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Changes in biochemical and microbiological parameters during the period of

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 Bioresource Technology xxx (2011) xxx–xxx

Contents lists available at ScienceDirect

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

Changes in biochemical and microbiological parameters during the period of

rapid composting of dairy manure with rice chaff
Dongyang Liu a, Ruifu Zhang a, Hongsheng Wu b, Dabing Xu a, Zhu Tang a, Guanghui Yu a, Zhihui Xu a,
Qirong Shen a,⇑
a
Jiangsu Key Laboratory for Organic Solid Waste Utilization, Nanjing Agricultural University, Nanjing 210095, China
b
Nanjing University of Information Science and Technology, Nanjing 210044, China

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

Article history: Various parameters were measured during the period of composting of dairy manure and rice chaff in
Received 6 May 2011 different ratios (dairy manure/rice chaff = V/V, pile 1: 75/25; pile 2: 80/20; pile 3: 85/15) to evaluate their
Received in revised form 15 July 2011 suitability as indicators for the composting process. The temperature in pile 1 increased rapidly and
Accepted 16 July 2011
remained above 60 °C for 30 days, while the temperature in pile 3 increased slowly relative to the other
Available online xxxx
two piles. Furthermore, the degradation of organic substrates, as indicated by the reduction of C/N ratio,
was rapid in pile 1 (below 20% 28 days after beginning of the composting). The major fluctuations of var-
Keywords:
ious water-soluble fractions in all piles were observed during the first 3 weeks, and the results in general
Composting
Dairy manure
showed that the highest microbial populations and enzymatic activities also appeared in this phase. Var-
Water soluble fraction ious parameters indicated that the rapid composting method was a feasible one for treating agricultural
Enzymatic activity wastes.
Microbial groups Ó 2011 Elsevier Ltd. All rights reserved.

1. Introduction rapid, is a useful way of transforming organic wastes into valuable

Many farmers in China have experienced declined crop yields
and qualities in recent years as a consequence of decreased soil fer-
tility. This low fertility has been caused by nutrient depletion
through excessive harvesting and insufficient return of nutrients
through the application of chemical fertilizer or organic matter.
However, continuous applications of chemical fertilizer has led to
the loss of soil structure, leading to compaction, wasted fertilizer
and environmental pollution including nitrous oxide emissions
and eutrophication of water bodies. Organic wastes can be a valu-
able and inexpensive soil conditioner and a source of plant nutri-
ents. The traditional application of organic manures as
amendments to improve long-term soil fertility and productivity
has been very effective (Goyal et al., 2005), but the number of
farmers to use organic manures in cultivation is becoming less
and less. On the other hand, a sudden increase of animal husbandry
in relatively big scales in China has lead to a big production of a
large volume of animal manure that occupies a significant land
area and constitutes a major source of pollution if not treated
appropriately. Application of undecomposed wastes or immature
composts to land can lead to the immobilization of plant nutrients
and cause phytotoxicity due to insufficient biodegradation of
organic matter (Butler et al., 2001). Composting, especially when
⇑ Corresponding author.
E-mail address: shenqirong@njau.edu.cn (Q. Shen).
organic amendments for soils (Said-Pullicino et al., 2007).
Composting proceeds through three phases: the mesophilic
phase, which lasts for a few days, is characterized by the activity
and growth of mesophilic organisms, leading to a rapid increase
in temperature. The thermophilic, or high-temperature, phase
can last from a few days to several months. In this phase, thermo-
philic organisms dominate the degradation process, and the
growth and activity of non-thermotolerant organisms are inhib-
ited. Finally, a several-month cooling and maturation phase occurs,
characterized by the development of new mesophilic communities
(Amir et al., 2008). Traditional composting can take several
months, however, the land shortage and large volume of animal
manures in China require these wastes to be treated more quickly.
As a result of the current situation in China, we selected a rapid
composting technology that uses a turning machine with a crush-
ing function in our research and this technology is now being ex-
tended very quickly in China.
Composting is the microbial degradation of different organic
materials under moist, self-heating and aerobic conditions and is
a process characterized by a succession of various microbial popu-
lations. Large numbers of different mesophilic, thermotolerant and
thermophilic aerobic microorganisms play key roles in the com-
posting process. In this process, microorganisms break down or-
ganic matter and produce carbon dioxide, water, heat and
relatively stable organic products. Microorganisms promote the
degradation of organic materials through the activity of different

0960-8524/$ - see front matter Ó 2011 Elsevier Ltd. All rights reserved.
doi:10.1016/j.biortech.2011.07.052

Please cite this article in press as: Liu, D., et al. Changes in biochemical and microbiological parameters during the period of rapid composting of dairy
manure with rice chaff. Bioresour. Technol. (2011), doi:10.1016/j.biortech.2011.07.052
2 D. Liu et al. / Bioresource Technology xxx (2011) xxx–xxx
hydrolytic enzymes (Raut et al., 2008). Important enzymes in-
volved in the composting process included cellulase, b-glucosidase,
protease and xylanase, which depolymerize cellulose, hydrolyze
glucosides, promote N-mineralization and hydrolyze xylan, respec-
tively (Mondini et al., 2004). Characterizing and quantifying enzy-
matic activities during composting can reflect the dynamics of the
composting process in terms of the decomposition of organic mat-
ter and nitrogen transformations and may provide information
about the maturity of composted products (Tiquia, 2002). The en-
zymes secreted by various microorganisms during composting
break down several complex organic compounds, finally leading
to the formation of simple water-soluble compounds (Benitez
et al., 1999). Thus, the analysis of water-soluble fractions during
the composting process may be a useful tool for understanding
the entire process and evaluating the evolution of the organic mat-
ter (Castaldi et al., 2008).
In light of the above considerations, the main objective of this
investigation was to determine the efficiency of the rapid compost-
ing processes for dairy manure and rice chaff mixed in different ra-
tios, in which some useful parameters were determined to evaluate
composting process.
2. Methods
2.1. Source materials and composting experiments
Three composting experiments were performed in the compost
site with a big roof in Jiangying Lianye Biological Science and Tech-
nology Co., Ltd. (Wuxi, China) by using dairy manure and rice chaff
in different ratios: 75/25 (pile 1), 80/20 (pile 2) and 85/15 (pile 3)
(v/v), and the average ambient temperature was 14.3 °C. These
piles had the following dimensions: 5  1  1.5 m (length 
width  height). The compost feedstocks were dairy manure and
rice chaff, and the physicochemical properties of the raw material
were given out in Table 1. Dairy manure was collected from a cattle
ranch (Jiangying Bright Dairy & Food Co., Ltd. Wuxi, China), and the
rice chaff was obtained from Jiangying Lianye Biological Science
and Technology Co., Ltd.
Temperatures at different locations, including the top (125 cm
from the base of the pile), the middle (85 cm from the base of
the pile) and the bottom (25 cm from the base of the pile), were
measured using a glass thermometer (range: 20 to 100 °C, mea-
surement accuracy: 0.5 °C) during the composting process. The
piles were aerated by a turning machine at regular intervals, and
sampling was performed at 0, 3, 7, 10, 14, 18, 24, 28 and 40 days.
To ensure representative sampling, four longitudinal sections were
randomly dug from different parts of the piles, and the samples
drawn from different sections of the same pile were mixed. A total
of approximately 2 kg of subsamples were taken by this sampling
method. The collected samples were divided into two equal parts,
one was preserved at 4 °C, while the other part was ground and
sieved for subsequent analysis after air drying.
2.2. Chemical analyses
The moisture content of different samples was determined
based on weight loss at 105 °C, ending with a constant weight.
pH and electrical conductivity (EC) measurements were performed
Table 1
Physicochemical properties of compost feedstocks.
Moisture (% fw) pH Total C (%) Total N (%)
Dairy manure 84.3 7.5 44.15 ± 0.83 1.61 ± 0.19
Rice chaff 9.1 6.3 39.35 ± 0.71 0.97 ± 0.05
Moisture content is expressed as a% on a fresh weight (fw) basis; dw means dry weight.
Please cite this article in press as: Liu, D., et al. Changes in biochemical and microbiological parameters during the period of rapid composting of dairy
manure with rice chaff. Bioresour. Technol. (2011), doi:10.1016/j.biortech.2011.07.052
on aqueous suspensions of the fresh compost samples (1:6, w/v,
compost/water ratio) using a pH electrode (PB-10, Sartorius, Ger-
many) and a conductivity indicator (LF91, Wiss. Techn. Werkstat-
ten, Germany). Compost samples were analyzed for organic
carbon by oxidation with potassium dichromate (Walkley and
Black, 1934) and for total N using the Kjeldahl method (Kimberly
and Roberts, 1905). Results are expressed per dry weight of
material.
To analyze the water-soluble fractions of the composting mate-
rial, 20 g of fresh sample was extracted with 200 ml distilled water
(1:10 w/v ratio) by shaking for 24 h on a horizontal shaker at room
temperature, according to the method of Castaldi with some modi-
fications (Castaldi et al., 2008). The extracts were centrifuged
(12,000 rpm for 10 min at room temperature) and filtered through
0.45 lm filter membranes. The clear supernatant provided the
different water-soluble fractions for subsequent analyses. Water-
soluble carbon (WSC) and water-soluble nitrogen (WSN) were
determined using a TOC/TN analyzer (multi N/C 3000, Analytik Jena

AG, Germany). The concentrations of WSN-NHþ 4 and WSN-NO3 were
measured with an AutoAnalyzer (AA3, Bran and Luebbe, Germany).
The concentration of water soluble carbohydrates (WS-Carb),
expressed as mg of glucose, was measured spectrophotometrically
using the anthrone method (Brink et al., 1960). The concentration
of water soluble phenols (WS-P), expressed as gallic acid, was
determined using the Folin–Ciocalteau method (Shindo and
Kuwatsuka, 1977).
2.3. Microbiological analysis
Quantitative estimation of different culturable aerobic microor-
ganisms, including bacteria, filamentous eumycetes and actinomy-
cetes, was conducted during the rapid composting process by
inoculating the appropriate media with 0.1 ml volumes of different
tenfold serial dilutions according to the methods of Vargas-García
et al., 2010. Media and incubation times for different microorgan-
ism were as follows: nutrient agar for 2 days – aerobic bacteria;
rose bengal agar for 4 days – aerobic filamentous eumycetes;
sodium caseinate agar for 4 days – actinomycetes; cellulose agar
for 2 days – cellulolytic bacteria (Hatami et al., 2008); and mineral
salts cellulose agar for 5 days – cellulolytic fungi (Pečiulytė, 2007).
All microorganisms were incubated at 37 °C, and the numbers
were expressed as colony forming units (CFU) per dry weight of
composts.
2.4. Enzymatic activities
Enzymatic activities were analyzed using aqueous compost ex-
tracts prepared according to the method of Herrmann and Shann
(1993). The protease activity was evaluated by determining the
amount of amino acids released after incubating the aqueous com-
post extracts with casein according to the methods of Ladd and
Butler (1972). The urease activity was quantified based on the col-
orimetric determination of the ammonia released after incubating
aqueous compost extracts with a urea solution for 2 h at 37 °C
(García et al., 1995). Cellulase activity was quantified by measuring
reducing sugars according to the methods of Schinner and Von
Mersi (1990). b-Glucosidase activity was determined according to
the quantity of p-nitrophenol released after the incubation of aque-
C:N ratio NHþ
3 -N mg g
1
dw NO
3 -N mg g
1
dw P mg g1 dw K mg g1 dw
27.4 5.13 ± 0.17 0.61 ± 0.10 4.71 ± 0.16 22.41 ± 0.72
40.6 0.48 ± 0.05 0.31 ± 0.07 1.26 ± 0.11 16.38 ± 1.05
 D. Liu et al. / Bioresource Technology xxx (2011) xxx–xxx 3

ous compost extracts with a p-nitrophenol glucoside (pNPG) solu-
tion for 1 h at 37 °C according to the method of Masciandaro et al.
(1994). The xylanase activity was estimated according to the meth-
od of Schinner and Von Mersi (1990) using birchwood xylan as a
substrate, and the enzyme activity was expressed as lg sugar
g dw1 h1 under the assay conditions. Finally, dehydrogenase
activity (DA) was assayed according to the method of Barrena
et al. (2008) by detecting triphenyl formazan (TPF) in a triphenyl-
tetrazolium chloride (TTC) solution treated with aqueous compost
extracts. The values of DA were expressed as lg TPF g dw1 h1.
2.5. Statistical analysis
Data were reported as the means of three replicates and were
analyzed using a one-way ANOVA design with the software SPSS
16.0. Duncan test was used to separate the means.
3. Results and discussion
3.1. Changes in physico-chemical parameters during composting
Temperatures within a composting process indicate a rate at
which many of the biological process takes place and plays a
selective role in the evolution and succession of microbiological
communities (Hassen et al., 2001). Temperature measurements
within the composting matrix during the active phase give an ade-
quate real-time indication of the establishment of ideal conditions
that support microbial degradation (Said-Pullicino et al., 2007). The
temperature changes in different piles at different depths during
the composting process were shown in Fig. 1. The temperature of
pile1 and pile 2 increased rapidly to 55 °C except the bottom after
one day, and the peak temperature of pile1 and pile 2 was obtained
at 7 days for all locations except in pile 3, in which the temperature
increased gradually and reached its peak at 17 days for all loca-
tions. The interruptions in the temperature curve were due to
pile-turning and a rapid recovery of thermophilic conditions was
observed the following day, which indicated a recovery of the ther-
mophilic microbial population. Compost temperatures showed a
downward trend after day 33 especially at the top of pile1 and pile
2, and further turning over did not result in a rapid temperature in-
crease but, instead, gradually decreased except in pile 3. The de-
crease in the pile temperature was attributed to the depletion of
easily degradable organic materials (Caceres et al., 2006).
Moisture content, pH and EC were important parameters during
composting, and Table 2 showed the changes that occurred during
composting for the different piles. Moisture loss during the com-
posting process could be considered as an index of decomposition
rate because the heat generation that accompanied decomposition
drove vaporization (Liao et al., 1997). Moisture contents were

Fig. 1. Temperature variations during composting of different piles.

Please cite this article in press as: Liu, D., et al. Changes in biochemical and microbiological parameters during the period of rapid composting of dairy
manure with rice chaff. Bioresour. Technol. (2011), doi:10.1016/j.biortech.2011.07.052
4 D. Liu et al. / Bioresource Technology xxx (2011) xxx–xxx

Table 2 The changes in total organic carbon (TOC) content during the
Changes of moisture content, pH and EC during composting of different piles. composting process of the different piles were shown in Table 3.
Time Moisture content pH EC (mS cm1) The initial TOC in the piles varied from 41% to 43% and then de-
(days) (% fw) creased as the decomposition progressed, reflecting a notable min-
Pile Pile Pile Pile Pile Pile Pile Pile Pile eralization of organic matter. At the end of the process, the lowest
1 2 3 1 2 3 1 2 3 TOC was obtained in pile 1, and the highest in pile 3. The high TOC
0 64.6 68.4 71.9 7.03 6.98 6.98 2.13 2.03 2.01 mainly came from the higher concentrations of more recalcitrant
3 62.3 65.9 69.7 7.47 7.22 7.18 2.17 2.11 2.04 compounds present in pile 3 compared to the other two piles. Dur-
7 60.7 64.2 68.9 7.66 7.59 7.66 2.46 2.36 2.10 ing the composting process, most of the carbon was lost in the
10 59.6 62.1 67.1 7.29 7.13 7.37 2.87 2.33 2.08
form of carbon dioxide. Pile 3 contained the highest proportion
14 60.3 60.7 64.1 7.99 7.88 7.28 2.63 2.40 2.13
18 54.0 58.5 60.4 8.13 8.17 7.83 3.17 2.72 2.37 of dairy manure and the least rice chaff compared to the other
21 49.3 54.3 59.3 8.03 8.05 8.09 3.52 3.03 2.69 piles; hence, its decomposition occurred slowly. At the beginning
28 42.5 48.1 56.2 8.14 8.15 7.90 3.83 3.19 2.93 of the composting process, the total nitrogen (TN) varied from
40 40.3 46.7 50.7 8.15 8.23 8.05 3.87 3.23 3.04
1.22% to 1.39% of the dw material, with the lowest N in pile 1
Moisture content is expressed as a% on a fresh weight (fw) basis; EC: electrical and the highest in pile 3. The TN decreased with time until the
conductivity. 14th day and then increased continuously, except in pile 3, where
there was no obvious change over the time. The decrease in TN
could be attributed to the loss of N through the formation of
reduced from 64.6% to 40.3%, 68.4% to 46.7% and 71.9% to 50.7% for ammonia Goyal et al. (2005); the loss of carbon in the form of car-
pile 1, pile 2 and pile 3, respectively, during the composting pro- bon dioxide resulted in an increase in N content per unit material.
cess. Lower moisture loss (21%) was observed in pile 3 compared The initial C:N ratio of the piles ranged from 29.5 to 34.4, and the
to 24% and 22% loss in piles 1 and 2, respectively, as a result of C:N ratio decreased during the composting process, due to the loss
the slower rise in temperature and longer thermophilic phase. of carbon and the increase in N content per unit material.
The pH analysis of the compost samples from the different piles WSC is one of the active parameters in defining compost
showed a gradual change from neutral to alkaline conditions; how- stability. WSC concentrations decreased gradually during the
ever, an apparent decrease in the pH of all piles was observed as composting process in pile 1 (26.2–17.5 mg g1 dw) and pile 2
the degradation progressed, and then it increased after the mid- (29.2–19.0 mg g1 dw); however, it decreased gradually in the first
point of the composting process. These results were similar to week, then increased in the second week and decreased again until
those of Nakasaki et al. (2005). The initial high moisture content the end of the composting process for pile 3 (Fig. 2). The conditions
of the samples promoted fermentative metabolism and resulted were favorable for composting in piles 1 and 2, in which microbes
in the production of incompletely decomposed products such as abundantly proliferated and utilized the soluble compounds.
organic acids. In light of this observation, decreasing pH could be Although a portion of new WSC might be synthesized by microor-
due to the production of organic acids and the incomplete oxida- ganisms during composting (Castaldi et al., 2008), WSC degrada-
tion of organic matter. The subsequent increase in pH was attrib- tion and utilization were much greater, resulting in a sustained
uted to the production of ammonia associated with protein decrease during the composting process. A different situation oc-
degradation in the samples and to the decomposition of organic curred in pile 3 where the microbial activities were low compared
acids according to Ohtaki et al. (1998). to the other two piles because of the high moisture content and
The EC reflects the salinity of various substrates and it is also a low temperature; consequently degradation and utilization of
good indicator for the maturity of compost. The highest EC values WSC were much lower than the rate of synthesis, resulting in an
of the piles were obtained at the end of the composting process. increase in WSC in the second week of the composting process.
Yadav and Garg (2011) obtained the same results, and they indi- The WSN and WSN-NHþ 4 of the different piles showed a similar
cated that the increase in EC might have been due to release of dif- trend, being increased during the first week and reaching a peak
ferent mineral ions, such as phosphate, ammonium, and (4.3, 4.7, 5.4 mg g1 dw for WSN in piles 1, 2 and 3, respectively;
potassium. The increased moisture content during decomposition and 4.2, 3.5, 3.9 mg g1 dw for WSN-NHþ 4 in piles 1, 2 and 3,
reduced EC values. This finding indicated that the high water con- respectively) at 10 days. The amounts of WSN declined signifi-
tent during the initial stages reduced the decomposition rate and cantly after reaching a peak in each pile, and the amount of
facilitated the release of ions, such as Fe3+ and Mn2+, resulting in WSN-NHþ 4 remained unchanged until the 14th day in pile 1, while
decreased EC values (Niwagaba et al., 2009). The final EC values there was a certain tendency to decrease from the 10th day in piles
of each pile also confirmed this result. 2 and 3. In pile 3, the amount of WSN-NO 3 increased with time,

Table 3
Changes of organic carbon, total N and C:N ratio during composting of different piles. Values followed by the same letter are not significantly different according to the Duncan
Test (p = 0.05).

Time (days) Organic C (%) Total N (%) C:N

Pile 1 Pile 2 Pile 3 Pile 1 Pile 2 Pile 3 Pile 1 Pile 2 Pile 3
0 42.94 ± 0.79a 40.09 ± 0.52a 41.15 ± 0.37a 1.25 ± 0.03b 1.22 ± 0.01c 1.39 ± 0.05ab 34.4 32.8 29.5
3 39.29 ± 0.52b 38.17 ± 1.13ab 40.28 ± 0.71ab 1.20 ± 0.02bc 1.22 ± 0.01c 1.38 ± 0.02ab 32.7 31.3 29.1
7 36.17 ± 1.21c 36.72 ± 0.72bc 40.10 ± 3.70a 1.10 ± 0.07d 1.21 ± 0.01bc 1.40 ± 0.01ab 32.9 30.4 28.7
10 34.14 ± 1.09d 37.73 ± 2.32cd 39.10 ± 0.52abc 1.11 ± 0.01d 1.14 ± 0.03bc 1.33 ± 0.05b 30.8 33.0 29.4
14 30.49 ± 0.72e 35.77 ± 0.62cd 39.37 ± 1.22abc 1.09 ± 0.04d 1.12 ± 0.02bc 1.40 ± 0.02ab 28.0 31.9 28.0
18 30.04 ± 0.98e 34.51 ± 1.48de 38.92 ± 0.16abc 1.18 ± 0.04bc 1.25 ± 0.11b 1.32 ± 0.05bc 25.4 27.6 29.5
21 28.09 ± 1.01f 33.95 ± 2.39e 38.04 ± 0.68bc 1.16 ± 0.03cd 1.27 ± 0.03b 1.25 ± 0.05c 24.3 26.8 30.5
28 25.88 ± 0.84g 29.88 ± 0.62f 37.22 ± 0.92c 1.43 ± 0.07a 1.46 ± 0.11a 1.35 ± 0.08ab 18.3 19.6 27.5
40 24.62 ± 1.01g 27.73 ± 1.01g 34.83 ± 0.18d 1.47 ± 0.02a 1.52 ± 0.03a 1.44 ± 0.03a 16.7 18.2 24.2

Expressed as% dw.

Please cite this article in press as: Liu, D., et al. Changes in biochemical and microbiological parameters during the period of rapid composting of dairy
manure with rice chaff. Bioresour. Technol. (2011), doi:10.1016/j.biortech.2011.07.052
 D. Liu et al. / Bioresource Technology xxx (2011) xxx–xxx 5

Fig. 2. Changes of water soluble fractions in different piles during composting. Results are the mean of three replicates, and bars indicate standard error of three replicates.

peaking (0.085 mg g1 dw) at 28 days; however, there was no sig-
nificant difference in the other two piles during the composting
process. Nitrifying bacteria, which oxidized reduced compounds
for energy, were likely responsible for nitrate accumulation during
the composting process.
The WS-Carb fraction mainly consists of hexose and pentose
monomers, which are the most labile and therefore the most sensi-
tive for indicating biochemical transformations of the matrix during
composting (Castaldi et al., 2008). Pile 1 and pile 2 showed a similar
trend in the change of WS-Carb (Table 4), and the highest content
(3.83, 3.98 mg g1 dw for piles 1 and 2, respectively) were obtained
on the 10th day; and for pile3, the highest value was at the begin-
ning of the composting process, and another peak (3.73 mg g1 dw)
was obtianed at the 10th day then it decreased until the end of the
process. The increase in the WS-Carb fraction in the first week
might be from the microbial degradation of cellulose and hemicel-
luloses in the matrix (Canet and Pomares, 1995). After that time
point, the WS-Carb fraction decreased sharply until the end of the
composting process. The major phenolic fraction was generated
by the partial degradation of lignin, which was recalcitrant to
microbial degradation due to its aromaticity. However, because of
their simple structure and smaller size, water-soluble phenol frac-
tions were more sensitive to the transformations occurring during
the composting process. The WS-P in different piles increased with
the time and the peak contents (2.81 mg g1 dw for pile 1 and
2.54 mg g1 dw for pile 2) were obtained at 14 days and then

Table 4
Changes of WS-Carb and WS-P of different piles during composting. The results are expressed as mean plus standard error of three replicates. Values followed by the same letter
are not significantly different according to the Duncan Test (p = 0.05).

Time (days) WS-Carb (mg g1 dw) WS-P (mg g1 dw)
Pile 1 Pile 2 Pile 3 Pile 1 Pile 2 Pile 3
0 3.10 ± 0.22bc 3.66 ± 0.11cd 3.81 ± 0.23a 1.88 ± 0.10e 1.72 ± 0.11d 2.55 ± 0.11a
3 2.82 ± 0.29bc 2.85 ± 0.22e 3.22 ± 0.18c 2.18 ± 0.13cd 2.02 ± 0.08bc 2.44 ± 0.21ab
7 3.65 ± 0.26a 3.67 ± 0.13cd 3.33 ± 0.17c 2.55 ± 0.12b 2.19 ± 0.03b 2.50 ± 0.24a
10 3.83 ± 0.20a 3.98 ± 0.30b 3.73 ± 0.13ab 2.56 ± 0.12b 2.51 ± 0.18a 2.35 ± 0.02ab
14 3.25 ± 0.21b 3.42 ± 0.20a 3.42 ± 0.03c 2.81 ± 0.13a 2.54 ± 0.14a 2.44 ± 0.05ab
18 3.19 ± 0.30b 2.97 ± 0.23s 3.48 ± 0.16bc 2.53 ± 0.12b 2.19 ± 0.16b 2.22 ± 0.08bc
21 2.91 ± 0.05bc 2.78 ± 0.12d 2.80 ± 0.12de 2.36 ± 0.09bc 2.09 ± 0.15bc 2.05 ± 0.14c
28 2.69 ± 0.25cd 2.05 ± 0.21f 2.96 ± 0.14d 2.22 ± 0.05cd 2.04 ± 0.22bc 1.59 ± 0.09d
40 2.35 ± 0.17d 1.92 ± 0.17f 2.67 ± 0.04e 2.12 ± 0.07d 1.82 ± 0.17cd 1.71 ± 0.17d

Please cite this article in press as: Liu, D., et al. Changes in biochemical and microbiological parameters during the period of rapid composting of dairy
manure with rice chaff. Bioresour. Technol. (2011), doi:10.1016/j.biortech.2011.07.052
6 D. Liu et al. / Bioresource Technology xxx (2011) xxx–xxx

decreased gradually reaching a final point of 2.22 and
2.04 mg g1 dw for pile 1 and pile 2, respectively. The decrease in
WS-P could be attributed to utilization by microorganisms either
as an energy source or as substrate for the synthesis of new com-
pounds according to Castaldi et al. (2008). However, the highest
WS-P content of pile 3 was detected at the beginning of composting,
suggesting a low efficiency of biodegradation in this pile.
3.2. Changes in the microbiologic populations during the composting
process of each piles
Microbial succession plays an important role during decompo-
sition, acting as an indicator of the composting process, and the
appearance of specific microorganisms reflects the maturity of
compost (Ishii et al., 2000). Various methods can be used to evalu-
ate different microorganisms, such as measurements of ATP con-
tent, microbial biomass and microbial community composition
and analysis of phospholipid fatty acid (PFLA) profiles (Goyal
et al., 2005), and real-time quantification was also used to estimate
the microbial populations (Sharma et al., 2011). However, until
now, no single method has been demonstrated to be reliable for
evaluating the microbial succession. In our study, changes in cul-
turable microbial communities were monitored by plating serial
dilutions on selective agar.
Populations of total aerobic bacteria of pile 1 increased gradu-
ally and were found to be the largest at 14 days, and then de-
creased gradually until the end of the composting period (Table
5). However, the tendency of decrease from 21st day was quite
weak compared to the tendency of increase within the initial
14 days. Total aerobic bacteria in pile 2 also peaked at 14 days
but did not show a subsequent downward trend; in contrast, the
aerobic bacteria in pile 3 increased slowly and remained at a low
level relative to the bacteria in the other two piles. Similarly, the
highest filamentous eumycete population was observed at 14 days
in pile 1, while it was obtained after 21 days in pile 2; this popula-
tion then decreased sharply in the both piles. In contrast to the
other two piles, the filamentous fungi population of pile 3 in-
creased gradually and then remained at a relatively stable level un-
til the end of the composting. In early stage of composting, bacteria
were thrived as the major fast growers responsible for the initial
decomposition of organic matter and the generation of heat
(Rashad et al., 2010). Tiquia et al. (2002) also studied microbial
succession during composting and reported that most fungi were
eliminated when temperatures exceeded 50 °C but the populations
recovered when the temperature decreased to below 45 °C. How-
ever, a large number of colony forming units of filamentous eumy-
cetes was obtained at the active phase of the composting. Similar
results were obtained by Goyal et al. (2005) who reported a high
mesophilic fungal population (144  107 cfu g1 dw). In the pres-
ent study, there were no significant differences in the size of the
actinomycete community between the three piles at the initial
stages of composting. In pile 1, the population of actinomycetes in-
creased quickly, and the peak was obtained at the active phase
(21 days). In contrast to other microorganisms, the population of
actinomycetes in pile 2 was higher than in pile 1 at 21 days.
Lignocellulolytic microbial communities play a key role in the
biodegradation that occurs during composting because lignocellu-
lose is the main component of organic wastes (Vargas-García et al.,
2010). The communities involved in lignocellulose biotransforma-
tion were detected throughout the entire composting process. The
succession of total aerobic cellulolytic bacteria was tracked, and
these reached peak values in all three piles at different stages of
the process, although the rates of increase in all piles were very
low at the initial phase of composting. These low rates might be
due to the existence of copious water-soluble carbon fractions at
the early stage of the process. Microorganisms preferentially uti-
lized these soluble and easily-degradable carbon sources, which
were present in the starting material; however, once the easily-de-
graded compounds were exhausted, the complex substrates such
as lignocellulosic materials started to be degraded, resulting in
the increase in lignocellulolytic microbial communities. The pro-
gression of cellulolytic fungi in the piles was different from those
of cellulolytic bacterial populations. The population size of cellulo-
lytic fungi increased gradually and the largest populations were
obtained at 14 days in pile 1. However, the population size of cel-
lulolytic fungi decreased at the initial stage of piles 2 and 3, and the
peak was detected at 21 days in pile 2, and the largest populations
of cellulolytic fungi in pile 3 occured at the beginning and at the
end of composting process.
3.3. Evolution of enzyme activities during the composting process
Microbes reproduced in the composting pile metabolize insolu-
ble particles of organic matter by secreting different hydrolytic

Table 5
Evolution of microbiological populations during composting. Results are the mean of three replicates, data are expressed as log (CFU g1 dw).

Piles Composting time Total aerobic Filamentous Actinomycetes Total aerobic cellulolytic Total aerobic cellulolytic
(days) bacteria eumycetes bacterial fungi
Pile 1 0 6.19 ± 0.23 5.38 ± 0.26 3.22 ± 0.14 3.39 ± 0.14 5.19 ± 0.19
3 7.81 ± 0.09 6.44 ± 0.10 4.16 ± 0.06 3.51 ± 0.23 5.83 ± 0.50
7 8.76 ± 0.16 6.68 ± 0.15 4.77 ± 0.09 4.54 ± 0.18 6.54 ± 0.18
14 9.59 ± 0.15 7.19 ± 0.10 5.28 ± 0.09 5.54 ± 0.12 7.47 ± 0.11
21 9.57 ± 0.10 7.05 ± 0.06 5.41 ± 0.13 5.22 ± 0.25 6.22 ± 0.25
28 8.75 ± 0.20 6.19 ± 0.12 4.52 ± 0.23 5.21 ± 0.28 6.04 ± 0.27
40 8.86 ± 0.07 6.03 ± 0.13 4.32 ± 0.08 4.95 ± 0.03 6.37 ± 0.18
Pile 2 0 6.34 ± 0.11 5.64 ± 0.18 3.41 ± 0.11 3.53 ± 0.18 5.38 ± 0.07
3 7.58 ± 0.07 6.01 ± 0.14 4.02 ± 0.05 3.75 ± 0.13 4.73 ± 0.02
7 8.65 ± 0.08 6.12 ± 0.08 4.29 ± 0.10 4.02 ± 0.05 5.54 ± 0.19
14 8.98 ± 0.03 6.33 ± 0.02 5.12 ± 0.05 4.83 ± 0.21 6.45 ± 0.35
21 9.03 ± 0.02 6.84 ± 0.07 5.80 ± 0.23 4.90 ± 0.08 6.42 ± 0.17
28 9.03 ± 0.02 6.22 ± 0.14 5.68 ± 0.13 4.99 ± 0.17 5.88 ± 0.24
40 9.12 ± 0.04 6.20 ± 0.09 5.33 ± 0.22 4.85 ± 0.11 5.76 ± 0.06
Pile 3 0 6.55 ± 0.13 5.94 ± 0.22 3.56 ± 0.18 3.56 ± 0.16 5.65 ± 0.09
3 6.93 ± 0.42 5.91 ± 0.20 3.64 ± 0.11 3.54 ± 0.14 4.65 ± 0.64
7 7.74 ± 0.06 5.76 ± 0.09 3.71 ± 0.13 3.80 ± 0.16 4.85 ± 0.26
14 7.87 ± 0.11 5.90 ± 0.31 3.99 ± 0.46 3.96 ± 0.14 4.80 ± 0.08
21 8.16 ± 0.08 5.87 ± 0.07 4.66 ± 0.14 3.91 ± 0.23 5.01 ± 0.06
28 8.34 ± 0.05 5.95 ± 0.06 4.56 ± 0.18 4.11 ± 0.08 5.44 ± 0.25
40 7.62 ± 0.12 6.20 ± 0.07 4.79 ± 0.11 4.23 ± 0.07 5.58 ± 0.16

Please cite this article in press as: Liu, D., et al. Changes in biochemical and microbiological parameters during the period of rapid composting of dairy
manure with rice chaff. Bioresour. Technol. (2011), doi:10.1016/j.biortech.2011.07.052
 D. Liu et al. / Bioresource Technology xxx (2011) xxx–xxx 7

enzymes. These various hydrolytic enzymes are thought to control
the degradation rates of different substrates, and they are the main
mediators of various degradation process (Tiquia, 2002). Thus, the
monitoring of various enzyme activities throughout the process
provides useful information on the dynamics of important nutri-
tional elements such as C and N and is beneficial for understanding
the transformations occurring during composting (Vargas-García
et al., 2010). Thus, changes in the concentrations of key enzymes
(protease, urease, cellulase, b-glucosidase, xylanase and dehydroge-
nase) were studied to understand how microbes degraded various
organic wastes.
Proteases, considered as appropriate indicators of organic mat-
ter decomposition, are important enzymes during the composting
process. At the beginning of composting, the protease activity
(Fig. 3A) was the highest in pile 1 (336.9 lg Tyr g1 dw h1) fol-
lowed by pile 2 (330.7 lg Tyr g1 dw h1) and pile 3 (190.7 lg
Tyr g1 dw h1) and then gradually decreased until the end of the
composting process, except for in pile 3. In pile 3, the protease
activity increased gradually, and the highest activity
(300.7 lg Tyr g1 dw h1) was obtained at 10 days and then
decreased to 105.4 lg Tyr g1 dw h1 at 40 days. The same trend
of protease activity was obtained by DE LA Horra et al. (2005) when
composting horse and poultry manures with wheat straw. The evo-
lution of protease in the different piles could be the result from
breakdown of complex nitrogen compounds to more simple frac-
tions, which occurred during the active phase of composting
(Cunha-Queda et al., 2007). Castaldi et al. (2008) found that prote-
ase activity was strongly correlated with the water-soluble nitrog-
enous forms. However, the correlations between protease activity
and water-soluble nitrogenous forms of the three piles were very
low. This low correlation might be due to the original materials
used for composting. The dairy manure contained a small number
of proteins, and these were degraded quickly in the initial stage of
the composting process.
Urease activity is involved in the hydrolysis of urea to ammo-
nium and carbon dioxide (Castaldi et al., 2008). The urease activity

Fig. 3. Evolution of protease (A) and urease (B) activities of different piles during composting. dw means dry weight basis, and results are the mean of three replicates, and
bars indicate standard error of three replicates.

Please cite this article in press as: Liu, D., et al. Changes in biochemical and microbiological parameters during the period of rapid composting of dairy
manure with rice chaff. Bioresour. Technol. (2011), doi:10.1016/j.biortech.2011.07.052
8 D. Liu et al. / Bioresource Technology xxx (2011) xxx–xxx

Fig. 4. Evolution of cellulase (A), b-glucosidase (B), aylanase (C) and dehydrogenase (D) activities of different piles during composting. dw means dry weight basis, and results
are the mean of three replicates, and bars indicate standard error of three replicates.

Table 6
Correlation matrix between enzymatic activities and microbiological populations during composting of different piles.

Protease Urease Cellulase b-Glucosidase Xylanase Dehydrogenase

Pile 2
Pile 1
Total aerobic bacteria 0.715 0.281 0.915* 0.648 0.878* 0.790
Filamentous eumycetes 0.456 0.487 0.825* 0.818* 0.829* 0.803
Actinomycetes 0.669 0.289 0.899* 0.671 0.865* 0.790
Total aerobic celullolytic bacterial 0.900* 0.059 0.893* 0.468 0.914* 0.678
Total aerobic celullolytic fungi 0.548 0.649 0.878* 0.918** 0.901* 0.893*
Total aerobic bacteria 0.763 0.173 0.932** 0.721 0.882* 0.891*
Filamentous eumycetes 0.773 0.092 0.816* 0.769** 0.926** 0.794
Actinomycetes 0.957** 0.201 0.917* 0.802 0.974** 0.886*
Total aerobic celullolytic bacterial 0.922** 0.072 0.959** 0.743 0.964** 0.946**
Total aerobic celullolytic fungi 0.717 0.094 0.884* 0.706 0.826* 0.910*
Pile 3
Total aerobic bacteria 0.287 0.199 0.921** 0.826* 0.812* 0.850*
Filamentous eumycetes 0.292 0.303 0.097 0.106 0.176 0.081
Actinomycetes 0.643 0.627 0.897* 0.683 0.979** 0.925**
Total aerobic celullolytic bacterial 0.371 0.405 0.917* 0.844* 0.871* 0.942**
Total aerobic celullolytic fungi 0.560 0.423 0.092 0.122 0.043 0.101
*
Correlation is significant at the 0.05 level.
**
Correlation is significant at the 0.01 level.

in pile 3 did not change obviously compared to the other two piles, Although the urease activities changed significantly in piles 1
and the highest activity (103.9 lg NHþ 4 -N g
1
dw h1) was and 2, the highest activity was obtained at 7 days for pile 1
obtained at the beginning of the composting (Fig. 3B). The activity (227.5 lg NHþ 4 -N g
1
dw h1) and at 10 days for pile 2 (222.3 lg
then remained at a lower level until the end of the composting. NHþ4 -N g1
dw h1
). These activities then decreased to a low level

Please cite this article in press as: Liu, D., et al. Changes in biochemical and microbiological parameters during the period of rapid composting of dairy
manure with rice chaff. Bioresour. Technol. (2011), doi:10.1016/j.biortech.2011.07.052
 D. Liu et al. / Bioresource Technology xxx (2011) xxx–xxx
similar to that in pile 3. Correlation analysis showed that the ure-
ase activity in piles 1 and 2 was strongly related to WSN and WS-
+
NHþ 4 (pile 1: WSN, r = 0.927; WS-NH4 , r = 0.919; P < 0.01, pile 2:
þ
WSN, r = 0.813; WS-NH4 , r = 0.791; P < 0.05), and the results were
consistent with those obtained by García et al. (1995), who pointed
out that the increase in urease activity was due to the availability
of WSN. However, the urease activity in pile 3 was not related to
WSN or WS-NH4+ (WSN, r = 0.222; WS-NHþ 4 , r = 0.079) in our
study.
The cellulase activity (Fig. 4A) increased gradually with the
decomposition process. The highest cellulase activity (93.1 lg glu-
cose g1 dw h1) was detected in pile 1 at 10 days, and the highest
activity (82.9 lg glucose g1 dw h1) was obtained in pile 2 at
14 days. In contrast to the other enzymes, cellulase in pile 3 in-
creased to 71.2 lg g1 dw h1 at 18 days and then decreased. Cel-
lulases were secreted by various cellulolytic microorganisms
developed on waste materials. In pile 1, more rice chaff that bene-
fited for the growth of cellulose-producing microorganisms was
added compared to the other two piles; thus, cellulase activity
was found to be the highest in this pile. b-Glucosidase was a key
enzyme involved in the degradation of polysaccharides, in which
polysaccharides were degraded by hydrolyzing the reducing termi-
nals of the b-D-glucose chains (Castaldi et al., 2008). Therefore, the
change in b-glucosidase activity could indicate the activities of dif-
ferent microorganisms. The b-glucosidase activity had a trend sim-
ilar to cellulase, showing an increase in its activity at the beginning
of composting in all piles, with the highest activity being obtained
in pile 2 (3.6 lmol p-nitrophenol g1 dw h1) at 21 days (Fig. 4B).
Cellulase and b-glucosidase played important roles in the degrada-
tion of cellulose, and the changes in their activities were correlated
with each other (pile 1: r = 0.751, P < 0.05; pile 2: r = 0.752,
P < 0.05; pile 3: r = 0.900, P < 0.01). Cellulase was negatively related
to the total carbon of each pile (pile 1: r = 0.672, P < 0.05; pile 2:
r = 0.59, P < 0.05; pile 3: r = 0.812, P < 0.01).
Cellulase is responsible for degrading cellulose, a process that
depends on the types of cellulolytic microorganisms developed in
the wastes. For all of the composting experiments, our results
showed a clear and consistent relationship between cellulase activ-
ity and all microorganisms (Table 6). Specifically, fungi are primar-
ily involved in the decomposition of cellulose, hemicellulose and
lignin present in the organic matter (Raut et al., 2008). However,
cellulase activity in pile 3 was not related to filamentous eumy-
cetes and total aerobic cellulolytic fungi, possibly because the
growth of cellulolytic fungi was insufficient during the composting
of pile 3 and because most of the cellulase was secreted by bacte-
rial species and actinomycetes. Correlation analysis results be-
tween b-glucosidase and different microorganisms indicated that
b-glucosidase activity was closely related to the presence of fila-
mentous eumycetes and total aerobic cellulolytic fungi in piles 1
and 2 (Table 6). These results indicated that fungi played a key role
in the decomposition of polymeric substances such as cellulose,
hemicellulose and lignin. Results obtained by Tiquia et al. (2002)
showed that b-glucosidase was also significantly positively corre-
lated to fungal populations (r = 0.98).
Xylanase is responsible for the hydrolysis of hemicellulose
(Goyal et al., 2005), one of the major components of the plant cell
walls, during the composting process. The initial xylanase activity
of pile 1 was 59.8 lg reducing sugar g1 dw h1, and then it in-
creased with the composting period and reached the peak
(191.7 lg reducing sugar g1 dw h1) at 14 days. The highest
xylanase activity (166.1 lg reducing sugar/g dw h) was obtained
in pile 2 at 18 days. The xylanase activity in pile 3 increased grad-
ually, and the peak (156.6 lg reducing sugar g1 dw h1) was ob-
tained at 21 days (Fig. 4C). Correlation analysis showed that
xylanase activity was positively correlated with cellulase (pile 1:
r = 0.769, P < 0.05; pile 2: r = 0.815, P < 0.01; pile 3: r = 0.913,
Please cite this article in press as: Liu, D., et al. Changes in biochemical and microbiological parameters during the period of rapid composting of dairy
manure with rice chaff. Bioresour. Technol. (2011), doi:10.1016/j.biortech.2011.07.052
9
P < 0.01) and b-glucosidase (pile 1: r = 0.706, P < 0.05; pile 2:
r = 0.897, P < 0.01; pile 3: r = 0.811, P < 0.01). Xylanase was posi-
tively correlated to all of the microorganisms that were detected
in piles 1 and 2 (Table 6).
Dehydrogenase, which is used as a measure of overall microbial
activity, is important for all microorganisms because it is involved
in the respiratory chain (Castaldi et al., 2008). During the first
10 days of composting, the highest dehydrogenase activity
(89.7 lg TPF g1 dw h1) was obtained in pile 1, while after this
time point, it progressively decreased until the end of composting.
The highest dehydrogenase activity (85.6 lg TPF g1 dw h1) was
recorded in pile 2 at 18 days; however, it increased gradually dur-
ing the composting progress in pile 3 and reached the peak
(65.2 lg TPF g1 dw h1) at the end of the composting process
(Fig. 4D). Because dehydrogenase activity stood for the overall pop-
ulation of heterotrophic microorganisms, it should be positively re-
lated to all microorganisms. However, correlation analysis
between dehydrogenase activity and various microorganisms indi-
cated that dehydrogenase activity was only significantly related to
filamentous eumycetes (r = 0.803) and total aerobic cellulolytic
fungi (r = 0.893) in pile 1, and it was not positively related to fila-
mentous eumycetes (r = 0.794) in pile 2. This finding could be
attributed to the detection technique used. Hardy and Sivasitham-
param (1989) concludes that culturing serial dilutions provide an
approximate estimate because the technique records only the
number of cells, spores and mycelial fragments growing on the
agar media, and slow-growing or non-culturable microorganisms
would be rapidly masked by opportunistic or abundantly sporulat-
ing microorganisms.
4. Conclusions
From this study, conclusions can be drawn that parameters
such as TOC, TC, pH, EC, water-soluble fractions, microbial popula-
tions and enzymatic activities can be considered representative
indicators that reflect the dynamics of rapid and good composting.
Various parameters show that pile 1 where dairy manure and rice
chaff is in the ratio of 75/25 has the most appropriate composting
condition and this ratio can be extended when composting indus-
try is developed.
Acknowledgements
This work was financially supported by the Chinese Ministry of
Science and Technology (2011CB100503), the Agricultural Ministry
of China (201103004), Priority Academic Program Development of
Jiangsu Higher Education Institutions and the ‘‘Fundamental Re-
search Funds for the Central Universities’’ to RZ (KYZ201003).
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