Uptake of Ag, Co and Ni by the Organs of <i>Typha domingensis</i> (Pers.) Poir. ex Steud. in Lake Burullus and Their Potential Use As Contamination Indicators

doi:10.4236/ojmh.2012.21004

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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)

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.

Email: *[email protected]

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

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

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).

Concentration(mg·kg·DW

–1

)Concentration (mg·kg·DW

–1

)Concentration (mg·kg·DW

–1

)

Leaves

Root

Rhizome

Fmonth=1.06,P= 0.439

Forgan=0.56,P= 0.583

Fmonth*organ=3.81,P= 0.000

Month

FebMarAprMay JunJulAug Sep

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

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

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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