RUHUNA JOURNAL OF SCIENCE
Vol 7: 21-31, December 2016
eISSN: 2536-8400 Faculty of Science
University of Ruhuna
Faculty of Science, University of Ruhuna 21
Sri Lanka
Effect of Na2SiO3 on heavy metal uptake by field grown
Basella alba L. in Matara, Sri Lanka
Samanthika R. Hettiarachchi
1*
and Darshani Weerahewa
2
1
Department of Chemistry, The Open University of Sri Lanka, P.O. Box 21, Nawala, Nugegoda
10250 Sri Lanka.
2
Department of Botany, The Open University of Sri Lanka, P.O. Box 21, Nawala, Nugegoda
10250 Sri Lanka.
Correpondence:
1
srhet@ou.ac.lk
Received: August 05
th
2016, Revised: September 29
th
2016, Accepted: October 10
th
2016
Abstract. In this study, we investigated heavy metal uptake and the effects of
Na2SiO3 on heavy metal absorption by field grown Basella alba L (Basellaceae). The
concentrations of Fe, Cr, Pb and Cd in the field soils were 29755.30 ± 292.02, 32.99 ±
0.97, 26.01 ± 1.02, 0.13 ± 0.004 µg/g, respectively. These concentrations are
significantly below the maximum permissible limits reported by FAO/WHO.
Although Fe, Cr, Pb and Cd were present in the soil, only Fe was absorbed by B. alba;
the tissue concentrations of other heavy metals were below the detection limit. The
distribution of Fe from soil to different plant parts was investigated by calculating
transfer factors. Low transfer factors indicated low absorption and translocation of Fe
from soil to plant tissue. We also investigated the effects of Na2SiO3 on metal
absorption by applying two different concentrations of Na2SiO3 (Si-100 mg/L and Si-
50 mg/L) alongside a control. There was a significant reduction of Fe absorption in B.
alba treated with Si-100mg/L of Na2SiO3 compared to that of plants treated with Si-
50 mg/L of Na2SiO3 and the control.
Keywords. Heavy metal uptake, maximum permissible limits, silicon
1 Introduction
Farmers use synthetic and organic fertilizers as well as pesticides at several
stages during the cultivation of vegetables. These fertilizers and pesticides
enhance the growth of crops by providing essential nutrients and by
controlling pests but some of these cause soil contamination via the release of
heavy metals (McLaughlin et al. 2000). Heavy metals can be toxic even under
low concentrations and can have lasting impacts on human and ecosystem
health (Gall et al. 2015). Most farmers apply fertilizers 2-8 times in excess
than the dosage recommended by the Department of Agriculture, Sri Lanka
(Jayathilaka et al. 1989). Although several studies have been carried out on
soil contamination by heavy metals in the up country region (elevation 1000
Hettiarachchi and Weerahewa Heavy metal uptake by field grown Basella alba
Ruhuna Journal of Science 22
Vol 7: 21-31, December 2016
m above the sea level) of Sri Lanka (Jayathilaka et al. 1981, Premarathna et
al. 2005), limited research has been conducted to date on heavy metal
contamination in the low country region of Sri Lanka (Premarathne et al.
2011).
Farmers in the low country region of Sri Lanka mainly use animal
fertilizers such as cattle and poultry manure during the cultivation of green
leafy vegetables, including Basella alba L (Premarathna et al. 2011). These
natural fertilizers contain relatively high concentrations of Zn, Se, Mn, Co, As
and Fe (Bolan et al. 2010). Consumption of heavy metal contaminated
vegetables is one of the direct pathways of heavy metal entry to the food chain
(Sharma et al. 2009; Chen et al. 2014). World Health Organization (WHO)
has proposed maximum permissible limits for different heavy metals in soil
and vegetables (Chiroma et al. 2014). Leafy vegetables are known to
accumulate heavy metals (Neilson and Rajakaruna 2014); several studies have
been carried out to assess heavy metals in vegetables (Guptha et al. 2010;
Abah et al. 2014, Kananke et al. 2014; Rajapakshe et al. 2011; Premarathna et
al. 2005), including those grown in Sri Lanka. Results of studies conducted in
Sri Lanka have shown that heavy metals present in several leafy vegetables
grown in certain areas of the country are above the maximum permissible
limits set by WHO (Guptha et al. 2010; Abah et al. 2014; Kananke et al.
2014; Rajapakshe et al. 2011; Premarathna et al. 2005; Jayasinghe et al. 2005;
Rathnayake et al. 2004).
Silicon (Si) is present as silicate minerals in the Earth’s crust and these
minerals undergo chemical and physical withering, finally getting
incorporated in to the soil. In the soil solution, Si is present as uncharged
monomeric orthosilicic acid (H4SiO4) with concentration in the range of 0.1-
0.6 mM (Epstein et al. 1994; Ma et al. 2002). Although Si is the second most
abundant element on the Earth’s crust, plants can absorb Si only in the form
of orthosilicic acid which is quickly precipitated as amorphous Si after
absorption (Lux et al. 2003). Therefore, amorphous Si is the only form of Si
present in plants (Ding et al. 2008). Amorphous Si particles that are
precipitated in plant cells are called phytoliths but the locations and the
proportions can vary with the plant species as well as the age of plants (Ponzi
et al. 2003; Sangster et al. 2001). Number of studies has shown that metal
toxicity can be alleviated with the application of small quantities of Si
(Neumann et al. 2001; Ma et al. 2002; Rogalla et al. 2002; Liu et al. 2009;
Ma et al. 2008). Ma and Takahashi (2002) have showed that after the
application of Si, the oxidizing capacity of roots increases so that ferrous ions
oxidize to ferric ions, preventing the uptake of Fe. Manganese toxicity is also
reduced with the application of Si because Mn binds to the cell wall, limiting
Hettiarachchi and Weerahewa Heavy metal uptake by field grown Basella alba
Ruhuna Journal of Science 23
Vol 7: 21-31, December 2016
cytoplasmic concentrations (Rogalla et al. 2002). Neumann and zur Nieden
(2001) showed that with the application of Si, Zn can be co-precipitated with
Si in cell walls, resulting in less soluble Zn in plants. It was also shown that
silicic acid has the ability to decrease As accumulation (Ma et al. 2008).
As heavy metals have persistent and accumulative nature, they have the
ability to concentrate through the food chain and reach lethal doses to humans
(Sharma et al. 2009; Gall et al. 2005). Therefore, it is important to analyze
heavy metals present in field grown vegetables such as B. alba to determine
whether they comply with the permissible limits proposed by WHO. Basella
alba is a green leafy vegetable with important mineral nutrients; people
frequently include this leafy vegetable in their diet. We conducted the present
study to investigate heavy metal absorption by B. alba and the effect of Si on
heavy metal absorption by the plant.
2. Materials and Methods
2.1 Study site
The study was conducted at Sulthanagoda, Matara District, Southern Province
of Sri Lanka. Average annual temperature and the annual rain fall of this area
are 26.7
0
C and 2327 mm, respectively.
2.2 Experimental design
Experiment was conducted using three different concentrations of Na2SiO3
(Si- 0 mg/L-control, Si- 50 mg/L and 100 mg/L). Each treatment was
composed of three replicate beds (1m x 2m × 2m) arranged in a Randomized
Complete Block Design (RCBD). Basal fertilizer (NPK) application was done
as recommended by the Department of Agriculture, Sri Lanka (Bolan et al.
2010). Cattle and poultry manure were also applied as basal fertilizer. We
commenced this work on 15.01.2015.
2.3 Plant material
Seeds of B. alba were from one mother plant of the farmer’s field at
Sulthanagoda and they were sawn in a nursery and maintained for one month,
and then seedlings were transferred into beds.
Hettiarachchi and Weerahewa Heavy metal uptake by field grown Basella alba
Ruhuna Journal of Science 24
Vol 7: 21-31, December 2016
2.4 Preparation of plant and soil samples prior to the analysis of heavy metals
(Before the application of Na2SiO3)
After one month of planting, three plants were pulled off randomly from each
bed and washed with tap water, followed by three separate washes with
deionized water and air dried. Then, roots, stems and leaves were separated
from each plant, cut into small pieces, freeze dried for 5 days in separately
labeled zip lock bags and stored at -4
0
C until analyses were carried out.
10 g of three soil samples were taken from the middle of each bed up to 1
feet depth from the rhizosphere of the harvested plants, using a stainless steel
spatula, mixed well and air dried for two days followed by oven drying at 70
o
C for three days. Soil samples were kept in labeled zip lock bags until further
analysis.
2.5 Application of Na2SiO3 and preparation of plant and soil samples prior to the
analysis of heavy metals
Three different concentrations of liquid Na2SiO3 (Si - 100 mg/L, 50 mg/L and
0 mg/L) were added to the rooting zone of the plants in the three replicate
beds as a spray application on a weekly basis for two months. After one
month of Na2SiO3 application, three plants from each bed were pulled out and
washed with tap water followed by three washes with deionized water and air
dried. Then the roots, stems and leaves were separated and cut into small
pieces and freeze dried for five days. Labeled samples were stored at -4
o
C
until analyses were carried out.
10 g of three soil samples from each bed were collected, air dried, and then
oven dried for three days at 70
o
C. Dried soil samples were kept in labeled zip
lock bags. Same procedure was repeated for the samples collected after
second month.
2.6 Analysis for heavy metals
Soil Samples:
Soil samples were crushed, sieved (less than 2 mm pore size) and mixed to
obtain homogenized mixtures. Approximately 4 g of soil sample was ashed
using a muffle furnace for 6-8 h by controlling the temperature within the
range of 490-500
0
C. Subsequently, the sample was cooled down to room
temperature and about 10 mL of analytical grade HCl: HNO3 (1:3) mixture
was added and the resultant sample, filtered using 0.45µm filter paper,
Hettiarachchi and Weerahewa Heavy metal uptake by field grown Basella alba
Ruhuna Journal of Science 25
Vol 7: 21-31, December 2016
transferred in to a 50 mL volumetric flask and diluted up to the mark with
deionized water.
GF-AAS was calibrated by using Fischer Scientific calibration standards
and the results were obtained from Graphite Furnace Atomic Absorption
Spectrophotometer (GF-AAS) [model GBC 932+, Australia].
Plant Materials:
Plant materials were ground and mixed well to get homogenized mixtures.
The procedure used for soil samples was followed for acid digestion of plant
materials, but, only 10 mL of HNO3 was added instead of HCl:HNO3 (1:3)
mixture. Concentration of heavy metal ions were obtained from Graphite
Furnace Atomic Absorption Spectrophotometer after calibration.
2.7 Transfer factors
In order to understand the translocation of Fe into different plant parts,
transfer factors among different plant parts:soil were calculated.
Fe transfer factor of leaves:soil = Concentration of Fe in leaves
------------------------------------
Concentration of Fe in soil
3 Results and Discussion
3.1 Heavy metals present in soil
As shown in Table 1, higher concentrations of Fe, Cr and Pb were detected
compared to Cd in all the soil samples tested. Concentrations of Fe, Cr, Pb
and Cd in field soils were 29755.30 ± 292.02, 32.99 ± 0.97, 26.01 ± 1.02, 0.13
± 0.004 µg/g, respectively. All the concentrations were below the maximum
permissible limits set by WHO (Chiroma et al. 2014).
Premarathna et al. (2011) have reported heavy metal concentrations in
certain crops and soil in up-country and some parts of low-country regions of
Sri Lanka. They have observed much higher concentrations of Cd and Pb in
soil samples than those observed in the present study. According to their
results, concentration of Cd in Sedawatta in Colombo district, Sri Lanka has
been in the range of 0.61-3.28 µg/g whereas those in Kandapola in Nuwara
Eliya District, Sri Lanka has been in the range of 0.39-1.96 µg/g.
Concentrations of Pb were reported to be 39-118 and 27-97 µg/g respectively.
Some of these reported concentrations in up- and low-country soils of Sri
Hettiarachchi and Weerahewa Heavy metal uptake by field grown Basella alba
Ruhuna Journal of Science 26
Vol 7: 21-31, December 2016
Lanka are higher than the maximum permissible limits. In contrast, the soil
samples analyzed in the present study showed negligible amount of Cd and
considerably lower amount of Pb when compared to the maximum
permissible limits (Chiroma et al. 2014).
Table 1. Heavy metals present in soil after the Silicon (Si) treatments.
Metal concentration in soil (µg/g)
Before spraying
Na2SiO3
1 month after
spraying Na2SiO3
2 months after
spraying Na2SiO3
Fe
Si (100 mg/L) 28582.31 ± 290.45
a
27877.96 ± 290.45
d
27240.80 ± 296.86
g
Si (50 mg/L) 27362.71 ± 287.40
b
25188.91 ± 298.52
e
27171.35 ± 286.38
g
Si (0 mg/L) 29755.30 ± 292.02
c
29445.89 ± 294.41
f
29523.45 ± 293.61
h
Cd
Si 100 mg/L 0.13 ± 0.004
a
0.11 ± 0.004
c
0.11 ± 0.004
d
Si 50 mg/L 0.00002 ± 0.004
b
0.00012 ± 0.004
b
0.00002 ± 0.004
e
Si 0 mg/L 0.13 ± 0.004
a
0.11 ± 0.004
c
0.00002 ± 0.004
d
Cr
Si 100 mg/L 35.56 ± 1.02
a
30.89 ± 1.03
cd
34.56 ± 1.06
f
Si 50 mg/L 29.19 ± 1.00
b
29.52 ± 0.98
ce
29.54 ± 1.04
g
Si 0 mg/L 32.99 ± 0.97
a
30.91 ± 1.01
de
32.56 ± 1.06
fg
Pb
Si 100 mg/L 28.31 ± 1.11
ab
27.90 ± 1.15
d
28.10 ± 1.29
f’
Si 50 mg/L 25.50 ± 1.13
ac
21.15 ± 1.27
e
23.79 ± 1.53
g
Silicon 0 mg/L 26.01 ± 1.02
bc
24.43 ± 1.13
de
21.59 ± 1.22
g
The values which share the same letter have no significant difference. Comparisons were carried out for
each metal separately.
Based on a one-way ANOVA, a significant difference (p<0.05) was noted for
soil Fe among the treatments (100 mg/L, 50 mg/ L, and the control) during
both application stages: before spraying (28,582.31 µg/g, 27,362.71 µg/g,
29,755.30 µg/g, respectively) and one month after spraying (27,877.96 µg/g,
25,188.91 µg/g, 29,445.89 µg/g, respectively). Two months after spraying, a
significant difference was noted in both treatments, including 100 mg/L
(27,240.80 µg/g) and 50 mg/L (27,171.35 µg/g) compared to the control
(29,523.45 µg/g). Furthermore, there was no significant difference in the Fe
concentrations in soil among three application stages.
Hettiarachchi and Weerahewa Heavy metal uptake by field grown Basella alba
Ruhuna Journal of Science 27
Vol 7: 21-31, December 2016
3.2 Fe accumulation in different plant parts of Basella alba
Table 2 summarizes Fe transfer factors of different plant parts:soil. All
transfer factors are very small thus only small portion of Fe present in soil has
been translocated to plant tissue. Transfer factors decreased in the order of
root:soil > stems:soil > leaves:soil. In other words, translocation of Fe
decreased from the bottom to the top of the plant. About one thousandth of Fe
in soil was transferred to leaves of B. alba.
Table 2. Fe transfer factors of different plant parts:soil of B. alba.
Plant part: Soil Fe Transfer factors
Leaves: Soil 1.30 ×10
-3
Stems:Soil 1.90 ×10
-3
Roots:Soil 9.70 ×10
-3
Although heavy metals were present in the soil, only Fe was absorbed by B.
alba. All the other heavy metals were below the detection limit. Kananke et
al. (2014) have reported heavy metal accumulation in some leafy vegetables
including B. alba collected from open market sites in Piliyandala area in
Colombo district, Sri Lanka. According to their report, concentrations of Ni,
Cd, Cr and Pb in B. alba were above the maximum permissible limits set by
FAO/WHO (Chiroma et al. 2014).
Si-mediated heavy metal absorption has been observed in many plants
(Rogalla et al. 2002; Neumann et al. 2001; Liu et al. 2009; Ma et al.2008;
Wang et al. 2000). Wang et al. have (2000) reported a reduction of Cd uptake
in rice with the application of Si (Wang et al. 2000). Similarly, Si mediated
Cd uptake has been observed in other plants such as strawberry, cucumber,
and maize (Nwachukwu et al. 2007; Chiroma et al. 2014; Wijewardena et al.
2004).
Table 3 shows that the Fe content in different plant tissues are significantly
different among two treatments of Na2SiO3 and the control, indicating
differences in the capacity for Fe uptake. Increase in accumulation of Fe was
observed during the first month despite the Na2SiO3 treatment. It may be due
to increase in accumulation of Fe with time. However, after two months of
Na2SiO3 application, Fe accumulation was decreased. Fe concentrations of
leaves after two months of Si applications (both in Si-100mg/L and Si-50
mg/L) are less than before treatments. For example, Fe concentrations in
Hettiarachchi and Weerahewa Heavy metal uptake by field grown Basella alba
Ruhuna Journal of Science 28
Vol 7: 21-31, December 2016
leaves treated with Si-100 mg/L before and after application are 55.02 ± 2.05
μg/g and 16.27 ± 2.30
μg/g respectively. Further, Table 3 shows that the
application of higher concentration of Si lowers the capacity for Fe
absorption. For example, Fe concentrations of leaves treated with Si – 100
mg/L before and after the application and the leaves treated with Si-50 mg/L
before and after the application are 55.02 ± 2.05
μg/g, 16.27 ± 2.30
μg/g
respectively, and 24.13 ± 1.99, 13.27 ± 2.09
μg/g, respectively. There is no
significant difference in leaves treated with Si-0 mg/L (control) before and
after the application.
Table 3. Fe absorption capacities of different plant parts of B. alba after treating with
different concentrations of Na2SiO3 at different time periods.
Fe concentration in plant samples (µg/g)
Na2SiO3
(Si-100 mg/L)
Na2SiO3
(Si - 50 mg/L)
Control
(Si -0 mg/L)
Before spraying
Na2SiO3
Leaves 55.02 ± 2.05
a
24.13 ± 1.99
d
32.90 ± 2.26
g
Stem 67.96 ± 2.01
b
60.95 ± 2.15
e
69.04 ± 2.30
h
Root 394.73 ± 2.11
c
233.24 ± 2.19
f
198.53 ± 1.87
i
1 month after
spraying Na2SiO3
Leaves 114.33 ± 1.77
a
74.21 ± 2.79
d
37.62 ± 2.70
g
Stem 363.73 ± 1.77
b
133.93 ± 2.82
e
123.56 ± 3.16
h
Root 472.32 ± 1.77
c
545.04 ± 2.81
f
462.57 ± 2.75
i
2 months after
spraying Na2SiO3
Leaves 16.27 ± 2.30
a
13.27 ± 2.09
d
34.54 ± 2.33
g
Stem 84.89 ± 2.31
b
129.91 ± 2.35
e
82.46 ± 2.53
h
Root 285.22 ± 2.14
c
741.99 ± 2.16
f
341.49 ± 2.29
i
The values which share the same superscript letters have no significant (p<0.05) difference. Comparisons
were made separately for different spraying stages.
Our results show a significant difference in Fe accumulation among different
plant tissues including stem, leaves and roots collected from the plants
exposed to different treatments. Our results also show that Fe accumulation in
different plant parts is significantly different (p<0.05) within treatments.
When comparing the accumulation of Fe in a particular plant part within
Hettiarachchi and Weerahewa Heavy metal uptake by field grown Basella alba
Ruhuna Journal of Science 29
Vol 7: 21-31, December 2016
different treatments, significant differences were noted in all the plant parts.
Also, when comparing the accumulation of Fe among different treatments
under different time periods a significant difference was shown in all the plant
parts.
We document that the highest Fe concentrations are found in the roots and
the lowest concentrations are found in the leaves in all three treatments under
all three application stages.
4 Conclusion
Concentrations of Fe, Cr, Pb and Cd in the soils tested were 29755.30 ±
292.02, 32.99 ± 0.97, 26.01 ± 1.02, 0.13 ± 0.004 µg/g, respectively.
Concentration of Cd in the tested soil is much less, compared to other heavy
metals. All these concentrations are below the maximum permissible limit
reported by FAO/WHO. Therefore, the soil samples from our study site were
not heavily contaminated by the studied heavy metals. Among the metals
studied, only Fe was absorbed by Basella alba. Transfer factors calculated for
Fe among different parts of the plant:soil revealed that translocation of Fe is
different among individual parts of the plant. Our experimental results (we
had to limit up to three replicates due to high cost of analysis) also showed
that application of Na2SiO3 reduces Fe absorption capacity of B. alba. There
was a significant difference in Fe accumulation in different plant tissue treated
with different treatments of Na2SiO3. Fe accumulation in different plant parts
was significantly different within treatments and among different treatments
from three different application stages. Between the two concentrations of
Na2SiO3 used, Si-100 mg/L reduced the absorption capacity more than that of
Si-50 mg/L. Therefore, we can conclude that Fe absorption in field grown B.
alba can be decreased by treating the plants with Si-100 mg/L of Na2SiO3 than
treating with Si-50mg/L of Na2SiO3.
Acknowledgements This work was funded by the Faculty Research Grant –
2015, Faculty of Natural Sciences, The Open University of Sri Lanka.
Authors would like to acknowledge Ms. D. S. W. Wickramasinghe,
undergraduate student at the Open University of Sri Lanka for the support
during the research project and Dr. M. N Kaumal, Senior Lecturer,
Department of Chemistry, University of Colombo, Sri Lanka for the
assistance given in sample analysis.
Hettiarachchi and Weerahewa Heavy metal uptake by field grown Basella alba
Ruhuna Journal of Science 30
Vol 7: 21-31, December 2016
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