Introduction
Currently, one of the
serious ecological problems, the world facing is heavy metal pollution in
agricultural soils. This problem is a consequence of industrialization,
urbanization (Tan et al. 2016; Qian et al.
2017; Xu et al. 2020), mineral mining (Xiao et al.
2017), industrial wasting (Qing et al. 2015; Golui et al. 2019; Yang et al.
2019; Alam et al. 2020), abuse
pesticides (Peña et al. 2020) and chemical fertilizers in agricultural
cultivation (Ning et al. 2017; Edogbo et al.
2020; Wang et al. 2020). The
farming on heavy metal contaminated soil will lead to the absorption and
accumulation of these metals on agricultural products (Xu et al. 2006; Bi et al. 2010; Malandrino et al. 2011; Naz et al. 2013; Rodriguez et
al. 2014; Edogbo et al. 2020). Therefore, the accumulation of
heavy metals in agricultural products is becoming serious
concern for many countries, including Vietnam, because of their
toxicity, sustainability and bioaccumulating potential. Heavy metals can be
accumulated in vital organs such as kidney, bone, and liver where it can pose
threats to the health of human beings (Bosch et al. 2016; Lamas et al. 2016; Ma et al.
2016). Moreover, long-term exposure to these can cause physical,
muscular and neurological degenerative processes, and even cancer (Álvarez-Mateos et
al. 2019).
There have
been many studies focused on the methods to decrease amount of heavy metals in
soil to limit their accumulation in agricultural products. Several techniques,
included physical separation, chemical washing, electro-remediation have been
suggested to solve soil contamination by heavy metals (Akcil et al. 2015).
However, these methods require high costs and disrupt the soil structure. Use
of natural materials such as goethite, magnetite, and hematite reduce the activity
of heavy metals in contaminated soil as iron oxides in these materials can bind
strongly with heavy metal (Hartley et al. 2004; Liu et al. 2014; Suda and Makino 2016). As chemical properties
of soil changes, heavy metals immobilized by iron oxides may be released back
into the soil. Moreover, the presence of iron ion in soil also affects the
growth of plants. Although applying some natural materials (e.g., red-mud and
biochar) to the soil remediation work has certain environmental benefits (Lu et al.
2018; Xu et al. 2018), this
practice takes much time and expenses to absolutely solve the problem of heavy
metals in soil. Some studies have focused on identifying plants with
a high potential for heavy metal accumulation to be used as phytoremediation (Álvarez-Mateos et al. 2019). Nevertheless,
several factors such as growth rate of plants, phytotoxicity of metals,
geochemistry of the contaminated soil and uptake ability of metals prevent the
efficiency of such methods (Jin et al. 2019; Al-Thani and Yasseen 2020). These
evidences show that the treatment of heavy metals in agricultural soils is not
simple, and requires a lot of time as well as cost. Therefore, in many
countries, especcially in poor and underdeveloped countries, farmers are still
cultivating in polluted areas (Rodriguez et al. 2014; Ávila et al. 2017; Alam et al.
2020). This situation is extremely worrying because the absorption of
heavy metals from soil to plants is one of the main ways for heavy metals to
infiltrate through the food chain, and to a certain level, these metals will
cause risks to human health (Akinyele and
Shokunbi 2015; Ávila et al. 2017;
Qian et al. 2017). It
seems that, so far, there not have been many reports related to the
identification of the kinds of vegetables which have the ability to grow in
metal polluted soil with limitative accumulation. There have been also no studies
monitoring changes in morphology as well as productivity of vegetables grown in
lead-contaminated soil. Moreover, as far as we know, there are very few studies
which evaluated the effect of farming mode on the ability to absorb and
accumulate of heavy metals from soil to plants (Zhu et al. 2010; Liu et al. 2016). These works only surveyed effect of
each factor of cultivation process, such as the amount of nitrogen fertilizer
and on the accumulation of heavy metals in plants. Zouheir Elouear et al (Elouear et al.
2016) evaluated the effects for the use of KCl on the growth and heavy
metal accumulation of alfalfa (Medicago sativa L.) in a Cd, Pb and Zn
mine soil but this kind of plants was used as a phytoextraction in contaminated
soil.
Among
heavy metals, lead is a highly toxic one which, plays no role in metabolic
processes in the organism and can be toxic even in tiny amounts (Pourrut et al.
2011). Lead is a contaminant that can easily accumulate in soil and
sediments. Lead accumulates in the surface soil layer, and its concentration
decreases with the depth of the soil. Therefore, lead can easily be absorbed
and accumulated by plants in different parts when cultivated on contaminated
soil. When exposed to a certain extent, lead is toxic to animals, including
humans, damaging the nervous system and causing brain disorders. High exposure
to lead will result in blood disorders in animals. Like mercury, lead is a
neurotoxin, accumulating in soft tissue and in bones, which is difficult to
eliminate (Tan et al. 2016).
In an
attempt to make good use of lead-polluted soil, present study paid attention to
the growth responses of potatoes (Solanum tuberosum L.), carrots (Daucus
carota L.). - representing for tuber vegetables - spinach (Spinacia
oleracea L.), and lettuce (Lactuca sativa L.) - representing for
leafy vegetables. These vegetables are planted widely in Vietnam and other
areas in the world. Besides, the accumulation of lead from contaminated soil on
the biomass of these vegetables were determined. Amounts of lead in different
parts of examined plants were also investigated. On the other hand, the effect
of lime and N-, P-, K-fertilizer on lead accumulation from soil to these
vegetables were also investigated. The result of present work will help in
choosing kinds of vegetables which can adapt to lead contaminated soil with
limitative accumulation. Besides, the result obtained of this study provides
the basic to identify the effects of some factors in cultivation mode to limit
the accumulation of lead from soil to vegetables. The result of this
investigation also suggests kind of vegetables and suitable cultivation mode to
limit the content of lead in the edible parts of vegetables grown in lead
contaminated soil.
Materials and Methods
Experimental treatments and designs
Experimental was conducted in Ward 8, Dalat city,
Lam Dong Province (11°57’39.7’’N –108°26’28.3’’E, 103°36’ E–109°35’ E) in
Vietnam. Lam Dong Province presents area with suitable climatic and soil
conditions for the cultivation of carrots, potatoes, lettuce, and spinach. The present
study was conducted from March to September, during 2019 vegetation season. The soil was collected from uncontaminated paddy fields (0‒20 cm of topsoil) of areas
specializing in vegetable cultivation. After
air-dried and passed through a mesh sieve (2 mm
mesh size), fifteen kilograms of soil was placed in each pot
(40 cm in diameter and 35 cm in height). The
properties of soil sample used in this study were analysed (Table 1).
Empirical model included two areas
Area 1: Study on accumulate levels of
lead from soil to plants. In this area, vegetables were grown under cultivation
mode currently used by farmers, except for the soil which was contaminated by lead at different levels of
content, including: 100, 200, 400, 600, 800, 1000, 1200 and 1500 mg/kg. The soil was spiked with different lead doses
by spraying of Pb(NO3)2 solution and then stabilized for
three weeks before use. Total concentration of lead in the soils of all
treatments after lead additions were determined, ensuring sting that the doses
of lead added to the soils of all treatments were accurate. For comparison,
experimental field had a controlled area where studied vegetables were grown under the same conditions as
models for uncontaminated soil mentioned above.
Area 2: Investigation the effect of cultivation mode to lead accumulation from soil to plants. The soil was contaminated by lead at 100 mg/kg and the added amounts of agricultural
lime (CaCO3) as well as N-, P-, K- fertilizers were changed. The
amounts of lime added to the soil and commensurate soil pH are presented in
Table 2. Other soils were fertilized with phosphorus (P) as calcium phosphate
[Ca(H2PO4)2] or potassium (K) as potassium
chloride (KCl), or nitrogen (N) as ammonium nitrate (NH4NO3).
The amounts of each fertilizer added for each kind of vegetables were Table 1: Properties of soil
sample
|
|
Unit |
Content |
|
pH |
|
5.97 ± 0.01 |
|
Total organic matter |
(g/kg) |
8.62 ± 0.7 |
|
Total of nitrogen |
(g/kg) |
0.28 ± 0.04 |
|
Total of phosphorus |
(g/kg) |
0.62 ± 0.01 |
|
Total of potassium |
(g/kg) |
16.22 ± 0.12 |
|
Lead |
|
not detected |
Values are means
of three replicates followed by ±standard error of means (n = 3)
Table 2: The amount of lime added in
the soils and corresponding pH
|
Treatment |
Amount
of lead (mg/kg soil) |
Amount
of lime (g/15kg soil) |
pH |
|
Control |
100 |
0 |
5.97 |
|
T1 |
100 |
7.5 |
6.42 |
|
T2 |
100 |
13.8 |
7.05 |
|
T3 |
100 |
19.2 |
7.52 |
Table 3: The
amount of N, P, K fertilizer added to the soil
|
Samples |
Spinach |
Lettuce |
Carrots |
Potatoes |
||||||||
|
N* |
P* |
K* |
N* |
P* |
K* |
N* |
P* |
K* |
N* |
P* |
K* |
|
|
Control |
2.30 |
10.30 |
2.5 |
3.00 |
4.50 |
0.90 |
4.90 |
14.10 |
6.00 |
4.10 |
5.60 |
1.40 |
|
T4 |
1.15 |
10.30 |
2.5 |
1.50 |
4.50 |
0.90 |
2.45 |
14.10 |
6.00 |
2.05 |
5.60 |
1.40 |
|
T5 |
3.45 |
10.30 |
2.5 |
4.50 |
4.50 |
0.90 |
7.35 |
14.10 |
6.00 |
6.15 |
5.60 |
1.40 |
|
T6 |
4.60 |
10.30 |
2.5 |
6.00 |
4.50 |
0.90 |
9.80 |
14.10 |
6.00 |
8.20 |
5.60 |
1.40 |
|
T7 |
2.30 |
5.15 |
2.5 |
3.00 |
2.25 |
0.90 |
4.90 |
7.05 |
6.00 |
4.10 |
2.80 |
1.40 |
|
T8 |
2.30 |
15.45 |
2.5 |
3.00 |
6.75 |
0.90 |
4.90 |
21.15 |
6.00 |
4.10 |
8.40 |
1.40 |
|
T9 |
2.30 |
20.60 |
2.5 |
3.00 |
9.00 |
0.90 |
4.90 |
28.20 |
6.00 |
4.10 |
11.2 |
1.40 |
|
T10 |
2.30 |
10.30 |
1.25 |
3.00 |
4.50 |
0.45 |
4.90 |
14.10 |
3.00 |
4.10 |
5.60 |
0.70 |
|
T11 |
2.30 |
10.30 |
3.75 |
3.00 |
4.50 |
1.35 |
4.90 |
14.10 |
9.00 |
4.10 |
5.60 |
2.10 |
|
T12 |
2.30 |
10.30 |
5.00 |
3.00 |
4.50 |
1.80 |
4.90 |
14.10 |
12.00 |
4.10 |
5.60 |
2.80 |
(* : mg/kg soil)
stated in Table 3. The amounts of each fertilizer for every studied vegetable were changed depending on the Technical process of each kind the planted vegetable (Department of Agriculture and Rural
Development of Lam Dong Province 2013). Specifically, the amount of each
kind of N-, P- and K-fertilizer applied for each type of the vegetables was
decreased a half, increased a half, and increased double as much as those
suggested by Technical process of this vegetable planting. The control
experiments were carried out by adding the amount of N-, P-, K-fertilizers the
same as those suggested by above technical processes.
Planting vegetables
Lettuce and spinach seeds were submerged in water for about 48 h at room
temperature (20–25oC), prior to germinating
under moist condition at 32oC for 30 h. These germinated seeds were
then grown in uncontaminated soil within 15 days before being transplanting
into the pots (five plants per pot).
Carrot seeds were soaked in warm water at 40°C for 8 h
before being kept for six days until the seeds germinated. These germinated
seeds were then shown with a density of 10 seeds per pot.
Potatoes seedlings were collected at nursery, then
planted in each treatment with a density of 2 plants per pot.
These vegetables were grown under cultivation mode as
defined by Department of Agriculture and Rural Development, Lam Dong Province,
Vietnam. Plants were watered every two days or as needed to maintain
field capacity. Each pot was given a plastic tray below to collect
leachate returned to the pots. Mature plants (after 45 days for lettuce and
spinach, 100 days for carrots and potatoes) were harvested at the same time.
Soil and plants analysis
After
preparing soil samples, the soil pH was measured with a glass electrode by
distilling water slurry (1:2.5, w/v) (Margesin and Schinner, 2005). For determining the content of
elements in soil, soil sample was dissolved by a mixture of HNO3,
HCl and HF in a microwave digester (iLINK MARS 6 CEM). The total and
bio-available contents of nitrogen (N), phosphorus (P) and potassium (K) were
determined by the AOAC Official Method 955.04, 958.01 %2049-58_files/image002.jpg)
Fig. 1: Effects of lead on the morphology of studied vegetables
and 965.09. The content of lead in soil was performed using an Atomic
Absorption Spectrophotometer (AAS, SHIMADZU AA-7000).
At the
end of the growth period, the plants were carefully removed from the soil. The
stems, leaves, and roots were separated, cleaned, and washed adequately, then
they were dried at 60oC in the drying oven (MEMMERT UF55) to their
constant weight. These dried samples were homogenized separately in a porcelain
mortar.
Acid
digestion with vegetable parts (500 mg each) was performed in a microwave
digester using 10 mL of 65% HNO3, cooled,
filtered and made up to 25 mL using deionized water. Lead determined in the
respective samples was done by Atomic Absorption Spectrophotometer. Blank tests indicated
that the level of contamination induced by the acid digestion procedure was
negligible.
Statistical analyses
All experiments were triplicated (n = 3) and the experimental
data were presented in average ± standard deviation (SD). The analytical procedure
was validated based on the internationally certified plant standard
reference material (Citrus Leaves 1572). The Relative Standard Deviation (RSD)
of each analysis was found within ± 2.4% of the certified values. The one-way
analysis of variance (ANOVA) was utilized to evaluate the significant
differences between the lead content in particular vegetables and contaminated
soil. Statistical significance was evaluated via the student’s t-test
with the P-value < 0.005.
Results
Effect of lead on the morphology
and growth rate of some vegetables
The changes in the morphologies of four kinds of vegetables (spinach,
lettuce, carrots, and potatoes) planted in soil with different concentrations
of Pb showed no toxicity symptoms in the spinach and the lettuce at the concentration of lead less than %2049-58_files/image004.png)
Fig. 2: Changes in the morphological
form of spinach, carrots, lettuce, and potatoes roots when grew on
lead-contaminated soils
%2049-58_files/image006.png)
Fig. 3: Effect of lead on the growth characteristics of inspected vegetables (a)
height of plants, (b) fresh weight of edible parts per plant (error bar = SD, n
= 3)
800 mg/kg. The growth parameters including height of plants, number and dimension of
leaves, average yield showed a negligible change. However, there is a stunted
growth in soil contaminated by lead higher than 1200 mg/kg for the spinach and 800 mg/kg for the lettuce. Carrots
can normally grow in soil contaminated by the excess of lead from 100 to 400
mg/kg. Meanwhile, the growth inhibition together with a progressive decrease in
the number and dimension of leaves, the low weight of tubers is observed at
above 600 mg/kg of the Pb(II) concentration. In particular, the dead plants
were recorded at the lead doses of 1200 mg/kg or above. In potatoes, the rate
of growth reduced significantly when the Pb(II) concentrations of 600 and 800
mg/kg and plants could not grow in soil with the Pb(II) content of 1000 mg/kg
and above (Fig. 1).
The results
showed that Pb was highly toxic to the growth of the carrot roots. The
diameter, length, weight, and yields of carrot roots decrease dramatically with
the increase in the Pb level in the soil. Indeed, the change in carrot root in
shape is recorded at the Pb(II) concentration of 200 mg/kg and above. When the
Pb concentrations of 200‒400 mg/kg, although the carrot
growth is not significantly influenced, the root shape is altered and the roots
yield is decreased by 20% or more. The root shape and weight are significantly
affected under the Pb levels of 600–1000 mg/kg. In potatoes, a decrease in the
number and dimension of roots was observed in all the Pb(II) concentration from
400 to 800 mg/kg (Fig. 2).
There was a considerable
decrease in the height of plants and the weight of edible parts when the concentrations
of Pb (II) increased from 100 mg/kg to 1500 mg/kg. For instance, carrots and potatoes
will be dead if the Pb (II) levels in soil is higher than 800 mg/kg and 1000
mg/kg, respectively. The height and the edible parts’ weight of the spinach
decrease by 69.4 and 64.6% from 26.5 cm and 100.5 g, respectively, while a
decline by about 70% occurs on the lettuce when the Pb(II) concentrations are
changed from 100 mg/kg to 1500 mg/kg (Fig. 3).
The accumulation of lead in the
biomass of studied vegetables
When lead content in soil ranged from 100 to
1500 mg/kg, the amount of this metal in the biomass of four studied vegetables
ranged between 0.05 and 6.79 mg/kg. Lead accumulation in these vegetables were
as the following the order: carrots > potatoes > spinach > lettuce.
For example, the lead amount was 0.85 and 6.79 mg/kg in
the roots of carrots, 0.20 and 1.79 mg/kg in edible parts of lettuce when the
amount of lead in the polluted soil was 100 mg/kg and 1000 mg/kg, respectively.
Besides, lead tended to be accumulated in the roots of all studied vegetables.
Generally reporting, the amount of lead decreased in the order of roots of
carrots > potatoes > spinach > lettuce > stems and leaves of
spinach > carrots > potatoes > lettuce (Table 4).
For leafy vegetables, the
average lead content in spinach roots was 2.53 times higher than in stems and leaves.
Meanwhile, the lead content of lettuce roots is 2.40 times higher than in stems
and leaves. For carrots, the lead content in roots is 2.67 times higher than in
stems and leaves. This rate in potatoes is 2.65.
Besides the growth, the data
of lead amount in the biomass of selected vegetables obtained in experimental
field were recorded to give a clear answer to the question of which plants can
be used as food under those farming circumstances. The results obtained showed
that lead was a cumulative metal. When we increased lead amount in the soil,
its levels hoarding in the biomass of examined vegetables were increased (Table
4).
The results showed that, when
lead content in soil ranged from 100 to 1500 mg/kg, the amount of this metal in
the biomass of four studied vegetables ranged between 0.05 and 6.79 mg/kg.
Effects of cultivation mode on the
accumulation of lead from soil to vegetables
Effect of lime: The results
showed that the level of absorption and accumulation of lead from the soil on
the biomass of vegetables decreased when the pH of the soil increased from 6.0
to 7.5. The average lead content in every part of examined vegetables decreased
by 7‒15% when
the pH in soil increased from 5.97 to 6.42, reduced by 13‒25% when pH soil rose from 5.97 to 7.05 and
decreased by 23‒35% when
pH increased from 5.97 to 7.52 (Fig. 4a).
Table 4: The amount of lead in
inspected vegetables
|
Amount of lead in soil
(mg/kg) |
Amount of lead in the
biomass of vegetables (mg/kg) |
|||||||
|
Spinach |
Lettuce |
Carrots |
Potatoes |
|||||
|
Stems & Leaves |
Roots |
Stems & Leaves |
Roots |
Stems & Leaves |
Roots |
Stems & Leaves |
Roots |
|
|
Control |
0.07 ± 0.01 |
0.11 ± 0.01 |
0.09 ± 0.01 |
0.13 ± 0.01 |
0.11 ± 0.01 |
0.13 ± 0.01 |
0.05 ± 0.01 |
0.19 ± 0.02 |
|
100 |
0.23 ± 0.02 |
0.72 ± 0.06 |
0.20 ± 0.02 |
0.71 ± 0.06 |
0.25 ± 0.03 |
0.85 ± 0.09 |
0.28 ± 0.03 |
1.02 ± 0.09 |
|
200 |
0.33 ± 0.02 |
1.11 ± 0.10 |
0.26 ± 0.03 |
0.83 ± 0.07 |
0.96 ± 0.11 |
2.38 ± 0.24 |
0.46 ± 0.05 |
1.79 ± 0.18 |
|
300 |
0.89 ± 0.07 |
1.79 ± 0.16 |
0.68 ± 0.07 |
1.26 ± 0.11 |
1.37 ± 0.14 |
3.15 ± 0.30 |
1.57 ± 0.16 |
2.75 ± 0.25 |
|
400 |
1.19 ± 0.11 |
2.75 ± 0.25 |
0.73 ± 0.06 |
1.97 ± 0.21 |
1.90 ± 0.20 |
4.53 ± 0.43 |
1.67 ± 0.15 |
3.85 ± 0.40 |
|
600 |
1.31 ± 0.12 |
2.77 ± 0.25 |
1.17 ± 0.20 |
2.05 ± 0.22 |
2.15 ± 0.20 |
5.29 ± 0.50 |
2.00 ± 0.21 |
4.79 ± 0.46 |
|
800 |
1.79 ± 0.16 |
3.98 ± 0.40 |
1.62 ± 0.17 |
2.41 ± 0.22 |
2.48 ± 0.25 |
5.84 ± 0.60 |
2.72 ± 0.25 |
5.17 ± 0.50 |
|
1000 |
1.98 ± 0.20 |
4.97 ± 0.49 |
1.79 ± 0.19 |
3.89 ± 0.40 |
2.72 ± 0.26 |
6.79 ± 0.65 |
Dead |
Dead |
|
1200 |
2.16 ± 0.21 |
5.14 ± 0.49 |
1.93 ± 0.20 |
4.72 ± 0.49 |
Dead |
Dead |
Dead |
Dead |
|
1500 |
2.29 ± 0.21 |
5.52 ± 0.51 |
2.07 ± 0.21 |
4.99 ± 0.50 |
Dead |
Dead |
Dead |
Dead |
%2049-58_files/image008.png)
Fig. 4: Effects of agricultural lime
(a) and N, P, K fertilizers (b, c, d) on lead accumulation of studied
vegetables (error bar = SD, n = 3)
The Effects of N-, P-, K-fertilizers on the
Pb(II) accumulation
Inorganic
fertilizers, such as N, P, K, are often used for a cultivation process due to
their nutrient levels. However, the use of large amounts of fertilizers to
achieve maximum yields can affect the chemical properties of agricultural soil
and the quality of crop products. In addition, the presence of this kind of
fertilizer in the soil can affect the Pb(II) accumulation of some vegetables. Fig.
4b, c, d show the effects of N-, P-, K-fertilizers on the Pb(II)
accumulation of four plants, namely carrots, potatoes, spinach, and lettuce.
Clearly, the contents of accumulated lead in all the biomass were increased as
the amount of N applied to the plants increased by 3 times. For instance, the
accumulated lead content in the stem & leaves of spinach, lettuce, carrot,
and potato increased order by 30.9, 55.6, 61.5 and 50.0%, whereas the lead
content in the roots of the four kinds above rose by 52.0, 52.9, 30.4 and
55.8%, respectively. Similarly, the presence
of K in the soil will promote the absorption and transport of lead from the
soil to the plants. When increasing the amount of N fertilizer by 3 times
during the cultivation process, the level of lead accumulation in the stem
& leaves and roots increased by 32.4 and 37.6% for spinach, 66.7 and 47.2% for lettuce, 54.5 and 27.4% for
carrot, 52.9 and 38.8% for potato, respectively. In contrast, the absorption of
lead from the soil to the biomass of the studied vegetables was inhibited when
the P fertilizer in the soil was increased by triple. For example, the amount
of accumulated lead in the stem & leaves, and roots was ordered decreased
by 39.6 and 33.1% for spinach, 40.7 and 38.8% for lettuce, 43.5 and 31.5% for
carrot, and 51.5 and 42.8% for potato.
Design of experiments for estimation of
optimum conditions on the cultivation mode
Table 5: Maximum and minimum levels of
selected factors
|
Factors |
Symbol |
Unit |
Min (-1) |
Central point |
Max (+1) |
|
Mass of N fertilizer |
X1 |
mg/kg soil |
1.15 |
2.875 |
4.6 |
|
Mass of P fertilizer |
X2 |
mg/kg soil |
5.15 |
12.875 |
20.6 |
|
Mass of K fertilizer |
X3 |
mg/kg soil |
1.25 |
3.125 |
5 |
%2049-58_files/image010.png)
Fig. 5: Response
surfaces estimated from factorial design
The above results showed that lettuce and spinach can adapt with lead
contaminated soil better than carrots and potatoes. Besides, mass of inorganic
fertilizers, i.e., N-, P-, K-fertilizer significantly affected the accumulation
of lead from soil to vegetables. Thus, a two-level full factorial design with
five replicates of central point was carried out to determine the mass of N-,
P-, and K-fertilizers to limit the content of lead accumulated in the edible
parts of spinach and lettuce. The independent variables selected are shown in
Table 5 along with their min, medium and max levels, which were determined from
preliminary trials.
The
responses of this matrix included the amount of lead accumulated in the edible
parts of spinach (Y1) and lettuce (Y2). The factorial
design demonstrated that the variables in the studied required a final
optimization. The response surface considering the equation is shown in Fig. 5.
The relation among these factors and lead content in the edible parts of
spinach and lettuce was described in these equations:
For spinach:
Y1 =
0.2360 + 0.0187X1 – 0.0188X2 + 0.03X3 – 0.005X1X2
– 0.0025X1X3 + 0.0125X2X3 + 0.007X12
– 4.75X22 – 3.08X32.
For lettuce:
Y2 = 0.208
+ 0.0237X1 – 0.0163X2 + 0.04X3 – 0.005X1X2
+ 0.0077X1X3 + 0.0175X2X3 + 0.011X12
– 0.009X22 – 0.0015X32;
where X1:
Mass of N fertilizer (mg/kg soil); X2: Mass of P fertilizer (mg/kg
soil); X3: Mass of K fertilizer (mg/kg soil).
According
to this result, the optimal conditions on the cultivation mode to limit the amount
of lead accumulated in the edible parts of spinach and lettuce were determined
as follows: 1.329 mg of N fertilizer, 19.950 mg of P fertilizer and 1.562 mg of
K fertilizer per 1 kg of soil. At the optimal value of these factors, the
content of lead accumulated in the edible parts of spinach and lettuce
estimated by were 0.165 and 0.135 mg/kg, respectively (p < 0.0001).
Discussion
The results showed that the content of lead
in the biomass of vegetables depends on the nature of each vegetable. Lead accumulation
in these vegetables were as the following the order: carrots > potatoes >
spinach > lettuce. The highest lead amount was found in roots of carrots
(1.29 ÷ 6.79 mg/kg), while edible parts of lettuce showed the lowest lead level
(0.20 ÷ 2.07 mg/kg), suggesting a resistance towards lead accumulation.
Besides, lead accumulated in the roots of all studied vegetables. The amount of
lead decreased in the order of roots of carrots > potatoes > spinach >
lettuce > stems and leaves of spinach > carrots > potatoes >
lettuce.
For leafy vegetables, the
average lead content in spinach roots were 2.53 times higher than in stems and
leaves. While the lead content of lettuce roots were 2.40 times higher than in
stems and leaves. For carrots, the lead content in roots is 2.67 times higher
than those in stems and leaves. This rate in potatoes is 2.65. Basu et al.
(2013) showed that lead accumulation in the crops follows the order: carrots
> beet > cabbage > brinjal > cauliflower > spinach > tomato
> chilly. Whereas, its concentration in various parts of plants showed: root
> stems > leaves > other edible parts. This demonstrated the
characteristic tendency of lead to be accumulated in the roots rather than in
other parts of plants.
By WHO standards (FAO/WHO, Codex Alimentarius
Commission. (2001), 0.3 mg/kg is the maximum allowable limit of lead
in edible parts of vegetables, beyond which health is affected. According to
this regulation, all edible parts of potatoes and carrots exceeded the
allowable limit when cultivated on soil contaminated by lead at 100 mg/kg in
present study. For spinach and lettuce, when grown on contaminated soil by lead
below 100 mg/kg and 200mg/kg, respectively, neither drop the crop yields nor
pose any risk to consumers’ health.
According to QCVN
03-MT:2015/BTNMT, Vietnam Ministry of Natural Resources & Environment 2015 the maximum allowable
concentration of lead for Vietnamese agricultural soil is 70mg/kg. However,
based on the results of this study, Pb content in edible parts of spinach grown
in soil contaminated by Pb at 100 mg/kg did not exceed the allowable limit.
Lettuce could grow in Pb soil 200 mg/kg but lead contents in stems and leaves
were still lower than its permissible level.
The contents of accumulated lead in all the biomass increased
as the amount of N applied to the plants increased. For instance, the levels of
lead in edible parts of selected vegetables are risen from 25.0 to 28.4% and
from 35.0 to 49.4% when increasing in the amount of nitrogen by a half and
double, respectively. This can be explained by the soil acidification by adding
of N-fertilizer into the soil (Tian and Niu
2015; Ghimire et al. 2017).
The increase in the amount of nitrogen will promote nitrification, plant
assimilation, and volatilization (as ammonia) of ammonium, resulting in the
release of protons to the soil (Reuss and
Johnson 2012). Additionally, the N fertilizer can stimulate the growth
rate of plants due to an uptake of cations and the release of equivalent
amounts of protons to the rhizosphere (Van
Breemen et al. 1983). These leads to the increase in the content of
dissolved lead in soil, which enhances the Pb(II) accumulation.
Similarly,
an increase in the amount of K in soil promotes the uptake and transport of
lead from the soil to biomass. Fig. 4c presents that when doubling the amount
of K fertilizer, the lead content in stems plus leaves and roots of leafy
vegetables increases by 30.4 and 34.7% for spinach, 30.0 and 38.0% for lettuce;
meanwhile, the amount of this metal in roots of carrots and potatoes raised by
42.4 and 40.2%, respectively. Obviously, potassium promotes nutrient metabolism
between plants and soil, leading to increasing the uptake of metal ions. In
addition, this phenomenon may be related to the amount of chloride anion by
using fertilizer as KCl salt due to the formation of soluble complexes of the
participated PbCl2 at the Cl- high concentrations. The obtained results are consistent
with some previous reports (Zhao et al. 2003; Elouear et al.
2016).
On the other hand, the uptake of lead from the soil on the biomass
of vegetables decreases when the phosphorus are applied to the soil. With an
(1.5–2 fold) increase in the amount of P fertilizer, the average content of
lead accumulated in all parts of these vegetables reduces to 12.5% compared to
control. Meanwhile, reducing the amount of phosphorus fertilizer raised the
average lead content by 25.12%. It is understandable that by adding phosphorus
fertilizer to the soil, Pb2+ reacts with phosphate anion to produce
precipitated pyromorphite. Therefore, P-containing fertilizers reduce the
solubility of lead, resulting in a decrease in the lead accumulation in plant
biomass. However, Weber JS et al. (Weber et al. 2015) proved that the P
fertilizer contained not only nutrient elements but also non-nutrient ones such
as Cd or Hg, etc. The presence of these metals in phosphate fertilizer has
caused the phenomenon of competition in the transport process of lead from soil
to plants, reducing the accumulation of lead in plants. Thus, cultivation mode
should add phosphorus at a suitable dose to avoid soil to be contaminated by
other heavy metals (Table 4 and Fig. 4d).
Conclusion
Results showed that when the lead
content in soil ranged from 100 to 1500 mg/kg, the accumulation
of lead in the biomass of these vegetables
ranged between 0.05 and 6.79 mg/kg. The amount of
agricultural lime, N-, P- and K-fertilizer
had certain effects on the accumulation of lead from soil to plants. The
optimal conditions on the cultivation mode to limit the amount of lead
accumulated in the edible parts of vegetables which can adapt to heavy
contaminated soil with limitative accumulation - spinach and lettuce - were
also determined.
Acknowledgments
This
research was supported by a Grant-in-Aid for Scientific Research
No.
08TĐ from Dalat University, Vietnam.
Author Contributions
TLTT and HNV planned
the experiments, TLTT, V-PD and TLV interpreted the results, TLTT and HNV
histological observation, TLTT and V-PD statistically analyzed the data and
made illustration, TLTT, V-PD and TLV writing original draft and editing. All
authors revised and completed the final version.
Conflicts of Interest
Authors declare no
conflict of interest.
Data Availability
Data are available
from the first author on reasonable request.
Ethics Approval
Not applicable in
this paper
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