4J
rl tH
13 13
MH m
cd cd
cu cu
rH rH
oT *
*j" > >~.
cfl co cd en
-^. cd -^ ca
v£> 13 CM "VJ
m
>n CM
rH CM
• •
o o
co
cu
4J -H
a o
cd cu
rH P.
P4 CO
a
cu
13
M
cfl
00
4-1
CU
CU
Pfl
cd
•H
4J
H
O
« O
c *->
Id a
CU iH
M PM
4J
rH
„ o
cd C
CU -H
pq P-i
!H
cfl
•H
4-1
U
« o
c ^
cfl fi
cu r1
PQ CU
* O
M
11-50
-------
4J
O
O
CO
H
cfl
co
CU
rl PM
CO 13
o cu
w cu
rH
Q) CU
(3 c/>
O
N O
O 4-1
CU rl
^ rH 3
H -n
in O 13
I rl H
rH 4J
rH C rl
O CO
CU O -rl
CU
H 13
60 CO
cu
MH -H
O >H
CO "
4J 43
O 4-1
CU &
<4H O
MH rl
W O
B-s
A
CU
CO
o
ft
CO
cu
4J
a
cfl
rH
PH
CU
}H
3
co
1
C
cu
CJ
C
0
O
cu
C
0
N
0
4-1
rj
cfl
rH
0)
a
g
rl
CU
MH
QJ
rH
O
M
4J
£3
O
0
o
<4H
13
O
•H
4J
a
3
t3
CU
rl
(Data available on 319
whole plants, roots,
leaves, injury, and
3 levels of soil
moisture stress)
* s s
rl rl rl
nj *"Q rO
<4H <4H <4H
cfl cd cd
cu cu cu
rH rH rH
A «v «\
CO O VD
vo st r-~
43
•H
H
S
A
a
«
c
o
•H
4-1
cfl
j_i
4-1
*
• cfl ^
CN 13
0
CM
e
0
M
CO
CU
rH
o
ft
^
O
cd
£3
o
H
oo
1— 1
4-J
rl 4-14-1
rl cT 00
*"O CNj "*^
O 4J
4-1 S
* !>i
CN rl
.ft rH
13 CU
rH 13
CU !H
•H CU
^ M
ft ft
in co
*3~ t — i
«^-
CO rH
ft ft CO
cd S «
13 -» >>
— .03 cd
m >, 13
* • cd Ai ^
S CN 13 IS CO
in o
CO CM
9 v
0 0
J_J
cd
^
4J
rH
3
CJ
*t
4-J
cu
cu
^
CO
ft
(3
M
O
4-1
4-1 4-1
rl M
13 rH 13
CU
4-1 P! 4J
0 rl O
0 CU 0
JH v^ M
ft
0
CN
rH rH
rH rH
•H -H
4-1 4-1
ft CO «
AS 4J AS 4J
> CO « & CO
\ (U >,-^. CU
CO > cfl 03 >
>> M 13 f^ rJ
cO CO ^ — cfl cfl
13 43 co 13 43
LO
OO
0
0
cu
cu
rH
•H
ri
3
h-^
c
cu
rH
cS
00
^
ft
cd co
»-. CO
"J" *"O
o
CN
f
O
SH
cfl
^
•rH
4-J
H
3 H
O r^
- rl
4-1 3
cd 43
CU 4-1
1 <
/•N
CO
•H
CO
cu
43
4-1
Cfl
oo
4-J
CO
CU
WH
ft
O
4-1
„
CN
m
•*
1
co
in
o
o
rj
§
cu
ri
o
w
4J
CO
cu
rl
<4H
4-1
O
J-l
A
^j-
CN
CO
ft
A!
&
CO
o
B
0
4-1
43
co
cu
rl
MH
ft
O
ft
rH
CN
*
11-51
-------
cu
o
a
0)
rl
CU
03
i—
oo
uo
CM
•
4-J
e
o
u
N»X
in
1
i — i
•— i
cu
rH
O
CO
H
one Exposures on
N
0
13
cu
rH
rH
0
rl
4-1
c
o
u
cu
H
1
60
C
O
"""
m
o
o Selected Plants
J-J
K*^
M
^
«| — )
pj
M
H
03
-H
rH
o
fe
13
rt
A
13
rH
cu
•H
^
esponse, %
Pi
4-1
d
cO
rH
PM
cu
rl
3
co
o
ft
w
on from control
•H
4-J
O
^
T3
OJ
}_i
4-J
&
CO
CU
14-4
4-1
O
0
M
n
^)-
CNJ
j
«t
cu
e
f— t
<4_^
O
cu
^
^]
4-J
X
•H
e
4-J
f
CO
(1)
14-1
ft
O
4-1
9\
CN
r-H
O
cn
>-^j
d
o
crease in shoot: root rat
eatest effect on roots)
G M
•H 60
V •
•N
O
CO
CN
CU -^
g CO
CO 13
to o
•H
rl rl
CO O CU
M-l ft
4-J 4-1 4-1
^^ ^> ?*^ CO
13 T3 13 cd
ft ft ft O
0 O 0 -H
4-1 4-J 4-J J2
91 «\ #v «N
vD vO C^ CO
r-4 CN CO OO
1 — 1 1 — 1 1 — 1
CM CN CM in •>
A! 60
** ** ** ** L? t~i rt
K^> K^ t*i ^> ^ - *rl O
cdencOcocdcQ coco&en
13 ^t "^3 ^i "^ ^> *^3 ^» O cO
^^ cd — ^ cd *^^ cd "~*^. cd J-i CU
CMi3CNli3cNi3
o
**~s
r^
Jj
vHj-
*\
^
£5
*^
CO
>>
03
TJ
cu
rH
-U
4_)
§
cu
rH
13
cu
cu
c
*
**0
I— 1
M-l
O CN
O
CU CO
S 13
4-> C
X cd
•H
0 m
v-' 0
CU x— s
e eo
cd 13
eo o
•H
J-i M
O CU
»4H ft
CO
•rl
CO
CU
-C
4-1
CO
O
4-1
O
ft
•s
cd co
13 K*^
~- cd
cr\ 13
tosynthesis
0
Xi
ft
«*
LO
CN
O
CM
f,
j>^
cd eo
rrj *>*,
CO
c^ *"O
en •>
4-1 Xi
O 4-J
cu &
<4-> O
m j-i
w o
C 0
cu ft
a ft
o *
o e
o
cu -H
a 4J
o cd
N J-l
LO
o
o LO o
r-l 1—I CN
o o o
CO
CO /—s
• 13
o cu
I -H
LO J-l
rH Cd
o
rH
o
in in
rH rH
O O
CO
CU
4-1 -H
a o
cd CU
rH ft
PM co
«
cu
c
c/o
cd
UH
rd
14H
CU
o
co
co
cd
!-i
O
C
M
cu
4-J
en
nj
cu
». CU
CU 4-J
C -H
•H X!
CM &
rd
CO
o
rl
CU
"S
o
ft
PM
11-52
-------
CU
u
c
cu
M
CU
M-l
0)
vo
CN
\O
CM
-a-
VD
CM
o-
^D
CM
/— N
t
4-1
a
o
o
If)
\
i— i
i — i
CU
rH
42
crl
CO
H
CO
C3 4-J
0 C3
cd
M rH
CU PH
3 *"O
CO CU
O 4-1
ft 0
f3 rH
CU
cu c/3
C3
0 0
N 4-1
o
13 r-l
CU 3
rH -r-l
rH C3
O H
}-l
4J M
C cd
0 -H
O rH
o
0 Pn
CU T3
H C
1 cd
60
C3 -
o *x)
cu
MH -H
O J>-f
CO ft
4J 43
U 4->
CU £
M-l O
1 | l t_j
w o
0
4J
c
5-S O
CJ
dT 0
CO O
P w
O MH
co c3
cu 0
Pi -H
4-1
4J CJ
C 3
cd T3
rH QJ
PH r-l
0)
CO "
o cu
ft 0
fjH £-(
1
f3 6
cu ft
O ft
c
o •>
cj £
o
CU -H
C3 4-1
O cd
N r-l
O 4J
CO
•H
CO
cu
p.
^
CO
o
4J
o
ft
*
in
CM
o
CO
>>
cd
13
CT\
m
F-H
•
0
CO
•H
CO
CU
a
^*>
CO
o
4-1
O
ft
«v
X^J-
CO
o
*sO
t^
CO Cfl
^i T3
cd ^
in
r-H
•
O
CO
•H
CO
cu
p
P-I
CO
0
4_)
O
43
ft
*»
CM
i— 1
O
1— I
>^
co nj w
K*1** "^ ^*>
cd "^^ ctf
*"O C3*\ r^
o
CO
•
o
CO
•H
CO
CU
rt
p^
CO
o
4J
o
43
ft
A
O
o
CM
>-.
cd
13
-.
co cd
^» *T3
cd ^.
o
CO
•
0
CO
•H
CO
CU
43
rt
^»
CO
0
4-1
0
43
ft
ft
in
oo
o
CO
>>
en cd co
t>» n3 ^»
cd -^ cd
in
^j-
•
0
4J
43
60
•H
43
•t
0
• n
0
M
**o
M-i
cd
CU
t — j
ft
CM
00
CO
i — I
in ft
Ai
I^JJ
Cfl CO
•^^ Cfl ^
OO 13 £
O
CO
•
0
4J
43
60
•H
CU
43
oo"
.«
0
(H
M-t
d
QJ
f— (
**
o
m
CO
,—1
in "
^i
f^-2-
cd co
rrj ^y,
"^^ Cfl ^
OO TJ |5
O
CO
•
O
4J
43
60
•H
CU
43
«\
O
O
J-J
rrj
MH
cd
CU
rH
ft
**o
vD
CO
1 — 1
in ft
AJ
;^J^
Cfl CO
TJ ^l
"^ Cfl ^
OO T3 U
o
CO
•
O
4J
43
60
•H
CU
43
ft
CM
CN
• ft
ft
O
M
T)
MH
cd
cu
rH
ft
o
CO
1 — 1
in ft
^
K"-^.
cd co
13 r^
^ cd
OO 13
o
CO
•
O
CO
0)
4-1 -H
C cj
cd 01
T-H ft
PH
Cd
CO
O
t3
O
ft
CU
C
•H
o
rH
rH
CU
S-i
cd
ft
o
cu
rH
ft
43
CO
cu
)H
cd
CJ
&Q
11-53
-------
CU
o
c
CU
rl
cu
4-1
0)
PS
«\ ^
K^l ^^
CO CO
'd p^*
<%^. cd ^
oo 13 B
3
•fi1
•H
-* CO
rH CU
CO
•« fi
4J O
S ft
ca
>. cu
13
13
CU CU
C -rl
M >>
^ ^J-
A
CT»
^*
^O
^
K*l
Cfl CO
nrj ^
~^ Ctf
me responses
cO
CO
rl
0
in
CO
*«
m
CM
«\
m
o-
^«
v0
r\
^
cO co
rd K^I
"^•^ cfl
\O TO
CO
CU
rl
<4H
C
Cfl
rH
ft
A
CM
CM
• A
13
CU
•rl
^ ^
rl
13 3
CU -T-)
Q) £
CO -rl
•\
CO
CO
CO
1— 1
n
>>
rcj co
*""••** cQ
vo ^
me responses
cO
CO
rl
O
f^.
CO
•X
m
**
m
in
CO
CO
1— 1
•\
>.
tO
•v^
\Q
me responses
cfl
CO
rl
O
>4H
vO
^«
fi
m
«\
CO
4H
O
CU
rl
4-1
CO X
cO €
•"O ^— ^
cO
cu
CM
O
CO CU ^>
3 CO
C CO 0
cfl -H
CO O CU
O m ft
13
m 4J
o
4-1 4-1
O &
O
.fl !^
CO V-t
O
m
m ••
n5 co
13 >>
--~ cfl
CO TJ
fi
o *
o fi
o
CU -H
C 4-1
O cfl
N V4
o
CO
CO
cu
4J -H
G O
CO CU
P-l C/l
V)
cfl
60
a)
rH
ft
in
o
)H
cfl
3
UQ
4J
•• CU
4-1 00
CU 13
CU tH
en
fi
~ cu
t-i *"O
o o
u o
m o
O rH
o
I—I
o o
in
•
o
(-1
cfl
3
o
a
n)
QVQ
,0 cu
t^ rl
O CO
T)
•H
rl
rl
Cfl
rH
ft
O
PH
O
rl
4J
C
o
o
cu
rl
CO
CD
o
4-1
T3
cu
CO
o
rH
a
cu
CO
4J
c
cfl
rH
ft
4-1
Cfl
4-1
ft
CU
O
X
CU
CO
C
o
o
o
13
rH
cu
CU
CO
cO
CU
u
o
fi
•rl
>.
r-l
fi
O
dJ
^(~J
H
CU
13
C
3
13
CU •
4J CO
0 CU
3 co
13 O
C -d
o
O 4J
c
CO cfl
CU 4-1
•H 3
13 rH
3 rH
4-1 O
W ft
•Q
11-54
-------
vO
1
i — l
CU
rH
n
cO
H
f^
•H
C
3
^3
O
CJ
£*
cu
ft
CO
.
O
4J
CD
^_l
CU
T)
fJ
£3
"X?
cu
4-1
O
cu
rH
CU
CO
c
0
cu
£
o
N
O
o
CO
4J
0
CU
>4H
W
rQ
CO
a
o
•rl
4-1
CO
4-1
C!
cu
CJ
C
0
CJ
0)
p)
O
N
0
4-1
C
CJ
J_l
cu
m
UH
•H
p
4-1
cfl
0)
CO
C
o
ft
CO
CU
Pi
4-1
C
cO
rH
PL,
rH
o
M
•1— )
C
O
O
UH
O
&~S
A
4-1
|jg
T3
Q)
CU
CO
a
p
p
O
ro
•
0
a
P
&
in
i — i
o
B
ft
ft
in
o
0
* *
r~- I I vO 1^ ^3" OO
p^« CN *^~ o** r^» co
00 CO 1 I C^ r^ CN CT»
1 — ( 1 — I
rH
O
J-,
4-1
C
o
CJ
MH
0
&*s
ft
4-1
£2
4-)
c
CO
rH
PH
a
ft
o
CO
•
0
a
P
m
i — i
•
0
a
ft
LO
o
o
******
COCNvO ro >— 1 CO CT> in
oo co m m co >-H CN
* * * *
i — i oor^ -i 0)
M Q)
Q !_i
CO
cu
4-1 -H
c o
CO CU
rH ft
PM CO
J
•H
B
•H
TJ
o
ft
§
CU
CJ
•rl
4-J
rj
0
•j §
§
J2
rH
CO
IM
•
O
(J ' _1
^J . 1 -rl
CO
•H
c
•rl
2
O
CO
cu
p
*H
** ^*> ^
•r-J rrt d
•H
S
• M
ft CU
co O
•rf
4J
I
cu
MH
S
"•3
. T3
CO
cO
4-1
CO
rl
Cfl
•H
T3
S
1
0
H
M
B
C
o
rH
0
PL,
CU
M
cfl
rH
3
•H
CO
CO
rH
M
o
PM
J-
cr>
§
J2
CO
0)
1
13
>-!
cO
a
o
M
MH
CO
4J
cO
p
c
o
co
cO
CU
CD
M
O
rJ
M
60
O
cfl
13
cfl
13
CO
CD
cu
4-J
CJ
0)
MH
MH
CU
4-1
C
cO
o
•H
•H
C
00
Cfl
CU
4-J
Cfl
O
•H
13
C
•H
CO
•H
3
CO !H
O CU
ft 4-)
X CO
W
-------
The results of these experiments suggest that overall economic effects
on agricultural production could be extensive, depending on the sensitivity of
cultivars used in production, and should be considered in the attempt to arrive
at valid economic-damage functions for vegetation.
Factors Affecting Plant Response
The sensitivity of plants to ozone and PAN is conditioned by many
210
interrelated factors. Heck reviewed these factors and found that our
understanding of the importance of any given factor on plants was fragmentary.
Since then, a new body of research has become available that permits a more
concise discussion of many factors that affect the response of plants.
Although the response of a given plant is not predetermined by the response
of related plants, sufficient information to predict relative responses under
given sets of conditions is available. Information to predict interactions
between variables and to predict whether species respond the same way to
environmental factors under different pollutant stresses is not available.
Current research demonstrates our inadequacies in understanding interacting
variables.
Before we can predict the response of a plant variety to a specific
pollutant or group of pollutants, we must understand the following factors:
genetic variability (both between and within species), climatic and edaphic
factors, interactions with other pollutants, interactions with biotic pathogens
and insects, and the growth and physiologic age of susceptible plant tissue.
The overall conceptualization of relationships between pollutant exposure and
ultimate effects is shown simplistically (Figure 11-1) in an adaptation from
572
van Haut and Stratmann.
11-56
-------
POLLUTANT
CONCENTRATION
NUMBER OF
EXPOSURES
DOSE
CLIMATIC FACTORS
EDAPHIC FACTORS -
BIOTIC FACTORS
X t
^ PLANT
""^RECEPTOR
MECHANISM OF ACTION
I
EFFECTS
I
ACUTE
CHRONIC
DURATION OF
EACH EXPOSURE
GENETIC MAKEUP
.STAGE OF PLANT
DEVELOPMENT
SUBTLE
Figure 11-1. Conceptual model of factors involved in air pollution effects
on vegetation. Modified from van Haut and Stratmann.
11-57
-------
Genetic Factors. Knowledge concerning the influence of genetic
variability on plant response to ozone has been obtained from both field
observations and chamber experimentation since the mid-1960's. Similar
information on PAN is scarce, but several published reports are available.
Resistance to ozone and PAN varies between species of a given genus and
between cultivars within a given species. Variations in response are
functions of genetic variability and environmental stress as they affect
morphologic, physiologic, and biochemical characteristics. In native
populations and in breeding experiments, both ozone and PAN may act as
selective pressure stresses.
Variations in species response to ozone and PAN are well
235, 236, 269, 301, 401, 506, 510, 593a
documented. A list of species suscep-
tibilities to ozone is found in Table 11-24, which was generated from results
of controlled exposures and the use of the sensitivity table, Table 11-23.
210
Heck summarized variations in cultivar responses of several
445
species. Reinert developed a compendium of research papers covering
horticultural cultivar responses to ozone, PAN, and other pollutants that
is complete, but gives no summary of results. A number of papers have
49
been published since Brennan et_ al. first published their results on the
separation of oat and potato cultivars exposed to ozone and stressed the
importance of cultivar differences within species. Additional ozone studies
109 5 400 48,
are available for bean, begonia, morning glory, chrysanthemum,
284 340 338 449 449 44
poinsettia, spinach, lettuce, radish, turfgrass,
52 257 256 254,382,546
forage legume, alfalfa, safflower, soybean, small
477 47
grain (oat, rye, wheat, barley), and English holly. Petunia was
162
studied with auto exhaust and PAN, and both petunia and chrysanthemum
11-58
-------
128, 593
have been studied with PAN. Screens using ambient oxidant
conditions, sometimes without pollutant concentration, are fairly common:
247 42,247,310 226,247,355,362 310
bean, potato, tobacco, petunia,
310 63 273
poinsettia, sweet corn, and grape. Most of these studies used
acute exposures, which may or may not relate to results from chronic
exposures. Some reports of ambient oxidant exposures covered part or all
of a growing season. These screens used injury as the response measure.
We do not know whether foliar injury ranking relates to economic yield
loss ranking.
Cultivar variations in three species have been intensively studied in
5,67,162 75,76,177,
relation to their sensitivity to ozone: petunia, tomato,
448 115,181,226,239,358,361,362
and tobacco. These studies have resulted
in recommendations that some cultivars not be used in areas of high oxidant
potential. The susceptible Bel W tobacco is widely used as a biologic indicator
3
of oxidant.
A summary of cultivar responses to oxidants, ozone, and PAN is given
in Table 11-7. Summary data •were also included in the development of the
dose-response equations and Table 11-24 on plant sensitivities.
188
Hanson presented a list of 160 woody species from observations
at the Los Angeles State and County Arboretum that were sensitive or tolerant
to oxidants. Several recent investigations have considered susceptibility of
264 25
tree species to ozone. Jensen studied nine hardwood species, Berry
107, 112
looked at three pine species, Davis and Wood reported on 18 con-
373
iferous species, and Miller reported on 15 western conifers. In general,
selection within natural tree species has not been studied.
11-59
-------
cd
H
PH
cu
a
o
N
o
CO
cu
•H
o
cu
P.
4-1
•H
tfl
•H
S
cu
CO
CO
cu
cu
0
0
CU
cu
cu
ON m r^»
ON ON O ON St
Sf St rH St CM
Sensitive,
Resistant
Cultivars
o
j-i
4J
0
B^ 0
O ^
ft •
4-4 1
ft 0
co 0 cd
cu o cu
aj -H S
4J 1
4-1 O o
030
cd T3 -H
iH CU B
PH rl ^
I— 1
r^ ft
CM O
r-~ VH 0
C.I. 7540, C.I.
Chippewa, Avon
Sanilac, Tenderc
Sanilac, Tempo
Norchip, Katohdi;
0)
rO
^™\ *~*< t*~* *r!
^> ^» /*-"N ^i 4—1
3 3 rl 3 CU
•j—) •!—> ;3 -r-> cj
C C •!-) 0 co
•H -H 0 -H 3
\^ **s *,^<^ CO
ON O st O
VD LO CO *.O "I-J
CO
II 1 4J ,->
i a >•>
oo m r— cd s-i
CO rH 00 CO J-l 3
CU -r-i
1 1 1 1 -H C
O -H
O O —1 ON H •-'
Q
0
T3 0
0 O
cd -H
4-J
4-1 Cd
0 rH
Cd 4->
4-1 0 ,0
3 CU
i-H U «
i-H 0 S
o o a
PH U P.
CO
cd
•H
4-1
. T-{
0 3
3 u
O
CO
CM Cd
st st st CU
•> CO
ft ft ft CM
CM CO in rH »
CM CM CM • 4-1
• • o o c
o o o n)
" "T3
CO CO CO ^ J^
O O O PH O
ON OO O O vO
rH i— 1
CM
Haig, Superior
^
^s,
«J
3
C?
•H
v— '
00
ON
1
v^-
LO
1
o
l
CO
ft
in
rH
ft
4J
0
cd
T3
•rl
O
^j-
CM
O
rH
CO
g
3
r-l
PH
0)
r-l
&
s
•v
cd
4-1
to
cu
•rH
Pn
CO
cu
ll
iw
ft
o
4-1
I— I
CM
1
in
, — i
4-1
0 &
a
rj
O
CO
cd
CU
CO
^ „
Ctf 4J
CU 0
ft cd
T3
>•> -rl
•3
i .
13
ft
0
4-1
O
m
1
ON
CO
' 4J"
r- >
CM
O
00
O
CO
O
CO
m
, i
51
Capri, Canadian .
Double Mix
^"»
< i
T3
ft
O
4-1
O
st
1
ON
i — 1
4-1
ON £
CM
O
oo
0
•V
CO
O
CO
CM
vO
r— 1
CU
£j
Festival, Lilac
/•— v
>>
•i—)
0
•rl
00
CO
1
CO
CM
1
i— 1
, — |
O
0
r-l
CO
O
sj-
I— 1
CM
vO
rH
V/»
0
•H
PH
•H
4J
U
cd
PH
f\
CU
rP
1
Q
CU
H
PQ
/— ^
^>
3
•n
0
•H
^j-
CM
1
in
rH
1
^
1— 1
f
in
CM
.
O
•>
1
vO
CM
VO
rH
•H
4-1
M
cd
White Cascade, P
Pink
^— s
K.
M
3
•n
0
•H
"^
m
^j-
1
CM
, — i
1
CM
«v
in
rH
.
O
ft
4-1
cd
32
in
rH
oo
CM
i — l
O
•H
00
cd
E
rH
cd
t-l
0
O
A
4-)
M-l
•H
13
1
^f^
r?
3
•r->
^j.
PH
00
CM
otv
CM
O
oo
r^*
*"O
ctf
Tranquility, Ann
/— •*,
^s
3
rj
•A
^
O
p^
r
CO
CM
1
O
CO
O
O
CO
O
in
CO
m
4-J
•H
CU
rH
A
CU
0
O
^•^
rl
3
"r"1
•rl
"^-^
in
I
o
1
o
Si-
ft
v£>
•
O
A
§
00
oo
st
0
cd
•rl
Golden Arrow, In
Summer
,—*
^
^•i
•in
0
•H
^~*
m
vO
1
in
CM
l
o
rH
St
O
•*
O
CO
O
VD
rH
O
sj-
CO
cu
4-1
£
oo
co
•
CO
$
Eckespoint C-1, ft
Annette Hegg
Virginia Blight
Savoy , Bounty
'""'^
^i
rH
**— )
0
^J,
CO
vO
1
in
CO
1
VO
st
m
CO
o
CO
O
m
s^
r^
rl
3
•r~i
0
^
O
in
1
in
CM
1
m
st
m
rH
o
CO
0
vO
ON
st
st
4-J
Cd
CU
rH
O
0"
O
4-J
CO
O
0
CU
CU
o
CO
rW CU
« cd
Q rJ
r-N
^>
^|
3
0
•rl
*°~*
VO
st
1
st
CM
1
O
i— i
in
*
rH
O
•^
0
CO
O
OO
ON
St
st
cu
i — i
o
•rl
O
H
A
rH
rH
CU
PQ
CU
/•^
^t
^H
3
0
•rl
N— s
in
CO
l
in
CM
1
r^.
rH
m
.
r— 1
m
CO
o
CO
0
ON
CO
cu
4-1 -rl
0 0
cd cu
•H p.
PH C«
O
4J
cd 0 0
4-1 4-1 Cd "J
cd o cu
-------
4-J
(3
O
O
cu
£3
O
N
O
o
4-J
CO
CU
•H
O
CU
ft
CO
•3
H
CO
r-l
U
14-4
O
CU
CO
fl
o
ft
ca
cu
Pi
cu
o
G
CU
r-l
cu
cu
•V
CU 4-> CO
> t3 r-l
•H cd cd
4J 4J >
•H CO -H
CO l-l 4-1
G CO H
CU CU 3
co pi u
H
o
r-l
4J
G
tNJ O
0 x-v
•* •
co o cd
G n 0
O M-4 I
ft G
co G cd
cu o cu
Bi iH 0
4J 1
4-J O •
G 3 C
cd TJ iH
rH CU 0
P-I r-l v— '
T3 G"
G 0
cd -H
4-1
4-1 Cd
G r-l
Cd 4-)
4-1 G JS
3 CU
rH O •
r™l G 0
O 0 ft
P-i U ft
CO
cd
•H
4J
• I— 1
• ^H
0 3
i2 C_>
oo r-
33 CM in
^•^ O^
4V #V pN.
t> > 0
CO •
eg cd cu ft
00 0
q q • -H
Pi pi nJ ft
X~S
r*1 X"N
r-l r^>
3 r-l
•n 3
C -o
•H C
V ^ - 1
v-x
oo m
r^.
l
l
m
CO O >-.
in M
1 3
1 n
0 G
rH in H
m m
• • cu
rH rH rH
O
•> •> cd
o in -H
-d" CM r-l
• • cd
0 O >
CO OO OO
0 0 O
CM st CO
rH CM VO
vO ^"
r~-
J_J J_(
3 3
•n T-)
G C
,_J ,_l
"M n
^^/ \,^/
m o
1 1
O 0
-d- vo
1 1
o o
m
•
rH VO
•k ft
m o
CN CO
0 0
OO (
0 0
in »~H
o^ r-^
CVJ
CNJ
LO
r^
cu
Prf
rO
G
cd
rH
c
(U
fs/^
A
rG
U
4J
CU
>
o
r-l
C_>
X"N
^
JH
3
n
.s
O
m
l
0
i—4
l
o
- (
0
^
ft
ftO
CO rH
^
r**
in
CM
1
PQ
CO
S
**
cd
CO
•H
CO
M 1 CN
cu G
> cd
C G
•H -H
^x^x
CO CTt
r~- r^-
1 |
m -*
vO vo
1 1
CM m
CO -
•
o
A
^.
m co
CN ^O
)_i
cu
rH
4-1
3 CO
CJ CU
0
. cd
4-1 C
Q) O
>sxj J^
>->X-v
r-l t>-i
3 >-"
•n 3
•S t?
>~"H
(Ti
OO 00
Ox
1
( .
m sr
«,^
i
V.Q
H in
o
CO
CM O
A
^
O •>
m 4J
• C
o cd
rQ
•s *|-|
oo oo oo co bd
0 O O 0 O
CO
V^
cd
cu
oo
1
p^
00
rH
r-l
cu
o
*t
m
4-1
J3
oo co
cu o
ft -H
CO 33
X£
?-<
3
•i—i
5
^-'
CTi
in
l
m
1
i — i
CN
CO
A
o
ft CM
•
>,0
cd
*"U
1
CO
•t
00
0
00
m
CO
r-l
CU
o
u
*
CO CO
O O
•H
-M p"!
rC
00 1
•H
CU I~-
ft 00
CO rH
~
i-i
3
^
^^
r^.
oo
1
oo
vO
1
oo
CO
in
CM
*
vO
CO
•
O
•t
OO CO
0
m
m
CO
00
£2
rH
(U
pq
CTi
1— 1
1
o
vO
cd
PH
^
J-l
3
•r-l
G
•H
m
vO
|
VO
i — i
1
rH
Q
/"""s
cu
rH
rH
•r-l
4-) >
G CQ
cd 4-1
13 rH
•H CU
m
rH
1— 1
CU
1
CO
cu
•H
41
Q
ft
O^
•xj-
•
g
o
°
*
r-l
3
•r-i
C
"•-^
O
CO
1
o
CM
1
O
rH
O'
•t
vO
O
•
O
*
rH
OO
I— 1
C
1
cd
CO
cd
CO
o
G
•H
3
rH
(30 X-N
• §
sz ^
^
r-l
3
•H
CM
in
l
r-l
3
G
v_x
CN
*^-
|
CT\
1
"*
CO
v-'
vO
* X-N
in co
CM >-,
• cd
O T)
•I
oo
O
vO
CN
CM
CU
rH
o
n3
&
A
u
1
rH
CU
pq
^
3
'G1
•H
CO
r^*.
1
i— *
m
1
"*
*3
/0?
H
rH
•H
4J >
G co
cd 4-1
T3 rH
*H (U
c§ S-
c^
CO
CM
rH
O
m
cd
G
cd
^
cd
33
„
CM
rH
cd
G
g
cd
33
x-\
M
3
•n
.5
^
r^.
CO
1
CM
CO
1
p^
rH
in
rH
A
O
CM
•
O
«t
(
0
CN
CN
CO
m
m in
m
CU
CO
CU
4-J -H
C 0
cd
cd
£3
o
H
O 0
4-1 4-1
cd td
S p
0 0
H H
O
4-1
cd
£3
0
H
CO
co
m
M
00
4-1
H
Z
CO
cu
0
!3
00
cu
rH
0)
00
cd
M
o
cd
M-l
H
cd
M-l
5J
M
0)
O
rH
<4-l
m
cd
CO
c
cd
cu
fl
^»
o
CO
G
CU
tD
>-.
o
CO
c
to
o
C o
cd
CU 4-1
rQ CU
>> cu
o S
CO CO
3
a
1
cu
3
rH
MH
•V
0
O
o
cd
,£>
O
H
g
O
1
(U
3
M-l
A
O
o
0
cd
o
EH
rH
fl
cd
•H
r-l
cd
>
««
o
o
o
cd
0
H
r-l
cu
ft
ft
cd
H
is
A
o
o
a
cd
0
EH
C
cd co
r-l
• cd
ft >
ft -H
CO 4-1
H
* 3
O O
O
O T3
cd G
| *
O
a
a
cd
0
H
o
o
o
cd
0
H
o
o
0
cd
,0
o
H
11-61
-------
0)
a
G
ai
CM
vO
ro
4J
a
o
u
•s
H
cfl
PM
0)
§
N
O
CO
OJ
•H
U
CD
O.
C/D
fi
•rl
J=
4J
•r!
a)
CO
a
o
P.
CO
•k
CU
•S
4->
•rl
CO
PI
CD
Crt
B~S
•t
cu
CO
0
p.
CO
cu
prf
4J
a
cd
rH
PH
T3
s
cfl
4-1
a
cfl
4->
3
H
rH
o
PH
4-1
§
4J
CO
•H
CO
•H
4J
rH
3
U
x-^
•
X
ctf
?
C
cfl
CD
s
T
•
a
•H
s
x_^
^2
*l
e
a
p
CO
V-i
cfl
>
•1— 1
•PI
4-»
i — 1
3
CJ
CO
CD
•H
0
CD
PJ
C/J
a
0
en
rH
•rl
&
A
a
o
4J
M
cu
4J
4-J
Cfl
U
/— • \
>>
M
3
•r-)
C
•rl
V— '
00
CO
|
m
M
cu
)-l
CD
>
CD
CO
o
4->
O
13
C
ctf
•
>H
•
a
-^«
/^N
4J O
C -rl
ctf !H
T3 cfl
•H 4J
>< c
0 0
-*
rf*
r1 )
r— I
CD
Pi
Ctf
SM
0
>,
rH
1
1^1
O
JS
CO
•H
rH
60
C
W
CO
4J
o
0)
4-1
U-l
0)
o
a
r-~
«\
0
in
•
o
•*
o
CNJ
>,
rH
rH
O
EC
4J
C
cfl
4-1
CO
•rl
CO
CD
U
*^^*
CO
•rl
60
a
o
•rl
4J
Ctf
O
o
Ctf
4J
C
0)
co
O
•rl
4J
Ctf
S-l
4J
ti
CU
O
a
o
o
11-62
-------
Two studies have explored the mechanism of genetic resistance to
141 142
ozone. Engle and Engle and Gabelman found that ozone sensitivity
in onion is probably controlled by a single gene pair, with dominance of the
resistant gene. In resistant plants, the membrane of the guard cells was
more sensitive to ozone and lost its differential permeability, thus causing
stomatal closure. This did not occur in the guard cells of the sensitive
500
cultivar, and thus the stomata remained open. Taylor crossed the
sensitive Bel W tobacco with a resistant line and found that the F was of
3 1
intermediate sensitivity. The F segregated into 40% resistant, 10% sensitive,
2
and 50% intermediate. He postulated that sensitivity was controlled by at least
two genes. Resistance mechanisms need to be studied in other species.
116
Dean reported a 50% increase in stomatal density of two sensitive
tobacco cultivars over two resistant cultivars. Stomatal size was not a
factor in this study.
Differential susceptibility of individual clones of eastern white pine to
28 82
ozone and sulfur dioxide was shown by Berry and Heggestad and Costonis.
126
When Dochinger ei_ al_. determined that chlorotic dwarf could be caused by an
interaction of ozone and sulfur dioxide, they used a chlorotic dwarf-susceptible
249
clone to eliminate the genotype variable. Houston tested the response of
tolerant and susceptible clones of eastern white pine (on the basis of symptom
expression under ambient conditions) to ozone or sulfur dioxide. Injury caused
by sulfur dioxide or sulfur dioxide plus ozone correlated well with the earlier
field responses, but ozone did not produce a consistent response. They also
found that a 6-h exposure to a mixture of sulfur dioxide and ozone caused a
difference in needle elongation between clones within tolerant and sensitive
groups. This suggests that tollerance may function over a wise range of
responses.
11-63
-------
It is reasonable to suggest that a spectrum of genotypes represents
various susceptibilities to oxidants, singly or in combination. Although
environmental factors are important in conditioning pollutant susceptibility,
the control of environment over injury to sensitive genotypes may be less
pronounced, if specific biochemical or physiologic mechanisms that have
weak interactions with the environment are involved.
Climatic Conditions. Plant response to ozone and PAN may be
altered by climatic conditions before, during, and after
210
exposure. Plants may be sensitized to a given set of conditions after
1-5 days. It appears that the major conditioning occurs within the first
3 days under a given set of environmental conditions. Conditions during
exposure may be critical, and conditions after exposure are probably
important, but less so than those before and during exposure. The responses
of plants to ozone and PAN under varied climatic conditions are studied
primarily under laboratory and greenhouse conditions, but field observations
have often substantiated the results. Most studies have involved individual
climatic factors and one or two response measures, usually including injury.
Several have dealt with environmental interactions. Sufficient information
exists for generalizations of plant response, but there is much uncertainty,
because of the small number of species studied and the lack of information
on the interactions of factors.
• Light quality: The quality of light affects the growth and development
of plants and plays some role in determining the response of pinto bean to
134,136
PAN. Injury to pinto bean from PAN was maximal when exposed at
420 and 480 nm and less than half that at 640 nm. The response is apparently
487
associated with changes in carotenoid pigments. Shinohara et: a_l. reported
11-64
-------
an effect on tobacco (H-mutant) when exposed at 0.40-ppm ozone for 30 min.
They found the least injury in far red, followed by blue, green, and white,
with the greatest effect in red. This work was preliminary. More information
is needed on the effects of light quality.
• Photoperiod; The effect of a given light period within a 24-h cycle
exerts physiologic control over some aspects of plant development. Research
has shown that plants are more sensitive to ambient oxidants and ozone when
212,
grown under an 8-h photoperiod than either a 12-h or a 16-h photoperiod
268,320
(Table 11-8).
• Light intensity: The intensity of light affects many physiologic
processes within plants and is known to affect the response of plants to
oxidant pollutants. Studies have been reported on effects of intensity before,
during, and after exposure (Table 11-9).
136
Dugger et aL found a direct correlation between the sensitivity of
pinto bean to PAN and increasing light intensity. Pinto bean required light
136, 513
just before, during, and after a PAN exposure for injury to occur.
This was not true with exposure to ozone, although some light period was
necessary.
Generally, plants are more sensitive to ozone when grown at lower
137,138,212 137,
light intensities. This was shown for pinto bean and tobacco,
212,487 138
but was reversed in tobacco Bel W . The reason for this
3
reversal was unclear. In both pinto bean and tobacco, there was greater
injury from ozone when plants were grown at lower light intensities when
137 136
the humidity was 60% or 80%. Dugger et al. found greater injury in
plants grown at 900 ft-c (about 9, 690 luces) than at 2, 200 ft-c (about 23, 680
138
be), but Dunning and Heck reported no difference between 1, 000 and 2, 000
ft-c (about 10, 760 and 21, 530 Ix) for either pinto bean or tobacco exposed
11-65
-------
Table 11-8
Response of Plants to Ozone, as Conditioned by Photoperiod
Plant
Species
Tobaco,
cultivar White
Gold
Tobacco,
cultivar
Bel W_
Bean,
cultivar Pinto
Ozone Con-
centration,
ppm, h Notes
0.67, 5
0.30, 1
0.30, 1
Response, % injury
Photoperiod, h
57
Control 54
conditions,
2,000 ft-c
(21,529 Ix)
Control 71
conditions,
2,000 ft-c
(21,529 Ix)
Reference
40
27 320
19 212
18 212
11-66
-------
cu
o
C
cu
M
cu
CM
CN
i—i
CN
CN
i—I
CN
oo
00
CO
CO
Oi
I
cfl
H
4J
•H
CO
5
I
4J
•a
•H
CU
M
CO
O
P.
a
I
O
M
O
CU
rt
o
•H
O
o
co
cfl
cu
C
o
N
O
O
4J
C
cd
CU
CO
rt
o
p.
CO
CU
4-l9
fl rH
•H
IJ 0
1
4J 4->
cd in
* •»
6-S >,
>> CO
M C
3 CU
•n 4J
rt rt
H H
o P1
O 00
vO O\
f ft
CN l~»
CN
x~ \
o m
f" '• i^x
OO CO
9 «
f CTi
fl
v*— '
O VO
O r-
fl O
f 1
v^/
o o"
~
O CU
M
4-J CO
& o
O P.
a
CO
cu
4-1
o
#1
c
o
•H
4-1
cd
M
4-1
rt ,fl
CU CU
rt o •>
0 C 0
N O P
OOP
rH
o fTi
M in
4-1 en
rt "
0 H
a w
M ••>
cu ca
*t3 ci
rt o
3 -H
4J
rt -H
? T3
o rt
M 0
O 0
i— 1
ft
in
co
o
CO
cu
4-1 -rl
rt o
cd cu
I—I P
fl C/l
M
cd
•H
4-1
H
3
a
„ 0
rt _j
cfl C
0) iH
W PH
a.
oo
CO
o
"
cu
M
CO
0
p.
s~i
O
CTi
CN
~
x"\
O CO
o o\
O CN
t* *
CO CN
CO
v— **
O /"N
o cy\
O CN
CN •>
CN
N— '
CO
C
O
•H
4-1
•rl
rt
0
0
rH &
O
to oo
4-1
C «
O PH
U P-i
rH
91
O
CO
0
M
cfl
^
•H
-P
iH
^j
O
* O
£4 "^
cd ^
*
O vO
o* r^-
i^ CO
ci
I
i
oo
CN
^j.
oo
o
oo
(~l
4-1
O
M
O
co o
rt o
O O x-^
•H » X
4J CN i-H
•H
"rt i-TcO
o w m
O •>
• •> i — I
f— 1 *rt CN
O ^
M 00
4J a
fl * i
U PH HH
i — i
•V
O
^j-
•
O
M
cd
>
•H
4-1
rH
3
„ 0
rt ti
Cd rt
a) -H
pq PH
^.
vO
r~-
in
oo
CN
I— 1
cu
M
CO
o
p.
X
w
co o
rt o
O O x-v
•H •• X
4J -* rH
•H
IB i-Tin
o o o
CJ ft
• •> CO
rH trt *J"
O *~s
to oo
4J U
O P-{ 4-*
u a. *w
^H
A
o
sj-
«
o
1
1
oo
CO
CTi
r-4
CN
r|
^
0
s
CO O
C 0
0 0 x-s
•H « X
4-1 *3" rH
•rl
'rt i-f in
o w o
CJ 1
• * CO
I— 1 fi
•rl
4J
•3
a
o
CJ CO
0 &
cfl
43 H
O 0)
EH fi
CN
CO
00
CO
1 —
CN
oo
cu
M
rj
CO
o
P,
fl
oTo
rt o
O O X-N
•H « X
JJ »^- ,_ 1
•H
"H i-Tin
o o o
CJ •*
• « CO
I — 1 rrt
O PH
I— 1
fi
0
t
o
M
cd
>
•rl
4-1
rH
CJ
« 0
fl ^
cd e
CU -H
pq PH
1
1
00
vO
o
m
i
a)
}-|
3
CO
0
P.
£
CO
C
O
•rl
4J
•rl
"rt
o
o
rH rO
o
M 00
4J
O PH
U PH
i— I
ft
O
0
O
11-67
-------
01
o
Pi
QJ
ro
co
Q)
HJ
0)
M
CO
O
ft
X
w
60^
•H
i-l O
4J 4-1
Cd 14-4
>, CO
H Pi
3 OJ
•I-) 4-1
C C
H H
I 1 I
I I I
CN CO
VO CO CO
m
0 P-i
U P-i
o
•H
4-1
cd
M
4-1
C J2
CU 01
pi o •
oca,
N O &J
00^
o
•H
4J
i-H
3
O
*l
O
O
o
cd
,n
0
H
CO
ts
I— 1
0)
pq
o
-------
136
to ozone. Dugger et al_. found a relation between plant age and light
intensity. Peak sensitivity to ozone -was about the same at both intensities,
but the span of plant age that was sensitive was increased at 900 ft-c (about
9, 690 be). This could have an important bearing on environmental work and
has not been seriously considered by other workers.
Sensitivity to ozone a6 light changes during exposure generally increases
138
with intensity. This was found for tobacco between 1, 000 and 4, 000 ft-c
(about 10, 760 and 43, 060 be), with a slight decrease at 6, 000 ft-c (about
137, 216
64, 580 be), and for pinto bean between 1, 000 and 6, 000 ft-c
(about 10, 760 and 64, 580 be). When pinto bean was grown at 4, 000 ft-c
(43, 060 be), there -was an increase in sensitivity from 1, 000 to 6, 000 ft-c
(10, 760 and 64, 580 be) during ozone exposure; but, at lower intensity during
growth, the 4,000- and 6,000-ft-c (43,060- and 64,580-lx) exposure intensity
138 137
gave similar responses. Heck reported that exposure light had
no effect on the response of tobacco or pinto bean to ozone when the relative
humidity was 80%, but had an effect at 60%.
487
Shinohara et a_L reported that up to 10 h of postexposure light did
113
not affect the response of tobacco (H-mutant) to ozone. Davis and Wood
delayed symptom development in Virginia pine when the plants were held in
the dark for extended periods after ozone exposure. However, the final
severity of response was unchanged.
• Temperature: Variations in plant response to ozone or oxidants
occur with increasing growth temperature, if a given temperature is maintained
320
for 3 days or more before exposure. Macdowall found that a low day or
high night temperature increased the susceptibility of White Gold tobacco to
ozone. He reported no interaction between day and night temperatures.
11-69
-------
268
Juhren et al_. used eight combinations of day and night growth temperatures
with Poa annua and then exposed these plants to ambient oxidants for a day.
The sensitivity varied with plant age, showed a partial reversal after 3 days
of changed temperatures, and was greatest at the 26 C-20 C day-night
4,417 139
temperatures. Radish and pinto bean were more sensitive if
7 139
grown under cooler conditions, whereas snap bean, soybean, pinto
138,139 138,363,485 107,113
bean, Bel W tobacco, Virginia pine, and
589 3
white ash -were more sensitive if grown under warmer conditions.
486
Shinohara et_ a_L looked at growth, exposure and postexposure
temperatures, and their effect on the response of several tobacco cultivars
to ozone. Plants were grown at constant temperature (day/night) during
growth and were kept in the dark for 48 h after exposure. These elements
of design weaken the value of this report. However, generally they showed
an interaction between growth and postexposure temperature, night temper-
atures were more important than day temperatures, and lower temper-
atures during expos\ire increased the sensitivity of tobacco to ozone.
128
Drummond reported increased injury to petunia (cultivar White
Cascade) with increasing temperature when exposed for 1 h to PAN at
0. 15 ppm.
Early reports suggested a positive correlation between plant response
to ozone and increasing exposure temperature, to about 30 C. These results
216
were shown for pinto bean when exposures -were under greenhouse conditions,
but an inverse correlation was found when they were under controlled lighting in
growth chambers. This suggested that, under greenhouse conditions, it was
not possible to separate light and temperature effects. This inverse relation-
64,65,138,216 159
ship has been shown for Bel W tobacco, Lemna minor,
3
11-70
-------
107,113 589
Virginia pine, and white ash. Under some conditions, this does
138, 139
not seem to hold for pinto bean, in which a direct correlation was
found from 20 to 32 C.
210
It has been suggested that higher postexposure temperatures will
107, 113
cause an increase in sensitivity. This was shown for Virginia pine
589 485
and for white ash, but the reverse occurred in Bel W tobacco and in
4 3
in radish.
Two papers have considered interactions between temperature and
139
other variables. Dunning ^t al. studied possible interactions among
species (Dare soybean and pinto bean), ozone dose, potassium nutrition,
growth temperature, and exposure temperature. The two species did not
respond the same, except that there -were no interactions with potassium
nutrition in either species. Soybean showed no interactions between dose
and temperature under either temperature design. Pinto bean showed
strong interactions between dose and growth temperature and between
exposure and growth temperatures and a mild interaction between dose and
exposure temperature, with no higher-order interactions. The dose-growth
temperature interaction is shown graphically in Figure 11-2. Apparently,
pinto bean is very sensitive to a variety of stresses, and these variations
make pinto bean both a unique test plant and one that can be very difficult
138
to handle. In later studies, Dunning and Heck looked at interactions
among growth temperature, exposure temperature, and plant species (Bel W
3
tobacco and pinto bean). They found that the two species responded differently
to the temperature conditions. Pinto bean showed no interaction between
growth and exposure temperatures, whereas tobacco showed a strong inter-
action. For tobacco, growth temperature had little effect at an exposure
11-71
-------
35-4
20 PINTO BEAN
28° PINTO BEAN
25-4
45-1
60-1
50-2
Figure 11-2.
The significant interaction of growth temperature in C, ozone dose (con-
centration x time), and species on foliar response (% injury) to ozone.
Dose is shown at the end of each of the eight axes as concentration (parts
per hundred million) and time (hours). Percentage injury is shown in 5%
increments along each axis. Each value is a mean of 15 observations.
The LSD at the 1% level is 8.3 for the injury response. This value can
be used to compare any two points in the figure. (Reprinted with per-
139
mission from Dunning et al. )
11-72
-------
temperature of 16 or 32 C, but a marked effect at 21 or 27 C (sensitivity
increased with increasing growth temperature). These types of interactions
need further clarification as we attempt to understand the effects of a total
environmental system on the response of plants to oxidant pollutants.
Crops that show greater injury under cooler conditions may be more
severely injured in early spring (assuming that oxidant is present). Feder
159
and Sullivan used duckweed to remove the confounding effects of stomatal
movement. They reported similar results in light and dark fumigations with
139
temperature variations. Dunning et a_l. found no changes in carbohydrate
content associated with sensitivity of either pinto bean or Dare soybean.
4
This was also reported for radish, except that cultivar Cavalier showed
an increase in carbohydrate after an ozone exposure in a single experiment.
A summary of these temperature effects is found in Table 11-10.
• Relative humidity: Field observations suggest that plants are
more sensitive to oxidants as relative humidity increases. Davis and
107,113
Wood found an increase in sensitivity of Virginia pine to ozone at a
high humidity during exposure, but reported no effects from growth or
424
postexposure humidity changes. Otto and Daines found similar results
over a wider humidity range and over several ozone concentrations during
exposure of pinto bean and Bel W tobacco. They did not study growth or
3 137
postexposure conditions. Dunning and Heck showed a significant increase
in the response of pinto bean, but not of tobacco, to increased exposure
humidity. For growth humidity, tobacco sensitivity decreased with an
increase in humidity; pinto bean response was unaffected by humidity at a
growth light of 4, 000 ft-c (43, 060 be), but was increased with an increased
138
humidity at 2, 000-ft-c (21, 530-lx) growth light. In later work, Dunning
11-73
-------
o
I—I
I
H •
r* 5
cfl CU
P H
O r^
CM rH
ro 4-l CO
0 C
o
0) ft
ft CO
>> Ol
H erf
^ .t"?
r-l 4-1
3 12
•r-l O
•H 60 TJ
CU
B^2 &-£ r-l
Q
CO
Ol
4-1
o
rC
VD
i— 1
n
1 PH
«\
rj
o
•H
4J
cfl
r-l
4-1
C ,£
Ol
U «
c e
O ft
O ft
CO
0)
•H
o
0)
ft
to
4J
c
cfl
rH
PH
• tO
*rH ^
4J -H
rH 4-1
3 rH
0 T3 3
rH 0
* O M
0 CJ f, 0)
CJ J3 -H
O CU CO rH
cfl 4-1 -H CO
^^ "rH T"j ^
O rg Cfl CO
H 5 erf o
in
CN
CM
ro
m
CM
o in
ro m
o
CM
m
CM
c^
CN
ro
CM
ro
oo
CM
m
o
CN
m
r-.
CN
o
CJ
CJ X)
01
4J
*%
£2
T3 •
^ 0)
CO
CO
en
o
ft
T->
•H
B-S
0)
CJ
cu
CO
o
ft
M
CM
o
m
cfl
•H
4-1
rH 0)
O CO
t-J
C o)
cfl 3
CU rH
m CQ
m
CO
rH O
ro O
m
CN O
oo
oo
ro
in
Ol
S-i
CO
o
ft
T3
QJ
V-i
ro
CN O
o o
CM rH
ro ro
rH CO
olo
i-i|in
• 3
4J O
en ft
o X
PH CU
rl
CO
CN O
ro
CM
00
CM m
ro KO
rH|VD
0)
Vr
3
en
O
w
3 cfl
^rH
m
TJ
0)
4J
O
0)
ft Cfl
o
1 PC
4-1 P5
U— 1
&^5
o m
o oo
0
CM /-s
• *% rH
CM CM
rH m
**
PH CN
PH ^^
»^-
*«
O
CN
•
O
^
cfl
•H
4J
i — 1
3
O
^
O
O ro
O |3
CO
i£3 rH
O 0)
H eq
o
I
4-1
14H
O
O
m /— *
•«- rH
rC
CN
OO 00
ro
PH in
PH ^^
*zf
^
m
CM
«
o
rJ
jj"
O
C3
•H
0
cO
C
e
0)
rJ
1
4, '^
C CU ^0
CU
•H 4-1 O
rQ C '-N
S cfl « J3
fd T3 * I
^ -H cu e
X > ft
ro O CO ft
V-i
cfl
•H
4-1
i-H
3
U
f,
O
U ro
CJ |3
CO
rQ 1 — 1
O 0)
H m
" r-l
x^ cu
CO U 4J
^i i ) i
cO ro cfl
id CM
j.
O) ro
Q- 3
d CO 4-1
0) O CO
4-1 CU rJ
cO 0) 'TJ
4J fH
CO O 43
O 0) OO
O rD ^f
CN
**
m
ro
•
O
^
cd
•H
4-1
rH
3
U
•V
O
CJ
CJ
cfl
,O CM
0 1
H JU
0)
3
CO
0
%
cu
11-74
-------
cu
o
C
cu
^
cu
U-l
cu
oo
vO
CM
ro
00
vD
rH
CM
C!
O
co
H
CU
3
4-1
Cfl
rJ
CU
ex
s
cu
H
cu
cu
to
C
0
ex
w
cu
4-1
60
•H
C
cfl
P
O
•
exu
e
cu «
H •
PL
>> a
cfl CU
P H
in
CN
^^
0
CO
m
i—4
**N^
O
CN
m co
CN m
P- CN
ro m
CO
o
fx
o
43
4J
O
o
T)
C
O
•H
4-1
•H
-d
a
o
o
to
cO
CU
a
o
N
o
o
4-1
c
cs
14-1
O
CU
CO
C
O
CX
to
cu
CU
MH to
O C
O
cu a
ex to
>. cu
H pet
o
•H
C 43
CU CU
a a '
o c! e
N o a
o o a
oo ao
CM CM
O
CM
~* ro ro
CM ~* "^
OO *«O "^f
CN m
CM
r-. CN m
CN CN
Growth o:
Exposure
to
cfl
T)
in
i— i
to
4J CO
IS T3
O
rJ in
60 -H
post-
exposure
Growth
Growth
H
W
O 4J
CM £
O
4-1 rJ
Cfl O
H
w
oo
CM
CU H
rJ O
CO OO
O CM
ex
X 4J
W CO
Growth
Growth
Exposure
O CO
>J • 4-1
60 13 O
0) O
PM m
PM P^
ro
• en
§*£
cu
4-1 O
I
M O Ed
O O P
rC
CM
i-H
•%
PM
PM
4-J
cfl
^
^
rH
/-C
X
rH
(
oo
vO
«x
fO
CN
• —
4-1
&
O
J_J
60
j^
O
MH
•
&
CU
4J
, 1
^n
cfl
•H
O
CU
ex
CO
o
1
Ij
MH
O
0
CM
CN
• *
43
CN
i— 1
A
PM
PM
4-1
co
A5
[5
*— t
/^•C
X
rH
00
*
f*~)
CM
N —
4-1
13
0
^_j
60
j^
0
<4-i
•
£3*
cu
4-1
cfl
•H
O
CU
ex
to
CO
0)
to
O
TJ
oo
4-1
O
60
O
r4
4-1
C
O
CJ>
CM
I
4-1 4J
C C
0) cfl
*rH ^3
43 -H
CM
CN
CO
r?
60
C
"rH
c
o
•H
4-1
•H
rrj
c
o
o
MH
O
AJ
[5
60
CU -H
3 ^
CO 43
0 4J
ex-H
CU
13
CU CU X-N
en 4-> >»
3 Cfl 4J
O rH -rl
43 a; 03
13 rJ P!
CU rJ CU
CU O 4J
HOC
0
in
m
•rC CU
4-> rH
rH rH
3 0)
U pq
CD M
^1
K O
3
O
A
cfl
cu
xi a)
o <"
Cfl
•H
4-1
rH
O
« o
cfl fi
CU 'H
PQ PH
S-i
cO
3
cfl
3
C
(3
cfl
cfl
O
PM
u
A
o
§aT
43 i-l
o ^
H PO
•H
4-1
rH
3
O
» 0
(3 <-"
§ d
cu •"
pq PM
11-75
-------
c
o
o
o
1—I
I
cfl
H
0)
M
3
4-1
rd
^4
01
I1
01
H
CO
O
P.
4-J
S
O
^J
o
13
cu
o
•H
C
O
CJ
cn
cfl
cu
C
O
N
O
o
4-1
C
Cfl
CU
CO
O
P.
cn
0)
cu
o
C
cu
j-i
0)
M-l
cu
Pi
4J
60
•H
C
>-.
cfl
O
"4-1
0
0) P. CJ
co e
C CU »
O H •
p a
cn t>. a
cu co cu
Pi O H
o cu
j_j
,n 3
4-1 cn
& o
0 P
u x
CJ W
cu
MH CO
0 C
0
cu p,
p, cn
>•> cu
E-1 Pi
**O
i — i
CN
co m
•-.
j_i
~j
•r-i
a
•H
&~S
CO
cn
o
P.
•H
CN CO CN O-
CO -d" CO
CN
i— 1
CN
m
i — i
o
i — i
|m
M
Ir-.
|CN
Ico
|co
ICN
|m
cu
^i
3
to
o
p.
£
s»
3
'f?
•H
1
1
1
1
CO
1
1
rC
4-1
^
0
CJ
>,
3
*' )
•H
1
1
1
1
cr\
i — i
1
1
1
4J
cn
o
P-i
cu
jj
3
CO
o
px
X
cu
cu
C
o
N
o
t
e"
0
•H
•4—)
cfl
(-1
pj
cu
CJ
o
CJ
5
CO
01
4-1
O
J3
A
e
P
P
rH
0
J-I
4-J
C
o
CJ
J-J
0)
T3
C
3
rj
g
O
J-I
O
«%
in
CO
«
o
CO
cu
•H
CJ
CU
P
Cfl
4-1
C
cfl
P-I
S-J
CO
^
•H
4J
r-(
3
O
«i
G
tfl
0)
pa
cu
PO
a
3
T)
cu
cn
o
p.
X
cu
• «\
cn
C
o
•H
4-J
•H
*"O
C
0
o
o
4-1
•H
P-l
cn
C
0
•H
4-J
•H
T3
C
O
CJ
4-J
rj
Cfl
4-J
tn
C
O
o
H
O
^t
J-J
C
o
o
J-I
0)
rrj
C
3
rj
£5
O
0
«\
CN
CO
O
cu
T)
C
3
T3
CU
cn
0
p.
X
01
• M
CO
C
o
•H
4J
•H
*T3
C
0
CJ
cn
C
0
•H
4-1
•H
*rj
C
O
U
4-1
C
Cfl
4-1
CO
C
O
o
,_!
0
^-i
4-1
C
O
O
Vl
0)
T)
C
3
C
[5
O
j_i
CJ
v\
LO
CO
•
o
j-i
cfl
•H
j->
t-l
3
CJ
n
o
fj
U
cfl
O
H
CU
^O
C
3
"C
cu
cn
o
P,
X
cu
«^
cn
C
o
•H
4_)
•H
T3
C
O
O
C
JS
1 — 1
cu
M
cn
C
0
•H
4-1
•H
T3
C
O
CJ
4-1
fi
Cfl
4J
CO
C
O
CJ
o
J_l
^
1
CO
.„
cn
C
O
•H
4-1
•H
13
pj
0
CJ
rH
O
^_,
4-1
a
o
o
m
•
1-1
v\
o
m
o
cfl
•H
a
•H
00
J-I
•H
^
CU
•H
CM
cn
60
C
•H
, — |
T3
0)
CU
cn
!_i
^
1
CO
• n
CO
C
O
•H
4-1
•H
T3
C
0
a co
60
rH C
O -H
J-I rH
4J 13
C CU
O CU
CJ CO
*^"
"
m
CN
•
O
a\
oo
oo
CO
CNllvD
rH CO
in \o
oo
i-tlCTi CN
CN|CO co
m
cu
4-i cn
& o
O P. CO
M X O
O W PH
0)
H
CO
o
p
9
i~>
C
cu
M
42 3
4J CO
& O
o p,
V4 X
O W
S-i M
3 3
•r-j T-)
C C
•H -H
CO
C!
O
•H
4-i cn
•H 60
T3 C
C -H
O iH
O T3
CU
r-H CU
o co
O I
U rH
CO
C
o
•H
4-1
P-l
PH
CO
C
o
•H
C r-~ C r-.
O CN O CN
o a
r-l H rH H
O W O CJ
Vi J-i
o o
CJ 00 CJ OO
CN
•
o
cu
J-I
o o
**^J" "*^
• •
o o
cfl
o
-
S
CO
11-76
-------
QJ
O
d
o>
00
co
c
o
u
cu
H
cd
H
01
3
4-1
cd
CU
cx
co
O
CX
&
43
4->
&
O
o
0)
C3
4J
•rl
Is
O
O
CO
c
cd o>
P H
CMlrH rH
CO
^
CM
rH
^O i — 1
CM CM
O
o a
r4 X
o w
MH CO
0 §
CU CX
cx co
>-, 01
H P3
a
o
•H
4J
cd
M
4-1
c
cu cu
C O
O C B
N O CX
O O CX
£ 3
4-1 CO
O CX
* X
3 3
c? c?
(X:
CO
a
o
•H
CO
C
O
T)
C r-
O CM
O
rH H"
O W
t-l
C3 t^
O CM
O
rH H"
O O
t-l
O O
O 00 U 00
01
t-l
3
01
CX
B
ai
§
60
II
H
O
0)
S-i
t-i
CU
CX
§
13
01
ti
0)
cd
ca
01
3
CO
cd
o
o
cd
o
u
O 0)
H tf>
3
TO
0
CX
X
OI
II
H
W
M
*X3
o
•H
t-l
01
CX
o
4-1
o
CX
II
&
4J
C3
01
B
4-1
cd
cu
t-i
4-*
cu
P
3
4-1
cd
M
cu
CX
B
cu
4_)
<4H
O
01
3
JH
j>^
cd
CO
cd
g
o
43
CO
cu
1-1
cd
CO
0)
3
4-1
cd
M
0)
CX
B
OI
11-77
-------
and Heck found an increase in sensitivity of both tobacco and pinto bean to
ozone with increasing exposure humidity from 45 to 90%, regardless of growth
humidity. However, there was an interaction between growth humidity and
exposure humidity such that the response of these two species to growth
humidity was conditioned by the exposure humidity. Plants were always more
sensitive when grown at 75% humidity, regardless of the exposure humidity.
Table 11-11 shows some of these results.
• Carbon dioxide; Stomatal activity is affected by carbon dioxide,
212
and it may affect plant sensitivity to oxidants. Heck and Dunning reported
a decrease in sensitivity of tobacco to ozone if the tobacco was exposed to
added carbon dioxide at 500 ppm immediately before and during exposure
to ozone (22% injury with added carbon dioxide, and 66% injury without).
If this is a general plant response, the carbon dioxide now added to green-
houses to increase productivity may also increase resistance of the plants
to oxidant pollutants.
• Field observations: Canadian workers using ambient oxidant dose
324, 396
have correlated meteorologic variables with plant injury. A cor-
relation was discovered when an empirical relationship involving evapotrans-
piration (the coefficient of evaporation) was developed and used to modify
the dose information. This empirical relationship has been used on a
limited basis to predict damaging oxidant concentrations from monitored
meteorologic conditions.
313
Linzon reported SNB symptoms on white pine after several days of
wet weather followed by a continuous sunny period. Symptoms were noted
several times during the 1957 - 1964 growing seasons at Chalk River, Ontario,
Ontario, but time of occurrence did not correlate well with peak oxidant
11-78
-------
4-1
•H
T3
•H
I
01
t-t
CO
o
ft
X
w
cd
rC
4J
£
O
)M
o
CU
O
fi
cu
n
0)
<4H
cn s-i
a 3
O TT
ft S
CO H
01
CO
oo
CO
o
ON
inlm oo >n ol
OO|CM in co '-o|
o|H Ko m
4J CO
IS O
O ft
co
CM
CO
CO
o
ft
o
mlo
ON|in
rHlON
in|co
^OlON
CNI|
0)
rl
3
CO
O
m
m
o
o
3
CO
o
ft
X
W
,0
cfl
H
T3
0)
C
O
a
o
u
CO
cfl
cu
o
N
o
CO
4-1
(3
cfl
rH
PU
0)
CO
c
o
ft
CO
CU
Pi
c
o
•H
4J
cfl
S-i
4J
C
0) 0)
e o
o C
N o
o u
m
I
CO
CO
C
O
•H
(3
O
O CO
bO
rH C
O -H
rl rH
4-1 13
C CU
O CU
C_> CO
m
CM
•H
CU
m
CM
PM
PM
CO
C
O
•H
4-1
•H
13
C
O
O
O
U 00
00
r\
PM
PM
• M
CO
C
O
•H
4-1
•H
T3
C PC
0 O
CJ
6^5
rH in
O l^~
tH
4J ,r
a ji
o
U 00
»1
PM
PM
• «s
CO
C
O
•H
4J
•rl
13
C
0
CJ
rH
0
JH
4J
C
o
o
ON
CN
in
n
i— 1
CM
N — ^
O
1
4-1
<4H
O
o
0
•\
CM
• n
43
00
n
PM
PM
* n
CO
C
0
•H
4-1
•H
T3
C
O
a
rH
O
S-i
4-1
fi
o
u
n
PM
PM
CO
C
o
•H
4->
•H
13
C
O
a
i-H
o
rl
4-1
C
o
o
ON
CM
in
*
i— i
CM
>*^
O
1
4-1
14H
0
O
0
*
CN
• «\
43
00
rv
PM
PM
• *\
CO
C
0
•H
4-J
•H
13
C
0
O
rH
0
M
4-1
C 43
O
U 00
U
rH
CO
• r>
CO
C
O
•H
4-1
•H
13
a
0
o
rH
O
!H
4-1
C
0
u
u
,— 1
CO
• W
CO
C
0
•H
4-1
•H
T3
a
0
CJ
rH
0
)H
4-1
a
o
u
o
cu
^ -H 60
cd 4J cd
> rH rl
•H 3 CU
4-J 13 O >
H C cd
3 cd -
O O
» o
•> o o
a 4-i cd
Cd 0 43 r-t
CU -rl O CU
pq PM H pq
CO
cd
>
•H
a
•> O
4J
d C
a)
pq
si
rs
H
0)
o cd
o >
CJ -H
O 3
H O
3
O
cd C!
CU -H
P5 PM
11-79
-------
0)
u
e
0)
t-l
01
M-l
01
Pi
oo
4-1
(3
o
cd
H
•H
1
CO
o
Pi
G
cd
O
rl
o
13
(U
(3
O
CO
cd
cu
o
N
o
OI >•
CO t-l
8 3
O T-
Pu G
CO M
0)
OlvO
olm oo
vD|rO ro
P
C/D
LO
CN
,£3
•^
O
rl
60
II
33
0
*•
O
•H
H
01
P,
O
4-1
O
P.
II
P4
P4
«
4-1
a
0)
4J
cd
CU
rl
4-1
4J
•H
T)
•H
3
3
r^H
MH
O
01
0
•rl
E-4
rQ
CU
^
TH
i-H
rl
a)
d
3
0)
j-j
cd
CO
cu
3
rH
cd
^
^
•rl
•H
3
J^
nd
'O
11-80
-------
314 29
concentrations. Berry and Ripperton observed emergence tipburn on
susceptible trees in West Virginia several days after oxidant peaks of 0. 065
ppm. They found that container-grown susceptible pine clones were protected
from injury if placed in a chamber supplied with charcoal-filtered air.
Such factors as windspeed and barometric pressure appear to play
little or no role in affecting plant sensitivity to oxidant pollutants. Air move-
ment would be expected to play a role under ambient conditions, because of its
known effect on leaf boundary layers, but it probably has little effect in chamber
45, 207, 232
•work, unless wind velocities are greater than 1 mph (1. 6 km/h).
It is widely believed that vegetation growing in the humid eastern
United States would be severely injured, if oxidant concentrations reached
the daily peak concentrations (0. 20-0.40 ppm) commonly experienced in the
less humid sections of California. An air pollution episode that occurred on
July 27-30, 1970, in the Washington, D.C., area is indicative of what may
happen. During this 4-day period, the peak oxidant concentrations ranged
from 0. 14 to 0. 22 ppm and were accompanied by a low concentration of
sulfur dioxide (0.04 ppm). Oxidant injury was observed on 31 tree, 15 shrub,
2 2
and 18 herbaceous species in an area of 72 mi (about 187 km ). Increased
emission of the precursors of photochemical oxidant formation could result
in repeated episodes of acute injury or even chronic injury to eastern
vegetation.
Several workers have explored the relationships between ozone
effects on vegetation and several climatic factors. Thus, we have some
understanding of how these factors may affect a plant's response to ozone
137-
and probably to ambient oxidants. The few reports on these interactions
139
suggest that much remains to be learned about how these climatic
11-81
-------
factors interact in causing a plant response. Studies to date suggest that
stresses applied during exposure have their greatest effect on stomatal
activity, -whereas those applied during growth affect a physiologic basis
of resistance that is not related to stomatal function. Postexposure
reactions -would no doubt be physiologic. Interactions between growth
and exposure conditions would combine these stress factors. A physiologic
stress may be so pronounced that the normally responsive stomatal
137
mechanism would not function during exposure. More emphasis needs
to be placed on the study of multiple-stress interactions.
Edaphic Conditions. Soil -water stress during growth and exposure to
oxidant is probably the most significant environmental factor affecting plant
280
response. Khatamian et_ al_. found less reduction in chlorophyll content
and an increase in dry-matter production in tomato exposed to ozone at 0. 50
or 1. 00 ppm for an hour, if plants were grown under a -water stress that
did not itself cause a reduction in growth. Plants in the three-leaf stage
•were most sensitive to ozone if grown in optimal soil moisture (Table 11-12).
348
Markowski and Grzesiak found protection from ozone in bean and barley
117, 504, 577
grown under drought conditions. Several early field studies
showed a close correlation between soil moisture and oxidant injury to several
tobacco cultivars. Field observations generally suggest that sensitive plants
may become resistant under drought conditions. It is possible that drought
during growth causes physiologic changes within the plant that increase re-
sistance, whereas similar conditions during exposure may reduce stomatal
8
opening. Adedipe et al_. reported some stomatal closure in tomato exposed
to ozone at 1. 00 ppm for 1. 5 h. However, closure may have been triggered
by the low light intensity of exposure (50 ft-c, or about 540 Ix). Rich and
11-82
-------
CM
i — 1
1
i — I
i — I
cu
iH
43
Cfl
H
CO PI
co o
CU -H
j^ 4-1
4J O
CO 3
Tj
4J CU
c Pi
cfl
•H
X "*
o cu
CO
O Pi
4-J O
ft
CO CO
4-1 CU
CH P5
CO
P-i
CU
O
cu
iH
cu
CO
(4-1
o
cu
CD
p3
0
ft
CO
cu
Pi
c
o
3
4-1
CO
•H
o
a
TH
•H
0
CO
M-l
O
CO
4-1
a
O>
M-l
w
a)
a
PI
cu
cu
M-l
CU
pi
0
^D
CO
•£
o
-]
> k
CO
c
0
•H
4-J
•H
13
M C
O O
r-l U
4-1
e cu
0 H
° S 43
S CO M
O -H «H
>-i O 43
M-4 S v— '
iH
cfl
ai — i
i — i
O
£5
""O
cu
4J
CO CTi
00 CM
•H
M
j_j
M
CU
CO
PI
0
CO
cu
Pi
M-f
o
CU
ft
^»
H
^»
}_i
3
p?
•H
gsO
„
Pi
0
•H
4-1
CO
^
4-1
C
cu
o
C3
o
a
4-1
C 43
CO
•H 0"
X ft
O ft
CO
cu
•H
O
0>
a
CO
4-1
C
cfl
iH
PH
4J
PI
Cfl
•H
X
O
4-1
a
CU
•H
O
1
cd
.,-1
4J
TH
•J2
CJ
CJ
• O
0 4J
U S-i
CJ CU
Cfl 4J '
43 4-1
O CO
H U
00 0
00
CM
rrj
•H
S-J
3
4J
O ->d"
B>S -H CM
O
00
r^
•H
OC
SSIS
&^s
o
TH TH
1 1 1 1
rt~j rj~;
p, p)
0 0
t-l i-l
o o
^-1 rH
43 43
a a
Pl C
•H -H
• •
T3 TJ
CU cu
gs° 6*^
10 O
i-H i-H
A **
o o
o o
1 — 1 1 — 1
cfl
•H
4-1
iH
3
a
TH
" TH
O CO
4-J 43
cfl 0)
0 -H
H fe
O 0 CM
00 OO .-i
CM CM O O
^ M M
i[ | .[ i
r~> PJ
J-l 4-J O
T3 O CJ
O
£3 M CU
•H C3
0) -H
• 00 tH
^c? cO cfl
cu M co
^ 0 C
4-> 0
B^S CO C
j_j
O
M-l
K^
iH
•H
cfl
T)
iH en co
O >i
>-l "Cfl
4-1 O T3
C CN
o .00
0 O en
CN CM oo
O m
CM
4J 0
t-i O
T3 CJ
4-1 CU
O Pi
O -H
M TH
cfl
(3 CO
O
Pi
13
e
o
CO CO
cfl cfl
T3 13
en en
cfl cfl
*"O *"O
iH CM CM
O
4-1 m m
C ^ CM
o • •
u o o
CM
o
X
co
cO
O
CO
cfl
ft
O
CO
a
13
0)
C
C
01
S-i
Cfl
CO
PI
o
•H
O
CJ
4-1
CO
•H
O
CO
CJ
CU
ft
CO
11-83
-------
457
Turner found rapid stomatal closure in pinto bean during a 30-min
exposure to ozone at 0. 20-0. 25 ppm, if plants were grown under a soil
moisture stress. Closure under optimal water availability was slower.
They also reported rapid closure in pinto bean and Bel W tobacco if the
3
plants were conditioned and exposed to ozone at a relative humidity of 37%;
this was not found at 73%. Their evidence suggests that ozone may induce
more rapid closure when plants are already under some type of water stress.
530
Ting and Dugger related activitivity of two tobacco cultivars to the size of
the root systems; those with larger root systems were more sensitive. Several
•workers have recommended withholding water from greehouse and irrigated
crops during times of high pollution potential.
495
Starkey found that a sensitive bean exposed to subacute concen-
trations of PAN was sensitive to postexposure drought, but more resistant
plants were not. This -was related to effects of PAN on membranes.
In perennial vegetation, adequate soil moisture in the early season
interacts to allow open stomata, and thus oxidant injury occurs. When soil
moisture becomes limiting, the nonfunctional stomata of injured leaves may
remain open, thus increasing transpiration. The moisture stress induced
in the late season is additive with oxidant injury, because both increase
defoliation.
411
Oertli found that both salinity and low soil moisture increased the
resistance of sunflower to ambient oxidants. He used four different strength
salt solutions from 0. 75 to 6 atm and two soil moisture levels (0. 3 and 0. 8
412
atm). Ogata and Maas exposed garden beet for 38 days to ozone at
0. 20 ppm and varied exposure time from 0 to 3 h/day. The garden beet
was protected from ozone injury and yield reductions at high soil salinity,
11-84
-------
but this protection was offset by growth reductions caused by the salinity
(Table 11-12). The storage root was the most sensitive yield indicator for
both salinity and ozone stress. They found that yield was not affected until
the daily ozone exposure was 2 h (-40 kPa) or 3 h (-440 kPa). Ozone had no
244
effect at -840 kPa. Hoffman e_t aL reported similar results with pinto
bean exposed to four ozone concentrations for 2 h/day from seed to harvest.
They had three degrees of nutrient osmotic potential and used sodium chloride
to increase salinity. The 0. 15-ppm treatment at -40 kPa gave a 46% reduction
in bean fresh weight, whereas no yield was found at 0. 25 ppm and above.
Results for top and root dry-weights were similar (Table 11-12). Maas
319
et. al. studied the response of pinto bean to ozone and salinity as conditioned
by concentration and duration of exposure (Table 11-13). They found the
injury and growth reductions were sigmoidal at the low salinity (Tables 11-3,
11-5, and 11-13). Salinity suppressed plant growth, but extended the ozone
tolerance for both growth and injury response. In this study, the roots
were more severely affected than the tops. However, in contrast with their
244
earlier study, the pinto beans were exposed for only 14 days and harvested
319
as young plants. Maas e_t al. also looked at nutritional effects; although
some redistribution of nutrient was found (with respect to calcium, magnesium,
potassium, and nitrogen), no serious nutritional imbalances occurred. In
245
the last of a series of excellent papers on salinity effects, Hoffman et al.
studied the effects of four ozone concentrations (2 h/day for 21 days) at
four levels of salinity on biomass production in alfalfa (Table 11-14). As
in the earlier studies, the ozone effect decreased with increasing salinity.
However, in contrast, they found that -200 kPa gave protection from ozone
11-85
-------
Table 11-13
The Interaction of Ozone and Salinity on Biomass
of Pinto Bean Exposed to Ozone^-
Reduction from Control Weight of Plants Grown at
-40 kPa and Not Exposed to Ozone,
Osmotic Ozone
Dry Wt of Leaves
Potential, Concentration, 0 0.30 0.60 0.90
kPa ppm (ozone dose, ppm-h)
-40
-240
-440
0.
0.
0.
0.
0.
0.
15
30
15
30
15
30
0
0
25
25
59
59
14
36
31
39
65
55
28
68
41
70
60
63
67
75
50
76
67
75
Dry Wt of Roots
0 0.30 0.60 0.90
(ozone dose, ppm-h)
0
0
24
24
47
47
18
64
25
50
49
42
53
83
35
81
40
56
72
87
51
85
53
74
319
—Data from Maas et al.
—Specific dose was given daily for 14 days; the duration of exposure can be
determined from ozone concentrations used.
11-86
-------
Table 11-14
•a
Interaction of Ozone and Salinity on Top Growth of Alfalfa-
Ozone Reduction from Control Weight of Plants c
Concentration, Grown at -40 kPa and Not Exposed to Ozone,%^
ppm 2. -40 kPa -200 kPa -400 kPa -600 kPa
0 0 +2 24 35
10 16 11 29 41
15 26 14 33 49
20 39 23 31 48
245
a
-Data from Hoffman et al.
—Concentration shown was given 2 h/day for 21 days.
c
—Values that differ by 10 are probably significantly different.
11-87
-------
with no effect of salinity on biomass production. This suggests that moderate
salinity, in areas of high oxidant, could protect forage legumes (such as
alfalfa) from yield reductions. They also found that both high salinity and
ozone increased water use efficiency of alfalfa and leaf diffusion resistance.
These reports on salinity suggest that we are dealing -with a moisture stress
problem. Although this may involve stomatal response, it is more likely
that we are dealing with a changed physiologic state that increases the resistance
of the plants to ozone effects. At high salinity, both phenomena may play
a role, but salinity itself can cause major yield reductions in the crops
reported on here.
The importance of soil fertility in the response of plants to oxidants
is not understood. No research has attempted to explore, in depth, the
nutritional interactions with oxidants. Nitrogen nutrition has received the
360
most attention. Menser and Street, in an ambient-oxidant study, reported
an increase in tobacco fleck with increasing application of soil nitrogen.
54 311
This was also found in spinach exposed to ozone. Leone et aJ. reported
that nitrogen concentrations optimal for growth produced the most sensitive
tobacco, •whereas either higher or lower nitrogen applications increased
resistance to ozone. The opposite was reported for White Gold tobacco, in
which the optimal nitrogen concentration for growth gave the greatest resistance
320 417
to ozone. Ormrod e_t aL found no effect of two nitrogen concentrations
on growth of radish exposed to ozone. It is apparent that nitrogen concen-
trations and other conditions used in these experiments were not sufficiently
90
critical for an evaluation of nitrogen-oxidant interactions. Craker reported
that increased nitrogen in the nutrient increased chlorophyll loss in duckweed
exposed to ozone. Several studies have explored the importance of phosphorus
11-88
-------
417
in controlling the sensitivity of plants to oxidants. Work by Ormrod et al.
suggested that radish grown at 20 C is more sensitive to ozone at a higher
phosphorus concentration, but that phosphorus has no effect at a growth
464
temperature of 30 C. Ripaldi and Brennan reported an increase in tissue
phosphorus for pinto bean after exposure to ozone. They did not determine
308
nutrient phosphorus. Leone and Brennan reported an increased ozone
injury to tomato with increasing nutrient and tissue phosphorus (1.5 - 62 ppm).
54
Brewer et: al. found an interaction bet-ween potassium and phosphorus in the
response of spinach to ozone. They reported that, at low phosphorus, an
increase in potassium tends to increase injury, but, at high phosphorus, the
90
potassium increase tends to reduce injury. Craker reported a similar
effect on duckweed; chlorophyll loss increased with increasing potassium at
a medium phosphorus content, but decreased with increasing potassium at
zero or higher phosphorus content. There is an apparent interaction
139
betv/een these nutrients, but its importance is not known. Dunning et al.
found that pinto bean and soybean were more sensitive to ozone at low
7
nutrient potassium, -whereas Adedipe je_t al. reported that low nutrient sulfur
351
increased the response of Blue Lake snapbeans to ozone. Mcllveen et al.
90
reported increased injury with increasing soil zinc. Craker found no
change in the response of duckweed to ozone when total salt was varied from
one-tenth to one-half of a full-strength nutrient solution. The response in a
full-strength nutrient was about one-third less. Soil nutrition probably plays
a fairly important role in plant response to pollutants only in cases of nutrient
imbalances, although total salts should affect response under some conditions.
In soils with balanced fertilizer, plants may respond fairly uniformly to
oxidant stress. Table 11-15 summarizes several nutritional studies.
11-89
-------
CO
CO
cu
to
4-1
C/2
^ c
4J O
C -H
Cfl 4J
T3 O
•H 3
X TJ
o cu
^ PH
rH
CU &•? O
£J tl
O « 4J
N CU C
O MO
C U
o o
4-1 ft B
CO O
M O! to
4-1 Pi M-l
C
cO
rH
PH
13
01
4-1
CJ
m cu
rH rH
i cu
•-I C/1
( — I
01 O
1
X> CU
Cfl CO
H C
o
p ,
CO
cu
PH
c
o
CO
4-1
c
CU
to
4-1
3
M
0
•H
to
Cfl 4->
> c
cd
M-l ^3
O -H
CO O
4J
o
01
M-l
MH
W
0)
a
o>
to
cu
III
0)
PH
a
4
-1
00
4
/
M
rH
01
£>
0)
rH
cfl
C!
0
•H
4-1
•H
VH I
4-1 C
3 r-
4
-1
s
£
D
-1
^
o
CN
CO
^
m
o
•
i— t
m
0
,— |
•
0
j
C
c
U
B
I-
U
H
W
cu
c
0
C
0
c
c
1
0
0)
p
M
=1
-1
0
C
]
1
U
i
^
H
ft
a
o
,_j
rn
4-1
cd
}_4
4-1
C XI
01
U
*
C B
0 ft
U ft
00
^)-
*
in
CO
o
M
c
U
•H
CJ
0)
(
a.
C/3
4-1
cd
rH
PH
to
cd
^
•H
4-1
rH
3
a
•t
o
CJ
u
cfl
O
H
O
vO
CO
o
CN CN
CN i— 1
O
VD
t — I
CU
VH
O
cfl
fl
, — 1
•H O
CN v£>
C
cu
oc
o
to
4-1
•H
'Z
^"l
J_|
_3
(?
•H
B-S
4-1
C
CO
TJ
,J_I
Q
4-1
C
0)
•H
1
to
cd
^
•H
4-J
!— j
3
T3 CJ
rH
O »
O O
CJ
cu o
4-1 CO
•H XI
rC O
3 EH
i — i
i — i
CO
s
•— 1 rH
O
0 vO
CNI m
o
oo
CN
i — I
O1. \
CN 00
B
00
CN
C
01
00
0
to
4-i
•H
£2
K^l
VH
3
•T—)
£
•H
B-S
^3-
n
OO
1 — 1
o
to
cd
•H
4J
, — 1
3
C 0
O
4J r.
to O
CU 4-1
4J Cd
4-1 B
cd o
U H
•H
'Z,
•
*"O
a)
j_i
x:
4-1
13
O
^H
00
B~«
CM
A
m
CO
o
•
rJ
»,
to
O
C
to -H
01 B
•H
rH Cfl
Cfl C
> e
cd 01
U rJ
c
cu
00
o
to
4_)
.3.
m
o o o
-d" *^D *«O
B
ft
ft
O O O CO CT
^d" vO O ' — I
m
i — i
B
ft
000 ft
PH
•
13
Ol
VH
r\
4-1
^
0
to
OO
&-S
*^"
M
m
CN
o
to
cd
•H
1 1
rH
CJ
* cu
XI -H
CO rH
•H cd
T3 >
cd cd
PH CJ
11-90
-------
^^
*
.j_J
£
o
s^
m
i-H
I
i — i
CU
rH
^
cd
H
to
cn
cu
C/3
/""s CJ
4-1 0
CJ -H
cd 4_>
T3 CJ
•H 3
X ^3
O CU
, — |
0) B^S O
rj j__j
O r. 4J
N CU C
O CD O
C CJ
0 0
4J ft, S
cn o
CO CU (-1
4-) cd m
C
cd
rH
P-.
13
0)
4J
CJ
01
rH
0)
cn
4— 1
0
cu
CD
CJ
0
cn
0)
C
o
CO
4J
cj
0)
•H
4-1
3
CO
3
0
•H
}_i
Cd 4J
> a
cd
14H t3
0 -H
^
cn O
a
cu
UH
4-1
W
CO
c-H
01
>
cu
rH
cd
rj
O
•H
4-1
•H
4J
3
^t
•s
C
O
•H
4-1
cd
SH
4-)
0)
o
c
o
o
0)
o
c
cu
V4
CU
m
cu
£"
00
•H
A
t
O
iH
s*-x
•P
(3
Q.)
0
cu
rH
W
O r^* O^
co
!-H
1 — 1
1 — 1 ^^
\ oo
rQ 0£ 0 CO
VD 0 •-< CM
V^ 1 — 1 1 — 1 O
• <)• CM rH
O co r^
CO
. CO
0
•— 1 rH
00 00
0 00
CO LO LH
-tf • O
O |c^ i— 1 i— •
CO
M 3
0 -H
x: t-j co
ft 3 cn
cn MH cd
O rH 4-J
^30
0)
cn
pj
o
ft
to
cu
Pi
M-l
O
CU
ft
K*1
H
i-C
#,
0
ft
ft
• •
13 13
CU 0)
^ *"* M
3
i~H i~H *F~)
,£4 ,(~I £
u a -H
B^ B^S 5^S
^— \
CU
4J
3
>> CJ
cd cd
13 ^
*^^
CM CM cn
cn cu
•> « >s cn
u-i o cd o
CO i/~l 13 13
• •
O O CM CO
cn
cu
•H
CJ
CU
ft
cn
4-J
C
cd
rH
P-l
cd
Cfl 4-1
> rH
J-i -H 3
o X-N 4J a
0 13 rH 0)
•iH CU 3 J5
0 cu 0 cd cd
cd £i « cu
CO rj CU ,O CU
03 cd 3 J^» M
CU P CU rH O Cd
i-J ^~/ PQ PQ cn p
o>
CO
rH
oo
1 — 1
CM
0
3
•H
CO
cn
cd
4-1
o
PM
M
3
•1— )
a
•H
B^S
^
0)
4-1
3
O
cd
*• — '
cn
cu
cn
o
13
oo
cd
>
•H
4-1
rH
3
O
A
0
cd
cu
PQ
o
pj
•H
PH
a
cu
cu
MH
rl
CU
I
§
CJ
o
cn
13
CJ
cd
13
0)
•H
rH
cu
•s
3
0)
cd
CO
CU
3
rH
cd
,_!
cd
C
o
, -I
•rl
4-1
•H
r(
4-J
3
O
cn
4-1
CJ
cu
•H
jl
4™l
3
CJ
j2
4J
00
CJ
cu
5H
^J
cn
I
rH
rH
3
>4H
Cd
0
4-1
CU
•H
4J
cd
cu
(ri
11-91
-------
498
Stolzy £t al. found that low oxygen partial pressures over soil
(0-10 mm Hg) for 40 h effectively protected tomato from injury by ozone
(0. 35 ppm. for 3 h). These anaerobic conditions also decreased water use
497
and general vigor. In later work, Stolzy ^taJ. reported that, with
anaerobic soil conditions, the photosynthetic rate stablized within 24 h, -well
below the control (32%). Exposure to ozone (at 0. 17 ppm for 3 h) caused no
injury, but caused a marked reduction in the photosynthetic rate of the control
with a slight increase in photosynthetic rates in plants under anaerobic con-
ditions. They also showed that a 3-h period of anaerobic treatment of the
soil affected the plant response to an ozone exposure 22 h later. The
anaerobic treatment showed less injury and the photosynthetic rate was reduced
less than in the control plants. These changes were related to carbohydrate
changes within the plants. These experiments suggest that even passing
periods of low soil oxygen tension could reduce plant response to ozone stress.
34
Blum and Tingey found that ozone reduction in soybean root
growth and nodulation was a function of foliar impact. They found no direct
effect of ozone on the roots or soil systems surrounding the roots.
Pollutant interactions. Oxidant air pollutants exist as parts of a
complex mixture of gases, many of which may be phytotoxic. However,
except for ambient air studies and simulated photochemical oxidant studies,
little research was done with pollutant combinations until the classic work
357 517
of Menser and Heggestad in 1966. It is of interest that Thomas et al.
suggested that sulfur dioxide might lessen the effect of oxidants in causing
368
foliar injury to pinto bean. Middleton et al. , working with ratios of
sulfur dioxide to ozone of from 4:1 to 6:1, did not observe an increase in
11-92
-------
injury, although hey found that, at 4:1, ozone appeared to interfere with the
209
expected sulfur dioxide injury. Heck found that various combinations of
ethylene, propylene, and acetylene, when mixed -with products of irradiated
propylene-nitrogen dioxide mixtures, did not decrease or increase the
development of foliar injury.
357
Menser and Heggestad first reported that exposure to mixtures
of sulfur dioxide (0. 50 ppm) and ozone (0. 03 ppm) for 2 or 4 h caused 23-48%
foliar injury to the sensitive tobacco cultivar Bel W , whereas the concen-
3
trations of the individual gases produced no injury. This study stimulated
plant scientists to develop research on pollutant combinations.
447
Reinert £t aL have suggested the use of the terms "simultaneous"
(mixtures of pollutants), "sequential" (one pollutant followed by a second
pollutant), and "intermittent" (when there is some period between sequential
exposures) to refer to exposures in discussing studies of pollutant combinations.
They also recommended terminology for use in describing plant response to
pollutant combinations: less than additive, -; additive, 0; and greater than
additive, -f.
Ozone and sulfur dioxide mixtures are of special interest, owing to
their widespread occurrence and to the greater than additive effect on Bel W
357 3
tobacco. Concentrations of either or both that may cause foliar injury
are found around major metropolitan areas throughout the world and are
323
widespread throughout rural eastern United States. Macdowall and Cole
reported that the two-gas combination lowered the threshold for injury of
tobacco (cultivar White Gold) by sulfur dioxide, but not the threshold for
324
ozone injury. Macdowal et_ al_. defined the threshold in terms of dose
when they reported the threshold at 20 pphm-h (0. 20 ppm-h). This has not
11-93
-------
357,547
appeared true in several other reports, nor -within the results
323
reported by Macdowall and Cole. Symptoms reported, -when sulfur
dioxide was below the threshold for the specific plant, are similar to those
reported for ozone.
547
Tingey ^t al. exposed 11 species to different ratios of sulfur
dioxide and ozone mixtures. There was no general trend in terms of how
the ratios of pollutant concentrations influenced foliar injury; additive,
greater than additive, and less than additive responses were noted (Table 11-16).
They described an undersurface silvering and collapse of epidermal tissue,
whereas the upper-surface injury was generally an interveinal necrotic fleck
181, 239,359, 362
or stipple (pigment accumulation). Menser and associates
determined the response of many Nicotiana tabacum types, several Nicotiana
species, and various cultivars within N. tabacum to sulfur dioxide and ozone
mixtures. They found, generally, that tobacco was more sensitive to the
sulfur dioxide-ozone mixtures than to the individual pollutants, but the
relative sensitivity was often similar to that shown to exposure to ozone,
201
ambient oxidant, or both. Heagle and Neely compared the relative
foliar injury among cotton and soybean cultivars exposed to sulfur dioxide-
ozone mixtures and to the individual pollutants. The relative cultivar
261
sensitivity to each pollutant was normally different. Jacobson and Colavito
found that sulfur dioxide at 0. 04 ppm decreased the sensitivity of bean and
331
increased that of vetch to ozone during a 4-h exposure. Mandl et al.
found that the response threshold of alfalfa to sulfur dioxide was increased
126 83
by ozone at 0. 07 ppm during a 4-h exposure. Dochinger et al. , Costonis,
249
and Houston presented evidence that ozone-sulfur dioxide mixtures change
126
the response of white pine to the individual pollutants. Dochinger et al.
11-94
-------
Table 11-16
Summary Effects of Sulfur Dioxide
and Ozone Mixtures on Foliar Injury
Plant Species
Alfalfa
Broccoli
Cabbage
Radish
Tomato
Tobacco, Bel W
Response at Concentration Ratio, SO :0 , ppm'
2 3
0. 50:0.05
0
0
0
0.10:0.10 0.25:0.10
0
0
0.50:0.10
547
'Data from Tingey et al.
+ = greater than additive, 0 = additive, - = less than additive.
11-95
-------
249
and Houston found that the mixture increased the amount of injury, -whereas
83
Costonis reported less injury from the mixture than from sulfur dioxide
alone. Both Costonis and Houston reported effects from sulfur dioxide and
its mixture -with ozone at concentrations of both gases
well below those of other reports. It is possible that they used ultrasensitive
clonal materials. Whatever the reason, this work needs verification.
13
Applegate and Durrant reported injury to peanut at sulfur dioxide-ozone
concentrations and ozone concentrations -well below those reported for other
plants. Their work also requires substantiation. In the latter two cases,
the concentrations reported are close to the detection limits of the monitors
used.
545
Tingey ^t aJ. found additive inhibition of top growth of radish and
less than additive inhibition of root growth after exposure to sulfur dioxide-
538 548
ozone mixtures. Tingey and Reinert and Tingey etaA. exposed soybean,
tobacco, and alfalfa to mixtures of sulfur dioxide and ozone and reported greater
than additive inhibition of root growth of soybean, additive inhibition for
205
tobacco, and less than additive inhibition for alfalfa. Heagle et al.
reported greater than additive effect on growth and yield in soybean, grown
under field conditions, from a mixture of these gases, but the differences
between the mixture and the ozone treatments were not significant. Heagle
203
and Trent reported a less than additive effect on yield of peanut from a
mixture of the two pollutants.
581
Weber reported reductions in plant growth and nematode pop-
ulations from mixtures of ozone and sulfur dioxide, but these changes were
similar to those caused by ozone alone.
11-96
-------
Other combinations of pollutants with ozone, PAN, or both may be
349
important, but have received little study. Matsushima reported additive
foliar effects on pinto bean and tomato from a mixture of sulfur dioxide and
PAN and a less than additive effect on tomato from mixtures of ozone and
174
nitrogen dioxide. Fujiwara reported a greater than additive effect on
290 287
pea from a mixture of ozone and nitrogen dioxide. Kress and Kohut
studied the response of hybrid poplar to ozone-PAN mixtures. Kress used
sequential exposures and found a greater than additive effect after most
exposures; after others, he reported mixed responses. Kohut used simul-
taneous exposure and found all three responses in three replicates of a study.
The reasons for these variations are unclear.
174 447
Fujiwara and Reinert jjt aL have recently reviewed the subject
of pollutant interaction. Fujiwara gave a straightforward reporting of research
that is fairly comprehensive, -whereas Reinert _et al. interpreted and analyzed
results. Fujiwara also included some of his data on peas and spinach. His
graph (Figure 11-3) showing the greater than additive response of pea to the
mixtures of ozone and sulfur dioxide is of interest, because of the linear
responses of the two ozone concentrations across sulfur dioxide concen-
447
tration. Reinert ^t aL developed some useful tabular material, some of
which is shown in Tables 11-17 and 11-18.
Studies of pollutant interactions are preliminary. We are still not
able to define adequately the total potential impact of pollutant combinations
on the production of quality food, feed, and fiber. We do know that plant
species respond differently to pollutant combinations and that responses can
be additive, greater than additive, or less than additive. We still do not
understand variations in species or cultivar responses or the responses of
plants grown or exposed under a variety of environmental stresses.
11-97
-------
4J
a
w
70 -
50 -
40 -
30 -
20 -
10
0
20 pphm 0,
10 pphm 0
0-0,
10
20
SO Cone, (pphm)
Figure 11-3. The effects of sulfur dioxide and ozone on percentage foliar injury to
174
garden pea. (Reprinted with permission from Fujiwara. )
11-98
-------
Table 11-17
Foliar Response of Selected Plants
to Sulfur Dioxide and Ozone Mixtures
Concentration
Ratio, SO :O
Plant 2 3
Species ppm
Exposure Foliar
Duration, Injury,
h %
Response to
Mixture Reference
Bean,
garden
Bean, lima
Broccoli
Cabbage
Tomato
Radish
Alfalfa
Eastern
white pine
Cotton (6
cultivars)
Tobacco,
cultivar
Bel W
3
Tobacco,
cultivar
Bel W
3
Tobacco,
Md (6
cultivars)
1.
0.
0.
1.
0.
0.
0.
0.
1.
0.
0.
0.
70:
25:
50:
00:
10:
50:
50:
0.
0.
0.
0.
0.
0.
0.
025:0
00:
25:
50:
50:
0.
0.
0.
0.
19
05
05
10
10
10
10
.05
30
03
10
10
0. 5
4
4
4
4
4
4
6
6
4
4
2
24 +
0 0
17 +
28 0
10
50 +
60 +
26 +
10-24 0
41 +
88 +
20 +
349
547
547
547
547
547
547
249
201
357
547
362
447
Data from Reinert et al.
+ = greater than additive, 0 = additive, - = less than additive.
11-99
-------
Table 11-18
Growth Response of Selected Plants
to Sulfur Dioxide and Ozone Mixtures
C one entr ation
Plant
Plant
Species
Radish
Radish
Alfalfa
Soybean
Soybean
Tobacco
Ratio, SO :O , Exposure
2 3 Duration,
0.05:0. 05 8/day, 5
days/wk,
5 wk
0.45:0.45 4
0.05:0.05 8/day, 5
days/wk,
12 wk
0.05:0. 05 7/day, 5
days/wk,
3 wk
0. 10:0. 10 6/day, 5
days/wk
0.05:0.05 7/day, 5
days/wk,
4 wk
Response, Response
% reduction fa to ^
from control Mixture
10 TDW
55 RDW
16 TDW
70 RDW
18 TDW
24 RDW
24 RDW
52 TDW
63 seed wt
32 TDW
49 RDW
0
0
0
-
+
0
0
0
0
Reference
545 •
447
447
548
205
447
T>ata from Reinert et al.
447
TDW = top dry wt, RDW = root dry wt.
a
+ - greater than additive, 0 = additive, - = less than additive.
11-100
-------
Pollutant-pathogen interactions. An important factor in the response
of vegetation to oxidants (primarily ozone) is the presence of biotic pathogens.
Such responses have been studied from several perspectives since Yarwood
596
and Middleton accidentally found that rust-infected bean leaves were less
sensitive to photochemical oxidants (probably PAN). Several investigators
have looked at the protection from ozone injury afforded to plants with active
infections; others have noted that ozone injury increases the sensitivity of
plants to infection; some have studied the effects of ozone on pathogens; and
several have found no interacting effects.
596
Yarwood and Middleton reported the first protective effects in
1954. Little more was done until about 1968. Protection of plants from ozone
200
has been shown in several instances: rust infection of wheat; Botrytis
328 279
cinerea on broad bean; Pseudomonas phaseolicola on pinto bean; mosaic
46,385 443
virus on tobacco; three tobacco viruses; and mosaic virus on
110, 111
bean. In the latter two cases, protection was reported without visible
symptoms of the virus. This may be a general phenonemon, inasmuch as
some protection was reported with very mild symptoms by Brennan and
46
Leone. This protective action has generally been ascribed to the production
of a diffusible substance by the invading pathogen. This might be due to
an alteration in plant metabolism caused by the viral infection.
Several investigators have reported that ozone injury increases the
infectivity of some weak pathogens. This was originally investigated when a
high incidence of B. cinerea was reported on potato that appeared to have
346
severe ozone fleck. The authors later reproduced the symptoms and
disease incidence in greenhouse exposures. B. cinerea also invades ozone-
33£~~
injured geranium leaf tissue more rapidly. It was suggested that the ozone
11-101
-------
336
injured geranium leaf tissue more rapidly. It was suggested that the ozone
lesions serve as infection sites for the weak pathogens.
Plant pathologists have used the possibility of pathogen-pollutant inter-
actions to study the direct effects of ozone on the pathogen while it is active
on plant tissue. This is the best way to study the effects of ozone and is the
only way to study these effects on obligate parasites. The results have
195 452
included reduced growth of crown rust uredia on oat and bean,
199
reduced hyphal growth and number of urediospores of wheat stem rust,
202
reduced infectivity of barley by powdery mildew conidia, and a small
344
reduction in symptoms caused by Fusarium oxysporium on cabbage.
In general, it is felt that the results are due to changes in the host physiology,
and not to direct effects on the pathogen. This may not be true for reduced
infectivity of fungal spores.
There are several reports of the use of ozone with biotic pathogens,
and the responses noted were independent of each other. These reports include
86
Lophodermium pinastri infection of white pine, Fusarium infection of
344 339 452
cabbage, Botrytis infection of poinsettia bracts, rust on bean, and
335
brown root rot of tomato. These results could reflect the conditions used.
196
Heagle has developed an excellent review of this entire subject.
He has also covered the direct effects of pollutants on pathogenic organisms.
We have used the portion of this tabular material that covers the effects
of ozone on plant diseases (Table 11-19).
494 378
Other factors. Stark e_t ah and Miller £Jbal_. reported
that oxidant (ozone) injury to ponderosa pine predisposed the trees to later
invasion by pine bark beetles. The beetles increase the rate of decline and
11-102
-------
Table 11-19
a
Effects of Ozone on Plant Diseases
Disease Affected
Botrytis on gladi-
olus and chrysan-
themum petals
Botrytis on
geranium petals
Oat crown rust
Wheat stem rust
Wheat stem rust
Wheat stem rust
Barley powdery
mildew
Barley powdery
mildew
Botrytis on potato
leaves
Botrytis on broad
bean leaves
Botrytis on potato
le a ve s
Botrytis on
Geranium leaves
Tobacco mosaic
virus
Effects
Fewer infections by
conidia
Decreased patho-
genesis
Smaller pustules
Fewer infections by
urediospores
Decreased hyphal
growth
Decreased urediospore
production
Fewer infections by
conidia
Fewer infections by
conidia
Increased incidence
and pathogenesis
More infections and
pathogenesis
More infections and
pathogenesis
More infections and
pathogenesis
More infections on
pinto bean
Ozone Concen-
tration and Time
Not measured
0. 35 ppm, 4 h
0. 10 ppm, 6 h/
day, 10 days
0.06 ppm, 6 h
0. 06 ppm, 6 h/
day, 3 days
0. 06 ppm, 6 h/
day, 17 days
0. 10 ppm, 24 h
after inoculation
0. 25 ppm, 8th
through 12th h
after inoculation
Ambient
0. 15 ppm, 8 h
0. 15 - 0. 25 ppm,
6 - 8 h
0. 07 - 0. 10 ppm,
10 h/day, 15
days
0. 30 ppm, 6 h
Reference
329, 330
337
195
199
199
199
202
474
346
327
346
336
46
"Under ambient conditions, pollutants often exist in mixtures. Therefore, some
of the effects observed in the field (ambient) may have been caused by inter-
196
actions of more than one pollutant. Adapted from Heagle. All work done
in United States.
11-103
-------
77
may be the final cause of tree mortality (see Chapter 12). It is possible
that oxidant stress in other parts of the country contributes to insect infestation
581
in forest areas. Weber has shown that ozone and mixtures of ozone
w^ith sulfur dioxide (0. 25 ppm, 4 h/day) can decrease the population of four
nematodes associated with soybean. These types of interactions may be
significant in areas of the country with significant oxidant pollution problems.
198
Heagle and Heck found that Bel W tobacco was predisposed to
3 320
later oxidant injury by exposure to ambient pollutants. Macdowall
reported the same -when the preexposure was to low oxidant and the later
exposure was also low. Antagonism was noted when both doses were high.
Sensitivity of plants to ozone and PAN is conditioned by leaf maturity
(Table 11-20). This has received its best documentation in the work by
36 368
Bobrov. Middleton ^t a_l. found that pinto bean primary leaves were
most sensitive at the age of 14 - 34 days when exposed to an ozone-hexene
mixture. Under ambient oxidant conditions, leaves of White Gold tobacco
320
did not fleck until a week or so after the logarithmic growth phase. Ting
529
and Dugger found that cotton leaves were most sensitive at about 70%
expansion and that sensitivity was rapidly lost. Stomatal resistance -was
low, even if plants -were not resistant, all other things being equal. Ting
531
and Mukerji associated this with reduced amino acid and carbohydrate
pools. There was a twofold increase in amino acids 24 h after a 1-h exposure
to ozone at 0. 80 ppm; it was a transient increase. This suggests that low
pool compounds could reduce the speed of repair mechanisms. Tingey
542
et a_l. reported that the first trifoliate leaf of soybean was most sensitive
during the latter stages of leaf expansion. However, their metabolite studies
suggested that metabolic pools did not directly affect foliar sensitivity.
11-104
-------
O
CN
I
CO
0)
V-I
3
CO
o
ex
X
w
01
C
o
N
o
0)
3
CO
CO
cu
CJ
C
CU
^
CU
4H
cu
Pi
sf r^
-H CM
i — I
"d
o
cu
4-1
4H
W
01
4-1
O
cu
4H
4H
cd
CO
00
£
?^ ^ ?? -H
333 £
"i™} *r^ *i ) rt)
fi C C cu
•H -H -H a]
B-S B^S B-S B^S
O in O OO
in CN co in
13
01
4-1
O
cu
4H
4-1
cd
CO
60
C
•H
i — I
TJ
cu
cu
CD
B^S
in
o-
T-,
0)
4J
o
01
4H
4H
cd
CO
60
C
•H
i— 1
cu
01
CO
B-S
m
H
4-1
01
hJ
O }->
'O t^ cd
cu ^H rrj
•H cd (3
!>> G O
4-1 -H O
o !-i a>
U pn C/>
cd cd cd cd
01
3
t-i
H
01
4-1
CO
<4-4
•H
V-i
•H
>-l
PH
CO
O
4-1
O
0)
CO
C
o
ex
w
Oj
Pi
0
o
•H
QJ
CJ
C
O
cu
C
o
N
o
m
CM
CM CN CM CN
ri *t A rt
m in in m
CM CM CM CM
• • • •
o o o o
cd
TJ
m
r-
O CO
O
•
O
cu
I
CM
O
m
cd
•H
C
•H
•H
PH
cd
•H
C
•H
60
}_i
•H
>
„
cu
C
•H
PH
4-1
cd
CU
rH
4J
£_j
0
JS
CO
„
CU
C
•H
PH
j>^
rH
rH
O
rH
n
O
rH
•s
cu
C
•H
PH
^CJ
CO
cd
rH
CO
«
cu
C
•H
PH
'O
o>
O)
i-H
CU
cd
&
Ctf
O
51
3
U
C
o
4J
4-1
O
a
o
4-J
-S
PH
M
Cd
3
(3
cd
cu
C
cd
cu
11-105
-------
564
Townsend and Dochinger did definitive work on red maple seedlings
exposed to ozone at 0. 75 ppm, 7 h/day over 3 days. They reported that
leaves of seedlings about 90% expanded were most sensitive, but that
young leaves were tolerant.
Generally, studies have shown that plants are most sensitive to ozone
at a physiologic age associated with nearly expanded leaves. Sensitivity is
associated with functional stomata, intercellular spaces, and rate of cutin
36
formation on cell walls. This is not true in the case of PAN, in which
leaves of a lower physiologic age, just before maximal leaf expansion, are
most sensitive. Plants generally are more sensitive to oxidant pollutants
during rapid growth stages and lose sensitivity as leaves mature. When
oxidant episodes occur throughout the growing season, the older leaves,
weakened during their stage of maximal physiologic growth, show early
senescence.
190
Hanson etaL reported an increased tolerance in petunia cultivars
as they approach the flowering stage. This was true for both sensitive and
tolerant cultivars, with the latter more strongly influenced. They sug-
gested that bud development produced a diffusible substance that moved
down the plant and acted as a protectant.
6
Adedipe _et al. found that Bel W tobacco leaves were more sensitive
3
to ozone when attached, rather than detached or used as leaf disks. Effects
were seen as visual injury and change in chlorophyll content.
107, 114
Davis and Wood found that ages of Virginia pine needles
influenced their response to a 4-h exposure to ozone at 0. 25 ppm. Generally,
cotyledons were more sensitive than primary needles, which -were more
sensitive than secondary needles. Secondary needles of seedlings were
11-106
-------
about as sensitive as those of 3-year-old trees. This suggests that seedlings
may be good test plants for determining the sensitivity of mature trees.
The cotyledons and secondary needles became resistant after 16 and 18 weeks,
respectively, whereas the primary needles remained sensitive beyond 18
27
weeks. Berry reported that Virginia, shortleaf, loblolly, and slash pines
at 2 - 6 weeks from seed were most sensitive to ozone at 0. 25 ppm for 2 h.
Most species had peak sensitivities at about 2 weeks for the primary needles.
The species were listed in order of sensitivity. These results may not be
contradictory, inasmuch as the exposures and growth conditions varied
greatly between the two reports.
450, 536
Ozone is known to reduce nodulation in soybean and in ladino
286
clover. The reduction in fixed nitrogen was related to a reduced nodule
33
number, and not to nodule size. Blum found no direct effect of ozone on
Rhizobium or on nodule formation. He attributed the reduction in nodule
number to the reduction in available energy in the root tissue. This reduction
in nitrogen fixation could affect total biomass and agricultural production,
286
especially in areas of high oxidant pollution and low soil nitrogen. Kochhar
also reported an inhibition of plant growth and nodulation of Trifolium repens
(clover) when the plants were treated with root exudates from fescue grass
exposed to ozone. If these factors are widespread, they could change the
competitive ability of plant species, with a resulting change in plant diversity
and a possible decrease in agricultural productivity.
Although there has been considerable interest in understanding how
various factors, including air pollutants, affect the response of plants to
pesticides, especially herbicides, very little has been done with air pol-
240-242
lutants. Hodgson and associates first showed an effect of ozone
11-107
-------
on the metabolism of herbicides. They found that ozone inhibited the
dealkylation of atrazine in corn and altered the pathway of diphenamid
metabolism in tomato. The changes could be beneficial, if oxidants increase
pesticide degradation, or harmful, if oxidants stop biologic breakdown at
66
a toxic intermidiate. Carney ^taL reported that the herbicide
pebulate in combination with ozone gave a greater than additive response
on White Gold tobacco and that chloramben did the same with Delhi 34
tobacco. They reported a less than additive response of both tobacco cultivars
to the combination of benefin and ozone. These and other herbicides acted
414
independently of ozone exposure on tomato and white bean. Ordin et al.
found that Avena coleoptile growth was less inhibited by PAN when 2, 4-D
was used in amounts giving optimal growth. These interactions with herbicides
need additional investigation, to determine whether the responses noted are
of general importance. Research needs to be directed at possible interactions
between atmospheric pesticides (vapors or fine particles) and oxidant air
pollutants.
Another interaction has recently been rt:ported between cadmium applied
100
to soil and ozone exposure of cress. If cadmium potentiates the ozone
response of cress, maybe other heavy metals respond in a similar fashion.
Discussion. A complete understanding of the many factors that affect
the response of vegetation to oxidant pollutants is probably impossible. An
understanding of the individual factors is possible, however, and much is
already known; but the interactions between some of these many factors are
unclear. It is possible that, as the mechanism of response becomes better
understood, we can develop an expectation as to how various factors will
interact. However, a well-trained and knowledgeable investigator can
11-108
-------
develop a subjective estimate of response that is repeatable. Inherent
genetic resistance is probably the most important factor that affects the
response of a plant to an oxidant dose. However, the factors discussed
here will influence the severity of response of sensitive genotypes. Even
normally resistant genotypes can be injured by appropriate combinations
of other factors.
Genetic or other factors that induce stomatal closure will reduce plant
sensitivity to oxidant pollutants. Generally, the sensitivity of plants at the
time of exposure is controlled primarily by factors that affect the stomatal
aperture. The internal resistance to gas flow may also influence leaf
sensitivity. Factors that affect sensitivity during growth usually cause
physiologic changes in the plant that tend to make it more resistant to the
added stress of oxidant. Many of these stresses may alter membrane
physiology and make the membranes either more or less sensitive to
oxidant stress.
Dose-Response Relationships
The development of criteria for setting air quality standards requires
a sufficient data base relating a given dose (concentration of pollutant
x duration of exposure) of oxidant (e. g. , ozone or PAN) to some meaningful
effect on plants. An understanding of dose response is also important for
a basic understanding of the mechanism of oxidant effects on plants. Heck
211
and Brandt have suggested that an ideal criterion would be a set of standard
equations that would relate response to concentration and duration of exposure
and that would reflect the effects of all other factors that control the response
of the plant. If these equations were developed, they would be different for
acute and chronic exposures and perhaps specific for individual species or
cultivars. Such a depth of coverage would have little practical value for
11-109
-------
overall understanding or for ambient air quality standards. However, some
average equation involving groupings of plants expressed -with confidence
limits might permit a more reasonable interpretation of dose-response
functions under average ambient conditions. Discussions of the relationship
211,
of time, concentration, and response are found in several publications.
318,401
Data regarding the chronic effects of oxidants (including ozone and
PAN) have not been gathered on a scale wide enough to permit the development
of usable equations in regard to concentration and duration of exposure. Much
of the information available was discussed and tabulated earlier in this chapter.
The data suggest that chronic and acute-chronic effects with resulting yield
and biomass reductions can occur -when average concentrations of oxidant
(ozone) are between 0. 05 and 0. 10 ppm for 2-6 h/day over a number of days
during the growing season. This type of statement is not yet possible for
PAN, but in the Los Angeles basin it is always a factor in ambient-oxidant
studies.
Even that kind of information is not available for forest species. Other
than chronic injury to white pine (associated with ozone, sulfur dioxide, and
their mixtures), no clearly defined examples of chronic injury from ozone
have been reported for eastern forests, and no information is available on
PAN. It is of interest that both Virginia and jack pine appear more sensitive
25, 112
than white pine to acute ozone exposures, but chronic symptoms have
not been observed in either species. The relationship between oxidant dose
507
and injury in the San Bernardino Mountains area suggests that ponderosa
pine is moderately to severely injured in areas that receive oxidant at above
0.08 ppm for 12-13 h each day (Chapter 12). Ponderosa pine seems to be the
most sensitive western pine, but in some areas Jeffrey pine is about as sensitive.
11-110
-------
White fir, incense cedar, and sugar pine all appear more tolerant, even to
373
the high oxidant concentrations in the San Bernardino Mountains. PAN
may play some role in the chronic responses noted in the western forest
species, particularly by broadleaf deciduous trees and some shrubs.
The information available on exposures to PAN and its homologues
506
is not sufficient to develop dose-response curves. Taylor reported
comparative results from exposures to PAN, PPN, PEN, and P BN.
iso
He found increasing sensitivity in the first three homologues.
128
Drummond found a nonlinear response of petunia to PAN that was
similar to those reported for ozone. Representative information for
108
PAN is presented in Table 11-21. Davis was unable to injure
cotyledons or primary needles of ponderosa pine with PAN concentrations
of 0.08, 0. 20, or 0.40 ppm during 8-h exposures. A species-sensitivity
510
table for PAN was developed in the Atlas.
The information on acute exposures of forest species to ozone is
25, 107,112,125, 227, 373, 589, 594
limited. These results of these reports
suggest that many eastern deciduous species are sensitive to exposures to
ozone at 0. 20-0. 30 ppm for 2 - 4 h. Generally, the eastern conifers are
somewhat more sensitive, and the western conifers, somewhat less sensitive.
These results are included in the summary data presented in this section.
568
Treshow and Stewart developed an extensive list (70 plants) from two
plant communities, but it is impossible to determine percentage effect
from their data. They found some injury to several species at 0. 15 ppm
for a 2-h exposure. This list of plants should interest investigators concerned
with plant communities.
11-111
-------
Table 11-21
Effects of Time and Concentration on
Foliar Response of Selected Plants to PAN
Plant PAN Concen-
Species tration, ppm
Time, h
Plant Response
Ref
Controlled Exposures:
Petunia
Petunia
Petunia, cultivar
Rosy Morn
Petunia, cultivar
White Cascade
Bean, cultivar
Pinto
Bean, cultivar
Pinto
Bean, cultivar
Sanilac
Acer, Fraxinus,
Gleditsia, and
Quercus spp.
0.10
0.12
0.14
0.05
0.10
0.20
0.02
0.04
0.14
0.10
0.12
0.20-0.30
5
1
1
2
1
0.5
8
4
1
5
2
8
Severe injury
11% injury
33% injury
23% injury
19% injury
15% injury
44% injury
90% injury
55% injury
Moderate injury
64% injury
Variable symptoms;
sensitivity related
to tissue age
496
162
506
128
506
496
495
127
Ambient Exposures;
Petunia, tomato, 0.025-0.03
swiss chard, others
Petunia, tomato
Petunia, tomato,
Romaine lettuce,
others
Tomato, cultivar
Pearson
ca. 0.014
0.015-0.02
0.10
Several Typical symptoms
4 Acute injury
4 Acute injury
5 Severe injury
560
506
510
498
11-112
-------
This section deals with published data related to short-term exposures
of sensitive plants to ozone and the resulting responses. In most cases, the
measure of response is a subjective estimate of visible injury. However,
various growth measures have been reported in some research, and cor-
relations between injury and growth measures are often possible (Table 11-3).
These acute ozone effects have received sufficient study to permit the con-
struction of preliminary models to relate time, ozone concentration, and
plant response for a number of plant species.
A graphic expression was developed for pinto bean and Bel W tobacco
217 3
exposure to ozone by Heck and Dunning. Later work with a number of
plants permitted the development of a simplistic model derived as an empirical
214
relationship between ozone concentration, time, and response; this gave
a reasonable interpretation of acute response up through a single 8-h
exposure. It also permitted the development of a reasonable acute threshold
concentration for a number of species. The equation was a variant of the
O'Gara equation for sulfur dioxide and is shown as:
C=A+AI+A /T,
.012
where C is concentration of ozone; I is the response measure, in percentage
injury or percentage reduction from control; T is time, in hours; and the
constants A , A , and A relate to inherent and external factors affecting
01 2 211 318
sensitivity. Heck and Brandt and Linzon et al. critically reviewed
these dose-response relationships. They summarized much of the available
acute-response data and analyzed the data on the basis of the O'Gara
211
equation. Heck and Brandt reported the 95% confidence curves for 5%
11-113
-------
318
and 33% response; Linzon je_t al. reported the curve for 5% response,
along with data points. They constructed a threshold curve from the minimal
data points shown. These reviews attempted to develop an average response
across much of the useful information on acute plant response.
297
Larsen and Heck analyzed data on the foliar response of 14 plant
214 217
species to ozone (from Heck and Tingey and Heck et al. ). They
depicted the data using a mathematical model with two characteristics: a
constant percentage of leaf surface is injured by an air pollutant concentration
that is inversely proportional to exposure duration raised to an exponent
(Figure 11-4); and, for a given exposure duration, the percentage leaf injury
as a function of pollutant concentration fits a log-normal frequency distribution
(Figure 11-5). The complete leaf injury equation combines the equations
shown in Figures 11-4 and 11-5. This equation expresses pollutant concen-
tration as a function of the other variables:
Zp
c = m s t ,
g hr g
where c is concentration in parts per million, m is geometric mean con-
g hr
centration for 1-h exposure, s is standard geometric deviation, Z is number
g
of standard deviations from the median (injury), t is time in hours, and p is
slope of injury line on logarithmic paper. From the data for pinto bean in
Figures 11-4 and 11-5:
Z -0. 57
c = (0. 31)1.44 t
Thus, c = 0. 10 ppm to give 10% injury in a 3-h exposure. The summary
table of Larsen and Heck for the exposure of 14 plant species (two cultivars
of corn) appears as Table 11-22. From this analysis, they suggested that
averaging times of 1, 3, and 8 h should be used in the development of
oxidant standards for the protection of vegetation.
11-114
-------
For the present report, the literature was critically reviewed for
information on the three measures--duration of exposure, ozone concen-
tration, and plant response. From this review, 74 references were found to
have usable data. Several criteria -were established before data were used:
the monitoring technique and method of calibration should be defined (40%
of the references used a calibrated Mast instrument, 50% used the Mast
uncalibrated or the calibration procedure was impossible to determine, 4%
used a 20% buffered potassium iodide wet chemistry, 3% were unknown but
other procedures suggested that the data were reliable, one report used an
ultraviolet method, and one used an automated iodometric technique); the
plant response must be subject to the development of a percentage
evaluation in comparison with the control plant (about 93% of the responses
were foliar injury--for these we often made a subjective evaluation of scales
used, on the basis of injury description given--other responses included
a reduction in chlorophyll, yield, leaf area, root dry weight, or top dry
weight and an increase in respiration; and the general experimental pro-
cedures used needed to conform to those generally reported around the
country. The data used came from a number of laboratories where
growth and exposure conditions were highly variable and plants were
exposed at different ages, at various times of year, and under various
soil conditions. The investigators always attempted to grow and expose
plants under sensitive conditions. We have assumed that these variations
have given us some average over environmental conditions. The above
-------
10
£
o,
a
c
o
•H
-p
TO
O
C
O
O
Q)
O
N
O
0.1
3.09
2.33
1.28
-1.28
-2.33
-3.09
c
2
•5
-------
z. Number of stand deviation
from median
a
c
o
03
5-c
•P
C
0)
O
c
o
o
0)
c
o
N
O
0.01
0,01
10 16 50
Leaf injury, %
99.9
99.99
Figure 11-5.
Percentage leaf injury in pinto bean exposed to various ozone concentrations
for various durations—concentration versus percentage injury. c=m s ,
where c=concentration in ppm, m =geometric mean concentration for a^plrticula
exposure duration, s =standard geometric deviation, and Z=number of standard
deviations that the percentage of leaf injury is from the median. (Z for
10% injury is -1.28.) (Reprinted with permission from Larsen and Heck.297)
11-116
-------
Table 11-22
Calculated Injury Parameters for Plants Exposed to Ozone
297
Calculated. 1 njury Leaf injury
threshold (ppn) equation** —
for exposure of parameters
Pollutant and plant
Ozone
a. Bean, Pinto
b.
c.
d.
e.
f.
K.
h.
1.
j.
k.
'-
-..
. n.
o.
Torna to, Roma
Clover, Pennscott Red
Toba'cco, Bel U-3
Spinach, Northland
Chrysanthemum, Oregon
Begonia, Thous. Wonders
Corn, Pioneer 509
Corn, Golden Cross
Bronegrass, Sac Smooth
Oats, Cllntland Bit
Radish, Cherry Belle
Periwinkle, Bright Eyes
Wheat, Wells
Squash, Summer
1 hr
0.10
0.06
0.13
O.OS
0.17
0.21
0.11
0.11
0.08
0.10
0.05
0.05
0.3U
0.30
0.11
3 hr
0.05
0.04
0.08
0.014
0.09
0.16
0.08
0.06
0.05
0.07
0.03
O.OU
0.22
0.18
0.11
8
hr
1
0.03
0.03
0.
0.
0.
0.
0.
0.
0.
0.
0.
0.
0.
0.
0.
.05
,02
05
12
06
03
03
05
02
03
15
11
10
m
g hr
0.31
0.24
0.65
0.34
0.72
1.79
0.76
0.80
0.83
0.64
O.l»7
0.29
1.37
0.83
0.70
s p
e
l.lifc -0.57
1.53 -0.35
1.68 -O.!i3
1.60 -0.68
1.
2.
1.
1.
2.
1.
2.
1.
1.
1.
1.
60 -0.55
00 -0.27
85 -0.31
91 -0.57
11 *"0 • ^ 1*
80 -0.3S
02 -O.lil
72 -0.32
57 -O.ltO
39 -O.US
83 -0.01
Multiple
corrcl .
coeff .
0.98
0.98
0.89
0.93
0.89
0.76
0.90
0.94
0.99
0.95
0.91
0.93
0.91.
0.94
0.96
Injury cone.
ratio
Median
Threshold
3.1
3.7
It
- t
t
8
6
7
10,
6,
.9
.3
.2
.C
.7
.%
.0
.2
8.8
S.W
%.
.0
2.S
C.
5
* The Injury threshold is arbitrarily defined here as 1 percent leaf injury
in the median plant of an exposed set
TJ
** c=m , s^ tp.
g hr g
11-117
-------
data (1, 135 data points) were divided into three susceptibility groupings,
on the basis of information from Table VIII in reference 211 and Table
6-6 in reference 401. These tables -were modified, on the basis of the
analysis of the data used (Table 11-23). The three susceptibility groups
were: sensitive (471 data points), intermediate (373 data points), and
resistant (291 data points). The plants (and appropriate references) in
each susceptibility group are shown in Table 11-24. The underlined
references (in the table) were not used in compiling the data for the
generation of Figure 11-6 and Table ll-24a.
The data developed for each susceptibility group were then analyzed
214
with the equation of Heck and Tingey (Figure 11-6 and Table ll-24a).
This is not to say that the data generated could not be used to develop a
different or more complex model. However, this model presents a
better interpretation of data than other simple models that have been
used. It should be emphasized that the data presented are pertinent
only to pollutant concentrations that produce an acute response in 8 h or
less (two data points in the sensitive group were for 12 h). None of the
information should be extrapolated beyond this period. The data from
exposure of the plants in Table 11-24 (except for underlined references)
were used in the model. Several rather extensive lists of species and
cultivar sensitivities to oxidants, ozone, and PAN are found in a number
67, 235, 236, 269,401,475, 510, 515, 568
of references.
11-118
-------
Table 11-23
Ozone Concentrations for Short-Term Exposures That Produce a
5% or 20% Injury to Vegetation Grown under Sensitive Conditions
Concentrations That May Produce
Exposure 5% (or 20%) Injury, ppm
Time, h
0. 5
1.0
2.0
4.0
8. 0
Sensitive Plants
0. 35-0. 50
(0.45-0. 60)
0. 15-0.25
(0. 20-0. 35)
0.09-0. 15
(0. 12-0. 25)
0.04-0.09
(0. 10-0. 15)
0.02-0.04
(0.06-0. 12)
Intermediate Plants
0. 55-0. 70
(0. 65-0. 85)
0. 25-0.40
(0. 35-0. 55)
0. 15-0. 25
(0. 25-0. 35)
0. 10-0. 15
(0. 15-0. 30)
0. 07-0. 12
(0. 15-0. 25)
Resistant Plants
10. 70 (0. 85)
10.40 (0. 55)
10. 30 (0.40)
10. 25 (0. 35)
10. 20 (0. 30)
a
Data developed from analysis of acute responses shown in Table ll-24a and
Figure 11-6.
11-119
-------
Table 11-24
List of Plant Species and Cultivars by
Susceptibility to Acute Ozone Exposures
SENSITIVE
Alfalfa
410
Dawson257
Glacier257
Mesa-Sirsa257
Moapa
Vernal
257
257
Williamsburg257
Aspen, quaking568
Bean
Pint089»109'136,139,147,212,216,217,
368,433,435,464,492,513,561
Seeway65'105
White166
Sanilac]
.109, 580
Broccoli
214
Calabrese
Chrysanthemum
King's Ransom2-8-^
Mango284
Minn White2-8-4-
Mt. Snow284
Red MischiefM4-
Tranquility2-84.
Clover, red
Kenland52
Coleus
Scarlet Rainbow5
r o
Corn, sweet
Cucumber1*10
Duckweed159
Grass, annual
Grass, bent
Astoria44
Cohansey44
Holfior44
Grass, bent
Penncross
Seaside44
44
Grass, brome
Sac Smooth214
Mustard410
Oats
329-80214
C. I. 754049
Clintland 62214
MO-0-20549
Oneida49
Pendek214
Petunia
Capri5
Pink Cascade67
Pine, jack25
Pine, red25
Pine, Virginia112 113
Pine, eastern white25) 83
Radish
Cavalier4,1*17
Champion449
Cherry Belle4,214,449
Crimson Giant449
Comet449
Safflower
Arizona 14154256
Biggs256
Jordan256
Nebraska 1-1-5-1256
Nebraska-4051256
Nebraska-6256
Nebraska-8256
Pacific-2256
Utah 1421-9-16256
Ute256
11-120
-------
Table 11-24 (Cont.)
List of Plant Species and Cultivars by
Susceptibility to Acute Ozone Exposures
a
SENSITIVE
Soybean410
Clark382
Clark 63382
Cutler382
Dare139,254,382
Haberlandt382
Kent251*'382
Lee382
Lincoln382
Peking382
Richland382
Roanoke382
S100382
Semmes382
Wye382
Spinach
AmericaA3-8.
Dark Green Bloomsdale-3-3-8-
Hybrid 612^18.
Virginia Blight Res. Savoy-3-3-3-
Tobacco
Bel B214
Bel C383
Bel W S*11^4,139,212,214,216,217,
3352,354,361,363,464,1+84
Bel B, Callus11
Bel W , Callus11
Catterton362
Coker 187358
Coker 187-Hicks358
Coker 316358
Coker 319358
Delcrest358
Delhi 61358
Havana 142239
Havana 307239
Havana 501239
Havana 503239
Hicks358
Maryland, 6 cv362
Maryland 10362
Tobacco
Maryland 59362
Maryland 64362
Maryland 609362
McNair 30358
NC 95358
Reams 64358
Samsun181
Speight G-3358
Speight G-7358
Speight G-36358
Va 115358
White Gold214'358
Wilson362
Xanthi181
Tobacco, (N_. glutinosa) l 81
Tobacco, (Itf. rustica)
Brasilia181
Tomato
Heinz 1350448
Marglobe448
Pearson448'497
Red Cherry41*8
Roma214
Roma VF448
Rutgers308'311
11-121
-------
Table 11-24 (Cont.)
List of Plant Species and Cultivars by
Susceptibility to Acute Ozone Exposures
INTERMEDIATE
Alfalfa
Cherokee257
Iroquois257
Kanza257
MSA-CW3An2257
MSB-CW5An2257
MSHp6F-An2W2257
Saranac257
Team2 5 7
Vernal214
Ash, white589
Bean109
Astro109
Bush Blue Lake109
Clipper105
Pinto469
Tempo109
Bean, lima
Thaxter
214
Beet
214
Perfected Detroit
Begonia
Linda5
Thousand Wonders White214
White-Tausendschon5
«
Cabbage
All Season214
Chard, Swiss
Fordhook Giant214
Chrysanthemum
Baby Tears2!4.
Chris Columbus2!!
Corsage Cushion2!4.
Crystal Pat284
Gay Blade284
Golden Arrow48
Pancho284
Penguin284
Pink Chief284.
Sleighride2!4,
Chrysanthemum
Tinkerbell-2-84
Touchdown2-^4-
Yellow Supreme^-8-4-
Clover, red
Chesapeake52
Pennscott52'214
Clover, ladino52
Clover, white sweet52
Coleus
Pastel Rainbow5
Corn
Golden Cross214
Pioneer 509214
Cucumber
Chicago Pickling433
Long Marketer214
Duckweed90
Grass, bent
Highland44
Kingstown44
Grass, Bermuda
Kansas P-1644
Grass, brome
Smooth Sac214
Grass, Kentucky blue
Delta44
Merion44
Grass, perennial rye
Lamora44
Manhattan44
11-122
-------
Table 11-24 (Cont,)
List of Plant Species and Cultivars by
Susceptibility to Acute Ozone Exposures
a
INTERMEDIATE
Grass, red fescue
Highlight44
Pennlawn44
Larch, European112
Lettuce
Dark Green Boston449
Oats
C. I. 757549
C. I. 757849
Clarion119
Clintland 64214
Garry49
Onion
SW34144
Petunia
Comanche67
Pine, Austrian112
Pine, jack112
Pine, Virginia114
Poinsettia
Eckespoint340
Paul Mikkelson340
Radish
Calvalrondo449
Cavalier3
Early Scarlet Globe449
French Breakfast449
Icicle449
Red Boy449
Safflower
Friozi>6
Nebraska-10256
Sorghum
Martin214
Soybean
Amsoy546
Arksoy382
Chippewa 64 546
Clark 63 546
CNS382
Delmar254
Dunfield382
Hark546
Hawkeye546
Kent546
Lee546
Ogden382
P. I. 157474382
P. I. 181550382
Scott214, 546
Traverse546
Wayne546
York382
Spinach
Bounty_33j8_
Northland214
Winter BloomsdaleJLl8-
Spinach, New ZealandlM.
Squash, summer214
Tobacco
56-92B352
Ast— C352
Bel B6-»354»361>363
Bel
Bel W3214
Catterton352'361'363
Delhi 61354
11-12S
-------
Table 11-24 (Cont.)
List of Plant Species and Cultivars by
Susceptibility to Acute Ozone Exposures6
INTERMEDIATE
Tobacco
H,
McNair 12 354
NC-95354
Samsun NN181
White Gold354
Tomato
Fireball8, 28°
Manapal448
Ohio WR-7448
Ohio WR-25448
VF 13L448
VF 145B7879448
RESISTANT
Wheat
Wells214
Alfalfa
Atlantic52
DuPuits52
Vernal211*
Chrysanthemum
Arborvitae
112
Azalea
Alaska214
Bean
Eagle109
Harvester109
Provider109
Stringless Black Valentine109
Tender Crop109
Begonia
Christmas214
Begonia
Scarletta5
Chard, Swiss
.Fordhook Giant214
Chrysanthemum2^
Ann Lady go?-8-4-
Bonnie Jean284
Bright Yellow Tuneful284
Cameo48
Dark Yellow Tokyo2!!*
Distinctive?-8-4.
Flair284
Fuji Jess Williams2-84:
Fu j i-Mef o?H
Golden Cushion284
Golden Peking2-8-4
Golden Yellow Princess
Indian Summer48
Jessamine Williams-?-8-4.
Larry284
Lipstick2-^4-
Mandalay2!4
Muted Sunshine48
Oregon2 l 4
Pink Chief48
Queens Lace
Red Dessert 48»^i
Redskin48.284
Resolute48
Rosey Nook^i
Ruby Mound4 8^2J4
Silver Sheen48
SpinwheelMl
Tinkerbell48
Touchdown48
Tranquility48
Trident48
White Grandchild2-8-^
11-124
-------
Table 11-24 (Cont.)
List of Plant Species and Cultivars by
Susceptibility to Acute Ozone Exposures
a
RESISTANT
Chrysanthemum
Wildfire^84
Yellow Jess Williams284
Yellow Jeanette48
Yellow Moon1*8; 284
Clover
Alsike52
Corn, sweet62
Cotton
Acala214
Acala SJ-1529
Cucumber
Long Marketer211*
Fir, balsam112
Fir, Douglas112
Fir, white112
Grass, Orchard
Potomac 214
Grass, zoysia
Common 4*+
Meyer 44
Hemlock, Easternil2
Holly. English47
Larch, Japanese 112
Lettuce
Big Boston449
Butter Crunch449
Dark Green Boston214
Grand Rapids Forcing 449
Lettuce
Great Lakes449
Imperial #456449
Romaine449
Simpson, Black Seeded449
Maple, sugar229
Oats
Clintland 642l4
Onion2!4
Periwinkle
Bright Eyes2!4
Petunia
Blue Danube162
Blue Jeans162
Blue Sea162
Bonanza5
Calypso162
Canadian-all Double Mix5
Cherry Blossom162
Festival162
Lilac Time162
Parti Pink (Pink)162
Peach Blossom162
Peaches & Cream162
Red Magic (Red)162
Roulette162
Victory I62
Warrior162
Pine, pitch112
Pine, red112
Pine, Scotch112
Pine, eastern white112
Poinsettia214
Annette Hegg68
Dark Red Annette Hegg340
Eckespoint C-l68
Mikkelwhite340
White Annette Hegg340
11-125
-------
Table 11-24 (Cont.)
List of Plant Species and Cultivars by
Susceptibility to Acute Ozone Exposures
a
RESISTANT
Snapdragon
Floral Carpet 5
Rocket Mixture5
Sorghum
Sartin21"
Soybean
Culler2^
Harosay546
Hood546
Pickett546
Scott214
York254
Spinach
Viroflay!
Spruce, black112
S pruce , blue112
Spruce, Norway 1 1 2
Spruce, white112
Sultana
White Imp214
Tobacco
Bel C6
Hicks354
Tomato
Fireball280
Heinz
VF
Vetch, crown
Chemung52
Penngift52
Plants are listed by common generic names followed by species common
name. Cultivars are listed under the common names. Data from the under-
lined references were not used in developing Figure 11-6 or Table H-24a.
11-126
-------
c
o
(0
h
4J
g
-------
fll 1
v |
to S
O ft
01
cn
O
ft
tn
01
P* fr*
0)
QJ 1 0
cO «iH
tfl Q) H JZ
ft 3
3 H
O Cd
ocdl •
QJ £j CJ
!>s ti Cfl £2 6
Ki W »v M (-*
4J O QJ O ft
•H N £3 CJ ft
rH O
•^
,0 O
•H 4J
P* 4-1
QJ U
CJ QJ
to ft
3 to
cn QJ Cd
QJ Cd 10
Q) ,fl O 4-1
!-l 4J 0
JC -rl • *H
H & O O
55 Pt
M to
O QJ
cd m ft
sr >v
CM W H "
1 C G
rH- O 4J O
H 'H C -H
4-1 Cd 4-1
Q) Cd rH T3 Cd
rH 3 P4 i-l I-l
cd w t-i j3 fi ,
E_i O to QJiS
QJ Q) O
Wrf\ i_i f* R
uj H M R
C3 4J J3 0 ft
O C H O ft
ft cd
to rH
QJ PM
T3 1
•> QJ Cj|
QJ 4-1
iH QJ Ptf
H -H
0)
•• cn
C
O M
•HO f>\
4-> >4-l x-s
Co r^
4J a c>
gcd <3
O +
{3
O H
r-
~*~
C
f
CJ
W
1
CO 00 O
O O CO
^O ^0 ^J
o o o
ST ON rH
m o oo
sr m sr
sr vo CM
r*^ vo sr
rH rH rH
, CM CO CO
,0 O 0
*
rH rH O
r-- r-- o
ST rH
- --
CO rH ON
| O 0 O
' • • •
o o o
1
r>. sr vo
in r-» sr
o o o
--
H H H
^^ *^*. ^*^
CO rH CM
rH ON r-
1 CM CM rH
+ + +
O CO vO
^f* ^^ co
1 o 0 0
CM in CM
in vo m
* rH m sr
I i
n u n
CJ O CJ
CO
4-1
C
QJ co tn cn
> rH OJ 01
•H ft & Q
4-1 cn 3
•H rH (d 60
CQ r-i t-i cu
tn
CO rH O OO
ON rH r- sT
^j ^5 CO ^f
o o o o
m CM CM ON
vo oo r-~ oo
in sr sr co
oo vo co oo
in vo CM ON
rH rH rH H
.
rH f^ 0 CO
CO CO CO CM
O O O O
--
oo o CM r~
CM CO vO ON
rH
- - '
)
|
.
0) CM rn vo
C 0 O O
o * • *
2: o o o
, .
OO vo OO CM
in r«. m m
o o o o
.H |H H H
co co sr r^*
sr r** vo co
CM CM rH rH
+ + + +
co r-i oo sr
sr m co co
o o o o
c*> r^ oo in
CM CM ON ST
oo sr o CM
i I 1
R D 0 D
CJ CJ CJ CJ
QJ
CO
O iH
O CJ -O
u a cu
cd c cd -I
E 4J co 43 C
o ca QJ o rl 0) 0)
in 00 rH
ON 00 in
m m m
o o o
O ON f»
co oo m
CM CM i-H
co in ON
rH CM ON
CM rH rH
-i_
sss
000
_ . _ — .
^
st m ON
CM I-H m
VO 00 CO
0 0 rH
o o o
in oo oo
ON OO f»
0 O 0
H H E-i
^^^ ^^» ^^
OO CM CM
vo o m
CM CO iH
+ + Hh
i-H t-H r>-
r^. oo oo
o o o
ON co co
CD CD NO
1 1
n H H
CJ CJ CJ
O 4-1
rl CJ C
0) 4-1 o cd
O QJ ,O 0)
-^ ° ^
c5
vo CM m ON m
ON CM in rH 00
vo r>> vo co ON
o o o o o
vo CM m co oo
O CM vO !*• l*»
rH rH rH
in ON r** o o
m co sr m m
rH tH rH r-l CM
*• *.--
in "oo m m ON
sr 'CO st m co
o o o o o
tr... — .
I
'.
rH vD CO VO vO
0\ CO rH rH ST
CM
m oo oo oo o
CM rH CM CM CO
O O O O O
__^
rH CM in O m
m oo m r-» sr
o o o o o
H H H H H
^m^ "*••»» ^x» *^^ ^x*.
oo sr co r~ oo
r*» o \o co oo
CM CO CM rH CM
M i i i -t
m oo r^ vo rH
ON O rH CM vO
O rH rH rH O
ON CIO VO ON CM
00 ON O r- rH
VO 00 ON ON CO
rH r-| rH CM
n n B n n
CJ O CJ CJ O
tn
4-1
n m c
4-1 OJ CB
C rH rH
cd co co ,0 ft
rH 0) 0) Cd
ft e tn 4-1 x
3 CO QJ *O
•H 60 td 00 O
rH 01 i-l CJ O
rH r-
OO St
m oo
O o
CO vO
CO CM
rH rH
rH !«*
St rH
rH CM
- .
»H ON
st co
0 0
oo m
rH st
co r*.
CM CM
0 0
co oo
oo sr
0 0
H H
^^» '^^^
vO vo
o m
rH CM
+ +
l-l CM
sr m
rH O
O vo
m o
rH CM
n n
o cj
§
E
QJ
r*
t-l 4-1
oi c
jz cd
e w
U t-l
3 JC
11-128
-------
o
4-1
d
•H 10
O
co •
4J O
d
•H 0
O 0
ex M
MH
J3
cu
CM 60
H d
1 rt
CM J-l
U CO
o d
4-4 O
•H
4J 4J
cx rt
CU t-i
O 4J
X d
CU 0)
CJ
« d
X! O
o
oo
1 •
CO
in 4J •
. C- rH
o rt o
v-' rH t-l
cx 4J
cu d
S cu o
•H ,13 U
4J 4->
4-1
d »w o
•H 0
^s
•O CO /-N
CU 0) O
4J CO O
•H d rH
0 O ^
•H ex,
rH CO CTi
CU O>
co s-i
cu o
Kl Ol -U
3 4J
CO 3 O
o o
cx rt 0
X 0
CU CU M
4-1 m
0 0
o d co
t-i 0) 01
<4H T3 CO
T3 T3 O
3 t)
01 o fi
T3 M rt
00
cu 0
M cu ex,
0) > CX
CS -H
4J /-s
CO -H O
d co .
O d H
•H CU ^
4-1 CO
rt o\
3 cu a\
0- rC .
dT^0
M
0
CM
0 0
•rl vH
^J MH
•H
co a
•H 01
ex
H CO
.« CU
01 rl
co rt
d
O 4J •
CX rt T3
CO fi 0)
CU 4-1 CO
H 3
/~\
4J CO CO
d -u d
d rl d
O 01
•rl rH
4-1 rt T3
rt -H d
rl 4J rt
4-1 rl
d rt •>
0) (X CO
o — ' cu
d -rl
o co cj
cj 4J a)
d ex
cu rt co
d 4J
O CO 14-1
N d O
o o
o ex
co 3
•rl 01 O
M S-l
o rt oo
^>l
0)
X!
4-1
>s
Xi
T3
01
d
•H
rt
rH
CX,
X
Ol
d
o
•H
4-1
rt
•H
rl
rt
>
4-1
d
01
u
>-l
01
cx
cu
fi
4J
CO
4-1
d
cu
CO
cu
M
ex
01
rl
X!
o
•H
X!
£
*t
T3
OJ
rl
rt
3
a-
CO
4-1
d
CU
•H
CJ
•rl
<4-4
14H
CU
O
CJ
d
0
•H
4-1
rt
rH
CU
rl
rl
O
U
CU
rH
cx •
•rl rH
4J Q)
rH TJ
3 O
JF s
.
T3
O
•H
M
CU
ex
XI
i
00
d
rt
d
•H
0)
CO
d
o
ex
CO
0)
S-i
frS
m
tH
O
•of
•
CO
•H
CO
>•>
rH
rt
C3
rt
M
01
4-1
3
CX
0
0
O
cu
X!
4-1
J-i
oT
ll-128a
-------
The equations developed and the figures shown reflect the fact
that concentration plays a greater role in the response of plants to ozone
than does time. Although the concept has long been accepted, it is often
217,
forgotten that equal doses do not necessarily give equal responses.
379
That is, a given dose applied over a short period produces a much
greater plant response than an equal dose applied over a longer period.
The concept of a concentration threshold actually ensures this basic dose
concept. Although some disagree with the threshold concept with respect
to the oxidant pollutants, the concept must have mechanistic validity,
inasmuch as organisms have some inherent mechanism for detoxifying
oxidants. This might not be true in the case of some individuals of a given
species that might have lost the inherent protective mechanism. However,
when we are dealing with a large number of species of vegetation and are
attempting to develop some type of realistic oxidant dose response, we must
use the species as a whole, or at least a major subdivision (cultivar) of it.
In these cases, in the work that has been done, there is a rational body of
data to support a threshold concept.
Plants as an Oxidant Sink
211
Heck and Brandt discussed the effectiveness of green belts in
relation to vegetation as a pollutant sink and concluded that vegetation probably
acts as a major sink for air pollutants, including oxidants and ozone, over
time, but has a relatively minor effect on oxidant concentrations during high-
pollution episodes; is more effective in some seasons than others or with some
cultural and management practices than others; and should not be considered
an important contributor to short-term reductions in oxidant or ozone con-
centrations.
11-129
-------
The concept of vegetation as a pollutant sink is significant to the
atmospheric chemist and meteorologist who is attempting to develop air pol-
lution material budgets. There is a need to know the ultimate sinks of air
pollutants released by the activities of man. The preliminary research
results available show attempts to understand the parts played by plants,
soils, and soil organisms.
569
Turner et al_. reported that freshly turned soil exposed to air
was a significant sink for ozone. They found that soil was about 50% as active
570
as charcoal in removing ozone from air. Turner e_t aL reported ozone
flux within a maize field and a forest. They determined that vegetation
could reduce ozone loss to soil -when plants were under stress, but
supported the view that vegetation and soil could be the primary sinks
322
for ozone. Macdowall found that soil absorbed twice as much ozone
as mature field-grown tobacco growing on the soil. He concluded that soil
is an effective sink and may play a protective role, in that it tends to keep
2
the oxidant concentration within the canopy low. Abeles suggested that most
soil activity, in relation to reduced pollutant concentration, is associated
with the metabolic activity of soil microorganisms. This may not be true
with ozone, because it is such a reactive gas. Soils may play a more important
role than has been suggested, but they are usually covered with vegetation
and in general are probably less important than vegetation in acting as pol-
lutant sinks.
460,527
Two reports based on rather gross measuring techniques
found a close correlation between ozone uptake and transpiration. These
studies indicated that stomatal control is the prime factor in controlling
pollutant uptake and that cuticular sorption is negligible in relation to
11-130
-------
stomatal absorption. These findings are generally supported by past work
that indicates that stomata are the prime sites of pollutant entry into plant
tissues. However, cuticular sorption may be a. small but effective sink,
563
over time. Townsend used similar techniques and reported ozone
sorption by nine tree species. He did not attempt to separate stomatal and
cuticular sorption. White birch showed a linear uptake from 0. 10 to 0. 80
ppm (Figure 11-7) and only a 5% decrease in uptake rate over an 8-h exposure
at 0. 20 ppm. Uptake in red maple was linear to 0. 60 ppm and was at
only 40% of the maximal rate after an 8-h exposure to 0. 20 ppm. Townsend
presented values of actual uptake rates that may be of value. Several of
these are given in Table 11-25. All these studies determined uptake on the
basis of the time needed to deplete the ozone in a closed system. This does
not permit a high reliability in the data given, but they are among the best
available.
233
Hill reported pollutant uptake values for a number of gaseous
pollutants, including ozone and PAN, with alfalfa as his test organism (Table
11-25). These values were obtained with a dynamic, but closed, exposure
facility. Uptake was determined by the amount of pollutant needed to maintain
a constant chamber concentration over an alfalfa bed. Uptake values, expressed
on the basis of leaf area, reflect the effect of the plant canopy on the exchange
of gases within the canopy and do not give the maximal capability of plants for
pollution sorption. They are, however, representative of the agricultural
situation. The values shown are an order of magnitude below those reported
563
by Townsend and reflect the experimental conditions used, as well as the
test species. Hill's use of the alfalfa canopy partially explains his lower values,
but the technique used by Townsend could have resulted in inflated values.
11-131
-------
CM
I
E
T3
o
s
v_x
0
(B
white
birch
0
Ozone Conc.(pphm)
Figure 11-7. Net ozone uptake by foliage of red maple and white birch seedlings
in relation to ozone concentrations. (Reprinted with permission from
563
Townsend. )
11-132
-------
Table 11-25
Rates of Oxidant Uptake by Selected Plant Species
Plant
Species
White oak
Pollutant
O
Uptake Rate
-2 -1 -1
(yg, dm , hr < pphm. ) Reference
32
563
White birch
O
27
563
Sugar maple
O
19
563
Sweet gum
O
14
563
Red maple
O
14
563
Alfalfa
O
1. 1
233
Alfalfa
PAN
1.2
233
11-133
-------
22
Bennett et aL have presented a model for gaseous pollution sorption
by plants. The model includes all the known factors that might have a
significant effect on pollution sorption by plant leaves, including gas con-
centration (ambient air and internal leaf), gas fluxes (external and internal),
resistance to flow (Leaf boundary layer, stomatal, and internal), nature of
leaf surfaces (stomatal presence, cutin, and surface properties), importance
of gas solubility and thus solute concentration -within the leaf, and ability
of the plant to metabolize pollutants (decontaminate itself). They mentioned
the reactivity of ozone as another factor to consider. They believe that
surface sorption may be important, at least over short periods. They
presented a possible mathematical representation of these factors, which
they suggested is equivalent to the mathematical statement of Ohm's law.
21
This material is well integrated in the review by Bennett and Hill.
466
Rogers used a constantly stirred tank reactor that permitted
instantaneous mixing of incoming air with air already in the chamber. The
system was based on a dynamic exposure design with a single-path air flow-
system. This system, should permit the development of maximal uptake
rates under given oxidant loads and a more accurate appraisal of the effects
of oxidants on stomatal activity. The chamber design permits a constant
turbulence within the chamber and an average air flow over leaf surfaces.
Within bounds, one can vary this turbulence, -while maintaining a uniform
mixture of pollutants in the chamber. Preliminary work with this chamber
233
have produced uptake rates essentially doubling those reported by Hill
for nitrogen dioxide. However, Rogers has not yet used the design to
study other oxidants (ozone and PAN).
11 -134
-------
Oxidant uptake rates are controlled by inherent variations within plant
species, the effect of the oxidant on the uptake potential of the plant, the effect
of environmental stresses on the uptake potential, and meteorologic factors
that affect pollutant distribution. It is important to know •whether both resistant
and sensitive plants act as oxidant sinks or whether only sensitive plants are
major sinks. This knowledge requires some understanding of the mechanism
of plant resistance to oxidants. If resistance is associated with stomatal
142
closure due to the oxidants, then resistant plants will not act as effective
sinks. However, if resistance is physiologic, these plants could act as effective
oxidant sinks, with little adverse effect on the plants. Neither resistant nor
sensitive plants would be effective sinks under environmental stress that caused
stomatal closure.
Plants probably act as major oxidant sinks over both time and
distance. However, it is important to remember that plants do not respond
in a predictable way over time and are not active over the greater portion
of the year. The total capacity of plants as sinks with or without harm to
the receptors is not known.
Plant Protection
Air pollution research in effects on vegetation has focused largely on
symptom identification, dose response, and mechanisms. The purpose has
been to develop criteria necessary to understand effects and to form a basis
for the promulgation of ambient air quality standards. Environmentalists
were not concerned with protecting plants per se, but in controlling emission.
Thus, those interested in protection of plants received little encouragement.
In addition, no economical ways were suggested for control, and research
11-135
-------
leaders were not convinced of the importance of adding air pollution stress
to breeding programs. It -was the hope of most research -workers that air
quality standards would protect vegetation from ozone and other oxidants.
Most research workers are now convinced that pollution abatement
will have little impact on overall pollution concentrations until clean energy
forms are developed and in widespread use. Because phytotoxic concen-
trations of ozone and other oxidants are inevitable for the foreseeable future,
researchers are seriously considering other means of protecting plants from
injurious effects of oxidants.
For managed agricultural crops, including forest species and other
woody perennials, the addition of air pollution stress into standard breeding
programs has begun or is being discussed. Some workers are trying to
develop protective sprays for the more sensitive species and cultivars.
Some consideration is also being given to the management of cultural
415
practices and to general land management. Ormrod and Adedipe have
presented an excellent review of the concepts and work to date regarding
the protection of horticultural plants from, atmospheric pollutants.
Breeding for resistance. Varietal studies define the genetic
variability in resistance to oxidants within different species. These types
of studies are necessary to select genetic lines or accessions for breeding
programs. Although plant-breeders have not selected for oxidant resistance,
selection probably has occurred, for two reasons: breeders normally select
plants with the highest yield and least injury, regardless of cause; and many
breeding programs are carried out in areas of relatively high oxidant content.
In this regard, natural selection pressures should increase the tolerance of
11-136
-------
populations of native species near urban industrial areas, although this would
tend to reduce the genetic plasticity-within sensitive species.
Oxidant problems are starting to be of concern to plant-breeders.
Extensive varietal screening of tomato, petunia, and other plants has permitted
some resistant cultivars to be recommended for use in high-oxidant areas.
None of the varietal screens have involved breeding experiments in -which
resistant lines are developed and used in the development of resistant varieties
for new introductions.
Growers in the Connecticut valley have probably selected wrapper
tobacco for oxidant resistance since the 1950's. Similar selection is probably
472
taking place in other tobacco-growing areas. Sand worked with a number
of wrapper selections and suggested a partial dominance of genes for fleck
resistance. He found that the F hybrid between a sensitive and a resistant
1 440
selection was more resistant than the parental average. Povilaitis used
five tobacco varieties and made six crosses with six genetic populations from
each cross, for 36 different populations. He used injury ratings and, unlike
Sand, suggested that susceptibility may be dominant over tolerance (dominance
•was important in five of six crosses).
266
Johnson .et al. determined the variation in response of 16 sweet
corn hybrids to ambient oxidants in California. From these observations,
62
Cameron and Taylor selected five inbreds and three of their F hybrids
1
for further field studies and four inbreds and two hybrids for use in ozone
exposures. The relative effects of the polluted environments were the same.
The final data suggested an inheritance for partial dominance to ozone sus-
ceptibility.
564
Townsend and Dochinger worked with four red maple selections
and found sensitive and tolerant selections that showed the same relative
11-137
-------
susceptibility over four growth stages and four Leaf developmental phases.
Symptoms were similar in the four selections, but the design should have
used lower ozone dosages. These results suggest a strong genetic control
that will facilitate selection of ozone-tolerant seedlings for urban use.
248 250
Houston and Houston and Stairs did clonal repeatability analyses
to determine genetic: control of tolerance in white pine with an ozone-sulfur
dioxide mixture and a 6-h exposure. They used needle elongation and two
injury estimates in assessing effects. The repeatability estimates indicated
that tolerance to the pollutant mixture is under genetic control. The nature
of the inheritance of tolerance is still not understood, but field selection of
122
tolerant or susceptible individuals is possible. Demeritt e_t aj_. reported
an evaluation system that used visible needle injury for determining resistance
of Scotch pine to ozone. This permitted the discrimination of phenotypic
differences in a quantitative way. Results suggested that a few genes were
responsible for resistance in Scotch pine. A program -was initiated to select
582
for ozone resistance in loblolly pine, but no definitive results are available.
As genetic understanding develops, it will be incorporated into basic
breeding programs that are concerned -with such characteristics as yield,
growth habit, insect and disease resistance, flavor, and texture. These
programs will be most effective if present ambient ozone and other oxidant
concentrations do not increase.
278
Protectant sprays. Kendrick ^t al_. first reported protection
of pinto bean foliage from sprays or dusts of four fungicides. They later
11-138
-------
reported rather extensive studies that used a number of fungicides and
277
antioxidants on selected test plants. These tests were in general
agreement with the earlier studies and suggested that the response was due
267
to a surface deactivation of ozone and other oxidants. Jones found
protection of tobacco with various particulate substances, including charcoal.
170
Freebairn and Taylor found protection from use of ascorbate sprays
as antioxidants. They reported partial protection to pinto bean, petunia,
celery, lettuce, and grapefruit from oxidant injury in the Los Angeles basin.
Several other early studies reported various degrees of chemical protection
30,575 502
from fleck injury to tobacco. Taylor and Rich found that an
antiozonant-treated cloth protected wrapper tobacco from oxidant injury.
These early studies, along with the recognition that oxidant pollution
will continue as a significant problem, encouraged a number of studies
directed at finding chemical treatments that might serve a dual function
with a minimum of applications. Some selected results of these studies are
summarized in Table 11-26.
The fungicides, as a group, have received the most attention, and
Benomyl (methyl-l-butylcarbamoyl-2-benzimidazolecarbamate) has been most
widely studied, owing to its protective properties. Benomyl has been used
as a foliar spray, a soil drench, and a soil amendment. Mixed results have
been reported when benomyl was used as a spray. Protection was reported
446 334,343,479 99 276
on tobacco, pinto bean, white bean, and grape; no
433,434 433
protection was found for pinto bean, and cucumber. It was not
possible to equate the Benomyl concentrations used, but most were 20 - 4, 000
ppm. Most reports on soil applications showed protection against oxidants.
Soil drenches at 10-1,000 ppm gave complete to partial protection for
11-139
-------
6
O
OJ
CJ
ti
CD
O
t-
O
CO
in
t^
m
1/5
l>
m
c-
cd
H
cd
O
•H
OJ
01
•H
4-1
CJ
OJ
PH
c
o
•H
4-1
Cd
a
•H
rH
O.
PL.
S-l
C
cd
3
C
>4-( O
O iH
4-1
a o
a) o
u 4-1
oo o «
4) M
Q PH S-?
a
cd
»4H 4-1
O O
CD
CD 4J
PH O
>, *H
H PL,
O
•H
4-1
tti
M
cd
u
0) C
cScS
CM
m
0
-P
C3
C S
O
<£ °
^ o
I O
CO
-P
c
co
•o
•H
X
O
•H
-P
C
<
•P
c
CO
T3
•H
X
O
•H
-P
C
<
0
TD
•H
CJ
•H
bO
C
3
P-.
0
•P
CO
O S
CJ
J? o
< o
I O
4-1
cd
a)
cd ,£>
a) u cd
d o -H
0) v-l M
rH .fl
i>> 4J
J-i -H
CTj
(D 4-1
I en en
C -H 3
N ,0 T3
00
•P
c
CO
TD
•H
X
O
•H
•P
X
0
G co
O -H
bfl f-i
00
t>
03
TJ
•H
X
O
•H
X r-l
X2
C ca
O -H
M ^
>> C3
O
O
I-l
co
•D
•H
X
0
•H
-P CD
51
cd
.H
K^
K^>
S
0)
rC
ft
•H
rr-\
U
rH
>.
4-)
CJ
O
•H
n
<
CD
1)
cd
rH
rH
t^
4-1
3
^
a
•rH
0
TD
•H
O
•H
M
C
f=4
i— (
CO
S
In
0
c
' — ^
pi
*i-i
0
C
•H
N
1
^
0
tfl
P
0
•D
•H
O
•H
be
C
£
co
E
k
O
C
0
Cfi
CO
rH
PH
4-4
O
C
o
•H
4-1
O
CD
4J
O
J-l
PH
4-1 T3
C 0)
Cd 4J
4J CJ
3 0)
rH 4-1
rH O
O )-l
PH PH
-P
C
KI
T3
•H
X
o
-P
&
co
"V
•r-t
X
o
•P
c
CO
TD
-rH
X
O
4J
§
C/3
O
4J
C
•H
PH
cd
•H
3
O
c
cd
0)
co
•r-t
c
o
o
u
co
•P
C
C3
•u
-H
u
cd
>
•H
4J
rH
3
U
O O
o
U 0)
CO 4-1
xa -H
O rC
H 3
-P
C
C3
•a
•H
X
o
ivar
« O
o o
o
CJ 0)
Cd 4-1
f -H
O ,C
H 3
-P
c
as
"O
•H
X
O
ivar
U TD
O O
O
O CD
Cd 4-1
42 -H
O JS
H S
-P
c
a
•o
•H
X
o
C
•H
PH
J-J
CB
D
a
C
cd
0)
pp
c
o
N
O
c
•H
PH
J-l
cfl
C!
n)
CD
M
11-14 )
-------
B
o
a
3
0)
M
4)
v
C W
CD f-<
T3 ft
CO CO
i-l
>>£
N ft
a ft
WO
C0| CO
^ ^
.B
•p
o
0
iH
O
•D
•H
>»
O
C
<'
•p
CO
J-I
CO
•p
M
J>,
CO
ft
w
E
ft
a
4
o
M
•s-X
(!)
T>
•H
O
•H
&UO
C!
fe
x^\
O
c
0
TJ
E
ts a
o o
C 0
0 in
CQ '^-^
0
•H
to
r*4
3
e
> e
O ft
CD in
0
.,_!
4-1
rH
o
W
+J
C
0
•H
J-i
•P
3
B
0
•D
•H
CJ
•H
C
^
(^
s~<.
•H
O
to
B
•H
>, ft
O
B 0
0 CO
CQN.X
0
-0
•H
CJ
•H
bO
rH
fe
rH
>>
enom
CQ'
*
CO
\ to
00 0
^ E
•H
r> -P
CD CO
^.x
CO
4-1
O
•H
4-1
O
Q)
4J
o
M
CM
C
CO
TJ
•H
X
o
a)
4J
-------
>
• i-H
|H O ^
E m
V(
ca
"^
C
C3
SH
fcJJ
t^-
O
rH
G
0)
E ^
r* ^
c O
CD (H
S a
CO P
p— 1 -^^
•H 60
£«>
xide Insecticide 99
n)
0 O
4-1 -rl
3 4-1
1_r^ j3
rH rH
>, O
C to
O
CU B
ft
•H CM
PH *-»
3
rH
PM
MH
O
o
•H
4J
O
0)
4J
O
rl
PH
i
4-1
H
H
O
PL,
C
O
N
O
-P
C
CO
t>
•H
X
O
O
m
CM
a)
C «
o 0
N ft
O ft
CO
t>
0)
T3
•H
CJ
•H
•P
CJ
(1)
tfl
G
r-l
CD
C
ca
n
C72
m
co
o 43"
CM
CU
SB
N ft
O ft
CM
CO
-P
C
ca
T3
•H
X
O
m
CO
CO
oo
01
> >»
E 03
O JH
c a
0) W
CQ ^-^
cu
*o
•H
o
•H
M
c
fax^x
•p
G
E
T3
C
0
E
ca
rH E
£>•> Pi
E a
O 1
G 0
0) CD
CQ ^^
cu
•o
•H
0
•H
bfi
c
3
r-H
O
E
•H
^
CQ
•H
JH
fH
CD
•o
•H
O
•H
bO
C
3
60
60
i ^^
O 4-1
CO Cj
. v QJ
S
^ _j (^
TD
r-i CU
K*> §
SCO
0 rH
G -H
OJ 0
(X) W
-p
G
ca
13
•H
X
O
•H
4J
C
*o
•H
O
ca
o
•H
o
?H
O
CJ
CO
•a;
m
CM
0
O
S^
CU
o
N
0
^— ^
43
CM
t\
S
ft
o
CO
a
0
cu
0
N
-O
^— \
43
^
A
a
ft
&
m
CM
o
O
cu
a
o
N
o
S-*ti,
43
^j.
€\
a
&
&
o
1
CO
i — i
•
O
cu
(3
O
N
O
/—\
43
in
0
A
a
&
ft
S
H
PM
co
(U
U
(!)
ft
CO
Vl
cd
>
•H
4J
i — 1
O
*
cd
cu
m
0
jj
(3
•H
PM
c
o
g
cu
H
CO
^1
cd
>
•H
4J
3
O
c
CU
«
o
4J
(3
•H
PM
C
cd
o
£j
CO
H
o
CJ
o
C3
o
CJ
o
C3
Vl
cd
^
•H
4-1
rH
3
O
*
G
cd
cu
pq
0
Pn
a
cu
H
H
cd
3
C
C
cd
CO
01
cd
J-l
O
CU
3
rH
43
Vl
cd
^
•H
4-1
rH
3
U
91
C
. cd
cu
o
4-1
C
•H
PM
^l
cd
•H
4J
rH
3
O
„
C
cd
cu
PQ
O
4J
C
•H
PH
j_j
cd
•rl
4-1
rH
3
CJ
„
13
cd
01
pq
CO
4J
•H
|3
11-142
-------
V
o
s
i!
ID
co
o
10
CD
r-
CO
x^»
•
U
a
0
u
cd
o •>
•H a
S <4H O
01 O -rl
.fl 4J
CJ CU cj
0) CJ
CU rl 4J
> 60 O O
•H CU rl
4-> Q p* M
CM 00
00 CD
a
01
•I—)
o
t.
H
PH
H j
O
c
o
•H CJ
4-1 P,
cd £
•2 H
0)
jj ^
a -H
•C § 0
•P T3 -H
* % &>
o « e
r< $ 3
o (S ^
, ^
fl
M-4
rv
3* ,
^
a>
m
0)
•a
•H
0
•H
be
a
3
PC<
teS>
O*^
/v^
<3^
00
0)
>,
N
C
w
o
rH
•
CN
CO
H
C
cd
§
M
10
4-1
e
cd
c
o
•rl
4J
U
o>
•H
4-1
(0
•3"
°-g
o
JA O
CJ CJ
4-1
1-1
o
in
o
ffi ca
Q V<
< D.
CO 03
01
C
r-( CD iH
6 T3 S >>
O O C3
C E C ^
0} ft (U ft
« ftCQ W
C
a
•a
•H
X
O
•p
c
03
T3
•H
•P
c
ra
"0
•H
X
O
CO
ra
-D
•H
X
o
SH
(V
0)
•P
O
0
•i-J
c
€
ft
ft
cu
g
•
4J *
rt o
cd o)
H p.
PM OT
CO O
•H 0
C 0
3 CO
•P ft
0) O
ft f-l
o
CJ
CJ
CO
ft
o
H
o
o
o
co
ft
o
ft
•
T3
CU
4J
•H
0
CO
CU
o
c
cu
)-J
CJ
>4H
01
M
cu
j3
4J
0
o
rl
14-1
cd
4J
cd
T3
T3
CU
4J
0
0)
iH
>
cd
rl
p.
CO
CO
cd
T3
cu
•rl
i-H
P.
P.
cd
01
^-1
cd
0)
CO
cu
H
tCs
a result of the protectant treatmen
CO
cd
0)
rt
0
N
o
§
J_l
IK
p>%
!_i
3
•r~)
c
•rl
4J
(3
cd
, — 1
p.
•H
o
•rl
4-1
o
3
T3
01
M
4-1
c
0)
O
}4
CU
^
•
Pi
o
•rl
4J
cd
a
•H
rH
Pi
P.
cd
4J
c
cfl
4-1
O
CD
4-1
O
M
P.
>,
,0
T3
rH
0>
•H
^
c
•rl
01
CO
cd
cu
rl
a
M
ti
11-143
-------
342 434,561 284
poinsettia, pinto bean, chrysanthemum, and annual
384
bluegrass. Soil amendments
341,433,434,469,479
at 2-160 ppm were effective for pinto bean, annual
384 433 503
bluegrass, and cucumber. Taylor and Rich reported that a
single soil amendment at about 25 ppm protected the first eight leaves of
tobacco, but not the younger leaves. They also found less tobacco root
cyst nematodes from benomyl applications, and the fungicide -was not toxic
433
to the plants at the rates used. Benomyl does not induce stomatal closure,
503
so an internal physiologic mechanism must be involved. The active
434,561
ingredient is the benzimidazole moiety, which inhibits senescence
561
in bean and also inhibits the loss of free sterols in plant membranes.
493
Sterols themselves are effective inhibitors, and the mechanism of action
may involve effects on membrane sterols and thus membrane permeability.
492
Spotts e_t al. studied the effects of benzimidazole and ozone on several
water relation effects that suggest that the protection is due to the effect
of benzimidazole on the cell membrane.
The fungicide Carboxin has received some study, but with varied results.
98
A 0.43 mM solution gave protection at 5-10 days in white bean, a 0. 36%
334
spray gave no protection to pinto or tempo bean, and a 0. 01% spray
386
increased injury to azalea. Soil applications of Carboxin were generally
more beneficial, but results were still varied. A Carboxin soil amendment
503 458
was phytotoxic to tobacco and pinto bean, although protection -was
noted in pinto bean. Pinto and tempo bean were protected from oxidant for
334
36-40 days after a soil amendment with Carboxin at 8 g per 4. 6-m row,
and the sulfoxide analogue gave protection to white bean, with a 13% yield
99
increase. A soil drench gave protection to soybean, cotton, tomato, and
11-144
-------
458
tobacco at 9. 5 ppm, but a soil drench at 1-100 ppm increased
386
senescence in azalea due to oxidants. These differences in species
or conditions of application, but they do call for clarification of the possible
role of this fungicide (Carboxin) in protection against oxidants. Carboxin
458
had no effect on stomatal opening, and its protective action appears
99,458
due to the sulfoxide breakdown product, -which is not fungistatic.
Thus, although it can serve a dual role, the modes of action are dissimilar.
In addition to the compounds named, several others have been studied
68
briefly. Cathey and Heggestad found protection to eight cultivars of
poinsettia after treatment with the growth retardant Ancymidol and
Chlormequate. They also reported a 75% protection in petunia treated with
the growth retardant succinic acid 2, 2-dimethylhydrazide (SADH) as a 0. 5%
67
spray. This was part of a screen of 65 petunia cultivars to ozone.
They found that the resistant cultivars did not respond to SADH; this suggested
that protection may be related to modified leaf structure (reduced cell size,
intercellular space and stomata, and thicker cell walls). The SADH treatment
was not effective above an ozone concentration of 0.45 ppm for 3 h. Adedipe
3
and Ormrod found that a 30-ppm spray of the growth hormone N-6-
benzyladenine protected radish from ozone at 0. 25 ppm (4 h), and Fletcher
166
£t aL protected white bean by use of a 1-ppm abscisic acid (ABA)
solution. The ABA caused partial stomatal closure, which the authors
suggested is the mechanism of protection. Studies with ascorbic acid on
105 288
white bean, the insecticide piperonylbutoxide on tobacco, road dust
573 435
on pinto bean, and a wax emulsion (Folicote) on pinto bean all stressed
that many compounds can act as protectants to vegetation against oxidant
(ozone) effects.
11-145
-------
296
Larkin injected several peroxidases at 0. 1-10 ppm into one half
of a tobacco leaf and found some protection. He suggested that peroxidase,
which is often associated with plant stress conditions, may be important
in physiologic resistance. It is doubtful that any one mechanism of action
exists. It is important that we understand the mechanism of ozone injury
and resistance in plants, so that we can determine better what chemicals
may play a role in protecting plants against oxidants.
We do not yet have good answers to four basic questions that have kept
protective chemicals from practical use: we do not know the frequency or
rate of application needed for continued resistance, or, therefore, the total
cost of application. We have little idea of the specificity of selected chemicals
on different plants. Little is known of possible undersirable residues or side
effects. We do not have sufficient prediction accuracy for high-oxidant
days for chemicals that are not long-lived. These basic questions need to
be answered as chemicals are tested and promoted for use. The ideal
chemical would be effective on several species (cultivars), have multiple
uses (e.g., fungicides), have a long life (a single preemergence soil application
would be best), and leave no toxic residues. Such chemicals would have
value, at least until breeding programs can incorporate resistance to pol-
lution stress into new cultivar introductions.
415
Cultural practices and land use. Ormrod and Adedipe have
developed an excellent presentation on edaphic and climatic factors that play
a role in making plants more resistant to ozone and other oxidant stress.
They suggest how these environmental factors may be used in cultural and
management practices to help to alleviate the effects of oxidant pollutants.
11-146
-------
These practices may be of help in greenhouse management and to some
extent in field irrigation systems. The association of water stress with
resistance to oxidant has long been recognized, and growers have been
urged to keep this in mind during periods of high air pollution potential.
The increased use of carbon dioxide in greenhouse management would have
a positive effect, but the additions are made during cooler months, when
oxidant concentrations are not high. These practices are worth considering,
but are as yet of no more than supplemental help.
124
Dochinger was able to predict chlorotic dwarf on seedbed white pine
501
with greater than 90% accuracy. Taylor found that susceptible and resistant
tobacco could be identified in seedbeds. Both suggested that, for some sensitive
plants, time could be saved by visual screening of transplant beds and the use
of only the more resistant members of the population as transplants.
Interest in land use planning--with respect to areas to be set aside
for agricultural use, as opposed to industrial use--needs to be considered
as a potential ameliorating factor in the control of air pollution effects on
vegetation. Land use might not be as effective for the oxidant pollutants,
211
because of their ubiquitous nature. Heck and Brandt have developed
a brief but acceptable point of view in terms of the need for land use planning
and protection of agricultural commodities from air pollution.
A rational approach to land use planning for air quality maintenance
may be built on the basis of diffusion modeling. Although the photochemical
versions of the models that relate air quality to emission are only beginning
to be applied, there has been sufficient validation to permit their use at least
to obtain relative assessments (in contrast with prediction of absolute pol-
lutant concentrations). Chapter 5 discusses the principles and performance
11-147
-------
of models that can be used for studying the distribution of photochemical
ozone and other oxidant concentrations. The application of these techniques
requires a succession of forecasts, beginning with land use patterns and
continuing with transportation network usage, vehicle emission intensities,
stationary-source contributions, and, finally, patterns (in space and time)
of pollutant input to the atmosphere. Meteorologic characterizations based
on detailed weather data provide the transport measures needed. For various
scenarios, the model generates statistics on the air quality that should be
expected. The loop is closed by adjusting the land use to achieve the desired
atmospheric pollutant concentrations.
RESPONSES OF NONVASCULAR GREEN PLANTS
Lichenologists have long used the presence and abundance of lichen
and moss species to map the biologic impact of latrge urban and industrial
164
areas. Early workers considered changes in the presence and abundance
of these organisms to be related to such factors as temperature and humidity.
More recently, most researchers have tended to relate changes in lichen
population more to industrial air pollution than to other environmental changes.
Although most of the air pollution work lacks ambient air quality measurements,
there is strong indication that both the presence and the abundance of lichen
and moss species are correlated with sulfur dioxide concentrations in large
urban and industrial areas. Such studies have not been done in areas where
oxidants are the primary air pollutants, nor in rural areas -with relatively
high oxidant and mixtures of sulfur dioxide and nitrogen dioxide. Thus,
little is known about the direct effects of ozone or other oxidants on lichen
and moss morphology or physiology.
11-148
-------
78
Comeau and Le Blanc found that a 4-h exposure of Funaria
hygrometrica to ozone at 0. 25-1. 00 ppm stimulated the regenerative
capacity of the moss leaves. This •was not true for 6- and 8-h exposures.
178
Glater reported oxidant injury to several species of fern in the
Los Angeles area. Initially, tan lesions appeared near the smaller veins,
but in no special pattern. Later, the entire leaf became necrotic. Symptom
development and sensitivity of leaves were different from those noted in
vascular plants. All leaves appeared to be equally sensitive, except for the
growing tip and the youngest uncoiling leaves. Occasionally, a young plant
was killed.
We know little about the overall effects of ozone or other oxidants in
the nonvascular green plants. Although they may not be economically important,
such effects may have an adverse ecologic impact.
RESPONSES OF MICROORGANISMS
Heagle reviewed the effects of ozone on fungus growth, sporulation,
and germination. Ozone may inhibit colony growth on artificial media, but
rarely causes death, even at high concentrations. Differences in species
susceptibility are known. Exposure to ozone at 0. 10 ppm for 4 h stopped
455
conidiophore elongation and spore production in Alternaria solani. In
several fungi, exposure to ozone at 0. 10 or 0.40 ppm for 4 h caused a 10-
196 197
fold to 25 -fold increase in sporulation. Heagle reported effects
on three obligate fungi from low ozone exposures. Spore germination was
292
not affected in any of these studies. Kuss grew 30 representative fungi
on agar and often found increased spore production after exposure to ozone.
Spore germination was decreased in most species, but increased in others.
11-149
-------
442
Rabotonova exposed two species of yeast to ozone: Candida
lipolytica "was sensitive, and C. auilliermondii was resistant. The
biocidal activity of ozone was determined under various cultural conditions
with air streams of about 150 or 5, 500 ppm (v/v for 10-30 min). Ozone
was an effective biocide under most conditions, and effectiveness increased
270
with decreasing pH. Kanoh found that exposure to ozone at 30 ppm for
30 min increased oxygen uptake in slime mold (Physarum polycephalum)
homogenate. The ozone also increased succinoxidase activity and inhibited
118-121
part of glycolysis. deKoning and Jegier reported effects of ozone
on Euglena gracilis that included reduction of net photosynthesis, increase
in respiration, and effects on pyridine nucleotide reduction and phosphorylation.
They reported that reduction of net photosynthesis was a logarithmic function
118
of ozone concentration in 1-h exposures. They also found a 5% reduction
in oxygen evolution after a 1-h exposure to 0. 5-ppm ozone bubbled into 5 ml
121
of solution and an additive effect with a mixture of sulfur dioxide and ozone.
574
Verkroost carried out a. detailed study of the effects of ozone on
Scenedejamus obtusiusculus, Chod. with special concern over the effects on
photosynthesis and respiration. A major weakness in this study was the
use of an air stream containing ozone at 150 ppm. The report suggested
that the primary site of ozone action is the membrane structure, -which
produces changes in photosynthesis and respiration.
Ozone at high concentrations has been used in a variety of applications
for the control and suppression of fungi and bacteria. These applications
182
have included food protection, drinking-water purification, and treat-
281,350
ment of sewage. It is generally accepted that ozone is not an
effective germicide at concentrations below the point of human sensitivity--
11-150
-------
0. 04 pprn. The germicidal effectiveness depends on concentration,
relative humidity, and the specific organism. In many cases, even a
concentration of 3-5 ppm -was not sufficient to kill some bacteria.
58
Burleson et al. showed inactivation of several viruses and bacteria
after ozone exposure and a greater inactivation with simultaneous
597
sonication. Zobnina and Morkovina related the tolerance of a
carotinoid strain of Mycobacterium carothenum with the presence of
the pigment. The dwarf mutant was much more sensitive.
Large doses of ozone may inhibit growth and sporulation of fungi
490
on fruit, although most fungi tested were resistant to ozone. Spaulding
reported that ozone acted as a surface biocide. Above 0. 5 ppm, ozone
inhibited surface growth of fungi on strawberry and peach. At 0. 06 ppm,
it severely injured leaves on head lettuce after 8 days. He also reported
463
some direct injury on peach fruits above 0. 5 ppm. Ridley and Sims
extended the shelf-life of strawberry and peach by exposing them to ozone,
but stated no concentrations. Ozone at 1-2 ppm for 1-2 h/day controlled
the surface growth of fungi and sporulation on apple, reduced offensive odors,
489 579
and decreased the ripening rate. Watson found that ozone at 0.4-2.0
ppm acted as a surface fungicide, but did not penetrate. Thus, there was
no effect on fungal growth within the fruit. Sporulation and some decay
control of Penicillium digitatum and P. italicum were noted in open storage
92
boxes of lemon and orange exposed to ozone at 1 ppm. Ozone was more
effective than a fungicide dip in controlling Botrytis bud rot of gladiolus,
329
but no concentrations were determined. In general, researchers have
suggested that rather large dosages of ozone are required to protect storage
fruits from fungal infection. These concentrations may be so high as to
11-151
-------
preclude the use of ozone in storage facilities. The ability of ozone to
reduce spore germination in fungi apparently depends on species, spore
196
morphology, moisture, and substrate. Single-celled spores and those
with thin cell walls are most sensitive. Wet spores are more sensitive than
dry spores.
185
Haines reported that ozone at 4 ppm retarded growth of Escherichia
476
coli, whereas 10 ppm prevented growth. Scott and Lesher found that
7
approximately 2 x 10 molecules of ozone per bacterium killed 50% of the
cells of E. coli and that the primary effect was on the cell membrane. Only
140
metabolites leached from the cell were affected. Elford and van den Ende
reported that ozone at 20 ppm had a lethal effect on some bacteria deposited
from aerosol mists on various surfaces. Relative humidity is an important
factor, particularly when ozone concentration is low. They found little death
at a humidity below 45%, at concentrations of 1 ppm, as opposed to a 90%
kill in 30 min at 0. 025 ppm with a humidity of around 70%. A 5-m.in exposure
of Bacillus cereus to ozone at 0. 12 mg/liter was the minimal lethal dose,
56
whereas 0. 10 mg/liter was effective for B. megaterium and E. coli.
Spores of the Bacillus sp. -were killed by ozone at 2. 29 mg/liter. These
responses were of the all-or-none type with ozone between 0. 4 and 0. 5
mg/liter of water. Time of exposure, from 1 to 32 min, was not important.
Chlorine was effective at 0. 27-0. 30 mg/liter, with time an important con-
sideration. These two gases did not affect E. coli in the same way.
In most research on lower organisms, there has been an attempt to
use ozone as a germicide or to understand the interactions of pollutants and
pathogens on the responses of higher plants. In few studies has the interest
been on the effects of ozone on the organisms themselves, except in the
studies of effects on algae.
11-152
-------
BIOLOGIC MONITORS
The use of biologic indicators as an early detection system for severe
air pollution episodes or for chronic air pollution problems is of interest to
many urban and industrial control officials. Plants served as air pollution
detection systems long before it was acknowledged a problem by industry or
government. Higher plants serve as useful detection tools, because they develop
characteristic symptoms from acute exposure, even though the symptoms are
not necessarily specific to cause. Cause and effect can be reliably ascertained,
when an air pollution source is identified and symptom patterns are identified
within given sensitive species.
Plants have been used effectively in field surveys to determine the
extent and magnitude of pollution problems and in bioassay techniques in
conjunction with field surveys. Most general review articles (Table 11-1)
treat, to some extent, the use of plants as indicators of air pollution.
585
Went covered plant sensitivities to pollutants and the use of plants as
indicators. He stressed the photochemical oxidants and recommended
209
charcoal filtration for greenhouse use. Heck presented a detailed
discussion and review of plants as indicators in field surveys and in the
222
bioassay of photochemical problems. Heggestad and Darley reviewed
plants as indicators of ozone and PAN and recommended pinto bean as the
best indicator of both oxidants. They also suggested three variably resistant
tobacco cultivars for use in monitoring the severity of ozone episodes.
It may be of value to differentiate the indicating and monitoring uses
of plants. Most reported work has used the indicator concept, with plant
injury (symptoms) as indicative of a problem. Monitoring implies some
degree of reliability. Several studies have attempted to use plant response
11-153
-------
as a monitor of pol lution concentrations or doses, with variable but uncertain
success. Plants could also be considered monitors if they gave a reliable
index of the biologic effects on biologic systems of concern to man (crops,
forests, animals, and man himself). The latter has not been seriously
discussed.
This section is divided into reviews of plants in field surveys and
plants as a bioassay technique and a brief discussion of the possible value
of biologic indicators.
Field Surveys
Field surveys have played a significant role in the assessment of air
pollution problems. Basic techniques were developed in surveys around point
sources of sulfur dioxide and fluoride. Similar techniques have been
developed regarding photochemical pollutants, starting with the early report
369
by Middleton et al.
~
Treshow has developed the thesis that foliar injury is a useful
criterion in the identification and analyses of air pollution effects on vege-
tation and presented some basic concepts for use in field evaluation.
482
Sharma and Butler found that white clover in a highly polluted
area (Nashville, Tenn. ) had a lower stomatal frequency, a higher trichome
frequency, and a greater trichome length than the same species growing in
an area of lower pollution. They suggested oxidants as one of the pollutant
stressors. It is possible that pollutant stress (among other things) is
causing selective pressures that favor these changes; thus, a separate race
may be evolving. This type of work needs further evaluation and exploration.
Most researchers have felt that biochemical changes in plant tissues
are associated .with so many normal growth and stress phenomena that they
* 11-154
-------
272
would have no relevance in field evaluations of air pollution effects. Keller
has associated changes in peroxidase activity-with different pollution stresses
(flouride and oxidants) in apricot and -white ash growing in areas of high pol-
lution, as opposed to those of low pollution. This study suffers from lack
of pollution monitoring (although leaves were analyzed for flouride) and con-
sideration of other stress factors. This is the same type of criticism that
164
has long been made of lichen studies in industrialized areas. Lichens
may respond to the photochemical complex, although such work has not been
reported. The larger question of the value of these studies persists. If, in
fact, changes in some biochemical entity could be clearly associated with one
or more pollutant and if this could be separated from other stresses, what
would it tell an interested party? Can it be related to adverse yield,
quality, or genetic changes? These approaches to understanding air pollution
effects through field surveys appear to be of doubtful value and must rely on
statistical methodology involving many variables.
A technique that offers greater potential is the use of remote sensing
of injury to vegetation. This technique was first tried with ponderosa pine as
586 587 298
the species of concern. Wert^t aL and Larsh^t al. found that
injury to ponderosa pine in the San Bernardino Mountains was severe enough
for the technique to have real potential. They were able to identify the severity
of diseased areas through color photography -with a high degree of correlation
with ground plots. In severely affected areas where air pollution is the
principal stressor, this approach offers a rapid and inexpensive technique
for surveying large tracts. It is not yet possible to use remote sensing to
identify pollutant stress amid a variety of other stressors. However, as
these techniques are improved, they should be applied to air pollution problems.
11-155
-------
Early field surveys depended on identification of a syndrome of responses
that included symptoms on both native and cultivated plant species. Middleton
366
and Paulus directed the first large-scale survey to determine the extent
and severity of photochemical oxidant effects in California on crops of agronomic
importance. They delineated four categories of crops (field, flower, fruit,
and vegetable) and one of weeds. This was the most extensive survey of
oxidant effects until the late 1960's. The information was later used as a
basis for subjective estimates of economic losses. This type of visual
assessment of foliar injury has been attempted in many states and has been
purposefully developed in some for use in economic estimates of damage to
vegetation.
Plant Bioassay of Oxidant Effects
During the 1950's, when the phytotoxic components of the photochemical
oxidant complex were not known, plants were used extensively as a bioassay
183, 209, 238,406,408,
of many simulated reaction mixtures to indicate toxicity.
496
Plants were also used to help in identifying specific components of
496
photochemical reaction products, such as PAN and its analogues.
This bioassay technique was also used to determine the phytotoxicity
of the ambient photochemical complex and to attempt to standardize plants,
so that oxidant concentrations could be determined from severity of injury.
Two such studies were initiated at about the same time in the Los Angeles
368
basin. Middleton ejt aL established five stations where young pinto bean
plants, grown under uniform conditions, were set out daily and foliar injury
intensity was compared with results from oxidant instruments. Results
were recorded as the percentage of days showing plant injury and the average
injury index per day per station. There was a relationship between injury
11-156
-------
and oxidant values, but the correlations were not significant and the
association was obscure. The most detailed study was carried out over a
407
period of about 4 years with annual bluegrass. The plants
268
were grown under standardized conditions, and injury development was
37
concisely defined. The plants were transported daily to locations around
Los Angeles County, California. They were exposed for 24 h and returned
for a control posttreatment period before injury assessment. The injured
leaf areas were measured and correlated with the severity of oxidant episodes.
The procedures were time-consuming, and the results were poorly cor-
related with oxidant concentrations. Thus, this procedure was discontinued
as automatic instrumentation became available.
The bioassay technique was developed to reduce the uncertainties
associated with the use of native vegetation or cultivated crops. Plants can
be started under controlled conditions and exposed under standardized con-
ditions. Species and cultivars can be selected for oxidant sensitivity and
symptom characteristics. The two studies just noted were the most closely
controlled. Similar work has not been repeated. However, many investi-
gators have grown plants under known cultural conditions and then transplanted
them to field sites where they received special care. These plants can then
be read for foliar symptoms throughout a given period, and the symptoms
related to oxidant concentrations. The lack of apparent correlation in the
two early studies could be due to the lack of specificity for the monitored
oxidants, the presence of different concentrations of interacting oxidants at
different times, or variations in cultural conditions between exposure times.
50
Brennan et al_. , using petunia, found a better correlation with
atmospheric aldehydes than with total oxidants. This appears spurious,
11-157
-------
because researchers do not regard aldehydes themselves as important
324
atmospheric phytotoxicants. Macdowal et al_. were able to correlate
tobacco injury with oxidant concentrations by considering ozone flux into
plant leaves. They then predicted fleck attacks with fair consistency on
the basis of meteorologic considerations. Several investigators have used
acknowledged plant sensitivity and emphasized the importance of accurate
84 123
monitoring for pollutants and meteorologic factors. These aspects
must concern any investigator who is seriously considering a plant monitoring
26
system. Berry developed clonal white pine material for use with specific
421
atmospheric pollutants. Oshima has recommended pinto bean as a
reliable monitor of oxidant intensity with a subjective injury evaluation (0-5)
that has been standardized against colored photographs. This is not as
sensitive as a percentage separation, but is no doubt easier for an untrained
observer to use. He did show good correlation between weekly oxidant
concentrations and plant response. This a relatively simple system, but
the monitoring plant is not as sensitive to low concentrations of oxidant
of oxidant as is Bel W tobacco.
3
The most extensively used monitoring system for photochemical oxidants
224
has used the ultrasensitive Bel W tobacco. The technique was first developed
213,220 3
by Heck and associates. The response of this tobacco variety was
used to determine the distribution, frequency of occurrence, and approximate
average concentrations of photochemical oxidants in and around Cincinnati,
Ohio, over four growing seasons. Monitoring sites were set up at various
distances from Cincinnati, up to 75 miles (120 km) due east. Injury responses
from this monitoring network showed that the average effective concentration
of photochemical oxidants was as high in rural Ohio as in Cincinnati. Although
11-158
-------
oxidant concentrations did not correlate well with plant injury on a weekly
basis, the seasonal ratio of injury to oxidants was similar over a 3-year
period. It was suggested that all areas east of the Mississippi have suf-
ficient photochemical oxidants to cause injury to sensitive plants at some
stage of their development. This monitoring system has since been used
as part of a regional study to determine the importance of oxidant pollutants
262
with respect to sensitive crops in the northeastern United States, and
176
similar systems have been used as oxidant indicators in South Dakota,
285 18
Germany, the United Kingdom, and other locations--including North
Carolina, Washington State, and Arizona. This type of monitoring system
was designed to provide communities with estimates of the frequency of
occurrence of phytotoxic concentrations of oxidants, of the relative severity
of each episode, and of the regional distribution of oxidant pollutants. The
system will not give a reliable estimate of oxidant concentrations. Thus,
it is an indicator of oxidant phytotoxicity, instead of a monitor for oxidant
concentrations.
96
Craker et a_l. used Bel W tobacco as a relatively simple monitoring
3
device whereby interested citizens in a community could develop some idea
of the biologic severity of oxidant pollution in their community. There are
problems with their study, but the concept is useful and might alert a com-
munity to potential pollution problems.
Several investigators have used systems ranging in complexity from
578
simple antioxidant-impregnated cloth covers to fairly elaborate filtered
145,204, 228, 237
and unfiltered chambers to determine the effects of ambient
oxidants on sensitive indicator (monitoring) plants. Bel W tobacco was
3
used in all these tests. Such tests can be used to determine growth and yield
reductions, as well as to identify possible problems.
11-159
-------
Discussion
Many investigators have discussed the use of biologic indicators as
early detection systems for air pollution problems. Some have viewed the
possibility of a nationwide monitoring system for air pollutants and other
environmental contaminants. Others have felt that the increased collection
of chemical data at many sites obviates biologic indicators or monitors.
However, the chemical and meteorologic data do not yet give a clear picture
of the biotoxicity of air pollution episodes. Thus, agencies should give
serious consideration to the development of national networks. If such
interest becomes widespread, it should be possible to correlate the biologic
response of the monitors with the response of important economic species,
ornamental species, or some human health measures. Without the ability
to correlate these factors, bioindicators are merely another index of pollution
that carries no rational value. Without the use of the bioindicator, we are
back to a direct assessment of the effects of a given pollution episode on
the biologic organisms of interest to man.
ECONOMIC ASSESSMENT
This section will bring into focus our present understanding of the
211
economic effects of oxidant air pollution on vegetation. Heck and Brandt
presented in depth the problems inherent in making an economic evaluation
of the response of pla.nts to air pollutants, including ozone and other oxidants.
They used the distinction between injury and damage that was proposed by
41
German workers. Injury is defined as any identifiable and measurable
response of a plant to air pollution; damage is any measurable adverse
effect on the desired or intended use of the plant. Thus, before an effect
11-160
-------
on a plant can be evaluated in terms of economics, the plant must have
been altered either quantitatively or qualitatively in such a way as to reduce
its use value. In this context, visible symptoms or transient changes in
physiologic responses may not result in an economic loss. Thus, leaf necrosis
in soybean is injury; to be classified as damage, the injury must affect yield.
In the same way, a severe oxidant episode that bronzes the leaves of romaine
lettuce may not affect biomass, but will affect use and may result in complete
economic loss. Ornamental plants, whose major use value depends on
appearance, may be both injured and damaged.
23
Emergence tip burn of white pine and other physiogenic diseases of
white pine associated with air pollution occur throughout the natural range of
the species. Insular stands containing ponderosa pine are frequently injured
in the Southwest. The significance of these physiogenic diseases is not
understood because they affect only sensitive genotypes. The disease occurs
randomly in the forest, and its most obvious effect is the slow selection
and gradual elimination of genotypes that may have otherwise superior
silvicultural characteristics. This could be a serious loss to future tree
improvement efforts and may be occurring in other forest species. Economic
considerations have not been addressed in any reasonable way.
Early work with sulfur dioxide showed a linear relationship between
visible injury and reduction in yield for many crop species. The assessment
•was made that no reduction in yield would be found unless visible injury were
noted. Definitive research with ozone, other oxidants, or mixtures of these
pollutants -with other gases has not been done. Thus, we do not know
whether such relationships between visible injury and yield hold for the
oxidants, but data in Table 11-3 suggest that for acute exposures there may
11-161
-------
be good correlations between injury and yield reductions. Many researchers
have hypothesized that the oxidants may have an effect on plants that will
produce a yield reduction with little or no visible injury. Such studies need
to be designed in a more definitive manner before it is concluded that yield
reductions without visible symptoms are clearly acceptable. Projections of
19, 370
yield losses have made use of some of the data reported earlier.
419,4ZO
Oshima has developed a methodology for evaluating and
reporting economic crop losses that involves continuous air monitoring,
chamber exposures, and monitoring plant species. He has attempted to weld
these into a comprehensive method of determining yield reductions. He
has reported yield reductions for some species, but has not fully clarified
the procedure. He presented no economic values in either report. This
type of approach needs to be considered further.
540,
The reports of specific effects related to sensitive growth stages,
542, 543, 545
especially to reproductive growth stages in which the pollutant
62, 63, 155
may be affecting reproductive structures and not leaf tissues,
are probably of greater importance to the understanding of reduced yield
without visible symptoms than to the potential of a debilitating effect caused
by chronic continuous exposure to ozone or other oxidants. These economic
considerations have not been addressed.
Any attempt to assess oxidant damage to agricultural crops requires
294
judgment by a competent investigator. Landau and Brandt believe that
the success of crop surveys is directly related to the number of subjective
decisions required in data collection. The first surveys were conducted in
366, 369
California and were used, with a general survey of conditions on the
East Coast, to develop some of the early economic estimates of $8-10 million
11-162
-------
in California and $18 million on the East Coast. These estimates were raised
to $500 million on the basis of increased awareness of pollution effects and
increased recognition of additional sensitive species. However, all early
estimates -were subjective, with no substantial backup data.
Since 1969, a number of states have instituted an intensive training
program for county agricultural agents and made detailed reports of crop
163, 292,295,370,399,429
injury and damage (Table 11-27). The first such
295
report came from Pennsylvania in 1969 and gave an estimate of a $9. 6
million loss to agronomic commodities from oxidant pollutants. This survey
included direct and some indirect cost. Similar surveys have been conducted
399 163,429 370
in New England, New Jersey, California, and Michigan (no
report is currently available). These surveys considered yield reductions
on the basis of injury and made no direct growth or yield assessments,
432
although subjective estimates of damage were obtained. Pell and Brennan
presented a well-developed thesis on the rationale for the difference in
estimated losses to agriculture in New Jersey between 1971 and 1972. They
discussed this in relation to the overall problem of assessing agricultural
losses.
19
A survey \vas initiated in 1969 by Stanford Research Institute
(SRI) to develop an empirical model for assessing damage to vegetation.
This program made use of laboratory and field data from controlles
exposures on various crops and chemical data from simulated reaction
chambers, so estimates of ozone and other oxidants could be made on the
basis of concentrations of primary pollutants. Hydrocarbon was chosen
as the basic pollutant from which to develop the model for prediction of
expected oxidant values and, therefore, effects on various crops. From
11-163
-------
r-
CN
I
cd
H
•rH
C
co
CO
Sf
4-1
CO
W
a
§
o
a
w
CD
CJ
C
CD
JH
0)
S-l
CD
«
CO
-P
S3
CD
£
o
O
o
4-1 O
co o
o •>
O i-H
-c/v
st approximation for
mercial crops (SRI) 19
SH E
•H O
r>H U
o
o
0
•K
m
CD
ised SRI report to include ornamentals 19
>
CD
CJ
o
o
•*
•t
rH
CM
rH
ised SRI report 19
s not include ornamentals or 370
irect costs
> CD 73
CD O C
« P -H
o o
o o
c^ in
•S M
CO t-
CO i-i
ised SRI report 19
survey ; includes indirect costs 295
> «
0 CO
OJ Pk
0 0
o o
CO CD
•» ••*
CD CD
CO
o>
CM
0
>
O
ft
CO
CO
CO
>>
CD
>
!H
3
CQ
•
CO
CU
O
CD
J. survey of a limited number 163
crops, based on visible injury
J. as above 429
is. survey; primarily crops 399
1 ornamentals
' W -0 i
• =H . CO C ,
Jz; 0 :s S to
o o o
CD CD o
CD rH
**
I-t
cd
CU
CO
CD
CQ
0
•P
CO
•P
03
73
0
•P
CO O
CD t^
cr> cn
rH rH
CO
•H
C
SH
O
CO
O
CO O5
CD CD
Ol CO
rH r-H
CO
•rH
CO
C
C
0
o
r~
CD
(N
I>
CD
CD
CQ
r4
CD
CD
rH
t>
CD
73
C
CO
|H
W)
C
w
z
CD
C
o
•rl
r-l
O
•H
rH
•H
^3
•H
4-1
CX
0)
a
03
CO
cfl
rH
a.
c
•rl
CO
0)
0
a)
o
cu
a)
X
4-1
O
o
rH
O
C1J
e
CO
4.)
O
0)
rH
<4H
0)
S-l
c
o
•H
4-1
cd
•rl
rl •
Cd CO
> rl
CO
UH ,
CU !-i
S
w o
11-164
-------
the oxidant value, injury and damage for specific crops were calculated for
over 100 statistical reporting areas in the United States. The report used
many subjective assumptions and -was related primarily to visible injury
symptoms. The results were preliminary, and the approach had many
deficiencies; but similar approaches should be contemplated in the develop-
ment of damage functions that will give some reliable estimates of economic
losses. On the basis of the SRI model, the 1969 estimated loss to vegetation
from oxidants in the United States was approximately $125 million. Con-
sidering the increase in crop values and assuming that oxidant concentrations
have not been significantly reduced during the last few years, the loss in
1974 from oxidants could approach $300 million, on the basis of the SRI
study.
A summary of estimates derived from various surveys and assessment
techniques is shown in Table 11-27. These values are suggestive at best.
As with all values developed for agricultural losses, these have been directed
at losses to the producer—not to the consumer.
Whereas a reduction in production may actually increase the aggregate
farm income and produce serious income distribution problems, the consequent
reduction in marketable surplus would cause a significant rise in the cost to
consumers, because of the inelastic consumer demand for most agricultural
crops. Therefore, at the consumer level, losses based on farm prices are
not appropriate and are likely to be conservative. Because of percentage
markups and fixed •wholesale and retail marketing costs, the cost to the
consumer of agricultural losses could be twice as great as that observed
at the farm level--i. e. , a $300 million loss at the farm level in 1974 could
represent a $600 million loss to the consumer.
11-165
-------
SUMMARY
Oxidant injury to vegetation was first identified in 1944 in the Los
Angeles basin. Our understanding of oxidant effects and of the widespread
nature of their occurrence has increased steadily since then. Although the
major phytotoxic components of the oxidant (photochemical) complex are ozone
and peroxyacetylnitrate (PAN), indirect data support the contention that other
phytotoxicants are present in the photochemical complex. Ozone is considered
the most important phytotoxic component and was first identified as the specific
cause of weather fleck on tobacco and stipple on grape. PAN is associated
with the undersurface glazing and bronzing associated with many of the vegetable
crops.
Plant response to oxidants (including ozone and PAN) is often divided
into visible and subtle effects. Visible effects are identifiable pigmented,
chlorotic, and necrotic foliar patterns resulting from major physiologic
disturbances. Subtle effects produce no visible injury, but include metabolic
disturbances and may be measured on the basis of growth and long-term
biochemical changes. These effects may influence plant populations and
communities and could have an adverse influence on ecosystems. Visible
injury may be acute or chronic. Acute injury breaks down the cell membrane
and causes cell death, with leaf necrotic patterns that may be characteristic
for a given oxidant, but can be confused with other stress factors. Classic
injury from ozone is the upper-surface fleck on tobacco and the stipple of
grape. Many plants show an upper-surface bleach with no lower-surface
injury. Bifacial necrotic spotting is common and may appear flecklike.
Classic injury from PAN appears as a glaze followed by bronzing of the
lower leaf surface in many plants. Complete collapse of leaf tissue can
11-166
-------
occur, if concentrations are high. Chronic injury is associated with
disruption of normal cellular activity followed by chlorosis or other color
or pigment changes that may lead to cell death. Chronic injury patterns
are generally not characteristic and may be confused with symptoms caused
by biotic diseases, insects, nutritional disorders, or other environmental
stresses. Early leaf senescence and abscission may result from chronic
exposure.
Leaf stomata are the principal entry sites for ozone and PAN.
Stomata, when closed by any of a number of factors, will protect plants.
Ozone and PAN may interfere with various oxidative reactions in plant cells.
Membrane sulfhydryl groups and unsaturated lipid components may be primary
targets of oxidants. Physiologic leaf age is an important consideration in
the response of the leaf to oxidants. Young leaf tissue is more sensitive
to PAN, whereas newly expanding and maturing tissue is most sensitive to
ozone. Light is required before plant tissue will respond to PAN, but not
to ozone. Oxidants affect such physiologic processes as photosynthesis,
respiration, transpiration, stomatal opening, metabolic pools, biochemical
pathways, and enzyme systems. The acute response of plants to ozone and
PAN may result from a saturation of sensitive cell sites and a disruption
of normal cellular repair mechanisms. Chronic injury probably results
from secondary reactions involving membrane injury.
There is evidence that ozone is a radiomimetic gas. Ozone affects
pollen germination in some species and thus may directly affect yield. A study
with Arabidopsis thaliana suggested no mutagenic effects from ozone on this
plant over five generations.
11-167
-------
Ambient-oxidant studies in filtered versus nonfiltered field chambers
have reported up to 50% reduction in citrus yield (orange and lemon), a 10 -
15% reduction in grape yield in first year and 50 - 60% reductions over the
following 2 years, and a 5 - 29% reduction in yield of cotton lint and seed in
California. Losses of 50% in some sensitive potato, tobacco, and soybean
cultivars have been reported from the eastern United States. It is apparent
that ambient oxidants do reduce yields of many sensitive plant cultivars.
Growth reductions associated with acute exposure to ozone are often associated
with injury; sometimes the correlations are high. Even multiple exposures
and sometimes chronic exposures have shown fair to good correlation between
injury and growth (biomass) reductions. The greater reductions in root
growth than in top growth reported in several species are related to solute
transport and may be fairly common under some conditions. Ozone affects
nodule number, but not nodule size or efficiency in clover, soybean, and
pinto bean. This causes a reduction in nitrogen fixation associated with legumes
and, if widespread, could have a major impact on plant communities and
affect fertilizer needs. The effect on nodulation is related to carbohydrate
supply. Yield reductions with little injury after chronic exposure are known
for several crops. Severe injury in tomato was required before a yield
reduction -was found. Chronic exposures to ozone at 0. 05-0. 15 ppm for 4-6
h/day will produce yield reductions in soybean and corn grown under field
conditions. The threshold appears to be 0. 05-0. 10 ppm for some sensitive
cultivars and is well within values monitored in the eastern United States.
Growth or flowering effects, at chronic exposures to ozone at 0. 05-0. 15
ppm for 2-24 h/day are reported for carnation, geranium, radish, and pinto
bean grown in greenhouse chambers.
11-168
-------
Plant sensitivity to ozone, PAN, and other oxidants is conditioned
by many factors. Genetic diversity between species and between cultivars
•within a species is well documented. The mechanism of genetic resistance
is known for only one onion cultivar and is related to the effect of ozone
on stomatal closure. Variants within a natural species are well known for
several pine species, including white, loblolly, and ponderosa. Plant
sensitivity to oxidants can be changed by both climatic and edaphic factors.
A change in environmental conditions will initiate a change in sensitivity at
once, but it will be 3-5 days before the response of the plant is completely
changed. Plants generally are more sensitive when grown under short
photoperiods, medium light conditions, medium temperature, high humidity,
and high soil moisture. Injury to PAN may increase with increasing light
intensity. Conditions during exposure and growth affect the response of
plants to oxidants in similar ways. However, plants exposed to ozone are
more sensitive to increasing light intensity and, in some cases, to decreasing
temperature during the exposure period. In general, growth factors that
tend to cause a physiologic hardening of plant tissue make the plants more
tolerant to ozone. At the time of exposure, factors that increase water
stress tend to make plants more tolerant to ozone. Soil moisture is probably
the most important environmental factor that affects response during the
normal growing season.
Plants respond in different ways to pollutant mixtures; less than
additive, additive, and greater than additive effects have been reported.
Mixtures of ozone with sulfur dioxide and of nitrogen dioxide with sulfur
dioxide can cause oxidant-like symptoms in some sensitive plants. Mixtures
can cause effects below the threshold for either gas, although there is some
11-169
-------
disagreement on this in regard to ozone. Ratios of mixtures, intermittent
exposures, sequential exposures to pollutants, and predisposition by one
pollutant to the effects of a second pollutant may all be important in nature,
but little research has been done.
The response of some plants to oxidants is conditioned by the
presence or absence of biotic pathogens. Depending on the plant and the
pathogen, oxidants may cause more or less injury to a given species.
Pathogens may protect their host or make it more sensitive. The pathogens
themselves may be injured or may be protected by the host plant. This
subject is just starting to be understood.
Oxidant injury to ponderosa pine predisposes the trees to later
invasion by pine bark beetles. Ozone and ozone-sulfur dioxide mixtures
may decrease the population of soybean nematodes. Both greater and smaller
effects have been noted -when herbicides have been used in the presence of
high oxidant concentrations.
The two most critical factors in terms of air quality standards are
duration of exposure and concentration. These two factors determine the
exposure dose for a plant. In determining the response of vegetation, con-
centration is more important than time. A given dose presented to a plant
in a short period has a greater effect than the same dose applied over a longer
period. This suggests a threshold effect for plant populations and is probably
related to the repair mechanisms inherent in biologic systems. Sufficient
information is not available from long-term chronic studies, but a threshold
between 0. 05 and 0. 10 ppm is probable for ozone (oxidant). For acute effects,
an overall threshold concentration with respect to time can be determined
from Figure 11-6 and Table ll-24a. For pinto bean (Table 11-22), this threshold
11-170
-------
for injury is about 0.03 ppm for 8 h and about O.lOppm for 1 h. This
suggests that oxidant standards may be needed for periods up to 8 h.
Vegetation can act as a major sink for oxidants over time, but has a
relatively minor effect on oxidant concentrations during episodes of high air
pollution, is more effective at some seasons or under some cultural and
management practices than others, and should not be considered an important
contributor to short-term reductions in oxidant or ozone concentrations.
Plant protection from air pollution stress has involved three types of
programs. Several researchers are including pollutant stress in standard
breeding programs -with the aim of developing resistant cultivars. Our present
concepts of pollution effects suggest that the gene pool of all species is large
enough to permit the development of more tolerant cultivars. Natural selection
•will slowly do this for native vegetation. If pollution concentrations go no
higher, this should be an effective protection device. Interim measures
involve the use of chemical sprays. Such sprays are not yet economically
feasible, but several do give adequate protection against oxidants. Fungicides,
such as Benomyl, may serve a dual function. Cultural and land use practices
may also play important roles, especially on a short-term basis.
Little research on the effects of oxidants on nonvascular green plants
and microorganisms has been reported. Lichens and mosses are responsive
to acid gases, but there is no definite evidence that they respond to oxidants.
Ferns may be especially sensitive, but their injury response is much different
from that of higher plants. Growth and sporulation of fungi on surfaces
are usually, but not always, affected. Ozone does not penetrate the leaf
tissue or the colony and thus does not cause death of colonies. O^one from
11-171
-------
0. 1 to several milligrams per liter of solution is required to kill many
microorganisms in liquid media. Most work with microorganisms has
been done to study the effectiveness of ozone as a biocide i-n the storage of
vegetation or treatment of water or sewage supplies.
Plants have been used as biologic indicators of oxidant pollutants
for many years. Attempts have been made to use plants as monitors, but
too many unknown variables are involved. Plants may be capable of
monitoring the total biologic potential for adverse effects, but no research
has been developed along these lines.
Losses based on farm prices are not appropriate at the consumer
level and are likely to be conservative. Because of percentage markups and
fixed wholesale and retail marketing costs, the cost to the consumer from
agricultural losses to oxidant pollutants could be as much as $600 million per
year.
11-172
-------
RECOMMENDATIONS
These recommendations are not listed in a priority order, but
many could be followed in parallel or simultaneously. In general, the recom-
219
mendations presented by Heck et_ al. are still germane to research
needs in the subject of oxidant pollutants.
A few definitive experimental designs are needed to further our
knowledge of acute dose-response information on ozone. Much of this type
of information is still needed for PAN and its analogues. All experimental
designs should incorporate dose response.
Studies to develop dose-response curves for chronic exposures of
crop and native species over growing seasons and under field conditions
are needed for ozone, PAN, and other oxidants.
Research should be continued with filtered and nonfiltered field
chambers to study effects of ambient oxidants on important agronomic,
horticultural, and native species. We know that there is a problem, but
its significance and magnitude are matters of conjecture.
There is a critical need to understand the interaction of multiple pol-
lutants on individual plant species and ecosystems. Multiple-pollutant effects
are generally important, but little is known of their effects on most plants.
Variable concentrations, ratios of pollutants, and age of plants all affect
response.
Models should be developed to understand the relative importance of
other variables as they affect plant dose response. These include, but are
not limited to, climatic, edaphic, biotic, and genetic factors. Considerable
11-173
-------
information is available, but there are many gaps, and no comprehensive
programs are in progress to determine how these factors act and interact
to affect a plant's response.
The mechanism of response and the biochemical systems affected
are not understood. Although plant membranes are considered the primary
sites of action for the oxidant pollutants, there is no definitive work on
this. An understanding of these responses would be supportive of breeding
and spray protective programs.
Both breeding and spray protective programs need to be
developed, so that better-yielding and better-quality cultivars will be pro-
tected against oxidant pollutants.
Some effort is needed to explore the feasibility of using plants to
monitor the overall biologic activity (or biomass reductions) caused by
photochemical oxidants in specific air basins or regions. The response
of sensitive plants should be correlated with the response of plants of
economic and aesthetic importance.
Additional monitoring of multiple pollutants is needed in rural areas.
Whenever possible, measures that vary on a continuous scale (e.g. ,
biomass) should be used with subjective estimates of injury (e. g. , indexes
of visible injury).
11-174
-------
APPENDIX TO CHAPTER 11
INDEX OF PLANT NAMES AND REFERENCE NUMBERSa
ALFALFA (Medicago sativa, L.) — 79,233,245,331,447,487,538,547,548
APPLE (Malus, sp.) — 371,489
APRICOT (Prunus armeniaca, L.) — 272
Arabidopsis thaliana, L, Britt — 57
ARBORVITAE (Thuja orientalis, L.)
ASH, white (Fraxinus americana, L.) — 264,272
ASPEN, quaking (Populus tremuloides, Michx.) — 194
AVOCADO (Persea, sp.) — 512
AZALEA (Rhododendron, sp.) — 386
BARLEY (Hordeum vulgare, L.) — 22a,202,348,474,477
BEAN (Phaseolus vulgaris, L.) -- 7,22a,69-71,98,99,110,111,133,134,137,
138,141,143,153,170,222,244,247,261,277-
279,297,319,327,328,334,341,343,344,345,
348,349,421,424,434,452,457,458,479,495,
496,506,517,551,552,556,573,596
BEAN, lima (P. limensis. Macf.) — 547
BEET, table (Beta vulgaris, L.)— 60,369,412
BEGONIA, Christmas (Begonia socotrana, Hook, f.)
BEGONIA (Begonia, sp.) -- 214,297
BIRCH, white (Betula alba, L.) — 563
BROCCOLI (Brassica oleracea, L.) — 214,547
CABBAGE (B. oleracea, L.) — 344,547
CARNATION (Dianthus caryophyllus, L.) — 156,157
CEDAR (Juniperus, sp.) — 373,507
Chenopodium album, L. — 194
11-175
-------
APPENDIX TO CHAPTER 11 (Cont.)
INDEX OF PLANT NAMES AND REFERENCE NUMBERS'2
Chenopodium fremontii, L. — 194
CELERY (Apium graveolens, Linn) — 170
CELOSEA (Celosea, sp.) — 5
CHARD, swiss (Beta vulgaris. L.) — 369,560
CHRYSANTHEMUM (Chrysanthemum, sp.) — 128,297,329,330,593
CITRUS (Citrus, sp.) — 520
CLOVER, red (Trifolium pratense, L.) 297
CLOVER, white (T. repens, L.) — 286,482
CLOVER, white sweet (Melilotus alba, Desr.) — 482
COLEUS (Coleus blumei, Benth.)
CORN (Zea mays, L.) — 63,206,240-242,266,297,397,418,509,570
COTTON (Gossypium hirsutum, L.) — 53,201,458,531
CRESS (Lepidium sativum, L.) — 100
CUCUMBER (Cucumis sativus, L.) - 416
Descurainia, sp. — 194
DUCKWEED (Lemna minor, L.) — 158
FIR, balsam (Abies balsamea (L.), Mill.)
FIR, Douglas (Pseudotsuga menziesii (Mirb.) Franco.)
FIR, white (Abies concolor (Gord. & Clend.) Lindl.)
GERANIUM (Geranium, sp.) — 156,336,337
GERANIUM, wild (£. fremontii L. Torr. ex A. Gray) — 194
GLADIOLUS (Gladiolus, sp.) — 329,330
GRAPE (Vitis, sp.) — 273,276,461,518,519,522
11-176
-------
APPENDIX TO CHAPTER 11 (Cont.)
INDEX OF PLANT NAMES AND REFERENCE NUMBERS
GRAPEFRUIT (Citrus, sp.) — 170
GRASS, annual blue (Poa annua, L.) — 268,384,407
GRASS, bent (Agrostis palustris, Huds.)
GRASS, Bermuda (Cynodon dactylon, L.)
GRASS, brome (Bromus tectorum) — 441
GRASS, brome (B. inermis, Leyss) — 297
GRASS, Kentucky blue (Poa pratensis, L.)
GRASS, orchard (Dactylis glomerata, L.)
GRASS, perennial rye (Lolium perenne, L.)
GRASS, red fescue (Festuca rubra, L.)
GRASS, zoysia (Zoysia japonica, Steud.)
GUM, sweet (Liquidambar styraciflua) — 563
HEMLOCK, Eastern (Tsuga canadensis (L.), Carr.)
HOLLY, English (Ilex, sp.)
IMPATIENS (Impatiens sullanii, Hook) — 5
LARCH, European (Larix decidua, Mill.)
LARCH, Japanese (L. leptolepis (Sieb & Fucc.) Gord.)
LEMON (Citrus, sp.) — 92,129,192,521
Lepidium virginicum, L. — 47,194
LETTUCE (Lactuca sativa, L.) — 170,369,490,510
LOCUST, honey (Gleditsia triacanthos, L.) — 127
Madia glomerata — 194
MAPLE, red (Acer rubrum, L.) — 563,564
11-177
-------
APPENDIX TO CHAPTER 11 (Cont.)
INDEX TO PLANT NAMES AND REFERENCE NUMBERS
MAPLE, silver (A. saccharinum, L.) -- 127,264
MAPLE, sugar (A., saccharuim, Marsh) — 264,563
MARIGOLD (Tagetes patula, L.) — 5
MORNING GLORY (Ipomoea purpurea, Roth ) — 400
MUSTARD (Brassica pekinensis)
OAK, red (Quercus rubra, L.) — 127
OAK, swamp (Q. palustris, DuRoi) — 127
OAK, white (Q. alba) — 127,563
OATS (Arena sativa, L.) -- 62,64,186,195,297,477
ONION (Allium cepa", L.) -- 141,142,416
ORANGE (Citrus sinensis. Osbeck) — 92,192,521
PEACH (Prunus persica, Sieb. & Zucc.) — 463,490
PEA, cream (Pisum sativum, L.) — 174
PEANUT (Arachis hypogaea, L.) — 13,203
PERIWINKLE (Vinca minor, L.) -- 297
PETUNIA (Petunia hybrida, Vilm.) — 50,91,93,128,170,190,191,193,310,
496,506,510,560,593
PINE, Austrian (Pinus nigra, Arnold)
PINE, eastern white (P. strobus, L.) — 16,23,26,28,40,82,86,113,124-
126,248-250,313,315,590
PINE, jack (P. banksiana, Lamb.)
PINE, Jeffrey (P. jeffreyi) — 373,507
PINE, loblolly (JP. taeda, L.) — 27,582
PINE, pitch (P. rigida. Mill.)
PINE, ponderosa (P. ponderosa, Laws) — 77,108,149-151,298,372,374,375,
378-380,426,507,586,587
PINE, red (P. resinosa,Ait.) — 113
11-178
-------
APPENDIX TO CHAPTER 11 (Cont.)
INDEX OF PLANT NAMES AND REFERENCE NUMBERS
PINE, Scotch (P. sylvestris, L.) -- 122
PINE, shortleaf (P. echinata, Mill.) — 27
PINE, slash (P. caribaea, Morelet) — 27
PINE, sugar (P. lampertiana) — 373,507
PINE, Virginia (P. virginiana. Mill.) — 25,27,107
POINSETTIA (Poinsettia pulcherrima, Willd.) — 93,214,310,339,342
Polygonum aviculare, L. — 50,194
POPLAR, hybrid (Populas deltoides Earth, x P_._ trichocarpa (Torr. and Gray)
265,287,290
POPLAR, yellow (Liriodendron tulipifera) ~ 264
POTATO (Solanum tuberosum, L.) 42,49,221,247,310,346,416
RADISH (Raphanus sativus, L.) — 297,447,540,545,547
RYE (Secale cereale, L.) -- 477
SAFFLOWER (Carthamus tinctorius, L.)
SALVIA (Salvia splendens, Sello) — 5
SMARTWEED (Polygonum lapathlfolium) — 22a
SNAPDRAGON (Antirrhinum majus, L.)
SORGHUM (Sorghum vulgare, Pers.)
SOYBEAN (Glycine max, Merr.) — 34,105,171,201,205,253,271,358,450,458,
536,538,543,544,548,581
SPINACH (Spinacea oleracea, L.) — 72,174,297,369
SPINACH (Tetragonia expansa)
SPRUCE, black (Picea glauca var. densata Bailey)
SPRUCE, blue (P. pungens, Engelm.)
11-179
-------
APPENDIX TO CHAPTER 11 (Cont.)
INDEX OF PLANT NAMES AND REFERENCE NUMBERS
SPRUCE, Norway (P. abies (L.), Karst.)
SPRUCE, white (P. glauca CMoench,) Voss.)
SQUASH, summer (Curcurbita pepo, L.) — 297
STRAWBERRY (Fragaria, sp.) — 463,490
SULTANA (Impatiens sultani, Hook.)
SUNFLOWER (Helianthus annus, L.) — 411
SWEETGUM (Liquidambar styraciflua, L.) — 563
SYCAMORE (Platanus occideutalis, L.) — 264
TOBACCO (Nicotiana tabacum.L.) — 30,37,46,65,66,96,115-117,137,138,145,
155,198,204,222,224-226,228,237,243,247 ,
267,288,296,297,303,311,320,322-324,349,
353,355-357,359,360,385,424,440,443,446,
447,454,458,472,485-487,500-504,530,538,
547,548,557,575,577
TOBACCO (N. glutinosa, L.)
TOBACCO (N. rustica)
TOMATO (Lycopersicon esculentum, Mill.) — 75,76,177,240-242,289,297,335,
349,402,418,423,454,458,498,506,
510,547,560
TOMATO (L^ pimpinellifolium) — 177
VETCH, broad bean (Vicia faba, Linn.) — 261
VETCH, crown (Coronilla varia, L.)
WHEAT (Triticum duram, Desf.) — 199,200,297,477,481
References are in addition to those found in Table 11-24 for the same
plants. For complete references on a single species, check both the
Appendix and Table 11-24.
11-180
-------
REFERENCES
1. Abeles, A. I., and F. B. Abeles. Biochemical pathway of stress-induced
ethylene. Plant Physiol. 50:496-498, 1972.
2. Abeles, F. B., L. E. Craker, 1. E. Forrence, and G. R. Leather. Fate of
air pollutants: Removal of of ethylene, sulfur dioxide, and nitrogen
dioxide by soil. Science 173:914-916, 1971.
3- Adedipe, N. 0., and D. P. Ormrod. Hormoral regulation of ozone phytotox-
icity in Raphanus sativus. Z. Pflanzenphysiol. 68:254-258, 1972.
4. Adedipe, N. 0., and D. P. Ormrod. Ozone-induced growth suppression in
radish plants in relation to pre- and post-fumigation temperatufes.
Z. Pflanzenphysiol. 71:281-287, 1974.
5. Adedipe, N. 0., R. E. Barrett, and D. P. Ormrod. Phytotoxicity and growth
responses of ornamental bedding plants to ozone and sulfur dioxide.
J. Amer. Soc. Hort. Sci. 97:341-345, 1972.
6. Adedipe, N. 0., R. A. Fletcher, and D. P. Ormrod. Ozone lesions in rela-
tion to senescence of attached and detached leaves of tobacco.
Atmos. Environ. 7:357-361, 1973.
7. Adedipe, N. 0., G. Hofstra, and D. P. Ormrod. Effects of sulfur nutrition
on phytotoxicity and growth responses of bean plants to ozone. Can.
J. Bot. 50:1789-1793, 1972.
8. Adedipe, N. 0., H. Khatamian, and D. P. Ormord. Stomatal regulation of
ozone phytotoxicity in tomato. Z. Pflanzenphysiol. 68:323-328, 1973.
9. Anderson, L. E. , T.-C. L. Ng., and K-E. Y. Park. Inactivation of pea leaf
chloroplastic and cytoplasmic glucose 6-phosphate dehydrogenases by
light and dithiothreitol. Plant Physiol. 53:835-839, 1974.
11-181
-------
Deleti 10
11. Anderson, W. C., and 0. C. Taylor. Ozone induced carbon dioxide evolution
in tobacco callus cultures. Physiol. Plant. 28:419-423, 1973.
12. Glossary o£ air pollution terms and selected reference list. Phytopath.
News 8(8), 1974. (insert)
13, Applegate, H. G., and L. C. Durrant. Synergistic action of ozone-sulfur
dioxide on peanuts. Environ. Sci. Technol. 3:759-760, 1969.
14. Barnes, R. L. Effects of chronic exposure to ozone on suluble sugar and
ascorbic acid contents of pine seedlings. Can. J. Bot. 50:215-219,
1972.
15_ Barnes, R. L. Effects of chronic exposure to ozone on photosynthesis and
respiration of pines. Environ. Pollut. 3:133-138, 1972.
16. Barnes, R. L., and C. R. Berry. Seasonal changes in carbohydrates and
ascorbic acid of white pine and possible relation to tipburn sensi-
tivity. Forest Service Research Note SE-124, 1969. 4 pp. (UNVERIFIED)
Delete 17
18. Bell, J. N. B., and R. A. Cox. Atmospheric ozone and plant damage in the
United Kingdom. Environ. Pollut. 8:163-170, 1975.
19. Benedict, H. M., C. J. Miller, and R. E. Olson. Economic Impact of Air
Pollutants on Plants in the United States. Final Report. SRI
Project LSD-1056. Menlo Park, Calif.: Stanford Research Institute,
1971. 77 pp.
Delete 20
11-182
-------
21. Bennett, J. H. , and A. C. Hill. Interactions of air pollutants with cano-
pies of vegetation, pp. 273-306. In J. B. Mudd and T. T. Kozlowski,
Eds. Responses of Plants to Air Pollution. New York: Academic
Press, 1975. (UNVERIFIED)
22. Bennett, J. H., A. C. Hill, and D. M. Gates. A model for gaseous pollut-
ant sorption by leaves. J. Air Pollut. Control Assoc. 23:957-962,
1973.
22a. Bennett, J. P., H. M. Resh, and V. C. Runeckles. Apparent stimulations
of plant growth by air pollutants. Can. J. Bot. 52:35-42, 1974.
23. Berry, C. R. White Pine Emergence Tipburn, a Physiogenic Distrubance.
S. E. Forest Experiment Station Paper 130, 1961. (UNVERIFIED)
24. Berry, C. R. A plant fumigation chamber suitable for forestry needs.
Phytopathology 60:1613-1615, 1970.
25. Berry, C.' R/ Relative sensitivity of red, jack, and white pine seedlings to
ozone and sulfur dioxide. Phytopathology 61'.231-232, 1971.
26. Berry, C. R. The differential sensitivity of eastern white pine to three
types of air pollution. J. Can. Forest. Res. 3:543-547, 1973.
27. Berry, C. R. Age of pine seedlings with primary needles affects sensitiv-
ity to ozone and sulfur dioxide. Phytopathology 64:207-209, 1974.
28. Berry, C. R. , and H. E. Heggestad. Air pollution detectives, pp. 142-146.
In Yearbook of Agriculture 1968. Science for Better Living. Washington,
D. C.: U. S. Government Printing Office, 1968.
29, Berry, C. R., and L. A. Ripperton. Ozone, as possible cause of white pine
emergence tipburn. Phytopathology 53:552-557, 1963.
11-183
-------
30. Bertinuson, T. A., H. LeCoultre, and W. C. Waterman. The inhibitory effect
of zinc ethylene bisdithiocarbamate dust on weather fleck of Connecti-
cut shade-grown tobacco. Tobacco 152:22-24, 1961. (UNVERIFIED)
Delete 31
32. Blattny, C., and J. Break. Die Bedrohung der Futterpflanzen durch Smog
und Poa annua als Indikator dieser Schadquelle. Wiss. Z. Karl-Marx-
Univ. 11:111-113, 1962.
33. , Blum, U. North Carolina State University, Raleigh, Personal Communication.
,1976.
34. Blum, U., and D. T. Tingey. Effects of soil-ozone complex on root growth
and nodulation. Environ. Qual. (in press) (UNVERIFIED)
35. Bobrov, R. A. The effect of smog on the anatomy of oat leaves. Phytopath-
ology 42:588-563, 1952.
36. Bobrov, R. A. The anatomical effects of air pollution on plants, pp. 129-134.
In Proceedings of the Second National Air Pollution Symposium, Pasadena,
California, 1952. Los Angeles: National Air Pollution Symposium, 1952.
37. Bobrov, R. A, The leaf structure of Poa annua with observations on its Smog
sensitivity in Los Angeles County. Amer. J.~Bot. 42:467-474, 1955.
38. Bobrov, R. A. Cork formation in table beet leaves (Beta vulgaris) in respons
to smog, pp. 199-205. In Proceedings of the Third National Air Pollution
Symposium, Pasadena, California, 1955. Los Angeles: National Air Pollu-
tion Symposium, 1955.
Delete 39
40. Botkin, D. B., W. H, Smith, R. W. Carlson, and T. L. Smith. Effects of
ozone on white pine saplings: Variation in inhibition and recovery
of net photosynthesis. Environ. Pollut. 3:273-289, 1972.
11-184
-------
41. Brandt, C. S., and U. Holzel. Problems of the Recognition and Evaluation
of the Effects of Gaseous Air Impurities on Vegetation. Technical
Report A61-37. Cincinnati: U. S. Department of Health, Education,
and Welfare, 1961.
42. Brasher, E. P., D. J. Fieldhouse, and M. Sasser. Ozone injury in potato
variety trials. Plant Dis. Rep. 57:542-544, 1972.
Delete 43"
44. Brennan, E., and p.' M. Halisky. Response of turfgrass cultivars to Ozone and
sulfur dioxide in the atmosphere. Phytopathology 60:1544-1546, 1970.
45. Brennan, E., and I. A. Leone. The response of plants to sulfur dioxide or
ozone-polluted air supplied at varying flow rates. Phytopathology 58:
1661-1664, 1968.
46. Brennan, E., and I. A. Leone. Suppression of ozone toxicity symptoms in
virus-infected tobacco. Phytopathology 59:263-264, 1969.
47. Brennan, E., and I. A. Leone. The response of English holly selections
to ozone and sulfur dioxide. Holly Lett. 37:6-7, 1970.
48. Brennan, E., and I. A. Leone. Chrysanthemum response to sulfur dioxide and
ozone. Plant Dis. Rep. 56:85-87, 1972.
49. Brennan, E., I. A. Leone, and R. H. Daines. The importance of variety in
ozone plant damage. Plant Dis. Rep. 48:923-924, 1964.
50. Brennan, E. G. , I. A. Leone, and R. H. Daines. Atmospheric aldehydes related
to petunia leaf damage. Science 143:818-820, 1964.
51. Brennan, E., I. A. Leone, and R. H. Daines. Characterization of the plant
damage problem by air pollutants in New Jersey. Plant Dis. Rep. 51:
850-854, 1957.
11-185
-------
52. Brennan, E., I. A. Leone, and P4 M. Halisky. Response of forage legumes to
ozone fumigations. Phytopathology 59:1458-1459, 1969.
53. Brewer, R. P., and C. Ferry. Effects of air pollution on cotton in the San
Joaquin Valley. Calif. Agric. 28(6) '.6-7, 1974.
54. Brewer, R. P., P. B. Guillemet, and R, K. Creveling. Influence of N-P-K
fertilization on incidence and severity of oxidant injury to mangels and
spinach. Soil Sci. 92:298-301, 1961.
Delete 55
56. Broadwater, to, T., R. C. Hoehn, and P. H. King. Sensitivity of three selected
bacterial species to ozone. Appl. Microbiol. 26:391-393, 1973.
57. Bruton, V. C. Environmental Influence on the Growth of Arabidopsis thaliana.
Ph.D. Thesis. Raleigh: North Carolina State University, 1974. iQ5 pp<
pp.
58. Burleson, G. R., T. M. Murray, and M. Pollard. Inactivation of viruses
and bacteria by ozone, with and without sonication. Appl. Microbiol.
29:340-344, 1975.
59. Butler, W. L., H. W. Siegelman, and C, 0. Miller. Denaturation of phytochrome.
Biochemistry 3:851-857, 1964.
60. Bystrom, B. G., R. B. Glater, F. M. Scott, and E. S. C. Bowler. Leaf sur-
face of Beta vulagris--electron microscope study. Bot. Gaz. 129:
133-138, 1968.
Delete 61
62. Cameron, J. W., and 0. C. Taylor. Injury to sweet corn inbreds and hybrids
by air pollutants in the field and by ozone treatments in the green-
house. J. Environ. Qual. 2:387-389, 1973.
11-186
-------
63. Cameron, J. W. , H. Johnson, Jr., 0. C. Taylor, and H. W. Otto. Differen-
tial susceptibility of sweet corn hybrids to field injury by air
pollution. HortScience 5:217-219, 1970. (UNVERIFIED)
64. Cantwell, A. M. Effect of temperature on response of plants to ozone as
conducted in a specially designed plant fumigation chamber. Plant
Dis. Rep. 52:957-960, 1968.
65. Cantwell, A. M. Air Pollution in Delaware and Its Effects on Plants
Under Ambient and Controlled Environmental Conditions. M.S. Thesis.
Newark: University of Delaware, 1969. 86 pp. (UNVERIFIED)
66. Carney, A. U., G. R. Stephenson, D. P. Ormrod, and G. C. Ashton. Ozone-
herbicide interactions in crop plants. Weed Sci. 21:508-511, 1973.
67. Cathey, H. M. , and H. E. Heggestad. Reduction of ozone damage to Petunia
hybrida Vilm. by use of growth regulating chemicals and tolerant
cultivars. J. Amer. Soc. Hort. Sci. 97:695-700, 1972.
68. Cathey, H. M., and H. E." Heggestad. Effects of growth retardants and fumiga-
tions with ozone and sulfur dioxide on growth and flowing of Euphorbia
pulcherrima Willd. J. Amer. Soc. Hort. Sci. 98:3-7, 1973.
69. Chang, C. W. Effect of ozone on sulfhydryl groups of ribosotnes in pinto bean.
leaves. Relationship with ribosome dissociation. Biochem. Biophys. Res.
Commun. 44:1429-1435, 1971.
70. Chang, C. W. Effect of ozone on ribosomes in pinto bean leaves. Phyto-
chemistry 10:2863-2868, 1971.
71. Chang, C. W. The influence of ozone on growth and ribosomal RNA in pinto
bean plants. Phytochemistry 11:1347-1350, 1972.
72. Chang, C. W., and H. E. Heggestad. Effect of ozone on photosystem II in
Spinacia oleracea chloroplasts. Phytochemistry 13:871-873, 1974.
11-187
-------
73. Chow, C. K., and A. L. Tappel. An enzymatic protective mechanism against
lipid peroxidation damage to lungs of ozone-exposed rats. Lipids
7:518-524, 1972.
Delete 74
75. Clayberg, C. D. Screening tomatoes for ozone resistance. HortScience &•
396-397, 1971.
76. Clayberg, C. D. Evaluation of tomato varieties for resistance of ozone.
Connecticult Agricultural Experiment Station Circular 246, 1972.
11 pp. (UNVERIFIED)
77. Cdbb, P." W., Jr., and R." W. Stark. Decline and mortality of smog-injured
ponderosa pine. J. Forest 68:147-149, 1970.
78. Comeau, G., and F. LeBlanc. Influence de 1'ozone et de 1'anhydride sul-
fureaux sur la regeneration des feuilles de Funaria hygrometrica
HEDW. Natural. Can. 98:347-358, 1971.
79. National Research Council. Committee on Medical and Biologic Effects of
Environmental Pollutants. Vapor-phase Organic Pollutants. Volatile
Hydrocarbons and Oxidation Products. Washington, D. C.: National
Academy of Sciences, 1976. (in press) (UNVERIFIED)
80. National Academy of Sciences. Committee on Medical and Biologic Effects
of Environmental Pollutants. Nitrogen Oxides. Washington, D. C.:
National Academy of Sciences, 1976. (in press) (UNVERIFIED)
Delete 81
82. Costonis, A. C. Acute foliar injury of eastern white pine induced by sulfur
dioxide and ozone. Phytopathology 60:994-999, 1970.
11-188
-------
83. Costonis, A. C. Injury to eastern white pine by sulfur dioxide and ozone
alone and in mixture. Eur. J. Forest. Path. 3:50-55, 1973.
84. Costonis, A. C., and S.'M.' Linzon. Methods for measuring photochemical air
pollution in forest areas. Mitt. Forst. Bundes-Versuch. 92:57-70, 1971.
85. Costonis, A. C., and W. A. Sinclair. Relationships of atmospheric ozone to
needle blight to eastern white pine. Phytopathology 59:1566-1574, 1969.
86. Costonis, A. C., artd W. A. Sinclair. Susceptibility of healthy and ozone-
injured needles of Pinus strobus to invasion by Lophodermium pinastri
and Aureobasidium pullulans. Eur. J. For. Path. 2:65-73, 1972.
87. Coulson, C., and R~ L. Heath. Inhibition o£ the photosynthetic capacity of
isolated chloroplasts by ozone. Plant Physiol. 53:32-38, 1974.
Delete 88
89. Craker, I. E. Ethylene production from ozone injured plants. Environ.
Pollut. 1:299-304, 1971.
90. Craker, L. E. Effects of mineral nutrients on ozone susceptibility of Lemna
minor. Can. J. Bot. 49:1411-1414, 1971.
91. Craker, L.' E. Decline and recovery of petunia flower development from ozone
stress. HortScience 7:484, 1972.
92. Craker, L. E. Influence of ozone on RNA and protein content of Lemna minor 1.
Environ. Pollut. 3:319-323, 1972.
93. Craker, L. E., and W. A. Feder. Development of the inflorescence in petunia,
geranium, and poinsettia under ozone stress. Hortscience 7:59-60, 1972.
94. Craker, L, E., and J,' S.' Starbuck. Metabolic changes associated with ozone
injury of bean leaves. Can. J7 Plant Sci. 52:589-597, 1972.
11-189
-------
Delete 95
96. Craker, I. E. , J. 1. Berube, and P. B. Fredrickson. Community monitoring
of air pollution with plants. Atmos. Environ. 8:845-853, 1974.
97. Curtis, C. R., and R. K. Howell. Increases in peroxidase isoenzyme activity
in bean leaves exposed to low doses of ozone. Phytopathology 61:1306-
1307, 1971.
98. Curtis, L. R., L. V. Edgington, and G. Hofstra. Relationship of ozone
injury to time of application of carboxin analogues. Phytopathology
63:200, 1973. (abstract)
99. Curtis, L. R., L. V. Edgington, and D. J. LittleJohns. Oxathin chemicals
for control of bronzing of white beans. Can. J. Plant Sci. 55:151-
156, 1975.
100. Czuba, M. , and D. P. Ormrod. Effects of cadmium concentration on ozone-
induced phytotoxidity in cress. Plant Physiol. Ann. Suppl. 1974:31.
(abstract)
101. Daines, R. H. Air pollution and plants response, pp. 436-453. In J. E.
Gunckel, Ed. Current Topics in Plant Science. New York: Academic
Press, 1969.
102. Darley, E. F., E. R. Stephens, J. T. Middleton, and P. L. Hanst. Oxidant
plant damage from ozone-olefin reactions. Int. J. Air Pollut. 1:155-
162, 1959.
103. Oarley, E; F., W. M. Dugger, j; B," Mudd, L. Ordin, 0. C. Taylor, and E. R.-
Stephens. Plant damage by pollution derived from automobiles. Arch.
Environ. Health 6:761-770, 1963.
11-190
-------
104. Darnall, K. R. , and J. N. Pitts, Jr. Peroxyacetyl nitrate. A novel reagent
for oxidation of organic compounds. Chem. Commun. 1970:1305-1306.
105. Dass, H. C., and
-------
116. Dean, C. E. Stomate density and size as related to ozone-induced weather
fleck in tobacco. Crop Sci. 12:547-548, 1972.
117. Dean, C. E., and D. R. Davis. Ozone and soil moisture in relation to the
occurrence of weather fleck on Florida cigar-wrapper tobacco in 1966.
Plant Dis. Rep. 51:72-75, 1967.
118. de Koning, H. W., and Z. Jegier. Quantitative relation between ozone con-
centration and reduction of photosynthesis of Euglena gracilis. Atmos,
Environ. 2:615-616, 1968.
119. de Koning, H. W., and Z. Jegier. A study of the effects of ozone and sul-
fur dioxide on the photosynthesis and respiration of Euglena gracilis.
Atmos. Environ. 2:321-326, 1968.
120. de Koning, H., and Z. Jegier. Effect of ozone on pyridine nucleotide
reduction and phosphorylation of Euglena gracilis. Arch. Environ.
Health 18:913-916, 1969.
121. deRoning, H. W., and Z. Jegier. Effects of sulfur dioxide and ozone on
Euglena gracilis. Atmos. Environ. 4:357-361, 1970.
122. Demeritt, M. E., Jr., W. M. Chang, J. D. Murphy, and H. D. Gerhold. Sel-
ection System for Evaluating Resistance of Scotch Pine Seedlings to
Ozone and Sulfur Dioxide. Center for Air Environment Studies. Publ.
243-72. University Park: Pennsylvania State University, 1972. 21
pp. (UNVERIFIED)
123. Dethier, B. E., and D," W,"' Lecher. Atmospheric pollution by oxidants and its
effect on vegetation in a rural environment. Trans. New York Acad. Sci
30:863-868, 1968.
124. Dochinger, L. S. U. S. Forest Service, Delaware, Ohio. Personal Commun-
ications .
11-192
-------
125. Dochinger, L, S,, and C. E, Seliskar. Air pollution and the chlorotie dwar£
disease of eastern white pine. For. Sci. 16:46-55, 1970.
126. Dochinger, 1. S., F. W. Bender, F. I. Fox, and W. W. Heck. Chlorotic
dwarf of eastern white pine caused by an ozone and sulphur dioxide
interaction. Nature 225:476, 1970.
127. Drummond, D, B. Influence of high concentrations of peroxyacetylnitrate
on woody plants. Phytopathology 61:128, 1971. (abstract)
128. Drummond, D. B. The Effect of Peroxyacetyl Nitrate on Petunia (Petunia
hybrida Vilm). Center for Air Environment Studies Publ. 260-72.
University Park: Pennsylvania State University, 1972. 70 pp. (UNVER.)
128a. Bugger, M., Ed. Air Pollution Effects on Plant Growth. American Chemical
Society Symposium Series 3. Washington,,D. C.: American Chemical
Society, 1974. 150 pp. (UNVERIFIED)
129. Dugger, W. M., Jr., and R. I. Palmer. Carbohydrate metabolism in leaves
of rough lemon as influenced by ozone, pp. 711-715. In H. D. Chapman,
Ed. Proceedings of the First International Citrus Symposium. Held
at the University of California, Riverside, March 16-26, 1968. Vol.
2. Riverside: University of California, 1969.
130. Dugger, W. M., and I. P. Ting. The effect of peroxyacetyl nitrate on
plants: Photoreductive reactions and susceptibility of bean plants
to PAN. Phytopathology 58:1102-1107, 1968.
131. Dugger, W. M., and I. P. Ting. Physiological and biochemical effect of air
pollution oxidants on plants. Rec. Adv. Phytochem. 3:31-58, 1970.
132. Dugger, W. M., J. Koukol, and R. L. Palmer. Physiological and biochemical
effects of atmospheric oxidants on plants. J. Air Pollut. Control
Assoc. 16:467-471, 1966.
11-193
-------
133. Dugger, W. M., Jr., 0. C. Taylor, E. Cardiff, and C. R. Thompson. Rela-
tionship between carbohydrate content and susceptibility of pinto
bean plants to ozone damage. Proc. Amer. Soc. Hort. Sci. 81:304-
314, 1962.
134. Dugger, W. M., Jr., 0. C. Taylor, W. H. Klein, and W. Shropshire, Jr.
Action spectrum of peroxyacetyl nitrate damage to bean plants.
Nature 198:75-76, 1963.
135. Dugger, W. M., Jr., 0. C. Taylor, E. Cardiff, and C. R. Thompson. Stoma-
tal action in plants as related to damage from photochemical oxidants,
Plant Physiol. 37:487-491, 1962.
136. Dugger, W. M. , Jr., 0. C. Taylor, C. R. Thompson, and E. Cardiff. The
effect of light on predisposing plants to ozone and PAN damage. J.
Air Pollut. Control Assoc. 13:423-428, 1963.
137. Dunning, J. A., and W. W. Heck. Response of pinto bean and tobacco to
ozone as conditioned by light intensity and/or humidity. Environ.
Sci. Technol. 7:824-826, 1973.
138. Dunning, J. A., and W. W. Heck. Agricultural Research Service. Raleigh,
North Carolina. Personal Communication, 1976.
139. Dunning, J. A., W. W. Heck, and D. T. Tirtgey. Foliar sensitivity of pinto
bean and soybean to ozone as affected by temperature, potassium nutri-
tion and ozone dose. Water Air Soil Pollut. 3:305-313, 1974.
140. Elford, W. J., and J. van den Ende. An investigation of the merits of
ozone as an aerial disinfectant. J. Hyg. 42:240-265, 1942.
141. Engle, R. 1. Reaction of Onion, Allium cepa I., and Pinto Bean, Phaseolus
vulgaris L., to Ozone. Ph.D. Thesis. Madison: University of Wiscon-
sin, 1966. 54 pp.
11-194
-------
142. Engle, R. L., and W. H. Gabelman. Inheritance and mechanism for resistance
to ozone damage in onion, Allium cepa L. Proc. Amer. Soc. Hort. Sci.
89:423-430, 1966.
143. Engle, R. L., and W. H. Gabelman. The effects of low levels of ozone on
pinto beans, Phaseolus vulgaris L. Proc. Amer. Soc. Hort. Sci. 91:
304-309, 1967.
144. Engle, R. L., W. H. Gabelman, and R. R. Romanowski. Tipburn, an ozone
incited response in onion, Allium cepa L. Proc. Amer. Soc. Hort.
Sci. 86:468-474, 1965.
145. U. S. Environmental Protection Agency. Technical Report. Mount Storm,
West Virginia--Gorman, Maryland, and Luke, Maryland--Keyser, West
Virginia, Air Pollution Abatement Activity. Pre-Conference Investi-
gations. Air Pollution Control Office Publ. No. APTD-0656. Research
Triangle Park, N. C.: U. S. Environmental Protection Agency, 1971.
Delete 146
147. Evans, L.' S. Bean leaf growth response to moderate ozone levels. Environ.
Pollut. 4:17-26, 1973.
148. Evans, L. S. Microscopic changes in, avena and Phaseolus from ozone expos-
ure. Preprint. 22 pp. (UNVERIFIED)
149. Evans, L. S., and P. R. Miller. Ozone damage to ponderosa pine: A histo-
logical and histochemical appraisal. Amer. J. Bot. 59:297-304, 1972.
150. Evans, L. S., and P. R. Miller. Comparative needle anatomy and relative
ozone sensitivity of four pine species. Can. J. Bot. 50:1067-1076,
1972. ^ __ ^
151. Evans, I. S., and ?. R. Miller. Histological comparison of single and
additive 0., and SO injuries to elongating ponderosa pine needles.
Amer. J. Bot. 62:416-421, 1975.
11-195
-------
Delete 152
153. Evans, I. S., and I. P. Ting. Ozone sensitivity of leaves: Relationship
to leaf water content, gas transfer resistance, and anatomical char-
acteristics. Amer. J. Bot. 61:592-597, 1974.
6d
154. Evans, L. S. , and I. P. Ting. Effect of ozone on ° Rb-labeled potassium
transport in leaves of Phaseolus vulgaris L. Atmos. Environ. 8:855-
861, 1974.
155. Feder, W.' A. Reduction in tobacco pollen germination and tube elongation,
induced by low levels of ozone. Science 160:1122, 1968.
156. Feder, W. A. Plant response to chronic exposure of low levels of oxidant
type air pollution. Environ. Pollut. 1:73-79, 1970.
157. Feder, W. A,, and F. J. Campbell. Influence of low levels of ozone on
flowering of carnations. Phytopathology 58:1038-1039, 1968.
158. Feder, W. A., and F. Sullivan. Ozone: Depression of frond multiplication
and floral production in duckweed. Science 165:1373-1374, 1969.
159. Feder, W. A., and F. Sullivan. The effect of ambient temperature on the
sensitivity of aquatic green plants to low levels of ozone. Paper
72-158 Presented at 65th Annual Meeting of the Air Pollution Control
Association, 1972. 9 pp. (UNVERIFIED)
Delete 160
161. Feder, W. A., J. Donoghue, and I. Perkins. Response of poinsettia cultivars
to ozone. Florogram 5:13-14, 1972. (UNVERIFIED)
162. Feder, W. A., F. 1. Fox, W. W. Heck, and F. J. Campbell. Varietal responses
of petunia to several air pollutants. Plant Dis. Rep. 53:506-509, 1969.
11-196
-------
163. Feliciano, A. Survey and assessment of air pollution damage to vegetation
in New Jersey. Cooperative Extension Service. New Brunswick, N. J.:
Rutgers, The State University, 1971. 43 pp. (UNVERIFIED)
164. Ferry, B. W., M. S. Baddeley, and D. L. Hawksworth, Eds. Air Pollution and
Lichens. Toronto: University of Toronto Press, 1973. 389 pp.
165. Fetner, R. H., and R. S. Ingols. A comparison of the bactericidal activity
of ozone and chlorine against Escherichia coli at 1 . J. Gen. Micro-
biol. 15:381-385, 1956.
166. Fletcher, R. A., N. 0. Adedipe, and D. P. Ormrod. Abscisic acid protects
bean leaves from ozone-induced phytotoxicity. Can. J. Bot. 50:2389-
2391, 1972.
Delete 167
168. Frederick, P. E., and R. 1. Heath. Ozone-induced fatty acid and viability
changes in Chlorella. Plant Physiol. 55:15-19, 1975.
169. Freebairn, H. T., Reversal of inhibitory effects of ozone on oxygen uptake
of mitochondria. Science 126:303-304, 1957.
170. Freebairn, H. T., and 0. C. Taylor. Prevention of plant damage from air-
borne oxidizing agents. Proc. Amer. Soc. Hort. Sci. 76:693-699, 1960.
171. Frey, J. E. The Effects of Ozone on the Synthesis and Storage of Nutrients
in Soybean Seeds. Ph.D. Thesis. Greeley: University of Northern
Colorado, 1972. 109 pp.
Delete 172
Delete 173
174. Fujiwara, T. Damage to plants by combined air pollution. Shokubutsu
Boeki (Plant Protection) 27:233-236, 1973. (in Japanese)
11-197
-------
175. Yamazoe, F. Plant-damaging air pollutants. Shokubutsu Boeki (Plant Pro-
tection) 27:220-223, 1973. (in Japanese)
176. Gardner, W. S. 'Ozone injury to tobacco plants in South Dakota. Plant Dis.
Rep. 57:106-110, 1973.
177. Gentile, A. G., ft. A, Feder, R." E. Young, arid 2. Santner. Susceptibility of"
Lycopersicon spp. to ozone injury. J. Amer. Soc. Hort. Sci. 96:94-96,
1971.
178. Glater, R. A. B. Smog, damage to ferns in the Los Angeles area.
Phytopathology 46:696-698, 1956.
179. Glater, R. B. , R. A. Solberg, and F. M. Scott. A developmental study of
the leaves of Nicotiana glutinosa as related to their smog-sensitivity.
Amer. J. Bot. 49:954-970, 1962.
180. Gross, R. E. , and W. M. Dugger, Jr. Responses of Chiamydomonas reinhardtii
to peroxyacetyl nitrate. Environ. Res. 2:256-266, 1969.
181. Grosso, J. J., H. A. Menser, G. H. "Hodges, and H. H. McKinney. Effects
of air pollutants on Nicotiana cultivars and species used for virus
studies. Phytopathology 61:945-950, 1971.
182. Guinvarc'h, P. Three years of ozone sterilization of water in Paris. Adv.
Chem. Ser. 21:416-429, 1957.
183. Haagen-Smit, A. J., E. F. Darley, M. Zaitlin, H. Hull, and W. Noble.
Investigation on injury to plants from air pollution in the Los
Angeles area. Plant Physiol. 27:18-34, 1952.
184. Haas, J. H. Relation of crop maturity and physiology to air pollution
incited bronzing of Phaseolus vulgaris. Phytopathology 60:407-410,
1970.
11-198
-------
185. Haines, R. B. Effect of pure ozone on bacteria, pp. 30-31. In Report of
the Food Investigation Board for the Year 1936. London: His Majesty's
Stationary Office, 1937. (UNVERIFIED)
186. Hall, M. A., and L. Ordin. Subcellualr location of phosphoglucomutase
and UDP glucose pyrophosphorylase in avena coleoptiles. Physiol.
Plant. 20:624-633, 1967.
Delete 187
188. Hanson, G. P. Relative air pollution sensitivity of some Los Angeles
Arboretum plants. Lasca Leaves 22:86-89, 1972.
189. Hanson, G. P., and W." S." Stewart. Photochemical oxidantsi Effect on starch
hydrolysis in leaves. Science 168:1223-1224, 1970.
• ." • I '////;"
190. Hanson, G. P., L. Thorne, and D. H. Addis. Ozone sensitivity of Petunia
hybrida Vilm. as related to physiological age. J. Amer. Soc. Hort.
Sci. 100:188-190, 1975.
191. Hanson, G. P., L. Thorne, and C. D. Jativa. Ozone tolerance of petunia
leaves as related to their ascorbic acid concentration, pp. 261-
266. In H. M. Englund and W. T. Beery, Eds. Proceedings of the
Second International Clean Air Congress. Held at Washington, D. C. ,
Dec. 6-11, 1970. New York: Academic Press, 1971.
192. Harding, P. R., Jr. Effect of ozone on penicillium mold decay and sporu-
lation. Plant Dis. Rep. 52:245-247, 1968.
193. Harrison, B. H., and W. A. Feder. Ultrastructural changes in pollen
exposed to ozone. Phytopathology 64:257-258, 1974.
194. Harward, M., and M. Treshow. Impact of ozone on the growth and reproduc-
tion of understorey plants in the aspen zone of western U.S.A.
Environ. Conserv. 2:17-23, 1975.
11-199
-------
95. Heagle, A. S. Effect of low-level ozone fumigations on crown rust of oats.
Phytopathology 60:252-254, 1970.
196. Heagle, A. S. Interactions between air pollutants and plant parasites. Ann
Rev. Phytopath. 11:365-388, 1973.
197. Heagle, A. S. Response of three obligate parasites to ozone. Environ.
Pollut. 9:91-95, 1975.
198. Heagle, A. S., and W. W. Heck. Predisposition of tobacco to oxidant air
pollution injury by previous exposure to oxidants. Environ. Pollut.
7:247-252, 1974.
199. Heagle, A4 S., and L. W. Key. Effect of ozone on the wheat stem rust fungus.
Phytopathology 63:397-400, 1973.
200. Heagle, A. S.', and L. W. Key. Effect of Puccinia graminis f. sp. tritici on
ozone injury in wheat. Phytopathology 63:609-613, 1973.
201. Heagle, A. S., and G. E. Neely. Agricultural Research Service. Raleigh,
North Carolina. Personal Communication. 1976.
202. Heagle, A. S., and A. Strickland. Reaction of Erysiphe graminis f. sp.
hordei to low levels of ozone. Phytopathology 62:1144-1148, 1972.
203. Heagle, A. S., and L. L. Trent. Agricultural Research Service. Raleigh,
North Carolina. Personal Communication. 1976.
204. Heagle, A. S. , D. E. Body, and W. W Heck. An open-top field chamber to
assess the impact of air pollution on plants. J. Environ. Qual. 2:
365-368, 1973.
205. Heagle, A. S., D. E. Body, and G. E. Neely. Injury and yield responses
of soybean to chronic doses of ozone and sulfur dioxide in the field.
Phytopathology 64:132-136, 1974.
11-200
-------
206. Heagle, A. S., D. E. Body, and E. K. Pounds. Effect of ozone on yield of
sweet corn. Phytopathology 62:583-687, 1972.
207. Heagle, A. S., W. W. Heck, and D. Body. Ozone injury to plants as influ-
enced by air velocity during exposure. Phytopathology 61:1209-1212,
1971.
208. Heck, W. W. Plant injury induced by photochemical reaction products of
propylene-nitrogen dioxide mixtures. J. Air Pollut. Control Assoc.
14:255-261, 1964.
209. Heck, W.'W. The use of plants as indicators of air pollution. Int. J. Air
Water Pollut. 10:99-111, 1966.
210. Heck, W. W. Factors influencing expression of oxidant damage to plants.
Ann. Rev. Phytopath. 6:165-188, 1968.
211. Heck, W. W., and C. S. Brandt. Impact of air pollutants on vegetation:
Crops, forests, native, pp. In. A. C. Stern, Ed. Air Pollu-
tion. (3rd ed.) Vol. 2. New York: Academic Press, (in press)
212. Heck, W. W., and J. A. Dunning. The effects of ozone on tobacco and pinto
bean as conditioned by several ecological factors. J. Air Pollut.
Control Assoc. 17:112-114, 1967.
213. Heck, W. W., and A. S. Heagle. Measurement of photochemical air pollution
with a sensitive monitoring plant. J. Air Pollut. Control Assoc. 20:
97-99, 1970.
214. Heck, W. W., and D. T. Tingey. Ozone. Time-concentration model to predict
acute foliar injury, pp. 249-255. In H. M. Englund and W. T. Beery,
Eds. Proceedings of the Second International Clean Air Congress.
Held at Washington, D. C., December 6-11, 1970. New York: Academic
Press, 1971.
11-201
-------
215. Heck, W. w., R. H. Dairies, and I. J. Hindawi. Other phytotoxic pollutants,
pp. F1-F24. In J. S. Jacobson, and A. C. Hill, Eds. Recognition of Air
Pollution Injury to Vegetation: A Pictorial Atlas. Pittsburgh: Air
Pollution Control Association, 1970.
216. Heck, W. W., J. A. Dunning, and I. J. Hindawi. Interactions o£ environmental
factors on the sensitivity of plants to air pollution. J. Air Pollut.
Contr. Assoc. 15:511-515, 1965.
217. Heck, W. W. , J. A. Dunning, and I. J. Hindawi. Ozone: Non-linear relation
of dose and injury in plants. Science 151:577-578, 1966.
218. Heck, W. W. , J. A. Dunning, and H. Johnson. Design of a Simple Plant
Exposure Chamber. National Air Pollution Control Administration Publ.
No. APTD 68-6. Cincinnati, Ohio: U. S. Department of Health,
Education, and Welfare, 1968. 24 pp.
219. Heck, W. W., 0. C. Taylor, and H. E. Heggestad. Air pollution research
needs: Herbaceous and ornamental plants and agriculturally generated
pollutants. J. Air Pollut. Control Assoc. 23:257-266, 1973.
220. Heck, W. W., F. L. Fox, C. S. Brandt, and J. A. Dunning. Tobacco, a
Sensitive Monitor for Photochemical Air Pollution. National Air
Pollution Control Administration Publ. No. AP-55. Cincinnati:
U. S. Department of Health, Education, and Welfare, 1969. 23 pp.
221. Heggestad, H. E. Photochemical air pollution injury to potatoes in the
Atlantic coastal states. Amer. Potato J. 50:315-328, 1973.
222. Heggestad, H. E., and E. F. Darley. Plants as indicators of the air pollutants
ozone and PAN, pp. 329-335. In Air Pollution. Proceedings of the First
European Congress on the Influence of Air Pollution on Plants and Animals.
Wapeningen, April 22 to 27, 1968. Wageningen, The Netherlands: Centre
for Agricultural Publishing and Documentation, 1969.
11-202
-------
223. Heggestad, H. E., and W. w. Heck. Nature, extent, and variation of plant
response to air pollutants. Adv. Agron. 23:111-145, 1971.
224. Heggestad, H. E., and H. A. Menser. Leaf spot-sensitive tobacco strain
Bel W-3, a biological indicator of the air pollutant ozone. Phyto-
pathology 52:735, 1962. (abstract)
225. Heggestad, H. E., and J. T. Middleton. Ozone in high concentrations as
cause of tobacco leaf injury. Science 129:208-210, 1959.
226. Heggestad, H. E,, F. R. Burleson, J. T. Middleton, and E. F. Darley. Leaf
injury on tobacco varieties resulting from ozone, ozonated hexene-1
and ambient air of metropolitan areas. Int. J. Air Water Pollut. 8:
1-10, 1964.
227. Hibben, C. R. The distinction between injury to tree leaves by ozone and
mesophyll-feeding leafhoppers. Forest Sci. 15:154-157, 1969.
228. Hibben, C. R. Plant injury by oxidant-type pollutants in the New York City
atmosphere. Plant Dis. Reptr. 53:544-548, 1969.
229. Hibben, C. R. Ozone toxicity to sugar maple. Phytopathology 59:1423-1428,
1969.
230. Hibben, C. R. , and M. P. Taylor. The leaf roll-necrosis disorder of
lilacs: Etiological role of urban-generated air pollutants. J.
Amer. Soc . Hort. Sci. 99:508-514, 1974.
Delete
232. Hill, A. C. A special purpose plant environmental chamber for air pollution
studies. J. Air Pollut. Contr. Assoc. 17:743-748, 1967.
233. Hill, A." C, Vegetation: A sink for atmospheric pollutants. J. Ait Pollut.
Control Assoc. 21:341-346, 1971.
11-203
-------
234. Hill, A. C., and N. Littlefield. Ozone. Effect on apparent photosynthesis,
rate of transpiration, and stomatal closure in plants. Environ. Sci.
Technol. 3:52-56, 1969.
235. Hill, A. C., H. E. Heggestad, and S. N. Linzon. Ozone, pp. B1-B22. In
J. S. Jacobson and A. C. Hill, Eds. Recognition of Air Pollution
Injury to Vegetation: A Pictorial Atlas. Pittsburgh: Air Pollution
Control Association, 1970.
236. Hill, A. C., M. R. Pack, M. Treshow, R. J. Downs, and L. G. Transtrum. Plant
injury induced by ozone. Phytopathology 51:356-363, 1961.
237. Hindawi, I. J. Natural pollutants in Staten Island, New York and Perth
Amboy, New Jersey as reflected on vegetation. Paper Presented at
New York/New Jersey Air Pollution Abatement Conference 1968. 24 pp.
237a. Hindawi, I. J., and A. P. Altshuller. Plant damage caused by irradiation
of aldehydes. Science 146:540-542, 1964.
238. Hindawi, I. J. , J. A. Dunning, and C. S. Brandt. Morphological and micro-
scopical changes in tobacco, bean, and petunia leaves exposed to
irradiated automobile exhaust. Phytopathology 55:27-30, 1964.
239. Hodges, G. H., H. A. Menser, Jr., and W. B. Ogden. Susceptibility of
Wisconsin havana tobacco cultivars to air pollutants. Agron. J.
63:107-111, 1971.
240. Hodgson, R. H. Alteration of triazine metabolism by ozone, p. 28. In
Weed Science Society of American Abstracts 1970.
241. Hodgson, R. H., K. E. Dusbabek, and B. L. Hoffer. Diphenamid metabolism
in tomato: Time course of an ozone fumigation effect. Weed Sci. 22:
205-210, 1974.
11-204
-------
242. Hodgson, R. H,, D.' S.' Frear, H. R. Swanson, and L. A. Regan. Alteration of
diphenamid metabolism in tomato by ozone. Weed Sci. 21:542-548, 1973.
243. Hoffmann, A. R. The Effect of Ozone on Nicotine Concentration in Nicotiana
tabacum L. Leaves. Ph.D. Thesis. Philadelphia: Temple University,
1974. 88 pp.
244. Hoffman, G.'J,, E.' V. Maas, and S. L, Rawlins. Salinity-ozone interactive
effects on yield and water relations of pinto bean. J. Environ. Qual.
2:148-152, 1973.
245. Hoffman, G. J. , E. V. Maas, and S. L. Rawlins. Salinity-ozone inter-
active effects on alfalfa yield and water relations. J. Environ.
Qual. 4:326-331, 1975.
246. Homan, C. Effects of ionized air and ozone on plants. Plant Physiol. 12:
957-978, 1937.
247. Hooker, W. J., T. C. Yang, and H. S. Potter. Air pollution injury of
potato in Michigan. Amer. Potato J. 50:151-161, 1973.
248. Houston, D. B. Physiological and Genetic Response of Pinus strobus L.
Clones to Sulfur Dioxide and Ozone Exposures. Ph.D. Thesis.
Madison: University of Wisconsin, 1971. 85 pp.
249. Houston, D. A. Response of selected Pinus strobus L. clones to fumigations
with sulfur dioxide and ozone. Can. J. Forest Res. 4:65-68, 1974.
25°- Houston, D. B., and G. R. Stairs. Genetic control of sulfur dioxide and
ozone tolerance in Eastern white pine. Forest Sci 19:267-271, 1973.
251. Houten, J. G. ten. Aspects of air pollution in agriculture. Landbouwkundig
Tijdschrift 78:2-13, 1966. (in Dutch, summary in English)
11-205
-------
251a. Howell, R. K. Influence of air pollution on quantitites of caffeie acid
isolated from leaves of Phaseolus vulgaris. Phytopathology 60: 1626-
1629, 1970.
252. Howell, R. H. Phenols, ozone, and their involvement in pigmentation and
physiology of plant injury, pp. 94-105. In M. Dugger, Ed. Air Pol-
lution Effects on Plant Growth. American Chemical Society Symposium
Series 3. Washington, D. C.: American Chemical Society, 1974. (UNVER.)
253. Howell, R. K., and E. J. Koch. An experimental design for open-top field
chambers to estimate crop losses caused by air pollution. (in press)
254. Howell, R. K., and D. F. Kremer. Ozone injury to soybean cotyledonary
leaves. J. Environ. Qual. 1:94-97, 1972.
255. Howell, R. K., and D. P. Kremer. Chemistry and physiology of pigmentation
in leaves injued by air pollution. J. Environ. Qual. 2:434-438, 1973.
256. Howell, R. K., and C. A. Thomas. Relative tolerances of twelve safflower
cultivars to ozone. Plant Dis. Rep. 56:195-197, 1972.
257. Howell, R. K., T. E. Devine, and C. H. Hanson. Resistance of selected
alfalfa strains to ozone. Crop. Sci. 11:114-115, 1971.
Delete 25S
259. Hull, H. M., and F. W. Went. Life processes of plants as affected by air
pollution, pp. 122-218. In Proceedings of the Second National Air
Pollution Symposium, Pasadena, California, 1962. Los Angeles: National
Air Pollution Symposium, 1952.
Delete 260
261. Jacobson, J. S., and S. Colavito. The effect of SCL on the phytotoxicity
of Cy Plant Physiol. Ann. Suppl. 1974:31. (abstract)
11-206
-------
262. Jacobson, J. S., and W, A. Feder. A Regional Network for Environmental
Monitoring: Atmospheric Oxidant Concentrations and Foliar Injury -to
Tobacco Indicator Plants in the Eastern United States. Massachusetts
Agricultural Experiment Station Bulletin No. 604. Amherst: Univer-
sity of Massachusetts, College of Food and Natural Resources, 1974.
31 pp.
Delete 263
264. Jensen, K. F. Response of nine forest tree species to chronic ozone fum-
igation. Plant Dis. Rep. 57:914-917, 1973.
265. Jensen, K. F\, and" L." S. Dochirtger. Responses 6f hybrid poplar cuttings to
chronic and acute levels of ozone. Environ. Pollut. 6:289-295, 1974.
266.' Johnson, H., Jr., J. W. Cameron, and 0. C. Taylor. Air pollution resis-
tance in sweet corn varieties. Calif. Agric. 25(5):8-10, 1971.
267. Jones, J. L. Ozone damage: Protection for plants. Science 140:1317-
1318, 1963.
268. Juhren, M., W. Noble, and F. W. Went. The standardization of Poa annua as
an indicator of smog concentrations. I. Effects of temperature,
photoperiod, and light intensity during growth of the test plants.
Plant Physiol. 32:576-586, 1957.
269. Kadota, M. , and K. Ohta. Ozone sensitivity of Japanese plant species in
summer, with special reference to a tentative sensitivity grade list for
applying to field survey on ozone injury. Taiki Osen Kenkyu (J. Jap.
Soc. Air Pollut.) 7:19-26, 1972. (in Japanese, summary in English)
270. Kanoh, F. Ozone reaction on slime mold. Tokyo Toritsu Eisei Kenyssho
Kenkyu Nempo 24:337-342, 1972. (in Japanese) (UNVERIFIED)
11-207
-------
271. Keen, N. T., and 0. C. Taylor. Ozone injury in soybeans: Isoflavonoid
accumulation is related to necrosis. Plant Physiol. 55:731-733, 1975.
272. Keller, T. The use of peroxidase activity for monitoring and mapping air
pollution areas. Eur. J. Forest Path. 4:11-19, 1974.
273. Render, W. J., and S. G. Carpenter. Susceptibility of grape cultivars and
selections to oxidant injury. Fruit Var. J. 28:59-61, 1974.
Delete 274
Delete
276. Render, w. j., E. F»" Taschenberg, and N. Jk Shaulis. Benomyl protection of
grapevines from air pollution injury. HortScience 8:396-398, 1973.
277. Kendrick, J.' B.5 Jr., E. F/ Darley, and J." Tf Middleton. Chemotherapy for
oxidant and ozone induced plant damage. Int. J. Air Water Pollut. 6:
391-402, 1962.
278. Kendrick, J. B., Jr., J. T. Middleton, and E. F. Darley. Chemical protec-
tion of plants from ozonated olefin (smog) injury. Phytopathology
44:494-495, 1954. (abstract)
279. Rerr, E. D., and R. A. Reinert. The response of bean to ozone as related to
infection by Pseudomonas phaseolicola. Phytopathology 58:1055, 1968.
(abstract)
280. Rhatamian, H., N. 0." Adedipe, and D," ?. Ormrod. Soil-plant-water aspects of
ozone phytotoxicity in tomato plants. Plant Soil 38:531-541, 1973.
281. Kinman, R. N. Uater and wastewater disinfection with ozone: A critical
review. CRC Crit. Rev. Environ. Control 5:141-152, 1975.
Delete 282
Delete 283
11-208
-------
284. Klingaman, G. I., and C. B. Link. Reduction air pollution injury to foli-
age of Chrysanthemum morifolium Ramata using tolerant cultivars and
chemical protectants. J. Amer. Soc. Hort. Sci. 100:173-175, 1975.
285. Knabe, W., C. S. Brandt, H. van Haut, and C. J. Brandt. Nachwech photochem-
ischer Luftverunreiniqungen dutch biologische Indikatoren in der Bundes-
republik Deutschland, pp. A110-A114. In Proceedings of the Third
International Clean Air Congress. Held at Dusseldorf, Federal Repub-
lic of Germany, October 8-12, 1973. Dusseldorf: Verlag des Vereins
Deutscher Ingenieur, 1973.
285a. Knight, R. C., and J. H.' Priestley. The respiration of plants under various
electrical conditions. Ann. Bot. 28:135-161, 1914.
286. Kochlar, M. Phytotoxic and Competitive Effects of Tall Fescue on Ladino
Clover as Modified by Ozone and/or Rhizoctonia solani. Ph.D. Thesis.
Raleigh: North Carolina State University, 1974. 71 pp. (UNVERIFIED)
287. Kohut, R. J. Response of Hybrid Poplar to Simultaneous Exposure to Ozone
and PAN. Center for Air Environment Studies Publ. #288-72. Univer-
sity Park: Pennsylvania State University, 1972. 26 pp. (UNVERIFIED)
288. Koiwai, A., H. Kitano, M. Fukuda, and T. Kisaki. Methylenedioxyphenyl and
its related compounds as protectants against ozone injury to plants.
Agric. Biol. Chem. 38:301-307, 1974.
289. Koritz, H. G., and F. W. Went. The physiological action of smog on plants.
I. Initial growth and transpiration studies. Plant Physiol. 28:50-
62, 1953.
290. Kress, I. W. Response of Hybrid Poplar to Sequential Exposures of Ozone
and PAN. Center for Air Environment Studies,Publ. #259-272. Univer-
sity Park: Pennsylvania State University, 1972. 39 pp. (UNVERIFIED)
11-209
-------
Delete 291
292. Kuss, F. R. The Effect of Ozone on Fungus Sporulation. M.S. Thesis.
Durham: University of New Hampshire, 1950. 27 pp. (UNVERIFIED)
293. Lacasse, N. I. Assessment of Air Pollution Damage to Vegetation in Penn-
sylvania. Center for Air Environment Studies Publ. #209-71. Univer-
sity Park: Pennsylvania State University, 1971. 61 pp. (UNVERIFIED)
294. Landau, E., and C." S. Brandt. The use of surveys to estimate ait pollution
damage to agriculture. Environ. Res. 3:54-61, 1970.
295. Lacasse, N. L., and T. C. Weidensaul. A cooperative extension-based system
of assessing air pollution damage to vegetation: Organization, results,
and recommendations for future surveys, pp. 132-136. In H. M. Englund
and W. T. Beery, Eds. Proceedings of the Second International Clean
Air Congress. Held at Washington, D. C., December 6-11, 1970. New
York: Academic Press, 1971.
296. Larkin, R. C. Reduction of Ozone Damage on Bean and Tobacco with Peroxi-
dase Injections. M. S. Thesis. Newark: University of Delaware,
1973. 19 pp. (UNVERIFIED)
297. Larsen, R. I., and W. W. Heck. An air quality data analysis system for
interrelating effects, standards, and needed source reductions--
Part 3. Vegetation Injury. J. Air Pollut. Control Assoc. (in press)
(UNVERIFIED)
298. Ursh, R." N., P, R.~ Miller, and S»~ L." Wert. Aerial photography to detect a
evaluate air pollution damaged ponderosa pine. J7 Air Pollut. Control
Assoc. 20;289-292, 1970.
Delete 299
11-210
-------
300. Lea, M. C. On the influence of ozone and some other chemical agents on
germination and vegetation. Amer. J. Sci. Arts. 37:373-376, 1864.
301. ledbetter, M. C., P. W. Zimmerman, and A. E. Hitchcock. The histopatholog-
ical effect of ozone on plant foliage. Contrib. Boyce Thompson Inst.
20:275-282, 1959.
302. Lee, T. T. Sugar content and stomatal width as related to ozone injury in
tobacco leaves. Can. J. Bot. 43:677-685, 1965.
303. Lee, T. T. Chemical regulation of ozone susceptibility in Nicotiana tabacum.
Can. J. Bot. 44:487-496, 1966.
304. Lee, T. T. Inhibition of oxidative phosphorylation and respiration by
ozone in tobacco mitochondria. Plant Physiol. 42:691-696, 1967.
305. Leffler, H. R., and J. H. Cherry. Destruction of enzymatic activities o£ corn
and soybean leaves exposed to ozone. Can. J. Bot. 52:1233-1238, 1974.
306. Leh, F., and J. B. Mudd. Reaction of peroxyacetyl nitrate with cysteine,
cystine, methionine, lipoic acid, papaj.n, and lysozyme. Arch. Biochem.
Biophys. 161:216-221, 1974.
307. Leh, F., and J. B. Mudd. Reaction of ozone with lysozyme, pp. 22-39. In
M. Dugger, Ed. Air Pollution Effects on Plant Growth. ACS Symposium
Series 3. Washington, D. C.: American Chemical Society, 1974. (UNVER.)
308. Leone, I. A., and E. Brennan. Ozone toxicity in tomato as modified by phos-
phorus nutrition. Phytopathology 60:1521-1524, 1970.
Delete 363
310. Leone, I. A., and D. Green. A field evaluation of air pollution effects
on petunia and potato cultivars in New Jersey. Plant Dis. Rep. 58:
683-687, 1974.
11-211
-------
311. Leone, I. A., E. Brennan, and R. H. Daines. Effect of nitrogen nutrition
on the response of tobacco to ozone in the atmosphere. J. Air Pollut.
Control Assoc. 16:191-196, 1966.
Delete
313. Linzon, S. N. The development of foliar symptoms and the possible cause and
origin of white pine needle blight. Can. J. Bot 38:153-161, 1960.
314. Linzon, S. N. Semimature-tissue Needle Blight of Eastern White Pine and
Local Weather. Ontario Department of Forestry, Research Laboratories
Information Report O-X-1, 1965. (UNVERIFIED)
315. Linzon, S. N. Damage to Eastern white pine by sulfur dioxide, semi-mature-
tissue needle blight, and ozone. J. Air Pollut. Control Assoc. 16:
140-144, 1966.
Delete 316
317. Linzon, S. N., and A. C. Costonis. Symptoms caused by photochemical air
pollution injuries to forest trees. Mitt. Forst. Bundes-Versuch. 92:
71-82, 1971.
318. Linzon, S. N., W. W. Heck, and F. D. H. Macdowall. Effects of photochem-
ical oxidants on vegetation, pp. 89-142. In Photochemical Air Pollu-
tion: Formation, Transport and Effects. NRC Associate Committee on
Scientific Criteria for Environmental Quality. Report No. 12. Publ.
No. NRCC 14096. Ottawa: National Research Council of Canada, 1975.
319. Maas, E. V,, G. J. Hoffman, S. L. Rawlins, and G. Ogata. Salinity-ozone
interactions on pinto bean: Integrated response to ozone concentra-
tion and duration. J. Environ. Qual. 2:400-404, 1973.
320. Macdowall, F. D. H. Predisposition of tobacco to ozone damage. Can. J.
Plant Sci. 45:1-12, 1965.
11-212
-------
321. Macdowall, F. D. H. Stages of ozone damage to respiration of tobacco leaves.
Can. J. Bot. 43:419-427, 1965.
322. Macdowall, F. D. H. Importance of soil in the absorption of ozone by a crop.
Can. J.' Soil Sci. 54:239-240, 1974.
323. Macdowall, F. D. H., and A. F, W. Cole. Threshold and synergistic damage to
tobacco by ozone and sulfur dioxide. Atmos. Environ. 5:553-559, 1971.
324. Macdowall, F. D. H., E. I. Mukammal, and A. F. W. Cole. Direct correla-
tion of air-polluting ozone and tobacco weather fleck. Can. J. Plant
Sci. 44:410-417, 1964.
Delete 325
326. MacKnight, M. L. The Effect of Ozone on Stmatal Aperture and Transpiration.
M.S. Thesis. Salt Lake City: University of Utah, 1968. 80 pp.
327. Magdycz, W. P. The Effects of Concentration and Exposure Time on the
Toxicity of Ozone to the Spores of Botrytis cinerea. M.S. Thesis.
Waltham: University of Massashucetts, 1972. 39 pp.
328. Magdycz, W. P., and W. J. Manning. Botrytis cinerea protects broad bean
against visible ozone injury. Phytopathology 63:204, 1973. (abstract)
329. Magie, R. 0. Controlling gladiolus botrytis bud rot with ozone gas, Proc.
Flor. State Hort. Soc. 73:373-375, 1960.
330. Magie, R. 0. Botrytis disease control on gladiolus, carnations, and chrysan-
themums. Proc. Fla. State Hort. Soc. 76:458-461, 1963.
331. Mandl, R. H., M. C. O'Neill, and L. H. Weinstein. The effect of ozone on the
phototoxicity of sulfur dioxide for alfalfa. Plant Physiol. Ann. Suppl.
1974:30. (abstract)
332. Mandle, R. H., L. H. Weinstein, D. C. McCune, and M. Keveny. A cylindrical,
open-top chamber for the exposure of plants to air pollutants in the
field. J. Environ. Qual. 2:371-376, 1973.
11-213
-------
Delete 333
334. Manning, W. J., and P. M. Vardaro. Suppression of oxidant injury on beans by
systemic fungicides. Phytopathology 63:1415-1416, 1973.
335. Manning, W. J. , and P. M. Vardaro. Ozone and Pyjrenochaeta lycopersici;
Effects on growth and development of tomato plants. Phytopathology
64:582, 1974. (abstract)
336. Manning, W. J., W. A. Feder, and I. Perkins. Ozone injury increases infec-
tion of geranium leaves by Botrytis cinerea. Phytopathology 60:669-
670, 1970.
337. Manning, W. J., W. A. Feder, and I. Perkins. Ozone and infection o£ geranium
flowers by Botrytis cinerea. Phytopathology 60:1302, 1970. (abstract)
338. Manning, W. J., W. A. Feder, and I. Perkins. Sensitivity of spinach cul-
tivars to ozone. Plant Dis. Rep. 56:832-833, 1972.
339. Manning, W. J., W. A. Feder, and I. Perkins. Effects of Botrytis and ozone
on bracts and flowers of poinsettia cultivars. Plant Dis. Rep. 56:
814-816, 1972.
340. Manning, W. J., W. A. Feder, and I. Perkins. Response of poisettia culti-
vars to several concentrations of ozone. Plant Dis. Rep. 57:774-775,
1973.
341. Manning, W. J., W. A. Feder, and P. M. Vardaro. Benomyl in soil and res-
ponse of pinto bean plants to repeated exposures to a low level of
ozone. Phytopathology 63:1539-1540, 1973.
342. Manning, W. J., W. A. Feder, and P. M. Vardaro. Reduction of chronic ozone
injury on poinsettia by benomyl. Can. J. Plant Sci. 53:833-835, 1973.
343. Manning, W. J., W. A. Feder, and P. M. Vardaro. Suppression of oxidant
injury by benomyl: Effects on yields of bean cultivars in the field.
J. Environ. Qual. 3:1-3, 1974.
11-214
-------
344. Manning, W. J., W. A. Feder, P. M. Papia, and I. Perkins. Effect of low
levels of ozone on growth and susceptibility of cabbage plants to
Fusarium oxysporum F. sp. conglutinans. Plant Dis. Rep. 55:47-49, 1971.
345. Manning, w. J4, W. A. Feder, P. M. Papia, and I, Perkins. Influence of foliar-
ozone injury on root development and root surface fungi of pinto bean
plants. Environ. Pollut. 1:305-312, 1971.
346. Manning, W. J4, W, A, Fedet, I. Perkins, and M. Glickman. Ozone injury and
infection of potato leaves by Botrytis cinerea. Plant Dis. Rep. 53:
691-693, 1969.
347. Mansfield, T. A. The Role of Stomata in Determining the Responses of
Plants to Air Pollutants. Commentaries Plant Sci. 2:11-20, 1973.
348. Markowski, A., and S. Grzesiak. Influence of sulfur dioxide and ozone on
vegetation of bean and barley plants under different soil moisture
conditions. Bull. Acad. Pol. Sci. Ser. Sci. Biol. 22:875-887, 1975.
349. Matsushima, J. On composite harm to plants by sulfurous acid gas and
oxidant. Sangyo Kogai 7:218-224, 1971. (in Japanese)
350. McCarthy, J. J., and C. H. Smith. A review of ozone and its application
to domestic wastewater treatment. J. Amer. Water Works Assoc. 66:
718-725, 1974.
350a. McCarty, R. E., P. R. Pittman, and Y. Tsuchiya. Light-dependent inhibition
of photophosphorylation by N-ethylmaleimide. J. Biol. Chem. 247:3048-
3051, 1972.
351. Mcllvenn, W. D. , R. A. Spotts,and D. D. Davis. The influence of soil
zinc on nodulation, mycorrhizae, and ozone-sensitivity of pinto
bean. Phytopathology 65:645-647, 1975.
11-215
-------
351a. Mellanby, K., Ed. (Issue devoted to effects of pollutants on plants.)
Environ. Pollut. 9(2)85:155, 1975.
352. Menser, H. A., Jr. The Effects of Ozone and Controlled Environment Factors
on Four Varieties of Tobacco, Nicotiana tabacum L. Ph.D. Thesis.
College Park: University of Maryland, 1963. 146 pp.
353. Menser, H. A. Response of plants to air pollutants. III. A relation
between ascorbic acid levels and ozone susceptibility of light-
preconditioned tobacco plants. Plant Physiol. 39:564-567, 1964.
354. Menser, H. A., Jr. Response to ozone of five flue-cured tobacco varieties.
Tobacco 162:32-33, 1966.
11-216
-------
355. Menser, H. A., Jr. Effects of air pollution on tobacco cultivars grown
in several states. Tobacco 169:20-25, 1969. (UNVERIFIED)
356. Menser, H. A., and J. F. Chaplin. Air pollution: Effects on the phenol
and alkaloid content of cured tobacco leaves. Tobacco 169:73-74,
1969. (UNVERIFIED)
357. Menser, H. A., and H. E. Heggestad. Ozone and sulfur dioxide synergism:
Injury to tobacco plants. Science 153:424-425, 1966.
358. Menser, H. A., and G. H. Hodges. Tolerance to ozone of flue-cured tobacco
cultivars in field and fumigation chambers tests. Tobacco 169:
19-22, 1969. (UNVERIFIED)
359. Menser, H. A., and G. H. Hodges. Effects of air pollutants on burley
tobacco cultivars. Agron. J. 62:265-269, 1970.
360. Menser, H. A., and 0. E. Street. Effects of air pollution, nitrogen levels,
supplemental irrigation, and plant spacing on weather fleck and leaf
losses of Maryland tobacco. Tobacco 155:192-196, 1962. (UNVERIFIED)
361. Menser, H. A., H. E. Heggestad, and 0. E. Street. Response of plants to
air pollutants. II. Effects of ozone concentration and leaf matur-
ity on injury to Nicotiana tabacum. Phytopathology 53:1304-1308, 1963.
362. Menser, H." A. , G> H.' Hodges, and C.' G." McRee. Effects of air pollution on
Maryland (Type 32) tobacco. J. Environ. Qual. 2:253-258, 1973.
363. Menser, H. A., H. E. Heggestad, 0. E. Street, and R. N. Jeffrey. Response
of plants to air pollutants. I. Effects of ozone on tobacco plants
preconditioned by light and temperature. Plant Physiol. 38:605-609,
1963.
364. Middleton, J. T. Response of plants to air pollution. J. Air Pollut.
Control Assoc. 6:7-9, 1956.
11-217
-------
365. Middleton, J. T. Photochemical air pollution damage to plants. Ann. Rev.
Plant Physiol. 12:431-448, 1961.
366. Middleton, J. T. , and A. 0. Paulus. The identification and distribution
of air pollutants through plant response. A.M.A. Arch. Ind. Health
14:526-532, 1956.
367. Middleton, J.'T,, E. F." Darley, and R." P. Brewer. Damage to vegetation from
polluted atmospheres. J7 Air Pollut. Control Assoc. 8:9-15, 1958.
368. Middleton, J. T. , J. B. Kendrick, Jr., and E. F. Darley. Air-borne oxidants
as plant-damaging agents, pp. 191-198. In Proceedings of the Third
National Air Pollution Symposium, Pasadena, California, 1955. Los
Angeles: National Air Pollution Symposium, 1955.
369. Middleton, J. T., J. B. Kendrick, Jr., and H. W. Schwalm. Injury to
herbaceous plants by smog or air pollution. Plant Dis. Rep. 34:
245-252, 1950.
370. Millecan, A. A. A Survey and Assessment of Air Pollution Damage to Califor-
nia Vegetation in 1970. Sacramento: California Department of Agricul-
ture, 1971. (UNVERIFIED)
371. Miller, P. M., and S. Rich. Ozone damage on apples. Plant Dis. Rep. 52:
730-731, 1968.
372. Miller, P. R. Relationship of Ozone to Suppression of Photosynthesis and
the Cause of the Chlorotic Decline of Ponderosa Pine. Ph.D. Thesis.
Berkeley: University of California, 1965. 129 pp.
373. Miller, P. R. Susceptibility to ozone of selected western conifers.
Paper Presented at Second International Congress on Plant Pathology,
Minneapolis, 1973. (abstract) (UNVERIFIED)
374. Miller, P. R., and L. S. Evans. Histopathology of oxidant injury and win-
ter fleck injury on needles of Western pines. Phytopathology 64:801-
806, 1974.
11-218
-------
375. Miller, P. R., and A. A. Millecan. Extent o£ oxidant air pollution damage •
to some pines and other conifers in California. Plant Dis. Rep. 55:
555-559, 1971.
Delete 376
Delete 377
378. Miller, P". R., F.'W. Cobb, Jr., and E. 2avarin. Photochemical oxidant injury
and bark beetle (Coleoptera: Solytidae) infestation of ponderosa pine.
IIlT Effect of injury upon oleoresin composition, phloem carbohydrates,
and phloem pH. Hilgardia 39:135-140, 1968.
379. Miller, P. R., J. R. Parmeter, Jr., B. H. Flick, and C. W. Martinez. Ozone
dosage response of ponderosa pine seedlings. J. Air Pollut. Control
Assoc. 19:435-438, 1969.
380. Miller, P. R., J. R. Parmeter, 0. C. Taylor, and E. A. Cardiff. Oaone
injury to the foliage of Pinus ponderosa. Phytopathology 53:1072-
1976, 1963.
Delete 381
382. Miller, V. I., R. K. Howell, and B. E. Caldwell. Relative sensitivity of
soybean genotypes to ozone and sulfur dioxide. J. Environ. Qual. 3:
35-37, 1974.
383. Mohr, H. Lectures on Photomorphogenesis. New York: Springer-Verlag, 1972.
237 pp.
384. Moyer, J., H. Cole, Jr., and N. L. Lacasse. Reduction of ozone injury on Poa
annua by benomyl and thiophanate. Plant Dis. Reptr. 58:41-44, 1974.
385. Moyer, J. W., and S. H. Smith. Oxidant injury reduction on tobacco induced
by tobacco etch virus infection. Environ. Pollut. 9:103-106, 1975.
11-219
-------
386. Moyer, J. W. , H. Cole, Jr., and N. 1. Lacasse. Suppression of naturally
occurring oxidant injury on azalea plants by drench or foliar spray
treatment with benzimidazole or oxathin compounds. Plant. Dis. Rep.
58:136-138, 1974.
387. Mudd, J. B. Enzyme inactivation by peroxyacetyl nitrate. Arch. Biochem.
Biophys. 102:59-65, 1963.
388. Mudd, J. B. Reaction of peroxyacetyl nitrate with glutathione. J. Biol.
Chem. 241:4077-4080, 1966.
389. Mudd, J. B., and W. M. Dugger, Jr. The oxidation of reduced pyridine
nucleotides by peroxyacyl nitrates. Arch. Biochem. Biophys. 102:
52-58, 1963.
390. Mudd, J. B., and T. E. Kozlowski, Eds. Responses of Plants to Air Pollut-
ants. New York: Academic Press, 1975. 383 pp. (UNVERIFIED)
391. Mudd, J. B., R. Leavitt, and W. A. Kersey. Reaction of peroxyacetyl nitrate
with sulfhydryl groups of proteins. J. Biol. Chem. 241:4081-4085, 1966
392. Mudd, J. B., F. leh, and T. T. McManus. Reaction of ozone with nicotinamide
and its derivatives. Arch. Biochem. Biophys. 161:408-419, 1974.
393. Mudd, J. B., T. T. McManus, and A. Ongun. Inhibition of lipid metabolism
in chloroplasts by ozone, pp. 256-260. In H. M. Englund and W. T.
Beery, Eds. Proceedings of the Second International Clean Air
Congress. Held at Washington, D. C., December 6-11, 1970. New
York: Academic Press, 1971.
394. Mudd, J. R., R. Leavitt, A. Ongun, and T. T. McManus. Reaction of ozone with
amino acids and proteins. Atmos. Environ. 3:6'69-681, 1969.
11-220
-------
395. Mudd, J. B., T. T. McManus, A. Ongtm, and T. E. McCullough. Inhibition
of glycolipid biosynthesis in chloroplasts by ozone and sulfhydryl
reagents. Plant Physiol. 48:335-339, 1971.
396. Mukammal, E. 1. Ozone as a cause of tobacco injury. Agric. Meteorol. 2:
145-165, 1965.
397. Mumford, R. A., H. Lipke, D. A. Laufer, and W. A. Feder. Ozone-induced
changes in corn pollen. Environ. Sci. Technol. 6:427-430, 1972.
398. Naegele, H. A., Ed. Air Pollution Damage to Vegetation. Advances in Chemis-
try Series 122. Washington, D. C.: American Chemical Society, 1973.
137 pp.
399. Naegele, J. A., W. A. Feder, and C. J. Brandt. Assessment of Air Pollution
Damage to Vegetation in New England: July, 1971-July, 1972. Final
Report, Suburban Experiment Station, University of Massachusetts,
Amherst. (Contract No. 68-02-0084)
400. Nakamura, H., and S. Maisunaka. Indicator plants for air pollutants. 1.
Susceptibility of morning glory to photochemical oxidants: Varietal
difference and effect of environmental factors. Proc. Crop Sci. Soc.
Jap. 43:517-522, 1974. (in Japanese, summary in English)
401. U. S. Department of Health, Education, and Welfare, public Health Service.
National Air Pollution Control Administration. Effects of photochem-
ical oxidants on vegetation and certain microorganisms, pp. 6-1--6-23.
In Air Quality Criteria for Photochemical Oxidants. NAPCA Publ. AP-63.
Washington, D. C.: U. S. Government Printing Office, 1970.
402. Neil, L. J., D. P.'Ormrod, and G. Hofstra. Ozone stimulation of tomato stem
elongation. HortScience 8:488-489, 1973.
11-221
-------
403. Nicksic, S. W. , J. Harkins, and P. K. Mueller. Some analyses for PAN and
studies of its structure. Atmos. Environ. 1:11-18, 1967.
Delete 404
405. Nobel, P. S., and C. T. Wang. Ozone increases the permeability of isolated
pea chloroplasts. Arch. Biochem. Biophys. 157:388-394, 1973.
406. Noble, W. M. The relation of plant damage to fuel composition. Paper
Presented at the Conference on Motor Vehicle Exhaust Emissions and
Their Effects, Dec. 5, 1961, University of California, Los Angeles,
11 pp.
407. Noble, W. M., and L. A. Wright. Air pollution with relation to agronomic
crops: II. A bio-assay approach to the study of air pollution.
Agron. J. 50:551-553, 1958.
408. Noble, W. M. , W. Peele, L. Wright, and P. P. Mader. A Comparison of the
Smog Forming Properties of the Exhaust Gases from Two Types of Motor
Fuels Using Plants as Indicators. Los Angeles County Air Pollution
Control District, 1958. 10 pp.
Delete 409.
410. Nouchi, I., T. Odaira, T. Sawada, K. Oguchi, and T. Komeiji. Plant ozone
injury symptoms. Taiki Osen Kenkyu (J. Jap. Soc. Air Pollut.) 8:
113-119, 1973. (in Japanese)
411. Oertli, J. J. Effect of salinity on susceptibility of sunflower plants
to smog. Soil Sci. 87:249-251, 1959.
412. Ogata, G. , and E. V. Maas. Interactive effects of salinity and ozone on
growth and yield of garden beet. J. Environ. Qual. 2:518-520, 1973.
413. Ordin, L., and B. Propst. Effect of photochemically produced oxidants on
growth of avena coleoptile sections. Plant Physiol. 36:326-330, 1961.
11-222
-------
414. Ordin, L., M. J. Garber, and J. I. Kindinger. Effect of 2,4-dichlorophen-
oxyacetic acid on growth and on ^-glucan synthetases of peroxyacetyl
nitrate pretreated Avena coleoptile sections. Physiol. Plant. 26:
17-23, 1972.
415. Ormrod, D. P., and N. 0. Adedipe. Protecting horticultural plants from
atmospheric pollutants: A review. HortScience 9:108-111, 1974.
416. Ormrod, D. P., N. 0. Adedipe, and G. Hofstra. Responses of cucumber,
onion, and potato cultivars to ozone. Can. J. Plant Sci. 51:283-
288, 1971.
417. Ormrod, D. P., N. 0. Adedipe, and G. Hofstra. Ozone effects on growth of
radish plants as influenced by nitrogen and phosphorus nitrition and
by temperature. Plant Soil 39:437-439, 1973.
418. Oshima, R. J. Effect of ozone on a commercial sweet corn variety. Plant
Dis. Rep. 57:719-723, 1973.
419. Oshima, R. J. Development of a System for Evaluating and Reporting
Economic Crop Losses Caused by Air Pollution in California. I.
Quality Study. Sacramento: California Department of Food and
Agriculture, 1973.
420. Oshima, R. J. Development of a System for Evaluating and Reporting
Economic Crop Losses Caused by Air Pollution in California. II.
Yield Study. Sacramento: California Department of Food and
Agriculture, 1974.
421. Oshima, R. J. A viable system o£ biological indicators for monitoring air
pollutants. J.' Air Pollut. Control Assoc. 24:576-578, 1974.
Oshima, R., 0. C. Taylor, and E. A. Cardiff, severe air pollution episode
in south coast basin. Calif. Agric. 28(2):12-13, 1974.
11-223
-------
423. Oshima, R. J. , 0. C. Taylor, P. K. Braegelmann, and D. W. Baldwin. Effect
of ozone on a commercial variety of tomato. J. Environ. Qual. 4:463-
464, 1975.
424. Otto, H. W. , and R. H. Daines. Plant injury by air pollutants: Influ-
ence of humidity on stomatal apertures and plant response to ozone.
Science 163:1209-1210, 1969.
425. Parmeter, J. R., Jr., and P. R. Miller. Studies relating to the cause of
decline and death of Ponderosa pine in southern California. Plant
Dis. Rep. 52:707-711, 1968.
426. Parmeter, J. R., Jr., R. V. Bega, and T. Neff. A chlorotic decline of
ponderosa pine in southern California. Plant Dis. Rep, 46:269-273,
1962.
427. Peak, M. J., and W. I. Belser. Some effects of the air pollutant, peroxy-
acetyl nitrate, upon deoxyribonucleic acid and upon nucleic acid bases,
Atmos. Environ. 3:385-397, 1969.
428. Pearson, R. G. , D. B. Drummond, W. D. Mcllveen, and S. N. Linzon. PAN-
type injury to tomato crops in southwestern Ontario. Plant Dis.
Rep. 58:1105-1108, 1974.
429. Pell, E. J. 1972 Survey and Assessment of Air Pollution Damage to Vegeta-
tion in New Jersey. EPA-R5-73-022. New Brunswick: Rutgers, The
State University Department of Plant Biology, 1973. 44 pp.
Delete 430
431. Pell. E. L. , and E. Brennan. Changes in respiration, photosynthesis,
adenosine 5-triphosphate, and total adenylate content of ozonated
pinto bean foliage as they relate to symptom expression. Plant
Physiol. 51:378-381, 1973.
11-224
-------
432. Pell, E. J., and E. Brennan. Economic impact of air pollution on vegeta-
tion in New Jersey and an interpretation of its annual variability.
Environ. Pollut. 8:23-33, 1975.
433. Pellissier, M. Effect of Foliar and Root Treatments of Benomyl in Reduc-
ing Ozone Injury to Pinto Bean and Cucumber. M. S. Thesis. Center
for Air Environment Studies Publ. #213-71. University Park:
Pennsylvania State University, 1971. 29 pp. (UNVERIFIED)
434. Pellissier, M., N. I. Lacasse, and H. Cole, Jr. Effectiveness of benomyl
and benomyl-folicote treatments in reducing ozone injury to pinto
beans. J. Air Pollut. Control Assoc. 22:722-725, 1972.
435. Pellissier, M., N. L.'Lacasse, C. D. Ercegovich, and H. Cole. Jr. Effects 6f
hydrocarbon wax emulsion sprays in reducing visible ozone injury to
Phaseolus vulgaris 'Pinto III1. Plant Dis. Reptr. 56:6-9, 1972.
436, Penkett, S. A., F. J. Sandalls, and J. E. Lovelock. Observations of per-
oxyacetyl nitrate (PAN) in air in southern England. Atmos. Environ.
9:139-140, 1975.
437. Perchorowicz, J. T., and I. P. Ting. Ozone effects on plant cell permea-
bility. Amer. J. Bot. 61:787-793, 1974.
Delete 438
Delete 439
440. Povilaitis, B. Gene effects for tolerance to weather fleck in tobacco.
Can. J. Genet. Cytol. 9:327-334, 1967.
441. Price, H., and M. Treshow. Effects of ozone on the growth and reproduction
of grasses, pp. 275-280. In Proceedings of the International Air
Pollution Conference, Melbourne, Australia, 1970 or 1972. (UNVERIFIED)
11-225
-------
442. Rabotnova, I. 1., V. S. Somov, T. S. Bobkova, I. V. Zlochevskaya, L. N.
Chekunova, I. F. Knyazeva, and S. I. Belen'kiy. The relationship
between the toxic action of ozone on yeast and certain components and
medium pH. Vestnik Moskovskogo Uniiver. Biol. Pochvored. 6(5):
47-51, 1971. (in Russian)
443. Reinert, R. A. Agricultural Research Service, Raleigh, N. C., Personal
Communication, 1976.
Delete 444
445. Reinert, R. A. Monitoring, detecting, and effects of air pollutants on
horticultural crops. Sensitivity of genera and species. HortScience
10:495-500, 1975.
446. Reinert, R. A., and H. W. Spurr, Jr. Differential effect of fungicides
on ozone injury and brown spot disease of tobacco. J. Environ.
Qual. 1:450-452, 1972.
447. Reinert, R. A., A. S. Heagle, and W. W. Heck. Plant response to pollu-
tant combinations, pp. 159-178. In B. Mudd and T. E. Kozlowski, Eds.
Responses of Plants to Air Pollution. New York: Academic Press, _
1975. (UNVERIFIED)
448. Reinert, R. A., D. T. Tingey, and H. B. Carter. Sensitivity to tomato
cultivars to ozone. J. Amer. Soc. Hort. Sci. 97:149-151, 1972.
449. Reinert, R. A., D. T. Tingey, and H. B. Carter. Ozone induced foliar
injury in lettuce and radish cultivars. J. Amer. Soc. Hort. Sci.
_ 97:711-714, 1972.
450. Reinert, R. A., D. T. Tingey, and C. E. Koons. The early growth of soy-
bean as influenced by ozone stress. Agron. Abstr. 63:148, 1971. (UNVER
11-226
-------
451. Reinert, R. A., A. S. Heagle, J. R. Miller, and W. R. Geckeler. Field
studies of air pollution injury to vegetation in Cincinnati, Ohio.
Plant Dis. Rep. 54:8-11, 1970.
452. Rcsh, H. M., and V. C. Runeckles, Effects of ozone on bean rust Uramyces
phaseoli. Can. J.'Bot. 51:725-727, 1973.
453. Rich, S. Ozone damage to plants. Ann. Rev. Phytopath. 2:253-266, 1964.
454. Rich, S., and G, S, Taylor. Antiozonants to protect plants from ozone
damage. Science 132:150-151, 1960.
455. Rich, S., and H. Tomlinson. Effects of ozone on conidiophores and conidia of
Alternaria_ solani. Phytopathology 58:444-446, 1968.
Delete 456
457. Rich, S., and N. C. Turner. Importance of moisture on stomatal behavior of
plants subjected to ozone. J. Air Pollut. Control Assoc. 22:718-721,
1972.
458. Rich, S., R. Ames, and J. W. Zukel. 1,4-oxathin derivatives protect plants
against ozone. Plant Dis. Rep, 58:162-164, 1974.
459. Rich, S., G. S. Taylor, and M. Tomlinson. Crop damaging periods of ambient
ozone in Connecticut. Plant Dis. Rep. 53:960-973, 1969.
460. Rich, S., P. E. Waggoner, and H. Tomlinson. Ozone uptake by bean leaves.
Science 169:79-80, 1970.
461. Richards, B. L., J. T. Middleton, and W. B. Hewitt. Air pollution with
relation to agronomic crops: V. Oxidant stipple of grape. Agron.
J. 50:559-561, 1958.
462. Richards, B. L., Sr., 0. C. Taylor, and G. F. Edmunds, Jr. Ozone needle
mottle of pines of southern California. J. Air Pollut. Control Assoc.
18:73-77, 1968.
11-227
-------
463. Ridley, J. D., and E. T. Sims, Jr. Preliminary Investigations on the Use
of Ozone to Extend the Shelf-life and Maintain the Market Quality of
Peaches and Strawberries. South Carolina Agricultural Experiment
Station Research Series No. 70. Clemson: Clemson University, 1966.
22 pp.
464. Ripaldi, C. P., and E. Brennan. Effect of ozone on phosphorous levels o£
pinto bean stems and foliage. Phytopathology 63:206, 1973. (abstract)
465. Roehm, J. H. , J. G. Had'ley, and D. B. Merizel. Aritidxidarits vs lurig disease.
Arch. Intern. Med. 128:88-93, 1971.
466. Rogers, H. H., Jr. Uptake of Nitrogen Dioxide by Selected Plant Species.
Ph.D. Thesis. Chapel Hill: University of North Carolina, 1975.
140 pp.
467. Rosen, P. M., and V. C. Runeckles. Adaptation to ozone. Plant Physiol.
Ann Suppl. 1974:31. (abstract)
Delete 468
469. Rufner, R., F. H. Witham, and H. Cole, Jr. Ultrastructure of chloroplasts
of Phaseolus vulgaris leaves treated with benomyl and ozone. Phyto-
pathology 65:345-349, 1975.
470. Runeckles, V. C., and H. M. Resh. The assessment o£ chronic onzone injury
to leaves by reflectance spectr'ophotometry. Atmos. Environ. 9:447-
452, 1975.
Delete 471
472. Sand, S. A. What the tobacco plant does to ozone. Frontiers Plant Sci.
12(l):4-5, 8, 1959.
Delete 473
11-228
-------
Schuette, 1. R. Response of the Primary Infection Process of Erysiphe
graminis F. sp. hordei to Ozone. Ph.D. Thesis. Salt Lake City:
University of Utah, 1971. 76 pp.
475. Scott, D. H. Air Pollution Injury to Plant Live. Washington, D. C.:
National Landscape Association Guide, 1973. 12 pp.
476. Scott, D. B. M., and E. C, Lesher. Effect of ozone on survival and per-
meability of Escherichia coli. J. Bacteriol. 85:567-576, 1963.
477. Sechler, D., and D. R. Davis. Ozone toxicity in small grain. Plant Dis.
Rep. 48:919-922, 1964.
Delete 478
479. Seem, R.' C., M. Cole, Jr., and N. L. Lacasse. Suppression of ozone injury to
Phaseolus vulgaris "Pinto III1 with triarimol and its monochlorophenyl
cyclohexyl analogue. Plant Dis. Rep. 56:386-390, 1972.
Delete 480
481. Shannon, J. G., and C. 1. Mulchi. Ozone damage to wheat varieties at
anthesis. Crop Sci. 14:335-337, 1974.
482. Sharma, G. K., and J. Butler. Leaf cuticular variations in Trifolium
repens L. as indicators of environmental pollution. Environ.
Pollut. 5:287-293, 1973.
483. Shaulis, N. J., W. J. Kender, C. Pratt, and W. A. Sinclair. Evidence for
injury by ozone in New York vineyards. HortScience 7:570-572, 1972.
484. Shinohara, T. , Y. Yamamoto, and H. Kitano. The relation between ozone
treatment and the injury in tobacco. Proc. Crop Sci. Soc. Jap.
42:412-417, 1973.
485. Shinohara, T., S. Kuroda, T. Kitamura, and K. Kunisawa. Studies on weather
fleck on tobacco leaves. VI. Effects of temperature on the fleck
injury induced by air-borne oxidants. Bull. Okayma Tob. Exp. Stat.
33(Special #2):51-54, 1973. (in Japanese, summary in English)
11-229
-------
486. Shinohara, T. , Y. Yamamoto, Y. Kitano, and M. Fukuda. Effects of tempera-
ture on ozone injury to tobacco. Proc. Crop Sci. Soc. Jap. 42:418-
421, 1973.
487. Shinohara, T., Y. Yamamoto, H. Kitano, and M. Fukuda. Interactions of
light and ozone injury in tobacco. Proc. Crop. Sci. Soc. Jap. 43:
433-438, 1974.
488. Sinclair, M. G. The Effects of Ozone on TVo Varieties of Tobacco Pollen
and on the Conidia of the Fungus Monilinia fructicola. M. S. Thesis.
Newark: University of Delaware, 1969. 59 pp.
489. Smock, R. M., and R. D. Watson. Ozone in apple storage. Refrig. Eng. 42:
97-101, 1941.
490. Spalding, D. H. Appearance and Decay of Strawberries, Peaches, and Lettuce
Treated with Ozone. Marketing Research Report No. 756. Agriculture
Research Service, U. S. Department of Agriculture. Washington, D. C. :
U. S. Government Printing Office, 1966. 11 pp.
491. Sparrow, A. H., and I. A. Schairer. Mutagenic response of tradescantia
to treatment with X-rays, EMS, DBE, ozone, S02, NoO and several
insecticides. Amer. Envir. Mutagen Soc. 26:445, 1974.
492. Spotts, R. A., F. L. Lukezic, and R. H. Hamilton. The effect of benzimida-
zole on some membrane properties of ozonated pinto bean. Phytopath-
ology 65:39-45, 1975.
493. Spotts, R. A., F. L. Lukezic, and N. L. Lacasse. The effect of benzimida-
zole, cholestrol, and a steroid inhibitor on leaf sterols and ozone
resistance of bean. Phytopathology 65:45-49, 1975.
11-230
-------
494. Stark, R. W., P. R. Miller, F. W. Cobb, Jr., D. I. Wood, and J. R. Parmeter,
Jr. Photochemical oxidant injury and bark beetle (Coleoptera:
Scolytidae) infestation of Ponderosa pine. I. Incidence of bark
beetle infestation in injured trees. Hilgardia 39:121-126, 1968.
495. Starkey, T. D. The Influence of Peroxyacetyl Nitrate on Bean (Phaseolus
vulgaris L) Subjected to Post-Exposure Water Stress. Center for Air
Environment Studies Publ. #400-75. University Park: Pennsylvania
State University, 1975. 45 pp. (UNVERIFIED)
496. Stephens, E. R. , E. F. Darley, 0. C. Taylor, and W. E. Scott. Photochemical
reaction products in air pollution. Int. J. Air Water Pollut. 4:79-
100, 1961.
497. Stolzy, L. H. , 0. C. Taylor, W. M. Dugger, Jr., and J. D. Mersereau. Phys-
iological changes in and ozone susceptibility of the tomato plant
after short periods of inadequate oxygen diffusion to the roots. Proc.
Soil Sci. Soc. Amer. 28:305-308, 1964.
498. Stolzy, L. H., 0. C. Taylor, J, Letey, and T. E. Szuszkiewicz. Influence of
soil-oxygen diffusion rates on susceptibility of tomato plants to air-
borne oxidants. Soil Sci. 91:151-155, 1961.
499. Swanson, E. S., W. W. Thomson, and J. B. Mudd. The effect of ozone on
leaf cell membranes. Can. J. Bot. 51:1213-1219, 1973.
500. Taylor, G. S. Ozone injury on Bel W-3 tobacco controlled by at least two
genes. Phytopathology 58:1069, 1968. (abstract)
501. Taylor, G. S. Ozone injury on tobacco seedlings can predict susceptibility
in the field. Phytopathology 64:1047-1048, 1974.
502. Taylor, G. S., and S, Rich. Antiozonant-treated cloth protects tobacco from
fleck. Science 135:928, 1962.
11-231
-------
503. Taylor, G. S. , and S. Rich. Ozone injury to tobacc£«4ft- the field influ-
enced by soil treatments with benomyl and carbonin. Phytopathology
64:814-817, 1974.
504. Taylor, G. S., H. G. DeRoo, and P. E. Waggoner. Moisture and fleck of
tobacco. Tobacco 150:22-28, 1960. (UNVERIFIED)
505. Taylor, 0. C. Effects of oxidant air pollutants. J. Oeeup. Mod. 10:485-499
1968.
506. Taylor, 0. C. Importance of peroxyacetyl nitrate (PAN) as a phytotoxic air
pollutant. J. Air. Pollut. Control Assoc. 19:347-351, 1969.
507. Oxidant Air Pollutant Effects on a Western Coniferous Forest Ecosystem.
Rask C Report: Study Site Selection and Verification Data on
Pollutants and Species. Riverside: University of California, State-
wide Air Pollution Research Center, 1973. (UNVERIFIED)
Delete 508
Delete 509
510. Taylor, 0. C., and D. C. Maclean. Nitrogen Oxides and the peroxyacyl rtitrati
pp. E1-E14. In J. S. Jacobson and A. C. Hill, Eds. Recognition of Air
Pollution Injury to Vegetation: A Pictorial Atlas. Pittsburgh: Air
Pollution Control Association, 1970.
Delete 511
512. Taylor, 0. C., E. A. Cardiff, J. D. Mersereau, and J. T. Middleton. Effect
of air-borne reaction products of ozone and 1-N-hexene vapor (synthetic
smog) on growth of avocado seedlings. Proc. Amer. Soc. Hort. Sci.
_^ 71:320-325, 1958.
513. Taylor, 0. C., W. M. Dugger, Jr., E. A. Cardiff, and E. F. Darley. Inter-
action of light and atmospheric photochemical products ('smog') within
plants. Nature 192:814-816, 1961.
11-232
-------
Delete
515. Thomas, M. D. Effects of air pollution on plants, pp. 233-278. In Air
Pollution. World Health Organization Monograph Series No. 46. New
York: Columbia University Press, 1961.
516. Thomas, M. D. Photochemical Smog. Air Quality Monograph #69-6. New York:
American Petroleum Institute, 1969. 40 pp.
517. Thomas, M. D. , R. H. Hendricks, and G. R. Hill. Some impurities in the
air and their effects on plants, pp. 41-47. In U. S. Technical
Conference on Air Pollution. New York: McGraw-Hill Book Co., 1950.
(UNVERIFIED)
518. Thompson, C. R. University of California, Riverside. Personal Communications,
519. Thompson, C. R., and G. Kats. Antioxidants reduce grape yield reductions
from photochemical smog. Calif. Agric. 24(9):12-13, 1970.
520. Thompson, C. R., and G. Kats. Effects of ambient concentrations of per-
oxyacetyl nitrate on navel orange trees. Environ. Sci. Technol. 9:
35-38, 1975.
521. Thompson, C. R., and 0. C. Taylor. Effects o£ air pollutants on growth leaf
drop, fruit drop, and yield of citrus trees. Environ. Sci. Technol. 3;
934-940, 1969.
522. Thompson, C. R., E. Hensel, and G. Katz. Effects of photochemical air
pollutants on Zinfandel grapes. HortScience 4:222-224, 1969. (UNVER.)
Delete 523
524. Thomson, W. W., W. M. Dugger, Jr., and R. L. Palmer. Effects of ozone on the
fine structure of the palisade parenchyma cells of bean leaves. Can. J.
Bot. 44:1677-1682, 1966.
525. Thomson, W. W., ft. M. Dugger, Jr., and R.' L. Palmer. Effects of peroxyacetyl
nitrate on ultrastructure of chloroplasts. Bot. Gaz. 126:66-72, 1965.
11-233
-------
Delete 526
527. Thorne, L., and G.'P. Hanson. species differences in rates o£ vegetal 6z6ne
absorption. Environ. Pollut. 3:303-312, 1972.
528. Teige, B., T. T. McManus, and J. 8. Mudd. Reaction of ozone with phosphathyi-
cholinc kiposomes and the lytic effect of products on red blood cells.
Chem. Phys. Lipids 12:153-171, 1974.
529. Ting, I. P., and W. M. Dugger, Jr. Factors affecting ozone sensitivity
and susceptibility of cotton plants. J. Air Pollut. Control Assoc.
18:810-813, 1968.
530. Ting, 1. P., and W. M. Dugger. Ozone resistance in tobacco plants: A
possible relationship to water balance. Atmos. Environ. 5:147-150,
1971.
531. Ting, I. P., and S. K. Mukerji. leaf ontogeny as a factor in susceptibil-
ity to ozone: Amino acid and carbohydrate changes during expansion.
Amer. J. Bot. 58:497-504, 1971.
Delete 532
533. Ting, I. P., J. Perchorowicz, and 1. Evans. Effects of ozone on plant cell
membrane permeability, pp. 8-21. In M. Dugger, Ed. Air Pollution
Effects on Plant Growth. ACS Sympsoium Series 3. Washington, D. C.:
American Chemical Society, 1974. (UNVERIFIED")
534. Tingey, D. T. Ozone induced alteration in the metabolite pools and enzyme
activities of plants, pp. 40-57. In M. Dugger, Ed. Air Pollution
Effects on Plant Growth. ACS Symposium Series 3. Washington, D. C.:
American Chemical Society, 1974. (UNVERIFIED)
Delete 535
536. Tingey, D. T., and U. Blum. Effects of ozone on soybean nodules. J.
Environ. Qual. 2:341-342, 1973.
11-234
-------
Delete 537
538. Tingey, D. T., and R. A. Reinert. The effect of ozone and sulfur dioxide
singly and in combination on plant growth. Environ. Pollut. 9:117-
126, 1975.
539. Tingey, D. T. , and C. Standley. Factors influencing ethylene evolution
from ozone stressed plant. Plant Physiol. 56(Suppl.):5 , 1975. (abstract)
540. Tingey, D. T. , J. A. Dunning, and G. M. Jividen. Radish root growth
reduced by acute ozone exposures, pp. A154-A156. In Proceedings of
11
the Third International Clean Air Congress. Held at Dusseldorf,
Federal Republic of Germany, October 8-12, 1973. Dusseldorf: Verlag:
des Vereins Deutscher Ingenieur, 1973.
Delete 541
542. Tingey, D. T., R. C. Fites, and C. Wickliff. Foliar sensitivity of soy-
beans to ozone as related to several leaf parameters. Environ. Pollut.
4:183-192, 1973.
543. Tingey, D. T., R/ C. Fites, and C. Wickliff. Ozdrte alteration of nitrate
reduction in soybean. Physiol. Plant. 29:33-38, 1973.
544. Tingey, D. T., R. C. Fites, and C. Wickliff. Activity changes in selected
enzymes from soybean leaves following ozone exposure. Physiol. Plant.
33:316-320, 1975.
545. Tingey, D. T., W. U. Heck, and R. A. Reinert. Effect of low concentrations
of ozone and sulfur dioxide on foliage, growth and yield of radish. J.
Amer. Soc. Hort. Sci. 96:369-371, 1971.
546. Tingey, D. T., R. A. Reinert, and H. B. Carter. Soybean cultivars: Acute
foliar response to ozone. Crop Sci. 12:368-370, 1962.
547. Tingey, D. T. , R. A. Reinert, J. A. Dunning, and W. W. Heck. Foliar injury
responses of eleven plant species to ozone/sulfur dioxide mistures.
Atmos. Environ. 7:201-208, 1973.
11-235
-------
548. Tingey, D. T., R. A, Reinert, C. Wickliff, and W. W. Heck. Chronic ozone or
sulfur dioxide exposures or both, affect the early vegetative growth of
soybeans. Can. J".' Plant Sci. 53:875-879, 1973.
Delete 549
550. Todd, G, W. Effect of low concentrations of ozone on the enzymes catalase,
peroxidase, papain and urease. Physiol. Plant. 11:457-463, 1958.
551. Todd, G. W. Effect of ozone and ozonated 1-hexene on respiration and
photosynthesis of leaves. Plant Physiol. 33:416-420, 1958.
552. Todd, G. W., and W. N. Arnold. An evaluation of methods used to determine
injury to plant leaves by air pollutants. Bot. Gaz. 123:151-154, 1961.
553. Todd, G. W., and M. J. Garber. Some effects of air pollutants on the
growth and productivity of plants. Bot. Gaz. 120:75-80, 1958.
554. Todd, G. W., and B. Propst. Changes in transpiration and photosynthetic
rates of various leaves during treatment with ozonated hexene or
ozone gas. Physiol. Plant. 16:57-65, 1963.
Delete 555
556. Tomlinson, H., and S. Rich. Metabolic changes in free amino acids of bean
leaves exposed to ozone. Phytopathology 57:972-974, 1967.
557. Tomlinson, H., and S. Rich. The ozone resistance of leaves as related to
their sulfhydryl and adenosine triphosphate content. Phytopathology
58:808-810, 1968.
558. Tomlinson, H., and S. Rich. Relating lipid content and fatty acid synthe-
sis to ozone injury of tobacco leaves. Phytopathology 59:1284-1286,
1969.
559. Tomlirtson, M., and Sk Rich. Lipid peroxidation, a result of injury in bean
leaves exposed to ozone. Phytopathology 60:1531-1532, 1970.
11-236
-------
560. Tomlinson, H. , arid §.' Rich. Effect of. ozone on Sterols and sterol derivatives
in bean leaves. Phytopathology 61:1404-1405, 1971.
561. Tomlinson, H., and S. Rich. Anti-senescent compounds reduce injury and
steroid changes in ozonated leaves and their chloroplasts. Phyto-
pathology 63:903-906, 1973.
Delete 562
563. Townsend, A. M. Sorption of ozone by nine shade tree species. Proc. Amer.
Soc. Hort. Sci. 99:206-208, 1974.
564. Townsend, A. M. , and L. S. Dochinger. Relationship of seed source and
developmental stage to the ozone tolerance of Acer rubrum seedlings.
Atmos. Environ. 8:957-964, 1974.
565. Treshow, M. Evaluation of vegetation injury as an air pollution criterion.
J. Air Pollut. Control Assoc. 15:266-269, 1965.
566. Treshow, M. Environment and Plant Response. New York: McGraw-Hill Book Co.,
1970. 422 pp.
567. Treshow, M. Ozone damage to plants. Environ. Pollut. 1:155-16, 1970.
568. Treshow, M., and D. Stewart. Ozone sensitivity of plants in natural com-
munities. Biol. Conserv. 5:209-214, 1973.
569. Turner, M. C., S.' Rich, and P. E. Waggoner. Removal of ozone by soil. J.
Environ. Qual. 2:259-264, 1973.
570. Turner, N. C., P. E. Waggoner, and S. Rich. Removal of ozone from the
atmosphere by soil and vegetation. Nature 250:486-489, 1974.
571. Turri, E., and M. P. Benetti. La "contaminazione di fondo" dell' atomsfera
("smog") e sua influenza sulla vegetazione erbacea. Bol. Staz. Pat.
Veg. (Roma) 18:173-190, 1960.
11-237
-------
572. van Haut, H., and H. Stratmann. Experimentalle Untersuchungen liber die
Wirkung von Stickstoffdioxid auf Pflanzen. Schriftenr. Landesanst.
Immiss. Bodennutzungssch. Land. Nordrheim-Westfalen 7:50-70, 1967.
573. Vasiloff, G. N., and D. B. Drummond. The effectiveness of road dust as a
protective agent on buckwheat and pinto bean against sulfur dioxide
and ozone. Phytopathology 64:588, 1974. (abstract)
574. Verkroost, M. The effect of ozone on photosynthesis and respiration of
Scenedesmus obtusiusculus Chod., with a general discussion of effects
of air pollutants in plants. Meded. Landbouwhogesch. Wag. 74:1-78,
1974.
575. Walker, E. K. Chemical control of weather fleck in flue-cured tobacco.
Plant. Dis. Rep. 45:583-586, 1961.
Delete 576
577. Walker, E. K. , and L. S. Vickery. Influence of sprinkler irrigation on
the incidence of weather fleck on flue-cured tobacco in Ontario.
Can. J. Plant Sci. 41:281-287, 1961.
578. Walker, J. T., and J. C. Barlow. Response of indicator plants to ozone
levels in Georgia. Phytopathology 64:1122-1127, 1974.
579. Watson, R. D. Ozone as a Fungicide. Ph.D. Thesis. Ithaca, N. Y. :
Cornell University, 1942. 74 pp.
580. Weaver, G. M., and H. 0. Jackson. Relationship between bronzing in white
beans and phytotoxic levels of atmospheric ozone in Ontario. Can.
J. Plant Sci. 48:561-568, 1968.
581. Weber, D. The Effect of Ozone and/or Sulfur Dioxide on Selected Species
of Plant Parasites Nematodes. Ph.D. Thesis. Raleigh: North Carolina
State University, 1975.
11-238
-------
582. Weir, R. Worth Carolina State University, Raleigh. Personal Communica-
tion, 1975.
583. Wendschuh, P. H., H. Fuhr, J. S. Gaffney, and J. N. Pitts, Jr. Reaction of
peroxyactyl nitrate with amines. Chem. Commun. 1973:74-75.
584. Went, FV W. Air pollution. Sci. Amer. 192(5):63-70, 72, 1955.
585. Went, F. W. Plant damage due to air pollution and the use of plants as
indicators of air pollution. Air Pollut. Control Assoc. News 6:
3-6, 1958. (UNVERIFIED)
586. Wert, S. L. A system for using remote sensing techniques to detect and
evaluate air pollution effects on forest stands, pp. 1169-1178. In
Proceedings of the Sixth International Symposium on Remote Sensing
of the Environment. Vol. 2. Ann Arbor, University of Michigan, 1969.
587. Wert, S. L., P. R. Miller, and R. N. Larsh. Color photos detect smog in-
jury to forest trees. J. Forest. 68:536-539, 1970.
588. white, N. H. Observations on air-oxidant injuries on plants in the
Sydney metropolitan area. Paper #7 Presented at First Clean Air
Conference held at the University of New South Wales, 1962. 7 pp.
(UNVERIFIED)
589. Wilhour, R. G. The Influence of Ozone on White Ash. Center for Air Envir-
onment Studies Publ. #188-71. University Park: Pennsylvania State
University, 1971. 86 pp. (UNVERIFIED)
590. Wilkinson, T. G., and R. L. Barnes. Effects of ozone on 14C02 fixation
patterns in pine. Can. J. Bot. 51:1573-1578, 1973.
591. Winberry, L. K., and J. B. Mudd. S-acyl glutathione thioesterase of plant
tissue. Plant Physiol. 53:216-219, 1974.
11-239
-------
592. Wood, F. A., D. B. Drummond, R. G. Wilhour, and D. D. Davis. An'Exposure
Chamber for Studying the Effects of Air Pollutants on Plants. Agri-
cultural Experiment Station Progress Report No. 335. University Park:
Pennsylvania State University, 1973. 7 pp.
593. Wood, F. A., and D. B. Drummond. Response of eight cultivars of chrysan-
themum to peroxyactyl nitrate. Phytopathology 64:897-898, 1974.
b93a.Wood, F, A., and J. B. Coppolino. The influence of ozone on selected woody
ornamentals. Phytopathology 61:133, 1971. (abstract)
594. Wood, F. A., and J. B. Coppolino. Response of 11 hybrid poplar clones
to ozone. Phytopathology 62:501-502, 1972. (abstract)
595. Yamaga, M., K. Omori, K. Abe, and T. Tozawa. The effects of air pollut-
ants on vegetation. The effects of ozone on carbohydrase. Symp.
Jap. Soc. Air Pollut. Proc. 13:230, 1972. (in Japanese) (UNVER.)
596. Yarwood, C. E., and J. T. Middleton. Smog injury and rust infection.
Plant Physiol. 29:393-395, 1954.
597. Zobnina, V. P., and E. A. Morkovina. Effect of ozone on survival of
carotinoid strain of Mycobacterium carothenum and its white mutant
obtained with nitrosoguanidine. Microbiology 40:79-81, 1971.
11-240
-------
Chapter 12
ECOSYSTEMS
The effects of ozone and other photochemical oxidants on indivi-
dual species of green plants and microorganisms were discussed in detail
in Chapter 11. The purpose of this chapter is to examine the effects
of oxidant pollutant stress on both simple and complex communities of
organisms. The human population is an integral and dependent component
49
of these biotic communities, or ecosystems.
It is usually not possible to interpret the meaning of a
stable ecosystem for man's welfare in the terms of conventional economics,
for example, as a cost-benefit analysis. In the case of some natural
ecosystems, there may be only social and psychologic values to be
70
considered, which are only remotely related to monetary values through
79
the recreational opportunities that they offer. One of the most import-
ant justifications for the examination of the effects of oxidant stress
on an ecosystem is the concern that it will not revert to its prior
condition even after removal of the stress. For example, it has been
suggested that the arid lands of India are the result of defoliation and
elimination of vegetation, which induced local climatic changes that
were not conducive to the reestablishment of the original vegetation.
A natural ecosystem is a distinct association of plants and
animals with the physical environment that controls them. Spatial boundaries
of ecosystems are defined when the physical and biologic parts form an
integrated unit in which there are defined paths for energy flow and
material transport or cycling. Classes of terrestrial ecosystems called
"biomes" are distinguished by their dominant vegetation form — e.g.,
-------
grasslands and deciduous and coniferous forests. Additional character-
istics are emphasized in Odum's more formal definition: "any unit includ-
ing all of the organisms (i.e., the community) in a given area interacting
with the physical environment so that a flow of energy leads to a clearly
defined trophic structure, biotic diversity, and material cycles (i.e.,
exchange of materials between living and non-living parts) within the
50
system is an ecological system or ecosystem. The agroecosystem is
defined as "a unit composed of the total complex of organisms in the crop
area together with the overall conditioning environment and as further
modified by the various agricultural, industrial, recreational, and
63
social activities of man." The important components and processes of
natural ecosystems are summarized in Table 12-1.
Ecosystems may be described developmentally as young (serai,
successional) or mature (climatic). In a young ecosystem, developmental
stages or communities are rapidly replaced by other communities. This
succession leads ultimately to the mature stage. The distinguishing
characteristic of the mature, or climax stage is that the dominant species
that form the community can replace themselves; thus, the community is
in equilibrium with its normal environment.
There are important differences among the components and processes
of young and mature ecosystems that result in different degrees of response
to environmental stresses or new perturbations, such as the presence of
oxidant air pollutants (Table 12-2). The greater diversity of a mature
ecosystem slows down the disruption of normal structure and function.
For example, a forest ecosystem in which many species make up the producer
community would show less immediate visible damage than a successional
stage with only a few species. Even greater damage would be anticipated
12-2
-------
Table 12-1
Elements of an Ecosystem
Components:
Inorganic substances (C,N,H20, etc.)
Organic substances
Climatic regime
Autotrophs (producers)
Phagotrophs (macroconsumers)
Saprotrophs (microconsumers)
Processes:
Energy flow circuits
Food chains (trophic relationships)
Diversity patterns in time and space
Nutrient (biogeochemical) cycles
Development and evolution
Control
12-3
-------
Table 12-2
Characteristics of Ecosystem Development
Agroecosystems and
Successional (Young) Stages
High production:respiration
ratio
High net production
Short food chains
Small organisms
Open nutrient cycles
Lack of stability
Maintenance cost reduced
by energy subsidies (by man);
production increased
Climax (Mature) Stages
High biomass:respiration
ratio
Low net production
Complex food webs
Great diversity in size
and numbers of organisms
Closed nutrient cycles
High stability
Maintenance cost high,
but rarely subsidized
12-4
-------
In an agroecosystem (which might be considered the simplest of successional
stages, inasmuch as often only a single producer species is present).
GENERAL RESPONSES OF NATURAL ECOSYSTEMS AND AGROECOSYSTEMS TO STRESS BY
OXIDANTS
Ecosystems subjected to oxidant air pollutants must be carefully
observed and described individually if we are to understand and predict
Q O
the complex consequences of chronic injury. Woodwell has summarized
some of the expected effects of air pollutants on ecosystems: elimination
of sensitive species and reduction of diversity in numbers of species;
selective removal of larger overstory plants and a favoring of small plants;
reduction of the standing crop of organic matter, which leads to a reduc-
tion of nutrient elements held within the living system; and increase in
the activity of insect pests and in some diseases that hasten producer
mortality. Many other effects can be suggested.
Photochemical oxidant air pollutants have constituted a chronic
problem only during the last 20 - 25 years, at first principally in south-
ern California, where both natural ecosystems and agroecosystems have been
subjected to these pollutants for the longest period. Citrus groves and
vineyards in the inland valleys of southern California are prime examples
of agroecosystems stressed by chronic exposure to oxidants. Studies were
72
initiated in 1960 on lemon and navel orange trees and in 1968 on wine
73
grapes to determine the economic losses due to oxidant pollutants. Both
studies were performed under field conditions for several years. The lemon
and orange studies provide data that may be interpreted in an agroecosystem
context, although they were highly oriented toward the primary producer
components. ' ' ' There was no effort to examine the effects on
consumer and decomposer components.
12-5
-------
At two lemon groves and one orange grove near Ontario and
Upland, California, 24 trees were selected at each grove and divided
according to a randomized block design into six treatments with four
replications each. The most important treatments for this discussion
were greenhouse-enclosed ambient air, enclosed carbon-filtered air, and
unenclosed ambient air. The first difference noted was a lower rate of
water use by oxidant-stressed trees. The number of irrigations required
by trees in filtered air was always significantly greater than that in
ambient-air treatments; this behavior could not be correlated well with
transpiration rates. From a systems view, one of the major input variables,
irrigation water needed, would be lower for this stressed ecosystem. Com-
parisons of the apparent photosynthesis of single branches of trees in
filtered and ambient air yielded mixed results, but with a trend toward
71
reduced apparent photosynthesis in ambient-air treatments. After five
consecutive seasons of treatment at the two lemon groves and four years
at the orange grove, there were no significant differences in tree circum-
74
ference among the treatments. The lemon trees showed significantly
greater leaf drop in both ambient-air treatments; the orange trees also
followed this trend, but the differences were not significant. The drop
of small, unripened fruit was a severe problem in ambient-air treatments
with orange trees, but insignificant for lemons. The average annual yields
at both lemon groves and the orange grove were significantly reduced when
filtered versus unfiltered treatments were compared; yield was sometimes
74
reduced by as much as 50%. Additional studies with navel oranges exposed
to ambient air, carbon-filtered air, and carbon-filtered air containing
either ambient or half-ambient concentrations of ozone again showed increases
in leaf and fruit drop and decreases in yield of marketable fruit in accor-
dance with increasing ozone or oxidant dose. None of the above studies
12-6
-------
managed to separate the different effects of ozone and peroxyacetylnitrate
or its homologues in the photochemical oxidant mixture.
In summary, oxidant stress reduced water use and photosynthesis,
increased leaf drop and fruit drop, and resulted in a severe reduction in
yield of marketable fruit. All these effects occurred without the develop-
ment of plainly visible leaf symptoms.
Several inferences can be drawn from these data that may suggest
the impacts to be expected at the consumer and decomposer levels. Accelerated
leaf drop may influence the development of pests—namely, aphids, scale insects,
and red citrus mites. Pest populations might be increased if injured leaves
had higher concentrations of amino acids or free sugars before abscission
(see Chapter 11) or diminished if leaves fall too rapidly. Leaf and fruit
drop would provide a larger substrate for populations of decomposer organisms
at the soil surface.
In southern California, the coastal chaparral ecosystem, dominated by
chamise and manzarita or woodland species (including the live oaks and big-
cone Douglas fir), and the coniferous forest ecosystem have received severe
exposure; and the desert ecosystems in the vicinity of mountain passes connect-
ing the coastal and desert regions have undoubtedly been exposed. Injury
has been well documented only in the mixed-conifer forest ecosystem of the
San Bernardino Mountains. Early symptoms of injury in conifer species were
42
reported in a number of California national forests in 1970. In the south-
82
ern Sierra Nevada, Forest Service surveys in 1974 have detected increased
injury in ponderosa pine since 1970 at many locations in the Sequoia National
Forest, Sequoia National Park, and Kings Canyon National Park. Particular
stands of mixed-conifer forest on the western slopes of the southern Sierra
44
Nevada now appear to be affected by oxidants from the San Joaquin Valley.
12-7
-------
The potential loss of timber growth alone in this area is a very serious
prospect.
Injury to important primary producer species constituting forest
ecosystems is not limited to California. In the eastern United States, a
disease Qalled emergence tipburn of eastern white pine was related to
3
ozone by Berry and Ripperton. Occurrence of similar symptoms on the same
species in eastern Canada could not be definitely related to ozone by
38
Linzon. The disease is characterized by bands of necrosis initiated in
the semimature tissue of elongating needles; the necrosis spreads to the
needle tip. In other studies with ozone fumigations at 0.07 ppm for 4 h or
0,03 ppm for 48 h, the tipburn appeared; additional symptoms were silvery
13
or chlorotic flecks and chlorotic mottling.
Under forest conditions, the affected trees occur randomly in the
stand; the same trees are injured successively in a single season or in successive
4
years. Eastern white pine either forms pure stands or occurs in mixtures
with other species in abandoned fields; under these conditions, it is an
80
important pioneer tree. In established stands, it is a major component
of four forest types and an associate in 14 other types with a range extending
80
over 7 million acres from the lake states to the Appalachian Mountains.
Berry reported that emergence tipburn occurs throughout the natural range
of this species; there is also evidence of a slow decline in tree vigor due
to the deterioration of feeder rootlets.
Higher concentrations of ozone in the forested areas of the eastern
United States would undoubtedly cause greater injury to eastern white pine
and other forest species. Chapter 11 reported additional studies that suggested
that other conifer species, in particular Virginia pine and jack pine, may
16
more sensitive to ozone than eastern white pine. In addition, there is
a synergistic interaction between low concentrations of ozone and sulfur
12-8
-------
dioxide that ±s the cause of the chlorotic dwarf disease of eastern white
pine. A study by Ellertsen jit al_. showed 10% mortality between 1956
and 1965 of dominant and codominant eastern white pines near an industrialized
area including several hundred square miles on the Cumberland Plateau. Both
ozone and sulfur dioxide were considered responsible for tree decline. Because
eastern white pine represented only 5% of the total wood volume available
for harvest, the economic impact was slight. There was no effort to interpret
pollutant effects in an ecosystem context. An air monitoring network was
operated by Virginia Polytechnic Institute in 1975 at three locations —
the Blue Ridge Mountains, the Shenandoah Valley, and the southern Appalachians.
62
According to J.M. Skelly, a pollution episode occurred during early July
1975 during which total oxidant peaks as high as 0.13 ppm were observed, along
with 43 h when concentrations were 0.08 ppm or higher. After this episode,
significant increases in oxidant injury were observed, particularly in the
Blue Ridge Mountains in three categories of eastern white pine — those
previously without symptoms, those with chlorotic mottle, and those exhibiting
chlorotic dwarf symptoms. Such incidences suggest the need for more compre-
hensive studies of oxidant (and sulfur dioxide) effects in forests of the
eastern United States. In the long run, the broader question regarding
effects of pollutant stress on all ecosystems components—primary producers,
consumers, and decomposers—should be addressed. An analysis of the multiple
effects of oxidants on eastern forest ecosystems will be a much more adequate
measure of their future usefulness to man than the small amount of information
now available related mainly to single primary-producer species.
The purpose of this chapter is to examine in the greatest detail
possible the effects of oxidant air pollutants on ecosystems. A project
is now going on to study the effects on a mixed-conifer forest ecosystem in
southern California, ' and the planning documents and early results from
this study constitute the major source of information for the remainder of
12-9
-------
this chapter. Other examples of damage to agroecosystems and natural ecosystems
will be included.
ORIGIN OF INJURIOUS CONCENTRATIONS OF OZONE AND OXIDANTS AFFECTING NATURAL
ECOSYSTEMS
Advection from Urban Centers to Remote Areas
Southern California. Descriptions of the vertical and horizontal distribu-
tions of photochemical smog in the Los Angeles basin (southern coastal air
basin) during typical summer days have recently been provided by Blumenthal
5 20 19 43
et al_., Edinger, Edinger e_t a.1., and Miller e_t _al. Important observa-
tions to be drawn from their reports are the interactions of basin and
mountain topography and local meteorology in determining the transport and
concentrations of oxidant air pollutants in relation to elevational zones
of vegetation.
The marine temperature inversion layer that frequently forms above
the heavily urbanized Los Angeles metropolitan area often extends inland as
far as 90 miles (144 km), depending on season and time of day. Surface
heating of air under the inversion increases with distance eastward in
the basin and often disrupts the inversion by midmorning at its eastern edge.
The northern rim of the basin is formed by the San Gabriel and San Bernardino
Mountains, interrupted only by the Cajon Pass about 55 miles (88 km) inland
(see Figure 12-1). The marine temperature inversion layer encounters the
mountain slopes usually below 4,000 ft (1,200 m). In the morning, the
temperature inversion often remains intact at this juncture, and air pollu-
19 a 20
tants are confined beneath it. Studies by Edinger et al. and Edinger
have described how the heated mountain slopes act to vent oxidant air
pollutants over the crest of the mountains and cause the injection of
pollutants into the stable inversion layer horizontally away from the slope.
12-10
-------
Oxidant concentration within the inversion is nonuniform, containing multiple
layers and strong vertical gradients. In some cases, the inversion may serve
as a reservoir for oxidants, principally ozone, which may arrive at downwind
locations along the mountain slopes relatively undiluted, because of a lack
of vertical mixing within the inversion layer and a lack of contact with
ozone-destroying material generated at the ground. The important result of
the oxidant's being trapped in these layers is its prolonged contact with
high terrain at night.
The most important effect of the interaction of pollutant and inversion
layer at the heated mountain slope is the vertical venting of oxidants over
the mountain crest by upslope flow. A gradient of oxidant concentrations
or doses is established across distinct vegetation zones ordered along an
elevational gradient—i.e., the chaparral and conifer forest ecosystems
that occupy the slopes and mountain terrain beyond the crest, respectively.
The altitudinal sequence of these ecosystems is illustrated in Figure 12-2.
27
According to Horton, the chaparral zone is subdivided from lower to higher
elevations into three subzones called the chamise, manzanita, and woodland
chaparral; the mixed-conifer forest occupies the mountain crest.
The daytime changes in oxidant concentrations at several stations
(A, B, C, and D in Figure 12-1) along the southern slope and at the crest of
the San Bernardino Mountains is illustrated in Figure 12-3. In the late
afternoon, the highest concentrations in this profile were at 3,000 - 4,000 ft
(900 - 1,200 m) and adjacent to the mountain slope. The oxidant was not always
confined below the inversion layer, but was present in the inversion layer
19
and above the mountain crest. An instrumented aircraft measured concentra-
tions of oxidant ranging from 0.05 to 0.11 ppm as high as 2,432 m (approximately
1,033 m above the ridge crest) during several noon and 4 p.m. flights. At these
12-11
-------
r;-:v,. \
t:jj, ;-,\:: : :^ :;•::::::::•::: y:::::::::::::: \::::.-..
'*.."- • v " •-- -'V i ' ' ' ; Feef cb&v" f-.a (eve1
•» —..* --j, - - ^ • • -^ •
•.. . . ,f", ..-i 7^^. ... . • «i ,_,..„„ ..
• ^ ^ • '•". _ • " I • I iLC.t 9,^^X5
r—I wo-rcco
?O 1/lUS
FIGURE 12-1. Major topographic features of the Los Angeles basin with
inland valleys and mountains. Station locations; A, Highland;
B, City Creak; C, Mud Flat; D, Rim Forest. Aircraft flight
paths for the study area are also shown. (Reprinted with
19
permission from Edinger et al. )
12-12
-------
OOL X i33j
o
CK
O
K
O
10
o
CO
o
o
GO —
o
!_U
Q£.
CO CN
p~—
CN CN
O
CN
0
co
•rl
cd
O
g
s
•H
T)
S-l
(fl
S
•H
w
o
o
01
01
o
QJ
CT1
a;
CO
CM
I
CM
o
H
6
O
S-l
a
o
•H
03
CO
•H
M
0)
p-
P.
0)
12-13
-------
0900
June 19, 1970
1,000ft.
8
Temperatur
Tvrrain profile
Rsdlands
FIGURE 12-3. Daytime changes in oxidant concentrations along
a west-to-east transect in the southern coastal
air basin, including the slopes of the San Ber-
nardino Mountains (see Figure 12-1). (Reprinted
19
with permission from Edinger et al. )
12-14
-------
times, downwind diffusion of oxidant beyond the crest—on the basis of aircraft
flights approximately 500 ft (150 m) above the terrain—suggested only
19
slight dilution in the first 10 km north of the crest. Observations on
/ Q
other days suggested a 50-60% reduction in oxidant 10 km north of the crest.
There was no ground station at this point for comparison with the aircraft
measurements at either time.
Total oxidant, temperature, and vapor-pressure gradient were
measured continuously during 16 days in July and August at mountain slope
and crest stations (A, B, C, and D in Figure 12-1). In Figure 12-4, the
time of the daily peak oxidant concentration was progressively later at stations
of higher elevation. Temperatures and vapor-pressure gradients were also
progressively lower at higher elevations at the time of oxidant peak. The
duration of oxidant concentrations exceeding 0.10 ppm was 9, 13, 9, and 8
h/day going from lower to higher stations. The longer duration at City
Creek (elevation, 817 m) probably coincides with the point where the
inversion layer most often contacts the mountain slope. The oxidant concen-
trations rarely decreased below 0.05 ppm at night on the slope of the mountain
crest, whereas it usually decayed to near zero at the basin station (Highland).
The vegetation zones along the slope and at the crest are subjected
to oxidant exposure differently. Even though the lower chaparral receives
longer exposure, the peak concentrations coincide more closely with the maximal
evaporative stress for the day. There is some support for the hypothesis that
stomates would be closed during this period and that pollutant uptake would
be lower. There is in fact very little visible injury to the species in this
zone. In contrast, the daily oxidant peak occurs well after the temperature
and vapor-pressure gradient maximums in the conifer forest at the mountain
crest; the oxidant injury to plant species here is severe. These suggestions
of strong microclimatic control of the sensitivity of these native species
to ozone form a working hypothesis that needs further investigation. •
12-15
-------
O 10 O 0 O >O
CN co 03
•o O "O O ir> O
ro co CN CN •— -—
WHdd iMVQIXO 1V101
3«nSS3Hd HOdVA
•o
12-16
-------
42,82
The San Joaquin Valley and Adjacent Sierra Nevada Mountains. Field surveys
have confirmed oxidant injury to ponderosa pine and associated species at
numerous locations in the Sierra Nevada foothills east and southeast of
Fresno. Oxidant measurements at ground stations and by instrumented aircraft
show late-afternoon peaks of "transported" oxidant on the western slopes of
the Sierras. Limited measurements by instrumented aircraft suggest the
development of a layer of oxidant approaching the forested mountain slopes
44
between 610 and 1,829 m during the late afternoon. A very weak inversion
or isothermal layer may serve as a reservoir of oxidant, which is advected
to the mountain slope in the southern coastal air basin, as suggested by
20
Edinger.
Considerable concern has been registered about air quality in the Lake
9
Tahoe Basin, where local development may cause adverse oxidant concentrations.
Seasonal and Daily Variations of Injurious Concentrations
Synoptic Weather Patterns Associated with Episodes of High Pollution.
McCutchan ana Schroeder classified 145 days during May through September 1970
with data collected on the southern slopes of the San Bernardino Mountains.
Five general weather patterns were described, with the associated synoptic
patterns at the surface and at 500 millibars (Table 12-3). An analysis of
eight meteorologic variables was used to classify days during May through
September into the five general weather categories. Of 123 days classified
by stepwise discriminant analysis, 10, 13, 44, 23, and 24 were correctly
categorized into classes 1-5, respectively; the remainder could not be
clearly placed in the five classes. The oxidant concentrations associated
with these classes were: 1, low; 2, low and high; 3, high; 4, low; and
5, low. In this sample, the sum of days in classes 2 and 3, namely 57 days,
suggests that about 46% of the sample days had high concentrations of oxidant
air pollutants.
12-17
-------
Table 12-3
Descriptions of Meteorologic Patterns
for Five Classes of Spring and
Summer Days in Southern California-
Class
General Weather
Associated Synoptic Pattern
at
Surface
at
500 mb
Hot, dry continental air
throughout the day
(Santa Ana)
Large high pressure
over Great Basin
Strong northerly
winds over area
with trough east
of the area
Relatively dry forenoon;
modified marine air in
afternoon; very hot (heat
wave)
Moist, modified marine
air; hot in afternoon
Moist, modified marine
air; warm in afternoon
Cool, moist, deep marine
air throughout the day
High pressure over Subtropical closed
Great Basin and high over area
thermal trough over
desert
Thermal trough over
desert
Thermal trough over
desert
Synoptic low over
desert
Ridge over area
Trough over area
Deep trough or
closed low over
area
a 40
"~ Derived from McCutchan and Schroeder.
12-18
-------
Class 2 and 3 days are both characterized by high pressure (500-
mb ridge over the area). Descriptions of the synoptic weather patterns
(contained in the U.S. Forest Service "California Fire Weather Severity,
10-Day Summaries") for May through August 1972-1974 were compared with
episodes of severe oxidant concentration at Rim Forest and nearby Sky Forest.
For the purposes of this comparison, all days having maximal hourly concen-
trations of 0.33 ppm or higher were compared with the synoptic patterns for
those days. In all cases, a persistent 500-mb high pressure over the area
was the most common synoptic feature. For 8 qualifying days in 1972, the
mean of the maximal hourly concentrations for those days was 0.37 ppm; for
16 days in 1973, 0.41 ppm; and for 46 days in 1974, 0.38 ppm. The highest
hourly concentration ever obtained was 0.60 ppm, on June 28, 1974.
During episodes of severe oxidant pollution, the weather is generally
very hot (85-100 F or about 29-38 C) and the relative humidity may be either
low or moderately high on class 2 and 3 days, depending on the behavior of
the marine layer. The small difference between means of maximal hourly
concentrations on high-pollution days in 1972-1974 suggests continuation of
heavy primary pollutant emission in spite of current control strategies.
Annual Trends of Total Oxidant Concentrations at a San Bernardino Mountain
Station and the Nearby City of San Bernardino. Since 1968, total oxidant
concentrations have been measured continously with a Mast ozone meter
(calibrated by the California Air Resources Board method) from May through
3 la
September at Rim Forest-Sky Forest. The fall, winter, and early spring
months have generally been omitted until recently, because synoptic patterns
are usually not conducive to oxidant accumulation and transport. For example,
average maximal hourly oxidant concentrations from October through April 1973
70
and 1974 stayed below 0.10 ppm; those for April were 0.10-0.15 ppm. The
12-19
-------
main data collection period coincides with the growing season and thus
permits a reasonable estimate of the total annual dcse of oxidant air
pollution received by vegetation.
Two methods of documenting trends of axidant concentrations during
the 1968-1974 period at Rim Forest-Sky Forest express the accumulated
dose as a sum of all hourly values in micrograms per cubic meter and as
number of hours with a concentration of 0.08 ppm or more (the federal
standard) for each month separately, June through September (Figure 12-5).
o
The dose excludes background concentrations — those less than 59 ug/m
(0.03 ppm). The percentage of valid data recovered is also indicated.
The absence of some data — ranging up to 17.8% in 1970, but averaging
8.3% during the 7 years — represents an underestimate that cannot be
adjusted with any certainty. The total number of hours with concentrations
3
of 157 jag/m (0.08 ppm) or more during June through September was never
less than 1,300 during each of the 7 years. These measures of oxidant
trends indicate no improvement in air quality.
Data are available back to 1963 from the downtown San Bernardino
station operated by the County Air Pollution Control District (APCD). The
colorimetric potassium iodide method used to measure total oxidants was
calibrated according to the method of the California Air Resources Board.
A positive correction factor of 1.22 was used to adjust mountain data for
the decreased air pressure at the higher elevation.
The data from the Rim Forest-Sky Forest station were compared with
published data from the San Bernardino County APCD. The numbers of hours
n
with concentrations exceeding 392 /ig/m (0.20 ppm) during July, August,
and September in 1969 - 1974 were compared (Figure 12-6). For 1963 - 1968,
data are shown only from the San Bernardino APCD. A large part of the year-
12-20
-------
2oi* [3)ujddoo'o^ iNvoixo ivioi'sanon
o
CJ
IO
o
ff\ •--—...-
0> u> ~
cn m o
C' CO
to
*
cn
(T 10
UJ 10
CD 00
. y*
UJ x
!- of
QL ui
UJ . CO
> < 2 ^
i O £ <*•
UJ Q] '^
~ZL - id
ZD co
"3 1— i
1 UJ ^j CM
^ CC -a cvj •
< O " °°
o ii y.
X1"" —3
x
0 >• x
-J co ^
< V. • H 10
Oh- ^ ^
J— CO U.
X-^v CC J—
CD *~
,., U_ ^ ro
c/> -5: o: f
O _ uj m
• • -" • !.--._.- 'i : :•• i
1 1 1
i W | 4>
_ < ( 1 ^ °
1 1 ~* 1 °
:-. -- - " i.- • '.: ' ..'• " \ . . • -i -.-•
'• ' \ ••' '-• • i • ". ! .' '••';•' :
:.:• - - 1 ' • _ ' ...._ ' .,_
' ' '
cJ o i cr> ? i !!; '5 i co i
tn o> i 1 o o
I i i
:;>;'T ". - - ' ":•'•;.'..' ..: - :":' ..r".--":-
"•'i- : ;'-" -I.:.....:.. •=••-' -.-i-_.-."
i f
to f ' LO" p 1 Q "5 f CD ^
ox cn ^ < i0"3 i^'"3
' ".'.' r : '-..- . -t. i • .-
' ' V c,
oic?1 2^ i 2 ~:\ > S -3
.,',-..- I I
::;- •':••! - i . . ]' • .'••-•
If-.-- en • 1 co 1 ^ j:
1 to 5^ to " i '-o "3 i 10 a
1 CO (X h- -^ Ol -t Ol ~>
1 1,'--
i
0
CM
N
CD
CO
O
<7>
CO
CO
IO
CD
IA
™*^
oc
^—
111
X
M-l
O
M
(U
&
Q
^
(3
H
a
4-1
0
4J
T3
C
to
a)
U)
0
•d
4J
G
co
•d
•H
X
o
•H
n)
4-1
oc
4J
i+-i
0
^
^s-
i~^
ON
•— 1
|
CO
VO
ON
rH
M
01
,J3
4-1
a.
01
c/3
1
(11
a
a
>->
n
c
0
•H
•U
[rt
g
g
3
CD
>-.
r-(
.C
4-1
d
o
2
l
(Nl
H
&
O
4-1
co
, 4J
^i
W <4-l
1 O
4-1
CO HI
ID 00
>-i cS
0 4J
P4 G
QJ
•S 2
Pi 0)
ex
4J
(fl 01
4-1
<• — «. co
B o
&-rl
a. -a
OO -rl
0
• 01
0 H
^^ nj
jz
•o
B G
--. 01
oo a
a o
f» C
u~l -H
iH
CO
C 1J
rt a)
X J3
3
s-i a
m
4J
PQ
tt) G
«
4J !/3
rt
u
CD J2
>J 4J
3
O G
J3 -H
S
O
!-l
14-1
G
O
•H
CO
CO
•H
a
^
01
a.
J
4J
•H
s
13
QJ
4J
G
•H
^
O.
0)
C6
^~s
M
•H 0)
CO ^
CO O
O -iH
P. «
o ""> o
S0lx(
^rrjfO^o — — o
// ) 3GOQ INVOIXO TV1
12-21
-------
8
o
10
o o
O o
C\J _ O
' I I I I I I I
o>
u
(/
X
U
Q
U
a
<
^
<
h
c
1-
2
U
C.
Q
U
Q
V
^*
2
H
3
C
C
*•_
c
(_
Q
<
C
-?
c
a
2.
a
u
DC
2
c
CA
o
o
l\ \ \ \
•*
JO \
J -*r \ •
\ \
1 \ \
5 _ \
c w I
< I
C s \
? "° T
C o>
E \
j \
> CO •
i K Q
00
a>
•*
p
»
>
p
^ Qt
5 H ui
- cn co
3 Ul -5
3 CC S
OH- '
C ^ £ - •
) CZ CO - ' u-
; ^ . > g eo
J £ W 2 < K
c co CP < v>
'. ui -3 uj UJ
J O • **
^ 1 1 UJ ^-
111 ^3
1 > I III
6 6
8 8
\ \ \ \ \
\\ \\ \\
^ \ \ \
\
\
j\
>\\\\\
/
/
/
'\\ \\\\
\
\
\
\
X \\\\V
\
\
\ EX
1
1
r\?\ \ \ \
;
• l\ \ \ \\
•
\1\\ \\
\
i\\\\
E
0 0
0
§
.
p
a>
i^
2
0
K
a>
o>
u>
^ CC
^J
UJ
0 oS nj'l
60 a\ 4J|
CN •• 4-1
CTi C 1-1
ro o 0)
•H _ ^
CJ 4-1 U
03 nj *H
r-^ 4J ^
4-1 C/l
e
H 4-1 O
OJ O (-1
4J -H M-l
0) 4J C
1-1 CD O
M -H -H
Q to
l-l OJ
O i-l -H
0 0
O M M
4-J 4-1 QJ
C CX
i-H O
tfl U ,G
3 4-1
cr c -H
4J T3
1-130)
0) r-l 4J
& <-< G
S O "^
0) PL, l-i
CX fi 0)
(U O P£l
C/3 > — '
O ON
« O ^H
4-1 I
C O 00
•H T3 iH
iH ^ tn
03 0) O
4-i m ^
o o
4J C fa
(0
u o
3 4-1
o a
co
o o
4-1 13 fa
o
L, £ §
;•( nj -ri
Xi ••
2 CX nj
CM
- INVQIXO ivioi HUM sanoH
B
12-22
-------
to-year differences at the same station and between stations can be attributed
to differences in synoptic and mesoscale (local) meteorologic patterns. For
example, the increases in 1972, 1973, and 1974 at Rim Forest-Sky Forest are
associated with 6, 16, and 46 days, respectively, when a persistent 500-mb
ridge occurred over the Southwest, particularly southern California. The
difference between stations in the same year is probably influenced most
by inversion height. Lower inversions partially restrain transport upslope
to shorter periods each day. Higher inversions would have the opposite
effect and also allow a greater air volume below to dilute oxidants. The
3
index for comparison chosen in Figure 12-6 — i.e., hours >^ 392
would be sensitive to inversion height. The 3-year moving averages for
each station tend to remove some of the variation due to meteorology.
3
In terms of hours equal to or exceeding 392 jig/m , the moving average between
1970 and 1973 at Sky Forest-Rim Forest has increased from 175 to 290. The
increased oxidant concentrations at both these stations are the reverse of
those in upwind, urban Los Angeles County, where increased emission of NO
X
tends to shift the chemical equilibrium to the left, toward the ozone
precursors. The most recent data firmly indicate that oxidant concentra-
tions will either increase annually or continue to oscillate around the
mean of present high concentrations in the foreseeable future at these
distant locations.
The tropospheric ozone cycle describing rural upwind, urban, and
rural downwind variations in concentration can be easily demonstrated in
the Los Angeles and connected inland basins. The effects on both natural
ecosystems and agroecosystems also become apparent. For example, oxidant
doses during August 1972 at six oxidant stations — Costa Mesa, La Habra,
Corona, Riverside, City Creek, and Rim Forest — extending in a line
12-23
-------
northeastward from the coast to the mountains show low doses at the coast
increasing to a maximum on the chaparral-covered mountains and decreasing
beyond the mountain crest (Figure 12-7). The oxidant dose is indicated
hy the dashed line. A crude estimate of the relative economic value of the
products from ecosystems encountered along this transect are expressed in
a very general way by the solid line and the nomenclature on the abscissa.
Finally, the relative complexity of the ecosystems involved is shown below
the abscissa. This conceptualization emphasizes the enormously greater
dosage received by the natural ecosystems during this month. This pattern
of dosages is very typical of June, July, and August, but the offshore flow
typified by the Santa Ana winds may reverse the situation in September or
October; susceptible crops growing on the coastal plain may be seriously
damaged.
In general, the permanent vegetation constituting natural ecosystems
receives much greater chronic exposure, whereas the short-lived higher-
value vegetation constituting the agroecosystems of the coastal plain can
be subject to injurious doses, but in intermittent short-term fumigations.
Each situation has measurable economic and aesthetic effects, but on diffe-
rent time scales. The simple agroecosystem has little resiliency to pollu-
tant stress; losses are immediate and may be catastrophic. The complex
natural ecosystem is initially more resistant to pollutant stress, but
the longer chronic exposures cause the disruption of both structure and
function in the system. Damage may not be reversible.
AN EXPERIMENTAL DESIGN FOR INVESTIGATING THE EFFECTS OF OXIDANT STRESS
ON ECOSYSTEMS
Techniques for Ecosystem Modeling
The steps needed to understand the effects of oxidant air pollu-
tants on an ecosystem are description of ecosystem components or subsystems
12-24
-------
r-
Ld
o
o
2
O
o
UJ
-J
h-
2
Ul
f--
o
CL
P"
COSTA
MESA'
LA
HA BRA
-------
and identification of the most important processes within organisms or
interactions between organisms or communities of organisms that would be
most vulnerable to pollutant stress, including an evaluation of factors
of the physical environment that may limit ecosystem processes. This infor-
mation can be conveniently arrayed in terms of interaction tables that show
which variables are involved in various subsystems and whether the inter-
action between any two variables is positive or negative. The next step
involves the selection of the most appropriate paradigm for the substance
or "unifying thread" that flows through the various subsystems. Examples
of possible "flows" are energy, biomass, mineral nutrients, water, numbers
of species, population densities, or area occupied per biotic unit.
The state of the art of ecosystem modeling has evolved rapidly in
recent years. Discussions of various ecologic subsystem simulators are
30, 34, 52
published. Recently, discussions of the utility of computer
simulation modeling in ecologic research have been published by the National
47 48
Academy of Sciences and the National Science Foundation.
Depending on the "flows" through the ecosystem that one chooses to
study, the modeling procedures may be either deterministic or stochastic.
58
Rochow has described the step-by-step procedure for studying the flow
of nitrogen through a forest ecosystem. In this case, nitrogen can be found
in a number of well-defined storage compartments. The transfers of nitrogen
between compartments are described by transfer coefficients arrayed in a
symmetric transfer matrix. Differential equations are written that represent
the rate of change (or flow) of nitrogen through time for each of the various
compartments. Computer programs already exist to solve these equations. Once
the model is running smoothly on the computer, it is possible to impose
12-26
-------
various experimental conditions — e.g., clear-cutting or selective cutting -
and observe the effects on nitrogen flow. Sensitivity analysis can then
be performed to study which transfer coefficients are sensitive to small
changes and which only to large changes. The useful outputs of these manipu-
lations include a determination of how much particular transfers in the
system can be changed or stressed before the ecosystem deteriorates. This
example uses a deterministic model; however, the flow of water through an
ecosystem may have both deterministic and stochastic mathematical proper-
ties.15
Models of energy flow or biomass flow have been more successful when
uniform plant canopies were involved — e.g., a field of corn. A recent
development from the field of integrated pest management has been described
in which an alfalfa growth model has been coupled with an alfalfa weevil
23
population dynamics model. The plant growth model in this example might
be adaptable to air pollutant injury studies in agroecosystems. Because the
model is built to incorporate current weather data that have direct influen-
ces on pollutant concentration and plant sensitivity, this type of model
seems to be a worthwhile departure point for simulating dose responses.
The simulation of the population structure and dynamics of autotrophs
and phagotrophs is another important interaction that can be modeled to test
for effects of pollutant stress. A standard approach is the use of a finite-
35
population-difference model. The model assumes that the population change
of a species in a specific period is equal to the species population multi-
plied by an intrinsic coefficient of rate of change. The rate coefficients
are difficult to define without extensive data. The task is further compli-
cated because "a consistent feature of communities is that they contain a_
comparatively few species that are common— that is, represented by large
numbers of individuals or a large biomass—and a comparatively large number
12-27
-------
49
of species that are rare at any given locus^ in time and space." It is
Implied by this statement that adequate sampling procedures may be difficult
to design if only the spatial aspect of the problem is considered. The
constraints of short-term research funding in the form of grants or contracts
21
generally preclude adequate sampling of the time dimension. Ewing et al.
have considered a related modeling constraint: the simulation of the hierar-
chic structure inherent in a biologic population. Through exploitation of
the structure of the biologic, mathematical, and computer systems, a Monte
Carlo simulation of a structured population is possible. With a nonhomo-
geneous Poisson process, events are defined and a suitable risk structure
is developed that satisfies mathematical and biologic requirements. A
structured computer language allows one to mimic the structure and organiza-
tion of a population — different levels of organization ranging from the
individual to the complete population.
A description of another "flow," the area occupied per biotic
unit over time, is also very important for defining and predicting long-
term successional changes in plant communities due to pollutant stress.
61
Schugart et al. have described a model for 250 years of succession in
the western Great Lakes Region in the absence of fire, epidemics, and
6
forest management. Botkin and Miller predicted successional changes
during a 100-year period after logging in a northern hardwood forest.
There are no examples of models dealing directly with oxidant
stress on communities or ecosystems. However, the types of models
just described may be applicable to this problem. In view of the trend
of increasing oxidant concentrations downwind from urban areas, a much
more precise understanding of chronic effects on both natural ecosystems
and agroecosystems is required. Descriptive and predictive models dealing
with the responses of biologic systems can provide the best input to the
12-28
-------
decision models needed for standard-setting, land-use planning, and resource
management.
Modeling the Effects of Oxidant Stress on a Western Mixed-Conifer Forest
Ecosystem
The recent history of the mixed-conifer forest of the San Bernardino
68
Mountains has been analyzed. This analysis included an initial inventory
of ecosystem components and processes, as indicated in Figures 12-8 through
12-12. The inventory emphasizes ponderosa and Jeffrey pines, the most
dominant species in the climax community, and is stratified according to
organizational level — namely, organism or tree (Figures 12-8 and 12-9),
community or stand (Figures 12-10 and 12-11), and finally a time-oriented
analysis of plant succession in the aggregation of relatively distinct
communities or stands that collectively make up the mixed-conifer forest
ecosystem (Figure 12-12). This analysis was assembled by nearly a dozen
70
coinvestigators representing many disciplines. These detailed diagrams
are presented here to emphasize the complexity of ecosystem interactions
at each level of biologic organization. Only the interactions considered
to be the most important ones guiding the course of plant succession in the
several forest plant communities now constituting the mixed-conifer forest
69
have been selected by project investigators for immediate investigation.
In the case of each interaction, it is important to decide the time frequency
at which the selected state variables and driving variables will be measured—
i.e., hourly, weekly, or annually.
A data capture, storage, and retrieval system is being devised to
provide modelers with immediate access to all subproject data. Because
this project is currently the most active effort directed toward under-
standing the effects of ozone and other oxidants on a natural ecosystem, most
of this chapter is a discussion of its latest progress.
12-29
-------
OXIDANT
;f UAiUAM ^
[ AIR ]
\}2.\ POLLUTANTS-'^;
A
•":i^«'v
SOIL
>LlCRO-
H;\ARTI!RO?ODS J
^ \
7 8 9 10 X I3 14
liATURAL \
ENEMIES OF ^
BARK BEETLES^
A1,"D OTHER
HOLE NESTING
BIRDS
FIGURE 12-8.
Organism-level interactions irr'a mixed-conifer forest. Types of
interaction: 1, competition for food supply; 2, direct effect of
ozone on small-mammal physiology; 3, climatic control of oxidant
concentration in forest; 4, direct effect of ozone on soil micro-
arthropods; 5, effect of precipitation and temperature on soil
moisture and soil temperature; 6, insect damage to developing
cones; 7, small-mammal damage to developing cones and importance
of cone crop as animal food supply; 8, direct effect of ozone on
physiology of cavity-nesting birds; 9, role of fruiting bodies
of nonpathogenic fungi in nutrition of small mammals; 10, direct
effect of ozone on tree physiology; 11, role of fruiting bodies
12-30
-------
of pathogens in nutrition of small mammals; 12, direct effect
of ozone on nonpathogenic fungi; 13, effect of temperature
and evaporative stress on tree growth; 14, direct effect of ozone
on pathogenic fungi; 15, interaction of nonpathogenic fungi and
soil microarthropods; 16, interaction of pathogenic fungi and soil
microarthropods; 17, effect of soil microarthropods on litter
reduction; 18, impact of predation and parasitism on bark
beetles; 19, predation of bark beetles by woodpeckers; 20, effect
of bark beetles on tree mortality and vigor and effect of phloem
thickness and moisture on bark beetles; 21, effect of phloem
moisture and thickness on natural enemies of bark beetles;
22, influence of woodpeckers on rate of parasitism; 23, effect
of nonpathogenic fungi on tree growth; 24, effect of pathogens
on tree vigor and mortality; 25, effect of soil moisture and
soil temperature on tree growth; 26, effect of soil moisture
and temperature on occurrence of nonpathogenic fungi; 27, inter-
action of pathogenic and nonpathogenic fungi; 28, effect of soil
moisture and temperature on occurrence of pathogenic fungi.
(Reprinted with permission from Taylor.™)
-------
• OX I DAN T \!
.POLLUTANTS
SYNTHESIS
AND
RESPIRATION
/
/ MINERAL
WATER
UPTAKE
AND
TRANSPIRA-
TION / [CARBOHYDRATE
PHLOEM Th'.CKMESS
PHLOEM MOISTURE
RESIN DUALITY
RESIN QUANTITY
FIGURE 12-9. Tree-level interactions in a mixed-conifer forest ecosystem.
Types of interaction: A, relationship between net photosynthesis,
foliage age, and foliage retention; B, effect of plant moisture
stress on net photosynthesis; C, relationship between mineral
12-31
-------
uptake and net photosynthesis; D, relationship between net
photosynthesis and carbohydrate storage; E, relationship between
water uptake and mineral nutrition; F, relationship between
carbohydrate storage and bark characteristics; G, relationship
between carbohydrate storage and cone production; H, relationship
between carbohydrate storage and cone production; 1, relationship
between cone crop and seed crop; 6, cone insect damage to develop-
ing cones; 7a, small-mammal damage to developing cones; 7b, small-
mammal predation of seeds; lOa, effect of ozone on photosynthesis
and respiration; lOb, effect of ozone on needle retention; 13,
effect of temperature, light intensity, and evaporative stress
on photosynthesis and respiration; 20a, effect of bark beetles
on water uptake and transpiration and relationships of tree
moisture stress to bark beetle attack; 20b, effect of bark
beetles on tree carbohydrate concentration and relationships of
carbohydrate concentration to bark beetle population in tree;
20c, relationships between bark characteristics and bark beetle
attack and population; 21, relationship between bark characteris-
tics and natural enemies of bark beetles; 23a, relationship bet-
ween root characteristics and mycorrhizal-forming nonpathogenic
fungi; 23b, effect of nonpathogenic fungi on mineral uptake;
24a, effect of pathogens on tree carbohydrate concentration and
relationship of carbohydrate concentrations to pathogen attack;
24b, effect of pathogens on water uptake and transpiration;
24c, relationship between stem and root characteristics and
pathogen attack; 25a, effect of soil moisture and temperature
on water uptake and transpiration; 25b, effect of soil mineral
concentration and temperature on mineral nutrition of tree.
a indicates direct influence of external factor on trees.
b and c indicate influence of tree condition on external factor.
(Reprinted with permission from Taylor.^0)
-------
FIGURE 12-10.
Community-level interactions in a mixed-conifer forest ecosystem.
Types of interaction: 1, competition between woodpeckers and
small mammals; 2, climate control of oxidant concentration in
different forest communities; 3, effect of precipitation and
12-32
-------
temperature on soil moisture and soil temperature in
different forest communities; 4, predation of bark beetles
by woodpeckers in different forest communities; 5, effect
of cone crop abundance on cone insect populations in different
forest communities; 6, effect of cone crop abundance on small-
mammal populations in different forest communities; 7, fruiting
bodies of nonpathogenic fungi as food for small mammals in
different forest communities; 8, smog-caused mortality and
morbity in different forest communities; 9, fruiting bodies
of pathogens as food for small mammals in different forest
communities; 10, effect of temperature and evaporative stress
on species composition in different forest communities; 11,
relationship between soil characteristics and population
density of burrowing small mammals in different 'communities;
13, relationship between soil characteristics and microarthro-
pod population; 14, bark beetle mortality caused by natural
enemies in different forest communities; 15, effect of bark
beetles on tree mortality and vigor in different forest
communities; 16, relationship between soil characteristics and
forest community composition and growth; 17, relationship
between soil characteristics and species distribution and
behavior of nonpathogenic fungi; 18, relationship between
soil characteristics and species distribution and behavior
of pathogens; 19, influence of forest community type on
populations of natural enemies of bark beetles; 20, woodpecker
distribution and density in different forest communities;
21, effect of pathogens on tree vigor and mortality in different
forest communities; 22, relationship between nonpathogenic
fungi and forest community composition and growth. (Reprinted
with permission from Taylor. ^)
-------
xl PATHOGENIC
FUNG/
22 b
ENEMIES CF I \
BARK / 2!b
BEETLCS
ABUNDANCE
OF
COf.'ES 0 SEEDS
PLAN!
COMPETITION
SOIL
MICRO-
ARTHROPODS
SMALL
MAMMALS
FIGURE 12-11.
Stand-level interactions in a mixed-conifer forest ecosystem.
Types of interaction: A, effect of plant competition on
abundance of cone and seeds; B, effect of plant competition
12-33
-------
on characteristics of liying trees; C, effect of plant
competition on characteristics of shrubs; D, effect of
plant competition on characteristics of herbs; E, effect
of plant competition on tree mortality; 5, abundance of
cones and seeds and predation by cone insects; 6a, abun-
dance of cones and small-mammal predation of cones; 6b,
characteristics of forest stands and small-mammal popu-
lations; 6c, influence of shrub and herb layer vegetation
on small-mammal populations; 8a, smog-caused mortality
and morbidity in different tree species with forest stands;
8b, influence of stand conditions on concentration of
oxidants; lOa, influence of temperature and evaporative
stress on stand structure and composition; lOb, influence
of stand condition on temperature and evaporative stress;
12b, influence of stand condition on soil microarthropod
population; 15a, influence of bark-beetle-caused tree
mortality on stand condition; 15b, influence of stand
condition on bark beetle population; 16a, influence of
soil moisture and temperature on stand characteristics;
16b, influence of stand condition on soil characteristics;
19, influence of stand condition on population dynamics
of natural enemies of bark beetles; 20, relationship
between smog occurrence and woodpecker population; 21a,
influence of pathogen-caused mortality on stand condition;
21b, influence of stand condition on pathogen population;
22a, influence of mycorrhiza fungi; 22b, influence of
snags (and downed trees) on nonpathogenic fungi; 22c,
influence of stand condition on nonpathogenic fungi.
a indicates direct influence of external factor on trees
in stands, b and c indicate influence of stand condition
on nonpathogenic fungi. (Reprinted with permission from
Taylor.70)
-------
SOIL
CtlARACT ER-
ISTICS
COMMUNITY
STRUCTURE
#1
J
1
i
I
6
7
f
if) —
1 \J
I
?
I
r
c* r~i ^ f ^'^r r^ * T ' • — \*
CTPT Tp-T" '">ir
^2
8
FIGURE 12-12.
Community-succession interactions in a mixed-conifer forest
ecosystem. Types of interaction: 1, oxidant modification
of community structure; 2, climate modification of community
structure; 3, fire modification of community structure; 4,
soil characteristics and their influence on community structure;
5, insect modification of community structure; 6, mammal
modification of community structure; 7, pathogen modification
of community structure; 8, people impact on community structure;
9, logging modification of community structure; 10, predictive
capability through integration of submodels for items 1-9.
(Reprinted with permission from Taylor.
12-34
-------
25, 56, 77
Other researchers at the University of Utah have completed
studies to determine the ozone susceptibility of the most prevalent species
in some major vegetation associations in the intermountain area. These data
are intended to be combined with background information on community stability
and integrated into mathematical equations. The equations may be able to
predict the community changes that occur after stress of various degrees.
The ozone concentrations in grassland and aspen plant communities in the
Wasatch Mountains above Salt Lake City are much lower than those in the
77
San Bernardino I-!ountains. According to Treshow and Stewart, "Background
ozone concentrations in the grassland communities geographically contiguous
to the Salt Lake Valley occasionally reached peaks at 15 pphm, but the
average concentration over a 1-hour period never exceeded 6 pphm at any of
the plots. Concentrations measured in the aspen community during the study
reached 9 pphm but never for more than a few minutes at a time." The
, . -, . 25, 56
present low concentrations may be important to some species or cultivars
and the plant communities of which they are members.
EFFECTS ON PRIMARY PRODUCERS (GREEN PLANTS)
The ozone dose responses and the specific effects on the photo-
synthetic activity of both herbaceous and woody plants, principally in
controlled short exposures, are discussed in Chapter 11. The main aim
of this section is to evaluate the effects of the chronic exposure of
vegetation in natural ecosystems to total oxidants (more than 90% ozone)
under field conditions or simulated field conditions. The effects of
chronic exposure on agroecosystems is also discussed to a limited extent
in Chapter 11.
64
H. W. Smith has suggested three classes of ecosystem response
to air pollution: those in which vegetation and soils serve only as a sink
for pollutants, with no visible injury; those in which some species or
sensitive individuals within species are injured and are more subject to
12-35
-------
other stresses; and those in which high dosages cause acute morbidity or
mortality of some species. Although these classes are convenient for
discussion, in most situations they are not clearly separated in space.
More often, these classes of response occur along a gradient of decreasing
pollutant exposure, as in the San Bernardino Mountains.
Extent and Intensity of Injury to Overstory Trees in the San Bernardino
National Forest.—Wert (1969) used aerial photography to determine the
extent of oxidant injury to ponderosa and Jeffrey pines in diameter classes
larger than 30 cm. Injury was categorized as heavy, moderate, light or
negligible, and it generally decreased with distance from the source area.
Of the 160,950 acres (64,380 hectares) of ponderosa-Jeffrey type within
the forest boundaries, 46,230 acres (18,492 ha) had heavy damage, 53,920
acres (21,568 ha) had moderate damage; and 60,800 acres (24,320 ha) had
light or negligible damage. An estimated 1,298,000 trees were affected;
of them, 82% were moderately affected, 15% were severely affected, and 3%
were already dead.
The term "ponderosa-Jeffrey type" is a general term that includes
a mosaic of five subtypes described by McBride on the basis of species
3 la
dominance. These subtypes are: ponderosa pine forest, ponderosa pine-white
fir forest, ponderosa pine-Jeffrey pine forest, Jeffrey pine forest, and
Jeffrey pine-white fir forest. The injury by oxidant air pollutants is most
intense in the types dominated by ponderosa pine and less intense in the
Jeffrey pine types. In the field plots of these various types, the average
area covered by shrubs is only 3.8% in the ponderosa types, but 26% in the
31a
Jeffrey pine types.
45, 68, 70
Later studies have expressed the amount of injury to
ponderosa and Jeffrey pines and associated tree species in permanent study
12-36
-------
plots as a numerical score. The range of scores is subdivided into seven
45
categories ranging from dead to no visible symptoms.
In 1974, all tree species at 19 permanent study plots were scored
individually by binocular inspection. The data can be obtained from conifers
early in the fall, but the most important deciduous species, black oak, was
evaluated during 3 days, August 28-31, to prevent confusion of oxidant-injury
symptoms with natural autumn senescence of leaves. The injury to black oak
as of August 31, 1974, at several representative study sites and the June -
August accumulated dose at nearby monitoring stations are shown in relation to
the topographic projection of the San Bernardino Mountains in Figure 12-13.
Lower scores mean greater injury. The darkened portion of the bar represent-
ing oak injury is for leaf chlorotic mottle and interveinal necrosis. A
score of 8 means no injury. The remaining portion of the score is the sum of
scores for leaf complement, leaf size, and twig mortality, not shown separately.
These data suggest that oak shows no visible injury where the accumulated
5 3
June - August dose does not exceed about 2.5 x 10 jag/m -h from about Snow
Valley eastward.
The distribution of ponderosa and Jeffrey pines into various injury
classes with respect to the distance of the study site along the gradient
of oxidant dose (June - September) is illustrated above the topographic
projection in Figure 12-14. It is important to realize that the 1974 distribu-
tion into injury classes is also a product of earlier years, when the oxidant
concentrations were not always as high as in 1974 (see Figure 12-5). The
trend toward greater numbers in the very slight (29-35) and no visible injury
(36 and greater) categories is quite evident in the eastern plots receiving
lower doses — e.g., Holcomb Valley (HV). The assumption has been made that
ponderosa and Jeffrey pine respond similarly to oxidant. Ponderosa pine is
12-37
-------
X
o
id
H
43
o
4-1
;>,
M
•3
•r-i
G
•H
CO
p
00
3
<3
1 43
0)4-1
fl-rl
3 !S
>T>
'O
^ CU
O4J
m c
•H
CU M
co a.
O 0)
3
•a c
•rl CO
X T3 !
O -rl 1
O G
i-H'rl
G to
O 4-1 CO
CO O CO
•H 4J 0)
^ 1-1
CO -o
&. cu co
a 4-1 c
O CO CO
O r-l 0)
^ 3 e
4-1
•H
3 0)
O M
O O
CO U
" CO
tO 43
(3 4-1 (-1
•H -i-t CU
CO & 43
•u M
C --H
3 si- a
O r~-
O CO
C - C
•H t-H o
TJ 00 -H
>-( 4J
CO 4-1 cflcfl
S CO +JH
S-i 3 COro
0) bO
C ^ -S *'
CO •> M 4J|
w w o cu
0) 4-1
•> 4J -H 4-1
C -H C h
o co o cu
cu 3 43 :*;
•!-) 4-) S-l
o w co B
M cu o
ft H (3 H
O m
O T-i 4-1
•H cd cfl G
43 B O
P. T3 -rt
Ctf 4J CU CO
M CO ^i 03
00 3 -H
o co co a
ft 4xi CO C
O cfl CU CU
HOBO.
I
CN
O
f-f
12-38
-------
J£ \JW\y//ti:''>-?1- ' •vy////'','///..V. :.:• ,/)/
\ \ VT
"™-
Q o
r- u>
•H- m/3
O O o o o o
in v n <\j _ ,5
XNiVQIXO TY101
rw
Vv ;?(/>
co
01 OJ
e! en
•H W
cd o
en
o ^
a) s
M cd
CU 13
CU CU
CO rH
42
- -A
iJ CO
•H
oo
O -H
O~
O
c
C
00 -rl
-S-d
S CU
O 4J
Jl s
CO 42
CU O
M
CU .«
> m
cu m
CO I
ON
>.CM
M
cu *
•H O
•Hcd
i-M
con
cd
cu
CD
o a)
ti w
•H -r)
id co
cfl 1^
•0 .""
fH 4J
M
<• .- a)
00 Ai
CM U
• I -rl
4-1 CM M
C CM
Cd S
T3 •> O
(3 t-i O 00
cd O -H C
c/l •!-) T—I rH o
cd cd co -H
- e 4J co
fl O ^ CO
O C 4-1 PC] -rl
O -~v O iH CU
CU P-( CM P<
•n >~J 0) I
o ^^ co m 43
H O r-t 4-1
CX CO T3 T-(
CU . ^
O C rH CU
•rl 'rl cd 4-1 "d
43 CX (3 cd CU
CX O M 4-1
cd t^. co cu fi
!-i CU cfl T3 -H
00 M CD O !-(
o m co e ex
ex u-i cu
O CU O « CiJ
H *-> 4J Q ^
-------
replaced by Jeffrey pine in the natural stands east of Camp O'ongo, and
they intermix at Barton Flats (BF). The validity of this assumption can be
partially verified by examining the distributions of the two species into
injury classes at Barton Flats (Figure 12-14). These data indicate reasonable
similarity at a common site; but the influence of other environmental variables
that change continuously along the oxidant gradient — such as soil moisture
availability, temperature, and humidity — must be examined more intensively
to understand the degree to which they influence oxidant susceptibility (see
Figures 12-8 through 12-12).
Trends in Oxidant Damage to Conifer Species in the 19 Major Study Plots
from 1973 to 1974.—The first evaluation of oxidant injury to all tree
species in the new study plots was completed in September and October 1973.
The second evaluation, in 1974, offered the first opportunity to assess
trends of tree injury and mortality. In Table 12-4, the plots are arranged
in the order of severe injury (first) to no visible injury (last), according
to the 1974 average injury score for all ponderosa or Jeffrey pine in
each plot. Of the 12 plots categorized as severe and moderate, all but six
showed significantly lower scores (increased injury) with a probability of
0.05. Among the remaining 6 plots classified as slight, very slight, or no
visible injury, there were three significant increases, one insignificant
increase, and two decreases (one significant and one insignificant), all at
a probability of 0.05.
The general increase in injury in the severe and moderate plots
is probably related to the 1974 increase in June-September dose (Figure 12-5).
Tree mortality among ponderosa and Jeffrey pines was about the same in
1973 and 1974. The largest mortality was at permanent study plots in the
moderate injury category. Perhaps the populations in these plots still
12-40
-------
ANNUAL GROWTH OF BRANCHES, UPPER HALF OF SAPLINGS
3S-
30-
2R -
26-
£«-
X jo-
ts e-
uj e-
_t
4 -
2-
0-
e-
6-
TERMINAL SHOOT GROWTH
1 AVi.ENT AJr< OUTSIDE
2 AV3:ENT A,R HOUSE
J FILTERED AIR HOUSE
i —
T
t
1 2
[f
3 1
1969
1 rl
2 3 1
1970
-
-
\
2 3
1971
••
_
2 3
1972
-
2 3
1973
YEAR
32-
3O-
28-
26-
£22-
I20
5 •«>-
5 16-
FIRST ORDER BRANQ< GROWTH
l AVS1L^.T AIR OUTSIDE
2. AMBIENT A« HOUSE
3 FILTERED ArR HOUSE
:lra
I 2 i
1963
jt
r"
2 3
1972
Z 3
I97J
YEAR
FIGURE 12-15.
Annual growth of the terminal shoot (upper) and first-
order branches (lower) in upper half of ponderosa pine
saplings maintained in filtered or unfiltered (ambient)
air greenhouses, and an outside ambient air treatment
from 1968 through 1973. (Reprinted with permission
from Kickert et al.31a)
12-41
-------
retain greater numbers of the more susceptible genotypes. In earlier years,
tree mortality rates for ponderosa or Jeffrey pines in several stands suffering
68
moderate to severe injury were 8% and 10%, respectively, from 1968 to 1972,
45 10
8% from 1969 to 1971, and 24% from 1966 to 1969 . The final cause of death
65
of weakened trees is usually the pine bark beetle. Mortality has not been
observed in tree species other than ponderosa and Jeffrey pine.
Data for the longest observation period of tree decline extend from
1952 to 1972 in two 5-acre (2-ha) control plots in the vicinity of Barton Flats
80
in the San Bernardino National Forest. These plots are in the Jeffrey pine-
white fir subtype and are now considered to be in an area of moderate injury
(see Barton Flats and Camp Oceola plots in Table 12-4). All Jeffrey pines,
with a diameter breast height (dbh) of 12 in. (30.5 cm) and larger were measured and
their vigor was described by judging the risk or the probability that they would
be susceptible to attack and kill by bark bettles (Dendroctonus sp.). Risk
classes 1 and 2 indicate low-risk trees that would definitely be preserved
if trees were being marked for a timber sale. Classes 3 and 4 are high-risk
trees that would be marked for removal in a timber sale. In Table 12-5, the
changes in merchantable volume in board feet (bd ft) in all four classes are
recorded for two control plots in 1952, 1963, and 1972. The increases in
volume of high-risk trees since 1952 are remarkable; decreases in volume of
low-risk trees and total volume in the plots are very large. The total volume
decrease is related, first, to one-by-one removal of bark-beetle-killed trees
inside the plots indicated for certain by the increase in snags and current
stumps and, second, possibly to suppressed radial growth.
One of the objectives of the two 5-acre (2-ha) control plots was to
show what would have happened in the absence of sanitation salvage logging.
The distributions of trees in all categories in 1952, 1963, and 1972 (Table
12-5) suggest that by 1972 in plots 1 and 2 the sanitation salvage logging
12-42
-------
13
1 i
C/3
M
0
C?
a
oo
rH
4-1
cd
CO
CU
q!
•rl
PH
cu
M
MH
MH
cu
1-5
13
(3
cd
cd
CO
o
QJ
13
C3
O
PH
O
CO
CU
4-1 -. 1
4J CO
•H I
rH ON
Cd i— 1
4-1
M
O
13
p!
cd
CO
CU
o
o
C/3
E>i
^i
~j
•r-)
C
4-1
PI
cd
13
•rl
O
fi
•H
CO
CU
00
PI
o
p!
o
•H
>-, 4J
Vl CX
3 -H
•!-! rl
a o
M CO
CU
Q
13 5^2
01
4-1 »
cd >~,
r-f 4-1 -*
3 -rl r-~
C3 I rtfc
fS »"~l >Jl
3 Cd rH
CJ 4-1
CJ M
<$ o
S
-3-
o^
rH
>N 6^S
4-1
•H -
rH OJ
Cd 4-1
H (2
O CO
a r~~
ON
rH
>^ -*
vi ^~
3 ON
•f~l rH
f!/"t 1
rH 0)
p
D O
00 CJ
cd w
CU CO
*£ ON
,— j
58 L
^^
CU 4J CO
01 -H r-x
IH en ON
H G rH
CU
Q
en
CU
•H
O
OJ
a
4-1
0
rH
CU
u
cu
CU
en
r~^*"~"}
O O NO
O 0 rH
O O OO
o o o
O O 00
o o o
^
r-. ON r-~
rH CM CO
rH rH rH
-3- rH CO
CN m co
rH rH rH
oo o -*
CN CN >CT
rH
OH PH PH
>-3 Pi PH
1 — *
o
c/>
^—^ /~*.
o
X 0 ^
0) U PH
M ^-^
0 0
60 4J
M Pi CO
cu o cu
13 •- rl
•H O O
cu Pn
a cx
C/l O C/l
cu
4J
cd
^_l
cu
13
o
a
^^
, ^ "^
inunrHcN-a-u-i^rcooin
rHinCOrHrHrHr~-r~-HrH
inr-rHO-*mr--.vDom
rHCNCOOrHrHCOCOrHrH
Oi^OcNOOr^vOOO
OCNOrHOOCOcOOO
•JC -K -K ^< *K HC
^oo-3-inr~-oor--r^r-.m
u-l^DvOvDvOy30OONONO
rHi-HrHrHrHrHrHrHrHCN
mCOrHONU-|vO
4J Z 5
CU H CM
U •>-• ,! CU
. PL, /— ^ CU O % 01
§rH Cd Cd CU 1 — 1
CU rH rH rH rH
CO Cd 13 Pi Cd >
rl ^Pn Oi — l
0) N O 0) O O Pi
J>CUCX^(3CX4-14-1^CU
'HOlfl60C3SrlrlOCiJ
PirlCdO33cdCdPlrl
12-43
4-1
00
•H
rH
4-1 CO
_(~]
00 ^
•H rl
rH 01
C/3 >
'-^""l
O O O
OO O O
CN O O
r~ O o
CO O O
o o o
•K -X
OO CO rH
CN rH CM
CM CO CO
r^ -
CJ
K
&
^-^ ^,
O CU
0 Cj rH
N--1 M cd
cd ^
rH CU Pi
O ^ OJ
01 cd a)
CJ J M
o o
«4H
CX 4H •
i 3 w
Co rH •
0 M 3
1
o
s
CO
01
OrH
p^I ^ CN
•H
en
•H
>
*"-"" ^
ON O O
o o o
ON O O
000
o o o
o o o
•K -K
CM co r~
ON r^ r~-
CO *^" ^!"
o co
ffl
o
Q3*~s<\)
]TJ ,—f
^ PI rH
O cd
rl >^ t>
cd PI
PQ cd ja
o S
4-1 0
rl 13 O
Cd PI rH
a) cd o
S3 c/> S3
CO
^i
pi
a)
cu
3
4J
CU
•£>
rH
O
'^
•H
<~H
cd
p>
CO
c
0
en
•H
1-j
cd
CX
g
CJ
s^^
m
o
•
o
m
o
p>.
4-1
•H
i — !
•rl
.0
cd
rQ
o
vi
cx
4-1
cd
4J
a
cd
CJ
•H
W-l
•H
(3
00
•H
CO
cu
o
cu a
Vl 0)
cd vi
4-1 CU
CJ l*H
0) V4H
43 -H
13 .
QJ CO 4-1
CX CU O
4-1 rH
en cd cx
cu o
CU -HCU
Vl 13 rH
4J pi 60
•H pi
MH -H
O rM CO
eo
VJ -H cd
CU M
rQ CU 4-1
S 4-1 cd
3 eo
Z <
Cdl ,D|
-------
m
I
CX|
rH
Ol
rH
ft
cd
H
01
O 4-1
2s
H.S
4-J
rt co
4-J
CD Cd
Ol rH
CO [in
CD
cd a
rH 0
CJ 4-t
S-4 .->
.ii rt oo
CD W CO
•H
Oi 4J >
rt rt
O CXI J2
0) r-. bo
CO ON >H
C rH K
M
T)
>-i el a.
3 rt E
o «
pi-l CN CJ
in
el o\ <
•H rH CJ,
4-J >-}
co el co x^
01 01 Ol
ti 01 M rH
•H |S O
PL, 4J tu 4J
Ol O
0) rt PH
s-i oo a
M-l C O rH
M-l iH -H O'
a) 60 4J j-i
>-3 60 rt 4J
02 e
rH rJ O
rt o cj
4-1 Ol C
O 60 -rl
H M T3
t> r-l
CXI
ON
rH
0)
60 CD
cd 0)
C rJ
Ol H
CJ
M M-l
01 0
4-1
1^1
T3
o
1-J
01 -
4= Ol
S S
•H 3
H rH
O
^
O
O
rH
O
CO
f^
(S
cx|
in
CO
VD
0\
rH
01
60 CO
rt 01
4-J Q)
C M
0) EH
CJ
M M-l
Ol O
PJ
4-1
M-l
^3
j_,
01 .
J3 Ol
e i
•H 3
H rH
o
o
o
rH
O
CO
m
^
CO
VO
M-l rH rt i
o cd c
en ^4
Ol Ol
60 C M
rt o
.p T-i a
el 4-1 rt
o> cd co
O 4-1
M -H
01 a 'cxi
PLI rt
en
T3
el B
cd o
Ol M-l
g
3 T3
rH Ol
O T3
> 3
rH
VJ O
m
o\
rH
01
60
rt CD
4-1 Ol
C 01
Ol tJ
CJ H
Ol MH
P^ O
4-J
M-l
13
01
40 r.
S 01
•H €
H 3
H
O
O
0
rH
O
-J-
O
f.
CO
01 X
43 W
•9 CO
H 4-1
O
M-l rH
O PJ
CO rH
01 0
MM CO
fi 4J 01
a) pi co
43 O CO
cj u rt
rH
CJ
^
CO
•H
Pi
CO
Ol
co
CO
rt
rH
CJ
rH
rH
rt
n
rH
cd
4J
O
H
in ^o o oo
in rH CXI
o o o co
CO •* rH rH
P^ rH 00
co
oo vo r-
m
ml
CD
a
3
4-1
CD
4-J
Ol
tJ
CX| M
3
•O CJ
el
rt TS
C
rH rt
CO -3-
CO CD
ri^ ^ r^ 60
co co co rt
•H -H -H fi
a! e
CNI m r^-* ON
rH <3- CO OJ
rH
CO
ON
rH
^3 CNJ vQ ^O ^-O
o oo
rH
O O O O CO
\O 00 r*- rH rH
VD O rH ^J-
csj co O *
o o in co
CX| rH
rH rH
rt |
CO
a
e
4-1
CO
CD
01 4-1
CO fi
CD 01
cd M
rH CXI 1-1
CJ 3
TJ CJ
H a
rH Cd T3
cd d
rH rt
•» CO <1"
rH CO CD
rt ^ ^ ^ 60
4-J co co co rt
O -H -H -H C
H Pi Pi pi en
4J
CO
O
M
O
rH
rt
a
o
4-1
rt
o
•rt
T3
M
rt
S
M
01
CQ
C
cd
CO
oT
CJ
•H
M-l
M-l
O
CO
—
o
CO
•H
M
01
C/3
0)
4-1
B
o
M-l
T3
Ol
C
•H
cd
4-J
O
rt
4J
rt
0
o
•H
^t
01
a,
rt
01
i
o
rH
60
C
•H
j_j
3
•a
a
o
•H
4-1
cd
rH
3
3
o
CJ
cd|
12-44
-------
or timber sales would have removed 45% and 68% of overstory trees, respect-
ively. The more selective tree-by-tree salvage would have removed only 8%
and 10% of the overstory trees in plots 1 and 2, respectively. These results
must be treated as suggestions, not firm conclusions, because of the lack of
a more adequate statistical design, which should have included more plots
in additional stand types and sampling of several kinds of sites at various
distances from the pollution source. However, because of the suggested
impact, the sanitation salvage logging practice needs careful scrutiny.
Other information is available from the ponderosa pine subtype that suggests
that biomass production of overstory species is diminished in proportion
54
to the oxidant dose received. Parmeter et al. observed decreases in
height growth of ponderosa pine that showed injury symptoms. Injured
trees did not respond with greater growth during years with more favorable
soil moisture content; uninjured trees (often side by side with injured
trees) did have increased height growth in these years. McBride (in
3 la
Kickert et al. ) studied two populations, each including 19 ponderosa
pines dominant in their stands. One population ranged in age from 52 to
71 years in 1972, and the other, from 20 to 39 years. The influence of
tree age on ring width growth was minimized by comparing rings of equivalent
age in each population. The measured rings in the older group were produced
from 1910 to 1940, before the advent of "Los Angeles smog," and in the
younger group, from 1941 to 1971, when smog was present. After the
influence of precipitation on growth was evaluated, there was a difference
of 0.20 cm in average annual growth attributable to oxidant air pollutant
injury. In this sample, a 30-year-old tree subjected to air pollution would
be 24 ft (7.2 m) tall and 7.5 in. (19 cm) in dbh, with one 16-ft (48-m) log
having a volume of 30 bd ft. In comparison, a 30-year-old tree growing
12-45
-------
before the injury by oxidant air pollutants (1910-1940) would be 30 ft (9 m)
tall and 12 in. (30.5 cm) in dbh and could yield a 4.8-m log with a volume
of 80 bd ft. The impact of oxidant stress on forest growth is apparent
without further eleboration.
The growth suppression of ponderosa pine saplings has been demonstrated
by enclosing a group of 10 naturally seeded trees in the plastic-covered
72
greenhouses used by Thompson; enclosed trees were provided with activated-
charcoal-filtered air (FAH) from April through October 1968 - 1973 by
31a
Miller and McBride (in Kickert et al). The controls consisted of two
similar groups of trees, one in a greenhouse receiving unfiltered or ambient
air (AAH) and another group not enclosed (AAO). Precipitation was rare
during the summer enclosure period, and all three groups received the same
amount of winter precipitation. At the end of the 1973 growing season,
most of the saplings were harvested from each treatment for growth analysis.
One indicator of the response to these treatments was the length of annual
growth of terminal shoots and first-order branches in the upper half of
the saplings (Figure 12-15). After an initial lag in 1969 and 1970, the
growth of shoots and branches on the FAH trees increased dramatically. The
retention of annual needle whorls was remarkably different by 1973; needles
in internodes older than 1972 were completely absent from the AAH and AAO
trees. The decrease in needle biomass on the AAH and AAO trees for the
1973 whorl was 32 and 37%, compared with that on FAH trees (Figure 12-16).
Needle length and litter production furnish another important
measure of biomass decrease. In field studies, it was found that the
average amount of litter production increased with decreasing ozone injury
of selected ponderosa and Jeffrey pines (r = 0.55) and that the average mass
of needles per fascicle increased with decreasing ozone injury (r = 0.96).
Early studies suggested that injury to ponderosa pine was similar
in all size classes, but Cobb and Stark later reported higher mortality
12-46
-------
180
170
§,.50
uj 150-
KJ .33
S 120
£ MO
0.
TO
| 60.
< 50-
s
UI 40-
cr
u.
o ,„
MASS OF NEEDLES RETAINED PER iNTFRNODE BY
PONDEROSA PINE SAPLINGS M 1973
I AW3IENT ArR OUTSIDE
2 AMBIENT AR HOUSE
J FILTERED AIR HOUSE
I 2 5
1969 1970 1971 1972
YEAR INTERNOOE AND NEEDLES WERE PRODUCED
I 2 3
1973
FIGURE 12-16.
Average weight of all needle fascicles retained in 1973
per internode in filtered or unfiltered (ambient) air
greenhouses, and an outside ambient air treatment after
treatment since 1968. (Reprinted with permission from
Kickert et al.31a)
12-47
-------
rates in understory ponderosa pines (9-12 in., or 22.9 - 30.5 cm, in
diameter) than in larger size classes. The probable effect of tree
mortality on stand composition can be anticipated to some extent from an
example of the present species and size-class composition, as shown in
45
Table 12-6. In this severely damaged stand in the ponderosa pine-white
fir subtype, nearly 50% of the overstory and about 22% of the understory
is ponderosa pine. With all size classes considered, 16.1% had slight,
33.3% moderate, 31.2% severe, and 19.4% very severe injury. White fir
and incense cedar are well established in the understory, but their poorer
survivorship to 12.00-23.99 in. (30.5 - 60.9 cm) in dbh compared with
ponderosa pine suggests that other mortality factors have acted heavily
on them in the past. Incense cedar and sugar pine are the most tolerant
to oxidant, but sugar pine is present in very low numbers. The accelerated
mortality of ponderosa pines has particular significance in this ecosystem,
because it is the dominant member of the climax community.
The direct effects of ozone on plant species constituting the
shrub layer in the conifer forest are not yet sufficiently understood
to permit any conclusion to be drawn. In many sites where the conifer
overstory is well developed, the shrub species are excluded completely.
In more open pine stands, some shrubs are very common, such as skunk bush
(Amorpha californica) and white thorn (Ceanothus cordulatus). Of these
two species, only skunk bush shows highly visible chlorotic mottle of
leaflets and premature defoliation where ozone dosages are high. A shrub
species common to the lower chaparral zone, squaw bush (Rhus trilobata),
57
is even more susceptible to ozone injury. In the San Bernardino Mountains,
166 herb-layer species have been identified as common to the conifer forest.
12-48
-------
Table 12-62.
Tree Species and Size Composition on a Study Site Affected by
-------
The phenology of these species is being studied so that growth and flowering
can be correlated with soil moisture availability and seasonal changes of
ozone dose. Initial field observations suggest that at least 10 species are
obviously injured by total oxidant in areas receiving high dosages. These
areas have been subject to exposure for at least 20 years, so some species
18
or subspecies may have been completely eliminated. Dunn reported that
smog may have acted as a selective agent to remove oxidant-sensitive
subspecies of Lupinus bicolor from the Los Angeles area. Furthermore,
L.' latifolius appeared to have floral ontogeny inhibited without damage
to leaves, and _L. densiflorus was severely damaged by ambient total oxidant
at Claremont, California.
56
Price selected six important grass species found in either the
Gambel oak or quaking aspen communities in the Wasatch Mountains of Utah.
The selected species were fumigated under greenhouse conditions with ozone
varying from 0.15 to 0.30 ppm during each experiment. These treatments
caused a 53% reduction in top-growth biomass of the six species. The initia-
tion of reproductive structures of all species was inhibited, and the repro-
ductive potential of Bromus tectorum and ,B_. carinatus declined to zero.
These results suggest that the species composition of affected natural
communities could be altered. In other studies, 17 representative species
from the quaking aspen community were fumigated with ozone 3 h each day, 5
days/week, with ozone at 0.30, 0.15, and 0.05-0.07 ppm in the first two
cases and with ambient total oxidant in the last case. Experiments extended
through three seasons. At concentrations of 0.15 ppm or below, growth
reduction and stimulation were both observed in different species; growth
was reduced in all but 2 species at 0.30 ppm. Seed production was reduced
in 2 species at 0.15 ppm and in 3 species at 0.30 ppm, of the total of 6
25
species that produced fruits or seeds.
12-50
-------
77
In a third series of experiments, Treshow and Stewart fumigated
native plants growing naturally under field conditions. The threshold ozone
concentrations required to injure important species in the grassland-oak and
aspen-conifer communities during 2-h exposures were determined (Table 12-7).
Three important species — Bromus tectorum, Quercus gambelli, and Populus
tremuloides — were injured by a single 2-h exposure to ozone at 0.15, 0.25,
and 0.15 ppm, respectively; over half the remaining species showed visible
injury after exposure to 0.30 ppm or less. The implications for possible
imbalances in community stability are readily apparent if these plant
communities receive dosages similar to those typical in the San Bernardino
Mountains.
84
Yonkers et al. have tested the ozone susceptibility of 15 species
of annuals common to the Mojave Desert just north and east of the Los
Angeles basin (and San Bernardino Mountains). Compared with the susceptible
pinto bean plants included in the experiment with ozone at 0.35 ppm, Plantago
sp., Cercidium sp., and Prosopsis sp. were also sensitive. Further
interpretation of these results is complicated by the influences of plant
age and preexposure conditions.
Dose-Injury Observations with Ambient Oxidant and Native Ponderosa Pine
Saplings.—During 1969, 1970, and 1971, 10 sapling-size ponderosa pines
that received the ambient air outside (AAO) treatment for comparison with
trees enclosed in filtered- or ambient-air greenhouses were observed
to determine the rate of current-year needle growth and appearance of
3 la
oxidant injury symptoms on both current and 1-year-old needles. Forty
new needles on each tree were measured monthly (Figure 12-17, left); growth
leveled off in early September. Current-year and 1-year-old needles were
12-51
-------
Table 12-7-
Injury Thresholds for 2-hour-s Exposures to Ozone
Species
Grassland -Oak Ccm.-.yjnity Species
Injury
thresh-
old
(pphm
c:one)
injury'
ihrcsh-
olci
Tiees & Shrubs
Acer gr2,*~,'d-::-:2':,(m Nutt.
Xet/-;;^../:^L.
Ar!-.-..--'-!J !i;J-:-'3!a Xutt
/,/.7'.^ ••••- u r:,:5- G.Don
Cclcckcrtt'.s r.'.mdi.i icrr.
Cirsi'.irr. crceiise (L.) Seep.
Ccr.in.-r: n:ocn^sliim L.
Ifrdyssrum boreale Nutt.
Hclicn'ik'.is cr.nus L.
i /" _7* ' y
F>:ime.~ crisp:is L.
Urtica grsciif: Ait.
Glasses
Era:-us brizzeforrr.is Fisch. & Mcy.
/?,-/-".'J ledoriim L.
Foci j-re. leasts L.
A;p;-n and Cofiif-.-r Community Species
Trees & Sbrubs
yJi.Vs c^rc.'cr (Cord. crc G!end.) Lindl.
T.ehiicLier cln:.fc'.:a Nutt.
c.':; J.'.V;:.7 ,;,^rsi::il€; (T,-rsh) Raf.
over 40
o\er 25
40
o^er40
30
25
over 30
over 30
over 40
over 40
40
over 25
15
over 30
25
25
30
.over 40
30
15
25
• AOJJ v. crJ^n' Lindl.
Scn!::icii5 !r.r!::nocurj:n A. Gray
Sjrrpl-oriccrpjs i ore// 'u'/iVj Rvdb.
Perennial Forbs
slctr.CJ cr^!;!tt Nutt.
yi'^.'M/i/c/.u' iirticifola (l.'in'.h ) Kunt-.e
. 25
20
over 30
15
30
over 30
over 25
30
25
20
Perennial Forbs
Allhnn acumlr.alum Hook.
Angelica p'nrcia S.V/ats.
Asicr ci^cl^crr.: (Eat.) A.Gray
Co ex sicca.'z DiN'-ey
Cickoriiim iiiybus L.
Cirsi.im cr< £'-•;? (L.) Scop.
£pi!cbi'.ps:c!a Piper
O$rr.or'r.'::a cc-::dsr.lalis Torr.
Pl'.ncelia hfliropr.ylia Pursh
Polcmcn;:irr> fc':osisi'.m'.) O.E.Scliulr
Gdimn bifc!:'i,i:i V.'ais.
Guyepfiylitn: racc;rs^'.,.T, T. JL G.
Po[/~ont:!r, dc.i\;h:i'. Gieeri
Grasses
A$ropyron cn::'i nisi (L.) F-cauv.
}lroir,:/s ccr,'"j'i;s Moo!<- ^- AMI.
25
under 25
15
30
' 25
under-10
30
30
30
30
over 15
under 25
15
over 25
over 25
25
30
over 25
under -40
over 3D
25
under 25
30
30
under 30
" 15
over 25"
over 25
25
over 25
over 30
under 25
under 25
25
over 30
30
over 25
over 25
under 25
Reprinted with permission from Treshow and Stewart.77
12-52
-------
inspected monthly for amount of chlorotic mottle, necrosis, and abscission.
Each symptom was given a descriptive rating: 0, none; 1, very slight; 2,
slight; 3, moderate; and 4, severe. In Figure 12-17, an average of the 3
years shows that, by Julian day 250 (September 7), the current-year needles
had a visible-injury score of 2.2, indicating slight chlorotic mottle (sig-
nifying severe injury to the trees); there was usually no necrosis and almost
always no abscission of current-year needles. Symptoms developed more rapidly
on 1-year-old needles; the combined score of the current-year and 1-year-old
needles was about 9.
The accumulated ozone dose since June 1, which is associated with the
current-year and 1-year-old needle injury expressed on the left of Figure 12-17
can be roughly estimated by transferring the injury score to the right. For
example, the current-year needle score of 2.2 on September 7 is associated with
5 o
a total oxidant dose of 2.75 X 10 ug/m -h. These results assume that all the
air monitoring data were available, but on the average about 90% were available.
The dose-injury curve is apparently not linear as assumed, and interpretation
is further confounded by the random occurrence of injurious doses in the
field. Additional observations of ponderosa and Jeffrey pine are required
to define more completely the ozone or total oxidant dose response. The
development of a model relating injury to dose and important controlling
environmental variables is a high-priority need for understanding chronic-
exposure effects.
Effects on Reproduction
The effect of ozone injury on herbaceous plant reproduction has
been mentioned earlier in this chapter and in Chapter 11. Seed production
by annuals is influenced mainly by the environmental conditions of the current
12-53
-------
SYMPTOMS COMFiPED TO 3ATE AND
STAGE OF NEW NEE^IF GrC>,TH,
JUIt THRU senrw.HsTF 195». 1570. 1971
JULliN DATE
INCREASE OF VIS'atE NEEDLE STMPTOMS
COUPCRfO WITH TOTAL OXIMKT DOSE
ERCt*. P'NE SAPLINGS
RIM FORfST. CA
JUNE- SEPTEMBER
1969,1970. 1971
CURRENT PLUS
OHE-TtAR-OLD
NEEDLES
CURRENT >TAR
•CEDLES ALONE
OS
ACCUMULATED DOSE
FIGURE 12-17.
Development of oxidant injury symptoms on current and
current-plus-1-year-old needles of ponderosa pine
saplings, in relation to stage of current-year needle
growth and time during the summer season (left) and
in relation to total dose of oxidant (right). „..
(Reprinted with permission from Kickert et al. )
12-54
-------
year, but perennial woody plants — particularly conifers — are erratic
seed-producers. Intrinsic factors affecting cone production include age
and vigor; seasonal temperature and soil moisture are important environmen-
22
tal factors.
The effects of sulfur dioxide on cone production have been described
by Scheffer and Hedgecock and Pelz. Generally, the decrease in tree
vigor caused by the pollutant may eliminate or lower the frequency of cone
production and diminish the size, weight, and germination of seed. The
effects of chronic ozone injury on conifer seed production may be similar,
in that tree vigor is drastically reduced. The effects of chronic ozone
injury on ponderosa and Jeffrey pine seed production are under investigation
3 la
by Luck (in Kickert at al. )
Seeds from individual species may constitute the bulk of the diet
of small vertebrates, such as the deer mouse (Peromyscus sp.) and the western
gray squirrel (Sciurus griseus anthonyi). During periods of low seed
production due to diminished tree vigor, squirrels converge on the few
remaining vigorous ponderosa pines and consume about half the seed crop
before it matures and reaches the ground. In the areas severely affected
by ozone, squirrels return to the same trees year after year. After the
seed reaches the ground, other small vertebrates, such as mice, seek it out.
The habit of preferential seed use by small vertebrates may be a stress
acting additively with ozone injury to decrease seriously the regeneration
potential of ponderosa pine.
Indirect Effects
Most indirect effects of oxidant air pollutants on primary production
and reproduction would be mediated through changes in the physical environ-
28
ment resulting from disruption of stand structure. For example, Hursh
12-55
-------
described three microclimates in the area surrounding the ore smelter at
Copper Basin, Tennessee. These zones were distinguished by changes in air
and soil temperatures, winds, evaporation, air moisture, and rainfall.
Because sulfur dioxide was the pollutant in this case, there were also
changes in soil pH and sulfur content, which would not accompany oxidant
air pollution damage. Soil erosion increased dramatically.
Changes in such physical factors as light, temperature (particularly
maximums and minimums), relative humidity, and wind speed in forest communities
subject to structural alteration by mortality of susceptible species could
change the suitability of some sites for growth, reproduction, and reestablish-
ment of survivor species. We can only speculate on some of the possible
45
secondary effects until more data are gathered.
Wildfire is a very important factor in western forest ecosystems.
In the San Bernadino Mountains, the fire frequencies were determined by
J. R. McBride and R. Laven (in manuscript) in two stand types before and
after 1893, when the area was first set aside as a forest preserve and
fire protection began. Before 1893, the average interval between fires in
ponderosa stands was 12 years; after 1893, it was 24 years. The comparable
numbers for Jeffrey pine stands were 16 and 38 years. The buildup of heavy
fuels due to ozone-caused mortality and fire protection results in hotter
fires, and the thinning of the tree canopy results in increased rates of
14
fire spread. Hotter fires decrease tree survival. Moisture interception
by condensation in living tree crowns would decrease as the stands became
32
thinner, thus causing some sites to be drier.
EFFECTS ON CONSUMER POPULATIONS
Vertebrate Populations
The effects of oxidant air pollutants on vertebrates can be
segregated into direct and indirect categories. Direct effects are clinical
12-56
-------
and pathologic alterations of tissues that result from exposure to ambient
air. Indirect effects result from alterations in numbers or distribution
of the plant and animal populations exposed to ambient air. For example,
if air pollution eliminates or thins numbers of a susceptible plant species,
the food chain of the consumers that feed on it may break down. The result
could be a simpler and less stable ecosystem, with fewer plants and animals
in species and numbers.
The clinical and pathologic effects of oxidant air pollutants on
domesticated vertebrates have received little study in the laboratory. We
have found no major references to studies of these effects on free-ranging
native species. It is therefore necessary to extrapolate from laboratory
results to probable effects on wildlife in the field and forest.
Chapter 8 indicates that oxidant air pollutants may adversely affect
the olfactory and sight senses, degree of activity, general health and vigor,
reproductive rate, heart and kidney function, protein synthesis, respiratory
function, and disease resistance in domestic vertebrates in laboratory
conditions. Many of these adverse physical responses develop at or near
the concentrations of ozone currently experienced daily in ambient air in
parts of the San Bernardino Mountains.
Although it is risky to extrapolate from domestic species in a
laboratory to free-ranging species in the forest, it appears likely that
some wild vertebrates in the San Bernardino Mountains could be affected
adversely by their prolonged exposure to current concentrations of ozone.
Nitrogen dioxide, PAN, ozone, and environmental factors may act additively or syne
gistically to increase the overall stress on the individual. Potentially, the
direct effects of oxidant air pollution on wild vertebrates within a forest
system could be great. A reduction in visual or olfactory acuity or other
12-57
-------
loss of health or condition could be a serious handicap for a predator
whose survival depends on overcoming prey, and equally serious for the
prey that survives by staying one jump ahead of a predator.
In the San Bernardino Mountains, our goals have been to describe
the terrestrial vertebrate community within this mixed-conifer forest,
particularly in relation to ponderosa and Jeffrey pine stands, and to
determine the effects of oxidant air pollutants on this community. The
possible interactions of vertebrates in this system are shown in Figures
12-9 through 12-12.
The most abundant species of small mammals were selected to exemplify
vertebrate interactions, because of the importance of this group as seed-
eaters. The results from trapping of abundant species show that the deer
mouse (Peromyscus spp.) is the most numerous. Chipmunks (Eutamias spp.),
the golden-mantled ground squirrel (Callospermophilus lateralis), the
dusky-footed woodrat (Neotoma fuscipes), the meadow mouse (Microtus californi-
cus), and the harvest mouse (Reithrodontomys megalotus) are the other common
33
small mammals. Numbers have fluctuated widely from year to year and
from plot to plot, as is characteristic of small-mammal populations. Deer
mouse numbers fluctuate the laost. Preliminary analysis indicates that the
same species of small mammals are present in this forest as were reported
33
from similar trappings 70 years ago. Thus, it appears that oxidant air
pollution has not yet resulted in a reduction in the diversity of this
component of the vertebrate fauna. Population numbers of the common small-
mammal species do, however, appear to be low, in comparison with other
31a
similar forest regions. This is particularly true for the study plots
in areas of heavy oxidant air pollution. We have not yet determined whether
these low population densities of small mammals are directly or indirectly
related in any measure to the oxidant air pollution. These differences
12-58
-------
may result from variations in other aspects of habitat quality. For example,
the study plots in the areas of heavy oxidant air pollution are dominated by
ponderosa pine and have sparse shrub cover, whereas the study plots in areas
of light oxidant air pollution are dominated by Jeffrey pine and have much
u v 31a
more shrub cover.
When changes occur in one part of an ecosystem, the intimate nature
of the interrelationships results in changes in many other parts. Any
factor that causes change in one component of a system potentially affects
all subsystems of that ecosystem. The most important indirect effects of
oxidant air pollutants on vertebrates are those resulting in changes in the
habitat. Foremost among these effects are those on the vegetation and
the successional patterns of the plant community. Because of the high
degree of interrelationship and interaction between the vegetation, the
fauna, and the inorganic matrix of an ecosystem, effects of air pollution
on the vegetation potentially can result in changes throughout the ecosystem.
Damage to vegetation is probably the most important effect of chronic, low-
concentration air pollution on wildlife. Ponderosa pine, Jeffrey pine, and
black oak are all susceptible to damage, and these are the most important
trees within the forest as providers of food and habitat for wildlife. A
similar selectivity by species doubtless occurs within the shrub and herb
layers of the vegetation. The long-term effects will be reduced production
of fruits and seeds and elimination of the sensitive plant species and,
therefore, reduction in the diversity of the vegetation. In turn, this will
lead to a reduction in abundance and diversity of the vertebrate fauna.
Q O
Likewise, Woodwell's prediction of enhancement of the activity
of insect pests and some disease agents (which has been demonstrated on
this forest) could lead to an increase in vertebrate species that feed
on invertebrates or utilize dead plants for cover. Birds would be the
12-59
-------
most likely to increase and, to a lesser extent, such small mammals as
deer mice, which are partially insectivorous.
Fruit and seeds make up the largest part of the diet of most of
the common small mamals on our study sites, particularly the deer mouse,
harvest mouse, chipmunk, ground squirrel, and western grey squirrel (Sciurus
griseus). The grey squirrel is an excellent example of the interactions
within this forest and of the potential effects of oxidant air pollution.
It is abundant throughout the mixed-conifer type, depending specifically
on the pines and oaks for the majority of its food, cover, and nest sites.
This squirrel eats or stores a major portion of the pine and oak seed crops
each year. On some yellow pine trees on our study plots, grey squirrels
cut more than 2,000 cones per tree.
Thus, tree squirrels are a major source of loss of seeds of
ponderosa, Jeffrey, and sugar pine and of black oak acorns. Vertebrates,
then, can have a major effect on the reproduction of these species, particu-
larly because the grey squirrel is only one of numerous species in this
forest that feed on conifer seeds and acorns.
An alteration of the balance between pine and oak, a change in squirrel
populations, or a reduction in any of the mast crops brought about by oxidant
air pollution obviously could have a major impact on this forest, particularly
on tree reproduction and successional patterns. Reductions in conifer seed
crops as a result of air pollution has been suggested in other forests,
where cone production was lowered and size, weight, and germination ability
55, 60
of the seeds were reduced.
Another way that oxidant air pollution could affect this subsystem
is through an alteration in forest moisture. Elimination of vegetation cover
allows the exposed soil to dry more rapidly, which would affect soil-burrowing
and soil-inhabiting vertebrates. The lower moisture content may reduce or
12-60
-------
inhibit fruiting-body formation of fleshy fungi. These fleshy fungi are an
important food source for tree squirrels, making up a third or more of their
diet in some seasons. A reduction in this food source doubtless would result
in an even greater utilization of conifer seeds and acorns, reducing further
the reproductive capabilities of these trees and eventually limiting future
food supplies for the squirrel population.
In summary, subtle and simple initial changes may radiate and
magnify throughout all trophic levels of the ecosystem. Restoration of
the system may be impossible.
Kacroarthropods
2
Laboratory studies have indicated that ozone at 196 pg/m (0.10
ppm) was lethal to adult houseflies (Musca domestica L.) and caused them to
2
lay fewer eggs. Two cockroach species (Paraplaneta americana L. and
Nauphoeta cinerea, Oliver) and the red fire ant (Solenopsis invicta Buren)
were exposed to ozone at 588 ;ug/m (0.30 ppm) for up to LO days. There was
no unusual mortality or evidence of direct injury to individual insects.
The fire ant workers were stimulated to migrate inside their nest initially,
but further observations indicated no disruption of social behavior. These
reports do not suggest that free-ranging insects would be directly affected
by ambient concentrations of ozone in natural ecosystems or agroecosystems.
The indirect effects of ozone through modification of the availa-
bility of food for insects, particularly in a conifer-forest ecosystem, has
received some investigation. ' The weakening of ponderosa pines by
chronic exposure to ozone makes them more vulnerable to successful infesta-
tion by pine bark beetles (Dendrqctonus brevicomis and _D. ponderosae).
Figure 12-18 shows a positive relationship between degree of tree injury and
frequency of bark beetle infestation and the relative frequency of attack
12-61
-------
SF .^ f*
WJJftTT
SMOG INJURY RATING
I
I 20
M
'.Iv^CO'-'-S CNLT
V;H-EO BY uorw :
SMOO IUJ'JflY RATING
FIGURE 12-18.
Relationship between degree of oxidant injury to ponderosa
pines and bark-beetle attack (left) and numbers of trees
killed by western pine beetle, mountain pine beetle, of
the two species together (right). (Reprinted with permission
from Stark and Cobb. )
12-62
-------
by the two species of bark beetles. The relationship (see Figures 12-9
through 12-12) between tree health and brood productivity and the population
dynamics of bark beetles and their insect associates in infested trees are
31a, 70
being investigated. Pine bark beetles have been a constant threat
to ponderosa pines in the San Bernardino Mountains for many years, since
67
before the inception of oxidant air pollution injury. Bark beetles are
a key element responsible for accelerating the modification of stand structure.
Plant Parasites and Symbionts
Parasitic Phanerogams. Both true mistletoe and dwarf mistletoe are common
parasites of forest tree species. The true mistletoes (Phoradendron sp.)
occur commonly on California black oak and white fir and less often on incense
cedar in the San Bernardino Mountains. No direct effects of oxidants have
been noted on the mistletoe plant itself under field conditions. The true
mistletoe obtains mainly water from its host and would be indirectly affected
by debilitation of the host tree. The dwarf mistletoes (Arceuthobium sp.)
are common on ponderosa, Jeffrey, and sugar pines in the San Bernardino
National Forest. They depend on their host for both water and carbohydrates.
Heavily infected or "broomed" branches on ponderosa or Jeffrey pines severely
injured by ozone often have more annual needle whorls retained than do uninfec-
ted branches on the remainder of the tree. The needles are also greener.
It can be hypothesized that the infected branch is a carbohydrate sink where
a pooling of carbohydrates occurs; higher carbohydrate concentrations may be
instrumental in either preventing or helping to repair ozone injury to needles
on the broomed branches. In the long term, stresses from mistletoe and ozone
are probably additive and hasten tree death.
Parasitic Fungi. Fungi that infect above-ground plant parts causing leaf
or stem diseases may be directly affected by ozone, as discussed in Chapter 11.
12-63
-------
Ozone injury to needles of eastern white pine increased infection by
12
Lophodermium pinastri and Pullularia pullulans. These results suggest
that leaf tissue of many species may be made susceptible to fungi that are
normally saprophytes but may be low-grade parasites when circumstances permit.
In the San Bernardino National Forest, the needle- and twig-
infecting fungus Elytroderma deformans is a common fungus disease of ponde-
rosa and Jeffrey pines. The additive stresses of ozone and fungus on the
host may hasten tree decline in severe cases. In some situations, it appears
that infected or broomed twigs may die sooner than uninfected twigs at the
31a
same position in the tree. Observations are continuing.
Root-infecting fungi, such as Armillaria mellea and Fomes annosus,
are generally more virulent pathogens when they encounter trees already
weakened by other stresses. This observation has been made mostly in
Europe, where sulfur dioxide was the principal pollutant; the spread and
virulence of j?. annosus across the gradient of decreasing oxidant dosage
31a
are being studied in the San Bernardino Mountains.
Significant increases have been reported in length of root tissue
colonized by annosus when artificially inoculated ponderosa and Jeffrey
pine seedlings were fumigated with ozone at 431 pg/m^ (0.22 ppm) and 888 fig/m
3 la
(0.45 ppm) 12 h/day for 58 and 87 days.
Beneficial mycorrhizal fungi infect the small feeder roots of
trees and other plants. The resulting relationship is symbiotic and involves
an intimate exchange of minerals and essential metabolites. The host tree
benefits through increased efficiency of nutrient uptake from the soil. Any
interruption or imbalance of the exchange of materials between the host root
tissue and the fungus mantle surrounding it can have deleterious effects on
the fungus and the host. Such stresses as air pollution injury to the host
24
undoubtedly disrupt this balance. The feeder rootlet system of ponderosa
pines in the San Bernardino Mountains and those of eastern white pine have
12-64
-------
shown remarkable deterioration involving diminished numbers of mycorrhizal
54
rootlets, which are replaced by saprophytic fungi that decay smaller rootlets.
EFFECTS ON DECOMPOSERS
Although some of the solar energy fixed by producing plants is
released by the respiration of these plants and of animals, much of it is
stored in dead organic matter until released by decomposer organisms at
rates that vary greatly with place, season, and kind of organic matter.
Generally, one-third or more of the energy and carbon annually fixed in
53
forests is contributed to the forest floor as litter, mostly leaves.
Because litter is generally related to the quantity of photosynthetic
tissue in the ecosystem, it is a useful index of ecosystem productivity.
One of the predicted effects of pollutants on ecosystems suggested
83
by Woodwell is a reduction in the standing crop of organic matter, which
would lead to a reduction in nutrient elements held within the living system.
The evidence discussed earlier definitely shows that primary production is
much lower in an ozone-stressed conifer-forest ecosystem. This result
would be anticipated in all similarly stressed natural ecosystems or
agroecosystems.
The reservoir of energy and mineral nutrients represented by
litter is a very important resource in natural ecosystems with closed nutrient
cycles. The growth of new green plant tissue depends on the slow release of
nutrients by decomposer organisms. In agroecosystems geared for high
producticn, litter is often removed or burned, and fertilizer is added to
the soil; the nutrient cycle is open and subsidized.
In a conifer forest, litter production and decomposition release
about 80% of the total minerals in the biomass of the stand; the remainder
41
is retained in the living parts of the tree. Standing dead material is
not considered litter.
12-65
-------
In terrestrial ecosystems, most decomposers occupy the mantle
of litter or the surface layers of the soil, where they supply the necessary
recycling mechanisms to convert dead plant or animal material into humus and
eventually into minerals, gases, and water. Small animals, arthropods, fungi,
and bacteria exist as a complex in intricate food chains in which they feed
not only on dead material, but also on one another, ultimately releasing the
mineral nutrients needed by the producer populations. Without the decomposers,
some essential elements — such as calcium, phosphorus, and magnesium — would
concentrate in the litter until the supply in the soil was depleted; growth
of green plants would then be seriously limited.
Direct Effects
The decomposition of tree leaves is not entirely confined to the
litter layer on the forest floor. Leaves and needles are invaded by bacteria
and fungi even as they grow; these microorganisms may be either pathogens or
29
saprophytes.
The first possible interaction between ozone and decomposer organisms
might be with the bacteria and fungi that occupy the surface of the living
green leaf. The direct effects of ozone on microorganisms are discussed in
Chapter 11, but very little conclusive information is available that can be
applied to natural conditions.
It is not known whether ozone, PAN, or other oxidants could have
any direct influence on decomposer organisms in the litter layer; however,
there does appear to be a rapid flux of ozone to soil surfaces. The ozone
flux to some kinds of surfaces constituting ecosystems—e.g., vegetation, soil,
and water—has been determined by Aldaz; he expressed the flux as molecules
per square centimeter per second times 10. The relative fluxes into
o
different surfaces, assuming an ozone concentration of 40 jig/m , were:
12-66
-------
fresh water, 0.5; snow, Q.9; grass, 1.1; sand or dry grass, 5; and juniper
bush, 10. Furthermore, it was found that bare soil destroyed about 75% more
ozone when dry than when moist. The determination of ozone flux to surfaces
may be a far more realistic measure of dose to living organisms than atmospheric
46
concentration of ozone, according to Munn.
Indirect Effects
The concentration of plant nutrients in litter influences both the
rate of decomposition and the amount of nutrients released after decomposition.
Ozone-injured foliage may be deficient in inorganic nutrients, because of the
54
concomitant decay of the root systems of chronically injured trees.
Coniferous leaf litter is more resistant to decomposition than
41
broad-leaved litter. Both low inorganic nutrient status and the presence
of organic compounds that are toxic to microorganisms may account for slower
decay. Ozone injury to needles or broad leaves might result in an accumula-
tion of phenolic compounds that are toxic to bacteria and fungi. The rate
of litter decomposition might be decreased. A high carbon:nitrogen ratio
related to nitrogen deficiency may also slow decomposition.
31
Katz and Lieth have categorized the roles of both microflora and
microfauna groups in litter decomposition. They have discussed the success-
ional trends of microflora and microfauna populations during the warm season.
A typical problem emerges when population sampling is attempted: "a consis-
tent feature of communities is that they contain a comparatively large
49
number of species that are rare at any given locus in time and space."
The task of identifying interactions (see Figures 12-9 through 12-12) of
decomposer populations with pollutants, particularly oxidants, is formidable.
In the San Bernardino Mountains, studies are going on to describe
the effects of oxidant injury to ponderosa and Jeffrey pines on the microar-
thropods and fungi of the litter layer under trees with various degrees of
12-67
-------
injury. Initial observations suggested lower population densities of
microarthropods in the classes Insecta, Arachnida, and Myriapoda under some
31a
severely injured trees.
A coincident effect on decomposers may be from the accumulation of
heavy metals, such as lead, which is entrained in the photochemical oxidant
59
complex. In Sweden, Ruhling and Tyler have preliminary evidence that litter
decomposition rate in a spruce forest was limited by increased concentration
of heavy-metal ions, but only during times of the year when water and tem-
perature were not limiting factors.
The difficulties of understanding population changes of litter-
decomposing microflora and microfauna as an index of pollutant effects suggest
that a more simple approach should be used at the outset. The least sophisti-
51
cated expression of accepted procedure is:
Ax
— = income for interval - loss for interval,
At
where Ax is the change in amount of litter over the interval t. This express-
ion describes energy storage in litter and indicates the balance between
producers and decomposers. Typical annual litter production, steady-state
accumulation on the forest floor, and associated decomposition rate factors
51
have been estimated for several locations and types of forest litter.
Comparisons of litter decomposition rate factors under similar stands of trees
subjected to various doses of oxidant air pollutants could be useful for
quantifying the dynamics of ozone-induced tree decline. This approach is
3 la
being investigated by Arkeley (in Kickert et al. ) in the San Bernardino
Mountains.
Sophisticated decomposition models are being developed. A simulation
o
model developed by Bunnell and Dowding for tundra sites is a nine-compart-
ment model with 23 transfers between compartments. This type of model may
provide the only method for understanding the extremely complex litter
decomposition process.
12-68
-------
In summary, it is anticipated that decreasing litter production by
green plants experiencing pollutant stress would result in a similar reduction
in the inventory of nutrient elements held within the system, owing to the
37
interruption of cycling pathways and mechanisms of nutrient conservation.
CONCLUSIONS
The transport of injurious concentrations of ozone and other oxidants
to rural areas downwind from urban centers at numerous locations in the United
States appears to be on the increase. ' Blumenthal j^t al. conservatively
estimate that the urban plume from the Los Angeles area "could cause ozone
concentrations to exceed the Federal standard of 0.08 ppm at locations as
far as 260 km." Other areas where significant rural concentrations of oxidant
have been observed are Salt Lake City, Denver, and the Blue Ridge Mountains.
In general, the permanent vegetation constituting natural ecosystems
receives much greater chronic exposure, and the short-lived higher-value
vegetation constituting the agroecosystem of the Los Angeles coastal plain
can be subject to injurious doses, but in intermittent short-term fumigations.
Each situation has measurable economic and aesthetic effects, but on
different time-scales. The single agricultural ecologic system (the
agroecosystem) has little resilience to pollutant stress; losses are
sometimes immediate and occasionally catastrophic. The complex natural
ecosystem is initially more resistant to pollutant stress, but the longer
chronic exposures cause disruption of both structure and function in the
system that may be irreversible.
47 52
Simulation models of ecosystem subsystems are developing rapidly. '
They deal with flows of energy, biomass, mineral nutrients, water, numbers
of species, population densities, and area occupied per biotic unit. Inter-
actions between ecosystem components must be understood before prediction can
be attempted. Simulation models offer a bright opportunity for determining
12-69
-------
the long-term effects on natural ecosystems and agroecosystems. New knowledge
of biologic effects should suggest the importance of prevention and some means
for ameliorating damage.
Oxidant injury to the mixed-conifer stands of the San Bernardino,
Mountains beginning in the early 1940's is well advanced. A similar problem
is developing in the forests of the southern Sierra Nevada. Both places
show both direct and indirect effects on all subsystems of the forest eco-
system — producers, consumers, and decomposers. For example:
• Ozone injury limits biomass production by the primary
producers and their capacity to reproduce.
• The decrease of biomass or energy flow to consumer and
decomposer in the ecosystem affects the populations of
these organisms.
• Essential recycling processes, such as recycling of
nutrients, may be interrupted, further limiting primary
production.
• Stand structure is altered rapidly in some areas by salvage
logging of high-risk trees; as a result, species composition
is changing, and wildlife habitat is being altered.
Oxidant injury to eastern white pine in some forest stands in
the eastern United States is a significant problem. There is an important
concern about injury caused by a synergistic reaction between ozone and
sulfur dioxide at low concentrations.
The relationship between man's welfare and stable natural ecosystems
and agroecosystems can be established in terms of the economic and aesthetic
values derived from them. In some situations, where ecosystems are stressed
by oxidant pollutants, the benefits realized by present and future generations
may soon diminish. Considerable research is required to find alternatives that
prevent stress or that may salvage some of these benefits. New management
12-70
-------
strategies should be instituted only when their consequences are predictable
within reasonable limits.
RECOMMENDATIONS
The present knowledge of the biologic consequences of chronic
oxidant injury to both natural ecosystems and agroecosystems must be communi-
cated to groups in the public sector that work in planning and enforcement.
The indirect effects on man's health and the direct effects on his welfare
resulting from ecosystem deterioration due to oxidant injury are serious
enough to be given more thorough consideration in all decisions related to
abatement of air pollution from both mobile and stationary sources. Land-use
planning and proper airshed classification should be used to prevent further
deterioration of air quality, particularly in prime timber-producing areas
and in remote, pristine areas, regardless of their present use designation.
The most important research needs are related to the determination
of the responses of natural ecosystems and agroecosystems to chronic exposure
to oxidant pollutants. In particular, chronic-dose-response models are needed
to understand the responses of the dominant primary-producer species constituting
forest ecosystems in both the eastern and the western United States. The result-
ing alteration of interactions with other subsystems—e.g., consumers and
decomposers—must also be investigated.
12-71
-------
REFKRliNCi:S
1. Aldaz, L. Flux measurement o£ atmospheric ozone over land and water, pp.
In V. H. Regener and L. Alci^z, Eds. Studies of Atmospheric Ozone.
Air Force Cambridge Research Laboratories. AFCRL-69-0]38, 1969.
2. Beard, R." L. Observations on house flies on high-ozone environments. Ann.
Entomol. 3oc. Amer. 58:404-405, 1965.
3< Berry, C. R., and L. A. Ripperton, Ozone, as possible cause of white pine
emergence tipburn. Phytopathology 53:552-557, 1963.
4. Berry, C. R. White pine emergence tipburn, a physiogenic disturbance.
U. S. Department of Agriculture, S. E. Forest Experiment Station
Paper 130, 1961. 8 pp.
5. Blumenthal, D. L. , W. H. White, R. L. Pesce, and T. B. Smith. Determination
of the feasibility of the long-range transport of ozone or ozone precur-
sors. Environmental Protection Agency EPA 450/3-74-061., 1974. 92 pp.
6. Botkin, D. B.~> and R." S." Miller. Complex ecosystems: Models and prediction.'..
Amer. Sci. 62:448-453, 1974.
7. BrySOrt, R. A., and W. M. Wendland. Climatic effects of atmospheric pollu-
tion, pp. 130-138. In S. F. Singer, Ed. Global Effects of Environ-
mental Pollution. New York: Springer-Verlag New York, Inc., 1970.
8. Bunnell, F. L., and P. Dowding.
In U. S. Participation in the International Biological Program.
Biomc Report No. 73/6, 1973.
9. California Air Resources Board. Air Quality in the Tnhoe Basin, Summer
1974. 26 pp.
12-72
-------
10. Cobb, F." W."', Jr., and R.~' wV Stark. Decline and mortality of smog-injured
ponderosa pine. J. Forest 68:147-149, 1970.
11. Corn, M. , R. W. Dunlap, I. A. Goldmuntz, L. H. Rogers. Photochemical
oxidants: Sources, sinks, and strategies. J. Air Pollut. Control
Assoc. 25:16-18, 1975.
12. Costonis,,A, C, Relationships of Ozone, Lophodermium pinastri and Pullularia
pullulanus to Needle Blight of Eastern White Pine. Ph.D. Thesis.
Ithaca, N.Y.: Cornell University, 1968. 184 pp.
13. Costonis, A. C., and W. A. Sinclair. Susceptibility of healthy and ozone-
injured needles of Pinus strobus to invasion by Lophodermium pinastri
and Aureobasidium pullulans. Eur. J. For. Path. 2:65-73, 1972.
14. Countryman, C. M. Old growth conversion also converts fire climate. Proc.
Soc. Amer. Forest. 1955:158-160.
15. Curlin, J. W. Models of the hydrologic cycle, pp. 26S-2S5. In D. E. Reichle,
Ed. Analysis of Temperate Forest Ecosystems. New York: Springer-Verlag,
1970.
l_ga Davis, D. D. , and F. A. Wood. The relative susceptibility of eighteen coni-
ferous species to ozone. Phytopathology 62:14-19, 1972.
17. fcoctiirtger, L," S,', F." W." Bender, F." L." Fox, and w," W." Heck. Chlorotic dwarf of
Eastern white pine caused by an ozone and sulphur dioxide interaction.
Nature 225:476, 1970.
18> Dunn, D.' B,' Some effects of air pollution on Lup jnus in the Los Angeles area.
Ecology 40:621-625, 1959.
19. Edinger, J. G., M. H. McCutchan, p. R. Miller, B. C. Ryan, M. J. Schroeder,
and J. V. Behar. PenetMtion and duration of oxidant air pollution in
the south coast air basin of California. J. Air Pollut. Control Assoc.
22:882-886, 1972.
12-73
-------
20. Edinger, J. G. Vertical distribution of photochemical smog in Los Angeles
basin. Environ. Sci. Technol. 7:247-252, 1973.
20a. Ellertsen, B. W., C. J. Powell, and C. 1. Massey. Report on study o£
diseased white pine in Tennessee. Mitt. Forstl. Bundesversuchanst.
Wien. 97:195-206, 1972.
2] m Ewing, B., P. Rauch, and J. F. Barbieri. Simulating the dynamics and struc-
ture of population, pp. . In Third Annual Integrated Pest Manage-
ment Modellers Conference, Berkeley, California, January 1975. Univer-
sity of California, Lawrence Radiation Laboratory.
22. Powells, H." A., and G-." H." Schubert. Natural reproduction in certain cutover
pine-fir stands of California J? Forest. 49:192-196, 1951.
23. Giese, R.~'L., R." M.'Peart, and R.~ T. Huber. Pest management. Science 187:
1045-1052, 1975.
24. Hacskaylo, E. The Torrey symposium on current aspects of fungal development.
IVT" Dependence of mycorrhizal fungi on hosts. Bull. Torrey Bot. Club
100:217-223, 1973.
25. Harvard, M. R. The Impact of 6zone on the Understory plants of the Aspen
Zone. Ph.D Thesis. Salt Lake City: University of Utah, 1971. 104 pp.
26. Hooven, E. F. The influence of forest succession on populations of small
animals in western Oregon, pp. 30-34. In H. C. Black, Ed. Wildlife and
Reforestation in the Pacific Northwest. Proceedings of a Symposium held
Sept. 1968, Corvallis, Oregon State University, 1969.
27. Horton, J. S. Vegetation Types of the San Bernardino Mountains. U. S.
Department of Agriculture Forest Service Technical Paper No. 44,
1960. 29 pp.
12-74
-------
28. Hursh, C. R. Local Climate in the Copper Basin of Tennessee as Modified by
r
Removal of Vegetation. U. S. Department of Agriculture Circular No.
774, 1948. 38 pp.
29. Jensen, V. Decomposition of angiosperm tree leaf litter, pp. 69-164. In C.
H. Dickinson, and G. J. F. Pugh, Eds. Biology of Plant Litter Decomposi-
tion. Vol. 1. New York: Academic Press, 1974.
30. Kadlec, J. A. A Partial Annotated Bibliography of Mathematical Models in
Ecology. University of Michigan, Ann Arbor, 1971.
31< Katz, B. A., and H. Leith. Seasonality af decomposers, pp. 163-184. In H.
Leith, Ed. Phenology and Seasonality Modeling (Ecological Studies:
Analysis and Synthesis, Vol. 8). New York: Springer-Verlag, 1974.
31a. Kickert, R. M., P. R. Miller, 0. C. Taylor, J. R. McBride, J. Barbieri, R.
Arkeley, F. Cobb, Jr., D. Dahlsten, W. W. Wilcox, J. Wenz, J. R. Parmeter,
Jr., R. F. Luck, and M. White. Photochemical Air Pollutant Effects on
Mixed Conifer Forest Ecosystems—A Progress Report. Contract No. 68-03-
0273, U. S. Environmental Protection Agency, Corvallis, Oregon, 1975.
<
32. Kittredge, J. Forest Influences. New York: McGraw-Hill Book Company, Inc.,
1948. 394 pp.
33. Kolb, J. A., and M. White. Small mammals of the San Bernardino mountains.
Calif. Southwest. Naturl. 19:112-113, 1974.
34. Kowctl, N. E. A rationale for modeling dynamic ecological systems, pp. 123-1^4.
In B. C. Patten, Ed. Systems Analysis and Simulation in Ecology. Vol. 1.
New York: Academic Press, 1971.
35. Lassiter, R. R. , and D. W. llayne. A finite difference model for simulation of
dynamic processes in ecosystems, pp. 367-440. In B. C. Patten, Ed. Sys-
tems Analysis and Simulation in Ecology. Vol. 1. New York: Academic
Press, 1971.
12-75
-------
36. Levy, R. , D. P. Jouvenaz, And H. I. Cromroy. Tolerance of three species o£
insects to prolonged exposures to ozone. Environ. Entomol. 3:184-185,
1974.
37. likens, G. E., and F. H. Borman. Nutrient cycling in ecosystems, pp. 25-67.
In Wiens, Ed. Ecosystem Structure and Function. Proceedings of 31st
Annual Biology Colloqium. Corvallis: Oregon State University Press,
1971.
38. Linzon, S. N. Semimature-tissue Needle Blight of Eastern White Pine and
Local Weather. Ontario Department of Forestry, Research Laboratory
Information Report' )-X-l, 1965.
39. McBride, J. R., and R. Laren. Fire frequency in the Ponderosa and Jeffrey
Forests of the San Bernardion Mountains, California. (in press)
40. McCutchan, M. H., and M. J. Schroeder. Classification of meteorological
patterns in southern California by discriminant analysis. J. Appl.
Meteorol. 12:571-577, 1973.
41. Millar, C, S. Decomposition of coniferous leaf litter, pp. 105-128. In C.
H. Dickinson and G. J. F. Pugh, Eds. Biology of Plant Litter Decomposi-
tion. Vol. 1. New York: Academic Press, 1974.
42. Miller, P. R., and A. A. Millecan. Extent of oxidant air pollution damage
to some pines and other conifers in California. Plant Dis. Reptr. 55:
555-559, 1971.
43. Miller, P. R., M. H. McCutchan, and B. C. Ryan. Influence of climate and
topography on oxidant air pollution concentrations that damage conifer
forests in southern California. Mitt. Forst. Bundes-Versuchsanst. Wien.,
97:585-607, 1972.
12-76
-------
44. Miller, ?T R., M.~' H." McCutehan, and H." P." Milligan. Oxidant air pollution in
the Central Valley, Sierra Nevada foothills, and Mineral King Valley of
California. Atmos. Environ. 6:623-633, 1972.
45. Miller, P. 1. Oxidant-induced community change in a mixed conifer forest.
Adv. Chem. Ser. 122:101-117, 1973.
46. Munn, R. E. Biometeorological Methods. New York: Academic Press, 1970.
336 pp.
47. National Research Council. U. S. National Committee for the International
Biological Program. U. S. Participation in the International Biological
Program. Washington, D. C.: National Academy of Sciences, 1974. 166 pp.
48, Terrestrial ecosystems, pp. 277-315. In Patterns and Perspectives in Environ-
mental Science. (Prepared for the National Science Foundation) Washing-
ton, D. C.: U. S. Government Printing Office, 1972.
• •• i t '
49. Odum, E. P. Ecology. New York: Holt, Rinehart and Winston, Inc., 1963.
152 pp.
50, Odum, E. P. Ecosystem theory in relation to man, pp. 11-24. In Wiens,
Ed. Ecosystem Structure and Function. Proceedings of 31st Annual
Biology Colloquim. Corvallis: Oregon State University Press, 1971.
51. Olson, J. S4 Energy storage and the balance o£ producers and decomposers in
ecological systems. Ecology 44:322-331, 1963.
52. Oneill, R. V., J. M. Hett, and N. F. Sollins. A Preliminary Bibliography
of Mathematical Modeling in Ecology. ORNL-IBP-70-3. Oak Ridge
National Laboratory, 1970. 97 pp.
53. Ovington, J.' D. Dry-matter production by Pinus sylvestris L. Ann. Bot. NS
21:287-314, 1957.
12-77
-------
54. Parmeter, J, R., Jr., R. V. Bega, and T. Neff. A chlorotic decline of
ponderosa pine in southern California. Plant Dis. Reptr. 46:269-273,
1962.
55. Pelz, E. Untersuchungen tiber die Fruktification rauchgeschadigter Fichten-
bestande. Arch. Forstwesen 12:1066-1077, 1963. (summary in English)
56. price, H. E. Effects of Ozone on Growth and Reproduction of Grasses. Ph.D.
Thesis. Salt Lake City: University of Utah, 1973. 84 pp.
57. Richards, B. L., Sr., 0. C. Taylor, and G. F. Edmunds, Jr. Ozone needle
mottle of pines of southern Californir. J. Air Pollut. Control Assoc.
18:73-77, 1968.
58. Rochow, J. J. Simulating ecosystems, pp. 129-145. In C. 1. Kucera, and J. J.
Rochow. The Challenge of Ecology. St. Louis: C. V. Mosby Co., 1973.
59> Ruhling, A., and G. Tyler. Effects of Heavy Metal Pollution on the Decom-
position of Spruce Needle Litter. Department of Plant Ecology, Univer-
sity of Lund, Sweden, 1972. 48 pp.
60. Scheffer, T. C., and G. G. Hedgecock. Injury to Northwestern Trees by
Sulfur Dioxide from Smelters. U. S. Department of Agriculture
Forest Service Technical Bulletin No. 1117, 1955. 49 pp.
61. Shugart, H. H., Jr., T. R. Crow, and J. M. Hett. Forest succession models:
A rationale and methodology for modeling forest succession over large
regions. For. Sci. 19:203-212, 1973.
62. Skelly, J. M. Personal Communication, 1975.
63. Smith, R. F., and H. T. Reynolds. Integrated Pest Control. Proceedings
of FAO Conference, Rome, 1965.
12-78
-------
64, Smith, W. H, Air pollution effects on the quality and resilience of the
forest ecosystem, pp. . In Proceedings of AAAS Symposium on
Temperate Climate Forestry and the Forest Ecosystem; An Environmental
Issue? Washington, D. C. : American Association for the Advancement
of Science, 1972.
65. Stark, R. W., P. R. Miller, F. W. Cobb, Jr., D. 1. Wood, and J. R. Parmeter,
Jr. Photochemical oxidant injury and bark beetle (Coleoptera: Scolytidae)
infestation of ponderosa pine. I. Incidence of bark beetle infestation
in injured trees. Hilgardia 39:121-126, 1968.
66. stark, Rf Wf, and F," W." C6bb, Jr. Smog injury, ro&t diseases, and bark beetle
damage in ponderosa pine. Calif. Agric. 23(9):13-15, 1969.
67. Oxidant Air Pollutant Effects on a Western Coniferous Forest Ecosystem.
Task R Report: Historical Background and Proposed Systems Study of
the San Bernardino Mountain Area. Riverside: University of California,
Statewide Air Pollution Research Center, /not dated, circa 1973_/
68. Oxidant Air Pollutant Effects on A western Coniferous Forest Ecosystem.
Task C Report: Study Site Selection and On-Site Collection of
Background Information. EPA-R3-73-043B. Riverside: University of
California, Statewide Air Pollution Research Center, 1973. /189 pp._7
69. Taylor, 0. C., and P. R. Miller. Modeling the oxidant air pollutant impact
on a forest ecosystem. Calif. Air Environ. 4:1-3, 1973.
70. Oxidant Air Pollutant Effects on a Western Coniferous Forest Ecosystem.
Annual Progress Report, 1973-1974, Task D. Riverside: University
of California, Statewide Air Pollution Research Center, 1974.
71. Thompson, C. R., 0. C, Taylor, M. D. Thomas, and J. 0. Ivie. Effects of
air pollutants on apparent photosynthesis and water use by citrus
trees. Environ. Sci. Technol. 1:644-650, 1967.
12-79
-------
72. Thompson, C. R. Effects of air pollutants on lemons and navel oranges.
Calif. Agric. 22(9):2-3, 1968.
73. Thompson, C. R., and C. Rats. Antioxidants reduce grape yield reductions f"roni
photochemical smog. Calif. Agric. 24(9):12-13, 1970.
74. Thompson, C. R.', and 0. C. Taylor. Effects of air pollutants on growth leaf
drop, fruit drop, and yield of citrus trees. Environ. Sci. Technol. 3;
934-940, 1969.
75, Thompson, C. R., 0. C. Taylor, and B. L. Richards. Effects of photochemical
smog on lemons and navel oranges. Calif. Agric. 24(5):10-11, 1970.
76. Thompson, C. R., G. Kats, and E. Hensel. Effects of ambient levels of ozone
on navel oranges. Environ. Sci. Technol. 6:1014-1016, 1972.
77. Treshow, M., and D. Stewart. Ozone sensitivity of plants in natural com-
munities. Biol. Conserv. 5:209-214, 1973.
78 Tocher, R., and H. Kopp. People and forests—the challenge of forest recre-
ation, pp. 91-101. In Proceedings of 15th IUFRO Congress, 1971.
79. U. S. Department of" Agriculture. Forest Service. A Model for the Determin-
ation of Wildland Resource Values. Clarke-McNary, Sec. 2, Study Comm.,
1971. 39 pp.
80. U. S. Department of Agriculture, Forest Service. Silvicultural Systems for
the Major Forest Types of the United States. Agriculture Handbook 445,
1973. 114 pp.
81. Wert, S. I. A system for using remote sensing techniques to detect and
evaluate air pollution effects on forest stands, pp. 1169-1178. In
Proceedings of 6th International Symposium on Remote Sensing of the
Environment, 1969. Vol. 2. Ann Arbor: University of Michigan, 1969.
12-80
-------
82. Williams, W. T.. M. Brady, and S. Willison. Air Pollution Damage to forest
Trees in the Sequoia National Forest, Sequoia and Kings Canyon National
Parks, California. San Francisco: U. S. Department of Agriculture,
Forest Service, 1975.
83. Woodwell, fif M. Effects of pollution on the Structure and physiology of eco-
systems. Science 168-429-433, 1970.
84p Yonkers, T. A., F. C. Vasek, and H. B. Johnson. Seed germination and air
pollutant sensitivity in selected species of desert plants, pp.
In F. C. Vasek, H. B. Johnson, and W. W. Mayhew, Eds. Biological
Impact of the Southern California Edison Company Proposed Generating
Station in Upper Johnson Valley and Associated Transmission and Fuel
Lines. Riverside: University of California, Dry Lands Research
Institute, 1974.
12-81
-------
Chapter 13
EFFECTS OF PHOTOCHEMICAL OXIDANTS ON MATERIALS
The effect of photochemical oxidants on materials has been investigated
by exposure of materials to ambient air containing photochemical oxidants,
including ozone, PAN, peroxybenzoylnitrate (PBzN), and all other molecules
in ambient air that oxidize iodide ion (but not nitrogen dioxide), as pre-
scribed in the photochemical oxidant ambient air quality standard.1
Laboratory experiments for corroboration of field tests always use ozonized
air that contains no NO if photochemical generation is used and may contain
x
NO if electric discharge is the method of ozone generation. The reactivity
x
of oxidizing species, such as atomic oxygen and excited electronic states of
molecular oxygen, must be assessed both in test chambers and in ambient air
before blame for damage is assigned to ozone. On the presumption that ozone
is the damaging species in test-chamber experiments in which PAN and similar
oxidants are absent, photochemical oxidant damage is often referred to in
this discussion as "ozone" damage. The subject has been reviewed in Air
Quality Criteria for Photochemical Oxidants2 and in a systems study by
Salmon3 and more recently by Sanderson.4 Other, rather comprehensive,
although specialized, reviews have appeared on the effects of air pollutants
on textiles and dyes,5 on rubber,6 and on paint7*8 and on their economic
effects.9 In preparing this document, the literature has been reviewed with
special emphasis on papers published since 1970, when the EPA criteria
document appeared.2
-------
TEST-CHAMBER STUDIES
Experimental studies on the effects of ozone on materials usually
involve the laboratory generation10 of ozone by photolysis of air with a
mercury resonance lamp or by some form of electric discharge through air or
oxygen. Several oxidizing species result, among which are the first singlet
1 3
state of atomic oxygen, 0( D); ground-state atomic oxygen, 0( P); the lowest-
1
lying singlet molecular oxygen, 0 ( A ); and ozone. To identify the species
2 g
responsible for the effect, one must know the rate constants characteristic
of the interactions of these species with the material in question and the
relative concentrations of the species at the contact surface between the
ozonized air and the damaged material.
The Photochemical Ozone Generator
The standard ASTM test method10 (D-1149-64) for rubber damage includes
3
a test chamber (volume, 0.11-0.14 m ) through which ozonized air flows at a
rate greater than 0.6 m/s. Because the residence time of the ozonized air
in the test chamber is about 1 5, the ozone may be expected to reach the
material in about 0.1 s. A somewhat similar test procedure10 (AATCC test
method 109-1972; ANSI L14, 174-1973) is used in testing colorfastness. The
ozone generator is usually (but not necessarily) a mercury-vapor resonance
lamp with emission lines at 184.9 and 253.7 nm. The 184.9-nm line is absorbed,
and two ground-state oxygen atoms are produced:
3
0 + hv (184.9 nm) ->• 20( P). (1)
2
Each oxygen atom then reacts with diatomic oxygen to form ozone:
0 + 0 + M -> 0 + M, (2)
2 3
13-2
-------
where M signifies any gaseous molecule, such as 0 or N . Usually, the
2 2
253.7-nm line is more intense than the 184.9-nm line and falls in a very
strong absorption band of ozone:
1 1
0 + hv (253o7 nm) -> 0( D) + 0 ( A ). (3)
3 2 g
The species produced by this photochemical reaction can be quenched to their
ground electronic states by collisional processes:
1 3
0( D) + M -> 0( P) + M; (4)
1 3 -
0 ( A ) + M -> 0 ( T, ) + M. (5)
2 g 2 g
In addition, the ground—state oxygen atom reacts with ozone:
0 + 0 -> 20 . (6)
3 2
Rate constants of these reactions are summarized in Table 13-1.
Concentrations in the Generator. The absorbed intensity, I , is
a
obtained from the Beer-Lambert law, which relates the incident intensity,
o
I , and the transmitted intensity, I ,
t
o
I /I = exp (-ecA), (7)
t
where e is the absorption coefficient, c is the concentration of the absorbing
species, and £ is the path length. It follows that
o
I - I I
t _a = 1 -exp (-ec£). (8)
o o
I I
13-3
-------
CD
a
a
OJ
CM
1 — 1
1
CO
i — i
01
rH
cd
H
y— >,
^
•H
<
t-i
O
CM
0
1 1 1
sa
r^
^—X
O ^
o ^
CO
4->
MH fd
o cd
4J
0) CO
rl C
3 0
4J O
cd
t-l 01
^^^
CM
0
O rH
rH 1
1 CO
o ^o
01 0
rH 5
O
(U
H
cd
4-1
cd
CO
II
•4-J
a
a
4J
CO
a
0
u
0)
CO
cd
v3
CM
0
O
t— 1
1 rH
0 1
0) CO
rH CO
i 9
t — i
r~- |
rH O
1 01
O rH
rH O
0
X rH
I — 1
r~- 1
CM O
• 1 — 1
rH
X
II
CO •
to r-~
^^
60
<
rH
CM
O
-|~
/-^
P
rH
1
CO
CO
g
1 — 1
1
O
01
! — |
O
0
00
r— 1
1
0
1 — 1
X
CM
•
CM
/~v
60
1
IX]
CO
v— '
rH
1
CO
CO
s
. — 1
1
o
0)
! 1
0
0
1 — 1
1
o
1 — 1
X
VO
•
00
o
CM
O
t
a
CO
m
OO
CM
CO
O
CM
CM
60
O
t
s
CM
O
~"~
o
r^ "• — '
O
CO
u~l *t~
CM
^ s
J3 +
^•^
+ P
CO >— '
0 0
CO
* — •*
CM
0 0
CM
+ |
"^ 60
<] O
rH
CM
0 0
13-4
-------
For ec£«l,
o
1=1 ECio (9)
a
The stationary-state expressions are:
1
d[0]/dt = 21 - k [0] [0 ] [M] + [0( D)] [M] - k [0] [0 ] = 0; (10)
122 63
1 1
d[0( D)]/dt = I - k [0( D)][M] = 0; (11)
3 4
d[0 ]/dt = k [0][0 ][M] - I - k [0][0 ] = 0; (12)
3 22 363
The values of I and I —the absorbed light intensities at 184.9 nm and 253.7
1 3
nm, respectively—are related to incident intensities by expressions like Eq0
8. The incident intensities depend heavily on lamp design and construction.
For the purpose of the stationary-state computation, we use (on the basis of
17 3 17 3
experience) I = 10 photons/cm and I = 3 x 10 photons/cm -s. In the
1 3
calculations, a 1-cm path length is assumed. Summing Eqs. 10-12 and referring
to Table 13-1,
o
I = k [0][0 ] = I e [0 ]. (13)
163 12
18 3
The oxygen concentration in air is taken to be 5 x 10 molecules/cm „
30
[0] = 1.16 x 10 /[O ]. (14)
3
1
The concentration of 0( D) is obtained from Eq. 11.
o
1 I I e [0 ] -9
[0( D)] = 3 = 333 = 2.1 x 10 [0 ]. (15)
k [M] k [M]3
4 4
13-5
-------
1
The concentration of 0 ( A ) is obtained by means of its stationary-state
2 g
expression:
1
d[0 ( A)] 1
2 = I - k [0 ( A)]M = 0; (16)
dt 352
o
1 I e [0 ] -2
[0 ( A)] = 33 3 = 7.1 x 10 [0 ]. (17)
2 k M 3
5
1
Because I = k [0][0 ] and I = k [0( D)][M], Eq. 10 yields:
163 34
I + I = k [0][0 ][M]. (18)
1322
Substituting for [0] and solving with the quadratic formula:
30 o o
I +1 = k [0 ][M] x 1.16 x 10 =1 e [0 ] + I e [0 ]; (19)
1322 112333
o 2 o 30
I e [0 ] + I e [0 ][0 ] - k [0 ][M] x 1.16 x 10 =0 (20)
333 1123 22
[0 ] = -b * / b - 4ac (21)
3 2a
Evaluating a, b, and c:
a = 3.3,
15
b = 3.7 x 10 , and
34
c = 8.5 x 10 ,
13-6
-------
17 3
the solution is [0 ] = 1.6 x 10 molecules/cm . The concentrations of the
3 17 3
oxidizing species for [0 ] = 1.6 x 10 molecules/cm are given in Table 13-2.
3 3
The ratio of rates of attack of 0( P) and ozone on a material in the ozone
generator is given by:
3 k
R /R = [0( P)] . _0 , (22)
0 0 [0 ]k
330
3
where k and k are the rate constants. A hypothetical example of a
0 0
3
material undergoing a damage test may be chosen to be an olefinic polymer.
In the absence of data on appropriate material, we may presume that damage
done to an olefinic material by oxygen atoms and ozone would proceed at the
same relative rates as attack on a typical olefin, e.g., butene-^l. Rate
*-
constants for attack of various oxygen species on butene->L are presented in
A
Table 13-3. Thus, we estimate
5
k /k = 3.5 x 10 (23)
0 0
3
-5 5
and R /R = (4.5 x 10 ) (3.5 x 10 ) = 15.8. (24)
0 0
3
It follows that, although the ozone concentration is more than 10,000 times
that of the oxygen atom, the latter reacts so rapidly with olefins that
oxygen atoms, rather than ozone, will be the species responsible for material
damage, if the material is placed in the ozone generator.
13-7
-------
Table 13-2
Stationary State Concentrations of Oxidants in
Photochemical Ozone Generator*3
Concentration,
3
Oxidant molecules/cm
17
0 1.6 x 10
3
3 12
0( P) 7.3 x 10
1 8
0( D) 3.4 x 10
1 16
0 ( A ) 1.1 x 10
2 g
o 17 3 o 17 3
a 1=1 cm, I = 10 photons/cm -s, I = 3 x 10 photons/cm -sc
1 3
13-8
-------
Table 13-3
Rate Constants for Reaction of Oxygen
Species with trans—2—Butenea
Oxidant
0 ( A )
2 g
Rate Constant
-1 3 -1
(k, molec cm s )
-18
4.6 x 10
-17
3.5 x 10
3
0( P)
-11
2.3 x 10
a Data from Demerjian et al.1!
13-9
-------
1
Similarly, for 0 ( A )•
2 g
1
R 0 ( A )
2 g
R 0
3
k
A
k
0
3
1
[0 ( A)]
2
[0 ]
3
= 2.3 x
1.1 X
-18
10
-17
10
1.1 X
1.6 x
16
10
17
10
1
Therefore, 0 ( A ) could be a significant problem in ozone damage tests on
2 g
olefin-like materials, if the test were done in the ozone generator. The
results in Table 13-2, although only very approximate because of the
assumptions made, show that in a photochemical ozone generator we may expect
1
0 ( A ) concentrations to be an appreciable fraction of the ozone concen-
2 g 1
tration. The 0( D) concentration is negligibly small, because it is removed
in the reaction shown in Eq. 4 on almost every collision.
Concentration Downstream from the Generator. The ASTM method requires
that the ozone generator be outside the test chamber, and we must ask how
1 3
long 0 ( A ) and 0( P) survive after the ozonized air leaves the generator
2 g
on its way to the material under test. About 0.1 s is required for the ozone
to reach the material after leaving the generator. As the light source is
extinguished (t = 0) or as the ozonized air leaves the photolysis chamber,
1 1
the rate at which 0 ( A ) is removed is—using S to signify 0 ( A )—
2 g 2 g
d[S]= k [S][M]; (26)
dt 5
- d£n[S] = k [M]dt. (27)
5
13-10
-------
Thus, 0.1 s after the light is turned off, [S ] decays to [S] by Eq. 5,
o
whose rate constant is given in Table 13-1. The concentration, [M], is
19 3
2.7 x 10 molecules/cm . Solving Eq. 27, we obtain
[S]
d£nS = 6; (28)
[S]
£n [S] = -6; (29)
TsT
o
-2.6
[S] = 10 . (30)
FT
o
1
Therefore, although the 0 ( A ) is only very inefficiently quenched by
2 g
collision, at a pressure of 1 atm quenching is sufficiently rapid that only
1
a few tenths of 1% of the original 0 ( A ) can reach the test material.
2 g 18
However, when the pressure is smaller — say, 76 torr or 2.5 x 10 molecules/
3 1
cm — In ([S]/[S] ) = -0.6 after 0.1 s and more than half the original 0 ( A )
o 2 g
molecules may reach the test material.
Finally, we must ask whether the ASTM procedure is likely to result in
removal of oxygen atoms sufficiently rapid for the observed damage to be
attributed to ozone. The rate of removal of oxygen atoms by the reaction of
Eq. 2, which is the major sink, is given by:
-d[0]/dt = k [0][0 ][M]; (31)
2 2
13-11
-------
[o]
[o]
d£n[0] = k [0 ][M]
2 2
0.1
dt; (32)
0
3
£n[0] = -8.1 x 10 ; (33)
ToT
o
-3500
[0]/[0] = 10 . (34)
o
Therefore, the ASTM test is a valid ozone damage test, inasmuch as both the
1
oxygen atoms and the 0 ( A ) are rapidly removed downstream from the generator.
2 g
The importance of having the ozone generator outside the test chamber cannot
be overemphasized. The validity of any ozone damage test using other sources
depends very heavily on the test procedure. If an electric discharge is used
as the ozone generator, the test chamber should be designed in accord with
such chemical kinetic considerations as indicated in the model discussed
here. The relative concentrations of oxidizing species in a radiofrequency
or microwave discharge or a photochemical generator are subject to conditions
3 1
and to some speculation. However, equal concentrations of 0( P) and 0( A )
g
have been suggested as emerging from discharged air.17 The ratio of oxygen
atoms to ozone depends critically on the pressure. In a microwave discharge
where the pressure may be 1 torr, 0.1 s after leaving the discharge a
substantial fraction of the oxygen atoms remains.
Because oxygen atom reaction rate constants can be orders of magnitude
greater than those for ozone, an experiment done on material subject to a
reduced-pressure discharge is likely to signify damage done by oxygen atoms,
rather than ozone.
13-12
-------
Oxidant Species Concentrations in Polluted Air
We have shown that, in a properly designed laboratory experiment, ozone
is likely to be the only oxidant species producing damage in the test material.
In a real atmosphere, such photochemical oxidants as PAN and PBzN are formed
in complex atmospheric reactions. Because there is no information on the
effects of these oxidants on materials, no consideration is given to them
in assessing material damage in this discussion. Sunlight and energy transfer
1 3
processes result in generation of 0 ( A ) and particularly 0( P). Therefore,
2 g
it is necessary to consider the concentrations of these species relative to
that of ozone in a real atmosphere. This has been done, notably by
Demerjian et_ al.,18 one of whose estimates, calculated from smog-chamber
considerations, is shown in Table 13—4. The ozone concentration assumed in
Table 13-4 is typical of a fairly polluted atmosphere. To estimate the
relative contributions of each oxidizing species to oxidant damage, it is
necessary to multiply the concentration by the rate contant for each
individual material. Unfortunately, there is almost no information on rate
constants, and it is assumed in nearly all cases that the oxidizing species
is ozone.
EFFECTS OF OXIDANTS ON INDIVIDUAL MATERIALS
According to the Midwest Research Institute study of 1970,3 both ferrous
and nonferrous metals have excellent resistance to ozone. Such materials as
building stone, building brick, cement, glass, and graphite also have excel-
lent resistance. Some synthetic rubbers have good ozone resistance, but
natural rubber has notoriously poor resistance. Polyethylene, polystyrene,
and polypropylene are believed to have only fair resistance to ozone, and
13-13
-------
Table 13-4
Calculated Concentrations of Oxidant
Species in Smog Chambers'3
Concentration,
3
Oxidant molecules/cm
1 8
0 ( A ) 1.4 x 10
2 g
12
0 3.8 x 10
3
3 5
0( P) 2.6 x 10
6
OH 1.9 x 10
HO 10
2 1.0 x 10
a Calculated concentrations for oxidants in smog
chamber under conditions outlined in Chapter 2
for 60-min irradiation (see Table 2-2).
13-14
-------
acetate, nylon, and fibers of cotton, rayon, and cellulose esters are also
in the "fair" category„ Wood is considered fairly resistant, but little
information is available. The approach used by MRI in assessing economic
effects is that the value of material exposed to air pollution, Q, is the
product of four factors: the annual production, P; the average economic
life of the material, N; the fraction of material exposed to air pollution,
F; and the labor factor, R, which reflects the cost of putting the material
in place where it is used. Hence,
Q = P • N • F • R. (35)
Having defined Q, the MRI report defines the damage costs as the product of
Q and v, the "interaction" value per year0 For example, if Q = $1 billion
and a pollutant causes a 1% reduction in economic life per year of exposure,
then v = 0.01, and the economic loss, L, due to the pollutant is Qv, or $10
million/year. The values of v for pollutant damage generally are difficult
to obtain, because few data are available. For the particular pollutant,
ozone, the values of v are almost impossible to assess. The MRI report
points out that "intuitive feelings" are sometimes used to assess v. The
materials that have been classified poor or fair in ozone resistance are
listed in Table 13-5 in order of decreasing in-place value. The chemical
interaction value, v, and the economic loss, L, are also tabulated. Because
it is difficult at best to estimate overall pollutant interaction, ozone
damage has been assessed in the last column of Table 13-5 by estimating L1,
the ozone damage, as follows: If chemical resistance has been estimated by
MRI as either poor or fair for one pollutant other than ozone for which a
13-15
-------
c
o
•> iH
Tj rH
0
o
m
o
CN
c
o
cd
C
cd
H
ft
c
o
•H
•> rH
rJ rH
m
OO
CM
in
CM
oo
en
in
en
o
M-l
X
cu
m
en
O
•H
4J
O
FM
O
4-1
-§
CO
o
w
cd
•H
cu
4J
^
cd
0)
ft
m
o
0
o
o
o
o
o
o
o
o
o
1 — 1
o
o
0
o
o
o
o
o
r-l
o
o
o
0
o
o
en
CM
en
•
en
o
CM
o
o
00
o
m
o
in
oo
in
o
en
en
o
CM
oo
cu
cu
to
,0
cd
H
CO
CU
CO
cu
c
o
N
o
14-1
o
cu
en
o
CM
o
CM
o
CM
o
in
o
CM
o
CM
o
o
en
00
cu
M-l
OJ
cd
>
§
a
o
a
w
ti
o
•H
PH
00
CM
OO
cT
en
en
en
o
en
00
o
m
oo
en
O
O
oo
oo
VD
O
00
m
H
cd
•H
J_|
cu
4-1
cd
s
4-1
fi
•rl
cd
fi
O
T3 4-1
O 4J
O 0
Es o
0)
a
cu
rH
^
,f~]
4-1
CU
^t
iH
O
ft,
H
cu
n
•H
M-l
C
O
rH
^
5z;
cu
C
cu
M
^
4J
CO
^>
T-H
O
PH
cu
c
CU
^
DH
0
ft
^»
i— |
o
^_J
0)
rQ
rQ
3
rH
cd
13
4J
cd
&
J_j
0)
O
•H
4-1
a
o
^"t
cd
<&
CO
o
•H
4-1
CO
cd
! 1
ft
C
0
i — I
^
2
o
•rl
4-1
CO
cd
rH
ft
ai
4-J
cd
4-J
cu
0
cu
60
cd
§
CU CO
a &o
O C
N -H
O T3
cd
o cu
co C
M 6
cu 3
4-1 i-l
a) o
n u
t-l O
13-16
-------
national ambient air quality standard has been set, L* = %L; if two other
pollutants are in the poor or fair category, L' = 1/3L. The data in Table 13-5
should be regarded as very rough and indicative only of broad-brush outlines.
For example, paint damage is undoubtedly a very important economic conse-
quence of ozone pollution, but, as we shall see, the estimate of rubber
damage in Table 13-5 is much too low.
The most studied materials, as well as the most important economically,
with respect to ozone damage are paint and elastomers (e.g., rubber). Other
materials will be reviewed individually in cases in which scientific data
are available.
Paint
Failure of Paint Films. Paint formulation consists of a binder (a
natural or synthetic polymer or dryingoil), a solvent, and a pigment or
colorant, including an extender, typically calcium carbonate or a silicate.
Because of the reactivity of organic polymers toward ozone, it is not
surprising that ozone damage ftas been observed, at least in laboratory
experiments. In 1968, paint sales of over $2.5 billion were recorded in
the United States. Table 13-6 outlines these sales.8 The failure of paint
films takes on a variety of forms, as shown in Table 13-7, and methods for
testing the various forms of failure have been delineated by the ASTM.19
These methods are listed in Table 13-8. The paint industry has been con-
cerned mainly with "weatherability" of paints, rather than specifically
with the effect of air pollutants.
13-17
-------
Table 13-6
Trade and Industrial Paint Sales, United States, 1968a
Type of Sale
Trade:
Interior house paints:
Latex emulsion
Oil and alkyd
Primer, sealers, etc.
Miscellaneous
Exterior house paints:
Latex emulsion
Oil and alkyd
Enamels
Primers, sealers, etc.
Miscellaneous
Automotive refinishing
Traffic
Other
Industrial:
Automotive, new
Marine
Railroad, aircraft, etc.
Coil coating
Prefinished wood
Industrial maintenance
Machinery and equipment
Miscellaneous
Amount,
millions
of gallons
424
145
45
10
25
55
40
15
10
20
30
25
4
419
55
20
15
20
15
45
30
219
Cost,
$ millions
1,428
Unit Cost,
$/gal
3.37
425
170
30
100
190
155
55
35
50
150
45
23
1,159
170
85
40
80
40
160
75
509
2.93
3.78
3.00
4.00
3.45
3.88
3.67
3.50
2.50
5.00
1.80
5.75
2.77
3.09
4.25
2.67
4.00
2.67
3.56
2.50
2.32
a Data from Spence and Haynie.8
13-18
-------
Table 13-7
Types of Film Failurea
Type Failure
Description
Chalking
Cracking or checking
Alligatoring
Peeling
Color fading
Blistering
Rusting
Formation of powdery layer on surface
of coating that is being eroded away
Shrinkage of the coating resulting in
film rupture
Film rupture resulting from the appli-
cation of a brittle film over a more
flexible coating
Poor adhesion of the coat to substrate
Reaction of binder or pigment in
presence of sunlight or environment
Projections or pimples on film that
result from trapping of solvent or
moisture between substrate and film
Oxidation of metallic substrates, such
as iron or steel, when film permits
moisture or chemicals to attack
substrates
a Data from Spence and Haynie.8
13-19
-------
Table 13-8
ASTM Test Methods for Exterior Paint Films
Test Purpose
D 659-44 Evaluating degree of resistance to chalking
D 660-44 Evaluating degree of resistance to checking
D 661-44 Evaluating degree of resistance to cracking
D 662—44 Evaluating degree of resistance to erosion
D 772-47 Evaluating degree of resistance to flaking (scaling)
D 1641-59 Measuring exterior durability of varnishes
D 1543-63 Measuring color change of white architectural enamels
D 1654-61 Evaluating painted or coated specimens subjected to corrosive
environments
D 2197-68 Measuring adhesion of organic coatings
D 2370-68 Measuring elongation and tensile strength of free films of
paint, varnish, lacquer, and related products with tensile
testing apparatus
13-20
-------
Probably the most definitive study of the effect of air pollutants on
paint is contained in a 1972 report of the Sherwin-Williams Company.20
Five commercially important coating systems were selected for study:
1. House paint—lead-titanium-zinc extender in oil with 100% rutile
titanium dioxide.
2. House paint—titanium extender in acrylic latex with 100% rutile
titanium dioxide.
3. Industrial maintenance coatings—titanium in alkyl with 100% rutile
titanium dioxide.
4. Coil coating finishes—titanium extender in urea-alkyl with 75%
rutile and 25% anatase titanium dioxide.
5. Automotive refinish lacquer—titanium in nitrocellulose-acrylic
with 100% rutile titanium dioxide.
For each coating system, three tasks were performed:
• Existing exterior exposure records were reviewed with respect to
visual erosion ratios.
• Short-term exposures were studied at Leeds, North Dakota; Los
Angeles, California; Chicago, Illinois; and Valparaiso, Indiana.
The North Dakota location was a clean, rural site; Los Angeles
represented a high-oxidant urban site; Chicago was a high-sulfur
dioxide location; and Valparaiso was considered to have moderate
sulfur dioxide pollution and low oxidant concentrations. Tests
with commercial instruments included those for erosion, gloss,
sheen, surface roughness, and tensile strength.
13-21
-------
• Accelerated laboratory exposures were made at various pollutant
concentrations: no pollutant, 0.1-ppm sulfur dioxide, 1-ppm
sulfur dioxide, 0.1-ppm ozone, and 1-ppm ozone.
As measured by erosion rates (linearly related to pollutant concen-
tration) , it was found that in all cases coatings were affected more by
sulfur dioxide than by ozone. Sulfur dioxide at: 1 ppm had the following
effects on the five paint systems: System 1, "considerable"; systems 2
and 4, "moderate"; and systems 3 and 5, "no effect." Both attenuated total
reflection and scanning electron photomicrographs showed that the damage
was greater in Chicago and Valparaiso than in Los Angeles and North Dakota.
Studies have been conducted on creep compliance tests8 in which paint
2 32
films were subjected to tensile loads of 4-7 Ib/in. (27.2—47.6 x 10 N/m )
and to 6% ozone for 505 h. A typical result for a high-quality emulsion-
base paint is shown in Figure 13-1. Creep compliance is reduced by exposure
to 6% ozone. If the effect is linearly related to ozone concentration, we
might expect the same reduction in creep compliance at 0.1-ppm ozone in
8
3 x 10 h, or some 30,000 years. Thus, reduction in creep compliance is not
viewed as having a serious ozone contribution.
Economic Effects. The Midwest Research Institute Report (pp. 41 ff.)
computes L, the increased cost of cleaning or repainting per year, as the
product of Q, the consumer purchase price of a unit of material; y> the cost
of cleaning or repainting one such unit; and Af, the fractional increase in
cleaning frequency resulting from particulate pollution.
L = Q«yAf, dollars/(yr. x unit). (36)
13-22
-------
30
CM
20
«c
_l
D_
i 10
o
CL.
LD
•^ «
0= 0
O
20
40
60
80 100
TIME, minute
120
140 160
180
Figure 13-1.
Initial creep of EM 7338 first-quality emulsion-base paint,
before and after 505-h exposure to ozone at 60 C. (Reprinted
from Spence and Haynie.8)
13-23
-------
The cost, Y» of cleaning one unit is determined for two classes of material,
fibers and nonfibers. For fibers, $0.10/lb is taken as the cost of cleaning;
2
for nonfibers, $0.10/ft is taken as the cost of cleaning (removal of par-
ticulate material). The purchase price is defined as the material cost
times a factor that gives the consumer purchase price including labor
(painters, outlet salesmen and their overheads, etc.). The quantity yAf is
given by v = yAf = L/Q-yr and is called the soiling interaction:
L = Qv. (37)
The determination of the quantity Af, the fractional increase in cleaning
frequency due to particulate matter, is the difficult part of the problem.
The data of Michelson and Tourin21 suggest a value of v for paint of 1.5/
year. The value of Q is obtained as follows: According to Noble,22 the
annual production of paint in 1968 was $2.59 billion0 Because the economic
life of paint is considered to be 4 years, $10.36 billion worth of paint is
in place, of which only 70% is exposed to atmospheric pollutants. Thus,
$7.25 billion is the manufacturers' value of in-place paint exposed to air
pollution. Using a labor factor of 3.3, the total in-place value of paint
is $23.9 billion. Because v = 1.5 for particulate soiling, the cost of
pollution damage (cleaning costs) is some $36 billion per year.
The costs associated with chemical effects of gaseous pollutants could
not be ascertained for each pollutant, because of a paucity of information.
The value of v for chemical deterioration was obtained by an educated guess
that repainting is needed every 4 years in a polluted environment and every
5 years in a pristine air environment. Thus, v (chemical) = 0.050 The
13-24
-------
corresponding figure for chemical deterioration costs is 0.05 ($23.9
billion) = $1.195 billion per year.
Spence and Haynie have attempted to assess costs of air pollution
damage to paints without special regard to the identity of the pollutant
doing the damage. However, repainting frequencies have been determined in
five American cities whose particulate concentrations have been measured.
There appears to be a linear (although not necessarily causal) relationship
0 1
between the maintenance frequency and particulate concentration. Economic
loss due to pollution was estimated by the following procedure: The average
service life of exterior household paint in urban areas is 3 years, and in
rural areas, 6 years. Thus, 0»33 and 0.17 are the replacement probabilities
per year. Because 60% of the surface painted is urban and 40% rural, it may
be calculated that some 74% of the paint used over a long period is consumed
in urban areas. The total value of manufactured paint is $485 million, of
which 74%, or $359 million per year, is the cost of paint consumed in urban
areaso Its service life is 50% less than in rural areas, so 0.50 ($359
million) = $180 million is the annual cost of exterior household paint
deterioration due to pollution., The value of loss of paint in place was
computed to be 3.0 ($180 million) = $540 million. It is noteworthy that
the Midwest Research Institute report estimates $1.195 billion repainting
costs due to chemical pollution.
The economic assessment of air pollution damage to exterior paints is
summarized in Table 13-9. There appears to be no definitive way to determine
the fraction of the $225 million loss for all exterior paints that is due
to photochemical oxidants» According to the convention introduced by Midwest
13-25
-------
Table 13-9
Economic Assessment of Air Pollution Deterioration of
Exterior Paints (1968 Figures—Manufacturers Costs)a
Loss Due to Air
Exterior Paint Value of Paint Exposed in Urban Pollution,
Class Areas, $ million $ million
Coil coatingb 31 8
Automotive
refinishing 111 22
Industrial
maintenance 74 15
b
Household 359 180
Total 575 225
a Data from Spence and Haynie.
b Extender Type Paints.
13-26
-------
Research Institute—that repainting costs may be considered to be due to
chemical pollution—only NO , sulfur dioxide, and photochemical oxidants
x
seem likely to be involved in this kind of paint damage. Sulfur dioxide
seems to attack only the extender (e.g., calcium carbonate) component. It
might also be expected that nitrogen dioxide would attack only extender
paints. Sulfur dioxide has no effect on the nonextender types—industrial
maintenance and automotive refinishing paints. Therefore, the $37 million
worth of damage done to the nonextender types each year may be attributed
to the effects of oxidants. Of the $188 million worth of damage to extender
paints, we may expect some 80% to be caused by sulfur dioxide and nitrogen
dioxide, with $38 million worth of damage (20%) due to oxidants. Thus, a
total of $75 million worth of paint damage per year is caused by oxidants.
The figure of $75 million includes only the cost at the manufacturers'
levelo The cost at the consumer level—i.e., the total cost of the paint
applied to a surface—is obtained by multiplying by a factor of 3.0 (according
to Spence and Haynie8) or 3.3 (according to Salmon3). Thus, the ozone
damage to paint (using a 3.3 factor) is $248 million per year.
Elastomers
Failure of Elastomers. Elastomers include both synthetic elastomers
and natural rubber. The most extensive study of the effects of ozone on
elastomers (including economic effects) was done by Mueller and Stickney6
and Stickney et_ al_. ,23 and much of what follows is taken from the 1971
report.23 Table 13-10 presents the estimated elastomer production in 1975.
The effect of ozone on cracking of natural rubber was proved by Newton2lf
and by Crabtree and Kemp.25 In general, highly unsaturated elastomers are
13-27
-------
Table 13-10
Polymer Usage Projected to 1975a
Estimated
Estimated
Average
Production, Price Per
Polymer
SBR — copolymer of butadiene
and styrene
Natural — natural polyisoprene
Polybutadiene— polymerized
butadiene
Neoprene — polymerized
chloroprine
Nitrile — copolymer of
butadiene and
acrylonitrile
Urethane — polymers containing
urethane linkage
Butyl — copolymer of
isobutylene and isoprene
Silicons — polydimethylsiloxane
Polyisoprene— synthetic
polyisoprene
Polyacrylate — polymer or
copolymer based on an
acrylate
EPDM — copolymer of ethyl ene,
propylene, and a diene
Polysulfide— ^polysulfide
Fluorocarbon — f luorinated
polymers
Chlorohydrin — polymer of
epichlorohydrin or
copolymer of
epichlorohydrin and
ethylene oxide
Total
1,000
tons^1
1,748
689
375
146
95
45
101
13
134
3
168
17
2
8
3,544
Pound ,
cents5
23
22
27
40
50
125
27.5
250
26
80
25
135
1,250
85
Value,
$ million
804.1
303.2
202.5
116.8
95.0
112.5
55.5
65.0
69.7
4.8
84.0
45.9
50.0
13.6
2,022.6
Portion
of Total
Polymer
Value, %
39.8
15.0
10.0
5.8
4.7
5.6
2.7
3.2
3.4
0.2
4.2
2,3
2.5
Oo7
100.0
a Derived from Stickney et al.23
b Chemical Week, March 18, 1970, p. 58.
o Battelle and industry estimates.
13-28
-------
more subject to ozone attack than are saturated elastomers, because ozone
attacks aliphatic double bonds. The more highly unsaturated elastomers are
listed in Table 13-11. Of these, neoprene is particularly resistant to
ozone, owing to the presence of the electronegative chlorine atom in its
structure. Elastomers crack under the influence of ozone when stressed,
and the crack propogates in a direction normal to the stress direction. The
chemical mechanism may be written:27
o'N,
I I
0 + - C = C- -> -C - C-
3 H H H H
(38)
+
+ -C -0-0+0= C- •
H H
The zwitterion and aldehydic group are thought to combine,
+ - 0^
-C - 0 - 0 + 0=C- -> -C C- , (39)
H H H\ /H
0—0
to form a highly oxidized structure of much lower extensibility than the
unoxidized elastomer. Cracking is the result.
There are two main approaches to avoidance of ozone damage. One is
the addition of antiozonants. The more extensively used antiozonants are
listed in Table 13-12. These antiozonants have limited solubility in
elastomers and tend to "bloom" to the surface. The antiozonant action is
not well understood chemically, but probably involves formation of a pro-
tective film. Crack initiation occurs at critical stress, which is strongly
influenced by the presence of a few percent of the N,N'-dialkyl-p-
phenylenediamines. Dithiocarbamates are a second class of antiozonants that
13-29
-------
Table 13-11
Highly Unsaturated Elastomers'2
Polymer
Use
SBR
Natural
Polybutadiene
Neoprene
Nitrile
Polyisoprene
General
General
Wear-resistant
Oil-resistant
Oil-resistant
General
Crack Growth
Rate, mm/min^
0.37
0.22
ND
0.01
ND
ND
1970 Cost,
cents/lb
23
25
25
40
50
24
a Derived from Mueller and Stickney.
b Data from Braden and Gent.26 ND = no datac
13-30
-------
Table 13-12
Elastomer Antiozonants
Antiozonants Price, cents/lb (1970)
N-N1— Diphenyl-jD-phenylenediamine 99
N-N'-Di-(2-octyl)-2-phenylenediamine 90
N-N'-Di-3-(5-methylheptyl)-£-phenylenediamine 90
N-Nf-bis-(l,4-Dimethylpentyl)-£-phenylenediamine 86
N-N'-bis-(l-Ethyl-3-methylpentyl)-£- 90
phenylenedlamine
i-N'-bis-(1-Methylheptyl)-p_-phenylenediamine 90
N
13-31
-------
act by slowing crack growth rates. The crack growth rates depend linearly
on the concentration of ozone, as shown in Figure 13-20 In addition to
antiozonants and special polymeric structures, protection against ozone
damage during storage is afforded by the use of waxes, protective coatings,
and paper wrapping.
3
Identity of Oxidizing Species. It is known that atomic oxygen, 0( P),
reacts with double bonds at room temperature to produce a rupture of the
carbon—carbon chain. Because elastomers are known to be very stable to
3 -
ground-state ( £ ) molecular oxygen, the possible oxidants responsible for
g 1
rubber-cracking in polluted air are atomic oxygen, 0 ( A ), ozone, OH, and
2 g
HO . Relative rates of reaction are products of rate constants and concen-
2
trations of oxidizing species.
One elastomer, cis-polybutadiene, has been exposed specifically to
1
0 ( A ) in the absence of ozone or oxygen atoms.28 cis-Polybutadiene forms
2 g
hydroperoxides (-OOH) when exposed to oxygen at 5 torr that has been subjected
to an electrodeless discharge (2,450 MHz). Oxygen atoms and ozone were
1
removed by mercuric oxide in these experiments, leaving on!i}r 0 ( A ). As we
1 2 _ g
have seen, 0 ( A ) survives for a long time at the low pressures used, nearly
2 g
half of it surviving 1 s after leaving the discharge zone. No measurements
1
have been made of relative rates of reaction of 0 ( A ), ozone, atomic oxygen,
2 g
OH, and HO with individual materials, and it is therefore not possible to
2
know the relative importance of attack by these species. The results in
Table 13-13 would lead to the speculation that ozone is more important
1
than 0 ( A ) in cis-polybutadiene damage. Because we do not have information
2 g
on the relative rates of reaction of the five species with elastomers, we can
13-32
-------
100
ex
ex
c:
o
O
o
o
c
o
M
O
10
\
\
\
\
\
\
'-
t
\
V
\
/
I
\
V,
1
\
\
s
\
x
\
X
\
\
\
\l
s.
N
\
*\f
s\
\
\
\
\
\
I 10
Time, minutes
Figure 13-2. Effect of ozone concentration on cracking time. (Reprinted
from Mueller and Stickney.6)
100
13-33
-------
Table 13-13
Rates of Attack of Oxidants on
trans-2-Butene In Simulated Polluted Air
Oxidant
OH
HO
Rate constant
-1 3 -1
(k), molec cm s a
Concentration,
3 ,
molecules/cm
-11
2.5 x 10
-11
2.4 x 10
1.9 x 10
10
1.0 x 10
Relative Rate
1
0 ( A )
2 g
°3
0(3?)
-18 8 -10
4.6 x 10 1.4 x 10 6.4 x 10
-17 12 -4
3.5 x 10 3.8 x 10 1.3 x 10
-11 5 -6
2.3 x 10 2.6 x 10 6.0 x 10
-5
4.8 x 10
0.24
a Data from Demerjian et al.18
b Data from Table 13-4»
13-34
-------
assume that the rate constants parallel those of the reactions with trans-
butene-2 (see Table 13-3), as was done in estimating the rates of reaction
with an olefinic polymer in the laboratory ozone generator. Using the con-
centrations in Table 13-4 with the rate constants in Table 13-3, we arrive
at the attack rates shown in Table 13-13. These results suggest that HO
2
is the most important oxidant in attack on elastomers in ambient air.
Economic Effects. The Battelle study5 revealed very substantial
compounding costs for protection against photochemical oxidants. Table 13-14
summarizes the results of an analysis based on responses to a questionnaire.
These costs include the introduction of such ozone-resistant polymers as
butyl, neoprene, EPDM, Hypalon, and polysulfide. Fair agreement was obtained
between costs obtained from the questionnaire and those from estimates of
individual compounding costs as summarized in Table 13-15. In addition to
the costs outlined in Table 13-15, other costs are associated with replacement
of entire assemblies when a part fails, labor costs for replacement, etc0
These costs at the retail level have been estimated by Battelle to total
$226 million per year, of which $100 million is attributed to damage of
medical goods. In 1969, the cost of antiozonants in automobile tires2 alone
was about $100 million, which represents the cost of avoiding ozone damage
to tires. The $226 million estimate does not include labor costs for actual
replacement. Because antiozonants tend to discolor, they cannot be used in
white sidewall tires, which use, instead, such costly elastomers as Hypalon
and EPDM. It is of interest that tires, hoses, and belts do not represent
the only important use of rubber in automobiles. Some $50 per car or $500
million per year in other rubber parts represents the value at the manufacturer
13-35
-------
Table 13-14
Estimate of AddedAManufacturing
Costsa on National Level®
Product
Passenger tires
Truck and bus tires
Other tires
Rubber belts and belting
Rubber hose and tubing
Sponge and foam-rubber goods'3
Rubber floor and wall covering
Mechanical rubber goods
Rubber soles and heels'3
Drug and medical
Footwear
Other rubber products
Total
Estimated
Value of
1970
Shipments,
$ million
2,352
1,037
679
300
480
325
66
1,295
165
100
400
650
7,849
Estimated
Added Cost
per Dollar of
Production,
mils
12
12
10
4
2
8
1
1
Total
Added
Cost,
$ million
2802
12.4
6.8
1.2
1.0
2.6
0.8
0.4
0.7
54.1
a Extra costs due to special compounding or formulation to protect against
oxidant damage,
b Derived from Mueller and Stickney.5
G No protective compounding or formulation used.
13-36
-------
Table 13-15
Summary of Added Costs at Manufacturer Levela
Type of Cost Cost, $ million
Special polymers 20.6
Antiozonant 34.1
Wax 5.0
Protective Finishes
Wrapping
Compound development
26.0^
Total 85.7
a Derived from Mueller and Stickney.6
b Rough estimate.
13-37
-------
level. The cost of ozone damage is summarized in Table 13-16. An approximate
25% rise in rubber production was expected between 1969 and 1975. Therefore
the cost of ozone damage to elastomers in 1975 should be 1.25 x 596= ~$750
million.
Textile Fibers
It is difficult to find any definitive information that indicates ozone
damage as extensive as that suggested in the Midwest Research Institute
report.3 The latter identifies cotton, nylon, and rayon as particularly
susceptible to ozone. The oxidation of cellulose fibers by ozone was the
subject of a study2g in 1952 that showed that dry cotton was not seriously
degraded by ambient ozone. In more recent studies, these conclusions were
confirmed. »31 The only information available on fibers other than cotton
addressed the effect of ozone on modacrylic, acrylic, Nylon 66 and polyester
fabrics.32 The results indicated minimal effects on these fibers.
However, Jellinek and Chaudhuri33 exposed Nylon 66 films to nitrogen
dioxide, ozone, and ultraviolet radiation. The degree of degradation of
polymer, a, was measured by
a = _! - _!_ , (40)
L L
t o
where L and L are the number-average chain lengths at times Q and t,
o t
respectively0 Degradation proceeds rapidly at 19.2 ppm and stops at around
a = 0.002 after 1 h. Lower concentrations produce lower ultimate degrees
of degradation after longer times (see Figure 13-3). The mechanism of the
degradation is believed to be attack at the N-H bond.
13-38
-------
Table 13-16
TV,
Summary of Ozone Damage Cost Per Year (1969)
Mfr. Level
Cost, Retail Cost,
Type of Cost _ $ million Labor Factor $ million
Special formulations 85.7 3 257
Early replacements 225.7 1.5 339
Total 596
13-39
-------
*0
o
20
18
16
14
12
10
e
4
a
I 1 I t I I — 1 — 1 — I — 1 — 1 — 1 — p
1 » *
„
*
x^"*
/
^S^-- 1 P 1 !' 1 I 1 i i i i .
0 1 * 3 4 9 6 7 8 9 10 I) 12 13
HOURS
Figure 13-3.
Plots of a vs. time for BI films at 35 C in presence of 1 atm
of air containing ozone;B, 19.2 ppm; A} 11 ppm; •, 5.2 ppm0
(Reprinted with permission from Jellinek and Chaudhurio )
13-40
-------
OH Q OOOH
ii i n • . .
0 + C-N -> C-N (41)
3
Pi 9
-C-N + HO „
2
Protection of the peptide link is afforded by the addition of hydrogen-
bonding compounds, such as benzaldehyde:
C H - C = 0
65 | :
H H
•
»
*
0
11
,C
The overall evidence of ozone damage to fibers is not compelling.
Dye Fading
0-Fadlng. The discovery that dyes faded under the influence of ambient
ozone was made by accident in 1955.^ The dye molecule is converted by
oxidation to much less deeply colored molecules. The phenomenon became
known as "0-fading." Laboratory tests had shown a new dye, Disperse Blue
27, to be resistant to attack ("gas fading") by nitrogen dioxide. Field
tests to confirm the laboratory findings were run on acetate draperies
containing this dye in a high-nitrogen dioxide area (Pittsburgh) and a low-
nitrogen dioxide area (Ames, Iowa). The draperies in both locations were
protected from sunlight. The result of 12 months of exposure was opposite
to that expected—the Ames draperies had faded more than the Pittsburgh
draperies. Ozone was identified as the damaging pollutant, and 0-fading
was found to occur only when Disperse Blue 27 was used on cellulose
13-41
-------
triacetate and polyester, but not with acrylic and nylon. The dyes most
susceptible to 0-fading were found to be anthraquinone blues, some reds,
and some azo reds. Gas-fading inhibitors (such antioxidants as
diphenylethylenediamine and tert-butylhydroquinone) are used to retard
fading. The American Association of Textile Chemists and Colorists Committee
on Colorfastness of Textiles to Atmospheric Contaminants (RA-33) later
conducted extensive tests,35 and these tests eventually led to the discovery
of fading problems due to the effect of ozone on permanent-press fabrics
and on nylon carpets."* Other very extensive tests on dye fading by air
pollutants have been carried out under the auspices of the AATCC Committee
RA-33, the EPA,36,37 and others.38
Test procedures established by Committee RA-33 include a test ribbon
intended to characterize the ozone content of air to which fabrics are
exposed. The test ribbon is dyed to the tertiary gray shade, with CI Disperse
Blue 27. Committee RA-33 has also established a test ribbon for nitrogen
dioxide gas fading.
Fading of Permanent-Press Fabrics. Permanent-press garments are blends
of polyester and cotton in a ratio of 50:50 or 65:35. The permanent-press
formulation includes a catalyst (zinc nitrate or magnesium chloride*), a
softener (polyethylene), a nonionic emulsifying agent, and a wetting agento
The anthraquinone blues react with the magnesium chloride catalyst to form a
chelate that is soluble in the polyethylene softener and in the emulsifying
agent, both of which, are contained in the "finish." In the curing process
(at 320-340 F,or 160-171 C), disperse dyes (e.g., anthraquinone blues)
migrate to the "finish"—i.e., migrate preferentially to the folds and creases.
13-42
-------
The dye in this substrate, at folds, fades under the influence of ozone.
Storage of garments in the summer in warehouses with open windows has
resulted in fading in as few as 10 days.^9 Remedial measures include
replacing anthraquinone dyes with azo disperse dyes, avoiding the use of
magnesium chloride catalyst, and using different surfactants and softeners,
Nylon Carpeting. Consumer complaints of fading nylon carpeting in the
warm, humid areas of Texas and Florida gave rise to the term "Gulf Coast
fading. "^ j1* 1 Laboratory experiments showed the fading to be due to a
combination of ozone and high relative humidity (above 65%). It was found
that fading was reduced on nylon fibers textured by dry heat, rather than
by steam, which produces a moisture-absorbing fiber structure. Such a
structure encourages diffusion of ozone throughout the fiber. Measures
have been taken to mitigate Gulf Coast fading, and it is no longer considered
to be a serious problem.
Economic Effects. Although measures can be and have been introduced
to eliminate dye fading due to ambient ozone, these measures are expensive
and represent a minimal cost of pollution damage that would otherwise be
sustained.
Oppenheimer42 and Waddell1*3 attribute the preliminary economic summary
in Table 13-17 to Salvin. These figures are based on increased costs of
fade—resistant dyes, inhibitors, research, and quality control. Also
included are costs to consumers of decreased product life. Waddell concluded
that the "best" estimate of damage to materials for all air pollutants is
about $2.2 billion per year.
13-43
-------
Table 13-17
Cost of Dye Fading, 1970a
Pollutant
NO
x
Material
Acetates
Rayon
Cotton
Spandex
Subtotal
Cost, $ Million
73
22
22
5
122
Ozone
Acetates
Nylon Carpets
Permanent Press
Subtotal
25
42
JL7_
84
a Derived from Waddell.43
13-44
-------
Other Materials
A number of rather tenuous arguments suggest ozone damage to such
materials as recording tape,44 asphalt,45 and dried milk.46 However, studies
on such subjects are scattered and generally uncorroborated. Some studies
even discuss beneficial effects of ozone, such as reduction of corrosion
rates in steel47 and improvement in adhesion of ink to polyethylene films.
Polyethylene is a major electric insulating material, and the suggestion
that ozone may "disastrously" affect its insulating properties48 bears
examination.
Laboratory studies carried out by Priest and his co-workers
have demonstrated by means of infrared and other techniques that terminal
double bonds in polyethylene end groups are attacked by "ozonized" oxygen
to form carboxylic acid groups and by rupture of the polymer chain to
produce short-chain dicarboxylic acids. A net gain in weight results.
Razumovskii5^ and his colleagues appear not to have been aware of the
work of Priest et al. and prefer to interpret their own results as supporting
a mechanism that involves attack of ozone on the CH -CH unit in polyethylene.
2 2
Rate constants for the reactions have not been measured, and no assessment
of the role of other oxidizing species has been made. However, it is pre-
sumed that a high-pressure ozonizer was used and that ozone was the active
species.
It is known that atomic oxygen reacts with polyethylene at room
temperature53 to produce a loss in weight and some morphologic changes.
The work of Trozolo and Winslow54 and of Kaplan and Kelleher28 suggests that
1
0 ( A ) also interacts with polyethylene to form hydroperoxides. Because
2 g
13-45
-------
3 -
polyethylene is known to be very stable to ground-state ( £ ) molecular
g
oxygen, the possible oxidants responsible for polyethylene damage in
1
polluted air are atomic oxygen, 0 ( A ), and ozone, Off «•£ HQ . Relative rates
2 g 2
of reaction are products of rate constants and concentrations of oxidizing
species in the real atmosphere. Thus the relative rates of reaction of these
species with polyethylene could be assessed, if we had rate
constants for their reactions with polyethylene. Because we do not, we
can assume that the rate constants parallel those of the reactions with
butene-yt, (see Table 13-3). With the concentrations in Table 13-4 and the
rate constants in Table 13-3, we arrive at the attack rates shown in
Table 13-13.
These results suggest that H02 may be the dominant oxidant that attacks
polyethylene or other materials in ambient air.
However, despite the known interactions of oxidants with polyethylene
and other polyolefins to form intermediate peroxy radicals,52 there is no
evidence that the chemical reactions go far beyond the surface. In fact,
polyethylene is specially treated with the products of a corona discharge
to improve the surface adhesion of printing ink.55 Winslow55 believes that
the effects of atmospheric ozone on polyethylene insulation and other
polyethylene products are negligible, compared with the embrittlement of
polyethylene by a combination of oxygen and solar ultraviolet radiation.,
The mechanisms by which this embrittlement occurs probably involve
sensitization to oxidation by absorption of ultraviolet radiation by
residual hydroperoxy and carbonyl groups in the polymer and by surface
13-46
-------
deposits of aromatic sensitizers from polluted air. Deterioration of the
electric insulating properties of polyethylene48 by oxidation in some
environments cannot be attributed to ozone. Damage to polyethylene by
ozone suggested by the figures in Table 13-5 is undoubtedly overestimated.
In view of the relative stability of polyethylene toward ozone, it is
surprising that the perfluorinated analogue (Teflon) reacts with ozone to
produce perfluoroformaldehyde and carbon dioxide.57 Because Teflon is
widely used to contain ozone-air mixtures, researchers are cautioned to be
aware of this reaction.
SUMMARY
In the context of this review, the term "photochemical oxidants" is
considered to be synonymous with "ozone." In test chambers that have
external ozone generators and that operate at or near atmospheric pressure,
ozone is the only likely oxidizing species. In ambient air, however,
ground-state atomic oxygen, hydroxyl radicals, and especially hydroperoxy
avA »*<*y ev/ei\ c(ov*\w>te
radicals can compete with ozone in attacking materials, such as rubber,
A
that contain olefinic bonds. The most economically important materials
with respect to ozone damage are paint, elastomers (rubber), and textile
fiber-dye systems. Damage to polyethylene by ozone is considered to be
negligible. The ozone-specific damage in 1970 to materials has been assessed
in economic terms and is approximately as follows: paint, $540 million;
elastomers, $569 million; and textile fibers and dyes, $84 million. Total
material damage attributable to ozone is, therefore, $1.22 billion. This
is to be compared with Waddell's estimate of total air pollutant material
damage of $2.2 billion. It is clear that otidavfc &re very important molecule*"
in pollutant damage to materials.
13-47
-------
RESEARCH RECOMMENDATIONS
• Laboratory studies of effects of photochemical oxidants other than
ozone—e.g., PAN, peroxybenzoylnitrate, atomic oxygen, excited
1
molecular oxygen, 0 ( A ), and hydroperoxy and hydroxyl radicals—
2 g
on specific materials should be conducted.
• Concentrations of oxidants other than ozone should be measured in
real atmospheres.
• Mechanisms of attack of oxidants on materials should be investigated,
so that distinctions can be made between effects on a given material
due to various pollutants.
• An integrated study should be conducted in which relative effects
of all major air pollutants on materials are assessed.
13-48
-------
REFERENCES
1. U. S. Environmental Protection Agency. Title 40. Protection of environment.
Part 50. National primary and secondary ambient air quality standards.
Federal Register 36:22384-22397, 1971.
0 U. S. Department of Health, Education, and Welfare. Public Health Service.
£• •
Environmental Health Service. National Air Pollution Control Adminis-
tration. Air Quality Criteria for Photochemical Oxidants. NAPCA Publ.
AP-63. Washington, p. C.: U. S. Government Printing Office, 1970.
3. Salmon, R. L. Systems Analysis of the Effects of Air Pollution on Materials.
CPA-22-69-113. Kansas City, Missouri: Midwest Research Institute,
1970. 84 pp.
4. Sanderson, H. P, The effects of photochemical smog on materials, pp. 7l-8"7\
In Photochemical Air Pollution: Formation, Transport and Effects. NRC
Associate Committee on Scientific Criteria for Environmental Quality.
Report no. 12. NRCC no. 14096. Ottawa: National Research Council of
Canada, 1975.
5. Upham, J. B., and V. S. Salvin. Effects of Air Pollutants on Textile
Fibers and Dyes. EPA-650/3-74-008. Research Triangle Park, N. C.:
U. S. Environmental Protection Agency, 1975.
6. Mueller, W. J., and P. B. Stickney. Final Report on A Survey and Economic
Assessment of the Effects of Air Pollution on Elastomers. National Air
Pollution Control Association Contract CPA-22-69-146. Columbus, Ohio:
Battelle Memorial Institute, 1970. 56 pp.
7. Campbell, G. G., G. G. Schurr, and D. E. Slawikowski. Final Report on A
Study to Evaluate Techniques of Assessing Air Pollution Damage to
Paints. Chicago: The Sherwin-Williams Research Center, 1972. 85 pp.
13-49
-------
8. Spence, J. w., and F. H. Haynie. Paint Technology and Air Pollution: A
Survey and Economic Assessment. EPA-AP-103. Research Triangle Park,
N. C.: U. S. Environmental Protection Agency, 1972. 49 pp.
>,. Waddell, T. E. The Economic Damages of Air Pollution. EPA-600/5-74-012.
Washington, D. C.: Washington Environmental Research Center,
U. S. Environmental Protection Agency, 1974. 156 pp.
lOa. Standard method of test for accelerated ozone cracking of vulcanized rubber
_/ Test method D-1149-64 (reapproved 1970)_7, pp. 554-560. In 1972
Annual Book of ASTM Standards. Part 28. Rubber; Carbon Black; Gaskets,
Philadelphia: American Society for Testing and Materials, 1972.
10-b. American National Standards Institute (ANSI) Test Method Li4, 174-19"73.
10c- American Association of Textile Colorists and Chemists. Colorfastness to
ozone in the atmosphere under low humidities. AATCC Test Method 109-
1972, pp. 137- . In AATCC Technical Manual.
11. Washida, N., Y. Mori, and I. Tanaka. Quantum yield of ozone formation from
o
photolysis of the oxygen molecule at 1849 and 1931 A. J. Chem. Phys.
54:1119-1122, 1971.
i2. Garvin, D., and R. F. Hampson.
National Bureau of Standards Interim Report
74-430, p. 11, 1974.
Hampson, R. F., W. Braun, R. L. Brown, D. Garvin, J. T. Herron, R. E. Huie,
M. J. Kurylo, A. H. Laufer, J. D. McKinley, H. Okabe, M. D. Scheer, W.
Tsang, and D. H. Stedman. Survey of photochemical and rate data for
twenty-eight reactions of interest in atmospheric chemistry. J. Phys.
Chem. Ref. Data 2:267-311, 1973.
13-50
-------
14. Ackerman, R. A., J. N. Pitts, Jr., and I. Rosenthal. Singlet oxygen in
the environmental sciences. Reactions of singlet oxygen 0?( A g)
with olefins, sulfides, and compounds of biological significance.
Amer. Chem. Soc. Petrol. Div. Preprints 16:A25-A34, 1971.
15. Huie, R. D., and J. T. Herrort.
Int. J. Chem. Kinetics (in press)
16. Huie, R. E., Jf, T.' Herron> and D. D. Davis. Absolute rate constants for the
additional abstraction reactions of atomic oxygen with 1-butene over the
temperature range 190-491R. J. Phys. Chem. 76:3311-3313, 1972.
17. Faliek, A. M., B. H. Mahan, and R. J. Myers. Paramagnetic resonance spectrum
of the *Ag oxygen molecule. J. Chem. Phys. 42:1837-1838, 1965.
18. Demerjian, K. L., J. A. Kerr, and J. G. Calvert. The mechanism of photochem-
ical smog formation. Adv. Environ. Sci. Technol. 4:1-262, 1974.
19. Test for formulated products, pp. . In 1^70 Annual Book of ASTM
Standards. Part 21. Paint, Varnish, Lacquer and Related Products.
Philadelphia: American Society for Testing and Materials, 1970.
20. Campbell, G. G., G. G. Scburr, and D. E. Slawikowski. Final Report on A
Study to Evaluate Techniques of Assessing Air Pollution Damage to
Paints. Chicago: The Sherwin-Williams Research Center, 1972. 85 pp.
21. Michelson, I., and B. Tourin.
Environmental Health & Safety Research
Association Contract PH 27-68-22, Aug. 1967.
22. Noble, P. Marketing Guide to the Paint Industry. Fairfield, N. J.:
Chas. H. Kline and Co., 1969.
13-51
-------
23. Stickney, P. B., W. J. Mueller, and J. w. Spence. Pollution vs. rubber.
Rubber Age 103 (9):45-51, 1971.
24. Newton, R. G. Mechanism of exposure-cracking of rubbers, with a review of
the influence of ozone. Rubber Chem. Tech. 18:504-556, 1945.
25. Crabtree, J., and A. R. Kemp. Weathering of soft vulcanized rubber. Ind.
Eng. Chem. 38:278-296, 1946.
26. Braden, M., and A. N. Gent. Attack of ozone on stretched rubber vulcanizates,
I. Rate of cut growth. J. Appl. Polymer Sci. 3:90-99, 1960.
27. Criegee, R. Products of ozonization of some olefins. Adv. Chem. Ser.
21:133-135, 1959.
28. Kaplan, M. L., and P.' G. Kelleher. Oxidation of a polymer surface with gas-
phase singlet ('A ) oxygen. Science 169:1206-1207, 1970.
O
29. Bogarty, H., K. S. Campbell, and W. D. Appel. The oxidation of cellulose by
ozone in small concentrations. Textile Res. J. 22:81-83, 1952.
30. Morris, M. A.
University of California, Davis, Bulletin
828, June 1966.
it. Kerr, N., M. A. Morris, and S. H. Zeronian. The effect of ozone and laund-
ering on a vat-dyed cotton fabric. Amer. Dyestuff Rep. 58(l):34-36,
1969.
32. Zeronian, S. H., K. W. Alger, and S. T. Omaye. Reaction of fabrics made
from synthetic fibers to air contaminated with nitrogen dioxide, ozone,
or sulfur dioxide, pp. 468-476. In H. M. Englund and W. T. Beery, Eds.
Proceedings of the Second International Clean Air Congress, Washington,
D. C., Dec. 6-11, 1970. New York: Academic Press, 1971.
13-52
-------
33. Jellinek, H, H. G., and A. R. Chaudhuri. Inhibited degradation of Nylon 66 in
presence of nitrogen dioxide, ozone, air, and near-ultraviolet radiation.
J. Polymer. Sci.: Part A-l. 10:1773-1778, 1972.
34. Salvin, V. S., and R. A. Walker. Service fading o£ disperse dyestuffs by chem-
ical agents other than the oxides of nitrogen. Textile Res. J. 25:
571-584, 1955.
35. Salvin, V. S. Relation of" atmospheric contaminants and ozone to light fastness.
Amer. Dyestuff Rep. 53:33-41, 1964.
36. Beloin, N. J. Fading of dyed fabrics by air pollution. Textile Chem. Colorist
4:77-82, 1972.
37. Beloin, N". J. Fading of dyed fabrics exposed to air pollutants. Textile
Chem. Colorist 5:128-133, 1973.
38. Dorset, B. C. M. Pollution and fading fabrics. Textile Manufact. 99(10):
27-29, 31, 1972.
39. Salvin, V.' S. Ozone fading of dyes. Textile Chem. Colorist 1:245-251, 1969.
40. Salvin, V. S. Effect of atmospheric contaminants on fabrics--dyed and undyed,
pp. 56-64. In Textile Quality Control Papers Vol. 16, 1969. American
Society for Quality Control, Textiles and Needle Trade Division.
41- Salvin, V. S. Ozone fading of dyes. Textile Chem. Colorist 1:245-251, 1969.
42. Oppenheimer, L. p. 540. In
N. I. Sax, Ed. Industrial Pollution. New York: Van Nostrand Reinhold
Company, 1974.
43. Waddell, T. E. The Economic Damages of Air Pollution. EPA-600/5-74-012.
Washington, D. C.: Washington Environmental Research Center.
U. S. Environmental Protection Agency, 1974. 155 pp.
13-53
-------
44. Somogyi, G. Effect of ozone atmosphere on the detecting properties of plastic
track recorders. Radiat. Eff. 16:233-243, 1972.
4i, Travnicek, Z. Effects of air pollution on textiles, especially synthetic
fibres, pp. 224-226. In International Clean Air Congress, London, 4-7
October 1966. Proceedings: Part I. London: The National Society for
Clean Air, 1967.
46. Kurtz, P." E., A. Tamsma, R." L. Selman, and M. J. pallansch. Effect of pollution
of air with ozone on flavor of sprayed-dried milk. J. Dairy Sci. 52:
158-161, 1969.
47, tiaynie, F. M., and J. B. Upham. Effects of atmospheric pollutants on corro-
sion behavior of steel. Mater. Protect. Perform. 10(11):18-21, 1971.
48. Grassie, N. Atmosphere on the attack. New Scient. 45:12-15, March 19, 1970.
49. Keller, A., and D. J." Priest. Experiments on the location of chain ends in
monolayer single crystals of polyethylene. J. Macromol. Sci. Phys. B.
2:479-495, 1968.
50. Priest, D. J. Fold surface of polyethylene single crystals as assessed by
selective degradation. I. Ozone degradation method. J. Polymer Sci.
Part A-2 9:1777-1791, 1971.
5!. Keller, A., E. Martuscelli, D. J. Priest, and Y. Udagawa. Fold surface of
polyethylene single crystals as assessed by selective degradation studies.
III. Application of the improved techniques to single crystals. J.
Polymer Sci. Part A-2 9:1807-1837, 1971.
52, Razumovskii, S. D,,, A. A, Kefeli, and G. E. Zaikov. Degradation of polymers
in reactive gases. Eur. Polymer J. 7:275-285, 1971.
.13-54
-------
53. Reneker, D. H. , and L. H. Bolz. Effect of atomic oxygen on the surface
morphology of polyethylene, pp. .In Symposium on Plasma
Chemistry of Polymers, American Chemical Society Meeting, Philadel-
phia, Pa., April 6-11, 1975.
54. Trozzolo, A. M. , and F. H. Winslow. A mechanism for the oxidative photo-
degradation of polyethylene. Macromolecules 1:98-100, 1968.
55. Hansen, R. H. , J. V. Pascale, T. DeBenedictis , and P. M. Rentzepis. Effect
of atomic oxygen on polymers. J. Polymer Sci. Part A 3:2205-2214, 1965,
56. Winslow, F. H. Private communications.
57. Daubendiek, R. L. , and J. G. Calvert. The reaction of ozone with per-
fluorinated polyolefins. Environ. Lett. 6:253-272, 1974.
13-55
-------
CHAPTER 14.
GENERAL SUMMARY AND CONCLUSIONS
The general summary and conclusions that appear below is a collage
taken from the individual chapters.
CHEMICAL ORIGIN
The major primary pollutants of importance to bxidant formation are
nitric oxide, hydrocarbons, aldehydes, and carbon monoxide. A few free
radicals are formed by photolysis of aldehydes and nitrous acid by sunlight
or by the reaction of traces of ozone with reactive hydrocarbons. These
free radicals initiate chain reactions involving hydroperoxy and alkylperoxy
radicals. During these chain reactions, the nitric oxide is converted to
nitrogen dioxide, and the hydrocarbons and aldehydes are degrated. The
photolysis of nitrogen dioxide by sunlight forms a free oxygen atom, which
combines with an oxygen molecule to form ozone. Because of the NO-NC^-O^
of Chapter 2,
cycle (Eqs. 1-3/) the ozone concentration is determined primarily by the
ratio [N02J : [NO] and so does not become large until most of the nitric
oxide has been converted to nitrogen dioxide. The total amount of oxidant
formed depends, in a nonlinear fashion, on the amount of hydrocarbons
available to continue pumping the nitric oxide to nitrogen dioxide. Al-
dehydes and even carbon monoxide can also serve this pumping function.
When some of the peroxy radicals recombine or react with the nitrogen oxides,
many secondary products, such as hydrogen peroxide and PAN, are formed.
Recent chemical modeling studies have been reasonably successful
In reproducing the concentration — time histories of smog-chamber experi-
ments. An examination of these models shows a need for much more detailed
chemical knowledge. Modeling studies also point out the necessity of
carefully defining the initial conditions of smog-chatr.ber experiments. Some
observations that have been made with these models are:
14-1
-------
» Even if hydrocarbons arc co; .\>1 c icly rwrmviHl i ro.a the air,
aldehydes and N(\. cap ^enei.:Lc hi[',h concent) at i ons of photo-
chemical oxidants.
• If both hydrocarbons and aldehydes are eliminated, carbon
monoxide and NOX alone can generate significant concentrations
of ozone.
• The concentration of ozone generated photochemically goes through
a maximum as the NOX concentration is increased.
• The steady-state concentration of free radicals in smog is
approximately 0.3 ppb and is rather insensitive to primary
pollutant concentration.
The concentrations, average lifetimes, and rates of attack of the reactive
intermediates can be calculated with chemical models.
The effects of free radicals on biologic surfaces cannot be
ignored.
The development of lasers has opened up several new techniques
for monitoring pollutants in the atmosphere. Sensitivities down to the
parts-per-billion range are claimed, and continuous monitoring is possible.
The photoionization mass spectrometer has been developed as a sensitive
detector for free radicals in the gas phase. A high-resolution mass
spectrometer coupled to a computer is capable of detecting up to 300
compounds in air, both in particulate form and in the gas phase.
AEROSOLS
Review of the literature provides ample evidence that aerosol formation
is an important part of the atmospheric chemistry linked with photochemical
oxidant production. The important chemical constituents of concern include
sulfate, nitrate, and secondary organic material.
Secondary organic aerosols, formed by gas-phase reaction between
nitrogen oxide, ozone, and hydrocarbons constitute an important fraction
of urban photochemical smog. Data obtained at high ozone concentrations
14-2
-------
(0.67 ppm) can be taken as an upper limit of the contribution of secondary
organic aerosols to the organic aerosol fraction and total suspended
particulate material (95% and 65%, respectively). Most of the identified
ambient secondary organic aerosols are difunctional compounds that bear
carboxylic, nitrate, aldehyde, and alcohol groups. The same compounds
have been identified in smog chambers from C_ cyclic olefins and diolefins,
with gas-to-aerosol conversion factors exceeding by more than an order of
magnitude those measured for the ambient average conversion of all reac-
tive hydrocarbons. The formation of such species in the gas phase in
excess of their saturation concentration followed by condensation on
preexisting particles and further growth in the light-scattering range
is the predominant physical mechanism that controls the gas-to-aerosol
conversion process.
Because of their very low vapor pressures, difunctional compounds
are readily converted to the aerosol phase, whereas more volatile
monofunctional compounds require much higher precursor and ozone concen-
trations to reach their saturation concentration. This explains why
most of the'*tompounds formed from alkenes remain in the gas phase, whereas
C cyclic olefins and diolefins are efficient aerosol precursors. How-
ever, there is no known source of the latter class, so cyclic olefins,
identified in both gasolines and auto exhaust, can be regarded as the
most important source of secondary organic aerosols. The role of aromatics
as aerosol precursors is essentially unknown. Because of their accumulation
in the submicrometer range, all secondary organics are potentially
dangerous. However, there is almost no information on health effects
associated with the presence of such compounds in the atmosphere.
Because the conclusions presented in this chapter rely heavily on
a few recent studies, it is extremely difficult to relate the urban con-
14-3
-------
centrations of secondary aerosols to the concentration of their gas-phase
precursors. Simple relations of the type d(secondary aerosol)/dt = a
(precursor) (ozone) have been derived from smog-chamber data for organic
aerosol formation in mixtures of cyclic olefins and NO and sulfate
X
aerosol formation in mixtures of NO , sulfur dioxide, and C alkenes.
X J ^
Such kinetic data are consistent with the organic (a few micrograms per
cubic meter per hour) and sulfate (up to 13%/h) aerosol formation rates
observed in photochemically polluted urban areas. More complex kinetic
relations reflect certainly all the possible variations between these
extreme and rather simple systems. Although control of ozone, through
control of NO and total hydrocarbon emission, would obviously have a
x
roughly proportional effect on the formation of organic aerosols, present
data suggest the identification and control of a few specific hydrocarbon
precursors as an alternative approach. The contribution of photochemical
reactions involving hydrocarbons to inorganic nitrate and sulfate aerosol
••s.
formation "remains to be determined. More data on the identification of
hydrocarbon precursors and on the kinetics of formation, physical parameters,
and health effects of their products would ultimately permit quantifying
the complex relations between secondary aerosols and ozone concentrations
in urban atmospheres.
ATMOSPHERIC CONCENTRATIONS OF PHOTOCHEMICAL OXIDANTS
In comparison v;ith previously available piaterial on atmospheric con-
centrations of photochemicaloxidants, we now have a far richer data baye and
a deeper understanding of how to interpret the reported concentrations. The
recent information on hydrogen peroxide and the broader geographic coverage
of measurements abroad are examples of new data that have come to light.
14-4
-------
Subtleties in future standard-setting must consider receptor damage in
terms of exposure location and time and receptor distributions and response
functions. The formula for damage function points up the need for improved
knowledge of spatial and temporal distribution. The use of second-to-worst
hourly readings for an ambient air quality standard must give way to a
specification stated in terms of a statistically defensible higher-frequency
event. This will reduce substantially the uncertainty inherent in confining
one's attention to the. "worst case."
Long-term trends in oxidant concentration canrot be identified with
nearly the degree of certainty that we might like. The data suggest a
decrease in oxidant concentrations in central-city areas and an increase in
downwind areas. Measurements of nonurban oxidant are exhibiting a higher
frequency of violations of the ambient standard than was once believed to
occur. Figure 4-43 shows typical ranges of concentrations in various regions
in and out of urban complexes.
Probably the most critical question today regarding atmospheric concen-
trations of ozone and other photochemical oxidants is, "uliat fraction of the
observed values in each locale is susceptible to control by anthropogenic
emission reduction?" As brought out in this chapter, there, is one school
of thought embracing the idea that nature frequently presents us with con-
centrations that exceed the U.S. national ambient air quality standards.
The other point of view is that globaJ background ozone concentrations do not
exceed 0.05 - 0.06 pp:n at the surface and that higher concentrations than
this have anthropogenic sources.
The data presented in the literature reviewed above support the second
point of view. The observation of ozone concentrations exceeding the ambient
standard in nonurban areas does not demonstrate that this is of natural
14-5
-------
origin. However, the measurement£3 in remote areas of the northern hemisphere,
compared with those in the continental United States, do support the thesis
that anthropogenic soui'ces are involved in cases where the standard is
exceeded.
This is a very broad conclusion, and additional measurements must be
made. Some of this effort (which is goingon) should address the problem of
other pollutants and condensation nuclei that accompany the nonurban oxidant.
Interpretation of these measurements will increase the specificity of
separating anthropogenic sources from natural background sources. Theoretical
assessments of the existing observations will shed ligh't on the relative
roles played by stratospheric injection, plant emission, background methane,
and dry deposition on surfaces in the natural portion of the tropospheric
ozone cycle.
Geographically, our best measurements have focused on the Los Angeles,
California, region because of the severity of the problem there. The
Regional Air Pollution Study and its extensions will, it is hoped, supply
an additional rich data base for the St. Louis, Missouri, region. Airborne-
pollutant measurements aimed at specific experimental objectives are needed
in the central and eastern areas of the United States to broaden the foundations
of a national control strategy. Existing ground-based continuous monitoring
networks will not provide an adequate basis for the regional control of
oxidant. Ad hoc, one-shot aircraft measurements have led mainly to specu-
lation that can establish incorrect attitudes on the origin and fate of nonurban
ozone. In the vigor of environmental control efforts, incomplete data sets
have stimulated hasty targeting on specific sources (for example, rural
vehicular emission, power stations, trees, and frontal passages).
14--6
-------
Another subject of recent interest has been tbe question of indoor-
outdoor oxidant concentrations. Available measureiuc-nts and models suggest
that indoor exposures may be substantially reduced by appropriate choices
of ventilation systems, air filters, and interior surface materials. The
cost-benefit relationships coming from these studies may well have a great impact
on future decisions based on atmospheric concentrations of oxidant pollutants.
Much care must be exercised in comparing atmospheric concentrations
between one place and another because of differences in primary ca]ibration
techniques or in instrumentation. Chap.er 6 summarizes these problems in
detail.
MODELS FOR PREDICTING AIR QUALITY
The literature contains reviews of air quality modeling that stress
special purposes. Some concentrate on meteorologic aspects, and others combine
this with air chemistry. Proceedings of several conferences are another
information resource. Recent surveys have been addressed specifically to
photochemical modeling problems. It may be concluded that, although they are
relatively complex, the photochemical-diffusion models perform as well as, if
not better than, available inert-species models.
A variety of goals and objectives may be met with air quality modeling.
They are summarized as:
• Scientific understanding of atmospheric phenomenology,
• Rational application of the regulatory process.
• Land-use planning within environmental constraints.
• Real-time control of episodes.
14-7
-------
The fundamental elements of deterministic models involve a combination of
chemical and meteorologic input, preprocessing with data transmission, logic
that describes atmospheric processes, and concentration-field output tables or
displays. In addition to deterministic models, there are statistical schemes
that relate precursors (or emission) to photochemical oxidant concentrations.
Models may be classified according to time and space scales, depending on the
purposes for which they are designed.
Specific model applications to the oxidant problem include both the
simple rollback (with modifications) and the photochemical-diffusion tech-
niques. Very little modeling of intermediate complexity seems to have been
attempted for the oxidant system.
Model performance is now receiving critical attention because of the need
for cost-effective control measures. Standard statistical performance de-
scriptors can sometimes mislead a prospective user; therefore, more specialized
tests are being devised. Various model types are being compared for a specified
set of initial and boundary conditions. It is apparent from these studies
that added fidelity is purchased at the expense of added complexity of a logical
structure that must represent the controlling phenomenology.
MEASUREMENT METHODS
With the exception of calibration, the measurement problems which
were apparent in 1970, at the time of publication of the first air quality criteria
document on photochemical oxidants, have essentially been solved for ozone.
This remarkable achievement is the result of unstinting efforts by individuals
working at EPA's National Environmental Research Center, North Carolina;
the National Bureau of Standards; private research contractors sponsored
14-8
-------
primarily by EP. ; private instrument manufacturers; the Jet Propulsion
Laboratory of the California Institute of Technology; the Air and Industrial
Hygiene Laboratory, California Department of Health; the Air Pollution
Research Center of the University of California at Riverside, and the Califor-ia
Air Resources Board (CARB).
Due to the focus on the problem brought about by the CARB , a
significant advance in the accurate calibration of instruments for monitoring
ozone in ambient air was achieved during 1975. Asa result, this agency
adopted the measurement of ozone in the ultraviolet region at 254 run as a
primary calibration reference standard. They have also adopted statewide,
as a transfer standard for calibrating ozone and oxidant monitoring instrumer.-.3
at air monitoring stations, a commercially available instrument (coupled with
the precise controlled generation of ozone in air), which measures the dif-
ferential absorption of ultraviolet radiation.
It is important to separate conceptually, and in practice, the
calibration process from the monitoring process. Photochemical oxidants
consisting primarily of ozone were first continuously measured in Southern
California by measuring the color change of potassium iodide solutions brought
into contact with the ambient air. This measurement continues to yield valic
photochemical oxidant data in California. However, it has yielded questionable
data at ambient air monitoring sites elsewhere in the United States. For this
reason at the end of 1971, EPA officially adopted a continuous monitoring
process that measures the chemiluminescence produced when o?,one in air is
brought into contact with the gas ethylene. This reference procedure when
calibrated with the primary reference procedure using ultraviolet absorption
is widely accepted.
14-9
-------
Instruments based on differential ultraviolet absorption still
need to be evaluated, and possibly modified, prior to their acceptance
for monitoring ozone in polluted atmospheres on a nationwide scale.
The California Air Resources Board and other air pollution control
agencies are currently conducting multi-year programs for evaluating
ultiaviolet absorption side-by-side with chemiluminescent and potassium
iodide based instruments, to determine their applicability and
needed modification, as well as to assure continuity in the data base
•while the older monitoring instruments are being replaced.
Thus despite the remarkable progress in the monitoring for ozone,
nitrogen oxides and non-methane hydrocarbons, which has strengthened the
implementation and evaluation of control programs, substantial research
and development is still required to help resolve the uncertainties in our
knowledge which 3.re inhibiting the actual achievement of desired air quality
standards.
RESPIRATORY TRANSPORT AND ABSORPTION
This chapter har, discussed tho. general approach required to rood«I
the transport and absorption of ozone and other pollutant gases in the
respiratory tract. For unraactive or very weakly reactive gases, there
are a few models that are qualitative descriptions for assessing total
dosage and dosage in major regions. However, there is no adequate model
for gases like ozone, which are strongly reactive within the mucous
and tissue layers.
14-10
-------
TOXICOLOGY
The acute lotlviJ act .1.0,1 or or- :>:'_• i" due Lo its capacity to prodj.cc
pjlrnonary edema. The LCr. for rats and ndce c tco",'d for a single 4-h
is approximately C pp:n, cind cats, rabbits, guinea pig.c; , and do;js
(in that order) arc decreasing!/ .':.u:;coptible in the lethal action.
Numerous review's have considered the tcxieity of ozone at Jetlial <:a;d
1 ox\7er cone jnt ration s .
In the foregoing discussion ami in Table 14-1. attention has focused
on studies in laboratory animals th.it have bacn exposed to ozone concen-
trations of about 1 ppm or less, because results of studies conducted
with such concentrations are thought to be irore directly relevant to
ambient oxidant air pollution, which is the source of exposure for largo
human populations. In Table 14-1, no attempt has been made to list all
studies; more comprehensive suirnvaries am te found JJi some of the mono-
graphs cited. Instead, the table cites studies thought to be most useful
for evaluating the health ini£ilic:jtions of exposure to ]ov; concentratjc.nj
of ozone, and the concentrations listed arc the ,lo",;est at which the
described effects have been observed. Unfortunately, m;my studies have
not included a sufficient range of oqperin.'jntnl concoiTb"al-Jcnr> to pc-n^ilt
construction of reliable dose-response curves or to cvetermJ ne vdiat, if
any, would be a "no-observed-effcct" concenti-ation for the o:/x;rimental
conditions usad. Zilthough it is ujvilcrstandable that research scientists
find little stimulation in conduct jng exposure experiments at concen-
trations that fail to pro. iuce cliongcs in the biologic system in which
they are interested, the conduct (and reporting) of such experiments .is
extremely important for a pragrratic evaluation of the implications of
positive findings for human health.
The table illustrates tha wide variety of biologic effects produced
in laboratory animals exposed to relatively low concc-ntxations of ozonoc
-------
1
-r"*
u < n
OC,
P O
IH
O
£
•rl
28J
H
8
r-t
£
J?
^'J?«
3 Ji •'-'
M (C T>'
Q rH b
8 2 -8
7j~c
-P t/3 >i
S£.ti
^§:1
fi d -iJ
Ch '/-•
VI O
O rq 4-i
^,'
OJ c; TJ
CJ Q O
-; ,:- o
>*J x r;
rCj l,-'^
ri '£
ti <~
< W X
£ >l g
r-~ ro M
^^^^
jf
!a
4->
r
fd
TJ
•rj
(j
O
.i J
v'
'L
^ t
03
JU
m
K
O
.u
i1
1
rH
4-1
a
fi
oj
&
n
7
ii)
jj
«!
c;
•A
o
p
03
TJ
0)
f.J
M
S"i
' i
P
03
^>i
n?
rd
r-
6
?!r>
5»-
ll
O TO
•H 4J
-U -H
U< >>
R
rJ q
(-3 -A
r;
8§
t — i
S
d >i
b^rH
f?^
O -H
JJ
H nj
rj H
•H CO
X*
?iti
X -rl
o ro
at
41
,°i
S^
S4 O
! N
W O
q u-t
1°
J 0'
•H T-l
> 4J
(3
.2.b
4. B
cj ;j
o :\
'H CJ
M) CJ
«
03
4-> -J
q ,q
ra 4J
u
•H 4-3
'II fj
'r! c/3
t)i 4-1
•H (j
W H
IV^e I alveolar Sat
£i
•rl
03
O
fn
£H
r]
rc.!
CJ
^
:d
^
J;l
s
Ml
0
Q
,C
ri
03
M
'oj
U
H
H
I
f-i
>i
J5
"S
Ji
PI
rj
i-l
8
*!
or
H
OJ
O
b,i
^
bi
i3
(!)
b M
')
• •* !-:
« :J
Or-'
%*
a >T>
* U
T1 rH
H -
r^i ';;'•-
•r-l
C ,r;
•H
OJ (d
03
a 3
M .-i
C) -P
.Hq
c,1^1 03
^^ T|
-H Tj
03
:J CM
O n
J i
n co
•H CM
4-1
r: M
8 3
o
r,
• t.
B1
•.H
•9
4J
01
(')
'(i)
•5
C)
f)l
> ,
'j
H
"o
o
;;;
cj
t/i
(3->
•H
j j
i'3
C)
tn
03
>i
Ii
r-l
H
5
^
C^Q
8 M
^
ti a
ll-l Oj
&«'
0 rH
4J rj
' J ^ '
M J-j
H a
Oj4J
03 :-;
g"1
g^
•M
R,S
^
£ ($
O r-(
g
1
f
IjJ^
>, a 3
•-rla.l
> O 0
•H -H rj
4J 4-1
o d M
r- ]j .S
ri1 s a
L: U
c r; 03
p C5 W
fi u o
u
r?<) D1
a J -n
4-i 'W f)
:-1 'M CJ
•3 O ^
i-f 1 ^
O O O
> « J-i
rrt •» •>.
o oj "j
(.3 M O
tj'jt!
ci il 8,
') X •! ,'i
r^ci
i
&S
"H U
&£
(U 3
rd 03
xp
-P 6
9 r:'
03 0
d) >t
M -H
Cj -
CJg
S'iJ!
M V-j
0 P
o
0
14-12
-------
#
cu
.S
a
o
o
rH
S
.5
k
to
o
CD
u-j
W
1
h
O
t/1)
O
4->
t-J "~X
^4 1
r1 ^
b 3) W •
fl n g°
M_l CO OJ 4J
o § g1"3
£2 £13
.tj 4J >i W
.gjs-ss
rj d fo M
n --1 °
si &i5.g
13 ^l^
d ^ 0^41
s^>^d
n d a, cj
y T3 i -H
H -H LO 4-1
X 1 -H
n-! H W gi
0 '.U O -H
•P & CJ CO
d y
i-H d) rH >,
cu c en 4J
M 0 -' -H
SiS^-J
S^5^
3
4-1
§
i
1
u)
^
1-1
1
l/l
^-
1
u
8
zed airways
ium-si
*X3
.5
CO
CD
tn
•6
o
•H
jf
O
I
4J
1
§
ormati'
4-1
1
*8
s^
3 co
H
•H
2
3
i
(!) H
4-5 0
(TJ 0
& >
to"1 d
0,
0-j -f~t
P) U
\-i d
^-1
M C)
O '-0
CO -0
r^T-H
T:1 O
b 2
-t !-l r-!
u m
O I
Q on
rly related
^
•3
(j)
\j CJ
rrf &
Q-j
to
4J
to
0) CX
tn 3
3: Q)
p' 0
d
gs
jj
3
0)
CN Oi
O
-P r— 1
-^
5 u
r-l 0
M—J *T— 1
l|
r$ ^~)j
U) ^O
r3 cxj
O •
>4 0
i— 1 d
(rt
ffl
•3
3
d
1
m Q)
° n
frequency
tidal vol
•5-3
0) 0)
co co
d d
0 (U
M M
U 0
S cu
•3 T3
o'P rto
0 0
CO CN
£j
1
sterase
(no
C ^i
•H -P
rH -H
5d
O (Ji
T1 [J
Ipil
S 0
10 -II^
3 1 a
GJ M Qi
V°m
•S'S^.
M to o
d
13
-------
c
o
o
-a-
rH
B -
IH H
rH
rj
1
1
alities
o
1
rH
! g
£ 3
^
o
q 1
a
o
H
1
in
«
o
-P
•rl
X)
U
p
C
3
rH
^
P
q
>4H
o
ition i
,Q
•pi
'2
M
^q
n
01 tO
ni '!)
P t!
6 o1
.- CJ
tO rH
}-,' 'J
°j r -I
) O
r; O
!-l !•!
ri O
rH (J
•J rH1
•SB,
"J m
,.. o
.-1 O
',- JJ
>i CJ
M rj
q 'ci
i
H i d
XI M
to rj g
q d d
O -P
•rl C1J -H
•p q >
(3 3
Alrer
ir.embr.
serum
.p
^
in
rH
CJ
01
1
esis
1
'<
^
Q
cji
fj
01
rfl
OJ
S-l
CJ
c-j
vo
4J
n
nse of specif L
ed-rospop.se
as
to >
CU 0
U 4-*
. ,_) -)
•r-l H3
TJ r-l
W iTj
OJ -H
cn ^rH
q to o
rj OJ O
X! r-l >
O O rH
-r-l (Tj
u .q
•H O rd
tn q ai
O O 4->
r-l S-i ra
O XJ -H
.q c;
pi >i O
S M hi
q o 01
^•H ij CO
g
q p-i
-P ' ^4
O (J
O MH n
c»
CO
o
l(
in
«
0
OJ
01
^ -P
0)
ated with ozon
chronaxial
r- 1 M
•H O
1 1
^>
Q) frt
tJi -q
rd CJ
O X)
01
M-l q O
o -a ,j
OJ CU rj
CJ g> !H
•H U O
O CO
s sg
rj
•H
rH
& '4
til >1
rrj
-P
O n
"Z, en
l-O
*
o
dJ
01
ial killing in
bacter
UH
o
Is
s!
01 -P
rrj
CD 01
o H1
0) P
Q rH
(£4
rr
O3
t
O
3
M
-------
a
0)
0)
Ul
>,
Ul
a
8
'J
•
to
$
I
w
1
4-1
O
8 Ei
•H p
-P CO
i Q
•ti 8
5^
sl
•Si
10 r~)
rd O
P
S-S
§,
to id1
rJ T)
IK
d 6 j-t
M p M ^
H v t ,"i n
tr*
fl
3
1-1
.3
0)
CO
e hydroxyla
TnLlCOSci
benzopyren
obronchial
Decreased
and trache
^
to
T"J
I
r^
•H
n paratiiyro
changes i
liistologic
r.
CO
i
£*
*rn
1
-P
rd
U
nrir.ed alte
activities
UJ
« i
10 &
>i C
33
8H1
Histccherrd.
several lu
to ii
% '3
•£j r-
-P
d o
^^^
rt &
rd m
r-M •
fio
•d rq
g§
D1CM
H '
^°
4J
4-i rd
activity o
no effect
Increased
lysozyms (
co to
§1
•Sco
-p O
f* .(— I
'01 r^
r^
cu
01 Tj
o ,^
•In §
-i^o
.p -H rj
U 4J 01
d >i fl
TJ 'o §
0 CJ &
o.' >i 0
H) rH U
OJ DlTJ
clTl^1
c c cD
M iy •a
to
>i
^
N
H
^1 *rn
4J CU
n3 fd
j_i .,-^
•H r*
P-, O
01 §
0 3
n cj
0 U,
rd
4^-i
d.S
•r4 (0
X! J
•H 0
4-1 -H
DJ W
8^
CO 4-J
3 -H
to ^
r-j C
(_)
(I)
ulating red
to decreas
S3
^1
to
to o
QJ D<
••H X
n3 C rd tjj
(DO Q
W -iH X) J-l
rt! 4-1 0)
QJ O NX;
bS .sS
C C Op
H -H a ci
in d
>i^
rg ^_
x; >i s x:
t*.
U)
o
c
'o
ty
CO
S '> 3
O rd oo
•H OJ _
4-J ^J C
J3 ow -^
^1 co iJ
0 ro rj
4q CU
>t DI
'CJ C c\o
O do
xi (-4 m
3
d
.3
4-»
.a
fTj
G
8
C
(n
4_j
&
-S
to
cu
ro c!
X! -H
00)
H 0
SH,
Ig1
63
XJ
4J
^1
0
O
!
CO
to
i
to
H
lood vesse
pillaries
^s
!r
&H
fi-S
X!
U 4-1
CN
o c.
If
o r
5-11
4J
s
o
I
o
03
o
CO
o
m
co
o
14-15
-------
C -:
8
fi
4-1
w
rQ
O
•8
O
•rH
OJ
^
4-) m
sp.
aii
q g
§
O j-j
o -bi
1
o
LO
^
I
Oi
sed lung cytochror
Decr
4J
8
u/
^.rs
tion
atio
-G
of
tn
a. w
a) ><
0 aj
rH ^3
w
r-
H I
a •*
•
•M
sS
^•; 4-1
o, (d
4-1 4-J
O MH
TJ <"
d o
rH
0)
•H
^-i 01
O w
4H 0)
ro CM
i
rrt
>a
4-) 44
fl O
OJ C
-C '4J
Pi rt)
1 a!
rH
.N 0)
U) U
•rH O
4-1 fi3
•H
rH •-
bronchio
changes
pnent
u o
•-•H rH
W P 0)
•H O >
4-) M 0)
•A a *
o 4H JH
f-! 0
S|N
33 n3 -P
to
3 O WJ
0 -P .q
3 4-1
5 o< a
•H 3 Q
4-) d
C M
Q O co
O 4-1 rH
>i
">
'$
O
(tj
tn
*n
5
P
Cj
luntary
o
>
^
01
i
S-i rH
p GJ
XJ ^
4.1
o •-
(11
&> CJ
q H
•H O
d -r-j
3
A4 O
u a
•r-l 0
,C !H
e xi
rH
rH
^ii
r~H
O '+-)
•H 0
c; tri
0 -rH
•p
'HI
a
'H tn
o r;
•rl
rmation
result
o .q
m 4J
•H
•> 3:
Hi W <0
aj^ I1
m r-l &
4J O -rj
(d U ro
Guinea pig
8
01
•H
C/)
(U
§
rH
IK
1
-------
CONTROLLED STUDIES ON HUMANS
Convincing new information on the health effects of oxidant
exposure has emerged from controlled studies on humans, from which tentative
dose-response curves have been constructed. The new data show statistically
significant reduced pulmonary function in healthy smokers and nonsmokers
at ozone concentrations at and above 0.37 ppm for 2-h exposures. Other cases
and aerosols found in an urban atmosphere were not present in these experiments.
Some studies suggest that mixtures of sulfur dioxide and ozone at a
concentration of 0.37 ppm are more active physiologically thai: would be
expected from the behavior of the gases acting separately.
Wide variation in response among different individuals is a general
finding in studies of oxidants, as well as other pollutants.
Undesirable health effects of oxidant air pollution exposure are
increased by exercise, and many people apparently limit strenuous exercise
voluntarily when oxidant pollution is high.
Safety, ethical, and legal considerations require that the utmost
care be exercised in human experimentation. The risk inherent in this work
can be minimized by taking reasonable precautions while ensuring the satis-
factory performance of the study.
14-17
-------
PLANTS AND MICROORGANISMS
Oxidant injury to vegetation -was first identified in 1944 in the Los
Angeles basin. Our understanding of oxidant effects and of the widespread
nature of their occurrence has increased steadily since then. Although the
major phytotoxic components of the oxidant (photochemical) complex are ozone
and peroxyacetylnitrate (PAN), indirect data support the contention that other
phytotoxicants are present in the photochemical complex. Ozone is considered
the most important phytotoxic component and was first identified as the specific
cause of weather fleck on tobacco and stipple on grape. PAN is associated
with the undersurface glazing and bronzing associated with many of the vegetable
crops.
Plant response to oxidants (including ozone and PAN) is often divided
into visible and subtle effects. Visible effects are identifiable pigmented,
chlorotic, and necrotic foliar patterns resulting from major physiologic
disturbances. Subtle effects produce no visible injury, but include metabolic
disturbances and may be measured on the basis of growth and long-term
biochemical changes. These effects may influence plant populations and
communities and could have an adverse influence on ecosystems. Visible
injury may be acute or chronic. Acute injury breaks down the cell membrane
and causes cell death, with leaf necrotic patterns that may be characteristic
for a given oxidant, but can be confused with other stress factors. Classic
injury from ozone is the upper-surface fleck on tobacco and the stipple of
grape. Many plants show an upper-surface bleach -with no lower-surface
14-18
-------
injury. Bifacial necrotic spotting is common and may appear flecklike.
Classic injury from PAN appears as a glaze followed by bronzing of the
lower leaf surface in many plants. Complete collapse of leaf tissue can
occur, if concentrations are high. Chronic injury is associated with
disruption of normal cellular activity followed by chlorosis or other color
or pigment changes that may lead to cell death. Chronic injury patterns
are generally not characteristic and may be confused with symptoms caused
by biotic diseases, insects, nutritional disorders, or other environmental
stresses. Early leaf senescence and abscission may result from chronic
exposure.
Leaf stomata are the principal entry sites for ozone and PAN.
Stomata, when closed by any of a number of factors, will protect plants.
Ozone and PAN may interfere with various oxidative reactions in plant cells.
Membrane sulfhydryl groups and unsaturated lipid components may be primary
targets of oxidants. Physiologic leaf age is an important consideration in
the response of the leaf to oxidants. Young leaf tissue is more sensitive
to PAN, whereas newly expanding and maturing tissue is most sensitive to
ozone. Light is required before plant tissue will respond to PAN, but not
to ozone. Oxidants affect such physiologic processes as photosynthesis,
respiration, transpiration, stomatal opening, metabolic pools, biochemical
pathways, and enzyme systems. The acute response of plants to ozone and
PAN may result from a saturation of sensitive cell sites and a disruption
of normal cellular repair mechanisms. Chronic injury probably results
from secondary reactions involving membrane injury.
There is evidence that ozone is a radiomimetic gas. Ozone affects
pollen germination in some species and thus may directly affect yield. A study
with Arabidopsis thaliana suggested no mutagenic effects from ozone on this
plant over five generations.
14-19
-------
Ambient-oxidant studies in filtered versus nonfiltered field chambers
have reported up to 50% reduction in citrus yield (orange and lemon), a 10 -
15% reduction in grape yield in first year and 50 - 60% reductions over the
following 2 years, and a 5 - 29% reduction in yield of cotton lint and seed in
California. , Losses of 50% in some sensitive potato, tobacco, and soybean
cultivars have been reported from the eastern United States. It is apparent
that ambient oxidants do reduce yields of many sensitive plant cultivars.
Growth reductions associated with acute exposure to ozone are often associated
•with injury; sometimes the correlations are high. Even multiple exposures
and sometimes chronic exposures have shown fair to good correlation between
injury and growth (biomass) reductions. The greater reductions in root
growth than in top growth reported in several species are related to solute
transport and may be fairly common under some conditions. Ozone affects
nodule number, but not nodule efficiency in clover, soybean, and pinto bean.
This causes a reduction in nitrogen fixation associated -with legumes and, if
•widespread, could have a major impact on plant communities and affect
fertilizer needs. The effect on nodulation is related to carbohydrate supply.
Yield reductions •with little injury after chronic exposure are known for
several crops. Severe injury in tomato was required before a yield reduction
was found. Chronic exposures to ozone at 0. 05-0. 15 ppm for 4-6 h/day
will produce yield reductions in soybean and corn grown under field con-
ditions. The threshold appears to be 0.05-0. 10 ppm for some sensitive
cultivars and is well within values monitored in the eastern United States.
Growth or flowering effects, at chronic exposures to ozone at 0. 05-0. 15
ppm for 2-24 h/day are reported for carnation, geranium, radish, and pinto
bean grown in greenhouse chambers.
14-20
-------
Plant sensitivity to ozone, PAN, and other oxidants is conditioned
by many factors. Genetic diversity between species and between cultivars
within a species is well documented. The mechanism of genetic resistance
is known for only one onion cultivar and is related to the effect of ozone
on stomatal closure. Variants within a natural species are -well known for
several pine species, including white, loblolly, and ponderosa. Plant
sensitivity to oxidants can be changed by both climatic and edaphic factors.
A change in environmental conditions will initiate a change in sensitivity at
once, but it will be 3-5 days before the response of the plant is completely
changed. Plants generally are more sensitive when grown under short
photoperiods, medium light conditions, medium temperature, high humidity,
and high soil moisture. Injury to PAN may increase with increasing light
intensity. Conditions during exposure and growth affect the response of
plants to oxidants in similar -ways. However, plants exposed to ozone are
more sensitive to increasing light intensity and, in some cases, to decreasing
temperature during the exposure period. In general, growth factors that
tend to cause a physiologic hardening of plant tissue make the plants more
tolerant to ozone. At the time of exposure, factors that increase water
stress tend to make plants more tolerant to ozone. Soil moisture is probably
the most important environmental factor that affects response during the
normal growing season.
Plants respond in different ways to pollutant mixtures; less than
additive, additive, and greater than additive effects have been reported.
Mixtures of ozone with sulfur dioxide and of nitrogen dioxide with sulfur
dioxide can cause oxidant-like symptoms in some sensitive plants. Mixtures
can cause effects below the threshold for either gas, although there is some
14-21
-------
disagreement on this in regard to ozone. Ratios of mixtures, intermittent
exposures, sequential exposures to pollutants, and predisposition by one
pollutant to the effects of a second pollutant may all be important in nature,
but little research has been done.
The response of some plants to oxidants is conditioned by the
presence or absence of biotic pathogens. Depending on the plant and the
pathogen, oxidants may cause more or less injury to a given species.
Pathogens may protect their host or make it more sensitive. The pathogens
themselves may be injured or may be protected by the host plant. This
subject is just starting to be understood.
Oxidant injury to ponderosa pine predisposes the trees to later
invasion by pine bark beetles. Ozone and ozone-sulfur dioxide mixtures
may decrease the population of soybean nematodes. Both greater and smaller
effects have been noted when herbicides have been used in the presence of
high oxidant concentrations.
The two most critical factors in terms of air quality standards are
duration of exposure and concentration. These two factors determine the
exposure dose for a plant. In determining the response of vegetation, con-
centration is more important than time. A given dose presented to a plant
in a short period has a greater effect than the same dose applied over a longer
period. This suggests a. threshold effect for plant populations and is probably
related to the repair mechanisms inherent in biologic systems. Sufficient
information is not available from long-term chronic studies, but a. threshold
between 0. 05 and 0. 10 ppm is probable for ozone (oxidant). For acute effects,
an overall threshold concentration with respect to time can be determined
from Figures 11-6 and Table ll-24a. Fcr pinto bean (Table 11-22), this threshold
14-22
-------
for injury is about 0. 03 ppm for 8 h and about 0. 10 ppm for 1 h. This
suggests that oxidant standards may be needed for periods up to 8 h.
Vegetation can act as a major sink for oxidants over time, but has a
relatively minor effect on oxidant concentrations during episodes of high air
pollution, is more effective at some seasons or under some cultural and
management practices than others, and should not be considered an important
contributor to short-term reductions in oxidant or ozone concentrations.
Plant protection from air pollution stress has involved three types of
programs. Several researchers are including pollutant stress in standard
breeding programs with the aim of developing resistant cultivars. Our present
concepts of pollution effects suggest that the gene pool of all species is large
enough to permit the development of more tolerant cultivars. Natural selection
•will slowly do this for native vegetation. If pollution concentrations go no
higher, this should be an effective protection device. Interim measures
involve the use of chemical sprays. Such sprays are not yet economically
feasible, but several do give adequate protection against oxidants. Fungicides,
such as Benomyl, may serve a dual function. Cultural and land use practices
may also play important roles, especially on a short-term basis.
Little research on the effects of oxidants on nonvascular green plants
and microorganisms has been reported. Lichens and mosses are responsive
to acid gases, but there is no definite evidence that they respond 1o oxidants.
Ferns may be especially sensitive, but their injury response is much different
from that of higher plants. Growth and sporulation of fungi on surfaces
are usually, but not always, affected. Ozone does not penetrate the leaf
tissue or the colony and thus does not cause death of colonies. Ozone from
14-23
-------
0. 1 to several milligrams per liter of solution is required to kill many
microorganisms in liquid media. Most work with microorganisms has
been done to study the effectiveness of ozone as a biocide in the storage of
vegetation or treatment of water or sewage supplies.
Plants have been used as biologic indicators of oxidant pollutants
for many years. Attempts have been made to use plants as monitors, but
too many unknown variables are involved. Plants may be capable of
monitoring the total biologic potential for adverse effects, but no research
has been developed along these lines.
Losses based on farm prices are not appropriate at the consumer
level and are likely to be conservative. Because of percentage markups and
fixed wholesale and retail marketing costs, the cost to the consumer from
agricultural losses to oxidant pollutants could be as much as $600 million per
year.
ECOSYSTEMS
The transport of injurious concentrations of ozone and other oxidants
to rural areas downwind from urban centers at nuir-erous locations in the United
States appears to be on the increase. Bluraenthal et_ al. conservative!;.
estimate that the urban plume from the Los Angeles area "could cause ozone
concentrations to exceed the Federal standard of 0.08 ppm at locations as
far as 260 km." Other areas where significant rural concentrations of oxidant
have been observed are. Salt Lake City, Denver, and the lilue Ridge Mountains.
In general, the permanent vegetation const. Ltutlng natural ecosystems
receives nuch greater chronic exposure, end the short-lived higher-value
vegetation constituting the agroe.cosypt^i o! uhc LOR Angules coastal plaLn
14-24
-------
can be subject to injurious doses, but in intermittent short-term fumigations.
Each situation has measurable economac and aesthetic effects, but on
different time-scales. The simple agroecosystem has little resilience to
pollutant stress; losses are immediate and sometimes catastrophic. The
complex natural ecosystem is initially more resistant to pollutant stress,
but the longer chronic exposures cause disruption of both structure and
function in the system that may be irreversible.
Simulation models of ecosystem subsystems are developing rapidly.
They deal with flows of energy, biomass, mineral nutrients, water, numbers
of species, population densities, and area occupied per biotic unit. Inter-
actions between ecosystem components must be understood before prediction can
be attempted. Simulation models offer a bright opportunity for determining
the long-term effects on natural ecosystems and agroecosystens. New knowledge
of biologic effects should suggest the importance of preveiition and some means
for ameliorating damage.
Oxidant injury to the mixed-conifer stands of the San Bernardino,
Mountains beginning in the early 1940's is well advanced. A similar problem
is developing in the forests of the southern Sierra Nevada. Both places
show both direct and indirect effects on all subsystems of the forest eco-
system — producers, consumers, and decomposers. For example:
e Ozone injury limits biomass production by the primary
producers and their capacity to reproduce.
• The decrease of biomass or energy flow to consumer and
decomposer in the ecosystem affects the populations of
these organisms.
14-25
-------
0 Essential recycling processes, such as recycling of
nutrients, may be interrupted, further limiting primary
production.
• Stand structure is altered rapidly in some areas by salvage
logging of high-risk trees; as a result, species composition
is changing, and wildlife habitat is being altered.
Oxidant injury to eastern white pine in some forest stands in
the eastern United States is a significant problem. There is an important
concern about injury caused by a synergistic reaction between ozone and
sulfur dioxide at low concentrations.
The relationship between man's welfare and stable natural ecosystems
and agroecosystems can be established in terms of the economic and aesthetic
values derived from them. In some situations, where ecosystems are stressed
by oxidant pollutants, the benefits realized by present and future generations
may soon diminish. Considerable research is required to find alternatives that
prevent stress or that n.ay salvage :,o;nc of these benefits. New management
strategies should be instituted only when their consequences are predictable
within reasonable limits.
EFFECTS Of PHOTOCHEMICAL OXIDANTS ON MATERIALS
In the context of this review, the term "photochemical oxidants" is
considered to be synonymous with "ozone." In test chambers that have
external ozone generators and that operate at or near atmospheric pressure,
ozone is the only likely oxidizing species. In ambient air, however,
ground-state atomic oxygen, hydroxyl radicals, and especially hydroperoxy
14-26
-------
radicals can compete with ozone in attacking materials, such as rubber,
that contain olefinic bonds. The most economically important materials
with respect to ozone damage arc paint, elastomers (rubber), and textile
fiber-dye systems. Damage to polyethylene by ozone is considered to be
negligible. The ozone-specific damage in 1970 to materials has been assessed
in economic terms and is approximately as follows: paint, $540 million;
eL '
-------
CHAPTER 15.
RECOMMENDATIONS FOR FUTURE RESEARCH
The recommendations for research that appear below is a
collage taken from the individual chapters.
CHEMICAL ORIGIN
• Rate constants are needed for almost all the reactions of H02
and R02-
• The homogeneous and heterogeneous reactions of the oxides of
nitrogen with water vapor need study.
• The yields of free radicals from -the photolysis of nitrous acid
and of aldehydes should be established.
of Chapter 2,
e Equation 4/ [0-j] = k-jNC^]/k3[NO], should be tested in the real
atmosphere, as well as in laboratory experiments. Simultaneous
measurements of the concentrations of ozone, nitric oxide, and
nitrogen dioxide and of the intensity of sunlight for a variety of
conditions will provide a much-needed check on this dynamic
equilibrium.
• A quantitative measure of the concentration of free radicals in
smog (probably OH or HO ) under well-defined conditions will provide
an important test of present chemical models.
• Strong support for fundamental gas-phase kinetics is needed. Most
of the reaction mechanisms and rate constants that are needed to
construct realistic and detailed models of the polluted atmosphere
are determined in laboratory studies under very special conditions,
not in smog simulations at a pressure of 1 atm. Because there are
still very serious gaps in the present models, further research
should be supported.
15-1
-------
• Smog-chamber studies are needed for validating both the detailed
chemical models and the lumped models. Many of the past chamber
studies have not used sufficiently well-defined initial conditions.
Measurements of more products and of the reactive intermediates
will provide more stringent tests for models.
• Modeling studies are very useful in pointing out the important
kinetic data that are lacking, in clarifying some of the past
smog-chamber studies, and generally in making the very complex
chemistry more comprehensible. Accurate models can make unique
predictions about the polluted atmosphere. There are very useful
interactions between the modeling studies, the smog-chamber
experiments, and fundamental chemical kinetics; it is not
possible to ignore one without hurting progress in the others.
• It seems probable that many new and unstable compounds are
present in the polluted atmosphere or in smog chambers. A care-
ful search for some of these compounds may provide some surprises.
• Promising new instrumental techniques should be supported, both
for monitoring pollutants and for following reactive intermediates
in kinetic studies. A reliable and accurate method of standardizing
concentrations in the parts-per-billion range is needed.
• The possibility that free radicals, particularly H0~, have signifi-
cant effects on biologic surfaces exposed to the irradiated atmosphere
should be investigated. Sticking coefficients are needed. In
experiments in which the observed biologic effects cannot be attributed
to the measured ozone and PAN concentrations, the possibility of
damage by the steady-state concentrations of free radicals in the
atmosphere should be considered.
15-2
-------
AEROSOLS
Our present knowledge of the chemical and physical processes that
govern aerosol formation in the atmosphere is rather limited, and further
studies are needed in most of the relevant areas of research. This may
leave the reader—and the decision-maker—with a feeling of endlessness.
However, substantial improvements could be made in a reasonable period
by focusing research efforts in the subjects most directly involved:
• Laboratory (smog-chamber) studies of aerosol formation from
aromatic hydrocarbons; gas-phase reaction mechanism, physical processes
controlling gas-to-aerosol conversion, kinetic data on aerosol formation
and aerosol growth, identification of the aerosol products, and effect
of hydrocarbon concentration on aerosol formation (threshold).
• Careful search, in the atmosphere, for aerosol precursors, such
as cyclic olefins and C alkenes.
6+
• Study of the possible health effects of exposure to difunctional
oxygenated organics (such as dicarboxylic acids) that are present in urban
aerosols.
• Identification of organic components of ambient aerosols, to
permit estimation of the relative importance of olefinic and aromatic
hydrocarbons as aerosol precursors.
• Estimation of the relative contributions of photochemical and
nonphotochemical pathways to the formation of inorganic nitrate and
sulfate aerosols.
Identification of organic components of ambient aerosols and esti-
mation of the contributions of various pathways are of immediate interest
for control strategies and could be achieved by using the existing
monitoring networks so as to provide more information on aerosol chemical
15-3
-------
composition. In view of the adverse effects (e.g., on health and visi-
bility) associated with submicroraeter aerosols, an air quality standard
for submicrometer particles might be more adequate than the present
standard for tot;al suspended particles.
ATMOSPHERIC CONCENTRATIONS OF PHOTOCHEMICAL OXIDANTS
• Nonmethane hydrocarbons and both oxides of nitrogen should
be monitored concurrently whenever photochemical oxidant or ozone
is monitored.
• Photochemical oxidant monitoring stations should be sited
upwind and downwind from urban areas, as well as within those urban
areas, wherever possible.
• A common primary calibration standard should be established
for all monitoring networks.
• Documentation should be provided in each case to outline
the rationale for location and design of monitoring stations and
the rationale for data validation for photochemical oxidants.
• A clear indication of what constitutes background
concentrations of photochemical oxidants and ozone must be made,
in order to form the basis of emission control programs.
• The results of monitoring data must be generalized, in
order to relate air quality to emission in a stochastic fashion.
15-4
-------
MODELS FOR PREDICTING AIR QUALITY
Internal improvements in deterministic methods will be based on accounting
for more physicochemical effects in the logical structure. One challenge to
the researcher is to do this without making something that is already complex
still more difficult to understand, and another challenge is to avoid needless
elaboration of detail. Both pitfalls will be avoided, first, by asking how
accurate a modeling job is demanded and, second, by carrying out order-of-
magnitude analytic appraisals of the omitted phenomenology.
Perhaps the most important thing that research will contribute is-a set
of criteria delineating the fidelity of existing models, rather than a single
supermodel that will consider all effects. Much remains to be done in statis-
tical modeling. The scientific community is on the threshold of potentially
great strides with these methods, because of the veritable explosion of data
from measurement programs. It is absolutely essential for all agencies
interested in environmental management to begin mounting analysis programs that
are carefully designed to capitalize on the data base. Traditionally, support
has been more readily obtained for making additional measurements in hope
that useful information would emerge directly or that someone would sponta-
neously dig out the useful information. Seldom has either been the case.
Specific research subjects have emerged with respect to improved des-
criptions of specific phenomena. Some time ago, it was speculated that gas-
solid interactions and turbulence effects on reaction kinetics would be
Important areas of advance in the modeling art. Gas-solid interactions include
both chemical formation of aerosols and reactions on surfaces of preexisting
suspended particulate matter. Because of differing effects of a material in
the gas phase and in some condensed phase, it will be important to characterize
transformation processes. The ACHEX (Aerosol Characterization Experiment)
15-5
-------
program recently carried out under the direction of Hidy will provide an
extensive data base with which to test new ways of treating the gas-solid
interaction problem.
The turbulent mixing of emitted reactant gas (such as nitric oxide) with
atmospherically formed reactant gas (such as ozone) results in macroscopic
heterogeneities, which under some circumstances can significantly change the
reaction rate from the value that the mean concentrations used in a rate
equation would predict. Airborne measurement from some 40 operational days
from the LARPP (Los Angeles R.eactive Pollutant Program) study gives 6-s-interval
gas-phase data for six gas-phase species simultaneously. This program (under
the field management of W. Perkins and under the direction of Coordinating
Research Council's CAPA-12 committee, chaired by J. Black) has produced archives
of these data that can serve as a test bed for theories of turbulent inter-
actions with kinetics.
In a broader sense, the data obtained from the Regional Air Pollution
Study (RAPS) and the California Three-Dimensional Pollutant Gradient Study
Program should also serve as bases of further model development. It is
incumbent on the agencies responsible for air quality control to identify
resources specifically aimed at using these data for improving techniques for
designing pollution abatement strategies.
Suggested Applications to Pollution Abatement. Without doubt, the top-priority
application of air quality models is the determination of emission controls needed
to achieve ambient air quality standards. With the reexamination of transportation
beyond
control strategies and with the pressures of fuel substitutions, refinements well /
15-6
-------
traditional proportional models are imperative. Where validated diffusion
models are available, they should be used to recalculate the emission require-
ments that came from initial hasty efforts to implement the Clean Air Act
Amendments of 1970. This is the greatest national service that could be
performed by the air quality modelers at present. Before this can be achieved,
however, the institutional apparatus must provide the impetus and resources
called for in a recent National Academy of Sciences report to the U.S. Senate.
Much of the research work will add content to the model structures, but
future applications demand simplifications that are oriented toward the non-
specialist user. One of the largest obstacles to the effective use of air
quality prediction schemes is the resolution of this apparent conflict. At
least two steps can be taken by those who produce models to encourage appli-
cations and to aid the user:
• Compile a catalog of air quality models that describes their capa-
bilities in terms of a common set of performance standards.
• Clarify data communication in the input-output interfaces between
user and model.
To accomplish the first step, model standards will be evolved on the
basis of legislative mandates and regulatory needs. Each of the various
types of model has undergone performance evaluation through the application
of a set of tests peculiar to its own structure or output. For example,
Gaussian models that predict long-term averages are often evaluated by
computing only the correlation coefficient between measured and computed con-
centrations. Early evaluations of species-mass-balance models stressed hour-
by-hour comparison of the predicted and observed concentrations. Recently,
a broader range of descriptors has evolved, as evidenced by the work of
Nappo and Whitney.
15-7
-------
The performance indexes must be designed with the model applications in
mind. Will the model be used to predict local effects around a highway or a
smelter where short-term high doses are as important as long-term averages?
Will the model be called on to compare trends in air quality between two
different scenarios of urban population growth? Will the model be used to
select a control plan that will result in a given hourly air concentration's
being exceeded only once a year? A properly designed set of performance
standards will allow a potential user to compare models with respect to
suitability for any specific application. The particular performance char-
acteristic of interest influences strongly the rank-ordering of models on a
scale of goodness.
•
Fundamental to the definition of an optimal set of performance measures
will be the relationship of risk (of health, property, or aesthetic attributes)
to exposure (average pollutant concentration, time-integrated pollutant con-
centration, synergistic combination of pollutant dosages, or dosages integrated
with respect to space, time, and population ). Derived from the risk factor
will be, not a single number, but a distribution of effects for each degree of
exposure.For example, a range of pulmonary effects can be expected in a sample
population in which each individual has been exposed to ozone at an average
concentration of 100 ug/m3 for 5 years. The expectation value of the effect
will be the risk factor that is the function of exposure described above.
The model performance index will utilize these relationships to connect a
probability density distribution output from the model (associated with imperfect
knowledge) to a probability density distribution of the threat to public health
and welfare. Stated in a different way, each model will be assessed on the
basis of the uncertainty of damage estimate that arises from it imperfections.
This must be done in an unambiguous way for the user, who may not be a specialist.
15-8
-------
The second step that will be needed to ensure ready application of air
quality models is largely a question of packaging and presentation. User-
oriented documentation will be needed for personnel at data processing centers,
who may not be specialists in chemistry, mathematics, or meteorology. Expe-
rience has shown that the user desires to operate the model in his own data
center and wishes to understand enough about the model structure .:o explain it
to others in his field. Models that cannot be adapted to these requirements
have not been widely applied. In somo cases, an operating manual intended for
persons with some knowledge of programing will need to be rewritten to allow
the user to supply completed data foiins to a computer center and routinely
receive output in return. Other adaptations may require a user to punch data
in on a teletypewriter and receive output on the same machine in an interactive
mode. This involves a network of remote terminals served by the computer
center, such as that under development in UNAMAP.
Output displays will be required to bring the abstract aspects of
voluminous output data into some form chat appeals to the experience of the
user. Isopleth maps are useful, as ar throe-dimensional isometric plots
like SYMVU, produced by Harvard University. Printer plots of concantration
maps will undoubtedly enjoy an even greater application, because of the common
availability of line printers or teletypewriters as output devices. Examples
of these techniques are SYMAP and GRID, both produced by Harvard University.
Another aspect of matching output to user needs involves presentation of
results in a statistical framework—namely, as frequency distributions of con-
centrations. The output of deterministic models is not directly suited to this
task, because it provides a single sample "point" for each run. Analytic
linkages can be made between observed frequency distributions and computed
15-y
-------
model results. The model output for a particular set of meteorologic conditions
can be on the frequency distribution of each station for which observations are
available in sufficient sample size. If the model is validated for several
different points on the frequency distribution based on today's estimated
emission, it can be used to fit a distribution for cases of forecast
emission. The fit can be made by relating characteristics of the distribution
with a specific set of model predictions. For example, the distribution could
be assumed to be log-normal, with a mean and standard deviation each determined
by its own function of output concentrations computed for a standardized set
of meteorologic conditions. This, in turn, can be linked to some effect on
people or property that is defined in terms of the predicted concentration
Statistics. The diagram below illustrates this process:
Concentration field
predictions
Statistical Predicted Injury or Expected
module frequency distributions damage te harm to heal tl
'
. ,
Historical air^ - nodule am}
quality data
We have seen the wide variety of methods now available to calculate air
quality. The priority for adapting these methods to current needs is clearly
established. Only through clear expositions of model performance and simple
implementation procedures will the present techniques have a favorable impact
on air quality management. A growing appreciation by the specialist community
of the policy requirements will be essential for the successful fulfillment
of these goals.
15-10
-------
MEASUREMENT METHODS
Instruments based on differential ultraviolet absorption still
need to be evaluated, and possibly modified, prior to their acceptance
for monitoring ozone in polluted atmospheres on a nationwide scale.
The California Air Resources Board and other air pollution control
agencies are currently conducting multi-year programs for evaluating
ultraviolet absorption side-by-side with chemiluminescent and potassium
iodide based instruments, to determine their applicability and
needed modification, as well as to assure continuity in the data base
while the older monitoring instruments are being replaced.
Thus despite the remarkable progress in the monitoring for ozone,
nitrogen oxides and non-methane hydrocarbons, which has strengthened the
implementation and evaluation of control programs, substantial research
and development is still required to help resolve the uncertainties in our
knowledge which are inhibiting the actual achievement of desired air quality
standards.
The areas in which further research and development are needed,
in sequence of priority are:
• Evaluation of primary calibration nrocedures applicable
nationwide for ozone measurement.
• Development principles and instruments which can easily track
the sources of those hydrocarbons reactive in the production of ozone and
those which are reactive in the production of particles.
• Chemical identification of both gas and particle phase compounds
occurring in the atmosphere, which cause eye irritation and respiratory
difficulties.
15-11
-------
• Methods for the direct and continual measurement of those
chemicals in the particles of the atmospheric haze, that are known to be
formed during photochemical pollution episodes and are already suspect
as respiratory irritants. By implementing such measurements it will be
possible to find out to what extent the occurrence of such substances can be
reduced by various emission controls. To assess actual population
exposures, it is also necessary that these measurement methods be
easily carried out indoors and in vehicles.
• Improved measurement methods suitable for observations from
airborne platforms so that the regional scale impacts of urban emissions
can be accurately assessed. This is needed because some control options
for solving the urban-scale problem have the potential of transferring
pollution from one geographic area to other geographic areas.
RESPIRATORY TRANSPORT AND ABSORPTION
The development of models requires more knowledge about the chemical,
physical, morphologic, and flow properties of the mucous layer; the
kinetics of the reactions of ozone in the mucous arid tissue layers; and
the molecular diffusivity of ozone in these layers. Similar information
is needed for the hydroperoxy, HO , and singlet oxygen, 02 (a A), free
radicals, which are reactive intermediates in photochemical smog.
Furthermore, a realistic model hased on such knowledge needs to be
verified by measurements of uptake and tissue dosage in the various
regions of the respiratory tract. These are currently difficult to make,
but are required to establish accuracy and reliability. New methods of
sampling and techniques using tagged gases should be developed, so that
local uptake can be measured.
15-12
-------
An extensive effort d s needed in studies of pollutant-gas transfer,
absorption, and reaction in the respiratory tract. After some of the
experimental questions about behavior of o/.one in the mucous layer and
adjacent tissue arc answered, available methods for calculating the local
dosage to critical airway sites can be used in new uptake models. Gas-
absorption and particle-deposition models for the upper respiratory
tract (nose, mouth, pharynx, larynx) also need to be improved. Experimen-
tal data now available can be used to develop seniempirical relations for
gas uptake in the nose in a procedure analogous to that used to model
particle deposition. Development of a more refined model for nonreactive
gases requires data on gas diffusivities in the mucus and tissue,
local blood perfusion rates in the nasal epithelium, and physiologic and
pharmacologic factors affecting the mucosa and local blood flow rates.
Models need to be developed for mixtures of gases that may interact
chemically in .the gas phase, in the mucus, or in aerosol droplets to form
other species. This requires theoretical and experimental studies of
dissolution, absorption, adsorption, and desorption of gases in or on
aerosols in the respiratory tract.
Improved modeling is needed for the design and interpretation of
animal experiments and controlled human studies, and for the collation
of diverse data from animal and human exposures to ozone. Calculations
of local dose at reactive tissue sites can help to explain the mechanisms
of tpxicity and are needed to extrapolate animal and human data for
assessing population rislcs under different environmental conditions.
15-13
-------
TOXICOLOGY
Enhanced susceptibility to respiratory exposure to infectious agents
is of considerable potential poblic health significance. This has been
reported to occur in mice exposed to ozone at as low as 0.08 ppm, the
lowest reported "effect" concentration in laboratory animal studies.
It seems essential, therefore, to continue and expand research on the
effect of ozone and other photochemical oxidants on physiologic protective
mechanisms of the lung. Appropriate dose-response studies should be
included to confirm or establish the exposure concentration-time rela-
tionships that result in increased suscepti-bility to inhaled microorganisms,
and studies of the cellular responses and mechanisms should be conducted
with a view to providing methods that are applicable to epidemiologic
studies in oxidant-exposed human populations.
Research designed to elucidate the pathophysiologic implications of
reversible changes in lung function, histology, and biochemistry that
have been observed at concentrations of 0.2-0.5 ppm would be especially
valuable in evaluating the significance of these changes for health. In
particular, it would be useful to determine what, if any, causal or
correlative relationships exist between different effects detected by
various experimental assay systems and between reversible changes and
more chronic effects, such as reduced lung elasticity, fibrosis, and
adenora formation. Studies on laboratory animals are particularly
suited, to this type of mechanism-correlative research; but, with appropriate
experimental designs, such research should be very useful in determining
which methods or biologic changes can be usefully applied to clinical or
15-14
-------
epidcmiologic studies. At the came tJJne, .such research could determine
whether seme of the changes (e.g., increased activity of enzynias involved
in cell redox systems) are indicative of injury or are honeostatic
adaptive responses. This information will have value in predicting
potential injury in the "average" population and possibly help to identify
people who are hypersusceptible by virtue of sane deficiency in adaptive
protective mechanisms. Related to these research efforts, further
investigation of the influence of oxidant exposure on enzymes that bio-
transform other inhaled chemicals (e.g., aromatic hydrocarbons) and the
interaction effect of dietary antioxidants (e.g., vitarruji E) should be
pursued, particularly in relation to oxidant-induced oxidation of membrane
lipids and free-radical formation.
There are several scattered reports of extrapalmonary effects of
ozone exposure .in laboratory animals. Some (e.g.r chrorrasomal aber-
rations in hamster lymphocytes) occur at or near concentrations that
cause local effects in the lung and portend serious and long-term health
implications. Others(e.g., reduction of voluntary activity) may be
transient or reversible, but nevertheless contribute to decrements in
performance or well-being. It is particularly important that further
research be conducted to confirm (or refute) these reported extrapalmonary
actions of ozone and the exposure concentrations at which they occur.
If confirmation of their occurrence is obtained at or below the currently
reported effective exposure concentrations, useful research efforts could
be directed toward determining whether they are direct or secondary
effects and toward identifying the chemical species responsible. Fore
15-15
-------
importantly, confirmation of an isolated effect on cell genetic material
would demand a thorough expert evaluation of its significance on the
basis of existing knowledge of the long-term implication of the effect
and, accordingly, intensified laboratory and epidemiologic 10search.
CONTROLLED STUDIES ON HUMANS
Further studies are needed to give better dose-response information
and to provide a frequency distribution of the population response to oxidants
alone and in combination with other pollutants at various concentrations.
Such studies should include the effects of mixed pollutants over ranges
corresponding to the ambient atmosphere. With combinations of ozone and
sulfur dioxide, the mixture should be carefully characterized to be sure
of the effects of trace pollutants on sulfate aerosol formation. The design
of such studies should consider the need to use the information for cost-
benefit analysis and for extrapolation from animals to humans and from small
groups of humans to populations. Recent research has indicated the possibility
of human adaptation to chronic exposure to oxidants. Further study is
desirable.
Studies are needed to clarify the importance of age, so:, ethnicity,
familial elements, nutritional factors, and pharmacologic agents in detenr.inir.:
response to oxidants. Because people with Jung disease are thought to be r.or-i
susceptible to oxidant pollutants, exposure studies are needed to quantify tl.i;
Better methods for measuring or estimating the actual dose of oxidants absorbe.:
by each subject are needed. The usual time variation in measures of human
response should be evaluated p_cr_ _s_e, because this information is needed to
optimize experimental design.
15-16
-------
More informal: ion is needed before rational guidance can be given
limiting exercise during periods oi high oxidant pollution.
J^ J r ' r) 'i. t °,_c«p rr o I l_e d at-.in
as
Academy of Sciences_,_J^j^erJ£j^n^K^^c^__Aj ; socin Urn i ,_Jind__the J^TJ. i or i al
Ins t.ij:uj:_es__of_ JI oa It h .
EPIDEMIOLOGIC STUDIES
Modification of the method in which the CHESS studies are
designed and in which the data are displayed would add considerably
to their value. The scientific data collected in all the CHESS studies
should be made available through accepted scientific publications
to the scientific community as a whole.
The continuation of epidemiologic studies, including those of
the CHESS program, is vital to our understanding of the effects of air
pollution on health. There is no other way to determine the needed
dose-response (exposure-response) relationships between the complex
urban atmospheres and specific health effects. No animal or clinical
experiment can duplicate the full range of variables to be found in
ambient urban air. For this reason, all necessary support should
be given to qualified scientists to conduct epidemiologic studies
designed to answer these questions. Although such studies are
expensive and time-consuming, the data they produce can be produced
in no other way and are essential in the development of useful air
quality standards.
It is important to know whether such phenomena as tolerance
and cross-protection, well demonstrated or suggested in animals,
occur in man. Analogues for all these phenomena should be sought
in human populations, and methods should be devised for assessing
their significance for human health.
15-17
-------
PLANT AND MICROORGANISMS
These recommendations are not listed in a priority order, but
many could be followed in parallel or simultaneously. In general, the recom-
mendations presented by Heck jet al. are still germane to research
needs in the subject of oxidant pollutants.
A few definitive experimental designs are needed to further our
knowledge of acute dose-response information on ozone. Much of this type
of information is still needed for PAN and its analogues. All experimental
designs should incorporate dose response.
Studies to develop dose-response curves for chronic exposures of
crop and native species over growing seasons and under field conditions
are needed for ozone, PAN, and other oxidants.
Research should be continued with filtered and nonfiltered field
chambers to study effects of ambient oxidants on important agronomic,
horticultural, and native species. We know that there is a problem, but
its significance and magnitude are matters of conjecture.
There is a critical need to understand the interaction of multiple pol-
lutants on individual plant species and ecosystems. Multiple-pollutant effects
are generally important, but little is known of their effects on most plants.
Variable concentrations, ratios of pollutants, and age of plants all affect
response.
Models should be developed to understand the relative importance of
other variables as they affect plant dose response. These include, but are
15-18
-------
not limited to, climatic, edaphic, biotic, and genetic factors. Considerable
information is available, but there are many gaps, and no comprehensive
programs are in progress to determine how these factors act and interact
to affect a plant's response.
The mechanism of response and the biochemical systems affected
are not understood. Although plant membranes are considered the primary
sites of action for the oxidant pollutants, there is no definitive work on
this. An understanding of these responses would be supportive of breeding
and spray protective programs.
Both breeding and spray protective programs need to be
developed, so that better-yielding and better-quality cultivars will be pro-
tected against oxidant pollutants.
Some effort is needed to explore the feasibility of using plants to
monitor the overall biologic activity (or biomass reductions) caused by
photochemical oxidants in specific air basins or regions. The response
of sensitive plants should be correlated with the response of plants of
economic and aesthetic importance.
Additional monitoring of multiple pollutants is needed in rural areas.
Whenever possible, measures that vary on a continuous scale (e.g.,
biomass) should be used with subjective estimates of injury (e. g. , indexes
of visible injury).
ECOSYSTEMS
The present knowledge of the biologic consequences of chronic
oxidant injury to both natural ecosystems and agroecosystc-ms must be. commuai-
cated to groups in the public sector that work in planning and enforcement.
The indirect effects on man's health and the direct effects on his welfare
resulting from ecosystem deterioration due to oxidant in-jury are serious
15-19
-------
enough to be given more (.borough consideration in all decisions related to
abatement of air pollution from both mobile and stationary sources. Land-use
planning and proper airshed classification should be used to prevent further
deterioration of air quality, particularly in prime timber-producing areas
and in remote, pristine areas, regardless of their present use designation.
The most important research needs are related to the determination
of the responses of natural ecosystems and agroecosysterns to chronic exposure
to oxidant pollutants. In particular, rhronic-dose-response models are needed
to understand the responses of the dominant primary-producer species constituting
forest ecosystems in both the eastern and the western United States. The result-
ing alteration of interactions with other subsystems—e.g., consumers and
decomposers—must also be investigated.
EFFECTS OF PHOTOCHEMICAL OXIDANTS ON MATERIALS
o Laboratory studies of effects of photochemical oy.idants other than
ozone—e.g., PAN, peroxybenzoylnitratc, atomic oxygen, cxc.ited
1
molecular oxygen, 0 ( A ), and hydroperoxy and hydroxy] radicals—
2 g
on specific materials should be conducted;
» Methods to measure concentrations of transient oxidants such as OH, HO ,
0~ ( 0 ) in real atmospheres should be developed.
» Mechanisms of attack of oxidants on materials should be investigated,
so that distinctions can be made between effects on a given material
due to various pollutants.
• An integrated study should be conducted in which relative effects
of all major air pollutants on materials are assessed.
15-20
------- |