ARTICLE IN PRESS
Ecotoxicology and Environmental Safety 66 (2007) 258–266
www.elsevier.com/locate/ecoenv
Heavy metal contamination of soil and vegetables in suburban areas
of Varanasi, India
Rajesh Kumar Sharmaa, Madhoolika Agrawala,, Fiona Marshallb
a
Ecology Research Laboratory, Department of Botany, Banaras Hindu University, Varanasi 221005, India
b
SPRU, The Freeman Centre, University of Sussex, Brighton BN1 9QE, UK
Received 7 July 2005; received in revised form 1 November 2005; accepted 23 November 2005
Available online 7 February 2006
Abstract
Heavy metal contamination of soil resulting from wastewater irrigation is a cause of serious concern due to the potential health
impacts of consuming contaminated produce. In this study an assessment is made of the impact of wastewater irrigation on heavy metal
contamination of Beta vulgaris (palak); this is a highly nutritious leafy vegetable that is widely cultivated and consumed in urban India,
particularly by the poor. A field study was conducted at three major sites that were irrigated by either treated or untreated wastewater in
the suburban areas of Varanasi, India according to normal practice. Samples of irrigation water, soil, and the edible portion of the palak
(Beta vulgaris L. var All green H1) were collected monthly during the summer and winter seasons and were analyzed for Cd, Cu, Zn, Pb,
Cr, Mn, and Ni. Heavy metals in irrigation water were below the internationally recommended (WHO) maximum permissible limits set
for agricultural use for all heavy metals except Cd at all the sites. Similarly, the mean heavy metal concentrations in soil were below the
Indian standards for all heavy metals, but the maximum value of Cd recorded during January was higher than the standard. However, in
the edible portion of B. vulgaris, the Cd concentration was higher than the permissible limits of the Indian standard during summer,
whereas Pb and Ni concentrations were higher in both summer and winter seasons. Results of linear regression analysis computed to
assess the relationship between individual heavy metal concentration in the vegetable samples and in soil showed that Zn in soil had a
positive significant relationship with vegetable contamination during winter. Concentrations of Cd, Cu, and Mn in soil and plant showed
significant positive relationships only during summer. Concentration of Cr and Pb during winter season and Zn and Ni during summer
season showed significant negative relationships between soil and plant contamination. The study concludes that the use of treated and
untreated wastewater for irrigation has increased the contamination of Cd, Pb, and Ni in edible portion of vegetables causing potential
health risk in the long term from this practice. The study also points to the fact that adherence to standards for heavy metal
contamination of soil and irrigation water does not ensure safe food.
r 2006 Elsevier Inc. All rights reserved.
Keywords: Wastewater; Irrigation; Heavy metals; Accumulation; Contamination; Beta vulgaris
1. Introduction
It is known that serious systemic health problems can
develop as a result of excessive accumulation of dietary
heavy metals such as Cd, Cr, and Pb in the human body
(Oliver, 1997). Heavy metals are extremely persistent in the
environment; they are nonbiodegradable and nonthermodegradable and thus readily accumulate to toxic levels.
Heavy metals can accumulate in the soil at toxic levels due
Corresponding author. Fax: +91 542 2368156.
E-mail address: madhoo58@yahoo.com (M. Agrawal).
0147-6513/$ - see front matter r 2006 Elsevier Inc. All rights reserved.
doi:10.1016/j.ecoenv.2005.11.007
to the long-term application of wastewater (Bohn et al.,
1985). One important dietary uptake pathway could be
through crops irrigated with contaminated wastewater.
Soils irrigated by wastewater accumulate heavy metals such
as Cd, Zn, Cr, Ni, Pb, and Mn in surface soil. When the
capacity of the soil to retain heavy metals is reduced due to
repeated use of wastewater, soil can release heavy metals
into ground water or soil solution available for plant
uptake.
In suburban areas, the use of industrial or municipal
wastewater is common practice in many parts of the world
(Feigin et al., 1991; Urie, 1986), including India (Singh
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et al., 2004). Access to adequate water for irrigation is a
matter of increasing concern in India. To face the growing
demand for irrigation water, nonconventional resources
are often used. Important sources of heavy metals in
wastewater are urban and industrial effluents, deterioration
of sewerage pipe and treatment works, and the wear of
household plumbing fixtures. Wastewater irrigation is
known to contribute significantly to the heavy metal
content of soils (Mapanda et al., 2005; Nan et al., 2002;
Nyamangara and Mzezewa, 1999; Singh et al., 2004). Other
sources of heavy metal contamination of agricultural soil
are sewage sludge, fertilizers, and pesticides (Alloway and
Ayres, 1993; Ross, 1994).
A number of previous studies from developing countries
have reported heavy metal contamination in wastewater
(Cao and Hu, 2000; Mapanda et al., 2005; Nyamangara
and Mzezewa, 1999; Singh et al., 2004) and wastewaterirrigated soil (Cao and Hu, 2000; Mapanda et al., 2005;
Nan et al., 2002; Nyamangara and Mzezewa, 1999; Singh
et al., 2004). However, there are very few empirical data
from India for heavy metal contamination of soil and
irrigation water and its transfer to vegetable crops.
The present study was carried out around Varanasi,
India, where wastewater has been commonly used for
irrigation of periurban crops for several decades. The
objective of the present report is to quantify spatial and
temporal variations in the total concentrations of Cd, Zn,
Cr, Mn, Cu, Pb, and Ni in irrigation water, soil, and Beta
vulgaris (var. All green H1, a leafy vegetable used for iron
supplement, grown widely in the suburban region of
Varanasi) from sites having long-term use of wastewater
for irrigation of agricultural land. The concentrations in
soil, crops, and water are compared with established safe
limits. This provides a basis for guiding further activities
aimed at preventing excessive exposure of humans through
monitoring and control of irrigation water and/or amelioration of uptake to crops.
2. Materials and methods
The field study took place in the urban fringe area of Varanasi city,
situated in the Eastern Gangetic plain (251180 N latitude and 831 010 E
longitude) of northern India. A reconnaissance survey was conducted in
urban and suburban areas of Varanasi to identify the locations where
wastewater from industries and municipal/domestic sewage is currently
used for irrigation of vegetable crops. Interviews with government
authorities and farmers helped to identify areas where wastewater
irrigation has been common practice for many years, and where the
irrigation water can be clearly sourced to treated or untreated industrial
effluent. Three major vegetables production sites, Dinapur, Shivpur, and
Lohta, were selected (Fig. 1). The soil properties of these sites were
evaluated for pH, conductivity, organic matter, and NO3–N levels. The
most common vegetable grown at all the study sites is palak (Beta vulgaris
L. var. All green H1) throughout the year. Other seasonally produced
vegetables are radishes (Raphanus sativus), tomatoes (Lycopersicum
esculentum), lady’s finger (Abelmoschus esculentus), cauliflower (Brassica
oleracea var. acephala), cabbage (Brassica oleracea var. capitata), and
carrots (Daucus carota). These vegetable crops are mainly produced for
home consumption and sale to residential areas of urban and suburban
region of Varanasi.
259
At Dinapur, a sewage treatment plant (DSTP) of 80 MLD capacity was
installed in 1986, where wastewater containing sewage and effluents
discharged from various industries such as fabric printing, batteries, and
paint, in urban areas of Varanasi is treated before discharge into the
Ganges River. Farmers use this treated wastewater directly for irrigation
via channels off the main outlet towards the fields. At Dinapur, five
microsites were identified as D1, D2, D3, D4, and D5 (Fig. 1). Water
samples were taken from D1 and D4 sites, while water, soil, and vegetable
samples were taken from D2, D3, and D5 sites.
Shivpur is a major industrial and residential area of Varanasi, having
several small-scale industries such as fabric printing and dyeing, food
processing, and electrical cables and paint manufacturing industries.
Industrial effluents, in addition to untreated domestic sewage, flow
through open drains in some areas and are directly used for irrigation of
vegetables. Irrigation is conducted by lifting the water by pumps or by
directly diverting from the drain. Three microsites, S1, S2, and S3, were
identified in Shivpur area (Fig. 1). Water and soil samples were taken from
all the sites, whereas vegetable samples were taken from the S2 site only.
The Lohta site receives untreated sewage and industrial effluents from
more than 100 industries located upstream of the drain at Chandpur,
Maruadih, Lahartara, and Lohta industrial estates. The main industries
are fabric printing, newspaper printing, and various manufacturing
industries including iron gates, window nets, table fans, bicycle tires,
and heavy agricultural equipment. The site also receives treated wastewater from the treatment plant of a large diesel locomotive works that
manufactures diesel engines. Four microsites, L1, L2, L3, and L4, were
identified in Lohta area. Water and soil samples were collected from
all the sites, whereas vegetable samples were collected from the L4 site
only (Fig. 1)
3. Sampling and analysis
Water and soil samples were collected from the sites
monthly from August 2003 to June 2004. However,
vegetable and soil samples were taken randomly across
the field during winter (December–January) and summer
(April–May) seasons. Three replicate polyethylene bottles
(acid-washed) of capacity 100 mL were immersed one by
one at an interval of 15 s in an open drain that was being
used for irrigation purposes and immediately after filling,
1 mL of concentrated HNO3 was added to the water to
avoid microbial utilization of heavy metals. The bottles
were brought back to the laboratory and digestion was
completed within a week. Soil samples were collected in
triplicate from the field receiving wastewater regularly for
irrigation. A monolith of 10 10 15 cm was dug for the
collection of soil. Soil samples were air dried, crushed, and
passed through 2-mm-mesh sieve and stored at ambient
temperature before analysis of soil properties and concentrations of heavy metals.
Vegetable samples were also collected in triplicate (2 kg
each) from the same field simultaneously. Care was taken
to get samples of the same varieties and age group from
different selected sites. Replicate samples were washed
using clean water and then separately oven-dried at 80 1C
till constant weight was achieved. The samples were then
crushed separately through a steel grinder and the crushed
material was passed through 2-mm sieve. The sieved
samples were kept at ambient temperature before analysis.
The soil pH was measured in suspension of 1:5 soil to
water using a glass electrode (Orion, EA, 940 USA). In the
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Fig. 1. Map of study sites in suburban region of Varanasi.
same suspension, conductivity and concentration of
NO3–N were measured using conductivity meter (Systronics, India) and NO3–N electrode (Orion, EA 940 USA),
respectively. The organic carbon was determined using
Walkley and Black’s method (Allison, 1986).
The irrigation water samples (50 mL) were digested with
10 mL of concentrated HNO3 at 80 1C until the solution
became transparent (APHA, 1985). The solution was
filtered through Whatman No. 42 filter paper and the
solution was diluted to 50 mL with distilled water. For soil
and vegetable samples, 0.5 g of dried samples were digested
with 15 mL of HNO3, H2SO4, and HClO4 in 5:1:1 ratio at
80 1C until a transparent solution was obtained (Allen
et al., 1986). The solution was filtered through Whatman
No. 42 filter paper and the solution was diluted to 50 mL
with distilled water.
The concentrations of heavy metal in filtrate of water,
soil, and plant samples were determined with an atomic
absorption spectrophotometer (Perkin-Elmer model 2130,
USA) fitted with a specific lamp of a particular metal using
appropriate drift blanks. Quality control measures were
taken to assess contamination and reliability of data. Blank
and drift standards (Sisco Research Laboratories Pvt. Ltd.,
India) were run after five determinations to calibrate the
instrument. The coefficient of variation of replicate analysis
was determined for different determinations and for
precision of analysis. Variations were found to be less
than 10%. Precision and accuracy of analysis were also
ensured through repeated analysis of samples against
National Institute of Standards and Technology standard
reference material (SRM 1570) for all the heavy metals.
The results were found to be within 72% of the certified
value.
The data were subjected to two-way analysis of variance
(ANOVA). Mean, median, and range was also used to
assess the contamination levels of heavy metals in soil and
irrigation water. Linear regression analysis was used to
determine the relationship between heavy metal concentrations in soil and plant during different seasons.
4. Results
Soil pH and conductivity were higher during summer
than in the winter season at all sites (Table 1). Organic
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261
Table 1
Physicochemical properties of soil collected from different study sites during winter and summer
Study sites
Dinapur
Shivpur
Lohta
Organic matter (g kg1)
Electrical conductivity (mS cm1)
pH
NO3–N (mg kg1)
Summer
Winter
Summer
Winter
Summer
Winter
Summer
Winter
95.8670.60
85.1770.60
94.5770.35
89.5770.75
80.6970.40
89.1470.20
0.3070.00
0.3270.01
0.3770.00
0.2070.00
0.2370.00
0.3670.00
8.5170.00
8.6370.00
8.6370.01
8.0270.02
8.0270.01
8.3670.01
17.1770.32
25.7770.09
34.1070.81
16.0670.06
15.3770.03
28.1070.06
Table 2
Results of two-way ANOVA for heavy metal concentrations in wastewater, soil, and Beta vulgaris L. plants in Varanasi, India
Variations
Wastewater
Site
Month
Sites months
Soil
Site
Month
Sites months
B. vulgaris
Site
Season
Sites seasons
df
Cd
Zn
Cr
Mn
Cu
Pb
Ni
2
5
10
2.527NS
9.335
1.888
10.397
6.894
3.124
10.755
5.476
2.202
1.572NS
6.454
3.358
4.585
4.140
4.015
6.639
98.508
5.047
2.220NS
19.167
5.687
2
5
10
22.201
331.219
86.738
16.595
4.491
4.365
25.894
5.726
10.678
23.212
12.959
18.618
7.817
4.101
3.116
7.671
29.570
15.616
2.771NS
40.623
17.967
2
1
2
32.436
361.920
18.206
208.044
17698.037
585.698
101.992
678.574
162.235
2166.173
5694.45
701.027
333.411
275.490
206.332
234.395
701.548
97.723
55.104
154.574
12.553
Note: NS, not significant; df, degree of freedom.
Po 0.01.
Po 0.001.
Po 0.05.
matter content also showed a similar trend. The value was
highest at Dinapur during summer and lowest at Shivpur
during winter (Table 1). NO3–N content did not vary
significantly between winter and summer at Dinapur, but
was significantly higher at Lohta and Shivpur during the
summer as compared to the winter. The ANOVA showed
significant variations in different soil properties due to sites
and seasons. Site season interaction was also significant
except for organic matter.
Heavy metal concentrations in irrigation water showed
significant variations between sites and months and for the
site month interaction. However, the sitewise variation
was not significant for Cd, Mn, and Ni (Table 2). The mean
concentrations (mg L1) of heavy metals ranged from 0.01
to 0.02 for Cd, 0.09 to 0.23 for Zn, 0.03 to 0.09 for Cr, 0.12
to 0.15 for Mn, 0.04 to 0.11 for Cu, 0.08 to 0.10 for Pb, and
0.03 to 0.05 for Ni (Table 3). Among the heavy metals, Cu
and Pb were higher at Dinapur, which received only treated
wastewater, while sites receiving untreated wastewater
(Lohta and Shivpur), Zn, Cr, and Mn were higher than
at Dinapur (Table 3).
ANOVA tests showed that variations in concentrations
of heavy metals in soil were significant due to site, month,
and site month interaction, except for Ni, which did not
show significant sitewise variation (Table 2). The concentration (mg kg1 dry soil) of heavy metals in soil of the
study sites ranged between 0.55 and 8.85 for Cd, 14.23 and
387.78 for Zn, 13.40 and 679.89 for Cr, 0.36 and 339.36 for
Mn, 2.55 and 203.45 for Cu, 0.46 and 44.50 for Pb, and
2.00 and 34.45 for Ni during different months (Table 4).
The highest mean concentrations were recorded for Mn at
all sites, followed by Zn, Cr, Cu, Pb, and Ni, and the
minimum was observed for Cd. Chromium concentration
was, however, second highest at Lohta. The highest mean
concentrations of Zn, Cr, Cu, and Pb were recorded at
Lohta and then Shivpur, followed by Dinapur. Mn
concentration was in decreasing order from Lohta4Dinapur4Shivpur, but an opposite trend was found for Cd
(Table 4).
The concentrations of Cd, Zn, Cr, and Mn were higher
during summer, whereas Cu, Pb, and Ni were higher
during winter season in B. vulgaris receiving wastewater for
irrigation (Fig. 2). Both sites and seasons individually and
in combination showed significant effects on heavy metal
concentrations in B. vulgaris (Table 2). In terms of absolute
concentration, Mn was highest in B. vulgaris, followed by
Zn, and then Cr, Cu, Pb, and Cd, and the lowest
concentration was observed for Ni during the summer
season. In the winter season, however, the trend from
highest to lowest concentration was Mn then Cu, Pb, Cr,
Zn, Ni, and Cd. The mean concentrations in B. vulgaris
(mg kg1 dry weight) varied from 0.50 to 4.36 for Cd, 2.22
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262
Table 3
Heavy metal concentrations (mg L1) in wastewater used for irrigation in suburban region of Varanasi, India
Suburban area
Cd
Dinapur
(n ¼ 84)
Mean
Median
Range
Lohta
(n ¼ 60)
Mean
Median
Range
Shivpur
(n ¼ 54)
Mean
Median
Range
Cr
Mn
Cu
Pb
Ni
0.09
0.07
0.00-0.056
0.03
0.02
0.00-0.82
0.12
0.09
0.00–1.08
0.11
0.05
0.00–1.54
0.10
0.06
0.00–0.37
0.05
0.03
0.00–0.37
0.17
0.09
0.02–1.25
0.09
0.06
0.00–0.30
0.15
0.14
0.01–0.81
0.06
0.03
0.00–0.49
0.08
0.05
0.00–0.29
0.05
0.04
0.00–0.19
0.01
0.01
0.00–0.03
0.23
0.15
0.01–0.86
0.04
0.04
0.00–0.14
0.15
0.10
0.00–0.67
0.04
0.03
0.00–0.20
0.08
0.05
0.00–0.31
0.03
0.01
0.00–0.14
0.01
2.0
0.1
0.2
0.2
0.5
0.2
0.02
0.01
0.00–0.10
0.02
0.01
ND–0.23
WQ criteria for irrigationa
a
Zn
Source: Pescod (1992).
Table 4
Heavy metal concentration (mg kg1 dry weight) in wastewater irrigated soil of three major vegetable production areas at suburban region of Varanasi,
India
Suburban area
Cd
Zn
Cr
Mn
Cu
Pb
Ni
Dinapur
(n ¼ 54)
Mean
Median
Range
2.80
1.65
0.63–8.30
43.56
33.70
14.23–121.85
30.67
29.75
13.40–98.65
156.96
155.81
0.36–286.15
20.35
19.00
2.55–52.60
15.57
13.23
5.46–35.00
13.37
10.25
2.00–34.45
Lohta
(n ¼ 66)
Mean
Median
Range
2.26
1.50
0.69–6.95
92.57
65.82
17.89–387.78
172.75
70.39
18.05–679.89
191.51
182.88
40.20–339.36
42.03
20.35
5.45–203.45
19.51
15.53
6.50–38.90
14.52
11.55
2.45–32.30
Shivpur
(n ¼ 53)
Mean
Median
Range
2.69
1.45
0.55–8.85
87.89
65.89
20.75–223.56
79.27
29.15
13.55–500.00
145.74
159.56
21.75–256.80
33.50
21.30
8.90–107.10
18.35
14.96
0.46–44.50
15.61
11.23
4.03–32.25
3–6
300–600
n/a
n/a
135–270
250–500
75–150
0.01–0.7
10–300
5–3000
100–4000
2–100
2–200
10–1000
Permissible limits of
indian standarda
Range of heavy metal
concentrations in
uncontaminated soilb
Note: n/a, not available.
a
Source: Awashthi (2000).
b
Source: Bowen (1966).
to 41.51 for Zn, 5.37 to 27.83 for Cr, 7.53 to 117.94 for Mn.
10.95 to 28.58 for Cu, 3.09 to 15.74 for Pb, and 1.81 to 7.57
for Ni (Fig. 2).
Linear regression analysis was used to evaluate the
relationship between individual heavy metal concentration
in soil and in the edible leafy portion of B. vulgaris. The
trend of metal concentrations in the plants would be a
function of trace metal content in the soil and their
absorption in plant tissues. The relationships between the
individual heavy metals in soil and B. vulgaris are presented
in Figs. 3 and 4. Significant positive correlations were
found for Zn and Cu during winter and Cd, Cr, and Mn
during summer season. Negative significant correlations
were, however, found for Cr and Pb during the winter
season and Zn and Ni during the summer season. The
relationships for Cr, Mn, and Ni during winter season and
Cu and Pb during summer season were not significant
(Figs. 3 and 4).
5. Discussion
The results of the field study showed that continuous
application of treated and untreated wastewater led to
elevated levels of heavy metals in the soil and edible
portion of B. vulgaris. The concentrations of all the heavy
metals showed spatial and temporal variations, which may
be ascribed to the variations in heavy metal sources and the
quantity of heavy metals discharged through the sewage
and effluents in irrigation water.
The mean concentrations of Cd, Cr, Ni, and Mn in
treated wastewater of Dinapur recorded during the present
study were similar to those in the earlier report of Singh et
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263
Fig. 2. Heavy metal (Cd, Zn, Cr, Mn, Cu, Pb, and Ni) concentrations
(mg kg1 dry weight) in Beta vulgaris L. var. all green H1 during summer
and winter seasons at Dinapur, Shivpur, and Lohta sites.
al. (2004). However, the mean concentrations of Pb and Cu
were higher and that of Zn was lower than the reported
values of Singh et al. (2004). The comparison of mean
heavy metal concentrations in treated and untreated
wastewater from the data of other countries suggests that
the values of the present study were manyfold lower than
the levels observed at Harare, Zimbabwe (Mapanda et al.,
2005; Nyamangara and Mzezewa, 1999), but higher than
those recorded at Wodonga and Canberra, Australia
(Smith et al., 1996). Cao and Hu (2000) in China also
reported manyfold higher Cu concentration (12 mg L1) in
wastewater than the present study value (0.11 mg L1). The
metal concentrations in wastewater used for irrigation are
above the recommended maximum value for Cd at Lohta
and Dinapur sites (Table 3). Cr concentration was close to
the permissible level at Lohta only (Table 3), but lower at
the other sites. The elevated levels of Cd in irrigation water
at Dinapur and Lohta may be due to effluents discharged
from various heavy-metal-based industries such as the
fabric printing (Cu, Cd, Zn, Ni, and Cr), battery (Pb, Mn,
As, and Cd), and paint industries (Pb, Cd, Zn, Cu, and Pb).
The higher Cr content at Lohta site is due to effluent
discharged from more than 50 industries where chromium
and its compounds are used as color and pigment, plating,
and alloys for metal surface treatment and as catalysts,
situated in the catchment area of drains discharging
Fig. 3. Relationships between heavy metal (Cd, Zn, Cr, and Mn)
concentrations (mg kg1 dry weight) in Beta vulgaris L. var. all green
H1 and soil during summer and winter seasons. P ¼ concentration of
heavy metal in plant; S ¼ concentration of heavy metal in soil; NS ¼ not
significant.
wastewater at Lohta. The diesel locomotive works, where
chromium plating is carried out on a large scale, also
discharges water into the drain after treatment. Significant
positive correlations were observed between Pb and Ni
(R2 ¼ 0:43; Po0:01), Pb and Cr (R2 ¼ 0:39; Po0:01), Pb
and Zn (R2 ¼ 0:27; Po0:05), Pb and Cd (R2 ¼ 0:65;
Po0:01), Ni and Cd (R2 ¼ 0:51; Po0:01), and Ni and
Zn (R2 ¼ 0:29; Po0:05) at Shivpur and between Pb and Ni
(R2 ¼ 0:32; Po0:05), Pb and Cr (R2 ¼ 0:47; Po0:01), Pb
and Zn (R2 ¼ 0:43; Po0:01), and Zn and Cr (R2 ¼ 0:56;
Po0:01) at Lohta, suggesting that these heavy metals in
irrigation water originate from common sources. At
Dinapur no strong correlation was found except between
Cd and Cu (R2 ¼ 0:43; Po0:01) and between Cd and Pb
(R2 ¼ 0:23; Po0:05), suggesting that Cd, Cu, and Pb are
more common in sewage water, which also receives
effluents from some small-scale industries. It is evident
that treatment of wastewater is not helpful in elimination
of heavy metals at Dinapur. The range of concentrations of
Zn, Cu, Pb, and Ni in soil observed during the present
study was below the official Indian standard (Awashthi,
2000). The maximum observed value of Cd was higher than
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Fig. 4. Relationships between heavy metal (Cu, Pb, and Ni) concentrations (mg kg1 dry weight) in Beta vulgaris L. var. all green H1 and soil
during summer and winter seasons. P ¼ concentration of heavy metal in
plant; S ¼ concentration of heavy metal in soil; NS ¼ not significant.
the Indian standard during January. Cd, Zn, and Cu
concentrations were, however, higher than the values
reported for typical uncontaminated soil (Bowen, 1966).
The comparison of the data from the present study with
earlier findings of Singh et al. (2004) at Dinapur, Varanasi
suggested that the range of concentrations of Cd and Cr in
soil was higher; however, Zn, Mn, Cu, Pb, and Ni were
lower than the previously reported range. This variation
may be ascribed to the differences in sites, frequency of soil
collection, and crops under cultivation between the two
studies.
There were significant variations in the concentrations of
heavy metals in soil between sites and seasons. This trend
may be correlated with the soil properties that influence
heavy metal availability at different sites. The higher values
of soil pH, conductivity, organic matter, and NO3–N
content observed during summer as compared to winter
may be ascribed to a higher frequency of irrigation during
summer associated with high temperature and low soil
moisture availability. Higher soil pH during summer may
have maintained higher concentrations of heavy metals in
the topsoil layer owing to higher evaporation. The
concentration of Cu (2.55–203.45 mg kg1) in soil observed
in the present study is higher than concentrations reported
in Zimbabwe by Tandi et al. (2004) (2.50–133.3 mg kg1)
and Mapanda et al. (2005) (7–145 mg kg1). The concentrations of Cd, Cr, Ni, and Zn in soil observed during the
present study were also higher than those reported at
Zimbabwe (Mapanda et al., 2005). The relatively low heavy
metal contamination in soil as compared with water and
crops, and a lack of significant correlations between the
concentrations of heavy metals in soil and wastewater at
various sites, may be ascribed to the continuous uptake of
heavy metals by plants during their growth and development. This is supported by the data of heavy metal
concentrations in the edible portion of B. vulgaris.
Significant positive correlations were observed between
the concentration of Zn and Cu in soil and plant tissue
during winter and Cd, Cr, and Mn in soil and plant tissue
during summer season.
Absorption and accumulation of heavy metals in plant
tissue depend upon many factors, which include temperature, moisture, organic matter, pH, and nutrient availability. Soil properties influencing heavy metal availability
varied significantly between the sites.
The Dinapur and Lohta sites showed higher organic
matter content than the Shivpur site. The Dinapur and
Lohta sites also showed similar contamination levels for
Cd, Zn, and Mn during the summer, which may be at least
partially explained by the high organic matter. Organic
complexing molecules of low molecular weight (LMW)
serve as carriers of micronutrients. LMW has been shown
to increase Cd uptake (Chen and Aviad, 1990), whereas the
presence of organic matter has been reported to increase
the uptake of Zn in the wheat plant (Rupa et al., 2003).
The pH of the soil was close to 8 at all sites. The alkaline
range of soil (48.0) is known to restrict the mobilization of
heavy metals, thus reducing their uptake. However, the
high nutrient input from irrigation water at these sites
could result in relatively high growth rates and relatively
high uptake of heavy metals as a result. The field data
support this argument in that a higher yield of B. vulgaris
was recorded at all three sites that were irrigated with
wastewater as compared to the area receiving uncontaminated irrigation water.
The NO3–N content was similar at all sites, while the
concentration in summer was consistently higher than in
winter. Long-term application of N is known to be
associated with an increase in plant uptake and bioavailability of heavy metals (Nambiar and Ghosh, 1984). In the
present study it seems that many soil factors such as pH,
organic matter, nitrogen bioavailability, soil moisture, and
temperature have interacted to impact on uptake.
The uptake and accumulation of Cd, Zn, Cr, and Mn in
B. vulgaris were higher during the summer season, whereas
Cu, Ni, and Pb accumulated more during the winter
season. It may be expected that during the summer season
the relatively high decomposition rate of organic matter is
likely to release heavy metals in soil solution for possible
uptake by plants (McGrath et al., 1994). The higher uptake
of heavy metals such as Cd, Zn, Cr, and Mn during the
summer season may be due to high transpiration rates as
compared to the winter season due to high ambient
temperature and low humidity (Ingwersen and Streck,
2005). From Fig. 2 it can be predicted that LMW organic
molecules act as a good carrier for Cd, Cr, Mn, and Zn but
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a poor carrier for Cu, Pb, and Ni during the summer
season. During the winter season the concentrations of Cu,
Ni, and Pb were higher in irrigation water as compared to
summer season, which may have had a direct impact on
uptake. For Zn and Mn the present results agreed with the
observation of Gadallah (1994) for sunflower that during
the summer season, concentrations of Zn and Mn were
higher as compared to other seasons.
The mean concentrations of all the heavy metals in B.
vulgaris at Dinapur were considerably higher than the
values reported by Singh et al. (2004) in vegetable crops
from the same area. This may be ascribed to the
considerable variation in heavy metal uptake by different
types of vegetables. In the present study, samples of B.
vulgaris only were collected, whereas Singh et al. (2004)
analyzed a range of vegetable crops having different heavy
metal absorption potentials. In the present study plants
were harvested at maturity; no such information is available
for the study of Singh et al. (2004), but if harvest occurred
earlier, clearly less heavy metal absorption would have
taken place. The comparison of mean values of heavy
metals recorded in the plant material during the present
study with Indian permissible limits (Awashthi, 2000)
showed that Pb and Ni concentrations were higher both
during summer and winter seasons, however, Cd was higher
only in the summer season at all the sites during 2004. Mean
concentrations of Zn, Cu, and Mn were below the
permissible limits at all the sites. Cr concentration at Lohta
was also higher than the permissible limit during summer,
whereas at Dinapur it was approaching the limit. This study
clearly showed that consumption of B. vulgaris by the urban
and suburban population might pose health hazards due to
Cd, Pb, and Ni contamination. Significant negative
correlations were observed between heavy metal concentrations in soil and plant for Cr and Pb during winter and Zn
and Ni during summer. This response clearly indicates
antagonism between the metals during absorption.
The results of linear regression analysis further showed
that during the winter season the interaction of Cd and Zn
was synergistic. Similar synergism has been reported by
Hinsely et al. (1984) in the sewage-sludge-amended corn
plants. Nan et al. (2002) also showed synergism of Cd and
Zn absorption in fields irrigated by wastewater. In summer,
however, Cd and Zn interacted antagonistically, as
concentrations of Cd in soil and plant tissue were positively
correlated and for Zn negatively correlated (Fig. 3). During
summer, presumably due to moisture limitation and high
temperature, Cd interfered with the Zn uptake. This trend
agreed with a previous report of Zhou et al. (1994), where
interaction of Cd and Zn resulted in reduction of Zn
uptake with consequent increase of Cd uptake and
bioaccumulation in rice plants grown in pots.
6. Conclusion
The study concludes that irrigation by treated or
untreated wastewater has increased the heavy metal
265
concentrations in soil and plants of receiving area.
Cadmium concentration in irrigation water was found
above the permissible limit set by WHO for irrigation of
agricultural land at Dinapur and Lohta sites. Heavy metal
concentrations in plants show significant spatial and
temporal variations. Cd, Pb, and Ni were above the Indian
permissible limits, while Zn and Cu were within limits in
the edible portion of B. vulgaris. Cr concentration was
above the permissible limit at Lohta site, receiving effluents
from Cr based industries. The results of the present study
further suggest that Zn, Cr, and Mn concentrations in
plants are influenced by seasonal variations, whereas Cd,
Cu, Pb, and Ni did not show any change in uptake pattern
due to seasonal variations. The consumption of Cd, Pb,
and Ni-contaminated portion of B. vulgaris plants by
suburban people of Varanasi may pose health hazards. An
important issue is that the contamination levels were
frequently higher than permissible limits in the plant tissue,
at the same sites as water and soil samples that comply with
established safe standards. This has important implications
for policy in that programmes aimed at monitoring and
controlling heavy metal concentrations in irrigation water
sources will not necessarily result in acceptable levels in
vegetables. Policies and programs need to be adapted so
that local edaphic conditions and agricultural practices are
taken into account, and appropriate local measures
developed for ameliorating heavy metal uptake by crops
for a given set of local conditions. These measures need to
be regularly reviewed to take into account factors such as
the accumulation of heavy metals in the topsoil over time.
Acknowledgments
The authors gratefully acknowledge that the present
research work is an output of a collaborative research
project entitled ‘‘Contaminated irrigation water and food
safety for the urban and peri-urban poor: Appropriate
measures for monitoring and control from field research in
India and Zambia,’’ which is funded by Department for
International Development (DFID), United Kingdom, for
the benefit of developing countries (R8160). The present
study work was not conducted on human or experimental
animals where national or institutional guidelines are used
for the protection of human subjects and animal welfare. In
the present study, national and international norms of
heavy metals in irrigation water, soil, and vegetables are
used to compare contamination levels found with standards prescribed for the protection of human health.
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