Journal of Environmental Management 250 (2019) 109525

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Journal of Environmental Management

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Research article

Comparison of the effects of different maturity composts on soil nutrient, T

plant growth and heavy metal mobility in the contaminated soil
Ling Liua, Siqi Wangb, Xiaoping Guoc,d, Hongjie Wanga,∗
a
Xiong'an Institute of Eco-Environment, Hebei University, Baoding, 071002, Hebei Province, PR China
b
College of Environmental Science and Engineering, Beijing Forestry University, Beijing, 100083, China
c
College of Soil and Water Conservation, Beijing Forestry University, Beijing, 100083, PR China
d
Key Lab of Soil and Water Conservation and Desertification Combating, Ministry of Education, Beijing Forestry University, Beijing, 100083, PR China

A R T I C LE I N FO A B S T R A C T

Keywords: Numerous studies on the remediation of metal-contaminated soil by compost focus on the remediation efficiency
Compost maturity of compost, however, they have not delved into the issue of nutrients and metal speciation. In this study, the
Nutrients application of municipal solid wastes primary compost (MSW-C), secondary compost (MSW-SC) and the aging
Heavy metal compost (MSW-AC) has been conducted in heavy metal contaminated soil remediation. Eight different treat-
Soil remediation
ments were carried out to compare the effect of three different maturity composts and their addition ratio (i.e. 0,
Sedum aizoon
25%, 50%) on the changes of physical properties, nutrient content and metal morphology distribution of soil.
The enhancement of Sedum aizoon growth was also compared. The results showed that the treatments applied
with composts increased the nutrient, organic carbon and the cation exchange capacity. In overall, the most
effective treatment method was to use MSW-AC to improve soil physicochemical properties and reduce the
heavy metals immobilization, and the addition of 25% MSW-AC showed significant promotion on plant biomass
accumulation and root growth. The ability of compost to improve the conditions of the contaminated soil and
increase the plant stress resistance was demonstrated by analyzing the root membrane lipid peroxidation, which
was lower in the soil treatments with compost, especially with MSW-AC. Based on the compost maturity indexes,
soil properties, and efficiency of metal activity reduction, the treatment of 25% MSW-AC is suggested for effi-
cient soil remediation.

1. Introduction abundant in macro- and micronutrients (Kulikowska et al., 2015; Zhao

et al., 2013). The utilization of compost has a positive effect on soil
Heavy metal contaminated soil has become a matter of environ- biological and physicochemical properties (Weber et al., 2014; Głąb
mental concern all around the world (Karer et al., 2015). The physical et al., 2018), which meets the safe and quality standards. Besides,
and nutritional structure of most soil contaminated by heavy metals, compost can be used as a fertilizer during the cultivation of consump-
such as abandoned mines, has been destroyed, requiring potential so- tion plants species. Liu et al. (2018) reported that the application of
lution for ecological restoration (Carbonell et al., 2011; Jiang et al., compost to subsoil enhanced the nutrient cycling processes and im-
2016). Methods such as chemical extraction or electrochemical re- proved sugarcane growth. Winery-distillery composts were applied as
mediation need high costs and can cause soil structure destruction, substituted growing media for the cultivation of thyme, showing sig-
thus, the application of natural attenuation measures has been more nificant influence on the production of essential oils from thyme plants
adopted in the soil remediation (Smolinska, 2015; Rajaie et al., 2006). (Bolechowski et al., 2015).
Concerning the application of chelate-induced techniques can increase With the rapid development of urbanization, a large quantity of
the risk of heavy metal leaching from soil to groundwater, some studies municipal solid waste (MSW) is generated each year. Composting has
have investigated the economically reasonable remediation for in- become an effective management of the MSW for recycling and con-
creasing the efficiency without causing metal leaching (Karami et al., verting organic waste into a useful product (Papafilippaki et al., 2015).
2011; Fang et al., 2016). Compost is one of the substances with that However, the application of MSW compost can lead to the accumula-
potential, which characterizes by high organic matter content as well as tion of heavy metals in soils and plants, and the entrance of metals into

∗
Corresponding author. No. 180 Wusi east road, Baoding, 071002, Hebei province, China.
E-mail address: [email protected] (H. Wang).

https://doi.org/10.1016/j.jenvman.2019.109525
Received 2 March 2019; Received in revised form 15 August 2019; Accepted 2 September 2019
Available online 07 September 2019
0301-4797/ © 2019 Elsevier Ltd. All rights reserved.
L. Liu, et al. Journal of Environmental Management 250 (2019) 109525

the food chain or groundwater will threaten human health and the with the dosage of 0.03 g kg−1. The secondary compost samples were
environment (Fagnano et al., 2011; Papafilippaki et al., 2015). The stacked and aged for 1 year after composting for 45 days, and then
contents of heavy metals in the soil environment with the application of adopted as the raw materials for MSW-AC. The compost methods and
MSW compost are determined by factors such as the compost quality, conditions were the same as that of MSW-SC.
soil types and plant species (Zhao et al., 2013; Rizzo et al., 2015). Al-
though the MSW compost could improve soil remediation, there are still 2.2. Soil and plant material
concerns for potential risk of toxic metals to soils due to the insufficient
classification of municipal waste (Fagnano et al., 2011; Lakhdar et al., The soil was sampled from the deep layer of mountainous area of
2012). Therefore, it is vital to apply MSW to vegetation restoration in Beijing (no heavy metal pollution). The sampled soil was air dried and
degraded soils far from the food chain. In order to fully and safely use removed impurities, then screened by 5 mm sieve and mixed with
compost resources, the migration and transformation of metal elements heavy metal reagent in 50 L container. For the variant of experiment,
in compost should be explored. CuCl2·2H2O, NiCl2·6H2O, CdCl2·2.5H2O and ZnCl2 was add into the soil
Most of the studies on the remediation of contaminated soils have as metal pollutants, in order to make the concentration of Cu2+, Zn2+,
focused on the problems caused by pollutants, seldom addressing the Cd2+ and Ni2+ in the growing medium reached 600, 600, 30 and
issues of soil nutrients and vegetation growth. However, the restoration 200 mg kg−1 (dry weight), respectively (Table S1). After blending the
and sustainable use of degraded soils requires permanent vegetation soil and reagents, the mixed soil aged for 25 days and stabilized for
construction to prevent soil erosion and restore soil ecosystem func- planting.
tions. The toxicity of heavy metals to plants is influenced by their Sedum aizoon was purchased from flower market and cut to the
species presented in soil, which is determined by many soil factors in- same height and quantity of stem and leaf for cuttage. The plant ma-
cluding soil texture, cation exchange capacity, pH and organic matter terial used for planting experiments was originated from Sedum aizoon
contents, etc (Mbarki et al., 2008). Several studies have demonstrated cuttage with consistent growth conditions after 3 weeks of cutting.
that the application of different composts during soil reclamation was
effective in reducing the bioavailability of metals (Silvetti et al., 2017; 2.3. Experimental design
Moreno-Jiménez et al., 2013). Pardo et al. (2011) demonstrated that
the application of manure composts enhanced Zn and Pb contaminated The planting experiment was carried out with eight different
soil remediation and changed the speciation of metals. The changes in growing media. The percent contributions of Zn, Cu, Ni, and Cd in the
the Cd speciation had been explored in the compost-amended soil by total metal contents of three composts are presented in Fig. S1. The
Rajaie et al. (2006). eight treatments were illustrated as follows:
In addition, there are few researches concerning the correlation
between maturity of composts and migration of heavy metals. Compost CK1: original soil
is generally rich in humus, with strong sorption capacity (Silvetti et al., CK2: heavy metal contaminated soil
2017; Liu et al., 2018). The composts with different maturity may cause T1: 25% MSW-C + 75% contaminated soil
significant effects on the humus composition and change their passi- T2: 25% MSW-SC + 75% contaminated soil
vation efficiency on heavy metals. Al-Mashaqbeh and Mclaughlan T3: 25% MSW-AC + 75% contaminated soil
(2014) found that the aging composts had a significant effect on zinc T4: 50% MSW-C + 50% contaminated soil
adsorption. Another study suggested that secondary fermentation could T5: 50% MSW-SC + 50% contaminated soil
improve compost maturity with the humus structure more complex and T6: 50% MSW-AC + 50% contaminated soil
stable (Spaccini and Piccolo, 2009). However, the effects of different
maturity of MSW compost on the remediation of heavy metal con- Sedum aizoon was grown in the greenhouse under controlled tem-
taminated soil have not been widely studied. perature (20 °C) in Beijing Forestry Technology co. LTD (Beijing,
Therefore, the goals of this study were 1) to characterize MSW-C China). Sedum aizoon cuttages (4.5 cm tall) were planted in pots. Each
physicochemical properties during different maturity compost process, treatment was in sextuplicate. The substrate moisture was maintained
exploring the feasibility of compost as a substituted substrate for soil at 50%. Moreover, there was no additional fertilization for all treat-
and peat; 2) to evaluate the potential of using composts as organic ments. On the 105th day of the planting experiment, aboveground and
materials in metal immobilization, afforestation and greening; 3) to underground part of all the plant materials were harvested separately.
assess the Sedum aizoon growth characterization and plant stress re- Part of the plants for each treatment were used for determining the
sistance when applying different maturity composts during the re- fresh weight and phytophysiological index; and the left were dried at
mediation of metal contaminated soils. The fulfillment of the above 60 °C in an oven for 72 h, for the determination of dry weight and
objectives will help to determine the appropriate maturity of MSW chemical analysis.
compost for the growth of Sedum aizoon, and obtain the effects of MSW
compost on soil improvement, providing verification for the application 2.4. Soil, composts and plant analysis
effect of composts (e.g. increase of heavy metals accumulation and
bioavailability). Soil, compost and planting substrate samples were air-dried at room
temperature. Soil and substrate density, water content, and porosity are
2. Material and methods determined by cutter ring method. The pH and electric conductivity
(EC) value of composts, soil and substrates were measured by water
2.1. Composting experiment soluble extract and suspension (1:2.5, W/V). The organic carbon (OC),
total nitrogen (TN), total phosphorus (TP), available phosphorus (AP),
The soil remediation and Sedum aizoon growth media for cultivation available potassium (AK), cation exchange capacity (CEC), humic acid
were elaborated using MSW compost (MSW-C), MSW secondary com- (HA) and fulvic acid (FA) were determined as described by Liu et al.
post (MSW-SC) and MSW aging compost (MSW-AC). MSW-C was ob- (2018). Total content of heavy metals was determined by ICP-OES
tained from the sanitary waste composting site in Beijing. The MSW-SC (Prodigy XP, LEEMAN LABS INC. USA). The modified BCR (Community
adopted the strip-type composting method, with the raw material of Bureau of Reference) sequential extraction procedure was used to de-
MSW-C. The composting volume was set to 1.5 m3, the water content of termine the heavy metal speciation (Bacon and Davidson, 2008).
secondary compost was controlled at about 60%. Materials were turned Sedum aizoon growth rates were determined by measuring the
over every 5 days. The microbial inoculum was added in the compost height weekly. The final plant biomass was determined by assessment

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L. Liu, et al. Journal of Environmental Management 250 (2019) 109525

of the fresh and dry mass after 3 months’ growth. Immediately after stable (Avramidou et al., 2013; Moldes et al., 2007). The humic acid
harvest, half of the plants were washed with distilled water, and the (HA) content of the aging compost was 27.3 ± 6.5 mg g−1, and the
fresh weight of the plant tissues were both determined. The three-di- humic/fulvic acid (HA/FA) ratio increased as the parameter for de-
mension (3D) root scanner 3DLS500 was conducted for the root length, scribing the humus substrates transformation and compost maturity
volume and surface area measurement. Dried and crushed plant tissues (Dev and Antil, 2011). In addition, the MSW-AC showed a higher CEC,
were digested using microwave oven with concentrated HNO3 indicating the generation of negatively charged surface groups during
(Papafilippaki et al., 2015). The concentrations of nutrients and heavy further maturity of the compost. And the GI values of MSW-SC and
metals were determined by ICP-OES. Malondialdehyde (MDA) content MSW-AC were 89% and 95%, respectively, for disappearance of phy-
of root was measured following the method of Heath and Pacher totoxicity (Awasthi et al., 2014), while the GI of MSW-C was much
(1968). The root fresh material was further ground with chilled tri- lower than 80%.
chloroacetic acid solution and quartz sand. Then, 2 mL supernatant was The heavy metal contents of composts were lower than the limits of
taken after centrifugation and added with thiobarbituric acid solution. organic-inorganic compound fertilizers standard in China (AQSIQ,
Boiling water bath for 15 min, the supernatants were determined for OD 2002). The contents of Zn and Cu in the MSW-SC and MSW-AC were
(optical density) values at 450, 532 and 600 nm, respectively. higher, due to further decomposition and reduction of compost material
during the composting process (Valentin et al., 1997). Table 2 showed
2.5. Statistical analysis metal contents in MSW-C determined in several other studies, and the
average contents in this study were at a moderate level. Comparing
Statistical analyses were performed with SPSS 18. Analysis of var- with the legislative values, composts analyzed herein could be used in
iance (ANOVA) was used to evaluate the effects of different compost greening application. This favors the composts’ utilization as reactive
treatments on soil properties, heavy metal immobilization and plant materials in natural environments, but the risk of metal accumulation in
growth. Statistically significant level was set at p < 0.05 using Tukey's the environment and the effect on biota should be taken into full ac-
test. The canonical correspondence analysis was performed using count (Faverial et al., 2016; Lima et al., 2018).
Canoco 4.5 software. A lower percentage of exchangeable Cu was found in MSW-AC
The MDA concentration was calculated according to the following (5.4%) than that in MSW-SC (7.8%) and MSW-C (12.4%), and the re-
formula: ducible fraction in MSW-AC also showed a decrease by 6.3% and 8.2%
compared with that in the MSW-SC and MSW-C. Similar to Cu, rela-
MDA concentration (μmol L−1) = 6.45×(D532 − D600) − 0.56×D450.
tively lower exchangeable fraction of Zn and Ni was found in the aging
where D532, D600 and D450 represent the optical density values at the compost. Cd was mainly in the residual fraction in all the compost
wavelengths of 532, 600 and 450 nm, respectively. materials. The decrease of exchangeable and reducible fractions could
be attributed to the strong chemical binding ability of metal ions with
3. Results and discussion more stable organic matters in secondary fermentation (Haroun et al.,
2007; Singh and Kalamdhad, 2012). Furthermore, the bioavailable
3.1. Composts properties fractions of total metal content were low in composts, suggesting that
heavy metals absorbed by plants was low (Venkateswaran et al., 2007).
The pH values of MSW-AC were neutral, and MSW-SC showed
moderately alkaline (Table 1). Higher EC value of MSW-C suggested 3.2. Soil material properties
higher soluble salts content, which had potential effects on biological
activity, plant growth and soil salinization (Avramidou et al., 2013; The composts showed significant effect on soil properties and nu-
Moldes et al., 2007). There were no remarkable differences among the trient availability in different treatments. The physicochemical char-
organic carbon (OC) content for three composts. However, the con- acterization of substrates remediated with composts are shown in
centrations of nutrient elements including total phosphorus (TP) and Fig. 1. The decrease of soil bulk density was positively correlated with
available phosphorus (AP) in MSW-AC were significantly higher than the amount of added compost. As studies suggested, the smaller the
those in MSW-C and MSW-SC. Total nitrogen (TN) and available po- bulk density, the more porous and better the structure of soil (Li et al.,
tassium (AK) in MSW-AC and MSW-SC were higher than those in MSW- 2017). Substrates with 50% compost had significantly higher soil sa-
C. Moreover, the C/N ratio of the MSW-SC and MSW-AC were 11 and turated water content and field capacity. The increase of composts
10, respectively, indicating that both of composts were mature and amount led to the decrease of the solid material volume per unit soil

Table 1
Properties of the municipal solid waste composts.
Property Units MSW-C MSW-SC MSW-AC

pH (1:25) – 7.8 ± 0.3ab

8.2 ± 0.4b
7.1 ± 0.4a
EC mS·cm−1 7.0 ± 0.7c 5.15 ± 0.5 b 3.7 ± 0.8a
Organic carbon (OC) g·kg−1 189 ± 22 218 ± 31 209 ± 19
Total nitrogen (TN) % 1.2 ± 0.2a 1.9 ± 0.4 b 2.1 ± 0.5 b
Total phosphorus (TP) g·kg−1 0.27 ± 0.03a 0.42 ± 0.09a 0.61 ± 0.11 b
Available potassium (AK) mg·kg−1 4551 ± 167a 5362 ± 209 b 5153 ± 416 b
Available phosphorus (AP) mg·kg−1 61.3 ± 9.6 b 42.8 ± 7.7a 78.5 ± 9.0c
C/N ratio – 16 ± 2.0 b 11 ± 2.4 ab 10 ± 1.7a
BET m2·g−1 0.85 1.39 1.41
Pore volume cm3·g−1 0.005 0.015 0.011
Humic acid (HA) g·kg−1 13.2 ± 1.8a 25.8 ± 2.2 b 27.3 ± 6.5 b
Fulvic acid (FA) g·kg−1 34.9 ± 2.7 b 23.1 ± 2.1a 20.8 ± 3.4a
H/F – 0.38 ± 0.09a 1.12 ± 0.1 b 1.31 ± 0.4 b
CEC cmol(+)·kg−1 21.1 ± 2.4a 24.4 ± 4.1a 36.0 ± 5.2 b
Germination index (GI) % 64 ± 9 b 89 ± 13 ab 95 ± 11a

Notes: Data are reported as Mean ± SD with n = 3. a, b and c indicate multiple comparisons of p < 0.05 at each level. The same letter means no significant
difference, while the different letter indicates a significant difference between different composts using ANOVA.

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L. Liu, et al. Journal of Environmental Management 250 (2019) 109525

Table 2
Concentration of various elements found in different organic composts.
Composts Cu (mg kg−1) Zn (mg kg−1) Cd (mg kg−1) Ni (mg kg−1) Reference

MSW-C 83 ± 23 339 ± 39 1.7 ± 0.8 30.1 ± 2.3 This study

MSW-SC 125 ± 29 363 ± 38 2.2 ± 0.9 34 ± 4.2
MSW-AC 139 ± 30 439 ± 52 2.1 ± 0.7 33 ± 3.5
MSW-C 12.80 132.80 1.30 1.60 Jacqueline et al. (2018)
MSW-C 39.2 ± 26.8 114.7 ± 4.7 < 0.01 9.84 ± 0.93 Alessandra et al. (2019)
MSW-C 329 ± 83 505 ± 216 ND 87.2 ± 19.2 Farrell & Jones. (2010)
MSW-C 133 523 2.9 40 Venegas et al. (2015)
M+SS-C 68.1 ± 1.8 663 ± 17 2.69 ± 0.33 – Gondek et al. (2018)
MSW-C 19.24 ± 1.74 30.52 ± 3.2 ND – Margherita et al. (2017)
MSW-C 147.2 170 2.1 23 Soobhany et al. (2015)

MSW-C: municipal solid waste compost; MSW-SC: MSW secondary compost; MSW-AC: MSW aging compost; M+SS-C: shredded maize straw with municipal sewage
sludge compost.

volume, and increased the corresponding volume of gas and liquid 50% compost addition treatments, from about 13.8 cmol(+) kg−1 in the
phase in soil, which improved the soil ventilation and permeability to a control up to 38 cmol(+) kg−1 in T5. As expected, OC and TN were
certain extent (Meng et al., 2017). Awasthi et al. (2016) showed that significantly increased by the composts application in all samples,
long-term application of compost with high organic matter content will especially in the 50% application rates of MSW-AC. Both addition ratios
promote the formation of soil aggregates and increase soil porosity. (25% and 50%) of compost significantly increased TP, AP and the AK
The pH of all substrates were alkaline (7.5–8.2) and there was no contents in all substrates.
significant difference between soil and composts. EC was significantly The effects of composts on soil OC, TN, TP and other nutrient in-
higher after addition of composts (1.51–2.41 mS cm−1), while that of dicators showed that the addition of MSW-AC improved the soil nu-
original soil was 0.3 mS cm−1. Also, the composts addition significantly trients most significantly. As mixture rich in humus and TN, the addi-
increased CEC in all soil samples. The increase of CEC was greater in the tion of compost can not only improve the soil microenvironment,

Fig. 1. Effects of the compost addition factors on physical and chemical properties in contaminated soils. Bar height denotes the average value per level of each
factor.

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L. Liu, et al. Journal of Environmental Management 250 (2019) 109525

Table 3 (Carbonell et al., 2011; Zhang et al., 2006; Baldantoni et al., 2010). In
Metal concentrations (mg kg−1) in the control and the composts -remediated this research, the exchangeable fraction constitutes 3–7% of total Cu,
soils at stable stage of experiment (before planting). 3–7.7% of total Zn, 1–4% of total Ni and less than 1% of total Cd in the
Treatments Heavy metal content (mg kg−1) MSW compost-remediated soil, respectively. According to the results of
different patterns for metals availability, the low application rate of
Cu Zn Cd Ni MSW compost in soil showed no change in available Cu (Valentin et al.,
1997). However, Jordao et al. (2006) summarized the opposite con-
CK1 39 ± 5a 75 ± 7a 0.17 ± 0.07a 26 ± 4a
CK2 422 ± 30d 623 ± 31f 28 ± 5c 278 ± 18e clusion that available Cu concentration in soil was significantly related
T1 347 ± 16c 501 ± 16c 17 ± 4 b 200 ± 14 cd to the compost addition ratio. In this study, the exchangeable Ni in the
T2 346 ± 17c 538 ± 24 de 18 ± 2 b 202 ± 16 cd compost-remediated soils was lower than that in contaminated soil, but
T3 332 ± 22 bc 466 ± 19 b 15 ± 3 b 220 ± 20d
higher than that in the original soil, which could be interpreted as in-
T4 342 ± 19c 451 ± 25 b 12 ± 2 b 183 ± 19 bc
T5 364 ± 26c 547 ± 27e 12 ± 2 b 179 ± 23 bc dicator of the potential Ni mobility and availability in soil (Hargreaves
T6 298 ± 21 b 519 ± 31 cd 11 ± 2 b 160 ± 17 b et al., 2008). However, Zhang et al. (2006) showed that Zn infiltrated
through the profile after the compost applied. The Cd content in the
compost-remediated soil was higher than that in the original soil and
optimize the soil structure, but also improve the soil nutrient content composts due to the higher Cd content in contaminated soil. The MSW
(Carbonell et al., 2011; Fagnano et al., 2011). There was a positive compost was observed different effects on metal concentration and
correlation between organic matter and TN content in soil nutrient metal speciation, the Cd and Cu concentrations have been reported an
remediation (Keuskamp et al., 2013). The degradation of protein and increasing trend when remediated by MSW compost, while the result
other organic substances made the compost rich in nitrogen content. On that no changes for Ni and Cd concentrations in MSW compost re-
the other hand, the addition of compost can increase the species and mediated soil was also obtained (Zhang et al., 2006). In present study,
quantity of microorganisms in the soil, improving the soil effective remediation affected the metal concentration and the exchangeable
nutrient content. Soil phosphorus availability and migration rate can fraction decreased comparing with the contaminated soil.
increase with the addition of MSW compost because of the increasing
competition between organic ligands and phosphates (Jin et al., 2016). 3.4. Plant growth and heavy metal uptake
Therefore, with the increase of compost application amount, the for-
mation of phosphate complexes can be promoted, reducing the reten- 3.4.1. Plant growth
tion rate of soil phosphorus. Fig. S2 shows the dry mass of above- and under-ground plant tissue.
The average change in the dry biomass of Sedum aizoon after 3 months
3.3. The heavy metal immobilization in plant substrates indicates an optimum application rate of 25% composts. There was a
negative mass change in the metal contaminated soil. Application ratio
The concentration of Cu, Zn, Cd and Ni in the composts-remediated of 50% compost had lower average change in dry mass compared to
soil showed statistically significant differences (p < 0.05) compared to that of no compost-remediated soil, however, the biomass increased
CK2, but the composts enhanced the metal concentration compared with the increase of compost addition. After 3 months of growth, the
with CK1 (Table 3). Cu concentration decreased after the addition of optimum application based on average change in dry mass was 25%
composts compared to the contaminated soil, and MSW-AC showed the composts. The different maturity composts had significant effect
most significant effect on the reduction of Cu content in the soil. The (p < 0.05) on biomass production, especially the application of MSW-
Zn, Cd and Ni concentration corresponding to compost-remediated AC indicated the most significant influence on biomass promotion.
treatments increased comparing with the original soil, while there was Table 4 shows the height and root characteristics for each treat-
a significant decrease comparing with the contaminated soil. ment. The plant height of all treatments ranged between 5.78 and
The effects different composts on metal speciation of Cu, Zn, Cd and 8.52 cm over the 3 months. Higher height was generally associated with
Ni in substrates are shown in Fig. 2. Metals were significantly im- the increase of compost addition. The highest plant height was obtained
mobilized in each of the compost treatments; especially Cd was stabi- in the 50% treatment of MSW-AC, with significant difference from other
lized with the exchangeable content decreasing from 3.6% to 0–1.2%. treatments with composts addition. The root distribution and physio-
The order of oxidizable and reducible Cd content was MSW-AC < logical characteristics of plant roots correlated with the soil environ-
MSW-SC < MSW-C. The oxidizable and residual fraction of Cd for the ment. The soils microenvironment characteristics such as soil structure
compost addition treatments was significantly higher than that in CK2. and nutrients space distribution can also be reflected by the growth of
Similarly, Cu, Zn and Cd were immobilized in all compost-remediated plant roots (Lynch, 1995). The root length is an important index to
treatments. The exchangeable Cu and Zn in the contaminated soil were determine the water and nutrient absorption efficiency of plants.
10% and 13%, respectively. After addition of composts, the exchange- Compared with the root system data of different compost treatments,
able Cu and Zn reduced to 3%–7% and 3.1%–7.7%, respectively. The the largest root length were 158.99 cm and 145.89 cm obtained in CK1
residual content of Cu increased from 48% in the contaminated soil and CK2, indicating that soil nutrient content was low without com-
without composts to 65%–82% in the compost-remediated treatments, posts addition, and the root system continuously extended and ex-
and the residual Zn increased by 16%–26%. panded to extract nutrients in the barren soil condition. And the root
The addition of MSW-AC caused the highest reduction (3%) of ex- length of the plant in MSW-AC was more than 100 cm, which was
changeable Cd in the substrates, followed by MSW-SC (2.4%). significantly longer than that of other treatments (p < 0.05). The root
Similarly, Cu, Zn and Cd were most strongly immobilized by MSW-AC, length of 50% compost addition treatment was shorter than that of the
the exchangeable fraction reduced by 9.2%, 9.7% and 4.3%, respec- treatment with 25% compost addition, indicating that the root length
tively. And Zn reduced significantly in MSW-AC addition treatments. In was closely correlated with the soil nutrient condition. However, if the
the compost-remediated soil, exchangeable Zn and Cd increased com- nutrient content in the planting substrates have satisfied the nutrient
paring with CK1, but exchangeable Cu and Ni in the compost-re- requirement for the plant growth, the root length will no longer in-
mediated soil showed no significantly difference comparing to the crease with the increase of compost addition.
original soil. Ni could be significantly immobilized in 50% composts Roots are usually stimulated to grow in fertile soil patches (Zhao
addition treatments. et al., 2004), and some studies on different plant species suggested that
The MSW compost increased the total Cu, Zn, Cd and Ni contents in fine roots might be quickly deployed to nutrient-rich soil areas to de-
the original soil; similar results have been obtained in other studies velop available resources (Wijesinghe et al., 2001; Gaiotti et al., 2017).

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L. Liu, et al. Journal of Environmental Management 250 (2019) 109525

Fig. 2. Effect of different compost treatments on the metal fraction distribution.

In this study, longer roots were found in MSW-AC treatment, implying with larger root volume and root biomass indicate the stronger ab-
that the plant roots had a rapidly growth and biomass accumulation sorption and reservation of nutrients by roots, thus to promote the
when water and nutrient supply was adequate, which was in agreement drought tolerance of plants (Zhao et al., 2004). Plants in the 25%
with results obtained by Keller (2005). The root surface, which better compost addition treatment have strong environmental adaptability.
reflected the water and nutrient capacity of the roots, was relevant to The MDA content accumulated and the degree of membrane lipid
the root length. The root surface area of the plants in 50% compost peroxidation increased because of the environmental stress conditions.
remediated soil is smaller than that of the treatment with 25% compost MDA content in root system (Table 4) reflected the degree of plant
addition. The root surface is the rhizosphere interfacial soil area, and stress. MDA content of plant roots in CK1 was 5.86 μmol g−1, sig-
larger root surface area means that the roots will be able to absorb more nificantly higher than that of the treatment with composts addition. The
nutrients from soil. MDA content of plant roots in CK2 increased by 65% compared with the
All compost treatments caused an increase in crown diameter treatment without heavy metals. The addition of compost can reduce
compared to the control. The largest root volume (1.73 ± 0.07 cm3) the MDA content in roots in certain degree and relieve heavy metal
was obtained in 25% MSW-AC, which differed significantly from that of stress. The addition of MSW-AC showed a more significant effect on the
the control. Root volume is an important indicator to determine the degree of membrane lipid peroxidation in plant roots. According to
spatial distribution of roots, reflecting the growth of plants and the soil- Fabrega et al. (2009), the humic acid adding to heavy metal con-
fixing effect. As for the control groups, the root length and surface area taminated soil could act as an antioxidant and reduce the degree of
were large, but with small root volume, indicating that poor soil nu- membrane lipid peroxidation in plants. The compost is rich in humic
trient conditions led to root epitaxial growth, however, the lack of acids, and contains functional groups such as phenolic, sulfhydryl and
nutrients was not conducive to the root biomass accumulation. Plants carboxyl groups, making it have reducing capacity. Therefore, compost

Table 4
The effects of composts on plant growth and root character in contaminated soil.
Treatments Height (cm) Root length (cm) Root surface area (cm2) Root volume (cm3) MDA (μmol/g)

a d d a
CK1 5.93 ± 0.64 158.99 ± 14.75 43.81 ± 2.82 0.61 ± 0.02 5.86 ± 0.36c
CK2 5.78 ± 1.25a 145.89 ± 3.93d 37.66 ± 0.99 cd 0.59 ± 0.05a 8.03 ± 0.31d
T1 6.90 ± 1.17 b 46.41 ± 7.15 b 17.51 ± 0.95a 0.63 ± 0.05 ab 5.06 ± 0.77 bc
T2 7.30 ± 0.85 b 48.74 ± 8.17 b 20.56 ± 2.13 b 0.76 ± 0.12 b 4.68 ± 0.66 b
T3 8.00 ± 0.87d 80.96 ± 2.34 bc 33.15 ± 2.46c 1.73 ± 0.07c 3.36 ± 0.97a
T4 6.20 ± 1.70c 41.15 ± 6.22a 17.07 ± 1.68a 0.66 ± 0.10 ab 5.24 ± 0.37 bc
T5 6.40 ± 0.37 cd 41.92 ± 7.99a 17.34 ± 4.15a 0.71 ± 0.04 b 3.73 ± 0.62 ab
T6 8.52 ± 1.29d 129.64 ± 8.65c 36.23 ± 2.96 cd 1.55 ± 0.12c 3.19 ± 0.57a

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L. Liu, et al. Journal of Environmental Management 250 (2019) 109525

Fig. 3. The heavy metal accumulation within the plant after 3 months growth.

humus can alleviate the stress of plants in contaminated soil. complex by Zn and compost organics is due to that Zn is involved in
chemical reactions or absorbed by biota with less kinetically restricts
3.4.2. Heavy metal uptake by plant (Jansen et al., 2002). Different results found that MSW compost
Total heavy metal accumulation in Sedum aizoon after growing for 3 amendments in soil may cause the immobilization of Zn, resulting in
months is shown in Fig. 3. Plants in CK2 accumulated more heavy reduced availability to plants (Moldes et al., 2007).
metals compared to those in other treatments; Cu and Zn of the plants Moreover, the bioavailability of Cd and Zn decreased when alkaline
of 50% composts addition treatments was a little higher than that of remediation was applied to contaminated soil, not only because of the
25% compost-remediated treatment. The concentration of Cd and Ni in increase of negative charge caused by soil pH increase, but also due to
plants were in the order of MSW-C > MSW-SC > MSW-AC. Re- the reduced solubility of the newly formed complex (Lee et al., 2009).
mediation of composts to contaminated soil changed the amount of These results are consistent with those of carbonate application re-
metals in the growing medium. The higher the compost content, the less sulting in a decrease of exchangeable Zn and an increase in residual
the Cu and Zn pollution of growing medium. The accumulation of Cd fraction. The FTIR results (Fig. 4) showed that the composts were rich
and Ni showed no significant change after composts addition. As Cu and in organic functional groups. The irregular surface of composts ampli-
Zn are both essential elements for plant growth, heavy metal accumu- fied 1000 times were observed by SEM (Fig. 4a-c), the diameters of
lation increased by the end of the 3 months growth trial. MSW-AC and MSW-SC were longer than that of MSW-C. The prominent
Comparing with original soil treatment, addition of compost im- change in the diameter of composts could be explained by further de-
proved the phytoextraction of metal contaminated soil. At this point, gradation of organic matter.
the 25% compost addition samples had the highest accumulation. Many As the FTIR analysis of composts presented in Fig. 4d, the bands of
stabilizing materials such as biochar and compost have been tested to MSW-C at 3434 cm−1 exhibited shifts to 3432 and 3435 cm−1 of MSW-
treat and control the heavy metal pollution of soil system (Ding et al., SC and MSW-AC, respectively, suggesting that the C–H in the saturated
2016). The organic functional groups suggested to be important in re- carbons stretching vibration and hydroxyl and amide groups shifted.
ducing the concentration of the dissolved Cd, thus the plant bioavail- The stretching band at 2957 cm−1 of MSW-AC showed decrease, which
ability of the metal was reduced with the addition of compost (Welikala was due to decomposition of aliphatic fractions. The adsorption bands
et al., 2018). However, the relatively high bioavailability of Zn in soils at 1492 cm−1 were characteristic of aromatic substances which shifted
with composts addition may also affect plant uptake of Cd (Welikala during secondary composting and aging process. Moreover, the change
et al., 2018). Studies have also been conducted on the analysis of of spectral peak at 1009 cm−1 for 1004 cm−1 corresponded to the de-
compost extracts, indicating that Zn and Cd complexes were relatively composition of polysaccharide components. As the organic matter in
unstable compared to Ni (Levy et al., 2012). the MSW-C was degraded by microorganisms and the degree of poly-
The bioavailability and potential hazard of metals is an important merization of humus increased, the relative abundance of structurally
issue during the organic soil remediation, that is, the duration of the complex aromatic functional groups increased in humic acid.
metal binding effect is affected by the degradation of organic matter by In addition, carboxyl or phenolic hydroxyl groups can directly affect
microbial action. Composts were expected to manage Cd bioavailability the adsorption of metal ions by metal complexation, which can provide
and exist in the soil for a longer period prior to dissociation. In addition, nutrient exchange sites and increase the absorption of minerals by
the utilization of compost to control Ni contamination may increase the plants and microorganisms (Khan et al., 2017). On the other hand,
mobility of Ni in soil (Custos et al., 2014). However, the less unstable humic substances concentration reflects the humification process of

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L. Liu, et al. Journal of Environmental Management 250 (2019) 109525

Fig. 4. SEM of MSW-C (a), MSW-SC (b) and MSW-AC (c); and FTIR spectra of composts (d).

organic wastes composting, which can affect metal solubility and properties by increasing the organic carbon, major nutrients and ex-
bioavailability. Chen et al. (2007) showed that the aging process can changeable cations (Papafilippaki et al., 2015; Weber et al., 2014).
change the compost characteristics. For instance, the presence of some Thus, the benefits of compost application include the prevention of
metal ions and organic matter with hydrophobic or large molecular can nutrient loss through leaching and the retention of nutrients in the root
alter the surface structure of the composts. The aging process can in- zone (Ippolito et al., 2012). Also, the MSW compost enhanced the total
troduce functional groups on the surface of composting material, metal concentrations compared with original soil (Carbonell et al.,
thereby affecting their adsorption properties (Zhang et al., 2006). 2011). In addition to the intrinsic properties of metals, the influencing
factors for the distribution of heavy metals in soil are related to the soil
3.5. The effects of the compost maturity on plant and soil properties properties and environmental factors, thus compost can indirectly
change the metal stability (Yin et al., 2016). Metal stabilization can be
To discern the relationship between compost maturity and soil or achieved by interactions between heavy metals and compost humic
plant properties in different treatments, principal components analysis acids, primarily through specific and non-specific adsorption and pre-
(PCA) was performed based on plant and substrate properties of dif- cipitation with different functional groups on the compost (Paradelo
ferent treatments (Fig. 5). The highest values for TN, CEC, OC, TP, AK, and Barral, 2012). Therefore, high organic matter and microbial con-
AP, water content and field capacity were associated with T3, T4, T5 tent in compost could be conducive to metal fixation (Zhou et al.,
and T6, whereas the exchangeable metals, bulk density were associated 2014). Composts with different added proportions showed enhance-
with CK2, T1 and T2 (Fig. 5a). The substrate nutrients were higher for ment on the available fraction of metals, indicating the bound force of
the treatments with 50% compost addition. On the contrary, available metal to soil with amendments, however, this contrasts with other
metals were higher in the control group and treatments with 25% MSW- studies (Liang et al., 2017). Composts in soil increased the metal uptake
C and MSW-SC, respectively. Fig. 5b shows that with higher metal in plants compared with original soil, but limited the heavy metals
content in plants, underground-biomass and MDA in CK2 were in- uptake compared with contaminated soil. The uptake rate of different
versely correlated with plant height, root volume and over-ground metals depended on the properties of metals (Carbonell et al., 2011). As
biomass. As mentioned, a mixture with appropriate addition of com- Yusuf et al. (2011) suggested, the increase of Ni uptake by plants in the
posts can improve the plant growth, especially with MSW-AC. acidic soil was due to that the high soil pH diminished Ni uptake for the
Domènech et al. (2011) found that seed of plants could be significantly formation of insoluble compounds. Metal uptake may be a more reli-
affected by compost addition amount and the time of composting able indicator than metal concentrations in the study of ecological risks
process. associated with contaminated soils (Singh and Agrawal, 2007). Overall,
It is widely accepted that compost application improves soil the variances in compost types and the addition amount did have

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L. Liu, et al. Journal of Environmental Management 250 (2019) 109525

Fig. 5. Principal component analysis of parameters of substrates (a) and plants (b). Dots correspond to the different treatments.

impacts on the immobilization effects during soil amendments. compost products as organic fertilizer requires consideration on the soil
pollution and safety problems. Thus, future research may focus on
3.6. The environmental engineering applications of MSW compost greenhouse gas emissions, heavy metal fixation, and leachates of ni-
trogen and phosphorus during composting and application process (Sui
In order to accomplish sustainable soil remediation, it is desirable to et al., 2019).
use composts for improving soil structure, retaining water and in-
creasing the nutrients availability (Zanella et al., 2018; Fagnano et al., 4. Conclusions
2011). MSW compost obtained through biodegradation process can be
used to reduce conventional landfill disposal. According to Cala et al. Applying different maturity composts with different proportions to
(2005), the use of compost from municipal solid waste helped enhance heavy metal contaminated soil could change soil physicochemical
the content and stability of soil organic matter. Several studies de- properties and improve the plant growth due to the high organic matter
monstrated that the repeated application of MSW compost consistently and nutrients in composts. The higher soil OC, TN, AP and AK caused by
increased soil organic matter content and soil C/N ratio greater than added compost were found in a certain compost addition (especially in
those of un-remediated soil (Montemurro et al., 2005). 50%). In addition, compost with different addition amount significantly
MSW compost was applied to different types of field crops, causing reduced the bioavailability of metals. Compost addition could improve
various plant responses, because different kinds of soil have their own metal stability and increase the residual fraction comparing with the
chemical and physical characteristics, thereby the nutrients existed in contaminated soil. The height growth and biomass accumulation of
the compost may vary in their availability. It was found that a combi- Sedum aizoon were higher in the 25% compost remediation soil treat-
nation of 50% MSW compost and 50% mineral fertilizer produced the ments, and the addition of MSW-AC was more suitable for plant growth
same marketable yield of growing vegetables as that produced by 100% and root volume accumulation. The root length and root surface area of
inorganic fertilizer (Mylavarapu and Zinati, 2009). Also, MSW compost Sedum aizoon were not affected by compost addition. The MDA content
was found to be an appropriate media mixed with peat for rapeseed decreased after composts addition, suggesting that the plants have
growth, and the optimum mixing ratio was 50%:50% (Avramidou et al., better resistance to stress. Consequently, the MSW-AC application at
2013). At the application rate with 60 t ha−1, MSW compost can be 25% was suitable for Sedum aizoon cultivation, and contributed to the
used as effective organic amendment in sandy soil (Papafilippaki et al., stability of metals in contaminated soil. However, long-term field trials
2015). However, it is very important to control the amount of composts, are needed to further assess the effectiveness of compost in soil re-
avoiding pollution and inhospitable conditions for plant growth. mediation.
The treatment efficiency and product quality of aerobic compost are
the determinants for its application and promotion. Therefore, re- Acknowledgments
searches should focus on the following aspects:
The selection of suitable compost additives is crucial to ensure op- The authors are grateful for the financial support by the Hebei
timal effects. A wide range of additives have been explored, for ex- University Scientific Research Foundation (No. 801260201305). We are
ample, biochar showed positive effects on reducing the compost process also thanks to our all laboratory colleagues and research staff members
time and improving compost quality (Onwosi et al., 2017). However, for their constructive advice and help.
the cost-effectiveness and efficiency of additives need further study. In
addition, it is crucial to adjust the ratio of raw materials and additives Appendix A. Supplementary data
to improve compost efficiency, thus to ensure the humification process
and humic acid content. The relationship between composting process Supplementary data to this article can be found online at https://
parameters and the humic formation also need to be further explored doi.org/10.1016/j.jenvman.2019.109525.
(Petric and Mustafic, 2015). During the MSW-C application in greening,
it is necessary to explore the mechanism of compost characteristics on References
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