Endocrine Disruption in Aquatic Organisms Invertebrates

In 1970, Blaber [6] reported that many female dogwhelks (Nucella lapillus) in Plymouth Sound (UK) had a penis-like structure behind the right tentacle. This was the first report of what is now probably the clearest, and best documented, case of endocrine disruption in any organism. It is so because there is unequivocal evidence, from both field and laboratory studies, on the cause of the mas-culinisation, the effects are well described, and the consequences of these effects, at both the individual and population level, are known. It is also the only documented example of endocrine disruption where remedial action has been shown to lead to recovery of populations of affected organisms [7].

Following Blaber's report [6], Smith [8] reported similar structural mas-culinisation of the American mud snail (Ilyanassa obsoleta) along the Connecticut coast. He coined the term imposex to describe these female snails which had a penis and a vas deferens (the sperm duct), the latter often disrupting the oviducts and hence egg laying. Nevertheless, it was a decade later that it was first suggested [9-11] that this superimposition of male characteristics in females was caused by exposure to antifouling paints, in particular tributyltin (TBT) and related compounds used as biocides.

A large amount of subsequent research (reviewed in [12]) has supported the earlier reports. For example, there is strong evidence from studies in coastal European [13] and American [14] waters of imposex in gastropod molluscs caused by TBT. Imposex has been observed in areas where the concentration of TBT is only 1 ng/l; where concentrations have reached 6-8 ng/l, complete reproductive failure and local extinctions due to sterility of females has occurred. Even in the middle of the North Sea (between the UK and the Netherlands), tens of miles from land, the incidence of imposex in a whelk (Buccinum undatum) has been strongly correlated with the intensity of shipping traffic.

Laboratory studies have been used to investigate the species specificity of the phenomenon of intersexuality caused by TBT, the dose-response relationship, the critical period when exposure causes imposex, the permanence of the effect, and the mechanism of action of TBT (specific references can be found in [12]). The latter issue is not yet completely resolved, although it seems likely that TBT acts as a competitive inhibitor of aromatase (the enzyme that converts androgen to oestrogen). TBT also appears to inhibit the conjugation of androgens (which would normally de-activate these steroid hormones). Both mechanisms of action would lead to elevated androgen concentrations, and hence masculinisation.

Because the 'TBT story" is so well documented (and accepted), the pressure to ban the use of TBT-based antifouling paints has grown relentlessly, and it looks presently as though a world-wide ban can be achieved in the next few years. Hopefully, a ban would lead to the recovery of mollusc populations.

Ironically, other than this extremely well documented example of endocrine disruption in some species of molluscs, there is very little evidence available presently to suggest that any other invertebrates are adversely affected by endocrine disrupting chemicals (EDCs). Of course this absence of evidence does not imply that other groups of invertebrates are not experiencing endocrine disruption, but rather that the necessary studies do not appear to have been undertaken yet (though some are in progress). Some recent laboratory-based studies (e.g. [15]) have shown that reproduction of water fleas (daphnids) is affected by exposure to nonylphenol, an oestrogenic xenobiotic, but such studies are at a very early stage, and the significance of the results is presently unclear. Aquatic invertebrates are a very large, very heterogeneous group of organisms, often with unique hormones (e.g. the ecdysteroids, which are not found in vertebrates), that deserve serious study. I would not be at all surprised if other examples (besides TBT-induced imposex in some molluscs) of endocrine disruption in aquatic invertebrates came to light.

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