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Article

Potential of Cassia alata L. Coupled with Biochar for Heavy Metal Stabilization in Multi-Metal Mine Tailings

by
Lige Huang
1,
Yuanyuan Li
1,
Man Zhao
1,
Yuanqing Chao
1,2,3,
Rongliang Qiu
1,2,3,
Yanhua Yang
1,2 and
Shizhong Wang
1,2,3,*
1
School of Environmental Science and Engineering, Sun Yat-sen University, Guangzhou 510275, China
2
Guangdong Provincial Key Lab of Environmental Pollution Control and Remediation Technology, Guangzhou 510275, China
3
Guangdong Provincial Engineering Research Center for Heavy Metal Contaminated Soil Remediation, Guangzhou 510275, China
*
Author to whom correspondence should be addressed.
Int. J. Environ. Res. Public Health 2018, 15(3), 494; https://doi.org/10.3390/ijerph15030494
Submission received: 20 January 2018 / Revised: 13 February 2018 / Accepted: 23 February 2018 / Published: 12 March 2018
(This article belongs to the Special Issue Soil Pollution and Remediation)
Browse Figures
Versions Notes

Abstract

:
To explore the effect of different biochars on Cassia alata L. growth and heavy metal immobilization in multi-metal mine tailings, a 100-day pot experiment was conducted. Three biochars derived from Hibiscus cannabinus core (HB), sewage sludge (SB) and chicken manure (MB), were added to mine tailings at rates of 0.4%, 1% and 3% (w/w). The results showed that the root biomass, shoot biomass, plant height and root length were 1.2–2.8, 1.7–3.2, 1–1.5 and 1.6–3.3 times of those in the control group, respectively. Pb, Zn, Cu, Cd and As contents in the shoot decreased by 63.9–89.5%, 46.9–66.0%, 32.7–62.4%, 40.4–76.4% and 54.9–77.5%, respectively. The biochar significantly increased the pH and decreased the mild acid-soluble Pb and Cu concentrations in the mine tailings. Specifically, SB immobilized Pb and Cu better than MB and HB did, although it did not immobilize As, Zn or Cd. Meanwhile, more attention should be paid to the potential As release as the biochar application rate increases. In conclusion, Cassia alata L. coupled with 3% of SB could be an effective measure for restoring multi-metal mine tailings. This study herein provided a promising ecological restoration technique for future practice of heavy metal stabilization in mine tailings.

Graphical Abstract

1. Introduction

China possesses diversified and large-scale mineral resources, accounting for more than 12% of the world’s proven reserves of mineral resources in 2010 [1]. Moreover, there are many types of polymetallic minerals with multi-metal paragenetic metallic minerals, including Pb, Zn, Cu, Cd, and as [2]. With the steady development of excessive metal mining and processing activities, mining and ecological environmental issues are giving rise to growing concern from the community, particularly with respect to mine tailings. The major industrial solid waste comprehensive utilization of the 12th Five-Year Plan of China indicates that mining activities generated 1.21 × 108 tons of mine tailings, with less than 14% comprehensive utilization rate every year since 2010. Many tailings are still being dumped, forming tailing ponds. Mine tailings are the materials remaining after the extraction and beneficiation of ores, which contain an abundance of prominent toxic elements, such as Pb, Zn, Cu, Cd, and As [3]. These toxic elements can spread to surrounding areas through water erosion and wind erosion, which might cause water pollution and soil contamination and consequently pose risks to human health. Therefore, management and remediation of these mine tailings has become an important national issue concerning the national economy and people’s livelihood.
Phytostabilization is an effective and inexpensive rehabilitation strategy coupling metal-tolerant plants and mineral or organic soil amendments that help absorb and accumulate heavy metals in roots and promote precipitation within the rhizosphere [4], particularly for highly contaminated soils such as those containing mine tailings, which cannot be remediated by phytoextraction [5]. To date, phytostabilization research on multi-metal mine tailings is insufficient due to the extreme conditions posed by mine tailings, such as nutrient deficiencies, deficient inorganic matter and multi-metal toxicity. Thus, to provide an appropriate method for phytostabilization under such extreme mine tailing conditions, amendments should be considered to improve multi-metal mine tailing quality and stabilize contaminants, making conditions suitable for establishing metal-tolerant plants.
Amending with biochar has been shown to be an effective method of improving multi-metal-contaminated soil quality. Biochar is a carbon-rich co-product produced from biomass by pyrolysis under high-temperature and low-oxygen conditions. Biochar can be used as a soil amendment to improve soil quality and supply and retain nutrients, thereby enhancing plant growth [6,7,8]. Furthermore, biochar can absorb heavy metals to alleviate the associated toxicity toward plants through bulk surface area, pore size distribution, surface negative charges, high charge density and abundant functional groups [9,10,11]. Fellet et al. [12,13] also proposed that biochar can ameliorate substrates in terms of nutrient supply, decrease the availability of heavy metals in mine tailings and promote plant establishment, highlighting the potential of biochar as a soil amendment for multi-metal mine tailings. However, biochar’s effects in phytostabilization vary with biochar feedstock, biochar addition rate and the characteristics of the mine tailings. Further experiments should be performed to select the best biochar and biochar application rate for specific multi-metal mine tailings.
Metal-tolerant plants are another key factor for the ecological restoration of multi-metal mine tailings. Cassia alata L. is commonly known as a member of the Leguminosae family, an evergreen perennial shrub as well as a potential ornamental and medicinal plant that grows in the subtropical climate regions of China [14]. The plant’s medicinal functions in alleviating the symptoms of asthma attacks and ecological functions in enhancing resistance to soil ecosystem disturbances are becoming increasingly attractive to researchers [15]. However, studies have shown that Cassia alata L. cultivation might help reclaim degraded mining lands [16]. Practices involving the remediation of multi-metal-contaminated soil using Cassia alata L. have shown that the plant offers potential metal tolerance with good growth performance. However, the potential of this plant for the phytostabilization of multi-metal mine tailings has rarely been studied. Thus, in this study, a pot experiment was conducted to explore the effects of different biochars on Cassia alata L. growth and heavy metal immobilization in multi-metal mine tailings. This study is the first to examine the effects of Cassia alata L. coupled with different biochars and addition rates on heavy metal stabilization of multi-metal mine tailings.

2. Materials and Methods

2.1. Mine Tailings and Biochar

The mine tailings were collected from a Pb/Zn tailing pond in Meizhou, China (116°13′0″ E, 24°23′10″ N). The climate of the mine tailings pond is subtropical, with precipitation reaching 1473 mm per year and with an annual average temperature of 21.7 °C. The average relative humidity is 78%. The mine tailings pond, measuring 36 m in height, has accumulated 3.8 × 105 m3 of mine tailings and is considered the fourth level tailing pond in China. The mine tailings were air-dried at room temperature and sifted through a 20-mesh sieve for the pot experiment.
The biochars were produced from kenaf (Hibiscus cannabinus) core, sewage sludge and chicken manure at 500 °C for 3 h, using the slow pyrolysis method described by Fellet et al. [12]. The biochars were named Hibiscus cannabinus biochar (HB), sewage sludge biochar (SB), chicken manure biochar (MB). The biochars were passed through a 20-mesh sieve for the pot experiment.
The basic properties of the mine tailings and biochars are presented in Table 1. The mine tailings had high total Pb, Zn, Cu, Cd and As contents (3642.7, 981, 70.5, 31.8 and 1587.1 mg·kg−1, respectively), a pH of 6.5, and low total carbon (TC) (0.3%) and total nitrogen (TN) contents (0.01%). The three biochars were suitable for alkaline soil amendment, with high TC and TN contents 23–250 and 39–275 times higher than those of the mine tailings, respectively. The biochars also had low heavy metal contents, except for SB, which showed high Zn (813.4 mg·kg−1) and Cd contents (2.6 mg·kg−1). BET surface area, Langmuir surface and pore volume of HB (117.61 m2·g−1, 232.63 m2·g−1 and 0.024 cm³·g−1) were higher than SB (14.10 m2·g−1, 71.46 m2·g−1 and −0.00073 cm³·g−1) and MB (6.52 m2·g−1, 20.74 m2·g−1 and −0.0013 cm³·g−1).

2.2. Pot Experimental Design

A pot experiment was conducted over 100 days under greenhouse conditions with the following 10 treatments (Table 2). The control group contained only 1 kg mine tailings (CK), while the amendment group featured three types of biochar amendment at rates of 0.4%, 1%, and 3% w/w. The rates of biochar were set in an appropriate range according to related works [17]. Specifically, the 1 kg mine tailings was mixed with the appropriate amounts of biochar; the mixture was then placed in a plastic pot (height of 11 cm, top diameter of 15 cm, and bottom diameter of 10 cm). All samples in the mine tailings group, which showed a 70% field water retention capacity, were incubated at 20–25 °C in the greenhouse for 14 days.
Seeds of Cassia alata L., sterilized with 1% H2O2, were sown on top of silicon sand, and 7 days later, the seedlings were replanted in incubated tailings. All pots, with two plants per pot, were watered every other day under greenhouse conditions with natural light and at an ambient temperature of 20–25 °C. The plants were harvested for measurements 100 days after transplanting.

2.3. Sampling and Analysis

In the harvest stage, plants and soil samples were collected, and plant height, biomass and root length were measured by WinRHIZO (Pro STD4800, Regent Instruments Inc., Sainte Foy, QC, Canada). Each Cassia alata L. plant was divided into roots and shoots and rinsed with deionized water, dried at 105 °C for 1 h, stored at 60 °C for 3 days to allow the samples to reach a constant weight, and then ground into powders. All powders were digested using an acid mixture (HClO4:HNO3 = 1:4, v/v) at 180 °C on a hotplate and then determined by ICP-OES (Optima 5300DV, Perkin Elmer, Waltham, MA, USA).
The rhizosphere soil of each Cassia alata L. plant was air-dried and sequentially ground and passed through 20-mesh and 100-mesh sieves. Samples of 20-mesh soil were used to analyze the following parameters: pH, which was measured in a solid/water slurry (solid:water = 1:2.5 w/w); and NH4NO3-extractable metal content, using the method described by Gryschko et al. [18]. Samples of 100-mesh soil were used to analyze the following parameters: total heavy metals, digested using an acid mixture (HCl:HNO3:HClO4 = 3:1:1, v/v) at 180 °C on a hotplate and then determined by ICP-OES; C, H, N and S contents, using an elemental analyzer (Vario EL cube, Elementar, Langenselbold, Germany); and chemical fractionation of metals in soil, using the improved BCR sequential extraction method of the China National Standard (GB/T 25282-2010) [19].

2.4. Statistical Analysis

The experimental data were subjected to a one-way ANOVA and Duncan’s multiple comparison test (p < 0.05) with the SPSS statistical software package ver. 20 (SPSS Inc., Chicago, IL, USA).

3. Results

3.1. Effects of Different Biochar Treatments on Plant Growth

In general, the results (Figure 1) indicated that Cassia alata L. is a potential metal-tolerant plant because it was able to grow on multi-metal mine tailings without any amendments, and the amendments with different biochars had significant effects by increasing the root and shoot biomass and the height and root length of the plants. In contrast to the control group, the different biochar treatments remarkably increased the shoot biomass by factors of 1.2–2.8, except for the HB1 and HB3 treatments. Plants treated with SB presented the highest shoot biomass, and the shoot biomass of plants increased with the amount of added SB. Similarly, the root biomass was enhanced by the biochar treatments, reaching 1.7–3.2 times the biomass of the CK-treated plants, and only the HB1 treatment had no significant effect.
The data pertaining to plant height and root length indicate that the SB3 treatment provided outstanding acceleration in growth. The plant height and root length of the CK-treated plants were 8.1 cm and 112.4 cm, respectively, and the SB3 treatment increased plant height and root length to 12.1 cm and 370.9 cm, respectively. SB3 (1.5 times), HB0.4 (1.3 times) and MB0.4 (1.2 times) were the optimum treatments for increasing plant height. With respect to root length, the optimum addition rates were provided by SB3 (3.3 times), HB3 (2.9 times) and MB0.4 (2.2 times).

3.2. Heavy Metal Concentration in Shoots and Roots of Cassia alata L.

The effects of the different biochar treatments on the concentration of metals in the shoots and roots of Cassia alata L. plants are illustrated in Figure 2. The concentrations of the five metals tested were higher in roots than in shoots. The different biochar amendments reduced the concentrations of Pb, Zn, Cu, Cd and As in the shoot of plants. Compared with the CK group, adding biochar decreased the Pb, Zn, Cu, Cd and As contents in shoots by 63.9–89.5%, 46.9–66.0%, 32.7–62.4%, 40.4–76.4% and 54.9–77.5%, respectively. Among these biochar treatments, plants treated with HB3, SB0.4, MB1, SB0.4 and MB0.4 presented the lowest shoot Pb, Zn, Cu, Cd and As concentrations. However, there were no significant differences in the shoot metal concentrations of Cassia alata L. plants among different biochar addition rates for the same type of biochar.
In general, plants treated with biochar increased the root Pb, Zn, Cu, Cd and As concentrations. Only the SB3 and HB0.4 treatments reduced the root Pb concentrations, by 17.3% and 15.5% respectively, but the results showed no significant differences. All biochar treatments increased the root Zn concentrations, by 1.05–1.30 times compared with the concentrations measured for the CK group. The MB treatments produced significant differences in root accumulation of Cu: MB0.4 and MB1 increased the concentration of Cu in roots by 37.2% and 24.2%, respectively, while the MB3 treatment decreased the concentration by 18.1%. None of the biochar treatments produced significant differences in root Cd content, while the SB3, MB3 and MB1 treatments reduced the root accumulation of Cd. HB0.4 and SB3 treatments reduced the uptake of As slightly, while the other treatments increased As differently.

3.3. Effects of Different Biochar Treatments on pH, TC, and TN in Mine Tailings

As shown in Table 3, the plant itself as well as the plant-biochar system could significantly increase the pH of mine tailings soil. The soil pH value of the control group was 6.5, which is faintly acidic, but the soil amendments increased this pH value to 6.8–7.1 due to the alkalinity of biochar and the application of large amounts of carbonates.
TC was affected by the rate of biochar addition as well as the biochar type. The TC contents of the HB treatments were significantly higher than those of the other biochar treatments. The TC contents of HB0.4, HB1 and HB3 were 159.24%, 355.13% and 590.01% higher than the TC content of CK, respectively. The TC content of SB3 was 56.01% higher than that of CK, while other treatments had no effect on TC content. Similar to the changes in TC contents, TN increased with the rate of biochar addition (Table 3). The TN contents of the HB0.4, HB1 and HB3 treatments were 120%, 90% and 100% higher than the TN content of CK, respectively. The TN contents of MB0.4, MB1 and MB3 were 20%, 40% and 140% higher than the TN content of CK, respectively. In addition, the TN contents of the SB treatments were significantly higher than those of the other biochar treatments: the TN contents of SB0.4, SB1 and SB3 were 80%, 210% and 650% higher than the TN content of CK.

3.4. Effects of Different Biochar Treatments on NH4NO3-Extractable Metal Content in Mine Tailings

Table 4 shows that the mine tailings were naturally low in NH4NO3-extractable metal contents. In general, the biochar treatments did not affect the contents of NH4NO3-extractable Pb and Cu, while small increments in the contents of NH4NO3-extractable Zn, Cd and As were observed. HB1 increased the NH4NO3-extractable Zn and As contents by 35% and 30%, respectively. The NH4NO3-extractable Zn and Cd contents under the SB treatment were 1.2–1.3, 1.2–1.4 times those of CK, respectively. In addition, the NH4NO3-extractable As contents under the MB treatments were significantly higher than those of CK: the contents under the MB0.4, MB1 and MB3 treatments were 23.1%, 30.8% and 35.9% higher than the content of CK, respectively.

3.5. Effects of Different Biochar Treatments on Chemical Fractionation of Metals in Mine Tailings

Table 5 and Figure 3 show that the chemical fractionation of Pb, Cu, Cd and As in the mine tailings mainly existed in the residual fraction. The residual fractions in the mine tailing have been considered as inert and inaccessible to biota [20]. All biochar treatments produced low mild acid-soluble Pb and As contents, which indicated low mobility in the mine tailings. The addition of biochar significantly reduced the activities of Pb and Cu, with the SB treatments decreasing the activities of mild acid-soluble Pb and Cu by 23.4–34.5% and 27.8–59.1%, respectively. In addition, the mild acid-soluble Pb and Cu contents decreased with the rate of biochar addition. In contrast, a difference in the mild acid-soluble Zn, Cd and As contents was observed among the biochar treatments; the mild acid-soluble Zn, Cd and As contents of the HB treatments were 21.3–34.3%, 10.7–25.9% and 6.1–165.3% higher than those of CK, respectively. Most intriguingly, adding MB had the most significant effect on the mild acid-soluble As content, which was 16.4–250% higher than that of CK. Increasing the amount of added biochar stimulated the leaching of As, and the mild acid-soluble As contents of HB3 and SB3 were 2.6 and 3 times the content of CK.

4. Discussion

4.1. Effects of Biochar on Plant Growth and Heavy Metal Concentration

The main factors affecting metal tolerance in plants are growth speed, high biomass, heavy metal tolerance and low metal accumulation in shoots [21]. The results of our study show that Cassia alata L. could be a potential phytostabilization plant in high-multi-metal-contaminated soils, and biochar amendment can help increase the plant shoot biomass as well as the root biomass. In our study, all three biochars significantly increased the shoot and root biomass of plants. The SB3 treatment showed the best effect on plant growth in the growth substrate, increasing the biomass of shoots and roots of plants by factors of 2.8 and 3.2, respectively. These positive effects on the biomass of plants after biochar addition have been observed in research on corn and other plants [13,22]. This finding may be attributed to the reduction in metal toxicity caused by immobilization and biochar-provided nutrients [23]. Our research shows that biochar significantly increased the TC and TN contents, which might be attributed to biochar feedstocks and the high TC and TN contents of biochar. SB generally showed a higher TN content than the other biochars, enabling it to supply nutrients to enhance plant growth [24,25]. However, not all types of biochar showed improved performance at high application rates. For example, The HB0.4 and MB0.4 treatments produced higher biomass than the other rates of biochar addition. This finding is similar to that reported by Rillig et al. [26], who showed that plant biomass depended on biochar type and addition rate, with positive effects at low rate of biochar addition (<20%, v/v), but negative effects for higher rates. The reason is that some biochar can not only increase nutrient retention and increase nutrient efficiency but may also decrease the availability of nutrients by adsorbing phosphate in such poor nutrients as mine tailings [27,28]. In addition, high concentration of biochar addition may change soil function by inducing adverse impact on microbial community structure and activity [29], which may also affect the plant growth. Therefore, the suitable addition rate of biochar combined with other organic amendment might be suitable to regulate both nutrient and heavy metal stabilization in nutrient poor mine tailing.
Low metal accumulation in shoots is another important standard for assessing the phytostabilization potential of plants grown on multi-metal-contaminated soils, which would help control the spread of heavy metals to surrounding areas and reduce the long-term threat to ecosystems, food security and human health. Our results showed that Cassia alata L. did not accumulate high concentrations of heavy metals in shoots in general. In contrast, metals were precipitated or accumulated in roots. Himd et al. [30] indicated that biochar application could reduce Pb, Cd and Zn concentrations in the shoots of bean. Zheng et al. [31] also conducted an experiment involving the application of three biochars to a multi-metal-polluted soil with rice, and the biochars reduced the shoot metal concentration. However, our research showed no significant differences in the Pb, Zn, Cu, Cd and As concentrations of the shoots of plants, regardless of the biochar addition rate. This finding can be attributed to the immobilization of bioavailable metals as well as the dilution effect caused by increasing plant biomass [32]. In our study, application of biochar significantly increased the soil mild acid-soluble As, whilst the As content in shoot still decreased remarkably. This is in line with the results reported by Beesley et al. [33], in which the solubility and mobility of As were increased by orchard prune residue biochar amendment, but uptake to tomato plant was reduced. Such a phenomenon could be explained by that compartmentalisation of As in the roots of plant has been identified in As(III) spiked soils as root cell damage above toxic As thresholds can reduce transport of As upwards in the plant. The competition between As and other element linked with the mobility and bioavailability of As species, e.g. P originated from the sludge derived biochar [34], allowed As (V) to be more retained, which consequently led to the reduction of As uptake to plant [33]. In addition, the formation of soluble As-DOC (dissolved organic carbon) complexes might be another mechanism, since As in this form are mobile but might not be able to diffuse through the tissue of the plant [35].

4.2. Effect of Biochar on Mine Tailings

The mine tailings used in our study contained high multi-metal concentrations and low organic matter and nutrient contents, which limited natural plant establishment. In abandoned mine tailings ponds, biochar can be used to improve soil quality, reduce the mobility of heavy metals and increase the pH and cation exchange capacity (CEC) [12], which will help restore soil function and enhance pioneer plant establishment. The results of our research suggest that the pH of mine tailings increased with the addition rate of biochar, regardless of the biochar type (HB, SB and MB). This finding is in line with previous studies indicating that biochar pH and the liming effect could increase soil pH [12,13]. Reverchon et al. [36] also described increases in soil pH following biochar application to acidic soil. Increasing pH can decrease the mild acid-soluble Pb and Cu concentrations in mine tailings. Because HB, SB and MB are alkaline soil amendments, they can regulate soil pH. The pH of the SB treatment was 6.83, and the mild acid-soluble Pb and Cu contents still decreased significantly. This finding may be linked to the high ash content of the SB treatment [37].
Previous studies have indicated that the properties of biochar are conducive to metal stabilization. The high surface area, spatial structure and various organic functional groups of biochar could reduce mild acid-soluble metals [38,39]. HB is a low-ash biochar with a carbon content greater than 75%, while SB is a high-ash biochar with a carbon content less than 20%. The results showed that SB had a better effect than the HB treatment on metal immobilization. The results are similar to those of Yang et al. [34], whose soil incubation experiment showed that sewage sludge biochar had a better effect on Pb immobilization. The metal (Pb and Cu) sorption mechanism of biochar is attributed to metal precipitation, providing surface Ca2+ and Mg2+ with which to exchange metal and organic hydroxyl and carboxyl functional groups for surface complexation [40,41]. Cao et al. [42] noted that for SB containing a high P content, the dissolution of P is attributed to the presence of Pb and precipitation. Therefore, the reduction of mild acid-soluble Pb and Cu may further promote the growth of Cassia alata L. However, the biochars tested in this study had little positive effect on the immobilization of As, Zn and Cd. At a 3% addition rate in particular, the content of mild acid-soluble As increased significantly. An increase in arsenic availability has also been observed in other studies on soil and plant systems [43]. It has been reported that biochar amendment can increase the soil pH due to its alkaline effect, which may further increase As release. In our study, the pH of different biochar treatments significantly increased in the pot experiment. Increased soil pH will reduce positively charged sites in soil, hence the sites available for the As binding are reduced in the biochar treated soil [35]. Meanwhile, the biochar can act as electron donors to govern the rapid reduction of As(V) to As(III) through its O-containing functional groups. In addition, other studies [44,45] have indicated that the redox reaction of Fe, biotransformation of As and high P content of biochar are related to the enhanced concentration of mild acid-soluble As. Sewage sludge biochar as a soil amendment for acid soil remediation represents a potential application of abundant sewage sludge [41]. Compared with plant biochar, the SB treatment had a better effect on Pb and Cu immobilization. In addition, SB contains more nutrients, which may prevent nutrient leaching and increase plant biomass in multi-metal mine tailings. Although the pyrolyzed sewage sludge biochar showed better heavy metal stability, Zn and Cd, present in high concentrations, have high activities [46]. In our study, SB as a soil amendment was more suitable for Cassia alata L. plant establishment in multi-metal mine tailings. However, the potential risks of mild acid-soluble As release and As activation caused by SB in the high-As-contaminated mine tailings deserve further attention.

5. Conclusions

Cassia alata L. could be a potential phytostabilization plant in high-multi-metal-contaminated mine tailings because of its good growth and low heavy metal accumulation in shoots. Adding the three types of biochar examined in this study can increase plant growth and decrease heavy metal accumulation in shoots. The SB3 treatment showed the best effect on plant growth, increasing the biomass of shoots and roots, plant height and root length by factors of 2.8, 3.2, 1.5 and 3.3 compared with the CK treatment, respectively. The biochars can increase the soil pH, TC, and TN and decrease the mild acid-soluble Pb and Cu concentrations in the mine tailings. However, all of these biochars had little positive effect on the immobilization of As, Zn and Cd, and the potential risks of As release and activation observed with increasing biochar dose deserve further attention. Overall, Cassia alata L. plant establishment in such multi-metal mine tailings can be enhanced by biochar amendment, where the SB3 treatment might be the best choice, but the potential risk of As release must still be monitored and controlled.

Acknowledgments

This study was financially supported by the Special Fund of Environmental Protection Research for Public Welfare from the Ministry of Environmental Protection, China (No. 201509037); the Fundamental Research Funds for the Central Universities (No. 16lgjc57); and Science and Technology Planning Project of Guangdong Province, China (No. 2016A020221012; 2017B020216008).

Author Contributions

Lige Huang, Yuanqing Chao and Shizhong Wang conceived and designed the experiments; Lige Huang and Yuanyuan Li performed the experiments; Lige Huang analyzed the data; Man Zhao and Yanhua Yang contributed materials and analysis tools; Lige Huang wrote the paper; Rongliang Qiu and Shizhong Wang provided comments on the paper.

Conflicts of Interest

The authors declare no conflict of interest.

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Figure 1. The effects of HB, SB and MB treatments on the plant growth. Shown are the (A) shoot biomass, (B) root biomass, (C) plant height and (D) root length of Cassia alata L. grown in mine tailings with different treatments. The vertical bars in the figures represent the standard errors of the means (n = 3), Different letters indicate significant differences among different treatments at a significance level of 0.05. CK, HB/SB/MB0.4, HB/SB/MB1 and HB/SB/MB3 refer to no biochar input and the incorporation of biochar into the soil at 0.4%, 1% and 3% by mass, respectively. HB: Hibiscus cannabinus core biochar; SB: sewage sludge biochar; MB: chicken manure biochar.
Figure 1. The effects of HB, SB and MB treatments on the plant growth. Shown are the (A) shoot biomass, (B) root biomass, (C) plant height and (D) root length of Cassia alata L. grown in mine tailings with different treatments. The vertical bars in the figures represent the standard errors of the means (n = 3), Different letters indicate significant differences among different treatments at a significance level of 0.05. CK, HB/SB/MB0.4, HB/SB/MB1 and HB/SB/MB3 refer to no biochar input and the incorporation of biochar into the soil at 0.4%, 1% and 3% by mass, respectively. HB: Hibiscus cannabinus core biochar; SB: sewage sludge biochar; MB: chicken manure biochar.
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Figure 2. Effects of HB, SB and MB treatments on (A) Pb, (B) Zn, (C) Cu, (D) Cd and (E) As contents in shoots and roots of Cassia alata L. The vertical bars in the figures represent the standard errors of the means (n = 3), Different letters indicate significant differences among different treatments at a significance level of 0.05. CK, HB/SB/MB0.4, HB/SB/MB1 and HB/SB/MB3 refer to no biochar input and the incorporation of biochar into the soil at 0.4%, 1% and 3% by mass, respectively. HB: Hibiscus cannabinus core biochar; SB: sewage sludge biochar; MB: chicken manure biochar.
Figure 2. Effects of HB, SB and MB treatments on (A) Pb, (B) Zn, (C) Cu, (D) Cd and (E) As contents in shoots and roots of Cassia alata L. The vertical bars in the figures represent the standard errors of the means (n = 3), Different letters indicate significant differences among different treatments at a significance level of 0.05. CK, HB/SB/MB0.4, HB/SB/MB1 and HB/SB/MB3 refer to no biochar input and the incorporation of biochar into the soil at 0.4%, 1% and 3% by mass, respectively. HB: Hibiscus cannabinus core biochar; SB: sewage sludge biochar; MB: chicken manure biochar.
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Figure 3. Effects of HB, SB and MB treatments on chemical fractionation of (A) Pb, (B) Zn, (C) Cu, (D) Cd and (E) As in mine tailings (n = 3). CK, HB/SB/MB0.4, HB/SB/MB1 and HB/SB/MB3 refer to no biochar input and the incorporation of biochar into the soil at 0.4%, 1% and 3% by mass, respectively. HB: Hibiscus cannabinus core biochar; SB: sewage sludge biochar; MB:chicken manure biochar.
Figure 3. Effects of HB, SB and MB treatments on chemical fractionation of (A) Pb, (B) Zn, (C) Cu, (D) Cd and (E) As in mine tailings (n = 3). CK, HB/SB/MB0.4, HB/SB/MB1 and HB/SB/MB3 refer to no biochar input and the incorporation of biochar into the soil at 0.4%, 1% and 3% by mass, respectively. HB: Hibiscus cannabinus core biochar; SB: sewage sludge biochar; MB:chicken manure biochar.
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Table
Table 1. Basic properties of mine tailings and different biochars.
Table 1. Basic properties of mine tailings and different biochars.
MaterialHBSBMBMTSEQS
Pb (mg·kg−1)3571.412.43642.7500
Zn (mg·kg−1)100.3813.4328981500
Cu (mg·kg−1)0.2203.540.470.5400
Cd (mg·kg−1)0.32.60.231.81
As (mg·kg−1)1.818.73.41587.140
pH7.57.19.16.5-
C (%)75.119.370.3-
H (%)2.91.30.50.3-
N (%)0.392.750.710.01-
S (%)0.210.350.471.3-
BET Surface (m2·g−1)117.6114.106.52--
Langmuir Surface (m2·g−1)232.6371.4620.74--
Micro-pore volume (cm3·g−1)0.024−0.00073−0.0013--
Median pore width (nm)0.730.740.74--
HB: Hibiscus cannabinus core biochar; SB: sewage sludge biochar; MB: chicken manure biochar; MT: Mine Tailing; SEQS: Soil environmental quality standard in China (GB 15618-1995).
Table
Table 2. Experimental design for pot trial.
Table 2. Experimental design for pot trial.
GroupNumberMine Tailings (kg)Amendment (w/w)Repetition
Control groupCK1-3
Amendment GroupHB0.410.4% HB3
HB111% HB3
HB313% HB3
SB0.410.4% SB3
SB111% SB3
SB313% SB3
MB0.410.4% MB3
MB111% MB3
MB313% MB3
HB: Hibiscus cannabinus core biochar; SB: sewage sludge biochar; MB: chicken manure biochar. CK, HB/SB/MB0.4, HB/SB/MB1 and HB/SB/MB3 refer to no biochar input and the incorporation of biochar into the soil at 0.4%, 1% and 3% by mass, respectively.
Table
Table 3. Effects of HB, SB and MB treatments on pH, TC, and TN in mine tailings.
Table 3. Effects of HB, SB and MB treatments on pH, TC, and TN in mine tailings.
TreatmentpH 1TC 1 (g·kg−1)TN 1 (g·kg−1)
CK6.53 ± 0.02f3.41 ± 0.07d0.1 ± 0.01f
HB0.47.13 ± 0.01a8.84 ± 0.46cd0.22 ± 0.02c
HB17.05 ± 0.03b15.52 ± 4.47b0.19 ± 0.05cd
HB37.08 ± 0.04ab23.7 ± 1.51a0.2 ± 0.02cd
SB0.46.89 ± 0.01de4.52 ± 0.2cd0.18 ± 0.01cde
SB16.88 ± 0.03e5.32 ± 0.12cd0.31 ± 0.01b
SB36.83 ± 0.02e8.28 ± 0.21c0.75 ± 0.03a
MB0.47.03 ± 0.01b4.03 ± 0.26cd0.12 ± 0.01ef
MB17.01 ± 0.02bc4.12 ± 0.08cd0.14 ± 0def
MB36.95 ± 0.03cd5.47 ± 0.04cd0.24 ± 0.01c
1 Values represent the mean ± standard error (n = 3), different letters indicate significant differences among different treatments at a significance level of 0.05.
Table
Table 4. Effects of HB, SB and MB treatments on NH4NO3-extractable Pb, Zn, Cu, Cd and As contents in mine tailings.
Table 4. Effects of HB, SB and MB treatments on NH4NO3-extractable Pb, Zn, Cu, Cd and As contents in mine tailings.
TreatmentNH4NO3-Extractable Metal Contents (mg·kg−1)
Pb 1Zn 1Cu 1Cd 1As 1
CK0.35 ± 0.02ab3.42 ± 0.1d0.39 ± 0.00abc0.1 ± 0.00de0.39 ± 0.04cd
HB0.40.34 ± 0.01ab3.17 ± 0.09d0.39 ± 0.00abc0.08 ± 0.00e0.38 ± 0.02cd
HB10.35 ± 0.01ab4.62 ± 0.33a0.39 ± 0.01abc0.13 ± 0.01ab0.34 ± 0.01d
HB30.37 ± 0.01ab4.17 ± 0.26abc0.38 ± 0.00bcd0.12 ± 0.01abc0.43 ± 0.02abcd
SB0.40.34 ± 0.02ab4.32 ± 0.17ab0.37 ± 0.00cd0.12 ± 0.01abcd0.35 ± 0.01d
SB10.46 ± 0.11a4.14 ± 0.1abc0.38 ± 0.00cd0.14 ± 0.01a0.42 ± 0.04abcd
SB30.34 ± 0.00ab4.32 ± 0.16ab0.36 ± 0.00d0.13 ± 0.01ab0.41 ± 0.03bcd
MB0.40.35 ± 0.01ab3.78 ± 0.14bcd0.4 ± 0.02ab0.1 ± 0.00de0.48 ± 0.05abc
MB10.33 ± 0.00b3.68 ± 0.16cd0.4 ± 0.01ab0.11 ± 0.01bcd0.51 ± 0.06ab
MB30.36 ± 0.01ab3.7 ± 0.22cd0.41 ± 0.01a0.1 ± 0.00cde0.53 ± 0.02a
1 Values represent the mean ± standard error (n = 3), different letters indicate significant differences among different treatments at a significance level of 0.05.
Table
Table 5. Effects of HB, SB and MB treatments on chemical fractionation of metal in mine tailings (%).
Table 5. Effects of HB, SB and MB treatments on chemical fractionation of metal in mine tailings (%).
MetalTreatmentMild Acid-Soluble 1Reducible Fraction 1Oxidizable Fraction 1Residual 1
PbCK1.45 ± 0.26ab22.34 ± 0.87b0.61 ± 0.15b75.6 ± 0.66a
HB0.41.36 ± 0.1ab23.38 ± 0.32ab0.63 ± 0.1b74.63 ± 0.18ab
HB11.27 ± 0.18ab25.99 ± 1.31ab0.56 ± 0.08b72.19 ± 1.53ab
HB31.71 ± 0.12a33.44 ± 1.37a0.63 ± 0.26b64.22 ± 1.38b
SB0.41.11 ± 0.11ab20.77 ± 6.47b0.94 ± 0.14ab77.19 ± 6.58a
SB11.01 ± 0.11b20.39 ± 1.79b0.66 ± 0.05b77.94 ± 1.69a
SB30.95 ± 0.03b15.02 ± 0.25b0.82 ± 0.15ab83.21 ± 0.4a
MB0.40.96 ± 0.11b20.53 ± 1.52b0.9 ± 0.1ab77.6 ± 1.73a
MB11.38 ± 0.31ab19.71 ± 1.56b1.27 ± 0.29ab77.64 ± 1.83a
MB31.22 ± 0.29ab22.83 ± 7.17b1.51 ± 0.58a74.45 ± 8ab
ZnCK31.81 ± 4.85a16.65 ± 0.32a6.69 ± 0.22c44.85 ± 4.37a
HB0.438.64 ± 1.95a17.96 ± 0.58a9.17 ± 1.12ab34.24 ± 1.32abc
HB141.31 ± 6.56a18.71 ± 1.33a9.61 ± 0.47a30.37 ± 8.31bc
HB342.72 ± 1.71a20.42 ± 0.52a9.56 ± 1.11a27.3 ± 2.96c
SB0.432.06 ± 1.38a17.94 ± 5.63a7.07 ± 0.3bc42.93 ± 4.87ab
SB132.89 ± 0.94a19.92 ± 3.01a7.84 ± 0.6abc39.35 ± 1.8abc
SB332.06 ± 1.82a16.06 ± 0.85a7.56 ± 0.3abc44.32 ± 1.57a
MB0.435.41 ± 3.22a17.29 ± 0.37a9.12 ± 0.17abc38.18 ± 3.69abc
MB134.32 ± 1.28a13.89 ± 0.55a7.97 ± 0.62abc43.83 ± 1.34ab
MB333.88 ± 3.4a13.75 ± 0.31a8.71 ± 0.82abc43.66 ± 4.45ab
CuCK10.2 ± 1.65ab16.57 ± 0.25ab14.64 ± 3.96a58.59 ± 4.69a
HB0.410.32 ± 0.68ab16.34 ± 1.28ab12.65 ± 2.3a60.7 ± 3.03a
HB19.93 ± 1.3ab19.98 ± 0.97ab11.31 ± 2.79a58.78 ± 3.99a
HB310.46 ± 0.14ab22.39 ± 0.6a12.29 ± 1.56a54.86 ± 1.69a
SB0.47.36 ± 0.71bc15.59 ± 4.59b10.45 ± 1.87a66.59 ± 2.85a
SB17.23 ± 0.72bc19.15 ± 2.71ab18.66 ± 2.28a54.96 ± 3.77a
SB34.17 ± 0.44c14.71 ± 0.34b19.98 ± 3.16a61.15 ± 3.22a
MB0.410.77 ± 1.1ab18.2 ± 1.2ab19.21 ± 2.94a51.82 ± 5.22a
MB112.61 ± 2.7a16.71 ± 1.84ab18.77 ± 5.12a51.91 ± 9.49a
MB38.32 ± 1.39ab16.17 ± 1.34ab20.16 ± 4.61a55.35 ± 7.33a
CdCK7.56 ± 1.21a13.17 ± 0.37ab3.1 ± 0.58a76.18 ± 0.28a
HB0.48.37 ± 0.34a13.74 ± 0.15ab4.08 ± 0.14a73.8 ± 0.11ab
HB18.88 ± 0.91a14.73 ± 0.94ab4.48 ± 0.4a71.91 ± 0.96ab
HB39.52 ± 0.24a17.63 ± 0.41a4.38 ± 0.48a68.47 ± 1.12b
SB0.47.03 ± 0.25a13.8 ± 4.21ab4.12 ± 0.58a75.05 ± 4.35a
SB17.75 ± 0.19a16.05 ± 1.68ab4.63 ± 0.42a71.56 ± 1.57ab
SB37.57 ± 0.4a13.02 ± 0.3ab3.9 ± 0.4a75.51 ± 0.41a
MB0.48.57 ± 1.02a13.05 ± 0.99ab4.11 ± 0.09a74.27 ± 1.93ab
MB19.16 ± 0.8a12.39 ± 0.27b4.21 ± 0.55a74.25 ± 1.25ab
MB39.1 ± 1.35a12.37 ± 0.66b4.04 ± 0.56a74.49 ± 2.42ab
AsCK0.49 ± 0.1d16.55 ± 0.62a3.69 ± 0.9a79.28 ± 1.42a
HB0.40.52 ± 0.05d17.5 ± 0.51a4.6 ± 0.38a77.37 ± 0.4ab
HB10.53 ± 0.09d18.51 ± 1.5a5.18 ± 0.54a75.78 ± 0.91ab
HB31.3 ± 0.2b22.94 ± 0.69a5.21 ± 0.56a70.55 ± 1.42b
SB0.40.63 ± 0.09cd17.77 ± 5.41a5.28 ± 0.93a76.33 ± 5.94ab
SB10.88 ± 0.06cd20.05 ± 1.94a5.53 ± 0.66a73.55 ± 2.14ab
SB31.49 ± 0.07ab16.43 ± 0.33a4.73 ± 0.51a77.34 ± 0.71ab
MB0.40.57 ± 0.06cd16.2 ± 1.12a4.78 ± 0.31a78.44 ± 0.97ab
MB10.92 ± 0.07c16.97 ± 1.01a5.43 ± 1.06a76.68 ± 2.13ab
MB31.73 ± 0.23a16.94 ± 2.06a4.99 ± 0.61a76.33 ± 2.65ab
1 Values represent the mean ± standard error (n = 3), different letters indicate significant differences among different treatments at a significance level of 0.05.

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Huang, L.; Li, Y.; Zhao, M.; Chao, Y.; Qiu, R.; Yang, Y.; Wang, S. Potential of Cassia alata L. Coupled with Biochar for Heavy Metal Stabilization in Multi-Metal Mine Tailings. Int. J. Environ. Res. Public Health 2018, 15, 494. https://doi.org/10.3390/ijerph15030494

AMA Style

Huang L, Li Y, Zhao M, Chao Y, Qiu R, Yang Y, Wang S. Potential of Cassia alata L. Coupled with Biochar for Heavy Metal Stabilization in Multi-Metal Mine Tailings. International Journal of Environmental Research and Public Health. 2018; 15(3):494. https://doi.org/10.3390/ijerph15030494

Chicago/Turabian Style

Huang, Lige, Yuanyuan Li, Man Zhao, Yuanqing Chao, Rongliang Qiu, Yanhua Yang, and Shizhong Wang. 2018. "Potential of Cassia alata L. Coupled with Biochar for Heavy Metal Stabilization in Multi-Metal Mine Tailings" International Journal of Environmental Research and Public Health 15, no. 3: 494. https://doi.org/10.3390/ijerph15030494

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