Trophic transfer of trace metals: subcellular compartmentalization in a polychaete and assimilation by a decapod crustacean-

Abstract

The chemical form of accumulated trace metal in prey is important in controlling the bioavailability of dietary metal to a predator. This study investigated the trophic transfer of radiolabelled Ag, Cd and Zn from the polychaete worm Nereis diversicolor to the decapod crustacean Palaemonetes varians. We used 2 populations of worms with different proportions of accumulated metals in different subcellular fractions as prey, and loaded the worms with radiolabelled metals either from sediment or from solution. Accumulated radiolabelled metals were fractionated into 5 components : metal-rich granules (MRG), cellular debris, organelles, metallothionein-like proteins (MTLP), and other (heat-sensitive) proteins (HSP). Assimilation efficiencies (AE) of the metals by P. varians were measured from the 4 categories of prey (i.e. 2 populations, radiolabelled from sediment or solution). There were significant differences for each metal between the AEs from the different prey categories, confirming that origin of prey and route of uptake of accumulated trace metal will cause intraspecific differences in subsequent metal assimilation. Correlations were sought between AEs and selected fractions or combinations of fractions of metals in the prey-MRG, Trophically Available Metal (TAM = MTLP + HSP + organelles) and total protein (MTLP + HSP). TAM explained 28% of the variance in AEs for Ag, but no consistent relationships emerged between AEs and TAM or total protein when the metals were considered separately. AEs did, however, show significant positive regressions with both TAM and total protein when the 3 metals were considered together, explaining only about 21% of the variance in each case. A significant negative relationship was observed between MRG and AE for all metals combined. The predator (P. varians) can assimilate dietary metal from a range of the fractions binding metals in the prey (N. diversicolor), with different assimilation efficiencies summated across these fractions. TAM and/or total protein may represent an approximate minimum for trophic availability but neither of these alone is a fully accurate predictor.

Trophic transfer of trace metals: subcellular compartmentalization in bivalve prey, assimilation by a gastropod predator and in vitro digestion simulations

“…In fact, the predator (P. varians) assimilated dietary metal from a range of the fractions binding metals in the prey (N. diversicolor), with different AEs summated across these fractions. TAM could only explain about 21% of the variation in AE of the metals by the predator, while there was a significant negative correlation (46% variance explained) between the predator's AE and the percentage of accumulated metal present in MRG (Rainbow et al 2006a).…”

“…It is therefore relevant to identify general principles that govern the trophic bioavailability of trace metals (Wang & Fisher 1999). The chemical form of trace metals accumulated by food organisms is one potential major factor controlling the assimilation of a trace metal from the diet (Reinfelder & Fisher 1991, Wallace & Lopez 1996, 1997, Wallace et al 1998, Ng et al 2005, Rainbow et al 2006a. Reinfelder & Fisher (1991) observed a linear 1:1 relationship between the metal assimilated by marine copepods from diatoms Thalassiosira pseudonana and various metals partitioned in the cytoplasm of the ingested phytoplankton, suggesting that only metal bound to the soluble fraction in diatoms is available to copepods.…”

“…Cheung & Wang (2005) found a variation in the assimilation efficiency (AE) of the neogastropod mollusc Thais clavigera of metals bound in different subcellular fractions in prey, from soluble proteins to insoluble MRG. Rainbow et al (2006a) also examined the general application of the TAM combined fraction of in a study of the trophic availability of Ag, Cd and Zn accumulated by 2 populations of the polychaete worm Nereis diversicolor to the decapod crustacean Palaemonetes varians. In fact, the predator (P. varians) assimilated dietary metal from a range of the fractions binding metals in the prey (N. diversicolor), with different AEs summated across these fractions.…”

“…Nevertheless, the testing of its wider applicability (e.g. Cheung & Wang 2005, Rainbow et al 2006a, Zhang & Wang 2006 has confirmed that the chemical binding of metals in prey does affect their subsequent assimilation by a predator, with further variation introduced by the digestive capacity of the predator itself. Thus, metals bound in MRG appear to be more susceptible to the assimilatory powers of neogastropod molluscs (Cheung & Wang 2005) than those of palaemonid decapod crustaceans (Wallace & Lopez 1997, Rainbow et al 2006a.…”

“…Thereafter we pooled all remaining soft tissues, except in the case of the scallop where we investigated only the large adductor muscle, the specific tissue typically used for human consumption. We used 2 forms of radiolabelling of the bivalves to promote differences in the subcellular fractionation of accumulated radiolabelled metals (see also Rainbow et al 2006a): from solution (Cd, Ag and Zn) and from a diet of radiolabelled diatoms (Cd, Zn).…”