Acidic Seawater can Promote Larval Metamorphosis in the Marine Mud Snail, Nassarius obsoletus

Elevated levels of atmospheric CO2 have had the unintended effect of acidifying the world's oceans by at least 0.1 pH unit since the beginning of the industrial revolution. Current models of the effects of continued CO2 release anticipate a further increase in ocean acidity by 0.14 to 0.4 pH units by the end of this century. Numerous marine organisms with calcareous shells or exoskeletons are expected to undergo deleterious effects, including shell or exoskeletal dissolution or calcification with increased metabolic costs. While many studies have documented potential effects of ocean acidity on adult calcareous organisms, less work has focused on embryonic or developmental changes. Alterations in ocean biochemistry can affect metabolic processes beyond calcification, and our investigations into the development of the local intertidal mudsnail, Nassarius obsoletus, led us to hypothesize that rising ocean acidity would increase incidents of larval shell decalcification, decrease larval growth rates, and induce precocious metamorphosis. As an initial study of potential effects of future acidic conditions on larval N. obsoletus, we raised larvae in seawater adjusted to lower than normal pH levels with hydrochloric acid (HCl), measured larval growth every 5 days in 15 randomly selected individuals from each culture, and conducted experiments on larval metamorphosis in physiologically competent larvae. We found no major trend in growth patterns of larvae from pH 8.2 to 7.7. However, results from a number of pharmacological experiments demonstrated that larvae grown in acidic conditions metamorphose more readily than controls. Our investigations are far from a definitive exploration of the effects of oceanic acidity on the development of this marine mollusc, but our data suggest that key developmental processes in marine invertebrates may be influenced in unexpected ways by continued climatic changes.

A Comparison of the Effectiveness of Tri-N-Butyltin Chloride and Five other Organotin Compounds in Promoting the Development of Imposex in the Dog-Whelk, Nucella Lapillus

Populations of the common dog-whelk Nucella lapillus (L.) are declining or have already disappeared at many sites on rocky shores around the United Kingdom (Bryan et al. 1986). There is conclusive evidence that this is caused mainly by tributyltin (TBT) compounds leached from ships' antifouling paints (Bryan et al. 1987). These compounds impose male sexual characters (or imposex) on female N. lapillus. Other stenoglossan gastropods including Nassarius obsoletus Say (Smith, 1981a) and Ocenebra erinacea (L.) (Féral & Gall, 1982) are similarly affected by TBT. The intensity of expression of imposex in N. lapillus can generally be related to the sea water concentration of TBT. The appearance of a small penis and the partial development of a vas deferens first occurs at TBT concentrations below 0.5 ng/1 (as tin), although reproduction appears to be unaffected at this level. At 1–2 ng Sn/1 penis size is markedly increased and in some females proliferation of vas deferens tissue overgrows the genital papilla, thus sterilizing the animal. At slightly higher concentrations virtually all females become sterilized and at around 10 ng Sn/1 oogenesis is suppressed and spermatogenesis initiated (Gibbs, Pascoe & Burt, 1988). Since development is direct and there is no planktonic stage, N. lapillus has a very limited capacity for dispersion: thus the sterilization of females heralds the almost certain decline of so affected populations (Gibbs & Bryan, 1986).

The effects of tributyltin (TBT) accumulation on adult dog-whelks, Nucella lapillus: long-term field and laboratory experiments

Populations of the gastropod, Nucella lapillus (L.), normally one of the commonest of rocky-shore macroinvertebrates, have recently suffered from declining numbers at many sites along the south coast of England. Bryan et al. (1986) showed that these declining populations exhibited a high degree of imposex (the induction of a penis and vas deferens in females) and that imposex was almost certainly caused by tributyltin (TBT) compounds leached from ships' antifouling paints. Evidence implicating TBT compounds in the development of imposex included: (1) a good relationship between the degree of imposex and the proximity of affected populations to harbours and marinas; (2) in Plymouth Sound, the degree of imposex increased dramatically between its discovery in 1969 (Blaber, 1970) and 1985, thus coinciding with the introduction and increasing usage of TBT-based paints; (3) tissue concentrations of tin as TBT increased consistently with the degree of imposex; (4) animals transplanted from a ‘clean’ area to a harbour site absorbed TBT and developed imposex; (5) preliminary experiments showed that imposex was induced by exposure to 20 ng/1 of tin as TBT leached from a TBT-based paint; (6) TBT is implicated in the induction of imposex in other stenoglossan gastropods including Nassarius obsoletus (Say) (Smith, 1981) and Ocenebra erinacea (L.) (Féral & Gall, 1982).

The use of the dog-whelk, Nucella lapillus, as an indicator of tributyltin (TBT) contamination

The term ‘imposex’ was coined by Smith (1971) to describe the superimposition of male characters onto unparasitized and parasitized females of gonochoristic gastropods. In Nassarius obsoletus (Say) the development of imposex results in the female having one or more of the following characters: (1) a penis with a duct leading to (2) a vas deferens which passes back to the ventral channel of the capsule gland and (3) convolution of the normally straight gonadial oviduct (Smith, 1980). Imposex in the similarly gonochoristic Nucella lapillus (L.) was first noted by Blaber (1970) who found females with penis-like outgrowths in Plymouth Sound populations. Subsequent studies (Bryan et al. 1986; Gibbs & Bryan, 1986) have demonstrated that the incidence and intensity of imposex have since increased markedly in the same populations and that the phenomenon is widespread around south-west England.