w a t e r r e s e a r c h 4 6 ( 2 0 1 2 ) 3 9 6 7 e3 9 7 6

Available online at www.sciencedirect.com

journal homepage: www.elsevier.com/locate/watres

The use of Bassia indica for salt phytoremediation

in constructed wetlands
Oren Shelef a,1, Amit Gross b, Shimon Rachmilevitch a,*
a

French Associates Institute for Agriculture & Biotechnology of Drylands, The Jacob Blaustein Institutes for Desert Research,
Ben-Gurion University of the Negev, Midreshet Ben Gurion 84990, Israel
b
Zuckerberg Institute for Water Research, The Jacob Blaustein Institutes for Desert Research, Ben-Gurion University of the Negev,
Midreshet Ben Gurion 84990, Israel

article info

abstract

Article history:

The treatment and reuse of wastewater in constructed wetlands offers a low-cost, envi-

Received 7 December 2011

ronmentally-friendly alternative for common engineered systems. Salinity in treated

Received in revised form

wastewater is often increased, especially in arid and semi-arid areas, and may harm crops

22 April 2012

irrigated from wetlands. We have strong evidence that halophyte plants are able to reduce

Accepted 13 May 2012

the salinity of wastewater by accumulating salts in their tissues. Bassia indica is an annual

Available online 23 May 2012

halophyte with unique adaptations for salt tolerance. We performed three experiments to
evaluate the capability of B. indica for salt phytoremediation as follows: a hydroponic

Keywords:

system with mixed salt solutions, a recirculated vertical flow constructed wetland (RVFCW)

Constructed wetland

with domestic wastewater, and a vertical flow constructed wetland (VFCW) for treating

Salt phytoremediation

goat farm effluents. B. Indica plants developed successfully in all three systems and reduced

Bassia indica

the effluent salinity by 20e60% in comparison with unplanted systems or systems planted

Desert

with other wetland plants. Salinity reduction was attributed to the accumulation of salts,
mainly Na and K, in the leaves. Our experiments were carried out on an operative scale,
suggesting a novel treatment for green desalination in constructed wetlands by salt phytoremediation in desert regions and other ecosystems.
2012 Elsevier Ltd. All rights reserved.

1.

Introduction

1.1.

Wastewater treatment

Water scarcity has led to the search for alternative water

resources. One solution is the recycling of wastewater (WW)
for irrigation. In Israel, for example, wide areas are irrigated
with treated wastewater, and more than 70% of sewage water
is recycled for agricultural use. Treated wastewater is rich in
nutrients for plants, but is also characterized by a higher
salinity than fresh water. The use of wastewater for irrigation

may reinforce soil salinization since the concentrations of the

dominant ions (Na, Ca, K and Cl) which create the overall
salinity are not reduced (Hillel, 2000).
The salinization of soil and water is a major global environmental problem that may cause land degradation, reduction of water quality and detrimental effects to vegetation
(Schofield et al., 2001). Estimations by the United Nations
Environment Program suggest that 20% of agricultural land
and 50% of cropland in the world is salt-stressed (Flowers and
Yeo, 1995). Salinity in drylands is accelerated by strong sun
radiation and increased evapotranspiration. Larcher (1995)

* Corresponding author. Tel.: 972 8 6563435; fax: 972 8 6596742.

E-mail addresses: shelefo@bgu.ac.il (O. Shelef), amgross@bgu.ac.il (A. Gross), rshimon@bgu.ac.il (S. Rachmilevitch).
1
Albert Katz International School for Desert Studies.
0043-1354/$ e see front matter 2012 Elsevier Ltd. All rights reserved.
doi:10.1016/j.watres.2012.05.020

3968

w a t e r r e s e a r c h 4 6 ( 2 0 1 2 ) 3 9 6 7 e3 9 7 6

suggested that the salinity rate of irrigated crops should not

exceed EC (electric conductivity) values of 2 dS m1. The Israeli
Ministry of Environmental Protection determined, through
the Inbar committee, a level of 1.4 dS m1 as the threshold for
unlimited use of water (Inbar, 2007).
Wastewater treatment is often based on biological systems
such as activated sludge or other engineered units in urban
areas. In rural areas, low-cost, environmentally-friendly
alternative treatments such as constructed wetlands (CW), are
more common. CWs are man-made planted systems that
utilize natural processes to improve water quality for human
benefit (Kadlec and Knight, 1996).

1.2.

Role of plants in CWs

Most treatment processes that occur in CWs are driven by

chemical, physical and biological mechanisms. These mechanisms include oxidation, fragmentation, desorption, sedimentation, microbial biodegradation and uptake (Vymazal,
2007). The role of plants in the CW cleaning process is not
clear (Imfeld et al., 2009; Stottmeister et al., 2003). Brix (1997)
suggested the following potential attributes of plants in
CWs: (1) increasing retention time by reducing water velocities; (2) improving hydraulic conductivity by root growth, and
(3) root activity. By utilizing elements such as (N) and phosphorus (P), plants may affect the elemental composition of
WW. In addition, plants can prevent odor nuisances, enhance
aesthetic appearance, provide surface area for microbial
growth, and be used as bioindicators for CW management
(Shelef et al., 2011). Plant involvement in nutrient cycling and
the exchange between water and sediment affects the water
and sediment quality (Barko et al., 1991; Biernacki and Doust,
1997; Catling et al., 1994; Petticrew and Kalff, 1992).

1.3.

Phytoremediation

Phytoremediation is the use of plants for remedying water and

soil pollution. The treatment of heavy metals in contaminated
lands or water reservoirs has attracted most of the research
attention as it seems to be a promising technology to mitigate
pollution without excavation of the contaminants for
mechanical disposal (Salt et al., 1995a; Weis and Weis, 2004).
Another important target for phytoremediation is the treatment of nutrients, mainly N and P (Singh et al., 2010). Raskin
et al. (1994) suggested the following three types of application: 1) phytoextraction e when plants transport and
concentrate pollutants from the media to aboveground
harvestable shoots; 2) rhizofiltration - when plant roots store
elements used for the accumulation, precipitation and
concentration of contaminants; and 3) phytostabilization e
elimination of toxins through the stabilization of the growth
media by plants, without necessarily involving bioaccumulation in plant tissues.
Several studies have offered means of reducing heavy
metal or other toxic contaminant concentrations (Chaney
et al., 1997; Rascio and Navari-Izzo, 2011; Schwitzguebel
et al., 2009). However, the volumes in which the experiments were carried out were often too small to have any
implications in the practical world (Salt et al., 1995b; Weis and
Weis, 2004). Sklarz et al. (2009) showed that nutrient uptake

may not be significant in relation to water loads in a recirculating vertical flow CW. In the last several years, attempts
have been made to use phytoremediation techniques to find
solutions for soil and water salinization.

1.4.

Salt phytoremediation

This approach is based on plants that are especially tolerant to

salt environments. Around 1% of all plant species are halophytes that can complete their life cycle in relatively high
saline environments, as much as 200 mM NaCl or more
(Flowers and Colmer, 2008; Waisel, 1972). Breckle (2002) classified halophytes as salt-excluders, salt-includers (i.e., Tamarix spp.) and salt-accumulators (as Atriplex spp.).
Phytostabilization can be practiced by all these classifications,
e.g., by growing halophytes on salt affected soils to halt soil
degradation (Keiffer and Ungar, 2002; Young et al., 2011).
However, for the purpose of water phytodesalination, saltincluders are more suitable if they are able to accumulate
sodium in their tissues and reduce the medias sodium
content and overall salinity. This amelioration of salinity has
been reported in soils (Carty et al., 1997; Hbirkou et al., 2011;
Rabhi et al., 2009; Ravindran et al., 2007; Zhao, 1991).
Bassia indica (Wight) A.J. Scott is an annual halophyte,
widespread on disturbed lands throughout Israel. B. indica
plants exhibit a unique phenomenon of halotropism in
which the root seems to search for high salinity in the soil to
enable better conditions for enhanced growth (Shelef et al.,
2010). B. indica was our candidate for salt phytoremediation
due to its following advantages: 1) tolerance for a wide
gradient of salinities; 2) fast growth rate in the summer (up to
9 kg DW (dry weight) in less than a year) that enables a high
uptake under increased evaporation (which increases soil
salinity); 3) accumulation of ions within tissues and not in
specified glands that can be washed easily by water; and 4) B.
indica can be easily removed at the beginning of the blooming
season to avoid seed dispersal.
In the current study, we addressed the problem of soil
salinization due to the use of treated WW that is often more
saline than fresh water, especially in desert environments. We
aimed at testing the potential to recruit halophyte plants for
salt phytoremediation in constructed wetlands. Our main
hypothesis was that halophyte plants can accumulate salts in
their leaves to a level that is high enough to reduce water
salinity in treated WW from CWs. More specifically, we asked
whether B. indica plants can be recruited for salt phytoremediation in constructed wetlands; how tolerable B. indica
plants are for the CW environment for different WW solutions
and for salt solutions; and which elements are accumulated
and in which tissues of the plant.

2.

Materials & methods

2.1.

Establishment

B. indica seeds were collected in the central Negev highlands

near Midreshet Ben Gurion (30 510 N, 34 470 E), Israel. Seeds
were sprouted inside pots in a greenhouse, and then seedlings
were moved to hydroponic containers or to a growing

3969

w a t e r r e s e a r c h 4 6 ( 2 0 1 2 ) 3 9 6 7 e3 9 7 6

medium. Established seedlings were planted in the CWs.

Initial DW/height of seedlings was w0.04 g/5 cm in the
hydroponic experiment and w1 g/25 cm in the CWs. The day
of planting was considered the first day of the experiment.

2.2.

Experimental setup

The use of B. indica plants for water desalination was studied

in a controlled hydroponic system in a greenhouse and in two
field systems that are regarded here as case studies in operational scale. Different CWs exhibit different dynamics of
water flow, oxygenation and nutrient loadings. Therefore the
role of plants in CW is strongly affected from the CW
construction. For example, Vymazal (2011) stressed that the
role of plants in horizontal flow CWs (HFCWs) is significantly
different in comparison to their role in VFCWs. Therefore, to
broaden our impression of B. indica salt phytoremediation
abilities we tested it in different CW systems. In the first
system the plants were planted in a recirculating vertical flow
CW treating domestic wastewater, and in the second, they
were planted in a vertical flow CW treating agro wastewater,
as summarized in Table 1 and described below. Average daily
evaporation measured by a Class A evaporation pan in the
research area ranged between 2 mm in January and 8.6 in
June, and 8.4 mm in July. The potential evapotranspiration
(PET) calculated by the PenmaneMontieth equation reached
a maximum of 6.2 mm d1 (Israel Meteorological Service). B.
indica plants with high surface area had relatively elevated
evapotranspiration as compared to evaporation without
plants. To test water balance we measured daily water loss in
the hydroponic containers.

2.3.

Hydroponic solutions

B. indica plants were grown in 4 l buckets in a greenhouse for

48 days. Four solutions were used: fresh water (EC w1 dS m1),
a mild saline solution (EC w5 dS m1), an intermediate saline
solution (EC w8 dS m1), and a hyper saline solution (EC
w16 dS m1). The mild saline solution was ground saline
water, and the other solutions were artificially enriched with
salts to elevate the salinity while keeping the partial proportions of each element in all systems (Table 1). All four solutions were fertilized with a Long Ashton nutrient solution

(Hewitt, 1966; Ottow et al., 2005). Eight plants were planted in

each container with four containers per treatment as replications. Four containers were used as controls and did not
contain any plants in order to estimate physicochemical
effects such as precipitation and aeration. The control
included one container from each solution (EC w1 dS m1,
w5 dS m1, w8 dS m1 and w16 dS m1). Altogether we had 20
containers (4 replicates for 4 solutions plus 4 controls). Four
cycles of 10 days were used as repetitions in the control
containers. All twenty containers were aerated with small
aquarium air stones (See Fig. 6 in the supplementary data).
After an establishment period of 5 days the solutions in all
buckets were exchanged, and thereafter every 10 days. Water
was sampled before and after exchanges (approximately
every ten days). Water was added daily to compensate for
evaporation and transpiration losses within the containers.
Water additions were recorded to allow calculation of actual
evaporation and evapotranspiration.

2.4.

Recirculating vertical flow CW (RVFCW)

Two identical RVFCWs that are used for treating domestic

WW in Midreshet Ben Gurion, Israel were used. The RVFCWs
are described in detail by Sklarz et al. (2009) and briefly in the
supplementary information (SI Fig. 7). Eighteen B. Indica plants
were planted in one RVFCW while the other was operated
without plants (SI Fig. 7). Plants were grown for 70 days
between July and September 2010. Samples of raw and treated
WW (from both systems) were collected weekly in the evening
to ensure at least 8 h of treatment. Measurements of plant
growth were also conducted weekly for the duration of the
experiment. Daily global sun radiation was measured in the
Sde Boker Campus meteorology station, Department of Solar
Energy and Environmental Physics in collaboration with the
Israel Meteorological Service.

2.5.

Vertical flow CW (VFCW)

The vertical flow CW was located in a boutique dairy farm

producing artisanal goat cheeses in the Negev highlands,
Israel (30 580 N, 34 460 E). The VFCW treats domestic WW from
a small restaurant and from goat cheese manufacturing. A
detailed description of the system is given in Travis and Gross

Table 1 e Outline of three experimental setups for the study of salt phytoremediation by B. Indica that was conducted in the
central Negev desert around Midreshet Ben Gurion, Israel.
Facility type
Hydroponic
containers
RVFCWa
VFCWb
alternated

Water resource

Raw water
salinity (dS m1)

4 artificial solutions

1,5,8,16

Domestic wastewater
Domestic wastewater,
small restaurant and
goat cheese dairy

0.9
2.2

a RVFCW recirculating vertical flow constructed wetland.

b VFCW vertical flow constructed wetland.
c DW dry weight.

Volume of treated
water (L)
4
500
3000

Volume treated
per day L/day
0.4
300
2500

Plants
number

Final plant biomass

total DWc (g)

63

18
100

2828
20,000

3970

w a t e r r e s e a r c h 4 6 ( 2 0 1 2 ) 3 9 6 7 e3 9 7 6

(2012). Briefly, following an initial anaerobic treatment stage

WW flowed to one of two similar beds. Feed was alternated
between the two beds every seven days to allow periodic
drying to prevent clogging, control biomass growth, and
maintain aerobic conditions. Average flow to the VFCW was
2.6 m3 per day, fed in approximately 250e300 l batches
throughout the day. The size of each bed was 30 m2, and they
were constructed with locally available crushed limestone
sand and gravel with a total depth of 60 cm: an upper layer
(30 cm) of coarse sand and gravel mix (d10 0.4 mm; d60 3 mm),
underlain by two 15 cm layers of 1 and 3 cm diameter gravel,
respectively (SI Fig. 8). Both beds contained the water plants
Cana sp., Salvia Indigo Spires and Wedelia trilobata. In the first
experiment over 100 plants of B. indica were planted in March
2010 in the eastern bed and grown for 89 days until June 2010.
In the second experiment 100 seedlings of B. indica were
planted in the western bed for 92 days between July and
October 2010. Plant growth measurements and WW sampling
were carried out weekly. WW samples were taken from the
VFCW inlet and outlet (after treatment). Since only one bed
was watered every week, the comparison between the B. indica
treatment and the control alternated accordingly.

To estimate the element distribution in plant tissues, we

compared roots and shoots from hydroponic solutions. The
results were the averages of 80 measurements e 40 plants, 2
periods of w10 days of treatment (18e27 and 27e38 days). In
addition, we compared leaves and branches after 40 and 63
days of growth in the VFCW. These results represent an
average of 10 plants (5 plants from each date). Values for EC
and total dissolved solids (TDS) were converted using the
following equation (Lewis, 1980).
0
10:5
SC=
1000 C
B
S 0:012  0:2174$@
A
53:087
0
0
11
11:5
SC=
SC=
1000 C
1000 C
B
B
25:3283$@
A 13:7714$@
A
53:087
53:087
0
B
 6:4788$@

2.8.
2.6.

Data analysis

Plant growth

To estimate plant growth, we used four different measures: 1)

shoot and root dry weight (DW) which was determined after
drying at 65  C for 48 h; 2) shoot and root surface area (SA) was
measured by preparing digital images with a flat-bed scanner
(Epson Expression 10000 XL, Seiko Epson Corporation, Japan);
the images were analyzed using WinRhizo (WinRhizo Pro
v.2005b, Regent Instruments, Quebec, Canada); 3) basal stem
diameter; and 4) height. The first two measures were
destructive and, therefore, were used only in the hydroponic
experiment. Two plants were harvested from each container
periodically so that at the end of the experiment only two
plants grew in each bucket. Stem diameter and height were
measured weekly in the RVFCW and VFCW systems.

2.7.

0
12
12:5
SC=
SC=
1000 C
1000 C
B
A 2:5842$@
A :
53:087
53:087

The study was made up of three separate experiments with

different types of data sets. The data sets that fit the
requirements of statistical analysis were tested for a Gaussian
distribution with a ShapiroeWilk test. We used a parametric
Tukey procedure to test for significant differences if
a Gaussian distribution was detected. A nonparametric ManneWhitney U-test was used whenever the data set did not fit
the requirements of normal distribution. Calculations were
conducted with SAS 9.1 (SAS Institute, Cary, NC). We mention
the number of repetitions (n) and the statistical procedure that
was performed for each measurement.

3.

Results

3.1.

Plant growth

EC and elemental analysis

Water was sampled periodically before and after the treatments. Electrical conductivity (EC) was measured in the lab in
50 ml centrifuge tubes (Corning inc., USA). 10 ml of WW were
kept at 4  C for elemental analysis.
Samples were analyzed for EC using two EC meters (CON
510 conductivity/TDS bench meter, EUTECH Instruments,
Singapore, and a portable Multimeter MM 40, CRISON instruments SA, Barcelona), and the averaged results were used.
Elemental analyses for both water and plant extracts were
carried out using an inductively coupled plasma (ICP) optical
emission spectrometer (Varian ICP720-OES, (Eaton et al.,
2005)). To execute elemental analysis on B. indica, we used
dry plants (65  C for 48 h). The dried plant tissue was ground to
powder and samples (0.25 g) were digested in a 5 ml acid
mixture of HClO4 and HNO3 (15:85% v/v) in digestion glass
tubes overnight. Digestion was completed by a gradual
increase of temperature from 60  C to 195  C according to Zhao
et al. (1994). The resulting extracts were then analyzed by
an ICP.

In the hydroponic system plants developed successfully in all

measured salinities, which ranged from an EC of 1 dS m1 up
to 16 dS m1 (Fig. 1). Shoot and root biomass and surface area
were similar among all treatments. Overall, the average shoot
growth rate in the hydroponic system was 0.48 g/day with
a root: shoot ratio of 0.26  0.04.
Plants also developed successfully in the RVFCW with an
average shoot growth rate of 0.9 g/day. Average height was
150 cm, stem diameter 9.4 mm (Fig. 2), and average plant
biomass of 157 g DW. In the VFCW B. Indica plants grew
continuously, reaching an average of 226 cm height, 13.4 mm
stem diameter (Fig. 3), and average plant biomass of 244 g DW
(average shoot growth rate of 0.33 g/day). Since plant growth
was similar in both experiments in the VFCW, the results of
only the first experiment are given (Fig. 3). We measured six
developed plants in the field and found they can reach
a maximum of 9 kg DW, with an average of 4.7 kg DW per
shoot.

w a t e r r e s e a r c h 4 6 ( 2 0 1 2 ) 3 9 6 7 e3 9 7 6

Fig. 1 e Shoot growth of B. indica in a hydroponic system;

dashed lines and empty symbols represent surface area;
full symbols and solid lines stand for dry weight. Plant
growth was similar in all salinities (n [ 8, p < 0.05).

3.2.

3971

Fig. 3 e Shoot growth of B. indica in a vertical flow

constructed wetland (n [ 10). Full circles and solid lines
denote basal stem diameter; dashed lines with empty
triangles represent shoot height.

Element distribution in plant tissues

Element accumulation in shoot was measured in all systems

(hydroponic, VFCW and RVFCW) to allow mass balance
calculations. However, since it was similar (Na 30e50 mg/
g DW; K 17e30 mg/g DW; Ca 10e22 mg/g DW) in all systems we
relate here only to the hydroponic systems, where roots could
be analyzed and to VFCW where leaves were separated from
branches. Based on the results from the hydroponic system,
over 80% of the K, Ca and Na accumulated in the shoots and
less than 20% in the roots (Fig. 4A). These proportions were
similar over time from 27 to 48 days after the beginning of the
experiment (data not shown). Among shoot organs, more
accumulation was measured in the leaves as compared with
the branches (Fig. 4B). Nonetheless, these differences were
much smaller in comparison with the differences between
roots and shoots. Accumulation of Ca and Na in the shoots
branch tissues were 27 and 18%, respectively. Potassium was
distributed evenly between branches (48%) and leaves (52%).
Overall, it was estimated that 80% of the total Na

Fig. 2 e Shoot growth of B. indica grown in a recirculating

vertical flow constructed wetland (n [ 10 at a time). Full
circles and solid lines denote basal stem diameter; dashed
lines with empty triangles represent shoot height.

Fig. 4 e A) Element distribution in plant tissues in the

hydroponic system; n [ 80 for each element; B) Element
distribution in plant tissues in the VFCW; n [ 10 for each
element.

3972

w a t e r r e s e a r c h 4 6 ( 2 0 1 2 ) 3 9 6 7 e3 9 7 6

accumulation was allocated in the leaves, 13% in the woody

tissues of the canopy and only 7% in the roots. Regarding Ca,
64% was allocated in the leaves, 24% in the woody tissues and
12% in the roots. Potassium was distributed evenly in both
leaves and branches (80% accumulation) and only 17% in the
roots.

3.3.

Effect of plants on salinity of inspected solution

The EC of water treated by B. indica was significantly reduced

compared with untreated water (Fig. 5AeC). In the hydroponic
system treatment with B. indica resulted in an EC decrease of
61.8% in tap water, 22.2% in saline water of 5 dS m1 and
a decrease of 12.9% in the remaining two hyper saline solutions (Fig. 5A). The average daily water loss was 110 ml in
occupied buckets, 28% higher than empty buckets with an
average of 86 ml daily evaporation. Unexpectedly, we noticed
a reduction in the EC in the control treatment ranging on
average from 6% to 9% in the different salinities, possibly due
to precipitation of some ions. Nevertheless, this reduction was
significantly smaller than in the treated solutions.
In the RVFCW the effluent EC in the bed planted with B.
indica was lower (mean 0.84 dS m1) than the inlet EC (mean
0.9 dS m1), and usually higher in the control bed (0.95 dS m1,
Fig. 5B). The maximal difference between the EC measured in
the control bed and in the treatment bed was on September
20. We then measured an EC of 1.05 dS m1 in the control bed,
28% higher than in the raw WW (0.82 dS m1). At the same
time the EC in the B. indica treated WW was 0.75 dS m1, 9%
lower than the inflow. Similar differences between treatments
were measured between the 4th and the 8th weeks of the
experiment where the EC of the control bed exceeded the
inflow EC and the salinity of the B. indica treated WW was
lower than the inflow salinity. At this time the growth of green
tissues of B. indica was at maximum (Fig. 2) and global radiation was high (26e20 MJ per square meter).
A reduction in EC was measured in the VFCW (Fig. 5C). The
reduction in EC was higher in the bed that was enriched with
B. indica plants, in comparison with the control bed that contained only other plant species. The maximal EC reduction
(19.9%) was observed at the end of September, seven weeks
after planting. As described in the methods section, since each
week one bed was active and the other was resting, sampling
took place with a weeks difference between the control and
the B. indica planted bed.

3.4.
Accumulation of elements in plants and their effects
on water quality
The effect of B. indica plants on element concentrations in four
hydroponic solutions is presented in Table 2. To make sure

Fig. 5 e A) Average (SE) change of electrical conductivity

(EC) in four different saline growing solutions after 10 d of
treatment with B. indica plants as compared with a control
where no plants were present (n [ 16). *denotes significant
differences ( p < 0.05) between values before and after
treatment. B) The percent EC change in the recirculating

vertical flow constructed wetland (RVFCW) effluent (of the

influent) treated by B. indica over time as compared with
the EC change in unplanted RVFCW (control). Daily global
sun radiation on the sampling days is given in the upper
graph in MJ/m2. C) The percent EC change in the VFCW
effluent (of the influent) treated by B. indica over time as
compared with the EC change in VFCW without B. indica
(control).

3973

w a t e r r e s e a r c h 4 6 ( 2 0 1 2 ) 3 9 6 7 e3 9 7 6

Table 2 e Concentrations of elements in hydroponic solutions. Raw and treated represent concentration in solution before
and after treatment with B. indica (mg/l); D [ change of concentration during treatment (%) after compensating for the
background change that was measured in the control buckets. All significant changes are marked in bold.
Salinity of growing
solution EC (dS m1)
1
5
8
16

Na

Treated

Raw

Treated

Raw

Treated

Raw

Treated

51.3
661.3
1229.4
3067.4

25.4
545.5
1022.9
2409.9

L51%
L12%
L9%
L13%

31.2
50.9
72.9
138.3

0.9
13.6
19.5
65.0

L85%
L66%
L64%
L42%

67.3
177.0
328.2
737.0

27.2
180.7
255.8
570.0

L12%
24%
L2%
L8%

20.6
86.3
174.2
428.6

6.4
99.1
140.1
320.6

L57%
24%
L11%
L18%

Raw

Treated

Raw

Treated

Raw

Treated

0.3
0.3
0.5
0.8

0.1
0.2
0.4
0.6

L24%
L15%
L11%
L10%

17.0
9.2
11.0
12.8

1.5
4.4
3.1
4.5

L1%
37%
22%
30%

29.9
183.1
175.3
172.2

18.3
144.7
133.7
134.5

L21%
L10%
L8%
L6%

that EC measurements were related to TDS (as determined by

the elemental analysis), we calculated TDS from the measured
EC (Lewis, 1980) and found that it was similar. For example the
average TDS concentrations measured in the empty buckets
were 429, 2445, 4520 and 10939 mg/l compared to 442, 2581,
4378 and 9885 mg/l average calculated TDS. In the tap water
solution (EC 1 dS m1), the plants reduced concentrations of
all the measured elements by 12e85%. P was an exception e it
was reduced by 91%, but taking into account a similar reduction in the control buckets resulted in an insignificant effect of
the plants in all solutions. Concentrations of Na, Ca, Mg, Fe, S
and microelements were also reduced in the high salinities
(EC 8 and 16 dS m1), but to a smaller magnitude (only
w10%). K and P were reduced by 50e90% in all four solutions.
Table 3 presents the total accumulation of elements in B.
indica shoots at the end of the experiment. Accumulation of
Na per g DW was 3.1 higher in the most hyper saline solution
(EC 16 dS m1) in comparison with the tap water. For K and
Mg the accumulation increased by 1.7 fold. Ca, Fe, P and S
accumulation reached tissue capacity under tap water and
remained the same with higher salinities.
Table 4 presents the concentration of elements per gained
shoot biomass in comparison with the pretreated solution.
During 10 days of growth plants gained a total of 3.2 g shoot
biomass in the fresh water treatment, 3.5 g 1.7 g and 1.4 g in
the 5, 8 and 16 dS m1 solutions, respectively. This gained
biomass times the measured concentration per gram DW
shoot (Table 4) is the framework for our estimations of the

Table 3 e Element accumulation in shoots of B. indica

growing in hydroponic solutions. Values in mg per g DW
of plant shoot se (n [ 24).
Salinity of growing
solution EC (dS m1)
1
5
8
16

Mg

Raw

Fe

1
5
8
16

Ca

Na
22.2
46.6
47.2
69.2






K
0.7
2.6
1.5
1.4

21.7
31
33.6
37.5






Ca
0.8
0.7
1.1
1.3

12.9
19.4
13.2
16.9

 0.5
 0.8
 0.5
 0.5

capability of B. indica to reduce element concentration in

solutions of different salinity. The most prominent effects
include 35% reduction of Na concentration in the tap water
solution within 10 days, 56% reduction of K, 25% of Mg and
reductions of P and K in all solutions.

3.5.

Sodium mass balance

Sodium mass balance in the hydroponic solutions and RVFCW

was conducted and recoveries were acceptable, ranging from
81 to 116% (Table 5). In the hydroponic experiment, accumulation of Na in plants ranged from 2% in the highest salinity to
43% in the lowest. In the RVFCW it was estimated that 730.8 g
Na was introduced into the CW during the experiment and B.
indica plants accumulated in total 66.6 g of Na suggesting over
a 9% reduction. In the control RVFCW, Na concentration was
increased most likely because of evaporation in the summer
time (Fig. 5B). This coincide with the observations of enhanced
evapotranspiration from the hydroponic study in which the
total water loss measured in the planted containers was up to
30% greater in comparison to evaporation from the empty
containers (controls).

4.

Discussion

Seedlings of B. indica exhibited tolerance for a wide range of

mixed salt solutions, completing their life cycle in all solutions
in all three systems (Figs. 1e3). The growth of a xerophyte in
hydroponic systems and particularly in a CW is not obvious,
as this environment is extremely different from their natural
habitat. This wide range of tolerance may be attributed to the
firmness of halophytes that are especially adapted to extreme
environments (Manousaki and Kalogerakis, 2011). Our experiments showed that not only can water plants be used as
macrophytes in CWs, but also other terrestrial plants,
provided that they survive the specific conditions. This may
broaden the services that plants provide in CWs. B. indica grew
to a maximum of 244 g DW in a VFCW in 89 days. However,
potentially they can grow as much as 30 times more. This
limited growth may be explained by: 1) a relatively short

3974

w a t e r r e s e a r c h 4 6 ( 2 0 1 2 ) 3 9 6 7 e3 9 7 6

Table 4 e Element concentration in solution and accumulation in plants in hydroponic solutions. Water [ concentration of
an element in solution prior to treatment with B. indica (mg/l); plant [ accumulation of an element in B. indica shoot related
to the biomass that was gained during 10 days of growth (mg/gained gDW/l); reduction [ potential reduction of an
elements concentration during 10 days of treatment. Prominent reductions are bold marked.
Salinity

Na
1

Ca

EC (dS m )

Water

Plant

Reduction

Water

Plant

Reduction

Water

Plant

Reduction

1
5
8
16

51.3
661.3
1229.4
3067.4

17.9
40.5
19.8
23.6

35%
6%
2%
1%

31.2
50.9
72.9
138.3

17.5
26.9
14.0
12.8

56%
53%
19%
9%

67.3
177.0
328.2
737.0

10.4
16.9
5.5
5.8

15%
10%
2%
1%

Mg
Water

Fe

Plant

Reduction

Water

Plant

Reduction

Water

Plant

Reduction

Water

Plant

Reduction

5.1
9.5
3.6
3.7

25%
11%
2%
1%

0.3
0.3
0.5
0.8

0.07
0.08
0.04
0.03

26%
24%
7%
4%

17.0
9.2
11.0
12.8

3.8
7.0
2.4
2.0

22%
76%
22%
16%

29.9
183.1
175.3
172.2

3.5
3.8
1.9
1.4

12%
2%
1%
1%

20.6
86.3
174.2
428.6

growth time (only 90 days or less, compared with about 200

days in the wild); 2) disturbances such as a non-contiguous
water supply and interspecies competition (in the VFCW);
and 3) malnutrition. Whatever the cause, the phytoremediation potential of B. indica may be much higher than it
appears in our experiments.
Testing the ability of B. indica to reduce the salinity of WW
in CWs resulted in promising findings. Vymazal (2007) suggested that due to poor ventilation plant uptake is low in subsurface CWs. Our findings stand in contradiction to this
conclusion. We found a significant reduction of EC in solutions that were treated with B. indica plants (Fig. 5AeC). This
reduction was limited to mild salinities lower than 5 dS m1.
Plants did not reduce WW salinity below the agriculture
threshold for use (1.4 dS m1); meaning that salt phytoremediation as we constructed it cannot stand alone for salt
susceptible and non-tolerant crops.
In the hydroponic system we measured a small reduction
in ions in the empty containers. We explain this reduction by
the inevitable addition of diluted water to the buckets due to
evaporation and by physicoochemical processes. The reduction of EC in the treated RVFCW was highest between August

and September. One might claim this reduction is not caused

by plant salt accumulation, but merely by the shade effect that
reduces evaporation in comparison to the empty RVFCW.
However, the evapotranspiration in the treated RVFCW
exceeded the transpiration effect in the control system.
Moreover, we found a reduction of EC in the VFCW in which
the control pool was not empty, but planted with other
species. In this case both evaporation and transpiration did
not differ greatly between treatment and control, and salt
phytoremediation by B. indica plants was the direct cause of EC
reduction.
To track the allocation of salts in B. indica plants, we
measured their concentrations in different plant tissues. The
results showed that salts accumulated primarily in the upper
parts of the plants, mainly in the leaves (Fig. 4A). These results
explain the decrease in EC reduction in the RVFCW (Fig. 5B)
towards the end of the experiments, when B. indica started
blooming, the leaves shrunk and some fell, so that the accumulation potential of the plant was diminished. The practical
implication is that B. indicia plants are most effective at their
initial stages of growth, when most of the shoot biomass is
composed of green tissues. When the shoots become woodier,

Table 5 e Sodium mass balance in hydroponic setup and field scale recirculating vertical flow constructed wetland
(RVFCW).
Treatment
Hydroponic
Hydroponic
Hydroponic
Hydroponic
RVFCW treated
RVFCW control

WW EC
dS m1
1
5
8
16
0.9
0.9

Initial Na content
in solution g
0.21
2.65
4.92
12.27
730.8
730.8

Final Na content
in solution g
0.1
2.2
4.1
9.6
641
848

c
Na accumulation
by plants g (% initial)

0.09 (43)
0.18 (7)
0.16 (3)
0.28 (2)
66.6 (9)
No plants

Recovery %
85
89
86
81
97
116

a Na concentration in the initial solution.

b Na concentration in the treated solution (g/l)  the solution volume (l).
c Na accumulation in plants was calculated as Na content in plant (mg/g DW)  total plant DW. The values in parenthesis represent percent
accumulation of Na by the plants.

w a t e r r e s e a r c h 4 6 ( 2 0 1 2 ) 3 9 6 7 e3 9 7 6

they lose their main accumulative tissues, so in the blooming

period plants should be removed.
Another practical question that arises regards what
a farmer should do with the removed plants. Although beyond
the scope of this article, it would be worth considering B. indica
as an energy source as it produces a significant biomass in
a short time. Several authors showed that B. indica or its
relatives Kochia spp. are a fine food additive resource for sheep
and lambs with regard to palatability and nutrition (Kafi et al.,
2010; Kafi and Jami Al Ahmadi, 2008).
Concentrations of Na per g DW of shoot increased with the
higher salinity of the hydroponic solution (Table 3). This
increase was not high enough to create a significant accumulation effect in relation to Na reduction in the high salinities (Table 4). We conclude that the B. indica effects on Na
reduction are limited to medium and low salinities. K
concentrations in the shoots increased two fold with higher
salinities (Table 3), yet the impact of B. indica on K in hyper
salinity decreased (Table 2). It seems that the high salinities
are beyond B. indicas capacity to create a significant accumulation effect for salt phytoremediation. Yet the accumulative potential of B. indica is very high.
Summing up the accumulation of the dominant elements
(Table 3 and other elements) showed that in solutions of 1, 5, 8
and 16 dS m1, B. indica plants accumulated salts up to 7, 11, 12
and 14%, of their DW, respectively. These amounts are
expected to be even higher since our results do not include
important elements such as Cl. Given that B. indica plants can
grow to about 1 kg DW in the first stages of their growth and
potentially accumulate salts to about 10% of their DW, we
estimate that a single plant can remove during its lifetime
approximately 100 g of salts. Based on our experience with
different volumes and salinities, we estimate that accumulation of salts by B. indica can reduce salinities up to 20% of the
initial EC in low salinities (up to 2 dS m1). An individual plant
can treat approximately 500 L of WW during its growth. Our
results showed that a high leaf: woody tissue ratio is correlated to improved salt phytoremediation by B. indica. Therefore, plants can be cultivated for a high leaf index. The
preferred time for recruiting B. indica for salt phytoremediation in CWs is during the early summer (MayeJuly).
Further research is needed to improve this use by agricultural
management, including subjects such as pruning, replantation, cultivation, fertilization and synergism with
additional species.

5.

Conclusions

The current study has demonstrated a novel strategy for green

desalination through salt phytoremediation in CWs. B. Indica
plants tolerated a wide range of salinities and accumulated
salts. Accumulation occurred mainly in leaves and branches,
making B. Indica fit for the phytoextraction of Na and other
elements. Na and K were the dominant accumulated elements
driving the salinity reduction. B. indica is a good candidate for
salt phytoremediation in CWs due to its rapid and large
annual growth. Optimization of the plant performance in
terms of growth and salt accumulation is needed to further
improve its efficiency.

3975

Acknowledgments
The authors would like to thank Ms. Tanya Gendler for
assisting with the laboratory and field work, Dr. Ludmila Katz
for her part in the elemental analysis, Daniel & Anat Kornmehl for letting us work in their farm, Dr. Menahem Sklarz for
his help in the operation of the RVFCW and Dr. Micheal Travis
for the collaboration in the VFCW and manuscript editing. The
research was partly supported by the Koshland Foundation.

Appendix A. Supplementary material

Supplementary data associated with this article can be found,
in the online version, at doi:10.1016/j.watres.2012.05.020.

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