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EVALUATION OF AIR P O L L U T I O N P H Y T O T O X I C I T Y IN A

SEASONALLY DRY TROPICAL URBAN ENVIRONMENT

JITENDRA PANDEY and USHA PANDEY


Centre of Advanced Study in Botany, Banaras Hindu University, Varanasi - 221 005, India

(Received: March 1994; revised: September 1994)

Abstract. This study was conducted in the urban environment of Varanasi, India, to evaluate the
plant responses to urban air pollution. Twenty sites were selected in four different zones of the city.
At each site, seven woody perennials of same age classes were selected. Out of the four zones (I,
II, III and IV), zone IV was used as a reference (control) zone as it received the minimum pollution
input. Plant species growing in polluted and control areas were compared with respect to foliar dust
load, per cent leaf area injury, leaf area, specific leaf weight and chlorophyll, ascorbic acid, SO]- S
and total N concentration in the leaves. Results indicated that the air pollution level in Varanasi
causes leaf damage, reduces leaf area, specific leaf weight and chlorophyll, ascorbic acid and total N
concentrations in the leaves. Sulphur concentration in leaves increased with increasing level of SO2
in the ambient air. The magnitude of such changes was maximum at the zone receiving maximum
pollution load. Carissa carandas was found to be the most sensitive species and Bougainvillea
spectabilis, the least. The study shows that the urban air pollution level in Varanasi is detrimental for
the growth of plants involved in this study.

1. Introduction

Interest in air pollution injury to plants is increasing in developing countries as new-


ly developing industries and urbanization have resulted in increased concentrations
of phytotoxic air pollutants. A high rate of economic growth in India during the
last few decades has resulted in large increases in urban populations and industries
concentrated in the cities. Emissions from heavily loaded and badly maintained
automobiles, domestic and industrial combustion of coal, and from other industrial
activities account for most of the urban pollution in India. Large-scale urban con-
struction, emission from railways, open disposal and burning of municipal solid
wastes are additional sources of urban air pollution. In Indian cities, concentrations
of phytotoxic air pollutants often exceed the toxic limits (NEERI, 1981; Dave,
1986; Mathur, 1986; Pandey et al., 1992; Pandey and Agrawal, 1992).
The ambient environment of urban-industrial areas generally contains several
pollutants, and plants growing in such areas are exposed to many pollutants in their
different combinations. It is possible to study the overall effect of a large number
of pollutants as total pollution load through quantifying unfavourable changes in
plants growing in their natural habitats. Such studies also help in monitoring the
level of air pollution in urban industrial areas (Le Blanc et al., 1972; Keller, 1983;
Posthumus, 1985; Agrawal and Agrawal, 1989; Chaphekar, 1990; Pandey and
Agrawal, 1991; Agrawal et al., 1991). Various plant morphological characters and
physiological and biochemical assays have been used for this purpose. Although

Environmental Monitoring and Assessment 33: 195-213, 1994.


(~ 1994 Kluwer Academic Publishers. Printed in the Netherlands.
196 JITENDRA PANDEY AND USHA PANDEY

inconsistent results have been reported, some plant parameters have proved to
be useful as diagnostic field tests for air pollution stress. Transplants of lichen
and bryophytes have been successfully used to monitor the level of air pollution
(Gilbert, 1970; LeBlanc et aL, 1972). However, in seasonally dry tropical regions
where the populations of lichen and mosses are very scarce, such studies can
only be performed with species of higher plants commonly found in these areas.
The literature available on the plant performance in urban areas shows that air
pollution reduces plant growth and the extent of growth reduction depends on
the plant species, concentration and distribution of pollutants and a number of
environmental factors (Mann et al., 1980; Mansfield and Freer-Smith, 1981; Smith
and Brennan, 1984; Treshow, 1984; O'Sullivan, 1985; vanBreemen, 1985; Agrawal
and Agrawal, 1989; Pitelka and Raynal, 1989; Ulrich, 1989; Smith, 1990, 1991;
Pandey and Agrawal, 1994; Narayan et al., 1994). In India, however, only a few
studies have compared plants growing in different urban areas for air pollution
sensitivity (Varshney, 1986; Chaphekar, 1990; Singh et al., 1991; Pandey and
Agrawal, 1991, 1994).
The present study was conducted in Varanasi, which is found to be one of the
most polluted cities in India (Pandey, 1993). The occurrence of distinctly wet and
dry seasons in an annual cycle was found to be the most important factor that
results in marked seasonality of air pollutant concentrations (Pandey and Agrawal,
1992; Pandey et al., 1992). Vegetation of the area has been chronically exposed to
spatially and temporally varying levels of air pollutants. Limited contemporary air
monitoring data suggest that although 24-h average concentrations of SO2, NO2
and total suspended particulates were generally below primary pollutant standards,
2-h peak concentrations were considerably higher (Pandey et al., 1992). Ozone
monitoring data showed chronic exposure during summer months only (Pandey and
Agrawal, 1992). There is however a general lack of information on plant pollutant
interaction in such areas. The present study was designed to investigate how and
to what extent the urban air pollution level in Varanasi affects the performance of
selected woody perennials. Such studies are important for the scientific and rational
management of tropical cities.

2. Materials and Methods

2.1. STUDYAREA

The study area (25 ° 181N, 83°011E and 76.19 m altitude), with population of about
1.03 million, is located in the eastern Gangetic plain of the Indian subcontinent.
The climate of the area is tropical monsoonic, with three distinct seasons, hot
and dry summer (March to June), warm and wet rainy (July to October) and a
cool and dry winter season (November to February). The first half of the summer
season experiences strong hot dry winds and high temperatures, while the second
AIR POLLUTIONPHYTOTOXICITY 197

half is generally hot and humid. During the summer of 1989-1990, the maximum
temperature ranged from 22°C to 41°C and the day light duration from 10 to 14 h.
During the 1989-1990 rainy season, which accounted for about 90% of total annual
rainfall (924 mm average), the maximum temperature ranged from 32°C to 34°C
and the relative humidity from 65% to 85%. The temperature varied between 6°C to
31 °C in the winter season during 1989-1990. Wind direction shifted predominantly
westerly and north-westerly in October to April and to easterly and north westerly
in the remaining months.
The soil of the region is alluvial, sandy loam in texture and usually light brown
in colour with a moderate water holding capacity (34-57%). The pH ranges from
7.3 to 7.6. Total soil nitrogen ranges from 0.05 to 0.09%; organic C, 1-2%; avail-
able P, 0.003-0.005%; exchangeable K, 0.1-0.14%; exchangeable Ca, 0.5-0.8%
and cation exchange capacity from 11.2 to 15.4 meq 100 g-1 (Pandey, 1993).
The vegetation was mainly comprised of artificial plantations interspersed with
seasonally growing weeds and perennial shrubs.
The study area was divided into four pollution zones and five microsites were
selected in each zone. Two of the zones (I and II) represented the area along major
highways which receive pollutants from motor vehicles, small-scale industries and
railway tracks. The third zone (III) is characterized by moderate traffic frequency
but often experiences traffic congestions, while the fourth zone (IV) situated at
south-west of the city, represents a residential locality with official buildings,
gardens and cultivated land. Temperature and relative humidity did not show
significant variations between sites (e.g. T+0.5°C, RH+2). All plants were selected
in unshaded open areas, and received uniform light.

2.2. AIR MONITORING

Continuous air quality monitoring was done by using High Volume Samplers
located at 1.5-3.0 m above ground level in the city at each site. Total suspend-
ed particulates were trapped on a glass-fibre filter paper attached to the hopper
of HVS. The high volume samplers were not equipped with a particle size cut.
Gaseous pollutants such as SO2, NO2 and 03 were scrubbed separately in tetra-
chloromercurate, NaOH (0.1 N) and buffered KI (0.1 N), respectively, at 2-h inter-
vals. These absorbing solutions were analyzed colorimetrically for SO2 (West and
Gaeke, 1956), NO2 (Merryman et al., 1973) and 03 (Byers and Saltzman, 1958),
respectively. The data were presented as 24-h average and 2-h peak concentrations,
and expressed as #g m -3 (Table I).

2.3. SELECTION OF PLANT SPECIES

The plant species chosen for this study are commonly found in and around the
city of Varanasi. Two of them are fruit trees (Mangifera indica L. and Psidium
guajava L.), two leguminous avenue trees (Delonix regia Rafin and Peltophorum
198 JITENDRAPANDEYANDUSHAPANDEY

TABLE I
Annual 24-h average air pollutant concentrations (/zg m - 3 in different
zones of Varanasi city. Values in parentheses represent 2-h peak concen-
trations.
Year Pollutants Zones
I II III IV

1989 SO2 66(234) 59(205) 48(176) 15(37)


NO2 5 1 ( 1 5 9 ) 50(125) 38(94) 19(39)
03 45(169) 44(149) 33(105) 14(36)
TSP* 305(733) 280(694) 231(540) 143(265)

1990 SO2 79(238) 74(203) 52(181) 15(39)


NO2 5 9 ( 1 5 9 ) 51(119) 43(101) 19(42)
03 48(149) 50(159) 41(105) 16(30)
TSP* 336(1056) 323(892) 258(610) 126(215)

*Total suspended particulates.

pterocarpum (DC) Baker ex. K. Heyne), one deciduous timber tree (Dalbergia
sissoo Roxb), one ornamental shrub (Bougainvillea spectabilis, Wild) and a spiny
shrub bearing edible acidic berries (Carissa carandas L.). These species are well
represented in seasonally dry tropical areas. Five individuals of each species of the
same age class and basal diameter were marked at each microsite. Branches of the
same age group were tagged for each individual.

2.4. PLANT SAMPLING AND ANALYSIS

Sampling was done at monthly intervals from January 1989 to December 1990. For
this purpose fully expanded leaf samples were collected at the 3rd to 5th positions
from terminal buds of tagged branches between 08.00 and 10.00 h. These leaves
were then pooled together and samples in triplicate were taken from five replicates
of each species at each microsite.
For foliar dust load, leaves were carefully and repeatedly washed off with
deionized water into a beaker of known weight. The water was then evaporated
on a hot plate and reweighed. The difference between initial and final weights of
the beaker gave the amount of dust deposited on the leaf surfaces. The data were
expressed as mg particulates cm -2 of the leaf area.
Leaf area was measured with a portable leaf area meter (LI-COR, USA). Plant
leaves were closely examined for lesions, if any, in the form of chlorosis, necrosis,
bronzing, etc. and the injury was quantified as percentage of leaf area injured using
a Planimeter (Type KP-27, Koizumi, Japan). For computing specific leaf weight
(SLW), the dry weight of leaf was divided by leaf area. Chlorophyll was extracted
AIR POLLUTION PHYTOTOXICITY 199

TABLE II
Seasonal variation in foliar dust load (mg cm-2) of plants growing at differentzones of Varanasi
city.

Plant species I II III IV


W S R W S R W S R W S R

M. indica 8.35 4.25 2.05 8.12 4.20 2.15 6.35 2.48 1.86 2.22 1.55 1.05
D. sissoo 2.45 2.20 0.78 2.47 2.15 0.86 2.05 1.89 0.62 1.00 0.95 0.45
D. regia 4.40 3.62 1.85 4.28 3.19 1.73 3.35 1.72 1.28 1.65 1.12 0.72
B. spectabilis 6.61 4.14 3.80 6.25 4.12 2.90 4.19 3.10 2.00 2.20 1.18 0.85
P. guajava 5.25 3.78 1.50 4.88 2.92 1.40 3.86 2.20 1.21 1.75 0.98 0.75
C. carandas 3.28 3.10 1.25 3.10 3.12 1.20 2.35 2.30 0.92 1.16 1.20 0.65
P. pterocarpum 3.75 3.48 1.40 3.66 3.50 1.15 2.60 2.62 1.18 1.85 1,55 1.00

W: winter; S: summer; R: rainy.

in 80% acetone. The optical densities of the extracts were measured at wavelengths
of 645 and 663 nm through a spectronic 1001 spectrophotometer (Milton, Roy and
Co., USA). The amount of chlorophyll was calculated using the formula given
by Maclachlan and Zalik (1963). For ascorbic acid, the method given by Keller
and Schwager (1977) was followed. For nutrient analysis, thoroughly washed leaf
samples were oven dried at 80°C until a constant weight was obtained. Dry and
powdered samples were used for the determination of total N and S O ] - - S contents
following the micro-kjeldahl technique of Misra (1968) and turbidimetric method
of Rossum and Villarruz (1961), respectively.
To test the level of significant differences among plant species, sites and seasons,
data for leaf area, specific leaf weight, chlorophyll, ascorbic acid, total N and
sulphate S were analyzed using three-way analysis of variance.

3. Results

On the basis of air quality data the sites in the urban areas of Varanasi can be ranked
from maximum pollution load to a minimum as ! > II > III > IV (Table I). Zone
IV situated at south-west of the city, is typically a residential locality with official
buildings, gardens and cultivated land. Since the predominant wind direction of
the area is westerly, this zone received minimum pollution input. Since all the
pollutants are lowest in zone IV, the data for this zone was used as the reference
for comparing the changes in plant parameters obtained at other zones.
The results presented here are an average of the data collected for two years
of study. Maximum dust deposition was observed for M. indica, followed by
B. spectabilis, P. guajava, D. regia, P. pterocarpum, C. carandas and D. sissoo
plants in zone I, the respective values being 8.35, 6.61, 5.25, 4.40, 3.75, 3.28 and
200 JITENDRA PANDEYAND USHA PANDEY

TABLE III
Percent leaf area injury in plants growing at different zones of
Varanasi city.

Plant species I II III


W S R W S R W S R

M. indica 16.0 14.6 4.2 14.8 14.1 3.5 5.1 5.0 2.2
D. sissoo 17.5 6.2 4.8 14.9 5.6 3.9 5.6 3.2 2.6
D. regia 12.5 4.8 4.5 10.2 4.9 3.9 4.7 2.2 2.0
B. spectabilis 6.1 5.0 3.9 6.0 5.1 3.8 3.2 3.2 1.8
P. guajava 7.2 4.5 4.0 6.8 4.6 3.9 3.6 3.1 2.0
C. carandas 19.2 18.0 7.6 17.5 17.2 6.9 8.6 8.2 3.0
P. pterocarpum 7.8 6.6 4.7 7.3 7.0 4.6 4.0 3.8 2.4

W: winter; S: summer; R: rainy.


At zone IV visible injury symptoms were not seen.

2.45 mg cm -2 during the winter season. Foliar dust deposition at all sites was
maximum during winter followed by summer and rainy seasons (Table II).
A visual inspection of pollution-impacted areas indicated an overall physical
effect of air pollution in terms of reduced plant growth. With respect to foliar
injury, C. carandas leaves were most extensively damaged followed by D. sissoo,
M. indica, D. regia, P. piterocarpum, P. guajava and B. spectabilis (Table III). In
all the plant species, per cent foliar injury was maximum in zone I and the extent
of leaf damage was highest during winter months.
Plants growing at polluted sites (i.e zones I, II and III) showed reduced leaf area
(LA) and specific leaf weight (SLW) compared to the plants at zone IV. Maximum
reductions in both LA and SLW were observed in C. carandas plants (Table IV
and Figure 1). In zone I the per cent reductions in LA and SLW as compared to the
plants in zone IV, were 31.3 and 36.3, respectively for C. carandas during the winter
season. Leaf area reduced minimally in D. sissoo while SLW reduced minimally
in B. spectabilis. Differences in leaf area and specific leaf weight were significant
with respect to plant species, sites and seasons (Table V). Sitewise differences both
in leaf area and specific leaf weight were usually greater, however.
Chlorophyll concentration in plant leaves in zones I, II and III was reduced
compared to the plants in zone IV (Figure 2). Significant negative correlations
were observed between total chlorophyll contents of different plant species and
ambient air concentrations of pollutants (p < 0.01 for SO2, NO2 and O3 and
p < 0.05 for TSP). Chlorophyll a was found to be more sensitive to pollution than
chlorophyll b. Maximum reduction in total chlorophyll content was observed in D.
regia followed by C. carandas, D. sissoo, M. indica, P. guajava, B. spectabilis and
then in R pterocarpum in zone I during winter and the respective per cent decreases
compared to the plants in zone IV were 57.6, 56.7, 45.8, 43.5, 40.4, 39.1 and 35.3.
AIR POLLUTION PHYTOTOXICITY 201

O
t~

65

..=
202 JITENDRA PANDEY AND USHA PANDEY

1B m

Iv. . . .
17

16"
F~ W i n t e r
15
B Summer
14
r] R a i n y
13
(~
I
12 D. sissoo D. regia B. spectabiiis
E
u 11
E~
E 10

J:: 9
o ~

0) 8

7
0
6
U
I II III IV I I I I I I IV III I I I IV I I I I I I IV
13
, w

U P.guajava C.carandas P. pterocarpum


e 12
o.
V)
11

10

8 ~

7
6 -
I II [IIIV I II mIV I II III IV
Zone
Fig. 1, Seasonal variation in specific leaf weight of plants growing at different zones of Varanasi
city.

Mean square estimates of chlorophyll were significantly affected (at P < 0.005)
by plant species, seasons, sites and their interactions (Table V).
AIR POLLUTION PHYTOTOXICITY 203

7 -M. indica D. sissoo _.D.recdia ._B.spectabilis


5
5

T 0
tm I II IIITV I II IIIIV I II IIIIV I I I I I I IV
E
7 P. g u o j a v a C. corandas P. pterocorpum
>, 6 1
d~
O.
o 5 Chl b__
l.,
o
e, D Ch,
3

0
I II I I I IV I II Trl IV I II 111 IV
Zone
Fig. 2. Chlorophyll content of plants growing at different zones of Varanasi city. At each site the
left, middle and right column represent total chlorophyll contents during winter, summer and rainy
season, respectively.

Ascorbic acid concentration was maximum in B. spectabilis followed by P.


guajava, P. pterocarpum, M. indica, D. regia, D. sissoo and C. carandas plants
(Figure 3). These species in Zone I had 30.6, 40.0, 24.5, 34.1, 36.7, 5.9 and 42.9%
respectively less ascorbic acid than those in Zone IV. Differences in ascorbic acid
content due to plant species, sites and seasons were significant at P < 0.005.
Foliar N concentration decreased in plants growing in zones I, II and III com-
pared to those growing in zone IV (Table VI). Maximum reduction in foliar N
content was observed in D. regia (38.9%) followed by C. carandas (36.7%), D.
sissoo (32.0%), M. indica (31.8%), P. pterocarpum (26.0%), P. guajava (25.0%)
and B. spectabilis (15.5%) in zone I during the winter season. Differences in nitro-
204 JITENDRAPANDEYAND USHAPANDEY

TABLE V
Variance ratios (f) obtained from three way analysis of variance for difference plant parameters.

Plant parameter P SS S P × SS P× S SSx S PxSS x S

Leaf area 9435.76* 525.08* 69.65* 142.26" 42.65* 16.28" 16.52"


Specific leaf weight 1653.28" 227.56* 86.72* 297.85* 33.76* 168.25" 16.21"
Chlorophyll 6677.38* 7984.69* 1886.24" 178.34" 251.13" 13.93" 92.75*
Ascorbicacid 81614.83*7204.15" 1596.38" 551.41" 169.48" 49.59* 28.90*
Sulphate S 96.46* 55.74* 13.97" 1.14Ns 0.33Ns 0.40ys 0.10Ns
TotalN 786.74* 1465.45" 118.01" 48.17" 12.56" 3.27* 1.98"

P: plant species; SS: study site; S: season.


Significance at *p < 0.005; NS: not significant.

TABLE VI
Seasonal variation in total nitrogen concentration (mg g-~ dry weight) of plants growing at
different zones of Varanasi city.

Plant species I II Ill IV


W S R W S R W S R W S R

M. indica 15.0 14.0 15.8 14.6 14.2 16.2 21.0 18.9 23.0 22.0 21.0 23.7
D. sissoo 13.6 13.0 13.2 14.0 13.7 13.9 16.7 14.8 16.2 20.0 19.0 19.6
D. regia 18.2 17.4 19.0 19.0 17.8 19.8 23.6 21.5 23.0 29.8 27.8 29.5
B. spectabilis 13.6 12.6 14.0 14.2 12.6 14.5 15.0 13.6 15.1 16.1 14.9 16.9
P. guajava 13.5 13.0 12.5 13.6 13.5 13.0 14.5 13.0 14.2 18.0 17.2 16.3
C. carandas 14.0 12.0 13.8 15.4 12.6 13.5 17.8 15.7 18.0 22.1 18.5 21.0
P. pterocarpum 16.5 16.0 16.0 17.2 17.0 17.7 19.0 18.2 18.8 22.3 22.0 21.5

W: winter; S: summer; R: rainy.

gen concentration were significant a m o n g the plant species, sites, seasons and their
interactions (Table V).
In all the plant species SO 2 - - S accumulation was m a x i m u m at zone I followed
by zone II, III and IV (Table VII). Sulphate S accumulated maximally in C. carandas
(+91.3%) followed by P. pterocarpum (+68.0%), P. guajava (+67.7%), D. sissoo
(+55.3%), M. indica (+44.8%), B. spectabilis (+36.9%) and D. regia (+26.9%) in
zone I during the winter season.

4. Discussion

Differences in leaf area, specific leaf weight and in chlorophyll, ascorbic acid and
nitrogen concentrations in plants growing at different zones m a y be ascribed to the
AIR POLLUTION PHYTOTOXICITY 205
10
B. spectabitis

l.i/
_ I..~
I:v
FV
I."
w
M. indic__.._~a D. sissoo D_ regi..__...aa
•- ~ 4 - 1.1/
(1/

I-V
I.v
[.'v
'-
"IJ 2

7"
t~ 0
E I II TIT IV I II 1111V I II ]II IV I II IIl IV
P. g u a j a v a
19
tJ
6
19
°m
n R pterocer )urn
t-
O
Winter
o 4 -
,< Summer
['] Rainy
2-

_
I 11 111 IV I II llllV I II I I I IV
Zone
Fig. 3. Seasonal variation in ascrobic acid content o f plants g r o w i n g at different z o n e s o f Varanasi
city.

varying levels of air pollution input in Varanasi city. Reductions in these parameters
were maximum in zone I receiving maximum pollution load. Maximum reductions
in different plant characteristics during winter may also be correlated with max-
imum pollution load during this season. Bleasdale (1952) observed significant
growth depression in Lolium perenne plants grown at polluted urban sites in the
U.K. Other studies on plant growth along gradients of ambient air pollution have
confirmed that air pollution is a major factor influencing plant growth in and around
206 JITENDRAPANDEYANDUSHAPANDEY

TABLEVII
Seasonal variationin sulphate-sulphur concentration(rag g- 1dry weight) of plants growing at
differentzones of Varanasi city.

Plant species I II III IV


W S R W S R W S R W S R
M. indica 2.10 1.90 1.78 2.05 1.92 1.65 1.82 1.72 1.42 1.45 1.42 1.38
D. sissoo 1.32 1.18 1.10 1.20 1.16 1.00 1.10 1.05 0.82 0.85 0.72 0.69
D. regia 2.40 2.21 2.05 2.40 2.46 2.10 2.27 2.21 2.00 1.89 1.79 1.76
B. spectabilis 3.15 3.00 2.76 2.95 2.95 2.69 2.72 2.67 2.32 2.30 2.24 2.14
P. guajava 2.43 2.37 2.07 2.39 2.30 2.00 1.69 1.60 1.40 1.45 1.36 1.20
C. carandas 1.76 1.64 1.59 1.70 1.57 1.60 1.34 1.25 1.21 0.92 0.90 0.85
P. pterocarpum 2.10 1.94 1.67 2.11 2.00 1.62 1.74 1.45 1.40 1.25 1.25 1.12

W: winter; S: summer; R: rainy.

urban industrial areas (Ashmore et al., 1988; Agrawal and Agrawal, 1989; Smith,
1990; Narayan et al., 1994; Pandey and Agrawal, 1994). The forest decline, which
has been noted in Europe (Van Breemen, 1985; Ulrich, 1989) and north-eastem
United States (Smith, 1991), has been blamed on a variety of factors including
atmospheric deposition (Van Breemen, 1985; Pitelka and Raynal, 1989).
The visible injury symptoms were in the form of biracial chlorosis and necrosis.
The necrotic symptoms were mainly observed towards the tip and the margins of the
leaves. This may be an interactive response of the dust deposited on foliar surfaces
and the simultaneous absorption of various gaseous pollutants. In the presence of
a variety of pollutants, specific injury symptoms are difficult to identify. Severity
in foliar injury during winter may be ascribed to high concentrations of SO2, NO2
and TSP in the winter months. Leaves of all the species retained varying levels of
dust particulates; however, the severity of foliar injury was not associated with the
amount of dust deposited on leaf surfaces. Maximum dust deposition was observed
on M. indica, whereas foliar injury was maximum in C. carandas.
Reduction in leaf areas due to leaf injury, as well as reduced leaf expansion as
observed in the present study, is known to reduce the photosynthetic capacity of
plants (Heck et al., 1981; Steubing and Fangmeier, 1987; Byres e t a l . , 1992). Cell
elongation is known to be more sensitive to stresses than photosynthesis and cell
division (Horst and Nelson, 1979), consequently leaf elongation may cease when
stress is imposed, resulting in reduced leaf size.
As specific leaf weight (SLW) is the measure of dry matter accumulation per
unit leaf area, reduction in SLW further reflects reduced plant photosynthesis
and poor photosynthate reserves in leaves at sites receiving a higher pollution
load. Maximum reduction of SLW in C. c a r a n d a s indicates the sensitivity of
this species under pollution stress conditions. It is well established that pollutants
AIR POLLUTION PHYTOTOXICITY 207

affect the growth and physiology of plants (Darrall, 1989). Altered physiological
and metabolic processes in plants may reduce dry matter accumulation per unit
leaf area. Rao and Dubey (1988) also observed significant reduction in the foliar
dry weight of plants growing in an area contaminated with SO2.
Reductions in chlorophyll, ascorbic acid and nitrogen concentrations provide
further evidence that urban air of Varanasi contains pollutants at phytotoxic levels.
Several investigators have described chlorophyll as a sensitive indicator for air
pollution levels and effects (Darrall and Jager, 1984; Nandi et al., 1986). It is
suggested that pollutant gases such as SO2, NOx and 03 produce oxyradicals
which damage plant cell membrane and other cell molecules including chlorophyll
pigments (Shimazaki et al., 1980; Sakaki et al., 1983; Malhotra and Khan, 1984;
Wolfenden et al., 1992). Agrawal and Agrawal (1989) and Pandey and Agrawal
(1991) reported significant reductions in chlorophyll concentrations in different
woody perennials growing in a polluted environment. The loss of chlorophyll a
was greater than that of chlorophyll b in all the species. A similar trend was reported
by Kondo et al. (1980).
Some investigators have established a direct relationship between endogenous
levels of ascorbic acid and plant susceptibility to pollutants (Lee et al., 1984; Chen
et al., 1990). Ascorbic acid, a natural antioxidant, maintains the stability of the
plant cell membrane during pollution stress (Dhindsa et aL, 1982) and scavenges
cytotoxic free radicals (Halliwell, 1982; Mehlhorn et al., 1987; Halliwell and
Gutteridge, 1989; Pandey and Agrawal, 1993). Significantly high levels of AA in
B. spectabilis and P. guajava have rendered these species less sensitive to urban
air pollution. Contrary to this, C. carandas containing a markedly low level of AA
showed maximum reduction in its level at polluted zones, which further suggests
the higher sensitivity of this species. Varshney and Varshney (1984) have reported
high A A concentrations in leaves of resistant plant species compared to sensitive
ones, and a slower decline of AA in the previous species. Keller and Schwager
(1977) reported a reduction in AA concentration of forest trees fumigated with
S O 2. Lee et al. (1984) however reported AA accumulation in plant cells. Mehlhorn
et al. (1986) have found no effects on ascorbate levels in needles of spruce and
fir fumigated over a two-year period with ozone. Ascorbic acid concentration in
leaves thus also influenced the sensitivity of plants in the present study as the
concentration was maximum in B. spectabilis which showed minimum decline
in AA vis-&-vis less sensitivity to urban air pollution in terms of less leaf area
damage and lower reductions in specific leaf weight and of chlorophyll and nitrogen
concentrations.
In spite of the high level of NO2 in the urban atmosphere of Varanasi, nitrogen
concentration in leaves decreased at sites receiving a higher pollution input (zones
I, II and III) compared to the plants growing in zone IV. Reduced N concentrations
in the needles of Betula pubescens, Betula pendula, Picea abies and Pinus sylvestris
in two industrial areas of Sweden contaminated with SO2 and heavy metals have
been reported (Balsberg-Pahlsson, 1989). NO2 has been shown to be absorbed
208 JITENDRA PANDEY AND USHA PANDEY

and assimilated into various organic-N compounds leading to elevated foliar-


N concentrations (Troiano and Leone, 1977; Wellburn et al., 1980). Fumigation
with NO2 has been shown to stimulate nitrite reductase activity in pea seedings
(Zeevart, 1974), and nitrate reductase activity in tomato plants (Wellburn et al.,
1980). Wellburn et al. (1981), however, have shown that the presence of SO2
inhibits the reduction of nitrite in leaves which may further interfere with the
assimilation of NO2.
The differences in the amount of S in leaf tissues reflected the varying degree
of SO2 contamination at different zones. Sulphate fraction is usually considered to
represent a pool of accumulated S when uptake of SO2 exceeds to metabolic demand
for the synthesis of organic S compounds (Cowling and Koziol, 1978). Atmospheric
SO2 has been shown to increase foliar S concentrations (Agrawal and Agrawal,
1989; Fangmeier, 1989). Varshney (1985) observed that the sulphur content of
eleven woody perennials growing around a thermal power plant vary with species
and the extent of pollution load in the area. In the present study, S content in leaves
varied depending on species, site and season. Significant positive correlations
between foliar S and atmospheric SO2 concentrations (Figure 4) indicate that the
S accumulation in plant may be a reliable measure of SO2 concentration in the
air. Foliar S accumulation in plants has been used for monitoring SO2 emission
(Agrawal and Agrawal, 1989).
In the present study, the pattern of change observed in plant characteristics of
different species may be related to their susceptibility. A comparison of the foliar
response of different species indicates that C. carandas suffered maximally due
to air pollution stress while B. spectabilis, the least. Other species such as D.
sissoo, M. indica, P. pterocarpum and P. guajava were at an intermediate position.
Delonix regia may also be ranked sensitive like C. carandas as this showed similar
levels of reduction in leaf area, SLW and ascorbic acid and greater reductions
in chlorophyll and N concentrations. Carissa carandas showed maximum foliar
injury and reductions in leaf area, SLW and AA concentrations. The low level of
A A and a greater reduction of it in C. carandas at polluted sites have rendered this
species more sensitive than others to urban air pollution. Bell and Mudd (1976)
have suggested that sensitive plants undergo higher chlorophyll reduction than
resistant plants in the presence of air pollutants. Singh et al. (1991) have suggested
that a high chlorophyll concentration in resistant plants enables them to tolerate
pollution stress better than sensitive species. However, this did not appear true for
the present study as the plants with higher chlorophyll concentrations (D. sissoo
and P. pterocarpum) showed an intermediate level of sensitivity with respect to the
changes in other plant characters. The direct relationship between per cent foliar
injury and sulphur accumulation in leaves was not observed except in the case
of C. carandas which showed maximum sulphur accumulation and consequent
maximum leaf damage. Some sensitive plants are known to take up a greater
amount of SO2 than resistant ones (Klein et aL, 1978). The other plants such as P.
guajava and P. pterocarpum accumulated higher amounts of S but showed lower
AIR POLLUTION PHYTOTOXICITY 209

- M. indic__.__.£a O. s i s s o o

r = 0.96; p<0.01 r=0.94 ; p < 0.01


y = 1.3300,0.0031x • y=0.7650 t. 0 . 0 0 2 2 X
2

I i i I I 1 _..1 I I ! I ; t 1
>,
t_ 0
"O

- I- 3 - _D. recjia
r =0.94 ;p<0.01
E~
y = 1.7748.0,0029 o x~ _ , , ,e , ~ -
E
2 m

B. s p e c t a b i l i s
r = 0.93 ; p<O.01
_ y = 2.1657.0.0040 x
c 1
ell
t"
O

u 0 I I I 1 I I I I I I I I I I I
K..
3
"
O.
3 P. g u a j a v a C. c a r a n d a s
r =0.84; p<O.01 r = 0.82 ~ p<O.01
t/I y = 1.2441-* 0.0050 x y = 0.9314.0.O035x

' 2
-
O

13.

Ui II •

4; I I I I I I I I I I I I ! 1
"-- 0
O 20 60 100 140 1 8 0 220 2 6 0
3 _P. p t e r o c a rpum,,, SO 2 c o n c e n t r a t i o n (,ugm -31
r :0.93 ; p < 0.01
y=1.1215,0.0042 x

0 -41 I i I t I i I

20 60 100 140 180 220 260


SO 2 c o n c e n t r a t i o n (JJg m -3 )

Fig. 4. Correlations between ambient SO2 and sulphate-sulphure content in plants.


210 JITENDRA PANDEY AND USHA PANDEY

levels of injury. B. spectabilis however, showed lower foliar injury at low levels
of accumulated S. The only exception was D. regia which accumulated minimum
S but showed higher foliar injury compared to B. spectabilis, P. guajava and P.
pterocarpum.
The data presented in Table I show that the annual 24 hourly mean concentrations
of any of the gaseous pollutants occasionally exceed 0.03 ppm and never reached
the value of 0.05 ppm. Fumigation studies have not revealed significant effects
at concentrations < 0.03 ppm for either of the gas (Agrawal, 1982). But the
magnitude of the effects observed in the present study at similar concentrations
was significant. This suggests that the distribution of pollutant peak concentrations
and the coincidence of pollutant mixtures in relation to plant damage may be
crucial in the field studies. Combinations of SO2 and NO2 have been shown to
cause visible injury at considerably lower concentrations than those required for
either gas alone (Wellburn et al., 1981; Bennett et al., 1990). This is especially
important in seasonally dry tropical areas where frequent temporal variations in
the concentration of phytotoxic air pollutants occur (Pandey et al., 1992). Because
most of the available information on air pollution related to the temperate zones,
and it is often dangerous to extrapolate this to the tropics where the climate and
vegetation pattern are quite different, there is need for a wider range of studies in
the tropics to generate a realistic set of environmental criteria, and to provide a
guideline for the design of monitoring systems.
Our study suggests that the air pollution level in Varanasi is detrimental to the
growth of plants and that the unfavourable effects varied depending upon the species
and measured response variables. C. carandas appears to be the most sensitive to
urban air pollution followed by D. regia, D. sissoo, M. indica, P pterocarpum, P.
guajava and B. spectabilis. The sensitive species such as C. carandas may be used
as biomonitors of the air pollution status in tropical cities.

Acknowledgements

The authors are grateful to the Head, CAS in Botany, for laboratory facilities and
to the University Grants Commission for financial support.

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