Environ. Sci. Technol. 1997, 31, 2577-2583
Effect of Sedimentary Organic Matter Composition on the Partitioning and Bioavailability of Dieldrin to the Oligochaete Lumbriculus variegatus L. J. STANDLEY* Stroud Water Research Center of the Academy of Natural Sciences, Avondale, Pennsylvania 19311
Current hypotheses link the bioavailability of contaminants in sediments to their partitioning behavior to organic matter in sediments. Because contaminant partitioning varies with sediment composition, it follows that composition should also affect contaminant bioavailability. In this study, variations in dieldrin partitioning and bioavailability, as measured by organic carbon/lipid-normalized bioaccumulation factors for Lumbriculus variegatus, were related to sediment composition. Study sediments covered a wide range of composition and organic matter content. Normalizing the bioaccumulation factors to the organic carbon content of sediments and lipid content of organisms reduced ranges of measured dieldrin accumulation factors from 38-fold to 8-fold. Factors describing sediment composition were tested to determine whether they explained the remaining variability between sediments. Variations in partitioning were best explained by the proportion of sedimentary organic matter that was solvent extractable. However, bioavailability correlated most strongly to pH. There was little correspondence between factors that explained variability in partitioning and those covarying with bioaccumulation.
Introduction Toxicity of contaminants in sediments to benthic biota is limited by the bioavailability of those contaminants. Many factors control the bioavailability of contaminants and include sorption by organic matter (1, 2), length of time of association between contaminants and sediment (3), kinetics of contaminant desorption (4), and the feeding mechanisms of exposed organisms (5-9). A recently proposed approach for developing sediment quality criteria for nonionic organic contaminants is based on the assumption that biological availability is dependent on the chemical activity or fugacity of contaminants in pore waters and that this portion can be approximated using the organic carbon-normalized equilibrium partitioning coefficient, Koc (1, 2). This approach assumes that sedimentary organic matter has a fairly uniform binding capacity toward nonionic organic contaminants regardless of sediment source or biogeochemical history, that the system is at equilibrium, and that benthic organisms are primarily exposed through uptake of pore water contaminant residues. * Corresponding author e-mail:
[email protected].
S0013-936X(96)01005-X CCC: $14.00
1997 American Chemical Society
Researchers have noted a range in Koc and Kdoc (the equilibrium partitioning coefficient describing contaminant sorption by dissolved organic carbon) values relative to the chemical nature of both the contaminants and the sedimentary organic substrate, the latter assessed by factors such as elemental composition or aromaticity (e.g., refs 10-16). Because the bioavailability of contaminants has been linked in theory to their partitioning behavior, factors affecting partitioning would be expected to affect the extent of contaminant uptake by biota. Brannon et al. (17) measured fluoranthene and PCB bioaccumulation factors that ranged over an order of magnitude for clams in sediments with varying organic matter composition. Conversely, DeWitt et al. (18) measured less than 2-fold difference in fluoranthene toxicity, a measure of bioavailability, to amphipods exposed to sediments amended with organic matter ranging from fresh plant and fecal matter to relatively well-weathered mud and suspended sediments. This study was undertaken to determine the extent to which sediment composition played a role in the partitioning and bioavailability of dieldrin to Lumbriculus variegatus (oligochaeta) and whether measures of partitioning were predictive of the bioavailable pool of dieldrin, as determined from L. variegatus biota sediment accumulation factors.
Materials and Methods Sediments. Surface (e20 cm) sediments were collected from four stream sites that represented a range in organic carbon content, source, and extent of biogeochemical weathering. Sediments were collected from three sites in White Clay Creek (Chester County, PA), a Piedmont stream draining mixed deciduous forest and agriculture. These include low organic sandy sediments (WCC, foc 0.0036, organic carbon content, g of C/g of sediment), high organic wetland sediments (WTL, foc 0.0803), and sediments with a moderate organic carbon content (foc 0.0309) located below the outflow of a sewage treatment plant (STP). Sediments were also collected from a low-flow tributary of Broad Creek (Sussex County, DE) a coastal plain river draining pinelands (PLC, foc 0.0754). After sieving to 0.05). Bioaccumulation factors normalized to foc and lipids decreased between week and month preexposures for three of the four sediments; however, BSAF were higher in week than day preexposures for WCC and PLC sediments. Again, mean BSAF calculated for the four sediments were not significantly different for the three equilibration periods (p > 0.05). Because trends over time were not statistically significant, data from day, week, and month exposures were combined to compare the overall differences in bioaccumulation between the four sediments. One month may not have been sufficient time to appreciably alter the extent of incorporation of dieldrin into sediment matrices and thus reduce bioavailability of the residues. Future work will include longer preequilibration times. If equilibrium partitioning was the primary factor controlling bioavailability and partitioning was controlled simply by the amount of organic carbon present in sediments, normalization of bioaccumulation factors to foc and lipid content would have eliminated differences between sediments. However, as shown above, partitioning was dependent on sediment composition. Uptake capacity of organisms is also dependent on their lipid composition (30). Because experiments were confined to one taxon, differences in uptake in this experiment should primarily be related to variations in sediment composition and not biological factors such as feeding mechanisms or lipid composition. For the four sediments studied here, normalization of bioaccumulation factors to foc and lipid content reduced ranges in measured accumulation of dieldrin by L. variegatus from 38- to 8-fold between the four sediments (Figure 2 panel b versus panel a). Factors that might account for the remaining variability in bioaccumulation from the four sediments were investigated and included partition coefficients (Koc and Kdoc), growth rates of organisms, and measures of sediment composition such
FIGURE 5. Correlation coefficients (R 2) for sediment characteristics versus (a) log Koc and BSAF and (b) log Kdoc and BSAF. *Correlations significant at p < 0.05. Abbreviations: ewt, extract weight; foc, organic carbon content; ewt/C, organic carbon-normalized extract weight. as humic substance content, pH, particle size, and extract weight (i.e., % ewt and ewt/C). Sorptive “strength” of sedimentary organic matter might be predictive of whether organisms can successfully extract contaminant residues. However, BSAF did not correlate significantly with either log Koc or log Kdoc (r 2 ) 0.368 and 0.509, respectively, p > 0.05), although BSAF was inversely correlated with log Koc and positively correlated with log Kdoc, as would be expected if the former is a measure of increased sorption by sediments and the latter a measure of increased solubilization into a faster desorbing pool as discussed above. Thus, partition coefficients determined with the extraction techniques utilized during this study did not prove to be predictive of differences in biological extractability of contaminant residues. To determine whether dilution of residues from growth or unpalatability of sediments (and thus reduced growth, though no avoidance behavior was observed during the experiment) played a role in the accumulation of contaminants, BSAF was corrected for growth. This correction did not reduce the differences between BSAF values since oligochaetes grew at approximately the same rate in all experimental sediments (Figure 3). Sediment pH was also tested as a potential factor controlling the bioaccumulation of dieldrin. pH has been linked to
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changes in the tertiary structure of dissolved humic substances that may alter the latter’s capacity to partition nonpolar organics, typically resulting in a reduction of contaminant sorption as pH increases and humic substances swell. For example, Jota and Hasset (31) noted a decrease in Kdoc with increasing pH. Thus, by extension, pH should also affect the biological extractability of contaminant residues. BSAF and pH were inversely correlated in these sediments (Figure 4, r 2 ) 0.899, p < 0.05). At first glance, this is counterintuitive because increasing the pH swells organic substances such as humics and that should have reduced sorption of the contaminant and thus increased uptake by biota. However, two components that control the freelydissolved pool of contaminants in sediments (particulate and dissolved organic matter) were competing for contaminant residues. While, log Koc increased as pH increased in these sediments, the log Kdoc decreased, which was a result similar to that of Jota and Hassett (31). Thus, this may indicate that the DOC plays a greater role in determining the biological availability of contaminant residues than the POM. The effect of pH on bioavailability will have to be investigated further. Other factors were tested to determine their effect on bioavailability. These included % ewt, ewt/C, mean particle size, and humic and fulvic acid content; none of which correlated significantly with BSAF (r 2 ) 0.584, 0.591, 0.422, 0.815, and 0.585, respectively, p > 0.05). These factors may play a role, but clearly pH was the most powerful descriptor of sedimentary composition that played a role in biological extractability of dieldrin residues for L. variegatus. Sediment Composition versus Dieldrin Partitioning and Bioavailability. Sediment composition played a role in both the partitioning and bioavailability of dieldrin in the four sediments studied here. One would expect that factors altering partitioning behavior of contaminants would have a similar effect on the bioavailability of those contaminant residues. Factors that correlated positively with log Koc correlated inversely with BSAF (Figure 5a), as would be expected since increased sorption should reduce the bioavailable pool of contaminants. However, factors that were most strongly correlated to log Koc were not the same factors that correlated with bioavailability and vice versa (Figure 5a). The extract weight, which had the strongest effect on log Koc (although not at a significant level, p > 0.05) did not correlate as well with BSAF. And pH, which had the strongest effect on BSAF, had little effect on log Koc. This result indicated that chemical measures typically utilized for determining partitioning coefficients were not good indicators of biological extractability of contaminant residues. Similarly, sediment composition factors that correlated most strongly with log Kdoc (i.e., foc and ewt/C, Figure 5b) were different than the factor that correlated most strongly with BSAF (i.e., pH). Factors correlated with log Kdoc and BSAF were either both positive or negative (Figure 5b), a trend that supports the hypothesis that contaminant binding by DOC increased the bioavailable pool by solubilizing residues into faster desorbing compartments. These results imply that the prediction of biological responses from chemical measures of bioavailability must be approached with caution and that current chemical measures of partitioning do not accurately reflect biological extractability, at least in regard to bioaccumulation by sediment processing organisms such as L. variegatus. Research has shown that bioavailability is reduced before chemical extractability (32). Other researchers are investigating alternate chemical measures of quantifying “biologically” extractable residues such as extracting sediments using invertebrate digestive fluids (9) and relating bioaccumulation to the kinetics of desorption (4). Ultimately, the bioavailable pool of contaminant residues is highly dependant on feeding mechanisms of organisms (5-9), interactions between species
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(33), and organism density (20) and may be more accurately modeled by accounting for feeding preferences, assimilation efficiencies, and the relative fugacities of contaminants in prey and environmental compartments (34, 35).
Acknowledgments I thank the Environmental Associates of the Academy of Natural Sciences and Pennswood Number 2 Research Fund for supporting this research. I also thank Drs. Thomas Bott and Louis Kaplan (Stroud Center) and Drs. Susan Hendricks and David White (Murray State University) for helpful suggestions and John Henderson for excellent technical support. I also thank a couple of anonymous reviewers for astute and helpful suggestions. This work was presented in part at the 16th Annual Meeting of the Society of Environmental Toxicology and Chemistry, Washington, DC.
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Received for review December 4, 1996. Revised manuscript received May 9, 1997. Accepted May 19, 1997.X ES961005S X
Abstract published in Advance ACS Abstracts, July 15, 1997.
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