Evaluation of the impact of reducing national emissions of SO2 and metals in Poland on background pollution using a bioindication method

Abstract

Changes in environmental pollution by S, Cd, Cu, Pb and Zn in 2006–2014 were evaluated using a bioindication method. This method was based on measurements of pollutants in Scots pine (Pinus sylvestris L.) needles. The measurements were performed in the Chojnowskie Forests, a region recognized as a background area for central Poland. The changes in the contents of sulfur (S) and metals in needles were not comparable with the changes in the global emissions of the pollutants in Poland. On average, the pollution level in the study area decreased by 9.9% for S, 61.4% for Pb, 22.5% for Cd, 11.7% for Zn and 10.4% for Cu. During the same period, global emissions in Poland decreased by 38.1% for S, 8.0% for Pb, 63.2% for Cd, 11.7% for Zn and 14.0% for Cu. Therefore, the differences in the changes in emissions and the needle contents of each element should be examined separately which was not a goal of this study. However, the discrepancy between these results did not prevent the use of bioindication methods. Evaluation of pollutant contents in plants reflected their incorporation in biological processes rather than air or soil pollution levels.

About the Authors:

Wojciech Dmuchowski

Roles Conceptualization, Data curation, Investigation, Methodology, Validation, Writing – original draft, Writing – review & editing

* E-mail: [email protected]

Affiliations Warsaw University of Life Sciences–SGGW, Nowoursynowska, Warsaw, Poland, Polish Academy of Sciences Botanical Garden–Center for Conservation of Biological Diversity, Warsaw, Poland

ORCID http://orcid.org/0000-0003-0092-365X

Dariusz Gozdowski

Roles Data curation, Project administration

Affiliation: Warsaw University of Life Sciences–SGGW, Nowoursynowska, Warsaw, Poland

Aneta H. Baczewska-Dąbrowska

Roles Investigation, Methodology, Writing – original draft, Writing – review & editing

Affiliation: Polish Academy of Sciences Botanical Garden–Center for Conservation of Biological Diversity, Warsaw, Poland

Piotr Dąbrowski

Roles Investigation, Methodology, Writing – original draft

Affiliation: Warsaw University of Life Sciences–SGGW, Nowoursynowska, Warsaw, Poland

Barbara Gworek

Roles Writing – review & editing

Affiliation: Warsaw University of Life Sciences–SGGW, Nowoursynowska, Warsaw, Poland

Irena Suwara

Roles Data curation, Methodology, Writing – original draft

Affiliation: Warsaw University of Life Sciences–SGGW, Nowoursynowska, Warsaw, Poland

Introduction

Bioindication methods offer an opportunity for significant intensification of studies on air pollution, especially on the content of trace elements. Biomonitoring in a general sense can be defined as the use of plants and animals with the objective of gaining quantitative and qualitative information on certain characteristics of the biosphere [1–4].

Measurement of contaminant accumulation in Scots pine needles has been used as a biomonitoring method for entire countries, industrial regions, administrative units and single emission sources (Table 1) [5–86]. Measurement of sulfur and heavy metal concentration levels in Scots pine needles gained a recommendation from the United Nations Environment Program as a standard method for the assessment of environmental contamination [87].

[Figure omitted. See PDF.]

Table 1. A summary of some relevant literature concerning of the use Scots pine needles in the biomonitoring of environmental pollution.

https://doi.org/10.1371/journal.pone.0192711.t001

In Poland, measurements of air pollution via the measurement-and-control approach are mainly conducted in cities within the framework of the State Environmental Monitoring. In agro-forest areas, the number of measuring points is negligible. Application of bioindication methods provides the possibility of a significant intensification of studies into environmental pollution.

Sulfur dioxide air pollution is considered one of the main causes of forest decline in the northern hemisphere [5,88–91]. Several studies have shown that the sulfur content in Scots pine needles is correlated with the concentration of SO₂ in the air [18–19,24,92].

The needles of Scots pine have been used to detect the deposition, accumulation and distribution of heavy metal pollution. Although it is often difficult to determine the sources of the heavy metals [93], trees can be used as effective biomonitors for detecting low concentrations of pollutants of both soil and atmospheric origin.

Trees are not the best indicators for monitoring air pollution when compared to lower plants (lichens or mosses) [94,95]. However, their one great advantage is that they are long-lived, so that a repetition of the investigation is possible after a few decades, as was conducted by Ballach and Wittig [96]. Thus, trees can be sampled systematically with standardized sampling and analytical techniques for comparative monitoring of the time-trend distribution of trace elements [97]. In addition, trees are usually easier to identify than lower plants [98]. They provide useful data for the design of international networks for deposition monitoring, and they greatly facilitate the analytical determination of trace elements.

Sulfur is emitted into the atmosphere mainly as sulfur dioxide (SO₂). Emissions of dimethyl sulfide (H₂S) are of marginal significance. The major anthropogenic source of sulfur dioxide emissions is the sulfur content of fossil fuels released by combustion, mainly hard coal and lignite. In addition, some sulfur is produced in petroleum refining, the smelting of sulfidic ores in the production of heavy metals, and the production of sulfuric acid, paper and sulfur. Natural fluxes of sulfur originate from volcanoes and from the biological and photochemical production in the oceans of volatile sulfur gases, notably dimethyl sulfide. Comparatively small amounts of sulfur are also emitted from forest fires, soils and vegetation, sulfur springs and sea salt. Emissions from natural sources are negligible outside those areas near active volcanoes [99–100].

Global sulfur dioxide emissions increased from 2,447 Gg in 1850 to 115,507 Gg in 2005. This emissions growth was observed in every region of the world up to the 1970s–1980s. Subsequently, there has been a substantial decrease in emissions in western Europe, the USA, Canada and Japan. In eastern Europe, a decrease in emissions has been recorded, starting in 1990–2000; emissions decreased in China and Russia, starting in 2005. Only in India, which has a significant share of global emissions, are emission levels still rising. The fall in global emissions started in 2005 [100–102].

In 2014 in the European Union (EU), the production of energy constituted 91% of overall SO₂ emissions [103]. These overall emissions dropped by 81.6%: from 16.800 Gg in 1995 to 3.083 Gg in 2014 (Table 2). In Poland, the emissions fell by 65.2%: from 2.300 Gg in 1995 to 800 Gg in 2014. The emissions of SO₂ in Poland constituted 11.9% of the overall EU emissions in 1990, and 26.0% in 2014, meaning that Poland was the highest emitter of SO₂ in the EU. The second heaviest polluter, Germany, emits less than half as much [103]. The reason for such a high share in emissions for Poland (Table 3) is the use of coal as the main energy source. Coal contributes to more than 82% of overall energy production, while the share of renewable energy amounts to only 12%. In the years 1995–2014, the consumption of coal decreased by only 19.0% [104–105`].

[Figure omitted. See PDF.]

Table 2. Decrease in SO₂ and metals emissions in the European Union (EU-28) and Poland in the years 1995–2014 [103].

https://doi.org/10.1371/journal.pone.0192711.t002

[Figure omitted. See PDF.]

Table 3. Coal consumption for energy purposes in Poland in the years 1995–2014 [104,105].

https://doi.org/10.1371/journal.pone.0192711.t003

Contamination of the environment with heavy metals is primarily related to human activities. The sources of emissions are coal fuels (power stations, boiler houses, households), industry (especially metallurgy), transport and the use of sewage drift, some mineral fertilizers and pesticides in agriculture and horticulture, and improper waste storage [105–107]. In the EU, fuel combustion contributed to 72% of Cd and 61% of Pb emissions. The overall emissions of Cd, Pb and Zn in the EU fell significantly between 1995 and 2014, by 59.2% for Cd, 82.5% for Pb and 34.1% for Zn. The reductions were smaller in Poland: 48.1% for Cd, 14.5% for Pb and 23.2% for Zn. Cu emissions in Europe were close to a constant level. Poland is the largest source of Cd (22.2%) and Pb (26.9%) in the EU and the second largest source of Cu (9.1%) and Zn (20.0%) [103].

The aims of the study were as follows:

* to determine the background pollution by SO₂ and heavy metals in central Poland using bioindication methods

* to evaluate the impact of changes in overall country emissions on environmental pollution expressed as the accumulation of pollutants in plants.

Study area

The Chojnowskie Forests have an area of 10 200 ha and are characterized by a rather high forest density. Mixed fresh coniferous forest with a predominance of pine constitutes the majority of the habitat at 74.1%, with 9.1% oak and 8.6% birch [108]. The forests are located in central Poland beyond the direct impact of large stationary pollution emitters. The air quality of the Chojnowskie Forests is influenced by the city (Warsaw). However, there are no large industrial emitters in the city. The sources of air pollution in the Chojnowskie Forests are large hard coal-fired power stations: 3 combined heat and power stations in Warsaw (total 4266 MW, located approximately 30 km northeast of the Chojnowskie Forests), Kozienice Power Station (2905 MW) 48 km southeast, and the lignite-fired Bełchatów Power Station (5420 MW) situated approximately 148 km southwest of the Chojnowskie Forests. The flue gases of these plants are emitted into the atmosphere through stacks whose heights are 200–300 m. The air pollution levels of the Chojnowskie Forests can be regarded as background air pollution for central Poland [21]. The locations of the study area and sampling points are presented in Fig 1.

[Figure omitted. See PDF.]

Fig 1. Map of Poland indicating geographical features discussed in the article and the study area.

https://doi.org/10.1371/journal.pone.0192711.g001

The study was carried out on state land which belong to State Forests (Poland). We have obtained the respective agreement from regional office of State Forests for sampling collection in study area (Chojnowskie Forest).

We confirm that the field studies did not involve endangered or protected species.

Materials and methods

The highest possible standardization of all activities involved in the study was applied; this is necessary to obtain comparable results using bioindication [109]. The Scots pine needles used for the analyses were collected in the second half of March in the years 2006 and 2014 according to the methodology presented by Dmuchowski and Bytnerowicz [21]. In the first year, needles were collected from 15–25-year-old trees, the same trees in both years of the study, from the 2^nd to 4^th whorl from the top by cutting branches from the outer parts of the canopy. The needles were collected from eight trees growing side by side. From the collected needles, a collection sample was created from each location, taking 40 g from each tree. Only the needles from previous year's growth were used. Total samples from 31 locations were collected. The materials collected were placed in linen bags and dried at 70°C. The dried materials were pulverized in a stainless-steel impact mill (Fritsch 14702) and stored in tightly sealed plastic containers until the time of analysis. Needles were washed for one minute in distilled water before being dried and pulverized. The powdered samples were dry-mineralized in a muffle oven (Naberthern L40/11/P320) using the following time/temperature procedure: 120°C/2 h, 200°C/1 h, 300°C/1 h, and 450°/5 h. The ashes were digested in 30% HCl (Merck Suprapur) and filtered through filter paper [110].

The analyses were performed via flame AAS (Perkin Elmer 1100A) corrected to deuterium background correction using hollow cathode lamps (HCl) and acetylene burners [111]. Three identical subsamples of each sample were processed. Three blanks were run with each batch of samples; thus, each sample was blank-corrected. Total sulfur content was determined using a LECO 132 apparatus [112].

To provide quality control (QC), the elemental content in the plant samples was determined using certified reference materials (Table 4). The obtained results were in close agreement with the certified values. The recovery range was from 94.7% to 106.0%.

[Figure omitted. See PDF.]

Table 4. Comparisons of measured and certified concentrations of elements in certified materials.

https://doi.org/10.1371/journal.pone.0192711.t004

Results and discussion

All results for element content and comparisons with other studies concern Scots pine needles from the previous year. The results for metal and SO₂ content in needles are presented in Table 5 and on the maps with isolines (Fig 2). The distribution and values of isolines suggest a significant decrease in pollution in 2006–2014 for all studied elements. The higher level of pollution in the northern region of the Chojnowskie Forests indicates the influence of the emissions in the Warsaw area. For almost all elements presented in Table 5, the mean content was significantly lower in 2014 than in 2006. Only for the Cu levels was the difference not significant (P > 0.05). The highest relative variability of the content of elements was observed for Pb (high standard deviation in relation to the mean). The lowest variability was observed for S and Cu. The strongest relationship between pairs of elements (Table 6) was observed for Pb and Zn in 2006, which means that these elements are pollutants that almost always spread together in the air. Very strong relationships were also observed between Cd and S, Pb, and Zn in 2006. In 2014, the relationships were quite strong, but weaker in comparison with the year 2006. The strongest relationship between the content of an element in 2006 and the content of an element in 2014 was observed for sulfur (Table 7). This means that a similar spatial pattern of pollution was observed for the sulfur content. The weakest relationship was observed for the Cu content, i.e. that the spatial distribution of the Cu content was different in 2006 and in 2014.

[Figure omitted. See PDF.]

Fig 2. Contamination of the environment with S and metals based on the accumulated concentration of this element in the Scots pine needles in the years 2006 and 2014.

https://doi.org/10.1371/journal.pone.0192711.g002

[Figure omitted. See PDF.]

Table 5. Sulfur content (%) and metals (mg kg^-1) in Scots pine needles–descriptive statistics.

https://doi.org/10.1371/journal.pone.0192711.t005

[Figure omitted. See PDF.]

Table 6. Spearman’s rank correlation coefficients between the contents of elements in Scots pine needles.

https://doi.org/10.1371/journal.pone.0192711.t006

[Figure omitted. See PDF.]

Table 7. Spearman’s rank correlation coefficients between the contents of the same elements in Scots pine needles in two years (2006 vs. 2014).

https://doi.org/10.1371/journal.pone.0192711.t007

The content of S and metals in needles is affected by air pollution associated with the transport of pollutants from distant and local emission sources, and soil pollution from current and historical deposition. Important is also the different availability of the tested elements from the soil and air.

In 2006, the sulfur content in the needles ranged from 0.112% to 0.159%, with an average of 0.133%. In 2014, the content was approximately 9.9% lower (average 0.120%, range 0.101%–0.137%). The positive correlation between the sulfur content in needles and the concentration of SO₂ in the air has been known for many years [18,21,24,113]. The level of S is determined by its level in the air and not in the soil. The study area can be recognized as a background area for central Poland [21]. At the beginning of the 1980s in the Białowieża Primeval Forest, the least polluted region in northeastern Poland, the sulfur content in needles ranged from 0.088% to 0.091%, compared to 0.091% to 0.120% in central Poland, while at the same time it averaged 0.071% in Lapland in northern Finland [13,21]. In 2002, the background level amounted to 0.087% in northeastern Poland and 0.109% in central Poland [51]. In a background pollution region in Lapland, the sulfur content in needles was measured to be 0.066% in 2001 and 0.063% in 2007 [67]. Significantly lower levels, ranging from 0.030% to 0.033%, were observed in the Baikal region in Siberia in 2010 [58]. The sulfur content in needles is significantly higher in industrial regions with high SO₂ emissions, e.g. 0.320% in Finland in 1976–1978 [10] and 0.201% in the Upper Silesian Industrial Region in Poland in 1982 [13], as well as 0.212% in 1991 [25].

The total SO₂ emissions in Poland decreased by 38.1% in the years 2006–2014 [103], along with a fall in the needle sulfur content by 9.9% (Fig 3). The reduction of sulfur emissions did not correspond with a change in coal consumption, the combustion of which is the main source of SO₂ pollution in the air. Rather, it was a result of the installation of gas desulfurization equipment in some power stations. In 2006, only 61% of SO₂ was retained and neutralized in these devices, while in 2014 this figure was 81.0% [104–105]. The smaller drop in the sulfur content in Scots pine needles compared to the reduction of emissions could have been caused by low local emissions from stoves without filtration devices.

[Figure omitted. See PDF.]

Fig 3. Changes in coal consumption for energy purposes, SO₂ and metals emissions in Poland and contents of elements in Scots pine needles in the years 2006–2014.

https://doi.org/10.1371/journal.pone.0192711.g003

The average Cd content in pine needles in the research area was 0.23 mg kg^-1 (0.15–0.33 mg kg^-1) in 2006, and this decreased to 0.18 mg kg^-1 (0.08–0.30 mg kg^-1) in 2014 (a 22.5% reduction). In 1982, needles in the Lapland area contained 0.17 mg kg^-1 Cd, while in the Białowieża Primeval Forest, the least polluted region of Poland, it was 0.22 mg kg^-1 in 1990 and 0.12 mg kg^-1 in 2005 [13,59]. In the years 1984–1988 in Norway in a background pollution region, pine needles contained 0.27 mg kg^-1 Cd [72]. The level of Cd was 0.63 mg kg^-1 in Slovakia in 1979 [9]. In 2005, in a high-pollution area in Poland near a Pb-Zn smelter, the Cd content in needles reached 5.78 mg kg^-1 [59] and 2.4 mg kg^-1 in 2014 [82].

In the period 2006–2014, Cd emissions in Poland decreased by 63.2% in spite of a reduction of coal combustion of 3.8% (coal is the main Cd emission source) [103]. The Cd content in needles fell by 22.5% and thus this did not have a direct connection with changes in Cd emissions or in the coal consumption rate. The content of Cd in needles is affected not only by pollution from current emissions, but also by historical deposition into the soil. Cd emissions and coal consumption in Poland in the years preceding the study were larger. The mean Pb content in needles in the Chojnowskie Forests was 2.66 mg kg^-1 in 2006 (range 1.30–4.70 mg kg^-1) and this fell to 1.03 mg kg^-1 in 2014 (range 0.29–2.24 mg kg^-1). Earlier in Poland in the area with the least background pollution, pine needles contained significantly higher amounts of Pb: 10.8 mg kg^-1 in 1982 [13] and 1.29 mg kg^-1 in 1992 [21]. Background pollution in Slovakia was 5.4 mg kg^-1 in 1980 [9], and in southern Norway it was 4.0 mg kg^-1 in 1982, and 1.1 mg kg^-1 in 1992 [72]. The mean needle content of Pb was significantly higher in highly polluted regions. In the Upper Silesian Industrial Region in Poland, needles contained 54.8 mg kg^-1 Pb in 1982 [13] and 10.1 mg kg^-1 in 1992 [21]. In the Warsaw Steelworks region, the mean Pb content was 19.2 mg kg^-1 in 1991 and, in the proximity of a Pb-Zn smelter in Olkusz, it reached 255 mg kg^-1 at its peak in 1991 [25]. In the proximity of a Cu-Ni smelter in Lapland, needles had 9.3 mg kg^-1 of Pb content in 1991 [30], while in Erzurum in Turkey, it was 29.0 mg kg^-1 on average.

The Pb content in needles in the Chojnowskie Forests decreased by 63.2% on average in the period 2006–2014. The reduction of total Pb emissions in Poland in this period was only 8.0% [103]. The Pb content in the needles is influenced by the Pb content in the soil and the direct inflow from the air. The availability of Pb from the soil increases with the lowering of pH. Soils in coniferous forests in Poland are naturally acidic. Hovmand et al.'s [114] research showed little root uptake of Pb compared to Pb absorbed by the needles from atmospheric deposition. This tendency has also been confirmed in research on other plants [115–118]. Such a high decrease in pollution at the studied sites could be a result of the elimination of leaded gasoline in 2000 [21], which was a decisive factor in local pollution levels. The relatively low decrease in overall Pb emissions was caused by changes in coal combustion, which was reduced by only 3.8% [104–105].

Zinc, unlike the abovementioned metals, is a common element in human and natural environments and plays multiple roles in living organisms. In the study area, the mean Zn content in needles was 55.9 mg kg^-1 in 2006 (range 40.0–97.0 mg kg^-1) and this dropped to 45.7 mg kg^-1 in 2014 (range 24.7–66.2 mg kg^-1), i.e. by 18.3%. The background Zn level in needles in northeastern Poland was 51 mg kg^-1 in 1992 [21] and this fell to 34.0 mg kg^-1 in 2005 [64]. Similar Zn levels were observed in needles in Lapland in 1982 (45 mg kg^-1) [13]. In 1982, in southern Norway the background content was higher than in Poland and amounted to 75 mg kg^-1 on average (range 56–99 mg kg^-1) [72]. The needle Zn content was significantly higher in polluted environments. In the Upper Silesian Industrial Region in Poland, needles contained 164 mg kg^-1 Zn in 1982 and 174 mg kg^-1 in 1992 [13,21]. The highest Zn needle contents were found near a Pb-Zn smelter in Olkusz, reaching 548 mg kg-1 [64]. A very high Zn content was also observed in the proximity of an Ni smelter in Lapland in 2000, ranging from 319–1010 mg kg-1 Zn [33]. In the period 2006–2014, global Zn emissions in Poland decreased by 11.7%, and there was a decline in Zn needle content of 18.3%.

Investigation into the Cu content in Scots pine needles is not recognized as a good bioindication method for measuring environmental pollution, because an excessive accumulation of Cu in roots and transport of Cu to upper parts of trees may occur when the demand for this element emerges [21,119]. The Cu content in needles in the Chojnowskie Forests ranged from 2.53 to 2.82 mg kg-1 and this was at the same level as the background content in the preceding years in the Białowieża Primeval Forest in Poland, as well as in Slovakia, in southwestern Finland and in Lapland [9,13,22]. The needle Cu content was at a level that is typical for plants [120].

Conclusion

Environmental pollution by sulfur and metals in the Chojnowskie Forests, except for the northern part, mean that it can be recognized as a background area for central Poland. In the northern part, there has been a noticeable influence of pollution from the Warsaw area.

The changes in the contents of the analyzed elements in Scots pine needles in the period 2006–2014 (in the previous year’s needles) in the Chojnowskie Forests can be arranged in a decreasing series:

The changes in the total emission of SO₂ and metals in Poland can be arranged as follows:

The changes in Scots pine needle pollution content from sulfur and heavy metals were not compatible with the levels of changes in global emissions in Poland. The causes of this result could include the availability of the emitted pollution forms for plants, the spread of contamination at short distances from emission sources, historical environmental contamination in the study area, the ability of plants to take up nutrients from soil and the biological fixation in soil of inactive forms.

The changes in emissions of each element should be considered separately. The highest decrease in pollution in needles was found for Pb (61.4%), much greater than the reduction of the global emissions (8.0%). The reason for this could be soil pollution depletion derived from historical emissions from leaded gasoline. The lack of compatibility of emissions and contents in plants does not disprove bioindication methods. The estimation of pollution levels in plants reflects their incorporation in biological processes rather than air or soil pollution levels.

Coal combustion is the main source of emissions of sulfur and other studied elements. In 2006–2014, a 3.8% decrease in coal consumption was observed. This was significantly lower than the reduction in emissions. This is probably the result of the installation of gas desulfurization technologies in power stations and higher levels of reduction of pollutant emissions in neighboring countries and thus the reduction of pollution from cross-border transport.

Citation: Dmuchowski W, Gozdowski D, Baczewska-Dąbrowska AH, Dąbrowski P, Gworek B, Suwara I (2018) Evaluation of the impact of reducing national emissions of SO2 and metals in Poland on background pollution using a bioindication method. PLoS ONE 13(2): e0192711. https://doi.org/10.1371/journal.pone.0192711

References

1. Wolterbeek B. Biomonitoring of trace element air pollution: principles, possibilities and perspectives, Environ. Pollut. 2002; 120:11–12. pmid:12199457

2. Markert B. Definitions and principles for bioindication and biomonitoring of trace metals in the environment, J Trace Elem. Med. Biol. 2007; 21:77–82.

3. Heink U, Kowarik I. What are indicators? On the definition of indicators in ecology and environmental planning, Ecol. Indic. 2010; 10:584–593.

4. Forbes PB, van der Wat L, Kroukamp EM. Biomonitors, Comprehensive Analytical Chemistry 2015; 70:53–108.

5. Farrar JF, Relton AJ, Rutter AJ. Sulphur dioxide and the scarcity of Pinus sylvestris in the industrial Pennines. Environ. Pollut. 1970; 14:63–68.

6. Grodzinska K. Changes in the Forest Environment in Southern Poland as a Result of Steel Mill Emission. In: Miyawaki A, Tüxen R, editors, Vegetation Science and Environmental Protection. Tokyo: Maruzen Co., Ltd.; 1977, pp. 207–215.

7. Malcolm DC., Garforth MF. The sulphur: nitrogen ratio of conifer foliage in relation to atmospheric pollution with sulphur dioxide. Plant Soil 1977; 47:89–102.

8. Laaksovirta K, Olkkonen H. Effect of air pollution on epiphytic lichen vegetation and element contents of a lichen and pine needles at Valkeakoski, S Finland. Ann. Bot. Fenn. 1979; 16:285–296.

9. Maňkowska B. The natural content of F, Pb and Cd in the forest trees. Biólogia (Bratislava) 1980; 35:267–274.

10. Lehtiö H, Juutilainen J, Jantunen M. Visible injuries and sulphur contents of the needles of Pinus sylvestris and Picea abies in the city of Kuopio and around two factories in central Finland. in: Ann. Bot. Fenn. 1980; 17:1–6.

11. Soikkeli S. Comparison of cytological injuries in conifer needles from several polluted industrial environments in Finland. Ann. Bot. Fenn. 1981; 18:47–61.

12. Niemtur S. The content of Zn, Pb, Cd, Fe, Mg, Ca and K in the needles of Scots pine various families growth in the experimental areas near the zinc smelter. Arch. Environ. Prot. 1981; 2–4:17–28.

13. Molski B, Dmuchowski W. The Comparison of Environmental Pollution in Northern Finland near Kevo and in Poland with the use of Pinus silvestris L. as bioindicator. Rep. Kevo Subarctic Res. Stat. 1990; 21:27–30.

14. Vilkka L, Aula I, Nuorteva P. Comparison of the levels of some metals in roots and needles of Pinus sylvestris in urban and rural environments at two times in the growing season. Ann. Bot. Fenn. 1990; 27:53–57.

15. Manninen S, Huttunen S, Torvela H. Needle and lichen sulphur analyses on two industrial gradients. Water Air Soil Pollut. 1991; 59:153–163.

16. Polle A, Eiblmeier M, Rennenberg H. Sulphate and antioxidants in needles of Scots pine (Pinus sylvestris L.) from three SO2‐polluted field sites in eastern Germany. New Phytol. 1994; 127:571–577.

17. Lumme I, Arkhipov V, Kettunen I. Deposition gradients and foliar and soil leachate concentrations of air pollutants in Scots pine stands of S.-E. Finland and the Karelian Isthmus, N.-W. Russia. Water Air Soil Pollut. 1995; 85:1263–1268.

18. Innes JL. Influence of air pollution on the foliar nutrition of conifers in Great Britain. Environ. Pollut. 1995; 88:183–192. pmid:15091559

19. Raitio H, Tuovinen JP, Anttila P. Relation between sulphur concentrations in the Scots pine needles and the air in northernmost Europe. Water Air Soil Pollut. 1995; 85:1361–1366.

20. Palomäki V, Raitio H. Chemical composition and ultrastructural changes in Scots pine needles in a forest decline area in southwestern Finland. Trees 1995; 9:311–317.

21. Dmuchowski W, Bytnerowicz A. Biomonitoring of the environmental pollution in Poland using chemical analysis of Scots pine (Pinus silvestris L.) needles. Environ. Pollut. 1995; 87:87–104. pmid:15091612

22. Helmisaari HS, Derome J, Fritze H, Nieminen T, Palmgren K, Salemaa M, et al. Copper in Scots pine forests around a heavy-metal smelter in south-western Finland. Water Air Soil Pollut. 1995; 85:1727–1732.

23. Poikolainen J. Sulphur and heavy metal concentrations in Scots pine bark in northern Finland and the Kola Peninsula. Water Air Soil Pollut. 1997; 93:395–408.

24. Manninen S, Huttunen S, Kontio M. Accumulation of sulphur in and on Scots pine needles in the subarctic. Water Air Soil Pollut. 1997; 95:147–164.

25. Kurczyńska EU, Dmuchowski W, Włoch W, Bytnerowicz A. The influence of air pollution on needles and stems of Scots pine (Pinus silvestris L.) trees. Environ. Pollut. 1997; 98:325–334.

26. Giertych MJ, Temmerman LO, Rachwal L. Distribution of elements along the length of Scots pine needles in a heavily polluted and a control environment. Tree Physiol. 1997;17:697–703. pmid:14759894

27. Migaszewski ZM, Geochemistry of soils and vegetation of the Holy Cross Mts. between 1994 and 1996. Geol. Quart. 1998; 42:99–112.

28. Rautio P, Huttunen S, Lamppu J. Seasonal foliar chemistry of northern Scots pines under sulphur and heavy metal pollution. Chemosphere 1998; 37:271–287.

29. Oleksyn J, Karolewski P, Chalupka W, Reich PB, Tjoelker MG. Nutritional status of pollen and needles of diverse Pinus sylvestris populations grown at sites with contrasting pollution. Water Air Soil Pollut. 1999; 110:195–212.

30. Steinnes E, Lukina N, Nikonov V, Aamlid D, Røyset O. A gradient study of 34 elements in the vicinity of a copper-nickel smelter in the Kola Peninsula. Environ. Monit. Assess. 2000; 60:71–88.

31. Karolewski P, Siepak J, Gramowska H. Response of Scots pine (Pinus sylvestris), Norway spruce (Picea abies) and Douglas fir (Pseudotsuga menziesii) needles to environment pollution with flourine compounds. Dendrobiology 2000; 45:41–46.

32. Manninen S, Huttunen S. Response of needle sulphur and nitrogen concentrations of Scots pine versus Norway spruce to SO2 and NO2. Environ. Pollut. 2000; 107:421–436. pmid:15092988

33. Koptsik GN, Koptsik SV, Aamlid D. Pine needle chemistry near a large point SO2 source in northern Fennoscandia. Water Air Soil Pollut. 2001; 130:929–934.

34. Reimann C, Koller F, Kashulina G, Niskavaara H, Englmaier P. Influence of extreme pollution on the inorganic chemical composition of some plants. Environ. Pollut. 2001; 115:239–252. pmid:11706797

35. Pöykiö R, Torvela H. Pine needles (Pinus sylvestris) as a bioindicator of sulphur and heavy metal deposition in the area around a pulp and paper mill complex at Kemi, northern Finland. Int. J. Environ. Anal. Chem. 2001; 79:143–154.

36. Ayodele JT, Ahmed A. Monitoring air pollution in Kano municipality by chemical analysis of Scots Pine (Pinus sylvestris L.) needles for sulphur content. Environmentalist 2001; 21:145–151.

37. Migaszewski ZM, Gałuszka A, Pasławski P. Polynuclear aromatic hydrocarbons, phenols, and trace metals in selected soil profiles and plant bioindicators in the Holy Cross Mountains, South-Central Poland. Environ. Int. 2002; 28:303–313. pmid:12220117

38. Penuelas J., Filella I. Metal pollution in Spanish terrestrial ecosystems during the twentieth century. Chemosphere 2002; 46: 501–505. pmid:11838427

39. Lamppu J., Huttunen S. Relations between Scots pine needle element concentrations and decreased needle longevity along pollution gradients. Environ. Pollut. 2003; 122: 119–126. pmid:12535600

40. Schulz H, Härtling S. Vitality analysis of Scots pines using a multivariate approach. For. Ecol. Manage. 2003; 186:73–84.

41. Yilmaz S, Zengin M. Monitoring environmental pollution in Erzurum by chemical analysis of Scots pine (Pinus sylvestris L.) needles. Environ. Int. 2004; 29:1041–1047. pmid:14680886

42. Nieminen TM, Derome J, Saarsalmi A. The applicability of needle chemistry for diagnosing heavy metal toxicity to trees. Water Air Soil Pollut. 2004; 157:269–279.

43. Karolewski P, Giertych MJ, Oleksyn J, Żytkowiak R. Differential reaction of Pinus sylvestris, Quercus robur and Q. petraea trees to nitrogen and sulfur pollution. Water Air Soil Pollut. 2005; 160:95–108.

44. Luyssaert S, Sulkava M, Raitio H, Hollmén J. Are N and S deposition altering the mineral composition of Norway spruce and Scots pine needles in Finland? Environ. Pollut. 2005; 138:5–17. pmid:15967552

45. Thiry Y, Schmidt P, Van Hees M, Wannijn J, Van Bree P, Rufyikiri G, et al. Uranium distribution and cycling in Scots pine (Pinus sylvestris L.) growing on a revegetated U-mining heap. J. Environ. Radioact. 2005; 81:201–219. pmid:15795035

46. Afanasyeva LV, Kashin VK, Mikhaylova TA. Effect of Industrial Pollution on Sulphur Accumulation in the Needles of Scotch Pine (Pinus sylvestris L.) in the South-Western Transbaikalia. Chem. Sust. Dev. 2005; 13:459–465.

47. Samecka-Cymerman A, Kosior G, Kempers AJ. Comparison of the moss Pleurozium schreberi with needles and bark of Pinus sylvestris as biomonitors of pollution by industry in Stalowa Wola (southeast Poland). Ecotoxic. Environ. Saf. 2006; 65:108–117.

48. Szynkowska M, Pawlaczyk A. The influence of mercury content on the structural changes of bioindicator surfaces. Pol. J. Chem. Techn. 2007; 9:115–120.

49. Fältmarsch R, Peltola P, Åström M, Raitio H. Abundance, correlations and spatial patterns of nutrients and metals in till, humus, moss and pine needles in a boreal forest, western Finland, Geochemistry: Exploration, Environment. Analysis 2007; 7:57–69.

50. Afanasieva LV, Kashin VK, Mikhailova TA, Berezhnaya NS. Effect of the industry-related air pollution on the accumulation of heavy metals in the pine needles in the basin of the Selenga River. Chem. Sust. Dev. 2007; 15:25–31.

51. Gałuszka A A review of geochemical background concepts and an example using data from Poland. Environ. Geol. 2007; 52:861–870.

52. Maňkovská B, Oszlányi J. Mosses and foliage of forest tree species as biomonitors of nitrogen pollution. Int. J. Environ. Stud. 2008; 65:379–389.

53. Shcherbenko TA, Koptsik GN, Groenenberg BJ, Lukina NV, Livantsova SY. Uptake of nutrients and heavy metals by pine trees under atmospheric pollution. Moscow Univ. Soil Sci, Bull. 2008; 63:51–59.

54. Sochacka J, Kusa Z, Baran W. Influence of the Combinated Bioaccumulation of Fluoride and Sulfur on Chlorophyll Content in Needles of Selected Trees from the Areas of Southern Poland. Ecol. Chem. Eng. A 2009; 16:427–432.

55. Ladanai S, Ågren GI, Olsson BA. Relationships between tree and soil properties in Picea abies and Pinus sylvestris forests in Sweden. Ecosystems 2010; 13:302–316.

56. Yucel E, Guner ST. Sulphur Pollution and its Dependency on the Altitude in the West Anatolian Scots Pine Forest. Ekoloji 2010; 19:1–7.

57. Pöykiö R, Hietala J, Nurmesniemi H. Scots pine needles as bioindicators in determining the aerial distribution pattern of sulphur emissions around industrial plants. World Acad. Sci. Eng. Technol. 2010; 4:311–314.

58. Mikhailova TA, Kalugina OV, Afanaseva LV, Nesterenko OI. Trends of chemical element content in needles of Scots pine (Pinus sylvestris L.) under various natural conditions and emission load. Contemp. Prob. Ecol. 2010; 3:173–179.

59. Dmuchowski W, Gozdowski D, Baczewska AH. Comparison of four bioindication methods for assessing the degree of environmental lead and cadmium pollution. J. Hazard. Mater. 2011; 197:109–118. pmid:21978583

60. Dmuchowski W, Gozdowski D., Baczewska A.H., Brągoszewska P. Evaluation of the arsenic environmental pollution on the basis of different bioindicative methods. Environ. Prot. Nat. Resour. 2011; 48: 84–95.

61. Pridacha VB, Sazonova TA, Talanova TY, Ol’chev AV. Morphophysiological responses of Pinus sylvestris L. and Picea obovata Ledeb. to industrial pollution under conditions of Northwestern Russia. Russ. J. Ecol. 2011; 42:22–29.

62. Parzych A, Jonczak J. Content of heavy metals in needles of Scots Pine (Pinus sylvestris L.) in selected pine forests in Słowiński National Park. Arch. Environ. Prot. 2013;39:41–51.

63. Przybysz A, Sæbø A, Hanslin HM, Gawroński SW. Accumulation of particulate matter and trace elements on vegetation as affected by pollution level, rainfall and the passage of time. Sci. Total Environ. 2014; 481:360–369. pmid:24607629

64. Dmuchowski W, Gozdowski D, Baczewska AH, Brągoszewska P. Evaluation of various bioindication methods used for measuring zinc environmental pollution. Int. J. Environ. Pollut. 2013; 51:238–254.

65. Chudzińska E, Diatta JB, Wojnicka-Półtorak A. Adaptation strategies and referencing trial of Scots and black pine populations subjected to heavy metal pollution. Environ. Sci. Poll. Res. 2014; 21:2165–2177.

66. Chudzinska E, Pawlaczyk EM, Celinski K, Diatta J. Response of Scots pine (Pinus sylvestris L.) to stress induced by different types of pollutants–testing the fluctuating asymmetry. Water Environ. J. 2014; 28:533–539.

67. Sukhareva TA, Lukina NV. Mineral composition of assimilative organs of conifers after reduction of atmospheric pollution in the Kola Peninsula. Russ. J Ecol. 2014; 45:95–102.

68. Rautio P, Poikolainen J. State of the terrestrial environment in the joint Finnish, Norwegian and Russian border area on the basis of bioindicators. Final technical report of the Pasvik Environment Monitoring Programme, Kuopio: Finland; 2014.

69. Parzych A, Jonczak J. Pine needles (Pinus sylvestris L.) as bioindicators in the assessment of urban environmental contamination with heavy metals. J. Ecol. Eng. 2014; 15:29–38.

70. Pietrzykowski M, Socha J, van Doorn NS. Linking heavy metal bioavailability (Cd, Cu, Zn and Pb) in Scots pine needles to soil properties in reclaimed mine areas. Sci. Total Environ. 2014; 470:501–510. pmid:24176697

71. Mori J, Hanslin HM, Burchi G, Sæbø A. Particulate matter and element accumulation on coniferous trees at different distances from a highway. Urban For. Urban Greening 2015; 14:170–177.

72. Gjengedal E, Martinsen T, Steinnes E. Background levels of some major, trace, and rare earth elements in indigenous plant species growing in Norway and the influence of soil acidification, soil parent material, and seasonal variation on these levels. Environ. Monit. Assess. 2015; 187:1–28. pmid:25600401

73. Mazur Z., Radziemska M., Fronczyk J., Jeznach J. Heavy metal accumulation in bioindicators of pollution in urban areas of northeastern Poland. Fresen. Environ. Bull. 2015; 24: 216–23.

74. Pająk M, Gąsiorek M, Cygan A, Wanic T. Concentrations of Cd, Pb and Zn in the top layer of soil and needles of Scots pine (Pinus sylvestris L.); a case study of two extremely different conditions of the forest environment in Poland. Fresen. Environ. Bull. 2015; 24:71–76.

75. Andráš P, Turisová I, Buccheri G, de Matos JMX, Dirner V. Comparison of heavy-metal bioaccumulation properties in Pinus sp. and Quercus sp. in selected European Cu deposits. Web Ecol. 2016; 16:81–87.

76. Kosiorek M, Modrzewska B, Wyszkowski M. Levels of selected trace elements in Scots pine (Pinus sylvestris L.), silver birch (Betula pendula L.), and Norway maple (Acer platanoides L.) in an urbanized environment. Environ. Monit. Assess. 2016; 188:598. pmid:27696092

77. Kandziora-Ciupa M, Ciepał R, Nadgórska-Socha A, Barczyk G. Accumulation of heavy metals and antioxidant responses in Pinus sylvestris L. needles in polluted and non-polluted sites. Ecotoxic. 2016; 25:970–981.

78. Holt E, Kočan A, Klánová J, Assefa A, Wiberg K. Polychlorinated dibenzo-p-dioxins/furans (PCDD/Fs) and metals in scots pine (Pinus sylvestris) needles from Eastern and Northern Europe: Spatiotemporal patterns, and potential sources. Chemosphere 2016; 156:30–36. pmid:27160632

79. Baczewska AH, Dmuchowski W, Gworek B, Dąbrowski P, Brągoszewska P. Comparison of bioindication methods for assessing the level of air pollution with heavy metals in Warsaw. Przem. Chem. 2016; 95:334–338.

80. Popova MG. Micronutrient composition of woody plants in Central Yakutia. Russ. Agric. Sci. 2016; 42: 31–33.

81. Nickel S, Schröder W. Integrative evaluation of data derived from biomonitoring and models indicating atmospheric deposition of heavy metals. Environ. Sci. Poll. Res. 2017; 24:11919–11939.

82. Pająk M, Halecki W, Gąsiorek M. Accumulative response of Scots pine (Pinus sylvestris L.) and silver birch (Betula pendula Roth) to heavy metals enhanced by Pb-Zn ore mining and processing plants: Explicitly spatial considerations of ordinary kriging based on a GIS approach. Chemosphere 2017; 168:851–859. pmid:27836278

83. Navrátil T, Šimeček M, Shanley JB, Rohovec J, Hojdová M, Houška J. The history of mercury pollution near the Spolana chlor-alkali plant (Neratovice, Czech Republic) as recorded by Scots pine tree rings and other bioindicators. Sci. Total Environ. 2017; 586:1182–1192. pmid:28237461

84. Parzych A, Mochnacký S. Sobisz Z, Kurhaluk N, Polláková N. Accumulation of heavy metals in needles and bark of Pinus species. Folia For. Polonica 2017; 59:34–44.

85. Kalugina OV, Mikhailova TA, Shergina OV. Pinus sylvestris as a bio-indicator of territory pollution from aluminum smelter emissions. Environ. Sci. Pollut. Res. 2017; 24:10279–10291.

86. Klink L, Polechońska M, Dambiec K. Białas A. Comparative Study on Macro-and Microelement Bioaccumulation Properties of Leaves and Bark of Quercus petraea and Pinus sylvestris, Arch. Environ. Contam. Toxicol. 2017; 72:1–9.

87. Environmental Data Report GEMS Monitoring and Assessment Research Centre, United Nation Environment Programme. Oxford: Blackwell; 1989/90.

88. Legge SV, Krupa AH. Effects of sulphur dioxide. In: Bell JNB, Treshow M, editors. Air pollution and plant life. nd. editors. Chichester, England: John Wiley & Sons; 2002. pp. 135–162

89. Bytnerowicz A, Omasa K, Paoletti E. Integrated effects of air pollution and climate change on forests: a northern hemisphere perspective. Environ. Pollut. 2007; 147:438–445. pmid:17034915

90. Tausz M. Sulfur in forest ecosystems. In: Hawkesford MJ, De Kok LJ. editors, Sulfur in Plants An Ecological Perspective, Berlin: Springer; 2007. pp. 59–75.

91. De Vries W, Dobbertin MH, Solberg S, Van Dobben HF, Schaub M. Impacts of acid deposition, ozone exposure and weather conditions on forest ecosystems in Europe: an overview. Plant Soil 2014; 380:1–45.

92. Molski BA, Dmuchowski W. Effects of Acidification on Forests and Natural Vegetation, Wild Animals and Insects. In: Schneider T, editor, Acidification and its Policy Implications, Amsterdam: Amsterdam: Elsevier; 1986. pp. 29–51.

93. Oliva SR, Espinosa AJF. Monitoring of heavy metals in topsoils, atmospheric particles and plant leaves to identify possible contamination sources. Microchem. J. 2007; 86:131–139.

94. Celik A, Kartal AA, Akdogan AA, Kaska Y. Determining the heavy metal pollution in Denizli (Turkey) by using Robinia pseudo-acacia L. Environ. Int. 1995; 31:105–112.

95. Sawidis T, Chettri MK, Papaioannou A, Zachariadis GA, Stratus J. A study of metal distribution from lignite fuels using trees as biological monitors. Ecotox. Environ. Saf. 2001; 48:27–35.

96. Ballach HJ, Wittig R. Twenty-five years of biomonitoring lead in the Frankfurt/Main area. Envrion. Sci. Pollut. Res. Int. 2001; 8:136–142.

97. Tarricone K, Wagner G, Klein R. Toward standardization of sample collection and preservation for the quality of results in biomonitoring with trees—A critical review. Ecol. Indic. 2015; 57:341–359.

98. Berlizov AN, Blum OB, Filby RH, Malyuk IA, Tryshyn VV. Testing applicability of black poplar (Populus nigra L.) bark to heavy metal air pollution monitoring in urban and industrial regions. Sci. Total Environ. 2007; 372:693–706. pmid:17140640

99. Simpson D, Winiwarter W, Börjesson G, Cinderby S, Ferreiro A, Guenther A., et al. Inventorying emissions from nature in Europe. J. Geophys. Res. 1999; 104:8113–8152.

100. Vestreng V, Myhre G, Fagerli H, Reis S, Tarrasón L. Twenty-five years of continuous sulphur dioxide emission reduction in Europe. Atmos. Chem. Phys. 2007; 7:3663–3681.

101. Smith SJ, van Aardenne J, Klimont Z, Andres RJ, Volke A, Delgado Arias S. Anthropogenic sulfur dioxide emissions: 1850–2005. Atmos. Chem. Phys. 2011; 11:1101–1116.

102. Klimont Z, Smith SJ, Cofala J. The last decade of global anthropogenic sulfur dioxide: 2000–2011 emissions. Environ. Res. Lett. 2013; 8:014003.

103. European Union emission inventory report 1990–2014 under the UNECE Convention on Long-range Transboundary Air Pollution (LRTAP). Technical report No 16/2016, Copenhagen: European Environment Agency; 2016.

104. Environment, Statistical Information and Elaborations. Warsaw: Central Statistical Office, Poland; 2016.

105. Environment, Statistical Information and Elaborations. Warsaw: Central Statistical Office, Poland; 2007.

106. Adriano DC. Trace elements in the terrestrial environment. New York: Springer-Verlag; 1986.

107. Newman MC. Fundamentals of ecotoxicology: the science of pollution, 4th. ed. Boca Raton, London, New York: CRC Press; 2014.

108. Pawlat-Zawrzykraj A, Brzank M. Evaluation of the ecological corridors in the context of land use changes in the commune. Infrast. Ecol. Rural Areas 2015; 4:1021–1033.

109. Kloepper-Sams PJ, Owens JW. Environmental biomarkers as indicators of chemical exposure. J. Hazard. Mater. 1993; 35:283–294.

110. Allen SE, Grishaw HM, Parkinson JA, Quarmby C. Chemical Analysis of Ecological Materials. Oxford: Blackwell; 1974.

111. Elmer Perkin. Analytical methods for atomic absorption spectrophotometry, Bodenseewerk, Pub., B353, 1990.

112. Leco Corporation. Application Bulletin, St. Joseph, Mi, 1987.

113. Huttunen S, Laine K, Torvela H. Seasonal sulphur contents of pine needles as indices of air pollution. Ann. Bot. Fenn. 1985; 22:343–359.

114. Hovmand M.F, Nielsen S.P, Johnsen I. Root uptake of lead by Norway spruce grown on 210 Pb spiked soils. Environ. Pollut. 2009; 157:404–409. pmid:19013698

115. Tjell JC, Hovmand MF, Mosbćk H. Atmospheric lead pollution of Grass grown in a background area in Denmark. Nature 1979; 280:425–426.

116. Mosbaek H, Tjell JC, Hovmand MF. Atmospheric lead input to agricultural crops in Denmark. Chemosphere 1989; 19:1787–1799.

117. Anderson S, Chappelka AH, Flynn KM, Odom JW. Lead accumulation in Quercus nigra and Q. velutina near smelting facilities in Alabama, USA. Water Air Soil Poll. 2000; 118: 1–11.

118. Sheppard SC, Sheppard MI, Ilin M, Thompson P. Soil-to-plant transfers of uranium series radionuclides in natural and contaminated settings. Radioprotection 2005; 40(S1): 253–259.

119. West PW. Release to shoots of copper stored in roots of Pinus radiata D. Don. Ann. Bot. 1979; 43:337–340.

120. Kabata-Pendias A. Trace elements in soils and plants, 4th ed. Boca Raton: CRC press; 2010.