Significance of subcellular metal distribution in prey in influencing the trophic transfer of metals in a marine fish

Abstract

We investigated how the subcellular metal distribution in prey affects metal dietary assimilation in a marine fish, the grunt Terapon jarbua. The assimilation efficiency (AE) of metals (Cd, Se, and Zn) in the grunt varied by prey, which included copepods, barnacles, clams, mussels, and fish viscera. The AEs were 3-9% for Cd, 13-36% for Se, and 2-52% for Zn. The AEs of Se and Zn were significantly correlated with the subcellular Se and Zn distributions in the prey, suggesting that the subcellular forms of Se and Zn in the fish's diet affected assimilation. Further experiments determined AEs using purified subcellular fractions of copepods and mussels as fish diets. AEs were higher in the grunts fed the heat-stable protein fraction or the heat-sensitive protein fraction than in those fed insoluble fractions. AEs were comparable in fish fed purified subcellular fractions from different prey, further indicating the importance of subcellular metal distribution in metal assimilation. AEs of Se and Zn but not Cd were significantly dependent on the ingestion rate of fish and gut passage times for metals, suggesting that fish had different digestive strategies to handle essential and nonessential elements. Assimilation of metals by marine fish is determined both by the subcellular metal distribution in the prey and by the feeding process of the fish.There have been wide concerns about the accumulation of metals in fish because of their commercial values and health risks to humans due to consumption. Fish are exposed to various sources of metals, including from water and food. It has become increasingly clear that trophic transfer of metals contributes to (or dominates) overall metal accumulation in fish (Spry et al. 1988; Xu and Wang 2002;Zhang and Wang 2005). Understanding the dietary assimilation in fish has become important in modeling metal accumulation (Luoma and Rainbow 2005). Metal assimilation results from digestive processing of metals associated with ingested prey. The assimilation efficiency (AE) indicates the fraction of ingested metal remaining in the fish body after the undigested materials are evacuated. Many studies have determined the AEs of different metals in a wide range of aquatic organisms, including fish (Reinfelder and Fisher 1994;Zhao et al. 2001;Long and Wang 2005). However, mechanisms underlying the dietary assimilation of metals in marine fish are not yet clearly understood.Assimilation is an interactive process between food and the digestive system of the consumer. It has been shown that different prey resulted in a variation of metal AEs in fish (Ni et al. 2000; Xu and Wang 2002), suggesting that different forms of metals in the food may influence the availability of metals. Some previous studies have indicated that the cytosolic distribution of metals in marine phytoplankton is important in dietary assimilation by marine herbivores (Reinfelder and Fisher 1991;Wang and Fisher 1996;Chong and Wang 2000), but assimilation in marine predators appears to be more complicated. Recently, th...

Feeding ratio and frequency affects cadmium bioaccumulation in black sea bream Acanthopagrus schlegeli

“…The ingestion rate (IR, equivalent to FR in the present study) and gut passage time (GPT) are suggested to be the 2 most important factors determining the AEs of metals in many aquatic organisms (e.g. Zhang & Wang 2006a, Croteau et al 2007). In most cases, the AEs of metals increased with prolonged GPT, and AEs were higher at a lower IR and vice versa (Zhang & Wang 2006a, Croteau et al 2007).…”

“…Although a growing body of study has revealed that changes in food quality have a significant effect on dietary metal assi milation in farmed marine fish (e.g. food type [Wang & Wong 2003, Zhang & Wang 2006a and dietary protein sources [Mai et al 2006), little is known about the influence of food quantity management (e.g. feeding ratio and frequency adjustments) on dietary metal bioaccumulation in farmed fish.…”

“…Diet is the predominant route of exposure for most aquatic organisms (Rainbow 2007. Several studies have demonstrated that dietary trace metal assimilation is closely related to the ingestion rate (IR) and gut passage time (GPT) of diets (Zhang & Wang 2006a, Croteau et al 2007. Feeding ratio and frequency have a substantial influence on the IR and GPT of diets in fish (Lee et al 2000, Riche et al 2004, and thus probably affect the assimilation process of dietary trace metals.…”

Multielement analysis in the fish hepatic cytosol as a screening tool in the monitoring of natural waters

“…in mummichog (Goto and Wallace 2010); brown trout and European eel (Linde et al 1999)), Ni and Tl (e.g. in yellow perch (Campbell et al 2008); fathead minnow (Lapointe and Couture 2009)) and Se (e.g. in grunt (Zhang and Wang 2006)). The benefit of metal and metalloid determination in the soluble tissue fraction over determination of total tissue load lays in the fact that accumulated metals and metalloids, as described for Cd, fractionate into metabolically reactive and detoxified pools.…”

Exposure-dose-response of Tellina deltoidalis to contaminated estuarine sediments 3. Selenium spiked sediments

“…Alternatively the granule fraction may 463 represent selenium associated with incompletely digested tissue and cell debris in the NaOH 464 digestion step of the fractionation procedure (Taylor and Maher, 2013). The fractionation 465 procedure used by Zhang and Wang (2006) which found 40 and 60% of selenium in 466 crustaceans and bivalves associated with the granule fraction used a shorter NaOH digestion 467 step, 10 minutes rather than the 60 minutes used in this study, so incomplete digestion of the 468 tissue and cell debris fraction in their study is also a possibility. If this is the case then it is 469 still a reasonable assumption that a fair proportion of this fraction represents detoxified 470 selenium.…”