ATION
U. S. DEPARTMENT OF HEALTH, EDUCATION, AND WELFARE
Public Health Service
Environmental Health Service
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AIR POLLUTION
INJURY TO VEGETATION
Ibrahim Joseph Hindawi
U. S. DEPARTMENT OF HEALTH, EDUCATION, AND WELFARE
Public Health Service
Environmental Health Service
National Air Pollution Control Administration
Raleigh, North Carolina
1970
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The AP series ot reports is issued by the National Air
Pollution Control Administration to report the results of
scientific and engineering studies, and information of general
interest in the field of air pollution. Information reported in
this series includes coverage of NAPCA intramural activities
and of cooperative studies conducted in conjunction with
state and local agencies, research institutes, and industrial
organizations. Copies of AP reports may be obtained upon
request, as supplies permit, from the Office of Technical
Information and Publications, National Air Pollution Control
Administration, U.S. Department of Health, Education, and
Welfare, 1033 Wade Avenue, Raleigh, North Carolina 27605.
The author wishes to thank the following contributors
who furnished additional color photographs contained in this
publication:
Dr. Howard Heggestad, U.S. Department of Agriculture
(Figure 13); Dr. Ruth Glater, University of California (Figure
24); Misses Ida Leone and E. Brennan, Rutgers University
(Figures 30 and 41); Dr. D. F. Adams, Washington State
University (Figures 35 and 38); Dr. M. D. Thomas, American
Smelting and Refining Co. (Figure 23); Dr. Clyde Hill, Uni-
versity of Utah (Figure 36); Dr. J. S. Jacobson, Boyce-
Thompson Institute (Figure 39); The American Society of
Agronomy and the National Fertilizer Association (Figure
49).
; v- :
••
National Air Pollution Control Administration Publication No. AP-71
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r /
'••_ U
INTRODUCTION 1
STRUCTURE AND ACTIVITIES OF PLANTS 3
PHOTOCHEMICAL REACTION OF HYDROCARBONS AND NITROGEN OXIDES
PRODUCES OZONE AND PAN 10
NITROGEN DIOXIDE CAUSES DIRECT VEGETATION DAMAGE 18
SULFUR DIOXIDE CAUSES ACUTE AND CHRONIC INJURY 20
SYNERGISTIC EFFECT OF OZONE AND SULFUR DIOXIDE CAN CAUSE MORE
SEVERE INJURY THAN EITHER POLLUTANT ALONE 25
PLANT DAMAGE APPEARS FROM LOW CONCENTRATION OF FLUORIDES 26
CHLORINE DAMAGE OCCURS CLOSE TO SOURCE 30
ETHYLENE INJURES VEGETATION IN URBAN AREAS 32
AIR POLLUTION RETARDS GROWTH OF VEGETATION 34
VEGETATION INJURY FROM OTHER AGENTS CAN BE CONFUSED WITH AIR
POLLUTION INJURY 36
AIR POLLUTION INJURY TO VEGETATION INDICATES DEGRADATION OF
ENVIRONMENT 38
REFERENCES.
40
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©TO
A
ir pollution fouls the air in every community of more than
50,000 population in the United States as well as in a major propor-
tion of smaller towns.1 A number of natural variables play an impor-
tant role in the formation, duration, and location of air pollution.
Because of variation in wind direction and speed, air pollution re-
spects no arbitrary boundaries. Pollutants may travel freely from
their sources, cross city and state lines, and contaminate other com-
munities many miles away. Meteorological and topographical condi-
tions that cause stagnant air masses may cause a buildup of pollution
at certain times and places.
In Los Angeles, pollution from automobile exhaust is the major
problem. In London, it is the smoke and gases from high-sulfur-con-
tent coal. In New York and New Jersey, air pollution has been traced
to petroleum refineries, automobile exhaust, power-generating facili-
ties, waste disposal systems, and many other sources. In some cases
the problem arises from a series of chemical reactions in the atmos-
phere involving by-products of combustion and other processes. A
chemical reaction takes place, for instance, between hydrocarbons
and nitrogen oxides, with sunlight acting as an energy source, to
produce photochemical smog. Pollutants from these various sources
injure crops, trees, and property and reduce the amount of sunlight
reaching the earth's surface.
Since a threat to human health is implicit in air pollution, and
since agricultural and other economic losses can be attributed to
pollution, means must be found to detect and control atmospheric
pollutants. The study of the effects of pollutants on vegetation is
important not only because of the obvious relationship of such ef-
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fects to agricultural production, but also because many plants can
serve as indicators of the presence of pollutants. The usefulness of
plants as indicators is based primarily on the sensitivity to pollutants
of selected species or varieties.
For the past 20 years, scientists have been growing plants under
controlled conditions and exposing them to various concentrations
and combinations of certain chemicals. In this way they have been
able to determine the relative effects of these chemicals on plant life.
By now, characteristic injuries to certain plants can be interpreted
not only to determine the presence but even the relative concentra-
tions of aerial pollutants that cause injury. In some instances when
analytical techniques and measuring instruments are inadequate,
plant injury alone may be used to determine the presence of pollu-
tants.
One variety of tobacco is used by many investigators as an effec-
tive ozone indicator. Pinto bean plants are used to detect peroxy-
acetyl nitrate (PAN); petunias, to investigate total oxidants; and glad-
ioli, to determine fluoride accumulations. Dahlias, petunias, alfalfa,
and cotton are excellent detectors of sulfur dioxide injury.
Actual leaf injury and its relationship to crop, losses have been
measured quantitatively. In fact, alfalfa and grain crop losses have
been shown to be directly proportional to visible damage caused by
sulfur dioxide.2 Field vegetation surveys and plant damage reports
have been used to estimate the presence, distribution, and general
levels of pollution.3
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^ir pollutants are divided into two major types, gases and particu-
lates. Gaseous pollutants account for the most widespread injury to
plant life. Gases known to damage vegetation include: ozone, PAN,
nitrogen dioxide, sulfur dioxide, hydrogen fluoride, ethylene, and
chlorine. These pollutants destroy plant chlorophyll, disrupt the pho-
tosynthesis process, and consequently reduce food production. In
severely polluted areas, adjacent to certain industrial operations,
plant life has been almost entirely exterminated.
An interaction of even low concentrations of these gases can cause
injury that is not readily apparent. This injury may show up as
growth suppression, dwarfing, or early maturation or as symptoms
similar to those of nitrogen deficiency or virus infection.
The leaf is the primary indicator of the injurious effects of air
pollution. Its structure plays an important role in building carbo-
hydrates and other vital plant products and foods. Some of the basic
anatomy, morphology, and physiology of the leaf are discussed on
the following pages to facilitate understanding of leaf activity in
relation to air pollution symptoms and injuries.
Plants and animals alike are composed of tiny cells, which may be
compared to the bricks or stones that make up the walls of a house.
Cell sizes range from 0.01 to 0.1 millimeter in diameter. A typical
plant cell (Figure 1) has three main components: the cell wall; the
protoplast, which is the protoplasm of one cell; and the inclusions,
which are composed of nonliving structures.
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Protoplast
Inclusions
Cell Nucleus
Chloroplasts
Cell Wall
Figure 1. All or part of a cell may be injured by air pollutants.
Cell walls are extremely thin when they are first formed, but they
become relatively thick with age. The cell wall, produced by the
protoplast that it encloses, is made up almost entirely of cellulose.
Protoplasm
Protoplasm, usually colorless, is a jelly-like substance that is found
in all living plant and animal matter. It is considered living matter in
its simplest form.
Protoplasm is composed of several chemical compounds. The most
important is protein; others are fat and carbohydrate. The water
content of the protoplasm ranges from 60 to 90 percent. The dense
bit of protoplasm found in the center of the cell is the nucleus, and
the protoplasm located outside the nucleus is the cytoplasm. Within
the cytoplasm are three types of tiny bodies, or plastids, that per-
form vital functions in the life of a plant: chloroplasts, leucoplasts,
and chromoplasts.
All green plant cells contain chloroplasts, oval microscopic bodies
that contain the green pigment chlorophyll plus some yellow pig-
ment. Chloroplasts are of enormous biological importance because
they are key structures in the plant's food manufacturing process,
photosynthesis.
Leucoplasts are colorless plastids that convert starch into starch
grains. As these grains increase in size and number, the leucoplasts
stretch to many times their normal size.
Chromoplasts are responsible for the red, yellow, or orange colors
appearing in many flowers and fruits.
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Inclusions
Inclusions are the nonliving structures of cells. They are seldom
found in very young cells, but appear in increasing numbers as cells
mature. They are particularly evident in old cells with large food-
storage capacity. Inclusions may be crystals, noncrystals, or sacs con-
taining liquid mixtures. These sacs, called vacuoles, contain mixtures
of water and substances such as nitrogen oxides, carbon dioxide,
inorganic salts, soluble protein, and simple nitrogen compounds.
Vascular Bundle-
ANATOMY OF THE LEAF
Plant structure is formed by the leaf, stem, and root. The leaf
(Figure 2) is the principal organ involved in photosynthesis. Micro-
scopic examination of a typical mature leaf reveals three primary
tissue systems: the outer epidermis, the mesophyll.and the vascular
bundle (veins).
Air Spaces
Upper Epidermal Cells
11 •* Palisade
j . Parenchyma
Spongy
Parenchyma
Mesophyll Cells
jf Lower Epidermal Cells
Guard Cells (enlarged)
Figure 2. Cross section of intact leaf shows air spaces within leaf that serve as passages lor pollutants that may subsequently
injure leaf.
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The epidermis covers the entire surface and protects the tissue
within from injury caused by such things as excessive water loss and
wind and rain. Epidermal cells are relatively long-lived, dying just
before the leaf falls. Chloroplasts are usually absent from epidermal
cells. Oval openings in the leaf epidermis are called stomata. Bounded
by two special cells called guard cells (Figures 3 and 4), stomata are
found among ordinary epidermal cells on the lower side of a leaf and
occasionally on the upper epidermis. These openings regulate the
entrance and exit of gases. The function of the guard cells in opening
and closing stomata depends upon change in the turgor (normal dis-
tention and resiliency) of the cell.
Stem a
Guard Cells
Chloroplasts
Figure 3. Cross section of leal inward from epidermis illustrates stoma through which pollutants enter.
6
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Epidermal Cells
Guard Cells
Figure 4. Enlarged view of leaf surface reveals open stoma.
The mesophyll is the soft tissue between the lower and upper
epidermis of typical leaves and is made up of two principal types of
tissue, the palisade parenchyma and the spongy parenchyma. Palisade
parenchyma consists of one or several layers of elongated cells lo-
cated between the upper epidermis and the spongy cells. Spongy
parenchyma cells are not elongated. They are formed and arranged so
that many large spaces exist between them. The cells of both palisade
and spongy parenchyma contain chloroplasts.
Vascular bundles carry water, minerals, and carbohydrates
throughout the leaf area. The mid-rib is the largest vein.
ACTIVITIES OF THE LEAF
The primary functions within a typical leaf are photosynthesis,
transpiration, and respiration.
Photosynthesis: Basic Food Manufacturing Process
The mesophyll tissue contains a large number of chloroplasts. In
the presence of light, photosynthesis takes place in the chloroplasts.
This involves the union of water and carbon dioxide to form sugar
(glucose) and then starch. Photosynthesis is described by the follow-
ing equation:
6CO, +
6H2O
C6H1206
+ 6O,
The excess oxygen generated in the process escapes from the plant
and into the atmosphere during photosynthesis. Light is the source
of energy for photosynthesis, and part of this energy is stored in the
molecules of glucose.
Transpiration: Coo/ing and Nutritional Processes
A plant suffers constant water loss to the atmosphere through
evaporation. As shown in Figure 5, the water is siphoned from the
soil through the roots and moves through conducting tissue or veins
to the leaves. In the leaves, the moisture escapes in vapor form from
the moist cell walls of the mesophyll into the intercellular spaces. It
is then released through the stomata into the atmosphere. Transpira-
tion causes a continuous stream of water to move from the roots to
the top of the plant. It transports soil minerals through the plant and
also cools the plant. These processes increase during hot sunny
weather and greater-than-normal air movement.
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Figure 5. Flow of moisture in the growing plant provides for transpiration and respiration
processes. Sunlight serves as energy source for photosynthesis.
Plants breathe through leaves.
Bark or hard case protects plant from bruises and insect damage
Trunk, stem, and tendrils reach up into sunlight and air.
Foods manufactured
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Blossom uses food in production of seeds.
Carbon dioxide is absorbed.
Oxygen is released.
Chlorophyll, the green substance in the plant, absorbs energy from
light and water. This energy is used to make starch and sugar.
Branches and leaves are arranged to expose greatest possible area to light.
Fats and proteins are made by chemical changes
in the sugar and starches in various parts of the plant.
in leaves and branches are carried down stem .
Roots anchor the plant, absorb minerals and moisture, and serve as
food reservoir.
Respiration: Energy-Producing Mechanism
Respiration, a continuous process in the protoplasts of all living
cells, involves the reaction of oxygen with carbohydrates to release
energy. In effect, oxygen acts as a fuel to burn carbohydrates and
produce energy. Thus, photosynthesis (see Figure 5) is an energy-
absorbing or storing process and respiration is an energy-releasing
process.
Because they obtain all the energy necessary for food production
and storage directly from the sun, plants form the beginning of the
food chain that sustains all animal life, for animals derive all their
food, and thus all their energy, directly or indirectly from plants.
The immediate end product of photosynthesis in plants is glucose, ,
which, conversely, is the substrate oxidized in respiration. The equa-
tion for respiration, then, is the reverse of that for photosynthesis:
+ 6On
6H,O + 6CO,
While the process of photosynthesis is taking place, plants release
oxygen into the air and help maintain the correct atmospheric bal-
ance. At night, or at other times of photosynthesis inactivity, plant
cells take in oxygen and release carbon dioxide to the atmosphere.
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I he i
I he photochemical reaction of hydrocarbons and nitrogen oxides
produces ozone and PAN. When exposed to sunlight, nitrogen diox-
ide absorbs ultraviolet light, which furnishes the energy to break the
bond between oxygen and nitrogen in the gas molecule. The result is
the formation of nitric oxide and atomic oxygen. This reaction
causes a number of oxidations, with ozone the principal oxidant
produced.
Major sources of hydrocarbons and nitrogen oxides are automobile
engines and industrial plants.
AND ALTERS COLOR
Ozone severely injures many forms of plant life (Figures 6-15).
"Weather flecks" on tobacco leaves have been attributed to ozone.4
These marks appear first on mature leaves of Tobacco Bel W3 and
then progress to the youngest leaves. The first lesions to appear on
tobacco leaves are dark (Figure 7), and remain dark for about 24
hours. Then they become lighter in color (Figure 8) and finally turn
white several days later (Figure 9).
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V- $V
i ^•••l^^^
Figure 7. Tobacco leaves exposed to ambient air in New York City
developed dark lesions attributed to ozone.
Figure 6. Tobacco plant displayed oxidant (ozone} injury at Staten
Island, New York, in 1966. Injury progressed from oldest
to youngest leaves.
Figure 8. Ozone-injured tobacco leaves develop light-colored le-
sions approximately 3 or 4 days alter exposure.
11
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Figure 10. Enlarged surface of pinto bean leaf shows stipple (pig-
mentation) along veins of plant grown outside at Staten
Island, New York.
Figure 9. Lesions on tobacco leaves appear white several days after
exposure to ozone.
'•'igure 11. Microscopic cross section of pinto bean leaf shows se-
vere ozone injury. Palisade cells plasmolyzed and lost
their integrity, but spongy and epidermal cells remained
intact.
12
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Figure 12. Fleck and symptoms of dehydration appeared on old pri-
mary leaf of pinto bean plant exposed to natural pollu-
mary leal
tants.
Figure 13. Injury on tobacco leaf exposed to ozone in laboratory did
not develop on upper part of leaf because it was shaded
during ozone exposure. Severe ozone injury appeared on
unshaded part of leaf. Light caused the stomata to open,
thus a greater amount of ozone entered and injured this
portion.
Ozone causes stipple and bleaching on the upper surface of leaves
of the pinto bean plant (Figure 10). Fleck and stipple caused by
ozone also appear on the upper surface of grapevines. These symp-
toms are similar to those of ozone injury in other species of plants
and were first recognized in 1958.5
Ozone injures the palisade cells of plants (Figure 11). Initially, the
chloroplasts condense and accumulate at the center or at both ends
of the cell. This is followed by collapse of the cell wall. Occasionally,
the chloroplasts granulate and form a jelly-like mass. As the result of
pigment breakdown in the damaged cells, a reddish-brown color is
produced. When exposed to ozone, leaves of woody plants develop
red-brown spots from the formation of new pigment.6 When small
islands of palisade tissues are injured, discrete punctate spots appear.
Studies made at the greenhouse facilities of the National Air Pol-
lution Control Administration in Cincinnati revealed that sensitivity of
Tobacco Bel W3 and pinto bean plants to ozone exposure is influ-
enced by environmental conditions and the time of day of expo-
sure.7 Plants were significantly more sensitive during the mid-portion
of the day. The importance of the time factor is recorded in Tables 1
and 2. Table 3 indicates the effect of light intensity during ozone
exposure tests on pinto bean plants.
Published information concerning tobacco varieties indicates that
test plants grown in California and Utah are not as sensitive to ozone
as are the same plant varieties when grown in the middle and eastern
regions of the United States.4 Studies in California showed that 25
parts per hundred million (pphm) of ozone for 6 hours causes injury
to plants.4 In Utah in 1961, it was found that an average of 24 pphm
of ozone for 2 hours injured tobacco plants.8 In 1959 in New York
City, however, tobacco injury was reported at 10 pphm for 8 hours,9
and in 1962 in Beltsville, Maryland, studies showed that Tobacco Bel
W3 was injured after 4 hours fumigation at an ozone concentration
of only 5 to 7 pphm.10 In 1965 it was found that greenhouse-grown
Tobacco Bel W3 plants were injured after 4 hours' fumigation at 3.5
pphm of ozone,7 a concentration about half of that used at Belts-
ville.
This variation suggests that the plant injury threshold of ozone in
one location may vary from day to day and that a concentration of
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the gas that would not cause injury in a certain location may be
injurious to comparable plants in other locations. Conditions that
may cause the injury threshold to vary include light intensity, tem-
perature, humidity, available nutrition, and season. Examples of
ozone injury to agricultural specimens are shown in Figures 14 and
15.
Figure 14. Symptoms on spinach leaves indicate injury from oxi-
dants, mainly ozone.
Figure 15. Injured leal shows reddish-brown bleach attributed to at-
mospheric oxidants.
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Table 1. EFFECT OF TIME OF DAY OF EXPOSURE
ON SENSITIVITY OF PINTO BEAN TO OZONE 7
Time of day
Portion of leaf damaged, %
9 a.m.
11 a.m.
1 p.m.
3 p.m.
39
63
60
47
Table 2. SENSITIVITY OF TOBACCO BEL W3
TO LOW LEVELS OF OZONE 7
Concentration, pphm
3.5
3.5
5.0
5-0
9.0
9.0
Time, hours
4
8
2
4
2
4
Portion of leaf damaged, %
12
56
1
14
11
45
Table 3. EFFECT OF LIGHT INTENSITY ON SENSITIVITY OF PINTO
BEAN TO OZONE EXPOSED AT CONSTANT TEMPERATURE7
Light intensity, ft-c
Portion of leaf damaged, %
2,600
1,800
100
Dark
89
73
10
2
15
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PAN IS HIGHLY TOXIC TO MANY PLANT SPECIES
Peroxyacetyl nitrate, commonly called PAN, is extremely toxic to
many plant species, especially small plants and young leaves. PAN is
unstable, particularly at temperatures above 90° F. Visible symptoms
of PAN injury include bronzing, silvering, and glazing on lower leaf
surfaces (Figures 16-19).
In this kind of damage, some of the spongy or the lower epidermis
cells or both become plasmolyzed, and the chloroplasts tend to lose
their integrity. After severe damage, additional spongy cells become
plasmolyzed and the cytoplasm changes color to light or dark brown.
The microscopic pattern of injury associated with PAN is shown in
Figure 19.
Studies have shown that injury varies directly with concentration
and length of exposure to PAN. Exposure to high concentrations of
PAN (0.8 ppm for 30 minutes or more) can cause severe injury on
young pinto bean plants. A low concentration of PAN, 0.5 ppm for 1
hour or 0.1 ppm for 5 hours, caused severe injury to pinto bean,
petunia, and tomato plants.11 Glazing or bronzing on the lower leaf
surface with little or no symptom visible on the upper surface devel-
oped when bean leaves were exposed to 0.8 ppm for 15 minutes.12
PAN concentrations as low as 0.01 ppm for 6 hours can cause plant
injury.
13
Physical changes have been found in the chloroplast structure of
pinto bean leaves exposed to 1 ppm for 30 minutes although injury
was not evident to the unaided eye.14
The light intensity under which pinto bean plants are grown and
exposed to PAN has a very pronounced effect on development of
visible symptoms. For the visible symptom to develop light is re-
quired by the plant for at least 3 hours preceding exposure, during
exposure, and for at least 2 to 3 hours following exposure.1 5
Figure 16. Triloliate leaf olpinto bean plant exposed to ambient air
shows bronzing symptoms caused by severe PAN injury.
Figure 17. Lower surface of primary leal ol pinto bean plant shows
silvering.
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Figure IS. Severe oxidant injury developed on lettuce plants grown
in Los Angeles, California, area.
Figure 19. Microscopic cross section ol petunia leaf exposed in
laboratory shows PAN injury. Spongy cells adjacent to
lower epidermis plasmolyzed, and chloroplasts lost their
integrity. Upper and lower epidermis and palasade cells
remained intact.
Overt symptoms of injury by PAN may be indistinguishable from
those produced by other pollutants. For example, PAN causes glaz-
ing and silvering on the lower surface of young trifoliate and primary
leaves of the pinto bean plant, but identical symptoms develop on
comparable plants exposed to irradiated automobile exhaust fumes
and irradiated pure components such as propylene and nitrogen ox-
ide, when tested under controlled conditions.16.1 7
Other studies demonstrated that plant injury similar to that found
on the lower surfaces of old leaves of pinto beans grown in Los
Angeles could be reproduced by exposing similar plants to a mixture
of gasoline vapor and ozone.18 Comparable results were obtained
with mixtures of ozone and certain olefins.16^ 7.19,20 Mixtures of
nitrogen dioxide and gasoline vapor also produced the same type of
injury.
Reddening and bronzing developed on the lower surfaces of old
primary and trifoliate leaves of pinto beans grown and exposed to
ambient air at Staten Island, New York, and Perth Amboy, New
Jersey.21 These symptoms also resemble those produced by ozone-
olefin products. It has been reported that a non-irradiated mixture of
ozone and 1-pentane, 1-hexane, and 3-heptane caused typical PAN-
type injuries to 14-day-old primary leaves of pinto beans, but did not
injure 8-day-old bean leaves or petunia leaves.22 During the course of
the studies at Staten Island and Perth Amboy21 in 1965 and 1966,
cloud cover and heavy concentrations of particulate matter in the
atmosphere were encountered. Because light intensity was reduced,
the ozone-olefin mixture was not fully irradiated.
17
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c
ombustion of coal, fuel oil, natural gas, and gasolines used in
power-generating operations is the source of nitrogen dioxide. In
addition to its role in producing ozone and PAN in the presence of
light and hydrocarbons, nitrogen dioxide alone injures vegetation.
Symptoms of nitrogen dioxide injury appear as irregular white or
brown collapsed lesions on tissue between the veins and near the leaf
margin (Figure 20).
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r
Figure 20. Petunia plant exposed to 13.5 ppm nitrogen dioxide lor 1
hour shows injury that resembles sullur dioxide damage.
Studies indicate that visible leaf damage to tomato seedlings is
caused by a concentration of 2.5 ppm nitrogen dioxide after 4 hours
exposure.15 Pinto bean plants are reportedly injured by a 3-ppm
concentration after 4 to 8 hours exposure.3 Nitrogen dioxide injury
to a tomato plant exposed to ambient air is shown in Figure 21.
Acute symptoms found on bean, tomato, and tobacco seedlings,
induced by an exposure to 2.5 ppm of nitrogen dioxide, also closely
resemble necrotic lesions (surface spotting) caused by sulfur dioxide
or injuries caused by excessive concentrations of ozone.11 A nitro-
gen dioxide concentration of 25 ppm injures most indigenous vegeta-
Plant growth may be inhibited by continuous exposure to 0.5 ppm
nitrogen dioxide or perhaps less.1 5 When applied continuously, ni-
trogen dioxide in concentrations below 0.5 ppm (and equivalent to
the levels recorded in the Los Angeles atmosphere) cause marked
chlorosis of basal leaves of tobacco.1 2
tion.
23
Figure 21. Tomato plant exposed In ambient air in Chattanooga,
Tennessee, ira.s injured hy nitrogen dioxide.
19
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ajor sources of sulfur dioxide are residential and commercial
buildings heated by coal or fuel oil of high-sulfur content, industrial
facilities such as petroleum refineries and some chemical plants, and
power-generating plants that burn sulfur-bearing fuel.
Sulfur dioxide causes both acute and chronic plant injury (Figures
22-29). Acute injury is characterized by clearly marked dead tissue
between the veins or on the margins of leaves. Chronic injury is
marked by brownish-red, turgid, or bleached white areas on the blade
of the leaf. The plant injury threshold for sulfur dioxide is 0.3 ppm
for 8 hours.
Plant injury is thought to be caused by sulfur dioxide, sulfuric acid
that forms as a by-product of sulfur dioxide in the atmosphere, or a
combination of both. It has been reported that for each 25 to 30'
parts of sulfur dioxide formed during combustion of fossil fuel, one
part of sulfur trioxide is formed. It continues to form as the combus-
tion products mix with the atmosphere. Sulfur trioxide, in turn, mav
rapidly combine with atmospheric moisture to form sulfuric acid.24
This acid may be suspended as small droplets, which cause distinct
punctate spots to appear on leaves. Most often, acid aerosol damage
occurs during foggy weather and the injury develops on non-waxy
leaves (Figure 25). This type of spotted injury has been reported in
the Los Angeles area during a period of heavy air pollution accom-
panied by fog or light rain.1 4 Similar injury may also occur without
fog, and its attendant moisture, in an area where there are combus-
tion by-products containing sulfur oxides and where the effluent
dew-point permits acid droplets to form. Usually the upper leaf sur-
faces display the initial necrosis. Cellular collapse and punctate spots
develop progressively through the upper epidermis, mesophyll layers,
and the lower epidermis of the leaf. No glazing or bleaching accom-
panies this injury.
20
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Figure 22. Rose leaves in Independence, Missouri, show marginal
and interveifiaJ necrotic injury from sulfur dioxide.
Figure 23. Laboratory-exposed potato leaves reveal typical sulfur
dioxide injury.
Figure 24. Salt bush plant was exposed to sulfur dioxide in lab-
oratory: this plant is excellent indicator of excess SOg.
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Figure 26. Pinto bean plant was sprayed with water before sulfur
dioxide exposure in laboratory.
Figure 25. Bindweed injury in Staten Island, New York, was caused
by sulfuric acid droplets.
Figure 27. Apple tree leaves near power plant in Pennsylvania shows
typical sullur dioxide injury.
22
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Figure 29. Forsythia in upper Ohio River Valley near Steubenville,
Ohio, was injured by sulfur dioxide.
Figure 28. Castor bean leaf injury resulted from laboratory exposure.
Figure 30. Necrotic injury on hydrangea leaf was caused by fly ash
from New Jersey power plant.
23
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Plants are particularly sensitive to sulfur dioxide during periods of
intense light, high relative humidity, adequate plant moisture, and
moderate temperature. Plants are, therefore, especially sensitive to
sulfur dioxide during the growing season in late spring and early
summer.
Time and levels of exposure affect plant sensitivity to sulfur diox-
ide. Plants exposed to high sulfur dioxide concentrations during the
early or late daylight hours are less affected by the gas than plants
exposed from 10:00 a.m. to 2:00 p.m. At night, when the stomata of
most plants are closed, the plants are much less susceptible to sulfur
dioxide injury.
The degree of turgidity of test plants is extremely important in
sulfur dioxide sensitivity. Soil dry enough to cause a slight wilting
increases plant resistance to sulfur dioxide injury. Turgid tomato
leaves are severely injured by sulfur dioxide, but slightly wilted leaves
are uninjured by the same concentration of the toxicant. Young
plants are more resistant than old plants, and middle-aged leaves are
most susceptible to injury. These differences are probably caused by
variations in the number, size, and activity of the stomata and the
quality of the cytoplasmic contents of the cells.
Microscopic examination of leaf tissue injured by sulfur dioxide
reveals that the mesophyll cells are affected and the chloroplasts
become plasmolyzed or bleached out. The spongy cells are often
more readily affected than the palisades. Under severe conditions the
epidermis cells are also plasmolyzed. The mid-rib and large veins
remain intact and green, even though most of the leaf has collapsed.
Injury to agricultural crops exposed to a given concentration of
sulfur dioxide is greater than the injury to laboratory-exposed plants
subjected to the same concentration because of possible additional
toxicants present in the uncontrolled ambient atmosphere. For this
reason, injury to agricultural crops is usually greater than can be
projected from laboratory experiments involving only one toxicant.
Low concentrations of sulfur dioxide can interfere with the
growth and functioning of a plant without leaving visible injury. This
injury may interfere with or reduce photosynthesis. Grain crops may
suffer a reduction in yield, especially if crops are damaged by sulfur
dioxide at the blossom stage.2
24
-------
0
that t
:one and sulfur dioxide together produce a synergistic action
tfiat reduces the injury threshold of leaf tissue. It has been reported
that an ordinarily harmless concentration of ozone, when combined
with sulfur dioxide, produced ozone-type injury to Tobacco Bel W3
plants.25 No injury developed from exposure of similar plants to
identical concentrations of the individual gases. See Table 4.
Table 4. SYNERGISTIC EFFECT OF OZONE AND SULFUR
DIOXIDE ON TOBACCO BEL W3 PLANTS25
Duration, hr
2
2
2
4
4
4
Toxicants,
03
0.03
0-027 <
0.031
0-28 +
ppm
S02
0.24
0-24
0.26
0.28
Leaf damage, %
0
0
38
0
0
75
Laboratory work has indicated that a single 4 hour exposure to
nitrogen dioxide below 2 ppm and to sulfur dioxide below 0.7 ppm
will not injure tobacco. Exposure for 4 hours to a mixture of 0.1
ppm of nitrogen dioxide and 0.1 ppm of sulfur dioxide produces
moderate injury to the older leaves of Tobacco Bel W3. Preliminary
experiments with ozone, nitrogen dioxide, and sulfur dioxide suggest
that a mixture containing 0.05 ppm of each of these toxicants injures
tobacco.26
In 1966 it was revealed that tobacco exposed to ambient air in the
Brooklyn Botanical Garden; Staten Island, New York; and Bayonne
and Roselle, New Jersey, showed ozone injury on plant leaves al-
though the ozone concentration was far below the injury thres-
hold.27. 28 Sulfur dioxide was shown to be present, however. Figure
31 shows a tobacco leaf exposed to ambient air and another to a
controlled, uncontaminated atmosphere during the New York-New
Jersey study.
Figure 31. Tobacco Bel W3 plants exposed to clean atmosphere
(le(t)andto ambient air(right) dramatize the possibility
of ozone • sulfur dioxide synergistic action.
AEROSOLS-SULFUR DIOXIDE
The presence of an aerosol may substantially increase the toxic
effects of sulfur dioxide. A study has indicated that in the presence
of dew, mist, or very light rain, a lower level of sulfur dioxide con-
centration than that required during a dry period could cause plant
injury.29 Heavy rains, however, might wash away the gas rather than
concentrate it on leaf surfaces.
25
-------
_| luorides in concentrations as low as 0.1 part per billion are toxic
to some plants.2 Fluorides in either gaseous or particulate form can
accumulate outside or inside plant leaves and cause leaf injury (Fig-
ures 32 through 39). Fluorides do not translocate from the leaf to
other parts of the plant. Even when high fluoride concentrations
exist in the leaf tissue, the root systems, flower seeds, and all other
plant parts remain very low in fluoride content.
Gaseous fluoride compounds are responsible for most fluoride in-
juries suffered by plants. Hydrogen fluoride and other gaseous com-
pounds are readily absorbed by the leaves. An accumulation of a
solid fluoride on its surface will not injure the leaf, however, unless
the fluoride on the leaf is dissolved by moisture. Dew or light rain
can provide the necessary moisture. The soluble fluoride then can be
absorbed readily by the tissues.
Principal sources of fluorides emitted to the atmosphere are ferti-
lizer manufacturing, aluminum reduction, ore smelting, and ceramic
manufacturing.
26
-------
Figure 33. In advanced stage, injury
progresses from tip to base
of gladiolus leaves.
Figure 32. Gladiolus plant shows beginning of fluoride injury on tips
of leaves.
Figure 34. Fluoride-injured pear leaves were collected in Staten Is-
land, New York.
27
-------
Figure 35. Prune /eaves (urn brown at edges when exposed to fluo-
ride.
Figure 37. Maple leaves from West Virginia were injured by fluoride
from nearby industry.
Figure 36. Italian prune leaves were injured during laboratory expo-
sure to fluoride.
Figure .38. Pine needles show sporadic injury.
28
-------
Figure 39. Young needles of ponderosn pine exposed to fluoride
Iright) were injured: control on left is healthy plant.
Vegetation closest to and downwind from a fluoride source suffers
the most severe injury.30 Measurements taken over the years from
such locations have disclosed alarmingly high fluoride concentra-
tions. Concentrations as high as 300 ppm of fluorine were found in
vegetation near aluminum and fertilizer plants in Tennessee.31 In
another case the fluoride level was 462 ppm. Nine miles from this
source the concentration on grape leaves was still 114 ppm. In still
another investigation, concentrations of more that 10,000 ppm fluo-
ride were found on pine trees in Montana.
Fluoride contamination of plants is manifested in several ways. In
gladioli, for instance, necrotic injury of the tissue starts at the tip of
the leaf and advances downward. On broad-leaf plants, the injury is
along the margin, and there is often a sharp demarcation line be-
tween injured and intact tissue. Injury to some plants appears as spots
of injured tissue surrounded by healthy tissue.
A study of citrus trees exposed to 2 to 3 ppm fluoride for several
months revealed leaf chlorosis. Compared with comparable trees
growing in fluoride-free air, the trees studied produced smaller leaves
and lower fruit yields, and grew less vigorously. In other plants stud-
ied, fluoride accumulations also caused dwarfing, leaf abscission,
dropping of fruit, and lower yields.32
of fluoride pollution at Staten Island, New York.21 Gladioli bulbs
were planted at five sites on June 27, 1965. Tip and margin burn
developed by July 20, and injury on the leaf blades gradually ex
tended downward and maintained a fairly uniform front. The gladioli
plants were harvested September 20, 1965, and leaf and petal sam-
ples from each of the five test stations were analyzed chemically. The
results are shown in Table 5. The amount of fluoride found and the
predominance of fluoride injury that appeared on the tips of the
gladioli leaves indicated that gaseous fluorides were present in the
atmosphere.
Table 5. RESULTS OF FLUORINE ANALYSIS OF GLADIOLUS
LEAF SAMPLES3
Location
Port Richmond
Willowbrook
Willowbrook (Control)
Princess Bay
Greenhouse at U. S.
Public Health Hospital
Location of sample
analyzed, inches
from blade tip
0 - 2
2 - 4
4 - 8
0 - 2
2 - 4
4 - 8
0 - 2
2 - 4
4 - 8
0 - 2
2 - 4
4 - 8
0 - 2
2 - 4
4 - 8
Fluoride
concentration, b-c
ppm
58.9
23.8
3.3
82.9
38.2
9.3
37.9
6.7
10.7
31.3
11.4
3.4
123.4
30.8
10.4
aGlodiolus petals collected from all five locations and analyzed forflu
found to contain 3.9 ppm, calculated on a dry weight basis.
In 1965, Snow Princess gladioli plants were used to locate
sources
Calculated on a dry weight basis.
cValues above 10 ppm are considered
ppm ore accurate to about ' 3 ppm.
ate to about ' 5 ppm; values under 10
29
-------
_ hlorine is found in the atmosphere primarily in those areas where
it is being used as a disinfectant or where it is involved in a chemical
process. For example, chlorine-injured plants are often observed near
swimming pools and sewage disposal systems.
Chlorine pollution causes marginal and tip necrosis, which may be
similar to the plant injury caused by sulfur dioxide. Middle-aged
leaves are most susceptible to chlorine injury, followed by the oldest,
then the youngest leaves. Photographs of chlorine injury are shown
in Figures 40-43.
The chlorine concentration required to injure plants is greater than
that reported for hydrogen fluoride, but less than the level reported
for sulfur dioxide.33
In a study at Rutgers University, tomato plants were exposed for 2
and 3 hours at three different chlorine levels.34 Half of the plants
were periodically sprayed with water. Response of plants, wet or dry,
was similar. A chlorine concentration of 0.31 ppm caused no injury,
0.61 ppm caused slight injury, and 1.38 ppm caused severe injury.
Stanford Research Institute reported injury to alfalfa and radishes
that were exposed for 2 hours to 0.10 ppm chlorine.33
30
-------
Figure 40. Chlorine injury to silver maple leaves is similar to sulfur
dioxide injury.
Figure 42. Begonia was injured by chlorine and by hydrochloric acid
mist in Pennsylvania.
Figure 41. Cucumber leaf exposed to 0.75 ppm Cl? lor 4 hours shows
injury similar to sullur dioxide injury.
Figure 43. Redbud leaves from
were also injured.
same area as begonia in Figure 42
31
-------
ethylene is one of the few hydrocarbons possessing the ability to
injure plants without undergoing photochemical reaction with nitro-
gen oxides.35 Unlike PAN and ozone, ethylene is difficult to extract
by carbon-filtering processes.
Ethylene is found principally in the atmospheres of larger cities
and urban areas because of the high concentrations of automobile
and truck exhaust, natural-gas and fuel-oil heating systems, and coal-
burning industrial processes.
Ethylene injury to orchids and azaleas is shown in Figures 44 and
45. In the Los Angeles area and Hawaii, ethylene has been reported
to cause the sepals of orchid flowers to become brown or withered
and dry. In an experimental study, the sepals of orchid flowers be-
came withered and dry after a 24-hour exposure to 5 ppm of ethyl-
ene.36 Exposure to 0.3 ppm ethylene for 1 hour or 0.05 ppm for 6
hours causes abnormalities in the sepals of cattleya orchids.
Ethylene interferes with the activities of plant hormones and
thereby causes growth retardation.6 In addition, carnation flowers,
for example, failed to open properly after a 6-hour exposure to 0.1
ppm.37 A 0.05-ppm ethylene exposure impaired normal develop-
ment of marigold leaves.38 Abnormalities of tomato leaves and loss.
of flower buds were observed after exposure of tomato and pepper
plants to 0.01 ppm ethylene for several hours.
32
-------
Extensive injury to a cotton field adjacent to a polyethylene man-
ufacturing area has been reported.3? The pollutant traveled 1 mile
downwind from the source, and the damaged field suffered almost
complete loss of yield.
Figure 45. Contra/ azalea on left has rigorous blooms, but plant on
right dropped blooms when exposed to ethylene.
Figure 44. Orchid at top was exposed to ethylene in laboratory;
intact orchid of same variety is shown at bottom.
33
-------
numi
TTC3
|n addition to the visible injuries caused by toxicants in the atmos-
phere, atmospheric pollutants or combinations of pollutants may
cause considerable injuries that disturb plant function and that alter
or suppress growth. An example of growth suppression is shown in
Figure 46.
Figure 46. Petunia on left was grown out ol doors. Larger plant on
right was grown in controlled environment.
34
-------
In one experiment, the action of ozone and 1-hexane in combina-
tion reduced tomato plant growth, but no visible symptoms of leaf
injury were observed. Tomato plants exposed to naturally occurring
oxidants in contaminated air had abnormally small leaves. Blossom
initiation was completely suppressed. Comparable plants grown in
carbon-filtered air developed normal blossoms and set fruit.
In 1966, it was found that growth was suppressed in Tobacco Bel
W3, pinto beans, petunias, and geraniums when grown for 8 weeks in
ambient air at Steubenville, Weirton, and Wheeling and for 10 weeks
in New York and New Jersey. These plants were compared to similar
plants grown in ambient air that was passed through an activated-car-
bon filter. Leaves on plants grown in carbon-filtered air were longer,
more vigorous, and darker green. Root systems of plants grown in
carbon-filtered air also were larger and more vigorous than those
grown in unfiltered air26' 27 as shown in Figure 47.
In a later study, chlorosis, dwarfing, and growth suppression of
petunia, columbine, geranium, and pinto bean plants developed.
These plants were exposed to ambient air, and the injuries probably
were caused by the interaction of a combination of toxicants.
It also has been shown that tree growth may be reduced by expo-
sure to ozone-olefin reaction products and to naturally occurring
oxidants.40 Exposure to ozone and hexane 41 for 280 hours over a
period of 8 weeks caused the following growth reductions in avocado
seedlings: stem growth, 56 percent; leaf width, 35 percent; and stem
diameter, 21 percent. The fresh weight of seedlings, including the
root system, was reduced 52 percent. The dry weight of seedlings,
including the root system, was reduced 58 percent. All comparisons
were made with comparable lots of avocados grown in carbon-fil-
tered air.
Figure 47. Root systems of pinto bean plants
grown with (above) and without (below)
activated-charcoal-filtered air.
35
-------
VEGETATION INJURY FROM OTHER AGENTS
CAN BE CONFUSED WITH AIR
POLLUTION INJURY
me striking similarities exist between visible injury from air pol-
ution and injury from other agents. Natural factors that may be
injurious are drought, frost, and mineral deficiencies. Other agents of
plant injury and disease include insects, nematodes, and viruses. Not
only can natural factors mimic pollution-like damage, but pollutants
themselves can sometimes mimic each other.
In 1965, injury by natural agents was thoroughly explored.42 It
was pointed out, for example, that terminal bleach disease in cereal
plants was caused by excessive water loss associated with hot winds.
Symptoms similar to sulfur dioxide injury can be induced by frost
(Figure 48) or even by mineral deficiency (Figure 49). Symptoms of
virus or nematode attack (Figure 50) also have to be taken into
consideration in diagnosis. Virus-like symptoms (Figure 51) are
sometimes confused with ozone injury.
In addition to the major air pollutants, other agents may cause
extensive damage to vegetation. One such agent is the herbicide 2,
4-D. Very low concentrations of 2, 4-D cause defoliation, dwarfing,
curling, stiffening, and twisting (Figure 52). Cotton, grape, and toma-
to plants are especially sensitive to 2, 4-D. Some insecticides are also
harmful to vegetation (Figure 53).
Because of the many possible mechanisms and sources of injury to
vegetation, investigators determining damage attributable to air pol-
lution should have extensive experience in the field.
36
-------
Figure 49. Cucumbers and leaves from plants with potash (center)
and nitrogen (right) deficiencies are shown with healthy
leal and cucumber (left).
Figure 48. Frost injury
oxide injury.
to geranium plants is similar to sulfur di-
Figure 50. Suspected sullur dioxide injury to Texas cotton
rightfully identified as nematode attack.
37
-------
Figure 51. Strikingly similar tobacco injury was from ozone (top)
and mosaic virus (right). Ozone attacks old leaves first,
then young leaves. Mosaic virus attacks young leaves
first and progresses to old leaves.
38
-------
Figure 52. Cotton leaves exposed to 2, 4-D are subject to "crow/-
footing," shown at right of photograph; healthy leaves
are shown on the left.
Figure 53. Tobacco was exposed to methyl paratnion.
39
-------
D D
_ir pollution injury to vegetation is not only important for the
economic losses it causes agriculture, but because vegetation injury is
a sign or forewarning of air pollution problems that can affect man
and his well being. Plants are considered to be a sensitive tool by
which the presence of several airborne toxicants in low concentra-
tions can be detected and evaluated.
The photographs in this document illustrate the damage that air
pollution can cause to vegetation. A number of the most serious
pollution offenders have been identified, and their effects have been
determined. Synergistic effects of multiple pollutants have also been
revealed. In most cases injury observed in indigenous vegetation has
been reproduced in laboratory experiments. Table 6 is a summary of
the well-known airborne pollutants that cause vegetation injury.
The investigator will need to use caution in diagnosing pollution
injury symptoms; and where there are uncertainties, he should obtain
help from scientific experts. Special care must be taken to differenti-
ate between pollutant symptoms and problems associated with min-
eral deficiency, plant disease, and other agents.
Toxicants stemming from photochemical reactions and the injuri-
ous effects of these toxicants have been found in at least 27 states
and the District of Columbia. Canada, Mexico, and Europe also are
known to suffer from similar problems.
The cost of agricultural losses in the United States was recently
estimated to be in the neighborhood of $500 million annually.
Losses to agronomic species in California alone are estimated to
amount to $132 million, with a 50 percent loss in citrus fruit.43 No
estimates have been made of the real economic loss caused by sup-
pression of growth, delayed maturity, reduction in yield, and the
attendant increase in the cost of crop production. Since air pollution
is growing in intensity in many areas of the country, the losses from
vegetation damage also are undoubtedly increasing.
40
-------
Table 6. SUMMARY OF POLLUTANTS, SOURCES, SYMPTOMS, VEGETATION AFFECTED, INJURY THRESHOLDS, AND CHEMICAL ANALYSES
Pollutants
Ozone (03)
Peroxyacetyl
nitrate (PAN)
Nitrogen
dioxide (N02)
Sulfur dioxide
(S02)
Hydrogen
fluoride (HF)
Chlorine (CI2)
Ethylene (CH2)
Source
Photochemical reaction of
hydrocarbon and nitrogen
oxides from fuel combustion,
refuse burning, and evapora-
tion from petroleum products
and organic solvents.
Same sources as ozone
High-temperature combustion
of coal, oi 1, gas, and gasol ine
combustion engines.
Coal, fuel oil, and petroleum.
Phosphate rock processing.
aluminum industry, iron
smelting, brick and ceramic
works, and fiber-glass
manufacturiag.
Leaks in chlorine storage
tanks; hydrochloric acid
mi st.
Incomplete combustion of
coal, gas, and oil for heat-
ing, and automobile and
truck exhaust.
Symptom
Fleck, stipple, bleaching
bleached spotting, pigmen-
tation, growth suppression.
and early abscission. Tips
of conifer needles become
brown and necrotic.
Glazing, silvering, or
bronzing on lower surface
leaves.
Irregular, white or brown
collapsed lesion on inter-
leaf margin.
Bleached spots, bleached
areas between veins,
bleached margin, chlorosis,
growth suppression, early
abscission, and reduction
in yield.
Tip and margin burn,
chlorosis, dwarfing, leaf
abscission, and lower
yield.
Bleaching between veins,
tip and margin burn, and
leaf absci ssion.
Sepa 1 withering, leaf
abnormalities,' flower
dropping, and failure of
flower to open properly.
Type of leaf
affected
Old,
progressing
to young
Young
Middle-aged
Middle-aged
Mature
Mature
(Flower)
Part of leaf
affected
Palisade
Spongy cells
Mesophyll
cells
Mesophy 11
cells
Epidermi s
and
mesophy 1 1
Epidermis
and
mesophy 1 1
All
Injury threshold0
ppm
0.03
0.01
2.5
0.3
0.1 (ppb)
0.10
0.05
Mg/m3
70
250
4700
800
0.2
300
60
Sustained
exposure
4 hours
6 hours
4 hours
8 hours
5 weeks
2 hours
6 hours
Reference
7
13
15
24
2
34
35
Chemical analysis
for po llutants
in plants
None
None
None
b
Distillation
and
ti tration
b
None
°Metric equivalent based on 25"C and 760mm mercury.
Chemical analysis often is not reliable for diagnosing chloride or sulfate accumulation in leaf tissue because undamaged plants often contain higher concentrations of these pollutants tha
41
-------
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44
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