Interactions of trace metals and different marine food chains

There is increasing recognition of the quantitative importance of metal accumulation from dietary pathways in different marine food webs. With a simple kinetic model requiring mea- surements of metal assimilation efficiency (AE), metal efflux rate and ingestion activity of the rele- vant animals, it is possible to predict the transfer (and potential biomagnification) of metals along diverse marine food chains. In this paper, food chain transfer in different marine food chains (plank- tonic and benthic) is reviewed, and any potential biomagnification of metals is predicted using the simple kinetic equation. It is well recognized that metal concentrations in animals are probably not related to the trophic level in the food chain, but some metals (Hg and Zn) may potentially be influ- enced by the numbers of trophic interactions involved. Depending on these different trophic inter- actions, the potential biomagnification of metals is influenced by metal assimilation or metal efflux rate or both. Metals may potentially be biomagnified in benthic food chains; principally, in those with gastropods as top predators, as they can efficiently sequester dietary metals. The biodiminution of metals (concentration decreases at a higher trophic level) in the classical marine planktonic food chain (phytoplankton to copepods to fish) is largely the result of the effective efflux of metals by the copepods and the very low assimilation of metals by marine fish. Although many past studies have considered the physico-chemical properties of metals in prey in controlling food chain transfer, it is suggested that the physiological and biochemical processes in the herbivore or predator should be emphasized in future studies. Also, the complicated metal-handling strategies found in different marine organisms clearly need to be appreciated.

[1]  Amiard-Triquet,et al.  Changes in metallothionein concentrations in response to variation in natural factors (salinity, sex, weight) and metal contamination in crabs from a metal-rich estuary. , 2000, Journal of experimental marine biology and ecology.

[2]  J. Klaverkamp,et al.  Uptake, elimination and tissue distribution of dietary and aqueous cadmium by rainbow trout (salmo gairdneri richardson) and lake whitefish (coregonus clupeaformis mitchill) , 1989 .

[3]  H. Tjälve,et al.  Accumulation of silver from the diet in two marine benthic predators: The snow crab (Chionoecetes opilio) and American plaice (Hippoglossoides platessoides) , 2000 .

[4]  W. Langston,et al.  Metallothionein induction inMytilus edulis exposed to cadmium , 1991 .

[5]  G. Blackmore.  Interspecific variation in heavy metal body concentrations in Hong Kong marine invertebrates. , 2001, Environmental pollution.

[6]  W. Wang,et al.  Comparative studies on the biokinetics of Cd, Cr, and Zn in the green mussel Perna viridis and the Manila clam Ruditapes philippinarum. , 2001, Environmental pollution.

[7]  R. Pentreath.  Some further studies on the accumulation and retention of 65Zn and 54Mn by the plaice, pleuronectes platessa L. , 1976 .

[8]  B. Morton,et al.  The interpretation of body trace metal concentrations in neogastropods from Hong Kong. , 2001, Marine pollution bulletin.

[9]  C. Folt,et al.  Accumulation of heavy metals in food web components across a gradient of lakes , 2000 .

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

[11]  J. Reinfelder,et al.  Assimilation and regeneration of trace elements by marine copepods , 1996 .

[12]  T. O’Connor,et al.  Recent trends in coastal environmental quality , 1995 .

[13]  C. Marcaillou,et al.  Alternative Methodologies for Predicting Metal Transfer in Marine Food Webs including Filter-Feeders , 1992 .

[14]  H. Dahlgaard.  Effects of season and temperature on longterm in situ loss rates of Pu, Am, Np, Eu, Ce, Ag, Tc, Zn, Co and Mn in a Baltic Mytilus edulis population , 1986 .

[15]  J. Rasmussen,et al.  Modeling the Elimination of Mercury by Fish , 1997 .

[16]  W. Langston,et al.  Cadmium accumulation, distribution and elimination in the bivalve Macoma balthica: neither metallothionein nor metallothionein-like proteins are involved , 1987 .

[17]  S. Fowler,et al.  Cephalopods as a vector for the transfer of cadmium to top marine predators in the north-east Atlantic Ocean. , 1998, The Science of the total environment.

[18]  M. Kennish,et al.  Practical Handbook of Estuarine and Marine Pollution , 1996 .

[19]  J. Nott.  Metals and marine food chains , 1998 .

[20]  A. Nicolaidou,et al.  Transfer of metal detoxification along marine food chains , 1990, Journal of the Marine Biological Association of the United Kingdom.

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

[22]  G. Bryan.  Bioaccumulation of marine pollutants. , 1979, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[23]  M. C. Newman,et al.  Quantitative methods in aquatic ecotoxicology , 1995 .

[24]  B. Berthet,et al.  Bioaccumulation, toxicity and physico-chemical speciation of silver in bivalve molluscs: ecotoxicological and health consequences , 1992 .

[25]  J. Amiard,et al.  Influence of different essential and non-essential metals on MTLP levels in the Copepod Tigriopus brevicornis. , 2001, Comparative biochemistry and physiology. Toxicology & pharmacology : CBP.

[26]  R. Pentreath.  The accumulation and retention of 65Zn and 54Mn by the plaice, Pleuronectes platessa L , 1973 .

[27]  R. Thomann.  Equilibrium Model of Fate of Microcontaminants in Diverse Aquatic Food Chains , 1981 .

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

[29]  D. Hutchins,et al.  Copepod grazing and the biogeochemical fate of diatom iron , 1995 .

[30]  M. Depledge,et al.  The significance of trace metal concentrations in marine invertebrates , 1990 .

[31]  Samuel N. Luoma,et al.  Flexible Digestion Strategies and Trace Metal Assimilation in Marine Bivalves , 1996 .

[32]  Wen-Xiong Wang,et al.  Sediment geochemical controls on Cd, Cr, and Zn assimilation by the clam Ruditapes philippinarum , 2001, Environmental toxicology and chemistry.

[33]  N. Fisher,et al.  Assimilation of trace elements and carbon by the mussel Mytilus edulis: Effects of food composition , 1996 .

[34]  P. Qian,et al.  Significance of Trophic Transfer in Predicting the High Concentration of Zinc in Barnacles , 1999 .

[35]  A. Nicolaidou,et al.  Variable transfer of detoxified metals from snails to hermit crabs in marine food chains , 1994 .

[36]  J. Rasmussen,et al.  Bioaccumulation of Radiocesium by Fish: the Influence of Physicochemical Factors and Trophic Structure , 1994 .

[37]  A. Willcocks,et al.  Concentrations of Mn, Fe, Cu, Zn and Cd in the mesopelagic decapod Systellaspis debilis from the East Atlantic Ocean , 1985 .

[38]  W. Fan,et al.  Geochemistry of Cd, Cr, and Zn in highly contaminated sediments and its influences on assimilation by marine bivalves. , 2002, Environmental science & technology.

[39]  A. Decho,et al.  Time-courses in the retention of food material in the bivalves Potamocorbula amurensis and Macoma balthica : significance to the absorption of carbon and chromium , 1991 .

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

[41]  N. Fisher,et al.  Accumulation of trace elements in a marine copepod , 1998 .

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

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

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

[45]  A. Mason,et al.  The role of intracellular biomineralized granules in the regulation and detoxification of metals in gastropods with special reference to the marine prosobranch Littorina littorea , 1981 .

[46]  J. Reinfelder,et al.  Bioaccumulation, Subcellular Distribution, and Trophic Transfer of Copper in a Coastal Marine Diatom , 2000 .

[47]  N. Fisher,et al.  Assimilation of selenium in the marine copepod Acartia tonsa studied with a radiotracer ratio method , 1991 .

[48]  William G. Wallace,et al.  Bioavailability of biologically sequestered cadmium and the implications of metal detoxification , 1997 .

[49]  Bryant Gw.  Bioaccumulation of marine pollutants. , 1979 .

[50]  T. Dillon,et al.  Trophic transfer and biomagnification potential of contaminants in aquatic ecosystems. , 1994, Reviews of environmental contamination and toxicology.

[51]  Wen-Xiong Wang,et al.  Individual responses of trace-element assimilation and physiological turnover by the marine copepod Calanus sinicus to changes in food quantity , 2001 .

[52]  S. White,et al.  Heavy metal concentrations and size effects in the mesopelagic decapod crustacean Systeilaspis debilis , 1987 .

[53]  C. Folt,et al.  Bioaccumulation and Diminution of Arsenic and Lead in a Freshwater Food Web , 2000 .

[54]  Richard S. Stemberger,et al.  Fish tissue metals and zooplankton assemblages of northeastern U.S. lakes , 1998 .

[55]  W. Langston,et al.  Cadmium and the phosphate granules in Littorina littorea , 1989, Journal of the Marine Biological Association of the United Kingdom.

[56]  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.

[57]  S. Baines,et al.  Assimilation and retention of selenium and other trace elements from crustacean food by juvenile striped bass (Morone saxatilis) , 2002 .

[58]  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.

[59]  J. Garnier-Laplace,et al.  Dietary uptake, retention and tissue distribution of 54Mn, 60Co and 137Cs in the rainbow trout (Oncorhynchus mikiss Walbaum) , 2000 .

[60]  T. Hung,et al.  Mussel watch: a review of Cu and other metals in various marine organisms in Taiwan, 1991-98. , 2000, Environmental pollution.

[61]  F. Kasamatsu,et al.  Natural variation of radionuclide 137Cs concentration in marine organisms with special reference to the effect of food habits and trophic level , 1997 .

[62]  M. Bebianno,et al.  Metal handling strategies in molluscs , 1998 .

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

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

[65]  W. Langston,et al.  Evaluation of the significance of metal-binding proteins in the gastropod Littorina littorea , 1986 .

[66]  C. Ke,et al.  Bioaccumulation of Cd, Se, and Zn in an estuarine oyster (Crassostrea rivularis) and a coastal oyster (Saccostrea glomerata). , 2001, Aquatic toxicology.

[67]  B. Bayne,et al.  Feeding Physiology of Bivalves: Time-Dependence and Compensation for Changes in Food Availability , 1993 .

[68]  Wen-Xiong Wang,et al.  The assimilation of detritus‐bound metals by the marine copepod Acartia spinicauda , 2002 .

[69]  D. Nahabedian,et al.  Analysis of some factors that may modify the bioavailability of cadmium and lead by Biomphalaria glabrata , 2000 .

[70]  R. Furness,et al.  Effects of Animal Size on Concentrations of Metallothionein and Metals in Periwinkles Littorina littorea Collected from the Firth of Clyde, Scotland , 1999 .

[71]  J. Reinfelder,et al.  Relative importance of dissolved versus trophic bioaccumulation of copper in marine copepods , 2002 .

[72]  Wen-Xiong Wang,et al.  Influences of metal concentration in phytoplankton and seawater on metal assimilation and elimination in marine copepods , 2001, Environmental toxicology and chemistry.

[73]  P. Rainbow.  Copper, cadmium and zinc concentrations in oceanic amphipod and euphausiid crustaceans, as a source of heavy metals to pelagic seabirds , 1989 .

[74]  J. Garnier-Laplace,et al.  Experimental Kinetic Rates of Food-Chain and Waterborne Radionuclide Transfer to Freshwater Fish: A Basis for the Construction of Fish Contamination Charts , 2000, Archives of environmental contamination and toxicology.

[75]  A. Brooks,et al.  Selenium uptake and transfer in an aquatic food chain and its effects on fathead minnow larvae , 1986 .

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

[77]  J. Levinton,et al.  Cadmium resistance in an oligochaete and its effect on cadmium trophic transfer to an omnivorous shrimp , 1998 .

[78]  I. Ni,et al.  The Uptake of Cd, Cr, and Zn by the Macroalga Enteromorpha crinita and Subsequent Transfer to the Marine Herbivorous Rabbitfish, Siganus canaliculatus , 2003, Archives of environmental contamination and toxicology.

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

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

[81]  J. Reinfelder,et al.  Assimilation efficiencies and turnover rates of trace elements in marine bivalves: a comparison of oysters, clams and mussels , 1997 .

[82]  H. Segner,et al.  Contaminated food and uptake of heavy metals by fish: a review and a proposal for further research , 1987, Oecologia.

[83]  D. A. Nelson,et al.  Biochemical and ultrastructural observations of long-term silver accumulation in the mussel, Mytilus edulis , 1986 .

[84]  G. Blackmore.  Field Evidence of Metal Transfer from Invertebrate Prey to an Intertidal Predator, Thais clavigera (Gastropoda: Muricidae) , 2000 .

[85]  G. Zauke,et al.  Evaluation of trace metal toxicokinetics in Greenland Sea copepod and amphipod collectives from semi-static experiments on board ship , 1997, Polar Biology.

[86]  D. Phillips,et al.  Biomonitoring of Trace Aquatic Contaminants , 2012 .

[87]  W. Sunda,et al.  Relative contributions of food and water in the accumulation of zinc by two species of marine fish , 1984 .

[88]  A. Nicolaidou,et al.  Metals in gastropods—metabolism and bioreduction , 1989 .

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

[90]  P. Lam,et al.  Modeling radiocesium bioaccumulation in a marine food chain , 2000 .

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

[92]  D. Turner,et al.  Metal speciation and bioavailability in aquatic systems , 1995 .

[93]  B. Berthet,et al.  Metal transfer in marine food chains: bioaccumulation and toxicity. , 1993, Acta biologica Hungarica.

[94]  J. Reinfelder,et al.  Retention of elements absorbed by juvenile fish (Menidia menidia, Menidia beryllina) from zooplankton prey , 1994 .

[95]  B. Berthet,et al.  Determination of Cadmium Partitioning in Microalgae and Oysters: Contribution to the Assessment of Trophic Transfer , 2001, Archives of Environmental Contamination and Toxicology.

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

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