Page 996 - The Toxicology of Fishes

976 The Toxicology of Fishes

al., 1997). In contrast, vitellogenic responses were seen in fish up to 1.5 km and 4.5 km downstream of
discharges in the River Arun and River Lea, respectively (Harries et al., 1995, 1997) (Figure 25.3).
Simultaneous measurements of testicular weight—gonadosomatic index (GSI) = gonad weight ÷ (body
weight – gonad weight)—showed that the rate of testis growth was diminished at some, but not all, sites
compared with the laboratory controls. The most marked effects seen at any of the sites studied were
downstream of Marley STW on the River Aire in Yorkshire (Harries et al., 1997). This sewage treatment
works treats influent from wool-scouring plants and the textile industry, as well as from domestic sources
(see below). Significant elevations in concentrations of plasma VTG (that ranged between 25 and 52
mg/mL) were observed in the caged trout placed at all the sites along a 5-km stretch of the River Aire
below the effluent discharge from Marley STW (Figure 25.3). Simultaneous measurements of the
hepatosomatic index (HSI), which is equal to the liver weight ÷ (bodyweight – liver weight) and is an
indicator of metabolic load/activity, showed that it was elevated in the fish at all the sites along the
surveyed stretch of river. Furthermore, testis growth was significantly reduced in the trout at all study
sites on the Aire. Subsequent to these findings with caged fish in the River Aire, tighter discharge limits
and effluent treatment processes at source were introduced for the industries discharging alkylphenolic
chemicals into this river through the Marley STW, and this action has resulted in a gradual reduction in
the estrogenic effects seen (VTG induction) (Sheahan et al., 2002a,b). From the caged trout work, it
was clear that the estrogenic activity in some rivers in the United Kingdom was not limited to areas
immediately surrounding STW outfalls but rather persisted along significant stretches of rivers

Widespread Sexual Disruption in Wild Fish in English Rivers
Following the discovery of estrogenic activity in some U.K. rivers, a critical issue to address was whether
the concentrations of estrogenic chemicals in the river were sufficient to exert adverse reproductive
effects in wild fish. In fish, estrogens not only are responsible for VTG induction but also play important
roles in sexual maturation (Bohemen and Lambert, 1981) and in sexual differentiation (Yeoh et al., 1996)
and induce hepatic synthesis of vitelline envelope (eggshell) proteins (Hyllner et al., 1991). In fish,
therefore, estrogens are vital for egg formation and provision of yolk for the developing embryo (Tyler
et al., 1998). The main naturally occurring estrogens in fish (as in all classes of vertebrates) are
estradiol-17β, estrone, and estriol. Both the amount of circulating endogenous natural estrogen and the
timing of its release into the blood are carefully controlled by the hypothalamic–pituitary–gonadal axis.
Inappropriate exposure to these estrogens (or their mimics) at critical times in the life cycle or at
uncharacteristic concentrations may cause adverse effects (Hunter and Donaldson, 1983; Milston et al.,
2003; Tyler et al., 1998). As an example, exposure to estrogens or estrogen mimics during the period
of sexual differentiation has been shown to induce sex reversal and intersexuality by altering the normal
developmental pathway of the reproductive ducts and the primordial germ cells such that they differentiate
in a manner opposite to that of the genotypic sex of the individual (Balch and Metcalfe, 2006; Gimeno
et al., 1996; Nash et al., 2004; van Aerle et al., 2002). Furthermore, exposure to estradiol-17β during
sexual maturation has been shown to inhibit gonadal growth and development in male trout (Jobling et
al., 1996). The possibility existed, therefore, that these reproductive effects might occur in wild popu-
lations of fish that were exposed to estrogenic substances in sewage effluents entering rivers.
In 1995, we undertook an extensive survey of wild roach in English rivers to determine whether sexual
disruption was occurring in wild fish exposed to STW effluent. In this study, the presence of developing
oocytes and/or an ovarian cavity in the testis of “male” roach was used as a diagnostic feature to
characterize intersexuality in the captured fish (Jobling et al., 1998; Nolan et al., 2001) (Figure 25.4 and
Figure 25.5). Roach of mixed age and sex were randomly sampled at locations upstream and downstream
of sewage treatment works on eight rivers and at five reference sites throughout England and Ireland.
The rivers selected for study varied with respect to the amount of sewage effluent they received, and,
whenever possible, the sampling sites were selected where a physical barrier occurred (such as a weir)
that separated the fish from the sites located upstream and downstream of the sewage treatment works.
These barriers would limit the movement of fish between the two populations; fish downstream of the
sewage treatment works could not migrate to the upstream population, although movement of fish from