Why Smurfs are like slipper limpets

Yes, I do mean Smurfs, those little blue Belgian cartoon characters... and slipper limpets are marine gastropods, Crepidula fornicata. So, why are they similar? Well, you probably know that, although there are lots of Smurfs (101 in fact), only one is female - Smurfette. Now, this could easily lead into pornographic territory (and undoubtedly has, somewhere on the Internet), but that's not what the Ecology Spot is about... instead I want to be a bit speculative and look at how this might affect Smurfs biologically if they were real...

One possibility would be that they became eusocial (like ants, bees and termites for example), with Smurfette as the only reproductive female (I assume Smurfs are viviparous, but maybe there are Smurf eggs - who knows?). However, Smurfette does not appear to be a large sedentary egg-layer (or large sedentary birther-of-live-young Smurflings), nor do there appear to be non-reproductive females rendered infertile by Smurfette pheromones. This is the case in, for example, the honey bee Apis mellifera, where the queen emits Queen Mandibular Pheromone (QMP), a pheromone set which, among other functions, inhibits ovary development in other females. So, the queen bee remains on the throne, and the princesses have to wait in line.With no other females present, and Smurfette running around actively, this seems unlikely. Instead, I think Smurfs might be an example of sequential hermaphroditism (SH).

One of the best-known examples of SH is C. fornicata. Though native to the eastern coast of North America, it has been widely introduced into the coastal waters of Europe, Japan and the NW Pacific, where it is invasive (having no predators away from its original range), competing with native filter-feeders for food. For more on its British history see here.

A stack of C. fornicata (plus a small chiton on the left) - photo by F. Lamiot, and used here under the Creative Commons Attribution-Share Alike 1.0 Generic license.

They can often be found in stacks and chains, their SH reproductive strategy meaning that the largest, oldest individuals, found at the base of  the stack are female, while the younger, smaller ones at the top are male, and some in between are 'transient'. If the female(s) die, the largest male becomes a new female.

Proestou (2005) showed that C. fornicata tended towards a 1:1 sex ratio, and that as a male's distance from a female increased, his reproductive success decreased i.e. that the males closest to the female have a competitive advantage. From this, it follows that if these males suffer a reduction in reproductive success (e.g. from competition with other males) that is greater than that due toswitching sex at a small size, then they should change. Only the lowest male in a stack can change sex, a process that takes around 60 days, during which the penis regresses and the pouches and glands of the female duct develop. If a juvenile settles on an existing stack, it develops as a male and may stay like this for up to 6 years due to pheromones released by females at the base of the stack (Fretter & Graham, 1981). Presumably the death of a female means this pheromone ceases to be produced and thus the male can change sex - another process must prevent others from changing, possibly pheromones from the new female-to-be? As there are 'transients' which complicate the picture, a pheromone gradient seems plausible.

So, although the sex ratio is different in Smurfs (100:1 rather than 1:1), an SH strategy fits well. If Smurfette dies, then as the oldest male, Papa Smurf should become Mama Smurf, with some of the others (who after all, could be 'transient' and we wouldn't know by looking at them) waiting in line.

Next post - normal service will resume!



References

Fretter, V. & Graham, A. (1981). The Prosobranch Molluscs of Britain and Denmark. Part 6. Journal of Molluscan Studies Supplement 9: 309-313.
Proestou, D.A. (2005). Sex change in Crepidula fornicata: Influence of environmental factors on reproductive success and the timing of sex change. Dissertation, University of Rhode Island.