Abstract
This study aimed to investigate the lead (Pb) and cadmium (Cd) concentrations in the soil and plants (medicinal and fodder) grown in chromite mining-affected areas, Northern Pakistan. Soil and plant samples were collected and analyzed for Pb and Cd concentrations using atomic absorption spectrometer. Soil pollution load indices (PLIs) were greater than 2 for both Cd and Pb, indicating high level of contamination in the study area. Furthermore, Cd concentrations in the soil surrounding the mining sites exceeded the maximum allowable limit (MAL) (0.6 mg kg−1), while the concentrations of Pb were lower than the MAL (350 mg kg−1) set by State Environmental Protection Administration (SEPA) for agriculture soil. The concentrations of Cd and Pb were significantly higher (P < 0.001) in the soil of the mining-contaminated sites as compared to the reference site, which can be attributed to the dispersion of toxic heavy metals, present in the bed rocks and waste of the mines. The concentrations of Pb and Cd in majority of medicinal and fodder plant species grown in surrounding areas of mines were higher than their MALs set by World Health Organization/Food Agriculture Organization (WHO/FAO) for herbal (10 and 0.3 mg kg−1, respectively) and edible (0.3 and 0.2 mg kg−1, respectively) plants. The high concentrations of Cd and Pb may cause contamination of the food chain and health risk.
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Introduction
The local flora is an important source of traditional medicines that are used for the treatment of various diseases. More than 50,000 plant species have been used for medicinal purposes (Bako et al. 2005). Local people get knowledge from their ancestors about the utilization of medicinal plants. A major part of Pakistan is quite rich in medicinal herbs due to its healthy climate (Abbasi et al. 2010a, b). Heavy metals such as lead (Pb), cadmium (Cd), zinc (Zn), and copper (Cu) are considered as global environmental contaminants. These metals have both natural (weathering of parent rocks and ore deposits) and man-made (mining, industrial emission; smelting, waste water irrigation and application of fertilizers) sources (Nawab et al. 2015; Khan et al. 2013a, 2013b; Wei and Yang 2010). Mining activities cause serious adverse effects on plants and soil (Jung 2008) which are mostly connected with open dumping of mine tailings that usually affect the condition of natural plants growing on it (Nawab et al. 2015; Nouri et al. 2011). Native plant species growing on mine-affected sites have greater potential for Pb and Cd accumulation considering the combine pollution of most contaminated sites (Zhao et al. 2014). Plant species can tolerate these severe conditions up to some level. However, high heavy metal concentrations in medicinal plants can cause stress and stomata resistance (Shah et al. 2009; Fayiega et al. 2004). Heavy metals play an important role in food chain contamination (Waqas et al. 2015); ruminants such as cattle, sheep, and goats feed on fodder grasses and accumulate heavy metals over time. It is now well understood that there is transfer of toxic heavy metals from contaminated soil to plants and from plants to livestock (Oskaron et al. 1992). The toxicity of heavy metals in the food chain increases as the heavy metal concentrations exceed the maximum allowable limits (MALs) in the soil. Mostly, the health risk is associated with toxic metal-contaminated soil or dust deposited on plants (Holmgren et al. 1993; Carrington and Bolger 1992). Therefore, grazing animals are more at risk as fodder grasses are consumed directly without being washed.
Pb and Cd are toxic pollutants, and they are not known for any significant biological functions. They rather produce different toxic effects in animals and human beings, which may result in undesirable biochemical and physiological functions (Khan et al. 2014). Abnormal liver disorders and plasma hormonal changes have been reported in cows that were exposed to Pb and Cd in industrial areas (Ogundiran et al. 2012; Swarup et al. 2007).
Plants play an important role for the transformation of heavy metals such as Cd and Pb from contaminated soils to humans (Khan et al. 2015). In polluted soil, the grown plants can uptake more heavy metals. Cd and Pb were chosen for risk assessment because of their high toxicity or comparatively high levels in all of the collected rice samples in previous research. Cd is toxic to the kidney and has a long biological half-life in human. Cd also affects lungs, reproductive system, kidneys, and bones (Godt et al. 2006). Pb has shown to be associated with densification of central nervous system and can cause various health problems like anemia, neurological disorders, hyperactivity, and enzyme changes in humans (Muhammad et al. 2011; Marsden 2003; Chamannejadian 2011). Previous studies indicated that overdose or prolonged ingestion of medicinal plants leads to the chronic accumulation of different elements and hence creates various health problems (Sharma et al. 2009; WHO 1992). Therefore, it is important to screen out the elemental concentrations in medicinal plants for their quality control insurance (Kunle et al. 2012; Arceusz et al. 2010; Liang et al. 2004). Assessment of toxic metals in raw herbal material and finished products must be ensured. Recently, several research works have been focused on heavy metal concentrations in different medicinal plants (Hussain et al. 2011; Baye and Hymete 2010).
In the view of the previous research work, the current study is aimed to evaluate the Cr associated toxic metals like Pb and Cd levels in mine-affected soil, medicinal herbs, and fodder grasses that are locally used in the study area. The pollution load index and transfer factor of selected elements were also investigated.
Materials and method
Study area
The study area is mainly comprised of mining-affected sites (MAS) that are Shangla District (MAS1), Malakand Agency (MAS2), and Mohmand Agency (MAS3) in northern parts of Pakistan. Geographically, MAS1 lies between latitude 34, 31, to 33°, 08° N and longitude 72, 33, to 73°, 01° E with a total area of 1586 km2 and elevation of 3164 m above from mean sea level. MAS1 is bound on the east by district Batagram and tribal area of Kala Dhaka along which the river Indus flows for about 75 km, on the west by district Swat, on the south by district Buner and tribal area on Kala Dahka, and on the north by district Kohistan.
MAS2 is located between latitude 34° 30′ N and longitude 71° 45′ E and stretches over an area of about 95,200 ha (Fig. 1). The area is bounded on the north by mountainous range of Swat and lower Dir, on the west by mountainous range of Bajur and Mohmand Agency, on the east by Buner, southeast by Mardan District, and southwest by Charsada District. MAS3 is located between latitude 34° 22′ 20″ N and longitude 71° 27′ 26″ E. Bajaur Agency is in the north, Khyber Agency is in the south, Malakand Agency and Charsada District are in the east, and Peshawar District is in the southeast of Mohmand Agency. Geologically, the MAS1, MAS2, and MAS3 are mainly comprised of mafic and ultramafic rocks (Searle and Khan 1996). These rocks are hosting chromite deposits and at some places lead-zinc, copper, and manganese ores are present where small-scale minings are in progress. The study was conducted in these areas because the flora is enriched with medicinal and fodder plants and majority of the people use the medicinal plants for various health problems, while the fodder plants consume by the cows, goats, and sheeps in the study area.
Background sampling area
For background sampling, Charsadda area was selected which has lacustrine soil deposits with no contamination from the mafic and ultramafic rocks (Shah and Tariq 2007). It is 20–170 km away from contaminated sampling site. Therefore, for comparison purposes, soil and plant samples were collected for background heavy metal concentrations.
Soil and plant sampling
The soil samples were collected with auger (from where the plant samples uprooted, n = 115) from the upper horizon (0–20 cm). Organic matter, gravels, pebbles, and twigs were removed with hands from the collected soil samples and were kept in the kraft papers. Plants samples were randomly collected, properly marked, and stored in polythene bags. Herbarium sheets for each plant species were prepared, and plants were identified with the help of taxonomist. Names of the collected plants with their common uses are given in Table 1. Both soil and plant species were transported to the Department of Environmental Sciences, University of Peshawar, Pakistan for further analysis.
Preparation and digestion of soil samples
Soil samples were air dried at room temperature and passed through ≤2 mm mesh for further analysis. The subsamples were analyzed for the physicochemical parameters like soil texture, pH, electrical conductivity (EC), and soil organic matters (SOMs) according to the standard procedures. For heavy metal extraction, wet digestion method (WDM) was used (Khan et al. 2013a; Macalalad et al. 1988). Dried soil samples of 0.5 g were taken in Teflon beakers, and 15 ml of aqua regia (1:3 HNO3 and HCl) was added to each beaker. The samples were kept overnight and then gently heated on hot plate at 80 °C until the appearance of transparent extract was observed. The digested extracts were filtered into clean volumetric flasks and diluted up to 100 ml with double deionized water for further analyses. Digestion was performed in triplicates.
Preparation and digestion of plant samples
Plants were washed with double deionized water, separated into roots and shoots and oven dried at 70 °C. The samples were ground into powder with electric grinder. About 1 g of each sample was taken in beaker digested with 15 ml mixture of perchloric (HClO4) and nitric acid (HNO3) in the ratio of 1:4 (Khan et al. 2013a). The samples were kept overnight. Each sample was heated on hot plate at low temperature until transparent solution was observed. After cooling, the solution was filtered and diluted with double deionized water up to 100 ml for further interpretation. Like soil, digestion of plants was also performed in triplicates
Analytical procedure and quality control
Analytical grade chemicals were used for sample preparation and analysis. Standards for each heavy metal were prepared according to the procedure adopted by Khan et al. (2008). The concentrations of Cd and Pb in the plant and soil samples were analyzed using (AAS Perkin-Elmer A-700). The standard reference soil and plant materials (GBW-07406 (GSS-6) and GBW-07602 (GSV-1), respectively, were purchased from National Research Centre for Certified Reference Materials, China) and blank samples were included in each sample batch to verify the accuracy and precision of the digestion procedure and subsequent analyses. The accuracy and precision were found within 90–95 % confidence limit. All analyses were performed in triplicates at the National Center for Excellence in Geology (NCEG), University of Peshawar, Pakistan.
Contamination factor
Contamination factor (CF) is a ratio obtained from heavy metal concentrations in contaminated and background sites, as adopted by Mmolawa et al. (2010).
where Cm represents the concentrations of metals in contaminated and background sites, respectively
Pollution load index
In this study, the pollution load index (PLI) was calculated by the following formula adopted from Tomlinson et al. (1980).
where n is the number of metals and Cf is the contamination factor value.
Bioaccumulation factors
Heavy metal concentrations were calculated in the extracts of roots, shoots, and soils on dry weight (d.w) basis. Root concentration factors (RCFs) and shoot concentration factors (SCFs) are often used for contaminant concentrations in plants because heavy metal accumulation by plants is one of the main source for pollutants to enter in to food chain. RCFs and SCFs were calculated according to formula adopted from (Khan and Cao 2012).
where C root, C shoot, and C soil represent heavy metal concentrations in root, shoot, and soil on dry d.w, respectively.
Translocation factor
Translocation factor (TF) is a ratio, calculated to determine relative translocation of metals from root to shoot of the plant species (Gupta et al. 2008).
where C is the contaminant concentrations in shoot and root samples of the selected plant species.
Statistical analyses
The data was statistically analyzed using the one-way analysis of variance (ANOVA) and Pearson correlation provided in SPSS (version 21). Mean and standard deviation were calculated using Statistix (version 8.1)
Results and discussion
Soil contamination
Table 2 summarizes the physicochemical properties of the soil samples collected from Shangla District, Mohmand Agency, Malakand Agency, and the reference sites. The soil pH values ranged from 5.5 to 8.2, EC ranged from 0.014 to 1.3 mS cm−1, and the SOMs ranged from 1.75 to 3.8 %. Almost all the soil properties varied in the study area except the soil class that was loamy sand. This variation in the soil physical properties may be due to the different environmental conditions (rainfall, altitude, and climate) of the study area.
Figure 2a represents the Pb and Cd concentrations in the soil samples collected from different locations. Pb concentrations in the study area ranged from 7 to 82 mg kg−1 and the Cd from 0.5 to 8 mg kg−1. Highest mean Pb concentration (49.9 mg kg−1) was reported in Malakand Agency, while the lowest (34.2 mg kg−1) in Shangla. Highest Cd mean concentration was found in Malakand Agency (4.28 mg kg−1), while the lowest in Shangla (3.39 mg kg−1). The Pb and Cd concentrations in the soil samples of Shangla District, and Mohmand and Malakand agencies were significantly higher (P ≤ 0.001) than the reference soil. However, the results showed that Pb concentrations were below the permissible limit (350 mg kg−1) set for agriculture soils by (SEPA 1995), while Cd concentrations were observed multifold higher than the permissible limit (0.6 mg kg−1) as shown in Table 3.
Contamination factor and pollution load index
Figure 2b summarizes the values of Pb and Cd CF and PLI. The PLI values were >2 in the soil samples of Shangla District and Mohmand and Malakand agencies. The CF and PLI values for Pb and Cd were in order of Malakand Agency > Mohmand Agency > Shangla District. The PLI showed that the soil of MAS2 site was highly contaminated as compared to MAS1 and MAS3. This high contamination could be due to the bed rocks, mining activities, and fossil fuel combustion in the study area.
Pb and Cd concentration in plant species
Medicinal plant species
Table 3 represents the concentration of Pb and Cd in plant roots and shoots collected from the study area. The concentration of Pb in the roots of the plant species ranged from below detection limit (BDL) to 45 mg kg−1. The highest mean concentration (39.7 mg kg−1) was reported in Zanthoxylum armatum and the lowest (BDL) in Solanum xanthocarpum. The concentration of Pb in the shoots of the plant species ranged from BDL to 28.4 mg kg−1. The highest mean concentration (20.6 mg kg−1) was reported in Z. armatum and lowest (BDL) in S. xanthocarpum and Pantago lenceolata. The concentrations of Pb in 50 % medicinal plant samples exceeded safe limits (10 mg kg−1) set by WHO (2007). Pb can cause various health risks like anemia, neurological disorders, hyperactivity, and enzyme changes in humans (Marsden 2003). In this study, the concentrations of Pb in medicinal plants were higher than those reported by Baye and Hymete (2010) in medicinal plants collected from environmentally different sites in Ethiopia.
The concentrations of Cd in the roots of the selected medicinal plant species ranged from 0.07 to 6 mg kg−1 with highest mean concentration (4.63 mg kg−1) reported in Razia stracta and lowest (0.3 mg kg−1) in Tribulus terrestris. The concentrations of Cd in the shoots ranged from 0.08 to 7.4 mg kg−1, with the highest mean concentration (5 mg kg−1) in R. stracta and lowest (0.2 mg kg−1) in T. terrestris. Cd toxicity affect plant cells, even at low concentrations (Dai et al. 2012). High concentration of Cd is toxic to plants for a number of reasons, which inhibit germination, chlorosis of leaf, and plant biomass reduction (Wang et al. 2008). In 100 % plant samples, the Cd concentration exceeded the safe limits (0.3 mg kg−1) set by WHO (2007). Cd accumulates in the human body and has a long biological life, which affects the lungs, kidneys, liver, bone, cardiovascular system, and immune system (Dai et al. 2011).
Almost all the medicinal plant species showed detectable concentrations of Pb and Cd in samples. The one-way ANOVA result showed that the Pb and Cd concentrations in roots and shoots of the selected plant species were significantly (P < 0.001) higher than the reference plant species. Considering the MAL of Pb (10 mg kg−1) and Cd (0.3 mg kg−1) set by WHO (2007) for medicinal herb, majority of the plant species exceeded these limits and showed high enrichment for the selected metals. The concentrations of Cd and Pb in medicinal plants also exceeded from the study conducted by Ebrahim et al. (2012) in Sudan. The heavy metal concentrations were within the permissible limit set by WHO (2007). Similar study was also conducted by Kulhari et al. (2013) in environmentally diverse locations in Northwest India. They also found Cd and Pb within the permissible limit set by WHO (2007). High concentration of heavy metals may pose serious problem on quality of medicinal plants and their products (Baye and Hymete 2010, 2013). To improve quality standards for herbal medicines, it is necessary to examine the concentrations of toxic heavy metals in medicinal plants (Cao et al. 2009). The present results indicate that there is a serious potential health risk associated with Cd and Pb in medicinal plants that threatens inhabitants of the study area as majority of the local people uses these species for various medicinal purposes.
Fodder plant species
Table 4 represents the concentrations of Pb and Cd in fodder plant species collected from the study area. The Pb concentrations in roots ranged from 2 to 17 mg kg−1, while in shoots ranged from 1 to 11 mg kg−1. The highest mean concentration in root (11.6 mg kg−1) and shoot (7 mg kg−1) was found in Sonneratia griffithii, while the lowest in root (3.66 mg kg−1) and shoot (2 mg kg−1) of Aristida cyanantha, respectively. Cd concentrations in roots ranged from 1.1 to 5.9 mg kg−1, while in shoots, it ranged from 1 to 7 mg kg−1. The highest mean concentrations in root (4.43 mg kg−1) and shoot (5.66 mg kg−1) was reported in Apluda mutica, and lowest was found in root (1.76 mg kg−1) and shoot (1.41 mg kg−1) of Cenchrus ciliaris (Table 3). Almost all fodder species exceeded the safe limit of WHO (2007) for Pb (0.31 mg kg−1) and Cd (0.2 mg kg−1) in edible plants. Pb is highly toxic to animals at a level of 30 mg kg−1 in diet on a d.w basis (FAO 1992) and leads to different problems in red blood cell synthesis (NRCC 1978). The Pb and Cd concentrations in fodder plant species were significantly (P < 0.001) higher than the reference site. Previously, Pb contamination has been reported from natural and anthropogenic sources (Rozso et al. 2003). Pb concentrations in fodder plants grown in agriculture areas, industrial area, and busy highways showed that Pb contamination was higher in industrial and highway sites as compared to agriculture sites. Mor (2005) also reported high Pb concentrations in fodder plants grown in agriculture areas of Busra, Turkey. Cd rapidly accumulates in kidney and other organs of animals, therefore, can create potential hazards for human health after consumption (Canadian Council of Resource and Environment Ministers (CCREM), 1995). The United State Environmental Protection Agency (USEPA) reported that the continuous intake of Pb in diet from 2 to 8 mg kg−1 of body weight day−1 can cause death in most animals (USEPA 1993). Our present study highlights that Pb and Cd concentrations in majority of fodder grasses were above the threshold level (10 and 0.3 mg kg−1, respectively) in mining areas. Such high concentrations of these metals may pose health problem for grazing animals (cows, sheeps, and goats) and local community in the study area.
Contamination and translocation factors of Pb and Cd in medicinal and fodder plant species
Table 4 represents the CF and TF values for plant species in MAS1, MAS2, and MAS3 sites. The CF value for Pb and Cd highly varied among the selected plant species. Highest CF value (×6.9) for Pb was reported in Z. armatum and lowest (BDL) in medicinal plants such as S. xanthocarpum and P. lanceolata. The highest CF (×18) for Cd was reported in medicinal plant (Sisymbrium irio), while the lowest (×0.6) was reported in medicinal (Indigofera heterantha). The CF values of Pb and Cd were reported greater than 1 in 88 and 97 % plant species, respectively.
The TF indicates internal metal transportation from root to shoots. The present study revealed that Pb accumulated by the medicinal herbs and fodder plants growing near chromite mines was largely retained in roots that have TF values <1 (Table 4). The highest TF value (1.00) for Pb was reported in medicinal plant (Artemisia scoparia), while the lowest (BDL) in S. xanthocarpum and P. lanceolata.
The TF values for Cd were greatly varied among the selected medicinal and fodder plant species. Highest TF value (3.04) for Cd was reported in Solanum surattense, while lowest (0.5) in P. lenceolata. Out of 32 plant species, 13 plants showed TF values >1, while 19 plant species showed TF value <1. Unlike medicinal plants, all the fodder plant species showed CF and TF values at medium level for both Pb and Cd.
Bioaccumulation factor of Pb and Cd in medicinal and fodder plant species
Bioaccumulation factor for Pb and Cd was calculated for roots and shoots (Table 4). The RCF values for Pb in the study area ranged from BDL to 0.8. The highest concentration was reported in medicinal plant Z. armatum and the lowest in S. xanthocarpum. No plant species in the study area showed RCF value greater than 1 for Pb. Similarly, the RCF values for Cd ranged from 0.1 to 1.6 with the highest value reported in fodder plant S. griffithii and lowest in medicinal plant Cynodon dactylon. The SCF values for Pb ranged from BDL to 0.41, with highest value in medicinal plant C. dactylon and lowest in medicinal plant S. xanthocarpum and P. lanceolata. In almost all plant species, SCF values for Pb were found less than 1. The SCF values for Cd ranged from 0.06 to 4.27 with the highest SCF value in medicinal plant S. surattense and lowest in C. dactylon. The medicinal plant species showed SCF value greater than 1 for Cd in S. surattense (4.27), Calotropis procera (1.81), Lotus corniculatus (1), S. irio (1.27), and Z. armatum (1.27) and the fodder plant species such as Dichantum annulatum (1.13), Heteropogon contortus (1.21), S. griffithii (1.92), and A. mutica (1.13). These plant species are generally used for medicinal and fodder purposes in the study area (Table 1). Therefore, such high concentrations in the shoots of these plant species can create health problems in the study area for both human and animals.
Pearson’s correlation
Pearson’s correlation was used to correlate the concentrations of Pb and Cd in the (soil–plant roots) and (soil–plant shoots) samples of the study area. The correlation matrix for Pb between soil and plant roots was strong (r = 0.610), followed by correlation between soil and plant shoots (r = 0.593). Similarly, the correlation matrix for Cd between soil and plant roots was slightly weak (r = 0.458) than the correlation between soil and plant shoots (r = 0.52). The results indicate that these metals originate from the same polluting source. The significant correlation coefficients P < 0.01 between Pb and Cd (soil–plant roots) and (soil–plant shoots) can be attributed to anthropogenic (chromite mining and fossil fuel combustion) activities in the study area.
Conclusion
The current research work has shown high levels of Pb and Cd contamination in the soil, medicinal, and fodder plants species along MAS1, MAS2, and MAS3 in Northern Pakistan. The results clearly showed that PLI values for Pb and Cd in soil of study area were greater than 2. MAS2 was highly contaminated as compared to MAS3 and MAS1. The concentrations of Pb and Cd in soil, medicinal, and fodder plant species surrounding the mine areas were significantly (P < 0.001) higher than the reference site and showed multifold enrichment. Cd concentrations exceeded its MAL in soil, while Pb was observed within its MAL. The Pb and Cd concentrations in the majority of medicinal and fodder plants exceeded the safe limits set by FAO/WHO for herbal and edible plants of the study area. Such high contamination with toxic metals may be a threat to the local community; therefore, this study suggests that both medicinal and fodder plant species should be analyzed for heavy metal concentrations in the contaminated sites before utilization.
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Acknowledgments
The financial assistance was provided by the Higher Education Commission Pakistan in the form of Ph.D indigenous scholarship, University of Peshawar, Pakistan and funded by the Chinese Academy of Sciences Key Deployment Project (Project No. KZZD-EW-16-02). Mr. Javed Nawab thanks Chairman and Executive Director Environmental Protection Society Saidu Sharif, Swat for facilitating the field work.
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Nawab, J., Khan, S., Shah, M.T. et al. Contamination of soil, medicinal, and fodder plants with lead and cadmium present in mine-affected areas, Northern Pakistan. Environ Monit Assess 187, 605 (2015). https://doi.org/10.1007/s10661-015-4807-9
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DOI: https://doi.org/10.1007/s10661-015-4807-9