Ecotoxicology and Environmental Safety 220 (2021) 112368

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Ecotoxicology and Environmental Safety

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

Evaluation of phytoremediation potential of native dominant plants and

spatial distribution of heavy metals in abandoned mining area in
Southwest China
Bohan Wu a, He Peng a, Mingping Sheng a, Huanyan Luo a, Xitong Wang a, Rong Zhang a,
Fei Xu a, *, Heng Xu a, b, *
a
Key Laboratory of Bio-Resource and Eco-Environment of Ministry of Education, College of Life Sciences, Sichuan University, Chengdu 610065, Sichuan, PR China
b
Key Laboratory of Environment Protection, Soil Ecological Protection and Pollution Control, Sichuan University & Department of Ecology and Environment of Sichuan,
Chengdu 610065, Sichuan, PR China

A R T I C L E I N F O A B S T R A C T

Edited by: Dr R. Pereira A field investigation on the content of heavy metals in soils and dominant plants was conducted in three sites
(A<0.5 km, B<1.0 km, C<1.5 km) with different distances of mine tailings. The spatial distribution of heavy
Keywords: metals and the accumulation in plants were compared, and the candidate species for ecosystem restoration were
Dominant plants selected. The results indicated that the soil was polluted by chromium (Cr), Cadmium (Cd), copper (Cu), nickel
Phytoremediation
(Ni) in varying degrees, which is 2.07, 2.60, 1.79, and 4.49 times higher than the Class-II standard in China. The
Accumulation
concentrate of Ni, Cd, and Zinc (Zn) increased, while Cr, Lead (Pb), and Cu decreased with the distance from the
Heavy metals
Mine mine tailings. 73 species (34 families) were found and mainly herbaceous plants. The concentrate of Cd, Cu, Cr,
and Ni in 29 dominant plants were measured and 66.67%, 21.43%, 100%, 47.62% plants exceeded the normal
concentration range. Based on the comparative analysis of heavy metal content, bioconcentration factor, and
translocation factor in plants, Polygonum capitatum has good phytoextraction ability, Boehmeria nivea, Chrysan­
themum indicum, Miscanthus floridulus, Conyza canadensis, Rubus setchuenensis, Senecio scandens, and Arthraxon
hispidus showed remarkable phytostabilization abilities of Cr, Cd, Ni, and Cu, which can be used as potential
phytoremediation candidate.

1. Introduction and biological remediation (Wei et al., 2020; Sarwar et al., 2017).
Generally, disadvantages exist in physical and chemical methods such as
Mining provides a lot of material and energy for human society high cost, irreversible soil properties, and secondary pollution (Xin
(Omer, 2008; Zhu et al., 2018). However, large area of soil have been et al., 2020; Salas-Moreno and Marrugo-Negrete, 2020). Among these
contaminated with heavy metals because of the mine tailings or dis­ restoration methods, phytoremediation has been widely used due to its
charged wastewater, especially in China (Liu et al., 2020b; Cui et al., advantages of cost-effective, economical, eco-friendly, and sustainable
2020; Li et al., 2014). Heavy metal pollution has the characteristics of (Emenike et al., 2018; Li et al., 2020b). Currently, As hyperaccumulators
long-term, concealment, accumulation, extensiveness, and irrevers­ such as Pteris vittata (Yang et al., 2020) and Pteris cretica (Jeong et al.,
ibility (Ali et al., 2013; Stylianou et al., 2020), which pose serious 2015), Zn hyperaccumulator Sedum alfredii (Zhu et al., 2019), Cd
environmental threats (Shen et al., 2017). It not only reduces the quality hyperaccumulator Viola baoshanensis (Wu et al., 2010), and Mn hyper­
of soil, water, and crops but also leads to serious human health risks accumulator Phytolacca acinose (Xue et al., 2010) have been found in
through the food chain (Li et al., 2020a; Wei et al., 2020). Therefore, it is China for the phytoremediation of mine tailings. However, the lack of
necessary to block and clean up the heavy metal contaminated areas to nutrients, extreme pH value, loose and flowing soil, poor fertilizer and
minimize their impacts on the ambient ecosystem. water-holding capacity, and excessively high surface temperature in the
The methods of soil remediation mainly include physical, chemical, mining area makes the remediation plants hard to survive and unable to

* Corresponding author.
* Correspondence to: Sichuan University, No.24 South Section 1, Yihuan Road, Chengdu 610065, China.
E-mail addresses: [email protected] (F. Xu), [email protected] (H. Xu).

https://doi.org/10.1016/j.ecoenv.2021.112368
Received 17 October 2020; Received in revised form 17 May 2021; Accepted 23 May 2021
Available online 31 May 2021
0147-6513/© 2021 Published by Elsevier Inc. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
B. Wu et al. Ecotoxicology and Environmental Safety 220 (2021) 112368

achieve the phytoremediation function (Xiao et al., 2018; Wei et al., the enrichment and migration potentials of these native dominant
2020). plants, screen out species with remediation potential and apply them to
The solution is to select native dominant plants with phytor­ the phytoremediation project in this mine tailings area. The research
emediation capacity (Rufo and de la Fuente, 2010; Wei et al., 2020). results can provide a guidance and reference for remediation of heavy
These plants should have well-developed roots and large biomass, which metal contaminated soil in the mining area and other similar environ­
can thrive in the mining area and tolerate the high metal concentrations mental conditions.
(Wei et al., 2020), thereby fixing or extracting heavy metals in the
contaminated soil (Liu et al., 2020b). Native dominant plants are 2. Materials and methods
considered keys to the restoration and phytoremediation of heavy metal
influenced soils, especially in mining areas (Stylianou et al., 2020; 2.1. Site description
Parraga-Aguado et al., 2013). Xiao et al. (2018) investigated the heavy
metals of soil and plants around a zinc smelter in Feng Country, China, The study area was a typical karst landform located in a wasteland of
and found that Symphytum officinale Linn. has a great capacities for the downstream of a pyrite mine in the southwestern of Xingwen
absorb Cd, Pb, and Zn and can be used in phytoremediation. Midhat County, Sichuan Province, China (Fig. 1). This area has a subtropical
et al. (2019) assessed the mental pollution in soils and accumulation humid monsoon climate with an average temperature of 17.6 ◦ C and an
potential of plants in three abandoned mining sites in Morocco, selected average rainfall of 1344.9 mm. This pyrite mine was closed in the 1990
8 native plants were considered as the best-performing specimens with s, but after more than four decades of mining, mountains of slag have
strong tolerance and the ability to accumulate heavy metals as effective piled up. Due to the smelter, soils in the study areas were severely
tools for phytoremediation. Therefore, the vegetation surveys around contaminated. The surveyed area is high in the northwest and low in the
the contaminated areas to screen the native accumulators is the pre­ southeast, with an elevation of 545.96–504.64 m and a height difference
requisite of future systemic phytoremediation (Stylianou et al., 2020; of 41.32 m. The slag heaps are located in a high-altitude area. In the
Zhu et al., 2018). long-term stacking process, heavy metals from the slag heaps enter the
Due to the accumulation of tailings and frequent earthquakes in surrounding soil due to scouring and leaching through rainfall, causing
Xingwen County, Sichuan Province, serious contaminated has been soil environmental pollution. In recent years, frequent earthquakes have
caused to the surrounding areas, which endangers the environment and aggravated pollute heavy metals, so it is urgent to treat the waste dumps
human health. At present, although there are many studies on utilizing and contaminated soil in this area for agricultural production and resi­
native plants for phytoremediation of mine tailings (Zhu et al., 2018; Liu dents’ safety purpose.
et al., 2020b; Ghazaryan et al., 2019), the application of native plants in Three sites were classified as being within about 0.5 km (A),1.0 km
this study area is very weak and there is no information on their vege­ (B), and 1.5 km (C) from the mine tailings to identify the distribution of
tation distribution, metal concentrations in plants and soils. Therefore, heavy metals in soil. The detailed map of study sites was presented in
the aim of this study is:(1) to investigate the spatial distribution of soil Fig. 1.
heavy metals in this region; (2) to explore the abundance and distribu­
tion of vegetation in different distances away from tailings; (3) to
measure metal contents in the native dominant plants; (4) to evaluate

Fig. 1. Location map and different sampling sites of investigated mining areas. Three sites were classified as being within about 0.5 km (A),1.0 km (B), and 1.5 km
(C) away from the mine tailings.

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2.2. Sample collection and pretreatment analyses were performed using R (analysis of variance one way ANOVA
with Tukey’s Test, Pearson’s correlations).
The field investigation was carried out in June 2020. The environ­
mental status and the vegetation pattern were studied by taking the 3. Results and discussion
samples from the sites. The analysis of vegetation pattern and plant
species distribution at different studied sites was undertaken to identify 3.1. Composition and dominant plants
the dominant plant species through the quadrat method of analysis. In
each site, 5 plots (2 m × 2 m) were randomly selected, in which the Regarding the life form of plants (Table S1), the vegetation was
plant varieties, quantities, height, and the coverage were recorded. dominated by herbaceous plants in the study area, which accounted for
Collected plant species were identified and named at taxonomy division. 65.22%, similar to the previous studies (Zhu et al., 2018; Xiao et al.,
Additionally, there were five replicates of each species and soils. 3–5 2018; Marrugo-Negrete et al., 2017). The simple composition of the
individual plants were collected and combined into one sample at each plants is probably caused by low soil fertility, which limited plants’
plot. Simultaneously, the soils (0–20 cm) were collected based on the growth (Mohanty et al., 2012). With fine and light seeds quantity, easy
five-point sampling method and homogenized as a composite one. All propagation, and fast germination, herbaceous plants can easily survive
soil and plant samples were sealed in clean polythene bags for transport in the contaminated areas (Zhu et al., 2018; Karaca et al., 2017). Also,
to the laboratory. herbaceous plants have the developed roots, fast growth rates, and the
Once in the lab, the fresh plants were carefully and repeatedly capacity to grow in barren sites (Yang et al., 2014). Therefore, herba­
washed with tap water and rinsed three times with deionized water, ceous are more likely to develop a tolerance to heavy metals. The
then the plant samples were treated by high-temperature desiccation common hyperaccumulators Pteris vittaia, Festuca arundinacea, Lolium
under 105 ℃ for 30 min, and oven-dried at 65 ℃ to constant weight. perenne, and Vetiveria zizanioides are all herbaceous plants (Steliga and
The dried plant tissues were then separated into roots and shoots, milled Kluk, 2020; Liu et al., 2018; Wei et al., 2020).
into a fine powder, and placed in polythene bags for further analyses. In total, 73 species of native plants were collected and classified into
The soil samples were air-dried, milled to a particle size less than 34 families (Fig. 2A, Table S1). 20 species (belonging to 19 genera in 11
0.147 mm (Xiao et al., 2018), and stored in polyethylene bags until families) were observed in site A. Six plant samples were identified as
analyzed. Asteraceae, followed by Gramineae (2), Thelypteridaceae (2), Polygo­
naceae (2), and Urticaceae(2). The highest plant diversity is in site B with
2.3. Sample analysis 47 species (belonging to 38 genera in 23 families), among which Rosa­
ceae (12) had the most plants, followed by Asteraceae (5), Gramineae (4),
The soil pH were measured by the pH meter (METTLER-S220). Labiatae (4), Urticaceae (3). 37 species (belonging to 36 genera in 23
Cation exchange capacity (CEC) were determined according to Liu et al. families) were observed in site C, among which Gramineae (5), Aster­
(2020a). Soil organic matter (SOM) were analyzed as previous aceae (5), Rosaceae (5) had the most plants, followed by Labiatae (2) and
description (Walz et al., 2017). Total Nitrogen (TN) were determined Urticaceae (2). Moreover, M floridulus from Gramineae were the domi­
using the Kjeldahl method. Total phosphate (TP) and potassium (TK) nant plant species in all sites. The coverage of Gramineae was the highest
were determined using the Mehlich extractor method. Organic Carbon in the three sites, and the total coverage of site C was the highest(Fig. 2B,
(OC) were determined by the oxidation of organic matter using potas­ Table S1). The vegetation coverage increased with the increase of dis­
sium dichromate. The content of soil alkali-hydrolyzed nitrogen (AN) tance from the mine tailings, which may be related to the change of soil
were measured according to Wang (2017). Soil available phosphorus heavy metal concentration and soil nutrients with the distance. Overall,
(OP) were determined with sodium bicarbonate extraction method Gramineae were the most frequently encountered in the three sites,
(Olsen, 1954). Soil available potassium (AK) were determined by which had the highest coverage (61.27%) and dominance (40.66%),
NH4AC extraction-flame photometry method (Guangming et al., 2017). followed by Urticaceae (15.47%) and Asteraceae (10.71%). These plants
The soil and plant samples (1 g) were digested using HNO3 and H2O2 are with lightly small seeds, able to endure the harsh mine surrounding
(5:2, v/v) according to Tuzen et al. (2007), then determined by induc­ environment, easily spread by the wind, thereby widely distributed.
tively coupled plasma mass spectrometry (ICP-MS, aurora M90). Besides, they generally have higher biomass, which can form a single
species and is also easy to form a community with some other plants
2.4. Calculation of phytoremediation indices (Midhat et al., 2019). Therefore, they were frequently utilized for heavy
metal contaminated soil remediation (Bothe, 2011).
The bioaccumulation factor (BAF) was calculated to determine the
efficiency of the plant accumulating heavy metals from soil. While the 3.2. Physicochemical properties of soil
translocation factor (TF) was calculated to evaluate the ability of plants
to translocate heavy metals from roots to shoots. The phytoremediation The soil properties of the study area are presented in Table 1. The
indices were calculated using the following formula (Mohanty et al., soils showed an acidic condition with rather low nutrients contents. The
2012). pH of the sites (4.05,6.22,6.88 for site A, B, and C, respectively) grad­
ually increases with the distance increasing from the mine tailing,
BAF=C plant root /C soil indicating the soil properties have been seriously affected by the tailing.
TF=C The metal sulfides such as pyrite and pyrrhotite in the tailings can be
plant shoot/C plant root
oxidized easily under natural weathering conditions, producing large
BAF and TF are often used to evaluate the efficiency of heavy metal quantities of acid mining drainage (AMD), influencing the surrounding
accumulation in plants, and estimate the potential of plant for phy­ environment (Tuo et al., 2014). The farther the studied sites are from the
toextraction and/or phytostabilization (Ali et al., 2013; Xiao et al., mine tailing, the more suitable they are for the plants’ growth, with
2017). more vegetation and higher soil nutrients.
Site A, which was nearest to the mine tailings (<0.5 km), showed a
2.5. Statistical analysis significantly lower soil physio-chemical indices (CEC, SOM, TN, TK, AN,
OP, AK) than other sites (<0.05), except for TP. With the distance from
The spatial distribution map of heavy metals in the study area was the tailings, the soil indices gradually increased, the highest SOM, TC,
made in ArcGIS 10.2 software using the Inverse Distance Weighted TN, AN, and AK were observed in site B (0.5–1.0 km), while the highest
(IDW) interpolation method (Manson et al., 1999). All the statistical CEC, TK, and OP were determined in site C (1.0–1.5 km). To investigate

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Fig. 2. Composition(A) and coverage(B) of the family of species in different study sites.

Table 1
Physicochemical parameters and concentrations of heavy metals in soils from different sites.
Sample site A B C Threshold

Mean SD CV Mean SD CV Mean SD CV

pH 4.05a 0.58 0.14 6.22b 1.36 0.22 6.88 BCE 0.48 0.07
CEC(cmol/kg) 12.25a 0.15 0.01 11.77b 0.68 0.06 15.76c 1.20 0.08
SOM(g/kg) 31.75a 6.18 0.19 62.35b 12.07 0.19 43.69a 12.07 0.28
TC(%) 1.79a 0.32 0.18 5.24b 0.78 0.15 2.31a 0.78 0.34
TN(g/kg) 0.84a 0.14 0.17 2.35b 0.46 0.19 1.31a 0.46 0.35
TK(g/kg) 4.41a 0.30 0.07 6.95b 0.84 0.12 7.06 BCE 0.84 0.12
TP(g/kg) 0.73a 0.14 0.19 0.87a 0.18 0.21 0.87a 0.18 0.21
AN(mg/kg) 57.44a 0.48 0.01 97.77b 2.38 0.02 72.50c 3.49 0.05
AK(mg/kg) 30.55a 3.89 0.13 68.45b 3.87 0.06 63.44 BCE 3.87 0.06
OP(mg/kg) 0.82a 0.00 0.00 3.90b 0.00 0.00 4.17c 0.00 0.00
Clay(%) 8.4a 1.77 0.21 9.8ab 2.05 0.21 11.10b 0.24 0.02
Silt(%) 16a 0.76 0.05 14.80b 1.38 0.09 21.00c 0.94 0.04
Sand(%) 75.60a 1.01 0.01 75.40a 3.29 0.04 67.90b 3.13 0.05
Texture sandy sandy sandy
Cd(mg/kg) 0.56a 0.19 0.35 1.28ab 0.68 0.53 1.52b 0.68 0.45 0.3
Cr(mg/kg) 389.05a 94.49 0.24 279.68b 37.68 0.13 232.50 BCE 37.68 0.16 150
Ni(mg/kg) 53.84a 7.44 0.14 56.87ab 8.82 0.16 89.46b 8.82 0.10 40
Cu(mg/kg) 179.68a 30.25 0.17 119.31b 14.19 0.12 161.90ab 14.19 0.09 50
Zn(mg/kg) 101.66a 4.62 0.05 107.23a 7.19 0.07 119.64a 7.19 0.06 200
Pb(mg/kg) 47.06a 8.01 0.17 41.54a 9.84 0.24 37.98a 9.84 0.26 250

Note: Different letters behind the average indicate significant differences existed among different sampling sites (p < 0.05). SD: standard deviation; CV: Coefficient of
variation; Threshold: The Class-IIstandard of soil environment quality in China.

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the correlation between the soil physicochemical parameters, pearson Ni, Cd, and Zn showed similar distribution, whose concentrations
correlation analysis (Fig. 5) was conducted, which indicated that TC, increased with the distance from the tailings (at the bottom). Due to
SOM, pH are significantly related to N, P, K. these heavy metals fractions change gradually with the downstream pH,
With the distance, the species richness gradually increased, the soil the leachate continues to bleed and diffuse, these heavy metals are not
nutrients gradually improved, indicating the relationship between easily absorbed by plants, so they accumulate in the downstream soil
native plants and soil nutrients is improved continuously (Hinsinger, (Xing et al., 2020). The concentration of Cr, Pb, and Cu decreased
2001). The secretions of plant roots provide carbon and nitrogen sources gradually from upstream to downstream, which may be related to the
for the growth and reproduction of plant rhizosphere microorganisms, gradual increase of vegetation that can absorb the heavy metals. Heavy
improving the soil property. The nitrogen-fixing bacteria that are sym­ metals in the soil beyond crustal background value generally have the
biotic with plants can increase nitrogen fixation from the atmosphere, same source (Shen et al., 2017). Further analysis of the correlation of the
increasing the soil nutrient content. Meanwhile, the well-developed six heavy metals in the soil also shows the six heavy metals can be
plant root can absorb more nutrients. Furthermore, the deposition and divided into Ni, Cd, Zn and Cr, Pb, Cu (Fig. S1A), of which Ni, Cd, and Zn
decomposition of plant biomass also increase the soil nutrient content may be derived from the primary minerals of the surrounding rocks, and
(Jones et al., 2009). The change of N, P, K, and SOM in soil are vital for Cr, Pb, and Cu may be derived from mine tailings. Pearson correlation
plant population and community structure. With the succession of plant analysis indicated a significant negative correlation between Cd, Ni, and
communities, plants, in turn, promote the increase of N, P, K, and Cr, while a significant positive correlation between Cd, Ni, and Zn was
organic matter in the soil, and finally form a virtuous cycle (Burges et al., found (Fig. 4), indicated that these elements might have common
2018). The soils in all sites showed sandy loam texture, with low vis­ sources, mutual dependence, and similar behavior during transport. Cr,
cosity, large porosity, strong aeration and permeability, poor water Cu, Pb were negatively correlated with these physicochemical parame­
storage, and fertilizer retention, which were not conducive to plant ters. Principal component analysis (PCA) proved that heavy metals
growth. However, as the distance increased, the soil sand percentage concentrations were related to the distance from mine tailings
decreased gradually, which also showed the soil quality was improved (Fig. S1B).
by the thrive of the plants.
3.4. Heavy metal contents of dominant plants
3.3. Metal contents in the surface soils
8, 18, and 16 dominant plants were selected in site A, B, and C, 29
The soil heavy metal contents in the study area are shown in Table 1. species in total (Zhu et al., 2018). Metal accumulation in different parts
In the three studied sites, the concentrations of Cr, Cu, Zn, Ni, Pb and Cd of the plants collected from different sites (A, B, C) is illustrated in Fig. 5.
varies from 176.54 to 512.00 mg/kg, 97.06–248.92 mg/kg, Metal concentrations in the investigated plants were variable. They were
94.33–154.93 mg/kg, 41.67–151.17 mg/kg, 17.94–59.38 mg/kg, different in the same plant species of different sites and in different plant
0.28–2.45 mg/kg respectively. Cr, Cu, Ni and Cd were far exceeded the species of the same site. C. indicum, F. vesca, S. scandens showed the
Grade-II standard for soil environment quality of China highest Zn content in the three sites respectively. The average content of
(GB15618–1995), indicating the soils of all the three sites were heavily Pb was the highest in C. indicum, P. capitatum. However, the content of
polluted. Zn and Pb in the soil of the studied site did not exceed the standard. The
Fig. 3 presented the spatial analysis of heavy metals in the study area. highest average content of Cu was C. indicum, followed by

Fig. 3. Spatial distribution maps of heavy metals in study area.

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Fig. 4. Pearson correlation coefficient between soil heavy metals and physicochemical parameters.

C. canadensisand P. capitatum. The highest average content of Cd were C growth, photosynthesis, antioxidant enzyme system) after a long period
acuminatus, C. canadensis and S. scandens. R. setchuenensis, P. capitatum of natural selection (Song et al., 2020; Peco et al., 2020). These plants
had the highest average content of Ni. The highest average content of Cr are tolerant to Cd, Cr, Ni and Cu, and can be used as pioneer species or
were M. floridulus, P. capitatum and C canadensis. Moreover, details on potential accumulator for the remediation of contaminated soils.
metal distribution in shoots and roots were given in Tables S2.
The heavy metal contents in roots and shoots of the dominant plants 3.5. Evaluation of heavy metals accumulation and translocation potential
are presented in Fig. S2, which varies. The differences in the total metal
concentrations and their bioavailability might cause varied metal Because of the soil heavy metal concentration in the study area were
accumulation in plants. Plants transport metals from roots to shoots far exceeded the Soil Environmental Quality Risk Control Standard for
through root pressure and leaf transpiration. The metal content in roots Agricultural Land Soil Pollution of China (GB15618–2018) (Liu et al.,
was much higher than shoots for all plants. (Rehman et al., 2007; Bose 2020a), it is necessary to study the accumulation and transport of the
et al., 2008). The roots can immobilize heavy metals by adsorbing them potential accumulators. The BAF and TF of heavy metals in 29 dominant
or forming precipitation in rhizosphere soil (Tangahu et al., 2011). The plants in the study area are shown in Fig. 6. Among the plant species, the
metal contents in plants were above the normal levels of general plants average value of BAFs of the six heavy metals decreased in the order of:
except for Zn and Pb, which were 1–160 mg⋅kg− 1 for Zn, Cd > Zn > Cu > Ni > Pb > Cr. C.canadensis, R.setchuenensis, C.indicum, F.
0.4–45.8 mg⋅kg− 1 for Cu, 0.1–10 mg⋅kg− 1 for Ni, 0.2–0.8 mg⋅kg− 1 for tikoua, A.hispidus, S.scandens, P.capitatum showed strong enrichment
Cr, 0.1–41.7 mg⋅kg− 1 for Pb, 0.2–0.8 mg⋅kg− 1 for Cd, respectively (Zhu ability to Cd only. They are more efficient at removing Cd from the soil.
et al., 2018). Table S3 compares the absorption capacity of heavy metals by plants in
Correlations between soil and plant metal concentrations are pre­ different study areas, where the BAFs for Cd was higher than other heavy
sented in Fig. S3. Significant correlations were found between total soil metals in most of the studies. Chang Kee et al. (2018) reported the
concentrations and plant Cr (R2 = 0.921), Ni (R2 = 0.992), Cd (R2 highest BAF value of plants in the Central-Northern Peru that J.bufonius
= 0.8221), and Pb (R2 = 0.4918) concentrations. The heavy metal (3.91) for Cd, A.alata (1.37) for Ni, W. nubigena (1.08) for Pb and A. alata
content accumulated by plants is related to the heavy metal content in (1.85) for Zn. It has been reported by Guarino et al. (2019) for Western
soil (Xing et al., 2020). Cu, Zn, and Ni are essential for plant growth, of Naples and Baycu et al. (2015) for Cyprus Turkish both showed that
which are related to many enzymes, regulatory proteins, the develop­ plants have the strongest absorption capacity for Cd.
ment and metabolism of plants (Küpper and Andresen, 2016). Never­ The highest value of TF in dominant plants for Zn is with an average
theless, the excessive presence of these will seriously affect the normal value of 1.16, and the lowest for Cr is with an average value of 0.27. The
physiologica of plants (Guo et al., 2020). Cr, Cd and Pb are not essential average value of TFs of the six heavy metals decreased in the order of
for plants, which have adverse effects on plant growth and metabolism, Zn>Cd>Pb>Ni>Cu>Cr. C.acuminatus for Zn, Cd, Pb, S.scandens for Cu,
leading to inhibition of seed germination, reduction of biomass, chlo­ Ni, Cd, Pb, P.capitatum for Ni, Cu, Zn, Cd, Pb, C.canadensis for Pb, Cd, Zn,
rosis of leaves, and even mutagenesis (Nawab et al., 2015). Dominant C indicum and F. tikoua for Zn, Cd showed strong transfer ability (TF>1).
plants had obvious tolerance and accumulation characteristics for Cd, However, the TF is below 1 in all plants for Cr, indicating that Cr was
Cu, Cr, and Ni. As native plants, they may have developed a defense mainly accumulated in the roots and rarely transported to the shoots. TF
strategy to the high-level heavy metals and had good tolerance (such as can explain the transfer and redistribution of heavy metals among

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Fig. 5. Heavy metals concentration in different parts of the plants collected from the different sites. Different letters indicate significant differences in the total heavy
metal content of different plants (p < 0.05).

different parts of plants (Zhang et al., 2020; Dai et al., 2013). Plants with pollution in the soil can be gradually reduced by phytoextraction with
strong transferability can absorb heavy metals in the soil around the strong accumulation and transfer capacity. Also, phytoremediation can
rhizosphere through their roots, and transfer most of them to their be realized by phytostabilization with low TF, high BAF, and
shoots to protect the roots from toxicity and maintain their normal life well-developed root (Zhan et al., 2014; Wei et al., 2012).
(Pandey et al., 2016; Rodriguez et al., 2012). Plant response to heavy metals in soil depends on plant species, total
It can be seen from Table S3 that the same species has different ab­ soil metal concentration, the bioavailability of the metals themselves,
sorption capacity in different areas. In the present investigation C.can­ and physical and chemical properties of the soil (Bonanno, 2011; Gha­
adensis showed a BAF value of 0.18 for Pb, the research by Zhu et al. zaryan et al., 2019). Results proved the strong enrichment and transport
(2018) showed 1.96 for Pb. This dissimilarity may be due to different ability of the dominant plant P. capitatum for Ni, Cu, Zn, Cr, and Pb.
soil pollution conditions and different forms of heavy metals (Zhan et al., Some other dominant plants were also found similar metal accumulation
2014). Moreover, the BAFs varied dramatically among different plant ability with low TF and high BAF value (B.nivea for Cd, Cu, Zn and Pb, C.
species in the same studied area (Table S3) because of their different indicum for Cd, Cu, Cr and Pb, M.floridulus for Pb, Cu, Ni, Cr, C.canadensis
absorption and tolerance strategies for different heavy metals (Rascio for Cr, Ni, Cu, Pb and Cd, R.setchuenensis for Ni and Cd, S.scandens for Zn
and Navari-Izzo, 2011). In the process of phytoremediation, heavy metal and Cd, A.hispidus for Cu and Zn), which could extract and stabilize

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Fig. 6. BAF and TF of dominant plants in the study areas.

heavy metals in the rhizosphere. In general, the soil in the study area is 4. Conclusions
mainly polluted by Cr, Cd, Ni and Cu, for which P. capitatum has good
phytoextraction ability, B.nivea, C.indicum, M.floridulus, C.canadensis, R. 73 plants (34 families) were observed in the field survey, mainly
setchuenensis, S.scandens, and A.hispidus have good phytostabilization herbaceous plants and Gramineae. On the whole, the soil in this area is
ability (Table 2). Moreover, most of these plants are common perennial sandy and acidic soils mainly polluted by Cr, Cd, Ni, Cu. The concen­
herbs, which can settle, grow and reproduce in the wasteland in a short tration of soil heavy metals, the soil fertility, and the texture is related to
time and produce a large amount of biomass (Mohanty and Kumar Patra, the distance from the mine tailings. Moreover, the vegetation coverage
2020; Guarino et al., 2019). Therefore, they are expected to be applied and richness increased with the distance and played a certain role in the
to phytoremediation of soil heavy metals pollution in this area. accumulation and transportation of heavy metals. Based on the

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Table 2 Bothe, H., 2011. Plants in heavy metal soils. In: Sherameti, I., Varma, A. (Eds.),
The heavy metal removal capacity of the eight dominant plants in the study area. Detoxification of Heavy Metals. Springer Berlin Heidelberg, Berlin, Heidelberg,
pp. 35–57.
Dominant plant Heavy metal Function Burges, A., Alkorta, I., Epelde, L., Garbisu, C., 2018. From phytoremediation of soil
contaminants to phytomanagement of ecosystem services in metal contaminated
P. capitatum Ni, Cu, Zn, Cr, Pb phytoextraction sites. Int J. Phytoremediat. 20, 384–397.
B.nivea Cd, Cu, Zn, Pb phytostabilization Chang Kee, J., Gonzales, M.J., Ponce, O., Ramírez, L., León, V., Torres, A., Corpus, M.,
C.indicum Cd, Cu, Cr, Pb phytostabilization Loayza-Muro, R., 2018. Accumulation of heavy metals in native Andean plants:
M.floridulus Pb, Cu, Ni, Cr phytostabilization potential tools for soil phytoremediation in Ancash (Peru). Environ. Sci. Pollut. Res.
C.canadensis Cr, Ni, Cu, Pb, Cd phytostabilization 25, 33957–33966.
R.setchuenensis Ni, Cd phytostabilization Cui, J.L., Zhao, Y.P., Chan, T.S., Zhang, L.L., Tsang, D.C.W., Li, X.D., 2020. Spatial
S.scandens Zn, Cd phytostabilization distribution and molecular speciation of copper in indigenous plants from
A.hispidus Cu, Zn phytostabilization contaminated mine sites: implication for phytostabilization. J. Hazard Mater. 381,
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Guarino, C., Zuzolo, D., Marziano, M., Baiamonte, G., Morra, L., Benotti, D., Gresia, D.,
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CRediT authorship contribution statement plant species in situ: environmental implications and functional traits. Sci. Total
Environ. 650, 3156–3167.
Bohan Wu: Conceptualization, Investigation, Data curation, Writing Guo, B., Hong, C., Tong, W., Xu, M., Huang, C., Yin, H., Lin, Y., Fu, Q., 2020. Health risk
assessment of heavy metal pollution in a soil-rice system: a case study in the Jin-Qu
- original draft, Writing - review & editing, Visualization, Supervision. Basin of China. Sci. Rep. 10.
He Peng: Investigation, Data curation, Software. Mingping Sheng: Hinsinger, P., 2001. Bioavailability of soil inorganic P in the rhizosphere as affected by
Investigation, Visualization. Xitong Wang: Writing - review & editing. root-induced chemical changes: a review. Plant Soil 237, 173–195.
Jeong, S., Moon, H.S., Nam, K., 2015. Increased ecological risk due to the
Huanyan Luo: Writing - review & editing. Rong Zhang: Investigation. hyperaccumulation of As in Pteris cretica during the phytoremediation of an As-
Fei Xu: Revising and editing, Data processing, Supervision. Heng Xu: contaminated site. Chemosphere 122, 1–7.
Resources, Supervision, Project administration, Funding acquisition. Jones, D.L., Nguyen, C., Finlay, R.D., 2009. Carbon flow in the rhizosphere: carbon
trading at the soil-root interface. Plant Soil 321, 5–33.
Karaca, O., Cameselle, C., Reddy, K.R., 2017. Mine tailing disposal sites: contamination
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Declaration of Competing Interest Environ. Sci. Bio/Technol. 17, 205–228.
Küpper, H., Andresen, E., 2016. Mechanisms of metal toxicity in plants. Metallomics 8,
269–285.
The authors declare that they have no known competing financial Li, S., Wu, J., Huo, Y., Zhao, X., Xue, L., 2020a. Profiling multiple heavy metal
interests or personal relationships that could have appeared to influence contamination and bacterial communities surrounding an iron tailing pond in
the work reported in this paper. Northwest China. Sci. Total Environ.
Li, S., Zhao, B., Jin, M., Hu, L., Zhong, H., He, Z., 2020b. A comprehensive survey on the
horizontal and vertical distribution of heavy metals and microorganisms in soils of a
Acknowledgments Pb/Zn smelter. J. Hazard. Mater. 400, 123255.
Li, Z., Ma, Z., van der Kuijp, T.J., Yuan, Z., Huang, L., 2014. A review of soil heavy metal
pollution from mines in China: pollution and health risk assessment. Sci. Total
This study was financially supported by the National Key Research Environ. 468–469, 843–853.
and Development Program (2018YFC1802605), Agricultural science Liu, H., Wang, C., Xie, Y., Luo, Y., Sheng, M., Xu, F., Xu, H., 2020a. Ecological responses
of soil microbial abundance and diversity to cadmium and soil properties in
and Technology Achievements Transformation Program of Sichuan farmland around an enterprise-intensive region. J. Hazard Mater. 392, 122478.
Province (2017NZZJ008) and the Key Research and Development Pro­ Liu, K., Zhang, H., Liu, Y., Li, Y., Yu, F., 2020b. Investigation of plant species and their
gram of Sichuan Province (2017SZ0181, 2018NZ0008), the Funda­ heavy metal accumulation in manganese mine tailings in Pingle Mn mine, China.
Environ. Sci. Pollut. Res.
mental Research Funds for the Central Universities (SCU2019D013).
Liu, X., Feng, H.Y., Fu, J.W., Chen, Y., Liu, Y., Ma, L.Q., 2018. Arsenic-induced nutrient
The authors also wish to thank Director Zhi Xing, Engineer Kui Chen uptake in As-hyperaccumulator Pteris vittata and their potential role to enhance
from No. 605 of Sichuan Province Metallurgy Geological Bureau for plant growth. Chemosphere 198, 425–431.
Manson, S., Burrough, P., McDonnell, R., 1999. Principles of geographical information
their technical assistance.
systems: spatial information systems and geostatistics. Econ. Geogr. - Econ Geogr.
75.
Appendix A. Supporting information Marrugo-Negrete, J., Pinedo-Hernandez, J., Diez, S., 2017. Assessment of heavy metal
pollution, spatial distribution and origin in agricultural soils along the Sinu River
Basin, Colombia. Environ. Res. 154, 380–388.
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online version at doi:10.1016/j.ecoenv.2021.112368. heavy metals in metallophytes from three mining sites (Southern Centre Morocco)
and evaluation of their phytoremediation potential. Ecotoxicol. Environ. Saf. 169,
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