Pigment migration in the compound eye of Manduca sexta: Effects of light, nitrogen and carbon dioxide

Abstract

Migration of screening pigment granules was studied in the secondary pigment cells of the compound eye of the tobacco hornworm moth Manduca sexta. The granules aggregate at the distal ends of these elongate cells during dark-adaptation, and disperse proximally during light-adaptation, to provide a longitudinal pupil regulating the entrance of light into the eye. Pigment position was measured directly during the couse of migration in sectioned quick-frozen eyes, and the pupillary response was measured in the intact eyes of living moths by reflectance microscopy. The influences of nitrogen and carbon dioxide anaesthesia on pigment migration were investigated in the light of earlier studies on other speicies showing that hypoxia results in dispersal. In accordance with these previous studies, rapid dispersal results from nitrogen hypoxia in Manduca, the pigment spreading farther than it does in light-adaptation. By contrast, the pigment disperses only slightly in response to carbon dioxide hypoxia. Carbon dioxide also inhibits the rapid, extensive dispersal caused by light and nitrogen. Thus the pseudopupil of the eye remains dilated in carbon dioxide anaesthetized moths even under bright illumination. Light-induced dispersal is restored with the addition of oxygen to the carbon dioxide atmosphere. These results suggest, contrary to the conclusions of earlier studies, that pigment dispersal in light-adaptation requires metabolic energy. The inhibition of pigment migration by carbon dioxide is unlikely to be the result of hypoxia; we suggest that low cellular pH affects the mechanism of pigment-granule motility.