Page 427 - The Toxicology of Fishes

The Osmoregulatory System 407

membranes forming slit-like lumina communicating by pores with the extracellular space at the serosal
side of the epithelium, with many elongated mitochondria between these folds. The membranes are
the probable location of ion-translocating mechanisms that have been demonstrated in the intestine:
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Na /K -ATPase, Ca -ATPase, and a Na /Ca exchanger (Schoenmakers et al., 1993). In the brush
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border of the enterocytes of Mozambique tilapia, a low-affinity Ca transporting carrier has been
demonstrated. Ample evidence for transcellular and paracellular ion transport has been presented (see
review by Flik et al., 1996).
The structure of the enterocytes is essentially similar in freshwater and seawater fish, although the
basal labyrinth is more extensive in the latter. This reflects the high intensity of the intestinal reabsorption
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of water, Na , and Cl in marine fish that is required to offset the osmotic loss of water across the
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integument in seawater; however, an important qualitative difference is the presence of the Na /K /2Cl –
cotransporter in seawater fish.
The more than tenfold difference in drinking rate between freshwater and seawater fish has important
consequences for the exposure of the intestine to toxic agents. Whereas in freshwater it is mainly the
pharyngeal area that is in contact with the ambient water as a result of the respiratory water movements,
in seawater the entire alimentary tract is exposed, particularly the rectal part, where most of the water
and ions are taken up. Thus, in seawater, waterborne toxicants are potentially more threatening to fish
than in freshwater; however, a direct comparison is complicated by the differences in bioavailability of
toxic agents that may occur as a result of salinity effects on speciation of the toxicants. This holds in
particular for toxic metals.
Heavy Metals

From the point of view of hydromineral control, the actions of heavy metals on the intestine are
comparable to those on the gills, as they affect inhibition of ion-transporting mechanisms and increase
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the permeability of the intestinal epithelium. Reduction of intestinal Na /K -ATPase activity has been
reported for several metals, including mercury (Lakshmi et al., 1991), chromium (Boge et al., 1988;
Thaker et al., 1996), and cadmium (Schoenmakers et al., 1992). Mozambique tilapia has been shown to
become hypocalcemic when fed cadmium-containing food (Pratap et al., 1989). Apparently, these fish
could not compensate the decrease of intestinal calcium uptake by stimulation of branchial uptake from
the water. This may be the result of dietary cadmium entering the blood and inhibiting branchial calcium
uptake, as was shown by Baldisserotto et al. (2005) for rainbow trout. Conversely, these authors also
showed that an increase of dietary calcium reduced both intestinal and branchial cadmium uptake. In
tilapia, increased apoptosis and necrosis of chloride cells has been reported for Mozambique tilapia
exposed to dietary cadmium, similar to what occurs after exposure to waterborne cadmium (Pratap et
al., 1989). The hypocalcemia induced by cadmium already at low concentrations may be partially caused
by inhibition of intestinal calcium uptake. Schoenmakers et al. (1992), studying intestinal basolateral
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membrane preparations of Mozambique tilapia, showed that Cd inhibits the active transport of Ca 2+
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across these membranes, probably by inhibiting the Ca -ATPase activity in these membranes. The same
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authors, studying the effects of Cd on stripped intestinal epithelium of the same species in an Ussing
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chamber, further demonstrated that the addition of Cd at the mucosal, but not serosal, side decreased
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the active transcellular Ca transport across this epithelium (Schoenmakers et al., 1992). The ATP-driven
calcium translocation across these membranes was extremely sensitive to cadmium, indicating inhibition
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via the calcium site of the enzyme (Figure 8.4). Intestinal Na /K -ATPase activity was half maximally
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inhibited at 2.6 µM Cd , with cadmium probably competing for the Mg site of the enzyme. Thus, the
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sensitivity for Cd of both enzymes differs by five orders of magnitude. The Na /Ca exchanger was
only partially blocked by cadmium binding. Finally, the mucosal and serosal addition of Cd resulted
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in increased permeability to Ca of the paracellular route in this epithelium, and this may result in
passive losses of Ca in freshwater or the inflow of Ca in seawater.
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In an electrophysiological study on seawater eels, evidence was obtained that Cd affects intestinal
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Na and Cl reabsorption via both cellular and paracellular mechanisms. In marine fish, the intestinal
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Na and Cl reabsorption is affected by the luminal Na /K /2Cl cotransporter in conjunction with serosal
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Na /K -ATPase activity and Cl conductance (Trischitta et al., 1992). Cd blocked Na /K -ATPase
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