Dietary Uptake Patterns Affect Bioaccumulation and Biomagnification of Hydrophobic Organic Compounds in Fish

Abstract

Biomagnification of hydrophobic organic compounds (HOCs) increases the eco-environmental risks they pose. Here, we gained mechanistic insights into biomagnification of deuterated polycyclic aromatic hydrocarbons (PAHs-d 10 ) in zebrafish with carefully controlled water (ng L −1 ) by a passive dosing method and dietary exposures using pre-exposed Daphnia magna and fish food. A new bioaccumulation kinetic model for fish was established to take into account discrete dietary uptake, while the frequently used model regards dietary uptake as a continuous process. We found that when freely dissolved concentrations of the PAHs-d 10 were constant in water, the intake amount of the PAHs-d 10 played an important role in affecting their steadystate concentrations in zebrafish, and there was a peak concentration in zebrafish after each dietary uptake. Moreover, considering the randomness of predation, the Monte Carlo simulation results showed that the probabilities of biomagnification of the PAHs-d 10 in zebrafish increased with their dietary uptake amount and frequency. This study indicates that in addition to the well-known lipid−water partitioning, the bioaccumulation of HOCs in fish is also a discontinuous kinetic process caused by the fluctuation of HOC concentration in the gastrointestinal tract as a result of the discrete food ingestion. The discontinuity and randomness of dietary uptake can partly explain the differences among aquatic ecosystems with respect to biomagnification for species at similar trophic levels and provides new insight for future analysis of experimental and field bioaccumulation data for fish.

Contribution of Dietary Uptake to PAH Bioaccumulation in a Simplified Pelagic Food Chain: Modeling the Influences of Continuous vs Intermittent Feeding in Zooplankton and Fish

“…The difference in the feeding interval between zooplankton and fish had a significant impact on their dietary uptake kinetics of PAHs. The intermittent food ingestion would induce an instantaneous increase of PAH concentrations in the GI tract of zebrafish, and a convex variation (first increase then decrease) of concentrations in the whole body except the GI tract of zebrafish . In contrast, the approximately continuous food ingestion would cause a gradual increase of PAH- d 10 concentrations in the gut and the body except the gut of D.…”

“…Combined with our previous studies on bioaccumulation of PAHs- d 10 in zebrafish, we postulated that dietary uptake was expected to range from none for phytoplankton to approximately continuous for zooplankton to discrete for fish, and such discontinuity for fish might increase with increasing trophic levels. The difference in the feeding interval between zooplankton and fish had a significant impact on their dietary uptake kinetics of PAHs.…”

“…magna and spiked fish food in a passive dosing system to maintain constant freely dissolved concentrations, as well as depuration experiments. Detailed experimental manipulation and measurements are given in our previous publication . The results showed that additional dietary uptake would increase the steady-state concentrations of PAHs- d 10 in zebrafish when the freely dissolved concentrations remained constant; there was a peak concentration in zebrafish after each dietary uptake.…”

“…However, field studies showed that some HOCs such as polycyclic aromatic hydrocarbons (PAHs) underwent trophic dilution instead of magnification in some aquatic ecosystems. , This is likely because PAHs are prone to being biotransformed by fish compared with other legacy HOCs such as polychlorinated biphenyls (PCBs) . Nevertheless, additional dietary uptake may still significantly increase the steady-state concentrations of PAHs in macroinvertebrates and fish , compared to waterborne-only uptake (bioconcentration). However, the relative contributions of diet-borne PAHs to the steady-state bioaccumulation in aquatic organisms at different trophic levels are unclear.…”

“…Nevertheless, dietary uptake kinetics are different for different aquatic animals. The reported feeding interval is very short for macroinvertebrates within seconds to minutes (pulse food ingestion). , Thus, dietary uptake for zooplankton may be simulated as an approximately continuous process, while its uptake for fish can be viewed as an intermittent (discrete) process rather than a continuous one because predation causes a random feeding interval. , Therefore, we hypothesized that dietary uptake for pelagic organisms ranged from none for phytoplankton to approximately continuous for zooplankton to discrete for fish; and the differences in dietary uptake rate and interval across trophic levels might affect the dietary uptake kinetics and further steady-state concentrations, especially for HOCs that are prone to being biotransformed such as PAHs.…”