Effect of exogenous additives on heavy metal passivation and nitrogen retention in pig manure composting

Highlights

● Research on heavy metal passivation and nitrogen emissions is necessary for the pig industry.

● Mechanism of heavy metal passivation and nitrogen retention by different additives was introduced.

● Development and prospect of metal passivation, nitrogen preservation technology were discussed.

Abstract

The widespread use of feed additives in intensive and large-scale pig farming has resulted in high levels of heavy metals in pig manure. The long-term application of organic fertilizers containing high levels of heavy metals leads to the accumulation of heavy metals in the soil, which not only causes heavy metal pollution in the soil, and also affect food safety and endanger human health. Composting is an economical and effective technical measures to achieve environmentally-sustainable treatment of pig manure and is a practical method to reduce the problem of heavy metals and to improve the resource value of pig manure. The composting process is accompanied by high temperatures and the production and emission of gases, and also lead to changes in the nitrogen content of the compost and provide opportunity for heavy metal passivation additives. This paper summarizes the forms and types of heavy metals present in pig manure and reviews the progress of research as well as the techniques and problems of in the composting process, and provides recommendations for research on heavy metal passivation and nitrogen retention in pig manure composting.

Graphical abstract

Keywords

Additives / composting / heavy metals passivation / nitrogen retention / pig manure

1 INTRODUCTION

In recent years, with the expansion of the livestock industry in China and the increasing intensive production, the number of pigs slaughtered in China reached 0.4 billion at the end of 2020^[1]. The rapid development of scale and intensification of the pig industry has produced an increasing amount of pollutants^[2]. The annual production of livestock manure in China in 2021 is about 3.8 Gt^[3]. A survey showed that as a proportion of livestock and poultry manure in China was about 29% of gas emissions come from pig manure, and for heavy metal pollution pig manure contributed about 71%^[4].

Heavy metal contamination from pig manure is widespread in agricultural soils in China, with average concentrations ranging from 0 to 10 mg·kg^−1[5]. A survey found that in some areas pig manure contained 767 mg·kg⁻¹ of copper and 3130 mg·kg⁻¹ of zinc^[6], and heavy metals are present in agricultural soils for a long time and most of them are toxic, causing impacts on the growth and development of soil organisms and crops, and even affecting animal and human health through the food chain.

Nitrogen, one of the important nutrients for crop growth, but during the fermentation of compost, there is a significant release of greenhouse and harmful gases, including CO₂, NH₃, CH₄ and N₂O. Most nitrogen loss is through NH_3, with a smaller proportion through N₂O. China aims to be carbon neutral by 2035, so greenhouse gas emissions from animal industries cannot be ignored. Understanding and control of greenhouse gas emissions from manure is necessary. Nitrogen retention in pig manure compost is as important as the passivation of heavy metals. Also addition of heavy metal passivators can be used to change the form of heavy metals present and also changes the composting environment, thus affecting the release and retention of nitrogen.

Therefore, it is crucial to investigate the origin, form and type of heavy metals in pig manure, passivation techniques, and the impact of passivators on nitrogen retention in compost in order to make this treatment of pig manure suitable for applying the material to agricultural fields.

2 SOURCES, FORMS AND BIOAVAILABILITY EVALUATION OF HEAVY METALS IN PIG MANURE

2.1 Heavy metal sources

The use of high doses of Cu and Zn has been increasing since it was discovered that there metals promote piglet growth, reduce diarrhea and increase daily feed intake and performance^[7]. This has resulted in a widespread problem of excess Cu and Zn in pig manure^[8]. Although China has clearly defined the concentration thresholds of heavy metals in agricultural soils in the Environmental Quality Control Standards for Contaminated Soil on Agricultural Land^[9]. However, some companies still add large amounts of these feed additives containing high doses of metals for financial gain. In general, the concentration of feed Cu can reach 200−300 mg·kg⁻¹ and selenium 0.3–0.5 mg·kg⁻¹. However, 95% of Cu²⁺ and Zn²⁺ in CuSO₄ and ZnO is not absorbed and utilized livestock. Pigs have a low utilization rate of metal additives in feed, most of which are eliminated in feces and urine^[10]. Feed processing also results in residues of trace metal elements, which combined with the misuse of feed additives, leading to serious pollution of agricultural soils by heavy metals such as zinc, copper, lead, cadmium, chromium, mercury, arsenic and nickel^[11,12]. Soil heavy metal contamination affects the survival of soil microorganisms, leading to a decrease in soil microbial load and changes in microbial activity and structure^[5]. In addition, heavy metal migration in soil following rainwater can lead to water pollution, deteriorating water quality and toxicity to aquatic organisms.

The most concentrated heavy metals in pig manure are mostly Cu, Zn and Cr^[13], and this mostly comes from feed additives. It has been found that the excess Cu in manure of fattening pigs and piglets was 82% and 97%, respectively, and the content of Zn all exceeded the standard^[14]. Heavy metal overload has become the biggest source of pollution in pig industry in China^[15].

2.2 Heavy metal forms

Currently single and step-by-step chemical extraction methods are often used to study the morphological distribution of heavy metals in livestock manure and amended soil^[16]. In 1979, Tessis et al.^[17] proposed that heavy metals in soil or sediment could be classified after a five-step sequential extraction method as exchangeable, carbonate-bound, Fe manganese oxide bound, organic bound and residue, in order of biological availability^[18]. A standardized extraction protocol was also proposed by the European Bureau of Reference Materials and modified in 1999, referred to as the BCR stepwise extraction method. This method classifies the heavy metals into a weak acid extracted state, a reduced state, an oxidized state and a residue state^[19]. For heavy metals in pig manure, the biological effectiveness of different forms varies. The main way to control heavy metal pollution in livestock and poultry manure is to fix heavy metals in livestock and poultry manure by changing their forms and reducing their mobility and availability, and then to remove them from the manure. The main method to control heavy metal pollution in livestock manure is to use livestock manure composting^[20,21]. It has been shown that composted sludge has about 7.3% to 16% less heavy metals due to the dilution effect of conditioning agents and significant changes the morphology of heavy metals^[22]. More recently, it has been found that an effective way is to add heavy metal passivator to the composting process to transform the form of heavy metals from high to low activity, reducing bioavailability.

2.3 Heavy metals bioavailability evaluation

The bioeffective properties of heavy metals reflect the degree of their uptake and utilization by organisms, which is a key parameter in heavy metal pollution risk assessment and is receiving more attention in practical research and application^[23,24]. However, biological effectiveness is based on both chemical and biological concepts. Nelson^[25] defines the bioavailability of heavy metals as a property of heavy metals that produces toxic effects on organisms or leads to uptake by organisms, including toxicity and bioavailability, as evaluated by indirect toxicity data or organism concentration data. Biological effectiveness has also been viewed as a dynamic process that must be considered in relation to the environment around the organism^[26] but there is no unified international standard for the evaluation of biological effectiveness of heavy metals^[27,28].

The study of morphological distribution of heavy metals in pig manure is important for predicting the biological effectiveness and environmental risk of heavy metals in pig manure, which can provide more useful information on the migration transformation, biological effectiveness and leaching of heavy metals after applying livestock manure to agricultural fields^[29].

3 NITROGEN AND HEAVY METALS

Nitrogen is an essential element for plant growth and one of the main elements of the compost microenvironment^[30]. Nitrogen conversion in composting systems is a fundamental biochemical process mediated by a variety of microorganisms^[31], mainly including ammonification, ammonia assimilation, nitrification and denitrification (Fig.1). These processes occur simultaneously with heavy metal passivation. Compost heavy metal passivators are mainly divided into three categories: physical, chemical and microbial. Physical technology mainly uses activated carbon, zeolite, bentonite and other substances with high adsorption capacity, which can effectively adsorb heavy metals and reduce their biological effectiveness. These additives also affect the emission of nitrogen from the composting process. Likewise, chemical and microbial additives for heavy metal passivation can affect nitrogen emissions. Therefore, it is necessary to study heavy metal passivation and nitrogen retention in parallel.

Fig.1 Mechanisms of physical additives passivation of heavy metals.

Full size|PPT slide

4 METHODOLOGICAL INITIATIVES TO IMPROVE THE EFFICIENCY OF HEAVY METAL PASSIVATION

Heavy metal contamination is a major limiting factor in the application of composting products. Therefore, determining how to effectively reduce the toxicity of heavy metals in the composting process has become a primary concern in composting^[32]. There are many studies on heavy metal passivation methods and the effectiveness of passivation.

4.1 Physical additives

Biochar, zeolite, bentonite and other additives has been extensively researched and used for the safe, minimization of toxins as well as resource recovery of agricultural waste^[33,34]. In agricultural production, the application of biochar can reduce soil nutrient runoff^[35], improve land fertility and raise the pH of acidic soils duet to the high specific surface area, pore size characteristics and strong adsorption capacity^[36]. Improving the final quality of the compost can effectively reduce the biological impact of manure in terms of organic or inorganic pollutants^[37].

Fig.1 shows the interaction mechanism between physical additives and fecal heavy metals. In general, the interaction between physical additives and fecal heavy metals involves cation exchange, complexation, coprecipitation, electrostatic adsorption, cation-π interactions and physical adsorption^[38].

Kong et al.^[39]. found that the addition of biochar, calcium magnesium phosphate fertilizer and spent mushroom substrate to compost with 42% to 53% exchangeable zinc and 2.5% to 39%, reducible zinc, the exchange zinc content was reduced by 5.9% to 6.8%. Zinc passivation achieved by the treatments increased in the order: CK < biochar < mushroom substrate < calcium magnesium phosphate fertilizer. Ingelmo et al.^[40] found that Zn availability was positively associated with the fulvic acid (FA) fraction and negatively associated with the humic acid fraction. Therefore, the availability of zinc was strongly affected by the humification process.

Yang et al.^[41] investigated the immobilization properties and mechanisms of heavy metals using biochar modified by KH₂PO₄ during the anaerobic digestion of pig manure. This was found to it make these heavy metals more stable and reduce the biological risk. The modified biochar was quite efficient in passivating copper and lead. Therefore, KH₂PO₄ modified biochar can be used as a new type of heavy metal passivation remediation agent. The effect of additives biochar and humic acid, on the passivation of heavy metals in pig manure compost was investigated by Zhou et al.^[42] Their results showed that the addition of fertilizer passivators to compost products with sawdust charcoal improved the passivation of heavy metals during composting. The deactivation rates of copper, lead and zinc were greatly reduced. The application of compost also increases the yield of oilseed rape. Chen et al.^[43] added biochar and H₃PO₄ modified biochar to explore the effects on heavy metal stability, antibiotic resistance genes. Biochar and H₃PO₄ modified biochar significantly reduced the concentration of DTPA extractable copper and zinc compared to the control. There was also a significant reduction in the total abundance of nine antibiotic resistance genes and five metal resistance genes in the compost products treated with biochar and H₃PO₄ modified biochar compared to the control. Wang et al.^[44] studied the effect of adding different proportions of biochar to pig manure to increase biogas production and reduce the biological effectiveness of heavy metals, while the potential biological risk of heavy metals in the digestate was also assessed. The results showed that methane production significantly increased with the addition of different proportions of biochar. Also, there were significant changes in heavy metal morphology in each group. Cui et al.^[45] investigated the correlation between bacterial diversity and heavy metal fractions during the composting of with a range of doses of biochar. Their results showed that the bioavailability coefficients of zinc, copper, cadmium and lead were significantly reduced in all groups after the addition of biochar. This indicates that biochar had an effect on bacterial population structure and heavy metal passivation in the pig manure compost. The bioavailability coefficients of heavy metals were significantly reduced by biochar-amended compost compared to the control. Addition of 12% date palm biochar to pig manure compost resulted in significantly higher passivations of Cu and Zn. Also, the maximum composting temperature was advanced regardless of the percentage of date palm biochar added^[46]. Composting was significantly improved and the composted product was less toxic^[47]. The effect of heavy metal passivation through adsorption and humification during aerobic composting of zeolites of various particle sizes has been investigated^[48]. The morphological changes of heavy metals during composting were also observed. In comparison to the control, zeolites significantly reduced the bioavailability coefficients of heavy metals, especially copper, cadmium and lead. Redundancy analysis and structural equation modeling indicated that the passivation promotion of heavy metals was comparable for coarse and fine zeolites and was accelerated by surface adsorption for cadmium and lead and by humification for copper. Wang et al.^[49] study inorganic additives phosphate rock and boron waste were added to the compost and monitored for temperature, pH, EC, OM, TN, TP and other indicators during composting. It was found that phosphate rock and boron waste provided certain nutrients and promoted the degradation of organic matter in the humus chelating Cu and Zn, and the passivation of Cu was promoted. Xu et al.^[50] investigated the effect of sodium hydroxide addition on the properties and environmental risks of heavy metals in pig manure biochar. It was found that the addition of various doses of sodium hydroxide at different temperatures increased pH, EC, ash content, yield, aromaticity and hydrophilicity, while promoting the conversion of mobile fractions of Cu, Zn and Cd to oxidizable fractions. This study also found that NaOH-assisted pig manure pyrolysis can be an effective method for immobilizing heavy metals. The addition of NaOH promoted the formation of more stable metal compounds and increased the alkalinity of the biochar. Li et al.^[51] natural bentonite and microwave-treated bentonite were added to composted pig manure. The analysis of the samples and the extraction by BCR method showed that the percentage of heavy metal Cr in the oxidizable and residual state increased, indicating that anaerobic fermentation reduced the biological activity of heavy metal Cr in pig manure. Microwave treated modified bentonite effect is better than the addition of natural bentonite treatment. At the same time, surface source pollution is reduced and energy material and high quality organic manure is obtained. It was found that the addition of maize straw significantly increased the degradation of organic matter in pig manure during composting^[52]. The migration rate of Cu and Zn decreased at an initial C:N of 25:1 and eventually 90% Cu was the residual fraction. In addition, the compost mixture with an initial C:N of 25:1 accelerated the decrease in urease activity compared to the compost mixtures with an initial C:N of 15:1 and 20:1. Hui et al.^[53] use of agricultural lime and a newly designed alabaster activated carbon composite (AACC) in a pig manure composting system enhanced the stability of heavy metals and improved the degradation of antibiotics. The addition of AACC reduced the enrichment of chromium, cadmium, lead and arsenic during the composting process. Concurrently, the high heavy metal hazard in the manure inhibited the dissipation of antibiotics. The addition of lime and AACC promoted the fixation of heavy metals in the manure and accelerated the breakdown of antibiotics. Therefore, mixing pig manure and AACC for composting not only significantly reduced compost contaminants, but also improved nitrogen conversion and reduces the phytotoxicity of compost products. Liu et al.^[54] found that the addition of magnetic Fe₃O₄/FA composite additive to pig manure anaerobic compost could promote methane production in the anaerobic digestion system by adding different concentrations of Fe₃O₄/FA. Also, the introduction of Fe₃O₄/FA composites could effectively control the migration of heavy metals and Fe₃O₄/FA enhanced the passivation of Cu and Zn in the solid digestion residue. The mechanism of heavy metal passivation by Fe₃O₄/FA mainly involves physical adsorption during anaerobic digestion. This process converts heavy metals into stable mineral precipitates and reduces the solubility and mobility of heavy metals.

4.2 Chemical additives

Chemical techniques are mainly used to remove heavy metals from surface acidification, ion exchange, solubilization, complexing agents and surfactants. The diagram below shows the mechanism by which chemicals passivate heavy metals (Fig.2). The chemical additives for treatment fecal heavy metals mainly act as acidification treatments, surfactants and complexing agents. Acidifiers remove large amounts of heavy metals by dissolving them. Surfactants and complexing agents convert insoluble metals into soluble metals or complexes which can be removed.

Fig.2 Chemical passivation agent passivation mechanism.

Full size|PPT slide

Liphadzi et al.^[55] investigated the conversion of heavy metals in compost from an insoluble compound to a soluble ionic state as the principle of the chemical approach to remove heavy metals from compost. The most studied chemical method is acidification, and the other method is the use of complexing agents.

Acidification treatment usually uses sulfuric acid, hydrochloric acid, nitric acid, phosphoric acid, organic acid and other chemical reagents to dissolve a wide range of metals. However, it has been shown that when sulfuric acid is used alone, the removal effect of copper and lead is not ideal^[56]. While using 1:1 hydrochloric acid/sulfuric acid to treat sludge the removal rate of heavy metal copper, lead, zinc and tin can achieve 60% or more. The use of nitric acid leaching of sludge can achieve copper and arsenic removal rates of 87% and nickel removal of up to 100%^[57].

The use of organic complexing agents for the removal of heavy metals is based on the principle that the addition of complexing agents to insoluble metal compounds converts them into soluble metal complexes for removal. Studies have shown that organic complexing agents (EDTA and DTPA) are very effective in removing heavy metals. For example, EDTA can form stable compounds with many heavy metals and 0.1 mol·L⁻¹ EDTA was able to remove Pb. It was found that the extraction of Pb by EDTA could reach over 60%^[58]. A study on the removal of heavy metals by surfactants found that surfactants mixed with EDTA were effective in removing heavy metals in the order: Cd > Pb > Zn^[59]. Surfactants can remove heavy metals from soil by desorption, but may have serious environmental impacts. So, it is important to use rapidly degradable and non-toxic surfactants to remove heavy metals from manure.

4.3 Microbial additives

The addition of microbial agents to the composting process has become one of the most effective ways to reduce the biological activity of heavy metals^[60]. The dosage of microbial additives in compost generally ranges from 0.05% to 5.0%, and the amount of bacterial agent varies for different times of composting^[61]. Phosphate mineralizing bacteria can also mineralize heavy metals. Many bacteria and fungi can mineralize heavy metals in soil and water bodies by hydrolyzing inorganic phosphate sources (apatite minerals) or organic phosphate sources (phenolphthalein diphosphate, glycerophosphate, acetylmethamidophosphate, glycerol 2-phosphate and phytate) in the presence of phosphatase or phytase to release phosphate, thereby reducing the mobility of toxic ions^[62]. The diagram below shows the mechanism of mineralization by phosphate-mineralization bacteria (Fig.3).

Fig.3 Mechanism of mineralization by phosphate-mineralization bacteria.

Full size|PPT slide

Li et al.^[63] studied composting supplemented with different types and doses of biochar and found these treatments increased fixation of heavy metals in pig manure composts. Seventy percent of copper was fixed by addition of peanut shell biochar and microbial preparations. The fulvic and humic acid-like substances in the humus increased to nearly twice the pre-compost level. The conversion of copper and zinc to a more stable state was closely related to the formation of fulvic and humic acids, and the immobilization and humification of copper and zinc were positively correlated with pH. Cui and Wang^[64] used Thiobacillus ferrous oxide amended sludge to examine if biological leaching could effectively dissolve the heavy metals in the sludge. After 4−10 d of biological leaching, the removal rates of Cr, Cu and Zn reached 80%, 80% and 100%, respectively. Cao et al.^[65] found that anaerobic fermentation could mitigated heavy metal contamination with migration rates higher under high temperature ana fermentation. The metabolic activity of microorganisms such as fungi, bacteria and algae can be used to effectively mitigate heavy metal toxicity and contamination. Luo and Wu^[66] report that the addition of earthworms to the compost was able to reduce the heavy metal content, but the reduction was dependent on the in earthworm species. The production of biogas and passivation of heavy metals during anaerobic digestion were analyzed using treated rice straw as feedstock. It was found that more than 80% of the copper was present in the oxidizable and residual fractions, also, that zinc was effectively improved by microwave and ultrasonic treatment for adsorption^[67]. The addition of rice straw also effectively improved the passivation efficiency of copper and zinc. Therefore, the addition of rice straw facilitated the passivation of heavy metals, but the cost for removing heavy metals in the substrate and pretreatment needs to be further investigated.

4.4 Comparison of heavy metal passivation methods for pig manure

By comparing the operability, efficiency, cost effectiveness and environmental safety of several heavy metal removal methods, it was found that physical methods are less efficient than chemical and microbiological methods for removal of heavy metals from sludge, but such methods were less expensive and simpler to operate^[68]. The use of chemical and microbiological methods to reduce the content of heavy metals can achieve in higher heavy metal removal rate, but the high cost, complex operation and environmental friendless limit their practical application^[69]. The following table lists the advantages and disadvantages of the different additives available today (Tab.1).

Tab.1 Advantages and disadvantages of different additives

Type of additives	Advantages	Disadvantages	References
Physical additives	Easy operation	Less effective	[40–51]
	Low cost	Low repeatability
	Wide range of sources
Chemical additives	Better effects	Difficult operation	[56–60]
	Fast results	Higher costs
		Waste liquid pollution
		Application difficulties
Microbial additives	Reusable	High technical demands	[63–67]
	Better effects	Higher costs
	Great prospects	Further research needed

5 EFFECT OF EXOGENOUS ADDITIVES ON NITROGEN RETENTION IN COMPOST

Nitrogen losses during composting are mainly as NH₃ and N₂O emissions and account for 79% to 94% and 0.2% to 9.9% losses, respectively^[70]. The main pathways of nitrogen conversion in aerobic composting include ammonification, nitrification, denitrification and biofixation (Fig.4)^[71].

Fig.4 Nitrogen conversion processes in composting.

Full size|PPT slide

NH₃ emissions are mainly produced by the biodegradation of nitrogenous substances. Ammoniation, also known as deamination, is a process by which microorganisms decompose organic nitrogen compounds to produce ammonia^[72] by the following two processes: (1) protein is hydrolyzed into peptide by the catalysis of microbial protease; then (2) deamination, which primarily involves the separation of amino acids to produce NH₄⁺/NH₃. The most common type of amino acid degradation is oxidative deamination. NH₄⁺ and NH₃ maintain chemical equilibrium through NH₃·H₂O in the aqueous phase. Under high pH and high temperature conditions, the equilibrium moves in favor of producing NH₃, which results in the release of NH₃ into the atmosphere.

Nitrification is a critical step to accelerate conversion of ammonium nitrogen to oxidized N and reduce ammonia volatilization. Ammoxidation is the first and rate-limiting step of nitrification, including two reactions, wherein NH₃/NH₄⁺ forms hydroxylamine by ammonia monooxygenase and then NO₂⁻ is formed by hydroxylamine oxidoreductase^[73]. Given that nitrifying microorganisms are sensitive to temperature, their growth is inhibited by high temperature in composting, so that nitrification is weak in the thermophilic phase of composting^[74].

Denitrification is a process in which microorganisms successively reduce NO³⁻ to NO₂⁻, NO, N₂O and N₂^[75]. In general, microbial denitrification occurs in the anoxic microenvironment of composting, including four enzymatic reduction reactions corresponding to the following four reductases: nitrate reductase, nitrite reductase, nitric oxide reductase, and nitrous oxide reductase. Nitrite and nitrous oxide reductases contribute to denitrification.

5.1 Physical additives

Physical additives are either natural or synthetic, with large specific surface area, strong adsorption, strong ion exchange ability, through its adsorption capacity to reduce the conversion of NH₄⁺ to NH₃^[48]. Similar to heavy metal physical passivation, physical additives (Tab.2) can significantly reduce NH₃ and N₂O emissions during composting, with average values reaching 35% and 60%, respectively.

Tab.2 Effects of physical additives on nitrogen retention in pig manure compost

Feedstock	Additive	Impact on N conservation (%)				Reference
		TN	CH4	NH3	N2O
Pig manure and maize straw	Ca(H2PO4)2 + MgSO4	65↓	59↓			[72]
Pig manure and maize straw	Guano crystals + nitrification inhibitors			50↓		[76]
Pig manure and wheat straw	Biochar (10%)a	54.5↓	51↓			[77]
	Biochar (10%)a + zeolite (10%)a			63.4↓	78.13↓
	Biochar (10%)a + zeolite (10%)a + wood vinegar solution (2%)a			74.32↓
Pig manure and sawdust	Raffinate + zeolite + biochar + wood	55.5↓	80↓			[75]
	vinegar solution		74↓	69↓
Pig manure and sawdust	Clay (10%)a		45↓	86↓		[78]
Pig manure and wheat straw	Calcium superphosphate	22↑				[79]
	Apple dregs	87↓
	Bentonite		55↓
Pig manure and sawdust	Bamboo charcoal + bamboo vinegar liquid	74↑				[78]
Pig manure and maize straw	Phosphogypsum (10%)	22↓				[80]

Note: a Dry weight.

The effects of adding bamboo charcoal and bamboo vinegar liquid to compost piles on nitrogen retention and copper and zinc fixation during the composting of pig manure were investigated^[78]. Total Kjeldahl nitrogen loss, as well as copper and zinc migration, decreased with increasing bamboo charcoal addition. Total Kjeldahl nitrogen loss and mobility of copper and zinc were significantly reduced compared to the control. The addition of BV further reduced the total Kjeldahl nitrogen losses. It also influenced the changes in compost temperature, pH and germination index (GI), shortening the time to the high temperature phase of composting, reducing the pH at the high temperature stage and increasing the GI of the compost product. Therefore, the addition of bamboo charcoal or bamboo charcoal + vinegar to pig manure compost is an effective way to reduce total Kjeldahl nitrogen losses and control Cu and Zn migration. The effect of additives such as apple pomace, bentonite and calcium superphosphate on nitrogen, carbon and phosphorus conversion and compost maturity during the composting of pig manure has been investigated^[79]. It was found that the additives all prolonged the high temperature phase of composting compared to the control. Calcium superphosphate helped facilitate composting and significantly reduced ammonia volatilization during the high temperature phase and increased the total nitrogen and phosphorus content of the compost, while bentonite increased ammonia volatilization and reduced the total nitrogen concentration. These results indicate that calcium superphosphate is an effective additive for maintaining nitrogen during composting of pig manure. The effect of clay on greenhouse gas emissions and humification during the composting of pig manure has also been investigated^[81]. The results show that the addition of clay resulted in a significant reduction in CH₄ and N₂O emissions, promoted the degradation of organic matter and facilitated the synthesis of humic acids. Dissolved organic matter spectra showed that the addition of clay promoted the formation of aromatic carbon compounds and the degradation of aliphatic carbon. Also, the decomposition of tyrosine and tryptophan and the formation of humic acid-like substances were promoted, increasing humification^[82].

5.2 Chemical additives

Chemical additives reduce nitrogen losses during composting, for example, by adding acidic chemicals or nitrification inhibitors, or by inducing guano stone crystallization^[49]. The mechanism for this is shown in Fig.5. Chemical additives reduce nitrogen loss in the composting process by adding acidic chemicals and nitrification inhibitors (dicyandiamide) and inducing struvite crystallization. Chemical additives (acidic chemicals and struvite crystallization) can significantly reduce NH₃ emissions in the composting process, but N₂O emission reduction was low.

Fig.5 Mechanism of action of chemical additives on nitrogen loss during composting.

Full size|PPT slide

Tab.3 lists the effects of different chemical additives in pig manure and straw compost on nitrogen content of the compost. Of the effects, the retention and emission of total nitrogen, ammonia and nitrous oxide were improved by the additives.

Tab.3 Effect of chemical additives on nitrogen retention in pig manure compost

Feedstock	Additive	Impact on N conservation (%)				Reference
		TN	CH4	NH3	N2O
Pig manure and maize straw	H3PO4 (15%)a, MgO (15%)a	49.8↑		55.4↓		[76]
	H3PO4 (15%)a, Mg(OH)2 (15%)a	44.5↑		50.8↓
	Ca(H2PO4)2 (15%)a, MgSO4 (15%)a	53.1↑		59.1↓
	H3PO4 (15%)a, MgSO4 (15%)a	73.9↑		81.9↓
Pig manure and maize straw	H3PO4 (15%)a, MgO (15%)a				78.6↓	[80]
	Dicyandiamide (10%), H3PO4 (15%)a and MgO (15%)a				53.7↓
Pig manure and maize straw	Calcium magnesium phosphate (10%)b			42.9↓		[83]
Pig manure and maize straw	Phosphogypsum (10%)b			21.6↓		[84]
	Phosphogypsum and dicyandiamide (0.2%)b			29.3↓
Pig manure and maize straw	Calcium magnesium phosphate (20%)			29.3↓		[85]

Note: a Initial molar ratio of nitrogen and b dry weight.

The effects of four different struvite crystallization process (SCP) on pig manure compost were compared^[76]. Four combinations of magnesium and phosphate were evaluated and compared with a control group without the addition of additives. The addition of magnesium salts and phosphates with an initial nitrogen content of 15%. SCP significantly reduced the NH₃ emissions. With the addition of sulfate, CH₄ emissions were significantly reduced and a fully mature compost was produced. In practice, Ca(H₂PO₄)₂ + MgSO₄ can be used for nitrogen retention in compost. The results showed that the combination of SCP and dicyandiamide was phytotoxic, SCP significantly reduced NH₃ losses, dicyandiamide significantly inhibited nitrification at higher levels and it significantly reduced N₂O emissions^[80]. Li et al.^[85] in a study of the nitrogen retention properties of phosphogypsum and calcium magnesium phosphate on pig manure composts it was found that mixing phosphogypsum with calcium magnesium phosphate was effective in retaining nitrogen. The mixture of these two additives can synergistically regulate NH₃ and N₂O emissions, thereby increasing NH₄⁺-N and the total N content of the compost. The addition of phosphogypsum alone can also reduce NH₃ emissions. The addition of calcium magnesium phosphate alone can slow the release of N₂O. Regardless of the addition, both additives can improve the maturity and quality of the compost by introducing additional nutrients. Liu et al.^[83] found that calcium magnesium phosphate fertilizer, biochar and spent mushroom substrate significantly reduced total emissions of nitrogen- and sulfur-containing gases. It also effectively reduced emissions of NH₃, H₂S, dimethyl sulfide and dimethyl disulfide, while improving GI values.

5.3 Microbial additives

Microbial additives can contain a single strain of bacteria, but also a combinations of strains. Currently, these are commonly species of Bacillus, Lactobacillus, Pseudomonas and/or Streptomyces, or wood mold or white rot bacteria^[86]. Different bacterial products have their own characteristics and the appropriate microbial preparation should be selected according to the types and characteristics of the organic matter being composted. Fig.6 shows the mechanism of reducing nitrogen loss during composting with microbial inoculants. Adding exogenous microorganisms to the compost can reduce ammonia emissions and retaining more nitrogen by changing the metabolism of carbon and nitrogen. Microbial additives can significantly reduce NH₃ and N₂O emissions during composting. During the thermophilic phase of composting, microorganisms rapidly decompose and utilize organic nitrogen substances, resulting in the formation of a large amounts of NH₄⁺, and the increase in pH accelerates the transformation from NH₄⁺ to NH₃. The presence of nitrate in compost was previously considered as a clear indicator of maturity^[71].

Fig.6 Mechanism of reducing nitrogen loss during composting by inoculating microorganisms.

Full size|PPT slide

As shown in Tab.4, it was found that the addition of Bacillus, Lactobacillus paracasei or a mixture of bacteria to pig manure composting materials reduced total N losses by 22%, 17% and 35%, respectively, while the addition of Bacillus megaterium and bentonite reduced NH₃ and N₂O emissions.

Tab.4 Effect of microbial additives on nitrogen in pig manure compost

Feedstock	Additive	Impact on N conservation (%)				Reference
		TN	CH4	NH3	N2O
Pig manure and sawdust	Bacillus	22↑				[87]
Pig manure and wheat bran	Lactobacillus paracasei	17↑				[88]
Pig manure and wheat straw	Bacillus megaterium (5%)a			31.3↓	53.1↓	[89]
	Bentonite (5%)a			18.8↓	72.6↓
	Bacillus megaterium and bentonite (mix 5%)a			23.7↓	63.4↓
Pig manure and wheat straw	Ammoniation bacteria, nitrifying bacteria and nitrogen fixing bacteria	35↑				[32]

Note: a Dry weight.

Li et al.^[90] found that inoculation with 1% Bacillus immobilis, prolonged the high temperature phase of composting, increased the number of heat-tolerant bacteria and the concentration of NH₄⁺-N and NO₃-N, and increased cellulase activity during the cooling phase of composting. The final results indicate that inoculation of microorganisms accelerated the composting process and significantly modulated microbial function. Analysis of the effect of biochar on changes in compost bacterial communities showed that bacterial activity in the thermophilic stage was controlled by the dissolved organic carbon content and the temperature of the compost mixture, while conductivity and total Kjeldahl nitrogen also influenced the maturity stage of the compost^[91]. In experiments investigating the preservation of nitrogen and sulfur and the passivation of heavy metals during the composting of sewage sludge with KH₂PO₄ and FeSO₄, it was found that the addition of KH₂PO₄ and FeSO₄ resulted in a significant reduction in the rate of N loss during the composting process^[92]. The addition of KH₂PO₄ resulted in lower migration rates of Cu, Zn and Pb after composting compared to before composting. Also, the addition of FeSO₄ retained more nitrogen. FeSO₄ enhanced the passivating effect of KH₂PO₄ on Pb. He et al.^[93] report the effect of different types and particle sizes of biochar on greenhouse gas and ammonia emissions during composting. Compared to powdered biochar, granular biochar improved pore connectivity, favored methanogenic activity and reduced CH₄ emissions. At the same particle size, bamboo biochar had higher pore volume and better aerobic microenvironment than straw biochar. Bamboo biochar had a higher concentration of aromatic compounds and NO₃⁻, which inhibits denitrifying bacteria and reduces N₂O emissions. The effects of biochar and soybean residue on nitrifying and denitrifying bacteria and on NH₃ and N₂O emissions were in vestigated^[94]. The soybean residue + biochar treatment produced significantly lower peak NH₃ and N₂O emissions compared to the soybean residue treatment. This was mainly due to the suppression of NH₃ and N₂O emissions by limiting nitrification and denitrification during the composting process, reduced nitrogen losses from the composting process.

6 OUTLOOK

As discussed above, heavy metal passivation and nitrogen retention in pig manure composting are issues that need to be urgently addressed. Especially, the mechanism of heavy metal passivation needs to be further investigated and new additives discovered. It is not difficult to see the limitations in the above studies and experiments summarized above. Here, several aspects that need to be addressed and emphasized in future research are:

(1) Most of the studies were small-scale, lacking large-scale trials for validation, and it is uncertain if the benefits of the additives tested, such as biochar for pig manure composting, will occur in large-scale practice. Theories and results from the laboratory need to be scaled up in practice to verify their effectiveness.

(2) In recent years, many studies on composting pig manure or other livestock manure have focused on compost gas emissions and nitrogen retention. There is a lack of follow-up research on the effects of compost products on improving the soil environment and enhancing soil microorganisms after intensive use. More field trials are needed to assess the potential of additive composts, such as biochar, in the agro-environment and resource use of processed manure.

(3) In many trials on compost additives the additives were pretreated under certain conditions. In real life production, it is necessary to consider the cost of additives and the complexity of the composting process, both for companies and individuals. Therefore, research needs to control the actual cost of the method or the additives while considering factors such as improving the composting effect.

(4) More sustainable materials or additives need to be developed and researched, for example, developing combinations of additives that reduce the use of physical and chemical additives, starting with microorganisms as renewable additives.

7 CONCLUSIONS

This article has reviewed research progress on heavy metal passivation and nitrogen retention in pig manure composting in recent years. There has been considerable progress in the passivation of heavy metals. For the treatment of heavy metals in compost for production applications, physical additives are still the main choice, due to their wide availability and simplicity of operation, but their heavy metal passivation is insufficient. Chemical and microbiological additives have yet to be further promoted for practical production applications. Chemical passivators are effective, technically mature and time-consuming, but as the volume of manure treated increases, so does the consumption of passivators, which not only increases costs but also makes subsequent treatment more likely to cause secondary pollution. Microbial additives for passivation of heavy metals have advantages over physical and chemical methods, and are more economic and effective, but the difficulty of extracting microorganisms from microbial passivators is a challenge that must be faced. For current production applications dealing with heavy metals in compost, the main choice is still physical additives, mainly because of the wide range of sources and simplicity of operation. Therefore, in promoting the application of new heavy metal passivators, the ease and time of use is also a points that needs more attention.

For the retention of nitrogen during composting, the main focus is reducing the emission of nitrogenous gases and the solid nitrogen content. Physical additives are generally natural or synthetic substances with a large surface area and strong adsorption properties to ammonia and ammonium ions, reducing their conversion to ammonia. Chemical additives reduce the loss of nitrogen from the compost by adding chemicals, nitrification inhibitors and inducers of guano stone crystallization. Microbial additives alter the metabolism of carbon and nitrogen by adding exogenous microorganisms, such as ammonia oxidizing archaea, thermophilic ammonia tolerant bacteria, nitrogen fixing bacteria and nitrifying bacilli, thus retaining more nitrogen in the compost. Currently physical, chemical and microbial additives each have their own advantages in terms of nitrogen retention in compost. Combining all three additives is a key area for future research. Compound additives can reduce the overall amount of additives used, and show great promise for both nitrogen retention and heavy metal passivation in compost.

References

[1] Tan Y. Forecast analysis of China’s pig market in 2022. Northern Animal Husbandry, 2022, (8): 10−12 (in Chinese)

[2] Zhao S, Schmidt S, Qin W, Li J, Li G, Zhang W. Towards the circular nitrogen economy—A global meta-analysis of composting technologies reveals much potential for mitigating nitrogen losses. Science of the Total Environment, 2020, 704: 135401

[3] Yao X F, Zhou H B, Meng H B, Ding J T, Shen Y J, Cheng H S, Zhang X, Li R, Fan S Y. Amino acid profile characterization during the co-composting of a livestock manure and maize straw mixture. Journal of Cleaner Production, 2021, 278: 123494

[4] Liu W R, Zeng D, She L, Su W X, He D C, Wu G Y, Ma X R, Jiang S, Jiang C H, Ying G G. Comparisons of pollution characteristics, emission situations, and mass loads for heavy metals in the manures of different livestock and poultry in China. Science of the Total Environment, 2020, 734: 139023

[5] Shao D, Zhan Y, Zhou W, Zhu L. Current status and temporal trend of heavy metals in farmland soil of the Yangtze River Delta Region: field survey and meta-analysis. Environmental Pollution, 2016, 219: 329–336

[6] Zhang W, Shi J. Effects of different passivators and vermicomposting on fractionations of copper and zinc in pig manure. Journal of Zhejiang University, 2017, 43(6): 775–786

[7] Wang F. The effect of high zinc on liver fat metabolism in piglets and its mechanism of action. Dissertation for the Doctoral Degree. Hangzhou: Zhejiang University, 2010 (in Chinese)

[8] Ding H, Zhang Q, Xu H, Yu X, Chen L, Wang Z, Feng J. Selection of copper and zinc dosages in pig diets based on the mutual benefit of animal growth and environmental protection. Ecotoxicology and Environmental Safety, 2021, 216: 112177

[9] Yuan G J, Lu S H, Mei X X, Pang R L. Extended understanding of soil contamination risk control standards for agricultural soils and analysis of the current status of their evaluation criteria. China Agricultural Science Bulletin, 2020, 36(2): 84−89 (in Chinese)

[10] Meng H J, Jiang H L, Zhu S X, Hui S Z, Kong X J, Yang H T. Effect of trace elements in feed on livestock tissues and environment. Heilongjiang Animal Husbandry and Veterinary, 2017, (2): 4 (in Chinese)

[11] Peng H, Chen Y, Weng L, Ma J, Ma Y, Li Y, Islam M S. Comparisons of heavy metal input inventory in agricultural soils in North and South China: a review. Science of the Total Environment, 2019, 660: 776–786

[12] Leclerc A, Laurent A. Framework for estimating toxic releases from the application of manure on agricultural soil: National release inventories for heavy metals in 2000–2014. Science of the Total Environment, 2017, 590-591: 452–460

[13] Yang S, Wen Q, Chen Z. Impacts of Cu and Zn on the performance, microbial community dynamics and resistance genes variations during mesophilic and thermophilic anaerobic digestion of swine manure. Bioresource Technology, 2020, 312: 123554

[14] Jiang P, Jin S Y, Hao X Z, Zhou D M, Li L Z, Lv J L. Distribution characteristics of heavy metals in feeds, pig manures,soils and vegetables. Journal of Agro-Environment Science, 2010, 29(5): 942−947 (in Chinese)

[15] Zhao R, WU Z S, Luo Y, Dong L,Wang S N, Wang H B, Yu L H. Correlation analysis of heavy metals accumulation pollution in pig manure and farmland soil. Soils, 2017, 49(4): 753−759 (in Chinese)

[16] Meng J. Application of heavy metal morphology changes and products in pig manure piling and pyrolysis. Dissertation for the Doctoral Degree. Hangzhou: Zhejiang University, 2014 (in Chinese)

[17] Tessier A, Campbell P G C, Bisson M. Sequentia extraction procedure for the speciation of particulate trace metals. Analytical Chemistry, 1979, 51(7): 844–851

[18] Ma L Q, Rao G N. Effects of phosphate rock on sequential chemical extraction of lead in contaminated soils. Journal of Environmental Quality, 1997, 26(3): 788–794

[19] Rosado D, Usero J, Morillo J. Ability of 3 extraction methods (BCR, Tessier and protease K) to estimate bioavailable metals in sediments from Huelva estuary (Southwestern Spain). Marine Pollution Bulletin, 2016, 102(1): 65–71

[20] Uizhenhe R. Uptake rate of heavy metals by plant with respect to their content and form in soil in the east suburbs beijing. Acta Ecologica Sinica, 1983, 3(3): 277–297

[21] Laperche V, Logan T J, Gaddam P, Traina S. Effect of apatite amendments on plant uptake of lead from contaminated soil. Environmental Science & Technology, 1997, 31(10): 2745–2753

[22] Conder J M, Lanno R P, Basta N T. Assessment of metal availability in smelter soil using earthworms and chemical extractions. Journal of Environmental Quality, 2001, 30(4): 1231–1237

[23] Huang D, Yang Y Q, Xiao X H, Zhang Z Q, Chen S H, Huang Z H, Xiao H N. Technology for measuring bioavailability of heavy metals in soil. Modern Chemical Industry, 2019, 39(S1): 89–94, 98 (in Chinese)

[24] Chen D, Liu X, Bian R, Cheng K, Zhang X, Zheng J, Joseph S, Crowley D, Pan G, Li L. Effects of biochar on availability and plant uptake of heavy metals—A meta-analysis. Journal of Environmental Management, 2018, 222: 76–85

[25] Thomas N A. Use of biomonitoring to control toxics in the United States. Water Science and Technology, 1988, 20(10): 101–108

[26] McCarty L S, Mackay D. Enhancing ecotoxicological modeling and assessment. Body residues and modes of toxic action. Environmental Science & Technology, 1993, 27(9): 1718–1728

[27] He J Q, Liu D H, Deng L, Chang H W, Qin H, Yin Z Y. Bioavailability and exposure assessment of cadmium in farmland soil: a review. Asian Journal of Ecotoxicology, 2017, 12(6): 69–82

[28] Dai Y C. The research of affecting factors and evaluation methods of cadmium and arsenic bioavailability in soils. Dissertation for the Doctoral Degree. Yangling: Northwest A&F University, 2018

[29] He Z M. Effects of passivator on transformation of heavy metal forms and its bioavailability in pig manure composting. Dissertation for the Doctoral Degree. Changsha: Hunan Agricultural University, 2011

[30] Li Y J, Feng Y Q, Zhao Y Y, Shi H Z. A review of the absorption and utilization of different nitrogen forms and their effects on plant physiological metabolism. Journal of Agricultural Science and Technology, 2022 [Published Online] doi: 10.13304/j.nykjdb.2021.0909

[31] Jiang J, Liu X, Huang Y, Huang H. Inoculation with nitrogen turnover bacterial agent appropriately increasing nitrogen and promoting maturity in pig manure composting. Waste Management, 2015, 39: 78–85

[32] Chen X, Zhao Y, Zhang C, Zhang D, Yao C, Meng Q, Zhao R, Wei Z. Speciation, toxicity mechanism and remediation ways of heavy metals during composting: a novel theoretical microbial remediation method is proposed. Journal of Environmental Management, 2020, 272: 111109

[33] Awasthi M K, Duan Y, Awasthi S K, Liu T, Chen H, Pandey A, Zhang Z, Taherzadeh M J. Emerging applications of biochar: improving pig manure composting and attenuation of heavy metal mobility in mature compost. Journal of Hazardous Materials, 2020, 389: 122116

[34] Zhang M Y, Liang W, Tu Z N, Li R H, Zhang Z Q, Ali A, Xiao R. Succession of bacterial community during composting: dissimilarity between compost mixture and biochar additive. Biochar, 2021, 3(2): 229–237

[35] Laird D, Fleming P, Wang B, Horton R, Karlen D. Biochar impact on nutrient leaching from a Midwestern agricultural soil. Geoderma, 2010, 158(3−4): 436−442

[36] Turan V, Khan S A, Mahmood-Ur-Rahman , Iqbal M, Ramzani P M A, Fatima M. Promoting the productivity and quality of brinjal aligned with heavy metals immobilization in a wastewater irrigated heavy metal polluted soil with biochar and chitosan. Ecotoxicology and Environmental Safety, 2018, 161: 409–419

[37] Beesley L, Moreno-Jiménez E, Gomez-Eyles J L. Effects of biochar and greenwaste compost amendments on mobility, bioavailability and toxicity of inorganic and organic contaminants in a multi-element polluted soil. Environmental Pollution, 2010, 158(6): 2282–2287

[38] Duan C, Ma T, Wang J, Zhou Y. Removal of heavy metals from aqueous solution using carbon-based adsorbents: a review. Journal of Water Process Engineering, 2020, 37: 101339

[39] Kong Y, Ma R, Li G, Wang G, Liu Y, Yuan J. Impact of biochar, calcium magnesium phosphate fertilizer and spent mushroom substrate on humification and heavy metal passivation during composting. Science of the Total Environment, 2022, 824: 153755

[40] Ingelmo F, Molina M J, Soriano M D, Gallardo A, Lapeña L. Influence of organic matter transformations on the bioavailability of heavy metals in a sludge based compost. Journal of Environmental Management, 2012, 95(Suppl): S104–S109

[41] Yang S, Wen Q, Chen Z. Effect of KH₂PO₄-modified biochar on immobilization of Cr, Cu, Pb, Zn and as during anaerobic digestion of swine manure. Bioresource Technology, 2021, 339: 125570

[42] Zhou H, Meng H, Zhao L, Shen Y, Hou Y, Cheng H, Song L. Effect of biochar and humic acid on the copper, lead, and cadmium passivation during composting. Bioresource Technology, 2018, 258: 279–286

[43] Chen Z, Bao H, Wen Q, Wu Y, Fu Q. Effects of H₃PO₄ modified biochar on heavy metal mobility and resistance genes removal during swine manure composting. Bioresource Technology, 2022, 346: 126632

[44] Wang J, Hao X, Liu Z, Guo Z, Zhu L, Xiong B, Jiang D, Shen L, Li M, Kang B, Tang G, Bai L. Biochar improves heavy metal passivation during wet anaerobic digestion of pig manure. Environmental Science and Pollution Research International, 2021, 28(1): 635–644

[45] Cui H, Ou Y, Wang L, Yan B, Li Y, Ding D. The passivation effect of heavy metals during biochar-amended composting: emphasize on bacterial communities. Waste Management, 2020, 118: 360–368

[46] Wang Y M. Effect of biochar on the maturity of pig manure compost and the passivation effect of heavy metals. Thesis for the Master’s Degree. Alaer, China: Tarim University, 2021 (in Chinese)

[47] Sanchez-Monedero M A, Cayuela M L, Roig A, Jindo K, Mondini C, Bolan N. Role of biochar as an additive in organic waste composting. Bioresource Technology, 2018, 247: 1155–1164

[48] Cui H, Ou Y, Wang L, Yan B, Li Y, Bao M. Critical passivation mechanisms on heavy metals during aerobic composting with different grain-size zeolite. Journal of Hazardous Materials, 2021, 406: 124313

[49] Wang L, Liu H, Prasher S O, Ou Y, Yan B, Zhong R. Effect of inorganic additives (rock phosphate, PR and boron waste, BW) on the passivation of Cu, Zn during pig manure composting. Journal of Environmental Management, 2021, 285: 112101

[50] Xu Y, Bai T, Yan Y, Ma K. Influence of sodium hydroxide addition on characteristics and environmental risk of heavy metals in biochars derived from swine manure. Waste Management, 2020, 105: 511–519

[51] Li Y, Gong X L, Cui T H, Rong F Z, Zhang X X, Zhang Z, Gu S Y, Yi W M. Effect of bentonite on the passivation of heavy metal chromium by anaerobic fermentation of pig manure. Transactions of the Chinese Society of Agricultural Engineering, 2021, 37(8): 195−203 (in Chinese)

[52] Wu S, Shen Z, Yang C, Zhou Y, Li X, Zeng G, Ai S, He H. Effects of C/N ratio and bulking agent on speciation of Zn and Cu and enzymatic activity during pig manure composting. International Biodeterioration & Biodegradation, 2017, 119: 429–436

[53] Lin H, Sun W, Yu Y, Ding Y, Yang Y, Zhang Z, Ma J. Simultaneous reductions in antibiotics and heavy metal pollution during manure composting. Science of the Total Environment, 2021, 788: 147830

[54] Liu C, Tong Q, Li Y, Wang N, Liu B, Zhang X. Biogas production and metal passivation analysis during anaerobic digestion of pig manure: effects of a magnetic Fe₃O₄/FA composite supplement. RSC Advances, 2019, 9(8): 4488–4498

[55] Liphadzi M S, Kirkham M B, Mankin K R, Paulsen G M. EDTA-assisted heavy-metal uptake by poplar and sunflower grown at a long-term sewage-sludge farm. Plant and Soil, 2003, 257(1): 171–182

[56] Zhang S Q, Zhang F D, Liu X M, Wang Y J, Zhang J F. Degradation of antibiotics and passivation of heavy metals during thermophilic composting process. Scientia Agricultura Sinica, 2006, (2): 337–343 (in Chinese)

[57] Pan X, Zhang D, Wang J, He G, Zhang J, Huang C. Different effects of EDTA on uptake and translocation of Pb and Cd by Typha latifolia. Chinese Journal of Geochemistry, 2006, 25(S1): 133

[58] Chen Y X, Hua Y M, Zhang S H, Tian G M. Transformation of heavy metal forms during sewage sludge bioleaching. Journal of Hazardous Materials, 2005, 123(1–3): 196–202

[59] Qu T X. Study on remediation of heavy metals zinc chromium and cadmium in soil by biological leaching. Thesis for the Master’s Degree. Hefei: Hefei University of Technology, 2021 (in Chinese)

[60] Ferreira J A, Mahboubi A, Lennartsson P R, Taherzadeh M J. Waste biorefineries using filamentous ascomycetes fungi: present status and future prospects. Bioresource Technology, 2016, 215: 334–345

[61] Lu J, He M M. Research progress of aerobic composting treatment of river bottom sediment. Zhejiang Agricultural Science, 2017, 58(8): 1456–1461, 1464 (in Chinese)

[62] Jiang L, Liu X, Yin H, Liang Y, Liu H, Miao B, Peng Q, Meng D, Wang S, Yang J, Guo Z. The utilization of biomineralization technique based on microbial induced phosphate precipitation in remediation of potentially toxic ions contaminated soil: a mini review. Ecotoxicology and Environmental Safety, 2020, 191: 110009

[63] Li R, Meng H, Zhao L, Zhou H, Shen Y, Zhang X, Ding J, Cheng H, Wang J. Study of the morphological changes of copper and zinc during pig manure composting with addition of biochar and a microbial agent. Bioresource Technology, 2019, 291: 121752

[64] Cui J L, Wang Z Z. Study on the removal effect of heavy metals from sewage sludge by biological leaching. Journal of Taiyuan University of Technology, 2011, 42(4): 383−387 (in Chinese)

[65] Cao L, Keener H, Huang Z, Liu Y, Ruan R, Xu F. Effects of temperature and inoculation ratio on methane production and nutrient solubility of swine manure anaerobic digestion. Bioresource Technology, 2020, 299: 122552

[66] Luo T X, Wu W C. Review on the effect of earthworms on composting of livestock and poultry manure. Heilongjiang Animal Science and Veterinary Medicine, 2019, (05): 36−41 (in Chinese)

[67] Xiang S, Lu F, Liu Y, Ruan R. Pretreated rice straw improves the biogas production and heavy metals passivation of pig manure containing copper and zinc. Journal of Cleaner Production, 2021, 315: 128171

[68] Liu Y L, Tie B Q. Research Process on Treatment of Cadmium Contaminated Soil by Microbial Remediation. In: The 6th Workshop on Heavy Metal Pollution Prevention and Risk Assessment and the 2016 Annual Academic Conference of the Professional Committee on Heavy Metal Pollution Prevention and Control. Beijing: Chinese Society for Environmental Sciences, 2016 (in Chinese)

[69] Feng C, Yang G, Du J, Wu B X, Yuan J, Jiang X Y, Qin R B, Zheng Y. Study on the changes of total contents and the status of heavy metals for sewage sludge composting. Research of Environmental Sciences, 2008, 21(1): 97−102 (in Chinese)

[70] Shan G H, Li W G, Gao Y J, Tan W, Xi B D. Additives for reducing nitrogen loss during composting: a review. Journal of Cleaner Production, 2021, 307: 127308

[71] Cáceres R, Malińska K, Marfà O. Nitrification within composting: a review. Waste Management, 2018, 72: 119–137

[72] Wang S G, Zeng Y. Ammonia emission mitigation in food waste composting: a review. Bioresource Technology, 2018, 248(Pt A): 13–19

[73] Deng L, Zhao Y, Zhang J, Bello A, Sun Y, Han Y, Wang B, Uzoamaka Egbeagu U, Li D, Jong C, Xu X. Insight to nitrification during cattle manure-maize straw and biochar composting in terms of multi-variable interaction. Bioresource Technology, 2021, 323: 124572

[74] Zhao Y, Li W, Chen L, Meng L, Zheng Z. Effect of enriched thermotolerant nitrifying bacteria inoculation on reducing nitrogen loss during sewage sludge composting. Bioresource Technology, 2020, 311: 123461

[75] Li Q, Guo X, Lu Y, Shan G, Huang J. Impacts of adding FGDG on the abundance of nitrification and denitrification functional genes during dairy manure and sugarcane pressmud co-composting. Waste Management, 2016, 56: 63–70

[76] Jiang T, Ma X, Yang J, Tang Q, Yi Z, Chen M, Li G. Effect of different struvite crystallization methods on gaseous emission and the comprehensive comparison during the composting. Bioresource Technology, 2016, 217: 219–226

[77] Wang Q, Awasthi M K, Ren X, Zhao J, Li R, Wang Z, Wang M, Chen H, Zhang Z. Combining biochar, zeolite and wood vinegar for composting of pig manure: the effect on greenhouse gas emission and nitrogen conservation. Waste Management, 2018, 74: 221–230

[78] Chen Y X, Huang X D, Han Z Y, Huang X, Hu B, Shi D Z, Wu W X. Effects of bamboo charcoal and bamboo vinegar on nitrogen conservation and heavy metals immobility during pig manure composting. Chemosphere, 2010, 78(9): 1177–1181

[79] Jiang J, Huang Y, Liu X, Huang H. The effects of apple pomace, bentonite and calcium superphosphate on swine manure aerobic composting. Waste Management, 2014, 34(9): 1595–1602

[80] Jiang T, Ma X, Tang Q, Yang J, Li G, Schuchardt F. Combined use of nitrification inhibitor and struvite crystallization to reduce the NH₃ and N₂O emissions during composting. Bioresource Technology, 2016, 217: 210–218

[81] Ren X, Wang Q, Li R, Chang C C, Pan J, Zhang Z. Effect of clay on greenhouse gas emissions and humification during pig manure composting as supported by spectroscopic evidence. Science of the Total Environment, 2020, 737: 139712

[82] Godlewska P, Schmidt H P, Ok Y S, Oleszczuk P. Biochar for composting improvement and contaminants reduction. A review. Bioresource Technology, 2017, 246: 193–202

[83] Liu Y, Ma R, Li D, Qi C, Han L, Chen M, Fu F, Yuan J, Li G. Effects of calcium magnesium phosphate fertilizer, biochar and spent mushroom substrate on compost maturity and gaseous emissions during pig manure composting. Journal of Environmental Management, 2020, 267: 110649

[84] Luo Y, Li G, Luo W, Schuchardt F, Jiang T, Xu D. Effect of phosphogypsum and dicyandiamide as additives on NH₃, N₂O and CH₄ emissions during composting. Journal of Environmental Sciences, 2013, 25(7): 1338–1345

[85] Li Y, Luo W, Li G, Wang K, Gong X. Performance of phosphogypsum and calcium magnesium phosphate fertilizer for nitrogen conservation in pig manure composting. Bioresource Technology, 2018, 250: 53–59

[86] Ye J S, Wu K, Cai J M, Yu Z M, Chen T H. Progress on research methods for microorganisms during aerobic composting. Journal of Anhui Agricultural Sciences, 2008, 36(30): 13287–13291 (in Chinese)

[87] Kuroda K, Waki M, Yasuda T, Fukumoto Y, Tanaka A, Nakasaki K. Utilization of Bacillus sp. strain TAT105 as a biological additive to reduce ammonia emissions during composting of swine feces. Bioscience, Biotechnology, and Biochemistry, 2015, 79(10): 1702–1711

[88] Zhu F X, Hong C L, Wang W P, Lyu H H, Zhu W J, Xv H J, Yao Y L. A microbial agent effectively reduces ammonia volatilization and ensures good maggot yield from pig manure composted via housefly larvae cultivation. Journal of Cleaner Production, 2020, 270: 122373

[89] Guo H, Gu J, Wang X, Nasir M, Yu J, Lei L, Wang J, Zhao W, Dai X. Beneficial effects of bacterial agent/bentonite on nitrogen transformation and microbial community dynamics during aerobic composting of pig manure. Bioresource Technology, 2020, 298: 122384

[90] Li C, Li H, Yao T, Su M, Li J, Liu Z, Xin Y, Wang L, Chen J, Gun S. Effects of microbial inoculation on enzyme activity, available nitrogen content, and bacterial succession during pig manure composting. Bioresource Technology, 2020, 306: 123167

[91] Mao H, Lv Z, Sun H, Li R, Zhai B, Wang Z, Awasthi M K, Wang Q, Zhou L. Improvement of biochar and bacterial powder addition on gaseous emission and bacterial community in pig manure compost. Bioresource Technology, 2018, 258: 195–202

[92] Wang X, Chen T, Zheng G. Preservation of nitrogen and sulfur and passivation of heavy metals during sewage sludge composting with KH₂PO₄ and FeSO₄. Bioresource Technology, 2020, 297: 122383

[93] He X, Yin H, Han L, Cui R, Fang C, Huang G. Effects of biochar size and type on gaseous emissions during pig manure/wheat straw aerobic composting: Insights into multivariate-microscale characterization and microbial mechanism. Bioresource Technology, 2019, 271: 375–382

[94] Yang Y, Kumar Awasthi M, Wu L, Yan Y, Lv J. Microbial driving mechanism of biochar and bean dregs on NH₃ and N₂O emissions during composting. Bioresource Technology, 2020, 315: 123829

Acknowledgements

This work was supported by the National Key Research and Development Program of China (2018YFE0127000), Key R&D Program of Shaanxi Province (2022ZDLNY02-09), China Agriculture Research System (CARS-23-C-05) and Postdoctoral Foundation of the Shaanxi Province (2018BSHEDZZ20).

Compliance with ethics guidelines

Ziqi Wang, Guotao Sun, Jiamin Wang, and Gongshe Yang declare that they have no conflicts of interest or financial conflicts to disclose. This article does not contain any studies with human or animal subjects performed by any of the authors.

RIGHTS & PERMISSIONS

The Author(s) 2023. Published by Higher Education Press. This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0)