Toxic Agents And Sex Change In The Sea

In the world of cold-blooded animals, skinny doesn't quite cut the mustard – especially if you're female. As a general rule, the bigger you are, the bigger your eggs, or the more offspring you are able to produce. Both of these things increase the chance of passing genes on to the next generation: bigger eggs mean a bigger food supply for the developing animal and more eggs mean there's a better chance of at least some of them surviving to adulthood.

This is why some animals start out as males but as they grow older and, more importantly, larger, they become female and make the most of being large! Animals that do this are known as protandrous hermaphrodites. A great example of this is the limpet, which after settling as a male, metamorphoses into a female, though the time required to make the change varies with environmental conditions and between species. Animals that go from male to female are known as protogynous hermaphrodites, rather than protandrous.

Limpets are thought to be protandrous because it is rare to find large males and small females. Instead, limpet surveys often find lots of small males, lots of large females and a mix at intermediate sizes. What's more, limpets of an intermediate size have been found to have both male and female sexual organs (gonads).

Sex detectives

Sexing a limpet is no easy process as inspecting their underside yields no obvious clues – only a large muscular foot. Instead, marine biologists often dissect a limpet to find out if it's male or female. This is where working out if it changes sex during its lifetime gets difficult. A dissected limpet is a dead limpet. No chance of seeing if he turns into a female later on.

Fortunately, a team from the Spanish National Museum of Sciences have developed a reliable method to sample sexual organs and let the limpet live on to a ripe old age. They do this by inserting a hypodermic needle through the tissue close to the shell, known as the mantle, to obtain a gonad biopsy. Using this technique, the team tagged and monitored specimens to suss out how their sex changed over time. During their investigations, they found that the endangered limpet, Patella feruginea, is not only capable of going from male to female, but from female to male, too! While all the studied limpets reached adulthood as the same sex (males), they were capable of repeatedly changing sex during their lifetimes.

What use is this to limpets, if bigger females mean better reproductive success? One possibility is that small females revert back to males early on, as they would only produce a few eggs. In doing this, they would have better success as males where – in limpets at least – reproductive success is less dependent on male size. But even some of the largest limpets were males, suggesting that the ability to alternate between male and female may be a way of keeping the relative number of male and female limpets constant. We know now that limpets are capable of two-way sex change, but there's still a lot of work to be done as the cues that trigger these changes have yet to be identified.

Don't you know that it's toxic?

Unfortunately, sex change is not always beneficial and can be induced by toxic compounds in the water column, or in the sediment. The compound that causes the most trouble for gastropods is tributyl tin (TBT), a chemical paint that used to be applied to boats to prevent animals from growing on them. These chemicals are known as antifouling agents and their production is a big business – with good reason. When marine animals cement themselves to boats, they increase the friction between the ship and the water; while one extra passenger makes little difference to how streamlined the ship is, several do. The increased friction means more energy is needed to power the ship to its destination, meaning the amount of fuel needed per journey increases and the cost of this adds up.

TBT was used in ship paint during the 1970s and 80s, but its use was restricted (in the UK) in 1987, following rapid declines in the population of the dogwhelk (Nucella lapillus). Together with many other gastropods, female dogwhelks were found to develop male sexual organs in the presence of TBT - a condition known as imposex. This caused a huge shift in the sex ratio of dogwhelk populations and the unusually high proportion of male dogwhelks meant there weren't enough reproductive females to replenish the population.

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The TBT ban has allowed dogwhelk populations to recover throughout much of the UK, but the compound takes a long time to break down and can leach from the sediment back into the water column. Despite France putting in a restriction on TBT use in 1982, dogwhelk populations were still suffering 7 years later!

Chemical antifouling agents are, by nature of their purpose, harmful to marine animals. If they weren't at least a decent deterrent, they wouldn't be able to do their job. The difficulty lies in making sure they only affect their target animals (cementing marine animals such as barnacles) and that their impact is restricted to their target area (the outside of the ship), rather than leaching into the water. In this respect, they are much like the pesticides of the ocean and their effects need careful monitoring. Biologists and engineers are working hard to develop alternatives to antifouling paints, including physical deterrents that make the ship's surface less suitable for settling on - watch this space!

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References

Crowe, T. P., Thompson, R. C., Bray, S. and Hawkins, S. J. Impacts of anthropogenic stress on rocky intertidal communities Journal of Aquatic Ecosystem Stress and Recovery 7 273-297 (2000)

Guallart, J. , Calvo, M. Acevedo, I. and Templado, J. Two-way sex change in the endangered limpet Patella ferruginea (Mollusca, Gastropoda) Invertebrate Reproduction and Development 57 247-253 (2013)

Magin, C. M., Cooper, S. P. and Brennan, A. B. Non-toxic antifouling strategies. Materials Today 13 36-44 (2010)

Rees, H. L., Waldock, R. Mathiessen, P. and Pendle, M. A. Improvements in the Epifauna of the Crouch Estuary (United Kingdom) Following a Decline in TBT Concentrations Marine Pollution Bulletin 42 137-144 (2001)

Spence, S.K, Bryan, G. W., Gibbs, P. E., Masters, D., Morris, L. and Hawkins, S. J. Effects of TBT Contamination on Nucella Populations Functional Ecology 4 424-432 (1990)

Images

1) Limpets sat safely in their home scars. Credit: Antonella Guarracino

2) The underside of the common limpet, Patella vulgata - there's not much to see but a creeping, muscular foot. Credit: Wikimedia Commons user Tango22

3) A host of dogwhelks (Nucella lapillus) - most of the barnacles in the picture have lost their lives to the dogwhelks that feed on them. Credit: Martin Talbot via Wikimedia Commons.