Spatial Resolution Determined by Electrophysiological Measurement of Acceptance Angle in two Species of Benthic Decapod Crustacean

Angular sensitivity functions were determined electrophysiologically for retinula cells in Nephrops norvegicus and Munida rugosa. For such aquatic species it is shown that reliable measurements cannot be obtained unless the eyes are submerged. In both cases, for submerged eyes, there is a significant reduction in retinula cell acceptance angles with light adaptation. In N. norvegicus the change is from 11·3° dark adapted (DA) to 8·85° light adapted (LA). In M. rugosa there is a larger difference, 12·5° (DA)–6·58° (LA). The changes in acceptance angle with adaptational state can be attributed to differences in screening pigment position between light- and dark-adapted eyes. In N. norvegicus only the retinula cell proximal pigment is migratory. The small change in acceptance angle with adaptation is consistent with the fact that the eye uses superposition optics even when light-adapted.

Depth related variation in the structure and functioning of the compound eye of the Norway lobster Nephrops norvegicus

The mobility and quantity of retinula cell proximal screening pigment, and the liability of the eyes to light-induced damage, were investigated in the Norway lobster, Nephrops norvegicus (L.), obtained from three separate populations from depths of 18, 75, and 135 m.During the morning after capture, the migration of the proximal pigment in response to the onset of illumination below the threshold for damage varied between the three populations. In the eyes of deep water N. norvegicus, the proximal screening pigment was located close to or below the basement membrane when dark-adapted and rose to a position midway up the rhabdoms when light-adapted. In the dark-adapted N. norvegicus from shallow water the proximal pigment was located more distally than in eyes of deep water animals. After the onset of illumination, the pigment migrated distally to completely cover the rhabdoms. The amount of retinula cell proximal screening pigment was found to decrease linearly with depth.When dark-adapted individuals from each depth were exposed to light a positive correlation was obtained between the photon fluence rate (PER) and the proportion of the retina damaged. For a given light exposure the amount of damage was highest in animals from deeper water. The PFR causing 25% damage was approximately 1 log unit higher in animals from 18 m compared to those from 135 m.The amount of damage varied with the delay between capture of the animals and exposure to light. When exposed 2 h after capture significant differences between depths were seen but the results were influenced by the incomplete dark adaptation of some specimens.

Eye structure and optics in the pelagic shrimp Acetes sibogae (Decapoda, Natantia, Sergestidae) in relation to light-dark adaptation and natural history

The structure and optics of the compound eyes of the neritic sergestid shrimp, Acetes sibogae , are described. The eyes are nearly spherical and heavily pigmented. The facets are square, indicating that the eye operates by the recently recognized mechanism of reflecting superposition. The most distal portion of each ommatidium is the corneal lens, which is secreted by two underlying corneagenous cells. These two cells surround the crystalline cone and cone stalk and the four cells of which they are composed and extend proximally at least as far as the distal rhabdom. Near the base of the cone stalk the extensions of the corneagenous cells swell and enclose spheres which bear on their surfaces small particles similar to ribosomes in appearance. Beneath the corneagenous cells lie four crystalline cone cells, parts of which differentiate to form the crystalline cone and cone stalk. The latter structures are compound, one quarter of each being contributed by each crystalline cone cell. Distally the crystalline cone cells send a small projection, which is surrounded by the corneagenous cells, to the cornea. Proximal extensions of each of the four parts of the cone stalk extend between the retinula cells and meet within the basement membrane. Between the base of the cone stalk and the regularly layered rhabdom lies the distal rhabdom. It is surrounded by a cell that we have termed retinula cell eight (R8), by analogy with other crustacean systems, and consists of unordered microvilli projecting from the cell membrane into the extracellular space above the layered rhabdom. In addition to R 8, which contributes only to the distal rhabdom, seven other retinula cells contribute to the proximal rhabdom, which consists of alternating ordered layers of orthogonally arranged microvilli. Four of these retinula cells are arranged orthogonally and extend far distally along the crystalline tract. The other three do not extend as far distally and alternate with the first four in their position around the axis of the ommatidium. R8 is located still further proximally at the level of the distal rhabdom. All seven of the retinula cells which contribute to the proximal rhabdom contain proximal pigment and extend through the basement membrane. The basement membrane consists of a meshwork grid with each intersection supporting a rhabdom so at this point the retinula cell axons project into different squares of the meshwork. Tapetal pigment cells are present in the vicinity of the basement membrane and extend downward to the lamina. The granules of tapetal pigment are covered or exposed by movements of the proximal pigment and also change their intracellular distribution depending on illumination. In addition to the proximal (retinula cell) pigment and the tapetal pigment the eye contains four types of distal pigment. Moving inward from the cornea these are the distal yellow pigment (DYP) which surrounds the entire eye; the distal reflecting pigment (DRP), which forms a thin layer and is continuous with the tapetal pigment at the edge of the eye; and the black distal pigment and the mirror pigment (MP) both contained within distal pigment cells (DPC). In the light-adapted state the proximal pigment moves distally, surrounding the rhabdoms, and the tapetal pigment granules move proximally so that they are mainly found beneath the basement membrane. Movements of the distal pigments are less clearcut, but they all appear to move somewhat proximally in the light-adapted state. Multivesicular bodies are more abundant in the retinula cells shortly after dawn, and are possibly related to membrane turnover. Interommatidial angle, as measured on both fixed and fresh material, varied from 2.8 to 3.8° in different parts of the eye. The crystalline cones were found to have a uniform refractive index radially, which, combined with their square shape, indicates that they function by reflecting superposition. Total internal reflection from the sides of the cones is adequate to explain the maximum diameter of the eyeshine from the dark-adapted eye at night without the need for additional mirrors. Nevertheless, from its organization and appearance the mirror pigment could act as a reflector in the dark-adapted eye. Also, the size of the glow patch indicates that there would be a gain of nearly two log units in image brightness in going from the light-adapted to the dark-adapted state. Each corneal facet was found to act as a weak converging lens, with a focal length of approximately 300 μm. The eye structure of Acetes is discussed in relation to that of other shrimp and to the natural history of Acetes .

Light and retinal damage in Nephrops norvegicus (L.) (Crustacea)

Nephrops norvegicus is a burrow-dwelling marine crustacean normally only active in dim light. The eye has typical crustacean rhabdoms each consisting of alternating layers of microvilli. On light adaptation, proximal shielding pigment moves up from the bases of retinula cells to surround the rhabdoms. In dark-adapted eyes the proximal pigment moves proximally to form a band just above the basement membrane. In this position the tapetum is unshielded and it reflects light back into the eye. The only other detectable difference between light- and dark-adapted eyes is a night-time increase in rhabdom volume. Creel-caught animals raised to the surface of Loch Torridon (NW Scotland) were exposed to ambient surface light for periods ranging from 9 min to 5 h. A short exposure (9 min, average intensity 380 μmol m –2 s –1 ) is sufficient to cause damage to the retinula cell layer. It is histologically detectable one month later. Animals fixed immediately after 15 min exposure show evidence of retinula cell breakdown with swelling of cell bodies and nuclei, escape of proximal shielding pigment from the retinula cells and vesiculation of the rhabdoms. After 2 h of illumination the microvilli of the rhabdom are completely disrupted with only membrane whorls remaining; proximal shielding pigment is found deep within the rhabdom. After 6 h of illumination the retinula cell body layer is absent and there is a massive invasion of the eye by haemocytes. By using animals acclimated to a 12 h light–12 h dark cycle (green light, 0.24 μmol m –2 s –1 ) we were able to test the effects of natural day­light (average intensity 180 μmol m –2 s –1 ) on dark- and light-adapted eyes of known physiological state. The animals were kept alive for two weeks after exposure and the percentage area of the retina destroyed was measured from serial wax sections. Dark-adapted eyes have substantial damage (76.74%) after only 15 s but light adaptation prevents damage with a similar exposure. After 5 min exposure, destruction is almost total (light-adapted, 97.16%; dark-adapted, 98.97%). Intensities of 1000 and 250 μmol m -2 s –1 with an artificial tungsten light source gave similar results. Light-adapted eyes are less sensitive than dark-adapted ones and longer exposures cause greater damage. At these relatively high intensities the damage caused by the two light levels is not very different. At lower intensities (10–250 μmol m –2 s –1 ) the amount of damage is proportional to the intensity. By using the tungsten source and 10 s expo­sures we found that dark-adapted eyes are damaged at 25 μmol m –2 s –1 and that light-adapted eyes are affected at 100 μmol m –2 s –1 .

Nonconventional Interactions between Photoreceptor Axons in the Butterfly Lamina Ganglionaris

Butterflies have nine photoreceptors within each ommatidium which have been named from their positional orientation across the rhabdom. Within all ommatidia ex­amined, there are four morphologically discrete receptor types: 1. Two dorsal-ventrally aligned cells - the vertical receptors; 2. two anterior-posteriorly aligned cells - the horizontal receptors; 3. four diagonally aligned cells -the diagonal receptors; 4. one basally occuring bilobed cell - the basal receptor. The nine retinula cell axons pass through the basement membrane and enter an optic car­tridge of the lamina ganglionaris as a single bundle. The organization of these axons within their cartridge has been investigated in the nymphalid-type butterfly Agraulis vanillae. Prior to entry into the optic cartridge, the axonal bun­dle undergoes a 90° positional rotation. Retinula axons become grouped into three regions: a dorsal triad and a vent­ral triad of three axons, one horizontal and two diagonal retinula cells each; a central group composed of two verti­cal retinula cells, the basal cell, and 4 -5 lamina monopolar cells. Retinula axons of the triads appear to be coupled by bulbous cytoplasm ic projections. Two types of coupling ap­pear to occur: 1. Within each triad, the horizontal retinula cell axon is coupled to both diagonal axons. 2. The horizon­tal retinula cell axon of one triad is coupled to the horizon­tal cell of the adjacent triad. Because of the 90° reposition­ing of the ommatidial axon bundle, specific cell types from one ommatidium appear to be linked to retinula cells of ommatidia immediately above or below them. These non­conventional receptor cell interactions are described and a possible function in receptor coupling suggested.

The eye of Orchomene sp. cf. O. rossi , an amphipod living under the Ross Ice Shelf (Antarctica)

The structural organization of the eye of freshly caught Orchomene sp. cf. O. rossi is described and compared with that of individuals that were exposed to sunlight for 2 h, or were kept in complete darkness for 2 and 7 days. Orchomene sp. cf. O. rossi occurs under the 400 m thick Ross Ice Shelf in water of — 2 °C. Its eyes, containing 360 ommatidia, are relatively large and of orange colour. External facets are not developed, but the dioptric structures, consisting of a cornea 30 μm thick and the bipartite crystalline cones (ca. 65 μm long and 55 μm wide), are transparent and allow one to see the underlying ommatidial organization and retinula. Rhabdoms, comprising rhabdomeres of five retinula cells per omma, are voluminous (up to 50 μm in diameter and 160 μm in length) and surround the proximal ends of the crystalline cones. There are a few black screening pigment granules in the retinula cell plasma, but their number is too small to effectively shield and insulate neighbouring ommatidia from each other. Interstitial cells, containing vesicles of 0.3 μm diameter, occupy the spaces between adjacent ommatidial groups of retinula cells, but do not extend into the layer of retinula cell nuclei. Based on the anatomy, the eye of Orchomene sp. cf. O. rossi seems to be adapted to maximize photon capture at the expense of acuity.