Oehlmann, J, U Schulte-Oehlmann, M Tillmann and B Markert. 2000. Effects of endocrine disruptors on Prosobranch snails (Mollusca: Gastropoda) in the laboratory. Part I: Bisphenol A and Octylphenol as xenoestrogens. Ecotoxicology 9:383-397.
Oehlmann et al. report that bisphenol A and octylphenol create "superfemale" snails at extremely low levels, indeed the lowest doses they tested, which are well within the range of exposures encountered in the environment.
What did they do? The authors exposed two species of snail, one from freshwater habitatsthe ramshorn snail Marisa cornuarietis the other from salt waterthe dogwhelk Nucella lapillusto varying concentrations of bisphenol A and octylphenol (1 µg/L to 100 µg/L, or approximately 1 part per billion to 100 ppb), and examined the consequences of exposure on morphology and reproduction in the two snails. The experiments tested the direct effects on exposed adults of both species, plus an additional test on Marisa looking at the impact of BPA and OP on development from the egg. This latter test examined hatching success of the offspring of animals exposed during development.
What did they find? Oehlmann et al. found that two species of snail were quite sensitive to BPA and octylphenol at levels of contamination comparable to those regularly encountered in the natural environment.
Exposed adults of both species responded even to the lowest level of exposure with a "complex syndrome of morphological and physiological alterations." The female genital system was malformed while spawning mass and egg production were increased. Oehlmann et al. called these "superfemales." According to the authors, they had never seen this phenotype in their laboratory before, even though they had examined more than 8000 specimens during the previous decade.
The details of the changes in the female reproductive tracts differed between the two species:
In Marisa, they observed dramatic excessive growth ("hypertrophy") of the two female glands and enhanced production of spawning mass (eggs and fluid), which was so extreme that it ruptured the pallial oviduct in almost 4% of cases, resulting in the animal's death. Rupturing occurred at all levels of BPA exposure (above 0), irrespective of the applied concentration.
The dose-response curve for Marisa treated with octylphenol revealed a dramatic nonmonotic form: intermediate levels of exposure produced a much greater change in spawning masses per female and eggs per female than did lower or higher exposures.
Nucella females also developed the "superfemale" phenotype, with an increase in egg production and expansion of the pallial female sex glands. No rupturing occurred, however, because of a difference in the anatomy of Nucella compared with Marisa.
Nucella males were also affected while Marisa males were not. Fewer males had sperm in the seminal vesical, and penis and prostate glands were reduced in size, enough to raise the possibility that they were incapable of breeding successfully.
In the tests performed on Marisa developing from eggs (not done with Nucella), Oehlmann et al. found that while neither BPA or OP decreased hatching success, the two contaminants produced effects comparable to those observed in the adult tests (above). The enhancement of spawning mass and egg production was less marked at the highest level of exposure for the animals raised from eggs than those exposed only in adulthood. Ohelmann et al. suggest this may be a result of desensitization of those exposed in the egg which could be a result of down-regulation of estrogen receptors.
In Marisa exposed as developing eggs, there was also a striking increase in the frequency of imposex. Ohelmann et al. interprete this as a possible result of the up-regulation of androgen receptors.
What does it mean? "Invertebrates, like vertebrates, are sensitive to endocrine disruption at environmentally relevant concentrations." The contamination levels used by Oehlmann et al. are well within the range of values found in marine and freshwater sediments, indeed they are phenomenally low. Moreover, they found impacts at the lowest level tested (1 part per billion) and thus effects at lower levels are likely.
Of particular importance here is that the effects reported by Oehlmann et al. are inarguably adverse and likely to have impacts at the population level of these snails.