Open Journal of Modern Hydrology, 2012, 2, 21-27
http://dx.doi.org/10.4236/ojmh.2012.21004 Published Online January 2012 (http://www.SciRP.org/journal/ojmh)
1
Uptake of Ag, Co and Ni by the Organs of Typha
domingensis (Pers.) Poir. ex Steud. in Lake Burullus and
Their Potential Use as Contamination Indicators
Ebrahem M. Eid1*, Mohamed A. El-Sheikh2,3, Abdulrahman A. Alatar2
1Botany Department, Faculty of Science, Kafr El-Sheikh University, Kafr El-Sheikh, Egypt; 2Botany & Microbiology Department,
College of Science, King Saud University, Riyadh, Saudi Arabia; 3Botany Department, Faculty of Science, Damanhour University,
Damanhour, Egypt.
Received October 24th, 2011; revised November 27th, 2011; accepted December 29th, 2011.
ABSTRACT
The concentrations of Ag, Co and Ni in the sediments and the different organs of Typha domingensis from Lake Burul-
lus, Egypt, were investigated monthly from February to September 2010 to evaluate the aquatic environment quality of
the lake and to test the suitability of these organs for bio-indicating of sediment metals. The sediment heavy metals
were found to decrease in the order of Ni > Co > Ag. The sediment contents of Ag were about 45 times above the
worldwide range. On the other hand, Co concentrations were below the reference ranges of United States and Chinese
soils. The heavy metals bioaccumulation decreased according to the order of rhizome > root > leaf for Ag; and root >
rhizome > leaf for Co and Ni. It was found also that, T. domingensis had no significant differences in heavy metals
concentrations over time. The transfer factors of Ag, Co and Ni from sediment to below-ground organs were smaller
than one. Co had the maximum transport from below-ground to above-ground organs, while Ag had the minimum.
There was a significant linear correlation between the concentration of Ag in root of T. domingensis and that in sedi-
ment. This result suggested that T. domingensis can be regarded as bio-indicator for Ag pollution of Lake Burullus.
Keywords: Bio-indicators; Cattails; Heavy metals; Lake Burullus; Macrophytes; Wetlands
1. Introduction
Heavy metals are serious pollutants in natural environm-
ents due to their toxicity, persistence and bioaccumulation
problems. The accumulation of heavy metals in the enviro-
nment has become a concern due to the health risks to
humans and animals. The problem is not restricted to soils
with high metal levels, such as mining areas, but also incl-
udes those with moderate to low contamination of metals.
These toxic elements are present at elevated levels mainly
through human activities, as smelting, refining of non-fer-
rous metals, electroplating, agricultural practices, and ind-
ustrial and municipal waste disposal on land [1]. Recently,
there has been an increasing interest in using biological
indicators such as plants for monitoring soil, air and water
pollution [2-6]. Perception the environmental pollution by
using biological indicators is a cheap, reliable and simple
alternative to the conventional sampling methods [7].
Aquatic macrophytes are widely distributed in various
wet environments, from fresh to salt water [4] and they
play an important role in heavy metals cycling in the wet-
lands due to uptake, storage, and release processes. Spe-
cifically, plants with potentially high annual primary pro-
duction can extract large amounts of heavy metals from
their environment and store these metals in biomass and
litter [8]. Therefore, some aquatic plants such as Eichhor-
nia crassipes (C. Mart.) Solms, Phragmites australis (Cav.)
Trin. ex Steud., Potamogeton pectinatus L. and Typha
domingensis (Pers.) Poir. ex Steud. have been used to in-
dicate, monitor and purify water pollution [3,4,8-11].
Typha domingensis (Pers.) Poir. ex Steud. is a warm-
temperate and tropical regions plant that occurs every-
where in ditches and marshy places in Egypt [12,13]. It is
one of the major components of vegetation stands along
the shores of Lake Burullus close to the Deltaic Mediter-
ranean coast [14]. T. domingensis is one of the emergent
plants most commonly used in constructed wetlands for
the enhancement of water quality in water treatment sys-
tems [10,15] due to its high growth rate and great capac-
ity for heavy metals accumulation in its tissues [16,17].
In the present study, Ag, Co and Ni concentrations in
the plant and sediment samples were analyzed in order to
evaluate the aquatic environment quality of Lake Burul-
lus, and to investigate possible relationships between
*Corresponding author.

Uptake of Ag, Co and Ni by the Organs of Typha domingensis (Pers.) Poir. ex Steud. in Lake Burullus and
Their Potential Use as Contamination Indicators
22
heavy metal concentrations in the plant and sediment in
order to ascertain if this plant can be used as an indicator
for the heavy metal contamination of the study area.
2. Materials and Methods
2.1. Study Area
Lake Burullus is one of the Egyptian northern lakes that
connected with the Mediterranean Sea through a natural
outlet, Bughaz El-Burullus, (Figure 1). It is bordered
from the north by the Mediterranean Sea and from south
by agricultural lands of the Nile Delta. Its coordinates are
31˚36'N and 30˚33'E in north-west, 31˚36'N and 31˚07'E
in the north-east, 31˚22'N and 30˚33'E in the south-east,
31˚22'N and 31˚07'E in the south-west. The lake extends
for a distance of 47 km along the NE-SW axis with ob-
long shape of a total area of 410 km2. The depth of this
lake varies between 20 cm close to the shore of the east-
ern basin and 200 cm at the middle basin and near the sea
outlet. A marine sand bar separates the Mediterranean
coast from the lake shore, with a width that varies be-
tween a few hundred meters near the sea outlet till a
maximum of 6 km in the west [18]. The main human
activity in Lake Burullus is fish production, with fish
yield of 52,000 ton·yr−1 [19]. It is one of the major dis-
posal areas that receives most of the drainage water of
the Nile Delta’ agricultural lands which feeds the lake
with about 4 billion m3·yr−1 [20]. Also it receives fish
farms and industrial drainage water [18]. It is alkaline,
shallow, brackish, and polluted lake [8]. The Mediterra-
nean deltaic coast, in which this lake occurs, belongs to
the arid region where the climatic conditions are warm
summers (20˚C - 30˚C) and mild winters (10˚C - 20 ˚C).
2.2. Sample Collection
Sampling was carried out at three locations of Lake Bu-
rullus and three sampling sites were randomly chosen in
each location (Figure 1). In each sampling site, leaves,
rhizomes and roots of T. domingensis were collected
monthly from February to September 2010 from more
than 10 individual plants within a 100 m2, and then they
were mixed up to form a composite plant sample. At each
sampling site, one sediment sample was collected monthly
close to sampling plants as a profile of 20 cm depth.
2.3. Sample Analysis
The plant samples were washed thoroughly with tap water
and rinsed with deionized water, then dried at 85˚C in an
oven to constant weight after that was ground into a pow-
der using a metal-free plastic mill. The sediments were air
dried at room temperature and passed through 2 mm sieve
to separate gravel and debris. Plant samples were digested
with concentrated HNO3 and HClO4 (87:13, v/v), while
sediment samples with concentrated HF:HNO3:HClO4
(4:1:1, v/v) [21]. Estimation of Ag, Co and Ni was carried
out by Atomic absorption (Shimadzu AA-6200). All these
procedures are according to Allen [22].
Figure 1. Map of Lake Burullus (Egypt) indicating the three sampling locations by asterisks.

Uptake of Ag, Co and Ni by the Organs of Typha domingensis (Pers.) Poir. ex Steud. in Lake Burullus and
Their Potential Use as Contamination Indicators
23
2.4. Statistical Analysis
The significance of variation in heavy metal concentra-
tions in sediment supporting the growth of T. domingen-
sis was assessed using one-way ANOVA. The signify-
cance of variation in heavy metals of T. domingensis
organs in relation to plant organs over time were assessed
using repeated measurement ANOVAs. We used the
correlation procedures to evaluate statistical relationships
between heavy metals of plant organs and sediment. All
statistical analyses were carried out using software SPSS
version 15.0 of Statistical Software Package [23].
The translocation of heavy metals from sediment to
plant tissues was assessed following transfer factor (TF).
It was calculated to determine the relative uptake of heavy
metals by the plants with respect to sediment [24]: TF =
Concentration of metals in plant body (mg·kg−1)/Concen-
tration of metals in sediment (mg·kg−1) at that site.
3. Results
In sediment, the heavy metals were found to decrease in
the order of Ni > Co > Ag (Table 1). No significant dif-
ferences in sediment heavy metals concentrations were
found over time. The concentrations of Ag ranged from
5.28 mg·kg−1 in April to 6.33 mg·kg−1 in August with an-
nual mean 5.86 mg·kg−1; Co ranged from 11.85 mg·kg−1
in July to 14.07 mg·kg−1 in May with annual mean 13.06
mg·kg−1; Ni ranged from 21.57 mg·kg−1 in April to 27.65
mg·kg−1 in March with annual mean 25.07 mg·kg−1.
Heavy metals concentrations in the organs of T. dom-
ingensis are shown in (Figure 2). The bioaccumulation
decreased according to the order of rhizome > root > leaf
for Ag; and root > rhizome > leaf for Co and Ni. The
heavy metals of the plant organs were found to decrease
in the same order of sediment (Ni > Co > Ag). It was
found that T. domingensis had no significant differences
in heavy metals concentrations over time. Ag, Co and Ni
concentrations ranged between 1.24 - 3.09, 3.64 - 6.63
and 5.08 - 15.39 mg·kg·DW−1 in leaf; 1.12 - 3.87, 4.48 -
6.89 and 10.44 - 17.44 mg·kg·DW−1 in root; 1.23 - 6.89,
2.08 - 8.69 and 6.52 - 20.99 mg·kg·DW−1 in rhizome,
respectively (Figure 2).
Ag
Concentration(mg·kg·DW
–1
)Concentration (mg·kg·DW
–1
)Concentration (mg·kg·DW
–1
)
0
2
4
6
8
10
12
14
Leaves
Root
Rhizome
Co
0
2
4
6
8
10
12
14
Fmonth=1.06,P= 0.439
Forgan=0.56,P= 0.583
Fmonth*organ=3.81,P= 0.000
Ni
Month
FebMarAprMay JunJulAug Sep
0
3
6
9
12
15
18
21
24
27
30
Fmonth=1.39,P= 0.284
Forgan=3.12,P= 0.076
Fmonth*organ=1.69,P= 0.088
Fmonth=0.50,P= 0.816
Forgan=5.87,P= 0.014
Fmonth*organ=7.92,P= 0.000
Figure 2. Monthly mean and standard error (vertical bars)
of Ag, Co and Ni concentrations of Typha domingensis or-
gans in Lake Burullus.
Table 1. Monthly mean (1st line) and standard error (2nd line) of Ag, Co and Ni concentrations in sediment supporting the
growth of Typha domingensis in Lake Burullus. F-values represent the one way ANOVA. The minimum and maximum values
are in the bold letters.
Month
Site
Feb. Mar. Apr. May Jun. Jul. Aug. Sep.
Annual
mean F-value P
Ag (mg·kg−1) 5.35
0.71
5.47
0.63
5.28
0.73
5.88
0.47
6.01
0.48
6.25
0.72
6.33
0.59
6.32
0.69
5.86
0.21 0.485 0.832
Co (mg·kg−1) 11.97
0.92
13.76
0.72
12.95
1.45
14.07
0.55
13.39
0.43
11.85
0.59
13.23
0.80
13.23
1.17
13.06
0.30 0.783 0.611
Ni (mg·kg−1) 24.29
0.80
27.65
1.69
21.57
1.48
23.41
1.28
25.19
5.59
25.73
1.86
26.63
3.48
26.07
4.75
25.07
0.99 0.390 0.895

Uptake of Ag, Co and Ni by the Organs of Typha domingensis (Pers.) Poir. ex Steud. in Lake Burullus and
Their Potential Use as Contamination Indicators
24
The transfer factors of Ag, Co and Ni from sediment to
below-ground organs were smaller than one. Co had the
maximum transport from below-ground to above-ground
organs, while Ag had the minimum (Table 2). Ag accu-
mulated in higher concentration in roots grown in sedi-
ment containing greater amount of this element (r = 0.56,
P < 0.01; Table 3). Significantly positive correlation was
found between Co contents in roots and the level of Ni
element in sediment (r = 0.41, P < 0.05).
4. Discussion
Silver is very toxic to heterotrophic bacteria and thus is
widely used as an aseptic substance [25]. However, some
bacteria (e.g., Thiobacillus ferrooxidans) are capable of
accumulating great amounts of Ag [26]. Ag compounds
are known to precipitate bacterial proteins as well as to
form insoluble complexes with ribonucleic acids [27].
The average Ag content for worldwide soils is estimated
as 0.13 mg·kg−1, and range of its mean contents in soils
of various countries is 0.05 and 0.13 mg·kg−1 [25]. In the
present study, Ag concentrations of Lake Burullus sedi-
ment were about 45 times above the worldwide range.
Concentrations of Ag in plants were reported by Smith
and Carson [28] to range from 0.03 to 0.5 mg·kg−1.
Chapman [29] established the intermediate range of Ag
in plant foodstuffs as 0.07 to 2.0 mg·kg−1. In the present
study, the average concentrations of Ag were 2.01, 2.23
and 4.26 mg·kg−1 in leaves, roots and rhizomes of T.
domingensis, respectively; and these detected values
were not in the phytotoxic range (> 5.04 mg·kg−1) re-
ported by Cunningham and Stroube [30].
Most of Co is used for special alloys utilized in several
industries. It is also used in chemical catalysis and syn-
thesis, as well as a plastic hardener. In pharmacy Co is
used for medical and veterinarian drugs. The radionu-
clide 60Co is applied for some medical treatments [25].
Cobalt is an essential micro-nutrient for animals, being
part of the structure of vitamin B12, and is involved with
certain enzymes. The essentiality of Co for both blue-
green algae and microorganisms in fixing N2 is now well
established [25]. Plants require only minute amounts
mainly for catalytic functions and levels are often <5
mg·kg−1 dry weight [22]. The range of Co in reference
soil samples of United States is from 5.5 to 29.9 mg·kg−1
and in Chinese soils, in the range of 5.5 - 97.0 mg·kg−1
[31]. In the present study, Co concentrations of sediment
were below the reference ranges of the United States and
Chinese soils. Different concentrations of Co in plant
tissues have been reported to produce toxicity symptoms,
as follows (in mg·kg−1): 43 - 142 in bush beans [32]; 19 -
32 in Sudan grass [33]; and 6 in barley seedlings [34].
However, commonly reported critical Co levels in plants
range from 30 to 40 mg·kg−1 [35]. In the present study,
Co concentrations of T. domingensis organs were below
the phytotoxic range (30 - 40 mg·kg−1).
Table 2. Mean and standard error (SE) of the transfer factor of Ag, Co and Ni from sediment to roots (RT/SE), sediment to
rhizomes (RE/SE), below- to above-ground organs (AG/BG) in Typha domingensis in Lake Burullus.
Transfer factor
RT/SE RE/SE AG/BG
Mean SE Mean SE Mean SE
Ag 0.40 0.03 0.75 0.08 0.88 0.09
Co 0.46 0.03 0.41 0.05 1.18 0.13
Ni 0.55 0.06 0.51 0.06 0.89 0.12
Table 3. Pearson correlation coefficient (r-values) between Ag, Co and Ni concentrations of sediment and plant organs of
Typha domingensis in Lake Burullus. The significant values are in the bold letters. *P < 0.05, **P < 0.01.
LeafAg RootAg RhizomeAg SedimentAg LeafCo RootCo RhizomeCo SedimentCo LeafNi RootNi RhizomeNi
RootAg −0.499*
RhizomeAg 0.493* −0.542**
SedimentAg −0.231 0.564** 0.038
LeafCo −0.257 0.087 −0.093 −0.003
RootCo −0.119 −0.270 0.233 −0.090 0.134
RhizomeCo 0.187 −0.415* 0.158 −0.306 0.018 0.073
SedimentCo 0.148 −0.118 0.180 −0.171 0.017 −0.383 −0.160
LeafNi 0.062 0.136 −0.078 0.220 0.249 0.002 −0.040 −0.119
RootNi 0.078 −0.026 0.122 0.170 −0.016 0.140 0.205 −0.040 0.323
RhizomeNi 0.298 −0.190 0.273 −0.008 −0.324 −0.307 0.528** −0.071 0.191 0.094
SedimentNi −0.336 0.077 −0.183 −0.023 0.140 0.411* −0.224 0.084 0.160 −0.097 −0.266

Uptake of Ag, Co and Ni by the Organs of Typha domingensis (Pers.) Poir. ex Steud. in Lake Burullus and
Their Potential Use as Contamination Indicators
25
Nickel is considered as a serious pollutant that is re-
leased from metal processing plants and from the in-
creased combustion of coal and oil. Also some sewage
sludge and phosphate fertilizers may be importance
sources of Ni in agricultural soils. There is no evidence
of an essential role of Ni in plant metabolism [25]. Soils
throughout the world contain Ni in the very broad range,
however its mean concentrations, as reported for various
countries are within the range 13 - 37 mg·kg−1 [25]. In
the present study, Ni concentrations in sediment were in
the world range. The phytotoxic Ni concentrations range
widely among plant species and cultivars from 40 to 246
mg·kg−1 [33]. Davis et al. [34] found the toxic Ni content
of barley seedlings to be as low as 26 mg·kg−1, whereas
Khalid and Tinsley [36] found 50 mg·kg−1 Ni in ryegrass
to cause slight chlorosis. The mean Ni values detected in
T. domigensis organs were below the phytotoxic range
(26 - 246 mg·kg−1).
The transfer factor generally showed the movement of
heavy metals from sediment to root and shoot, indicating
the efficiency to uptake of the bio-available metals from
the environment and gives an idea whether the plant is an
accumulator, excluder or indicator [37]. Zu et al. [38] re-
ported that TF > 1 were determined in metal accumulating
plants, whereas TF was typically < 1 in metal excluding
plants. In the present study, the mean TF for Ag, Co and
Ni from sediment to below-ground organs were lower than
one. That may be partly attributed to the fact that the TF
was calculated based on the total metal concentrations in
sediment instead of the bioavailable fractions, which are
the dominant form for metal uptake by plant roots [39].
The mean TF for Ag and Ni from below- to above-ground
tissues were lower than one, which means that T. domin-
gensis is metal excluding plant and did not effectively
transfer Ag and Ni from below-to above-ground tissues.
On the other hand, the higher translocation ratio of Co in T.
domingensis shoots make it suitable for Co phytoextrac-
tion from sediment. The differences in TF values indicated
that each metal has different phytotoxic effect on T.
domingensis [40]. In addition, these results could be re-
lated to differences in solubility and availability of each
heavy metal ion [41]. Variability of within-plant distribu-
tion of Ag, Co and Ni in T. domingensis may be also due
to compartmentalization and translocation in the vascular
system [41]. These mechanisms are poorly understood and
need further study.
There was a significant linear correlation between the
concentration of Ag in root of T. domingensis and that in
sediment. This result suggested that T. domingensis can
be regarded as bio-indicator for Ag pollution of Lake
Burullus, defined as organisms providing quantitative
assessment of the environmental quality. However, no
significant relationships were found between Co and Ni
concentrations in T. domingensis organs and those in
sediment. This may be partly attributed to the fact that
the correlation was developed based on the total metal
concentrations in sediment instead of the bioavailable
fractions [39].
In conclusion, T. domingensis in Lake Burullus could
be regarded as bio-indicator on the Ag pollution and a
suitable green filter to reduce the pollution load reaching
the lake, if the above-ground biomass is harvested at the
maximum biomass. In Lake Burullus, the above-ground
biomass reached the maximum value in July [6327 g·m−2;
11], as much as (in mg m−2) 11.64 Ag, 33.32 Co and
63.52 Ni could be theoretically removed annually from
the lake by harvesting above-ground biomass of T.
domingensis in July. Thus, we recommend removing the
shoots immediately after cutting to avoid heavy metals
leaching from shoots to sediment and water. However,
over the long term, annual harvesting may lead to the
deterioration of T. domingensis primary productivity.
Thus for the sustainable use of T. domingensis stands,
harvests should not be conducted annually; perhaps har-
vest rotation could be used (similar to crop rotation in
farming).
5. Acknowledgments
This project was supported by the Center of Excellence
in Biodiversity Research, King Saud University for en-
couragement and support.
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Their Potential Use as Contamination Indicators
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