Page 87 - The Toxicology of Fishes

Toxicokinetics in Fishes 67

6, proposed that structural attributes of these compounds limit branchial uptake (Bruggeman et al., 1984;
Konemann and Van Leeuwen, 1980; Sugiura et al., 1978; Tulp and Hutzinger, 1978; Zitko, 1974; Zitko
and Hutzinger, 1978). Alternatively, because uptake of these compounds is extremely slow, steady-state
concentrations may not have been achieved in these studies, leaving the false impression of a downward
deflection in BCF. Branchial uptake of highly lipophilic compounds may also be limited by binding to
dissolved organic matter in the water, thereby reducing the concentration of the free or bioavailable form
of the compound. Ionized organic compounds exhibit limited ability to cross the gill membranes and
must be dealt with as a special group.
Water and blood flows through the gills maintain xenobiotic diffusion gradients across the gill
epithelium. Norstrom et al. (1976), Neely (1979), and Bruggeman et al. (1981) suggested that branchial
uptake may be correlated to the rate of water flow across the gills and thus to respiration rate. Gobas
and MacKay (1987) considered multiple diffusion and flow steps to be part of the branchial exchange
process. Barber et al. (1988) presented a hydrodynamic-based model for chemical bioconcentration in
fish that incorporates effects of advection and diffusion in water flowing through the gills. Hayton and
Barron (1990) suggested that blood flow, water flow, and diffusional barriers all have the potential to
influence branchial flux, and they proposed a model based on the concept of serial resistance. Erickson
and McKim (1990a,b) developed a counter-current model of branchial flux for non-ionized compounds
that includes both flow and diffusion limitations, as well as chemical binding to dissolved organic
material. Detailed descriptions of both models are given later in this chapter.

Physiological Impacts on Branchial Absorption
Gill ventilation and blood perfusion rates vary with activity level, temperature, and environmental oxygen
tension (Barron et al., 1987a; Hughes, 1984; Randall and Daxboeck, 1984). Differences in environmental
conditions and activity level also impact the toxicity and bioconcentration of chemicals in fish. We now
understand that these observations are linked; changes in environment and activity increase or decrease
branchial absorption of xenobiotics by impacting the rate-limiting processes that control this uptake.
Dissolved Oxygen—Four decades ago, Lloyd (1961) observed increases in the toxicity of several
chemicals to rainbow trout as ambient oxygen concentrations were reduced from 100% to 30% of
saturation. He suggested that the increase in toxicity was caused by an increase in ventilation volume
that occurred at reduced oxygen concentrations, resulting in a larger quantity of chemical being brought
in close contact with the gills. Lloyd’s (1961) observations were supported by those of McKim and
Goeden (1982), who measured changes in branchial uptake of endrin (log K 5.02) in response to a
ow
stepwise decrease in afferent water oxygen concentration. Initial oxygen and endrin extraction efficiencies
were nearly constant at oxygen saturation values of 100% and 80% but dropped progressively at oxygen
saturation values of 50% and 30% (Figure 3.5A). Apparently, endrin extraction efficiency was maintained
in the face of moderate increases in ventilation volume because diffusion was fast enough to clear
lamellar channels of most of the chemical (i.e., there was no change in physiological dead space; see
Hughes, 1984), or because the number of blood-perfused gill lamellae increased (Randall and Daxboeck,
1984). Observed declines in extraction efficiency may have been due to an increase in ventilatory stroke
volume, resulting in greater bypass of water around the lamellar channels (i.e., increased anatomical
deadspace), or an increase in physiological deadspace associated with increased water velocities. Because
ventilation volume increased more than extraction efficiency decreased, total endrin uptake rate at 50%
of oxygen saturation was about double that at 100% (Figure 3.5B). The additional decrease in oxygen
saturation from 50% to 30% did not result in higher endrin uptake rates.
Opperhuizen and Schrap (1987) examined the impact of aqueous oxygen concentration on uptake of
two polychlorinated biphenyl (PCB) congeners by guppies. Over the range of oxygen concentrations
tested (60%, 40%, and 25% of saturation) they saw no differences in uptake of either chemical and
suggested that a drop in chemical extraction efficiency occurred as ventilation volume increased in
response to lower oxygen saturations. Based on these observations, the authors concluded that diffusional
constraints have more impact on total chemical flux at the gill than changes in water flow. The results
of McKim and Goeden (1982) suggest that this conclusion does not apply at higher oxygen concentrations
(>60% of saturation), where uptake appears to be related to ventilation volume, at least for some fish.