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The influence of fungi on the long-term behaviour of radiocaesium in Norwegian sheep
The Science of the Total Environment 224 Ž1998. 9]17
The influence of fungi on the long-term behaviour of radiocaesium in Norwegian sheep Hanne MehliU , Lavrans Skuterud Norwegian Radiation Protection Authority, P.O. Box 55, N-1345 Østeras, ˚ Norway Received 20 April 1998; accepted 29 June 1998
Abstract Results from 11 years of live monitoring of sheep from a grazing area in Norway formed the basis for a study of the importance of ingested fungal fruit bodies in determining radiocaesium activity concentrations in sheep grazing freely on mountain pasture. The 137Cs activity concentration due to ingested vegetation decreased with an estimated effective ecological half-life of 7.0" 2.6 years. The contribution from ingested fungal fruit bodies to radiocaesium activity concentrations in the sheep was up to 75]85% in the years when fruit bodies were most abundant. The study demonstrates that using a simple exponential function in assessments of long-term consequences of radiocaesium fallout for grazing sheep may be inappropriate. Q 1998 Elsevier Science B.V. All rights reserved. Keywords: Radiocaesium; Sheep; Long-term behaviour; Fungi; Chernobyl; Norway
1. Introduction When radioactive contamination of the environment occurs it is important to know the period for which foodstuffs will remain contaminated. This is determined by the physical decay rate of each radionuclide, and by various natural physical, chemical and biological processes which influence accumulation and elimination of radionuclides in the environment. One example is the rate of fixation of radionuclides in soil which influences bioavailability and hence uptake by vegetation. U
Corresponding author. Tel.: q47 67 16 26 06; fax: q47 67 14 54 44; e-mail: [email protected]
The ‘effective ecological half-life’ ŽTeff . is a parameter commonly used to describe the longterm decline in contamination levels in the environment. This is defined as the time over which the activity concentration in the product falls to one half of the initial value when no measures are taken to reduce the contamination levels. It is expressed as: 1 1 1 s q Teff Tphys Teco
Ž1.
where Teff is the effective ecological half-life, Tphys represents the physical half-life and Teco the ecological half-life of the radionuclide being considered. This implies that the contamination levels decreases exponentially. An inherent assump-
0048-9697r98r$ - see front matter Q 1998 Elsevier Science B.V. All rights reserved. PII S0048-9697Ž98.00255-1
10
H. Mehli, L. Skuterud r The Science of the Total En¨ ironment 224 (1998) 9]17
tion is the constant rates of change in the processes influencing accumulation and elimination of radionuclides, and therefore ‘time’ since the contamination event is the main factor determining the activity concentration levels. The deposition of radiocaesium in Norway from the Chernobyl accident was estimated to be about 6% of the total 134 Cs and 137 Cs released. The mean national deposition was 11 kBq my2 , with maximum mean values within some municipalities of 160 kBq my2 ŽBacke et al., 1986.. Some of the most affected areas in the country were mountain and forest areas heavily used as pasture for reindeer, goat and sheep. In 1988, the 137 Cs activity concentrations in meat of animals grazing on unimproved mountain and forest pastures in Norway increased rapidly during the second half of the summer. The increase coincided with the early appearance of large quantities of fungal fruit bodies, and resulted in higher activity concentrations than in 1987 ŽHove et al., 1990.. It has long been known that fungi accumulate caesium more effectively than green plants ŽHaugen and Uhlen, 1992; Olsen, 1994; Haselwandter and Berreck, 1988., and similar effects had also been observed earlier in a study based on bomb fallout data ŽJohnson and Nayfield, 1970.. It has later been shown that consumption of fungal fruit bodies is also important in the transfer of radiocaesium to humans ŽSkuterud et al., 1997.. Since fungal fruit bodies are seasonally important in the diets of free ranging animals ŽWarren and Mysterud, 1991., years with abundant fungi fruiting can yield elevated radiocaesium activity concentrations in these animals. This annually varying factor suggests that the long-term behaviour of radiocaesium in grazing animals is poorly described using the exponential decrease approach. However, the applicability of this approach will depend on how important the radiocaesium ingested via fungi is, compared to that ingested via vegetation, for the activity concentrations in the animals. Temperature and precipitation are known to be important parameters affecting fruit body growth, and fruit bodies are expected to be more abundant in warm and humid conditions, than in cold and dry weather. However, as long as there is no
satisfactory model available to predict the appearance and abundance of fungal fruit bodies, it is also difficult to predict the influence of ingested fungi on radiocaesium activity concentrations in animals. Annually recorded data on the live monitoring of sheep and fruit body abundance in Norway have been used in this paper to develop a regression model in order to determine the influence of fruit body abundance on the long-term behaviour of 137 Cs in sheep grazing freely in Norwegian mountains. 2. Materials and methods 2.1. The data sets Since 1987, live monitoring of free ranging sheep grazing in contaminated areas of Norway has been conducted in the autumn to ensure that only animals with radiocaesium activity concentrations below the national intervention limit of 600 Bq kgy1 are slaughtered. The monitoring is performed using NaI-detectors and the total radiocaesium Ži.e. 134 Cs and 137 Cs combined. activity concentration is recorded ŽBrynildsen and Strand, 1994.. Before analysis the contribution from 134 Cs was calculated for each year and subtracted from the recorded data and the modelling results consider 137 Cs only. It was assumed that fallout from the nuclear weapons tests did not affect the results because it constitutes less than 10% of the Chernobyl 137 Cs deposition in the area. The live monitoring records used in this study were from the ‘grazing unit’ 1 Fonnasfjellet in the ˚ county of Hedmark. The grazing area of this unit is roughly 120 km2 , and incorporates forest and mountain areas from about 300 to 1000 m above sea level ŽFig. 1.. No deposition measurements have specifically been made in this grazing area. Average 137 Cs deposition at municipality level in
1 In Norway most sheep farmers are organised in associations based on geographical connection or proximity. All animals belonging to members of one association graze in the same area, a so-called ‘grazing unit’.
H. Mehli, L. Skuterud r The Science of the Total En¨ ironment 224 (1998) 9]17
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Table 1 Overview of the information that forms the basis for the study Year
1987 1988 1989 1990 1991 1992 1993 1994 1995 1996 1997 a b
Monitoring date
28.08 01.09 15.08 15.08 11.09 02.09 04.09 06.09 15.08 09.10 05.09
No. of animals
11 10 36 25 10 10 10 10 10 10 6
137
Cs activity concentration levels, Bq kgy1 Median
Mean " s.e.a
582 1099 250 105 1120 334 596 345 189 504 569
562 " 39 1136 " 128 270 " 16 122 " 10 1154 " 37 324 " 26 602 " 52 391 " 46 195 " 13 497 " 33 562 " 66
Mushroom abundanceb
3 3 1 1 3 1 2 2 1 1 3
s.e., standard error of mean. 1, low abundance; 2, medium abundance; 3, high abundance.
the area is about 20 kBq my2 ŽBacke et al., 1986.. From the grazing unit usually 10 animals Žmixed ewes and lambs. were monitored annually providing an estimate of the average 137 Cs activity concentration for all animals. Altogether the data set consisted of 148 records Ž69 ewes and 79 lambs, different animals from year to year. obtained between August 15 and October 9 during 1987]1997. The data used were part of a routine monitoring where animals should be representative for the whole grazing unit. Details of the data set are given in Table 1. In the nearby area of Elgvasshø ŽFig. 1., appearance and abundance of fungal fruit bodies were observed annually by a person living in the area. The abundance of fruit bodies was categorised according to the crude relative units: low, medium and high fruit body abundance Žbased on the number of samples collected.. This information Žshown in Table 1. was used as an indication of the abundance of fruit bodies in the grazing areas. 2.2. Model de¨ elopment Winter feeds such as hay and silage are produced on cultivated land and contain low radiocaesium concentrations compared to the summer feed in unimproved forest and mountain areas. Combined with an effective biological half-life
ŽT bio . of about 2]3 weeks for sheep ŽHove et al., 1994., winter feeding leads to low radiocaesium contents in sheep in early summer, at the beginning of the grazing season. Thus, when the animals are released onto contaminated pasture the radiocaesium activity concentrations in meat rises rapidly. If we assume that the animals graze a pasture with constant and homogenous radiocaesium activity concentrations in vegetation, the increase in radiocaesium concentrations in sheep can be described by ŽFig. 2a.: AŽ t p . s B ? Ž 1 y eyl bio?t p .
Ž2.
where AŽ t p . is the radiocaesium activity concentrations in sheep in Bq kgy1 , t p is days on pasture and l bio is the effective biological elimination rate for sheep Ž l bio s ln 2rT bio .. In this study a value in the middle of the above mentioned range, 18 days, was selected for the effective biological half-life. The parameter B is the equilibrium radiocaesium activity concentration in sheep Ždepending on the radiocaesium activity concentration in the feed.. If no measures are taken to reduce the contamination, the year by year change in the equilibrium level B will then follow an exponential decrease due to physical decay and ecological processes ŽFig. 2b.:
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H. Mehli, L. Skuterud r The Science of the Total En¨ ironment 224 (1998) 9]17
the genera appearing, abundance of fruit bodies, how long the fruit bodies are available as feed for the animals and the extent of ingestion by animals. If, for simplicity, fruit bodies are assumed to arrive at approximately the same time every year Žand the same species arrive in the same relative amounts., the most important variable for radiocaesium activity concentration in animals will be the time grazing on the pasture, or, more specifically, the time grazing on pasture when fruit bodies are available. Radiocaesium levels in animals during a grazing season can then be described by: AŽ t c , t p , F . s C ? eyl eff ?t c q F ? Ž 1 y eyl bio?t p .
Fig. 1. Map of the study area in Hedmark county, southern Norway. Fonnasfjellet is the area of the grazing unit, and ˚ Elgvasshø is the site where fungal fruit body abundance was recorded.
B Ž t c . s C ? eyl eff ?t c
Ž3.
Here B Ž t c . is the radiocaesium activity concentration in sheep ŽBq kgy1 ., t c is years since the fallout event Žthe Chernobyl accident., leff is the effective elimination rate Ž leff s ln 2rTeff . and C is the radiocaesium activity concentration at t c s 0. However, since the fallout in spring 1986 gave direct contamination of above ground plant parts, data from that year were not included in the analysis. Fruit bodies with higher radiocaesium activity concentrations than most vegetation species Že.g. Hove et al., 1990; Olsen, 1994. appear in late summer and will increase the radiocaesium activity levels of animals consuming them ŽFig. 3.. The total increase in radiocaesium activity concentrations in animals caused by fungi will depend on
Ž4.
Here, the first term gives the radiocaesium activity concentration due to consumed vegetation Žas in Fig. 2. and the second term gives the additional radiocaesium activity concentration due to consumption of fruit bodies ŽFig. 3.. The factor F represents the equilibrium radiocaesium activity concentration as a result of ingested fungi only, and t p the time that fungi are ingested for. The information available about fungi was recorded as the relative units low, medium and high fruit body abundance. Since the equilibrium level F will vary with the abundance of fruit bodies ŽFig. 3., F was divided into three parts, F1 ? f 1 q F2 ? f 2 q F3 ? f 3 , to account for differences between years. The factor f 1 was given the value 1 in years with low abundance and the value 0 otherwise, and correspondingly for f 2 Žmedium abundance. and f 3 Žhigh abundance.. The complete model to describe radiocaesium activity concentrations in sheep then becomes: AŽ t c , t p , f 1 , f 2 , f 3 . s C ? eyl eff ?t c q Ž F1 f 1 q F2 f 2 qF3 f 3 . ? Ž 1 y eyl bio?t p .
Ž5.
With the information given in Table 1 Žmean Cs activity concentrations, year, time on pasture, information about fruit body abundance Ž f 1 , f 2 , f 3 .. and the effective biological half-life, the model was used to estimate the effective elimination rate and the relative importance of fruit body abundance for the radiocaesium activity concen137
H. Mehli, L. Skuterud r The Science of the Total En¨ ironment 224 (1998) 9]17
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Fig. 2. Theoretical development in radiocaesium activity concentrations in sheep during each grazing season Ža. and year by year decrease in equilibrium activity concentrations Žb. due to intake of contaminated vegetation.
tration in sheep. As mentioned above, data for 1986 were not included in the study, and the value of C was therefore not interpreted. The statistical analysis and model development was performed using nonlinear regression with SPSS2 software. 3. Results and discussion Conducting the regression analysis on the data using the model in Eq. Ž5. gave the results presented in Table 2. The model output is compared with the experimental data in Fig. 4, illustrating the significant correlation indicated by the R 2 value of 0.70. There are several assumptions made in the model development: 1. Radiocaesium activity concentrations in sheep are assumed to increase exponentially during the first weeks on pasture, and then stabilise at a level dependent on the radiocaesium activity concentration in the vegetation in the
2 SPSS version 6.0, SPSS Inc., 444 N. Michigan Avenue, Chicago, IL 60611, USA.
grazing area. This assumes that contamination of the vegetation is homogenous in the grazing area throughout the grazing season. However, as deposition, soil type and potential for uptake of radiocaesium by vegetation species vary across the area, radiocaesium activity concentration in vegetation will also vary. This may be especially apparent over different vegetation zones Žfor instance forested areas, bogs, highland areas.. After the animals are released onto the pasture, they graze freely over the whole area without daily or any routine care for the whole summer. Animal movement may therefore, to some extent, even out differences in activity concentrations in feed. 2. Average radiocaesium activity concentrations in vegetation are assumed to decrease exponentially with years. The decrease in activity concentrations varies between species Že.g. Haugen and Uhlen, 1992; Rosen ´ et al., 1995., and the decrease in the average radiocaesium concentration in mixed vegetation may therefore be better estimated by more than one factor. However, the current approach, with a relatively small data set, did not allow for the implementation of more complex models.
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H. Mehli, L. Skuterud r The Science of the Total En¨ ironment 224 (1998) 9]17
Fig. 3. The effect of appearance of fungal fruit bodies on radiocaesium activity concentrations in sheep; ] ] ], the radiocaesium concentration due to consumed vegetation; }}}, the additional radiocaesium concentration due to intake of fruit bodies, for three different levels of fruit body abundance.
3. The amount of radiocaesium available in fruit bodies in the pasture is assumed to be constant from the first day they appear until the animals were monitored. However, species of fungi differ in their rate of accumulation of radiocaesium ŽOlsen, 1994; Amundsen et al., 1996; Kammerer et al., 1994.. In contrast to vegetation, the composition of fungi species may vary greatly between years, and the presence of fruit bodies of different species may therefore be critical Žsince in some years substantial amounts of certain ‘high accumulating’ species may appear.. The model only considers relative amounts of fruit bodies regardless of species.
4. The date for appearance of fungal fruit bodies varies from year to year but the season in the studied area is assumed to start in August as observed by Amundsen et al. Ž1996.. In another mountain area in southern Norway the date for fruiting of fungi was observed to vary from 25 July to 5 September ŽR.A. Olsen, Agricultural University of Norway, pers. comm... The factor ‘time on pasture’ in the model should ideally have been time on pasture after appearance of fruit bodies, and assuming the same fruiting date every year is therefore probably one of the larger sources of uncertainty in the model. August is generally the main season for the appearance of
Table 2 Results of the regression analysis using the developed model for long-term behaviour of Parameter
leff C F1 F2 F3
Estimated value y1
0.10 year 300 Bq kgy1 406 Bq kgy1 609 Bq kgy1 1300 Bq kgy1
137
Cs in sheep ŽEq. Ž5..
95% conf.int.
R2
Estimated Teff " s.e.
Ž0.03, 0.17. Ž200, 390. Ž360, 450. Ž542, 677. Ž1160, 1440.
0.70
7.0" 2.6 year
Mid August Ž15th. was chosen as the time of fruit body appearance.
H. Mehli, L. Skuterud r The Science of the Total En¨ ironment 224 (1998) 9]17
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Fig. 4. Estimated mean Ž`. 137 Cs activity concentration in sheep at Fonnasfjellet compared with the observed mean Žv., ˚ mean " standard error Žs.e.. of mean. The dot line shows the estimated decrease in 137 Cs activity concentrations in sheep due to decreasing contamination levels in vegetation. Time for appearance of fruit bodies was set to 15 August.
fungi in Norway, and the largest quantities of fruit bodies seemed to be found at the end of August and beginning of September at Elgvasshø. Thus it is difficult to estimate the exact time for fruit body appearance as an input to the model. Mid-August Ž15th. was chosen as the date of fruit body appearance, and also gives the best model fit. Regression analysis of Eq. Ž5. gave the ratios 1:1.5:3.2 between the three levels of fungal abundance Ž F1: F2 : F3 .. 5. The fact that the data set consists of measurements of both ewes and lambs adds another factor of uncertainty to the model. Since the data set mostly consists of only 10 measurements each year, dividing the data set into sub groups increases the uncertainty. However, since we are using the model to analyse the year to year changes in radiocaesium activity concentrations, the difference in biological half-lives between animals due to age was not thought to be of significance. This was also supported by analysis after dividing the data set into ewes and lambs and applying biological half-life values of 18 and 14 days ŽIAEA, 1994. respectively; the result-
ing model parameter values did not differ significantly between the groups. Therefore lambs and ewes were treated as one homogenous group in the data analysis. This also demonstrates that the variability in biological half-lives that exists between individual animals will be of little importance for the final model output. 6. Information about abundance of fungi in the observed grazing areas was adopted from the area of Elgvasshø, which is geographically separated from Fonnasfjellet. However, since ˚ the relative, not the absolute, amount of fungi is important in this model, and relative abundance is similar over large distances, the fungi information from Elgvasshø was assumed to be valid for the area of Fonnasfjellet as well. ˚ Additionally the two areas are ecologically and climatically similar. Abundance of fruit bodies at Elgvasshø was recorded at approximately the same time every year. This introduces some uncertainty in determining the amount of fungi available to sheep over the growing season because the timing of appearance and duration of fruit bodies changes from year to year. The classification of levels
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H. Mehli, L. Skuterud r The Science of the Total En¨ ironment 224 (1998) 9]17
of fungi abundance was subjective and with no clear distinction between levels. A better approach might have been to quantify the number of fruit bodies per unit ground surface. 7. Ideally the model should also account for decreasing radiocaesium activity concentration in fruit bodies with time after the Chernobyl accident. However, evidence for the long-term behaviour of radiocaesium in different mushroom species is not unequivocal. A recent study suggests classification of mushrooms into three groups depending on their changes in radiocaesium activity concentrations with time; decreasing, increasing and with roughly constant concentrations ŽWirth et al., 1996.. For control the term eyl fu ngi t c was included in the last part of Eq. Ž5.. The regression analysis returned an insignificant lfungi and the possible decrease in fungi radiocaesium concentration levels was therefore ignored. In addition to the uncertainties introduced by the model assumptions, there are also considerable statistical uncertainties connected to the live monitoring data. Firstly, there is no statistically random selection of sheep to be monitored, nor control that they actually are representative of the grazing unit. Furthermore, a study of variability within two whole grazing units of about 200 sheep showed that the coefficient of variance was about 30% ŽMehli, 1996.. This implies that even if the monitored sheep were randomly selected, sampling only 10 sheep from a grazing unit of several hundred animals gives an inherent statistical uncertainty of about 20% in the estimated mean radiocaesium activity concentration ŽMehli, 1996.. Taking these factors into account, the obtained R 2 value was satisfactory for the developed model. The estimated 137 Cs activity concentration in 1987, which was a year with large amounts of fruit bodies Žalthough not as much as 1988., was high compared with the observed level. This may be due to soil complexation processes and the relatively short time after the fallout which may not have allowed much radiocaesium to move down
the soil profile for uptake and accumulation in vegetation and fungi ŽElster et al., 1987.. In particular 1988, but also 1991, were years with high fruit body abundance. The results suggest that 75]85% of the radiocaesium activity concentrations in sheep these years were due to ingested fungi. The rate of decrease in 137Cs activity concentrations in the environment will differ between areas, and earlier estimates of effective half lives for 137Cs in Norwegian sheep have indicated values in the range 3]20 years ŽStrand, 1994.. The value derived in this study was 7.0" 2.6 years when the influence of mushrooms is excluded. Fitting a simple exponential function to the data set returned a positive leff Ži.e. a negative half-life . and an R 2 of only 0.03. This clearly illustrates that using simple exponential functions alone in estimates of long-term behaviour have definite limitations when time since the contamination event is not the only important factor affecting the radiocaesium activity concentrations. There were several ways the data set could have been split to obtain a more exact model, for instance including more than three levels of fungi abundance. However, dividing the data set decreased the number of observations in each group and increased the uncertainties in the estimated mean values. Teff estimated from different model variants was not significantly different from the effective half-life given in Table 2. 4. Conclusions The suggested model appears to describe adequately the long-term behaviour of radiocaesium in sheep grazing unimproved pasture. Despite several assumptions and uncertainties, the observed and estimated values of radiocaesium activity concentrations in sheep showed good correlation with an R 2 of 0.70. The results support the hypothesis that fungal fruit bodies are important sources of radiocaesium for grazing sheep in Norway. The contribution from ingested fruit bodies was estimated to be 75]85% of the radiocaesium activity concentrations in sheep in 1988 and 1991 which were years with a high fruit body abundance. The esti-
H. Mehli, L. Skuterud r The Science of the Total En¨ ironment 224 (1998) 9]17
mated effective half-life for 137 Cs activity concentrations in sheep due to consumed vegetation in the studied grazing unit was 7.0" 2.6 years, but years with high fruit body abundance are likely to continue to result in more elevated radiocaesium activity concentrations in sheep in the future. Depending on the abundance of fruit bodies, the model suggests that the average 137 Cs concentration levels in the grazing unit will be 260]630 Bq kgy1 in 1998 Žpresumed 2 weeks grazing after appearance of fruit bodies.. The study demonstrates that using a simple exponential function in assessments of long-term consequences of radiocaesium fallout for grazing sheep may be inappropriate. Acknowledgements This study would not have been possible without access to the live monitoring files at the office of the County Veterinary in Hedmark, and the help by Johan Teige was highly appreciated. Of equal importance was the fungal fruit body abundance information kindly provided by Hans Myhre. We are also grateful to Professor Henning Omre, Norwegian University of Science and Technology, who provided valuable ideas during the initial phase of the model development. Thanks also go to Dr Brenda J. Howard at the Institute of Terrestrial Ecology ŽUK., and our colleagues Dr Per Strand, Dr Andrew I. Cooke and Dr Justin Brown at the Norwegian Radiation Protection Authority, for comments during the course of writing this paper. References Amundsen I, Gulden G, Strand P. Accumulation and long term behaviour of radiocaesium in Norwegian fungi. Sci Total Environ 1996;184:163]171. Backe S, Bjerke H, Rudjord AL, Ugletveit F. Deposition of caesium in Norway after the Chernobyl accident. Østeras, ˚ National Institute of Radiation Hygiene, Report 1986:5 Žin Norwegian.. Brynildsen LI, Strand P. A rapid method for the determination of radioactive caesium in live animals and carcasses, and its practical application in Norway after the Chernobyl accident. Acta Vet Scand 1994;35:401]408. Elster EF, Fink R, Holl ¨ W, Lengfelder E, Ziegler H. Natural and Chernobyl-caused radioactivity in mushrooms, mosses
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and soil-samples of defined biotopes in SW Bavaria. Oecologia 1987;73:553]558. Haselwandter K, Berreck M. Fungi as bioindicators of radiocaesium contamination: Pre- and post-Chernobyl activities. Trans Br Mycol Soc 1988;90:171]174. Haugen LE, Uhlen G. Transport av radionuklider i jord og opptak i planter og sopp. In: Garmo TH, Gunnerød TB, editors. Radioaktivt Nedfall fra Tsjernobyl-ulykken. Oslo: Norges Landbruksvitenskapelige Forskningsrad, ˚ 1992:43]64 Žin Norwegian.. Hove K, Pedersen Ø, Garmo T, Hansen HS, Staaland H. Fungi: a major source of radiocaesium contamination of grazing ruminants in Norway. Health Phys 1990;59:189]192. Hove K, Lonsjo ¨ ¨ H, Andersson I, Sormunen-Cristian R, Hansen HS, Indridason K, Joensen HP, Kossila V, Liken A, Magnusson S, Nielsen SP, Paasikallio A, Palsson SE, Rosen ´ ´ K, Selnæs T, Strand P, Vestergaard T. Radiocaesium transfer to grazing sheep in Nordic environments. In: Dahlgaard H, editor. Nordic Radioecology. Amsterdam: Elsevier, 1994:211]228. IAEA: Guidelines for agricultural countermeasures following an accidental release of radionuclides. Technical Reports Series No 363. Vienna: International Atomic Energy Agency, 1994. Johnson W, Nayfield CL. Elevated levels of cesium-137 in common mushrooms ŽAgaricaceae. with possible relationship to high levels of cesium-137 in whitetail deer, 1968]1969. Radiol Health Data Rep 1970;11:527]531. Kammerer L, Heirsche L, Wirth E. Uptake of radiocaesium by different species of mushrooms. J Environ Radioact 1994;23:135]150. Mehli H. Radiocaesium in grazing sheep. Østeras, ˚ Norwegian Radiation Protection Authority, StralevernRapport 1996:2. ˚ Olsen R. The transfer of radiocaesium from soil to plants and fungi in seminatural ecosystems. In: Dahlgaard H, editor. Nordic Radioecology. Amsterdam: Elsevier, 1994:265]286. Rosen ´ K, Andersson I, Lonsjo ¨ ¨ H. Transfer of radiocaesium from soil to vegetation and to grazing lambs in a mountain area in Northern Sweden. J Environ Radioact 1995;26: 237]257. Skuterud L, Travnikova IG, Balonov MI, Strand P, Howard BJ. Contribution of fungi to radiocaesium intake by rural populations in Russia. Sci Total Environ 1997;193:237]242. Strand P. Radioactive fallout in Norway from the Chernobyl accident. Østeras, ˚ Norwegian Radiation Protection Authority, NRPA Report 1994:2. Warren JT, Mysterud I. Fungi in the diet of domestic sheep. Rangelands 1991;13:168]171. Wirth E, Ruhm W, Kammerer L, Steiner M. Model for ¨ predicting future cesium-137 contamination in fungi. In: Amiro B, Avadhanula R, Johansson G, Larsson C-M, Luning M, editors. Protection of the Natural Environment. ¨ Proceedings of the International Symposium on Ionising Radiation. The Swedish Radiation Protection Institute and The Atomic Energy Control Board of Canada. Stockholm, May 20]24, 1996:176]187.
The influence of fungi on the long-term behaviour of radiocaesium in Norwegian sheep Hanne MehliU , Lavrans Skuterud Norwegian Radiation Protection Authority, P.O. Box 55, N-1345 Østeras, ˚ Norway Received 20 April 1998; accepted 29 June 1998
Abstract Results from 11 years of live monitoring of sheep from a grazing area in Norway formed the basis for a study of the importance of ingested fungal fruit bodies in determining radiocaesium activity concentrations in sheep grazing freely on mountain pasture. The 137Cs activity concentration due to ingested vegetation decreased with an estimated effective ecological half-life of 7.0" 2.6 years. The contribution from ingested fungal fruit bodies to radiocaesium activity concentrations in the sheep was up to 75]85% in the years when fruit bodies were most abundant. The study demonstrates that using a simple exponential function in assessments of long-term consequences of radiocaesium fallout for grazing sheep may be inappropriate. Q 1998 Elsevier Science B.V. All rights reserved. Keywords: Radiocaesium; Sheep; Long-term behaviour; Fungi; Chernobyl; Norway
1. Introduction When radioactive contamination of the environment occurs it is important to know the period for which foodstuffs will remain contaminated. This is determined by the physical decay rate of each radionuclide, and by various natural physical, chemical and biological processes which influence accumulation and elimination of radionuclides in the environment. One example is the rate of fixation of radionuclides in soil which influences bioavailability and hence uptake by vegetation. U
Corresponding author. Tel.: q47 67 16 26 06; fax: q47 67 14 54 44; e-mail: [email protected]
The ‘effective ecological half-life’ ŽTeff . is a parameter commonly used to describe the longterm decline in contamination levels in the environment. This is defined as the time over which the activity concentration in the product falls to one half of the initial value when no measures are taken to reduce the contamination levels. It is expressed as: 1 1 1 s q Teff Tphys Teco
Ž1.
where Teff is the effective ecological half-life, Tphys represents the physical half-life and Teco the ecological half-life of the radionuclide being considered. This implies that the contamination levels decreases exponentially. An inherent assump-
0048-9697r98r$ - see front matter Q 1998 Elsevier Science B.V. All rights reserved. PII S0048-9697Ž98.00255-1
10
H. Mehli, L. Skuterud r The Science of the Total En¨ ironment 224 (1998) 9]17
tion is the constant rates of change in the processes influencing accumulation and elimination of radionuclides, and therefore ‘time’ since the contamination event is the main factor determining the activity concentration levels. The deposition of radiocaesium in Norway from the Chernobyl accident was estimated to be about 6% of the total 134 Cs and 137 Cs released. The mean national deposition was 11 kBq my2 , with maximum mean values within some municipalities of 160 kBq my2 ŽBacke et al., 1986.. Some of the most affected areas in the country were mountain and forest areas heavily used as pasture for reindeer, goat and sheep. In 1988, the 137 Cs activity concentrations in meat of animals grazing on unimproved mountain and forest pastures in Norway increased rapidly during the second half of the summer. The increase coincided with the early appearance of large quantities of fungal fruit bodies, and resulted in higher activity concentrations than in 1987 ŽHove et al., 1990.. It has long been known that fungi accumulate caesium more effectively than green plants ŽHaugen and Uhlen, 1992; Olsen, 1994; Haselwandter and Berreck, 1988., and similar effects had also been observed earlier in a study based on bomb fallout data ŽJohnson and Nayfield, 1970.. It has later been shown that consumption of fungal fruit bodies is also important in the transfer of radiocaesium to humans ŽSkuterud et al., 1997.. Since fungal fruit bodies are seasonally important in the diets of free ranging animals ŽWarren and Mysterud, 1991., years with abundant fungi fruiting can yield elevated radiocaesium activity concentrations in these animals. This annually varying factor suggests that the long-term behaviour of radiocaesium in grazing animals is poorly described using the exponential decrease approach. However, the applicability of this approach will depend on how important the radiocaesium ingested via fungi is, compared to that ingested via vegetation, for the activity concentrations in the animals. Temperature and precipitation are known to be important parameters affecting fruit body growth, and fruit bodies are expected to be more abundant in warm and humid conditions, than in cold and dry weather. However, as long as there is no
satisfactory model available to predict the appearance and abundance of fungal fruit bodies, it is also difficult to predict the influence of ingested fungi on radiocaesium activity concentrations in animals. Annually recorded data on the live monitoring of sheep and fruit body abundance in Norway have been used in this paper to develop a regression model in order to determine the influence of fruit body abundance on the long-term behaviour of 137 Cs in sheep grazing freely in Norwegian mountains. 2. Materials and methods 2.1. The data sets Since 1987, live monitoring of free ranging sheep grazing in contaminated areas of Norway has been conducted in the autumn to ensure that only animals with radiocaesium activity concentrations below the national intervention limit of 600 Bq kgy1 are slaughtered. The monitoring is performed using NaI-detectors and the total radiocaesium Ži.e. 134 Cs and 137 Cs combined. activity concentration is recorded ŽBrynildsen and Strand, 1994.. Before analysis the contribution from 134 Cs was calculated for each year and subtracted from the recorded data and the modelling results consider 137 Cs only. It was assumed that fallout from the nuclear weapons tests did not affect the results because it constitutes less than 10% of the Chernobyl 137 Cs deposition in the area. The live monitoring records used in this study were from the ‘grazing unit’ 1 Fonnasfjellet in the ˚ county of Hedmark. The grazing area of this unit is roughly 120 km2 , and incorporates forest and mountain areas from about 300 to 1000 m above sea level ŽFig. 1.. No deposition measurements have specifically been made in this grazing area. Average 137 Cs deposition at municipality level in
1 In Norway most sheep farmers are organised in associations based on geographical connection or proximity. All animals belonging to members of one association graze in the same area, a so-called ‘grazing unit’.
H. Mehli, L. Skuterud r The Science of the Total En¨ ironment 224 (1998) 9]17
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Table 1 Overview of the information that forms the basis for the study Year
1987 1988 1989 1990 1991 1992 1993 1994 1995 1996 1997 a b
Monitoring date
28.08 01.09 15.08 15.08 11.09 02.09 04.09 06.09 15.08 09.10 05.09
No. of animals
11 10 36 25 10 10 10 10 10 10 6
137
Cs activity concentration levels, Bq kgy1 Median
Mean " s.e.a
582 1099 250 105 1120 334 596 345 189 504 569
562 " 39 1136 " 128 270 " 16 122 " 10 1154 " 37 324 " 26 602 " 52 391 " 46 195 " 13 497 " 33 562 " 66
Mushroom abundanceb
3 3 1 1 3 1 2 2 1 1 3
s.e., standard error of mean. 1, low abundance; 2, medium abundance; 3, high abundance.
the area is about 20 kBq my2 ŽBacke et al., 1986.. From the grazing unit usually 10 animals Žmixed ewes and lambs. were monitored annually providing an estimate of the average 137 Cs activity concentration for all animals. Altogether the data set consisted of 148 records Ž69 ewes and 79 lambs, different animals from year to year. obtained between August 15 and October 9 during 1987]1997. The data used were part of a routine monitoring where animals should be representative for the whole grazing unit. Details of the data set are given in Table 1. In the nearby area of Elgvasshø ŽFig. 1., appearance and abundance of fungal fruit bodies were observed annually by a person living in the area. The abundance of fruit bodies was categorised according to the crude relative units: low, medium and high fruit body abundance Žbased on the number of samples collected.. This information Žshown in Table 1. was used as an indication of the abundance of fruit bodies in the grazing areas. 2.2. Model de¨ elopment Winter feeds such as hay and silage are produced on cultivated land and contain low radiocaesium concentrations compared to the summer feed in unimproved forest and mountain areas. Combined with an effective biological half-life
ŽT bio . of about 2]3 weeks for sheep ŽHove et al., 1994., winter feeding leads to low radiocaesium contents in sheep in early summer, at the beginning of the grazing season. Thus, when the animals are released onto contaminated pasture the radiocaesium activity concentrations in meat rises rapidly. If we assume that the animals graze a pasture with constant and homogenous radiocaesium activity concentrations in vegetation, the increase in radiocaesium concentrations in sheep can be described by ŽFig. 2a.: AŽ t p . s B ? Ž 1 y eyl bio?t p .
Ž2.
where AŽ t p . is the radiocaesium activity concentrations in sheep in Bq kgy1 , t p is days on pasture and l bio is the effective biological elimination rate for sheep Ž l bio s ln 2rT bio .. In this study a value in the middle of the above mentioned range, 18 days, was selected for the effective biological half-life. The parameter B is the equilibrium radiocaesium activity concentration in sheep Ždepending on the radiocaesium activity concentration in the feed.. If no measures are taken to reduce the contamination, the year by year change in the equilibrium level B will then follow an exponential decrease due to physical decay and ecological processes ŽFig. 2b.:
12
H. Mehli, L. Skuterud r The Science of the Total En¨ ironment 224 (1998) 9]17
the genera appearing, abundance of fruit bodies, how long the fruit bodies are available as feed for the animals and the extent of ingestion by animals. If, for simplicity, fruit bodies are assumed to arrive at approximately the same time every year Žand the same species arrive in the same relative amounts., the most important variable for radiocaesium activity concentration in animals will be the time grazing on the pasture, or, more specifically, the time grazing on pasture when fruit bodies are available. Radiocaesium levels in animals during a grazing season can then be described by: AŽ t c , t p , F . s C ? eyl eff ?t c q F ? Ž 1 y eyl bio?t p .
Fig. 1. Map of the study area in Hedmark county, southern Norway. Fonnasfjellet is the area of the grazing unit, and ˚ Elgvasshø is the site where fungal fruit body abundance was recorded.
B Ž t c . s C ? eyl eff ?t c
Ž3.
Here B Ž t c . is the radiocaesium activity concentration in sheep ŽBq kgy1 ., t c is years since the fallout event Žthe Chernobyl accident., leff is the effective elimination rate Ž leff s ln 2rTeff . and C is the radiocaesium activity concentration at t c s 0. However, since the fallout in spring 1986 gave direct contamination of above ground plant parts, data from that year were not included in the analysis. Fruit bodies with higher radiocaesium activity concentrations than most vegetation species Že.g. Hove et al., 1990; Olsen, 1994. appear in late summer and will increase the radiocaesium activity levels of animals consuming them ŽFig. 3.. The total increase in radiocaesium activity concentrations in animals caused by fungi will depend on
Ž4.
Here, the first term gives the radiocaesium activity concentration due to consumed vegetation Žas in Fig. 2. and the second term gives the additional radiocaesium activity concentration due to consumption of fruit bodies ŽFig. 3.. The factor F represents the equilibrium radiocaesium activity concentration as a result of ingested fungi only, and t p the time that fungi are ingested for. The information available about fungi was recorded as the relative units low, medium and high fruit body abundance. Since the equilibrium level F will vary with the abundance of fruit bodies ŽFig. 3., F was divided into three parts, F1 ? f 1 q F2 ? f 2 q F3 ? f 3 , to account for differences between years. The factor f 1 was given the value 1 in years with low abundance and the value 0 otherwise, and correspondingly for f 2 Žmedium abundance. and f 3 Žhigh abundance.. The complete model to describe radiocaesium activity concentrations in sheep then becomes: AŽ t c , t p , f 1 , f 2 , f 3 . s C ? eyl eff ?t c q Ž F1 f 1 q F2 f 2 qF3 f 3 . ? Ž 1 y eyl bio?t p .
Ž5.
With the information given in Table 1 Žmean Cs activity concentrations, year, time on pasture, information about fruit body abundance Ž f 1 , f 2 , f 3 .. and the effective biological half-life, the model was used to estimate the effective elimination rate and the relative importance of fruit body abundance for the radiocaesium activity concen137
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Fig. 2. Theoretical development in radiocaesium activity concentrations in sheep during each grazing season Ža. and year by year decrease in equilibrium activity concentrations Žb. due to intake of contaminated vegetation.
tration in sheep. As mentioned above, data for 1986 were not included in the study, and the value of C was therefore not interpreted. The statistical analysis and model development was performed using nonlinear regression with SPSS2 software. 3. Results and discussion Conducting the regression analysis on the data using the model in Eq. Ž5. gave the results presented in Table 2. The model output is compared with the experimental data in Fig. 4, illustrating the significant correlation indicated by the R 2 value of 0.70. There are several assumptions made in the model development: 1. Radiocaesium activity concentrations in sheep are assumed to increase exponentially during the first weeks on pasture, and then stabilise at a level dependent on the radiocaesium activity concentration in the vegetation in the
2 SPSS version 6.0, SPSS Inc., 444 N. Michigan Avenue, Chicago, IL 60611, USA.
grazing area. This assumes that contamination of the vegetation is homogenous in the grazing area throughout the grazing season. However, as deposition, soil type and potential for uptake of radiocaesium by vegetation species vary across the area, radiocaesium activity concentration in vegetation will also vary. This may be especially apparent over different vegetation zones Žfor instance forested areas, bogs, highland areas.. After the animals are released onto the pasture, they graze freely over the whole area without daily or any routine care for the whole summer. Animal movement may therefore, to some extent, even out differences in activity concentrations in feed. 2. Average radiocaesium activity concentrations in vegetation are assumed to decrease exponentially with years. The decrease in activity concentrations varies between species Že.g. Haugen and Uhlen, 1992; Rosen ´ et al., 1995., and the decrease in the average radiocaesium concentration in mixed vegetation may therefore be better estimated by more than one factor. However, the current approach, with a relatively small data set, did not allow for the implementation of more complex models.
14
H. Mehli, L. Skuterud r The Science of the Total En¨ ironment 224 (1998) 9]17
Fig. 3. The effect of appearance of fungal fruit bodies on radiocaesium activity concentrations in sheep; ] ] ], the radiocaesium concentration due to consumed vegetation; }}}, the additional radiocaesium concentration due to intake of fruit bodies, for three different levels of fruit body abundance.
3. The amount of radiocaesium available in fruit bodies in the pasture is assumed to be constant from the first day they appear until the animals were monitored. However, species of fungi differ in their rate of accumulation of radiocaesium ŽOlsen, 1994; Amundsen et al., 1996; Kammerer et al., 1994.. In contrast to vegetation, the composition of fungi species may vary greatly between years, and the presence of fruit bodies of different species may therefore be critical Žsince in some years substantial amounts of certain ‘high accumulating’ species may appear.. The model only considers relative amounts of fruit bodies regardless of species.
4. The date for appearance of fungal fruit bodies varies from year to year but the season in the studied area is assumed to start in August as observed by Amundsen et al. Ž1996.. In another mountain area in southern Norway the date for fruiting of fungi was observed to vary from 25 July to 5 September ŽR.A. Olsen, Agricultural University of Norway, pers. comm... The factor ‘time on pasture’ in the model should ideally have been time on pasture after appearance of fruit bodies, and assuming the same fruiting date every year is therefore probably one of the larger sources of uncertainty in the model. August is generally the main season for the appearance of
Table 2 Results of the regression analysis using the developed model for long-term behaviour of Parameter
leff C F1 F2 F3
Estimated value y1
0.10 year 300 Bq kgy1 406 Bq kgy1 609 Bq kgy1 1300 Bq kgy1
137
Cs in sheep ŽEq. Ž5..
95% conf.int.
R2
Estimated Teff " s.e.
Ž0.03, 0.17. Ž200, 390. Ž360, 450. Ž542, 677. Ž1160, 1440.
0.70
7.0" 2.6 year
Mid August Ž15th. was chosen as the time of fruit body appearance.
H. Mehli, L. Skuterud r The Science of the Total En¨ ironment 224 (1998) 9]17
15
Fig. 4. Estimated mean Ž`. 137 Cs activity concentration in sheep at Fonnasfjellet compared with the observed mean Žv., ˚ mean " standard error Žs.e.. of mean. The dot line shows the estimated decrease in 137 Cs activity concentrations in sheep due to decreasing contamination levels in vegetation. Time for appearance of fruit bodies was set to 15 August.
fungi in Norway, and the largest quantities of fruit bodies seemed to be found at the end of August and beginning of September at Elgvasshø. Thus it is difficult to estimate the exact time for fruit body appearance as an input to the model. Mid-August Ž15th. was chosen as the date of fruit body appearance, and also gives the best model fit. Regression analysis of Eq. Ž5. gave the ratios 1:1.5:3.2 between the three levels of fungal abundance Ž F1: F2 : F3 .. 5. The fact that the data set consists of measurements of both ewes and lambs adds another factor of uncertainty to the model. Since the data set mostly consists of only 10 measurements each year, dividing the data set into sub groups increases the uncertainty. However, since we are using the model to analyse the year to year changes in radiocaesium activity concentrations, the difference in biological half-lives between animals due to age was not thought to be of significance. This was also supported by analysis after dividing the data set into ewes and lambs and applying biological half-life values of 18 and 14 days ŽIAEA, 1994. respectively; the result-
ing model parameter values did not differ significantly between the groups. Therefore lambs and ewes were treated as one homogenous group in the data analysis. This also demonstrates that the variability in biological half-lives that exists between individual animals will be of little importance for the final model output. 6. Information about abundance of fungi in the observed grazing areas was adopted from the area of Elgvasshø, which is geographically separated from Fonnasfjellet. However, since ˚ the relative, not the absolute, amount of fungi is important in this model, and relative abundance is similar over large distances, the fungi information from Elgvasshø was assumed to be valid for the area of Fonnasfjellet as well. ˚ Additionally the two areas are ecologically and climatically similar. Abundance of fruit bodies at Elgvasshø was recorded at approximately the same time every year. This introduces some uncertainty in determining the amount of fungi available to sheep over the growing season because the timing of appearance and duration of fruit bodies changes from year to year. The classification of levels
16
H. Mehli, L. Skuterud r The Science of the Total En¨ ironment 224 (1998) 9]17
of fungi abundance was subjective and with no clear distinction between levels. A better approach might have been to quantify the number of fruit bodies per unit ground surface. 7. Ideally the model should also account for decreasing radiocaesium activity concentration in fruit bodies with time after the Chernobyl accident. However, evidence for the long-term behaviour of radiocaesium in different mushroom species is not unequivocal. A recent study suggests classification of mushrooms into three groups depending on their changes in radiocaesium activity concentrations with time; decreasing, increasing and with roughly constant concentrations ŽWirth et al., 1996.. For control the term eyl fu ngi t c was included in the last part of Eq. Ž5.. The regression analysis returned an insignificant lfungi and the possible decrease in fungi radiocaesium concentration levels was therefore ignored. In addition to the uncertainties introduced by the model assumptions, there are also considerable statistical uncertainties connected to the live monitoring data. Firstly, there is no statistically random selection of sheep to be monitored, nor control that they actually are representative of the grazing unit. Furthermore, a study of variability within two whole grazing units of about 200 sheep showed that the coefficient of variance was about 30% ŽMehli, 1996.. This implies that even if the monitored sheep were randomly selected, sampling only 10 sheep from a grazing unit of several hundred animals gives an inherent statistical uncertainty of about 20% in the estimated mean radiocaesium activity concentration ŽMehli, 1996.. Taking these factors into account, the obtained R 2 value was satisfactory for the developed model. The estimated 137 Cs activity concentration in 1987, which was a year with large amounts of fruit bodies Žalthough not as much as 1988., was high compared with the observed level. This may be due to soil complexation processes and the relatively short time after the fallout which may not have allowed much radiocaesium to move down
the soil profile for uptake and accumulation in vegetation and fungi ŽElster et al., 1987.. In particular 1988, but also 1991, were years with high fruit body abundance. The results suggest that 75]85% of the radiocaesium activity concentrations in sheep these years were due to ingested fungi. The rate of decrease in 137Cs activity concentrations in the environment will differ between areas, and earlier estimates of effective half lives for 137Cs in Norwegian sheep have indicated values in the range 3]20 years ŽStrand, 1994.. The value derived in this study was 7.0" 2.6 years when the influence of mushrooms is excluded. Fitting a simple exponential function to the data set returned a positive leff Ži.e. a negative half-life . and an R 2 of only 0.03. This clearly illustrates that using simple exponential functions alone in estimates of long-term behaviour have definite limitations when time since the contamination event is not the only important factor affecting the radiocaesium activity concentrations. There were several ways the data set could have been split to obtain a more exact model, for instance including more than three levels of fungi abundance. However, dividing the data set decreased the number of observations in each group and increased the uncertainties in the estimated mean values. Teff estimated from different model variants was not significantly different from the effective half-life given in Table 2. 4. Conclusions The suggested model appears to describe adequately the long-term behaviour of radiocaesium in sheep grazing unimproved pasture. Despite several assumptions and uncertainties, the observed and estimated values of radiocaesium activity concentrations in sheep showed good correlation with an R 2 of 0.70. The results support the hypothesis that fungal fruit bodies are important sources of radiocaesium for grazing sheep in Norway. The contribution from ingested fruit bodies was estimated to be 75]85% of the radiocaesium activity concentrations in sheep in 1988 and 1991 which were years with a high fruit body abundance. The esti-
H. Mehli, L. Skuterud r The Science of the Total En¨ ironment 224 (1998) 9]17
mated effective half-life for 137 Cs activity concentrations in sheep due to consumed vegetation in the studied grazing unit was 7.0" 2.6 years, but years with high fruit body abundance are likely to continue to result in more elevated radiocaesium activity concentrations in sheep in the future. Depending on the abundance of fruit bodies, the model suggests that the average 137 Cs concentration levels in the grazing unit will be 260]630 Bq kgy1 in 1998 Žpresumed 2 weeks grazing after appearance of fruit bodies.. The study demonstrates that using a simple exponential function in assessments of long-term consequences of radiocaesium fallout for grazing sheep may be inappropriate. Acknowledgements This study would not have been possible without access to the live monitoring files at the office of the County Veterinary in Hedmark, and the help by Johan Teige was highly appreciated. Of equal importance was the fungal fruit body abundance information kindly provided by Hans Myhre. We are also grateful to Professor Henning Omre, Norwegian University of Science and Technology, who provided valuable ideas during the initial phase of the model development. Thanks also go to Dr Brenda J. Howard at the Institute of Terrestrial Ecology ŽUK., and our colleagues Dr Per Strand, Dr Andrew I. Cooke and Dr Justin Brown at the Norwegian Radiation Protection Authority, for comments during the course of writing this paper. References Amundsen I, Gulden G, Strand P. Accumulation and long term behaviour of radiocaesium in Norwegian fungi. Sci Total Environ 1996;184:163]171. Backe S, Bjerke H, Rudjord AL, Ugletveit F. Deposition of caesium in Norway after the Chernobyl accident. Østeras, ˚ National Institute of Radiation Hygiene, Report 1986:5 Žin Norwegian.. Brynildsen LI, Strand P. A rapid method for the determination of radioactive caesium in live animals and carcasses, and its practical application in Norway after the Chernobyl accident. Acta Vet Scand 1994;35:401]408. Elster EF, Fink R, Holl ¨ W, Lengfelder E, Ziegler H. Natural and Chernobyl-caused radioactivity in mushrooms, mosses
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and soil-samples of defined biotopes in SW Bavaria. Oecologia 1987;73:553]558. Haselwandter K, Berreck M. Fungi as bioindicators of radiocaesium contamination: Pre- and post-Chernobyl activities. Trans Br Mycol Soc 1988;90:171]174. Haugen LE, Uhlen G. Transport av radionuklider i jord og opptak i planter og sopp. In: Garmo TH, Gunnerød TB, editors. Radioaktivt Nedfall fra Tsjernobyl-ulykken. Oslo: Norges Landbruksvitenskapelige Forskningsrad, ˚ 1992:43]64 Žin Norwegian.. Hove K, Pedersen Ø, Garmo T, Hansen HS, Staaland H. Fungi: a major source of radiocaesium contamination of grazing ruminants in Norway. Health Phys 1990;59:189]192. Hove K, Lonsjo ¨ ¨ H, Andersson I, Sormunen-Cristian R, Hansen HS, Indridason K, Joensen HP, Kossila V, Liken A, Magnusson S, Nielsen SP, Paasikallio A, Palsson SE, Rosen ´ ´ K, Selnæs T, Strand P, Vestergaard T. Radiocaesium transfer to grazing sheep in Nordic environments. In: Dahlgaard H, editor. Nordic Radioecology. Amsterdam: Elsevier, 1994:211]228. IAEA: Guidelines for agricultural countermeasures following an accidental release of radionuclides. Technical Reports Series No 363. Vienna: International Atomic Energy Agency, 1994. Johnson W, Nayfield CL. Elevated levels of cesium-137 in common mushrooms ŽAgaricaceae. with possible relationship to high levels of cesium-137 in whitetail deer, 1968]1969. Radiol Health Data Rep 1970;11:527]531. Kammerer L, Heirsche L, Wirth E. Uptake of radiocaesium by different species of mushrooms. J Environ Radioact 1994;23:135]150. Mehli H. Radiocaesium in grazing sheep. Østeras, ˚ Norwegian Radiation Protection Authority, StralevernRapport 1996:2. ˚ Olsen R. The transfer of radiocaesium from soil to plants and fungi in seminatural ecosystems. In: Dahlgaard H, editor. Nordic Radioecology. Amsterdam: Elsevier, 1994:265]286. Rosen ´ K, Andersson I, Lonsjo ¨ ¨ H. Transfer of radiocaesium from soil to vegetation and to grazing lambs in a mountain area in Northern Sweden. J Environ Radioact 1995;26: 237]257. Skuterud L, Travnikova IG, Balonov MI, Strand P, Howard BJ. Contribution of fungi to radiocaesium intake by rural populations in Russia. Sci Total Environ 1997;193:237]242. Strand P. Radioactive fallout in Norway from the Chernobyl accident. Østeras, ˚ Norwegian Radiation Protection Authority, NRPA Report 1994:2. Warren JT, Mysterud I. Fungi in the diet of domestic sheep. Rangelands 1991;13:168]171. Wirth E, Ruhm W, Kammerer L, Steiner M. Model for ¨ predicting future cesium-137 contamination in fungi. In: Amiro B, Avadhanula R, Johansson G, Larsson C-M, Luning M, editors. Protection of the Natural Environment. ¨ Proceedings of the International Symposium on Ionising Radiation. The Swedish Radiation Protection Institute and The Atomic Energy Control Board of Canada. Stockholm, May 20]24, 1996:176]187.