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Chemosphere 119 (2015) 177–183

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Chemosphere
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Effects of inorganic and organic amendments on the uptake of lead


and trace elements by Brassica chinensis grown in an acidic red soil
Xianjin Tang, Xia Li, Xingmei Liu, Muhammad Z. Hashmi, Jianming Xu ⇑, Philip C. Brookes
Institute of Soil and Water Resources and Environmental Science, Zhejiang Provincial Key Laboratory of Subtropical Soil and Plant Nutrition, Zhejiang University, Hangzhou
310058, China

h i g h l i g h t s

 Organic amendments were more effective to reduce Pb availability and uptake.


 Organic amendments greatly increased the Fe–Mn oxides fractions.
 Fe, Mn, Cu and Zn was not significantly affected in soil and plants.
 The organic amendments have the potential to remediate Pb-contaminated soil in situ.

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

Article history: A greenhouse study was conducted to investigate the effects of inorganic (phosphate rock, single
Received 25 January 2014 superphosphate and calcium magnesium phosphate) and organic amendments (peat, straw manure
Received in revised form 9 May 2014 and pig manure) on the uptake of lead (Pb) and trace elements by Chinese Cabbage (Brassica chinensis)
Accepted 28 May 2014
grown in an acidic red soil. The application of all organic amendments increased the soil pH while inor-
ganic amendments such as single superphosphate did not. Both inorganic and organic amendments
Handling Editor: X. Cao decreased the availability and uptake of Pb while the organic amendments were superior to the inorganic
(phosphate) amendments in reducing the availability of the more labile (soluble and exchangeable Pb)
Keywords: forms of soil Pb. More Pb was taken up by roots than shoots with all soil amendments. Among the organic
Pb amendments, straw manure and pig manure caused the largest decrease in Pb availability at 456.5 and
Trace metals 457.3 mg kg1, respectively, when a high level of 30 g organic amendments kg1 was applied. The organic
Chemical immobilization amendments greatly increased the fraction D targeted to Fe–Mn oxides bound Pb, and decreased the frac-
Uptake tion A (water-soluble), B (exchangeable), and C (carbonate-bound), thereby decreasing the solubility and
Brassica chinensis mobility of Pb in soil. The organic amendments also significantly improved the concentrations of Fe, Mn,
Cu and Zn in the soil and shoots (except Fe in shoots and/or roots), which are essential for plant nutrition.
The organic amendments of straw and pig manure lowered the availability and uptake of Pb but not that
of other trace metals. Thus, these amendments have the potential to remediate Pb-contaminated soils
in situ.
Ó 2014 Elsevier Ltd. All rights reserved.

1. Introduction adversely affect seed germination, plant growth, and photosynthe-


sis in large-scale agricultural operations (Ruley et al., 2006). There-
Heavy metal contamination in soil originates from various fore, the remediation of Pb contamination in agricultural soils is an
anthropogenic activities, such as mining, smelting, and the dis- important concern. Ex situ soil remediation options, including land-
posal of industrial wastes, and has attracted considerable public fill, washing, etc., are effective treatments for highly polluted and
attention worldwide (Adriano, 2001; Cui et al., 2007). Among small volumes of soil (Fedje et al., 2013). However, these methods
heavy metals, lead (Pb) is particularly persistent in nature, as it suffer from recognizable drawbacks, such as being environmental
has no biological role and is highly toxic to wildlife and humans unfriendly, and may also involve some risk to ecosystems and
via the food chain (Papanikolaou et al., 2005). Lead in soils can also human health. Other in situ technologies, including phytoremedia-
tion and bioremediation are less expensive, more environmental
friendly and better suited for use in less polluted and larger areas.
⇑ Corresponding author. Tel./fax: +86 571 8898 2069.
However, these processes are sometimes less efficient and more
E-mail address: jmxu@zju.edu.cn (J. Xu).

http://dx.doi.org/10.1016/j.chemosphere.2014.05.081
0045-6535/Ó 2014 Elsevier Ltd. All rights reserved.
178 X. Tang et al. / Chemosphere 119 (2015) 177–183

time-consuming than physical and chemical approaches (Pulford contents were 1.4%, 4.6 and 53.0 mg kg1, respectively. The soil
and Watson, 2003). amendments included inorganic and organic fertilizer: (1) phos-
Chemical immobilization, a remediation technique that phate rock (RP), (2) single superphosphate (SSP), (3) calcium mag-
decreases the concentration of dissolved contaminants by sorption nesium phosphate (CM), (4) peat (PE), (5) straw manure (SM) and
or precipitation (Basta et al., 2001), is suitable for soil remediation. (6) pig manure (PM). The straw manure was taken from a small
Various inorganic (Yang et al., 2003; Park et al., 2011a; He et al., farmer in Feixi city of Anhui, while the pig manure was sourced
2013) and organic amendments (Madejón et al., 2006; Park et al., from a big farm in Huzhou city of Zhejiang, China.
2011b) have been used for the chemical immobilization of heavy
metals in soil. Inorganic materials that have been successfully 2.2. Treatments
tested to reduce the availability of heavy metals to plants include
rock phosphate, apatite, hydroxyapatite, iron and manganese oxi- The soil amendments were applied to soil at two levels: low
des and oxyhydroxides, and liming agents (Keller et al., 2005). Inor- level, 152.8 mg P kg1 soil for phosphate rock (RP1), single super-
ganic fertilizers, such as NH+4–N-containing fertilizers, can greatly phosphate (SSP1), and calcium magnesium phosphate (CM1);
decrease the mobilization of Pb (Tu et al., 2000). Many studies have and 10 g kg1 for peat (PE1), straw manure (SM1), and pig manure
examined P-induced immobilization in Pb-contaminated soil (Cao (PM1). A high level, 458.5 mg P kg1 soil, was used for phosphate
et al., 2002; Zhu et al., 2004; Shahid et al., 2013) and found a rock (RP2), single superphosphate (SSP2), and calcium magnesium
significant reduction in Pb uptake by plants. Organic amendments phosphate (CM2); and 30 g kg1 was used for peat (PE2), straw
are low-cost adsorbents that will supply plant nutrients and manure (SM2), and pig manure (PM2). The experiment included
improve the water-retention capacity of soil. They may also help thirteen treatments (including the control) with three replicates
to reduce phytotoxicity, which increases plant growth and survival per treatment. The selected physicochemical properties of the
(Levy et al., 1999). Farmyard manure, cow or pig manure, and com- amendments are given in Table 1.
post decrease the availability of heavy metals in soils and crops
(Pichtel and Bradway, 2008). Numerous studies have evaluated
the effects of soil amendments in controlling the availability and 2.3. Plant and greenhouse experiments
mobility of metals in contaminated soils (Kumpiene et al., 2008;
Cao et al., 2009). One cultivar of Chinese Cabbage, Brassica chinensis (var. Huang-
Trace metals, such as Zn, Fe, Mn and Cu, are essential for plant guan qingjiang), was chosen for the greenhouse pot experiments.
growth but are required in very small amounts. Trace metals are The soil was mixed thoroughly with 600 mg Pb kg1 as Pb(NO3)2.
involved in almost all metabolic functions, such as energy metab- Each amendment was applied separately to the soil at two levels
olism, primary and secondary metabolism, cell protection, gene of 152.8 and 458.5 mg P kg1 for the inorganic amendments and
regulation, hormone perception, signal transduction, and 10 and 30 g kg1 for the organic amendments. Subsequently,
reproduction (Hänsch and Mendel, 2009; Hebbern et al., 2009). 1.4 kg of soil was placed in each plastic pot (20 cm  20 cm). After
Historically, their physiological role was first described based on a two-week incubation period, 15 seeds were planted in each pot.
deficiency symptoms. The addition of organic fertilizers signifi- One week later, uniformly emerged seedlings were thinned to
cantly increases the amounts of trace metals that accumulate in three seedlings per pot. The plants were grown for two months
plants (Yang et al., 2003). However, the application of inorganic in a greenhouse at 18–25 °C, and supplied with water as required.
fertilizers, such as phosphate rock, calcium magnesium phosphate At harvest, the plants were removed from the pots, and the shoots
and single superphosphate, can reduce the mobility of trace ele- were separated from the roots. The two parts were rapidly and
ments (Biling et al., 2008). Similarly, Fang et al. (2012) reported thoroughly washed in de-ionized water, then dried at 70 °C for
that P amendments significantly decreased the uptakes of Zn, Cu 24 h and weighed. Approximately 100 g soil from each treatment
and Pb by Chinese Cabbage and kale in a soil contaminated with was collected for analysis. The soil samples were air-dried, ground
several heavy metals. <2 mm mesh and stored in labeled Ziploc polythene bags until
Red soils (Ultisols) are widespread in China and the high con- analysis.
centration of iron (III), aluminum oxides and hydroxides, as well
as the low level of pH in these soils has a major effect on the soil 2.4. Analysis
properties and behavior of metals in soils. Inorganic P is the most
frequently used amendment to decrease soil Pb availability Soil pH was determined with a pH meter in 1:5 soil water sus-
(Hettiarachchi et al., 2001; Park et al., 2011a). However, studies pensions after 0.5 h. The total soil Pb contents were determined via
of organic amendments and comparisons between inorganic and flame atomic absorption spectrometry (FAAS300, Germany) after
organic amendments for acidic red soil are relatively scarce digestion with HNO3 and HCl (Singh et al., 2010). The soil available
(Rotkittikhun et al., 2007). Furthermore, most studies have only Pb was determined by extracting 10 g soil with 50 mL of 1 M HCl
focused on Pb uptake, and fewer have considered the effects of soil on an orbital shaker for 1.5 h. Sequential extraction was performed
amendments on trace elements in Pb-polluted soil. Therefore, the for the speciation of Pb in soil samples according to the scheme of
objectives of the present study were to identify the effects of inor- Tessier et al. (1979), which is briefly listed in Table 2. However, it
ganic and organic amendments on Pb uptake by plant biomass and should be pointed out that this method just gives the operation-
on soil Pb speciation, and to verify their effects on the availability ally-defined fractions of Pb in soil and the accuracy and validity
of trace metals (Zn, Fe, Mn and Cu) in an acidic red soil. of sequential extraction method for the purpose of metal specia-
tion has been questioned (Kim and Fergusson, 1991; Kim and
McBride, 2006; Tai et al., 2013). Generally, 2 g of air-dried soil
2. Materials and methods was taken for the sequential extraction in 50 mL centrifuge tubes.
After each extraction, a separation was performed by centrifuga-
2.1. Soil and amendments tion at 3000 rpm for 5 min. For the analysis of Fe, Zn, Cu, Pb and
Mn in plant tissues, 1 g of dried tissue was digested in 15 mL
A red clay soil contained 23.3% clay, 51.4% silt and 25.3% sand HCl/HNO3/HClO4 (3:1:2 v/v) at 150 °C until the solution became
from a garden in Longyou city of Zhejiang province, China clear. The resulting solutions were filtered, diluted to 25 mL in
(29°60 N, 119°110 E) was used. The organic matter, pH and total Pb volumetric flasks and stored at 4 °C prior to analysis.
X. Tang et al. / Chemosphere 119 (2015) 177–183 179

Table 1
Selected physicochemical properties of soil and amendments.

Soil or amendments pH Clay (%) Silt (%) Sand (%) Organic matter (%) Total N (g kg1) Total P (g kg1) Total Pb (mg kg1)
Soil 4.62 23.3 51.4 25.3 1.4 0.8 0.3 53.0
Phosphate rock (RP) 7.00 NAa NA NA NA NA 320 88.6
Single superphosphate (SSP) 2.75 NA NA NA NA NA 160 1.4
Calcium magnesium phosphate (CM) 8.89 NA NA NA NA NA 130 25.8
Peat (PE) 6.06 NA NA NA 40.9 11.1 NA NDb
Straw manure (SM) 6.48 NA NA NA 68.9 10.0 NA ND
Pig manure (PM) 7.54 NA NA NA 29.8 13.2 NA 14.2
a
NA: not available.
b
ND: not detected.

Table 2
7.0
Sequential extraction scheme according to Tessier et al. (1979).

Extraction Fraction Methods Pb form 6.5


step ID targeted
6.0
1 A 30 mL of deionized water for 2 h Water
soluble

pH
5.5
2 B 16 mL MgCl2 (pH 7.0, 1 M) for 1 h Exchangeable
3 C 16 mL NaOAc (pH 5.0, 1 M) for 5 h Carbonate 5.0
bound
4 D 20 mL 0.04 M NH2OH–HCl in 25% Fe–Mn 4.5
(v/v) HOAc at 96 °C with occasional oxides bound
agitation for 6 h 4.0
5 E 6 mL of 0.02 M HNO3 and 10 mL of Organic CK RP1 RP2 SSP1 SSP2 CM1 CM2 PE1 PE2 SM1 SM2 PM1 PM2
30% H2O2 (adjusted to pH 2) with bound
HNO3 at 85 °C with occasional Fig. 1. Change of pH in the tested red soil as affected by inorganic and organic
agitation for 2 h; repeated for 3 h. amendments.
After cooling, 10 mL of 3.2 M
NH4OAc in 20% (v/v) HNO3 added.
Then the samples were diluted and the application of SM2 and PM2 increased the soil pH to 5.5 and
agitated continuously for 30 min 5.4, respectively. Organic amendments, such as cow manure, local
6 F Residuals were digested in HCl– Residual Pb
farmyard manure and straw, have been reported to increase soil
HNO3–HClO4 mixture
pH (Singh et al., 2010; Chaiyarat et al., 2011). Wang et al. (2013)
also observed that the addition of organic amendments (Chinese
milk vetch, rice and wheat straw) increased pH by 0.1–0.8 U in
paddy soils. When organic amendments were amended in the soil,
2.5. Statistical analysis
the microbial breakdown of organic anions (as indicated by excess
cations) appeared to be a major cause of soil pH increase (Xu et al.,
All data were analyzed by using Microsoft Office 2003 and DPS
2006; Wang et al., 2013).
7.0. The probability value (p 6 0.05) indicates statistical signifi-
cance. All results are the means of triplicate determinations.
3.2. Availability and speciation of Pb in soil

3. Results and discussion The concentrations of available Pb in the acidic red soil after
application of inorganic and organic amendments are given in
3.1. Soil pH Table 3. Compared to the control, which did not receive soil
amendments, the concentration of available Pb was only slightly
Because pH is one of the most important parameters to affect reduced, or not reduced significantly, by most of the inorganic
the availability of heavy metals, the effects of inorganic and organic and organic amendments. It was found that high levels of single
amendments on the soil pH were tested. The soil pH was mostly superphosphate (SSP2) and calcium magnesium phosphate (CM2)
increased by the application of inorganic amendments (Fig. 1). significantly decreased the available Pb from 507.1 to approxi-
When the calcium magnesium phosphate was applied, the soil mately 358.3 and 436.0 mg kg1, respectively. Similarly, decreased
pH increased from 4.6 to 4.8 and 6.3 with low and high levels of Pb availability after the application of various inorganic treatments
amendment, respectively. Zhu et al. (2004) also found that inor- has also been previously reported (Cao et al., 2009). The organic
ganic amendments (phosphate rock and hydroxyapatite) had no amendments also decreased the Pb availability from 507.1 to as
negative effects or even increased the soil pH. However, the appli- low as 456.5 mg kg1, a small but significant decrease. However,
cation of single superphosphate also slightly decreased the soil pH the available Pb concentration was not significantly different
from 4.6 to 4.5 when a high level was applied. This decrease of pH among the three organic amendments at either rate.
might be mainly due to the lowest original pH of single superphos- Different inorganic and organic amendments resulted in signif-
phate (2.75). A decrease in the soil pH after amendment with inor- icant changes in the Pb speciation (Fig. 2). With the application of
ganic nutrients (phosphate and phosphorus) was also observed in inorganic amendments, there were high percentages of fraction A
other studies (Chen et al., 2007; Fang et al., 2012). Specially, all targeted to water-soluble (0.14–0.28%), B targeted to exchangeable
organic amendments (peat, straw manure, and pig manure) (11.3–62.0%), and C targeted to carbonate bound (22.8–49.2%) of
increased the soil pH, as shown in Fig. 1. Singh et al. (2010) found Pb. The effect of inorganic amendments on the fraction A, B and
that soil pH increased to 7.2 after the application of farmyard man- C was marginal when compared to the control without any
ure and this pH value was higher than that in our study, in which amendments. However, the application of high levels of calcium
180 X. Tang et al. / Chemosphere 119 (2015) 177–183

Table 3
Concentrations of available Pb and other trace elements in soil with inorganic and organic amendments (mg kg1).

Treatment Pb Fe Mn Cu Zn
CK 507.1 ± 23.7 a 112.2 ± 17.4 ab 80.3 ± 2.1 c 2.4 ± 0.03 de 10.4 ± 0.4 cd
Rock phosphate (low level, RP1) 462.3 ± 30.6 abc 72.3 ± 6.2 cde 70.4 ± 3.1 cd 2.4 ± 0.03 de 9.9 ± 0.2 de
Rock phosphate (high level, RP2) 482.5 ± 12.6 ab 45.5 ± 16.5 e 61.0 ± 20.5 de 2.4 ± 0.12 cde 9.9 ± 0.3 de
Single super phosphate (low level, SSP1) 498.6 ± 33.8 ab 70.7 ± 28.4 de 80.1 ± 2.3 c 2.4 ± 0.07 de 10.5 ± 0.5 cd
Single super phosphate (high level, SSP2) 358.3 ± 8.1 d 88.4 ± 25.9 bcd 76.6 ± 2.7 c 2.4 ± 0.05 de 10.3 ± 0.4 cd
Calcium magnesium phosphate (low level, CM1) 476.9 ± 22.2 abc 65.2 ± 3.3 de 48.6 ± 16.2 f 2.5 ± 0.07 cde 9.5 ± 0.2 e
Calcium magnesium phosphate (high level, CM2) 436.0 ± 11.8 c 78.5 ± 18.6 cd 53.6 ± 2.5 ef 2.1 ± 0.09 e 9.1 ± 0.1 e
Peat (low level, PE1) 499.3 ± 19.6 ab 98.9 ± 3.3 bc 81.2 ± 3.6 c 2.3 ± 0.08 de 10.7 ± 0.6 cd
Peat (high level, PE2) 459.1 ± 11.9 bc 88.4 ± 16.1 bcd 61.3 ± 4.9 de 2.1 ± 0.17 de 10.9 ± 0.7 c
Straw manure (low level, SM1) 468.3 ± 17.6 abc 127.7 ± 13.8 a 98.4 ± 8.3 b 2.5 ± 0.03 cd 11.0 ± 0.2 c
Straw manure (high level, SM2) 456.5 ± 9.3 bc 80.4 ± 12.1 cd 115.3 ± 5.0 a 2.8 ± 0.54 c 10.7 ± 1.0 cd
Pig manure (low level, PM1) 457.9 ± 21.1 bc 71.7 ± 9.6 cde 76.6 ± 2.0 c 4.1 ± 0.06 b 13.8 ± 0.5 b
Pig manure (high level, PM2) 457.3 ± 32.0 bc 64.0 ± 22.3 de 97.4 ± 2.22 b 7.7 ± 0.55 a 19.8 ± 0.7 a

Note: values in the columns followed by different letters indicate significant differences (p 6 0.05) among different treatments, and values represent means ± standard
deviation.

to the non-amended control. Organic matter has been previously


Distribution of different forms of Pb

A B C D E F shown to adsorb Pb in soil and so reduce the availability of soil


100% Pb (Pichtel and Bradway, 2008). Organic matter or humic sub-
stances are introduced into the soil by adding organic amendments
80%
and are the main sites of Pb sorption in soil, due to strong complex-
60% ation, while Pb-phosphate compounds are likely to precipitate
(Song and Greenway, 2004; Kumpiene et al., 2008; Udovic and
40% McBride, 2012). The application of organic amendments increases
soil organic matter, humic substances and pH which decrease the
20%
availability of Pb (Zhu et al., 2004; Wang et al., 2012). However,
0% apparently very low concentration in the fraction E targeted to
CK RP1 RP2 SSP1 SSP2 CM1 CM2 PE1 PE2 SM1 SM2 PM1 PM2
organic bound Pb with both inorganic and organic amendments
might be an artifact of the sequential extraction method according
Fig. 2. Speciation of Pb in soil after the application of inorganic and organic
amendments (fraction A, B, C, D, E and F is targeted to the water soluble, to Tessier et al. (1979). Previous researches have shown that the
exchangeable, carbonate bound, Fe–Mn oxides bound, organic bound and residual step immediately before the ‘‘organic extraction’’ step could bring
Pb in soil, respectively, which could be seen clearly in Table 2). a large part of the organic-bound Pb into solution, ensuring that
the ‘‘organic fraction’’ as defined by the method is biased low or
certainly not correct (Kim and McBride, 2006; Tai et al., 2013).
Thus the extraction method should be improved for the analysis
magnesium phosphate (CM2) resulted in the highest percentage of of Pb forms in soil in further study. Overall, the organic amend-
fraction F (residual Pb, 22.3%). Inorganic treatments, such as ments were superior to the inorganic amendments in reducing
hydroxylapatite, natural phosphate rock and single super phos- the solubility and mobility of Pb, despite the minimal effect of
phate, could increase the residual Pb (Zhu et al., 2004). They also organic amendments on strong-acid extractable Pb. In addition,
found that different inorganic amendments reduced the fraction more experiments about the mineralization process and products
A, B and C targeted to water soluble, exchangeable and carbonate of organic amendments and there effects on Pb fractions in soil
bound Pb, respectively, by a similar percentage to that observed are needed to better understand the role of organic amendments
in our study. The application of organic amendments significantly in Pb immobilization.
increased the fraction D targeted to Fe–Mn oxides bound Pb
(29.4–45.0%) compared to the control and inorganic amendments.
The fraction A, B and C targeted to water soluble, exchangeable and 3.3. Plant biomass and uptake of Pb
carbonate bound Pb, respectively, was much lower than the inor-
ganic amendments. The higher fraction D targeted to Fe–Mn oxides The inorganic and organic amendments considerably increased
bound Pb in the present study was probably due to the strong the dry weight of the shoots of B. chinensis while the roots in the
affinity of Pb for humic acid and its tendency to form stable Pb amended treatments weighed less than those in the control except
humic acid complexes, therefore, the solubility and mobility of for the inorganic treatment of single superphosphate. The highest
Pb were greatly decreased. Similarly, there was an increase in the shoot and root biomasses occurred with the inorganic amendment
fraction D after the application of bone biochar (Chen et al., of calcium magnesium phosphate (2.52 g pot1) and single
2006). The fraction E (organic bound, 0.42–1.99%) with the organic superphosphate (0.14 g pot1), respectively. The shoot biomass
amendments was little higher than the inorganic treatments (1.01–1.60 g pot1) in all organic treatments was higher than the
(0.15–1.11%), while the residual Pb was just the reverse. Among control, which had a biomass of 0.77 g pot1. However, the root
the organic amendments, high levels of pig manure caused the biomass (0.06–0.08 g pot1) was slightly lower than the control
highest increases in the fraction D (targeted to Fe–Mn oxides at 0.12 g pot1 in the organic amended pots. The major benefits
bound Pb), E (targeted to organic bound Pb) and F (targeted to of manure addition to soil are related to the increased organic
residual Pb) at 45.0%, 2.0%, and 12.9%, respectively. matter content and biological activity, leading to increased plant
Soil pH is one of the important factors that control the availabil- biomass. However, manure and compost provide total nutrient
ity of the different chemical forms of metals in soil (Kumpiene contents and the availability of the nutrients for plant growth will
et al., 2008). The application of most amendments increased soil depend on their mineralization from the organic components
pH, thus the concentration of available Pb was lower compared (Rosen and Allan, 2007).
X. Tang et al. / Chemosphere 119 (2015) 177–183 181

20.0 70.0
18.0 A B

Pb content in roots (mg/kg)


Pb content in shoots (mg/kg)
60.0
16.0
14.0 50.0
12.0
40.0
10.0
8.0 30.0
6.0 20.0
4.0
10.0
2.0
0.0 0.0

CK
RP1
RP2
SSP1
SSP2
CM1
CM2
PE1
PE2
SM1
SM2
PM1
PM2
CK
RP1
RP2
SSP1
SSP2
CM1
CM2
PE1
PE2
SM1
SM2
PM1
PM2
Fig. 3. Effects of soil amendments on Pb concentration in shoots (A) and roots (B) of plants.

The uptake of Pb by B. chinensis grown in acidic soil amended with 3.4. Phytoavailability and uptake of trace elements
inorganic and organic amendments are shown in Fig. 3. The Pb
uptake in shoots was considerably decreased by the application of The phytoavailability of trace metals (Fe, Mn, Cu and Zn)
inorganic amendments of single superphosphate (2.9–5.2 mg kg1) showed a different trend in both the inorganic and organic amend-
and calcium magnesium phosphate (1.3–4.8 mg kg1) compared to ments compared to the control (Table 3). With all inorganic
the control (13.7 mg kg1). All inorganic treatments reduced Pb amendments, the concentrations of available Fe, Mn, Zn and Cu
uptake by roots, and the calcium magnesium phosphate had the were reduced compared to the control. The calcium magnesium
largest reduction of 3.0 mg kg1 compared to the control of phosphate treatment decreased the following metals the most:
55.4 mg kg1. Calcium magnesium phosphate and single super Mn (23.7%), Cu (1.0%) and Zn (4.5%), while phosphate rock (RP2)
phosphate treatments significantly decreased the Pb concentrations showed the highest reduction for Fe (22.2%). This reduction in Cu
in plant tissues, which might be attributed to the precipitation of and Zn was lower in our study than that of Cao et al. (2009). They
pyromorphite-type minerals and ion exchange at lower soil pH, reported that Cu and Zn were reduced by 81% and 74%, respec-
which decreased Pb mobility (Zhu et al., 2004). All organic amend- tively, after the application of phosphorus to soybean plants
ments efficiently decreased the Pb uptake by shoots and root, except (G. max L.) and lettuce (L. sativa L.). However, the reduction of
treatment of SM1 for root. The highest decrease in Pb uptake in Mn, Cu and Zn in our study was similar to that found by Singh
shoots (3.5 mg kg1) and roots (6.9 mg kg1) was recorded for pig et al. (2010) for Beta vulgaris L. The addition of P fertilizer in soluble
manure (PM2) compared to the control and other organic amend- and highly available forms in inorganic treatments could result in
ments (5.1–14.7 mg kg1). Pichtel and Bradway (2008) also found decreased Zn availability. Thus, improved P nutrition might be one
similar decrease in the Pb uptake in upper parts of spinach (Spinacea of the major mechanisms involved in the alleviation of plant metal
oleracea), cabbage (Brassica oleracea), and a grass–legume mix (red toxicity (Chen et al., 2003). The concentrations of available trace
fescue, Festuca rubra; ryegrass, Lolium perenne) after the application elements in soil were significantly higher in response to organic
of organic amendments such as peat and compost. However, the Pb amendments than inorganic ones or the non-amendment control,
concentration in plant tissue did not follow a clear pattern with although some reductions were still observed (i.e., Fe). The concen-
respect to soil pH in all amendments. trations of Fe (127.7 mg kg1) and Mn (115.3 mg kg1) were high-
Several factors could be responsible for this low uptake of Pb est in soil after the application of straw manure, while the
from soil. Concentration of available Pb in soil may be the main fac- concentrations of Cu (7.7 mg kg1) and Zn (19.8 mg kg1) were
tor that controls plant uptake. Singh et al. (2010) reported that dif- the highest in response to pig manure. The results suggested that
ferent initial Pb contents in soil may affect uptake by different straw manure and pig manure increased the contents of these
plant species. The limited uptake of Pb by plants is relatively low metals. The positive effects of organic amendments such as dairy
due to its low availability of Pb. Similar results were obtained in manure and farmyard manure on these metals have been reported
previous investigations, i.e. the Pb concentrations in shoots of previously (Cao et al., 2009; Singh et al., 2010).
sudex (Sorghum bicolor L.), St. Augustine grass (Stenotaphrum The uptake of trace metals by plants also significantly differed
secundatum), Chinese cabbage (B. chinensis L.), soybean (Glycine between the inorganic and organic amendments (Fig. 4). The Fe con-
max L.), lettuce (Lactuca sativa L.), and ryegrass (L. perenne L.) were tents were higher in response to inorganic than organic amendment.
reduced after the application of inorganic fertilizer to Pb-polluted Higher Fe contents were found in RP2 compared to other treatments,
soil (Cao et al., 2002; Chen et al., 2006; Waterlot et al., 2011). Fur- while the Mn, Cu and Zn contents were higher in response to organic
thermore, the formation of insoluble compounds from inorganic amendments. The Mn, Cu and Zn contents were higher in SM1 com-
ions released during organic matter mineralization and from pared to the other amendments and control. However, peat signifi-
organic Pb complexes (favoured at higher pH) could be responsible cantly reduced the contents of Fe, Mn and Zn in shoots compared to
for the low Pb accumulation in B. chinensis (Walker et al., 2004). In the other organic amendments. Al Chami et al. (2013) also reported
addition, the high efficiencies in reducing plant uptake of Pb by that Zn concentrations were higher in shoots when an organic
both inorganic and organic amendments in this experiment could amendment (manure) was applied compared to the inorganic
also be partly contributed by the spiked soil with Pb(NO3)2 in amendments. Complexes of Zn with low-molecular-weight organic
which proportionally more Pb is highly reactive initially. Tai acids are more available to uptake by plants, and consequently, more
et al. (2013) found that the spiked soil generally contained more Zn was absorbed into plant roots and transferred to plant shoots
labile fraction of Pb (soluble and exchangeable) compared to (Huang et al., 2013). The availability of trace metals in soil also
long-term contaminated soil. Therefore, in the case of filed con- depends on the chemical speciation of the metal, pH and other soil
taminated soil (e.g., smelter-contaminated soil) with less soluble chemical and physical properties (Smith, 2009). In summary, the
forms of Pb, especially when soil pH is not low, the formation of trace metal results indicated that most of the organic amendments
insoluble compounds, the reducing of Pb solubility and mobility, increased the contents of trace metals except Fe compared to
and consequently, the low uptake of Pb are likely to be less evident. inorganic amendments in soil and plants.
182 X. Tang et al. / Chemosphere 119 (2015) 177–183

8.0
45.0 A B

Mn content in shoots (mg/kg)


7.0

Fe content in shoots (mg/kg)


40.0
6.0
35.0
30.0 5.0
25.0 4.0
20.0 3.0
15.0
2.0
10.0
5.0 1.0

0.0 0.0
CK
SSP1
SSP2
RP1
RP2
CM1
CM2
PE1
PE2
SM1
SM2
PM1
PM2

CK
SSP1
SSP2
RP1
RP2
CM1
CM2
PE1
PE2
SM1
SM2
PM1
PM2
1.2 C 50.0 D
45.0

Zn content in shoots (mg/kg)


Cu content in shoots (mg/kg)

1.0 40.0
35.0
0.8
30.0

0.6 25.0
20.0
0.4 15.0
10.0
0.2
5.0
0.0 0.0
CK
SSP1
SSP2
RP1
RP2
CM1
CM2
PE1
PE2
SM1
SM2
PM1
PM2

CK
SSP1
SSP2
RP1
RP2
CM1
CM2
PE1
PE2
SM1
SM2
PM1
PM2
Fig. 4. Fe (A), Mn (B), Cu (C) and Zn (D) concentration in plants with soil amendments.

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