Chemosphere 81 (2010) 321–326
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Bioindication capacity of metal pollution of native and transplanted Pleurozium schreberi under various levels of pollution G. Kosior a, A. Samecka-Cymerman a,*, K. Kolon a, A.J. Kempers b a b
Department of Ecology, Biogeochemistry and Environmental Protection, Wrocław University, ul. Kanonia 6/8, 50-328 Wrocław, Poland Department of Environmental Sciences, Huygens Building, Heyendaalseweg 135, 6525 AJ Nijmegen, The Netherlands
a r t i c l e
i n f o
Article history: Received 19 May 2010 Received in revised form 14 July 2010 Accepted 15 July 2010 Available online 8 August 2010 Keywords: Bioindication Heavy metal Pleurozium schreberi Pollution Upper Silesia Transplant
a b s t r a c t During a period of 90 d assays were carried out with the moss Pleurozium schreberi transplanted from an uncontaminated control site to 27 sites selected in one of the most polluted regions of Upper Silesia (Poland). The native mosses of this species were collected from the polluted sites. Concentrations of Cd, Cr, Cu, Pb and Zn were determined in P. schreberi and in the soil of all of the sites. The sites were divided into more and less polluted ones. The obtained results indicate that the native P. schreberi from the more polluted sites accumulated significantly more Cd, Cr, Cu, Pb and Zn than the transplanted moss from the same sites. The transplanted P. schreberi from the less polluted sites accumulated significantly more Cr, Pb, Zn, significantly less Cu and comparable amounts of Cd, as compared to the native moss. The selection of native versus transplant P. schreberi as a bioindicator depends on the level of pollution. Ó 2010 Elsevier Ltd. All rights reserved.
1. Introduction Upper Silesia (centred around the city of Katowice, Fig. 1) is one of the most urbanised, industrialised and polluted regions of Poland, with a high population density characterised by hard coal mines, zinc and lead ore mining, smelters, iron and steel metallurgical works, nonferrous metal processing, chemical and cement plants, and power stations (Szarek-Łukaszewska et al., 2002). Both the exploitation of mineral resources and industrial activity have caused high levels of air pollution, soil and surface water contamination and the accumulation of industrial wastes. Two ecological hazard areas were identified within this region: the Upper Silesian Ecological Hazard Area and the Rybnik Ecological Hazard Area. These regions have been recognised as areas of ecological disaster (Wcisło et al., 2002). The examined area receives emissions from the local industry, and these are regarded to be primarily responsible for most of the trace elements in the air. Additionally, this area is affected by heavy traffic and air-borne transboundary pollution from Germany and the Czech Republic (Appleton et al., 2000). The accumulation of heavy metals in such an environment may cause chronic damage to living organisms and must be carefully controlled. Bryophytes have been described in the literature as being able to intercept, retain and accumulate pollutants. Their
* Corresponding author. Tel.: +48 71 3754103. E-mail addresses:
[email protected] (A. Samecka-Cymerman), L.Kem
[email protected] (A.J. Kempers). 0045-6535/$ - see front matter Ó 2010 Elsevier Ltd. All rights reserved. doi:10.1016/j.chemosphere.2010.07.029
bioconcentration ability is such that they accumulate metals to levels far above their expected physiological needs (Zechmeister et al., 2003). Metal biomonitoring with naturally growing mosses, first used by Rühling and Tyler (1968), has been a valid technique used in Europe for over 40 years (Markert et al., 2003; Kłos et al., 2010). These plants have a high surface-to-volume ratio enabling particles to be trapped, as well as a high cation exchange capacity and the lack of a well-developed cuticle in their tissues, which leads to the accumulation of large amounts of elements (Zechmeister et al., 2003). An additional advantage of these plants is that they are available for investigation all year round. Sampling and analysis of these plants is fast and economical. The technique of analysing the contents of contaminants in mosses is known as passive biomonitoring (Rühling and Tyler, 1968). Moss transplants have also been used as active biomonitors by Tyler (1990). This method was developed in Scandinavia and applied on an international, regional or local scale by Zechmeister et al. (2003). Transplants are often used because of an absence of native mosses. Fernándèz et al. (2000) assumed that it is well known that plants have a capacity to adapt to certain environmental conditions, so native mosses should accumulate significantly less heavy metals than the transplanted mosses of the same species. In this investigation we compared the bioconcentration of metals in Pleurozium schreberi transplanted from an unpolluted control site to an extremely polluted area in Upper Silesia with the bioconcentration of identical elements in this species growing naturally at the contaminated and control sites.
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50°30'40"N 18°29'49"E
50°30'40"N 19°40'42"E
N
Zawiercie
8
78 11 Pyskowice
9
10
78
Siewierz
5 6
7
S1
Tarnowskie Góry
24
25
12
4
Bytom
Dąbrowa Górnicza
Gliwice
17
22
13
E40
14
19
Jaworzno E40
S1
18
POLAND Warszawa
16 0
2
1
27
Mikołów ł
Rybnik
23
Katowice
Olkusz 3
20 10 km
15
26 Oświęcim
21
50°03'11"N 18°29'49"E
Katowice Sieniawa
50°03'11"N 19°40'42"E Fig. 1. Location of the investigated area.
We tested the hypotheses that the bioindication value of native and transplanted P. schreberi is dependent on the level of pollution of the investigated area. 2. Materials and methods We selected the terrestrial, carpet forming, pleurocarpous and ectohydric P. schreberi (a moss species) because it occurs widely in the Northern Hemisphere, including Poland. This species has been used successfully in recent decades and has proved to be a suitable bioindicator of inorganic substances and, therefore, has been widely used to map and monitor heavy metal pollution in European countries (Samecka-Cymerman et al., 2006). P. schreberi is a widespread species abundant in acid and organic substrates in coniferous forests (Aichele and Schwegler, 1984). 2.1. Sampling design Samples were collected within a rectangular area of 80 60 km2 (Fig. 1). This area was divided into 48 squares of 10 10 km2. From these 48 squares, 27 were selected randomly. Within the central part (an area of 50 50 m2) of each of the selected 27 squares, 5 sub-squares of 2 2 m2, covered with P. schreberi, were selected randomly for the collection of this native moss (only the green parts of P. schreberi were taken) and topsoil (0–5 cm) samples. Each plant and soil sample consisted of a mixture of three sub-samples. In each of these five 2 2 m2 sub-squares, five randomly chosen places were cleaned from vegetation into which patches (20 20 cm2) of P. schreberi (originating from the control site) were transplanted. The remaining part of the 2 2 m2 subsquare was left covered with native P. schreberi. The total number of samples was N = 28 5 = 140, including the five samples from the unpolluted control site between Sieniawa and Adamowka,
200 km east of Katowice and 112 km south of Lublin (50°130 0300 N; 22°430 5300 E). Within the control site, five 2 2 m2 sub-squares were selected randomly into which patches (20 20 cm2) of P. schreberi were transplanted in the same way as in the Upper Silesia area in order to control the influence of transplantation on metal accumulation. In the same sampling site of the control area, five samples of the topsoil (0–5 cm, each sample consisted of a mixture of three sub-samples) were taken, giving a total of N = 50. Plant remains and stones were removed from the soil samples before transporting them to the laboratory. The amount of replications was sufficient for proper statistical interpretation of the data. As required by the rules set by the Environmental Monitoring and Data Group (Markert et al., 1996) and within the European Heavy Metal Survey (UNECE, 2003), the collected moss had not been exposed directly to canopy throughfall. Dead material, soil particles and litter were manually removed from the moss samples. The moss samples were not washed (Markert et al., 1996; UNECE, 2003).
2.2. Plant and soil analysis The moss and soil samples (300 mg of dry weight, in triplicate) were digested with 3 ml of nitric acid (ultra pure, 65%) and 2 ml of perchloric acid (ultra pure, 70%) in a CEM Mars 5 microwave oven (Matusiewicz 2003). The temperature/pressure programme consisted of five steps: (1) 5 min 110 °C at a pressure of 344.74 kPa;(2) 5 min 170 °C at 827.38 kPa; (3) 20 min 190 °C at 1654.74 kPa; (4) 5 min 200 °C at 2068.43 kPa and (5) cooling down to 25 °C. After dilution to 50 mL, the soil digest was filtered using Whatman type 2 filter paper into polyethylene containers (the first drops were discarded). The plant digest was clear and filtering was not necessary. The plant and soil digests were analysed for Zn
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log-transformed data to obtain a normal distribution of features according to Zar (1999). The normality of the analysed features was checked by means of Shapiro–Wilk’s W test, and the homogeneity of variances was checked by means of Bartlett’s test (Sokal and Rohlf, 2003). Concentrations of elements in the soils and native and transplanted mosses from the control and Upper Silesia sites were examined with the t-test applied to the log-transformed data. A post hoc LSD test was used to compare the concentrations of metals in the moss after 0–45–90 d of exposure (Zar, 1999). The accumulation factor for the transplanted P. schreberi collected after 0–45–90 d of the experiment was examined by calculating the ratio 45/0 and 90/45. All calculations were done with the Statistica 8.0 program (StatSoft, 2008).
using FAAS and Cd, Cr, Cu, Pb using ETAAS with Graphite Furnace GF3000 both Atomic Absorption Spectrophotometry AVANTA PM GBC Scientific Equipment (Lajunen and Perämäki 2004). The technical details of the AAS methods were as follows: Cd lamp wavelength: 228.8 nm, slit width: 0.5 nm, ashing (temp/ramp time/ hold time): 650 °C/10 s/15 s, atomisation (temp/ramp time/hold time): 1700 °C/1 s/0.6 s, matrix modifier: NH4H2PO4. Pb lamp wavelength: 283.3 nm, slit width: 0.6 nm, ashing: 750 °C/10 s/ 25 s, atomisation: 1600 °C/0.8 s/2 s, matrix modifiers: NH4H2PO4 + Mg(NO3)2. Cu lamp wavelength: 327.4 nm, slit width: 0.5 nm, ashing: 800 °C/10 s/15 s, atomisation: 2300 °C/0.8 s/0.8 s without matrix modifiers. Cr lamp wavelength: 425.4 nm, slit width: 0.2 nm, ashing: 1100 °C/10 s/15 s, atomisation 2500 °C/0.8 s/2.0 s, matrix modifiers: Pd(NO3)3. Some of the samples had to be diluted. Zn lamp wavelength: 213.9 nm, slit width: 0.5 nm flame: air + acetylene. The detection limit for the GF AAS was in lg L1 Cd: 0.006, Cr: 0.06, Cu: 0.08, Pb: 0.15. The detection limit for the flame AAS was Zn: 1.5 lg L1. All elements were determined against standards (Atomic Absorption Standard Solution from Sigma Chemical Co.) and blanks containing the same matrix as the samples and were subjected to the same procedure. All results for the plants were calculated on a dry weight basis. Accuracy of the methods as applied for the determination of Cd, Cr, Cu, Pb and Zn after microwave-assisted digestion of plants and soil samples was checked by analysis of Certified Reference Materials. We used as certified reference materials bush branches and leaves DC73348 LGC standards and RTH 907 Dutch Anthropogenic Soil (Wageningen Evaluating Programms for Analytical Laboratories, WEPAL). The coefficient of variance (CV) was calculated for the determined concentrations of elements in the reference materials. The results are presented in Table 1. The chlorophyll-to-phaeophytin (D665/D665a) ratio, as an index of physiological stress, was measured by the Lopez et al. (1997) method. Cellular distribution of Cu and Pb in P. schreberi was analysed with the Sequential Elution Technique using EDTA 20 mM and HNO3 1 M (Vázquez et al., 1999).
3. Results and discussion The ranges of metal concentrations in the soil of P. schreberi are displayed in Table 2. The soil and moss samples differed significantly in terms of concentrations of the elements assessed (ANOVA, P < 0.05). The metal concentrations in soils from the control site were significantly lower (Table 2) than the concentrations of these elements in soils from the Upper Silesia sites. In terms of the pollution classes for Polish soils as proposed by Kabata-Pendias (2001), the samples from the polluted sites exceeded the upper limits for clean soils (limits indicated in parentheses in mg kg1) for Cd (0.5), Cu (25; except for the soil from the less polluted sites), Pb (50) and Zn (70). The metal concentrations in P. schreberi from the control site (Table 3) were similar to those in P. schreberi from the non-polluted Puszcza Biała Forest (Kozanecka et al., 2002), thus indicating that the control site we selected can be regarded as relatively free from the influence of anthropogenic pollution. Compared to the values of the control site, the concentrations of all of the investigated metals were significantly higher (test t, P < 0.05) in the mosses from the Upper Silesia sites (Table 3) and exceeded the upper concentrations (in parentheses mg kg1) of Cd (<0.2), Cr (0.9–3), Cu (4.5), Pb (5.7) and Zn (25) of the background values given by Bykowszczenko et al. (2006) for terrestrial mosses from unpolluted areas. These metal concentrations, as we found in P. schreberi, reflected the
2.3. Statistical analysis Differences between the sampling sites in terms of concentrations of elements in the mosses were evaluated by ANOVA on
Table 1 Analysis of certified reference material. Element
Bush branches and leaves DC73348 LGC
Cd Cr Cu Pb Zn
Dutch anthropogenic soil RTH907
Certified (lg g1)
Found (lg g1)
Recovery (%)
CV (%)
Certified (lg g1)
Found (lg g1)
Recovery (%)
CV (%)
0.140 ± 0.06 2.30 ± 0.30 5.20 ± 0.50 7.10 ± 1.10 20.60 ± 2.20
0.136 ± 1.01 2.29 ± 0.07 5.04 ± 0.13 6.77 ± 0.22 20.82 ± 0.33
97.14 99.57 96.94 95.28 101.05
4.5 3.2 2.6 3.3 1.6
2.18 ± 0.33 48.60 ± 6.64 121.00 ± 12.00 318.00 ± 25.00 714.00 ± 50.00
2.23 ± 0.09 53.71 ± 1.24 118.83 ± 1.78 309.22 ± 7.41 715.35 ± 9.43
102.29 110.51 98.21 97.24 100.19
4.0 2.3 1.5 2.4 1.3
Table 2 Minimum/maximum values (mg kg1), mean and SD of concentrations of elements in soil from more polluted (MP) and less polluted (LP) and control (C) sites; t-tab.0.05 MP–LP (133) = 1.978; t-tab.0.05 MP–C (68) = 1.995; t-tab.0.05 LP–C (73) = 1.993. Element
Cd Cr Cu Pb Zn
More polluted (MP)
Less polluted (LP)
Control (C)
Minimum
Maximum
Mean
SD
Minimum
Maximum
Mean
SD
Minimum
Maximum
Mean
SD
2.3 50 10 85 113
4.3 395 155 460 497
2.7 145 73 150 250
1.1 25 9 43 58
0.4 12 1.6 49 67
3.9 92 21 287 183
1.6 51 10 90 100
0.3 9 1.2 25 43
0.1 8.5 1.2 7.7 8.4
0.5 31 3.3 28 25
0.3 20 2.6 18 14
0.1 6.0 0.5 4.5 3.6
Test t MP– LP
Test t MP–C
Test t LP–C
8.05 29.48 58.03 10.00 17.15
4.84 11.09 17.37 6.82 9.04
9.60 7.56 13.63 6.39 4.44
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Table 3 Minimum/maximum values (mg kg1), mean and SD of concentrations of elements in native P. schreberi from more polluted (MP) and less polluted (LP) and control (C) sites; ttab.0.05 MP–LP (133) = 1.978; t-tab.0.05 MP–C (68) = 1.995; t-tab.0.05 LP–C (73) = 1.993. Element
Cd Cr Cu Pb Zn
More polluted (MP)
Less polluted (LP)
Control (C)
Minimum
Maximum
Mean
SD
Minimum
Maximum
Mean
SD
Minimum
Maximum
Mean
SD
3.6 6.0 9.6 93.0 245.0
4.7 9.0 12.4 133 317
4.0 7.5 11 113 280
0.3 1.0 1.0 13 25
0.2 4.9 8.9 27 90
2.6 7.5 11 39 116
1.4 6.2 9.9 33 102
0.7 0.9 0.6 3.5 9.7
0.3 2.4 3.5 2.5 28
0.5 3.7 4.6 3.7 36
0.4 3.0 4.1 3.1 32
0.1 0.4 0.4 0.4 2.5
emissions produced by the heavy industry of Upper Silesia (Kabata-Pendias, 2001). Especially the concentrations of Pb and Zn, reaching values 816 and 1673 (in mg kg1), respectively, were extremely high and much higher than the harmful concentrations of above 300 mg Pb kg1 and 400 mg Zn kg1 as mentioned by Kabata-Pendias (2001). These concentrations were characteristic of the P. schreberi collected in the most important Zn–Pb ore mining area located around Olkusz in Southern Poland (site 3 Fig. 1). This area was contaminated by past exploitation and processing (mining and smelting) of these ores (Cabala et al., 2009). P. schreberi from this extremely polluted site was defined as healthy-looking and without any chlorotic/necrotic symptoms, which could have obvious detrimental effects on vitality. These results point to the assumption that some bryophytes accumulate potentially toxic levels of metals without any apparent damage (Wells and Brown 1995). The chlorophyll-to-phaeophytin (D665/D665a) ratio (Küpper et al., 1996) was the highest for P. schreberi from the control site. In transplants, the ratio diminished significantly during the exposure time (Fig. 2). As could be expected, this ratio for the native mosses did not differ significantly between the beginning and end of the experiment. A statistically significant lowering of the level of this ratio (post hoc LSD P < 0.01) in the transplanted mosses during the exposure time was probably caused by an increase in the concentration of heavy metals in the new, polluted sites (Guschina and Harwood, 2002). This influence of metals was confirmed by negative Pearson correlations (P < 0.05) between concentrations of Cd, Pb or Zn in both the native and transplanted mosses and the chlorophyll-to-phaeophytin ratio. The Sequential Elution Technique showed that cellular distribution of Cu and Pb in P. schreberi was mostly extracellular in both
chlorophyll-to-phaeophytin ratio
1.2
1.1
1.0
0.9
0.8
0.7
0. 6
T0
T45
T90
M0
M45
M90
Dayof exposure Fig. 2. Minimum/maximum values ( ), mean (s) and SD (h) of the chlorophyll-tophaeophytin (D665/D665a) ratio in the control, native and transplanted Pleurozium schreberi after 0, 45 and 90 d of exposure.
Test t MP– LP
Test t MP–C
Test t LP–C
27.65 8.02 7.79 49.05 56.26
23.20 10.14 15.32 18.54 22.53
3.23 8.24 19.91 19.09 16.14
the native and transplant mosses collected after 0–45–90 d of exposure. This was in agreement with Vázquez et al. (1999), who stated that in most cases more metal was taken up in the extracellular compartment than in the intracellular one, while particulatefraction content was negligible. All sites were divided into less and more contaminated ones as we found that significant differences in the accumulation of metals by the transplant mosses depended on the level of pollution of the sampling places. We based this division on the sum of standardised concentrations of Pb and Zn in the native mosses from the 27 experimental sites. As a border value we stated their median value as 0.48. According to this median, sites 1–5, 8–10, 13, 18, 23–24 and 26 were grouped as more polluted, and sites 6–7, 11–12, 14– 17, 19–22, 25 and 27 were grouped as less polluted. According to Fernándèz et al. (2000), plants have the capacity to adapt to certain environmental conditions. His study on Scleropodium purum, as well as a study by Samecka-Cymerman and Kempers (2007) on Pohlia nutans illustrated that the native mosses accumulated significantly less heavy metals than the transplanted mosses of the same species. Therefore, the transplanted species reflected a better level of contamination with metals as examined by the above-mentioned authors. Our results on the bioaccumulation of elements were partially different. There was a significant difference in accumulation by the native and transplanted mosses between the more or less polluted areas. The concentration of all metals in the native mosses from the more polluted sites was always higher (Fig. 3) than in the transplanted mosses from the more polluted sites. Therefore, in the more polluted sites the native mosses were better bioindicators than the transplants. This result indicates a possible mechanism of adaptation which allowed these mosses to survive the accumulation of extremely high levels of metals (Fernándèz and Carballeira, 2001). According to Shaw (1994) and Guschina and Harwood (2002), some species of mosses appear to have inherently high levels of metal tolerance, which permits them to colonise and thrive in metal-contaminated environments. Fernándèz et al. (2000) and Samecka-Cymerman and Kempers (2007) reported better accumulation abilities of transplanted rather than native P. schreberi, whereas the results of this investigation point to the opposite. This difference in results originates from the differences in the levels of pollution of the investigated areas, with these being higher in Upper Silesia. The concentration of Cr, Pb and Zn in the transplants was higher than in the native ones in the less polluted sites (Fig. 3). Therefore, our results concerning the accumulation of Cr, Pb and Zn by P. schreberi from the less polluted sites were in agreement with Fernándèz et al. (2000) and Samecka-Cymerman and Kempers (2007). In addition, P. nutans, investigated by Samecka-Cymerman and Kempers (2007), is one of the most pollution-resistant moss species commonly colonising the surroundings of industrial plants (Huttunen, 2003). The transplants of this species probably survived better in the new, more polluted environmental conditions than P. schreberi, which was more sensitive to pollution (Salemaa et al. 2001). Rao (1982) describes cases where various species of terres-
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8
4
12
2 1
mg Cu kg-1
mg Cr kg-1
mg Cd kg-1
7 3
6 5 4
0
45
90
0
Day of exposure
6
2
90
45
Day of exposure
250
mg Zn kg-1
300
100 80 60 40 20
0
45
90
Day of exposure
120
mg Pb kg-1
8
4
3 2
10
200 150 100 50
0 90
45
0
0
45
90
Day of exposure
Day of exposure
Fig. 3. Concentration of Cd, Cr, Cu, Pb and Zn in Pleurozium schreberi after 0–45–90 d of exposure in: (1) native mosses from more (NMP) –d– and less (NLP) - d - polluted sites and (2) transplanted mosses from more (TMP) –s– and less (TLP) - s - polluted sites. The concentration of metals on day 0 in the transplanted Pleurozium schreberi is represented by the value in the moss at the control site from which the transplanted mosses were collected.
trial mosses block the uptake of the contaminants to which they are exposed, thus allowing them to survive in unfavourable surroundings. Shaw (1990) characterises bryophytes as plants with a tendency to accumulate metals and to develop a high degree of tolerance, but without finding evidence of local adaptation. Therefore, the author suggests that phenotypic plasticity is more important in the adaptation of bryophytes to extreme environments than it is in angiosperms, where genetic specialisation seems to be the rule (Shaw, 1990). Thus, if the ecological tolerance of individuals is sufficiently broad, genetic specialisation may not be necessary. In less polluted areas the native mosses were better accumulators of Cu than the transplants, whereas Cd was accumulated by the native and transplant mosses in equal amounts. It is probable that the well-known antagonisms between Cd–Zn, Cu–Zn and Pb–Cu influenced the accumulation of these elements in sites polluted with Zn and Pb (Kabata-Pendias, 2001). Throughout the exposure time, no significant differences were found in the metal bioconcentration of Cd, Cr, Cu Pb and Zn in the native mosses (Table 4), whereas in the transplanted mosses the differences were significant for all metals between 0–45–90 d of the experiment (post hoc LSD, P < 0.05). Accumulation of metals by the transplants increased much faster in the first 45 d of the
Table 4 Accumulation ratio day 45/0 and 90/45 for transplanted and native P. schreberi from more polluted (MP) and less polluted (LP) sites after 0–45–90 d of exposure. Element
Transplanted
Native
45/0
90/45
45/0
90/45
Cd
MP LP
4.3 3.7
1.1 1.0
1.0 1.0
1.0 1.0
Cr
MP LP
2.3 2.2
1.0 1.0
1.0 1.0
1.0 1.0
Cu
MP LP
2.7 2.4
1.0 1.1
1.1 1.0
1.0 1.0
Pb
MP LP
16 13
1.2 1.2
1.0 1.1
1.0 1.0
Zn
MP LP
4.3 3.5
1.0 1.1
1.0 1.0
1.0 1.1
experiment in comparison with the second period – from day 45 to 90 (Table 4). Accumulation was highest for Pb and Zn, with both elements having an extremely high concentration in the soils and mosses of the examined sites. In a similar experiment, Fernándèz and Carballeira (2001) also observed the highest level of bioconcentration in transplanted Scleropodium purum during the first 4 weeks, after which the accumulation tended to stabilise during the following 4 weeks, reaching a state of equilibrium for Cr and Cu. Similar results have been presented for the moss Rhytidiadelphus squarrosus by Brown and Beckett (1985) and for Hylocomium splendens by Brown and Brumelis (1996). These results suggest that the exposure period of 90 d in the present investigation was long enough to allow for a comparison of bioconcentration in transplanted and native P. schreberi. The question as to why native mosses accumulate relatively more of certain elements in extremely polluted areas needs further investigation. 4. Conclusions 1. The present study supports the statement that the deposition of Cr, Pb and Zn in the study area may be underestimated in biomonitoring studies involving native mosses in less polluted areas. 2. In the investigated areas of Upper Silesia classified as more polluted, the native moss was a better bioindicator than the transplanted P. schreberi of Cd, Cr, Cu, Pb and Zn pollution. 3. Bioindication of Cd by the native and transplanted P. schreberi in the less polluted Upper Silesia areas was comparable as a method of pollution control. 4. In the less polluted areas of Upper Silesia, the native P. schreberi was a better bioindicator of Cu than the transplanted P. schreberi, but the transplants were better bioindicators of Cr, Pb and Zn than the native ones.
References Aichele, D., Schwegler, H.W., 1984. Unsere Moss-und Farnpflanzen. Kosmos, Stuttgart.
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Appleton, J., Lee, K.M., Sawicka-Kapusta, K., Damek, M., Cookec, M., 2000. The heavy metal content of the teeth of the bank vole (Clethrionomys glareolus) as an exposure marker of environmental pollution in Poland. Environ. Pollut. 110, 441–449. Brown, D.H., Beckett, R.P., 1985. Intracellular and extracellular uptake of cadmium by the moss Rhytidiadelphus squarrosus. Ann. Bot. – London 55, 179–188. Brown, D.H., Brumelis, G., 1996. A biomonitoring method using the cellular distribution of metals in moss. Sci. Total Environ. 187, 153–161. Bykowszczenko, N., Baranowska-Bosiacka, I., Bosiacka, B., Kaczmarek, A., Chlubek, D., 2006. Determination of heavy metal concentration in mosses of Slowinski national park using atomic absorption spectrometry and neuron activation analysis methods. Pol. J. Environ. Stud. 15, 41–46. Cabala, J., Krupa, P., Misz-Kennan, M., 2009. Heavy metals in mycorrhizal rhizospheres contaminated By Zn–Pb mining and smelting around Olkusz in Southern Poland. Water, Air, Soil Pollut. 199, 139–149. Fernándèz, J.A., Carballeira, A., 2001. A comparison of indigenous mosses and topsoils for use in monitoring atmospheric heavy metal deposition in Galicia (northwest Spain). Environ. Pollut. 114, 431–441. Fernándèz, J.A., Rey, A., Carballeira, A., 2000. Differences in the responses of native and transplanted mosses to atmospheric pollution: a possible role of selenium. Environ. Pollut. 110, 73–78. Guschina, I.A., Harwood, J.L., 2002. Lipid metabolism in the moss Rhytidiadelphus squarrosus (Hedw.) Warnst. from lead-contaminated and non-contaminated populations. J. Exp. Bot. 53, 455–463. Huttunen, S., 2003. Reproduction of the moss Pleurozium schreberi and Pohlia nutans in the surroundings of copper smelters at Harjavalta, SW Finland. J. Bryol. 25, 41–47. Kabata-Pendias, A., 2001. Trace Elements in Soils and Plants. CRC Press, Boca Raton, London, New York, Washington DC. 413 pp. Kłos, A., Rajfur, M., Wacławek, M., Wacławek, W., Wuenschmann, S., Markert, B., 2010. Quantitative relations between different concentrations of micro- and macroelements in mosses and lichens: the region of Opole (Poland) as an environmental interface in between Eastern and Western Europe. Int. J. Environ. Health 4 (2/3), 98–119. Kozanecka, T., Chojnicki, J., Kwasowski, W., 2002. Content of heavy metals in plant from pollution-free regions. Pol. J. Environ. Stud. 11, 395–399. Küpper, H., Küpper, F., Spiller, M., 1996. Environmental relevance of heavy metalsubstituted chlorophylls using the example of water plants. J. Exp. Bot. 47, 259– 266. Lajunen, L.H.J., Perämäki, P., 2004. Spectrochemical Analysis by Atomic Absorption and Emission. Royal Society of Chemistry, Cambridge, UK. Lopez, J., Retuerto, R., Carballeira, A., 1997. D665/D665a index vs. frequencies as indicators of bryophyte response to physicochemical gradients. Ecology 78, 261–271. Markert, B., Breure, A., Zechmeister, H., 2003. Bioindicators & Biomonitors – Principles, Concepts and Applications. Elsevier, Amsterdam, New York, Tokyo. Markert, B., Herpin, U., Siewers, U., Berlekamp, J., Lieth, H., 1996. The German heavy metal survey by means of mosses. Sci. Total Environ. 182, 159–168. Matusiewicz, H., 2003. Wet digestion methods. In: Mester, Z., Sturgeon, R. (Eds.), Sample Preparation for Trace Element Analysis, Comprehensive Analytical Chemistry, vol. 41. Elsevier, Amsterdam, pp. 193–233.
Rao, D.N., 1982. Responses of bryophytes to air pollution. In: Smith, A.J.E. (Ed.), Bryophyte Ecology. Chapman and Hall, London, pp. 445–471. Rühling, Å., Tyler, G., 1968. An ecological approach to the lead problem. Bot. Notiser 121, 321–342. Salemaa, M., Vanha-Majamaa, I., Derome, J., 2001. Understorey vegetation along a heavy-metal pollution gradient in SW Finland. Environ. Pollut. 112, 339–350. Samecka-Cymerman, A., Kosior, G., Kempers, A.J., 2006. Comparison of the moss Pleurozium schreberi with needles and bark of Pinus sylvestris as biomonitors of pollution by industry in Stalowa Wola (southeast Poland). Ecotoxicol. Environ. Saf. 65, 108–117. Samecka-Cymerman, A., Kempers, A.J., 2007. Differences in concentration of heavy metals between native and transplanted Pohlia nutans (Hedw.) Lindb. – a case study from a dump exposed to industrial emissions in Poland. Pol. J. Environ. Stud. 16, 251–258. Shaw, A.J., 1990. Metal tolerance in bryophytes. In: Shaw, A.J. (Ed.), Heavy Metal Tolerance in Plants: Evolutionary Aspects. CRC Press Inc., Boca Raton, pp. 133– 152. Shaw, A.J., 1994. Adaptation to metals in widespread and endemic plants. Environ. Health Perspect. 102 (Suppl. 12), 105–108. Sokal, R.R., Rohlf, F.J., 2003. Biometry. The principles and practice of statistics in biological research. Freeman and Company, New York. Szarek-Łukaszewska, G., Grodzin´ska, K., Braniewski, S., 2002. Heavy metal concentration in the moss Pleurozium schreberi in the Niepołomice forest, POLAND: changes during 20 years. Environ. Monit. Assess. 79, 231–237. StatSoft, Inc., 2008. STATISTICA (data analysis software system), version 8.0.
. Tyler, G., 1990. Bryophytes and heavy metals: a literature review. Bot. J. Linn. Soc. 104, 231–253. UNECE, 2003. In: Buse, A., Norris, D., Harmens, H., Buker, P., Ashenden, T., Mills, G. (compilers), Heavy metals in European Mosses 2000/2001 survey. UNECE ICP Vegetation. Center for Ecology and Hydrology, Bangor University of Wales Bangor, UK. Vázquez, M.D., López, J., Carballeira, A., 1999. Uptake of heavy metals to the extracellular and intracellular compartments in three species of aquatic bryophyte. Ecotoxicol. Environ. Saf. 44, 12–24. Wcisło, E., Dutkiewicz, T., Konczalik, J., 2002. Indicator-based assessment of environmental hazards and health effects in the industrial cities of Upper Silesia, Poland. Environ. Health Perspect. 110, 1133–1140. Wells, J.M., Brown, D.H., 1995. Cadmium tolerance in a metal-contaminated population of the grassland moss Rhytidiadelphus squarrosus. Ann. Bot. – London 75, 21–29. Zar, H., 1999. Biostatistical Analysis. Prentice Hall, Upper Saddle River, New Jersey. Zechmeister, H.G., Hohenwallner, D., Riss, A., Hanus-Illnar, A., 2003. Variations in heavy metal concentrations in the moss species Abietinella abietina (Hedw.) Fleisch. according to sampling time, within site variability and increase in biomass. Sci. Total Environ. 301, 55–65.