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Article

Remediation of Pb-, Zn-, Cu-, and Cd-Contaminated Soil in a Lead–Zinc Mining Area by Co-Cropping Ilex cornuta and Epipremnum aureum with Illite Application

by
Qi Li
1,
Yanxin Tang
1,
Dubin Dong
2,
Xili Wang
3,
Xuqiao Wu
1,
Saima Gul
4,
Yaqian Li
5,
Xiaocui Xie
1,
Dan Liu
1,* and
Weijie Xu
1
1
State Key Laboratory of Subtropical Silviculture, Key Laboratory of Soil Contamination Bioremediation of Zhejiang Province, Zhejiang A&F University, Hangzhou 311300, China
2
College of Life Science and Technology, Central South University of Forestry and Technology, Changsha 410004, China
3
Zhejiang Economic & Information Center, Hangzhou 310006, China
4
Department of Chemistry, Islamia College University Peshawar, Peshawar 25120, Pakistan
5
People’s Government of Jiaxing, Jiaxing 323500, China
*
Author to whom correspondence should be addressed.
Agriculture 2024, 14(6), 867; https://doi.org/10.3390/agriculture14060867
Submission received: 22 April 2024 / Revised: 25 May 2024 / Accepted: 28 May 2024 / Published: 30 May 2024
(This article belongs to the Section Agricultural Soils)
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Abstract

Phytoremediation is considered an effective strategy for remediation of heavy-metal-contaminated soil in mining areas. However, single-species plants cannot reach the highest potential for uptake of heavy metals due to inhibition of their growth by high concentrations of heavy metals in the soil. Therefore, this study has explored the effects of illite application and two plant species’ co-cropping on soil quality, plant growth, and heavy metal transformation in a soil–plant system. The results reveal that the addition of 1% (mass fraction) of illite significantly enhances soil pH. The co-cropping of Ilex cornuta and Epipremnum aureum is beneficial for improving the organic matter content of the soil. The contents of EDTA-extractable Pb, Zn, and Cu were significantly reduced by 29.8–32.5%, 1.85–5.72%, and 30.0–32.9%, respectively, compared to the control. The co-cropping of Ilex cornuta and Epipremnum aureum promoted enrichment effects of Epipremnum aureum on Pb and Ilex cornuta on Cd (p < 0.05). The co-cropping pattern lowered the biomass of Ilex cornuta and Epipremnum aureum; however, co-cropping of Ilex cornuta and Epipremnum aureum promoted the elimination of Pb, Zn, Cu, and Cd from the soil at 13.0–75.8%, 11.1–38.2%, 8.39–88.4%, and 27.8–72.5%, respectively. It is concluded that illite application combined with co-cropping of Ilex cornuta and Epipremnum aureum is highly effective for the elimination of Pb, Zn, Cu, and Cd from contaminated soil. This study provides a theoretical basis and pathway for the restoration of heavy-metal-contaminated soil in mining with the application of bentonite combined with phytoremediation.

1. Introduction

In recent years, intensive metal mining and smelting activities have resulted in significant heavy metal contamination in farmland soils surrounding mining areas. Pollution of these farmland soils poses a serious threat to the soil ecosystem due to its high toxicity, mobility, and non-degradation and its transfer to the food chain through uptake by crops, which induces diseases such as bone pain and kidney failure [1,2,3]. Consequently, research into remediation techniques for heavy-metal-contaminated soils in mining areas has garnered widespread attention from scholars worldwide. Remediating soils polluted by heavy metals has emerged as a challenging task globally [4,5]. Stabilization/solidification technology has become one of the commonly used repair technologies due to its rapid process and economic advantages [6]. Hyperaccumulating phytoremediation of heavy-metal-contaminated soils is a current research area.
Phytoremediation refers to the utilization of plants with characteristics such as hyperaccumulation, high stability, and volatility to adsorb heavy metal elements in soil, thereby reducing the quantity of heavy metal elements in contaminated soil and restoring soil quality. This technique typically exploits hyperaccumulator enrichment capabilities towards heavy metals, absorbing them from the soil through the roots and subsequently transporting and storing them in the aboveground parts of the plants. A hyperaccumulator must be tolerant to a variety of heavy metals, have a high growth rate, and be able to produce large amounts of biomass, thus ensuring good phytoremediation efficiency [7,8]. Previous studies have demonstrated that Southeastern Sedum has good enrichment and a good uptake capacity for cadmium in low-cadmium-contaminated soil, and lobelia has a good enrichment effect on arsenic in soil [9,10]. Epipremnum aureum is an ecological niche landscape plant commonly used for the remediation of river water pollution. Abdulkadir’s research revealed that the combined application of Epipremnum aureum and immobilized bacteria can reduce lead concentrations in water and enhance the abilities of Epipremnum aureum for uptake and enrichment [11]. Singh’s research findings revealed that Epipremnum aureum achieved removal rates of 44.3% for Cr and 38.9% for Cd from water, suggesting promising prospects in the field of phytoremediation [12]. Phytoremediation involves reduced expenses in contrast to alternative approaches, while also reducing the quantity of heavy metal elements in polluted soil to levels compliant with environmental regulations. Although hyperaccumulators can survive in highly contaminated soils, their slow growth rate and small biomass constrain the elimination effect in these soils.
The clay minerals (such as kaolinite, montmorillonite, illite, etc.) as stabilizing materials of repair technologies can absorb interlayer toxic cations and can fix ions in the crystal structure. The clay minerals as passivate contaminants can change the existing forms of pollutants in the soil and can reduce their mobility and bioavailability in the environment, which can deactivate pollutants [13,14]. The research conducted by Liu et al. revealed that the application of phosphate rock and zeolite separately to soil led to a significant reduction in the bioavailability of Cd in the soil and changed the soluble, exchangeable, and specifically sorbed fractions to oxide-bound and organic-bound fractions, effectively remediating Cd-contaminated soil [15]. Ou’s study found that the addition of illite/smectite clay reduced the DTPA-extracted fractions of Cd, Zn, Cu, and Pb in the soil by 5.1%, 5.6%, 12.2%, and 14.2% [16]. The clay minerals are rich in reserves, low in price, and have great potential for practical application [17,18].
The current studies have emphasized the adsorption of heavy metal ions from soil by clay minerals or the uptake of heavy metals by hyperaccumulators [19,20]. Phytoremediation often employs the inter-cropping of a hyperaccumulator and a non-hyperaccumulator. Meanwhile, a single remediation technology cannot achieve the elimination of heavy metals from soil. A few studies have emphasized the potential of phytoremediation combined with clay minerals to immobilize heavy metals in soil. Currently, there is limited research on the effectiveness of co-cropping multiple ecological niche landscape plant species for the removal of heavy metals from soil. Before commencing this study, we conducted on-site surveys of the mining area and observed that Ilex cornuta is extremely resistant to heavy metals and is appropriate for growth in heavily polluted soil. Therefore, in this study, Ilex cornuta and Epipremnum aureum were selected as co-cropping plants, combined with illite for a pot experiment, to explore the remediation effect of adding illite to heavy-metal-contaminated soil in Pb-Zn mining areas under a co-cropping mode. This strategy has implications for the ecological restoration of mining areas.

2. Materials and Methods

2.1. Soil Samples

The soil in the pot experiment was collected from 0–20 cm cultivated surface soil near a lead–zinc mine in Shaoxing City, Zhejiang Province. The soil physical and chemical properties are presented in Table 1. The collected soil samples were air-dried, sieved to remove humus and plant residues from the soil, and passed through a 2 mm nylon sieve. Illite was purchased from a commercial chemical company in Hangzhou, Zhejiang Province. The illite physical and chemical properties are presented in Table 2.

2.2. Experimental Design

The experiment was conducted at the Pingshan Experimental Base of Zhejiang Agriculture and Forestry University (30°15′52″ N, 119°42′54″ E), located in Hangzhou, Zhejiang Province, China. The seeds of Ilex cornuta and Epipremnum aureum were planted on 18 March 2019 and harvested on 18 May 2019. The indoor pot experiment container was a plastic pot with a diameter of 26.5 cm. A 1% mass fraction of illite was added and mixed with the soil in the pot. Each pot contained 3 kg of soil, stabilized for a week. There were five treatments in the experiment: illite application and Ilex cornuta mono-cropping (II); illite application and Epipremnum aureum mono-cropping (IE); illite application and co-cropping of Ilex cornuta and Epipremnum aureum (IIE); illite application and non-planting (IN); and the control (non illite application and non-planting, CK). There were three repetitions for each group, with a total of 15 pots. There were five plants per pot in the single-plant mode, and three Ilex cornuta in each pot and four Epipremnum aureum in the co-cropping mode. Seedlings with similar and vigorous growth were selected for transplantation. The plants were grown in natural light conditions in a greenhouse. The field water-holding capacity was maintained at 60% during the growth period. The plants were harvested and tested after a two-month period.

2.3. Soil Physicochemical Properties

The soil samples were air-dried naturally, and then any remaining animal or plant remains were removed. Subsequently, the samples were ground and sieved through 100 mesh sieves for further use. The soil pH value was determined in a suspension of 1:2.5 H2O with a pH meter. The total organic matter content in soils was determined by oxidation with potassium dichromate in a heated oil bath. The total amount of heavy metals in the soil was determined by using the aqua regia-perchloric acid digestion/ICP-OES method. The different forms of heavy metals in the soil were extracted by BCR sequential extraction. This method divided heavy metals in four chemical forms [21]: the acid-exchangeable fraction (F1, 20 mL 0.11 mol/L acetic acid solution, oscillated for 16 h, centrifuged at 1006× g for 20 min); reducible fraction (F2, 20 mL 0.5 mol/L hydroxylamine hydrochloride, pH = 1.5, oscillated for 16 h, centrifuged at 1006× g for 20 min); oxidizable fraction (F3, hydrogen peroxide 5 mL, water bath heated to 85 °C, added 5 mL of hydrogen peroxide after 1 h, added 25 mL of 1 mol/L ammonium acetate solution with pH = 2 after 1 h, oscillated for 16 h, centrifuged at 1006× g for 20 min); and residual fraction (F4, digestion with HNO3-HF-HCLO4).

2.4. Plant Growth and Metal Accumulation

The plant samples were washed with tap water and deionized water and then soaked in 20 mmol/L ethylenediaminetetraacetic acid (EDTA) for about 15 min for the removal of heavy metal ions adsorbed on the root surface, and rinsed with deionized water. The samples were divided into the upper part and lower part of the ground. The samples were heated at 105 °C for 30 min, then baked at 70 °C for about 2 days. The samples were pulverized and ground. Plant samples were digested in 5 mL concentrated HNO3 at 180 °C. Then, the mineralized samples were transferred to volumetric flasks, diluted to a final volume of 25 mL with ultrapure water, and filtered through 0.22 µm filters. The filtrate was used for flame atomic absorption analysis to quantify the Pb, Zn, Cu, and Cd contents. The content of malondialdehyde was determined by thiobarbiturate acid [22]. The content of proline was determined by the ninhydrin method, and the total amount of heavy metals in plants was determined by nitric acid digestion/inductively coupled plasma spectroscopy (ICP-OES) (Shimadzu, Kyoto, Japan).
The Cd bioconcentration factors (BCFs) and translocation factors (TFS) were calculated using the following equations [23].
B C F s h o o t = C s h o o t C s o i l
B C F r o o t = C r o o t C s o i l
T F S / R = C s h o o t C r o o t
where Cshoot represents the metal concentration in aboveground tissue or shoots (mg/kg WD), Croot represents the metal concentration in roots (mg/kg WD), and Csoil is the heavy metal concentration in the soil sample (mg/kg).

2.5. Statistical Analysis

Statistical analysis was performed with SPSS 18.0 for Windows (SPSS Inc., Chicago, IL, USA). All values reported are the means of three independent replicates. The data variability indicates the probability of significant differences (p < 0.05). Analysis of variance (ANOVA) was used to analyze the difference between treatments. The results were visualized by Origin Pro 8.0 (Origin Lab Corporation, Northampton, MA, USA).

3. Results

3.1. Soil Properties

Figure 1 reveals the variable soil pH values and organic matter contents in different planting modes due to the action of illite. The addition of illite significantly (p < 0.05) enhanced soil pH and improved soil acidity when compared with the control. The overall performance of soil pH in each treatment with diverse planting patterns was as follows: Single species of Ilex cornuta > No plant > Single species of Epipremnum aureum > Co-cropping of Ilex cornuta and Epipremnum aureum. The difference was not significant when compared to the control group. The application of illite significantly (p < 0.05) reduced the organic matter content in the soil compared to the control. The co-cropping of Ilex cornuta and Epipremnum aureum improved the soil organic matter content by 12.9%. The soil organic matter content when co-cropping Ilex cornuta and Epipremnum aureum was significantly (p < 0.05) higher than when mono-planting two plants.

3.2. Heavy Metal Cd Availability and Fractions

The contents of EDTA-extractable Pb, Zn, and Cu were reduced significantly (p < 0.05) with the application of illite, by 29.8–32.5%, 1.85–5.72%, and 30.0–32.9%, respectively, compared to the control (Figure 2). In the co-cropping mode, the content of EDTA-extractable Cd in the soil was significantly reduced, and there was significant variation compared to single-plant models (p < 0.05), which revealed that a co-cropping model can effectively reduce the content of the EDTA-extractable Cd in the soil. The addition of illite reduced the acid-exchangeable fractions of Pb and Cu by 0.9% and 5.0%, respectively, compared to the control (Figure 3). The co-cropping patterns diminished the acid-exchangeable contents of Pb, Zn, Cu, and Cd compared to single species of two plants. The addition of illite improved the reducible fractions of Pb, Zn, and Cu by 5.4%, 2.1%, and 1.2%, respectively, compared to the control. The contents of Pb, Zn, Cu, and Cd in a reducible state in the co-cropping mode were higher compared to single species of Epipremnum aureum, and they were lower than single species of Ilex cornuta. The application of illite improved the oxidizable fractions of Cu and Cd by 9.0% and 7.0% compared to the control. The oxidizable fractions of Zn, Cu, and Cd were enhanced compared to single species of two plants in the co-cropping mode. The oxidizable fraction content of Pb was decreased. The addition of illite reduced the residual contents of Cd and Zn by 5.0% and 3.5%, respectively, compared to the control. The residual fractions of Pb and Cu were higher than Ilex cornuta in the co-cropping mode when compared with single species of two plants and were lower than single species of Epipremnum aureum. The residual fraction of Zn was higher than in the single-species mode.

3.3. Heavy Metal Content in Plants

The plant Pb contents were recorded in the order of Epipremnum aureum > Ilex cornuta (Figure 4). The contents of Pb and Cu in the roots were higher than in the shoots. The contents of Zn and Cd in the shoots followed a sequence of Ilex cornuta > Epipremnum aureum, while the sequence was Epipremnum aureum > Ilex cornuta in the roots. The content of Zn in Ilex cornuta shoot was lower than in the roots (p < 0.05), irrespective of the planting mode. The contents of Pb, Cu, and Cd in the co-cropping mode were higher than in the single-plant mode. The content of Zn in the shoots was greater in Ilex cornuta with the co-cropping mode than Ilex cornuta in the single-plant mode. In terms of Pb content, there was significant variation between Epipremnum aureum in the co-cropping mode and Epipremnum aureum in the single-plant mode, with a variation of 39.6% recorded. However, there was no significant variation between Ilex cornuta in the co-cropping mode and Ilex cornuta in the single-plant mode. Epipremnum aureum in the co-cropping mode was not significantly different from the single-plant mode. The absorptive capacities of Pb, Cu, and Cd of Epipremnum aureum were significantly stronger than those of Ilex cornuta. The absorptive capacities of Pb, Cu, and Cd in the roots of Ilex cornuta were significantly higher than in the shoots. The absorption capacity of Zn in the roots was lower than in the shoots. The absorption capacities of Pb, Zn, Cu, and Cd in the roots of Epipremnum aureum were obviously more than in the shoota; this indicated that the absorption of Pb, Zn, Cu, and Cd was promoted by Ilex cornuta and Epipremnum aureum in the co-cropping mode.

3.4. Bioconcentration Factor and Translocation Factor of Plants

Under the co-cropping model, the transport ability of Ilex cornuta for Zn was significantly improved, and the transport ability for Cu was reduced (Table 3). There was no significant variation in the transport ability of Epipremnum aureum, which indicated that co-cropping of Ilex cornuta and Epipremnum aureum can promote the transportation of Zn by Ilex cornuta. Table 4 reveals that the Pb enrichment of the two plants in the roots was higher than that in the shoots, by 87.5% and 112%. In the co-cropping mode, cornflower had no significant effect on Pb enrichment; however, Epipremnum aureum shoots and roots were significantly more effective at Pb enrichment, by 107% and 24.3%. The Zn enrichment law of Ilex cornuta is that shoots have higher enrichment than roots, while the rule of Zn enrichment by Epipremnum aureum is that roots have higher enrichment than shoots. In the co-cropping mode, the enrichment ability of Ilex cornuta in shoots is significantly higher than it is in the single-plant mode. This is consistent with the law of the transport coefficient response. The Cu enrichment of two plants is higher in the roots than in the shoots. The Cu enrichment of the roots of two plants is significantly higher than that of single species in the co-cropping mode. There is no significant variation in the enrichment of Cu in the aerial parts of Ilex cornuta under different modes. Cu enrichment in the co-cropping mode is significantly higher than in the single-plant mode. This shows that the co-cropping mode promotes the absorption of Cu in the roots of Ilex cornuta. Cd enrichment in Epipremnum aureum roots is higher than in the shoots. There is no significant difference in Cd enrichment of Epipremnum aureum under different modes. Cd enrichment in the roots was 4.5% higher than in the shoots under an Ilex cornuta monoculture pattern. The concentration of Cd in the co-cropping mode of Ilex cornuta roots was 23.9% higher than that in the shoots. The shoot and root parts of Ilex cornuta in the co-cropping mode had significantly higher Cd accumulation abilities, by 70.1% and 78.7%, than those of cotoneaster in the single-plant mode. This reveals that the co-cropping mode significantly improved the Cd accumulation ability of Ilex cornuta.

3.5. Physiological Processes and Growth Parameters of Plants

Figure 5 exhibits the contents of proline and malondialdehyde in Ilex cornuta and Epipremnum aureum in different planting modes. The proline content of Ilex cornuta acid was higher by 114% than that in the single-plant mode (p < 0.05) in co-cropping. The proline content of Epipremnum aureum was 35.7% (p < 0.05) higher than in the monoculture pattern. The contents of malondialdehyde in Ilex cornuta and Epipremnum aureum were slightly lower in the co-cropping mode than in the single-plant mode, but, overall, the difference was not significant. The contents of malondialdehyde in Ilex cornuta and Epipremnum aureum were reduced by 18.7% and 32.6% in the co-cropping mode compared to the mono-cropping mode. The results revealed the contents of biomass in Ilex cornuta and Epipremnum aureum in different planting modes (Figure 6). The biomasses of Ilex cornuta and Epipremnum aureum shoots in the monoculture mode were 2.45 g/plant and 1.47 g/plant, respectively. The shoot biomasses of Ilex cornuta and Epipremnum aureum in the co-cropping mode were reduced by 22.6% and 44.9%, respectively, compared to the monoculture mode. The root biomasses of Ilex cornuta and Epipremnum aureum were 1.07 g/plant and 0.94 g/plant, respectively, in the monoculture mode. The patterns of change in the stem biomass and root biomass of Ilex cornuta and Epipremnum aureum in the co-cropping mode were decreases of 13.7% and 27.3% compared to the monoculture mode. The accumulation of heavy metals in plants under different treatments was measured to evaluate the effectiveness of the cropping pattern for the elimination of metals from soil (Figure 7). The content of heavy metals accumulated per plant pot indicated that Epipremnum aureum has a higher removal capacity than Ilex cornuta for Pb, Cu, and Cd, at 55.7%, 73.8%, and 35.0%, respectively. However, Epipremnum aureum removed 24.4% less Zn than Ilex cornuta. The co-cropping pattern promoted total accumulations of metals (Pb, Zn, Cu, and Cd) per plant pot of 13.0–75.8%, 11.1–38.2%, 8.4–88.4%, and 27.8–72.5%, respectively, compared to mono-cropping.

4. Discussion

The soil pH and organic matter content are important indicators of soil quality [24,25]. The mobility and availability of heavy metals in soil were significantly affected by soil pH, which can control the adsorption–desorption and precipitation–dissolution of heavy metals in the soil [26,27]. The results revealed that the application of illite significantly raised the soil pH, which is consistent with findings of previous studies [28]. Illite has a high pH, and its application to soil can increase the soil pH, thereby improving soil conditions and promoting plant growth. However, during the growth process, plant roots may secrete organic acids, which could potentially lower the soil pH [29]. The organic matter content in the soil was reduced with the application of illite and after plantation. The organic matter content in the co-cropping mode was higher than that in the single-plant mode, which indicated that co-cropping Ilex cornuta and Epipremnum aureum has a positive effect on soil improvement when compred to the single-plant mode. Co-cropping can improve the soil organic matter and nitrogen contents, with long-term effects leading to further improvements in the soil fertility and productivity of co-cropping systems. Co-cropping can also effectively enhance the soil organic matter content, improved the soil texture, and enhance the soil fertility [30,31].
BCR facilitates the extraction of heavy metals such as Pb, Zn, Cu, and Cd, dividing the occurrence of heavy metals into an acid-exchangeable fraction, reducible fraction, oxidizable fraction, and residual fraction. The acid-exchangeable fraction is most readily absorbed by plants, and the reducible fraction is the easiest form for use by plants, while the oxidizable fraction is less readily accessible to plants [32]. The residual fraction is the form that plants can hardly use, which is almost ineffective for plants [33]. The results indicated that the co-cropping mode can reduce the acid-exchangeable fractions of Pb, Zn, Cu, and Cd in the soil. The addition of clay minerals can affect the microenvironment in the soil and can change the occurrence state of heavy metals [34]. Clay minerals can self-dissolve to produce anions, which will combine with heavy metal cations in the soil for surface adsorption and coordination with ions [35,36], thereby greatly reducing the effectiveness of heavy metals in the soil, changing the bioavailability and mobility of heavy metals, and alleviating heavy metal stress [37]. The results indicated that the application of illite can reduce the content of HCL-extractable heavy metals. The application of different amounts of clay mineral compound modifiers can significantly reduce the content of Cd extracted from diethylene triamine pentaacetic acid (DTPA) in the soil [38], and it can significantly reduce the Cd content in vegetables. In the co-cropping mode, the bioavailable Cd content in the soil was significantly lower compared to single-cropped Ilex cornuta and Epipremnum aureum. It is assumed that plant root exudates can influence the bioavailability of heavy metals, and that the co-cropping model alters the interaction of plant roots, leading to changes in the types of organic acids present in root exudates [39]. Consequently, this affects the bioavailable content of heavy metals in the soil.
Proline and malondialdehyde serve as indicators of plant stress resistance and the extent of damage [40]. Co-cropping can improve the content of proline in Ilex cornuta, which shows that co-cropping can relieve the stresses of heavy metals on Ilex cornuta and can enhance the stress resistance of Ilex cornuta. The co-cropping mode can promote the accumulation of Pb, Cu, and Cd in Ilex cornuta and Epipremnum aureum, which illustrates that co-cropping can promote the absorption of Pb, Cu, and Cd in Ilex cornuta and Epipremnum aureum from soil. Deng et al. found that the co-cropping mode can promote the accumulation of Zn in the shoots of Ilex cornuta [41]. The co-cropping mode can reduce the accumulation of Zn in the roots of Epipremnum aureum. This reveals that co-cropping can promote the absorption of Zn from the soil in the shoots of Ilex cornuta and inhibit the absorption of Zn in the roots of Epipremnum aureum from the soil [29]. Plants can be roughly divided into three types, i.e., the enrichment type, root-hoarding type, and avoidance type, according to the absorption and distribution of heavy metals in plants [42]. Enrichment plants actively absorb and accumulate heavy metals from the soil; heavy metals are concentrated in plant roots in large amounts, and a small amount is transferred to the shoots in root-hoarding plants. Meanwhile, avoiding plants deposit heavy metals on the surface of the root system to resist heavy metals in the plant. The enrichment coefficient and transport coefficient can characterize the ability of a plant to absorb heavy metals from the soil, the migration of heavy metals from the roots to the shoots, and the absorption mechanism and plant types. Ilex cornuta is a Pb and Cu root-hoarding plant and a Zn and Cd enrichment plant. All four types of heavy metals in Epipremnum aureum prove its capacity for root hoarding.

5. Conclusions

Our research findings indicate that under the co-cropping of Ilex cornuta and Epipremnum aureum, the addition of illite significantly increased the soil pH and reduced the bioavailability of Pb, Zn, Cu, and Cd. Co-cropping also increased the soil organic matter content, improved the soil texture, and enhanced the soil fertility. Additionally, co-cropping alleviated the heavy metal stress on Ilex cornuta and Epipremnum aureum, and it enhanced their resistance to adversity. Moreover, co-cropping promoted the translocation of Pb and Cd by Epipremnum aureum, facilitated Cu absorption by Ilex cornuta, and significantly enhanced the Cd enrichment capacity of Ilex cornuta. Therefore, we conclude that under the co-cropping of Ilex cornuta and Epipremnum aureum, the addition of illite can enhance the remediation effectiveness for heavy-metal-contaminated soil in mining areas.

Author Contributions

Conceptualization, Q.L. and W.X.; methodology, D.D.; software, Y.T.; validation, D.D., X.W. (Xili Wang), and Y.L.; formal analysis, Y.L.; investigation, X.W. (Xuqiao Wu); resources, D.L.; data curation, S.G.; writing—original draft preparation, Q.L.; writing—review and editing, W.X.; visualization, S.G.; supervision, X.X.; project administration, X.W. (Xili Wang); funding acquisition, D.L. All authors have read and agreed to the published version of the manuscript.

Funding

This work was supported by grants from the National Natural Science Foundation of China [grant number 32271532] and the National Key Research and Development Program of China [grant number 2023YFD1902900].

Institutional Review Board Statement

No humans or animals were involved in this study.

Data Availability Statement

Data will be made available on request.

Conflicts of Interest

The authors declare no conflicts of interest.

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Agriculture 14 00867 g001
Figure 1. Soil pH (A) and organic matter (B) contents in different planting modes under the action of illite. II = add illite, plant Ilex cornuta; IE = add illite, plant Epipremnum aureum; IIE = add illite, Ilex cornuta and Epipremnum aureum co-cropping system; IN = add illite, without plants; CK = control. Lowercase letters on the bar chart indicate significant differences among different treatments (p < 0.05). All values are presented as mean ± standard error (n = 3).
Figure 1. Soil pH (A) and organic matter (B) contents in different planting modes under the action of illite. II = add illite, plant Ilex cornuta; IE = add illite, plant Epipremnum aureum; IIE = add illite, Ilex cornuta and Epipremnum aureum co-cropping system; IN = add illite, without plants; CK = control. Lowercase letters on the bar chart indicate significant differences among different treatments (p < 0.05). All values are presented as mean ± standard error (n = 3).
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Figure 2. The contents of soil-available Pb (A), Zn (B), Cu (C), and Cd (D) in different treatments. II = add illite, plant Ilex cornuta; IE = add illite, plant Epipremnum aureum; IIE = add illite, Ilex cornuta and Epipremnum aureum co-cropping system; IN = add illite, without plants; CK = control. Lowercase letters on the bar chart indicate significant differences among different treatments (p < 0.05). All values are presented as mean ± standard error (n = 3).
Figure 2. The contents of soil-available Pb (A), Zn (B), Cu (C), and Cd (D) in different treatments. II = add illite, plant Ilex cornuta; IE = add illite, plant Epipremnum aureum; IIE = add illite, Ilex cornuta and Epipremnum aureum co-cropping system; IN = add illite, without plants; CK = control. Lowercase letters on the bar chart indicate significant differences among different treatments (p < 0.05). All values are presented as mean ± standard error (n = 3).
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Figure 3. Distribution of chemical forms of Pb (A), Zn (B), Cu (C), and Cd (D) in different treatments. F1 = acid-exchangeable fraction; F2 = reducible fraction; F3 = oxidizable fraction; F4 = residual fraction. II = add illite, plant Ilex cornuta; IE = add illite, plant Epipremnum aureum; IIE = add illite, Ilex cornuta and Epipremnum aureum co-cropping system; IN = add illite, without plants; CK = control. All values are presented as mean ± standard error (n = 3).
Figure 3. Distribution of chemical forms of Pb (A), Zn (B), Cu (C), and Cd (D) in different treatments. F1 = acid-exchangeable fraction; F2 = reducible fraction; F3 = oxidizable fraction; F4 = residual fraction. II = add illite, plant Ilex cornuta; IE = add illite, plant Epipremnum aureum; IIE = add illite, Ilex cornuta and Epipremnum aureum co-cropping system; IN = add illite, without plants; CK = control. All values are presented as mean ± standard error (n = 3).
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Figure 4. The contents of Pb (A), Zn (B), Cu (C), and Cd (D) in the shoots and roots of plants under different treatments. II = add illite, plant Ilex cornuta; IE = add illite, plant Epipremnum aureum; IIE-I = add illite, Ilex cornuta and Epipremnum aureum co-cropping system, Ilex cornuta in co-cropping; IIE-E = add illite, Ilex cornuta and Epipremnum aureum co-cropping system, Epipremnum aureum in co-cropping. Lowercase letters on the bar chart indicate significant differences among different treatments for the same indicator (p < 0.05). All values are presented as mean ± standard error (n = 3).
Figure 4. The contents of Pb (A), Zn (B), Cu (C), and Cd (D) in the shoots and roots of plants under different treatments. II = add illite, plant Ilex cornuta; IE = add illite, plant Epipremnum aureum; IIE-I = add illite, Ilex cornuta and Epipremnum aureum co-cropping system, Ilex cornuta in co-cropping; IIE-E = add illite, Ilex cornuta and Epipremnum aureum co-cropping system, Epipremnum aureum in co-cropping. Lowercase letters on the bar chart indicate significant differences among different treatments for the same indicator (p < 0.05). All values are presented as mean ± standard error (n = 3).
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Figure 5. The contents of proline (A) malondialdehyde (B) in coltsfoot and scleroderma under different planting modes. II = add illite, plant Ilex cornuta; IE = add illite, plant Epipremnum aureum; IIE-I = add illite, Ilex cornuta and Epipremnum aureum co-cropping system, Ilex cornuta in co-cropping; IIE-E = add illite, Ilex cornuta and Epipremnum aureum co-cropping system, Epipremnum aureum in co-cropping. Lowercase letters on the bar chart indicate significant differences among different treatments (p < 0.05). All values are presented as mean ± standard error (n = 3).
Figure 5. The contents of proline (A) malondialdehyde (B) in coltsfoot and scleroderma under different planting modes. II = add illite, plant Ilex cornuta; IE = add illite, plant Epipremnum aureum; IIE-I = add illite, Ilex cornuta and Epipremnum aureum co-cropping system, Ilex cornuta in co-cropping; IIE-E = add illite, Ilex cornuta and Epipremnum aureum co-cropping system, Epipremnum aureum in co-cropping. Lowercase letters on the bar chart indicate significant differences among different treatments (p < 0.05). All values are presented as mean ± standard error (n = 3).
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Figure 6. Biomasses of plant shoots and roots under different treatments. II = add illite, plant Ilex cornuta; IE = add illite, plant Epipremnum aureum; IIE-I = add illite, Ilex cornuta and Epipremnum aureum co-cropping system, Ilex cornuta in co-cropping; IIE-E = add illite, Ilex cornuta and Epipremnum aureum co-cropping system, Epipremnum aureum in co-cropping. Lowercase letters on the bar chart indicate significant differences among different treatments for the same indicator (p < 0.05). All values are presented as mean ± standard error (n = 3).
Figure 6. Biomasses of plant shoots and roots under different treatments. II = add illite, plant Ilex cornuta; IE = add illite, plant Epipremnum aureum; IIE-I = add illite, Ilex cornuta and Epipremnum aureum co-cropping system, Ilex cornuta in co-cropping; IIE-E = add illite, Ilex cornuta and Epipremnum aureum co-cropping system, Epipremnum aureum in co-cropping. Lowercase letters on the bar chart indicate significant differences among different treatments for the same indicator (p < 0.05). All values are presented as mean ± standard error (n = 3).
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Figure 7. Accumulation of Pb (A), Zn (B), Cu (C) and Cd (D) in plants of different treatments. II = add illite, plant Ilex cornuta; IE = add illite, plant Epipremnum aureum; IIE-I = add illite, Ilex cornuta and Epipremnum aureum co-cropping system, Ilex cornuta in co-cropping; IIE-E = add illite, Ilex cornuta and Epipremnum aureum co-cropping system, Epipremnum aureum in co-cropping. Lowercase letters on the bar chart indicate significant differences among different treatments (p < 0.05). All values are presented as mean ± standard error (n = 3).
Figure 7. Accumulation of Pb (A), Zn (B), Cu (C) and Cd (D) in plants of different treatments. II = add illite, plant Ilex cornuta; IE = add illite, plant Epipremnum aureum; IIE-I = add illite, Ilex cornuta and Epipremnum aureum co-cropping system, Ilex cornuta in co-cropping; IIE-E = add illite, Ilex cornuta and Epipremnum aureum co-cropping system, Epipremnum aureum in co-cropping. Lowercase letters on the bar chart indicate significant differences among different treatments (p < 0.05). All values are presented as mean ± standard error (n = 3).
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Table 1. Basic properties of the soil samples.
Table 1. Basic properties of the soil samples.
Soil SampleValue
pH5.891 ± 0.112
Organic matter (g/kg)20.413 ± 1.265
Total Pb (mg/kg)25,069.346 ± 693.218
Total Zn (mg/kg)1199.087 ± 30.849
Total Cu (mg/kg)432.568 ± 17.392
Total Cd (mg/kg)13.561 ± 0.617
Table 2. Basic properties of the illite samples.
Table 2. Basic properties of the illite samples.
Illite SampleValue
pH8.952 ± 0.365
Organic matter (g/kg)3.439 ± 0.161
Surface area (m2/g)1.037 ± 0.061
Total Pb (mg/kg)0.993 ± 0.042
Total Zn (mg/kg)34.626 ± 1.193
Total Cu (mg/kg)ND
Total Cd (mg/kg)0.136 ± 0.007
ND signifies non-detectable.
Table 3. Translocation factor (TF) of Pb, Zn, Cu, and Cd under different treatments.
Table 3. Translocation factor (TF) of Pb, Zn, Cu, and Cd under different treatments.
TreatmentTFS/R
PbZnCuCd
II0.553 ± 0.051 ab1.360 ± 0.115 a0.569 ± 0.052 a0.951 ± 0.102 a
IE0.384 ± 0.042 c0.452 ± 0.061 b0.224 ± 0.021 c0.616 ± 0.058 b
IIE-I0.477 ± 0.041 bc1.504 ± 0.102 a0.242 ± 0.014 c0.942 ± 0.071 a
IIE-E0.636 ± 0.064 a0.424 ± 0.011 b0.358 ± 0.051 b0.809 ± 0.056 a
TFS/R = translocation factor of root to shoot; II = add illite, plant Ilex cornuta; IE = add illite, plant Epipremnum aureum; IIE-I = add illite, Ilex cornuta and Epipremnum aureum co-cropping system, Ilex cornuta in co-cropping; IIE-E = add illite, Ilex cornuta and Epipremnum aureum co-cropping system, Epipremnum aureum in co-cropping. Lowercase letters on the bar chart indicate significant differences among different treatments (p < 0.05). All values are presented as mean ± standard error (n = 3).
Table 4. Bioconcentration factor (BCF) of Pb, Zn, Cu, and Cd under different treatments.
Table 4. Bioconcentration factor (BCF) of Pb, Zn, Cu, and Cd under different treatments.
TreatmentBCFshootBCFroot
PbZnCuCdPbZnCuCd
II0.008 ± 0.001 c0.149 ± 0.015 b0.013 ± 0.001 b0.535 ± 0.113 c0.015 ± 0.001 c0.111 ± 0014 d0.024 ± 0.005 c0.559 ± 0.051 c
IE0.014 ± 0.001 b0.110 ± 0.016 c0.018 ± 0.002 b0.867 ± 0.123 b0.037 ± 0.004 b0.244 ± 0.004 b0.081 ± 0.007 a1.398 ± 0.012 a
IIE-I0.008 ± 0.001 c0.208 ± 0.017 a0.012 ± 0.003 b0.910 ± 0.135 b0.017 ± 0.002 c0.139 ± 0.014 c0.051 ± 0.010 b0.999 ± 0.221 b
IIE-E0.029 ± 0.001 a0.116 ± 0.011 c0.031 ± 0.005 a1.291 ± 0.228 a0.046 ± 0.005 a0.273 ± 0.020 a0.088 ± 0.009 a1.599 ± 0.256 a
BCFshoot = bioconcentration factor of shoot; BCFroot = bioconcentration factor of root. II = add illite, plant Ilex cornuta; IE = add illite, plant Epipremnum aureum; IIE-I = add illite, Ilex cornuta and Epipremnum aureum co-cropping system, Ilex cornuta in co-cropping; IIE-E = add illite, Ilex cornuta and Epipremnum aureum co-cropping system, Epipremnum aureum in co-cropping. Lowercase letters on the bar chart indicate significant differences among different treatments (p < 0.05). All values are presented as mean ± standard error (n = 3).
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Li, Q.; Tang, Y.; Dong, D.; Wang, X.; Wu, X.; Gul, S.; Li, Y.; Xie, X.; Liu, D.; Xu, W. Remediation of Pb-, Zn-, Cu-, and Cd-Contaminated Soil in a Lead–Zinc Mining Area by Co-Cropping Ilex cornuta and Epipremnum aureum with Illite Application. Agriculture 2024, 14, 867. https://doi.org/10.3390/agriculture14060867

AMA Style

Li Q, Tang Y, Dong D, Wang X, Wu X, Gul S, Li Y, Xie X, Liu D, Xu W. Remediation of Pb-, Zn-, Cu-, and Cd-Contaminated Soil in a Lead–Zinc Mining Area by Co-Cropping Ilex cornuta and Epipremnum aureum with Illite Application. Agriculture. 2024; 14(6):867. https://doi.org/10.3390/agriculture14060867

Chicago/Turabian Style

Li, Qi, Yanxin Tang, Dubin Dong, Xili Wang, Xuqiao Wu, Saima Gul, Yaqian Li, Xiaocui Xie, Dan Liu, and Weijie Xu. 2024. "Remediation of Pb-, Zn-, Cu-, and Cd-Contaminated Soil in a Lead–Zinc Mining Area by Co-Cropping Ilex cornuta and Epipremnum aureum with Illite Application" Agriculture 14, no. 6: 867. https://doi.org/10.3390/agriculture14060867

APA Style

Li, Q., Tang, Y., Dong, D., Wang, X., Wu, X., Gul, S., Li, Y., Xie, X., Liu, D., & Xu, W. (2024). Remediation of Pb-, Zn-, Cu-, and Cd-Contaminated Soil in a Lead–Zinc Mining Area by Co-Cropping Ilex cornuta and Epipremnum aureum with Illite Application. Agriculture, 14(6), 867. https://doi.org/10.3390/agriculture14060867

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