The Rhabdomere organization of some nocturnal pisaurid spiders in light and darkness

Abstract

The retinae of the posterior eyes of pisaurid spiders in the genus Dolomedes are described.They resemble those of Lycosidae, but the receptors are much larger, and proximal to the strips of tapetum upon which they rest the receptor axons are grossly dilated. Each receptive segment contains two rhabdomeres, and pairs of rhabdomeres belonging to adjacent receptors are contiguous. Prolonged (6 h) illumination at physiological levels causes the rhabdomeres to diminish in volume by loss of membrane which is restored on return to darkness. W hen spiders are kept in darkness for 4-5 d, the rhabdomeres grow by the orderly addition of membrane to the microvilli until they completely fill the receptive segments, and such novel membrane is subsequently disassembled when the retina is illuminated. It is proposed that under normal conditions there is a balance maintained between the growth and destruction of rhabdomere membrane. The paired rhabdomeres are flanked by the processes of supportive cells which exhibit much membrane amplification, and the supportive cell system extends below the tapetum completely to ensheath the swollen receptor axons, which are some 70-80 pm long. In dark-adapted retinae the supportive processes are shrunken; illumination causes them to swell, and the extracellular space between the interdigitations fills with electron-dense material derived from the breakdown of rhabdom ere membrane. The material is passed basally and reintroduced into the receptor axons via an extensive system of endocytotic pleats. The tips of pleats often enclose pigment granules from the supporting system, and identical granules in various states of lysis are found within the axoplasm after exposure to light, thus implying that the pleats burst rather than merely transport material across their membranes. There is evidence that pleats may become detached. Exposure of retinae to infrared radiation also evokes breakdown of rhabdomere membrane, but the extracellular route is not employed. The swollen axons are filled with whorls of rough endoplasmic reticulum, abundant Golgi bodies, and mitochondria. After long periods of darkness, all these systems are depleted, and the space they occupied becomes highly vacuolated. Light adaptation from dim light on a normal diurnal cycle evokes dilation of the cisternae of the endoplasmic reticulum, which pinch off smooth vesicles, and the Golgi bodies become highly active and produce coated vesicles in abundance. The relations between smooth vesicles and microvilli are ambiguous; precedents exist for supposing that smooth vesicles in the inter-rhabdom eral cytoplasm are pinocytotic and have been pinched off from the bases of the microvilli, but in Dolomedes there is some evidence to suggest that they may be identical with those manufactured by the endoplasmic reticulum and are also fusing with rhabdomere membrane. Multivesicular and multilamellar bodies are the product of membrane fragments which have broken off from the rhabdomeres during light adaptation, and of coated vesicles produced by pinocytosis; they are transported within the receptors to the swollen axons where they undergo lysis. It is proposed that in Dolomedes the role of the endoplasmic reticulum is to synthesize materials for the repair of rhabdomere membrane, and that the bulk of precursors to sustain this process is obtained by recycling the products of rhabdom ere breakdown via the supportive cell system. The hypothesis is discussed in terms of current information about invertebrate retinae, and analogous processes which are well established for those of vertebrates. Dolomedes do not move retinal pigment granules to modulate the shielding of their receptors, and it is likely that manipulation of the properties of photoreceptor membrane is the only strategy of adaptation available to them.