Page 34 - The Toxicology of Fishes

14 The Toxicology of Fishes

1. They process large volumes of water, ranging from several to hundreds of times the volume
of the fish per hour, and are supplied by a large blood flow (typically about an order of magnitude
lower than the water flow).
2. They have a large surface area with a small distance separating water and blood. To accomplish
this, gills contain a grid of numerous small, parallel, plate-like structures called secondary
lamellae. Each pair of lamellae delimits a narrow channel through which water flows, and each
lamella contains a blood space separated from the water by a thin layer of epithelial tissue.
3. Within the gill lamellar system, blood and water generally flow counter-current to each other,
which improves the efficiency of transfer of material between the two. This combination of
counter-current exchange, large surface area, and short diffusion distance results in highly
efficient extraction of the small concentrations of oxygen present in water. This high extraction
efficiency also depends on oxygen being (a) a small, neutral molecule that readily diffuses
across lipid cellular membranes, and (b) strongly bound to hemoglobin in blood (which helps
to maintain steep diffusion gradients between water and blood as they flow through the gill).
4. Gill epithelial tissue contains a variety of biochemical systems that regulate or otherwise affect
the exchange of various chemicals between blood and water passing through the gills. Sites
on the cellular membranes for ion exchange (transport proteins, ion channels) can serve as
uptake sites for toxic chemicals with suitable physicochemical properties.
5. Because of the chemical exchanges that are part of their normal functions, gills create a chemical
environment adjacent to their surface that can differ markedly from that of the surrounding
water. Due to excretion of carbon dioxide and ammonia, the pH at the gill surface of a fish
can differ from that in the surrounding water (Lloyd and Herbert, 1960; Playle and Wood,
1989; Wright et al., 1991). Gill epithelial cells are also covered by a thin layer of polysaccharide
mucus, which can affect chemical speciation at the gill surface and in the adjacent water (Tao
et al., 2002).
Figure 2.3 illustrates transport pathways and chemical reactions that can be important for the uptake
of toxic chemicals at fish gills. For simplicity, just two species of a toxic chemical (T) are shown
here—that which is bound to some other chemical constituent (B) in water or blood and that which is
not bound (free). These two species are connected by a double arrow to represent the speciation reaction
by which they interconvert. Sometimes speciation reactions are slow enough that chemical species will
not change during passage through the gill; however, many reactions are fast enough that chemical
species can be altered within the gill, with possible consequences for uptake rates and bioavailability.
As the toxic chemical is swept along the water channel, free chemical can be absorbed into the
epithelial tissue via various routes and mechanisms. If the chemical can readily cross lipid cellular
membranes, a principal route of uptake will be passive diffusion across the epithelial tissue (arrow 1 on
Figure 2.3). Other chemicals might have the appropriate size and electrochemical properties to be taken
up via specific biochemical exchange sites on the epithelial tissue surface (arrow 2 and rectangular S).
A significant site for ion loss in freshwater fish can be via junctions between epithelial cells. These
junctions are not depicted on Figure 2.3 but might also be important for the uptake of chemicals that
are not effectively absorbed via other routes.
The bound chemical might also be directly absorbed via one or more of the same routes as the free
chemical, although probably at a different rate (arrow 3); however, the bound chemical can also affect
uptake in other ways. If absorption of the free chemical significantly reduces its concentration within
the lamellar channel and if the speciation reaction is fast enough, net dissociation of the bound chemical
(arrow 4) will replenish the free chemical concentration, supporting additional uptake. In this way, the
bound chemical can be considered bioavailable, even though it is not directly absorbed. Such shifts in
speciation equilibrium require significant net absorption of the chemical during passage through the gill,
and so will be important only when chemical concentrations in fish are below those in equilibrium with
the surrounding water. This will be true during the early stages of exposure to a chemical but can also
be true at steady state if the chemical is rapidly metabolized or eliminated via routes other than the gill.
These uptake relationships can be modified by the chemical characteristics of the water in the gill
lamellar channels (C in Figure 2.3). This chemistry is a function of both the incoming exposure water