You are on page 1of 13

The Science of the Total Environment 267 Ž2001.

53 ᎐ 65

A dynamic compartmental food chain model of radiocaesium transfer to Apodemus syl¨aticus in woodland ecosystems
M.E. Toala,U ,1, D. Copplestonea , M.S. Johnsona , D. Jackson b, S.R. Jones b
b

School of Biological Sciences, Uni¨ ersity of Li¨ erpool, Li¨ erpool L69 3BX, UK Westlakes Scientific Consulting, Westlakes Science and Technology Park, Moor Row, Cumbria, CA24 3JZ, UK Received 22 February 2000; accepted 3 August 2000

a

Abstract A study was undertaken to quantify the activity concentrations of 137Cs in Apodemus syl¨ aticus Žthe woodmouse. in two woodland sites, Lady Wood and Longrigg Wood, adjacent to British Nuclear Fuels Ltd. ŽBNFL. Sellafield, Cumbria, UK. A deterministic dynamic compartmental food chain model was also constructed to predict 137Cs activity concentration wBq kgy1 dry weight Ždw.x in A. syl¨ aticus on a seasonal basis given the activity concentrations in its diet. Within the coniferous woodland site ŽLady Wood., significant differences were found between seasons Ž P - 0.05, summer vs. autumn cohort; P - 0.001, spring vs. autumn cohort., with an autumn peak in activity y1 concentration Žgeometric mean s 140= dw. being attributed to mycophagy. Fungal concentrations %2.3 Bq kg y1 ranged from 2 ᎐ 3213 Bq kg dw. The modelled activity concentrations fell between the confidence intervals of the observed data in four of the six seasonal cohorts sampled. Disparities between predicted and observed activity concentrations are attributed to uncertainties surrounding the fundamental feeding ecology of small mammals. ᮊ 2001 Elsevier Science B.V. All rights reserved.
Keywords: Woodland; Radiocaesium; Apodemus syl¨ aticus; Dynamic; Model

Corresponding author. Tel.: q44-1487-772400; fax: q44-1487-773467. E-mail address: mto@ceh.ac.uk ŽM.E. Toal.. 1 Present address: Centre for Ecology and Hydrology, Monks Wood, Abbots Ripton, Huntingdon, Cambridgeshire, PE28 2LS, UK. 0048-9697r01r$ - see front matter ᮊ 2001 Elsevier Science B.V. All rights reserved. PII: S 0 0 4 8 - 9 6 9 7 Ž 0 0 . 0 0 7 6 7 - 1

U

⌽ is the fraction of radiation absorbed by .. but this method is labour-intensive and prohibitively expensive for a wide range of biota. Internal dose rates are high. 1996. this tenet has been questioned by a number of authors ŽThompson.. Toal et al. UK ŽLady Wood. Radionuclide transport and dosimetry modelling Physically measuring the radiation dose absorbed by non-human biota is possible using implanted thermoluminescent dosimeters ŽTLDs. One method of assessing risk to natural ecosystems from xenobiotic chemicals is to estimate exposure to the most vulnerable wildlife receptor species in the ecosystem of concern. small mammals have been recognised as the wildlife group most likely to receive high doses in radionuclide-affected terrestrial ecosystems ŽMaslov et al. 1996. Ž1990. sterility and. r The Science of the Total En¨ ironment 267 (2001) 53 ᎐ 65 1. OSGR NY037045.. A previous study has investigated the transfer of radionuclides to wildlife in different semi-natural ecosystems in the UK ŽCopplestone. Previously. e. If no damage occurs to these species. 1986. The outputs of food-chain transfer models can then be input into dosimetric models so that internal radiation doses can be estimated... External dose rates will be elevated. syl¨ aticus in wooded areas.. small mammals and birds.. as it is not based on empirical study and is inconsistent with the precautionary approach used to protect the environment from non-radioactive discharges ŽPentreath.. 1983. at the highest dose rates. as they derive 100% of their diet from foodstuffs in their home range and they are constantly exposed to radionuclides via the inhalation pathway.. 1999. can be predicted.. 1978.54 M. 2. Home range sizes are small Žapprox. These estimates. 1998. Whicker et al.. 1996.. Consequently.. 1967. the impetus is growing for research into the fate of pollutants in food chains that do not have man as the ultimate receptor. as small mammals burrow and forage in the soilrlitter layer. NCRP.60 E y 16)3. Introduction With increasing interest in ecological risk assessment ŽERA. 2700 m2 for A. reviewed the effects of high levels of radiation exposure on a diversity of wildlife species Žincluding invertebrates. so for small mammals whose range is within the affected zone. it is then assumed that less sensitive species will not be affected and the integrity of the ecosystem will be maintained ŽMauriello. Due to their habitat and behavioural characteristics. the standard method of estimating exposure today is via the use of dosimetry models ŽKocher. mortality.16 E q 07 Ž1. it has been assumed that if humans are adequately protected from the effects of ionising radiation. 1988. Grooming causes ingestion of contaminated soil particles adhered to fur. external exposure is permanent. given dietary concentrations of radionuclides. then the natural environment is protected also ŽICRP. ⅷ Mammals are the taxonomic group most sensitive to the effects of ionising radiation ŽBlaylock et al. and found a range of effects including reduced growth rates.. 1986. Arthur et al.g. Kennedy et al. IAEA 1992... However.: Internal dose rate s E ) ⌽ ) Q )1. At- where E is the gamma energy of the radionuclide.. This is due to several reasons: ⅷ ⅷ ⅷ ⅷ tuquayefio et al. The objective of the present study is to extend these findings by constructing a food-chain transfer model of 137 Cs to small mammals in the vicinity of BNFL Sellafield. can then be compared to guideline values at which physiological damage to the individual is caused Ž) 1 mGy dayy1 for terrestrial organisms. ŽMiera and Hakonson. 1993.E.. combined with estimates of external dose. so that activity concentrations in Apodemus syl¨ aticus Žthe woodmouse. Significant uptake of the radionuclide 137 Cs by invertebrates and small mammals was found in a coniferous woodland ecosystem adjacent to BNFL Sellafield in Cumbria. 1977. Linsley. 1991.

5 g. the average dry weight Ždw. Muller and Prohl.2. dynamic compartmental models can be constructed that predict the levels of pollutant in the organism through time. In essence. was used in the following calculation: Cm s Q s 181.. 1993. OSGR NY040046. Full site descriptions are given by Toal Ž1999. or by the use of environmental transport models ŽJackson et al.5 / t t Ž4. Total 137 Cs assimilated into tissues of A... Quantifying radionuclide distribution in the environment can be achieved by field sampling and radioanalytical regimes. r The Science of the Total En¨ ironment 267 (2001) 53 ᎐ 65 55 137 the organism and Q is the activity concentration of radionuclides in the body of the organism. 1995. Modelling rationale Today. 137 To convert individual A. in units of Bq kgy1 dw. 1987. Such models have been used to predict the concentration of radionuclides.E.. and a mixed deciduous woodland ŽLongrigg Wood. 1993. k Ž2. 1998. A total s ns 1 Ý Ž In CnUn . Two constants are also included in the equation to convert from keV to joules and from seconds to years. Brown and Simmons. it is a deterministic model within which a number of parameters have been calibrated. Where: Q: A total : k: Cs body burden of an individual A. Ž5.M. . in the tissues of the receptor species of interest. Avila et al. Methods 3. Models were constructed for two sites within the vicinity of BNFL Sellafield. 137 Cs elimination rate constant Ždayy1 . stated that the main limitation in developing dose ᎐ rate estimates is the lack of information on the distribution of radionuclides in the environment.. syl¨ aticus per day ŽBq dayy1 .. 137 Cs levels in dietary items throughout the year. and 137 Cs biological elimination rate... 3.1. The present paper describes such a dynamic model that predicts the changing levels of 137 Cs in A. syl¨ aticus throughout one year. Forseth et al. ⅷ ⅷ bioavailability Žproportion of ingested assimilated into tissues . a number of modelling techniques are used to predict pollutant concentrations in wildlife receptors. syl¨ aticus from Lady Wood Ž5.82 Q ž 1000 5. it is essential to adequately characterise the levels of radionuclides Žin Bq. Toal et al. Indeed. 1993. syl¨ aticus ŽBq. In the present study: 6 ingestion rate and dietary diversity. Ma and van der Voet. of an individual A.e. This study is an example of an environmental transport model that predicts seasonal wildlife activity concentrations so that Q values in the above equation can be calibrated for use in internal dosimetry models. 1999. The models were then validated by comparing predictions with observed activity concentrations in small mammals from these sites. a coniferous woodland ŽLady Wood OSGR NY037045. Woodhead Ž1996. Cs These model parameters were calibrated from the literature and by measurement of 137 Cs levels in the dietary foodstuffs of the small mammals. As can be seen from the above equation. heavy metals and organic pollutants in a range of wildlife ŽGobas. If sufficient information is available on the kinetics of the pollutant under study. syl¨ aticus 137 Cs body burden to 137 Cs activity concentration Ž Cm .. Model equations dQ s A total y kQ dt A total Ž 1 y ey k t . 3.: ⅷ ⅷ Qs Ž3. i.

are given in Toal Ž1999. 3. i. dietary item n Žkg individualy1 dayy 1 . Seasonal 137 Cs concentration of dietary item n ŽBq kgy1 dw. syl¨ aticus per day. 1993.56 M. of each dietary item ingested by an individual A. of the dietary items .07 to obtain the appropriate values for the Lady Wood and Longrigg models. The seed activity concentrations were calibrated by using a concentration factor approach.E. seeds. The input values of each dietary item for each season are illustrated in Table 1. Peromyscus maniculatus.3. sampling and radioanalytical regime. Gut transfer factor of 137 Cs in dietary item n Žunitless .. syl¨ aticus and P. Toal et al. The derivation of the seed concentration factor is given in Toal Ž1999. 3. Mixed grass species. Montgomery Ž1985. syl¨ aticus itself ŽUSEPA. Inputs into the model (137 Cs acti¨ ity concentrations in dietary items ᎏ Cn ¨ alues) The input values into the model are the mean 137 Cs activities ŽBq kgy1 dw. Symbol Season Spring Summer 95 273c 97 33 53c 473 7 146c 15 10 20c 142 Autumn 96 355 140 33 53 473 10 310 32 10 20 142 Winter 96 263 140c 33 53c 473 10 310c 32c 10 20c 142 Dietary type Lady Wood Invertebrates a Fungi Vegetationb Seeds Fruits Soils Invertebrates a Fungi Vegetationb Seeds Fruits Soils C1 C2 C3 C4 C5 C6 C1 C2 C3 C4 C5 C6 76 273 54 33 53c 473 8 146 16 10 20c 142 Longrigg Wood Mixed invertebrate species. Ingestion rate (In ) This parameter is defined as the mass Ždw..3. fungi..3. Deri¨ ation of model parameters 3. invertebrates. Due to sampling difficulties. berries and soil during each season.. diets and behaviours were so similar that they can be The above theoretical model was used in both Lady Wood and Longrigg simulations. syl¨ aticus dietary item seasonal Site 137 Cs activity concentrations ŽBq kgy 1 . Figures for the food ingestion rate of A. r The Science of the Total En¨ ironment 267 (2001) 53 ᎐ 65 Table 1 A. vegetation. c Due to low sample masses.1.e. in which the soil activity was multiplied by 0. site specific 137 Cs activity concentrations for seeds were not obtained. Further details of the diets. investigated the ecology of A. maniculatus and concluded that their physiologies. due to a paucity of information on A. activity concentrations were not measured for these dietary items in the specified season. Cn and In values were site specific ŽTables 1 ᎐ 3. b a Where: In : Cn : Un : n s 1: n s 2: n s 3: n s 4: n s 5: n s 6: Ingestion rate of dry weight Ždw. Invertebrates Fungi Vegetation Seeds Berries Soil for small mammals during each season.2. hence activity concentration from the previous season was used. syl¨ aticus were based on the ingestion rate of the deer mouse.

20 0.000154 0. Ž ¨ b.000154 0. Consequently.330 0.000911 0.000024 0..035 0.11 0.000220 0. The average mass of A.11 0.16 0.E.000018 0.000000 0.M. syl¨ aticus was taken as 0. USEPA 1993. 1966. conversion ratio Žr. syl¨ aticus.16 0.45 0.035 0.443 0.007 ᎐ 0. It was assumed that the volume of a given dietary item in the gut contents of A.15 ᎐ 0.000004 0.000549 0. Season Dietary item Ž n.000025 0.. 1979.000653 0. 0.001 0.4 g A. for invertebrates.45 0.024 0.16 0. and the seasonal changes in diet for A.20 0. syl¨ aticus in coniferous woodlands ŽObrtel and Holisova. and the calculations are illustrated in Tables 2 and 3.007 ᎐ Mass of dietary type ingestedrday Žkg fw. Longrigg Wood: Watts.19 g Žfw.000027 0.000004 0. Mass of dietary type ingestedrday Ž In .. Toal et al.002094 0..037 0.000233 0. 0. 1993.000390 0. 0.001874 0.476 0.050 0. seeds and fruits are illustrated in Tables 2 and 3. syl¨ aticus is an omnivore. 1994.. The total mass of food consumed per day by the model organisms was therefore 0. quantified mass ingestion of soil as a percentage of diet Ždw.000026 0. for a variety of wildlife species and stated a value of 2% for omnivorous small mammals.460 0.000911 0.000843 0.000025 0.001949 0.11 0.000026 0. This figure has been used to calibrate I6 .002024 0.426 0.15 ᎐ 0.460 0.002746 0.rfresh wt. the food ingestion rate of A.000017 0.001452 0. Ž1994.000390 0.053 0.11 0.2 g diet wfresh weight Žfw.45 0.20 0.x ingested per g Žfw.15 ᎐ Summer Autumn Winter considered ‘ecological equivalents’.001949 0..16 0.007 ᎐ 0. Beyer et al.45 0. maniculatus have been used to calibrate the ingestion rate for A.000106 0.000163 0.443 0.000004 0. .000025 0. Beyer et al. Several authors have stated that accidental ingestion of contaminated soil may also contribute to radionuclide uptake ŽBelli et al.000031 ᎐ Dry wt. syl¨ aticus in the study is 22. syl¨ aticus were calibrated from the literature ŽLady Wood: Obrtel and Holisova.20 0. r The Science of the Total En¨ ironment 267 (2001) 53 ᎐ 65 Table 2 Dietary diversity and ingestion parameter calculations for A.000027 57 Spring Invertebrates Fungi Vegetation Seeds Berries Soil Invertebrates Fungi Vegetation Seeds Berries Soil Invertebrates Fungi Vegetation Seeds Berries Soil Invertebrates Fungi Vegetation Seeds Berries Soil 0. fungi.000026 0.000 ᎐ 0.000001 0. syl¨ aticus was proportional to the mass ingested during that season.000000 ᎐ 0.000000 ᎐ 0.053 0.2 = 22 g s 4.000031 ᎐ 0.624 0. hence the figures for daily ingestion rates of P. syl¨ aticus per day Žaverage value for non-breeding adult individuals.000004 0. of A.000419 0. Fraction of total diet ingestedrday Ž¨ .15 ᎐ 0. so the model organism was assumed to have a mass of 22 g.002024 0. 1979.000233 0. vegetation. Ž ¨ br . Ingestion rate parameters Ž In values. Žkg dw.

45 0. r6 s 0.000 0.000629 ᎐ 0.000028 0. Fraction of total diet ingestedrday Ž¨ .593 0.000079 0.000000 0. ModelMakerT M simulation Numerical analysis was carried out using ModelMaker TM 3.000 ᎐ 0.3.000127 0.000029 0. 0.000 0.123 ᎐ 0.001174 0.16 0.083 0.263 0.000000 ᎐ 0.000000 0.16 0. Season Dietary item Ž n.000000 0.20 0. Ž ¨ b. 0.000295 0.20 0.000 ᎐ Mass of dietary type ingestedrday Žkg fw.11 0.310 0.11 0.15 ᎐ Summer Autumn Winter 3.3. as 6 days.16 0.16 0.58 M.5.000614 0.5. 3.45 0.001847 0.004105 0.040 0. Žkg dw.000000 0.12 dayy1 Ž6. Therefore: k s yln Ž 0.000000 0. Toal et al.000000 0.181 0.4. 3.000000 0. r The Science of the Total En¨ ironment 267 (2001) 53 ᎐ 65 Table 3 Dietary diversity and ingestion parameter calculations for A.E. Ž1976.4. Mass of dietary type ingestedrday Ž In .000000 0.. Biological clearance coefficient (k) The biological clearance coefficient for the tissue compartment was derived from biological half-lives published in the literature.000 0.000000 0. syl¨ aticus in deciduous woodlands ŽWatts. The biological half-life of 137 Cs for 22-g laboratory mice Žtissue compartment.15 ᎐ 0.797 0.000040 0.003507 0.rfresh wt.11 0. Loss due to radioactive decay from the small mammal tissues is insignificant compared to biological elimination due to the relatively long physical half-life of 137 Cs Ž30 years.000176 0.000092 0. The gut transfer factors of radiocaesium from each item in the diet were calibrated from the literature.001879 0. and the values are given in Table 4.3.001157 0.000176 0.15 ᎐ 0.20 0.45 0.427 0. therefore.040 0.000000 0. physical decay of the nuclides was not included in the present simulation. is given in Kitchings et al.000038 Spring Invertebrates Fungi Vegetation Seeds Berries Soil Invertebrates Fungi Vegetation Seeds Berries Soil Invertebrates Fungi Vegetation Seeds Berries Soil Invertebrates Fungi Vegetation Seeds Berries Soil 0.000365 0.000000 ᎐ Dry wt.000000 0.000376 0.001364 0.000 0.000022 0. so the proportion of radiocaesium that crosses the gut wall and becomes bound up in the internal tissues of the organism from each dietary component must be defined.000159 0.11 0.067 0. Gut transfer factors (Un ) The bioavailability of radiocaesium differs between foodstuffs. rbiological half life Ž tissue . 1966.3 and the integration technique used was a fourth order Runge ᎐ Kutta integration .001578 0.002609 0.0.143 ᎐ 0.000000 0.000 0. conversion ratio Žr.000541 ᎐ 0. 0.000034 0.000796 0.15 ᎐ 0.20 0.933 0.000019 0.000032 0. s yln Ž 0. Ž ¨ br .45 0.

0 ᎐ 59. Ž1996. the output of the model was multiplied by 181.15 Reichle et al .f 3. c Various grass species. Hence. The output of the model is the prediction of mean seasonal 137 Cs activity ŽBq kgy1 dw. The simu- Fig. were linked to the model using . Various fungal species. Eq. 1990.82 Ž1000rdw of an individual.. 137 59 lation began on 1st January Žday 1.M.7 and 1 ha. and dietary preference changes ŽTables 2 and 3. f Organic soil ingestion by Scottish Blackface ewes. a single seasonal cohort of small mammals was trapped in each year of the study 1996 Žautumn. from a range of environmental matrices Dietary type Ž n. 1998 Žspring. As the study sites were small Ž4. for an adult woodmouse in each woodland site.. ModelMaker TM dynamic compartmental model of food chain 137 Cs transfer to A.. algorithm.a Salbu et al. Soil Ž6.c Mayes et al. d Assumed as for vegetation. Ž1992.. to activity concentration ŽBq kgy1 dw.d Salbu et al. Ž4..txt files in the ModelMaker TM look-up table facility ŽFig. Validation data: small mammal sampling Small mammals were trapped from the leading edge of Lady Wood and throughout Longrigg Wood. Small mammals were sampled using Longworth live traps ŽGurnell and Flowerdew. syl¨ aticus. and the days in each season are illustrated below: Season Duration of season Žday numbers throughout the year. Ž1996. as harvesting animals then would damage the population structure in the experimental sites by culling overwintering breeding stock. 1997 Žsummer. This was deemed acceptable. To convert from body burdens ŽBq individualy1 .82 1 0... 1. Small mammals were not sampled during winter. syl¨ aticus would not remain viable if all the trapping sessions were carried out within 1 year. 335 ᎐ 365 60 ᎐ 151 152 ᎐ 243 244 ᎐ 334 Cs gut transfer factor ŽUn . Toal et al.e Mayes et al. Ž1970. Ž1992. r The Science of the Total En¨ ironment 267 (2001) 53 ᎐ 65 Table 4 Mammalian 137 Cs gut transfer factors ŽUn . Fruit Ž5. Reference Winter Spring Summer Autumn Invertebrates Ž1. as there were no significant inputs of 137 Cs into the sites during the study period that would negate inter-comparison between the cohorts sampled..5. respectively. The inputs ŽTable 1. . a b 0.b Mayes et al. the populations of A. Ž1996.. Vegetation Ž3. 1.E. e Assumed as for fungi. As only Median value for mammalian gut transfer factors.85 1 0. Fungi Ž2. Seeds Ž4. The model was run for Lady Wood and Longrigg Wood with a 1-day time step.82 0.

60 M. reflecting dietary change. The results for A. However. Differences in mean activity concentration were predicted between seasons in both . but no additional animals were caught. All animals were frozen no more than 2 h after capture. 2.. The average individual fresh weight Žfw. 1992. and the homogenised material was subjected to gamma spectrometry analysis using an EG & G Ortec high purity germanium detector linked to a multi-channel analyser. depending on activity concentration. then placed in a cool box packed with ice in order to minimise tissue deterioration before freezing. Results The target sample size was 12 animals from each site in every season Žexcept winter. and the stomach and intestines were excised. and the resultant spectra were analysed using OmnigamTM software. a one-way analysis of variance ŽANOVA. so ANOVAs were carried out on logtransformed data to determine whether seasonal changes in 137 Cs accumulation occurred throughout the year. was carried out on the A. The availability of A. Each trap was lined with straw bedding and baited with rolled oats in order to maintain the animals between each trap check. sexed.. A further trapping session was carried out later in the season.. The animals were then dried in an oven at 105ЊC for 2 days. weighed.0. between autumn and summer animals.001. washed to remove any adhered surface contamination. hence the dry weight-to-fresh weight conversion factor was Žapprox.05. The activity of these dietary foodstuffs also differs on a temporal basis ŽTable 1.19 g. at the base of trees and under fallen logs throughout Longrigg and Lady Wood. Variances were greater than the arithmetic means for each cohort.5 g. so log transformation was necessary ŽFowler and Cohen. and no significant differences were found between any of the seasonal cohorts of animals from Longrigg Wood Ž P ) 0. and the dry weight recorded prior to homogenising in a blender. Each mammal was designated as one replicate. or until constant dry weight was obtained.. between autumn and spring animals Žwith autumn having the highest activity concentrations in all comparisons. syl¨ aticus activity concentrations from each site.. Toal et al. Suitable animals were culled in the field.05.05. Fig. in the spring cohort for Longrigg Wood. only 5 animals were trapped. specimens were thawed. A Tukey LSD test found a significant difference Ž P . syl¨ aticus seasonal activity concentration changes ŽLady Wood. no significant differences were found between spring and summer animals Ž P ) 0..04. 4. Fig. In order to determine if there were any sex differences in 137 Cs accumulation..E. of a woodmouse in Lady Wood was 22. This procedure was carried out to ensure that no gut contents or faecal matter contaminated the internal tissues of the animal. 137 Cs in Longrigg Wood and 4. Samples were counted for between 80 000 and 350 000 s. show a significant difference between cohorts. No significant 137 Cs accumulation differences were found between the sexes for either site Ž P ) 0. and a highly significant difference Ž P . Dynamic behaviour of Lady Wood A. syl¨ aticus dietary items changes throughout the year. However. Samples for each sex were pooled across the seasons. r The Science of the Total En¨ ironment 267 (2001) 53 ᎐ 65 adults were destructively sampled. using live traps allowed for the release of juveniles.0. 2 illustrates the results of the ModelMaker simulation for a period of 365 days beginning on 1st January. the dry weight was 5.05. In the laboratory. The traps themselves were then placed beneath understorey vegetation. syl¨ aticus.

The model accurately predicts activity concentrations for A. there are differences between the sites in terms of the dietary items that are most important in terms of mediating 137 Cs flux to the small mammals.. To determine the importance of each food item by way of contribution to the final activity concen- Fig. syl¨ aticus during spring and summer at Lady Wood. At both sites. Furthermore. 5 and 6. 1992. it is important to recognise that proving that a number of radionuclides in the tissues of the animals were derived from a particular dietary item is impossible experimentally. respectively. 5.. however.. In Lady Wood. the model was deemed to be acceptable. syl¨ aticus 137 Cs activity concentrations ŽLady Wood. and hence 137 Cs body burdens. n . to final activity s 6 concentration of small mammal Ý Ž In CnUn . Model predicted vs... However. Toal et al. Figs. Model predicted vs. syl¨ aticus activity concentrations with confidence intervals derived from log-transformed data ŽFowler and Cohen. observed A. 1992. The upper limit of the range is therefore an order of magnitude higher than the mean value predicted by the model simulation. It must be recognised. As can be seen from the figures. whereas at Longrigg the body burdens are dominated by seed-derived contamination. fungi contribute a significant proportion of the 137 Cs to body burdens recorded during the autumn Ž10 ᎐ 30%.E. instead.M. syl¨ aticus 137 Cs activity concentrations ŽLongrigg Wood. 3. Observed arithmetic means given with 95% confidence intervals derived from log transformed data ŽFowler and Cohen. that a step-wise change in dietary activities may not occur in nature and. ns 1 Ž7. with autumn being the season with the highest mean 137 Cs activity concentrations. are more gradual. with 137 Cs body burdens equilibrating approximately 1 month after shifts in dietary diversity. the following calculation was carried out: Percentage contribution of 100) In CnUn dietary type. The dynamics of the system are also rapid. It must be stressed that these are modelled calculations only and are not validated against measured data. 3 and 4 illustrate the predicted and observed 137 Cs body-burdens for Longrigg Wood and Lady Wood. r The Science of the Total En¨ ironment 267 (2001) 53 ᎐ 65 61 sites. 1992. changes in dietary abundances. the range of measured activity concentrations during this season is very high Ž5 ᎐ 1000 Bq kgy1 dw.. If the mean predicted activity concentration from the model fell between the confidence intervals of the observed data. but underpredicts autumn values.. with a slight underestimation of observed activity concentrations in summer. Observed arithmetic means given with 95% confidence intervals derived from log transformed data ŽFowler and Cohen. Discussion Previous work investigating seasonal accumulation of radionuclides in small mammals ŽMihok et . observed A. tration of the experimental animals. The data are shown as arithmetic means of the A. Fig. the invertebrates contribute approximately 50% of the 137 Cs body burden. The results are shown in Figs. There was good agreement between predicted and observed data for Longrigg Wood. 4.

. voles have a proportionally greater intake of fungi.. which accumulate high levels of 137 Cs during the autumn period ŽHaselwandter and Berreck. from a minimum of 1% in Lagurus curtatus Žsage vole. an underestimation of the magnitude of fungal ingestion may result in underprediction of autumnal body burdens.. Ovaska and Herman. syl¨ aticus and other mammals are known to consume fungi. Copplestone... syl¨ aticus in the autumn was an order of magnitude lower than the upper limit measured in the observed population. 1991.. 1996. The greater stepwise increase observed by Mihok was expected. 1978.. however. Amundsen et al. syl¨ aticus 137 Cs activity concentrations ᎏ modelled results ŽLongrigg Wood.. Ž1989. 1986. Toal et al. 1993. as. compared to mice. was the red-backed vole. ŽUre and Maser. 1982. Maser et al. Generally the model performed well. 1989. The autumnal increase reported by Rudge et al.. 1989. The percentage of diet composed of fungi varies greatly. for Lady Wood at least. al. This study confirms this hypothesis and. Rudge et al.. but this is mainly attributed to the differences in taxa in the two studies. Ž1989.. Furthermore. 1994. 1994.. Ž1993. and several studies have shown that the consumption of fungal fruiting bodies is largely responsible for elevated 137 Cs body-burdens during the autumn ŽMihok et al. The two main sources of variation in the model that are most likely to affect body burdens are the ingestion rate and dietary input activity concentration values. Lindner et al. r The Science of the Total En¨ ironment 267 (2001) 53 ᎐ 65 Fig. Therefore. 6. 5. the autumnal peak is statistically significantly elevated above activity concentrations recorded in spring and summer. Karlen et al. undertook a study in a range of Canadian habitats where Chernobyl deposition was minimal and an 8 = elevation in vole 137 Cs activity concentration was noted from summer to autumn. Ure and Maser.1. A. This figure is higher than the stepwise increase in the present study. Percentage contribution of dietary items to A. syl¨ aticus 137 Cs activity concentrations ᎏ modelled results ŽLady Wood. syl¨ aticus in this study was Fig. The percentage of fungi in the diet of A. . Mihok et al. 1996.62 M. indicated that elevated body burdens occur during the autumn. 5. Ingestion rate Mycophagy is a well documented phenomenon in small mammal ecology ŽFogel and Trappe.. Percentage contribution of dietary items to A. This difference deserves further consideration. 1982. the mean predicted 137 Cs activity concentration for Lady Wood A. The fungal ingestion pathway was therefore recalibrated to investigate whether the model could correctly predict the large range in autumn activity concentrations for Lady Wood. Clethrionomys gapperi.. as the Chernobyl input greatly influenced seasonal differences.. The species of small mammal used by Mihok et al.E. to 100% during November in Clethrionomys californicus californicus ŽCalifornia red-backed vole. but real activity concentrations were underpredicted for the Lady Wood autumn cohort. cannot be compared directly to the present data set. 1978.

1999. 1968. mycophagy may be underestimated for specific sites. 1991. If small mammals graze preferentially on fungi that contain 137 Cs activities that are higher than the mean. which would double ‘ In’ values in the present model. but Maser et al..E. Ža. Žc. 7. 1992. Once again. fungal activity s 355 Bq kgy1 . Fungal ingestion s 10% of diet. in coniferous forests and found an average value of 10%. the intake of 137 Cs via fungi will be seriously underestimated. it has been assumed that A. lactating female P. Fungal ingestion s 10% of diet. or between physiological states.2. the activity of fungi in Lady Wood varies greatly with a range of 2 ᎐ 4655 Bq kgy1 dw ŽToal. Fungal ingestion s 30% of diet. Observed s arithmetic mean with 95% CI derived from log transformed data ŽFowler and Cohen. Žd. syl¨ aticus consumes 4. quantified fungal consumption in several species of mice ŽCricetidae.5. fungal activity s 3213 Bq kgy1 . Fig. Ž1978. not enough quantitative information is available about the changes in consumption rates of small mammals in the wild in order to confidently incorporate this variability into the model. This figure may not remain constant throughout the year. 1993. Žb.4 g 137 Fig. 7 illustrates these updated results alongside the observed data for Lady Wood animals caught in the autumn. as in the present study. Cs was adopted in this model for the activity of fungi during autumn. Thus far. Fungal ingestion s 3. Specific acti¨ ity concentrations A geometric mean value of 355 Bq kgy1 Ždw. Furthermore. Effect of varying dietary intake and 137 Cs activity concentration of fungi on the 137 Cs activity concentration of A. fungal activity s 3213 Bq kgy1 .M.e. however. if the preferred foods Žseeds. hence the effect of this variability could not be analysed. Žf. The model was therefore re-calibrated with realistic increases in fungal ingestion rates. Lady Wood is a dense spruce forest with little understorey and..5% of diet. The effect of consuming Mycena galariculata Ža high accumulator species ᎏ mean autumn Bq kgy1 dw value s 3213. reaching 34% in a dense lodgepole pine forest with little understorey. A number of other factors affect radionuclide accumulation in small mammals. Fungal ingestion s 30% of diet. alongside the ingestion parameter. The biological half life of 137 Cs will also affect radionuclide retention and hence activity concentrations in the small mammals. fungal activity s 3213 Bq kgy1 . Fungal ingestion s 3. Consequently. Biological halflives are themselves inherently variable Žvan Straalen and Ernst. syl¨ aticus. are scarce. although these figures only give a guide as to the probable role of fungi in producing elevated activity concentrations in the autumn-caught animals. due to genetic differences in animal populations. significantly increasing small mammal activity concentrations. r The Science of the Total En¨ ironment 267 (2001) 53 ᎐ 65 63 approximately 4%. 3. For example. etc. as mice are opportunistic feeders. Že. syl¨ aticus... Žfw. with one species Ž Neotoma cinerea.5% of diet. However. . of ‘diet’ per individual per day. fungal activity s 355 Bq kgy1 . 10 and 30% of diet. animals are known to increase consumption in autumn in order to lay down fats for the oncoming winter ŽSawicka-Kapusta. Toal et al. the fungi specific activity was also varied in a re-calibration of the model. It is clear that varying the consumption of fungi can alone bring about significant changes in the activity concentration of A. i. If models are calibrated using generic literature values. was investigated. however. inadequate quantitative information on this parameter was found in the literature. fungal activity s 355 Bq kgy1 . maniculatus have an ingestion rate of approximately 9 g fresh weight of diet per day ŽUSEPA. they may have to increase their proportional consumption of secondary choice foods Žfungi. 5.

332. Ugedal O.64 M. Stockholm. Gobas FAPC. 1996. J Environ Radiat 1991. Ecol Model 1993. Accumulation and long term behaviour of radiocaesium in Norwegian fungi. Karlen G. sex and seasonal differences. ICRP. Publication No. 1992. Jonsson B. Home range sizes in the wood mouse Apodemus syl¨ aticus: habitat. Blasi M. Fogel R. A model for predicting the bioaccumulation of hydrophobic organic chemicals in aquatic food-webs: application to Lake Ontario. Fowler J. 1977. NRPB-R273. 1990. Environmental monitoring in the vicinity of Sellafield following deposition of radioactivity from the Chernobyl accident. 1994:259 ᎐ 277. editor. Acknowledgements The authors gratefully acknowledge the financial support of British Nuclear Fuels Limited. The disparities between modelled and observed 137 Cs activity concentrations can be attributed to a lack of information about a number of ecological parameters. 26. Conclusions A model of 137 Cs transfer to A. Kennedy VH. 1st John Wiley and Sons. Strand S. such as the ingestion rate and dietary diversity of small mammals in the wild. The Food Chain Transfer of Radionuclides through Semi-Natural Habitats. Effects of Ionizing Radiation on Plants and Animals at Levels Implied by Current Radiation Protection Standards. Oxon: NRPB. Capra E et al. J Zool 1986. Blaylock BG. Northwest Sci 1978. IAEA. Jones SR. Larsson C. Gorman ML. Fungus consumption Žmycophagy. Berreck M. Brown J.14:91 ᎐ 103. J Appl Ecol 1986. Technical Reports Series No. Forseth T. J Radiol Prot 1987. Jackson D. Recommendations of the International Commission on Radiological Protection. Trappe JM.79:1 ᎐ 17. Radioactivity and Wildlife. The results of such food chain models can be used in dosimetric studies. J Environ Rad 1999.35:847 ᎐ 856. Accumulation of radionuclides in fungi.53. Haselwandter K. Toal et al. 1992. Johanson KJ. and subsequently ecological risk from environmental radioactivity. In: Amiro B. Groves CR. Flowerdew JR. Ingested soil as a source of 137 Cs to ruminants. Livens FR. editors. DiGregorio D. Model of the seasonal variations of fungi ingestion and 137 Cs activity concentrations in roe deer. Live trapping small mammals ᎏ a practical guide. Gurnell J. J Wildl Manage 1994.136:243 ᎐ 249. If well-calibrated and validated models can be constructed for a range of critical wildlife groups and pollutants of ecotoxicological concern.:375 ᎐ 382. Gulden G. The dynamic compartmental approach has been used here to quantify 137 Cs transfer to small mammals. Keller BL.1Ž3.58Ž2.52Ž1. Metal Ions in Fungi. PhD Thesis. syl¨ aticus in woodland ecosystems has been constructed. Sci Total Environ 1996.7Ž2. the need for extensive destructive sampling could be reduced. Nature Conservancy Council. In: Cushing CE. Report no 24. Van Voris P. Chilton.23:13 ᎐ 26. A review of the ecological parameters of radionuclide turnover in vertebrate food chains. Markham OD. 256 pp.:1 ᎐ 31. Radiation dose to small mammals inhabiting a solid radioactive waste disposal area. 39 pp. Biological effects of ionising radiation. Halford DK. where dose. Arthur WJ. Proceedings of 6.:75 ᎐ 87. Shugart LR. An Occasional Publication Of The Mammal Society. 91 pp. Attuquayefio DK. r The Science of the Total En¨ ironment 267 (2001) 53 ᎐ 65 Avila R. Didcot. This paper has shown that dynamic compartmental modelling is a valid tool when attempting to make ecological risk assessments. Annals of the ICRP. Naesje TF. Estimates of soil ingestion by wildlife. . editors. Bergstrom R. Avadhanula R. Marcel Dekker Inc.210:45 ᎐ 53.E.46:99 ᎐ 112. Seasonal variation in the activity concentration of 137 Cs in Swedish roe-deer and in their daily intake. Horrill AD. 1990. Belli M. 1996. J Appl Ecol 1998. 1995. References Amundsen I. but there are no theoretical reasons why this approach could not be adopted for other radionuclides and other wildlife species if the fate of xenobiotic chemicals needs to be quantified in natural ecosystems. Radiocaesium elimination in fish: variation among and within species. Gerould S. International Atomic Energy Agency. Simmons JR. Kitchings T. Bergstrom R. Sci Total Environ 1993. Connor EE. 369 pp.184:163 ᎐ 171. where seasonal body burdens could be predicted from a knowledge of dietary 137 Cs activities. In: Winkelmann G. Swedish Radiation Protection InstituterAtomic Energy Control Board International Symposium on Protection of the Natural Environment: International Symposium on Ionising Radiation. Fulker MJ. Beyer WN. Theodorakis CW. Further fundamental ecological research to quantify these ecological parameters would surely improve model estimates. Winge DR. Johanson KJ. Practical Statistics for Field Biologists. Cohen L. Johansson G. Luning M. can be calculated. Copplestone D. University of Liverpool. Coverdale NGM. by small animals. 20 ᎐ 24 May. 3. 1996:39 ᎐ 50. FARMLAND ᎏ A Dynamic Model for the Transfer of Radionuclides Through Terrestrial Food Chains. Wolton E.

USEPA. Maslov VI. Schwartz B. University of Liverpool. Characteristics of the radioecological groups of mammals and birds of biogeocoenoses with high natural radiation. Johansson G. 1996:51 ᎐ 64. Watts CHS. Swedish Radiation Protection InstituterAtomic Energy Control Board International Symposium on Protection of the Natural Environment: International Symposium on Ionising Radiation. Office of Research and Development. Prohl G. 65 Obrtel R. NCRP. Environ Pollut 1999. Washington DC: US Environmental Protection Agency. 1999.13Ž19.28Ž4. Garmo TH. Folia Zool 1979. Sawicka-Kapusta K. editors.60:3307 ᎐ 3315. and bank voles Ž Clethrionomys glareolus. Maser C. Woodhead DS. Maser C. editor. J Hazard Mater 1993. Sci Total Environ 1993. Jones SR. J Mammal 1986. J Radiol Prot 1998. Ure DC.:43 ᎐ 55. 45Ž3. Avadhanula R. Holm E. Stakelum G. 109. Radiological protection criteria for the natural environment. Wildlife Exposure Factors Handbook. Deer Mouse Ždeer and white-footed mice. Mayes RW. Luning M. National Council on Radiation Protection and Measurements. Herman TB. J Anim Ecol 1966. 67Ž1. In: Cook LM. Mihok S. The foods eaten by wood mice Ž Apodemus syl¨ aticus . Effects of ionizing radiation on aquatic organisms. 1976:304 ᎐ 313. Verkhovskaya IN. Environmental monitoring for radionuclides in marine ecosystems: are species other than man protected adequately? J Environ Radiat 1988. Ostby G. van der Voet H. Maslova KI. Johansson G.:799 ᎐ 809. Northwest Sci 1978. Fungal-small mammal interrelationships with emphasis on Oregon coniferous forests.117:487 ᎐ 491. J Environ Radiat 1993. Turnover and concentrations of radionuclides in food chains.: 199 ᎐ 212.57Ž6. In: Amiro B. EPAr600rR-93r187a.751Ž4. Miera FR.: 329 ᎐ 339. Hungate FP. Montgomery WI. Kocher DC. Report no. Radioactive contamination: state of the science and its application to predictive models. Stockholm.133Ž2.100Ž1 ᎐ 3. Small mammals. Thompson PM.11Ž1. Health Phys 1978. Vandecasteele CM.:1701 ᎐ 1714.37:25 ᎐ 42.7:575 ᎐ 583.M. Salbu B. 20 ᎐ 24 May.:665 ᎐ 686. Larsson C.34:603 ᎐ 609. Muller H. Drissner J. 1996. Radiat Environ Biophys 1996. Rudge SA. Stockholm. Health Phys 1989.. A risk-assessment model for toxic exposure of small mammal carnivores to cadmium in contaminated natural environments.E. Holisova V.. Toal et al. Radiation doses to rodents inhabiting a radioactive waste receiving area. Avadhanula R. 1967:561 ᎐ 571. Wiewel AM.:299 ᎐ 310. Shaw G. Analyst 1992. 2. 1991. Acta Theriol 1968.:175 ᎐ 179. 20 ᎐ 24 May 1996. Whicker FW. Sci Total Environ 1994. Johnson MS. Hakonson TE. Metal biomagnification may endanger species in critical pathways. Nelson DJ. Stress to indicator species as assessment endpoints..:959 ᎐ 966. Lindner G. . Pergammon Press. In: Aberg B.62Ž2. Larsson C. Nussbaum RA. Reichle DE.:133 ᎐ 149. Vol. Case Studies in Population Biology. Voight G. 2. Health Phys 1983. ECOSYS-87: a dynamic model for assessing radiological consequences of nuclear accidents.35:273 ᎐ 282. Seasonal and regional variations in the transfer of caesium radionuclides from soil to roe deer and plants in a prealpine forest. The Transport of Radiocaesium in Semi-Natural Woodland Ecosystems: Measurement and Modelling. The food eaten by Apodemus syl¨ aticus in a spruce monoculture. Northwest Sci 1982. Saf. Luning M. Herrmann T et al. Ovaska K. van Straalen NM. Howard BJ. editors. Use of the true absorption coefficient as a measure of bioavailability of radiocaesium in ruminants. Leah RT. Hove K. Protection of the natural environment and internationally accepted practice. Annual fat cycle of field mice. Availability of caesium isotopes in vegetation estimated from incubation and extraction experiments. Nucl. in Wytham Woods. Radiological Concentration Processes.35:101 ᎐ 109. Beresford NA. 1970.157:189 ᎐ 196.59Ž4. Interspecific competition and the comparative ecology of two congeneric species of mice. Radioecology and Energy Resources. Ma W. Toal ME. r The Science of the Total En¨ ironment 267 (2001) 53 ᎐ 65 the Fourth National Symposium on Radioecology. 1834. Dunaway PB. Environmental dosimetry: which target? What dose rate? In: Amiro B. Oikos 1991. Mycophagy of red-backed voles in Oregon and Washington. Health Phys 1993.: 255 ᎐ 256. Fungal consumption by six species of small mammals in Nova Scotia. Berkshire. editors. Trappe JM. PhD Thesis.19Ž3.:232 ᎐ 252.64Ž3. Pentreath RJ. 1985:126 ᎐ 187. Biological transport of radiocesium in a seminatural grassland ecosystems. 214 pp. Mauriello DA. Ernst WHO. Swedish Radiation Protection InstituterAtomic Energy Control Board International Symposium on Protection of the Natural Environment: International Symposium on Ionising Radiation. 1993:2 ᎐ 2309. Dose-rate conversion factors for external exposure to photons and electrons. Manchester University Press. Bioconcentration of fallout 137 Cs by fungi and red-backed voles Ž Clethrionomys gapperi. Linsley G.:208 ᎐ 211. Apodemus fla¨ icollis ŽMelchior. 1996:27 ᎐ 35.