1. Introduction
Heavy metal pollution has become a worldwide environmental concern because of its latency, toxicity, and contamination within soils over time [
1]. Heavy metal pollution is generally considered to result from anthropogenic activities, such as mining, mineral fertilizers, vehicle exhaust, and other industrial activities [
2,
3]. Industrial activities are regarded as the principal contributor for heavy metal pollution [
4]. With the rapid industrialization and urbanization of China over the last decades, various industrial activities have contributed a large amount of heavy metals to the soil, directly and indirectly [
5]. The urban soil around electronics manufacturing has been subject to multiple heavy metal contaminations in the Hebei province of China [
6]. Wastewater from unregulated manufacturers is the primary heavy metal contributor in urban river systems [
7]. It has been found that about 50% of the soil samples are contaminated by heavy metals in the gold-mining region of Shanxi province, China [
8]. Heavy metal exposure in ecosystems can endanger both animals and plants, and harm human health via the food chain [
9,
10,
11]. Long-term exposure to heavy metals has been associated with problems such as hearing loss, intellectual disabilities, nervous system dysfunction, behavioral problems, and various cancers. Furthermore, exposure to multiple heavy metals may induce more severe diseases such as immune system damage, skin cancer, skeletal damage, vascular disease, and so on [
12,
13].
Over the past decade, in order to reduce the heavy metal risks to human health, the remediation of heavy metal contaminated soils has been a worldwide environmental goal. Various technologies (surfication, landfilling, soil flushing, electro kinetic, extraction, phytoremediation, bioremediation, etc.) have been applied to remediate heavy metal contaminated soils. However, most of these techniques are costly and may cause secondary pollution [
14]. Phytoremediation is a promising method for the removal of heavy metals from contaminated soils, which is considered a low-cost, effective, and environmental friendly approach for remediation, and has been widely adopted over the world [
15]. In general, phytoremediation is classified into several subcategories, namely: phytostabilization, phytoextraction, phytovolatilization, phytodegradation, and so on. Phytostabilization minimizes or restricts the movement of pollutants by plants, phytoextraction relies on plants to absorb soil heavy metals, phytovolatilization removes volatile pollutants or metabolites using plants, and phytodegradation degrades organic pollutants by inducing the metabolic activities of plant root microbes [
16]. Although in the future, the genetic engineering of plants may help improving phytoremediation [
17], presently, there is an urgent demand to select promising species from native plants [
18,
19,
20]. The use of native plants is a valuable option, because these plants are better adapted to the regional multi-stressful environment than the introduced ones [
21,
22]. Previous studies also reported that heavy metal accumulators were usually found in metal-contaminated environments [
23,
24]. Therefore, it could be an effective way to assess the phytoremediation potential of native plants in a metal-contaminated environment.
With the implementation of China’s Western Development Policy, more industrial areas have improved their economies in the northwest. However, the soil quality has been severely deteriorated, especially because of the heavy metal soil pollution. Most industrial parks have been built on the edges of rivers to have better access to water resources, thus causing severe heavy metal pollution in rivers, because of surface runoff and the mobility of heavy metal in soils [
25]. As one of the fastest-growing cities with an industrial economy, Shizhuishan, located in northwestern Ningxia, China, is considered as a typical city that has exhausted coal as a resource. The leading industries include mining, smelting, electroplating, energy, chemical, fuel production, and power transmission. Despite the economic development generated from these industries, it is well known that these industries can lead to serious heavy metal contamination by discharging waste residue into soils and waste water into the river. Wang et al. [
26] found that the soil heavy metal pollution in the industrial area of Ningxia is the most serious in different functional zones. A previous study by Zhou et al. [
27] showed that the groundwater heavy metal pollution in Ningxia has been worsened by industry. Heavy metals dissolved in water are easily absorbed by organisms and can be bio-accumulated into the food chain. The long-term exposure to heavy metals for humans may affect growth, metabolism, reproduction, and even lead to various diseases. Therefore, it is urgent to find and evaluate the heavy metal pollution of surface soils in the Shizuishan industrial district. It is also necessary to further effectively remediate the heavy metal pollution by phytoremediation technology. Phytoremediation utilizes plants to clean the heavy metal contamination. Many plants have been reported to tolerate and accumulate heavy metals, and can be used to eliminate the heavy metal contamination in soils [
28,
29]. However, plants that grow in the arid zone of northwest China are subjected not only to heavy metals, but to saline conditions and sometimes drought 30. Heavy metal accumulators from introduced ones cannot survive in these multiple environmental stresses. Thus, it is the best option to use native plants for phytoremediation, as they grow well in the harsh environment. The main objectives of this study were (1) to assess heavy metal pollution through different methods and (2) to identify potential phytoremediator of Cd, Cr, As, Pb, and Cu for phytoremediation in this region.
3. Results
3.1. Heavy Metal Concentration in Soils
The descriptive statistics of six heavy metal contents in soils arre presented in
Table 3.
As a whole, the mean value of the six heavy metal contents in the soils followed a descending order of Zn > Cr > As > Pb > Cu > Cd. All of the metal concentrations were far higher than their background values in Ningxia. Relatively, they were 36.91, 1.67, 7.20, 1.38, 1.27, and 6.66 times that of the corresponding background values, respectively. Based on their background values [
41], the overall standard rate of six heavy metals were 90% higher, while Cd, As, and Zn were 100% higher. The coefficients of variation varied from 12.86% for Cr to 38.03% for Pb, and decreased in the order of Pb > Cd > Zn > As > Cu > Cr (
Table 3).
3.2. Pollution Assessment of Heavy Metals
The single factor pollution index and Nemerow synthetic pollution index for the six heavy metals that were measured are summarized in
Table 4.
The average single factor pollution index for the six heavy metals decreased in the order of Cd > As > Zn > Cr > Cu > Pb. The average single factor pollution index for Cd and As were greater than three, showing severe pollution. The values of Cd in all of the sampling sites ranged from 3.5 to 14.1, indicating serious contamination at all sites. The average single factor pollution index for Zn was between one and two, indicating that the study areas were slightly polluted by Zn. The maximum single factor pollution indices of Cr, Pb, and Cu in all of the samples were 0.40, 0.08, and 0.28, respectively. These values were lower than one, indicating that all of the samples were not polluted by Cr, Pb, and Cu. The average Nemerow synthetic pollution index in the industrial area was higher than three, which was serious pollution. On the whole, our data show that 97.78% of the samples were seriously polluted, and the rest were moderately polluted.
3.3. Relationship between Metal Levels in Soil and Plants
The correlation coefficients of the six heavy metals between the soils and plants are presented in
Table 5. For
Artemisia blepharolepis,
Suaeda salsa,
Mulgedium tataricum,
Leymus secalinus, and
Chloris virgata, the Cd content between the soils and plants showed a higher significant positive correlation.
Polygonum aviculare,
Amaranthus retroflexus,
Chenopodium glaucum,
Tribulus terrester,
Chenopodium album, and
Achnatherum splendens, their Cr content showed a higher significant positive correlation with corresponding soil, Cr. For
Halogeton arachnoideus,
Polygonum aviculare,
Bassia dasyphylla,
Suaeda salsa,
Salsola collina,
Mulgedium tataricum, and
Chloris virgata, the Pb content between the soils and plants showed a higher significant positive correlation. For
Halogeton arachnoideus,
Echinochloa crusgalli,
Amaranthus retroflexus,
Setaria viridis,
Artemisia scoparia,
Achnatherum splendens, and
Chloris virgata, the Cu content between the soils and plants showed a higher significant positive correlation. For
Halogeton arachnoideus,
Polygonum aviculare,
Tribulus terrester, and
Kochia scoparia, the Zn content between the soils and plants showed a higher significant positive correlation at the 0.05 probability level.
3.4. Heavy Metal Concentration in Plants
The concentration of heavy metals in the different plant samples are given in
Table 6. For metal Cd,
Artemisia blepharolepis and
Leymus secalinus presented a higher accumulation, due to their higher biomass, than other plants. However, the Cd concentrations in the shoot and root of all of the studied plants were limited. The Cr concentrations in the shoots among the studied species had no significant differences. But
Achnatherum splendens presented a higher level of Cr in the root compared with the other plants (
p > 0.05).
Chloris virgata had a higher value of metal Pb in the root, but the low biomass limited the application in phytoremediation.
Halogeton arachnoideus and
Salsola collina showed a relatively higher biomass and Pb contents than the other plants. For Cu, the concentrations in the roots among the studied species showed no significant differences, and
Artemisia scoparia and
Echinochloa crusgalli had significantly higher concentrations in the shoots (
p > 0.05).
Tribulus terrester and
Halogeton arachnoideus showed higher levels of metal Zn in shoots and roots than other plants, but the biomass of
Tribulus terrester was lower than that of
Halogeton arachnoideus.
3.5. Bioconcentration and Translocation Factors in Native Plants
The ANOVA results showed that the bioconcentration factor and translocation factor were significantly different in different plants; the Duncan’s test results are shown in
Figure 2 by capital and small letters.
The bioconcentration factors of Cd in the order of Leymus secalinus > Suaeda salsa > Artemisia blepharolepis > Chloris virgata > Mulgedium tataricum, and the top three species, were not significantly different at the 0.05 probability level. The translocation factors of Suaeda salsa and Leymus secalinus had the same significance (p < 0.05), but Suaeda salsa was the highest. In the studied plants for Cr, the bioconcentration factors were lower than one. Achnatherum splendens, Tribulus terrester, and Chenopodium glaucum were relatively higher than the other plants, and they were not significantly different at the 0.05 probability level. The translocation factors of Cr were in the order of Amaranthus retroflexus > Tribulus terrester > Polygonum aviculare > Chenopodium glaucum > Achnatherum splendens > Chenopodium album, and the top four species were not significant at the 0.05 probability level. For Pb, the bioconcentration factors of all of the samples were far lower than one, and they were relatively stable, ranging from 0 to 0.1. These values were not significant at the 0.05 probability level. The translocation factor of Bassia dasyphylla was significantly higher than other plants. The bioconcentration factors of Cu were lower than one in the studied species. The values of Artemisia scoparia and Echinochloa crusgalli were relatively higher than other plants, but they were not significant at the 0.05 probability level. The translocation factor of Artemisia scoparia was significantly higher than the other plants. For Zn, the bioconcentration factor of Tribulus terrester was the highest, closely followed by Halogeton arachnoideus, however, they were not significantly different at the 0.05 probability level. The translocation factors for all of the samples of Zn were not significantly different, and the highest was Halogeton arachnoideus.
4. Discussion
Most studies used soil samples to monitor the environmental metal levels [
42]. This study found that the mean values of Cd, Cr, As, Pb, Cu, and Zn in soils were 36.91, 1.67, 7.20, 1.38, 1.27, and 6.66 times that of the corresponding background values, respectively. Based on their background values, the overall standard rate of the six heavy metals were higher than 90%, of which Cd, As, and Zn were 100% (
Table 3). These results indicate that all of the six heavy metal contents were relatively high in the study area and almost all of the study area was contaminated by exogenous pollutants. The CV values were used for the description of global variability [
43]. Large CV values indicate a considerable spatial variation and imply a significant input from external sources [
44]. A low CV suggests that the nonpoint input is predominant [
45]. The coefficients of variation varied from 12.86% for Cr to 38.03% for Pb, and decreased in the order of Pb > Cd > Zn > As > Cu > Cr (
Table 3), which suggested that there was a moderate degree of spatial variability of the six heavy metals, and the anthropogenic factors significantly influenced the distribution of Pb and Cd.
The heavy metal of the soil pollution status was evaluated by a single factor pollution index and the Nemerow synthetic pollution index (
Table 4). From the single factor pollution index, the Cd and As were found to be the most serious pollutants in the industrial area, especially Cd, as all of the samples were seriously contaminated. The study area was slightly polluted by Zn. Areas were relatively clean of Cr, Pb, and Cu, and all of the samples were not polluted by Cr, Pb, and Cu. As a result of the complexity of the soil, the Nemerow synthetic pollution index was employed to evaluate the comprehensive impact caused by the six heavy metals in soil, rather than a single factor pollution index, which can only reveal the pollution level of one metal [
46]. According to the Nemerow synthetic pollution index, the industrial area was seriously polluted. As for the pollution level in every sampling site, the results showed that almost all of the samples in the industrial area were seriously polluted by anthropogenic sources. According to the Nemerow synthetic pollution index model, the high single factor pollution indices of Cd, As, and Zn are the main reasons for heavy metal pollution in this region.
Evaluating the phytoremediation potential of heavy metals in different plants should be utilized in the remediation of heavy metal contaminated soils. In general, it is regarded as a hyperaccumulator when the heavy metal concentrations, BCF, and TF for plants are up to corresponding standards [
47,
48,
49]. However, these nominal thresholds should not be regarded as the absolute cut-off when the phytoremediation potential is assessed. Plants that grow in the semi-arid and arid regions of northwest China are subjected not only to heavy metal contamination, but also to drought and saline stresses. Thus, many studied heavy metal hyeraccumulators, such as
Thlaspi caerulescens,
Pteris vittata,
Reynoutria sachalinensis, and so on, cannot survive and be used for phytoremediation in this region. Some similar studies for this region were conducted in the laboratory. For example,
Ligustrum obtusifolium was found to have a high capacity of Pb accumulation and translocation under drought stress [
50], and
Buddleja alternifolia had a great potential application in Cd phytoremediation of arid regions [
51]. However, these studies were conducted under controlled single heavy metal stresses, which could not reflect the hash and complex situation in situ. Thus, assessing the potential phytoremediators from native plants is necessary. Although the plants in this study are not hyperaccumulators for heavy metals, their phytoremediation potential is still valuable.
As a whole, the bioconcentration factors of five heavy metals in all of the studied species were lower than one, and presented lower levels in the shoot and root than the accumulator, but they had a stronger tolerance under the regional multi-stressful environment. Some plants with a high biomass would share a high resultant capability for phytoremediation. Based on the comprehensive consideration of heavy metal concentrations, BCF, and TF for native plants, we thought Achnatherum splendens for metal Cr presented a phytostabilization potential. It grew very well and was abundant in this study area, and had the highest BCF; what is more, the metal Cr was less distributed in the shoot than in the root. As a result of their higher shoot content and BCF in the metal Cu and Zn than other plants (p < 0.05), and the ability to tolerate the regional multi-stressful environment, Artemisia scoparia and Echinochloa crusgalli for metal Cu and Halogeton arachnoideus for metal Zn could be considered as the most promising species for phytoextraction. Almost all of the selected plants were perennials and had a higher important value, which also contributes to enhanced uptake of metal. Although the TF of some plants in metal Cd and Pb was higher than one, all of the studied species presented a low shoot content and BCF, and had no significant differences. Thus, all of the studied plants were limited as phytoremediators for Cd or Pb contaminated soil. Further research should be done in a wider region.
5. Conclusions
The discharge of heavy metals through various industrial activities is an important cause of soil contamination by heavy metals. As the study area has experienced rapid urbanization and industrialization over the past decades, the problem of heavy metal contamination has also become increasingly prominent. The results suggest that the study area was seriously polluted by Cd and As, slightly polluted by Zn, and was relatively clean for Cr, Pb, and Cu contamination. In addition, almost all of the samples in the study area were seriously polluted. The heavy metal remediation of industrial zones should be an important concern; therefore, strategies should be implemented to ban the discharging or dumping of unqualified industrial waste.
In order to reduce heavy metal risks to the human health of local residents, phytoremediation, a natural, esthetically pleasing, and low-cost technology, has opened a new avenue in the remediation of heavy metal contamination soil. The phytoremediators should adapt to heavy metal contamination, drought, and saline stresses in arid and semi-arid land of northwest China. Our results suggest that because of its low shoot content in metal Cr, BCF was the highest compared with other plants, and its ability to tolerate a regional multi-stressful environment, Achnatherum splendens for metal Cr presented phytostabilization potential. And, because of its higher shoot content and BCF, and its ability to tolerate a regional multi-stressful environment, Artemisia scoparia and Echinochloa crusgalli for metal Cu and Halogeton arachnoideus for metal Zn presented a phytoextraction potential. And, as a result of its low shoot and root content and BCF, all of the studied plants were limited as phytoremediators for Cd or Pb contaminated soil.
More importantly, the phytoremediation areas should be fenced off from wildlife to prevent contamination of the food chain. The phytoremediation areas could be combusted as biofuel feedstock after harvesting, and the ashes could be recovered from the metals or concentrated landfilled. In addition, as important characteristic of phytoremediation, time-consuming should be noticed compared with other remediation techniques. More research is needed to obtain fast-growing hyperaccumulators though genetic techniques.