Introduction

Vanadium (V) is considered one of the most important elements in the steel, electronics and automotive production industries because of its utilisation in high-strength steel and battery manufacturing. Vanadium has been mined extensively in China, South Africa, Russia and the USA (Amorim et al. 2007). While petroleum and coal combustion are the main anthropogenic sources of V, it is also dispersed in the environment by weathering and using of phosphate-containing fertilisers (Vachirapatama et al. 2011). Vanadium is the fifth most abundant transitional metal in Earth’s crust (Imtiaz et al. 2015). Previous studies have reported that V retards plant nutrient and mineral absorption by obstructing hydrogen ion function in the plasma membrane, which is necessary for ATPase activity (Wuilloud et al. 2000). In soil, 30 mg kg−1 V causes toxicity and reduces plant biomass (Wang and Liu 1992), and Rosso et al. (2005) reported that V causes shoot mortality and reduces plant height in pickleweed (Salicornia), while Olness et al. (2002) observed that V significantly inhibited the growth of various plants. High concentrations of V inhibit plant growth by significantly reducing the shoot length, number of leaves and dry weights of roots, shoots and leaves in Chinese green mustard and tomato plants (Vachirapatama et al. 2011). Heinemann et al. (2000) showed that high levels of V cause renal damage, especially in patients with pre-existing renal function impairment.

Vanadium is an essential nutrient in numerous animals, and its deficiency causes metabolic disturbance or inhibition, growth retardation and reduced reproductive capacity in chickens and rats (Frank et al. 1996; McCrindle et al. 2001). However, excess levels of essential or non-essential elements in soil/substrata can have toxic effects on plants, animals and humans.

In this study, sites were investigated that have a range of V concentrations exceeding the permissible limit of the Chinese national standards (exposure draft; MEPPRC 2015), posing potential health risks to communities that farm and graze cattle adjacent to the mining area. There have been few reports of V distribution in soils or its accumulation in plants, and thus the behaviour and effects of V in most ecosystems remain poorly understood. Plants grown in metal-rich soils or mining areas exhibit innate tolerance and may accumulate large amounts of toxic metals. Species with the ability to accumulate greater than 1000 mg kg−1 of metals, with a bioaccumulation factor (BAF) or translocation factor (TF) value > 1, are considered to be hyperaccumulators (Yanqun et al. 2005). Plants with a BAF > 1 have the ability to phytostabilise, and those with a TF > 1 can phytoextract metals from contaminated soils, comprising the two branches of phytoremediation. There have been reports of phytoremediation of Cr, Cu, Cd, Zn, As, Mn and Pb (Bala et al. 2011; Orlex 2007; Kumar et al. 2002; Oorts 2007; Gautam et al. 2016; Sainger et al. 2011; Yang et al. 2014; Aboughalma et al. 2008), but studies of in situ tolerance and bioaccumulation of V are lacking. Native plant species are preferable for phytoremediation because of their advantages of not disrupting the ecosystem and high bioaccumulation/ translocation efficiency. In this study, eight dominant native plant species found on sites adjacent to V mine tailings without any obvious metal toxicities (i.e. chlorosis) were chosen to investigate the in situ metal (V, Cr, Cu, Zn) tolerance, bioaccumulation and translocation efficiency of these plants, as well as the effects of soil properties on metal uptake.

Material and methods

Site description

The sampling sites are located in southeastern Yunxi County, Shiyan City, Hubei Province, China (latitude 32°58′, longitude 110°26′), which has a mean annual temperature of 16 °C and an average precipitation of 820 mm. This area is classified as having a northern subtropical continental monsoon climate. This county is rich in natural resources such as fossil fuels and minerals and especially rich in V. This study was conducted in a V mine tailing field that consists of a flat area containing powdered or ball-shaped roasted stone coal slag, produced from roasting and leaching raw stone coal, that was discarded and flattened, as well as hills contaminated by leachate from tailings. No plants grow on the flat area because it lacks soil, but various plant species are found in the margins of the flat area and on hills severely polluted with V, Cr and Cu.

Soil analysis

Soil samples (0–20-cm depth) were collected from six sites in May 2016. At each site, five subsamples were collected and combined into a composite sample; One kilogram of this composite sample was transported to the laboratory, dried naturally and passed through a 5-mm mesh filter in preparation for analysis. The chemical characteristics of the soils from the six sampling sites are listed in Table 1.

Table 1 Chemical characteristics of the soils (mean ± SD) from the six study sites
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Soil pH was measured in a soil–H2O suspension (1:5, w/w) using a 716 DMS Titrino pH meter (Thermo Scientific, Origon Star A214, USA) fitted with a glass electrode. Organic matter was measured by the Walkley-Black titration method (Walkley et al. 1934; Baker 1936). The cation exchange capacity (CEC) was analysed by leaching with NH4OAc at pH 7, followed by distillation (Rayment and Higginson 1992). Available P was extracted using the Bray II method (Bray and Kurtz 1945), and available K was extracted using a fresh sample-to-extractant ratio of 1:5 (w/v) in 1 M NH4OAc at pH 7, which was shaken for 1 h on a reciprocating shaker at 250 rev min −1 (Helmeke and Sparks 1996) and then analysed using a flame photometer. Total N was measured using the Kjeldhal method (George Estefan et al. 2013).

Total metals were measured in 0.5 g soil, collected in triplicate from each sample after microwave digestion (CEM MARs5, USA) using 10 ml sulfuric acid, 30 ml nitric acid and 10 ml 10% hydrogen peroxide. Total metal concentrations were determined using an inductively coupled plasma emission spectrometer (Thermo Scientific iCAP 7000 series).

Plant analysis

Plant samples were collected in August 2016 from the same sites as the soil samples. Only the most abundant species at each site were collected: Chenopodium album from site 1, Daucus carota and Rorippa indica from site 2, Cirsium setosum and Kochia scoparia from site 3 and Eleusine indica (L.) Gaertn., Setaria viridis and Scutellaria sessilifolia Hemsl. from sites 4, 5 and 6, respectively. For each sample, three to five individual plants were collected randomly from each selected site. All plants appeared healthy with root systems in good condition and no leaf chlorosis. Species identification was performed at the Institute of Botany, Chinese Academy of Sciences, according to the Plant Photo Bank of China. Fresh plant material was washed thoroughly with tap water, cleaned with distilled water and then separated into roots and shoots. All plant parts were oven dried at 72 °C for 72 h and then ground into powder using a hammer mill. The total metal concentrations were measured using a similar method, procedure and instruments as those used to measure the total soil metal concentrations.

Statistical analysis

BAF, a measure of the ability of a plant to take up and transport metals to its shoots, is calculated using the formula proposed by Caille et al. (2005). The TF is calculated according to the formula of Zu et al. (2005):

$$ TF=\frac{Metal contents in shoot tissue}{metal contents in root tissue} $$
(1)
$$ BAF=\frac{Metal contents in root tissue}{metal contents in soil} $$
(2)

Data obtained from triplicate observations are presented as means ± standard deviation (SD). The SPSS 20 and MS Excel 2016 programs were used for statistical analysis of the data. Pearson product moment correlation coefficients (r) were used to identify associations among the quantitative variables.

Results

Soil characteristics

The physicochemical properties of the soils from six sampling sites are presented in Table 1. Soil pH ranged from 8.1 to 9.1 (Table 1), thus all sampling sites had alkaline pH values, the soil pH at site 4 was significantly (p < 0.01) higher than the values observed at other sites. The organic matter content was relatively low, with the highest value observed at site 1. The CEC ranged from 7.6 to 21.9, with no significant difference (p > 0.05) among sites 1, 2, 5 and 6, while site 4 had the lowest value. Sites 1 and 2 had relatively high amounts of available P, site 4 had significantly greater (p < 0.01) available P relative to all other sites and site 6 the lowest amount. Soil available K amounts significantly varied (p < 0.01) among six sites, site 1 had the highest value. Total N contents at sites 2, 3, 4, 5 and 6 were significantly lower (p < 0.01) than the value observed at site 1; there were no significant differences (p > 0.05) among site 2 and site 3, site 3 and site 4 and site 5 and site 6, respectively.

Metal concentrations in the soil samples

Soil at the sampling sites was contaminated primarily by V, Cr and Cu, with relatively low concentrations of Zn also found. Total V concentrations in the investigated soils varied from 129.8 to 754.4 mg kg−1 (Table 1). According to the Chinese Soil Environmental Quality Standard for Agricultural Land (exposure draft; MEPPRC 2015), site 4 is classified as having heavy V pollution (750 mg kg−1), sites 3 and 5 as moderate V pollution (300 to < 450 mg kg−1) and sites 1 and 2 as mild pollution (150 to < 300 mg kg−1); the V concentration at site 6 was below the permissible limit (exposure draft; MEPPRC 2015), but higher than the background level (114 mg kg−1), could be considered as potential V pollution. Total Cr and Cu concentrations in the soils from the six sites ranged from 106.9 to 736.3 mg kg−1 and 43.4 to 212.7 mg kg−1 (Table 1), respectively. The Cr concentration surpassed the national standard (≥ 250 mg kg−1) at sites 3, 4 and 5, and Cu surpassed the national standard (≥ 100 mg kg−1) at sites 3 and 4, the Cr and Cu contents at all sites were higher than the background level, existing a potential Cr and Cu contamination.

The total Zn concentrations in the soil samples ranged from 43.2 to 212.7 mg kg−1 (Table 1), which did not reach the pollution threshold of 300 mg kg−1 (soil pH > 7.5), but soil Zn contents at all sites, except site 2 and site 6, were exceeded background level. Taking the metal concentrations from all sites into consideration, site 4 had the highest V, Cr, Cu and Zn concentrations, which can be ascribed to the proximity of site 6 to V mine tailings. Pearson correlation coefficients (r) were used to assess the correlations of metal concentrations among the six sites. Total metal concentrations in soil samples collected from the six sites were significantly correlated (V vs. Cr, r = 0.99, p < 0.01, N = 6; V vs. Cu, r = 0.97, p < 0.01, N = 6; V vs. Zn, r = 0.97, p < 0.01, N = 6; Cr vs. Cu, r = 0.95, p < 0.01, N = 6; Cr vs. Zn, r = 0.96, p < 0.01, N = 6; and Cu vs. Zn, r = 0.99, p < 0.01, N = 6), indicating that the four metals measured in soils from six sites all were derived from a similar pollution source.

Metal concentrations in plants

Metal concentrations in shoots and roots of the investigated plants were highly variable. Total V concentrations in roots ranged from 18.9 to 1454.7 mg kg−1 (Fig. 1), and those in shoots ranged from 20.4 to 1208.3 mg kg−1 (Fig. 1). The highest V concentrations were found in the roots of K. scoparia and in the shoots of S. viridis (Fig. 1), the accumulation amounts equal to about 4.8 and 3.2 folds of soil V contents, respectively. The roots of C. album and S. viridis and the roots and shoots of E. indica (L.) also accumulated significant amounts of V (Fig. 1). The C. setosum and K. scoparia were growing up in site 3 with same soil metal contents and soil properties; there was no significant difference (p > 0.05) of V concentrations in shoots between two plants, but K. scoparia accumulated significantly higher (p < 0.01) amount of V in its roots compared to C. setosum, indicating that K. scoparia has greater potentials to remediate V-contaminated soils than C. setosum. Soil V concentrations at site 3 was significantly higher (p < 0.05) than the values at site 1, site 2 and site 6, respectively; there were no obvious differences (p > 0.05) of soil pH and CEC among these three sites; V accumulation amounts in the roots of K. scoparia were conspicuously higher (p < 0.01) than the V contents in the roots of C. album, D. carota, R. indica and C. setosum; soil V levels in site 4 and site 5 were significantly higher (p < 0.01) than the ones in other sites; V concentrations in the shoots of E. indica and S. viridis were apparently higher (p < 0.01) than the V contents in the shoots of all other plants, demonstrating that V accumulation amounts and distribution patterns in the roots and shoots were very plant specific.

Fig. 1
figure 1

Vanadium accumulation (mean ± SD) in native plant species from six sites contaminated with mine tailings. The different lower case letters at the top of error bars represent statistical difference at a level of p < 0.05; the different upper case letters at the top of error bars represent statistical difference at a level of p < 0.01(one-way analysis of variance, Tukey’s test); bars with the same letter do not differ significantly (p > 0.05). For example, there were no significant differences (p > 0.05) of V accumulations in the shoots of C. album, D. carota, C. setosum and K. scoparia which followed by (ab) and with respect to V concentrations in the shoots of R. indica followed by (b) and S. sessilifolia followed by (a); but V content in the shoots of R. indica followed by (b) was significantly higher (p < 0.05) than the one in the shoots of S. sessilifolia followed by (a); V accumulation in the shoots of S. viridis followed by (D) was significantly higher (p < 0.01) than the accumulation in the shoots of all other plants followed by lower case letters (a, b and ab) and upper case letter (B)

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The distributions of Cr in shoots and roots of all investigated plants, except D. carota, showed similar patters to V accumulations in plants. The Cr concentrations in the shoots and roots of investigated plants were also highly variable; they are ranged from 30.9 to 862.9 mg kg−1 and 7.7 to 261.2 mg kg−1, respectively (Fig. 2). The highest Cr concentrations were found in the roots of E. indica and in the shoots of S. viridis, no plants accumulated Cr higher than 1000 mg kg−1 in their shoots or roots. The Cr accumulation amounts in the shoots of E. indica, S. viridis, R. indica and in the roots of K. scoparia were higher than soil Cr contents. Except R. indica, other three plants were naturally growing in the most polluted sites, especially the E. indica, showing that these plant species have strong tolerance to Cr phytotoxicity and high Cr bioaccumulation efficiency.

Fig. 2
figure 2

Chromium accumulation (mean ± SD) in native plant species from six sites contaminated with mine tailings. The different lower case letters at the top of error bars represent statistical difference at a level of p < 0.05; the different upper case letters at the top of error bars represent statistical difference at a level of p < 0.01; bars with the same letter do not differ significantly (p > 0.05)

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The Zn concentrations in the shoots of all plant species, except S. sessilifolia, were higher than soil Zn contents; the highest Zn concentrations were found in the shoots and roots of D. carota, the values, ranging from 227.6 to 936.3 mg kg−1 (Fig. 3), equals to about 12 folds and 3 folds of soil Zn levels, respectively. The soil characteristics (Table 1) and soil Zn concentrations (Table 2) of site 3 and site 4 where K. scoparia and E. indica were growing were varied significantly, but no evident differences were found between Zn contents in the shoots of these two plants, D. carota and R. indica; C. setosum and K. scoparia were growing up in same sites with similar soil characteristics and soil Zn concentrations, respectively, but significant differences of Zn concentrations in the shoots of these plants were observed manifesting that varieties of species were the main factor affecting plant bioaccumulations of Zn in V mining area. In this study, all investigated plants accumulated higher amounts of Zn in their shoots than in their roots; this may be ascribed to the special property of Zn which is being an essential element for numerous biochemical and enzymatic reactions in plants, so Zn is considered to have high tendency to translocate to the active organs or tissues of plants; furthermore, soil Zn levels in all studying areas did not exceed permissible limits to cause pollutions.

Fig. 3
figure 3

Zinc accumulation (mean ± SD) in native plant species from six sites contaminated with mine tailings. The different lower case letters at the top of error bars represent statistical difference at a level of p < 0.05; the different upper case letters at the top of error bars represent statistical difference at a level of p < 0.01; bars with the same letter do not differ significantly (p > 0.05)

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Table 2 Soil metal concentrations (mean ± SD) of investigated sites
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Setaria viridis exhibited the highest amount of Cu in its shoots and roots (Fig. 4); the K. scoparia and E. indica also concentrated relatively high amount of Cu their roots and shoots, the accumulation amounts were higher than soil Cu content, while the lowest Cu concentrations were observed in the shoots of S. sessilifolia and the roots of C. setosum. In general, S. viridis presented high accumulation amounts in its shoots and roots for all investigated toxic metals, especially showed the highest accumulation efficiencies in its shoots for V, Cr and Cu. The E. indica also showed strong tolerance and high shoot accumulations for V, Cr, Cu and Zn, while K. scoparia exhibited high root accumulations of these toxic metals.

Fig. 4
figure 4

Copper accumulation (mean ± SD) in native plant species from six sites contaminated with mine tailings. The different lower case letters at the top of error bars represent statistical difference at a level of p < 0.05; the different upper case letters at the top of error bars represent statistical difference at a level of p < 0.01; bars with the same letter do not differ significantly (p > 0.05)

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Metal bioaccumulation and translocation by native plants

The efficiencies of metal uptake from soil by plant species, metal accumulation in plants and metal movement from roots to shoots can be estimated using the BAF and TF, respectively.

BAF values > 1 indicate that a plant is efficient at accumulating and taking up metals from the soil, while BAF values < 1 indicate that plants are metal excluders (Yanqun et al. 2005). Plants with both BAF and TF values > 1 may be suitable candidates for hyperaccumulation of metals, while plants with TF values < 1 can phytostabilise metals in roots (Yoon et al. 2006). The BAF and TF values of all plant species are shown in Figs. 5 and 6, respectively. Among eight plant species, only C. album (Fig. 5) had BAF > 1 for V. Furthermore, S. sessilifolia and K. scoparia showed relatively high BAF of 0.97 and 0.81 for V, respectively. Among these three plant species, C. album was growing up in moderately V polluted soils, and also showed BAF of 0.97 and 1.8 for Cr and Zn, respectively, indicating that C. album has great potentials to phytostabilise V, Cr and Zn multi-metal-contaminated soils. Scutellaria sessilifolia had BAF > 1 for Cr, Zn and Cu, and showed the highest BAF for Cr and Cu; this may be the reason of S. sessilifolia growing up in the least polluted soils in this study. Setaria viridis showed relatively low BAF for V, Cr and Zn, but exhibited BAF > 1 for Cu. In addition, C. album and S. sessilifolia, D. carota and R. indica also had BAF > 1 for Zn. However, these plants were growing up in potential Zn polluted soils (i.e. below than national standard); the BAFs in Zn-contaminated soils need to further study.

Fig. 5
figure 5

The bioaccumulation factors of all plant species collected from contaminated soils

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Fig. 6
figure 6

The translocation factors of all plant species collected from contaminated soils

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The only TF > 1 for V was found in S. viridis (Fig. 6); in addition to this, S. viridis had TF > 1 for Cr and Zn. All investigated plants exhibited high root to shoot translocation efficiencies for Zn; among them, C. setosum and K.scoparia had TF > 1 for Zn. Besides, C. setosum also showed TF > 1 for Cr. Daucus carota, R. indica, C. setosum and S. viridis showed high TF for Cu; among them, D. carota was the only plant species that had TF > 1 for Cu.

In this study, no single plant had both BAF and TF values > 1 for V concurrently, but S. viridis accumulated high concentrations of V, Cr, Cu and Zn in its roots and shoots, the V accumulation amounts in its shoots were over 1200 mg kg−1. In addition, the TFs for V, Cr and Zn were > 1, BAF > 1 for Cu, and also showed relatively high root to shoot translocations of Cu without chlorosis or necrosis, showing that S. viridis has strong resistance to multi-metal pollution (i.e. V, Cr, Zn and Cu) and high multi-metal bioaccumulation efficiencies. Setaria viridis was grown in moderately V polluted and slightly Cr- and Cu-contaminated soils, demonstrating that S. viridis was practical for phytoextractions of V and Cr, and phytostablising of Cu in multi-metal-contaminated soils in V mining area. Cirsium setosum could be used to phytoextract V and Cr from moderately V and slightly Cr polluted soils, respectively. Although D. carota had TF > 1 for Cu, it was growing up in potentially polluted soils; its practicability in Cu-contaminated soils was unclear.

Discussion

Soil properties and metal concentrations

Plants in metal-enriched soil take up metal ions to varying degrees; this uptake is highly plant specific and largely influenced by metal bioavailability (Deng et al. 2004). Soil pH, CEC, organic matter and nutrient contents were the most influential parameters affecting the mobility and bioavailability of metals (Sainger et al. 2011). The present study showed that all sampling sites had alkaline soil, and the most polluted site (site 4) exhibited the highest pH value, which may be attributed to its proximity to mine tailings.

According to the Chinese national standards, V levels at sites 1–5, Cr levels at sites 3, 4 and 5 and Cu levels at sites 1, 3, 4 and 5 exceeded the permissible limits (with soil pH > 7.5) of 150, 250 and 100 mg kg−1, respectively, while no Zn concentrations surpassed the permissible limit. Soil collected from site 4 had the highest metal (V, Cr, Cu, Zn) concentrations, but plants at this site did not exhibit the greatest metal concentrations in roots and shoots; this could be an effect of the high soil pH, which decreased metal bioavailability or affected root uptake of metals (Brown et al. 1995), or could be attributed to differences among plant species and phytotoxicity of high metal concentrations.

Results of Pearson correlation analysis (data not shown) indicated that the investigated metals in soils were negatively correlated with soil CEC. This could be ascribed to the low plant diversity at the highly polluted sites, which leads to low contents of organic matter and humic substances, resulting in smaller soil aggregates (Bian et al. 2014) and fewer metal adsorption sites. Some reports have shown that increased CEC can enhance heavy metal precipitations and complexations (Gu et al. 2011; Chen et al. 2000); decreased toxic metal bioavailability, consequently reduced metal accumulation in plant tissues, but in this study, soil CEC has no significant effect on plant metal accumulation; this may be ascribed to low soil CEC in investigated soils.

Available P and metal concentrations in soil were significantly correlated with each other (p < 0.05, n = 6), indicating that the available P and toxic metals in these soils originated from the same source. There were poor correlations of other measured parameters with soil metal concentrations. E. indica was growing up in the most polluted site, but the V, Cr and Cu accumulation amounts in the roots and shoots of E. indica were higher than metal concentrations in the shoots and roots of C. setosum, R. indica and C. album; this may be reason of high available P contents which reduced metal availability and toxicity through precipitation (Bolan et al. 2014; Nawab et al. 2016), ensured normal growing of plants, consequently enhanced relative accumulation of toxic metals with plant biomass.

Higher soil OM contents determine more metal sorption sites and more metal chelators and reduced the concentrations of extractable metal (Clemente et al. 2007; Venegas et al. 2016), but in our study, all investigated soil showed very low contents of soil OM, had no significant effect on toxic metal accumulations in plant tissues. Daucus carota and R. indica, C. setosum and K. scoparia were growing up in same sites, respectively. These sites showed similar soil pH, soil OM and soil metal contents. No obvious difference (p > 0.05) of V accumulations in the shoots (Fig. 1) of D. carota and R. indica, C. setosum and K. scoparia were found, respectively. However, V accumulations in the roots (Fig. 1) of these plant differed significantly (p < 0.01). In addition, there were noticeable differences of Cr, Zn and Cu accumulations in the roots of D. carota and R. indica, C. setosum and K. scoparia, respectively. These results indicating that soil pH and soil OM made little difference in toxic metal accumulations of these plants in V mining area, the results were in line with the findings of Qian et al. (2014); this may be the reason of low OM in sampling sites, which determines low soil microbial activity and less organic chelators, control the release of metal from different soil fractions and strongly affect toxic metal speciation and absorption by plants (Violante et al. 2010). In alkaline soil, in addition to soil pH, soil carbonate also played important role for sequestering toxic metals (Ramos et al. 2007); it has been reported that Ca2+ can reduce toxic metal bioavailability and toxicity (Bolan et al. 2003); as a result, decreased harmful effects on plant roots while growing in soil contained high toxic metal contents, ensured normal growing of plants and enhanced relative metal accumulations with the increasing of plant biomass. The E. indica and S. viridis showed the highest Cr accumulations, in spite of growing in the most contaminated soils; this may be caused by the toxicity abatement effects of high soil pH, soil carbonate (pH > 8) and soil P in studying area.

Metal accumulation and tolerance in native plant species

As shown in Table 1, the eight species investigated in the present study were capable of growing in soils varying widely in their V, Cr, Zn and Cu concentrations at sampling sites contaminated with V, Cr and Cu levels exceeding the Chinese national standards.

To our knowledge, there have been no prior reports of in situ V tolerance in these plant species. Plant biomass, root length and leaf chlorophyll content all exhibit highly sensitive responses to metal stress. Previous studies conducted in soybean (Wang and Liu 1992), rice (Gu et al. 2011), green mustard (Vachirapatama et al. 2011) and onion plants (Marcano et al. 2006) found that > 30 mg/kg V in the soil matrix led to severe toxicological effects and significant biomass loss. Alan et al. (2005) also reported that high levels of V lead to leaf chlorotic symptoms in Cuphea. In this study, all plant species except S. sessilifolia tolerated V concentrations higher than the permissible limit, and E. indica grew in soil contaminated with 754.4 mg/kg V without chlorosis, suggesting that it is the most V-tolerant of the eight species investigated.

Few studies have investigated V accumulation in native plants. In general, plants do not accumulate or bioconcentrate non-essential metals. In this study, the V accumulation amounts in the roots of C. album, D. carota, K. scoparia and S. sessilifolia were higher than V contents in their shoots, corroborating the findings of Vachirapatama et al. (2011), Martin and Kaplan (1998) and Chongkid et al. (2007). On the other hand, R. indica, C. setosum, E. indica and S. viridis had higher V concentrations in their shoots than in their roots, even though these plants were growing up in the most V polluted sites. The wide variation in V concentration in the plant tissues (Fig. 1) indicates that uptake and translocation is the result of complex interaction of chemical, biological and physical factors (Ehlken and Kirchner 2002). In other words, these processes can be different between various plant species and same plant species with different biomass, which were growing in soils contained similar amount of toxic metals and similar soil characteristics. In this study, S. viridis accumulated 1208.28 mg/kg V in its shoots, accounting for 2.03% of the shoot dry weight, and thus it may be a strong V phytoextractor candidate. D. carota, R. indica, C. setosum and K. scoparia were collected from the same sampling sites but showed very different accumulation strategies, indicating that accumulation of V is plant specific; this may be ascribed to the difference in aerial biomass of these plants, which can dilute the concentration of V in aerial tissue and protect the plant from the toxic effect caused by high V concentration (Pulford and Watson 2003). Among these species, K. scoparia concentrated 1454.73 mg/kg V in its roots, which was 4.02% of its root dry weight. From the viewpoint of V ecotoxicity, K. scoparia may be useful as a V hyperaccumulator to prevent V from entering the human food chain.

Kabata-Pendias and Pendias(1992) reported typical Cr, Cu and Zn contents of 0.2–8.4, 0.1–3.7 and 1–160 mg kg−1, respectively, in terrestrial plants growing in uncontaminated soils, while the concentration ranges considered toxic to plants are 10–50 mg kg−1 for Cr (Lepp 1981), 60–125 mg kg−1 for Cu and 70–400 mg kg−1 for Zn (Kabata-Pendias and Pendias 1992). Our results showed that the Cr, Cu and Zn concentrations in the plants species evaluated were approximately 3–20-, 1–4- and 1–3-fold higher than those that cause toxicity in normal plants, indicating that these native species have strong tolerances to Cr, Cu and Zn.

Cr exhibited a similar distribution pattern to that of V in the roots and shoots of the examined plants (Fig. 3). Five plant species had high Cr translocation efficiencies and accumulated significant levels of Cr in their shoots. S. viridis had the highest Cr concentrations in its shoots, accounting for 1.46% of the shoot dry mass, similar to the results of Rafati et al. (2011), Rezvani et al. (2011), Vwioko et al. (2006), Atayese et al. (2009) and Liu et al. (2008). This may be attributed to inefficient immobilisation of toxic metals by the roots of these plants, resulting in their efficient translocation and accumulation to aerial parts. Plants grown at the most polluted sites exhibited increased Cr levels in their shoots compared to their roots and high biomass, which could represent a strategy for metal toxicity reduction, by which these plants take up harmful metals to non-photosynthetically active organs such as shoots to diminish metal toxicity in roots by biomass diffusion. Banks et al. (2006), Orlex (2007) and Shanker et al. (2005) also found that roots accumulate greater Cr concentrations than those of shoots, indicating that Cr accumulation patterns in plants were highly variable and plant specific.

Zn is an essential element for plants, is found in nearly 100 specific enzymes and is the only metal represented in all six enzyme classes (Webb 1992); Zn is an indispensable metal for the active centres of superoxide dismutase (SOD), an antioxidant enzyme which attends reducing metal toxicity; this may be the reason for the higher Zn concentrations in shoots than in roots in all investigated plants (Fig. 4). This result is in accordance with the findings of Baker et al. (1994), Kashem et al. (2010) and Qiu et al. (2006).

The highest Zn accumulations were found in the shoots of D. carota and R. indica, this may be ascribed to the lower soil Zn contents (i.e. significantly lower than all sites except site 6) which determine lower metal toxicity compared to plants grown in other sites. D. carota and R. indica, C. setosum and K. scoparia were growing up in same sites, respectively, but Zn accumulations in their shoots and roots differed significantly; in addition to this, S. sessilifolia was grown in the least polluted sites, but also accumulated the least amount of Zn in its shoots and roots, showing metal accumulations and distributions were very plant specific.

Cu is also essential for plant growth, but excess levels can cause toxic effects. Among all plants, S. viridis had the highest Cu concentrations of 967.97 mg kg−1 in shoots and 315.09 mg kg−1 in roots, while S. sessilifolia, with a BAF of 6.48, exhibited strong Cu tolerance and high accumulation efficiency. Marschner (1995), Nissen and Lepp (1997), and Khan (2001) found that Cu was not actively transported to aboveground tissues due to storage in roots, which was not in accordance with our finding that most plants had higher Cu concentrations in their shoots. This may be due to plant and matrix differences between these studies, confirming that metal tolerance and accumulation patterns of plants were highly variable and dependent upon species and matrix.

BAF and TF

Among the eight plant species investigated, S. viridis exhibited TF values > 1 for all of the main pollutants (V, Cr and Zn). The V concentrations in shoots exceeded 1000 mg kg−1. The BAF and TF values for Cu were 1.157 and 0.93, respectively, suggesting that this species has potential use as V and Cu hyperaccumulator and a multi-metal phytoextractor (Qian et al. 2014), which is an environmentally friendly, cost-effective tool for cleaning soils polluted with multiple metals in V mining areas.

S. sessilifolia had BAF values of 1.57, 0.97, 1.80 and 0.65, and C. album had BAF values of 0.97, 2.66, 1.02 and 6.49 for V, Cr, Zn and Cu, respectively, perhaps due to their deep-root systems and high-root biomass reported by Baker and Whiting (2002). These species can thus be categorised as good accumulators of the investigated metals, and could be co-cropped with human food plants in soils polluted with multiple metals to avoid or reduce the metal amounts entering human food directly or indirectly.

Kochia scoparia accumulated relatively high amounts of Cr, Cu and the highest amount of V in its roots; furthermore, it had TF > 1 for Zn and could be used as a potential candidate for phytoremediation of multi-metals in V mining area. Daucus carota also showed TF > 1 for Cu and BAF > 1 for Zn, and could be use as phytoextractor of Cu and phytostabliser of Zn in V mining area.

Conclusion

Six sites in V mining areas contaminated primarily with V, Cr, Cu and Zn were investigated. The concentrations of toxic metals in soils and plants varied among the sites and plants and generally exceeded the normal ranges. Among the eight species evaluated, only S. viridis and K. scoparia accumulated more than 1000 mg kg−1 V in their shoots and roots, respectively. S. viridis had a TF > 1 for V and also accumulated high concentrations of Cr, Cu and Zn in its shoots; therefore, it could be considered a hyperaccumulator. Although not all plant species met the standards for hyperaccumulators, they all concentrated significant levels of toxic metals in their tissues and exhibited high BAF and TF values. The present study identified some plant species as suitable candidates for phytoextraction and phytostabilisation of toxic metal pollution caused by V mining, providing reference for revegetation, for erosion control, and in situ phytoremediation of V mining area. Evaluation of the effect of different soil V, Cr, Cu and Zn contents and soil properties on toxic metal accumulations and phytoremediation potentials of S. viridis, K. scoparia, D. carota and E. indica will be the continuation of this study.