Bioresource Technology 243 (2017) 154–162

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

Addition of seaweed and bentonite accelerates the two-stage

composting of green waste
Lu Zhang, Xiangyang Sun ⇑
College of Forestry, Beijing Forestry University, Beijing 100083, PR China

h i g h l i g h t s

 Seaweed (SW) and bentonite (BT) were the additives in green waste (GW) composting.
 SW and/or BT addition enhanced the degradation and the humification of GW composting.
 Water retention, porosity, respiration rate, enzymes, and nutrients were optimized.
 Combination of 35% SW and 4.5% BT reduced the two-stage composting time to 21 days.

a r t i c l e i n f o a b s t r a c t

Article history: Green waste (GW) is an important recyclable resource, and composting is an effective technology for the
Received 7 April 2017 recycling of organic solid waste, including GW. This study investigated the changes in physical and chem-
Received in revised form 14 June 2017 ical characteristics during the two-stage composting of GW with or without addition of seaweed (SW,
Accepted 17 June 2017
Ulva ohnoi) (at 0, 35, and 55%) and bentonite (BT) (at 0.0, 2.5%, and 4.5%). During the bio-oxidative phase,
Available online 20 June 2017
the combined addition of SW and BT improved the physicochemical conditions, increased the respiration
rate and enzyme activities, and decreased ammonia and nitrous oxide emissions. The combination of SW
Keywords:
and BT also enhanced the quality of the final compost in terms of water-holding capacity, porosity,
Bentonite
Compost product
particle-size distribution, water soluble organic carbon/organic nitrogen ratio, humification, nutrient
Green waste content, and phytotoxicity. The best quality compost, which matured in only 21 days, was obtained with
Seaweed 35% SW and 4.5% BT.
Two-stage composting Ó 2017 Elsevier Ltd. All rights reserved.

1. Introduction et al., 2016). GW, however, consists primarily of cellulose, hemicel-

With increases in urbanization and the human population, vast
amounts of green waste (GW) are now produced in China (Zhang
and Sun, 2014). In Beijing city, for example, approximately 6 mil-
lion tons of GW is generated each year (Zhang and Sun, 2017). At
present, the GW in China is either burned or deposited in landfills.
As a result, considerable amounts of nutrients are lost, environ-
mental pollution is increased via emissions of toxic and green-
house gases, and land resources are wasted (Meng et al., 2017;
Zhang and Sun, 2016). Composting is considered effective for
reducing the mass of GW, for sanitizing it, and for transforming
it into a nutrient-rich product useful for plants and soil (Awasthi
⇑ Corresponding author at: College of Forestry, Beijing Forestry University, P.O.
Box 111, Beijing 100083, PR China.
E-mail addresses: sunxy1211@163.com, sunxy@bjfu.edu.cn (X. Sun).
lulose, and lignin, which are not readily decomposed by microor-
ganisms. In addition, if composting is improperly managed, it can
be slow and require a large area, generate foul smells, and produce
an immature product (Shi et al., 2006; Zhang and Sun, 2017).
Therefore, the present study investigated the composting of GW
with seaweed (SW, Ulva ohnoi) and bentonite (BT) with the goal
of accelerating the degradation of organic wastes, shortening the
composting period, and producing a high quality compost.
Aquatic farming systems in many parts of the world generate
large amounts of algal wastes including those from SW like Ulva
ohnoi and other marine macroalgae (Hardouin et al., 2014; Illera-
Vives et al., 2015a; Ozdemir et al., 2014). Drift SW, a kind of natural
organic resource, is deposited on beaches in large amounts as a
result of tidal or wind action and has been commonly used in agri-
culture and forestry as a fertilizer (Illera-Vives et al., 2015b). SW
contains many macro- and micro-nutrients and trace elements.
Kuwada et al. (2006) reported that the advantages of using

http://dx.doi.org/10.1016/j.biortech.2017.06.099
0960-8524/Ó 2017 Elsevier Ltd. All rights reserved.
 L. Zhang, X. Sun / Bioresource Technology 243 (2017) 154–162
SW-derived fertilisers in agriculture include increased nutrient
uptake, enhanced growth rates, and increased resistance to dis-
eases, pests, and climatic stress in crops. SW is particularly rich
in bioactive compounds (peptides, proteins, and oligo and polysac-
charides) that can increase soil aggregate stability and the rate at
which microorganisms respire and mineralize nitrogen (N)
(Hardouin et al., 2014; Stutter, 2015). In addition, the lactic acid
produced during SW biodegradation can decrease the pH of com-
posts (Dao and Kim, 2011). SW also contains large numbers of
microorganisms and substantial quantities of enzymes that could
enhance microbial diversity and succession, and thereby reduce
the time required to produce a mature compost (Leceta et al.,
2014). The addition of SW in the composting of lingocellulosic
organic residues, such as GW, could also reduce the hydrophobic
nature of GW because the major algal polysaccharide in SW is algi-
nate, which is hydrophilic (Ozdemir et al., 2014). Although adding
the appropriate quantity of SW can improve the composting pro-
cess, addition of high quantities of SW may cause the excessive
accumulation of some heavy metals in the compost product; such
accumulations can inhibit plant growth and lead to environmental
pollution (Khan et al., 2015; Riosmena-Rodriguez et al., 2010).
Finally, SW also contains plant growth hormones, such as auxins
and cytokinins, which could promote plant root growth (Illera-
Vives et al., 2015a). The effects of SW on the ‘‘two-stage compost-
ing” of GW, however, have not been determined. In the two-stage
composting of GW, the GW undergoes two rather than one ther-
mophilic periods (Zhang and Sun, 2014).
BT is a widely distributed, low-cost mineral that mainly consists
of montmorillonite, a 2:1 mineral with one octahedral sheet of alu-
mina between two sheets of silica (Jiang et al., 2014). Like SW, BT
could improve composting in many ways. BT has been used during
composting to improve the structural properties and water-
holding capacity (WHC) of the composting feedstock (Li et al.,
2012). Another study found that BT has substantial nutrient- and
water-adsorbing capacity due to its porous sponge-like structure,
high cation exchange capacity (CEC), and large specific surface area
(Fernandez-Calvino et al., 2015). BT can also reduce ammonia
(NH3) emissions during compositing and thereby increase the total
Kjeldahl nitrogen (TKN) content in the compost product. Li et al.
(2012) reported that addition of BT can increase organic matter
degradation and the TKN content, and decrease the carbon/nitro-
gen (C/N) ratio and the extractable copper (Cu) and zinc (Zn) con-
tents during the composting of swine manure. Addition of BT can
also enhance microbial activity and the temperature increase dur-
ing the thermophilic phase of compositing (Wang et al., 2016).
Moreover, BT contains high amounts of N and available phospho-
rus (P) and potassium (K), which can increase the nutrient content
of the compost product (Aranyos et al., 2016). Addition of BT can
buffer the increases in pH that typically occur during composting
(Fernandez-Calvino et al., 2015). BT can promote the synthesis of
urease and alkaline phosphatase during composting
(Wyszkowska and Wyszkowski, 2006). Another important prop-
erty of BT is its hydrophilic surface; when BT is added to compost-
ing organic waste, the hydrophilic surface of BT binds to the
hydrophobic surface of the organic waste, which accelerates the
degradation of lignocellulose and reduces the time required to pro-
duce a mature compost (Gedikoglu et al., 2012). Little information
is available, however, on the effects of BT on the two-stage com-
posting of GW.
The use of SW and BT as additives in the two-stage composting
of GW has not been previously reported. Therefore, the aims of this
study were to determine (1) how addition of various quantities and
combinations of SW and BT affects the physical and chemical char-
acteristics of GW during composting; (2) how these additives affect
the quality of the final compost; and (3) the optimal combination
of SW and BT for GW composting.
155
2. Materials and methods
2.1. Composting feedstock collection and processing
The GW used in this study was collected from urban landscape
maintenance in Beijing, China, in the spring of 2016. It was cut into
1-cm-long pieces with a grass-cutting multifunctional shredder
(model 9ZF-500B, Shandong, China) to obtain a uniform and appro-
priate particle size (Zhang and Sun, 2014). The air-dried SW was
purchased from the Qingdao Huifulin Marine Biology Technology
Co. Ltd., China. The SW was crushed into fine particles and passed
through sieves to obtain particles ranging from 1.0 to 1.5 mm
(Vendrame and Moore, 2005). BT was purchased from the Guangz-
hou Danlong Technology Co. Ltd., China. The BT was air dried
before it was added to the composting feedstock (Fernandez-
Calvino et al., 2015). Urea was obtained from the Beijing Kaiyin
Organic Fertilizer Production Co., China, and was used to adjust
the C/N ratio of the composting mass (Zhang et al., 2013). Microbial
inoculum, which consisted of a mixture of Trichoderma spp. (60%,
v/v) and Phanerochaete chrysosporium Burdsall (40%, v/v), was used
to accelerate the initial composting (Wei et al., 2007). Table 1 lists
the main physicochemical characteristics of the composting
materials.
2.2. Composting procedure
Nine treatments were used in the two-stage composting of GW
(Table 2). Two-stage composting includes a primary composting
stage (PC) and a secondary composting stage (SC) and results in
greater lignocellulose degradation than single-stage composting
(Zhang and Sun, 2017).
Before the start of the experiment, SW and/or BT were mixed
with GW in nine proportions as indicated in Table 2. The initial
moisture and C/N ratio of the nine composting mixtures were then
adjusted to 60% and 30%, respectively. The moisture content of the
composting mass was determined daily with an SK-100 moisture
meter (Tokyo, Japan) and was maintained at about 60% throughout
the composting process by addition of water. Finally, after the ini-
tial water content and C/N ratio were adjusted, the microbial
inoculum (5 ml kg 1 dry GW) was added, and the composting mass
was well mixed (Zhang and Sun, 2017).
On day 0 (the start of the PC), the composting mixtures were
added to digester cells. Each digester cell (6 m long  2 m
wide  1.5 m high) was a non-covered cement container with an
automatic compost-turning and -watering system. Three replicate
digester cells per treatment were used for the PC. The mixtures
were automatically turned over for 40 min every day during the
PC to increase aeration. When the composting temperature
dropped to 35–45 °C (on day 6 for all cells), the PC was considered
complete. On day 6 (the start of the SC), the mixture was removed
from each digester cell and formed into windrows (three windrows
per digester cell). Each windrow was about 3 m3, and was about
2 m long, 1 m high, and 1.5 m wide at the bottom. The windrows
were located in a ventilated area and were turned with a mini-
excavator (model DLS830-9B, Shandong, China) every 3 days to
ensure adequate aeration during the SC. When the temperature
of a windrow decreased and remained at the ambient temperature,
the composting process was considered complete. During the bio-
oxidative phase, the temperatures of treatments T1–T4 and T7
increased to 50–60 °C (the thermophilic temperature range) on
day 4 in the PC and on day 18 in the SC. In contrast, the tempera-
tures of treatments T5, T6, T8, and T9 increased to 50–60 °C on day
1 in the PC and on day 10 in the SC. Treatments T1 and treatments
T2–T4, and T7 required 30 days and 28 days, respectively, to
mature, while treatments T5, T8, and T9 required 24 days to
156 L. Zhang, X. Sun / Bioresource Technology 243 (2017) 154–162

Table 1
Selected physicochemical characteristics of green waste (GW), seaweed (SW), bentonite (BT), and final composts. Values are means (SD); n = 3. Treatments T1–T9 are described in
Table 2.

Treatment BD (g/cm3) WHC (%) TPS (%) AP (%) WHP (%)

GW 0.79(0.06) 48.11(1.31) – – –
SW – 98.62(1.10) – – –
BT – 89.53(2.03) – – –
T1 0.62(0.02)g 60.10(1.56)i 43.19(1.16)i 12.00(0.89)i 31.19(1.17)i
T2 0.58(0.03)f 68.35(1.22)h 54.28(1.32)h 17.02(0.65)h 37.26(1.02)h
T3 0.54(0.02)e 69.82(1.90)g 59.67(1.24)g 18.23(0.74)g 41.44(1.43)g
T4 0.49(0.01)d 74.61(0.98)e 67.73(1.38)e 22.51(0.19)e 45.22(1.20)e
T5 0.40(0.04)ab 81.03(1.76)b 82.51(2.04)b 27.02(0.50)b 55.49(1.39)b
T6 0.39(0.01)a 83.19(1.34)a 86.80(2.00)a 28.97(1.16)a 57.83(1.01)a
T7 0.53(0.01)e 72.24(1.04)f 63.95(1.65)f 20.45(1.20)f 43.50(1.54)f
T8 0.42(0.06)c 80.01(0.83)d 77.47(1.08)d 24.86(1.08)d 52.61(1.10)d
T9 0.41(0.03)bc 80.46(1.17)c 80.05(1.21)c 26.13(0.44)c 53.92(1.00)c
IRa 0.4000 75.00 70.00–90.00 20.00–30.00 50.00–60.00
pH EC (mS/cm) CEC (cmol/kg) WSOC/ON ratio –
GW 7.42(0.44) 1.84(0.42) 35.78(1.03) 24.12(1.02) –
SW 5.13(0.67) 1.20(0.63) 223.14(2.11) – –
BT 4.89(0.39) 1.09(0.74) 183.80(1.23) – –
T1 7.79(0.90)i 3.20(0.56)h 50.94(1.38)i 1.21(0.18)a –
T2 7.62(0.68)h 3.27(0.60)g 61.00(1.08)h 0.96(0.07)b –
T3 7.53(0.49)g 3.29(0.54)f 70.23(1.54)g 0.83(0.10)c –
T4 7.26(0.53)e 3.37(1.07)d 97.34(1.66)e 0.65(0.09)e –
T5 6.75(0.22)b 3.49(0.79)b 161.29(1.45)b 0.39(0.11)h –
T6 6.61(1.01)a 3.53(0.80)a 176.09(1.97)a 0.32(0.06)i –
T7 7.47(0.33)f 3.34(0.73)e 84.71(2.28)f 0.70(0.12)d –
T8 6.84(0.74)d 3.43(0.48)c 139.90(1.83)d 0.47(0.04)f –
T9 6.79(0.85)c 3.48(1.11)b 145.33(2.30)c 0.44(0.15)g –
IRa 6.50–7.50 <4.00 >60.00 <0.55 –

BD = bulk density; WHC = water-holding capacity; TPS = total porosity; AP = aeration porosity; WHP = water-holding porosity; EC = electrical conductivity (at 25 °C);
CEC = cation exchange capacity; WSOC/ON ratio = water soluble organic carbon/organic nitrogen ratio.
Means in a column followed by the same letter are not significantly different at p  0.05 by LSD.
a
IR = ideal range, according to Zhang and Sun (2014).

Table 2 content, NH3 and nitrous oxide (N2O) emissions, humic acid, TKN
Orthogonal design L9(34) of the experiment. content, and organic nitrogen (ON) content. The third part was
Treatment SW content in GW (% dry BT content in GW (% dry oven-dried at 65 °C for 24 h, crushed to pass through a 2-mm sieve,
weight) weight) thoroughly mixed, and used for analysis of the contents of total
T1 0 0 potassium (TK) and macro- and micro-nutrients.
T2 0 2.5
T3 0 4.5 2.4. Analytical methods
T4 35 0
T5 35 2.5
T6 35 4.5 2.4.1. Physical analyses
T7 55 0 WHC, total porosity (TPS), aeration porosity (AP), water-holding
T8 55 2.5 porosity (WHP), and bulk density (BD) of the composting materials
T9 55 4.5
and the final composts were determined by the ring knife method
GW = green waste; SW = seaweed; BT = bentonite. described by Zhang and Sun (2014). The particle-size distribution
of the final compost was determined by the sieve method of
Gabhane et al. (2012). The air-dried samples were passed through
mature. Treatment T6 required only 21 days to mature. The final soil sieves (mesh sizes of 0.10, 0.25, 0.50, 1.00, 2.00, and
characteristics of the nine compost products are shown in Table 1. 12.60 mm), and the material retained on each sieve was weighed.
The coarseness index (CI), expressed as a percentage (based on air-
2.3. Sampling dried weight) of particles >1 mm, was also determined (Jayasinghe,
2012).
Samples were collected 10 times (on day 0, 1, 4, 6, 10, 18, 21, 24,
28, and 30) during composting. Before sampling, the composting 2.4.2. Chemical analyses
mixtures were thoroughly turned. Subsamples were collected from pH and EC were determined in a 1:10 ratio of sample:water
the top, middle, and bottom (200 g per subsample) of each com- (w:v) using an MP521 pH/EC meter (Shanghai, China); CEC was
posting mixture and then mixed completely to obtain one repre- measured at pH 7.0 with ammonium acetate; and TKN was mea-
sentative sample per replicate digester cell or windrow. This sured by the modified micro-Kjeldahl procedure with a KDY-9830
representative sample was divided into three parts. One part was automatic Kjeldahl apparatus (Beijing, China) (Zhang and Sun,
immediately placed in a refrigerator at 4 °C and was subsequently 2016). The respiration rate (CO2 emission) was monitored with a
used for analysis of respiration rate, water soluble organic carbon ‘‘jar test” (Rawoteea et al., 2017); in this test, 25 g of fresh compost-
(WSOC) content, and enzyme activities (dehydrogenase, b- ing sample was placed in a jar along with a small beaker that con-
glucosidase, acid phosphatase, and alkaline phosphatase), and for tained 25 ml of 1.0 mol L 1 NaOH. After 24 h at 58 ± 2 °C, the NaOH
a seed germination test. The second part was air-dried (3–5% mois- was titrated with 1.0 mol L 1 HCl to calculate the CO2 emission rate.
ture content) and used for determination of physical characteris- Emitted NH3 was trapped in boric acid and detected by titration
tics, pH, electrical conductivity (EC), CEC, total phosphorus (TP) with 1 mol L 1 hydrochloric acid. N2O concentration was
 L. Zhang, X. Sun / Bioresource Technology 243 (2017) 154–162
determined using gas chromatography (Agilent Technologies
6890 N Network GC system, Beijing, China) as described by Wang
et al. (2016). Humic acid in the final compost was determined as
described by Moharana and Biswas (2016). The E4/E6 ratio, which
is the ratio of the optical density of humic acid solutions at 465
and 665 nm, respectively, was determined from the absorbance of
0.05 M NaHCO3 solutions containing 0.02% (w/v) final compost
(Zhang and Sun, 2014). ON was measured by the modified micro-
Kjeldahl procedure with a KDY-9830 automatic Kjeldahl apparatus
(Beijing, China); WSOC was determined in 1:10 (w/v) water
extracts using a Shimadzu TOC-5000A total organic carbon analyser
(Kyoto, Japan) (Zhang and Sun, 2017). The WSOC/ON ratio was then
computed based on the contents of WSOC and ON in the final
compost.
2.4.3. Enzyme activity analyses
The activities of dehydrogenase, b-glucosidase, acid phos-
phatase, and alkaline phosphatase were determined according to
the methods of Tiquia (2005), Oliveira and Ferreira (2014),
Frankenberger and Tabatabai (1980), and Wyszkowska and
Wyszkowski (2006), respectively.
2.5. Phytotoxicity test
The seeds of pakchoi (Brassica rapa) and lucerne (Medicago
sativa) were used in a seed germination experiment to assess the
phytotoxicity of the final compost (Zhang and Sun, 2017). Twenty
seeds were distributed evenly on a sterile 9-cm-diameter Petri dish
that contained a filter paper wetted with compost extract. The
compost extract was obtained by adding 50 ml of water to 5 g of
compost in a flask and agitating at 150 rpm for 1 h; the extract
was passed through a filter before it was used. Distilled water
was used as the control. Each treatment represented by three repli-
cate Petri dishes. After the dishes were kept at 25 °C in the dark for
72 h, seed germination and root lengths were determined in each
dish. The seed germination rate (SGR) and GI were calculated using
the following formula (Zucconi et al., 1981): SGR (%) = number of
germinated seeds in a replicate dish  100%/number of seeds in
that dish. GI (%) = (number of germinated seeds in a dish with com-
post extract  root length in that dish  100%)/(mean number of
germinated seeds in dishes with distilled water  mean root length
in that dish).
2.6. Statistical analysis
One-way analyses of variance (ANOVAs) were used to deter-
mine whether the physical and chemical characteristics differed
among the treatments. As noted earlier, the composting samples
collected from individual composting reactors and from individual
windrows were treated as replicates for each sampling time. For
statistical analysis of data, Microsoft Excel 2010 (Microsoft Corpo-
ration, USA) and SPSS Windows Version 16.0 (Statistical Package
for the Social Science, SPSS, Inc., Chicago, USA) were used. When
ANOVAs were significant, means were compared based on least
significant difference (LSD) at the 5% level of probability.
3. Results and discussion
3.1. Effects of additives on the WHC and porosity in the final compost
In the final composts, the values for WHC and porosity (TPS, AP,
and WHP) greatly differed (p < 0.05) among the treatments
(Table 1). Mature compost should provide a WHC of at least 75%
of dry weight (Rawoteea et al., 2017). The WHC values in treat-
ments T5, T6, T8, and T9 exceeded 75%. Treatment T6 (with 35%
157
SW and 4.5% BT) had the highest value, while treatment T1 had
the lowest. TPS values were within the acceptable range for treat-
ments T5, T6, T8, and T9; AP values were within the acceptable
range for treatments T4–T9; and WHP values were within the opti-
mal range for treatments T5, T6, T8, and T9 (Zhang and Sun, 2014).
The TPS, AP, and WHP values were highest in treatment T6 and
lowest in treatment T1. As a consequence, in terms of the physical
characteristics (WHC, TPS, AP, and WHP), treatments T5, T8, and T9
and especially treatment T6 produced more stable and more
mature compost products than the other treatments.
The WHC and porosity of the final compost indicate its ability to
hold sufficient water and to maintain gas exchange, respectively
(Zhang and Sun, 2014). Hence, the composts obtained in the treat-
ments with addition of both SW and BT, especially in the treatment
with 35% SW and 4.5% BT, had excellent water holding and gas
exchange characteristics. Because of their moisture absorption
and moisture retention properties, alginates in the SW could miti-
gate the hydrophobic characteristic of compost particles and
thereby enhance the penetration of water into the pores of the par-
ticles, reduce evaporation from particle surfaces, and increase the
WHC of compost (Ozdemir et al., 2014). Addition of SW to GW
composting could also contribute to the formation and develop-
ment of microscopic pores during composting (Hardouin et al.,
2014). Moreover, BT increased the WHC of compost due to its high
water-adsorbing capacity (Jiang et al., 2014). The skeleton void
ratio of BT also supports suitable gas exchange in the compost pro-
duct (Aranyos et al., 2016). Consistent with the findings of Zhang
and Sun (2016), the WHC of the compost products increased as
the CI value decreased (Section 3.2).
3.2. Effects of additives on the particle-size distribution and CI value in
the final compost
Table 3 shows the particle-size distributions and CI values of
the final compost products. Compost particles between 0.25 and
2.00 mm will tend to form a desirable network of pores that
increases the percentage of the WHC that is available to plants
(Gabhane et al., 2012). This was especially true for the treatments
T5, T6, T8, and T9, which were all amended with both SW and BT.
Treatment T6 (with 35% SW and 4.5% BT) had the highest percent-
age of particles between 0.25 and 2.00 mm, while treatment T1
had the lowest percentage. The CI values of the final composts
decreased (p < 0.05) with SW and/or BT addition. Jayasinghe
(2012) reported that good quality composts have CI values
between 30.0 and 45.0%; treatments T4–T6, T8, and T9 had CI val-
ues within this range.
The particle-size distribution and CI value of a compost product
are important because they influence its porosity, BD, and WHC,
and the uptake of water and nutrients by plants (Zhang and Sun,
2014). SW and BT in combination and especially the combination
of 35% SW and 4.5% BT increased the percentage of particles of
optimal size and improved the CI value. SW contains readily
decomposed organic matter that could favour particle aggregation
and therefore support increases in porosity and decreases in BD
during composting and in the compost product. The results
reported here for SW agree with those reported by Bernal et al.
(2009). Gums and binding molecules produced by SW degradation
could also improve the formation of aggregates in the final com-
post (Illera-Vives et al., 2015b). Moreover, the main component
of BT is montmorillonite, which is cohesive and enriched in pores;
these characteristics may be useful for obtaining a compost pro-
duct with the desired particle sizes and structural stability. Similar
observations were made by Li et al. (2012). SW and BT addition
also extended the thermophilic period, which could contribute to
a more complete degradation of GW (Section 2.2) and thus to an
improved physical structure (especially the particle-size distribu-
158 L. Zhang, X. Sun / Bioresource Technology 243 (2017) 154–162

Table 3
Particle-size distribution and coarseness index (CI) of final composts. The values for particle-size distribution and 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.

Treatment >12.60 (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 18.02 22.32 15.10 8.33 6.34 3.54 36.35 19.77(1.02)i 55.44(1.24)a
T2 0 32.53 20.18 12.09 7.21 4.43 23.56 39.48(0.65)h 52.71(1.13)b
T3 0 34.09 17.26 15.26 8.33 3.77 21.29 40.85(1.23)g 51.35(1.30)c
T4 0 28.26 16.33 20.45 10.09 7.26 17.61 46.87(0.79)e 44.59(1.09)e
T5 0 20.11 20.19 21.70 18.04 11.20 8.76 59.93(1.16)b 40.30(1.21)h
T6 0 16.87 22.42 19.06 20.30 9.44 11.91 61.78(0.83)a 39.29(1.40)i
T7 0 32.29 18.67 16.83 6.98 7.25 17.98 42.48(1.00)f 50.96(0.92)d
T8 0 27.41 15.09 20.02 15.20 9.19 13.09 50.31(1.34)d 42.50(1.35)f
T9 0 25.20 17.12 17.29 21.55 8.40 10.44 55.96(0.92)c 42.32(1.27)g
IRa – – – – – – – – 30.00–45.00

Means in a column followed by the same letter are not significantly different at p  0.05 by LSD.
a
IR = ideal range, according to Jayasinghe (2012).

tion) of the final compost (Zhang and Sun, 2016). In addition, 90%
of the compost particles should be smaller than 12.60 mm
(Gabhane et al., 2012), a standard that was achieved by all treat-
ments except the control (treatment T1) in the current study.
These results indicate that addition of SW and BT could accelerate
compost maturity and result in an optimal particle size distribu-
tion in the compost product (Gabhane et al., 2012).
activity and GW degradation because it contains a rich microbial
community (Leceta et al., 2014). BT could not only provide nutri-
ents for microorganisms to facilitate organic matter degradation
but could also increase the porosity so as to support gas exchange
and nutrient transformation during composting. Thus, BT addition
increased respiration and CO2 emission. This result was in accor-
dance with the observations of Meng et al. (2017) and Jiang et al.
(2014).

3.3. Effects of additives on the respiration rate during composting

3.4. Effects of additives on NH3 emission during composting
The respiration rates of treatments T5, T6, T8, and T9 increased
rapidly and peaked on day 1; the respiration rates in the other The trend in NH3 emission during composting was similar in all
treatments peaked on day 4 (Fig. 1). The respiration rates of all treatments (Fig. 2a): during the PC, NH3 emission increased to an
treatments subsequently decreased gradually until day 6. The res- initial peak and then decreased until day 6; during the SC, it again
piration rates then increased again and peaked on day 10 in treat- increased to a second peak and then decreased. Over the bio-
ments T5, T6, T8, and T9 and on day 18 in treatments T1–T4 and T7. oxidative phase, NH3 emission was lower in treatments T5, T6,
Thereafter, the respiration rates decreased until the end of com-
posting. Throughout the bio-oxidative phase, the respiration rates
were highest in treatments T5, T8, and T9 and especially in treat-
ment T6. The respiration rate was lowest in treatment T1.
The activity of microorganisms during composting is indicated
by the amount of CO2 released, and the respiration rate therefore
indicates the degradation rate of the organic matter and the stabil-
ity of the compost (Nikaeen et al., 2015). The respiration rate was
increased by SW or BT addition and especially by the combined
addition of SW and BT (the optimum was 35% SW and 4.5% BT).
Because it helps prevent pH increases and contains substantial
amounts of C, N, P, and K, SW can increase the activity of microor-
ganisms and therefore the rate of organic matter degradation and
CO2 evolution. The addition of SW could also enhance microbial

Fig. 1. Effects of seaweed (SW) and bentonite (BT) on the respiration rate during Fig. 2. Effects of seaweed (SW) and bentonite (BT) on ammonia (NH3) (a) and
the two-stage composting of green waste (GW). Treatments T1–T9 are described in nitrous oxide (N2O) (b) emissions during the two-stage composting of green waste
Table 2. Values are means of 3 replicates. (GW). Treatments T1–T9 are described in Table 2. Values are means of 3 replicates.
 L. Zhang, X. Sun / Bioresource Technology 243 (2017) 154–162
T8, and T9 (with the combined addition of SW and BT) than in the
other treatments NH3 emission was highest in treatment T1 and
lowest in treatment T6 (with 35% SW and 4.5% BT).
NH3 emission, which is the main reason for N loss during com-
posting, not only reduces the quality of the compost product but
also leads to environmental pollution at large composting facilities
(Zhang and Sun, 2017). In general, NH3 volatilization during com-
posting is increased by high temperatures and high pH (Wang
et al., 2016). Although addition of SW and BT to GW increased
the degradation rate, it also reduced NH3 emissions probably
because the N was assimilated rather than volatilized. Treatments
with the combined addition of SW and BT, and especially with 35%
SW and 4.5% BT, reduced the quantity of emitted NH3 and also
shortened the total time during which such emissions occurred.
Both SW and BT had low pH values (Table 1), which could decrease
the pH and therefore reduce NH3 emissions during composting. In
addition, SW contains nitrifying bacteria and related enzymes (i.e.,
glutamine synthetase and glutamate synthase) that can oxidize
NH3 into nitrite and then immobilize N (Leceta et al., 2014). BT is
a natural micro-mesoporous material with a high sorption capac-
ity, and its large surface area could adsorb NH3. The results
obtained here for BT agree with those reported by Fernandez-
Calvino et al. (2015).
3.5. Effects of additives on N2O emission during composting
The trends for N2O emission were similar to those for NH3 emis-
sion (Fig. 2b). N2O emissions were higher for treatment T1 (with-
out SW or BT), treatments T2–T4, and T7 (with SW or BT alone)
than for treatments T5, T6, T8, and T9 (with the combined addition
of SW and BT). In the bio-oxidative phase, N2O emissions were
highest in treatment T1 and lowest in treatment T6.
Bacteria that thrive under low oxygen conditions commonly
emit the greenhouse gas N2O, and N2O is therefore often released
if anaerobic conditions develop during compost storage (Wang
et al., 2016). N2O is emitted mainly because of incomplete nitrifica-
tion or denitrification (Wang et al., 2016). Compared to the control,
SW and BT addition significantly decreased N2O emissions during
composting, probably because their increased porosity supported
gas exchange (Section 3.1) and reduced the development of anaer-
obic conditions. As a consequence, the aerobic bacteria responsible
for ammonification and nitrification were probably enhanced
while the anaerobic denitrifying bacteria were probably inhibited.
These results agree with those of Wang et al. (2016) and Zhang and
Sun (2014). In addition, SW can contain microbial communities
that could inhibit denitrification and thus greatly reduce N2O emis-
sion (Leceta et al., 2014).
3.6. Effects of additives on the WSOC/ON ratio in the final compost
The WSOC/ON ratios were lower in the final compost products
than in the initial GW in all treatments (Table 1), which was con-
sistent with Moharana and Biswas (2016). The decline in the
WSOC/ON ratio was greater in treatments T5, T6, T8, and T9 (with
addition of both SW and BT) than in treatments T1–T4 and T7; the
decline was greatest in treatment T6 and was least in treatment T1.
The WSOC/ON ratio indicates the forms of organic C and N in
the composting mixture that are most susceptible to microbial
transformation and are therefore most responsible for compost
stability with respect to the total content of organic C and N
(Moharana and Biswas, 2016). The lower ratio in the final compost
than in the GW probably resulted from the degradation and trans-
formation of C and N. A WSOC/ON ratio <0.70 has traditionally
been used as an indicator of compost maturity, but Bernal et al.
(2009) proposed that a well-matured and stabilized compost
should have a WSOC/ON ratio <0.55. In the current study, WSOC/
159
ON ratios were lower in treatments with the combined addition
of SW and BT, and especially with 35% SW and 4.5% BT, than in
the other treatments. This is reasonable because SW contains read-
ily available organic matter that could increase microbial activity
and accelerate the decomposition of GW and the emission of
CO2, and thereby reduce the WSOC/ON ratio. A similar explanation
was proposed by Hardouin et al. (2014) and Stutter (2015). In addi-
tion, SW and BT addition improves the pore distribution, favouring
gas exchange and an increased capacity for water storage, which
would increase the rate of decomposition and enhance compost
maturity and stability (Hardouin et al., 2014; Jiang et al., 2014).
3.7. Effects of additives on the humification and E4/E6 ratio during
composting
Humic acid content in the final composts was significantly
increased (p < 0.05) by addition of SW or BT and especially by
the combined addition of SW and BT (Fig. 3a). The humic acid con-
tent was highest in treatment T6, followed by treatments T5, T8,
and T7, all of which had been amended with both SW and BT.
The values were lowest in treatment T1.
Humification is considered an indicator of GW compost matu-
rity because the humification of organic matter is an important
process in decomposition and therefore in composting (Zhang
and Sun, 2014). As previously discussed in this report, the com-
bined addition of SW and BT (especially the addition of 35% SW
and 4.5% BT) generated physical and chemical characteristics dur-
ing composting that enhanced microbial growth and activity,
which would increase the humification of organic matter and the
production of humic-like substances, and therefore enhance com-
post maturity and stability. In addition, the cellulose and hemicel-
lulose in GW are large molecules with many hydrophobic regions
which can reduce GW humification (Shi et al., 2006). As mentioned
above, the alginate in SW and the hydrophilic surfaces of BT could
reduce the hydrophobic nature of GW and therefore enhance GW
humification (Ozdemir et al., 2014).
An E4/E6 ratio 1.7 indicates that the compost is mature (Wong
et al., 2001). Based on that criterion, all of the compost products
except those for treatments T1–T3 were mature and suitable for
further use. The combined addition of SW and BT, and especially
of 35% SW and 4.5% BT, resulted in relative low ratios. Moharana
and Biswas (2016) reported that the E4/E6 ratio is directly corre-
lated with microbial abundance and activity. By supporting micro-
bial growth and activity (see Section 3.8), SW and BT could
enhance the humification of organic wastes (Hardouin et al.,
2014; Wyszkowska and Wyszkowski, 2006). Therefore, the com-
posting of GW with SW and BT could promote the accumulation
Fig. 3. Effects of seaweed (SW) and bentonite (BT) on the humic acid content (a)
and the E4/E6 ratio (b) during the two-stage composting of green waste (GW).
Treatments T1–T9 are described in Table 2. Values are means ± SE of 3 replicates.
160 L. Zhang, X. Sun / Bioresource Technology 243 (2017) 154–162
of stable humus, improve compost quality, and increase its E4/E6
ratio.
3.8. Effects of additives on enzyme activities during composting
The changes in the activities of dehydrogenase, b-glucosidase,
acid phosphatase, and alkaline phosphatase during the bio-
oxidative phase are shown in Fig. 4. In the PC and then in the SC,
enzyme activities significantly increased and then declined for all
treatments. Over the bio-oxidative phase, enzyme activities were
highest in treatment T6 and lowest in treatment T1.
Microbial degradation of organic matter relies on various
hydrolytic enzymes, and the most important of these are dehydro-
genase, b-glucosidase, acid phosphatase, and alkaline phosphatase
(Wyszkowska and Wyszkowski, 2006; Zhang and Sun, 2016).
Dehydrogenase is related to a group of enzymes that catalyse the
production of ATP through the oxidation of organic matter; b-
glucosidase is the rate-limiting enzyme in the microbial degrada-
tion of cellulose to glucose and plays a critical role in C cycling;
and acid and alkaline phosphatases are extracellular enzymes that
catalyse the hydrolysis of organic phosphates, releasing plant- and
microbial-available phosphate (Baker et al., 2011; Zhang and Sun,
2014). The current results indicate that both SW and BT addition,
especially 35% SW and 4.5% BT, greatly increased the activities of
these enzymes. SW is a good source of active polysaccharides
and macro- and micro-nutrients that support the synthesis and
secretion of enzymes by microorganisms (Baker et al., 2011). SW
also contains substantial amounts of many kinds of enzymes that
could enhance enzyme activity during composting (Leceta et al.,
2014). By adsorbing enzymes due to its porous microstructure
and high surface area, BT could provide the habitat and refuge
for enzymes and then enhance enzyme activity and stability
(Fernandez-Calvino et al., 2015). Because SW and BT have low EC
values (Table 1), their addition to GW did not substantially
Fig. 4. Effects of seaweed (SW) and bentonite (BT) on the activities of dehydrogenase (a), b-glucosidase (b), acid phosphatase (c), and alkaline phosphatase (d) during the two-
stage composting of green waste (GW). Treatments T1–T9 are described in Table 2. Values are means of 3 replicates.
increase the salt content of the compost, and a low salt content
could favour the formation and activity of phosphatase and other
enzymes that are important during composting (Zhang and Sun,
2016, 2014).
3.9. Effects of additives on the nutrient content in the final compost
Macro- and micro-nutrient contents of the final composts were
significantly higher (p < 0.05) in treatments T5, T6, T8, and T9 (with
both SW and BT addition) than in the other treatments (Table 4). In
the final composts, nutrient content was highest in treatment T6
(with 35% SW and 4.5% BT) and lowest in treatment T1.
Insufficient or unbalanced nutrients can reduce the usefulness
and therefore the quality of a compost. Macro- and micro-
nutrients in the compost product were increased by the combined
addition of SW and BT and especially by the addition of 35% SW
and 4.5% BT. SW and BT contain substantial quantities of macro-
and micro-nutrients, which when released would increase the
nutrient content of the compost (Kuwada et al., 2006; Li et al.,
2012). The adsorbent properties of BT could also reduce nutrient
leaching (Jiang et al., 2014). Furthermore, SW and BT addition
enhanced enzyme activities (Section 3.8) and thereby accelerated
the mineralization of GW, which would increase the release of
nutrients. A higher CEC value indicates an increased capacity to
retain nutrients. Therefore, the increased CEC values with addition
of SW and BT (Table 1) could also explain why nutrient contents in
final composts were higher with these additives (Zhang and Sun,
2016, 2014).
3.10. Effects of additives on compost phytotoxicity
To assess compost phytotoxicity, GI values were determined
for seeds exposed to compost extracts or distilled water. GI
values of pakchoi and lucerne seeds were substantially higher
 L. Zhang, X. Sun / Bioresource Technology 243 (2017) 154–162 161

Table 4
Contents of macro-nutrients (TKN, TP, TK, Ca, Mg, and S) and micro-nutrients (Fe, Cu, Mn, Zn, B, and Mo) in the final composts. Values are means (SD); n = 3. Treatments T1–T9 are
described in Table 2.

Treatment Macro-nutrients
TKN (%)a TP (%)a TK (%)b Ca (%)b Mg (%)b S (%)b
T1 1.85(0.29)i 0.24(0.08)i 0.48(0.06)i 1.05(0.10)i 0.58(0.10)i 8.35(0.87)i
T2 2.11(0.16)h 0.44(0.10)h 0.60(0.08)h 1.13(0.11)h 0.66(0.07)h 10.19(0.53)h
T3 2.53(0.44)g 0.51(0.05)g 0.76(0.12)g 1.16(0.20)g 0.71(0.11)g 11.80(0.82)g
T4 3.16(0.22)e 0.70(0.03)e 0.92(0.07)e 1.28(0.13)e 1.02(0.16)e 13.05(1.20)e
T5 4.62(0.35)b 1.06(0.12)b 1.22(0.16)b 1.55(0.35)b 1.31(0.30)b 16.03(0.79)b
T6 5.10(0.31)a 1.21(0.24)a 1.30(0.11)a 1.62(0.27)a 1.40(0.25)a 17.11(1.14)a
T7 2.84(0.07)f 0.63(0.06)f 0.83(0.10)f 1.21(0.44)f 0.84(0.09)f 12.36(0.76)f
T8 4.01(0.19)d 0.85(0.10)d 1.10(0.09)d 1.43(0.09)d 1.20(0.12)d 14.77(0.98)d
T9 4.38(0.45)c 0.92(0.09)c 1.17(0.05)c 1.49(0.38)c 1.27(0.54)c 15.24(1.02)c
Micro-nutrients
3
Fe (10 %)b Cu (10 3
%)b Mn (10 3
%)b Zn (10 3
%)b B (10 3
%)b Mo (10 3
%)b
T1 8.19(1.87)i 0.10(0.02)i 3.24(0.89)i 0.51(0.03)i 1.10(0.17)i 0.71(0.11)i
T2 11.44(1.03)h 0.21(0.05)h 5.12(1.01)h 0.65(0.10)h 1.39(0.65)h 1.03(0.02)h
T3 13.30(1.41)g 0.24(0.01)g 6.04(0.67)g 0.73(0.08)g 1.43(0.52)g 1.19(0.15)g
T4 17.36(0.87)e 0.32(0.06)e 7.03(1.12)e 0.87(0.09)e 1.61(0.41)e 1.30(0.10)e
T5 23.02(1.32)b 0.47(0.02)b 9.11(0.76)b 1.14(0.25)b 1.88(0.18)b 1.53(0.23)b
T6 25.11(1.10)a 0.52(0.03)a 10.20(1.03)a 1.23(0.21)a 2.09(0.22)a 1.62(0.09)a
T7 15.92(0.76)f 0.30(0.04)f 6.65(1.10)f 0.81(0.30)f 1.54(0.13)f 1.22(0.10)f
T8 21.08(1.24)d 0.40(0.01)d 8.24(0.95)d 1.05(0.46)d 1.73(0.27)d 1.46(0.07)d
T9 22.46(1.08)c 0.43(0.05)c 8.76(0.54)c 1.10(0.52)c 1.76(0.10)c 1.49(0.18)c

TKN = total Kjeldahl nitrogen; TP = total phosphorus; TK = total potassium.

Means in a column followed by the same letter are not significantly different at p  0.05 by LSD.
a
Percentages are based on air-dried weight.
b
Percentages are based on oven-dried weight.

(p < 0.05) in treatments T5, T6, T8, and T9 (with the combined
addition of SW and BT) than in the other treatments (Table 5).
Treatment effects on radicle length (RL) and SGR were similar
to those on GI values. The RL, SGR, and GI values were highest
in treatment T6 (with 35% SW and 4.5% BT) and lowest in treat-
ment T1.
According to Zucconi et al. (1981), composts with GI values
>80% are mature and are not phytotoxic. Thus, all of the final com-
posts produced in this study, with the exception of those produced
by treatments T1 and T2 with lucerne seeds and treatment T1 with
tomato seeds, could be considered mature and stable. Negative
effects of compost products on plant growth are mainly caused
by high pH and high levels of soluble salts (as indicated by EC val-
ues) (Zhang and Sun, 2016). The pH (6.61–6.84) and EC (3.53–3.43)
values of compost products treated with both SW and BT were
within the range considered optimal for plant growth (Table 1)
and probably explain the high GI values. Overall, the seed germina-
tion test showed that addition of SW and BT (and especially 35%
SW and 4.5% BT) to GW not only promoted the maturity and stabil-
ity of the final compost and reduced its toxicity but also enhanced
its ability to support seed germination and seedling root
elongation.
For GI values and for many other characteristics measured in
this study, the combined effects of SW and BT were greater than
the sum of their individual effects. Determining the reason for this
will require additional research.
4. Conclusion
The present study indicated that the addition of SW and BT
improved the two-stage composting of GW. Addition of 35% SW
and 4.5% BT produced the highest quality and the most mature
compost and did so in only 21 days. This combination improved
the particle-size distribution of the compost and increased its
WHC and porosity. It also decreased NH3 and N2O emissions and
the WSOC/ON ratio, increased enzyme activities, enhanced nutri-
ent contents, and reduced phytotoxicity. Consequently, SW and
BT addition accelerated the degradation and humification of GW
in the two-stage composting.

Table 5
Radicle length (RL), seed germination rate (SGR), and germination index (GI) of pakchoi and lucerne seeds as affected by extracts from the final compost products. Values are
means (SD); n = 3. Treatments T1–T9 are described in Table 2.

Treatment Pakchoi Lucerne

RL (mm) SGR (%) GI (%) RL (mm) SGR (%) GI (%)
T1 8.05(0.35)i 76(1)f 70(2)i 6.11(0.54)i 73(1)f 79(3)i
T2 9.11(1.02)h 82(2)e 74(3)h 7.45(0.43)h 80(2)e 85(2)h
T3 10.73(0.89)g 83(1)e 81(1)g 8.38(0.89)g 84(1)d 94(2)g
T4 12.00(0.74)e 87(3)c 105(3)e 9.66(1.04)e 92(3)b 119(1)e
T5 17.34(0.97)b 100(1)a 160(2)b 15.07(0.73)b 100(1)a 171(3)b
T6 18.12(1.11)a 100(1)a 173(2)a 16.29(0.62)a 100(1)a 184(1)a
T7 11.59(0.56)f 85(2)d 92(1)f 9.01(0.56)f 88(2)c 100(1)f
T8 15.87(0.48)d 98(2)b 139(4)d 13.85(0.90)d 99(1)a 143(1)d
T9 16.22(1.20)c 99(3)ab 142(3)c 14.32(1.21)c 100(1)a 152(1)c
IRa – – >80 – – >80

Means in a column followed by the same letter are not significantly different at p  0.05 by LSD.
a
IR = ideal range, according to Zucconi et al. (1981).
162 L. Zhang, X. Sun / Bioresource Technology 243 (2017) 154–162
Acknowledgements
This study was supported by the Special Fund for Forest Scien-
tific Research in the Public Welfare (No. 201504205) and the Fun-
damental Research Funds for the Central Universities (No.
BLX2015-07). We also thank Prof. Bruce Jaffee for his linguistic
modification of this paper.
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