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Salinity reduction and biomass accumulation inhydroponic growth of purslane (Portulaca oleracea)Laís Pessôa de Lacerdaa, Liséte Celina Langea, Marcel Giovanni Costa Françab & EveraldoZontac
a Department of Sanitation and Environmental Engineering, Federal University of MinasGerais, Av. Antônio Carlos, 6627, Belo Horizonte, MG, Brazil.b Department of BotanyFederal University of Minas Gerais, Av. Antônio Carlos, 6627, BeloHorizonte, MG, Brazil. Tel.: + 55 31 3409-2682. E-mail:c Department of SoilsFederal Rural University of Rio de Janeiro, BR 465 km 7, Seropédica,RJ, Brazil. Tel.:+ 55 21 3787-3772. E-mail:Accepted author version posted online: 16 May 2014.
To cite this article: Laís Pessôa de Lacerda, Liséte Celina Lange, Marcel Giovanni Costa França & Everaldo Zonta (2014):Salinity reduction and biomass accumulation in hydroponic growth of purslane (Portulaca oleracea), International Journal ofPhytoremediation, DOI: 10.1080/15226514.2014.883494
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Salinity reduction and biomass accumulation in hydroponic growth of purslane
(Portulacaoleracea)
Laís Pessôa de Lacerdaa*
Liséte Celina Langea
Marcel Giovanni Costa Françab
Everaldo Zontac
a*Corresponding author: Department of Sanitation and Environmental Engineering, Federal
University of Minas Gerais, Av. Antônio Carlos, 6627 – Belo Horizonte,
MG, Brazil. E-mail: [email protected]
a Department of Sanitation and Environmental Engineering, Federal University of Minas Gerais,
Av. Antônio Carlos, 6627 – Belo Horizonte, MG, Brazil.
b Department of Botany, Federal University of Minas Gerais, Av. Antônio Carlos, 6627 – Belo
Horizonte, MG, Brazil. Tel.: + 55 31 3409-2682. E-mail: [email protected]
c Department of Soils, Federal Rural University of Rio de Janeiro, BR 465 km 7, Seropédica, RJ,
Brazil. Tel.: + 55 21 3787-3772. E-mail: [email protected]
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Abstract
In many of the world’s semi-arid and arid regions, the increase in demand for good quality water
associated with the gradual and irreversible salinisation of the soil and water have raised the
development of techniques that facilitate the safe use of brackish and saline waters for agronomic
purposes. This study aimed to evaluate the salinity reduction of experimental saline solutions
through the ions uptake capability of purslane (Portulaca oleracea), as well as its biomass
accumulation.The hydroponic system used contained three different nutrient solutions composed
of fixed concentrations of macro and micronutrients to which three different concentrations of
sodium chloride had been added. Two conditions were tested, clipped and intact plants. It was
observed that despite there being a notable removal of magnesium and elevated biomass
accumulation, especially in the intact plants, purslane did not present the expected removal
quantity of sodium and chloride. We confirmed that in the research conditions of the present
study, purslane is a saline-tolerant species but accumulation of sodium and chloride was not
shown as previously described in the literature.
Keywords: phytoremediation, saline water, salt uptake, soilless cultivation
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Introduction
Due to increased demand for good quality water for domestic and industrial use, as well
as for agriculture, this natural resource is becoming increasingly more limited and expensive.
Beyond this, in many countries there has been observed a gradual and irreversible salinisation of
soil and hydric resources. However, the safe use of brackish and saline waters for agronomic
uses is a necessity, especially in semi-arid and arid regions (Rozema and Flowers, 2008). Plant
species present different responses in relation to environmental salinity, not only dependent on
substract osmotic potential but also on the present ions (Kiliç et al., 2008; Grieve and Suarez,
1997). It is reported that only one percent of terrestrial plants are able to grow in saline zones
(coastal and non-coastal areas). These halophytic plants can tolerate saline conditions that kill the
majority of other species (Flowers and Colmer, 2008).
Nowadays, phytotecnologies include a broad set of techniques that make use of plants to
achieve several environmental goals – extract, degrade, contain or immobilize contaminants in
soil, groundwater, surface water, and other contaminated media (U. S. Environmental Protection
Agency (USEPA), 2010).
Regarding wastewater treatment, plants are usually used to remove nutrients, mainly N
and P (Sooknah and Wilkie, 2004; Klomjek and Nitisoravut, 2005; Singh et al., 2010). Water
hyacinth (Eichhornia crassipes), a species widely studied, was also tested for removal of
pollutants (suspended solids and chemical oxygen demand) in petroliferous wastewaters (De
Casabianca and Laugier, 1995).
Although phytodesalination is generally described as the use of halophytic plants to
remove salts from salt-affected soils (Manousaki and Kalogerakis (2011); Zorrig et al. (2012);
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Sakai et al. (2012); Ali et al. (2013)), a new approach proposes the use of halophytes to treat
saline wastewater, since they are able to accumulate sodium in their tissues. As described by
Shelef et al. (2012) and Shelef et al. (2013), the use of Bassia indica for water desalination was
tested in three different constructed wetlands (hydroponic aerated containers in a greenhouse,
vertical-flow and recirculated vertical-flow), reducing salinity by 20 to 60% in comparison to
systems without B. indica.
Purslane (Portulaca oleracea) is considered to be a promising crop for saline agriculture
due to its high nutritive value and antioxidant properties, and can be used for human and animal
nourishment, as well as for medicinal purposes. Furthemore, it has a short vegetable cycle and
high fresh mass production (Kiliç et al., 2008). It is an annual plant, probably originating in
Central Asia, commercially cultivated in many parts of the world, including Mediterranean
countries, Africa and Asia (Shannon and Grieve, 1999; Cros, Martínez-Sánchez and Franco,
2007a). Its cultivation has been evaluated with solutions simulating saline wastewater (15.2 and
28.5 dS m-1
) in tanks containing sand substrate, with an increase in the salt tolerance and
vigorous growth even after consecutive cuts, as long as the first node was preserved (Grieve and
Suarez, 1997). Other studies have been conducted on its cultivation in hydroponic systems
(Floating system) under non-saline (2.2 – 2.45 dS m-1
) and saline conditions (2.5, 5, 7.5, 10, 12.5
and 15 dS m-1
) with the addition of sodium chloride (NaCl) (Cros et al., 2007a, b).
In recent years, due to the quantitative and qualitative reduction of hydric resources, there
has been observed a search for techniques that permit the rational use of waters considered to be
of inferior quality which can be reconciled to economic, social and environmental factors. In this
way, the cultivation of saline-tolerant edible plants can decisively contribute to environmental
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protection and the promotion of economic activity in areas that are extremely restricted by
limited and salinised surface waters.
Considering that, according to the literature, the halophytic nature of purslane is
expressed after the first cut (Grieve and Suarez, 1997), the objective of this study was to evaluate
its ions removal capacity, as well as growth and biomass accumulation in two distinct
hydroponic saline conditions – with intact and clipped plants.
1. Methods
1.1 Plant material and growth conditions
Plants used in this experiment were grown from germination of commercially available
purslane seeds (TOPSEED TM). Seeds were placed in a gerbox with a double layer of filter
paper and incubated in a Nystatin solution (2%) at 25 ± 2 °C with a 12h photoperiod.
Germination was evaluated after three days, and germinated seedlings were then transferred to
plastic pots filled with vermiculite, and initially watered with tap water.
Later, the seedlings were watered with Hoagland standard solution (1/5 strength, without
NaCl), each four to five days. After 41 days, the plants reached 12 – 16 cm, being considered
ready for use in the experiment. All plants were then thoroughly washed to remove the substrate
(vermiculite) adhering to the roots.
Thereafter, the complete trial lasted five weeks, being conducted from 12 April to 17 May
2012, in a greenhouse located on the Campus of Federal University of Minas Gerais, in Belo
Horizonte (MG) Brazil (19° 52’ 19.85” S; 43° 57’ 43.63” W), and altitude of 812 m.The local
climate is classified as tropical at altitude, humid/warm summer and a dry/cool winter.
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The experiment was carried out simulating a floating hydroponic system (without
aeration). Each experimental unit was composed of (1) a plant (purslane), (2) a lower reservoir
(plastic container) with 1.5 L capacity, (3) a plastic support (without substrate and funnel shaped)
used to hold the plant on the lower reservoir and (4) a black plastic bag cover to protect the
nutrient solution from light exposure and avoid the proliferation of algae.
Nutrient solutions were based on the Hoagland standard solution but in low
concentrations of the analytical salts so as to allow for uptake of the ions studied (calcium,
magnesium, sodium and chloride) for more rapid observation. Macronutrient concentrations
were (mg L-1
): N (186), P (19), K (47), Mg (10), S (38) and Ca (40). Micronutrients were
supplied through a commercially available mixture of chelated salts (ConMicros Standard) in the
following concentrations (µg L-1
): Fe (363), Cu (91), Zn (37), Mn (91), B (91), Mo (18) and Ni
(17).
Three different concentrations of sodium chloride (NaCl) were added to nutrient
solutions: 0.76 (A1), 1.27 (A2) and 2.54 (A3) mg L-1
. Therefore, the theoretical concentrations of
the ions studied were: (1) calcium (40 mg L-1
Ca2+
), (2) magnesium (10 mg L-1
Mg2+
),(3) sodium
(300, 500 and 1,000 mg L-1
Na+, respectively) and (4) chloride (and 460, 770 and 1,540 mg L
-1
Cl-, respectively). On average, the nutrient solutions showed initial electrical conductivity (CE)
of 1.9, 2.9 and 5.1 dS m-1
, respectively.
1.2 Plant growth experiment in saline conditions
The growth experiment (five weeks) was divided into: (1) Acclimatization period (first
two weeks): used to acclimatize the plants to the saline conditions and (2) Extraction period
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(three remaining weeks): at the beginning of the third week, half of the purslane plants were cut
above the third node. Simultaneously, a control treatment (without plants) was assessed for
comparison, since differences between them would indicate direct plant actions. Therefore, three
different treatments were monitored: (1) Purslane intact (IN), (2) Purslane clipped (CL), (3)
Control (CO). Each treatment had 5 replicates, totaling 15 experimental units for each applied
nutrient solution.
All experimental units received 0.5 L of nutrient solution, which were changed weekly.
Therefore, at the beginning of the first three weeks, they had the same physicochemical
conditions. From weeks three to five (after clipping), nutrient solutions were no longer changed
but volume losses were replaced with deionized water.
1.3 Biomass accumulation and water consumption parameters
Five single plants were collected at the beginning of the experiment. The material was
separated into shoots and roots, dried in a forced circulation oven at 70 °C and weighed to
determine the initial dry biomass. After the end of the experimental period, all plant samples
were cut (shoots and roots), dried and weighed to determine the dry biomass of shoots and roots
accumulated during 35 days. The relative growth rate (RGR) was then calculated using Equation
(1) (Fisher, 1921).
12
12 lnln
tt
WWRGR
Equation (1)
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Where W1 and W2 are the dry biomass at the beginning (t1) and at the end of the
experimental period (t2), respectively. The RGR facilitated the assessment of changes in biomass
accumulation.
The clipped material (week three) was also dried and weighed to assess the final dry
biomass of the clipped condition.
The biomass accumulation and its associated ions uptake in saline nutrient solution were
analyzed during this experimental period. The uptake of nutrient solutions was recorded weekly
and totaled at the end of the experiment, providing the TUV (total uptake volume). The TUV of
nutrient solutions A1, A2 and A3 were measured to identify differences regarding water-use
efficiency in the biomass accumulation due to clipping.
1.4 Solution salinity reduction from ion uptake promoted by plants’ growth
Ion uptake assessment was conducted during the last three weeks of the experimental
period. At the end of week five, the final volume of the residual solutions produced by the three
conditions (intact, clipped and control) was measured. Samples were then collected and used to
determine the final concentrations of calcium, magnesium, sodium and chloride ions. The ion
extraction promoted during this period was initially estimated based on the final concentration
presented in the control treatment. For complementary information, pH and electrical
conductivity (EC) were also measured.
Due to different volume loss, an analysis based on the final concentration of the ions
studied (expressed in mg L-1
) would be inappropriate to evaluate the possible ion extraction
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promoted by the treatments tested. Thus, a mass balance (mg) was carried out to determine the
mass of each ion in the final volume of the nutrient solutions of the intact, clipped and control
plants.
The final concentration of cations (sodium, calcium and magnesium) was determined by
Atomic Absorption Spectrophotometry (AAS), while the final concentration of chloride was
found by titration (Mercuric Nitrate Method) (American Public Health Association (APHA),
2005). All samples analyzed by AAS were previously filtered to remove any suspended solids;
specifically for determination of sodium concentration, it was necessary to dilute them to meet
the detection thresholds of the equipment used.
During the experimental period, the environmental conditions (ambient air temperature
(°C) and relative humidity (RH) (%)), as well as the appearance of the plants to detect any
symptom of saline stress in the shoots and root systems were also monitored.
1.5 Statistical analyses
All data were statistically analyzed through the STATISTICA software (version 6). Due
to asymmetry noticed in the data sets, a nonparametric test (Kruskal-Wallis) was employed to
determine significant differences between medians (at 95% of confidence).
2. Results and discussion
2.1 Environmental conditions
Mean weekly maximum and minimum ambient air temperatures and RH at the study site
over the course of the experiment are shown in Table 1.
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2.2 Biomass accumulation associated with the consumption of nutrient solutions
Assessing the consumption of nutrient solutions during the complete experimental period,
it was noticed that the intact treatment differed significantly, presenting higher uptake of the
three different concentrations of sodium solutions used. Alternatively, clipped plants showed
intermediate performance. Results observed of TUV using solutions A1, A2 and A3 are shown in
Figures 1(A), 1(B) and 1(C), respectively.
Regarding dry biomass accumulation, intact plants had distinct responses, especially in
shoot growth. Furthermore, no significant difference was verified in biomass accumulation.
Thus, intact and clipped plants between them presented similar performance (shoot and root)
when grown in the three sodium concentrations (300, 500 e 1,000 mg L-1
), as shown in Figures
2(A) and 2(B).
Previous findings regarding biomass accumulation were confirmed through RGR
assessment since intact plants presented significant differences and intact or clipped plants,
independent of nutrient solution used, showed similar growth performance between them (Figure
3).
In this case, observations by Kiliç et al. (2008) were confirmed in that, when grown in
different salinities (0.65 (control), 3.5, 5.0 and 6.4 dS m-1
) for 38 days, this species presented
significant growth in respect to increased dry biomass accumulation. Another important finding
refers to nutrient solutions uptake efficiency since, despite presenting greater removal of saline
nutrient solutions during the experimental period (35 days), the intact plants showed greater
relative growth than clipped plants.
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3.3. Salinity reduction
Salinity reduction promoted by the uptake capacity of plants studied was determined by
residual solution evaluation obtained at the end of the ions removal period (3 weeks) in
qualitative (final ions concentration) and quantitative form (final volume). Physical-chemical
results (EC, pH and final volume) of residual solutions served as a preliminary indication of
plants’ capability differences (Table 2).
In general, it was observed that intact plants presented significant differences in solution
electrical conductivity, pH and final volume in relation to the control, suggesting significant ions
removal from saline nutrient solutions used. Clipped plants, except for final volume, did not have
distinct differences in EC and pH, indicating different capability. Mass balance was used to
determine final calcium, magnesium, sodium and chloride mass present in residual saline
solutions at the end of control, intact and clipped plant evaluations (Figures 4(A), 4(B) and 4(C),
respectively). Final ions mass results were calculated using treatment volume (0.5 L). It was
verified that, with saline solution A1, intact plants presented significant differences in calcium
removal; whereas, in the same conditions, clipped plants did not. With solutions A2 and A3,
treatments did not present significant removal capability compared with the control plants. In all
saline solutions, intact plants were significantly different in magnesium removal, almost
completely exhausting their availability. Despite there being no significant differences between
saline solutions for clipped plants, intermediate results were observed in relation to the control
plants. Results obtained from solutions A1 and A2 indicated significant differences for both
intact and clipped plants in sodium removal. However, distinct capacity was only observed in
solution A3 with clipped plants. It was verified in solutions A1 and A2 in relation to chloride
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removal that intact plants had distinct capacity in comparison to the control plants; however,
clipped plants showed no differences. Intact and clipped plants did not significantly remove
chloride in solution A3.
Results presented by Grieve and Suarez (1997) for this species grown in saline conditions
(2.1 (control); 15.2 and 28.5 dS m-1
)) showed that the whole plant had progressive sodium
concentrations in its tissues (15.3, 45.3 and 72.1 g kg-1
dry mass, respectively) and chloride
(10.2, 12.1 and 20.4 g kg-1
dry mass, respectively). In another study, purslane also accumulated
increased sodium concentrations (1.20, 1.72, 1.85 and 2.06 %, respectively) and chloride (4.35,
5.81, 6.32 and 6.61 %, respectively) in its shoot tissues (Kiliç et al., 2008). Thus, despite this
species being indicated as a sodium and chloride accumulating plant, in this present study the
residual solution analysis after the experimental period did not present significant removal of
these ions by hydroponic growth, ruling out the possibility that this had occurred due to a lack of
aeration of nutritive solutions (Lara et al., 2011).
2.3 Visual symptoms
Clipped and intact purslane plants did not present distinct visual symptoms in solutions
A1, A2 and A3. Throughout the five week period, plants presented vigorous shoot development
without leaf and root colour alterations or necrosis in the three saline solutions.
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3. Conclusions
The results indicated that, despite there being notable magnesium removal and elevated
biomass accumulation, especially in intact plants, purslane did not present the expected capacity
for sodium and chloride removal. The salinity tolerance of this species was thus confirmed,
although accumulation of these ions as described in the literature was not demonstrated in the
hydroponic conditions of this study.
Acknowledgements
The authors are grateful to Technical School of the Federal University of Minas Gerais –
UFMG (MSc. Lúcia Maria Porto de Paula), Agricultural Research Agency of Minas Gerais –
EPAMIG (Dr. Marinalva Woods Pedrosa), Research Support Agency of the State of Minas
Gerais (FAPEMIG) and Coordination of Higher Education Development (CAPES) for support
this study. Thanks also to Alistair Hayward for critical review of the English text.
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TABLE 1– Ambient air temperature and relative humidity (RH) during the experimental period
Variable
Minimum values (n=5) Maximum values (n=5)
Min Max Mean
Standard
deviation
Min Max Mean
Standard
deviation
Air temperature °C 13.1 17.2 15.6 1.5 30.7 35.6 33.5 2.4
RH % 40.0 61.0 48.8 8.2 87.0 92.0 91.0 2.2
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TABLE 2– Final volume, electrical conductivity and pH at the end of ions removal period (3
weeks)
Variable Treatment
Solution
A1 A2 A3
Mean Min Max Mean Min Max Mean Min Max
EC
(dS m-1
)
Control 1,92 a 1,90 1,95 2,83 a 2,80 2,88 5,13 a 5,09 5,17
Intact 1,52 b 1,50 1,54 2,55 b 2,50 2,58 4,88 b 4,85 4,91
Clipped 1,60 a,b 1,56 1,62 2,57 a,b 2,52 2,64 4,95 a,b 4,92 5,03
pH
Control 7,45 a 7,17 7,73 7,55 a 6,76 7,97 6,56 a 6,39 6,84
Intact 4,46 b 4,13 6,37 3,71 b 3,63 3,88 3,33 b 3,25 3,56
Clipped 6,60 a,b 5,65 6,76 6,51 a,b 3,85 7,05 6,58 a,b 3,33 7,08
Final
volume
(mL)
Control 495 a 490 495 495 a 490 495 495 a 490 495
Intact 460 b 450 470 460 b 455 465 465 b 460 470
Clipped 460 b 455 475 470 a,b 460 470 465 b 465 470
Different letters are significantly different at P< 0.05 (Kruskal-Wallis test)
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Solution A1
Median 25%-75% Min-Max
Tota
l upta
ke
volu
me
(mL
)
ControlIntact
Clipped40
80
120
160
200
240
a
b
a,b
(A)
Solution A2
Median 25%-75% Min-Max
Tota
l upta
ke
volu
me
(mL
)
ControlIntact
Clipped40
80
120
160
200
240
a
b
a,b
(B)
Solution A3
Median 25%-75% Min-Max
Tota
l upta
ke
volu
me
(mL
)
ControlIntact
Clipped40
80
120
160
200
240
a
b
a,b
(C)
FIGURE 1 – Total uptake volume (mL): (A) Solution A1 (300 mg L-1
Na+); (B) Solution A2
(500 mg L-1
Na+); (C) Solution A3 (1,000 mg L
-1 Na
+)
Box and whisker plots with different letters are significantly different at P< 0.05 (Kruskal-Wallis
test)
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Shoot
Median 25%-75% Min-Max
Acc
um
ula
ted d
ry m
ass
(mg)
Init
ial
IN A
1 (
Fin
al)
IN A
2 (
Fin
al)
IN A
3 (
Fin
al)
CL
A1
(F
inal
)
CL
A2
(F
inal
)
CL
A3
(F
inal
)0
300
600
900
1200a
aa
A AA
(A)
Root
Median 25%-75% Min-Max
Acc
um
ula
ted d
ry m
ass
(mg)
Init
ial
IN A
1 (
Fin
al)
IN A
2 (
Fin
al)
IN A
3 (
Fin
al)
CL
A1
(F
inal
)
CL
A2
(F
inal
)
CL
A3
(F
inal
)0
40
80
120
160
a
aa A
A A
(B)
FIGURE 2 – Dry biomass accumulation (mg): (A) Shoot – initial and final dry biomass
(Solution A1 (300 mg L-1
Na+); Solution A2 (500 mg L
-1 Na
+); Solution A3 (1,000
mg L-1
Na+)); (B) Root – initial and final dry biomass (Solutions A1, A2 and A3
with the same concentrations)
Box and whisker plots with different letters are significantly different at P< 0.05 (Kruskal-Wallis
test)
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Median 25%-75% Min-Max
Rel
ativ
e gro
wth
rat
e (g
d-1
)
IN (
A1
)
IN (
A2
)
IN (
A3
)
CL
(A
1)
CL
(A
2)
CL
(A
3)0,07
0,08
0,09
0,10
0,11
a aa
A
AA
FIGURE 3 – Relative growth rate (g d-1
): intact and clipped plants (Solution A1 (300 mg L-1
Na+); Solution A2 (500 mg L
-1 Na
+); Solution A3 (1,000 mg L
-1 Na
+))
Box and whisker plots with different letters are significantly different at P< 0.05 (Kruskal-Wallis
test)
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Solution A1
Ca
2+
(mg)
ControlNot clipped
Clipped10
12
14
16
18
20
22
a
b
a,b
Solution A2
Ca2
+ (m
g)
ControlNot clipped
Clipped10
12
14
16
18
20
22
aa
a
Solution A3
Ca2
+ (m
g)
ControlNot clipped
Clipped10
12
14
16
18
20
22 aa
a
Solution A1
Mg
2+
(mg)
ControlNot clipped
Clipped
0
4
8
12
a
ba,b
Solution A2
Mg
2+
(mg)
ControlNot clipped
Clipped
0
4
8
12
a
b
a,b
Solution A3
Mg
2+
(mg)
ControlNot clipped
Clipped
0
4
8
12
a
b
a,b
Solution A1
Na
+ (
mg)
ControlNot clipped
Clipped120
130
140
150
160 a
b
b
Solution A2
Na
+ (
mg)
ControlNot clipped
Clipped
195
210
225
240
a
b
b
Solution A3
Na
+ (
mg)
ControlNot clipped
Clipped360
400
440
480
520a
a,b
b
Solution A1
Median 25%-75% Min-Max
Cl- (
mg)
Control Intact Clipped
220
240
260
280
300a
b
a,b
(A)
Solution A2
Median 25%-75% Min-Max
Cl- (
mg)
Control Intact Clipped
390
420
450
480
a
b
a,b
(B)
Solution A3
Median 25%-75% Min-Max
Cl- (
mg)
Control Intact Clipped
810
840
870
900
930
960
aa
a
(C)
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FIGURE 4 – Final mass of calcium, magnesium, sodium and chloride ions (mg): (A) Solution
A1 (300 mg L-1
Na+); (B) Solution A2 (500 mg L
-1 Na
+); (C) Solution A3 (1,000
mg L-1
Na+)
Box and whisker plots with different letters are significantly different at P< 0.05 (Kruskal-Wallis
test)
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