Abstract
The aim of this study was to test a possible use of Urtica dioica (common nettle) plant as a biomonitor of polonium 210Po and lead 210Pb contamination near phosphogypsum stacks by determining concentrations of these radionuclides in samples collected from the area of phosphogypsum stockpile in Wiślinka (northern Poland). The 210Po and 210Pb contents in roots depended on their concentrations in soils. Bioconcentration factor values from soil to root of the plant did not depend on 210Po and 210Pb contents in soils that leads to the conclusion that different polonium and lead species have different affinities to U. dioica plants. The main sources of both analyzed radionuclides in green parts of plants are wet and dry air deposition and transportation from soil. The values of 210Po/210Pb activity ratio indicate natural origin of these radioisotopes in analyzed plants. 210Po and 210Pb concentration in U. dioica roots is negatively weakly correlated with distance from phosphogypsum stockpile.
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Introduction
Phosphogypsum consists mainly of CaSO4·2H2O and is a by-product of phosphoric acid production from phosphate rocks (Hull and Burnett 1996). It is usually stored on stacks in specially designated areas. The phosphogypsum stockpile in Wiślinka (northern Poland) contains about 16 million tons of phosphogypsum (Boryło et al. 2013). It is located between the Martwa Wisła river and farm fields, close to the Gdańsk agglomeration (Fig. 1). Phosphate rocks are the starting material for the production of all phosphate products and the main source of phosphorus for fertilizers. They are characterized by high content of natural alpha radioactive elements, especially from 238U decay chain (226Ra, 222Rn, 210Po) and beta emitter 210Pb. The essence of radiotoxicity of the phosphogypsum is gamma radioactivity and high content of natural radioactive elements which could be leached by rain and bioaccumulated in plants, animals, and humans. In the process of phosphoric acid production, about 80 % of uranium is associated with the phosphoric acid fraction, while about 90 % of the 210Po and 210Pb is bound to the phosphogypsum fraction (Azouazi et al. 2001; Baxter 1996; Hull and Burnett 1996). Phoshphogypsum stockpile in Wiślinka is considered to be one of the main contaminators of the Martwa Wisła river. Our previous researches indicate that it might have serious radiological impact on the local environment. Phosphogypsum can be moved by the wind, and radionuclides might be leached by wet precipitation and transported through groundwaters to plants where they are accumulated (Bem 2005; Boryło et al. 2009, 2012, 2013; Skwarzec et al. 2010; Boryło and Skwarzec 2011; Olszewski et al. 2015).
Both 210Po and 210Pb are natural radionuclides, daughters of 238U decay series. Their half-lives are 138.38 days for 210Po and 22.3 years for 210Pb (Boryło et al. 2013). These natural radionuclides are found in varying concentrations in soil, sand, sediment, and natural water and constitute an important component of the natural background radiation. They are known to significantly contribute to the radiation dose of the population (Rajashekara and Narayana 2010). The main source of 210Po and 210Pb in the atmosphere is 222Rn emanation from the ground. 210Po and 210Pb return to the earth as dry fallout or are washed out in the rain. Important anthropogenic sources of these radionuclides are burning of fossil fuels, tetraethyl lead in petrol, dust storms, refineries, superphosphate fertilizers, the sintering of ores in steelworks, and the burning of coal in coal-powered power stations (Boryło et al. 2012). 210Po is highly toxic, and its presence in soils may be traced to the decay of radionuclides of the 238U chain in the soil (Aslani et al. 2005). Lead is widely distributed in the earth’s crust, but the main ore is galena, PbS, PbO, and PbO2. Carbonates, chlorophosphates, sulfates, sulfatocarbonates, and uosilicates are all less abundant than galena (Jia and Torri 2007). The possible different chemical behavior of both 210Po and 210Pb in the water column is characterized by a stronger affinity of 210Po for particles than its precursor, 210Pb (Gasco et al. 2002). The usual atmospheric input by rain has 210Po/210Pb activity ratio of 0.1–0.2 (Jia et al. 2003). The value of activity ratio higher than 1.0 must be affiliated with biogeochemical processes that can control the distribution of the two radionuclides (Jia et al. 2003).
The main aim of this work was to establish a possible use of Urtica dioica (common nettle) plants as 210Po and 210Pb contamination bioindicator in the area of phosphogypsum stockpile and to examine the impact of phosphogypsum stockpile on the surrounding environment. Additionally, the values of the 210Po/210Pb activity ratio and bioconcentration factor (BCF) and translocation factor (TF) were calculated in order to define both possible 210Po and 210Pb sources and level of their accumulation in plants.
Materials and methods
Sample collection and analysis
The U. dioica plant samples along with corresponding soils were collected from multiple locations in the area of phosphogypsum stack in Wiślinka (northern Poland) (Fig. 1) in September and October 2014. Over ground shoots of U. dioica plant die during winter, and it spends the winter in the form of underground rhizomes. In this case, we decided to collect samples in autumn when shoots are old and long enough exposed to air deposition. All of the collected samples had similar height (about 1.5 m). Control samples were collected in Malbork in Pomeranian Voivodeship, Poland. U. dioica was chosen for this research due to its commonness in Polish environment. Collected plants were divided into green parts and roots. Roots were washed with double deionized water in order to remove soil particles. Green parts were not washed due to examination of possible dry deposition impact. Only soil particles were removed. Before analysis, each plant sample was air-dried, homogenized using mortar, and dried in 60 °C. Soil samples were homogenized and passed through 0.25-mm sieve. From homogenized sample, three subsamples were weighted and enriched with approximately 20 mBq of 209Po yield tracer. Samples were mineralized using HCl, HNO3, and H2O2 mixture. Polonium was electrodeposited on silver discs according to the procedure presented by Skwarzec (1997, 2009). 210Pb was analyzed indirectly through its daughter’s 210Po activity measurement after 6-month storage. After this time, polonium was again electrodeposited on silver disc and 210Pb activity was calculated through 210Po activity (Skwarzec 1997, 2009).
Measurement technique
The activities of 210Po were measured using an alpha spectrometer (Alpha Analyst S470) equipped in a surface barrier PIPS detector with an active surface of 300–450 mm2 placed in a vacuum chamber connected to a 1024 multichannel analyzer (Canberra—Packard, USA). Detector yield ranged from 0.30 to 0.40. In most of the used detectors, the resolution was 17–18 keV. Minimum detectable activity (MDA) for 210Po and 210Pb were 0.05 and 0.06 mBq g−1. The accuracy and precision of the radiochemical method were estimated to be less than 7 % by participation in international intercomparison exercises and analyses of IAEA materials. The precision between subsamples was estimated to be less than 3 % for all analyzed radioisotopes. 210Po activities were corrected for decay between deposition on silver discs and counting on alpha spectrometer. 210Po and 210Pb activities were calculated for sampling date. The value of BCF and TF were calculated as (Boryło et al. 2012)
Results and discussion
210Po and 210Pb in U. dioica roots, shoots, and soils
The obtained concentrations of 210Po and 210Pb in analyzed plants and soils samples are presented in Table 1. The values of 210Po concentrations ranged from 5.67 ± 0.11 to 34.81 ± 0.25 Bq kg−1 dry wt. in green parts, from 1.21 ± 0.05 to 69.09 ± 1.93 Bq kg−1 dry wt. in roots, and from 18.42 ± 0.35 to 258.34 ± 4.18 Bq kg−1 dry wt. in corresponding soils. 210Pb concentrations in analyzed U. dioica green parts, roots, and soils ranged from 10.73 ± 0.10 to 40.93 ± 0.41 Bq kg−1 dry wt., from 1.20 ± 0.15 to 57.54 ± 1.56 Bq kg−1 dry wt., and from 18.28 ± 0.45 to 273.55 ± 4.12 Bq kg−1 dry wt., respectively. For analyzed common nettle control sample collected in Malbork, the obtained 210Po results were 9.61 ± 0.18 Bq kg−1 dry wt. for green part, 3.09 ± 0.15 Bq kg−1 dry wt. for root, and 21.09 ± 0.63 Bq kg−1 dry wt. for soil while 210Pb activities were 16.24 ± 0.11, 2.73 ± 0.09, and 21.36 ± 0.22 Bq kg−1 dry wt., respectively.
Comparison with other studies on 210Po and 210Pb uptake by plants
In Huleva, Spain, 210Po activities in Spartina densiflora plants were surveyed and obtained results ranged from 5.58 ± 0.41 to 45.2 ± 4.5 Bq kg−1 dry wt. in whole plant (Martinez-Aguirre et al. 1997). In 2011, samples of different plants (meadow, hygrophilous, edible, ruderal plants, and corn) were collected around phosphogypsum stack in Wiślinka and surveyed on polonium concentrations. Higher activities of 210Po were measured in roots of analyzed plants (from 6.4 ± 0.3 to 89 ± 1 Bq kg−1 wet wt. for roots and from 2.1 ± 0.1 to 51 ± 1 Bq kg−1 wet wt. for green parts). The only exception were edible plants where higher 210Po contents were measured in green parts than in roots (2.2 ± 0.1 and 1.2 ± 0.1 Bq kg−1 wet wt., respectively). The highest 210Po concentrations were noticed in ruderal plants collected from sewage sludge that covers the phosphogypsum stockpile (Boryło et al. 2012). In Finland, 210Po and 210Pb activities in wild berries were measured and the highest activities were noticed in stems of the analyzed samples (from 30 to 60 Bq kg−1 dry wt., for 210Pb, and from 30 to 90 Bq kg−1 dry wt. for 210Po), the lowest in fruits (<10 Bq kg−1 wet wt. for both analyzed radionuclides), while in roots, the measured concentrations were between 50 and 100 Bq kg−1 wet wt. for 210Po and between 35 and 45 Bq kg−1 wet wt. for 210Pb (Vaaramaa et al. 2010). Both 210Po and 210Pb concentrations in edible plants vary depending on the type of plants (e.g., leafy, rooty) (Ekdal et al. 2006).
The values of 210Po/210Pb activity ratios in U. dioica
The values of 210Po/210Pb activity ratio in analyzed common nettle U. dioica plants and soils are presented in Table 2. The values ranged from 0.50 ± 0.17 to 0.90 ± 0.08 in green parts, from 1.03 ± 0.13 to 1.53 ± 0.10 in roots, and from 0.91 ± 0.11 to 1.09 ± 0.09 in soils. In green parts, roots, and soils of control samples collected in Malbork, the calculated values of 210Po/210Pb activity ratio were 0.60 ± 0.09, 1.13 ± 0.11, and 1.00 ± 0.04, respectively, while in wild berries, roots and green parts collected in Finland were higher than 1. This is probably connected with the fact that 210Po is more available to plants roots than 210Pb. The authors suggest further research in this matter (Vaaramaa et al. 2009). The 210Po excess in green parts of Finnish wild berries suggests another source of this radioisotope than wet and dry deposition, probably connected with transfer from soil. Similar results were observed in U. dioica roots in this study. In all analyzed common nettle samples, the values of 210Po/210Pb activity ratio were higher than 1 that suggests that 210Po is more mobile in soil where the values of these ratios are close to 1 (Table 2). In green parts of U. dioica plants, values of 210Po/210Pb activity ratio were lower than 1 suggesting that wet and dry deposition is significant source of 210Po and 210Pb radioisotopes in common nettle stems and leaves. Values that are close to unity could suggest either higher rate of metal transfer from soils or impact of phosphogypsum stockpile. The value of 210Po/210Pb activity ratio in air deposition ranges from 0.03 to 0.05 (Vaaramaa et al. 2010). It is assumed that up to 80 % of natural 210Po and 210Pb radioactivity in wild plants is connected with wet and dry deposition of 222Rn decay products (Persson and Holm 2011). In analyzed U. dioica plants, we received very high Spearman’s correlation factors between 210Po and 210Pb activities: r s = 0.97 in green parts, r s = 1.00 in roots, and r s = 1.00 in corresponding soils that confirm natural origin of these radionuclides. Spearman’s rank correlation is a non-parametrical alternative for Pearson’s correlation. It can be used to calculate the correlation between two variables that do not have normal distribution and are not linear. Moreover, Spearman’s rank correlation is resistant for outlier results (Corder and Foreman 2014).
The values of 210Po and 210Pb BCF and TF in U. dioica
TF, TFgreen part/soil and BCF, BCFplant/soil common nettle samples were calculated according to Eqs. (1) to (4). The values of obtained factors are presented in Tables 3 and 4. For 210Po, they ranged from 0.066 ± 0.003 to 0.327 ± 0.020 for BCF, from 0.024 ± 0.001 to 1.889 ± 0.036 for TFgreen part/soil, from 0.17 ± 0.01 to 1.96 ± 0.09 for BCFplant/soil, and from 0.090 ± 0.003 to 28.67 ± 1.18 for TF. In control sample, calculated TF and BCF values were 0.147 ± 0.006, 0.456 ± 0.015, 0.60 ± 0.03, and 3.11 ± 0.11, respectively. In case of 210Pb, the obtained values ranged from 0.063 ± 0.008 to 0.297 ± 0.010 for BCF, from 0.039 ± 0.001 to 2.174 ± 0.021 for TFgreen part/soil, from 0.184 ± 0.006 to 2.288 ± 0.401 for BCFplant/soil, and from 0.19 ± 0.01 to 34.10 ± 4.28 for TF. For control samples, these values were 0.128 ± 0.004, 0.760 ± 0.009, 0.888 ± 0.031, and 5.95 ± 0.20, respectively.
Comparison with other 210Po and 210Pb TF and BCF studies
Al-Masri et al. (2008) published TF values between fruits and leaves of vegetables and soils for both 210Po and 210Pb. Due to atmospheric deposition, TF to fruits (from 0.024 to 0.14 for 210Pb and from 0.028 to 0.2 for 210Po) were smaller than to leaves (from 0.37 to 1.4 for 210Pb and from 0.3 to 1.0 for 210Po). The values of 210Po TFgreen part/soil for Menthea L. and Petroselinum crispum were 0.20 ± 0.08 and 0.46 ± 0.20, respectively (Al-Masri et al. 2010). These values are similar to some of our previous results as calculated TF values for 210Po concentrations in plants from Wiślinka were in the range from 0.06 for edible plants to 1.36 for hygrophilous plants, while BCF values ranged from 0.22 for hygrophilous plants to 2.30 for edible plants (Boryło et al. 2012). Manigandan and Manikandan (2008) analyzed different wild plants and calculated BCFplant/soil values for 210Po between 0.292 and 0.336.
Characteristics affecting 210Po and 210Pb bioavailability
Uptake of Po and Pb by plants can occur both through the root system and from atmospheric deposition through activity interception by external plant surfaces (Vandenhove et al. 2009). Large number of factors is known to control metal bioavailability in soils and their accumulation level in plants. These are soil and climatic conditions, plant genotype, and agronomic management, including active/passive transfer processes, sequestration and speciation, redox states, the type of plant root system, and the response of plants to elements in relation to seasonal cycles (Kabata-Pendias and Pendias 1984; Malik et al. 2010). One of the major factors that contribute to extent of the metals taken up by the plants is also the structure and type of the soil. Also, such factors as clay particles, metal solubility controlled by pH, amount of metal cation exchange capacity, organic carbon content, and oxidation state of the system are important in metal availability (Malik et al. 2010). Narayana et al. (2006) reported higher 210Po and 210Pb sorption in soils with increasing organic matter content that was confirmed by high correlation factors (0.62 for 210Pb and 0.70 for 210Po). Vaaramaa et al. (2010) conducted research of soil cores divided into litter, organic, illuvial, and eluvial horizons and showed that 210Pb activity is correlated with organic matter content in soil. In all analyzed soil horizons, high 210Pb activity correlations between organic matter content were proved (the highest 0.85 for eluvium). No relevant correlations between organic matter content and 210Po concentrations in soils were reported. Similar results were obtained for relationships between Mn, Fe, Al, and Pb contents and 210Po and 210Pb activities in soils. Radiolead is strongly correlated with these metal concentrations, while no significant correlations were received for 210Po activities (Vaaramaa et al. 2010). Berger et al. (1965) indicated that organic soils contain on average three times more 210Po than mineral soils. These differences might be associated with higher 210Po sorption on clay and organic matter. In case of 210Po and 210Pb, the bioavailability is mainly dependent on their content in soils, plant morphology, and the level of wet and dry precipitation.210Po and 210Pb activity concentrations in root and tuber crops, cereals, and legumes, where the edible portion is protected by inedible plant parts, should not be affected by air deposition containing both 210Po and 210Pb (Vandenhove et al. 2009).
TF and BCF values’ variability explanation
210Po and 210Pb concentrations in analyzed U. dioica samples are lower than their contents in corresponding soils. It is clearly seen that both 210Po and 210Pb activities in common nettle’s roots are dependent on their content in soils (r s = 0.72 for 210Po and 0.65 for 210Pb) (Fig. 2), while the value of BCF does not exhibit this correlation (r s = 0.17 for 210Po and 0.18 for 210Pb) (Fig. 3). BCFplant/soil values are strongly and negatively correlated with 210Po and 210Pb concentrations in soils (r s = −0.92 for 210Po and −0.93 for 210Pb) (Fig. 4). According to Chen et al. (2005). there are considerable differences in the uptake and translocation of long-lived radionuclides among different plant species. Perianez and Martinez-Aguirre (1997) reported that BCFplant/soil factor in relation with 210Po contents in soil can be described using function
This phenomenon is confirmed in our study on Fig. 4 where BCFplant/soil factor is not linearly related with 210Po concentration in soil and can be described by function
It is probably connected with the fact that plants readily uptake elements essential for their growth when substrate concentrations are low (Mengel and Kirkby 1979). Usually, plant uptake of non-essential elements is constant in this substrate concentration. Only in high substrate concentrations for both essential and non-essential elements it can decrease, leading to toxicity or death of a plant (Martinez-Aguirre et al. 1997). Even though, some non-essential elements can mimic an essential element resulting in non-linear relationship between soil concentration and BCFplant/soil at low substrate concentrations (Sheppard and Sheppard 1985). This phenomenon in lesser extent can be also noticed in case of relation between BCF values and 210Po and 210Pb concentrations in soils (Fig. 3). Plants take up radionuclides of similar chemical forms as the essential nutrient and transport them to specific tissues based on the function of the element in plant metabolism that is reflected in its higher concentration in a particular part compared to others (Al-Kharouf et al. 2008). Another explanation could be connected with the level of wet and dry deposition on green parts of the plants and with differences in previously mentioned soil and plant characteristics that may affect bioavailability of metals (Persson and Holm 2011). According to Vandenhove et al. (2009). the soil type and texture are crucial for Pb BCFplant/soil values, while in case of 210Po, this factor is highest on coarse-textured soils and lowest on fine-textured and organic soils. Our results suggest that U. dioica roots could be used as a biomonitor of 210Po and 210Pb contamination in exploratory studies even though there are differences in both radionuclide bioavailability from soils to roots. The highest BCFplant/soil values were calculated for plants grown on soil with low both 210Po and 210Pb contents. Sample numbers 3 and 4 (Table 1) have significantly lower 210Po and 210Pb activities in green parts. Probable explanation is that the exposure to precipitation varies with the degree of covering of leaves. Roots serve as a natural barrier preventing the transport of many trace metals including radionuclides to the upper plant parts. The radionuclide translocation from roots to shoots is probably dependent on the species (Shtangeeva 2010). Relations between 210Po and 210Pb content in soils and in green parts of analyzed U. dioica plants is also negatively correlated (r s = −0.67 for 210Po and −0.60 for 210Pb) (Fig. 5) that confirms differentiated impact of air deposition on these radioisotope contents in plant leaves. As a confirmation, we plotted TF and TFgreen part/soil values. Received linear function and high r s values (r s = 0.90 for both radionuclides) suggest similar source of both 210Po and 210Pb in green parts of U. dioica (Fig. 6). According to these results, it is impossible to use common nettle’s leaves and stems as a biomonitor of possible phosphogypsum particle deposition from air as their impact is probably irrelevant when compared to air particles or metal transfer from soil. BCF and TF values received for control samples (Tables 3 and 4) indicate that soil characteristics and air deposition are mainly responsible for 210Po and 210Pb uptake.
Impact of the phosphogypsum stack
Possible impact of 210Po and 210Pb from phosphogypsum stockpile on green parts, roots, and whole plants of common nettle U. dioica in respect with distance from the stack was evaluated. The obtained results indicate that concentrations of both radionuclides in roots of analyzed plants are weakly but negatively correlated with distance from phosphogypsum stockpile (r s = −0.43) (Fig. 7). Stronger correlations were obtained between 210Po and 210Pb concentrations in soils and distance from the stack (r s = −0.61 and −0.78, respectively). In case of green parts of U. dioica, no relevant correlations were calculated (r s = 0.37) (Fig. 8). Moreover, no significant correlations were observed for 210Po and 210Pb activities in whole plants (r s = −0.20 and −0.08, respectively) that suggests the crucial impact of air deposition on 210Po and 210Pb activities in U. dioica plants.
Conclusions
Polonium 210Po and lead 210Pb concentrations in analyzed plants and soils allow us to conclude that U. dioica roots can be used as a biomonitor of both 210Po and 210Pb soil contamination especially during exploratory surveys. We noticed that both radionuclides activities in roots were related to their concentrations in soils although BCF values did not present similar dependence. The relation between 210Po and 210Pb soil concentrations and BCFplant/soil values is non-linear what confirms that some forms of Po and Pb can mimic essential elements for plant growth, and depending on soil characteristics, they can be more easily absorbed by plants. Another explanation could be connected with the level of wet and dry deposition on green parts of the plants. These facts prevent using common nettle’s leaves and stems as a biomonitor of possible phosphogypsum particles deposition. The decrease of 210Po and 210Pb concentrations in common nettle’s root was noticed with increasing distance from phosphogypsum stockpile. This relation was not confirmed for analyzed green parts that is probably connected with the impact of the air deposition. The problem of phosphogypsum stockpile is limited to the zone of maximum 400 m. The highest contents of both 210Po and 210Pb were measured in samples collected from the slopes of the stack. The values of 210Po/210Pb activity ratio confirm natural sources of these radionuclides in U. dioica plants.
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Acknowledgments
The authors would like to thank National Science Centre Poland for the financial support under grant UMO-2012/05/N/NZ7/00978 and Ministry of Science and Higher Education under grant DS 505-8630-D505-15. The publication is financed from the European Social Fund as part of the project “Educators for the elite—integrated training program for PhD students, post-docs, and professors as academic teachers at University of Gdansk” within the framework of Human Capital Operational Programme, Action 4.1.1, improving the quality of educational offer of tertiary education institutions. This publication reflects the views only of the author, and the funder cannot be held responsible for any use which may be made of the information contained therein. Presented map in this article come from the collection of Documentation Centre of Geodesy and Cartography in Warsaw, Poland. The authors also thank Grzegorz Romańczyk, M.Sc. for help in plant sampling.
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Olszewski, G., Boryło, A. & Skwarzec, B. A study on possible use of Urtica dioica (common nettle) plant as polonium 210Po and lead 210Pb contamination biomonitor in the area of phosphogypsum stockpile. Environ Sci Pollut Res 23, 6700–6708 (2016). https://doi.org/10.1007/s11356-015-5879-3
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DOI: https://doi.org/10.1007/s11356-015-5879-3