Journal of

Environmental Radioactivity 61 (2002) 21–31

Transfer of 137Cs and 60Co from irrigation waterto a soil–tomato plant system

C. Sabbaresea,*, L. Stellatoa, M.F. Cotrufoa, A. D’Onofrioa,A. Ermicea, F. Terrasia, S. Alfierib

aDipartimento di Scienze Ambientali, Seconda Universit "aa di Napoli, via Vivaldi, 81100 Caserta, ItalybCentrale Nucleare Garigliano, Sogin, Sessa Aurunca, Caserta, Italy

Received 19 December 2000; received in revised form 27 April 2001; accepted 9 May 2001

Abstract

An experiment has been performed at the nuclear power plant of Garigliano (Caserta,Italy), aiming at the measurement of transfer factors of 137Cs and 60Co radionuclides from theirrigation water to a soil–plant system, with particular attention to the influence on such

transfers of the irrigation technique (ground or aerial). Tomato plants were irrigated weeklywith water contaminated with 137Cs and 60Co (about 375Bq/m2 week), using both irrigationtechniques. After 13 weeks, fruits, leaves, stems, roots and soil were sampled, and radionuclide

concentrations were measured by high-resolution g spectroscopy. It was found that the activityallocated to the plant organs is significantly dependent upon the irrigation technique,amounting to 2.1% and 1.6% of the activity given in the cultivation for aerial treatment and

0.4% and 0.3% for the ground treatment, for 137Cs and 60Co respectively. The activityabsorbed by plants is allocated mainly in leaves (>55%), while less then 10% is stored in thefruits, for both irrigation techniques. Transfer factors (soil–plant and irrigation water–plant)of tomato plants and of weeds have been determined for 137Cs and 60Co, as well as for natural40K in the soil. r 2002 Elsevier Science Ltd. All rights reserved.

Keywords: 60Co; 137Cs and 40K transfer factor; Foliar sorption; Root sorption; Tomato

1. Introduction

The assessment of internal doses to humans from the ingestion of radionuclidespresent in agricultural products requires detailed information on the main processes

*Corresponding author. Tel.: +39-0823-274-6335; fax: +39-0823-274-6055.

E-mail address: sabbares@na.infn.it (C. Sabbarese).

0265-931X/02/$ - see front matter r 2002 Elsevier Science Ltd. All rights reserved.

PII: S 0 2 6 5 - 9 3 1 X ( 0 1 ) 0 0 1 1 1 - 4

determining the route of radionuclides in the environment (Russel, 1966; Peterson,1983; IAEA, 1995). A large amount of data is available but, generally, they do notreflect natural conditions, and the mechanisms of translocation and mobility ofradionuclides within the soil–plant system are still not fully understood (Coughtrey& Thorne, 1983; Fresquez, Armstrong, Mullen, & Naranjo, 1998; Krouglov, Filipas,Alexakhin, & Arkhipov, 1997; Frissel, 1992; Roca & Vallejo, 1995; Desmet,Nassimbeni, & Belli, 1990).The knowledge of the contributions of direct contamination of plant fruits and of

the process of root to fruit transfer can improve the understanding of exposurethrough ingestion and of the mechanisms determining sorption and translocation.Agricultural soil can be contaminated because of a radioactive fallout in theatmosphere or because of irrigation which uses contaminated water. Plants growingon that soil absorb radionuclides by roots and/or by leaves. The radionuclidesabsorbed are transferred to the plant organs and their quantities are determined onthe basis of the kind of contamination source and of biological and environmentalprocesses. Plant physiology, soil characteristics, nuclide and the kind of plant areimportant parameters which influence sorption (Coughtrey & Thorne, 1983).Few studies have been designed that consider real agricultural conditions and very

few simulate contaminated rain which fall daily on the plants or on the soil surfaceonly. In the present research, both kinds of contaminations have been studied inexperimental conditions very close to the real-life situation. Transfer factors havebeen calculated considering the weekly increase of contamination in soil and theincrease of plant mass.

2. Materials and methods

An experimental field, 25� 30m2 long, was arranged in the soil area of the nuclearpower plant of Garigliano (Caserta, Italy) to perform the experiment. The field soilwas characterised by a horizon, 15–20 cm deep, that constituted the cover of thestratifications of materials used to fill the area. After adequate soil preparation andfertilization, the field was divided into 30 plots as displayed in Fig. 1. Tomato plantswere cultivated under the same conditions in 24 plots, 2� 2m2. Twelve plots (namedP) were contaminated using a low radioactivity water solution containing 137Cs and60Co, while the other 12 plots (named B) were not contaminated and used as blankreference. The remaining six plots were also contaminated but not cultivated (namedS) to obtain a control of uncultivated soil. The 12 P-plots were divided into twogroups of six plots named P1 and P2, and, in the same way, B1 and B2 for B plots.The indices 1 and 2 indicate aerial and ground irrigation, respectively. Hence, fivedifferent groups of plots with different cultivation kinds were obtained:

B1: aerial irrigation using uncontaminated water,B2: ground irrigation using uncontaminated water,P1: aerial irrigation using contaminated water,P2: ground irrigation using contaminated water,S: irrigation of nude soil using contaminated water.

C. Sabbarese et al. / J. Environ. Radioactivity 61 (2002) 21–3122

Each plot was irrigated weekly using 80 l of water with or without contaminationas explained. Water due to natural rain, eventually present during the week, wasmeasured and subtracted from 80 l; hence, every week supplemented water quantitywas variable but the contamination was the same.The contamination solution was obtained from two radioactive sources produced

by Amersham International containing 2MBq of 137Cs and 60Co, respectively. Thecontaminant solution used for irrigation was prepared in our laboratory in an acidenvironment and on April 7, 1998 contained (0.3170.02) kBq/ml of 137Cs and(0.3070.02) kBq/ml of 60Co. Weekly, 5ml of such solutions were used for irrigationof each plot. At the end of the 13 weeks long cultivation, each plot received(19.971.7) kBq of 137Cs and (19.571.7) kBq of 60Co, and the entire experimentalfield received about 700 kBq (19 mCi). It is worth emphasising that such activityrepresents 0.00019% of dumping liquids of the nuclear power plant of Garigliano;hence, the environmental impact was practically zero.After 13 weeks of cultivation, tomatoes, leaves, stems, roots and soil of the entire

experimental field were collected, separated per plot, disposed in containers andexposed to the sun for two days. Tomatoes were separated in ripe (red colour) andunripe (green colour) and were analysed separately; as no significant difference wasfound between the two categories, we have analysed the data without distinctionbetween ripe and unripe. Each part of the plant was placed in an oven at 601C for36 h and, then, at 1051C for 12 h to obtain a satisfactory sample dehydration. Thesample removed from the oven was pulverised to obtain a homogeneous matrix,which was weighed and placed in a 350 cm3 Marinelli beaker. The root samples wereplaced in 80 cm3 volume cylindrical containers because of the small amountavailable. In addition, weed grown in the plots was collected and analysed using thesame procedure as for tomato plants.Soil samples were collected in 20 cm deep 30� 30 cm2 cores from six contaminated

plots (S1, S2, P11, P15, P23, P24). Four 5 cm deep sections of soil cores of each plotwere considered. They were placed in an oven at 601C for 36 h and 1051C for 12 h,

Fig. 1. Experimental field scheme, with indications of the five treatments.

C. Sabbarese et al. / J. Environ. Radioactivity 61 (2002) 21–31 23

then sieved at 2mm and placed in 2.8 l Marinelli beaker. Moreover, in the P15 plot,six soil cores were collected at different positions to study the variability ofradionuclide concentration. Soil density was also determined in six plots, which weassumed to be representative of the entire experimental field. The samples wereextracted by using 270 cm3 volume metallic cylinders, which are open at two bases.Soil captured by cylinders was oven-heated and its mass was determined to calculatedry bulk density. High-resolution g-spectrometry was used to measure radionuclideactivities of the vegetable and soil samples. Two germanium hyperpure detectors(1.9 keV resolution and 30% efficiency) properly shielded, were used with standardelectronics, spectra were analysed, displayed and stored using a computer.The total efficiencies for each detection geometry were experimentally determined

by using the same matrix contaminated in a uniform way by a polynuclides sourceproduced by Amersham International. Radionuclide specific activities were obtainedfrom a quantitative analysis of g-ray spectra using the g lines at 661.6 keV (137Cs),1173.2 keV and 1332.5 keV (60Co). As potassium and caesium elements have similarchemical characteristics and 40K is naturally present in the soil, we also analysed the40K peak (1460.5 keV) present in g-ray spectra. Specific activities of each detectedradionuclide with reference to dry mass were determined.

3. Results and discussion

Data analysis was performed by dividing data per plant organs: tomatoes, leaves,stems, and roots. Then, we compared the results obtained on the same organ of thesix plots for the same treatment. Table 1 shows 137Cs, 60Co and 40K specific activitiesof the plant organs of all the plots. The variability in the six repetitions per organ andtreatment was found to be larger than the respective experimental errors. For thisreason, sample standard deviations in each group were taken as representative of thevariability of experimental conditions. In Fig. 2, mean values and standard errors ofmeasured specific activities are reported for the plant organs and the two treatments.The specific activities of uncontaminated plant organs are negligible compared to

the corresponding contaminated ones. The differences in 137Cs and 60Co resultsbetween the two irrigation techniques are statistically significant at 95% confidencelevel, as indicated by the Student t-test. It is evident from the results that theprocedure of irrigation strongly influences the sorption of radionuclides: the aerialirrigation (P1-plots) leads to higher contamination than the ground irrigation (P2-plots). The 40K values between the two irrigation techniques, are not different asexpected. In Table 2 the ratios between P1 and P2 specific activities for each plantorgan and each radionuclide are reported.The relative distribution of mean specific activities among plant organs has been

displayed in Fig. 3. No significant difference appears between the two irrigationtechniques; indeed, percentage values are about the same for P1 and P2. This factindicates that plants do not distinguish between the two methods of sorption andthey distribute the absorbed quantity of radioactivity in the same way. In addition,40K distributions in the plant organs are similar in the P1, P2, B1 and B2 plots, as

C. Sabbarese et al. / J. Environ. Radioactivity 61 (2002) 21–3124

Table 1

Specific activities of 137Cs, 60Co and 40K (Bq/kg) measured in all vegetable samples of the present experiment

P1 P2 B1 B2

137Cs 60Co 40K 137Cs 60Co 40K 137Cs 60Co 40K 137Cs 60Co 40K

Tomato 8272 3671 1524741 5.670.2 4.770.3 1466741 1.670.2 o0.1 1857747 0.770.2 o0.1 13107346371 2771 1314740 8.270.2 4.670.4 1560749 0.970.2 o0.1 1404737 0.570.2 o0.1 12197326571 1971 1411749 6.670.2 1.470.2 1518742 0.970.2 o0.1 1555741 0.370.1 o0.1 11147294771 1671 1272739 9.870.2 4.570.4 1513743 0.570.2 o0.1 1104729 0.670.2 o0.1 12887345771 1771 1646745 5.470.2 2.670.2 1497742 0.770.2 0.870.2 1428737 0.270.1 o0.1 13977364671 1471 1450742 9.470.3 2.270.2 1460742 0.970.2 0.870.1 1303735 o0.1 o0.1 1303734

Stem 34739 26677 1034738 48712 3178 1215739 2.170.3 o0.1 1381739 0.570.3 o0.1 1140731438711 28377 1147731 3872 2471 1137740 1.770.3 o0.1 957729 0.570.3 o0.1 110873022476 16175 951735 6271 3871 1435744 1.370.3 o0.1 938727 o0.1 o0.1 106272935079 20175 934728 5571 3871 799723 o0.01 o0.1 989729 o0.1 o0.1 92773824677 16475 746730 3371 2571 969733 1.370.3 o0.1 1027729 o0.1 o0.1 786722373710 22876 1057731 9373 5272 742726 o0.01 o0.1 807725 o0.1 o0.1 776722

Leaves 1269731 1136727 695726 12173 10173 726725 2.470.2 o0.1 747720 4.370.3 4.970.3 6977211040725 851720 710725 22776 16775 847728 1.770.2 0.870.1 675719 2.670.3 o0.1 713722750718 670717 688724 17475 13874 1006733 2.170.3 o0.1 647719 2.570.3 o0.1 730722840720 624715 596722 13174 10473 486722 1.170.3 1.070.2 653719 1.970.3 o0.1 645719841720 661716 620723 14974 11473 498722 2.170.2 o0.1 658719 1.870.3 o0.1 532717759718 585714 653723 33979 24077 456720 1.470.3 o0.1 464716 1.770.3 o0.1 535717

Root 9578 139710 1296799 4674 7676 886777 o0.2 o0.2 o0.2 o0.2 o0.2 7517695675 10178 12947100 2172 4073 15257116 o0.2 o0.2 12987121 o0.2 o0.2 132171019077 150711 14347110 2373 4374 13357103 o0.2 o0.2 13517104 o0.2 o0.2 149271137676 11579 1255796 1373 3673 1177791 o0.2 o0.2 469761 o0.2 o0.2 12667972773 5074 302754 3173 6775 14667112 o0.2 o0.2 787773 o0.2 o0.2 133671026376 11779 785773 3474 7576 1001779 o0.2 o0.2 13047100 o0.2 o0.2 13547104

Weed 5572 4871 863724 4372 4272 901735 0.370.2 o0.2 340711 o0.2 o0.2 7517697472 6972 1212732 4372 3471 874729 0.670.5 0.370.2 918727 o0.2 o0.2 132171013172 2971 859794 3172 2571 493723 1.770.3 o0.2 1003728 o0.2 o0.2 149271133474 3371 1011735 4272 4972 970732 o0.2 o0.2 705721 o0.2 o0.2 12667973871 3971 904725 1871 1971 975733 o0.2 o0.2 821724 o0.2 o0.2 12327941771 1671 847731 4972 6172 860730 o0.2 o0.2 536721 o0.2 o0.2 13547104

C.Sabbarese

etal./J.Enviro

n.Radioactivity

61(2002)21–31

25

Fig. 2. Mean specific activities obtained for the different radionuclides and plant organs using treatments P1, P2, B1 and B2.

C.Sabbarese

etal./J.Enviro

n.Radioactivity

61(2002)21–31

26

expected, but they are very different from the distributions of artificial radionuclides.Fruits contain about 60% of 40K of plant, stems and roots contain a percentagesimilar to that of 137Cs and 60Co. In conclusion, 40K is especially allocated in fruitsand 137Cs and 60Co are allocated especially in leaves, independent of treatment, asshown by Smolders and Merckx (1993) for hydroponic cultivation.To obtain data of direct human interest, we have also calculated specific activities

with reference to fresh mass of tomato. Such mean specific activities of fresh mass are(3.070.5) and (0.470.1) Bq/kg for 137Cs, (1.170.2) and (0.270.1) Bq/kg for 60Cofor P1 and P2 treatments, respectively and (7576) Bq/kg for 40K.Weed grown during the cultivation in the plots was also collected and analysed.

The mean specific activities of 137Cs and 60Co measured in weed samples show nodifferences within the measurement errors for the two treatments, as expected, due tothe small weed height above the ground (Table 1).To calculate transfer factors from soil to plants, specific activities of 137Cs, 60Co

and 40K in the upper 20 cm of soil have been measured. Mean specific activities are

Fig. 3. Percentage distribution of mean specific activities among plant organ for each analysed

radionuclide.

Table 2

Ratios between the specific activities of three radionuclides studied in two cultivation treatments (P1 and

P2)

Plant organs 137Cs 60Co 40K

Tomatoes 8.071.1 6.571.5 0.9670.04Stems 6.071.1 6.271.0 0.9370.11Leaves 4.870.9 5.371.0 0.9970.14Roots 2.470.6 2.070.4 0.8670.16

C. Sabbarese et al. / J. Environ. Radioactivity 61 (2002) 21–31 27

(2272) , (2172) and (1080796) Bq/kg for 137Cs, 60Co and 40K, respectively. About80% of the activity present in the soil is detained in the upper 5 cm. The variability ofradionuclide distributions in the plot area is characterised by a standard deviation ofabout 20%.Using the mean density of analysed soils of six plots (1.1570.08) g/cm3, the total

activities detained in the upper 20 cm of each plot of (5.170.9) , (4.870.8) and(250766) kBq/m2 for 137Cs, 60Co and 40K are in agreement with the total activitysupplied to the plot through water (5.070.9 kBq/m2 of 137Cs, 4.970.9 kBq/m2 of60Co). The resulting transfer factors, calculated as ratios of the plant specific activityto the soil activity (expressed in Bq/m2) at the end of the experiment (i.e. 13 weeks)are reported in Table 3 for P2 treatment. In order to compare the two kinds oftreatments, the transfer factors from irrigation water to plant was also calculated forP1 and P2 plots and are reported in Table 3, together with transfer factors fromirrigation water to weed.Coming back to soil–plant transfer, one may note from Table 3 that 137Cs has a

transfer factor about twice that of 40K. The average 137Cs to 40K specific activityratio in the soil is 0.029. On the other hand, if one considers the individual transfersto different plant organs, one can see from the data in Table 4 that the 137Cs to 40Kdiscrimination is strongly dependent on the compartment considered.The transfer factors obtained above have been calculated assuming that the total

amount of radionuclides was present in soil from the beginning of cultivationwithout considering its weekly increase due to the contaminated irrigation water.

Table 3

Transfer factors calculated in the described experiment

Transfer factor Cultivation

treatment

137Cs 60Co 40K

Soil–tomato plant

(Bq/kg/Bq/m2)

P2 0.01170.002 0.00970.002 0.00570.001

Soil–weed (Bq/kg/Bq/m2) P1, P2, S 0.00770.001 0.00770.001 0.00470.001Irrigation water–tomato plant

(Bq/kg/Bq/l)

P1 1572 1172 F

P2 3.070.7 2.270.6 FIrrigation water–weed (Bq/kg/Bq/l) P1, P2, S 1.970.2 1.770.2 F

Table 4

Ratios of 137Cs to 40K specific activities in plant organs relative to the corresponding average ratio in soil

P2 plant organs (137Cs/40K)plant/(137Cs/40K)soil

Tomatoes 0.17

Stems 1.81

Leaves 9.83

Roots 0.79

Weed 1.54

C. Sabbarese et al. / J. Environ. Radioactivity 61 (2002) 21–3128

Hence, the transfer factors reported in Table 3 are not comparable with thosemeasured in conventional experiments performed in soils that are fully contaminatedbefore plantation. In order to correlate the two approaches, we consider thedifferential equation which describes the increase of the activity in the tomato plantsas a function of the activity in the soil (Smolders & Merckx, 1993). If we neglect thedecrease of activity due to the radioactive decay and we assume an exponentialbehaviour of plant growth (constant value of relative growth rate, RGR), thevariation of the specific activity in the plant, C, is

dC

dt¼ UðtÞ �RGR�CðtÞ; ð1Þ

where UðtÞ; expressed in Bq/kg/d, is the increase of radionuclide activity at constantmass per mass unit and RGR is the relative growth rate of plant per mass unitexpressed in d�1. If UðtÞ and RGR are considered as constants, the solution ofEq. (1) is

CðtÞ ¼U

RGRð1� e�RGRtÞ; ð2Þ

where U=RGR is the asymptotic value of the specific activity absorbed from theplant. This is equal to FCs; where F is the soil–plant transfer factor and Cs is thespecific activity of radionuclide in the soil. Hence,

U ¼ F�RGR�Cs: ð3Þ

In our experiment CsðtÞ is increasing linearly with time and it can beexpressed as CsðtÞ ¼ kt; with k ¼ Csðt* Þ=t* and t� the time at the end of theexperiment.The solution of Eq. (1), in this case, is

CðtÞ ¼F�Csðt* ÞRGR� t *

f ðtÞ; ð4Þ

where

f ðtÞ ¼ e�RGR t � 1þRGR t:

The transfer factor F (Eq. (4)) has to be compared with the transfer factor Fccalculated by neglecting the time dependence of soil contamination, i.e. bynormalising the specific activity at time t�; Cðt�Þ; to the total activity supplied tothe soil during time t�; Csðt�Þ :

F ¼Cðt* Þ �RGR t*

Csðt* Þ � f ðt * Þ¼ Fc

RGR� t *

f ðt* Þ:

In our cultivation, we calculated Cðt�Þ from the average specific activities of the sixplots of the same treatment at the end of cultivation (t ¼ 92 d, RGR=0.051/d andk ¼ 54Bq/g/m2 for 137Cs and k ¼ 53Bq/g/m2 for 60Co). To correct the transferfactors calculated above, the following expression can be used:

F ¼ Fc�RGR�t* =f ðt* Þ:

C. Sabbarese et al. / J. Environ. Radioactivity 61 (2002) 21–31 29

The soil–tomato plant and soil–weed transfer factors calculated with this formula are0.014 and 0.011 Bq/g/m2 for 137Cs and 60Co, respectively. This correction increasesthe values by about 27%; accounting for the fact that the entire quantity ofradionuclides was not available to the plants from the beginning of the cultivation. Ifone takes into account the fact that uptake efficiency is in fact decreasing withplant growth (Sabbarese et al., 2000), the correction factor can be expected to belarger.

4. Conclusions

The experiment presented, regarding tomato plant cultivation in an agriculturalsoil with irrigation water containing 137Cs and 60Co, allowed one to conclude thattomato plants absorb less than 2% of the activity available in the soil. Theabsorption is about 6 times higher if contaminated irrigation was aerial withconsequent foliar absorption. In effect, the absorption of radionuclides from the rootis about 80% smaller than the foliar absorption; in turn, this fact means that thesame amount of contaminated irrigation water supplied at the base reducessignificantly the absorption with respect to aerial irrigation. The relative distribu-tions of radionuclide in the organs of tomato plants are not different for thetwo treatments. In both the treatments, more than 90% of the entire activity of theplant was absorbed by steams and leaves, and the remaining activity is distributedbetween the fruit and root. This finding differs from the values reported inCoughtrey and Thorne (1983), where a ratio between specific activities in fruits andin leaves of 0.48 is quoted to be compared with our average value of about 0.10. Onthe other hand, the 40K activity distribution is very different from the artificialradionuclides. The transfer factors are also calculated for tomato plants and forweed with respect to irrigation water and to soil contamination for 137Cs, 60Co and40K. Transfer factors for ground-irrigated tomato plants and for 137Cs are found tobe in agreement with the values quoted in Coughtrey and Thorne (1983) (0.011against 0.0072).

Acknowledgements

The authors are grateful to the technical operators of the Nuclear Power Plant ofGarigliano who participated in the experiment, and they thank, in particular, Mr. G.Fiore for his continuous attention for cultivation.

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