Academic journal article Environmental Health Perspectives

Long-Term Exposure to Environmental Concentrations of the Pharmaceutical Ethynylestradiol Causes Reproductive Failure in Fish

Academic journal article Environmental Health Perspectives

Long-Term Exposure to Environmental Concentrations of the Pharmaceutical Ethynylestradiol Causes Reproductive Failure in Fish

Article excerpt

Heightened concern over endocrine-disrupting chemicals is driven by the hypothesis that they could reduce reproductive success and affect wildlife populations, but there is little evidence for this expectation. The pharmaceutical ethynylestradiol (E[E.sub.2]) is a potent endocrine modulator and is present in the aquatic environment at biologically active concentrations. To investigate impacts on reproductive success and mechanisms of disruption, we exposed breeding populations (n = 12) of zebrafish (Danio rerio) over multiple generations to environmentally relevant concentrations of E[E.sub.2]. Life-long exposure to 5 ng/L E[E.sub.2] in the [F.sub.1] generation caused a 56% reduction in fecundity and complete population failure with no fertilization. Conversely, the same level of exposure for up to 40 days in mature adults in the parental [F.sub.0] generation had no impact on reproductive success. Infertility in the [F.sub.1] generation after life-long exposure to 5 ng/L E[E.sub.2] was due to disturbed sexual differentiation, with males having no functional testes and either undifferentiated or intersex gonads. These [F.sub.1] males also showed a reduced vitellogenic response when compared with [F.sub.0] males, indicating an acclimation to E[E.sub.2] exposure. Depuration studies found only a partial recovery in reproductive capacity after 5 months. Significantly, even though the [F.sub.1] males lacked functional testes, they showed male-pattern reproductive behavior, inducing the spawning act and competing with healthy males to disrupt fertilization. Endocrine disruption is therefore likely to affect breeding dynamics and reproductive success in group-spawning fish. Our findings raise major concerns about the population-level impacts for wildlife of long-term exposure to low concentrations of estrogenic endocrine disruptors. Key words: ecotoxicology, endocrine disruption, ethynylestradiol, mating systems, population effects, reproductive success, zebrafish. Environ Health Perspect 112:1725-1733 (2004). doi: 10.1289/ehp.7209 available via http://dx.doi.org/ [Online 4 November 2004]

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Major worldwide attention has focused on the possibility that disruption of reproductive systems by endocrine-disrupting chemicals (EDCs) may be affecting the reproductive health of wildlife populations (Guillette and Gunderson 2001; Kime 1998; Tyler et al. 1998; Van Der Kraak 1998) and possibly, of humans (Colborn and Clement 1992; Ohtake et al. 2003). In fish, exposure to EDCs alters their reproductive physiology and morphology (Kime 1998; Tyler et al. 1998), resulting in, for example, the induction of female-specific proteins in male fish (Tyler and Routledge 1998), induction of gonopodia in females (Bortone and Davis 1994), reduced sperm counts (Haubruge et al. 2000), skewed sex ratios (Larsson et al. 2000), and prevalence of intersexuality (Jobling et al. 1998). Concern over the effects of EDCs on wildlife is driven by the hypothesis that disruption to the reproductive system may have serious deleterious consequences on the reproductive success of populations, but there is little evidence bearing on this expectation. An exception to this in a natural population is recent work on the roach (Rutilus rutilus); this study shows that sexual disruption (intersex) as a consequence of exposure to sewage treatment works effluents (STWs)--which contain a complex mixture of EDCs--results in gametes with reduced fertilizing capacity, as determined by in vitro studies (Jobling et al. 2002b). Direct population-level consequences of exposure to a specific EDC are known only for the antifouling agent tributyltin, which disrupts steroidogenesis, inducing an imposex condition that reduces reproductive success and causes localized extinctions in marine gastropods in the United Kingdom (Gibbs et al. 1991; Matthiessen and Gibbs 1998).

Many EDCs have a weak capacity to disrupt reproductive function. In contrast, natural steroidal estrogens control sexual differentiation and/or development in vertebrates and are potent modulators of sexual development and capacity (Bern 1992; Dawson 1998; Nagahama 1994; Strussmann and Nakamura 2002). …

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