Relationships between pupil working range and habitat luminance in flies and butterflies

The luminance range over which the pupil mechanism operates was measured with pupil reflectometry in 11 species of butterflies and 13 species of dipteran flies. The different species were selected to be as different as possible regarding the range of ambient luminances in which they are active. Habitat luminance ranges were also measured and correlated to luminances in the experimental situation. The pupil mechanism in butterflies operates in the centre of the luminance range in which the different species are active. Three distinct groups of butterflies with pupil sensitivities matched to their specific types of activity pattern were identified: species active only in direct sunlight, species active also in shaded places and species extending their activity into dawn and dusk. Quite differently, the pupil mechanisms of dipteran flies operate in the upper end of the ambient luminances, and in some species well above the luminances normally encountered by the animal. All fly pupils start to close roughly at the same luminance, irrespective of the luminances in which the species are active. The results suggest that the most important role for the pupil mechanism in many of the butterfly species is to maximize acuity over a wide range of luminances, whereas in flies it is to avoid saturation of transduction units and thereby maximize the photoreceptor's signal-to-noise ratio at high light intensities. Accepted: 1 July 1997     

Evolution of color vision in pierid butterflies: blue opsin duplication,ommatidial heterogeneity and eye regionalization in <Emphasis Type="Italic">Colias erate</Emphasis>

This paper documents the molecular organization of the eye of the Eastern Pale Clouded Yellow butterfly, Colias erate (Pieridae). We cloned four cDNAs encoding visual pigment opsins, corresponding to one ultraviolet, two blue and one long wavelength-absorbing visual pigments. Duplication of the blue visual pigment class occurs also in another pierid species, Pieris rapae, suggesting that blue duplication is a general feature in the family Pieridae. We localized the opsin mRNAs in the Colias retina by in situ hybridization. Among the nine photoreceptor cells in an ommatidium, R1-9, we found that R3-8 expressed the long wavelength class mRNA in all ommatidia. R1 and R2 expressed mRNAs of the short wavelength opsins in three fixed combinations, corresponding to three types of ommatidia. While the duplicated blue opsins in Pieris are separately expressed in two subsets of R1-2 photoreceptors, one blue sensitive and another violet sensitive, those of Colias appear to be always coexpressed.     

Localization of the pupil trigger in insect superposition eyes

Summary In the superposition eyes of the sphingid moth Deilephila and the neuropteran Ascalaphus, adjustment to different intensities is subserved by longitudinal migrations of screening pigment in specialized pigment cells. Using ophthalmoscopic techniques we have localized the light-sensitive trigger that controls pigment position.In both species, local illumination of a small spot anywhere within the eye glow of a dark-adapted eye evokes local light adaptation in the ommatidia whose facets receive the light. Details of the response pattern demonstrate that a distal light-sensitive trigger is located axially in the ommatidium, just beneath the crystalline cone, and extends with less sensitivity deep into the clear zone. The distal trigger in Deilephila was shown to be predominantly UV sensitive, and a UV-absorbing structure, presumably the distal trigger, was observed near the proximal tip of the crystalline cone.In Ascalaphus we also found another trigger located more proximally, which causes local pigment reaction in the ommatidia whose rhabdoms are illuminated (the centre of the eye glow). The light-sensitive trigger for this response appears to be the rhabdom itself.     

Did neural pooling for night vision lead to the evolution of neural superposition eyes?

Observations of the infrared deep pseudopupil, optical determinations of the corneal nodal point, and histological methods were used to relate the visual fields of individual rhabdomeres to the array of ommatidial optical axes in four insects with open rhabdoms: the tenebrionid beetle Zophobas morio, the earwig Forficula auricularia, the crane fly Tipula pruinosa, and the backswimmer Notonecta glauca.The open rhabdoms of all four species have a central pair of rhabdomeres surrounded by six peripheral rhabdomeres. At night, a distal pigment aperture is fully open and the rhabdom receives light over an angle approximately six times the interommatidial angle. Different rhabdomeres within the same ommatidium do not share the same visual axis, and the visual fields of the peripheral rhabdomeres overlap the optical axes of several near-by ommatidia. During the day, the pigment aperture is considerably smaller, and all rhabdomeres share the same visual field of about two interommatidial angles, or less, depending on the degree of light adaptation. The pigment aperture serves two functions: (1) it allows the circadian rhythm to switch between the night and day sampling patterns, and (2) it works as a light driven pupil during the day.Theoretical considerations suggest that, in the night eye, the peripheral retinula cells are involved in neural pooling in the lamina, with asymmetric pooling fields matching the visual fields of the rhabdomeres. Such a system provides high sensitivity for nocturnal vision, and the open rhabdom has the potential of feeding information into parallel spatial channels with different tradeoffs between resolution and sensitivity. Modification of this operational principle to suit a strictly diurnal life, makes the contractile pigment aperture superfluous, and decreasing angular sensitivities together with decreasing pooling fields lead to a neural superposition eye.Abbreviations DPP deep pseudopupil - LMC large monopolar cell     

Comparison between temperature-induced changes and effects caused by dark/light adaptation in the eyes of two species of Antarctic crustaceans

Summary The amphipod, Orchomene plebs, and the isopod, Glyptonotus antarcticus, both adapted to live in seawater of a temperature of-2° to 0° C, were kept for 7h at the unphysiologically high temperature of +10° C. Temperature elevation appeared to mimic light adaptation with regard to the position of the screening pigment granules within the visual cells, but not with respect to ultrastructural changes in the microvillar array of the rhabdom, i.e. the visual membranes. Cellular metabolism, membranous fatty acid composition, and ion fluxes, all known to be readily affected by an increase in temperature, are thought to be responsible for the observed effects. Pigment granules could possibly cause an elevation of intracellular temperatures due to the fact that they are dark and dissipate absorbed energy as heat.     

Spectral organization of the eye of a butterfly,Papilio

Journal of Comparative Physiology A - This review outlines our recent studies on the spectral organization of butterfly compound eyes, with emphasis on the Japanese yellow swallowtail butterfly,...     

Mechanisms controlling the sensitivity of the Limulus lateral eye in natural lighting

Electroretinograms were recorded from the horseshoe crab compound eye using a high-intensity light-emitting diode and a whole-eye seawater electrode. Recordings were made from both lateral eyes in natural daylight or in continuous darkness with the optic nerve intact or cut. Recordings from two eyes of the same animal in different conditions facilitated direct comparisons of the effects of diurnal lighting and circadian efferent activity on the daily patterns of sensitivity of the eye. Structural changes appear to account for about half of the total electroretinogram excursion. Circadian input begins about 45 min in advance of sunset and the nighttime sensitivity returns to the daytime values 20 min after sunrise. When the optic nerve is cut, the nighttime sensitivity shows exponential decay over the next 5 or 6 days, consistent with a light-triggered structural light adaptation process unopposed by efferent input. Our results suggest that two mechanisms mediate the increase in lateral eye sensitivity at night—physiological dark adaptation and circadian efferent input. Three mechanisms appear to be involved in mediating the decrease in lateral eye sensitivity during daylight—physiological light adaptation, a continuous structural light adaptation process, and a separate light-triggered, efferent-primed structural light adaptation process.     

夜行性昆虫微光视觉行为及其视觉适应机制

作为昆虫种群的重要组成部分,夜行性昆虫成功进化出了与其生存环境相适应的感觉机制,普遍认为夜行性昆虫主要依靠嗅觉和机械性感受等来探索环境,其视觉器官发生了退化或功能丧失.近年来,随着红外夜视、视网膜电位(electroretinogram,ERG)和视觉神经等生物新技术的应用,昆虫视觉生态学研究出现了突破性进展,自200...     

Visual and lenticular pigments in the eyes of demersal deep-sea fishes

We report on the lens pigmentation and visual pigments of 52 species of demersal deep-sea fishes caught at depths ranging from 480 m to 4110 m in the Porcupine Seabight and Goban Spur area of the North-eastern Atlantic. Only one species, caught between 480 and 840 m, had a lens with large amounts of pigment, consistent with the hypothesis that heavily pigmented lenses in deep-sea fish serve to enhance the contrast of bioluminescent signals by removing much of the background radiance, which is only visible to fish living shallower than 1000 m. Low concentrations of lens pigmentation were also observed in a further two species (Rouleina attrita and Micromesisteus poutassou). The retinae of all species except five, contained only a single visual pigment, as determined by microspectrophotometry of individual rods, and/or spectrophotometry of retinal wholemounts and retinal extracts. Those fishes caught between 500 m and 1100 m had wavelengths of peak sensitivity (_max) ranging from 476 nm to 494 nm, while most fish living below 1100 m tended to be more conservative with (_max) values ranging from 475 nm to 485 nm. The only exceptions to this were three deep-living species caught between 1600 m and 2000 m whose retinae contain abnormally short-wave sensitive visual pigments (Cataetyx laticeps — _max 468 nm; Alepocephalus bairdii — _max 467 nm; Narcetes stomias _max 472 nm), suggesting adaptation for the detection of short-wave bioluminescence.     

Comparative analysis of the size and shape of the lizard eye

Lizards occupy both scotopic (light-limited) and photopic (light-rich) environments, thereby making this clade ideal for analyses of eye morphology adaptations. This study examines how in lizards the morphology of the eye varies according to activity in these different light environments. Measurements were collected on corneal diameters and axial lengths of the eye for 239 specimens of 116 lizard species (including Sphenodon) that include both species with scotopic and photopic visual adaptations. I show that the light level available to a lizard for vision has a significant effect on eye shape and size. Scotopic lizards have eye shapes that are optimized for visual sensitivity, with larger corneal diameters relative to axial lengths. However, photopic lizards do not exhibit absolutely larger axial lengths than do scotopic lizards, and the groups have the same absolute axial lengths of the eye. Results also indicate that the light level the lizard functions under is a more significant influence on eye shape, as defined by the relationship between corneal diameter and axial length of the eye, than is phylogeny.     

Photoreceptor visual fields, ommatidial array, and receptor axon projections in the polarisation-sensitive dorsal rim area of the cricket compound eye

We made intracellular recordings from the photoreceptors of the polarisation-sensitive dorsal rim area of the cricket compound eye combined with dye marking. By measuring visual field sizes and optical axes in different parts of the dorsal rim area, we assessed the optical properties of the ommatidia. Due to the large angular sensitivities (median about 20°) and the high sampling frequency (about 1 per degree), the visual fields overlap extensively, such that a given portion of the sky is viewed simultaneously by a large number of ommatidia. By comparing the dye markings in the retina and in the optic lobe, the axon projections of the retinula cells were examined. Receptors R1, R2, R5 and R6 project to the lamina, whereas R7 projects to the medulla. The microvilli orientation of the two projection types differ by 90° indicating the two analyser channels that give antagonistic input to polarisation-sensitive interneurons. Using the retinal marking pattern as an indicator for the quality of the intracellular recordings, the polarisation sensitivity of the photoreceptors was re-examined. The polarisation sensitivity of recordings from dye-coupled cells was much lower (median: 4.5) than that of recordings in which only one cell was marked (median: 9.8), indicating that artefactual electrical coupling between photoreceptors can significantly deteriorate polarisation sensitivity. The physiological value of polarisation sensitivity in the cricket dorsal rim area is thus typically about 10. Accepted: 4 November 1999     

Y-chromosomal red-green opsin genes of nocturnal New World monkey

The X-chromosomal locality of the red-green-sensitive opsin genes has been the norm for all mammals and is essential for color vision of higher primates. Owl monkeys (Aotus), a genus of New World monkeys, are the only nocturnal higher primates and are severely color-blind. We demonstrate that the owl monkeys possess extra red-green opsin genes on the Y-chromosome. The Y-linked opsin genes were found to be extremely varied, in one male appearing to be a functional gene and in other males to be multicopy pseudogenes. These Y-linked opsin genes should offer a rare opportunity to study the evolutionary fate of genes translocated to the Y chromosome.     

Retinal and optical adaptations for nocturnal vision in the halictid bee<Emphasis Type="Italic"> Megalopta genalis</Emphasis>

The apposition compound eye of a nocturnal bee, the halictid Megalopta genalis, is described for the first time. Compared to the compound eye of the worker honeybee Apis mellifera and the diurnal halictid bee Lasioglossum leucozonium, the eye of M. genalis shows specific retinal and optical adaptations for vision in dim light. The major anatomical adaptations within the eye of the nocturnal bee are (1) nearly twofold larger ommatidial facets and (2) a 4–5 times wider rhabdom diameter than found in the diurnal bees studied. Optically, the apposition eye of M. genalis is 27 times more sensitive to light than the eyes of the diurnal bees. This increased optical sensitivity represents a clear optical adaptation to low light intensities. Although this unique nocturnal apposition eye has a greatly improved ability to catch light, a 27-fold increase in sensitivity alone cannot account for nocturnal vision at light intensities that are 8 log units dimmer than during daytime. New evidence suggests that additional neuronal spatial summation within the first optic ganglion, the lamina, is involved.B.G. is thankful for travel awards from the Royal Physiographic Society, the Per Westlings Fond, the Foundation of Dagny and Eilert Ekvall and the Royal Swedish Academy of Sciences. E.J.W. is grateful for the support of a Smithsonian Short-Term Research Fellowship, the Swedish Research Council, the Crafoord Foundation, the Wenner-Gren Foundation and the Royal Physiographic Society of Lund for their ongoing support     

The visual ecology of fiddler crabs

With their eyes on long vertical stalks, their panoramic visual field and their pronounced equatorial acute zone for vertical resolving power, the visual system of fiddler crabs is exquisitely tuned to the geometry of vision in the flat world of inter-tidal mudflats. The crabs live as burrow-centred grazers in dense, mixed-sex, mixed-age and mixed-species colonies, with the active space of an individual rarely exceeding 1 m². The full behavioural repertoire of fiddler crabs can thus be monitored over extended periods of time on a moment to moment basis together with the visual information they have available to guide their actions. These attributes make the crabs superb subjects for analysing visual tasks and the design of visual processing mechanisms under natural conditions, a prerequisite for understanding the evolution of visual systems. In this review we show, on the one hand, how deeply embedded fiddler crab vision is in the behavioural and the physical ecology of these animals and, on the other hand, how their behavioural options are constrained by their perceptual limitations. Studying vision in fiddler crabs reminds us that vision has a topography, that it is context-dependent and pragmatic and that there are perceptual limits to what animals can know and therefore care about. For Mike Land     

Spectral sensitivities of photoreceptors and lamina monopolar cells in the dragonfly,Hemicordulia tau

Summary Five spectral types of photoreceptors with peak sensitivities at 330 nm, 410 nm, 460 nm, 525 nm and 630 nm were recorded from the ventral eye of the dragonfly, Hemicordulia tau. Often the 525 nm photoreceptors presented broader, and the 630 nm photoreceptors narrower, spectral sensitivities than would be excepted of a photopigment with the same peak sensitivity. Four types of lamina monopolar cells (cell types 1–4) were recognised from their dark-adapted spectral sensitivities and their anatomy. The anatomical identification allows tentative assignation to the monopolar cell classification from Sympetrum rubicundulum obtained using Golgi staining (Meinertzhagen and Armett-Kibel 1982). When dark-adapted, the monopolar cells had peak spectral sensitivities that were similar to single photoreceptors or appeared to pool receptor outputs, but in some cases spectral sensitivity changed markedly upon adaptation to white and to chromatic light, in one case (cell type 2) apparently switching off a UV-sensitive input.     

Tuning of photoreceptor spectral sensitivity in fireflies (Coleoptera: Lampyridae)

Sexual communication between male and female fireflies involves the visual detection of species-specific bioluminescent signals. Firefly species vary spectrally in both their emitted light and in the sensitivity of the eye, depending on the time when each is active. Tuning of spectral sensitivity in three firefly species that occupy different photic niches was investigated using light and electron microscopy, microspectrophotometry, and intracellular recording to characterize the location and spectral absorption of the screening pigments that filter incoming light, the visual pigments that receive this filtered light, and the visual spectral sensitivity. Twilight-active species had similar pink screening pigments, but the visual pigment of Photinus pyralis peaked near 545 nm, while that of P. scintillans had a λ_max near 557 nm. The night-active Photuris versicolor had a yellow screening pigment that was uniquely localized, while its visual pigment was similar to that of P. pyralis. These results show that both screening and visual pigments vary among species. Modeling of spectral tuning indicates that the combination of screening and visual pigments found in the retina of each species provides the best possible match of sensitivity to bioluminescent emission. This combination also produced model sensitivity spectra that closely resemble sensitivities measured either with electroretinographic or intracellular techniques. Vision in both species of Photinus appears to be evolutionarily tuned for maximum discrimination of conspecific signals from spectrally broader backgrounds. Ph. versicolor, on the other hand, appears to have a visual system that offers a compromise between maximum sensitivity to, and maximum discrimination of, their signals. Accepted: 29 September 1999     

Intraspecific variation in retinal cone distribution in the bluefin killifish,<Emphasis Type="Italic"> Lucania goodei</Emphasis>

Studies of visual ecology have typically focused on differences among species while paying less attention to variation among populations and/or individuals. Here, we show that the relative abundance of UV, violet, yellow, and red cones varies between two populations of bluefin killifish, Lucania goodei. Animals from a spring population (high-transmission UV/blue light) have a higher frequency of UV and violet cones and a lower frequency of yellow and red cones than animals from a swamp population (low-transmission UV/blue light). Visual sensitivity does not vary significantly between the populations, but spring animals tend to be more sensitive in the UV/blue wavelengths (360–440 nm) and less sensitive in longer wavelengths (560–600 nm) than swamp animals. The results have two important implications. First, the tight conservation of functional regions of opsin genes across taxa does not imply that visual systems are constrained in their evolution; differential sensitivity can arise through differential expression of cone classes within the retina. Second, intraspecific visual signals in this species may evolve to maximize contrast between the signaler and the background (as opposed to brightness); males with blue anal fins are most abundant in swamp habitats where animals express fewer UV and violet cones.Electronic Supplementary Material Supplementary material is available in the online version of this article at .     

Colour-dependent target detection by bees

The distance over which an object is detected by bees depends on the subtended visual angle and on spectral cues. At large angular subtenses detection is mediated only by chromatic cues. Achromatic targets, however, are also detectable. We investigated how chromatic and achromatic cues interact in detecting large-size targets. Coloured targets were used, with varied chromatic contrast that either did or did not present L-receptor contrast. Better detection correlated with higher chromatic contrast. Adding L-receptor contrast did not affect detection. It did allow the detection of achromatic targets, but at a lower level than most coloured ones, which indicates that the input from the achromatic system is negligible due to low sensitivity.     

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.Dedicated to Professor Rolf Elofsson on the occasion of his retirement from the Chair of Zoology in Lund