phytoremediation of heavy metal contaminated soil by jatropha curcas

Phytoremediation of heavy metal contaminated soil by Jatrophacurcas

Fang-Chih Chang • Chun-Han Ko •

Ming-Jer Tsai • Ya-Nang Wang • Chin-Yi Chung

Accepted: 9 August 2014 / Published online: 19 September 2014

� Springer Science+Business Media New York 2014

Abstract This study employed Jatropha curcas (bioen-

ergy crop plant) to assist in the removal of heavy metals

from contaminated field soils. Analyses were conducted on

the concentrations of the individual metals in the soil and

in the plants, and their differences over the growth periods

of the plants were determined. The calculation of plant

biomass after 2 years yielded the total amount of each

metal that was removed from the soil. In terms of the

absorption of heavy metal contaminants by the roots and

their transfer to aerial plant parts, Cd, Ni, and Zn exhibited

the greatest ease of absorption, whereas Cu, Cr, and Pb

interacted strongly with the root cells and remained in the

roots of the plants. J. curcas showed the best absorption

capability for Cd, Cr, Ni, and Zn. This study pioneered the

concept of combining both bioremediation and afforesta-

tion by J. curcas, demonstrated at a field scale.

Keywords Field contaminated soils � Phytoremediation �Jatropha curcas � Accumulation

Introduction

Global industrial activities, such as the mining and smelting

of metalliferous ores, electroplating, gas exhaust, energy

and fuel production, fertilizer and pesticide application, and

the generation of municipal waste, have resulted in the

release of large amounts of potentially toxic compounds

into the biosphere, among which are trace elements, like

cadmium, mercury, lead, arsenic, zinc and nickel, which are

collectively referred to as heavy metals (Lasat et al. 1998;

Kabata-Pendias 2001). Soil contamination often results

from these metals, and this is widespread across Taiwan,

where more than 500 sites are potentially contaminated by

localized pollution sources, with about 120 ha probably

requiring some remediation (Soil and Groundwater Reme-

diation Fund Management Board 2007). Soil contamination

by heavy metals (As, Cd, Cr, Cu, Pb, and Zn) is one of the

major environmental problems raising critical concerns for

both human health and ecosystems (Kabata-Pendias 2001)

due to their carcinogenic and mutagenic effects in animals

and humans (Baudouin et al. 2002).

Various physical, chemical, and biological processes are

currently being used to remediate metal-contaminated

soils. The cleanup of most of these soils is mandatory for

reclaiming the area and minimizing the entry of potentially

toxic elements into the food chain. There are certain plants

that can be used to treat many classes of contaminants,

including petroleum hydrocarbons, chlorinated solvents,

pesticides, metals, radionuclides, explosives and excess

nutrients. Phytoremediation is the in situ application of

plants and their associated microbes for environmental

cleanup. This technology makes use of the naturally

occurring processes by which plants and their microbial

rhizospheric flora degrade and sequester organic and

inorganic pollutants (Pilon-Smits 2005).

F.-C. Chang � M.-J. Tsai

The Experimental Forest, National Taiwan University,

Nan-Tou 55750, Taiwan

e-mail: [email protected]

C.-H. Ko (&) � M.-J. Tsai � Y.-N. Wang � C.-Y. Chung

School of Forestry and Resource Conservation, National Taiwan

University, Taipei 10617, Taiwan

e-mail: [email protected]

C.-H. Ko

Bioenergy Research Center, National Taiwan University,

Taipei 10617, Taiwan

123

Ecotoxicology (2014) 23:1969–1978

DOI 10.1007/s10646-014-1343-2

Despite its obvious advantages, the effectiveness of

phytoremediation must be confirmed to validate its use in

practical remediation. Such criteria have the ability to

remove or neutralize contaminants and time effectiveness

need to be evaluated. This technology depends on the level

and depth of soil contamination, the types of metals and

their chemical forms, the uptake capability of the plants

and their ability to tolerate metal accumulation without

phytotoxic effects, the biomass production capacity of the

harvested crop and the final level of heavy metals in the

soil to be considered remediated (McGrath 1998; Yadav

et al. 2010). Previous studies have shown that Cr and Pb

are not easily transferred to aerial plant biomass as they

are mainly stored in root cells (Mellem et al. 2009; Tiwari

et al. 2009; Yu et al. 2010), whereas Zn is easily accu-

mulated in green tissues like leaves (Probst et al. 2009;

Liu et al. 2011). Additionally, this study is the first to

report the bioremediation by Jatropha curcas for heavy

metal contaminated soils in a field scale. The other two

studies were conducted in pot cultures in combination

with fly ashes (Jamil et al. 2009) and dairy sludge (Yadav

et al. 2009).

This study employed J. curcas to assist in the removal of

heavy metals from contaminated soils on a field scale (a

derelict paddy field in Chang-Hwa city, Taiwan). J. curcas

is a flowering plant in the Euphorbiaceae. It is cultivated in

tropical and subtropical regions around the world,

becoming naturalized in some areas (USDA 2008). J.

curcas seeds contain 27–40 % oil that can be processed to

produce a high-quality biodiesel fuel, usable in a standard

diesel engine (Achten et al. 2007). Afforestation by J.

curcas can also contribute to carbon sequestration.

Phytoremediation employs on-site plants to take up heavy

metals and to prevent their further transport. The heavy

metal contents of roots, stems, and leaves for each species

were sampled and analyzed by ICP-AES. The enrichment

coefficient (EC) and transfer factor (TF) of heavy metals

for each species were also compared.

Materials and methods

Study sites and J. curcas description

The soil used in this study was taken from an area located

in Chang-Hwa City, where polluted of heavy metals many

years. An area of about 6,667 m2 located in the center of

the study site was chosen for field trials and sampling, as

shown in Fig. 1. Based on a previous characterization of

the site, it was observed that the soil was mainly polluted

with Cd, Pb and Zn. Ten soil samples were collected at

depths of 0–30 cm in the locations of the polluted area.

Plant samples were collected from several different places.

The 800 J. curcas plants selected for the study were

planted on the experimental site in July 2006. The planting

density of J. curcas was about 0.12 plant m-2.

Jatropha curcas grows in tropical and subtropical

regions. The flowers only develop terminally (at the end of

a stem), so a good ramification (plants presenting many

branches) produces the greatest amount of fruit. The use of

pesticides is not necessary due to the inherent pesticidal

and fungicidal properties of the plant. J. curcas starts

yielding from 9 to 12 months of age; the best yields are

obtained after 2–3 years.

Fig. 1 The study site located in Chang-Hwa City

1970 F.-C. Chang et al.

123

Contaminated soil characterization

Soil samples were collected at 0–30 cm depth in July 2006,

January 2008, and July 2008, kept at 4 �C before dying.

Soil samples were dried in an oven at 105 �C for 24 h, then

crushed and sieved to 2 mm. Soil pH was determined with

a glass electrode in distilled water and in soil suspensions

at a 2:1 soil to liquid ratio. Total organic carbon (TOC) was

analyzed by the Walkly-Black method. Available phos-

phorus (Pava) was determined by UV/Vis spectrophotom-

etry on sodium bicarbonate/sodium hydroxide soil extracts

according to the Olsen method. To determine the total

contents of heavy metals, dry soil samples were subjected

to microwave assisted digestion with a Suprapure�

HNO3:H2O2:HCl mixture (7:1:1 v/v). The total concen-

trations of heavy metals in soil were determined using

inductively coupled plasma atomic emission spectroscopy

(ICP-AES).

Metal contents in plant samples

Plant tissues (leaves, stems and roots) of J. curcas were

collected from contaminated soil in January 2008 and July

2008. Five J. curcas samples were analysed, originating

from different randomly chosen trees. Plant tissues were

carefully washed with deionized water to eliminate puta-

tive metallic surface contamination. All plant tissues were

first dried in an oven at 70 �C for 72 h. Stems and roots

were cut into 1-mm pieces and ground into powder using

an acid-washed porcelain mortar and pestle. Subsequently,

0.2 g of leaves, stems, or roots was fully mineralized with

2 ml H2O2 and 5 ml HNO3 70 % (w/v) in a microwave

oven. The samples were filtered through a Whatman no. 42

filter. The total concentrations of heavy metals in plant

were determined using ICP-AES.

Transfer factor and enrichment coefficient

The transfer factor (TF) of heavy metals/metalloids from

roots to shoots and the enrichment coefficient (EC) of

heavy metals/metalloids in a plant were calculated as fol-

lows (Zu et al. 2005):

TF ¼ ½Element]shoot=½Element�root ð1Þ

EC ¼ ½Element]shoot=½Element�soil ð2Þ

All these factors were used to evaluate the heavy metals/

metalloids accumulation capacity of plants.

Statistical analysis

The degrees of the linear relationships among the metal

concentrations in roots, leaves or stems were calculated using

the SPSS statistical package. The effects of species and tissue

metal concentrations were tested with a one-way analysis of

variance (Scheffe) using the SPSS statistical package.

Results and discussion

Contaminated soil characteristics

The physical and chemical properties of the soil used in

this study are as listed in Table 1. The pH value of the soil

(tested at a soil to water ratio of 2:1) was 6.84, which is

considered a weakly acidic soil. A particle size analysis

showed that the texture of the soil used in this study was

clay loam soil. The cation exchange capacity (CEC) was

8.70 cmol (?) kg-1 soil. An analysis of soil fertility shows

that the organic matter of the soil used in this study was

1.64 %, inorganic nitrogen 1.92 mg kg-1, available phos-

phate 2.42 mg kg-1, exchangeable potassium 516.50

mg kg-1, exchangeable calcium 1,891.50 mg kg-1,

exchangeable magnesium 493.00 mg kg-1 and exchange-

able sodium 283.15 mg kg-1. The soil had a relatively

high content of exchangeable calcium, and this may be due

to the impact of the mother soil. The Changhua area is an

elevated coastal plain that was formed by layers of alluvial

deposits from the Jhuoshuei River, the Dadu River and the

Pakua Plateau; hence, the soil used in this study contained

some shell deposits. The main composition of these shells

is calcium carbonate, and therefore the content of

exchangeable calcium in the soil of the Changhua area was

relatively high. The total concentration of heavy metals in

the soil is shown in Table 2. The concentrations of heavy

metals showed no significant differences in January and

July when the Scheffe statistical method was applied

(P \ 0.05), but the concentrations of Cd, Cu, and Pb dis-

played significant differences before and after the phyto-

remediation process. When compared with the results of

heavy metal concentrations in the soils in Table 2, the

Table 1 Physical and chemical characteristics of the studied soil

pH (H2O) CEC (cmol kg-1) EC (mScm-1) OM (%) Ino.N BrayP Ex.K Ex.Ca Ex.Mg Ex.Na

(mg kg-1)

6.84 ± 0.35 8.70 ± 0.65 0.23 ± 0.02 1.64 ± 0.10 1.92 2.42 516.5 1,891.5 493.0 283.2

Phytoremediation of heavy metal contaminated soil by Jatropha curcas 1971

123

statistical analysis showed that concentration of heavy

metals was clearly declining and that the final level of

heavy metal contamination was lower than the monitoring

baseline value for food agricultural farmland listed in the

soil pollution control standards of the Environmental Pro-

tection Agency (Taiwan EPA 2008).

Plant growth

The J. curcas selected for the study were seedlings of

1-3 years of age and were planted on the experimental

site in July 2006. The dry based biomass of the J. curcas

is listed in Table 3. The dry based biomasses of the J.

curcas roots, stems, and leaves in January were 61.62,

120.40, and 9.57 g, respectively. The dry based biomasses

of the J. curcas roots, stems, and leaves increased 35.1,

39.7, and 31.8 %, respectively, from January, 2008 to

July, 2008.

Accumulation of heavy metals in root, stem, and leaf

The accumulation of heavy metals in J. curcas tissues

(Root, Stem, and Leaf) in January and July are shown in

Table 4. The metal uptake capacities of the different tis-

sues for the various metals were found to be in the orders:

root, Zn [ Cu [ Cr [ Ni [ Pb [ Cd; stem, Zn [ Cu [Ni [ Cr [ Pb [ Cd; and leaf, Zn [ Ni [ Cu [ Cr [Pb [ Cd. The highest amount of accumulation was for Zn

(Stem [ Leaf [ Root). Further statistical analysis to

determine whether the growth period of the plants in soil

contaminated with heavy metal had any relationship to the

increase or decrease of the absorption of the heavy metal

contaminants in J. curcas tissues revealed that the Cu and

Zn concentrations in the stem and leaves increased sig-

nificantly with growth time.

In recent years, an increasing number of scholars have

been researching the phytoremediation effects of candidate

plants (Pulford et al. 2002; French et al. 2006). There exists

a great deal of data on the analysis of the range of heavy-

metal concentrations absorbed from the soil by plants

(Mertens et al. 2004; French et al. 2006; Brunner et al.

2008). A review of the related literature on phytoremedi-

ation shows that analyses of the relationship of heavy metal

concentrations absorbed by plants and their concentrations

in the soil follow a linear relation, with the absorption

concentration of plants (MPlant), concentration in the soil

(MSoil) and the ratio of absorption by the plant (UPlant)

related by:

UPlant ¼MPlant

MSoil

� 100: ð3Þ

From Tables 5 and 6, the Uplant of Cd in J. curcas tissues

was lower than in the trees Averrhoa carambola, Picea

abies, and Populus tremula (Brunner et al. 2008; Li et al.

2009). The study by Archer and Caldwell (2004) on the

Table 3 Biomass of Jatropha curcas in January and July, 2008

Jatropha curcas (g per plant) January 2008 July 2008

Root 061.62 ± 9.41* 083.22 ± 13.85*

Stem 120.40 ± 7.24* 168.25 ± 6.63*

Leaf 009.57 ± 1.49* 012.61 ± 1.71*

* Indicates significant differences in the biomass of the same part

(P \ 0.05)

Table 4 Heavy metal concentrations in Jatropha curcas tissues (Root, Stem and Leaf)

Heavy metal (mg kg-1) January 2008 July 2008

Root Stem Leaves Root Stem Leaves

Cd 4.34 ± 0.22* 7.34 ± 0.39 5.58 ± 0.27 3.86 ± 0.25* 8.07 ± 0.70 6.18 ± 1.08

Cr 27.99 ± 8.10 15.90 ± 4.52 15.17 ± 3.31 29.08 ± 8.67 18.23 ± 4.23 15.17 ± 3.31

Cu 38.81 ± 3.46 25.87 ± 1.71* 15.60 ± 2.50* 37.51 ± 2.31 29.44 ± 2.59* 24.14 ± 2.21*

Ni 12.69 ± 3.83 22.60 ± 4.92 17.49 ± 1.76* 16.45 ± 2.47 19.40 ± 2.75 25.65 ± 7.71*

Pb 8.63 ± 0.86* 8.37 ± 1.07 7.36 ± 0.81 13.12 ± 1.41* 8.20 ± 0.46 5.70 ± 4.38

Zn 84.72 ± 7.68* 74.96 ± 9.79* 72.87 ± 8.30* 57.60 ± 4.10* 108.27 ± 5.81* 87.06 ± 8.23*

* Indicates significant differences in the degree of heavy-metal content of the same parts in the different seasons (P \ 0.05)

Table 2 Heavy metals concentrations in soils

Heavy metals

(mg kg-1)

Polluted soil

July 2006

January 2008 July 2008

Cd 4.30 ± 2.36* 2.34 ± 0.28 2.10 ± 0.31

Cr 30.53 ± 1.86 28.34 ± 4.32 26.62 ± 3.30

Cu 23.07 ± 7.01* 16.41 ± 5.70 14.10 ± 5.46

Ni 20.99 ± 2.25 17.90 ± 2.72 18.03 ± 4.86

Pb 43.42 ± 8.12* 36.16 ± 4.47 35.77 ± 3.42

Zn 118.63 ± 39.96 102.31 ± 14.46 97.41 ± 19.60

* Indicates significant differences in the degree of heavy metal con-

tents in the soil at the different time points as analyzed using the

Scheffe statistical method (P \ 0.05)


123

Table 5 Heavy metals absorbed from contaminated soil by plants in various tissues and at different times

Species Cd concentrations (mg kg-1) Time (year) Ref.

Plants Soil

Jatropha curcas

Root 3.86 ± 0.25 2.10 ± 0.31 2 This study

Stem 8.07 ± 0.70

Leaf 6.18 ± 1.08

Acacia decurrens 5 ± 5 4 1 Archer and Caldwell (2004)

Acer pseudoplatanus L. 0.5 ± 0.3 5.7–5.9 2 Mertens et al. (2004)

Averrhoa carambola

Stem 11.6 1.6 0.47 Li et al. (2009)

Leaf 10.54

Twig 12.26

Fraxinus excelsior L. 0.3 ± 0.3 5.7–5.9 2 Mertens et al. (2004)

Paulownia tomentosa 0.57 64.9 ± 15.7 0.25 Doumett et al. (2008)

Picea abies 2.1 0.1

11.1 10

Populus tremula 3.9 0.1 4 Brunner et al. (2008)

7.7 10

Populous sp. (Leaf) 2.43 ± 1.08 20 2.67 King et al. (2006)

Populus alba L. 8.0 ± 2.0 5.7–5.9 2 Mertens et al. (2004)

P. tremula9P. Tremuloides

Stem 15 8.14–10.0 0.75 Migeon et al. (2009)

Leaf 44

Salix 9 calodendron (Stem) 5.6 6 3 French et al. (2006)

Salix sp.

Stem 8.86 41.6 ± 0.58 1.42 Maxted et al. (2007)

Leaf 8.20

Salix sp.

Wood 4.9 44.0–45.6 1.83 Pulford et al. (2002)

Bark 14.1

Salix viminalis

Wood 1.6–3.3 1.0–4.6 0.42 Meers et al. (2005)

Bark 3.2–5.9

Root 4.4–12.2

Leaf 5.0–8.8

Species Cr concentrations (mg kg-1) Time (year) Ref.

Plants Soil

Jatropha curcas

Root

Stem

29.08 ± 8.67

18.23 ± 4.23

26.62 ± 3.30 2 This study

Leaf 15.17 ± 3.31

Acacia arabica

Root 0.54

Leaf 0.19

Dalbergia sissoo

Root 0.70 0.63 Khan (2001)

Leaf 0.16

Populus euroamericana


123

Table 5 continued

Species Cr concentrations (mg kg-1) Time (year) Ref.

Plants Soil

Root 0.46

Leaf 0.11

Salix viminalis

Wood 0.2–0.3 28–115 0.42 Meers et al. (2005)

Bark 0.3–0.4

Root 1.6–3.2

Leaf 0.2–0.4

Species Cu concentrations (mg kg-1) Time (year) Ref.

Plants Soil

Jatropha curcas

Root 37.51 ± 2.31 14.10 ± 5.46 2 This study

Stem 29.44 ± 2.59

Leaf 24.14 ± 2.21

Acacia decurrens 12 ± 5 167 1 Archer and Caldwell (2004)


Alnus glutinosa L. 5.8 ± 0.9 53.9–54.2

Fraxinus excelsior L. 12.4 ± 1.8 53.9–54.2

Paulownia tomentosa 46.6 2081 ± 387 0.25 Doumett et al. (2008)

Picea abies 46 28 4 Brunner et al. (2008)

908 640


Populus tremula 65 28 4 Brunner et al. (2008)

339 640

Robinia pseudoacacia L. 8.3 ± 1.2 53.9–54.2 2 Mertens et al. (2004)

Salix sp.

Wood 10.2 937–952 1.83 Pulford et al. (2002)

Bark 27.4

Salix viminalis

Wood 5.9–7.8

Bark 8.6–9.7 18–99 0.42 Meers et al. (2005)

Root 9.8–13.3

Leaf 10.0–11.3

Species Ni concentrations (mg kg-1) Time (year) Ref.

Plants Soil

Jatropha curcas

Root 16.45 ± 2.47 18.03 ± 4.86 2 This study

Stem 19.40 ± 2.75

Leaf 25.65 ± 7.71

Salix 9 calodendron 1.5–3 24–50 3 French et al. (2006)

Salix sp.

Wood 4.8 937–952 1.83 Pulford et al. (2002)

Bark 15.8

Salix viminalis

Wood 0.2–0.5

Bark 0.5–0.8 13–44 0.42 Meers et al. (2005)


123

Table 5 continued

Species Ni concentrations (mg kg-1) Time (year) Ref.

Plants Soil

Root 1.7–3.7

Leaf 0.8–1.4

Species Pb concentrations (mg kg-1) Time (year) Ref.

Plants Soil

Jatropha curcas

Root 13.12 ± 1.41 35.77 ± 3.42 2 This study

Stem 8.20 ± 0.46

Leaf 5.70 ± 4.38


Alnus cordata L. (Leaf) 11.1 ± 2.18 1,445 2.67 King et al. (2006)

Alnus glutinosa L. 5.0 ± 0.5 74.3–75.2 2 Mertens et al. (2004)

Fraxinus excelsior L. 5.0 ± 1.2

Paulownia tomentosa 31.0 3,362 ± 721 0.25 Doumett et al. (2008)

Picea abies 6.1 37 4 Brunner et al. (2008)

36.4 90


Populus tremula 8.0 37 4 Brunner et al. (2008)

23.9 90

P. tremula 9 P. alba (Stem) 100 400–500 0.75 Migeon et al. (2009)

Robinia pseudoacacia L. 2.3 ± 0.3 74.3–75.2 2 Mertens et al. (2004)

Salix viminalis

Wood 1.6–3.3 28–147 0.42 Meers et al. (2005)

Bark 3.2–6.0

Root 1.9–5.2

Leaf 5.0–8.8

Species Zn concentrations (mg kg-1) Time (year) Ref.

Plants Soil

Jatropha curcas

Root 57.60 ± 4.10 97.41 ± 19.60 2 This study

Stem 108.27 ± 5.81

Leaf 87.06 ± 8.23

Acer pseudoplatanus L. 74 ± 48 358

Alnus glutinosa L. 65 ± 12 358–359 2 Mertens et al. (2004)

Fraxinus excelsior L. 26 ± 8 358–359

Paulownia tomentosa 149 4,680 ± 922 0.25 Doumett et al. (2008)

Picea abies 230 97 4 Brunner et al. (2008)

3,009 3,000

P.tremula 9 P. tremuloides (Leaf) 950 415–742 0.75 Migeon et al. (2009)

Populus tremula 513 97 4 Brunner et al. (2008)

1,193 3,000

Populus alba L. 465 ± 125 358–359 2 Meers et al. (2005)

Robinia pseudoacacia L. 45 ± 5 358–359

Salix sp.

Stem 129 2,418 ± 81.8 1.42 Maxted et al. (2007)

Leaf 430


123

relationship between the concentrations of heavy metals

absorbed by the trees Acacia decurrens and their concen-

trations in the soil revealed results similar those for J.

curcas. However, the Uplant of Cr in J. curcas tissues was

higher than in the trees Dalbergia sissoo and Salix vimi-

nalis (Khan 2001; Meers et al. 2005). The Uplant of Cu in J.

curcas tissues was higher than the trees Acer pseudoplat-

anus L., Alnus glutinosa L., Fraxinus excelsior L., Picea

abies, and Robinia pseudoacacia L. (French et al. 2006;

Brunner et al. 2008; Doumett et al. 2008). The Uplant of Ni

in J. curcas tissues was higher than in the trees Sa-

lix 9 calodendron and another Salix sp. (Pulford et al.

2002; Meers et al. 2005; French et al. 2006). The Uplant of

Pb in J. curcas tissues was higher than in the trees Acer

pseudoplatanus L., Alnus cordata L., Alnus glutinosa L.,

Fraxinus excelsior L., Paulownia tomentosa, P. tremu-

la 9 P. alba, and Robinia pseudoacacia L. (King et al.

2006; Doumett et al. 2008; Migeon et al. 2009). The Uplant

of Zn in J. curcas tissues was higher than in the trees Acer

pseudoplatanus L., Alnus cordata L., Alnus glutinosa L.,

Fraxinus excelsior L., Paulownia tomentosa, Robinia

pseudoacacia L., and Salix 9 calodendron (Archer and

Caldwell 2004; French et al. 2006; Doumett et al. 2008).

The uptake quantities of Cd, Cr, Cu, Ni, Pb, and Zn

removed by J. curcas in July were 1.41, 4.53, 6.71, 3.97,

2.03, and 19.3 g, respectively (Fig. 2). After cultivation for

two years, the total amounts of metals removed from the

experimental soil by the plants were: Cd, 0.21 mg m-2; Cr,

0.68 mg m-2; Cu, 1.01 mg m-2; Ni, 0.60 mg m-2; Pb,

0.31 mg m-2; and Zn, 2.90 mg m-2.

Transfer factor and enrichment coefficient

The transfer coefficient refers to the ratio of the heavy

metal concentration of the aerial parts to that of the roots of

the plant. This can be used to determine the ability of the

plant to transport heavy metals from the roots to the aerial

parts (Fig. 3a). The transfer coefficient of J. curcas tissues

was found to be in the order: Ni [ Cd [Zn [ Pb [ Cr [ Cu in January and Cd [ Ni [ Zn [

Table 5 continued

Species Zn concentrations (mg kg-1) Time (year) Ref.

Plants Soil

Salix 9 calodendron 96 250 3 French et al. (2006)

Salix sp. (Leaf) 1,220 ± 71.7 4,285 2.67 King et al. (2006)

Salix sp.

Wood 55.4 2,333–2,402 1.83 Pulford et al. (2002)

Bark 237

Salix viminalis

Wood 38–65 144–729 0.42 Meers et al. (2005)

Bark 262–460

Root 173–250

Leaf 275–674

Table 6 Ratio of absorption by the Jatropha curcas tissues (UPlant)

Heavy metal January 2008 July 2008

URoot UStem ULeaves URoot UStem ULeaves

Cd 1.85 3.14 2.38 1.84 3.84 2.94

Cr 0.99 0.56 0.54 1.09 0.68 0.57

Cu 2.37 1.58 0.95 2.66 2.09 1.71

Ni 0.71 1.26 0.98 0.91 1.08 1.42

Pb 0.24 0.23 0.20 0.37 0.23 0.16

Zn 0.83 0.73 0.71 0.59 1.11 0.89


123

Cu [ Cr [ Pb in July. Summarizing the above experi-

mental results, we observed that the transfer coefficients of

Cd, Ni, and Zn were higher than those of the other heavy

metals. This result is consistent with the conclusion by

Kloke et al. (1984) that Cd and Zn have the highest transfer

coefficients and are the metals most easily absorbed by

plants. According to the view proposed by Kabata-Pendias

(2001) that the transportation of microelements by plants is

based on changes in the electrochemistry of the elements,

metals with moderately easy transportation include Mn, Ni,

Cd, and Zn; and metals that strongly interact with the roots

include Co, Cu, Cr, Pb, Hg, and Fe. The experiments by

Lin showed that Cd is relatively mobile in plants, and

Chaney et al. (1997) also classified Cd as a metal that is

easily transferred to the aerial parts of the plant after

absorption. Cu is easily absorbed through the gap between

the cell walls but has a low mobility in the plant; hence, Cu

is mainly accumulated in the roots after absorption. Our

experiments showed high concentrations of Zn in the aerial

parts, which was secondary only to Cu, and the transfer

coefficient of Zn was higher. The transfer coefficient of Cd

was higher than those of Ni and Pb, meaning that the rate

of transfer of Cd within the plant was higher than Ni and

Pb. From the above results, we concluded that a lower

concentration of heavy metals in the soil led to a higher

transfer coefficient. This may be because the low concen-

tration of heavy metals in the soil induced their absorption

by the plants, as the heavy metal concentrations in the

plants were still relatively low. Hence, when using the

transfer coefficient to determine the absorption capability

of the plants with regard to these heavy metals, the impact

due to the concentrations of heavy metals in the soil must

be taken into account.

Enrichment coefficients are a common important factor

when considering the phytoremediation potential of a given

species (Zhao et al., 2003). In this study, EC values for Cr,

Pb, and Zn were found to be less than 1 (Fig. 3b). The

decrease in enrichment coefficients may be due to the

saturation of metal uptake and/or root to shoot transport

when internal metal concentrations were high. Baker

(1981) concluded that any species may act as an accumu-

lator, an indicator and excluder over different ranges of soil

metal concentration and this seems to be the case for J.

curcas for those heavy metal. J. curcas might behave dif-

ferently with a higher concentration of Cr, Pb, and Zn in

the soil. On the other hand, EC values of Cd, Cu and Ni

were greater than 1 (Fig. 3b) which indicated the phyto-

remediation potential of J. curcas for these heavy metals

from the field contaminated soils.

Conclusions

With regard to the ease of transfer of the heavy metals

absorbed from the roots to the aerial parts of the plant, the

transfer coefficients of Cd, Ni, and Zn were the highest

among the six types of metals analyzed, whereas Cu, Cr

and Pb interacted strongly with the root cells and thus

accumulated at the roots. J. curcas had the best absorption

capability for Cd, Cr, Ni, and Zn. The results from the

present study demonstrate the substantial practical value of

the on-site phytoremediation of a heavy metal contami-

nated field with J. curcas.

0

5

10

15

20

Cd Cr Cu Ni Pb Zn

Heavy metals

Upt

ake

quan

tity

(g)

Leaves

Stem

Root

Fig. 2 The total quantity of heavy metals removed by Jatropha

curcas in July

0.0

0.5

1.0

1.5

2.0

2.5

3.0

Cd Cr Cu Ni Pb Zn

Elements

Tra

nslo

catio

n Fa

ctor

January

July

a

0.0

0.5

1.0

1.5

2.0

2.5

3.0

Cd Cr Cu Ni Pb Zn

Elements

Enr

ichm

ent C

oeff

icie

nt January

July

b

Fig. 3 Translocation factor (a) and enrichment coefficient (b) of

Jatropha curcas


123

Acknowledgments The authors gratefully acknowledge the finan-

cial support of the Chang-Hwa County Government, and the Forest

Bureau, Council of Agriculture, Executive Yuan, ROC.

Conflict of interest The research was conducted in the absence of

any commercial or financial relationships that could be construed as a

potential conflict of interest.

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