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Article

Phosphate Fertilizers’ Dual Role in Cadmium-Polluted Acidic Agricultural Soils: Dosage Dependency and Passivation Potential

by
Hongyi Liang
1,
Yi Tan
1,
Junhui Yin
2,
Yutao Peng
2,
Mi Wei
2,
Hao Chen
2 and
Qing Chen
1,*
1
Beijing Key Laboratory of Farmland Soil Pollution Prevention and Remediation, College of Resources and Environmental Sciences, China Agricultural University, Beijing 100193, China
2
School of Agriculture, Sun Yat-sen University, Shenzhen 518107, China
*
Author to whom correspondence should be addressed.
Agronomy 2024, 14(10), 2201; https://doi.org/10.3390/agronomy14102201
Submission received: 13 August 2024 / Revised: 11 September 2024 / Accepted: 19 September 2024 / Published: 25 September 2024
(This article belongs to the Section Soil and Plant Nutrition)
Browse Figures
Versions Notes

Abstract

:
Cadmium (Cd) contamination in agricultural soils is a common issue, posing health risks as it enters the human body through the food chain. Commonly used phosphate fertilizers (PFs) not only provide essential phosphorus (P) nutrients to crops but also serve as P-containing materials for immobilizing heavy metals (HMs) like Cd in soils. Therefore, understanding the passivation effects of PFs on soil Cd and their potential influencing factors is crucial for mitigating soil Cd pollution. In this study, the impact of multi-crop applications (75 mg P kg−1, 150 mg P kg−1) of four kinds of PFs on reducing soil Cd toxicity and decreasing Cd accumulation in spinach was investigated. The results indicated that under the low application rate (75.0 mg P kg−1), all PFs could passivate Cd, and CMP demonstrated the most effective passivation of Cd. However, under the high application rate (150 mg P kg−1), the immobilization effect diminished or even activated Cd. Among the different types of PFs, CMP application alleviated soil acidification and significantly reduced soil-available Cd, showing the best performance in promoting spinach growth and Cd inhibition. These results suggest that PF application in Cd-contaminated soils affects spinach growth and Cd accumulation, with soil pH, available phosphorus (AP), and Cd dynamics being crucial; moreover, low-P, micronutrient-rich, alkaline PFs like CMP optimize spinach yields and minimize Cd uptake, and excessive application of soluble PFs decreases pH, increases Cd mobility, and poses health risks, suggesting a need for balanced fertilizer use.

1. Introduction

Heavy metal (HM) pollution of agricultural soils is a major environmental issue affecting food safety and human health [1]. Cadmium (Cd) is a common pollutant in agricultural soils [2]. Due to its strong toxicity and mobility, Cd contamination hinders plant growth, alters the soil microbial community, affects the quality of surface water and shallow groundwater in the surrounding areas, and jeopardizes human health through food chain exposure [3,4,5,6]. Various in situ and ex situ remediation techniques have been employed to address soil Cd contamination [7]. Among them, in situ immobilization is considered an economically efficient and environmentally friendly approach. This method converts highly toxic and mobile Cd into more stable and less bioavailable forms through ion exchange, adsorption, precipitation, and complexation processes [8].
Phosphorus (P)-based immobilizers are promising materials for Cd stabilization in agricultural soils, with the advantages of effective immobilization, high cost-effectiveness, and minimal ecological destructiveness [9]. Among them, phosphorus fertilizer (PF), as a special class of P-containing materials, applied to HM-polluted soils can not only reduce soil Cd pollution to a certain extent [10,11], but also meet the demand for P for crop growth. Research indicates that PFs can immobilize soil Cd through mechanisms such as complexation, ion exchange, and precipitation [12,13]. Still, there are many types of PFs, resulting in uncertainty in their interaction effects with Cd in soil. For example, monoammonium phosphate (MAP) is acidic and tends to cause a decrease in soil pH after addition to the soil, potentially activating soil Cd [14]; meanwhile, CMP is alkaline and contains calcium (Ca), magnesium (Mg), and other ions, which tend to compete with Cd in the soil, thus reducing Cd uptake by crops [15]. The amount of PF applied also affects the passivation effect. It was found that as the input of CSP increased, the effectiveness of Cd in the corresponding treatment decreased [16]. In addition, environmental conditions can also influence the effectiveness of PFs in immobilizing Cd, leading to varied outcomes in polluted soils [15,17]. For example, the input of organic PF [15] and water-soluble PF (diammonium phosphate) reduced eutectic Cd levels in alkaline soils [18].
However, the unnecessarily application of PF reduces soil Cd availability and Cd plant uptake. For instance, it was reported that hog manure and diammonium phosphate application instead increased Cd in the active state under non-alkaline soil conditions [17,19]. This may be because under alkaline soil conditions (pH > 7), Cd can precipitate with uptake of anions such as SO42−, CO32−, OH−, and HPO42− [20]. Al-Faiyz et al. [21] also evaluated the effects of various levels of superphosphate on tomato, lettuce, and radish plants in loamy sand soil in Saudi Arabia, and the results implied that increasing levels of P2O5 significantly raised Cd concentrations in radish leaves, with levels rising from 0 g P2O5 m−2 to 72 g P2O5 m−2, while Cd levels in roots remained consistent, indicating greater Cd accumulation in leaves likely due to active transport. Further, it is noteworthy that under acidic soil conditions, PF application could enhance the uptake of calcium, magnesium, and cadmium ions by crops through non-selective ion channels [22]. Herein, parameters that affect soil ion activity, such as soil cation exchange capacity (CEC), soil organic matter (SOM) content, and duration, after PCM inputs could affect Cd uptake to some extent [23,24].
Considering their solubility and release mechanisms, PFs are categorized into three types: water-soluble phosphates, acid-soluble phosphates, and P-containing organic fertilizers [25,26]. Water-soluble phosphates, such as MAP, potassium dihydrogen phosphate, and SP, dissolve readily in water and are quickly absorbed by plant roots [27]. Acid-soluble phosphates dissolve in organic acids present in the soil or acids secreted by roots, gradually releasing nutrients, and include compounds like metal ammonium phosphates and partially acidified phosphate rocks [28]. The P in P-containing organic fertilizers exists partly in the form of inositol hexaphosphate in some organic fertilizers. In general, inorganic PFs reduce the soil’s Cd availability mainly by changing the soil pH, and promoting the occurrence of ion exchange, surface complexation, and precipitation. The input of organic PFs increases the adsorption sites of Cd. It reduces the effective state of Cd, but the input of PFs also leads to a decrease in soil pH and the disadvantage of bringing Cd into the soil. Studies on the passivation effect of PFs on soil HMs usually focus only on the effect of different dosages of the fertilizers [14,18]. Since different types of PFs have different passivation effects and mechanisms on Cd in soil, two water-soluble and two acid-soluble PFs (AMP, MAP, CMP, and CSP) were selected for the experimental study.
Spinach (Spinacia oleracea L.) is a widely cultivated vegetable, commonly consumed by people due to its high nutritional content and short growth cycle. However, spinach is sensitive to HMs and can exhibit a response to Cd stress within 2–4 weeks, which makes it an excellent candidate for studying the effects of Cd pollution and exploring the potential benefits of remediation materials [29,30]. Given the common practice of continuous cropping in traditional greenhouse cultivation, this study designed a multi-cropping pot experiment to simulate traditional cultivation patterns. Based on previous research [26], different types and input levels of phosphorus fertilizers (PFs) were applied to evaluate their effectiveness in remediating acidic cadmium (Cd)-polluted soils and their impact on reducing Cd uptake by spinach.
The research objectives are threefold: (1) to compare and analyze the efficiency and mechanisms of these PFs in immobilizing Cd in acidic soil; (2) to elucidate the influence of PFs on the reduction in available Cd and its subsequent uptake by spinach; and (3) to investigate the underlying reasons for the variability in the effectiveness of PFs in controlling Cd levels in acidic soils. This comprehensive approach aims to provide a deeper understanding of the factors influencing the performance of PFs in Cd remediation and offer insights into optimizing their use for enhanced soil health and crop safety. This investigation aims to contribute to the development of sustainable and effective strategies for managing Cd pollution in farmland, thereby enhancing crop productivity and ensuring food safety.

2. Materials and Methods

2.1. Soil

Acidic Cd-polluted soil (0–20 cm) was collected from farmland near Zhaoyuan (37°21′40.00″ N, 120°23′55.70″ E) in Shandong Province, China [31]. The soil samples were immediately transferred to the laboratory, air-dried, and ground to pass through 20-mesh and 100-mesh sieves before being stored in plastic bags. The soil’s field water-holding capacity was 36.5% and the clay, silt, and sand particle contents were 0.5%, 76.0%, and 23.5%, respectively. The soil’s texture was loamy sand, classified as anthrosols according to the Food and Agriculture Organization of the United Nations (FAO) [32]. The soil had a pH of 6.34, electrical conductivity (EC) of 125 μS cm−1, soil organic matter of 16.5 g kg−1, alkaline hydrolyzable nitrogen of 145 mg kg−1, available phosphorus of 49.6 mg kg−1, and available potassium of 232 mg kg−1. The total Cd and DTPA-Cd contents in the soil were 3.79 mg kg−1 and 1.02 mg kg−1, respectively.

2.2. Amendments and Plant

AMP and MAP (EKEAR Bio@Tech Co., Shanghai, China) are analytically pure reagents with ≥99% active ingredients; CMP and CSP (Hualan Chemical Technology Co., Shanghai, China) are commercial compound fertilizers. The properties of all P-containing fertilizers are shown in Table 1. Spinach seeds (Spinacia oleracea L.) were purchased from Harim Seeds Co., Ltd (Tianjin, China).

2.3. Experimental Design

A pot experiment was performed with 5 treatments: (1) control (CK); (2) monoammonium phosphate (MAP); (3) calcium superphosphate (CSP); (4) ammonium magnesium phosphate (AMP); and (5) calcium magnesium phosphate (CMP). Each treatment was replicated thrice and placed randomly in a greenhouse at China Agricultural University (40°0′54″ N, 116°21′0.72″ E). In each pot, 1950 g of contaminated soil was mixed with different PFs (75.0 mg P kg−1 of PF was applied as per the inputs in Table S1), and 100 mg N kg−1 (applied urea (Yatai Chemical Co., Shanghai, China)) and 100 mg K kg−1 (applied potassium sulfate (Comeo Chemical Reagent Co., Tianjin, China) were applied according to the standard recommendations for commercial fertilizers. (Note: In treatments 2 and 4, there was additional carryover of N in the P-containing material; after calculations, the N was reduced to the amount needed for urea application, maintaining a total of 100 mg N kg−1) [33]. After mixing, some water was added to moisten the soil, maintaining 60.0% of its field holding capacity (soil field holding is 36.5%, which equates to 438 cm3 of water per 2000 g of soil), and incubated for 7 d in the greenhouse.
Disinfected spinach seeds (10 per pot) were sown on the surface of the pre-cultivated soil (1950 g), covered with an additional 50.0 g of soil, irrigated with distilled water to maintain soil water content at 60% of field water-holding capacity, and the weight of each pot was recorded [34]. After germination, plastic films were removed, and 4 seedlings were interplanted per pot [33]. During cultivation, pots were weighed and watered every day. After 30 days, soil (500 g) and plant samples were collected, and the remaining soil (1500 g) was used for a second cultivation cycle with the addition of 75 mg P kg−1 of the corresponding PF. The second round of soil cultivation, spinach planting, and daily management were consistent with the first round.

2.4. Sampling and Chemical Analysis

During sampling, shoots and roots were carefully separated and washed with distilled water for further analysis. Potting soil was sampled by removing plant roots and other material from it, air dried, and then ground, sieved, and mixed well; 150 g of soil sample was then taken and stored for analysis.
pH was analyzed in 1:2.5 (w:v) ratios using a pH meter (pH500, Shanghai Thunder Magnetic Instrument Co., Shanghai, China), while EC was analyzed in a 1:5 (w:v) ratio using an EC meter (DDSJ-308A, INESA Scientific Instrument Co., Shanghai, China) [35]. Available P (AP) in soil was leached using CaCl2 and NaHCO3, respectively, to determine soil CaCl2-P and Olsen-P [36,37]. Available potassium (AK) was extracted using 1 M NH4OAc and measured with a flame photometer (AP-1200, Precision Instrument Co., Shanghai, China). The soil alkali-hydrolyzable nitrogen was measured with the alkaline hydrolysis diffusion method, and the soil organic matter was determined by the potassium dichromate volumetric method. The DTPA (pH 7.3, 0.1 M TEA, 0.01 M CaCl2, 0.005 M DTPA) was applied to extract the available content of Cd and measured by inductively coupled plasma atomic emission spectroscopy (ICP-OES; Avio 200, Perkin Elmer, Waltham, MA, USA) [38]. Cd fractionation was determined using the Bureau Communautaire de Référence (BCR) sequential extraction method [39], as detailed in Table S2.
The plant parts were packed into marked envelopes and put into the oven at 105 °C to remove the green, and then dried for 1 h at 65 °C to obtain dry weights, which were then analyzed. Then, 0.2 g samples were ground in a stainless-steel grinder, sieved (0.15 mm), and then digested with 8 mL concentrated HNO3. The metal concentrations in the digested samples were analyzed using inductively coupled plasma optical emission spectroscopy (ICP-OES) [40].

2.5. Statistical Analysis

The mean and standard deviations of 3 replicates of experimental data were taken, and all the data were analyzed using SPSS statistical 27.0 software (IBM Co., Armonk, NY, USA). Duncan’s multiple range tests (p < 0.05) were carried out using SPSS 27.0 to test the significance of the treatment effects on every measurement indicator, and the significance level was set at p < 0.05. The Shapiro–Wilk test was employed to assess the normality of the data, followed by an analysis of variance (ANOVA). Figures were visualized utilizing Origin 2024b (OriginLab Co., Northampton, MA, USA).

3. Results and Discussion

3.1. Changes in Soil Physicochemical Properties

Figure 1a shows that in the first batch of pot experiments, the control soil had a pH of 6.17. The application of acidic PFs (MAP, SP, AMP) significantly lowered the soil pH (p < 0.05). In contrast, the alkaline PF (CMP) increased the soil pH to 6.23. Compared to the control (392 μS cm−1), SP significantly increased the soil EC value (618 μS cm−1) (p < 0.05), while other PFs (MAP: 354 μS cm−1; AMP: 433 μS cm−1; CMP: 336 μS cm−1; commercial organic fertilizer: 393 μS cm−1) showed no significant difference from the control (Figure 1b). In the second batch of pot experiments, the trends in soil pH and EC changes were consistent with the first batch’s results.
The change in soil pH is related to the acidity and solubility of the applied PFs [25]. MAP and SP are water-soluble PFs with high solubility in soil solution, leading to the release of more acidic ions and a decrease in soil pH. The ammonium ions carried by MAP can significantly lower the soil pH. Both MAP and CMP are acid-soluble phosphorus fertilizers, thus their effect on changing soil pH is not substantial. Compared with the first crop test, the second crop of various types of PF inputs led to an increase in soil pH due to the replacement of hydroxyl groups by anions brought in by the PF. Regarding the change in soil EC, CSP significantly increased soil EC due to the introduction of Ca ions and its good solubility properties [41]. Although MAP is a water-soluble PF, it has no significant effect on soil EC because its cation is ammonium ion. The two groups of treatments, AMP and CMP, required a certain time to decompose and mineralize after being put into the soil, which in turn resulted in little change to the soil EC.
The data on soil AP indicate that all treatment groups with added PFs, except the control (CK), showed an increase in soil AP content. Compared to the first batch of pot experiments, the second batch showed a significant increase in soil CaCl2-P content with the application of MAP and SP, reaching 2.76 and 2.74 mg kg−1, respectively (Figure 1c). Additionally, in the second batch, all four types of PFs significantly increased soil Olsen-P content to 85.4, 73.8, 49.7, and 66.6 mg kg−1, respectively (p < 0.05) (Figure 1d).
The level of AP in soil is related to the solubility of the applied PFs. Compared to the control (CK), the application of MAP and SP significantly increased soil CaCl2-P and Olsen-P due to their good water solubility [37]. Over time, acid-soluble PFs such as AMP and CMP also significantly increased soil Olsen-P content in the second batch of experiments [42]. CaCl2-P primarily indicates the water-soluble P content in the soil, explaining the significant increase in CaCl2-P in treatments with water-soluble fertilizers (MAP and SP) and the relatively smaller increase in treatments with acid-soluble fertilizers (AMP and CMP) [43]. Additionally, pH also influences the AP in the soil. The results indicated that the application of MAP and CSP decreased soil pH and significantly increased the AP content in the soil. Applying AMP and CMP had opposite effects on pH and AP (Figure 1). These findings do not align with the common research outcomes regarding the impact of pH on AP [44]. This discrepancy may be due to the more pronounced fixation of phosphorus by Ca and Mg under the conditions of AMP and CMP application, which might obscure the positive effect of increased pH on reducing iron (Fe) and aluminum (Al) ions, thereby enhancing P availability [45]. The acidification effect induced by MAP and CSP themselves could potentially increase their solubility, thereby increasing the content of AP [46].

3.2. Available Cd and Classification of BCR Fractions of Cd

In the first batch of pot experiments, compared to the control (0.998 mg kg−1), the application of MAP (0.969 mg kg−1), SP (1.04 mg kg−1), and AMP (0.875 mg kg−1) did not significantly affect the soil DTPA-Cd content (p > 0.05). However, CMP (0.655 mg kg−1) reduced the soil DTPA-Cd. In the second batch of experiments, the immobilization effect of all PFs weakened, and some even exhibited an activation effect on Cd (Figure 2a).
The detection and analysis of various types of changes in soil Cd components was performed to further understand the influence of different types of PF inputs on the potential effects of soil Cd. In this paper, four types of soil Cd fractions were determined using the BCR continuous leaching method, namely: the acid-extractable state, reducible state, oxidizable state, and residual state of Cd (Figure 2b,c; Table S3).
In the first batch of pot experiments, compared to the control, the application of MAP increased the proportion of reducible Cd by 8.0% and decreased the proportion of residual Cd by 7.0%. SP increased the proportions of acid-extractable and reducible Cd by 3.0% and 4.0%, respectively, while reducing residual Cd by 7.0%. AMP reduced the proportion of acid-extractable Cd by 8.0%, increased reducible Cd by 6.0%, and increased residual Cd by 3.0%. CMP decreased the proportion of acid-extractable Cd by 6.0%, increased reducible Cd by 6.0%, and slightly increased residual Cd by 1.0%. In the second batch of experiments, all PFs (MAP, SP, AMP, and CMP) increased the proportion of acid-extractable Cd, reaching 6.0%, 6.1%, 4.1%, and 5.9%, respectively.
Overall, acid-soluble PFs (such as AMP and CMP) exhibited better immobilization effects on Cd, likely because these fertilizers convert acid-soluble Cd into reducible and residual forms [14]. At low P application rates (75 mg P kg−1), the immobilization effect is mainly related to the properties of the fertilizers themselves. In the first batch of pot experiments, the application of MAP and SP caused the conversion of residual Cd to reducible Cd, leading to overall Cd activation in the soil and increased pollution risk, despite no significant change in acid-extractable Cd compared to the control. Conversely, the application of acid-soluble PFs such as AMP and CMP resulted in the conversion of acid-extractable Cd to reducible and residual Cd, aligning with previous studies showing that acid-soluble fertilizers like hydroxyapatite convert acid-soluble Cd into more stable forms [14]. Studies have shown that adding Ca and Mg to plant nutrient solutions can reduce Cd accumulation in rice [47]. In this experiment, the Ca2+ and Mg2+ from AMP and CMP antagonized Cd in the soil solution, reducing its bioavailability and plant uptake [48]. Additionally, soil pH is an important factor affecting the available Cd content. Previous research has indicated that alkaline soil conditions (pH > 7) promote the precipitation of HMs with anions such as SO42−, CO32−, OH−, and HPO42−, thus reducing available Cd. CMP slightly increased soil pH, fixing some Cd through a liming effect [20,49]. Although SP also introduced Ca ions, its application lowered soil pH, resulting in no significant difference in the overall immobilization effect compared to the control.
At a moderate application rate (150 mg P kg−1), the increased P input may cause phosphate ions to replace the surface hydroxyl groups coordinating with Cd. Since Cd3(PO4)2 has a much higher solubility compared to Cd(OH)2, this substitution can release Cd into the soil solution, leading to an activation effect on Cd. However, the specific mechanisms behind this phenomenon require further investigation [50].

3.3. Changes in Spinach Biomass and Cd Enrichment

Compared to the control, all PF treatments significantly increased both the dry and fresh weights of spinach to some extent (p < 0.05) (Figure 3a,b). This is likely due to the addition of P, which provided essential nutrients early in the growth phase, promoting root development and laying a solid foundation for later growth [51,52]. Additionally, the introduction of Ca and Mg through SP and CMP not only supplemented these micronutrients but also may have reduced Cd toxicity in spinach by competing with Cd2+ for uptake through root cell membranes and subsequent transport within the plant [53]. Furthermore, the application of CMP also raised soil pH and reduced acid stress. Consequently, in consecutive experiments, CMP significantly enhanced spinach biomass (Figure 3b) [54,55].
In the first batch of pot experiments, the Cd content in spinach across treatments was as follows: 47.6, 43.3, 66.7, 40.7, and 22.6 mg kg−1. The results from the second batch of experiments were generally consistent with those from the first batch (Figure 3c). Compared to the control, SP significantly increased the Cd content in spinach, while CMP significantly reduced it (p < 0.05). Other treatments showed no significant change compared to the control. Cd levels in spinach were associated with soil pH, spinach biomass, and the type of PF used. SP application lowered soil pH, reduced the proportion of residual Cd in the soil, increased the proportion of reducible Cd, and consequently increased the effective Cd content in the soil, thereby elevating the Cd content in spinach. PF application facilitated spinach growth and enhanced its ability to absorb mineral nutrient ions [56], thereby increasing its Cd accumulation potential. In contrast, CMP significantly lowered the effective Cd content in the soil, reduced soil pH, and through the antagonistic effects of Ca2+, Mg2+, and the adsorption of Cd by acid-soluble PFs, significantly decreased the Cd content in crops.

3.4. Correlation Matrix and SEM Interpretation of Cd Content in Spinach

The Pearson correlation coefficients presented in Figure 4a reveal that soil pH was strongly negatively correlated with Olsen-P and CaCl2-P, which may be related to the properties of PF itself (acidity, solubility with alkali metal ions). Additionally, pH is strongly negatively correlated with DTPA-extractable Cd and positively correlated with residual Cd, consistent with existing knowledge [57]. The dry weight of spinach is strongly positively correlated with soil Olsen-P and CaCl2-P, indicating that the growth of spinach is primarily influenced by AP and essential micronutrients such as Ca and Mg. The correlation coefficients between spinach dry weight and soil DTPA-Cd and acid-extractable Cd are 0.033 and 0.133, respectively, indicating that Cd contamination did not significantly affect spinach growth under the experimental conditions. Soil pH is strongly negatively correlated with both Olsen-P and CaCl2-P, likely due to the acidic nature of the PFs used. This underscores the role of PF application, particularly at low doses, in affecting soil pH, which is crucial for the immobilization effects of P. Furthermore, spinach Cd content is strongly positively correlated with both DTPA-extractable and acid-extractable Cd. Levels of AP (Olsen-P, CaCl2-P) are strongly and very strongly negatively correlated with residual Cd, likely due to the pH decrease caused by soluble PF application, which facilitates the conversion of residual Cd to more mobile forms [58]. Additionally, phosphate ions may replace surface hydroxyl groups coordinated with Cd, given the high solubility of Cd3(PO4)2, thereby activating Cd as a result of PF application [59].
Overall, at low P application rates, the effectiveness of PFs is primarily influenced by their intrinsic properties. The biomass of spinach is mainly determined by the P and micronutrients introduced by the fertilizer, but its Cd accumulation is primarily affected by the levels of available Cd in the soil. All PF applications can increase the essential nutrients in the early stage of spinach growth and play a role in growth promotion. However, water-soluble phosphates were prone to causing a decrease in pH, increasing the available Cd, and leading to an increase in Cd accumulation in spinach under the corresponding treatments, which was not conducive to the safe utilization of the crop. Therefore, in practical spinach production contexts, the use of CMP, which is alkaline and rich in micronutrients, is recommended. This approach not only ensures high spinach yields but also reduces the transport of Cd from the soil to the spinach. Additionally, acid-soluble PFs can effectively supply P over the long term, thereby reducing P loss from agricultural systems.
To verify the inferences from the experiments, we also performed SEM analysis to evaluate the direct and indirect effects of pH, EC, CaCl2-P, DTPA-Cd, and biomass on Cd content in spinach (Figure 4b). The results showed that soil CaCl2-P had a significant negative effect on the biomass of spinach and soil DTPA-Cd (Biomass SPC = 0.475, DTPA-Cd SPC = 0.466, p < 0.05). DTPA-Cd had a significantly positive effect on Cd content in spinach (SPC = 0.397 for Cd content in spinach, p < 0.05). This result indicates that increasing the application of PF raises the concentration of soluble P, which promotes spinach growth but also increases the available Cd content in the soil. This, in turn, enhances the uptake of Cd by spinach, thereby increasing health risks associated with Cd bioavailability (Figure 4).
Notably, pH had a relatively small effect on DTPA-Cd (SPC = −0.215 for Cd, p > 0.05) in our study, indicating that under conditions of high PF application, pH may not be a primary factor in activation of Cd. Additionally, EC did not significantly affect DTPA-Cd (SPC = −0.062, p > 0.05), and this result was consistent with our previous inference in this study. For instance, despite the increased EC from high CMP application, it did not promote HM immobilization, indicating that the process of immobilizing HM in the soil is complex and influenced by multiple factors.

3.5. Practical Application of PF in Cd-Contaminated Farmland

In Cd-contaminated agricultural soils, the application of PFs must consider not only the immobilization effects of these fertilizers on soil Cd but also their effects on crop growth, the inhibition of HM absorption, and the prevention of secondary pollution. High P input can effectively immobilize soil Cd pollution but may also cause other environmental issues, as referenced in related studies [26]. At moderate P application levels, although there is some increase in spinach biomass compared to low input levels, this increase is not significant, and it may lead to an increased proportion of acid-extractable Cd in the soil, promoting Cd accumulation in spinach and posing health risks. Therefore, in the cultivation of Cd-polluted fields, it is advisable to use a suitable low-P input. Regarding P types, while water-soluble PFs can quickly provide readily available P for spinach, they may not effectively immobilize bio-available Cd in the soil, potentially leading to Cd accumulation in crops [60]. Although large P applications can immobilize soil Cd, they can also cause other environmental problems, such as P resource waste and eutrophication of water bodies [61,62]. Acid-soluble PFs, such as CMP, effectively immobilize bioavailable Cd, provide essential P to crops, and their controlled release reduces the risk of P loss [25]. Additionally, the nutrients like Ca2+ and Mg2+ introduced by these fertilizers promote crop growth and compete with soil Cd2+, effectively limiting the accumulation of HMs like Cd in crops.

4. Conclusions

The results confirmed that at a low phosphorus fertilizer application rate (75 mg P kg−1), the inherent characteristics of different PFs were the primary factors influencing the passivation effect. Among these, acid-soluble PF (CMP) significantly increased soil pH, reduced DTPA-extractable Cd content, and decreased Cd accumulation in spinach, demonstrating a markedly superior immobilization effect compared to water-soluble PFs (MAP, CSP). However, at medium input levels (150 mg P kg−1), the immobilization effects of all four fertilizers diminished. Among the tested fertilizers, CMP exhibited the best Cd immobilization and growth-promoting effects in weakly acidic Cd-contaminated silt loam soil. It is recommended that in actual spinach production, alkaline phosphorus fertilizers rich in micronutrients be selected. In this paper, the experiments were conducted in pots, but in actual production process, whether in greenhouses or open fields, soil Cd changes after PF input are more complex, so comparisons of experimental results from field experiments involving different soil conditions and different planting crops are needed to obtain a more in-depth understanding of the impact of PF on the effects of Cd in farmland soils.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/agronomy14102201/s1, Table S1: Experimental treatment and phosphorus fertilizer input; Table S2: Continuous extraction steps of different forms of cadmium in soil by BCR method; Table S3: Changes of cadmium components in soil BCR classification after application of different phosphorus fertilizers; Table S4: Pearson correlation coefficient among the indexes of soil spinach system.

Author Contributions

Conceptualization, Y.T.; software, H.L. and Y.T.; validation, J.Y. and H.C.; formal analysis, H.L.; resources, Q.C.; data curation, H.L. and Y.T.; writing—original draft preparation, H.L.; writing—review and editing, Y.P., J.Y. and M.W.; visualization, H.L. and Y.T.; supervision, Q.C.; funding acquisition, Q.C. and Y.P. All authors have read and agreed to the published version of the manuscript.

Funding

This work was supported by the China Agriculture Research System (CARS-24-B15); the National Natural Science Foundation of China (No. 42207015); the National Natural Science Foundation of China (No. 42007047); Fundamental Research Funds for the Central Universities, Sun Yat-sen University (23qnpy40); and Research Funding for post-doctorates coming to Shenzhen (szbo202207).

Data Availability Statement

The original contributions presented in the study are included in the article; further inquiries can be directed to the corresponding author.

Conflicts of Interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

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Figure 1. Changes in soil physicochemical properties (pH (a), EC (b), CaCl2-P (c) and Olsen-P (d)) after application of different phosphorus fertilizers (CK: control; MAP: monoammonium phosphate; CSP: calcium superphosphate; AMP: ammonium magnesium phosphate; CMP: calcium magnesium phosphate). Different letters indicate significant differences between treatments (p < 0.05).
Figure 1. Changes in soil physicochemical properties (pH (a), EC (b), CaCl2-P (c) and Olsen-P (d)) after application of different phosphorus fertilizers (CK: control; MAP: monoammonium phosphate; CSP: calcium superphosphate; AMP: ammonium magnesium phosphate; CMP: calcium magnesium phosphate). Different letters indicate significant differences between treatments (p < 0.05).
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Figure 2. Changes in soil DTPA-Cd (a) and Cd components in soil BCR classification ((b) the first batch of pot experiments; (c) the second batch of pot experiments) after application of different phosphorus fertilizers (CK: control; MAP: monoammonium phosphate; CSP: calcium superphosphate; AMP: ammonium magnesium phosphate; CMP: calcium magnesium phosphate). Different letters indicate significant differences between treatments (p < 0.05).
Figure 2. Changes in soil DTPA-Cd (a) and Cd components in soil BCR classification ((b) the first batch of pot experiments; (c) the second batch of pot experiments) after application of different phosphorus fertilizers (CK: control; MAP: monoammonium phosphate; CSP: calcium superphosphate; AMP: ammonium magnesium phosphate; CMP: calcium magnesium phosphate). Different letters indicate significant differences between treatments (p < 0.05).
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Figure 3. Illustration of spinach samples (a), changes in spinach dry weight (b), and Cd content in spinach under each treatment (c) (CK: control; MAP: monoammonium phosphate; CSP: calcium superphosphate; AMP: ammonium magnesium phosphate; CMP: calcium magnesium phosphate). Different letters indicate significant differences between treatments (p < 0.05).
Figure 3. Illustration of spinach samples (a), changes in spinach dry weight (b), and Cd content in spinach under each treatment (c) (CK: control; MAP: monoammonium phosphate; CSP: calcium superphosphate; AMP: ammonium magnesium phosphate; CMP: calcium magnesium phosphate). Different letters indicate significant differences between treatments (p < 0.05).
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Figure 4. Pearson correlation coefficients among the indices of the soil–spinach system (a) (“*” indicates that Pearson correlation is medium correlation; “**” indicates strong correlation; “***” indicates strong correlation) and SEM showing the direct and indirect effects of pH, EC, CaCl2-P, DTPA-Cd, and biomass on Cd content in spinach (b). (SEM: Red arrows represent positive effects, and blue arrows represent negative effects, respectively; numbers above the arrows represent the standardized path coefficient (SPC); dotted lines represent p ≥ 0.05; solid lines represent p < 0.05).
Figure 4. Pearson correlation coefficients among the indices of the soil–spinach system (a) (“*” indicates that Pearson correlation is medium correlation; “**” indicates strong correlation; “***” indicates strong correlation) and SEM showing the direct and indirect effects of pH, EC, CaCl2-P, DTPA-Cd, and biomass on Cd content in spinach (b). (SEM: Red arrows represent positive effects, and blue arrows represent negative effects, respectively; numbers above the arrows represent the standardized path coefficient (SPC); dotted lines represent p ≥ 0.05; solid lines represent p < 0.05).
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Table 1. Physicochemical properties of tested phosphorus fertilizers.
Table 1. Physicochemical properties of tested phosphorus fertilizers.
pHTotal P
(g kg−1)		Total Nitrogen
(g kg−1)		Total Potassium
(g kg−1)		Organic Matter
(g kg−1)		Cd
(mg kg−1)
Ammonium magnesium phosphate (AMP)6.00126102NDNDND
Monoammonium phosphate (MAP)4.50267122NDNDND
Calcium magnesium phosphate (CMP)7.9749.7NDNDNDND
Calcium superphosphate (CSP)2.5052.4NDNDNDND
Note: ND means none detected.
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Liang, H.; Tan, Y.; Yin, J.; Peng, Y.; Wei, M.; Chen, H.; Chen, Q. Phosphate Fertilizers’ Dual Role in Cadmium-Polluted Acidic Agricultural Soils: Dosage Dependency and Passivation Potential. Agronomy 2024, 14, 2201. https://doi.org/10.3390/agronomy14102201

AMA Style

Liang H, Tan Y, Yin J, Peng Y, Wei M, Chen H, Chen Q. Phosphate Fertilizers’ Dual Role in Cadmium-Polluted Acidic Agricultural Soils: Dosage Dependency and Passivation Potential. Agronomy. 2024; 14(10):2201. https://doi.org/10.3390/agronomy14102201

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Liang, Hongyi, Yi Tan, Junhui Yin, Yutao Peng, Mi Wei, Hao Chen, and Qing Chen. 2024. "Phosphate Fertilizers’ Dual Role in Cadmium-Polluted Acidic Agricultural Soils: Dosage Dependency and Passivation Potential" Agronomy 14, no. 10: 2201. https://doi.org/10.3390/agronomy14102201

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