Endocrine-Disrupting Chemicals and Their Environmental Impacts - Organic Pollutants: An Ecotoxicological Perspective - page 272

the sole contributing factor. As a final note in the alligator story, it is very difficult
to control the dose to the embryo for applications of chemicals to the outside of the
egg, and as no dose verifications were provided in the previously mentioned studies,
some have questioned the robustness of the cause-effect relationship drawn between
DDT/PCBs and sexual disruption in alligators in Lake Apopka (Muller et al. 2007).
15.4.2 TbT a n d i m p o s e x i in m of l l u s k s
In 1981, Smith reported the occurrence of imposex, the expression of a penis and/
or a vas deferens in females of the marine gastropod Nassarius obstoletus, and
hypothesized that the antifouling agent tributyl tin (TBT) was responsible. This was
subsequently proved by Gibbs and Bryan for imposex in the dog whelk ( Nucella
lapillus ), which resulted in reproductive failure and population level declines in this
species (Bryan et al . 1986; Gibbs and Bryan 1986). The imposex condition has now
been reported over extensive geographical regions and in over 150 species of marine
mollusks (Matthiessen and Gibbs 1998). Extensive laboratory-based exposures have
shown that imposex is induced by TBT in adults at concentrations as low as 5 ng
TBT/L in the water (Gibbs et al . 1988) and in juvenile or larval dog whelks at expo-
sure concentrations of only 1 ng TBT/L (Mensink et al. 1996). Concentrations of TBT
in some harbors and in busy shipping lanes exceeded 30 ng/L (Langston et al. 1987).
Environmental concentrations of TBT therefore were, and in some areas still are, suf-
ficient to induce imposex in some marine mollusks. The unequivocal evidence that
TBT has caused population-level declines, and even localized population extinctions,
in marine mollusks, led to its ban from use on ships less than 25 m in the United
Kingdom in 1987 and from 1982 in France. The International Maritime Organisation
has phased out TBT, and a complete ban of TBT on all European vessels was imposed
in January 2008. In areas where TBT is no longer used, there has been recovery in the
populations of marine mollusks (Waite et al. 1991; Rees et al. 2001).
The mechanisms through which TBT masculinizes female gastropods are still
uncertain. One hypothesis is that TBT acts as an inhibitor of aromatase, restrict-
ing the conversion of androgen to estrogen and/or that it inhibits the degradation of
androgen, both of which would cause higher levels of circulating androgen (Bettin
et al . 1996). Oberdörster and McCelland-Green (2002) argued that TBT acts as a
neurotoxin to cause abnormal release of the peptide hormone Penis Morphogenic
Factor. A more recent study (Horiguchi et al . 2007) provides persuasive evidence
that TBT acts through the retinoid X receptor (RXR); the suggestion is that RXR
plays important roles in the differentiation of certain cells required for the devel-
opment of imposex symptoms in the penis-forming area of females. Interestingly,
despite the known harmful effects of TBT, it is still used widely as an antibacterial
agent in clothes, nappies, and sanitary towels, providing further routes of entry into
the environment (via landfills, etc.). Triphenyl-tin (TPT), which is widely used as
a fungicide on potatoes and to control algae in rice fields (Strmac and Braunbeck
1999), has been shown to induce sexual disruption in various species of gastropods at
environmentally relevant concentrations (Schulte-Oehlmann et al . 2000; Horiguchi
et al. 2002; Santos et al . 2006) as well as causing a delay in hatching and producing
histological alterations in the gonads of zebrafish (Strmac and Braunbeck 1999). We