CHROMIUM and Sediment Toxicity
ERIK RIFKIN RIFKIN & ASSOCIATES PAT R I C K G W I N N AMEC EARTH AND ENVIRONMENTAL EDWARD BOUWER JOHNS HOPKINS UNIVERSITY
Chromium speciation indicates toxicity to benthic organisms better than total chromium does.
ontaminated sediments in fresh and marine ecosystems throughout the world
C
have been associated with ecological and potential human health risks (1–3). Among the pollutants are metals and hydrophobic organics that have low solubility and a strong tendency for sorption (4). Numerous metals fall into this
MICHAEL DORMAN & NOAA
category, such as lead, arsenic, chromium, mercury, and cadmium; organic
contaminants include polycyclic aromatic hydrocarbons (PAHs), polychlorinated biphenyls (PCBs), and pesticides. Although the organics elicit serious concern, quantifying the toxicity due to metals in sediments is especially challenging; the speciation of metals, which is determined by the geochemistry of the water/sediment system, significantly affects their mobility, bioavailability, and toxicity (4, 5).
© 2004 American Chemical Society
JULY 15, 2004 / ENVIRONMENTAL SCIENCE & TECHNOLOGY ■ 267A
In the United States, federal and state environmental agencies are attempting to define levels of chemical exposure to biota that constitute the impairment of a waterbody—for example, Total Maximum Daily Loads—and these can then be used as guidelines for remediation (i.e., point and/or nonpoint source reduction or elimination, sediment capping, or dredging). Currently, only the State of Washington has promulgated criteria or standards for chemicals in sediments, and those are only for marine sediments. Across the country, sediment quality values (SQVs) are used as guidelines or screening levels to assess potential sediment toxicity and, in some cases, to determine acceptable exposure levels (6–11). There appears to be general agreement, however, that sediment-quality guidelines alone may not predict adverse impacts resulting from exposure to contaminated sediments (6–11). Because practically all contaminated sediments contain mixtures of organics and metals, it is virtually impossible to cull out the causative agent(s) responsible for ecological risks. In certain instances, Toxicity Identification Evaluations, which in this case is a site-specific study to focus the search for effective control measures of sediment toxicity, can narrow the sources of sediment toxicity by eliminating some chemicals. But even with this additional characterization, the specific causes of toxicity generally cannot be confirmed. In addition, sediment quality guidelines are usually based on total concentrations of a putative pollutant, thereby ignoring the differences in bioavailability, toxicity, and mobility of different forms of the chemical (e.g., different valence states for metals) in the environment.
Clear evidence indicates that exposure to certain levels of Cr(VI) can result in significant human health and ecological risks. Using published studies, we intend to demonstrate that measuring one such contaminant, total chromium, is not a good indicator of toxicity to benthic organisms. The chromium example can be applied to other metal contaminants that exhibit differences in bioavailability and toxicity depending on chemical form.
Characteristics of chromium Chromium is a heavy metal that is used primarily for manufacturing steel and other alloys. It is also used to preserve wood, tan leather, and electroplate metals. Chromium is also found in refractory bricks used in high-temperature furnaces, pigments, dyes, drilling muds, rust and corrosion inhibitors, textiles, and toner for photocopiers (12). In part because of its widespread industrial use in the United States, chromium has been introduced as a byproduct or waste material to water, soil, sediment, and air. As of November 268A ■ ENVIRONMENTAL SCIENCE & TECHNOLOGY / JULY 15, 2004
2003, a search of the U.S. EPA’s National Priority List database for current sites with chromium in sediment yields 135 sites throughout the country. In aquatic systems, chromium exists primarily in either the trivalent [Cr(III)] or hexavalent [Cr(VI)] states (13). Behavior in these two oxidation states is markedly different. Under oxic conditions, Cr(VI) is the dominant form and, depending on pH, typically exists as either hydrogen chromate (HCrO4– ) or chromate (CrO–2 4 ). Dichromate (Cr2O7– 2 ) forms at low pH and high total concentrations of Cr(VI). Cr(VI) forms anions in water that may remain dissolved or can partition to solids such as iron or aluminum oxides in the water. Cr(VI) can sorb onto metal oxides, but the partitioning of the Cr(VI) species to solids will depend on pH and the concentrations of solids. Under anoxic conditions, Cr(VI) is readily reduced to Cr(III) by a number of chemical (e.g., reduced sulfur, iron, and organic reductants) and microbial species found in the natural environment. Cr(III) has very low solubility at mid-range pH values due to the formation of Cr(OH)3. Because most sediments are anoxic, the oxidation of Cr(III) to Cr(VI) does not readily occur. Consequently, Cr(VI) is more mobile than Cr(III) in many aquatic systems. Clear evidence indicates that exposure to certain levels of Cr(VI) can result in significant human health and ecological risks. Once in vivo, this soluble form of chromium can readily cross the cell membrane and oxidize intracellular compounds (14). Cr(VI) is also a potent human carcinogen when inhaled (15). Dermal contact can result in allergic contact dermatitis (16), and ingestion can result in numerous adverse systemic effects (15). Similarly, bioavailability and toxicity to aquatic organisms have also been associated with dissolved Cr(VI) (17 ). In contrast, Cr(III) is rarely found in the dissolved form, is generally sorbed to organic particles, cannot pass through cell membranes readily, and does not have the same oxidative potential as Cr(VI) (14).
Toxicity of sediments Recognizing that the dissolved fraction better represents the biologically active portion of the metal than the total or total recoverable fraction, EPA recommended that dissolved metal concentrations be used as a basis for the development of ambient water-quality criteria (AWQC) to protect aquatic life (18). While AWQC have been established for Cr(VI), sediment quality guidelines (7) continue to reference total chromium concentrations. The following section provides an analysis of data from field studies and laboratoryspiked experiments to show how chromium chemistry must be considered before the toxicity from sediments is assessed. These case studies provide convincing evidence that the threshold for toxicity is directly correlated with the valence state of chromium (19, 20). EPA chromium sediment toxicity studies. The Atlantic Ecology Division of the EPA’s National Health and Environmental Effects Research Laboratory recently conducted studies to understand the complex relationship between geochemistry, chromium speciation, and toxicity to marine amphipods (19, 20). Berry et al. (19) and Boothman et al. (20) used marine sediments collected off the coast of Southern New
FIGURE 1
Chromium and amphipods Cr(III) (represented by diamonds) is not toxic throughout the spiked range. Cr(VI) (represented by squares) is far more lethal to amphipods once the reducing capacity of acid volatile sulfide is exceeded. (Data from Ref. 19.) 100 90 80 70 % mortality
England and the amphipod Ampelisca abdita to conduct several studies that demonstrated three points. First, sediment containing Cr(III) is not acutely toxic to the amphipod. Second, anoxic sediments, which contain acid volatile sulfide (AVS) and are spiked with Cr(VI), reduce the chromium to the less toxic trivalent oxidation state. Third, sediment with detectable AVS should not contain Cr(VI) and, therefore, will not be toxic to marine organisms. The following paragraphs detail these experiments. Berry et al. conducted a standard EPA acute 10-day amphipod toxicity study on marine sediments spiked with Cr(III) at concentrations ranging from 20 g/kg (Figure 1; 19). No increase was observed in acute amphipod mortality resulting from exposure to even the most highly spiked sediment. In contrast, significant mortality to amphipods was observed in sediments that were spiked with Cr(VI). Berry et al. also evaluated amphipod toxicity on field sediments that contained primarily Cr(III) at concentrations ranging from 10 mg/kg to ~3 g/kg (19). The results were similar to the spiked Cr(III) sediment results: No significant difference occurred in amphipod mortality regardless of chromium concentration. The authors concluded that Cr(III) was not acutely toxic to A. abdita, even at the highest tested concentration (3 g/kg). This conclusion means that one of the most frequently used sediment guidelines, the National Oceanic and Atmospheric Administration (NOAA) sediment guidelines for total chromium, may be overly conservative when used as an indicator of toxicity to A. abdita (19). The NOAA ER-L (effects range-low) and the ER-M (effects range-medium) are defined as the 10th- and 50th-percentile concentration, respectively, in the Biological Effect Database (21). For chromium, the ER-L and ER-M values are 81 and 370 mg total Cr/kg, respectively. In addition, Chapman et al. lists ~50 alternative SQVs for total chromium in marine sediments, which vary depending on which endpoint was evaluated and the databases from which the SQVs are derived (6). However, regardless of which SQV is used for total chromium, the same previously mentioned issues regarding speciation and toxicity apply, including the marine chromium SQVs listed by Chapman et al. (6). A second set of experiments by Berry et al. (19) and Boothman et al. (20) explores the relationship between the presence of Cr(VI) and AVS. Cr(VI) is not thermodynamically favored in anoxic sediment and is readily reduced to Cr(III) under these conditions. However, AVS forms in anoxic sediment only. Therefore, Berry et al. (19) and Boothman et al. (20) spiked increasing concentrations of Cr(VI) into sediment with a known amount of AVS and subjected the sediment to the 10-day acute toxicity test using the amphipod A. abdita. Both groups found that sediment spiked with Cr(VI) is not acutely toxic to the amphipod if AVS is present in sediment because Cr(VI) is reduced to the less-toxic Cr(III) (19, 20). However, once the spiked level of Cr(VI) exceeded the capacity of AVS to reduce the chromium to the trivalent form, Cr(VI) remained and became acutely toxic to the amphipod (Figure 1).
60 50 40 30 20 10 0 10
100
1000
10,000
100,000
Total chromium in sediment (mg/kg)
For sediment containing 20 µmol AVS/g sediment, acute toxicity was not observed until the level of spiked Cr(VI) exceeded 13.8 µmol/g (719 mg/kg), nearly twice the ER-M for total chromium. Studies on freshwater sediments conducted by the U.S. Geological Survey showed similar trends in Cr(VI) reduction in the presence of AVS (22). The findings of these studies strongly suggest that if AVS is present, the chromium should be trivalent and nontoxic. This type of reductive mechanism is a significant natural attenuation process. In the absence of AVS, metal oxides in sediments can sorb Cr(VI) when present as CrO4–2, which also contributes to reduced bioavailability of the Cr(VI) (23). Orange, Texas, stream sediment. As part of an environmental assessment, the Firestone Synthetic Rubber and Tire Co., in Orange, Texas, hired a firm to conduct a baseline ecological risk assessment of its non-process-area property (24). As part of the ecological risk assessment, 11 sediment samples were collected from a brackish water stream referred to as the “stormwater ditch”. As summarized in Table 1, the 11 stormwater ditch sediment samples contained total chromium at levels ranging from 296 to 846 mg/kg, with an average of 496. Seven of the 11 samples contained total chromium at levels in excess of the chromium ER-M. None of the stations contained volatile organic chemicals or concentrations of other bioavailable metals that would pose a potential ecological risk. The sediment samples were subjected to a 10-day acute toxicity test using two amphipod species, Hyalella abdita and Leptocheirus plumulosus. The mean percent survival of the reference stations was between 90 and 96% for the H. abdita and 93 and 98% for the L. plumulosus. None of the stormwater ditch samples exhibited significant toxicity to either the H. abdita or the L. plumulosus when compared with the reference samples (using a one-tailed t-test at a P = 0.05; 24). Although not collected for the purpose of evaluating chromium bioavailability, measurements of AVS were also taken for the 11 stormwater ditch sediment JULY 15, 2004 / ENVIRONMENTAL SCIENCE & TECHNOLOGY ■ 269A
TA B L E 1
Total chromium, acid volatile sulfide (AVS), and amphipod toxicity test results from Firestone Synthetic Rubber and Tire Co., Orange, Texas. Sediment sample
Total chromium (mg/kg)
AVS (µmol/g)
10-day acute toxicity test results (mean % survival) Hyalella Leptocheirus azteca plumulosus
STD1 STD2 STD3 STD4 STD5 STD6 STD7 STD8 STD9 STD10 STD11 REF1A2 REF1B2 REF22 1 This
811 406 846 520 310 426 362 357 678 453 296 18.7 19.5 19.9
47 15 29 33 3.1 12 19 16 27 17 24 32 3 12
81 90 97 91 95 95 89 90 97 93 92 90 96 93
96 681 94 86 91 90 91 87 87 94 95 96 98 93
sample exhibited a relatively high standard deviation in survival. stations are reference locations.
2 These
samples (24). AVS levels in the 11 stormwater ditch samples ranged from 3.1 to 47 µmol/g, with an average of 22. The presence of AVS at these levels indicates that the sediment in the stormwater ditch is anoxic and thus does not support the presence of Cr(VI). As such, it is likely that all of the chromium is nontoxic Cr(III). Baltimore Harbor. McGee et al. collected 25 sediment samples from the Baltimore Harbor–Patapsco River system and measured acute toxicity and population viability of L. plumulosus (25 ). In addition, a sample from a relatively uncontaminated site was subject to the same amphipod toxicity testing as a control or reference station (25 ). Sediments were chemically analyzed in an attempt to correlate the presence of contaminants with acute toxicity. Figure 2 shows a scatter plot of the mean percent amphipod survival versus measured total chromium concentration in sediment derived from the McGee et al. data (25). Of the eight samples with total chromium above the ER-M, only four exhibited toxicity to the amphipod that was statistically different than the reference location (P = 0.05). Interestingly, in three samples having a statistically significant lower amphipod survival, the total chromium concentrations (129, 235, and 325 mg/kg) are below the ER-M. McGee et al. point to the presence of PAHs, cadmium, and PCBs as likely sources of observed toxicity (25). The authors did find a statistically significant negative correlation between survival and sedimentassociated cadmium, copper, and PCBs. These findings are consistent with the results of McGee et al.’s correlation analysis, which did not find a statistically significant correlation between total chromium levels in sediment and observed acute amphipod toxicity (25). This analysis suggests that, in many instances, levels of chromium in excess of the ER-M may not be 270A ■ ENVIRONMENTAL SCIENCE & TECHNOLOGY / JULY 15, 2004
significantly toxic to benthic marine organisms. In addition, McGee et al. reported that the sediments in one location contain both elevated levels of total chromium and high levels of AVS (25 ). Hansen et al. conducted a study in which 14 well-distributed sediment samples collected from this same location all contained AVS, which ranged in concentration from 0.4 to 304 µmol/g, with a mean concentration of 78.4 (26). To put these concentrations into context, Berry et al. found that as long as sediment AVS levels were present in significant amounts (i.e., >0.1 µmol/g), no significant acute amphipod toxicity was observed due to the presence of chromium (19). Presence of elevated AVS in sediments at this location indicates that the sediments are anoxic. As a result, the chromium in sediment at this location is more likely to be the relatively nontoxic trivalent form.
Correctly identifying the hazard According to Chapman et al., “The key to correctly identifying the hazard posed by metals in sediments is evaluation of their exposure potential, which includes bioavailability. Even relatively high levels of contamination may be of little or no biological significance if bioavailability is limited” (27 ). The data reviewed herein demonstrate that the presence of total chromium in sediment at levels considerably higher than the NOAA ER-M can have no significant effect on the survival of marine amphipods. Sediments are rarely contaminated by a single chemical group. Rather, mixtures of contaminants with varying physical and chemical properties, such as petroleum hydrocarbons (fuels and oils), PAHs, PCBs, and one or more metals, are much more likely to be present. Consequently, the observed toxicity, if any, in samples reported in the previously described studies is likely due to other chemicals present in the sediments that are more bioavailable and toxic.
Fate and transport models currently used to predict contaminant concentrations in sediment based solely on total chromium are inappropriate. The primary reason that total chromium is not a reliable determinant of toxicity in sediments is that chromium has two predominant valence states with markedly different properties. Lumping the two chromium oxidation states as total chromium for quantifying toxicity and bioavailability in aquatic systems is not a scientifically valid approach. This serious deficiency in using total chromium is confirmed by the lack of correlation that exists between total chromium and sediment toxicity in the three case studies reviewed in this article.
These case studies also illustrate the importance of site-specific assessments of chemical mobility, bioavailability, and toxicity in determining whether chemicals are adversely affecting the environment. This approach contrasts with relying solely on generic fate and transport models and SQVs to arrive at a conclusion or risk-management decision that may not be scientifically justified or warranted. Fate and transport models currently used to predict contaminant concentrations in sediment based solely on total chromium are inappropriate, because they do not consider the redox chemistry of this metal. One caveat is that under extreme environmental conditions, such as low pH and the presence of strong chelating agents and oxic sediments, Cr(III) can become mobilized and oxidized to Cr(VI), which could lead to better association between total chromium and observed toxicity. Although sediments contaminated with chromium are discussed in detail in this article, other examples exist in which the bioavailability of metals such as mercury, cadmium, copper, lead, nickel, silver, and zinc in sediments may result in significant differences in aquatic toxicity. The case studies with chromium clearly point to a need for a reassessment of approaches to determine toxicity of metals in sediments. Erik Rifkin owns Rifkin & Associates, an environmental consulting firm in Baltimore, Md. Patrick Gwinn is a consultant with AMEC Earth and Environmental in Portland, Maine. Edward Bouwer is a professor in the Department of Geography and Environmental Engineering at Johns Hopkins University. Address correspondence regarding this article to Rifkin at
[email protected].
References (1) Long, E. R.; et al. Environ. Sci. Technol. 1996, 30, 3585–3592. (2) Turgeon, D. D.; et al. Sediment Toxicity in U.S. Coastal Waters; NOAA, National Ocean Service, Coastal Monitoring and Bioeffects Division, Office of Ocean Resources Conservation and Assessment, Coastal Ocean Program, 1998. (3) The Incidence and Severity of Sediment Contamination in the Surface Waters of the United States. National Sediment Quality Survey: Second Edition; EPA-823-R-01-01; U.S. EPA, Office of Science and Technology: Washington, DC, 2001. (4) Bioavailability of Contaminants in Soils and Sediments: Processes, Tools, and Applications; National Research Council, National Academies Press: Washington, DC, 2003. (5) Stumm, W.; Morgan, J. J. Aquatic Chemistry: Chemical Equilibria and Rates in Natural Waters, 3rd ed.; Wiley Interscience, 1996. (6) Chapman, P. M.; et al. Environ. Sci. Technol. 1999, 3, 3537– 3941. (7) Long, E. R.; Morgan, L. G. The Potential for Biological Effects of Sediment-Sorbed Contaminants Tested in the National Status and Trends Program; NOAA Tech. Memo. NOS OMA 52; National Oceanic and Atmospheric Administration: Seattle, WA, 1990. (8) Long, E. R.; MacDonald, D. D. Hum. Ecol. Rick Asses. 1998, 4, 1019–1039. (9) O’Connor, T. P.; Paul, J. F. Mar. Poll. Bull. 2000, 40, 59–64. (10) O’Connor, T. P.; et al. Environ. Toxicol. Chem. 1998, 17, 468–471. (11) Long, E. R.; et al. Environ. Toxicol. Chem. 2000, 19, 2598–2601. (12) Toxicological Profile for Chromium. U.S. Department of Health and Human Services, Agency for Toxic Substances and Disease Registry, Atlanta, Ga. Sept 2000. www.atsdr. cdc.gov/toxprofiles/tp7.html.
FIGURE 2
Survival and total chromium The circular blue symbols designate locations where the mean percent amphipod survival is significantly less than the control1. The vertical line illustrates the NOAA effects range-medium (ER-M) for total chromium (370 mg/kg). (Data from Ref. 25.) 140 % amphipod survival
Implications for risk management
120 100 80 60 40 Total chromium ER-M
20 0
0
500
1000
1500
2000
Total chromium in sediment (mg/kg) 1 For
some samples, the mean percent amphipod survival is >100. This probably occurred as the result of incomplete removal of indigenous amphipods from sediment samples prior to laboratory seeding.
(13) Evanko, C. R.; Dzombak, D. A. Remediation of Metals-Contaminated Soils and Groundwater; Technology Evaluation Report TE-97-01; Ground-Water Remediation Technologies Analysis Center: Pittsburgh, PA, 1997. (14) Wang, W; Griscom, S. B.; Fisher, N. S. Environ. Sci. Technol. 1997, 31, 603–611. (15) Toxicological Review for Chromium (VI); CAS No. 1854029-9; U.S. EPA, Aug 1998, www.epa.gov/iris/toxreviews/ 0144-tr.pdf. (16) Fowler, J. F.; et al. Occup. Environ. Med. 1999, 41, 150–160. (17) Ambient Water Quality Criteria for Chromium—1984; EPA 440/5-84-029; U.S. EPA, Office of Water: Washington, DC, 1985. (18) The Metals Translator: Guidance for Calculating a Total Recoverable Permit Limit from a Dissolved Criterion; EPA 823-B-96-007; U.S. EPA, Office of Water: Washington, DC, 1996. (19) Berry, W. J.; et al. Effects of Chromium in Sediment: 1. Toxicity Tests with Saltwater Field Sediments; U.S. EPA, National Health and Environmental Effects Research Laboratory, Atlantic Ecology Division: Narragansett, RI. Presented at the SETAC 23rd Annual Meeting, Salt Lake City, UT, Nov 16–20, 2002. (20) Boothman, W. S.; et al. Predicting Toxicity of ChromiumSpiked Sediments by Using Acid-Volatile Sulfide and Interstitial Water Measurements; U.S. EPA, National Health and Environmental Effects Research Laboratory, Atlantic Ecology Division: Narragansett, RI. Presented at the 6th Annual NAC/SETAC Conference, Newport, RI, April 2000. (21) Long. E. R.; et al. Environ. Manag. 1999, 19, 81–97. (22) Brumbaugh, W. G.; et al. Effects of Chromium in Sediment: 4. Monitoring of Chromium in Sediment, Pore Water, and Overlying Water of Cr(VI) Spiked Freshwater Sediments; U.S. Geological Survey. Presented at the SETAC 23rd Annual Meeting, Salt Lake City, UT, Nov 16–20, 2002. (23) Dzombak, D. A.; Morel, F. M. M. Adsorption of Inorganic Pollutants in Aquatic Systems. J. Hydraul. Eng. 1987, 113, 430–475. (24) Exponent. Baseline Ecological Risk Assessment, Firestone Synthetic Rubber and Tire Co., Orange, TX, 1998. In Environmental Site Assessment Report, Firestone Synthetic Rubber and Tire Co., Orange, Texas, Dec 10, 1998 submitted to the Texas Natural Resources and Conservation Commission Docket #94-0124-SWR-E. (25) McGee, B. L.; et al. Environ. Toxicol. Chem. 1999, 18, 2151–2160. (26) Hansen, D. J.; et al. Environ. Toxicol. Chem. 1996, 15, 2080–2094. (27) Chapman, P. M.; et al. Can. J. Fish. Aquat. Sci. 1998, 55, 2221–2243. JULY 15, 2004 / ENVIRONMENTAL SCIENCE & TECHNOLOGY ■ 271A
