In the early 1980’s scientists in Britain noticed a decline in numbers of whelks Thais lapillus, especially around marinas.  Later, the same situation was noted in other parts of the world, including the west coast of North America.  The problem was traced to contamination from tributyltin (TBT), a component of anti-fouling paints used on boats at that time.  The tin component leaches slowly from the paint and is lethal to settling larvae and spores.  It also interferes with the endocrine control of secondary sexual characteristics in neogastropods, and manifests as the imposition of male sexual organs (penis and vas deferens) in females.  The condition is termed “imposex”.  The effect occurs in just a few months, is irreversible, and leads to sterilisation of females and, ultimately, to demise of the whelks.  The presence of imposex in neogastropods is now widely acknowledged as symptomatic of the past presence of TBT in the seawater (sensitive at levels down to 1 ng/liter).  A worldwide programme of elimination of tributyltin from anti-fouling paints has eased the problem.  Stickle et al. 1990 J Exper Mar Biol Ecol 143: 165.

In a normal female whelk such as Nucella lamellosa the fertilised eggs pass through a capsule gland where up to several hundred at a time are enclosed in capsules (see generalised drawing on Left).  The female releases the capsules via its genital pore and attaches them to the sea bottom.  In an area contaminated by tributyltin, a vas deferens begins to form near the genital pore in the female and lengthens towards the head region.  In time, a small bump appears just posterior to the right tentacle that eventually enlarges to become a non-functional penis.  Soon, the vas deferens overgrows and blocks the genital pore as a thickened pad (see drawing on Right). The female N. lamellosa is now functionally sterile, and any eggs present in the capsule gland are resorbed. 

Not all neogastropods are affected in the same way, and the females of some species, while developing a vas deferens and penis, may not become sterile.  Studies of imposex in neogastropods around the southern end of Vancouver Island, British Columbia, for example, show varying levels of manifestation of the condition.  Note that in Nucella ostrina the vas deferens thickens around the opening of the genital pore, but may not completely block it.  Similarly, in neither of the species N. canaliculata nor Lirabuccinum dirum is the genital pore occluded.  Thus, of the 4 species figured here, only Nucella lamellosa is almost certain to become sterile. Bright & Ellis 1990 Can J Zool 68: 1915. Photographs of N. canaliculata and L. dirum below courtesy Linda Schroeder, Pacific Northwest Shell Club, Seattle, WA PNWSC.

Studies on several species of neogastropods collected at 11 locations in British Columbia show a marked reduction in incidence in imposex from 1989 when Canadian government legislation was enacted to restrict TBT usage to vessels greater than 25m in length (see histogram).  However, while federal legislation or other guidelines on use of TBT for antifouling purposes are in place in most or all developed countries, the authors of the study note that few developing countries are following suit.  They caution that without a total ban on TBT-based antifouling paints, ship repairs may shift progressively to countries with cheap labour and less stringent environmental regulations, with a resulting shift of an environmental problem from developed countries to countries least able to address them.  Tester & Ellis 1995 Mar Poll Bull 30: 90; Saavedra & Ellis 1990 Mar Poll Bull 21: 244; Tester et al., 1996 Envir Toxicol Chem 15: 560; data summary of these papers from Reitsema et al. 2002 Mar Pollut Bull 44: 257.  

NOTE  including  Nucella lamellosa, N. canaliculata, N. ostrina, and Lirabuccinum dirum. The histogram presents mean values for the 11 sites sampled. The proportion of N. lamellosa making up the histogram is not known

A recent study on whelks Nucella lima at 7 harbor-sites in Alaska reveals a 36-88% incidence of imposex in females at 3 of the sites.  At the same time, the author finds significant tributyltin (TBT) contamination in bay mussels Mytilus trossulus at 4 of the 10 harbours,  but with 2 of the sites showing reduced levels from those recorded in 1987.  The author expresses surprise at finding TBT and imposex at all in Alaskan waters, as TBT-bearing paints have been banned there for over 2 decades.  Tallmon 2012 Bull Envir Contam Toxicol 88: 245. Photograph courtesy Linda Schroeder, Pacific Northwest Shell Club, Seattle PNWSC.

NOTE  in contrast, researchers comparing tributyltin contamination in estuarine shipyard areas on east and west coasts of North America report relatively low TBT levels in Nucella spp. in Puget Sound, Washington, suggesting that regulations prohibiting the use of TBT-based antifoulant paints in this area are yielding favourable results.  Evans et al. 2001 Invert Repr Dev 39 (3): 221

Nucella lima