Principal Eyes Research Articles

The retinae of Ewyattus bleekeri, an aberrant salticid spider from Queensland

The retinal ultrastructure of an aberrant salticid spider, Euryattus bleekeri (Doleschall, 1859) is described, and discussed in the context of a model of the evolution of the Salticidae previously proposed by Jackson & Blest (1982a). The evolutionary model suggested that the Salticidae are derived from web‐building ancestors that acquired the strategy of invading the webs of other species and families of spiders; it predicts that the evolution of the principal eyes preceded that of the accessory eyes, and that traces of this sequence of events should be observable in contemporary forms. Euryattus exhibits an unusual pattern of web‐dependency (Jackson, 1985). The principal eyes conform to those of ‘advanced’ Salticidae, but the anterior lateral eyes exhibit two features associated, so far, with the primitive Spartaeinae: transverse sections of the rhabdoms present rectangular (rather than circular) profiles, and the non‐pigmented glial cytoplasm is depleted of microtubules. These findings marginally support a case for Euryattus having primitive affinities, but their import is ambiguous, and the evidence cannot be regarded as conclusive. Possible affinities between the Gnaphosidae and Salticidae based upon common tactics of web‐invasion are qualified by a comment on the retinae of the two families.

Fields of View of the Eyes Of Primitive Jumping Spiders

ABSTRACT Most spiders have eight simple eyes, of which one forward-pointing pair (the principal eyes) has a different structure from the other three pairs (the secondary eyes). The principal eyes are often movable, whereas the secondary eyes are fixed. In most jumping spiders (Salticidae) two of the secondary eyes, the postero-median pair, are so reduced that they seem to be vestigial, and their fields of view overlap those of the other secondary eyes (the antero-and postero-laterals) (Homann, 1928; Land, 1969a; Eakin & Brandenburger, 1971). However, in certain supposedly primitive Salticid sub-families the postero-median eyes are comparable in size with the other secondary eyes, and would appear to play a more equal part in the function of the secondary eye system, which is the detection of movement (Land, 1972). The origins of the Salticidae are something of a mystery, and it is therefore of considerable interest to see whether the fields of view of the eyes of these primitive sub-families give any clue that might indicate to which of the other spider families the Salticidae might be linked. The form of the fields of view appears to be a conservative feature in spider evolution (Land, 1985), just as does the layout of the eyes themselves. The anatomy and ultrastructure of these eyes have been described before (Blest, 1983, 1984, 1985; Blest & Sigmund, 1984) and the systematic position of the sub-family considered here, the Spartaeinae, is discussed by Wanless (1984).

Retinal mosaics of the principal eyes of jumping spiders (Salticidae) in some neotropical habitats: optical trade-offs between sizes and habitat illuminances

1. The anatomy and geometrical optics of the principal eyes of some neotropical jumping spiders are examined, with particular reference to the receptors of Layer I of the tiered retina. The consequence of small size and of low habitat illuminances for spatial acuity are assessed. 2. In all phylogenetically advanced salticids examined in the present study, a foveal Layer I receptor contains a single rhabdomere organised as a light-guide. The following sections discuss Layer I: 3. For open-space species, small size minimally prejudices spatial acuities: for the very largePhiale magnifica, optimal spatial acuity is estimated to be 2.3 arc min for adults, and 4.6 arc min for second-instar spiderlings. For adults of the small speciesJollas geniculatus (only slightly larger than second-instarPhiale) we obtain 5.2 arc min. 4. For species occupying habitats in the forest understory, low illuminances appear to prejudice spatial acuity. For adults of the large speciesItata completa which lives beneath broad foliage, we obtain 5.8 arc min; for the small ant-mimicFluda princeps which inhabits the litter layer, we estimate 16.8 arc min. 5. The results indicate that habitat illuminance only constrains retinal design when it is extremely low. Impaired spatial acuities in such dark habitats are predicted to limit behavioural repertoires, and, as a secondary consequence, the number of species that can co-exist in a given forest microhabitat. 6. Receptor illuminances could, in principle, be modulated by adjustments to four factors: (i) focal lengths of the corneal lenses; (ii) the extent, or absence of the pigment stops that lie directly behind them; (iii) the magnification factors afforded by the diverging components of the telephoto lens systems; (iv) the tip diameters of foveal Layer I rhabdomeres. The first parameter is not manipulated: all corneal lenses have roughly the sameF-number (≃ 1.80). Forest species usually lack a pigment stop behind the corneal lens, the power of the diverging component is reduced or virtually absent, and rhabdomere diameters are large. 7. The interface between the retinal matrix and the anterior chamber of the eye is irregularly convexiclivate in advanced salticids, two convexiclivate surfaces forming “saddles” that overlie the narrow dorsal and ventral arms of the retinal mosaics. It is confirmed that inPortia andLyssomanes, both from “primitive” subfamilies, the interfaces are not convexiclivate, as Williams and McIntyre (1980) noted.

Retinal mosaics of the principal eyes of some jumping spiders (Salticidae: Araneae): Adaptations for high visual acuity

Retinal mosaics of the four tiers of receptors (layers I–IV) in the principal eyes of two species of salticid spider known to exhibit high visual acuity are described at the ultrastructural level. The four tiers of receptors have been previously classified byLand (1969 a) andBlestet al. (1981). Only the tier (layer I) farthest from the dioptric system has a mosaic quality capable of sustaining the visual discriminations that have been demonstrated by behavioural experiments. More distal layers are of poor to negligible mosaic organization.

Retinal mosaics of the principal eyes of two primitive jumping spiders, Yaginumanis and Lyssomanes : clues to the evolution of Salticid vision

Retinae of the principal eyes of jumping spiders (Salticidae) have four tiers of photoreceptors. A previous paper described the receptor mosaics in all four layers at the retinal fovea for two forms, Lagnus and Portia , shown by behavioural experiments to possess high visual acuities. Only Layer I farthest from the dioptric apparatus has a mosaic quality that can sustain the demonstrated visual discriminations, leaving the roles of Layers II—III open to question. We now describe the retinal mosaics of two presumptively primitive species Yaginumanis is placed with Portia in a newly erected subfamily of Salticidae, the Spartaeinae, whose members possess functional posterior median eyes; those of Lyssomanes are vestigial as in advanced Salticids, but the genus is usually considered primitive and its ethology indicates restricted visual capabilities. Layer I receptors of Yaginumanis each bear two rhabdomeres on opposite faces of the cell which are contiguous with those of adjacent receptors, so that optical pooling substantially limits acuity. The same arrangement is present in receptors in the peripheral retina of Lyssomanes but at the fovea each cell bears only a single rhabdomere, as in Salticids with high visual acuities. In both species, Layer II receptors have two rhabdomeres throughout the retina and centre-to-centre spacings that approximately match those of the Layer I receptors that they overlie. Layers III and IV are essentially the same in all Salticids: Layer III amounts to a virtually continuous sheet of rhabdomeres, and Layer IV is divided into three regions with a complex organisation. Neither is suitable to sustain fine visual discriminations. The organization of the salticid principal retina emerges as anatomically conservative, and contrasts with that of the secondary eyes which varies greatly between primitive and advanced species. A working hypothesis is proposed to explain its evolution.

The Distances at Which a Primitive Jumping Spider,Portia Fimbriata, Makes Visual Discriminations

ABSTRACTThe anterior median (AM) or principal eyes of the primitive jumping spider, Portia fimbriata (Doleschall), are miniature telephoto systems (Williams & McIntyre, 1980). Another study on the AM eyes of Plexippus suggests that most salticid principal eyes may be of similar design (Blest, Hardie, McIntyre and Williams, 1982). Both studies assumed, from anecdotal evidence (e.g. Forster, 1979), that jumping spiders can make visual discriminations between prey and mates at distances of ca. 20 cm. This estimate is necessary to the functional analyses that were essayed; because it is impossible to make sufficiently accurate direct measurements of some of the parameters of these small eyes, their optics can only be modelled with confidence when something is known about what they are designed to see. Land (1969 a, b), in an elegant optical study, followed Drees (1952) in stating that jumping spiders respond to significant objects some 5-10 body-lengths in front of them. In the case of Portia, this would be a distance of no more than 10 cm at most. Recognition of objects is mediated through the AM eyes (Drees, 1952).

The spectral sensitivities of identified receptors and the function of retinal tiering in the principal eyes of a jumping spider

1. The functional organisation of the central retina of the anterior median (AM) eyes of a jumping spider,Plexippus (Salticidae) is examined by anatomical, electrophysiological and optical methods. A model of the eye is derived from the data. 2. The anatomy of the AM eye is similar to that of salticid eyes described by Land (1969a) and Williams and McIntyre (1980). There are four tiers of receptors of which only the most proximal (Layer I) is a regular mosaic with rhabdoms designed to have light-guide properties. The receptor population of Layer I is homogeneous, whereas in Layers II–IV more than one receptor type can be considered to contribute to each layer. 3. Intracellular recordings from AM photoreceptors reveal only two spectral classes: green cells with peak responses at ca. 520 nm, and ultraviolet (UV) cells with peak responses at ca. 360 nm. ERGs from intact retinae exhibit similar peaks. Spectral sensitivities from pooled intracellular recordings from green cells and ERGs correspond reasonably closely. The comparison does not, therefore, support the possibility that the retina contains receptors with peak responses at longer wavelengths, although it does not exclude it. 4. Spectrally characterised cells were marked by the injection of Lucifer Yellow. From the results of 13 successful injections, (a) peripheral Layer I and peripheral and central Layer II cells are green receptors; (b) Layer IV cells are UV receptors. Central Layer I and Layer III receptors were not marked. 5. The chromatic aberration, focal length and other optical parameters of the corneal lens of the AM eye were measured directly. The lens functions essentially as a single-surface lens of refractive index 1.40, and, together with the curved interface between the anterior chamber of the eye and the receptor matrix, forms a telephoto system. 6. The spacing between receptor Layers I and IV is matched to the chromatic aberration of the eye; if green light from an object in front of the spider is focused on Layer I, UV light will be focused on Layer IV (and Layer III). 7. The distal ends of Layer I receptors form a staircase, those lying laterally being closer to Layer II than those lying medially. This staircase enables the spider to receive in-focus images from objects at distances between ca. 3 cm — ∞ in front of it. It is suggested that the scanning movements of the retinae described by Land (1969b) serve to sweep an image across the staircase so that it will be in focus on some part of Layer I, provided that the object is within that range of distances. 8. Retinal tiering (including the staircase of Layer I) compensates both for the chromatic aberration of the dioptrics of the eye and for its inability to accommodate.

The principal eyes of a jumping spider have a telephoto component

Jumping spiders are a cosmopolitan family (Salticidae) of predators that can make visual discrimination between prey and mates1,2. This task is mediated through the anterior median eyes, described by Land3 as consisting of a corneal lens and a motile retina that comprises four layers of receptors embedded in a matrix. The retinal matrix contains a pit distal to the receptors and symmetrically centred on-axis. We have now found that in Portia fimbriata (Doleschall) and some other species, this pit has a refracting interface that increases the focal length of the eye beyond its axial length, thereby magnifying the retinal image and increasing visual resolving power above that possible with only a corneal lens. The most effective part of the conical pit is its rounded apex, which augments the corneal lens to provide a telephoto system that increases the overall focal length by about 1½ times. This mechanism is of particular value to small spiders like P. fimbriata, for the possible axial length of their eyes is constrained by the small size of their prosomae (Fig.1).

The neural organization of the first optic ganglion of the principle eyes of jumping spiders (Salticidae).

AbstractThe first optic ganglion (FOG) of the principal eyes of jumping spider has been studied by both light and electron microscopy. Each FOG receives projections from the ipsilateral principal eye in a compact optic nerve. Some of the retinal axons, as they pass to the ganglion, cross in a chiasm within the optic nerve. The FOG is composed of a rind of nerve cell bodies which are unipolar cells giving rise anteriorly to second order nerve fibers in the central neuropile of the ganglion and posteriorly to processes which pass into the second optic ganglion. The neuropil is composed of neural and glial processes and of scattered glial cell bodies and it can be divided into a terminal zone and a fibrous zone. The terminal zone is the site of termination for all of the retinal axons. A unique feature of the retinal axon terminals is the presence of numerous fine post‐terminal processes extending away from the main portion of the retinal terminal. The fibrous zone is composed of second order nerve fibers with terminals in the terminal zone and it is continuous with a connective between the FOG and the second optic ganglion called the chiasm where the majority of the second order fibers cross.All of the synapses in the FOG are modified ribbon synapses and occur in the terminal zone within ensheathed synaptic glomeruli as dyads or triads. Large retinal terminals containing pleomorphic vesicles are presynaptic to smaller second order terminals containing spherical vesicles. Second order terminals are also presynaptic to retinal terminals in addition to forming serial‐like synapses with each other.

Ultraviolet and green receptors in principal eyes of jumping spiders.

Spectral sensitivities of cells in principal eyes of the jumping spider Phidippus reqius were measured using techniques of intracellular recording. Three types of cells were found. UV cells had peak sensitivities at 370 nm and were over 4 log units less sensitive at wavelengths longer than 460 nm. Green-sensitive cells had spectral sensitivities which were well fit by nomogram curves peaking at 532 nm. UV-green cells had dual peaks of sensitivity at about 370 and 525 nm, but the ratios of UV-to-green sensitivities varied over a 40: 1 range from cell to cell. Moreover, responses of UV-green cells to flashes of UV light were slower than to flashes of green light. Segregation of receptor types into the known layers of receptors in these eyes could not be shown. It is concluded that jumping spiders have the potential for dichromatic color vision.

Dual sensitivities of cells in wolf spider eyes at ultraviolet and visible wavelengths of light.

Intracellular recordings have been made from visual cells in principal and secondary eyes of in vitro wolf spider preparations. The responses of all cells to all wavelengths of light were graded depolarizations; no hyperpolarizations or nerve discharges were seen. Cells in a secondary eye, the anterior lateral eye, had a maximum sensitivity in the visible at 510 nm and a secondary maximum, or shoulder, of sensitivity in the near ultraviolet at 380 nm. Cells in principal eyes, the anterior median eyes, all responded maximally both in the visible at 510 nm and in the ultraviolet at 360-370 nm or less. However, there was no typical ratio of ultraviolet to visible sensitivities; the differences in log sensitivities (log UV/VIS) varied from 3.3 to -0.5. Each principal eye had a population of cells with different ratios. These populations varied with the time of the year, possibly due to changes in light upon the animals. Chromatic adaptations of cells in anterior median (but not anterior lateral) eyes resulted in small, selective changes in spectral sensitivities, and there was some facilitation of responses from cells repeatedly stimulated. It is concluded that cells of secondary eyes contain only a visual pigment absorbing maximally in the visible, while cells of principal eyes probably contain variable amounts of both this pigment and one absorbing in the ultraviolet as well.

Structure of the retinae of the principal eyes of jumping spiders (Salticidae: dendryphantinae) in relation to visual optics.

ABSTRACT The retinae of the principal (AM) eyes of jumping spiders contain four layers of receptors, one behind the other with respect to the incident light. The distribution of receptors in each layer has been determined. The deepest layers (1 and 2) cover the whole area of the retina, and have the greatest density of receptors. The minimum receptor separation is 1.7 μm., or 11 min. visual angle. The more superficial layers (3 and 4) are confined to the central region of the retina. In layers 1, 2 and 3 the rhabdomere-containing segments are rod-shaped, and are parallel to the incident light. In layer 4 they are ovoid, and are oriented approximately at right angles to the light. At the first optic glomerulus the primary fibres from each receptor layer appear to terminate in separate regions of neuropile. The focal lengths, radii of curvature and refractive indices of the lenses of the principal and side eyes have been measured. For the principal eyes, estimates have also been made of the diffraction limit, the depth of focus, and the magnitudes of chromatic and spherical aberration. The normal position of the image in the eye was found by ophthalmoscopy. For blue-green light, the best image of distant objects is formed on the next-to-deepest layer (2). The deepest layer (1) is conjugate with a plane about 2 cm. in front of the animal for blue-green light, or with infinity for red light, because of the eye’s chromatic aberration. Two theories are offered to account for the retinal layering. Either the spider uses different layers to examine maximally sharp images of objects at different dis tances; or each layer exploits the sharpest image of distant objects, but for light of different wavelengths. Optical considerations indicate that either theory is possible, but the seconds (wavelength) theory is the more probable, because jumping spiders are known to possess colour vision. It predicts that layer 1 receptors contain red-sensitive, layer 2 blue-green sensitive and layer 3 violet-ultraviolet Sensitive pigments. The structural peculiarities of the most superficial layer (4), and the fact that it is not conjugate with any plane in front of the animal for any visible wavelength, suggest that it is not resolving an image, but performing some other function. Reasons are given for thinking that this might be the analysis of the pattern of polarization of skylight.

Movements of the retinae of jumping spiders (Salticidae: dendryphantinae) in response to visual stimuli.

ABSTRACT Movements made by the principal eyes of jumping spiders (Phidippus and Metaphidippus spp.) have been investigated using an ophthalmoscopic technique which permits simultaneous observation and stimulation of the retinal surface. The eye-movements are produced by six muscles. Four are attached to the carapace, and displace each retina latero-medially and dorso-ventrally. The remaining pair are thin bands of muscle which encircle the eye-tube. TThe nerve supplying these muscles contains only six axons. Each axon terminates in one of the six muscles. The nerve supplying these muscles contains only six axons. Each axon terminates in one of the six muscles. Four types of eye-movements are observed. These are spontaneous activity, saccades, tracking and scanning. All movements are usually conjugate. Spontaneous activity consists of a very variable, periodic side-to-side motion of the retinae. It is associated with states of high excitability, and occurs whether or not there is any structure in the field of view. Saccades occur when a small stimulus (e.g. a dark dot) is presented to, or moved upon, the retinae of either the principal eyes or the antero-lateral eyes. In a saccade the retinae move towards the image of the target so that they come to rest with their central regions fixated on the target. If the target moves the retinae track it, maintaining central fixation. Scanning normally follows a saccade. It consists of an oscillatory, side-to-side movement of the retinae across the stimulus, with a period of 1-2 sec., and a simultaneous torsional movement in which the retinae partially rotate about the visual axes, through an angle of approximately 50° and with a period of 5-15 sec. Jumping spiders distinguish other jumping spiders from potential prey by the geometry of their legs. It is suggested that scanning is a pattern-recognition procedure in which the torsional movements are concerned with the spatial alignment of line or edge detectors, and the horizontal component with providing relative motion between these detectors and the stationary stimulus.

Spectral sensitivities of wolf spider eyes.

ERG's to spectral lights were recorded from all eyes of intact wolf spiders. Secondary eyes have maximum relative sensitivities at 505-510 nm which are unchanged by chromatic adaptations. Principal eyes have ultraviolet sensitivities which are 10 to 100 times greater at 380 nm than at 505 nm. However, two animals' eyes initially had greater blue-green sensitivities, then in 7 to 10 wk dropped 4 to 6 log units in absolute sensitivity in the visible, less in the ultraviolet. Chromatic adaptations of both types of principal eyes hardly changed relative spectral sensitivities. Small decreases in relative sensitivity in the visible with orange adaptations were possibly retinomotor in origin. Second peaks in ERG waveforms were elicited from ultraviolet-adapted principal eyes by wavelengths 400 nm and longer, and from blue-, yellow-, and orange-adapted secondary eyes by wavelengths 580 nm and longer. The second peaks in waveforms were most likely responses of unilluminated eyes to scattered light. It is concluded that both principal and secondary eyes contain cells with a visual pigment absorbing maximally at 505-510 nm. The variable absolute and ultraviolet sensitivities of principal eyes may be due to a second pigment in the same cells or to an ultraviolet-absorbing accessory pigment which excites the 505 nm absorbing visual pigment by radiationless energy transfer.

The fine structure o the visual system of Lycosa (Araneae: Lycosidae). II. Primary visual centers.

Wolf spiders have four pairs of eyes distributed in three rows. The first row which lie in the frontal region of the caparace, just above the chelicera, contains four eyes: a medial pair known as the anterior medial eyes (AM eyes or principal eyes) and two smaller eyes known as the anterior lateral eyes (AL eyes). The second row which is located also in the frontal region of the prosoma consists of two big eyes. These are the posterior median eyes (PM eyes). The third row contains the posterior lateral eyes (PL eyes) which lie in the flanks of the prosomal caparace. The AL, PM and PL eyes are the so-called secondary eyes.