Improving green waste composting by addition of sugarcane bagasse and exhausted grape marc

Bioresource Technology 218 (2016) 335–343

Contents lists available at ScienceDirect

Bioresource Technology journal homepage: www.elsevier.com/locate/biortech

Improving green waste composting by addition of sugarcane bagasse and exhausted grape marc Lu Zhang, Xiangyang Sun ⇑ College of Forestry, Beijing Forestry University, Beijing 100083, PR China

h i g h l i g h t s  Sugarcane bagasse (SCB) and exhausted grape marc (EGM) were added to compost.  SCB and/or EGM enhanced the two-stage composting of green waste.  Physico-chemical and microbiological properties explained the rapid decomposition.  Temperature, water retention, microorganisms, enzymes, and nutrients were optimized.  Combination of 15% SCB and 20% EGM reduced the two-stage composting time to 21 days.

a r t i c l e

i n f o

Article history: Received 5 May 2016 Received in revised form 21 June 2016 Accepted 24 June 2016 Available online 27 June 2016 Keywords: Exhausted grape marc Green waste Sugarcane bagasse Two-stage composting

a b s t r a c t The composting of lignocellulosic waste into compost is a potential way of sustainably disposing of a waste while generating a useful product. The current study determined whether the addition of sugarcane bagasse (SCB) (at 0, 15, and 25%) and/or exhausted grape marc (EGM) (at 0, 10, and 20%) improved the two-stage composting of green waste (GW). The combined addition of SCB and EGM improved composting conditions and the quality of the compost product in terms of temperature, water-holding capacity, particle-size distribution, coarseness index, pH, electrical conductivity, water-extractable organic carbon and nitrogen, microbial numbers, enzymatic activities, polysaccharide and lignin content, nutrient content, respiration, and phytotoxicity. The optimal two-stage composting and the best quality compost were obtained with the combined addition of 15% SCB and 20% EGM. With the optimized two-stage composting method, the compost matured in only 21 days rather than in the 90–270 days required for traditional composting. Ó 2016 Elsevier Ltd. All rights reserved.

1. Introduction With the rapid development of urban green space in China, urban green waste (GW), i.e., park and garden litter and trimmings, has dramatically increased. In Beijing, for example, the amount of GW produced has increased by about 50,000–100,000 tons per year (Zhang and Sun, 2014a; Zhang et al., 2013). Traditional GW disposal has involved incineration or deposition in landfills, which reduce the efficiency of land use and cause environmental problems such as water contamination and odour pollution (Bustamante et al., 2013; Gabhane et al., 2012). As an alternative, composting technology has been considered an effective method for transforming the organic matter into a potentially safe, stable ⇑ Corresponding author at: College of Forestry, Beijing Forestry University, P.O. Box 111, Beijing 100083, PR China. E-mail addresses: [email protected], [email protected] (X. Sun). http://dx.doi.org/10.1016/j.biortech.2016.06.097 0960-8524/Ó 2016 Elsevier Ltd. All rights reserved.

and sanitary product that can be used as a soil amendment, an organic fertilizer, or a substitute for peat in soilless culture (Chen et al., 2014). For biomasses that are high in lignocellulose, however, traditional composting is time consuming, produces odorous gases (i.e., NH3 and H2S), and generates a low quality compost product unsuitable for commercial use (Gabhane et al., 2012). Thus, reducing the time required for composting and increasing the quality of the compost product have become important goals in the use of composting for GW disposal. Researchers previously described an innovative, two-stage composting technology that includes a primary composting (PC) and a secondary composting (SC) (Zhang et al., 2013). This new method results in two peaks in composting temperature (at 55– 60 °C or even higher) and a longer thermophilic period. As a consequence, the production of a mature and stable compost requires only 30 days rather than the 90–270 days required for traditional composting (Zhang et al., 2013).

336

L. Zhang, X. Sun / Bioresource Technology 218 (2016) 335–343

Previous studies have indicated that the addition of various substances to the composting mass can accelerate the composting time and improve the quality of the compost product (Gabhane et al., 2012; Karak et al., 2013; Makan, 2015). One of these additives, sugarcane bagasse (SCB), is the fibrous residue left after the crushing and extraction of juice from sugar cane stalks during the manufacture of raw sugar (Mohee et al., 2015). In the composting of organic waste from livestock, SCB is commonly used as the structuring agent, whose main purpose is to correct the water content of the mixture by forming porous spaces in the composting mass. This increases the availability of oxygen and reduces the loss of static pressure in systems using forced aeration (Teixeira et al., 2015). The addition of sufficient SCB, which is acidic, can also enhance the nutrient transformation of organic wastes by controlling the pH (Cole et al., 2016). Moreover, SCB can be used as a carbon source to adjust the carbon:nitrogen (C:N) ratio and enhance the availability nutrients, including nitrogen (N), phosphorus (P), and potassium (K) (Kumar et al., 2010). Mohee et al. (2015) found that the use of SCB in the composting of municipal solid waste improved the compost quality and shortened the time required to achieve stabilization. Furthermore, the addition of SCB to municipal soil waste significantly increased the contents of organic matter (OM) and N in the compost product and greatly reduced N gaseous losses (Kumar et al., 2010; Mohee et al., 2015). However, the use of SCB in the two-stage composting of GW has not been studied. With the development of a wine industry in China, the generation of exhausted grape marc (EGM), an abundant and low-value winery waste, has greatly increased (Torres-Climent et al., 2015). Addition of EGM can increase the composting temperature especially in the thermophilic phase and thereby ensure the effective destruction of pathogens and other undesirable organisms (Bustamante et al., 2013; Paradelo et al., 2013). Addition of EGM also tends to reduce the pH of the compost (perhaps because of the high water-soluble carbohydrate content of EGM) and may therefore help balance the pH during composting (Achmon et al., 2016). Winery and distillery wastes like EGM also tend to have low electrical conductivity (EC), high OM content, low heavy metal content, and significant contents of P and K that support microbial activity and reproduction during composting (Bustamante et al., 2011). Researchers have reported that the phytotoxicity of the compost product is reduced when animal manures are cocomposted with winery and distillery wastes (Bustamante et al., 2011, 2013). Furthermore, EGM may reduce the rate and duration of NH3 emission during composting, which could increase the N content in the compost product and reduce air pollution (Requejo et al., 2014). However, nothing is known about the effects of EGM on GW composting. The overall goal of the present study was to optimize the two-stage composting of GW. The specific objectives were (i) to determine the optimal ratio of SCB and/or EGM in the two-stage composting of GW; (ii) to characterize the changes in the physical, chemical, biochemical, and microbial properties of GW during composting; and (iii) to evaluate the quality of the compost product.

2. Materials and methods 2.1. Composting materials The GW that was used as the raw material for composting consisted mainly of the fallen leaves and branch cuttings of poplar (Populus tomentosa Carr.) produced by urban landscape maintenance in Beijing in the spring of 2015. The GW was mechanically shredded into 1 cm pieces (Zhang et al., 2013). SCB was obtained

from Fujian Chengfa Agriculture Development Co. (China) and was air-dried and shredded into 3–6 cm pieces. EGM was obtained from Nanjing Nongaigou Farm Products Department (China). Bamboo vinegar was also added during the composting because it can reduce N volatilization and therefore increase the retention of N in the compost (Zhang et al., 2013). Bamboo vinegar, which is a lightyellow and transparent acidic liquid with a slightly smoky smell, was obtained from the Beijing Kaiyin Organic Fertilizer Production Co. (China). A microbial inoculum, which was a mixture of Trichoderma spp. inoculum (60%, v/v) and Phanerochaete chrysosporium Burdsall inoculum (40%, v/v), was prepared as described by Wei et al. (2007); it was added at the onset of composting to accelerate the degradation process. The main physico-chemical characteristics of the initial materials are listed in Table 1. The determination methods are described in Section 2.4.

2.2. Experimental design and composting process A two-stage composting process was used in this study (Fig. 1). The amount of GW in each treatment was the same. Before the start of the process and based on a previous report (Zhang and Sun, 2014b), the C:N ratio of the GW was adjusted to 25–30 by the addition of urea, and the moisture content of the GW was adjusted to about 60% by water addition. Various quantities of SCB and/or EGM were then combined with the GW (Table 2) to produce a uniform mixture of composting mass. Finally, an equal amount of microbial inoculum was added to each composting mixture (5 ml of inoculum kg 1 dry GW) (Zhang et al., 2013). The nine combinations of GW, SCB, and EGM are hereafter referred to as nine treatments. At the beginning of the PC (day 0), the nine treatments were added to composting reactors, which were non-covered cement containers (6 m long, 2 m wide, and 1.5 m high) with an automatic compost-turning and -watering system. Each treatment was represented by three replicate composting reactors, resulting in 27 composting reactors. The automatic system turned the mixture in each reactor for 40 min every day during the PC to ensure oxygen supply (Zhang and Sun, 2014a; Zhang et al., 2013). When the temperature of the mixture increased to 50–60 °C, 2 ml of bamboo vinegar (diluted in 2 L of water) per 100 kg of mixture (dry weight) was sprinkled onto the mixtures as they were being turned (Zhang et al., 2013). When the temperature dropped to 35–45 °C, the PC was considered complete. The temperatures in all treatments decreased to 35–45 °C by day 6. At that time, the mixtures were once again treated with the vinegar solution. On day 6, the mixture was removed from each composting reactor with an excavator and placed in open windrows (three windrows per reactor). The SC of all treatments began on day 6. Each windrow had a trapezoidal cross-section and was 2 m long, 1.5 m wide, and 1 m high. The windrows were turned over manually with a mini-excavator for 40 min every 3 days to ventilate the mixtures (Zhang and Sun, 2014b). Diluted bamboo vinegar was added during the SC as described for the PC. When the temperature of a windrow decreased to the ambient temperature, the whole composting process was considered complete. Throughout the composting process, water was added to the mixtures whenever the water content dropped below 60%. The moisture content of the composting mixture was determined daily with an SK-100 moisture meter (Tokyo, Japan). The ambient temperature and the temperatures at a depth of 60 cm in the front, centre, and back of each composting mixture were measured daily with a self-made temperature sensor with a temperature dial and a 1 m long rod; this was done before the composting mixtures were turned and watered. The three readings per composting mixture were averaged.

337

L. Zhang, X. Sun / Bioresource Technology 218 (2016) 335–343

Table 1 Selected physico-chemical properties of green waste (GW), sugarcane bagasse (SCB), exhausted grape marc (EGM), and final compost products. Values are means (SD); n = 3. Treatments T1–T9 are described in Table 2. Treatment

BD (g/cm3)

WHC (%)

pH

EC (mS/cm)

OM (%)

TKN (%)

GW SCB EGM T1 T2 T3 T4 T5 T6 T7 T8 T9 IRa

0.81(0.02) 0.36(0.04) 0.43(0.01) 0.53(0.09)e 0.49(0.05)d 0.46(0.03)c 0.47(0.06)c 0.40(0.01)a 0.40(0.02)a 0.49(0.04)d 0.43(0.05)b 0.41(0.08)a 0.40

50.07(1.03) 61.84(0.97) 88.02(1.07) 56.54(1.11)i 60.08(0.87)h 71.11(0.92)e 70.06(1.33)f 81.02(1.78)b 83.13(0.46)a 62.36(0.62)g 73.28(0.79)d 76.49(1.00)c 70.00–85.00

8.16(1.30) 4.10(1.00) 5.22(0.87) 7.90(1.08)a 7.69(0.65)b 7.34 (0.43)e 7.47 (0.97)d 6.89(1.05)h 6.62(0.41)i 7.58(0.73)c 7.11(0.48)f 6.93(0.26)g 6.50–7.50

1.73(0.39) 0.35(0.09) 1.24(0.45) 2.61(0.32)i 3.20(0.25)h 3.42(0.10)e 3.31(0.04)f 3.75(0.47)b 3.82(0.13)a 3.23(0.65)g 3.60(0.96)d 3.64(0.54)c <4.00

– 71(7) 68(6) 45(1)h 51(4)g 63(2)d 60(3)e 78(1)b 89(2)a 55(4)f 73(5)c 75(8)c –

1.30(0.53) 0.75(0.22) 2.54(0.11) 3.00(0.65)i 4.05(0.87)h 6.43(0.54)e 5.73(0.78)f 9.55(0.92)b 11.08(0.89)a 4.66(0.65)g 7.93(0.98)d 8.74(0.22)c –

TP (%)

TK (%)

WEOC (%)

WEON (%)

WEOC/TKN

Ca (%)

0.05(0.01) 0.94(0.20) 0.15(0.09) 0.30(0.05)i 0.44(0.10)h 0.59(0.07)e 0.55(0.03)f 0.74(0.08)b 0.83(0.02)a 0.52(0.11)g 0.65(0.05)d 0.70(0.12)c –

0.26(0.04) 0.33(0.07) 0.71(0.09) 0.28(0.04)h 0.35(0.07)g 0.46(0.10)d 0.43(0.05)e 0.61(0.03)b 0.68(0.01)a 0.39(0.09)f 0.54(0.10)c 0.56(0.08)c –

8.93(1.21) – – 3.09(0.69)i 3.77(0.54)h 4.82(0.94)e 4.53(0.35)f 6.11(1.01)b 6.76(0.87)a 4.10(0.76)g 5.39(0.98)d 5.68(1.10)c –

6.22(0.76) – – 1.70(0.21)i 2.31(0.87)h 3.62(1.03)e 3.18(1.29)f 5.07(0.98)b 5.23(0.56)a 2.66(0.73)g 4.39(0.45)d 4.76(0.62)c –

1.24(0.54) – – 1.03(0.24)a 0.93(0.16)b 0.75(0.02)e 0.79(0.33)d 0.64(0.19)g 0.61(0.20)h 0.88(0.11)c 0.68(0.07)f 0.65(0.04)g <0.70

0.51(0.09) 0.70(0.08) 1.68(0.01) 1.02(0.02)h 1.13(0.10)g 1.32(0.06)d 1.29(0.04)e 1.47(0.08)b 1.52(0.11)a 1.21(0.53)f 1.40(0.12)c 1.45(0.06)b –

Mg (%)

S (%)

Fe (10

0.29(0.04) 0.62(0.08) 0.33(0.02) 0.93(0.01)i 1.05(0.25)h 1.19(0.09)e 1.15(0.10)f 1.31(0.44)b 1.39(0.03)a 1.09(0.12)g 1.25(0.36)d 1.28(0.07)c

4.04(1.07) 8.02(0.98) 11.01(1.03) 9.14(1.02)i 10.28(0.96)h 12.20(0.65)e 12.03(0.94)f 14.01(1.07)b 15.87(0.46)a 10.92(0.54)g 13.07(0.87)d 13.63(0.46)c

7.11(1.01) 14.20(1.23) 7.64(1.03) 8.02(0.87)i 9.89(1.11)h 14.08(1.26)e 13.01(1.06)f 18.09(1.00)b 19.11(1.76)a 11.32(1.03)g 15.79(1.28)d 16.86(1.07)c

GW SCB EGM T1 T2 T3 T4 T5 T6 T7 T8 T9 IRa

GW SCB EGM T1 T2 T3 T4 T5 T6 T7 T8 T9

3

%)

B (10

3

%)

1.01(0.62) 2.33(0.21) 1.86(0.09) 0.98(0.70)i 1.17(0.24)h 1.82(0.16)e 1.70(0.22)f 2.49(0.09)b 2.78(0.27)a 1.43(0.65)g 2.03(0.32)d 2.19(0.12)c

3

–

1.32(0.43) 2.00(0.12) 1.65(0.29) 0.89(0.15)i 1.15(0.06)h 1.45(0.11)e 1.40(0.49)f 1.81(0.38)b 1.93(0.04)a 1.27(0.10)g 1.61(0.23)d 1.67(0.54)c

– – – – – – – – – – – –

Mo (10

%)

BD = bulk density; WHC = water-holding capacity; EC = electrical conductivity (at 25 °C); OM = organic matter; TKN = total Kjeldahl nitrogen; TP = total phosphorus; TK = total potassium; WEOC = water-extractable organic carbon; WEON = water-extractable organic nitrogen. Means in a column followed by the same letter are not significantly different at p 6 0.05 by LSD. a IR = ideal range, according to Zhang and Sun (2014a), Karak et al. (2013), and Hue and Liu (1995).

Table 2 Orthogonal design L9(34) of the experiment. Treatment

SCB (% in initial GW, based on dry weight)

EGM (% in initial GW, based on dry weight)

T1 T2 T3 T4 T5 T6 T7 T8 T9

0 0 0 15 15 15 25 25 25

0 10 20 0 10 20 0 10 20

GW = green waste; SCB = sugarcane bagasse; EGM = exhausted grape marc.

2.3. Sample collection and preparation

Fig. 1. Flow chart of the two-stage composting process of green waste (GW) used in this study. SCB = sugarcane bagasse; EGM = exhausted grape marc.

The compost was sampled while it was being turned on day 0, 2, 4, 6, 14, 18, 21, 23, 25, and 30. Each sample consisted of about 80 g of waste materials from each composting reactor or windrow. To collect a sample, the cross-section of the reactor or windrow was horizontally marked into quarters, and a subsample of about 20 g

338

L. Zhang, X. Sun / Bioresource Technology 218 (2016) 335–343

was taken from the top to the bottom of the waste at the centre of each quartered section. The subsamples from each reactor or windrow were combined into one composite sample, which was then divided into three parts. The first part was air-dried, and the second part was oven-dried at 65 °C. All dried samples were ground to pass through 0.25 and 0.10 mm sieves. The third part was not dried. The three kinds of samples were stored in re-sealable plastic bags in a refrigerator at 4 °C. 2.4. Analytical methods The air-dried samples were analysed for physical properties, pH, electrical conductivity (EC), the contents of total Kjeldahl nitrogen (TKN), water-extractable organic carbon (WEOC), water-extractable nitrogen (WEON), total phosphorus (TP), polysaccharides, and lignin. The oven-dried samples were analysed for the contents of total potassium (TK), OM, and macro- and micro-nutrients. In addition to being used for a seed germination test, the fresh samples were used to determine numbers of culturable microorganisms (bacteria, actinomycetes, and fungi), enzyme activities (dehydrogenase activity [DHA] and b-glucosidase activity [b-GA]), and respiration rate. All analyses were performed on three replicate subsamples per sample. 2.4.1. Physico-chemical analysis Bulk density (BD) and water-holding capacity (WHC) were determined in the initial materials and in the final compost products as described by Zhang et al. (2013). The particle-size distribution of the final compost products was determined according to Gabhane et al. (2012) and Zhang et al. (2013). The coarseness index (CI), expressed as a percentage (based on air-dried weight) of particles >1 mm, was also determined (Jayasinghe, 2012). TKN was measured by the modified micro-Kjeldahl procedure with a KDY-9830 automatic Kjeldahl apparatus (China). WEOC and WEON were determined in 1:10 (w/v) water extracts using a TOC-TN analyser (Japan). The OM content was measured by the potassium bichromate titrimetric method. Polysaccharides and lignin were determined after quantitative hydrolysis in a two-stage acid treatment as described by Paradelo et al. (2013). Samples were also tested for maturity and stability using respirometry as described by Makan (2015). 2.4.2. Microbiological analyses Throughout the two-stage composting, the abundances of culturable bacteria, actinomycetes, and fungi in the composting samples were determined by serial dilution and plating as described by Sen and Chandra (2009) and Shi et al. (2006). DHA and b-GA were determined according to the methods of Gabhane et al. (2012) and Carrnona et al. (2012). 2.4.3. Phytotoxicity test The phytotoxicity of the compost products was evaluated with a seed germination assay as described by Zucconi et al. (1981). Chinese cabbage (Brassica parachinensis) and tomato (Lycopersicon esculentum L.) seeds were used. A fresh sample of each final compost was placed in distilled water at a ratio of 1:5 (W/V). The suspensions were shaken for 24 h and then passed through medium-speed qualitative filter paper to remove the suspended particles. After the extract was passed through the filter paper, 5 ml of the filtrate was placed in a 9 cm dia. Petri dish containing two sheets of filter paper. Twenty-five seeds were then added to each dish. Each combination of the nine final compost products and the two kinds of seeds was represented by three replicate dishes; as a control, seeds were also germinated in Petri dishes containing deionized water rather than compost extract. After

incubation at 25 °C for 48 h in darkness, the number of seeds that germinated and their root lengths were determined. The germination index (GI) value was determined with the following formula (Zucconi et al., 1981): GI = (mean number of germinated seeds in the treatment  mean root length in the treatment  100%)/(mean number of germinated seeds in the control  mean root length in the control). 2.5. Statistical analysis One-way analyses of variance (ANOVAs) were used to determine whether the physical, chemical, biochemical, and microbial properties differed among the treatments. When ANOVAs were significant, means were separated with an LSD test. As noted earlier, the samples collected from individual composting reactors and from individual windrows were treated as replicates for each sampling time. All statistical analyses were performed with SPSS16.0. 3. Results and discussion 3.1. Temperature changes Compost temperature is an indicator of microbial activity during composting, and a return to near ambient temperatures is a good indicator of the end of the bio-oxidative phase (Teixeira et al., 2015). The pattern of temperature changes through time was similar in all treatments (Table 3). In the PC, the temperatures quickly increased and then declined; in the SC (from day 6), the temperatures increased again and subsequently declined. In both the PC and the SC, the temperatures were higher in treatments T5, T6, T8, and T9 with the combined addition of SCB and EGM than in the other treatments; the temperatures were highest in treatment T6 (15% SCB and 20% EGM) and lowest in treatment T1. The composting temperature should remain in the thermophilic range (50–60 °C) for at least 3 days to maximise sanitisation (Zhang and Sun, 2014b). All nine treatments produced temperatures that remained within the thermophilic range for at least 3 days during either the PC or SC or during both the PC and SC (Table 3). The thermophilic phase began earlier and lasted longer in treatments T5, T8, and T9, and especially in treatment T6 than in the other treatments. The increases in temperature and duration of the thermophilic period resulting from the addition of SCB and EGM can be partly explained by reductions in BD and increases in moisture holding capacity (Section 3.2) during composting that enhanced the degradation of organic wastes and helped maintain high temperatures (Zhang and Sun, 2014b). The effects of SCB and EGM on temperature may also be explained by their enhancement of microbial numbers and activities, which could enhance the production of metabolic heat (Section 3.6). Furthermore, the high absorption capacity of these additives tends to limit evaporation and to therefore limit the heat losses associated with evaporation (Bustamante et al., 2013; Teixeira et al., 2015). 3.2. Water-holding capacity of the final compost Addition of SCB and/or EGM substantially increased (p < 0.05) the WHC of the compost product (Table 1). This was especially true for the combined addition of SCB and EGM (treatments T5, T6, T8, and T9). Treatment T6 (15% SCB and 20% EGM) had the highest value, while treatment T1 had the lowest. These effects of SCB and EGM can be explained by their effects on BD and OM content because WHC is greatly influenced by BD and OM content (Mohee et al., 2015). Addition of SCB and EGM

339

L. Zhang, X. Sun / Bioresource Technology 218 (2016) 335–343

Table 3 Composting temperatures of treatments T1–T9 during the two-stage composting of green waste. Also indicated is the composting period, which is the number of days required to obtain a mature and stable compost. Treatments T1–T9 are described in Table 2. Treatment

PC Peak temp. day

Peak temp. reached (°C)

Time spent in thermophilic range (days)

SC Peak temp. day

Peak temp. reached (°C)

Time spent in thermophilic range (days)

T1 T2 T3 T4 T5 T6 T7 T8 T9

4 4 4 4 2 2 4 2 2

50.2 52.3 54.0 53.6 57.2 58.9 53.0 55.8 56.5

1 3 3 3 4 5 3 4 4

23 18 18 18 14 14 18 14 14

51.0 53.3 55.8 54.7 58.5 59.7 54.1 57.0 57.4

3 7 7 7 9 10 7 9 9

Total time spent in thermophilic range (days)

Composting period (days)

4 10 10 10 13 15 10 13 13

30 25 25 25 21 21 25 21 21

resulted in high OM contents and low BD values (Table 1). These positive changes in the absorption and holding water capacities of the compost products may also reflect the development of pores within the particles of the final compost (Gupta et al., 2010). Mesopores in particular are commonly associated with the ability of substrates to retain water (Haynes and Belyaeva, 2009). Mohee et al. (2015) and Teixeira et al. (2015) both suggested that the high proportion of mesopores in SCB might contribute to a high WHC in the final compost product. In addition, the treatments with both SCB and EGM significantly reduced the CI value (Section 3.3), and Abad et al. (2005) reported that WHC significantly increased with a decrease in CI value.

complete degradation of the GW (Section 3.1) and thus to an improved physical structure (especially the particle-size distribution) of the final compost. Because of their relatively coarse particle size and high surface area, SCB and EGW may be particularly useful for obtaining a product with the desired particle sizes (Mohee et al., 2015; Teixeira et al., 2015). Thus, the combination of SCB and EGM could enhance the formation of particles between 0.25 and 2.00 mm and reduce the CI value of the compost product, i.e., the two additives could improve compost structure in terms of its ability to support plant growth.

3.3. Particle-size distribution and coarseness index of the final compost

The maturity and stability of the compost product are related to its pH and EC (Jumnoodoo and Mohee, 2011; Zhang and Sun, 2014a). In the current study, the pattern of pH change during composting was similar for all treatments (Fig. 2a). In the PC, pH increased to an initial peak and then decreased until day 6. After day 6, the pH of all treatments increased to a second peak. At the end of composting process, the pH of the compost had stabilized. The peak values were higher for treatments without the combined addition of SCB and EGM (treatments T1, T2, T3, T4, and T7) than for treatments with the combined addition of SCB and EGM (treatments T5, T6, T8, and T9). The final pH of treatments T3, T4, T5, T6, T8, and T9 was within the acceptable range (6.50–7.50) for mature compost as prescribed by Karak et al. (2013) (Table 1). According to Jumnoodoo and Mohee (2011), a pH between 7.00 and 8.00 will support the microbial activity and reproduction necessary for composting. Moreover, a pH between 7.00 and 8.00 may increase N retention (Raphael and Velmourougane, 2011). During the whole composting process, treatments with the combined addition of SCB and EGM (treatments T5, T8, T9, and especially treatment T6) had a more suitable pH for composting than the other

The particle-size distribution and CI value of the final compost products are listed in Table 4. According to Zhang et al. (2013), a high percentage of particles between 0.25 and 2.00 mm in the final compost is optimal for gas exchange, water exchange, and especially WHC. The percentage of these particles increased significantly (p < 0.05) with the addition of SCB or EGM individually or in combination. Treatment T6, which was amended with 15% SCB and 20% EGM, had the highest percentage of these particles, while treatment T1 had the lowest percentage. In contrast, the CI value of the compost product decreased (p < 0.05) with addition of SCB and/ or EGM. Except for treatments T1, T2, T4, and T7, all other treatments had CI values within the ideal range of 30–45% (Jayasinghe, 2012). SCB was previously reported to improve the particle-size distribution during composting (Teixeira et al., 2015) and the particlesize distribution of the final product (Bustamante et al., 2011; Curtin and Mullen, 2007). Furthermore, SCB and EGM both extended the thermophilic period, which could lead to a more

3.4. Changes in pH and EC

Table 4 Particle-size distribution of final compost products. The values for particle-size distribution and coarseness index (CI) indicate the percentage in each size range (in mm). Values in each row (excluding values for 0.25–2.00 and >1.00 mm) add to 100%. Values are means (SD); n = 3. Treatments T1–T9 are described in Table 2. Treat-ment

>12.00 (mm)

12.00–2.00

1.00–2.00

0.50–1.00

0.50–0.25

0.25–0.10

<0.10

0.25–2.00

CI (>1.00)

T1 T2 T3 T4 T5 T6 T7 T8 T9 IRa

0 0 0 0 0 0 0 0 0 –

10.28(1.22) 15.00(1.09) 17.43(1.38) 15.10(1.11) 20.08(1.67) 21.34(1.34) 14.03(1.78) 20.28(1.46) 20.43(1.43) –

10.03(1.79) 12.16(1.87) 14.55(1.54) 16.22(1.43) 20.13(1.07) 20.90(1.32) 14.18(1.76) 15.06(1.03) 18.11(0.98) –

11.88(1.44) 13.01(1.78) 22.27(1.60) 12.33(1.45) 20.96(1.02) 24.88(0.65) 11.59(1.06) 20.58(1.53) 21.13(1.18) –

10.10(1.74) 14.05(1.52) 11.28(1.23) 15.74(1.80) 21.04(1.03) 24.09(0.52) 15.31(1.44) 19.57(1.01) 20.20(1.52) –

20.30(1.00) 17.24(1.32) 23.44(1.05) 13.28(0.47) 5.22(1.07) 6.24(1.32) 11.04(1.20) 10.35(1.39) 12.53(1.17) –

37.41(1.14) 28.54(1.19) 11.03(1.23) 27.33(1.44) 12.57(1.36) 2.55(1.01) 33.85(1.65) 14.16(1.20) 7.60(1.39) –

32.01(0.65)i 39.22(0.89)h 48.10(1.62)e 44.29(1.49)f 62.13(1.56)b 69.87(1.08)a 41.08(1.32)g 55.21(1.24)d 59.44(1.95)c –

56.79(1.21)i 52.16(0.87)h 43.98(1.09)e 46.32(1.02)f 34.29(0.78)b 31.45(1.33)a 49.21(1.49)g 41.04(1.06)d 39.11(1.11)c 30.00–45.00

Means in a column followed by the same letter are not significantly different at p 6 0.05 by LSD. a IR = ideal range, according to Komilis and Ham (2003).

340

L. Zhang, X. Sun / Bioresource Technology 218 (2016) 335–343

Fig. 2. Effects of sugarcane bagasse (SCB) and exhausted grape marc (EGM) on the pH and electrical conductivity (EC) during the two-stage composting of green waste (GW). Treatments T1–T9 are described in Table 2.

with both SCB and EGM (treatments T5, T6, T8, and T9); the decline was greatest in treatment T1 and was least in treatment T6. The WEOC and WEON losses can indicate C and N losses, which could reduce the nutrient value of the final compost and could also cause serious atmospheric pollution (Paradelo et al., 2013). Most C is usually lost through the release of CO2, and most N is usually lost through the volatilization of NH3 (Kumar et al., 2010). As indicated by their lower losses, treatments with the combined addition of SCB and EGM, and especially 15% SCB and 20% EGM, helped dissolve CO2 and NH3 and immobilize C and N, and thereby increased the quality of the compost product. The results indicate that SCB and EGM addition reduced the losses of easily available C and N during the composting process. Mohee et al. (2015) and Requejo et al. (2014) also indicated that SCB and EGW could suppress the formation of odours during composting. Their high sorption capacity and the large surface areas also suggest that SCB and EGW could absorb gases. Furthermore, SCB is a good source of bioavailable C, which could partly compensate for the loss of C to respiration (Kumar et al., 2010), and the nutrients in EGM could accelerate take up of NH3 by N-cycle microorganisms (Requejo et al., 2014). Hue and Liu (1995) proposed that the ratio between WEOC and TKN indicates the degree of organic matter decomposition of composting materials; they suggested that a ratio <0.7 indicates a mature and stable compost. In the current study, the ratio was <0.7 for treatments T4, T6, T8, and T9, and was lowest for treatment T6 (15% SCB and 20% EGM); the ratios for treatments T1– T4 and T7 were >0.7 (Table 1). These results indicated that the combined addition of SCB and EGM enhanced the decomposition of organic waste and increased the maturity and stability of the compost product. 3.6. Microbial numbers

treatments. The pH of SCB is acidic and could lower the pH during composting and thus accelerate the rate of microbial degradation (Cole et al., 2016). In addition to being acidic, EGM has a large surface area and strong absorptive power, which could inhibit ammonia volatilization and regulate the pH during composting (Requejo et al., 2014). The results indicate that a specific combination of SCB and EGM, especially the optimum of 15% SCB and 20% EGM, changed the pH of the materials from slightly alkaline to slightly acidic and also increased the degree of compost maturity and stability. The EC value reflects the soluble salt content of compost, and high EC values can inhibit plant growth and seed germination (Karak et al., 2013). The responses of EC to the treatments were the opposite to those of pH, i.e., treatments that caused the lowest pH caused the highest EC (Fig. 2b). This is consistent with a previous report (Zhang and Sun, 2014b). During composting, the EC was higher for treatments T5, T6, T8, and T9 with the combined addition of SCB and EGM than for treatments T1, T2, T3, T4, and T7. Still, the EC values for all treatments were within the acceptable range (<4 mS cm 1) for mature and stable compost (Karak et al., 2013) (Table 1). The increase in EC values with addition of SCB and EGM is reasonable because, by increasing the composting temperature and enhancing the breakdown of the GW, these additives could accelerate the production of inorganic compounds and the release of soluble salts. On the other hand, SCB and EGM may help reduce EC values during composing to some extent (Bustamante et al., 2011; Mohee et al., 2015). 3.5. Contents of water-extractable organic carbon and nitrogen in the final compost WEOC and WEON were lower in the final compost products than in the initial GW in all treatments (Table 1), which was consistent with Paradelo et al. (2013). The decline in WEOC and WEON was greater in treatments T1, T2, T3, T4, and T7 than in treatments

The trends for microbial numbers were similar to those for composting temperatures (Fig. 3). The numbers of culturable microorganisms increased sharply leading up to the thermophilic phase of the PC and then decreased slightly. In the SC, the numbers increased again and then dropped gradually until the end of the process. Throughout the composting, microbial numbers were higher in treatments with the combined addition of SCB and EGM (treatments T5, T6, T8, and T9) than in the other treatments; numbers were highest in treatment T6 and lowest in treatment T1. The above results indicate that an appropriate combination of SCB and EGM (the best combination in the current study was 15% SCB and 20% EGM) can enhance microbial abundance. The ability of SCB to act as a habitat and refuge for microorganisms can result in the rapid reproduction and high activity of microorganisms (Teixeira et al., 2015). In addition, the sugars from the polysaccharides that compose the most external part of the cell wall in sugarcane are likely the first to be released and assimilated as a main C source by culturable microorganisms (Mohee et al., 2015). EGM contains an abundant and rich microbial community (Bovo et al., 2012), which could support an increase microbial numbers and activity during composting (Torres-Climent et al., 2015). The elemental nutrients and especially P in SCB and EGM may also favour the formation of the ATP needed for microbial reproduction (Bustamante et al., 2011; Kumar et al., 2010). Finally, SCB and EGM could improve the particle structure, BD, and moisture content of the composting materials (Sections 3.2 and 3.3) and thereby provide a favourable physical microenvironment for microbial activity and reproduction. 3.7. Enzymatic activities Enzymes are important in composting because they can enhance the degradation processes. DHA and b-GA have often been

L. Zhang, X. Sun / Bioresource Technology 218 (2016) 335–343

341

Fig. 3. Effects of sugarcane bagasse (SCB) and exhausted grape marc (EGM) on the numbers of culturable bacteria (a), actinomycetes (b), and fungi (c) during the two-stage composting of green waste (GW). Treatments T1–T9 are described in Table 2.

used to monitor microbial activity during composting (Carrnona et al., 2012; Gabhane et al., 2012). DHA is related to a group of enzymes that catalyse metabolic reactions that produce ATP through the degradation of GW (Gabhane et al., 2012). The data for enzyme activities were similar to those for microbial numbers (Fig. 4). In the PC, enzyme activities progressively increased and then declined for all treatments. In the SC, the enzyme activities increased again and subsequently declined in all treatments. In the whole composting process, DHA and b-GA were highest in treatment T6 and lowest in treatment T1. These results indicate that the addition of SCB and EGM, especially 15% SCB and 20% EGM, enhanced enzyme activities. The high sorption capacity and the large surface areas of SCB and EGM may provide a microenvironment that can increase the adsorption and stabilization of enzymes so that they remain active during composting (Teixeira et al., 2015; Torres-Climent et al., 2015). The nutrients supplied by SCB and EGM could also increase enzyme production and secretion and then accelerate the degradation of organic wastes (Bustamante et al., 2011; Kumar et al., 2010). In addition, the microorganisms in the EGM could contribute to microbial abundance and enzymatic activity in the composting mixture and could thereby contribute to the degradation of the lignocellulosic raw materials (Torres-Climent et al., 2015). 3.8. Lignin and polysaccharide changes The cellulose:lignin ratio can indicate the quality of the compost product. If the final ratio is far below 0.5, the compost product can be considered mature and stable (Komilis and Ham, 2003). At the end of the process, the final ratios were <0.5 for all treatments except treatment T1, and the ratio was lowest for treatment T6. These ratios indicate that the final compost products, except for treatment T1, were biologically mature and stable (Table 5). The lignocellulosic index (LCI), defined as the ratio of acidinsoluble polysaccharides to the sum of acid-soluble and acidinsoluble polysaccharides (LCI = lignin:cellulose + hemicellulose + lignin), is also used as an indicator of the quality of the compost

Fig. 4. Effects of sugarcane bagasse (SCB) and exhausted grape marc (EGM) on the dehydrogenase activity (DHA) and b-glucosidase activity (b-GA) during the twostage composting of green waste (GW). Treatments T1–T9 are described in Table 2.

product and its potential biodegradability (Melillo et al., 1989). The final LCIs were higher in treatments T5, T6, T8, and T9 (with both SCB and EGM addition) than in the other treatments. The LCI was highest in treatment T6 and lowest in treatment T1 (Table 5).

342

L. Zhang, X. Sun / Bioresource Technology 218 (2016) 335–343

Table 5 Polysaccharide and lignin concentrations (normalized to a constant ash content) and related ratios in final compost products. Values are means (SD); n = 3. Treatments T1–T9 are described in Table 2. Treatment

Cellulose (%)

Hemicellulose (%)

Lignin (%)

Cellulose:lignin

LCI

T1 T2 T3 T4 T5 T6 T7 T8 T9 IRa

35.97(1.79)a 15.40(1.45)b 7.12(1.02)e 8.58(1.34)d 3.60(1.18)h 2.21(1.23)i 11.23(1.07)c 5.38(1.23)f 4.15(1.00)g –

28.89(0.78)a 12.57(0.92)b 7.25(1.01)e 7.44(0.54)d 3.21(0.80)h 1.56(0.79)i 9.23(0.37)c 5.18(0.76)f 4.36(0.54)g –

71.06(1.27)a 65.70(1.15)b 58.02(1.48)e 60.18(1.03)d 48.20(1.27)h 42.43(1.38)i 62.01(1.30)c 56.07(1.43)f 53.36(1.75)g –

0.51(0.09)a 0.23(0.02)b 0.12(0.06)e 0.14(0.03)d 0.07(0.04)g 0.05(0.01)h 0.18(0.02)c 0.10(0.05)f 0.08(0.07)g <0.50

0.52(0.10)g 0.70(0.09)f 0.80(0.01)d 0.79(0.06)d 0.88(0.02)b 0.92(0.04)a 0.75(0.03)e 0.84(0.07)c 0.86(0.08)bc –

LCI = the lignocellulosic index = lignin:cellulose + hemicellulose + lignin. Means in a column followed by the same letter are not significantly different at p 6 0.05 by LSD. a IR = ideal range, according to Komilis and Ham (2003).

These results indicate that the combined addition of SCB and EGM, and especially the combined addition of 15% SCB and 20% EGM in treatment T6, not only increased the decomposition of organic wastes but also enhanced the maturity and stability of the compost product. The enhanced degradation of cellulose and hemicellulose in GW amended with both SCB and EGM was likely due to the effects of these amendments on the physical, chemical, and microbiological properties during composting, as previously discussed. 3.9. Nutrient contents of the final compost Insufficient or unbalanced nutrients can reduce the usefulness of compost as a soil amendment (for soil amelioration or fertilization) and as an alternative substrate for soilless culture (Zhang and Sun, 2014a). Nutrient levels in the compost products were significantly greater (p < 0.05) in treatments T5, T6, T8, and T9 than in treatments T1, T2, T3, T4, and T7 (Table 1). Nutrient contents were highest in treatment T6 and lowest in treatment T1. The above results show that the combined addition of SCB and EGM, and especially the combined addition of 15% SCB and 20% EGM, resulted in high levels of nutrients in the final compost products. One possible reason is that SCB and EGM increased microbial activity and thereby enhanced the mineralization of GW, which would increase the release of nutrients. Another possible reason is that SCB and EGM contain substantial quantities of macro- and micro-nutrients, which when released would increase the nutrient content of the compost (Bustamante et al., 2011; Kumar et al., 2010). Furthermore, adherence of the essential nutrients to SCB pores could reduce nutrient leaching, and thus, could significantly increase the content and availability of nutrients in the final compost (Teixeira et al., 2015). 3.10. Respiration and germination The amount of CO2 released by final compost is an indicator of its organo-chemical condition (Chen, 2003). The CO2 respiration rate of the final compost products was lower in treatments T5, T6, T8, and T9 than in the other treatments (Table 6). The rate was highest in treatment T1 and lowest in treatment T6 (15% SCB and 20% EGM). If the maturity and stability of compost are indicated by a CO2 respiration rate <1 mg CO2-C g 1 OM day 1, all of the treatments except treatment T1 had generated a mature and stable compost (Thompson et al., 2003). The above result shows that the combined addition of SCB and EGM in the two-stage composting process not only shortens the composting period but also enhances the degradation of the organic materials and the stability and maturity of the compost

Table 6 The CO2 respiration rate and the germination index (GI) of final compost products. Values are means (SD); n = 3. Treatments T1–T9 are described in Table 2. Treatment

CO2 respiration rate (mg CO2-C/g OM/day)

GI (%, Brassica parachinensis)

GI (%, Lycopersicon esculentum L.)

T1 T2 T3 T4 T5 T6 T7 T8 T9 IRa

1.07(0.60)a 0.87(0.15)b 0.58(0.19)e 0.63(0.31)d 0.29(0.08)g 0.20(0.10)h 0.79(0.34)c 0.36(0.22)f 0.35(0.06)f <1

80(4)i 87(7)h 118(1)e 109(8)f 163(3)b 172(4)a 92(9)g 135(3)d 142(2)c >80

82(2)i 93(4)h 140(2)e 129(6)f 171(8)b 180(4)a 101(3)g 162(7)d 167(1)c >80

Means in a column followed by the same letter are not significantly different at p 6 0.05 by LSD. a IR = ideal range, according to Thompson et al. (2003) and Zucconi et al. (1981).

products so that the CO2 respiration rate of the final compost is quite low. A germination test was used to evaluate possible phytotoxic effects of the final compost products. The GI values for the two kinds of seeds were significantly greater (p < 0.05) in treatments with addition of both SCB and EGM (treatments T5, T6, T8, and T9) than in the other treatments. According to Zucconi et al. (1981), GI values >80% indicate the absence of significant phytotoxicity. Based on this threshold, none of the nine compost products was phytotoxic. The GI value was highest for treatment T6 (15% SCB and 20% EGM) and was lowest for treatment T1. Negative effects of compost products on plant growth are mainly caused by high pH values and high levels of soluble salts (EC value) (Paradelo et al., 2013). The high GI values obtained with the combined addition of SCB and EGM may be attributed to the lower pH and EC values in the compost products treated with these additives. In addition, both SCB and EGM appear to be good sources of plant nutrients such as N, P, and K, which could evidently promote seed germination and root elongation. 4. Conclusion SCB and EGM enhanced not only the rate of two-stage composting but also the quality of the compost product. The combined addition of SCB and EGM optimized the composting process by extending the thermophilic period, adjusting the pH and EC, increasing microbial numbers and enzyme activities, and accelerating lignocellulose degradation. For the compost product, the combined addition of SCB and EGM improved water retention and particle-size distribution, enhanced macro- and micronutrient contents, and increased seed germination. Two-stage

L. Zhang, X. Sun / Bioresource Technology 218 (2016) 335–343

composting of GW with the combined addition of 15% SCB and 20% EGM produced a high quality compost in only 21 days. Acknowledgements This study was supported by the Fundamental Research Funds for the Central Universities (NO. BLX2015-07). The authors thank Prof. Bruce Jaffee for his linguistic modification of this paper. References Abad, M., Fornes, F., Carrion, C., Noguera, V., Noguera, P., Maquieira, A., Puchades, R., 2005. Physical properties of various coconut coir dusts compared to peat. HortScience 40, 2138–2144. Achmon, Y., Harrold, D.R., Claypool, J.T., Stapleton, J.J., VanderGheynst, J.S., Simmons, C.W., 2016. Assessment of tomato and wine processing solid wastes as soil amendments for biosolarization. Waste Manage. 48, 156–164. Bovo, B., Nardi, T., Fontana, F., Carlot, M., Giacomini, A., Corich, V., 2012. Acidification of grape marc for alcoholic beverage production: effects on indigenous microflora and aroma profile after distillation. Int. J. Food Microbiol. 152, 100–106. Bustamante, M.A., Restrepo, A.P., Alburquerque, J.A., Perez-Murcia, M.D., Paredes, C., Moral, R., Bernal, M.P., 2013. Recycling of anaerobic digestates by composting: effect of the bulking agent used. J. Cleaner Prod. 47, 61–69. Bustamante, M.A., Said-Pullicino, D., Agullo, E., Andreu, J., Paredes, C., Moral, R., 2011. Application of winery and distillery waste composts to a Jumilla (SE Spain) vineyard: effects on the characteristics of a calcareous sandy-loam soil. Agric. Ecosyst. Environ. 140, 80–87. Carrnona, E., Moreno, M.T., Aviles, M., Ordovas, J., 2012. Composting of wine industry wastes and their use as a substrate for growing soilless ornamental plants. Spanish J. Agric. Res. 10, 482–491. Chen, Y.N., 2003. Nuclear magnetic resonance, infra-red and pyrolysis studies of solid organic waste composts. Compos. Sci. Util. 11, 152–168. Chen, Y.N., Zhou, W., Li, Y.P., Zhang, J.C., Zeng, G.M., Huang, A.Z., Huang, J.X., 2014. Nitrite reductase genes as functional markers to investigate diversity of denitrifying bacteria during agricultural waste composting. Environ. Biotechnol. 98, 4233–4243. Cole, A.J., Roberts, D.A., Garside, A.L., de Nys, R., Paul, N.A., 2016. Seaweed compost for agricultural crop production. J. Appl. Phycol. 28, 629–642. Curtin, J.S., Mullen, G.J., 2007. Physical properties of some intensively cultivated soils of Ireland amended with spent mushroom compost. Land Degrad. Dev. 18, 355–368. Gabhane, J., William, S.P., Bidyadhar, R., Bhilawe, P., Anand, D., Vaidya, A.N., Wate, S. R., 2012. Additives aided composting of green waste: effects on organic matter degradation, compost maturity, and quality of the finished compost. Bioresour. Technol. 114, 382–388. Gupta, R.D., Arora, S., Gupta, G.D., Sumberia, N.M., 2010. Soil physical variability in relation to soil erodibility under different land uses in foothills of Siwaliks in NW India. Trop. Ecol. 51, 183–197. Haynes, R.J., Belyaeva, O.N., 2009. Use of municipal green wastes as the basis for production of manufactured soil in Australia. In: Proceedings of the 11th International Conference on Environmental Science and Technology, Chania, Crete, Greece. Hue, N.V., Liu, J., 1995. Predicting compost stability. Compos. Sci. Util. 3, 8–15.

343

Jayasinghe, G.Y., 2012. Synthetic soil aggregates as a potting medium for ornamental plant production. J. Plant Nutr. 35, 1441–1456. Jumnoodoo, V., Mohee, R., 2011. Evaluation of FTIR spectroscopy as a maturity index for herbicide-contaminated composts. Environ. Waste Manage. 9, 89–99. Karak, T., Bhattacharyya, P., Paul, R.K., Das, T., Saha, S.K., 2013. Evaluation of composts from agricultural wastes with fish pond sediment as bulking agent to improve compost quality. Clean Soil Air Water 41, 711–723. Komilis, D.P., Ham, R.K., 2003. The effect of lignin and sugars to the aerobic decomposition of solid wastes. Waste Manage. 23, 419–423. Kumar, R., Verma, D., Singh, B.L., Kumar, U., Shweta, 2010. Composting of sugarcane waste by-products through treatment with microorganisms and subsequent vermicomposting. Bioresour. Technol. 101, 6707–6711. Makan, A., 2015. Windrow co-composting of natural casings waste with sheep manure and dead leaves. Waste Manage. 42, 17–22. Melillo, J.M., Aber, J.D., Linkins, A.E., Ricca, A., Fry, B., Nadelhoffer, K.J., 1989. Carbon and nitrogen dynamics along the decay continuum: plant litter to soil organic matter. Plant Soil 115, 189–198. Mohee, R., Boojhawon, A., Sewhoo, B., Rungasamy, S., Somaroo, G.D., Mudhoo, A., 2015. Assessing the potential of coal ash and bagasse ash as inorganic amendments during composting of municipal solid wastes. J. Environ. Manage. 159, 209–217. Paradelo, R., Moldes, A.B., Barral, M.T., 2013. Evolution of organic matter during the mesophilic composting of lignocellulosic winery wastes. J. Environ. Manage. 116, 18–26. Raphael, K., Velmourougane, K., 2011. Chemical and microbiological changes during vermicomposting of coffee pulp using exotic (Eudrilus eugeniae) and native earthworm (Perionyx ceylanesis) species. Biodegradation 22, 497–507. Requejo, M.I., Cartagena, M.C., Villena, R., Arce, A., Ribas, F., Cabello, M.J., Castellanos, M.T., 2014. Wine-distillery waste compost addition to a dripirrigated horticultural crop of central Spain: risk assessment. Biosyst. Eng. 128, 11–20. Sen, B., Chandra, T.S., 2009. Do earthworms affect dynamics of functional response and genetic structure of microbial community in a lab-scale composting system? Bioresour. Technol. 100, 804–811. Shi, J.G., Zeng, G.M., Yuan, X.Z., Dai, F., Liu, J., Wu, X.H., 2006. The stimulatory effects of surfactants on composting of waste rich in cellulose. World J. Microbiol. Biotechnol. 22, 1121–1127. Thompson, W., Leege, P., Millner, P., Watson, M.E., 2003. Test Methods for the Examination of Composts and Composting. The US Composting Council, US Government Printing Office. Teixeira, D.L., de Matos, A.T., Melo, E.D.C., 2015. Resistance to forced airflow through layers of composting organic material. Waste Manage. 36, 57–62. Torres-Climent, A., Gomis, P., Martin-Mata, J., Bustamante, M.A., Marhuenda-Egea, F. C., Perez-Murcia, M.D., Perez-Espinosa, A., Paredes, C., Moral, R., 2015. Chemical, thermal and spectroscopic methods to assess biodegradation of winerydistillery wastes during composting. PLoS One 10, e0138925. Wei, Z.M., Xi, B.D., Zhao, Y., Wang, S.P., Liu, H.L., Jiang, Y.H., 2007. Effect of inoculating microbes in municipal solid waste composting on characteristics of humic acid. Chemosphere 68, 368–374. Zhang, L., Sun, X.Y., 2014a. Effects of rhamnolipid and initial compost particle size on the two-stage composting of green waste. Bioresour. Technol. 163, 112–122. Zhang, L., Sun, X.Y., 2014b. Effects of earthworm casts and zeolite on the two-stage composting of green waste. Waste Manage. 39, 119–129. Zhang, L., Sun, X.Y., Tian, Y., Gong, X.Q., 2013. Effects of brown sugar and calcium superphosphate on the secondary fermentation of green waste. Bioresour. Technol. 131, 68–75. Zucconi, F., Pera, A., Forte, M., de Bertoldi, M., 1981. Evaluating toxicity of immature compost maturity. Biocycle 22, 54–57.