Development of the compound eyes of dragonflies (Odonata). IV. Development of the adult compound eyes

The changes in the directions of view of marked larval ommatidia were observed after the emergence of the adult. Those ommatidia that had been present during the first larval instar had the most posterior directions of view in the adult visual field while the newest ommatidia that had not been functional for vision in the aquatic larva contributed to the anterior and dorsal foveas of the aerial adults. The changes in interommatidial angles at emergence are discussed. Contrary to the general trend for interommatidial angles between retained larval ommatidia to decrease at emergence, the interommatidial angles in the larval fovea of aeshnid visual predators increase at emergence. The modifications in an odonate compound eye at emergence are like an exaggeration of the modifications that occur at the moult from one larval instar to the next, except that the newest ommatidia do not have any compromises in their design for use in the aquatic vision of the larvae. This is in contrast to the ommatidia retained from the earliest larval instars which have to have the most compromises in their design so that they can be adapted for the visual requirements of every larval instar, as well as the adult. This is discussed in relation to the trend among advanced species of odonates to replace the larval ommatidia by an entirely new set of adult ommatidia.     

Development of the compound eyes of dragonflies (Odonata). III. Adult compound eyes

The distribution of ommatidial diameters and interommatidial angles, as determined by measuring the angles between the optic axes of adjacent ommatidia, are mapped across the surface of the compound eyes of a variety of species selected for different adult behaviors, developmental histories, and taxonomic positions. The size of the visual fields, prey capture foveas, foveas composed of large dorsal ommatidia, and other specializations in the numbers of ommatidia that view various directions in the visual field are discussed in relation to adult behavior. Advanced species have less resemblance between their larval and adult eyes than primitive species. In contrast to their larvae, adults increase the monocular resolution of each eye at the expense of binocular vision. Most species have foveas which view in approximately the anterior direction, instead of in a region of binocular overlap, and many species have foveal bands which view along the horizon. Some advanced perching species, which approach their prey and other odonates from below, have an additional vertical foveal band that views along a vertical plane from the anterior direction to a more dorsal direction. The most unusual foveal band is seen in active flying species. The large dorsal ommatidia of the migratory Anax junius, which cover approximately one third of the eye surface, view a narrow region of the visual field that extends along a plane from the most lateral direction of one eye to a dorsal direction, and continues without interruption to the most lateral direction of the other eye.     

Development of the compound eyes of the water stick insect, Ranatra linearis

ABSTRACT. Relationships between estimation of predator-prey distance prior to a capture attempt and some features of the compound eye are investigated at all stages of post-embryonic development. Interommatidial angles increase gradually from the anterior and the dorsal regions to the posterior and ventral regions. Facet diameters vary only slightly over the eye surface but increase with age. New ommatidia appear around the borders of eye after each moult. The older ommatidia are pushed away from the border. From one instar to another ommatidia change their direction of view from between 10 to 30 relative to the body axes. This change in direction far exceeds the calculated changes in direction that would be optimal if ommatidia were to continue viewing the same relative directions in space. This suggests a high degree of plasticity of the underlying neuronal networks.     

Visual field structure in the Empress Leilia, Asterocampa leilia (Lepidoptera, Nymphalidae): dimensions and regional variation in acuity

Male Empress Leilia butterflies ( Asterocampa leilia) use a sit-and-wait tactic to locate mates. To see how vision might influence male behavior, we studied the morphology, optics, and receptor physiology of their eyes and found the following. (1) Each eye's visual field is approximately hemispherical with at most a 10 degrees overlap in the fields of the eyes. There are no large sexual differences in visual field dimensions. (2) In both sexes, rhabdoms in the frontal and dorsal ommatidia are longer than those in other eye regions. (3) Interommatidial angles are smallest frontally and around the equator of the eye. Minimum interommatidial angles are 0.9-1 degrees in males and 1.3-1.4 degrees in females. (4) Acceptance angles of ommatidia closely match interommatidial angles in the frontal region of the eye. We conclude that vision in these butterflies is mostly monocular and that males have more acute vision than females, especially in the frontal region (large facets, small interommatidial angles, small acceptance angles, long rhabdoms, and a close match between interommatidial angles and acceptance angles). This study also suggests that perched males direct their most acute vision where females are likely to appear but show no eye modifications that appear clearly related to a mate-locating tactic.     

Allometry and resolution of bee eyes (Apoidea)

A sample of compound eyes from 15 species of female pollen foraging bees (apiform Apoidea) was morphometrically analyzed. These species were chosen for size differences, different social organization, and a wide geographic and taxonomic distribution (Apidae, Megachilidae, Andrenidae, Halictidae). The results demonstrate the following characteristics for the typical compound eye in female foraging bees: (1) the vertical diameter of the eye is about twice the horizontal diameter; (2) the eyes of diurnal foragers scale isometrically with body size; (3) the eyes of three species of nocturnal foragers have about 1.8 times the surface area as compared to diurnal foragers of matching size; (4) the number of ommatidia per eye range from about 1000 in Perdita minima to about 16 000 in Xylocopa latipes; and (5) the corresponding mean interommatidial angles range from 4.7 to 1.2 degrees . Body size, rather than species-specific ecological adaptation, is the major (97%) determinant of the number of ommatidia per eye in diurnal, as well as nocturnal foragers. The number of ommatidia per eye, and hence the visual resolution, is proportional to the square root of both body size and eye size across all species studied. The eye parameter (the product of the mean interommatidial angle and the mean lens diameter) increases slightly with decreasing body size. All this is taken as evidence that the features of the bees' visual macro-niche remained largely constant over the roughly 130 million years of their macro-evolution.     

Micro-optical artificial compound eyes

Natural compound eyes combine small eye volumes with a large field of view at the cost of comparatively low spatial resolution. For small invertebrates such as flies or moths, compound eyes are the perfectly adapted solution to obtaining sufficient visual information about their environment without overloading their brains with the necessary image processing. However, to date little effort has been made to adopt this principle in optics. Classical imaging always had its archetype in natural single aperture eyes which, for example, human vision is based on. But a high-resolution image is not always required. Often the focus is on very compact, robust and cheap vision systems. The main question is consequently: what is the better approach for extremely miniaturized imaging systems-just scaling of classical lens designs or being inspired by alternative imaging principles evolved by nature in the case of small insects? In this paper, it is shown that such optical systems can be achieved using state-of-the-art micro-optics technology. This enables the generation of highly precise and uniform microlens arrays and their accurate alignment to the subsequent optics-, spacing- and optoelectronics structures. The results are thin, simple and monolithic imaging devices with a high accuracy of photolithography. Two different artificial compound eye concepts for compact vision systems have been investigated in detail: the artificial apposition compound eye and the cluster eye. Novel optical design methods and characterization tools were developed to allow the layout and experimental testing of the planar micro-optical imaging systems, which were fabricated for the first time by micro-optics technology. The artificial apposition compound eye can be considered as a simple imaging optical sensor while the cluster eye is capable of becoming a valid alternative to classical bulk objectives but is much more complex than the first system.     

The eyes of mesopelagic crustaceans

Summary In Streetsia challengeri left and right eyes have fused and become a single cylindrical photoreceptor, which occupies the basal half of a forward directed head projection. This unusual compound eye consists of approximately 2500 ommatidia, which are arranged in such a way that the animal has almost circumferential vision, but cannot look ahead or behind. It is thought that the eye operates on light-guide principles, and that the crystalline cones are the major dioptric component. Ommatidia in anterior-posterior rows show a greater overlap of visual fields than dorso-ventrally arranged ommatidia. Cone layer and retinula are separated by a 4 m thick screen-membrane, which contains tiny pigment granules of 0.15 m diameter. Cells of unknown function and origin, containing unusual multitubular organelles, are regularly found near the proximal ends of the crystalline cone threads. The twisted rhabdoms measure 18–20 m in diameter, and consist of microvilli 0.05 m in width, which belong to five retinula cells and which show no trace of disintegration. The position of interommatidial screening pigment, the density of retinula cell vesicles and inclusions, and the narrowness of the perirhabdomal space all suggest that the eyes have been light-adapted at the time of fixation for electron microscopy. The retinula cell nuclei lie on the proximal side of the heavily pigmented basement membrane. A tapetum or basal retinula cells are not developed. It is concluded that the eye optimally combines acuity with sensitivity, and that for distance estimation parallax may be important.Address until January 25th 1978: Scott Base, Ross Dependency, Antarctica (C/-Chief Post Office, Christchurch, New Zealand)     

Visual behaviour and the structure of dark and light-adapted larval and adult eyes of the New Zealand glowworm Arachnocampa luminosa (Mycetophilidae: Diptera)

Both larval and adult New Zealand cave glowworms exhibit reactions to light; their photoreceptors must, therefore, be regarded as functional. The two principal stemmata of the larva possess large biconvex lenses and voluminous rhabdoms. Approximately 12 retinula cells are present. In light-adapted larvae the diameter of the rhabdom is 8 μm and that of an individual microvillus is 49.5 nm. Dark-adapted eyes have rhabdoms that measure 14 μm in cross section and microvilli with an average diameter of 54 nm. The compound eye of the adult comprises approximately 750 ommatidia, each with a facet diameter of 27–28 μm. A facet is surrounded by 1–6 interommatidial hairs which are up to 30 μm long. The interommatidial angle is 5.5°. Cones, consisting of 4 crystalline cone cells, are of the ‘acone’ type. Pigment granules in the primary pigment cells are twice as large as those of the retinula cells which measure 0.6–0.75 μm in diameter. The rhabdom is basically of the dipteran type, i.e. six open peripheral rhabdomeres surround 2 central rhabdomers arranged in a tandem position. The microvilli of cells 1–6 and cell 8 have diameters ranging from 68 to 73 nm, but those of the distally-located central rhabdomere 7 are 20% larger. This is irrespective of whether the eye is dark or light-adapted. In the latter the cones are long and narrow, the screening pigment granules closely surround the rhabdomeres, and the rhabdom is less voluminous than that of the dark-adapted eye.     

The spatial resolutions of the apposition compound eye and its neuro-sensory feature detectors: observation versus theory

For 100 years three ideas dominated efforts to understand the apposition compound eye. In Müller's theory, the eye viewed the panorama through an array of little windows without overlaps and without gaps, with no details within windows. Spatial resolution then depended on the interommatidial angle (Deltaphi) and the number of ommatidia. In the second proposal, the insect detected the temporal modulation of the light, which was limited by the aperture of the lens and the wavelength, assuming good focus. Modulation is the change of intensity in the receptor, usually caused by motion of a spatial contrast in the stimulus. Thirdly, motion was detected from the successive temporal modulations at adjacent visual axes. Recently, two more principles arose. The light-sensitive elements, called rhabdomeres, project through the nodal point of the lens to the outside world, and the resolution was limited by their grain size, like the pixels in a digital camera. Finally, detection of contrast and colour was limited by the signal/noise ratio (SNR) which was improved by brighter light and more visual pigment. These five physical principles provide satisfying explanations of eye function but they all originated from theory. Actual measurements of resolution depend on the operation of the test. The visual system of the honeybee recognizes a limited variety of simple cues, but there is no evidence that the pattern of ommatidial stimulation is re-assembled, or even seen. The known cues are: the temporal modulation of groups of receptors, the direction and angular velocity of motion, some measure of the spatial disruption of the pattern or the length of edge (related to spatial frequency and contrast), colour, the intensity, the position of the centre and the size of large well-separated areas of black or colour, the angle of orientation of a bar or grating, radial or tangential edges, and bilateral symmetry. Neurons connected to more than two adjacent ommatidia collaborate in the detection of cues, and the resolution depends on the neuro-sensory feature detectors at work at the time. Although some behavioural and electrophysiological measurements give a spatial resolution similar to the interommatidial angle, different spatial properties of neuro-sensory detectors predominate at different light intensities and with a diurnal rhythm. During the long history of this topic, the belief that the resolution ought to be Deltaphi has frequently been overturned by experimental measurement.     

Visual orientation by the crown-of-thorns starfish (<Emphasis Type="Italic">Acanthaster planci</Emphasis>)

Photoreception in echinoderms has been known for over 200 years, but their visual capabilities remain poorly understood. As has been reported for some asteroids, the crown-of-thorns starfish (Acanthaster planci) possess a seemingly advanced eye at the tip of each of its 7–23 arms. With such an array of eyes, the starfish can integrate a wide field of view of its surroundings. We hypothesise that, at close range, orientation and directional movements of the crown-of-thorns starfish are visually guided. In this study, the eyes and vision of A. planci were examined by means of light microscopy, electron microscopy, underwater goniometry, electroretinograms and behavioural experiments in the animals’ natural habitat. We found that only animals with intact vision could orient to a nearby coral reef, whereas blinded animals, with olfaction intact, walked in random directions. The eye had peak sensitivity in the blue part (470 nm) of the visual spectrum and a narrow, horizontal visual field of approximately 100° wide and 30° high. With approximately 250 ommatidia in each adult compound eye and average interommatidial angles of 8°, crown-of-thorns starfish have the highest spatial resolution of any starfish studied to date. In addition, they have the slowest vision of all animals examined thus far, with a flicker fusion frequency of only 0.6–0.7 Hz. This may be adaptive as fast vision is not required for the detection of stationary objects such as reefs. In short, the eyes seem optimised for detecting large, dark, stationary objects contrasted against an ocean blue background. Our results show that the visual sense of the crown-of-thorns starfish is much more elaborate than has been thus far appreciated and is essential for orientation and localisation of suitable habitats.     

Egfr signalling defines a protective function for ommatidial orientation in the Drosophila eye

Ommatidial rotation in the Drosophila eye provides a striking example of the precision with which tissue patterning can be achieved. Ommatidia in the adult eye are aligned at right angles to the equator, with dorsal and ventral ommatidia pointing in opposite directions. This pattern is established during disc development, when clusters rotate through 90 degrees, a process dependent on planar cell polarity and rotation-specific factors such as Nemo and Scabrous. Here, we demonstrate a requirement for epidermal growth factor receptor (Egfr) signalling in rotation, further adding to the manifold actions of this pathway in eye development. Egfr is distinct from other rotation factors in that the initial process is unaffected, but orientation in the adult is greatly disrupted when signalling is abnormal. We propose that Egfr signalling acts in the third instar imaginal disc to 'lock' ommatidia in their final position, and that in its absence, ommatidial orientation becomes disrupted during the remodelling of the larval disc into an adult eye. This lock may be achieved by a change in the adhesive properties of the cells: cadherin-based adhesion is important for ommatidia to remain in their appropriate positions. In addition, we have evidence that there is an error-correction mechanism operating during pupal stages to reposition inappropriately orientated ommatidia. Our results suggest that initial patterning events are not sufficient to achieve the precise architecture of the fly eye, and highlight a novel requirement for error-correction, and for an Egfr-dependent protection function to prevent morphological disruption during tissue remodelling.     

Eye morphology and optics of the double-eyed mysid Euchaetomera typica

The structure and optics of the mesopelagic double-eyed mysid crustacean Euchaetomera typica Sars, 1884 are described for the first time. The lateral eye is a typical refracting superposition eye with a wide field of view (172°) and low resolution (interommatidial angle of 7.3°). The antero-dorsal part of the eye is elongated due to the extension of the clear zone. This dorsal eye has a restricted field of view (33°) but much higher resolution (1.5°). The dorsal eye also uses refracting superposition optics, although the optical array is unusual as many of the peripheral ommatidia lack crystalline cones. The centre of curvature of the cornea is in front of the flattened rhabdom layer whereas the axes of the crystalline cones are centred on a point about twice as deep as the rhabdom layer. This results in a well-focused eye, free of spherical aberration. There is a remarkable similarity in eye structure between this species and some mesopelagic double-eyed euphausiid crustaceans.     

Arrangement of optical axes and spatial resolution in the compound eye of the female blowfly Calliphora

We determined the optical axes of ommatidia in the wild-type female blowfly Calliphora by inspecting the deep pseudopupil in large parts of the compound eye. The resulting map of optical axes allowed us to evaluate the spatial resolution in different parts of the eye in terms of interommatidial angles as well as the density of optical axes, and to estimate the orientation of ommatidial rows along the hexagonal eye lattice. The optical axes are not homogeneously distributed over the eye. In the frontal visual field the spatial resolution is about two times higher than in its lateral part and about three times higher as compared to the eye's dorsal pole region. The orientation of the ommatidial rows along the eye lattice is not the same for different regions of the eye but changes in a characteristic way. The inter-individual variability in the orientation of the ommatidial rows is estimated to be smaller than 8 degrees . The characteristic arrangement of the ommatidial lattice is discussed as an adaptation for efficient evaluation of optic flow as induced during self-motions of the animal.     

Morphological specializations of dorsal rim ommatidia in the compound eye of dragonflies and damselfies (Odonata)

We have examined the fine structure of dorsal rim ommatidia in the compound eye of the three odonate species Sympetrum striolatum, Aeshna cyanea and Ischnura elegans. These ommatidia exhibit several specializations: (1) the rhabdoms are very short, (2) there is no rhabdomeric twist, and (3) the rhabdoms contain only two, orthogonally-arranged microvillar orientations. The dorsal rim ommatidia of several other insect species are known to be anatomically specialized in a similar way and to be responsible for polarization vision. We suggest that the dorsal rim area of the odonate compound eye plays a similar role in polarization vision. Since the Odonata are a primitive group of insects, the use of polarized skylight for navigation may have developed early in insect phylogeny.     

Structural changes in light- and dark-adapted compound eyes of the australian earwig Labidura riparia truncata (dermaptera)

The apposition acone eye of Labidura is relatively small—550–600 facets—with a thick corneal lens and shallow retina. The retinula cell columns are each formed of six peripheral cells plus two central cells, a partially fused rhabdom, and dense pigment in two or three cell types. Upon adaptation from light to dark, the most striking photomechanical response is a proximal broadening of the cone cells, which results in a 38-fold increase in cross-sectional area of the aperture. While longitudinal rhabdom movement is small, microvillar diameters swell in response to light and contract in the dark. Irregularities of facet pattern and shape, and in ommatidial alignment were found, particularly towards eye margins. Three types of interommatidial sense organs on the eye surface are described, one of which has not been previously reported. An argument is presented to explain how the field of view and sensitivity are both apparently decreased in the acone eye by exposure to light.     

<Emphasis Type="Italic">echinus</Emphasis>, required for interommatidial cell sorting and cell death in the <Emphasis Type="Italic">Drosophila</Emphasis> pupal retina,encodes a protein with homology to ubiquitin-specific proteases

Background  

Programmed cell death is used to remove excess cells between ommatidia in the Drosophila pupal retina. This death is required to establish the crystalline, hexagonal packing of ommatidia that characterizes the adult fly eye. In previously described echinus mutants, interommatidial cell sorting, which precedes cell death, occurred relatively normally. Interommatidial cell death was partially suppressed, resulting in adult eyes that contained excess pigment cells, and in which ommatidia were mildly disordered. These results have suggested that echinus functions in the pupal retina primarily to promote interommatidial cell death.     

Optical parameters of euphausiid eyes as a function of habitat depth

Summary The relationships between habitat depth, eye diameter relative to body length, and the dimensions of rhabdoms and crystalline cones have been examined for 13 species of three oceanic euphausiid genera with habitats ranging from near-surface waters to the deep-sea. Rate of eye growth decreases with depth. Longer rhabdoms may increase the visual sensitivity to point and extended light sources by an eye of a particular size with depth. Larger interommatidial angles suggest that visual acuity decreases at depth. Depth-related changes in euphausiid eyes are considered with respect to the probable roles of vision and bioluminescence in the deep-sea. Unusual features of the eyes of several species are described.     

Distribution of photoperiodic receptors in the compound eyes of the bean bug, Riptortus clavatus

  The bean bug, Riptortus clavatus shows a long-day photoperiodic response with respect to the control of adult diapause. The location of photoreceptors for photoperiodism was examined in this species by complete or partial removal of photoreceptor organs. Even after one compound eye or both ocelli were removed, the insects were sensitive to photoperiod. After both compound eyes were removed, however, the insects became reproductive regardless of the photoperiod. Therefore, photoreceptors for photoperiodism were not in the ocelli but in the compound eyes. To clarify whether ommatidia in compound eyes have a regional difference in reception of photoperiod, sensitivity to photoperiod was examined after one compound eye and a part of the contralateral one were removed. Only when the central region of compound eyes was removed did the insects lose sensitivity to photoperiod. It is concluded that the ommatidia in the central region of compound eyes play a principal role in the reception of photoperiod. Accepted: 23 September 1996     

The optics of tsetse fly eyes in relation to their behaviour and ecology

Abstract The visual acuity of two species of tsetse flies, Glossina morsitans morsitans Westw. and Glossina pallidipes Aust., was investigated. Male G. morsitans eyes have an acute zone in the forward region, with large hexagonal lenses (mean minimum diameter, D=33, SE±0.7 μm), relatively small interommatidial angle (Δ(φ=1.08^o) and angular receptive field of individual ommatidia (Δp) of not less than 1.14^o. A narrow band of square lenses, with intermediate diameter and Δφ, merges with smaller hexagonal lenses in the periphery (24±0.7 μm), with relatively large interommatidial angle (Δφ=3.7^o) and small angular receptive field (Δp = c. 1.6^o). G.pallidipes eyes are similar, except that the lenses in the acute zone are larger than those of G.morsitans , in proportion to their larger body size. Female eyes are not significantly different from male eyes, except that they have a narrower region of binocular overlap (maximum for males = 24^o, for females = 18^o). The eye parameter (p=DΔφ) in the acute zone of male G.morsitans = 0.62, and in the peripheral zone = 1.56. These relatively high values are consistent with fast flight, visual detection of drift due to low wind speeds, mating chases and discrimination of cryptic host animals at high light intensities. The extended region of binocular overlap in males may serve as an early warning system of the approach of potential females. From our estimates, tsetse flies ought to be able to detect small objects against the sky c. 30 min before sunrise and after sunset, and to use their peripheral vision perhaps 15 min earlier and later than this.     

Mechanisms of eye development and evolution of the arthropod visual system: The lateral eyes of myriapoda are not modified insect ommatidia

The lateral eyes of Crustacea and Insecta consist of many single optical units, the ommatidia, that are composed of a small, strictly determined and evolutionarily conserved set of cells. In contrast, the eyes of Myriapoda (millipedes and centipedes) are fields of optical units, the lateral ocelli, each of which is composed of up to several hundreds of cells. For many years these striking differences between the lateral eyes of Crustacea/Insecta versus Myriapoda have puzzled evolutionary biologists, as the Myriapoda are traditionally considered to be closely related to the Insecta. The prevailing hypothesis to explain this paradox has been that the myriapod fields of lateral ocelli derive from insect compound eyes by disintegration of the latter into single ommatidia and subsequent fusion of several ommatidia to form multicellular ocelli. To provide a fresh view on this problem, we counted and mapped the arrangement of ocelli during postembryonic development of a diplopod. Furthermore, the arrangement of proliferating cells in the eyes of another diplopod and two chilopods was monitored by labelling with the mitosis marker bromodeoxyuridine. Our results confirm that during eye growth in Myriapoda new elements are added to the side of the eye field, which extend the rows of earlier-generated optical units. This pattern closely resembles that in horseshoe crabs (Chelicerata) and Trilobita. We conclude that the trilobite, xiphosuran, diplopod and chilopod mechanism of eye growth represents the ancestral euarthropod mode of visual-system formation, which raises the possibility that the eyes of Diplopoda and Chilopoda may not be secondarily reconstructed insect eyes.