Explaining differences between bioaccumulation measurements in laboratory and field data through use of a probabilistic modeling approach

In the regulatory context, bioaccumulation assessment is often hampered by substantial data uncertainty as well as by the poorly understood differences often observed between results from laboratory and field bioaccumulation studies. Bioaccumulation is a complex, multifaceted process, which calls for accurate error analysis. Yet, attempts to quantify and compare propagation of error in bioaccumulation metrics across species and chemicals are rare. Here, we quantitatively assessed the combined influence of physicochemical, physiological, ecological, and environmental parameters known to affect bioaccumulation for 4 species and 2 chemicals, to assess whether uncertainty in these factors can explain the observed differences among laboratory and field studies. The organisms evaluated in simulations including mayfly larvae, deposit‐feeding polychaetes, yellow perch, and little owl represented a range of ecological conditions and biotransformation capacity. The chemicals, pyrene and the polychlorinated biphenyl congener PCB‐153, represented medium and highly hydrophobic chemicals with different susceptibilities to biotransformation. An existing state of the art probabilistic bioaccumulation model was improved by accounting for bioavailability and absorption efficiency limitations, due to the presence of black carbon in sediment, and was used for probabilistic modeling of variability and propagation of error. Results showed that at lower trophic levels (mayfly and polychaete), variability in bioaccumulation was mainly driven by sediment exposure, sediment composition and chemical partitioning to sediment components, which was in turn dominated by the influence of black carbon. At higher trophic levels (yellow perch and the little owl), food web structure (i.e., diet composition and abundance) and chemical concentration in the diet became more important particularly for the most persistent compound, PCB‐153. These results suggest that variation in bioaccumulation assessment is reduced most by improved identification of food sources as well as by accounting for the chemical bioavailability in food components. Improvements in the accuracy of aqueous exposure appear to be less relevant when applied to moderate to highly hydrophobic compounds, because this route contributes only marginally to total uptake. The determination of chemical bioavailability and the increase in understanding and qualifying the role of sediment components (black carbon, labile organic matter, and the like) on chemical absorption efficiencies has been identified as a key next steps. Integr Environ Assess Manag 2012;8:42–63. © 2011 SETAC

[1]  L. Looper,et al.  Stockholm Convention on Persistent Organic Pollutants , 2020, Essential Concepts of Global Environmental Governance.

[2]  Cathy L. Schott,et al.  Experimental Results , 2009 .

[3]  R. W. Kapp,et al.  Toxic Substances Control Act , 2014 .

[4]  Thomas F Parkerton,et al.  Comparing laboratory and field measured bioaccumulation endpoints , 2012, Integrated environmental assessment and management.

[5]  Ad M J Ragas,et al.  Parameter uncertainty in modeling bioaccumulation factors of fish , 2011, Environmental toxicology and chemistry.

[6]  M. Croteau,et al.  Measurement and modeling of polychlorinated biphenyl bioaccumulation from sediment for the marine polychaete Neanthes arenaceodentata and response to sorbent amendment. , 2010, Environmental science & technology.

[7]  J. Middelburg,et al.  Uncertainties in ecological, chemical and physiological parameters of a bioaccumulation model: implications for internal concentrations and tissue based risk quotients. , 2010, Ecotoxicology and environmental safety.

[8]  D. Cassin,et al.  Is the polychaete, Perinereis rullieri (Pilato 1974), a reliable indicator of PCB and PAH contaminants in coastal sediments? , 2010, Ecotoxicology and environmental safety.

[9]  K. Drouillard,et al.  The influence of diet on the assimilation efficiency of 47 polychlorinated biphenyl congeners in Japanese koi (Cyprinus carpio) , 2010, Environmental toxicology and chemistry.

[10]  K. Drouillard,et al.  Steady and non-steady state kinetics describe polychlorinated biphenyl bioaccumulation in natural populations of bluegill (Lepomis macrochirus) and cisco (Coregonus artedi) , 2009 .

[11]  A. Koelmans,et al.  Triple domain in situ sorption modeling of organochlorine pesticides, polychlorobiphenyls, polyaromatic hydrocarbons, polychlorinated dibenzo-p-dioxins, and polychlorinated dibenzofurans in aquatic sediments. , 2009, Environmental science & technology.

[12]  Frank A. P. C. Gobas,et al.  Revisiting Bioaccumulation Criteria for POPs and PBT Assessments , 2009, Integrated environmental assessment and management.

[13]  Albert A Koelmans,et al.  Evaluation of Bioaccumulation Using In Vivo Laboratory and Field Studies , 2009, Integrated environmental assessment and management.

[14]  S. Luoma,et al.  Emerging opportunities in management of selenium contamination. , 2009, Environmental science & technology.

[15]  Marco Ratto,et al.  Global uncertainty and sensitivity analysis of a food‐web bioaccumulation model , 2009, Environmental toxicology and chemistry.

[16]  K. Drouillard,et al.  A combined food web toxicokinetic and species bioenergetic model for predicting seasonal PCB elimination by yellow perch (Perca flavescens). , 2009, Environmental science & technology.

[17]  A. Koelmans,et al.  Quantification methods of Black Carbon: comparison of Rock-Eval analysis with traditional methods. , 2009, Journal of chromatography. A.

[18]  Mark Bonnell,et al.  Bioaccumulation Assessment Using Predictive Approaches , 2009, Integrated environmental assessment and management.

[19]  Wen-Xiong Wang,et al.  Comparative approaches to understand metal bioaccumulation in aquatic animals. , 2008, Comparative biochemistry and physiology. Toxicology & pharmacology : CBP.

[20]  W. Fisher,et al.  Ontogenetic and Seasonal Diet Shifts of Smallmouth Bass in an Ozark Stream , 2008 .

[21]  L. Rasmussen,et al.  Biotransformation of polycyclic aromatic hydrocarbons in marine polychaetes. , 2008, Marine environmental research.

[22]  S. Hawthorne,et al.  Measured partition coefficients for parent and alkyl polycyclic aromatic hydrocarbons in 114 historically contaminated sediments: Part 2. Testing the KOCKBC two carbon–type model , 2007, Environmental toxicology and chemistry.

[23]  I. Roessink,et al.  Modeling decreased food chain accumulation of PAHs due to strong sorption to carbonaceous materials and metabolic transformation. , 2007, Environmental science & technology.

[24]  Albert A Koelmans,et al.  Including sorption to black carbon in modeling bioaccumulation of polycyclic aromatic hydrocarbons: uncertainty analysis and comparison to field data. , 2007, Environmental science & technology.

[25]  K. Drouillard,et al.  PCB elimination by yellow perch (Perca flavescens) during an annual temperature cycle. , 2007, Environmental science & technology.

[26]  T. O. Said,et al.  The Distribution and Sources of Polycyclic Aromatic Hydrocarbons in Surface Sediments Along the Egyptian Mediterranean Coast , 2007, Environmental monitoring and assessment.

[27]  Frank A. P. C. Gobas,et al.  A review of bioconcentration factor (BCF) and bioaccumulation factor (BAF) assessments for organic chemicals in aquatic organisms , 2006 .

[28]  Albert A Koelmans,et al.  Black carbon: the reverse of its dark side. , 2006, Chemosphere.

[29]  M. Granberg,et al.  Role of sediment organic matter quality and feeding history in dietary absorption and accumulation of pyrene in the mud snail (Hydrobia ulvae) , 2006, Environmental Toxicology and Chemistry.

[30]  K. Drouillard,et al.  Quantifying resource partitioning in centrarchids with stable isotope analysis , 2006 .

[31]  M. U. Beg,et al.  Spatial Distribution of Polychlorinated Biphenyls in Coastal Marine Sediments Receiving Industrial Effluents in Kuwait , 2006, Archives of environmental contamination and toxicology.

[32]  F. Gobas,et al.  A bioenergetic biomagnification model for the animal kingdom. , 2006, Environmental science & technology.

[33]  J. Trygg,et al.  A statistical resampling method to calculate biomagnification factors exemplified with organochlorine data from herring (Clupea harengus) muscle and guillemot (Uria aalge) egg from the Baltic sea. , 2005, Environmental science & technology.

[34]  A. Koelmans,et al.  Extensive sorption of organic compounds to black carbon, coal, and kerogen in sediments and soils: mechanisms and consequences for distribution, bioaccumulation, and biodegradation. , 2005, Environmental science & technology.

[35]  K. Hylland,et al.  Experimental results on bioaccumulation of metals and organic contaminants from marine sediments. , 2005, Aquatic toxicology.

[36]  A. Koelmans,et al.  Black carbon and ecological factors affect in situ biota to sediment accumulation factors for hydrophobic organic compounds in flood plain lakes. , 2005, Environmental science & technology.

[37]  Samuel N Luoma,et al.  Why is metal bioaccumulation so variable? Biodynamics as a unifying concept. , 2005, Environmental science & technology.

[38]  Ian M. Voparil,et al.  Digestive bioavailability to a deposit feeder (Arenicola marina) of polycyclic aromatic hydrocarbons associated with anthropogenic particles , 2004, Environmental toxicology and chemistry.

[39]  R. Delahay,et al.  The diet of Little Owls Athene noctua in Gloucestershire, England , 2004 .

[40]  S. Pflugmacher,et al.  Uptake and Effects on Detoxication Enzymes of Cypermethrin in Embryos and Tadpoles of Amphibians , 2004, Archives of environmental contamination and toxicology.

[41]  Jon A Arnot,et al.  A food web bioaccumulation model for organic chemicals in aquatic ecosystems , 2004, Environmental toxicology and chemistry.

[42]  A. Fisk,et al.  Biological and chemical factors of importance in the bioaccumulation and trophic transfer of persistent organochlorine contaminants in arctic marine food webs , 2004, Environmental toxicology and chemistry.

[43]  R. Luthy,et al.  Effects of particulate carbonaceous matter on the bioavailability of benzo[a]pyrene and 2,2',5,5'-tetrachlorobiphenyl to the clam, Macoma balthica. , 2004, Environmental science & technology.

[44]  Ian M. Voparil,et al.  Commercially available chemicals that mimic a deposit feeder's (Arenicola marina) digestive solubilization of lipids. , 2004, Environmental science & technology.

[45]  C. Field,et al.  QUANTITATIVE FATTY ACID SIGNATURE ANALYSIS: A NEW METHOD OF ESTIMATING PREDATOR DIETS , 2004 .

[46]  F. Whiteman,et al.  A physiologically based toxicokinetic model for dietary uptake of hydrophobic organic compounds by fish: II. simulation of chronic exposure scenarios. , 2004, Toxicological sciences : an official journal of the Society of Toxicology.

[47]  S. Wanless,et al.  Self-feeding and chick provisioning diet differ in the common guillemot Uria aalge , 2004 .

[48]  V. Forbes,et al.  Uptake, depuration, and toxicity of dissolved and sediment‐bound fluoranthene in the polychaete, Capitella sp. I , 2003, Environmental toxicology and chemistry.

[49]  V. Forbes,et al.  Biotransformation of dissolved and sediment‐bound fluoranthene in the polychaete, Capitella sp. I , 2003, Environmental toxicology and chemistry.

[50]  A. Fisk,et al.  Trophic transfer of persistent organochlorine contaminants (OCs) within an Arctic marine food web from the southern Beaufort-Chukchi Seas. , 2003, Environmental pollution.

[51]  A. Bosveld,et al.  Ecotoxicological suitability of floodplain habitats in The Netherlands for the little owl (Athene noctua vidalli). , 2003, Environmental pollution.

[52]  P. Wilkinson,et al.  Assessing Trends in Organochlorine Concentrations in Lake Winnipeg Fish Following the 1997 Red River Flood , 2003 .

[53]  K. Drouillard,et al.  The Influence of Diet Properties and Feeding Rates on PCB Toxicokinetics in the Ring Dove , 2003, Archives of environmental contamination and toxicology.

[54]  R. Connolly,et al.  Sulfur stable isotopes separate producers in marine food-web analysis , 2003, Oecologia.

[55]  L. L. Goldman,et al.  Crystal Ball Professional introductory tutorial , 2002, Proceedings of the Winter Simulation Conference.

[56]  Lawrence I. Goldman Crystal ball software tutorial: crystal ball professional introductory tutorial , 2002, WSC '02.

[57]  A. Koelmans,et al.  Sorption of polycyclic aromatic hydrocarbons and polychlorinated biphenyls to soot and soot-like materials in the aqueous environment: mechanistic considerations. , 2002, Environmental science & technology.

[58]  W. Bowen,et al.  Among- and within-species variability in fatty acid signatures of marine fish and invertebrates on the Scotian Shelf, Georges Bank, and southern Gulf of St. Lawrence , 2002 .

[59]  D. Post USING STABLE ISOTOPES TO ESTIMATE TROPHIC POSITION: MODELS, METHODS, AND ASSUMPTIONS , 2002 .

[60]  P. Gschwend,et al.  Assessing the combined roles of natural organic matter and black carbon as sorbents in sediments. , 2002, Environmental science & technology.

[61]  D. Bird,et al.  Bioaccumulation and toxicokinetics of 42 polychlorinated biphenyl congeners in American kestrels (Falco sparverius) , 2001, Environmental toxicology and chemistry.

[62]  F. Mehlum CRUSTACEANS IN THE DIET OF ADULT COMMON AND BRÜNNICH'S GUILLEMOTS URIA AALGE AND U. LOMVIA IN THE BARENTS SEA DURING THE BREEDING PERIOD , 2001 .

[63]  K. Weber,et al.  Species-specific elimination of polychlorinated biphenyls in estuarine animals and its impact on residue patterns. , 2001, Marine environmental research.

[64]  Jan-Willem Wegener,et al.  Ecotoxicologisch onderzoek naar effecten van verontreinigingen in uiterwaarden op steenuilen (Athene noctua): een integratie , 2001 .

[65]  S. Sheppard Handbook of Property Estimation Methods for Chemicals, Environmental and Health Sciences , 2001 .

[66]  S. Gewurtz,et al.  Comparison of polycyclic aromatic hydrocarbon and polychlorinated biphenyl dynamics in benthic invertebrates of Lake Erie, USA , 2000 .

[67]  T. Crommentuijn,et al.  Environmental risk limits for polychlorinated biphenyls in the Netherlands: Derivation with probabilistic food chain modeling , 2000 .

[68]  N. Collins,et al.  Annual cycle of energy allocation to growth and reproduction of yellow perch , 2000 .

[69]  Frank A. P. C. Gobas,et al.  Bioconcentration and Biomagnification in the Aquatic Environment , 2000 .

[70]  N. Fisher,et al.  Assimilation efficiencies of chemical contaminants in aquatic invertebrates: A synthesis , 1999 .

[71]  R. Rosenberg,et al.  Influence of sediment‐organic matter quality on growth and polychlorobiphenyl bioavailability in Echinodermata (Amphiura filiformis) , 1999 .

[72]  M. Hillebrand,et al.  The use of microsomal in vitro assay to study phase I biotransformation of chlorobornanes (Toxaphene) in marine mammals and birds. Possible consequences of biotransformation for bioaccumulation and genotoxicity. , 1998, Comparative biochemistry and physiology. Part C, Pharmacology, toxicology & endocrinology.

[73]  C. Metcalfe,et al.  Chemical accumulation and toxicological stress in three brown bullhead (Ameiurus nebulosus) populations of the Detroit River, Michigan, USA , 1998 .

[74]  Aaron T. Fisk,et al.  Dietary accumulation and depuration of hydrophobic organochlorines: Bioaccumulation parameters and their relationship with the octanol/water partition coefficient , 1998 .

[75]  S. Chipps Temperature-dependent consumption and gut-residence time in the opossum shrimp Mysis relicta , 1998 .

[76]  Frank A. P. C. Gobas,et al.  Development and Verification of a Benthic/Pelagic Food Web Bioaccumulation Model for PCB Congeners in Western Lake Erie , 1997 .

[77]  J. Ciborowski,et al.  The Distribution and Contaminant Burdens of Adults of the Burrowing Mayfly, Hexagenia, in Lake Erie , 1997 .

[78]  F. Law,et al.  Toxicokinetics of waterborne pyrene in rainbow trout (Oncorhynchus mykiss) following branchial or dermal exposure , 1996 .

[79]  A. Mcelroy,et al.  Bioaccumulation and metabolism of benzo[A]pyrene in three species of polychaete worms , 1996 .

[80]  O. Donard,et al.  Bioavailability of Sedimentary Contaminants Subject to Deposit-Feeder Digestion , 1996 .

[81]  J. Ciborowski,et al.  Estimation of the Uptake of Organochlorines by the Mayfly Hexagenia limbata (Ephemeroptera: Ephemeridae) , 1996 .

[82]  A. Hendriks,et al.  Modelling non-equilibrium concentrations of microcontaminants in organisms: comparative kinetics as a function of species size and octanol-water partitioning. , 1995, Chemosphere.

[83]  Frank A. P. C. Gobas,et al.  A model for predicting the bioaccumulation of hydrophobic organic chemicals in aquatic food-webs: application to Lake Ontario , 1993 .

[84]  P. Magnan,et al.  Variation saisonnière dans la répartition des ressources alimentaires entre cinq espèces de poissons en fonction de la disponibilité des proies , 1992 .

[85]  R. Oremland,et al.  Determination of selenium bioavailability to a benthic bivalve from particulate and solute pathways , 1992 .

[86]  E. Korpimäki,et al.  Numerical and Functional Responses of Kestrels, Short‐Eared Owls, and Long‐Eared Owls to Vole Densities , 1991 .

[87]  J. Hutson Modelling in Ecotoxicology (Developments in Environmental Modelling 16) , 1991 .

[88]  Mace G. Barron,et al.  Bioconcentration. Will water-borne organic chemicals accumulate in aquatic animals? , 1990 .

[89]  Frank A. P. C. Gobas,et al.  Model of Organic Chemical Uptake and Clearance by Fish from Food and Water , 1990 .

[90]  by,et al.  Chapter 2 - Modelling Concepts , 1990 .

[91]  F. Gobas,et al.  Bioaccumulation of chlorinated hydrocarbons by the mayfly (Hexagenia limbata) in Lake St. Clair , 1989 .

[92]  V. Forbes,et al.  Time‐Dependent Absorption in Deposit Feeders , 1989 .

[93]  W. Hayton,et al.  Detection of pentachlorophenol and its glucuronide and sulfate conjugates in fish bile and exposure water. , 1988, Journal of environmental science and health. Part. B, Pesticides, food contaminants, and agricultural wastes.

[94]  P. Landrum,et al.  Toxicokinetics of Selected Xenobiotics in Hexagenia Limbata , 1988 .

[95]  J. Levinton,et al.  Ecology of Deposit-Feeding Animals in Marine Sediments , 1987, The Quarterly Review of Biology.

[96]  Frank A. P. C. Gobas,et al.  Dynamics of hydrophobic organic chemical bioconcentration in fish , 1987 .

[97]  R. Norstrom,et al.  Dynamics of organochlorine compounds in herring gulls (Larus argentatus). II: A two-compartment model and data for ten compounds , 1987 .

[98]  B. Peterson,et al.  STABLE ISOTOPES IN ECOSYSTEM STUDIES , 1987 .

[99]  J. Connolly,et al.  Model of PCB in the Lake Michigan lake trout food chain. , 1984, Environmental science & technology.

[100]  J. Flannagan An Introduction to the Aquatic Insects of North America. , 1979 .