Environ. Sci. Technol. 2008, 42, 2162–2167
Phylogeny and Growth Strategy as Predictors of Differences in Cobalt Concentrations Between Plant Species N. J. WILLEY* AND J. WILKINS Faculty of Applied Sciences, University of the West of England, Coldharbour Lane, Frenchay, Bristol BS16 1QY, United Kingdom
Received June 22, 2007. Revised manuscript received December 3, 2007. Accepted December 17, 2007.
Analyses reported here quantify the contribution of plant phylogeny and plant growth strategy to soil-to-plant transfer of Co. Estimated relative mean (ERM) Co concentrations in shoots of 241 species of flowering plant were derived using a residual maximum likelihood (REML) analysis. There were significant differences in, and a loge-normal frequency distribution of, ERM Co concentrations between species. A significant percentage of interspecies variance could be assigned to taxonomic categories above the species, (Family and above 21.5%; Order and above 12.22%). Time-series analysis of ERM Co concentrations ordered in the species-sequence of the Angiosperm Phylogeny Group (APG II (2003)) revealed significant autocorrelation with an increase from Commelinid Monocot to Asterid Eudicot and a pronounced peak in the Core Eudicots. ERM Co concentrations categorized by plant growth strategy sensu Grime (2001) showed an increase toward stress-tolerant strategies. Plant species are not, therefore, independent units of Co concentration — factors derived from higher levels of biological organization exert significant effects. These effects can provide the basis of new techniques for selecting plant species for biotechnologies and for predicting the exposure of organisms to Co. They show that plant phylogeny and growth strategy might help refine predictions of soil-to-plant transfer of a variety of pollutants, and suggest research that might link molecular and higher level processes in contaminated soil-plant systems.
Introduction The stable isotope 59Co and the radioisotope 60Co are pollutants of terrestrial ecosystems—59Co via industrial activities and 60Co from nuclear installations. 60Co is also an important constituent of radioactive waste. The most common entry point of Co to terrestrial food chains is uptake from soil through plant roots. Soil-to-plant transfer of Co is the focus of continuing research for both nutrition (1–3) and pollution/phytoremediation (4). There are refined predictions of the availability of Co to plants from soils (5–7), and a detailed understanding of the mechanisms mediating Co uptake in roots (8), impacting on Co tolerance in plants (9) and affecting compartmentation within shoots (2). There are also established differences between plant species in Co concentrations after similar root exposures (10). Such dif* Corresponding author e-mail:
[email protected]. 2162
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ferences contribute significantly to soil-to-plant transfer of Co and, hence, both to the potential of species in phytotechnologies and to ecotoxicological assessments of exposure through foodchains. However, although soil availability and root uptake of Co are being explored in detail, there is less research focused on understanding interspecies differences in Co concentration following similar exposure. In fact, there are reported concentration data for only a small proportion of the world’s domesticated food crops/cultivars and for a very small proportion of the approximately 300 000 wild species of flowering plants (angiosperms). There is no method to predict values for uninvestigated species or cultivars, and models for pollution prevention and remediation are based primarily on quantification of soil availability. This neglect of interspecies differences arises because of the difficulty in amassing data sets with sufficient interspecies comparisons and the lack of identified plant factors on which to base predictions. There have been significant changes in the past decade in understanding the phylogeny (evolutionary history) of angiosperms (11, 12). It is now clear that differences between plant species in many traits are affected by the phylogenetic position of the species and that new phylogenies have clarified knowledge of these effects. For example, and pertinently for an inorganic pollutant such as Co, characteristic mineralogies can be detected in certain clades (branches) of the angiosperm phylogeny (13–16). Further, it has been shown that there are phylogenetic influences on the concentration in plants of the stable inorganic pollutants Cu, Zn, Ni, Pb, Cd, and Cr (17) and the radioactive inorganic pollutants 134/137Cs (18, 19), 89/90Sr (20), 109Ru (21), and 36Cl (22). These results, based on ANOVAs coded with recent angiosperm phylogenies, have begun to provide an understanding of how the effects of high-level biological organization constrain the exposure of the biosphere to pollutants from the soil. It is an understanding based on evolutionary influences that have seldom been considered in environmental technologies or assessments. An influence of phylogeny on 59Co concentrations was detectable in a recent analysis of plant element composition across four different field sites (16). Here we focus on Co, and we include different Co isotopes, a multispecies comparison from controlled conditions, and a statistical analysis that provides a novel, graphical quantification of relative concentration across the flowering plant phylogeny. Further, for Co and for almost all other elements, there are no previous analyses comparing, as we do here, the effect in intervarietal differences to those higher up the phylogeny. Grime’s plant growth strategy theory describes, for plant species in the established phase of growth, three primary and four secondary growth strategies and makes some explicit predictions about their influence on mineral concentrations and ecosystem processes (23). There is now much empirical evidence that Grime’s growth strategy theory can be used to make reasonable predictions of plant traits such as response to nutrient supply and response to stress (24). In the aftermath of the deposition of Chernobyl-derived radioactive fall-out on Britain, Grime predicted the now widely acknowledged persistence of 137Cs in British upland vegetation (25). It has recently been shown that Grime’s plant growth strategies can be linked not just to the persistence of 137Cs but also to the relative concentrations of 137Cs in different plant species, and that together with the influence of phylogeny it can be used to make general predictions of relative 137Cs concentrations in angiosperms (19). 137Cs is the only pollutant for which the influence of growth strategies on relative concentrations 10.1021/es071531r CCC: $40.75
2008 American Chemical Society
Published on Web 02/14/2008
has been investigated. In contrast to evolutionary effects manifest through phylogeny, growth strategies reflect more recent plant adaptations to particular types of environment. They are, therefore, an additional aspect of high-level biological organization superimposed on that of phylogeny. Growth strategy theory provides a new test of the importance of levels of organization above the species to determining the transfer of pollutants in the soil-plant system. To investigate the influence of phylogeny and growth strategy on relative Co concentrations in angiosperms, a database with concentration values for many species is necessary. This is condition-specific if derived empirically in one set of conditions. A statistical method has been developed based on residual maximum likelihood (REML) analysis to make estimates of relative concentrations in species from different data sets. It provides databases that include concentration data for sufficient species to enable the effects of higher levels of biological organization to be tested (13–22). Here we report experiments that grew 32 plant species and 9 cultivars, analyzed their mean shoot Co concentrations, and then used REML analysis to construct a database of this experimental data plus similar literature data to give estimated relative mean (ERM) Co concentrations for 241 species of angiosperm. We use the database to test the hypotheses that angiosperm phylogeny and plant growth strategy affect Co uptake by plants, and we show that these factors have sufficient influence to help refine predictions of the relative concentrations of 59/60Co in the shoots of important categories of flowering plants.
Experimental Methods Experimental Data. Thirty-two species and nine cultivars were chosen to complement those for which data existed in the literature. The species included both domesticated and wild species from across the angiosperm phylogeny (Table S1) sourced from, respectively, King’s Seeds (Essex, United Kingdom) and Chiltern Seeds (Cumbria, United Kingdom). Five cultivars of Beta vulgaris (“Italian Chard”, “Cheltenham Green”, “Perpetual Spinach”, “Rhubarb Chard”, “Mangel Wurzel”; King’s Seeds, Essex, United Kingdom) and 4 cultivars of Cicer arietenum (“G130”, “C214”, “H358”, “H208”; ICRISAT, Patencheru, AP, India) were grown. For each of the 32 species and 9 cultivars, five replicate 12 cm diameter pots with a single plant were grown in Levington’s F2 compost in a greenhouse with 22 °C 16 h light/15 °C 8 h night. Species/ varieties were grown in three successive batches with five replicate pots of Aster “Michaelmas Daisy” in batches 1 and 2, and five replicate pots of Celosia x “flamingo purple” in batches 2 and 3 providing link species. In each batch, species/ varieties were grown in a randomized block design. At 5 weeks old, plants in each batch were radiolabeled in a randomized block design in an arena supplied with supplementary light at 350 µE m-1 s-1, with 50 mL of 300 µM CoCl2 radiolabeled with 1125 kBq 57Co L-1 added to the substrate surface of each pot, and harvested after 5 h. We assume that this saturated the substrate homogenously because in almost every pot this procedure resulted in excess solution that was caught by saucers and often partially reabsorbed during radiolabeling. Plant shoots were dried at 80 °C, ground, and counted for 57Co γ-emissions with appropriate blanks, standards, and background correction in an LKB Wallac CompuGamma 1282 γ-counter (NaI(Tl) detector). Plants at radiolabeling were in the exponential, established phase of their growth and had not flowered. Literature Data. We found 54 data sets from 28 publications in which concentrations (which ranged from 0.01 to 426 µg/g) of a Co isotope in above-ground green shoots had been compared in at least 2 species of angiosperm under similar conditions (Table S1). Data sets in which foliar contamination might have occurred were not included. The
literature provided data for 214 species. There were 5 species in common with the experimental data, so there were data for 241 species in all, consisting of 568 concentration values from 3 + 54 ) 57 data sets. Statistical Analyses. Two-way ANOVA of experimental data using batch and species as factors was carried out on SigmaStat 3.0. The program of previously reported analyses for other pollutants including radionuclides (18–22), heavy metals (17), and inorganic nutrients (13, 14) was used to relativise Co concentrations across data sets. A REML analysis of loge-transformed concentration values relativizes data for each species across the 54 literature data sets plus the 3 experimental batches by treating data sets as blocks (fixed factors) and their 241 species as treatments. This was run in Genstat for Windows 5th ed. release 4.2 (VAG International, Oxford, United Kingdom) with units and nomenclature of original authors and, as expected, produced relative concentrations for species that in some instances were positive and in others negative (26). Blocking data sets in this way adjusts the absolute differences in values arising from the different edaphic conditions of each data set to provide a database of ERM concentrations in treatments (species). A Kolmogorov–Smirnov test was run on SigmaStat 3.0 for Windows (Systat Software UK Ltd., Hounslow, United Kingdom) to test for normality of ERM concentrations for the 241 species. Time-series analysis in APG II (2003) sequence of the ERM concentrations was performed in Systat 11.0 for Windows (Systat Software UK Ltd., Hounslow, United Kingdom). ERM concentrations were coded using a recent angiosperm phylogeny (APG II, 2003) (12) with 7 levels down the taxonomic hierarchy (“Class”, “Subclass”, “Group”, “Superorder”, Order, Family, Genus), and seven-way ANOVA was run in Genstat for Windows 5th ed. release 4.2. The taxonomic categories Class, Subclass, Group, and Superorder were used in a nominal sense only because they derive from a Linnaean hierarchy that does not have a clear relationship with recent angiosperm phylogenies. A one-way ANOVA was run on SigmaStat 3.0 for Windows on Group values, with Holm-Sidak posthoc tests. ERM concentrations included values for 26 exemplar species of Grime’s growth strategies (27) (Table S1), which were averaged for the three primary strategies and four secondary strategies and were contour plotted using SigmaPlot 9.0 for Windows (Systat Software UK Ltd., Hounslow, United Kindom).
Results ERM concentrations in the 241 species ranged from -6.31 (Arundinaria tecta) to 9.01 (Arenaria marcescens), with a standard error of 0.16 (Table S1) and a frequency distribution that was a negatively skewed bell-curve that failed the Kolmogorv-Smirnov normality test (KS distribution ) 0.113, P ) 0.001) (Figure 1). ERM concentrations for some species were based on numerous absolute concentration values from a variety of different environmental conditions whereas others were made from a single absolute concentration value (Table S1). However, despite the differences in the accuracy of the estimates that this produced, the ERM concentrations in Table S1, together with two-way ANOVA of experimental data (F ) 4.67, P < 0.001; Figure 2), strongly indicate that there are significant differences between species in relative Co concentrations. Given that the absolute values used for the estimates in Table S1 are loge-transformed prior to REML analysis, it seems likely that, from a given Co availability in soil, absolute interspecies differences in Co concentrations in plants might vary by several orders of magnitude. There was some difference between cultivars in Co concentrations, but ANOVA indicated that these were not significant. Time-series analysis of ERM concentrations in APG II (2003) sequence showed significant autocorrelation (Figure VOL. 42, NO. 6, 2008 / ENVIRONMENTAL SCIENCE & TECHNOLOGY
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FIGURE 1. Frequency distribution of estimated relative mean Co concentrations in 241 species of flowering plant following logetransformation and REML analysis of 568 absolute concentration values.
TABLE 1. Results of ANOVA for Mean Relative Concentrations of Co in 241 Species of Plants Coded Using the Phylogeny of APG II (2003)a Cumulative df Class Subclass Group Superorder Order Family Genus residual total
2 1 3 6 15 20 118 75 240
SS x
106
3.17 0.49 19.00 4.06 3.31 22.87 100.90 91.94 245.70
%SS
MS x 106
VR
1.29 1.49 9.22 10.87 12.22 21.53 62.60 100.02
1.58 0.49 6.33 0.68 0.22 1.14 0.86 1.23
1.29 0.40 5.17 0.55 0.18 0.93 0.70
FIGURE 2. Mean Co concentrations in green shoots of 32 species of flowering plants following 5 h of exposure to 50 mL of 300 µM CoCl2 radiolabeled with 1125 kBq 57Co L-1 added to the substrate surface of pot (n ) 5, (1 SE). Species numbers: 1, Allium sativum; 2, Allium cepa “ailsa craig”; 3, Cucumis sativus “telegraph improved”; 4, Amaranthus paniculatus; 5, Mentha spicata; 6, Violax “Swiss giants mixed”; 7, Borago officinalis “bianca”; 8, Gallium vernum; 9, Dianthus caryophyllus “giant chabaud”; 10, Antirrhinum “scarlet giant”; 11, Aster “michaelmas daises mixed”; 12, Euphorbia lathyrus; 13, Papaver commutatum; 14, Helianthemum numularium; 15, Linum lewisii; 16, Fraxinus excelsior; 17, Aesculus hippocastenum; 18, Veronica spicata; 19, Commelina coelestris; 20, Rhuem tataricum; 21, Begonia cordifolia; 22, Fragaria vesca; 23, Phoenix dactylifera; 24, Juncus effusus; 25, Juncus ensifolius; 26, Carex nigra; 27, Lolium perenne; 28, Zingerber officinarum; 29, Celosia x “flamingo purple”; 30, Digitalis purpurea; 31, Beta vulgaris; 32, Cicer arietinum. (F ) 4.67, P < 0.001 for ANOVA of species).
a df, degrees of freedom; SS, sums of squares; MS, mean square; VR, variance ratio.
3 inset) indicating that species-values were not sequentially independent but were correlated to nearby values. Nearby values derive from species that are phylogenetically related. ANOVA coded with a recent angiosperm phylogeny (APG II, 2003) for ERM concentrations in 241 species showed that there was significant variation at the genus level and above, that is, species are not independent samples for Co concentration but have differences that depend to an extent on phylogenetic factors. About 12% of variance was at the level of Order and above, there being especially significant effects at the level of the Group (VR ) 5.17; Table 1). Figure 3 describes an upward trend in ERM concentrations but the most notable feature is the high ERM concentrations in the core eudicot Group (Figure 4). There were 26 species in the database reported here whose growth strategies have been defined experimentally (27). When plotted onto the triangular representation of growth strategies used by Grime (25, 27), there is a trend toward high ERM Co concentrations in plants of the stress-tolerator strategy (Figure 4).
Discussion To describe interspecies differences in Co concentrations by simultaneously measuring uptake in replicates of hundreds of species is time-consuming and impractical. Further, if identical conditions can be attained for all species in such an experiment, then it would generate results that are specific to that set of conditions. The database reported here is 2164
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FIGURE 3. Estimated relative mean Co concentrations in 241 species of plants from REML analysis of 568 concentration values plotted in the species order of Angiosperm Phylogeny Group II (2003), smoothed with a moving mean over 10 values and dashed lines showing (3 SE of overall mean. (Inset: Results of autocorrelation using time-series analysis on plotted values with P ) 0.05 thresholds up to lag of 50). composed of three data sets of experimental concentration measurements derived to complement 54 data sets previously reported in the literature. Data has been relativized from different numbers of replications across a variety of conditions (Table S1). Further, plant exposure time to Co differs between data sets (there being a bias toward acute exposures),
FIGURE 4. Average estimated relative mean Co concentrations in plants of three primary (C ) Competitor, S ) Stress-tolerator, R ) Ruderal) and four secondary growth strategies sensu Grime (2001) contour plotted onto Grime’s triangular representation of growth strategies. (Carex nigra (SC/S), Carex panacea (S) Juncus effusus (C/SC), Anthoxanthum odoratum (SR/CSR), Dactylis glomerata (CSR/ C), Deschampsia caespitosa (CSR/S), Lolium perenne (CR/CSR), Molinia caerulea (SC), Phleum pratense (S/CSR), Poa pratensis (CSR), Poa trivialis (CSR/CR), Chenopodium album (R/CR), Trifolium pratense (CSR), Trifolium repens (CSR/CR), Fragaria vesca (CSR), Sanguisorba minor (S), Helianthemum nummularium (S), Calluna vulgaris (SC), Erica cinerea (S), Vaccinium myrtillus (SC), Galium verum (CSR/S), Fraxinus excelsior (C), Plantago lanceolata (CSR), Digitalis purpurea (CR/CSR), Daucus carota carota (SR/CSR), Campanula rotundifolia (S)) [Species with growth strategies in zone A tend to accumulate nutrient resources; species in zone D tend to convert nutrient resources into growth].
as does plant age and type (there being a bias toward young, herbaceous nonaquatic plants in the database). These differences in conditions, exposure, and plant status are the weakness and the strength of the database because, respectively, accuracy of the estimates of mean relative concentrations varies but estimates are mean values across a range of experimental/plant combinations and thus provide general estimates across a variety of conditions. There is also a limitation with the REML procedure described; it does not take account of any interactions between interspecies differences and environmental conditions, potentially confounding the estimation of relative mean concentration. If relative concentrations change with conditions, then variance would increase and make it less likely that we would find the effects reported here. If there is a correlation between phylogeny and environmental conditions (which might arise through adaptation of taxa to particular soil types for example), then the effects described might not be phylogenetic. However, there is much data from controlled conditions in Table 1, and based on field samples, it has been reported that such correlations are not significant in any case (16). So, despite the above limitations, we suggest that the effects detected are real but that they apply most securely to young herbaceous plants acutely exposed to Co. This is itself frequently an important pattern of exposure to Co, but given that most plants take up the majority of nutrient ions during the exponential growth phase (28), in which most of the plants in the database were exposed, it is likely also to reflect longer term exposure patterns. Analyses of the experimental data, the largest interspecies comparison yet reported for Co under controlled conditions,
confirm that there are significant differences between species in Co concentration after identical exposures. Intervarietal comparisons suggest that if such differences exist then they are of lower magnitude than interspecies differences. This accords with recent reports that, in contrast to other macroand micronutrients, there are no intervarietal differences in Lens culinaris in Co concentrations after similar exposures (29). So, the great range of Co concentrations reported here suggests that, even if Co is highly available in a soil, there are some plant species that will take it up to relatively low concentrations, that is, there is a significant plant-derived contribution to difference in soil-to-plant transfer. To make accurate predictions of soil-to-plant transfer of 59/60Co for all combinations of soil type and plant species it is, therefore, necessary to be able to predict not just availability in a soil but also the species contribution to differences in transfer. Figure 1 suggests that although ERM Co concentrations fail the test of normality they have an essentially normal but skewed distribution. In fact, the database includes a few species with particularly high concentrations (Supporting Information Table S1; Figure 1), and although there are no Co hyperaccumulating species of plants included in Table S1, a few species are skewing the frequency distribution. Figure 1 therefore suggests that concentrations in different plant species in the field after similar exposure will be approximately loge-normally distributed. This is the frequency distribution reported from field collected samples in the only other study that has described it (16). Knowledge of the attributes of this frequency distribution is useful for modeling differences, especially using probabilistic modeling, in soilto-plant transfer and has been noted for some other radionuclides, although for many fewer plant species (30). It is part of an increasing body of evidence that loge-normal frequency distributions characterize soil-to-plant transfer across numerous plant species for many elements (16) and pollutants (19–22). There are at present no methods to predict relative concentrations of Co in plant species. To do this it is useful to isolate plant factors that explain some of the variance in ERM Co concentrations. Figure 3 and Table 1 show that there is a significant phylogenetic signal in ERM Co concentration that might aid the prediction of relative Co concentrations in plants. At the Ordinal level and above, with 12% of the cumulative sum of squares, Co concentrations have phylogenetic effects greater than those on N (3.3%) and P (6.8%) (14), similar to those on Cs (15%) (19) and Sr (15%) (20), but less than those for Pb (20%), Cr (23%), Cu (24%) (16), Na (23%) (13), Cd (27%) (15), Cl (35%) (20), Ru (39%) (19), Zn (44%), Ni (46%) (15), K (49%) (14), or Ca (63%) (13). At the family level and above, 21.5% of the variance is associated with phylogeny (Table 1) — a value very nearly the same as that reported (20.7%) in the only other report of effects of phylogeny on Co concentrations in plants (16). Of the taxonomic categories above the species, there is reasonable replication in the data reported here in each of the Group categories, and it seems very clear (Figure 3) that, in general terms, the Commelinid Monocots have lower than average relative mean Co concentrations in them, that Core Eudicots have higher than average, and Rosids have average concentrations. One-way ANOVA of Group values confirmed the existence of significant differences between Groups (F ) 14.77, P < 0.001) with both Core Eudicots and Asterids having significantly higher concentrations than non-Commelinid Monocots, Commelinid Monots, and Rosids (Holm-Sidak posthoc test at P ) 0.05). Interestingly, the phylogeny of protein transporters that mediate the uptake of ions in plant roots is currently being described (e.g., via PlantsT database: http://plantst.genomics.purdue.edu/ plantst/html/phylo.html). If phylogenetic effects in relative Co concentrations and the phylogeny of transporters that mediate Co uptake become known in sufficient detail, then they might VOL. 42, NO. 6, 2008 / ENVIRONMENTAL SCIENCE & TECHNOLOGY
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provide a useful test of the links between molecular effects and those at higher levels of biological organization. The three primary and four secondary growth strategies defined by Grime (23) have mineral accumulation strategies as an axis of specialization, primarily because nutrient deficiency is an important stress to plants. Grime’s growth strategy theory has recently been reported to be a better predictor of response to stress than those based on resourceratio hypotheses (24). Given that many inorganic pollutant ions are chemically closely related to plant mineral nutrients, or even are plant mineral nutrients but in above optimal amounts, it seems likely that the growth strategies of plants sensu Grime might influence the uptake of inorganic pollutants by plants. The concentrations of Cs in flowering plants have been shown to be influenced by plant growth strategy, with stress-tolerant ruderals having the highest concentrations (19). Figure 4 here suggests that stress tolerant plants have the highest relative concentrations of Co. It is notable that for neither Cs nor Co do plants of competitive strategies have high concentrations but rather those that fall within zone A of the growth strategy triangle where there is a tendency to accumulate nutrient resources. Growth strategy theory can be used to predict numerous aspects of ecosystem processes, including those that impact on nutrient dynamics (23, 24); linking pollutant behavior to plant growth strategy might thus be the basis of improved predictions of pollutant dynamics in ecosystems. It is, however, necessary to know growth strategies of many plant species to do this in a variety of ecosystems. The growth strategies of 286 ordinal species has been defined using an extensive set of experiments (27), but simpler methods have been developed that, in theory, enable the growth strategy of many more plant species to be predicted (31). In the 54 literature data sets used here, values are not given for the variables necessary to predict growth strategies. However, the link between growth strategy and Co concentration we have established shows that predicted growth strategies can provide a new perspective on the effects of high levels of biological organization on pollutant movement in the soil-plant system. We conclude that, from a given set of environmental conditions, there are significant interspecies differences in the concentrations to which plants accumulate Co and that a significant proportion of these differences can be predicted from plant phylogeny. Further, we suggest that much of the remaining variance should not just be ascribed to site conditions but that other plant factors such as growth strategy can be significant. We predict that, for a given soil Co availability, plant species on the Core Eudicot clades of the stress-tolerant growth strategy will have the highest Co concentrations and that Commelinid Monocots of the competitive strategy will have the lowest. We suggest that the magnitude of variation in relative concentrations, the frequency distribution, and the effects of phylogeny and growth strategy reported will be useful in predicting the plantderived differences in soil-to-plant transfer of Co. They are, therefore, a useful complement to models that predict the availability of Co in soil and the compartmentation of Co within shoots. For a number of inorganic heavy metal and radioactive pollutants it is now established that phylogenetic effects in plant concentrations exist and that for some inorganic pollutants there are links to growth strategies. Differences in plant traits impacting on organic pollutant degradation and uptake have been investigated for genera within a family (29), between species (30), and between varieties (31) but not yet within recent phylogenetic frameworks. We suggest that the influence of phylogeny and growth strategy on plant traits impacting on many pollutants, including organic pollutants, is worth further investigation. As the foundation of terrestrial foodchains, the soil-plant system plays a key role in determining the exposure of 2166
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terrestrial organisms to pollutants. The ability to predict pollutant behavior in the soil-plant system is crucial not just for calculating exposure but also to plant-based environmental technologies. Such technologies are rapidly becoming part of the tool-kit of environmental engineers (35, 36). There is more knowledge of pollutant behavior in soils than of the influence of plant characteristics, especially of factors related to higher levels of biological organization in plants. This is unfortunate because plant factors have often been shown to significantly influence soil-to-plant transfer of pollutants. The methods we report here and the effects we establish show that influential factors derived from high levels of biological organization can be identified and that they can be useful for quantifying the contribution that any plant taxon might make to soil-to-plant transfer of a pollutant. This can help to refine predictions of the exposure of organisms and provides a basis for species selection for plantbased environmental technologies. For environmental biotechnologies, biodiversity is an exploitable resource, but most species used are selected on the basis of their occurrence at contaminated sites. The plant factors identified here might help mine plant biodiversity for taxonomic units, and ultimately for genes, useful to plant-based environmental technologies. They reflect evolutionary processes and growth strategies linked to vegetation processes/ecosystem properties and are thus a reminder that fundamental mechanisms important to ecotoxicology and environmental health occur at high levels of biological organization.
Acknowledgments We would like to thank the UK Food Standards Agency for funding, Judy Brown of UWE, Bristol for help with radioanalysis, and A. Mead of Warwick HRI for developing the REML program.
Supporting Information Available Table S1 provides ERM Co concentrations for all 241 species in phylogenetic layout and includes details of all data sources and data extracted from them. This material is available free of charge via the Internet at http://pubs.acs.org.
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