Environmental processes affectingplant root uptake of radioactive trace elements and variability of...

Journal of

Environmental Radioactivity 58 (2002) 97112

Environmental processes aecting plant rootuptake of radioactive trace elements andvariability of transfer factor data: a review

Sabine Ehlken*,1, Gerald Kirchner

Department of Physics=FB 1, University of Bremen, Postfach 330440, D-28334 Bremen, Germany

Received 3 July 2000; received in revised form 22 September 2000; accepted 22 September 2000

Abstract

Soil-to-plant transfer factors are commonly used to estimate the food chain transfer ofradionuclides. Their denition assumes that the concentration of a radionuclide in a plant

relates linearly solely to its average concentration in the rooting zone of the soil. However, thelarge range of transfer factors reported in the literature shows that the concentration of aradionuclide in a soil is not the only factor inuencing its uptake by a plant. With emphasis onradiocesium and -strontium, this paper reviews the eects of competition with major ions

present in the soil-plant system, the eects of rhizosphere processes and soil micro-organismson bioavailability, the factors inuencing transport to and uptake by roots and the processesaecting long-term uptake rates. Attention is given to summarizing the results of recent novel

electrophysiological and genetic techniques which provide a physiologically based under-standing of the processes involved in the uptake and translocation of radiocesium and-strontium by plants. # 2001 Elsevier Science Ltd. All rights reserved.

Keywords: Root uptake; Soil-to-plant transfer factor; 137Cs; 90Sr; Heavy metals

1. Introduction

The entry of trace contaminants, which are present in the terrestrial environment,into human food chains is controlled in the long term by their uptake by plant roots.For radionuclides, it is generally assumed that the concentration of a nuclide i in a

1Present address: ZKH St.-J .uurgen-Strasse, Abt. .OOkologie, D-28205 Bremen, Germany.

*Corresponding author. Tel.: +49-421-218-3266; fax: +49-421-218-9555.

E-mail address: [email protected] (S. Ehlken).

0265-931X/01/$ - see front matter # 2001 Elsevier Science Ltd. All rights reserved.PII: S 0 2 6 5 - 9 3 1 X ( 0 1 ) 0 0 0 6 0 - 1

plant or plant part, Cpi (Bq kg

1, dry weight), is linearly related to its concentrationin soil within the rooting zone, Csi (Bq kg

1, dry weight), i.e.

Cpi TFiC

si : 1

The proportionality constant TFi in Eq. (1) which is called the soil-to-plant transferfactor (or concentration ratio) is given as

TFi activity concentration of nuclide i per kg dry plant mass

activity concentration of nuclide i in dry soil within the rooting zone:

2

Similar ratios of plant and soil concentrations were applied to characterize soil-to-plant transfer of heavy metals (Chamberlain, 1983; Gast, Jansen, Bierling, &Haanstra, 1988) and of pesticides (Trapp, Matthies, Scheunert, & Topp, 1990). TFiis an empirical quantity. The enormous number of observations which have beenaccumulated during the last decades demonstrates that, for a number of long-livedradionuclides, soil-to-plant transfer factors show variations which may exceed threeorders of magnitude (Coughtrey & Thorne, 1982; Frissel, 1992). For radiocesiumuptake from agricultural soils, transfer factors show ranges of up to three orders ofmagnitude even for individual soil-crop combinations (Nisbet & Woodman, 2000).This extreme variability indicates that a general relationship between the soil andplant concentrations of a radionuclide does not exist, in contrast to the basicassumption of Eq. (1). This conclusion is corroborated by eld experiments whichshowed almost no correlation between soil and plant concentrations of radioactivecesium (Wirth et al., 1994) and of heavy metals (Zhang, Rahman, Vance, & Munn,1995). The validity of the transfer factor concept was also questioned by McGee,Johanson, Keatinge, Synnott, and Colgan (1996) who found that 137Cs concentra-tions of Juncus squarrosus and Calluna vulgaris taken from a site in Ireland, and ofVaccinium myrtillus and Vaccinium vitis-idaea taken from Sweden, were not relatedto soil concentrations of 137Cs.The reason for the high variability of soil-to-plant transfer factors is obvious. This

macroscopic parameter integrates a number of soil chemical, soil biological,hydrological, physical and plant physiological processes, each of which shows itsown variability and in addition may be inuenced by external factors such as climateand human agricultural practices. Evaluation of the inuence of these processes hasbeen attempted by statistical inference from soil-to-plant transfer factor data bases(Van Bergeijk, Noordijk, Lembrechts, & Frissel, 1992; Sheppard & Evenden, 1997;Nisbet & Woodman, 2000) but with moderate success. Generally, a minor part of thetransfer factor variability could be explained by the analyses. Moreover, the resultsof the statistical analyses do not seem to be unequivocal. For example, Van Bergeijket al. (1992) established an association of transfer factors of radiocesium and-strontium with soil organic matter, an association which was absent in the dataanalyzed by Nisbet and Woodman (2000). A potential explanation may be that thesestatistical analyses suer from general limitations. Since the data bases werecompiled from individual observations made by dierent researchers and eachinvolving a large number of parameters, it is unlikely that they altogether represent a

S. Ehlken, G. Kirchner / J. Environ. Radioactivity 58 (2002) 9711298

statistically well-dened sample of the underlying population. Biased samples,however, may seriously aect any statistical inference and may give rise to spuriousresults. Another limitation may be provided by the well known fact that even astatistically valid correlation of soil-to-plant transfer factors with a soil- or plant-specic parameter does not necessarily reect a cause-eect relationship or provideinsight into the mechanisms governing plant uptake.The primary application of soil-to-plant transfer factors is in food chain models

used for calculating radiological consequences from routine or accidental release ofradioactive substances into the environment. These models usually are designed togive conservative assessments (Homan, Bergstr .oom, Gyllander, & Wilkens, 1984;Peterson, 1995). For this purpose, the use of parameters which are as simple aspossible is desirable to keep model complexity down. The wealth of soil-to-planttransfer factor data now available at least for temperate environments seems to beadequate to derive probability distributions from which representative values for usewith screening models can be derived (IAEA, 1994; Sheppard & Evenden, 1997;Nisbet & Woodman, 2000).In radioecological research, on the other hand, interest shifts more and more to

elucidating the chemical, biological and physical mechanisms governing the rootuptake and translocation of radionuclides from soils. The best example may be thepioneering work of Cremers and coworkers (Cremers, Elsen, De Preter, & Maes,1988; De Preter, 1990; Valcke & Cremers, 1994) on the chemistry of radiocesium insoils. Recent understanding of processes involved in soilplant transfer oers theperspective for developing mechanistic models but such models, although deemedrequired (Nisbet & Woodman, 2000), are not yet available. Focusing on radiocesiumand -strontium, this paper intends to summarize present knowledge on processeswhich inuence root uptake of radionuclides (as well as of other trace metals) byplants and to identify areas where our present understanding is still limited.Although important, species variations in soilplant transfer are not discussed, sincecomprehensive compilations and reviews are available (e.g. Andersen, 1967;Coughtrey & Thorne, 1982; Frissel, 1992).

2. Competing ions

Eventually the most important conceptual limitation of the transfer factor approach isthat it does not take into account competition between ions. Soil-to-plant transferfactors are most often measured for trace substances whose behavior in the soilplantsystem largely depends on the concentrations of macro-nutrients present. For example,an activity concentration in a soil solution of 1 Bq=l of 90Sr or 137Cs corresponds to ca.2 1015 M=l, whereas median concentrations of Ca, K and Mg in soil solution are inthe order of 1 mM=l (Robson & Pitman, 1983). A number of substances naturallypresent in soils have been found to inuence the uptake of radionuclides and heavymetals by plants, though not always benecially (Wallace, 1989; Desmet, 1991; Lorenz,Hamon, McGrath, Holm, & Christensen, 1994a, b). For radioactive cesium andstrontium, these competitive eects form the basis of countermeasures at the soilplant

S. Ehlken, G. Kirchner / J. Environ. Radioactivity 58 (2002) 97112 99

level after a nuclear accident (Howard & Desmet, 1993). As discussed in detail in thefollowing paragraphs, the concentration of a trace substance accumulating in plantsmay not primarily depend on its absolute concentration in the soilplant system but onthe concentration ratio to other micro- and macro-nutrients.

3. Interactions within the soil

3.1. The concept of bioavailability

As is well known, a major fraction of a trace element present in the rooting zonemay be xed to soil constituents. This has led to the development of the concept ofbioavailability of trace substances in soil (e.g. Desmet, van Loon, & Howard 1991;Schnoor, 1996). Modication of Eq. (2) by replacing the total soil concentration of atrace substance by its bioavailable fraction should considerably reduce variability. Itshould be noted, however, that this concept does not account for the eects ofcompetition of the substance studied with other trace or major elements.Procedures which are simple and reliable unfortunately do not seem to be available

for determining the bioavailable fractions of radionuclides in soils. Commonly,sequential extraction techniques are applied which use a sequence of progressivelyaggressive reagents to selectively leach the fractions of trace substances bound tospecic soil components (Pickering, 1981; Beckett, 1989; Riise, Bjornstad, Lien,Oughton, & Salbu, 1990; Quevauviller, 1996). Both selectivity and reproducibility ofthe extraction steps, however, have been debated (Kheboian & Bauer, 1987; Martin,Nirel, & Thomas, 1987; Beckett, 1989; Nirel & Morel, 1990; Xiao-Quan & Bin, 1993;Clark, Johnson, Malek, Serkiz, & Hinton, 1996; Ho & Evans, 2000). Specically, arelationship between the operationally-dened bioavailable fraction determined bythese techniques and plant root uptake remains to be established.

3.2. Soil=soil solution interactions

The concentration of an ion in solution in most soils is determined by cationexchange reactions with the soil matrix which by their nature are competitive butother processes, e.g. co-precipitation, also depend on the concentrations ofcompeting substances in solution. Sorption of radiostrontium in most soils isdominated by reversible exchange with major cations (mainly Ca2) present on theexchanger. Strontium is exchanged in preference to Ca in minerals but the preferencereverses in organic matter (Valcke, 1993). The soil chemistry of cesium is morecomplex. As elucidated by Cremers and coworkers (Cremers et al., 1988; De Preter,1990; Valcke & Cremers, 1994), the fate of radiocesium in soils is dominated by ionexchange to a small number of sites located in weathered mica which are accessibleonly to poorly hydrated cations and show high selectivity for Cs over K and NH4 .In addition, there is a slow almost irreversible sorption process of radiocesium toclay minerals (Comans & Hockley, 1992).Recent studies (Konoplev et al., 1997; Roca et al., 1997; Kirchner & Ehlken, 1999;

Sauras Yera et al., 1999) have shown that taking into account these soil chemical


processes for a variety of soils considerably improves predictions of soil-to-planttransfer of radiostrontium and -cesium. They also demonstrated that the traditionaltransfer factor denition of Eq. (2) can be easily modied to include the soilchemistry of both radioelements.

3.3. Rhizosphere eects

A potential limitation of the above approaches to determining the plant-availablefraction of a radionuclide or heavy metal is that they relate to the chemistry of thetrace substance in the bulk soil but ignore rhizosphere eects on its availability.Roots excrete a variety of substances including organic acids, sugars, amino acids,H and HCO3 (Russell, 1973; Marschner, Godbold, & Jentschke, 1986) and,thereby, create micro-environments with availabilities which may greatly dier fromthose in the bulk soil (Merckx, Sinnaeve, Van Ginkel, & Cremers, 1983; Lorenz,Hamon, & McGrath, 1994b; Courchesne & Gobran, 1997). Organic root exudatesincrease the solubility of metals by forming soluble organometallic complexes(Merckx et al., 1983; Mench, Morel, Guckert, & Guillet, 1988; Treeby, Marschner, &R .oomheld, 1989; Naidu & Harter, 1998), although the eectiveness of this process inmobilizing nutrients is still a matter of debate (Jones & Brassington, 1998). Byrelease of H or HCO3 , roots actively inuence the pH in their immediateenvironment, thereby increasing the availability of potassium and phosphorus,respectively (Jungk & Claassen, 1986). In the case of potassium, root-inducedmobilization of non-exchangeable K xed in clay mineral interlayers maysignicantly contribute to the potassium nutrition of plants (Jungk & Claassen,1986; Mitsios & Rowell, 1987). As a consequence of the K removal, clay minerals aretransformed (Tributh, Boguslawski, Lieres, Steens, & Mengel, 1987; Hinsinger &Jaillard, 1993; Courchesne & Gobran, 1997). The impact of these processes onradiocesium seems to be complex. Root-induced degradation of vermiculitesremobilizes xed cesium (Thiry, 1997; Delvaux, Kruyts, & Cremers, 2000) but alsoincreases Cs adsorption on the minerals (Guivarch, Hinsinger, & Staunton, 1999).Compared to the bulk soil the rhizosphere is populated by large concentrations of

micro-organisms (Russell, 1973) which mainly consist of bacteria and mycorrhizalfungi (Richards, 1987). The principal sources of nutrition of rhizosphere bacteria areorganic root exudates and moribund root tissues (Russell, 1973). Incorporation intothe bacterial biomass reduces the availability of ions at low solution concentrationsto plants (Barber, 1968) but there is also evidence that soil bacteria can mobilizenutrients and non-nutrient trace metals by enhanced production of CO2 in therhizosphere (Richards, 1987), by release of chelating ligands (Treeby et al., 1989), bybreaking down complexes (Barber & Lee, 1974), by degradation of minerals (Barber,1968; Richards, 1987; Zezina, Savchuk, Kutlakhmedov, Serdiuk, & Izzheurova,1992) and by decomposition of organic matter (Tegen, D .oorr, & M .uunnich, 1991).Data on the accumulation of radioisotopes by soil fungi are rare but the potential ofthe soil fungal biomass to immobilize a signicant fraction of the radiocesiumpresent in upland organic and forest soils has been demonstrated (Clint, Dighton, &Rees, 1991; Dighton, Clint, & Poskitt, 1991). Recently, Nikolova, Johanson, and


Clegg (2000) also showed that in forest soils a considerable fraction of theradiocesium may be present within the fungal component of the soils.Taken together, the combined eects of roots and rhizosphere organisms in a

small volume of soil create bioavailabilities which may be completely dierent tothose of the bulk soil. For radionuclides, present knowledge of the importance ofthese eects still seems to be inadequate to enable quantication.

4. Transport to roots

Solutes are transported to plant roots by mass ow and diusion (Barber, 1962).Mass ow occurs with the convective ow of water which is created by root wateruptake in response to transpiration. If, however, root uptake rates of a solute exceedmass ow rates, depletion of the solute at the rootsoil interface creates aconcentration gradient which initiates additional diusional transport of the solutetowards the roots. As a consequence, a depletion zone around the absorbing rootdevelops, which in the long term reduces uptake rates of the solute (Nye & Tinker,1977). For potassium it is assumed that both the plant-induced depletion ofexchangeable K and the excretion of H discussed previously contribute to therelease of non-exchangeable K and Cs from interlayer positions of clay minerals(Tributh et al., 1987; Hinsinger & Jaillard, 1993; Thiry, 1997). It follows thatdepletion of a nutrient within the rhizosphere may aect the quantities of thenutrient and trace substances taken up by a plant. This eect may be of majorimportance in soils which are poor in nutrients (Delvaux et al., 2000).Variations of soil moisture inuence solute transport to roots in a complex way,

since a reduction decreases both diusion and mass ow, but increases concentra-tions of exchangeable cations in soil solution (Nye & Tinker, 1977). In short-termlaboratory experiments, in which solute transport was dominated by diusion, areduction of uptake with decreasing water content was observed (Nye & Tinker,1977), while uptake increased when diusional transport was low (Shalhevet, 1973).Under natural conditions, the inuence of moisture changes on plant uptakeprocesses may be even more complex, since variations in water content also inuencethe physiology and morphology of root systems (Russell, 1973; Smucker & Aiken,1992). In a three-year eld study, Ehlken & Kirchner (1996) observed thatconcentrations of 90Sr and 137Cs in pasture vegetation growing on dierent soiltypes were negatively correlated with soil moisture. They interpreted this nding asthat under eld conditions the increase of solute concentrations with decreasing soilmoisture is of primary importance for the root uptake rates of both radionuclides.

5. Root uptake and translocation

5.1. Cellular transport mechanisms

Minerals are taken up from the soil solution and transported into the xylem inionic form. Two pathways were identied (Clarkson, 1988). Ions may move in theapoplasm of the root tissue to the endodermis where they enter the symplasm, since


the hydrophobic Casparian band prevents ions from directly entering the stele. Thispathway dominates for Ca2. For most ions, transport in the symplasm is moreimportant: ions cross the plasma membrane of the epidermal or cortical cells andmove into the cytoplasma through the plasmadesmata connecting adjoining cells,thus crossing the endodermis, to the xylem parenchyma cells where they are released(again across a plasma membrane) into the apoplasm of the xylem vessel.Mechanisms involved in the passage of ions through the plasma membranes ofcortical and xylem parenchyma cells include ion pumps (Cowan, Clarkson, & Hall,1993; Michelet & Boutry, 1995), carriers (Tanner & Caspari, 1996) and ion channels(Maathuis, Ichida, Sanders, & Schroeder, 1997; White, 1997).Competitive and inhibitory interactions play a major role in root uptake and

translocation of alkaline (Epstein & Hagen, 1952) and alkaline-earth (Epstein &Leggett, 1954) elements and also of heavy metals with essential ions of similar ionicradii (Kawasaki & Moritsugu, 1987). Root uptake of potassium shows twocomponents exhibiting MichaelisMenten kinetics and operating at low and high(i.e., above ca. 1 mM) K concentrations, respectively (Epstein, Rains, & Elzam, 1963).Focusing on the Cs : K competition, these results were conrmed by Shaw and Bell(1991) and by Smolders, Kiebooms, Buysse, and Merckx (1996); Smolders, Sweeck,Merckx, and Cremers (1997a) and Smolders, Van den Brande, and Merckx (1997b).Using novel electrophysiological and molecular techniques, it has been shown recentlythat K transport across the plasma membranes of plant root cells in the high-anity(low concentration) range is mediated by carriers (Schachtman & Schroeder, 1994;Rubio, Gassmann, & Schroeder, 1995), whereas transport proceeds via K-channels(Maathuis & Sanders, 1995) at high potassium concentrations (the low-anity range).Selectivity sequences for alkaline ions of the two plasma membrane transportmechanisms are related to selectivities which have been observed for intact roots innutrient solution experiments (Maathuis & Sanders, 1995). Moreover, parameter valuesof the two MichaelisMenten kinetic components measured in the soil solution studiesmentioned above are in good agreement with those derived from electrophysiologicalexperiments studying K plasma membrane uptake systems of plant root cells(Maathuis & Sanders, 1996). For a number of divalent cations including both macro-and micro-nutrients and the non-essential cations of Sr2, Ba2, Co2, Ni2, Cu2 andCd2, transport across plasma membranes of plant root cells is mediated by so-calledcalcium channels (Rivetta, Negrini, Lucchini, & Cocucci, 1997; White, 1998), which arealso permeable to monovalent cations (White, 1998).These recent ndings not only have resulted in a detailed understanding of the

physiological processes involved in ion uptake by plant roots, but they also oer afascinating perspective to interpret or even to predict empirical relationships}e.g., asused by Smolders et al. (1997b), to take 137Cs : K competition into account}fromour present knowledge of physiological mechanisms involved in plant root uptake.

5.2. Impact of mycorrhizae

The roots of most plants are associated with mycorrhizal fungi. One of the majorbenets of this symbiosis for the host plant is that a mycorrhizal infection often


enhances nutrient acquisition. Mechanisms responsible include an increase of thesurface area accessible to soil, due to the external hyphae of the fungi, changes inmorphology and longevity of infected roots and modications of the plasmamembranes of cortical cells surrounding intercellular hyphae (Richards, 1987;Bonfante-Fasolo & Scannerini, 1992; Benabdellah, Azc !oon-Aguilar, & Ferrol,2000). However, this response is not universal: Kothari, Marschner, & R .oomheld(1990) showed that the eect of mycorrhizae on root morphology and onrhizosphere microorganisms may reduce uptake of some nutrients. In addition,mycorrhizae aect acquisition and translocation of nutrients and trace substancesby storage or immobilization in the fungal biomass (Richards, 1987; Turnau,Kottke, & Oberwinkler, 1993; Marschner, R .oomheld, Horst, & Martin, 1996).Variability in the importance of these various mechanisms may explain the factthat the impact of mycorrhizae on the plant root absorption of heavy metals(Killham & Firestone, 1983; Dixon & Buschena, 1988; B .uucking & Heyser, 1994;Weissenhorn, Leyval, Belgy, & Berthelin, 1995) and of radioactive trace substances(Haselwandter & Berreck, 1994; Brunner, Frey, & Riesen, 1996; Entry, Watrud, &Reeves, 1999) cannot be generalized. Since plantmycorrhiza associations arecommon rather than an exception, their eect on the plant availabilities of nutrientsand trace substances should be taken into account in interpreting root uptakestudies.

6. Time trends

Transfer factors of radiocesium and -strontium in lysimeter and eld experimentswere frequently observed to decrease slowly with time for some years aftercontamination of the soils (Squire & Middleton, 1966; Noordijk, van Bergeijk,Lembrechts, & Frissel, 1992; Nisbet & Shaw, 1994). Commonly this timedependency is attributed to a slow irreversible xation of the radionuclides to thesoil matrix (IAEA, 1994). Following the work of Cremers and coworkers (Cremers,Elsen, De Preter, & Maes, 1988; De Preter, 1990), a long-term decrease inradiocesium uptake by plants most often is attributed to its sorption and xation toclay minerals (e.g. Shand, Cheshire, Smith, Vidal, & Rauret, 1994; Hird, Rimmer, &Livens, 1996).In the context of the present paper, we would like to point out that, as a

consequence of the simple denition of Eq. (2), time trends apparent in transferfactor data may arise from the redistribution of the radionuclide within the rootingzone (Fig. 1). For radiocesium, this process obviously will become important mainlyin organic soils for which xation by clay minerals does not dominate. As discussedelsewhere (Ehlken & Kirchner, 1996), seemingly conicting results on long-termtrends of transfer factors can be consistently interpreted by redistribution ofradionuclides within the rooting zone. Using a simplied model, it was shown thatthe higher transfer factor of Chernobyl than of weapons fallout cesium and its timetrend, which were observed for pasture vegetation on a peaty soil, could be explainedby the diering depth distributions of the two Cs fractions and their evolution with


time (Ehlken & Kirchner, 1996). For deep rooting plants, e.g. trees, theredistribution of the contaminant within the soil prole may even cause an increaseof the transfer factors with time (Belli et al., 1996).The inuence of the non-uniform root densities and concentrations of a trace

substance on root uptake is illustrated in Fig. 2. It shows predictions of theredistribution of 137Cs activity in a peat soil within 30 years after deposition and ofthe resulting time-dependent root uptake by pasture vegetation. Apparently, rootuptake decreases drastically within three decades as a consequence of the cesiumtransport down the soil column. The inuence of the decreasing root density on 137Csroot uptake is also demonstrated in Fig. 2. During the whole time period considered,the majority of 137Cs taken up by the plants originates from the upper 2:5 cm,although after only 3.5 years the majority of the activity has already moved togreater depths. This illustrates that by simply using the average concentration of acontaminant within the rooting zone}which is the basis of the transfer factorconcept, Eq. (2)}not only is a bias introduced (since uptake occurs mainly frommuch smaller soil layers) but also information on the long-term dynamics of rootuptake processes is lost. This conclusion applies primarily to uncultivated soils but,in ploughed soils, depth distributions of radionuclides may also be highly non-uniform as documented by Meisel, Gerzabek, and M .uuller (1991) for Chernobylfallout radionuclides.

Fig. 1. Redistribution of a trace substance within the rooting zone (left: typical concentration-versus-

depth curve for two dierent times, t2 > t1, after a single deposition event) leads to lower uptake rates byplants due to the decrease of root densities with depth (right).


7. Conclusions

The behavior of alkaline and alkaline-earth trace elements, and also of heavymetals, in the soilplant system is dominated by competitive and inhibitoryinteractions with the major ions present. These processes control the concentrationsof trace ions present in soil solution and the cellular plasma membrane transportresponsible for root uptake and translocations of those trace elements. Forradiocesium and -strontium, the mechanisms acting at soil=solution interfaces andplasma membranes of root cells have been elucidated during the last decade.Modications to the traditional transfer factor approach which take into account

Fig. 2. Prediction of time-dependent Cs migration and of root uptake rates using model and parameter

values from Ehlken and Kirchner (1996). Top: Fractions of the 137Cs activity deposited at t 0 which arepresent in the rooting zone (010 cm) and in the upper (02:5 cm) and lower (2.510 cm) part of it.Bottom: Fractional total 137Cs root uptake and contributions of the upper and lower part of the rooting

zone. 100% corresponds to root uptake 1 year after deposition.


many of these recent ndings have been proposed and successfully tested. Theseapproaches should be extended to fully include the present information on thephysiological basis of ionic competition during root uptake and should replace thetraditional transfer factor of Eq. (2) for quantifying experimental data on the soil-to-plant transfer of both radioelements.Present knowledge seems to be too limited to enable quantication of the eect of

interactions of plant roots, microbial communities and soils within the rhizosphereon plant availabilities of trace substances. However, recent ndings indicate thatthese processes may play a major role in semi-natural ecosystems. We therefore feelthat future research eorts should be directed to enhance understanding and allowquantication of the eect of these processes on soil-to-plant transfer.

Acknowledgements

We would like to thank W. Heyser, Physiologische Panzenanatomie, Universityof Bremen, for fruitful discussions.

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