Bioavailability of Barium to Plants and Invertebrates in Soils

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Bioavailability of Barium to Plants and Invertebrates in Soils Contaminated by Barite Dane T. Lamb,†,‡ Vitukawalu P. Matanitobua,†,‡ Thavamani Palanisami,†,‡ Mallavarapu Megharaj,*,†,‡ and Ravi Naidu†,‡ †

Centre for Environmental Risk Assessment and Remediation, University of South Australia, Mawson Lakes, SA 5095, Australia Cooperative Research Centre for Contamination Assessment and Remediation of the Environment (CRC CARE), University of South Australia, Mawson Lakes, SA 5095, Australia

‡

ABSTRACT: Barium (Ba) is a nonessential element to terrestrial organisms and is known to be toxic at elevated concentrations. In this study, the bioavailability and toxicity of Ba in barite (BaSO4) contaminated soils was studied using standard test organisms (Lactuca sativa L. “Great Lakes”, Eisenia fetida). Contamination resulted from barite mining activities. Barium concentrations in contaminated soils determined by Xray fluorescence were in the range 0.13−29.2%. Barite contaminated soils were shown to negatively impact both E. fetida and L. sativa relative to control soil. For E. fetida, pore-water concentrations and acid extractable Ba were linearly related to % body weight loss. In L. sativa, pore-water Ba and exchangeable Ba were both strongly related to shoot Ba and shoot biomass production. A negative linear relationship was observed between shoot Ba content and shoot weight (P < 0.0004, R2 = 0.39), indicating that Ba accumulation is likely to have induced phytotoxicity. Plant weights were correlated to % weight loss in earthworm (r = −0.568, P = 0.028). Barium concentrations in pore-water were lower than predicted from barite solubility estimates but strongly related to exchangeable Ba, indicating an influence of ion exchange on Ba solubility and toxicity to E. fetida and L. sativa.

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colloids by ion exchange,3,11 and is not known to form stable complexes with dissolved organic matter.12 In montmorrilonite, Ba was shown to predominantly be adsorbed to permanently charged basal surfaces. However, Zhang et al. 11 reported that Ba2+ sorbed to montmorrillonite by outer-sphere and innersphere complexes using extended X-ray absorption fine structure spectrometry (EXAFS) and Lee et al. 13 reported inner-sphere adsorption to muscovite. The available data indicate that Ba does not complex (no sharing of electrons) appreciably with humic substances or clay minerals.11,13,14 However, barite solubility is extremely important on the toxicity of Ba in the environment. Barium is known to be toxic to plants and soil invertebrates when soluble. Kuperman et al.15 reported toxicity benchmark values for Eisenia fetida, Folsomia candida, and Enchytaeus crypticus at Ba concentrations in soil in the range 165−2000 mg kg−1. Similarly, Ba is known to accumulate to significant concentrations in aerial plant tissues. Critical tissue Ba concentrations in Panicum maximum (Tanzania guinea grass) were reported in the range 156−383 mg kg−1 when grown in nutrient culture. Similarly, significant Ba accumulation was observed in aerial shoot parts of Bertholletia excelsia (Brazil nut) (5.00 to 325 mg kg−1), with the higher concentrations found in

INTRODUCTION Barium (Ba) is a group 2 element that shares several chemical characteristics with calcium (Ca), strontium (Sr), and lead (Pb). Barium is used in the production of soaps, explosives, fire extinguishers, drilling fluids, and even insecticides.1−3 Barium is not an essential nutrient to animals and plants but instead is known to cause several deleterious effects in most organisms. Exposure to high quantities of Ba in humans may cause hypokalaemia, acute hypertension, vomiting, diarrhea, cardiac arrhythmia, and even death if not treated.4,5 The Australian National Environmental Protection Council (NEPC) has not provided human health guidance values, although it does provide an ecological investigation level of 300 mg kg−1.6 The NEPC value is on par with the U.S. ecological soil screening levels of 330 mg kg−1 for soil invertebrates but not wildlife (2000 mg kg−1).7 Speciation of Ba is well-known to influence solubility.3,8 Chloride, acetate, perchlorate, and nitrate salts of Ba are readily soluble in water, but barite (BaSO4) is a highly insoluble mineral.9,10 Barite is insoluble in water, acids, and bases and on its own is unlikely to cause a risk to humans or the environment. Barite is orally administered to patients deliberately as a radiological tool to visualize the gastrointestinal tract. As has been noted,4 despite the deliberate oral supply of barite, little is known about the risk posed by barite to humans and ecological receptors from environmental media, although it is generally stated to be of little to no risk.3 Barium may be highly mobile in soil, as Ba primarily associates with soil © 2013 American Chemical Society

Received: Revised: Accepted: Published: 4670

May 23, 2012 February 12, 2013 March 13, 2013 March 13, 2013 dx.doi.org/10.1021/es302053d | Environ. Sci. Technol. 2013, 47, 4670−4676

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Table 1. Total Ba Concentrations Estimated from Acid Digestion and XRF, Proportion of BaSO4 a

a

soil

soil pH

% OC

% sand

% clay

ECEC (cmol(+) kg−1)

total Ba acid digest (mg kg−1)

total Ba XRF (mg kg−1)

exch Ba (mg kg−1)

% mortality E. fetida

% weight loss E. fetida

L10/1b L1/1 L1/2 L3/1 L3/2 L4/1 L4/2 L6/1 L6/2 L7/1 L9/1 L9/2

7.8 6.5 6.1 8.1 8.2 8.2 8.3 8.0 8.2 8.2 8.3 8.2

2.54 2.42 1.87 1.92 2.84 2.48 2.97 2.71 2.03 2.42 2.15 1.91

78 65 58 63 60 65 68 75 83 80 78 78

7.5 13 15 10 10 10 10 7.5 5.0 7.5 7.5 7.5

22.0 13.0 nd 21.4 21.9 22.2 23.0 14.2 12.8 10.8 17.1 21.6

120.0 483.0 500.0 1833.0 1867.0 2033.0 1667.0 3367.0 3300.0 4733.0 2167.0 2367.0

700.0 1300 1400 5300 7700 5700 10100 26.9 × 104 29.2 × 104 26.5 × 104 10100 6700

22.04 85.98 nd 77.45 76.36 41.74 44.61 58.28 62.76 41.66 99.69 109.9

0 0 0 0 0 0 0 0 0 40 0 0

−5.59 3.02 5.87 12.7 19.1 7.94 13.0 42.5 43.0 37.2 42.4 41.0

The soil pH, organic carbon contents, cation exchange capacity, clay content, texture classification (USDA) are also included. bControl sample.

fruit.16 In addition, in vitro gastric bioaccessibility has been reported to exceed 2000 mg kg−1 in barite contaminated soils.17 The USEPA7 guidance ECO-SSL values are based on the use of soluble Ba salts and not on barite.3,15 Barite toxicity studies in 100% barite have reported no obvious symptoms of toxicity,3,18 and significant differences in biological response have not been observed even at the highest doses (>106 mg kg−1 soil). However, the use of 100% barite, unweathered or aged samples unlikely represents field sites contaminated by barite. Previous reports on the effect of barite on soil biota have indicated that because of the relatively low solubility of barite (2.2 mg L−1, 25 °C), Ba is unlikely to have deleterious impacts on soil organisms.3,15,19 The present study reports data on the bioavailability and toxicity of Ba to lettuce (Lactuca sativa L. “Great Lakes”) and earthworm (Eisena fetida) in barite contaminated soils as a result of barite mining practices.

again for 24 h. Earthworms were then weighed before being stored at −18 °C. Depurated earthworms were digested in concentrated HNO3 using fresh weights. Plant Uptake. Lettuce (Lactuca sativa L. “Great Lakes”) seeds were sown to plant pots containing barite contaminated soils. Each pot was lined with fine nylon mesh and 300 g of airdry soil added. Each pot was placed within a collecting tray, to which reverse-osmosis water was added (13 μS cm−1). Sufficient seed was added to ensure germination, which was later trimmed to 1 plant per pot. Each soil sample was replicated 4 times. Plants were subsequently grown for 8 weeks. After harvesting, soil samples were allowed to dry. To sample pore-water from the pots, soils were remoistened 14 days prior to sampling, allowing for wet−dry cycles. Five days prior to sampling, soils were moistened and allowed to drain for another 2 days prior to rewetting to field capacity. Twenty-four hours later, soil solution was extracted with Rhizon samplers (pore size of 8) does Ba2+ decline to a small degree. At a pH > 9, BaCO3 dominates Ba speciation in solution. However, in the pH range of soils in this study, Ba2+ represents >90% of 4672

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in our study (i.e., 483.0−4733 mg kg−1). Our results show that despite barite being a highly insoluble mineral in water and acid, barite contamination resulted in stress in the earthworm E. fetida, as indicated by increasing weight loss with barite loading and pore-water concentrations. In this study, acid digestion estimation of Ba content was at least as good an indicator of Ba induced stress in E. fetida as pore-water or exchangeable Ba (P > 0.05). Mortality was only observed in the L7/1 soil, which had the highest observed acid digestion Ba content and barite concentration (45%). No other soil factor (e.g., soil pH, organic carbon) was significantly related to weight loss. Plant Response to Barite. Lettuce dry weight biomass in barite enriched soils was significantly reduced compared to the control soils (see Figure 3). Moreover, all soils enriched with

Figure 2. Solubility of barite and different Ba species (BaX) over a wide pH range (pH 1−14) in a closed system. Inorganic C was constant at 200 mM, although it was predicted to be oversaturated at low pH. Included are measured pore-water concentrations (M) at measured pH values.

aqueous Ba. Pore-water Ba concentrations are all below concentrations predicted by barite solubility. Further complexation would increase the predicted solubility of barite; however, Ba is not known to complex appreciably with dissolved organic matter,12,14 demonstrating that soil solutions are undersaturated with respect to barite. Earthworm Response to Barite. Barite contaminated soils impacted the health of E. fetida as indicated by mortaility and % weight loss (Table 1). Mortality in E. fetida was observed only in soil L7/1 (40%) and not in any other soils. Soil L7/1 had the highest concentrations measured by acid digestion and highest barite content of the studied soils. It was observed that weight loss occurred in barite contaminated soils and was positively related to Ba concentration in the soil. A significant relationship was observed between acid extractable Ba (×10−2) and % weight loss (% weight loss = (0.598 ± 0.134)(Baacid × 10−2) + (7.301 ± 3.7301), P = 0.001, n = 12). Therefore, results of the bioassay show that earthworms were negatively affected as acid extractable Ba concentration in soils increased. Barium porewater concentrations were also linearly related to % weight loss in earthworms (y = (0.26 ±0.009)x − (1.451 ± 8.67), n = 11, P = 0.013). Previous reports have suggested that soil invertebrates are impacted by soluble Ba salts but not barite.29 Menzie et al. 3 summarized several studies and reported that no negative response was reported by soil invertebrates up to 17 000 mg kg−1 Ba (as barite), but an effect was observed on juvenile enchytraeids at 17 000 mg kg−1. Kuperman et al. 15 studied the response of soil invertebrates over a wide range of Ba concentrations (BaSO4, Ba(NO3)2). Adult survival of the three species studied (E. fetida, Enchytraeus crypticus, and Folsomia candida) was not shown to be affected by Ba concentrations (as barite) up to 10 000 mg kg−1 (nominal concentration 15). However, barite was shown to result in a 60% reduction in cocoon production of E. fetida and a 36% reduction in juvenile production of E. crypticus. Furthermore, in Ba(NO3)2 spiked soils survival and reproduction of E. fetida, E. crypticus and F. candida were all significantly reduced with Ba concentrations between 165 and 2000 mg kg−1. The no observed effect concentration (NOEC) of E. fetida was estimated at 1350 mg kg−1 and earthworm reproduction at 260 mg kg−1 measured with concentrated HNO3/HCl. Thus, Kuperman et al. 15 found that E. fetida was affected at acid extractable Ba concentrations much lower than that measured

Figure 3. Lettuce growth in soils contaminated with barite. All soils produced significantly lower biomass than controls: (∗) P < 0.05.

Ba supported significantly lower lettuce growth than the control (P < 0.05). Growth reductions relative to the control soil were greatest in soils L9 and L4, where almost complete growth retardation was observed. In soils where plant growth was severely impacted relative to control soils, leaves become yellow indicating general chlorosis in leaves. Dry weights were not observed to correlate with either XRF or aqua regia extractable metal concentrations. Increasing Ba shoot concentration in lettuce shoots was strongly related to a decrease in shoot weight (P < 0.0004, R2 = 0.39) (Figure 4a). As shoot Ba concentration increased from 0.459−49.0 mg kg−1 in the control treatments to 186 mg kg−1, shoot growth decreased to almost zero. Figure 4c shows that as pore-water Ba increased, there was a significant increase in Ba accumulation in shoots of lettuce; however, the relationship was not linear and significant scatter is evident. A significant relationship between lettuce growth and pore-water Ba was also observed (Figure 4e, P = 0.001). In Figure 4e it is also noted that there is a clear upper limit to plant growth in relation to Ba in soil pore-water. Other factors such as variation in pH, organic C, organic N, negative charge, and clay would influence productivity, but a multiple regression model could not improve the relationship between Ba in pore-water and Ba shoot content and growth. Barium concentration in soil solutions and plant tissue is the primary controlling factor of plant growth in these soils (Figure 4). Barium pore-water concentrations in all soils were below or approximately equal to Ba concentrations from barite solubility (Figure 2). Complexation of Ba by organic ligands such as EDTA or humic substances is limited compared to other metals such as Pb.12,30 Although no speciation of Ba was performed in this study, the limited evidence of complexation by humic 4673

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Figure 4. Relationships between soluble (pore-water) and exchangeable Ba with plant response. Relationships between shoot Ba and shoot biomass (a), exchangeable and pore-water Ba (b), Ba shoot content and pore-water Ba (c) and exchangeable Ba (d), and plant shoot (grams) and pore-water (e) and exchangeable Ba (f).

The presence of negatively charged sites on the soil colloids would promote dissolution of barite over time, with cation exchange sites subsequently becoming a “sink” for baritederived Ba. There is therefore evidence to suggest Ba in porewater is supplied from cation exchange sites associated with surface of soil colloids and thus supply Ba to plant roots. The hypothesis is supported in Figure 4d. Figure 4d depicts a strong linear relationship between shoot Ba and exchangeable Ba (R2 = 0.98, P < 0.0004), where the slope of the line of best fit approximates unity. Furthermore, Figure 4f shows a decrease in plant growth with increasing exchangeable Ba, although the regression is strongly influenced by the control datum point. Ion exchange, in contrast to chemisorption, is a fast chemical reaction, and a loss from soil solution is rapidly resupplied from ion exchange sites.31 Indeed, in plant−soil−solute systems controlled by ion exchange, diffusion from ion exchange sites to plant roots control the rate of solute uptake.32,33 Precipitation and dissolution of barite are known to be rate limited, especially

substances in natural waters indicates that total pore-water concentrations are a reasonable approximation of Ba 2+ concentrations.12 Smith et al.12 reported that between 0.2% and 1.7% of Ba was complexed with fulvic or humic acid. The Ba concentrations observed in most pore-waters were well below that predicted by Ba2+ concentrations from barite solubility, indicating that Ba concentrations in pore-water may have been reduced or impacted by other reactants in the soil, such as negatively charged soil colloids. There is a strong linear relationship observed between measured pore-water concentrations and exchangeable (1 M NH4AOc) Ba (Figure 4b). Since the Ba concentrations were below predicted barite solubility and there was a close correspondence between pore-water Ba and exchangeable Ba, this indicates that ion exchange sites are likely to be an important controlling influence on Ba solubility in these soils. The ECEC soils of these soils are relatively high, being in the range 10.8−23.0 cmol kg−1 (mean = 18.2 ± 1.42 cmol kg−1). 4674

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in the presence of other ions.27,30 Liu and Nancollas 30 showed that the presence of organic ligands and polyphosphate reduced both the precipitation and dissolution rate of barite markedly. The presence of dissolved organic compounds was also shown to modify barite morphology and the steady state Ba concentration.12 In previous studies on Ba toxicity in nutrient culture, root elongation tests have suggested that Ba is toxic only at very high concentrations.18,19,34 Similarly, studies on soil invertebrates with very high barite concentrations added to soils have indicated an absence of Ba-induced impacts.18 However, nutrient solution or freshly “spiked” soil systems do not reflect accurately the conditions found in soils that have been naturally weathered over time. For example, the use of 100% barite, with no ion exchangers, cannot simulate weathered soil samples as was observed in the soils of this study. Our data show that barite contaminated soils may impact plant and earthworm productivity and increase Ba movement in the ecosystem, although this to some extent disagrees with results from previous studies.4,7,35−37

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(11) Zhang, P. C.; Brady, P. V.; Arthur, S. E.; Zhou, W. Q.; Sawyer, D.; Hesterberg, D. A. Adsorption of barium(II) on montmorillonite: An EXAFS study. Colloids Surf., A 2001, 190 (3), 239−249. (12) Smith, E.; Hamilton-Taylor, J.; Davison, W.; Fullwood, N. J.; McGrath, M. The effect of humic stubstances on barite precipitationdissolution behaviour in natural and synthetic waters. Chem. Geol. 2004, 207, 81−89. (13) Lee, S. S.; Nagy, K. L.; Fenter, P. Distribution of barium and fulvic acid at the mica-solution interface using in-situ X-ray reflectivity. Geochim. Cosmochim. Acta 2007, 71 (23), 5763−5781. (14) Hiraide, M.; Hiramatsu, S.; Kawaguchi, H. Evaluation of humic complexes of trace metals in river water by adsorption on indiumtreated XAD-2 resin and DEAE-Sephadex A-25 anion exchanger. Fresenius’ J. Anal. Chem. 1994, 348 (11), 758−761. (15) Kuperman, R. G.; Checkai, R. T.; Simini, M.; Phillips, C. T.; Speicher, J. A.; Barclift, D. J. Toxicity benchmarks for antimony, barium, and beryllium determined using reproduction endpoints for Folsomia candida, Eisenia fetida, and Enchytraeus crypticus. Environ. Toxicol. Chem. 2006, 25 (3), 754−762. (16) Smith, K. The comparative uptake and translocation by plants of calcium, strontium, barium and radium. Plant Soil 1971, 34 (1), 369− 379. (17) Shock, S.; Bessinger, B.; Lowney, Y.; Clark, J. Assessment of the solubility and bioaccessibility of barium and aluminum in soils affected by mine dust deposition. Environ. Sci. Technol. 2007, 41 (13), 4813− 4820. (18) ESG International. Ecotoxicity Evaluation of Reference Site Soils Amended with Barium Sulphate; ESG International: Toano, VA, 2003. (19) Monteiro, F. A.; Nogueirol, R. C.; Melo, L. C. A.; Artur, A. G.; da Rocha, F. Effect of barium on growth and macronutrient nutrition in Tanzania guineagrass grown in nutrient solution. Commun. Soil Sci. Plant Anal. 2011, 42 (13), 1510−1521. (20) OECD. Test 207: Earthworm, Acute Toxicity Tests. OECD Guidelines for Testing of Chemicals; Organisation for Economic CoOperation and Development: Paris, 1984. (21) Rayment, G.; Higginson, F. Australian Laboratory Handbook of Soil and Water Chemical Methods; Inkata Press: Melbourne, Australia, 1992. (22) Gee, G. W.; Bauder, J. W. Particle-Size Analysis; Soil Science Society of America: Madison, WI, 1986. (23) Amacher, M.; Henderson, R.; Breithaupt, M.; Seale, C.; LaBauve, J. Unbuffered and buffered salt methods for exchangeable cations and effective cation-exchange capacity. Soil Sci. Soc. Am. J. 1990, 54 (4), 1036−1042. (24) Zar, G. Biostatistical Analysis, 4th ed.; Prentice-Hall: London, 1999. (25) Lawlor, A. J.; Tipping, E. Metals in bulk deposition and surface waters at two upland locations in northern England. Environ. Pollut. 2003, 121 (2), 153−167. (26) McBride, M.; Mathur, R. R.; Baker, L. L. Chemical extractability of lead in field-contaminated soils: implications for estimating total lead. Commun. Soil Sci. Plant Anal. 2011, 42 (13), 1581−1593. (27) Christy, A. G.; Putnis, A. The kinetics of barite dissolution and precipitation in water and sodium chloride brines at 44−85° C. Geochim. Cosmochim. Acta 1993, 57 (10), 2161−2168. (28) Parkhurst, D. L.; Appelo, C. A. J. User’s Guide to PHREEQC (Version 2). A Computer Program for Speciation, Batch-Reaction, OneDimensional Transport, and Inverse Geochemical Calculations; U.S. Department of the Interior, U.S. Geological Survey: Washington, DC, 1999. (29) Berger, J.; Fornés, L. V.; Ott, C.; Jager, J.; Wawra, B.; Zanke, U. Methane oxidation in a landfill cover with capillary barrier. Waste Manage. 2005, 25 (4 SPEC.ISS.), 369−373. (30) Liu, S.-T.; Nancollas, G. H. The crystal growth and dissolution of barium sulfate in the presence of additives. J. Colloid Interface Sci. 1975, 52 (3), 582−592. (31) McBride, M. B. Environmental Chemistry of Soils; Oxford University Press: New York, 1994.

AUTHOR INFORMATION

Corresponding Author

*Telephone: +61-8- 83025044. Fax: +61- 8-8302 3057. E-mail: [email protected]. Notes

The authors declare no competing financial interest.

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ACKNOWLEDGMENTS We thank the Cooperative Research Centre for Contamination Assessment and Remediation of the Environment (CRC CARE Pty Ltd.) for their support.

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REFERENCES

(1) Miller, R. M.; Honarvar, S.; Hunsaker, B. Effects of drilling fluides on soils and plants: 1. Individual fluid components. J. Environ. Qual. 1980, 9 (4), 547−551. (2) Ippolito, J. Biosolids affect soil barium in a dryland wheat agroecosystem. J. Environ. Qual. 2006, 35 (6), 2333. (3) Menzie, C.; Southworth, B.; Stephenson, G.; Feisthauer, N. The importance of understanding the chemical form of a metal in the environment: The case of barium sulfate (barite). Hum. Ecol. Risk Assess. 2008, 14 (5), 974−991. (4) USEPA. Toxicological Review of Barium Compounds (CAS No. 7400-39-3); United States Environmental Protection Agency: Washington, DC, 2005. (5) Dallas, C. E.; Williams, P. L. Barium: rationale for a new reference dose. J. Toxicol. Environ. Health , Part B 2001, 4, 395−429. (6) NEPC. Schedule B(5) Guideline on Ecological Risk Assessment; Australian Government: Canberra, Australia, 1999. (7) USEPA. Ecological Soil Screening Levels for Barium (OSWER Directive 9285.7-63). United States Environmental Protection Agency: Washington, DC, 2005. (8) Allan, N. L.; Rohl, A. L.; Gay, D. H.; Catlow, C. R. A.; Davey, R. J.; Mackrodt, W. C. Calculated bulk and surface properties of sulfates. Faraday Discuss. 1993, 95, 273−280. (9) Lasley, K. K.; Evanylo, G. K.; Kostyanovsky, K. I.; Shang, C.; Eick, M.; Daniels, W. L. Chemistry and transport of metals from entrenched biosolids at a reclaimed mineral sands mining site. J. Environ. Qual. 2010, 39 (4), 1467−1477. (10) Hatipoglu, S.; Eylem, C.; Gokturk, H.; Erten, H. N. Sorption of strontium and barium on clays and soil fractions. Sci. Geol., Mem. 1990, 86, 79−86. 4675

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Environmental Science & Technology

Article

(32) Pedler, J. F.; Kinraide, T. B.; Parker, D. R. Zinc rhizotoxicity in wheat and radish is alleviated by micromolar levels of magnesium and potassium in solution culture. Plant Soil 2004, 259 (1−2), 191−199. (33) Antunes, P. M. C.; Hale, B. A.; Ryan, A. C. Toxicity versus accumulation of barley plants exposed to copper in the presence of metal buffers: progress towards development of a terrestrial biotic ligand model. Environ. Toxicol. Chem. 2007, 26, 2282−2289. (34) Kopittke, P. M.; Blamey, F.; McKenna, B. A.; Wang, P.; Menzies, N. W. Toxicity of metals to roots of cowpea in relation to their binding strength. Environ. Toxicol. Chem. 2011, 30 (8), 1877− 1833. (35) Suwa, R.; Jayachandran, K.; Nguyen, N. T.; Boulenouar, A.; Fujita, K.; Saneoka, H. Barium toxicity effects in soybean plants. Arch. Environ. Contam. Toxicol. 2008, 55 (3), 397−403. (36) Li, G. Y.; Hu, N.; Ding, D. X.; Zheng, J. F.; Liu, Y. L.; Wang, Y. D.; Nie, X. Q. Screening of plant species for phytoremediation of uranium, thorium, barium, nickel, strontium and lead contaminated soils from a uranium mill tailings repository in South China. Bull. Environ. Contam. Toxicol. 2011, 86 (6), 646−652. (37) NTP. NTP Technical Report on the Toxicology and Carcinogenesis of Barium Chloride Dihydrate (CAS No. 10326-279) in f344/N Rats and B6c6F1 Mice (Drinking Water Studies). NIH Publication 94-3163 and NTIS Publication PB94-214178; National Toxicology Program, Department of Health and Human Services: Research Triangle Park, NC, 1994.

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