Willey, N. J. (2013) Soil to plant transfer of radionuclides: Predictingthe fate of multiple radioisotopes in plants. Journal of Environmen-

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Soil to plant transfer of radionuclides: predicting the fate of multipleradioisotopes in plants

Neil J. WilleyCentre for Research in Bioscience, University of the West of England, Bristol BS16 1QY, UK

a r t i c l e i n f o

Article history:Received 19 November 2012Received in revised form31 July 2013Accepted 31 July 2013Available online xxx

Keywords:PhylogenyStrontiumRadiumStoichiometryIonomics

a b s t r a c t

Predicting soil-to-plant transfer of radionuclides is restricted by the range of species for which con-centration ratios (CRs) have been measured. Here the radioecological utility of meta-analyses ofphylogenetic effects on alkali earth metals will be explored for applications such as ‘gap-filling’ of CRs,the identification of sentinel biomonitor plants and the selection of taxa for phytoremediation ofradionuclide contaminated soils. REML modelling of extensive CR/concentration datasets shows that theconcentrations in plants of Ca, Mg and Sr are significantly influenced by phylogeny. Phylogenetic effectsof these elements are shown here to be similar. Ratios of Ca/Mg and Ca/Sr are known to be quite stable inplants so, assuming that Sr/Ra ratios are stable, phylogenetic effects and estimated mean CRs are used topredict Ra CRs for groups of plants with few measured data. Overall, there are well quantified plantvariables that could contribute significantly to improving predictions of the fate radioisotopes in the soil-plant system.

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1. Introduction

Predicting the soil-to-plant transfer of radionuclides is impor-tant to many assessments of radionuclide fate in terrestrial eco-systems. Soil availability of radionuclides contributes significantlyto the magnitude of their transfer to plants but there are manyplant factors, from molecular to ecological scale, that also help todetermine transfer. For most radionuclides these plant factors are,in general, less well understood than the factors controlling avail-ability from soil. Understanding the influence of plant factors onsoil-to-plant transfer of radionuclides might help the developmentof techniques that can predict radionuclide transfer to species forwhich there are no measured transfer factors at present (Willey,2010). It might also help clarify the effects of soil and other envi-ronmental variables on transfer by providing an explanation for asignificant proportion of the variation in soil-to-plant transfer ofradionuclides.

Previous research has shown that there are phylogenetic in-fluences on the transfer of radionuclides from soils to plants (e.g.Willey et al., 2010; Willey et al., 2005). Phylogenetics studies theevolutionary history of groups of organisms. The rapid increase inboth molecular data and the power of computational techniqueshas enabled new phylogenies to be described for many groups of

organisms including plants. These phylogenies are very useful incomparative biological studies, i.e. in attempts to gain insight aboutfundamental biological characteristics by comparing them indifferent taxonomic groups. A molecular-based plant phylogeny foruse in comparative biology was first proposed by Soltis et al. (1999).This has continued to be updated by the Angiosperm PhylogenyGroup who have constructed one of the most widely acceptedphylogenies of flowering plants (Bremer et al., 2003, 2009). Thesenew phylogenies, and taxonomies derived from them, now providea framework for many comparative analyses in plant biology. Onesuch analysis is that of element concentrations in plants, includingelements with radioisotopes.

Previous investigations have suggested that there are phyloge-netic effects in plant uptake from soil of several heavy metals(Broadley et al., 2001), numerous elements (Watanabe et al., 2007)andmany radionuclides including those of Cs (Broadley et al., 1999;Willey et al., 2005), Cl (Willey and Fawcett, 2005), Sr (Willey andFawcett, 2006a), Ru (Willey and Fawcett, 2006b), S (Willey andWilkins, 2006), Co (Willey and Wilkins, 2008) and Tc (Willeyet al., 2010). Analyses of phylogenetic and taxonomic effectsdepend on large datasets of element concentrations in plants.Particularly for radionuclides there are few datasets that providecomparative species data, i.e. data from species studied under thesame conditions, for more than 5 or 6 species. In all the afore-mentioned analyses of taxonomic effects residual maximum like-lihood (REML) modelling was used to construct datasets ofE-mail address: Neil.Willey@uwe.ac.uk.

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Please cite this article in press as: Willey, N.J., Soil to plant transfer of radionuclides: predicting the fate of multiple radioisotopes in plants,Journal of Environmental Radioactivity (2013), http://dx.doi.org/10.1016/j.jenvrad.2013.07.023

estimated relative concentrations in many species (Fig. 1). Theiterative REML procedure can minimize the influence of one factoron variation in measured values in order to reveal the influence ofanother factor. In the procedure these are termed the ‘random’ and‘fixed’ factors respectively. In the aforementioned analyses therandom factor was ‘study’ and the fixed factor was’ species’. Clas-sifying data by ‘study’ included all the soil and environmentalvariables that might have contributed to determining the elementconcentration in plants. REML modelling across several datasetsrequires that they have values for the fixed factor in common. Inmost instances data for plant concentrations or activities wasgenerated to overlap with species data from the literature. REMLanalyses of these datasets were used to minimize the influence ofsoil and environmental variables and thus provide estimates ofrelative values in many species. Full details of the analysis areprovided in Willey (2010).

Data analysed for phylogenetic effects in element concentra-tions in plants has focused on concentrations in green shoots.Although there are many plants with significant woody parts andthe element concentrations in roots also contribute to ecosystemflows of elements, green shoots often have the most dynamic rolein the flows of nutrients and elemental contaminants in ecosys-tems. Many radionuclides and elements have been shown sepa-rately to have low uptake by monocotyledonous plants ascompared to eudicot plants. For some elements there are signifi-cant differences between the commelinid and non-commelinidmonocot groups (Broadley et al., 2003). For some elements thereare significant differences between the Asterid and Rosid groupsbut for several elements with important radionuclides including Cs,Co, Sr and Tc, plants on the Caryophyllid clade have the highestrelative activities (Willey et al., 2005; Willey and Fawcett, 2006a, b;Willey and Wilkins, 2008). Although a proportion of the differencebetween concentrations of elements in plants is related to phy-logeny, its contribution to these differences is not the same fordifferent elements. For alkaline earth metals like Ca and Mg theproportion of the differences between species related to phylogenyis in excess of 60% (Broadley et al., 2003), whereas for some metalsless than 20% is related to phylogeny (Broadley et al., 2001). It is alsopossible that there is an interaction between environmental vari-ables and phylogenetically constrained differences, perhaps mostobviously with differences in the concentrations of elements thatplants are exposed to. This was recently tested in herbage from the

Park Grass Experiment at Rothamsted UK in which hay meadowshave been exposed to different fertiliser regimes for well over acentury. For those species that inhabited all of the great variety ofmeadows produced by differing fertiliser regimes, principle com-ponents analysis for their concentrations of 17 elements showedthat plant family explained a significant proportion of differences(White et al., 2012). Plants ionomes, i.e. their elemental concen-trations, are an increasingly important area of study for under-standing the flows of nutrients in agricultural and naturalecosystems. The evidence that plant ionomes are, at least in sig-nificant part, constrained phylogenetically is increasing, suggestingthat they have predictable biodiversity (Willey, 2012).

Fundamental understanding of the biodiversity of plant ionomesmight be very useful for predicting the fate of radionuclides. For thevast majority of plant species there are no measurements of con-centration ratios (CRs). Databases of CRs for major crop plants areextensive and thus provide, formajor soil types at least, quite robustestimates of the partitioning of important radionuclides betweensoil and plant. Data is, however, much less extensive for the manyminor crop plants that are often of great significance to criticalgroups. For almost all wild plants, which have to be demonstrablyprotected from the effects of radioactive contamination in anincreasing number of nations, CRs are non-existent. Methods thatcan predict CRs in any plant might, therefore, make a significantcontribution to radiological protection. In addition, species selectioncan be very important in environmental monitoring programmesand in phytoremediation schemese both of whichmight be guidedby the phylogenetic constraints on transfer. Further, phylogeneticconstraints are really a reminder that there is no a priori reasonwhyspecies should be thought of as the origin of difference in CR e thespecies is a reproductive unit and there is no particular reason tothink that fundamental ionomic differences vary just at the specieslevel.Here I report an analysis for somealkali earthmetals, includingSr, which reveals theyall have quite similar phylogenetic constraintson their transfer. I suggest that for alkali earthmetals at least generalpredictions of the fate radionuclides in the soil-plant system for awide variety of plant species can be made using recent plant tax-onomies and stoichiometric ratios.

2. Methods

Datasets were derived from previous publications that had usedREML modelling to compile estimates of relative concentrations ofCa, Mg and Sr (Broadley et al., 2003, 2004; Willey and Fawcett,2006a). Before REML modelling raw concentrations or CRs wereloge transformed. This provided data that was normally distributedformodelling in the original analyses. For analyses reportedhere theREML-estimated relative species means of loge transformed datawere selected because they were approximately normally distrib-uted rather than the exponents of the transformed means which,although theyconvert data back to scales relevant to concentrations,are approximately loge-normally distributed. Data for all the speciesreported in Broadley et al. (2003, 2004) for Ca and Mg, and for Sr inWilley and Fawcett (2006a) were included in analysis.

The estimated relative mean concentrations of Ca, Mg and Srwere standardized to give a mean of zero and a standard error of 1.Running means for n ¼ 10 were then calculated. Transformedmeans were then plotted in the order of the taxonomies used in theoriginal publications that were based on Angiosperm PhylogenyGroup I phylogeny (Soltis et al., 1999). The data for Ca, Mg and Sreach included a large dataset generated under a single set of con-ditions in the greenhouse plus a compilation of numerous literaturereports of CRs. The datasets generated in the greenhouse were usedto link literature studies and provide phylogenetic spread. In totalfor Ca n ¼ 206 species, Mg n ¼ 117, and for Sr n ¼ 155. There was

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Fig. 1. An illustration of the REML modelling technique. Three different datasets ofconcentration ratios (open symbols) have, overall, different means because of differ-ences in the environment that the plants grew in. If there are species in commonbetween datasets, perhaps because they overlap or because datasets can be producedthat link them, the REML procedure can minimise differences due to, for example soiltype, and make a prediction (closed symbols) for the relative CRs for all the species.

N.J. Willey / Journal of Environmental Radioactivity xxx (2013) 1e42

Please cite this article in press as: Willey, N.J., Soil to plant transfer of radionuclides: predicting the fate of multiple radioisotopes in plants,Journal of Environmental Radioactivity (2013), http://dx.doi.org/10.1016/j.jenvrad.2013.07.023

data for more than one element for many species with in total 272species being represented.

3. Results

The significant phylogenetic effects on the relative concentra-tions of Ca, Mg and Sr have, when standardised, clear similarities(Fig. 2). Much of the data for the individual elements is for differentspecies so a direct correlation of values is not possible. However, forthese alkali earth metals there is a clear indication of relatively lowuptake in the monocot clades of plants as defined by the Angio-sperm Phylogeny Group (APG). The data suggest that this is partic-ularly the case in the Commelinid monocots that have the higherspecies numbers. For Mg and Sr the Caryophyllid clades have thehighest relative concentrations (Broadley et al., 2003, 2004; Willeyand Fawcett, 2006a). For Mg this is a particularly significantfeature. The Rosid clades have higher relative concentrations thanthemonocot clades and lower concentrations than the Caryophyllidclades. For Sr and Mg this is a product of relative means that arearound or just below average. There is an indication that the Asteridclades have slightly higher concentrations than the Rosid clades.

For several soil types and crops the IAEA recommended CR for Sris about 0.5. For the same soil types and crops the CRs for radiumare significantly lower. Assuming that Ra will have a similarphylogenetic signal to other alkali earth metals and multiplyingthrough by, for example, 0.025, Fig. 3 illustrates what the CRs forradioisotopes of Ra in groups of plants might be. Clearly the valuesin Fig. 3 would need testing but this might be very well worthwhilebecause if the phylogenetic signals are maintained across the alkaliearth metals and stoichiometric ratios are too e as seems to be thecase for Ca, Mg and Ra e then it might be possible to make usefulgeneral predictions of the uptake of radionuclides from a knowl-edge of phylogenetic effects and stoichiometry.

4. Discussion

There is emerging evidence that the concentration of many el-ements in plants is influenced by phylogeny (White et al., 2012).When such large datasets are needed to not only establish theexistence of phylogenetic effects but also to investigate themfurther there are some clear potential limitations. First, even withover 270 species only a small proportion of flowering plants are

represented in the data. At higher taxonomic levels this number ofspecies can provide a representative sample but at lower taxonomiclevels comparisons can become less statistically meaningful. Thus,although there are effects reported individually at lower taxonomiclevels for Ca, Mg and Sr, here only higher taxonomic levels havebeen compared as they explain most of the effect and have goodreplication. It is possible that statistical interactions betweendifferent environmental conditions can affect the relative meanconcentrations in different species, i.e. the order of concentrationsin different species might change in different environments. Thiswould make the detection of phylogenetic effects more difficultstatistically but the phylogenetic signal for Sr (Fig. 2), with muchdata generated under different conditions to those of Ca and Mg, issimilar to those for Ca and Mg. The similar conditions under whicha significant proportion of the Ca and Mg data were collected hasproduced a similar signal to the compilation of data from differentenvironmental conditions for Sr, indicating that interaction withenvironment has relatively little effect on the rank order of con-centrations in different plants. So, despite the potential limitationsof the analysis that might be produced by statistical interactions,Fig. 2 indicates that there is phylogenetic influence on the fate ofalkali earth metals in the soil-plant system.

In plants Ca is primarily important in the cell wall, and at verylow concentrations in cell signalling in the cytosol, whereas theprimary role of Mg is in the chlorophyll molecule. There is muchevidence that plants do not distinguish significantly between Caand Sr during uptake and metabolism. Monocotyledonous plantshave characteristic morphologies and cell walls. The comparisonreported here emphasises that the monocots and perhaps theCommelinids in particular have the lowest concentrations of alkaliearth metals in their shoots. The shoots of, for example, grasses inthis group are mineralogically distinct (White et al., 2012), whichaccords with their having different concentrations of alkali earthmetals to most other plant groups. This might be very useful inradioecology because both 90Sr and 226Ra are important radionu-clides when they occur in the environment and the analysis re-ported here suggests that in general monocots and especiallyCommelinid monocots accumulate them to low concentrations ingreen shoots compared to other plants. The Caryophyllid clades arealso mineralogically distinct. The Caryophyllids include a notablyhigh proportion of halophytic species that frequently accumulateNa and Mg to high concentrations (Flowers and Colmer, 2008). The

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Fig. 2. Estimates of relative mean concentrations of Ca from Broadley et al. (2003), Mgfrom Broadley et al. (2004) and Sr from Willey and Fawcett (2006a) standardised andplotted as running means according to the Angiosperm Phylogeny Group II phylogeny(Bremer et al., 2003).

Fig. 3. Possible CRs for Ra based on an overall geometric means of 0.025 and dividedup according to the phylogenetic effects on Sr and assuming a constant stoichiometricratio of 0.5:0.025 between Sr and Ra. Geomeans plus and minus 95% CIs based on thosecalculated for Sr in each of these plant groups.

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analysis reported here suggests that the Caryophyllids, in general,accumulate the highest concentrations of alkali earth metals of anyplants. This might be particularly significant for the transfer of 90Srand 226Ra in natural environments because the Caryophyllids are alarge and cosmopolitan group of plants. It might also be importantagriculturally because there are several important crops in theCaryophyllidae including the grain amaranths, buckwheat and thechards and beets. Sentinel species for biomonitoring of contami-nants are chosen because of their high uptake and plant species forphytoremediation of contaminated soils because they haveparticularly high or low uptake. The analysis reported here suggeststhe particular taxonomic groups that might be targeted whenchoosing species for these purposes.

For many species of plants CRs for Sr and Ra are not available.The data reported here suggest that, for a given soil type, generalpredictions for Sr can be made on the basis of phylogeny. Forexample, there are many Sr CR values for a few cereal crops. Isuggest that these are generally representative of most Commelinidmonocots and are in general lower than the CRs for any other typeof plant growing in a similar environment. I suggest that it isprobably not necessary to measure CRs for all Commeliniidmonocot species in a large ‘gap-filling’ programme but rather toquantify how variable CRs are for this group of plants and assesshow representative current CRs are for this group. Similarly I sug-gest that we already have enough data to suggest that CRs for Sr inthe Caryophyllid are amongst the highest for any plants. A previouspublication (Willey, 2010) analysed the variation in CRs for Csisotopes in the Caryophyllidae and showed that, although theywere variable and were of different magnitude on different soiltypes, most members of the Caryophyllidae had above average CRs.In general, the variation in Ca and Mg concentrations in plants isfound higher up the taxonomic hierarchy than that of Cs (Broadleyet al., 2003, 2004), so the high CRs in the Caryophyllidae for thealkali earth metals might be less variable than those of Cs. There isan indication in the data reported here, which might be worthfurther investigation, that the Rosids in general have slightly lowerthan average, whereas the Asterids have slightly higher thanaverage, CRs for alkali earth metals. Therefore it is possible that forthe very large numbers of Rosids and Asterids in a given environ-ment, CRs of about the average of those measured could predict thefate of Sr. Currently there are insufficient data for the Rosidae andAsteridae to either quantify the variation in CRs or establish abso-lutely that they have slightly below and above average CRsrespectively. To establish this would, however, be much less prac-tically demanding than ‘gap-filling’ by measuring large numbers ofspecies and provide a scientific basis for choosing CRs.

In some environments 226Ra is radiologically important butthere are fewer concentration ratios for Ra than for Sr. I suggest thatthe data in Fig. 2 indicate that known ratios of CRs for alkali earthmetals might be used to make predictions of Ra CRs using phylo-genetic effects. CRs for Sr vary significantly but for many agricul-tural soils and crops a value of about 0.5 is recommended. There’sno doubt that Ra CRs are much lower than those for Sr and from thedata that is available it seems possible that, across different envi-ronmental conditions, the ratio between Ra and Sr might be quitestable. It is certainly the case that ratios between Ca and Sr are quitestable because in many instances there is almost no discriminationbetween them during uptake by plants (Willey and Fawcett, 2005)and that concentrations of Ca and Mg are highly correlated(Broadley et al., 2004; Rios et al., 2012). For Cs it has been proposedthat high uptake in the Caryophyllidae is due to them being muchless discriminatory between Cs and K than other plants (Broadleyand Willey, 1997). Thus, understanding the ratios betweenelemental concentrations that plants accumulate, i.e. their

stoichiometry, might enable predictions of CRs for isotopes forwhich there are few data. This could avoid extensive gap-fillingexercises and suggests that research into phylogenetic effects andstoichiometry might be an efficient way to develop techniques thatcan predict the fate of a wide range of radioisotopes in a wide va-riety of species.

5. Conclusions

Studies of plant ionomes reveal some interesting patterns in theelemental distributions in plants (e.g. Conn and Gilliham, 2010) butthere are also general phylogenetic effects on concentrations ofelements in plants, including those that have radioisotopes. Iono-mics is therefore revealing that the fate of elements in the soil-plantsystem is influenced by phylogeny and that there are correlationsbetween elements. Clearly, the environmental factors that controlavailability in soil will have significant influence over the absolutevalues of CRs for radioisotopes but plant factors also influence thefate of radionuclides and evidence is increasing that phylogeny andstoichiometry might help make general predictions of the fate ofradioisotopes during soil-plant transfer.

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