Predicted exposures to steroid estrogens in U.K. rivers correlate with widespread sexual disruption in wild fish populations

Abstract

Steroidal estrogens, originating principally from human excretion, are likely to play a major role in causing widespread endocrine disruption in wild populations of the roach (Rutilus rutilus), a common cyprinid fish, in rivers contaminated by treated sewage effluents. Given the extent of this problem, risk assessment models are needed to predict the location and severity of endocrine disruption in river catchments and to identify areas where regulation of sewage discharges to remove these contaminants is necessary. In this study we attempted to correlate the extent of endocrine disruption in roach in British rivers, with their predicted exposure to steroid estrogens derived from the human population. The predictions of steroid estrogen exposure at each river site were determined by combining the modeled concentrations of the individual steroid estrogens [17beta-estradiol (E2), estrone (E1), and 17alpha-ethinylestradiol (EE2)] in each sewage effluent with their predicted dilution in the immediate receiving water. This model was applied to 45 sites on 39 rivers throughout the United Kingdom. Each site studied was then categorized as either high, medium, or low "risk" on the basis of the assumed additive potency of the three steroid estrogens calculated from data derived from published studies in various cyprinid fish species. We sampled 1,438 wild roach from the predicted high-, medium-, and low-risk river sites and examined them for evidence and severity of endocrine disruption. Both the incidence and the severity of intersex in wild roach were significantly correlated with the predicted concentrations of the natural estrogens (E1 and E2) and the synthetic contraceptive pill estrogen (EE2) present. Predicted steroid estrogen exposure was, however, less well correlated with the plasma vitellogenin concentration measured in the same fish. Moreover, we found no correlation between any of the end points measured in the roach and the proportion of industrial effluents entering the rivers we studied. Overall, our results provide further and substantive evidence to support the hypothesis that steroidal estrogens play a major role in causing intersex in wild freshwater fish in rivers in the United Kingdom and clearly show that the location and severity of these endocrine-disrupting effects can be predicted.

Figure 1

Sex ratios of roach sampled. (A) The proportions of each sex at each study site. (B) Sex ratios of roach sampled (pooled data). Significant difference from the expected sex ratio (50:50): *p = 0.05.

Figure 2

The proportion of “male” roach with oocytes in their testes or feminized reproductive ducts from pooled high- (> 10 ng E₂ equivalent/L), medium- (1–10 ng/L), and low-risk (< 1 ng/L E₂ equivalent) sites. Significant differences from the expected sex ratio at the following significance levels: *p = 0.05, **p = 0.01, #p = 0.001.

Figure 3

Relationship between the incidence of oocytes in the testes of roach caught from high-, medium-, and low-risk categories and age of roach at capture. Each point represents an individual site within each category.

Figure 4

(A) Mean intersex index values in pooled samples of roach collected from predicted high-, medium-, and low-risk sites. The number of oocytes within the testes was assessed using the intersex index (0–7). The mean of the scores (six sections per fish) for all intersex fish was used to derive the intersex index for each group of fish. Both the absolute index (fish with ovotestes only, striped bars) and the combined index (including the males and intersex fish with no oocytes in testes, solid bars) are shown. (B) Average intersex index for each age group of fish and for each category (high-, medium-, and low-risk). Error bars indicate SD. Significant differences from the low-risk category: *p = 0.05, **p = 0.01.

Figure 5

Monthly variation in VTG concentrations in female (A), intersex (B), and male (C) roach within each of the predicted risk categories: high-risk , > 10 ng E₂ equivalent/L; medium-risk, 1–10 ng/L; low-risk, < 1 ng/L. The month in which the fish were sampled is also shown. All sites were within 9 km of a sewage effluent input. Error bars indicate SD. Significant difference from the low-risk category: *p = 0.05, **p = 0.01, ^#p = 0.001.