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Radionuclides in fruit systems: A review of experimental studies
Science of the Total Environment 359 (2006) 188 – 193 www.elsevier.com/locate/scitotenv
Radionuclides in fruit systems: A review of experimental studies F. Carini a,*, N. Green b, S. Spalla a a
Universita` Cattolica del Sacro Cuore, Institute of Agricultural and Environmental Chemistry, Faculty of Agricultural Sciences, Via Emilia Parmense 84, I-29100 Piacenza, Italy b NRPB, Chilton, Didcot, Oxfordshire OX11 0RQ, United Kingdom Received 29 November 2004; accepted 25 May 2005 Available online 13 September 2005
Abstract Existing information on processes and parameters analysed in experimental studies on fruits was reviewed at the inception of the activities of the IAEA BIOMASS Fruits Working Group. Additional information on experimental studies, collected during the activities of the Group and not included in the Review, is presented and discussed in this paper. Studies on deposition of 14 CO2, CO35S and 3H2O in the gas phase to apple, raspberry, strawberry and blackcurrant have filled gaps in knowledge of uptake of gaseous pollutants in fruit plants, quantifying processes of deposition, translocation and carry-over between seasons. Measurements over a period of six years on vine plants contaminated via leaves and soil by dry deposition of 137Cs and 90Sr have improved knowledge of the processes of direct deposition to fruit, translocation and carry-over of radionuclides from year to year. Additional information is given on soil to fruit transfer of U, Th and Pb for apple and mandarin grown under intensive agricultural conditions. D 2005 Elsevier B.V. All rights reserved. Keywords: Radionuclides; Fruits; Experimental studies
1. Introduction Radionuclides introduced into the environment during routine nuclear operations, as a consequence of nuclear accidents, or from waste disposal facilities can migrate through foodchains, thus posing a potential risk for the population. Fruit is an important component of diet, particularly for some groups of the population who rely heavily on fruit consumption, * Corresponding author. Tel.: +39 0523599478; fax: +39 0523599448. E-mail address: [email protected] (F. Carini). 0048-9697/$ - see front matter D 2005 Elsevier B.V. All rights reserved. doi:10.1016/j.scitotenv.2005.05.034
either by choice or because of their geographical location. Consumption in Europe can be as much as 25% of the total diet (Brenot and Noordijk, 1991). Information on the behaviour of radionuclides in the fruit systems was recognized as a gap in knowledge in the assessment of the internal dose to human beings from contaminated food ingestion (Carini, 1999; Venter et al., 2001). On the basis of the work completed by a Task Force on radionuclide transfer to fruits under the International Union of Radioecologists (IUR) in 1996, a Fruits Working Group was established within the framework of the International Atomic Energy Agency (IAEA) Biosphere Modelling and Assessment (BIO-
F. Carini et al. / Science of the Total Environment 359 (2006) 188–193
MASS) Co-ordinated Research Programme, under Theme 3 in late 1997. The objective was to improve understanding of the processes affecting the transfer of radionuclides in fruit systems. The activities were completed in November 2000. They included a review (Atkinson and Webster, 2001; Carini, 2001; Carini and Bengtsson, 2001; Fulker, 2001; Green, 2001; Kinnersley and Scott, 2001; Mitchell, 2001; Ould-Dada et al., 2001; Stewart et al., 2001. These references are hereafter referred to collectively as bthe reviewQ), the derivation of a fruit conceptual model, the compilation of a database of model parameters for use in fruit models (Mitchell, 1997), the collection of information from experimental studies additional to that summarised in the review (this paper), two model intercomparison studies (Linkov et al., 2005—this issue) and a validation study (Ould-Dada et al., submitted for publication). A final document has been issued by the IAEA (2003). A summary is included in a special issue of the Journal of Environmental Radioactivity on the results of the BIOMASS Co-ordinated Research Programme (Carini et al., in press). The activities of the Fruits Working Group were initiated by discussions on the processes leading to the contamination of fruit after transfer of radionuclides into various fruit systems and on the parameters measured in experimental studies and used in modelling activities. The state of the art at that time has been published in the review. During the subsequent meetings, new information from recently completed or ongoing experimental studies or from those not included in the review was presented and discussed. The aims were to collect additional information, to improve knowledge of processes, and to provide data valuable either for the further development of models or for the testing and validation of existing ones. The present paper summarises information on those experimental studies that have formed the basis for discussion. The most important results, in terms of data or understanding of processes, have been compared with the existing review.
2. Deposition of gaseous radionuclides to fruit plants Information reported in the review on the uptake of gaseous pollutants by vegetation showed that, although
189
uptake by vegetable crops has been studied fairly extensively, there has been relatively little investigation into uptake by fruit crops (Stewart et al., 2001). Recent studies supplied new information on the process of deposition of 14CO2, CO35S and HTO (tritiated water) in apple, raspberry, strawberry and blackcurrant (Stewart, 2002). The deposition velocity calculated per unit plant mass (Vgw: the mass normalised deposition velocity: cm3 g 1 s 1) revealed significant differences between fruit plants for deposition of 14CO2 and CO35S, confirming what reported in the review. However the deposition velocities calculated per unit area of the plant (Vga: the standard deposition velocity: cm s 1) were of the same magnitude as those observed for other crops, ranging from 1.9 10 2 to 9.4 10 2 for 14CO2 and from 5.4 10 2 to 1.5 10 1 for CO35S. The authors suggested that a single deposition velocity for all crops should be used in assessment studies. This should be the highest value, unless a probabilistic approach was being pursued (Stewart, 2002).
3. Post deposition transport of radionuclides in fruit plants 3.1. Direct deposition to fruit The processes of interception, retention and absorption of radioactive fallout can directly involve the fruit. Many variables contribute to the process of direct contamination of fruit: the physiological stage of the plant at time of deposition, the radionuclide, the kind of deposit (wet or dry), the fruit surface properties, the fruit’s physical exposure to the fallout and to the subsequent weathering, and the time elapsed between deposition and harvest. Information reported in the review showed that few data in the literature distinguished between the contribution of the activity directly deposited on the fruit surface and that translocated from other plant components to the fruit (Carini and Bengtsson, 2001). New information on this topic has been supplied from two series of data concerning dry deposition of Cs and Sr on vines bearing some bunches purposely protected from direct deposit, which allowed to distinguish the process of leaf to fruit translocation from that of direct deposition.
F. Carini et al. / Science of the Total Environment 359 (2006) 188–193
The two datasets, from Madoz-Escande et al. (1998, 2002) and Arapis (1999), are compared with those on vines reported in the review (Carini et al., 1996). The three experimental works were carried out under different conditions — field or controlled, used different devices to simulate the radioactive source and considered different plant stages at deposition time. Results, expressed as percentage of the whole activity in fruit at harvest, show a wide variability from 13% to 97%, revealing the difficulty of reproducing natural conditions and the complexity in data interpretation, and underlining as an appraisal of the contribution from the different variables to contamination of fruit at harvest is still difficult.
4. Translocation from the above-ground parts to fruit
% of the activity in whole plant
Data on radionuclide translocation from the aboveground parts to fruit were discussed in the review (Carini and Bengtsson, 2001). The datasets concerned mainly Cs and Sr on apple, grapevine and strawberry, and, in a few cases, gooseberry, blueberry, orange, pear and redcurrant. Two recent experimental studies provided new information on the translocation of gaseous 14CO2, CO35S and HTO to apple, raspberry, strawberry and blackcurrant (Stewart, 2002) and of dry 137Cs and 90 Sr to vines (Madoz-Escande et al., 1998, 2002). Results are not comparable, being expressed with different units of measure and carried out under
70
14C(g)
60
35S(g)
50
3H(g)
40 30 20 10 0 ring
flowe
t n men matio velop f. de
f. for
ening
f. rip
stage at time of deposition Fig. 1. 14C, 35S and 3H activity in apple fruit at harvest after foliar deposition at four growing stages.
% of the intercepted activity
190
7
90Sr
6
137Cs
5 4 3 2 1 0 late flowering
beginning of ripening
stage at time of deposition Fig. 2. 137Cs and 90Sr activity in grapes at harvest after foliar deposition at two growing stages.
different experimental conditions. However some general conclusions can be drawn. Both studies derived the radionuclide concentration in fruits after deposition at different phenological stages. As an example, Fig. 1 shows the allocation of 14C, 35S and 3H to apple fruit and Fig. 2 that of 137Cs and 90 Sr to grapes, both studied after deposition at various growing stages. When the contamination process occurred at flowering, in absence of fruits, 35S, 3H (Fig. 1) and 137Cs (Fig. 2) were translocated to fruits, while very little 14C and 90Sr were remobilised from leaves to fruits late in the growing season, demonstrating that the partitioning of radionuclides in the plant is radionuclide-dependent. Results also confirm that the time of contamination relative to production of the fruit plays a role in the percentage found in the fruit at harvest. Even if the times of contamination considered under the two scenarios are not comparable, it is possible to infer that the highest values in fruit at harvest occurred following deposition between fruit development (Fig. 1) and beginning of ripening (Fig. 2). This lapse of time is regarded by horticulturists as the stage of the higher demand of fruits for photosynthetic products from leaves, and that could explain the higher transport of 14 C and of 137Cs, analogous to potassium, from leaves to fruits. The temporal changes in concentrations of 137Cs and 90Sr in the grape have also been studied picking fruits 2, 7, 20 and 30 days after contamination (Madoz-Escande et al., 1998). Fig. 3 shows as, after the initial deposition, the distribution of 137Cs increased with time due to the process of leaf to fruit
% of intercepted activity
F. Carini et al. / Science of the Total Environment 359 (2006) 188–193 8 7 6 5 4 3 2 1
Cs Sr
0 0
10
20
30
40
days from contamination to harvest Fig. 3. 137Cs and 90Sr activity in grapes at different harvest times after foliar deposition at beginning of ripening.
translocation, conversely, that of 90Sr decreased initially, due to the loss process, and then increased in the last ten days, although not significantly.
5. Residual activity Little information has been reported on the residual activity of radiocaesium and radiostrontium in fruit in the years following that of deposition from the Chernobyl accident (Carini, 2001). Generally speaking, when the scenario is a single deposition event, the residual activity in the plant is regarded as deriving from soil as the donor compartment, through the processes of soil to plant transfer and/or resuspension and splash. Although this may hold true for annual plants, it is not always so for perennial plants such as fruit trees. Information collected in the review (Carini, 2001; Mitchell, 2001) provided some evidence that radiocaesium, once introduced into the plant, could be retracted from leaves at fall into perennial organs of deciduous fruit trees, mainly wood and roots, and translocated the following spring toward leaves and fruits, hypothesis supported by data of various authors (Antonopoulos-Domis et al., 1988; Baldini et al., 1987; Frissel, 1997). Therefore the components involved in the contamination of fruit in the years following a single, acute deposition are both the soil reservoir and the plant reservoir. The relative importance of these reservoirs will change with time. Few experimental studies provided new information on the fruit activity in the years following that of deposition. Studies on gaseous deposition of 14CO2, CO35S and HTO to apple, raspberry, strawberry and blackcurrant (Stewart, 2002) showed that the propor-
191
tion of radionuclides carried over from one growth season to the next was very low. The authors assumed that a high proportion of the deposited radionuclides is retained in the leaf throughout the growth season, and is then lost at the end of the season when the leaves fall from the plants. In a more complex scenario 137Cs and 90Sr were deposited onto the above-ground part of the plant and onto the soil surface and the soil was not ploughed during the following years (Madoz-Escande et al., 1998, 2002). The 137Cs activity in the whole grape, juice, vine leaves and shoots decreased by approximately two orders of magnitude in the six years after deposition and, more in detail, by a factor of three between the first and the second year. These results are in agreement with those reported in the review on the concentration of 137Cs after the Chernobyl accident in various perennial tree products (Carini, 2001; Antonopoulos-Domis et al., 1990) and support the hypothesis that, other than the process of soil to plant transfer, that of retranslocation from storage organs to other plant components plays also a role in the first years after deposition. Results from a third study on vines (Arapis, 1999) also provided information on the 134Cs activity of grapes one year after dry deposition, but showed a reduction (up to 4 orders of magnitude) considerably larger than that observed in the studies of grapes and apricots discussed above. Discrepancies between results from different studies come also out for Sr. The work carried out by Madoz-Escande et al. (1998, 2002) showed that, in contrast to 137Cs, the 90Sr concentrations in whole grape, juice and vine leaves tended to increase by a factor 2 to 5 in the first three years, while data on the time dependence of 90Sr concentration in various fruits collected after deposition from the Chernobyl accident (Juznic, 1989) and reported in the review (Carini, 2001) showed a reduction of transfer from soil to apples, pears and blackcurrants by a factor of 2 or more from 1987 to 1988.
6. Radionuclide transfer from soil to fruit Additional information to the soil to fruit transfer discussed in the review (Carini, 2001) has been provided by the FAO/IAEA/IUR Co-ordinated Research Project (CRP) on bThe Classification of Soil Systems
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F. Carini et al. / Science of the Total Environment 359 (2006) 188–193
on the Basis of Transfer Factors of Radionuclides from Soil to Reference PlantsQ. Data obtained by Sasaki, Tashiro and Gunji, were collected by Uchida (personal communication, 2001). New information is given with soil to fruit Transfer Factors (TFs) for Pb (order of 10 4) in apple and mandarin grown on twelve soils in Japan. They were two orders of magnitude higher than those for U and Th and in general higher in mandarin than in apple. The only TFs for U and Th reported in the review concerned melon (Tsukada and Nakamura, 1998) and watermelon (IAEAIUR, 1997) and were two-three orders of magnitude higher (10 3 ) than those for apple and mandarin. Data on soil characteristics to compare such different results were not available.
7. Conclusions New information additional to that summarised in the original review carried out by the Fruits Working Group has provided further results and knowledge. Some gaps in knowledge on deposition velocities of gaseous radionuclides on fruit plants have been filled by recent results on 14CO2, CO35S and HTO (tritiated water) deposition to apple, strawberry, blackcurrant and raspberry. Deposition velocities of 14 CO2 and CO35S are of the same magnitude as those observed for other crops; however they significantly differ between fruit crops. Additional information for radiocaesium and radiostrontium confirms the importance of direct deposition on fruit, but knowledge is still insufficient to draw any conclusions on the role of the different variables affecting this process. Results on deposition of 14CO2, CO35S and HTO to apple, raspberry, strawberry and blackcurrant, and of 137 Cs and 90Sr to vines have confirmed that the process of translocation of radionuclides from the aboveground part to fruit occurs to a greater extent during the time from fruit development to beginning of ripening for those radionuclides mobile in the phloem. The residual activity in fruit in the years following that of deposition shows a decrease of various order of magnitude, depending not only on the kind of radionuclide and the kind of plant, but also, presumably, on a different anthropic intervention on the soil-plant system. Processes of retranslocation from storage
organs to other plant components and of transfer from soil to plant would be expected to be responsible for residual fruit contamination, but their respective role has not yet been clearly defined. Soil to fruit transfer factors provided for U, Th and Pb in apple and mandarin fill gaps in a topic area where only a very limited amount of information had been collected previously.
Acknowledgements The authors are grateful for the financial support to the Fruits Working Group by the Food Standards Agency (formerly Ministry of Agriculture, Fisheries and Food- MAFF), UK, and the Environment Agency for England and Wales, UK, and for the support and resources made available by International Atomic Energy Agency for meetings and report production.
References Antonopoulos-Domis M, Clouvas A, Tervisidis F, Gagianas A. A correlation study between radiocaesium deposition and contamination in a variety of Mediterranean agricultural products. Environmental radioactivity in the Mediterranean area, Barcelona, Spain; 1988. p. 503 – 9. Antonopoulos-Domis M, Clouvas A, Gagianas A. Compartment model for long-term contamination prediction in deciduous fruit trees after a nuclear accident. Health Phys 1990;58(6): 737 – 41. Arapis G. Reduction of radiocontamination of vines by the method of bnon-lethal defoliationQ. Personal communication; 1999. Atkinson CJ, Webster AD. The influence of the development of temperate fruit tree species on the potential for their uptake of radionuclides. J Environ Radioact 2001;52:131 – 46. Baldini E, Bettoli MG, Tubertini O. Effects of the Chernobyl pollution on some fruit trees. Adv Hortic Sci 1987;1(2):77 – 9. Brenot J, Noordijk H. Food consumption. Underlying data for derived emergency reference levels. Post-Chernobyl action. In: Sinnaeve J, Gerber G, editors. Report of CEC radiation protection; 1991. p. 61 – 98. Carini F. Radionuclides in plants bearing fruits: an overview. J Environ Radioact 1999;46(1):77 – 97. Carini F. Radionuclide transfer from soil to fruit. J Environ Radioact 2001;52:237 – 79. Carini F, Bengtsson GB. Post-deposition transport of radionuclides in fruit. J Environ Radioact 2001;52:215 – 36. Carini F, Anguissola Scotti I, Montruccoli M, Silva S. 134Cs foliar contamination of vine: translocation to grapes and transfer to wine. In: Gerzabek MH, editor. Proceedings of the international symposium on radioecology ten years terrestrial radioecological
F. Carini et al. / Science of the Total Environment 359 (2006) 188–193 research following the chernobyl accident Austrian soil science society and federal environment agency, Vienna, Austria; 1996. p. 163 – 9. Carini F, Atkinson CJ, Collins C, Coughtrey PJ, Eged K, Fulker M, et al. Modelling and experimental studies on the transfer of radionuclides to fruit. Journal of Environmental Radioactivity; in press. Frissel MJ. A report of the IAEA-IUR joint project bTransfer of radionuclides from air, soil, and freshwater to the foodchain of man in tropical and subtropical environmentsQ. In: Gerzabek MH, editor. Proceedings of the XXVII annual meeting of ESNA, WG 3; 1997. p. 189 – 95. Fulker MJ. The role of fruit in the diet. J Environ Radioact 2001; 52:147 – 57. Green N. The effect of storage and processing on radionuclide content of fruit. J Environ Radioact 2001;52:281 – 90. IAEA-IUR. Data from the CRP on bTransfer of radionuclides from air, soil, and freshwater to the foodchain of man in tropical and subtropical environmentsQ. provided by Frissel MJ. International Atomic Energy Agency. Modelling the transfer of radionuclides to fruit Report of the Fruits Working Group of BIOMASS Theme 3 BIOsphere Modelling and ASSessment programme IAEA-BIOMASS-5, Vienna, Austria; 2003. Juznic K. On transfer of 90Sr from soil to plants. VIth report of the working group soil-to-plant transfer factors. Bilthoven, The Netherlands7 RIVM; 1989. p. 45 – 51. Kinnersley RP, Scott LK. Aerial contamination of fruit through wet deposition and particulate dry deposition. J Environ Radioact 2001;52:191 – 213. Linkov I, Carini F, Collins C, Eged K, Mitchell NG, Mourlon C, et al. Radionuclides in fruit systems: model–model intercom-
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parison study. Sci Total Environ 2005—this issue. doi:10.1016/ j.scitotenv.2005.08.002. Madoz-Escande C, Colle C, Brechignac F, Jouglet H, Fernandez V. Time dependent evolution of 137Cs and 90Sr deposited as aerosols on vine. Poster presented at the 8th annual meeting of SETAC-Europe, Bordeaux, 14–18 April; 1998. Madoz-Escande C, Colle C, Adam C. Evolution of cesium and strontium contamination deposited on vines. Radioprotection—Colloques 2002;37:C1-515 – 20. Mitchell NG. Development of an international radionuclide flux database: Progress Report. Mouchel Report No 48146001TN1; 1997. January–June. Mitchell NG. Models for radionuclide transfer to fruits and data requirements. J Environ Radioact 2001;52:291 – 307. Ould-Dada Z, Fairlie I, Read C. Transfer of radioactivity to fruit: significant radionuclides and speciation. J Environ Radioact 2001;52:159 – 74. Ould-Dada Z, Carini F, Eged K, Kis Z, Linkov I, Mitchell NG, et al. Radionuclides in fruit systems: model–data intercomparison study. Sci Total Environ (submitted for publication). Stewart A. The deposition of C-14, S-35 and H-3 to fruit crops. PhD Thesis. Department of Environmetal Science and Technology, Imperial College, London; 2002. Stewart A, Brudenell A, Collins CD. Deposition of gaseous radionuclides to fruit. J Environ Radioact 2001;52:175 – 89. Tsukada H, Nakamura Y. Transfer factors of 31 elements in several agricultural plants collected from 150 farm fields in Aomori, Japan. J Radioanal Nucl Chem 1998;236:123 – 31. Uchida S. Personal communication; 2001. Venter A, Coughtrey PJ, Carini F, Inoue Y. Foreword. J Environ Radioact 2001;52:117 – 22.
Radionuclides in fruit systems: A review of experimental studies F. Carini a,*, N. Green b, S. Spalla a a
Universita` Cattolica del Sacro Cuore, Institute of Agricultural and Environmental Chemistry, Faculty of Agricultural Sciences, Via Emilia Parmense 84, I-29100 Piacenza, Italy b NRPB, Chilton, Didcot, Oxfordshire OX11 0RQ, United Kingdom Received 29 November 2004; accepted 25 May 2005 Available online 13 September 2005
Abstract Existing information on processes and parameters analysed in experimental studies on fruits was reviewed at the inception of the activities of the IAEA BIOMASS Fruits Working Group. Additional information on experimental studies, collected during the activities of the Group and not included in the Review, is presented and discussed in this paper. Studies on deposition of 14 CO2, CO35S and 3H2O in the gas phase to apple, raspberry, strawberry and blackcurrant have filled gaps in knowledge of uptake of gaseous pollutants in fruit plants, quantifying processes of deposition, translocation and carry-over between seasons. Measurements over a period of six years on vine plants contaminated via leaves and soil by dry deposition of 137Cs and 90Sr have improved knowledge of the processes of direct deposition to fruit, translocation and carry-over of radionuclides from year to year. Additional information is given on soil to fruit transfer of U, Th and Pb for apple and mandarin grown under intensive agricultural conditions. D 2005 Elsevier B.V. All rights reserved. Keywords: Radionuclides; Fruits; Experimental studies
1. Introduction Radionuclides introduced into the environment during routine nuclear operations, as a consequence of nuclear accidents, or from waste disposal facilities can migrate through foodchains, thus posing a potential risk for the population. Fruit is an important component of diet, particularly for some groups of the population who rely heavily on fruit consumption, * Corresponding author. Tel.: +39 0523599478; fax: +39 0523599448. E-mail address: [email protected] (F. Carini). 0048-9697/$ - see front matter D 2005 Elsevier B.V. All rights reserved. doi:10.1016/j.scitotenv.2005.05.034
either by choice or because of their geographical location. Consumption in Europe can be as much as 25% of the total diet (Brenot and Noordijk, 1991). Information on the behaviour of radionuclides in the fruit systems was recognized as a gap in knowledge in the assessment of the internal dose to human beings from contaminated food ingestion (Carini, 1999; Venter et al., 2001). On the basis of the work completed by a Task Force on radionuclide transfer to fruits under the International Union of Radioecologists (IUR) in 1996, a Fruits Working Group was established within the framework of the International Atomic Energy Agency (IAEA) Biosphere Modelling and Assessment (BIO-
F. Carini et al. / Science of the Total Environment 359 (2006) 188–193
MASS) Co-ordinated Research Programme, under Theme 3 in late 1997. The objective was to improve understanding of the processes affecting the transfer of radionuclides in fruit systems. The activities were completed in November 2000. They included a review (Atkinson and Webster, 2001; Carini, 2001; Carini and Bengtsson, 2001; Fulker, 2001; Green, 2001; Kinnersley and Scott, 2001; Mitchell, 2001; Ould-Dada et al., 2001; Stewart et al., 2001. These references are hereafter referred to collectively as bthe reviewQ), the derivation of a fruit conceptual model, the compilation of a database of model parameters for use in fruit models (Mitchell, 1997), the collection of information from experimental studies additional to that summarised in the review (this paper), two model intercomparison studies (Linkov et al., 2005—this issue) and a validation study (Ould-Dada et al., submitted for publication). A final document has been issued by the IAEA (2003). A summary is included in a special issue of the Journal of Environmental Radioactivity on the results of the BIOMASS Co-ordinated Research Programme (Carini et al., in press). The activities of the Fruits Working Group were initiated by discussions on the processes leading to the contamination of fruit after transfer of radionuclides into various fruit systems and on the parameters measured in experimental studies and used in modelling activities. The state of the art at that time has been published in the review. During the subsequent meetings, new information from recently completed or ongoing experimental studies or from those not included in the review was presented and discussed. The aims were to collect additional information, to improve knowledge of processes, and to provide data valuable either for the further development of models or for the testing and validation of existing ones. The present paper summarises information on those experimental studies that have formed the basis for discussion. The most important results, in terms of data or understanding of processes, have been compared with the existing review.
2. Deposition of gaseous radionuclides to fruit plants Information reported in the review on the uptake of gaseous pollutants by vegetation showed that, although
189
uptake by vegetable crops has been studied fairly extensively, there has been relatively little investigation into uptake by fruit crops (Stewart et al., 2001). Recent studies supplied new information on the process of deposition of 14CO2, CO35S and HTO (tritiated water) in apple, raspberry, strawberry and blackcurrant (Stewart, 2002). The deposition velocity calculated per unit plant mass (Vgw: the mass normalised deposition velocity: cm3 g 1 s 1) revealed significant differences between fruit plants for deposition of 14CO2 and CO35S, confirming what reported in the review. However the deposition velocities calculated per unit area of the plant (Vga: the standard deposition velocity: cm s 1) were of the same magnitude as those observed for other crops, ranging from 1.9 10 2 to 9.4 10 2 for 14CO2 and from 5.4 10 2 to 1.5 10 1 for CO35S. The authors suggested that a single deposition velocity for all crops should be used in assessment studies. This should be the highest value, unless a probabilistic approach was being pursued (Stewart, 2002).
3. Post deposition transport of radionuclides in fruit plants 3.1. Direct deposition to fruit The processes of interception, retention and absorption of radioactive fallout can directly involve the fruit. Many variables contribute to the process of direct contamination of fruit: the physiological stage of the plant at time of deposition, the radionuclide, the kind of deposit (wet or dry), the fruit surface properties, the fruit’s physical exposure to the fallout and to the subsequent weathering, and the time elapsed between deposition and harvest. Information reported in the review showed that few data in the literature distinguished between the contribution of the activity directly deposited on the fruit surface and that translocated from other plant components to the fruit (Carini and Bengtsson, 2001). New information on this topic has been supplied from two series of data concerning dry deposition of Cs and Sr on vines bearing some bunches purposely protected from direct deposit, which allowed to distinguish the process of leaf to fruit translocation from that of direct deposition.
F. Carini et al. / Science of the Total Environment 359 (2006) 188–193
The two datasets, from Madoz-Escande et al. (1998, 2002) and Arapis (1999), are compared with those on vines reported in the review (Carini et al., 1996). The three experimental works were carried out under different conditions — field or controlled, used different devices to simulate the radioactive source and considered different plant stages at deposition time. Results, expressed as percentage of the whole activity in fruit at harvest, show a wide variability from 13% to 97%, revealing the difficulty of reproducing natural conditions and the complexity in data interpretation, and underlining as an appraisal of the contribution from the different variables to contamination of fruit at harvest is still difficult.
4. Translocation from the above-ground parts to fruit
% of the activity in whole plant
Data on radionuclide translocation from the aboveground parts to fruit were discussed in the review (Carini and Bengtsson, 2001). The datasets concerned mainly Cs and Sr on apple, grapevine and strawberry, and, in a few cases, gooseberry, blueberry, orange, pear and redcurrant. Two recent experimental studies provided new information on the translocation of gaseous 14CO2, CO35S and HTO to apple, raspberry, strawberry and blackcurrant (Stewart, 2002) and of dry 137Cs and 90 Sr to vines (Madoz-Escande et al., 1998, 2002). Results are not comparable, being expressed with different units of measure and carried out under
70
14C(g)
60
35S(g)
50
3H(g)
40 30 20 10 0 ring
flowe
t n men matio velop f. de
f. for
ening
f. rip
stage at time of deposition Fig. 1. 14C, 35S and 3H activity in apple fruit at harvest after foliar deposition at four growing stages.
% of the intercepted activity
190
7
90Sr
6
137Cs
5 4 3 2 1 0 late flowering
beginning of ripening
stage at time of deposition Fig. 2. 137Cs and 90Sr activity in grapes at harvest after foliar deposition at two growing stages.
different experimental conditions. However some general conclusions can be drawn. Both studies derived the radionuclide concentration in fruits after deposition at different phenological stages. As an example, Fig. 1 shows the allocation of 14C, 35S and 3H to apple fruit and Fig. 2 that of 137Cs and 90 Sr to grapes, both studied after deposition at various growing stages. When the contamination process occurred at flowering, in absence of fruits, 35S, 3H (Fig. 1) and 137Cs (Fig. 2) were translocated to fruits, while very little 14C and 90Sr were remobilised from leaves to fruits late in the growing season, demonstrating that the partitioning of radionuclides in the plant is radionuclide-dependent. Results also confirm that the time of contamination relative to production of the fruit plays a role in the percentage found in the fruit at harvest. Even if the times of contamination considered under the two scenarios are not comparable, it is possible to infer that the highest values in fruit at harvest occurred following deposition between fruit development (Fig. 1) and beginning of ripening (Fig. 2). This lapse of time is regarded by horticulturists as the stage of the higher demand of fruits for photosynthetic products from leaves, and that could explain the higher transport of 14 C and of 137Cs, analogous to potassium, from leaves to fruits. The temporal changes in concentrations of 137Cs and 90Sr in the grape have also been studied picking fruits 2, 7, 20 and 30 days after contamination (Madoz-Escande et al., 1998). Fig. 3 shows as, after the initial deposition, the distribution of 137Cs increased with time due to the process of leaf to fruit
% of intercepted activity
F. Carini et al. / Science of the Total Environment 359 (2006) 188–193 8 7 6 5 4 3 2 1
Cs Sr
0 0
10
20
30
40
days from contamination to harvest Fig. 3. 137Cs and 90Sr activity in grapes at different harvest times after foliar deposition at beginning of ripening.
translocation, conversely, that of 90Sr decreased initially, due to the loss process, and then increased in the last ten days, although not significantly.
5. Residual activity Little information has been reported on the residual activity of radiocaesium and radiostrontium in fruit in the years following that of deposition from the Chernobyl accident (Carini, 2001). Generally speaking, when the scenario is a single deposition event, the residual activity in the plant is regarded as deriving from soil as the donor compartment, through the processes of soil to plant transfer and/or resuspension and splash. Although this may hold true for annual plants, it is not always so for perennial plants such as fruit trees. Information collected in the review (Carini, 2001; Mitchell, 2001) provided some evidence that radiocaesium, once introduced into the plant, could be retracted from leaves at fall into perennial organs of deciduous fruit trees, mainly wood and roots, and translocated the following spring toward leaves and fruits, hypothesis supported by data of various authors (Antonopoulos-Domis et al., 1988; Baldini et al., 1987; Frissel, 1997). Therefore the components involved in the contamination of fruit in the years following a single, acute deposition are both the soil reservoir and the plant reservoir. The relative importance of these reservoirs will change with time. Few experimental studies provided new information on the fruit activity in the years following that of deposition. Studies on gaseous deposition of 14CO2, CO35S and HTO to apple, raspberry, strawberry and blackcurrant (Stewart, 2002) showed that the propor-
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tion of radionuclides carried over from one growth season to the next was very low. The authors assumed that a high proportion of the deposited radionuclides is retained in the leaf throughout the growth season, and is then lost at the end of the season when the leaves fall from the plants. In a more complex scenario 137Cs and 90Sr were deposited onto the above-ground part of the plant and onto the soil surface and the soil was not ploughed during the following years (Madoz-Escande et al., 1998, 2002). The 137Cs activity in the whole grape, juice, vine leaves and shoots decreased by approximately two orders of magnitude in the six years after deposition and, more in detail, by a factor of three between the first and the second year. These results are in agreement with those reported in the review on the concentration of 137Cs after the Chernobyl accident in various perennial tree products (Carini, 2001; Antonopoulos-Domis et al., 1990) and support the hypothesis that, other than the process of soil to plant transfer, that of retranslocation from storage organs to other plant components plays also a role in the first years after deposition. Results from a third study on vines (Arapis, 1999) also provided information on the 134Cs activity of grapes one year after dry deposition, but showed a reduction (up to 4 orders of magnitude) considerably larger than that observed in the studies of grapes and apricots discussed above. Discrepancies between results from different studies come also out for Sr. The work carried out by Madoz-Escande et al. (1998, 2002) showed that, in contrast to 137Cs, the 90Sr concentrations in whole grape, juice and vine leaves tended to increase by a factor 2 to 5 in the first three years, while data on the time dependence of 90Sr concentration in various fruits collected after deposition from the Chernobyl accident (Juznic, 1989) and reported in the review (Carini, 2001) showed a reduction of transfer from soil to apples, pears and blackcurrants by a factor of 2 or more from 1987 to 1988.
6. Radionuclide transfer from soil to fruit Additional information to the soil to fruit transfer discussed in the review (Carini, 2001) has been provided by the FAO/IAEA/IUR Co-ordinated Research Project (CRP) on bThe Classification of Soil Systems
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on the Basis of Transfer Factors of Radionuclides from Soil to Reference PlantsQ. Data obtained by Sasaki, Tashiro and Gunji, were collected by Uchida (personal communication, 2001). New information is given with soil to fruit Transfer Factors (TFs) for Pb (order of 10 4) in apple and mandarin grown on twelve soils in Japan. They were two orders of magnitude higher than those for U and Th and in general higher in mandarin than in apple. The only TFs for U and Th reported in the review concerned melon (Tsukada and Nakamura, 1998) and watermelon (IAEAIUR, 1997) and were two-three orders of magnitude higher (10 3 ) than those for apple and mandarin. Data on soil characteristics to compare such different results were not available.
7. Conclusions New information additional to that summarised in the original review carried out by the Fruits Working Group has provided further results and knowledge. Some gaps in knowledge on deposition velocities of gaseous radionuclides on fruit plants have been filled by recent results on 14CO2, CO35S and HTO (tritiated water) deposition to apple, strawberry, blackcurrant and raspberry. Deposition velocities of 14 CO2 and CO35S are of the same magnitude as those observed for other crops; however they significantly differ between fruit crops. Additional information for radiocaesium and radiostrontium confirms the importance of direct deposition on fruit, but knowledge is still insufficient to draw any conclusions on the role of the different variables affecting this process. Results on deposition of 14CO2, CO35S and HTO to apple, raspberry, strawberry and blackcurrant, and of 137 Cs and 90Sr to vines have confirmed that the process of translocation of radionuclides from the aboveground part to fruit occurs to a greater extent during the time from fruit development to beginning of ripening for those radionuclides mobile in the phloem. The residual activity in fruit in the years following that of deposition shows a decrease of various order of magnitude, depending not only on the kind of radionuclide and the kind of plant, but also, presumably, on a different anthropic intervention on the soil-plant system. Processes of retranslocation from storage
organs to other plant components and of transfer from soil to plant would be expected to be responsible for residual fruit contamination, but their respective role has not yet been clearly defined. Soil to fruit transfer factors provided for U, Th and Pb in apple and mandarin fill gaps in a topic area where only a very limited amount of information had been collected previously.
Acknowledgements The authors are grateful for the financial support to the Fruits Working Group by the Food Standards Agency (formerly Ministry of Agriculture, Fisheries and Food- MAFF), UK, and the Environment Agency for England and Wales, UK, and for the support and resources made available by International Atomic Energy Agency for meetings and report production.
References Antonopoulos-Domis M, Clouvas A, Tervisidis F, Gagianas A. A correlation study between radiocaesium deposition and contamination in a variety of Mediterranean agricultural products. Environmental radioactivity in the Mediterranean area, Barcelona, Spain; 1988. p. 503 – 9. Antonopoulos-Domis M, Clouvas A, Gagianas A. Compartment model for long-term contamination prediction in deciduous fruit trees after a nuclear accident. Health Phys 1990;58(6): 737 – 41. Arapis G. Reduction of radiocontamination of vines by the method of bnon-lethal defoliationQ. Personal communication; 1999. Atkinson CJ, Webster AD. The influence of the development of temperate fruit tree species on the potential for their uptake of radionuclides. J Environ Radioact 2001;52:131 – 46. Baldini E, Bettoli MG, Tubertini O. Effects of the Chernobyl pollution on some fruit trees. Adv Hortic Sci 1987;1(2):77 – 9. Brenot J, Noordijk H. Food consumption. Underlying data for derived emergency reference levels. Post-Chernobyl action. In: Sinnaeve J, Gerber G, editors. Report of CEC radiation protection; 1991. p. 61 – 98. Carini F. Radionuclides in plants bearing fruits: an overview. J Environ Radioact 1999;46(1):77 – 97. Carini F. Radionuclide transfer from soil to fruit. J Environ Radioact 2001;52:237 – 79. Carini F, Bengtsson GB. Post-deposition transport of radionuclides in fruit. J Environ Radioact 2001;52:215 – 36. Carini F, Anguissola Scotti I, Montruccoli M, Silva S. 134Cs foliar contamination of vine: translocation to grapes and transfer to wine. In: Gerzabek MH, editor. Proceedings of the international symposium on radioecology ten years terrestrial radioecological
F. Carini et al. / Science of the Total Environment 359 (2006) 188–193 research following the chernobyl accident Austrian soil science society and federal environment agency, Vienna, Austria; 1996. p. 163 – 9. Carini F, Atkinson CJ, Collins C, Coughtrey PJ, Eged K, Fulker M, et al. Modelling and experimental studies on the transfer of radionuclides to fruit. Journal of Environmental Radioactivity; in press. Frissel MJ. A report of the IAEA-IUR joint project bTransfer of radionuclides from air, soil, and freshwater to the foodchain of man in tropical and subtropical environmentsQ. In: Gerzabek MH, editor. Proceedings of the XXVII annual meeting of ESNA, WG 3; 1997. p. 189 – 95. Fulker MJ. The role of fruit in the diet. J Environ Radioact 2001; 52:147 – 57. Green N. The effect of storage and processing on radionuclide content of fruit. J Environ Radioact 2001;52:281 – 90. IAEA-IUR. Data from the CRP on bTransfer of radionuclides from air, soil, and freshwater to the foodchain of man in tropical and subtropical environmentsQ. provided by Frissel MJ. International Atomic Energy Agency. Modelling the transfer of radionuclides to fruit Report of the Fruits Working Group of BIOMASS Theme 3 BIOsphere Modelling and ASSessment programme IAEA-BIOMASS-5, Vienna, Austria; 2003. Juznic K. On transfer of 90Sr from soil to plants. VIth report of the working group soil-to-plant transfer factors. Bilthoven, The Netherlands7 RIVM; 1989. p. 45 – 51. Kinnersley RP, Scott LK. Aerial contamination of fruit through wet deposition and particulate dry deposition. J Environ Radioact 2001;52:191 – 213. Linkov I, Carini F, Collins C, Eged K, Mitchell NG, Mourlon C, et al. Radionuclides in fruit systems: model–model intercom-
193
parison study. Sci Total Environ 2005—this issue. doi:10.1016/ j.scitotenv.2005.08.002. Madoz-Escande C, Colle C, Brechignac F, Jouglet H, Fernandez V. Time dependent evolution of 137Cs and 90Sr deposited as aerosols on vine. Poster presented at the 8th annual meeting of SETAC-Europe, Bordeaux, 14–18 April; 1998. Madoz-Escande C, Colle C, Adam C. Evolution of cesium and strontium contamination deposited on vines. Radioprotection—Colloques 2002;37:C1-515 – 20. Mitchell NG. Development of an international radionuclide flux database: Progress Report. Mouchel Report No 48146001TN1; 1997. January–June. Mitchell NG. Models for radionuclide transfer to fruits and data requirements. J Environ Radioact 2001;52:291 – 307. Ould-Dada Z, Fairlie I, Read C. Transfer of radioactivity to fruit: significant radionuclides and speciation. J Environ Radioact 2001;52:159 – 74. Ould-Dada Z, Carini F, Eged K, Kis Z, Linkov I, Mitchell NG, et al. Radionuclides in fruit systems: model–data intercomparison study. Sci Total Environ (submitted for publication). Stewart A. The deposition of C-14, S-35 and H-3 to fruit crops. PhD Thesis. Department of Environmetal Science and Technology, Imperial College, London; 2002. Stewart A, Brudenell A, Collins CD. Deposition of gaseous radionuclides to fruit. J Environ Radioact 2001;52:175 – 89. Tsukada H, Nakamura Y. Transfer factors of 31 elements in several agricultural plants collected from 150 farm fields in Aomori, Japan. J Radioanal Nucl Chem 1998;236:123 – 31. Uchida S. Personal communication; 2001. Venter A, Coughtrey PJ, Carini F, Inoue Y. Foreword. J Environ Radioact 2001;52:117 – 22.