- Email: [email protected]
Natural radioactivity in winter wheat from organic and conventional agricultural systems
Journal of Environmental Radioactivity 102 (2011) 163e169
Contents lists available at ScienceDirect
Journal of Environmental Radioactivity journal homepage: www.elsevier.com/locate/jenvrad
Natural radioactivity in winter wheat from organic and conventional agricultural systems Patric Lindahl, Alain Maquet, Mikael Hult*, Joël Gasparro, Gerd Marissens, Raquel González de Orduña European Commission, Joint Research Centre, Institute for Reference Materials and Measurements (EC-JRC-IRMM), Retieseweg 111, B-2440 Geel, Belgium
a r t i c l e i n f o
a b s t r a c t
Article history: Received 11 February 2010 Received in revised form 10 October 2010 Accepted 9 November 2010 Available online 8 December 2010
The distribution of natural radionuclides was studied in winter wheat plants collected from three sites in Belgium during 2004e2007. Activity concentrations of 40K, 226Ra, 228Ra and 228Th in organically and conventionally grown wheat, and in the corresponding soil samples, were determined using ultra low-level gamma-ray spectrometry. The observed soil-to-wheat concentration ratios were calculated for the different parts of the wheat plant (root, stem and grain) in the two agricultural systems (organic and conventional). There were large variations in radionuclide activity concentrations between the sites and fields, but no significant difference between conventionally and organically grown wheat plants was observed. Ó 2010 Elsevier Ltd. All rights reserved.
Keywords: Natural radionuclides Wheat Soil Organic farming Conventional farming
1. Introduction Radionuclides from the natural decay series (238U, 232Th and U) are present in the environment in different forms and quantities. Together with 40K, considerable amounts of these natural radionuclides and their daughter products can be found in soil with varying activity concentrations depending on the region and soil type. The reported average soil activity concentrations in Belgium for 40K, 226Ra and 232Th are 380 Bq kg1, 26 Bq kg1 and 27 Bq kg1, respectively, with large ranges in activity concentrations due to natural variability (UNSCEAR, 2000). These radionuclides may be absorbed, along with essential nutrients, by plant roots and transported to other parts of the plant. The uptake of radionuclides in terrestrial plants is mainly dependent on the soil characteristics, plant type and the individual chemical properties of the radionuclides in the soil matrix (Ehlken and Kirchner, 2002). In addition, external factors such as the climate and agricultural practices may also influence plant uptake of radionuclides. In recent years the importance of organic farming methods has increased due to growing consumer interest for certified organic products (Willer and Kilcher, 2009), hence the importance of valid analytical methods for the authentication of organic food products (Siderer et al., 2005). The organic farming systems aim to restrict the use of mineral fertilisers and chemical pesticides, and are mainly 235
* Corresponding author. Tel.: þ 32 14 571269; fax: þ 32 14 584273. E-mail address: [email protected] (M. Hult). 0265-931X/$ e see front matter Ó 2010 Elsevier Ltd. All rights reserved. doi:10.1016/j.jenvrad.2010.11.007
based on long-term naturally occurring biological processes. The conventional farming methods focus on immediate and isolated effects (i.e. not emulating living ecological systems and cycles) to increase the crop output by adding different types of synthetic inputs. Depending on the raw materials and the processing of the fertiliser, the synthetic input may contain enhanced levels of natural radionuclides in different chemical compounds (Righi et al., 2005; Khater and Al-Sewaidan, 2008) and hence may alter the overall radioactivity in the soil. This may affect the radionuclide uptake within the crop. It is a well known phenomenon that the phosphate ores that are used for the production of fertilisers contain significantly increased concentrations of uranium and thorium traces (Falck and Wymer, 2006). The activity level is strongly depending on the origin of the ores. There is also a strong difference between the geological formations from which the ore is extracted. The processing of the ores to fertilisers has also an impact on the radionuclide concentration. In most cases the uranium concentration will be increased, while on the contrary, the radium concentration will be reduced (Falck and Wymer, 2006). There is no clear trend for the evolution of the thorium concentration. One could suggest that due to the increased levels of natural radionuclides (40K and the 238, 235U and 232Th decay chains) in many types of synthetic fertilisers, one should be able to distinguish organic and conventional food products from each other by measuring the content of natural radionuclides. There are, however, many factors contributing to the amount of natural radioactivity taken up by plants (Golmakani et al., 2008) among them those related to the plant itself like the plant species, age of plant
164
P. Lindahl et al. / Journal of Environmental Radioactivity 102 (2011) 163e169
parts, depth of roots, etc. or to the soil like the kind of soil, organic matter content, pH, CEC, etc, or to the radionuclides (e.g. chemical form, mobility). Additionally, in recent years the use of synthetic fertilisers has been somewhat reduced (EFMA, 2005). There exist also practices at organic farms to use natural mineral fertilisers, which lead to further reduction in potential differences in radioactivity concentrations in crop from conventional and organic farming. In 2004, the Institute for Reference Materials and Measurements (IRMM) started field experiments to obtain suitable environmental crop samples for the development of a range of analytical techniques to distinguish between organic and conventional farming. As a part of this project, winter wheat grown in organic and conventional systems was collected and analysed during 2004e2007. The particular part of that project which is presented here aims to determine and compare the natural radionuclide contents in different parts of the wheat plant and the corresponding soil collected from organic and conventional agricultural systems. Four main approaches (i.e. retail purchase comparison, fertiliser treatment comparisons, whole farm comparisons, or animal feeding and human health) are used when comparing the two agricultural systems with their advantages and disadvantages and complement each other in terms of the statement they can make (Magkos et al., 2003). Farm studies are conducted on products from selected farms with different forms of cultivation for which the production conditions are recorded (Woese et al., 1997). A mean number of samples can be examined. Environmental factors such as climate and soil conditions can be made suitable for comparison by selecting neighbouring farms. The disadvantage of this method is that the accuracy of the information given cannot be verified. Another problem is that it is very difficult to select the farms and fields in such a manner that they truly represent the cultivation forms which are to be compared. 2. Materials and methods
same field. During the first two years of the study, only one site was selected. In 2004, site 2 was studied while in 2005 site 3 was studied. During the last two years of the study, the number of sites was increased to three. However, in site 3 in 2007 only samples from a conventional field were available due to difficulties in preparing the organic field. Each field was ploughed before sowing except the organic field of site 2 in 2007, which was without any tillage. In 2004 (site 2), the varieties "Bussard" and "Monopol" were sown as a 50/50 mixture in the organic field and the variety "Napier" was sown in the conventional field. During the period 2005e2007 all samples were from the variety "Cubus". Table 1 is showing the fertilisation practices for the selected fields. For each field, three sectors of about 8 8 m2 were delimited and separated by approximately 10 m. Within each sector, 35e40 plants were collected. The plants were separated into three parts (shallow root, stem and grain) and carefully cleaned with distilled water to remove any soil residue. During 2004 and 2007, only the grain was analysed and during 2005 the stem and grain were analysed. Additional root samples were analysed in the 2006 sampling campaign together with stem and grain. The root samples were cleaned with distilled water twice and any visible soil residue was removed manually. For each field, the amount of sample (mixture of three sectors per field) used for the radionuclide analysis were usually ∼1 g, ∼25 g and ∼50 g (dry weight) for root, stem and grain, respectively. The different plant parts were ground, homogenised and dried for 24 h at 80 C before being placed in cylindrical airtight Teflon containers for gamma-ray measurements. Six soil samples (layer 0e30 cm) were extracted from each field (2 from each sector) using a drill, these were then mixed and homogenised to obtain samples representative of each field. From each mixture, three sub-samples (∼100 g each) were dried for 24 h at 80 C and placed in cylindrical airtight Teflon containers for radionuclide analysis by gamma-ray spectrometry. The remaining homogenised soil sample was analysed by the Belgian Soil Science Service (BSSS) in Leuven, Belgium to determine the soil characteristics of each field. 2.2. Soil characteristics The soil characteristics are presented in Table 2. The fields in this study are characterised by a loamy soil (particle size < 50 mm) percentage higher than 45% and a clay (particle size < 2 mm) percentage lower than 30% except for the conventional field at site 2 (2004) which was at the limit between loamy and clay soil based on the Jamagne’s triangular diagram of soil texture. The combination of fertility and Table 1 Fertilisation practices for the selected fields used for winter wheat sampling in Belgium during 2004e2007.
2.1. Sampling and preparation Fertilisation Soil and mature winter wheat (Triticum aestivum L.) plants were collected during 2004e2007 from three regions in the south of Belgium (Fig. 1): 1) Marche-enFamenne, 2) Soignies, and 3) Ciney. The sampling sites were selected in collaboration with the National Union of Belgian Organic Farmers (UNAB) with one certified organic farmer and one conventional farmer for each site. Each site consisted of one organic and one conventional field in close proximity. Due to the rotation of crop types, it is not possible to collect the same crop for two consecutive years from the
Sampling year
AS
Site 1. Marche-en-Famenne 2006 O 27 Jul C 27 Jul 2007
O C
Site 2. Soignies 2004 O C
4 Aug 4 Aug
5 Sep 9 Aug
2006
O C
27 Jul 28 Jul
2007
O C
3 Aug 3 Aug
Site 3. Ciney 2005 O C
Fig. 1. Map showing sampling sites of organic and conventional grown winter wheat and corresponding soil collected during 2004e2007.
Harvest date
18 Aug 17 Aug
2006
O C
1 Aug 26 Jul
2007
C
27 Jul
Commercial name and composition (N/P/K þ MgO)
Amount applied
Orgaminea (7/5/10 þ 2)b i) Kemira (26/6/6)b ii) Nitrate 27% Orgamine (7/5/10 þ 2)b i) Mixture 1 (14/7/20 þ 3)b ii) Mixture 2 (23/5/5)b iii) Nitrates 27%
300 500 270 400 350 250 250
No fertiliser i) N solution (39/0/0)b ii) Potassium Chloride (40% þ 6 MgO þ 5 Na2O) iii) N 22% þ MgO 7% Orgamine (7/5/10 þ 2)b i) KCl 60 ii) N solution (39/0/0) b iii) Nitrate 27% Orgamine (7/5/10 þ 2)b i) N solution (39/0/0)b ii) Nitrate 27%
No fertiliser 250 L ha1 290 kg ha1
Liquid manure of bovine i) N solution (39/0/0)b ii) Nitrate 27% No fertiliser i) N solution (30/0/0)b ii) Nitrate 27% Nitrate 27%
10000 L ha1 300 L ha1 300 kg ha1 No fertiliser 320 L ha1 190 kg ha1 690 kg ha1
370 400 200 375 225 300 300 300
kg kg kg kg kg kg kg
ha1 ha1 ha1 ha1 ha1 ha1 ha1
kg ha1 kg ha1 kg ha1 L ha1 kg ha1 kg ha1 L ha1 kg ha1
AS: Agricultural system, O: Organic farming, C: Conventional farming. a Orgamine is distributed by ATBE in Chartres de Bretagne, France. b NPK formula: the three numbers indicate the percent of nitrogen (N), P2O5 and K2O.
P. Lindahl et al. / Journal of Environmental Radioactivity 102 (2011) 163e169 moisture-holding capacity with good drainage makes loamy soil systems an excellent medium for growing wheat. The pH (KCl) which is a fundamental property controlling biological and chemical processes in the soil was generally within the target zone for such soil types (target zone: pH 6.2e7.3) (Vandendriessche et al., 1996). Cation exchange capacity (CEC) is an important property of soil and is directly related to soil texture. Soil particles are negatively charged, which allows the soil to prevent cations from being leached away. A CEC greater than 10 cmol kg1 was observed across all sites indicating good base cation holding capabilities, except for the conventional field at site 2 in 2007 and the organic field at site 3 in 2005 (Table 2).
165
Table 3 Decision thresholds for the analysed radionuclides by gamma-ray spectrometry following ISO (2000) with a ¼ 0.05. The soil data refers to measurements above ground and the rest refers to measurements below ground in HADES. Sample type
Sample mass (g)
Soil Root Stem Grain
100 1 25 50
Decision threshold, Bq kg1 [a ¼ 0.05] 137
2.3. Gamma-ray spectrometry The radionuclide activity concentrations in the winter wheat samples collected during 2005e2007 were determined using ultra low background HPGe-detectors installed at the underground research facility HADES (Hult et al., 2006). The facility is located at a depth of 225 m (500 m water equivalent) below ground level at the Belgian Nuclear Research Centre in Mol, Belgium. The detectors are constructed using materials selected for a high degree of radiopurity and shielded with electrolytic copper and low-activity lead. The 2004 wheat samples were measured above ground with a Compton-suppression detector located at ITU (Institute for Transuranium Elements), as part of an initial collaboration (Peerani et al., 2002) and the 2005 samples were measured above ground with a low background HPGedetector. Due to the higher detection limits of the above ground measurements during 2005, only 40K was detectable in the wheat samples. All soil samples were measured above ground with the same low background HPGe-detector. The grain, stem and root samples were measured for ∼2 weeks and the soil samples for ∼5 days. Since the activity concentrations for the radionuclides reported in this study was higher in the soil samples than in the wheat samples, it was possible to measure the soil above ground and obtain adequate counting statistics within a shorter measurement time. The samples were stored for a minimum of three weeks before measurement to ensure secular equilibrium between 226Ra and its daughters since the half-life of the first daughter, 222Rn, is 3.8 days. The samples were measured in standard Teflon sample containers and the counting efficiencies, for each container, were calculated by Monte Carlo simulation using the EGS4 code (Nelson et al., 1985). The main uncertainty contributions were from detection efficiency and (for certain samples and radionuclides) counting statistics. Uncertainties from the efficiency determination varied between the detectors in the range 4%e8%. Measurements were carried out for up to two weeks per sample to obtain sufficient counting statistics for the major peaks. The activities were determined by measuring the daughter radionuclides (in parentheses) of 226Ra (214Pb and 214Bi), 228 Ra (228Ac), 228Th (212Pb and 208Tl) and 238U (234Th) assuming secular equilibrium. The weighted average was used for the different peaks from the daughter nuclides to determine the final activity concentrations for the radionuclides of interest. The 228 Ra and 228Th activities were decay corrected for the time between sampling and measurement. The activities of 40K and 137Cs were determined using the 1460 keV and 661 keV gamma-ray peaks, respectively. Due to their low-activity concentration in wheat as compared to soil, uranium and 137Cs were not detected in the wheat plant samples, only in the soil samples. Table 3 gives the a posteriori decision threshold following ISO (2000) with alpha ¼ 0.05.
Cs
0.2 0.1 0.06 0.01
40
K
238
1.2 3.5 0.4 0.1
2.1 1.6 0.7 0.4
U
226
228
Ra
0.4 0.6 0.07 0.02
Ra
0.7 0.6 0.3 0.05
228
Th
0.3 0.2 0.06 0.02
the grouping variable had two levels) was performed. All statistical analyses were carried out using Systat 13 (Systat Software Inc., Chicago, U.S.A.). These analyses were applied on radionuclides determined in soils and grains sampled in 2005, 2006 and 2007. Samples collected in 2004 were discarded due to the fact that two different wheat cultivars were grown in the organic field and the conventional one.
3. Results and discussion 3.1. Radionuclides in soil Activity concentrations of natural radionuclides and 137Cs observed in the soil from the three sampling sites are listed in Table 4. The overall average activity concentrations (1 SD) across all sampling years for 40K, 238U, 226Ra, 228Ra and 228Th were 513 111 Bq kg1, 32 4 Bq kg1, 32 6 Bq kg1, 40 10 Bq kg1, 41 11 Bq kg1, respectively. These values correspond well with the worldwide averages of 400 Bq kg1, 35 Bq kg1, 35 Bq kg1 and 30 Bq kg1 for 40K, 238U, 226Ra and 232Th (UNSCEAR, 2000), and with average activity concentrations reported in Belgium (see Section 1). The 137Cs activity concentration in soil showed an overall average activity concentration and standard deviation (1 SD) of 8 5 Bq kg1, reflecting the local variation of fallout 137Cs at the study sites, which was mainly dependent on the precipitation after the Chernobyl accident. The southernmost site (Number 1) had the highest average 137Cs activity concentration (12.4 2.0 Bq/kg) and the northernmost site (Number 2) had the lowest average 137Cs activity concentration (3.6 0.6 Bq/kg). This agrees well with previously published data on radiocaesium in Belgian soil (Pommé et al., 1998). The two 232Th daughters, 228Ra and 228Th, showed a very strong relationship with almost perfect correlation (r ¼ 0.97, p < 0.01) and the overall 228Ra/228Th activity ratio is very close to unity (1.03 0.08) indicating almost complete secular equilibrium between the daughters of 232Th in the soil. Uranium-238 showed a moderate correlation with 226Ra (r ¼ 0.60, p < 0.01) with an overall 226 Ra/238U activity ratio of 1.0 0.2 indicating secular equilibrium. Uranium is closely associated with the organic matter content in the soil (Vera Tomé et al., 2002) and it has been reported that Ra is linked with the cation exchange capacity (CEC) of the soil (Vandenhove and
2.4. Statistical analysis Normality and equality of variances of the populations were checked using the ShapiroeWilk test and Levene’s test, respectively. When required, the variables were log transformed. Two-way analyses of variance were then performed, testing the effects of the agricultural system and the environment. In case an effect was significant in any particular radionuclide, a Tukey’s test was calculated to make all pairwise mean comparisons. When assumption of normality or homogeneity of variances was not respected, a nonparametric test (i.e. KruskaleWallis test or ManneWhitney test in case Table 2 Soil characteristics for the three sites in Belgium collected during 2004e2007. Characteristics
Site 1
Sampling year
2006
pH (KCl) pH (H2O) CEC (cmol kg1) C (%) Clay (%) Silt (%) Sand (%) Total P (mg kg1) Total N (mg kg1) C/N
Site 2 2007
Site 3
2004
2006
2007
2005
2006
2007
O
C
O
C
O
C
O
C
O
C
O
C
O
C
C
5.6 6.7 17.8 2.4 18.0 68.2 13.8 909 25.4 9.5
5.8 6.7 14.1 2.0 13.0 73.5 13.5 671 19.9 10.1
4.9 5.8 17.1 e 13.2 72.7 14.1 1146 29.8 10.7
6.4 6.6 12.0 e 18.8 68.0 13.2 520 17.6 11.9
6.5 7.2 10.8 1.0 25.0 49.5 25.5 621 11.3 8.8
6.7 7.1 12.0 1.2 30.0 33.7 36.3 737 10.9 11.0
5.4 6.7 18.2 2.2 17.0 68.3 14.7 530 27.7 7.9
6.8 7.9 11.6 1.1 10.6 64.6 24.8 671 19.9 9.4
6.3 7.2 10.3 e 13.2 74.0 12.8 e 10.5 11.4
7.7 7.8 8.4 e 12.2 72.6 15.2 481 11.8 10.2
7.5 7.1 8.4 1.1 13.1 75.3 11.6 261 11.1 19.8
7.1 6.7 13.3 1.7 14.0 74.7 11.3 437 16.5 20.3
5.1 6.5 13.8 2.0 16.0 70.8 13.2 467 20.0 10.0
6.8 7.2 11.1 1.5 16.8 70.1 13.1 672 14.8 10.1
6.5 7.3 10.0 e 14.3 72.8 12.9 835 10.6 9.4
166
P. Lindahl et al. / Journal of Environmental Radioactivity 102 (2011) 163e169
Table 4 Activity concentrations (Bq kg1 dry weight) of natural radionuclides and 137Cs in soil from three sampling sites in Belgium collected during 2004e2007. The activity concentrations are expressed as the weighted mean of three sub-samples from each field if not otherwise noted. Uncertainties are expressed as the weighted extended uncertainty with coverage factor of 1.96 corresponding to 95% confidence level. Sampling year Site 1 2006 2007 Site 2 2004 2006 2007 Site 3 2005 2006 2007
AS
137
40
Oa Ca O C
11.4 13.6 14.5 10.1
2.3 2.7 1.8 1.2
752 551 678 518
O C O C O C
3.3 3.9 4.5 3.4 2.7 3.9
0.3 0.4 0.5 0.5 0.4 0.5
491 504 512 523 480 450
Oa Ca Oa C C
6.4 3.2 14.4 6.4 4.0
0.8 0.6 2.7 0.8 0.5
255 440 577 443 517
Cs
238
U
149 109 78 60
28 29 35 29
41 43 59 60 55 52
n.m. n.m. 28 34 33 30
50 87 115 51 59
28 28 33 34 40
K
226
228
Ra
228
Ra
Th
6 6 8 7
33.6 34.1 33.4 30.2
2.2 2.3 1.7 1.4
58 44 53.2 46.1
4 3 2.4 2.0
59 45 55.5 47.9
5 4 2.8 2.4
4 4 6 7
29.2 30.1 29.1 38.5 34.9 31.9
1.6 1.8 1.1 1.4 1.5 1.4
32.6 33.4 37.2 44.0 38.9 35.6
2.7 2.7 1.5 1.7 1.7 1.6
34.2 35.7 35.9 42.3 40.1 36.7
1.8 1.8 1.8 2.1 2.0 1.9
10 10 8 4 8
17.4 18.8 36.8 40.2 35.1
1.5 1.7 2.5 1.5 1.5
21.0 26.4 47 43.9 38.3
2.4 2.7 3 1.8 1.8
18.1 22.9 48 42.3 46.0
2.3 2.8 4 2.1 2.4
AS: Agricultural system, O: Organic farming, C: Conventional farming, n.m.: not measured. a Only one sub-sample analysed. Uncertainties expressed as the extended standard uncertainty (1.96 SD).
Van Hees, 2007). The overall 226Ra/228Ra activity ratio obtained was 0.8 0.1 reflecting similar levels of 232Th and 238U in soil. 3.2. Natural radionuclides in wheat roots The natural radionuclide activity concentrations observed in the winter wheat roots were considerably lower than in the corresponding soil (Table 5) reflecting the relatively low uptake by wheat roots of these radionuclides. Root samples were only available for the 2006 sampling campaign with overall average activity concentrations (1 SD) across the sampling years of 30 13 Bq kg1, 1.3 0.6 Bq kg1, 1.4 0.4 Bq kg1 and 0.6 0.2 Bq kg1 for 40 K, 226Ra, 228Ra and 228Th, respectively. Thorium-228 is a daughter of 228Ra and these two radionuclides are usually in secular equilibrium with each other in the environment. Radium (as an analogue of calcium) is biologically more available than Th, which results in a higher uptake of Ra isotopes to plants compared with Th (Baeza et al., 1996). The relationship between 228Ra and 228Th showed a weak correlation (r ¼ 0.80, p < 0.05) but the overall 228Ra/228Th activity ratio was higher than in the soil (2.9 1.4), reflecting the difference in availability for uptake in the roots for Ra and Th. The overall average 226Ra/228Ra activity ratio obtained (1.0 0.4) was similar as in soil, reflecting the identical uptake mechanisms for the two Ra isotopes. Table 5 Activity concentrations (Bq kg1 dry weight) of natural radionuclides in winter wheat roots from three sampling sites in Belgium collected in 2006. The activity concentrations are expressed as the weighted mean of three sub-samples from each field. Uncertainties are expressed as the weighted extended uncertainty with coverage factor of 1.96 corresponding to 95% confidence level. Site
AS
40
1
O C O C O C
39 48 13 22 22 36
2 3
226
K
7 7 4 4 4 8
228
Ra
2.4 1.19 1.0 0.74 1.23 1.1
0.4 0.20 0.3 0.26 0.25 0.4
228
Ra
1.4 1.0 1.9 0.7 1.7 1.5
0.5 0.3 1.1a 0.3 0.5 0.8b
Th
0.4 0.4a 0.71 0.27a n.d 0.3 0.3b 0.8 0.5b 0.8 0.4a
AS: Agricultural system, O: Organic farming, C: Conventional farming n.d: not detected in any of the three sub-samples. a Detected only in two sub-samples. b Detected only in one sub-sample. Uncertainties expressed as the extended standard uncertainty (1.96 SD).
Caesium-137 was below decision threshold (∼ 0.1 Bq/kg) except for two samples. By adding the gamma-ray spectra from several samples (measured using the same detector, live time and sample geometry) together it was possible to obtain a 662 keV peak from 137 Cs above decision threshold and giving a result of about 0.1 Bq/ kg, which can be considered as an overall average for the 137Cs in the roots. This result is consistent with the transfer factor in loamy soil of 0.014 reported by Zhu and Smolders (2000). Uranium-238 results were also below decision thresholds of around 1.6 Bq/kg. Vandenhove et al. (2009) reported a 238U transfer factor for cereal straw of 0.25 and cereal grain of 0.18, both for loamy soil. Blanco Rodríguez et al. (2008) aimed to evaluate the capacity of each granulometric fraction of the soil to liberate radionuclides in order to make estimates of their availability. This capacity was found to be dependent on both the fraction and the radionuclide. For uranium, the greater percentage of labile activity concentration was in the coarser fractions (sand or fine sand, depending on the Spanish soils analysed). In our study the most important fraction of the soil is silt (>65% except for two fields, Table 2). 3.3. Natural radionuclides in wheat stems Activity concentrations of natural radionuclides in winter wheat stems were determined from the 2005 and 2006 samples (Table 6). The overall average activity concentrations (1 SD) across the sampling years for 40K, 226Ra, 228Ra and 228Th were 221 84 Bq kg1, 0.8 0.3 Bq kg1, 1.0 0.3 Bq kg1 and 0.20 0.04 Bq kg1, respectively. The overall 228Ra/228Th activity ratio (4.9 1.3) obtained for the stem samples were about twice the value for the roots (2.9 1.4) and five times the value for the soil (1.03 0.08). This reflects the higher mobility of Ra in the stem compared with Th. A strong correlation (r ¼ 0.86, p < 0.01) was observed between 226Ra and 228 Ra with an overall 226Ra/228Ra activity ratio of 0.9 0.2 which corresponds well with 226Ra/228Ra ratios obtained in wheat straw from the UK (Smith, 1971). 3.4. Natural radionuclides in wheat grains Natural radioactivity concentrations in winter wheat grain collected during 2004e2007 are listed in Table 7. Activity concentration data for 226Ra, 228Ra and 228Th were only available for the
P. Lindahl et al. / Journal of Environmental Radioactivity 102 (2011) 163e169 Table 6 Activity concentrations (Bq kg1 dry weight) of natural radionuclides in winter wheat stems from three sampling sites in Belgium collected during 2005e2006. The activity concentrations are expressed as the weighted mean of three sub-samples from each field if not otherwise noted. Uncertainties are expressed as the weighted extended uncertainty with coverage factor of 1.96 corresponding to 95% confidence level. Sampling year Site 1 2006 Site 2 2006 Site 3 2005 2006
AS
40
226
K
228
Ra
228
Ra
Th
Table 7 Activity concentrations (Bq kg1 dry weight) of natural radionuclides in winter wheat grains from three sampling sites in Belgium collected 2004e2007. The activity concentrations are expressed as the weighted mean of three sub-samples from each field if not otherwise noted. Uncertainties are expressed as the weighted extended uncertainty with coverage factor of 1.96 corresponding to 95% confidence level. Sampling year
O C
229 26 215 25
0.71 0.07 0.93 0.09
1.08 0.17 0.78 0.19
0.18 0.10a 0.14 0.10a
O C
383 44 229 27
1.21 0.10 1.00 0.10
1.31 0.24 1.08 0.26
0.23 0.10 0.25 0.14
Ob Cb O C
133 172 128 283
Site 1 2006 2007
20 24 15 33
0.45 1.26 0.56 0.56
0.07 0.12 0.06 0.08
0.77 1.61 0.66 0.60
0.19 0.25 0.14 0.19
0.23 0.23 0.16 0.19
0.13 0.19 0.10a 0.12
AS: Agricultural system, O: Organic farming, C: Conventional farming. a Detected only in two sub-samples. b Only two sub-samples were analysed.
Site 2 2004 2006 2007 Site 3 2005 2006
2006e2007 sampling campaigns. Overall average activity concentrations (1 SD) obtained for 40K, 226Ra, 228Ra and 228Th were 115 22 Bq kg1, 0.10 0.05 Bq kg1, 0.15 0.05 Bq kg1 and 0.045 0.026 Bq kg1, respectively. The 40K activity concentrations are comparable to other reported values (Bilo et al., 1993; Drichko and Lisachenko, 1984; Pulhani et al., 2005; Schimmack et al., 2004), and the 226Ra activity concentrations are about one order of magnitude lower than levels reported from India (Pulhani et al., 2005) and in the same range as levels reported from Russia (Drichko and Lisachenko, 1984). The lower levels of radium in wheat grains compare to the reported levels in India can be explained by higher radium activity concentrations in the soil from India as well as different soil characteristics. According to Pulhani et al. (2005), the radium uptake in wheat grains is mainly affected by the nature of clay material in the soil. The overall 228Ra/228Th activity ratio (3.5 1.5) in wheat grains was in the same range as in the stems with a moderate correlation (r ¼ 0.79, p < 0.01) observed between 228Ra and 228Th. A moderate correlation (r ¼ 0.67, p < 0.01) was observed between 226Ra and 228 Ra with an overall 226Ra/228Ra activity ratio of 0.7 0.2. 3.5. Distribution of natural radionuclides in the wheat plant Distributions of natural radioactivity activity concentrations in the full set of winter wheat samples (organic and conventional added together) are shown in Fig. 2 as box plots. Potassium is an essential mineral nutrient needed for the growth of the plant and is transported together with water from the root to the grain through the stem (Taiz and Zeiger, 1998). The distribution of 40K reflects the mobility and transportation of the K from the roots to the rest of the plant with the highest activity concentration in the stem and the lowest in the roots. The gradients observed for 226Ra, 228Ra and 228 Th suggest that these radionuclides are not as metabolically active as K and there is little exchange between the different plant parts. Roots are known to retain a higher quantity of heavy metals (Bose and Bhattacharyya, 2008) as can be seen by the larger relative difference in concentrations of Th compared to K between the different plant tissues. The 226Ra/40K activity ratios (Fig. 3) clearly show the effects of higher mobility for 40K into the upper parts of the plant (stem and grain) compared to 226Ra. Similar 226Ra/40K ratios in wheat grain have been observed in fertilised and unfertilised fields by Drichko and Lisachenko (1984) and Pulhani et al. (2005). Pulhani et al. furthermore found that 226Ra and 40K
167
2007
AS
40
226
O C O C
108 89 127 124
12 10 15 14
0.089 0.060 0.121 0.210
O C O C O C
134 157 97 88 130 112
7 7 11 10 15 13
n.m n.m 0.171 0.086 0.089 0.088
O C O C C
129 133 96 76 125
15 16 11 9 14
n.m n.m 0.078 0.014 0.055 0.010 0.074 0.022
K
228
Ra
228
Ra
0.016 0.012 0.023 0.022
0.15 0.06 0.17 0.23
0.018 0.014 0.017 0.015
n.m n.m 0.18 0.12 0.13 0.16
Th
0.06 0.04 0.06 0.05
0.06 0.027 0.061 0.102
0.04a 0.020a 0.028a 0.022
0.05 0.04 0.04 0.05a
n.m n.m 0.06 0.03 0.020 0.063
0.06b 0.03a 0.011 0.019a
n.m n.m 0.11 0.05 0.08 0.05 0.23 0.14b
n.m n.m 0.016 0.014b 0.022 0.021b 0.05 0.04b
AS: Agricultural system, O: Organic farming, C: Conventional farming n.m: not measured. a Detected only in two sub-samples. b Detected only in one sub-sample; uncertainty expressed as the combined standard uncertainty with coverage factor of 1.96 corresponding to 95% confidence level.
concentrations in wheat grains were not affected by fertiliser treatment (i.e. ammonium phosphate vs none). 3.6. Concentration ratios of natural radionuclides in wheat A simple model for the uptake of any radionuclide by a plant is provided by the concentration ratio (CR) (Ehlken and Kirchner, 2002); the activity concentration in the plant (Bq kg1, dry weight) divided by the activity concentration in the soil (Bq kg1, dry weight). The CR gives a rough estimate of the uptake of a certain element within the plant. The actual uptake of an element by a plant from the soil depends on many factors including the genotype of the plant, concentrations of competing ions in the soil, the adsorption area of the roots, and the availability of the element in the soil for uptake by the roots of the plant (Ehlken and Kirchner, 2002; Greger, 2004). The average CRs and standard deviations (1 SD) for 40K, 226Ra, 228Ra and 228Th in winter wheat (root, stem and grain) from organic and conventional farming collected during 2004e2007 are listed in Table 8. Potassium-40 has in general a higher CR value in wheat than the other natural radionuclides, as stable K is a major nutrient for the growth of the plant. The uptake of Ra and Th has been suggested to depend mainly on the phosphorus and alkaline-earth concentrations in the soil (Blanco Rodríguez et al., 2002). The observed CR value in grain for 40K corresponds well with other studies in similar conditions (Bilo et al., 1993; Drichko and Lisachenko, 1984; Pulhani et al., 2005; Schimmack et al., 2004). IAEA (2010) compiled the CRs for radiological risk assessments and recommended in case of cereal grains grown in temperate environment the following CR values for K (all soil groups), Ra and Th (loamy soil): 0.74, 0.029 and 0.0027, respectively. IAEA’s report, compiled large ranges of CR values depending among other factors on the soil characteristics and plant type. Concentration ratios in cereal grains ranged from 8.0 105 to 6.7 101 for Ra and from 1.6 104 to 2.2 102 for Th. The disadvantage of the CR concept as a measure of the uptake of a certain element is the use of the total concentration in the soil instead of the available ion concentration (Baeza et al., 1996).
168
P. Lindahl et al. / Journal of Environmental Radioactivity 102 (2011) 163e169
Fig. 2. Box plots of the distribution of activity concentrations of natural radionuclides in the full set of winter wheat samples from three sampling sites in Belgium collected during 2004e2007 (organic and conventional added together). The mean and median values are represented by x and the middle horizontal line, respectively. The upper and lower limits of the boxes represent the standard deviation (1 SD) and the whiskers represent the range of the observed values.
3.7. Comparison between organic and conventional systems Statistical analyses (see Chapter 2.4) did not reveal any significant differences in concentrations of primordial radionuclides (i.e. 40K, 238 U, 226Ra, 228Ra and 228Th) in soil between agricultural systems or among environments. Furthermore, the average activity concentration ratio between organic and conventional soil was close to unity for all radionuclides (Table 9). However, a significant (p ¼ 0.003, Tukey’s test) higher activity concentration of 137Cs in soil of Marcheen-Famenne than in soil of Soignies was observed confirming the gradient of 137Cs in Belgium observed by Pommé et al. (1998). No significant difference (p > 0.05) in activity concentrations of the four radionuclides determined in wheat grains (i.e. 40K, 226Ra, 228 Ra and 228Th) was observed between the two agricultural systems or amongst the environments. Overall CR organic/conventional ratios (Table 9) showed values close to unity for stems and grains. However for roots, 40K and 228Th
showed tendencies of higher uptake in the conventional fields while there is a trend for a lower uptake of 226Ra in the same fields. Nonetheless a further study with a larger number of samples would be required to confirm such an observation. Similar long-term experiments in the USA on fields treated with P fertilisers also found no difference in U, Ra or Th concentrations in wheat grain grown on fertilised and non-fertilised soil (Mortvedt, 1994). No difference was also observed for Ra and U in vegetables grown in organic and conventional farming systems in Brazil (Lauria et al., 2009). The large residual variations observed when performing the analyses of variance reflect the high variability of each agricultural system considered in this study, which is characteristic of a farm approach experimental design. Nonetheless that is exactly the complex situation an inspector has to face when controlling an organic farm before delivering a certificate. Indeed despite the existence of norms, standards or regulation for the organic farming system, a huge variability exists. The situation is even more complex with the conventional agriculture; as a conventional farmer could for instance use manure in case it is economically relevant in a specific period of time.
Table 8 Average observed concentration ratios (Bq kg1 dry weight plant/Bq kg1 dry weight soil) in tissues from organic and conventional grown winter wheat collected from three sites in Belgium during 2004e2007. Uncertainties are expressed as one standard deviation (1 SD).
Fig. 3. 226Ra/40K activity ratios in winter wheat (root, stem and grain) and soil samples collected in Belgium during 2004e2007. The error bars represent the combined standard deviation (1 SD).
Plant AS part
40
Root
0.038 0.070 0.45 0.46 0.25 0.23
O C Stem O C Grain O C
226
K
Ra
0.013 0.046 0.025 0.027 0.24 0.026 0.12 0.034 0.12 0.0034 0.06 0.0029
228
Ra
0.022 0.037 0.007 0.025 0.011 0.026 0.023 0.029 0.0015 0.0033 0.0021 0.0036
228
Th
0.013 0.012 0.009 0.014 0.011 0.006 0.022 0.006 0.0010 0.0009 0.0018 0.0011
0.007 0.006 0.004 0.003 0.0005 0.0007
P. Lindahl et al. / Journal of Environmental Radioactivity 102 (2011) 163e169 Table 9 Average organic/conventional ratio for observed CR values in winter wheat (root, stem and grain) collected from three sites in Belgium during 2004e2007. Uncertainties are expressed as the extended standard uncertainty with coverage factor of 1.96 corresponding to 95% confidence level. Average radionuclide organic/conventional ratios in soil are included for comparison. Number of samples analysed are shown in parentheses. Plant part
40
226
Root CR Stem CR Grain CR Soil (activity)
0.55 0.14 (3) n.s 1.1 0.6 (7) 1.1 0.5 (7)
1.7 0.8 (3) n.s n.s 1.0 0.3 (7)
K
Ra
228
Ra
n.s 1.0 0.7 (4) 1.3 1.1 (5) 1.0 0.4 (7)
228
Th
0.7 0.6 (2) 1.0 0.4 (4) n.s 1.0 0.4 (7)
n.s: not significant; extended uncertainty larger than average value.
4. Conclusions The agricultural system productions tested (organic vs. conventional) in this study are not influencing the activity concentrations of the analysed radionuclides in the soils. Natural radioactivity was studied in winter wheat and the corresponding soil with the highest activity concentrations of 228Th and Ra isotopes (226Ra and 228Ra) found in the root and stem and the lowest in the grain. Potassium-40 showed the highest activity concentration in the stem and the lowest in the root. Despite the fact that wheat is not a high demanding crop for potassium, lack of this element often causes the weakening of the straw, which may result in lodging. The 228Ra/228Th ratios suggest no secular equilibrium between 232 Th and its daughters in the wheat plant. Thorium-232 cannot be determined directly using gamma-ray spectrometry but knowing its concentration would be valuable for future studies. For determination of 232Th concentration in biological material with no secular equilibrium one has to resort to alpha spectrometry or mass spectrometry. Overall CRs for K, Ra and Th in wheat grain correspond well with previously reported values (Drichko and Lisachenko, 1984; Pulhani et al., 2005). However, no significant difference was observed in the uptake of natural radionuclides between organically and conventionally grown winter wheat. Acknowledgements The authors would like to thank Mr. Ramon Carlos-Marquez for the help with the gamma-ray measurement at ITU, Karlsruhe, UNAB and the farmers for providing the wheat and soil samples, and Mr. Olivier De Rudder and Mr. Fernando Cordeiro from IRMM, Geel for carrying out the sampling campaigns. References Baeza, A., Paniagua, J., Rufo, M., Barandica, J., 1996. Bio-availability and transfer of natural radionuclides in a Mediterranean ecosystem. Applied Radiation and Isotopes 47, 939e945. Bilo, M., Steffens, W., Führ, F., Pfeffer, K.-H.,1993. Uptake of 134/137Cs in soil by cereals as a function of several soil parameters in three soil types in upper Swabia and North Rhine-Westphalia (FRG). Journal of Environmental Radioactivity 19, 25e39. Blanco Rodríguez, P., Vera Tomé, F., Lozano, J.C., 2002. About the assumption of linearity in soil-to-plant transfer factors for uranium and thorium isotopes and 226 Ra. The Science of the Total Environment 284, 167e175. Blanco Rodríguez, P., Vera Tomé, F., Lozano, J.C., Pérez-Fernández, M.A., 2008. Influence of soil texture on the distribution and availability of 238U, 230Th, and 226 Ra in soils. Journal of Environmental Radioactivity 99, 1247e1254. Bose, S., Bhattacharyya, A.K., 2008. Heavy metal accumulation in wheat plant grown in soil amended with industrial sludge. Chemosphere 70, 1264e1272. Drichko, V.F., Lisachenko, E.P., 1984. Background concentrations of 226Ra, 228Th, and 40 K in cultivated soils and agricultural plants. Soviet Journal of Ecology 15, 81e85. EFMA, 2005. Forecast of Food, Farming and Fertilizer Use in the European Union 2005-2015. Annual Forecast, Brussels, Belgium. European Fertilizer Manufacturers Association (EFMA): 7.
169
Ehlken, S., Kirchner, G., 2002. Environmental processes affecting plant root uptake of radioactive trace elements and variability of transfer factor data: a review. Journal of Environmental Radioactivity 58, 97e112. Falck, W., Wymer, D., 2006. In: Merkel, B.J., Hasche-Berger, A. (Eds.), Uranium in Phosphate Fertilizer Production. Uranium in the Environment. Springer, Berlin Heidelberg, Germany, pp. 857e866. Golmakani, S., Moghaddam, M.V., et al., 2008. Factors affecting the transfer of radionuclides from the environment to plants. Radiation Protection Dosimetry 130 (3), 368e375. Greger, M., 2004. Uptake of Nuclides by Plants. Technical Report TR-04e14. Swedish Nuclear Fuel and Waste Management Co, Stockholm, Sweden. Hult, M., Preusse, W., Gasparro, J., Köhler, M., 2006. Underground gamma-ray spectrometry. Acta Chimica Slovenica 53, 1e7. IAEA, International Atomic Energy Agency, 2010. Handbook of Parameter Values for the Prediction of Radionuclide Transfer in Terrestrial and Freshwater Environments. Technical Reports Series No 472 Vienna, Austria. ISO, International Standards Organisation, 2000. Determination of the Detection Limit and Decision Threshold for Ionising Radiation Measurements e Part 3: Fundamentals and Application to Counting Measurements by High Resolution Gamma Spectrometry, without the Influence of Sample Treatment. 11929e3 Geneva, Switzerland. Khater, A.E.M., Al-Sewaidan, H.A., 2008. Radiation exposure due to agricultural uses of phosphate fertilizers. Radiation Measurements 43 (8), 1402e1407. Lauria, D.C., Ribeiro, F.C.A., Conti, C.C., Loureiro, F.A., 2009. Radium and uranium levels in vegetables grown using different farming management systems. Journal of Environmental Radioactivity 100, 176e183. Magkos, F., Arvaniti, F., et al., 2003. Organic food: nutritious food or food for thought? A review of the evidence. International Journal of Food Sciences and Nutrition 54 (5), 357e371. Mortvedt, J.J., 1994. Plant and soil relationship of uranium and thorium decay series radionuclides e a review. Journal of Environmental Quality 23, 643e650. Nelson, W., Hirayama, H., Rogers, D., 1985. The EGS4 Code System, SLAC-265. Stanford Linear Accelerator Centre, USA. Peerani, P., Carbol, P., Hrnecek, E., Betti, M., 2002. Assessment of a Compton-event suppression g-spectrometer for the detection of fission products at trace levels. Nuclear Instruments and Methods in Physics Research A 482, 42e50. Pommé, S., Uyttenhove, J., et al., 1998. Radiocesium contamination in Belgium. Journal of Radioanalytical and Nuclear Chemistry 235 (1), 139e145. Pulhani, V.A., Dafauti, S., Hegde, A.G., Sharma, R.M., Mishra, U.C., 2005. Uptake and distribution of natural radioactivity in wheat plants from soil. Journal of Environmental Radioactivity 79, 331e346. Righi, S., Lucialli, P., Bruzzi, L., 2005. Health and environmental impacts of a fertilizer plant e Part I: assessment of radioactive pollution. Journal of Environmental Radioactivity 82, 167e182. Schimmack, W., Zimmermann, G., Sommer, M., Dietl, F., Schultz, W., Paretzke, H.G., 2004. Soil-to-grain transfer of fallout 137Cs for 28 winter wheat cultivars as observed in field experiments. Radiation and Environmental Biophysics 42, 275e284. Siderer, Y., Maquet, A., Anklam, E., 2005. Need for research to support consumer confidence in the growing organic food market. Trends in Food Science & Technology 16, 332e343. Smith, K.A., 1971. The comparative uptake and translocation by plants of calcium, strontium, barium and radium. II. Triticum vulgare (wheat). Plant and Soil 34, 643e651. Taiz, L., Zeiger, E., 1998. Plant Physiology, second ed. Sinauer Associates Inc, Sunderland, Massachusetts. UNSCEAR, United Nations Scientific Committee on the Effects of Atomic Radiations, 2000. Sources. Sources and Effects of Ionizing Radiation, vol. 1. United Nations Publication, New York. Vandenhove, H., Van Hees, M., 2007. Predicting radium availability and uptake from soil properties. Chemosphere 69, 664e674. Vandenhove, H., Olyslaegers, G., Sanzharova, N., Shubina, O., Reed, E., Shang, Z., Velasco, H., 2009. Proposal for new best estimates of the soil-to-plant transfer factor of U, Th, Ra, Pb and Po. Journal of Environmental Radioactivity 100, 721e732. Vandendriessche, H., Bries, J., Geypens, M., 1996. Experience with fertilizer expert systems for balanced fertilizer recommendations. Communications in Soil Science and Plant Analysis 27 (5), 1199e1209. Vera Tomé, F., Blanco Rodríguez, P., Lozano, J.C., 2002. Distribution and mobilization of U, Th and 226Ra in the plant-soil compartments of a mineralized uranium area in south-west Spain. Journal of Environmental Radioactivity 59, 41e60. Willer, H., Kilcher, L. (Eds.), 2009. The World of Organic Agriculture e Statistics and Emerging Trends 2009. International Federation of Organic Agriculture Movements (IFOAM), Bonn, Germany and Research Institute of Organic Agriculture (FiBL) Frick, Switzerland. Woese, K., Lange, D., et al., 1997. A comparison of organically and conventionally grown foods - results of a review of the relevant literature. Journal of the Science of Food and Agriculture 74, 281e293. Zhu, Y.G., Smolders, E., 2000. Plant uptake of radiocaesium: a review of mechanisms, regulation and application. Journal of Experimental Botany 51 (351), 1635e1645.
Contents lists available at ScienceDirect
Journal of Environmental Radioactivity journal homepage: www.elsevier.com/locate/jenvrad
Natural radioactivity in winter wheat from organic and conventional agricultural systems Patric Lindahl, Alain Maquet, Mikael Hult*, Joël Gasparro, Gerd Marissens, Raquel González de Orduña European Commission, Joint Research Centre, Institute for Reference Materials and Measurements (EC-JRC-IRMM), Retieseweg 111, B-2440 Geel, Belgium
a r t i c l e i n f o
a b s t r a c t
Article history: Received 11 February 2010 Received in revised form 10 October 2010 Accepted 9 November 2010 Available online 8 December 2010
The distribution of natural radionuclides was studied in winter wheat plants collected from three sites in Belgium during 2004e2007. Activity concentrations of 40K, 226Ra, 228Ra and 228Th in organically and conventionally grown wheat, and in the corresponding soil samples, were determined using ultra low-level gamma-ray spectrometry. The observed soil-to-wheat concentration ratios were calculated for the different parts of the wheat plant (root, stem and grain) in the two agricultural systems (organic and conventional). There were large variations in radionuclide activity concentrations between the sites and fields, but no significant difference between conventionally and organically grown wheat plants was observed. Ó 2010 Elsevier Ltd. All rights reserved.
Keywords: Natural radionuclides Wheat Soil Organic farming Conventional farming
1. Introduction Radionuclides from the natural decay series (238U, 232Th and U) are present in the environment in different forms and quantities. Together with 40K, considerable amounts of these natural radionuclides and their daughter products can be found in soil with varying activity concentrations depending on the region and soil type. The reported average soil activity concentrations in Belgium for 40K, 226Ra and 232Th are 380 Bq kg1, 26 Bq kg1 and 27 Bq kg1, respectively, with large ranges in activity concentrations due to natural variability (UNSCEAR, 2000). These radionuclides may be absorbed, along with essential nutrients, by plant roots and transported to other parts of the plant. The uptake of radionuclides in terrestrial plants is mainly dependent on the soil characteristics, plant type and the individual chemical properties of the radionuclides in the soil matrix (Ehlken and Kirchner, 2002). In addition, external factors such as the climate and agricultural practices may also influence plant uptake of radionuclides. In recent years the importance of organic farming methods has increased due to growing consumer interest for certified organic products (Willer and Kilcher, 2009), hence the importance of valid analytical methods for the authentication of organic food products (Siderer et al., 2005). The organic farming systems aim to restrict the use of mineral fertilisers and chemical pesticides, and are mainly 235
* Corresponding author. Tel.: þ 32 14 571269; fax: þ 32 14 584273. E-mail address: [email protected] (M. Hult). 0265-931X/$ e see front matter Ó 2010 Elsevier Ltd. All rights reserved. doi:10.1016/j.jenvrad.2010.11.007
based on long-term naturally occurring biological processes. The conventional farming methods focus on immediate and isolated effects (i.e. not emulating living ecological systems and cycles) to increase the crop output by adding different types of synthetic inputs. Depending on the raw materials and the processing of the fertiliser, the synthetic input may contain enhanced levels of natural radionuclides in different chemical compounds (Righi et al., 2005; Khater and Al-Sewaidan, 2008) and hence may alter the overall radioactivity in the soil. This may affect the radionuclide uptake within the crop. It is a well known phenomenon that the phosphate ores that are used for the production of fertilisers contain significantly increased concentrations of uranium and thorium traces (Falck and Wymer, 2006). The activity level is strongly depending on the origin of the ores. There is also a strong difference between the geological formations from which the ore is extracted. The processing of the ores to fertilisers has also an impact on the radionuclide concentration. In most cases the uranium concentration will be increased, while on the contrary, the radium concentration will be reduced (Falck and Wymer, 2006). There is no clear trend for the evolution of the thorium concentration. One could suggest that due to the increased levels of natural radionuclides (40K and the 238, 235U and 232Th decay chains) in many types of synthetic fertilisers, one should be able to distinguish organic and conventional food products from each other by measuring the content of natural radionuclides. There are, however, many factors contributing to the amount of natural radioactivity taken up by plants (Golmakani et al., 2008) among them those related to the plant itself like the plant species, age of plant
164
P. Lindahl et al. / Journal of Environmental Radioactivity 102 (2011) 163e169
parts, depth of roots, etc. or to the soil like the kind of soil, organic matter content, pH, CEC, etc, or to the radionuclides (e.g. chemical form, mobility). Additionally, in recent years the use of synthetic fertilisers has been somewhat reduced (EFMA, 2005). There exist also practices at organic farms to use natural mineral fertilisers, which lead to further reduction in potential differences in radioactivity concentrations in crop from conventional and organic farming. In 2004, the Institute for Reference Materials and Measurements (IRMM) started field experiments to obtain suitable environmental crop samples for the development of a range of analytical techniques to distinguish between organic and conventional farming. As a part of this project, winter wheat grown in organic and conventional systems was collected and analysed during 2004e2007. The particular part of that project which is presented here aims to determine and compare the natural radionuclide contents in different parts of the wheat plant and the corresponding soil collected from organic and conventional agricultural systems. Four main approaches (i.e. retail purchase comparison, fertiliser treatment comparisons, whole farm comparisons, or animal feeding and human health) are used when comparing the two agricultural systems with their advantages and disadvantages and complement each other in terms of the statement they can make (Magkos et al., 2003). Farm studies are conducted on products from selected farms with different forms of cultivation for which the production conditions are recorded (Woese et al., 1997). A mean number of samples can be examined. Environmental factors such as climate and soil conditions can be made suitable for comparison by selecting neighbouring farms. The disadvantage of this method is that the accuracy of the information given cannot be verified. Another problem is that it is very difficult to select the farms and fields in such a manner that they truly represent the cultivation forms which are to be compared. 2. Materials and methods
same field. During the first two years of the study, only one site was selected. In 2004, site 2 was studied while in 2005 site 3 was studied. During the last two years of the study, the number of sites was increased to three. However, in site 3 in 2007 only samples from a conventional field were available due to difficulties in preparing the organic field. Each field was ploughed before sowing except the organic field of site 2 in 2007, which was without any tillage. In 2004 (site 2), the varieties "Bussard" and "Monopol" were sown as a 50/50 mixture in the organic field and the variety "Napier" was sown in the conventional field. During the period 2005e2007 all samples were from the variety "Cubus". Table 1 is showing the fertilisation practices for the selected fields. For each field, three sectors of about 8 8 m2 were delimited and separated by approximately 10 m. Within each sector, 35e40 plants were collected. The plants were separated into three parts (shallow root, stem and grain) and carefully cleaned with distilled water to remove any soil residue. During 2004 and 2007, only the grain was analysed and during 2005 the stem and grain were analysed. Additional root samples were analysed in the 2006 sampling campaign together with stem and grain. The root samples were cleaned with distilled water twice and any visible soil residue was removed manually. For each field, the amount of sample (mixture of three sectors per field) used for the radionuclide analysis were usually ∼1 g, ∼25 g and ∼50 g (dry weight) for root, stem and grain, respectively. The different plant parts were ground, homogenised and dried for 24 h at 80 C before being placed in cylindrical airtight Teflon containers for gamma-ray measurements. Six soil samples (layer 0e30 cm) were extracted from each field (2 from each sector) using a drill, these were then mixed and homogenised to obtain samples representative of each field. From each mixture, three sub-samples (∼100 g each) were dried for 24 h at 80 C and placed in cylindrical airtight Teflon containers for radionuclide analysis by gamma-ray spectrometry. The remaining homogenised soil sample was analysed by the Belgian Soil Science Service (BSSS) in Leuven, Belgium to determine the soil characteristics of each field. 2.2. Soil characteristics The soil characteristics are presented in Table 2. The fields in this study are characterised by a loamy soil (particle size < 50 mm) percentage higher than 45% and a clay (particle size < 2 mm) percentage lower than 30% except for the conventional field at site 2 (2004) which was at the limit between loamy and clay soil based on the Jamagne’s triangular diagram of soil texture. The combination of fertility and Table 1 Fertilisation practices for the selected fields used for winter wheat sampling in Belgium during 2004e2007.
2.1. Sampling and preparation Fertilisation Soil and mature winter wheat (Triticum aestivum L.) plants were collected during 2004e2007 from three regions in the south of Belgium (Fig. 1): 1) Marche-enFamenne, 2) Soignies, and 3) Ciney. The sampling sites were selected in collaboration with the National Union of Belgian Organic Farmers (UNAB) with one certified organic farmer and one conventional farmer for each site. Each site consisted of one organic and one conventional field in close proximity. Due to the rotation of crop types, it is not possible to collect the same crop for two consecutive years from the
Sampling year
AS
Site 1. Marche-en-Famenne 2006 O 27 Jul C 27 Jul 2007
O C
Site 2. Soignies 2004 O C
4 Aug 4 Aug
5 Sep 9 Aug
2006
O C
27 Jul 28 Jul
2007
O C
3 Aug 3 Aug
Site 3. Ciney 2005 O C
Fig. 1. Map showing sampling sites of organic and conventional grown winter wheat and corresponding soil collected during 2004e2007.
Harvest date
18 Aug 17 Aug
2006
O C
1 Aug 26 Jul
2007
C
27 Jul
Commercial name and composition (N/P/K þ MgO)
Amount applied
Orgaminea (7/5/10 þ 2)b i) Kemira (26/6/6)b ii) Nitrate 27% Orgamine (7/5/10 þ 2)b i) Mixture 1 (14/7/20 þ 3)b ii) Mixture 2 (23/5/5)b iii) Nitrates 27%
300 500 270 400 350 250 250
No fertiliser i) N solution (39/0/0)b ii) Potassium Chloride (40% þ 6 MgO þ 5 Na2O) iii) N 22% þ MgO 7% Orgamine (7/5/10 þ 2)b i) KCl 60 ii) N solution (39/0/0) b iii) Nitrate 27% Orgamine (7/5/10 þ 2)b i) N solution (39/0/0)b ii) Nitrate 27%
No fertiliser 250 L ha1 290 kg ha1
Liquid manure of bovine i) N solution (39/0/0)b ii) Nitrate 27% No fertiliser i) N solution (30/0/0)b ii) Nitrate 27% Nitrate 27%
10000 L ha1 300 L ha1 300 kg ha1 No fertiliser 320 L ha1 190 kg ha1 690 kg ha1
370 400 200 375 225 300 300 300
kg kg kg kg kg kg kg
ha1 ha1 ha1 ha1 ha1 ha1 ha1
kg ha1 kg ha1 kg ha1 L ha1 kg ha1 kg ha1 L ha1 kg ha1
AS: Agricultural system, O: Organic farming, C: Conventional farming. a Orgamine is distributed by ATBE in Chartres de Bretagne, France. b NPK formula: the three numbers indicate the percent of nitrogen (N), P2O5 and K2O.
P. Lindahl et al. / Journal of Environmental Radioactivity 102 (2011) 163e169 moisture-holding capacity with good drainage makes loamy soil systems an excellent medium for growing wheat. The pH (KCl) which is a fundamental property controlling biological and chemical processes in the soil was generally within the target zone for such soil types (target zone: pH 6.2e7.3) (Vandendriessche et al., 1996). Cation exchange capacity (CEC) is an important property of soil and is directly related to soil texture. Soil particles are negatively charged, which allows the soil to prevent cations from being leached away. A CEC greater than 10 cmol kg1 was observed across all sites indicating good base cation holding capabilities, except for the conventional field at site 2 in 2007 and the organic field at site 3 in 2005 (Table 2).
165
Table 3 Decision thresholds for the analysed radionuclides by gamma-ray spectrometry following ISO (2000) with a ¼ 0.05. The soil data refers to measurements above ground and the rest refers to measurements below ground in HADES. Sample type
Sample mass (g)
Soil Root Stem Grain
100 1 25 50
Decision threshold, Bq kg1 [a ¼ 0.05] 137
2.3. Gamma-ray spectrometry The radionuclide activity concentrations in the winter wheat samples collected during 2005e2007 were determined using ultra low background HPGe-detectors installed at the underground research facility HADES (Hult et al., 2006). The facility is located at a depth of 225 m (500 m water equivalent) below ground level at the Belgian Nuclear Research Centre in Mol, Belgium. The detectors are constructed using materials selected for a high degree of radiopurity and shielded with electrolytic copper and low-activity lead. The 2004 wheat samples were measured above ground with a Compton-suppression detector located at ITU (Institute for Transuranium Elements), as part of an initial collaboration (Peerani et al., 2002) and the 2005 samples were measured above ground with a low background HPGedetector. Due to the higher detection limits of the above ground measurements during 2005, only 40K was detectable in the wheat samples. All soil samples were measured above ground with the same low background HPGe-detector. The grain, stem and root samples were measured for ∼2 weeks and the soil samples for ∼5 days. Since the activity concentrations for the radionuclides reported in this study was higher in the soil samples than in the wheat samples, it was possible to measure the soil above ground and obtain adequate counting statistics within a shorter measurement time. The samples were stored for a minimum of three weeks before measurement to ensure secular equilibrium between 226Ra and its daughters since the half-life of the first daughter, 222Rn, is 3.8 days. The samples were measured in standard Teflon sample containers and the counting efficiencies, for each container, were calculated by Monte Carlo simulation using the EGS4 code (Nelson et al., 1985). The main uncertainty contributions were from detection efficiency and (for certain samples and radionuclides) counting statistics. Uncertainties from the efficiency determination varied between the detectors in the range 4%e8%. Measurements were carried out for up to two weeks per sample to obtain sufficient counting statistics for the major peaks. The activities were determined by measuring the daughter radionuclides (in parentheses) of 226Ra (214Pb and 214Bi), 228 Ra (228Ac), 228Th (212Pb and 208Tl) and 238U (234Th) assuming secular equilibrium. The weighted average was used for the different peaks from the daughter nuclides to determine the final activity concentrations for the radionuclides of interest. The 228 Ra and 228Th activities were decay corrected for the time between sampling and measurement. The activities of 40K and 137Cs were determined using the 1460 keV and 661 keV gamma-ray peaks, respectively. Due to their low-activity concentration in wheat as compared to soil, uranium and 137Cs were not detected in the wheat plant samples, only in the soil samples. Table 3 gives the a posteriori decision threshold following ISO (2000) with alpha ¼ 0.05.
Cs
0.2 0.1 0.06 0.01
40
K
238
1.2 3.5 0.4 0.1
2.1 1.6 0.7 0.4
U
226
228
Ra
0.4 0.6 0.07 0.02
Ra
0.7 0.6 0.3 0.05
228
Th
0.3 0.2 0.06 0.02
the grouping variable had two levels) was performed. All statistical analyses were carried out using Systat 13 (Systat Software Inc., Chicago, U.S.A.). These analyses were applied on radionuclides determined in soils and grains sampled in 2005, 2006 and 2007. Samples collected in 2004 were discarded due to the fact that two different wheat cultivars were grown in the organic field and the conventional one.
3. Results and discussion 3.1. Radionuclides in soil Activity concentrations of natural radionuclides and 137Cs observed in the soil from the three sampling sites are listed in Table 4. The overall average activity concentrations (1 SD) across all sampling years for 40K, 238U, 226Ra, 228Ra and 228Th were 513 111 Bq kg1, 32 4 Bq kg1, 32 6 Bq kg1, 40 10 Bq kg1, 41 11 Bq kg1, respectively. These values correspond well with the worldwide averages of 400 Bq kg1, 35 Bq kg1, 35 Bq kg1 and 30 Bq kg1 for 40K, 238U, 226Ra and 232Th (UNSCEAR, 2000), and with average activity concentrations reported in Belgium (see Section 1). The 137Cs activity concentration in soil showed an overall average activity concentration and standard deviation (1 SD) of 8 5 Bq kg1, reflecting the local variation of fallout 137Cs at the study sites, which was mainly dependent on the precipitation after the Chernobyl accident. The southernmost site (Number 1) had the highest average 137Cs activity concentration (12.4 2.0 Bq/kg) and the northernmost site (Number 2) had the lowest average 137Cs activity concentration (3.6 0.6 Bq/kg). This agrees well with previously published data on radiocaesium in Belgian soil (Pommé et al., 1998). The two 232Th daughters, 228Ra and 228Th, showed a very strong relationship with almost perfect correlation (r ¼ 0.97, p < 0.01) and the overall 228Ra/228Th activity ratio is very close to unity (1.03 0.08) indicating almost complete secular equilibrium between the daughters of 232Th in the soil. Uranium-238 showed a moderate correlation with 226Ra (r ¼ 0.60, p < 0.01) with an overall 226 Ra/238U activity ratio of 1.0 0.2 indicating secular equilibrium. Uranium is closely associated with the organic matter content in the soil (Vera Tomé et al., 2002) and it has been reported that Ra is linked with the cation exchange capacity (CEC) of the soil (Vandenhove and
2.4. Statistical analysis Normality and equality of variances of the populations were checked using the ShapiroeWilk test and Levene’s test, respectively. When required, the variables were log transformed. Two-way analyses of variance were then performed, testing the effects of the agricultural system and the environment. In case an effect was significant in any particular radionuclide, a Tukey’s test was calculated to make all pairwise mean comparisons. When assumption of normality or homogeneity of variances was not respected, a nonparametric test (i.e. KruskaleWallis test or ManneWhitney test in case Table 2 Soil characteristics for the three sites in Belgium collected during 2004e2007. Characteristics
Site 1
Sampling year
2006
pH (KCl) pH (H2O) CEC (cmol kg1) C (%) Clay (%) Silt (%) Sand (%) Total P (mg kg1) Total N (mg kg1) C/N
Site 2 2007
Site 3
2004
2006
2007
2005
2006
2007
O
C
O
C
O
C
O
C
O
C
O
C
O
C
C
5.6 6.7 17.8 2.4 18.0 68.2 13.8 909 25.4 9.5
5.8 6.7 14.1 2.0 13.0 73.5 13.5 671 19.9 10.1
4.9 5.8 17.1 e 13.2 72.7 14.1 1146 29.8 10.7
6.4 6.6 12.0 e 18.8 68.0 13.2 520 17.6 11.9
6.5 7.2 10.8 1.0 25.0 49.5 25.5 621 11.3 8.8
6.7 7.1 12.0 1.2 30.0 33.7 36.3 737 10.9 11.0
5.4 6.7 18.2 2.2 17.0 68.3 14.7 530 27.7 7.9
6.8 7.9 11.6 1.1 10.6 64.6 24.8 671 19.9 9.4
6.3 7.2 10.3 e 13.2 74.0 12.8 e 10.5 11.4
7.7 7.8 8.4 e 12.2 72.6 15.2 481 11.8 10.2
7.5 7.1 8.4 1.1 13.1 75.3 11.6 261 11.1 19.8
7.1 6.7 13.3 1.7 14.0 74.7 11.3 437 16.5 20.3
5.1 6.5 13.8 2.0 16.0 70.8 13.2 467 20.0 10.0
6.8 7.2 11.1 1.5 16.8 70.1 13.1 672 14.8 10.1
6.5 7.3 10.0 e 14.3 72.8 12.9 835 10.6 9.4
166
P. Lindahl et al. / Journal of Environmental Radioactivity 102 (2011) 163e169
Table 4 Activity concentrations (Bq kg1 dry weight) of natural radionuclides and 137Cs in soil from three sampling sites in Belgium collected during 2004e2007. The activity concentrations are expressed as the weighted mean of three sub-samples from each field if not otherwise noted. Uncertainties are expressed as the weighted extended uncertainty with coverage factor of 1.96 corresponding to 95% confidence level. Sampling year Site 1 2006 2007 Site 2 2004 2006 2007 Site 3 2005 2006 2007
AS
137
40
Oa Ca O C
11.4 13.6 14.5 10.1
2.3 2.7 1.8 1.2
752 551 678 518
O C O C O C
3.3 3.9 4.5 3.4 2.7 3.9
0.3 0.4 0.5 0.5 0.4 0.5
491 504 512 523 480 450
Oa Ca Oa C C
6.4 3.2 14.4 6.4 4.0
0.8 0.6 2.7 0.8 0.5
255 440 577 443 517
Cs
238
U
149 109 78 60
28 29 35 29
41 43 59 60 55 52
n.m. n.m. 28 34 33 30
50 87 115 51 59
28 28 33 34 40
K
226
228
Ra
228
Ra
Th
6 6 8 7
33.6 34.1 33.4 30.2
2.2 2.3 1.7 1.4
58 44 53.2 46.1
4 3 2.4 2.0
59 45 55.5 47.9
5 4 2.8 2.4
4 4 6 7
29.2 30.1 29.1 38.5 34.9 31.9
1.6 1.8 1.1 1.4 1.5 1.4
32.6 33.4 37.2 44.0 38.9 35.6
2.7 2.7 1.5 1.7 1.7 1.6
34.2 35.7 35.9 42.3 40.1 36.7
1.8 1.8 1.8 2.1 2.0 1.9
10 10 8 4 8
17.4 18.8 36.8 40.2 35.1
1.5 1.7 2.5 1.5 1.5
21.0 26.4 47 43.9 38.3
2.4 2.7 3 1.8 1.8
18.1 22.9 48 42.3 46.0
2.3 2.8 4 2.1 2.4
AS: Agricultural system, O: Organic farming, C: Conventional farming, n.m.: not measured. a Only one sub-sample analysed. Uncertainties expressed as the extended standard uncertainty (1.96 SD).
Van Hees, 2007). The overall 226Ra/228Ra activity ratio obtained was 0.8 0.1 reflecting similar levels of 232Th and 238U in soil. 3.2. Natural radionuclides in wheat roots The natural radionuclide activity concentrations observed in the winter wheat roots were considerably lower than in the corresponding soil (Table 5) reflecting the relatively low uptake by wheat roots of these radionuclides. Root samples were only available for the 2006 sampling campaign with overall average activity concentrations (1 SD) across the sampling years of 30 13 Bq kg1, 1.3 0.6 Bq kg1, 1.4 0.4 Bq kg1 and 0.6 0.2 Bq kg1 for 40 K, 226Ra, 228Ra and 228Th, respectively. Thorium-228 is a daughter of 228Ra and these two radionuclides are usually in secular equilibrium with each other in the environment. Radium (as an analogue of calcium) is biologically more available than Th, which results in a higher uptake of Ra isotopes to plants compared with Th (Baeza et al., 1996). The relationship between 228Ra and 228Th showed a weak correlation (r ¼ 0.80, p < 0.05) but the overall 228Ra/228Th activity ratio was higher than in the soil (2.9 1.4), reflecting the difference in availability for uptake in the roots for Ra and Th. The overall average 226Ra/228Ra activity ratio obtained (1.0 0.4) was similar as in soil, reflecting the identical uptake mechanisms for the two Ra isotopes. Table 5 Activity concentrations (Bq kg1 dry weight) of natural radionuclides in winter wheat roots from three sampling sites in Belgium collected in 2006. The activity concentrations are expressed as the weighted mean of three sub-samples from each field. Uncertainties are expressed as the weighted extended uncertainty with coverage factor of 1.96 corresponding to 95% confidence level. Site
AS
40
1
O C O C O C
39 48 13 22 22 36
2 3
226
K
7 7 4 4 4 8
228
Ra
2.4 1.19 1.0 0.74 1.23 1.1
0.4 0.20 0.3 0.26 0.25 0.4
228
Ra
1.4 1.0 1.9 0.7 1.7 1.5
0.5 0.3 1.1a 0.3 0.5 0.8b
Th
0.4 0.4a 0.71 0.27a n.d 0.3 0.3b 0.8 0.5b 0.8 0.4a
AS: Agricultural system, O: Organic farming, C: Conventional farming n.d: not detected in any of the three sub-samples. a Detected only in two sub-samples. b Detected only in one sub-sample. Uncertainties expressed as the extended standard uncertainty (1.96 SD).
Caesium-137 was below decision threshold (∼ 0.1 Bq/kg) except for two samples. By adding the gamma-ray spectra from several samples (measured using the same detector, live time and sample geometry) together it was possible to obtain a 662 keV peak from 137 Cs above decision threshold and giving a result of about 0.1 Bq/ kg, which can be considered as an overall average for the 137Cs in the roots. This result is consistent with the transfer factor in loamy soil of 0.014 reported by Zhu and Smolders (2000). Uranium-238 results were also below decision thresholds of around 1.6 Bq/kg. Vandenhove et al. (2009) reported a 238U transfer factor for cereal straw of 0.25 and cereal grain of 0.18, both for loamy soil. Blanco Rodríguez et al. (2008) aimed to evaluate the capacity of each granulometric fraction of the soil to liberate radionuclides in order to make estimates of their availability. This capacity was found to be dependent on both the fraction and the radionuclide. For uranium, the greater percentage of labile activity concentration was in the coarser fractions (sand or fine sand, depending on the Spanish soils analysed). In our study the most important fraction of the soil is silt (>65% except for two fields, Table 2). 3.3. Natural radionuclides in wheat stems Activity concentrations of natural radionuclides in winter wheat stems were determined from the 2005 and 2006 samples (Table 6). The overall average activity concentrations (1 SD) across the sampling years for 40K, 226Ra, 228Ra and 228Th were 221 84 Bq kg1, 0.8 0.3 Bq kg1, 1.0 0.3 Bq kg1 and 0.20 0.04 Bq kg1, respectively. The overall 228Ra/228Th activity ratio (4.9 1.3) obtained for the stem samples were about twice the value for the roots (2.9 1.4) and five times the value for the soil (1.03 0.08). This reflects the higher mobility of Ra in the stem compared with Th. A strong correlation (r ¼ 0.86, p < 0.01) was observed between 226Ra and 228 Ra with an overall 226Ra/228Ra activity ratio of 0.9 0.2 which corresponds well with 226Ra/228Ra ratios obtained in wheat straw from the UK (Smith, 1971). 3.4. Natural radionuclides in wheat grains Natural radioactivity concentrations in winter wheat grain collected during 2004e2007 are listed in Table 7. Activity concentration data for 226Ra, 228Ra and 228Th were only available for the
P. Lindahl et al. / Journal of Environmental Radioactivity 102 (2011) 163e169 Table 6 Activity concentrations (Bq kg1 dry weight) of natural radionuclides in winter wheat stems from three sampling sites in Belgium collected during 2005e2006. The activity concentrations are expressed as the weighted mean of three sub-samples from each field if not otherwise noted. Uncertainties are expressed as the weighted extended uncertainty with coverage factor of 1.96 corresponding to 95% confidence level. Sampling year Site 1 2006 Site 2 2006 Site 3 2005 2006
AS
40
226
K
228
Ra
228
Ra
Th
Table 7 Activity concentrations (Bq kg1 dry weight) of natural radionuclides in winter wheat grains from three sampling sites in Belgium collected 2004e2007. The activity concentrations are expressed as the weighted mean of three sub-samples from each field if not otherwise noted. Uncertainties are expressed as the weighted extended uncertainty with coverage factor of 1.96 corresponding to 95% confidence level. Sampling year
O C
229 26 215 25
0.71 0.07 0.93 0.09
1.08 0.17 0.78 0.19
0.18 0.10a 0.14 0.10a
O C
383 44 229 27
1.21 0.10 1.00 0.10
1.31 0.24 1.08 0.26
0.23 0.10 0.25 0.14
Ob Cb O C
133 172 128 283
Site 1 2006 2007
20 24 15 33
0.45 1.26 0.56 0.56
0.07 0.12 0.06 0.08
0.77 1.61 0.66 0.60
0.19 0.25 0.14 0.19
0.23 0.23 0.16 0.19
0.13 0.19 0.10a 0.12
AS: Agricultural system, O: Organic farming, C: Conventional farming. a Detected only in two sub-samples. b Only two sub-samples were analysed.
Site 2 2004 2006 2007 Site 3 2005 2006
2006e2007 sampling campaigns. Overall average activity concentrations (1 SD) obtained for 40K, 226Ra, 228Ra and 228Th were 115 22 Bq kg1, 0.10 0.05 Bq kg1, 0.15 0.05 Bq kg1 and 0.045 0.026 Bq kg1, respectively. The 40K activity concentrations are comparable to other reported values (Bilo et al., 1993; Drichko and Lisachenko, 1984; Pulhani et al., 2005; Schimmack et al., 2004), and the 226Ra activity concentrations are about one order of magnitude lower than levels reported from India (Pulhani et al., 2005) and in the same range as levels reported from Russia (Drichko and Lisachenko, 1984). The lower levels of radium in wheat grains compare to the reported levels in India can be explained by higher radium activity concentrations in the soil from India as well as different soil characteristics. According to Pulhani et al. (2005), the radium uptake in wheat grains is mainly affected by the nature of clay material in the soil. The overall 228Ra/228Th activity ratio (3.5 1.5) in wheat grains was in the same range as in the stems with a moderate correlation (r ¼ 0.79, p < 0.01) observed between 228Ra and 228Th. A moderate correlation (r ¼ 0.67, p < 0.01) was observed between 226Ra and 228 Ra with an overall 226Ra/228Ra activity ratio of 0.7 0.2. 3.5. Distribution of natural radionuclides in the wheat plant Distributions of natural radioactivity activity concentrations in the full set of winter wheat samples (organic and conventional added together) are shown in Fig. 2 as box plots. Potassium is an essential mineral nutrient needed for the growth of the plant and is transported together with water from the root to the grain through the stem (Taiz and Zeiger, 1998). The distribution of 40K reflects the mobility and transportation of the K from the roots to the rest of the plant with the highest activity concentration in the stem and the lowest in the roots. The gradients observed for 226Ra, 228Ra and 228 Th suggest that these radionuclides are not as metabolically active as K and there is little exchange between the different plant parts. Roots are known to retain a higher quantity of heavy metals (Bose and Bhattacharyya, 2008) as can be seen by the larger relative difference in concentrations of Th compared to K between the different plant tissues. The 226Ra/40K activity ratios (Fig. 3) clearly show the effects of higher mobility for 40K into the upper parts of the plant (stem and grain) compared to 226Ra. Similar 226Ra/40K ratios in wheat grain have been observed in fertilised and unfertilised fields by Drichko and Lisachenko (1984) and Pulhani et al. (2005). Pulhani et al. furthermore found that 226Ra and 40K
167
2007
AS
40
226
O C O C
108 89 127 124
12 10 15 14
0.089 0.060 0.121 0.210
O C O C O C
134 157 97 88 130 112
7 7 11 10 15 13
n.m n.m 0.171 0.086 0.089 0.088
O C O C C
129 133 96 76 125
15 16 11 9 14
n.m n.m 0.078 0.014 0.055 0.010 0.074 0.022
K
228
Ra
228
Ra
0.016 0.012 0.023 0.022
0.15 0.06 0.17 0.23
0.018 0.014 0.017 0.015
n.m n.m 0.18 0.12 0.13 0.16
Th
0.06 0.04 0.06 0.05
0.06 0.027 0.061 0.102
0.04a 0.020a 0.028a 0.022
0.05 0.04 0.04 0.05a
n.m n.m 0.06 0.03 0.020 0.063
0.06b 0.03a 0.011 0.019a
n.m n.m 0.11 0.05 0.08 0.05 0.23 0.14b
n.m n.m 0.016 0.014b 0.022 0.021b 0.05 0.04b
AS: Agricultural system, O: Organic farming, C: Conventional farming n.m: not measured. a Detected only in two sub-samples. b Detected only in one sub-sample; uncertainty expressed as the combined standard uncertainty with coverage factor of 1.96 corresponding to 95% confidence level.
concentrations in wheat grains were not affected by fertiliser treatment (i.e. ammonium phosphate vs none). 3.6. Concentration ratios of natural radionuclides in wheat A simple model for the uptake of any radionuclide by a plant is provided by the concentration ratio (CR) (Ehlken and Kirchner, 2002); the activity concentration in the plant (Bq kg1, dry weight) divided by the activity concentration in the soil (Bq kg1, dry weight). The CR gives a rough estimate of the uptake of a certain element within the plant. The actual uptake of an element by a plant from the soil depends on many factors including the genotype of the plant, concentrations of competing ions in the soil, the adsorption area of the roots, and the availability of the element in the soil for uptake by the roots of the plant (Ehlken and Kirchner, 2002; Greger, 2004). The average CRs and standard deviations (1 SD) for 40K, 226Ra, 228Ra and 228Th in winter wheat (root, stem and grain) from organic and conventional farming collected during 2004e2007 are listed in Table 8. Potassium-40 has in general a higher CR value in wheat than the other natural radionuclides, as stable K is a major nutrient for the growth of the plant. The uptake of Ra and Th has been suggested to depend mainly on the phosphorus and alkaline-earth concentrations in the soil (Blanco Rodríguez et al., 2002). The observed CR value in grain for 40K corresponds well with other studies in similar conditions (Bilo et al., 1993; Drichko and Lisachenko, 1984; Pulhani et al., 2005; Schimmack et al., 2004). IAEA (2010) compiled the CRs for radiological risk assessments and recommended in case of cereal grains grown in temperate environment the following CR values for K (all soil groups), Ra and Th (loamy soil): 0.74, 0.029 and 0.0027, respectively. IAEA’s report, compiled large ranges of CR values depending among other factors on the soil characteristics and plant type. Concentration ratios in cereal grains ranged from 8.0 105 to 6.7 101 for Ra and from 1.6 104 to 2.2 102 for Th. The disadvantage of the CR concept as a measure of the uptake of a certain element is the use of the total concentration in the soil instead of the available ion concentration (Baeza et al., 1996).
168
P. Lindahl et al. / Journal of Environmental Radioactivity 102 (2011) 163e169
Fig. 2. Box plots of the distribution of activity concentrations of natural radionuclides in the full set of winter wheat samples from three sampling sites in Belgium collected during 2004e2007 (organic and conventional added together). The mean and median values are represented by x and the middle horizontal line, respectively. The upper and lower limits of the boxes represent the standard deviation (1 SD) and the whiskers represent the range of the observed values.
3.7. Comparison between organic and conventional systems Statistical analyses (see Chapter 2.4) did not reveal any significant differences in concentrations of primordial radionuclides (i.e. 40K, 238 U, 226Ra, 228Ra and 228Th) in soil between agricultural systems or among environments. Furthermore, the average activity concentration ratio between organic and conventional soil was close to unity for all radionuclides (Table 9). However, a significant (p ¼ 0.003, Tukey’s test) higher activity concentration of 137Cs in soil of Marcheen-Famenne than in soil of Soignies was observed confirming the gradient of 137Cs in Belgium observed by Pommé et al. (1998). No significant difference (p > 0.05) in activity concentrations of the four radionuclides determined in wheat grains (i.e. 40K, 226Ra, 228 Ra and 228Th) was observed between the two agricultural systems or amongst the environments. Overall CR organic/conventional ratios (Table 9) showed values close to unity for stems and grains. However for roots, 40K and 228Th
showed tendencies of higher uptake in the conventional fields while there is a trend for a lower uptake of 226Ra in the same fields. Nonetheless a further study with a larger number of samples would be required to confirm such an observation. Similar long-term experiments in the USA on fields treated with P fertilisers also found no difference in U, Ra or Th concentrations in wheat grain grown on fertilised and non-fertilised soil (Mortvedt, 1994). No difference was also observed for Ra and U in vegetables grown in organic and conventional farming systems in Brazil (Lauria et al., 2009). The large residual variations observed when performing the analyses of variance reflect the high variability of each agricultural system considered in this study, which is characteristic of a farm approach experimental design. Nonetheless that is exactly the complex situation an inspector has to face when controlling an organic farm before delivering a certificate. Indeed despite the existence of norms, standards or regulation for the organic farming system, a huge variability exists. The situation is even more complex with the conventional agriculture; as a conventional farmer could for instance use manure in case it is economically relevant in a specific period of time.
Table 8 Average observed concentration ratios (Bq kg1 dry weight plant/Bq kg1 dry weight soil) in tissues from organic and conventional grown winter wheat collected from three sites in Belgium during 2004e2007. Uncertainties are expressed as one standard deviation (1 SD).
Fig. 3. 226Ra/40K activity ratios in winter wheat (root, stem and grain) and soil samples collected in Belgium during 2004e2007. The error bars represent the combined standard deviation (1 SD).
Plant AS part
40
Root
0.038 0.070 0.45 0.46 0.25 0.23
O C Stem O C Grain O C
226
K
Ra
0.013 0.046 0.025 0.027 0.24 0.026 0.12 0.034 0.12 0.0034 0.06 0.0029
228
Ra
0.022 0.037 0.007 0.025 0.011 0.026 0.023 0.029 0.0015 0.0033 0.0021 0.0036
228
Th
0.013 0.012 0.009 0.014 0.011 0.006 0.022 0.006 0.0010 0.0009 0.0018 0.0011
0.007 0.006 0.004 0.003 0.0005 0.0007
P. Lindahl et al. / Journal of Environmental Radioactivity 102 (2011) 163e169 Table 9 Average organic/conventional ratio for observed CR values in winter wheat (root, stem and grain) collected from three sites in Belgium during 2004e2007. Uncertainties are expressed as the extended standard uncertainty with coverage factor of 1.96 corresponding to 95% confidence level. Average radionuclide organic/conventional ratios in soil are included for comparison. Number of samples analysed are shown in parentheses. Plant part
40
226
Root CR Stem CR Grain CR Soil (activity)
0.55 0.14 (3) n.s 1.1 0.6 (7) 1.1 0.5 (7)
1.7 0.8 (3) n.s n.s 1.0 0.3 (7)
K
Ra
228
Ra
n.s 1.0 0.7 (4) 1.3 1.1 (5) 1.0 0.4 (7)
228
Th
0.7 0.6 (2) 1.0 0.4 (4) n.s 1.0 0.4 (7)
n.s: not significant; extended uncertainty larger than average value.
4. Conclusions The agricultural system productions tested (organic vs. conventional) in this study are not influencing the activity concentrations of the analysed radionuclides in the soils. Natural radioactivity was studied in winter wheat and the corresponding soil with the highest activity concentrations of 228Th and Ra isotopes (226Ra and 228Ra) found in the root and stem and the lowest in the grain. Potassium-40 showed the highest activity concentration in the stem and the lowest in the root. Despite the fact that wheat is not a high demanding crop for potassium, lack of this element often causes the weakening of the straw, which may result in lodging. The 228Ra/228Th ratios suggest no secular equilibrium between 232 Th and its daughters in the wheat plant. Thorium-232 cannot be determined directly using gamma-ray spectrometry but knowing its concentration would be valuable for future studies. For determination of 232Th concentration in biological material with no secular equilibrium one has to resort to alpha spectrometry or mass spectrometry. Overall CRs for K, Ra and Th in wheat grain correspond well with previously reported values (Drichko and Lisachenko, 1984; Pulhani et al., 2005). However, no significant difference was observed in the uptake of natural radionuclides between organically and conventionally grown winter wheat. Acknowledgements The authors would like to thank Mr. Ramon Carlos-Marquez for the help with the gamma-ray measurement at ITU, Karlsruhe, UNAB and the farmers for providing the wheat and soil samples, and Mr. Olivier De Rudder and Mr. Fernando Cordeiro from IRMM, Geel for carrying out the sampling campaigns. References Baeza, A., Paniagua, J., Rufo, M., Barandica, J., 1996. Bio-availability and transfer of natural radionuclides in a Mediterranean ecosystem. Applied Radiation and Isotopes 47, 939e945. Bilo, M., Steffens, W., Führ, F., Pfeffer, K.-H.,1993. Uptake of 134/137Cs in soil by cereals as a function of several soil parameters in three soil types in upper Swabia and North Rhine-Westphalia (FRG). Journal of Environmental Radioactivity 19, 25e39. Blanco Rodríguez, P., Vera Tomé, F., Lozano, J.C., 2002. About the assumption of linearity in soil-to-plant transfer factors for uranium and thorium isotopes and 226 Ra. The Science of the Total Environment 284, 167e175. Blanco Rodríguez, P., Vera Tomé, F., Lozano, J.C., Pérez-Fernández, M.A., 2008. Influence of soil texture on the distribution and availability of 238U, 230Th, and 226 Ra in soils. Journal of Environmental Radioactivity 99, 1247e1254. Bose, S., Bhattacharyya, A.K., 2008. Heavy metal accumulation in wheat plant grown in soil amended with industrial sludge. Chemosphere 70, 1264e1272. Drichko, V.F., Lisachenko, E.P., 1984. Background concentrations of 226Ra, 228Th, and 40 K in cultivated soils and agricultural plants. Soviet Journal of Ecology 15, 81e85. EFMA, 2005. Forecast of Food, Farming and Fertilizer Use in the European Union 2005-2015. Annual Forecast, Brussels, Belgium. European Fertilizer Manufacturers Association (EFMA): 7.
169
Ehlken, S., Kirchner, G., 2002. Environmental processes affecting plant root uptake of radioactive trace elements and variability of transfer factor data: a review. Journal of Environmental Radioactivity 58, 97e112. Falck, W., Wymer, D., 2006. In: Merkel, B.J., Hasche-Berger, A. (Eds.), Uranium in Phosphate Fertilizer Production. Uranium in the Environment. Springer, Berlin Heidelberg, Germany, pp. 857e866. Golmakani, S., Moghaddam, M.V., et al., 2008. Factors affecting the transfer of radionuclides from the environment to plants. Radiation Protection Dosimetry 130 (3), 368e375. Greger, M., 2004. Uptake of Nuclides by Plants. Technical Report TR-04e14. Swedish Nuclear Fuel and Waste Management Co, Stockholm, Sweden. Hult, M., Preusse, W., Gasparro, J., Köhler, M., 2006. Underground gamma-ray spectrometry. Acta Chimica Slovenica 53, 1e7. IAEA, International Atomic Energy Agency, 2010. Handbook of Parameter Values for the Prediction of Radionuclide Transfer in Terrestrial and Freshwater Environments. Technical Reports Series No 472 Vienna, Austria. ISO, International Standards Organisation, 2000. Determination of the Detection Limit and Decision Threshold for Ionising Radiation Measurements e Part 3: Fundamentals and Application to Counting Measurements by High Resolution Gamma Spectrometry, without the Influence of Sample Treatment. 11929e3 Geneva, Switzerland. Khater, A.E.M., Al-Sewaidan, H.A., 2008. Radiation exposure due to agricultural uses of phosphate fertilizers. Radiation Measurements 43 (8), 1402e1407. Lauria, D.C., Ribeiro, F.C.A., Conti, C.C., Loureiro, F.A., 2009. Radium and uranium levels in vegetables grown using different farming management systems. Journal of Environmental Radioactivity 100, 176e183. Magkos, F., Arvaniti, F., et al., 2003. Organic food: nutritious food or food for thought? A review of the evidence. International Journal of Food Sciences and Nutrition 54 (5), 357e371. Mortvedt, J.J., 1994. Plant and soil relationship of uranium and thorium decay series radionuclides e a review. Journal of Environmental Quality 23, 643e650. Nelson, W., Hirayama, H., Rogers, D., 1985. The EGS4 Code System, SLAC-265. Stanford Linear Accelerator Centre, USA. Peerani, P., Carbol, P., Hrnecek, E., Betti, M., 2002. Assessment of a Compton-event suppression g-spectrometer for the detection of fission products at trace levels. Nuclear Instruments and Methods in Physics Research A 482, 42e50. Pommé, S., Uyttenhove, J., et al., 1998. Radiocesium contamination in Belgium. Journal of Radioanalytical and Nuclear Chemistry 235 (1), 139e145. Pulhani, V.A., Dafauti, S., Hegde, A.G., Sharma, R.M., Mishra, U.C., 2005. Uptake and distribution of natural radioactivity in wheat plants from soil. Journal of Environmental Radioactivity 79, 331e346. Righi, S., Lucialli, P., Bruzzi, L., 2005. Health and environmental impacts of a fertilizer plant e Part I: assessment of radioactive pollution. Journal of Environmental Radioactivity 82, 167e182. Schimmack, W., Zimmermann, G., Sommer, M., Dietl, F., Schultz, W., Paretzke, H.G., 2004. Soil-to-grain transfer of fallout 137Cs for 28 winter wheat cultivars as observed in field experiments. Radiation and Environmental Biophysics 42, 275e284. Siderer, Y., Maquet, A., Anklam, E., 2005. Need for research to support consumer confidence in the growing organic food market. Trends in Food Science & Technology 16, 332e343. Smith, K.A., 1971. The comparative uptake and translocation by plants of calcium, strontium, barium and radium. II. Triticum vulgare (wheat). Plant and Soil 34, 643e651. Taiz, L., Zeiger, E., 1998. Plant Physiology, second ed. Sinauer Associates Inc, Sunderland, Massachusetts. UNSCEAR, United Nations Scientific Committee on the Effects of Atomic Radiations, 2000. Sources. Sources and Effects of Ionizing Radiation, vol. 1. United Nations Publication, New York. Vandenhove, H., Van Hees, M., 2007. Predicting radium availability and uptake from soil properties. Chemosphere 69, 664e674. Vandenhove, H., Olyslaegers, G., Sanzharova, N., Shubina, O., Reed, E., Shang, Z., Velasco, H., 2009. Proposal for new best estimates of the soil-to-plant transfer factor of U, Th, Ra, Pb and Po. Journal of Environmental Radioactivity 100, 721e732. Vandendriessche, H., Bries, J., Geypens, M., 1996. Experience with fertilizer expert systems for balanced fertilizer recommendations. Communications in Soil Science and Plant Analysis 27 (5), 1199e1209. Vera Tomé, F., Blanco Rodríguez, P., Lozano, J.C., 2002. Distribution and mobilization of U, Th and 226Ra in the plant-soil compartments of a mineralized uranium area in south-west Spain. Journal of Environmental Radioactivity 59, 41e60. Willer, H., Kilcher, L. (Eds.), 2009. The World of Organic Agriculture e Statistics and Emerging Trends 2009. International Federation of Organic Agriculture Movements (IFOAM), Bonn, Germany and Research Institute of Organic Agriculture (FiBL) Frick, Switzerland. Woese, K., Lange, D., et al., 1997. A comparison of organically and conventionally grown foods - results of a review of the relevant literature. Journal of the Science of Food and Agriculture 74, 281e293. Zhu, Y.G., Smolders, E., 2000. Plant uptake of radiocaesium: a review of mechanisms, regulation and application. Journal of Experimental Botany 51 (351), 1635e1645.