Phytoremediation potentials of some wild plants around the chromium mine

Veli Çeliktaş (  [email protected] ) University: Amasya Universitesi https://orcid.org/0000-0001-7753-1422 Necattin Türkmen Cukurova University: Cukurova Universitesi

Research Article

Keywords: phytoremediation, phytoextraction, hyperaccumulation, bioconcentration, translocation, heavy metal

Posted Date: August 31st, 2021

DOI: https://doi.org/10.21203/rs.3.rs-857379/v1

License:   This work is licensed under a Creative Commons Attribution 4.0 International License. Read Full License

Page 1/9 Abstract

Phytoremediation is the general name of techniques that uses plants to remediate polluted environments. Heavy metals are one of the pollution resources caused by anthropogenic or natural ways. In this study, it was aimed to fnd new plant species for phytoremediation of heavy metals. For this purpose, feld researches were done in chromium mining sites. After that, plants were selected, which were relatively abundant in the mining sites. Aethionema spicatum, Alyssum alyssoides, Alyssum foribundum, Alyssum oxycarpum, Thlaspi oxyceras, Convolvulus compactus, Onosma cappadocica and Salvia multicaulis were researched. For understanding phytoremediation potentials of plants, heavy metal analyses (Cr, Ni, Co, Pb, Zn, Mn, Cu and Fe) were done in rhizosphere soils and different parts of plants. Then plants were evaluated for accumulation and translocation of heavy metals by using BCF and TF calculations. Aethionema spicatum, Alyssum foribundum, Alyssum oxycarpum and Thlaspi oxyceras were found as hyperaccumulators for Ni because of their metal accumulation abilities.

Introduction

It is very complicated to clean soils contaminated with heavy metals. Removing heavy metals by metal extraction or immobilization methods is expensive and adversely affects soil biological structure (Baker et al. 1994). Phytoremediation is the general name of techniques that uses plants to remediate polluted environments. This method is more economical than other techniques. Phytoremediation has fve different mechanisms as rhizofltration, phytostabilization, phytoextraction, phytovolatilization and phytodegradation. These mechanisms aimed to destruct, inactivate or immobilize the source of pollution (Ghosh and Singh 2005; Wan and Chen 2016).

Plants are needed because of their importance in phytoremediation. So it is necessary to increase the diversity of the plants used for this purpose. This work aims to contribute to phytoremediation studies by fnding new plant species to use for the remediation of heavy metals.

Materials And Methods Study sites

The study sites were located in the Aladağ region in province of (Fig. 1). This region has chromium mining sites and mining processing places. So, there is a lot of mining waste surround here. Three open mining sites were selected for this study that showed in Fig. 1.

Plants and soil samplings

Plants of mining sites were identifed according to the Davis (1965-1985). Plants were selected, which were relatively abundant in the sites and then sampled (5 replicates) from where they were spread the most. Studied plant species and families were Aethionema spicatum Post (Brassicaceae), Alyssum alyssoides L. (Brassicaceae), Alyssum foribundum Boiss. & Bal. (Brassicaceae), Alyssum oxycarpum Boiss. & Bal. (Brassicaceae), Thlaspi oxyceras (Boiss.) Hedge (Brassicaceae), Convolvulus compactus Boiss. (Convolvulaceae), Onosma cappadocica Siehe ex Riedl (Boraginaceae), Salvia multicaulis Vahl (Lamiaceae).

The name of Onosma cappadocicum (in Flora of Turkey and the East Aegean Islands) used as Onosma cappadocica because of the genus name’s gender (Aytaç and Türkmen 2011).

Plant and soil heavy metal analyses

Collected plants in mining sites were transferred to the laboratory with their rhizosphere soil and then separated root, stem, and leaves. And then, separated parts were washed with fowing tap water to remove soil particles around roots and rinsed with distilled water many times. Washed plant parts were dried in the oven at 65 0C and then powdered.

Dried and powdered plant samples were measured as 0.2 g and burned in a CEM microwave oven by a mixture of 2 ml H2O2 – 5 ml HNO3. After the burning, the samples were completed with distilled water as fnal volumes of 20 ml and fltered by blue band flter paper (Kaçar and İnal 2008). The soil samples belonged the rhizosphere area were dried on a bench in the laboratory and then passed through at a 2 mm sieve. The soil analyses were performed according to the EPA-3051A method (U.S. EPA. 2007).

Heavy metal concentrations (Cr, Ni, Co, Pb, Zn, Mn, Cu and Fe) were determined by using atomic absorption spectrophotometer.

Some physical and chemical analysis of soils

Soil textures were determined by hydrometer method (Bouyoucos 1951), soil pH was determined by pH-meter in 1: 2.5 soil-distilled water mixture (Jackson 1958). The organic carbon content (% C) in the soils was determined by the Anne method, and the total nitrogen content was determined (N%) by the Kjeldahl

Page 2/9 method (Duchaufour 1970).

Statistical analyses

The statistical analyses were performed with IBM SPSS 22 software. The ANOVA (for parametric data) and Kruscall Wallis (for non-parametric data) tests were used for evaluating data.

Evaluating phytoremediation potentials of plants

The bioconcentration factor and translocation factor were calculated for evaluating the phytoremediation properties of plants. Bioconcentration factor (BCF) is defned as the ratio of the different plant parts (BCF-Root, BCF-Stem and BCF-Leaves) metal concentrations to soil metal concentrations (Barman et al. 2000; Marques 2009). Translocation factor (TF) is defned as the ratio of the stem (TF-Stem) and leaves (TF-Leaves) metal concentrations to root metal concentrations (Yang et al. 2018).

Results And Discussion General properties of rhizosphere soils

Average values are shown in Table 1 as follows: the sand percentage is 69.67%, clay percentage is 7.53%, and silt percentage is 22.80%. According to these, the soil texture was determined as sandy loam for the study site soils. The average pH value was found 7.56. The soil of the study area has been determined to be slightly alkaline. For the soils of the study area, average nitrogen and carbon were found at 0.15% and 4.38%, respectively. In the study conducted by Kızıldag (2017), it was stated that the soils of the region were sandy clay loamy and slightly alkaline, and the carbon content of the soils was between 1.34- 2.63% and nitrogen content between 0.15-0.20%. Mbarki et al. (2008) reported that the concentrations of some heavy metals were found in sandy textured soils at lower concentrations than in clay textured soils in their study. Due to the sandy soil character, metals are washed and proceed along with the soil profle. In clay soils, it keeps metals and reduces the washing of metals (Madrid et al. 2007). It is known that there is a correlation between nitrogen and carbon and heavy metal concentrations of the soil (Dai et al. 2004). It is seen that in Table 1, the C and N concentrations of researched area soils are low levels. Low concentrations of C and N in serpentine areas have also been expressed in previous studies (DeGrood et al. 2005; Pal et al. 2005). The acidic or alkaline character of soils affects the metal concentrations in plants (Zeng et al. 2011; Adamczyk-Szabela et al. 2015).

Table 1 General Properties of Rhizosphere Soils

Species Sand% Clay% Loam% pH N% C%

Aet. spicatum 67.19 ± 1.33 6.08 ± 0.86 26.73 ± 1.09 7.74 ± 0.23 0.05 ± 0.02 2.84 ± 0.29

A. alyssoides 73.03 ± 0.89 1.64 ± 0.17 25.33 ± 0.96 7.36 ± 0.05 0.32 ± 0.13 8.70 ± 0.56

A. foribundum 71.97 ± 0.76 2.21 ± 1.02 25.82 ± 1.59 7.57 ± 0.20 0.05 ± 0.01 2.71 ± 0.31

A. oxycarpum 65.60 ± 1.19 8.51 ± 0.50 25.89 ± 0.70 7.61 ± 0.09 0.09 ± 0.03 2.39 ± 0.84

T. oxyceras 68.89 ± 1.80 8.36 ± 1.15 22.75 ± 0.71 7.48 ± 0.14 0.38 ± 0.07 9.05 ± 0.58

C. compactus 52.02 ± 0.57 26.10 ± 0.78 21.88 ± 1.18 7.62 ± 0.10 0.12 ± 0.00 2.66 ± 0.15

O. cappadocica 85.30 ± 0.84 5.47 ± 0.44 9.23 ± 0.47 7.75 ± 0.19 0.04 ± 0.00 2.21 ± 0.27

S. multicaulis 73.39 ± 1.68 1.83 ± 0.49 24.78 ± 1.19 7.34 ± 0.18 0.11 ± 0.03 4.45 ± 0.45

Average 69.67 7.53 22.80 7.56 0,15 4.38

Heavy metal concentrations of plants and rhizosphere soils

Heavy metal concentrations in plant parts (root, stem and leaves) and soils are shown in Table 1.

Average Cr concentrations (Table 1) are between 103.83-215.78 mg/kg in soils, 2.15-5.47 mg/kg in roots, 0.74-13.71 mg/kg in stems and 1.01-8.86 mg/kg in leaves. Adriano (1986) stated that total chromium concentrations in plants are under 10 mg/kg. It is seen that chromium concentrations of O. cappadocica

Page 3/9 and C. compactus are higher than others. Adriano (1986) stated that Cr concentrations are between 10-150 mg/kg in normal soils, but Krishna et al. (2013) reported that Cr concentrations around chromium mining area are about 64.1-4863 mg/kg. In researched soils (Table 2), Cr concentrations are in normal ranges for a chromium mining area.

Average Ni concentrations (Table 2) are between 873.11-896.21 mg/kg in soils, 11.68-1425.19 mg/kg in roots, 24.13-1190.03 mg/kg in stems and 22.77- 1539.39 mg/kg in leaves. Brooks and Radford (1978) stated that Ni concentrations of hyperaccumulator plants are higher than 1000 mg/kg. It is shown that Aet. spicatum, A. oxycarpum, A. foribundum and T. oxyceras have Ni concentrations of more than 1000 mg/kg in their different parts.

Average Co concentrations (Table 2) are between 235.43-325.65 mg/kg in soils, 0.67-10.48 mg/kg in roots, 1.40-11.66 mg/kg in stems and 1.40-128.61 mg/kg in leaves. Co concentrations throughout in ultramafc rocks are about 100-220 mg/kg (Kabata-Pendias and Pendias 2001). Study sites Co concentrations are between 235-310 mg/kg. Adriano (1986) stated that hyperaccumulators for Co must have at least 1000 mg/kg. The plants in the research area have not too much Co accumulation in their tissues.

Average Pb concentrations (Table 2) are between 4.39-30.11 mg/kg in soils, 1.13-4.86 mg/kg in roots, 0.64-3.63 mg/kg in stems and 1.12-3.01 mg/kg in leaves. It is known that Pb mining sites especially are in areas formed limestone (Davies et al. 1993; Ye et al. 2000). The researched areas have especially serpentine and ophiolite (Bingöl 1978). Pb concentrations of soils may be low for this reason. Also, it is stated that Pb concentrations may be low in chromium mining areas (Krishna et al. 2013; Olowoyo et al. 2013). Adriano (1986) stated that Pb concentrations in plants are between 0.1-30 mg/kg. According to these values, the results of the present study are in normal lines.

Average Zn concentrations (Table 2) are between 52.57-82.39 mg/kg in soils, 4.83-20.57 mg/kg in roots, 7.99-21.69 mg/kg in stems and 7.21-33.06 mg/kg in leaves. It is known that Zn concentrations in herbaceous vegetables are about 1-160 mg/kg, and in soils, it is 1-900 mg/kg (Adriano 1986). Zn concentrations of the researched plants and soils are low according to these values.

Average Mn Concentrations (Table 2) are between 560.15-725.43 mg/kg in soils, 10.30-58.95 mg/kg in roots, 11.52-75.11 mg/kg in stems and 27.44-207.93 mg/kg in leaves. Total manganese concentrations in herbaceous vegetables are 0.3-1000 mg/kg and in soils 20-10000 mg/kg (Adriano 1986). It is seen that the Mn concentrations of the plants are within these limits. Baker and Brooke (1989) stated that plants with Mn hyperaccumulators should have a concentration of 10000 mg/kg Mn in their bodies. According to the literature, the Mn concentrations of the studied plants are low.

Average Cu concentrations (Table 2) are between 6.08-19.72 mg/kg in soils, 0.52-1.44 mg/kg in roots, 0.48-1.31 mg/kg in stems, and 0.56-1.38 mg/kg in leaves. Adriano (1986) stated that the total copper concentrations in common agricultural plants are 6-40 mg/kg. Also, it has been stated that copper concentrations in the soils are 2-250 mg/kg (Adriano 1986). It is seen that the values are lower than the literature values.

Average Fe concentrations (Table 2) are between 3848.25-4166.75 mg/kg in soils, 53.73-276.57 mg/kg in roots, 33.65-313.33 mg/kg in stems, and 58.67- +3 248.89 mg/kg in leaves. Since the most amount of chromium (Cr ) present as chromite (FeCr2O4) or other structures, substituting for Fe or Al, in nature (Kabata-Pendias and Pendias 2001), high iron concentrations in chrome mining felds are an expected situation. According to the literature, Fe concentrations in studied soils are in normal lines (Samantaray et al. 2001; Das et al. 2013). István and Benton (1997) stated that 500 mg/kg Fe concentration may be toxic for plants. It is seen that the iron concentrations are generally less than 500 mg/kg in researched plants.

Table 2 Average heavy metal concentrations (mg/kg) of plants and rhizosphere soils and standard deviations

Page 4/9 Heavy Metal (mg/kg)

Cr Ni Co Pb Zn Mn Cu

Av. St. Av. St. D. Av. St. Av. St. Av. St. Av. St. Av. St. D. D. D. D. D. D.

Aet. Root 4.68 3.23 306.34 45.19 9.92 2.17 1.95 0.52 12.79 1.87 38.77 18.13 0.52 0.06 spicatum Stem 1.73 1.42 369.02 109.49 8.70 0.98 2.23 1.15 14.55 2.37 45.95 4.66 0.48 0.08

Leaves 1.01 0.75 1115.83 165.88 128.61 49.64 1.17 0.55 16.56 2.85 207.93 33.83 0.56 0.16

Soil 112.08 11.20 873.11 14.30 310.93 42.68 16.84 3.90 63.99 6.03 634.10 23.07 10.53 1.44

A. Root 4.42 1.54 11.68 3.74 0.67 0.13 4.86 2.80 19.75 3.01 23.75 2.11 1.32 0.10 alyssoides Stem 7.13 2.63 24.13 2.47 1.40 0.34 1.22 1.26 20.21 0.64 14.21 1.61 0.88 0.01

Leaves 5.10 1.30 22.77 1.14 1.40 0.08 3.01 1.54 18.19 1.17 28.37 10.39 1.27 0.23

Soil 123.13 8.16 878.28 11.85 259.98 16.01 29.76 11.99 82.39 2.64 673.85 4.55 16.14 2.06

A. Root 2.15 0.97 1425.19 21.90 6.02 0.43 1.43 1.25 20.57 4.45 10.30 1.33 0.59 0.10 foribundum Stem 0.99 0.18 1190.03 57.51 6.68 0.17 1.32 0.74 16.54 4.58 11.52 1.48 0.70 0.14

Leaves 1.81 0.30 1378.56 149.44 31.13 7.91 1.62 1.00 9.68 2.13 47.85 11.06 0.62 0.12

Soil 161.65 63.55 882.58 15.01 240.75 13.50 26.82 9.66 69.35 6.44 629.43 46.60 19.72 11.8

A. Root 5.47 1.74 711.50 289.49 7.18 0.90 1.58 1.10 7.49 0.73 17.26 2.03 0.71 0.01 oxycarpum Stem 7.87 0.81 1145.01 114.88 8.28 0.61 1.70 0.93 11.53 2.58 18.81 2.23 0.56 0.02

Leaves 6.89 2.45 1227.35 55.31 18.56 2.41 1.57 1.12 7.90 0.77 28.22 3.20 0.64 0.05

Soil 215.78 34.63 893.44 2.92 235.43 46.40 13.40 9.43 53.57 12.93 584.50 87.90 8.35 2.31

T. oxyceras Root 2.29 1.24 1159.25 47.64 7.43 0.66 1.78 1.22 19.86 1.15 17.92 8.37 0.92 0.17

Stem 0.74 0.32 1076.38 64.22 6.24 0.14 0.64 0.31 21.69 2.12 15.96 3.15 1.06 0.13

Leaves 5.17 5.51 1539.39 82.01 26.84 9.68 1.12 1.49 33.06 3.26 44.20 20.79 1.22 0.17

Soil 143.18 29.26 894.09 2.53 237.70 21.51 30.11 3.50 77.33 6.30 610.05 28.76 16.92 3.26

C. Root 3.96 1.82 40.40 23.90 8.79 1.37 1.81 0.91 9.79 1.17 31.88 11.85 1.30 0.33 compactus Stem 12.25 3.54 77.56 21.16 11.66 2.10 3.63 0.72 11.74 1.98 75.11 19.96 1.31 0.20

Leaves 7.26 5.27 85.59 29.80 13.12 2.96 1.82 1.10 10.52 2.18 79.74 25.88 1.38 0.52

Soil 130.53 7.41 875.08 11.98 325.65 21.19 23.02 4.42 81.32 3.71 725.43 30.51 15.81 1.75

O. Root 3.78 1.60 56.23 18.08 7.32 0.93 1.13 0.71 4.83 3.76 31.17 11.52 1.44 0.17 cappadocica Stem 13.71 5.60 119.56 53.57 11.05 2.62 1.25 1.31 7.99 2.13 70.26 16.98 0.91 0.09

Leaves 8.86 6.24 126.96 32.04 11.54 1.57 1.26 0.99 7.21 1.56 96.54 14.85 0.89 0.07

Soil 203.28 6.85 894.45 2.43 248.05 10.46 4.39 1.97 52.57 1.58 560.15 22.18 6.08 0.53

S. Root 5.31 5.66 116.63 51.88 10.48 3.18 1.36 0.89 13.32 2.67 58.95 16.68 0.92 0.14 multicaulis Stem 3.41 1.48 55.50 52.06 7.00 0.93 1.09 1.28 14.33 2.78 25.91 12.57 0.64 0.21

Leaves 3.13 0.92 68.47 64.19 7.64 0.60 1.48 0.74 14.08 3.17 27.44 1.75 0.61 0.09

Soil 103.83 21.05 896.21 0.10 238.97 2.45 26.58 3.61 67.26 7.50 621.48 35.99 10.99 1.78

Evaluating phytoremediation potentials of plants

It is shown that in Fig. 2, for chromium, all BCF values are lower than one. TF values of Aet. spicatum are under the line (Fig. 3) for the stem and leaves. For Cr, statistically (p<0.05) differences were found for BCF-Stem and TF-Stem. It is seen that for BCF-Stem C. compactus and O. cappadocica and for TF-Stem S. multicaulis, C. compactus and O. cappadocica have high values.

Page 5/9 It seems that in Fig. 2, for Ni BCF values (stem or leaves) of Aet. spicatum, A. foribundum, A. oxycarpum and T. oxyceras are higher than one. Also, the BCF values of these plants have statistical differences (p<0.05) from other plants. Although A. foribundum has not TF values (TF-Stem=0.84, TF-Leaves=0.97) over one accurately, its TF values are on lines. These plants are suitable for phytoextraction because of their high metal accumulation and high BCF (stem or leaves) and TF values. If BCF values of above-ground (harvestable) parts are higher than one, plants may be used for phytoextraction (Pilon-Smits 2005; Sun et al. 2016). A phytoextractor plant should transfer heavy metals from soil to harvestable parts (Pantola and Alam 2014). So, the translocation factor should be higher than one (Yoon et al. 2006; Wei et al. 2008). There are meaningful (p<0.05) differences between TF values of all plants. When looking at Fig. 3 for Ni, TF values of S. multicaulis are lower than for stem and leaves.

For Co metal, all BCF values (Fig. 2) of the plants are lower than one. For TF values (Fig. 3), excluding S. multicaulis, other plant’s values are over than one for at least one of the stem or leaves. There are meaningfully (p<0.05) differences between plants for TF and BCF values.

For Pb, all of the BCF values (Fig. 2) are lower than one, but TF values (Fig. 3) are higher than one or near the line for at least one of the stem or leaves. Excluding BCF-Stem, other BCF and TF values have not meaningful statistical differences (p<0.05). Respectively, BCF values of O. cappadocica are higher than others. In TF values, there are no too many differences between plants.

For Zn, excluding A. foribundum, all of the other TF values (Fig. 3) are higher than one for at least one of the stem or leaves, but all BCF values (Fig. 2) are under the line. Statistically (p<0.05), there are differences for BCF and TF values. It is seen that respectively O. cappadocica has higher values for TF calculations. BCF-Root of A. foribundum and BCF-leaves of T. oxyceras are higher than others, and BCF-Stem of C. compactus and O. cappadocica are lower than others.

For Mn, Cu and Fe, all BCF values (Fig. 2) are under one. BCF and TF values differences have statistically (p<0.05) importance for Mn, Cu and Fe. TF values (Fig. 3) of S. multicaulis (stem and leaves) is lower than one for these metals. It seems that in Fig. 3, TF values, especially for leaves, are near the lines for Cu. TF values (stem and leaves) of S. multicaulis and O. cappadocica are too low for the line. TF values for stem and leaves of A. foribundum, A. oxycarpum, C. compactus and O. cappadocica are higher than one for Fe.

Conclusion

Because of their metal accumulation abilities, Aet. spicatum, A. foribundum, A. oxycarpum and T. oxyceras are found as hyperaccumulators for Ni. Hyperaccumulator plants that accumulate heavy metals in their harvestable parts can be used for phytoextraction of metals. Our results showed that some plants are interesting for their calculations that have conspicuously lower BCF and TF values than one; for Ni S. multicaulis, for Cr Aet. spicatum, for Co S. multicaulis, for Zn A. foribundum, for Mn S. multicaulis, for Cu A. oxycarpum, O. cappadocica and S. multicaulis, for Fe Aet. spicatum, A. alyssoides and S. multicaulis. Especially BCF and TF values of S. multicaulis are lower than one excluding Cr, Pb and Zn. All of the plants in this study also should be grown in laboratory conditions to gain more knowledge about their heavy metal-related capabilities.

Declarations Funding

This work was supported by the Scientifc Research Projects Unit of Cukurova University (FDK-2016-4906).

Conficts of interest/Competing interests

There is no confict of interest.

Availability of data and material

The datasets generated during and/or analysed during the current study are available from the corresponding author on reasonable request.

References

Adamczyk-Szabela, D., Markiewicz, J., & Wolf, W. M. (2015). Heavy metal uptake by herbs. IV. Infuence of soil pH on the content of heavy metals in Valeriana ofcinalis L. Water, Air, & Soil Pollution, 226(4), 1-8. https://doi.org/10.1007/s11270-015-2360-3

Adriano, D. C. (1986). Other trace elements. Trace Elements in the Terrestrial Environment . Springer, New York, NY.

Aytac, Z., & TÜRKMEN, Z. (2011). A new Onosma (Boraginaceae) species from southern Anatolia, Turkey. Turkish journal of botany, 35(3), 269- 274. https://doi.org/10.3906/bot-1002-65

Baker, A. J., & Brooks, R. (1989). Terrestrial higher plants which hyperaccumulate metallic elements. A review of their distribution, ecology and phytochemistry. Biorecovery., 1(2), 81-126.

Page 6/9 Baker, A. J. M., McGrath, S. P., Sidoli, C. M. D., & Reeves, R. D. (1994). The possibility of in situ heavy metal decontamination of polluted soils using crops of metal-accumulating plants. Resources, Conservation and Recycling, 11(1-4), 41-49. https://doi.org/10.1016/0921-3449(94)90077-9

Barman, S. C., Sahu, R. K., Bhargava, S. K., & Chaterjee, C. (2000). Distribution of heavy metals in wheat, mustard, and weed grown in feld irrigated with industrial efuents. Bulletin of Environmental Contamination and Toxicology, 64(4), 489-496. https://doi.org/10.1007/s001280000030

Bingöl, A. F. (1978). Pétrologie du massif ophiolitique de Pozanti-Karsanti (Taurus cilicien, Turquie): Étude de la partie orientale. UER des Sciences de la vie et de la terre, Laboratoire de Minéralogie et Pétrographie.

Bouyoucos, G. J. (1951). A recalibration of the hydrometer method for making mechanical analysis of soils 1. Agronomy journal, 43(9), 434- 438. https://doi.org/10.2134/agronj1951.00021962004300090005x

Brooks, R. R., & Radford, C. C. (1978). Nickel accumulation by European species of the genus Alyssum. Proceedings of the Royal Society of London. Series B. Biological Sciences, 200(1139), 217-224.

Dai, J., Becquer, T., Rouiller, J. H., Reversat, G., Bernhard-Reversat, F., & Lavelle, P. (2004). Infuence of heavy metals on C and N mineralisation and microbial biomass in Zn-, Pb-, Cu-, and Cd-contaminated soils. Applied Soil Ecology, 25(2), 99-109. https://doi.org/10.1016/j.apsoil.2003.09.003

Das, S., Ram, S. S., Sahu, H. K., Rao, D. S., Chakraborty, A., Sudarshan, M., & Thatoi, H. N. (2013). A study on soil physico-chemical, microbial and metal content in Sukinda chromite mine of Odisha, India. Environmental earth sciences, 69(8), 2487-2497. https://doi.org/10.1007/s12665-012-2074-4

Davies, B. E., Paveley, C. F., & Wixson, B. G. (1993). Use of limestone wastes from metal mining as agricultural lime: potential heavy metal limitations. Soil use and management, 9(2), 47-52. https://doi.org/10.1111/j.1475-2743.1993.tb00928.x

Davis P.H. (Ed.) (1965–1985). Flora of Turkey and the East Aegean Islands Vol. 1-9. Edinburgh, Edinburgh University Press.

DeGrood, S. H., Claassen, V. P., & Scow, K. M. (2005). Microbial community composition on native and drastically disturbed serpentine soils. Soil Biology and Biochemistry, 37(8), 1427-1435. https://doi.org/10.1016/j.soilbio.2004.12.013

Duchaufour P. (1970). Precis de Pedologie. Masson et C1e, Paris.

Ghosh, M., & Singh, S. P. (2005). A review on phytoremediation of heavy metals and utilization of it’s by products. Asian J Energy Environ, 6(4), 18.

IBM Corp. (2013). IBM SPSS Statistics for Windows, Version 22.0. Armonk, NY: IBM Corp.

István P., Benton J.J. (1997). Hand book of trace elements, Boca Raton, St. Lucie Press

Jackson, M. L. (1958). Soil chemical analysis prentice Hall. Inc., Englewood Cliffs, NJ, 498, 183-204. https://doi.org/10.1002/jpln.19590850311

Kabata-Pendias, A., & Pendias, H. (2001). Trace elements in soils and plants, 3rd edn CRC Press. Boca Raton, FL, USA.

Kaçar, B., & İnal, A. (2008). Bitki analizleri. Nobel Yayın Dağıtım.

Kızıldağ, N. (2017). Doğu Akdeniz Bölgesindeki Krom Maden Alanı Topraklarında Azot Mineralizasyonu. Toprak Su Dergisi, 6(1), 52- 57. https://doi.org/10.21657/topraksu.305725

Krishna, A. K., Mohan, K. R., Murthy, N. N., Periasamy, V., Bipinkumar, G., Manohar, K., & Rao, S. S. (2013). Assessment of heavy metal contamination in soils around chromite mining areas, Nuggihalli, Karnataka, India. Environmental earth sciences, 70(2), 699-708. https://doi.org/10.1007/s12665-012-2153-6

Madrid, F., Lopez, R., & Cabrera, F. (2007). Metal accumulation in soil after application of municipal solid waste compost under intensive farming conditions. Agriculture, ecosystems & environment, 119(3-4), 249-256. https://doi.org/10.1016/j.agee.2006.07.006

Marques, A. P., Moreira, H., Rangel, A. O., & Castro, P. M. (2009). Arsenic, lead and nickel accumulation in Rubus ulmifolius growing in contaminated soil in Portugal. Journal of Hazardous Materials, 165(1-3), 174-179. https://doi.org/10.1016/j.jhazmat.2008.09.102

Mbarki, S., Labidi, N., Mahmoudi, H., Jedidi, N., & Abdelly, C. (2008). Contrasting effects of municipal compost on alfalfa growth in clay and in sandy soils: N, P, K, content and heavy metal toxicity. Bioresource Technology, 99(15), 6745-6750. https://doi.org/10.1016/j.biortech.2008.01.010

Olowoyo, J. O., Odiwe, A. I., Mkolo, N. M., & Macheka, L. (2013). Investigating the Concentrations of Different Elements in Soil and Plant Composition from a Mining Area. Polish Journal of Environmental Studies, 22(4).

Pal, A., Dutta, S., Mukherjee, P. K., & Paul, A. K. (2005). Occurrence of heavy metal‐resistance in microfora from serpentine soil of Andaman. Journal of Basic Microbiology: An International Journal on Biochemistry, Physiology, Genetics, Morphology, and Ecology of Microorganisms, 45(3), 207- 218. https://doi.org/10.1002/jobm.200410499

Pantola, R. C., & Alam, A. (2014). Potential of Brassicaceae Burnett (Mustard family; Angiosperms) in phytoremediation of heavy metals. International Journal of Scientifc Research in Environmental Sciences, 2(4), 120. https://doi.org/10.12983/ijsres-2014-p0120-0138

Page 7/9 Pilon-Smits E. (2005). Phytoremediation. Annu Rev Plant Biol, 56:15–39. https://doi.org/10.1146/annurev.arplant.56.032604.144214

Samantaray, S., Rout, G. R., & Das, P. (2001). Heavy metal and nutrient concentration in soil and plants growing on a metalliferous chromite minespoil. Environmental technology, 22(10), 1147-1154. https://doi.org/10.1080/09593332208618204

Sun, Z., Chen, J., Wang, X., & Lv, C. (2016). Heavy metal accumulation in native plants at a metallurgy waste site in rural areas of Northern China. Ecological Engineering, 86, 60-68.

U.S. EPA. (2007). Method 3051A (SW-846): Microwave Assisted Acid Digestion of Sediments, Sludges, and Oils, Revision 1. Washington, DC.

Wan, X., Lei, M., & Chen, T. (2016). Cost–beneft calculation of phytoremediation technology for heavy-metal-contaminated soil. Science of the total environment, 563, 796-802. https://doi.org/10.1016/j.scitotenv.2015.12.080

Wei, S., Zhou, Q., & Mathews, S. (2008). A newly found cadmium accumulator-Taraxacum mongolicum. Journal of hazardous materials, 159(2-3), 544- 547. https://doi.org/10.1016/j.jhazmat.2008.02.052

Yang, W., Zhao, F., Ding, Z., Wang, Y., Zhang, X., Zhu, Z., & Yang, X. (2018). Variation of tolerance and accumulation to excess iron in 24 willow clones: Implications for phytoextraction. International journal of phytoremediation, 20(13), 1284-1291. https://doi.org/10.1080/15226514.2014.922927

Ye, Z. H., Wong, J. W. C., & Wong, M. H. (2000). Vegetation response to lime and manure compost amendments on acid lead/zinc mine tailings: a greenhouse study. Restoration Ecology, 8(3), 289-295. https://doi.org/10.1046/j.1526-100x.2000.80041.x

Yoon, J., Cao, X., Zhou, Q., & Ma, L. Q. (2006). Accumulation of Pb, Cu, and Zn in native plants growing on a contaminated Florida site. Science of the total environment, 368(2-3), 456-464. https://doi.org/10.1016/j.scitotenv.2006.01.016

Zeng, F., Ali, S., Zhang, H., Ouyang, Y., Qiu, B., Wu, F., & Zhang, G. (2011). The infuence of pH and organic matter content in paddy soil on heavy metal availability and their uptake by rice plants. Environmental pollution, 159(1), 84-91. https://doi.org/10.1016/j.envpol.2010.09.019

Figures

Page 8/9 Figure 1

Evaluated chromium mining sites.

Figure 2

BCF (Root, Stem, Leaves) calculations for heavy metal concentrations in plants.

Figure 3

TLP (Stem, Leaves) calculations for heavy metal concentrations in plants.

Page 9/9