What do scallops do with all those eyes?

Scallops have hundreds of remarkable blue eyes (blue dots around the edge of the shell in the image).

 Their eyes are quite sophisticated, combining a lens and mirror to focus an image on a retina (which sits between the lens and retina) [1]. They appear to be able to focus a sharp enough image to have about a 2° angular resolution [2,3]. For comparison, that's about the size of one's thumb (while, my thumb) held at arm's length. Not great, but quite respectable for a bivalve. 

Clams are not particularly brainy, so what do they do with all these eyes? They can clearly see one coming when they're sitting in a tank. They clam up quickly. But lots of animals have shadow responses without sophisticated eyes. 

Speiser and Johnsen [3] tested clever idea: perhaps these filter feeders use their eyes to judge whether conditions are right for filter feeding. Scallops, like most clams, make a living by filtering nutritious particles out of the water. Perhaps they use their eyes to see when there are enough particles flowing fast enough to be worth expending the energy to pump water through their gills. To test this they played videos of particles flowing to the scallops and watched whether they opened up. 

It turned out that whether they opened depended on whether there were particles, how many, and how fast they were moving in the way they predicted based on the speed and resolution of the eyes. So it looks like this sophisticated visual system might be used to detect flowing particles. Perhaps even more interestingly, what we'd normally see as limitations on the eyes – their slow response and low resolution – might make it unnecessary to have sophisticated neural processing.

I remain curious about other possible functions [4]. Why would they need so many eyes for a particle or a shadow sensor? Could they use their eyes to detect distance as well like we use our binocular vision? Some simple calculations suggest an ~3 cm diameter scallop (such as the one shown) might be able to judge distances out to ~20 cm.

1. Land, M.F., Image formation by a concave reflector in the eye of the scallop, Pecten maximus. The Journal of Physiology, 1965. 179(1): p. 138-153.
2. Speiser, D.I. and S. Johnsen, Comparative morphology of the concave mirror eyes of scallops (Pectinoidea)*. American Malacological Bulletin, 2008. 26(1-2): p. 27-33 DOI: http://dx.doi.org/10.4003/006.026.0204.
3. Speiser, D.I. and S. Johnsen, Scallops visually respond to the size and speed of virtual particles. The Journal of experimental biology, 2008. 211(Pt 13): p. 2066-70 DOI: http://dx.doi.org/10.1242/jeb.017038.
4. Hamilton, P.V. and K.M. Koch, Orientation toward natural and artificial grassbeds by swimming bay scallops, Argopecten irradians (Lamarck, 1819). Journal of Experimental Marine Biology and Ecology, 1996. 199(1): p. 79-88 DOI: http://dx.doi.org/10.1016/0022-0981(95)00191-3.

Sensation and coordination based on cilia

How do organisms coordinate sensation and behavior? Ctenophores have linked the usual neuron-based system of other animals to an elegant coordination system based on mechanical interactions among cilia.

Ctenophores seem to me to have reached nirvana. The common ones that we see on the coast glide gracefully through the water, their transparent bodies sparkling with bright iridescence when their eight bands of beating "combs" catch the light.

The combs (or ctenes) are plates of thousands of very long cilia, which make a paddle that can get up to a millimeter or two wide and long. The rows of combs beat in a wave along the length of the body. Like all animals, ctenophores have muscles that control their body shape, and neurons which control the muscles and can signal the cilia to stop and reverse.

However a fascinating series of experiments by Dr. S. Tamm [1-3] suggests the wave of the comb rows' beat is coordinated by the mechanical drag of one cilium moving as it beats triggering the adjacent ones to beat. Mechanical interactions coordinate movements both within [2-3] and among the plates [1-2]. In the species shown - Mnemiopsis leidyi - in this picture, the wave is transmitted from one plate to the next along a row of smaller ciliated cells that runs between the big plates. Originally it was thought this transmission was electrical [1], but subsequent experiments indicate it is also based on mechanical interactions among cilia [2].

Their sensation and response to gravity is coordinated in a similar way [2,4]. At the back end of the animal, there is an gravity-sensing organ, the apical organ. It is formed by a dome of non-motile cilia enclosing small calcareous stones secreted by the animal. These stones are held by four groups of beating cilia. The force with which they press on the cilia depends on gravity, and pulling or pushing on the cilium changes the frequency that the cilia beat. This change of beat frequency appears to be transmitted mechanically along rows of ciliated cells to the comb rows.

So, their ability to orient to gravity seems to be built (almost) entirely out of the effects of mechanical force on ciliary beat. It turns out that the sign of the response to force can be changed electrically, which allows them to switch between orienting up or down with respect to gravity. This switch is probably under nervous system control, as are other responses that stop, reverse, or accelerate ciliary beat [2]. But still, a remarkably large amount of their sensation and coordination seems to be controlled by mechanical interactions among cilia more than by electrical and chemical interactions among neurons.

One intriguing question (at least to me) is how this mechanical coordination might work in turbulence. Is the turbulence in their environment strong enough to trigger or suppress the cilia wave? Could this enhance or limit their ability to navigate in their natural habitat? Another interesting question is, how important are non-neural mechanisms of coordination and sensory integration in other animals? (Ciliary beat is known to be mechanically modulated in other organisms.) And how has this unusual system affected the evolution of ctenophore body forms?

1. Tamm, S.L., Mechanisms of ciliary co-ordination in ctenophores. Journal of Experimental Biology, 1973. 59(1): p. 231-245.
2. Tamm, S.L., Ctenophora, in Electrical conduction and behaviour in 'simple' invertebrates, G.a.B. Shelton, Editor 1982, Oxford University Press: Oxford. p. 266-358.
3. Tamm, S.L., Mechanical synchronization of ciliary beating within comb plates of ctenophores. Journal of Experimental Biology, 1984. 113(1): p. 401-408.
4. Lowe, B., The role of ca2+ in deflection-induced excitation of motile, mechanoresponsive balancer cilia in the ctenophore statocyst. Journal of Experimental Biology, 1997. 200(11): p. 1593-606.