Environ. Sci. Technol. 2003, 37, 3926-3934
Bioavailability of Sediment-Associated PCDD/Fs and PCDEs: Relative Importance of Contaminant and Sediment Characteristics and Biological Factors M E R J A L Y Y T I K A¨ I N E N , * , † P I P S A H I R V A , ‡ PENTTI MINKKINEN,§ H E I K K I H A¨ M A¨ L A¨ I N E N , | ANNA-LEA RANTALAINEN,⊥ PIRJO MIKKELSON,# JAAKKO PAASIVIRTA,# AND JUSSI V. K. KUKKONEN† Departments of Biology, Chemistry, and Ecology, University of Joensuu, P.O. Box 111, FIN-80101 Joensuu, Finland, Department of Chemical Technology, Lappeenranta University of Technology, P.O. Box 20, FIN-53851 Lappeenranta, Finland, Department of Ecological and Environmental Sciences, University of Helsinki, Niemenkatu 73, FIN-15140 Lahti, Finland, and Department of Chemistry, University of Jyva¨skyla¨, P.O. Box 35, FIN-40351 Jyva¨skyla¨, Finland
Factors that determine accumulation of sediment-associated polychlorinated dibenzo-p-dioxins and furans and polychlorinated diphenyl ethers into semipermeable membrane devices (SPMDs) and benthic oligochaete worms (Lumbriculus variegatus) were examined. These factors included both physical-chemical and structural characteristics of the contaminants (water solubility, lipophilicity, dipole moment, molecular size, and conformation) and sediment characteristics (organic carbon content, particle size, aromaticity, and polarity of organic carbon). The results of partial least squares regression analysis indicated that lipophilicity alone is not a sufficient predictor for contaminant bioaccumulation potential, even though it is a significant contributor. It was shown that contaminant molecular size and conformation (specifically planarity/ nonplanarity) as well as sediment characteristics also have a significant role. The studied factors contributed up to 6388% of the variation in accumulation data for SPMDs and 50-65% for oligochaetes. Comparison of (bio)accumulation factors (BAF28d for oligochaetes and AF28d for SPMDs) revealed that accumulation of contaminants in oligochaetes is largely influenced by biological factors (e.g., feeding habits), while the physical-chemical nature of the process is emphasized for SPMDs. * Corresponding author telephone: +358-13-2513853; fax: +35813-2513890; e-mail:
[email protected]. † Department of Biology, University of Joensuu. ‡ Department of Chemistry, University of Joensuu. § Lappeenranta University of Technology. | Department of Ecology, University of Joensuu. ⊥ University of Helsinki. # University of Jyva ¨ skyla¨. 3926
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ENVIRONMENTAL SCIENCE & TECHNOLOGY / VOL. 37, NO. 17, 2003
Introduction Bioaccumulation can be described as a series of consecutive partitioning processes between different compartments of the environment. A sediment-associated contaminant desorbs from sediment into pore water, diffuses through the water phase, and finally transfers through the membrane(s) into the organism. According to equilibrium partitioning theory, the tendency toward the equal chemical activities in each environmental compartment drives these partitioning processes (1). In sediment exposures, it is commonly assumed that any neutral organic contaminant partitions according to its lipophilicity between the organism lipids and the sediment organic carbon (2). Validity of this equilibrium partitioning approach (EqP) has been evident in some studies (e.g., ref 2), but in many cases such an assumption is an oversimplification. The EqP approach neglects the impact of other characteristics of contaminants, environmental conditions, and organism biological characteristics on the partitioning process. For sediment-associated contaminants, the quantity, the chemical structure of sediment organic matter (functional groups, aromaticity, etc.), and the surface area of sediment organic matter (particle size distribution) are effective environmental characters (3-5). They influence the type, strength, and number of bonds that are formed between the sediment and the contaminant. The quality and origin of organic matter are important as well. For example, highly conjugated and condensed anthropogenic carbon (black carbon) has been found to sorb contaminants, especially planar ones, more efficiently than natural organic carbon (6, 7). Together these factors determine how easily sediment-associated contaminants desorb from sediment and become available to organisms. Once desorbed, the contaminant transfers through the water phase to the organisms and penetrates through the hydrophobic and hydrophilic layers of cell membrane(s) if steric and chemical properties of the contaminant and the structure of the cell membrane allow it (8). In the process, energy is needed for the forming of a cavity in membrane in which the contaminant fits. This means that interaction between membrane molecules must be overcome and that interactions between membrane and contaminant must be formed (9). Molecular size along with electrochemical characteristics of both contaminant and membrane (e.g., distribution of electronic charge) affect the thermodynamic energy required for reorganizing the interactions (9-11). Finally, behavior (e.g., feeding habits, avoidance) and physiology of the organism (e.g., condition, assimilation, and biotransformation capacity) affect the magnitude of the exposure the organism faces and the amount of contaminant that actually accumulates. Thus, the combination of chemical, environmental, and biological factors ultimately determines the bioavailability and bioaccumulation of the toxicants. Knowledge about the relative importance of each factor is essential for making more accurate risk assessments. This study focuses on bioaccumulation of sedimentassociated polychlorinated dibenzo-p-dioxins and furans (PCDD/Fs) and polychlorinated diphenyl ethers (PCDEs). PCDD/Fs and PCDEs are superlipophilic compounds with comparable octanol-water partition coefficients (Kow) and molecular weights (MW) (12). PCDD/Fs are planar compounds, while PCDEs pose sterically bulky structure (Figure 1). Trace concentrations of both PCDD/Fs and PCDEs have been detected in environmental samples all over the world, including the most remote areas in the Arctic and Antarctica (13-18). Wide distribution, high lipophilicity, and persistence of these compounds have raised concern about their bio10.1021/es034151o CCC: $25.00
2003 American Chemical Society Published on Web 08/05/2003
degree of exposure. The objectives of the study were (i) to determine the importance of various contaminant and sediment properties on bioaccumulation and (ii) to estimate the relative importance of biological factors on bioaccumulation by comparing the accumulation patterns of oligochaetes and SPMDs.
Experimental Section
FIGURE 1. Computationally optimized conformation of (a) 1,2,3,4,6,8HxCDF and (b) 2,2′,4,4′,5,6′-HxCDE (PCDE-154). The dimensions of the molecule were determined as illustrated in the figure. W, width; L, length; and H, height. accumulation, their potential biomagnification in the food webs, and their adverse effects. Factors affecting bioaccumulation of PCDD/Fs have been studied intensively, focusing mainly on fish and mammals (19-21), but comparable studies on PCDEs are lacking. The existing studies on PCDD/ Fs concentrate on contaminant characteristics and diets, while impacts of environmental and biological factors on bioaccumulation are mainly ignored. In the present study, the oligochaete worm Lumbriculus variegatus was used as a test organism. It dwells in sediment and is thus truly exposed to sediment-associated contaminants via several routes (integument and intestine). For comparison, semipermeable membrane devices (SPMDs) that were buried in sediments were used as surrogates for test organisms. SPMDs accumulate only truly dissolved chemicals being true representatives for passive uptake mechanisms, which are controlled solely by physicalchemical factors (22). The uptake rate in immobile SPMDs is basically controlled by the sum resistance of the compound to diffuse through the water phase and to transfer through the membrane (22). When deployed in sediment, resistance of compound to desorb from sediment becomes important (23, 24). For superlipophilic compounds, the impacts of desorption and water resistances are highlighted but increasing steric dimensions may also become restricting factor in membrane transfer (24, 25). Basically, the same factors influence the uptake in oligochaetes, but their relative importance may be affected by biological factors, such as burrowing and feeding activity. These factors may alter contaminant desorption, length of diffusion path, and thus
Sediments and Chemical Analyses. The test sediments were collected from 10 sites (labeled KJ0-KJ9) in the vicinity of an old chlorophenol production plant, in River Kymijoki, Southeast Finland. The analyses of PCDD/Fs and PCDEs from sediments, tissues, and SPMDs were performed as described by Lyytika¨inen et al. (26). Polychlorinated dibenzo-p-dioxin and furan congeners included in this study were 2,3,7,8TeCDF, 1,2,3,4,6,8-HxCDF, 1,2,4,6,7,8-HxCDF, 1,2,4,6,8,9HxCDF, 1,2,3,4,6,7,8-HpCDF, 1,2,3,4,6,8,9-HpCDF, OCDF, 1,2,3,4,7,8-HxCDD, and 1,2,3,4,6,7,8-HpCDD. Polychlorinated diphenyl ether congeners 99, 100, 138, 153, 154, 163, 167, 180, 182, 184, 196, 197, 203. and 204 were also included. These congeners were abundantly present in test sediments. Sediments were characterized for the organic carbon, nitrogen, and hydrogen content and a proportion of the finest (
