Journal of Cleaner Production 229 (2019) 727e738

Contents lists available at ScienceDirect

Journal of Cleaner Production

journal homepage: www.elsevier.com/locate/jclepro

Phytomonitoring of air pollution around brick kilns in Balochistan

province Pakistan through air pollution index and metal accumulation
index
Khanoranga*, Sofia Khalid
Fatima Jinnah Women University, The Mall, Rawalpindi, Pakistan

a r t i c l e i n f o a b s t r a c t

Article history: Some plants species can be used as biomonitoring agents around highly polluted sites. This study was
Received 2 November 2018 carried out to assess the sensitivity and tolerance of plants species against air pollution around brick kilns
Received in revised form in Balochistan province, Pakistan. Plant species were collected from the study sites and were evaluated
8 April 2019
against pollution by making use of air pollution tolerance index and metal accumulation index. The
Accepted 5 May 2019
susceptibility of plants to different pollutants was determined by analyzing various biochemical pa-
Available online 6 May 2019
rameters (i.e. total chlorophyll content, ascorbic acid, pH of the leaf extract and relative water content),
heavy metal(loid)s level of the investigated plant species. The pollution tolerance level of the analyzed
Keywords:
Brick kiln
plant samples showed that Morus alba was the most tolerant and Convolvulus arvensis, the most sensitive
Biomonitoring species to the air pollution. The metal accumulation index value was found highest for Lepidium sativum
Metal accumulation index and lowest for Malcolmia africana, depicting their metal accumulation capacity. Moreover, it was found
Heavy metal(loid)s that the pollution level of all the analyzed heavy metal(loid)s was beyond the permissible limits of WHO
Balochistan except Mn. Keeping in view this research, it is suggested that the mentioned tolerant plant species grown
in the vicinity of brick kilns may serve as sinks for pollution whereas, the sensitive ones may be used for
monitoring of pollution level.
© 2019 Elsevier Ltd. All rights reserved.

1. Introduction
Brick kilns industries are regarded as one of the main sources of
pollution in developing countries such as Pakistan, India, and
Bangladesh (Ahmad et al., 2012). The operational activities are
generally carried out without use of any modern technologies and
contaminate the environment through several emissions more
importantly gaseous and particulate forms of pollutants such as
NOx, SOx, COx, heavy metals and polycyclic aromatic hydrocarbons
(PAHs) (Kamal et al., 2014; Jan et al., 2014; Saha and Hosain, 2016).
Plants are the main components of an ecosystem maintaining
ecological balance through actively participating in the cycling of
nutrients and gases (photosynthesis and respiration) and also
providing large surface areas for assimilation and accumulation of
different pollutants in the environment (Díaz et al., 2007). The
accumulation of certain pollutants in plants may cause injuries or
physiological changes in numerous ways (Braun et al., 2017). It has
* Corresponding author.
E-mail address: khanoranga.achak@gmail.com (Khanoranga).
been reported that the sensitive species show greater injuries (i.e.,
Necrosis, chlorosis, stomatal damage altering the rate of respiration
and transpiration, impacts on the chlorophyll content reducing
photosynthetic activity, disruption of cell permeability and enzy-
matic reactions) due to air pollution compared to tolerant plant
species (Agrawal and Agrawal, 1989; Kuddus et al., 2011; Shah et al.,
2018). Biomonitroing is a cost effective and emerging technique
using the responses of organisms (plants and animals) to determine
the quality of their environment. Plants are widely used as bio-
indicators to pinpoint the possible sources of pollutants in the
environments. Changes occurring in the physiology, morphology
and other biochemical parameters are regarded as the biomarkers
of the pollution effects. Plant species vary in their responses to air
pollution exposures. Some plant species are very sensitive to
pollution stress resulting in measurable and visible symptoms
while certain plant species are resistant to different pollutants.
These biomarkers are used to convey information on alteration in
the quality of the environment (Chakrabortty and Paratkar, 2006;
Elloumi et al., 2018). The sensitive species can be good bio-
monitor of a pollution in the contaminated environment. Similarly,
the tolerant species are beneficial for the abatement of the

https://doi.org/10.1016/j.jclepro.2019.05.050
0959-6526/© 2019 Elsevier Ltd. All rights reserved.
728 Khanoranga, S. Khalid / Journal of Cleaner Production 229 (2019) 727e738
contaminated environment by acting as a sink and reducing the
level of certain pollutants (Lohe et al., 2015). Plants growing in the
vicinity of brick kilns are considered to be vulnerable to pollutant
exposure (Wahid et al., 2014). This is most likely, due to the gaseous
exchange of oxides of sulphur (SOx), nitrogen (NOx) and carbon
(COx), hydrogen fluoride (HF) and ozone (O3) through stomata, wet
and dry deposition of particulate matter, fly ash and other pollut-
ants which reduce the interception of incident light and result in
clogging of stomata (De Camargo and Lombardi, 2018). Brick kilns
industries in Pakistan are fired with low-quality fuel responsible for
the release of different types of hazardous emissions in the ambient
environment (Achakzai et al., 2017a,b). Generally, heavy metals
contamination of plants growing in the vicinity of brick kilns is of
major concern. Heavy metals such as Cd, Cr, Pb, Hg and As are the
most important hazardous, pollutants degrading the quality of the
environment and also imposing a threat to the health of people
(Begum et al., 2015). These are released in the environment due to
the incomplete combustion of coal in brick kilns (Ishaq et al., 2010).
Once, these are released into the environment they move into
different environmental matrices such as soil, plants, water, and air.
The soil in any ecosystem acts as a sink for different pollutants.
Contaminated soil, therefore, is also a threat to the vegetation
growing on it (Yang et al., 2016; Sikder et al., 2016). Although, some
metals are beneficial for the growth of plants such as Fe, Mn, Co, Cu
and Zn and are a major constituent of several enzymes and other
cellular structures (Malik et al., 2010).
Moreover, the other hazardous heavy metals such as Hg, Cd, Pb,
and Cr are very toxic to the plants by disrupting important enzymes
structures and replacing the essential metals (Fontenele et al.,
2017). Furthermore, plants may also have strong defense system
(antioxidant system) providing tolerance against heavy metals, but
the excess of heavy metals in plants may cause different physio-
logical, morphological and biochemical changes in the exposed
plants such as decrease in photosynthetic pigments, visible leaf
injuries, stomatal clogging, early senescence, reducing permeability
of cellular structure and causing restricted plant growth. In case of
staple crops, it may lead to yield losses (Waseem et al., 2014; Khalid
et al., 2018).
Thus, the ecophysiological response of plants to the exposures of
different pollutants can be used for biomonitoring of pollution level
(Josephine et al., 2019). Tolerant plants species can be used as a
remediation tool to protect environment indirectly lowering the
risk of exposure of human to hazardous pollutants. Biomonitoring
of heavy metal pollution with plants is a cost-effective method (Liu
et al., 2017; Nakazato et al., 2018).
Plants exposed to a pollution source absorb and accumulate
environmental pollutants (heavy metals). Different plants have
various tendencies of the accumulation of heavy metals thus acting
like hyperaccumulators of different pollutants (Shah et al., 2014;
Irshad et al., 2015). Phytomonitoring is a crucial step in studying
the transfer of pollutants in the food chain (Amin and Ahmad, 2015;
Van der Ent et al., 2015; Rodríguez-Bocanegra et al., 2018). In fact,
the hyperaccumulator plants species are also widely reported in
phytoremediation, a promising technique used in the reclamation
of the contaminated soil (Cristaldi et al., 2017). A wide range of
plants belonging to different families has been identified, having a
great tendency of the tolerance and accumulation for numerous
hazardous heavy metals (Mahdavian et al., 2017; Sarkar, 2018).
These tolerant plant species are regarded as appropriate for soil
stabilization and extraction of heavy metals through their roots
(Reeves et al., 2018).
The susceptibility of plants to air pollution can be determined by
analyzing different physiological and biochemical parameters
including total chlorophyll content, ascorbic acid, pH of the leaf
extract and relative water content respectively. These indicator
parameters are computed in a single index described as air pollu-
tion tolerance index (APTI) (Esfahani et al., 2013). The evaluation of
single parameters for the assessment of pollution load on the plants
may not give a clear picture of the impacts of pollution. Therefore,
APTI is an integrated tool for assessing the response of plants to a
diverse range of pollutants through biochemical and physiological
parameters. Thus, this reliable tool can be effectively utilized for
identification of indicators (tolerant and sensitive) plant species to
be grown in the contaminated environment (Okunlola et al., 2016;
Kashyap et al., 2018). Although many research studies have been
conducted in developing countries about the potential of plants for
air pollution monitoring and toxic elements (Zhan et al., 2014;
Alahabadi et al., 2017). Pollution monitoring in rapidly developing
province of Pakistan is important for sustainable development and
current study is the first assessment of brick kiln’s pollution im-
pacts on surrounding vegetation in the study area. The current
study has been designated: (1) To study the impacts of different
pollutants on the foliar biochemical parameters (2) To assess the
concentration of heavy metals and arsenic in the studied plants (3)
To determine the tolerance of plants against brick kilns pollution
through APTI and Metal accumulation index (MAI) (4) To recom-
mend suitable species of plants for phytomonitoring of air pollution
and toxic elements growing in the vicinity of brick kilns.
2. Materials and methods
2.1. Study site
The brick sector of Balochistan is mainly supported by the high
production of bricks from Quetta, Pishin and Mastung districts
respectively. The current study was conducted in these three dis-
tricts of Balochistan (Fig. 1). Sampling was conducted in Kuchlak
(Quetta) where approximately 30 brick kilns were operating
whereas, in Pishin and Mastung sampling was carried out in Yaroo,
Saranan, and Dasht where about 50e60 and 130 brick kilns were
operational. Three brick kilns in each study sites were selected for
sampling. The design of brick kilns was an old bull’s trench type
commonly used throughout the country. Coal, wood and rubber
tires were normally used as fuel at all sites. The selection criteria of
brick kilns were based on its nearness to the agricultural land and
production capacity. Brick kilns were surrounded by agricultural
land where wheat crops and orchards of fruits were cultivated.
2.2. Plant sampling
Representative plants species both cultivated and wild were
randomly selected with increasing distance of about 100 m, 300 m,
and 500 m away from brick kilns in three districts (Quetta, Pishin,
and Mastung) of Balochistan. In total nine plants i.e. Triticum aes-
tivum (Wheat), Chenopodium album (Goosefoot), Medicago sativa
(Alfalfa), Lepidium sativum (Garden cress), Prunus armeniaca
(Apricot), Convolvulus arvensis (Bindweed), Elaeagnus angustifolia
(Russian olive), Vitis vinifera (Wine grape), Punica granatum
(Pomegranate) were collected in Quetta whereas total of five plants
namely, Triticum aestivum, Peganum harmala (Wild rue), Lepidium
sativum, Morus alba (White mulberry), Malcolmia africana (African
mustard) were collected in Pishin and Mastung. Samples were
collected at the end of April 2017 and analysis was completed in
May 2017. Samples were collected in triplicates i.e. three leaves
samples from each plant species at each site. The collected samples
of plants were stored in ice container and then immediately
brought to the laboratory for analysis. After taking fresh weight
plants were washed with distilled water to remove soil and other
dirt particles. Some plant samples were kept refrigerated until
further analysis while others were oven dried. The refrigerated
 Khanoranga, S. Khalid / Journal of Cleaner Production 229 (2019) 727e738
Fig. 1. Map of the study area.
plant samples were investigated for different biochemical param-
eters (total chlorophyll content, ascorbic acid, relative water con-
tent, and pH of leaf extract) whereas dried samples were
investigated for the presence of heavy metals according to standard
methods. For identification purpose the collected plant samples
were pressed, dried and pasted on standard herbarium sheets. The
plant specimens were then identified by expert taxonomist at
Botany Department of the University of Balochistan according to
Flora of Pakistan. The identified plant specimens were deposited to
the herbarium of University of Balochsiatn (Shuaib et al., 2019). To
minimize the chance of variation all samples were collected on the
same day.
2.3. Biochemical analysis
2.3.1. Total chlorophyll content
Total chlorophyll content in leaves of selected plant species was
estimated using standard method used by Singh et al. (1991). 0.1 g
of leaf material was suspended in 80% prepared acetone solution
and small amount of sand or magnesium carbonate was also added
to get better suspension. Leaf extract was centrifuged at 3000 rpm
for about 3 min. Absorbance of leaf extract was measured through
UV spectrophotometer at wavelengths of 663 nm, and 645 nm. The
estimated chlorophyll content was calculated through Arnon
(1949) equations.
Chl a ðmg=gÞ ¼ ½ð12:7  A663Þ  ð2:6  A645Þ
ml acetone
 (1)
mg leaf tissue
Chl b ðmg=gÞ ¼ ½ð22:9  A645Þ  ð4:68  A663Þ
ml acetone
 (2)
mg leaf tissue
Total chlorophyll content (mg/g) ¼ Chl aþ Chl b (3)
729
2.3.2. Relative water content
Relative water content was determined by following the method
used by Singh (1977). Leaves of each plants species were weighed
immediately after sampling. The leaves were immersed into water
and kept overnight, after which they were blotted to dry and
weighed again to get turbid weight. The turbid leaves were dried in
an oven at 70  C for 24 h to get the constant dry weight. Relative
water content was determined by applying following formula:
FW  DW
Relative water content ð%Þ ¼  100 (4)
TW  DW
Whereas; FW Fresh weight, DW Dry weight and TW Turbid weight.
2.3.3. pH of leaf extract
For determination of pH, 5 g of sample was homogenized with
50 ml of distilled water. pH of prepared suspension was measured
using digital pH meter (Kuddus et al., 2011).
2.3.4. Ascorbic acid
Ascorbic acid was determined by titration method. 2 g of leaf
sample was weighed and then quickly homogenized with 5%
metaphosphoric acid. The sample was crushed with mortar pestle
until a slurry type mixture was formed. The mixture was filtered
with Whatman filter paper. 10 ml of aliquot was taken from the
mixture and titrated against dichloroindophenol (DCIP) dye solu-
tion (Reiss, 1993).
2.3.5. Air pollution tolerance index
APTI was calculated by computing all the four parameters in a
single equation;
AðT þ PÞ þ R
APTI ¼ (5)
10
Whereas,
A (Ascorbic acid) T (Total chlorophyll content) P (pH of leaf
730 Khanoranga, S. Khalid / Journal of Cleaner Production 229 (2019) 727e738

extract) R (Relative water content). the concentration of NO2 ranged between 11.38 and 298.48 ppb
(Quetta), 18.15e112.95 ppb (Pishin) and 91.28e492.15 ppb (Mas-
2.4. Method of digestion tung) respectively. The concentration of the NO2 was found above
the permissible limits of WHO (21 ppb) (Ahmad and Aziz, 2013).
0.5 g of crushed plant powder sample was taken in beaker and
12 ml (9 ml HCL þ 3 ml HNO3) of aqua regia was added. Beaker was 3.1. Total chlorophyll content
covered with watch glass and heated on hot plate at 80  C for 2 h.
After which, the suspension was allowed to cool and filtered Chlorophyll content is regarded as the index of the productivity
through Whatman No: 42 filter paper. Leaching was done with as well as it is suggestive of the photosynthetic activity, growth, and
dionized water and the volume was made up to 50 ml. The digested biomass (Ninave et al., 2001). It is very sensitive to the exposure of
plant samples were analyzed for heavy metal(loid)s (Bigdeli and pollutants and most liable to damage by pollution load (Areington
Seilsepour 2008). As and Hg were assessed using AAS coupled to and Varghese, 2017). It is also reported, that chlorophyll content
hydride generation and cold vapor (220 Spectra AA, Varian) while varies with the type of species, the age of leaf and pollution load as
the rest of heavy metals were assessed through Flame atomic ab- well as with several other biotic and abiotic factor (Prajapati and
sorption spectrophotometer (FAAS, AA-7000 Shimadzu). Tripathi, 2008). The results of the current study showed that
MAI was used to assess the heavy metal(loid)s accumulation marked variation was determined in the chlorophyll content of the
efficiencies of the plants using the standard formula; studied plants with increasing distance from the brick kilns

Xn (Table 1). Some decrease in chlorophyll content was observed with
1
MAI ¼ IJ (6) increasing distance from source but it was not statistically signifi-
N J¼1 cant (p > 0.05) except Quetta (Table 2). The most probable reasons
for this might be the fallout of the pollutants some distance away
Where N shows the total number of heavy metals studied and IJ is from the sources depending upon the speed and direction of the
sub-index of J gained by dividing the metal concentration by its wind. These results also confirmed that the impacts of pollution on

rska-Socha et al., 2017).
standard deviation (Hu et al., 2014; Nadgo the environment can be felt away from the sources (Laghari et al.,
2015; Achakzai et al., 2017a,b). Similarly, significant (p < 0.05) var-
2.5. Data precision and accuracy iations in the chlorophyll content among the studied plants and
study sites were also found, signifying the fact that plants vary in
Each sample was analyzed in triplicate and mean of the tripli- the chlorophyll contents as reported by several other authors
cate was used for further data interpretation. Reagent blanks were (Klumpp et al., 2000; Thawale et al., 2011). Variation in the chlo-
also included with samples in each step of the experiment. The rophyll content in the studied plants might be due to the increased
accuracy of Atomic absorption spectrophotometer was assessed pollution level near the source. The decreased in chlorophyll con-
through the standards of all metals prepared through the dilution tent near the source might be due to the released of different types
(1000 mg/L) of the certified reference solution (Merck) of corre- of emission (Gaseous and particulate forms of pollutants) due to the
sponding metal with double deionized water and working stan- combustion of coal and other operational activities of brick kilns
dards were analyzed after every 10 samples. All the chemicals and (Gupta and Narayan, 2010; Adrees et al., 2016). The aerial deposi-
reagent were of analytical grade. The limit of detection (LOD) and tion of particulate matter and other fly ash on the leaf surfaces
limit of quantification (LOQ) were determined through triplicates of blocks stomata and thus, disturbing the gaseous exchange for
10 method blanks digested in same way as the plant samples and photosynthesis, especially in sensitive plant species (Sarma et al.,
values were calculated through standard formulas (Radwan and 2017). The results of the current study are in line with several
Salama, 2006). LOD values for Cd, Cr, Pb, Cu, Mn, Zn, Ni, Co, Fe, As other studies that report the impacts of pollution stress on the
and Hg were 0.02, 0.02, 0.05, 0.1, 0.17, 0.06, 0.13, 0.09, 0.66, 0.01,
0.02 mg/kg respectively. LOQ values for Cd, Cr, Pb, Cu, Mn, Zn, Ni, Co,
Table 1
Fe, As and Hg were 0.06, 0.05, 0.14, 0.31, 0.45, 0.14, 0.34, 0.26, 1.95, The impacts of brick kilns pollution on the total chlorophyll content (mg/g) of the
0.04, 0.05 mg/kg respectively. The validation of analytical method studied plants in three districts of Balochistan.
was carried out through a recovery study, by spiking samples with
Name of plants 100 m 300 m 500 m
known concentration of standards of heavy metal(loid)s (Tang
Quetta
et al., 2018). The spiked samples were analyzed in the same way
Triticum aestivum 1.68 ± 1.56 2.39.15 3.58 ± 0.72
as like actual samples. The % average recoveries achieved for Cd, Cr, Chenopodium album 3.23 ± 2.61 3.06 ± 0.28 4.76 ± 1.5
Pb, Cu, Mn, Zn, Ni, Co, Fe, As and Hg were 93, 86, 87, 90, 90, 96, 96, Medicago sativa 4.89 ± 1.02 4.28 ± 1.06 6.56 ± 0.59
97, 94, 88, 86% respectively. Lepidium sativum 4.41 ± 2.32 3.50 ± 0.87 6.46 ± 0.32
Prunus armeniaca 1.99 ± 1.80 1.59 ± 0.32 3.49 ± 0.58
Convolvulus arvensis 0.87 ± 0.91 0.87 ± 0.06 2.23 ± 0.55
2.6. Statistical analysis Elaeagnus angustifolia 5.94 ± 1.53 5.57 ± 1.44 7.85 ± 0.14
Vitis vinifera 1.32 ± 1.35 1.96 ± 0.93 2.92 ± 0.09
For each plant samples mean was calculated from triplicates Punica granatum 3.69 ± 2.06 3.13 ± 0.78 5.69 ± 0.46
samples and presented with the standard deviation in tables. Mean Pishin
Triticum aestivum 0.89 ± 0.68 1.49 ± 1.14 1.95 ± 1.105
of variance for investigated biochemical parameters with respect to Peganum harmala 1.90 ± 0.57 2.29 ± 0.76 2.72 ± 0.64
distance, study sites and plant species was determined through Lepidium sativum 1.21 ± 0.90 2.72 ± 1.28 2.04 ± 0.75
One-way ANOVA using Microsoft Excel 2013. Morus alba 3.71 ± 1.02 3.72 ± 1.19 4.19 ± 1.49
Malcolmia africana 2.89 ± 0.39 3.03 ± 0.81 3.29 ± 0.86
Mastung
3. Results and discussion Triticum aestivum 0.99 ± 0.76 2.16 ± 0.18 2.89 ± 0.75
Peganum harmala 1.92 ± 0.59 3.62 ± 0.97 4.13 ± 1.63
The current study investigates the air quality through two Lepidium sativum 1.17 ± 0.97 2.94 ± 0.08 3.11 ± 1.55
important criteria pollutants viz. NO2 and CO at the study area. The Morus alba 4.01 ± 0.94 5.65 ± 1.09 5.87 ± 1.18
Malcolmia africana 3.56 ± 1.40 4.54 ± 0.76 4.54 ± 2.19
concentration of CO was found below the detection limit whereas;
 Khanoranga, S. Khalid / Journal of Cleaner Production 229 (2019) 727e738 731

Table 2 Table 3
Result of One Way ANOVA signifying variation in studied parameter with increasing The impacts of brick kilns pollution on the ascorbic acid content (mg/g) of the
distance from the source and among the studied plant species at the study sites. studied plants in three districts of Balochistan.

Variable Study site Distance Plantspecies Name of plants 100 m 300 m 500 m

Total chlorophyll content (mg/g) Quetta 0.05* 0.000* Quetta

Pishin 0.51 0.001* Triticum aestivum 2.42 ± 0.34 2.73 ± 0.56 3.19 ± 2.05
Mastung 0.11 0.01* Chenopodium album 3.28 ± 1.32 3.21 ± 0.87 4.2 ± 2.09
Study sites 0.001* Medicago sativa 7.66 ± 3.63 2.27 ± 0.60 3.81 ± 1.84
Ascorbic acid (mg/g) Quetta 0.98 0.04* Lepidium sativum 5.55 ± 0.38 3.47 ± 1.96 4.74 ± 1.90
Pishin 0.81 0.03* Prunus armeniaca 2.41 ± 0.82 1.63 ± 0.81 2.42 ± 0.72
Mastung 0.36 0.04* Convolvulus arvensis 1.23 ± 1.7 3.84 ± 2.91 3.62 ± 1.48
Study sites 0.000* Elaeagnus angustifolia 10.72 ± 2.52 4.22 ± 2.13 3.4 ± 1.99
pH of the leaf extract Quetta 0.00* 0.01* Vitis vinifera 1.47 ± 0.88 1.96 ± 1.69 4.07 ± 1.79
Pishin 0.31 0.000* Punica granatum 4.57 ± 1.18 3.50 ± 1.4 4.20 ± 1.39
Mastung 0.22 0.000* Pishin
Study sites 0.000* Triticum aestivum 1.77 ± 1.28 2.52 ± 0.31 3.33 ± 2.93
Relative water content (%) Quetta 0.95 0.001* Peganum harmala 5.89 ± 2.79 5.6 ± 1.94 5.43 ± 0.23
Pishin 0.58 0.01* Lepidium sativum 2.20 ± 0.97 3.06 ± 1.45 4.34 ± 40
Mastung 0.40 0.04* Morus alba 8.99 ± 1.83 11.12 ± 1.5 12.36 ± 2.97
Study sites 0.000* Malcolmia africana 7.70 ± 2.55 8.56 ± 1.94 8.29 ± 2.51
APTI Quetta 0.83 0.03* Mastung
Pishin 0.81 0.000* Triticum aestivum 5.70 ± 2.72 2.68 ± 0.67 5.70 ± 2.5
Mastung 0.28 0.000* Peganum harmala 9.99 ± 3.77 6.08 ± 3.21 9.99 ± 3.8
Study sites 0.000* Lepidium sativum 5.14 ± 2.16 3.63 ± 1.06 5.14 ± 0.38
Morus alba 15.9 ± 1.21 11.23 ± 6.55 15.9 ± 6.06
*p is significant at the level of 0.05.
Malcolmia africana 12.73 ± 3.14 8.33 ± 3.53 12.73 ± 5.28

chlorophyll content of the investigated plants (Gupta et al., 2016;

Molna
r et al., 2018). presence of the acidic pollutants, the pH of the cell sap become
acidic which restricts the conversion of hexose sugar to ascorbic
3.2. Ascorbic acid acid, which is helpful in the defense mechanism of the plants
(Agbaire and Esiefarienrhe, 2009). Similarly, acidic pH increases the
Ascorbic acid plays a significant role in the defense mechanism stomatal sensitivity to pollution thus altering important physio-
of plant and is regarded as strong reducing agent (Hussain et al., logical processes (i.e. rate of respiration and transpiration) of plants.
2017). It helps in protecting chloroplast of the plants from inacti- Additionally, pH also regulates several other physiological pro-
vation due to the exposure to air pollutants like SO2. The concen- cesses of the plants i.e. numerous enzymatic and photosynthetic
tration of ascorbic acid is directly proportional to its reducing activity is dependent upon the specific range of pH. The findings
power while the reducing property of the ascorbic acid is pH from the current study showed an inconsistent trend of variation in
dependent. High pH favors the conversion of hexose sugar into leaf extract pH with the increasing distance from the source
ascorbic acid (Tanee and Albert, 2013). In the current study a pos- (Table 4). Generally, the pH was found lower near the source
itive correlation (r ¼ 0.98) was determined between ascorbic acid (100 m) in most studied plants in all three sites. The output of one-
and pH of extract (data are not presented here). Ascorbic acid also way ANOVA (Table 2) illustrated that variations with distance were
helps in other physiological processes of the cell such as cell divi- statistically insignificant (p > 0.05) except in Quetta whereas vari-
sion, cell wall formation, and defense mechanism. It is a natural ations in the pH of the leaf extracts of plants among the study sites
antioxidant and reduces the effects of the pollution exposure. The
results of the current study illustrated that ascorbic acid showed an Table 4
inconsistent trend of variations with the increasing distance from The impacts of brick kilns pollution on the pH of the leaf extracts of the studied
the source (Table 3) and One-way ANOVA also confirmed that plants in three districts of Balochistan.
variations were statistically insignificant (p > 0.05) in all three sites Name of plants 100 m 300 m 500 m
with respect to distance from the source (Table 2). Ascorbic acid is
Quetta
generally produced in greater amounts in plants during stress Triticum aestivum 5.93 ± 0.72 6.73 ± 0.35 6.43 ± 0.35
conditions. In the current study, plants showed significant Chenopodium album 7.03 ± 0.20 6.43 ± 0.35 6.76 ± 0.35
(p < 0.05) differences in the ascorbic acid content confirming the Medicago sativa 6.07 ± 0.27 6.5 ± 0.72 6.96 ± 0.72
fact that plants vary in response to different pollutants. High level Lepidium sativum 6.46 ± 0.60 6.8 ± 0.45 7.13 ± 0.45
Prunus armeniaca 5.9 ± 0.50 6.3 ± 0.40 6.46 ± 0.40
of the ascorbic acid signifies the tolerance of plants against pollu-
Convolvulus arvensis 5.8 ± 0.46 7.23 ± 0.43 6.40 ± 0.44
tion exposure. The results of the study are in agreement with other Elaeagnus angustifolia 6.63 ± 0.23 6.96 ± 0.60 6.50 ± 0.60
authors (Dwivedi and Tripathi, 2007; Ogunrotimi et al., 2017). Vitis vinifera 5.83 ± 0.98 6.76 ± 0.76 6.63 ± 0.76
Variations in the level of ascorbic acid among the study sites and Punica granatum 6.13 ± 1.09 6.9 ± 0.20 6.70 ± 0.20
among different plant species were also significant (p < 0.05) as Pishin
Triticum aestivum 6.20 ± 0.15 6.40 ± 0.10 6.8 ± 0.25
shown in (Table 2). Peganum harmala 6.60 ± 0.25 6.91 ± 0.10 7.2 ± 0.29
Lepidium sativum 6.30 ± 0.25 6.50 ± 0.15 6.8 ± 0.12
3.3. pH of leaf extracts Morus alba 7.41 ± 0.43 7.63 ± 0.17 7.8 ± 0.23
Malcolmia africana 7.03 ± 0.15 7.20 ± 0.10 7.4 ± 0.35
Mastung
pH of the leaf extract is an important parameter which can help Triticum aestivum 6.57 ± 0.35 6.63 ± 0.23 7.03 ± 0.06
in determining the susceptibility of plants to the pollution exposure Peganum harmala 6.8 ± 0.85 6.93 ± 0.15 7.47 ± 0.38
i.e. SO2 and NOx (Rahul and Jain, 2014). pH of the leaf extract is Lepidium sativum 6.13 ± 0.32 6.60 ± 0.2 7.10 ± 0.17
generally lower in the presence of the acidic pollutants and will be Morus alba 7.50 ± 0.52 7.60 ± 0.2 8 ± 0.36
Malcolmia africana 7.40 ± 0.26 7.27 ± 0.23 7.60 ± 0.43
low in the sensitive species upon exposure to air pollutants. In the
732 Khanoranga, S. Khalid / Journal of Cleaner Production 229 (2019) 727e738

were statistically significant (p < 0.05). Besides this, plants also
showed significant (p < 0.05) differences in the pH of leaf extract
illustrating the fact that response to pollutants varies with the
types of plants i.e. acidic pH is the indication of the sensitivity of the
plant upon exposure to pollution (Lakshmi et al., 2009; Rai and
Panda, 2014). The findings are in agreement with several other
studies reporting acidic pH of the leaf extracts near the pollution
source and some also reported an inconsistent trend of variations
with distance away from the source (Thawale et al., 2011).
3.4. Relative water content
It is another crucial parameter determining the susceptibility of
plants to the pollution exposure (Kaur and Nagpal, 2017; Sharma
et al., 2017). The results of the current study demonstrate that
relative water content of studied plants showed an inconsistent
trend of variation with increasing distance from the source
(Table 5). The results of one-way ANOVA (Table 2) also showed that
variations in the increasing distance were statistically insignificant
(p > 0.05). Similarly, plants exhibited significant (p < 0.05) varia-
tions in the relative water content and variations in the level of
relative water content of plants among the study sites were also
statistically significant (p < 0.05). It may be due to the differences
among plants intolerance against air pollution. Increased level of
pollution increased the permeability of cell and dissolved nutrients
increasing the risk of early senescence (Sinha et al., 2017). The high
relative water content in the presence of high pollution is the
indication of greater tolerance of plants. The findings of the current
study are supported by other studies (Seyyednejad et al., 2017;
Ogbonna et al., 2017).
3.5. Air pollution tolerance index
APTI is a reliable method for screening the susceptibility of
different plants upon exposure to same or different pollutants
(Nadgo
rska-Socha et al., 2017). The method is very simple and easy
to adopt during field condition without acquiring large environ-
mental monitoring setups (Maity et al., 2017). The result of the
current study demonstrated that all the studied plants in three sites
showed an inconsistent trend of variations with respect to
increasing distance from the source. Achakzai et al. (2017a,b) also
reported similar result, where the APTI showed an inconsistent
trend of variations with increasing distance from the source. Re-
sults of the study also revealed that plants exhibited marked
demarcation with respect to their susceptibility to a similar source
of pollution (Table 6). The trend of APTI of plants collected around
brick kilns in Quetta was Elaeagnus angustifolia (21.75) > Medicago
sativa (17.59) > Lepidium sativum (14.21) > Punica granatum
(12.53) > Chenopodium album (10.38) > Triticum aestivum
(8.66) > Prunus armeniaca (8.41) > Vitis vinifera (7.58) > Convolvulus
arvensis (6.02). Furthermore, the trend of variation of air pollution
tolerance indices at Pishin and Mastung were Morus alba
(19.07) > Malcolmia africana (15.13) > Peganum harmala
(12.12) > Lepidium sativum (9.76) > Triticum aestivum (8.64) and
Morus alba (26.82) > Malcolmia africana (21.30) > Peganum harmala
(16.53) > Lepidium sativum (11.37) > Triticum aestivum (11.27)
respectively. According to the classification of Agrawal et al. (1991),
plants are classified into three different categories based on the air
pollution tolerance indices i.e. APTI values less than 16 are classified
as sensitive whereas, those having APTI above than 16 are regarded
as tolerant species. The current study places Elaeagnus angustifolia,
Medicago sativa, Morus alba, Malcolmia africana and Peganum har-
mala in tolerant species whereas, Convolvulus arvensis was found to
be the most sensitive species among all the studied plants (Table 7).
It is also evident from the results that plants exhibited considerable
variation in tolerance upon exposure to different pollutants. It
might be due to the difference in their biochemical parameters (Rai
and Panda, 2014). Conclusively, the tolerant plant species, identi-
fied through the current study could be employed as means of
pollution abatement in the highly polluted areas whereas, the
sensitive species can be recommended as a bio-indicator tool for
the assessment of pollution level (Bharti et al., 2018). The tolerant
plant species reduces significant amount of different types of pol-
lutants in the air thus acting like scavengers for pollutants in the
environment. Similarly, the sensitive plants acts as detective of
pollution. They show visible symptoms of air pollution long before
their effects are observed in the other organisms (Seyyednejad
et al., 2011; Jain et al., 2019).
The results of such biomonitoring studies are handy for a
landscaper to identify the most suitable species to be grown in the

Table 5 Table 6
The impacts of brick kilns pollution on the relative water content (%) of the studied Variations in APTI of plants collected around brick kilns in three districts of
plants in three districts of Balochistan. Balochistan.

Name of plants 100 m 300 m 500 m Name of plants 100 m 300 m 500 m

Quetta Quetta
Triticum aestivum 58.61 ± 4.69 63.17 ± 7.78 61.84 ± 6.37 Triticum aestivum 7.84 ± 0.71 8.07 ± 3.33 10.06 ± 1.74
Chenopodium album 66.35 ± 8.07 64.43 ± 4.75 64.5 ± 4.86 Chenopodium album 9.81 ± 2.10 10.74 ± 4.96 10.57 ± 1.38
Medicago sativa 79.24 ± 9.77 69.98 ± 7.08 77.99 ± 9.33 Medicago sativa 17.41 ± 2.120 17.35 ± 1.03 18.01 ± 5.51
Lepidium sativum 74.93 ± 5.39 77.14 ± 10.57 74.29 ± 5.75 Lepidium sativum 11.52 ± 5.20 15.7 ± 2.80 15.41 ± 3.84
Prunus armeniaca 47.5 ± 6.55 53.59 ± 11.77 54.50 ± 13.12 Prunus armeniaca 8.17 ± 1.73 8.51 ± 0.82 8.56 ± 2.28
Convolvulus arvensis 42.87 ± 11.13 47.39 ± 12.64 47.71 ± 13.44 Convolvulus arvensis 5.35 ± 0.63 6.5 ± 0.23 6.23 ± 1.61
Elaeagnus angustifolia 84.69 ± 7.55 79.82 ± 3.54 83.63 ± 6.61 Elaeagnus angustifolia 21.10 ± 3.59 21.84 ± 1.21 21.4 ± 6.84
Vitis vinifera 46.61 ± 11.02 46.37 ± 11.68 50.76 ± 13.96 Vitis vinifera 6.04 ± 0.59 8.86 ± 2.24 7.84 ± 2.21
Punica granatum 69.25 ± 2.62 70.60 ± 4.17 71.92 ± 5.77 Punica granatum 11.08 ± 1.66 13.48 ± 1.65 13.03 ± 2.34
Pishin Pishin
Triticum aestivum 56.67 ± 7.50 61.08 ± 5.63 65.67 ± 5.05 Triticum aestivum 6.95 ± 1.65 8.12 ± 3.61 10.84 ± 3.61
Peganum harmala 66.26 ± 1.02 65.04 ± 7.74 74.88 ± 3.45 Peganum harmala 11.69 ± 2.52 11.63 ± 0.18 13.02 ± 0.18
Lepidium sativum 61.05 ± 10.60 68.61 ± 11.94 69.12 ± 5.80 Lepidium sativum 7.68 ± 0.56 9.82 ± 3.19 11.78 ± 3.19
Morus alba 80.22 ± 7.90 80.01 ± 9.78 79.92 ± 9.69 Morus alba 18.09 ± 2.26 20.45 ± 4.66 18.65 ± 4.66
Malcolmia africana 76.04 ± 3.44 74.02 ± 7.79 76.82 ± 6.87 Malcolmia africana 15.23 ± 2.37 16.05 ± 2.81 14.1 ± 2.81
Mastung Mastung
Triticum aestivum 57.61 ± 8.74 68.27 ± 7.89 73.02 ± 10.11 Triticum aestivum 11.22 ± 4.31 19.19 ± 3.37 19.19 ± 3.37
Peganum harmala 68.94 ± 3.82 78.10 ± 2.72 80.72 ± 5.06 Peganum harmala 7.93 ± 0.64 12.94 ± 2.50 12.94 ± 2.5
Lepidium sativum 61.05 ± 13.24 67.65 ± 1.13 74.36 ± 9.21 Lepidium sativum 8.65 ± 2.41 12.73 ± 0.28 12.73 ± 0.28
Morus alba 84.72 ± 3.18 86.24 ± 1.96 85.38 ± 2.92 Morus alba 20.25 ± 1.48 30.11 ± 7.27 30.11 ± 7.27
Malcolmia africana 82.89 ± 6.33 81.67 ± 2.39 81.67 ± 1.96 Malcolmia africana 18.45 ± 4.07 22.73 ± 4.17 22.73 ± 4.17
 Khanoranga, S. Khalid / Journal of Cleaner Production 229 (2019) 727e738 733

Table 7 matter) some distance away from the source depending upon
Classification of the studied plants according to APTI values. metrological conditions (Wind speed and direction, humidity and
Name of plants APTI Category temperature). It is obvious that the impacts of pollution source on
Quetta
the environment can be felt far away from the source (Achakzai
Triticum aestivum 8.66 Sensitive et al., 2017a,b). Some other studies have also reported the high
Chenopodium album 10.38 Sensitive concentration of heavy metals in plants and soil around brick kilns
Medicago sativa 17.59 Intermediate (Pandhija and Rai, 2009; Ishaq et al., 2010; Ismail et al., 2012).
Lepidium sativum 14.21 Sensitive
Prunus armeniaca 8.41 Sensitive
Convolvulus arvensis 6.03 Sensitive 3.6.1. Metal accumulation index
Elaeagnus angustifolia 21.75 Intermediate Plants in contaminated environment accumulate different
Vitis vinifera 7.58 Sensitive metals simultaneously. MAI was used to assess the metals accu-
Punica granatum 12.53 Sensitive
mulation efficiencies of plants growing in the proximity of brick
Pishin
Triticum aestivum 8.64 Sensitive
kilns. The results of the current study are summarized in Table 11.
Peganum harmala 12.12 Sensitive According to the current study, Lepidium sativum exhibited the
Lepidium sativum 9.76 Sensitive highest MAI value whereas Malcolmia africana showed the lowest
Morus alba 19.07 Intermediate metal accumulation capacity. Moreover, the trend of MAI for
Malcolmia africana 15.13 Sensitive
studied metals in plant species collected around brick kilns in
Mastung
Triticum aestivum 11.27 Sensitive Quetta was Lepidium sativum (118.08) > Chenopodium album
Peganum harmala 16.53 Sensitive (108.83) > Elaeagnus angustifolia (98.77) > Medicago sativa
Lepidium sativum 11.37 Sensitive (74.87) > Prunus armeniaca (60.87) > Convolvulus arvensis
Morus alba 26.82 Intermediate (57.58) > Vitis vinifera (57.47) > Punica granatum (56.19) > Triticum
Malcolmia africana 21.30 Intermediate
aestivum (48.94). The MAI trend exhibited by plant species
collected around brick kilns in Pishin and Mastung followed, Lepi-
dium sativum (113.81) > Malcolmia africana (61.61) > Triticum aes-
contaminated environment for amelioration purposes. It is also tivum (60.70) > Peganum harmala (50.43) > Morus alba (44.38) and
worth noting that combining a variety of parameters for the esti- Morus alba (70.06) > Lepidium sativum (51.8) > Peganum Harmala
mation of pollution level through plants is more realistic and reli- (50.35) > Triticum aestivum (47.86) > Malcolmia africana (37.83)
able approach rather than assuming the level of pollution through respectively. The results of the current study are in agreement with
single parameter result (Okunlola et al., 2016; Sen et al., 2017). APTI Nadgo
rska-Socha et al. (2017), they studied Melandrium album and
is widely used by other researchers as a significant tool for a Robinia pseudoacacia for heavy metals bimonitoring. The present
landscaper for selecting and identifying the most suitable species to study suggests that Lepidium sativum can grow in soil contaminated
be grown in the urban environment as mean of mitigating pollution with heavy metal(loid)s in the vicinity of brick kilns. Furthermore,
due to rapid growth in urbanization and industrial sectors (Zhang plants also varied in the uptake of heavy metal(loid)s and spatial
et al., 2016; GHassanen et al., 2016). The results of One-way variations were also found among plants growing at different sites.
ANOVA showed that variation with increasing distance from the It might be due to differences in the metal uptake efficiency of
source was statistically insignificant (p > 0.05) at three sites plants and variation in the pollution load at different sites. Plants
(Table 2) whereas, variations in the ATPI among the studied plants exhibiting a higher value of MAI can be used as a barrier between
and study sites were statistically significant (p < 0.05). contaminated and uncontaminated environment. Plants with
higher MAI values have good accumulation capacities and also
3.6. Heavy metal(loid)s content in the studied plants regarded as tolerant species. The greater the MAI, the more efficient
is that plant to be grown in the heavy metal(loid)s contaminated
The concentration of all studied heavy metal(loid)s (except Mn) areas. Indigenous plants with high MAI values can be used in
was found to be beyond the permissible limits of WHO in the polluted areas as nature based solution to combat pollution. Plants
majority of the plants at the study sites (Tables 8e10). In the view of with greater MAI are regarded as tolerant species and can act as
current study, inconsistent trend of variation with distance was sink for heavy metal(loid)s pollution (Jamil et al., 2009; Nadgo
rska-
recorded and the variations where found insignificant (p > 0.05) Socha et al., 2016). The metal accumulation tendencies of the
except Cd (p ¼ 0.002), Cr (0.001) and As (0.01) in Mastung and Fe studied plants were greater than the earlier studies (Liu et al., 2007;
(0.001) in Quetta, respectively. Substantially, significant (p < 0.05) Khan et al., 2011; Monfared et al., 2013).
variations in the heavy metal(loid)s concentration with respect to
site and plant species were also recorded (Table 12). Some plants 4. Conclusion
showed high uptake for one particular metal whereas, the same
plant showed lower accumulation tendency for other heavy metals. Overall results indicate that all the studied parameters showed
Similar, results were also reported by Begum et al. (2015), they significant (p < 0.05) variations among the plant species, and study
found the similar trend of variations of heavy metals by different sites while variations in the level of studied parameters with
plants collected in the vicinity of brick kilns of Fetah Jang, Pakistan. respect to distance from the source (brick kilns) were found
A large number of factors controls the uptake of heavy metals and insignificant (p > 0.05) except Cd, Cr, As and Fe. APTI can be used as
arsenic in plants i.e. soil physiochemical properties, climatic con- an effective tool for phytomonitoring of pollution level. It was
ditions and plants genotypes (Trebolazabala et al., 2017). The calculated through four biochemical parameters namely, total
probable sources of the heavy metals and arsenic in the study area chlorophyll content, ascorbic acid, pH of the leaf extract, and rela-
might be due to the combustion of coal used in the baking of bricks tive water content. Consequently, the results showed that plants
in brick kilns and phosphate fertilizers being used in agricultural respond differentially to the pollution. Hence, Morus alba (26.82),
activities (Proshad et al., 2017; Ravankhah et al., 2017). The varia- Elaeagnus angustifolia (21.75), Malcolmia africana (21.30), Medicago
tions in the heavy metals and arsenic content of plants with sativa (17.59) and Peganum harmala (16.53) were found to be the
increasing distance from the source might be attributed to the most tolerant species whereas, Convolvulus arvensis (6.02) was
fallout of pollutants in various forms (gaseous and particulate found to be the most sensitive species. The most tolerant species
 734
Table 8
Heavy metal(loid)s concentration (mg/kg)± STDEV in the studied plant species collected around brick kilns in Quetta.

Name of plants Distance Cd Cr Pb Cu Mn Zn Ni Co Fe As Hg

Khanoranga, S. Khalid / Journal of Cleaner Production 229 (2019) 727e738

Triticum aestivum 100 m 3.65 ± 1.134 18.74 ± 14.87 36.2 ± 13.11 9.58 ± 4.7 59.98 ± 47.81 31.93 ± 10.1 57.23 ± 27.444 2.5 ± 0.55 1105.63 ± 110.42 1.96 ± 0.41 3.42 ± 0.52
300 m 10.74 ± 1.77 18.06 ± 6.41 37.25 ± 8.76 27.39 ± 5.83 112.28 ± 20.13 21.59 ± 10.54 43.15 ± 5 6.12 ± 2.84 533.66 ± 138.78 2.14 ± 0.14 2.28 ± 0.21
500 m 4.77 ± 3.38 30.4 ± 10.89 41.28 ± 8.11 5.54 ± 2.90 92.71 ± 20.13 49.37 ± 11.75 34.97 ± 13.55 2.95 ± 0.80 975.45 ± 400.84 1.71 ± 0.1 3.12 ± 0.10
Chenopodium album 100 m 2.92 ± 1.73 30.79 ± 1.96 30.77 ± 15.54 2.93 ± 1.54 80.26 ± 6.29 44.81 ± 7.33 50.18 ± 11 4.32 ± 4.42 773.28 ± 146.79 1.49 ± 0.40 1.031 ± 0.13
300 m 3.04 ± 1.52 29.41 ± 16.44 30.66 ± 7.01 5.29 ± 1.39 59.87 ± 36.80 34.28 ± 11.74 51.71 ± 35.16 4.68 ± 2.89 772.63 ± 227.52 1.82 ± 0.10 2.07 ± 0.05
500 m 3.41 ± 2.02 20.61 ± 15.79 29.69 ± 8.24 3.64 ± 1.14 44.1 ± 36.80 62.21 ± 0.56 36.56 ± 17.3 2.79 ± 0.97 661.97 ± 217.89 1.35 ± 0.16 1.51 ± 0.09
Medicago sativa 100 m 5.28 ± 2.85 22.86 ± 17.52 25.67 ± 7.96 21.38 ± 5.19 49.96 ± 13.03 45.41 ± 32.49 63.11 ± 7.19 5.9 ± 3.53 862.34 ± 148.64 1.26 ± 0.21 1.09 ± 0.06
300 m 5.41 ± 1.75 20.14 ± 10.75 29.52 ± 19.09 5.28 ± 0.63 71.13 ± 44.34 40.31 ± 3.37 68.2 ± 17.38 6.89 ± 4.26 523.17 ± 171.54 1.35 ± 0.14 1.72 ± 0.10
500 m 2.8 ± 1.80 35.75 ± 13.91 30.41 ± 7.85 17.86 ± 6.27 149.77 ± 44.34 35.45 ± 12.94 80.4 ± 15.22 3.95 ± 0.51 1119.33 ± 280.20 1.28 ± 0.312 1.24 ± 0.25
Lepidium sativum 100 m 6 ± 1.67 27.24 ± 15.55 28.47 ± 5.25 29.19 ± 39.47 197.28 ± 28.88 38.02 ± 5.27 81.79 ± 21.16 4.28 ± 3.3 789.98 ± 52.21 1.7 ± 0.25 0.75 ± 0.06
300 m 7.39 ± 2.54 31.21 ± 12.90 26.78 ± 5.54 14.82 ± 12.75 99.78 ± 13.46 69.01 ± 36.29 42.75 ± 12.09 3.79 ± 0.88 755.06 ± 135.24 1.78 ± 0.14 0.87 ± 0.13
500 m 6.92 ± 1.65 27.97 ± 13.38 25.06 ± 12.32 15.56 ± 18.85 83.42 ± 13.46 55.66 ± 30.54 63.34 ± 25.01 4.79 ± 1.68 834.06 ± 28.29 1.71 ± 0.17 1.93 ± 0.28
Prunus armeniaca 100 m 7.89 ± 2.72 16.33 ± 18.38 27.03 ± 9.94 9.62 ± 7.2 109.10 ± 0.33 54.06 ± 24.81 66.03 ± 6.72 10 ± 8.17 413.99 ± 96.30 1.11 ± 0.44 2.75 ± 0.22
300 m 5.71 ± 4.72 26.47 ± 23.64 29.17 ± 15.37 9.12 ± 6.77 171.65 ± 14.92 43.9 ± 1.54 62.15 ± 6.62 7.44 ± 4.08 1019.82 ± 356.55 1.18 ± 0.32 2.31 ± 0.18
500 m 7.26 ± 4.94 17.71 ± 6.59 38.4 ± 3.78 13.46 ± 4.78 52.27 ± 14.92 54.35 ± 12.42 55.72 ± 7.01 6.44 ± 1.22 523.93 ± 205.76 1.43 ± 0.32 3.35 ± 0.37
Convolvulus arvensis 100 m 7.41 ± 2.15 22.62 ± 7.62 28.49 ± 9.75 7.70 ± 0.62 143.9 ± 42.79 52.35 ± 26.39 6.92 ± 6 4.07 ± 2.3 1257.53 ± 502.1 2.37 ± 0.42 2.61 ± 0.94
300 m 7.03 ± 1.67 14.67 ± 3.68 20.82 ± 10.72 10.9 ± 5.34 80.01 ± 29.74 32.04 ± 7.30 13.7 ± 3.96 4.64 ± 3.34 617.39 ± 85.56 1.98 ± 0.53 1.93 ± 0.12
500 m 6.86 ± 1.67 13.95 ± 7.11 19.88 ± 6.24 18.16 ± 7.07 68.74 ± 29.74 49.87 ± 27.92 12.37 ± 4.08 7.03 ± 3.37 887.88 ± 32.46 0.86 ± 01.7 1.57 ± 0.87
Elaeagnus angustifolia 100 m 5.06 ± 1.35 16.4 ± 6.42 15.61 ± 2.37 7.36 ± 0.03 98.04 ± 73.44 48.37 ± 13.19 9.86 ± 7.31 5.24 ± 3.36 816.08 ± 75 1.32 ± 1.52 1.47 ± 0.89
300 m 4.65 ± 2.97 15.21 ± 3.63 21.28 ± 6.72 15.06 ± 11.24 106.11 ± 41.41 49.2 ± 11.67 12.28 ± 7.93 5.16 ± 2.03 797.99 ± 184.32 4.59 ± 1.14 1.56 ± 0.66
500 m 5.7 ± 1.90 13.23 ± 13.46 28.34 ± 9.01 11.04 ± 6.25 85.92 ± 41.41 50.57 ± 28.36 25.91 ± 11.86 3.73 ± 0.92 616.35 ± 134.06 3.9 ± 0.91 2.43 ± 0.07
Vitis vinifera 100 m 4.61 ± 1.32 14.48 ± 14.51 26.89 ± 8.48 8.51 ± 1.15 86.58 ± 35.44 60.02 ± 28.93 56.31 ± 32.83 4.43 ± 1.1 622.22 ± 551.55 4.14 ± 0.42 1.17 ± 0.66
300 m 7.78 ± 1.88 9.52 ± 10.8 37.44 ± 9.38 5.45 ± 2.06 73.31 ± 29.10 52.87 ± 26.03 38.94 ± 8.14 5.97 ± 3.15 504.26 ± 91.20 2.64 ± 1.84 1.35 ± 0.75
500 m 7.73 ± 9.12 18.93 ± 14 25.51 ± 5.03 5.69 ± 2.64 70.88 ± 29.10 43.44 ± 5.52 35.57 ± 7.58 4.98 ± 1.3 688.21 ± 362.78 2.69 ± 1.07 1.61 ± 0.78
Punica granatum 100 m 8.57 ± 3.81 15.53 ± 12.40 17.21 ± 2.57 10.41 ± 3.83 68.97 ± 27.26 36.01 ± 5.9 51.9 ± 17.57 9.79 ± 1.03 1042.8 ± 234.6 3.75 ± 0.10 0.99 ± 0.01
300 m 5.95 ± 4.73 12.81 ± 9.48 25.84 ± 13.53 16.02 ± 4.84 80.18 ± 63.27 56.09 ± 23.06 71.53 ± 8.33 11.18 ± 2.61 806.84 ± 355.83 1.91 ± 0.25 0.65 ± 0.05
500 m 8.25 ± 6.09 8.66 ± 6.45 22.54 ± 12.57 20.56 ± 8.09 126.18 ± 63.27 56.81 ± 23.11 53.47 ± 14.58 9.7 ± 4.23 894.38 ± 212.65 1.61 ± 0.42 0.97 ± 0.08
Range ————————— 2.8e10.74 8.66e35.75 15.61e41.28 2.93e29.19 44.1e197.28 21.59.69.01 6.92e81.79 2.5e11.18 413.99e1257.53 0.86e4.59 0.65e3.42
Table 9
Heavy metal(loid) s concentration (mg/kg)± STDEV in the studied plant species collected around brick kilns in Pishin.

Plant Distance Cd Cr Pb Cu Mn Zn Ni Co Fe As Hg

Triticum aestivum 100 m 8.64 ± 3.73 18.09 ± 5.23 42.49 ± 12.75 13.47 ± 5.44 90.04 ± 4.95 60.9 ± 22.72 24.79 ± 20.27 15.99 ± 13.04 795.61 ± 1.69 1.59 ± 0.07 1.89 ± 0.80
300 m 11.17 ± 9.10 20.62 ± 7.81 25.88 ± 7.59 18.69 ± 0.60 54.49 ± 34.35 48.69 ± 12.08 21.44 ± 8.50 5.7 ± 3.93 1319.45 ± 5.03 1.27 ± 0.39 2.47 ± 0.45
500 m 5.65 ± 2.99 35.57 ± 13.28 23.98 ± 17.65 14.69 ± 3.74 64.17 ± 19.31 54.69 ± 24.56 15.82 ± 3.1 5.48 ± 1.92 1122.94 ± 5.4 1.02 ± 0.44 2.63 ± 0.45
Peganum harmala 100 m 10.85 ± 2.74 23.87 ± 17.91 25.24 ± 6.22 8.33 ± 0.45 43.3 ± 40.85 33.8 ± 3.86 49.62 ± 36.32 19.16 ± 23.36 1155.9 ± 5.56 0.59 ± 0.18 1.61 ± 0.78
300 m 12.85 ± 12.70 22.8 ± 8.50 28.01 ± 9.76 34.41 ± 6.06 54.56 ± 40.28 35.34 ± 11.71 32.18 ± 0.25 19.85 ± 23.91 1200.63 ± 4.12 0.76 ± 0.38 1.17 ± 0.17
500 m 15.77 ± 19.53 14.84 ± 2.74 19.79 ± 11.62 21.96 ± 5.32 36.55 ± 29.12 50.44 ± 15.96 28.5 ± 17.19 14.97 ± 19.15 1596.19 ± 8.27 1.21 ± 0.43 1.3 ± 0.17
Lepidium sativum 100 m 17.8 ± 20.89 18.59 ± 9.72 29.38 ± 6.70 13.19 ± 3.68 67.88 ± 15.11 63.86 ± 42.36 48.93 ± 42.32 16.49 ± 19.61 1294.83 ± 3.17 1.65 ± 0.35 1.85 ± 0.31
300 m 23.76 ± 33.74 12.91 ± 7.44 20.61 ± 9.39 22.89 ± 6.04 74.9 ± 31.86 41.78 ± 2.28 36.81 ± 39.26 18.35 ± 21.04 1396.83 ± 4.75 1.21 ± 0.40 1.98 ± 0.89
500 m 26.38 ± 39.51 27.7 ± 21.00 17.29 ± 14.26 28.4 ± 15.84 61.98 ± 35.67 34.56 ± 13.25 47.94 ± 34.39 32.73 ± 43 1092.89 ± 5.71 0.94 ± 0.34 3.52 ± 0.89
Morus alba 100 m 7.26 ± 4.76 20.15 ± 3.39 8.08 ± 0.65 20.89 ± 7.11 46.49 ± 43.88 49.33 ± 23.61 45.76 ± 1.83 20.64 ± 26.79 473.46 ± 3.81 0.71 ± 0.52 1.75 ± 1.10

Khanoranga, S. Khalid / Journal of Cleaner Production 229 (2019) 727e738

300 m 12.36 ± 12.99 32.56 ± 12.73 16.81 ± 18.65 18.21 ± 5.60 58.72 ± 27.10 39.57 ± 2.84 51.95 ± 18.65 17.06 ± 13.56 493.53 ± 2.96 1.48 ± 0.41 1.79 ± 0.19
500 m 13.01 ± 18.36 29.99 ± 17.76 11.19 ± 6.84 25.08 ± 7.22 39.55 ± 2.84 47.43 ± 33.13 46.95 ± 18.17 10.17 ± 10.35 293.69 ± 2.33 1.56 ± 0.20 1.97 ± 0.19
Malcolmia africana 100 m 5.65 ± 4.90 21.49 ± 8.03 29.05 ± 0.61 35.38 ± 6.17 68.09 ± 18.78 42.29 ± 38.63 44.86 ± 21.93 21.38 ± 29.32 686.31 ± 1.89 0.82 ± 0.05 1.35 ± 1
300 m 19.24 ± 22.99 32.66 ± 11.03 7.93 ± 2.35 6.45 ± 1.03 80.92 ± 30.82 26.88 ± 4.55 14.56 ± 3.23 4.97 ± 3.29 613.23 ± 2.61 0.72 ± 0.34 1.59 ± 0.51
500 m 19.02 ± 23.03 22.98 ± 8.32 7.64 ± 0.44 4.55 ± 1.96 85.66 ± 27.23 34.02 ± 14.64 50.54 ± 41.31 3.21 ± 1.16 917.06 ± 4.27 2.15 ± 1.65 1.77 ± 0.51
Range ——— 5.65e26.38 12.91e35.57 7.64e42.49 4.55e35.38 36.55e90.04 26.88e63.86 14.56e51.95 3.21e32.73 293.69e1596.19 0.59e2.15 1.17e3.52

Table 10
Heavy metal(loid)s concentration (mg/kg) ± STDEV in the studied plant species collected around brick kilns in Mastung.

Name of plant Distance Cd Cr Pb Cu Mn Zn Ni Co Fe As Hg

Triticum aestivum 100 m 12.32 ± 0.88 22.1 ± 3.64 29.05 ± 9.61 34.98 ± 5.80 68.09 ± 18.78 29.29 ± 20.93 44.86 ± 21.93 28.05 ± 23.58 686.31 ± 189.54 0.82 ± 0.05 0.75 ± 0.07
300 m 22.58 ± 19.96 33.19 ± 11.47 14.59 ± 5.49 13.28 ± 5.10 80.92 ± 30.82 46.38 ± 31.34 14.56 ± 3.23 21.63 ± 10.61 613.23 ± 260.70 0.72 ± 0.34 2.13 ± 0.19
500 m 9.02 ± 6.64 26.81 ± 8.34 7.64 ± 0.44 12.14 ± 5.05 85.66 ± 27.23 27.68 ± 12.94 50.54 ± 41.31 9.55 ± 5.13 917.06 ± 426.99 2.15 ± 1.65 1.64 ± 0.30
Peganum harmala 100 m 13.91 ± 3.02 20.2 ± 5.18 32.49 ± 24.14 20.58 ± 0.57 199.22 ± 85.78 50.72 ± 28.33 42.84 ± 8.79 27.76 ± 20.05 2052.11 ± 1014.08 3.41 ± 1.73 1.04 ± 0.32
300 m 14.55 ± 4.25 14.39 ± 6.44 40.89 ± 4.63 33.34 ± 9.97 214.2 ± 104.63 50.28 ± 39.15 70.98 ± 14.71 24.11 ± 20.95 2841.13 ± 1302.05 0.91 ± 0.44 0.79 ± 0.19
500 m 6.36 ± 4.53 25.9 ± 1.24 43.69 ± 28.42 18.32 ± 0.39 264.64 ± 141.67 41.85 ± 38.57 70.17 ± 8.88 15.65 ± 22.40 2443.6 ± 740.03 0.88 ± 0.06 1.35 ± 0.15
Lepidium sativum 100 m 14.79 ± 3.97 32.96 ± 4.45 32.24 ± 7.35 34.01 ± 6.93 31.95 ± 20.94 39.8 ± 13.09 57.53 ± 26.09 23.65 ± 20.04 1982.1 ± 828.82 1.04 ± 0.50 1.83 ± 0.14
300 m 13.18 ± 8.72 28.23 ± 7.92 32.05 ± 6.21 32.93 ± 11.93 235.79 ± 145.32 56.9 ± 25.17 57.14 ± 26.06 24.41 ± 18.07 1469.72 ± 214.57 1.34 ± 0.32 1.76 ± 0.40
500 m 2.76 ± 0.54 31.94 ± 9.97 8.3 ± 1.38 33.28 ± 10.25 80.7 ± 68.64 68.65 ± 38.02 54.17 ± 34.70 17.95 ± 27.60 1430.61 ± 252.17 1.41 ± 0.10 1.50 ± 0.10
Morus alba 100 m 15.01 ± 4.07 30.89 ± 2.89 53.12 ± 14.83 68.69 ± 24.32 94.77 ± 14.15 62.6 ± 6.29 40.38 ± 7.08 27.91 ± 21.73 1079.4 ± 120.98 1.35 ± 0.31 1.42 ± 0.72
300 m 12.35 ± 4.13 32.22 ± 9.33 42.3 ± 21.65 37.48 ± 13.89 139.99 ± 50.49 40.33 ± 45.82 51.82 ± 14.56 29.92 ± 19.30 1801.3 ± 754.03 1.36 ± 0.69 2.03 ± 0.64
500 m 7.42 ± 0.53 43.94 ± 11.75 35.32 ± 9.04 21.12 ± 8.71 84.28 ± 15.24 67.3 ± 13.02 37.33 ± 13.59 21.8 ± 24.98 1908.73 ± 700.53 1.40 ± 0.51 2.01 ± 0.46
Malcolmia africana 100 m 15.59 ± 2.56 45.26 ± 31.09 42.43 ± 4.96 57.83 ± 30.84 45.85 ± 6.64 42.38 ± 21.30 66.15 ± 6.98 35.81 ± 9.09 2724.29 ± 1345.14 1.24 ± 0.21 2.34 ± 0.41
300 m 15.59 ± 3.55 47.41 ± 5.25 25.38 ± 6.30 53.74 ± 24.39 119.84 ± 148.64 44.25 ± 32.79 62.62 ± 30.93 27.47 ± 15.22 1096.2 ± 183.86 1.23 ± 0.56 1.93 ± 0.89
500 m 7.78 ± 2.18 58.37 ± 2.52 9.57 ± 1.26 37.81 ± 18.15 127.8 ± 103.10 39.74 ± 2.32 61.26 ± 28.27 41.76 ± 5.44 1608.68 ± 43.31 0.70 ± 0.19 2.36 ± 0.59
Range —— 2.78e22.58 14.39e58.37 7.64e53.69 12.14e68.69 31.95e264.64 27.68e68.65 14.56e70.98 9.55e41.76 613e2841.13 0.70e3.41 0.75e2.36

735
 736
Table 11
MAI of the studied plants in three districts of Balochistan.

Name of plants Cd Cr Pb Cu Mn Zn Ni Co Fe As Hg MAI

Quetta
Triticum aestivum 6.39 ± 3.81 22.40 ± 6.93 38.24 ± 2.68 14.17 ± 11.63 88.32 ± 26.42 34.29 ± 14.04 45.11 ± 11.26 3.86 ± 1.97 871.58 ± 299.8 1.93 ± 0.21 2.94 ± 0.59 48.94
Chenopodium album 3.12 ± 0.25 26.94 ± 5.53 30.37 ± 0.59 3.96 ± 1.21 61.70 ± 17.70 47.1 ± 14.10 46.15 ± 8.34 3.93 ± 1 735.10 ± 64.08 1.55 ± 0.24 1.54 ± 0.52 108.83
Medicago sativa 4.49 ± 1.47 26.25 ± 8.34 28.53 ± 2.53 14.84 ± 8.46 90.29 ± 52.59 40.39 ± 4.98 70.57 ± 8.89 5.58 ± 1.5 834.95 ± 299.02 1.30 ± 0.05 1.35 ± 0.32 74.86
Lepidium sativum 6.77 ± 0.71 28.81 ± 2.11 26.77 ± 1.70 19.86 ± 8.09 126.82 ± 61.56 54.23 ± 25.55 62.63 ± 19.53 4.29 ± 0.5 793.03 ± 39.59 1.73 ± 0.05 1.18 ± 0.65 118.08
Prunus armeniaca 6.96 ± 1.12 20.17 ± 5.5 31.53 ± 6.04 10.73 ± 2.37 111 ± 59.71 50.77 ± 5.95 61.30 ± 5.21 7.96 ± 1.84 652.58 ± 322.75 1.24 ± 0.17 2.80 ± 0.52 60.87
Convolvulus arvensis 7.10 ± 0.28 17.08 ± 4.81 23.06 ± 4.72 12.25 ± 5.36 97.55 ± 40.53 44.75 ± 11.07 10.99 ± 3.59 5.25 ± 1.57 920.94 ± 321.35 1.73 ± 0.78 2.04 ± 0.53 57.58
Elaeagnus angustifolia 5.14 ± 0.53 14.95 ± 1.60 21.74 ± 6.38 11.15 ± 3.85 96.69 ± 10.16 49.38 ± 1.12 16.01 ± 8.65 4.71 ± 0.85 743.47 ± 110.46 3.27 ± 1.72 1.82 ± 0.53 98.77
Vitis vinifera 6.71 ± 1.82 14.31 ± 4.71 29.946 ± 6.53 6.55 ± 1.70 76.92 ± 8.45 52.11 ± 8.32 43.60 ± 11.14 5.13 ± 0.78 604.90 ± 93.19 3.16 ± 0.85 1.38 ± 0.22 57.467
Punica granatum 7.59 ± 1.43 12.34 ± 3.46 21.86 ± 4.36 15.66 ± 5.08 91.77 ± 30.32 49.64 ± 11.81 58.96 ± 10.91 10.22 ± 0.83 914.67 ± 119.28 2.42 ± 1.16 0.87 ± 0.19 56.19
Pishin
Triticum aestivum 8.48 ± 2.76 24.76 ± 9.45 30.78 ± 10.18 15.62 ± 2.73 69.57 ± 18.38 54.76 ± 6.11 20.68 ± 4.53 9.06 ± 6 1079.33 ± 264.63 1.29 ± 0.28 2.33 ± 0.39 47.86
Peganum harmala 13.15 ± 2.48 20.50 ± 4.94 24.35 ± 4.28 21.57 ± 13.04 44.80 ± 9.10 39.86 ± 9.20 36.77 ± 11.28 17.99 ± 2.64 1317.57 ± 242.322 0.85 ± 0.33 1.36 ± 0.23 50.35

Khanoranga, S. Khalid / Journal of Cleaner Production 229 (2019) 727e738

Lepidium sativum 22.65 ± 4.40 19.73 ± 7.46 22.42 ± 6.25 21.49 ± 7.70 68.25 ± 6.47 46.73 ± 15.27 44.56 ± 6.73 22.52 ± 8.88 1261.52 ± 154.69 1.27 ± 0.36 2.45 ± 0.93 51.28
Morus alba 10.88 ± 3.15 27.57 ± 6.55 12.03 ± 4.43 21.40 ± 3.46 48.25 ± 9.71 45.44 ± 5.18 48.22 ± 3.28 15.96 ± 5.32 420.23 ± 110.04 1.25 ± 0.47 1.84 ± 0.12 70.06
Malcolmia africana 14.64 ± 7.78 25.71 ± 6.07 14.87 ± 12.28 15.45 ± 17.28 78.23 ± 9.09 34.39 ± 7.71 36.65 ± 19.34 9.85 ± 10.02 738.87 ± 158.59 1.23 ± 0.80 1.57 ± 0.21 37.83
Mastung
Triticum aestivum 14.64 ± 7.07 27.66 ± 5.15 17.09 ± 10.92 20.13 ± 12.87 78.23 ± 9.09 34.45 ± 10.36 36.65 ± 19.34 19.74 ± 9.39 738.87 ± 158.58 1.23 ± 0.80 1.51 ± 0.70 60.70
Peganum harmala 11.61 ± 4.56 20.16 ± 5.76 39.02 ± 5.83 24.08 ± 8.10 226.02 ± 34.28 47.62 ± 4.99 61.33 ± 16.01 22.51 ± 6.21 2445.60 ± 394.52 1.73 ± 1.45 1.06 ± 0.28 50.45
Lepidium sativum 10.24 ± 6.53 31.07 ± 2.45 24.2 ± 13.77 33.41 ± 0.55 116.15 ± 106.44 55.11 ± 14.51 56.28 ± 11.84 22 ± 3.53 1627.48 ± 307.74 1.26 ± 0.20 1.70 ± 0.18 113.81
Morus alba 11.59 ± 3.85 35.69 ± 7.18 43.58 ± 8.97 42.43 ± 24.17 106.35 ± 29.61 56.75 ± 14.41 43.18 ± 17.64 26.54 ± 4.23 1596.48 ± 451.01 1.37 ± 0.03 1.82 ± 0.35 44.38
Malcolmia africana 12.97 ± 4.54 50.35 ± 7.03 25.8 ± 16.43 49.79 ± 10.58 97.83 ± 45.19 42.12 ± 2.26 63.34 ± 12.53 35.01 ± 7.18 1809.72 ± 832.46 1.06 ± 0.31 2.21 ± 0.25 61.61
Declaration of interest

agencies in the public, commercial or not for profit sectors.

Funding

to be grown near the pollution sources.

the human health, these tolerant species are highly recommended
like scavengers of pollution. With the increased risk of pollution on
used for the reclamation of soil pollution with heavy metals acting
soil pollution with heavy metals while the tolerant species can be
species. The sensitive metal species can be used as an indicator of
those with low metal accumulation index regarded as sensitive
Plant showing highest MAI can be used as tolerant species whereas
africana (37.83) showed the lowest metal accumulation capacity.
sativum (118.08) displayed the highest MAI whereas; Malcolmia
showed that plant varied in metal accumulation capacity. Lepidium
contamination in the certain area. The results of the study also
according to APTI values can be regarded as biomarkers of
can be used as a sink for pollutants whereas; the sensitive species

*p is significant at the level of 0.05.

increasing distance from the source, among the plant species and the study sites.
Result of One Way ANOVA signifying variation in studied heavy metal (liod)s with
Table 12
Study sites

Hg
Study sites

As
Study sites

Fe
Study sites

Co
Study sites

Zn
Study sites

Mn
Study sites

Cu
Study sites

Pb
Study sites

Cr
Study sites

Cd

Variable
None.

This research did not receive any specific grant from funding

0.01*
Mastung
Pishin
Quetta
0.000*
Mastung
Pishin
Quetta
0.002*
Mastung
Pishin
Quetta
0.000*
Mastung
Pishin
Quetta
0.05*
Mastung
Pishin
Quetta
0.01*
Mastung
Pishin
Quetta
0.000*
Mastung
Pishin
Quetta
0.01*
Mastung
Pishin
Quetta
0.01*
Mastung
Pishin
Quetta
0.04*
Mastung
Pishin
Quetta

Study site
0.96
0.86
0.001*

0.36
0.49
0.64

0.89
0.24
0.42

0.32
0.57
0.76

0.2
0.11
0.99

0.17
0.21
0.61

0.001*
0.42
0.95

0.002*
0.25
0.78

Distance
0.65
0.32
0.65

0.01*
0.51
0.77
0.001*
0.001*
0.002*

0.004*
0.000*
0.002*

0.003*
0.001*
0.01*

0.000*
0.03*
0.002*

0.003*
0.001*
0.02*

0.03*
0.01*
0.000*

0.02*
0.0001*
0.000*

0.03*
0.01*
0.000*

0.01*
0.000*
0.000*

0.000*
0.04*
0.001*

Plant species
 Khanoranga, S. Khalid / Journal of Cleaner Production 229 (2019) 727e738
Acknowledgment
The first author graciously acknowledges Sardar Bahadur Khan
Women’s University Quetta, Balochistan and Higher Education
Commission (HEC) Pakistan by providing a scholarship for her Ph.D.
studies.
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