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

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, there has been an increasing awareness of the subcellular fate of metals in prey organisms and of how the subcellular metal forms may subsequently affect the trophic transfer to the next level (Wang 2002; Vijver et al. 2004). In these studies, using a metal subcellular partitioning method (Wallace et al. 2003; Wallace and Luoma 2003), the prey were separated into metal-rich granules (MRG), cellular debris, organelles, heat-denatured protein (HDP), and heat-stable protein (HSP) fractions. MRG and HSP (containing metallothionein [MT]) were considered to sequester and thereby detoxify metals. Furthermore, metals distributed in organelles, HDP, and HSP were considered to be trophically available (Wallace et al. 2003). A recent study used this subcellular partitioning method to determine the transfer of Cd from grass shrimps to mummichog fish, but the relationship between the metal speciation in the shrimps and the AE in the fish was not explored (Seebaugh et al. 2005). Additionally, feeding in the predators including food ingestion and digestion also controls the assimilation of metals. Active ingestion is a common behavior in fish because of their good swimming abilities. After food ingestion, digestion occurs in the acidic environment of the stomach and the alkaline environment of the intestine by the action of enzymes in digestive fluids and the epithelial cells. Assimilation occurs mostly in the intestine in most fishes (Fänge and Grove 1979; Horn 1997). The ingestion rate (IR) and the gut passage time (GPT), reflecting the amount of ingested food and the movement of the food in the digestive tract, are the two most important parameters of feeding and therefore are closely related to assimilation. The dependence of metal assimilation on IR and GPT has been demonstrated in marine 1 Corresponding author ([email protected]). Acknowledgments We thank the two anonymous reviewers for their very constructive comments. This study was supported by a Competitive Earmarked Research Grant from the Hong Kong Research Grants Council (HKUST6405/05M) to W.-X.W. Limnol. Oceanogr., 51(5), 2006, 2008–2017 E 2006, by the American Society of Limnology and Oceanography, Inc.