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Ecological Engineering 73 (2014) 17–25

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Ecological Engineering
journal homepage: www.elsevier.com/locate/ecoleng

Monthly variations of trace elements accumulation and distribution in


above- and below-ground biomass of Phragmites australis (Cav.) Trin. ex
Steudel in Lake Burullus (Egypt): A biomonitoring application
Ebrahem M. Eid a,b, *, Kamal H. Shaltout c
a
Botany Department, Faculty of Science, Kafr El-Sheikh University, 33516 Kafr El-Sheikh, Egypt
b
College of Sciences, King Khalid University, Abha, Saudi Arabia
c
Botany Department, Faculty of Science, Tanta University, 31527 Tanta, Egypt

A R T I C L E I N F O A B S T R A C T

Article history: This study was carried out in some natural stands of Phragmites australis (Cav.) Trin. ex Steudel grown in Lake
Received 5 January 2014 Burullus, a Mediterranean lake in north Egypt, to investigate: (1) the concentration of trace elements in the
Received in revised form 6 August 2014 organs of P. australis, (2) the extent of trace elements mobility from sediment to below-ground organs and
Accepted 2 September 2014
within the plant, (3) the organs of P. australis as potential bioindicators for the contamination of the water
Available online xxx
and sediment by the trace elements, and (4) the amount of trace elements that released back into the
surrounding water after decomposition of dead tissues. Above- and below-ground biomass of P. australis,
Keywords:
water and sediment were sampled monthly for one year at six sites of Lake Burullus (three sites represent
Bioindicator
Common reed
each of the northern and southern parts of the lake) using six randomly distributed quadrats (each of
Heavy metals 0.5  0.5 m) at each sampling site. The above- and below-ground biomasses of southern sites are
Macrophytes significantly higher than that of the northern sites. Above-ground biomass is >2.5 folds of the below-
Mediterranean lakes ground biomass in the northern and southern sites. The highest concentration in the below-ground organs
Phytoremediation is Cu, Fe and Zn; and in the leaf is Cd. The monthly highest values of trace elements are Cu and Fe in February
at the beginning of the growing season; and Cd and Zn in January at the end of the growing season. The
annual mean of trace element concentrations (in mg kg 1) in P. australis organs ranged from 11.0 to 23.8 for
Cd, from 31.0 to 65.6 for Cu, from 34.4 to 97.3 for Zn, and from 505.0 to 2833.0 for Fe. The mean
bioaccumulation factor of all trace elements from the sediment to the below-ground organs is greater than
unity for all elements with the following sequence: Cd > Fe > Zn > Cu. Cd has the highest translocation factor
from the below-ground to the above-ground organs, while Fe has the lowest. Positive linear correlations
are detected between the concentrations of all elements (except Cu) in plant organs, water and sediment.
The higher translocation factor of Cd in the above-ground organs of P. australis makes it suitable for the
phytoextraction of this element from the water and sediment, while the lower translocation factor for Cu,
Fe and Zn makes it suitable for their phytostabilization. In conclusion, all the organs of P. australis could act
as bioindicators and biomonitors of the examined trace elements.
ã 2014 Elsevier B.V. All rights reserved.

1. Introduction et al., 2010). Trace elements, such as Cd, Cu, Fe and Zn, are
elements that cannot be degraded by microbial or chemical
The contamination of aquatic and terrestrial environments process to alter or reduce their toxicity over time. These elements
with trace elements due to human activity is the common come from the use of pesticides, fertilizers, sludge and municipal
environmental problem all-over the world (Garbisu and Alkorta, compost, metals smelting, refining of non-ferrous metals,
2003). Their transfer and accumulation in the animal and human electroplating and industrial wastes (Garbisu and Alkorta,
bodies through the food chain cause DNA damage, carcinogenic 2003; Kabata-Pendias, 2011).
effects and induction of mutations (Knasmuller et al., 1998; Gupta There has been an increasing interest in the use of green plants
to remove or immobilize metals in process called phytoremedia-
tion (Raskin et al., 1997; Peng et al., 2008). Phytoremediation is a
* Corresponding author. Tel.: +20 010 2264 8840; fax: +20 047 321 5175.
biological, low-cost and eco-friendly clean-up technique for the
E-mail addresses: ebrahem.eid@sci.kfs.edu.eg, ebrahem.eid@gmail.com restoration of the water and soil properties (Pilon-Smits, 2005;
(E.M. Eid). Vymazal et al., 2009). One method of this technology is

http://dx.doi.org/10.1016/j.ecoleng.2014.09.006
0925-8574/ ã 2014 Elsevier B.V. All rights reserved.
18 E.M. Eid, K.H. Shaltout / Ecological Engineering 73 (2014) 17–25

phytostabilization, where plants are used to immobilise metals study aims to investigate: (1) the concentration of trace elements
and store them in their below-ground organs and/or soil. On the in the organs of P. australis, (2) the extent of trace elements
other hand, during phytoextraction, hyperaccumulators may be mobility from the sediment to below-ground organs and within
used to remove metals from the soil and concentrate them in the the plant, (3) the organs of P. australis as potential bioindicators for
above-ground organs (Weis and Weis, 2004; Bose et al., 2008). the contamination of the water and sediment by the trace
Aquatic plants have the ability to accumulate larger metal elements, and (4) the amount of trace elements that released
concentrations in their tissues than those in the surrounding water back into the surrounding water after decomposition of dead
due to their fibrous root system of large contact surface area tissues. This study could be useful in quantifying the role of
(Bragato et al., 2009). They can tolerate high metal concentrations reed stands in trace elements cycling in one of the south
in the water and sediments, and can be used in the biomonitoring Mediterranean wetlands, and could help in proper management
applications (Bonanno and Lo Giudice, 2010; Bonanno, 2011, 2013; of the wetland ecosystems that are used for biomass production or
Eid et al., 2012a). Consequently, wetland plants have been widely wastewater treatment in Egypt.
used in constructed and natural wetlands to reduce the metal
contents in the domestic, industrial and agricultural wastewaters 2. Materials and methods
(e.g., Vymazal, 2008).
Phragmites australis (Cav.) Trin. ex Steudel, common reed, is a 2.1. Study area
cosmopolitan emergent plant that grows throughout Europe, Asia,
Africa, America and Australia (Holm et al., 1977). In Egypt, it occurs Lake Burullus, one of the Egyptian northern lakes, is part of the
in all phytogeographical regions (Täckholm, 1974; Boulos, 2009; Deltaic Mediterranean Coast which belongs to the arid region with
Zahran and Willis, 2009), and it is the major component of reed warm summers (20–30  C) and mild winters (10–20  C) (Fig. 1). It is
stands along the shores of Lake Burullus (Shaltout and Al-Sodany, connected with the Mediterranean Sea through a natural outlet
2008). P. australis is widely used in constructing wetlands for called Al-Bughaz, and has an oblong shape with an area of 410 km2
treatment of industrial wastewaters containing metals (Bonanno, and bordered by the agricultural lands in the south, while a sand
2011; Bragato et al., 2009; Vymazal et al., 2007, 2009) because of its bar separates it from the Mediterranean Sea in the north. Its main
high growth rate and biomass production, deep fibrous root basin could be classified into eastern, middle and western basins.
system, adaptability to a wide range of climatic conditions, and The western basin is the narrowest with a width of 5 km
great capacity for metals accumulation (Baldantoni at al., 2009; (in north–south direction), while the middle basin is the widest
Bonanno and Lo Giudice, 2010). with a maximum width of 14 km. The depth of this lake varies
The effectiveness of a phytoremediation process depends on the between 20 cm close to the shore of the eastern basin and 200 cm
selection of appropriate plants for particular environment (Duman in the middle basin and near the sea outlet (see Shaltout and Khalil,
et al., 2007). Thus, the detailed baseline information on the 2005). The lake was registered as a Ramsar site in 1998 due to its
accumulation properties of wetland plant species can help in the importance for the wintering, foraging, refuge and breeding of the
selection of appropriate plants for wetland phytoremediation migrant birds (Kassas, 2002). Fish production is the main human
systems. Although it has been shown that P. australis plays an activity in this lake, with fish yield of 52,000 ton year 1 (Khalil and
important role in the cycling of macro-nutrients in Lake Burullus El-Dawy, 2002). It is one of the major disposal areas for agricultural
(Eid et al., 2010a), it is not yet clearly understood its role in trace drainage water in Egypt, where it receives about 4 billion m3 year 3
elements cycling and accumulation properties. Hence, the present of the drainage water from the Nile Delta agricultural lands,

Fig. 1. Map of Lake Burullus (Egypt) indicating the locations of the six sampling sites (*).
E.M. Eid, K.H. Shaltout / Ecological Engineering 73 (2014) 17–25 19

accounting for 97% of its water inflow (El-Shinnawy, 2002). The 2.4. Sediment sampling
source of trace elements in Lake Burullus are due to the input of
domestic, industrial, and agricultural drainage from human At each sampling site, six sediment samples were collected
settlements, factories, and reclaimed lands in its catchment area monthly from the same sampling quadrats as a profile of 50 cm
(Eid et al., 2010b; Masoud et al., 2011; Okbah and Hussein, 2006; depth. The sediments were air dried and passed through a 2 mm
Shaltout and Khalil, 2005). The main vegetation type in this lake is sieve to separate gravel and debris.
the reed swamps which include P. australis as the overwhelmingly
dominant species and Potamogeton pectinatus L. and Typha 2.5. Chemical analysis
domingensis (Pers.) Poir. ex Steudel as common associates (Shaltout
and Al-Sodany, 2008). For sediment samples, diethylenetriaminepentaacetic acid
solution (DTPA) was used for the extraction of available trace
elements (Cd, Cu, Fe and Zn). For plant samples, trace elements
2.2. Field and laboratory
were extracted from 0.5 to 1 g of plant organs (leaf, stem, and
below-ground organs) using a mixed-acid digestion method. For
The drainage water from the Nile Delta agricultural lands and
plant, water and sediment samples; Cd, Cu, Fe and Zn were
wastewater from fish farms, which enter Lake Burullus from the
determined by atomic absorption (Shimadzu AA-6200; Shimadzu
south, leads to a pronounced fertility gradient from the south to the
Co., Ltd. Japan). All of these procedures are outlined in Allen (1989)
north. Hence, sampling was carried out at six sites, three sites to
and Clesceri et al. (1999). Chemical concentrations were expressed
represent each of the northern and southern parts (Fig. 1). All these
based on dried matter. Finally, the trace element contents of the
six sites were pure or nearly pure P. australis flooded stands during
above- and below-ground organs (g m 2) were calculated by
the whole year. At each sampling site, above-ground biomass of
multiplying the trace element concentrations with the biomass of
P. australis was harvested monthly for one year within six randomly
the respective parts (g DM m 2).
distributed quadrats (0.5 m 0.5 m), where all P. australis shoots
were cut off at ground level and separated into leaves (including
2.6. Estimation
sheaths) and stems. Care was taken to randomly select quadrats
and to ensure that sampling was not conducted in quadrats that
The bioaccumulation factor (BAF) was calculated to determine
were less than 2 m from the edge or from previously sampled
the efficiency of the plant for accumulating a trace element from the
quadrats. Below-ground organs (roots and rhizomes) were
sediment (Ghosh and Singh, 2005): BAF = concentration of an
excavated from the same quadrats at a depth of 0.5 m (the deepest
element in the below-ground organs (mg kg 1)/concentration of
point of below-ground organs penetration; Eid et al., 2010a), and
the same element in the sediment at the same site (mg kg 1).
washed with lake water until free from sediment. In the laboratory,
The translocation factor (TF) was calculated to depict the ability of
samples were carefully washed with tap water over a 4 mm mesh
the plant to translocate a trace element from the below-ground to the
sieve to minimize material loss, oven dried at 85  C to a constant
above-ground organs (Ghosh and Singh, 2005): TF = concentration of
weight, weighted, and then ground using a metal-free plastic mill.
an element in the above-ground organs (mg kg 1)/concentration of
All biomass values were determined as g dry matter per square
the same element in the below-ground organs (mg kg 1).
meter (g DM m 2).

2.7. Statistical analysis


2.3. Water sampling
The data of the six sites were collated, which resulted in
At each sampling site, six water samples were collected eighteen replicates at each sampling date per each part of the lake
monthly from the same sampling quadrats. The water samples (north/south). Before performing ANOVA, the data were tested for
were taken as integrated composite samples from the top of the their normality of distribution and homogeneity of variance, and
water surface down to 50 cm. The samples were collected in plastic when necessary, data were log-transformed. The data of biomass,
bottles and brought to the laboratory where filtered. After that, concentration of trace elements in the water and sediment were
samples were deep-frozen for the analysis of dissolved Cd, Cu, Fe subjected to a two-way analysis of variance (ANOVA-2) to test the
and Zn. differences between sites over time. Trace elements data for

Table 1
Temporal variation in biomass characteristics (annual mean  standard error: SE) of Phragmites australis in northern and southern sites of Lake Burullus.
Parameters were measured monthly for one year. F-values represent the two-way analysis of variance (ANOVA-2).

Characteristics Minimum  SE Maximum  SE Mean  SE


Northern sites
Stem biomass (g DM m 2) 2741  187 6845  690 4478  217
Leaf biomass (g DM m 2) 226  42 1430  109 706  71
Total above-ground biomass (g DM m 2) 2969  208 7884  780 5184  269
Total below-ground biomass (g DM m 2) 863  73 2768  542 1960  127

Southern sites
Stem biomass (g DM m 2) 3857  475 6776  513 5102  186
Leaf biomass (g DM m 2) 262  69 1657  147 887  86
Total above-ground biomass (g DM m 2) 4119  544 8317  654 5988  261
Total below-ground biomass (g DM m 2) 942  74 3254  247 2306  146

Stem biomass: Fmonth = 31.7, P = 0.000, Fsite = 38.7, P = 0.000, Fmonthsite = 0.2, P = 0.994.
Leaf biomass: Fmonth = 20.6, P = 0.000, Fsite = 9.6, P = 0.010, Fmonthsite = 3.2, P = 0.003.
Total above-ground biomass: Fmonth = 99.7, P = 0.000, Fsite = 101.4, P = 0.000, Fmonthsite = 0.1, P = 1.000.
Total below-ground biomass: Fmonth = 41.8, P = 0.000, Fsite = 27.9, P = 0.000, Fmonthsite = 0.3, P = 0.972.
20 E.M. Eid, K.H. Shaltout / Ecological Engineering 73 (2014) 17–25

P. australis organs were subjected to a three-way analysis of 7.1 and 11.8 for Cu, 23.1 and 41.8 for Fe and 4.4 and 12.1 for Zn
variance (ANOVA-3) to test the differences between organs and (Fig. 4). Trace element concentrations followed different decreas-
sites over time. Correlations between the concentrations of trace ing trends as follows (Figs. 3–5): in the water, Fe > Zn> Cd> Cu for
elements in the plant organs and water or sediment samples were the northern and southern sites; in the sediment, Fe > Cu > Zn> Cd
evaluated using the Pearson’s r coefficient. The trace elements for the northern sites and Fe > Zn > Cu > Cd for the southern sites; in
releasing (g m 2) into the surrounding water was calculated by the leaf, stem and below-ground organs, Fe > Zn > Cu> Cd for the
multiplying the decomposed dry matter in a year (g DM m 2) with northern and southern sites. Fe attained the highest concentration
the trace element concentrations (mg kg 1) at the last month of the in the water, sediment and plant organs of the northern and
present study (January). Statistical analyses were carried out using southern sites. On the other hand, Cu attained the lowest
STATISTICA software (Statsoft, 2007). concentration in the water, while Cd had the lowest concentration
in the sediment and plant organs.
3. Results Regarding the P. australis organs, Cd, Cu and Fe concentrations of
the southern sites were significantly higher than those of the
Above- and below-ground biomasses of southern sites are northern sites (Fig. 5, Table 2). The highest concentration in the
significantly higher than that of the northern sites (Table 1). In below-ground organs was Cu, Fe and Zn; and in the leaf Cd.
addition, above-ground biomass is >2.5 folds of the below-ground The monthly highest values of trace elements were Cu and Fe in
biomass for both the northern and southern sites. Shoots started to February at the beginning of the growing season and those of Cd and
grow in February (early-spring), reached their maximum biomass Zn in January at the end of the growing season (Fig. 5). The annual
of 7884 and 8317 g DM m 2 in August (late-summer) for northern mean of trace element concentrations (in mg kg 1) in P. australis
and southern sites, and then rapidly decreased when they moved organs ranged between 15.4 and 15.9 for Cd, 37.1 and 54.0 for Cu,
into the senescence stage which ended in January by fully dying off 48.6 and 77.5 for Zn and 1177.5 and 1907.4 for Fe. The trace element
(Fig. 2). For the northern and southern sites, the total contents in the above-ground organs increased rapidly from the
below-ground biomass decreased to 863 and 942 g DM m 2 in early growing season (February) until reaching their maxima in
July (mid-summer) due to the upward translocation of reserves for August and then decreased. The contents of trace elements in the
the initial growth of shoots, and then gradually increased to a below-ground organs decreased sharply and reached minimum
maximum of 2768 and 3254 g DM m 2 in December (early-winter) content in July and increased thereafter.
by downward translocation from shoots. The mean bioaccumulation factor of all trace elements from the
Regarding the trace elements of Lake Burullus water, Cu sediment to the below-ground organs was greater than unity and
concentration of southern sites was significantly higher than that had the following order: Cd > Fe > Zn > Cu (Table 3). Cd had the
of the northern sites (Fig. 3), while Zn concentration of northern highest translocation factor from the below-ground to the above-
sites was significantly higher than that of the southern sites. The ground organs, while Fe had the lowest. Positive linear correlations
concentration of water trace elements (in mg l 1) in Lake Burullus were detected between all the trace elements concentrations
ranged between 64.0 and 88.0 for Cd, 28.0 and 54.0 for Cu, 1010.0 (except Cu) in plant organs, water and sediment (Table 4).
and 4200.0 for Fe, and 101.0 and 136.0 for Zn (Fig. 3). The trace elements remained in the dead biomass at the end of
For sediment, Cd concentration of southern sites was signifi- the study period were released into the ecosystem either through
cantly higher than that of the northern sites (Fig. 4), while Cu leaching or during decay of shoots. The dead shoot biomass at the
concentration of northern sites was significantly higher than that end of the study period amounted to 3702 and 4119 g DM m 2
of the southern sites. The concentration of sediment trace entering the decomposition process for the northern and southern
elements (in mg kg 1) ranged between 0.15 and 0.22 for Cd, sites (Fig. 2). Using a decay rate of 0.0117 and 0.0036 day 1 for the

AGB_Northern sites
9000 Stem_Northern sites
Leaf_Northern sites
8000 BGB_Northern sites
AGB_Southern sites
7000 Stem_Southern sites
Leaf_Southern sites
Biomass (g DM m )
-2

6000 BGB_Southern sites

5000

4000

3000

2000

1000

0
Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec Jan

Month

Fig. 2. Monthly variation in the above- (AGB) and below-ground biomass (BGB) of Phragmites australis in northern and southern sites of Lake Burullus during one year. Vertical
bars indicate the standard errors of the means (N = 18).
E.M. Eid, K.H. Shaltout / Ecological Engineering 73 (2014) 17–25 21

Northern sites
100 F
site
= 2.01, P = 0.170, df = 1 60 F
site
= 6.27, P = 0.020, df = 1 Southern sites
Cd F = 1.52, P = 0.243, df = 11 Cu F = 1.21, P = 0.373, df = 11
95 month 55 month

90 50

85 45
-1

-1
µg l

µg l
80 40

75 35

70 30

65 25

60 20
5000 F
site
= 3.04, P = 0.095, df = 1 150 F
site
= 15.40, P = 0.001, df = 1
Fe F
month
= 1.43, P = 0.273, df = 11 Zn F
month
= 1.09, P = 0.434, df = 11
4500
140
4000
3500 130
-1

-1
3000
µg l

µg l
120
2500
2000 110

1500
100
1000
500 90
Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec Jan

Month Month

Fig. 3. Monthly variation in the water trace element concentrations in northern and southern sites supporting Phragmites australis in Lake Burullus. Water characteristics
were measured monthly for one year. Vertical bars indicate the standard errors of the means (N = 18). F-values represent the two-way analysis of variance (ANOVA-2), df:
degree of freedom.

leaves and stems (Eid et al., 2014a), we calculated that 2764 and DM m 2; Hocking, 1989) and Iraq (13.5 kg DM m 2; Rezk and
3077 g DM m 2 were decomposed in a year for the northern and Edany, 1981). The high biomass of P. australis in the present study
the southern sites. This is equivalent to releasing the following into could be due to the favorable conditions for its growth in this lake.
the surrounding water (in g m 2): 0.06 Cd, 0.11 Cu, 3.71 Fe, and 0.14 Apart from the intra-specific genetic variations differences
Zn for the northern sites and 0.06 Cd, 0.12 Cu, 4.01 Fe, and 0.16 Zn between the populations (Koppitz, 1999; Koppitz et al., 1997;
for the southern sites. Lambertini et al., 2008), this can be partly attributed to the
photosynthetic characteristics and/or certain environmental
4. Discussion factors that vary with latitude such as temperature, day length,
solar irradiance, and length of growing season (Eid et al., 2010a,b).
Analysis of Lake Burullus water in the present study indicated Lessmann et al. (2001) reported significant impact of climate
pollution with Cd according to the maximum levels of trace changes on the photosynthetic characteristics of four populations
elements (in mg l 1) in the irrigation water (10.0 for Cd, 200.0 for of P. australis collected from geographically distinct areas in
Cu, 5000.0 for Fe and 2000.0 for Zn) as reported by Rowe and Europe. In addition, a study of another large emergent
Abdel-Magid (1995). On the other hand, the values of all trace macrophyte, T. domingensis, from the same study area had mean
elements in the sediment were lower than the polluted levels of above-ground biomass (3.6 kg DM m 2) which was higher than all
freshwater sediments as reported by NOAA (2009). Fertility was estimates for Typha species from the northern temperate zone
previously found to have a pronounced correlation with the (Eid et al., 2012b).
biomass characteristics of P. australis (Eid et al., 2010b). Our present In the present study, the ratio of below-ground to above-ground
results confirmed that above- and below-ground biomasses of biomass (0.4) is comparable to that reported for P. australis (0.25,
P. australis have had an increasing with increasing fertility from the Serag, 1996 in the north-eastern region of the Nile Delta, Egypt),
north to the south. T. domingensis (0.4, Eid et al., 2012b in Lake Burullus) and
The annual mean above-ground biomass of P. australis was Potamogeton pectinatus (0.3, Eid et al., 2014b; in Lake Burullus). It is
approximately 5.2 and 6.0 kg DM m 2 in the northern and much lower than the reported values at high latitudes (1.7 at 40 ,
southern sites of Lake Burullus, which is comparable to those of Windham et al., 2003 1.6 4.0 at 49 , Dykyjová and Hradecká,
the related Egyptian studies (e.g., Batanouny et al., 1991; Eid et al., 1976; 2.9–4.8 at 51, Soetaert et al., 2004). This pattern may be a
2010a, 2010b; Khedr, 1989; Serag, 1996). The present estimates are strategy of P. australis to store more assimilates in below-ground
higher than the previous estimates in the northern temperate zone biomass in the temperate zone compared with the south
(0.6–3.5 kg DM m 2; Björndahl, 1983; Boar et al., 1989; Cizkova Mediterranean zone, where photosynthesis is not a limiting factor
et al., 2001; Ho, 1979; Ksenofontova, 1988; Kve t et al., 1969; Lippert for biomass production due to high radiation and long growth
et al., 1999; Rolletschek et al., 2000; Soetaert et al., 2004; Van der period (Eid et al., 2010a). In Lake Burullus, photosynthesis was the
Toorn, 1972); but lower than those reported in Australia (9.9 kg dominant process contributing to the assimilate production (84%),
22 E.M. Eid, K.H. Shaltout / Ecological Engineering 73 (2014) 17–25

0.24 13
Cd Cu Northern sites
12 Southern sites
0.22

11
0.20
-1

-1
10
mg kg

mg kg
0.18
9

0.16 8

F = 15.15, P = 0.001, df = 1 F = 14.60, P = 0.001, df = 1


site 7 site
0.14 F = 0.09, P = 1.000, df = 11 F = 0.62, P = 0.779, df = 11
month month
6
45 14
Fe Zn
40 12

10
-1

-1
35
mg kg

mg kg
8
30
6
F = 1.57, P = 0.223, df = 1 F = 3.44, P = 0.077, df = 1
25 site site
F = 2.58, P = 0.059, df = 11 4 F = 2.07, P = 0.114, df = 11
month month

Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec Jan

Month Month

Fig. 4. Monthly variation in the sediment trace element concentrations in northern and southern sites supporting Phragmites australis in Lake Burullus. Sediment
characteristics were measured monthly for one year. Vertical bars indicate the standard errors of the means (N = 18). F-values represent the two-way analysis of variance
(ANOVA-2), df: degree of freedom.

while remobilization from rhizomes was estimated to contribute Bonanno and Lo Giudice, 2010; Du Laing et al., 2009; Duman et al.,
with 15% to assimilate production for P. australlis (Eid et al., 2010a). 2007; Kastratovic et al., 2013; Samecka-Cymerman and Kempers,
In the present study, the maximum Cu and Fe concentrations in 2001; Stoltz and Greger, 2002; Vymazal et al., 2007, 2009). In
P. australis organs were recorded in February at the beginning of addition, Cu, Fe, and Zn concentrations were comparable to some
the growing season, while the maximum Cd and Zn concentrations those measured in related previous studies (Aksoy et al., 2005;
were recorded in January at the end of the growing season. On the Baldantoni et al., 2009; Du Laing et al., 2009; Duman et al., 2007;
other hand, no monthly variations of trace element concentrations Hocking, 1989; Kastratovic et al., 2013; Windham et al., 2003). The
in the water and sediment were observed. Higher accumulation of differences between the results obtained in the present study and
Cd and Zn at the end of the growing season was higher probably the reported results by other researchers might be related to
due to decreased metabolic processes and smaller changes in plant sampling time, pollution levels, physico-chemical characteristics
biomass (Kastratovic et al., 2013). The concentration of metals in of the sediment and water at the sampling sites, soil texture, soil
P. australis depends on its growth stage, pH, redox potential and the microbial activity, and analytical methods used in digestion of
interactions between the metals and other elements which are P. australis materials (Du Laing et al., 2003, 2009; Kabata-Pendias,
more important in determining metal uptake than metal 2011; Weis et al., 2003).
concentration in the sediment and water (Du Laing et al., 2009; In the present study, the mean bioaccumulation factors for all
Duman et al., 2007). Compared to the other elements, Cd had the trace elements from the sediment to the below-ground organs were
lowest concentration in the sediment and all organs of P. australis, greater than one, which means that P. australis implies a
this is normal as this metal is usually very low (Vymazal et al., bioaccumulation process based on high concentrations in below-
2009). Although some metals concentrations in the above-ground ground organs (Bonanno, 2013; Bose et al., 2008). The mean
organs declined throughout the growing season, all the contents of translocation factors from the below-ground to the above-ground
trace elements content increased and reached its maxima in organs for Cu, Fe and Zn were lower than one, which indicating that
August, which means that biomass was the decisive factor in P. australis does not effectively transfer those metals from the
determining the quantity of metals per unit area of stand (Eid et al., below- to above-ground organs and these elements were largely
2012c). retained in under-ground organs, which suggests that this plant has
The mean Cd, Cu and Fe values recorded for P. australis organs in potentials for Cu, Fe and Zn phytostabilization. Translocation factors
the present study were within the phytotoxic ranges (5.0–30.0, <1 for Cu, Fe and Zn in the present study are in agreement with
20.0–100.0, and >500.0 mg kg 1, respectively). On the other several studies such as Baldantoni et al. (2009), Bonanno (2011),
hand, the mean Zn values were lower than the phytotoxic range Duman et al. (2007), Stoltz and Gregor (2002) and Weis et al. (2004).
of 100.0–400.0 mg kg 1 (Kabata-Pendias, 2011). Cd concentrations On the other hand, P. australis seems more suitable for Cd
in P. australis organs of Lake Burullus were higher than the range of phytoextraction given a value of the mean translocation factor
those recorded for the same species in some natural and from the below-ground to the above-ground organs higher than
constructed wetlands (Aksoy et al., 2005; Bonanno, 2011, 2013; one, and similar conclusion was reached by Fediuc and Erdei (2002).
E.M. Eid, K.H. Shaltout / Ecological Engineering 73 (2014) 17–25 23

Stem_Northern sites
Cd Leaf_Northern sites 70 Cu
24
Concentration (mg kg ) BGO_Northern sites 65

Concentration (mg kg )
-1

-1
22 Stem_Southern sites
Leaf_Southern sites 60
20 BGO_Southern sites 55
18 50

16 45

14 40

12 35

10 30

Fe 110 Zn
3000
100
Concentration (mg kg )

Concentration (mg kg )
-1

-1
2500 90

80
2000
70
1500
60

50
1000
40
500
30
Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec Jan

Month Month

Fig. 5. Monthly variation in the trace element concentrations in Phragmites australis organs in northern and southern sites of Lake Burullus during one year. Vertical bars
indicate the standard errors of the means (N = 18). BGO: below-ground organs.

The differences in values of translocation factor could be related


to the metal interactions which can be originated by conflicting and
Table 2 synergetic processes (Bonanno and Lo Giudice, 2010). Thus,
Results of the three-way analysis of variance (F-values) of trace element such interactions could affect the efficiency of metals uptake and
concentrations of Phragmites australis. Month: January–December, site: north/ alter their distribution (Weis et al., 2004). Plant physiological
south, organ: stem, leaf and below-ground organs.
factors, differences in the solubility and availability of each
Effect df Cd Cu Fe Zn metal ion, and the plant regulation mechanisms to control shoot
Month 11 21.8c 5.1b 2.4a 1.1ns concentrations could be other reasons for the different transloca-
Site 1 6.2a 19.2b 7.0a 0.1ns tion of metals (Bonanno, 2011; Du Laing et al., 2009; Kim et al.,
Organ 2 3.6a 87.3c 33.3c 81.6c 2003). On the other hand, the high concentration of Fe in the
Month  site 11 3.4b 1.4ns 2.7a 1.4ns
below-ground organs of P. australis could be due to the presence of
Month  organ 22 0.5ns 2.7a 3.8b 2.2a
Site  organ 2 1.1ns 27.9c 15.5c 0.2ns an iron plaque around the root. Iron plaques are commonly observed
Month  site  organ 22 0.5ns 0.7ns 0.6ns 0.7ns on the roots of wetland plants, and may play a key role in wetlands
ns = not significant (i.e., P > 0.05). df: degree of freedom. constructed to detoxify pollutants and purify water (Wang and
a
P < 0.05. Peverly, 1996). This plaque may protect the root from heavy
b
P < 0.01. metal toxicity by co-precipitation or adsorption of toxic metals
c
P < 0.001. (Ali et al., 2002).

Table 3
Mean  standard error of the bioaccumulation factors from sediment to below-ground organs; and translocation factors from below- to above-ground organs of the trace
elements in Phragmites australis in northern and southern sites of Lake Burullus.

Bioaccumulation factor Translocation factor

North South Mean North South Mean


Cd 83.4  3.6 80.3  5.1 81.8  4.1 1.03  0.02 1.02  0.01 1.02  0.01
Cu 5.1  0.4 7.1  0.2 6.1  0.2 0.80  0.03 0.67  0.03 0.74  0.03
Fe 57.6  2.7 71.6  3.1 64.6  1.5 0.71  0.04 0.58  0.05 0.64  0.05
Zn 11.5  0.8 8.9  0.5 10.2  0.5 0.68  0.04 0.68  0.03 0.68  0.03
24 E.M. Eid, K.H. Shaltout / Ecological Engineering 73 (2014) 17–25

Table 4 in P. australis above-ground organs, makes it suitable for its


Significant Pearson correlation coefficient (P < 0.05) between the trace elements in
phytoextraction from the water and sediment, while the lower
the sediment, water, and Phragmites australis organs in northern and southern sites
of Lake Burullus. Above diagonal represent the positive correlations and below translocation factors for Cu, Fe, and Zn make it suitable for their
diagonal represent the negative correlations. BGO: below-ground organs. phytostabilization.
Northern sites
Water Sediment Stem Leaf BGO
Acknowledgements
Water – Fe Fe Fe
Sediment – Cd Cd Cd, Zn
We thank the anonymous two reviewers for their useful
Stem Cu, Zn – Cd, Cu, Fe, Zn Cd, Cu, Fe comments on an earlier version, and Dr. A. H. Salama for English
Leaf Cu, Zn – Cd, Cu, Fe revision.
BGO –

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