Studies on Air Pollution Effects on Plants and

Development of Bio-indicators

In 1969, when Naveh started his research on air pollutants, the only information
available in Israel was from sporadic measurements of SO
2
by the Ministry of Health,
operating on a specially designed vehicle, and used chiefly in the Tel Aviv metropolitan
area. Therefore, he decided to put greatest emphasis on the development and use of bio-
indicators for quantitative monitoring of air pollution by fluor, photochemical oxidants
and sulphur dioxide.

Thanks to close personal contacts with the leading specialists from the North-Rhein
Westfalen Emission Control Institute (LIB) at Essen, Naveh gained most valuable
information on SO
2
pollution effects on plants and humans and monitoring by bio-
indicators, in the heavily polluted Ruhr-Rhein Region. To support Navehs pioneering
research in Israel, this institute donated two specially designed exposure chambers for
the measurement of controlled air pollutant concentrations. During his sabbatical year
at the University of California, Berkeley, he had long discussions with the scientists of
this university about the air pollution effects of smog and related insect pest infestations
of pine forests. He visited the San Francisco Municipality Center for Air Pollution
Control, at the State Wide Air Pollution Research Center of U.C. Riverside, and
examined closely the smog-damaged Ponderosa Pine forests in Southern California.

These studies were carried out with the help of Naveh's research assistant Silvia Chaim,
and in close cooperation with Dr. Eva Steinberger from the Department of Atmospheric
Sciences at the Hebrew University, Jerusalem. Steinberger was the first scientist in
Israel to measure atmospheric ozone concentrations with physical-chemical equipment
at her laboratory at the Terra Santa building in the center of the city of Jerusalem. She
found that ozone was carried with the Western Sea breeze from the heavily urbanized
coastal region up to the Judean hills. She also showed that with the complete cessation
of motorized traffic on Yom Kippur, these ozone concentrations dropped almost down
to nil.

The research methods included (1) systematic field surveys of the effects of air
pollution on natural vegetation, field and garden crops and ornamental shrubs in the
industrialized Haifa Bay area; (2) field exposure of seedlings of trees and shrubs for
early observation on sensitivity; and (3) exposure of sensitive plants and strains with
well-known typical responses to distinct air-pollutant concentrations in the field and
their fumigation with these pollutants in above-mentioned exposure chambers for the
development of quantitative bio-indicators with the help of bio-mathematical models.
The Technion Agricultural Experimental Farm in the Acre Plains served as control
station.


Phytotoxic effects of atmospheric SO2 concentrations on sensitive
plants and their bio-monitoring with Luzerne plants

The first indications of phytotoxic effects of SO
2
that could be damaging to human
health were obtained by Naveh, investigating the decline of the lichen Xantoria
parientina known for its high sensitivity to concentrations above 0.05ppm SO
2
. This
lichen, covering the stems of Maquis trees and shrubs on Mt. Carmel, was dying on the
north-western slope facing the industrialized Haifa Bay, up to the height of 300 m, but
was not damaged at all on the eastern slopes facing the Mediterranean Sea. Seven
years later in 1976 almost all the lichen colonies up to the top of the hills of the
western slope had degenerated. This was the first alarming sign of the impact of the
urban-industrial atmospheric environment not only on the biodiversity of these natural
landscapes, but also on human health.

Naveh and Chaim further detected wide-spread leaf damage attributed to SO
2
- on
field crops and Eucalypus canadulensis trees in the vicinity of the electricity power
station, the oil refineries, the steel plant, and on tree and shrub seedlings grown in the
ornamental plant nursery of Kibutz Ein Hashofet in the center of the Haifa Bay. The
only shrub without symptoms of damage was Pistacia lentiscus. The most severe
damage was observed on the ornamental plants and fruit trees in the home gardens of
Kirjat Benjamin at a distance of 700 meters from the refineries. Here, in 1972, Luzerne
plants (Medicago sativa, local Peruvian strain) were exposed as sensitive bio-
indicators. After only four weeks, these plants showed typical leaf biomass reduction
and acute lethal damage, occurring in SO
2
concentrations of 0.23-0.30 ppm that exceed
the tolerable air quality standards. At the instigation of Naveh, the Ministry of Health,
alarmed at the same time also by severe health complaints of the inhabitants and by
many asthma attacks among children of this quarter, carried out some sporadic
atmospheric SO
2
concentration measurements, ranging from 0.13-0.27 ppm.

However, it took almost ten years before physical-chemical instruments were installed
in the Bay Area, enabling the first control measures.

Bio-monitoring of fluorides with sensitive plants

In the vicinity of the phosphorus fertilizer plant "Deshanim" in the Haifa Bay, leaf
injuries and progressive degeneration were detected on sorghum, fruit trees, rose
shrubs, pine and cypress trees, attributable to fluoride gases (HF) that already, in low
atmospheric concentrations, could cause serious damage to humans, livestock and
plants. In fact, farmers complained that their cattle, fed by crops from fields in a
distance of 2000 m from "Deshanim" showed symptoms of poisoning. The research
team exposed the seedlings of eight plants with known sensitivity to HF at different
distances and wind-directions from the fertilizer plant and in these fields of Kfar
Chasidim, including Luzerne and "Snow Princess" gladiola, which are used for bio-
monitoring of fluor accumulation in pasture fields. They also determined the
accumulation of F in the exposed gladiola plants, comparing this with similar studies at
the Boyce Thompson Institute in the U.S. that were accompanied by exact
atmospheric measurements. In addition, to replace the lack of measurements for HF
concentration in the Haifa Bay, the researchers applied Pasquill's model of air pollutant
dispersion from a continued source in this case, the Deshanim fertilizer plant - for
mapping of isohletes with similar HF concentrations and used correlation equations for
the different stages of damage from known studies. As anticipated, they calculated
highly dangerous fluoride concentration of 26 ppb up to a distance of 300 m from the
fertilizer plant. At a distance of 2 km, these concentrations were still potentially
dangerous for humans and livestock. In fact, Luzerne plants in this field contained 100
ppm fluor. If consumed for longer periods by the cattle, this could have caused
fluorosis, infertility and other adverse effects.

As a practical guideline for early warning biological systems, researchers suggested the
use of acute damage of 10% of the leaf area and accumulation of 50 ppm fluorides as
indication of exceeding the allowed world quality standards for fluoride pollutants.

The use of sensitive plants for bio-monitoring of atmospheric
oxidant concentrations
In the 1970s, oxidants and chiefly ozone formed in the atmosphere in the presence of
sunlight were considered most serious air pollution hazards. Oxidants are components
of photochemical smog and their precursors are reactive hydrocarbons and nitrogen
oxides generated in urban regions during combustion of petroleum, chiefly by motor
cars. Under suitable meteorological and atmospheric conditions, they can also be
carried downwind to rural areas.

No information at all was available on these pollutants at that time in Israel. Therefore,
Naveh and his collaborators decided to investigate the possibility of damaging ozone
levels with the help of bio-monitors. Following the detection of phytotoxic atmospheric
concentrations of ozone above 0.05 ppm by exposure of three tobacco strains with
known different sensibility (kindly supplied by Dr. H. E. Heggestadt from the Beltsville
U.S. Agricultural Research Center), these tobacco strains were exposed in summer
1974 in the Haifa Bay at Kfar Massaryk, in the Acre Plains, in Jerusalem and in a
filtered and unfiltered exposure chamber at the Technion. In addition, Pinto beans,
showing typical ozone flecking leaf damage of above 0.09 ppm, were exposed in the
Haifa Bay. At the same time, Dr. Steinberger determined the constant atmospheric
ozone concentration monitoring of atmospheric ozone levels in Jerusalem. According to
the time required to obtain in the exposed plant a "threshold value" of maximum foliar
injury, in which 50% of the leaves showing 50 % of their surface injured by dark-
brown flecking a curve of an exponential non-linear type could be fit to indicate the
prevailing average atmospheric oxidant levels at each point of the curve for the period
of the measurement.

For practical agro-technical reasons, the researchers recommended the use of Pinto
beans. In conditions comparable to those prevailing in Israel, it can be assumed that if
Pinto beans reached the above described threshold value of ozone flecking after 20-25
days, then daily ozone concentrations could be expected ranging from 0.08 to 0.1 ppm.
These levels are highly damaging for many sensitive crops and can lead also to adverse
health effects.

As part of their matriculation requirements in biology, several high school students in
the Haifa region applied this bio-monitoring system successfully in their practical
studies. The research team recommended establishing a network of systematic ozone
bio-monitoring as an environmental education project in the Haifa metropolitan area
because at that that time the decision makers and the public were not yet aware of the
hazards of oxidant pollutants. If these recommendations had been implemented, this
information would have been available almost ten years earlier, when systematic
atmospheric ozone measurements were carried out, and which led to a long delay in
establishing oxidant emission control on cars.

The effect of photochemical air pollution by ozone on the decline
of pine forest trees in Israel

Extensive studies in California provided convincing evidence that Pinus species, and
especially Pinus ponderosa, after being exposed daily to ozone levels exceeding 0.05
ppm, are severely damaged in California forests and usually die as a result of attacks of
bark beetles on the ozonestressed trees. This knowledge was applied by Naveh,
Steinberger and Chaim to the study of the accelerating decline of Pinus halepensis
forests, observed along the road leading to Jerusalem in the Shaar Hagai canyon of the
central western Judean hills.

A preliminary survey of P. halepensis forests in the Western Galilee and Mt. Carmel
and the Shaar Hagai forests revealed the great resemblance of smog injury symptoms of
chlorotic mottle with those on pine tree needles in California, and the different stages of
gradual desiccation until the death of the injured tree. P. halepensis trees planted on the
campus of U. C. Berkeley also showed similar chlorotic mottle symptoms of light to
moderate degrees of smog conditions.

These findings were confirmed by fumigation tests in the exposure chambers. The tests
showed typical chlorotic mottle injuries on the needles of seedlings of P. halepensis in
concentrations of 0.05 and 0.1 ppm ozone, similar to those on P. ponderosa in
California. The same was true also for the pathological histological changes in the leaf
tissue, starting with the damage in plicate mesophyll cells and leading to the final
necrosis and collapse of all tissues. In P. halepensis, needles heavily infested by
Matsucoccus josephi scales, no specific damage to the mesophyll cells could be
detected and all tissues were consumed by the scales. In other pine species, including
Pinus brutia, which were apparently more resistant to these scale infestations, the
chlorotic mottle of ozone-injured needles was not marred by such heavy pest attacks.
However, in the Shaar Hagai forest, the only other conifers planted together with P.
halepensis were cypress Cupressus semperivirens, which were heavily ozone-damaged
and some, growing on the most exposed sites died.

Measurements by Steinberger in the summers of 1977 and 1978 showed that on 55% of
the days, the average hourly atmospheric concentrations of ozone in Jerusalem reached
0.057 ppm. The peak was reached after noon when the Sea breeze reached Jerusalem.

In 1975, a special committee including plant physiologists from the Hebrew University
was appointed by the Israeli government to investigate the cause of the decline of the
pine forest. Atmospheric measurements revealed high ozone concentrations of 0.2 ppm
in the most damaged forest parts of the hill slope. However, this research team could
not detect injury symptoms characteristic of ozone and distinct relationships between
the severity of injuries and distance from the highway. (Actually, no clear-cut gradient
would be expected because of the well-known great differences in sensitivity between
individual pine trees.) The research committee rejected the argument by the forest
entomologist, Dr. J. Halperin, that the Matsucoccus scales could be regarded as only a
secondary cause for the decline of the pine trees, after they had been predisposed by
other, unknown factors. No final conclusions for the causes of decline were reached and
the committee's only recommendation was to replace the dying P. halepensis trees with
P. brutia, because of their greater resistance to the scale attacks.

On the other hand, Naveh, Steinberger and Chaim concluded that like on the western
slopes of the Sierra Nevada Mountains in California, air masses carrying ozone from
the coast up to Jerusalem are apparently trapped in the Shaar Hagai canyon on their
way to Jerusalem on the western hill slopes. The result is atmospheric ozone
concentrations exceeding 0.05 ppm on most of the summer days. This ozone causes the
heavy damage to the pine trees, reducing their photosynthetic activity and their vitality
and therefore acting as a predisposing factor for pest infestation by the Matsucoccus
scales to which P. halepensis is especially susceptible. This, presumably in combination
with additional adverse factors such as chemical sprays and distorted predator-prey
relationships, led to the final decline of the pine trees.

Naveh and his colleagues stressed the urgent need for early recognition and monitoring
of present and potential impacts of air pollution by integrated long-term forest
ecosystem studies. As dense coniferous forests are vulnerable to air pollution, wildfires
and pest outbreaks, a new type of semi-natural, multi-species and multi-purpose open
Mediterranean forest is required with species of high fire and air pollution tolerance and
greater ecological and economic benefits.

Since the Shaar Hagai forest die-back, no more P. halepensis trees are planted in the
forests of Israel, but those still remaining are in progressive states of desiccation,
amounting to a great fire hazard because of the accumulation of vast amounts of dry
fuel. Because no follow-up survey of the above-described study has been carried out
since Navehs studies, there is no reliable information available on the status of the
newly planted P. brutia and other conifer trees in the forests of Israel.

A detailed report on the outcome of this study and the threats of photochemical air
pollutants to Mediterranean coniferous forests was published in 1980 in
"Environmental Conservation."

Detection of phytotoxic air pollutant concentrations within the Haifa
Oil Refineries

Invited by the management of the refineries to assist in assessing ambient pollutant
levels within the refineries, 19 indicator plants for the suspected air pollutants were
exposed from 1982 to 1983 in five sites within the refineries with control monitoring
stations at Kirjat Bialik Bay and the Technion. To confirm the concentrations indicated
by the field injuries of the exposed plants, ten of these species were studied in
laboratory fumigation tests with O
3
, SO
2
, NO
2
, C2H
4
(ethylene) and HF in Jerusalem.
To estimate the spatial distribution in the refineries of S0
2
- the major pollution detected
- a modified Gaussian dispersion model was applied.

These combined studies revealed that the only pollutant whose time-averaged
concentrations exceeded the greatly damaging threshold levels at specific exposure
sites was SO
2
, indicating a long-term average 0.10-0.15 ppm concentrations and peak
concentrations above 0.25ppm. The most severe, short-term emissions were
presumably caused by leakages in combination with high atmospheric stability. This
study showed that sensitive plants can be successfully utilized for the detection of
phytotoxic air pollutants within a given area.

In addition to reports of all these above-mentioned studies at the annual conferences of
the Israel Society for Ecology & Environmental Quality Sciences, their outcomes
appeared in 1979 in "Environmental Pollution" and by the Satellite Program in
Statistical Ecology of the International Statistical Program in "Statistical Ecology
Series", Volume 11. They created considerable interest, especially in developing
countries where no exact atmospheric concentrations of air pollutants were measured,
but no information is available on their actual application elsewhere.

With the exception of the last study at the refineries, all other studies were funded only
by the small internal research funds available from the Technion and the Hebrew
University. For this reason, no further studies on the effect of these air pollutants on
natural vegetation and economic crops could be carried out. As a result, this
information is still missing in Israel and most other Mediterranean countries.