phytoextraction of heavy metals from contaminated soil by co-cropping with chelator application and...
TRANSCRIPT
This article was downloaded by: [University of Hong Kong Libraries]On: 28 April 2013, At: 06:58Publisher: Taylor & FrancisInforma Ltd Registered in England and Wales Registered Number: 1072954 Registeredoffice: Mortimer House, 37-41 Mortimer Street, London W1T 3JH, UK
International Journal ofPhytoremediationPublication details, including instructions for authors andsubscription information:http://www.tandfonline.com/loi/bijp20
PHYTOEXTRACTION OF HEAVY METALSFROM CONTAMINATED SOIL BY CO-CROPPING WITH CHELATOR APPLICATIONAND ASSESSMENT OF ASSOCIATEDLEACHING RISKZ. B. Wei a , X. F. Guo a , Q. T. Wu a , X. X. Long a & C. J. Penn ba College of Natural Resources and Environment, Key Laboratoryof Ecological Agricultural of Ministry of Agriculture of China, SouthChina Agricultural University, Guangzhou, Chinab Department of Plant and Soil Sciences, Oklahoma State University,Stillwater, Oklahoma, USAVersion of record first published: 18 May 2011.
To cite this article: Z. B. Wei , X. F. Guo , Q. T. Wu , X. X. Long & C. J. Penn (2011):PHYTOEXTRACTION OF HEAVY METALS FROM CONTAMINATED SOIL BY CO-CROPPING WITHCHELATOR APPLICATION AND ASSESSMENT OF ASSOCIATED LEACHING RISK, International Journal ofPhytoremediation, 13:7, 717-729
To link to this article: http://dx.doi.org/10.1080/15226514.2010.525554
PLEASE SCROLL DOWN FOR ARTICLE
Full terms and conditions of use: http://www.tandfonline.com/page/terms-and-conditions
This article may be used for research, teaching, and private study purposes. Anysubstantial or systematic reproduction, redistribution, reselling, loan, sub-licensing,systematic supply, or distribution in any form to anyone is expressly forbidden.
The publisher does not give any warranty express or implied or make any representationthat the contents will be complete or accurate or up to date. The accuracy of anyinstructions, formulae, and drug doses should be independently verified with primarysources. The publisher shall not be liable for any loss, actions, claims, proceedings,demand, or costs or damages whatsoever or howsoever caused arising directly orindirectly in connection with or arising out of the use of this material.
International Journal of Phytoremediation, 13:717–729, 2011Copyright C© Taylor & Francis Group, LLCISSN: 1522-6514 print / 1549-7879 onlineDOI: 10.1080/15226514.2010.525554
PHYTOEXTRACTION OF HEAVY METALSFROM CONTAMINATED SOIL BY CO-CROPPINGWITH CHELATOR APPLICATION AND ASSESSMENTOF ASSOCIATED LEACHING RISK
Z. B. Wei,1 X. F. Guo,1 Q. T. Wu,1 X. X. Long,1 and C. J. Penn2
1College of Natural Resources and Environment, Key Laboratory of EcologicalAgricultural of Ministry of Agriculture of China, South China AgriculturalUniversity, Guangzhou, China2Department of Plant and Soil Sciences, Oklahoma State University, Stillwater,Oklahoma, USA
Phytoextraction using hyperaccumulating plants is generally time-consuming and requiresthe cessation of agriculture. We coupled chelators and a co-cropping system to enhancephytoextraction rates, while allowing for agricultural production. An experiment on 1 m3
lysimeter beds was conducted with a co-cropping system consisting of the hyperaccumulatorSedum alfredii and low-accumulating corn (Zea Mays, cv. Huidan-4), with addition of amixture of chelators (MC), to assess the efficiency of chelator enhanced co-crop phytoex-traction and the leaching risk caused by the chelator. The results showed that the additionof MC promoted the growth of S. alfredii in the first crop (spring-summer season) andsignificantly increased the metal phytoextraction. The DTPA-extractable and total metalconcentrations in the topsoil were also reduced more significantly with the addition of MCcompared with the control treatments. However, mono-cropped S. alfredii without MC wasmore suitable for maximizing S. alfredii growth and therefore phytoextraction of Zn andCd during the autumn-winter seasons. No adverse impact to groundwater due to MC ap-plication was observed during the experiments with three crops and three MC applications.But elevated total Cd and Pb concentrations among subsoils compared to the initial subsoilconcentrations were found for the co-crop + MC treatment after the third crop.
KEY WORDS: phytoextraction, co-crop, mixture of chelators, Sedum alfredii, Zea mays,leaching risk
INTRODUCTION
The contamination of soils with heavy metals is a major environmental concern inmany parts of the world due to rapid industrialization, increased urbanization, modernagricultural practices, and inappropriate waste disposal methods. Excessive accumulationof heavy metals in agricultural soils has led to elevated heavy metal uptake by crops,affecting food quality and safety (Wang et al. 2001), and potentially causing hazards tohuman health through the food chain.
Address correspondence to Qi-Tang Wu, College of Natural Resources and Environment, South ChinaAgricultural University, 510642 Guangzhou, China. E-mail: [email protected]
717
Dow
nloa
ded
by [
Uni
vers
ity o
f H
ong
Kon
g L
ibra
ries
] at
06:
58 2
8 A
pril
2013
718 Z. B. WEI ET AL.
Heavy metal contaminated soils can be remediated by chemical, physical, or biologi-cal techniques. Chemical and physical treatments such as chemical washing and incinerationirreversibly affect soil properties, destroy biodiversity, and may render the soil useless as amedium for plant growth. These remediation methods can be costly. Glass (2000) summa-rizes the cost of different remediation technologies, concluding that phytoextraction is costeffective compared with physicochemical technologies, but is generally time-consuming(Baker et al. 2000; Robinson et al. 1998). It would not be economically feasible to phytore-mediate agricultural soils contaminated with heavy metals as the farmer would be requiredto stop agricultural production for five years or more. Hence, improvement of metal accu-mulation in hyperaccumulating plant shoots is a prerequisite to improving feasibility.
To enhance phytoextraction rates, chelate-enhanced metal phytoextraction has beenstudied (Nowack, Schulin, and Robinson 2006). Among several complexing agents reportedin literature for chelant-enhanced phytoextraction, the synthetic chelator ethylenediaminete-traacetic acid (EDTA) has been most investigated. However, the slow degradation rate andlong persistence of EDTA in soil potentially increases the metal leaching risk which maycause groundwater contamination (Lombi et al. 2001; Meers et al. 2005; Wu et al. 2004;Romkens et al. 2002; Chen, Li, and Shen 2004), and EDTA is relatively expensive. There-fore, more biodegradable and less expensive enhancing additives have been investigated.A more biodegradable synthetic chelant, S,S-ethylenediaminedisuccinic acid (EDDS), wasidentified as a possible alternative to EDTA (Tandy et al. 2004), but it is still expensive.The use of a mixture of chelators (MC), including monosodium glutamate waste liquid(MGWL), citric acid, and EDTA at a mole ratio of 1:10:2, has also been investigated (Wu,Deng, and Long 2004). Advantages for using this MC are that it is less expensive andcauses less metal leaching from the soils into the underlying groundwater than EDTA (Guoet al. 2008).
Agronomic measures can also be used to improve phytoextraction rates. For example,appropriate fertilizer application is necessary for phytoremediation and could enhance theefficiency of metal removal from contaminated soils (Monsant, Tang, and Baker 2008;Robinson et al. 1998; Schwartz, Echevarria, and Morel, 2003). Utilizing a Co-croppingsystem of Thlaspi caerulescens (hyperaccumulator) with Thlaspi arvense increased thegrowth of the non-hyperaccumulator and reduced its Zn uptake and in contrast increasedZn uptake of the hyperaccumulator (Whiting et al. 2001). Recently, a co-planting system(growing a metal hyperaccumulator plant alongside a low metal accumulating crop) wasintroduced to simultaneously phytoextract heavy metals from contaminated sewage sludge,while also growing an agricultural crop (Liu, Wu, and Bank 2005). Results showed thatthis co-planting system effectively removed heavy metals from the sewage sludge by thehyperaccumulator plant while the harvested agricultural crop met the Chinese standard foranimal feeds (Liu, Wu and Bank 2005; Wu et al. 2007). The co-planting system, comprisedof a Zn and Cd hyperaccumulator (S. alfredii) and a low-accumulating crop (Z. mays), wasestablished in a paddy soil that was historically irrigated with Pb and Zn contaminatedmining wastewaters. At the same time the effects of the MC were investigated in regardto plant growth and phytoextraction efficiency. The combination of the co-planting systemwith the MC enhanced not only the removal of heavy metals from the contaminated soils butcould also produce safe corn for animal feed, allowing farmers to continue their agriculturalactivities (Wu, Wei, and Ouyang 2007). Continued agricultural production of safe animalfeeds from contaminated soils is necessary considering the limited arable land in China andtime required for phytoremediating metal-contaminated soils.
Dow
nloa
ded
by [
Uni
vers
ity o
f H
ong
Kon
g L
ibra
ries
] at
06:
58 2
8 A
pril
2013
CO-CROP PHYTOEXTRACTION WITH CHELATOR APPLICATION AND LEACHING RISK 719
However the previous experiments were conducted for only one season, a singleapplication of MC, and did not include monitoring of leachate. In regard to practicalphytoremediation cases, several crops or several years are generally needed to achieve theremediation goal. The objectives of this lysimeter plot experiment was to assess metalremoval efficiency of chelator-enhanced phytoextraction within a continuous cropped co-planting system and to investigate the potential leaching risk during phytoextraction.
MATERIALS AND METHODS
Soil
The contaminated soil utilized was collected from a paddy field at the Lechang Leadand Zinc Mining Site (25◦07′ N; 113◦22′ E) in Lechang District, Guangdong Province,China. The soil properties are shown in Table 1. Cd, Zn, and Pb exceeded the limitsspecified in the Chinese national standards for soils (GB15618-1995).
Plants and Chemical Chelators
Two plant species, S. alfredii and Z. mays, were used in the experiments. S. alfrediiwas obtained from an old Pb and Zn mining area in Zhejiang Province, China and waspropagated before transplanting in our experiments. Z. mays (var.Yunshi-5) is a low metal-accumulating cultivar with low concentrations of heavy metals in its grains (Samake et al.2003).
The chelator used in our experiments was a mixture of chelators (MC) that comprisedmonosodium glutamate waste liquid (MGWL), citric acid and EDTA at a mole ratio of1:10:2 (Wu, Deng, and Long 2004; Wu et al. 2006). The citric acid and EDTA wereanalytical reagent grade chemical reagents and the MGWL was purchased from GuangzhouGlutamate Factory with a residual monosodium glutamate concentration of 0.8 mol L−1,pH of 6.3, and chemical oxygen demand of 41,668 mg L−1.
Table 1 Selected properties of the soil used in this study (mean ± standard error)
Topsoil Subsoil
pH 6.59 ± 0.05 5.65 ± 0.03TN (g kg−1) 2.61 ± 0.13 0.52 ± 0.07TP (g kg−1) 0.69 ± 0.04 0.64 ± 0.06TK (g kg−1) 11.66 ± 0.62 2.70 ± 0.13OM (g kg−1) 38.68 ± 1.28 11.68 ± 0.76Total Fe (g kg−1) 42.99 ± 1.62 19.31 ± 0.51Total Metal (mg kg−1)
Zn 810 ± 11(250)† 50.3 ± 4.3Cd 1.55 ± 0.02(0.3) 0.049 ± 0.007Pb 861 ± 9(300) 102 ± 15
DTPA–Extractable Metal (mg kg−1)Zn 80.5 ± 0.78 —Cd 0.634 ± 0.0036 —Pb 341 ± 1.8 —
†Values in parentheses are limits set for heavy metal concentrations among agricultural soils with pH 6.5 to7.5 according to the Chinese National Standard GB15618-1995.
Dow
nloa
ded
by [
Uni
vers
ity o
f H
ong
Kon
g L
ibra
ries
] at
06:
58 2
8 A
pril
2013
720 Z. B. WEI ET AL.
Treatments and Experimental Design
The study was conducted in a series of custom-built square cement beds (inner size:0.9 m × 0.9 m × 0.9 m) in the open air. A 10 cm diameter hole in the bottom of thebed was used to facilitate drainage. The beds were filled with 20 cm of the heavy metalcontaminated soils (186 kg dry soil) overlying 60 cm of local subsurface soil (a lateric redsoil).
The planting treatments were as follows: Z. mays (mono-crop; 6 plants/bed), S. alfredii(mono-crop; 81 plants/bed), co-cropped Z. mays and S. alfredii (co-crop), and co-croppingamended with MC (Co-crop+MC). The plant population in the co-crop treatments werethe same as the mono-crop and the two species were mixed together within a bed. Therewere three replicates of each of the four treatments. All treatment beds were randomlydistributed in the field. S. alfredii was propagated vegetatively and transplanted as cuttingswhile Z. mays was seeded directly into the soil.
Three full growth cycles were completed for each treatment:First crop: On April 5, 2008, Z. mays and S. alfredii were planted in the beds in
accordance with the above description. All plots were fertilized with a compound fertilizer(N: P2O5: K2O = 15:15:15, from Batian Fertilizer Company) at a rate of 14 g plot−1
(meaning 2.6 g N, P2O5 and K2O per m2) one month after the planting. Two weeks beforeharvest (at June 15 and 21), two MC additions were applied to the co-crop+MC treatmentsat a rate of 5 mmol MC kg−1 soil at each application on the basis of the surface 0–20 cmsoil (i.e., 186 kg dry soil). The MC was dissolved in water and sprinkled on the soil surfaceby means of a watering can. Three months after planting (July 5), the shoots of maize andS. alfredii were harvested successively by cutting and 500 g of the 0–20 cm topsoil wassampled from each bed. The drainage water was sampled before and after MC applicationswhen rainfall was sufficient to naturally generate more than 200 ml leaching water foranalysis of heavy metals.
Second crop: On July 8, 2008, only Z. mays were planted (6 plants/bed), because S.alfredii does not grow in summer (July to September) in Guangdong Province, China. TheZ. mays was fertilized in the same manner to the first crop and harvested on September 24.
Third crop: Z. mays and S. alfredii (i.e., all treatments) were planted on September27 as described for the first crop. On January 15, 2009, MC was applied to the co-crop+MCtreatment at a rate of 5 mmol MC kg−1 soil. The plants were fertilized twice in the samemanner as the previous crops. The Z. mays was harvested on January 17, 2009 and the S.alfredii plants were harvested on March 27, 2009. After harvest, topsoil (0–20 cm) andsubsoil (30–50 cm) were respectively sampled from each plot.
Sample Treatments and Analysis
Plants were dried at 70◦C for 72 h to obtain the dry weights. The oven-dried materialswere finely ground in an automatic agate mill. The metals in the plants were analyzedaccording to Chinese standard methods (CAPM 1998). Plant samples were heated tosmokeless on a hotplate then dry combusted in muffle furnace at 500◦C for 5.5 h. The ashwas then dissolved in 2 ml 6 mol L−1 HCl and was transferred to a volumetric flask anddiluted to a final volume of 25 ml for total metal analysis.
The soil samples were air-dried and sieved. Soil pH was measured at a soil to waterratio of 1:2.5. Samples were digested with HF–HClO4–HNO3 for total heavy metal de-termination (Lu 2000). The DTPA (diethylenetriaminepentaacetic acid) extractable metals
Dow
nloa
ded
by [
Uni
vers
ity o
f H
ong
Kon
g L
ibra
ries
] at
06:
58 2
8 A
pril
2013
CO-CROP PHYTOEXTRACTION WITH CHELATOR APPLICATION AND LEACHING RISK 721
which approximates the phytoavailable metal fraction were extracted with 0.005 mol L−1
DTPA at pH 7.3 (Lu 2000). Metals in the solutions were analyzed by either flame or fur-nace Atomic Absorption Spectrometry (Hitachi Z-2300, Z-2700), depending on the metalconcentrations.
Data Analysis
Means and standard deviations were calculated for the three replicates using MicrosoftExcel. Statistical analysis was performed with SAS (r) Proprietary Software Release 8.1(SAS Institute Inc., Cary, NC, USA). Data were analyzed using ANOVA with the Duncantest (α = 0.05).
RESULTS AND DICUSSION
Plant Growth
There were no visible symptoms of heavy metal toxicity in Z. mays during germinationand growth. Grain and shoot yield of Z. mays (Table 2) indicated significant differences (atα = 0.05) among treatments. Addition of MC significantly enhanced growth of Z. mays.The yield of grains in the Co-crop +MC treatment was the highest for all three crops. Drymatter yield of stems and leaves in both the second and the third crops for the Co-crop+MCtreatment were also the highest. This may be due to increased nutrient availability by MCor because, MGWL, contains N, P, and K nutrients (Guo et al. 2008).
Mono-cropped Z. mays showed no statistically significant difference from the Z. maysco-cropped with S. alfredii (Table 2), indicating that the biomass production of Z. mays wasnot affected by co-cropping with S. alfredii.
S. alfredii was only planted for the first and third crops, as it cannot grow in Guang-dong Province between July and September. Therefore, all treatments listed under “sec-ond crop” describes Z. mays with no S. alfredii. This explains why “mono-crop” and“co-crop” treatments are nearly the exact yield. In the first crop, the Co-crop + MCtreatment significantly increased the biomass of the shoots of S. alfredii (Table 3). Thedry matter yield of the shoots of S. alfredii for the Co-crop +MC treatment was 1.2times higher than that of the Co-crop treatment and the mono-cropped S. alfredii treat-ment. Our previous studies during the same season demonstrated that the combination
Table 2 Grain and shoot yields of different parts of Z. mays grown under a mono-crop, co-crop (with S. alfredii),and co-crop system with a mixture of chelators (MC) treatments (g lysimeter−1)
Grains Stems and leaves
First Second Third First Second Thirdcrop crop† crop crop crop crop
Mono-crop 58.03 ± 27.0a‡ 63.86 ± 14.40b 16.22 ± 11.07b 240.1 ± 35.6a 194.1 ± 29.8a 40.35 ± 5.69bCo-crop 114.6 ± 22.6a 62.36 ± 16.32b 14.96 ± 4.72b 304.0 ± 18.1a 198.5 ± 40.0a 43.99 ± 1.86bCo-crop + MC 132.5 ± 26.1a 114.5 ± 10.2a 198.6 ± 35.9a 286.7 ± 26.7a 305.6 ± 22.1a 158.6 ± 4.8a
† Second crop does not have a co-crop due to the lack of growth of S. alfredii during summer.‡The values in the table are mean ± standard error; within a column, values followed by the same letter are not
significantly different from each other at α = 0.05.
Dow
nloa
ded
by [
Uni
vers
ity o
f H
ong
Kon
g L
ibra
ries
] at
06:
58 2
8 A
pril
2013
Tabl
e3
Yie
lds
(gly
sim
eter
−1)
and
met
alco
ncen
trat
ions
(mg
kg−1
)in
shoo
tsof
S.al
fred
iigr
own
unde
ra
mon
o-cr
op,c
o-cr
op(w
ithZ
.may
s),a
ndco
-cro
psy
stem
with
am
ixtu
reof
chel
ator
s(M
C)
Firs
tcro
pT
hird
crop
Yie
ldZ
nC
dPb
Yie
ldZ
nC
dPb
Mon
o-cr
op28
.6±
1.8b
†53
72±
205b
30.5
4±
2.54
a22
.28
±0.
84a
124.
5±
5.0a
8820
±43
4a81
.61±
12.4
9a28
.99±
2.33
aC
o-cr
op29
.0±
0.9b
7996
±42
8a48
.30±
2.17
a32
.96
±2.
01a
72.1
±4.
9b87
28±
942a
67.1
6±
14.0
6a31
.58±
5.35
aC
o-cr
op+M
C35
.2±
1.1a
7776
±63
8a47
.09±
9.33
a37
.49
±7.
78a
31.7
±10
.8c
7906
±77
2a72
.39±
22.2
7a29
.02±
2.52
a
†The
valu
esin
the
tabl
ear
em
ean
±st
anda
rder
ror;
with
ina
colu
mn,
valu
esfo
llow
edby
the
sam
ele
tter
are
nots
igni
fican
tlydi
ffer
entf
rom
each
othe
rat
α=
0.05
.
722
Dow
nloa
ded
by [
Uni
vers
ity o
f H
ong
Kon
g L
ibra
ries
] at
06:
58 2
8 A
pril
2013
CO-CROP PHYTOEXTRACTION WITH CHELATOR APPLICATION AND LEACHING RISK 723
of co-cropping and MC also increased the biomass of S. alfredii shoots (Wu, Wei, andOuyang 2007).
However, in the third crop, the dry matter production of S. alfredii was significantlyreduced by the addition of MC and co-cropping with Z. mays (Table 3). Two days afterMC addition into the soil there were numerous brown dots on the leaves of S. alfredii,indicating phytotoxicity from EDTA added with the MC application, because this plant istolerant to Cd, Pb, and Zn and other heavy metals were not high in the studied soil. Thedry weight of S. alfredii shoots in the Co-crop+MC treatment was significantly lower thanthat of the Co-crop treatment, which was lower again than the mono-cropped S. alfredii.These results reveal that S. alfredii is more sensitive to EDTA contained in MC and duringthe autumn-winter-spring seasons, the application of MC at the experimental dose was notsuitable for S. alfredii. The co-planting system decreased the dry matter weight of S. alfrediiwhen the sunlight was not intense (January to March).
Further studies are needed to determine why the addition of MC reduced S. alfrediigrowth in the third crop (during the cold season) and but not in summer.
Metal Concentrations in Plant Tissue
S. alfredii is a Zn hyperaccumulator native to China (Yang, Long, and Ni 2002)and has an ability to hyperaccumulate not only Zn but also Cd (Yang et al. 2004; Yeet al. 2003). Mono-cropped S. alfredii showed no statistically significant differences inthe metal concentrations in shoots from the co-cropped S. alfredii with or without MC,with the exception of the Zn concentration in first crop (Table 3). In this exception, theZn concentrations in S. alfredii shoots for the Co-crop and Co-crop+MC treatments werehigher than the mono-cropped S. alfredii. This is consistent with the observations by Whitinget al. (2001) where the hyperaccumulation of Zn by Thlaspi caerulescens was enhanced bythe co-cropped Thlaspi arvense.
The Zn and Cd concentrations in S. alfredii shoots were higher in the third crop thanin the first crop (Table 3). This may be due to the longer growing time for the plant duringthe autumn-winter-spring season than the spring-summer season. The high concentrationsof Zn and Cd in S. alfredii increased not only its phytoextraction efficiency but also thefeasibility for metal recovery. The high Zn and Cd concentration suggests that S. alfrediiis superior to the Cd hyper-accumulator, Brassica napus, which has also been co-croppedwith Zea mays in Southern China but contained only 10–20 mg kg−1 Cd in dry biomass(Selvam and Wong 2009).
The concentrations of Cd, Pb, and Zn in corn grains were not significantly differentamong treatments. The concentrations of Zn in the corn grains of the three crops werevaried from 33.5 mg kg−1 to 43.5 mg kg−1 and all below the standard limit for food basedon the Tolerance Limit for Heavy Metals in Food of China (GB2762-2005: Zn < 50 mgkg−1). The Cd and Pb concentrations varied from 0.14 mg kg−1 to 0.37 mg kg−1 and from0.07 mg kg−1 to 0.77 mg kg−1 respectively (data not shown), and exceeded the Chinesefood standard for corn (GB2762-2005: Cd < 0.1 mg kg−1, Pb < 0.2 mg kg−1), However,the Codex Committee has proposed maximum levels for Cd in rice grains of 0.4 mg kg−1
(CCFAC 2004). All corn grains produced satisfied the Chinese standard for animal feeds(GB13078-2001) concerning heavy metal contents (Cd < 0.5 mg kg−1, Pb < 5 mg kg−1). Astandard limit for Zn has not been established because animal feeds need a relatively highconcentration of this trace element. The concentration of Zn in the corn grains produced inour experiments is within the recommended range for animal feeds (45–80 mg kg−1) (Coic
Dow
nloa
ded
by [
Uni
vers
ity o
f H
ong
Kon
g L
ibra
ries
] at
06:
58 2
8 A
pril
2013
724 Z. B. WEI ET AL.
and Coppenet 1989). This indicates that the corn grains are suitable as feed for animalnutrition. Our study further revealed that metal concentrations in the stems and leaves of Z.mays were still suitable to be applied to agricultural soils according to Chinese agriculturalstandard NY 525-2002 (Cd < 3 mg kg−1, Pb < 100 mg kg−1). Another reason for choosingthe low metal-accumulating Z. mays in the phytoremediation of heavy metal contaminatedsoils is that this plant species has a large biomass and can be an energy crop for producingbiofuel from its corn grains (Altm, Cetinkava, and Yucesu 2001).
Metal Phytoextraction
Table 4 shows the total uptake of Zn, Cd, and Pb by aerial plant parts with differenttreatments from the first and third crops. In the case of the mono-cultures, Zn and Cduptake by S. alfredii was much higher than the uptake by Z. mays. Zn and Cd removal bythe co-crop was mostly due to S. alfredii.
In the first crop, the co-cropped S. alfredii increased the uptake of Zn, Cd, and Pbby 52%, 59%, and 51%, respectively, compared with mono-cropped S. alfredii. The MCaddition also increased the uptakes of Zn, Cd, and Pb by 17%, 17%, and 36%, respectively,compared with co-cropping alone. This is consistent with previous observations that theeffects of co-planting and the use of MC should be additive and the two techniques weresuitable for combination (Wu, Wei, and Ouyang 2007). During the first crop, co-crop+MCtreatment had the highest total uptake of Zn, Cd and Pb (Table 4), meaning that, in thesummer, the Co-crop+MC treatment has the greatest effectiveness at removing Zn, Cd,and Pb from the contaminated soils. However, during the third crop (in winter), the co-cropping and MC addition significantly reduced metal uptake by S. alfredii shoots (Table 4),mainly due to lower biomass production (Table 3). Hence, in winter in South China, mono-cropped S. alfredii is preferred for the phytoextraction of Zn and Cd from contaminatedsoils. Furthermore, considering the harvest problems, co-cropping practice maybe onlysuitable for developing counties, it maybe cost prohibitive in developed countries withoutdeveloping appropriate machines.
Heavy Metal Concentrations in Soils After Harvest
Changes in heavy metal concentrations in topsoil among each treatment after harvestare shown in Table 5. The greatest reduction in total topsoil Cd and Pb (relative to initialconcentrations, 1.55 and 861 mg kg−1, respectively) occurred for the Co-crop + MCtreatment, which was significantly different from the other treatments. Reduction in topsoiltotal metal concentrations by the Co-crop + MC treatment were 6%, 38%, and 12% ofinitial (i.e., pre treatment) topsoil Zn, Cd, and Pb, respectively. The greater reduction inCd and Pb from the topsoil in the Co-crop + MC treatment compared with mono-croppedand co-cropped S. alfredii is attributed to the leaching process which was enhanced by MCaddition. Evidence is found in the observation that the highest phytoextraction of Cd wasnot the Co-crop + MC treatment (Table 4) and because Pb removal by phytoextractionwas less than 0.1% of the total soil Pb for all treatments. Further evidence is found in theelevated total Cd and Pb concentrations among subsoils compared to the initial subsoilconcentrations (Tables 1 and 5).
The DTPA-extractable metal concentrations in topsoil after the third harvest areshown in Table 5. The concentrations of DTPA-extractable Zn, Cd, and Pb were significantlyreduced by the combination of co-planting + MC after the third crop compared to the
Dow
nloa
ded
by [
Uni
vers
ity o
f H
ong
Kon
g L
ibra
ries
] at
06:
58 2
8 A
pril
2013
Tabl
e4
Indi
vidu
alan
dcu
mul
ativ
eZ
n,C
dan
dPb
tota
lupt
ake
bypl
ants
unde
rdif
fere
ntcr
oppi
ngsy
stem
s.C
o-cr
opis
S.al
fred
iian
dZ
.may
s;M
Cin
dica
tes
appl
icat
ion
ofa
mix
ture
ofch
elat
ors.
All
valu
esex
pres
sed
asm
gly
sim
eter
−1
1stc
rop
3rd
crop
Tota
l
Zn
Cd
PbZ
nC
dPb
Zn
Cd
Pb
S.al
fred
ii15
3.1±
5.8b
†0.
882±
0.12
9b0.
636
±0.
033b
1097
±63
a10
.11±
1.51
a3.
626±
0.39
4a12
50±
580a
11.0
0±
1.52
a4.
262±
0.38
9aZ
.may
s31
.14±
9.08
c0.
119±
0.01
2c1.
165
±0.
123b
10.1
5±
2.65
d0.
059±
0.00
4c0.
262±
0.05
7c41
.29
±11
.2d
1.17
8±
0.01
3c1.
428±
0.14
5bC
o-cr
op27
0.1±
21.9
a1.
523±
0.09
1a2.
369
±0.
043a
641.
8±
95.6
b4.
900±
1.13
4b2.
515±
0.47
3ab
911.
9±
118b
6.42
3±
1.21
7b4.
884±
0.50
6aC
o-cr
op+
MC
306.
6±
18.7
a1.
792±
0.30
7a3.
093
±0.
497a
299.
2±
106.
5c2.
843±
1.38
5bc
1.95
5±
0.33
5b60
5.5
±12
3c4.
635
±1.
692b
5.04
8±
0.77
6a
†The
valu
esin
the
tabl
ew
ere
mea
n±
stan
dard
erro
r;w
ithin
aco
lum
n,va
lues
follo
wed
byth
esa
me
lette
rar
eno
tsig
nific
antly
diff
eren
tfro
mon
ean
othe
rat
α=
0.05
.
725
Dow
nloa
ded
by [
Uni
vers
ity o
f H
ong
Kon
g L
ibra
ries
] at
06:
58 2
8 A
pril
2013
726 Z. B. WEI ET AL.
Table 5 Total heavy metal concentrations in topsoil and subsoil and DTPA-extractable metals in the topsoil afterthe harvest of the 3rd crop under different cropping systems. Co-crop is S. alfredii and Z. mays; MC indicatesapplication of a mixture of chelators. All values expressed as mg kg−1
Zn Cd Pb
Total metal in topsoilS. alfredii 815.8 ± 29.6a† 1.432 ± 0.013a 891.1 ± 21.5aZ. mays 781.6 ± 31.9a 1.423 ± 0.035a 888.9 ± 12.8aCo-crop 727.9 ± 47.2a 1.441 ± 0.099a 829.2 ± 43.8abCo-crop +MC 756.5 ± 41.4a 0.951 ± 0.091b 754.5 ± 25.2b
Total metal in subsoilS. alfredii 34.49 ± 5.30b 0.025 ± 0.003b 93.81 ± 47.03bZ. mays 39.06 ± 6.93b 0.030 ± 0.022b 80.59 ± 32.83bCo-crop 44.85 ± 7.82ab 0.050 ± 0.023b 117.9 ± 24.2abCo-crop + MC 63.89 ± 2.29a 0.418 ± 0.089a 204.2 ± 42.0a
DTPA-extractable metal in topsoilS. alfredii 84.87 ± 3.36a 0.5810 ± 0.0195a 354.6 ± 3.7aZ. may 80.83 ± 4.76a 0.5929 ± 0.0215a 355.4 ± 6.9aCo-crop 77.69 ± 3.71a 0.5508 ± 0.0057a 352.0 ± 4.0aCo-crop + MC 58.36 ± 3.34b 0.3280 ± 0.0187b 268.5 ± 12.1b
†The values in the table are mean ± standard error; within a column, values followed by the same letter are notsignificantly different from each other at α = 0.05.
other treatments, which is a similar trend to the total metal concentrations. Compare tothe initial values in Table 1, extractable Cd decreased for all the treatments, however,extractable Zn and Pb decreased significantly only for the Co-crop + MC treatment.DTPA-extractable pools of heavy metals are similar to EDTA/MC leachable pools andgreater than phytoextractable pools; the reductions after leaching or phytoextraction aregenerally more significant than that of the total metals in soil. For example, the decreasein DTPA-extractable Pb (relative to pre-treatment) with the addition of MC was 21%compared to a 12% decrease for total Pb. The decrease in DTPA-extractable Cd was about48% and greater than Zn and Pb, indicating Cd is more mobile than the other two elements.
Leaching of Metals
The heavy metals mobilized from the topsoil are leached into the subsoil and thenpotentially into groundwater. Leachate collected from 6 rain events at 80 cm below thesoil surface showed that heavy metal concentrations ranged from 0.03 to 0.79 mg L−1 forZn, from non-detectable to 0.003 mg L−1 for Cd and from non-detectable to 0.188 mgL−1 for Pb, respectively. The Zn, Cd concentrations in leachate were low, and meet theQuality Standards for Ground Water in China (GB/T 14848-93: Zn < 1 mg L−1, Cd <
0.01 mg L−1, Pb < 0.05 mg L−1) and the intervention values of the Dutch ReferenceFramework environmental guidance criteria (Zn: 0.8 mg L−1, Cd: 0.006 mg L−1, Pb:0.075 mg L−1) (Swartjes 1999). In regard to Pb, some values exceeded the limit values,however, the application of MC did not significantly increase Zn, Cd, and Pb concentrationsin the leachate from the deep soil layer compared with no MC treatments. Thereforethe high leachate Pb concentrations were not caused by MC application but from thesoil Pb contamination itself. This means that the metals mobilized from the topsoil (0–20 cm) were adsorbed by the subsoil. Subsoil analysis (30–50 cm) showed that the Co-crop
Dow
nloa
ded
by [
Uni
vers
ity o
f H
ong
Kon
g L
ibra
ries
] at
06:
58 2
8 A
pril
2013
CO-CROP PHYTOEXTRACTION WITH CHELATOR APPLICATION AND LEACHING RISK 727
+ MC treatment significantly increased total Cd, Pb, and Zn compared with mono-croptreatments (Table 5). Mono-crop subsoil metals concentrations were similar to the initialsoil concentrations (Table 1). Contin et al. (2007) showed that it is possible to enhance metalfixation in soil by using Fe (hydr) oxides, either native to the soil or added as ameliorants. Inour experiments, the deep soil layer is a lateric red soil, which is rich in Fe (80 to 170 g Fe2O3
per kg soil clay) and is classified as a Udic Ferralisol (Liu, Liu, and He 1993). This soil mayalso have variable positive charges and considerable fixation capacity for the heavy metal-chelator complexes (mainly negatively charged EDTA and citric acid to metal complexes)which help prevent the complexes from leaching into groundwater. This suggestion needsto be verified. In addition plant transpiration can reduce the downward movement of water(Zhao, Schulin, and Nowack 2007) and therefore reduce potential leaching of dissolvedmetals. For this experiment, the addition of MC significantly increased the corn growthin the second and third crops, which might limit metal leaching through the subsoil. Noincreased environmental impact on groundwater was observed when MC was applied tothe co-planted S. alfredii and Z. mays.
CONCLUSION
Co-cropping experiments in lysimeter plots showed that the addition of MC promotedgrowth in the first crop (during the spring-summer season), which significantly increasedmetal phytoextraction. During the winter-spring season, mono-cropped S. alfredii exhibitedbetter growth and phytoextraction of Zn and Cd compared to co-cropping with Z. mays.The addition of MC increased significantly the growth of Z. mays in the second and thirdcrops, producing more corn. The concentrations of DTPA extractable and total metals inthe topsoil decreased more with the addition of MC compared to without MC, relative toinitial topsoil concentrations. Potential adverse environmental impact to groundwater dueto increased leaching from MC application was not observed after three continuous cropsand three applications of MC. This may be due to adsorption of chelator-metal complexesby iron oxides which are abundant in the subsoil used in this study. However, further studiesare needed to identify the fixation capacity for heavy metals by the deep layer soil.
ACKNOWLEDGMENTS
This work was supported by the Natural Science Foundation of China (grant40801115, 41071306, U0833004), the National High-tech R&D Program (863 program)of PR China (grant 2008AA10Z405, 2007AA061001-3) and the Science and TechnologyProject of Guangdong Province (grant 2007A032303001, 2009B030802016).
REFERENCES
Altm R, Cetinkava S, Yucesu HS. 2001. The potential of using vegetable oil fuels as fuel for dieselengines. Energ Convers Manage. 42: 529–538.
Baker AJM, McGrath SP, Reeves RD, Smith JAC. 2000. Metal hyperaccumulator plants: A reviewof the ecology and physiology of a biological resource for phytoremediation of metal-pollutedsoils. In: Terry N, Banuelos G, eds. Phytoremediation of Contaminated Soil and Water. BocaRaton, FL: Lewis Publisher. p. 85–107.
Chen YH, Li XD, Shen ZG. 2004. Leaching and uptake of heavy metals by ten different species ofplants during an EDTA-assisted phytoextraction process. Chemosphere. 57: 187–196.
Dow
nloa
ded
by [
Uni
vers
ity o
f H
ong
Kon
g L
ibra
ries
] at
06:
58 2
8 A
pril
2013
728 Z. B. WEI ET AL.
Chinese Academy of Preventive Medicine (CAPM). 1998. National standards for food hygiene (VI).Beijing: Standards Press. p. 16–113, 217–262.
Codex Committee on Food Additives and Contaminants (CCFAC). 2004. Codex Alimentarius Com-mission Report of the 36th Session of the Codex Committee on Food Additives and Contami-nants. Rotterdam, the Netherlands. p. 25, 205.
Coic Y, Coppenet M. 1989. Les oligo-elements en agriculture et elevege. Paris: INRA Publications.p. 77–93
Contin M, Mondini C, Leita L, De Nobili M. 2007. Enhanced soil toxic metal fixation in iron (hydr)oxides by redox cycles. Geoderma. 140: 164–175.
Glass DJ. 2000. Economic potential of phytoremediation. In: Raskin IYA, Ensley BD, eds. Phytore-mediation of toxic metals. New York: John Wiley and Sons, Inc. p. 15–31.
Guo ZM, Wei ZB, Wu QT, Long XX. 2008. Chelator-enhanced phytoextraction coupling withsoil washing to remediate multiple–metals-contaminated soils. Pract Period Hazard, Toxic,Radioact Waste Manage. 12: 210–215.
Liu SA, Liu SJ, He YG. 1993. Guangdong soils. Beijing: Science Press. p. 67–190.Liu XM, Wu QT, Banks MK. 2005. Effect of simultaneous establishment of Sedum alfredii and Zea
mays on heavy metal accumulation in plants. Int J Phytorem. 7: 43–53.Lombi E, Zhao FJ, Dunham SJ, McGrath SP. 2001. Phytoremediation of heavy-metal contaminated
soils: Natural hyperaccumulation versus chemically enhanced phytoextraction. J Environ Qual.30: 1919–1926.
Lu RK. 2000. Analytical methods for soil and agrochemistry. Beijing: Agricultural Science andTechnology Press. p. 205–214.
Meers E, Ruttens A, Hopgood MJ, Samson D, Tack FMG. 2005. Comparison of EDTA and EDDS aspotential soil amendments for enhanced phytoextraction of heavy metals. Chemosphere. 58:1011–102.
Monsant AC, Tang C, Baker AJM. 2008. The effect of nitrogen form on rhizosphere soil pH and zincphytoextraction by Thlaspi caerulescens. Chemosphere. 73: 635–642.
Nowack B, Schulin R, Robinson BH. 2006. Critical assessment of chelant-enhanced metal phytoex-traction. Environ Sci Technol. 40: 5225–5232.
Robinson BH, Leblanc M, Petit D, Brooks RR, Kirkman JH, Gregg PEH. 1998. The potential ofThlaspi caerulescens for phytoremediation of contaminated soils. Plant Soil. 203: 47–56.
Romkens P, Bouwam L, Japenga J, Draaisma C, 2002. Potentials and drawbacks of chelate-enhancedphytoremediation of soils. Environ Pollut. 116: 109–121.
Samake M, Wu QT, Mo CH, Morel JL. 2003. Plants grown on sewage sludge in South China and itsrelevance to sludge stabilization and metal removal. J Environ Sci. 15: 622–662.
Schwartz C, Echevarria G, Morel JL. 2003. Phytoextraction of cadmium with Thlaspi caerulescens.Plant Soil. 249: 27–35.
Selvam A, Wong JWC. 2009. Cadmium uptake potential of Brassica napus cocropped with Brassicaparachinensis and Zea mays. J Hazard Mater. 167: 170–178.
Swartjes FA. 1999. Risk-based assessment of soil and groundwater quality in the Netherlands:Standards and remediation urgency. Risk Anal. 19: 1235–1249.
Tandy S, Bossart K, Mueller R, Ritschel J, Hauser L, Schulin R, Nowack B. 2004. Extraction of heavymetals from soils using biodegradable chelating agents. Environ Sci Technol. 38: 937–944.
Wang Q, Dong Y, Cui Y, Liu X. 2001. Instances of soil and crop heavy metal contamination in China.Soil Sediment Contam. 10: 497–510.
Whiting SN, Leake JR, McGrath SP, Baker AJM. 2001. Hyperaccumulation of Zn by Thlaspicaerulescens can ameliorate Zn toxicity in the rhizosphere of cocropped Thlaspi arvense.Environ Sci Technol. 35: 3237–3241.
Wu QT, Deng JC, Long XX. 2004. Mixed chelators enhancing zinc and cadmium uptake by hyper-accumulators and its applying method. China patent, ZL03140098.1.
Wu QT, Deng JC, Long XX, Morel JL, Schwartz C. 2006. Selection of appropriate organic additivesfor enhancing Zn and Cd phytoextraction by hyperaccumulators. J Environ Sci. 18: 1113–1118.
Dow
nloa
ded
by [
Uni
vers
ity o
f H
ong
Kon
g L
ibra
ries
] at
06:
58 2
8 A
pril
2013
CO-CROP PHYTOEXTRACTION WITH CHELATOR APPLICATION AND LEACHING RISK 729
Wu QT, Hei L, Wong JWC, Schwartz C, Morel JL. 2007. Co-cropping for phyto-separation of zincand Potassium from sewage sludge. Chemosphere. 68: 1954–1960.
Wu LH, Luo YM, Xing XR, Christie P. 2004. EDTA-enhanced phytoremediation of heavy metalcontaminated soil with Indian mustard and associated potential leaching risk. Agric EcosystEnviron. 102: 307–318.
Wu QT, Wei ZB, Ouyang Y. 2007. Phytoextraction of metal-contaminated soil by Sedum alfredii H:Effects of Ccelator and o-planting. Water, Air, Soil Pollut. 180: 131–139.
Yang XE, Long XX, Ni WZ. 2002. A new zinc hyperaccumulating plant species native to China.Chin Sci Bull. 47: 1003–1006.
Yang XE, Long XX, Ye HB, Calvert DV. 2004. Cadmium tolerance and hyperaccumulation in anew-Zn hyperaccumulating plant specie (Sedum alfredii Hance). Plant Soil. 259: 181–189.
Ye HB, Yang XE, He B, Long XX. 2003. Growth response and metal accumulation of Sedum alfrediito Cd/Zn complex-polluted ion levels. Acta Bot Sin. 45: 1030–1036.
Zhao LY, Schulin R, Nowack B. 2007. The effects of plants on the mobilization of Cu and Zn in soilcolumns. Environ Sci Technol. 41: 2770–2775.
Dow
nloa
ded
by [
Uni
vers
ity o
f H
ong
Kon
g L
ibra
ries
] at
06:
58 2
8 A
pril
2013