Journal of Environmental Science and Health, Part A

Toxic/Hazardous Substances and Environmental Engineering

ISSN: 1093-4529 (Print) 1532-4117 (Online) Journal homepage: https://www.tandfonline.com/loi/lesa20

Evaluation of the impact of soil contamination

with mercury and application of soil amendments
on the yield and chemical composition of Avena
sativa L.

Wiera Sądej, Andrzej C. Żołnowski, Zdzisław Ciećko, Łukasz Grzybowski &

Radosław Szostek

To cite this article: Wiera Sądej, Andrzej C. Żołnowski, Zdzisław Ciećko, Łukasz Grzybowski
& Radosław Szostek (2019): Evaluation of the impact of soil contamination with mercury and
application of soil amendments on the yield and chemical composition of Avena�sativa L., Journal of
Environmental Science and Health, Part A, DOI: 10.1080/10934529.2019.1667671

To link to this article: https://doi.org/10.1080/10934529.2019.1667671

Published online: 24 Sep 2019.

Submit your article to this journal

View related articles

View Crossmark data

Full Terms & Conditions of access and use can be found at

https://www.tandfonline.com/action/journalInformation?journalCode=lesa20
JOURNAL OF ENVIRONMENTAL SCIENCE AND HEALTH, PART A
https://doi.org/10.1080/10934529.2019.1667671

Evaluation of the impact of soil contamination with mercury and application of

soil amendments on the yield and chemical composition of Avena sativa L.
Wiera Sa˛deja _
, Andrzej C. Zołnowskia
, Zdzisław Cieckoa,b, Łukasz Grzybowskic, and Radosław Szosteka
a
Department of Environmental Chemistry, University of Warmia and Mazury, Olsztyn, Poland; bHigher School of Ecology and Management in
Warsaw, Poland; cViridor – Energy From Waste, Salmon Pastures Attercliffe Road, Sheffield, UK

ABSTRACT ARTICLE HISTORY

The purpose of this study was to determine the effect of soil contamination with Hg on the yield Received 1 July 2019
and chemical composition of Avena sativa L. Mercury was incorporated into soil in amounts: 0, 50, Accepted 4 September 2019
100 and 150 mg Hg
kg1of soil. Zeolite, lime and bentonite were used to alleviate the soil con-
KEYWORDS
tamination. Plants cultivated in Hg-polluted soil showed growth inhibition even in the presence of
soil contamination; soil
bentonite, lime or zeolite. Under elevated doses of Hg, the yield of aerial mass and roots amendments; plants; yield;
decreased. The soil amendments mitigated the adverse effect of contamination, with lime and macronutrients uptake
bentonite having a more beneficial influence on the yield than zeolite. The incremental contamin-
ation with mercury led to an increase in the content of Hg in the biomass of the plants. A much
higher content of Hg was found in roots than in aerial parts. The inactivating substances applied
to soil to some extent limited the increase in the content of this metal in all plant organs. Lime
proved to be most effective in this regard. An increase in the soil contamination with mercury
caused an increased content of nitrogen and potassium in plant organs and a decrease content
of phosphorus.

Introduction Mercury is an element with a documented toxic action,

Among the multitude of pollutants emitted to the environ-
ment, mercury and mercury compounds pose a particularly
serious threat.[1–7] The presence of this element detected in
various compartments of the natural environment over the
past several years is perceived as a global threat, which
should be given a priority treatment.[8–10]
Natural sources of mercury in the environment are rock
weathering processes, volcanic eruptions, evaporation from
seas and oceans and forest fires. However, all these sources
are responsible for no more than a third of the global emis-
sion of mercury.[3,11] The remainder originates from
anthropogenic sources,[12] of which the most important are
surface mining of black coal, lignite and metal ores,[13–16]
power generation industry,[17] cement industry,[18,19] metal
smelting and metallurgy. Mercury can also be released from
inadequately stored mercury-containing waste[20–23] and
during waste incineration processes.[24–29]
Out of the anthropogenic sources mentioned above, com-
bustion of fossil fuels, particularly coal, is implicated as the
main source of mercury emission.[13,14,17,30–36] Poland is
responsible for the largest anthropogenic emission of mer-
cury in the European Union.[37] Estimates of the National
Centre for Emissions Management state that the annual
emission of mercury in Poland exceeds 10 Mg, of which
about 56% originates from coal combustion in the power
generation sector.[38]
and its actual toxicity depends on the form in which it
appears in the environment. While all forms of Hg are toxic,
organic Hg compounds such as methyl-Hg (CH3Hgþ) are
the most hazardous ones.[15]
Mercury can accumulate in different parts of living
organisms, causing enzymatic disorders and mutagenic
changes in the DNA structure.[39] In plant tissues, this
metal is strongly bound by protein sulfhydryl groups,
where it is responsible for distorting chemical processes
associated with cell respiration, mainly in the course of
enzymatic reactions. Although mercury does not play any
life functions in plants, they nonetheless absorb this elem-
ent from soil together with other substances. When com-
peting substances have been exhausted, the uptake of
mercury by plants grows.[40] Mercury accumulates mostly
in roots, from which it is transported, at different rates, to
aerial parts of higher plants.[41,42]
Soil polluted with chemical compounds can be purified
with both in situ and ex situ methods, for example using
inorganic adsorbents, such as clay minerals or aluminosili-
cates of alkali metals (zeolites). Depending on the acidity of
soil and its oxidative–reductive potential, such substances
create various assemblages of ions in the soil environment,
which can react with active centers located on the surface of
absorbents. According to Sarbak,[43] these reactions can be
physical ones, including dispersion, orientation of dipoles

_
CONTACT Andrzej C. Zołnowski andrzej.zolnowski@uwm.edu.pl Department of Environmental Chemistry, University of Warmia and Mazury, Olsztyn, Poland.
Color versions of one or more of the figures in the article can be found online at www.tandfonline.com/lesa.
ß 2019 Taylor & Francis Group, LLC
2 W. SA˛DEJ ET AL.
and induction of dipoles, and chemical ones, consisting of
the creation of a chemical bond between an adsorbed mol-
ecule and active centers of an adsorbent. The choice of an
adsorbent, and especially its proper surface and size of
pores, should correspond to the properties of molecules to
be removed.
Good results in terms of mercury inactivation are also
obtained through soil liming. In a study by Rolka et al.,[44]
following the stabilization of soil pH achieved by liming Hg-
polluted soil, an average content of this element in the aerial
biomass of yellow lupine was observed to have decreased by
33%. Moreover, application of lime alleviated the adverse
effect of mercury on the yield of lupine aerial biomass. A
significant role of soil pH was also indicated by Heermann
et al.[45] in their experiment on Vulpia myuros L., where the
mercury content declined by 50% after soil liming compared
to non-limed treatments. Similar results were reported by
Ciecko et al.[46] in an experiment with Zea mays L., where a
less severe decrease in yield due to the presence of mercury
occurred in limed soil.
The aim of this study was to analyze the impact of soil
contamination with mercury on the yield and chemical com-
position of selected plant species, and to determine the
usability of selected substances for the alleviation of adverse
effects of mercury on the test plants. This paper discusses
results of the research in which Avena sativa L. served as
the test plant.
Material and methods
Site and experimental design
The experiment was carried out in a greenhouse of the
Faculty of Environmental Management and Agriculture,
University of Warmia and Mazury in Olsztyn. All experi-
mental treatments were performed in three replications
using Kick–Brauckmann polyethylene pots, each filled with
9 kg of soil. The test plant was A. sativa L. The experiment
included two factors: (1) elevated doses of mercury (Hg)
polluting soil and (2) soil amendments neutralizing the toxic
effect of mercury. Contamination simulating mercury was
added to soil in the form of aqueous solution of HgSO4 in
doses of 0, 50, 100 and 150 mg Hg
kg1 of soil. In order to
mollify the toxic effect of mercury on the test plant, the fol-
lowing soil amendments were applied: natural zeolite, ben-
tonite and lime. Zeolite and bentonite were used in doses of
3% relative to the soil mass, while lime was added in a
quantity corresponding to 1 hydrolytic acidity (Hh) of soil
(6.8 g CaO
pot1). The substances added to the soil in order
to increase its sorption capacity (zeolite, bentonite) were
applied in doses most often recommended by the authors
studying the issues of phytostabilization of soils contami-
nated with heavy metals.[47]
All experimental treatments were fertilized with the same
doses of mineral NPK in accordance with the nutritional
requirements of A. sativa L. Nitrogen was used in the form
of CO(NH2)2 (46% N) in an amount of 1.2 g N per pot,
phosphorus as Ca(H2PO4)2H2O (20% P) in a dose of 0.52 g
P per pot, and potassium was added in the form of 60%
Table 1. Chemical composition of soil used in the experiment.
Available forms
Hg total
pH Hh C-org. P K Mg content
in H2O in KCl mmol (þ)
kg1 g
kg1 mg
kg1
6.07 5.20 27.0 5.5 21.7 65.0 32.5 0.02
KCl in a dose of 1.16 g K per pot. These fertilizers were
applied in water solutions. The soil amendments, fertilizers
and HgSO4 solutions were thoroughly mixed with soil
before sowing the plants. A. sativa L. cv. Borowiak was
sown in amounts of 24 grains per pot. During the plant
growing period, the soil moisture in the pots was main-
tained at the level of 60% field water capacity. After 45 days
of growing the A. sativa L. plants, the leaf greenness index
was measured. After 90 days, the plants were harvested and
three plant organs were separated: grain, straw and roots.
Having determined the yields, the plant material was dried
and submitted to chemical analyses.
Characteristics of the soil
The soil material used in the experiment originated from the
arable humic horizon Ap of a cultivated field. According to
Natural Resources Conservation Service Soils of USDA, the
soil was classified as fine loamy sand with the grain-size distri-
bution: 75.1% of sand (0.063–0.2 mm), 24.3% of silt (63–2
mm) and 0.4% of clay (<2 mm). Particle size distribution was
measured in distilled water on a Mastersizer 3000 (Malvern
Instruments Limited) equipped with a Hydro EV module.
Prior to the experiment, the soil underwent determina-
tions of physicochemical and chemical characteristics (Table
1). Based on the results, it was concluded that the soil was
of acid reaction (pHKCl 5.20), low in organic matter (0.94%),
rich in available phosphorus (21.7 mg P
kg1), available
potassium (65.0 mg K
kg1) and magnesium (32.5 mg
Mg
kg1). The hydrolytic acidity was 27.0 mmol (þ)
kg1.
The content of mercury in the analyzed soil was very low,
never exceeding the values generally viewed as representing
the geochemical background of soils (Table 1).
Characteristics of the soil amendments
Bentonite, natural zeolite and lime were used to inactivate
mercury incorporated into soil. The sorbent applied in the
experiment, in the form of bentonite, belongs to the group
of clay materials, which are divided into several subgroups
with different chemical composition and crystal structure.
Such materials are mainly composed of minerals that repre-
sent smectites (primarily montmorillonite), accompanied by
pyroclastic residues. All smectite-rich rocks share the follow-
ing characteristics: they are dispersible in water, are excellent
sorbents, swell in the presence of water and form thixotropic
suspensions which resist sedimentation for a long time.
These properties determine the technological usability of
bentonites. The poorest quality excavated smectite-rich rocks
are used for manufacture of organic fertilizers. They can be
applied to any type of soil and used for restoration of areas
degraded by industrial activities.[43,48] In the current study,

ground bentonite was applied to soil. It was characterized by
a high content of calcium and sodium. The content of mag-
nesium was twice as high as the level of potassium and five-
fold lower than the concentration of calcium (Table 2).
Natural zeolite type MHZ (clinoptylolite) originated from
the mined zeolitic deposits in the Zemplen Hills, Hungary.
The zeolite used in our experiment was very pure clinoptyo-
lite, which is successfully used in many branches of industry,
in agriculture and in environmental protection. Its sorption
and ion-exchange capabilities are taken advantage of in
purification of gases and liquids, oxygen enrichment of air,
inactivation of radioactive wastewater, water treatment for
drinking and technical purposes, including wastewater treat-
ment. The zeolite used in the current study had a low con-
tent of phosphorus and magnesium (<1 g
kg1), high
content of calcium and sodium (>15 g
kg1) and a very
high content of potassium (>23 g
kg1). Both bentonite and
zeolite contained trace amounts of mercury (Table 2).
Lime used in the experiment in order to elevate the soil
pH and consequently to decrease the phytoavailability of
mercury by the test plant was applied as an oxide, which
acts more rapidly than a carbonate. It had a very high con-
tent of calcium and a high content of magnesium (2.3
g
kg1) relative to the content of potassium, phosphorus
and sodium, whose concentrations were <1 g
kg1 of the
applied lime (Table 2).
Chemical analysis
The chemical analyses of soil and plant material samples as
well as the materials applied in order to inactivate the toxic
effect of mercury were carried out in a laboratory of the
Department of Environmental Chemistry, at the University
of Warmia and Mazury in Olsztyn, and in the Laboratory of
the Water and Food Chemistry owned by the company
ALcontrol Laboratories Ltd., seated in Rotherham (UK).
Prior to the experiment, the basic chemical composition
and physicochemical properties of the soil were determined.
To this end, soil samples were taken, air-dried and passed
through a 2 mm mesh sieve in order to remove large debris,
such as sticks or pebbles. The following were determined in
the soil material thus prepared:
1. pH in water and in 1 mol KCl
L1 water solution with
the potentiometric method, using a WTW pH-meter
and a silver chloride electrode, according to PN-
ISO-10390;
2. Hydrolytic acidity (Hh) with the Kappen method
according to PN-R-04027;
3. Organic carbon content (Corg) with the oxygen-reducing
method in a mixture of potassium dichromate(VI) and
concentrated sulfuric (VI) acid;[49]
4. Content of available phosphorus (P) and potassium (K)
according to the standard Egner–Riehm method (DL)
in calcium lactate solution;
5. Content of available magnesium (Mg) according to the
Schachtschabel method, with an atomic absorption
spectrophotometer AA240FS;
JOURNAL OF ENVIRONMENTAL SCIENCE AND HEALTH, PART A 3
Table 2. Content of macroelements and mercury in inactivating substances in
g
kg1 DM.
Element
Type of soil
amendment P K Mg Ca Na Hg (g
kg1)
Bentonite 0.47 2.43 5.03 26.72 12.11 0.04
Zeolite 0.11 23.21 0.32 15.28 16.12 0.04
Lime (CaO) 0.16 0.67 2.32 421.16 0.13 –
6. Content of Hg in the soil samples collected prior to the
experiment and after the crop harvest, using the tech-
nique of generating cold vapor in an atomic absorption
spectrophotometer (CV-AAS).
During the plant growing season, the leaf greenness index
SPAD of A. sativa L. plants was determined. The relative
content of chlorophyll in leaves of A. sativa L. was measured
with a chlorophyll-meter SPAD-502 Plus manufactured by
Konica Minolta. Differences in the absorption of light by a
leaf at wavelengths of 650 nm and 940 nm were measured.
Light absorption at 650 nm is associated with chlorophyll
while light absorption at 940 nm is mainly due to the pres-
ence of structural elements in a leaf (light is retained by the
leaf tissue). The quotient of light absorption at both wave-
lengths is expressed in dimensionless quantities known as
SPAD values or readings. The apparatus does not measure
directly the chlorophyll content in leaves but rather identi-
fies the ratio of leaf’s greenness, which is closely connected
to the plant’s nutritional status.[50]
After harvest, the yield of grain, straw and roots from
each pot was determined. The collected plant material
was dried to constant mass at 60  C for determination of dry
matter, after which it was ground and stored in plastic con-
tainers. The following were determined in all the plant parts:
1. Total nitrogen (Ntot) by the thermal conductivity method
on a nitrogen analyzer LECO Corporation FP-428;
2. After wet mineralization in concentrated nitric acid
using microwave accelerated reaction system MARS-5
(CEM Corporation), the content of potassium (K), cal-
cium (Ca), magnesium (Mg) and sodium (Na) was
determined by the ASA method using an atomic
absorption spectrometer AAnalyst 700 (Perkin Elmer
Instruments). The software program WinLab 32 version
6.5.0.0266 was applied;
3. The content of phosphorus (P) using the colorimetric
vanadate-molybdate method;
4. Hg in the plants using the technology of generation of cold
vapor in an atomic absorption spectrometer (CV-AAS).
5. Samples for Hg spectrometric analyses (soil and plant
tissue) were dry mineralized at a temperature of 500  C,
after which they were dissolved in concentrated nitric
acid and filtered. In order to eliminate unwanted events
caused by the presence of components which interfere
with analytical processes, 0.2% caesium chloride was
added, as it reduces ionization of atoms in an analyte
(eliminates ionization events). The spectrophotometer
was set to make triplicate measurements, after which an
averaged result was achieved. The calibration of the
4 W. SA˛DEJ ET AL.
Table 3. SPAD – leaf greenness index in the vegetation period Avena sativa L.
Soil contamination with
mercury in mg Hg
kg1of soil Without soil amendment
0 55.3
50
100
150
Mean
LSD0.05
LSD (least significant difference); n.s.: no significant.
spectrophotometer was monitored by analyzing 100
ppm (106) of the standard every 12 measurements. If
the result was different by ±5%, the instrument was
recalibrated.
Calculation methods and statistical analysis
The analytical results served to calculate the tolerance index
(TI), which reflects the phytotoxic Hg content in soil, trans-
location factor (TF) and bioaccumulation coefficient (BAC)
of mercury in organs of A. sativa L.[51] Values of these indi-
ces were calculated from the following formulas:
weight of the yield obtained in Hg contaminated objects
TI ¼
weight of the yield obtained from the control object ðwithout mercuryÞ
content of Hg in tissues of aerial organs of plants, mg kg1
TF ¼
content of Hg in tissues of plant roots, mg kg1
content of Hg in aerial organs of plants, mg kg1
BAC ¼
content of Hg in soil, mg kg1
The results of the chemical analyses were interpreted
through a two-factorial analysis of regression and variance
(ANOVA), tests of the significance of differences between
mean values (LSD) and the Duncan’s test at the level of sig-
nificance a ¼ 0.05, using the calculation module in Statistica
v. 10.0 as a tool. For selected properties, the Pearson’s sim-
ple correlation factors (R2) were calculated with the aid of
MS Excel 2010 software. Statistical significance of correlation
coefficients with n  2 degrees of freedom was assessed
according to the tables of critical values at levels of signifi-
cance a ¼ 0.05 and a ¼ 0.01, at which a correlation is sig-
nificant or highly significant.
Results and discussion
Leaf greenness index (SPAD) during the growing season
of A. sativa L
The relative content of chlorophyll measured by the leaf
greenness index (SPAD) during the growing season of
Type of soil amendment
Zeolite Lime (CaO) Bentonite
53.8 54.9 51.7
56.4 53.0 52.9 50.5
54.4 52.3 51.9 49.1
52.2 51.2 51.4 49.0
54.6 52.6 52.8 50.1
Soil contamination with mercury 1.32
Soil amendment 0.82
Interaction n.s.
A. sativa L. ranged from 49.0 to 56.4 (Table 3). Both Hg
contamination and addition of a mercury inactivating sub-
stance had a negative influence of the leaf greenness index
values. Significantly lower SPAD values were recorded at the
highest level of soil Hg contamination. Depending on the
applied soil amendment, a decrease in the SPAD values rela-
tive to the control object was as follows: series without soil
amendments – 7%, series with lime – 6%, and series with
zeolite or bentonite – 5%. These results show that the sub-
stances added to soil in order to neutralize Hg only slightly
halted the decrease in the leaf greenness index induced by
mercury. A negative effect of Hg on accumulation of plant
(1)
pigments was also demonstrated by Manikandan et al.[52] in
a study on Mentha arvensis L. as the test plant, and by
(2) Zhou et al.,[53] who tested the phytotoxicity of Hg on
Medicago sativa L. The quoted researchers ascribe the harm-
ful effect of Hg compounds on terrestrial plants to a lowered
(3) content of potassium in plant roots, inter alia, which has a
negative impact on the integrity of the cell membranes. This
in turn impairs the efficiency of water uptake, photosyn-
thesis as well as transpiration and synthesis of chloro-
phyll.[54] Similar conclusions were drawn by Azevedo and
Rodriguez,[55] who claimed that exposure of plants to inor-
ganic and organic mercury compounds may have a negative
effect not only on the course of photosynthesis, transpiration
and water uptake or chlorophyll synthesis, but also on the
uptake of such nutrients as P, Mg and Mn, which participate
in the course of these processes.
Yields of grain, straw and roots of A. sativa L
The research has shown that A. sativa L. is not very tolerant
to soil contamination with Hg. This is evidenced by
decreased yields of all three plant organs, which were pro-
gressively lower as the degree of soil contamination with
this element increased (Table 4, Figure 1). The increasing
soil contamination with mercury depressed the yield of each
of the three organs of A. sativa L., although the changes
were more distinct in yields of straw and roots than in
 JOURNAL OF ENVIRONMENTAL SCIENCE AND HEALTH, PART A 5

Table 4. Effects of soil contamination with mercury on yield of grains, straw and roots of Avena sativa L., DM g
pot1.
Type of soil amendment
Without soil amendment Zeolite Lime (CaO) Bentonite
Soil contamination with
mercury in mg Hg kg1 of soil Grain Straw Roots Grain Straw Roots Grain Straw Roots Grain Straw Roots
0 10.02 23.05 4.37 10.69 22.53 4.84 11.13 25.58 4.29 9.54 21.66 4.47
50 8.96 17.14 4.28 10.65 20.60 4.30 11.32 22.02 3.91 9.72 19.06 4.34
100 8.99 17.03 3.65 9.22 19.36 3.86 9.25 19.96 3.81 10.62 17.08 3.87
150 8.80 16.67 3.60 8.41 17.37 3.83 8.56 18.19 3.77 10.06 16.15 3.59
Mean 9.19 18.47 3.97 9.74 19.96 4.21 10.06 21.44 3.94 9.98 18.49 4.07
LSD0.05 Grain Straw Roots
Soil contamination with mercury 0.63 1.06 0.17
Soil amendment 0.63 1.06 0.17
Interaction 1.27 n.s. n.s.

Figure 1. Regression lines for yield of grains, straw and roots of Avena sativa L. depending on soil contamination with mercury.

yields of grain, which is confirmed by high values of the Table 5. Correlation coefficients (r) between mercury dose and yield and
correlation coefficients (Table 5). macronutrient content in individual Avena sativa L. organs.
In the series without soil amendments, Hg contamination Type of
organ Yield Hg N P K Ca Mg Na
decreased the grain yield produced by A. sativa L. by
Grain 
0.60 0.89 0.79 
0.20 0.59 
0.84 
0.62 
0.35
10.3–12.2% relative to the control treatment. The application Straw 
0.82 0.94 0.61 
0.70 0.25 
0.80 
0.89 
0.18
of zeolite did not prevent the negative effect of Hg on Roots 
0.88 0.93 0.72 
0.69 
0.02 
0.55 
0.55 
0.05

grain yield. However, at the lowest Hg contamination dose, Correlation coefficients (r) significant for P < 0.05.
Correlation coefficients (r) significant for P < 0.01.
the grain yield decrease was not significant. It was not until
the soil was polluted with mercury in doses of 100 and 150
mg Hg
kg1that the grain yield decreased significantly, by L. grain yield was over 23% compared to the yield produced
14% and 21%, respectively relative to the control treatment in the control treatment (Table 4).
(Table 4). It is worth noticing that although zeolite did Bentonite was the only soil amendment that prevented a
not prevent the grain yield decrease due to soil decrease in A. sativa L. grain yield caused by Hg soil
contamination with mercury, the average yield harvested contamination. The application of bentonite raised the grain
from this series was higher than from the series with no yield of A. sativa L. grown in Hg contaminated soil from
soil amendments. 1.9% to 11.3% compared to the control treatment (Table 4).
A similar effect was observed when lime was applied to Effects of the soil contamination with Hg were more evi-
soil in order to neutralize soil contamination with Hg. At dent in terms of the volume of straw biomass yield pro-
the highest soil contamination degree, a decrease in A. sativa duced by A. sativa L. In all the series, straw yield decreased
6 W. SA˛DEJ ET AL.

as the degree of Hg soil contamination increased. In the ser-

ies without soil amendments, even the lowest Hg dose con-
tributed to a significant decrease in the yield of straw
produced by A. sativa L., which was 26% lower than in the
control treatment (Table 4). Changes in straw yields that
were observed in the pots where soil was polluted with
higher mercury doses were not much bigger.
In the series with zeolite, a decrease in the A. sativa L.
straw biomass yield caused by soil contamination with Hg
was lower than in the control treatment. The highest
decrease in the straw biomass yield, by 6.1% and 14.7%,
respectively, occurred in the treatments where soil contam-
ination with Hg was higher (100 and 150 mg Hg
kg1of
soil) compared to the series where the lowest dose of Hg
(50 mg Hg
kg1of soil) was added to soil. When comparing
the yields obtained from individual treatments contaminated
with Hg, it can be concluded that zeolite had a positive
influence on A. sativa L. straw yield, as it was from 4% to
20% higher than the yield from analogous treatments with-
out soil amendments.
Lime added to soil had a positive effect on A. sativa L.
straw biomass yields. This dependence was observed in all
treatments of this series, and an average yield increase was
16.1% relative to the mean value calculated for treatments
without substances added to soil in order to inactivate the
toxic effect of Hg. Soil liming, however, did not prevent a Figure 2. Values of tolerance index (TI).
decrease in the volume of A. sativa L. straw biomass yield in
treatments with Hg polluted soil, and the said yield was growth or their complete death, while the value TI > 1
from 13.9% to 28.9% lower than in the control. shows a positive effect of a given pollutant on the growth
Of all the tested soil amendments neutralizing the toxic and development of plants. This parameter is thought to be
impact of Hg on the test plant, the least beneficial effect on the most reliable measure of the phytotoxic content of heavy
straw biomass yield was produced by bentonite. As the metals in soils.[56] In most objects, the TI value fell below
degree of Hg soil contamination rose, the A. sativa L. straw one even at the smallest Hg dose (Figure 2). This proves
yield decreased steadily. In the treatment contaminated with that A. sativa L. growth is limited under an elevated Hg
the highest mercury dose, i.e., 150 mg Hg
kg1of soil, straw content in soil. The grain yield produced by A. sativa A. sat-
yield decreased by 25%. Some reduction in the straw yield iva L. in objects where Hg contamination was neutralized
decline effected by bentonite was only observed in the treat- with bentonite was an exception. In this case, the TI values
ment polluted with the highest Hg dose. oscillated within 1.02–1.11.
The increasing soil contamination with Hg also resulted The phytotoxic influence of Hg on yields of various plant
in a significant decrease in the volume of A. sativa L. root species is confirmed by research results reported by other
biomass. This dependence appeared in both the series with- authors. Ansari et al.[57] demonstrated that even the smallest
out soil amendments and in the series where zeolite, lime or amount of Hg (5 mM
L1) in a hydroponic experiment
bentonite were applied to neutralize mercury. In each series caused a considerable decrease in the biomass yield pro-
of the experiment, the highest decrease in root biomass duced by Brassica juncea L., which manifested itself by both
occurred when Hg was added to soil in the dose of 150 mg shorter roots and shoots and a smaller leaf surface. Higher
Hg
kg1of soil, and it ranged from 12.1% in the series with doses of Hg (concentrations of solutions in the order of 25
lime to 20.9% in the series where zeolite was added to soil and 50 mM
L1) contributed to a decrease in the yield of
for neutralization of the toxic effect of Hg. It is worth men- dry matter produced by B. juncea L. by 25% and 37%,
tioning that in the series with zeolite, in which the highest respectively.
Hg dose caused the highest decrease in the volume of A. sat- Substantial decline in plant yields due to soil contamin-
iva L. root biomass, the average root yield was significantly ation with Hg has been also observed by Ciecko et al.[46]
higher than the root biomass yield obtained in the parallel 
and Rellan-Alvarez, [58]
who reported that the yield of Z.
treatments of the other experimental series. mays L. decreased by 25% and 50%, respectively, relative to
The value of tolerance index (TI) for A. sativa L. was the control. Similar results for the same crop were obtained
considered in three categories: TI ¼ 1, TI < 1, TI > 1. If by Mathe-Gaspar et al.[59] The negative effect of different
the value of TI ¼ 1, it proves that the increased amount of forms of Hg on the emergence and number of seedlings of
a pollutant in the soil has no effect on the yields of a given spring wheat (Triticum aestivum) was shown by Popa
crop. The value TI < 1 indicates the inhibition of the plants’ et al.[60] A drastic decrease in the number of seedlings was
 JOURNAL OF ENVIRONMENTAL SCIENCE AND HEALTH, PART A 7

observed by these authors when Hg was applied to soil as

mercury chloride (II).

Content of Hg in grain, straw and roots of A. sativa L

The volume of yields produced by plants is an important
indicator in an evaluation of the influence of soil amend-
ments neutralizing Hg in soil. However, when soil is pol-
luted with Hg, it is the content of this trace metal in the
plants which is the most faithful reflection of the positive
effect produced by inactivating substances. Numerous
authors report that a higher degree of soil contamination
with Hg tends to contribute to an increase in the Hg con-
tent in the plants which grow in that soil.[40,44,61] Such a
relationship has been observed in our study on A. sativa L.
(Figure 3). The highest Hg content was detected in roots,
followed by straw, while the grain of plants had the smallest
concentration of mercury. When soil was enriched with Hg
inactivating substances, the content of this element
decreased in all the plant organs. Statistical analysis revealed
the presence of a highly significant positive correlation
between the increasing soil contamination with Hg and the
mercury content of the analyzed A. sativa L. organs (Table
5). In the series without the soil amendments, the highest
Hg dose in soil raised the content of mercury in A. sativa L.
grain over ten-fold compared to the control (Figure 3). Soil
enrichment with zeolite resulted in a decreased Hg content
in A. sativa L. grain, by an average of over 3% relative to
Figure 3. Concentration of mercury (Hg) in Avena sativa L., mg Hg
kg1 DM.
the analogous treatments in the series without Hg inactivat-
ing additives.
Although a decrease in the content of mercury in A. sat-
iva L. grain was noted after the application of each of the The content of Hg in straw was higher than in grain of
three soil amendments, their effect was not proven A. sativa L. This is a desirable development because straw is
statistically. used for animal rather than for human nutrition, and Hg
Lime as a soil amendment, compared with zeolite and undergoes biomagnification in the food chain. The lowest
bentonite, most strongly decreased the content of Hg in A. Hg dose increased the content of this element in straw by
sativa L. grain. This finding confirms the commonly held three-fold, while the subsequently higher doses raised it by
belief that soil pH largely determines the availability of four- and five-fold, respectively.
heavy metals to plants. When the soil pH is decreased to The applied soil amendments contributed to a decrease
slightly acid or acid, the concentration of these elements in in the Hg content in A. sativa L. straw. However, same as in
the soil solution increases, and consequently, their phytoa- A. sativa L. grain, the effect of the tested substances on mer-
vailability improves.[62] Although soil liming tested in our cury accumulation in A. sativa L. straw could not be con-
research considerably depressed the grain content of Hg, the firmed statistically.
content of mercury was still highly elevated due to the The application of zeolite contributed to a decrease in the
increasing soil contamination with this trace metal. Contrary Hg content of A. sativa L. straw by 5–13% in comparison
results were obtained by Yang et al.[63] These researchers with the parallel treatments of the series without soil
analyzed three soils with similar properties, but different in amendments. However, zeolite did not inhibit the elevation
pH values (4.82, 6.20 and 7.11). They concluded that the of the Hg content in straw caused by the increasingly severe
highest Hg amounts were released from soil with the high- contamination of soil with this element.
est pH. Lime as a substance inactivating Hg made a larger contri-
Bentonite decreased the content of Hg in A. sativa L. bution to the decrease in the content of this trace metal in
grain slightly more than zeolite but less strongly than lime. A. sativa L. straw. In the treatment polluted with the small-
Compared to the control series, this type of substance est dose of Hg, the content of this element in straw was
applied to inactivate the toxic influence of Hg contributed nearly five-fold higher versus the control, whereas in the
to a decrease of the Hg content in A. sativa L. grain by treatment with the highest Hg soil contamination it was
5.4% in the treatment with 150 mg Hg
kg1of soil up to over seven-fold higher compared to its content of straw har-
over 7% in the other treatments. vested from the control treatment.
8 W. SA˛DEJ ET AL.

Bentonite added to soil also had a limiting effect on the

content of Hg in A. sativa L. straw. The influence of this
substance on reducing the content of Hg in A. sativa L.
straw was weaker than that of lime, but stronger than pro-
duced by zeolite. The highest content of Hg in the analyzed
organs of A. sativa L. was noted in roots, which supports
the results achieved by other authors, who claim that cell
walls of particular root tissues create a barrier that limits the
migration of trace elements to aerial parts of
plants.[41,42,64,65] This is the reason why most plant species
tend to accumulate Hg in roots, although some plants will
gather this element mostly in stalks via translocation or dir-
ect absorption of its gaseous form.[66]
Results reported by Ansari et al.[57] and Patra and
Sharma[8] also point to uneven distribution of Hg in
plant organs. Their experiments showed that roots had a
higher content of this element than aerial biomass, and
disproportions between roots and aerial organs grew
larger as the soil Hg contamination degree increased.
Similar relationships were reported by Moreno et al.[67]
and Su et al.[68]
The uptake of mercury by A. sativa L. was estimated
according to the translocation factor (TF) (Figure 4) and
bioaccumulation coefficient (BAC) (Figure 5). Nagajyoti
et al.[69] emphasize that under field conditions the values of
these indices are most optimal when a mercury concentra- Figure 4. Values of translocation factor (TF).
tion in soil is not too high. In our study, the values of both
indices were highly varied. Much higher values of TF and
BAC were observed for straw than for grain of A. sativa L.
With regard to grain, soil contamination with Hg caused an
increase in the value of TF, but a reverse relationship was
noted for A. sativa L. straw (Figure 4). Values of BAC were
clearly dependent on the amount of Hg introduced to soil.
Regardless of a plant organ, much higher values of this indi-
cator were observed after the application of higher Hg doses
than lower ones (Figure 5).
The results of a study by Szab o and Fodor,[70] where Z.
mays L. was tested, show that this plant absorbed small
quantities of Hg. The content of Hg in Z. mays L. stems
from treatments with the highest soil contamination with
Hg was as low as 0.6 mg Hg
kg1DM. The above research
also proved that Hg was not translocated to leaves and grain
of Z. mays L. Similar results were obtained by these authors
in experiments on T. aestivum L.
The current research showed that bentonite and zeolite
were characterized by similar abilities to limit the uptake
of Hg by A. sativa L. The positive influence of these sub-
stances in terms of reducing the toxic impact of Hg on
plants is the confirmation of the results reported by
Ciecko et al.[46] These researchers stated that the applied
neutralizing substances significantly depressed the accumu-
lation of Hg in the aerial and root mass of Z. mays L., Figure 5. Values of bioaccumulation coefficient (BAC).
with bentonite producing a stronger effect. Rodriguez
et al.[71] suggested that the uptake of Hg by plants could
be limited if soil was enriched with perlite which was pro- results were presented by Bednarek et al.,[72] who con-
duced from aluminosilicates. At the same time, our results cluded that in soils with slightly acid or neutral reaction,
show that lime introduced to soil exerted a positive effect i.e., not conducive to the uptake of heavy metals by plants,
on A. sativa L. by reducing its uptake of mercury. Similar the accumulation of Hg in T. aestivum L. was very low.
 JOURNAL OF ENVIRONMENTAL SCIENCE AND HEALTH, PART A 9

Figure 6. Concentration of total nitrogen and potassium in Avena sativa L. depending on soil contamination by mercury and applied soil amendments.
10 W. SA˛DEJ ET AL.

Figure 7. Concentration of phosphorus and calcium in Avena sativa L. depending on soil contamination by mercury and applied soil amendments.
 JOURNAL OF ENVIRONMENTAL SCIENCE AND HEALTH, PART A 11

Figure 8. Concentration of magnesium and sodium in Avena sativa L. depending on soil contamination by mercury and applied soil amendments.
12 W. SA˛DEJ ET AL.
Content of macronutrients in grain, straw and roots of
A. sativa L
Soil contamination with mercury may affect the content of
macro- and micronutrients in plants, which to a large extent
is essential for the quality traits of yields, their technological
value and suitability as food and feeds.
The statistical analysis of our results showed a highly sig-
nificant positive correlation between the increasing soil con-
tamination with Hg and the content of Ntot in grain, straw
and root mass of A. sativa L. (Figure 6). The highest average
N values were noted in grains, where they were twice as high
as the average Ntot in straw and roots. The increasing soil Hg
contamination tended to raise the content of Ntot in organs
of A. sativa L., more strongly in grain and straw than in
roots. Contrary results were achieved by Sahu et al.,[73] who
studied the phytotoxic effect of increasing Hg doses on T.
aestivum L. and the role of this pollutant in the induction of
oxidative stress, concluding that the total content of protein
in roots and leaves of this plant depended on the concentra-
tion of Hg. At a low concentration, i.e., 2.5 lM
L1, the con-
tent of protein in the analyzed organs rose by 10% in roots
and by 16% in leaves compared to the control treatment. The
increasing mercury concentration caused a decrease in the
total protein content in the analyzed organs, and its highest
decline was recorded at the concentration of 25 lM
L1
HgCl2 (less by 19% in leaves and by 24% in roots).
The substances applied in our experiment to inactivate
mercury differentiated the content of Ntot in all analyzed
organs of A. sativa L. In most treatments, these substances
contributed to a slight increase in the content of this elem-
ent in grain, straw and roots of the plants. However, a statis-
tically confirmed increase in the total nitrogen content
under the influence of the mercury inactivating soil amend-
ments was noted only in straw. A study carried out by
Ciecko et al.[46] proved that zeolite led to an increase in Ntot
in aerial organs of Z. mays L., while bentonite caused a
reduction of the content of this nutrient.
The content of K against the background of the increas-
ing soil Hg contamination depended on which A. sativa L.
organ was considered. A significant positive correlation
between the analyzed factors was verified only for grain
(Figure 6). Bentonite decreased the content of K in grain,
but only in the pots treated with the highest Hg dose, com-
pared to the analogous treatments in the series without ben-
tonite. The impact of the other substances inactivating the
phytotoxic effect of Hg on K in A. sativa L. grain was not
so unequivocal. Similar dependences were detected in the
case of roots, On the other hand, Hg was found to have a
stimulating effect on the accumulation of K in straw. The K
content increased as the soil contamination with Hg grew
more severe, reaching the highest values in treatments which
had received 100 mg Hg
kg1of soil.
The content of P in the analyzed organs of A. sativa L.
did not vary much (Figure 7). A negative correlation was
determined between the growing soil contamination with
mercury and the content of P in straw and roots of A. sativa
L. (Table 5). The amendment of soil with the Hg inactivat-
ing substances slightly decreased the P content of grain and
straw, but had no significant effect on the content of this
element in roots of A. sativa L.
The growing soil contamination with Hg in most series
contributed to a decrease in the Ca content in the analyzed
organs of the test part (Figure 7). The applied soil additives
inactivating Hg did not affect significantly the increase in
the calcium content in individual A. sativa L. organs. Zeolite
was an exception in that its addition to the treatments with
the doses of Hg equal 50 and 100 mg Hg
kg1of soil caused
a significant increase in the Ca content in roots.
There was a distinct decrease in the Mg content in all
series of the experiment and in all analyzed organs of A. sat-
iva L. due to the soil contamination with Hg (Figure 8). Out
of the three substances added to soil to inactivate the pollu-
tant, lime is worth attention as it contributed to an increase
in the content of Mg in grain (from 2.5% to 8.2%). There
was no unequivocal and significant effect of the increasing
soil contamination with Hg or the applied soil amendments
on the content of Na in organs of A. sativa L.
There are few reports concerning the effect of Hg on the
accumulation of essential nutrients in plants. Patra and
Sharma,[74] while analyzing the toxicity mechanism of mer-
cury, draw attention to its affinity with phosphate groups
and active ADP and ATP groups, and to the replacement of
basic cations by Hg cations. In turn, Radecka and
Wesołowski[54] conclude that the harmful effect of Hg com-
pounds on terrestrial plants includes a decrease in the K con-
tent in roots, which causes negative changes in the integrity
of the cell membrane. What follows are changes in the effi-
ciency of water uptake, transpiration process and photosyn-
thesis and synthesis of chlorophyll. This assumption is
supported by Boening,[1] who also suggested that plants
exposed to the presence of Hg in soil had depressed levels of
K, Mg and Mn, while their content of Fe increased. These
changes are a consequence of some damage to the root sys-
tem cell membranes, which leads to disorders in the uptake
and translocation of nutrients to the aerial parts of plants. In
a study by Sahu et al.,[73] the content of K, Ca and Mg in
roots and leaves of T. aestivum L. was strongly dependent on
the concentration of Hg in the substrate. An increase in the
concentration to 2.5 and 5 lM
L1 HgCl2 caused a decrease
in the K content in leaves relative to the control plants by
about 17% and 23%, respectively. Any further increase in the
concentration of the solution caused subsequent decrease in
the K content by 38% and 49%, compared to the treatments
with the lower Hg doses. The content of Ca and Mg in plants
treated with a small Hg dose (2.5 lM
L1) was only slightly
depressed compared with the control treatment (by 11%),
whereas the relationships observed at the higher Hg doses
resembled the ones noted for the content of K. Depressed lev-
els of K, Ca and Mg in other plant species (Rumex induratus,
Marrubium vulgare) due to Hg soil contamination have been
verified by Moreno-Jimenez et al.[10]
Conclusions
It has been confirmed that A. sativa L. is not tolerant to soil
contamination with Hg. As the degree of soil contamination

with this element increased, the yield of aerial mass and
roots of the test plant decreased. The use of amendments to
soil (bentonite, zeolite and lime) reduced the toxicity of
mercury to plants and its bioavailability, and contributed to
the improvement of plant growth conditions, which in turn
intensified the process of phytostabilization. More beneficial
effects were obtained after using lime and bentonite than
zeolite. The addition of bentonite, lime or zeolite to Hg pol-
luted soils did not have a distinct effect on the content of
macronutrients in organs of A. sativa L. Supported phytosta-
bilization may be a viable option for decontaminating mer-
cury polluted soils.
Funding
The article discusses the results of research funded by a doctoral (PhD)
grant (No. 1004-0206) awarded by the UWM in Olsztyn.
ORCID
Wiera Sa˛dej http://orcid.org/0000-0003-1738-308X
References
[1] Boening, D. W. Ecological Effects, Transport, and Fate of
Mercury: A General Review. Chemosphere 2000, 40, 1335–1351.
DOI: 10.1016/S0045-6535(99)00283-0.
[2] Horvat, M. Mercury as a Global Pollutant. Anal. Bioanal.
Chem. 2002, 374, 981–982. DOI: 10.1007/s00216-002-1605-3.
[3] Kindbom, K.; Munthe, J. Product-Related Emissions of Mercury
to Air in the European Union. IVL Svedish Environmental
Research Institute Report 2007, 1–22.
[4] Boszke, L.; Kowalski, A.; Astel, A.; Baranski, A.; Gworek, B.;
Siepak, J. Mercury Mobility and Bioavailability in Soil from
Contaminated Area. Environ. Geol. 2008, 55, 1075–1087. DOI:
10.1007/s00254-007-1056-4.
[5] Grandjean, P.; Nielsen, J. B. Mercury. In Environmental
Toxicants – Human Exposures and Their Health Effects;
Lippmann M., Ed.; John Wiley & Sons, Inc.: Hoboken, New
Jersey, 2009; pp 811–822.
[6] Pacyna, E. G.; Pacyna, J. M.; Sundseth, K.; Munthe, J.;
Kindbom, K.; Wilson, S.; Steenhuisen, F.; Maxson, P. Global
Emission of Mercury to the Atmosphere from Anthropogenic
Sources in 2005 and Its Future Projection until 2020. Atmos.
Environ. 2010, 44, 2487–2499. DOI: 10.1016/j.atmosenv.2009.06.
009.
[7] EPA Regulatory impact analysis for the final mercury and air
toxics standards. EPA-452/R, Washington, DC, 2011; 1–510.
http://www.epa.gov/ttn/ecas/regdata/RIAs/matsriafinal.pdf.
[8] Patra, M.; Sharma, A. Mercury Toxicity in Plants. Bot. Rev.
2000, 66, 379–422. DOI: 10.1007/BF02868923.
[9] Richard, S.; Arnoux, A.; Cerdan, P.; Reynouard, C.; Horeau, V.
Hg Levels of Soils, Sediments and Fish in French Guiana, South
America. Water. Air. Soil Pollut. 2000, 124, 221–244. DOI: 10.
1023/A:1005251016314.
[10] Moreno-Jimenez, E.; Penalosa, J. M.; Esteban, E.; Carpena Ruiz,
R. O. Mercury Accumulation and Resistance to Mercury Stress
in Rumex Induratus Marrubium Vulgare Grown in Perlite. J.
Plant Nutr. Soil Sci. 2007, 170, 485–494. DOI: 10.1002/jpln.
200625238.
[11] Kim, P. R.; Han, Y. J.; Holsen, T. M.; Yi, S. M. Atmospheric
Particulate Mercury: concentrations and Size Distributions.
Atmos. Environ. 2012, 61, 94–102. DOI: 10.1016/j.atmosenv.
2012.07.014.
JOURNAL OF ENVIRONMENTAL SCIENCE AND HEALTH, PART A 13
[12] Pirrone, N.; Cinnirella, S.; Feng, X.; Finkelman, R. B.; Friedli,
H. R.; Leaner, J.; Mason, R.; Mukherjee, A. B.; Stracher, G. B.;
Streets, D. G.; Telmer, K. Global Mercury Emissions to the
Atmosphere from Anthropogenic and Natural Sources. Atmos.
Chem. Phys. 2010, 10, 5951–5964. DOI: 10.5194/acp-10-5951-
2010.
[13] Galbreath, K. C.; Zygarlicke, C. J. Mercury Transformations in
Coal Combustion Flue Gas. Fuel Process. Technol. 2000, 65,
289–310. DOI: 10.1016/S0378-3820(99)00102-2.
[14] Galbreath, K. C.; Zygarlicke, C. J.; Olson, E. S.; Pavlish, J. H.;
Toman, D. L. Evaluation of Mercury Transformation
Mechanisms in a Laboratory-Scale Combustion System. Sci.
Total Environ. 2000, 261, 149–155. DOI: 10.1016/S0048-
9697(00)00637-9.
[15] Gray, J. E.; Theodorakos, P. M.; Fey, D. L.; Krabbenhoft, D. P.
Mercury Concentrations and Distribution in Soil, Water, Mine
Waste Leachates, and Air in and around Mercury Mines in the
Big Bend Region, Texas, USA. Environ. Geochem. Health 2015,
37, 35–48. DOI: 10.1007/s10653-014-9628-1.
[16] Sari, M. M.; Inoue, T.; Matsumoto, Y.; Yokota, K.; Isrun, I.
Assessing a Mercury Affected Area from Small-Scale Gold
Mining in Poboya, Central Sulawesi, Indonesia. EER. 2016, 4,
223–230. DOI: 10.13189/eer.2016.040406.
[17] Kostova, I. J.; Hower, J. C.; Mastalerz, M.; Vassilev, S. V.
Mercury Capture by Selected Bulgarian Fly Ashes: influence of
Coal Rank and Fly Ash Carbon Pore Structure on Capture
Efficiency. Appl. Geochem. 2011, 26, 18–27. DOI: 10.1016/j.
apgeochem.2010.10.009.
[18] Jaworska, H.; Da˛browska-NaskreR t, H.; Roz_ a nski, S. Total
Content of Mercury in Arable Soils in the Vicinity of Lafarge-
Cement Poland SA Plant (“Kujawy” Bielawy). Ecol. Chem. Eng.
A 2009, 16, 1299–1304.
[19] Zheng, Y.; Jensen, D.; Windelin, C.; Jensen, F. Review of
Technologies for Mercury Removal from Flue Gas from
Cement Production Processes. Prog. Energy Combust. Sci. 2012,
38, 599–629. DOI: 10.1016/j.pecs.2012.05.001.
[20] Lei, C. L.; Duan, Y.; Zhuo, Y.; Yang, L.; Zhang, L.; Yang, X.;
Yao, Q.; Jiang, Y.; Xu, X. Mercury Transformation across
Particulate Control Devices in Six Power Plants of China: The
co-Effect of Chlorine and Ash Composition. Fuel 2007, 86,
603–610. DOI: 10.1016/j.fuel.2006.07.030.
[21] Zhang, L.; Wong, M. H. Environmental Mercury
Contamination in China: sources and Impacts. Environ. Int.
2007, 33, 108–121. DOI: 10.1016/j.envint.2006.06.022.
[22] Cheng, H.; Hu, Y. Mercury in Municipal Solid Waste in China
and Its Control: A Review. Environ. Sci. Technol. 2012, 46,
593–605. DOI: 10.1021/es2026517.
[23] Smolinska, B. Green Waste Compost as an Amendment during
Induced Phytoextraction of Mercury-Contaminated Soil.
Environ. Sci. Pollut. Res. 2015, 22, 3528–3537. DOI: 10.1007/
s11356-014-3601-5.
[24] Ding, Z. H.; Tang, Q. H.; Liu, C.; Wang, W. H.; Zhuang, M.;
Lin, Y. M. Distribution and Ecological Effect of Mercury in
Laogang Landfill, Shanghai, China. J. Environ. Sci. 2007, 19,
200–204. DOI: 10.1016/S1001-0742(07)60032-1.
[25] Cao, Y.; Zhou, H.; Fan, J.; Zhao, H.; Zhou, T.; Hack, P.; Chan,
C. C.; Liou, J. C.; Pan, W. P. Mercury Emissions during
Cofiring of Sub-Bituminous Coal and Biomass (Chicken Waste,
Wood, Coffee Residue, and Tobacco Stalk) in a Laboratory
Scale Fluidized Bed Combustor. Environ. Sci. Technol. 2008, 42,
9378–9384. DOI: 10.1021/es8016107.
[26] Mukherjee, A. B.; Zevenhoven, R.; Bhattacharya, P.; Sajwan,
K. S.; Kikuchi, R. Mercury Flow via Coal and Coal Utilization
Byproducts: A Global Perspective. Resour. Conserv. Recy. 2008,
52, 571–591. DOI: 10.1016/j.resconrec.2007.09.002.
[27] Pyta, H.; Rogula-Kozłowska, W. Size Distribution of Particulate
Mercury by the Roads and in the Urban Background
Conditions – Preliminary Study. Sci. Rev. Eng. Environ. Sci.
2014, 63, 14–25.
14 W. SA˛DEJ ET AL.
[28] Tucaliuc, O. M.; Cretescu, I.; Nemtoi, G.; Breaban, I. G.;
Soreanu, G.; Iancu, O. I. Monitoring of Mercury from Air and
Urban Dust in the Industrial Area of Iasi Municipality.
Environ. Eng. Manag. J. 2014, 13, 20151–22061. DOI: 10.30638/
eemj.2014.228.
[29] Gworek, B.; Dmuchowski, W.; Gozdowski, D.; Koda, E.;
Osiecka, R.; Borzyszkowski, J. Influence of a Municipal Waste
Landfill on the Spatial Distribution of Mercury in the
Environment. PLoS One 2015, 10, e0133130–12. DOI: 10.1371/
journal.pone.0133130.
[30] Meij, R.; Vredenbregt, L. H. J.; Te Winkel, H. The Fate and
Behavior of Mercury in Coal-fired Power Plants . J. Air Waste
Manag. Assoc. 2002, 52, 912–917. DOI: 10.1080/10473289.2002.
10470833.
[31] Hławiczka, S.; Kubica, K.; Zielonka, U. Partitioning Factor of
Mercury during Coal Combustion in Low Capacity Domestic
Heating Units. Sci. Total Environ. 2003, 312, 261–265. DOI: 10.
1016/S0048-9697(03)00252-3.
[32] Pavlish, J. H.; Sondreal, E. A.; Mann, M. D.; Olson, E. S.;
Galbreath, K. C.; Laudal, D. L.; Benson, S. A. Status Review of
Mercury Control Options for Coal-Fired Power Plants. Fuel
Process. Technol. 2003, 82, 89–165. DOI: 10.1016/S0378-
3820(03)00059-6.
[33] Lee, S.; Seo, Y.; Jang, H.; Park, K.; Baek, J.; An, H.; Song, K.
Speciation and Mass Distribution of Mercury in a Bituminous
Coal-Fired Power Plant. Atmos. Environ. 2006, 40, 2215–2224.
DOI: 10.1016/j.atmosenv.2005.12.013.
[34] Gale, T.; Lani, B.; Offen, G. Mechanism Governing the Fate of
Mercury in Coal-Fired Power Systems. Fuel Process. Technol.
2008, 89, 139–151. DOI: 10.1016/j.fuproc.2007.08.004.
[35] Nguyen, Y. V.; Pessione, G. F. A Three-Year Assessment of
Mercury Mass Balance from LambtonTMs Coal Fired Boilers
Equipped with FGD and SC. Paper Presented at the EPA-DOE-
EPRI-A&WMA Power Plant Air Pollutant Control “Mega”
Symposium 2006, Aug 28–31, 2008, Baltimore, Maryland, USA,
vol. 1 pp 361–375.
[36] Wang, S. X.; Zhang, L.; Li, G. H.; Wu, Y.; Hao, J. M.; Pirrone,
N.; Sprovieri, F.; Ancora, M. P. Mercury Emission and
Speciation of Coal-Fired Power Plants in China. Atmos. Chem.
Phys. 2010, 10, 1183–1192. DOI: 10.5194/acp-10-1183-2010.
[37] Burmistrz, P.; Kogut, K. Mercury in Bituminous Coal Used in
Polish Power Plants. Arch. Min. Sci. 2016, 61, 473–488.
[38] NCEM National Centre for Emissions Management Institute of
Environmental Protection – National Research Institute, The
National Centre for Emissions Management, 2015, p 76.
[39] Moreno-Jimenez, E.; Gamarra, R.; Carpena-Ruiz, R. O.; Millan,
R.; Pe~nalosa, J. M.; Esteban, E. Mercury Bioaccumulation and
Phytotoxicity in Two Wild Plant Species of Almaden Area.
Chemosphere 2006, 63, 1969–1973. DOI: 10.1016/j.chemo-
sphere.2005.09.043.
[40] Chen, J.; Yang, Z. M. Mercury Toxicity, Molecular Response
and Tolerance in Higher Plants. Biometals 2012, 25, 847–857.
DOI: 10.1007/s10534-012-9560-8.
[41] Obrist, D. Atmospheric Mercury Pollution Due to Losses of
Terrestrial Carbon Pools? Biogeochemistry 2007, 85, 119–123.
DOI: 10.1007/s10533-007-9108-0.
[42] Dago, A.; Gonzalez, I.; Ari~ no, C.; Martınez-Coronado, A.;
Higueras, P.; Dıaz-Cruz, J. M.; Esteban, M. Evaluation of
Mercury Stress in Plants from the Almaden Mining District by
Analysis of Phytochelatins and Their Hg Complexes. Environ.
Sci. Technol. 2014, 48, 6256–6263. DOI: 10.1021/es405619y.
[43] Sarbak, Z. Application of Sorbents in the Process of Soil
Remediation. Chemia, Dydaktyka, Ekologia, Metrologia 2010,
15, 77–92.
[44] Rolka, E.; Grzybowski, Ł.; Ciecko, Z.; Szostek, R.; Rachuba, A.
Response of yellow lupine to soil contamination with mercury.
In Mercury in the Environment – Identifying Threats for Human
Health; Falkowska, L. Ed. University of Gda nsk Publisher:
Gdansk, 2013; pp 119–128.
[45] Heeraman, D. A.; Claassen, V. P.; Zasoski, R. J. Interaction of
Lime, Organic Matter and Fertilizer on Growth and Uptake of
Arsenic and Mercury by Zorro Fescue (Vulpia myuros L.).
Plant Soil 2001, 234, 215–231.
[46] Ciecko, Z.; Rolka, E.; OpeR chowska, M.; Grzybowski, Ł.
Response of Maize to Soil Contamination with Mercury. Ocean
Hydrobiol. Stud. 2007, 36, 117–126.
[47] Andrzejewska, A.; Diatta, J.; Spi_zewski, T.; Krzesi nski, W.;
Smurzy nska, A. Application of Zeolite and Bentonite for
Stabilizing Lead in a Contaminated Soil. In_z Ekolog. 2017, 18,
1–6. DOI: 10.12912/23920629/74950.
[48] Stentiford, M. J. Polished Performers - Minerals in Frits and
Glazes. Ind. Minerals 2004, 438, 54–61.
[49] Tiessen, H.; Moir, J. O. Total and organic carbon. In Soil
Sampling and Methods of Analysis Carter, M.R. Ed. Canadian
Society of Soil Science. Lewis Publishers: Boca Raton, 1993; pp
187–199.
[50] Machul, M. Use of the SPAD Test to Determine a
Supplementary Nitrogen Rate for Maize. PamieR tnik Puławski
2005, 140, 159–172.
[51] Nurzhanova, A.; Pidlisnyuk, V.; Abit, K.; Nurzhanov, C.;
Kenessov, B.; Stefanovska, T.; Erickson, L. Comparative
Assessment of Using Miscanthus  Giganteus for Remediation
of Soils Contaminated by Heavy Metals: A Case of Military and
Mining Sites. Environ. Sci. Pollut. Res. 2019, 26, 13320–13333.
DOI: 10.1007/s11356-019-04707-z.
[52] Manikandan, R.; Sahi, S. V.; Venkatachalam, P. Impact
Assessment of Mercury Accumulation and Biochemical and
Molecular Response of Mentha arvensis: A Potential
Hyperaccumulator Plant. Sci. World J. 2015, 2015, 1–10. DOI:
10.1155/2015/715217.
[53] Zhou, Z. S.; Huang, S. Q.; Guo, K.; Mehta, S. K.; Zhang, P. C.;
Yang, Z. M. Metabolic Adaptations to Mercury-Induced
Oxidative Stress in Roots of Medicago sativa L. J. Inorg.
Biochem. 2007, 101, 1–9. DOI: 10.1016/j.jinorgbio.2006.05.011.
[54] Radecka, I.; Wesołowski, M. Concentration and Distribution of
Mercury in Rhizomes and Roots of Medicinal Plants [l:] III; IOS:
Warsaw: 2005; pp 337–341.
[55] Azevedo, R.; Rodriguez, E. Phytotoxicity of Mercury in Plants.
J. Bot. 2012, 2012, 1–6. DOI: 10.1155/2012/848614.
[56] Spiak, Z.; Romanowska, M.; Radoła, J. The Content in Soils
Toxic to Different Species of Cultivated Plants. Zesz. Probl.
Post. Nauk Rol. 2000, 471, 1125–1134.
[57] Ansari, M. K. A.; Ahmad, A.; Umar, S.; Iqbal, M. Mercury-
Induced Changes in Growth Variables and Antioxidative
Enzyme Activities in Indian Mustard. J. Plant Interact 2009, 4,
131–136. DOI: 10.1080/17429140802716713.
[58] 
Rellan-Alvarez, 
R.; Ortega-Villasante, C.; Alvarez-Fern
andez, A.;
Del Campo, F. F.; Hernandez, L. E. Stress Responses of Zea
Mays to Cadmium and Mercury. Plant Soil 2006, 279, 41–50.
DOI: 10.1007/s11104-005-3900-1.
[59] Mathe-Gaspar, G.; Szili-Kovacs, T.; Takacs, T.; Mathe, P.;
Anton, A. Environmental Impact of Soil Pollution with Toxic
Elements from the Lead and Zinc Mine at Gy€ ongy€osoroszi
(Hungary). Commun. Soil Sci. Plant Anal. 2009, 40, 1–6.
[60] Popa, K.; Murariu, M.; Molnar, R.; Schlosser, G.; Cecal, A.;
Drochiiu, G. Effect of Radioactive and Non-Radioactive
Mercury on Wheat Germination and the anti-Toxic Role of
Glutathione. Isotopes Environ. Health Stud. 2007, 43, 105–116.
DOI: 10.1080/10256010701362112.
[61] Ciecko, Z.; Rolka, E.; Najmowicz, T.; Archacka, A.; Grzybowski,
Ł. Response of Potato to Soil Contamination with Mercury
Neutralised with Soil Improving Substances. Ecol. Chem. Eng. A
2009, 16, 523–530.
[62] Xu, J.; Kleja, D. B.; Biester, H.; Lagerkvist, A.; Kumpiene, J.
Influence of Particle Size Distribution, Organic Carbon, pH and
Chlorides on Washing of Mercury Contaminated Soil.
Chemosphere 2014, 109, 99–105. DOI: 10.1016/j.chemosphere.
2014.02.058.

[63] Yang, Y. K.; Zhang, C.; Shi, X. J.; Lin, T.; Wang, D. Y. Effect of
Organic Matter and pH on Mercury Release from Soils. J.
Environ. Sci. (China) 2007, 19, 1349–1354. DOI: 10.1016/s1001-
0742(07)60220-4.
[64] Dushenkov, V.; Kumar Nanda, P. B. A.; Motto, H.; Raskin, I.
Rhizofiltration: The Use of Plants to Remove Heavy Metals
from Aqueous Streams. Environ. Sci. Technol. 1995, 29,
1239–1245.
[65] Ericksen, J. A.; Gustin, M. S.; Schorran, D. E.; Johnson, D. W.;
Lindberg, S. E.; Coleman, J. S. Accumulation of Atmospheric
Mercury in Forest Foliage. Atmos. Environ. 2003, 37,
1613–1622. DOI: 10.1016/S1352-2310(03)00008-6.
[66] Suszcynsky, E. M.; Shann, J. R. Phytotoxicity and Accumulation
of Mercury in Tobacco Subjected to Different Exposure Routes.
Environ. Toxicol. Chem. 1995, 14, 61–67.
[67] Moreno, F. N.; Anderson, C. W. N.; Stewart, R. B.; Robinson,
B. H.; Ghomshei, M.; Meech, J. A. Induced Plant Uptake and
Transport of Mercury in the Presence of Sulphur-Containing
Ligands and Humic Acid. New Phytol. 2005, 166, 445–454.
DOI: 10.1111/j.1469-8137.2005.01361.x.
[68] Su, Y.; Han, F. X.; Chen, J.; Sridhar, B. B. M.; Monts, D. L.
Phytoextraction and Accumulation of Mercury in Three Plant
Species: Indian Mustard (Brassica Juncea), Beard Grass
(Polypogon monospeliensis), and Chinese Brake Fern (Pteris
JOURNAL OF ENVIRONMENTAL SCIENCE AND HEALTH, PART A 15
vittata). Int. J. Phytoremediat. 2008, 10, 547–560. DOI: 10.1080/
15226510802115091.
[69] Nagajyoti, P. C.; Lee, K. D.; Sreekanth, T. V. M. Heavy Metals,
Occurrence and Toxicity for Plants: A Review. Environ. Chem.
Lett. 2010, 8, 199–216. DOI: 10.1007/s10311-010-0297-8.
[70] Szabo, L.; Fodor, L. Uptake of Microelements by Crops Grown
on Heavy Metal – Amended Soil. Commun. Soil Sci. Plant
Anal. 2006, 37, 2679–2689. DOI: 10.1080/00103620600830070.
[71] Rodriguez, L.; Rinc on, J.; Asencio, I.; Rodriguez-Castellanos, L.
Capability of Selected Crop Plants for Shoot Mercury
Accumulation from Polluted Soils: phytoremediation
Perspectives. Int. J. Phytoremediat. 2007, 9, 1–13. DOI: 10.1080/
15226510601139359.
[72] Bednarek, W.; Tkaczyk, P.; Dresler, S. Heavy Metals Contents
as a Criterion for Assessment of Winter Wheat Grain Quality.
Acta Agrophys. 2008, 12, 315–326.
[73] Sahu, G. K.; Upadhyay, S.; Sahoo, B. B. Mercury Induced
Phytotoxicity and Oxidative Stress in Wheat (Triticum aestivum
L.) Plants. Physiol. Mol. Biol. Plants 2012, 18, 21–31. DOI: 10.
1007/s12298-011-0090-6.
[74] Patra, M.; Bhowmik, N.; Bandopadhyay, B.; Sharma, A.
Comparison of Mercury, Lead and Arsenic with respect to
Genotoxic Effects on Plant Systems and the Development of
Genetic Tolerance. Environ. Exp. Bot. 2004, 52, 199–223. DOI:
10.1016/j.envexpbot.2004.02.009.