Feed-borne exposure to zearalenone impairs reproduction of rainbow trout

To assess the effects on rainbow trout reproduction of feed contamination with zearalenone (ZEN) at the current European guidance value (2 mg∙kg−1 feed), we performed a life-cycle feeding trial under aquaculture conditions. The trial began when the fish larvae commenced external feeding and continued for 96 weeks, up to the point when the fish reached sexual maturity. To compare the reproductive development of the exposed and control fish, histological and molecular observations and analyses were performed at 12, 72, and 96 weeks of the feeding trial. To investigate the effect of ZEN exposure on the fertility of male and female fish, gametes obtained from mature fish were fertilized, after which offspring mortality was tracked at the eyed egg, hatched, and swimming larva stages. The mortality data were also used to estimate the risk of offspring death depending on the parental exposure scenario. We observed that feed-borne exposure to ZEN resulted in abnormal development of the fishes' gonads, and the occurrence of intersex fish and sex-reversed (feminized) males. These observations suggest that ZEN could have interfered with sex differentiation of the exposed fish at an early stage of their reproductive development. Our data indicate that the feed-borne exposure to ZEN probably did not affect the timing of sexual maturation or the relative fecundity of the female fish, but they suggest it might have led to advanced ovarian development. Moreover, ZEN-exposed male fish had a higher mean sperm concentration and markedly higher plasma levels of vitellogenin than males in the control group. These findings suggest that males could be more susceptible to the detrimental effects of ZEN than females. Importantly, offspring of fish that were fed with ZEN-contaminated feed throughout their whole reproductive cycle had a higher mortality risk than offspring of fish that were fed blank feed. Moreover, the offspring of parents that were only exposed to ZEN during the last 17 weeks of feeding before spawning also had a markedly increased mortality risk. Together, these findings not only demonstrate that ZEN harms rainbow trout reproductive outcomes, but also indicate that fish at sexual maturation may be especially vulnerable to ZEN contamination in feed. Our findings raise concerns about the safety of the current recommended guidance values for ZEN in feed and feedstuff used in aquaculture and suggest a need to consider lowering the maximum allowable levels of this mycotoxin.