Environ. Sci. Technol. 1992, 26, 96-101
Acid Volatile Sulfide Predicts the Acute Toxicity of Cadmium and Nickel in Sediments Domlnlc M. Di Taro,*#+ John D. Mahony,$ David J. Hansen,§K. John Scott,lI Anthony R. Carlson,l and Gerald T. Ankleyl
Environmental Engineering and Science Program and Chemistry Department, Manhattan College, Bronx, New York 1047 1, EPA Environmental Research Laboratory, Narragansett, Rhode Island 02592,Science Applications International Corporation, Narragansett, Rhode Island 02592,and EPA Environmental Research Laboratory, Duluth, Minnesota 55804 ~~
Laboratory toxicity tests using amphipods, oligochaetes, and snails with spiked freshwater and marine sediments and with contaminated sediments collected from an EPA Superfund site demonstrate that no significant mortality occurs relative to controls if the molar concentration of acid volatile sulfide (AVS) in the sediment is greater than the molar concentration of simultaneouslyextracted cadmium and/or nickel. Although it is well-known that these metals can form insoluble sulfides, it apparently has not been realized that AVS is a reactive pool of solid-phase sulfide that is available to bind metals and render that portion unavailable and nontoxic to biota. Thus, the AVS concentration of a sediment establishes the boundary below which these metals cease to exhibit an acute toxicity in freshwater and marine sediments.
Introduction Predicting the bioavailability and toxicity of metals in aquatic sediments is a critical component in the development of sediment quality criteria ( I ) . The use of total sediment metal concentration (pmollg dry weight) as a measure of the bioavailability concentration is not supported by available data (2). Different sediments exhibit different degrees of toxicity for the same total quantity of a metal. These differences have been reconciled by relating organism response to the chemical concentration in the interstitial water of the sediments (3-5). In addition, a substantial number of experiments using water-only exposures point to the fact that biological effects can be correlated to the divalent metal activity {M2+](6, 7). This suggests that the bioavailability of metals in sediments is related to the chemical activity of the metal in the sediment-interstitial water system. Hence, the sediment properties which determine the metal activity in the sediment-interstitial water system also determine the fraction of the metal that is bioavailable and potentially toxic. Unless explicitly stated, when we refer to metals in this paper we mean cadmium and/or nickel. For sediments and metals tested to date, metal activity in the sediment-interstitial water system, as measured by acute toxicity to benthic organisms, is strongly influenced by the sulfide and metal concentrations that are extracted from the sediment using cold hydrochloric acid. This sulfide fraction is conventionally referred to as the acid volatile sulfide or AVS (8). The metal concentration that is simultaneously extracted we term the simultaneously extracted metal or SEM. The significance of performing the sulfide and metal extraction under equivalent conditions +EnvironmentalEngineering and Science Program, Manhattan College. f Chemistry Department, Manhattan College. 8 EPA Environmental Research Laboratory, Narragansett, RI. 1 Science Applications International Corp. A EPA Environmental Research Laboratory, Duluth, MN. 96
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is discussed below. For [SEM]/[AVS] < 1,no acute toxicity (mortality >50%) has been observed in any sediment for any benthic test organism. For [SEM]/[AVS] > 1, the mortality of sensitive species (e.g., amphipods) increases in the range of 1.5-2.5 pmol of SEM/pmol of AVS. This observation is important because acid volatile sulfide is found in most freshwater and marine sediments. It is found in sediments with sandy and gravelly textures that do not resemble the anoxic sulfidic sediments that are more commonly associated with the presence of sulfide. Concentrations range from 50 pmol of AVS/g (9-13).
Experimental Procedures The results of four separate experiments are presented in this paper. The detailed experimental procedures are described elsewhere (14-1 7). The sediment toxicity tests generally followed ASTM recommendations (18). Flowing 10 volume replacements/day) and aeration enwater sured acceptable dissolved oxygen concentration. The tests were conducted using 200-900-mL exposure vessels with 200 mL of sediment (3.5-cm depth) and 600 mL of overlying water. The animals were exposed for 10 days to control and test sediments. Sediments were spiked by adding 1.0 L of wet sediment to 2.0 L of dilution water into which a weighted amount of cadmium or nickel chloride had been dissolved. The tests were initiated by adding the sediments to the exposure containers, waiting from 1to 6 days, and adding the animals. After termination, the contents of each exposure container were sieved and counted. Missing individuals were counted as mortalities. Parallel exposures were used for chemical measurements. The acid volatile sulfide (AVS) concentration is the solid-phase sulfide that is soluble in room-temperature 0.5 M HC1 in 1h. The measurement technique is to convert the sulfides to H,S(aq), purge it with oxygen-free nitrogen gas (four bubbles/s), and trap it in a gas-tight assembly (14,19). The reaction vessel is followed by a pH 4 chloride trap (0.05 M potassium hydrogen phthalate) and two sulfide traps (0.1 M silver nitrate) for trapping H2Sas AgzS precipitate. For 10-15 g of wet sediment the detection limit is -0.5 pmol/g. The simultaneouslyextracted metal (SEM) was measured in a filtered aliquot by conventional atomic absorption methods. The AVS and SEM were measured at the s t a r t of the experiment when animals were added and at the termination in the parallel exposure vessels. The initial experiment (14) exposed two marine amphipods (Ampelisca abdita and Rhepoxynius hudsoni) to three uncontaminated marine sediments: a fine-grained sediment with a relatively high AVS sediment (15 pmol of AVS/g) from central Long Island Sound, NY; a sandy sediment with a relatively low AVS (1.3 pmol of AVS/g) from a salt water pond in Ninigret, RI; and an equivolume mixture of the two sediments (4.3 pmol of AVS/g). For (w
0013-936X/92/0926-0096$03.00/0
0 1991 American Chemical Society
this experiment, the total acid extractable cadmium was measured separately. As shown below, this is equivalent to the SEM measurements for cadmium. For the remaining experiments, the SEM concentrations were measured directly. The second experiment (15)simultaneouslyexposed two freshwater organisms, a snail, Helisoma sp., and an oligochaete, Lumbriculus uariegatus, to cadmium added to three uncontaminated freshwater sediments from Pequaywan Lake, MN (42 pmol of AVS/g), East River, WI (8.8 pmol of AVS/g), and West Bearskin Lake, MN (3.6 pmol of AVS/g). The third experiment (16) exposed A. abdita to nickel added to central Long Island Sound and Ninigret Pond sediments. The final experiment (17)exposed the freshwater amphipod, Hyalella azteca, to 17 sediment samples taken from Foundry Cove, a small (213 ha) predominantly freshwater cove in the upper reach of the tidal portion of the Hudson River, NY. These sediments were contaminated with cadmium and nickel from a battery manufacturing facility (20,21). The sediments spanned the range from fine-grained sediments, highly enriched in organic carbon, to gravelly composites with low organic carbon concentrations. The cadmium and nickel concentrations are approximately equimolar throughout the range of sediment concentrations present, 0.3-1000 pmol of SEM/g. AVS ranged from 0.1 to 47 pmol/g, and [SEM]/[AVS] ranged from 0.1 to >lo0 with several in the critical range of 1-3, the mortality increases dramatically. For sediments with [SEM]/[AVS] > 10,8C-100% of individuals from all the tested species died. Conclusions These data suggest the following conclusions. If the ratio [SEM]/[AVS] = 1 is used to discriminate toxic from 98
Environ. Sci. Technol.. Vol.
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10 day) of
nontoxic sediments (greater or less than 50% mortality, respectively), then for the 117 experiments performed, 51% are correctly classified as nontoxic (bottom left quadrant in Figure 3) and 42% are correctly classified as toxic (top right quadrant). That 7% that are misclassified as toxic (bottom right quadrant) follows from the assumption that metal activity will invariably he high enough to cause toxicity if [SEM]/[AVS] > 1, eq 3. It is possible that other ligands, associated with sediment sorption, for example, are reducing the metal activity below that which is lethal to the text organisms. Also, less sensitive organisms can tolerate the increased metal activity even if [SEM]/[AVS] > 1. For organisms that are present when [SEM]/[AVS] > 1, preliminary data suggest that the extent to which metals bioaccmulate is strongly influenced by the AVS concentration (17,28). If a more restrictive interpretation is adopted and the criterion [SEMI/[AVS] < 1is used only to predict when a sediment is not acutely toxic, then all experiments are correctly Classified. We assume that the toxic Foundry Cove sediment with [SEMl/[AVS] = 0.98 is indistinguishable from a unity ratio. Hence our data indicate that sediments with [SEMl/[AVSl< 1, perhaps [SEM]/[AVS] < 0.9 as a safety factor, do not cause greater than 50% mortality in all the sediment toxicity tests performed to date. This is directly attributable to the excess AVS in the sediment, which Bssures that the metal activity in the sediient-inkmtitial water system is below the lethal metal activity for the organisms tested. It is possible that these results are due to a covariation of AVS with other sediment properties, for example, organic carbon or iron content, which are actually controllii the metal hioavailahility. However, the fact that the boundary occurs at [SEM]/[AVS] = 1,as predicted by eq 2, which is based on the supposition that AVS is the controlling sediment property, strongly argues that the relationship is casual, rather than correlative. It should be noted that if the AVS concentration is effectively zero, as it would he in fully aerobic sediments, then other sediment properties would control the metal activity. This does not contradict the assertion that the [SEM]/[AVS] molar ratio of less than 1predicts an absence of toxicity since in this case the molar ratio would be very large. The prediction is not much help hut it is still correct. However, even a small AVS concentration, [AVS] 0.1 pmol/g, can sequester a significant quantity of metal and should he taken into account in determining the potential for metal toxicity for these sediments.
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SEDIMENT (@mol SEM/gm dry wt) Animals and metals as indicated for Seawater (SW) and freshwater (FW) exposures. The lmes connect results Iran the same sediment. FW ihe FouKly Cove sediments,the metal wncenlratiinis the molar sum of the simultaneousiy extracted cadmium and nickel. Flgure 2. Organism mortality versus metal concentration.
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mortality versus the molar ratio of SEM to AVS of the sediment. The sediment metal and AVS are the averages of lhe infiiai and final measured concentrations. For the Foundry Cove sediments. the metal concentration is the molar sum of the simuiianeousiy extracted cadmium and nickel. Symbols defined in Figure 2. Flgure 3. Organism
Additionally, it is important to realize that "anaerobic" and "aerobic" sediments are not precise classifications. Sediments are characterized by an aerobic layer underlaid by an anaerobic layer. The sediments employed in these experiments did not inhibit the survival of the obligate aerobic organisms used in the control exposures-in parti& the tubebuilding amphipods. Most benthic aerobic organisms survive in sediments that are underlaid with
completely anaerobic sediments, which are characterized by significant AVS concentrations. Our experiments suggest that the presence of AVS in the anaerobic layer is sufficient to reduce the metal activity to which the animals are exposed. However, we have not examined the extent to which an aerobic layer depth is suffirient to mitigate the influence of the lower layer AVS. T h u s it is possible to imagine a situation where AVS at depth (>IO cmi might not control metal activity in a completely aerobic overlying layer- the top 10 cm for example-where the animals are exposed. It seems likely that even in this situation the presence of a sink of metals at depth would reduce the activity in the entire sediment to below toxic levels. 'me reasoning is that the diffusional transport of metal in the interstitial water would bring metals from a presumably higher concentration in the aerobic layer interstitial water to the lower concentration in the anaerobic layer. This would eventually deplete the aerobic laver of metals and establish a uniformly low metal activity in the interstitial watersediment system. Thus, even in this case, we would expect that excess A V S would predict the absence of acute toxicity. However, this is yet to be demonstrated experimentally. We believe that the data presented in this paper demonstrate that, for the first time, it is possible to predict Environ. Sci. Technoi.. Voi. 26.
No. 1, 1992
99
when a sediment will not be acutely toxic due to cadmium and/or nickel contamination and, by implication, to all toxic metals that form sulfides that are significantly less soluble than FeS. The criterion is that the molar sum of simultaneously extracted Cd, Cu, Hg, Ni, Pb, and Zn is less than the molar acid volatile sulfide concentration: [SEMlCd + [SEMlCu + [SEMlHg + [SEMlNi + [SEMIpb + [SEMlzn/[AVSl
< 1 (4)
It should be noted that in order to apply this relationship it is necessary to measure all the toxic simultaneously extracted metals that are present in amounts that contribute significantly to the molar SEM sum, typically Cd, Cu, Ni, Pb, and Zn. Failing to do this could lead to an incorrect prediction of the lack of acute toxicity, Le., the sum of the measured SEMs to AVS ratio is less than 1, when in fact the unmeasured metal could increase the SEM concentration so that the ratio exceeds 1and toxicity would be possible. Thus, the acute toxicities of these metals are interrelated, with each contributing to the AVS that is bound by toxic metal. If excess AVS remains, no acute toxicity is expected. If excess metal remains, then the most soluble, Ni and Zn, will appear as free metal and toxicity is possible. Acknowledgments
The assistance and encouragement of the following people is gratefully acknowledged: Christopher Zarba, Criteria and Standards Division, U.S. EPA; Richard Swartz, EPA Research Laboratory, Newport, OR; Mark Springer and Mark Huston, Region 11, U.S. EPA; Herbert Allen, University of Delaware; Robert Thomann, Manhattan College; and, most of all, our research assistants at Manhattan College, M. Hicks, S. Mayr, I. Sweeney, P. Morgan, C. Sydlik, L. Milevoj, and C. Begley; at the EPA Narragansett Laboratory, W. Berry, M. Redmond, D. Robson, and K. McKenna (SAIC); and at the EPA Duluth Laboratory, G. Phipps, V. Mattson, E. Leonard, P. Kosian (AScI), and A. Cotter (AScI).
total dissolved M(II), Fe(II), and S(I1) concentrations, [CM(aq)l, [CFe(aq)l, and [CS(aq)l,respectively. [MS(s)l and [FeS(s)] are the concentrations of solid-phase metal and iron sulfides at equilibrium. [FeS(s)liis the initial iron sulfide concentration in the sediment, and [MIAis the concentration of added metal. The solution of these five equation can be obtained as follows. The mass balance eqs 7 and 8 for M(I1) and Fe(I1) can be solved for [MS(s)] and [FeS(s)]and substituted in the mass balance eq 9 for S(I1): -cY-'sz-[s2-]
+ C X - ~ F ~ Z ++[ FLY-'Mz+[M~+] ~~+] = [MIA
(13)
The mass action eqs 5 and 6 can be used to substitute for [Fez+]and [M2+],which results in a quadratic equation for [S2-]:
[MIA (14) The positive root can be accurately approximated by
which results from ignoring the leading term in eq 14. This is legitimate because the term in parentheses in eq 14 is small relative to [MIAdue to the presence of the sulfide solubility products. As a result, [S2-]is also small since it is in the denominator. Hence, the leading term in eq 14 must be small relative to [MIAand can safely be ignored. The metal activity can now be found from the solubility equilibrium eq 5:
so that
Appendix Solubility Relationships for Metal Sulfides. Consider the following situation: a quantity of FeS is titrated with a metal that forms a more insoluble sulfide. We analyze the result using an equilibrium model of the M(11)-Fe(I1)-S(I1) system. The mass action laws for the metal and iron sulfides are
YMZ+[M~+]~SZ-[S~-] = KMS
(5)
Y F ~ z + [ F ~ ~ + ]= ~ ~KFes ~-[S~-]
(6)
where [M2+],[Fez+],and [S2-]are the molar concentrations; YMZt, yFe2+,and ySz-are the activity coefficients; and KMs and KFes are the sulfide solubility products. The mass balance equations for total M(II), Fe(II), and S(I1) are (Y-'Mz+[M~+][MS(s)] = [MIA
(7)
( Y - ~ F ~ z + [+ F ~[FeS(s)l ~+] = [FeS(s)li
(8)
(Y-'~Z-[S~-] + [MS(s)] + [FeS(s)] = [FeS(s)]i
(9)
where ~ M Z= + aFeZ+
[M2+]/[CM(aq)l
= [Fez+]/ [CFe(aq)l
ap- = [S2-l/[CS(aq)l
(10) (11)
(12)
are the ratios of the divalent species concentrations to the 100
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The magnitude of the term in parentheses can be estimated as follows. The first term in the denominator is always greater than or equal to 1, @Fez+2 1, because it is the reciprocal of two terms both of which are less than or equal to 1, eq 18. They are &Fez+ I1, which is the ratio of the divalent to total aqueous concentration, and ')'Fez+ I1, which is an activity coefficient. The second term in the denominator cannot be negative, PMz+KMs/KFeF> 0, since all of its terms are positive. Thus, the denominator of the expression in parentheses is always greater than 1, PFe2+ PMz+KMS/KFeS > 1. Therefore, the expression in parentheses is always less than 1. Hence, the magnitude
+
of the ratio of metal activity to total added metal is bounded from above by the ratio of the sulfide solubility products: (Me2')/[MlA
< KMS/KFeS
(21)
This result applies if [FeSIi > [MIAso that excess [FeS(s)] is present. If sufficient metal is added to exhaust the initial quantity of iron sulfide, then [FeS(s)] = 0. Hence, the iron sulfide mass action equation (6) is invalid and the above equation no longer applies. Instead, the only solid-phase sulfide is metal sulfide and [MS] = [FeSli
(22)
so that, from the metal mass balance equation (M2') = YM~+~~MZ+([M]A - [FeS(s)]i)
(23)
This completes the derivation of eqs 2 and 3.
acid volatile sulfide concentration (pmol/g) activity of Fe2+ (mol/L) concentration of Fez+ (mol/L) concentration of iron sulfide (mol/L) initial iron sulfide concentration in the sediment (mol/ L) solubility product for FeS(s) [ ( m ~ l / L ) ~ ] solubility product for MS(s) [ ( m ~ l / L ) ~ ] divalent metal activity (mol/L) concentration of M2+ (mol/L) concentration of added metal (mol/L) concentration of solid-phase metal sulfide (mol/L) activity of S2- (mol/L) concentration of S2- (mol/L) simultaneouslyextracted metal concentration (Pmol/g) simultaneously extracted Cd concentration (pmol/g) simultaneously extracted Cu concentration Gmollg) simultaneously extracted Hg concentration (pmol/g) simultaneously extracted Ni concentration Gmollg) simultaneously extracted Pb concentration (cLmol/g) simultaneously extracted Zn concentration (pmol/g) Fe2+1/[CFe(as)l W2+l/[CM(as)l W-l/ [CS(as)l ("Fez+YFe2+)-1 (ffMZ+YM2+)-l
activity coefficient of Fez+ activity coefficient of M2+ activity coefficient of S2concentration of total dissolved Fe(I1) (mol/L) concentration of total dissolved M(I1) (mol/ L) concentration of total dissolved S(I1) (mol/L) Registry No. Cd, 7440-43-9; Ni, 7440-02-0; S2-, 18496-25-8; ZnS, 1314-98-3;PbS, 1314-87-0;CuS, 1317-40-4;HgS, 1344-48-5.
Literature Cited Di Toro, D. M.; Zarba, C. S.; Hansen, D. J.; Swartz, R. C.; Cowan, C. E.; Pavlou, S. P.; Allen, H. E.; Thomas, N. A.; Paquin, P. R.; Berry, W. Environ. Toxicol. Chem., in press. Luoma, S. N. Sei. Total Environ. 1983, 28, 1. Adams, W. J.; Kimerle, R. A.; Mosher, R. G. In Aquatic Toxicology and Hazard Assessment: Seventh Symposium; Cardwell, R. D., Purdy, R., Bahner, R. C., Eds.; American Societyfor Testing and Materials, Philadelphia, PA, 1985; p 429.
Swartz,R, C.; Ditaworth, G. R.; Schulta,D. W.; Lamberson, J. 0. Mar. Enuiron. Res. 1985, 18, 133. Kemp, P. F.; Swartz, R. C. Mar. Environ. Res. 1988,26,135. Sunda, W.; Guillard, R. R. L. J. Mar. Res. 1976, 34, 511. Borgmann, U. In Aquatic Toricology; Nriagu, J. O., Ed.; J. Wiley: New York, 1983; p 47. Berner, R. A. Am. J . Sei. 1967, 265, 773. Aller, R. C. In Estuarine Physics and Chemistry: Studies in Long Island Sound; Saltzman, B., Ed.; Academic Press: New York, 1980; p 238. Reaves, C. Ph.D. Thesis, Yale University,New Haven, CT, 1984.
Nriagu, J. 0. Limnol. Oceanogr. 1963, 13, 430. Nriagu, J. 0.; Coker,R. D. Limnol. Oceanogr. 1976,21,485. Matisoff, G.; Fisher, J. B.; McCall, P. L. Geochim. Cosmochim. Acta 1981,45, 2333. Di Toro, D. M.; Mahony, J. D.; Hansen, D. J.; Scott, K. J.; Hicks, M. B.; Mayr, S. M.; Redmond, M. S. Environ. Toxicol. Chem. 1990,9,1487. Carlson, A. R.; Phipps, G. L.; Mattson, V. R.; Kosian, P.; Cotter, A. ERL-Duluth Report No. 2471, EPA Environmental Research Laboratory, Duluth, MN, 1990. Hansen, D. J.; Scott, K. J. ERL-Narragansett Report EPA Environmental Research Laboratory, Narragansett, RI, 1990.
Ankley, G. T.; Phipps, G. L.; Kosian, P.; Cotter,A.; Mattson, V. R.; Mahony, J. D. Enuiron. Toxicol. Chem., submitted. American Society for Testing and Materials. Proposed New Standard Guide for Conducting Solid Phase 10-DayStatic Sediment Toxicity Tests with Marine and Estuarine Amphipods. Draft No. 5,1989, American Society for Testing and Materials, Philadelphia, PA. Morse, J. W.; Millero, F. J.; Cornwell, J. C.; Rickard, D. Earth Sei. Rev. 1987, 24, 1. Hazen, R. E.; Kneip, T. J. In Cadmium in the Environment, Part I: Ecological cycling; Nriagu, J. O., Ed.; J. Wiley: New York, 1980; p 400. Knutson, A. B.; Klerks, P. L.; Levinton, J. S. Environ. Pollut. 1987, 45, 291. Boulegue, J. In Trace Metals in Sea Water;Wong, C. S., Boyle, E., Bruland, K. W., Burton, J. D., Eds.; Plenum Press: New York, 1983; p 563. Emerson, S.; Jacobs, L.; Tebo, B. In Trace Metals in Sea Water;Wong, C.S., Boyle, E., Bruland, K. W., Burton, J. D., Eds.; Plenum Press: New York, 1983; p 579. Cornwell, J. C.; Morse, J. W. Mar. Chem. 1987,22, 193. Landers,D. H.; David, M. B.; Mitchell, M. J. Int. J. Environ. Anal. Chem. 1983,14, 245. Schoonen, M. A. A.; Barnes, H. L. Geochim. Cosmochim. Acta 1988, 52, 649. Byme, R. H.; Kump, L. R.; Cantrell,K. J. Mar. Chem. 1988, 25, 163.
Striplin, B. D. Skagway Harbor Field Investigation. Tetra Tech, Inc., Bellevue WA, 1990. Received for review December 4, 1990. Revised manuscript received March 12,1991. Accepted July 19,1991. This research was supported by an E P A Cooperative Agreement between Manhattan College and EPA Environmental Research Laboratory, Narragansett, RI. The Manhattan College participation in the Foundry Cove investigation was supported by the National Institutes of Environmental Health Sciences, Superfund Hazardous Substances Basic Research Program, Environmental Medicine, New York University Medical Center,
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