Eye Glow Research Articles

Optical Modelling and Phylogenetic Analysis Provide Clues to the Likely Function of Corneal Nipple Arrays in Butterflies and Moths.

The lenses in compound eyes of butterflies and moths contain an array of nipple-shaped protuberances, or corneal nipples. Previous work has suggested that these nipples increase light transmittance and reduce the eye glare of moths that are inactive during the day. This work builds on but goes further than earlier analyses suggesting a functional role for these structures including, for the first time, an explanation of why moths are attracted to UV light. Using a phylogenetic approach and 3D optical modelling, we show empirically that these arrays have been independently lost from different groups of moths and butterflies and vary within families. We find differences in the shape of nipples between nocturnal and diurnal species, and that anti-glow reflectance levels are different at different wave-lengths, a result thereby contradicting the currently accepted theory of eye glow for predator avoidance. We find that there is reduced reflectance, and hence greater photon absorption, at UV light, which is probably a reason why moths are attracted to UV. We note that the effective refractive index at the end of the nipples is very close to the refractive index of water, allowing almost all the species with nipples to see without distortion when the eye is partially or completely wet and providing the potential to keep eyes dry. These observations provide a functional explanation for these arrays. Of special interest is the finding that their repeated and independent loss across lepidopteran phylogeny is inconsistent with the explanation that they are being lost in the ‘higher’, more active butterflies.

The eyes of Macrosoma sp. (Lepidoptera: Hedyloidea): A nocturnal butterfly with superposition optics

The visual system of nocturnal Hedyloidea butterflies was investigated for the first time, using light and electron microscopy. This study was undertaken to determine whether hedylids possess the classic superposition eye design characteristic of most moths, or apposition eyes of true butterflies (Papilionoidea), and, to gain insights into the sensory ecology of the Hedyloidea. We show that Macrosoma heliconiaria possesses a superposition-type visual mechanism, characterized by long cylindrical crystalline cones, a lack of corneal processes, 8 constricted retinular sense cells, rhabdoms separated from the crystalline cones forming a translucent ‘clear zone’, and tight networks of trachea that form a tapetum proximal to the retina and which also surround the rhabdoms to form a tracheal sheath. Dark-adapted individuals of M. heliconiaria, M. conifera, and M. rubidinarea exhibited distal retinular pigment migration, forming an eye glow. Correspondingly, light-exposure induced pigment to migrate proximally, causing the eye glow to be replaced by a dark pseudopupil. Other characteristics of the visual system, including relative eye size, facet size, and external morphology of the optic lobes, are mostly ‘moth like’ and correlate with an active, nocturnal lifestyle. The results are discussed in relation to the evolution of lepidopteran eyes, and the sensory ecology of this poorly understood butterfly superfamily.

Temperature-induced pupil movements in insect superposition eyes.

In this paper, we describe the hitherto largely overlooked effect of temperature on the pupil of insect compound eyes. In the turnip moth Agrotis segetum and in two other nocturnal insects with superposition eyes, the lacewing Euroleon nostras and the codling moth Cydia pomonella, the pupil not only opens and closes with changes in the ambient light level, as expected, but also with changes in temperature in the absence of light. In complete darkness, the pupil of A. segetum responds over a wide range of temperatures, with the pupillary pigments migrating to a light-adapted position when the animal is exposed to either low or high temperatures. At temperatures between 21.0 and 22.7 C, the pigments migrate to the fully dark-adapted position, resulting in an open pupil and maximal eye glow. Pupil closure at high temperatures shows two distinct thresholds: the first at 23.8+/-0.7 C and a second some degrees higher at 25.7+/-1.2 C (means +/- s.d., N=10). Temperatures exceeding the first threshold (the activation temperature, T(a)) initiate a closure of the pupil that is completed when the temperature exceeds the second threshold (the closure temperature, T(c)), which causes rapid and complete migration of pigment to the light-adapted position. All temperatures above T(a) affect the pupil, but only temperatures exceeding T(c) result in complete closure. Temperatures between T(a) and T(c) cause a slow, partial and rather unpredictable closure. The lacewing and the codling moth both show very similar responses to those of A. segetum, suggesting that this response to temperature is widespread in superposition eyes. The possibility that the ambient temperature could be used to pre-adapt the eye to different light intensities is discussed.

The visual ecology of pupillary action in superposition eyes

The two most common mechanisms of pupillary screening-pigment migration in arthropod superposition eyes are the cone and longitudinal pigment migration mechanisms. The dynamics of each were investigated by optical modelling and by determining experimentally the relationship between eye glow brightness and screening pigment position within the eyes of two representative insect species: the noctuid moth Agrotis infusa and the dung beetle Copris elphenor. During dark adaptation, in both mechanisms, the screening pigment is contracted distally to expose the proximal half of each crystalline cone. During light adaptation the pigment migrates proximally and reduces light flux in the retina. In the longitudinal mechanism, pigment migrates into the clear zone of the eye. In the cone mechanism, pigment never enters the clear zone and is instead restricted to the proximal half of each crystalline cone: a migrating sleeve of pigment creates a small aperture at the end of the crystalline cone, the area of which depends on the degree of light adaptation. According to the model, the cone mechanism provides a limited range of light attenuation (ca. 0.6 log units) for which both good spatial resolution and accuracy of control are maintained, and within this range attenuation is controlled very finely. Beyond this range, whilst attenuation is still possible, diffraction at the pigment aperture and increasing coarseness of control worsen visual performance significantly. In contrast, the longitudinal mechanism provides a much larger useful range of light attenuation (up to several log units) and maintains reasonable fineness of attenuation control over the entire range (although not as fine as the cone mechanism). The experimental results support the model. An extensive survey of arthropods with superposition eyes reveals that the cone mechanism is almost exclusively possessed by those animals experiencing a narrow range of light intensities, and the longitudinal mechanism by those experiencing a wide range.

Requirements for screening pigment migration in the eye of Ephestia kuehniella Z.

The influence of colchicine, cytochalasin B, calcium concentration, ouabain, 2,4-dinitrophenol, epinephrine, octopamine, and low temperature on the migration of pigment granules induced by light or darkness in the superposition eye of Ephestia kuehniella was investigated using the size of the eye glow to indicate the position of the granules. Colchicine, low extracellular calcium concentration, 2,4-dinitrophenol, and low temperature inhibit the aggregation of the granules in the secondary pigment cells from the dispersed state, and cause aggregated granules to disperse in darkness. Cytochalasin B inhibits aggregation from the dispersed state, but does not induce dispersal. Ouabain and high extracellular calcium concentration cause a light-induced inhibition of aggregation. The neurotransmitters, epinephrine and octopamine, have no effects on granule position. Dispersion is inhibited only by cytochalasin B. The requirements for aggregation and dispersion are discussed.

The phenomenon of eye glow

The coloured eye glow of animals, seen at night when their eyes are caught in a strong light, is a matter of common experience. It is caused by a reflecting layer known as the tapetum lucidum. A similar eye glow is seen in butterflies and apparently serves to enhance vision by increasing contrast and reducing glare.

The role of protocerebrum in the modulation of circadian rhythmicity in the crayfish visual system

Dark-adapted crayfishes with protocerebrum only, were submitted to continuous recordings of electroretinogram (ERG) and of eye glow area (EGA) during several days. Circadian variations of ERG amplitude similar to that of intact animals, were revealed by means of restrained test light stimuli (0.2 Cd/ft 2) bilaterally applied to each eyestalk. The period (24.6–38 hr) and range (40–80%) value of ERG oscillations always resulted quite similar to one another side. As in intact animals retinal shielding pigments (RSP) position as measured as EGA size showed a clear circadian rhythm, and also a clear consensual reflex in these preparations. We found a loss of both: circadian and consensual mobilization of distal RSP in animals with complete removal of cerebral ganglion. Our proposition is that the crayfish protocerebrum plays a major role in the modulation of circadian retinal sensitivity, probably through the control-release of hormonal neurosecretions from the sinus gland along the day.

Structural Differences in the Tracheal Tapetum of Diurnal Butterflies

Abstract The three-dimensional structure of the tracheal tapetum lucidum, its reflection properties and the resulting eye glow hue were studied in members of the diurnal butterfly families Pieridae, Nymphalidae, Satyridae and Lycaenidae. Two main groups of tapeta can be distinguished by structural and physiological differences. Whereas in pierids the main tracheal trunk at the bottom of the rhabdom bifurcates into two side branches before bifurcating again more distally, the tracheal trunk in the members of the family Nymphalidae, Satyridae and Lycaenidae investigated first divides into four side brandies. A second bifurcation shortly after the first results in eight subbranches which are regularly arranged between adjoining receptor cells. The broad banded reflection colour from incidently illuminated tapetal structures (at the level of the first bifurcation) varies between and within families but does not change significantly within the same eye. Whereas in nymphalids, satyrids and lycaenids the eye glow hue corresponds with the colour of the tapetal reflection, in pierids it is dominated by the coloured receptor screening pigment.

Bilateral Effects On Retinal Shielding Pigments During Monocular Photic Stimulation in the Crayfish, Procambarus

ABSTRACT Bilateral light adaptation of distal retinal shielding pigments was observed a few minutes after 60 min of sustained photic stimulation (2·69 Cd/m2) of a single eyestalk of the dark-adapted crayfish. Pigment migration was observed in intact animals as a diminution of eye glow area and electroretinogram amplitude, and was confirmed in sectioned material. The effect upon the contralateral eye was abolished by surgical bisection of the cerebral ganglion. It is suggested that the mechanism involved in the bilateral effect may be responsible for the mutual entrainment of ERG circadian rhythms of both eyes.

Coloured screening pigments cause red eye glow hue in pierid butterflies

The fine structure of the tracheal tapetum lucidum was investigated in six members of the diurnal lepidopteran family Pieridae. These observations were compared with the eye glow hue on intact eyes, the reflection colour of the incident illuminated tapetum and the distribution of the red screening pigments found in some receptor cells. The eye glow hue of dark adapted pierid eyes appears dark red. Whereas in the speciesColias crocea, C. australis andGonepteryx rhamni the red eye glow is observed all over the eye, appear the uppermost 35 horizontal eye rows in the speciesPieris brassicae, P. napi andP. rapae turquoise to yellow-green. The reflection colour of the tracheal tapetum of all examined pierid eyes is, however, uniformly turquoise to yellow-green all over the eye. In addition no regional structural differences in the tracheal tapetum at the proximal end of the rhabdom were observed. One knows, however, that inPieris brassicae, P. napi andP. rapae in the ventral and medial part of the eye, inColias crocea, C. australis andGonepteryx rhamni in all ommatidia the four proximally located receptor cells 5–8 contain red screening pigment which is arranged close to and even within the rhabdomeric structures (Ribi, 1978a). These observations show that the red eye glow observed in various pierid butterflies depends on coloured retinula cell screening pigment and not on the tracheal and rhabdomeric structures. Morphological and functional aspects of the Lepidopteran tapetum lucidum and the role of the coloured retinula cell pigmentation are discussed.

Effects of cerebroid ganglion lesions on ERG circadian rhythm of the crayfish

In the crayfish, the eye glow area and the voltage of the ERG evoked by brief light pulses applied at hourly intervals under continuous darkness shows high and low values occurring with a period of about 24 hr. Both a brain-less preparation and a complete destruction of the proto and deutocerebrum produced persistently high values with small circadian variations of the ERG. The circadian oscillations of the eye glow area were also diminished. Both the eye glow area and the ERG circadian rhythm remained unchanged either after: 1) the sagital section of the ganglion, 2) the section of the circum-oesophageal connections, or 3) the ablation of the opposite hemiganglion. In contrast, damage to the ipsilateral globuli cells, accessory and olfactory lobes (deutocerebrum) is followed by an increase in the length of nocturnal phase of the ERG voltage circadian rhythm. The decreased size and ultra-structural changes found in the simus glands of the eyestalk after lesion of the cerebroid ganglion, suggest a neurohumoral regulation of the retinal activity of the crayfish, probably exerted through changes in the position of the retinal shielding pigment.

Visual adaptation in butterflies

THE brilliant glow appearing in the compound eye of butterflies has intrigued investigators of insect eyes since the observations of Exner1. Miller and Bernard have presented a convincing optical interpretation of the butterfly glow, that the tracheole basal to the rhabdom is modified in such a way as to act as a quarter wavelength interference reflection filter (see refs 2–4). On light adaptation, the eye glow vanishes rapidly1. Miller and Bernard have conjectured that this is caused by a distal migration of pigment granules in the pigment cells surrounding the crystalline cone2.

Eye Glow in the Moth and Superposition Theory

EXNER'S theory of the formation of a retinal image by superposition1 in certain arthropod compound eyes requires that an object in front of a number of ommatidia is twice inverted by the dioptric system of each ommatidium. Thus erect images of the object are formed behind the crystalline cones. Converging proximally, those images grow in size and superimpose in the layer of the receptive structures, the rhabdoms. Exner tested his theory by observing the image formation in sectioned eyes and found agreement between experiment and theory in more than a dozen insect species. His findings were confirmed repeatedly using the firefly2–4. (Although Exner proposed the formation of superposition images in certain Crustacean eyes, he failed to obtain upright and superposition images. So did other observers2,3. Crustacea will therefore be excluded.)