No abstract

Rimicaris exoculata is a shrimp that swarms over high-temperature (350 degrees C) sulphide chimneys at Mid-Atlantic Ridge hydrothermal fields (3,600 m). This shrimp lacks an externally differentiated eye, having instead a pair of large organs within the cephalothorax immediately beneath the dorsal surface of the transparent carapace, connected by large nerve tracts to the supraesophageal ganglion. These organs contain a visual pigment with an absorption spectrum characteristic of rhodopsin. Ultrastructural evidence for degraded rhabdomeral material suggests the presence of photoreceptors. No image-forming optics are associated with the organs. We interpret these organs as being eyes adapted for detection of low-level illumination and suggest that they evolved in response to a source of radiation associated with the environment of hydrothermal vents.

At night efferent optic nerve activity generated by a circadian clock in the Limulus brain changes the structure of the photoreceptor and surrounding pigment cells in the animal's lateral eyes. The structural changes allow each ommatidium to gather light from a wider area at night than during the day. Visual sensitivity is thereby increased, but spatial resolution is diminished. At daybreak efferent activity from the clock stops, the structural changes reverse, and the field of view of each ommatidium decreases. The cyclic changes are endogenous and continue in the dark. Thus, under the control of a circadian clock, the Limulus eye exchanges its daytime acuity for greater sensitivity at night.

Photoreceptors of the Limulus lateral eye shed their light-sensitive membranes (rhabdoms) in a burst early each morning when the animal is maintained in natural lighting. This shedding burst produces a cloud of multivesicular bodies which coalesce and migrate away from the rhabdom. Within 24 hr, these gradually collapse to combination bodies and ultimately to lamellar bodies. Light initiates the burst of shedding. If animals are maintained in darkness beyond their normal dawn, the shedding burst is delayed until the first onset of light. We have not been able to produce a second burst of membrane shedding within one 24-hr period. Efferent optic nerve activity generated by a circadian clock in the brain primes the shedding burst. At least 3 hr of efferent activity in darkness must precede light onset to prime membrane shedding; however, the efferent fibers need not be active when the light-initiated burst occurs. Chronically blocking the efferent input to the retina abolishes the shedding burst. The burst of membrane shedding is robust and short-lived. Within 15 min of light onset the area of photosensitive membrane decreases by about 70%, and within an hour the rhabdom returns to essentially its preburst size. At other times in the diurnal light cycle, the size of the rhabdom undergoes significant variations which are not abolished by blocking the efferent input. Apparently the daily burst of shedding overlays a second cycle of membrane metabolism that is not controlled by efferent optic nerve activity.

Photosensitive membrane structures in the retinular cells of the Limulus lateral eye are broken down and renewed daily. The first light onset causes a rapid, synchronous disassembly and buildup of the rhabdom in each photoreceptor cell. The entire process is complete within 30 minutes. Blocking the efferent input to the retina from the brain blocks the turnover of the rhabdom, and mimicking the efferent input by optic nerve stimulation restores it.