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Seasonal variation in radiocaesium concentration in willow ptarmigan and rock ptarmigan in central Norway after the chernobyl fallout
J. Environ. Radioactivity, Vol. 41, No. 1, pp. 65—81, 1998 ( 1998 Elsevier Science Ltd. All rights reserved Printed in Great Britain PII: S0265-931X(97)00095—7 0265-931X/98 $19.00#0.00
Seasonal Variation in Radiocaesium Concentration in Willow Ptarmigan and Rock Ptarmigan in Central Norway after the Chernobyl Fallout Hans Chr. Pedersen,a Signe Nyb+b & Per Varskogc a Norwegian Institute for Nature Research, Dep. of Terrestrial Ecology, Tungasletta 2, N-7005 Trondheim, Norway b ALLFORSK, Dep. of Ecotoxicology, Norwegian University of Science and Technology, Gryta 2, N-7010 Trondheim, Norway c Institute for Energy Technology, P.O. Box 40, N-2007 Kjeller, Norway (Received 20 May 1996; accepted 22 October 1997)
ABS¹RAC¹ Radioactive caesium (20—60 kBq m~2) was deposited after the Chernobyl accident in the mountains of central Norway. ¹wo sympatric ptarmigan species, willow ptarmigan Lagopus lagopus and rock ptarmigan L. mutus, inhabit this alpine ecosystem and are important game species. In 1987 and 1988, a study was carried out to try to identify factors affecting radioactive caesium concentration in these birds. Juvenile willow ptarmigan contained more radiocaesium than adults, but the two sexes did not differ in radiocaesium concentration. ¹he radiocaesium concentration of food plants correlated with radiocaesium concentration of rock ptarmigan, and a seasonal variation in radiocaesium concentration of both ptarmigan species was seen. Rock ptarmigan contained more radiocaesium than willow ptarmigan during winter, but not in summer. ¹his difference was related to differences in diet. ¹he bioconcentration factor was 0)4—0)6. ¹he aggregated transfer coefficient was 0)003—0)009 m2 kg~1 for both species. In spite of the high deposition, the radiocaesium concentration in muscle rarely exceeded the limit recommended for human food consumption (600 Bq kg~1). ( 1998 Elsevier Science ¸td. All rights reserved
INTRODUCTION The fallout after the reactor accident of Chernobyl in April 1986 exposed several northern ecosystems to radionuclides (Medvedev, 1986; Webb et al., 65
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1986). In central Norway the major deposition was in the form of fuel or condensed particles (Salbu and Bj+rnstad, 1992), and consisted mainly of radiocaesium 134Cs and 137Cs (Lindahl and Has rbrekke, 1986). Alpine areas were contaminated and research conducted to understand contamination mechanisms of important aquatic and terrestrial ecosystems (Gaare et al., 1991). Until the Chernobyl accident, most studies of radiocaesium contamination in food chains have involved continuous release of fission by-products from power production reactors (e.g. Anderson et al., 1973; Brisbin, 1991), or from above ground nuclear weapon tests. Here we present a study of radiocaesium (137Cs) in willow ptarmigan (¸agopus lagopus), rock ptarmigan (¸agopus mutus) and their main food plants, in Dovrefjell, Norway. The objective of the study is to elucidate the factors affecting transfer of radiocaesium among trophic levels and accumulation of radiocaesium in ptarmigan throughout the year. Dovrefjell mountain area was heavily contaminated by the Chernobyl accident (Lindahl and Ha> brekke, 1986). The ptarmigan are the only two resident herbivore avian species inhabiting the alpine area throughout the year, being one of the keystone species in the alpine ecosystem. Furthermore, ptarmigan is the most important small game in Norway, involving 100 000 hunters annually harvesting 500 000—750 000 birds. Thus ptarmigan could be a source of transfer of radiocaesium to protected avian predators such as gyrfalcon (Falco rusticolus) as well as humans. Earlier studies have shown that accumulation and excretion of radionuclids in wild animals depend on factors such as contamination level in different habitats, food choice, tropic level, age and several physiological features (Reichele et al., 1970; Il’enko, 1973; Straney et al., 1975). The diet of both ptarmigan species varies throughout the year. As different plants were expected to differ in their accumulation rate of radiocaesium, it was predicted that ptarmigan would have a seasonal variation in contamination level. Furthermore, a different accumulation pattern was predicted in juveniles compared to adult birds because of differences in physiology and diet. To evaluate possible accumulation in the food chain involving ptarmigan species the calculation of the bioconcentration factor (BCF"radiocaesium concentration in birds/radiocaesium concentration in food) is important. BCF in herbivore mammals is lower than in carnivore mammals (Reichele et al., 1970; Kitchings et al., 1975), but so far few studies in birds have been reported (e.g. Lowe and Horrill, 1991; Kas las s et al., 1994; Moss and Horrill, 1996). By comparing radiocaesium concentration in ptarmigan and their food plants, BCF could be calculated.
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In the study area the deposition of radiocaesium increased with altitude (Gaare, 1987). The two ptarmigan species share the alpine habitat, but overlap only in the border between the low-alpine and middle-alpine zone. Hence we hypothesized that rock ptarmigan inhabiting the uppermost zone would have a higher radiocaesium concentration than willow ptarmigan.
MATERIALS AND METHODS Study area The study was carried out in Knutsh+, Dovrefjell National Park, in central Norway (62°17@N, 9°39@E) from 1987 to 1988. The study area measured 10 km2, covering the sub-, low- and middle-alpine zone (950—1690 m asl). Bedrock consisted mostly of phyllitic mica schist and green schist from the Upper Ordovicium, giving rise to mineral-rich soil (Heim, 1971), and thus a rich flora. The study area has been described in detail by Pedersen et al. (1983) and L+faldli et al. (1992). Total deposition of 134Cs and 137Cs in the area during May 1986 was estimated to be from 20 to 60 kBq m~2 (Bretten, 1991). Sampling of ptarmigan and vegetation Willow ptarmigan were collected from May 1987 to December 1988 (n"122). Rock ptarmigan were collected from March 1987 to September 1988 (n"37). Both years, birds were collected monthly from May throughout October, while in winter (November throughout April) birds were collected only once. All birds were collected by shooting and weight, sex and age were determined (e.g. Bergerud et al., 1963). Samples were taken from the breast muscle in both ptarmigan species and radiocaesium concentration was measured on a wet weight basis. In rock ptarmigan the crop content was sorted into plant species and thus the relative importance of food plants was determined. Based on the composition of crop content vegetation samples were collected in the same general area as the birds were shot. Vegetation samples and samples of crop content were dried in an oven at 70°C for 24 h. The relative proportion of different plant species in each crop was measured on dry weight basis. The radiocaesium concentration of each crop was estimated using the relative content of each plant species in the crop and the mean radiocaesium concentration of the relevant species collected at the same time. The most important food plants of willow ptarmigan are well known from earlier studies (Myrberget, 1979; Spids+, 1980), conducted in the same study area
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(Pedersen et al., 1983; Steen et al., 1985; Pedersen, unpublished). In parallel with sampling of willow ptarmigan, collection of important food plants was carried out (Bretten, 1989). To allow for calculation of a bioconcentration factor crops were collected from 18 willow ptarmigan and radiocaesium concentration analysed. In 20 individual rock ptarmigan radiocaesium concentration was analysed both on wet and dry weight basis. Breast muscle was dried in an oven at 70°C for at least 24 h. Calculations of bioconcentration factors (BCF) in rock ptarmigan were based on the relationship between radiocaesium concentration in dried breast muscle and radiocaesium concentration in the crop from the same bird. As all plant material was measured on dry weight basis and some ptarmigan muscle tissue on wet weight basis, a correction factor had to be calculated. The correction factor was calculated from c "c ) k, (1) $85 885 where c denotes concentration of radiocaesium in dried pectoral muscle $85 (Bq kg~1), c denotes concentration of radiocaesium in fresh pectoral 885 muscle (Bq kg~1) and k is the correction factor. The correction factor was 3.59 and was used for both ptarmigan species. BCF was then calculated from BCF"c ) k/c , (2) 885 #301 where c denotes radiocaesium concentration in crop (Bq kg~1). The #301 transfer coefficient (F ) given by Ward and Johnson (1986) deviates from the & BCF in that it takes into account daily food intake ( f ) (kg day~1) and that $ the concentration of radiocaesium (Bq kg~1) is measured in fresh muscle (3): F "c /c ) f . (3) & 885 #301 $ The aggregated transfer coefficient (¹ ) for 137Cs was calculated as given !' by Howard et al. (1986): ¹ "c /depositon, !' 885 where deposition is acitivity per unit area (Bq m~2).
(4)
Measurement of radiocaesium activity Total radiocaesium (134Cs#137Cs) in the samples was determined at the Isotope laboratory, Norwegian University of Science and Technology, Trondheim, using two 3]3 In. NaI well detectors (active volume 23)5 cm3). The samples were placed in plastic or glass containers of known geometry and gross counts (corrected for background) in a 460—932 keV window
Seasonal variation in radiocaesium concentration
69
were collected. The detectors were regularly re-calibrated using standards consisting of samples of lichen contaminated by the Chernobyl accident and packed in the same type of containers as the ordinary samples. This calibration routine automatically compensates for the change in 137Cs : 134Cs ratio with time. Differences in sample volume (i.e. the sample container fill height) were adjusted for according to correction functions specific for each NaI detector. The measured activity concentrations were not adjusted for eventual differences in sample density. No significant self-absorption was likely to occur at the used energy interval for the type of material in question. Calculations of 137Cs derived from determinations of the total radiocaesium were based on the 137Cs : 134Cs ratio determined at the Isotope laboratory, Trondheim. The ratio is based on samples of vegetation taken and counted the first few days after the Chernobyl accident, and was determined as 1)86 (SD"0)06, n"32, time adjusted to May 15, 1986) (Varskog et al., 1994). 137Cs thus accounted for 65% of the initial radiocaesium activity. Radiocaesium values were determined as Bq kg~1 dry weight for vegetation and crop samples, and both Bq kg~1 dry weight and Bq kg~1 wet weight for ptarmigan samples. For radiocaesium determinations below the detection limit (approximately 10% of the samples) 0)5]detection limit was used. The detection limit depends on the activity of the samples and its weight, and was between 20—40 Bq kg~1. Statistical procedures To examine differences in radiocaesium concentration in breast muscle between two groups of data such as sex, age, months, seasons, and species, we used Mann—Whitney tests (corrected for ties). We used Kruskal—Wallis tests (corrected for ties) to examine differences among months. To examine the relationship between radiocaesium concentration in rock ptarmigan breast muscle and calculated concentration in the diet we used a Spearman’s rank correlation test. All statistical tests present two-tailed p-values. Differences were considered significant when p-values were less than 0)05.
RESULTS No significant difference was found in radiocaesium concentration between male and female willow ptarmigan within months either in 1987 or 1988 (Mann—Whitney U-tests, p'0)05). In the further analyses the material from both sexes are therefore pooled. In rock ptarmigan the material was too limited to carry out a similar test. However, based on result from willow ptarmigan, we decided also to pool data from rock ptarmigan.
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A comparison of radiocaesium concentration in adult and juvenile willow ptarmigan from August and September 1987 indicated that juveniles had higher levels of radiocaesium than adults in August, although not significantly so (x"108)25 and x"83, 50, respectively, Mann—Whitney test, Z"1)70, n "4, n "12, p(0)10), but not in September (x"109)09 1 2 and x"102)67, respectively, Mann—Whitney test, Z"1)01, n "3, 1 n "11, p'0)10). In 1988 a significantly higher radiocaesium concentra2 tion was found in juveniles compared to adult willow ptarmigan in July (Mann—Whitney test, Z"1)94, n "3, n "5, p"0)05) and August 1 2 (Mann—Whitney test, Z"2)05, n "2, n "7, p(0)05) (Fig. 1). In Sep1 2 tember, juveniles still had higher radiocaesium concentration than adults but not significantly so (Mann—Whitney test, Z"1)73, n "6, n "10, 1 2 p(0)10). Neither in 1987 nor 1988 was any significant difference found in radiocaesium concentration in juvenile and adult willow ptarmigan from October to June (Mann—Whitney tests, p'0)05). During this period all birds were called ‘‘adults’’. The radiocaesium concentration of juvenile willow ptarmigan during July—October, 1987 and 1988 is shown in Fig. 2. In 1987 the radiocaesium concentration did not show any significant difference among months (Kruskal—Wallis test, H"4)13, n"25, DF"2, p'0)05). However, in 1988 a significant variation was found among months in radiocaesium concentration in juvenile willow ptarmigan (Kruskal—Wallis test, H"14)98, n"25, DF"3, p(0)01). In both years a reduction in radiocaesium concentration was observed from August/September to October (Fig. 2),
Fig. 1. Radiocaesium concentration (Bq kg~1 wet weight) in breast muscle of juvenile and adult willow ptarmigan collected at Dovrefjell in 1988. Radiocaesium concentration given as median values. N—number of birds. *—statistically significant difference.
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Fig. 2. Radiocaesium concentration (Bq kg~1 wet weight) in breast muscle of juvenile willow ptarmigan collected at Dovrefjell in 1987 and 1988. Radiocaesium concentration given as median values. N— number of birds.
but this reduction was only significant in 1988 (Mann—Whitney tests, p(0)05). A general pattern in accumulation of radiocaesium in adult willow ptarmigan was indicated in 1987 and 1988; a gradual increase in radiocaesium concentration is observed from May reaching a peak in September. From October onwards a decline in radiocaesium concentration was observed, reaching a low winter level in December which lasts until next spring (Fig. 3). In 1987, the radiocaesium concentration varied among months although not significantly so (Kruskal—Wallis test, H"12)04, n"39, DF"7, p"0)10). However, radiocaesium concentration of birds collected in December was significantly lower than birds collected from May to October (Mann—Whitney tests, p(0)05). During 1988 a significant variation was found among months in radiocaesium concentration in adult willow ptarmigan (Kruskal—Wallis test, H"26)20, n"44, DF"7, p(0)001). As in 1987, the December values was low, but not significantly lower than in other months (Mann—Whitney tests, p'0)05). In both years the highest radiocaesium concentration was found in willow ptarmigan collected in September (Fig. 3). Radiocaesium concentration in adult willow ptarmigan and rock ptarmigan did not differ within months from May to August 1987 (Mann— Whitney tests, p'0)05). However, during winter the radiocaesium concentration in the two ptarmigan species differed. Rock ptarmigan collected in midwinter 1987-1988 (January/February -1988) had significantly higher radiocaesium concentration than willow ptarmigan (December-1987)
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Fig. 3. Radiocaesium concentration (Bq kg~1 wet weight) in breast muscle of adult willow ptarmigan collected at Dovrefjell in 1987 and 1988. Radiocaesium conentration given as median values. N— number of birds.
Fig. 4. Radiocaesium concentration (Bq kg~1 wet weight) in breast muscle of adult rock ptarmigan collected at Dovrefjell in 1987 and 1988. Radicaesium conentration given as median values. N— number of birds.
(Mann—Whitney test, Z"2)74, n "5, n "6, p(0)01). Also in March 1 2 1988 rock ptarmigan had higher radiocaesium concentration than willow ptarmigan (Mann—Whitney test, Z"2)60, n "4, n "6, p(0)01). 1 2 In adult rock ptarmigan a significant variation was found in radiocaesium concentration among months in 1987 (Fig. 4) (Kruskal—Wallis test, H"12)11, n"24, DF"5, p(0)05). Rock ptarmigan collected in midwinter 1988 (February) had significantly lower radiocaesium concentration than birds collected during autumn (September 1987) and in late winter (March 1987) and early spring (May 1988) (Mann—Whitney tests, p(0)05). Contrary to findings in adult willow ptarmigan, the radiocaesium concentration in rock ptarmigan was significantly lower in August compared to all other months (Mann—Whitney tests, p(0)05). Thus the radiocaesium concentration in rock ptarmigan was lowest in summer and midwinter with peaks in autumn and spring. A significant positive correlation was found in radiocaesium concentration in rock ptarmigan and that calculated in the diet (Fig. 5) (Spearman
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Fig. 5. Radiocaesium concentration in the diet (Bq kg~1 dry weight) in relation to breast muscle (Bq kg~1 wet weight) of rock ptarmigan.
rank correlation test, r "0)57, n"18, p"0)007). Examination of crops S from collected rock ptarmigan showed that they were mainly eating dwarf birch (Betula nana), salix (Salix spp. ), crowberry (Empetrum hermaphroditum), cowberry (»accinium vitis-idaea) and leaves of the herb Dryas octopetala in winter. As snowmelt progressed during spring the rock ptarmigan shifted towards small willow species in their diet (Fig. 6). In May 1988 the snowcover was almost complete until 10 May and all the birds were collected before this date. This is reflected in the more winterlike diet in May 1988 compared to May 1987 (Fig. 6). As the snow melted small willows such as S. herbacea/polaris were uncovered, and these small willows were the major constituents of the diet before the availability of herbs increased (Fig. 6). Herbs were preferred during summer until their availability was reduced in autumn. Before the snow accumulated in the autumn small willows were again the preferred food plants (Fig. 6). The vegetation samples were grouped in three; winter 1987; summer 1987 (June—August); and winter 1988 (Table 1). There were no difference in radiocaesium concentration among different plant species during winter 1987 (Kruskal—Wallis test, H"3)80, n"13, DF"4, p"0)43). However, during winter 1988 such a difference was found (Kruskal—Wallis test, H"11)25, n"27, DF"3, p"0)01). The radiocaesium concentration of willow shrubs Salix spp. was significantly lower than in the other food plants e.g. Betula nana, Empetrum hermaphroditum and »accinium vitisidaea (Table 1). »accinium vitis-idaea had significantly higher radiocaesium concentration than Salix spp. and Empetrum hermaphroditum (Table 1). From winter 1987 to winter 1988, the radiocaesium concentration
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Fig. 6. Proportion of different food plants in crops of rock ptarmigan from Dovrefjell collected in 1987 and 1988 based on amount of dry matter in crops. The different food plants are grouped into 5 categories; (1) Small willows, mainly Salix herbacea, S. polaris and S. reticulata; (2) Shrub, maily Betula nana and larger Salix species; (3) »accinium vitis-idaea and Empetrum hermaphroditum; (4) Herbs, several species but during winter/spring mainly Dryas octopetala and during summer/autumn mainly Bistorta vivipara; (5) Other plant material; unidentified crop-content, mainly mosses, lichen or dead plant material.
decreased significantly in Salix shrubs and leaves of Empetrum hermaphroditum, but not in twigs/buds of Betula nana (Table 1). During the summer 1987 there were no significant differences in radiocaesium concentration among food plant species (Kruskal—Wallis test, H"1)89, n"21, DF"3, p "0)60). For small willows which are one of the major constituents of the diet during spring and autumn (Fig. 6), some additional sampling was done in spring (May) and autumn (September/October). The radiocaesium concentration of small willows varied significantly among seasons (Kruskal—Wallis test, H"8)35, n"21, DF"2, p"0)015), with lower levels in summer (median"841, range"130—1363 Bq kg~1, n"10) than in spring (median"1138, range"910—1691 Bq kg~1, n"8) (Mann—Whitney test, Z"!2)69, n "8, n "10, p"0)007) and autumn (median"1266, 1 2 range"968—1678 Bq kg~1, n"3) (Mann—Whitney test, Z"!1)86, n "10, n "3, p"0)06). The radiocaesium concentration of small willows 1 2 did not differ between spring and autumn (Mann—Whitney test, Z"!0)21, n "8, n "3, p"0)84). 1 2 Based on radiocaesium concentration in crops and muscle samples from rock ptarmigan an average bioconcentration factor (BCF) was calculated to be 0)41 (SD"0)14, n"18). No difference was found in BCF between juvenile and adult willow ptarmigan (Mann—Whitney test, p'0)05) and data from age groups were pooled. Average BCF in willow ptarmigan was
Plant species
Betula nana, twigs/buds Salix spp., shrubs, twigs/buds* Empetrum hermaphroditum* »accinium vitis-idaea, leaves Dryas octopetala, leaves Salix spp., small willows Salix reticulata Bistorta vivipara, bulbils ¹halictrum alpinum, leaves
Median
¼inter 1987 Range
N
1403 2024 1142 1763 848
672—2676 914—2350 1005—1306
4 3 3 1 2
783—914
Median
499 841 519 808 1067
Summer 1987 Range
130—1363 97—1039 369—841 459—1746
N
1 10 4 4 3
Median
¼inter 1988 Range
N
546!,# 313" 543! 1310#
313—1854 192—895 352—1151 1278—1342
6 10 9 2
Seasonal variation in radiocaesium concentration
TABLE 1 Radiocaesium concentration (Bq kg~1 dry weight) in Major Food Plants of Rock Ptarmigan From Winter 1987 to Winter 1988. Food Plants With Significantly Different Radiocaesium Concentration within Seasons are Marked with Different Letters (a, b, c). Significant Differences in Radiocaesium Concentration within a Plant Species Between Seasons are Marked by *
75
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H. Chr. Pedersen et al.
lower during winter (December—February; BCF"0)47) than during the summer and early autumn (August—September; BCF"0)68) although not significantly so (Mann—Whitney test, Z"1)639, n "6, n "12, p"0)10). 1 2 In willow ptarmigan average BCF was calculated to 0)61 (SD"0)25, n"18), which was significantly higher than BCF for rock ptarmigan (t "2)96, p"0)006). Transfer coefficient (F ) was calculated for willow 34 & ptarmigan assuming that food intake was similar to wild red grouse ¸. lagopus scoticus in Scotland, i.e. 55 g daily (see Moss and Horrill, 1996). F for willow ptarmigan at Knutsh+ was then 3)1$1)3 d kg~1. & The aggregated transfer coefficient (¹ ) for both willow and rock ptarmi!' gan was 0)003—0)009.
DISCUSSION During the regular hunting season for ptarmigan in September—February the radiocaesium concentration in both ptarmigan species was only rarely above the limit recommended for meat for human consumption ([134Cs #137Cs]"600 Bq kg~1 wet weight) (NOU 1987). Compared to other herbivore species in the study area such as root vole (Microtus oeconomus) (Steen and Skogland, 1991) and reindeer (Rangifer tarandus) (Skogland, 1987) the radiocaesium concentration in both willow ptarmigan and rock ptarmigan was relatively low and the levels were well below limits where negative effects on individual animals could be expected (Brisbin, 1991). As predicted, willow ptarmigan chicks had a different accumulation pattern compared to adults with significantly higher radiocaesium concentration during late summer and early autumn. A difference, although not statistically significant, was still present in September. From October onwards levels were the same in juveniles and adult birds. This is in accordance with earlier studies showing that the accumulation/excretion of radionuclides may change with age (e.g. Reichele et al., 1970; Palo et al., 1991). We suggest that differences in food and metabolism can cause such an accumulation pattern as observed. Earlier studies have shown that ptarmigan chicks mainly eat easily digestible herbs and only to a limited extent more heavily digestible woody plants (Norris et al., 1979; Spids+, 1980). Although also adult birds eat herbs during summer the proportion of woody shrubs like Salix spp. is much larger than in chicks. This relationship between herbs and woody plants in the food changes during early to late autumn and in late September early October the juvenile ptarmigan eat the same proportion of woody plants as adult birds (Stokkan and Steen, 1980). The ptarmigan chicks have a very rapid growth rate and are almost fully grown in September—October (e.g. Myrberget, 1975, 1984). This rapid
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growth can be met through high intake of nutrients and a large intake of minerals as Ca, K, Fe as well as other important minerals for muscle and bone tissue production. This implies that radiocaesium, because of the close relationship to K, is accumulated during this phase. In September when the chicks are almost fully grown the growth rate and the accumulation of radiocaesium decreases and the concentration approaches the level found in adults. Graminides and herbs from Knutsh+ have higher radiocaesium concentration compared to the last year shots and leaves of woody plants e.g. Salix spp. and Betula nana (Bretten, 1989, 1991). Based on this information it is possible to explain the seasonal variation in radiocaesium concentration found in willow ptarmigan; the relatively low radiocaesium concentration found during winter is because willow ptarmigan mainly eat Betula pubescens and to some extent other woody plants such as large Salix spp. and B. nana (Myrberget and Aabakken, 1987). As spring progresses the proportion of herbs and therefore the amount of radiocaesium ingested increases. The observed decrease in radiocaesium concentration in birds in October parallels a reduced intake of herbs and increased intake of woody plants. We did not find any significant difference in radiocaesium concentration between willow ptarmigan and rock ptarmigan during summer 1987. This is possibly due to a relatively similar food intake, namely herbs, in both species. In winter, rock ptarmigan have a higher radiocaesium concentration than willow ptarmigan. Both ptarmigan species have a high intake of woody shrubs in winter. However, B. pubescens dominates the diet of willow ptarmigan (Myrberget and Aabakken, 1987), while B. nana, Salix spp. and E. hermaphroditum dominates the diet of rock ptarmigan (Fig. 6). Also rock ptarmigan forages on winter green leaves of Dryas octopetala during winter. Differences in diet might therefore explain the difference in radiocaesium concentration between the two ptarmigan species. The radiocaesium concentration of rock ptarmigan during winter is probably regulated by the thickness of the snow cover. Thin snow cover exposes ridges where food-plants such as Dryas octopetala and Empetrum hermaphroditum, which are essential in the rock ptarmigan’s diet, become available. Thick snow cover forces the birds to forage on shrubs with lower radiocaesium concentration, especially Salix species. Our results indicate that Salix species are preferred to Betula species by the rock ptarmigan, which is in accordance with earlier studies (Gardarson and Moss, 1970). Chernobyl fallout was deposited in the study area mainly on 28 April 1986 (Gaare, 1987). At that time only ridges were snow free and thus vegetation on ridges received a higher contamination level than vegetation
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in e.g. snowbeds (Gaare, 1987). This is also reflected in the radiocaesium concentration of small willow species in the rock ptarmigan diet. Small willows growing on ridges were probably eaten during spring and autumn when the snow was accumulated in depressions in the terrain. These willow shrubs had a higher radiocaesium concentration than small willows eaten during summer, growing further down the slope from the ridge and in snowbeds. This resulted in a lower radiocaesium concentration in rock ptarmigan in August 1987, than in all other sampling periods. The bioconcentration factor (BCF) of rock ptarmigan and willow ptarmigan (0)41 and 0)61, respectively) is in accordance with BCFs found in mammalian herbivores (0)3—2)0) and lower than that found in mammalian carnivores (3)8—7)0) (Reichele et al., 1970). A low BCF indicates that the radiocaesium turnover is relatively fast, and that the biological half-life of radiocaesium in ptarmigan is short compared to most mammals. Another explanation might be that the absorption of radiocaesium in the intestine is low. The calculated transfer coefficient for willow ptarmigan (3)2 day kg~1) was in the same range as that found for domestic hens i.e. 1)4—9)5 day kg~1 (Voigt et al., 1993), but lower than what was found for wild red grouse (13)2 day kg~1) (Moss and Horrill, 1996). For willow ptarmigan, daily food intake of red grouse was used to calculate F . As daily food intake may & differ between the species the calculated transfer coefficient of willow ptarmigan is associated with uncertainties. The aggregated transfer coefficients (¹ ) for willow and rock ptarmigan are lower than ¹ found for !' !' game ruminants; red deer Cervus elaphus, roedeer Capreolus capreolus and moose Alces alces (see Howard et al., 1996). Both the low BCF and the low ¹ show that the potential for transferring 137Cs from ptarmigan to !' humans after the Chernobyl accident was low. Indications have been found showing that radiocaesium, in the same way as potassium, is most strongly bound to lignin in higher plants (Gaare and Skogen, 1989). Radiocaesium absorption in the intestines will therefore depend on the partition of caesium in the plant species and the digestibility of plant tissue. Ptarmigan digest fibrous food plants to a lesser extent than herbs (Moss and Hanssen, 1980) and it is therefore possible that the relative absorption of caesium from food plants is lower in the fibrous winter food than from herbs eaten during the summer. Such a situation was indicated in willow ptarmigan as the BCF in winter (0)47) was lower than during summer (0)68). The BCFs show that there is no increase in radiocaesium concentration from vegetation to ptarmigan. Hence, both due to the low BCFs and to a relatively low intake of ptarmigan meat, the potential for any appreciable exposure of humans to radioactivity through consumption of ptarmigan is low.
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ACKNOWLEDGEMENTS In this study a number of people have assisted in collecting the material in the field, preparing the material in the laboratory and by analysing it. We would like to thank them all. A special thanks to Simen Bretten and his crew at Kongsvold Biological Station. Thanks to Duncan Halley for checking the English.
REFERENCES Anderson, G. E., Gentry, J. B. and Smith, M. H. (1973) Relationships between levels of radiocaesium in dominant plants and arthropods in a contaminated streambed community. Oikos 24, 165—70. Bretten, S. (1989) Radioaktivitet i alpine plantearter og plantesamfunn pas Dovrejell: Statusrapport over arbeidet i 1988. In Radio~kologisk forskningsprogram, resultater fra unders~kelsene i 1988, eds E. Gaare and O. Ugedal, pp. 67—9. Norsk institutt for naturforskning, Trondheim, (in Norwegian; English abstract). Bretten, S. (1991) Radioaktivitet Cs-137 etter Tsjernobylnedfallet i alpine plantesamfunn pas Dovrefjell. In ¹sjernobyl- sluttrapport fra NINAs radio~kologiske program 1986—1990, eds E. Gaare, B. Jonsson and T. Skogland, pp. 28—35. Norsk institutt for naturforskning, Trondheim (in Norwegian). Bergerud, A. T., Peters, S. S. and McGrath, R. (1963) Determining sex and age of willow ptarmigan in Newfoundland. Journal of ¼ildlife Management 27, 700—11. Brisbin, I. L., Jr. (1991) Avian radioecology. In Current Ornithology, ed D. M. Power, Vol. 8, pp. 69—140. Plenum Press, New York. Gardarson, A. and Moss, R. (1970) Selection of food by icelandic ptarmigan in relation to its availability and nutritive value. In Animal populations in relation to their food resources, ed. A. Watson, pp. 47—71. Blackwell Scientific Publications, Oxford. Gaare, E. (1987) Hvorfor varierer innholdet av radiocaesium i lav sas sterkt over korte avstander? In Radio~kologisk forskningsprogram, resultater fra unders~kelser i 1986, ed. B.M. Jenssen, pp. 53—73. Direktoratet for naturforvaltning, Trondheim. Gaare, E. and Skogen, A. (1989) Radioaktivitet i lav, moser og noen beiteplanter: resultater fra innsamlinger i 1988 og beregning av halveringstider. In Radio~kologisk forskningsprogram, resultater fra unders~kelsene i 1988, eds E. Gaare and O. Ugedal, pp. 49—66. Norsk institutt for naturforskning, Trondheim. Gaare, E., Jonsson, B. and Skogland, T. (1991) Tsjernobyl — sluttrapport fra NINAs radio+kologiske program 1986—1990. NINA temahefte 2, 1—71. Heim, J. G. (1971) Zur geologie des su¨dlichen Trondheim-Gebietes. Ph.D. ¹hesis, University of Mainz, Germany. Howard, B. J., Johanson, K, Linsley, G. S., Hove, K., Pro¨hl, G. and Horyna, J. (1996) Transfer of radionuclides by terrestrial food products from semi-natural ecosystems to humans. In Modelling of radionuclide interception and loss processes in vegetation and of transfer in semi-natural ecosystems. Second report of the VAMP terrestrial working group, IAEA-TECDOC-857.
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Il’enko, A. I. (1973) Radioecology in wild animals. In Radioecology, eds V. M. Klechovski, G. G. Polokarpov and R. M. Aleksakhin, pp. 241—74. Wiley, New York. Kitchings, T., Digregoria, D. and van Voris, P. (1975) A review of the ecological parameters of radionuclide turnover in vertebrate food chains. In Radioecology and energy resources, Proc. fourth national symposium on radioecology, eds E. Colbert and C. E. Cushing, Dowden, pp. 304—13. Hutchinson and Ross, Inc., Stroudsburg. Kas las s, J. A., Bretten, S., Byrkjedal, I. and Njas stad, O. (1994) Radiocesium (137Cs) from the Chernobyl reactor in eurasian woodcock and earthworms in Norway. Journal of ¼ildlife Management, 58, 141—147. Lindahl, I. and Has brekke, H. (1986) Mapping radioactive fallout after the Chernobyl accident. NGº report 86, 160, 1—19. Lowe, V. P. W. and Horrill, A. D. (1991) Caesium concentration factors in wild herbivores and the fox (»ulpes vulpes ¸). Environmental Pollution, 70, 93—107. L+faldli, L., Kas las s, J. A. and Fiske, P. (1992) Habitat selection and diet of the endangered great snipe Gallinago media during breeding. Ibis 134, 35—43. Medvedev, Z. A. (1986) Ecological aspects of the Chernobyl nuclear plant disaster. ¹rends Ecology Evolution 1, 23—25. Moss, R. and Hanssen, I. (1980) Grouse Nutrition. Nutrition Abstracts and Reviews —Series B 50, 555—567. Moss, R. and Horrill, A. D. (1996) Metabolism of radiocaesium in red grouse. Journal of Environmental Radiation 33(1), 49—62. Myrberget, S. (1975) Age determination of willow grouse chicks. Norwegian Journal of Zoology 23, 165—171. Myrberget, S. (1979) Winter food of willow grouse in two Norwegian areas. Meddelelser fra norsk viltforskning 3(7), 1—32. Myrberget, S. (1984) As rsvariasjoner i kroppsvekt hos lirype i Nord-Norge. Fauna 37, 56—62. Myrberget, S. and Aabakken, R. (1987) Annual variation in the quality of winter food of willow grouse ¸agopus lagopus, and its effect on population dynamics. Fauna norv Ser. C, Cinclus, 10, 89—94. Norris, C., Norris, E. and Myrberget, S. (1979) Food preference of captive willow grouse ¸agopus lagopus. Fauna norv. Ser. C, Cinclus, 2, 49—52. NOU (1987) Tsjernobyl ulykken. Norges offentlige utredninger, 1987-1, 107 Palo, R. T., Nelin, P., Nylen, T. and Wickman, G. (1991) Radiocaesium levels in Swedish moose in relation to deposition, diet and age. Journal Environmental Quality 20, 690—695. Pedersen, H. C., Steen, J. B. and Andersen, R. (1983) Social organization and territorial behaviour in a willow ptarmigan population. Ornis Scandinavica 14, 263—272. Reichele, D. E., Dunaway, P. B. and Nelson, D. J. (1970) Turnover and concentrations of radionuclides in food chains. Nuclear Safety 11, 43—55. Spids+, T. (1980) Food selection by willow grouse ¸agopus lagopus chicks in northern Norway. Ornis Scandinavica 11, 99—105. Salbu, B. and Bj+rnstad, H. E. (1992) Radioaktivt nedfall ved nukleære uhell og konsekvenser for landbruk og naturmilj+. In Radioaktivt nedfall fra ¹sjernobylulykken, eds. T. H. Garmo and T. B. Gunner+d, pp. 15—30. Norges Landbruksvitenskapelige Forskningsras d, As s, (in Norwegian; English abstract).
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Skogland, T. (1987) Radiocaesium concentrations in wild reindeer at Dovrefjell, Norway. Rangifer 7, 42—45. Stokkan, K. A. and Steen, J. B. (1980) Age determined feeding behaviour in willow ptarmigan chicks ¸agopus lagopus lagopus. Ornis Scandinavica 11, 75—76. Steen, J. B., Pedersen, H. C., Erikstad, K. E., Hansen, K. B., H+ydal, K. and St+rdal, A. (1985) The significance of cock territories in willow ptarmigan. Ornis Scandinavica 16, 277—282. Steen, H. and Skogland, T. (1991) Lokale variasjoner av radiocaesium i fjellrotte og lemen. NINA ¹emahefte 2, 62—63. Straney, D. O., Beaman, B., Brisbin, I. L. Jr. and Smith, M. H. (1975) Radiocaesium in birds of the Savannah River Plant. Health Physics 28, 341—345. Varskog, P., Næumann R. and Steinnes, E. (1994) Mobility and plant availability of radioactive Cs in natural soil in relation to stable Cs, other alkali elements and soil fertility. Journal of Environmental Radioactivity 22(1), p. 43—53. Voigt, G., Mu¨ller, H, Partezke, H. G., Bauer, T. and Ro¨hrmoser, G. (1993) 137Cs transfer after Chernobyl from fodder into chicken meat and eggs. Health Physics 65, 141—146. Ward, G. and Johnson, J. E. (1986) Validity of the term transfer coefficient. Health Physics 50, 411—414. Webb, G. A. M., Simmonds, J. R. and Wilkins, B. T. (1986) Radiation levels in eastern Europe. Nature 321, 821—822.
Seasonal Variation in Radiocaesium Concentration in Willow Ptarmigan and Rock Ptarmigan in Central Norway after the Chernobyl Fallout Hans Chr. Pedersen,a Signe Nyb+b & Per Varskogc a Norwegian Institute for Nature Research, Dep. of Terrestrial Ecology, Tungasletta 2, N-7005 Trondheim, Norway b ALLFORSK, Dep. of Ecotoxicology, Norwegian University of Science and Technology, Gryta 2, N-7010 Trondheim, Norway c Institute for Energy Technology, P.O. Box 40, N-2007 Kjeller, Norway (Received 20 May 1996; accepted 22 October 1997)
ABS¹RAC¹ Radioactive caesium (20—60 kBq m~2) was deposited after the Chernobyl accident in the mountains of central Norway. ¹wo sympatric ptarmigan species, willow ptarmigan Lagopus lagopus and rock ptarmigan L. mutus, inhabit this alpine ecosystem and are important game species. In 1987 and 1988, a study was carried out to try to identify factors affecting radioactive caesium concentration in these birds. Juvenile willow ptarmigan contained more radiocaesium than adults, but the two sexes did not differ in radiocaesium concentration. ¹he radiocaesium concentration of food plants correlated with radiocaesium concentration of rock ptarmigan, and a seasonal variation in radiocaesium concentration of both ptarmigan species was seen. Rock ptarmigan contained more radiocaesium than willow ptarmigan during winter, but not in summer. ¹his difference was related to differences in diet. ¹he bioconcentration factor was 0)4—0)6. ¹he aggregated transfer coefficient was 0)003—0)009 m2 kg~1 for both species. In spite of the high deposition, the radiocaesium concentration in muscle rarely exceeded the limit recommended for human food consumption (600 Bq kg~1). ( 1998 Elsevier Science ¸td. All rights reserved
INTRODUCTION The fallout after the reactor accident of Chernobyl in April 1986 exposed several northern ecosystems to radionuclides (Medvedev, 1986; Webb et al., 65
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H. Chr. Pedersen et al.
1986). In central Norway the major deposition was in the form of fuel or condensed particles (Salbu and Bj+rnstad, 1992), and consisted mainly of radiocaesium 134Cs and 137Cs (Lindahl and Has rbrekke, 1986). Alpine areas were contaminated and research conducted to understand contamination mechanisms of important aquatic and terrestrial ecosystems (Gaare et al., 1991). Until the Chernobyl accident, most studies of radiocaesium contamination in food chains have involved continuous release of fission by-products from power production reactors (e.g. Anderson et al., 1973; Brisbin, 1991), or from above ground nuclear weapon tests. Here we present a study of radiocaesium (137Cs) in willow ptarmigan (¸agopus lagopus), rock ptarmigan (¸agopus mutus) and their main food plants, in Dovrefjell, Norway. The objective of the study is to elucidate the factors affecting transfer of radiocaesium among trophic levels and accumulation of radiocaesium in ptarmigan throughout the year. Dovrefjell mountain area was heavily contaminated by the Chernobyl accident (Lindahl and Ha> brekke, 1986). The ptarmigan are the only two resident herbivore avian species inhabiting the alpine area throughout the year, being one of the keystone species in the alpine ecosystem. Furthermore, ptarmigan is the most important small game in Norway, involving 100 000 hunters annually harvesting 500 000—750 000 birds. Thus ptarmigan could be a source of transfer of radiocaesium to protected avian predators such as gyrfalcon (Falco rusticolus) as well as humans. Earlier studies have shown that accumulation and excretion of radionuclids in wild animals depend on factors such as contamination level in different habitats, food choice, tropic level, age and several physiological features (Reichele et al., 1970; Il’enko, 1973; Straney et al., 1975). The diet of both ptarmigan species varies throughout the year. As different plants were expected to differ in their accumulation rate of radiocaesium, it was predicted that ptarmigan would have a seasonal variation in contamination level. Furthermore, a different accumulation pattern was predicted in juveniles compared to adult birds because of differences in physiology and diet. To evaluate possible accumulation in the food chain involving ptarmigan species the calculation of the bioconcentration factor (BCF"radiocaesium concentration in birds/radiocaesium concentration in food) is important. BCF in herbivore mammals is lower than in carnivore mammals (Reichele et al., 1970; Kitchings et al., 1975), but so far few studies in birds have been reported (e.g. Lowe and Horrill, 1991; Kas las s et al., 1994; Moss and Horrill, 1996). By comparing radiocaesium concentration in ptarmigan and their food plants, BCF could be calculated.
Seasonal variation in radiocaesium concentration
67
In the study area the deposition of radiocaesium increased with altitude (Gaare, 1987). The two ptarmigan species share the alpine habitat, but overlap only in the border between the low-alpine and middle-alpine zone. Hence we hypothesized that rock ptarmigan inhabiting the uppermost zone would have a higher radiocaesium concentration than willow ptarmigan.
MATERIALS AND METHODS Study area The study was carried out in Knutsh+, Dovrefjell National Park, in central Norway (62°17@N, 9°39@E) from 1987 to 1988. The study area measured 10 km2, covering the sub-, low- and middle-alpine zone (950—1690 m asl). Bedrock consisted mostly of phyllitic mica schist and green schist from the Upper Ordovicium, giving rise to mineral-rich soil (Heim, 1971), and thus a rich flora. The study area has been described in detail by Pedersen et al. (1983) and L+faldli et al. (1992). Total deposition of 134Cs and 137Cs in the area during May 1986 was estimated to be from 20 to 60 kBq m~2 (Bretten, 1991). Sampling of ptarmigan and vegetation Willow ptarmigan were collected from May 1987 to December 1988 (n"122). Rock ptarmigan were collected from March 1987 to September 1988 (n"37). Both years, birds were collected monthly from May throughout October, while in winter (November throughout April) birds were collected only once. All birds were collected by shooting and weight, sex and age were determined (e.g. Bergerud et al., 1963). Samples were taken from the breast muscle in both ptarmigan species and radiocaesium concentration was measured on a wet weight basis. In rock ptarmigan the crop content was sorted into plant species and thus the relative importance of food plants was determined. Based on the composition of crop content vegetation samples were collected in the same general area as the birds were shot. Vegetation samples and samples of crop content were dried in an oven at 70°C for 24 h. The relative proportion of different plant species in each crop was measured on dry weight basis. The radiocaesium concentration of each crop was estimated using the relative content of each plant species in the crop and the mean radiocaesium concentration of the relevant species collected at the same time. The most important food plants of willow ptarmigan are well known from earlier studies (Myrberget, 1979; Spids+, 1980), conducted in the same study area
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(Pedersen et al., 1983; Steen et al., 1985; Pedersen, unpublished). In parallel with sampling of willow ptarmigan, collection of important food plants was carried out (Bretten, 1989). To allow for calculation of a bioconcentration factor crops were collected from 18 willow ptarmigan and radiocaesium concentration analysed. In 20 individual rock ptarmigan radiocaesium concentration was analysed both on wet and dry weight basis. Breast muscle was dried in an oven at 70°C for at least 24 h. Calculations of bioconcentration factors (BCF) in rock ptarmigan were based on the relationship between radiocaesium concentration in dried breast muscle and radiocaesium concentration in the crop from the same bird. As all plant material was measured on dry weight basis and some ptarmigan muscle tissue on wet weight basis, a correction factor had to be calculated. The correction factor was calculated from c "c ) k, (1) $85 885 where c denotes concentration of radiocaesium in dried pectoral muscle $85 (Bq kg~1), c denotes concentration of radiocaesium in fresh pectoral 885 muscle (Bq kg~1) and k is the correction factor. The correction factor was 3.59 and was used for both ptarmigan species. BCF was then calculated from BCF"c ) k/c , (2) 885 #301 where c denotes radiocaesium concentration in crop (Bq kg~1). The #301 transfer coefficient (F ) given by Ward and Johnson (1986) deviates from the & BCF in that it takes into account daily food intake ( f ) (kg day~1) and that $ the concentration of radiocaesium (Bq kg~1) is measured in fresh muscle (3): F "c /c ) f . (3) & 885 #301 $ The aggregated transfer coefficient (¹ ) for 137Cs was calculated as given !' by Howard et al. (1986): ¹ "c /depositon, !' 885 where deposition is acitivity per unit area (Bq m~2).
(4)
Measurement of radiocaesium activity Total radiocaesium (134Cs#137Cs) in the samples was determined at the Isotope laboratory, Norwegian University of Science and Technology, Trondheim, using two 3]3 In. NaI well detectors (active volume 23)5 cm3). The samples were placed in plastic or glass containers of known geometry and gross counts (corrected for background) in a 460—932 keV window
Seasonal variation in radiocaesium concentration
69
were collected. The detectors were regularly re-calibrated using standards consisting of samples of lichen contaminated by the Chernobyl accident and packed in the same type of containers as the ordinary samples. This calibration routine automatically compensates for the change in 137Cs : 134Cs ratio with time. Differences in sample volume (i.e. the sample container fill height) were adjusted for according to correction functions specific for each NaI detector. The measured activity concentrations were not adjusted for eventual differences in sample density. No significant self-absorption was likely to occur at the used energy interval for the type of material in question. Calculations of 137Cs derived from determinations of the total radiocaesium were based on the 137Cs : 134Cs ratio determined at the Isotope laboratory, Trondheim. The ratio is based on samples of vegetation taken and counted the first few days after the Chernobyl accident, and was determined as 1)86 (SD"0)06, n"32, time adjusted to May 15, 1986) (Varskog et al., 1994). 137Cs thus accounted for 65% of the initial radiocaesium activity. Radiocaesium values were determined as Bq kg~1 dry weight for vegetation and crop samples, and both Bq kg~1 dry weight and Bq kg~1 wet weight for ptarmigan samples. For radiocaesium determinations below the detection limit (approximately 10% of the samples) 0)5]detection limit was used. The detection limit depends on the activity of the samples and its weight, and was between 20—40 Bq kg~1. Statistical procedures To examine differences in radiocaesium concentration in breast muscle between two groups of data such as sex, age, months, seasons, and species, we used Mann—Whitney tests (corrected for ties). We used Kruskal—Wallis tests (corrected for ties) to examine differences among months. To examine the relationship between radiocaesium concentration in rock ptarmigan breast muscle and calculated concentration in the diet we used a Spearman’s rank correlation test. All statistical tests present two-tailed p-values. Differences were considered significant when p-values were less than 0)05.
RESULTS No significant difference was found in radiocaesium concentration between male and female willow ptarmigan within months either in 1987 or 1988 (Mann—Whitney U-tests, p'0)05). In the further analyses the material from both sexes are therefore pooled. In rock ptarmigan the material was too limited to carry out a similar test. However, based on result from willow ptarmigan, we decided also to pool data from rock ptarmigan.
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A comparison of radiocaesium concentration in adult and juvenile willow ptarmigan from August and September 1987 indicated that juveniles had higher levels of radiocaesium than adults in August, although not significantly so (x"108)25 and x"83, 50, respectively, Mann—Whitney test, Z"1)70, n "4, n "12, p(0)10), but not in September (x"109)09 1 2 and x"102)67, respectively, Mann—Whitney test, Z"1)01, n "3, 1 n "11, p'0)10). In 1988 a significantly higher radiocaesium concentra2 tion was found in juveniles compared to adult willow ptarmigan in July (Mann—Whitney test, Z"1)94, n "3, n "5, p"0)05) and August 1 2 (Mann—Whitney test, Z"2)05, n "2, n "7, p(0)05) (Fig. 1). In Sep1 2 tember, juveniles still had higher radiocaesium concentration than adults but not significantly so (Mann—Whitney test, Z"1)73, n "6, n "10, 1 2 p(0)10). Neither in 1987 nor 1988 was any significant difference found in radiocaesium concentration in juvenile and adult willow ptarmigan from October to June (Mann—Whitney tests, p'0)05). During this period all birds were called ‘‘adults’’. The radiocaesium concentration of juvenile willow ptarmigan during July—October, 1987 and 1988 is shown in Fig. 2. In 1987 the radiocaesium concentration did not show any significant difference among months (Kruskal—Wallis test, H"4)13, n"25, DF"2, p'0)05). However, in 1988 a significant variation was found among months in radiocaesium concentration in juvenile willow ptarmigan (Kruskal—Wallis test, H"14)98, n"25, DF"3, p(0)01). In both years a reduction in radiocaesium concentration was observed from August/September to October (Fig. 2),
Fig. 1. Radiocaesium concentration (Bq kg~1 wet weight) in breast muscle of juvenile and adult willow ptarmigan collected at Dovrefjell in 1988. Radiocaesium concentration given as median values. N—number of birds. *—statistically significant difference.
Seasonal variation in radiocaesium concentration
71
Fig. 2. Radiocaesium concentration (Bq kg~1 wet weight) in breast muscle of juvenile willow ptarmigan collected at Dovrefjell in 1987 and 1988. Radiocaesium concentration given as median values. N— number of birds.
but this reduction was only significant in 1988 (Mann—Whitney tests, p(0)05). A general pattern in accumulation of radiocaesium in adult willow ptarmigan was indicated in 1987 and 1988; a gradual increase in radiocaesium concentration is observed from May reaching a peak in September. From October onwards a decline in radiocaesium concentration was observed, reaching a low winter level in December which lasts until next spring (Fig. 3). In 1987, the radiocaesium concentration varied among months although not significantly so (Kruskal—Wallis test, H"12)04, n"39, DF"7, p"0)10). However, radiocaesium concentration of birds collected in December was significantly lower than birds collected from May to October (Mann—Whitney tests, p(0)05). During 1988 a significant variation was found among months in radiocaesium concentration in adult willow ptarmigan (Kruskal—Wallis test, H"26)20, n"44, DF"7, p(0)001). As in 1987, the December values was low, but not significantly lower than in other months (Mann—Whitney tests, p'0)05). In both years the highest radiocaesium concentration was found in willow ptarmigan collected in September (Fig. 3). Radiocaesium concentration in adult willow ptarmigan and rock ptarmigan did not differ within months from May to August 1987 (Mann— Whitney tests, p'0)05). However, during winter the radiocaesium concentration in the two ptarmigan species differed. Rock ptarmigan collected in midwinter 1987-1988 (January/February -1988) had significantly higher radiocaesium concentration than willow ptarmigan (December-1987)
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Fig. 3. Radiocaesium concentration (Bq kg~1 wet weight) in breast muscle of adult willow ptarmigan collected at Dovrefjell in 1987 and 1988. Radiocaesium conentration given as median values. N— number of birds.
Fig. 4. Radiocaesium concentration (Bq kg~1 wet weight) in breast muscle of adult rock ptarmigan collected at Dovrefjell in 1987 and 1988. Radicaesium conentration given as median values. N— number of birds.
(Mann—Whitney test, Z"2)74, n "5, n "6, p(0)01). Also in March 1 2 1988 rock ptarmigan had higher radiocaesium concentration than willow ptarmigan (Mann—Whitney test, Z"2)60, n "4, n "6, p(0)01). 1 2 In adult rock ptarmigan a significant variation was found in radiocaesium concentration among months in 1987 (Fig. 4) (Kruskal—Wallis test, H"12)11, n"24, DF"5, p(0)05). Rock ptarmigan collected in midwinter 1988 (February) had significantly lower radiocaesium concentration than birds collected during autumn (September 1987) and in late winter (March 1987) and early spring (May 1988) (Mann—Whitney tests, p(0)05). Contrary to findings in adult willow ptarmigan, the radiocaesium concentration in rock ptarmigan was significantly lower in August compared to all other months (Mann—Whitney tests, p(0)05). Thus the radiocaesium concentration in rock ptarmigan was lowest in summer and midwinter with peaks in autumn and spring. A significant positive correlation was found in radiocaesium concentration in rock ptarmigan and that calculated in the diet (Fig. 5) (Spearman
Seasonal variation in radiocaesium concentration
73
Fig. 5. Radiocaesium concentration in the diet (Bq kg~1 dry weight) in relation to breast muscle (Bq kg~1 wet weight) of rock ptarmigan.
rank correlation test, r "0)57, n"18, p"0)007). Examination of crops S from collected rock ptarmigan showed that they were mainly eating dwarf birch (Betula nana), salix (Salix spp. ), crowberry (Empetrum hermaphroditum), cowberry (»accinium vitis-idaea) and leaves of the herb Dryas octopetala in winter. As snowmelt progressed during spring the rock ptarmigan shifted towards small willow species in their diet (Fig. 6). In May 1988 the snowcover was almost complete until 10 May and all the birds were collected before this date. This is reflected in the more winterlike diet in May 1988 compared to May 1987 (Fig. 6). As the snow melted small willows such as S. herbacea/polaris were uncovered, and these small willows were the major constituents of the diet before the availability of herbs increased (Fig. 6). Herbs were preferred during summer until their availability was reduced in autumn. Before the snow accumulated in the autumn small willows were again the preferred food plants (Fig. 6). The vegetation samples were grouped in three; winter 1987; summer 1987 (June—August); and winter 1988 (Table 1). There were no difference in radiocaesium concentration among different plant species during winter 1987 (Kruskal—Wallis test, H"3)80, n"13, DF"4, p"0)43). However, during winter 1988 such a difference was found (Kruskal—Wallis test, H"11)25, n"27, DF"3, p"0)01). The radiocaesium concentration of willow shrubs Salix spp. was significantly lower than in the other food plants e.g. Betula nana, Empetrum hermaphroditum and »accinium vitisidaea (Table 1). »accinium vitis-idaea had significantly higher radiocaesium concentration than Salix spp. and Empetrum hermaphroditum (Table 1). From winter 1987 to winter 1988, the radiocaesium concentration
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Fig. 6. Proportion of different food plants in crops of rock ptarmigan from Dovrefjell collected in 1987 and 1988 based on amount of dry matter in crops. The different food plants are grouped into 5 categories; (1) Small willows, mainly Salix herbacea, S. polaris and S. reticulata; (2) Shrub, maily Betula nana and larger Salix species; (3) »accinium vitis-idaea and Empetrum hermaphroditum; (4) Herbs, several species but during winter/spring mainly Dryas octopetala and during summer/autumn mainly Bistorta vivipara; (5) Other plant material; unidentified crop-content, mainly mosses, lichen or dead plant material.
decreased significantly in Salix shrubs and leaves of Empetrum hermaphroditum, but not in twigs/buds of Betula nana (Table 1). During the summer 1987 there were no significant differences in radiocaesium concentration among food plant species (Kruskal—Wallis test, H"1)89, n"21, DF"3, p "0)60). For small willows which are one of the major constituents of the diet during spring and autumn (Fig. 6), some additional sampling was done in spring (May) and autumn (September/October). The radiocaesium concentration of small willows varied significantly among seasons (Kruskal—Wallis test, H"8)35, n"21, DF"2, p"0)015), with lower levels in summer (median"841, range"130—1363 Bq kg~1, n"10) than in spring (median"1138, range"910—1691 Bq kg~1, n"8) (Mann—Whitney test, Z"!2)69, n "8, n "10, p"0)007) and autumn (median"1266, 1 2 range"968—1678 Bq kg~1, n"3) (Mann—Whitney test, Z"!1)86, n "10, n "3, p"0)06). The radiocaesium concentration of small willows 1 2 did not differ between spring and autumn (Mann—Whitney test, Z"!0)21, n "8, n "3, p"0)84). 1 2 Based on radiocaesium concentration in crops and muscle samples from rock ptarmigan an average bioconcentration factor (BCF) was calculated to be 0)41 (SD"0)14, n"18). No difference was found in BCF between juvenile and adult willow ptarmigan (Mann—Whitney test, p'0)05) and data from age groups were pooled. Average BCF in willow ptarmigan was
Plant species
Betula nana, twigs/buds Salix spp., shrubs, twigs/buds* Empetrum hermaphroditum* »accinium vitis-idaea, leaves Dryas octopetala, leaves Salix spp., small willows Salix reticulata Bistorta vivipara, bulbils ¹halictrum alpinum, leaves
Median
¼inter 1987 Range
N
1403 2024 1142 1763 848
672—2676 914—2350 1005—1306
4 3 3 1 2
783—914
Median
499 841 519 808 1067
Summer 1987 Range
130—1363 97—1039 369—841 459—1746
N
1 10 4 4 3
Median
¼inter 1988 Range
N
546!,# 313" 543! 1310#
313—1854 192—895 352—1151 1278—1342
6 10 9 2
Seasonal variation in radiocaesium concentration
TABLE 1 Radiocaesium concentration (Bq kg~1 dry weight) in Major Food Plants of Rock Ptarmigan From Winter 1987 to Winter 1988. Food Plants With Significantly Different Radiocaesium Concentration within Seasons are Marked with Different Letters (a, b, c). Significant Differences in Radiocaesium Concentration within a Plant Species Between Seasons are Marked by *
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lower during winter (December—February; BCF"0)47) than during the summer and early autumn (August—September; BCF"0)68) although not significantly so (Mann—Whitney test, Z"1)639, n "6, n "12, p"0)10). 1 2 In willow ptarmigan average BCF was calculated to 0)61 (SD"0)25, n"18), which was significantly higher than BCF for rock ptarmigan (t "2)96, p"0)006). Transfer coefficient (F ) was calculated for willow 34 & ptarmigan assuming that food intake was similar to wild red grouse ¸. lagopus scoticus in Scotland, i.e. 55 g daily (see Moss and Horrill, 1996). F for willow ptarmigan at Knutsh+ was then 3)1$1)3 d kg~1. & The aggregated transfer coefficient (¹ ) for both willow and rock ptarmi!' gan was 0)003—0)009.
DISCUSSION During the regular hunting season for ptarmigan in September—February the radiocaesium concentration in both ptarmigan species was only rarely above the limit recommended for meat for human consumption ([134Cs #137Cs]"600 Bq kg~1 wet weight) (NOU 1987). Compared to other herbivore species in the study area such as root vole (Microtus oeconomus) (Steen and Skogland, 1991) and reindeer (Rangifer tarandus) (Skogland, 1987) the radiocaesium concentration in both willow ptarmigan and rock ptarmigan was relatively low and the levels were well below limits where negative effects on individual animals could be expected (Brisbin, 1991). As predicted, willow ptarmigan chicks had a different accumulation pattern compared to adults with significantly higher radiocaesium concentration during late summer and early autumn. A difference, although not statistically significant, was still present in September. From October onwards levels were the same in juveniles and adult birds. This is in accordance with earlier studies showing that the accumulation/excretion of radionuclides may change with age (e.g. Reichele et al., 1970; Palo et al., 1991). We suggest that differences in food and metabolism can cause such an accumulation pattern as observed. Earlier studies have shown that ptarmigan chicks mainly eat easily digestible herbs and only to a limited extent more heavily digestible woody plants (Norris et al., 1979; Spids+, 1980). Although also adult birds eat herbs during summer the proportion of woody shrubs like Salix spp. is much larger than in chicks. This relationship between herbs and woody plants in the food changes during early to late autumn and in late September early October the juvenile ptarmigan eat the same proportion of woody plants as adult birds (Stokkan and Steen, 1980). The ptarmigan chicks have a very rapid growth rate and are almost fully grown in September—October (e.g. Myrberget, 1975, 1984). This rapid
Seasonal variation in radiocaesium concentration
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growth can be met through high intake of nutrients and a large intake of minerals as Ca, K, Fe as well as other important minerals for muscle and bone tissue production. This implies that radiocaesium, because of the close relationship to K, is accumulated during this phase. In September when the chicks are almost fully grown the growth rate and the accumulation of radiocaesium decreases and the concentration approaches the level found in adults. Graminides and herbs from Knutsh+ have higher radiocaesium concentration compared to the last year shots and leaves of woody plants e.g. Salix spp. and Betula nana (Bretten, 1989, 1991). Based on this information it is possible to explain the seasonal variation in radiocaesium concentration found in willow ptarmigan; the relatively low radiocaesium concentration found during winter is because willow ptarmigan mainly eat Betula pubescens and to some extent other woody plants such as large Salix spp. and B. nana (Myrberget and Aabakken, 1987). As spring progresses the proportion of herbs and therefore the amount of radiocaesium ingested increases. The observed decrease in radiocaesium concentration in birds in October parallels a reduced intake of herbs and increased intake of woody plants. We did not find any significant difference in radiocaesium concentration between willow ptarmigan and rock ptarmigan during summer 1987. This is possibly due to a relatively similar food intake, namely herbs, in both species. In winter, rock ptarmigan have a higher radiocaesium concentration than willow ptarmigan. Both ptarmigan species have a high intake of woody shrubs in winter. However, B. pubescens dominates the diet of willow ptarmigan (Myrberget and Aabakken, 1987), while B. nana, Salix spp. and E. hermaphroditum dominates the diet of rock ptarmigan (Fig. 6). Also rock ptarmigan forages on winter green leaves of Dryas octopetala during winter. Differences in diet might therefore explain the difference in radiocaesium concentration between the two ptarmigan species. The radiocaesium concentration of rock ptarmigan during winter is probably regulated by the thickness of the snow cover. Thin snow cover exposes ridges where food-plants such as Dryas octopetala and Empetrum hermaphroditum, which are essential in the rock ptarmigan’s diet, become available. Thick snow cover forces the birds to forage on shrubs with lower radiocaesium concentration, especially Salix species. Our results indicate that Salix species are preferred to Betula species by the rock ptarmigan, which is in accordance with earlier studies (Gardarson and Moss, 1970). Chernobyl fallout was deposited in the study area mainly on 28 April 1986 (Gaare, 1987). At that time only ridges were snow free and thus vegetation on ridges received a higher contamination level than vegetation
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in e.g. snowbeds (Gaare, 1987). This is also reflected in the radiocaesium concentration of small willow species in the rock ptarmigan diet. Small willows growing on ridges were probably eaten during spring and autumn when the snow was accumulated in depressions in the terrain. These willow shrubs had a higher radiocaesium concentration than small willows eaten during summer, growing further down the slope from the ridge and in snowbeds. This resulted in a lower radiocaesium concentration in rock ptarmigan in August 1987, than in all other sampling periods. The bioconcentration factor (BCF) of rock ptarmigan and willow ptarmigan (0)41 and 0)61, respectively) is in accordance with BCFs found in mammalian herbivores (0)3—2)0) and lower than that found in mammalian carnivores (3)8—7)0) (Reichele et al., 1970). A low BCF indicates that the radiocaesium turnover is relatively fast, and that the biological half-life of radiocaesium in ptarmigan is short compared to most mammals. Another explanation might be that the absorption of radiocaesium in the intestine is low. The calculated transfer coefficient for willow ptarmigan (3)2 day kg~1) was in the same range as that found for domestic hens i.e. 1)4—9)5 day kg~1 (Voigt et al., 1993), but lower than what was found for wild red grouse (13)2 day kg~1) (Moss and Horrill, 1996). For willow ptarmigan, daily food intake of red grouse was used to calculate F . As daily food intake may & differ between the species the calculated transfer coefficient of willow ptarmigan is associated with uncertainties. The aggregated transfer coefficients (¹ ) for willow and rock ptarmigan are lower than ¹ found for !' !' game ruminants; red deer Cervus elaphus, roedeer Capreolus capreolus and moose Alces alces (see Howard et al., 1996). Both the low BCF and the low ¹ show that the potential for transferring 137Cs from ptarmigan to !' humans after the Chernobyl accident was low. Indications have been found showing that radiocaesium, in the same way as potassium, is most strongly bound to lignin in higher plants (Gaare and Skogen, 1989). Radiocaesium absorption in the intestines will therefore depend on the partition of caesium in the plant species and the digestibility of plant tissue. Ptarmigan digest fibrous food plants to a lesser extent than herbs (Moss and Hanssen, 1980) and it is therefore possible that the relative absorption of caesium from food plants is lower in the fibrous winter food than from herbs eaten during the summer. Such a situation was indicated in willow ptarmigan as the BCF in winter (0)47) was lower than during summer (0)68). The BCFs show that there is no increase in radiocaesium concentration from vegetation to ptarmigan. Hence, both due to the low BCFs and to a relatively low intake of ptarmigan meat, the potential for any appreciable exposure of humans to radioactivity through consumption of ptarmigan is low.
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ACKNOWLEDGEMENTS In this study a number of people have assisted in collecting the material in the field, preparing the material in the laboratory and by analysing it. We would like to thank them all. A special thanks to Simen Bretten and his crew at Kongsvold Biological Station. Thanks to Duncan Halley for checking the English.
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