Effects of light and darkness on the visual pigments of amphibian tadpoles

Abstract

The effects of light and darkness on the visual pigment composition in the eyes of tadpoles of Rana clamitans, Rana catesbeiana, Ambystoma maculatum and Xenopus laevis have been investigated. Ranid tadpoles have mainly porphyropsin in the light, but in darkness the proportion of rhodopsin gradually increases over a period of several weeks. The process is reversible over several light-dark cycles. The light effect is extremely rapid: exposure to illumination of 85–150 ft-c. can return the system to nearly pure porphyropsin after 24–48 hr. The reaction appears to be the same at all developmental stages examined, i.e. from Taylor-Kollros stage IV–XV (early prometamorphosis). Illumination retards but does not prevent the switch to rhodopsin at natural or thyroxine-induced metamorphic climax (i.e. forelimb emergence). The dark increase of rhodopsin is not prevented by 0.04% thiourea. If tadpoles which have been permitted to increase their rhodopsin in the dark are illuminated after one eye in each specimen has been covered with black vaseline, the exposed eyes synthesize more porphyropsin. The difference is not observed if normal, clear vaseline is used instead, and it is therefore concluded that the light-stimulated formation of porphyropsin is a local response of the ocular tissues and is not mediated by hormones (such as thyroxine) or extraocular receptors (such as the stirnorgan). The quantities of visual pigment molecules appear to be the same in tadpoles kept in light and darkness, irrespective of the composition of the mixture. Like their adult forms, bullfrog tadpoles at or approaching metamorphic climax always had more porphyropsin in the dorsal retina. The premetamorphic tadpoles kept in the light did not show any significant differences between dorsal and ventral retinal areas, but those kept in darkness sometimes did. No porphyropsin was detectable in any part of the retinas of adult R. clamitans, R. pipiens, R. palustris, R. sylvatica, Hyla crucifer and H. versicolor. No dorsoventral gradient of visual pigment composition was found in R. clamitans tadpoles or Xenopus laevis adults. Unlike Rana, Ambystoma tadpoles have pure rhodopsin like the adults. Xenopus tadpoles (stages 58–59) have virtually pure porphyropsin, like the adults. Neither species changes its visual pigments when kept for several weeks in light or darkness. It is suggested that the increase of rhodopsin in the dark occurs because rhodopsin is the major pigment that is incorporated into the outer segment during the renewal process. On the other hand, the rise of porphyropsin in the light is partly a consequence of the interchange of retinol and 3-dehydroretinol between retinal visual pigment and stores in the pigment epithelium, which are composed predominantly of 3-dehydroretinol even in tadpoles kept in the dark. However, ultimately there is total disappearance of retinol and rhodopsin from the eyes of tadpoles kept in continuous light, so it is believed that a further light-driven reaction must be implicated.