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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 benets. 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: Emad23_1999@yahoo.com (E. Farahat), Hansl@gvc.gu.se
(H.W. Linderholm).
http://dx.doi.org/10.1016/j.scitotenv.2015.01.032
0048-9697/ 2015 Elsevier B.V. All rights reserved.
Fig. 1. Location map showing the planted forest sites of the present study.
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
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 050 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
gr
sen
gr
sen
gr
sen
Na
gr
sen
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
Table 2
Trace metals mean (SD) concentrations (g g1 DM) in green (gr) and senesced (sen)
shoots of Cupressus sempervirens. Signicance 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
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 3278.2
and 28.950 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 3.74.1 and 3.35.8
in green and senesced leaves, respectively (Fig. 2ac).
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 signicantly 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. ac. Variations in stoichiometric ratios of green and senesced shoots tissues. Error
bars are standard errors of means.
Table 4
Chemical characteristics of soil and water variables in the studied planted forests sites in Egypt. Signicant differences (at probability level p b 0.05) among forests sites, based on t-test, are
shown by p-values.
Site
pH
EC (dS m1)
1soil (mg/kg)
Sarapium
7.6
Sadat
7.8
Control
7.9
p-value
0.00
2.1
5.2
7.7
0.024
2water (mg/l)
Sarapium|
7.2
Sadat
7.5
Control
7.8
p-value
0.000
2.1
3.7
5.1
0.009
Total Na
Soluble N
Na
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 %.
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