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Published online 9 August 2005
Published in J Environ Qual 34:1497-1507 (2005)
DOI: 10.2134/jeq2004.0274
© 2005 American Society of Agronomy, Crop Science Society of America, and Soil Science Society of America
677 S. Segoe Rd., Madison, WI 53711 USA
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TECHNICAL REPORTS

Ecological Risk Assessment

Uptake and Transport of Radioactive Nickel and Cadmium into Three Vegetables after Wet Aerial Contamination

Joëlle Fismesa,*, Guillaume Echevarriaa, Elisabeth Leclerc-Cessacb and Jean Louis Morela

a Laboratoire Sols et Environnement, UMR 1120, ENSAIA-INPL/INRA, 2 avenue de la Forêt de Haye, BP 172, 54 505 Vandoeuvre-lès-Nancy cedex, France
b Agence nationale pour la gestion des déchets radioactifs, 1-7 rue Jean Monnet, 92 298 Châtenay-Malabry cedex, France

* Corresponding author (Joelle.Fismes{at}ensaia.inpl-nancy.fr)

Received for publication July 15, 2004.

   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
 REFERENCES
 
Knowledge of radionuclide or trace element retention and translocation to plants following an aerial contamination event, for example, sprinkling with contaminated water, is necessary for the evaluation of human exposure through consumption of contaminated vegetables. The fate of 63Ni and 109Cd in all plant parts of three different vegetables after wet deposition on leaves or on fruits was studied. Lettuce (Lactuca sativa L.), radish (Raphanus sativus L.), and bean (Phaseolus vulgaris L.) grown under controlled conditions in a growth chamber were contaminated with 63Ni and 109Cd either on leaves, by means of two different contamination methods (a single early contamination and a repetitive one), or on bean husks (third contamination method: a single contamination at a late stage). Spiked and nonspiked organs were harvested at maturity and radionuclide contents were measured. The fraction retained was on average 56% of the initially administered doses of 63Ni and 87% of 109Cd. The leaf-to-other organ translocation factor was considerably higher for 63Ni (on average 43% of retained radioactivity) than for 109Cd (8%). Nickel-63 migrated throughout the whole plant following foliar contamination, and mainly toward young leaves, seeds in formation, and sink organs, whereas 109Cd migrated to a much lesser extent and only to the organs that were closest to the spiked one, and not at all into fruit. After a fruit contamination event, both radionuclides were translocated into the seeds of spiked fruits. Radionuclide retention and translocation were not affected by plant species, but principally by the type of organ contaminated.

Abbreviations: RC, retention coefficient • TC, translocation coefficient


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
 REFERENCES
 
PLANTS CAN BE significant food vectors of radioactive contamination and the knowledge of radio-contamination of edible plants can improve the understanding of exposure through ingestion. Radionuclides released as fallout can be deposited either on the ground or on the leaves of plants. Thus, terrestrial plants can be contaminated by radionuclides through two pathways, namely root uptake and surface deposition. Surface deposition can be direct by radionuclide fallout, or indirect by sprinkling the plants with contaminated water (following the deposit and the leaching of radionuclide fallout onto the ground after a nuclear accident, or following a direct contamination of surface and/or ground waters by radioactive waste). Contamination of edible parts may occur by translocation of radio-elements within the plants after interception by exposed plant surfaces. This pathway is especially relevant for those crops where there is a large total leaf area relative to the fruit surface area or when contamination takes place before fruit emergence.

Foliar uptake of minerals and subsequent translocation within other organs have been investigated by many authors for plant nutrition (Chamel and Bougie, 1974; Giaquinta, 1983; Gougler and Geiger, 1981; Scalla, 1991; Thorne, 1985; Tiercelin, 1998; Tissut and Séverin, 1984), but other than after the Chernobyl accident, relatively few investigations have been undertaken into aerial uptake and translocation of radio-elements, especially on radionuclides, other than 37Cs and 90Sr, which were present at Chernobyl.

Before absorption and translocation into plants, radionuclides need to be previously retained by contaminated organ surfaces (Chamel and Bougie, 1977; Delmas et al., 1969). Retention of aerial contaminants depends on four groups of factors, specifically, factors related to the chemical and physical characteristics of the radionuclide concerned (form, nature, concentration, etc.), factors related to the mechanism of aerial contamination (wet or dry deposits, drop size in case of wet deposit, etc.), factors related to environmental conditions (temperature, air humidity, rainfall, wind, etc.), and factors related to plants (age, organ disposition, cuticle thickness, metabolism, etc.). Leaching of aerial organs by rain following aerial contamination is the main cause of soluble mineral element losses (Hoffman et al., 1992; Marschner, 1986; Middleton, 1959; Witherspoon and Taylor, 1970). However, in dry conditions, wind is the main cause of pollutant removal present on the leaf surface (Martin, 1965; Moorby and Squire, 1963). Thus, data measured in greenhouse experiments (Bengtsson, 1992; Kopp et al., 1990; Zehnder et al., 1995) show lower losses of radionuclides from plants than data obtained under field conditions. Chemical translocation following an aerial contamination is the result of both absorption into aerial organs (leaves or fruit) and subsequent translocation in the vascular system to other plant compartments. For most terrestrial plants, the main process of solute absorption is root absorption, as foliar and fruit absorption are strongly limited by the external tissues (cuticle, etc.) of epidermis cells (Marschner, 1986). Thus, a low translocation of chemicals can be due to a low absorption of these elements by the receptor organs (capacity of the chemicals to cross the different cell barriers i.e., the cuticle and the cell membrane), and/or to the low mobility of these elements in vessels. Aerial absorption of solutes depends on environmental conditions, the chemical–physical properties of the elements deposited, and on plant internal factors like metabolic activity (Marschner, 1986). Solute penetration requires a gradient of concentration through the cuticle and consequently a translocation of the solutes to maintain a low concentration in the underlying apoplast (Scalla, 1991).

The Chernobyl accident has demonstrated how important it is to have good knowledge and understanding of the initial uptake and the time-dependent distribution of radionuclides to the various plant parts. Indeed, activity measurements of various vegetables and fruits after Chernobyl accident as well as other experiments (Carini and Lombi, 1997; Katana et al., 1988; Kopp et al., 1990; Zehnder et al., 1995) have shown that fruit take up radioactive substances from fallout deposited on the leaves. The knowledge of the relative contribution of both direct edible organ contamination and of subsequent processes of nonedible-to-edible organ translocation is necessary to determine human exposure through food ingestion.

Nickel-63 and 109Cd are radioactive elements used as activation products in the nuclear industry and are found in nuclear waste. This waste can contaminate surface waters directly or ground waters by the convection of radionuclides from a underground storage place to the discharge system of the biosphere. A risk of plant contamination exists each time that surface or ground contaminated waters are used to irrigate crops. For safe disposal assessment studies, the knowledge of the environmental behavior of 63Ni and 109Cd is required to estimate their probable translocation through the human food chain after a wet aerial deposition on crops. Indeed, 65% of surface and ground waters are used for irrigation in France (Ducrocq, 1990; Tiercelin, 1998), and sprinkling is usually practiced for seed, fruit, and vegetable irrigation (Deloye and Rebour, 1958; Israelsen and Hansen, 1962; Pillsbury and Degan, 1968; Poirée and Ollier, 1971) to combat freezing (deposit of a film of insulating ice on the plants when the actinothermic temperature drops below –0.5°C) and also to fertilize some crops.

The present study concerns the surface deposition and the translocation of Ni and Cd in different parts (edible or not) of three staple vegetables with differing edible parts (leaf, fruit, root) following aerial contamination by sprinkling with polluted water. Our main interest is to study the accumulation of wet isotope deposit in the food chain (activity in edible organs, i.e., fruits, leaves, and storage organs), to evaluate the risk for human health. However, activity was also measured in all plant organs that are an intermediate in transport (e.g., stems) because this knowledge is essential to understand those factors governing translocation processes and to forecast the remobilization of radionuclides from these organs to fruit after initial contamination.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 CONCLUSIONS
 REFERENCES
 
The variables considered in the present study are three species of plants, two radionuclides, and three processes of aerial contamination.

Plants and Experimental Cultivation
Three commonly eaten plant species, whose edible parts are represented by different organs (roots, leaves, and fruits), were chosen—‘Salto’ radish, ‘Reine de Mai’ lettuce, and ‘Banjo’ dried bean.

Soil samples were collected in a private garden located in Lorraine, France, from the upper horizon (0–20 cm). Soil was calcareous and exhibited a slightly alkaline pH (7.9), an organic C content of 2.2%, and sufficient nutrients for vegetable growth. After air-drying and sieving (5 mm), 1 kg of dry soil was placed in plastic pots. To prevent radionuclide loss, the bottom of the pots was blocked with plastic.

Lettuce and radish seeds were sown directly into pots at 0.5- to 2-cm and 2- to 3-cm depths, respectively. After germination, seedlings were thinned to one lettuce and five radishes per pot. Three bean seedlings pregerminated on compost material were transplanted at the one- to two-leaf stage.

The soil was watered to 80% of the holding capacity, with nutrient solutions that brought essential nutrients in concentrations adapted to the specific requirements of each variety, i.e., 17 mg N kg–1 (equivalent to 50 kg N ha–1) and 7 mg S kg–1 (equivalent to 20 kg S ha–1) for radish, 12 mg N kg–1 (equivalent to 35 kg N ha–1) and 3 mg CaO kg–1 (equivalent to 10 kg CaO ha–1) for lettuce, and 20 mg N kg–1 (equivalent to 60 kg N ha–1) for bean. The soil was then moistened daily to maintain the humidity at 80% of the field moisture capacity for lettuce and bean, and at 60 to 70% for radish. An additional supply of 10 mg N kg–1 was provided to the lettuce just before heart formation. No pesticide was used during the experiment.

The pots were placed in three different greenhouses to respect the specific requirements of the different vegetables for optimum growth, flowering, and fruit maturation, under the following temperature and light conditions: 11°C day/7°C night (photoperiod 12 h) from seeding to one real leaf stage and then at 15°C day/10°C night (photoperiod 14 h) from one-leaf stage to root filling for radish; at 15°C day/10°C night (photoperiod 14 h) from seeding to eight-leaf stage and then at 20°C day/15°C night (photoperiod 14 h) from eight-leaf stage to coring stage for the lettuce; at 20°C day/16°C night (photoperiod 14 h) from seedling to stem elongation and then at 26°C day/20°C night (photoperiod 16 h) from stem elongation to fruit maturation for bean.

Application of Radionuclides
Two series of experiments were performed, one contaminating plants with only 63Ni, which is a beta emitter (half-life 120 yr), and the other one with only 109Cd, which emits gamma radiation (half-life 1.3 yr). Chloride salts of the radionuclides 63NiCl2 and 109CdCl2 in aqueous solution were used to contaminate the plants. The 63Ni stock solution had an activity concentration of 14700 kBq mL–1 and the 109Cd stock solution of 1500 kBq mL–1. Aliquots of these stock solutions were diluted with distilled water to obtain final solutions containing 430 kBq 63Ni mL–1 and 135 kBq 109Cd mL–1 at the date of plant contamination. Three different methods of contamination were tested (Fig. 1) : (i) a single contamination at an early stage, on the middle leaf of the first (oldest) trifoliate leaf of bean, on the eighth leaf of the lettuce, and on the third real leaf of radish; (ii) three successive contaminations during growth on the previous organs, every 10 d for bean, 8 d for lettuce, and 5 d for radish because of their short growth period; and (iii) a single contamination at a late stage, only on the ripest husk of bean. These three methods of contamination were respectively identified as (i) "early leaf contamination," (ii) "chronic leaf contamination," and (iii) "late fruit contamination." The oldest leaves and ripe husks were chosen because they are regarded as the major source of carbohydrate for the fruits in formation, and the other developing organs. The leaves selected (for radish, lettuce, and bean) or fruit (for bean only) were treated on the upper surface with, respectively, 50 µL for both single supplies (at early stage and at late stage) and 3 x 20 µL for the successive supplies of carrier-free solution of 63NiCl2 for one series of experiments, and 109CdCl2 for the other series. About 5 microdroplets of solution were applied to simulate sprinkling. These droplets dried within 1 h. Contaminated leaves and fruit were tagged by a white paint spot. Each combination plant x radionuclide x contamination method was replicated five times.



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  		Fig. 1. Spiked organs according to the three methods of contamination, and organs analyzed at harvest (edible stage).

 
Sampling and Analysis
The plants were harvested at maturity—when radish roots were tuberized (40 d of cultivation), when lettuce presented a well-developed core (stage called coring, reached after 80 d of cultivation), and when bean plants were fully ripe (3 mo of cultivation). All the organs were sampled to determine the activity distribution within the whole plant. Leaves that fell during cultivation were collected progressively and analyzed with the other leaves after harvest. Shoots were separated from roots, and aerial organs were also separated into contaminated leaves, uncontaminated oldest leaves and uncontaminated youngest leaves, and leaves of the core for lettuce. For bean, we separated lateral leaves of the first trifoliate leaf, stems, contaminated husks and uncontaminated husks, grains of the contaminated husks, and grains of the uncontaminated husks (Fig. 1, Table 1). The various organs were not washed to avoid desorption of radionuclides. They were weighed fresh, at harvest, air-dried under ventilation at 70°C for 24 h, weighed again, and then mixed for further analysis.


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  		Table 1. Different parts, spiked or not, harvested for each of the three vegetables.

 
The soils adhering to the roots and rhizosphere were collected, dried, and an aliquot of each soil was sampled for further analysis to estimate possible exsudation of radionuclides in soil after translocation from aerial spiked parts to roots. Plants contaminated with 63Ni and their adherent soils were mineralized by acid attack (25 min, 250°C) with a mixture (1:3:3) of H2SO4 (98%), HNO3 (98%), and H2O2 (70%). Nickel-63 concentrations in each sample were then measured by ß– counting using a liquid scintillation spectrometer (scintillation cocktail: Ready safe, BECKMAN; spectrometer: Tri-carb Liquid Scintillation Analyser, Model PACKARD 460 CD, A Canberra Co., Australia) whereas 109Cd concentrations were determined in each sample by direct gamma spectrometry (Model PACKARD COBRA, A Canberra Company, Australia).


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 CONCLUSIONS
 REFERENCES
 
Growth of the Contaminated Vegetables
The biomass of lettuce and bean cultivated in pots, under controlled conditions (Table 2), was weak and the high seedling density led to early senescence of lower bean leaves, due to competition for light. Fruit production (number of fruit) was also weak, but weight and length of bean husks was not affected by pot cultivation. Biomass production of radishes was equally unaffected by pot cultivation. No phytotoxicity symptoms were observed for plants whatever the radionuclide activity concentration of microdrops or the chloride salt form. No necrosis was visible at the drop application sites, whether on leaves or on fruit.


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  		Table 2. Dry biomass (g) of the different parts of the three vegetables studied at time of harvest.

 
Radionuclide Retention Coefficient
The fraction of applied 63Ni and 109Cd remaining in whole plants at harvest was defined as the retained fraction. The retention coefficient (RC) represents the sum of the activity retained in whole plants at harvest (sum of the radioactivity adsorbed on the spiked organs and absorbed into them, and translocated to other organs) compared to radioactivity administered per plant.


Retention coefficients of 63Ni and 109Cd by the three vegetables are reported in Table 3.


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  		Table 3. Retention coefficients of 63Ni and 109Cd in three spiked vegetables at time of harvest, expressed as radioactivity in whole plants at harvest/radioactivity administered per plant.

 
Plants showed a relatively low retained fraction of 63Ni (from 48 ± 3% to 63 ± 8% of administered radioactivity) compared with 109Cd (from 80 ± 17% to 93 ± 1% of administered radioactivity). In contrast, whichever the radionuclide considered, no clear trend was visible between the different vegetables despite of the very different leaf morphology and wettability (form and dimension of the leaves, cuticle thickness, roughness, pilosity) of the studied vegetables. The retained fraction of 63Ni varied, from 53 ± 12% to 60 ± 11% in lettuce, depending on the method of contamination, from 48 ± 3% to 52 ± 6% in radish and from 49 ± 4% to 63 ± 8% in bean. In the same way, the retained fraction of 109Cd varied from 89 ± 3% to 91 ± 5% in lettuce, from 87 ± 2% to 93 ± 1% in radish, and from 80 ± 17% to 92 ± 6% in bean (Table 3). Data showed that the 63Ni retained fraction was higher in the case of fruit contamination (63 ± 8%) than in the case of leaf contamination (from 49 ± 4% to 58 ± 7% depending on the method of leaf contamination). In contrast, the 109Cd retained fraction was lower following bean husk contamination (80 ± 17%) than following leaf contamination (from 89 ± 3% to 92 ± 6% depending on the method of leaf contamination). Except in radish, the 63Ni and 109Cd retained fractions tended to increase with fractionation of the contamination with time.

Radionuclide Translocation Coefficient
The radioactivity detected in all untreated plant parts represents the translocated activity. The translocation coefficient (TC) is expressed as the ratio of the sum of the activity recovered in nonspiked organs at harvest compared to retained radioactivity in whole plant at harvest (RC).


Translocation coefficients of 63Ni and 109Cd in the three vegetables are reported in Table 4.


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  		Table 4. Translocation coefficients of 63Ni and 109Cd from spiked leaf or fruit to nonspiked organs of three vegetables at time of harvest, expressed as radioactivity in nonspiked organs at harvest/radioactivity in whole plants at harvest.

 
Leaf- or fruit-to-nonspiked organ translocation coefficients were considerably higher for 63Ni than for 109Cd: from 0.35 ± 0.10 to 0.67 ± 0.24 for 63Ni, depending on the method of contamination and the organ considered, against 0.01 ± 0 to 0.16 ± 0.04 for 109Cd. As observed for the retention coefficient, the translocation coefficient modulated in the same order of magnitude for all plant species: the 63Ni translocation coefficient varied from 0.35 ± 0.10 to 0.41 ± 0.30 in lettuce, according to the method of contamination; from 0.26 ± 0.08 to 0.48 ± 0.15 in radish; and from 0.31 ± 0.07 to 0.67 ± 0.24 in bean. The 109Cd translocation coefficient varied from 0.07 ± 0.01 to 0.10 ± 0.01 in lettuce, from 0.06 ± 0.02 to 0.16 ± 0.04 in radish, and from 0.01 ± 0 to 0.07 ± 0.03 in bean.

For both radionuclides and all plant species, translocation of radionuclides from spiked leaf to nonspiked organs was always lowest when contamination was chronic vs. single. In bean, the highest translocation was noted from spiked fruits: 0.67 ± 0.24 for 63Ni compared with 0.31 ± 0.07 to 0.54 ± 0.14 in the case of leaf contamination, and 0.07 ± 0.03 for 109Cd against 0.01 ± 0 following leaf contamination.

Distribution of Radioactivity in Nonspiked Organs
The extent to which radionuclides are translocated away from the point of contamination and the translocation direction have been estimated by analyzing all noncontaminated organs. Results are reported in Fig. 2 and 3 for the lettuce, in Fig. 4 and 5 for the radish, and in Fig. 6 and 7 for the bean.



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  		Fig. 2. Distribution of 63Ni retained at harvest in lettuce, following (A) an early single leaf contamination or (B) a chronic leaf contamination (up. leaves: leaves upper to the spiked leaf; low. leaves: leaves lower to the spiked leaf).

 


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  		Fig. 3. Distribution of 109Cd retained at harvest in lettuce, following (A) an early single leaf contamination or (B) a chronic leaf contamination (up. leaves: leaves upper to the spiked leaf; low. leaves: leaves lower to the spiked leaf).

 


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  		Fig. 4. Distribution of 63Ni retained at harvest in radish, following (A) an early single leaf contamination or (B) a chronic leaf contamination (up. leaves: leaves upper to the spiked leaf; low. leaves: leaves lower to the spiked leaf).

 


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  		Fig. 5. Distribution of 109Cd retained at harvest in radish, following (A) an early single leaf contamination or (B) a chronic leaf contamination (up. leaves: leaves upper to the spiked leaf; low. leaves: leaves lower to the spiked leaf).

 


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  		Fig. 6. Distribution of 63Ni retained at harvest in bean, following (A) an early single leaf contamination, (B) a chronic leaf contamination, or (C) a late fruit contamination (up. leaves: leaves upper to the spiked leaf; low. leaves: leaves lower to the spiked leaf).

 


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  		Fig. 7. Distribution of 109Cd retained at harvest in bean, following (A) an early single leaf contamination, (B) a chronic leaf contamination, or (C) a late fruit contamination (up. leaves: leaves upper to the spiked leaf; low. leaves: leaves lower to the spiked leaf).

 
Nickel-63 applied to leaves could be translocated from spiked leaves to both lower and upper organs, whatever the method of contamination and plant species; therefore, following leaf contamination, 63Ni was present in all noncontaminated organs, that is, other leaves, stem, roots, and fruits when fructification was observable (husks and seeds of bean) (Fig. 2, 4, and 6). However, despite the capacity of 63Ni to migrate through all organs of the three vegetables considered, only a small fraction of 63Ni was translocated to the nonspiked lower leaves of plants (from 1 ± 1 to 2 ± 2%) and to roots of lettuce (from 3 ± 2 to 4 ± 2%) or bean (about 1 ± 1%); most of the radioactivity was translocated into the young organs undergoing growth and development (from 24 ± 6% to 30 ± 9% to the lettuce cores) (Fig. 2), to the sink storage organs (from 19 ± 2% to 36 ± 4% to the radish roots) (Fig. 4) or to the reproductive organs during their formation (from 7 ± 4% to 9 ± 5% to the bean husks and from 17 ± 9 to 39 ± 10% to the bean seeds) (Fig. 6A and 6B). In radish, a nonnegligible fraction of 63Ni (from 6 ± 1% to 11 ± 3%) was also translocated into developing upper leaves. When applied to bean husks, 63Ni was mostly translocated to inside seeds (61 ± 17%) (Fig. 6C); a large fraction of applied 63Ni (33 ± 13%) stayed in/on the spiked husks, while little radioactivity was detected in the closest organs (3 ± 6% in stem, 2 ± 1% in the close husks, and 1 ± 1% in the seeds of close husks); no radioactivity was measured in roots nor in leaves (Fig. 6C). When contamination was chronic, the observed decrease in translocation corresponded to a lower translocation of 63Ni to organs undergoing development, specifically, radish roots (19 ± 2% against 36 ± 4% in case of the single early contamination), lettuce cores (24 ± 6% against 30 ± 9%), or bean seeds (17 ± 9% against 39 ± 10%).

Contrary to what was observed for 63Ni, 109Cd was moderately translocated to other organs after leaf or fruit surface contamination (Fig. 3, 5, and 7). In lettuce, from 3 ± 1% to 5 ± 2% of the applied radioactivity was found at harvest in the upper leaves and from 3 ± 2% to 4 ± 1% in the roots (Fig. 3). Similarly, from 1.5 ± 1% to 6.5 ± 3% of the applied 109Cd was translocated from spiked radish leaves to upper leaves and from 4 ± 0.6% to 8.5 ± 0.5% from leaves to roots (Fig. 5). In bean, no radioactivity was detected in nonspiked leaves or in roots. Following leaf contamination, 109Cd generally migrated only into the stem and into the other two leaves of the spiked trifoliate leaf, but no radioactivity was found in seeds (Fig. 7A and 7B). After fruit contamination, no further radionuclides were found in roots, and just a small fraction of the applied 109Cd was measured in the inside seeds; 1.5 ± 1% of the applied radioactivity was detected in nonspiked husks, but no sign of radioactivity was found in the seeds inside these husks (Fig. 7C).

To compare data derived from nonsimilar organs of the plant presenting very different biomasses, radionuclide activity concentration in each organ was also calculated (calculations not reported): these data showed that 63Ni and 109Cd were two to seven times more concentrated in the nonspiked leaves of the contaminated bean trifoliate leaf (closest leaves) than in the other upper leaves; this fact was not visible when considering only the total distribution of radioactivity to the different organs due to the very low weight of the two nonspiked leaves of the trifoliate leaf as compared with the biomass of the other upper leaves. In the same way, 63Ni and 109Cd were twice as concentrated in the upper leaves of radish as in the roots, despite the higher biomass of the roots.

Activity Measured at Harvest in the Rhizospheric Soil
Table 5 describes the contamination of rhizospheric soils after aerial plant contamination by 63Ni and 109Cd. Radioactivity measured in rhizospheric soils following aerial contamination with 63Ni was substantially higher than the radioactivity due to 109Cd plant contamination (from 1010 to 6270 Bq of 63Ni kg–1 dry soil against from 20 to 160 Bq of 109Cd kg–1 dry soil). No quantitative difference was observed between the three vegetables studied. Translocation of 63Ni in soil increased slightly when leaf contamination was chronic. Except in lettuce where results were equivalent, the opposite trend was observed for 109Cd. The migration of both radionuclides from spiked bean fruit to soil was lower than following a leaf contamination.


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  		Table 5. Activity concentrations of 63Ni and 109Cd (Bq kg–1 dry soil) in rhizospheric soils at harvest.

 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
CONCLUSIONS
 REFERENCES
 
Growth and Development of Vegetables Cultivated on Polluted Soils
No phytotoxicity symptoms (necrosis) appeared on spiked organs, which therefore leads us to the supposition that radionuclide absorption and its following translocation into other organs was not perturbed by the toxicity responses of the plants.

Radionuclide Retention on Vegetable Spiked Organs
In our experiment, most of the loss due to meteorological conditions was reduced because plants were cultivated in growth chambers (precipitation-free conditions) and watered at the soil surface to avoid leaching of aerial parts. A high air humidity (70%) was maintained in the growth chambers to slow down the drying of contaminated droplets applied onto leaf or fruit surfaces. However, the growth chambers were ventilated by an air flow. At harvest, aerial organs were not rinsed to avoid desorption of the chemicals supplied. Thus, we worked in optimal experimental conditions for radionuclide absorption and adsorption; our results then correspond to the hypothetical conditions for the highest retention.

In these experimental conditions, radionuclide losses can be due to translocation of the chemicals in soil by root exudation after aerial absorption and translocation into the plants, to volatilization of the molecules nonabsorbed after the drying of deposited droplets (Martin, 1965; Moorby and Squire, 1963), and/or to plant surface destruction and water losses through transpiration (Marschner, 1986; Tissut and Séverin, 1984). Losses of 63Ni were high whatever the method of contamination, the organ spiked, and the plant species (from 37 ± 8% to 52 ± 3% of applied molecules). As high activity concentrations of radionuclides were measured in rhizospheric soils at harvest, we can suppose that 63Ni is quickly absorbed by leaf and fruit surfaces, and successively quickly translocated into plants. On the other hand, losses of 109Cd were very low (a maximum of 20 ± 17% of the applied radionuclides), and only small quantities of 109Cd were measured at harvest in nonspiked organs and in soils, suggesting that this radionuclide was strongly adsorbed on the plant surface and/or quasi-immobile when absorbed.

No significant difference was noted in retention coefficients between the three vegetables studied, although lettuce leaves have very low pilosity, which is favorable to leaching; bean leaves are slightly hairy, retaining water droplets; and radish leaves are very downy, thus limiting the contact between water droplets and leaf surface. Thus, our results showed that in our experimental conditions, the wettability of leaves was not a dominating factor in radionuclide retention, which does not agree with observations by Bittel (1965) and Scalla (1991), who observed a different retention of water droplets applied to different plant leaf surfaces according to the leaf surface wettability. The results of the present study demonstrate that the chemical and physical properties of the two radionuclides in determining leaf retention were more important than the plant species itself, in opposition to the results of Carini et al. (1999), who observed no difference in leaf retention of 134Cs and 85Sr after wet deposition of microdrops of 134Cs and 85Sr (in the form of chloride salts in aqueous solution) on the upper surface of leaves or fruit, but a very pronounced difference between plant species studied [‘Golden Delicious’ apple tree (Malus domestica Borkh.), ‘Chardonnay’ grapevine (Vitis vinifera L.), and ‘Conference’ pear trees (Pyrus communis L.)]. Carini et al. (1999) and Pinder et al. (1987) showed that 134Cs and 85Sr losses from fruit surface were considerably lower than losses from leaf surfaces (by a factor of five). They suggested that absorption of radionuclides was higher in fruit skin than in leaf cuticle and that the growth and transpiration rate of fruit were low at the contamination stage, limiting the losses by transpiration and wax shedding (Moorby and Squire, 1963). Despite having been measured in very different plant species, these results contrast with ours, where retention of 63Ni and 109Cd after bean husk contamination was slightly weaker than after leaf surface contamination (21 ± 8% of 63Ni and 73 ± 13% of 109Cd in spiked husk, against from 23 ± 4% to 40 ± 6% of 63Ni and from 88 ± 2% to 91 ± 6% of 109Cd in spiked leaf). The weaker retention of 63Ni in the case of fruit contamination may be due to a strong translocation of 63Ni to the insides of the spiked husk seeds, with a limited translocation to roots and a consequently low exudation in soils (activity concentration of 1010 Bq kg–1 of dry soil measured in rhizospheric soil after fruit contamination, against an average of 5600 Bq kg–1 of dry soil measured in rhizospheric soil after foliar contamination).

Except in radish, where results were almost similar, the retention coefficients of both 63Ni and 109Cd were greater following a chronic repeated foliar contamination than in the case of an early single foliar contamination. As in this research, chronic contamination consisted in sprinkling events that occur later than single contamination, we can suggest that retention is also a function of time. No difference was observed on radish because of the shorter interval between the three radionuclide supplies.

Radionuclide Translocation and Distribution in Aerial Contaminated Plants
In our study, 63Ni and 109Cd were supplied in chloride salt form, the most favorable to foliar absorption (Takenaga, 1981). High humidity was maintained in the growth chambers to limit the volatilization of radionuclides and to increase solute penetration (inflating and spacing of the cuticle waxes). Plants were cultivated in optimal conditions of temperature, water supply, and fertilization to favor metabolism and therefore radionuclide penetration and translocation.

Nickel-63 was highly mobile in the three vegetables studied, whatever the organ spiked and the contamination method. In contrast, 109Cd was moderately mobile in the plants. Nickel is known to be highly mobile in the phloem, because it occurs in plant metabolism as a component of the urease enzyme (Neumann and Chamel, 1986), whereas 109Cd was shown to migrate weakly and slowly and to accumulate on/in the aerial contaminated organs (De Cormis, 1968; Gouthu et al., 1999; Romney et al., 1969). The bivalence of the 63Ni ion did not seem to constitute a limit to its migration, although Russel (1966) mentioned that bivalent ions are less mobile than monovalent ones.

Some authors (Carini et al., 1999; Delmas et al., 1973; Kopp et al., 1990) have also demonstrated that differences in translocation exist among plant species, depending on metabolic processes of plants, since the extent of transfer from spiked fruit to leaves was affected more by the kind of plant than by the difference in the radionuclides 134Cs and 85Sr. In the present research, translocation of 63Ni and 109Cd varied in the same order of magnitude in the three vegetables studies, while the metabolism of these plants was markedly different (formation of fruit for bean, filling up of an underground storage organ for radish, the development of foliar organs for lettuce). These results suppose that the plant species is less important in determining translocation possibilities than the chemical–physical form of the two radionuclides studied.

Distribution of the radionuclides 63Ni and 109Cd in nonspiked organs varied greatly among the three species studied, as shown by Carini et al. (1999) and Delmas et al. (1973) for 134Cs, 137Cs, and 85Sr. Thus, 63Ni migrated mainly to developing organs following foliar contamination (Carini et al., 1999; Delmas et al., 1973): from 17 ± 9% to 39 ± 10% of intercepted 63Ni was measured in bean seeds and from 7 ± 4% to 9 ± 5% in bean husks, from 24 ± 6% to 30 ± 9% in young developing leaves of lettuce, and from 19 ± 2% to 36 ± 4% in storage roots of radish. After bean fruit contaminations, 61 ± 17% of intercepted radioactivity was detected at harvest inside the seeds of contaminated husks. Apparently, seeds undergoing formation and development acted as a sink for absorbed elements (65Zn; Arora et al., 1970). On the other hand, 109Cd migrated only a small distance and most of the radioactivity was found at harvest only in organs close to the contamination point (i.e., stems, bean leaves located on the same trifoliate leaf as the spiked leaf), in accordance with the observations of Bengtsson (1992), Carini et al. (1999), and Katana et al. (1998) on 85Sr. No 109Cd was detected in bean seeds following foliar contamination. These results are in accordance with the works of Baldini et al. (1987) and Monte et al. (1990) on 137Cs and 103Ru, Bengtsson (1992) and Zehnder et al. (1995) on 134Cs and 85Sr, and Gouthu et al. (1999) on Rb, Zn, Fe, Nb, Cr, and Sc, who demonstrated that mobile radionuclides (Cs, Zn, Fe, and Rb) accumulated mainly in the fruit of trees after foliar contamination (in average 25% of the intercepted radioactivity), while radionuclides with a low mobility (Nb, Cr, Sc, Sr) were not present in the fruit. In the same way, Bittel and Clément (1965), Gerdung et al. (1999), and Middleton and Squire (1963) showed a translocation of mobile 134Cs from potato leaves to tubers (storage organ) similar to the 63Ni translocation observed in our experiment from radish leaves to filling storage roots (20–50% in the potato tubers and 19 ± 2% to 36 ± 4% in the radish roots). These authors also measured a translocation of 134Cs of 20% from bean leaves to bean fruit, while we found from 24 ± 13% to 48 ± 15% of the retained 63Ni in the bean fruit (husks and seeds) according to the method of leaf contamination. On the other hand, they noted a low translocation (4–7%) of mobile 134Cs from the leaves to the cabbage (Brassica oleracea L.) core, while we observed an important translocation (24 ± 6% to 30 ± 9%) of 63Ni from leaves to lettuce core. We also detected radioactivity (63Ni and 109Cd) in nonspiked bean husks following fruit contamination, while Katana et al. (1988) think that there was no translocation of radionuclides 85Sr and 134Cs from spiked fruits to nonspiked fruits. Yet it must be borne in mind that translocation of radionuclides does not occur only through the vascular system, and the observed contamination of nonspiked husks was probably due to the action of wind (the growth chambers were ventilated), which can move isotopes (as can rain) to other compartments. Nevertheless, Bittel and Clément (1965) suggested that radioelements accumulated principally in the peduncle, pericarp, and mesocarp of fruit, with little in seeds. We verified this for low mobility elements, such as 109Cd, but not borne out for mobile elements, such as 63Ni (from 17 ± 9% to 61 ± 17% according to the contaminated organ). We observed ascending and descending migration of radionuclides; this proves that radionuclides 63Ni and 109Cd radionuclides may also be transported in the phloem vessels.

In the present research, translocation of radionuclides decreased when contamination was chronic, compared with a single early contamination. A probable explanation is that late contamination of leaves in the case of chronic supplies took place during a phase of reduction of plant metabolism (Kopp et al., 1990; Lin et al., 1995; Moorby and Squire, 1963), and subsequently led to a decrease in element absorption and translocation (Chamel, 1990; Scalla, 1991). Thus, with aging, the metabolic activity of leaves is reduced and cuticle thickness increases, thereby limiting absorption; therefore, translocation toward fruit and storage organs decreases when fruits are mature and when storage organs are full, since carbohydrate flux is reduced (Ambler, 1964; Bittel, 1965). Our results confirm these facts, since 63Ni translocation from leaves to bean husks and seeds decreased with chronic supplies (7 ± 4% in the husks and 17 ± 9% in the seeds) as compared with a single early contamination (9 ± 5% and 39 ± 10%, respectively). In the same way, 63Ni translocation from leaves to radish roots decreased with chronic contamination (19 ± 2%), as compared with a single early contamination (36 ± 4%, respectively). This is consistent with the results of Anguissola Scotti (1995) and Gerdung et al. (1999), who demonstrated that the translocation of radionuclide 134Cs from leaves to fruit or to storage organs was reduced by half after fruit or storage organ filling. Another probable explanation is that the interval between the final supply, during chronic contamination, and the harvest was too short to allow the translocation of radionuclides from leaves to fruit or to storage organs (Aarkrog, 1969).

Finally, we noted an uptake into bean seeds of 61 ± 17% of the 63Ni retained following direct husk contamination, higher than a leaf-to-seed translocation of 39 ± 10% maximum, these results being consistent with those of Katana et al. (1988) for 134Cs.


   CONCLUSIONS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
REFERENCES
 
The knowledge of edible plant contamination by two nuclear activation radionuclides (i.e., 63Ni and 109Cd) following sprinkling irrigation with surface and/or ground polluted water was studied by applying both radionuclides either to leaves or to the fruit of three commonly used vegetable plant species, with varying edible parts (leaf/fruit/root). Activity in the different organs, remaining either after direct deposition or translocation, was then measured at vegetable maturity.

Translocation of radionuclides varied depending on various factors, such as the chemical–physical properties of the radioelement, the method of contamination, the time between contamination and harvest, and the metabolic stage of the plants. The chemical–physical characteristics of the studied radionuclides seemed to be the most important factors affecting their fate in the plants, while plant species and method of contamination played a second role in radionuclide retention and distribution.

The analysis of indirectly contaminated organs demonstrated that 63Ni, an essential micronutrient, can be transported away from the point of contamination, throughout the various plant organs. This radionuclide was transported mainly to developing organs after leaf contamination, proving that mobile elements migrate essentially from source to carbohydrate sinks. The process of leaf-to-fruit translocation was less effective than the direct contamination of the fruit through wet deposition. However, even when plant contamination occurred before fruit initiation, mobile radionuclides migrated toward fruit during fruit formation. On the other hand, 109Cd translocation declined strongly with distance from the contamination source, and no radioactivity was found in bean seeds following a foliar contamination. When contamination was chronic, corresponding to both early and late contamination, radionuclide translocation declined, underlining the importance of plant metabolism in translocation processes.


   ACKNOWLEDGMENTS
 
Financial support for the present research was provided by Andra (Agence nationale pour la gestion des déchets radioactifs).


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
 REFERENCES
 


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