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Factors affecting the concentrations of lead in British wheat and barley grain
Environmental Pollution 131 (2004) 461e468 www.elsevier.com/locate/envpol
Factors affecting the concentrations of lead in British wheat and barley grain F.J. Zhaoa,), M.L. Adamsa, C. Dumonta, S.P. McGratha, A.M. Chaudria, F.A. Nicholsonb, B.J. Chambersb, A.H. Sinclairc a
Agriculture and Environment Division, Rothamsted Research, Harpenden, Hertfordshire AL5 2JQ, UK b ADAS Gleadthorpe Research Centre, Meden Vale, Mansfield, Nottinghamshire NG20 9PF, UK c Scottish Agricultural College, Craibstone, Bucksburn, Aberdeen AB21 9YA, UK Received 10 November 2003; accepted 28 February 2004
‘‘Capsule’’: A large survey showed that Pb concentrations in wheat and barley grain decreased between 1982 and 1998, although some recent samples were found to have elevated Pb due to surface contamination. Abstract The entry of Pb into the food chain is of concern as it can cause chronic health problems. The concentration of Pb was determined in cereal grain samples collected representatively from British Cereal Quality Surveys in 1982 and 1998 (n ¼ 176, 250 and 233 for wheat collected in 1982 and 1998, and barley in 1998, respectively). In addition, paired soil and grain samples were collected from 377 sites harvested across Britain in 1998e2000. Wheat grain Pb ranged from below the analytical detection limit (0.02 mg kg1 dry weight, DW) to 1.63 mg kg1 DW, and barley grain Pb from !0.02 to 0.48 mg kg1 DW. The vast majority of samples (O99% for both wheat and barley, excluding Scottish barley samples collected in 2000) were well below the newly introduced EU limit for the maximum permissible concentration of Pb in cereals (0.2 mg kg1 fresh weight, equivalent to 0.235 mg kg1 DW). There was a significant reduction in wheat grain Pb in the 1998 survey compared with the 1982 survey. However, 40 barley samples collected from Scotland in 2000 in the paired soil and crop survey showed anomalously high concentrations of Pb, with 10 samples exceeding the EU limit. Washing experiments demonstrated that surface contamination, introduced during grain harvest and/or storage, was the main reason for the high concentrations in these samples. In the paired soil and crop surveys, there were no significant correlations between grain Pb concentrations with total soil Pb and other soil properties, indicating low bioavailability of Pb in the soils and limited uptake and transport of Pb to grain. The Pb in cereal grain is likely to originate mainly from atmospheric deposition and other routes of surface contamination during harvest and storage. Ó 2004 Elsevier Ltd. All rights reserved. Keywords: Lead; Cadmium; Barley; Wheat; Food contamination; Regulations
1. Introduction Lead (Pb) is ubiquitous in the environment. It is a physiological and neurological toxin, and probably carcinogenic to humans. Pb poisoning, especially in young children, is an environmental and public hazard of global proportions (Adriano, 2001). The most important pathways of human Pb intake are ingestion ) Corresponding author. Tel.: C44-1582-763133; fax: C44-1582760981. E-mail address: [email protected] (F.J. Zhao). 0269-7491/$ - see front matter Ó 2004 Elsevier Ltd. All rights reserved. doi:10.1016/j.envpol.2004.02.011
of paint chips from Pb-painted surfaces, inhalation of Pb from automobile emissions, food from Pb-soldered cans and drinking water from Pb-soldered plumbing. Foods may contain Pb from the environment (e.g. uptake by plant roots or foliage) or from food processing and storage (e.g. containers). The transfer of Pb from soil to crop tissues is generally low. A review of literature indicated that the bioconcentration factor, i.e. the concentration ratio of Pb in plant tissues to Pb in soil, ranged mostly from 0.001 to 0.5, depending on plant species, environmental conditions and experimental setup (Chamberlain, 1983). In soils
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with background levels of Pb, foliar uptake of Pb from the atmosphere has been shown to be the predominant route of entry to plants. Studies using an isotopelabelling technique show that O90% of total Pb in ryegrass and wheat was derived from atmospheric Pb (Tjell et al., 1979; Dalenberg and Vandriel, 1990). Pb is released to the atmosphere from coal-burning power generation, smelting, incineration of wastes and, most prominently, the combustion of leaded petrol. Since 1970 Pb emissions to the atmosphere have declined by 97% in the UK (National Atmospheric Emissions Inventory, 2003). The Pb content of leaded petrol was reduced from around 0.34 to 0.143 g L1 in 1986 and since 1987 sales of unleaded petrol have increased rapidly. Leaded petrol was phased out from general sale at the end of 1999. A study by Jones and Johnston (1991) showed that the concentration of Pb in herbage at a semi-rural site in the UK decreased significantly following the enforced reduction of Pb use in petrol. Recently, the European Union has introduced legislation defining the maximum permissible concentrations (MPC) for Pb in a range of foodstuffs (European Commission, 2001). The MPC for cereals, including wheat (Triticum aestivum L.) and barley (Hordeum vulgare L.) grain, is 0.2 mg kg1 fresh weight (FW), equivalent to 0.235 mg kg1 DW assuming an average 15% moisture content in grain. Analysis of wheat and barley grain samples collected in the US, Austria, Finland, Germany and The Netherlands showed a range of Pb concentrations from below the analytical detection limit to 0.72 mg kg1 FW (Wolnik et al., 1983; Wiersma et al., 1986). Although the majority of the grain samples analysed contained !0.2 mg Pb kg1 FW, a proportion of samples in the different surveys exceeded the current EU MPC. The presence of high concentrations of contaminant metals in agricultural produce can limit its usage or sale in the international community. Analysis of a range of foods produced in the UK showed that most of the samples contained less than 0.05 mg Pb kg1 DW (Thornton and Culbard, 1986). However, there have been no systematic studies of the range and distribution of Pb concentrations in wheat and barley grain produced nation-wide in the UK. In light of the new EU regulations, we analysed Pb concentrations in wheat and barley grain samples collected from a representative nation-wide survey and from surveys of paired soils and crops from major cereal growing areas in the UK, with the aim of assessing whether cereals produced in the UK can meet the new Pb limit. We also analysed archived wheat grain samples, which were collected in 1982, to evaluate whether Pb concentrations in wheat grain had decreased since the introductions of low-Pb or Pb-free petrol in 1986. Furthermore, we explored the relationship between grain Pb concentrations and soil properties, and examined whether elevated Pb concentrations in some grain samples were caused by surface contamination.
2. Materials and methods 2.1. Cereal quality surveys Since 1974 the Home-Grown Cereals Authority (HGCA) in the UK has conducted an annual Cereal Quality Survey (CQS). In 1998, 250 wheat and 233 barley grain samples were collected from throughout Britain. These samples were selected at random from different regions of England (East, South Eastern, South Western, Western, Midlands and Northern), Wales and Scotland in approximate proportion to the amount of the crop being grown in that area. Within each region the number of samples of each variety collected was also related to the area of that variety grown. Therefore, these surveys can be considered as representative of the cereal growing area each year. In addition, we retrieved 176 wheat grain samples collected in the 1982 CQS, which had been stored in the Rothamsted Archive. Crop variety and sampling location (by county) were recorded. Grid references were recorded for each sample collected in the 1982 CQS. Grain samples were analysed for Pb as described below. 2.2. Paired crop and soil samples Paired soil and crop samples from wheat and barley crops were collected across the main cereal growing areas in Britain shortly before harvest. A total of 34, 61 and 67 paired soil and wheat samples were collected in the 1998, 1999 and 2000 harvest years, respectively. All but 11 of the wheat samples were winter varieties. For barley, 27, 95 and 93 paired samples were collected, respectively, in the three years. Of the barley samples, 125 were spring barley and 90 winter barley. Sites were selected on commercial farms to represent a range of soil types. In 1999 and 2000, some sites with potentially high concentrations of soil Pb were targeted, including soils of naturally high background levels due to geochemical factors, potential contamination from past sewage sludge/industrial or other waste applications, and proximity to major roads or motorways. Information recorded at the sampling site included details of site and sampling location, soil type, history of manure and/ or sewage sludge applications in the last 10 years, fertiliser inputs, crop variety, drilling and harvest dates, and proximity of the sampling location to any major roads or industrial sites. At each site, a 1 m2 quadrat was placed at random in the field to be sampled. A 0e15 cm topsoil sample (ca. 1 kg in weight and comprising 15 cores) was obtained by manual coring within the quadrat area. A crop sample was collected at the same time by hand-cutting the crop near ground level from all of the marked quadrat area. The sample was subsequently threshed and the resulting grain sample retained for analysis.
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2.3. Soil and grain analyses Soil samples were air dried and ground to pass through a 2-mm sieve. Soil pH was determined using a glass electrode in a soil:water ratio of 1:2.5. Soil organic matter was determined by loss on ignition based on the method described by Ball (1964). Soil Al, Fe and Mn oxides were extracted using a mixture of ammonium oxalate and oxalic acids (0.114/0.086 M) following the procedure of Janssen et al. (1997), before determination by inductively-coupled plasma atomic emission spectrometry ICP-AES (Fisons ARL Accuris, Ecublens, Switzerland). A portion of each soil sample was finely ground to !150 mm in an agate ball mill. Subsamples of 0.25 g were digested with aqua regia (4:1 v/v concentrated HCleHNO3), following the method of McGrath and Cunliffe (1985). Pb concentrations in the digest solutions were determined by graphite-furnace atomic absorption spectrometry (GF-AAS; Perkin Elmer 4100-ZL, Norwalk, USA). Samples of wheat and barley grain were ground to !0.5 mm using a Reitch ultracentrifugal stainless steel mill, and oven dried at 80 (C before analysis. Subsamples (ca. 1 g) of the dried and ground grain were digested in XP1500plus TeflonÒ PFA microwave liners (CEM Corp, Matthews, NC) using 3 mL of Primar ultra-pure concentrated nitric acid (70% w/v) (Fisher Scientific), 2 mL of Primar 30% w/v hydrogen peroxide (Fisher Scientific) and 7 mL ultra-pure water (18 MU specific resistance; ELGA Maxima, High Wycombe, UK). Digestion was carried out at 115 (C for 1 min and 175 (C for 10 min, both at a maximal pressure of 450 psi, using a CEM model Mars X microwave oven. After completion of the heating process, the vessels were allowed to cool before the contents were quantitatively transferred to 25 mL volumetric flask and made up to 25 mL with ultra-pure water prior to analysis (Adams et al., 2003). Pb concentrations in the digest solutions were determined by GF-AAS. Quality control was ensured by inclusion of the certified reference material BCR CRM191 brown bread and one blank vessel in each batch of samples. All glassware and microwave vessels were acid-washed (5% v/v HNO3) and thoroughly rinsed with de-ionised and ultra-pure water before use.
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water, (2) 0.05 M ethylenediaminetetraacetic acid (EDTA) or (3) 1% (v/v) HNO3. The grain samples were subsequently rinsed with ultra-pure water, before being dried (80 (C for 24 h) and microwave digested (see above). The 10 mL washing solutions (which contained particulate matter washed off the grain samples) were evaporated to approximately 1 mL volume, before being digested using the aqua regia method described above. The grain and washing digest solutions were analysed for Pb by GF-AAS, while marker elements (e.g. titanium) which indicate the presence of soil/dust contamination in plant samples were analysed by ICP-AES. For comparison, 10 additional barley samples with a wide range of cadmium (Cd) concentrations were selected and washed as described above. The effect of washing on grain Cd concentration was determined. 2.5. Statistical analyses Statistical analyses, including multiple linear regression and analysis of variance (ANOVA) were performed using Genstat 5 for Windows (Numerical Algorithms Group, 1998). Where appropriate, variates that showed skewed distributions were log-transformed prior to statistical testing to stabilise variance. For samples having Pb concentrations below the analytical detection limit (!0.02 mg kg1 DW), concentrations equal to half the value of the detection limit were used in the subsequent statistical analyses.
3. Results and discussion 3.1. Quality control Repeated analysis of the certified reference material BCR CRM191 brown bread gave a mean Pb concentration of 0.185 mg kg1 (SD 0.020 mg kg1, n ¼ 28). This mean value was very close to the certified value of 0.187 mg kg1 ( G confidence limit 0.014 mg kg1). The results show that the digestion and analysis procedures used were reproducible and accurate for Pb analysis. The detection limit of the GF-AAS used was 0.8 mg Pb L1 in solution, which was equivalent to a detection limit of 0.020 mg kg1 DW of Pb in grain samples.
2.4. Grain washing experiments 3.2. Cereals quality survey To establish whether high concentrations of Pb measured in some barley grain samples occurred as a result of plant uptake or were due to external factors such as surface contamination prior to analysis, a series of grain washing experiments was performed. Ten samples of barley grain collected in 2000 from Scotland were used in this experiment. Subsamples of whole grain (5 g) were rinsed for 2 min with 10 mL of either (1) ultra-pure
Fig. 1 shows the frequency distributions and boxplots of Pb concentrations in wheat grain samples collected in the 1982 and 1998 CQS, and also in barley grain samples collected in 1998. In 1982, the concentration of Pb in wheat grain ranged from below the detection limit (0.02 mg kg1 DW) to 1.63 mg kg1 DW, with a median of 0.043 mg kg1 DW. Only 1 out of 176
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Fig. 1. Frequency distributions (a) and box-plots of the Pb concentrations (b) in wheat and barley grain from the 1982 and 1998 Cereal Quality Surveys. Samples with Pb concentrations lower than the detection limit (0.02 mg kg1 DW) were assigned a value of 0.02 mg kg1 DW for the construction of frequency distribution and box-plot. The central line within each box is the median, and the bottom and top of each box represent the 25th and 75th percentiles, respectively. The whiskers represent the 10th and 90th percentiles, respectively, and values outside this range are plotted as individual outliers (B).
samples (0.6%) contained higher than the current EU MPC (0.235 mg kg1 DW), and 9 samples (5.1%) had a Pb concentration below the detection limit. In 1998, 13 years after the enforced reduction of Pb added to petrol, there was a clear shift toward lower Pb concentrations in wheat grain. The concentration range measured in 1998 was from below the detection limit to 0.11 mg kg1 DW, with a median of 0.022 mg kg1 DW. None of the 250 samples collected in 1998 exceeded the current EU MPC, and moreover 45% of the samples had Pb concentrations below the detection limit. The difference between the two surveys was highly significant (P ! 0:001) according to ANOVA. The significant decrease in wheat grain Pb from 1982 to 1998 was probably due to the eightfold decrease in the atmospheric emissions of Pb that took place during the same period in the UK (National Atmospheric Emissions Inventory, 2003). Jones and Johnston (1991) showed that the reduction of Pb added to petrol at the beginning of 1986 resulted in a decline in the concentrations of Pb in herbage from long-term experiments at Rothamsted, UK. The median value in our 1982 survey was larger than the median of 0.017 mg Pb kg1 FW in 288 wheat grain samples collected in the early 1980s from uncontaminated sites in the US (Wolnik et al., 1983). By 1998, the median value of Pb in British wheat was similar to the US median. In contrast, Wiersma et al. (1986) found higher concentrations of Pb (0.03e0.65 mg kg1 FW, with a median of 0.14 mg kg1 FW) in 84 wheat grain samples collected in 1976e1977 in The Netherlands. The relatively high concentrations of Pb in Dutch wheat grain samples, compared with the US and British samples, could be due to high atmospheric concentrations of Pb, contamination during sampling and storage, or inaccurate analysis. No information of analytical precision and accuracy was given by Wiersma et al. (1986).
In the 1982 survey, which included the grid reference for the location of each sample, Pb concentrations were mapped (Fig. 2). There was no clear pattern in the geographical distribution of wheat grain Pb. Most of the samples were collected from main cereal growing areas in Britain, i.e. in rural or semi-rural environments. Because the combustion of leaded petrol had been the main source of atmospheric Pb until recently, and the level of atmospheric Pb has a predominant influence on plant Pb concentrations (Chamberlain, 1983; Jones and Johnston, 1991), the short-distance influence of road transport is likely to contribute significantly to the
Pb (mg kg-1 DW) >0.100 0.075 – 0.100 0.050 – 0.075 0.025 – 0.050 <0.025
Fig. 2. Geographical distribution of the Pb concentration in wheat grain from the 1982 Cereal Quality Survey.
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variation of wheat grain Pb. This short-distance influence would not be reflected in the map shown in Fig. 2. Similarly, there were no significant differences between regions in wheat Pb concentrations in the 1998 survey. Significant (P ! 0:05) cultivar differences in mean lead concentrations were observed (data not shown). However, it is difficult to separate true cultivar differences from environmental variation in the surveys conducted. The concentration of Pb in barley grain collected in 1998 ranged from below the detection limit to 0.476 mg kg1 DW, with a median of 0.029 mg kg1 DW (n ¼ 233; Fig. 1). About 30% of the samples were around or below the detection limit for Pb. All except two samples (0.9%) contained a concentration of Pb below the current EU MPC. Analysis of variance showed that there were no significant differences in the concentrations of Pb in barley grain between different regions and between different cultivars. The concentrations of Pb in this survey were similar to those reported in the barley grain samples in Finland, but lower than those reported in barley grains in The Netherlands (Wiersma et al., 1986). The Pb concentrations in barley grain were generally higher than those in wheat grain collected in the same year (1998). A possible explanation for this difference is that barley grain is more exposed to the effects of atmospheric Pb and dust deposition than wheat grain; the latter is enclosed by glumes in floral spikelets.
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DW (Fig. 3). A large proportion of the wheat samples (ca. 50% of the total) contained concentrations of Pb that were below the detection limit. The frequency distribution (Fig. 3) was similar to that for the 1998 CQS data (Fig. 1). None of the wheat grain samples exceeded the EU MPC for Pb, even though, in this series of surveys, some sites with high soil Pb concentrations (up to 783 mg kg1) were sampled. Differences in mean Pb concentrations between cultivars were not significant. Pb concentrations in barley grain collected in the three harvest years (1998e2000; excluding samples from Scotland in 2000, see below) were low, ranging from below the detection limit to 0.131 mg kg1 DW, with a median of 0.030 mg kg1 DW (Fig. 3). No samples exceeded the current EU MPC for Pb. A substantial number of samples (42%) had Pb concentrations lower than the analytical detection limit. In common with the 1998 CQS data, the concentrations of Pb in barley grain were generally higher than those of wheat grain in the paired soil and crop surveys. Grain samples of barley collected from Scotland in the 2000 harvest year (n ¼ 40) appeared to have anomalously high concentrations of Pb, with a range of 0.078e0.309 mg kg1 DW and a median of 0.170 mg kg1 DW (Fig. 3). Ten of the 40 samples exceeded the EU MPC of 0.235 mg kg1 DW. Surface contamination was found to be responsible for the elevated Pb concentrations in this set of samples (see below).
3.3. Paired soil and crop surveys 3.4. Relationship with soil properties One hundred and sixty-two paired soil and wheat grain samples were collected in three harvest years (1998e2000). The concentration of Pb in wheat grain ranged from less than the analytical detection limit to 0.194 mg kg1 DW, with a median of 0.020 mg kg1
In the paired soil and crop surveys, soil properties varied widely (Table 1). For example, the concentration of total Pb in soil ranged from 4.8 to 783 mg kg1, and soil pH from 5.2 to 8.3. Multiple regression was used to
Fig. 3. Frequency distributions (a) and box-plots of the Pb concentrations (b) in wheat and barley grain from the paired soil and crop surveys in 1998e2000. Samples with Pb concentrations lower than the detection limit (0.02 mg kg1 DW) were assigned a value of 0.02 mg kg1 DW for the construction of frequency distribution and box-plot. See Fig. 1 legend for explanation of box-plots. In the case of wheat, the median was at the detection limit.
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Table 1 Summary of soil properties from the paired soil and crop surveys Crop
pH
Organic Al oxides Fe oxides Total Pb matter (%) (g Al kg1) (g Fe kg1) (mg kg1)
Barley Range 5.4e8.3 0.7e12.6 Mean 7.0 3.4 Median 6.9 2.9
0.18e4.6 1.5 1.2
0.40e10.0 4.8e783 3.4 40 3.1 26
Wheat Range 5.2e8.3 0.9e24.6 Mean 7.3 5.6 Median 7.6 4.5
0.40e3.8 1.3 1.1
0.31e17.4 15e772 3.6 56 2.9 32
analyse relationships between grain Pb concentration and soil properties. Despite wide variations in soil properties, none of the soil properties examined, either alone or in combination, could explain the variation of Pb concentration in wheat or barley grain. This is in contrast to Cd, for which soil pH and soil total Cd together explained 53% of the variation in Cd concentrations in wheat grain in the same surveys (Adams et al., 2004). Grain samples collected from the survey sites having elevated soil concentrations of Pb (e.g. O100 mg kg1) did not contain elevated levels of Pb. The results are consistent with the fact that the main entry route of Pb to plants is via atmospheric deposition (Tjell et al., 1979; Chamberlain, 1983; Dalenberg and Vandriel, 1990). Pb generally has a very low solubility in soil, and plants such as wheat and barley do not take up much Pb or transport Pb to grain (Lu¨bben and Sauerbeck, 1991; Hooda et al., 1997). Baumhardt and Welch (1972) studied Pb uptake by corn in a field experiment where 8 rates of lead acetate up to
3200 kg Pb ha1 were applied to the soil. They found that Pb additions to soil increased the concentrations of Pb in leaves and stalks, but did not affect the concentration of Pb in corn grain, again indicating negligible transport of Pb from leaves and stalks to grain.
3.5. Grain washing experiments A brief (2 min) washing with ultra-pure H2O, 0.05 M EDTA or 1% HNO3 reduced the concentrations of Pb substantially in the 10 barley grain samples collected from Scotland in 2000 (Fig. 4a). On average, washing with ultra-pure H2O, 0.05 M EDTA or 1% HNO3 removed 30, 62 and 77% of the Pb from the grain samples, respectively. Analysis of the wash solutions for these samples also showed high concentrations of Pb (data not shown), confirming that substantial amounts of Pb were removed by washing. The results indicate that the main reason for the high Pb concentrations measured in the Scottish barley samples collected in 2000 was surface contamination, rather than true uptake by plants. Titanium (Ti) concentrations were also determined in the wash solutions after digestion. Ti is commonly used as a marker to indicate the presence of soil or dust in crop samples, because it is hardly taken up by crops despite significant concentrations being present in soil. However, there was no indication of elevated Ti levels in the wash solutions, and therefore it is unlikely that the surface contamination of the Scottish barley samples was due to soil. Surface contamination could occur as a result of atmospheric deposition.
Fig. 4. Effects of washing for 2 min with H2O, 0.05 M EDTA or 1% HNO3 on grain Pb concentrations (a) and Cd concentrations (b). For Pb, 10 barley grain samples were selected from the Scottish survey in 2000. For Cd, 10 barley grain samples with high Cd were selected from the whole of the paired soil and crop surveys.
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Although atmospheric deposition undoubtedly contributed to grain Pb, this was unlikely to be the main reason causing the anomalously high concentrations of Pb in the 40 Scottish barley samples collected in 2000. Atmospheric inputs in most arable areas in Scotland are probably lower than those in England, and there is no reason to suspect that atmospheric deposition of Pb in Scotland would be much higher in 2000 than in the two previous seasons. It is likely that surface contamination occurred during harvest, threshing or sample storage prior to analysis. Contamination during sample grinding or analysis can be ruled out, because all samples were ground in the same way using the same stainless steel mill, and analysed together. In contrast to Pb, washing removed little of the grain Cd (Fig. 4b). On average, washing of 10 grain samples for 2 min with H2O, 0.05 M EDTA or 1% HNO3 removed 4.2, 6.7 and 7.7% of the grain Cd. There was good agreement between the concentrations of Cd in the grain samples before and after washing. The results demonstrate that most of the grain Cd was inside the grain, and plant uptake was the main pathway contributing to the high concentrations of Cd measured in the samples. Similar to our findings with cereal grain, Nicholson et al. (1995) showed that washing herbage samples prior to analysis made no difference to their Cd concentrations, indicating little surface contamination with Cd.
4. Conclusions The concentration of Pb was determined in 483 grain samples of wheat and barley from the 1998 Cereals Quality Survey and on 377 paired soil and grain samples collected from the 1998e2000 harvests. In addition, 176 archived wheat grain samples from the 1982 Cereal Quality Survey were also analysed for Pb. The samples were collected from the main cereal growing areas in the UK. The vast majority of samples (O99% for both wheat and barley samples, excluding the Scottish barley samples collected in 2000) were below the newly introduced European Commission limits specifying the maximum permissible concentration of Pb in foodstuffs (Pb in both barley and wheat grain 0.2 mg kg1 fresh weight, equivalent to 0.235 mg kg1 dry weight). There was a significant decrease in wheat grain Pb from 1982 to 1998, reflecting a marked reduction in Pb emissions. However, 40 barley samples collected from Scotland in 2000 in the paired soil and crop survey showed anomalously high concentrations of Pb, with 10 samples exceeding the EU limit. Washing experiments demonstrated that surface contamination, introduced during grain harvest and/or storage, was the main reason for the high concentrations in these samples. In the paired soil and crop surveys, there were no significant
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correlations between grain Pb concentrations and soil properties, such as total Pb concentration, soil pH, organic matter content, and contents of Fe, Al and Mn oxides, singly or in various combinations. The lack of a significant relationship was attributed to the low bioavailability of Pb in soils and limited uptake and transport of Pb to grain in wheat and barley.
Acknowledgements This work was funded by the UK Home-Grown Cereals Authority (HGCA) and the Royal Agricultural Society of England Hills Bequest. Rothamsted Research receives grant-aided support from the UK Biotechnology and Biological Sciences Research Council.
References Adams, M.L., Chaudri, A.M., Rousseau, I., McGrath, S.P., 2003. A practical evaluation of microwave and conventional wet digestion techniques for the determination of Cd, Cu and Zn in wheat grain. International Journal of Environmental and Analytical Chemistry 83, 307e314. Adams, M.L., Zhao, F.J., McGrath, S.P., Nicholson, F.A., Chambers, B.J., 2004. Predicting cadmium concentrations in wheat and barley grain using soil properties. Journal of Environmental Quality 33, 532e541. Adriano, D.C., 2001. Trace Elements in Terrestrial Environments: Biogeochemistry, Bioavailability, and Risks of Metals. SpringerVerlag, New York. Ball, D.F., 1964. Loss-on-ignition as an estimate of organic matter and organic carbon in non-calcareous soils. Journal of Soil Science 15, 84e92. Baumhardt, G.R., Welch, L.F., 1972. Lead uptake and corn growth with soil-applied lead. Journal of Environmental Quality 1, 92e94. Chamberlain, A.C., 1983. Fallout of lead and uptake by crops. Atmospheric Environment 17, 693e706. Dalenberg, J.W., Vandriel, W., 1990. Contribution of atmospheric deposition to heavy metal concentrations in field crops. Netherlands Journal of Agricultural Science 38, 369e379. European Commission, 2001. Commission Regulation (EC) No 466/2001 of 8 March 2001 setting maximum levels for certain contaminants in foodstuffs. Official Journal of the European Communities L77, 1e13. Hooda, P.S., McNulty, D., Alloway, B.J., Aitken, M.N., 1997. Plant availability of heavy metals in soils previously amended with heavy applications of sewage sludge. Journal of the Science of Food and Agriculture 73, 446e454. Janssen, R.P.T., Peijnenburg, W.J.G.M., Posthuma, L., Vanden Hoop, M., 1997. Equilibrium partitioning of heavy metals in Dutch field soils. 1. Relationship between metal partition coefficients and soil characteristics. Environmental Toxicology and Chemistry 16, 2470e2478. Jones, K.C., Johnston, A.E., 1991. Significance of atmospheric inputs of lead to grassland at one site in the United Kingdom since 1860. Environmental Science and Technology 25, 1174e1178. Lu¨bben, S., Sauerbeck, D., 1991. The uptake and distribution of heavy metals by spring wheat. Water, Air and Soil Pollution 57e58, 239e247. McGrath, S.P., Cunliffe, C.H., 1985. A simplified method for the extraction of the metals Fe, Zn, Cu, Ni, Cd, Pb, Cr, Co and Mn
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from soils and sewage sludges. Journal of the Science of Food and Agriculture 36, 794e798. National Atmospheric Emissions Inventory, 2003. Available from: http://www.naei.org.uk/ (access confirmed on 12 February 2004). Nicholson, F.A., Jones, K.C., Johnston, A.E., 1995. The significance of the retention of atmospherically deposited cadmium on plantsurfaces to the cadmium content of herbage. Chemosphere 31, 3043e3049. Numerical Algorithms Group, 1998. Genstat 5 for Windows Release 4.1. NAG Ltd., Oxford, UK. Thornton, I., Culbard, E., 1986. Lead in the Home Environment. Science Reviews, Northwood, UK.
Tjell, J.C., Hovmand, M.F., Mosbaek, H., 1979. Atmospheric lead pollution of grass grown in a background area in Denmark. Nature 280, 425e426. Wiersma, D., Vangoor, B.J., Vanderveen, N.G., 1986. Cadmium, lead, mercury, and arsenic concentrations in crops and corresponding soils in the Netherlands. Journal of Agricultural and Food Chemistry 34, 1067e1074. Wolnik, K.A., Fricke, F.L., Capar, S.G., Braude, G.L., Meyer, M.W., Satzger, R.D., Bonnin, E., 1983. Elements in major raw agricultural crops in the United States. 1. Cadmium and lead in lettuce, peanuts, potatoes, soybeans, sweet corn, and wheat. Journal of Agricultural and Food Chemistry 31, 1240e1244.
Factors affecting the concentrations of lead in British wheat and barley grain F.J. Zhaoa,), M.L. Adamsa, C. Dumonta, S.P. McGratha, A.M. Chaudria, F.A. Nicholsonb, B.J. Chambersb, A.H. Sinclairc a
Agriculture and Environment Division, Rothamsted Research, Harpenden, Hertfordshire AL5 2JQ, UK b ADAS Gleadthorpe Research Centre, Meden Vale, Mansfield, Nottinghamshire NG20 9PF, UK c Scottish Agricultural College, Craibstone, Bucksburn, Aberdeen AB21 9YA, UK Received 10 November 2003; accepted 28 February 2004
‘‘Capsule’’: A large survey showed that Pb concentrations in wheat and barley grain decreased between 1982 and 1998, although some recent samples were found to have elevated Pb due to surface contamination. Abstract The entry of Pb into the food chain is of concern as it can cause chronic health problems. The concentration of Pb was determined in cereal grain samples collected representatively from British Cereal Quality Surveys in 1982 and 1998 (n ¼ 176, 250 and 233 for wheat collected in 1982 and 1998, and barley in 1998, respectively). In addition, paired soil and grain samples were collected from 377 sites harvested across Britain in 1998e2000. Wheat grain Pb ranged from below the analytical detection limit (0.02 mg kg1 dry weight, DW) to 1.63 mg kg1 DW, and barley grain Pb from !0.02 to 0.48 mg kg1 DW. The vast majority of samples (O99% for both wheat and barley, excluding Scottish barley samples collected in 2000) were well below the newly introduced EU limit for the maximum permissible concentration of Pb in cereals (0.2 mg kg1 fresh weight, equivalent to 0.235 mg kg1 DW). There was a significant reduction in wheat grain Pb in the 1998 survey compared with the 1982 survey. However, 40 barley samples collected from Scotland in 2000 in the paired soil and crop survey showed anomalously high concentrations of Pb, with 10 samples exceeding the EU limit. Washing experiments demonstrated that surface contamination, introduced during grain harvest and/or storage, was the main reason for the high concentrations in these samples. In the paired soil and crop surveys, there were no significant correlations between grain Pb concentrations with total soil Pb and other soil properties, indicating low bioavailability of Pb in the soils and limited uptake and transport of Pb to grain. The Pb in cereal grain is likely to originate mainly from atmospheric deposition and other routes of surface contamination during harvest and storage. Ó 2004 Elsevier Ltd. All rights reserved. Keywords: Lead; Cadmium; Barley; Wheat; Food contamination; Regulations
1. Introduction Lead (Pb) is ubiquitous in the environment. It is a physiological and neurological toxin, and probably carcinogenic to humans. Pb poisoning, especially in young children, is an environmental and public hazard of global proportions (Adriano, 2001). The most important pathways of human Pb intake are ingestion ) Corresponding author. Tel.: C44-1582-763133; fax: C44-1582760981. E-mail address: [email protected] (F.J. Zhao). 0269-7491/$ - see front matter Ó 2004 Elsevier Ltd. All rights reserved. doi:10.1016/j.envpol.2004.02.011
of paint chips from Pb-painted surfaces, inhalation of Pb from automobile emissions, food from Pb-soldered cans and drinking water from Pb-soldered plumbing. Foods may contain Pb from the environment (e.g. uptake by plant roots or foliage) or from food processing and storage (e.g. containers). The transfer of Pb from soil to crop tissues is generally low. A review of literature indicated that the bioconcentration factor, i.e. the concentration ratio of Pb in plant tissues to Pb in soil, ranged mostly from 0.001 to 0.5, depending on plant species, environmental conditions and experimental setup (Chamberlain, 1983). In soils
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with background levels of Pb, foliar uptake of Pb from the atmosphere has been shown to be the predominant route of entry to plants. Studies using an isotopelabelling technique show that O90% of total Pb in ryegrass and wheat was derived from atmospheric Pb (Tjell et al., 1979; Dalenberg and Vandriel, 1990). Pb is released to the atmosphere from coal-burning power generation, smelting, incineration of wastes and, most prominently, the combustion of leaded petrol. Since 1970 Pb emissions to the atmosphere have declined by 97% in the UK (National Atmospheric Emissions Inventory, 2003). The Pb content of leaded petrol was reduced from around 0.34 to 0.143 g L1 in 1986 and since 1987 sales of unleaded petrol have increased rapidly. Leaded petrol was phased out from general sale at the end of 1999. A study by Jones and Johnston (1991) showed that the concentration of Pb in herbage at a semi-rural site in the UK decreased significantly following the enforced reduction of Pb use in petrol. Recently, the European Union has introduced legislation defining the maximum permissible concentrations (MPC) for Pb in a range of foodstuffs (European Commission, 2001). The MPC for cereals, including wheat (Triticum aestivum L.) and barley (Hordeum vulgare L.) grain, is 0.2 mg kg1 fresh weight (FW), equivalent to 0.235 mg kg1 DW assuming an average 15% moisture content in grain. Analysis of wheat and barley grain samples collected in the US, Austria, Finland, Germany and The Netherlands showed a range of Pb concentrations from below the analytical detection limit to 0.72 mg kg1 FW (Wolnik et al., 1983; Wiersma et al., 1986). Although the majority of the grain samples analysed contained !0.2 mg Pb kg1 FW, a proportion of samples in the different surveys exceeded the current EU MPC. The presence of high concentrations of contaminant metals in agricultural produce can limit its usage or sale in the international community. Analysis of a range of foods produced in the UK showed that most of the samples contained less than 0.05 mg Pb kg1 DW (Thornton and Culbard, 1986). However, there have been no systematic studies of the range and distribution of Pb concentrations in wheat and barley grain produced nation-wide in the UK. In light of the new EU regulations, we analysed Pb concentrations in wheat and barley grain samples collected from a representative nation-wide survey and from surveys of paired soils and crops from major cereal growing areas in the UK, with the aim of assessing whether cereals produced in the UK can meet the new Pb limit. We also analysed archived wheat grain samples, which were collected in 1982, to evaluate whether Pb concentrations in wheat grain had decreased since the introductions of low-Pb or Pb-free petrol in 1986. Furthermore, we explored the relationship between grain Pb concentrations and soil properties, and examined whether elevated Pb concentrations in some grain samples were caused by surface contamination.
2. Materials and methods 2.1. Cereal quality surveys Since 1974 the Home-Grown Cereals Authority (HGCA) in the UK has conducted an annual Cereal Quality Survey (CQS). In 1998, 250 wheat and 233 barley grain samples were collected from throughout Britain. These samples were selected at random from different regions of England (East, South Eastern, South Western, Western, Midlands and Northern), Wales and Scotland in approximate proportion to the amount of the crop being grown in that area. Within each region the number of samples of each variety collected was also related to the area of that variety grown. Therefore, these surveys can be considered as representative of the cereal growing area each year. In addition, we retrieved 176 wheat grain samples collected in the 1982 CQS, which had been stored in the Rothamsted Archive. Crop variety and sampling location (by county) were recorded. Grid references were recorded for each sample collected in the 1982 CQS. Grain samples were analysed for Pb as described below. 2.2. Paired crop and soil samples Paired soil and crop samples from wheat and barley crops were collected across the main cereal growing areas in Britain shortly before harvest. A total of 34, 61 and 67 paired soil and wheat samples were collected in the 1998, 1999 and 2000 harvest years, respectively. All but 11 of the wheat samples were winter varieties. For barley, 27, 95 and 93 paired samples were collected, respectively, in the three years. Of the barley samples, 125 were spring barley and 90 winter barley. Sites were selected on commercial farms to represent a range of soil types. In 1999 and 2000, some sites with potentially high concentrations of soil Pb were targeted, including soils of naturally high background levels due to geochemical factors, potential contamination from past sewage sludge/industrial or other waste applications, and proximity to major roads or motorways. Information recorded at the sampling site included details of site and sampling location, soil type, history of manure and/ or sewage sludge applications in the last 10 years, fertiliser inputs, crop variety, drilling and harvest dates, and proximity of the sampling location to any major roads or industrial sites. At each site, a 1 m2 quadrat was placed at random in the field to be sampled. A 0e15 cm topsoil sample (ca. 1 kg in weight and comprising 15 cores) was obtained by manual coring within the quadrat area. A crop sample was collected at the same time by hand-cutting the crop near ground level from all of the marked quadrat area. The sample was subsequently threshed and the resulting grain sample retained for analysis.
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2.3. Soil and grain analyses Soil samples were air dried and ground to pass through a 2-mm sieve. Soil pH was determined using a glass electrode in a soil:water ratio of 1:2.5. Soil organic matter was determined by loss on ignition based on the method described by Ball (1964). Soil Al, Fe and Mn oxides were extracted using a mixture of ammonium oxalate and oxalic acids (0.114/0.086 M) following the procedure of Janssen et al. (1997), before determination by inductively-coupled plasma atomic emission spectrometry ICP-AES (Fisons ARL Accuris, Ecublens, Switzerland). A portion of each soil sample was finely ground to !150 mm in an agate ball mill. Subsamples of 0.25 g were digested with aqua regia (4:1 v/v concentrated HCleHNO3), following the method of McGrath and Cunliffe (1985). Pb concentrations in the digest solutions were determined by graphite-furnace atomic absorption spectrometry (GF-AAS; Perkin Elmer 4100-ZL, Norwalk, USA). Samples of wheat and barley grain were ground to !0.5 mm using a Reitch ultracentrifugal stainless steel mill, and oven dried at 80 (C before analysis. Subsamples (ca. 1 g) of the dried and ground grain were digested in XP1500plus TeflonÒ PFA microwave liners (CEM Corp, Matthews, NC) using 3 mL of Primar ultra-pure concentrated nitric acid (70% w/v) (Fisher Scientific), 2 mL of Primar 30% w/v hydrogen peroxide (Fisher Scientific) and 7 mL ultra-pure water (18 MU specific resistance; ELGA Maxima, High Wycombe, UK). Digestion was carried out at 115 (C for 1 min and 175 (C for 10 min, both at a maximal pressure of 450 psi, using a CEM model Mars X microwave oven. After completion of the heating process, the vessels were allowed to cool before the contents were quantitatively transferred to 25 mL volumetric flask and made up to 25 mL with ultra-pure water prior to analysis (Adams et al., 2003). Pb concentrations in the digest solutions were determined by GF-AAS. Quality control was ensured by inclusion of the certified reference material BCR CRM191 brown bread and one blank vessel in each batch of samples. All glassware and microwave vessels were acid-washed (5% v/v HNO3) and thoroughly rinsed with de-ionised and ultra-pure water before use.
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water, (2) 0.05 M ethylenediaminetetraacetic acid (EDTA) or (3) 1% (v/v) HNO3. The grain samples were subsequently rinsed with ultra-pure water, before being dried (80 (C for 24 h) and microwave digested (see above). The 10 mL washing solutions (which contained particulate matter washed off the grain samples) were evaporated to approximately 1 mL volume, before being digested using the aqua regia method described above. The grain and washing digest solutions were analysed for Pb by GF-AAS, while marker elements (e.g. titanium) which indicate the presence of soil/dust contamination in plant samples were analysed by ICP-AES. For comparison, 10 additional barley samples with a wide range of cadmium (Cd) concentrations were selected and washed as described above. The effect of washing on grain Cd concentration was determined. 2.5. Statistical analyses Statistical analyses, including multiple linear regression and analysis of variance (ANOVA) were performed using Genstat 5 for Windows (Numerical Algorithms Group, 1998). Where appropriate, variates that showed skewed distributions were log-transformed prior to statistical testing to stabilise variance. For samples having Pb concentrations below the analytical detection limit (!0.02 mg kg1 DW), concentrations equal to half the value of the detection limit were used in the subsequent statistical analyses.
3. Results and discussion 3.1. Quality control Repeated analysis of the certified reference material BCR CRM191 brown bread gave a mean Pb concentration of 0.185 mg kg1 (SD 0.020 mg kg1, n ¼ 28). This mean value was very close to the certified value of 0.187 mg kg1 ( G confidence limit 0.014 mg kg1). The results show that the digestion and analysis procedures used were reproducible and accurate for Pb analysis. The detection limit of the GF-AAS used was 0.8 mg Pb L1 in solution, which was equivalent to a detection limit of 0.020 mg kg1 DW of Pb in grain samples.
2.4. Grain washing experiments 3.2. Cereals quality survey To establish whether high concentrations of Pb measured in some barley grain samples occurred as a result of plant uptake or were due to external factors such as surface contamination prior to analysis, a series of grain washing experiments was performed. Ten samples of barley grain collected in 2000 from Scotland were used in this experiment. Subsamples of whole grain (5 g) were rinsed for 2 min with 10 mL of either (1) ultra-pure
Fig. 1 shows the frequency distributions and boxplots of Pb concentrations in wheat grain samples collected in the 1982 and 1998 CQS, and also in barley grain samples collected in 1998. In 1982, the concentration of Pb in wheat grain ranged from below the detection limit (0.02 mg kg1 DW) to 1.63 mg kg1 DW, with a median of 0.043 mg kg1 DW. Only 1 out of 176
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Fig. 1. Frequency distributions (a) and box-plots of the Pb concentrations (b) in wheat and barley grain from the 1982 and 1998 Cereal Quality Surveys. Samples with Pb concentrations lower than the detection limit (0.02 mg kg1 DW) were assigned a value of 0.02 mg kg1 DW for the construction of frequency distribution and box-plot. The central line within each box is the median, and the bottom and top of each box represent the 25th and 75th percentiles, respectively. The whiskers represent the 10th and 90th percentiles, respectively, and values outside this range are plotted as individual outliers (B).
samples (0.6%) contained higher than the current EU MPC (0.235 mg kg1 DW), and 9 samples (5.1%) had a Pb concentration below the detection limit. In 1998, 13 years after the enforced reduction of Pb added to petrol, there was a clear shift toward lower Pb concentrations in wheat grain. The concentration range measured in 1998 was from below the detection limit to 0.11 mg kg1 DW, with a median of 0.022 mg kg1 DW. None of the 250 samples collected in 1998 exceeded the current EU MPC, and moreover 45% of the samples had Pb concentrations below the detection limit. The difference between the two surveys was highly significant (P ! 0:001) according to ANOVA. The significant decrease in wheat grain Pb from 1982 to 1998 was probably due to the eightfold decrease in the atmospheric emissions of Pb that took place during the same period in the UK (National Atmospheric Emissions Inventory, 2003). Jones and Johnston (1991) showed that the reduction of Pb added to petrol at the beginning of 1986 resulted in a decline in the concentrations of Pb in herbage from long-term experiments at Rothamsted, UK. The median value in our 1982 survey was larger than the median of 0.017 mg Pb kg1 FW in 288 wheat grain samples collected in the early 1980s from uncontaminated sites in the US (Wolnik et al., 1983). By 1998, the median value of Pb in British wheat was similar to the US median. In contrast, Wiersma et al. (1986) found higher concentrations of Pb (0.03e0.65 mg kg1 FW, with a median of 0.14 mg kg1 FW) in 84 wheat grain samples collected in 1976e1977 in The Netherlands. The relatively high concentrations of Pb in Dutch wheat grain samples, compared with the US and British samples, could be due to high atmospheric concentrations of Pb, contamination during sampling and storage, or inaccurate analysis. No information of analytical precision and accuracy was given by Wiersma et al. (1986).
In the 1982 survey, which included the grid reference for the location of each sample, Pb concentrations were mapped (Fig. 2). There was no clear pattern in the geographical distribution of wheat grain Pb. Most of the samples were collected from main cereal growing areas in Britain, i.e. in rural or semi-rural environments. Because the combustion of leaded petrol had been the main source of atmospheric Pb until recently, and the level of atmospheric Pb has a predominant influence on plant Pb concentrations (Chamberlain, 1983; Jones and Johnston, 1991), the short-distance influence of road transport is likely to contribute significantly to the
Pb (mg kg-1 DW) >0.100 0.075 – 0.100 0.050 – 0.075 0.025 – 0.050 <0.025
Fig. 2. Geographical distribution of the Pb concentration in wheat grain from the 1982 Cereal Quality Survey.
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variation of wheat grain Pb. This short-distance influence would not be reflected in the map shown in Fig. 2. Similarly, there were no significant differences between regions in wheat Pb concentrations in the 1998 survey. Significant (P ! 0:05) cultivar differences in mean lead concentrations were observed (data not shown). However, it is difficult to separate true cultivar differences from environmental variation in the surveys conducted. The concentration of Pb in barley grain collected in 1998 ranged from below the detection limit to 0.476 mg kg1 DW, with a median of 0.029 mg kg1 DW (n ¼ 233; Fig. 1). About 30% of the samples were around or below the detection limit for Pb. All except two samples (0.9%) contained a concentration of Pb below the current EU MPC. Analysis of variance showed that there were no significant differences in the concentrations of Pb in barley grain between different regions and between different cultivars. The concentrations of Pb in this survey were similar to those reported in the barley grain samples in Finland, but lower than those reported in barley grains in The Netherlands (Wiersma et al., 1986). The Pb concentrations in barley grain were generally higher than those in wheat grain collected in the same year (1998). A possible explanation for this difference is that barley grain is more exposed to the effects of atmospheric Pb and dust deposition than wheat grain; the latter is enclosed by glumes in floral spikelets.
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DW (Fig. 3). A large proportion of the wheat samples (ca. 50% of the total) contained concentrations of Pb that were below the detection limit. The frequency distribution (Fig. 3) was similar to that for the 1998 CQS data (Fig. 1). None of the wheat grain samples exceeded the EU MPC for Pb, even though, in this series of surveys, some sites with high soil Pb concentrations (up to 783 mg kg1) were sampled. Differences in mean Pb concentrations between cultivars were not significant. Pb concentrations in barley grain collected in the three harvest years (1998e2000; excluding samples from Scotland in 2000, see below) were low, ranging from below the detection limit to 0.131 mg kg1 DW, with a median of 0.030 mg kg1 DW (Fig. 3). No samples exceeded the current EU MPC for Pb. A substantial number of samples (42%) had Pb concentrations lower than the analytical detection limit. In common with the 1998 CQS data, the concentrations of Pb in barley grain were generally higher than those of wheat grain in the paired soil and crop surveys. Grain samples of barley collected from Scotland in the 2000 harvest year (n ¼ 40) appeared to have anomalously high concentrations of Pb, with a range of 0.078e0.309 mg kg1 DW and a median of 0.170 mg kg1 DW (Fig. 3). Ten of the 40 samples exceeded the EU MPC of 0.235 mg kg1 DW. Surface contamination was found to be responsible for the elevated Pb concentrations in this set of samples (see below).
3.3. Paired soil and crop surveys 3.4. Relationship with soil properties One hundred and sixty-two paired soil and wheat grain samples were collected in three harvest years (1998e2000). The concentration of Pb in wheat grain ranged from less than the analytical detection limit to 0.194 mg kg1 DW, with a median of 0.020 mg kg1
In the paired soil and crop surveys, soil properties varied widely (Table 1). For example, the concentration of total Pb in soil ranged from 4.8 to 783 mg kg1, and soil pH from 5.2 to 8.3. Multiple regression was used to
Fig. 3. Frequency distributions (a) and box-plots of the Pb concentrations (b) in wheat and barley grain from the paired soil and crop surveys in 1998e2000. Samples with Pb concentrations lower than the detection limit (0.02 mg kg1 DW) were assigned a value of 0.02 mg kg1 DW for the construction of frequency distribution and box-plot. See Fig. 1 legend for explanation of box-plots. In the case of wheat, the median was at the detection limit.
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Table 1 Summary of soil properties from the paired soil and crop surveys Crop
pH
Organic Al oxides Fe oxides Total Pb matter (%) (g Al kg1) (g Fe kg1) (mg kg1)
Barley Range 5.4e8.3 0.7e12.6 Mean 7.0 3.4 Median 6.9 2.9
0.18e4.6 1.5 1.2
0.40e10.0 4.8e783 3.4 40 3.1 26
Wheat Range 5.2e8.3 0.9e24.6 Mean 7.3 5.6 Median 7.6 4.5
0.40e3.8 1.3 1.1
0.31e17.4 15e772 3.6 56 2.9 32
analyse relationships between grain Pb concentration and soil properties. Despite wide variations in soil properties, none of the soil properties examined, either alone or in combination, could explain the variation of Pb concentration in wheat or barley grain. This is in contrast to Cd, for which soil pH and soil total Cd together explained 53% of the variation in Cd concentrations in wheat grain in the same surveys (Adams et al., 2004). Grain samples collected from the survey sites having elevated soil concentrations of Pb (e.g. O100 mg kg1) did not contain elevated levels of Pb. The results are consistent with the fact that the main entry route of Pb to plants is via atmospheric deposition (Tjell et al., 1979; Chamberlain, 1983; Dalenberg and Vandriel, 1990). Pb generally has a very low solubility in soil, and plants such as wheat and barley do not take up much Pb or transport Pb to grain (Lu¨bben and Sauerbeck, 1991; Hooda et al., 1997). Baumhardt and Welch (1972) studied Pb uptake by corn in a field experiment where 8 rates of lead acetate up to
3200 kg Pb ha1 were applied to the soil. They found that Pb additions to soil increased the concentrations of Pb in leaves and stalks, but did not affect the concentration of Pb in corn grain, again indicating negligible transport of Pb from leaves and stalks to grain.
3.5. Grain washing experiments A brief (2 min) washing with ultra-pure H2O, 0.05 M EDTA or 1% HNO3 reduced the concentrations of Pb substantially in the 10 barley grain samples collected from Scotland in 2000 (Fig. 4a). On average, washing with ultra-pure H2O, 0.05 M EDTA or 1% HNO3 removed 30, 62 and 77% of the Pb from the grain samples, respectively. Analysis of the wash solutions for these samples also showed high concentrations of Pb (data not shown), confirming that substantial amounts of Pb were removed by washing. The results indicate that the main reason for the high Pb concentrations measured in the Scottish barley samples collected in 2000 was surface contamination, rather than true uptake by plants. Titanium (Ti) concentrations were also determined in the wash solutions after digestion. Ti is commonly used as a marker to indicate the presence of soil or dust in crop samples, because it is hardly taken up by crops despite significant concentrations being present in soil. However, there was no indication of elevated Ti levels in the wash solutions, and therefore it is unlikely that the surface contamination of the Scottish barley samples was due to soil. Surface contamination could occur as a result of atmospheric deposition.
Fig. 4. Effects of washing for 2 min with H2O, 0.05 M EDTA or 1% HNO3 on grain Pb concentrations (a) and Cd concentrations (b). For Pb, 10 barley grain samples were selected from the Scottish survey in 2000. For Cd, 10 barley grain samples with high Cd were selected from the whole of the paired soil and crop surveys.
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Although atmospheric deposition undoubtedly contributed to grain Pb, this was unlikely to be the main reason causing the anomalously high concentrations of Pb in the 40 Scottish barley samples collected in 2000. Atmospheric inputs in most arable areas in Scotland are probably lower than those in England, and there is no reason to suspect that atmospheric deposition of Pb in Scotland would be much higher in 2000 than in the two previous seasons. It is likely that surface contamination occurred during harvest, threshing or sample storage prior to analysis. Contamination during sample grinding or analysis can be ruled out, because all samples were ground in the same way using the same stainless steel mill, and analysed together. In contrast to Pb, washing removed little of the grain Cd (Fig. 4b). On average, washing of 10 grain samples for 2 min with H2O, 0.05 M EDTA or 1% HNO3 removed 4.2, 6.7 and 7.7% of the grain Cd. There was good agreement between the concentrations of Cd in the grain samples before and after washing. The results demonstrate that most of the grain Cd was inside the grain, and plant uptake was the main pathway contributing to the high concentrations of Cd measured in the samples. Similar to our findings with cereal grain, Nicholson et al. (1995) showed that washing herbage samples prior to analysis made no difference to their Cd concentrations, indicating little surface contamination with Cd.
4. Conclusions The concentration of Pb was determined in 483 grain samples of wheat and barley from the 1998 Cereals Quality Survey and on 377 paired soil and grain samples collected from the 1998e2000 harvests. In addition, 176 archived wheat grain samples from the 1982 Cereal Quality Survey were also analysed for Pb. The samples were collected from the main cereal growing areas in the UK. The vast majority of samples (O99% for both wheat and barley samples, excluding the Scottish barley samples collected in 2000) were below the newly introduced European Commission limits specifying the maximum permissible concentration of Pb in foodstuffs (Pb in both barley and wheat grain 0.2 mg kg1 fresh weight, equivalent to 0.235 mg kg1 dry weight). There was a significant decrease in wheat grain Pb from 1982 to 1998, reflecting a marked reduction in Pb emissions. However, 40 barley samples collected from Scotland in 2000 in the paired soil and crop survey showed anomalously high concentrations of Pb, with 10 samples exceeding the EU limit. Washing experiments demonstrated that surface contamination, introduced during grain harvest and/or storage, was the main reason for the high concentrations in these samples. In the paired soil and crop surveys, there were no significant
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correlations between grain Pb concentrations and soil properties, such as total Pb concentration, soil pH, organic matter content, and contents of Fe, Al and Mn oxides, singly or in various combinations. The lack of a significant relationship was attributed to the low bioavailability of Pb in soils and limited uptake and transport of Pb to grain in wheat and barley.
Acknowledgements This work was funded by the UK Home-Grown Cereals Authority (HGCA) and the Royal Agricultural Society of England Hills Bequest. Rothamsted Research receives grant-aided support from the UK Biotechnology and Biological Sciences Research Council.
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