The heavy metal content of soil and shoots of Vaccinium myrtillus L. in the Słowiński National Park

Abstract

The research was carried out in the Słowiński National Park, in an area with 15 research stations in pine coniferous forests situated at locations (1) inaccessible to tourists, (2) most frequently visited by tourists as well as (3) in the vicinity of parking lots. The analysed samples comprised surface generic levels (Ol, Ofh, A), aboveground material (shoots; leaves and stems) and below-ground material (roots) of bilberry (Vaccinium myrtillus). The performed analyses showed statistically significant Spearman’s correlation coefficients for Zn content in the ‘soil - stems:’ (r = -0.44, p < 0.05, n = 45) relationship and the ‘soil - roots’ relationship (r = -0.52, p < 0.05, n = 45). Accordingly, there were significant statistical differences (U Mann-Whitney test) in zinc content in the ‘stems - roots’ relationship and the ‘leaves - roots’ relationship. Furthermore, the obtained results reveal an excessive accumulation of Mn in V. myrtillus. The content of the investigated heavy metals in V. myrtillus shoots decreased in the following order: Mn > Fe > Zn > Cu

Full text

Leśne Prace Badawcze (Forest Research Papers),
September 2014, Vol. 75 (3): 217–224
DOI: 10.2478/frp-2014-0020
ORIGINAL RESEARCH ARTICLE
Received 11 January 2014, accepted after revision 10 March 2014.
© 2014, Forest Research Institute
The heavy metal content of soil and shoots of Vaccinium myrtillus L.
in the Słowiński National Park
Agnieszka Parzych
Pomeranian University in Słupsk, Faculty of Mathematics and Natural Sciences, Institute of Biology and Environmental
Protection, Department of Environmental Chemistry, ul. Arciszewskiego 22b, 76-200 Słupsk, Poland.
Tel. +48 59 84 05 347, fax +48 59 84 05
Abstract. The research was carried out in the Słowiński National Park, in an area with
15
research stations in
pine
coniferous forests situated at locations (1) inaccessible to tourists, (2) most frequently visited by tourists as well
as (3)
in the vicinity of parking lots. The analysed samples comprised surface generic levels (Ol, Ofh, A), above-
ground
material (shoots; leaves and stems) and below-ground material (roots) of bilberry (Vaccinium myrtillus).
The performed
analyses showed statistically significant Spearman’s correlation coefficients for Zn content in the
‘soil – stems:’ (r = -0.44,
p < 0.05, n = 45) relationship and the ‘soil
–
roots’ relationship (r = -0.52, p < 0.05, n =
45). Accordingly, there were
significant statistical differences (U Mann-Whitney test) in zinc content in the
‘stems – roots’ relationship and the ‘leaves – roots’ relationship. Furthermore, the obtained results reveal an
excessive accumulation of Mn in V. myrtillus. The content of the investigated heavy metals in V. myrtillus shoots
decreased in the following order: Mn > Fe > Zn > Cu
935; e-mail: parzycha1@op.pl
Key words: bilberry, leaves, stems, roots, accumulation of Zn, Fe, Cu, Mn, protected area
1. Introduction
Heavy metals are innate components of the natural
environment. The intrinsic content of these elements in
the lithosphere shapes the so-called geochemical back-
ground and is spatially diversied. In the recent years,
the emission due to anthropogenic factors has become a
considerable source of heavy metals. These are subject
to long-range atmospheric transport as constituents of at-
mospheric particulate matter (PM10 and PM2.5) or else
aerosols, which results in contamination of ecosystems
situated quite far from emission sources (Klink et al.
2006; Tainio et al. 2010; Brożek, Zarembski 2011). As
natural components of ecosystems, the elements such as
zinc (Zn), iron (Fe), manganese (Mn) and copper (Cu) are
necessary for appropriate functioning of plants as long as
they are available in small amounts. Conversely, exces-
sively high concentrations of these metals are harmful to
natural environment. At increased heavy metal contents,
ecosystem functioning is disturbed, and this is threaten-
ing to plants, animals and humans (Gruca-Królikowska,
Wacławek 2006; Malzahn 2009). Heavy metals bioaccu-
mulate in plant and animal tissues, which results in high
risk of poisoning with these elements in subsequent links
of the trophic chain. Plant uptake of nutrients such as iron,
manganese, zinc and copper from soil relies upon plant
physiological requirements; nevertheless, it can also be
brought about by environmental contamination. The con-
tent of metals in plant tissues also depends on their avail-
ability in soil as well as on plant species, its growth stage
and morphological features. The results of research stud-
ies conrm that plants selectively uptake elements from
surrounding environment. The nutrients are utilised by
plants for own tissue building processes as well as they
take part in numerous metabolic pathways. In the world
of plants, there exist a distinct tendency to uptake and ac-
Unauthenticated
Download Date | 9/24/15 11:11 PM

218
A. Parzych / Leśne Prace Badawcze, 2014, Vol. 75 (3): 217
–
224
cumulate certain elements (Łaszewska et al. 2007). Plants
response in different ways to increased heavy metal con-
centrations in environment. The specic sensitivity of
some plant species to the presence of heavy metals in
soil allows for the determination of the degree, range
and structure of environmental changes. Amongst plant
utilised for bioindication purposes, bilberry low-growing
shrubs Vaccinium myrtillus L. offer practical application
for attaining information on a degree of environment con-
tamination (Reimann et al. 2001; Uhlig, Junttila 2001;
Salemaa et al. 2004; Białońska et al. 2007; Kukla, Kuk-
lová 2008; Mróz, Demczuk 2010; Kandziora-Ciupa et al.
2013; Remon et al. 2013). Bilberry V. myrtillus grows
both on contaminated areas and those free of pollution.
It is a domineering species in the majority of pine Pinus
silvestris and mixed forests growing under temperate cli-
mate conditions (Białońska et al. 2007). Vaccinio myr-
tilli-Pinetum habitat constitutes the ecological optimum
for bilberry plants, which means that the species shows
the highest frequency, density, biomass and productivity
under these habitat conditions (Moszyńska 1983; Gug-
nacka-Fiedor 1994; Gerdol 2004; Zvereva, Kozlov 2005;
Parzych, Sobisz 2010). Every year, in nearly all forest
communities, V. myrtillus puts back into the litter high
amounts of potassium, calcium, magnesium as well as
manganese and iron contained in fallen leaves and adds to
important elements for proper functioning of forest eco-
systems. Studies on bioindication include bilberry leaves,
stems and roots (Mróz, Demczuk 2010; Kozanecka et al.
2002) as well as fruits ((Demczuk, Garbiec 2009; Pająk,
Jasik 2012). Bylińska (1992), Reimann et al. (2001) and
Boyd (2007) ranked V. myrtillus as plant species with su-
perior abilities to accumulate manganese.
The aim of the present study was to: examine Zn,
Fe, Mn and Cu contents in the leaves, stems and roots
of bilberry V. myrtillus L. growing within the protected
area, evaluate metal accumulation capacity across plant
parts, assess the effect of heavy metal contents in soil on
their concentration in bilberry shoots and appraise con-
tamination extent in the Słowiński National Park.
2. Materials and research methods
2.1. Research area
The study comprised forest areas within the Słowiński
National Park (SNP) located within the Łebska Spit (pro-
tective zones: Rowy, Łeba, Smołdziński Las). The study
area was situated at 17°03′–17°33′ east longitude an
54°37′–54°46′ north latitude (Fig. 1). In the park, there
prevail pine forests (71.5%), mixed pine forests (21.4%),
mixed forests (1.6%) and unclassied forest (5.5%). The
groundcover includes mainly bilberry low-growing shrubs,
mosses and lichens. The samples of bilberry aboveground
parts (leaves and stems) and roots as well as soil samples
from organic and humus horizons (Ol, Ofh and A) were
collected in September 2011 from 15 research sites placed
within SNP area. The sites were positioned either in plac-
es with no access for tourists or within most often visited
areas or else in the vicinity of parking lots.
Figure 1. Situation
plan of
the Słowiński
National Park –
locations of the study
sites and parking
Unauthenticated
Download Date | 9/24/15 11:11 PM

219
A. Parzych / Leśne Prace Badawcze, 2014, Vol. 75 (3): 217
–
224
In the samples of organic and humus soil horizons, there
were assessed soil active acidity (pH in H2O), exchangea-
ble soil acidity (1 M·dm-3 KCl solution) as well as organic
matter content (loss on ignition method using a mufe fur-
nace at 550°C). Plant material was cleaned of soil mineral
particles, rinsed in distilled water, divided into above- and
underground parts, dried out at 65°C and then homoge-
nised in a blender. The samples of soil and V. myrtilus were
wet mineralised in a mixture of HNO3 and 30% H2O2 using
the closed system. In the obtained solution, the contents of
Zn, Fe, Mn and Cu by means of atomic absorption spec-
troscopy (AAS) with the use of Perkin Elmer Analyst 300
apparatus (Ostrowska et al. 1991) and Merck KGaA stand-
ard solutions (1 g/1000 ml) were analysed.
2.2. Analyses of the results
Comparisons of the concentrations of the heavy met-
als examined in the above- and underground parts of V.
myrtillus were based on computed mean as well as max-
imum and minimum values, standard deviations, coef-
cients of variation (CV) and enrichment factors (EF).
The normality of distribution of the concentration of Zn,
Fe, Mn and Cu in V. myrtilus shoots was evaluated using
the Shapiro-Wilk test. The non-parametric Mann–Whit-
ney U-test was used to compare heavy metal concen-
trations in the parts of plants examined. All statistical
analyses were performed using Statistica 7.1. software.
3. Results and Discussion
The samples of organic and humus soil horizons in
the Łebska Spit indicated strongly acidic reaction (Table
1). The organic fermentative humic subhorizon (Ofh)
showed the highest active (pH H2O) and exchangeable
acidity (pH KCl) with pH values from 3.1 to 4.1 and from
2.5 to 3.1, respectively. For all 15 research sites, coef-
cients of variation (CV) of pH (H2O) and pH (KCl) were
from 5% to 8%. Slightly lower acidity, i.e. pH (H2O)
ranging from 3.9 to 5.0, was observed in the humus hori-
zon (A). The largest content of organic matter was found
in the litter sub-horizon (Ol), i.e. 91.6–98.5% and then
in Ofh (39.0–97.2%), whereas the lowest organic matter
content was found in the soil horizon A (0.6–5.9%). With
an increasing depth of soil horizon position, organic mat-
ter content decreased and varied from 2% to 59%.
The content of the examined heavy metals in upper
soil horizons in SNP was differentiated. The largest am-
mounts of Zn, Fe and Mn were found in the subhorizon Ol,
then in Ofh, whereas in A horizon heavy metal contents
were the lowest. In case of copper, the highest contents
were observed in the subhorizon Ofh. Average concen-
tration of zinc in the soil horizons was: 68.9 mg.kg-1 (Ol),
47.0 mg.kg-1 (Ofh) and 2.9 mg.kg-1 (A), and varied within
15 research sites from 28% to 33% (Table 2). The con-
tent of iron showed variation from 35% to 134% within
15 research sites, and on average it was 469.0 mg.kg-1 in
Ol, 1609.0 mg.kg-1 in Ofh and 346.0 mg.kg-1 in the hori-
zon A. Average content of manganese was 206.2 mg.kg-1
in Ol, 40.0 mg.kg-1 in Ofh and 4.2 mg.kg-1 in A horizon,
whereas variation coefcient for this element took values
from 52% to 58%. In the soils tested, there were observed
considerably lower contents of copper, i.e. 0.8 mg.kg-1 in
the subhorizon Ol, 0.9 mg.kg-1 in Ofh and 0.09 mg.kg-1 in
the horizon A. At the same time, Cu concentration in the
soil horizons investigated indicated lesser variation as a
result of exceptionally low mobility of this element (Ka-
bata-Pendias, Pendias 1999).
The concentration of Zn in the above- and underground
V. myrtillus shoots showed considerable variation depend-
ing on the research site and the plant section analysed. The
content of zinc was from 14.9 to 69.4 mg.kg-1 in bilberry
leaves, from 38.0 to 108.0 mg.kg-1 in the stems and from
9.7 to 51.4 mg.kg1 in the roots (Fig. 2). The highest Zn
Table 1. pH and organic matter in organic and humus horizons in SNP
Statistical
measures
pH (H2O) pH (KCl) Organic matter [%]
Ol Ofh A Ol Ofh A Ol Ofh A
Average 4.4±0.2 3.8±0.2 4.4±0.3 3.5±0.2 2.8±0.2 3.3±0.2 96.6±0.02 76.9±0.2 3.1±0.01
Minimum 4.1 3.1 3.9 3.0 2.5 2.9 91.6 39.0 0.6
Maximum 4.7 4.1 5.0 3.8 3.1 3.6 98.5 97.2 5.9
Median 4.4 3.9 4.4 3.6 2.8 3.4 97.5 73.8 2.6
CV [%] 577868 2 23 59
CV – coefcient of variation
Unauthenticated
Download Date | 9/24/15 11:11 PM

220
A. Parzych / Leśne Prace Badawcze, 2014, Vol. 75 (3): 217
–
224
Table 2. Heavy metals content (mg.kg-1) in organic and humus horizons in SNP
Statistical
measures
Zn Fe Mn Cu
Ol Ofh AOl Ofh AOl Ofh AOl Ofh A
Average 68.9±19.0 47.0±15.4 2.9±1.1 469±505 1609±2161 346±120 206.2±113 40.0±23 4.2±2.1 0.80±0.14 0.90±0.29 0.09±0.03
Minimum 37.1 24.2 1.3 118 478 124 48.7 12.2 1.2 0.50 0.60 0.06
Maximum 101.0 82.0 5.7 2071 8517 568 415.0 86.2 8.3 1.10 1.70 0.19
Median 65.5 42.7 2.7 279 907 381.1 198.9 37.4 3.7 0.8 0.9 0.08
CV [%] 28 33 38 108 134 35 55 58 52 18 31 35
Figure 2. The heavy metal content in the leaves, stems and roots of Vaccinium myrtillus in SPN, point (mean), rectangle (standard
deviation), whiskers (minimum – maximum)
amounts were observed in the shoots of bilberry growing
within the research sites located in the central areas of the
Park – those in parking lot vicinity. The concentration of
zinc showed the highest values of CV for bilberry roots
(51.3%), and the lowest for the stems (29.3 %). Plants up-
take Zn in the amounts proportional to its concentration
in soil. Several studies showed that the content of zinc in
V. myrtillus growing on non-contaminated areas regularly
Unauthenticated
Download Date | 9/24/15 11:11 PM

221
A. Parzych / Leśne Prace Badawcze, 2014, Vol. 75 (3): 217
–
224
amounted to approximately 16.8 mg.kg-1 (Mróz, Demczuk
2010) or else 20.0 mg.kg-1 (Kozanecka et al. 2002). The
content of zinc in the shoots of bilberry growing on contam-
inated areas is usually higher and amounts to 24.4 mg.kg-
1 (Pająk, Jasik 2012) or even to 107.8 mg.kg-1 (Gworek,
Degórski 2000). Leaf Zn concentration ranging from 15 to
30 mg.kg-1 usually assures the fullment of physiological
requirements of the majority of plants. The present study
carried out within the territory of the Słowiński National
Park shows that Zn is accumulated in higher amounts in
bilberry stems when compared with the leaves, which is in
line with the results obtained by Kozanecka et al. (2002).
Similar to deciduous trees loosing leaves in the fall, bil-
berry low-growing shrubs accumulate larger amounts of
nutrients in their stems and roots when compared with the
leaves (Moszyńska 1983; Gugnacka-Fiedor 1994). Low
Zn concentration in bilberry shoots reects low amounts of
this element in podzolic soils of the Park, which is derived
from poor dune sands (Tobolski et al. 1997) as well as the
fact that the plants grow under conditions of relatively
clean atmosphere (Brożek, Zarembski 2011)
The concentration of iron in V. myrtillus also showed
variation depending on the research site and plant part. Leaf
Fe concentration was from 57.0 to 182.0 mg.kg1, whereas
in the stems it was from 47.0 to 344.0 mg kg-1, and in the
roots from 50.0 to 1019.0 mg kg-1 (Fig. 2). The highest Fe
content was observed at the research sites situated in vicini-
ty of parking lots. Coefcients of variation of Fe concentra-
tion were from 22.4% for bilberry leaves to 120.2% for the
roots. The highest Fe concentrations were observed in the
underground shoots. Similar Fe content in bilberry shoots
was found by Mróz and Demczuk (2010) – 120.0–217.0
mg kg-1, and Gworek and Degórski (2000) – 95.0–104.0
mg kg-1. In some bilberry samples collected in SNP, there
was observed an increased content of Fe, which can indi-
cate advanced ability to accumulate iron in this plant spe-
cies. Strongly acidic soil environment in the Park (Table 1)
enhances the availability of heavy metals to plants. Accord-
ing to Bylińska (1992), V. myrtillus has superior capability
to accumulate iron. Within the areas free of contamination,
Fe content is usually 74 mg kg-1 in bilberry leaves and 62
mg kg-1 in the stems (Kozanecka et al. 2002).
The content of copper in bilberry shoots indicated con-
siderable differentiation among the research sites and was
from 0.5 to 3.0 mg kg-1 in the leaves, from 0.6 to 2.8 mg.kg-
1 in the stems and from 0.6 to 1.9 mg.kg-1 in the roots. Co-
efcients of variation of Cu concentration in V. myrtillus
were on average from 32.0% in the roots to 49.5% in the
leaves (Fig. 2). Plant copper shows low mobility and the
amount of approximately 2 mg.kg-1 is sufcient to cover
physiological needs of the majority of plants. The con-
tent of copper in plants is usually below 4–5 mg.kg-1 and
considerably varies depending on plant part, developmen-
tal stage as well as plant species and variety. Average Cu
content in the aboveground parts of plants is 5–20 mg.kg-1
(Kabata-Pendias, Pendias 1999). The results of chemical
analyses of V. myrtillus shoots carried out by Gworek and
Degórski (2000) in several locations in Poland indicate that
depending on contamination degree, the concentration of
Cu can be from 0.5 to 8.1 mg.kg-1. Earlier chemical studies
on V. myrtillus aboveground shoots carried out in the fresh
pine forests within the Słowinski National Park showed
Cu concentration 3.1 mg.kg-1 (Parzych et al. 2012). The
content of Cu in bilberry plants from the Park is low and
not threatening – in contrast, it is sufcient for covering V.
myrtilus physiological needs.
Fairly different status was observed for manganese con-
tents. These were from 529.2 to 1736.0 mg.kg-1 in bilberry
leaves, from 658.0 to 2182.0 mg.kg-1 in the stems and from
105.9 to 746.3 mg.kg-1 in the roots (Fig. 2). The concen-
tration of Mn indicated related variation – from 34.9 to
35.3%, regardless of the part of plant analysed. According
to Kabata-Pendias and Pendias (1999), plant requirements
for manganese are much differentiated, but in most cases
the amount of 10–25 mg.kg-1 is sufcient. The concentra-
tion of about 500 mg.kg-1 can be toxic for the majority of
plants. The results obtained in this study indicate excessive
accumulation of manganese in V. myrtillus shoots. Rei-
mann et al. (2001) as well as Bylińska (1992) noted that
bilberry plants were distinctive of high contents of Mn,
apart from those observed in soil. Boyd (2007) described
this low-growing shrub as manganese accumulator in view
of the fact that the concentration of manganese in bilberry
tissues can be even above 2000 mg.kg-1. The results of re-
search reported by Gworek and Degórski (2000) indicated
that V. myrtillus could accumulate in its tissues even 2489.0
mg.kg-1, which proves the large capability of this species to
accumulate manganese.
The relationships among heavy metals determined
both in the aboveground and underground parts of V.
myrtillus showed the following decreasing order: Mn >
Fe > Zn > Cu.
The analyses carried out revealed statistically signif-
icant Spearman’s correlation coefcients for bilberry
zinc content in the relationship soil – stems (r = -0.44,
p < 0.05, n = 45) as well as soil – roots (r = -0.52, p <
0.05, n = 45). The decrease of zinc content in soil was
accompanied by the increase of Zn content in V. myrtil-
lus stems and roots, which is conrmed by the uptake
of high amounts of this element from the soil solution
Unauthenticated
Download Date | 9/24/15 11:11 PM

222
A. Parzych / Leśne Prace Badawcze, 2014, Vol. 75 (3): 217
–
224
(Table 3). Other heavy metals tested (Fe, Cu, Mn) did not
show statistically signicant relationships between their
concentrations in soil and those in billberry shoots, which
can indicate leaf uptake of these elements from either pre-
cipitation or atmospheric particulate matter settling to the
ground (Łaszewska et al. 2007).
Low contents of Zn, Fe and Cu in the above- and
underground V. myrtillus shoots as well as in surface
soil layers are well reected by the low values of en-
richment factors (EF). The highest EF values were ob-
tained for Mn (EF > 20), which conrms its tendency
to elevated accumulation in plants (Fig. 3), and the
lowest for copper (Mn > Fe > Zn > Cu). The results
obtained in the National Słowiński Park indicate that
zinc and manganese are accumulated to the largest ex-
tent in V. myrtillus stems, whereas copper in the leaves
and iron in the roots. According to Kłos (2009), EF
values >10 can indicate the inux of exterior pollution,
for example, with dry and wet precipitation. However,
heavy metal inux is in general relatively small. The
results of the study on particulate matter carried out in
2010 within the area of the Słowiński National Park
Table 3. Spearman correlation coefcients (r) of heavy metals
in the shoots V. myrtillus relative to ‘soil – leaves’, ‘soil –
stems’, ‘soil – roots’ (n = 45, p < 0.05, rcryt. = 0.30)
r in relation Fe Mn Zn Cu
soil – leaves 0.17 0.25 -0.28 0.20
soil – stems 0.01 0.27 -0.44 -0.21
soil – roots 0. 25 -0.06 -0.52 -0.01
Figure 3. Enrichment factors (EF) investigated metals in the leaves, stems and roots of V. myrtillus, point (mean), rectangle
(standard deviation), whiskers (minimum – maximum)
Unauthenticated
Download Date | 9/24/15 11:11 PM

223
A. Parzych / Leśne Prace Badawcze, 2014, Vol. 75 (3): 217
–
224
showed PM10 content 17 μg/m3 (Brożek, Zarembski
2011), and this did not exceed the threshold value. SNP
area has been considered by many researchers as one
of the cleanest in Poland. Among others, this is con-
rmed by chemical studies on forest bioindicative ora
(Grodzińska et al. 1990, 1999; Bykowszczenko et al.
2006; Parzych et al. 2012; Parzych, Sobisz 2012).
Comparative analyses of heavy metal concentrations
in the above- and underground shoots of bilberry V. myr-
tillus were performed using the Mann–Whitney U-test
(Table 4). The results obtained showed statistically signif-
icant differences in zinc content in the relationship stems
– root and leaves – stems as well as manganese content
in the relationship stems – roots and leaves – roots No
signicant differences were found for Fe and Cu concen-
trations in bilberry above- and underground shoots.
4. Conclusions
In the above- and underground shoots of bilberry V.
myrtillus growing on the territory of the Słowinski Nation-
al Park located within the Łebska Spit, there were found
varied contents of Zn, Fe, Mn and Cu depending on re-
search site localisation and the part of plant. The highest
amounts of the heavy metals tested were found in the sites
in vicinity of parking lots, which tells on the role of road
trafc in point contamination of the Park. The metals in-
vestigated were accumulated in V. myrtillus shoots to dif-
ferent extents. The highest amounts of copper were found
in bilberry leaves, those of iron – in the roots, and those
of zinc and manganese were observed in the stems. The
relationships among heavy metals determined both in the
aboveground and underground parts of V. myrtillus showed
the following decreasing order: Mn > Fe > Zn > Cu.
Small contents of Zn, Fe and Cu in bilberry shoots as
well as in the surface horizons of soil translate into the
low enrichment factor (EF) values obtained in this study.
Strongly acidic soil environment enhanced the bioavail-
ability of the heavy metals tested to bilberry shoots. The
highest EF values were obtained for Mn and Fe, which is
a sign of greater accumulation ability of V. myrtillus as for
these elements, despite their low contents in soil.
The analyses carried out showed statistically signi-
cant differences in Zn content in the relationships leaves
– stems and stems – roots as well as in Mn content in the
relationship stems – roots and leaves – roots. No signicant
differences were found for Fe and Cu concentration in the
above- and underground shoots of bilberry V. Myrtillus.
Acknowledgements
The study was carried out in the year 2011 in a frame-
work of the statutory research grant of the Department of
Environmental Chemistry, Institute of Biology and En-
vironmental Protection, Pomeranian Academy in Słupsk.
References
Białońska D., Zobel A. M., Kuraś M., Tykarska T., Sawic-
ka-Kapusta K. 2007. Phenolic compounds and cell struc-
ture in bilberry leaves affected by emissions from a Zn–Pb
smelter. Water, Air and Soil Pollution, 181: 123–133.
Boyd R.S. 2007. The defense hypothesis of elemental hyper-
accumulation: status, challenges and new directions. Plant
and Soil, 293: 153–176.
Brożek A., Zarembski A. 2011. Roczna ocena jakości powi-
etrza w województwie pomorskim, Raport za rok 2010.
Gdańsk, Wojewódzki Inspektorat Ochrony Środowiska.
Bylińska E. 1992. Studia nad biogeochemią roślin z obszaru
występowania złóż polimetalicznych w Rudawach Janow-
ickich (Sudety). Acta Universitatis Wratislaviensis, Prace
Botaniczne, T 50. Wrocław, Uniwersytet Wrocławski, 71
p. ISBN 8322907923.
Bykowszczenko N., Baranowska-Bosiacka I., Bosiacka B., Kacz-
marek A., Chlubek D. 2006. Determination of heavy metal
concentration in mosses of Słowiński National Park using
atomic absorption spectrometry and neutron activation anal-
ysis methods. Polish Journal of Environmental Study, 15(1):
41–46.
Demczuk M., Garbiec K. 2009. Heavy metals in edible fruits.
A case study of bilberry Vaccinium myrtillus L. Ochrona
Środowiska i Zasobów Naturalnych, 40: 307–312.
Gerdol R. 2004. Growth performance of two deciduous Vac -
cinium species in relation to nutrient status in a subalpine
heath. Flora, 200: 168–174.
Grodzińska K., Szarek-Łukaszewska G., Godzik B. 1999. Sur-
vey of heavy metal deposition in Poland using mosses as in-
dicators. The Science of the Total Environment, 229: 41–51.
Grodzińska K., Szarek G., Godzik B. 1990. Heavy metal
deposition in Polish National Parks – changes during ten
years. Water, Air and Soil Pollution, 49: 409–419.
Table 4. The signicance of variation of heavy metals concentra-
tion in the tested shoots V. myrtillus (Mann–Whitney U-test)
Metal Relations
leaves – stems stems – roots leaves – roots
Zn ** *** ns
Fe ns nsns
Cu ns nsns
Mn ns *** ***
The signicance level: ***p < 0.001, *p <0.05, ns – no differences
Unauthenticated
Download Date | 9/24/15 11:11 PM

224
A. Parzych / Leśne Prace Badawcze, 2014, Vol. 75 (3): 217
–
224
Gruca-Królikowska S., Wacławek W. 2006. Metale w środow-
isku. Cz. II. Wpływ metali ciężkich na rośliny [Metals in
the environment. Part II. Effect of heavy metals on plants].
Chemia, Dydaktyka, Ekologia, Metrologia, 11(1–2): 41–56.
Gugnacka-Fiedor W. 1994. Zmienność morfologiczna i chem-
iczna europejskich gatunków rodzaju Vaccinium L. Toruń,
Rozprawy – Uniwersytet Mikołaja Kopernika, 146 p.
ISBN: 83-231-0511-1.
Gworek B., Degórski M. 2000. Borówka (Vaccinium myr-
tillus) oraz igły sosny (Pinus sylvestris) wskaźnikami
zanieczyszczenia środowiska metalami ciężkimi w wy-
branych siedliskach borowych na terenie Polski. Roczniki
Gleboznawcze, 51(1/2): 79–86.
Kabata-Pendias A., Pendias H. 1999. Biogeochemia pierwiastków
śladowych, Warszawa, PWN, 400 p. ISBN 83-01-12823-2.
Kandziora-Ciupa M., Ciepał R., Nadgórska-Socha A., Barczyk
G. 2013. A comparative study of heavy metal accumula-
tion and antioxidant response in Vaccinium myrtillus L.
leaves in polluted and non-polluted areas. Environmental
Science and Pollution Research, 20: 4920–4932.
Klink A., Letachowicz B., Krawczyk J., Wisłocka M. 2006.
The content of heavy metals in soil and silver birch leaves
(Betula pendula Roth) from Wałbrzych and Głogów. Pol-
ish Journal of Environmental Study, 15: 347–350.
Kłos A. 2009. Zastosowanie współczynnika wzbogacenia
(EF) do interpretacji wyników badań biomonitoringowych
[Application of enrichment factor (EF) for intepretation of
the results of biomonitoring studies]. Chemia, Dydaktyka,
Ekologia, Metrologia, 14(1– 2): 49–55.
Kozanecka T., Chojnicki J., Kwasowski W. 2002. Content of
heavy metals in plant from pollution-free regions. Polish
Journal of Environmental Study, 11(4): 395–399.
Kukla J, Kuklová M. 2008. Growth of Vaccinium myrtillus
L. (Ericaceae) in spruce forests damaged by air pollution.
Polish Journal of Ecology, 56(1): 149–155.
Łaszewska A., Kowol J., Wiechuła D., Kwapuliński J. 2007.
Kumulacja metali w wybranych gatunkach roślin lec-
zniczych z terenu Beskidu Śląskiego i Beskidu Żywieck-
iego [Bioaccumulation of metals in selected species of
medicinal plants in the Silesian and Żywiec Beskids].
Problemy Ekologii, 11, 6: 285–291.
Malzahn E. 2002. Igły sosny zwyczajnej jako bioindykator
zagrożeń środowiska leśnego Puszczy Białowieskiej. Bi-
uletyn Monitoringu Przyrody, 1(3): 19–31.
Moszyńska B. 1983. Some problems on ecology of Vaccinium
myrtillus L. in pine forest communities. Polish Ecological
Studies, 9: 565–643.
Mróz L., Demczuk M. 2010. Contents of phenolics and chem-
ical elements in bilberry (Vaccinium myrtillus L.) leaves
from copper smelter area (SW Poland). Polish Journal of
Ecology, 58(3): 475–486.
Ostrowska A., Gawliński S., Szczubiałka Z. 1991. Metody
analizy i oceny gleb i roślin. Katalog. Warszawa, Instytut
Ochrony Środowiska, 333 p.
Pająk M., Jasik M. 2012. Zawartość cynku, kadmu i ołowiu
w owocach borówki czarnej (Vaccinium myrtillus L.) ros-
nącej w lasach Nadleśnictwa Świerklaniec [Concentration
of zinc, cadmium and lead in the fruits of bilberry (Vac -
cinium myrtillus L.) growing in the Świerklaniec Forest
District]. Sylwan, 156(3): 233–240.
Parzych A., Sobisz Z. 2010. Biomasa i produkcja pierwotna
netto runa leśnego w wybranych ekosystemach Słowińsk-
iego Parku Narodowego. Ochrona Środowiska i Zasobów
Naturalnych, 42: 72–83.
Parzych A., Sobisz Z., 2012: Zawartość makro- and mikro-
pierwiastków w igliwiu Pinus sylvestris L. i Pinus nigra
Arn. w Słowińskim Parku Narodowym [The macro- and
microelemental content of Pinus sylvestris L. and Pinus
nigra J.F. Arn. needles in Cladonio-Pinetumhabitat of the
Słowiński National Park]. Leśne Prace Badawcze, 73(4):
295–303.
Parzych A., Sobisz Z., Trojanowski J. 2012. Prognosis content
of heavy metals in soil and herbaceous plants in selected
pine forests in the Słowiński National Park. Archives of
Environmental Protection, 38(4): 35–47.
Reimann C., Koller F., Kashulina G., Niskavaara H., Englmai-
er P. 2001. Inuence of extreme pollution on the inorganic
chemical composition of some plants. Environmental Pol-
lution, 115: 239–252.
Remon E., Bouchardon L., Le Guedard M., Bessoule J., Conord
C. 2013. Are plants useful as accumulation indicators of
metal bioavailability? Environmental Pollution, 175: 1–7.
Salemaa M., Derome J., Helmisaari H.S, Nieminen T.,
Vanha-Majamaa I. 2004. Element accumulation in boreal
bryophytes, lichenes and vascular plants expose to heavy
metal and sulfur deposition in Finland. Science of the Total
Environment, 324: 131–160.
Tainio M., Kekkonen J., Nahorski Z. 2010. Impact of airborne
particulate master on human an assessment framework to
estimate exposure and adverse heath effect in Poland. Ar-
chives of Environmental Protection, 36(1): 95–115.
Tobolski K., Mocek A., Dzięciołowski W., 1997. Gleby Słow-
ińskiego Parku Narodowego w świetle historii roślinności
i podłoża. Bydgoszcz-Poznań, Wyd. Homini, 183 p.
Uhlig C., Junttila O. 2001. Airborne heavy metal pollution and
its effects on foliar elemental composition of Empetrum
hermaphroditum and Vaccinium myrtillus in Sor-Varanger,
northern Norway. Environmental Pollution, 114: 461–469.
Zvereva E.L., Kozlov M.V. 2005. Growth and reproduction
of dwarf shrubs, Vaccinium myrtillus and V. vitis-idaea,
in a severely polluted area. Basic and Applied Ecology,
6: 261–274.
Translated by: Bożena Kornatowska
Unauthenticated
Download Date | 9/24/15 11:11 PM