Eyes as optical alarm systems in fan worms and ark clams

Abstract

Eye structure and optics were investigated in two sabellid polychaetes (Sabella melanostigma, Dasychone conspersa) and three arcacean bivalves (Arca zebra, Barbatia cancellaria, Anadara notabilis). The polychaetes have numerous compound eyes arranged in pairs along the branchial tentacles. Each ommatidium is composed of three cells: one receptor cell forming a ciliary receptive segment, and two pigment cells forming an extracellular lens (crystalline cone). The ark clamsAreaandBarbatiapossess large numbers of compound eyes arranged along the mantle edge. The ommatidia of these eyes are composed of one or two ciliary receptor cells surrounded by several layers of pigment cells. There are no lenses in the ommatidia of the clam eyes. All three species of ark clam also have many pigment-cup eyes on the mantle edge. The cup eyes lack lenses, and the cavity of the cup is filled with rhabdomeric microvilli from the receptor cells. The crystalline cones in the sabellid compound eyes are powerful lenses that reduce the field of view of the receptor cells to slightly more than 10°. The lensless ommatidia ofBarbatiahave much larger fields of view (« 30°). This difference correlates with a behavioural response to much finer moving stripes in the fan worms. A comparison of compound eyes and cup eyes inBarbatiareveals a poor resolution in both, but a much higher sensitivity is estimated for the cup eyes. The tentacular eyes of fan worms and the mantle eyes of ark clams trigger protective responses: retraction into the tube and shell closure, respectively. The responses are triggered by visual motion and the eyes work as burglar alarms rather than imaging eyes. For this purpose, the compound eyes may seem to occur in affluent numbers: 240 eyes with a total of 12 000 ommatidia inSabellaand 300 eyes with a total of 39 000 ommatidia inBarbatia. The number of ommatidia that simultaneously monitors any direction in space is, on average, 43 inSabellaand 755 inBarbatia. The large number of eyes is explained as a visual strategy which provides a robust alarm system designed to reliably detect predators without causing false alarms. The literature on tentacular eyes of fan worms and mantle eyes of bivalves is reviewed, and the evolutionary origin of these independently-acquired visual organs is discussed. I suggest the possibility that hyperpolarizing photoreceptor cells (shadow detectors) evolved from chemoreceptors that were inhibited by light.