Microchemical Journal 99 (2011) 6775

Contents lists available at ScienceDirect

Microchemical Journal
j o u r n a l h o m e p a g e : w w w. e l s ev i e r. c o m / l o c a t e / m i c r o c

Heavy metal concentrations in soil and wild plants growing around PbZn sulde
terrain in the Kohistan region, northern Pakistan
Said Muhammad a,, M. Tahir Shah a, Sardar Khan b,
a
b

National Center of Excellence in Geology, University of Peshawar, Pakistan

Department of Environmental Sciences, University of Peshawar, Pakistan

a r t i c l e

i n f o

Article history:
Received 19 March 2011
Accepted 26 March 2011
Available online 2 April 2011
Keywords:
Heavy metals
Soil
Wild plants
PbZn terrain
Hyper accumulator
Pollution load index

a b s t r a c t
This study investigates the soil and wild plants of the PbZn sulde bearing mineralized zone of Indian plate
(IP) in the Pazang and Lahor sites, Kohistan region, northern Pakistan. Soil and plants were analyzed for major
cations (Na, K, Ca, Mg, Fe, Mn) and heavy metals (Pb, Zn, Cd, Cu, Cr, Ni, Co) concentrations by using atomic
absorption spectrometer. Metal concentrations were used to quantify pollution contamination factors such as
pollution load index (PLI) and plant bioaccumulation in soil and plants developed in mineralized zones in the
Lahor and Pazang sites and an unmineralized zone (reference sites) of the Besham area. Soil and plants of the
mineralized zone and surrounding areas have higher heavy metal (HM) contamination (P b 0.01) as compared
to the reference site, which can be attributed to the dispersion of metals due to mining. Furthermore, in
mineralized zones, the Lahor site was more contaminated than the Pazang site. This high HM contamination
may pose potential threats to local communities of Kohistan region. The results also showed that plant species
(Plectranthus rugosus, Rumex hastatus, Fimbristylis dichotoma, Heteropogon conturtus and Myrsine Africana)
were the best HM accumulators.
2011 Elsevier B.V. All rights reserved.

1. Introduction
The contamination of soil ecosystem with heavy metals (HM) is
considered as global environmental issue. These HM have both
natural sources like weathering/erosion of parent rocks and ores
deposits and anthropogenic sources like mining, smelting, energy,
electroplating, fuel production, power transmission, intensive agriculture, waste water irrigation; sludge dumping and dust [15]. In
past century, anthropogenic activity especially mining and smelting
have concentrated major cations like sodium (Na), potassium (K),
calcium (Ca), magnesium (Mg), iron (Fe) and manganese (Mn); and
HM likes chromium (Cr), cobalt (Co), copper (Cu), lead (Pb), zinc (Zn)
and cadmium (Cd). Mining activities are producing waste tailings that
pose serious environmental impacts to aquatic and terrestrial
ecosystems. In most mining activities, these waste tailings are left
without proper management [6,7]. Improper management results in
oxidation of sulde mineral, resulting in metalliferous acidic mine
drainage leads to leaching of concentrated metallic ions like Mn, Fe Cu,
Pb and Zn [8]. In soil ecosystems, the toxicity and mobility of these
metals depend on various factors like total concentration of metals,
specic chemical form, metal binding state and properties. These are
also controlled by environmental factors like pH, electrical conductivity (EC) and soil organic matter (SOM) [9].

Heavy metals were considered as highly toxic environmental

pollutants to ecosystems and human health [1012]. Different
methods and techniques have been used to address HM contaminated
soil and tailing deposits, [6,13]. However, phytoremediation with
native plants is the best and most cost-effective technique for
reclaiming HM contaminated land [1419]. Presently, more than
400 plant species have been identied as natural hyper accumulators
of HM and useful for phytoremediation [20]. These include such plants
that can accumulate exceptionally high quantities of one or more
kinds of HM [21].
Like other developing countries, open dumping of mining waste
and tailing deposits is a common practice in Pakistan. PbZn sulde
deposits have been identied and reported in the Lahor, Pazang sites
and the Besham area by Fletcher et al. [22] and Shah [23]. Sarhad
development authority (SDA) started mining PbZn in 1983 and their
waste/tailing deposits were dumped openly in the area surrounding
the mine. Therefore, this study aimed to quantify the HM contamination factor (CF) and pollution load index (PLI) in soil; bioaccumulation factor (BF) and identify native hyperaccomulator plant species in
the target area.
2. Materials and methods
2.1. Study area

Corresponding authors. Tel.: +92 91 9218182; fax: +92 91 9218183.

E-mail addresses: saidmuhammad1@gmail.com (S. Muhammad),
sardar.khan2008@yahoo.com (S. Khan).
0026-265X/$ see front matter 2011 Elsevier B.V. All rights reserved.
doi:10.1016/j.microc.2011.03.012

The target area, Pazang and Lahor sites in the Besham area,
Kohistan region northern-Pakistan is located about 250 km north of

68

S. Muhammad et al. / Microchemical Journal 99 (2011) 6775

Islamabad (the capital of Pakistan). It lies in between 34o5035o06 N

latitudes and 72437302 E longitudes, covering approximately a
total area of 1800 km with b0.25 Million population. Although, the
mountains have sporadic agriculture land but still it is the main
profession of residents. Indus river and its tributaries (Dubair and
Khan Khwars) are the main irrigation sources in the area (Fig. 1).
Region is warm in summer (32.5 C) except high altitude area and
very cold in winter ( 2.4 C) receiving an annual precipitation of
1415.9 mm [12,24].
The study area is part of the Kohistan region in northern Pakistan.
This region is composed of the rocks of three different entities such as
the Kohistan island arc (KIA), Indus suture zone (ISZ) and Indian plate
(IP). The ISZ is considered as the contact zone between KIA in the
north and IP in the south [25]. Rocks of these different lithologies vary
in composition from the mac and ultramac igneous rocks belonging
to KIA and ISZ to metasedimentary rocks of IP (Fig. 1). This region has
various types of metallic and non-metalic mineral deposits. According
to Fletcher et al. [22] and Shah [23], stratiform massive PbZn sulde
deposits were present in the metasedimentary sequence (ortho and
paragneises and calc-silicates rocks) of IP at the Pazang and Lahor
areas in vicinity of the Besham, main town of the Kohistan region. Pb
Zn sulde contains mainly sphalerite, galena and pyrite with lesser
amount of chalcopyrite and pyrrhotite.
2.2. Sampling
In the study area, different native wild plant species were
randomly collected from the PbZn sulde horizon/mineralized

sites (mining area) and surrounding area (Table 1). Plants (herbs
and shrubs) up to a height of b1 m were uprooted and stored in
polythene bags. Soil sample of 1 kg was collected up to a depth of
30 cm from the base of each uprooted plant. In eld, samples were
cleaned from stones and twigs, packed in polyethylene bags and
properly marked. Unmineralized zone (Reference site) soil and plant
samples were also collected about 10 km away from the mineralized
sites. Herbarium sheet of all different plant species was prepared,
identied and taxonomically classied with help of taxonomist in the
Botany Department, University of Peshawar, Pakistan.
2.3. Sample preparation and analysis
Soil samples were air dried, homogenized, sieved through 2 mm
mesh and stored in polyethylene bags at room temperature. Physical
parameters like pH and EC were measured in mixture of soil and
double distilled water (DDW) with ratio of 1:2.5 (w/v) according to
the procedure adopted form Das and Maiti [26], while SOM was
measured according to the method adopted from Konen et al. [27]. For
HM determination, soil samples were ground in ball mill to ner than
200 mesh size. About 0.5 g oven dried soil was digested in the Teon
beaker with a mixture of 40 ml hydrouoric acid (HF) and 10 ml
hydrochloric acid (HCl) at 130140 C for complete digestion. When
acids were completely evaporated, then 1:1 HCl added and the
solution was diluted to 100 ml with DDW [7].
Plant samples were washed with DDW, oven dried at 70 C and
powdered with electric grinder. Accurately, 2.0 g of plant samples
were taken in the Pyrex beaker and digested with mixture of acids

Fig. 1. Location map of the study area.

Modied from Dipietro et al., [25].

S. Muhammad et al. / Microchemical Journal 99 (2011) 6775

Table 1
Selected plant species along with their family and local names in the study area.
S. no

Species scientic name

Abbreviations

Family name

Local name

1.
2.
3.
4.
5.
6.
7.
8.
9.
10.

Plectranthus rugosus
Rumex hastatus
Fimbristylis dichotoma
Olea ferruginea
Heteropogon conturtus
Myrsine africana
Indigofera gerardiana
Daphne mucronata
Debregeasia salicifolia
Berberis lycium

P. rugosus
R. hastatus
F. dichotoma
O. ferruginea
H. conturtus
M. africana
I. gerardiana
D. mucronata
D. salicifolia
B. lycium

Labiatae
Polygonaceae
Cyperaceae
Oleaceae
Poaceae
Myrsinaceae
Papilionaceae
Thymeleaceae
Urticaceae
Berberidaceae

Sparakay
Tharukay
Barwaza
Khunah
Kabal
Ghanna
Ghwaraija
Naighonay
Azlai
Ziar largay

[nitric acid (HNO3), perchloric acid (HClO4) and aqua regia]; and
dilute the extract to 50 ml with DDW, according to the digestion
method adopted from Ryan et al. [28]. Digested soil and plant samples
were analyzed for major cations and HM by using atomic absorption
spectrometer (Perkin Elmer, AAS-PEA-700).
2.4. Data precision and accuracy
For data precision and accuracy, a reagent blank and standard
reference soil and plant materials were included in the digestion and
subsequent analysis. Each sample was digested and analyzed in
triplicate and mean value was taken for further interpretation.
Reproducibility of the triplicate samples was found within 95%
condence level. To check accuracy of AAS, the standard of all
thirteen metals were prepared by dilution of 1000 mg/l certied
standards solutions Fluka Kamica (Buchs, Switzerland) of corresponding metal ions with DDW and analyzed after every 10 samples.
Chemicals and regents were of analytical grade.
2.5. Pollution quantication
2.5.1. Contamination factor (CF)
Contamination factor ratio was obtained by using the equation
adopted from Rashed [7] and Khan et al. [29].
CF = Cheavy metal = Cbackground
Where, [C] heavy metal and [C] background means the concentrations of major cations and HM in the mineralized site (contaminated site) and the unmineralized site (reference site), respectively.
2.5.2. Pollution load index (PLI)
For entire sampling sites, PLI has been determined as nth root of the
product of the n CF [30]:
1=n

PLI = CF1 x CF2 x CF3 x CFn

In the study area, PLI provides a simple comparative means of

major cations and HM level.

69

3. Results and discussion

Many studies related with the terrestrial ecosystems have
reported anomalously high concentrations of HM in surrounding
areas of the ore deposits and mines [3,6,7]. Furthermore, abandoned
mining sites are signicant sources of HM contamination in soil. Their
severity of impact depends on the age of waste, the geological and
geographical settings, the technique used; and the prevailing
chemical conditions. These HM could cause soil substrate contamination, soil deterioration, increase in nutritional deciencies, destruction of the ecological landscape and tremendous decrease in biological
diversity [7,31].
3.1. Physical properties of soil
In the Pazang site, pH, EC and SOM ranged from 3.3 to 7.1, 224 to
611 S/cm and 1.38.4% in the contaminated site and from 5.3 to 7.5,
129 to 207 S/cm and 2.57.1% in the reference site, respectively
(Table 2). Similarly, in the Lahor site, pH, EC and SOM ranged from 3.5
to 7.7, 116 to 808 S/cm and 1.812.4% in the contaminated site
from 5.9 to 6.4, 57 to 118 S/cm and 2.36.0% in the reference site,
respectively (Table 2). Contaminated (Pazang and Lahor) sites
samples have caused lowering of pH due the existence of PbZn
sulde mineralization that caused increase in mobility of HM, which
resulted in high EC values as compared to the reference site. In the
study area, high SOM in the Lahor site may be attributed due to dense
pines species vegetation that further lowered the pH.
3.2. Major cations and heavy metals
3.2.1. Pazang site
Table 3 summarizes the major cations and HM concentrations in
soil and plant samples collected from the contaminated (Pazang area)
and reference site. Na, K, Ca, Mg, Fe, Mn, Cr, Ni, Co, Cu, Pb, Zn
and Cd concentrations in soil ranged from 2555 to 8345 mg/Kg, 8405
to 14300 mg/Kg, 3715 to 14755 mg/Kg, 4415 to 11020 mg/Kg,
12715 to 63815 mg/Kg, 465 to 5735 mg/Kg, 64 to 318 mg/Kg, 42 to
756 mg/Kg, 91 to 169 mg/Kg, 31 to 412 mg/Kg, 12 to 1337 mg/Kg,
95 to 1072 mg/Kg and 0.6 to 5.0 mg/Kg, respectively (Table 3). These
metal concentrations were found in the order of Fe N K N Ca N Mg N
Na N Mn N Zn N Cu N Cr N Co N Pb N Ni N Cd. Similarly, Na, K, Ca, Mg, Fe, Mn,
Cr, Ni, Co, Cu, Pb, Zn and Cd concentrations in plants ranged from 19
to 225 mg/Kg, 2515 to 12595 mg/Kg, 1602 to 24687 mg/Kg, 898
to 5487 mg/Kg, 187 to 5054 mg/Kg, 22 to 857 mg/Kg, 6 to 27 mg/Kg, 10
to 44 mg/Kg, 1 to 15 mg/Kg, 4 to 66 mg/Kg, 8 to 31 mg/Kg, 7 to 328 mg/
Kg and 0.2 to 2.1 mg/Kg, respectively (Table 3). Metal concentrations
in plants were found in the order of Ca N Na N Mg N Fe N Mn N K N Zn N
Cr N Ni N Cu N Pb N Co N Cd. High concentrations of these metals in soil

Table 2
Physical characteristics of soil in the Pazang, Lahor and Reference sites.
Pazang site

2.5.3. Plants bioaccumulation factor (BF)

Bioaccumulation factor is determined by using the equation
adopted from Rashed [7]:
BF = CHM in plant =CHM in soil

Results of chemical analysis like ranges, mean and standard

deviation were analyzed by using Excel 2007 (Microsoft Ofce) and
statistical analysis like one-way ANOVA, correlation and cluster
analysis (CA) by using statistical software SPSS version 17.

Statistics

Reference

Contaminated

Reference

Contaminated

pH

Range
Mean
Std deva
Range
Mean
Std dev
Range
Mean
Std dev

5.37.5
6.7
0.7
129207
140
141
2.57.1
4.6
1.8

3.37.1
5.6
1.3
224669
298
78
1.38.4
4.9
2.0

5.96.4
6.2
0.2
57118
77
23
2.36.0
4.2
1.6

3.57.7
6.3
1.2
116808
351
153
1.812.4
5.3
2.5

ECb cm/cm

2.6. Statistical analysis

SOMc%

Standard deviation.
Electrical conductivity.
c
Soil organic matter.
b

Lahor site

Properties

70

S. Muhammad et al. / Microchemical Journal 99 (2011) 6775

Table 3
Major cations and HM concentrations (mg/Kg) in soil and plant, contamination factor (CF) and pollution load index (PLI) of the study area.
Soil samples

Plant samples

Reference site
Metals

Range

Contaminated site
Mean

Std dev

2548
2805
4697
4179
6846
218
63
112
35
28
22
46
1.2

25558345
840514300
371514755
441511020
1271563815
4655735
64318
42756
91169
31412
121337
951072
0.65.0

4645
12146
9792
7153
25080
2437
99
146
117
193
117
361
2.0

1709
1611
2650
1389
10350
1186
48
132
18
91
251
287
1.0

1033
946
4452
1852
3363
328
8
12
6
20
24
113
0.5

4145575
249012915
583024915
321011945
1725051750
26615420
18324
92850
45136
111345
510300
21329755
0.4184

2600
8036
13124
6787
26960
5779
172
439
105
205
1753
5123
20

1155
2814
4698
2064
9179
4447
120
333
24
65
2521
7488
38

Std dev

5158
6303
6111
8223
14645
471
158
252
131
68
51
115
1.3

Lahor site
Na
770010405
K
767010280
Ca
322014995
Mg
32508415
Fe
584013905
Mn
2691048
Ni
2648
Cr
123154
Co
7089
Cu
2579
Pb
2397
Zn
86410
Cd
1.83.4
PLI

9173
8744
8993
5506
10958
636
35
139
78
48
70
202
2.8

Reference site

Range

Mean

Pazang site
Na
6508085
K
6009210
Ca
44713675
Mg
151514515
Fe
120023225
Mn
14702
Ni
51253
Cr
60409
Co
58168
Cu
23114
Pb
2381
Zn
24179
Cd
0.43.2
PLIe

Standard deviation,

Contamination factor, c Electrical conductivity,

CF

Contaminated site

Range

Mean

Std dev

Range

Mean

Std dev

0.9
1.9
1.6
0.9
1.7
5.2
0.6
0.6
0.9
2.8
2.3
3.1
1.5
1.51

66203
327117175
316721166
12027946
3811790
21831
618
921
310
313
613
548
0.41.0

107
9788
10744
3430
675
177
9
13
5
9
9
18
0.6

41
4179
6000
2292
452
257
5
5
2
3
2
15
0.2

19225
251512595
160224687
8985487
1875054
22858
627
1044
115
466
831
7328
0.22.1

102
7254
11647
2782
739
196
10
17
6
15
14
76
0.9

40
3382
6033
1356
857
202
5
6
4
15
5
80
0.4

0.3
0.9
1.5
1.2
2.5
9.1
5.0
3.2
1.3
4.3
24.9
25.4
7.1
3.25

30204
189117175
130812577
11855377
3061790
30152
3177
531
38
313
812
869
0.41.6

75
5674
7041
2345
732
79
9
12
5
7
10
24
0.7

51
4291
4170
1505
437
42
5
8
2
3
2
17
0.4

26146
170013791
369422321
8523794
1101461
32714
411
1016
526
524
699
161998
0.36.1

65
6277
9966
1780
446
210
7
12
8
11
28
293
1.3

36
2704
4615
681
347
188
2
1
4
4
25
464
1.3

Soil organic matter e Pollution load index.

Table 4
Major cations and HM concentrations and bioaccumulation factor of in plant species.
Metals
Pazang site
P. rugosus (n = 8)
R. hastatus (n = 5)
I. gerardiana (n = 4)
D. mucronata (n = 7)
F. dichotoma (n = 4)
O. ferruginea (n = 3)
D. salicifolia (n = 3)

Lahor site
P. rugosus (n = 8)
B. lycium (n = 5)
O. ferruginea (n = 3)
R. hastatus (n = 2)
F. dichotoma (n = 3)
H. conturtus (n = 3)
M. africana (n = 2)
a
b

Mean
BFb
Mean
BF
Mean
BF
Mean
BF
Mean
BF
Mean
BF
Mean
BF

Mean
BF
Mean
BF
Mean
BF
Mean
BF
Mean
BF
Mean
BF
Mean
BF

Bioaccumulation (mg/Kg).
Bioaccumulation factor.

bioaccoa
bioacco
bioacco
bioacco
bioacco
bioacco
bioacco

bioacco
bioacco
bioacco
bioacco
bioacco
bioacco
bioacco

Na

Ca

Mg

Fe

Mn

Ni

Cr

111
0.02
143
0.03
83
0.02
889
0.01
94
0.03
56
0.01
101
0.01

8850
0.77
11365
0.9
2699
0.22
5448
0.45
6297
0.53
4774
0.36
10423
0.79

11023
2.37
9321
1.1
20753
1.66
11353
1.28
3026
0.27
16344
1.67
15296
1.82

3099
0.42
4127
0.66
2791
0.4
1862
0.27
1377
0.16
2967
0.41
3982
0.55

1190
0.04
571
0.02
904
0.03
479
0.03
614
0.02
396
0.02
529
0.03

141
0.05
585
0.36
118
0.04
122
0.06
130
0.04
130
0.05
53
0.02

12
0.11
7
0.07
10
0.03
9
0.06
14
0.13
9
0.09
8
0.08

20
0.24
17
0.2
15
0.09
14
0.11
15
0.16
16
0.16
18
0.17

71
0.03
40
0.02
55
0.02
81
0.03
46
0.02
88
0.03
50
0.02

6971
0.97
5718
0.68
4980
0.64
10824
1.16
4096
0.47
5130
0.52
5424
4.85

12112
0.86
8708
0.83
9407
0.63
5620
0.37
6278
0.59
21013
2.31
7418
0.43

1670
0.23
1723
0.33
1784
0.33
3555
0.46
1682
0.25
886
0.11
1456
0.12

496
0.02
325
0.01
377
0.01
348
0.01
912
0.04
102
0
121
0

124
0.02
287
0.05
236
0.03
156
0.07
381
0.06
131
0.02
179
0.02

8
0.01
7
0.02
7
0.01
5
0.01
7
0.02
8
0.08
8
0.03

11
0.07
12
0.09
12
0.2
12
0.05
13
0.09
12
0.04
13
0.1

Co

Cu

Pb

Zn

Cd

7
0.06
6
0.05
8
0.06
7
0.06
5
0.04
6
0.05
1
0.01

11
0.05
45
0.22
14
0.05
8
0.05
9
0.03
8
0.06
8
0.05

14
0.21
12
0.16
16
0.99
14
0.16
16
0.04
12
0.11
10
0.74

84
0.22
132
0.26
59
0.19
88
0.29
46
0.14
18
0.05
22
0.04

0.6
0.25
1.3
0.9
0.8
0.64
1
0.53
0.6
0.59
0.6
0.42
1
0.63

9
0.08
6
0.06
8
0.08
8
0.07
7
0.07
7
0.06
10
0.13

12
0.05
11
0.06
10
0.05
9
0.05
9
0.05
15
0.08
10
0.03

32
0.01
13
0.01
49
0.02
51
0.03
26
0.03
23
0.02
12
0.24

115
0.02
73
0.03
324
0.06
174
0.04
753
0.07
903
0.06
61
0.14

0.9
0.06
0.6
0.01
1.7
0.13
2
0.15
2.9
0.12
0.6
0.02
1.2
0.55

S. Muhammad et al. / Microchemical Journal 99 (2011) 6775

and plants could be attributed due to the calc-silicate rocks and hosted
PbZn sulde mineralization [32].
3.2.2. Lahor site
Table 3 summarizes the major cations and HM concentrations in
soil and plant samples collected from the contaminated (Lahor area)
and reference sites. The concentrations of Na, K, Ca, Mg, Fe, Mn, Cr, Ni,
Co, Cu, Pb, Zn and Cd in soil ranged from 414 to 5575 mg/Kg, 2490 to
12915 mg/Kg, 5830 to 24915 mg/Kg, 3210 to 11945 mg/Kg, 17250 to
51750 mg/Kg, 266 to 15420 mg/Kg, 18 to 324 mg/Kg, 92 to 850 mg/
Kg, 45 to 136 mg/Kg, 111 to 345 mg/Kg, 5 to 10300 mg/Kg, 213 to
29755 mg/Kg and 0.4 to 184 mg/Kg, respectively (Table 3). Metal
concentrations were found in the order of Fe N Ca N K N Mg N
Mn N Na N Zn N Pb N Cr N Cu N Ni N Co N Cd. Similarly, the concentrations
of Na, K, Ca, Mg, Fe, Mn, Cr, Ni, Co, Cu, Pb, Zn and Cd in plants

71

ranged from 25 to 146 mg/Kg, 1700 to 13791 mg/Kg, 3694 to

22321 mg/Kg, 852 to 3794 mg/Kg, 110 to 1461 mg/Kg, 32 to
714 mg/Kg, 4 to 11 mg/Kg, 10 to 16 mg/Kg, 5 to 26 mg/Kg, 5 to
24 mg/Kg, 6 to 99 mg/Kg, 16 to 1998 mg/Kgand 0.3 to 6.1 mg/Kg,
respectively (Table 3). Metal concentrations in plants were found in
the order of Ca N Na N Mg N Fe N Mn N K N Zn N Cr N Pb N Ni N Cu N Co N Cd.
High concentrations of these metals in soil and plants may be
attributed due to the calc-silicate rocks and hosted PbZn sulde
mineralization and mining waste [32].
3.3. Pollution quantication
For assessment of major cations and HM contaminations in soil
and plants of the Pazang site, Lahor site and reference sites, the
pollution quantication factors like CF, PLI and BF have been applied.

Table 5
One-way ANOVA comparison in sources variation of selected physio-chemical parameter for the contaminated (Pazang and Lahor) and uncontaminated (Reference) sites.
Physio-chemical
parameters

Sources of variation

Sum of Squares

dfa

Mean Square

pH

Between Groups
Within Groups
Total
Between Groups
Within Groups
Total
Between Groups
Within Groups
Total
Between Groups
Within Groups
Total
Between Groups
Within Groups
Total
Between Groups
Within Groups
Total
Between Groups
Within Groups
Total
Between Groups
Within Groups
Total
Between Groups
Within Groups
Total
Between Groups
Within Groups
Total
Between Groups
Within Groups
Total
Between Groups
Within Groups
Total
Between Groups
Within Groups
Total
Between Groups
Within Groups
Total
Between Groups
Within Groups
Total
Between Groups
Within Groups
Total

4.626
62.460
67.086
138942.240
1633995.407
1772937.648
5.347
226.588
231.935
1.386E8
1.067E8
2.452E8
2.207E8
2.497E8
4.704E8
1.569E8
6.903E8
8.472E8
7876592.279
1.482E8
1.561E8
6.830E8
4.723E9
5.406E9
1.741E8
4.914E8
6.656E8
95095.289
389729.699
484824.988
1144400.928
3012875.333
4157276.261
5292.148
21879.032
27171.180
66694.914
315016.032
381710.946
3.590E7
1.478E8
1.837E8
2.936E8
1.292E9
1.585E9
4083.562
33932.477
38016.039

2
51
53
2
51
53
2
51
53
2
51
53
2
51
53
2
51
53
2
51
53
2
51
53
2
51
53
2
51
53
2
51
53
2
51
53
2
51
53
2
51
53
2
49
51
2
49
51

2.313
1.225

1.889

.162

69471.120
32039.126

2.168

.125

.602

.552

ECc

SOMd

Na

Ca

Mg

Fe

Mn

Ni

Cr

Co

Cu

Pb

Zn

Cd

The mean difference is signicant at a level of 0.01.

Degree of freedom.
Factor.
c
Electrical conductivity.
d
Soil organic matter.
e
Bold values are signicant.
a

2.673
4.443

Fb

Signicance

6.928E7
2091184.071

33.131

.000e

1.104E8
4895861.980

22.542

.000

7.845E7
1.354E7

5.796

.005

3938296.140
2905371.060

1.356

.267

3.415E8
9.261E7

3.687

.032

8.707E7
9635452.421

9.037

.000

47547.645
7641.759

6.222

.004

572200.464
59075.987

9.686

.000

2646.074
429.001

6.168

.004

33347.457
6176.785

5.399

.007

1.795E7
2898412.737

6.194

.004

1.468E8
2.636E7

5.569

.007

2041.781
692.500

2.948

.062

72

S. Muhammad et al. / Microchemical Journal 99 (2011) 6775

3.3.3. Plant bioaccumulation factor (BF)

Table 4 summarizes major cations and HM bioaccumulation and
BF in selected plants species in the Pazang site. Metal BF values
in plant species like Plectranthus rugosus (P. rugosus) were in the order
of Ca N K N Mg N Cd N Cr N Zn N Pb N Ni N Co N Cu N Mn N Fe N Na, for Rumex
hastatus (R. hastatus); Ca N Cd N K N Mg N Mn N Zn N Cu N Cr N Pb N Ni N Co N
Na N Fe, for Fimbristylis dichotoma (F. dichotoma); Cd N K N Ca N Mg N Cr N
Zn N Ni N Pb N Co N Mn N Cu N Na N Fe, for Olea ferruginea (O. ferruginea);
Ca N K N Pb N Cd N Mg N Cr N Ni N Cu N Zn N Mn N Co NFe N Na for Indigofera
gerardiana (I. gerardiana); CaN PbN CdN Mg N K N Zn N Cr N CoN CuN Mn N
NiN FeN Na, for Daphne mucronata (D. mucronata); CaN CdN K N Zn N Mg N
Pb N Cr N Co N Ni N MnN Cu N Fe N Na and for Debregeasia salicifolia
(D. salicifolia) CaN Cd N K N Zn N Mg N PbN CrN Co N NiN Mn N Fe N NaN Cu.
Table 4 summarizes the major cations and HM bioaccumulation
and BF values in selected plants species in the Lahor site. Metal BF
values in plant species like P. rugosus were in the order of
K N Ca N Mg N Co N Cr N Cd N Cu N Na N Zn N Fe N Mn N Ni N Pb, for R. hastatus;
K N Mg N Ca N Cd N Mn N Co N Cr N Cu N Zn N Na N Pb N Fe N Ni, for F. dichotoma; Ca N K N Mg N Cd N Cr N Co N Zn N Mn N Cu N Fe N Pb N Na N Ni, for O.
ferruginea; Ca N K N Mg N Cr N Cd N Co N Zn N Cu N Mn N Na N Pb N Fe N Ni, for
Berberis lyceum (B. lycium); Ca N K N Mg N Cr N Cu N Co N Mn N Zn N Na N
Ni N Fe N Cd N Pb, for Heteropogon conturtus (H. conturtus); Ca N K N Mg N
Cu N Ni N Zn N Co N Cr N Na N Mn N Cd N Pb N Fe and for Myrsine africana
(M. africana); Ca N Cd N K N Pb N Zn N Co N Mg N Cr N Cu N Ni N Na N Mn N Fe.
In the study area, major cations and HM analysis indicated that
plant species had good metal accumulation like P. rugosus for Fe
(1190 mg/Kg) and Cr (20 mg/Kg); R. hastatus for K (11365 mg/Kg),
Mg (4127 mg/Kg), Mn (585 mg/Kg), Na (143 mg/Kg), Cu (45 mg/Kg)
and Pb (51 mg/Kg); F. dichotoma for Ni (14 mg/Kg) and Cd (3 mg/Kg);
H. conturtus for Ca (21013 mg/Kg) and Zn (903 mg/Kg); M. africana
for Co (13 mg/Kg) as shown in Table 4. In the contaminated sites,
bioaccumulations of metal in plant species were multifold higher than
those of reference samples.

3.3.1. Contamination factor (CF)

In the Pazang site soil, CF values were 0.9, 1.9, 1.6, 0.9, 1.7, 5.2, 0.6,
0.6, 0.9, 2.8, 2.3, 3.1 and 1.5 for the Na, K, Ca, Mg, Fe, Mn, Cr, Ni, Co, Cu,
Pb, Zn and Cd, respectively (Table 3). The order of CF values was found
as Mn N Zn N Cu N Pb N K N Fe N Ca N Cd N Na N Cr N Co N Mg. Based on Muller
[33], soil contaminations were classied with Mn; very highly
polluted, Zn; highly polluted, Pb, Cu; moderate to highly polluted
and K, Ca, Fe and Cd; moderately polluted.
Similarly, in the Lahor site soil, CF values were 0.3, 0.9, 1.5, 1.2, 2.5,
9.1, 5.0, 3.2, 1.3, 4.3, 24.9, 25.4 and 7.1 for the Na, K, Ca, Mg, Fe, Mn,
Cr, Ni, Co, Cu, Pb, Zn and Cd, respectively (Table 3). These CF
values were found in the order of Zn N Pb N Mn N Cd N Ni N Cu N Cr N Fe N
Ca N Co N Mg N K N Na. Based on Muller [33], soil contaminations were
classied with Pb, Zn, Mn and Cd; was very highly polluted, Ni and Cu;
highly to very highly polluted, Cr; highly polluted, Fe; moderate to
highly polluted and Ca, Mg and Co; moderately polluted. In the
studied sites, CF values were higher than those reported for soil in
northern Pakistan by Shah et al. [3]. Comparison revealed that the
Lahor site showed higher CF values for Mg, Fe, Mn, Cr, Ni, Co, Cu, Pb, Zn
and Cd than the Pazang site. These higher CF values in the Lahor site
may be inuenced by excessive mining and open dumping of waste in
surroundings.
3.3.2. Pollution load index (PLI)
Based on CF values, PLI values of the Pazang and Lahor sites were
calculated as shown in Table 3. In the Pazang site, PLI value was 1.51,
while in the Lahor site that was 3.25. Comparison of PLI values showed
that the Lahor site was highly contaminated as compared to the
Pazang site. High PLI values in the Lahor site may attributed due to
open dumping of waste along the mining site that may pose a
potential threat to local community. In the study area, PLI values were
greater than that reported for tailing deposit in the Southeast Egypt by
Rashed. [7].

Table 6
Inter-correlation of major cations and HM in soil and plant in the Pazang site.

a. Soil
Na
K
Ca
Mg
Fe
Mn
Ni
Cr
Co
Cu
Pb
Zn
Cd

Na

Ca

Mg

Fe

Mn

Ni

Cr

Co

Cu

Pb

Zn

Cd

1.000

0.149
1.000

0.080
0.093
1.000
.

0.358
0.223
0.653a
1.000

0.362
0.416b
0.352
0.186
1.000

0.096
0.197
0.633
0.410
0.677
1.000

0.207
0.257
0.062
0.041
0.071
0.149
1.000

0.099
0.240
0.083
0.156
0.089
0.194
0.952
1.000

0.199
0.214
0.047
0.075
0.311
0.189
0.308
0.269
1.000

0.585
0.242
0.285
0.234
0.619
0.493
0.090
0.031
0.216
1.000

0.105
0.418
0.050
0.322
0.714
0.562
0.012
0.046
0.265
0.085
1.000

0.446
0.034
0.304
0.292
0.340
0.442
0.069
0.013
0.215
0.121
0.443
1.000

0.152
0.254
0.158
0.048
0.260
0.078
0.002
0.043
0.045
0.129
0.178
0.077
1.000

0.270
1.000

0.444
0.067
1.000

0.500
0.390
0.198
0.367
0.025
1.000

0.272
0.301
0.078
0.075
0.645
0.144
1.000

0.028
0.205
0.118
0.531
0.047
0.072
0.217
1.000

0.186
0.038
0.020
0.275
0.322
0.006
0.185
0.157
1.000

0.524
0.415
0.138
0.361
0.069
0.934
0.217
0.112
0.036
1.000

0.404
0.195
0.068
0.149
0.424
0.185
0.430
0.037
0.403
0.232
1.000

0.099
0.577
0.029
0.009
0.566
0.294
0.241
0.019
0.555
0.231
0.288
1.000

0.236
0.310
0.101
0.158
0.012
0.485
0.239
0.051
0.174
0.446
0.214
0.526
1.000

b. Plant
Na
1.000
K
.
Ca
Mg
Fe
Mn
Ni
Cr
Co
Cu
Pb
Zn
Cd
a
b

0.212
0.381
0.426
1.000

Bold correlation is signicant at the 0.01 level (2-tailed).

Italic correlation is signicant at the 0.05 level (2-tailed).

0.002
0.575
0.142
0.064
1.000

S. Muhammad et al. / Microchemical Journal 99 (2011) 6775

73

Table 7
Inter-correlation of major cations and HM in soil and plant in the Lahor site.

a. Soil
Na
K
Ca
Mg
Fe
Mn
Ni
Cr
Co
Cu
Pb
Zn
Cd

Na

1.000

0.678
1.000

b. Plant
Na
1.000
K
Ca
Mg
Fe
Mn
Ni
Cr
Co
Cu
Pb
Zn
Cd
a
b

0.318
1.000

Ca

Mg

Fe

Mn

0.426 b
.0628
1.000

0.199
.0223
0.507
1.000

0.598
0.629
0.495
0.419
1.000

0.704
0.677
0.46
0.349
0.775
1.000

0.093
0.582
1.000

.0465
0.138
0.500
1.000

0.146
0.233
0.252
0.089
1.000

0.232
0.262
0.103
0.150
0.370
1.000

Ni

Cr

Co

Cu

Pb

Zn

Cd

0.151
0.164
0.035
0.491
0.420
0.085
1.000

0.212
0.134
0.034
0.085
0.574
0.297
0.674
1.000

0.680
0.775
0.622
0.195
0.749
0.766
0.085
0.422
1.000

0.049
0.189
0.197
0.236
0.343
0.023
0.241
0.039
0.077
1.000

0.096
0.041
0.067
0.062
0.106
0.237
0.341
0.212
0.082
0.206
1.000

0.111
0.120
0.101
0.275
0.032
0.345
0.050
0.036
0.022
0.272
0.561
1.000

0.006
0.231
0.037
0.007
0.119
0.102
0.154
0.182
0.056
0.323
0.569
0.434
1.000

0.066
0.081
0.457
0.196
0.058
0.452
1.000

0.056
0.029
0.060
0.022
0.309
0.440
0.252
1.000

0.168
0.394
0.024
0.066
0.063
0.137
0.240
0.272
1.000

0.097
0.217
0.501
0.197
0.111
0.053
0.452
0.253
0.017
1.000

0.124
0.472
0.054
0.395
0.148
0.064
0.397
0.193
0.494
0.107
1.000

0.022
0.509
0.220
0.091
0.074
0.058
0.038
0.108
0.016
0.087
0.363
1.000

0.207
0.243
0.289
0.339
0.125
0.206
0.085
0.285
0.107
0.033
0.542
0.738
1.000

Bold correlation is signicant at the 0.01 level (2-tailed).

Italic correlation is signicant at the 0.05 level (2-tailed).

3.4. Statistical analysis

Table 5 summarizes the One-way ANOVA results of major cations
and HM in contaminated and reference sites. These results revealed
that the contaminated sites have signicantly (P b 0.01) higher
concentrations for some of major cations (Na, K Ca and Mn) and
HM (Ni, Cr, Co, Cu, Pb and Zn) as compared to reference site. These
multifold higher concentrations of major cations and HM in the
contaminated site may be attributed to the mac and ultramac rocks
hosting PbZn sulde mineralization and mining in the area [23,32].
Tables 6 and 7 summarize the inter-metal relationship of major
cations and HM in soil and plants of the Pazang and Lahor sites,
respectively. In the study area, plants and soil did not show signicant
inter-metal correlation. However, in the Pazang site, some metal pairs
like CaMg, FeMn, CuMn, PbFe showed positive correlation in
both soil (r = 0.653), (r = 0.410), (r = 0.493), (r = 0.714) and Plants
(r = 0.426), (r = 0.367), (r = 0.934), (r = 0.424), respectively
(Table 6). Similarly, in Lahor site, some metal pairs like PbZn, Pb
Cd, ZnCd showed positive correlation in both soil (r = 0.561),
(r = 0.569), (r = 0.434) and Plants (r = 0.363), (r = 0.542),

(r = 0738), respectively (Table 7). The inter-metal relationships are

providing interesting information on metal sources and pathways
[34]. The correlation metrics showed these inter-metal relationships
were not signicant. This could be due to different soil characteristics
and plants physiologies [3,29,35]. These weak correlations of major
cations and HM in soil and plants can be attributed to the greater
variation of these metals in soil of the area and variation in plant
uptake [32].
Cluster analysis (CA) was used for qualitative analysis of metal
concentrations in plant species. The CA produced three clusters and
two clusters of plant species in the Pazang and Lahor sites,
respectively. Pazang site had one large and two small clusters,
while that of the Lahor site had one large and one small cluster (Figs. 2
and 3). Cluster analysis suggested that plant species having strong
correlation in metal accumulation will be closely linked together in
primary clusters. Therefore, plant species like P. rugosus and R.
hastatus, F. dichotoma and O. ferruginea form primary clusters in
Pazang site (Fig. 2). Similarly, plant species like B. lycium and O.
ferruginea, (M. africana and F. dichtoma form primary clusters in Lahor
site may due to metal accumulation (Fig. 3).

Fig. 2. Based on accumulation of major cations and of selected plant in the Pazang area.

74

S. Muhammad et al. / Microchemical Journal 99 (2011) 6775

Fig. 3. Based on accumulation of major cations and of selected plant in the Lahor area.

4. Conclusions
PbZn sulde terrain and Pine trees may have caused lowering of
pH and high organic matter (OM) in soil. Low pH and high OM in soil
result in high mobility of metals that caused leaching and contaminations to surrounding area. Releases of high metal concentrations
lead to multifold CF values in the Pazang and Lahor sites as compared
to the reference sites. PLI values were 1.51 and 3.25 in the Pazang and
Lahor sites, respectively. Therefore, soil of these sites was classied as
very highly polluted when compared with Muller classication. This
study concluded that P. rugosus, R. hastatus, F. dichotoma and H.
conturtus is the best accumulator for Fe and Cr; K, Mg, Mn, Na, Cu and
Pb; Ni and Cd; and Ca and Zn, respectively. These plant species have
accumulated multifold higher concentrations in the Pazang and Lahor
sites than those of the reference sites. Metal correlation matrices
showed that they have weak correlation in soil and plants. Plant
species, which revealed high HM bioaccumulation, may be used for
phytoremediation techniques of the metal contaminated area and
also as path nder for specic types of mineral deposits. This study
suggests that for reclamation of the target area, plantation of
mentioned hyper accumulator species should be encouraged in the
Pazang and Lahor sites and after maturity, these plants should be
harvested and properly disposed off.
Acknowledgments
This research work was nancially supported by the Higher
Education Commission (HEC), Islamabad, Pakistan in the form of PhD
scholarship to the rst author. Director NCE in Geology, University of
Peshawar, Pakistan is thanked for providing the eld and analytical
facilities for acquisition of the chemical data. Mr. Liaqat Ali (Research
Associate), NCE in Geology and Prof. Dr. Abdur Rasheed Botany
Department, University of Peshawar is highly acknowledged for
assisting during eld and plant identication, respectively.
References
[1] J.C. Igwe, A.A. Abia, A bioseparation process for removing heavy metals from
waste water using biosorbents, Afr. J. Biotechnol. 5 (2006) 11671179.
[2] P. Chanpiwat, S. Sthiannopkao, K.W. Kim, Metal content variation in wastewater
and biosludge from Bangkok's central wastewater treatment plants, Microchem. J.
95 (2010) 326332.
[3] M.T. Shah, S. Begum, S. Khan, Pedo and biogeochemical studies of mac and
ultramc rocks in the Mingora and Kabal areas, Swat, Pakistan, Environ. Earth Sci.
60 (2010) 10911102.
[4] B. Wei, L. Yang, A review of heavy metal contaminations in urban soils, urban road
dusts and agricultural soils from China, Microchem. J. 94 (2010) 99107.
[5] S. Kong, B. Lu, Y. Ji, X. Zhao, L. Chen, Z. Li, B. Han, Z. Bai. Levels, risk assessment and
sources of PM10 fraction heavy metals in four types dust from a coal-based city,
doi:10.1016/j.microc.2011.02.012, In press
[6] L. Rodriguez, E. Ruiz, J. Alonso-Azcarate, J. Rincon, Heavy metal distribution and
chemical speciation in tailings and soils around a PbZn mine in Spain, J. Environ.
Manage. 90 (2009) 11061116.
[7] M.N. Rashed, Monitoring of contaminated toxic and heavy metals, from mine
tailings through age accumulation, in soil and some wild plants at Southeast
Egypt, J. Hazard. Mater. 178 (2010) 739746.

[8] F.A. Vega, E.F. Covelo, M.L. Andrade, Competitive sorption and desorption of heavy
metals in mine soils: inuence of mine soil characteristics, J. Colloid Interface Sci.
298 (2006) 582592.
[9] J. Nyamangara, Use of sequential extraction to evaluate zinc and copper in a soil
amended with sewage sludge and inorganic metal salts, Agri. Ecosyst. Environ.
69 (1998) 135141.
[10] B. Chehregani, R. Malayeri, Golmohammadi, effect of heavy metals on the
developmental stages of ovules and embryonic sac in Euphorbia cheirandenia,
Pak. J. Biol. Sci. 8 (2005) 622625.
[11] S. Megateli, S. Semsari, M. Couderchet, Toxicity and removal of heavy metals
(cadmium, copper and zinc) by Lemna gibba, Ecotoxicol. Environ. Saf. 72 (2009)
17741780.
[12] S. Muhammad, M.T. Shah, S. Khan, Health risk assessment of heavy metals and
their source apportionment in drinking water of Kohistan region, northern
Pakistan, Microchem. J. 98 (2011) 334343.
[13] Z. Yanqun, L. Yuan, C. Jianjun, C. Haiyan, Q. Li, C. Schvartz, Hyperaccumulation of
Pb, Zn and Cd in herbaceous grown on leadzinc mining area in Yunnan, China,
Environ. Int. 31 (2005) 755762.
[14] S.R. Oliva, A.J.F. Espinosa, Monitoring of heavy metals in topsoils, atmospheric
particles and plant leaves to identify possible contamination sources, Microchem.
J. 86 (2007) 131139.
[15] M. Chehregani, H.L. Noori, Yazdi, phytoremediation of heavy-metal-polluted soils:
screening for new accumulator plants in Angouran mine (Iran) and evaluation of
removal ability, Ecotoxicol. Environ. Saf. 90 (2009) 11061116.
[16] S. Khan, I. Ahmad, M.T. Shah, S. Rehman, A. Khaliq, Use of constructed wetland
for the removal of heavy metals from industrial wastewater, J. Environ. Manage.
90 (2009) 34513457.
[17] D. Desideri, M.A. Meli, C. Roselli, Determination of essential and non-essential
elements in some medicinal plants by polarised X ray uorescence spectrometer
(EDPXRF), Microchem. J. 95 (2010) 174180.
[18] C. Qi, F. Wu, Q. Deng, G. Liu, Changli Mo, Bijun Liu and Jing Zhu. Distribution and
accumulation of antimony in plants in the super-large Sb deposit areas, China,
Microchem. J. 97 (2011) 4451.
[19] V. Salla, C.J. Hardaway, J. Sneddon, Preliminary investigation of Spartina
alterniora for phytoextraction of selected heavy metals in soils from Southwest
Louisiana, Microchem. J. 97 (2011) 207212.
[20] J.L. Freeman, M.W. Persans, K. Nieman, C. Albrecht, W. Peer, I.J. Pickering, D.E. Salt,
Increased glutathione biosynthesis play a role in nickel tolerance in Thlaspi nickel
hyperaccomulator, Plant Cell 16 (2004) 21762191.
[21] S. Wei, Q. Zhou, H. Xiao, C. Yang, Y. Hu, L. Ren, Hyperaccumulative property
comparison of 24 weed species to heavy metals using a pot culture experiment,
Environ. Monit. Assess. 152 (2009) 299307.
[22] C.J.N. Fletcher, R.C. Leake, H.W. Haslam, Tectonic setting, mineralogy and
chemistry of a metamorphose stratiform base metal deposit within the Himalayas
of Pakistan, Geological Society of London. 143 (1986) 521536.
[23] M.T. Shah, Mineralogy, chemistry and genesis of the Proterozoic base metal
deposits at the northern margin of the Indian plate in Besham area, Himalaya,
northern Pakistan, in: S.S. Hussain, H.M. Akbar (Eds.), Economic Geology of
Pakistan. Pakistan Museum of Natural History, 2000, pp. 1157.
[24] S. Muhammad, M.T. Shah, S. Khan, Arsenic health risk assessment in drinking
water and source apportionment using multivariate statistical techniques
in Kohistan region, northern Pakistan, Food Chem. Toxicol. 48 (2010) 28552864.
[25] J.A.Y. Dipietro, K.R. Pogue, R.D. Lawrence, M.S. Baig, A. Hussain, I. Ahmad,
Stratigraphy south of the main mantle thrust, Lower Swat, Pakistan, in: P.J.
Treloar, M.P. Searle (Eds.), Himalayan Tectonics, Geological Society London, 45,
1993, pp. 207220.
[26] M. Das, S.K. Maiti, Comparison between availability of heavy metals in dry and
wetland tailing of an abandoned copper tailing pond, Environ. Monit. Assess.
137 (2008) 343350.
[27] M.E. Konen, P.M. Jacobs, C.L. Burras, B.J. Talaga, J.A. Mason, Equition for predicting
soil organic matter using loss-on-ignition for North Central US soil, Soil Sci. Soc.
Am. J. 66 (2002) 18781881.
[28] J. Ryan, G. Estefan, A. Rashid, Soil and plant analysis laboratory manual, Interaction
Center for Agricultural Research in the Dry Areas (ICARDA), Aleppo, Syria, 2nd ed,
2001, p. 172.
[29] S. Khan, Q. Cao, Y.M. Zheng, Y.Z. Huang, Y.G. Zhu, Health risks of heavy metals in
contaminated soils and food crops irrigated with wastewater in Beijing China,
Environ. Pollut. 152 (2008) 686692.

S. Muhammad et al. / Microchemical Journal 99 (2011) 6775

[30] U. Usero, A. Garcia, J. Fraidias, Calidad de las aguas y sedimentos del Litoral Andaluz,
Junta de Andalicia, Consejeria del Medio Ambiente, Sevilla (Editorial), 2000, p. 164.
[31] F.M. Romero, M.A. Armienta, G. Gonzalez-Hernandez, Solid-phase control on the
mobility of potentially toxic elements in an abandoned lead/zinc mine tailings
impoundment, Taxco, Mexico, Appl. Geochem. 22 (2007) 109127.
[32] M.T. Shah, Q. Kifyattullah, M. Irfan, Pedo and biogeochemical study of zinclead
deposits of the Besham area, northern Pakistan; its implication in mineral
exploration and environmental degradation, Environ. Geol. 45 (2004) 544549.

75

[33] G. Muller, Index of geoaccumulation in sediments of the Rhine River, GeoJournal

2 (1969) 108118.
[34] D.S. Manta, M. Angelone, A. Bellanca, R. Neri, M. Sprovieri, Heavy metals in urban
soils: a case study from the city of Palermo (Sicily), Italy, Sci. Total Environ. 300
(2002) 229243.
[35] W.L. Xio, C.L. Luo, Y.H. Chen, Z.G. Shen, X.D. Li, Bioaccumulation of heavy metals by
wild plants growing on copper mine spoils in China, Commun. Soil Sci. Plant Anal.
39 (2008) 315328.