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* For correspondence.
Journal of Environmental Protection and Ecology 18, No 2, 468–478 (2017)
Soil pollution
POTENTIAL OF RAPESEED (Brassica napus L.) FOR
PHYTOREMEDIATION OF SOILS CONTAMINATED WITH
HEAVY METALS
V. R. ANGELOVAa*, R. I. IVANOVAb, J. M. TODOROVb, K. I. IVANOVa
aDepartment of Chemistry, Agricultural University, Plovdiv, Bulgaria
E-mail: vileriz@abv.bg
bDepartment of Plant Science, Agricultural University, Plovdiv, Bulgaria
Abstract. A eld study was conducted to evaluate the efcacy of rapeseed (Brassica napus L.) for
phytoremediation of contaminated soils in the absence and presence of organic soil amendments
(compost and vermicompost). The experiment was performed on an agricultural eld contaminated
by the Non-ferrous-metal Works near Plovdiv, Bulgaria. The eld experimental was a randomised
complete block design containing ve treatments and four replications (20 plots). The treatments
consisted of a control (no organic amendments), compost amendments (added at 20 and 40 t/da),
and vemicompost amendments (added at 20 and 40 t/da). Upon reaching commercial ripeness, the
rapeseed plants were gathered. The oil from ground seed was derived under laboratory conditions
through an extraction method with the Socksle apparatus. Heavy metal contents in roots, stems, leaves,
pods, seeds, oils and meals of rapeseed were determined. The addition of compost and vermicompost
leads to decrease of the content of Pb, Zn and Cd, in the roots and stems, while the content of Pb
and Cd increases in the pods of the rape. The addition of organic meliorants signicantly reduces
the content of the heavy metals of seeds and the oil. The oil from the control, as well as the oils
obtained by processing the seeds from the variants with addition of compost and vermicompost,
does not contain Cd, while Pb and Zn have values below the permissible limit values. The rape is
a plant which is tolerant to heavy metals, can be grown in heavy metal polluted soils, and can be
successfully used in the phytoremediation of heavy metal polluted soils. The possibility of further
industrial processing of seeds to oil and using the obtained oil will make rapeseed economically
interesting crops for farmers of phytoremediation technology.
Keywords: phytoremediation, heavy metals, rapeseed, organic amendments.
AIMS AND BACKGROUND
Heavy metal contamination of agricultural soils is a worldwide problem. The
remediation of metal contaminated sites often involves expensive and environ-
mentally invasive and civil engineering based practices. A range of technologies
such as xation, leaching, soil excavation, and landll of the top contaminated
soil ex situ have been used for the removal of metals. Many of these methods have
high maintenance costs and may cause secondary pollution or adverse effect on
biological activities, soil structure, and fertility1. Phytoremediation is an emerg-
469
ing technology, which should be considered for remediation of contaminated sites
because of its cost effectiveness, aesthetic advantages and long term applicability.
This technology can be dened as the efcient use of plants to remove, detoxify or
immobilize environmental contaminants in soils, waters or sediments through the
natural, biological, chemical or physical activities and processes of the plants. It is
best applied at the sites with shallow contamination of organic, nutrient or metal
pollutants2. This plant-based technique is essentially an agronomic approach and
its success depends ultimately on agronomic practices applied at the site.
Addition of organic matter amendments, such as compost, fertilisers and
wastes, is a common practice for immobilisation of heavy metals and soil ameliora-
tion of contaminated soils3. Organic amendments are able to improve soil physical,
chemical and biological properties by: (i) raising the pH; (ii) increasing the organic
matter content; (iii) adding essential nutrients for plant growth; (iv) increasing the
water holding capacity, and (v) modifying heavy metals bioavailability4–6.
The use of crop plants for phytoremediation of contaminated soils has the
advantages of their high biomass production and adaptive capacity to variable
environments7,8. However, to succeed they must be tolerant to the contaminants
and be capable of accumulating signicant concentrations of heavy metals in their
tissues. Additionally, crops could make the long time-periods for decontamination
more acceptable, economically and environmentally. If the contaminated biomass
may be further proceed for added value products (not only concentrated on deposits
of hazardous wastes), then such fact represents an improvement of economical
efciency of phytoremediation technology. Industrial plants, i.e. energy crops
or crops for bio-diesel production, are therefore the prime candidates as plants
for phytoremediation. The use of energy and/or bio-diesel crops as plants for
phytoremediation would give contaminated soil a productive value and decrease
remediation costs.
Over the past years, there has been a growing interest in the use of oleaginous
crops (such as rapeseed (Brassica napus)) for phytoextraction, or the sustainable use
of land polluted with heavy metals9. Some plants of the Brassicaceae family have
an extraordinary capacity to accumulate metals in their above-ground parts, some
of which relate to the hyperaccumulators. For example, Thlaspi caerulescens can
contain more than 10 000 mg/kg Zn in the leaves10. It has been found that within
the genus Brassica, there are other types which have a tendency to accumulate high
concentrations of metals and which can be characterised as metal accumulators.
Examples include Brassica juncea (Indian mustard), Brassica rapa (eld mustard)
and Brassica napus (rape)11. It has been proven that Brassica juncea can accumu-
late high levels of heavy metals (Cd, Cr, Cu, Ni and Pb) when the solubility of the
metals in the soil increases. Meers et al.12 found that Brassica rapa showed a high
capacity for accumulation of Cd and Pb from the soil, with or without addition of
supplements to mobilize elements from the soil. However, the accumulation is too
470
low, and the rapeseed is not suitable for phytoremediation. Marchiol et al.13 found
that both Brassica species (Brassica napus and Raphanus sativus) are moderately
tolerant when grown on soils slightly polluted with heavy metal.
The main objective of this paper is to conduct a systematic study, which will
help to determine the impact of organic soil amendments on the uptake of the
heavy metals by rapeseed (Brassica napus L.), as well as the possibilities to use
the plant for phytoremediation of heavy metal contaminated soils.
EXPERIMENTAL
The experiment was performed on an agricultural eld contaminated by the
Non-ferrous-Metal Works near Plovdiv, Bulgaria. The eld experimental was a
randomised complete block design containing ve treatments and four replications
(20 plots): 1 – introduction of 20 t/da of vermicompost to the soil, 2 – introduc-
tion of 40 t/da of vermicompost to the soil, 3 – introduction of 20 t/da of compost
to the soil, 4 – introduction of 40 t/da of compost to the soil, 5 – control variant.
Characteristics of soils and organic amendments are shown in Table 1. The
soils used in this experiment were slightly acidic, with moderate content of organic
matter and essential nutrients (N, P and K) (Table 1). The psedo-total content of
Zn, Pb and Cd is high (1430.7 mg/kg Zn, 876.5 mg/kg Pb and 31.4 mg/kg Cd,
respectively) and exceeds the maximum permissible concentrations (320 mg/kg
Zn, 100 mg/kg Pb, 2.0 mg/kg Cd).
Table 1. Characterisation of the soil and the organic amendments used in the experiment
Parameter Soil Compost Vermicompost
pH 6.5 6.9 7.5
EC (dS/m) 0.2 0.2 2.2
Organic matter (%) 3.99 72.10 38.58
N Kjeldal (%) 0.24 2.22 1.57
C/N 9.41 32.43 24.59
Pseudo-total P (mg/kg) 642 12654 10211
Pseudo-total K (mg/kg) 5518 6082 10495
Pseudo-total Pb (mg/kg) 876.5 12.0 32.3
Pseudo-total Zn (mg/kg) 1430.7 170.8 270.3
Pseudo-total Cd (mg/kg) 31.4 0.19 0.69
To determine the effect of the organic amendments, the soil samples were
collected 1 month after addition of organic amendments. A soil subsample was
air-dried, passed through a 2-mm sieve and characterised for soil pH (H2O) in
deionised water suspension of 1:5 (w/v); total nitrogen by the Kjeldahl method
(N Kjeldahl); total oxidisable organic carbon according to Tube digestion method
(with titration)14.
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The pseudo-total and DTPA-extractable concentration of heavy metals in
the soils, after four weeks equilibration were determined. Pseudo-total content
of metals in soils was determined in accordance with ISO 11466 (Ref. 15). The
available (mobile) heavy metals contents were extracted by a solution of DTPA
(1 M NH4HCO3 and 0.005 M DTPA, pH 7.8) (Ref. 16). The same procedures were
applied to organic amendments.
The test plant was rapeseed (Brassica napus L.), hybrid Elit. Upon reaching
commercial ripeness, the rapessed plants were gathered and the content of heavy
metals in their different parts (roots, stems, pods and seeds) was quantitatively
determined. The oil from rapeseed was derived under laboratory conditions through
an extraction method with the Socksle apparatus, allowing the extraction of the oil
from the preliminarily peeled and ground seeds of rapeseed by using petroleum
ether and the subsequent liberation of the latter through distillation. The concen-
trations of Pb, Zn and Cd in their different parts (roots, stems and seeds), meals
and oils were determined by the method of dry mineralisation. To determine the
heavy metal content in the samples, inductively coupled emission spectrometer
(Jobin Yvon Emission – JY 38 S, Paris, France) was used.
Certied reference materials (contaminated brickworks soil – ERM CC135a
and Apple leaves –1515 standard reference material) were used for quality control.
The results show acceptable agreement between the found and certied values for
Cd, Pb and Zn. Statistical analyses were conducted with Statistica v. 7.0.
RESULTS AND DISCUSSION
ACCUMULATION OF HEAVY METALS IN VEGETATIVE AND REPRODUCTIVE
ORGANS OF RAPESEED WITHOUT AMENDMENT (CONTROL)
To clarify the issues of absorption, accumulation and distribution of heavy metals
in vegetative and reproductive organs of rapeseed were analysed samples of roots,
stems, pods and seeds. Table 2 presents the results obtained for the content of
heavy metals in the vegetative and reproductive organs of the study oilseed crop.
The content of Pb in the roots of rapeseed without amendments reached to 56.2
mg/kg, Zn – 330.70 mg/kg, Cd – 14.9 mg/kg. Our results indicate that a considerable
part of the heavy metals are accumulated in the roots, which is consistent with the
results of other authors17,18. This is explained by the fact that during the penetra-
tion of heavy metals in the plasma there is inactivation and disposal of signicant
quantities of them, as a result of the formation of slightly mobile compounds with
the organic substance. According to Mathe-Gaspar and Anton19, rape accumulates
mainly heavy metals in the roots, which is conrmed by our results. According to
Turan and Esringu20, the content of Pb in the roots is 31 times higher than than in
the aboveground mass. The high concentration of Cu and Pb in the roots and the
low translocation factor indicate the possibility of rapeseed to be used in phyto-
472
stabilisation. Most of the heavy metals in the soil are xed and accumulate in the
roots of the rapeseed, as in rapeseed the main root mass is developed and is set in
shallow in the surface soil horizon in which the heavy metal content is the highest.
Perhaps this is the reason to accumulate a larger amount of heavy metals in the
roots in the cultivation of rape on heavy metal polluted soils.
Тable 2. Content of heavy metals (mg/kg) in vegetative and reproductive organs of rapeseed, oil
and meal (without amendment, control)
Element Roots
x ± sd
Stems
x ± sd
Pods
x ± sd
Seeds
x ± sd
Oil
x ± sd
Meal
x ± sd
Pb 56.2±2.5 9.65±0.8 66.1±3.6 4.3±0.2 0.05±0.005 6.9±0.2
Cd 14.87±1.3 11.85±0.5 10.5±2.1 1.0±0.1 nd 1.1±0.1
Zn 330.7±5.3 288.1±2.8 171.4±6.8 133.5±2.0 1.3±0.4 136.4±2.1
x – average value (mg/kg) from 5 repetitions; sd – mean standard deviation, nd – not detectable.
The content of Pb, Zn and Cd in stems of rapeseed is less compared to the root
system, which indicates that their movement in the conduction system is severely
limited. There is a minor accumulation of Pb in the stems of rape. The content of
this element reaches 9.65 mg/kg in the stems, and is signicantly lower than the
toxic levels for the animals – 30 mg/kg (Ref. 21), despite that the total content of
Pb in the soil from the eld reaches up to 876.5 mg/kg and signicantly exceeds
the default values of 100 mg/kg for toxic effects on plants22.
The results show moderate ability of rape to accumulate Cd in the aboveground
mass. Such are the results of Ebbs and Kochian11 according to whom the content
of Cd in the aboveground mass of B. napus reaches up to 3 mg/kg DW after a
period of growth of 3 weeks in neutral clay soils with concentrations of total of Cd
40 mg/kg. The results are signicantly lower than the values established by Ebbs
and Kochian11 for Zn in the aerial aboveground mass of B. napus of 600 mg/kg in
growing it for 3 weeks in neutral clay soils.
The ratio of the heavy metals in the stem and the roots in the tested rape hybrid
grown on heavy metal polluted soil under eld conditions, is less than 1, which
means that the hybrid is not an accumulator of heavy metals and can not be used
for phytoextraction of heavy metals from the soil. Our results are in accordance
with Rossi et al.23 and Kadar et al.24 according to whom the rapeseed accumulates
moderate amount of heavy metals in the stems and has a relatively lower potential
for phytoextraction compared to the wild species of the family Brassicaceae.
The content of Pb, Cd and Zn in the fruits of the researched rape hybrid is
higher than that of the stems. The higher content of heavy metals in the fruit shell
is mainly due to their location and their rough surface, which is a prerequisite for
possible anthropogenic pollution. Our results are consistent with those of Del Rio
et al.25, according to whom signicant amount of Pb and Zn is accumulated in the
fruits of rapeseed.
473
The heavy metal content in the seeds was signicantly lower compared to the
root system and the aboveground mass of the plants. The content of Pb in the seeds
of rape reaches up to 4.3 mg/kg, Zn up to 133.5 mg/kg and Cd up to 1.0 mg/kg. The
results obtained strongly suggest that the pods act as a selective lter in the way
of heavy metals to the seeds and depends primarily on the specicity of studied
hybrid and the researched element. The statement of Dai et al.17 is conrmed ac-
cording to which the content of Cd in the seeds of rape is very low, and the main
part is localised in the carpellums of the fruits which appear the physiological
barrier regarding the absorption of Cd.
The results obtained are consistent with those of Korenovska and Palacekova26
and Dai et al.17, according to whom in the generative organs of rape grown on
heavy metal polluted soils small amounts of Cu, Zn, Pb and Cd are accumulated.
Signicantly higher are the results of Grisspen et al.27, according to whom in the
seed of rape the content of Cd varies between 3.6–8.1 mg/kg at a total content
of Cd in the soil of 5.5 mg Cd/kg soil in experiments conducted in Belgium, and
between 5.2 and 11.3 mg/kg at a total concentration of Cd in the soil 2.5 mg Cd/
kg soil in experiments conducted in the Netherlands.
The results show that the major part of the heavy metals contained in the
seeds, during processing do not pass into the oil, due to which their content is
signicantly lower. Pb content in rapeseed oil reaches up to 0.05 mg/kg and below
the limit concentrations of Pb in vegetable oils (0.1 mg/kg) and it can be used for
food purposes. Similar results were obtained for Zn and Cd. The values reported
for Zn and Cd in rapeseed oil are respectively 1.3 and 0.02 mg/kg and lower than
the maximum tolerances (10 mg/kg Zn and 0.05 mg/kg Cd).
The comparative analysis between our results and those published in the
literature shows that the content of Pb, Cd, and Zn is lower than the values of
Przybyliski28, Darracq et al.29 and Farzin and Moassesi30, although rapeseed from
our experiments was grown on heavily contaminated soil. The variation between
the individual results may be due to growing conditions, genetic factors, varietal
characteristics and other factors. Our results are in accordance with Anonymous31,
according to whom the reported content of Cu, Fe and Pb in rape oil is low. The
results obtained show that the main part of the heavy metals contained in the seeds
during processing does not go into the oil, thus their content is signicantly lower
than the maximum permissible concentrations.
The content of heavy metals in the rapeseed meal from control is shown
in Table 2. Our results for Zn are higher in comparison with the published data
(Bell32 – 72 mg/kg, Anonimous33 – 57–80 mg/kg), as rape is grown on heavy metal
polluted soil. In terms of Pb and Cd we can not do a comparative analysis of our
results as there is no data for these items published in the literature. The content
of Pb in the control meals reaches up to 6.9 mg/kg, Zn – 136.4 mg/kg, and Cd –
1.08 mg/kg. The amounts of Pb and Zn in the meals are below the critical values
474
of 30 mg/kg Pb and 300 mg/kg Zn, while the content of Cd exceeds the critical
value of 0.5 mg/kg Cd for feed.
IMPACT ON ORGANIC AMENDMENTS ON ACCUMULATION OF HEAVY METALS
IN THE VEGETATIVE AND REPRODUCTIVE ORGANS OF RAPESSED, RAPESEED
OIL AND MEAL
The inuence of compost on the uptake of heavy metals from the roots of rape is
not unidirectional. The addition of 20 t/da of compost leads to increased content
of Pb in the roots and stems of rape, while the addition of 40 t/da leads to decrease
in the content of Pb, Zn and Cd in the roots and stems of rape (Fig. 1).
The addition of compost leads to increase of the content of Pb and Cd in pods
of rape, as this increase is more pronounced in the addition of 40 t/da of compost.
The content of Zn in pods of rape decreases after the addition of compost, as this
decrease is more pronounced after the addition of 40 t/da of compost. The addition
of vermicompost also decreases the content of heavy metals in roots and stems
compared to the control, as this decrease is more pronounced in the addition of 20
t/da vermicompost (Pb and Zn), and in the respect of Cd – in the addition of 40 t/
da of vermicompost (Fig. 1).
Regarding the content of Pb and Cd in pods there is a tendency of increase,
while in Zn a decrease is observed.
Fig. 1. Effect of different organic amendments (compost and vermicompost) applications to accu-
mulation of heavy metals in the vegetative and reproductive organs of rapeseed
The decrease of the content of heavy metals in the seeds compared to the
control is strongly expressed, as in the option with compost the Pb content is
475
reduced from 4.3 to 2.5 mg/kg, and in the option with vermicompost there is a
slight increase (Fig. 1). Similar results are obtained for Cd. The Zn content in
seeds of rape after the addition of organic meliorants decreases to a much lesser
extent than Pb and Cd.
The addition of compost and vermicompost reduces the content of Pb in the
oil respectively to below the detection limits and these concentrations are lower
than the maximum permissible concentrations of oil of plant origin (0.1 mg/kg)
(Fig. 1). The addition of compost and vermicompost reduces Zn content in the oil,
as this decrease is more strongly expressed in the addition of 40 t/da of compost and
40 t/da of vermicompost (corresponding to 0.97 and 1.08 mg/kg, respectively). In
all variants, however, Zn content in the oil is lower than the maximum permissible
concentrations of oil of plant origin (10 mg/kg). The content of Cd in rapeseed oil
is below the limits of the quantitative measurement with the method used both in
the control and in the the variants with the addition of organic meliorants. Rapeseed
oil can be used for food purposes.
The importation of compost and vermicompost leads to increased content of
Pb in meals compared to the control of up to 7.58 mg/kg (40 t/da of compost) and
9.22 (20 t/da of vermicompost). Despite this increase in the Pb content, these values
are lower than the maximum permitted concentrations for animal feed (30 mg/kg).
The importation of 40 t/da of compost and 40 t/da of vermicompost reduces the
content of Zn in meals, respectively to 109.53 and 96.33 mg/kg, and these values
are lower than the maximum permitted concentrations of feed (500 mg/kg). The
importation of organic meliorants leads to a slight increase in the content of Cd,
with the exception of the option of deposit of 40 t/da of compost. The content
of Cd in meals reduces to 0.975 mg/kg, but this concentration is higher than the
maximum permissible levels for feed (0.5 mg/kg) (Ref. 34).
The distribution of heavy metals in the organs of rape has a selective character
and it is specic for the individual elements. The main part of Pb is accumulated
in the pods (46%) and a very small amount is contained in the seeds (3%). With
respect to Zn and Cd the main part is accumulated in the roots of rape (36 and
39%) followed by stems, pods and seeds. The seeds contain only 3% of the total
amount of Cd absorbed by rape. Signicantly higher is the content of Zn in the
seeds – 14% of the total amount of absorbed Zn.
The distribution of Pb in the organs of plants of all options with the addition
of compost follows the same correlation observed in the control. The highest con-
tent of Pb was found in the pods, followed by the roots, stems and seeds. These
results correspond to the results of Mathe-Gaspar and Anton19 who found that in
the aboveground parts of the plants the accumulation of heavy metals is less than
that in the roots.
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CONCLUSIONS
It can be concluded thah the rape is a plant which is tolerant to heavy metals and
can be grown in heavy metal polluted soils, and can be successfully used in the
phytoremediation of heavy metal polluted soils. The addition of compost and
vermicompost leads to decrease of the content of Pb, Zn and Cd, in the roots and
stems, while the content of Pb and Cd increases in the pods of the rape. The ad-
dition of organic meliorants signicantly reduces the content of the heavy metals
of seeds and the oil. The oil from the control, as well as the oils obtained by pro-
cessing the seeds from the variants with addition of compost and vermicompost,
does not contain Cd, while Pb and Zn have values below the permissible limit
values (0.1 mg/kg of Pb and 10.0 mg/kg of Zn, respectively). The processing of
the seeds to oil and the use of the obtained oil will signicantly reduce the cost
for phytoremediation.
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Received 7 May 2017
Revised 15 June 2017