Environmental estrogens suppress hormones, behavior, and reproductive fitness in male fathead minnows

This study explored the possibility that environmental estrogens in sewage effluent may reduce the reproductive fitness of adult male fish by suppressing their reproductive behaviors, including their ability to compete for nests and females. Male fathead minnows (Pimephales promelas) were exposed for three weeks to either blank control, effluent released by a sewage treatment plant (STPE), waterborne estradiol (E2), or a synthetic androgen (methyltestosterone [MT]). Afterward, fish were placed with females and a nest, and their behavior was monitored for 5 d in either the presence or the absence of a competing (unexposed control) male. Males exposed to either the STPE or E2 (approximately 50 ng/L, a level chosen to mimic the estrogenic content of the STPE) had elevated levels of circulating vitellogenin (p < 0.05) and lower levels of 11-ketotestosterone (KT; p < 0.05). Nearly all STPE- and E2-exposed males spawned successfully in the absence of a competing male, but in both cases, exposed males suffered nearly total reproductive failure when they had to compete. Conversely, males exposed to MT (approximately 50 ng/L) outcompeted control males. Behavioral observations suggested that subtle differences in agonistic behaviors, typically associated with circulating androgens (i.e., KT), were responsible. We speculate that male fish exposed to estrogenic effluent in the field are less likely to reproduce successfully within large populations of wild fish, thereby causing abnormal and potentially detrimental patterns of gene flow within those populations.