Journal of Environmental Protection, 2010, 1, 431-437
doi:10.4236/jep.2010.14050 Published Online December 2010 (http://www.SciRP.org/journal/jep)
431
Phytoextraction of Metal Contaminants by Typha
angustifolia: Interaction of Lead and Cadmium in
Soil-Water Microcosms
Thanawan Panich-Pat1*, Suchart Upatham2, Prayad Pokethitiyook3, Maleeya Kruatrachue3,
Guy R. Lanza4
1Faculty of Liberal Arts and Science, Kasetsart University, Nakhon Pathom, Thailand; 2Faculty of Science, Burapha University,
Chonburi, Thailand; 3Faculty of Science, Mahidol University, Bangkok, Thailand; 4Environmental Science Program, University of
Massachusetts, Amherst, USA.
Received September 6th, 2010; revised October 16th, 2010; accepted October 20th, 2010.
ABSTRACT
A greenhouse study was conducted on phytoextraction and accumulation of lead (Pb) and cadmium (Cd) from con-
taminated soil – water microcosms by the narrow-leaved cattail, Typha angustifolia. The plants were grown in sandy
loam soil containing 1,666 and 38.5 mg/L of Pb(NO3)2 and Cd(NO3)2 respectively. The trends of lead and cadmium by T.
angustifolia for all soil – water microcosms suggested interaction effects as decreased soil lead concentrations and
increased water cadmium concentrations over time. T. angustifolia expressed trends as increased biomass in all con-
taminated shoots and roots examined. Cadmium uptake in shoot and root biomass slightly decreased when lead was
initially added to the soil but cadmium uptake in root biomass increased after 30 days. Data suggested an interaction
between lead and cadmium and that lead uptake was inhibited when cadmium was present.
Keywords: Phytoextraction, Contaminant Interaction, Lead, Cadmium, Microcosm, Typha angustifolia
1. Introduction
Lead and cadmium are elements that are highly toxic to
plants [1]. Both heavy metals are capable of interacting
in biological systems and are persistent contaminants that
can change their speciation, but do not biodegrade. Cad-
mium is the heavy metal of greatest concern in most ag-
ricultural soils. It is loosely held by soil constituents and
is readily available to plant roots and transported through
the xylem to the vegetative and reproductive organs,
negatively affecting the crops [2]. In general, broadleaf
plants such as lettuce and swiss chard accumulate more
cadmium than grasses. Plant leaves and stems can also
accumulate more than seeds. Nevertheless, lead and
cadmium can be toxic and inhibit DNA synthesis, mitosis,
cell division and germination [3]. Iqbal et al. [3] also
investigated the effect of lead and cadmium individually
and in combination on the germination and seedling
growth of Leucaena leucocephala and Delonix regia.
They found reduced germination and seedling growth,
and that both species showed more tolerance to lead than
cadmium. Kastori et al. [4] found that the treatment of
sunflower plants with lead diminished the concentrations
of chlorophylls and carotenes, while Larsson et al. [5]
observed a reduction in the chlorophyll concentrations of
plants exposed to cadmium. Mohan and Hosetti [6] sug-
gested that both cadmium and lead drastically depressed
catalase activity but stimulated peroxidase activity. They
reported that the interaction between lead and cadmium
on growth of other plants e.g., the root of Juncus acustus,
was strongly inhibited by lead nitrate. Iqbal et al. [3]
reported that the toxicity of lead and cadmium to young
trees of Fagus silvatica is higher when both are com-
bined. Other reports indicated that these two metals can
bind to the cell wall, thus weakening their toxic effects to
plants [7].
Phytoremediation is the use of plants to remove con-
taminants from soil, water and air. One promising phy-
toremediation process is the phytoextraction of heavy
metal contaminants from soil. Typha spp has been stud-
ied for their ability to phytoextract metals from soil, but
most research to date reports the phytoextraction of indi-
vidual heavy metal contaminants rather than mixtures of
metals that commonly occur at contaminated sites. This

Phytoextraction of Metal Contaminants by Typha angustifolia: Interaction of Lead and Cadmium in
Soil-Water Microcosms
432
study examined the interaction of lead and cadmium
during metal phytoextraction from soil-water micro-
cosms by Typha angustifolia.
2. Materials and Methods
2.1. Plant Microcosm
T. angustifolia were obtained from New England Wet-
land Plant Company and planted in plastic bucket mi-
crocosms (50 cm height, 30 cm diameter) containing 10
kg of sandy loam soil, collected from Orchard Hill,
Massachusetts, USA. Sixteen buckets of microcosms
were prepared, each with 2 plants in 10 kg of soil with a
5 liter layer of surface water. The microcosms were
maintained in a greenhouse at a temperature of 24  1℃
under a full spectrum of 400 W light source providing a
16 hour per day photoperiod. The plants in microcosms
were allowed to grow for 30 days until the plants reached
an average height of 30 cm and then received the heavy
metal treatments.
2.2. Soil Characterization
One to three gram samples of soil were dried overnight
in an oven at 105℃. Soil samples were sieved through
2mm and 0.5 mm screen, thoroughly mixed and ground
in a mortar and pestle to obtain a uniform texture. Soil
subsamples of 0.1-0.3 g were digested in 3 ml of concen-
trated HNO3 using microwave digestion (CEM model
MDS – 2100) for approximately 30 minutes. Samples
were then evaporated to near dryness, filtered, and ad-
justed to a volume of 25 ml in distilled water. Soil sam-
ples were analyzed for lead and cadmium concentration
before and after the addition of lead and cadmium mix-
tures using Flame Atomic Absorption Spectrophotometer
(FAAS), Graphite Furnace Atomic Absorption Spectro-
photometer (GFAAS), and Hydride Generation (HG).
2.3. Preparation of Stock Solutions and
Application of Lead and Cadmium
Lead as Pb(NO3)2 and cadmium as Cd(NO3)2 were dis-
solved in distilled water to prepare a stock solutions for
treatment groups at concentrations of 10,000 mg/L and
1,000 mg/L, respectively. One liter of the lead stock so-
lution was added to 5 L of distilled water to obtain a
concentration of 1,666 mg/L for application to each mi-
crocosm. Two hundred ml of the cadmium stock solution
was added into 5 L to obtain a concentration of 38.5
mg/L. The sixteen microcosms were randomly divided
into 4 treatment groups, each group with four replicates
as follows:
Group 1 served as the controls (no additions of lead
and cadmium),
Group 2 received cadmium solutions at a concentra-
tion of 38.5 mg/L,
Group 3 received lead solutions at a concentration of
1,666 mg/L,
Group 4 received a mixture of lead at 1,666 mg/L and
cadmium at 38.5 mg/L.
2.4. Plant Analysis
Plant samples were harvested every fifteen days after
heavy metal treatment. The whole plant was washed
thoroughly with running tap water, divided into shoots
and roots, and weighed, dried in an oven at 80℃ for two
days and weighed again. Dried plant tissues were cut into
small pieces, and homogenized. Approximately 0.1-0.3 g
of shoot and root material were digested in a 3 ml con-
centration of HNO3 and microwave digestion (CEM
model MDS – 2100) for 30 minutes. Samples were eva-
porated to near dryness, filtered, and adjusted to a vol-
ume of 25 ml distilled water. The sample solutions were
collected in polypropylene bottles and measured using
FAAS, GFAAS, and HG.
2.5. Water Analysis
After fifteen days of treatment, 5 ml water samples were
collected from the control and the treatment groups. The
water samples were adjusted to a volume of 25 ml, col-
lected in polypropylene bottles, and analyzed for lead
and cadmium using FAAS, GFAAS, and HG.
2.6. Data Analysis
Data were analyzed using Excel analysis of variance
(ANOVA) for significant differences (P  0.05). Dun-
can’s New Multiple Range Test was used to determine
significant differences (P  0.05).
3. Results
3.1. Soil and Water Characteristics
The basic characteristics of the soil used in the soil-water
microcosms are presented in Table 1. The results indi-
cate that the soil is a sandy loam typical of many ecosys-
tems. At the end of the experiment, the soil and water
were examined in each microcosm for total lead and
cadmium.
Table 2 and Figures 1 and 2 summarized the lead and
cadmium concentrations for all soil – water microcosms
after 15 days. The results indicated that soil lead levels of
Group 4 microcosms were higher than Group 3 micro-
cosms (1061  476.6 as compared to 841.7  39.82
mg/kg), but the water lead levels were slightly different,

Phytoextraction of Metal Contaminants by Typha angustifolia: Interaction of Lead and Cadmium in
Soil-Water Microcosms
433
Table 1. Physical and chemical characteristics of microcosm
soils.
Soil properties
Clay (%) 6-18
Moist bulk density (g/cm3) 1.3-1.6
Permeability (h) 0.6-6.0
Available water capacity (in) 0.1-0.16
Soil pH 3.6-6.0
Organic matter (%) 2-6
Total soil Pb (mg/kg) 8.71
Total soil Cd (mg/kg) 0.38
Total water Pb (g/L) 9.96
Total water Cd (mg/L) ND
ND: Not detected
Figure 1. Cadmium and lead concentrations in soil micro-
cosms (mg/kg).
Figure 2. Cadmium and lead concentrations in water mi-
crocosm (mg/L).
thus there was a significant difference in mean lead in
water (P  0.05). Group 2 microcosms soil cadmium lev-
els were approximately 13  0.5 mg/kg as compared to
39.8  2 mg/kg in Group 4 microcosms indicating that
soil cadmium level increased 3 folds. There was a sig-
nificant difference in mean lead in soil (P  0.05). The
water cadmium level in Group 4 microcosms (24.2  2.6)
was higher than Group 2 microcosms (4.8  1.1). There
was a significant difference in mean cadmium in water (P
 0.05).
After 30 days, Group 4 microcosms had soil lead lev-
els of approximately 1,658  663 mg/kg as compared to
998  11 mg/kg in Group 3 microcosms and the soil lead
level in Group 4 microcosms was higher than Group 3
microcosms. The water lead level in Group 4 micro-
cosms (814.8  396.2) was higher than Group 3 micro-
cosms (697.4  668.9). Cadmium accumulation in soil
decreased when lead was added to the soil (14.3  1.3 as
compared to 6.5  0.6 mg/kg). There was a significant
difference in mean cadmium in soil (P  0.05). Group 4
microcosm water cadmium levels were 28.6  11.8 mg/L
as compared to 1.3  0.6 in Group 2 microcosm water.
The statistical trends suggested interaction effects be-
tween the two metals as increased soil lead concentra-
tions and decreased soil cadmium concentrations.
3.2. T. Angustifolia Growth Characteristics
The growth patterns of T. angustifolia expressed as fresh
and dry weights are summarized in Table 3 and Figures
3 and 4. Statistical trends indicated increased biomass
over time in all contaminated and control soil microcosm.
The lead and cadmium nitrate salts used as contaminants
most likely explain the differences in control and experi-
mental biomass. However, mean fresh and dry weights
were not significantly different between treatment groups
(P  0.05) over the 30 day exposure period (Figures 3
and 4). Interestingly, in Group 3 and 4 the fresh and dry
weight of shoot biomass increased while those of root
biomass seem to unchanged (Figures 3 and 4). Group 2
plants had trends with increased fresh and dry weight
shoot and root biomass.
3.3. Lead and Cadmium Accumulation in Plant
Biomass
Concentrations of lead and cadmium in T. angustifolia
shoot and root biomass are summarized in Table 4 and
Figures 5 and 6. The results on both 15 and 30 day
treatments indicated that there was a lead and cadmium
interaction which resulted in a marked reduction in lead
uptake and a slight decrease in cadmium uptake by T.
angustifolia.
Lead levels in shoot and root biomass in the combined

Phytoextraction of Metal Contaminants by Typha angustifolia: Interaction of Lead and Cadmium in
Soil-Water Microcosms
434
Table 2. Lead and cadmium concentrations in soil – water microcosms.
Soil (mg/kg)a Water (mg/L)a
Time Treatment (group)
Cd Pb Cd Pb
1 (control) b0.1 ± 0 h6.3 ± 0.7 lND p,*8 ± 0.7
2 (Cd) c13 ± 0.5 h10.3 ± 0 l4.8 ± 1.1 p,*7.5 ± 0.5
3 (Pb) b0.1 ± 0.1 h841.7 ± 39.8 l,*0.3 ± 0.1 q800 ± 12.5
15 days
4 (Pb + Cd) d39.8 ± 2 i1061.3 ± 476.6 m24.2 ± 2.6 q770 ± 149.2
1 (control) e0.1 ± 0 j5.2 ± 0.1 n,*0.4 ± 0.2 r,*4.6 ± 0.3
2 (Cd) f14.3 ± 1.3 j5.1 ± 0.1 n1.3 ± 0.6 r,*2.5 ± 0.5
3 (Pb) e0.1 ± 0.1 j997.6 ± 11.4 n,*0.3 ± 0.1 r697.4 ± 668.9
30 days
4 (Pb + Cd) g6.5 ± 0.6 k1657.6 ± 663.2 o28.6 ± 11.8 r814.8 ± 396.2
*g/L; avalues are means from 2 replications with standard error (n = 2); b,c,dhomogeneous subsets of soil cadmium in 15 days; e,f,ghomogeneous subsets of soil
cadmium in 30 days; h,ihomogeneous subsets of soil lead in 15 days; j,khomogeneous subsets of soil lead in 30 days; l,mhomogeneous subsets of water cadmium
in 15 days; n,ohomogeneous subsets of water cadmium in 30 days; p,qhomogeneous subsets of water cadmium in 15 days; rhomogeneous subsets of water cad-
mium in 30 days.
Table 3. Fresh and dry weight in shoot and root biomass of T. angustifolia in contaminated soil-water microcosms.
Fresh weight (g)a Dry weight (g)a
Time Treatment (group)
Shoot Root Shoot Root
1 (control) 23.9 ± 2.2 22.3 ± 1 2.2 ± 0.2 2.3 ± 0
2 (Cd) 26.7 ± 11.4 12 ± 5.3 2.5 ± 1.2 1.6 ± 0.4
3 (Pb) 35.7 ± 19.9 11.1 ± 5.1 3.2 ± 1.8 1.6 ± 0.3
15 days
4 (Pb + Cd) 48.4 ± 14.3 22.5 ± 2 5 ± 1.4 2.3 ± 0.1
1 (control) 37.3 ± 11.3 25.7 ± 4.7 4.1 ± 1.3 1.8 ± 0.2
2 (Cd) 36.5 ± 5.3 19.5 ± 7.3 4.1 ± 0 1.6 ± 0.4
3 (Pb) 77.6 ± 26 17.5 ± 2.1 10.7 ± 3.5 1.9 ± 0.3
30 days
4 (Pb + Cd) 75.5 ± 22.7 24.2 ± 7.5 10.6 ± 4.4 2.1 ± 0.8
avalues are means from 2 replications with standard error (n = 2).
Table 4. Concentration of lead and cadmium in shoot and root biomass of T. angustifolia.
Pb (mg/kg)a Cd (mg/kg)a
Time Treatment (group)
Shoot Root Shoot Root
1 (control) b2.8 ± 1.8 f6.6 ± 2.3 jND m0.6 ± 0.1
2 (Cd) b3 ± 0.4 f6.1 ± 0.1 j42.3 ± 14.9 n378.3 ± 141.5
3 (Pb) c1,875.9 ± 663.6 g22,462 ± 2,804.6 j0.7 ± 0.4 m0.6 ± 0.2
15 days
4 (Pb + Cd) b529.3 ± 57.8 g16,555 ± 2,854.5 j33.5 ± 24.7 m,n223.3 ± 18.7
1 (control) d1.2 ± 0.2 h3.4 ± 0.2 k0.1 ± 0 o0.8 ± 0.1
2 (Cd) d1.1 ± 0.5 h4 ± 0 l20.3 ± 2.6 o,p241 ± 119.5
3 (Pb) e354.9 ± 22.3 i20,173.6 ± 2,165.6 k0.4 ± 0.2 o1.5 ± 0.7
30 days
4 (Pb + Cd) e404.3 ±2 1.1 i13,675 ± 3,925 l20.5 ± 1.9 p369.2 ± 82.3
avalues are means from 2 replications with standard error (n = 2); b,chomogeneous subsets of lead in shoot in 15 days; d,ehomogeneous subsets of lead in shoot in
30 days; f,g homogeneous subsets of lead in root in 15 days; h,ihomogeneous subsets of lead in root in 30 days; jhomogeneous subsets of cadmium in shoot in 15
days; k,lhomogeneous subsets of cadmium in shoot in 30 days; m,nhomogeneous subsets of cadmium in root in 15 days; o,phomogeneous subsets of cadmium in
root in 30 days.

Phytoextraction of Metal Contaminants by Typha angustifolia: Interaction of Lead and Cadmium in
Soil-Water Microcosms
435
Figure 3. Biomass fresh weight (shoots and roots) (g).
Figure 4. Biomass dry weight (shoots and roots) (g).
lead and cadmium microcosms decreased approximately
two and one fold after 15 days of treatment Group 4
(529.3  57.8) as compared to Group 3 (1,875.9 
663.6)). There was a significant difference (P  0.05) in
mean shoot and root lead accumulation of T. angustifolia
at day 15. After 30 days, lead accumulation in shoot
biomass of Group 4 was slightly higher than that of
Group 3 (404.3  21.1 as compared to 354.9  22.3
mg/kg). In root biomass, lead concentration was lower in
Group 4 as compared to Group 3 (13,675  3,925 vs
20,173.6  2,165.6 mg/kg). There was a significant dif-
ference (P  0.05) in mean shoot and root lead accumula-
tion of T. angustifolia in 30 days (Figure 5).
Cadmium uptake in shoot biomass decreased when
lead was added to the soil in 15 days (Table 4) (Group 4
compared to Group 2). There was no significant differ-
ence (P  0.05) in mean shoot but there was a significant
difference in mean root cadmium accumulation of T.
angustifolia in 15 days. After 30 days, cadmium uptake
in root biomass increased when lead was added to the
soil (Group 4 compared to Group 2). There was a sig-
nificant difference (P  0.05) in the mean shoot but there
was no significant difference in mean root cadmium ac-
cumulation of T. angustifolia biomass in 30 days (Figure
Figure 5. Concentration of lead in shoot and root biomass
(mg/kg).
Figure 6. Concentration of cadmium in shoot and root
biomass (mg/kg).
6). The statistical trends suggested interaction effects
with cadmium inhibiting lead uptake in both roots and
shoots.
4. Discussion
In this study, lead treatments did not affect fresh or dry
weights of T. angustifolia. Plants growing in microcosms
with lead contaminated soils grew as well or better than
plants in control microcosms. Cadmium treatment plants
had fresh weight of shoot biomass similar to controls. It
is possible that cadmium could be taken up by the roots
and transported by the xylem to the vegetative and re-
productive organs, negatively affecting plant health [8].
Plants could also accumulate high quantities of cadmium
without suffering adverse effects on growth [9].
In the present study, increasing cadmium input to soil
microcosm highly increased cadmium accumulation in
shoot biomass and hence inhibited cadmium accumula-
tion in root biomass. This is in agreement with the find-
ing by Cunningham et al. [10] Plants grew well in the
lead and cadmium contaminated soils in this study,
however accumulated lower concentrations of lead a

Phytoextraction of Metal Contaminants by Typha angustifolia: Interaction of Lead and Cadmium in
Soil-Water Microcosms
436
30-day growth period.
Coughtrey and Martin [11] studied Midger plant
(Holcus lanatus) uptake of cadmium, lead, and zinc in
solution culture and showed interactions on lead concen-
trations in roots. Interestingly, the significant effects in
shoots of this population were positive and tend towards
increased metal concentrations. Miller et al. [12] reported
positive interactions between lead and cadmium on lead
and cadmium uptake in corn roots. Moshe et al. [13].
demonstrated that low levels ( 1 mg/L) of lead in-
creased the toxicity of cadmium (0.1 mg/L) in phyto-
plankton. Antagonism occured when the concentration of
lead exceeded that of cadmium but no synergistic effects
were noted in Chlorella when cadmium, copper, chro-
mium, and nickel were added to the culture media. Pre-
treatment of algae with nickel and mercury reduced cad-
mium toxicity; this may reflect competition among met-
als for cellular binding sites.
The results of this study provide evidence for phytoex-
traction interactions of lead and cadmium in soil-water
microcosms. The statistical trends suggested that the in-
teraction is complex and produced, decreased lead in root
biomass and increased cadmium in shoot biomass al-
though there were no significant variations in biomass
production. Chukwuma [14] compared the accumulation
of cadmium, lead, and zinc in cultivated and wild plant
species in a derelict lead - zinc mine and found an overall
reduction in the potential toxicity of cadmium by zinc
through simple mass action effects specific for cultivated
plants, they noted that other additional tolerant or adap-
tive mechanisms might be operative in the wild plants.
McKena et al. [15] reported the interactions between zinc
and cadmium in nutrient solution and their effects on the
accumulation of both metals in plant roots and leaves and
also reported higher cadmium concentrations in older
compared to younger leaves of lettuce and spinach.
Many other studies involving several metals and nu-
trients have been reported. Lagerwerff and Biersdorf [16]
reported that cadmium and zinc were competitive cations.
Similarly, Robert et al. [17] showed that cadmium can
functionally substitute for zinc. The changes in the iron
and zinc concentrations induced by increased cadmium
levels resulted in alterations of the iron/zinc ratio and the
alteration was more pronounced in roots than shoots,
with both tissues exhibiting increases in the iron/zinc
ratio with increased concentrations of cadmium. On the
contrary, the toxicity of cadmium has been linked to the
fact that cadmium competes for similar active sites but
does not functionally substitute for zinc [18].
Cadmium and lead are toxic heavy metals and zinc an
essential element makes this association interesting as it
raises the possibility that the toxic effects of cadmium
may be preventable or treatable by zinc. Hinesly et al.
[19] indicated that both cadmium and zinc uptake by
plants were dependent on the pH of the growing media.
Ravera [20] showed that cadmium had toxic effects in
plants on photosynthesis and also indicated various
changes in biological activities. Subsequent studies have
confirmed these findings and extended the interaction to
other toxic effects of cadmium like inhibition of cell pro-
liferation, and cytotoxic action [21] and growth suppres-
sion in plants [22].
The biochemical mechanisms of cadmium - zinc in-
teraction are unknown, but various cellular and subcellu-
lar processes like the ratio of the cadmium to zinc in the
tissues, induction of synthesis of different types of met-
allothionein, alteration of absorption and tissue distribu-
tion of one metal by another, and competition at the level
of zinc containing metalloenzymes are known to be in-
volved in the interaction [23]. Minnie et al. [24] studied
phytoextraction of soil cobalt using hyperaccumulator
plants and found interaction and decreased uptake of
nickel in the presence of cobalt. Homer et al. [25] also
reported that the uptake of cobalt may suppress nickel
uptake, indicating a possible synergistic or antagonistic
relationship between the elements.
5. Conclusions
T. angustifolia exhibited very good potential for the
phytoextraction of mixtures of lead and cadmium con-
taminants from soil-water microcosms. Although cad-
mium interaction appeared to reduce the uptake of lead in
soil-water microcosms contaminated with both metals,
uptake of lead into T. angustifolia roots was high, reach-
ing levels of 13,675  3,925 mg/kg after 30 days growth.
6. Acknowledgements
This work was supported by the Thailand Research Fund.
We thank Dr. Wipharat Chuachuad for analyzing the
samples.
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Soil-Water Microcosms
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