Resource Utilization of Biogas Waste as Fertilizer in China Needs More Inspections Due to the Risk of Heavy Metals

Abstract

The utilization of livestock waste has attracted increasing attention in recent years. The presence of high levels of heavy metals is a major obstacle to the utilization of biogas as a fertilizer resource. In this study, the heavy metal contents in biogas residue, slurry, and discharged sewage from three representative farms of gooseries, henneries, and dairy farms in the Yangtze River Basin were investigated and assessed. The results demonstrated that heavy metals, including Cd, Mn, As, Cu, Pb, Cr, Zn, etc., could be detected in all biogas residues, with significantly different contents between farm types (p < 0.005). Specifically, biogas residues from the goosery and the dairy farms met “China’s Organic Fertilizer Standards” (COF Standards); however, Cd concentrations in biogas residues from hennery farms exceeded the limits by five times. The concentrations of Cd and Pb in biogas slurries from all of the farms exceeded the limits of the “China Farmland Irrigation Water Quality Standard” (CFIWQ Standard). In particular, the Pb concentrations in biogas slurry from the dairy farms exceeded the limits by 29 times, and the discharged sewage from all three farm types complied with the comprehensive sewage discharge standards in China; however, only that from the goosery farms was suitable for irrigation. Thus, it is recommended to increase the feed selection, biogas engineering, and biological-purification-supporting technology, and to carry out regular sampling inspections of the biogas residue, slurry, and discharged sewage for heavy metals, so that environmental and crop pollution risks can be reduced when they are used as sources of nutrients for eco-friendly agriculture.

1. Introduction

In the late 20th century, the global research on the utilization of biogas residue (solid fraction) and biogas slurry (liquid fraction) increased rapidly, and countries around the world—including China, India, Pakistan, Germany, Australia, Bangladesh, Finland, Japan, Malaysia, and the United States—began to pay attention to environmental issues, and to pay more attention to the research of biogas slurry [1]. China is the world’s largest producer of livestock and poultry. The livestock and poultry breeding industry is not only a source of animal protein on which people depend, but also an important part of China’s agricultural economy. Compared to 30 years ago, the current per capita consumption of meat in China has increased by 50%, and the demand for livestock, poultry, eggs, milk, cheese and other dairy products is also increasing [2]. With the increase in intensive breeding, China’s livestock and poultry breeding has changed from traditional family sideline businesses to professional breeding households, breeding cooperatives, and breeding enterprises. Large-scale pig farms (>500 heads) and cattle farms (>100 heads) increased from 126,600 and 22,500 in 2008 to 215,500 and 31,500 in 2017, respectively [3,4]. The environmental pollution caused by the fast-developing livestock and poultry breeding industry has become increasingly prominent in China. Therefore, the bioremediation and resource utilization of livestock/poultry waste needs to be addressed urgently [5,6,7,8,9].

The utilization of biogas waste brings not only economic benefits, but also environmental benefits. As a byproduct of anaerobic fermentation of animal manure and crop straw, biogas residues can be used as high-quality organic fertilizer because of their high content of major nutrients such as nitrogen and phosphorus, which are necessary for plant growth. Biogas digestate is environmentally friendly compared to synthetic and fossil fertilizers, because it entails no greenhouse gas emissions or underground water pollution during production [10,11,12]. To produce 1 ton of synthetic fertilizer, 1 ton of oil and 108 tons of water are consumed, and 7 tons of CO₂ are emitted, usually [13], suggesting that the more synthetic fertilizers are used, the more resource consumption and greenhouse gas emissions will be caused. Biogas digestate can reduce chemical fertilizer use by up to 15–25% [10]. Thus, secure application of biogas residue and biogas slurry could finally provide a beneficial means of ecofriendly agriculture. However, biogas fertilizer also contains heavy metals, hormones, pesticide residues, pathogens, and other hazards [14,15], and could cause environmental pollution when it exceeds the environmental capacity per unit area of farmland [16].

China put forward the “Opinions on Accelerating the Utilization of Waste from Livestock and Poultry” in 2017 and the “Work Points for Resource Utilization of Livestock and Poultry Breeding Waste” in 2019 [17], and the government advocates the utilization of biogas residue (solid fraction) and biogas slurry (liquid fraction) based on a combination of planting and breeding. The promulgation and implementation of these reports in China will help to realize not only the recycling of nutrient elements, but also the reduction in environmental pressure caused by the discharge of aquaculture waste [18,19]. In Europe, different regulations and guidelines for anaerobic digestate production and usage can be found [20]. In the United Kingdom (UK), the utilization of anaerobic digestate is subject to environmental permission or licensing [21]. In Ireland, the Irish Bioenergy Association, in consultation with industry, has developed a draft standard for anaerobic digestate use [22], based on reviews of standards and quality assurance throughout Europe. These standards regulate environmental impacts, health risks, and waste management practices in the utilization of biogas residue. However, the utilization of biogas residues after anaerobic digestate as fertilizer still faces challenges in practice, such as different regional economic development, limited farmland, and hazardous contaminants [23,24], making it difficult to establish standard management practices. Biogas fertilizer may contain heavy metals (e.g., Cd, As, Cu, Pb, Cr) derived from the food chain or aquaculture feed additives [25,26,27,28]. These heavy metals not only cause long-term adverse effects to the soil and water environment [27,28,29,30], but can also enter the human body through the food chain, endangering human health [31,32]. Although the safety issues of fertilization have gradually been taken more seriously by scholars [33], there has been no conclusion about the safety of biogas slurry residue for use on cropland until now.

Meanwhile, the nutrient contents available for plant growth in the biogas residue and slurry containing wastewater from different farms are usually different, and the potential pollution risks of heavy metals can also vary greatly [34,35,36]. The number of livestock and poultry breeding farms in Suqian, Jiangsu Province, in the Yangtze River Basin, China, is relatively large. However, the pollution caused by intensive breeding has become a bottleneck, restricting the development of the livestock and poultry breeding industry in this area. We hypothesized that (1) the environmental and crop pollution risks could be reduced by carrying out regular heavy metals inspections of feed, feces, biogas residue, and slurry from different types of farms, and that (2) biogas residue and biogas slurry would provide a beneficial means of eco-friendly agriculture, including reducing the burden of fertilizer on the national economy, improving the sustainability of the fields, and improving the livestock and poultry breeding. Since the research on biogas waste takes “biogas slurry, anaerobic digestion, waste water” as the main line [1], here the heavy metals in biogas residue, biogas slurry, and discharged sewage from three types of farms with more than 500 heads in Suqian were selected in order to investigate how different types of anaerobic digestate vary in terms of their physicochemical properties. The results present the heavy metal contents of biogas waste from different farm types, and shed light on the policies, regulations, and management of the application of biogas waste.

2. Materials and Methods

2.1. Sample Collection

The sample collection area was located in the northern part of Jiangsu Province (33°12′17″~34°24′38″ N, 117°6′19″~119°12′50″ E), in a warm temperate monsoon climate zone. The average temperature is 14.2 °C, and the average annual precipitation is 910 mm. Six farms for each type of the Suyu henneries, Shuyang gooseries, and Sihong dairy farms, with a production volume of more than 500 heads, were sampled for detection and evaluation (Figure 1). The front-end manure treatment mode of the selected farms is an above-ground biogas project, which is composed of an above-ground fermentation tank, a biogas residue storage, a biogas slurry sedimentation tank, and a discharged water storage tank (Figure 2). Based on the principle of random sampling, 18 samples for each farm were collected from the biogas residue storage, the biogas slurry sedimentation tank, and the discharged water storage tank, respectively, including 6 replicates of biogas residue, biogas slurry, and sewage samples.

2.2. Sample Testing

After collection, the biogas residues were dried at 70 °C and then sieved with a 40-mesh sieve; 0.500 ± 0.010 g of each sample was weighed and digested with 8 mL of nitric acid by microwave, and then placed in an acid purifier. At 150 °C, the acid was dried until approximately 1 mL remained, and then a volume of 50 mL was prepared. For the biogas slurry, 5 mL of the sample was added to 5 mL of nitric acid for microwave digestion. The subsequent steps were the same as the biogas residue sample preparation, and the final volume was adjusted to 50 mL for testing. A continuous light source atomic absorption spectrometer (contrAA700, Analytik Jena, Jena, Germany) was used to measure the K, Ca, Na, Mg, Fe, and Zn concentrations via flame atomic absorption spectrometry, and to determine the Cd, Cr, Pb, Cu, and Mn concentrations via graphene atomic absorption spectrometry [37,38,39]. An atomic fluorescence instrument (8500, Beijing Haiguang Instrument, Beijing, China) was used to determine the As concentrations.

2.3. Safety Assessment of Heavy Metals

The agricultural use limits of heavy metals in biogas residue refer to “China’s Organic Fertilizer Standards” (NY 525-2012) (COF Standards) and the “German Standards for Rotten Composting” [40,41]. The limits of heavy metals in biogas slurry and sewage refer to the “Farmland Irrigation Water Quality Standard” (GB5084-2005), “Sewage Comprehensive Emission Standard” (GB8978-1996), and “Water Pollutant Discharge Standard for Livestock and Poultry Breeding Industry” (draft for comments) [42,43]. The single-factor pollution index method and the Nemerow pollution index method were employed for the safety assessments in this study [44,45].

The single-factor pollution index (Pi) can be calculated by following Equation (1):

$$\mathrm{Pi}=\frac{\mathrm{Ci}}{\mathrm{Si}}$$

(1)

where Ci is the monitoring value of the pollutant, while Si is the the evaluation standard value of the pollutant. The Nemerow pollution index (Pn) can be calculated by Equation (2):

$$\mathrm{Pn}=\sqrt{\frac{{\left(\frac{\mathrm{Ci}}{\mathrm{Si}}\right)}_{\mathrm{ave}}^2+{\left(\frac{\mathrm{Ci}}{\mathrm{Si}}\right)}_{\max }^2}{2}}$$

(2)

Based on the values of Pi and Pn, the heavy metal pollution can be evaluated as shown in

Table 1. Evaluation criteria for heavy metal pollution.

Single-Factor Pollution Index (Pi)	Nemerow Pollution Index (Pn)	Degree of Contamination
Pi ≤ 1	Pn ≤ 0.7	Safe
1 < Pi ≤ 2	0.7 < Pn < 1	Alert
2 < Pi ≤ 3	1 < Pn < 2	Mild pollution
3 < Pi ≤ 5	2 < Pn < 3	Moderate pollution
Pi > 5	Pn > 3	Serious pollution

. All data, based on the above investigation, were processed and analyzed using Excel 2010 and SPSS 22.0.

3. Results and Discussion

3.1. Concentrations of Heavy Metals

3.1.1. Concentrations of Heavy Metals in Biogas Residue from Three Types of Farms

Biogas residue and slurry are rich in organic matter and nutrient elements, and returning to the field as fertilizer is the main method of their resource utilization around the world [40]. Toxic heavy metals (e.g., As (promoting smooth fur) or Cr (replacing clenbuterol)), however, are widely added into the feed, resulting in residual heavy metals in livestock manure, biogas residue, biogas slurry, and discharged sewage [26,27,28]. In the biogas residues from all three farm types involved in this study, the detection rates of heavy metals (e.g., Cd, Mn, As, Cu, Pb, Cr, Zn) were 100%. Zn had the highest elemental content, followed by Cu, Cr, Pb, and As, while Cd and Mn had the lowest (Figure 3). Zhao et al. [46] showed that Cd and Cr concentrations in the soil where biogas residues were used as fertilizer increased slightly compared with the control, which used pure water. Chen et al. [47] showed that the contents of four heavy metal elements were increased along with cultivation time as a whole, and the increase varied in the order of Hg>Cd>Pb>As. In addition, it has been recognized that the speciation of heavy metals, in addition to the total concentrations, also needs to be considered when assessing the eco-toxicity and the bioavailability of metals in the environment [48,49,50,51,52]. In the present study, the results indicate that the biogas residues produced in different livestock and poultry breeding farms contain different kinds and contents of heavy metals. Because the levels of heavy metal bioavailability and toxicity are affected by many factors, and can be influenced by interactions between anaerobic digestate, soil, and plants [53], the ecological impact on farmland and the bioavailability of heavy metals for the main local crops when using biogas residue organic fertilizer should be further studied in the near future. As shown in Figure 3, the concentration of each specific heavy metal element in the biogas residue varied significantly between the farm types (p < 0.05), which can mostly be attributed to the different types of feedstock utilized, along with the non-feed additives and mineral additives [54,55]. However, the influence of the anaerobic process on the speciation of heavy metals should be clarified in future studies.

3.1.2. Concentrations of Heavy Metals in Biogas Slurry from Three Types of Farms

As shown in Figure 4a, it was found that in the biogas slurry from the Sihong dairy farms, all seven heavy metal elements were detected, and their concentrations followed the sequence of Zn (1286.67 μg/L) > Pb (2901.33 μg/L) > Mn (1580.00 μg/L) > Cu (178.80 μg/L) > Cd (57.69 μg/L) > As (32.44 μg/L) > Cr (11.99 μg/L). In the biogas slurry from the Suyu henneries, six heavy metal elements were detected, and their concentrations followed the sequence of Zn (586.67 μg/L) > Cu (144.20 μg/L) > Pb (102.6 μg/L) > Mn (53.95 μg/L) > Cd (41.09 μg/L) > As (10.33 μg/L). Meanwhile, in the biogas slurry from the Shuyang gooseries, six heavy metal elements were detected, and their concentrations followed the sequence of Zn (1154.67 μg/L) > Pb (112.07 μg/L) > Mn (86.87 μg/L) > Cd (47.47 μg/L) > As (26.39 μg/L) > Cu (12.44 μg/L). These results indicate that both the detection rates and the concentrations of heavy metals in biogas residues and slurries from the three farm types were high. This could bring a certain risk of enrichment of soil with heavy metals if biogas residues or slurries were used as fertilizer in the long term, without any treatment. In particular, the heavy metals favor the solid biogas residue rather than biogas slurry after anaerobic digestion [56,57]. Over a long period, in the uneven development of the feed industry, feed companies in China have faced the following problems: (1) lack of knowledge on feed quality and safety; (2) lack of knowledge of regulations among business practitioners; and (3) excessive market pursuit of nutritive indices and economic benefits. All of the above leads to additives beyond normal level in animal feed, causing high contents of different heavy metals in biogas residue and slurry. On the other hand, biogas slurry has significant potential to improve the physical and biological quality of soil, in addition to providing both macro- and micronutrients to crops. Increasing yield due to the application of biogas slurry has also been reported in many crops, including cereal crops, tobacco, castor, peas, mustard, onion, cabbage, banana, chilies, pearl millet, and sugarcane [10]. The high costs of synthetic fertilizers make it essential for most developing and African countries to find alternative fertilizers, and the use of biogas slurry could reduce the application of synthetic fertilizers by up to 15–20% [58]. Thus, the reduction treatment of heavy metals should be carried out before the application of biogas residue and slurry as organic fertilizers in farmland. Moreover, the concentrations of all heavy metals in the biogas slurry from the Sihong dairy farms were significantly higher than those from the Suyu henneries and the Shuyang gooseries.

3.1.3. Concentrations of Heavy Metals in Sewage from Three Types of Farms

As shown in Figure 4b, all seven heavy metal elements were detected in the discharged sewage from the Sihong dairy farms, and their concentrations followed the sequence of Zn (216.67 μg/L) > Pb (215.8 μg/L) > Mn (72.45 μg/L) > Cu (24.57 μg/L) > Cd (19.62 μg/L) > As (7.16 μg/L) > Cr (1.17 μg/L). This is consistent with the heavy metal concentrations in the biogas slurry from these farms. In the discharged sewage from the Suyu henneries, five heavy metal elements were detected, and their concentrations followed the sequence of Cu (24.27 μg/L) > Cd (23.75 μg/L) > Zn (12.57 μg/L) > Mn (8.89 μg/L) > As (4.65 μg/L). In the discharged sewage from the Shuyang gooseries, four heavy metal elements were detected, and their concentrations followed the sequence of Zn (82.33 μg/L) > As (22.87 μg/L) > Mn (2.08 μg/L) > Cd (0.27 μg/L). In summary, discharged sewage from the Sihong dairy farms contained the highest number of heavy metal elements, and the highest concentrations of Zn, Mn, Cu, Pb, and Cr. Additionally, the concentration of Cd was the highest in the discharged sewage from the Suyu henneries, while the highest concentration of As occurred in the discharged sewage from the Shuyang gooseries. There is a risk of Cd, Pb, and As pollution in the discharged sewage from the Suyu henneries, Sihong dairy farms, and Shuyang gooseries, respectively; for agricultural use, their reduction treatment should be carried out before the irrigation of the farmland. However, heavy metals in the water-soluble fraction of the discharged sewage deserve more attention, due to their direct toxicity to the environment and other living organisms [59].

3.2. Concentration of Mineral Elements

3.2.1. Concentrations of Mineral Elements in Biogas Residue from Three Types of Farms

As shown in Figure 5 and Figure 6, all six mineral elements were detected in the biogas residue, biogas slurry, and sewage from all three farm types, and their contents were high. Concentrations of K, Na, and Mg in biogas residues from the three farm types followed the sequence of Sihong dairy farms > Suyu henneries > Shuyang gooseries (Figure 5). There were significant differences in the contents of the mineral elements between the three farm types. The Fe content in the biogas residue from the Shuyang gooseries was significantly higher than that of the other two farm types, but the Ca content was significantly lower than that of the other two farm types. Meanwhile, concentrations of mineral elements in biogas residues from the Sihong dairy farms followed the sequence of Ca (68.38 g/kg) > K (54.41 g/kg) > Na (40.30 g/kg) > Mg (25.14 g/kg) > Fe (3.61 g/kg). Concentrations of mineral elements in biogas residues from the Suyu henneries followed the sequence of Ca (67.11 g/kg) > Mg (18.59 g/kg) > Na (7.15 g/kg) > Fe (5.76 g/kg) > K (3.32 g/kg), and concentrations of mineral elements in biogas residues from the Shuyang gooseries followed the sequence of Ca (32.25 g/kg) > Fe (14.31 g/kg) > Mg (9.32 g/kg) > K (3.40 g/kg) > Na (2.40 g/kg). Hence, the concentration of Ca in the biogas residues from all of the different farm types was significantly higher than that of other mineral elements; however, the concentration and order of mineral elements varied between farm types.

3.2.2. Concentrations of Mineral Elements in Biogas Slurry from Three Types of Farms

Although concentrations of all mineral elements were significantly higher in biogas slurry from the Sihong dairy farms than in that from both the Suyu henneries and the Shuyang gooseries, concentrations of mineral elements in sewage from the Sihong dairy farms were not significantly higher than those from the Suyu henneries and the Shuyang gooseries (Figure 6a). Concentrations of mineral elements in biogas slurry from the Sihong dairy farms followed the sequence of K (848.53 mg/L) > Na (778.54 mg/L) > Mg (242.18 mg/L) > Ca (25.46 mg/L) > Fe (11.99 mg/L); concentrations of mineral elements in biogas slurry from the Suyu henneries followed the sequence of Na (186.80 mg/L) > K (137.97 mg/L) > Mg (101.51 mg/L) > Ca (11.91 mg/L) > Fe (0.49 mg/L); and the concentrations of mineral elements in biogas slurry from the Shuyang gooseries followed the sequence of Na (137.01 mg/L) > K (51.86 mg/L) > Mg (48.07 mg/L) > Ca (11.53 mg/L) > Fe (1.54 mg/L). In other words, there was a high similarity in the order of contents of mineral elements in biogas slurry between the three farm types.

3.2.3. Concentrations of Mineral Elements in Sewage from Three Types of Farms

As shown in Figure 6b, the concentrations of mineral elements in discharged sewage from the Sihong dairy farms followed the sequence of Na (135.73 mg/L) > Mg (35.11 mg/L) > K (18.52 mg/L) > Ca (7.28 mg/L) > Fe (0.66 mg/L); concentrations of mineral elements in discharged sewage from the Suyu henneries followed the sequence of Na (128.37 mg/L) > Mg (35.11 mg/L) > K (18.52 mg/L) > Ca (7.28 mg/L) > Fe (0.66 mg/L); and the concentrations of mineral elements in discharged sewage from the Shuyang gooseries followed the sequence of Na (130.47 mg/L) > Mg (42.45 mg/L) ≥ K (42.43 mg/L) > Ca (11.33 mg/L) > Fe (0.52 mg/L). In summary, although the concentrations of the mineral elements contained in the discharged sewage of the three farm types were different from the concentrations of the corresponding biogas slurry, the order of the mineral elements in the discharged sewage of each site was the same.

3.3. Safety Assessment

3.3.1. Safety Assessment of Biogas Residues from Three Types of Farms

To date, there have been many studies on the impact of biogas residue and biogas slurry on the yield and quality of crops after being used in the field, but there have been few safety assessments of the reuse of biogas residue and biogas slurry at different sites, or of the reuse of discharged sewage [60,61,62,63]. In this study, a resource utilization safety assessment in terms of heavy metal concentrations was conducted on the biogas residues from the different farm types, according to the COF Standards (

Table 2. Maximum limits of heavy metals in biogas residue, biogas slurry, and sewage.

Type	Criteria	Zn	Cd	As	Cu	Pb	Cr
Biogas residue (mg/kg)	China Organic Fertilizer Standard (NY525-2012) (COF Standards)	-	3	15	-	50	150
	German Standards for Rotten Composting [28]	400	1.5	-	100	150	100
Biogas slurry and sewage (mg/L)	China Discharge Standard of Pollutants for Livestock and Poultry Breeding (GB18596-2001) (CDPLPB Standard)	1.5	-	-	0.5	-	-
	China Integrated Sewage Discharge Standard (GB8978-1996) (CISD Standard)	-	0.1	0.5	-	1.0	1.5
	China Farmland Irrigation Water Quality Standard (GB5084-2005) (CFIWQ Standard)	2.0	0.01	0.05, 0.1	0.5, 1	0.1	0.1

The As standard for paddy fields and vegetable land is ≤0.05 mg/L, and for dry land is ≤0.1 mg/L; the Cu standard for paddy fields is ≤0.5 mg/L, and for dry land and vegetable land is ≤1.0 mg/L.

) [40]. The results showed that concentrations of As, Pb, and Cr in biogas residues from all three farm types were lower than the critical levels, while Cd concentrations in biogas residues from the Sihong dairy farms and the Shuyang gooseries were lower than the critical level (3.0 mg/kg) (Figure 3 and Table 2). Since Zn and Cu are not limited in the COF Standards, the “German Standards for Rotten Composting” were used for the safety assessment. The results demonstrated that concentrations of Zn and Cu in biogas residues from the Sihong dairy farms and the Shuyang gooseries were significantly lower than the critical levels (400 and 100 mg/kg, respectively; see Figure 3 and Table 2) [41]. Hence, biogas residues from the Sihong dairy farms and the Shuyang gooseries met the COF Standards and the “German Standards for Rotten Composting”. These biogas residues contained abundant mineral elements, and could be recycled as organic fertilizer after composting. However, the Cd concentration in biogas residues from the Suyu henneries (15.45 mg/kg) was five times that of the critical level (3.0 mg/kg), while concentrations of Zn and Cu in biogas residues from the Suyu henneries exceeded the critical levels (400 and 100 mg/kg, respectively). It is therefore recommended that the Suyu henneries strengthen their feed quality inspection and safety practices, and improve the treatment efficiency of biogas projects.

Assessment by the single-factor pollution index method revealed that heavy metal concentrations in biogas residues from the Sihong dairy farms and the Shuyang gooseries were all at safe levels, while concentrations of Zn, Cu, and Cr in biogas residues from the Suyu henneries were at a pollution level (

Table 3. Heavy metal pollution indices of biogas residues, biogas slurries, and sewage water from three different farm types.

Type	Farm	Single-Factor Pollution Index (Pi)						Nemerow Pollution Index (Pn)
		Zn	Cd	Mn	As	Cu	Pb
Biogas residue (based on COF Standards) (NY525-2012)	Dairy	0.58 Safe	0.56 Safe	0.28 Safe	0.58 Safe	0.44 Safe	0.08 Safe	3.14 Serious
	Hennery	2.03 Moderate	5.15 Serious	0.22 Safe	1.23 Mild	0.75 Safe	0.25 Safe	2.01 Moderate
	Goosery	0.16 Safe	0.15 Safe	0.71 Safe	0.28 Safe	0.28 Safe	0.80 Safe	1.76 Mild
Biogas slurry (based on CFIWQ Standard, GB5084-2005)	Dairy	0.65 Alert	5.80 Serious	0.64/0.32 Safe	0.18 Safe	29.01 Serious	0.12 Safe	6.71/6.65 Serious
	Hennery	0.29 Safe	4.10 Serious	0.20/0.10 Safe	0.14 Safe	1.02 Mild	- Safe	1.21/1.19 Mild
	Goosery	0.58 Safe	4.80 Serious	0.52/0.26 Safe	0.01 Safe	1.12 Mild)	- Safe	1.45/1.40 Mild
Sewage (based on CFIWQ Standard, GB5084-2005)	Dairy	0.11 Safe	2.00 Moderate	0.14/0.07 Safe	0.03 Safe	2.16 Moderate	0.01 Safe	0.93/0.92 Alert
	Hennery	0.01 Safe	2.40 Moderate	0.10/0.05 Safe	0.02 Safe	- Safe	- Safe	0.63/0.62 Safe
	Goosery	0.04 Safe	0.00 Safe	0.46/0.23 Safe	- Safe	- Safe	- Safe	0.79/0.73 Alert
Sewage (based on CISD Standard, GB8978-1996)	Dairy		0.20 Safe	0.01 Safe		0.22 Safe	0.00 Safe	0.50 Safe
	Hennery		0.24 Safe	0.01 Safe		- Safe	- Safe	0.46 Safe
	Goosery		0.00 Safe	0.05 Safe		- Safe	- Safe	0.12 Safe

COF Standards: China Organic Fertilizer Standard; CFIWQ Standard: China Farmland Irrigation Water Quality Standard; CISD Standard: China Integrated Sewage Discharge Standard.

). This is consistent with assessments according to the COF Standards and the “German Standards for Rotten Composting”. Furthermore, overall evaluations of different heavy metals by the Nemerow pollution index method revealed that the combined pollution of heavy metals in biogas residues from the Sihong dairy farms, the Shuyang gooseries, and the Suyu henneries were serious, mild, and moderate, respectively (Table 3). The Nemerow pollution index provides an environmental pollution risk assessment on the resource utilization of biogas residues, which can be used to effectively ensure the safety of the ecological environment and agricultural production. The results of the Nemerow pollution index highlight how the biogas residues from the different farms have different levels of environmental pollution risks, and are not suitable for farmland utilization. The evaluation of the Nemerow pollution index indicates that the comprehensive pollution of heavy metals in the biogas residue from the Sihong dairy farms is severe. It is therefore recommended to increase the feed selection, biogas engineering, and biological-purification-supporting technology, and to carry out regular sampling inspections of feed, feces, biogas residue, and slurry for heavy metals, so that environmental and crop pollution risks can be reduced when they are returned to the field.

3.3.2. Safety Assessment of Biogas Slurry from Three Types of Farms

A resource utilization safety assessment in terms of heavy metals was applied to biogas slurries from different farms according to the “China Farmland Irrigation Water Quality Standard” (GB5084-2005) (CFIWQ Standard) [42]. The results demonstrated that concentrations of Zn, As, Cu, and Cr in biogas slurries from all three farm types were lower than the critical levels, while concentrations of Cd and Pb in biogas slurries from all three farm types were 0.01 and 0.1 mg/L higher than the critical levels, respectively (Figure 4a and Table 2). The Pb concentration (2.90 mg/L) in biogas slurry from the Sihong dairy farms was particularly high—29 times the critical level (Figure 4a and Table 2). For these reasons, the return of such slurry to the field would cause environmental pollution and Pb enrichment in crops, and eventually lead to human lead poisoning through the food chain. Meanwhile, evaluations of heavy metals in biogas slurry by the single-factor pollution index method revealed that concentrations of Zn, As, Cu, and Cr in biogas slurries from all three farm types were at safe or alert levels, while concentrations of Cd and Pb in biogas slurries from all three farm types were at the pollution level (Table 3). Hence, for the recycling of biogas slurry from the three farm types, Cd and Pb reduction and passivation treatment should be carried out in order to prevent heavy metal pollution of farmland soil and agricultural products [39,64,65]. The overall evaluations of different heavy metals in biogas slurry by the Nemerow pollution index method revealed a Pn > 3 for the Sihong dairy farms, and a Pn = 1–2 for the Suyu henneries and the Shuyang gooseries (Table 3); the former is considered serious pollution, while the latter is considered mild pollution (Table 1). Therefore, comprehensive assessment before resource utilization should be carried out on the biogas slurry in order to ensure safe agricultural use and minimize the ecological and environmental risks of single and multiple heavy metals. The biogas residue and slurry from the Sihong dairy farms, the Shuyang gooseries, and the Suyu henneries are rich in nutrients, but when carrying out nutrient recovery and resource utilization, it is recommended to conduct a comprehensive evaluation beforehand, with consideration of the agricultural and ecological environmental risks of individual and multiple heavy metals.

3.3.3. Safety Assessment of Discharged Sewage from Three Types of Farms

Concentrations of Cd and Pb in discharged sewage from the Sihong dairy farms and Cd concentrations in discharged sewage from the Suyu henneries were two times higher than the critical levels, while concentrations of heavy metals in discharged sewage from the Shuyang gooseries met the CFIWQ Standard (Figure 4b and Table 2). This is consistent with the single-factor pollution index evaluation results based on this standard (Table 3). In other words, concentrations of Cd and Pb in discharged sewage from the Sihong dairy farms, and Cd concentrations in discharged sewage from the Suyu henneries, were at a pollution level, while concentrations of heavy metals in discharged sewage from the Shuyang gooseries were at safe levels (Figure 4b and Table 3). Compared to biogas slurry, there was a great decline in the concentrations of heavy metals in discharged sewage from all three farm types (Figure 4). The Nemerow pollution index analysis showed that the Shuyang gooseries’ sewage was in an alert or safe state (Table 3). This is due to the large amount of dissolved organic matter (DOM) in the biogas slurry, which can interact with heavy metal ions, including Cu²⁺, Cr³⁺, Pb²⁺, Cd²⁺, and Zn²⁺, resulting in complexation, which greatly reduces the water-soluble heavy metal content [29,65]. The discharged sewage of the different farms in this study all passed through a purification pond, artificial wetland, or advanced treatment process, and then was discharged into the environment. The concentrations of Cd, As, Pb, and Cr in discharged sewage from the different farms all met the CFIWQ Standard (Figure 4b and Table 2). This was consistent with the single-factor pollution index assessment results based on this standard—that is, Cd, As, Pb. and Cr in the sewage from the three types of farm were all at safe levels (Table 3). Thus, only the discharged sewage from the Shuyang gooseries can be used for irrigation. The present study focused on the contents of heavy metals in the biogas residues. To further assess the safety of the use of biogas residues as organic fertilizer, the potential risks of hormones, antibiotics, and pathogens in biogas residues should also be considered. If the contaminants accumulate in the soil from applied fertilizer, the permeability and humidity would be increased [66], which could cause deeper damage to the soil ecosystem.

4. Conclusions

As shown in the present study, how to transform all native organic resources and recycle them into soil fertilizers as much as possible for farms with biogas residues severely polluted by heavy metals is a problem worthy of attention. The environmental and crop pollution risks could be reduced by carrying out regular heavy metals inspections for feed, feces, biogas residue, and slurry for different types of farms. In particular, for farms with low risk, such as the Shuyang gooseries, the discharged sewage could be used for irrigation directly, according to the sewage discharge standards in China. Although the discharged sewage samples from the Sihong dairy farms and Suyu henneries were evaluated as safe via the Nemerow pollution index, the high concentrations of Cd and Pb pose a high risk, suggesting that heavy metal reduction treatment is essential before utilizing biogas-residue-containing sewage, which is rich in nutrients. Thus, a comprehensive evaluation should be performed. Antibiotics, pathogens, and other risky contaminants also need to be considered in the future, and safe application of biogas residue and biogas slurry will finally provide a beneficial means of eco-friendly agriculture.

The results in this study indicate that biogas waste has potential for application as an organic fertilizer, due to its richness in mineral nutrients. Returning to farmland is the main means of utilization of biogas residues and slurries. However, high heavy metal contents might bring environmental risks, compromising the safe agriculture and ecology. In view of the limitations of each technology and the complexity of breeding modes, we put forward the following suggestions from the perspective of management: (1) through the regular inspections of feed, feces, biogas residue, and slurry for heavy metals, the environmental and crop pollution risks can be reduced from the source at different types of farms; (2) form a system of laws, policies, and regulations to manage the application of biogas waste efficiently, with reference to the experience of developed countries; (3) control the dosage of the biogas residues and slurries according to the consumption ability of different types of farmland; and (4) promote crop yield and soil fertility levels via the combination of synthetic and organic fertilizers. Furthermore, although types and contents of heavy metals in the biogas waste were determined in this study, the different forms of heavy metals and the effects of biogas waste used as organic fertilizer for crops need to be further studied before large-scale utilization.