Introduction
Location of study area.
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Contamination of soils by heavy metals, such as Cd, Ni, Zn, Pb, and Cu, has
increased dramatically during the last few decades (Chibuike and Obiora,
2014) due to mining, smelting, manufacturing, use of agricultural
fertilizers and pesticides, municipal waste, traffic emissions, and industrial
effluents (Morgan, 2013; Chibuike and Obiora, 2014). Contamination of soils by
heavy metals is now widespread (Al-Nagger et al., 2013). Land degradation
caused by heavy metals has significant adverse effects on the environment
and ecosystem worldwide (Li et al., 2013; Chen et al., 2015). Dispersion of
heavy metals in irrigated soils and the plants that are growing results in the
contamination of food that may be hazardous to humans and animals (Jolly et al., 2013).
Heavy metals in effluents are poorly soluble in water, and cannot be
degraded; they tend to accumulate in soils and subsequently accumulate in plants (Ghoneim et al., 2014). In addition, heavy
metals persist in soil which then leach down into the groundwater and may
induce enhanced antioxidant enzymatic activities in plants or become
adsorbed with solid soil particles (Iannelli et al., 2002). According to Roy
and McDonald (2013), carrots grown in soils contaminated by Cd have the
potential to cause toxicological problems in men, women, and young children.
Cd uptake by carrot roots was about 5 times more than the
regulatory limits for men, 8 times more for women, and 12 times more for
children. High levels of Cd in soil were identified as causing itai-itai
disease in Toyama Prefecture, Japan; however, soil solution levels similarly
high in Cd do not seem to cause health problems for people living in
Shipham, England (Morgan, 2013). For the Cu-contaminated soils planted with
tomato (Solanum lycopersicum L.), these values would range between 32.9 and
1696.5 mg kg-1, depending on soil properties (Sacristán et al.,
2015). Accumulation of toxic heavy metals in living plant cells results in
various deficiencies, reduction of cell activities, and inhibition of plant
growth (Farooqi et al., 2009).
Transfer of heavy metals from soils to plants is one of the key pathways for
exposure of humans via the food chain. In order to assess risks to health
associated with metals in soils, it is necessary to predict transfer of
heavy metals from soil to tissues of plants for subsequent use in
phytoremediation (Roy and McDonald, 2013; Ye et al., 2014). Heavy metal
pollution is persistent, covert, and irreversible (Wang et al., 2011). This
kind of pollution not only degrades the quality of the food crops,
atmosphere, and water, but also threatens the health of human and animals (Dong
et al., 2011). Excessive intake of the Pb to human body can damage the
nervous, skeletal, endocrine, enzymatic, circulatory, and immune system
(Zhang et al., 2012). The chronic effects of Cd consist of lung cancer,
pulmonary adenocarcinomas, prostatic proliferative lesions, kidney
dysfunction, bone fractures, and hypertension (Brevik et al., 2015).
Soil is a key part of the Earth system as it control the hydrological,
erosional, biological, and geochemical cycles. The soil system also offers
goods, services, and resources to humankind (Berendse et al., 2015; Brevik et al., 2015; Decock et al., 2015; Smith et al., 2015). This is why it is
necessary to research how soils are affected by societies.
Pollution is one of these damaging human activities, and we need more
information and assessment of soil pollution (Mahmoud and El-Kader, 2015;
Riding et al., 2015; Roy and Mcdonald, 2015; Wang et al., 2015). Soil
degradation is now considered a challenge of a global dimension and is
included in environmental policy frameworks. A prime example is the United
Nations Convention to Combat Desertification (UNCCD), which recognizes the
important role of soils in sustainable development and has anticipated the
ambitious aim to achieve zero net land degradation by 2030 (UNCCD, 2012).
Soils have been used to detect the deposition, accumulation, and
distribution of heavy metals in different locations (Alirzayeva et al., 2006;
Onder et al., 2007), but little quantitative information is available on the
contamination of agricultural soils in El-Mahla El-Kobra, Egypt, by heavy
metals. To close this knowledge gap, this study investigated the contamination
of agricultural soil and plants by heavy metals in residential and industrial
areas in El-Mahla El-Kobra, Egypt.
Materials and methods
Site description, samples, and analysis
El-Mahla El-Kobra (Fig. 1) is located at 30∘34′ N, 30∘45′ E.
The dominant sources of heavy metal pollution are waste water irrigation, manure, and sediment applications
for metallic ores. The El-Mahla El-Kobra area is density populated (4.5 million 462 683 km-2) and
contains 183 industrial factories such as for textiles, food, oil, and other industries. The quantity of industrial and
municipal waste water is around 243 500 m3 day-1 (107 500 m3 day-1 municipal sewage and 136 000 m3 day-1 industrial waste water), which discharges into Zefta drain (flow, 354 240 m3 day-1) and drain no. 5 (flow, 265 248 m3 day-1)
without treatment, except 63 627 m3 day-1 municipal waste water
which can be treated at Dawakhlia plant.
Seventy representative soil samples (0–30 cm) in summer 2012 were collected
from cultivated lands of El-Mahla El-Kobra, Egypt, which are irrigated with
drainage water from Zefta drain and drain no. 5, and 15 samples of soil were collected
which is irrigated with water from Baher El Mlah canal (fresh water). The soil samples were
air-dried and ground to pass through a 2 mm screen for chemical analysis. The
soils' pH was determined in a saturated soil paste extract (Richards, 1954).
Calcium and magnesium levels were determined titrimetrically using versenate
(Jackson, 1973). The level of sodium was determined using a flame photometer (Richards,
1954). The level of total carbonate was determined using the calcimeter as a CaCO3 percentage
according to Loeppert and Suarez (1996). The total heavy metals (Cd,
Pb, Zn, Fe, Mn, Cu, and Ni) were measured by the atomic absorption
spectrophotometer after the soil samples had digested concentrated
mixtures of HNO3 and HClO4 acids (Page, 1982). Samples of rice and
maize cultivated crops (age 65 days in summer 2012) that are grown in the
studied soils, and three other aquatic plant species (Cynodon dactylon, Phragmites australis, and Typha domingensis) which are grown in Zefta drain, were also collected at different times. The plant samples
were dried in an oven at 75 ∘C for 72 h. The total heavy metals
content in plant shoots was measured using the atomic absorption
spectrophotometer after the plant samples had digested concentrated
H2SO4 and H2O2 (Chapman and Pratt, 1961).
Transfer of heavy metals
The bioconcentration factor (BF) of each metal in plants was calculated by
dividing the total content in the plants by the total content in soil (Brooks,
1998). In addition, 17 water samples were collected from Zefta drain
and drain no. 5 at different times (March 2012 to March 2013) at about 20 cm
below the water surface and were chemically analysed for pH, electrical conductivity (EC), sodium adsorption
ratio (SAR), biological oxygen demand (BOD), chemical oxygen demand (COD),
and heavy metals content (APHA, 2005). The bioaccumulation coefficients of
each heavy metal in aquatic plants were calculated by dividing the total
heavy metal content in aquatic plants by the concentration in water.
The contaminant factor (Cf) for soil is the ratio obtained by dividing the
concentration of each heavy metal in the sediment by the background values
(Håkanson, 1980).
Cf=CHeavy metal/CBackground
According to Håkanson (1980), the values of Cf < 1 indicate low
contamination; 1 < Cf < 3 indicates moderate contamination; 3 < Cf < 6 indicates considerable contamination;
and Cf > 6 indicates very high contamination.
Total concentrations of heavy metals in soils irrigated by
contaminated water from Zefta drain, drain no. 5, and Baher El Mlah canal.
Surrounding soils
Parameters
Unit
Drain no. 5
Zefta drain
Baher El Mlah
Upper limit of total
heavy metals in soils
(Chen et al., 1992)
pH
–
7.80–8.30
7.80–8.50
7.30
–
CaCO3
%
4.10–8.20
3.28–5.74
4.10
–
Fe
mg kg-1
1226–4989
1790–4757
933
–
Zn
mg kg-1
102–187
184–449
54
120
Mn
mg kg-1
341–800
172–853
264
–
Cu
mg kg-1
82–167
123–386
60
35
Cd
mg kg-1
13–28
21–33
11
3
Pb
mg kg-1
48–92
55–80
53
120
Ni
mg kg-1
55–133
104–164
31
60
Concentration of heavy metals in maize and rice shoots grown in
soils irrigated by water from Zefta drain and drain no. 5.
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Results and discussion
Effect of contaminated water on plant and soil contamination
Heavy metals content was higher in rice and maize shoots grown in the soil
around the Zefta drain than the same crops in soil irrigated by water from drain no. 5 (Fig. 2). This
was due to the high total heavy metal contents in these soils (Table 1). Maize shoots
contained more Fe, Cd, Mn, and Pb than rice shoots, and this may be
attributed to the planting of rice under flooded conditions. Under flooded
conditions, Fe, Cd, Mn, and Pb could be precipitate as FeS2, CdS, MnS,
and PbS, respectively, due to the reducing conditions. Heavy metals content
in rice and maize shoots exceeded the defined limits reported by
Kabata-Pendias and Pendias (1992) and were above the levels acceptable for elemental
composition of uncontaminated plant tissue. Alloway (1990) reported that in
angiosperms, uncontaminated plant tissue contains 0.64, 2.4, 160, and 14 mg kg-1
of Cd, Pb, Zn, and Cu, respectively. It is clear from Fig. 2 and
Table 1 that the concentrations of Cd in rice and maize shoots are higher than other
heavy metals compared with the maximum limits according to Kabata-Pendias
and Pendias (1992). Li et al. (1994) found that plants absorb Cd
more readily than other heavy metals and levels are often reached that are hazardous to
human health before any stress symptoms appear. Chitdeshwari et al. (2002)
reported that the use of sewage water increased the uptake of Cd and Cr in
Amaranthus crops. Phosphate fertilizers were sources of Cd used in fertilization of rice
and maize plants in this study area. Phosphate fertilizers were even measured to contain 200 mg Cd kg-1 (Nziguheba and Smolders, 2008). The city of El-Mahla
El-Kobra is densely populated and is the capital of the local textile
industry. Large amounts of industrial and contaminated water are discharged
directly into irrigation canals without treatment, which often contain heavy
metals that contribute to metals' enrichment in soil (Fakayode and Onianwa,
2002). In addition, rice and wheat ash fertilization is carried out in El-Mahla El-Kobra on a large scale (Abou-Sekkina et al., 2010). Application of
ash to agricultural soils contributes significantly to the greater
concentration of Cd in agricultural soil from El-Mahla El-Kobra. The higher
concentration of Zn observed might be due to abrasion of tyres, barks, and
Zn-containing compounds, which are used in some manufactured goods, such as
paints, cosmetics, automobile tyres, and batteries (Imperato et al., 2003).
Bioconcentration factors of heavy metals in maize and rice shoots
grown in soils irrigated by waste water from Zefta drain, drain no. 5, and
limits of heavy metals.
Drain no. 5
Zefta drain
Elements
Rice
Maize
Rice
Maize
Limits of heavy
metals1 mg kg-1
Fe
0.29
0.35
0.54
0.34
–
Mn
3.40
2.97
1.71
1.51
300–500
Cu
0.59
1.54
1.75
1.83
20–100
Zn
2.82
1.71
1.44
1.32
100–400
Pb
6.73
6.83
5.26
5.66
30–300
Cd
6.14
6.45
6.55
2.26
5–30
1 Kabata-Pendias and Pendias (1992).
The range of pH, EC, and heavy metal contents in soil samples which are irrigated
by water from Zefta drain, drain no. 5, and Baher El Mlah are compared with background
limits (Table 3). The soils irrigated by contaminated water from
Zefta drain and drain no. 5 show an increase of soil pH with comparison to
soils irrigated by water from Baher El Mlah (fresh water). Similar results were
noticed by Gupta et al. (2010) and Saffari and Saffari (2013), who reported that
after irrigation with sewage water, pH increased significantly. The reason
for an increasing soil pH may be attributed to high pH values in Zefta drain
and drain no. 5 (Table 3). The soils irrigated by contaminated water from
Zefta drain and drain no. 5 affect the total dissolved solids (TDSs) (Table 3). Indeed, in comparison
to soils which are irrigated by water from Baher El Mlah, the TDS value is greater
in Zefta drain and drain no. 5. These results were in agreement with
Mollahoseini (2013) and Khaskhoussy et al. (2013), who reported that irrigating
with sewage water increased soil salinity, exchangeable Na, K, Ca, Mg, and
available P. In general, the concentrations of heavy metals in soils
irrigated by water from Zefta drain and drain no. 5 exceeded the upper
background limit of total heavy metals (Chen et al., 1992). Contents of Mn, Cd, and
Ni in soils at Zefta drain were higher than in soils at drain no. 5,
due to the high concentration of heavy metals in Zefta drain water
(Table 3). The level of heavy metals of soils irrigated by water from Zefta drain and
drain no. 5 was higher than the levels of the surrounding soils of Baher El Mlah
canal. Similar results were reported by Chen et al. (1992), who found
high levels of heavy metals in soils which are irrigated by polluted
industrial waste water. These results coincided with El-Gendi et al. (1997)
who indicated that irrigating sandy soil in the Abou-Rawash area with
drainage water increased total Cu, Zn, and Fe, which reached 125, 170, and 5
times that of the virgin soil in the same area. Both Cd and Pb levels in
soils measured during this study were higher than those reported by Nassef
et al. (2006) and Suciu et al. (2008). These differences might be related to
different anthropogenic activities and concentrations of urbanization at
each site.
The chemical analysis of water collected from the Zefta drain, drain
no. 5, and Baher El Mlah canal.
Parameters
Units
Drain no. 5
Zefta drain
Baher El
Water criteria for
Mlah
irrigation water
pH
–
9.80
12.2
7.20
6.5–8.4
TDS
mg L-1
1016
1130
334
2000
SAR
–
17.3
18.2
6.00
6–12
BOD
mg L-1
540–723
442–632
0.00
401
COD
mg L-1
882–2301
978–2445
0.00
601
Fe
mg L-1
0.09
0.56
0.01
5.0
Zn
mg L-1
0.02
0.037
0.00
2.00
Mn
mg L-1
0.68
2.91
0.03
0.20
Cu
mg L-1
0.15
0.28
0.12
0.20
Cd
mg L-1
0.03
0.07
0.001
0.01
Pb
mg L-1
1.05
0.18
0.05
5.00
Ni
mg L-1
0.12
0.31
0.02
0.20
1 Egyptian Chemical Standards (48/1992).
Bioconcentration factors (BFs)
The BF values in the rice and maize shoots are presented in Table 2. In
rice and maize grown in soils irrigated by water from Zefta drain and drain
no. 5, the BF values for Cd, Pb, Zn, Cu, and Mn were higher than 1. This
indicates that bioconcentrations of Cd, Pb, Cu, and Mn were high in the plants studied. Fe was an exception because its BF
value was lower than 1, indicating low accumulation in studied plants. The
BF values for Zn and Cu of rice shoots were higher than maize shoots grown in
the same soils irrigated by water from Zefta drain and drain no. 5. These
concentrations were attributed to using ZnSO4 as Zn fertilizer in rice
cultivation. Zhao et al. (2010) reported that BF values tend to decrease
with increasing soil heavy metal concentration, and values lower than 0.20
are considered normal when plants are grown on polluted soils (McGrath and
Zhao, 2003). The differences in the obtained BF values depend on the
heavy metals and the plant species. The higher BF value for Cd indicates
that Cd accumulated in rice and maize shoots. These differences might be
related to heavy metal-binding capacity to roots (Toth et al., 2009),
available metals, interactions between physicochemical parameters, and
the plant species grown in these soils (Bose and Bhattacharyya, 2008).
Quality of drainage water
Concentrations of BOD and COD ranged from 442 and 978 to 632 and
2445 mg L-1 in Zefta drain, while the BOD and COD value ranged from 540
and 882 to 723 and 2301 mg L-1 in drain no. 5 (Table 3). This water would be classified as high strength (Metcalf and
Eddy, 2003). These results were in agreement with Pescond (1992), who
reported that chemical properties of water include total dissolved solids
(TDSs); BOD and COD showed higher values in untreated sewage water compared
to groundwater. The BOD / COD ratio in Zefta drain and drain no. 5 ranged from
0.25 and 0.31 to 0.45 and 0.61, respectively. The waste water with a BOD / COD
ratio below 0.50 contains some toxic components such as dyes and heavy
metals (Linsley et al., 1992).
The average TDSs was 1016 in drain no. 5, 1130 in Zefta drain, and 334 mg L-1
in Baher El Mlah canal. The SARs in water of Zefta drain and drain no. 5 were above 12, which is considered a potential level for
aggregate slaking, soil swelling, and clay dispersion, and thus reduction in
hydraulic conductivity (Mace and Amrhein, 2001). The heavy metals in the two
drains were higher than in the water of Baher El Mlah canal which could be
attributed to discharge of industrial waste water into the two drains without
treatment. The level of heavy metals exceeded the criteria limits for
irrigation water (FAO, 2010; E.C.S, 48/1992). Similar results reported
by Matloub and Mehana (1998) showed that sewage often has high values of
temperature, pH, hardness, alkalinity, COD, TDS, NO3-,
NO2-, Na, K, Ca, and Mg. Chitdeshwari et al. (2002) reported that
increased levels of sewage water increased the uptake of Cd and Cr in
Amaranthus crops.
Average heavy metal concentrations, contaminant factor, and
distribution coefficients (Kd) in sediments of drain no. 5 compared with
toxicological reference values (US EPA, 1999).
Conc. (mg kg-1)
Element
mean ± SD
Et
Cf
Kd (L kg-1)
Zn
647.5 ± 36.7
110
6.25
32375.0
Mn
2125.0 ± 74.3
–
12.7
3125.0
Cu
425.0 ± 12.4
16
4.25
2833.3
Cd
97.5 ± 4.6
0.6
9.55
3250.0
Pb
145.0 ± 4.5
31
4.80
138.10
Ni
195.0 ± 9.8
–
7.33
1625.0
Et: US EPA toxicity reference value; Cf: contaminant factor; Kd: distribution coefficients (L kg-1).
Heavy metal concentrations in sediments
The high heavy metal concentrations in sediments of drain no. 5 (Table 4)
can be attributed to higher pH in water which can form ions of insoluble
precipitates. The measured concentrations of heavy metals are higher than US
Environmental Protection Agency (EPA) toxicity values (US EPA, 1999). Similar findings
were reported by Thuy et al. (2007) who found that heavy metals in sediments of five canals which received
untreated industrial waste water exceeded the US EPA toxicity levels. The
partitioning of heavy metals between sediment and water can be expressed by
distribution coefficient (Kd) values (L kg-1). Kd values of sediment
samples were the highest for Zn, Cd, and Mn, and lowest for Pb, Cu, and Ni.
The higher Kd value indicates that the sorption of heavy metals by sediments
was strong (Salomons and Forstner, 1980). Sediments are both carriers and
potential sources of contaminants in aquatic systems, and these materials also
affect groundwater quality and agricultural products when disposed of on land.
In this study, the mean Cf values of the drain no. 5 sediments revealed that
Zn, Mn, Cu, Cd, Pb, and Ni > 6, indicating very high contamination
due to the direct discharge of waste water from the residential and industrial
areas.
Bioaccumulation coefficients of heavy metals in Typha domingensis, Phragmites australis, and Cynodon
dactylon plants grown in Zefta drain.
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Bioaccumulation coefficients of aquatic plants
The bioaccumulation coefficients of heavy metals in plants of Cynodon, dactylon, Phragmites australis, and Typha domingensis grown in Zefta drain
are shown in Fig. 3. The bioaccumulation coefficients of metals in
Cynodon dactylon were higher than in Phragmites australis and Typha domingensis. These plant species can be considered as
hyperaccumulators, and are used for the decontamination of contaminated water. The
use of plants for decontamination of polluted waters has been described as
rhizofiltration (Brooks, 1998). The three species would be useful for
phytoremediation of contaminated water in a particular area. Bonanno (2013)
showed that Phragmites australis and Typha domingensis species may be used as biomonitors of trace element
contamination in sediment. Overall, T. domingensis and P. australis showed a greater capacity of
bioaccumulation as well as a greater efficiency of element removal than A. donax. In
particular, T. domingensis and P. australis may be used for Hg phytostabilization; the former
also acted as a hyperaccumulator for trace elements' phytoextraction and
phytostabilization. In contaminated wetlands, the presence of T. domingensis and P. australis may
increase the general retention of trace elements. Wafaa et al. (2010)
demonstrated that Phragmites australis and Tamarix aphllya species are significant as vegetation filters and for
cleaning the soils from contamination by heavy metals by phytoextraction.
Antioxidant thiol compounds were probably involved in the mechanisms used
by P. australis to alleviate metal toxicity. As P. australis is considered suitable for
phytostabilizing metal-contaminated sediments, understanding its tolerance
mechanisms to toxic metals is important to optimize the conditions for
applying this plant in phytoremediation (Rocha et al., 2014).