Published online 7 May 2007
Published in J Environ Qual 36:899-903 (2007)
DOI: 10.2134/jeq2006.0340
© 2007 American Society of Agronomy, Crop Science Society of America, and Soil Science Society of America
677 S. Segoe Rd., Madison, WI 53711 USA
Sample Drying Effects on Lead Bioaccessibility in Reduced Soil
Olha Furman,
Daniel G. Strawn* and
Steve McGeehan
Dep. of Plant, Soil, and Entomological Sciences, Univ. of Idaho, Moscow, ID 83844-2339
* Corresponding author (dgstrawn{at}uidaho.edu)
Received for publication August 28, 2006.
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ABSTRACT
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Risk-assessment tests of contaminated wetland soils often use experimental protocols that artificially oxidize the soils. Oxidation may impact bioavailability of contaminants from the soils, creating erroneous results and leading to improper management and remediation. The goal of this study was to determine if oxygenation of reduced sediments and soils influences Pb bioaccessibility measurements. The study site is located on the Coeur d'Alene River floodplain, downstream from the Silver Valley Mining District in Idaho. A physiologically based extraction test designed to simulate the gastrointestinal tract of waterfowl (W-PBET) was used to measure relative Pb bioavailability (bioaccessibility) from the soils. The soils were collected from a submerged wetland. One set of samples was allowed to air-dry, another set was freeze-dried, and a third set was analyzed wet. The wet soil showed decreased Pb bioaccessibility compared with the air- and freeze-dried soils. The changes in extractability of Fe and Mn on air-drying were opposite from each other: Fe extractability decreased while Mn increased. The results from this study show that redox changes may have significant impacts on Pb bioavailability, and should be considered when assessing Pb contamination risks in reduced soils.
Abbreviations: CDA, Coeur d'Alene • CV, coefficient of variation • ICP–AES, inductively coupled plasma atomic emission spectrometer • W-PBET, waterfowl-physiologically based extraction test
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INTRODUCTION
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MINING and smelting activities in the Silver Valley Region of Idaho have caused extensive heavy metal contamination in the Coeur d'Alene River Basin, including many of the lateral lakes and wetland areas. Migrating waterfowl, including tundra swans (Cygnus columbianus), Canada geese (Branta canadensis), and 14 other species (Blus et al., 1991; Sileo et al., 2001) are at significant risk from Pb poisoning. Waterfowl are particularly susceptible because they ingest contaminated soil when feeding and absorb Pb into the bloodstream during digestion (Oomen et al., 2002).
Risk assessment of Pb poisoning to wildlife requires either a feeding study, or an in vitro test, such as a physiologically based extraction test (PBET). We developed and validated such a test to measure Pb bioaccessibility to waterfowl feeding in the Coeur d'Alene River Basin (W-PBET) (Furman et al., 2006). Bioaccessibility is a relative measure of metal bioavailability from an in vitro test (USEPA, 1999). The W-PBET was developed by modifying in vitro models for humans to account for bird physiology (Furman et al., 2006). The W-PBET gizzard phase results were positively correlated with bird feeding studies described by Heinz et al. (2004). Results from both the in vivo and W-PBET study showed that Pb bioavailability was significantly reduced in P-amended soils. Thus, we concluded that the W-PBET model can be used to measure bioavailability to waterfowl feeding in the Coeur d'Alene River Basin. Such an in vitro test for waterfowl is useful because it is less expensive, simpler, and more easily reproduced than a bird feeding study. As a result of these benefits, the W-PBET model can be used to assess remediation strategies and relative bioavailability (bioaccessibility) on a site-specific basis.
Soils in contaminated wetlands undergo temporal fluctuations in water inundation, resulting in variations in the redox potential. A change in redox status affects the stability of solid phases including manganese, iron, and sulfide minerals (Hem, 1978; Matsunga et al., 1993), which, in turn, can impact the bioavailability of Pb associated with these minerals. Other common Pb forms in soils, such as Pb phosphates, carbonates, oxides, or Pb adsorbed onto clay minerals are not expected to be impacted by redox processes. However, in soils that undergo dynamic redox cycling, association of Pb with Fe, Mn, and S plays an important role in Pb solubility and bioavailability. For example, Beyer and Day (2004) measured exposure of mute swans (Cygnus olor) to metals from contaminated sediments in Chesapeake Bay, USA, and proposed that Pb bioavailability was controlled by sorption of the Pb to iron and manganese oxides. Thus, it is important to consider the redox status of the soils when assessing risks.
Feeding studies and in vivo tests often fail to account for changes in physicochemical properties that occur when saturated field soils are air-dried in preparation for risk assessment tests. Several studies have shown that oxygenation of soils during sampling can affect contaminant chemistry (Rapin et al., 1986; La Force et al., 1999; DeVolder et al., 2003). However, the redox status of the contaminated soils is rarely considered in bioavailability test. For example, feeding studies (Heinz et al., 2004) and in vitro tests (Furman et al., 2006) that reported Pb bioavailability of CDA wetland soils followed the typical protocol of drying the soils before the bioavailability tests. This approach fails to account for the possibility of soil physicochemical changes on drying that may have altered the test results. Hence, the goal of this study was to determine if oxygenation of reduced sediments and soils influences Pb bioaccessibility measurements. Because Pb is associated with iron and manganese oxides, which are redox-sensitive minerals, we also report the extractability of these elements.
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MATERIALS AND METHODS
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Soil Sampling
Soil samples were collected from a wetland at Bull Run Lake, Kootenai County, ID, USA on 13 July 2004. The soils at this site were submerged under approximately 10 to 20 cm of water, had low redox potentials, showed gleying, and released sulfide gas as determined from smell on compression. Thus the soils were deemed to be reducing, with either suboxic or anoxic conditions. Five samples in total were collected from five points separated by 5 m along two 10-m right angle transects that crossed at the midpoint (i.e., a cross pattern). The samples were taken using a 20 cm long, 5 cm diam. split core stainless steel sampler with plastic sleeve inserts and plastic caps (AMS Inc., American Falls, ID).
A Pt-AgCl (Corning, New York) combination reference electrode was used to measure redox state. The measured potentials of the samples were corrected to the standard H-electrode using the theoretical and measured redox potential of potassium ferric-ferro cyanide standard solution relative to the reference electrode (Kehew, 2001).
Five core samples were submersed in liquid N2, purged with N2 gas, sealed in 4 mil polyethylene bags, placed on ice, and transported back to the laboratory where they were freeze-dried and then homogenized in an N2–atmosphere glove box. An additional five duplicate core samples were placed in a nitrogen-purged sealed bag, placed on ice, and transported to the laboratory where they were transferred to the glove box. In the glove box the non-frozen soil cores were homogenized and split into two samples. The redox state of wet soils was measured in the glove box. One set of the split core samples (wet soil samples) were run through W-PBET extraction the day after field collection. Roots and plant debris were separated from the wet soils and water content (air-dried) was gravimetrically measured in triplicate for each sample. The other set of wet soils was air-dried open to the atmosphere at 23°C for 14 d. Redox state of the air-dried and freeze-dried soils was measured in the glove box after they were mixed with enough deionized water for a saturated paste (Rhoades, 1996). The dried soils were gently crushed to pass a 1 mm pore size sieve.
Waterfowl-Physiologically Based Extraction Test Experiment
The gizzard phase of the W-PBET (Furman et al., 2006) was used to measure Pb bioaccessibility on each of the soil cores. Each sample was extracted in replicate three or four times. Blanks (no soil) were also included in all experiments. The gizzard solution consisted of 1 N NaCl and 10 g L–1 pepsin (Sigma Chemical Co., from porcine stomach mucosa) acidified to pH 2.6 with HCl (Kimball and Munir, 1971). Thirty mL of the gizzard solution pre-equilibrated to 42°C was combined with 3.6 g of contaminated wet or dry soil in a 50 mL polycarbonate centrifuge tube. The tube was degassed with high purity N2 (g), sealed, and placed in a reciprocating water bath at 42°C. Samples were mixed in the water bath at 250 rpm for 1 h. Following incubation, samples were centrifuged for 24 min at 2404 relative centrifugal force and the supernatant was filtered through a 25 mm syringe filter with a 0.2 µm polyethersulfone membrane (Pall Life Sciences, Ann Arbor, MI). The filtrates were diluted 1:10 with deionized water before analysis for Cd, Pb, Zn, Fe and Mn using an inductively coupled plasma–atomic emission spectrometer (ICP–AES). National Institute of Science and Technology (NIST) traceable multi-element standards (CPI International, Santa Rosa, CA) were used to assure accuracy in measuring metal concentrations. Fifteen percent of the extracts were analyzed on the ICP in duplicate (relative standard deviation [RSD] < 5%).
Total concentrations of As, Cd, Mn, Pb, S, and Zn were determined using hydrofluoric acid and aqua regia acid-microwave assisted total digestion of the soils (USEPA, 1995). Each soil was digested in triplicate. Relative standard deviation of the triplicate digest ranged from 0.3 to 20% with a 90th percentile of 7%. Five samples of the Standard Reference Material (SRM) reference soil 2711 from the NIST were digested as well to assess accuracy. Recoveries from the standard soil were between 91 and 110% for all reported elements.
Extractable Mn and Fe concentrations were also measured. Although W-PBET assessed bioavailability of Fe and Mn has not been correlated to in vivo tests, we hypothesize that the extractability of these metals in the W-PBET is correlated to their solubility in the waterfowl gizzard. Thus, because Fe and Mn solubility is a function of redox, measuring their extractability in the W-PBET can be used to understand how redox influences Pb bioaccessibility. In this paper Fe and Mn concentrations measured in the W-PBET experiments are referred to as extractable Fe and Mn, as opposed to bioaccessible.
Data Analysis
Lead bioaccessibility values were calculated by normalizing the W-PBET extracted Pb to the total Pb concentration in the soil (i.e., mass of Pb extracted per mass of soil divided by total concentration Pb in soil). Bioaccessibility from the wet soils was calculated by subtracting the mass of water from the mass of wet soil (approximately 3.6 g) added to each extraction tube. Iron and Mn extractability were also calculated by normalizing to total concentration in the sample. W-PBET data were analyzed using a pooled-repeated measures of analysis of variance (ANOVA) test. Fischer's LSD was used to test for significance among mean extracted concentrations. Mean redox potentials were analyzed by ANOVA followed by a mean separation using Tukey's HSD test. The significance level for all tests was p < 0.05.
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RESULTS AND DISCUSSION
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The redox potential of the wet soils was anoxic to suboxic in the field, and after degassing in the glove box (Table 1). Redox potentials in air-dried and freeze-dried soils were significantly higher than the wet soils. Freeze-dried soils had lower redox potentials than air-dried soils.
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Table 1. Pt-electrode redox potential (relative to hydrogen half reaction) of the soils collected from a wetland at Bull Run Lake in Idaho, July 13, 2004.
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Average total concentrations of elements of interest from the 10 samples collected are reported in Table 2. Even though the samples were all taken from within 10 m of each other, coefficients of variation (CV) indicate all elements except Pb had a moderate degree of spatial heterogeneity (Table 2), and Pb spatial variability was high (Essington, 2004). Such high variability is common because of uneven depositional processes, erosion, and pedogenic fluxes. To compare bioaccessibility in samples with varying total Pb concentrations, the extractable Pb was divided by total concentration in the soil, thereby normalizing for the total concentration variance.
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Table 2. Average, standard deviation, range, and coefficient of variation (CV) of concentration of elements in soils collected from the Bull Run Lake wetland in Idaho (n = 10).
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Metal bioaccessibility (extractability) in wet, air-dried, and freeze-dried soils is shown in Fig. 1. All metals showed significantly different bioaccessibility between wet and air-dried soils. Average Pb bioaccessibility in wet soils was about 15% less than the air-dried soils after correcting for water content. Lead bioaccessibility in the freeze-dried soils was about 10% greater than the wet soils, indicating that freeze-drying did not preserve the low Pb bioaccessibility in the reduced soils. This indicates that air-drying of soils can lead to overestimation of Pb bioaccessibility. DeVolder et al. (2003) also reported a decrease in percent Pb bioaccessibility in wet soils as opposed to dry soils in an amendment-greenhouse experiment on metal-contaminated soils. LaForce et al. (1999) observed that the operationally defined exchangeable fraction of soil Pb increased by nearly 10-fold when reduced Coeur d'Alene sediments were artificially oxygenated for 25 d. While the DeVolder et al. (2003) and the LaForce et al. (1999) studies provided evidence that oxygenation increases Pb extractability, it is difficult to infer these results directly to waterfowl bioavailability because (i) LaForce et al. (1999) studied lake sediments and used a sequential extraction procedure to measure the effects of oxygenation, and (ii) DeVolder et al. (2003) measured Pb bioaccessibility from amended soils comprised of mine tailings incubated in the greenhouse using a human-specific waterfowl in vitro test. In the current study, Pb bioaccessibility in samples from a contaminated wetland in the lower CDA basin were compared to dried soils using a waterfowl-specific in vitro test. Hence, results have clear implications for measuring Pb bioavailability by feeding studies or in vitro test.
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Fig. 1. Waterfowl-physiologically based extraction test metal concentrations in wet (corrected for water content), air-dried and freeze-dried soils. Error bars are standard deviations of samples from five separate sites. Means with the same letter are not statistically different (p < 0.05).
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Contaminant minerals that are stable under reducing conditions, such as Pb sulfides, are oxidized on air-drying, thereby increasing their solubility and observed bioaccessibility. Alastuey et al. (1999) observed that when tailings from sulfide ores are exposed to oxygen and water, sulfides oxidize to sulfates, the pH decreases, and contaminants become solubilized. Metal sulfates are more bioavailable than metal sulfides; for example, PbSO4 is more bioavailable than PbS (Ruby et al., 1999).
The extractable Fe and Pb concentrations in the wet, freeze-dried, and air-dried soils were not correlated with the extractable Mn (Fig. 1). However, manganese extractability had similar trends to Pb in air-dried and wet soils, i.e., it was significantly lower in wet soils compared with air-dried soils (Fig. 1). This is in contrast to the expected decrease in Mn extractability due to oxygenation of the more soluble Mn(II) species, and suggests that the Mn(II) was not being oxidized. The observed increase on air-drying must be due to physical or chemical changes in the soil that liberate the Mn(II) species. Ross et al. (2001) showed that air-drying caused an increase in extractable Mn(II). The mechanistic reasons for the contradictory Mn behavior on soil drying are not well understood. Schulze et al. (1995) also observed that a large portion of Mn remains as reduced Mn(II) in completely aerated soils.
Iron extractability was 32 times higher in wet soils (corrected for water content) compared with air-dried soils, and five times higher than the freeze-dried soils. This trend is opposite from the trend observed for Mn. Under reducing conditions Fe(II) species are favored, which are more soluble than Fe(III) species. Air-drying and freeze-drying most likely oxidized the ferrous iron, decreasing its solubility, and therefore decreasing the Fe extractability. Iron extractability was negatively correlated with Pb bioaccessibility (p < 0.05).
Linear regression between Pb bioaccessibility values in wet vs. air-dried soils showed a negative linear relationship (r2 = 0.97) (Fig. 2); i.e., the wet soil with the least Pb bioaccessibility had the greatest bioaccessibility when air-dried. The presence of a negative correlation between Pb bioaccessibility in the air-dried soils and wet soils indicates that the extent of change in Pb bioaccessibility when wet soils are dried is dependent on the amount of bioaccessible Pb in the wet soils, and that the transformation is a distinct change in speciation. Lead species transformations could be sulfide oxidation, or changes in the solid phases that Pb is associated with, such as Fe oxidation, removal of diffusion barriers (e.g., coatings), or oxidation of organic matter. Further studies using molecular scale methods are required to further evaluate this trend.
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Fig. 2. Correlations between Pb bioaccessibility in air-dried and wet soils. Data points represent the average of replicate extractions (n = 4).
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CONCLUSIONS
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Results from this experiment show that artifacts induced from oxidizing reduced-contaminated soils cause overestimation of Pb bioaccessibility. The speciation changes that increase Pb bioaccessibility measured using the W-PBET will likely impact bioavailability results from feeding studies in which the soils are dried and incorporated in animal diet. Furman et al. (2006) showed that bioaccessibility is correlated to bioavailability in a bird feeding study. However, the in vitro and in vivo studies were done using air-dried soils. Results from this study show that for accurate risk assessment of Pb toxicity from soils in reducing environments, care must be taken to preserve the Pb speciation as it occurs in the natural habitat.
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ACKNOWLEDGMENTS
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Advice from Bill Price on statistical analyses is appreciated.
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REFERENCES
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- Alastuey, A., F. Garcia-Sanches, F. Lopez, and X. Querol. 1999. Evolution of pyrite mud weathering and mobility of heavy metals in the Guadiamar valley after the Aznalcollar spill, south-west Spain. Sci. Total Environ. 242:41–55.[CrossRef]
- Beyer, W.N., and D. Day. 2004. Role of manganese oxides in the exposure of mute swans to Pb and other elements in the Chesapeake Bay, USA. Environ. Pollut. 129:229–235.[CrossRef][Medline]
- Blus, J.L., C.J. Henny, D.J. Hoffman, and R.A. Grove. 1991. Lead toxicosis in tundra swans near a mining and smelting complex in Northern Idaho. Arch. Environ. Contam. Toxicol. 21:549–555.[CrossRef][Web of Science][Medline]
- DeVolder, P.S., S.L. Brown, D. Hesterberg, and K. Pandya. 2003. Metal bioavailability and speciation in a wetland tailings repository amended with biosolids compost, wood ash, and sulfate. J. Environ. Qual. 32:851–864.[Abstract/Free Full Text]
- Essington, M.E. 2004. Soil and water chemistry. An integrative approach CRC Press, Boca Raton.
- Furman, O., D.G. Strawn, G.H. Heinz, and B. Williams. 2006. Development of a physiologically based extraction test to measure lead bioaccessibility to waterfowl. J. Environ. Qual. 35:450–458.[Abstract/Free Full Text]
- Heinz, G.H., D.J. Hoffman, and D.J. Audet. 2004. Phosphorus amendment reduces bioavailability of lead to mallards ingesting contaminated sediments. Arch. Environ. Contam. Toxicol. 46:534–541.[Web of Science][Medline]
- Hem, J.D. 1978. Redox processes at surfaces of manganese oxide and their effects on aqueous metal ions. Chem. Geol. 21:199–218.[CrossRef][Web of Science]
- Kehew, A.E. 2001. Applied chemical hydrogeology. Prentice Hall, Upper Saddle River, NJ.
- Kimball, W.H., and Z.A. Munir. 1971. The corrosion of lead in a simulated waterfowl gizzard. J. Wildl. Manage. 35:360–365.[CrossRef]
- La Force, M.J., S. Fendorf, G. Li, and R.F. Rosenzweig. 1999. Redistribution of trace elements from contaminated sediments of Lake Coeur d'Alene during oxygenation. J. Environ. Qual. 28:1195–1200.[Web of Science]
- Matsunga, T., G. Karametaxas, H.R. Gunten, and P.C. Lichtner. 1993. Redox chemistry of iron and manganese minerals in river-recharged aquifers: A model interpretation of a column experiment. Geochim. Cosmochim. Acta 57:1691–1704.[CrossRef][Web of Science]
- Oomen, A.G., A. Hack, M. Minekus, E. Zeijdner, C. Cornelis, G. Schoeters, W. Verstraete, T. Van De Wiele, J. Wragg, C.J. Rompelberg, A. Sips, and J. Van Wijnen. 2002. Comparison of five in vitro digestion models to study the bioaccessibility of soil contaminants. Environ. Sci. Technol. 36:3326–3334.[Medline]
- Rapin, F., A. Tessier, P.G.C. Campbell, and R. Carignan. 1986. Potential artifacts in the determination of metal partitioning in sediments by a sequential extraction procedure. Environ. Sci. Technol. 20:836–840.
- Rhoades, J.D. 1996. Salinity: Electrical conductivity and total dissolved solids. p. 417–435. In D. L. Sparks (ed.) Methods of soil analysis. Part 3. Chemical methods. SSSA, Madison, WI.
- Ross, D.S., H.C. Hales, G.C. Shea-McCarthy, and A. Lanzirotti. 2001. Sensitivity of soil manganese oxides: Drying and storage cause reduction. Soil Sci. Soc. Am. J. 65:736–743.[Abstract/Free Full Text]
- Ruby, M.V., R. Schoof, W. Brattin, M. Goldade, G. Post, M. Harnois, D.E. Mosby, S.W. Casteel, W. Berti, M. Carpenter, D. Edwards, D. Cragin, and W. Chappell. 1999. Advances in evaluating the oral bioavailability of inorganics in soil for use in human health risk assessment. Environ. Sci. Technol. 33:3697–3705.
- Schulze, D.G., S.R. Sutton, and S. Bajt. 1995. Determining manganese oxidation state in soils using adsorption near-edge structure (XANES) spectroscopy. Soil Sci. Soc. Am. J. 59:1540–1548.[Web of Science]
- Sileo, L., L.H. Creekmore, D.J. Audet, M.R. Snyder, C.U. Meteyer, J.C. Franson, L.N. Locke, M.R. Smith, and D.L. Finley. 2001. Lead poisoning of waterfowl by contaminated sediment in the Coeur d'Alene River. Arch. Environ. Contam. Toxicol. 41:364–368.[CrossRef][Web of Science]
- USEPA. 1995. EPA Method 3052: Microwave assisted acid digestion of siliceous and organically based matrices. Test methods for evaluating solid waste, Vol. SW-846. USEPA, Office of Solid Waste and Emergency Response, Washington, DC.
- USEPA. 1999. IEUBK model bioavailability variable. Guidance Document EPA 540-F-00-006. Office of Emergency and Remedial Response, Washington, DC.
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ABSTRACT
INTRODUCTION
