Page 85 - The Toxicology of Fishes

Toxicokinetics in Fishes 65

described as follows: (1) presentation to the absorbing epithelium in water or gut contents; (2) transport
across the epithelium into blood; (3) incorporation into blood, including binding to plasma proteins; (4)
transport via the systemic circulation of freely dissolved and plasma-bound chemical to various tissues;
and (5) transport from blood into tissues. The character of the external medium may substantially
determine which forms of a compound are presented to these exchange surfaces, thereby influencing
the overall rate of uptake. The external medium may also impact uptake through its effects on the
structure and function of the membrane itself. From mass-balance considerations, the rate of uptake
cannot exceed the rate at which chemical is presented to the exchange surface. Rates of diffusion across
the membrane barrier and removal by the circulatory system also have the potential to limit the overall
rate of chemical uptake.

The Gills
Branchial Structure and Function
The anatomy of fish gills reflects their primary function as a gas-exchange, osmoregulatory, and excretory
organ (Figure 3.3). Gill ventilation is accomplished using a two-phase pump system (Figure 3.3A). The
first phase involves suction generated by opening the opercular flaps that cover the posterior portion of
the branchial cavity. This draws water through the mouth into the buccal cavity. The second phase utilizes
pressure, generated by the contraction of muscles lining the buccal cavity, to force water from the buccal
cavity through the gill arches into the opercular cavity. During the pressure phase of the respiratory
cycle, the oral valve prohibits water flow out of the mouth and directs water over the respiratory surface.
The respiratory surface, where branchial uptake of oxygen occurs, is composed of eight gill arches,
four on each side of the branchial cavity. Each gill arch has two rows of gill filaments, and each filament
is covered, top and bottom, with gas-exchange units called secondary lamellae (Figure 3.3B). The
lamellae are thin-walled, sac-like structures composed of two epithelial cell layers held together by
numerous pillar cells (Figure 3.3C). These pillar cells create a blood space between the two epithelial
layers. Oxygen-depleted venous blood flows through the lamellae, while oxygen-rich inspired water
flows between the lamellae. In most species, blood and water flow in opposite directions, creating an
efficient counter-current system for gas exchange. Oxygen that diffuses across the lamellar epithelium
binds to hemoglobin and is transported by blood to the tissues where it is utilized. Diffusion of oxygen
from the blood into tissues occurs at a rate dependent on the concentration gradient between the blood
and individual cells of the tissues. A general model for gas transfer in teleosts is presented in Figure 3.3D.
Emphasis in this chapter is placed on those aspects of normal gill function that control branchial
uptake of xenobiotic compounds. For further information on respiratory function in teleosts, the reader
is referred to pertinent reviews (Perry and McDonald, 1993; Piiper and Scheid, 1984; Randall and
Daxboeck, 1984). For detailed discussions of gill anatomy, see Hughes (1984) and Laurent (1984).
Additional reviews cover osmotic, ionic, and acid–base regulation (Evans, 1993; Heisler, 1993;
McDonald, 1983) and excretory function (Wood, 1993).

Branchial Absorption of Xenobiotics
The anatomical and physiological features of fish gills that promote efficient exchange of respiratory
gases also contribute to uptake of xenobiotic compounds directly from water—namely, a thin membrane
separating blood and water, large surface area, and high rates of counter-current blood (perfusion) and
water (ventilation) flow. Direct measurements of chemical uptake across fish gills have been obtained
using fish respirometer-metabolism chambers, which separate inspired and expired water flows (McKim
and Goeden, 1982; McKim and Heath, 1983). Using this model system, McKim et al. (1985) measured
branchial uptake rates in adult rainbow trout (Oncorhynchus mykiss) for a heterogeneous group of organic
chemicals. These measurements suggested a consistent relationship between the uptake rate of a chemical
and its relative hydrophobicity, as indicated by the log of its octanol–water partition coefficient (log K ;
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Figure 3.4A). Rate constants measured in subsequent studies with rainbow trout (Bradbury et al., 1986;
McKim et al., 1986, 1987a,b) further substantiated this relationship. Uptake rates were low for chemicals
with log K values less than 1, increased about fourfold between log K 1 and 3, leveled off between
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log K 3 and 6, and declined when log K exceeded 6. Working with a series of phenols, anisoles, and
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