Why is metal bioaccumulation so variable? Biodynamics as a unifying concept.

Ecological risks from metal contaminants are difficult to document because responses differ among species, threats differ among metals, and environmental influences are complex. Unifying concepts are needed to bettertie together such complexities. Here we suggest that a biologically based conceptualization, the biodynamic model, provides the necessary unification for a key aspect in risk: metal bioaccumulation (internal exposure). The model is mechanistically based, but empirically considers geochemical influences, biological differences, and differences among metals. Forecasts from the model agree closely with observations from nature, validating its basic assumptions. The biodynamic metal bioaccumulation model combines targeted, high-quality geochemical analyses from a site of interestwith parametrization of key physiological constants for a species from that site. The physiological parameters include metal influx rates from water, influx rates from food, rate constants of loss, and growth rates (when high). We compiled results from 15 publications that forecast species-specific bioaccumulation, and compare the forecasts to bioaccumulation data from the field. These data consider concentrations that cover 7 orders of magnitude. They include 7 metals and 14 species of animals from 3 phyla and 11 marine, estuarine, and freshwater environments. The coefficient of determination (R2) between forecasts and independently observed bioaccumulation from the field was 0.98. Most forecasts agreed with observations within 2-fold. The agreement suggests that the basic assumptions of the biodynamic model are tenable. A unified explanation of metal bioaccumulation sets the stage for a realistic understanding of toxicity and ecological effects of metals in nature.

[1]  G. Cutter The estuarine behaviour of selenium in San Francisco Bay , 1989 .

[2]  N. Fisher,et al.  Delineating metal accumulation pathways for marine invertebrates , 1999 .

[3]  N. Fisher,et al.  Field Testing a Metal Bioaccumulation Model for Zebra Mussels , 2000 .

[4]  S. Luoma The dynamics of biologically available mercury in a small estuary , 1977 .

[5]  Byeong‐gweon Lee,et al.  Influence of microalgal biomass on absorption efficiency of Cd, Cr, and Zn by two bivalves from San Francisco Bay , 1998 .

[6]  S. Luoma,et al.  Linking metal bioaccumulation of aquatic insects to their distribution patterns in a mining‐impacted river , 2004, Environmental toxicology and chemistry.

[7]  S. Luoma,et al.  Influences of dietary uptake and reactive sulfides on metal bioavailability from aquatic sediments. , 2000, Science.

[8]  M. Depledge,et al.  MODELS OF REGULATION AND ACCUMULATION OF TRACE METALS IN MARINE INVERTEBRATES , 1990 .

[9]  N. Cutshall Turnover of zinc-65 in oysters. , 1974, Health physics.

[10]  Wen-Xiong Wang,et al.  Comparative assimilation of Cd, Cr, Se, and Zn by the barnacle Elminius modestus from phytoplankton and zooplankton diets , 2001 .

[11]  Wen-Xiong Wang,et al.  Interactions of trace metals and different marine food chains , 2002 .

[12]  P. Chapman,et al.  Evaluation of bioaccumulation factors in regulating metals , 1996 .

[13]  M. Croteau,et al.  Differences in Cd accumulation among species of the lake-dwelling biomonitor Chaoborus , 2001 .

[14]  S. Luoma,et al.  Uptake and loss kinetics of Cd, Cr and Zn in the bivalves Potamocorbula amurensis and Macoma balthica: effects of size and salinity , 1998 .

[15]  P. Rainbow,et al.  Barnacles as biomonitors of trace metal availabilities in Hong Kong coastal waters: changes in space and time. , 2001, Marine environmental research.

[16]  N. Fisher,et al.  Sublethal effects of silver in zooplankton: Importance of exposure pathways and implications for toxicity testing , 2001, Environmental toxicology and chemistry.

[17]  Wen-Xiong Wang,et al.  Uptake and efflux of Cd and Zn by the green mussel Perna viridis after metal preexposure. , 2002, Environmental science & technology.

[18]  T. O’Connor Trends in chemical concentrations in mussels and oysters collected along the US coast from 1986 to 1993 , 1996 .

[19]  Wen-Xiong Wang,et al.  Effects of previous field-exposure history on the uptake of trace metals from water and food by the barnacle Balanus amphitrite , 2003 .

[20]  M. Croteau,et al.  Stable metal isotopes reveal copper accumulation and loss dynamics in the freshwater bivalve Corbicula. , 2004, Environmental science & technology.

[21]  P. Qian,et al.  The trophic transfer of Cd, Cr, and Se in the barnacle Balanus amphitrite from planktonic food , 1999 .

[22]  S. Luoma,et al.  Dietary Metals Exposure and Toxicity to Aquatic Organisms: Implications for Ecological Risk Asses... , 2001 .

[23]  N. Fisher,et al.  Bioavailability of Cr(III) and Cr(VI) to marine mussels from solute and particulate pathways , 1997 .

[24]  J. Reinfelder,et al.  Trace element trophic transfer in aquatic organisms: a critique of the kinetic model approach. , 1998, The Science of the total environment.

[25]  M. Croteau,et al.  Feeding patterns of migratory and non-migratory fourth instar larvae of two coexisting Chaoborus species in an acidic and metal contaminated lake: Importance of prey ingestion rate in predicting metal bioaccumulation , 2003 .

[26]  S. Fowler,et al.  Flux of cadmium through euphausiids , 1974 .

[27]  S. Luoma,et al.  Modeling selenium bioaccumulation through arthropod food webs in San Francisco Bay, California, USA , 2004, Environmental toxicology and chemistry.

[28]  S. Luoma,et al.  A statistical study of environmental factors controlling concentrations of heavy metals in the burrowing bivalve Scrobicularia plana and the polychaete Nereis diversicolor , 1982 .

[29]  Jr.,et al.  On the reactivity of metals for marine phytoplankton , 2000 .

[30]  W. Butte,et al.  Validation of estuarine gammarid collectives (Amphipoda: Crustacea) as biomonitors for cadmium in semi-controlled toxicokinetic flow-through experiments. , 1995, Environmental pollution.

[31]  P. Rainbow,et al.  The composition of pyrophosphate heavy metal detoxification granules in barnacles , 1991 .

[32]  Wen-Xiong Wang,et al.  Assimilation of cadmium, chromium, and zinc by the green mussel Perna viridis and the clam Ruditapes philippinarum , 2000 .

[33]  P. Campbel Interactions between trace metals and aquatic organisms : A critique of the Free-ion Activity Model , 1995 .

[34]  Don Mackay,et al.  Finding fugacity feasible, fruitful, and fun , 2004, Environmental toxicology and chemistry.

[35]  Beate I Escher,et al.  Internal exposure: linking bioavailability to effects. , 2004, Environmental science & technology.

[36]  J. Reinfelder,et al.  The Assimilation of Elements Ingested by Marine Copepods , 1991, Science.

[37]  A. Flegal,et al.  Decadal trends of silver and lead contamination in San Francisco Bay surface waters. , 2002, Environmental science & technology.

[38]  M. Lydy,et al.  Toxicokinetics in aquatic systems: Model comparisons and use in hazard assessment , 1992 .

[39]  I. N. Sneddon,et al.  The Mathematical Approach to Physiological Problems , 1972, The Mathematical Gazette.

[40]  S. Luoma Physiological characteristics of mercury uptake by two estuarine species , 1977 .

[41]  M. Vijver,et al.  Internal metal sequestration and its ecotoxicological relevance: a review. , 2004, Environmental science & technology.

[42]  Wen-Xiong Wang,et al.  Dietary uptake of Cd, Cr, and Zn by the barnacle Balanus trigonus: influence of diet composition , 2000 .

[43]  I. Ni,et al.  Transfer of Cd, Cr and Zn from zooplankton prey to mudskipper Periophthalmus cantonensis and glassy Ambassis urotaenia fishes , 2000 .

[44]  D Mackay,et al.  Correlation of bioconcentration factors. , 1982, Environmental science & technology.

[45]  J. Teyssie,et al.  Trace metals in marine copepods: a field test of a bioaccumulation model coupled to laboratory uptake kinetics data , 2000 .

[46]  S. Luoma,et al.  Kinetic determinations of trace element bioaccumulation in the mussel, Mytilus edulis , 1996 .

[47]  P. Burkhardt-Holm,et al.  Challenges in ecotoxicology. , 2004, Environmental science & technology.

[48]  W. Sunda The relationship between cupric ion activity and the toxicity of copper to phytoplankton , 1975 .

[49]  G. Ankley,et al.  Acid‐volatile sulfide as a factor mediating cadmium and nickel bioavailability in contaminated sediments , 1991 .

[50]  S. Wright,et al.  Integumental nutrient uptake by aquatic organisms. , 1989, Annual review of physiology.

[51]  R. Eisler Trace metal concentrations in marine organisms , 1981 .

[52]  A. Tovar‐Sánchez,et al.  Examining dissolved toxic metals in U.S. estuaries. , 2004, Environmental Science and Technology.

[53]  J. Reinfelder,et al.  The assimilation ofelements ingested by marine planktonic bivalve larvae , 1994 .

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

[55]  G. Walker “Copper” granules in the barnacle Balanus balanoides , 1977 .

[56]  S. Luoma,et al.  Subcellular compartmentalization of Cd and Zn in two bivalves. I. Significance of metal-sensitive fractions (MSF) and biologically detoxified metal (BDM) , 2003 .

[57]  S. Luoma,et al.  Kinetic modeling of Ag, Cd and Co bioaccumulation in the clam Macoma balthica: quantifying dietary and dissolved sources , 2002 .

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

[59]  Joop L. M. Hermens,et al.  Peer Reviewed: Internal Exposure: Linking Bioavailability to Effects , 2004 .

[60]  Nicholas S. Fisher,et al.  Assimilation of trace elements ingested by the mussel Mytilus edulis: Effects of algal food abundance , 1995 .

[61]  M. Doblin,et al.  Food web pathway determines how selenium affects aquatic ecosystems: a San Francisco Bay case study. , 2004, Environmental science & technology.

[62]  G. Lopez,et al.  Relationship between subcellular cadmium distribution in prey and cadmium trophic transfer to a predator , 1996 .

[63]  G. Benoit,et al.  Relating the Speciation of Cd, Cu, and Pb in Two Connecticut Rivers with Their Uptake in Algae , 2003 .

[64]  J. S. Gray,et al.  Biomagnification in marine systems: the perspective of an ecologist. , 2002, Marine pollution bulletin.

[65]  B. D. Smith,et al.  Geographical and seasonal variation of trace metal bioavailabilities in the Gulf of Gdansk, Baltic Sea using mussels (Mytilus trossulus) and barnacles (Balanus improvisus) as biomonitors , 2004 .

[66]  L. Bervoets,et al.  Dynamic model for the accumulation of cadmium and zinc from water and sediment by the aquatic oligochaete, Tubifex tubifex. , 2004, Environmental science & technology.

[67]  P. Santschi,et al.  Metals in aquatic systems. , 1988, Environmental science & technology.

[68]  W X Wang,et al.  Comparison of metal uptake rate and absorption efficiency in marine bivalves , 2001, Environmental toxicology and chemistry.

[69]  S. Luoma Can we determine the biological availability of sediment-bound trace elements? , 1989, Hydrobiologia.

[70]  J. Teyssie,et al.  Accumulation and retention of metals in mussels from food and water : A comparison under field and laboratory conditions , 1996 .

[71]  M. Croteau,et al.  Delineating copper accumulation pathways for the freshwater bivalve Corbicula using stable copper isotopes , 2005, Environmental toxicology and chemistry.

[72]  P. Rainbow Phylogeny of trace metal accumulation in crustaceans , 1998 .

[73]  C. Ke,et al.  Dominance of dietary intake of cadmium and zinc by two marine predatory gastropods. , 2002, Aquatic toxicology.

[74]  Wen-Xiong Wang,et al.  Effects of aqueous and dietary preexposure and resulting body burden on silver biokinetics in the green mussel Perma viridis. , 2003, Environmental science & technology.

[75]  R. Thomann,et al.  Steady-state model of biota sediment accumulation factor for metals in two marine bivalves , 1995 .

[76]  C. Wood,et al.  Biotic ligand model, a flexible tool for developing site-specific water quality guidelines for metals. , 2004, Environmental science & technology.

[77]  P. Rainbow,et al.  Does the accumulation of trace metals in crustaceans affect their ecology: the amphipod example? , 2004 .

[78]  P. Rainbow Erratum to “Trace metal concentrations in aquatic invertebrates: why and so what?” , 2003 .

[79]  P. Rainbow,et al.  Barnacles and mussels as biomonitors of trace elements: a comparative study , 1988 .

[80]  P. Rainbow,et al.  Talitrid amphipods (Crustacea) as biomonitors for copper and zinc , 1989 .

[81]  Janet K. Thompson,et al.  Assessing Toxicant Effects in a Complex Estuary: A Case Study of Effects of Silver on Reproduction in the Bivalve, Potamocorbula amurensis, in San Francisco Bay , 2003 .

[82]  S. Luoma,et al.  Uncertainties in assessing contaminant exposure from sediments , 1996 .