The radioactive fallout from the Chernobyl accident in 1986 contaminated parts of the boreal forest ecosystems in Sweden, and we report on the activity concentration of radiocaesium 137Cs in the meat of moose Alces alces caught in the county of Västerbotten in north-Sweden during 1986–1996. Countywide, the geographic distribution patterns of 137Cs activity in moose muscle were similar in 1986 and 1993. The underlying relationship between 137Cs concentration in moose muscle and ground deposition remained significant for all years, but the proportion of variation explained by this relationship was variable and low in most years. The transfer rate of 137Cs to moose underwent marked annual fluctuations that appear to be synchronous over large areas. The fluctuations in the uptake of 137Cs by moose most probably result from variations in food selection or shifts in habitats. The transfer rate of 137Cs to moose seems to be higher in coastal areas than in inland areas. The 137Cs activity in moose was considerably higher in 1993 than should be expected from a simple decay model based on original deposition data and the 137Cs levels in moose meat from 1986. The large temporal variations in transfer rate make future predictions of transfer to moose and man unreliable. We found that the annual hunting of moose is a major source of 137Cs transfer to man in this region.
Wild animals are threatened by airborne pollution in many parts of the world. Various types of contaminants, such as organic compounds, heavy metals and radionuclides, are spread over large distances and incorporated into remote food webs (AMAP 1997). This was especially evident after the Chernobyl nuclear accident in Ukraine in April 1986 which led to subsequent contamination of forest products in many parts of Europe (Savchenko 1995).
Northeastern Sweden was among the areas in Europe that received large amounts of nuclear fallout after the explosion of the reactor at Chernobyl. Subsequent contamination of plants and wildlife, such as moose Alces alces became of public concern, and a program to measure the spatial distribution of the fallout and to follow changes in contamination over time in animal populations was established. The forest ecosystem was severely contaminated by radiocaesium 137Cs fallout, and the activity concentrations in moose follow that pattern (Danell, Nelin & Wickman 1989, Bergman, Palo, Nylén & Nelin 1994). This radioactive isotope has a physical half-life of 30 years, and its turnover in the Scandinavian boreal forest is slow and largely determined by the radioactive decay (Edvardsson 1991, Moberg, Hubbard, Avila, Wallberg, Feoli, Scimone, Milesi, Mayes, Iason, Rantavaara, Vetikko, Bergman, Nylén, Palo, White, Ratio, Aro, Kaunisto & Guillitte 1999).
The moose is an important species for hunters in Sweden. In 1986, about 135,000 animals were shot making moose meat a potential major source of radionuclide transfer to man (Johansson, Bergström, Eriksson & Erixon 1994). About 40% of the moose in Sweden were shot in areas contaminated by fallout from Chernobyl (Swedish Association for Hunting, Uppsala).
Annual surveys of moose muscle samples have revealed large temporal variations in the activity concentration of 137Cs in moose (Palo, Nelin, Nylén & Wickman 1991, Nelin 1995, Palo & Wallin 1996). This variation is puzzling since activity concentrations in major food plants declined during the same period, and the physical half-life of the isotope would be expected to reduce levels by approximately 2.5% per year (Nelin 1994).
More than a decade after the Chernobyl accident, the amount of 137Cs which leaves the forest ecosystem by runoff is negligible (Nylén 1996). A major decline of 70% in the activity concentration was observed in boreal plants from 1986 to 1997, except in pine Pinus sylvestris, and mineral soils showed a slight increase over time (Moberg et al. 1999, Rosén, Öborn & Lönsjö 1999). If 137Cs is transferred to the moose in a simple direct manner and does not accumulate in the muscle, the 137Cs activity concentration in moose meat should decline with time at a similar rate as physical decay. From this relationship we assume that the aggregated transfer factor (AGTF) of 137Cs to moose would remain fairly constant over time. However, several other factors related to the foraging behaviour at larger scales, e.g. as habitat use, may cause significant temporal and spatial variations in the 137Cs intake by moose to a point at which a simple correlation with deposition and decay is masked (Palo & Wallin 1996).
Numbers of sampled moose and moose shot, meat yield and transfer of radiocaesium 137Cs to man in the county of Västerbotten during 1986–1990 and 1991–1996. Data on the number of moose shot were provided by the Swedish Association for Hunting (SJF).
We present data on the temporal variation in the 137Cs content in moose populations in Västerbotten over 11 years as related to variations in ground deposition and hunting. The magnitude of transfer to the hunters guild is discussed, as this is an important pathway for the transfer of 137Cs to man.
Material and methods
Moose muscle samples
Our study is based on the following three data sets that were combined in spatial and temporal analyses: 1) samples of moose muscle collected annually by hunters in September, 2) ground deposition of 137Cs recorded in 1986 following the Chernobyl accident (SGAB 1987) and 3) numbers of moose taken each year by the hunters.
During 1986–1996, a total of 7,540 moose muscle samples were collected in 6–15 districts of the county of Västerbotten. In 1995 and 1996, however, samples were obtained from only one district (Robertfors; Table 1). Sweden is divided into counties (län), which are subdivided into districts (kommun) and parishes (församling), respectively.
In 1986 and 1993, a higher spatial resolution of samples enabled analyses for most parishes within the county (see Table 1). The samples from these years were obtained from 41 and 50 out of the 54 parishes, respectively. The sample collection in 1986 included 1,899 males, 1,822 females and 266 animals of unknown sex. In 1993,590 males, 612 females and 21 of unknown sex were sampled. In other years, animals could only be located to districts. A complete time series for 1986–1994 was obtained for three districts only, Wilhelmina, Lycksele and Robertsfors. All muscle samples (100 g) were measured for 137Cs for 1–10 minutes in a Na-I-detector, giving a measurement error margin of less than 10% (Danell et al. 1989, Palo et al. 1991).
In 1986, the location from which a sample was taken was referenced to a 25 × 25 km grid covering the county of Västerbotten; in the later years samples were attributed to the nearest town or landmark. All grids in a parish were used for calculation of the mean and standard deviation of the activity concentration for 1986 and 1993 using Arcview (Version 3.2, Spatial Analyst 2.0, ESRI Inc. Redlands, Ca., USA).
Ground deposition of 137Cs following the Chernobyl accident, Ag(86) is the integrated gamma emission of 137Cs per m2, for each grid location was estimated from a deposition map (SGAB 1987). The mean values for each district and parish were obtained in the same way as the moose muscle activity. For each year (i) an expected ground deposition, Ag(i) was derived from Ag(86) assuming physical decay and corrected AGTF (m2kg-1) calculated for each year according to Ag(i) = Ag exp-0,023 *T, where T is time in years since 1986. The aggregated transfer factor (AGTF), which reflects the rate of transfer of 137Cs to moose, was also derived for each district and parish. AGTF is the quotientBréchignac, Moberg & Soumela 2000).
Numbers of moose taken
Numbers of moose shot were supplied for each parish by the Swedish Association for Hunting (Svenska Jägare-förbundet, SJF). Hunting success was calculated as the proportion of animals shot in relation to the number of animals allowed on the individual hunting permits. Transfer of 137Cs to man was calculated based on average meat mass available for consumption in the county of Västerbotten and was taken to be 120 kg per adult male moose, 90 kg per female and 30 kg per calf.
All statistical analyses were undertaken using Minitab 13.31. Heteroscedacity was reduced by logarithmic transformation.
Concentrations of 137Cs in moose muscle, Am(i), showed a distinct geographic variation among parishes and districts, being highest in the southeastern region in both 1986 and 1993 (Fig. 1). Notably, the 137Cs values in moose muscle were lower just after the accident in 1986 than in 1993. The geographic correspondance of 137Cs concentration in moose muscle with the ground deposition was significant, but weak in most years. The slopes of the regressions of 137Cs (Am(i)) against ground deposition (Ag(i)) were significant for all years. However, except for one year, the regressions explained less than 30% of the variation in 137Cs (Table 2). A clear geographic pattern was also seen in the aggregated transfer factor with higher transfer rates at coastal areas than in western and central districts (ANOVA: F = 8.297, df = 2, P < 0.002, r2 = 0.601; see Figs. 1 and 2).
Regressions of radiocaesium 137Cs vs ground deposition for the years 1986–1994.
The mean aggregated transfer factor (AGTF) for the three selected districts of the county of Västerbotten fluctuated markedly over time (see Fig. 2), and the fluctuations were most prominent in the Robertsfors district where the highest average (1993) was about six times higher than the lowest average (1987). Statistical analysis of AGTF for all districts for the period 1987–1994 showed that all years except 1987 were significantly different from 1986 (ANOVA: F = 110.91, df = 7, P = 0.0001). In 1989 and 1994, the AGTF was slightly lower than in 1986, whereas it was higher in the remaining years (Tukey's post hoc tests).
The AGTF time series data from the three districts appear to show synchronous fluctuations (see Fig. 2). We tested this by correlation analyses of mean annual AGTF levels for the period 1986–1994, but found that only the Wilhelmina and Lycksele districts gave significant correlations. Although fluctuations tended to mask time trends, we found a slight overall increase in the AGTF with time (Log AGTF = 0.077X-150.8, P < 0.0001, df = l,r2 = 0.055.
We specifically tested if the distribution of AGTF values within the county of Västerbotten in 1986 would serve as a predictor of the observed distribution in 1993 when corrected for physical decay of 137Cs. The predicted frequency distribution using 1986 data corrected for decay and the observed distribution in 1993 was significantly different (Test for goodness of fit: X2 - 206, df = 21, P < 0.0001). Although the distribution of AGTF in 1986 and 1993 correlated significantly (F = 7.17, df = 13, R2 = 0.37, P < 0.02) the latter year showed a considerably higher AGTF than predicted from the AGTF in 1986 (Fig. 3).
We combined data for the amount of 137Cs transferred from moose to the hunter guild in the periods 1986–1990 and 1991–1996, and found no statistical difference between them (t-test: t = 1.48, df = 9, P = 0.172). We estimated that the transfer to man from one single source, i.e. the moose, is slightly higher (1,180 Bq.person-1.year-1;SD = 633) than intake from commercial food products (estimated to be 811 Bq.person-1. year-1 in Västerbotten; L. Moberg, Swedish Radiation Protection Institute, Stockholm, pers. comm.). We estimated that 3.3 × 109 Bq has been transferred to the hunters guild since 1986, giving an average intake of 12,660 Bq.hunter-1.year-1 (SD = 7,119) which corresponds to a concentration of 181 Bq.kg-1.
On a large geographical scale, the 137Cs activity in moose muscle correlated with ground deposition, a pattern that is largely retained seven years after the fallout. Although significant, the explanatory power of this relationship was low. Looked at in more detail, the 137Cs activity in moose muscle did not follow a simple decay pattern through time nor can it be fully explained from the amount of deposition from Chernobyl over the landscape.
Discrepancies from the above expectations are most likely to be found in the variable rates of uptake and this is why we preferred to analyse the AGTF. These analyses revealed interesting patterns. First, the AGTF was higher in the eastern coastal areas than in the western and central districts. Second, the AGTF underwent marked annual fluctuations that to some extent were synchronous in three districs. Third, the AGTF showed a slightly increasing trend with time.
The reason for lower transfer rates of inland districts is unclear. It might be a result of the earlier onset of winter in this region and thus an earlier shift to winter diet, but such a shift would lead to lower levels and lower variability of AGTF in these locations than in the eastern coastal regions. Moose have lower 137Cs activity in winter than in other seasons (Nelin 1994). The AGTF appears to fluctuate synchronously in the three districts which suggests that the same influencing factor(s) may operate over large areas. However, longer time series are needed to elucidate whether these shifts are extended over large geographical areas. On the scale of single parishes or districts, the annual fluctuations in AGTF may be caused by various ecological factors. Most probably, this relates to differences in moose foraging behaviour, e.g. differences in food selection or habitat use. Major shifts in habitat use by moose have been reported from Norwegian studies (Bo & Hjeljord 1991) and were discussed theoretically by Palo & Wallin (1996). Given the fact that forest habitats generally show higher contamination than open habitats (Palo 1994), it can be envisaged how temporal changes in 137Cs uptake by moose could result from habitat shifts: in some years the moose may prefer foraging in forests whereas in other years they would shift to more open habitats (Bo & Hjeljord 1991). That we found a general relationship between body burden of 137Cs and ground deposition with different means in AGTF among years, may be in favour of the habitat shift hypothesis. Another factor that could theoretically induce annual variations in the transfer of 137Cs to moose is the changing availability of fungi between years. If consumed by moose in significant quantities, fungi can increase both transfer rate and activity concentration (Avila 1998, Moberg et al. 1999). Such an intake is unpredictable in time and space. However, mushrooms have not been found to be common in the diet of moose from analysis of rumen contents during 1986–1989 (Palo et al. 1991, Palo & Wallin 1996). It is clear that the simple assumption of constant AGTF does not hold for the time period studied. Given that the decay of 137Cs is a very deterministic process, the fluctuations seen in AGTF can only be explained by varied annual uptake of 137Cs by the moose. This variation makes it very difficult to predict with any accuracy near future levels of 137Cs in the moose population.
We can only speculate about the reason for the slight but significant increase in available AGTF in the study period, but possible explanations are: i) uptake through roots may have increased the levels of 137Cs in plants with time, and ii) in 1986 a major part of the deposition was large particles that were not immediately available in the food webs. This particle-bound deposition has with time released more 137Cs into circulation. The first explanation seems less probable since no increase in activity concentration in major food plants of moose has been detected (Nylén 1996, Moberg et al. 1999). Even though the increase in AGTF with time is not detected in some selected food plants, it is possible that the foraging pattern of moose integrate and magnify such small changes over a larger area. In order to understand variation of radiocaesium transfer in food webs and subsequent transfer to man, both animal behaviour in relation to food resources and human behaviour in relation to hunting and meat consumption must be studied in more detail than hitherto.
Although the data presented here cover more than a decade after the Chernobyl accident, a high transfer to man from a natural ecosystem is still possible through the consumption of meat from game. The average Swedish population is estimated to receive about 4,000 Bq. person-1.year-1 from forest products, i.e. berries, fungi, reindeer meat (excluding meat from game) and fish (Strand, Balanov, Aakrog, Bewers, Howard, Salo & Tsatsov 1997). The absorbed dose equivalent is measured in Sievert (Sv) and gives the radiation dose weighted by coefficients that reflect the capacity to harm biological tissues. The dose conversion factor is 2.5 μSv y-1 Bq.kg-1 which gives the effective annual dose in man by consuming moose meat to be 0.45 mSv (UNSCEAR 1988). It is estimated, that an extra dose of 10 mSv of radiation will increase the risk of dying from cancer by 0.05% (UNSCEAR 1988). In this perspective, the contribution from moose is negligible. However, 137Cs transfer from moose is considerably higher than from any other single source previously estimated from forest products, and moose hunters receive doses of the same magnitude as reindeer herders and fishermen in Scandinavian fallout areas (Strand et al. 1997, Mehli, Skuterud, Mosdöl & Tönnessen 2000).
the hunters of Västerbotten kindly provided muscle samples of moose, and Dr. Göran Wickman, Dr. Lennart Johansson and Sara Gunnare skilfully measured 137Cs at the Department of Radiophysics, Umeϵ University. Dr. Per Nelin helped with handling of data, and Peter Sunesson provided the hunting statistics. Dr. R. Bergman and two anonymous reviewers gave valuable suggestions. The associate editor is acknowledged for extensive comments and his patience with the preparation of this manuscript. This work was supported by the Swedish Radiation Protection Institute and the EU 4th framework programme.