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Applied Radiation and Isotopes 68 (2010) 1154–1159

Contents lists available at ScienceDirect

Applied Radiation and Isotopes

0969-80

doi:10.1

� Corr

E-m

journal homepage: www.elsevier.com/locate/apradiso

Transfer of 238U, 230Th, 226Ra, and 210Pb from soils to tree and shrub species ina Mediterranean area

P. Blanco Rodrıguez a, F. Vera Tome a,�, J.C. Lozano a,b, M.A. Perez Fernandez a,c

a Natural Radioactivity Group, Facultad de Ciencias, Universidad de Extremadura, Avda. de Elvas s/n, 06071 Badajoz, Spainb Laboratorio de Radiaciones Ionizantes, Facultad de Ciencias, Universidad de Salamanca, 37008 Salamanca, Spainc Area de Ecologıa, Universidad Pablo Olavide, Carretera de Utrera km. 1, 41013 Sevilla, Spain

a r t i c l e i n f o

Article history:

Received 4 December 2009

Accepted 28 January 2010

Keywords:

Natural radionuclides

Soil-to-plant transfer factors

Arboreal species

Fruit

Leaves

43/$ - see front matter & 2010 Elsevier Ltd. A

016/j.apradiso.2010.01.045

esponding author. Tel.: +34 924289524; fax:

ail address: fvt@unex.es (F. Vera Tome).

a b s t r a c t

The soil-to-plant transfer factors of natural uranium isotopes (238U and 234U), 230Th, 226Ra, and 210Pb

were studied in a disused uranium mine located in the Extremadura region in the south-west of Spain.

The plant samples included trees (Quercus ilex, Quercus suber, and Eucalyptus cameldulensis) and one

shrub (Cytisus multiflorus). All of them are characteristic of Mediterranean environments. The activity

concentrations in leaves and fruit were determined for the tree species at different stages of growth. For

the shrub, the total above-ground fraction was considered in three seasons. For old leaves and fruit, the

highest activity concentrations were found in Eucalyptus cameldulensis for all the radionuclides studied,

except in the case of 230Th that presented similar activity concentrations in all of the tree species

studied. In every case, the transfer to fruit was less than the transfer to leaves. In the shrub, the results

depended on the season of sampling, with the highest value obtained in spring and the lowest in

autumn. Important correlations were obtained for 238U and 226Ra between the activity ratio in soils

with that in leaves or fruit.

& 2010 Elsevier Ltd. All rights reserved.

1. Introduction

Uranium (238U, 235U, and 234U) is an element widely distributedin the environment. Due to natural processes and the origin of itsisotopes 238U and 235U as primordial radionuclides, they arenaturally distributed. But also the exploitation of materials thatcontain these natural radionuclides may lead to an increase in theirconcentration levels (technologically enhanced naturally occurringradioactive material: TENORM) or to enhanced potential exposure(naturally occurring radioactive material: NORM). Soils, sediments,and waters are considered as major reservoirs of these uraniumisotopes. Usually, the more or less long retention of uranium in thenatural compartments also leads to enhanced presence of theirradioactive descendants (Soudek et al., 2007a). 238U heads theradioactive series 4n+2 that contains the radionuclides 234U, 230Th,and 226Ra, with the last being a radionuclide with majorenvironmental implications, because it heads an important sub-chain in which are included 222Rn and 210Pb, perhaps the maincontributors to the total dose for humans (UNSCEAR, 2000).

The determination of the levels in which the uranium isotopesand their descendents are present in different compartments ofecological importance has long been of concern for scientists

ll rights reserved.

+34 924289651.

(Gerzabek et al., 1998). Several studies have been carried out indifferent regions of the world about the distribution and mobilityof these radionuclides in the environment (Radhakrishna et al.,1996; Vera Tome et al., 2002), and about their transferencebetween natural compartments (Vera Tome et al., 2003; Chenet al., 2005; Al-Masri et al., 2008). However, there seem to be fewdata on concentration levels of the natural radionuclides in treesand shrubs in a Mediterranean area. These data could be veryuseful for use in radiological assessment models, but also thetransfer factors of natural radionuclides from soil to these plantspecies could indicate if these can be used as remediationalternatives to the use of other plant species such as herbs(Soudek et al., 2007b). Another important issue to consider is thatthe mobilization of radionuclides from the subsoil by trees couldlead to an increase in the activity concentrations on the surfacedue to the accumulation of radionuclides in their fallen leaves.

Therefore, the aim of this work was to study the activityconcentration of 238U, 230Th, 226Ra, and 210Pb in some trees(Quercus ilex, Quercus suber, and Eucalyptus cameldulensis) and oneshrub (Cytisus multiflorus) in different periods of their vegetativecycle. The study area lies in an old, recently restored uraniummine located in south-west Spain. Leaves of these trees werecollected at two stages of foliation (young and old leaves), as wellas their fruits, for subsequent analysis. Also, the above-groundfraction of the shrub was collected in three seasons and analysed.

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2. Materials and methods

2.1. Study area description

The study was performed at the rehabilitated uranium mine‘‘Los Ratones’’ in the Extremadura region (south-west of Spain). Themine covers an area of approximately 2.3 km2. It was in exploita-tion from 1960 to 1974, and the restoration work was completedbetween 1998 and 1999. The zone is characterized by a warmcontinental climate, with moderate winters and hot summers(annual average temperature of 15 1C), and moderate rainfall(typically 500 mm per year). Geologically, the area is classified asbasically granitic. Additional details about the characteristics of thisfacility, as well as several studies about the distribution, mobiliza-tion, and transfer factors between compartments of this area can befound elsewhere (Vera Tome et al., 2002, 2003).

2.2. Sampling and sample preparation

Three sampling sites were chosen along the soil toposequence(Fig. 1). For the estimation of the uncertainty associated with thesoil sampling (i.e., the inhomogeneity of the soil), a 5 m�5 mquadrat was considered per sampling point, divided into nine equalcells. In each cell, three soil cores were randomly sampled and then

Relative points location NS

Fig. 1. Map of the study zone in which the mine is located. The major topographic

features and the sampling points are marked. The sampling points are located

along the toposequence.

mixed. The resulting coefficients of variation for the concentrationof each radionuclide were: 27% for 238U, 30% for 230Th, 28% for226Ra, and 16% for 210Pb (Blanco Rodrıguez et al., 2008). After that,other sampling campaigns were performed in order to carry outthe study described here. Soil samples and leaves of Quercus ilex,Quercus suber, and Eucalyptus cameldulensis were collected at thethree sampling sites of the study area: At the first sampling sitealong the toposequence was located the Eucalyptus cameldulensis

individual; one individual of Quercus suber (henceforth Quercus

suber#1) was located at the second sampling site; and at the third,the Quercus ilex and another individual of Quercus suber (Quercus

suber#2) were chosen. For Quercus suber, the two individualsconsidered were located at sites with very different activityconcentrations of the uranium and thorium isotopes in the soils.For the other two species (Quercus ilex and Eucalyptus

cameldulensis) only one individual was considered. The samplingof the tree leaves was performed in summer of 2003 (youngleaves), and summer of 2004 (old leaves). Also, samples of the fruitsof these trees were collected in autumn of 2003. Finally, samples ofthe above-ground portion of one shrub (Cytisus multiflorus) werecollected in summer and autumn of 2003, and spring of 2004,located at the same site as the Eucalyptus cameldulensis.

From each soil sample, several aliquots were taken to determinepH, weight loss by ignition (LOI), and the concentrations of majorelements. Also, three granulometric fractions of each soil wereobtained.

Other aliquots were used for radiochemical assays. For this,aliquots of the soil samples (0.5 g) and vegetation samples (5 g)were completely digested in a microwave oven (Millestone ModelEthos 900) with the reagents HF and HNO3 (3:6 mL) for soilsamples, and HNO3 and H2O2 (6:1 mL) for vegetation samples(Lozano et al., 2001).

2.3. Radiochemical methods and measurement techniques

The activity concentrations of the uranium, thorium, andradium isotopes in every sample were determined by alpha-spectrometry with PIPS semiconductor detectors of 450 mm2

active area, housed in NIM spectrometers (Canberra, Mod.7401VR), coupled to low-noise preamplifiers, amplifiers, and amultichannel analyser. For the uranium and thorium isotopes,chemical separation using tri-n-butyl phosphate (TBP), andfurther thorium purification by anionic exchange resin (Jianget al., 1986) were followed by electrodeposition to form the high-resolution alpha sources (Vera Tome et al., 1994). The methodused for the determination of radium was based on chemicalpurification by precipitation of PbSO4/BaSO4, and the subsequentsource preparation by microprecipitation of Ba(Ra)SO4 (BlancoRodrıguez et al., 2002).

The activity concentration of 210Pb was determined by liquidscintillation counting (LSC) (Blanco et al., 2004). A LKB Quantulus1220TM spectrometer was used for the LSC measurements.

The radiotracers used for the determination of uranium,thorium, radium were 232U, 229Th, 225Ra, respectively. In the caseof 210Pb the radiochemical yield was determined by gravimetryusing stable lead as tracer.

3. Results and discussion

3.1. Activity concentrations

Table 1 lists some of the physical and chemical characteristics,as well as the activity concentrations of the soils surrounding eachtree or shrub studied. One can see that physico-chemically the

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Table 1Characteristics and activity concentrations of soils around tree and shrub individuals.

Sampling point 1 (Eucalyptus cameldulensis)

(Cytisus multiflorus)

Sampling point 2 (Quercus suber#1) Sampling point 3 (Quercus suber#2)

(Quercus ilex)

Si (ppm) 313 307 320

Al (ppm) 37 38 39

Fe (ppm) 13 11 4.4

Mn (ppm) 0.4 0.4 0.3

Mg (ppm) 4.8 8.2 1.4

Ca (ppm) 2.9 11 1.7

Na (ppm) 6.0 9.2 9.2

K (ppm) 14 13 22

Ti (ppm) 3.6 3.9 1.0

P (ppm) 0.6 0.5 0.6

pH 6.2 6.7 4.6

LOI (%) 4.2 2.8 4.2

Coarse sand [0.5–2 mm] (%) 40.3 41.4 41.7

Fine sand [0.067–0.5 mm] (%) 42.0 49.6 46.7

Silt and clay [o 0.067] (%) 17.7 9.1 12.0238U (Bq kg�1) 344714 5273 66067273230Th (Bq kg�1) 25979 3972 23387115226Ra (Bq kg�1) 30579 21678 354714210Pb (Bq kg�1) 739716 32179 22779

230 Th

Q.suber#1 Q.suber#2 Q. ilex Euca.

Act

ivity

con

cent

ratio

n (B

q·kg

-1)

0

5

10

15

20

25

30

young leavesold leaves

238U

Q.suber#1 Q.suber#2 Q. ilex Euca.

Act

ivity

con

cent

ratio

n (B

q·kg

-1)

0

20

40

60

80

100

120

140

160

young leavesold leaves

226Ra

Q.suber#1 Q.suber#2 Q. ilex Euca.

Act

ivity

con

cent

ratio

n (B

q·kg

-1)

0

20

40

60

80

100

120

140

160

young leavesold leaves

210Pb

Q.suber#1 Q.suber#2 Q. ilex Euca.

Act

ivity

con

cent

ratio

n (B

q·kg

-1)

0

20

40

60

80

100

120

140

160

180

200

young leavesold leaves

Fig. 2. 238U, 230Th, 226Ra, and 210Pb activity concentrations in leaves of trees at two stages of foliation.

P. Blanco Rodrıguez et al. / Applied Radiation and Isotopes 68 (2010) 1154–11591156

soils present a great level of similarity with the most noticeabledifference being the pH. This was slightly more acid in the soilsaround Quercus ilex and Quercus suber#2. On the contrary, the

activity concentrations of the radionuclides analysed presentimportant differences, especially for the isotopes 238U and 230Th.The activity concentrations in the soils show their relative

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locations at the mine, the soil surrounding the Quercus ilex andQuercus suber#2 being the most influenced by the installation.However the Quercus suber#1 is located in an area with especiallylow concentrations of these radionuclides. In the case of 226Ra and210Pb the differences between the three soils are less significant.

Fig. 2 shows the activity concentrations in leaves collected attwo stages of the leaves growth: young leaves, sampled in July2003, and the same leaves sampled one year later (old leaves).

U-238

Act

ivity

con

cent

ratio

n (B

q·kg

-1)

0

10

20

30

40Summer 2003 Autumn 2003Spring 2004

Th-230 Ra-226 Pb-210

Fig. 4. 238U, 230Th, 226Ra, and 210Pb activity concentrations in leaves of Cytisus

multiflorus in three seasons.

Q.suber#1

Act

ivity

con

cent

ratio

n (B

q·kg

-1)

0

2

4

6

8

1055

60

U-238Th-230Ra-226 Pb-210

Q.suber#2 Q. ilex Euca.

Fig. 3. 238U, 230Th, 226Ra, and 210Pb activity concentrations in fruits of the tree

species.

Table 2Transfer factors (TF) to fruit and leaves of the tree and shrub individuals for 238U, 230T

238U 2

Q. suber#1 Leaves 0.3270.03

Fruit (2.570.5)�10�3

Q. suber#2 Leaves (5.770.4)�10�3

Fruit (771)�10�5

Q. ilex Leaves (10.670.6)�10�3

Fruit (771)�10�5

Eucalyptus cameldulensis Leaves 0.4070.02 0

Fruit (2.270.3)�10�3

Cytisus multiflorus Leaves 0.01170.004 0

nd=not detected (the activity concentration in acorns were below 1 Bq kg�1).

For 238U, all of the tree species analysed showed an effect ofaccumulation in the leaves, with activity concentrations muchhigher in the old leaves as compared with those in the young. Thiseffect was particularly important in the case of theEucalyptus cameldulensis (14 times greater). For 230Th, theaccumulation effect was observed in the Eucalyptus cameldulensis

and Quercus suber#2, especially in the latter. However, 226Rapresented different behaviour: only the Eucalyptus cameldulensis

showed an accumulation effect, but with a low factor ofconcentration (less than two). For 210Pb, there was an accumula-tion effect in every tree except Quercus ilex, for which the activityconcentration in old leaves was less than in the young leaves(2 times less). It is interesting to note that the two individuals ofQuercus suber analysed, located in soils with very differentconcentrations of 238U and 230Th, presented patterns that werevery similar for all the radionuclides studied except 230Th. For thisradionuclide, Quercus suber#2 showed an effect of accumulationwhereas Quercus suber#1 had a significantly higher activityconcentration in the young leaves than in the old leaves.

Considering the activity concentrations of the radionuclides inthe old leaves, one can see that the highest concentrations werefor 238U and 226Ra in leaves of Eucalyptus cameldulensis (Fig. 2).The activity concentrations for 226Ra in the Eucalyptus cameldu-

lensis leaves are higher than those found in other work (Vaca et al.,2001). The 230Th presented low activity concentrations in all thespecies analysed (less than 25 Bq kg�1). Again one observes thedifferent activity concentrations of this radionuclide in the twoQuercus suber individuals, reflecting the influence of the soilactivity concentration (two orders of magnitude higher in Quercus

suber#2). Nevertheless, the great differences observed in the soilssurrounding the two individuals of Quercus suber are notproportionally reflected in the leaf concentrations. Also, theQuercus ilex, located at the same point as Quercus suber#2, didnot show especially high concentrations of 230Th (in fact, this treepresented the lowest activity concentrations). For 238U, thecomparison of the two Quercus suber individuals again reflectsthe influence of the soil activity concentration on the accumula-tion in old leaves. For this uranium isotope the effect of the soilconcentration was also observed in the Quercus ilex leafconcentrations. For the leaves of these two species of Quercus,the activity concentrations obtained for uranium and thorium aregreater than those obtained for Quercus pubescens

(Mihucz et al., 2008).Fig. 3 shows the activity concentrations in the fruits

corresponding to the selected tree species. Unfortunately, theactivity concentration of 210Pb in acorns of Quercus ilex andQuercus suber were below the minimum detectable activity (about1 Bq kg�1). The values are so low that they have no radiologicalsignificance.

The highest value of the activity concentration correspondedto 226Ra in fruits of Eucalyptus cameldulensis (about 57 Bq kg�1).

h, 226Ra, and 210Pb.

30Th 226Ra 210Pb

0.1070.01 0.1670.01 0.11970.005

(872)�10�3 0.02070.001 nd

(9.970.6)�10�3 0.07670.004 0.2270.01

(1.470.2)�10�4 0.01170.001 nd

(1.470.1)�10�3 0.04870.006 0.3470.02

(1.870.5)�10�4 (7.570.4)�10�3 nd

.03070.006 0.4470.02 0.09370.002

(2.270.3)�10�3 0.1870.01 (10.770.4)�10�3

.02370.011 0.04870.011 0.03470.014

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Ra/U soil0 1 2 3 4 5

Ra/

U fr

uits

0

10

20

30

40

50

Ra/U soil0 1 2 3 4 5

Ra/

U le

aves

0

1

2

3

4

5

r = 0.975 s = 0.88 ± 0.14

r = 0.984s = 6.2 ± 0.8

Ra/U leaves0 1 2 3 4 5

Ra/

U fr

uits

0

10

20

30

40

50

r = 0.999 s = 6.9 ± 0.2

Fig. 5. Relations between the activity ratios in soil, leaves and fruits for 238U and226Ra.

P. Blanco Rodrıguez et al. / Applied Radiation and Isotopes 68 (2010) 1154–11591158

This radionuclide also presented the highest activity concentra-tions in all three tree species. In the case of 238U, similarly to thecase of 210Pb and 226Ra, the activity concentrations in acorns ofthe different Quercus species were less than that observed in fruitsof Eucalyptus cameldulensis. This tendency was not observed for230Th, which presented very similar activity concentrations for allthe species studied (less than 0.6 Bq kg�1).

Fig. 4 shows the activity concentration of the naturalradionuclides in leaves of Cytisus multiflorus. The resultscorrespond to the three sampling campaigns performed in

summer and autumn 2003, and spring 2004. The highestactivity concentrations corresponded to 210Pb, and the lowest to238U and 230Th. Except for 238U, the rest of the radionuclidespresented a clear tendency: the highest values were observed inspring and the lowest in summer. The results for 238U in thedifferent sampling campaigns were statistically indistinguishable.

In comparison with the activity concentrations in leaves of thetrees, in general the activity concentrations found in the shrubleaves were lower. An exception was the case of 230Th, whichpresented similar activity concentrations in trees and shrub.

3.2. Transfer factors

Table 2 lists the transfer factors (TFs), defined as the ratio ofthe activity concentration in the fraction of the plant studied(leaves or fruit) to the activity concentration in the soil around thetree or the shrub studied. In the case of leaves of trees, old leaveswere considered, since they are the leaves ready to fall. For Cytisus

multiflorus, the above-ground fraction collected in the lastcampaign (spring 2004) was considered.

One can see that the TFs to fruit are in all cases lower thanthose to leaves. This result is coherent with findings of otherauthors for different types of fruits (Al-Masri et al., 2008).

The comparison of the leaf-TF values of 238U and 230Thobtained for the two individuals of Quercus suber, and taking intoaccount the results of the activity concentrations, indicates that,although the activity concentration in the soils has a certaininfluence on the activity concentration in the leaves, this relationis not linear.

For 238U, the highest leaf-TF values were obtained for Quercus

suber#1 and Eucalyptus cameldulensis, with values statisticallyindistinguishable between these two tree species, and even higherthan those obtained for herbaceous species in this same area(mean value: 0.067) (Vera Tome et al., 2003). Similar results wereobtained for the fruit-TF, where the uranium TF again was higherin Quercus suber#1 and Eucalyptus cameldulensis with valuesstatistically indistinguishable between the two.

In the case of 230Th, the highest leaf-TF values, either for leavesor fruit, were obtained for Quercus suber#1, followed byEucalyptus cameldulensis. These TF values are in the rangeobtained for herbaceous species in this same area (0.008–0.249)(Vera Tome et al., 2003).

For 226Ra, the highest values were obtained in leaves and fruitof Eucalyptus cameldulensis. These TF values are in the rangeobtained for herbaceous species in this same area (0.097–0.504),although somewhat higher than the mean value (0.17) (VeraTome et al., 2003). The rest of the species analysed had muchsmaller TF values, except in the case of the leaves of Quercus

suber#1 with values of the order of those for Eucalyptus

cameldulensis.Contrary to the behaviour observed for 238U, 230Th, and 226Ra,

the TF values of 210Pb to the leaves of Eucalyptus cameldulensis

were the lowest of all the trees and to the fruits were low orundetectable for all four trees. For this isotope, the highest TFvalues were observed in leaves of the three Quercus treesanalysed, with similar values in the three individuals and of thesame order as the highest values obtained for the otherradionuclides studied.

3.3. Activity ratios

In order to compare the behaviour of the four radionuclidesstudied in the soil–tree system, we determined the activity ratios230Th/238U, 226Ra/230Th 210Pb/226Ra, and 226Ra/238U in the threecompartments: soil, leaf, and fruit. A statistically significant

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correlation between the activity ratio in soils and in leaves orfruits would indicate that the two radionuclides involved aretransferred under the same mechanisms from soils to leaves orfruits, with the ratio determining the relative affinity for eachradionuclide.

In this sense, we found a strong correlation (Fig. 5) for the ratio226Ra/238U between leaves and soils, with r=0.975 (p=0.025).Moreover the linear fit had a slope close to 1 (s=0.8870.14), i.e.the activity ratio is almost maintained from soils to leaves. Thisresult indicates that these two radionuclides present similarbehaviour in the uptake and translocation from soil to leaves oftrees, although uranium predominates slightly, probably becausethere is more amount available in the soil derived from its greateractivity concentration.

Also, we observed a strong correlation (Fig. 5) for the ratio226Ra/238U between fruits and soils (r=0.984, p=0.016), andbetween fruits and leaves (r=0.999, p=0.001). But, in these cases,the slope of the linear fit was always greater than 1, with values of6.270.8 and 6.970.2, respectively. These results indicate that,even though the translocation to fruit processes for these twoisotopes is related (strongly correlated) the radium isotope isaccumulated in the fruit preferentially (about 6 times more).

In the case of the ratio 230Th/238U, there was no statisticalevidence relating these radionuclides in their transfer from thesoils. However, a strong correlation was found between theactivity ratio in fruit with that in leaves (r=0.962, p=0.038) with aslope greater than 1 (2.270.4). Similar results were obtained forthe ratio 226Ra/230Th, with a strong correlation between theactivity ratio in fruit with that in leaves (r=0.995, p=0.005) andwith a slope greater than 1 (1.670.1).

4. Summary

The study of the activity concentrations in tree leaves at twostages of leaf growth indicated that Eucalyptus cameldulensis

leaves show a clear effect of accumulation for all the radionuclidesselected. Moreover, the highest activity concentrations (corre-sponding to 238U and 226Ra) were found in this tree.

For all the species analysed, the activity concentrations werelower in fruits than in leaves. Especially high activity concentra-tions were found in fruits of Eucalyptus cameldulensis, except inthe case of 230Th.

Although the activity concentration in the tree leaves showed acertain influence of the soil concentration, the relation was notlinear. This is reflected in the transfer factor values (much lowerin areas with a high activity concentration in the soil).

For the isotopes 238U and 226Ra, the transfer from soil and thetranslocation process are strongly related as reflected in thestrong correlations between the activity ratio in soils with that inleaves or fruits. Although this may suggest similar processes forthe uptake of uranium and radium, the question needs moreinvestigation.

Acknowledgements

Thanks are due to the Ministerio de Educacion y Ciencia, PlanNacional de I+D+I (2004–2007) (CTM2005-02910/TECNO pro-ject) and the Fondo Social Europeo de Desarrollo Regional (FEDER)for financial support. We also acknowledge financial support fromthe Empresa Nacional de Resıduos Radiactivos (ENRESA), theSpanish National Agency for Radioactive Management (project0078000102).

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