Effects of biosolid biochar on crop production and metal accumulation through a rice-wheat rotation system in fields

ABSTRACT

Biosolid-borne heavy metals are the main concern in soils. Therefore, the effects of biosolid biochar application in soils were evaluated in our study through a rice-wheat rotation in fields. The results showed that after the application of biosolid biochar, soil organic matter (SOM), soil pH, and soil total heavy metal concentrations (Cd, Zn, Cu, and Pb) were significantly increased. But the CaCl₂ extracted metals concentrations were decreased, and no significant differences in metal concentrations of soil deeper layers (20–100 cm) were found among different treatments. The Cd, Zn, Cu, and Pb concentrations in rice decreased by 13.2%, 37.0%, 9.92%, and 63.0%, respectively, and the concentrations of Cd, Zn, Cu, and Pb in wheat decreased by 20.85%, 19.7%, 48.6%, and 23.6%, respectively, compared with the control treatment. Biosolid biochar can decrease metal availability in soils and increase crop production in fields, thus is suggested to use in fields.

KEYWORDS:

• Biosolid biochar
• rice
• wheat
• metal accumulation
• crop production

1. Introduction

Biosolids are the treatment of sewage sludge, which contains a wide variety of nutrients, heavy metals, pesticides, other chemicals, and hormones [1,2]. It is estimated that the annual output of biosolids has been growing rapidly, with an average annual growth rate of 16.82% in China, and in 2016, the annual output of biosolids is over 4,800,000,000 [3]. In 2025, China’s annual biosolid production will exceed 90 million tons. Globally, by 2050, 17.5 × 10⁷ tons in 1 year of biosolids are produced at a rate of 50 g⁻¹ people⁻¹ day [4]. Therefore, a scientific, effective, and sustainable sludge disposal method is urgently needed.

The application of biosolids in agriculture has been widely used. In the United States, more than 5 million biosolids are produced annually and approximately 60% are applied in agriculture [5]. However, the safety of the pollutants released into the environment through biosolids is a matter of concern, especially heavy metals [2,6,7]. Heavy metals in sludge are stable and can accumulate in the human body through food chain transmission, resulting in serious damage to human health. Li et al. [8] did a 10- years field study and found that the application of biosolids significantly increases soil total metals like cadmium (Cd), zinc (Zn), copper (Cu), and lead (Pb) in soils. Wang and Zhou [9] also found that biosolids can increase Cd concentration in soil and rice grains, and lead to the migration of Cd into the soil profile. Heavy metals in biosolids have become the primary limiting factor for land use. According to the Chinese control standards of pollutants in sludge for agricultural use, the maximum limit values of Cd, Zn, Cu, and Pb concentrations are 3, 1200, 500, and 300 mg kg⁻¹, respectively (GB4284–2018). Therefore, methods should be taken to reduce the biosolid-borne heavy metals before their application in soils.

Pyrolysis of biosolids to produce biochar has been a new trend for the application of biosolids, which could reduce the volume of biosolids, preserve the valued products from biosolids, and decrease the impacts on the environment. Now it has been used as water and soil amendments, catalysts, and energy storage and generation materials [2,10]. Studies found that the application of biosolid biochar in soils could increase soil phosphorus (P), nitrogen (N), potassium (K), calcium (Ca), magnesium (Mg), and soil organic matter (SOM) contents, improve soil cation exchange capacity (CEC) and soil buffering capacity [11–13]. For example, Yue et al. [11] found that soil P availability increased up to 38 times after the application of biosolid biochar to soils. Lai et al. [13] found that the application of biosolid biochar mitigated greenhouse gas emissions and promoted carbon (C) sequestration with a rate of 0.54 Mg C ha⁻¹ year⁻¹. Penido et al. [14] proposed that the combination of biosolid biochar and fresh biosolid not only significantly promotes nutrient saving but also decreases metal concentrations. However, the biosolid-borne heavy metals are still retained in the char phase after pyrolysis and the concentration (per dry kg) will increase in the biochar compared to the biosolids [14,15]. Therefore, the heavy metals in biosolid biochar are still a major concern. Méndez et al. [16] and Song et al. [17] found that compared to biosolids, the bioavailability of heavy metals after the application of biosolid biochar was significantly inhibited. The biosolid biochar could reduce the mobility and bioavailability of heavy metals through adsorption, immobilization, stabilization, and microbial interactions [2,10,13]. However, the metal release from biosolid biochar may require a long time, with increasing time, the heavy metal may release from biosolid biochar and further increase the accumulation in crops and migrate into deeper soil profiles which contaminates the groundwater [18]. While, the previous studies were mainly conducted in labs with few solid results in fields [2,12,14,17], the effects of biosolid biochar in fields may help us better understand the fate of biosolid biochar-borne heavy metals and their potential risks.

Rice and wheat are important staple food crops globally, and China is one of the critical regions in rice and wheat production. Thus, the safe production of rice and wheat is essential. Our study aims to evaluate the effects of biosolid biochar-borne heavy metals on soils, crop production, and metal accumulation through a rice-wheat rotation system in fields. We hypothesize that after the application of biosolid biochar, crop yields could increase, while metal availability in soils and metal accumulation in crops could decrease. This information will help in elucidating the fate of biosolid biochar-borne heavy metals in the soil-crop system and identifying the potential risks associated with biosolid biochar application.

2. Materials and methods

2.1 Study area and experimental setup

The study area was located in the south of Jiangsu province, East China (31° 27′ N, 120° 25′ E). The local climate is subtropical oceanic monsoon with four distinct seasons. The traditional agricultural regime is a rice-wheat rotation. The field experiments were conducted from 2019 to 2020, with the rice season from June 2019 to November 2019, and the wheat season from November 2019 to June 2020. The rice variety is Suxiangjing 1 (Variety number: S015) and the wheat variety is Yangmai 19 (Variety number: CNA20080042.6), provided by the Suzhou Academy of Agricultural Sciences, which are widely used in Jiangsu province. There were three treatments: control with no biosolid amendment (CK); fresh domestic biosolids (FB, 16.2 t ha⁻¹, from Jiangsu Suzhou Fuxing sewage treatment plant, 75–85% water content [8]); biosolid biochar after pyrolysis at 550°C (BB, 16.2 t ha⁻¹). After flatted soils, fresh biosolids and biosolid biochar were applied evenly and covered by 2 cm soils. Each treatment has four replicate sites and is random in design with 13.5 m² in area (3.0 m wide × 4.5 m long, separated by a plastic separator 40 cm high above the ground). Compound fertilizers and urea (600 kg ha⁻¹) are applied in all treatments, and herbicides and pesticides are used when necessary. The basic properties of soil, fresh domestic biosolids, and biosolid biochar were shown in Table 1. The concentrations of Cd, Zn, Cu, and Pb in dry biosolids were within the requirements of GB4284–2018 for sludge used in agriculture, therefore were used in our study. During the harvest season, the soil and crop samples were collected by mixing five subsamples in one plot and air-dried for heavy metals determination. The total biomass of rice and wheat grain in each site was determined after cleaning and oven drying. After the last wheat seasons, the soil profiles (0–100 cm) were also collected by a soil sampler (diameter 2.5 cm) based on a 20 cm interval (P1, 0–20 cm; P2, 20–40 cm; P3, 40–60 cm; P4, 60–80 cm; and P5, 80–100 cm).

Table 1. The basic properties of soil, biosolids, and biosolid biochar.

	Soil	Biosolid	Biosolid biochar
pH	6.03	6.88	8.48
SOM (g kg^−1)	30.7	263	258
Cd (mg kg^−1)	0.49	1.79	2.42
Zn (mg kg^−1)	132	700	1100
Cu (mg kg^−1)	29.4	143	187
Pb (mg kg^−1)	26.8	121	166
Soil total N (g kg^−1)	1.54	33.8	48.7
Soil total P (g kg^−1)	1.00	41.1	39.8
Soil total K (g kg^−1)	18.7	26.3	33.5

2.2 Chemical analysis

The air-dried soil sample was ground and passed through a 2-mm sieve. Soil pH was determined with a pH meter (Model FE20, Mettler-Toledo, Columbus, OH) at a soil: water ratio of 1:2.5 (w/v). Soil organic matter (SOM) was determined by the potassium dichromate (K₂Cr₂O₇) method, and the nutrient element N, P, and K were determined by spectrophotometer based on the method of Lu [19]. Approximately 0.2 g soil samples were digested with 10 ml mixed HNO₃ (65%; ultrapure) and HCl (70%; ultrapure, 1:1 v/v) to determine total Cd, Zn, Cu, and Pb concentrations. The wheat and rice grain sample were washed cleaned, oven-dried, and then finely ground. Grain samples (approximately 0.5 g) were digested with 10 ml mixed HNO3 (65%; ultrapure) and H₂O₂ (30%; ultrapure, 3:1 v/v) to determine total Cd, Zn, Cu, and Pb concentrations. The samples and acids were placed inside 50-ml high-pressure polytetrafluoroethylene digestion containers and were placed in a digestion vessel at 105°C for 6 h. Then the containers were placed on an electric evaporation block at 105°C to remove acid until about 2 ml of solution remained. After cooling, the remaining solution was transferred into a clean polycarbonate tube and was made up to 15 ml with deionized water and filtered through a 0.45-μm syringe filter for metal analysis. Soil available metals were determined by extracting soils with 0.01 mol L⁻¹ CaCl₂ at a soil: extractant ratio of 1:10 (w/v) and continuously shaking for 2 h at 180 rpm, and then centrifuging for 5 minutes at 3500 rpm and filtering. The digested and extracted solution was analyzed by ICP-MS (Agilent 7500c×, Agilent, Santa Clara, CA). The certified reference material (GBW07429 and GBW10020, National Geochemical Standard Materials, Middle and Lower Yangtze River Plain, China) were used for quality control and were within the published acceptable ranges.

2.3 Statistical analysis

All data were expressed as mean ± standard deviation and were subjected to one-way analysis of variance (ANOVA) using the SPSS version 20.0 software package (SPSS, Chicago, IL). Duncan’s multiple range test was used to compare significant differences between different treatment means at the 5% level.

3. Results and discussion

3.1 Effects of biosolid and biosolid biochar application on soils

3.1.1 Soil surface

The addition of biosolid and biosolid biochar significantly changed soil chemical properties in both rice and wheat seasons (Table 2). The soil pH and soil organic matter increased significantly, and so did the heavy metal concentrations in soils(P < 0.001). Specifically, the soil pH in fresh biosolid treatment increased by 7.67% and 3.00%, respectively, in rice and wheat seasons. The soil pH in biosolid biochar treatment increased by 9.47% and 9.45%, respectively, in rice and wheat seasons. The soil SOM in fresh biosolid treatment increased by 18.0% and 17.2%, respectively, in rice and wheat seasons, and the soil SOM in biosolid biochar treatment increased by 26.4% and 20.8%, respectively, in rice and wheat seasons. The soil total Cd, Zn, Cu, and Pb increased by 8.86%, 15.3%, 9.18%, and 101%, respectively, in rice seasons after the application of fresh biosolid, and increased by 10.0%, 16.2%, 18.2%, and 91.6%, respectively, in wheat seasons. The soil total Cd, Zn, Cu, and Pb increased by 11.5%, 44.1%, 5.87%, and 86.2%, respectively, in rice seasons after the application of biosolid biochar, and increased by 12.4%, 47.0%, 9.67%, and 82.4%, respectively, in wheat seasons. This is probably because of the high pH values, SOM content, and heavy metal concentrations in fresh biosolid and biosolid biochar, which increase the pH values, SOM content, and heavy metal concentrations in soils after application. Notably, the total soil metal concentrations in BB treatment were higher than those in FB treatment. Méndez et al. [16] found the higher metal content in biochar samples than metal content in fresh biosolid was due to ash concentration during pyrolysis. However, the availability of heavy metals decreased a lot at BB treatment than FB treatment (Figure 1). The CaCl₂ extracted Cd, Zn, Cu, and Pb concentrations in soils after the application of biosolid biochar decreased by 48.3%, 36.7%, 56.1%, and 7.21%, respectively, at rice season and decreased by 50.8%, 46.6%, 49.7%, and 10.4%, respectively, at wheat season compared with the CK treatment. This is the same as previous studies. Studies found that the mobile forms of metals decreased after the pyrolysis process, the heavy metals dominantly remained as non-mobile forms [20,21], and the DTPA-extracted metal concentrations decreased in biosolid biochar-modified soils [16,22]. Although the total metal concentrations after the application of biosolid biochar were higher than the control treatment, the availability of metals seemed to be decreased [16,23]. When heavy metals are introduced into soils, they will experience a series of complex interactions with soil solid surface materials (inorganic constituents, organic ligands, and particle surface), such as adsorption and desorption reactions, complexation and dissociation reactions, precipitation and dissolution reactions, eventually influences its speciation and distribution [24,25]. The heavy metal speciations in soils significantly affect their mobility, bioavailability, and ecotoxicity. On the one hand, biosolid and biosolid biochar can change metal speciation in soils through ion exchange, electrostatic interaction, physical adsorption, complexation, and precipitation et al., further changing their availability. For example, Zhou et al. [26] found that the addition of biochar could significantly decrease the proportion of exchangeable and carbonate-bound states of Zn, Cu, Pb, and Cd, but significantly increase the proportion of residual states and iron-manganese oxide states of Zn, Cu, Pb, and Cd. In addition, the decrease rate is consistent with the biochar addition. Arabyarmohammadi et al. [27] conducted adsorption experiments of heavy metals on biochar and found that Cu is mainly involved in organic bonds of -NH2, -OH, and -COOH groups, Pb forms insoluble hydroxide, phosphate or carbonate precipitates, and Zn is mostly engaged in the residual fraction. On the other hand, the induced changes in soil properties are also a main factor affecting the availability of metals in soils. Studies found that the CaCl₂ extracted heavy metals concentration had a negative relationship with the soil pH, CEC, and SOC [28]. For example, the increase in soil pH could enhance the adsorption/complexation of iron oxide and manganese oxide, and increase the functional groups leading to chelation of organic matter, negative charge in soil clay minerals surface, hydration oxide, and organic matter, thus decreasing the availability of heavy metals [29,30]. Thus, the metal availability in soils after the application of biosolid biochar seems not significant in our study.

Figure 1. The CaCl₂-extracted metal concentrations in soils at different treatments and during rice and wheat seasons.

The lowercase letters indicate the significant difference among treatments.

Table 2. The selected soil characteristics of different treatments and during rice and wheat seasons.

		pH	SOM (g kg-1)	Cd (mg kg-1)	Zn	Cu	Pb
Rice	CK	6.25 ± 0.054d	31.7 ± 1.45c	1.56 ± 0.084b	177 ± 5.60c	27.9 ± 1.02ab	23.9 ± 2.60b
	FB	6.74 ± 0.128b	37.4 ± 3.73ab	1.70 ± 0.087ab	204 ± 5.29b	30.4 ± 4.98ab	48.1 ± 5.76a
	BB	6.85 ± 0.055a	37.2 ± 3.81ab	1.74 ± 0.099a	255 ± 13.8a	29.5 ± 1.91ab	44.5 ± 6.62a
Wheat	CK	6.19 ± 0.044d	30.7 ± 2.22c	1.54 ± 0.033b	175 ± 4.36c	27.7 ± 1.43b	25.0 ± 0.970b
	FB	6.58 ± 0.037c	38.8 ± 1.44a	1.69 ± 0.088ab	203 ± 6.24b	32.8 ± 4.10ab	47.8 ± 6.41a
	BB	6.78 ± 0.025ab	37.1 ± 3.40ab	1.73 ± 0.100a	257 ± 10.6a	30.4 ± 2.28ab	45.6 ± 7.30a

3.1.2 Soil profile

The transfer of metals from the soil surface to the groundwater is also a main safety concern to human health. In our study, after one year of rice-wheat rotation, although heavy metals were accumulated on the soil surface, no significant differences in heavy metal concentrations were found in soil profiles P2-P5 (Figure 2). These indicated that no metal transfer risks were detected to the deeper soil layers. This is probably because the metals are predominantly in less available forms thus hindering their migration into deeper soil layers [27,30]. Baldasso et al. [31] had similar results that the application of digestate from solid waste into soils had low metal mobility along soil profiles even if it carries high metal content. Beesley and Marmiroli [32] conducted a leaching experiment and concluded that biochar plays an important role in controlling the metal leaching decrement in biochar-amended soils, and the dominant mechanism is sorption rather than the increased pH for metal retention. In our study, no significant differences in metal concentrations in soil profile P2-P5 were found among different treatments. Thus, the transfer risks of biosolid biochar-borne heavy metal in the soil profile were also not significant, and biosolid biochar may be used in controlling the risk of contamination of groundwater by trace metals.

Figure 2. The total metal concentrations in soil profiles (0–100 cm) at different treatments.

3.2 Effects of biosolid and biosolid biochar application on crops

3.2.1 Crop production

As shown in Table 3, the application of biosolid and biosolid biochar significantly increased the yield and thousand seed weight of rice and wheat. Specifically, the rice yield increased by 6.40% and 12.1%, respectively, at FB and BB treatments, and the wheat yield increased by 4.87% and 8.23%, respectively, at FB and BB treatments. The thousand seed weights of rice and wheat also increased significantly at biosolid biochar treatment, with a 9.23% and 13.4% increase, respectively, compared to CK treatment. These may be due to the higher nutrients in biosolid and biosolid biochar. The previous studies had the same results. Hossain et al. [23] found that the application of biosolid biochar increased the height of cherry tomatoes by 30.0% and the production by 64%. Gascó and Lobo [33] also found that the application of biosolid biochar increased the level of trace elements and growth in plants. Faria et al. [12] did a two-year field experiment and found that the application of biosolid biochar increased soil chemical attributes, especially P, Mg, CEC, and base saturation. It has been confirmed that the application of biosolid biochar improves the availability of phosphorus (P), total nitrogen (N), and major cations in soils, and the increase in soil pH improves the efficiency of nutrient usage [11,14,34,35]. Firstly, biochar can act as a sponge, which can retain and release nutrients in the soil, making the nutrients available for plant uptake over an extended period. Secondly, the higher nutrients in biochar could increase nutrient availability in soils. As biochar gradually releases the retained nutrients into the soil, it creates a nutrient-rich environment around the plant roots. Adequate levels of N, P, and K promote healthy plant growth, increased root development, and crop productivity [4–6,35]. Biochar also has positive effects on soil quality with enhanced soil aeration, soil structure, and porosity, surface area, water holding capacity, and CEC [36–38]. The increased soil fertility also promotes the growth and development of the plant [28]. In addition, the application of biosolid and biosolid biochar may increase the activities of bacteria, which further promotes the mineralization of carbon compounds [39–41]. Although some studies found that the application of biosolid biochar had negative effects on plant germination and growth [42,43], these may be the differences between biochar properties, application rates, soil properties, environmental conditions, and plant species [44]. For example, Xie et al. [18] found that the addition of 10% of biosolids significantly increased the ryegrass growth, while, the application of 20% of biosolids inhibited the ryegrass height, tiller number, fresh biomass, and chlorophyll content. Thus, the application amount of biosolid in fields is also a main concern.

Table 3. The yield and seed performance of rice and wheat at different treatments.

	Rice		Wheat
Treatment	Yield (t hm^−2)	Thousand seed weight (g)	Yield (t hm^−2)	Thousand seed weight (g)
CK	3.454 ± 0.0646b	39.0 ± 0.100b	3.864 ± 0.208b	35.2 ± 0.542b
FB	3.675 ± 0.1026ab	39.2 ± 0.474b	4.052 ± 0.0980a	38.4 ± 0.482a
BB	3.871 ± 0.0892a	42.6 ± 0.323a	4.182 ± 0.0182a	39.9 ± 0.603a

3.2.2 Metal accumulation

As shown in Figure 3, the contents of heavy metals in rice and wheat grains were far lower than the Chinese national limit standard (GB 2762–2017), thus the food chain risks of heavy metals in crops in these areas were also low. The metal content in crops had no significant differences between the CK treatment and FB treatment, while with the application of biosolid biochar, the content of heavy metals in crops decreased significantly. The content of Cd, Zn, Cu, and Pb in rice decreased by 13.2%, 37.0%, 9.92%, and 63.0%, respectively, compared with the CK treatment. The content of Cd, Zn, Cu, and Pb in wheat decreased by 20.85%, 19.7%, 48.6%, and 23.6%, respectively, compared with the CK treatment. The decrease in metal content in crops was probably due to the decrease in metal availability after the application of biosolid biochar (Figure 1). In addition, the content of heavy metals in rice was lower than that in wheat. This may be due to wheat has high metal bioaccumulation factor (BCF) than rice. For example, Li and Zhou [45] found that BCF-Cd and the root-to-shoot Cd translocating ability of wheat were higher than rice. In addition, the availability of the metal was lower in the rice season than in the wheat season which was consistent with our studies. Under the rotation of irrigation and drought, the soil moisture content and state, redox state and pH value would change, thus further affecting the accumulation of metals in crops, and the heavy metal availability is increased during the dry season [46].

Figure 3. The metal concentrations in rice grain and wheat grain at different treatments.

The lowercase letters indicate the significant difference among treatments.

The pyrolysis of fresh biosolids to biochar and the application of biosolid biochar in agriculture has become a cost-effective and efficient method in addressing the issues of biosolid disposal and soil remediation [2,39]. However, the previous studies of the effects of biosolid biochar application in soils were commonly conducted in labs [16,28], our study confirmed that although biosolid biochar increased the total metal concentrations in soils in fields, the availability of the metals was inhibited. After one year of rice-wheat rotation, the effects of biosolid biochar on crop production and metal retention are still promising. However, it should be noted that except for heavy metals, biosolids may contain organic toxic compounds like poly-fluoroalkyl substances (PFAS), which can cause adverse effects in soils, groundwater, and plants, which eventually affect human health [15,47]. In addition, the pyrolysis temperature could affect the potential of biosolid biochar as a soil amendment, and the effects are more profound than the biosolid material [48]. Bamdad et al. [47] found that the higher pyrolysis temperature (550°C) can eliminate PFAS level by 97–100 wt% in the resulting biosolid biochar. However, the high pyrolysis temperature may also lose the nutrient elements such as Ca, Mg, and Zn [49,50]. Although the combination of fresh biosolid and biosolid biochar has been an alternative method for nutrient saving and metal remediation, the long-term effects still need to be determined [14].

4. Conclusion

In our studies, we conducted field research on the effects of biosolid biochar on soils through a rice-wheat rotation system, the application of biosolid biochar did increase the total heavy metal in the soil surface, but the metal availability in soils and the metal accumulation in crops were decreased, and the rice and wheat yields were increased. Our study provides solid evidence that biosolid biochar is beneficial in crop production and soil quality, thus, is suggested to use in the fields, but the pyrolysis temperature and the application amount should be concerns. In addition, long-term field trials of biosolid biochar are suggested to carry out in the future.

Authors contribution

All authors provided support and contributions to the conception and design of this article. All authors read and approved the final manuscript. Yonghua Liu: Conceptualization, Methodology, Data curation, Writing the original draft; Jing Wu: Conceptualization, Methodology, Writing review & editing; Guoqiang Liu: Data curation, Writing review & editing; Jialing Zhang: Writing review & editing; Haidong Li: Writing review & editing.

Disclosure statement

No potential conflict of interest was reported by the author(s).

Additional information

Funding

This study is supported by the National Natural Science Foundation of China (Grant No. 72174127).