A REVIEW OF 137Cs TRANSFER TO FUNGI AND CONSEQUENCES FOR MODELLING ENVIRONMENTAL TRANSFER

GILLETT*, A.G. and CROUT, N.M.J Environmental Science Division, School of Biological Sciences, University of Nottingham, LE12 5RD, UK

To whom all correspondence should be addressed.

Email: andy.gillett@nottingham.ac.uk

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ABSTRACT A review of the published literature describing

137

Cs transfer to fungi was carried out,

summarising the collated data to determine factors controlling transfer and identify an appropriate modelling approach to predict future contamination.
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Cs transfer ratios (TR) are derived for fungi species collected within Europe and the CIS.

Considerable variability in TRs is demonstrated, with TRs varying between <0.001 m2 kg-1 and > 10 m2 kg-1 across all species and over three orders of magnitude for individual species (e.g. Boletus badius). Generally, meta-information (such as habitat and soil attributes) is poorly reported in the literature so that classification of the TR is limited to the effect of nutritional type (P<0.025) in the order mycorrhizal > saprophytic parasitic. Analysis of the literature data set (a heterogeneous source) suggests that there is no statistical evidence to indicate a decrease in TRs for 10 years after the Chernobyl accident. Spatial analysis of a data set for Belgium indicates variability in
137

Cs transfer within a

sampling location, such that fruitbodies collected over a scale of approximately 5km would show activities as variable as those collected over a much larger scale ( or > 50km). Therefore, it is proposed that the collated data sets for individual species can be used to derive best estimates for the parameters describing the distribution of TRs. These can then be used to estimate an effective TR, which, when combined with local soil deposition level and frequency and effect of culinary practices, can give an estimate of the activity of fungi consumed by the general population.

INTRODUCTION

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The importance of the consumption of fungal fruitbodies (i.e. sporocarps) by some animal species, such as roe deer and sheep, as a source of 137Cs intake has been discussed by numerous authors (Hove et al., 1990; Johanson et al., 1994 and Kiefer et al., 1996). The intake of fungi (term used by the authors to indicate fungi sporocarps in the subsequent text) by humans has been shown to be a major factor in autumnal increases of radiocaesium activity of rural populations in Russia (Skuterud et al., 1997a). Urban populations have also been found to have significant radiocaesium intake due to fungi (Mehli and Strand, 1998). Ban-nai et al. (1997) estimated fungi consumption could account for 32% (6 Bq year-1) of the total annual dietary intake of radiocaesium within Japan. Higher potential annual intakes of
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Cs (based on the

measured daily dietary activities of potato, vegetable, beef, milk and cranberry collected between September and October 1994) of 4380 Bq per person (adult males) have been calculated for the Chernobyl affected Rovno and Volynsky regions of the Ukraine (Shiraishi et al., 1997). Shutov et al. (1996) estimated fungi could contribute up to 60-70 % of dietary adults collecting fungi and berries from forests within Russia. Although, fungal sporocarps may only account for 0.5% of the overall inventory of radiocaesium (ignoring the fungal mycelium) within a forest ecosystem (Seminat, 1998) their high contamination compared to other plant species (Bakken and Olsen, 1990), long ecological halflife (Jacob and Likhtarev, 1996) and dietary importance in some populations, especially within the CIS (Skuterud et al., 1997a), requires their attention in models estimating dose to human populations (Howard and Howard, 1996). Fungi fruitbodies have been known to have high activity concentrations of
137 137

Cs intake of those

Cs relative to

higher agricultural plants (Tsukada et al., 1998; Bakken and Olsen, 1990) since the 1960s and 1970s (Kiefer et al., 1965; Haselwandter et al., 1988) and elevated contamination levels have been measured worldwide (e.g. Elstner et al., 1987; Horyna and Randa, 1988; Teherani, 1988; Gaso et al., 1996; Garner and Jenkins, 1991; Sugiyama et al., 1994 and Yoshida et al., 1994).

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Observed contamination levels of

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Cs, even within the same species, show both high spatial

and temporal variability (Fraiture, 1992). Several factors have been implicated : mycelium habitat and depth (Giovani et al., 1990; Guillitte et al., 1994; Rhm et al., 1997); forest typefruitbody location (Andolina and Guillitte, 1990; Fraiture, 1992); sampling strategy (Andolina and Guillitte, 1990); soil clay content (Fraiture et al., 1990); pH (Bakken and Olsen, 1990); soil moisture and/or microclimate (Tsvetnova and Shcheglov, 1994; Jacob and Likhtarev, 1996). It is not presently possible to estimate generic effective ecological half-lives across fungi species because species with superficial mycelium (Collybia and Clitocybe sp.) will attain highest contamination within a few months of fallout whilst other deeper penetrating species (such as Boletus edulis) will achieve contamination peaks several years after deposition (Fraiture et al., 1990). Therefore, ecological half-lives can be deduced but may be site-specific and will be closely controlled by forest-type and litterfall (due to the effects on the weathering and recycling of radionuclides), soil properties and seasonal fluctuations in microclimate (Rhm et al., 1998). Amundsen et al. (1996) observed ecological half-lives for transfer factors of between 2 and 6 years in Norway for different fungi species (though standard errors were up to 8 years) by sampling soil to a 5 cm depth, whilst Rhm et al. (1998) derived ecological half-lives of between 2.8 and 7.7 years for the different horizons within a Bavarian forest utilised by the mycelia of different species. Conversely, using Russian data Jacob and Likhtarev (1996) found no
137

significant time dependency in clarify any time dependency.

Cs transfer. It is apparent further detailed study is required to

Information on the spatial scale over which mushroom contamination varies is generally lacking from the literature with some notable exceptions (Dahlberg et al., 1997). This is a serious gap in knowledge from a modelling perspective because if most of the variation occurs over very small scales (i.e. metres) it will be difficult to predict differences in uptake. The objective of this paper

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is to review and summarise the data collated for radiocaesium transfer to fungi and to identify an appropriate modelling approach to predict food chain contamination.

SOURCES OF DATA Two data sets have been used in the analysis : a survey of the published literature and a large scale study carried out in 1986 and 1987 in Belgium (Fraiture et al., 1989). The data and methodology are described below.

Literature data set A general review of the (primarily) post Chernobyl literature on radiocaesium (137Cs) transfer from soil to fungi fruitbodies has been carried out for the period 1986-1997. Transfer has generally been summarised in the literature as the aggregated Transfer Coefficient commonly referred to as the Tag (Skuterud et al., 1997b) or occasionally as the ATC (Gaso et al., 1996). This is defined as the ratio between fungi activity (at time t) and the initial deposit of radiocaesium (at time t=0, assumed to occur at 1st May 1986). Consequently, the variation in Tags over a period of time (as in this analysis) will include a systematic bias due to the physical decay of 137Cs. To account for this, in this paper, the initial soil deposit has been decay corrected (to the time of fungi sampling) and we shall term the ratio used as the Transfer Ratio or TR (defined as the ratio of fungi activity to soil deposit, both at time t). In practice, the difference between the two transfer terms (TR and Tag) will be relatively small compared to variability that is generally reported within and between species due to other factors. A total of 558 TRs have been found from the 27 literature sources shown in Table 1 (referred to in this paper as the NU97 data set) comprising samples collected from at least 13 countries within Europe and the CIS at 95 different sites. The number of TRs observed for each country was as follows : Ukraine (91); Germany (87); Denmark (54); Italy (47); Finland (45); Sweden

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(43); Poland (42); Croatia (36); Austria (35); Czech Republic (32); Russia (20); Norway (15); Slovenia (6) and unspecified (5). The largest number of TRs observed at one site (for a number of species) is 54 at Tisvilde Hegn (Denmark), only 15 sites had recorded > 10 TRs. It should be stressed that this review generally uses TRs as summarised by the authors (i.e. arithmetic mean) and, therefore, does not represent the entire population of individual TRs which will consist of many thousands. The TR values have either been directly taken from the published literature source (where soil, 520cm depth, and fruitbody contamination have been measured directly at the same time) or estimated where a fungi activity has been quoted along with a soil deposition level derived from an aerial gamma survey. If an estimate of initial Chernobyl deposition has been reported by the author this has been used to derive the TR. In this review TR values are presented on a dry weight basis (i.e. m2 kg-1 DW), when reported as fresh weight a conversion has been made assuming a dry matter content percentage of 10%. The average dry matter percentage observed from over 1900 fruit body samples (272 species) by Fraiture et al. (1989) was 7%, with an interquartile range between 6 and 9%, so that such an assumption is unlikely to introduce a significant source of variation. Due to the rather piecemeal way that TRs have historically been reported in the literature (necessitating the data handling outlined above) TR values reported as being obtained by individual authors in this paper may differ from the transcript from which they were derived. Such an approach is required to allow a proper comparison between authors and across species to be made.

Belgium data set The activity of 1927 fungi samples were measured by Fraiture et al. (1989) over two fungi seasons, 1986 and 1987, in the Wallone region of Southern Belgium from 120 different sites

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(nearest settlement names were recorded). The latitude and longitudes were obtained from a suitable Gazetter using the settlement names as geo-references. A
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Cs deposition map for the

region was generated from 57 observations of soil deposition (Simon Wright, ITE, personal communication) to allow estimation of the TRs at each sample location. A total of 1811 TRs were generated (116 samples had no geo-reference). The primary use of this data set was to study the spatial variation of fungi 137Cs activity.

NU97 DATA SET SUMMARY Comparison between NU97 data set values and individual authors The data collated from all of the literature sources (Table 1) are summarised by genus and species in Table 2 and Table 3, respectively. Only those genus or species which have five or more reported values are shown, whilst the statistics presented are derived from the mean TR values reported in the literature. The mean, median and ranges reported by individual authors at specific sites are also indicated for a particular genus or species as a comparison to the statistics derived over the whole literature data set.

Genus A total of 44 different genus have been found with at least one estimated TR value in the literature review, with number of TR values reported within each genus varying between a single entry (e.g. Calocybe) to as many as 132 for the genus Boletus (Table 2), making direct comparisons between genus difficult. The majority of genus show TR distributions which are positively skewed, with the degree of skew increasing significantly with sample size (P<0.05). For eight out of the ten genus which have ranges of TRs reported for individual sites the limits of the range are in good agreement with those derived from the whole NU97 data set (generally

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within a factor of 2 to 3). The exception to this observation are the Paxillus and Suillus genera with reported site minimum TR values an order of magnitude higher than that suggested by the NU97 data set. In general, it appears that the variation found by individual authors is similar or consistent to the variation found across a larger range of conditions over the whole of Europe (this is discussed in more detail below). The Boletus genus exhibits the largest variation in TR values with three orders of magnitude difference between the extremes (0.0025-11.6 m2 kg-1 DW), whilst the smallest within genus variation is at least one order of magnitude (e.g. Collybia).

Species Aggregated transfer ratios for a total of 132 different species have been obtained (20 are listed in Table 3), with the number of reported TR values varying between 1 (e.g. Agaricus campestris) and 59 (Boletus edulis). As with the genera a comparison of the statistics between species is difficult due to the different population sizes involved. The range of TRs for individual species observed by individual authors at specific sites is similar to that derived over the NU97 data set (Figure 1 and Table 3), suggesting statistics derived from the latter may be used to estimate the Cs transfer from an individual species with as much uncertainty as using site specific data. Dahlberg et al. (1997) found 60% of the total variation in 137Cs activity of individual fruitbodies of Suillus variegatus was accounted for by the variation within-populations (i.e. found at the same site and/or genetically affiliated) whilst 40% could be attributed to the variation between populations (i.e. between sites). They suggested the large within site variation could be due to a number of contributing factors. The findings of Dahlberg et al. (1997) combined with the NU97 data set findings (Figure 1) supports the hypothesis that the variation in TR for a given species at a specific site is similar to the variation over a range of sites, so that the NU97 data set provides a possible reference data base to describe the 137Cs transfer to specific fungi species across a range of sites.

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The two main exceptions are provided by Leccinum versipelle and Rozites caperatus with maximum NU97 TR values approximately 10% and 400% those obtained by individual authors. The most variable species is Boletus badius, with TRs between 0.01 and 10 m2 kg-1 DW (NU97), and generally the Boletes exhibit 2-3 orders of magnitude differences between minima and maxima. The Lactariae species show differences of 1-2 orders of magnitude, whilst the least variable genus would appear to be Cantharellus with differences closer to 1 order of magnitude. The effect of land type on TR values is indicated by vadlenkov et al. (1996) in Table 3, with considerably higher Cs accumulation prevalent in the mountain landscape, compared to the lowland agricultural area, for the same species. However, insufficient information has generally been reported by individual authors to make a statistical assessment of land-use and type, foresttype or similar factors impossible. All species listed in Table 3 are edible according to Dickinson and Lucas (1979) and Kaltchenko (1997). Of the 26 commonly eaten species within the Ukraine (Kaltchenko, 1997) 10 are listed in Table 3, with coverage generally lacking for the Russula species. This data provides a useful guide to the likely contamination for a given soil deposition (see Discussion).

EFFECT OF FUNGI NUTRITIONAL TYPE Reporting of site specific conditions such as fungi fruitbody habitat, forest type and soil properties is generally poor within the literature so that it was not possible to derive any relationships or classification using such variables within this study. However, it was possible to classify the fungi into three nutritional types based on the type of substrate from which the mycelium derives its nutrients (Guillitte et al., 1990; Juliet Frankland, ITE personal communication): mycorrhizal or symbionts (M); saprophytic (S) and parasitic (P). The

mycelium of mycorrhizal species are associated with fine roots of higher plants which supply them with hydrocarbons whilst they aid roots to extract mineral salts from the soil. Saprophytic

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species derive nutrients by decomposing the litter layer through enzyme excretion, whilst parasitic species derive resources directly from higher plants. The NU97 data set provided 709 values of fungi activity (534 M, 156 S and 19 P) and 530 TRs (440 M, 78 S and 12 P). These are unbalanced and consequently the use of ANOVA was not appropriate (Robinson, 1987). Therefore, the method of residual maximum likelihood (REML) was used to estimate the effect of nutritional type (fixed model) and variance components in a linear model with no random effects assumed, only random error (Genstat 5 Committee, 1993). The REML analysis for the nutritional types is summarised in Table 4, with effects presented relative to the mycorrhizal species. For both the fungi activity and TR there are significant (P<0.025) differences between the uptake of the different nutritional types in the order mycorrhizal > saprophytic > or parasitic. Therefore a classification based on nutritional type is justified, over this wide range of conditions and initial deposition levels. A number of authors have also attempted to classify levels of
137

Cs or transfer factors based on

an ecological nutritional approach (Giovani et al., 1990; Guillitte, 1990; Belli and Tikhomirov, 1996 and Yoshida and Muramatsu, 1994). It is generally accepted that radiocaesium

discrimination (compared to potassium) occurs during transfer from the fungi mycelium into root cells (Byrne, 1988; Kammerer et al., 1994; Wirth et al., 1994) so accumulation of 137Cs is higher for mycorrhizal (or symbiotic) species (e.g. Guillitte et al., 1994). However, transfer may also be affected by infection or co-existence of species with differing levels of Cs-affinity (Aumann et al., 1989). The effect of vegetation cover or habitat in which the fungi fruitbodies were collected was investigated for the calculated TRs of the Belgium data set, in which a total of 14 different habitats were recorded by (Fraiture et al., 1989). The most commonly collected mycorrhizal species, Russula ochroleuca, across the largest number of sites (62) was used with the fixed model defined as habitat type and the random model as the site. The habitat type effect was

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significant (P<0.001), with the following order of TR : spruce beech > oak (habitat codes as reported by the authors). This demonstrates for a particular species
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Cs transfer will vary

according to the type of tree beneath which it is found, at least within the first few years after a deposition event (samples were collected in 1987 and 1988). This may reflect differences in tree architecture, litter fall, and leaf decay. Fraiture (1992) summarises the major mechanisms by which initial deposition patterns may vary spatially beneath canopies of different tree species. The effect may be less marked after a period of time when needle shedding and continued weathering within coniferous trees will re-distribute the initial deposit onto the forest floor, although needles are normally retained for between 3 to 6 years reducing the total contamination due to radioactive decay (Fraiture, 1992). However, the importance of spatial variability in soil deposition (due to initial canopy interception) within a forest stand may be reduced as the mycelium of individual fungi species have been observed to spread over many square metres (Dahlberg, 1997).

FREQUENCY DISTRIBUTION FUNCTIONS TO DESCRIBE 137CS TRANSFER Two types of standard probability distribution function were fitted to the two TR data sets (NU97 and Belgium) : Normal and Log-normal. The TRs were classed into genus, species and

nutritional type and the distributions were fitted, using Genstat version 3.22 (Genstat 5 Committee, 1993), with the number of class intervals equal to the square root of the number of observations. This inevitably resulted in unequal class intervals between different species, genus and nutritional type. Distributions were not fitted to data sets that had less than 18 TR values. In each case it was possible to determine the most appropriate distribution for the underlying data set, based on the deviance between the expected and observed frequency of TR values in each TR class interval.

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For the best-fitting distributions for individual and pooled species (see below), the distribution parameters ( and with standard errors) are listed in Table 5. The distribution pattern of 137Cs transfer factors and activities has generally been found to be log-normal (e.g. Mietelski et al., 1994; Yoshida et al., 1994), which is consistent with the findings in this review (the TRs for only three of the 24 species listed in Table 5 are normally distributed). Jacob and Likhtarev (1996) presented (as graphs) species specific distributions for mushroom
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Cs transfer factors

for eight common species found in Belarus. Four of the five species common to both this review and their data set showed similar TR distribution patterns (Boletus badius, Boletus edulis, Russula ochroleuca and Cantharellus cibarius) with TRs for Armillaria mellea indicated as being normally distributed in their data set. The Belgium data set provides the majority of species listed in Table 5 and it is assumed that these will be representative on a larger scale. Generally, the differences between the observed and fitted distributions are not significant (P>0.05). The fitted parameters for individual species were ranked and the differences between them for species of similar rank were tested for significance (t-test). If the differences were not significant (P>0.05) the data sets were pooled and the distribution function re-fitted to the pooled observations. The result of pooling data sets is shown in Table 5 by grouping species with the same fitted distribution parameters. In some cases (e.g. Paxillus involutus and Boletus badius) it was necessary to re-normalise the frequency distribution to allow for that part of the function below zero. The effective transfer ratios were generated using the modelling approach outlined below (see Modelling Approach). The fitting of frequency distribution patterns were also investigated for the data grouped by genus and nutritional type but the results were generally poor (data not shown). If only the genus of a particular fruitbody collected could be determined then derived genus parameters could be used albeit with less accuracy than if the species parameters were applied.

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The Belgium data set (n>20) exhibited a significant exponential relationship (P<0.001) between the median TR and measure of skew which indicates that high accumulating species (e.g. Cortinarius anomalus) tend to be normally distributed whilst low accumulating species (e.g. Boletus subtomentosus) are log-normally distributed.

EFFECTS OF TIME The effect of physical decay has already been taken into account so this analysis considers only the ecological half-life. A total of 549 TRs for mushrooms species in the NU97 data set had a defined sampling date. Five hundred are classed as
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Cs contamination arising from the

Chernobyl accident (i.e. the effect of environmental 137Cs due to weapons tests has been removed or only Chernobyl fallout has been assumed by the authors). The number of TRs reported per year is very variable ranging from less than 20 to 140 (Figure 2). The most extensive species with time-series TR data are (number in brackets) : Boletus edulis (59); Boletus badius (52); Paxillus involutus (39); Lactarius rufus (27); Cantharellus cibarius (25) and Lactarius necator (24). The remaining species all have time-series datasets less than 10. The time-series data for the above species are summarised in Figure 3, with median values plotted together with the inter-quartile range. The only species to exhibit a significant relationship with time are both from the genus Lactarius (rufus and necator) with TR values increasing with time (P<0.05). These are both mycorrhizal species (as are all the others shown in Figure 3) and it is not clear why this particular genus should exhibit such a relationship. Conversely, Amundsen et al. (1996) observed a statistically significant (P<0.05) exponential decrease with time in the activity level of Lactarius torminosus at two sites in Norway (over the period 1989-1995) with effective ecological half-lives of

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between 2 and 5 years. This contrasting finding may be a consequence of using heterogeneous data taken over a large spatial scale in this study (Europe and the CIS) and probably greater between site variability in terms of experimental procedures, climate, soil type and land use. However, other authors have (over shorter time periods of 4-5 years) found both an increase (Borio et al., 1991) and no significant decrease in activity levels (Kammerer et al., 1994) of various fungi species. Analysis of the NU97 data set (using a variety of sources from Europe and CIS) indicates that generally there is no statistical evidence to indicate any significant decrease in TRs close to 10 years after the Chernobyl accident. This may suggest that contamination levels of common mushroom species are approximately constant, though data heterogeneity makes a definitive conclusion difficult. However, some site specific data sets (within the NU97 data set) could be analysed for time dependency using the data reported by Belli and Tikhomirov (1996) in Russia and Ukraine, with time series (n 4) per site for a particular species. Three species were considered : Lactarius necator; Lactarius rufus and Paxillus involutus. As an example, the time series for the former are presented for 4 different sites in Figure 4. These time series were analysed to determine the lines of best fit (assuming a straight line model with either negative or positive slope) which are plotted as the solid lines. The effect of site was also tested to determine if the slopes (and intercepts) were significantly different between sites. Significantly different intercepts (P 0.01) were found for each site (for a particular species), suggesting initial site properties such as soil, forest/land type and form of deposition (distance from source) will be important in determining the initial post deposit transfer factor. For two of the species, Lactarius rufus and Paxillus involutus, no significant differences (P > 0.05) in the rate at which the TR values are increasing or decreasing across sites (respectively) were found. Three out of the four sites for Lactarius necator indicated a negative intercept which may suggest a linear function may not be the most appropriate model, whilst at the remaining site (Dityatky,

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28.5km S of Chernobyl) the TR was apparently decreasing with time (Figure 4). In some instances a better fitting exponential model could be applied, although this sort of model (implying increasing or decreasing rates of 137Cs uptake) was not considered as meaningful. It is clear that the fitted trend line for site D1 (Figure 4) is dependent on the recorded TR 7 years after the initial deposition, so that it could be argued that a better description would be achieved with a slope of 0 followed by a year in which transfer was exceptionally high. Rhm et al. (1998) grouped 14 mushroom species collected within a coniferous forest near Hochstadt (Bavaria) into four groups depending on the location of their mycelium within the organic-mineral soil layers, derived from observations of the 137Cs : 134Cs ratio. By representing soil horizons as a five compartment model they deduced ecological half-lives ranging from 2.8 (litter horizon) to 7.7 years (upper mineral horizon), with different mushroom species exhibiting decreasing (mycelium in litter and organic layers), constant (mycelium solely in organic layer) and increasing (mycelium in organic and mineral layer) contamination dependent on which combination of horizons their mycelium exploited. It is expected that the ecological half-lives (and TRs) they obtained are site-specific (Rhm et al., 1998) due to local soil attributes (e.g. clay content), forest type and vary between seasons due to climatic influences on soil humidity and fruitbody age. The latter two factors may help explain the non-significant coefficients of determination they obtained. Although evidence exists to suggest that transfer of
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Cs to fungi does show time dependency,

this study of the available data indicates no clear effect of time can be deduced. Amundsen et al. (1996) suggest that a period of observation of an individual species (15-50 samples) at the same site for 6-7 years may not be long enough to determine a precise ecological half-life of fungi beyond concluding that it may approach the physical half-life.
137

Cs in

348 349 350 351 352 353 354 355 356 357 358 359 360 361 362 363 364 365 366 367 368 369 370 371 372 SPATIAL VARIATION The Belgium data set provides good spatial coverage of both activities and TRs for fruitbodies, with observations at 120 sites within the Wallonne Region in Southern Belgium (approximately 200km by 150km). It was proposed that analysis of the spatial correlation of the variation between sites would indicate over what scale it would be important to predict or estimate accurately the mushroom fruitbody activity or TR. The hypothesis was that the variation in radiocaesium transfer within a site was as large as that between sites (as suggested by the findings of Dahlberg et al., 1997). This could be tested by describing the spatial continuity in terms of an experimental variogram whereby the difference between sites is a function of the distance between them (Burrough, 1997). The Belgium data set provided a 2 sets of data which enables this hypothesis to be tested: 1. fungi activity and TR across all sites and species (n=120); 2. fungi activity and TR for one species, Russula ochroleuca (n=62). The pattern of the experimental variogram obtained by using the activity and TR was very similar and therefore only the activity data is described in this analysis (i.e. no assumptions for soil deposition were required). Data set 1 provided the most complete data set (in terms of spatial coverage) but had the disadvantage of incorporating the variation in 137Cs uptake due to different species, whereas data set 2 provides the most complete data set for a particular species not incorporating any species variation. At least 50-100 geo-referenced data points are required to achieve a stable variogram (Burrough, 1997) limiting the analysis to one particular species (Russula ochroleuca). In both cases, the fungi activity are positively skewed and it was necessary to transform the data (natural logarithm) as suggested by Burrough et al. (1996). The experimental variograms fitted

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in this study were omnidirectional, i.e. the data was sufficiently isotropic in all directions to negate the requirement for an analysis in specific directions. Standard rules of thumb were used to determine suitable values for the cut-off width or maximum lag distance and the lag increment (for example: EPA, 1991; Isaaks and Srivastava, 1989; and PCRaster, 1996). The GEOEAS version 1.2.1 software (EPA, 1991) was used. The cut-off width was taken as

50,000m whilst the lag increment was varied between 4000 and 10,000m. The experimental semi-variograms for the transformed fungi activity across all species for the 120 sample sites are shown in Figure 5 for a range of lag increments. A relatively stable structure is indicated for lag increments greater than 5000 m at distances of more than 5000m. The sampling strategy of the Belgium study limits the interpretation of the variation to be expected at such small distances (average nearest neighbour distance for the 120 sites is 8400m). This result suggests there is no distance-fungi activity variation relationship, with most of the difference between 137Cs uptake occurring over a relatively small scale (< 5 km). In other words, within the limitation of the data set it is possible to conclude that the variation within a forest site may be as large as the variation between sites. Dahlberg et al. (1997) studied the variation of
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Cs activity in individual fruitbodies of Suillus

variegatus at 7 sites over areas less than 50m by 50m. Their findings indicate that most of the variation occurred over very small distances, at scales that would be difficult to predict without very detailed soil and habitat information. Analysis of data at such a detailed scale could be useful in clarifying further the spatial continuity of mushroom contamination by 137Cs. When just one particular species (Russula ochroleuca) observed at 62 sites is analysed a markedly different pattern of variation is found (Figure 6), especially over the first lag increment. Although, the variation for one species is only slightly lower than that obtained over a large number of species. The more limited spatial coverage results in only 10 pairs in the first lag at an increment of 7km, rising to 38 pairs for a 10km increment. At the latter increment no discernible

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spatial pattern is evident, whilst at the lower lag increment sizes it would appear the variation actually increase at locations closer together. The data set suggests at distances up to 5-10km the variation in fungi activity for one species is as large at that experienced over greater distances.

MODELLING APPROACH The spatial analysis of the Belgium data set indicates variability of
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Cs transfer within a

sampling location such that fruitbodies collected over an area on a scale of approximately 5km would show activities as variable as those collected over a much larger scale. Therefore, a typical mushroom gatherer who, over the course of a mushroom season, may gather this particular product from a relatively large area (perhaps a number of forest locations or forests) would be expected to collect fruitbodies with highly variable activities. Thus, the majority of the variation in
137

Cs uptake may occur over a scale smaller than the mushroom gatherer collects

mushrooms. In this case using an effective TR for a particular species, derived from the distribution parameters for individual species (Belgium and NU97 data sets, Table 5), would give a more reliable estimate of the
137

Cs transfer ratio. The effective species TR (TRi effective) can

be calculated using the fitted distribution parameters (Table 5) as described by Equation 1.

414 415 416 417 418 419 420 where :

TRi effective =

pdf TRi dTRi

0

Equation 1

TRi effective = effective transfer ratio for species i (m2 kg-1 DW); pdf = the probability density or frequency distribution function. The effective TR represents the TR that should be applied if it is assumed that a sample is drawn from the p.d.f.s given. The effective TRs estimated using Equation 1 and confidence intervals (68%) are also given in Table 5.

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An estimate of the total 137Cs activity a mushroom gatherer would collect is given by Equation 2.

Activityi = B D TRi effective

where :

Equation 2

Activityi = total activity in mushrooms gathered for species i (Bq); Bi = total biomass of fungi species i collected (kg DW); D = soil deposition level (decay corrected) in area of mushroom picking (Bq m-2). The total weight of fungi collected could be easily determined (e.g. Voigt et al., 1998), and a dry weight fraction of 10% could be assumed to convert to dry matter. This total activity combined with daily consumption patterns and the appropriate dose conversion factors could be used to estimate the daily intake due to this particular semi-natural product for each species collected. Due to the incorporation of the spatial variation within the distribution parameters of Table 5 this approach assumes the gatherer would sample from the entire population of TRs, which would be valid if fungi were collected over an area on a scale of at least 5km. Consequently this method may only be appropriate for estimating the collective dose to a population, rather than the individual dose. Uncertainties in the distribution parameter estimates have been used to generate confidence intervals for the effective TRs, providing estimates for the uncertainty in corresponding dose estimates. The frequency and effect of culinary practices (processing factors) on the modification of the potential activity (derived from Equation 2) have been studied and quantified (Jacob and Likhtarev, 1996; Beresford et al., 1998), and these could be combined with the proposed model to estimate the effective activity within mushrooms consumed by the general population.

443 444 445 446 447 448 449 450 451 452 453 454 455 456 457 458 459 460 461 462 463 464 465 466

DISCUSSION Methodological differences between authors may account for some of the variation in transfer ratios reported within this paper. For example, use of soil deposition levels estimated from field or aerial gamma surveys and rainfall measurements (e.g. vadlenkov et al., 1996; Elstner, 1989) will be less representative of the localised soil contamination (e.g. Guillitte et al., 1994) which varies markedly within forest ecosystems (Fraiture, 1992; Wirth et al., 1994). Some authors report soil activity concentrations (e.g. Heinrich, G., 1992) and TFs (Yoshida et al., 1994) so TRs cannot be derived from the data sets, whilst some of the literature data sets have not been used because measured soil depositions have not been reported (Yoshida et al., 1994) or definition of units used are not clear (Tsvetnova et al., 1994). Andolina and Guillitte (1990) presented a methodology for soil sampling within forest ecosystems and suggest a standardisation of methods to enable comparisons between studies. Consideration, of the
137

potentially large scale (many square metres) over which fungi mycelium can take up

Cs

indicates an appropriate scale for soil sampling. Smith et al. (1993) found that between 10 and 20 individual fungi fruitbodies were required (based on the measured activity concentrations) in order to lie within a factor of two of the log-mean activities. It is reasonable to assume that a similar soil sample size would be required to achieve the same level of accuracy within heterogeneous forest sites. Analysis of time series TRs at a number of sites in Russia and the Ukraine (Belli and Tikhomirov, 1996) indicates the rate of increase (Lactarius rufus) or decrease (Paxillus involutus) of TR is similar across sites, though for some species (Lactarius necator) variation does occur (Figure 4). Considering TR time series data set averaged over a large spatial scale (Figure 3), it is apparent that there is no strong evidence to suggest TRs have decreased since the Chernobyl accident. Although, some authors (Rhm et al., 1998) have provided evidence for

467 468 469 470 471 472 473 474 475 476 477 478 479 480 481 482 483 484 485 486 487 488 489 490 491

and quantified the decrease in fungi TRs at particular sites, with ecological half-lives between 3 and 8 years dependent on nutritional source. Generally, some or all of the detailed meta-information required for a study of this nature (such as habitat, sample location relative to trees, localised climate, soil nutrient status and attributes) is not reported so that classification schemes are often limited to generic nutritional types. Problems also arise in analysing population means and individual population data together. It is suggested that a greater understanding of the mechanisms governing 137Cs transfer to mushroom fruitbodies would be achieved through a thorough re-evaluation of existing raw data sets and the reporting of meta-information in greater detail and a consistent manner. This may prove a costeffective and beneficial approach providing a data base for semi-natural products equivalent to that presently constructed for agricultural products by the International Union of Radioecologists (Sheppard and Evenden, 1997). This study also highlights a need for further clarification of the role of soil nutrient status upon the long-term uptake of radiocaesium within the fungi mycelium and the dynamics and transport to fruiting bodies within field settings to determine the relative importance of the local microclimate (temperature and humidity). Such studies should

concentrate on single species which are suited to study both in the field and laboratory studies (for example Dahlberg et al., 1997). It may then be possible to develop a generic modelling approach (not based on transfer factors) for the transfer of radiocaesium to fungal sporocarps similar to that developed for vascular plants by Absalom et al. (1999). The proposed modelling approach, using species specific characteristics (parameters for the mean, variance and assumed distribution pattern), is consistent with the hypothesis of Tsukada et al. (1998) that physiological differences between species of mushrooms causes the large fluctuations in radiocaesium activity concentrations between species, as reported by many authors for both
137

Cs (e.g. Kammerer et al., 1994; Yoshida et al., 1994) and stable Cs (Seeger

and Schweinshaut, 1981). The approach also agrees with evidence provided from the spatial

492 493 494 495 496 497 498 499 500 501 502 503 504 505 506 507 508 509 510 511 512 513 514

analysis of the Belgium data set, which indicates that on the scale of mushroom gathering (over a season) the variability in fungi fruitbody 137Cs transfer will be high.

CONCLUSIONS This review of transfer ratios has shown : variation in species TRs measured across Europe and the CIS is similar to that observed by authors at individual sites; confirmation of significant differences (P<0.025) in the uptake of nutritional type (M > S P); in general no significant time dependency in TRs can be deduced across such a heterogeneous data set; the variation in TRs to be relatively constant when collected over distances greater than about 5km; species specific frequency distribution parameters can be used to estimate an effective TR to be used for predicting doses to populations from this semi-natural product.
137

Cs by fungi of different

Acknowledgements The authors are grateful to Cath Barnett, Simon Wright and Brenda Howard (ITE) for their contribution and helpful comments in developing the data base. This study was supported financially by the European Commission (Contract F14P-CT95-0015 and Contract F14P-CT950021c) and this support is gratefully acknowledged.

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726

726 727 728 729 730 731 732 733 734 735 736 737 738 739 740 741 742 743 744 745 746 747 748 749 750 751 752 753 754 755 756 757 758 759

Figure Captions

Figure 1 Range of aggregated transfer factors, TR (m2 kg-1 DW), observed by individual authors at specific sites compared to that found across the whole literature search (NU97) Figure 2 Variation of TR values obtained and number recorded from published sources for each year since the Chernobyl nuclear power plant accident

Figure 3 TR time-series data for the most commonly recorded species, median values and interquartile range (n>20) obtained across a number of sites (NU97 data set). Note the last data point in the Lactarius rufus time-series is excluded from the regression line

28.5km S of Chernobyl (Ukraine); K1=Klintsy, Bryansk province, 210km NE of Chernobyl (Russia); S1=Shepelitchy, Kiev province, 7km W of Chernobyl (Ukraine))

Figure 4 Time series TR data for Lactarius necator for individual sites (taken from Belli and Tikhomirov, 1996) (D1=Dityatky, Kiev province, 26km S of Chernobyl (Ukraine); D2=Dityatky, Kiev province,

Figure 5 Experimental semi-variogram of fungi activity over all sites and species for the log transformed Belgium data set (see text for details)

Figure 6 Experimental semi-variogram of fungi activity over 62 sites for one species, Russula ochroleuca, for the log transformed Belgium data set (see text for details)

Gillett and Crout

A review of 137Cs transfer to fungi : importance of species, spatial scale and time

Fig. 1

12.0 10.0 8.0 6.0 4.0 2.0 0.0

Boletus badius

12.0 10.0 8.0 6.0 4.0 2.0

Boletus chrysenteron

2.0

Boletus edulis

1.0

KAM94

RAN90

SMI93

TEH88
RAN90c

HOW94a

HOW94b

HOW94b

HOW94a

HOW94b

HOW94d

HOW94e

HOW94c

3.0

Cantharellus cibarius

3.0

Cantharellus tubaeformis

2.0

2.0

1.0

1.0

KAM94

RAN90a

HOW94b

HOW94b

HOW94b

HOW94b

HOW94a

HOW94b

HOW94b

7.0 6.0 5.0 4.0 3.0 2.0 1.0 0.0

RAN90a RAN90b

HOW94b

HOW94b

RAN90c

RAN90b

RAN90a

SVA96a

SVA96b

RAN90c

KAM94

NU97

NU97

0.0

0.0

HOW94f

Lactarius rufus

7.0 6.0 5.0 4.0 3.0 2.0 1.0 0.0

Lactarius torminosus

7.0 6.0 5.0 4.0 3.0 2.0 1.0 0.0

Lactarius trivialis

HOW94b

HOW94c

KAM94

ELS87

NU97

SVA96a

SVA96a

SVA96b

SVA96b

NU97

HOW94b

4.0

9.0

Leccinum versipelle

Paxillus involutus

8.0 7.0 6.0 5.0 4.0 3.0 2.0 1.0 0.0

SVA96a SVA96b NU97

3.0

2.0

1.0

KAM94

FRA92

ELS87 = Slovenia, 1987 FRA92 = Slovenia, 1986 KAM94 = unknown site, 1988-91 HOW94a = Austria, 1987-91 HOW94b = Finland, 1984-91 HOW94c = Germany, 1987 HOW94d = Czechoslovakia, 1988 HOW94e = Austria / Germany, 1988-91 HOW94f = Norway, 1988

HOW94b

HOW94b

HOW94b

HOW94b

RAN90a = Finland, 1986 RAN90b = Finland, 1987 RAN90c = Finland, 1988 SMI93 = Finland, 1993 SVA96a = Czech Republic, (mountain landscape) SVA96b = Czech Republic, (agricultural landscape) TEH88 = Czech Republic, unknown date

HOW94b

HOW94b

RAN90a

RAN90b

NU97

NU97

0.0

11.0 10.0 9.0 8.0 7.0 6.0 5.0 4.0 3.0 2.0 1.0 0.0

Rozites caperatus

HOW94b

HOW94b

HOW94b

HOW94b

RAN90c

SVA96a

SVA96b

RAN90a

RAN90b

RAN90c

RAN90a

RAN90b

NU97

NU97

NU97

NU97

0.0

0.0

Gillett and Crout

A review of 137Cs transfer to fungi : importance of species, spatial scale and time

Fig. 2

100

160 140 120

10

1 TR (m2 kg-1)

100 80 60 40

0.1

0.01

0.001

20 0 0 1 2 3 4 5 6 7 8 9 10 Years since the Chernobyl Nuclear Power Plant Accident

0.0001

Number of TR' s reported

Gillett and Crout

A review of 137Cs transfer to fungi : importance of species, spatial scale and time

Fig. 3
Boletus edulis (n=59), 22 sites y = 0.0053x + 0.0793 R2 = 0.0188 Boletus badius (n=52), 19 sites y = -0.0294x + 1.7094 R2 = 0.015

0.60 0.50

5.00 4.00 3.00 2.00 1.00 0.00

TR (m kg-1DW)

0.40 0.30 0.20 0.10 0.00 0 6.00 5.00 1 2 3 4 5 6

0 1.00 0.90 0.80 0.70 0.60 0.50 0.40 0.30 0.20 0.10 0.00

Paxillus involutus (n=39), 12 sites y = 0.1081x + 0.8902 R2 = 0.2761

Cantharellus cibarius (n=25), 19 sites

y = 0.029x + 0.1415 R2 = 0.3788

TR (m kg-1DW)

4.00 3.00 2.00 1.00 0.00 0 7.00 6.00 1 2 3 4 5 6 7 8 9

0 2.00 1.80 1.60 1.40 1.20 1.00 0.80 0.60 0.40 0.20 0.00

Lactarius rufus (n=27), 8 sites

Lactarius necator (n=24),6 sites

TR (m kg-1DW)

5.00 4.00 3.00 2.00 1.00 0.00 0

y = 0.4137x + 0.0763 R2 = 0.861, P < 0.05

y = 0.0839x - 0.077 R2 = 0.6702, P < 0.05

years since Chernobyl

years since Chernobyl

Gillett and Crout

A review of 137Cs transfer to fungi : importance of species, spatial scale and time

Fig. 4
S ite D 1 Site D 2

1.6 0 1.4 0

0.1 2 0.1 0

TR (m kg DW)

1.2 0 1.0 0 0.8 0 0.6 0 0.4 0 0.2 0 0.0 0 0 1 2 3 4 5 6 7 8 0.0 2 0.0 0 0 1 2 3 y = 0 .2 56 9 x - 0.7 66 6 R 2 = 0 .64 1 7 0.0 8 0.0 6 0.0 4

y = -0.0 1 16 x + 0 .11 4 9 R 2 = 0 .4 3 6

-1

1.2 0 1.0 0 0.8 0

S ite K 1

0.6 0 0.5 0 0.4 0 0.3 0 0.2 0 0.1 0 0.0 0

S ite S 1

y = 0 .20 5 3x - 0.2 25 1 R 2 = 0 .8 2 1 4

y = 0 .0 88 x - 0 .0 6 9 3 R 2 = 0 .81 9 5

TR (m kg-1DW)

0.6 0 0.4 0 0.2 0 0.0 0 0 1 2 3 4 5 6

years since C herno byl

years since C hernob yl

Gillett and Crout

A review of 137Cs transfer to fungi : importance of species, spatial scale and time

Fig. 5

2.5

Fungi activity (transformed) semivariance

lag increment (m)

1.5

6000 7000 8000

0.5

0 0 5000 10000 15000 20000 25000 30000 35000 40000 45000 50000 55000 60000

Distance (m)

Gillett and Crout

A review of 137Cs transfer to fungi : importance of species, spatial scale and time

Fig. 6

1.8 1.6 1.4 1.2 1 0.8 0.6 0.4 0.2 0 0 5000 10000 15000 20000 25000 30000 35000 40000 45000 50000 55000 60000

Fungi activity (transformed) semivariance

lag increment (m) 7000 8000 9000 10000

Distance (m)

Gillett and Crout

A review of 137Cs transfer to fungi : importance of species, spatial scale and time

Table 1 Summary of data as reported by author in the literature data base (NU97 data set)
REFERENCE FUNGI SOIL OTHER Land-cover (arable or forest type)

Number of species studied Activity (Bq/kg) SD TR (m/kg) SD Range (min-max) TF (Bq/kg fungi / Bq/kg soil) SD Cs 137:134 ratio Deposit (Bq/m) Observed / Estimated Concentration (Bq/kg) Observed / Estimated Cs 137:134 ratio Soil Type Soil Attributes (e.g. % clay)

AUTHORS

Amundsen et al. (1996) 10 O O Battiston et al. (1989) 15 O O Belli and Tikhomirov (1996) 14 O O Bem et al. (1990) 8 E O Byrne et al. (1988) 6 E Elstner et al. (1987) 17 E O Elstner et al. (1989) 32 O O Franic et al. (1992) 20 O O Giovani et al. (1990) * O Guillitte et al. (1994) 38 O O Heinrich et al. (1989) 9 O O Heinrich, E (1992) 8 E O Heinrich, G (1992) 113 O O Horyna and Rand (1988) 21 O O IAEA (1994) 9 O O Kammerer et al. (1994) 28 O Lux et al. (1995) 11 O O Mascanzoni (1990) 5 Mietelski et al. (1994) 6 Pietrzak-Fils et al. (1996) 2 O O Rantavaara et al. (1990) 8 Smith et al. (1993) 16 Strandberg (1992) 33 O O Svadlenkova et al. (1996) 8 O Teherani (1988) 5 E Wasser and Grodzinskaya (1993) 55 E O Zagrodzki et al . (1994) 1 E O Note : all weights refer to dry weight fungi or soil location refers to a site name that can be geo-referenced data reported for majority of species data reported for some species * miscellaneous macromycetes

Location

Gillett and Crout

A review of 137Cs transfer to fungi : importance of species, spatial scale and time

Gillett and Crout

A review of 137Cs transfer to fungi : importance of species, spatial scale and time

Table 2 Data summary for NU97 TR database by GENUS (n 5)

Genus Name n Geometric mean 0.2578 0.0347 0.2198 0.2800 0.2366 0.1444 1.2940 1.2964 1.9949 0.5194 0.1431 0.0431 0.0135 0.8598 0.1507 2.2206 0.4132 0.4902 Median LQ (25%) 0.0529 0.0127 0.0637 0.1632 0.2286 0.1337 0.9785 0.5472 0.6053 0.2434 0.0609 0.0224 0.0086 0.5703 0.0696 1.2228 0.2163 0.2937 TR (m2 kg-1 DW) UQ (75%) 1.0078 0.0962 0.9766 0.6206 0.6027 0.2603 3.2476 2.0565 5.4000 1.4593 0.3364 0.0756 0.0279 2.5558 0.2003 8.2789 0.8887 0.8652 Arithmetic Mean 1.0954 0.0626 0.7944 0.4356 0.4901 0.1874 2.5538 2.4092 3.8604 1.0526 0.2437 0.0945 0.0254 1.6498 0.2184 4.1137 0.7617 0.7301 Range Skew Literature TR values (m2 kg-1 DW) Range

Amanita 15 0.2736 0.0076-5.2485 1.94 Armillaria 10 0.0362 0.0064-0.177 1.05 0.0218 - 0.0502 Boletus 132 0.2444 0.0012-9.9758 3.81 0.0025 - 11.6 Cantharellus 50 0.2855 0.0108-1.5091 1.23 0.01 - 2.47 Clitocybe 7 0.4643 0.0103-1.2933 0.95 Collybia 9 0.2050 0.03-0.303 -0.61 Cortinarius 18 1.8656 0.0212-10.2381 1.83 0.0144 - 3.84 Hygrophorus 5 1.8300 0.2412-7.3712 1.83 Laccaria 5 2.0800 0.4309-10.7857 1.29 0.48 - 4.68 Lactarius 83 0.7237 0.0058-4.3808 1.45 0.015 - 6.31 Leccinum 23 0.1100 0.0155-0.885 1.30 0.005 - 0.74 Lycoperdon 11 0.0300 0.0088-0.514 2.61 Macrolepiota 12 0.0130 0.0007-0.1106 2.26 Paxillus 42 1.3668 0.0116-5.41 0.74 0.627 - 8.97 Ramaria 5 0.1981 0.0488-0.5753 1.64 Rozites 13 2.2500 0.08-10.9123 0.80 0.01 - 2.7 Russula 34 0.3616 0.0445-5.2704 2.98 Suillus 19 0.6964 0.0169-2.1019 1.04 0.175 - 4.800 Note : 1. statistics are calculated from all available TR values reported by individual authors and groups and so represent the best estimates over a range of sites and conditions; 2. the TR Literature ranges listed represent the minimum to maximum values observed/reported by individual authors within a Genus (not necessarily the same author(s), site or species); 3. the Skew statistic characterises the degree of asymmetry of a distribution around its mean.

Table 3 Data summary for NU97 TR data for edible SPECIES (n > 5)

Gillett and Crout

Median 0.0255 1.1708 0.0064-0.177 0.0066-9.9758 0.98 2.82 Range Skew Mean Reported literature TR values (m2 kg-1 DW) Median Range Author(s)

A review of 137Cs transfer to fungi : importance of species, spatial scale and time

Species Name

Armillaria mellea Boletus badius

9 53

Geometric mean 0.0329 0.9507

NU97 TR values (m2 kg-1 DW) LQ UQ Arithmetic Mean 0.0100 0.1095 0.0633 0.6467 2.1493 1.6285

Boletus chrysenteron

0.4790

0.6188

0.2200

1.6725

0.9722

0.03-2.6667

0.78

Boletus edulis

59

0.0643

0.1087

0.0191

0.2369

0.1572

0.0012-0.7994

1.59

Cantharellus cibarius

26

0.1761

0.2021

0.1279

0.3288

0.2374

0.0108-0.7187

1.18

0.0359 0.76 3.22 2.19 1.4876 0.79 1.84 0.4394 0.28 0.06 0.25 0.045 0.96 0.29 0.35 0.1625 0.665 0.0489 0.98 1.13 0.825

0.0349 0.372 2.30 0.8329 0.60 2.00 0.4757 0.33 0.05 0.0163 0.0288 0.96 0.20 0.28 0.1050 0.665 0.0489

0.0218-0.0502 0.048-2.64 0.44-7.1 0.43-6.1 0.5292-3.0183 0.01-2.07 0.165-4.11 0.32-0.5379 0.04-0.42 0.03-0.13 0.0025-1.6875 0.005-0.175 0.1798-1.7470 0.01-0.96 0.02-1.00 0.0137-0.4375 0.273-1.06 0.0291-0.0686

vadlenkov et al. (1996)d Elstner et al. (1987) IAEA (1994) Kammerer et al. (1994) vadlenkov et al. (1996)d IAEA (1994) vadlenkov et al. (1996)c vadlenkov et al. (1996)d IAEA (1994) Kammerer et al. (1994) Rantavaara et al. (1990) Smith et al. (1993) Teherani (1988) IAEA (1994) Kammerer et al. (1994) Rantavaara et al. (1990) vadlenkov et al. (1996)c vadlenkov et al. (1996)d

Cantharellus lutescens Cantharellus tubaeformis

9 11

0.3927 0.8013

0.2685 0.8250

0.1663 0.6800

1.3226 0.9200

0.6292 0.8243

0.0999-1.5091 0.55-1.18

0.73 0.50

Lactarius necator Lactarius rufusb

24 29

0.1671 1.1519

0.2152 1.2501

0.0820 0.7237

0.4126 2.3674

0.3144 1.6561

0.0058-1.388 0.0271-4.3808

1.91 1.02

Lactarius torminosusa Lactarius trivialisb 0.8030 1.3294 0.2718 0.0706 0.0390 0.0141 0.8627 1.4496 0.0300 0.0229 1.5731 1.4868 0.0249 0.0054 0.4956 0.9837 0.0686 0.0288 2.5878 2.8707 0.3500 0.0619 0.1823 0.0538 0.5310 0.1076 0.3907 0.0899 0.0574 0.0299 1.6907 2.5663 0.8625 1.9200 0.4778 1.3700 1.2844 2.1500 1.0792 1.7261

6 9

0.2544-2.7214 0.1-2.66 0.0322-0.885 0.0155-0.2868 0.01-0.2087 0.0007-0.1106 0.0116-5.41 0.08-10.1597

1.43 -1.05 0.50 2.23 2.24 1.84 0.66 2.26

1.375 2.61 0.6616 0.9375 1.37 0.8875 0.11 0.1213

1.08 1.12 0.8125 2.42 0.7625 2.58 0.6858 0.925 1.02 1.025 0.05 0.05

0.44-1.61 0.92-1.37 0.3875-1.425 1.43-6.31 0.1625-6.0875 1.05-4.52 0.4489-0.8510 0.4-1.5 0.07-3.47 0.0187-3.0 0.02-0.74 0.0125-0.5625

IAEA (1994) Kammerer et al. (1994) Rantavaara et al. (1990) vadlenkov et al. (1996)c Rantavaara et al. (1990) vadlenkov et al. (1996)c vadlenkov et al. (1996)d Rantavaara et al. (1990) IAEA (1994) Rantavaara et al. (1990) IAEA (1994) Rantavaara et al. (1990)

Leccinum scabrum Leccinum versipelle

9 11

Lycoperdon perlatum Macrolepiota procera Paxillus involutusa Rozites caperatus

9 9 40 10

1.0843 0.904 1.54 2.25

1.0843 0.880 2.15

0.6777-1.4956 0.084-2.48 0.78-2.30 1.89-2.70

vadlenkov et al. (1996)d Franic et al. (1992) IAEA (1994) Kammerer et al. (1994)

Russula ochroleuca 9 0.3062 0.3000 0.2302 0.3631 0.3564 0.125-0.9048 1.92 Suillus luteus 7 0.4225 0.2766 0.1810 0.9843 0.6936 0.1462-2.1019 1.41 Suillus variegatus 8 0.4161 0.6528 0.5047 0.7676 0.5940 0.0169-0.8804 -1.32 0.7125 0.6125 Footnotes : a edible if cooked; b inedible; c mountain landscape (Sumava, Czech republic); d agricultural landscape (Temeln, Czech republic).

0.175-1.700

Rantavaara et al. (1990)

Gillett and Crout

A review of 137Cs transfer to fungi : importance of species, spatial scale and time

Table 4 Fungi nutritional type 137Cs activities and TRs, means and effects as predicted by REML analysis for the NU97 data set

Data type/units Activity (Bq kg-1 DW) (NU97 data set)

TR (m2 kg-1 DW) (NU97 data set)

Nutritional type Mycorrhizal Parasitic Saprophytic Average S.E.D Maximum S.E.D Minimum S.E.D Wald statistic (D.F.) Mycorrhizal Parasitic Saprophytic Average S.E.D Maximum S.E.D Minimum S.E.D Wald statistic (D.F.)

Observations 534 19 156

440 12 78

Mean 25562 1671 11103 12332 15841 5933 7.8 (2) P<0.025 1.0001 0.3811 0.3551 0.3344 0.4287 0.1699 16.1 (2) P<0.001

Effect 0 -23891 -14459

0 -0.6189 -0.6449

Gillett and Crout

A review of 137Cs transfer to fungi : importance of species, spatial scale and time

Table 5 Statistics describing the distribution parameters for TRs of individual fungi species and proposed effective TRs (NU97 and Belgium data sets)
Dataset Species Best-ftting distribution log(X) log(X) log(X-a) log(X-a) log(X-a) log(X-a) log(X)1 log(X) log(X) log(X) log(X) log(X)2 log(X-a) log(X) log(X) log(X) normal normal normal n -0.0938 1.9016 2.2134 0.6779 0.6778 0.3928 -0.6127 -2.0204 -1.7287 -1.3542 -1.8564 -2.7436 -1.1215 -2.117 -2.246 -3.1491 10.633 4.9863 1.6907 se 0.4096 0.0641 0.4489 0.1119 0.1067 0.1961 0.1132 0.3483 0.1902 0.1298 0.1768 0.2122 0.4364 0.1989 0.1997 0.1856 1.2614 0.4543 0.2187 2.28 0.3202 0.4351 0.9865 0.728 0.636 1.2759 1.6331 1.2323 0.5506 1.0605 1.6295 0.4395 1.1426 0.9986 0.9994 6.9073 3.5182 1.3827 se 0.2897 0.0453 0.2005 0.0969 0.0772 0.1272 0.0801 0.2464 0.1345 0.0918 0.125 0.1501 0.1977 0.1407 0.1413 0.1313 0.8922 0.3213 0.1547 TReffective (m2 kg-1) 7.022 7.076 6.228 3.072 2.242 1.492 1.226 0.504 0.380 0.302 0.275 0.243 0.242 0.232 0.175 0.071 11.513 5.530 1.963 CI (68%) 2.839 11.840 5.700 0.608 0.630 0.529 0.231 0.268 0.100 0.042 0.061 0.080 0.162 0.060 0.043 0.016 1.264 0.456 1.370

BE Laccaria laccata 31 BE Cortinarius armillatus 25 BE Dermocybe cinnamomea 31 BE Tylopilus felleus,Laccaria amethystina,Boletus chrysenteron 164 BE & NU Cortinarius delibutus,Boletus badius 200 BE & NU Lactarius rufus,Cantharellus tubaeformis 61 BE Russula ochroleuca 127 BE Hydnum repandum 22 BE & NU Kuehneromyces mutabilis,Lactarius necator 42 BE Collybia butyracea 18 BE Boletus subtomentosus 36 NU Boletus edulis 59 NU Cantharellus cibarius 26 BE Lepista nebularis 33 BE Lepista nuda 25 BE Armillaria mellea 29 BE Cortinarius anomalus 30 BE Clitocybe clavipes & Cortinarius brunneus 60 NU Paxillus involutus 40 Note difference between fitted and observed distribution patterns significant at : 1 P<0.01; 2 P < 0.05; BE = Belgium data set; NU97 = Literature data set; n = number of TRs for which distribution was fitted; se = standard error of fitted parameter; TReffective = effective transfer ratio (see text for defintion); CI (68%) = 68% confidence interval for the effective TR. Definition of parameters normal distribution : mean = ; variance = 2 ; log normal distribution : mean =

a+e

2
2

variance =

e(

2 + 2

) e 2 1 .

Gillett and Crout

A review of 137Cs transfer to fungi : importance of species, spatial scale and