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Journal of Environmental Quality 31:155-162 (2002)
© 2002 American Society of Agronomy, Crop Science Society of America, and Soil Science Society of America

TECHNICAL REPORT
Heavy Metals in the Environment

Natural Uranium and Thorium Distributions in Podzolized Soils and Native Blueberry

L. S. Mortona, C. V. Evans*,b and G. O. Estesc

a Usda/Nrcs, Durham, Nh 03824-2043
b Geology Dep., Univ. of Wisconsin-Parkside, Kenosha, WI 53141-2000
c Dep. of Plant Biology, Univ. of New Hampshire, Durham, NH 03824

* Corresponding author (evansc{at}uwp.edu)

Received for publication September 1, 1999.

   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
 REFERENCES
 
Plant uptake of radionuclides is one of many vectors for introduction of contaminants into the human food chain. Thus, it is critical to understand soil–plant relationships that control nuclide bioavailability. Our objectives in this study were to (i) determine the extent of U and Th uptake and cycling by blueberry (Vaccinium pallidum Aiton) in native habitat and (ii) identify the soil properties and processes that contribute most to U and Th bioavailability in this system. We collected composite samples of plant leaves and stems, and samples from surface (AE) horizons and from the upper part of the Bs horizon at two sites. Concentration ratios (CRs) for U and Th were calculated for all plant tissues, using both the AE and Bs horizons as the base. Soil concentrations of U ranged from 16 to 25 µg g-1, with a mean of 21.1 µg g-1. Soil concentrations of Th ranged from 14 to 97 µg g-1, with a mean of 41.8 µg g-1. Mean U concentrations were 8.65 x 10-3 µg g-1 in leaf tissue, and 7.95 x 10-3 µg g-1 in stem tissue. Mean Th concentrations were 1.59 x 10-1 µg g-1 in leaf tissue, and 9.10 x 10-2 µg g-1 in stem tissue. Blueberry plants are cycling both U and Th in this system, with Th cycling occurring to a greater extent than U. In addition, Th was translocated preferentially to plant leaves while U concentrations showed little preferential translocation. Uranium uptake, however, seemed more sensitive than Th uptake to soil properties.

Abbreviations: CEC, cation exchange capacity • CR, concentration ratio


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
 REFERENCES
 
RADIONUCLIDES exist in the environment naturally and, in more recent times, have been added by nuclear power and weapons. The carcinogenic nature and long half-lives of many radionuclides make them a potential threat to human health. Plant uptake of radionuclides into the human food chain is one of many vectors used for calculating exposure rates and performing risk assessment (Baker et al., 1976; Zach, 1982; Wadey et al., 1991; Hove, 1993; Frissel, 1994; Rosén et al., 1995). In addition, phytoremediation has been used to extract radionuclides and other pollutants from contaminated sites (Salt et al., 1995; Entry et al., 1996; Cunningham and Ow, 1996). The accuracy and success of these applications depend on an understanding of the processes involved in plant uptake of radionuclides.

One important impediment to such understanding is that plant tissue concentrations of radionuclides have rarely shown a linear relationship to radionuclide concentrations in the substrate (soil) (Sheppard and Sheppard, 1985; Sheppard and Evenden, 1988a, 1992; Sheppard et al., 1989). It is therefore critical to study soil–plant systems in order to elucidate the mechanisms that control bioavailability of radionuclides. In addition to bench-scale studies of introduced contaminants, plant and soil interactions on naturally radioactive sites may be extremely useful long-term analogs for anthropogenically introduced radioactivity. Therefore, we have chosen to investigate the soil–plant relationships of blueberry plants growing in soil formed in Conway Granite, which contains elevated levels of naturally occurring 238U and 232Th. Our objectives in this study were to (i) determine the extent of U and Th uptake and cycling by blueberry in native habitat and (ii) identify the soil properties and processes that contribute most to U and Th bioavailability to blueberry in this system.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 CONCLUSIONS
 REFERENCES
 
Hydrothermally altered Conway Granite provides an excellent substrate for the investigation of naturally occurring radioactivity due to its elevated levels of U and Th (Rogers and Adams, 1963; Brimhall and Adams, 1969; Richardson, 1964; Fehn et al., 1978). Conway Granite, as with most geologic materials, has a 232Th to 238U mass ratio of 3.5:1, provided that neither nuclide has been leached or enriched (Rogers and Adams, 1969; Ivanovich, 1994; Cowart and Burnett, 1994). For Conway Granite, U concentrations are typically 11 to 14 µg g-1 and Th concentrations are typically 50 µg g-1, which is approximately twice as radioactive as the average North American igneous rock. The Redstone series (fragmental, mixed, frigid, Typic Haplorthod), a well-drained Spodosol formed in hydrothermally altered Conway Granite material, also has higher radioactivity levels than other soils in the region that have formed in glacial till derived from unaltered Conway Granite (Morton and Evans, 1996).

Blueberry is known to take up radionuclides and heavy metals (Sheppard, 1991 and references cited within), and has been proposed as a metal indicator species by Buszman and Lorek (1982). Furthermore, blueberries are harvested from both natural and cultivated plants in the region, so food chain concerns further enhance the suitability of blueberry as a study population. Plants in this study area were located on banks of gravel quarries in deposits of hydrothermally altered material.

Plot Design and Sampling
Two locations were chosen as sampling sites: Hurricane Mountain in Conway, NH and Red Eagle Pond in Albany, NH. The soil at both sites was the Redstone series, with substratum developed from hydrothermally altered Conway Granite. At each site, five 3- x 3-m plots were selected for study. Since the blueberry plants growing on the plots typically had root systems that ran throughout the entire plot, we chose composite sampling of both plants and soil to accommodate this rooting pattern. Soil cores were collected from two depths—within (0–10 cm) and below (11–25 cm) the rooting zone—at five randomly selected points on each plot (Fig. 1) . Soil horizons in the rooting zone are referred to as AE horizons, because they are mineral horizons that were both organically enriched and somewhat leached, giving a "salt and pepper" appearance. Below the rooting zone, soil samples were collected from the upper part of the Bs horizon. Sampling depth did not exceed 25 cm, even though the Bs horizon often continued much deeper in the profile.



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  		Fig. 1. Diagrammatic representation of soil sampling scheme. Circles represent locations of random samples. Coring depth through horizons is represented as a cylinder in foreground.

 
Composite samples of aboveground vegetation were collected from each plot. Care was taken not to include any material that had external contact with the soil, such as extreme lower stems and soiled leaves. Unfortunately, the majority of these plants were no longer producing significant crops of fruit. This could be due to the drought that occurred that summer, or because these populations are on the fringe of their optimal habitat (Sheppard, 1991). Therefore, only stem and leaf samples could be obtained from the plants on these plots. Plant samples were refrigerated immediately after sampling and processed within 24 h of collection.

Sample Processing and Analysis
Soil samples were air-dried for approximately 3 d and split into four subsamples. The first quarter-sample was used to determine particle-size distribution. As Redstone soils contain as much as 900 g of coarse material per kg of soil, this characterization was limited to dry-sieving of sand fractions and determining the amount of silt and clay as a combined fraction. The second quarter-sample was ground for C and N analysis (PerkinElmer [Wellesley, MA] CHN Analyzer). The third quarter-sample, unsieved, was used for pH determination in 1:10 soil and water and 1:10 soil and 1.0 M KCl solutions. Reserve acidity was estimated by calculating delta pH as the difference between water and salt solution pH values (Mekaru and Uehara, 1972). The fourth quarter-sample was passed through a 62-µm mesh sieve and analyzed for total U and Th by neutron activation analysis (NAA) by a commercial laboratory. Cation exchange capacity (CEC) was determined using the sum of cations (exclusive of H+) extracted from the Mehlich III method (Mehlich, 1984; Tran and Simard, 1993).

The plant samples were weighed, separated into woody stem and leaf samples, and washed thoroughly with distilled deionized water for not more than two minutes. Samples were then immediately put into an oven at 105°C for 24 h. Dried samples were ground in a Wiley mill and ashed in a muffle furnace at 550°C for 4.5 h. When all replicates of the samples had been ashed and homogenized, the composited ashes were re-run at 550°C for an additional 4.5 h to ensure complete combustion. Total U and Th were determined by NAA of the ashed samples.

Data Analysis
Concentration ratios (CRs) for U and Th were calculated separately for stem and leaf tissue such that:

Concentration ratios were calculated twice for each plant tissue type, once using the AE horizon as the base and once using the Bs horizon as the base. Notations for CR values specify the nuclide first (either U or Th). The soil horizon (AE or Bs) and the tissue type (leaves = lv, stems = st) are added as subscripts. For example, the CR for U in leaves based on AE horizons is CRUAE-lv and the CR for Th in stems based on Bs horizons is CRThBs-st.

Data from the 20 soil samples (2 sites x 2 depths x 5 sampling points) were used in an initial analysis of variance (ANOVA) to examine differences among nuclides, horizons, and sites. As many significant interactions occurred between nuclides and the other factors, further ANOVAs (one-way, blocking by site) were done on U and Th separately. A simple correlation matrix was created for each horizon type to assess relationships between U, Th, and various soil properties (pH, delta pH, organic carbon concentration, (silt + clay) combined factor concentration, and CEC). To test whether plant U and Th concentrations were linearly related to soil concentrations, simple correlations were also examined for U and Th in leaves and stems and U and Th in both soil horizon types. Thus, each analysis represents 10 data points. Concentration ratios based on AE horizons were analyzed separately from those based on Bs horizons. One-way ANOVAs (StatSoft, 1996) were also used to test the effects of plant tissue type (stems vs. leaves, blocking by site) on CRs.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 CONCLUSIONS
 REFERENCES
 
Soil Uranium and Thorium
Uranium concentrations were much lower than Th concentrations (p << 0.001; Fig. 2) . In these soils, AE and Bs horizons had average Th to U mass ratios of 2.7:1 and 3.8:1, respectively. Uranium distribution was relatively homogeneous across sites and horizons, but Th levels were significantly lower (p < 0.01) in AE horizons than in Bs horizons. Thorium levels in both AE and Bs horizons were significantly higher (p < 0.01) at Hurricane Mountain than at Red Eagle Pond.



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  		Fig. 2. Concentrations of U and Th in AE (surface horizons) and Bs (subsurface horizons) at Hurricane Mountain and Red Eagle Pond.

 
In AE horizons (Table 1), U concentrations were not significantly correlated to any soil properties. Thorium concentrations, however, were positively correlated with delta pH values (p = 0.020) and negatively correlated with (silt + clay) (p = 0.008). In Bs horizons, both U (p = 0.024) and Th (p = 0.065) concentrations were negatively correlated to (silt + clay). Thorium was again positively correlated to delta pH.


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  		Table 1. Summary of the correlation matrix for horizon U and Th concentrations vs. soil properties. Correlation values are shown with relationships of p < 0.05 in italic type. For each horizon, n = 10.

 
Plant Uranium and Thorium
Mean U concentrations were 8.65 x 10-3 µg g-1 in leaf tissue, and 7.95 x 10-3 µg g-1 in stem tissue, on a dry weight basis. Mean Th concentrations were 1.59 x 10-1 µg g-1 in leaf tissue, and 9.10 x 10-2 µg g-1 in stem tissue, also on a dry weight basis. Thorium contents of stems were significantly lower (p < 0.002) than Th contents of leaves. Plants from Red Eagle Pond contained an average of 1.2 x 10-2 µg g-1 U in both leaves and stems. Mean Th values from Red Eagle Pond were 1.45 x 10-1 µg g-1 in leaves, and 9.19 x 10-2 µg g-1 in stems. Plants from Hurricane Mountain contained 5.31 x 10-3 µg g-1 U in leaves and 5.73 x 10-3 µg g-1 U in stems. Mean Th values from Hurricane Mountain were 1.72 x 10-1 µg g-1 and 9.02 x 10-2 µg g-1 in leaves and stems, respectively. Between sites, only leaf concentrations of U were significantly different (p < 0.03). Plant and soil concentrations of U and Th were not significantly correlated (Table 2).


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  		Table 2. Correlation values from comparison of U and Th in soils with U and Th in plant tissues. None of the correlations were less than p = 0.05. For each horizon type, n = 10.

 
Concentration Ratios
Plots of CRs identify a clear differentiation by tissue type, and by nuclide. Although CRs based on AE horizons are somewhat higher (Fig. 3) , CR trends were virtually identical for AE and Bs horizons (Fig. 4) . Thorium CR values were consistently higher than CRU values (p < 0.0001), and CRThst values were significantly (p < 0.05) lower than CRThlv values. In contrast, CRUlv values were not significantly different from CRUst. In contrast to soil levels (Fig. 2), CR values for both nuclides were higher at Red Eagle Pond (p < 0.05) than at Hurricane Mountain.



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  		Fig. 3. Concentration ratios (CRs) of leaves and stems based on AE horizons. Values for CR have been multiplied by 104 (i.e., actual CR values were no larger than 0.080).

 


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  		Fig. 4. Concentration ratios (CRs) of leaves and stems based on Bs horizons. Values for CR have been multiplied by 104 (i.e., actual CR values were no larger than 0.055).

 
When CRs were calculated based on AE horizons, CRTh in both stems and leaves declined decisively as soil concentrations of Th increased (Fig. 5) . Concentration ratios for U did not exhibit this trend, however (Fig. 5). Additionally, CRThAE-lv and CRThAE-st were highly correlated (R = 0.88, p = 0.001; Fig. 6) , but CRUAE-lv values were poorly related to CRUAE-st values (Fig. 6).



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  		Fig. 5. Regression plot of leaf and stem CRs of Th vs. Th concentration (upper) and CRs of U vs. U concentration (lower) in AE horizons.

 


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  		Fig. 6. Regression plot of U CRs (upper) and Th CRs (lower) in leaves versus stems. Ratios are based on soil concentrations in AE horizons.

 
These trends were repeated in CR data based on Bs horizons. The CRTh values of both stems and leaves declined with increasing Th concentration in the Bs horizon (Fig. 7) . However, CRUBs-lv and CRUBs-st were virtually unrelated to soil U concentrations (Fig. 7). In addition, correlations between CRThBs-lv and CRThBs-st were quite strong (Fig. 8) , but no relationship was apparent between CRUBs-st and CRUBs-lv (Fig. 8).



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  		Fig. 7. Concentration ratios of U (upper) and Th (lower) in leaves and stems versus soil concentrations of U and Th. Ratios are based on soil concentrations in Bs horizons.

 


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  		Fig. 8. Correlation of leaf and stem CRs for U (upper) and Th (lower). Ratios are based on soil concentrations in Bs horizons.

 
The relationships between soil properties and concentration ratios are summarized in an abbreviated correlation matrix (Table 3). The CRs based on AE horizons were more frequently related to soil properties than CRs based on Bs horizons. Also, CRs of U are significantly related to soil properties more frequently than CRs of Th.


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  		Table 3. Concentration ratio (CR) values vs. soil properties. Correlation values are shown with relationships of P < 0.05 in italic type.

 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
CONCLUSIONS
 REFERENCES
 
It has been commonly assumed that both U and Th movement through plant tissues is limited by adsorption onto cell wall materials (Sheppard and Evenden, 1988b). This assumption is reasonable since the tetravalent forms of U and Th are considered highly particle reactive and immobile and/or insoluble in aqueous environments (Langmuir, 1978). Additionally, previous research has shown uranyl (UO+22), a hexavalent and soluble form of U, binds to root cell wall materials (Robards and Robb, 1972). Therefore, the limitations on solubility and mobility might indicate that little U and Th is taken up or translocated within blueberry plants.

In previous studies, fruit was found to have lowest CRs (Mortvedt, 1994). Dunn (1986) showed that twigs and leaves in several tree species had higher concentrations than the roots and trunk. Levels may be highest in older leaves (Popova et al., 1964). Since very few studies have been done on natural systems that isolate and measure radioactivity in the different plant tissues, it is difficult to make generalizations across ecosystems.

Nonetheless, the results in this study compare well with those of others. For example, previous studies (Sheppard and Evenden, 1988b) found that U and Th CR values decrease as soil concentrations increase. This was true for CRTh in both leaves and stems, but not for CRU. The CRTh differences between stems and leaves are also typical of distributions noted by Sheppard (1991) for most elements in blueberry plants. In that study, all elements but Zn and P were more abundant in the leaves than in the stems.

Concentration ratios for blueberry reported by Mahon and Mathewes (1983) agreed well with those in our study, and CRs reported in native blueberry species by Sheard (1986) were close to the higher values obtained in this study. Sheppard and Evenden (1988a) reported results from a controlled pot study of blueberry plants grown in organic soil material artificially contaminated with U. Not surprisingly, they reported CR values nearly an order of magnitude greater than those found in our study, although CR values declined significantly with time. This suggests that plant uptake may eventually equilibrate, perhaps at CR values near values found in the New Hampshire blueberry plants.

It is surprising that CRTh values were significantly higher than CRU values. Thorium has historically been considered highly immobile because it is tetravalent and strongly sorptive (Langmuir, 1978). In this study, however, Th evidenced an apparently enhanced bioavailability, perhaps through complexation or chelation. Root CRs, which were not part of this study, might be useful in interpreting the differences between U and Th behavior and in discerning the relative roles of initial bioavailability and subsequent translocation of U and Th within the plant.

Thorium concentrations are significantly higher in the leaves than in the stem tissue. Leaf production and cycling occurs annually in this climate, but woody stem tissue is more long-lived and also more resistant to decomposition. Thus, Th cycles through the system on an apparent annual basis. In contrast, the more equal distribution of U across stems and leaves may lead to a slower return of U in litter and/or a longer-term sequestration of U in woody debris. Over thousands of years, plant cycles could also contribute to U homogeneity across soil horizons, particularly if U accumulates in resistant organic compounds, and is then absorbed by roots but not translocated to stem or leaf tissue (Robards and Robb, 1972).

Differences between U and Th distributions also point to discrimination mechanisms during uptake and the controls on translocation. Thorium is apparently taken up and translocated readily with stems and leaves having similar proportional amounts of Th. Although Th concentrations in plant tissues were not linearly related to soil Th concentrations, Th CRs were inversely correlated to soil concentration. To some extent, this indicates that Th uptake may plateau within a particular concentration range. Neither U plant concentrations nor U CRs were linearly related to U soil concentrations, suggesting that soil U may be partitioned more explicitly into available and non-available fractions.

In fact, the lack of correlation between CRUlv and CRUst, combined with their respective individual correlations to soil properties, suggests that soil dynamics may exert a strong influence on U partitioning in this system. The differences between stem and leaf concentrations of U and Th have implications for long-term pedogenic and ecosystem processes. It is clear that CRU was more frequently and more significantly related to soil properties than CRTh. For example, higher stem concentrations of U corresponded to higher organic matter in AE horizons, while CRUlv increased with higher (silt + clay) and CEC. It is not clear, however, exactly how soil properties affect the uptake of U and its translocation in the plant. It may be that detailed dissection of the stem tissue and measurement of U distribution would be required to better explain these relationships.

The negative relationship demonstrated between both U and Th and (silt + clay) is counterintuitive. These results appear to contrast with previous research, such as that of Sheppard and Evenden (1992), who reported background U concentrations in soil to be positively related to CEC (and/or organic matter content) at p < 0.01. Other studies have also indicated that radionuclides are associated with the finer material in soils (Frederickson, 1948; Megumi and Mamuro, 1977; Borovec, 1981; Burnett, 1988; Greeman et al., 1990; Baeza et al., 1995). Redstone soils, however, represent an extreme in terms of particle size (fragmental, with <5 g clay 100 g-1 soil). Therefore, variations in (silt + clay) concentrations are most likely based on differences in silt content. Since silt is not a strongly sorptive fraction, the data here do not necessarily contradict earlier findings.

Previous studies have also indicated that bioavailability is inversely related to sorption (Sheppard et al., 1989; Sheppard and Evenden, 1988b, 1992; Nisbet et al., 1993; Skarlou et al., 1996). In this study, Th bioavailability generally increased with higher (silt + clay), although CEC and organic matter relationships to nuclide availability are ambiguous at best. As noted above, however, (silt + clay) most closely represents the silt fraction, which is largely unreactive. Thus, the positive association may simply reflect effects of the larger surface area and the concomitant acceleration of weathering, which supplies Th more rapidly from silt particles than from coarser soil fractions.

Although U and Th are geologically linked (Evans et al., 1997; Ivanovich, 1991, 1994), it is clear that their behavior differs within the soils and plants of this system (Fig. 2). When comparing the eluvial and illuvial horizons, for example, Th to U mass ratios indicate an eluviation of Th, surface accumulation of U, or differential enrichment and/or depletion of both Th and U during soil formation. Thorium concentrations are markedly different between the AE and Bs horizons, which together reflect the process of podzolization. In contrast, U distribution tends to be more homogeneous between horizons. The poor correlation (i.e., disrupted linkage) of U to Th in AE horizons contrasts with the very strong correlation of U and Th in Bs horizons. This suggests that processes in the organic-enriched eluvial zone play a decisive role in distributing nuclides in these soil systems. Thus, nuclide retention and/or mobilization by organic complexes may well be the cause of the disparity between concentrations of Th and correlations of U and Th across horizon boundaries. It is also possible that nuclides associate with Fe or Al compounds that are translocated during podzolization, resulting in relative enrichment in Bs horizons.

Acid leaching, which is closely related to podzolization, has been correlated to nuclide distribution in other studies (Evans et al., 1997). Within the narrow range of pH values in these soils, pH is not correlated to U or Th. Delta pH, however, which tends to increase with intensive leaching, is correlated to Th. In these coarse-textured soils, leaching may remove colloidal particles. The effect may be concentration of resistant primary minerals, such as zircon, which is an important locus of Th in these soils (Evans and Bothner, 1994). The processes of plant uptake and leaching could act in tandem to deplete Th in the surface layer. Then, as Th is removed from surface horizons, Th cycling may be shifted to plant species with deeper roots, which have different uptake, growth, and/or turnover rates, altering ecosystem cycling patterns.


   CONCLUSIONS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
REFERENCES
 
It is clear that blueberry plants are cycling both U and Th in this system, although mechanisms controlling U and Th uptake differ considerably. Although Th uptake is greater than uptake of U, inverse correlations of CRTh to soil concentrations of Th suggest that Th uptake reaches a marked plateau. Furthermore, Th is translocated preferentially to leaves while U concentrations were very similar in both leaves and stems. These differences suggest that Th is more distinctly cycled on an annual basis, while U is more significantly sequestered in woody plant material. Uranium uptake and translocation do appear to be more sensitive to soil dynamics, as evidenced by relationships between CRU and soil organic matter, CEC, and delta pH. Thorium uptake appears to be less sensitive to soil properties. Finally, weathering processes responsible for particle-size reduction (i.e., production of silt-sized particles) and increased surface area appear to enhance release and availability of both U and Th.


   ACKNOWLEDGMENTS
 
This research was funded by a grant to C.V. Evans and G.O. Estes from USDA-NRICGP, #94-37101-0836.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
 REFERENCES
 




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