Page 38 - The Toxicology of Fishes

18 The Toxicology of Fishes

compounds spiked into synthetic diets or administered in oil (Burreau et al., 1997; Nichols et al., 2001).
Comparisons of metal uptake from formulated and natural diets have yielded varying results (Clearwater
et al., 2002).
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Vetter et al. (1985) used autoradiographic methods to show that [ C]-benzo(a)pyrene remains asso-
ciated with lipid throughout lipolysis, lipid absorption, and the formation of intracellular fat droplets in
the gut epithelium. These observations underscore the close association between hydrophobic compounds
and lipids throughout digestion but provide little information on processes that actually limit the rate of
absorption at the gastrointestinal epithelium. Working with goldfish, Gobas et al. (1993a) found that
dietary uptake of some very hydrophobic compounds (log K > 6.3) declined with an increase in dietary
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lipid content, while uptake of some moderate to high log K compounds (4.5 < log K < 6.3) did not
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vary among treatment groups. These findings were interpreted as evidence that simple diffusion controls
the rate of uptake across the gut epithelium.
Using an in situ channel catfish intestinal preparation, Doi et al. (2000) showed that the bioavailability
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of [ C]-3,3′,4,4′-tetrachlorobiphenyl ([ C]-PCB 77) varied with the fatty acid composition of lipid
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micelles and that these differences were related to the ability of micelles to solubilize the compound.
These observations suggest that dietary absorption of hydrophobic compounds depends on the capacity
of lipid micelles to deliver chemical to the gastrointestinal epithelium and possibly on regional differences
in fatty acid absorption. In addition, Doi et al. (2000) found that dietary pretreatment of fish with
unlabeled PCB 77 reduced the bioavailability of a subsequent radiolabeled dose. This decrease in uptake
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efficiency was accompanied by lower concentrations of [ C]-PCB in the cytosolic fraction of gut tissues.
The mechanism responsible for this pretreatment effect is unclear but may have been due to unlabeled
PCB occupying binding sites on proteins and lipids that transport chemicals through the cytosol.
To the extent that simple diffusion plays a role in controlling chemical uptake within the gut, the
process of digestion will tend to promote uptake of hydrophobic compounds by increasing the chemical
activity gradient between the gut contents and blood (Connolly and Pederson, 1988; Gobas et al., 1993b;
Nichols et al., 2004). This happens for two reasons: (1) a reduction in meal volume increases the
concentration of chemical remaining in the GIT, and (2) absorption of dietary lipid substantially reduces
chemical affinity for material remaining within the GIT and at the same time causes a transient increase
in chemical affinity for the absorbing tissues. Together, these two outcomes of digestion create a potential
for the lipid-normalized chemical concentration in a predator to exceed that of its prey, a condition
referred to as biomagnification. Initially, this finding might appear to violate thermodynamic principles
but, in fact, does not if equilibria are evaluated relative to digested rather than ingested material.
Chemical uptake from dietary sources may be reduced by biotransformations mediated by gut micro-
flora or occurring within the gastrointestinal epithelium. In studies with in situ gut preparations, the GIT
has been shown to play an important role in the metabolism of PAHs by fish, altering their form and
limiting transport to the systemic circulation (Kleinow et al., 1998; Van Veld et al., 1988). Operating in
series with first-pass metabolism in the liver, this activity can substantially reduce the accumulation of
contaminant residues by fish (James and Kleinow, 1994; Kleinow and James, 2001; Van Veld, 1990).
In an environmental setting, chemical uptake by an organism from its diet also depends on the accu-
mulation relationships for the organisms that it consumes (Figure 2.2). Under these circumstances, it
becomes necessary to extend bioavailability concepts to an entire assemblage of species. Organisms that
occupy the base of an aquatic food web generally accumulate chemicals directly from water. For these
animals, chemical speciation and the microenvironment within which the animal lives may be critical
determinants of uptake. Chemicals that possess characteristics that favor dietary uptake will then pass
through a series of trophic transfers, ultimately accumulating in fish that occupy the highest trophic level.
At each step along the way, the chemical concentration in the organism represents a dynamic balance
between uptake and elimination processes. Organism growth rate will also influence the concentration of
slowly accumulating chemicals by determining the mass of tissue into which chemicals are distributed.
An extension of bioavailability concepts from individual animals to entire food webs must also take
into account species differences in biotransformation; for example, some organic chemicals are efficiently
metabolized by benthic invertebrates. In extreme cases, this metabolism proceeds to such an extent that
organisms at higher trophic levels are exposed only to metabolites. Other organic chemicals may
accumulate at lower trophic levels but may be absent or present at reduced concentrations in fish tissues