Bioresource Technology 209 (2016) 397401

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Bioresource Technology
j o u r n a l h o m e p a g e : w w w . e l s e v ie r . c o m / l o c a t e / b i o r t e c h

Short Communication

Speciation and transformation of heavy metals during vermicomposting of animal

manure
Baoyi Lv

a, b

, Meiyan Xing

b,

, Jian Yang

College of Ocean Science and Engineering, Shanghai Maritime University, Shanghai 201306, China

Institute of Biofilm Technology, Key Laboratory of Yangtze River Water Environment, Ministry of Education, College of Environmental Science and Engineering, Tongji
University, Shanghai 200092, China

highlights
Speciation and mobility of heavy metal in vermicomposting was investigated.
Earthworm could improve the stability and agriculture values of animal manure. Vermicomposting
alleviates the mobility and availability of heavy metals.
that the pH, total organic carbon and C/N ratio were
reduced, while the elec-tric conductivity and humic acid
increased after 90 days vermicomposting. Moreover, the
addition of earthworm could accelerate organic
stabilization in vermicomposting. The total heavy metals
in final ver-micompost from CD and PM were higher than
the initial values and the control without worms.
Sequential extraction indicated that vermicomposting
decreased the migration and availability of heavy metals,
and the earthworm could reduce the mobile fraction,
while increase the stable fraction of heavy metals.
Furthermore, these results indicated that vermicomposting
played a positive role in stabilizing heavy metals in the
treatment of animal manure.

abstract
article info
Article history:
Received 5 January 2016
Received in revised form 29 February 2016 Accepted 1 March 2016
Available online 5 March 2016
Keywords:
Animal manure
Vermicomposting
Heavy metal
Stabilization
Sequential extraction

compone
nts can
be
degraded
1. Introduction
and the
residuals
Land application is one of the mostare transeffective methods for han-dling with animal formed
manure as considerable quantity of organicinto
mat-ter and nutrient in it ( Lazcano et al.,stabilize
2008). Prior to application in agricultural fields, d
bio-stabilization technique was usually used tovermico
convert the animal manure into value-addedmpost,
which is
and biological sta-bilized product ( Hsua andrich of
Lob, 2001). Vermicomposting is a novelnitrogen,
technique that utilizing the joint action ofphosphor
earthworm and microor-ganism under aerobicus,
condition. In this method, most of the organicpotassiu

This work was

conducted
to
evaluate the effects
of
vermicomposting
on the speciation
and mobility of
heavy metals (Zn,
Pb, Cr, and Cu) in
cattle dung (CD)
and pig manure
(PM) using tessier
sequential extraction
method.
Results
showed

2016 Elsevier Ltd.

All rights reserved.

m and humic substance ( Song

et al., 2014). Besides theseh
positive effects, the heavyt
t
metals (e.g. Zn, Cu, Pb, Cr) inp
vermicompost have gained:
/

more and more attention ( Li

/
et al., 2009; Suthar et al.,d
2014). Unlike bio-degradablex
.
compounds,
d
o
i
.
o
Corresponding author.r
g
Tel./fax: +86 21 65984275.
E-mail
addresses:/
xingmeiyan@tongji.edu.cn,
1
xmy5000@163.com (M. Xing).
0
.

1
0
1
6
/
j
.
b
i
o
r
t
e
c
h
.
2
0
1
6
.
0
3

.015 0960-8524/ 2016

Elsevier Ltd. All
rights reserved.

heavy
metals
cant be
decompo
sed
in
vermico
mposting
process (
He et al.,
2009).
Moreove
r,
the
heavy
metals

can accumulate in soil, uptakeal. (2014) reported

by plants, and finally affect the that the heavy metals
health of animals and people(As, Pb, Cu, and Zn)
in
vermicom-post
through food chain ( Liu et al.,
were clearly higher
2005). Therefore, it is necesthan the initial values
sary to explore the changes and
due
to
organics
transformation of heavy metals
degradation
by
in vermicomposting.
vermicomposting.
Conversely,
a
The total content of heavy
reduction in heavy
metals in final vermicompost
metal (Pb, Cd, Cr, and
and the effect of earthworm on
Cu) contents after
that were reported by several
sludge
authors ( Goswami et al., 2014;vermicomposting was
Suthar et al., 2014).

Song etfound by Suthar et al.

(2014), which might

be caused by the high

accumulation of heavy
metals in earthworm
tissues. Never-theless,
most of these studies
focused
on
total
concentrations
and
neglected
the
fractionation
of
metals. According to
previous findings, the
mobility
and
bioavailability of trace
metals largely depend
on
their
specific
chemical
speciation
rather than total

398

B. Lv et al. / Bioresource Technology 209 (2016) 397401

earthworms was conducted

as control. Moisture content
content ( He et al., 2009; Wang et al.,
was kept at 7090% by
2013). Although several reports indicated
sprinkling distilled water.
that vermicomposting could significantly
Vermire-actors were put in
reduce the heavy metals extracted by
dark
with
temperature
diethylene triamine pentacetic acid (maintaining at 23 1 LC.
Song et al., 2014), the speciation and
transformation of heavy met-als in The samples collected at
vermicomposting have not been fullyinitial (0 d) and the end of
experiment (90 d) from
understood.
Sequential extraction can reveal the vermicomposting
and
mobility and potential risk of heavycontrol
were
air-dried,
metals under different environmentalground and sieved through a
0.15 mm nylon mesh for
conditions ( Yuan et al., 2011). He et al.
further analysis. 5 g worms
(2009) reported that aerobic composting
were randomly selected and
could decrease the heavy metals
placed in dark for 24 h to
belonging to exchangeable and carbonate
clear their gut, cleaned by
fraction, while increase the oxidizable and
distilled water, and freezeresidual forms of heavy metals. Recent
dried prior to heavy metals
study conducted by
Singh andanalysis.
Kalamdhad (2013) also indicated the
exchangeable and carbonate fractions of
Cu, Ni, and Cr were reduced during 2.2. Physico-chemical
vermicomposting of water hyacinth.analysis
However, limited data are available that
use sequential extraction to investigate the The pH and electrical
composition and transfor-mation of heavyconductivity (EC) were
metals
in
animal
manuredetermined by a pH and
vermicomposting. Therefore, cattle dungconductivity meter in water
(CD) and pig manure (PM) were selected extracts (1:20, w/v), respecas the substrates of vermicomposting, andtively. An elemental analyzer
the main objectives of this study were to: Vario EL III (German) was
(1) study the variations of heavy metalused to measure the C and N
(Zn, Pb, Cr and Cu) speciation in raw contents in samples. The
substrates and the final vermicom-post;humic acid-like C (HAC)
(2)
evaluate
the
effect
of and fulvic acid-like C (FAC)
vermicomposting on mobility andwere measured according to
bioavailability of heavy metals.
the report of Romero et al.
(2007).

2. Methods
2.1. Substrates and vermicomposting

2.3. Heavy metal analysis

Sequential

extraction

recommended by Tessier et
CD and PM were procured from aal. (1979) was used to
livestock farm in the rural areas of determine the speciation of
Pudong New District, Shanghai, China.Zn, Pb, Cr and Cu in
The raw manure was dried under sunlight samples. The heavy metal
for one week with periodic stirring beforewas divided into five
the experiment. Young non-clitellatedfractions: exchangeable (F1),
earthworms Eisenia fetida raised inbound to carbonates (F2),
laboratory were picked for further using. bound to Fe and Mn oxides
Vermicomposting was carried out in (F3), bound to organic
bench scale vermireactor (30 cm diameter matter (F4), and residual
20 cm depth, plastic container) with each (F5). The specific extrac-tion
fed with 500 g CD and PM (dry weight) procedure was given in
as the substrate, respectively. 50 non-Table S1.
clitellated earthworms (E. fetida) with
200 mg average individual live weight
were inoculated into the reactors. Three
replicates were established for each
reactor and the container without adding

The plastic containers

and glassware were soaked
in nitric acid over-night and
cleaned with deionized water
before use. 1.0 g dried
sample was used to extract
heavy metals in 50 mL
polypropylene
centrifuge
tubes. After each extraction,
the
super-natant
was
collected by centrifugation at
8000g for 5 min, filtered
through a 0.45 lm membrane
and diluted to volume. The
residue was washed with 10
mL of Milli-Q water by
shaking, then centrifu-gated
at 8000g for 5 min to recover
the solids without loss.
Heavy metal concentrations
in
all
extracts
were
determined by induc-tively
coupled
plasma
optical
emission spectrometry (ICP)
(Optima
2100
DV,
PerkinElmer). Heavy metal
contents in earthworm tissue
were digested using HNO3
HFHClO4 and determined
by ICP as well.

2.4. Statistical analysis

All
results
were
presented as the average of
three replicates. The nutrient
and heavy metal contents
were expressed on dry
weight
basis.
One-way
ANOVA following Tukeys
test was used to identify the
significant
differences
between raw material and
final products with or
without earthworms by SPSS
17.0. The probability level
used
for
statistical
significance was p < 0.05 for
all tests.
3. Results and discussion
3.1. Performance of
vermicomposting
Vermicomposting
significantly modified the
physical
and
chemical
properties of raw substrates (
Table S2). The pH was obviously
lower
in
final
vermicompost and control as
compared to the initial
manure. This might be

ascribed to the generation of organic acids(11.2% and 11.6% for CD

from microbial metabolism duringand PM, respectively) in
compar-ison with initial
decomposition of raw substrates (
materials. The combined
Lazcano et al., 2008; Yadav and Garg,
action of earthworms and
2011). Moreover, the nitrification could
microorganisms was the
decrease the pH as well. On the contrary
main reason for more TOC
to pH, both vermicomposting and the
loss from raw manure as
control clearly increased the value of EC
in CD and PM. The release of solublerelative to the control (
salts, such as phos-phate, ammonium andYadav and Garg, 2011). C/N
nitrate could contribute to the increase of ratio is an important
indicator to assess the
EC ( Lazcano et al., 2008). It should be
maturity of compost or
noted that vermicompost had higher EC
vermicompost. In this study,
than the control, which indicating that
the reduction of C/N ratio
more avail-able mineral salts are
(43.6% and 28.9% for CD
accumulated in vermicompost over the
and PM, respectively) during
con-trol by organic matter degradation.
vermicomposting was much
more
significantly
as
compared to the control
As shown in
Table S2,(30.2% and 16.0% for CD
vermicomposting led to a significant sta- and PM, respectively) after
bilization in organic matter as reflected bythree months experiment.
the decline of total organic carbon (TOC).Therefore,
it
can
be
Moreover, the loss of TOC was more in concluded that the addition
ver-micompost (23.6% and 22.6% for CDof
earthworms
could
and PM, respectively) than the control accelerate the decomposition

of organic matter and

improve the stability of CD
and PM.

A great increase of HAC

was observed in the final
vermicompost ( Table S2),
which was consistent with
previous studies in vermicomposting of livestock
residues or other organic
wastes ( Romero et al.,
2007).
These
results
suggested
that
vermicompost-ing
could
stabilize raw organic wastes
by increasing the humus
contents
in
substrates.
Moreover, larger HAC was
found in vermi-compost than
that in the control, which
might indicate vermicompost
characterized with
higher humification degree.
The

B. Lv et al. / Bioresource Technology 209 (2016) 397401

earthworms could directly or indirectlytive to the change of pH, and

accelerate the humifica-tion processthe obvious decrease in pH
through their digestion, burrowing or after PM vermicomposting
simulating
microbial
activity
inmight increase F1 fraction.
Besides, F5 in vermivermicomposting ( Song et al., 2014). At
composting had similar
the same time, FAC decreased slightly
trends with the F1 in CD and
after vermicomposting. Romero et al.PM.
Vermi-composting
(2007) also reported that the FAC contentdecreased F2 fractions, while
in spent grape marc was not substantiallyincreased the F3 and F4
fraction of Zn in both
affected by vermicomposting.
treatments. In addition, F1
and
F2
fractions
in
3.2. Total contents of heavy metals
vermicomposts
were
lower
as
Total contents of heavy metalssignificantly
increased after the treatment with and
compared to the con-trol (
without earthworms in comparison to
Fig 2). E. fetida could absorb
initial values ( Fig. 1). Two pathwaysthe Zn from exchangeable
could affect the heavy metal contents in and
carbonates-bound
vermicomposting
process:
(i)
the
fractions ( Li et al., 2010).
bioaccumulation of earthworms, and (ii)
Therefore, the adop-tion by
volume reduction caused by organic
earthworms might be one
decomposition. The weight and volume
factor for the lower fractions
reduction resulted by mineralization and
of
F1
and
F2
in
decomposition of organic matter during
vermicompost than that in
vermicomposting could concentrate and
the control. Besides, the
increase the heavy metal contents ( Hsuaearthworms had slight effect
on F5 fraction of Zn, as no
and Lob, 2001; Zhu et al., 2014). In this
signif-icant difference was
study, vermicompost should contain more
found about this speciation
heavy metals than the control as
between vermi-compost and
vermicomposting had higher organics
the control.
degradation
rates.
Besides,
the
earthworms also accumulate some metals
Pb distributing in F1 and
in their tissues ( Table S3), thus reduceF2 fractions were clearly
reduced by vermicomposting
heavy metal contents in vermicompost (
of CD and PM ( Fig. 2). On
Sizmur and Hodson, 2009; Li et al.,
the contrary, Pb bound to
2010). In summary, the increase of heavyorganic/sulfide
was
metals in vermicompost indicated that theobviously increased after
concentration effect caused by organicvermicomposting. Moreover,
stabilization exceeded the accumulatedthe F3 fraction of Pb was
heavy metals in earthworm duringalso clearly increased in
vermicomposting.
vermi-compost. It might be
concluded
that
the
decomposition and conversion of organic materials
3.3. Heavy metal chemical speciation
into insoluble salts or humic
materials could immobilize
Pb
from
As shown in Fig 2, the CD and PMthe
treatments showed different changesexchangeable/carbonate
about
Zn
constitution
duringfractions, and thus develop
vermicomposting. F1 frac-tion wasto more stable forms in
greatly reduced from 3.0 to 0.7 mg/kg composting/
during CD vermi-composting, but itvermicomposting ( He et al.,
increased from 16.6 to 23.0 mg/kg in PM 2009; Song et al., 2014). In
vermicomposting. This might be caused addition, the fraction of F1
by the variation of pH between these twoand F2 in vermicompost was
treatments. It is reported that Zn is very significantly
lower
as
sensicompared to the control,
while Pb in F4 fraction was

399

clearly
higher
in
vermicompost
than
the
control.
A
suggested
mechanism
for
this
transformation
is
the
microbial
community
stimulated by earthworms
could enzymatically degrade
the organic matter and
release the metals into
solution
Hodson,

Sizmur and
2009),
then

combined with the humus (

Wang et al., 2013).
Most of Cr detected
belonged to organic and
residual fraction in CD and
PM ( Fig 2). Moreover, the
F1 and F2 fractions of Cr
were reduced in CD and PM
after vermicomposting. Total
F1 and F2 frac-tions
decreased by 35.3% and
22.2% in CD and PM after
vermicom-posting,
respectively. This suggested
that vermicomposting could
enhance the stability and
reduce the eco-toxicity of Cr.
It should

Fig. 1. Total concentrations of Zn, Pb, Cr and Cu

in raw substrates, control treatment and the
vermicompost. Columns annotated by the same
letter do not differ significantly (Tukey HSD test,
a = 0.05).

400

B. Lv et al. / Bioresource Technology 209 (2016) 397401

Fig. 2. Speciation of heavy metals (Zn, Pb, Cr, Cu) in raw substrates, control treatment and the vermicompost.

3.4. The mobility assessment of

heavy metals
be noted that the Cr bound to Fe/Mn oxides increased
significantly after vermicomposting, which was similar to In present study, the mobility
the change of Zn. In addition, Cr in F1 and F2 increased byfactor (MF) which calculated as
no-worm control, while ver-micomposting decreased it the ratio of heavy metal in F1+F2
fractions to the total contents,
clearly. As can be seen in Fig 2, the introduction of
was applied to evaluate the
earthworm reduced F5 fraction of Cr in CD treat-ment as
potential mobility of heavy
compared to the control, while earthworm increased the Cr
metals ( Narwal et al., 1999;
bounded with F5 fraction in PM.
Yuan et al., 2011). As shown in
Vermicomposting
significantly
reduced
theFig 3, Pb in mobile fractions
decreased significantly in both
exchangeable frac-tion of Cu in both of the two manures (
the CD and PM. This result was
Fig. 2). The uptake into earthworm body might be one
in accordance with previous
reason for this reduction. Li et al. (2010) has reported thatstudies that compost-ing and
E. fetida did absorb Cu and this bioaccu-mulation had vermicomposting could enhance
strong positive correlation with the concentration of
the stability of Pb ( He et al.,
exchangeable fraction. Moreover, Cu belonging to organic
2009; Singh and Kalamdhad,
and sulfuric fraction increased significantly in CD and PM
2013). The CD and PM treatafter vermi-composting. The substantial formation of humic
ments had similar influence on
materials might be responsible for the increasing organic
the mobility and availability of
and sulfuric fraction ( Hsua and Lob, 2001; Tandy et al., Cu, with the MF decreasing
2009). Besides, vermicomposting resulted in slightly lower obviously after vermicomposting.
F1 fraction of Cu as compared to the con-trol. It is reported
Li et al. (2009) have found that
that heavy metals could induce the synthesis of
metallothionein isoform in earthworm intestines, then bind Cu become more stable in PM
metal ions by forming organo-metallic ligands and thus after
reduce the exchangeable fraction of metals ( Goswami et
al., 2014). Moreover, the extractable heavy metals could
also be immobilized by insol-uble salt such as phosphates (
Yang et al., 2013). Furthermore, the earthworms enhanced
F4 fraction as relative to the no-worm con-trol. An increase
of Cu bound into organic matter was also reported for

Fig. 3. Comparisons of the mobility

factor of heavy metals in raw substrates,
control and the vermicompost. (a) cattle
dung; (b) pig manure. Columns
annotated by the same letter do not differ
significantly (Tukey HSD test, a = 0.05).

sewage sludge and water hyacinth vermicomposting ( Liu

et al., 2005; Singh and Kalamdhad, 2013).
transition through the gut of
earthworms
(E.
fetida).
Furthermore, it should be noted

that the MF of Zn was still the highest among the four introduction of earth-worms
heavy metals in PM even though vermicomposting could reduce the MF of heavy
decreased it clearly. Moreover, the MF of Cr was slightly metals in animal manure. For
changed after vermicomposting process. Besides, the example, the MF of Cu was
B. Lv et al. / Bioresource Technology 209 (2016) 397401

substrates properties could affect the

the control treatment. Other studies had also foundtransformation and mobility of heavy
earthworm activities could decrease the metalmetals during vermi-composting
availability by converting avail-able heavy metals process.
into unavailable fraction during vermicompost-ing
or vermifiltration system ( Yang et al., 2013; Song et
al., 2014).
Acknowledgements
The research was funded by the
National Natural Science Foundation of China (51109161), the PhD
Programs Foundation of Min-istry of
Compared
to
traditional
composting,
Education
of
China
vermicomposting com-bine the interaction of
(20110072120029), the Fundamental
earthworms and microorganisms, and the addition of
Research Funds for the Central
earthworms will undoubtedly increases the
Universities (0400219187), and the
complexity of heavy metal evolution in
National Spark Program of China
vermicomposting system. First of all, the
(2010GA680004).
earthworms could have direct effects on heavy
metals via uptaking it into tissue, namely as bioaccumulation or absorption, which was proved by
the increased heavy metal content in earth-worm
3.5. Heavy metal transformations during
vermicomposting

body after vermicomposting ( Table S3). This effect

was also confirmed by several studies which
conducted in soil or vermicom-posting experiment (
Sizmur and Hodson, 2009; Li et al., 2010). The other
mechanism was the process of mineralization and
humifica-tion under the interaction between
earthworms and microorgan-isms, which could also
affect
heavy
metal
transformation
in
vermicomposting. The variation of pH, organic
matter and humic acid will certainly affect the
speciation and mobility of heavy met-als ( Hsua and
Lob, 2001; He et al., 2009). This was similar to the
variation of heavy metals in traditional aerobic
composting ( He et al., 2009; Tandy et al., 2009). In
all, we concluded that the accu-mulation by
earthworms and the changes on physico-chemical
properties in substrates could affect the
transformation
of
heavy
metals
during
vermicomposting, and alleviate the mobility and
availability of heavy metals finally.

decreased by 56.4% after

vermicom-posting of CD, and
only a reduction of 28.1% was
observed after
401

Appendix A. Supplementary data

Supplementary data associated
with this article can be found, in the
online
version,
at
http://dx.doi.org/10.1016/j.biortech.2
016.03. 015.

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