Subcellular compartmentalization of Cd and Zn in two bivalves. II. Significance of trophically available metal (TAM)

This paper examines how the subcellular partitioning of Cd and Zn in the bivalves Macoma balthica and Potamocorbula amurensis may affect the trophic transfer of metal to predators. Results show that the partitioning of metals to organelles, 'enzymes' and metallothioneins (MT) com- prise a subcellular compartment containing trophically available metal (TAM; i.e. metal trophically available to predators), and that because this partitioning varies with species, animal size and metal, TAM is similarly influenced. Clams from San Francisco Bay, California, were exposed for 14 d to 3.5 µg l -1 Cd and 20.5 µg l -1 Zn, including 109 Cd and 65 Zn as radiotracers, and were used in feeding experiments with grass shrimp Palaemon macrodatylus, or used to investigate the subcellular parti- tioning of metal. Grass shrimp fed Cd-contaminated P. amurensis absorbed ~60% of ingested Cd, which was in accordance with the partitioning of Cd to the bivalve's TAM compartment (i.e. Cd asso- ciated with organelles, 'enzymes' and MT); a similar relationship was found in previous studies with grass shrimp fed Cd-contaminated oligochaetes. Thus, TAM may be used as a tool to predict the trophic transfer of at least Cd. Subcellular fractionation revealed that ~34% of both the Cd and Zn accumulated by M. balthica was associated with TAM, while partitioning to TAM in P. amurensis was metal-dependent (~60% for TAM-Cd%, ~73% for TAM-Zn%). The greater TAM-Cd% of P. amuren- sis than M. balthica is due to preferential binding of Cd to MT and 'enzymes', while enhanced TAM- Zn% of P. amurensis results from a greater binding of Zn to organelles. TAM for most species-metal combinations was size-dependent, decreasing with increased clam size. Based on field data, it is esti- mated that of the 2 bivalves, P. amurensis poses the greater threat of Cd exposure to predators because of higher tissue concentrations and greater partitioning as TAM; exposure of Zn to predators would be similar between these species.

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

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

[3]  G. Bordin,et al.  Trace metals in the marine bivalve Macoma balthica in the Westerschelde estuary, The Netherlands. Part 3: variability of the role of cytosol in metal uptake by the clams. , 1996, The Science of the total environment.

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

[5]  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 .

[6]  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 .

[7]  J. Levinton,et al.  Rapid Evolution of Metal Resistance in a Benthic Oligochaete Inhabiting a Metal-polluted Site , 1989 .

[8]  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 .

[9]  A. Rodrı́guez,et al.  Trace metals in the marine bivalve Macoma balthica in the Westerschelde estuary (The Netherlands). Part 1: Analysis of total copper, cadmium, zinc and iron concentrations-locational and seasonal variations , 1992 .

[10]  James T. Carlton,et al.  Remarkable invasion of San Francisco Bay (California, USA), by the Asian clam Potamocorbula amurensis. I. Introduction and dispersal , 1990 .

[11]  L.,et al.  Use of the euryhaline bivalve Potamocorbula amurensis as a biosentinel species to assess trace metal contamination in San Francisco Bay , 2004 .

[12]  W. Cope,et al.  Bioassessment of mercury, cadmium, polychlorinated biphenyls, and pesticides in the upper Mississippi River with zebra mussels ( Dreissena polymorpha ) , 1999 .

[13]  J. Weis,et al.  Trophic transfer of contaminants from organisms living by chromated-copper-arsenate (CCA)-treated wood to their predators , 1993 .

[14]  G. Roesijadi The significance of low molecular weight, metallothionein-like proteins in marine invertebrates: Current status , 1981 .

[15]  S. Luoma,et al.  Variations in the Correlation of Body Size with Concentrations of Cu and Ag in the Bivalve Macoma balthica , 1981 .

[16]  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 .

[17]  W. Wolff,et al.  Predation on 0-group and older year classes of the bivalve Macoma balthica: interaction of size selection and intertidal distribution of epibenthic predators , 2002 .

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

[19]  L. Hare,et al.  Relative importance of water and food as cadmium sources to an aquatic insect (Chaoborus punctipennis) : Implications for predicting Cd bioaccumulation in nature , 1997 .

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

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

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

[23]  E. Bonsdorff,et al.  Predation on the bivalve Macoma balthica by the sopod Saduria entomon: laboratory and field experiments , 1992 .

[24]  S. Luoma,et al.  Effect of seasonally changing tissue weight on trace metal concentrations in the bivalve Macoma balthica in San Francisco Bay , 1986 .

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

[26]  P. Rainbow,et al.  Availability of cadmium and zinc from sewage sludge to the flounder, Platichthys flesus, via a marine food chain. , 2001, Marine environmental research.

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

[28]  H. Govers,et al.  Bioaccumulation of cadmium by the freshwater isopod Asellus aquaticus (L.) from aqueous and dietary sources. , 1989, Environmental pollution.

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

[30]  M. Brouwer,et al.  Alterations in prey capture and induction of metallothioneins in grass shrimp fed cadmium‐contaminated prey , 2000 .

[31]  B. Brown THE FORM AND FUNCTION OF METAL‐CONTAINING ‘GRANULES’ IN INVERTEBRATE TISSUES , 1982 .

[32]  N. Fisher,et al.  Relating the reproductive toxicity of five ingested metals in calanoid copepods with sulfur affinity. , 2002, Marine environmental research.

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

[34]  C. Mouneyrac,et al.  Metallothionein-like proteins in Macoma balthica: effects of metal exposure and natural factors , 2000 .

[35]  S. Luoma,et al.  Influence of seasonal growth, age, and environmental exposure on Cu and Ag in a bivalve indicator, Macoma balthica, in San Francisco Bay , 1990 .

[36]  J. Weis,et al.  Genetic adaptation to heavy metals in aquatic organisms: a review. , 1987, Environmental pollution.

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

[38]  G. Roesijadi Metallothioneins in metal regulation and toxicity in aquatic animals , 1992 .

[39]  C. Hacker,et al.  Effects of salinity, temperature, and cadmium on cadmium-binding protein in the grass shrimp,Palaemonetes pugio , 1990 .

[40]  James G. Sanders,et al.  Pathways of silver uptake and trophic transfer in estuarine organisms , 1991 .

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

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

[43]  P. Klerks,et al.  Cadmium accumulation and detoxification in a Cd-resistant population of the oligochaete Limnodrilus hoffmeisteri , 1991 .

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

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

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

[47]  G. Bordin,et al.  Metallothionein-like metalloproteins in the Baltic clam Macoma balthica : seasonal variations and induction upon metal exposure , 1997 .

[48]  Artemis Nicolaidou,et al.  BIOREDUCTION OF ZINC AND MANGANESE ALONG A MOLLUSCAN FOOD CHAIN , 1993 .

[49]  C. R. BOYDEN,et al.  Trace element content and body size in molluscs , 1974, Nature.

[50]  A. Mason,et al.  Relationships between subcellular distributions of cadmium and perturbations in reproduction in the polychaete Neanthes arenaceodentata , 1988 .

[51]  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.