Open Journal of Soil Science, 2012, 2, 275-281
http://dx.doi.org/10.4236/ojss.2012.23033 Published Online September 2012 (http://www.SciRP.org/journal/ojss)
275
Peculiarities of Heavy Metals Accumulation by the Plants
of Meadow Phytocenosis
Тatyana А. Trifonova1, Ekaterina Y. Alkhutova2
1Soil Science Department, Lomonosov State University, Moscow, Russia; 2Faculty of Chemistry and Ecology, Vladimir State Uni-
versity, Vladimir, Russia.
Received June 12th, 2012; revised July 15th, 2012; accepted July 28th, 2012
ABSTRACT
This work is devoted to studying of the accumulation peculiarities of heavy metals (HM) by the meadow phytocenosis
plants and also plants phytomeliotating properties at various levels of soil contamination. The system “cespitose-podsol
soil—meadow vegetation” has been chosen as a research object. Heavy metals as a kind of industrial waste—galvanic
slurry enriched by zinc amounting 79.7% of all HM detected in the slurry—was introduced into the soil. Heavy metals
content and redistribution in soil at various amount of galvanic slurry, quantitative and specific content of phytocenosis,
heavy metals accumulation in the meadow vegetation crop at various contamination layers have been studied during
research. Among the researched phytocenosis the groups of plants with high and low heavy metals accumulation capa-
city have been defined. Cirsium arvense, Capsella bursa-pastoris, Artemisia vulgarus and Rumex confertus belonged to
the group accumulating several heavy metals in considerable amounts without significant phytomass loss. The majority
of these plants possess developed phytomass and their ability to accumulate heavy metals in large amount allows using
them as phytomeliorants for soil decontamination at the final stages of reclaiming.
Keywords: Heavy Metals; Meadow Phytocenosis Plants; Phytomeliotating Properties
1. Introduction
Russia like many other countries experiences vital dra-
matic problems of soil contamination by heavy metals.
Numerous studies are devoted to the research of various
aspects of this problem: HM migration in soil [1-4], soil
property transformation under HM impact [5-7], HM
content in soil rate setting [8-12].
From the practical point of view the problem of HM
accumulation by plants and the possibility to use the
plants for polluted soil decontamination ranks special in-
terest. In case there is no necessity for urgent soil decon-
tamination, phyto-extraction can be used as a very va-
luable technology possessing lots of advantages, if com-
pared with costly physical and physical-chemical me-
thods of reclamation. However from our point of view
the questions of HM accumulation and carry-over by the
plants have not been studied adequately.
This research objective was to study the accumulation
peculiarities of zinc, copper, nickel, iron and cadmium by
the meadow phytocenosis plants and also plants phytome-
liotating properties at various levels of soil contamination.
2. Materials and Methods
The system “cespitose-podsol soil—meadow vegetation”
has been chosen as a research object. The research was
carried out in upland meadow near Vladimir city. In
summer of 2006 four square plots were laid in the mea-
dow, each plot area was 27.5 m2, the distance between
the plots was about 5 - 8 m. In autumn of 2006 HM as a
kind of industrial waste—galvanic slurry enriched by
zinc amounting 79.7% of all HM detected in the
slurry—was introduced into the plots soil. Nickel, copper
and cadmium content in the slurry amounted 0.58, 1.13
and 0.16% correspondingly. Galvanic slurry share in the
plots No. 1, No. 2, No. 3 and No. 4 amounted 0.0; 2.3;
3.5; 4.7 kg/m2 correspondingly.
The plots were characterized by cespitose-podsol
sandy-loam temporarily overdamp soil (humus 1.31%,
рНKCl 6.22, S 6.27 mMole/100g). Soil sampling and
analysis were carried out during the period of 2006-2008.
Soil was sampled at the depth of 0 - 15, 15 - 30, 30 - 45,
45 - 60 cm.
Quantitative and specific content of phytocenosis was
studied from 2006 till 2007, the research was carried out
in mid August. Crop count was executed applying cutting
method; herbage was mowed down 3 - 5 cm high. The
cut plants were selected according to species and
weighed air dry.
About 29 species of higher plants from 14 families

Peculiarities of Heavy Metals Accumulation by the Plants of Meadow Phytocenosis 276
were registered in the researched plots. With Cirsium
arvense dominating, whose share comprised from 21.39%
to 23.86% of total phytomass cenosis. Tragopogon prat-
ensis (14.60% - 16.91%) and Dactylis glomerata (15.60%
- 17.57%) were co-dominant. Rumex confertus and Ar-
temisia vulgarus (5.02% - 7.11% and 7.97% - 11.40%
correspondingly) ranked insufficient share in the total
amount of species though they had quite considerable
phytomass (Figure 1).
HM gross content in galvanic slurry, soil and plants
was determined by X-ray spectral fluorescent method
applying “Spectroscan-MAX” device. The results of the
experiment were processed using software packages
“Excel” and “Statistica”.
3. Results and Discussion
3.1. HM Content and Redistribution in Soil at
Various Amount of Galvanic Slurry
Humus horizon pollution level of initial soil and soil de-
liberately contaminated with HM was assessed basing on
anthropogenic contamination aggregated coefficient (Zс)
[10]:

total
1
n
cbg
i
Z
KK ni


,
with Ktotal—HM content in the researched soil, Kbg—
metal content in background soil, n—number of elements
with Кс > 1 (with Zс < 16, pollution level is considered
allowable, with 16 - 32—medium, with 32 - 128—high,
with Zc > 128—very high).
Galvanic slurry introduction into the experimental
plots, dosed according to the test schedule, led to the HM
accumulation in soil root layer (Figure 2). Low con-
tamination level of initial soil after introducing even mi-
nimal waste dosage has considerably increased and was
characterized as “very high”. By 2008 the contamination
level of root layer had decreased though it had been still
characterized as “very high” or “high”.
In 2008 the distribution of all researched metals re-
garding soil type had similar characteristics not depend-
ing on galvanic slurry share. Maximum HM content at-
tributed to the upper humus soil horizon and lower layers
were characterized by elements concentration de- crease.
As mentioned above by 2008 considerable decrease of
HM concentration in humus soil horizon had been ob-
served (zinc, copper, nickel and cadmium concentration
decrease comparing to 2007 comprised 62% on average
for the contaminated plots); simultaneously high ex-
pected level of the considered elements in the underlying
horizons А2, А2В and in the upper horizon layer B was
not detected. Turf-spodosol soil is characterized by the
scrubbing water mode so the enumerated metals, which
Figure 1. Test plot vegetation.
Figure 2. Anthropogenic pollution aggregated coefficient
for root layer in 2007-2008.
could not get firmly fixed in the soil substance, impover-
ished by organics and physical clay, were washed away
from the humus horizon to the 60 cm depth and during
the flood period migrated into ground water.
3.2. Heavy Metals Accumulation in the Meadow
Vegetation Crop at Various Contamination
Layers
The tested plants accumulated HM in their tissues dif-
ferently, and contamination level influenced pollutants
accumulation process greatly. In order to arrange HM in
a sequence, characterizing their significance for he plants,
we have applied biological consumption ratio (BCR)
calculated as a relation of HM content in the plants ash to
HM content in soil. BCR values, calculated for HM of
the test check variant (Zс = 10,091), were arranged in the
following sequence: Zn > Cu > Cd > Ni > Fe (Table 1).
Biologic accumulation sequences were changing ac-
cording to the soil contamination level increase: with Zс
= 188,720 and Zс = 281,293 metals arranged the follow-
ing sequence Cu > Ni > Zn > Cd > Fe, but with Zс =
377,086—the sequence was different Cu > Ni > Zn ≈ Cd
≈ Fe. Developed plants selectivity regarding copper and
nickel at the plots No. 2, No. 3 and No. 4, enriched by
these metals, might be explained by the fact that the
plants didn’t get enough amount of the mentioned above

Peculiarities of Heavy Metals Accumulation by the Plants of Meadow Phytocenosis 277
Table 1. Biological consumption ratios (BCR) of HM by
vegetation coenosis phytomass at different levels of soil
contamination.
BCR (in terms of 5% ash content)
Zс
Zn Cu Ni Fe Cd
10.091 (test) 9.094 6.289 0.422 0.073 1.000
188.72 0.912 1.467 1.133 0.126 0.865
281.293 0.945 1.261 1.027 0.159 0.843
377.086 0.780 1.104 0.817 0.178 0.783
microelements from the test plot soil for a certain period
of time.
For characterizing specific peculiarities of the plants to
accumulate HM median-propotional method was applied,
which helped to reveal the groups of plants with high,
medium or low metal accumulation capacity.
Vegetation groups in terms of zinc accumulation are
presented in Table 2. Zinc is a very important microe-
lement, though is considered slightly toxic for the plants.
Maximum Zn permissible concentration in the plants is
determined in the range of 150.0 - 300.0 mg/kg of solids
[13].
Such species as Cirsium arvense, Trifolium pratense,
Tussilago farfara, Capsella bursa-pastoris, Gnaphalium
ulignosum and Rumex confertus can be referred to the
group with high zinc accumulation capacity. However
zinc content in the plants didn’t reach the lower limit of
maximum permissible concentration even at the highest
contamination level: maximum amount of this element
was detected in No. 4 plot Capsella bursa-pastoris and
comprised 139.22 mg/kg of solids.
Low accumulation capacity was typical for Conovo-
lvulus arvensis, Vicia cracca, Tragopogon pratensis,
Chenopodium rubrum, Erigeron canadensis, Mentha
arvensis, Cerastium holosteoides и Pilosella onegensis.
The rest meadow cenosis representatives belonged to the
zinc medium accumulation capacity group.
Copper is a true bio-element, involved in various
metabolic reactions of plants [14]. Nevertheless in spite
of the common tolerance of the vegetable types to copper,
this element is still considered to be heavily toxic. Cu
maximum permissible concentration in plants is deter-
mined at the level of 15.0 - 20.0 mg/kg of dry substance
[13].
Average absolute Cu content in plants comprised 6.04,
10.59, 12.91 and 14.16 mg/kg in the test plots No. 1, No.
2, No. 3 and No. 4 correspondingly (Table 2).
High Cu accumulation capacity group included Cir-
sium arvense, Trifolium pratense, Capsella bursa-pas-
toris, Artemisia vulgarus and Rumex confertus. These
plants actively accumulated Cu both from the uncon-
taminated soil and from soil with high content of this
element. Insignificant excess of Cu maximum permissi-
ble concentration in the plants was observed only at the
following soil contamination levels Zс = 281,293 and Zс
= 377,086. Thus maximum permissible concentration
excess of test plot No. 4 was detected for such plants as
Cirsium arvense, Trifolium pratense, Capsella bursa-
pastoris and Rumex confertus (copper content in these
plants amounted 24.79, 20.17, 23.10 and 24.00 mg/kg of
dry mass correspondingly).
Tragopogon pratensis, Linaria vulgarus, Erigeron
canadensis, Cerastium holosteoides and Pilosella one-
gensis were featured by low copper accumulation in all
the researched plots.
Cadmium is not a vital element for plants functioning
it ranks among extremely toxic elements. Having equal
concentrations with other HM it produces 2 - 20 times
more serious negative impact on the living organisms
[14].
Average ultimate cadmium content in plants, grown on
the soil free from galvanic slurry, was not high and com-
prised 0.03 mg/kg of dry mass. As soil contami-nation
grew cadmium content in dry phytomass also increased
approaching its maximum value (1303 mg/kg) at Zс =
377,086.
High rate of Cd accumulation was typical for such
plants as Cirsium arvense, Trifolium pratense, Atriplex
hastata, Tussilago farfara, Capsella bursa-pastoris, Ar-
temisia vulgarus and Rumex confertus (Figure 3). Cad-
mium maximum content was registered among Cir- sium
arvense in test plot No. 4 and amounted 3.09 mg/kg of
dry mass.
Stellaria media, Erigeron canadensis, Gnaphalium uli-
gnosum and Cerastium holosteoides accumulated cad-
mium in moderate amount.
The groups of plants with high, medium and low
nickel accumulation are presented in Table 3. Despite
insufficient study of nickel functions this metal is now
classified as an essential microelement for the higher
plants due to its physiologic importance. Ni maximum
permissible concentration in plants is stated within 20.0
and 30.0 mg/kg of dry substance [13].
Polygonum persicaria, Tussilago farfara, Artemisia
vulgarus and Gnaphalium ulignosum can be referred to
the high nickel accumulation capacity group. These
plants began to accumulate Ni in amounts higher than
average starting with soil contamination level ranking Zс
= 188.720. Cirsium arvense, Conovolvulus arvensis, Vi-
cia cracca, Epilobium rubescens, Trifolium pratense,
Rumex confertus and Dactylis glomerata accumulated
nickel well from soil which was not contaminated with
galvanic slurry. However when soil contamination rate
increased the mentioned plants Ni accumulating capacity
fell and they were referred to medium or low accumula-
tion capacity group.

Peculiarities of Heavy Metals Accumulation by the Plants of Meadow Phytocenosis 278
Table 2. Zinc and copper content in meadow phytocoenosis vegetation at various contamination levels (2007).
Zn content in plants, mg/kg Cu content in plants, mg/kg
Zс Zс
Species
10.091 188.72 281.293 377.086 10.091 188.72 281.293 377.086
Artemisia vulgarus 13.79 25.02 37.81 42.80 9.27 13.23 15.02 17.62
Atriplex hastata 14.10 29.69 77.44 80.85 6.15 10.85 11.06 14.22
Capsella bursa-pastoris 20.71 75.02 112.00 139.22 7.17 18.19 20.98 23.10
Cerastium holosteoides 9.57 13.43 21.26 24.17 4.11 6.32 7.00 6.82
Chenopodium rubrum 8.22 15.16 22.99 27.27 5.55 9.01 10.36 10.90
Cirsium arvense 18.47 44.36 68.36 78.47 7.24 19.49 23.72 24.79
Conovolvulus arvensis 8.11 14.70 18.42 20.61 5.19 7.23 9.88 10.19
Dactylis glomerata 17.71 48.15 50.46 63.37 6.12 7.46 8.10 11.11
Echinochloa crusgalli 11.22 26.32 32.64 44.00 7.05 10.53 13.06 14.75
Epilobium rubescens 11.15 25.15 31.54 33.59 10.39 12.03 12.89 14.08
Erigeron canadensis 10.40 16.69 15.85 19.23 4.68 5.83 6.04 6.16
Gnaphalium ulignosum 13.46 33.99 63.66 106.88 3.94 10.77 13.88 15.89
Polygonum persicaria 5.67 18.39 26.02 28.18 4.20 8.33 10.12 12.08
Rumex confertus 18.03 40.06 58.97 71.12 12.84 18.13 23.95 24.00
Stellaria media 7.03 19.69 31.61 39.71 4.36 8.15 9.68 10.11
Tragopogon pratensis 9.25 13.67 17.84 22.75 4.44 5.13 7.10 8.12
Trifolium pratense 8.32 40.05 82.79 111.52 7.69 16.91 18.74 20.17
Tussilago farfara 14.05 37.63 67.10 75.42 5.93 11.01 12.15 13.46
Vicia cracca 9.66 11.75 12.88 15.70 8.12 11.13 12.00 13.08
Note:
1
2
3
–low heavy metals accumulation capacity plants
–medium heavy metals accumulation capacity plants
–high heavy metals accumulation capacity plants
Table 3. Nickel and iron content in meadow phytocoenosis plants at various pollution levels (2007).
Ni content in plants, mg/kg Fe content in plants, mg/kg
Zс Zс
Species
10.091 188.72 281.293 377.086 10.091 188.72 281.293 377.086
Artemisia vulgarus 0.21 12.13 14.11 15.03 56.03 83.98 94.12 98.65
Atriplex hastata 0.08 4.00 6.11 7.95 17.92 30.61 36.76 40.11
Capsella bursa-pastoris 0.16 5.01 6.87 7.06 28.60 69.29 83.26 92.14
Cerastium holosteoides 0.08 2.05 3.65 3.07 12.56 36.98 52.73 63.09
Chenopodium rubrum 0.07 3.15 6.03 6.17 43.00 73.00 85.55 99.92
Cirsium arvense 0.65 4.61 7.12 11.52 48.40 73.60 95.98 104.64
Conovolvulus arvensis 0.43 3.61 4.01 6.19 35.50 82.16 88.72 90.68
Dactylis glomerata 0.38 1.19 6.00 6.91 50.71 60.80 70.88 83.38
Echinochloa crusgalli 0.22 4.63 5.91 6.50 52.46 95.33 104.68 114.76
Epilobium rubescens 0.63 3.21 3.86 4.17 116.61 68.58 71.11 77.87
Erigeron canadensis 0.04 1.19 3.89 4.30 37.31 52.18 55.40 61.12
Gnaphalium ulignosum 0.22 10.65 16.22 17.24 57.30 227.28 331.58 376.77
Polygonum persicaria 0.28 6.02 8.64 10.58 37.37 112.77 186.92 229.65
Rumex confertus 0.53 3.66 6.19 7.26 57.60 122.50 156.92 170.46
Stellaria media 0.08 2.66 3.27 3.71 111.90 220.21 249.82 276.71
Tragopogon pratensis 0.08 2.65 3.23 3.68 22.15 32.24 36.69 40.20
Trifolium pratense 0.53 1.33 4.02 5.90 62.22 55.11 66.08 69.87
Tussilago farfara 0.18 9.33 10.11 13.10 52.69 44.60 56.92 70.57
Vicia cracca 0.44 1.79 2.16 2.58 54.73 45.55 48.92 56.30
Note:
1
2
3
-low heavy metals accumulation capacity plants
-medium heavy metals accumulation capacity plants
-high heavy metals accumulation capacity plants

Peculiarities of Heavy Metals Accumulation by the Plants of Meadow Phytocenosis 279
0,000
0,500
1,000
1,500
2,000
2,500
3,000
3,500
10,091188,72281,293 377,086
Anthropogenic pollution cumulative rate (Zc)
Cd content in plants, mg/k
g
12345678910 11 12
3.500
3.000
2.500
2.000
1.500
1.000
0.500
0.000
Cd content in plants, mg/kg
10.091 188.72 281.293 377.086
Figure 3. Cadmium content in meadow phytocenisis at various contamination levels in 2007. 1: Cirsium arvense; 2: Atriplex
hastate; 3: Tussilago farfara; 4: Capsella bursa-pastoris; 5: Rumex confertus; 6: Artemisia vulgarus; 7: Vicia cracca; 8:
Dactylis glomerata; 9: Tragopogon pratensis; 10: Cerastium holosteoides; 11: Erigeron Canadensis; 12: Stellaria media.
It should be noted that none of the researched plants
accumulated nickel in the amount, exceeding its maxi-
mum permissible concentration in all the test plots. Ni
maximum content was detected in plot among Artemisia
vulgarus and Gnaphalium ulignosum and amounted
15.03 and 17.24 mg/kg of dry mass correspondingly.
Low zinc accumulation capacity was typical for Tra-
gopogon pratensis, Erigeron canadensis and Cerastium
holosteoides in all the test plots.
Iron is characterized by the highest concentration ratio
of all metals-bioelements in plants. For gramineous plants
Fe content in their phytomass is considered normal
within 20.0 and 300.0 mg/kg of dry substance [15]. Fe
maximum permissible concentration for gramineous plants
has not been defined.
Polygonum persicaria, Stellaria media, Gnaphalium
ulignosum and Rumex confertus had high iron accumu-
lation capacity (Table 3). The mentioned above plants
accumulated iron more actively with no regard to soil
contamination level. Fe highest concentration (376.77
mg/kg dry mass) was detected in Gnaphalium uligno-
sum phytomass and exceeded the lower limit of iron
content in gramineous plants in 1.6 times.
The basic part of the plants referred to the iron me-
dium accumulation capacity group and its averaged con-
tent in phytomass amounted 41.19, 70.15, 86.44 and
89.60 mg/kg of dry mass on plots No. 1, No. 2, No. 3 and
No. 4 correspondingly.
Tragopogon pratensis, Vicia cracca, Mentha arvensis
and Cerastium holosteoides belonged to the group of low
iron accumulation capacity. Minimal iron content was
detected in the plant—Cerastium holosteoides (12.56
mg/kg of dry mass), grown in soil not contaminated with
galvanic slurry.
It is important to state that the majority of the re-
searched species could not bear the load of toxic heavy
metals and in spite of the fact that HM ultimate content
in the plants was growing due to the soil contamination
level increase, plants phytomass was decreasing con-
siderably (Figure 4).
Cocksfoot, winterweed, waterwo rt, timothy grass and
field pansy were characterized by the most significant
phytomass decrease. These plants phytomass in test plot
No. 1 decreased by over 29%, in No. 2 plot-over 46%, in
plots No. 3 and No. 4-over 85%. Canadian thistle,
goat’s-beard, horse sorrel, sagebrush, caseweed and
treacle mustard can be referred to the plants resistant to
unfavorable growth conditions. These plants phytomass
in test plot No. 1 decreased by less than 12%, in plot
32—by less than 18%.
Different degree of phytomass decrease in these two
groups of plants can be explained by their rootage pe-
culiarities.
As its known rootage activity has the dependence al-
most concurring with the relation of root mass and depth,
and it monotonously decreases in the upper soil layer
[16]. The basic amount of plants roots in the first group
is located in the upper soil layer characterized by low
moisture reserve and high contamination level. The sec-
ond group of plants has pivotal rootage which is more
evenly spread in soil depth, so they revealed higher sta-
bility to unfavorable environmental factors due to the
possibility to absorb necessary substances from less con-
taminated HM of underlying soil horizon.
Considerable phytomass decrease of most researched
species influence HM carry-over from the soil, which
increases simultaneousely with crops growth and element
concentration. Despite HM concentration increase, caused

Peculiarities of Heavy Metals Accumulation by the Plants of Meadow Phytocenosis 280
Figure 4. Vegetation in maximum contamination level
plot.
by soil con tamination level in meadow vegetation, metals
carry over from the soil decreased (Figure 5).
Experiments have revealed that HM amount, carried
over from humus soil horizon with meadow phytocenosis
crop, is not significant as compared with the amount
washed away by the interflow. Plants share in the total
elements carry-over from humus horizon comprises from
0.003% to13.097%.
Having correlated the received data, concerning rate of
HM accumulation by plants and the data concerning
these plants crop capacity, we have revealed the species,
which can be used as phytomeliorants for contaminated
soil clearance at the final stages of restoration, when HM
amount in soil is not so great.
The majority of the revealed species possesses com-
prehensive phytomass, and its decrease compared with
other representatives of meadow vegetation is minimal
(with Zс = 188.720 amounts less 18%) (Table 4).
4. Conclusions
Among the researched phytocenosis the groups of plants
with high and low HM accumulation capacity have been
defined. The group with low HM accumulation capacity
regardless pollution level includes Tragopogon pratensis,
Erigeron canadensis and Cerastium holosteoides. Cir-
sium arvense, Capsella bursa-pastoris, Artemisia vul-
garus and Rumex confertus belonged to the group accu-
0,00
50,0 0
100,00
150,00
200,00
2
5
0
,
00
10,091188,72281,293 377,086
Anthropogenic pollution cumulative rate (Zc)
HM carry-over, g/he
c
Cu Ni Fe Zn Cd
250.00
200.00
150.00
HM carry-over, g/hec
10.091 188.72 281.293 377.086
100.00
50.00
0.00
Figure 5. Heavy metals carry-over with meadow vegetation crop at various levels of soil contamination 2007.
Table 4. Characteristics of plants phytomeliorating properties*.
Species HM, accumulated in high
amount
Phytomass variation, relative to
2006
Plants share in the
association crop
(2007), %
HM carry over with
harvest, g/hec
Cirsium arvense Cu, Zn, Cd Decrease by 15.32% 29.00 142.87
Capsella bursa-pastoris Cu, Zn, Cd Decrease by 18.35% 0.29 1.67
Artemisia vulgarus Ni, Cd Decrease by 16.00% 13.01 60.34
Rumex confertus Cu, Fe, Zn, Cd Decrease by 18.10% 6.43 40.87
*As phytoextraction is effective only for the low soil contamination level the table demonstrates only characteristics of plants growing in the plots with mini-
mum galvanic slurry share in soil (Zc = 188.720).

Peculiarities of Heavy Metals Accumulation by the Plants of Meadow Phytocenosis 281
mulating several HM in considerable amounts without
significant phytomass loss. The majority of these plants
possess developed phytomass and their ability to accu-
mulate heavy metals in large amount allows using them
as phytomeliorants for soil decontamination at the final
stages of reclaiming.
It has been stated that for more effective HM extrac-
tion from soil it is reasonable to involve several types of
plants with developed phytomass and ability to accu-
mulate various heavy metals.
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