Transfer factor of radioactive cesium to forage corn (Zea mays L.) from soil to which contaminated farmyard manure had been applied

Abstract

Radioactive cesium (Cs) deposited after the Fukushima Daiichi Nuclear Power Station accident contaminated farmyard manure (FYM) in the wide area surrounding the plant. We conducted a field trial to determine the transfer factor of radioactive Cs to forage corn (Zea mays L.) from soil to which the contaminated FYM had been applied. The main purpose of this experiment was to examine the behavior of the radioactive Cs from contaminated FYM that was incorporated in agricultural fields. Application of FYM containing 3900 Bq kg⁻¹ dry matter (DM) of cesium-137 (¹³⁷Cs) at a rate of 4.3 kg m⁻² increased the ¹³⁷Cs concentration in the soil by 64 Bq kg⁻¹ dry soil, and in the forage corn by 9.2 Bq kg⁻¹ DM. Therefore, we calculated the transfer factor to corn plants from the soil after application of contaminated FYM to be 0.14. This value is lower than that observed for soil to which uncontaminated FYM had been applied as a control, and it is within the range of reported soil-to-plant transfer factors of 0.003–0.49 listed in the recent parameter handbook by International Atomic Energy Agency. The increase in the radioactive Cs concentration in the corn plants, expressed as the sum of ¹³⁷Cs and cesium-134 (¹³⁴Cs), was only 3% of the 2012 provisional tolerance level for cattle roughage in Japan. Even though the application of contaminated FYM did not cause a large change in the radioactive Cs concentration in the corn plants in this trial, such application should be carefully controlled because it increased radioactive Cs concentrations in both soil and forage corn.

Key words:

• Radioactive cesium
• farmyard manure
• forage crop
• transfer

INTRODUCTION

It is very important to reduce the radioactive cesium (Cs) concentration in forage crops in the area around the Fukushima Daiichi Nuclear Power Station due to the deposition of radioactive Cs after the tsunami-caused accident in March 2011. To prevent or minimize contamination of animal products with radioactive Cs, in 2012, the Ministry of Agriculture, Forestry and Fisheries of Japan (MAFF) set a provisional tolerance level for cattle roughage of 100 Bq kg⁻¹, with a water content correction of 80% (MAFF 2012). This regulation applies to forage and animal production systems in Japan. There are various types of roughage produced in Japan, such as hay, silage, and green forage, each with a different water content. Those account for 77% of the total roughage consumption by dairy and beef cattle in Japan, whereas 88% of the concentrated feed consumed is imported (MAFF 2013a).

Because a large amount of the concentrated feed used in Japan is imported, cattle farmyard manure (FYM) is a major nutrient resource for forage crop production in Japan. Thus, understanding the effect of FYM application to the soil on radioactive Cs uptake by forage crops is important for developing countermeasures to control radioactive Cs contamination in the forage production system. In general, application of organic materials such as FYM and compost to fields reduces the radioactive Cs concentration in crops grown in those fields (Nishita et al. 1973; Tsumura et al. 1984; Lembrechts 1993). Applied organic materials can supply beneficial minerals for plant growth and increase the cation content of the soil, thus reducing the transfer of radioactive Cs from the soil to crops. After the Chernobyl accident, potassium (K) application was one of the most effective countermeasures for controlling the radioactive Cs concentration of crops under field conditions (Alexakhin 1993; Nisbet et al. 1993; Shaw 1993; Smolders et al. 1997; Zhu and Smolders 2000). Successive FYM applications thus effectively reduces radioactive Cs concentrations in forage corn (Zea mays L.) by increasing the soil exchangeable K level (Harada et al. 2012). Therefore, the application of uncontaminated cattle FYM can be recommended for farmers to reduce radioactive Cs transfer from contaminated soils.

However, in the area surrounding the Fukushima power station, FYM became contaminated by radioactive Cs after the accident (MAFF 2013b). This contamination occurred when a part of the highly contaminated roughage harvested in 2011 was composted or fed to calves and breeding cows. At that time, the provisional tolerance level was 3000 Bq kg⁻¹ for roughage to be fed to these animals. Quantitative data on the transfer of radioactive Cs from contaminated FYM to crops is very important for deciding how the contaminated FYM should be treated, but few reports have evaluated the transfer of radioactive Cs to crops after application of contaminated organic materials.

In this study, we examined the radioactive Cs concentration in forage corn after application of contaminated FYM under field conditions and measured the transfer factor of radioactive Cs from the soil containing contaminated FYM to forage corn. We expect that these data will contribute information necessary for the field reduction of contaminated FYM from cattle.

MATERIALS AND METHODS

Site description

In 2012, we carried out a field study at the National Agriculture and Food Research Organization (NARO) Institute of Livestock and Grassland Science (NILGS), Nasu campus, Japan (latitude 36°55’N, longitude 139°55’E), to estimate the transfer factor of radioactive Cs from contaminated cattle FYM to forage corn. Kurashima et al. (1993) classified the soil of the field used for this experiment as a loamy over fragmental, mixed, mesic Entic Haplumbrept (Soil Survey Staff 1999). The soil contains volcanic ash. Before 2012, the field was a meadow that had not been used for grazing for more than 5 years. The average monthly air temperature measured at NILGS was 18.6, 23.6, 25.7 and 22.5°C from June to September 2012, respectively. During these 4 months, 717 mm of precipitation was recorded.

FYM preparation

The contaminated FYM was prepared at NILGS from contaminated cattle excrement and sawdust by August 2011. The excrement was derived from contaminated grasses fed to cattle in spring 2011. The contaminated sawdust, with as much as thousands of Bq kg⁻¹, was not found in this area. The FYM was produced by an automated composting facility with forced aeration, followed by drying utilizing a rotary agitator. The water content of the produced FYM was low, so it was mixed with fresh FYM to adjust the moisture content and to promote composting. The FYM was piled and stocked until use.

Field preparation and corn cultivation

Before corn cultivation, the topsoil (0–10 cm) of the meadow was removed with an excavator to reduce the soil radioactive Cs concentration, thus minimizing interference from pre-existing contamination due to the Fukushima power station accident. After the topsoil removal, soil samples were collected for measurement of variations in the radioactive Cs and nutrient concentrations in the field. The phosphorus (P) level and pH were then adjusted by applying superphosphate, fused phosphate, and lime at the rates of 20 g P₂O₅ m⁻², 15 g P₂O₅ m⁻² and 192 g CaO m⁻², respectively. Contaminated FYM was applied at to a plot with a cultivated area of 13.1 m² at the rate of 4.3 dry matter (DM) m⁻² and uncontaminated FYM as a control was applied at the rate of 4.4 kg DM m⁻². Two repetitions of each treatment were performed, following a randomized design. Then, the fertilized soil was carefully plowed by using a rotary tiller and packed under the treads of a tractor. The field work before sowing seed was conducted on May 31, 2012. On June 11, seeds of forage corn (Zea mays L. cv KD771new) were sown 0.2 m apart in rows spaced 0.6 m apart. Then, ammonium sulfate was applied at a rate of 15 g N m⁻² to the soil surface immediately and the slow release nitrogen fertilizer MEISTER-8 (JCAM AGRI. CO., LTD.) was simultaneously applied at a rate of 10 g N m⁻². The herbicide treatment for forage corn was also conducted using alachlor and atrazine.

The corn plants were harvested on September 11, 2012 by cutting the plants at 10 cm above ground level. Two samples of 10 plants each were collected and weighed from each plot for analysis. The sampled plants were cut into pieces 2–3 cm long, and then the pieces were mixed well. A part of the mixed material of each sample was dried at 90°C for 3 d in a paper bag and water content was measured. The dried plant material was powdered using a Willey mill with a 2-mm screen. A bulk soil sample of about 8 kg was collected from 0 to 20 cm depth from the middle of each plant sampling plot on September 24.

Chemical analysis of soil and FYM

Before analysis, soil samples were air-dried and sieved through a 2-mm mesh. Soil pH was measured in water (1:2.5) using a glass electrode. Available P was extracted by the method of Truog (1930), and the P content as P₂O₅ was determined using an Auto-Analyzer system (QuAAtro, BLTEC, Osaka, Japan). Cation exchange capacity (CEC) was determined using the method of Schollenberger and Simon (1945). Exchangeable cations extracted by a 1 mol L⁻¹ ammonium acetate solution were measured using atomic absorption spectrometry (SpectroAA 220, Varian Japan, Tokyo).

FYM samples were air-dried and then milled into fine powder by using a vibrating sample mill. Mineral contents of FYM samples were analyzed by atomic absorption spectroscopy after wet digestion with nitric acid. The digested solution was also used for P analysis. Total carbon (C) and nitrogen (N) contents were determined by the dry combustion method using a CN analyzer (JM1000CN; J-Science, Kyoto, Japan).

Exchangeable ¹³⁴Cs and ¹³⁷Cs in the soil and FYM were extracted by using a 20-fold volume of 1 mol L⁻¹ ammonium acetate solution (pH 7.0) with shaking for 1 h at room temperature, followed by filtration though No. 5C filter paper (ADVANTEC, Tokyo). Water-soluble ¹³⁴Cs and ¹³⁷Cs were extracted from FYM by using a 10-fold volume of water with shaking for 1 h at room temperature. The extract was centrifuged at 12,000 g for 20 min, and then the supernatant was filtered through a membrane filter (0.45 µm pore size, nitrocellulose) and analyzed by gamma spectrometry.

¹³⁴Cs and ¹³⁷Cs measurement and calculation of the transfer factor

All plant and soil samples were analyzed for cesium-134(¹³⁴Cs) and cesium-137 (¹³⁷Cs) using high resolution gamma spectrometry with a germanium detector (GEM20P4-70; resolution 1.8 keV at 1.33 MeV, relative efficiency 20%; ORTEC, Oak Ridge, TN, USA) and a multi-channel analyzer (MCA7600, SEIKO EG&G, Tokyo, Japan). The radioactive Cs concentrations were shown on a DM basis for simplicity. Counting time was 50,000 s for each powdered plant sample of about 1 kg packed in a 2-L Marinelli vessel, and 2000 s for about 70 g of soil or FYM sample packed in a 100-mL vessel. If the measurement result of a sample was the same level as a detection limit, the soil was re-analyzed for 50,000 s in a 700-mL vessel. The extract solution of soil with 1 mol L⁻¹ ammonium acetate was analyzed for 10,000 s in a 2-L vessel. Average detection limits for both ¹³⁴Cs and ¹³⁷Cs were about 2, 12 and 0.1 Bq kg⁻¹ for powdered plant material, soil and extract solution samples, respectively. By adjusting sample volume and measurement time, every measurement result was above the detection level. The correction date used to account for radioactive decay of the soil and plant radioactive Cs concentrations was October 1, 2012. We calculated the transfer factor (TF) as follows:

(1)

We calculated TF due to the use of contaminated FYM by subtracting the average corn or soil concentration of the uncontaminated FYM plots from that of the contaminated FYM plots:

(2)

Statistical analysis

Differences in mean values were assessed by using two-way analysis of variance (ANOVA) and the Tukey-Kramer test. The R 2.11.1 statistical software package (R Development Core Team 2010) was used for the analysis.

RESULTS AND DISCUSSION

Chemical composition of FYM

The chemical compositions of the contaminated and uncontaminated FYM are shown in Table 1. The K concentration of both types of FYM was considerably higher than the average concentration for composted cattle manure of 24 g kg⁻¹ (n = 318) reported by Yamaguchi et al. (2000). The K concentration of the contaminated FYM was high because of the recycling use of FYM for promoting composting. We selected uncontaminated FYM from outside of NILGS with a K concentration per kilogram DM similar to that of the contaminated FYM.

Table 1 Chemical composition of uncontaminated and contaminated cattle farmyard manure (FYM) applied to soil for the cultivation of forage corn (Zea mays L.)

					Minerals (g kg^−1DM)				Radioactive Cs (Bq kg^−1 DM)
FYM	Dry matter (DM)(g kg^−1)	Total carbon (C)(g kg^−1DM)	Total nitrogen (N)(g kg^−1DM)	C/N ratio	P2O5	CaO	MgO	K2O	^134Cs	^137Cs
Uncontaminated	444	417	16.8	24.8	15.6	24.0	8.3	44.3	25	46
Contaminated	613	405	21.4	18.9	15.4	30.9	9.3	48.4	2510	3900

MAFF has regulated the use of contaminated FYM by setting a provisional tolerance level for radioactive Cs in manure of 400 Bq kg⁻¹ on a fresh matter (FM) basis (MAFF 2011), where the radioactive Cs concentration is the sum of the ¹³⁴Cs and ¹³⁷Cs concentrations. In this study, we calculated the radioactive Cs concentration of contaminated FYM to be 3800 Bq kg⁻¹ FM using the data in Table 1. This concentration is within the range of the radioactive Cs concentrations of FYM prepared in 2011 by farmers in the surrounding area of the Fukushima power station (MAFF 2013b). For example, in Tochigi Prefecture, where NILGS is located, the radioactive Cs concentration of 47% of FYM samples collected in October 2011 exceeded 1000 Bq kg⁻¹.

Saito et al. (2012) reported that most radioactive Cs in cattle manure cannot be extracted with water but is likely to be adsorbed onto the manure. In this study, the water-soluble fraction of radioactive Cs in contaminated FYM, relative to total radioactive Cs, was about 30%.

Application rate of FYM and crop yield

The standard FYM application levels for forage corn cultivation, recommended by prefectural governments around Fukushima Prefecture, are about 3 kg FM m⁻². In this field trial, we set the FYM application amount to about 2 (contaminated treatment) or 3 times (uncontaminated treatment) the standard level to obtain a clear radioactive Cs transfer result (Table 2). The application rates of DM and potassium oxide (K₂O) were similar between the treatments.

Table 2 Application rates of dry matter, nutrients, and radioactive Cs in the contaminated and uncontaminated cattle farmyard manure (FYM)

					Radioactive Cs (Bq m^−2)
Experimental plot	Fresh matter(kg m^−2)	Dry matter (kg m^−2)	K2O(g m^−2)	NH4-N(g m^−2)	^134Cs	^137Cs
Uncontaminated FYM	9.9	4.4	195	2.5	110	200
Contaminated FYM	7.0	4.3	208	0.3	10,800	16,800

The amounts of ¹³⁴Cs and ¹³⁷Cs applied to the uncontaminated treatment plots were negligible, as the concentrations in the uncontaminated FYM were much smaller than those in the contaminated FYM (Table 2). Further, by assuming a soil bulk density of 0.93 and a plowing depth of 20 cm, we estimated that the ¹³⁷Cs concentration of the soil in the uncontaminated plots would increase by only about 1 Bq kg⁻¹ dry soil. The application rate of K₂O, about 200 g m⁻², was much larger than the standard application level for corn. This high K₂O application rate might be expected to reduce the amount of radioactive Cs transferred from the soil to the corn plants despite the low exchangeable K₂O level (0.08 g kg⁻¹; Table 3) of the plots before the FYM application.

Table 3 Chemical properties of soil in the uncontaminated and contaminated FYM plots after cultivation

Chemical properties	Experimental plot		Before FYM and fertilizer application
	uncontaminated FYM	contaminated FYM
pH (H2O)	6.1 ± 0.1	6.1 ± 0.3	5.7
Available P2O5 (g kg^−1)	0.10 ± 0.05	0.08 ± 0.03	0.02
Exchangeable K2O (g kg^−1)	0.39 ± 0.10	0.45 ± 0.06	0.08
Exchangeable CaO (g kg^−1)	1.19 ± 0.18	1.32 ± 0.20	0.54
Exchangeable MgO (g kg^−1)	0.38 ± 0.09	0.38 ± 0.06	0.09
CEC (cmolc kg^−1)	15.6 ± 1.7	16.1 ± 2.4	15.1
^134Cs (Bq kg^−1)	11 a ± 2	50 b ± 12	16
^137Cs (Bq kg^−1)	21 a ± 4	85 b ± 21	31

Different lowercase letters indicate significant differences (P < 0.05; two-way analysis of variance). Data are presented as average ± standard deviation. Data before FYM and fertilizer application are the average of the two treatment areas, and the soil samples were collected at 0–10 cm depth (versus 0–20 cm depth after FYM application).

The average and standard deviation of DM yield of corn in the uncontaminated FYM plots were 1.46 and 0.25 kg m⁻², and those in the contaminated FYM plots were 1.59 and 0.24 kg m⁻². These yield values are within the standard level for this region, and there was no statistical difference in the yield between the treatments.

Soil chemical properties after corn cultivation

The application of FYM and fertilizers greatly improved the soil chemical fertility, as indicated by the exchangeable cation and available P contents (Table 3). Notably, the average exchangeable K₂O content increased from 0.08 to more than 0.39 g kg⁻¹. Unfortunately, we could not statistically compare the results obtained after FYM application with those obtained before FYM application because the soil samples were collected from different depths before plotting.

Except for the radioactive Cs concentrations, the chemical properties of the soil sampled after corn cultivation did not differ significantly between the FYM treatments. The exchangeable K₂O content was adequate for corn cultivation, according to the soil diagnostic criteria of 0.3–0.5 g kg⁻¹ for fertilizer management in this region (National Grassland Research Institute 1988).

The application of contaminated FYM clearly increased the ¹³⁴Cs and ¹³⁷Cs concentrations in the soil by 39 and 64 Bq kg⁻¹ (Table 3). However, the increased concentrations were only 68 and 72% of the values for ¹³⁴Cs and ¹³⁷Cs, respectively, calculated using the application rate of radioactive Cs (Table 2) and the sampling depth, and by assuming a soil bulk density of 0.93. The values for ¹³⁴Cs were calculated by the following equation:

(3)

In general, not all of the FYM that is applied to the soil surface becomes incorporated into the soil by rotary tillage, and some portion would have been washed away by precipitation, because the field had a gentle slope to allow for surface water drainage. However, we could not fully clarify the discrepancy between the measurement results and the theoretical calculation results.

Transfer factor of radioactive Cs to corn from soil to which contaminated FYM was applied

The ¹³⁴Cs concentration of forage corn was increased by 5.8 Bq kg⁻¹ DM, and the ¹³⁷Cs concentration was increased by 9.2 Bq kg⁻¹ DM, by the application of contaminated FYM (Fig. 1). Thus, to prevent increases in crop radioactive Cs concentrations, the application of highly contaminated FYM should be avoided. However, impacts of contaminated FYM application on radioactive Cs concentration in a crop depend on not only the contamination level in FYM but also on other factors, such as soil radioactive Cs and exchangeable K₂O contents. Contaminated FYM application would not necessarily increase the radioactive Cs concentration of a crop. For example, if the radioactive Cs concentration in field soil is much larger than the increased concentration by contaminated FYM application, the application effect would be masked or weakened by soil radioactive Cs. Further, Harada et al. (2012) showed that Cs transfer to forage corn cultivated in a contaminated field to which FYM had been applied depended on the exchangeable K₂O content of the soil. Therefore, the change in the concentration of radioactive Cs in corn depends on the soil K₂O level, which is increased by the application of FYM containing K₂O. This “potassium effect” can thus cause the radioactive Cs concentration of the corn to be reduced, even when contaminated FYM is applied to the contaminated soil. In this study, increased radioactive Cs was observed since the soil radioactive Cs concentration was decreased by the topsoil removal and the soil exchangeable K₂O contents was a similar level for both FYM plots.

Figure 1 ¹³⁴Cs and ¹³⁷Cs concentrations (left) and transfer factors (right) of forage corn (Zea mays L.) cultivated in contaminated and uncontaminated farmyard manure (FYM) treatment plots. Different lowercase or uppercase letters comparing with only lowercase or uppercase indicate significant differences (P < 0.01; two-way analysis of variance). The whiskers above the bars indicate standard deviations. We found no significant interaction between FYM application and repetition. Transfer factors (TF) were calculated as follows:

TF = [Cs concentration in forage corn (Bq kg⁻¹ dry matter (DM))]/[Cs concentration in soil (Bq kg⁻¹ dry soil)].TF deduced for contaminated FYM = [corn Cs concentration by subtracting uncontaminated FYM plot from contaminated FYM plot (Bq kg⁻¹ DM)] /[soil Cs concentration by subtracting uncontaminated FYM plot from contaminated FYM plot (Bq kg⁻¹ dry soil)].

Soil-to-plant TFs of ¹³⁴Cs and ¹³⁷Cs in the uncontaminated FYM plots were statistically larger than those in the contaminated FYM plots (Fig. 1). On the other hand, the ratio of exchangeable radioactive Cs to total radioactive Cs in soil was increased by the application of contaminated FYM (Fig. 2), because a large part of applied radioactive Cs with FYM was extractable by 1 M ammonium acetate. The analytical results for exchangeable ¹³⁴Cs in samples from uncontaminated plots were under the detection limit, so only the ¹³⁷Cs results were shown as the ratio of extractable ¹³⁷Cs to soil or FYM ¹³⁷Cs. The radioactive Cs in the contaminated FYM plots should be readily available to the corn. Thus, the soil exchangeable Cs ratio seems to be inconsistent with the TF results. We also analyzed the ammonium-N content of the FYM, because it has been suggested that ammonium-N stimulates soil-to-plant Cs transfer (Lembrechts 1993), and the Cs ion concentration in the soil solution has been found to depend in part on the ammonium (NH₄⁺) content (Takeda et al. 2008). However, because the amount of ammonium-N was less than one-tenth the amount of N applied in the fertilizer, we considered the effect of ammonium-N in the FYM to be negligible (Table 2).

Figure 2 Extraction ratio of ¹³⁷Cs to total ¹³⁷Cs in farmyard manure (FYM) and in soil before and after contaminated FYM application by 1 M ammonium acetate. Different letters indicate significant differences (P < 0.01; Tukey-Kramer test). The whiskers above the bars indicate standard deviations.

We calculated the apparent TF caused by application of contaminated FYM from the increases in the soil and corn concentrations of radioactive Cs, obtained by subtraction of the concentrations in the uncontaminated FYM plots from those in the contaminated FYM plots. The apparent TF was 0.15 for ¹³⁴Cs and 0.14 for ¹³⁷Cs (Fig. 1). These values are higher than the geometric mean TF of 0.073 collected and listed by Sanzharova et al. (2009). However, the TF depends greatly on soil and cultivation conditions, and Sanzharova et al. (2009) describes TFs ranging from 0.003 to 0.49. The observed values in this study are thus within this range.

Before the provisional tolerance level for FYM was set by MAFF in 2011, no data for TFs from contaminated FYM to crops was available. If FYM containing 400 Bq kg⁻¹ of radioactive Cs is applied at a rate of 5 kg m⁻², the soil ¹³⁷Cs concentration in 0–20 cm depth will increase by 10 Bq kg⁻¹, assuming a soil bulk density of 1. According to this application scenario and using the apparent TF by subtracted calculation for FYM, the ¹³⁷Cs concentration of forage corn should increase by 1.5 Bq kg⁻¹ DM. Therefore, the application of FYM contaminated with less than 400 Bq kg⁻¹ of radioactive Cs should not cause a large change in the radioactive Cs concentration of this forage crop.

It is useful to compare the radioactive Cs transfer from contaminated FYM to crops with transfer factors to crops from soils to which contaminated other organic material have been applied. In another experiment, we found that the incorporation of contaminated grass silage into contaminated soil did not affect the radioactive Cs concentration in forage corn (Amaha et al. 2012). Taken together, the results of these experiments suggest that the effect of contaminated FYM application to soil on the radioactive Cs concentration in forage corn depends only on the increase in the Cs concentration of the soil, even though the radioactive Cs in FYM is more soluble than that in soil. The soluble Cs in the FYM is adsorbed onto the soil clay minerals and FYM supplies potassium to soil, thus negating the effect of the greater solubility of Cs in FYM. Certain clay minerals in soils strongly adsorb Cs, thus reducing the transfer of radioactive Cs from contaminated organic materials to crops.

The information reported in this study will be useful to farmers who need to safely dispose of contaminated FYM in their fields, though further field trials are required to confirm safe application levels of contaminated FYM.

ACKNOWLEDGMENTS

We thank Ms. H. Kohyama for her helpful technical assistance.