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Bioresource Technology 101 (2010) 5437–5443

Contents lists available at ScienceDirect

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

Chemical characterization and evaluation of composts as organic amendments

for immobilizing cadmium
Y. Tapia a,*, V. Cala b, E. Eymar a, I. Frutos a, A. Gárate a, A. Masaguer c
a
Departamento de Química Agrícola, Universidad Autónoma de Madrid, Francisco Tomás y Valiente 7, 28049 Madrid, Spain
b
Departamento de Geología y Geoquímica, Universidad Autónoma de Madrid, Francisco Tomás y Valiente 7, 28049 Madrid, Spain
c
Departamento de Edafología, ETSIA, Universidad Politécnica de Madrid, Avda. Complutense s/n, 28040 Madrid, Spain

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

Article history: The ability of three composted materials to immobilize cadmium (Cd) was examined in order to assess
Received 30 May 2009 their potential for recovering soils contaminated with this metal. Composted pine bark (PB) pH 5.6, spent
Received in revised form 1 February 2010 mushroom compost (SM) pH 8.0, and composted pruning waste + biosolids (BS) pH 6.9 (containing 81%,
Accepted 4 February 2010
75% and 47% total organic matter, respectively) were characterized. FT-IR and CP-MAS 13C NMR spectros-
Available online 1 March 2010
copy indicated the BS and SM to have a higher percentage of aliphatic and carboxyl groups than PB. The
composts were artificially contaminated with Cd (80 and 200 mg kg 1) and, after 4 weeks incubation,
Keywords:
subjected to sequential extraction. In column leaching experiments, the total Cd leached from the com-
Heavy metal immobilization
Column leaching
posts exposed to both Cd treatments was similar, but much less leached from the BS (0.2%) than the PB
Biosolids (4.0%) or SM (0.7%). The greater capacity of BS to immobilize Cd was attributed to the greater humifica-
tion of its organic matter and higher content of inorganic components, particularly Fe.
Ó 2010 Elsevier Ltd. All rights reserved.

1. Introduction Smernik, 2004). Currently there is intense debate surrounding

The pollution of soils by heavy metals is a serious environmen-
tal problem affecting many territories around the world. In Spain,
the soil of some 4532 ha may be contaminated by such metals,
excluding those also contaminated with radioactive waste and
mine tailings (Bernal et al., 2007). Among the heavy metals, cad-
mium (Cd) is one of the most toxic to enter the food chain. It is
more mobile and more soluble than other metals, and therefore
more likely to leach into the deeper layers of the soil, contaminat-
ing the groundwater. In situ addition of organic amendments to
contaminated soil aims to reduce the availability of heavy metals
(Chen et al., 2000; Basta et al., 2001; Li et al., 2001; Bolan et al.,
2003; Walker et al., 2003; Lee et al., 2004). Organic amendments
provide sites for their adsorption, favoring their immobilization
(Shuman et al., 2002).
Composted materials provide a suitable organic amendment for
the remediation of soils contaminated with heavy metals (Kiikkila
et al., 2001; Shuman et al., 2002; van Herwijnen et al., 2007). Bio-
solid composts, manure, peat, paper mill waste have all been used
to immobilize Pb, Cd and Zn (Basta et al., 2001; Bolan et al., 2003;
Adriano et al., 2004). Although composts – especially biosolids –
may contain heavy metals themselves, they can actually reduce
the bioavailability of these metals in the soil (Merrington and
* Corresponding author. Tel./fax: +34 914973827.
E-mail address: yasnatapiafernandez@gmail.com (Y. Tapia).
which fraction – organic or inorganic – is responsible for their
immobilization (Li et al., 2001; Stacey et al., 2001; Bolan et al.,
2003; Hettiarachchi et al., 2003; Merrington et al., 2003; Antonia-
dis et al., 2007; Kumpiene et al., 2008). However, different materi-
als and technologies used in composting mean that compost
variables such as the organic matter, nitrogen, dissolved organic
carbon (DOC), nitrate and soluble sugar concentrations, the pH
and the electrical conductivity (EC) can vary significantly (Zmor-
a-Nahum et al., 2007). It is therefore difficult to predict compost
behavior with respect to the adsorption/mobility of metals.
For an amendment to be effective it must be able to make heavy
metals less bioavailable. However, not all organic amendments
achieve this (van Herwijnen et al., 2007). The addition of organic
matter to soil may increase the DOC, encouraging the mobility of
heavy metals (Antoniadis and Alloway, 2002). Some functional
groups such as hydroxyl, phenolic, carboxyl and sulphydryl groups
control the adsorption, formation and activity of soil–metal com-
plexes (Lee et al., 2004; Karlsson et al., 2007), with carboxyl groups
being the most commonly involved (Alloway, 1995).
The solubility of metal contaminants dictates – at least to some
extent – their mobility and bioavailability (Basta et al., 2001). For
the study of such mobility, leaching column experiments have
proven useful (Eymar et al., 2002). However, few studies have
been performed to determine how metals leach from organic
amendments (i.e., to assess their ability to immobilize metals) be-
fore being applied to soils. The aim of the present study was to

0960-8524/$ - see front matter Ó 2010 Elsevier Ltd. All rights reserved.
doi:10.1016/j.biortech.2010.02.034
 Author's personal copy
5438 Y. Tapia et al. / Bioresource Technology 101 (2010) 5437–5443
determine the capacity of composted materials commonly used as
organic amendments or growth media (pine bark, spent mush-
room and pruning waste + biosolids composts) to immobilize Cd,
and to identify the chemical characteristics of these materials
influencing metal immobilization.
2. Methods
2.1. Composted materials
Composts produced from various materials were obtained from
different composting plants in Madrid, Cuenca and Avila (Spain),
respectively:
– Pruning waste + biosolids (BS) (1:3 w/w). This mix is composted
in tunnels with forced air for 14 days and matured in the open
air. Composting is completed in about 5–6 months.
– Spent mushroom compost (SM). An initial compost is produced
from wheat straw (55%), grape marc (15%) and poultry litter
(30%) (w/w); this is commonly used as a mushroom (Agaricus
bispoprus) cultivation medium. When such cultivation is fin-
ished further straw used in the cultivation of another mushroom
(Pleurotus ostreatus) is added (30% v/v), and this mixture com-
posted in the open air. Composting is completed in about
6 months.
– Pine bark compost (PB). Pine bark (mix different species of
pines: Pinus sylvestris, Pinus pinaster and Pinus pinea) is com-
posted for 4 months in the open air, adding urea and water.
The resultant mixture is then milled and sieved and allowed to
mature for a further 4 months. Peat and wood fiber (20%) are
then added.
2.2. Physico-chemical characterization
Electrical conductivity (EC) and pH were determined in water
extracts (1:5 v/v) using a conductivimeter Crison CM 2200 (Barce-
lona, Spain) and pH electrode Orion 720A (Beverly, MA, USA),
respectively. The bulk density of the samples was determined in
stainless steel cylinders by applying a suction pressure provided
by a 10 cm column of water using a sandbox Eijkelkamp (Giesbeek,
The Netherlands), and then drying the samples at 103 °C. The index
particle size was obtained by determining the percentage (by
weight) of particles with a diameter of >1 mm using a series of
sieves (FiltraÒ). The concentrations of soluble Ca, Na, Cl and
NO3 were determined in water extracts (1:5 v/v). Ca and Na were
determined by atomic absorption spectroscopy (AAS) using AA
Analyzer 800 Perkin Elmer (Waltham, MA, USA). Cl was measured
using a selective electrode (Orion 720A). NO3 was determined col-
orimetrically as described by Cataldo et al. (1975) using a Shima-
dzu UV-160A spectrophotometer (Kyoto, Japan). Total N was
determined by the Kjeldahl method in a Block Digest 12 apparatus
Selecta (Barcelona, Spain). Total P was determined colorimetrically
following the method of Murphy and Riley (1962) after digestion of
the samples in aqua regia (HNO3–HCl, 1:3). Total S was determined
using a Leco CHNS-932 element analyzer (St Joseph, MI, USA). Total
organic matter (TOM) was determined by combustion at 450 °C in
a muffle furnace (Select-Horn, P Selecta); total organic carbon
(TOC) was calculated as 58% of the TOM value (Walkley and Black,
1947). The effective cation exchange capacity (CECE) was deter-
mined at the natural pH of the composts using the method of Anso-
rena (1994). Humic extract carbon (CEXT) was determined
following the method of Stevenson (1994). The CEXT/TOC ratio
was calculated to asses the degree of humification of the organic
matter (Roletto et al., 1985; Clemente et al., 2006). The hydrosolu-
ble organic carbon was measured spectrophotometrically using the
method of Hernández et al. (2007). The total concentrations of hea-
vy metals (Cd, Cu, Fe, Mn, Pb and Zn) were determined by AAS after
that the samples were dried (55 °C), sieved (<63 lm) and digested
with aqua regia (HNO3–HCl, 1:3) (McGrath and Cunliffe, 1985). All
determinations were performed in quadruplicate.
2.3. Spectrometric characterization
All composts were subjected to Fourier-transformed infrared
spectroscopy (FT-IR) using an IFS60v spectrometer Bruker (Bille-
rica, MA, USA); readings were obtained in arbitrary units of diffuse
reflectance. The composts were also subjected to cross-polariza-
tion and magic angle spinning nuclear magnetic resonance (13C-
CP-MAS NMR) in a Bruker AV-400-WB apparatus (Billerica, MA,
USA) (rotor spin rate 14 kHz; contact time 3 ms; acquisition time
2 s; 28,500 scans). Samples were packed in 4 mm zirconia rotors
with Kel-F caps. The pulse sequence was applied with a 1H ramp.
Chemical-shift (d) regions were divided into the main resonance
regions according to Stevenson (1994). Relative areas were ob-
tained from the integration of these regions.
2.4. Sample pretreatment
The pine bark (PB), spent mushroom (SM) and pruning
waste + biosolids composts (BS) were artificially contaminated
with Cd (CdSO4
8/3H2O) in the following manner: (1) 0 (control),
(2) 80 mg Cd kg 1 (80 Cd), or (3) 200 mg Cd kg 1 (200 Cd) dry mat-
ter. Samples were incubated for 4 weeks under laboratory condi-
tions (18 °C and 38% relative humidity [RH]). All samples were
shaken periodically. The moisture level was maintained at about
70% of the container capacity.
2.5. Cd extraction (DTPA-CaCl2)
Extractable Cd was determined in 1:5 (v/v) DTPA-CaCl2 (pH 2.6;
DTPA concentration 0.002 M) extracts of fresh samples of compost
BS, SM and PB (200 Cd treatment). All extracts (four replicates per
sample) were shaken for 1 h and filtered through a 0.45 lm micro-
filter. Cd was determined by AAS.
2.6. Sequential extraction of Cd
Sequential Cd extraction was performed on the control and 200
Cd PB, SM and BS composts (four replicates per sample), following
the method of Tessier et al. (1979). This provides the distribution of
Cd in the FI fraction (the soluble and/or interchangeable fraction),
the FII fraction (associated with carbonates and/or acid soluble),
the FIII fraction (associated with Fe and Mn oxides), the FIV or oxi-
dizable fraction (associated with organic matter), and the FV or
residual fraction. The Cd content of every fraction was determined
by AAS.
2.7. Column leaching
Seven hundred and fifty milliliters of the control, 80 Cd- and
200 Cd-treated PB, SM and BS composts were placed in methacry-
late columns (50 cm high by 6 cm in diameter) attached to Büchner
funnels, as described in Eymar et al. (2002) (four replicates per
treatment). The columns were saturated with distilled water be-
fore irrigating; all were maintained under laboratory conditions
(18 °C, 38% RH) throughout the assay. Distilled water (100 mL,
pH 6.0) was poured daily into each column for 30 days. Leachates
were collected daily to determine their volume, pH, and Cd concen-
tration by AAS.
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Y. Tapia et al. / Bioresource Technology 101 (2010) 5437–5443 5439

2.8. Statistical analysis
The statistical analysis was based on the one-way analysis of
variance (ANOVA) of the mean values of each parameter for each
fraction obtained in sequential extraction procedure and each Cd
concentration in leachates, in order to test the statistically signifi-
cant differences. All statistical tests were carried out using the SPSS
(Statistical Product and Service Solutions) 13.0 software package.
To compare the differences between fractions and composts, the
Duncan test at p < 0.05 was used (SAS Institute, 1988).
3. Results and discussion
Greater humification of organic matter can contribute signifi-
cantly to reducing the solubility and mobility of heavy metals in
the soil via adsorption and the formation of stable complexes with
humic substances (Halim et al., 2003; Clemente et al., 2006). The
CECE, a determinant variable in Cd adsorption (Christensen and
Huang, 1999; Lee et al., 2004), increases with humification (Ste-
venson, 1994). The SM showed a higher CECE than BS probably be-
cause of its higher pH. The hydrosoluble organic carbon of the BS
was higher than that of the SM, indicating a greater presence of
more labile organic compounds such as sugars, polysaccharides
and simple peptides (Zmora-Nahum et al., 2007). The total concen-
tration of heavy metals in the three composts was below the max-
imum level permitted for organic amendments by Spanish law (RD
824/2005).

3.1. Physico-chemical properties of the composts

The physico-chemical properties of the different composts are
shown in Table 1. Spent mushroom compost (SM) had an alkaline
pH, while the pruning waste + biosolids compost (BS) was neutral
and the pine bark compost (PB) was slightly acidic. The BS had a
smaller index particle size; it therefore had a greater density and
a larger exchange surface than the SM and PB. The EC of the BS
was higher than that of the PB and SM, indicating it to have a high-
er ion content (mainly nitrates, chlorides, calcium and sodium).
The SM and BS had higher total N, P and S contents than the PB.
The TOM of the PB and SM was higher than that of the BS. The C/
N ratio of the BS (15.2) was lower than that of the SM and PB
(34.9 and 66.8, respectively), indicating a greater degree of matu-
rity of the organic matter (Huang et al., 2006). Generally, a C/N ra-
tio of 15–20 reflects compost maturity; however, pruning waste
contains components that are difficult to degrade, and values of
about 30 may reflect maturity (Benito et al., 2006). Similarly (and
also indicating compost maturity) the CEXT/TOC ratio of the BS
(30.4%) was higher than that of the SM (26.5%) or PB (16.9%).
Table 1
Main physico-chemical properties of the three composts. (Values are means ± stan-
dard deviations, n = 4.)
3.2. FT-IR spectroscopy
The infrared spectra of the three composts were qualitatively
similar, although some differences were seen in the peak intensi-
ties (Fig. 1). The BS had higher peak intensities than the PB or
SM at 3680 cm 1 (OH alcohols, phenols), 3599 cm 1 (O H, carbox-
ylic acids), 2891, 1475 and 976 cm 1 (C H, aliphatic groups),
2058 cm 1 (C N type R N@C@S), 1182 cm 1 (C O, tertiary alco-
hols) and 1028 cm 1 (H O, polysaccharides) (see Silverstein et al.,
1981). These results suggest that BS has a highly aliphatic nature
(Vaca-Paulín et al., 2006). The BS also showed the highest degree
of humification, according to the peak close to 1117 cm 1 (Illera
et al., 2000). Peaks at 1028 cm 1 are attributable to the presence
of minerals containing phosphates and silicates (Zmora-Nahum
et al., 2007), while those at 3680 cm 1 are attributable to the OH
of kaolinite (Shoval et al., 1999). The SM spectrum showed peaks
at 1772 cm 1 (C@O of carbonyls) and 2536 cm 1 indicating the
presence of –SH groups (Illera et al., 2000). Like the BS, the SM
showed peaks at 3599 and 2891 cm 1. The PB spectrum showed
a peak at 1547 cm 1 (C@C, aromatic). This might indicate that PB
has fewer carboxylic acids and a lesser aliphatic nature than BS
and SM. Cd complexes formed with organic matter functional

PB SM BS BS

pH (extract 1:5) 5.6 ± 0.1 8.0 ± 0.1 6.9 ± 0.1

EC (dS m 1 25 °C) (extract 1:5)a 1.07 ± 0.02 1.58 ± 0.03 2.42 ± 0.06
3680

2058

Bulk density (g cm 3) 0.24 ± 0.01 0.26 ± 0.01 0.44 ± 0.01

Index particle size (%) 27.8 42.7 18.2
3599

Ca (mg L 1) (extract 1:5) 45.7 ± 4.7 9.5 ± 2.3 142.7 ± 11.8

2891

1475

Na (mg L 1) (extract 1:5)

1182

976
1028

25.4 ± 0.5 27.0 ± 5.3 35.6 ± 2.3

Cl (mg L 1) (extract 1:5) 25.5 ± 2.5 85.9 ± 5.4 130.1 ± 5.1
SM
N–NO3 (mg L 1) (extract 1:5) 45.6 ± 1.8 4.0 ± 0.3 137.6 ± 4.0
Total N (%) 0.70 ± 0.11 1.24 ± 0.24 1.82 ± 0.11 4000 3200 2400 1600 800
Total P (%) 0.08 ± 0.02 0.65 ± 0.09 0.87 ± 0.09
Total S (%) 0.05 ± 0.02 0.66 ± 0.03 0.22 ± 0.05
2536

TOM (%)b 80.5 ± 1.5 74.6 ± 2.4 47.5 ± 2.0

TOC (%)c
1772

46.8 ± 0.9 43.3 ± 1.4 27.6 ± 1.1

C/N 66.8 34.9 15.2
CECE (cmol+ kg 1)d 24.5 ± 3.2 99.5 ± 1.3 66.7 ± 2.4
Humic extract carbon (CEXT) (%) 7.9 ± 0.4 11.5 ± 0.8 8.4 ± 1.9
Humification ratio (CEXT/TOC) (%) 16.9 26.5 30.4 4000
PB 3200 2400 1600 800
HOC (mg kg 1)e 30.5 ± 4.7 159.4 ± 19.9 203.5 ± 11.1
Cd (mg kg 1) 0.45 ± 0.01 0.88 ± 0.01 1.63 ± 0.20
Cu (mg kg 1) 7.1 ± 0.4 24.3 ± 1.1 124.2 ± 9.8
Fe (mg kg 1) 2665 ± 203 2036 ± 69 8733 ± 797
Mn (mg kg 1) 93.3 ± 6.0 135.6 ± 8.8 183.8 ± 3.4
Pb (mg kg 1) 12.1 ± 1.7 37.3 ± 0.2 100.7 ± 4.8
1547

Zn (mg kg 1) 26.4 ± 1.0 80.1 ± 2.8 205.7 ± 1.1

a
EC: Electrical conductivity.
b
TOM: Total organic matter. 4000 3600 3200 2800 2400 2000 1600 1200 800
c
TOC: Total organic carbon. Wave number cm-1
d
CECE: Effective cation exchange capacity.
e
HOC: Hydrosoluble organic carbon. PB = pine bark, SM = spent mushroom Fig. 1. FT-IR spectra of the composts: PB = pine bark, SM = spent mushroom waste,
waste, and BS = pruning waste + biosolids. and BS = pruning waste + biosolids.
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5440 Y. Tapia et al. / Bioresource Technology 101 (2010) 5437–5443

groups containing S are stronger than those bound to O or N. Con- The aliphatic/O-alkyl ratios (an indicator of the decomposition
sequently, in soils rich in organic matter, the dominant species of of organic matter) of the SM and BS were higher than that of the
Cd is formed with R–SH groups (Karlsson et al., 2007). It is there- PB, and negatively correlated with the C/N ratio, as reported by
fore likely that the high S content, especially in SM (Table 1), Tang et al. (2006) for other composted materials.
encouraged the formation of these complexes.
3.4. Cd extraction
13
3.3. CP-MAS C NMR Diethylene triamine pentaacetic acid (DTPA) is capable of
extracting the Cd associated with the soluble and/or exchangeable
The results of the organic matter analysis by CP-MAS 13C NMR fractions, and even sometimes from organic matter (Walter et al.,
are shown in Table 2. All the composts showed a strong signal in 2002). For the 200 mg Cd kg 1 treatments, 168.5 ± 5.4 mg Cd kg 1
the O-alkyl region, attributable above all to cellulose and hemicel- (91% respect of total Cd extracted with aqua regia) of the Cd was
lulose (Rowell et al., 2001). O-alkyl groups are usually biodegraded extracted by DTPA-CaCl2 from the PB, 131.0 ± 9.3 mg Cd kg 1
during composting, with the production of aliphatic, aromatic and (62%) from the SM, and 123.7 ± 4.4 mg Cd kg 1 (61%) from the BS.
carboxylic groups (Tang et al., 2006; Spaccini and Piccolo, 2008). These results indicate that Cd is highly available in PB under these
The organic matter of PB therefore undergoes less change than that conditions.
of SM or BS.
The SM and BS showed the percentage of total carbon repre-
3.5. Cd distribution
sented by aliphatic groups to be 15.9–29.0%, as reported by Zmor-
a-Nahum et al. (2007) in composts of different origin (manure,
The values of Cd distribution obtained by sequential extraction
wood, municipal waste and spent mushroom compost). The large
are expressed in mg kg 1 for PB, SM and BS with control and 200
signal in the aliphatic region may be due to fatty acids and a great-
Cd treatments (Table 3). The percentage of recovery is within the
er presence of humic acids, with aliphatic structures (Stevenson,
range obtained by other authors with similar procedures (Alonso
1994; Senesi et al., 2007), or the presence of recalcitrant hydropho-
et al., 2002).
bic components related to cutin and suberin and the presence of
In PB, control and 200 Cd treatments, the Cd concentration was
soil organic matter (Spaccini and Piccolo, 2008).
significantly higher (p 6 0.05) in soluble fraction (FI) with 0.28 and
The SM and BS had three times the carboxyl group content of
84.7 mg kg 1, respectively. Unlike, in SM, control and 200 Cd treat-
PB. An increasing presence of carboxylic groups is directly related
ments, where Cd concentration was significantly higher in organic
to an increase in the cation exchange capacity (Butler et al.,
fraction (FIV) with 0.33 and 64.7 mg kg 1, respectively. In BS, con-
2001). The greater presence of carboxyl groups in SM and BS, and
trol treatment, the Cd concentration was significantly higher in the
their pH, therefore explains their greater cation exchange capaci-
fraction associated with carbonates (FII), with 0.87 mg kg 1,
ties compared to PB (see Alloway, 1995) (Tables 1 and 2). SM
whereas that in 200 Cd treatment, the Cd concentration was signif-
and BS are therefore most likely to induce the formation of heavy
icantly higher in organic fraction, with 57.4 mg kg 1. These results
metal complexes.
indicates that the organic matter has important role for to form
complexing with Cd in SM and BS, followed by the fraction associ-
Table 2 ated with Fe and Mn oxides (FIII).
Relative areas (percentage of total area) of the chemical shift (d) regions in 13C cross- The values of Cd distribution expressed in percentage are
polarization and magic angle spinning nuclear magnetic resonance (CP-MAS NMR) shown in Fig. 2. The Cd distribution was similar in the control
spectra.
and 200 Cd-treated SM, while for the 200 Cd-treated PB and BS,
Chemicalshift (ppm) Type of C bond PB SM BS compared to the controls, Cd decreased in the FII and increased
% total area in the FIII and FIV fractions. In 200 Cd treatments, the PB showed
0 < d 6 45 Alkyl (aliphatic) 7.2 29.4 21.5 a high Cd percentage (47%) in the soluble fraction, while in the
45 < d 6 60 N-alkyl 4.5 5.3 7.8 SM it was 15% and in the BS 20%. In the organic fraction, the per-
60 < d 6 93 O-alkyl 48.3 34.1 37.9
centage Cd was 8% in PB, and 37% and 35% in the SM and BS,
93 < d 6 110 Di-O-alkyl 12.9 11.7 11.5
110 < d 6 140 Aromatic 14.2 6.7 6.7 respectively.
140 < d 6 160 Phenolic 9.5 4.5 7.1 These results may be attributable to differences in pH and the
160 < d 6 190 Carboxyl 2.1 6.7 6.7 type and amounts of organic matter. In the PB, the greater presence
190 < d 6 220 Amide-ketonic 1.3 1.6 0.7
of aromatic and phenolic compounds indicated by the NMR analy-
Aliphatic/O-alkyl 0.1 0.9 0.6
sis (probably part of the DOC), and the lower pH, may have favored
PB = pine bark, SM = spent mushroom waste and BS = pruning waste + biosolids. the formation of soluble complexes with Cd, preventing the

Table 3
1 1
Sequential extraction (Tessier) of Cd (mg kg ) from the control and 200 mg Cd kg -treated composts. (Values are means ± standard deviations, n = 4.)

Treatments FI FII FIII FIV FV Sum of fractions % Recoverya

1
Cd (mg kg )
PB Control 0.28 ± 0.01a 0.26 ± 0.01b <D.L.b <D.L. <D.L. 0.54 120.0
200 Cd 84.7 ± 1.7a 34.2 ± 0.3c 37.7 ± 1.7b 14.6 ± 0.9d 7.4 ± 1.0e 178.6 96.6
SM Control 0.14 ± 0.01c 0.15 ± 0.01c 0.25 ± 0.01b 0.33 ± 0.01a <D.L. 0.87 98.8
200 Cd 27.0 ± 0.5c 27.9 ± 1.3c 48.2 ± 2.1b 64.7 ± 2.3a 6.4 ± 0.6d 174.2 82.2
BS Control 0.41 ± 0.1b 0.87 ± 0.1a 0.18 ± 0.1c <D.L. 0.11 ± 0.1d 1.57 96.3
200 Cd 33.0 ± 1.3c 26.6 ± 1.4d 44.8 ± 2.5b 57.4 ± 2.1a 2.7 ± 0.4e 164.5 81.6

PB = pine bark, SM = spent mushroom waste and BS = pruning waste + biosolids.

a
Percentage of total Cd extracted with aqua regia.
b
D.L: detection limit. Different letters, in rows, indicate significant differences among fractions according to Duncan test p 6 0.05.
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Y. Tapia et al. / Bioresource Technology 101 (2010) 5437–5443 5441

(a) Control humification than did the PB; they may therefore better immobi-
PB lize Cd. The formation of stable complexes between Cd and organic
100
SM matter in materials that contain composted biosolids has been re-
80 BS ported by other authors (Illera et al., 2000; Alonso et al., 2002; Bo-
60 lan et al., 2003). The effect of high pH SM on Cd immobilization has
% Cd

40 also been reported (Shuman et al., 2002).

20

0 3.6. Leaching Cd
FI FII FIII FIV FV
The concentration of Cd in the leachates from the control, 80
(b) 200 Cd Cd-treated and 200 Cd-treated PB, SM and BS, during the first 7
PB
100 days of irrigation with distilled water is presented in Fig. 3. The
SM
Cd concentrations in the control PB, SM and BS were below the
80 BS
detection limit. In the 80 Cd-treated and 200 Cd-treated PB, the
60 highest concentrations of Cd were achieved on the first day of irri-
% Cd

40 gation with 0.7 mg L 1 and 2.1 mg L 1, respectively. The SM and BS

showed the highest concentration of Cd in their leachates on the
20
third day of irrigation (0.2 mg L 1 and 0.5 mg L 1 for 80 Cd-treated
0 and 200 Cd-treated SM, respectively, and 0.1 mg L 1 and
FI FII FIII FIV FV 0.2 mg L 1 for the corresponding BS treatments). These results
agree with those obtained in the sequential extraction which
Fig. 2. Sequential extraction of Cd (%) in the (a) control and (b) 200 Cd-treated
showed greater concentrations of Cd in the PB soluble fraction (Ta-
(contaminated with 200 mg Cd kg 1) composts. PB = pine bark, SM = spent mush-
room waste, and BS = pruning waste + biosolids.
ble 3). Although BS and SM have a higher chloride concentration
than PB, leading to the formation of soluble Cd complexes (Chris-
tensen and Huang, 1999; Adriano et al., 2004), as well as a higher
adsorption of the metal by the solid phase. The SM and BS, in con- concentration of hydrosoluble organic carbon (Table 1) (which can
trast, showed a higher pH and a greater degree of organic matter also induce the formation of soluble Cd complexes [Antoniadis and
Alloway, 2002]), their higher pH renders them more efficient
Control 80 Cd 200 Cd immobilizers of Cd. After the fifth day, no Cd was detectable in
the leachates in any of the columns. The average pH of the leachate
(a) PB was 4.8 ± 0.3, 8.1 ± 0.8 and 7.3 ± 0.5 for the PB, SM and BS, respec-
2.5 tively, over the first 7 days of irrigation.
Cd leaching (mg L )
-1

The total Cd leached from the PB, SM and BS at the end of the
2.0
assay is shown in Table 4. The Cd concentration in leachates was
1.5 significantly higher (p 6 0.05) in PB for both treatments 80 and
1.0 200 Cd, with 2.96 and 8.01 mg Cd kg 1, respectively, whereas that
0.5 the lowest concentration was in BS with 0.16 and 0.41 mg Cd kg 1,
respectively. The results expressed in percentages indicate that Cd
0.0
1 2 3 4 5 6 7 leached in 80 and 200 Cd treatments were similar. The BS showed
the lowest percentage of leaching (0.2%) (PB 4.0%, SM 0.7%).
(b) SM These results may be attributable to both a higher degree of
humification of organic matter and a higher content of inorganic
Cd leaching (mg L )

1.0
-1

0.8
components, especially Fe, in the BS (Table 1). Several authors have
reported a predominant role of Fe and Mn oxides in the retention
0.6 and reduced mobility of Cd in biosolids (Li et al., 2001; Hettiarach-
0.4 chi et al., 2003; Merrington and Smernik, 2004). Fe and Mn in bios-
0.2 olids control the availability of Cd (Bolan et al., 2003) since their
oxides adsorb Cd in an almost irreversible manner (Hettiarachchi
0.0
et al., 2003). It is therefore likely that Cd was strongly adsorbed
1 2 3 4 5 6 7

(c) BS
Table 4
Cd leaching (mg L )

0.5
-1

Total Cd leachate from the 80- (80 Cd) and 200 mg Cd kg 1-treated (200 Cd) composts
0.4 after of 30 days of irrigation with distilled water. (Values are means ± standard
deviations, n = 4.)
0.3
Treatments Total Cd leachate % Leachinga
0.2 mg column 1 mg kg 1

0.1 PB 0.33 ± 0.03 2.96 ± 0.35a 3.7

0.0 80 Cd SM 0.07 ± 0.003 0.45 ± 0.02b 0.6
1 2 3 4 5 6 7 BS 0.04 ± 0.001 0.16 ± 0.01c 0.2
Time (day) PB 0.88 ± 0.05 8.01 ± 0.48a 4.0
200 Cd SM 0.21 ± 0.004 1.45 ± 0.03b 0.7
Fig. 3. Cd concentration (mg L 1) in compost leachates: (a) PB (pine bark), (b) SM BS 0.10 ± 0.01 0.41 ± 0.03c 0.2
(spent mushroom waste) and BS (pruning waste + biosolids). Composts were
a
treated with 0 mg Cd kg 1 (control), 80 mg Cd kg 1 (80 Cd) or 200 mg Cd kg 1 (200 Percentage of total extracted with aqua regia. Different letters, in columns,
Cd). Irrigation was performed using distilled water. (Lines in bars correspond to indicate significant differences among Cd leachate from composts, according to
standard deviation, n = 4.) Duncan test p 6 0.05.
 Author's personal copy
5442 Y. Tapia et al. / Bioresource Technology 101 (2010) 5437–5443
by the Fe and Mn oxides of the BS, preventing its leaching. Inor-
ganic phosphates and aluminum also play a role in metal retention
(Adriano et al., 2004). Clemente et al. (2006) found that, when or-
ganic amendments were added to the soil, phosphorus and inor-
ganic salts contributed more to changes in the fractionation of
heavy metals than the nature and degree of humification of the or-
ganic matter. However, the individual effects of organic and min-
eral colloids in the retention of Cd are usually not easily
ascertained since humified organic matter is intimately bound to
mineral colloids in most soils. Thus, humified organic matter and
mineral colloids generally function as a unit more than as separate
entities (Christensen and Huang, 1999). The immobilization of
metals by the organic amendments may be a consequence of sev-
eral mechanisms such as adsorption to mineral surfaces, the for-
mation of stable complexes with organic ligands, precipitation or
ion exchange, and depends on factors such as the pH, redox poten-
tial, and soil cation exchange capacity and only rarely is a single
mechanism the cause of immobilization of metals (Kumpiene
et al., 2008).
4. Conclusions
Spent mushroom (SM) and pruning waste + biosolids (BS) com-
posts showed a greater capacity to immobilize Cd than in pine bark
compost (PB), due to higher pH, greater degree of humification of
organic matter and higher cation exchange capacity. SM and BS
have a higher percentage of aliphatic and carboxyl groups that
PB. The Cd added was mainly associated with the organic fraction
in SM and BS while that in PB with the fraction more available. The
total Cd leached was lower in BS probably due to a higher content
of iron oxides.
Acknowledgments
This work was supported by the Ministry of Education and Sci-
ence of Spain (Project 2005-06258-C02-02/TECNO CTM) and the
Spanish International Cooperation Agency (AECI, scholarship MAE
2005-2007).
References
Adriano, D.C., Wenzel, W.W., Vangrosveld, J., Bolan, N.S., 2004. Role of assisted
natural remediation in environmental cleanup.. Geoderma 122, 121–142.
Alloway, B.J., 1995. Heavy Metals in Soils. Blackie Academic and Professional, UK.
Alonso, E., Callejón, M., Jimenez, J.C., Ternero, M., 2002. Heavy metal extractable
forms in sludge from wastewater treatment plant. Chemosphere 47, 765–775.
Ansorena, J., 1994. Sustratos. Propiedades y caracterización. Mundi-Prensa, Madrid.
Antoniadis, V., Alloway, B.J., 2002. The role of dissolved organic carbon in the
mobility of Cd, Ni and Zn in sewage sludge-amended soils. Environmental
Pollution 117, 515–521.
Antoniadis, V., Tsadilas, C.D., Ashworth, D.J., 2007. Monometal and competitive
adsorption of heavy metals by sewage sludge-amended soil. Chemosphere 68,
489–494.
Basta, N.T., Gradwohl, R., Snethen, K.L., Schroder, J.L., 2001. Chemical
immobilization of lead, zinc, and cadmium in smelter-contaminated soils
using biosólidos and rock phosphate. Journal of Environmental Quality 30,
1222–1230.
Benito, M., Masaguer, A., Moliner, A., De Antonio, R., 2006. Chemical and physical
properties of pruning waste compost and their seasonal variability. Bioresource
Technology 97, 2071–2076.
Bernal, M.P., Clemente, R., Vazquez, S., Walter, D.J., 2007. Aplicación de la
fitorremediación a los suelos contaminados por metales pesados en
Aznalcóllar. Ecosistemas 2007 (2), 68–82.
Bolan, N.S., Adriano, D.C., Duraisamy, P., Mani, A., 2003. Immobilization and
phytoavailability of cadmium in variable charge soils III. Effects of biosolids
compost addition. Plant and Soil 256, 231–241.
Butler, T.A., Sikora, L.J., Steinhilber, P.M., Douglass, L.W., 2001. Compost age and
sample storage effects on maturity indicators of biosólidos compost. Journal of
Environmental Quality 30, 2141–2148.
Cataldo, D.A., Harro, M., Schrader, L.E., Young, V.L., 1975. Rapid colorimetric
determination of nitrate plant tissue by nitration of salicylic acid.
Communications in Soil Science and Plant Analysis 6, 71–80.
Chen, Z.S., Lee, G.J., Liu, J.C., 2000. The effects of chemical remediation treatments on
the extractability and speciation of cadmium and lead in contaminated soils.
Chemosphere 41, 235–242.
Christensen, T.H., Huang, P.M., 1999. Solid phase cadmium and the reactions of
aqueous cadmium with soil surfaces. In: McLaughlin, M.J., Singh, B.R. (Eds.),
Cadmiun in Soil and Plants. Kluwer Academic Publishers, Netherlands, pp. 65–
91.
Clemente, R., Escolar, A., Bernal, P., 2006. Heavy metals fractionation and organic
matter mineralisation in contaminated calcareous soil amended with organic
materials. Bioresource Technology 97, 1894–1901.
Eymar, E., Martín-Rueda, I., Muñoz-Guerra, L.M., Esteban, E., Gárate, A., Lucena, J.J.,
Cadahía, C., 2002. Impacto de fertilizantes nitrogenados y practicas agrícola
sobre la calidad de las aguas. Estudio con columnas de suelos. En: La Gestión y
el Control del Agua frente a la Directiva Marco. Varios Editores. Madrid, pp.
211–217.
Halim, M., Conte, P., Piccolo, A., 2003. Potential availability of heavy metals to
phytoextraction from contaminated soils induced by exogenous humic
substances. Chemosphere 52, 265–275.
Hernández, D., Fernández, J.M., Plaza, C., Polo, A., 2007. Water-soluble organic
matter and biological activity of a degraded soil amended with pig slurry.
Science of the Total Environment 378, 101–103.
Hettiarachchi, G., Ryan, J., Chaney, R., La Fleur, C., 2003. Sorption and desorption of
cadmium by different fractions of biosolids-amended soils. Journal of
Environmental Quality 32, 1684–1693.
Huang, G.F., Wu, Q.T., Wong, J.W.C., Nagar, B.B., 2006. Transformation of organic
matter during co-composting of pig manure with sawdust. Bioresource
Technology 97, 1834–1842.
Illera, V., Walter, I., Cala, V., 2000. Short-term effects of biosolids and municipal
solid waste applications on heavy metals distribution in a degraded soil
under a semi-arid environment. The Science of the Total Environment 255,
29–44.
Karlsson, T., Elgh-Dalgren, K., Björn, E., Skyllberg, U., 2007. Complexation of
cadmium to sulphur and oxygen functional groups in an organic soil.
Geochimica et Cosmochimica Acta 71, 604–614.
Kiikkila, O., Perkiömäki, J., Barnette, M., Derome, J., Pennanen, T., Tulisalo, E., Fritze,
H., 2001. In situ bioremediation through mulching of soil polluted by a copper-
nickel smelter. Journal of Environmental Quality 30, 1134–1143.
Kumpiene, J., Lagerkvist, A., Maurice, C., 2008. Stabilization of As, Cr, Cu, Pb and Zn
in soil amendments. A review. Waste Management 28, 215–225.
Lee, T., Lai, H., Chen, Z., 2004. Effect of chemical amendments on the concentration
of cadmium and lead in long-term contaminated soil. Chemosphere 57, 1459–
1471.
Li, Z., Ryan, J., Chen, J., Al-Abed, S., 2001. Adsorption of cadmium on biosolids-
amended soils. Journal of Environmental Quality 30, 903–911.
McGrath, S.P., Cunliffe, C.H., 1985. A simplified method for the extraction of metals
Fe, Zn, Ni, Pb, Cr, Co, Mn from soils and sewage sludges. Journal of the Science of
Food and Agriculture 36, 794–798.
Merrington, G., Smernik, R.J., 2004. Cadmium sorption in biosolids amended
soils: results from a field trial. Science of the Total Environment 327, 239–
247.
Merrington, G., Oliver, I., Smernik, R.J., McLaughlin, M.J., 2003. The influence of
sewage sludge properties on sludge-borne metal availability. Advances in
Environmental Research 8, 21–36.
Murphy, J., Riley, J.P., 1962. A modified single solution method for determination of
phosphate in natural waters. Analytica Chimica Acta 27, 31–36.
RD 824/2005, 2005. Real Decreto sobre productos fertilizantes. Ministerio de la
Presidencia. España. Boletín Oficial del Estado (BOE) 171, pp. 25592–25669.
Roletto, E., Barberis, R., Consiglio, M., Jodice, R., 1985. Chemical parameters for
evaluating compost maturity. Biocycle 26, 46–47.
Rowell, D., Prescott, C., Preston, C.M., 2001. Decomposition and nitrogen
mineralization from biosolids and other organic materials: relationship with
initial chemistry. Journal of Environmental Quality 30, 1401–1410.
SAS Institute, 1988. SAS/STAT User’s Guide, Version 6.03. SAS Institute, Cary, NC
1088.
Senesi, N., Plaza, C., Brunetti, G., Polo, A., 2007. A comparative survey of recent
results on humic-like fractions in organic amendments and effects on native
soil humic substances. Soil Biology and Biochemistry 39, 1244–1262.
Shoval, S., Yariv, S., Michaelian, K.H., Boudeulle, M., Panczer, G., 1999. Hydroxyl-
stretching bands ‘A’ and ‘Z’ in Raman and infrared spectra of kaolinites. Clay
Minerals 34, 551–563.
Shuman, L.M., Dudka, S., Das, K., 2002. Cadmium forms and plant availability in
compost-amended soil. Communications in Soil Science and Plant Analysis 33,
737–748.
Silverstein, R.M., Bassler, G.C., Morrill, T.C., 1981. Spectrometric Identification of
Organic Compounds, fourth ed. John Wiley and Sons, New York.
Spaccini, R., Piccolo, A., 2008. Spectroscopic characterization of compost at different
maturity stages. Clean 36, 152–157.
Stacey, S., Merrington, G., McLaughlin, M.J., 2001. The effect of aging biosolids on
the availability of cadmium and zinc in soil. European Journal of Soil Science 52,
313–321.
Stevenson, F.J., 1994. Humus Chemistry. John Wiley and Sons Inc., NY.
Tang, J., Maie, N., Tada, Y., Katayuna, A., 2006. Characterization of maturing process
of cattle manure compost. Process Biochemistry 41, 380–389.
Tessier, A., Campbell, P.G.C., Bisson, M., 1979. Sequential extraction procedure
for the speciation of particulate trace metals. Analytical Chemistry 51, 844–
851.
 Author's personal copy
Y. Tapia et al. / Bioresource Technology 101 (2010) 5437–5443
Vaca-Paulín, R., Esteller-Alberich, M.V., Lugo-de la Fuente, J., Zavaleta-Mancera,
H.A., 2006. Effect of sewage sludge or compost on the sorption and distribution
of copper and cadmium in soil. Waste Management 26, 71–78.
van Herwijnen, R., Laverye, T., Poole, J., Hodson, M., Hutchings, T., 2007. The effect of
organic materials on the mobility and toxicity of metals in contaminated soils.
Applied Geochemistry 22, 2422–2434.
Walker, D., Clemente, R., Roig, A., Bernal, M.P., 2003. The effects of soil amendments
on heavy metal bioavailability in two contaminated Mediterranean soil.
Environmental Pollution 122, 303–312.
5443
Walkley, A.L., Black, A., 1947. A rapid determination of soil organic matter. Journal
of Agriculture Science 25, 563–568.
Walter, I., Martínez, F., Alonso, L., de Gracia, J., Cuevas, G., 2002. Extractable soil
heavy metals following the cessation of biosolids application to agricultural
soil. Environmental Pollution 117, 315–321.
Zmora-Nahum, S., Hadar, Y., Chen, Y., 2007. Physico-chemical properties of
commercial compost varying in their source materials and country of origin.
Soil Biology and Biochemistry 39, 1263–1276.