Distribution of heavy metals and arsenic in soils and

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CHNAES-00559; No of Pages 5 Acta Ecologica Sinica xxx (2018) xxx–xxx

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Distribution of heavy metals and arsenic in soils and indigenous plants near an iron ore mine in northwest Iran S. Maryam Hosseini a,⁎, Maryam Rezazadeh a, Azam Salimi a, Mahlagha Ghorbanli b,1 a b

Department of Plant Sciences, Faculty of Biological Sciences, Kharazmi University, Tehran, Iran Department of Biology, Islamic Azad University, Gorgan Branch, Gorgan, Iran

a r t i c l e

i n f o

Article history: Received 4 February 2017 Received in revised form 15 February 2018 Accepted 26 February 2018 Available online xxxx Keywords: Mining activity Phytoremediation Dactylis glomerata Scleranthus orientalis

a b s t r a c t Heavy metal contaminations in the environment of mining area have become a global problem. The vicinity of an iron ore mine was investigated to estimate the concentrations of As, Pb, Cd, Mn, Ni, Zn, and Cr in the soil and the feasibility of using native plants for phytoremediation. For this, concentrations of elements in soil samples collected and were analyzed by inductivity coupled plasma optical emission spectrometry. The concentrations of heavy metals and arsenic in the roots and aerial parts of Dactylis glomerata L. and Scleranthus orientalis Rössler were analyzed by inductively coupled plasma mass spectrometer too. As concentrations in the samples surpassed the soil toxicity threshold. Cd concentration in soil samples was considerably high next to mine pit. Neither species was identified as a hyperaccumulator, but both species could be considered as excluder plants for As. © 2018 Published by Elsevier B.V. on behalf of Ecological Society of China.

1. Introduction

2. Materials and methods

Heavy-metal pollution is one of the world's most environmental concerns because of the distribution and toxicity of heavy metals [1,2]. The disposal of mine waste in an open mine pit is a serious environmental problem [3]. Toxic mine waste contaminates the surrounding ecosystem [4] and also adversely affects the diversity of vegetal species and can inhibit the development of natural vegetation of the environment [5]. Some vegetal species are able to tolerate waste materials surrounding a mine and even accumulate metals from mine soils [6]. These tolerant species can be used for phytoremediation because of their capacity to uptake and accumulate toxic elements [7]. More than 500 species have been identified as accumulating high contents of trace metals [8]. Iran is one of the world's 15 most mineral-rich countries and one of the world's main mineral producers [9]. There is much metalcontaminated soil and a strong need to investigate metal values in soils and plants throughout Iran [10]. The objectives of the present study were (1) to record the concentrations of heavy metal(loid)s in the soil at selected sites around the Moeil mine and in the roots and aerial parts of Dactylis glomerata and Scleranthus orientalis (2) to compare metal concentrations in the aerial parts with those in roots and soil, and (3) to assess the feasibility of using the two species of plants for phytoremediation (i.e., phytoextraction and phytostabilization).

2.1. Study area

⁎ Corresponding author at: No. 43, South Mofatteh Ave., Tehran 1571914911, Iran. E-mail address: [email protected] (S.M. Hosseini). 1 Deceased.

The Moeil mine, the largest hematite iron ore mine in the province of Ardabil, is located south of the village of Moeil and 16 km south of the city of Meshginshahr in northwest Iran (38° 17′ 19″ N, 47° 42′ 54″ E) (Fig. 1). The major metalliferous minerals are hematite and limonite and minor minerals are goethite and jarosite. The original reserve of the mine was around 2 Mt of ore. Exploitation began in 2003 and lasted until 2013, and annual production was 35,000 tons. The area has mountainous topography and is mild in summer and cold and snowy in winter. The maximum and minimum temperatures are 17 and −28 °C respectively. The average precipitation is 450 mm. The altitude is approximately 2223 m above sea level. Owing to the harsh climate, there is a low diversity and limited distribution of plant species in the study area. There are no trees or shrubs in the vicinity of the mine, and vegetation is dominated by annual and perennial herbs (e.g., Agropyron repens L. and Cynodon dactylon L.). Far from the mine center at, for example, sites 2 and 4 shown in Fig. 1, Ranunculus arvensis L. can be seen. Dactylis glomerata L. and Scleranthus orientalis Rössler are the most dominant flora in the metal-polluted area. Dactylis glomerata L. from the Poaceae family is highly drought resistant and a summer active species and Scleranthus orientalis Rössler from the Caryophyllaceae family is a native plant species in the Middle East and widely distributed in Iran. These two species are tolerant to conditions in the contaminated area.

https://doi.org/10.1016/j.chnaes.2018.02.004 1872-2032/© 2018 Published by Elsevier B.V. on behalf of Ecological Society of China.

Please cite this article as: S.M. Hosseini, et al., Distribution of heavy metals and arsenic in soils and indigenous plants near an iron ore mine in northwest Iran, Acta Ecologica Sinica (2018), https://doi.org/10.1016/j.chnaes.2018.02.004

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S.M. Hosseini et al. / Acta Ecologica Sinica xxx (2018) xxx–xxx

Fig. 1. Map of the area of the Moeil mine and the four sampling points. The map of Iran is taken from lonelyplanet.com

2.2. Sampling The two species Dactylis glomerata and Scleranthus orientalis were chosen for study because of their wide distribution in the study area. Soil and plant samples were taken from four sites, denoted sites 1–4 in Fig. 1. Site 1 was south of and next to the mine pit, sites 2 and 3 were about 300 m southward and westward of the mine pit respectively, and site 4 was about 500 m west of the mine pit. Samples were taken in June 2012. Bulk soil samples were collected at a depth of 5–20 cm around each root-plant species. Soil and plant samples were collected in triplicate at each of the indicated sampling sites. Samples were taken of mature plants included roots and above-ground tissue (shoots and leaves). The soil and plant samples were placed in dark polyethylene bags and transported to the laboratory. 2.3. Soil physico-chemical characterization The soil samples were dried at 50 °C for 48 h. They were then mixed, homogenized, and sieved through a sieve with 2-mm holes. The soil pH and electrical conductivity (EC) were measured electrometrically (Corning pH meter 430; Hanna HI 8333 conductivity meter) after 1 g of soil had been stirred with 10 ml distilled water in a beaker and left for about 1 h. The organic carbon concentration and organic matter (OM) concentration were measured by titration employing the Walkley–Black method [11]. The total N concentration was determined employing the Kjeldahl method [12]. The calcium carbonate concentration was determined using a calcimeter [13]. The distribution of the soil particle size (sand, silt, and clay) was measured using a hydrometer [14]. 2.4. Analysis of elements in soils To determine soil element concentrations, 0.25 g of dried and ground soil sample that passed through the sieve having 2-mm holes was digested in a 10 ml of a mixture of HNO3, HCl, and HClO4 (6:3:1, v/v/v). The tube was left at room temperature overnight and was then simmered on a hot plate at 120 °C for 2 h. After cooling, the digest was transferred into a 50-ml volumetric flask and diluted with distilled water. After gently stirred, the supernatant solution was transferred into a test tube. The concentrations of major (Fe, Al,) and trace elements

(As, Pb, Cd, Mn, Ni, Zn, and Cr) were determined using inductively coupled plasma optical emission spectrometry (ICP-OES, Varian 735ES) according to the method described by Hseu et al. [15] 2.5. Analysis of elements in plants The roots of samples were separated from aerial parts. Samples were agitated in a distilled water/methanol solution. This step removed any soil and dust stuck to any surfaces. Samples were rinsed again in distilled water to remove remaining traces. The samples were then dried in an oven at 60 °C until ready for homogenizing. After homogenizing, 0.1 g of sample was digested in a mixture of 5 ml 65% HNO3 and 3 ml 30% H2O2 and then was placed into a sealed high-pressure vessel and was heated in 150 °C an automated microwave digestion machine. After the digestion was completed, the sample was completely decomposed and the solution was made to a final volume of 10 ml. The concentrations of Fe, As, Pb, Cd, Mn, Ni, Zn, and Cr were determined using inductively coupled plasma mass spectrometer (ICP-MS, Agilent 4500, Agilent Technologies, Waldbronn, Germany) according to the method reported by Margesin and Schinner [16]. 2.6. Measurement of biological concentration factor (BCF), biological accumulation coefficient (BAC) and transfer factor (TF) The biological concentration factor (BCF) is the capacity of plant to transfer metals from soil to root and is calculated as the ratio of concentration of metals in plant root to that of soil [17]. The biological accumulation coefficient (BAC) is the capacity of plant to translocate metals from soil to above-ground tissue and is calculated as the ratio of concentration of metals in plant above-ground tissue to that in soil [18]. The transfer factor (TF) measures the ability of plants to translocate metals from the roots to above-ground tissue and is calculated as the ratio of concentration of metals in plant above-ground tissue to that in root [19]. It also was named “translocation factor” [17]. 2.7. Statistical analysis Statistical analysis was performed using IBM SPSS version 21 software. Average results for different soil and vegetal samples were compared using one-way analysis of variance (ANOVA). Prior to ANOVA, homogeneity of variances was tested using Levene's test. Post hoc

Please cite this article as: S.M. Hosseini, et al., Distribution of heavy metals and arsenic in soils and indigenous plants near an iron ore mine in northwest Iran, Acta Ecologica Sinica (2018), https://doi.org/10.1016/j.chnaes.2018.02.004

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analysis of variance was used to evaluate differences among means using Tukey's test (p b 0.05) and Dunnet's T3 (p b 0.05) when Homogeneity of Variance was assumed and not assumed, respectively. Standard errors (SEs) were measured to determine the variability of means between triplets. 3. Results and discussion 3.1. Soil properties The main physicochemical properties of the soils are given in Table 1. PH, Electric conductivity (EC), total N, organic carbon (OC), organic matter (OM), Caco3, clay, silt, and sand ranged from 3.31 to 7.21, 0.41 to 1.21 (Ds/M), 0.02 to 0.24 (%), 0.18 to 3.4 (%), 0.31 to 5.86 (%), 3.75 to 12.33 (%), 16 to 72 (%), 8 to 6- (%), and 8 to 26 (%), respectively. Except for the neutral top soil of sample D4, soils in the study area were acidic with pH values ranging from 3.31 to 6.55. The OM concentration of soil samples was low (b2.5%), except for samples D2 and S4 (3.95% and 5.86% respectively). Likewise, total N and organic carbon concentrations were low, varying from 0.02% to 0.24% and from 0.18% to 3.4% respectively. Soil samples had a low lime concentration with the exception of D2 (12.34%). All soil samples had low salinity. Soil samples had low EC and thus low salt concentrations. The silt fraction was predominant in the soil samples (52%–60%). The textures of the soil samples were silty clay loam to silty loam, except that the texture of sample S1 was clay. 3.2. Heavy metals in soil samples The total concentrations of elements in the soil samples are shown in Table 2. As had the greatest concentrations across soils followed by Mn N Cr N Zn N Pb N Ni N Cd. The total concentration of Fe, As, Pb, Cd, Mn, Ni, Zn, and Cr varied within the range of 50,247–466,200, 39.9–10,826.9, 9–84, 0.2–58.4, 32–424, 4–32, 37–60, and 32–337 mg/kg, respectively. The total soil As concentration was high in the sites near the mine pit (i.e., D1 = 6163.3 mg/kg and S1 = 10,826 mg/kg). Three samples showed moderate soil As concentrations (i.e., D3 = 414.2 mg/kg, S3 = 692.1 mg/kg and S4 = 286.1 mg/kg). Even though other samples showed low soil concentrations of As (i.e., D2 = 99.9 mg/kg and S2 = 49.mg/kg), they were still higher than the acceptable soil limit for As of 20.0 mg/kg [20,21] or 20–50 mg/kg [22]. There was a significant difference in soil As concentration among the sites. The total Pb concentrations were low and varied within the range of 9–84 mg/kg. Significant differences were found among the different sites. The range of the maximum allowable concentration (MAC) for Pb in soils is 20–300 mg/kg [22]. According to this criterion, the soil samples in this study were within the acceptable concentrations for Pb. Soil samples taken from site 1 had a high concentration of Cd that was considerably higher than world average concentrations of Cd in uncontaminated soils, which range from 0.2 to 1.1 mg/kg [23]. In contrast, soil samples from Table 1 Physicochemical parameters of soils in the area of the Moeil mine (n = 3). Site Top soil sample

pH

EC Total (Ds/m) N (%)

OC (%)

OM (%)

Caco3 Clay Silt Sand (%) (%) (%) (%)

1

3.31 3.52 6.55 6.35 4.07 3.57 7.21 3.38

0.70 0.49 0.71 0.41 1.15 0.88 0.41 1.21

0.29 0.45 2.29 0.61 0.84 0.18 1.4 3.4

0.50 0.78 3.95 1.05 1.45 0.31 2.41 5.86

3.75 4.23 12.34 4.21 2.11 4.24 6.7 4.22

2 3 4

D1 S1 D2 S2 D3 S3 D4 S4

0.03 0.04 0.23 0.06 0.07 0.02 0.12 0.24

23 72 32 34 30 32 16 29

55 8 60 54 50 56 58 52

22 20 8 12 20 12 26 19

D and S in the sample ID represent bulk soil belong to D. glomerata and S. orientalis, respectively.

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other sites were in this uncontaminated range. There was a significant difference in soil Cd concentration among the sites. The total Mn concentrations did not surpass the MAC values for Mn in agricultural soils (1500–3000 mg/kg; [22]). But significant differences in Mn concentration were found among different sites. Total Ni concentrations in soils at all four sites of the study area were within normal worldwide concentration ranges of 13–37 mg/kg [23] and 20–40 mg/kg [20]. Like other elements, significant differences in Ni concentration were found among the sites. The Zn concentrations in soils at all four sites were in normal worldwide concentration ranges of 60 to 89 mg/kg [23] and 80 to 120 mg/kg [24]. Unlike mentioned elements, there was no significant difference in Zn concentration soil among the sites. The Cr concentrations in the soil samples were lower than the world soil average of 60 mg/kg [23], with the exception of the Cr concentration at site 1 (293 to 337 mg/kg). Anawar et al. [25] recorded concentrations of 5–160 mg/kg Cr for soils in the vicinity of a pyrite mine. Significant differences in Cr concentration were found between site 1, next to mine pit, and other sites. 3.3. Heavy metals in indigenous plants The concentrations of elements in the roots and aerial parts of native plant species were shown in Table 3. There is no evidence to support the necessity of As to plants [26]. In this study, D. glomerata and S. orientalis, accumulated 19.3–5430 and 13.3–3570 mg/kg As in the roots, respectively. The concentration of As in the roots increased with increasing As soil concentration for both species. A high positive correlation was found between soil As concentration and root As accumulation (R = 0.92, p b 0.01; data is not shown). The highest accumulation of As occurred in site 1, next to the mine pit, where the As concentration in soil samples was high. As tolerant plants could be termed as excluders when TFs b 1, even they translocated elevated concentration of As to aerial parts [27,28]. According to Fitz and Wenzel [28], in polluted regions excluder plants can accumulate N10,000 mg/kg in the roots. Both native plants investigated in this study could be considered as excluder plants for As. Samples of D. glomerata and S. orientalis accumulated 1.15–8.86 and 4.19–133 mg/kg As in the aerial parts, respectively. As concentration in various plants ranged from 0.009–1.5 mg/kg for most plants when grown in unpolluted soils [23], however, in polluted soils, accumulator plants can translocate several thousand mg/kg As to the aerial parts [28]. In this study, even though the plant species investigated accumulated more than the normal range, they could not accumulate a huge concentration as would be observed in accumulator plants. In fact, except in hyperaccumulator plants, As generally has low mobility in the plant and as a result, low translocation from roots to aerial parts [26]. In wild-type A. thaliana, only 2.6% of As accumulated by the roots was translocated to the aerial parts [29]. Álvarez-Ayuso et al. [30] reported various spontaneously-grown plants in the vicinity of a former mine in Clara, Spain, accumulated 0.05–1.42 mg/kg As in the aerial parts. The TF value (aerial parts/root) of As decreased with increasing soil As concentration for the two plant species (Table 4). Similar results were previously demonstrated by Caetano et al. [31] and Bergqvist et al. [32]. Because of the low translocation of solutes including As, the xylem sap decreases, which might result in the low TF value of As [33]. Reduction of xylem sap could be because of plant mechanisms to avoid As translocation in order to protect the photosynthesis process [32]. According to Baker [27], metal-tolerant plants are generally excluders, as they limit uptake and translocation of trace metals to aerial parts. Although Pb accumulates normally in all plants, it is not essential or beneficial for any plants [34]. In this study, the two native plants accumulated 1.54–15.2 and 0.2–2.6 mg Pb/kg in the roots and aerial parts, respectively. These results show that the root Pb concentrations were more than those in the aerial parts. Because of the low solubility of Pb in soils, its phytoavailability could be very small [35]. Plants concentrate

Please cite this article as: S.M. Hosseini, et al., Distribution of heavy metals and arsenic in soils and indigenous plants near an iron ore mine in northwest Iran, Acta Ecologica Sinica (2018), https://doi.org/10.1016/j.chnaes.2018.02.004

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S.M. Hosseini et al. / Acta Ecologica Sinica xxx (2018) xxx–xxx

Table 2 Concentrations of elements in soil samples taken from the area of the Moeil mine (mg/kg; n = 3). Site

Sample ID

Fe

Al

As

Pb

Cd

Mn

Ni

Zn

Cr

1

D1 S1 D2 S2 D3 D3 D4 S4

466,200 ± 5919 a 389,900 ± 4350 a 53,478 ± 3551 b 51,637 ± 2398 b 355,700 ± 3819 a 395,600 ± 3819 a 50,247 ± 2536 b 372,000 ± 7211 a

10,790 ± 616 a 22,504 ± 437 c 71,212 ± 1552 b 74,902 ± 1872 b 24,848 ± 741 c 15,532 ± 410 a 75,260 ± 1512 b 22,701 ± 699 c

6163.3 ± 122 a 10,827 ± 586 a 99.9 ± 17 b 49.5 ± 8 b 414.2 ± 76 c 692.1 ± 77 c 39.9 ± 8 b 286.1 ± 56 c

69 ± 8.71 a 64 ± 8.7 a 9 ± 2.6 b 9 ± 2.1 b 76 ± 8.7 a 86 ± 11.5 a 9 ± 2.1 b 64 ± 10.5 a

36.6 ± 9 a 58.4 ± 8 a 0.7 ± 0.2 b 0.2 ± 0.2 b 2.1 ± 0.5 c 3.7 ± 1.1 c 0.5 ± 0.2 d 1.6 ± 1.2 d

32 ± 10 a 52 ± 15 a 385 ± 39 b 397 ± 29 b 135 ± 21 c 102 ± 15 a 424 ± 39 b 98 ± 10 d

4 ± 1.1 a 9 ± 2.6 a 21 ± 3 b 18 ± 4 b 9 ± 2.1 a 6±1c 32 ± 7.2 b 13 ± 3.6 d

52 ± 13 a 45 ± 14 a 37 ± 11 a 38 ± 10 a 59 ± 13 a 61 ± 13 a 38 ± 10 a 60 ± 11 a

293 ± 24 a 337 ± 30 a 38 ± 5 b 34 ± 10 b 72 ± 11 b 70 ± 11 b 32 ± 8 b 50 ± 13 b

2 3 4

D and S in the sample ID represent bulk soil belong to D. glomerata and S. orientalis, respectively. Different letters in the same column represent significant difference at p b 0.05.

absorbed Pb in the roots and some of this is translocated to aerial parts [36]. Plants readily take up Cd from the soil and transfer it to aerial parts, even though this element is not needed for metabolic processes [37]. In the present study, the Cd concentration in the plant samples was very low. The species D. glomerata and S. orientalis accumulated from 0.03 to 0.5 mg/kg Cd in the roots and from 0.01 to 0.25 mg/kg Cd in the above-ground tissue respectively. Quezada-Hinojosa et al. [38] reported that the native plants including D. glomerata growing at Le Gurnigel in the Swiss Jura Mountains accumulated 0.8–9.4 mg/kg Cd in the aerial parts. Mn is a heavy metal but it is not generally known as a toxic element, unlike Pb and As [39]. In fact, Mn plays an essential role in higher plant growth and resistance to pests and disease [40]. In this study, the two native plants accumulated 1–190 and 22–461 mg/kg Mn in the roots and aerial parts, respectively. Mn content among different species ranges from 30 to 500 mg/kg [41]. According to Kabata-Pendias and Mukherjee [22], the sufficient or normal range of Mn in mature leaf tissue is between 30 and 300 mg/kg. In this study, accumulation of Mn in aerial plant parts was within the normal range. Only a low concentration (0.05 to 10 mg/kg) of Ni is needed [42]. It has also been confirmed that Ni increases a plant's resistance to disease [43]. Vegetal samples in our study accumulated 5.6 to 28.7 mg/kg Ni in the roots and 1.19 to 17.2 mg/kg Ni in the aerial parts. The concentration of Ni translocated to aerial parts remained in the normal range for D. glomerata samples and a little higher than the normal range for S. orientalis samples. Sommer and Lipman were the first to report the importance of Zn as an essential element for plants [44]. However, a high concentration of Zn may be toxic [45]. The normal concentration range and toxic range of Zn in mature leaf tissue are 25–150 and 100–400 mg/kg respectively [22] and the critical Zn deficiency for most species ranges from 10 to 100 mg/kg [44]. In the present study, the two indigenous species

accumulated 14.1–55.9 mg/kg Zn in roots and 13–78 mg/kg Zn in aerial parts, which lie in the normal range of Zn concentrations. It has not yet been conclusively demonstrated that Cr is necessary for plant metabolism [46]. The two plant species in our study accumulated 5.4–151 mg/kg Cr in roots and a low 0.7 to 6.9 mg/kg Cr in aerial parts even at site 1, where the soil had a considerable concentration of Cr. The accumulation of Cr in the aerial parts of plants is commonly 0.02–0.2 mg/kg and rarely higher than 5 mg/kg [46]. Anawar et al. [25] reported that 19 plant species growing in the area of a pyrite mine accumulated 2.6–10.6 mg/kg Cr. Hyperaccumulator thresholds for metals and metalloid include: 100 mg/kg for Cd, 300 mg/kg for Cr, 1000 mg/kg for As, Pb, and Ni, 3000 mg/kg for Zn and 10,000 mg/kg for Mn [47]. According to these criteria, neither of the two native species in this study is considered to be a hyperaccumulator. Meanwhile, plant species with BAC N 1 and translocation factor (TF) N 1 are characterized as species suitable for phytoextraction [48], whereas plant species with BCF N 1 and TF b 1 are considered useful for phytostabilization [17]. Tolerant plant species limit root-to shoot translocation and thus have less accumulation in aerial parts, while hyperaccumulators actively accumulate metal(loid)s in aerial parts [28]. The values of the BCF, BAC, and TF for the species in the present study were shown in Table 4. Both D. glomerata and S. orientalis had BAC and TF N 1 for Mn, therefore these two species seem suitable for the phytoextraction of Mn. Further study of course is needed.

4. Conclusion The study of the Moeil mine area showed high concentrations of pollution with As. The As concentrations greatly surpassed the acceptable limit for soils. The soil Cd concentration was considerably higher at a site 1 adjacent to a mine pit than at other sites. Totally, moderate concentrations of Pb, Cd, Mn, Ni, Zn and Cr were found in the study area.

Table 3 Concentrations of elements in roots and aerial parts of plant species growing in the studied area (mg/kg; n = 3). Values presented are means ± SD. Samples

Site

Part

Fe

As

Pb

Cd

Mn

Ni

Zn

Cr

D. glomerata

1

Root Aerial parts Root Aerial parts Root Aerial parts Root Aerial parts Root Aerial parts Root Aerial parts Root Aerial parts Root Aerial parts

280,000 ± 986 a 1220 ± 98 A 14,900 ± 331 b 1450 ± 76 A 218,000 ± 756 a 4100 ± 289 B 29,500 ± 378 b 5820 ± 256C 237,000 ± 1376 a 16,500 ± 767 A 8660 ± 199 b 7700 ± 832 B 196,000 ± 895 a 149,000 ± 649 A 56,000 ± 567 c 3310 ± 356 B

5430 ± 153 a 8.86 ± 0.8 A 19.3 ± 2.4 b 1.15 ± 0.1 B 263 ± 23.6 c 1.26 ± 0.1 B 22.4 ± 2.2 b 7.13 ± 0.8 A 3570 ± 216 a 133 ± 247 A 13.1 ± 2.5 b 14.4 ± 1.4 B 264 ± 25 c 17.3 ± 1.3 B 44.4 ± 2.3 b 4.19 ± 0.4C

1.85 ± 0.1 a 0.33 ± 0.1 A 1.54 ± 0.0 a 0.3 ± 0.0 A 15.2 ± 2.4 b 0.52 ± 0.1 A 4.6 ± 0.0 a 1.2 ± 0.7 A 1.96 ± 0.1 a 0.6 ± 0.1 A 2.31 ± 0.1 a 0.69 ± 0.0 A 15.1 ± 3.5 b 2.6 ± 0.5 B 4.1 ± 0.9 a 0.25 ± 0.0 A

0.03 ± 0.0 a 0.02 ± 0.0 A 0.04 ± 0.1 a 0.01 ± 0.0 A 0.03 ± 0.1 a 0.01 ± 0.0 A 0.03 ± 0.1 a 0.01 ± 0.0 A 0.10 ± 0.0 a 0.07 ± 0.0 A 0.16 ± 0.0 b 0.07 ± 0.0 A 0.07 ± 0.0 c 0.25 ± 0.0 B 0.50 ± 0.0 d 0.17 ± 0.0 B

1 ± 0.0 a 39 ± 10.5 A 73 ± 17 b 22 ± 5.2 A 40 ± 8.7 b 95 ± 21.7 B 190 ± 21 c 49 ± 9.8 A 7 ± 2.6 a 92 ± 22 A 62 ± 13 b 45 ± 13.2 A 67 ± 13 b 461 ± 39 B 142 ± 23 c 160 ± 18C

7.48 ± 2.0 a 5.36 ± 0.5 A 5.60 ± 1.2 a 1.19 ± 0.1 B 8.58 ± 2.2 a 6.96 ± 1.1 A 28.7 ± 3.7 b 8.30 ± 0.6C 9.19 ± 1.0 a 11.7 ± 1.1 A 7.6 ± 2.0 a 3.6 ± 0.3 B 14.2 ± 2.8 a 15.1 ± 2.5 A 28.6 ± 4.6 b 17.2 ± 2.4 A

14.1 ± 0.0 a 15.2 ± 3.3 A 14.8 ± 1.6 a 13.0 ± 4.5 A 44.1 ± 6.1 b 22.3 ± 5.2 A 36.6 ± 7.4 b 18.2 ± 3.4 A 29.5 ± 6.6 a 25.5 ± 4.7 A 42.7 ± 8.7 a 20.5 ± 3.1 A 55.9 ± 8.9 b 78.6 ± 10.2 B 46.5 ± 9.1 a 33.7 ± 8.8 A

151 ± 12 a 0.8 ± 0.1 A 5.4 ± 0.4 b 1.6 ± 0.2 A ` 4.20 ± 1.1 B 11.9 ± 2.7 b 5.90 ± 1.3 B 108 ± 19 a 6.9 ± 1.3 A 6.2 ± 0.24 b 2.9 ± 0.5 B 21.8 ± 3.7 b 5.30 ± 1.1 A 9.0 ± 3.6 b 0.7 ± 0.2 B

2 3 4 S. orientalis

1 2 3 4

Different small letters for the roots and capital letters for the aerial parts in the same column for each vegetal sample represent significant difference at p b 0.05.

Please cite this article as: S.M. Hosseini, et al., Distribution of heavy metals and arsenic in soils and indigenous plants near an iron ore mine in northwest Iran, Acta Ecologica Sinica (2018), https://doi.org/10.1016/j.chnaes.2018.02.004

S.M. Hosseini et al. / Acta Ecologica Sinica xxx (2018) xxx–xxx

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Table 4 Biological concentration factors (BCFs), biological accumulation coefficients (BACs), and transfer factors (TFs) of plant species growing in the area of the Moeil mine. Vegetal

Site

Species D. glomerata

S. orientalis

1 2 3 4 1 2 3 4

As

Pb

Cd

Mn

Ni

Zn

Cr

BAC

BCF

TF

BAC

BCF

TF

BAC

BCF

TF

BAC

BCF

TF

BAC

BCF

TF

BAC

BCF

TF

BAC

BCF

TF

0.00 0.01 0.00 0.18 0.01 0.29 0.02 0.01

0.88 0.19 0.64 0.56 0.32 0.26 0.38 0.15

0.00 0.05 0.00 0.31 0.03 1.1 0.06 0.01

0.00 0.03 0.00 0.12 0.00 0.07 0.03 0.00

0.02 0.17 0.19 0.54 0.03 0.26 0.17 0.06

0.17 0.19 0.03 0.24 0.3 0.29 0.17 0.06

0.00 0.01 0.00 0.03 0.00 0.36 0.06 0.15

0.00 0.06 0.01 0.10 0.00 0.8 0.02 0.45

0.92 0.22 0.33 0.32 0.79 0.46 3.3 0.84

1.23 0.05 0.69 0.11 1.7 0.11 4.5 1.6

0.03 0.18 0.29 0.44 0.13 0.15 0.65 1.44

39 0.3 2.3 0.25 13.5 0.71 6.9 1.13

1.36 0.09 0.79 0.26 1.4 0.2 2.5 1.3

1.85 0.26 0.95 0.91 1.09 0.42 2.4 2.2

0.7 0.34 0.82 0.29 1.2 0.48 1.06 0.6

0.29 0.34 0.37 0.48 0.58 0.54 1.3 0.55

0.27 0.41 0.75 0.97 0.66 1.1 0.92 0.77

1.06 0.85 0.5 0.49 0.86 0.48 1.4 0.71

0.00 0.04 0.05 0.18 0.02 0.08 0.75 0.13

0.51 0.14 0.28 0.37 0.31 0.18 0.31 0.17

0.00 0.28 0.19 0.50 0.06 0.46 0.24 0.07

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Please cite this article as: S.M. Hosseini, et al., Distribution of heavy metals and arsenic in soils and indigenous plants near an iron ore mine in northwest Iran, Acta Ecologica Sinica (2018), https://doi.org/10.1016/j.chnaes.2018.02.004