The transfer of l!7 Cs through the soil-plant-sheep food chain in different pasture ecosystems

A grazing experiment with sheep was carried out in 1990-1993 on natural, semi-natural and cultivated pasture on clay soil. The pastures were located in Southern Finland and were moderately contaminated with l37 Cs by Chernobyl fallout. Natural pasture refers to forest pasture and serai-natural pasture to set-aside field pasture, the latter having been under cultivation about 15 years ago. The transfer of l37 Cs to sheep was clearly higher from forest pasture than from the other two pastures and it was lowest from cultivated pasture. The transfer was higher to muscle and kidney than to liver and heart. The transfer of l37 Cs to plants and to meat varied with years. Seasonal variation in the plant l37 Cs was followed-up on forest and set-aside field pasture; the activity concentration of plants reached a maximum in June, a lesser increase occurred later in the autumn. In 1993, which was considered an average year with respect to l37 Cs transfer to plants, the mean soil-plant transfer factors of l37 Cs for forest, set-aside field and cultivated pastures were 1.78, 0.36 and 0.09, and soil-meat aggregated transfer factors 11.0, 0.28 and 0,03, respectively.

tivated pasture ntroduction The l37 Cs activity concentration in sheep grazing on natural or semi-natural ecosystems has been elevated since the Chernobyl reactor accident in 1986, and it has decreased more slowly than predicted (Mayes 1988, Salt et al. 1992. Sheep farmers in Great Britain, Norway and Sweden have had problems with the high activity level of radiocesium found in sheep grazing on natural grasslands (Mayes 1988, Hove et al. 1994. It is known that natural or semi-natural pastures of poor vegetation facilitate the longterm transfer ofradiocesium from soil via vegetation to sheep (Coughtrey et al. 1989, Howard et al. 1990,Livens et al. 1991). In Finland, sheep are mainly grazed on cultivat-ed pastures in southern areas, where Cs-fixing clay soils dominate. Both the cultivated pasture with high soil K status and the soil clay fraction are considered to contribute to the low transfer of radiocesium to plants. However, interest in the restoration of natural and ecological values in the countryside and, consequently, grazing on natural and semi-natural ecosystems have grown in recent years. Further, the importance of sheep husbandry has increased in eastern and northern parts of the country and especially in areas too sparse for cultivation. The aim of this study was to get more information about the problem of sheep grazing on natural and semi-natural pastures compared to cultivated pastures in case of a severe nuclear fallout.

Material and methods
Grasslands Natural, semi-natural and cultivated pastures were situated on heavy clay soil in Southern Finland in Jokioinen (60.9°N, 23.5°E) belonging to the Chernobyl fallout category 3 with an estimated surface activity of l37 Cs of 11-23 kßq nr 2 in 1987 (Arvela et al. 1987). The area of natural and semi-natural pasture was about 2 hectares. Half of it was forest pasture (natural pasture) with  1990 1991 1992 1993 1994 1990 1991 1992 1993 1994 1990 1991 1992 1993 1994   The cultivated pasture used in 1990 had not been ploughed after the Chernobyl accident and was partly on Carex peat soil and partly on clay soil. Since 1991, the cultivated pasture was moved to a nearby pasture on clay soil ploughed at least twice after the deposition. The pastures were fertilized normally (125 kg N, 50kg K and 25 kg P ha -1 ) during the growing season.
Soil to plant transfer of 137 Cs was studied also on cultivated ley and on two semi-natural meadows in 1990-1992. The ley on Carex peat soil was located near the cultivated pastures in Jokioinen and had been tilled once after the deposition and fertilized and harvested yearly. The two meadows were located in Pälkäne (61.3°N, 24.2°E) on fine sand soil. They had not been fertilized for 10-15 years but had been harvested yearly. The area belonged to the 137 Cs fallout category 4 (23-45 kßq nr 2 ). During the experiment, no agricultural practices were done on the ley and meadows. Meadow-1 was ploughed in 1991 and the sampling site was moved in 1992 to the nearby similar meadow established after the Chernobyl fallout. The same grass species dominated on ley as on cultivated pasture (Table 1). Only few species grew on meadow-1, while on meadow-2 several species were found.

Animals
Five pure-bred and five cross-bred Finnsheep ewe lambs grazed on the combined forest and set-aside field pasture in 1990-1992 and on cultivated pasture in 1990.Ten ram lambs were kept on the cultivated pasture in 1991-1992 (Table 3). In 1993, after dividing the combined pasture into two parts, six Finnsheep ewe lambs (four purebred and two cross-bred) grazed on forest pasture, six ewe lambs on set-aside pasture and 12 ram lambs on cultivated pasture. The lambs were supplemented with barley grain, 0.3 kg per head per day during the first ten grazing days. No other supplemental feeds except salt and minerals were given.

Soil and plant sampling
For studying soil to plant transfer of 137 Cs four random squares of 0.25 m 2 each were taken. The vegetation was cut at the height of 2 cm. Thereafter four soil samples were taken from each of the squares with the aid of a soil cylinder 10cm high and 5 cm in diameter. Samples were collected in the beginning of September. For studying the vertical distribution of l37 Cs in the soil cores, three of the four soil samples were divided horizontally into seven fractions in 1990; during the subsequent years the soil samples were divided into two fractions (0-5 and 5-10 cm). The fourth sample of a square was kept intact (0-10 cm). In addition, soil samples of unploughed (1990) and ploughed meadow (1992) were taken with a soil cylinder of 18 x 5 cm and divided into seven fractions. For studying the seasonal variation of l37 Cs in pasture vegetation four random squares were taken in 1992-1994. For studying the 137 Cs level of certain plant species of forest and set-aside field pastures single species were collected at different sites of pastures in July and combined for 137 Cs measurement. Moss and lichen samples were taken from forest pasture in 1994.
Sample analysis and measurement of activity Soil samples were air-dried, ground and passed through a 2-mm sieve. Soil potassium, calcium and magnesium were extracted with acid ammonium acetate (AAc, pH 4.65), pH was determined in soil-water suspension, organic carbon by dry combustion, clay fraction by dry and wet sieving and by the pipette method (Table 4) (MTT 1986). Plant samples were dried at 60°C and milled. The plant activity concentration of 40 K was used instead of K. (The amount of 40 K in the natural potassium is constant.) Samples of the neck muscle, heart, liver and kidney of the sheep were taken the day after slaughter. Visible fat was removed from the meat samples. Activity measurements were performed using a low-background semiconductor spectrometer with a high purity germanium detector placed in a 13 cm lead background shield. The gamma spectra were analyzed with a computer pro-gramme. The l37 Cs activity concentrations were decay-corrected to 1990. The plant and soil activity concentrations are presented in dry matter (DM) and that of meat in fresh weight (FW).

Calculation of l37 Cs transfer and concentration factors
Transfer factors (TF), aggregated transfer factors (T ) and concentration factors (CF) of l37 Cs were calculated as follows: TF and T f values for grasslands ploughed after the fallout might be too high due to the soil sampling depth of 10 cm. In this case, CF values are more reliable provided that l37 Cs was distributed rather evenly in the plough layer.

Statistical methods
The effect of year and pasture type on the 137 Cs activity concentration of plants was investigated by using the standard two-way analysis of variance. Differences between years were tested by means of trend contrasts. The effect of year on the l37 Cs activity concentration of tissues was investigated using the analysis on a univariate repeated measures model similar to the split-plot model (Crowder and Hand 1990) where year was the between subject factor and tissue type was the within subject factor. Differences between muscle and other tissues were tested by contrasts. All the 137 Cs activity concentrations were log-transformed. The data were analyzed with the SAS MIXED procedure.

Soil l37 Cs
In 1990, the 0-2 cm soil layer of forest pasture and other unploughed grasslands contained 80-90% of l37 Cs and that of tilled ley about 50% ( Fig. 1 a,b). In unploughed meadow, over 90% and in ploughed meadow, about 35% of 137 Cs was found in the soil layer of 0-3 cm ( Fig. 1 c,d). The distribution of l37 Cs in the undisturbed pasture soils between the layers of 0-5 and 5-10 cm (Table 5) remained rather constant during the experimental years. The l34 Cs/ l37 Cs ratio of pasture soils, decay-corrected to 1986, was 0.5.

Activity concentration
The l37 Cs activity concentration of plants on forest pasture was clearly higher than that on the other pastures, and it fluctuated with years. The plant 137 Cs of set-aside field pasture was significantly higher than that ofcultivated pasture, and the activity levels differed between years. When investigating the trend of the plant l37 Cs for the two pastures over years using orthogonal polynomials the quadratic polynomial proved to be the best approximation to this trend (Table 6). On forest pasture there were differences in the 137 Cs concentration between plant species (Table 7). There was no correlation between the plant 137 Cs and 40 K (Fig. 2). Lichens had much higher and mosses mostly higher 137 Cs concentrations than vascular plants. The average 137 Cs activity concentration was 180 in the mosses Aulacomnium palustre and Climacium dendroides, 370 in Hylocomium splendens and Polytrichum spp., 610 in Pleurozium Schreberi, 750 in Sphagnum spp. and 4880 Bq kg" 1 in Grimmia spp. In the lichen genera Cladonia and Stereocaulon the activity concentration was 490 and 5360 Bq kg' 1 , respectively, and in the mushroom Lactarius torminosus 2240 Bq kg" 1 . Sheep were not found to feed on mosses and lichens.

Transferfactor
The behaviour of the soil-plant transfer factors of 137 Cs resembled in general those of the plant concentration of 137 Cs in regard to pasture type and year (Table 8). The transfer factor of 137 Cs for cultivated ley was rather low compared to that for meadows. The soil-plant transfer factor for semi-natural meadows on finesand soil was higher than that for semi-natural (set-aside field) pasture on clay soil. For meadow-1 the transfer factor was higher and soil K lower than those for meadow-2.

Seasonal variation
The l37 Cs activity level of vegetation on forest and set-aside field pasture fluctuated during the growing season. The highest activity concentration was found at the time of vigorous growth in the early summer followed by a decrease in the middle of the summer and a slight increase in the autumn (Fig. 3). The second increase in growth was relatively more prominent on setaside field pasture. Potassium 40 in vegetation decreased during the growing season on both pastures from about 800 to 320 Bq kg -1 and plant dry weight (%) on forest pasture increased from 25 to 50% and on set-aside pasture from 30 to 43% (1993). Table 7. Activity concentration of l37 Cs of some plant species or genera of forest pasture (f) and set-aside field pasture (s). Each sample is a mixture of several subsamples. When the l37 Cs activity concentration of tissues of sheep on combined pasture in 1991-1992 was tested by the analysis of variance, the effects of year, tissue type and their interaction were highly significant (p < 0.001). Practically, the 137 Cs activity level between muscle and kidney and between liver and heart was of the same order of magnitude (Table 9). The mean and standard deviation (in parentheses) of l37 Cs activity concentration of muscle, kidney, liver and heart of 6 sheep grazing on forest pasture in 1993 was 254 (70), 185 (57), 134 (35) and 126 (47) Bq kg -1 and on set-aside field pasture 4.0 (0.9), 2.7 (1.4), 1.3 (1.1) and 1.9 (0.8) Bq kg -1 , respectively.

Transfer and concentration factors
The soil-meat aggregated transfer factor of l37 Cs for combined and cultivated pasture fluctuated by year and was clearly highest in 1991 (Table 10). The differences between forest, setaside field and cultivated pasture were obvious (Table 11). The meat/plant concentration factor was not calculated for combined pasture in 1990-1992 due to considerable differences in the plant concentration of 137 Cs of the two sampling sites. After dividing the pasture in 1993, the mean and the standard deviation (in parentheses) of the meat/plant concentration factor of l37 Cs for for-  (1991,1994) and moss species (1994) on forest pasture. Each sample is a mixture of several subsamples.

Soil distribution
The very slow vertical migration of the l37 Cs in the undisturbed soil profiles found in this study has been confirmed by several authors. Rogowski and Tamura (1970) found in their 2year study that most of the 137 Cs which was not eroded remained in the 0-3 cm soil layer. According to Fawaris and Johanson (1994), 5 years after the Chernobyl accident about 85% of the 137 Cs was found in the 0-5 cm humus layer of forest soil. Similar low cesium transfer has been reported by Colgan et al. (1990) and Livens et al. (1991).

Pastures and sheep
The soil-plant-meat transfer of l37 Cs of the Swedish mountain pasture was much higher than that of forest pasture in this study, although these areas had been nearly equally affected by fallout (Hove et al. 1994). The sandy and peaty soils of mountain pasture had lower concentrations of soluble potassium and calcium, lower pH and higher organic matter contents than the clay soil Table 10. Soil-meat aggregated transfer factors and concentration factors of l37 Cs for combined (forest and set-aside field) and cultivated pasture by years.  586 AGRICULTURAL AND FOOD SCIENCE IN FINLAND Vol. 5 (1996): 577-591. of forest pasture. Acid, coarse-textured soils with poor nutrient status and high humus content are known to increase the 137 Cs activity concentration ofherbage and grazing sheep, while l37 Cs is fixed in the soil unavailable for plant uptake by the clay fraction (Kiihn et al. 1984, Frissel et al. 1990, Rosén 1991, van Bergeijk et al. 1992, Thiry and Myttenaere 1993. The variation of the soil-plant and soil-meat transfer factors of 137 Cs followed by and large that of plant and meat activity concentrations. The meat/plant concentration factor of l37 Cs for forest pasture in 1993 was rather high compared to that for other pastures. In general, the ratio has been reported to be lower than one (Hove et al. 1994). Similarly, the higher 137 Cs activity level of plants and sheep of forest pasture than that of other pastures was due to the lower nutrient status of the forest soil and to the humus layer, where l37 Cs probably remained readily available for plant uptake (Livens et al. 1991). The low l37 Cs activity level of cultivated pasture was explained by the clay soil rich in nutrients and without organic matter. The distribution of the l37 Cs concentration between the different tissues of sheep agrees well with earlier studies (Andersson and Hansson 1989, Howard et al. 1989, Vandecasteele et al. 1989). The l37 Cs transfer factors for the soil-plantsheep system in this study are valid for natural and semi-natural pastures on clay soils. Pastures on coarse mineral soils with lower K status are supposed to have higher transfer of l37 Cs and, consequently, higher soil to plant and soil to meat transfer factors. The soil-plant transfer factor of this study was higher for semi-natural meadows on medium sand soil than for the semi-natural pasture on clay soil. The difference in the plant activity concentration and the soil to plant transfer factors of 137 Cs between the meadows was suggested to account for the differences in their soil K status.

Plant species
The observed differences in the interspecific l37 Cs activity concentration of vascular plants were considered mostly to be due to environmental factors like uneven distribution of cesium in the soil, differences in the soil properties of pastures and the yearly variation. High variability in the 137 Cs activity level between plant species grown on the same site has been reported by Horrill et al. (1990). Also Nelin and Nylén (1994) found significant differences in the activity concentration of l37 Cs between forest plant species. Kirton et al. (1990) observed that after the Chernobyl fallout the l37 Cs concentration of indigenous plants varied according to the growth pattern of individualplant species. Further, Salt and Mayes (1991) emphasized the importance of taking into account besides the growth pattern, the stage of development and possibly rooting depth when making interspecific comparisons of the plant 137 Cs. According to Guillitte et al. (1994), besides rooting depth, mycorrhizae had an important role determining the interspecific differences of the undercover vegetation of coniferous forests. On the forest pasture of this study, lichens and several mosses had higher l37 Cs ac-tivity levels than vascular plants, which has been documented by several authors (Paakkola and Miettinen 1963, Räsänen and Miettinen 1966, Jackson and Smith 1989, Horrill et al. 1990,Livens et al. 1991. The highest activity levels were detected in lichen and moss genera grown on rocks. Of the former ones, especially Stereocaulon spp. seemed to be able to trap radiocesium abundantly, probably due to the morphology of the thallus. The plant ,37 Cs did not correlate with plant 40 K, which has been confirmed by Evans and Dekker (1968) in crop plants. According to Andersen (1967), the relative uptake of l37 Cs and K by crop plants was more dependent on soil properties, thus affecting the relative availability of the elements, than on plant species. Coughtrey et al. (1990) reported that soil potassium status did not explain all the observed l37 Cs activity concentrations of plant species. The l37 Cs-K relations of plants in grassland ecosystems have been discussed by Salt and Mayes (1993) concerning the selectivity of K uptake, the discrimination of 137 Cs in favour of K and differences in 137 Cs uptake by plant groups.

Yearly variation
The plant and sheep l37 Cs on forest pasture did not vary with years with the exception of the fluctuations probably caused by weather. The results are confirmed by Beresford et al. (1992) who found that after 4 years the Chernobyl radiocesium in organic soils of natural grasslands was as available as aged radiocesium, present in soil for over 20 years. According to the predictions of Hove and Strand (1990), the Chernobyl cesium will remain available in natural ecosystems for decades. Johanson et al. (1991) reported that the 137 Cs activity concentration of moose had not decreased in 4 years after the Chernobyl accident.
The yearly variation of the plant 137 Cs has been suggested by several authors to be partly due to weather conditions (Coughtrey et al. 1989, Livens et al. 1991,Fawaris and Johanson 1994. In addition to the direct effect of moisture and temperature on root growth and nutrient uptake by plants, weather conditions may affect the plant uptake of l37 Cs also via the biological activity of soil micro-organisms. Guillitte et al. (1994) had estimated that even 40% of the soil 137 Cs could be retained in the humus layer by soil microflora. In the field studies ), the low 137 Cs level of leaf vegetables was suggested to be due to cold and rainy June. In this study, such weather conditions seemed to have had an opposite effect on the plant 137 Cs on forest pasture. In 1991, June was cool and rainy and the plant 137 Cs high, whereas in 1992, June was warm and dry and the plant 137 Cs low. The variable effect of weather factors on the plant 137 Cs level of the forest pasture with the humus layer and on the other hand, on the plant 137 Cs of cultivated fields lacking the humus layer might be partly associated with weather-microbe-cesium interactions of the humus layer.
Under certain conditions, fungi were the most important factor causing the yearly variation of 137 Cs in ruminants feeding on natural pasture. The 137 Cs activity concentration of fungal fruit bodies might be 50-100 times higher than that of herbage on the same site (Hove et al. 1990,Olsen 1994. Because only few fungal fruit bodies were found on forest pasture, fungi were not considered to be an important source of 137 Cs in sheep.

Seasonal variation
Seasonal changes in the l37 Cs concentration of vegetation are typical of permanent pastures (Jackson and Smith 1989, Salt and Mayes 1991, Rafferty et al. 1994. The second increase in the plant 137 Cs level in autumn was probably due to the regrowth of grasses dominating on this pasture. In general, the variation followed the most common seasonal patterns described by Salt and Mayes (1993) with seasonal and annual variations, which the authors suggested to be partly due to fluctuations of the water content of plants. The decrease of the plant 40 K on both pastures during the growing season was accounted for the increasing dry matter content of plants. The decline of the plant 40 K was in accordance with the results of Rafferty et al. (1994) and Bunzl and Kracke (1989).