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Science of the Total Environment 512–513 (2015) 1–7

Contents lists available at ScienceDirect

Science of the Total Environment
journal homepage: www.elsevier.com/locate/scitotenv

The effect of long-term wastewater irrigation on accumulation and
transfer of heavy metals in Cupressus sempervirens leaves and
adjacent soils
Emad Farahat a,b,⁎, Hans W. Linderholm b
a
b

Botany and Microbiology Department, Faculty of Science, Helwan University, Cairo, Egypt
Regional Climate Group, Department of Earth Sciences, University of Gothenburg, Gothenburg, Sweden

H I G H L I G H T S
• We studied the impacts of treated wastewater (TWW) on nutrients concentrations in green and senesced leaves of Cupressus sempervirens and soil in three desert plantations
• The species accumulated high amounts of Zn, Mn, Cu and Cd in senesced leaves compared to green
• Transfer factor of Zn and Cu from soil to trees was 2-15 times > that reported for forage crops
• Stoichiometric ratios were decreased under TWW irrigation
• A considerable amount of heavy metals return by senesced leaves to soil

a r t i c l e

i n f o

Article history:
Received 8 December 2014
Received in revised form 7 January 2015
Accepted 13 January 2015
Available online xxxx
Editor: Charlotte Poschenrieder
Keywords:
Cupressus sempervirens
Wastewater irrigation
Senesced tissues
Macro-nutrients
Heavy metals
Transfer and enrichment factor

a b s t r a c t
Wastewater reuse for agriculture is an important management strategy in areas with limited freshwater resources, yielding potential economic and environmental benefits. Here the effects of long-term irrigation with
wastewater on the nutrient contents of green and senesced leaves of Cupressus sempervirens L. were assessed
for three planted forests in Egypt. Stoichiometric ratios, transfer factors for nutrients from soil to plant and enrichment factors in contaminated soils were estimated and compared to a ground water irrigated control site. Under
wastewater irrigation, C. sempervirens transferred most of the estimated nutrients, particularly heavy metals,
from green to senesced leaves. This could be a self-protecting mechanism under continuous wastewater irrigation. The accumulation of four metals (Zn, Mn, Cu and Cd) with transfer factors N 1 for wastewater-irrigated
trees, indicated the ability for metal accumulation of C. sempervirens. Stoichiometric ratios decreased under
wastewater irrigation compared to the control site and global trends, which suggests nutrient disorders in
these plants. The values of enrichment factors in the wastewater-irrigated soils showed remarkable availability
and distribution of metals. Decreased resorption of metals by senesced leaves of C. sempervirens will add considerable amount of these metals to the soils, which will likely have adverse affects on the desert ecosystem
components.
© 2015 Elsevier B.V. All rights reserved.

1. Introduction
In Mediterranean countries, natural water resources are limited,
whereas their demand is constantly increasing. Thus, in this region,
and other arid and semi-arid regions confronted with increasing
water shortages, treated municipal wastewater is a valuable source
for recycling and reuse of water, and commonly used in agriculture
⁎ Corresponding author at: Botany and Microbiology Department, Faculty of Science,
Helwan University, Cairo, Egypt.
E-mail addresses: [email protected] (E. Farahat), [email protected]
(H.W. Linderholm).

http://dx.doi.org/10.1016/j.scitotenv.2015.01.032
0048-9697/© 2015 Elsevier B.V. All rights reserved.

(Pedrero et al., 2012). Consequently, there is a considerable interest
in the long-term effects of treated wastewater on the quality of crops
intended for human consumption (Klay et al., 2010; Belaida et al.,
2012; Pedrero et al., 2012). Wastewater can provide an important supplementary of some nutrients which have favorable effect on the
growth of certain crops. However, it can also cause soil quality modification by structure deterioration and soil pollution by hazardous elements such as metals (Bahri, 1995; Pedrero et al., 2010; Belaida et al.,
2012). The rate of metal uptake by plants remains difficult to forecast,
since it depends on a great number of factors, including metal speciation in soil and plant species (Belaida et al., 2012). Despite this being a
problem that may have direct impacts on consumer's health and the

2

E. Farahat, H.W. Linderholm / Science of the Total Environment 512–513 (2015) 1–7

environmental quality, the extent of accumulation of nutrients and
heavy metals in soils and plants due to wastewater irrigation has not
been adequately studied (Pedrero et al., 2010).
The main cultivation purposes of Cupressus sempervirens and other
woody trees in Egypt are to produce commercial wood for building
uses, fire wood, purifying the air by reducing air pollution and to reduce
the importation of wood from abroad (MESA, 2009). The wood of this
species is valued for its resistance to decay (Farjon, 2013). Environmentally, we found that C. sempervirens is a shelter for some understory
weed species and some birds (Farahat and Linderholm, 2012; Farahat
et al., 2012). By extensive cultivation of the species in Egyptian deserts,
the extraction of its essential oils for medicinal and commercial purposes will be economically important.
In Egypt, a few studies have focused on the impacts of wastewater
on native understory vegetation in terms of biodiversity, sizestructure, biochemical products and mineral content (Farahat and
Linderholm, 2012, 2013), and the effects, including growth dynamics
and ecological traits, of wastewater irrigation on several tree species
(Eucalyptus camaldulensis, Khaya senegalensis, Dalbergia sissoo,
C. sempervirens, Casuarina spp. and Pinus eldarica) have been described
previously (Farahat, 2011; Farahat and Linderholm, 2011; Tabari et al.,
2011). However, relatively little is known about the effect of continuous
application of wastewater on mature trees or age series of planted forest
tree species (e.g., Pereira et al., 2011), and the impact of long-term
wastewater application on the nutrient and heavy metal concentration
in green and senesced leaves in mature forest tress has, to our knowledge, not yet been studied. Such studies are important to fill the knowledge gaps related to the potential effects that the wastewater reuse
practices might induce on human health and the environment.
The overall goal of this study was to investigate the effect of 15 years
application of treated wastewater on the mineral content of green and
senesced leaves of C. sempervirens in two desert plantations and compare that to trees irrigated by ground water at another site. In addition,
the transfer of available heavy metals to the leaves and its enrichment in
the soils adjacent to the trees were assessed. Estimation of nutrient
contents in senesced and green leaves will enable us to determine the
strategy of the species to cope with continuous water and nutrient
availability and help in improving our understanding to the removal
efficiency of nutrients and heavy metals from wastewater by trees.

2. Material and methods
2.1. Study sites
The present investigation was conducted in three desert forests
plantations in Egypt, where two forests, Sadat Forest (30°27′56.11″
N, 30°35′12.58″ E) and Sarapium Forest (30°30′36.79″ N, 32°19′
28.38″ E) are irrigated by treated wastewater. The third forest
(Wadi El-Natrun, 30°28′11.04″ N, 30°11′5.18″ E) is irrigated by
ground water and was chosen as a control site (see Fig. 1 for the location of the sites). The treatment of wastewater in Sadat forest is
primary, where oxidation pools are used for precipitating the
suspended solid particulates and then the lightly treated water is directly used for irrigation. In Sadat forest, wastewater is mixed with
variable amounts of industrial water effluents. Treatment of wastewater in Sarapium forest is primary and secondary (MESA, 2009).
Drip irrigation is applied in both forests. The understory vegetation
was composed of native desert plants and agricultural weeds.
Rooting depths of the trees confined to the superficial moist soil
below the irrigation pipes, which could be attributed to the application of drip irrigation system (Personal observations) (see Farahat
and Linderholm (2012, 2013) for detailed information about these
forests and its soil physical analysis).
The study sites are characterized by mild winters and hot summers:
the mean temperature of the hottest month is 28 °C (daily average),
while total annual precipitation is around 30 mm year−1 (Ayyad and
Ghabbour, 1986).

2.2. Selected species
C. sempervirens L. (Italian cypress, Family Cupressaceae) is a
medium-sized coniferous evergreen tree that can reach heights of up
to 35 m. It is native to North America, Africa, southeastern Europe and
western Asia. It is cultivated in desert plantations in Egypt as a single
overstory species (Farahat and Linderholm, 2012). The average mean
density of the species in the study sites ranged from 1213 trees ha−1
in Sadat forest to 825 trees ha−1 in Sarapium forest with mean ages of
15 years (Farahat and Linderholm, 2011).

Fig. 1. Location map showing the planted forest sites of the present study.

E. Farahat, H.W. Linderholm / Science of the Total Environment 512–513 (2015) 1–7

2.3. Field sampling and laboratory analysis
In early June 2012, which is the peak growth period, small leafy
branches (hereafter referred to as leaves) with their carrying scale
leaves (10 branches per individual) were collected randomly from five
marked individuals at each forest. All leaves from the ten branches
were subsequently pooled into a composite sample for each individual
for further chemical analysis. In autumn (late September to early
October), similar collections were made for senescing leaves (yellow
and ready to drop) from the same marked individuals by gently clipping
off the branches (Aerts et al., 2007). The time of sampling was determined according to the reported phenology for the two species in
Egypt (Abou-Gazia and EL-Baha, 1989; personal observation) and
following the protocols of Lü and Han (2010). The leaf samples were immediately taken to the laboratory, oven dried at 60 °C for at least 48 h,
and then finely ground in an electric mill. Nitrogen and carbon concentrations were analyzed by the Fisons EA-1108 CHNS-O Elemental Analyzer (Fisons, Milan, Italy). For the other elements, 0.5 g dry samples
were ashed at 550 °C in muffle furnace for 3 h and then digested with
10 ml nitric acid (2.8%) overnight. The sample volume was brought to
50 ml using ultra-pure distilled water. The solutions were analyzed for
P, Na, K, Mg, Ca, Pb, Zn, Ni, Mn, Cu, Cd and Pb using ICP-MS (Agilent
7500). Nutrient concentrations in dry leaves expressed in mg g−1 dry
matter (DM) for macronutrients and in μg g− 1 DM for trace metals.
Nutrient analysis was conducted at the University of Gothenburg,
Sweden.
2.4. Transfer and enrichment factor
In order to investigate the relationship between the heavy metals
content of the soils and corresponding trees, the transfer factor (TF), defined as the ratio of heavy metal concentration in trees to that in soil,
was applied to assess the plants' capability to absorb heavy metals
from the soil (Barman et al., 2000; Gupta et al., 2008). A TF N 1 suggests
a possibility of heavy metal accumulation. However, it must be taken
into account that the dry matter basis of the ratio of plant biomass
and soil differ due to the specific weight of respective material, so that
the TF figures must be seen as relative but not absolute numbers
(Gupta et al., 2008).
TF ¼

Concentration of metals plant tissues ðpartsÞ at forest site
Concentration of metals in corresponding soil

We also calculated the enrichment factor (EF) which is used to derive the degree of soil contamination and heavy metals accumulation
in soil and plants growing on contaminated sites with respect to those
from uncontaminated sites (Kisku et al., 2000).
EF ¼

Concentration of metals in soil or plant parts at forest site
Concentration of metals in soil or plant parts at control site

type). Salinity was evaluated using a conductivity meter (dS m− 1).
Soluble soil cations (Na, K, Ca, Mg and P) were determined by atomic absorption spectrometer. The total and soluble nitrogen were determined
by the Kjeldahl method. For total heavy metal concentrations, soil
subsamples were digested by concentrated mineral acids. The metal
concentrations in the soil extracts were analyzed for Mn, Ni, Zn, Cu, Cd
and Pb using atomic spectrophotometer. The analytical methods in
soil samples were according to Allen et al. (1986).
Water samples were collected in plastic bottles directly from the
main pipe feeds in each forest and brought to the laboratory shortly
after collection. Both pH and EC were determined directly after collection, after which the samples were kept at − 4 °C for further analysis.
Ca, Mg, Na, Ka and N were estimated using the same methods as in
the soil analysis. It worth to note that there is no any documented periodical analysis data for water or soil in the studied forests due to the
absence of monitoring program for wastewater in this zone.
2.6. Data analysis
We used paired t-tests to test the differences between the nutrient
concentrations in green and senesced leaves from the three sampled
forest sites. The nutrient concentrations in the senesced leaves were
considered as direct indicators of nutrient resorption proficiency (RP),
which is defined as the absolute level to which a nutrient is reduced
in senesced leaves, and is an index for nutrient conservation in plants
(Aerts, 1996; Killingbeck, 1996). The significant variations in stoichiometric ratios (C:N:P) in green and senesced leaves among the sites
were tested using one-way ANOVA. In addition, one-way ANOVA was
carried out to test any significant differences among different sites in
water and soil characteristics. All statistical tests were conducted
using IBM-SPSS version 20.0 (SPSS, 2006). In all analyses, P b 0.05 was
set as the criterion for significant differences.
3. Results
3.1. Nutrient concentrations
For macro-nutrients, there were significant variations in N, P and K
contents in green and senesced leaves, in addition to C and Ca in
senesced shoots only (Table 1). The concentration ranges for N, P and
K in green (senesced) leaves were as follows: 5.7–14.3 (6.3–15.4),
1.5–4.1 (1.1–4.8) and 6.8–12.2 (6.3–15.2) mg g−1 DM, respectively. It
is apparent that the control site had the lowest concentrations of most
analyzed nutrients compared to the other sites. In addition, the
senesced leaves had higher nutrient concentrations than the green
ones for most nutrients.
Table 1
Variations in the mean ± standard deviation of macro-nutrients (as mg g−1 DM) in green
(gr) and senesced (sen) shoots of Cupressus sempervirens. Significance at p b 0.05.
Forest sites

2.5. Soil and water analysis

Variable Shoot Control

Soil samples were taken under the canopy of Cypress trees at three
stands in each forest. At each stand, soil samples were collected randomly with a shovel from 0–50 cm depth at three random locations
and pooled to obtain one composite sample. The soil samples were
brought to the laboratory in plastic bags shortly after collection, spread
over paper sheets; air dried, passed through a 2 mm sieve to remove
gravel and debris, and then packed in paper bags ready for physical
and chemical analysis. Soil extracts were prepared to meet the requirements for different determinants, 1:5 (w: v) soil (g): distilled water
(ml) extract. This extract was used to measure soil electrical conductivity (EC), pH, Na, K, Ca, Mg, P and N. The pH values of soil samples were
determined using a glass electrode pH meter (Model 9107 BN, ORION

3

C

gr
sen

N

gr
sen

P

gr
sen

Na

gr
sen

K

gr
sen

Ca

gr
sen

Mg

gr
sen

Sarapium

Sadat

F-value Probability

446.6 ± 2.8
460.4 ± 6.6
453.9 ± 9.8
2.9
315.0 ± 57.7 433.9 ± 11.8 440.2 ± 33.2
9.8
5.7 ± 0.6
14.3 ± 4.8
14.2 ± 1.0
9.1
6.3 ± 0.8
15.4 ± 4.0
15.3 ± 0.7
14.1
1.5 ± 0.4
2.3 ± 1.0
4.1 ± 1.4
5.4
1.1 ± 0.1
3.7 ± 0.9
4.8 ± 1.2
14.8
3.1 ± 1.1
7.4 ± 6.6
6.3 ± 2.4
0.9
12.3 ± 0.0
11.2 ± 2.0
10.5 ± 0.5
0.1
12.2 ± 0.7
6.8 ± 2.5
11.9 ± 1.9
7.9
6.3 ± 2.5
12.4 ± 1.1
15.2 ± 1.7
25.5
33.2 ± 3.9
22.5 ± 1.1
33.0 ± 2.0
2.4
62.9 ± 7.2
31.0 ± 4.2
37.9 ± 1.7
9.8
4.0 ± 0.3
5.4 ± 0.2
6.6 ± 0.1
3.1
7.7 ± 0.6
8.0 ± 1.6
7.3 ± 0.3
0.08

0.131
0.013
0.015
0.005
0.045
0.005
0.450
0.901
0.022
0.001
0.168
0.013
0.117
0.926

4

E. Farahat, H.W. Linderholm / Science of the Total Environment 512–513 (2015) 1–7

Table 2
Trace metals mean (±SD) concentrations (μg g−1 DM) in green (gr) and senesced (sen)
shoots of Cupressus sempervirens. Significance at p b 0.05.

Table 3
Descriptive statistical results of transfer factors (TF) of heavy metals from soil to trees, and
enrichment factor (EF) soil shoot tissues.

Forest sites
Variable Shoot Control
Zn

gr
sen

Mn

gr
sen

Cu

gr
sen

Ni

gr
sen

Cd

gr
sen

Pb

gr
sen

Transfer factor
Sarapium

10.6 ± 2.1
41.6 ± 8.5
29.5 ± 0.8
15.2 ± 0.4
108.7 ± 3.6
57.0 ± 1.5
234.1 ± 5.3
115.4 ± 2.8
6.7 ± 0.5
9.1 ± 0.7
15.8 ± 1.3
9.4 ± 2.5
3.7 ± 0.8
4.7 ± 1.2
14.6 ± 1.5
7.0 ± 2.2
0.05 ± 0.01
0.06 ± 0.0
0.09 ± 0.00
0.06 ± 0.01
1.6 ± 0.3
3.2 ± 0.6
8.3 ± 0.5
4.8 ± 0.4

Sadat

Enrichment factor

F-value Probability

27.6 ± 0.8
15.0
24.4 ± 0.8
3.0
77.2 ± 6.7
3.8
97.1 ± 3.7
9.8
8.7 ± 1.3
5.9
10.3 ± 2.2
8.4
3.6 ± 0.6
1.5
6.5 ± 1.1
22.6
0.05 ± 0.02
0.1
0.05 ± 0.00 16.8
3.2 ± 0.1
4.4
4.5 ± 0.2
6.9

0.005
0.124
0.084
0.013
0.038
0.018
0.298
0.002
0.877
0.003
0.066
0.028

The senesced of C. sempervirens displayed significant variations in
Mn, Cu, Ni, Cd and Pb among the sites, while in the green leaves, the
concentrations of Zn and Cu varied markedly among the sites
(Table 2). The senesced leaves accumulated higher concentrations of essential micronutrients compared to the green ones, particularly at the
control site. For instance, Zn concentration in senesced leaves in control
site was 2.78 times higher than the concentration in green leaves. On
the other hand, Mn concentrations in senesced leaves at all sites were
N2 times higher than the concentrations in green leaves at the control
and Sarapium sites (Table 2). The concentrations of trace metals were
at normal levels and below the phytotoxic concentrations (KabataPendias, 2011), in both green and senesced leaves at all sites.
3.2. Stoichiometric ratios
The results showed that C: N and C: P ratios in senesced and green
leaves were significantly different (at p b 0.05) throughout the studied
sites, where the highest values were obtained at the control site
(Fig. 2a, b). Conversely, the N: P ratios did not differ notably among the

Shoot

Soil

Metal/Site

Control

Sarapium

Sadat

Sarapium

Sadat

Sarapium

Sadat

Zn
Mn
Cu
Ni
Cd
Pb

5.3
4.2
1.5
0.4
2.5
2.0

13.9
1.9
1.7
0.4
2.0
0.5

8.6
1.8
1.6
0.2
1.7
0.4

2.6
0.5
1.1
1.0
0.8
0.2

1.6
0.4
1.0
0.5
0.7
0.2

1.5
1.2
1.2
1.2
1.5
8.9

1.6
1.7
1.2
1.8
1.5
11.0

sites regardless of the leaf type. Mean range of C: N ratio was 32–78.2
and 28.9–50 in green and senesced leaves, respectively. The C:P ratios
ranged from 119.2 to 315.9 in green tissues leaves and from 95.6–
290.7 in senesced leaves. The mean N: P range was 3.7–4.1 and 3.3–5.8
in green and senesced leaves, respectively (Fig. 2a–c).
3.3. Transfer and enrichment factors
The descriptive statistical results for the transfer factor (TF) for
heavy metal from soil to tree leaves (Table 3) led to values of TF N 1
for all heavy metals, except Ni (all sites) and Pb (Sarapium and Sadat
forests). However, the results must be interpreted with caution, and
be viewed as relative data (see above). The uptake capability from soil
to tree leaves at all sites (given as mean values) was in the order Zn
(9.3) N Mn (2.6) N Cd (2.1) N Cu (1.6) N Pb (1) N Ni (0.3). At the control
site, Mn, Cd and Pb were higher than the other two sites (Table 3).
The enrichment factor (EF) in the wastewater irrigated soils and
C. sempervirens leaves were similar for all elements at Sarapium and
Sadat forests, showing a remarkable contamination from Pb (EF = 8.9
and 11.0, respectively) (Table 3). The EF in the leaves showed
values b 1 for Cd and Pb at Sarapium and Sadat forests, and Ni and Mn
at Sadat forest. EF for Zn (1.6, 2.6, respectively) was higher than for
the other metals at both sites (Table 3).
3.4. Soil and water characteristics
The chemical analysis of soil and water variables showed lower
concentration of the analyzed elements at the control site compared
to the other sites. This was particularly evident for total N, soluble N,
soluble P, as well as trace metals (Table 4). On the other hand, soil
and water salinity (expressed as EC.), Mg, K and Na at the control
site and Sadat forest were higher than at Sarapium forest. Soils in
Sadat forest were characterized by the highest concentrations of K
(330.7 mg kg− 1), Mg (165.4 mg kg− 1) and trace metals. The three
forest sites were significantly different (p = 0.05) in all the analyzed
elements in soil (except Na, Ca and Pb) and water samples (except
Cd and Pb). The irrigation water in control site was characterized
by its high EC. (5.1 dS m− 1) and Na concentration (130.2 mg/l).
4. Discussion
4.1. Nutrient concentrations

Fig. 2. a–c. Variations in stoichiometric ratios of green and senesced shoots tissues. Error
bars are standard errors of means.

The presence of high nutrient concentrations and trace metals in the
senesced leaves of C. sempervirens compared to the green ones indicates
a high accumulation efficiency of the species to protect itself from excess elements. We suggest that C. sempervirens removes excess elements by transferring it from green to senesced leaves to cope with
the continuous availability of nutrients from irrigation. This mechanism
protects the trees from high elemental concentrations, but releases
more nutrients and contaminants to the soil through the decomposed
litter (Yang et al., 2004; González-Rodríguez et al., 2011). The spatial

E. Farahat, H.W. Linderholm / Science of the Total Environment 512–513 (2015) 1–7

5

Table 4
Chemical characteristics of soil and water variables in the studied planted forests sites in Egypt. Significant differences (at probability level p b 0.05) among forests sites, based on t-test, are
shown by p-values.
Site

pH

EC (dS m−1)

1—soil (mg/kg)
Sarapium
7.6
Sadat
7.8
Control
7.9
p-value
0.00

2.1
5.2
7.7
0.024

2—water (mg/l)
Sarapium|
7.2
Sadat
7.5
Control
7.8
p-value
0.000

2.1
3.7
5.1
0.009

a

Total Na

Soluble N

P

Na

K

Ca

Mg

Mn

Ni

Cu

Zn

Cd

Pb

0.57
0.55
0.25
0.01

23.0
19.0
5.0
0.031

8.3
7.9
3.1
0.016

234.3
1332.2
1377.7
0.076

138.9
330.7
212.6
0.024

181.5
700.0
269.2
0.09

77.2
165.4
132.7
0.029

30.0
44.0
25.9
0.003

11.3
16.8
9.2
0.005

5.4
5.6
4.5
0.001

3.0
3.2
2.0
0.002

0.03
0.03
0.02
0.002

7.1
8.8
0.8
0.069

53.1
55.5
32.8
0.004

38.1
38
23.9
0.003

0.04
0.03
0.03
0.002

76.3
105.8
130.2
0.007

17.9
23.4
4.9
0.031

151.4
128.3
44.8
0.025

38.6
36.3
14.9
0.023

17.1
29.5
15.5
0.007

7.1
13
8.8
0.005

4.7
5.1
4.8
0.002

3.5
4.2
3.3
0.001

0.06
0.09
0.03
0.06

9.2
12.3
1.4
0.125

Concentration as %.

variations in the elemental composition of C. sempervirens leaves at
different sites may reflect the sensitivity of the species towards the different water qualities and nutrient availability at the study sites. In
addition, the presence of high concentrations of most elements in
green and senesced leaves in trees irrigated by wastewater compared
to control plants refers to the availability of these elements in water
and soil of these sites, which has been previously reported for
Egyptian loamy sand soils irrigated by wastewater (El-Nennah et al.,
1982).
At the control site, the P and K concentrations were higher in green
leaves than in the senesced ones, and the same relationship was found
for Zn at the two wastewater irrigated sites. This way of nutrient conservation (i.e., resorption) in plants may be attributed to the importance of
these elements for plant nutrition. Zinc is a structural constituent and
regulatory co-factor of a wide range of different enzymes in many important biochemical pathways (Alloway, 2008). On the other hand, P
is a component of the complex nucleic acid structure and regulated
the protein synthesis. Adequate supply of P is required for optimum
growth and reproduction (Divito and Sadras, 2014). Potassium is essential to all plant life, and in most terrestrial plants, K+ is the major cationic inorganic nutrient. The role of K+ in plants is: (1) activation of
enzymatic reactions, (2) charge balancing, and (3) osmoregulation
(Mengel., 2007). The resorption of nutrient from senesced leaves is an
important energy mechanism employed by plants to endure nutrient
limitation (Li et al., 2013) (Aerts and Chapin, 2000; Li et al, 2013;
Vourlitis et al., 2014). In the present study, this mechanism is reduced
for heavy metals and the other available nutrients in irrigation water
and soil.

4.2. Stoichiometric ratios
The obtained stoichiometric ratios in senesced leaves of
C. sempervirens in the present study were lower than the reported
global mean (e.g., Kang et al., 2010; Yuan and Chen, 2009). Globally,
N:P ratios have been reported to be 18.3 (Kang et al., 2010) or 19.2
(Yuan and Chen, 2009), which is three times higher than the maximum
value (5.8) recorded in our study. Also, the global C:P ratio (1183) is
about four times higher than our recorded maximum value (315.9),
while the C:N ratio was about half of the global average (52.9, Yuan
and Chen, 2009). We attribute the low stoichiometric ratios in our
study to the relative high N and P concentrations in the senesced leaves,
which positively correlate with the availability of water nutrients
(Sardans et al., 2011). The availability of water and nitrogen in wastewater may affect the plant nutritional and stoichiometric responses
(e.g., Lü et al., 2012). This was emphasized by the relatively high values
of C:N and C:P at the control site compared to the wastewater irrigated
sites. Non-significant N:P ratios among the studied sites, regardless of
the leaf type, is consistent with similar findings of Lü et al. (2012) for
N:P ratio in senesced leaves of semi-arid grasslands.

4.3. Transfer and enrichment factor
Plants grown in metal-enriched substrata take up metal ions in
varying degrees. This uptake depends on the bioavailability of the
metals, which in turn is determined by both external (soil associated)
and internal (plant-associated) factors (Shukla et al., 2011). The transfer
factors (TFs) in our study generally showed a movement of heavy
metals from the soil to the roots and shoots, indicating the efficiency
to uptake of the available metals and give an idea whether the plant is
an accumulator, excluder or indicator (Bose et al., 2008; Galal and
Shehata, 2013). The TF results revealed that C. sempervirens showed
higher biomagnification of some metals in contaminated soils, whereas
the same species showed less accumulation of a particular metal in the
control soil. C. sempervirens showed accumulation of four metals (Zn,
Mn, Cu and Cd) out of six in the soils irrigated by wastewater, and the
TF was N1. According to Zu et al. (2005), a TF N 1 indicates an ability
of plants for metal accumulation. Consequently, the obtained TF value
may indicate that C. sempervirens can accumulate heavy metals, but
the different dry weights of soil and plant mass must be duly considered
in this case, i.e., the ratios must not be taken as absolute accumulation
values (Galal and Shehata, 2013). The TF of Zn and Cu in the leaves
was 2–15 times higher than that reported for forage crops (Alfalafa
and Sorghum) subjected to long-term irrigation by wastewater in
Tunisia (Belaida et al., 2012). Farahat et al. (2007) reported that the foliar application of ascorbic acid and Zn is recommended for increased
vegetative growth of C. sempervirens trees. This may explain the relative
high TF for Zn to tree leaves compared to the other elements.
The EF values were N1 in the soils, which suggest high availability
and distribution of metals in soils irrigated by wastewater. This will likely increase the metal accumulation in plants grown on such contaminated soil (Kisku et al., 2000; Gupta et al., 2008). In comparison, the transfer
values from soil to leaves showed lower values for some metal (e.g., Ni
and Pb) than the EF, and did not follow a similar pattern. This reveals
that the transfer of these elements from soil to leaves is restricted to a
certain extent. Similar values of TF and EF have been noted in soils,
crops and weed plants from an ash-contaminated area in India (Singh
et al., 2010).

4.4. Soil and water characteristics
Using of treated wastewater to irrigate planted forests results in
more available nitrogen, phosphorus and trace metals, which is a common result for wastewater recycling in agriculture. The presence of high
water EC and Na concentration at the control site is likely related to the
high natural soil salinity (Zahran and Willis, 2009). On the other hand,
the presence of high contents of total soluble N and P in soils with
prolonged application of sewage water compared with control sites is
in line with previous studies (e.g., El Keiy, 1983; Waley et al., 1987).
The remarkable high concentration of trace metals in Sadat forest may

6

E. Farahat, H.W. Linderholm / Science of the Total Environment 512–513 (2015) 1–7

be attributed to the industrial wastewater that is mixed with domestic
sewage effluents before treatment. Klay et al. (2010) reported that the
heavy metal content increases with wastewater irrigation period, especially for Pb and Cd. In addition, they found that the pH values of the
water and soil became slightly basic. Thus, the quality of the treatment
and the source of the wastewater play a significant role in the properties
of the soils and leaves.
Plants are essential components of natural ecosystems and
agrosystems, and represent the first compartment of the terrestrial
food chain. Due to their capacity to accumulate toxic metals when growing on soils polluted with heavy metals, they represent a threat to those
who consume them. In addition, high metal concentration may affect
their development and growth, resulting in economic loss. Accordingly,
the application of contaminated wastewater is, in practice, a kind of ecosystem disturbance, where along with the nutrients and water, also potentially toxic substances are introduced to the soils causing the plants
to have to adapt. It was reported that the use of wastewater in urban forests enriched the soils with heavy metals to concentrations that may
pose potential environmental and health risks on the long term due to
their toxicity and persistence in the environment (Wuana and
Okieimen, 2011). On the other hand, wastewater is considered as a
source of harmful pathogenic diseases and the risk of superficial and
groundwater contamination (Singh et al., 2004).
Despite the benefits of wastewater reuse, there is still a knowledge
gap in respect to possible elemental interactions that may influence
the accumulation of heavy metals and other elements in soil and the
subsequent uptake by plants and crops (Fatta-Kassinos et al, 2011).
More studies are needed to better understand the potential effects
that wastewater reuse practices have on ecosystems processes and
human health. Monitoring plans should be designed for these new
agrosystems (planted forests) in deserts to safeguard this environment
and conserve the natural habitats as much as we can. Besides, long-term
monitoring of soil structure, litter decomposition, understory flora and
fauna, and ground water quality should take priority in future management strategies. More new environmental and efficient water treatment
technologies should be applied to reduce the hazards of using wastewater in agricultural practices.
5. Conclusions
The results of this study revealed that, under wastewater irrigation,
C. sempervirens transfer most of the estimated nutrients, particularly,
heavy metals, from green to senesced leaves. The accumulation of four
metals (Zn, Mn, Cu and Cd) and TF values N 1 for wastewater-irrigated
trees, indicating the ability for metal accumulation of C. sempervirens. Our
findings suggest that transferring of excess elements to senesced leaves
is a self-protecting mechanism under continuous wastewater irrigation.
Resorption of some elements from senesced leaves may be a key physiological component contributing to the nutrient balance of Cypress trees.
The spatial variations in the elemental composition of C. sempervirens
leaves at different sites may reflect the sensitivity of the species towards
the different nutrient concentration in the irrigation water. The significant
difference in stoichiometric ratios at wastewater-irrigated sites compared
to the control, as well as the reported global trends, suggests nutrient disorders in these plants. The high enrichment factor in wastewater-irrigated
soils indicates higher availability and distribution of metals. It is necessary
to monitor the concentrations of heavy metals in plants and soils subjected
to long-term wastewater irrigation to avoid toxicity in plants and soils, as
well as major disturbance of the ecosystem.
Acknowledgments
This work was funded by the Swedish Research Council/Swedish
International Development Cooperation Agency SIDA (grant no. 20086087) and Egyptian Ministry of Higher Education and Scientific
Research (ParOwn Initiatives, 2012/13).

Appendix A. Supplementary data
Supplementary data associated with this article can be found in the
online version, at http://dx.doi.org/10.1016/j.scitotenv.2015.01.032.
These data include Google map of the most important areas described
in this article.

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