Transfer of uranium and radium to Chinese cabbage from soil ...

J Radioanal Nucl Chem (2015) 306:685–694 DOI 10.1007/s10967-015-4198-y

Transfer of uranium and radium to Chinese cabbage from soil containing elevated levels of natural radionuclides ˇ erne1 • Radojko Jacímovic´1 • Ljudmila Benedik1,2 Borut Smodisˇ1,2 • Marko C

Received: 10 February 2015 / Published online: 17 May 2015 Ó Akade´miai Kiado´, Budapest, Hungary 2015

Abstract The transfer of 238U and 226Ra to Chinese cabbage (Brassica rapa L. subsp. pekinensis (Lour.) Hanelt) was investigated from soils contaminated with uranium-mill tailings (UMT) by means of a pot experiment in laboratory-based conditions applying different levels of soil contamination under various growing conditions. Activity concentrations for 226Ra in Chinese cabbage varied from 56–276, 156–502 and 277–877 Bq kg-1 dry mass for 20, 40 and 60 % of UMT content in the soil, respectively, and for 238U from 1.0–2.3 and 2.3–4.7 Bq kg-1 dry mass for 40 and 60 % of UMT content in the soil, respectively. The results showed increased accumulation of 226Ra and low accumulation of 238U in cabbage leaves in more contaminated soil. Keywords Chinese cabbage 238U U-mill tailings Soil properties

226

Ra Transfer

Introduction Mining and milling of uranium ore may enhance the levels of natural radionuclides in the environment near the plant [1]. Natural radionuclides contained in U-ore processing materials are of major radiological concern due to inner or external exposure to ionising radiation received by the inhabitants living close to the uranium mine areas [2, 3]. & Borut Smodisˇ [email protected] 1

Jozˇef Stefan Institute, Jamova cesta 39, 1000 Ljubljana, Slovenia

2

Jozef Stefan International Postgraduate School, Jamova cesta 39, 1000 Ljubljana, Slovenia

Radionuclides emitted from the waste disposal sites can be retained in the soil by adsorption on the soil colloids thus becoming immobile or even more mobile depending on the soil properties, physicochemical conditions and microbial activity of soil [4–8]. The fraction of radionuclides that is soluble in the soil solution and exchangeable from soil colloids to the soil solution is bioavailable for the plant root uptake [9]. Terrestrial plants take-up radionuclides by root absorbing system from soil [9] or by leaves from the atmosphere via wet or dry deposition of the resuspended radioactive material [10, 11]. The uptake via leaves in terrestrial plants differs quite a lot from one plant species to another and can be less effective and more limited than root uptake, but it is very important in aquatic plants [12]. On the other hand, the foliar uptake of terrestrial plants can become important in areas where single or chronic releases of radionuclides are likely to happen which result in much higher plant surface contamination than the uptake by roots from the contaminated soil [11]. Soil-to-plant transfer of 238U and 226Ra was reported for different plant species grown in soil contaminated with UMT [13–23]. The Brassica plants tend to be highlighted particularly, as they have the capabilities to accumulate radionuclides in the edible parts in higher quantities [21, 24–26] which may represent a radiological concern in the case of ingestion of contaminated crops [3, 27]. In order to evaluate the soil-toplant transfer of radionuclides the plant-to-soil radionuclide concentration ratio needs to be determined. Concentrations ratio describes the accumulation of radionuclides in the plants [18] and is important parameter used in doseassessment methodology or phytoremediation efficiency evaluation. Plants having the metal concentration ratio greater than 1 are suitable for the phytoremediation technology [28].

123

686

The aim of this particular study was to quantify the transfer of 238U and 226Ra to Chinese cabbage (Brassica rapa L. subsp. pekinensis (Lour.) Hanelt) from soil contaminated with UMT. Tested plants were growing in pots in the laboratory-based environment to ensure the growing conditions controlled as far as possible. Different levels of soil contamination under various growing conditions were applied in the pot experiment to simulate different contamination scenarios. Radionuclides were determined in the cabbage leaves to calculate the plant-to-soil radionuclide concentration ratios. Soil properties were also assayed as they directly affect the availability of radionuclides to plants.

Materials and methods Design of the experiment The statistical ANOVA design was used as the experimental basis where three different soils (A, B and C; acidic-pH-4.4, alkaline-pH-7.2 and alkaline-pH-7, respectively) and four levels of soil contamination were applied in a two-factor design. Chinese cabbage (Nagaoka F1; Semenarna Ljubljana d.d.) was sown on contaminated and non-contaminated soil in 2 L plastic pots. The plant pots were situated in randomized positions on a shelf, arranged in 4 block (one block for one replicate) to reduce the influence of nuisance factors that have not been accounted for in the experimental design (potential inhomogeneity of soil and tailings mixtures or non-steady lighting, heat or humidity). Plants were irradiated by fluorescent lamps (Fluora, Osram, 58 W) with a daily light phase of 12 h. Contaminated soils were prepared by mixing garden soil with UMT at three different ratios, representing different contamination scenarios. The non-contaminated soil was used as a control. Soil samples used for preparation of soil-tailings mixtures were taken from the local fields at the root zone (30 cm) in the vicinity of Ljubljana. Three different soils were chosen according to a different pH value, organic matter content and the content of available P2O5 and K2O. The tailings samples were taken from the Borsˇt tailings pile [29] of the former Zˇirovski vrh uranium mill and mine (latitude: 46°050 46.1000 N; longitude: 14°100 38.1900 E; altitude 617 m). Soil and tailings samples were air dried (3 weeks), sieved to pass through 5 mm sieve and mixed in mass ratios, representing 20, 40 and 60 % of UMT content in the contaminated soil, respectively. Experiment was performed in Hot Cells Facility of the Jozˇef Stefan Institute (Ljubljana, Slovenia) due to radioactive waste (UMT) that was present in the samples, as the facility is licensed for work with radioactive material.

123

J Radioanal Nucl Chem (2015) 306:685–694

Growing period in controlled conditions Cabbage’s seeding was performed in the beginning of March 2011, while the harvest of fully-grown plants was after 4 months of growth. The plants were grown in the temperature range from 22 to 25 °C, relative humidity range from 40 to 60 % and light irradiation range from 53 to 94 lmol s-1 m-2 (LI-COR Quantum sensor, USA) at the plant surfaces (30 cm below the lamps), respectively. Daily, each pot of 2 L of contaminated soils was brought to field capacity with deionized water to enable optimal soil irrigation. To prevent contamination of plants by the hot particles, all possible pathways of external contamination were considered. At the beginning of seeding, garden mats were put into the pots to ensure the maximum protection of plants against the dust resuspension. The ventilation of the Hot Cells Facility was enabled during the daytime phase (from 8 a.m. to 8 p.m.) to prevent potential contamination of plants by the 222Rn decay products due to the presence of relatively high quantities of U-mill tailings in the pots. Sampling and sample preparation for the radionuclide measurements Chinese cabbage plants were harvested after 4 months of growth to obtain sufficient amount of the samples for the radionuclide measurements. After the harvest, plants were separated on roots and leaves, carefully washed with tap water (15–20 min), dried in an oven (SP-260, Kambicˇ) for 3 days at 40 °C and left outside at room temperature to reach a constant mass (at least 3 h). Dried plant leaves were milled by a rotor speed mill (Fritsch, Pulverisette 14) and homogenized. Samples of contaminated soils intended for radionuclide measurements were taken at the beginning of the pot experiment before the cabbage’s seeding. Three soil samples were randomly taken for each experimental treatment (control, 20, 40 and 60 % of UMT content in the soil, respectively) from the amount of 5 kg of contaminated and non-contaminated soil prepared for the pots. These soils were dried in an oven (ST-05, Instrumentaria, Zagreb) for 3 days at 60 °C, sieved to pass through 2 mm sieve (Fritsch) and left outside at room temperature to reach a constant mass. Bigger clods were crushed with a mortar and pestle and sieved again through 2 mm sieve. Determination of

238

U and

226

Ra in plants and soils

Direct gamma-ray spectrometry was used for the measurements of 238U and 226Ra in soil samples. 226Ra was determined by measuring its decay product 214Pb at 295.2 and 351.9 keV and 238U via its daughter product 234Th at 63.28 keV. In addition, the limit of detection at a 95 %


687

confidence interval is calculated using the following equation [30]: pffiffiffi DL ¼ 2:706 þ 4:653 B where B is the background, calculated for the energy interval below the gamma peak. Cylindrical polystyrene containers of 5.9 cm inner diameter and 3.8 cm height (sample height) were filled with about 100–130 g of dry soil material and sealed hermetically using a glue gun, and stored for 4 weeks to allow radioactive equilibrium of the 226Ra series to be established. After that time, the samples were counted for 11 and 28 h for contaminated and non-contaminated soils, respectively, on a coaxial HPGe detector (Canberra, USA) connected to a multichannel analyzer (Canberra, USA). The detector had an active volume of 114 cm3, relative efficiency 25 % and full width at half maximum (FWHM) resolution of 1.8 keV for 60Co gamma-energy line at 1332 keV. The system was calibrated by a certified mixed gamma source which was put in the same geometrical configuration of the samples. The mixed gamma source was in soil matrix form containing 210Pb, 241Am, 109Cd, 57 Co, 139Ce, 203Hg, 113Sn, 137Cs, 54Mn, 88Y, 65Zn and 60Co with relative expanded uncertainty (k = 2) of ±4.1, ±3.5, ±4.7, ±4.1, ±3.9, ±3.9, ±3.9, ±4.0, ±3.3, ±3.9, ±3.5 and ±3.9 %, respectively (Analytics). The relative expanded uncertainty was calculated by the methodology described in NIST Technical Note 1297 [31] and taken into account for the total measurement uncertainty, as it was applied for the peak-efficiency calibration. For the spectra evaluation and activities calculation, the Genie 2000 software (Canberra, USA) was used; while the EFFTRAN code [32] was applied for sample density and coincidence corrections as it is appropriate for cylindrical detectors and samples. The reference material IAEA-434 Radionuclides in phosphogypsum and certified reference material IAEA-447 Natural and artificial radionuclides in moss-soil were used to validate the quality of measurement results as shown in Table 1. The results were above the DL, which was around 2.5 Bq kg-1 for 238U and 0.5 Bq kg-1 for 226Ra. Direct gamma-ray spectrometry was also used for the measurement of 226Ra in cabbage leaves. The measurements

were done for each pot separately to ensure appropriate statistical evaluation. 226Ra was determined by measuring its decay product 214Pb at 295.2 and 351.9 keV. Cylindrical polystyrene vials of 1.7 cm inner diameter and 4.3 cm height (sample height) were filled with about 4–6 g of dried plant leaves, sealed hermetically using a glue gun and stored for 4 weeks to allow radioactive equilibrium of the 226Ra series to be established. After that time, the samples were counted for 50 h in a well-type HPGe detector (Ortec, UK) connected to a multichannel analyser (Canberra, USA). The detector had an active volume of 252 cm3 and full width at half maximum (FWHM) resolution of 2.6 keV for 60Co gamma-energy line at 1332 keV. The system was calibrated by a certified mixed gamma source which was measured in the same geometrical configuration as the samples. The mixed gamma source was in cellulose matrix form containing 210 Pb, 241Am, 109Cd, 57Co, 139Ce, 203Hg, 113Sn, 137Cs, 54 Mn, 88Y, 65Zn and 60Co with relative expanded uncertainty (k = 2) of ±4.1, ±3.5, ±4.7, ±4.1, ±3.9, ±3.9, ±3.9, ±4.0, ±3.3, ±3.9, ±3.5 and ±3.9 %, respectively (Analytics). The relative expanded uncertainty was calculated by methodology as described in NIST Technical Note 1297 [31] and taken into account for the total measurement uncertainty, as it was applied for the peak-efficiency calibration. 139Ce, 88Y and 60Co were not considered in peak-efficiency calibration as the true coincidence-summing effects present in the measurements are the worst of all when using a well detector [33]. For the spectra evaluation and activities calculation, the GENIE 2000 software (Canberra, USA) was used; while the ANGLE code [34] was applied for sample density corrections as it supports the calculation of detection efficiency for welltype HPGe detectors. Gamma-ray spectrometric measurements were additionally compared with alpha-particle spectrometric measurements to check for possible 222Rn loss from the sealed vials (Table 2). Alpha-particle spectrometry was used for this comparison due to its long-term application in determination of natural radionuclides in various environmental and biological materials for our regular monitoring surveillance of a former uranium mine and previous studies

Table 1 Comparison of certified values and measured values for 238U and 226Ra activity concentrations (Bq kg-1 dry mass) in IAEA-447 and IAEA-434 reference materials (uncertainties are presented as expanded uncertainties with coverage factor k = 2) Reference material

Radionuclide

IAEA-447

238

22 ± 2

18 ± 6

226

25 ± 4

28 ± 2

238

120 ± 11

82 ± 19

226

780 ± 62

732 ± 30

U Ra

IAEA-434

U Ra

Certified value

Measured value

123

688 Table 2 Comparison of alphaparticle- and gamma-ray spectrometric measurement results for 226Ra activity concentrations (Bq kg-1 dry mass) in Chinese cabbage from different soil contamination treatments (uncertainties are presented as expanded uncertainties with coverage factor k = 2)


Plant sample

Gamma-ray spectrometry

1/10

82 ± 7

1/18

59 ± 6

63 ± 4

1/19

127 ± 10

124 ± 7

2/11

178 ± 16

156 ± 8

3/6

97 ± 9

95 ± 5

3/7

186 ± 19

180 ± 10

3/12

407 ± 33

386 ± 18

conducted at the uranium mine area. Alpha-spectrometric measurements were validated by participation in interlaboratory comparisons and proficiency tests organized by the International Atomic Energy Agency, Austria, the Institute for Reference Materials and Measurements, Belgium and the National Physical Laboratory, UK. The results were in all cases satisfactory [4, 13]. The k0-instrumental neutron activation analysis (k0INAA) was used for determination of U in plants via nuclear reaction 238U (n,c) 239U/239Np (T1/2 = 2.3565 d). About 230 mg of dried plant leaves were pelletized using manual hydraulic press (Specac, UK) in diameter 10 and 2 mm thick. The samples and standards (Al-0.1 % Au IRMM-530R disc of 5 mm in diameter and 0.2 mm thick) were stacked together in sandwich form, fixed in the polyethylene vial and irradiated for 12 h in the carousel facility (CF) at the 250 kW TRIGA Mark II reactor of the Jozˇef Stefan Institute at a thermal neutron flux of 1.1 9 1012 cm-2 s-1 [35]. Measurements of activated samples for U determinations were performed on absolutely calibrated HPGe detectors (Ortec, Canberra) with 40 and 45 % relative efficiencies. Measurements were performed at such distances that the dead time was kept below 10 % with negligible random coincidences. The detector with 40 % relative efficiency was connected to a GENIE 2000 multichannel analyzer, while the detector with 45 % relative efficiency was connected to an EG&G ORTEC Spectrum Master high rate multichannel analyzer. For peak area evaluation, the HyperLab [36] program was used. For determination of f (thermal to epithermal neutron flux ratio) and a (parameter which measures the epithermal neutron flux deviation from the ideal 1/E distribution), the ‘‘Cdratio’’ method for multi monitor was applied [37]. The values f = 28.6 and a = -0.001 were used to calculate the element concentrations. For elemental concentrations and effective solid angle calculations, the software package Kayzero for Windows, KayWin [38], was employed. Complementary determinations in soil Organic matter content, pH value, the content of available P2O5 and K2O, cation exchange capacity (CEC), organic C,

123

Alpha-particle spectrometry

70 ± 4

total N and C/N were assayed in the Centre for Pedology of Agronomy Department, Biotechnical Faculty, University of Ljubljana. For these determinations, the standard ISO recommended procedures were applied [39–41]. The samples were taken before the cabbage seeding from each pot separately to ensure appropriate statistical evaluation. Evaluation of radionuclide soil-to-plant transfer To quantify the transfer of radionuclides to plants comprising the uptake from soil and radionuclide root-to-shoot translocation a plant-to-soil radionuclide concentration ratio (CR) needs to be determined. CR was calculated as the ratio of total activity concentration on a dry mass basis (Bq kg-1 dry mass) in the plant (harvestable) to that in the soil [18]. Data analysis Statistical analysis of data was performed with the statistical software R Commander for Windows, version R 2.12.1 and Microsoft Excel 2010. Pearson correlation coefficients (r) with corresponding p values were used for evaluation of the relationships between radionuclides and soil properties.

Results and discussion Soils Tables 3 and 4 report 238U and 226Ra activity concentrations in contaminated soils used in the pot experiment. The values are presented as mean values with standard deviations of 3 measured samples randomly taken from each contamination treatment before the cabbage seeding. These values were used for calculation of 238U and 226Ra concentration ratios in Chinese cabbage. The relative expanded uncertainties with coverage factor k = 2 for the measured radionuclides in soils were 10–15 and 14–27 % for contaminated and control samples, respectively, for 238 U, and 4 and 5 % for contaminated and control samples,

J Radioanal Nucl Chem (2015) 306:685–694 Table 3 238U activity concentrations (Bq kg-1 dry mass) in UMT-contaminated and control soils

Table 4 226Ra activity concentrations (Bq kg-1 dry mass) in UMT-contaminated and control soils

Soil

689

Control soil

20 % of UMT in the soil


A

50.3 ± 5.4

254 ± 31

459 ± 41

710 ± 83

B

40.5 ± 1.5

270 ± 9

489 ± 8

712 ± 77

C

54.0 ± 3.7

286 ± 23

540 ± 38

770 ± 59

Soil

Control soil




A

51.2 ± 0.3

1745 ± 32

3394 ± 53

5105 ± 216

B C

63.7 ± 1.2 101.7 ± 1.2

1822 ± 24 2064 ± 86

3581 ± 68 3839 ± 29

5143 ± 66 5390 ± 94

respectively, for 226Ra. The relative expanded uncertainties were calculated by methodology as described in ‘‘GENIE 2000 Customization Tools Manual’’ [42]. Table 5 show soil properties of A, B and C soils. The values are presented as mean values with standard deviations of 4 replicates taken from each contamination treatment as described in ANOVA experimental design. Plants 238


U activity concentrations in Chinese cabbage grown in different soils at various contamination levels were in the range from 1.0–2.3 and 2.3–4.7 Bq kg-1 dry mass for 40 and 60 % of UMT content in the soil, respectively, as shown in Fig. 1a. 238U activity concentrations in control plants were below the detection limit. The relative expanded uncertainties with coverage factor k = 2 for the measured 238U in plants were from 8 to 19 % for contaminated samples as calculated by methodology of the program Kayzero for Windows, KayWin [38]. 238U activity concentrations in plants from soil A at 20, 40 and 60 % of UMT content in the soil, respectively and from B and C soils at 20 % of UMT content in the soil are not shown due to the lack of measurement data as the sample quantity in pots was too low for the measurements. 238 U concentration ratios in Chinese cabbage grown in different soils at various contamination levels ranged from 0.002–0.005 and 0.003–0.006 for 40 and 60 % of UMT content in the soil, respectively, as shown in Fig. 1b. Correlations were tested among 238U activity concentrations in Chinese cabbage and soil properties for the plants grown in soil B. Positive or negative linear correlations were found between 238U activity concentrations in Chinese cabbage and the soil content of available P2O5 (r = -0.9803; p = 1.879E-5), available K2O (r = -0.9075; p = 0.0018), organic matter content (r = -0.9562; p = 0.0002), CEC (r = 0.9236; p = 0.0011), organic C (r = -0.9519; p = 0.0003), total N (r = -0.8775; p = 0.0042) and C/N (r = -0.7638; p = 0.0274).

No significant correlation was found between 238U activity concentration in Chinese cabbage and pH of this soil. No correlation was tested for A and C soils due to the lack of experimental data. Activity concentrations of 226Ra in Chinese cabbage grown in different soils at various contamination varied from 56–276, 156–502 and 277–877 Bq kg-1 dry mass for 20, 40 and 60 % of UMT content in the soil, respectively, as shown in Fig. 2a. 226Ra activity concentrations in control plants were below the detection limit, which was around 1.1 Bq kg-1. The relative expanded uncertainties with coverage factor k = 2 for the measured 226Ra in plants were 5–7 % for contaminated samples, as calculated by methodology described in ‘‘GENIE 2000 Customization Tools Manual’’ [42]. Concentration ratios for 226Ra in Chinese cabbage grown in different soils at various contamination levels varied from 0.031–0.158, 0.041–0.148 and 0.024–0.172 for 20, 40 and 60 % of UMT content in the soil, respectively, as shown in Fig. 2b. Negative linear correlations were found between 226Ra activity concentration in Chinese cabbage and the cabbage biomass for 20 % (r = -0.6769; p = 0.0156), 40 % (r = -0.6646; p = 0.0257) and 60 % (r = -0.8726; p = 0.0047) of UMT content in the soil, respectively. Positive or negative linear correlations were found: between 226Ra activity concentration in Chinese cabbage and the soil content of available P2O5 (r = -0.6901; p = 0.0188), available K2O (r = -0.6029; p = 0.0496), organic matter content (r = -0.7443; p = 0.0086), CEC (r = 0.6823; p = 0.0207), organic C (r = -0.7464; p = 0.0083), total N (r = -0.5929; p = 0.0545) and C/N (r = -0.7686; p = 0.0057) for plants from soil B and between 226Ra activity concentration in Chinese cabbage and the soil content of available P2O5 (r = -0.7737; p = 0.0032), available K2O (r = -0.7685; p = 0.0035), organic matter content (r = -0.8038; p = 0.0016), CEC (r = 0.7605; p = 0.0041), organic C (r = -0.7966; p = 0.0019), total N (r = -0.8006; p = 0.0018) and C/N

123

690


Table 5 Soil properties of UMT-contaminated and control soils Soil

Pedological parameter

A

pH in CaCl2



4.33 ± 0.05

4.90 ± 0.08

5.70 ± 0.08

6.18 ± 0.10

Avail P2O5 [mg kg ]

79.3 ± 16.0

71.5 ± 2.9

63.5 ± 3.7

59.8 ± 1.3

Avail K2O [mg kg-1]

129.0 ± 18.9

94.8 ± 5.7

73.8 ± 2.4

59 ± 2

4.18 ± 0.28

3.33 ± 0.21

2.60 ± 0.22

1.38 ± 0.05

Organic C [%]

2.43 ± 0.15

1.93 ± 0.13

1.50 ± 0.14

0.80 ± 0.00

Total N [%]

0.31 ± 0.01

0.32 ± 0.12

0.21 ± 0.02

0.17 ± 0.03

C/N CEC [cmol kg-1]

7.90 ± 0.70 201.0 ± 7.1

6.63 ± 1.88 374.3 ± 23.2

7.18 ± 0.59 541.8 ± 17.6

4.85 ± 0.77 717.3 ± 20.3

Exch Ca [%]

25.03 ± 6.18

69.53 ± 2.65

85.88 ± 0.68

93.33 ± 0.43

Exch Mg [%]

2.7 ± 0.6

1.5 ± 0.3

1.3 ± 0.5

0.5 ± 0.2

1.75 ± 0.21

0.70 ± 0.08

0.40 ± 0.00

0.20 ± 0.00

Exch K [%] Exch Na [%]

0.38 ± 0.05

0.25 ± 0.10

0.15 ± 0.06

0.10 ± 0.00

Exch H [%]

69.90 ± 5.63

28.00 ± 2.32

12.30 ± 0.55

5.83 ± 0.48

pH in CaCl2

6.85 ± 0.10

6.83 ± 0.10

Avail P2O5 [mg kg-1]

313.0 ± 7.8

6.90 ± 0.08

295.8 ± 11.2

247.0 ± 13.6

193.5 ± 9

Avail K2O [mg kg-1]

204.0 ± 12.7

168.5 ± 9.8

139.3 ± 7.3

103.3 ± 4.6

Organic matter [%]

5.85 ± 0.26

4.68 ± 0.05

3.18 ± 0.28

6.85 ± 0.06

2.05 ± 0.31

Organic C [%]

3.40 ± 0.14

2.70 ± 0.00

1.83 ± 0.15

1.20 ± 0.18

Total N [%]

0.44 ± 0.04

0.36 ± 0.04

0.29 ± 0.01

0.20 ± 0.02

C/N

C


-1

Organic matter [%]

B

Control soil

6.43 ± 0.62

6.05 ± 0.99

CEC [cmol kg-1]

288.0 ± 17.1

7.78 ± 0.64

425.5 ± 7.8

7.50 ± 0.75

557.5 ± 22.8

721.5 ± 13.9

Exch Ca [%] Exch Mg [%]

72.28 ± 0.96 14.1 ± 1.2

83.75 ± 0.66 8.0 ± 0.7

90.15 ± 0.90 4.6 ± 0.6

94.48 ± 0.28 2.4 ± 0.3

Exch K [%]

1.80 ± 0.18

0.95 ± 0.06

0.63 ± 0.05

0.35 ± 0.06

Exch Na [%]

0.60 ± 0.08

0.43 ± 0.05

0.25 ± 0.06

0.20 ± 0.00

Exch H [%]

11.08 ± 1.18

6.80 ± 0.47

4.33 ± 0.53

2.58 ± 0.21

pH in CaCl2

6.75 ± 0.13

6.70 ± 0.14

6.70 ± 0.14

6.73 ± 0.13

-1

Avail P2O5 [mg kg ]

241.8 ± 35.2

197.8 ± 23.8

163.5 ± 7.2

124.3 ± 7.8

Avail K2O [mg kg-1]

299.5 ± 17.3

221.5 ± 8.0

176.5 ± 3.1

131.3 ± 6.4

Organic matter [%]

9.65 ± 0.33

6.98 ± 0.26

5.00 ± 0.32

3.28 ± 0.15

Organic C [%]

5.58 ± 0.19

4.05 ± 0.17

2.90 ± 0.18

1.93 ± 0.10

Total N [%]

0.58 ± 0.01

0.45 ± 0.03

0.35 ± 0.02

0.25 ± 0.01

C/N

9.58 ± 0.32

9.13 ± 0.24

8.25 ± 0.66

7.73 ± 0.70

CEC [cmol kg-1]

336.8 ± 14.2

483 ± 8

607.8 ± 18.1

776.8 ± 54.5

Exch Ca [%]

63.38 ± 1.58

79.65 ± 0.66

87.15 ± 0.76

92.48 ± 0.82

Exch Mg [%]

19.1 ± 0.9

10.6 ± 0.9

6.6 ± 1.1

3.8 ± 1.1

Exch K [%]

2.15 ± 0.17

1.10 ± 0.14

0.68 ± 0.05

0.43 ± 0.05

Exch Na [%] Exch H [%]

0.20 ± 0.00 15.00 ± 0.90

0.15 ± 0.06 8.45 ± 0.57

0.10 ± 0.00 5.35 ± 0.90

0.10 ± 0.00 3.25 ± 0.53

Avail available, Exch exchangeable

(r = -0.6025; p = 0.0382) for plants from soil C. No significant correlations were found between 226Ra activity concentration in Chinese cabbage and pH of soils B and C, as well as between 226Ra activity concentration in Chinese cabbage and soil properties of soil A.

123

Soil-to-plant transfer of

238

U

Uptake of 238U by Chinese cabbage was low at all levels of UMT contamination (Table 3; Fig. 1a). Activity concentrations of 238U in Chinese cabbage did not differ


Fig. 1 Mean activity concentrations of 238U in Chinese cabbage grown in different soils at various levels of UMT content in the soil (a); Mean concentration ratios of 238U in Chinese cabbage grown in different soils at various levels of UMT content in the soil (b). Error bars depict standard deviations around the mean; n = 4

significantly between soils B and C, both at 40 % (p [ 0.05) and 60 % (p [ 0.05) of UMT content in the soil, but differed significantly between the levels of UMT contamination (p = 0.0035), resulting in higher 238U uptake found in more contaminated soil. 238U in Chinese cabbage was directly related with CEC in the soil which might be explained by higher exchange of 238U from soil colloids to the soil solution in UMT-contaminated soil and higher root uptake. CEC was already reported in the literature as an important soil parameter affecting the plant uptake of natural radionuclides [8]. Negative linear correlations were found between 238U activity concentration in Chinese cabbage and the soil content of available P2O5 and K2O, organic matter content, total N, organic C and C/N which indicates that reduced 238U uptake may be possible at increased values of tested soil parameters in UMTcontaminated soils. Low uptake of 238U may be attributed to the fact that majority of uranium was extracted from

691

Fig. 2 Mean activity concentrations of 226Ra in Chinese cabbage grown in different soils at various levels of UMT content in the soil (a); Mean concentration ratios of 226Ra in Chinese cabbage grown in different soils at various levels of UMT content in the soil (b). Error bars depict standard deviations around the mean; n = 4

UMT by chemical treatment thus maintaining, in the contaminated soils (Table 5), the remaining U in a biologically mostly inaccessible form, as well as low nutrient availability. However, the plant tolerance mechanism where the metals are excluded from entering the root tissue [43] or adsorption and complexation processes of 238U in the soil [7] may also reduce the root uptake of 238U. Concentration ratios (Fig. 1b) did not differ significantly between soils B and C at 40 % (p [ 0.05) and 60 % (p [ 0.05) of UMT content in the soil, but differed significantly between the levels of UMT contamination (p = 0.0320) leading to conclusion that the soil-to-plant transfer of 238U is more affected by the UMT contamination than by soil properties in this particular experiment. The maximum CR value was 0.006, which is about 30 times lower than the reported literature value for Chinese cabbage in U-contaminated soil [7]. However, the low activity concentrations of 238U in Chinese cabbage should be considered as a specific result of this experiment and could be related to particular soil environment while under different growing conditions, higher transfer of 238U to

123

692


Chinese cabbage can occur as shown in several studies concerned with various plant species [16, 22, 23]. Therefore, caution should be advised when growing Brassica crops at the mine areas potentially contaminated by uranium due to possible transfer of 238U to food chain from more contaminated soil and the related dose to the nearby living organisms.

Soil-to-plant transfer of

is as essential macro element [46], due to their analogue chemical behaviour [44]. The observed uptake of 226Ra in UMT-contaminated soil indicates that potential risk of internal radiation exposure to nearby living organisms should be considered in areas contaminated with UMT. Our particular study confirmed high 226Ra transfer from soil to Chinese cabbage, as being reported for other plants growing near or on a uranium mill tailings wastes [13–21].

226

Ra

Conclusions Uptake of 226Ra by Chinese cabbage was enhanced for all levels of UMT contaminated soils (Table 4; Fig. 2a) compared to control plants having 226Ra levels below the detection limit. Activity concentrations of 226Ra in Chinese cabbage were different for each soil and resulted in statistically significant differences between soils A, B and C at 20 % (p = 0.0008), barely significant differences at 40 % (p = 0.0505) and non-significant differences at 60 % (p [ 0.05) of UMT content in the soil. 226Ra activity concentration in Chinese cabbage correlated with CEC, which indicates that CEC may be one of the reasons for 226 Ra transfer to Chinese cabbage despite of its nonessential role in the plants. This correlation also suggests that a high fraction of exchangeable 226Ra is probably present in UMT-contaminated soil and therefore available for the root uptake. This assumption could also be confirmed by presence of relatively high levels of 226Ra similar exchangeable cations, such as Ca [44] in these soils (Table 5). Increased CEC levels are expected to result in higher exchange of 226Ra from soil colloids to the soil solution and consequently higher 226Ra uptake from more contaminated soil. Negative correlations between 226Ra activity concentration in Chinese cabbage and the content of available P2O5, K2O, organic matter, total N, organic C and C/N in soil indicate that reduced 226Ra uptake may occur at increased values of the tested soil parameters. The highest transfer of 226Ra to Chinese cabbage was observed for soil A, which can be explained by the reduction of 226Ra activity concentration in the plants with higher biomass production, as confirmed by negative correlation between 226 Ra activity concentration and the cabbage biomass. Concentration ratios (Fig. 2b) differed significantly among soils A, B and C at 20 % (p = 0.0003) and 40 % (p = 0.0299) of UMT content in the soil, as also reported by Vandenhove and Van Hees [8]. However, non-significant differences were observed among the tested soils at 60 % (p [ 0.05) of UMT content in the soil. The CR values were in agreement with the literature data range from 0.022 to 0.068 for Brassica plants grown in soils contaminated with UMT [21]. It is suggested that Chinese cabbage take-up 226Ra as a substitute ion of Ca [45], which

123

Chinese cabbage was used for the determination of 238U and 226Ra soil-to-plant transfer. The applied experimental design was shown as appropriate for the evaluation of radionuclide concentration ratios for UMT contaminated soils as confirmed by significant linear correlations between radionuclides in plants and soil properties. The study revealed the capabilities of Chinese cabbage to accumulate 238U and 226Ra in the edible parts from soils contaminated with UMT despite the non-essential role of those radionuclides in the plants. Soil-to-plant transfer was higher for 226Ra and lower for 238U. Low uptake of 238U may be related to specific characteristics of UMT (as most of the chemically available uranium had been previously extracted by technological process), plant resistance mechanism and adsorption or complexation processes of 238 U in the soil. 238U concentration ratios were lower compared to those found in the literature for Brassica plants, while the 226Ra CR values were comparable to the literature data. The higher soil-to-plant transfer of 226Ra could partly be attributed to its chemical characteristic, behaving similar as Ca, which is continuously taken-up by plants as an essential macro element. 226 Ra activity concentration in plants was decreasing with an increased biomass of the plants. CEC was found as important factor affecting the availability of 238U and 226Ra to Chinese cabbage while the opposite observation was noted for other soil properties such as the content of available P2O5 and K2O, organic matter content, total N, organic C and C/N ratio, which may reduce the root uptake of 238U and 226Ra in the UMT-contaminated soils. The study showed that soil-to-plant transfer of 238U and 226 Ra depend on particular radionuclide, radionuclide activity concentration and soil properties, as shown by different ranges of concentration ratios for each radionuclide in Chinese cabbage growing in different growing conditions at various contamination levels. Understanding of soil-to-plant transfer of natural radionuclides in contaminated areas is very important to ensure that instead of default CR values the more accurate site-specific values are adopted for the relevant calculations, thus improving the correctness of dose assessments.


In further studies, potential availability of particular radionuclides to plants, by performing e.g. sequential extraction procedures, should also be considered for better elucidation of mechanisms and processes involved in their plant uptake from the soil. Further investigations are required, due to lack of accurate data, for the quantification of radionuclide concentration ratios for other plant species, especially the ones of agronomic and/or potential phytoremediation importance. Also, other radionuclides from natural decay series should be considered to complement dose contributions. It is also suggested to determine concentration ratios for various trace- or macro-elements as they may also clarify environmental behaviour of some important fission products such as 90Sr or 137Cs. Acknowledgments This work was financially supported by the Slovenian Research Agency (contract No. P2-0075). The authors would like to thank Mr. Jozˇe Rojc of the Rudnik Zˇirovski vrh company for his cooperation and the Centre for Pedology of the Agronomy Department, Biotechnical faculty, University of Ljubljana, for soil characteristics determination.

References 1. Benedik L, Klemencˇicˇ H, Repinc U, Vrecˇek P (2003) Uranium and its decay products in samples contaminated with uranium mine and mill wastes. J Phys IV France 107:147–150 2. Stegnar P, Shishkov I, Burkitbayev M, Tolongutov B, Yunsov M, Radyuk R, Salbu B (2012) Assessment of the radiological impact of gamma and radon dose rates at former U mining sites in Central Asia. J Environ Radioact 123:3–13 3. Vandenhove H, Sweeck L, Mallants D, Vanmarcke H, Aitkulov A, Sadyrov O, Savosin M, Tolongutov B, Mirzachev M, Clerc JJ, Quarch H, Aitaliev A (2006) Assessment of radiation exposure in the uranium mining and milling area of Mailuu Suu, Kyrgyzstan. J Environ Radioact 88:118–139 4. Sˇtrok M, Smodisˇ B (2010) Fractionation of natural radionuclides in soils from the vicinity of a former uranium mine Zˇirovski vrh, Slovenia. J Environ Radioact 101:22–28 5. Tamponnet C, Martin-Garin A, Gonze M-A, Parekh N, Vallejo R, Sauras-Year T, Casadesus J, Plassard C, Staunton S, Norden M, Avila R, Shaw G (2008) An overview of BORIS: bioavailability of radionuclides in soil. J Environ Radioact 99:820–830 6. Parekh NR, Poskitt JM, Dodd BA, Potter ED, Sanchez A (2008) Soil microorganisms determine the sorption of radionuclides within organic soil systems. J Environ Radioact 99:841–852 7. Shahandeh H, Hossner LR (2002) Role of soil properties in phytoaccumulation of uranium. Water Air Soil Pollut 141: 165–180 8. Vandenhove H, Van Hees M (2007) Predicting radium availability and uptake from soil properties. Chemosphere 69:664–674 9. Ehlken S, Kirchner G (2002) Environmental processes affecting plant root uptake of radioactive trace elements and variability of transfer factor data: a review. J Environ Radioact 58:97–112 10. Colle C, Mandoz-Escande C, Leclerc E (2009) Foliar transfer into the biosphere: a review of translocation factors to cereal grains. J Environ Radioact 100:683–689 11. Pro¨hl G (2009) Interception of dry and wet deposited radionuclides by vegetation. J Environ Radioact 100:675–682

693 12. Greger M (2008) In: Prasad MNV (ed) Trace elements as contaminants and nutrients: consequences in ecosystems and human health. Wiley, New Jersey 13. Cˇerne M, Smodisˇ B, Sˇtrok M, Jacímovic´ R (2010) Accumulation of 238U, 226Ra and 230Th by wetland plants in a vicinity of U-mill tailings at Zˇirovski vrh (Slovenia). J Radioanal Nucl Chem 286:323–327 14. Sˇtrok M, Smodisˇ B, Eler K (2011) Natural radionuclides in trees grown on a uranium mill tailings waste pile. Environ Sci Pollut Res 18:819–826 15. Sˇtrok M, Smodisˇ B (2013) Soil-to-plant transfer factors for natural radionuclides in grass in the vicinity of a former uranium mine. Nucl Eng Design 261:279–284 16. Petrova R (2006) In: Merkel BJ, Hasche-Berger A (eds) Uranium in the environment. Springer, Heidelberg 17. Popa K, Tykva R, Podracka´ E, Humelnicu D (2008) 226Ra translocation from soil to selected vegetation in the Crucea (Romania) uranium mining area. J Radioanal Nucl Chem 278:211–213 18. Madruga MJ, Brogueira A, Alberto G, Cardoso F (2001) 226Ra bioavailability to plants at the Uregiriça uranium mill tailings site. J Environ Radioact 54:175–188 19. Tykva R, Podracka´ E (2005) Bioaccumulation of 226Ra in the plants growing near uranium facilities. Nukleonika 50:S25–S27 20. Carvalho FP, Oliveira JM, Neves MO, Abreu MM, Vicente EM (2009) Soil to plant (Solanum tuberosum L.) radionuclide transfer in the vicinity of an old uranium mine. Geochem Environ Anal 9:275–278 21. Soudek P, Petrova´ Sˇ, Benesˇova´ D, Kotyza J, Va´gner M, Vanˇkova R, Vane˘k T (2010) Study of soil-plant transfer of 226Ra under greenhouse conditions. J Environ Radioact 101:446–450 22. Stojanovic´ MD, Mihajlovic´ ML, Milojkovic´ JV, Lopicˇic´ ZR, Adamovic´ M, Stankovic´ S (2012) Efficient phytoremediation of uranium mine tailings by tobacco. Environ Chem Lett 10:377–381 23. Petrescu L, Bilal E (2003) Plant availabilty of uranium in contaminated soil from Crucea Mine (Romania). Environ Geosci 10(3):123–135 24. Huang JW, Blaylock MJ, Kapulnik Y, Ensley BD (1998) Phytoremediation of uranium-contaminated soils: role of organic acids in triggering uranium hyperaccumulation in plants. Environ Sci Technol 32(13):2004–2008 25. Ebbs SD, Brady DJ, Kochian LV (1998) Role of uranium speciation in the uptake and translocation of uranium by plants. J Exp Bot 49:1183–1190 26. Duque`ne L, Vandenhove H, Tack F, Meers E, Baeten J, Wannijn J (2009) Enhanced phytoextraction of uranium and selected heavy metals by Indian mustard and ryegrass using biodegradable soil amendments. Sci Total Environ 407:1496–1505 27. Choi M-S, Lin X-J, Lee S-A, Kim W, Kang H-D, Doh S-H, Kim D-S, Lee D-M (2008) Daily intakes of naturally occurring radioisotopes in typical Korean foods. J Environ Radioact 99: 1319–1323 28. Vamerali T, Bandiera M, Mosca G (2010) Field crops for phytoremediation of metal-contaminated land. A review. Environ Chem Lett 8:1–17 29. Krizˇman M, Byrne AR, Benedik L (1995) Distribution of 230Th in milling wastes from the Zˇirovski vrh uranium mine (Slovenia) and its radioecological implications. J Environ Radioact 26:223–235 30. Currie LA (1968) Limits for qualitative detection and quantitative determination. Anal Chem 40:586–593 31. Taylor BN, Kuyatt CE (1994) NIST technical note 1297 guidelines for evaluating and expressing the uncertainty of NIST measurement results. U. S. Government Printing Office, Washington

123

694 32. Vidmar T (2005) EFFTRAN: a Monte Carlo efficiency transfer code for gamma-ray spectrometry. Nucl Instrum Methods A 550:603–608 33. Gilmore GR (2008) Practical gamma-ray spectrometry. Wiley, England 34. Jovanovic´ S, Dlabac A, Mihaljevic N (2010) ANGLE v2.1-New version of the computer code for semiconductor detector gammaefficiency calculations. Nucl Instrum Methods A 622:385–391 35. Jacímovic´ R (2003) Evaluation of the use of the TRIGA Mark II reactor for the k0-method of activation analysis (in-Slovene), PhD Thesis, University of Ljubljana 36. HyperLab 2002 System (2002) Installation and quick start guide. HyperLabs Software, Budapest 37. Jacímovic´ R, Smodisˇ B, Bucˇar T, Stegnar P (2003) k0-NAA quality assessment by analysis of different certified reference materials using the KAYZERO/SOLCOI software. J Radioanal Nucl Chem 257:659–663 38. Kayzero for Windows (KayWinÒ), User’s Manual for reactor neutron activation analysis (NAA) using the k0 standardization method, Version 2, November 2005 39. Biasioli M, Grcˇman H, Kralj T, Madrid F, Dıáz-Barrientos E, Ajmone-Marsan F (2007) Potentially toxic elements contamination in urban soils: a comparison of three European cities. J Environ Qual 36:70–79

123

J Radioanal Nucl Chem (2015) 306:685–694 40. Ajmone-Marsan F, Biasioli M, Kralj T, Grcˇman H, Davidson CM, Hursthouse AS, Madrid L, Rodrigues S (2008) Metals in particle-size fractions of the soils of five European cities. Environ Pollut 152:73–81 41. Vodnik D, Grcˇman H, Macˇek I, van Elteren JT, Kovacˇevicˇ M (2008) The contribution of glomalin related-soil protein to Pb and Zn sequestration in polluted soil. Sci Total Environ 392:130–136 42. GENIE 2000 Spectroscopy Software: Customization Tools (2000) Canberra industries. GENIE 2000 Spectroscopy Software: Customization Tools, Meriden 43. Ann Peer W, Baxter IR, Richards EL, Freeman JL, Murphy AS (2005) In: Tama´s MJ, Martinoia E (eds) Molecular biology of metal homeostasis and detoxification: topics in curent genetics. Springer, Berlin 44. Gerzabek MH, Strebl F, Temmel B (1998) Plant uptake of radionuclides in lysimeter experiments. Environ Pollut 99:93–103 45. Tagami K, Uchida S (2009) 226Ra transfer factor from soils to crops and its simple estimation method using uranium and barium concentrations. Chemosphere 77:105–114 46. White PJ, Broadley MR (2003) Calcium in plants. Ann Bot 92:487–511