CHAPTER TWENTY SIX
Vision is the perception of light. Insects perceive light through three classes of sensory organs. Most adult insects have a single pair of compound eyes. Larvae of hemimetabolous insects and most adults have usually three simple eyes called ocelli. These are typically located on the dorsum of the head capsule, and they are sometimes called dorsal ocelli. Larvae of holometabolous insects do not have compound eyes. These insects perceive forms, to a limited extent through stemmata located on either side of the head.
The compound eyes are prominent features of adult insects. The eyes occupy a fairly large portion of the surface of insect heads, and they facilitate a rather wide field of vision. Compounds eyes are not present in all insects. They are reduced or absent in parasitic forms, many soil insects, and in some species that live in very dark places, such as caves.
The basic unit of compound eyes is the ommatidium (singular of ommatidia). Ommatidia vary in size and number among insect groups. At one extreme, dragonflies have thousands of ommatidia in each compound eye; many insects have far fewer, and at the other extreme, the workers of the ant species Pomera punctatissima have only one ommatidium in each eye. The sizes of ommatidia vary from about 5 to 40 microns in diameter. Sizes vary among species and even within a single compound eye. In some dragonflies, for example, the dorsal units are considerably larger than the ventral ones.
A figure shows the structure of a single ommatidium. The ommatidium rests on a basement membrane. The height of the eye comes from the long retinula cells and secondary pigment cells. The corneagen cells (sometimes called primary pigment cells) rests atop the long retinula and secondary pigment cells. The crystalline cone lies within the corneagen cells. The surface of the ommatidium is covered with the corneal lens. The corneal lens is a specialized part of insect cuticle. It is secreted by the corneagen cells, which are specialized epidermal cells. The crystalline cone is a clear, intracellular structure synthesized within Sempter cells. The primary pigment cells surround the Sempter cells. Not all compounds eyes feature a crystalline cone; those that do are called eucone eyes.
The corneal lens and crystalline cone make up the optical part of ommatidia. The sensory elements are just under the optical apparatus. The retinula cells are long neurons. Part of each retinula cell is a specialized area known as a rhabdomere. The rhabdom indicated in the figure is a collection of up to eight rhabdomeres. A nerve axon from each retinula cell projects through the basement membrane into the optic nerve. Ommatidia are functionally isolated because the retinula cells are surrounded by the secondary pigment cells.
Compound eyes are commonly categorized as either apposition eyes or superposition eyes. There is no separation between the corneal layer and the photoreceptors in apposition eyes. There is a clear space between the two units in superpositions eyes. Some authors use the expression "clear zone eyes" for the superposition eyes. Superposition eyes are generally found in crepuscular and nocturnal insects, while apposition eyes occur in diurnal insects.
The crystalline cone couples the lens and photoreceptors in apposition eyes. Some higher Diptera have pseudocone eyes. Crystalline cones do not occur in pseudocone eyes, and optical coupling is by means of a gelatinous substance that is contained in a two-celled structure. Still another arrangement is found in some apposition eyes that lack solid cones or gelatinous pseudocones. In these acone eyes four flat transparent cells are found in place of the cones. In superposition eyes the space between the corneal lines and the photoreceptors is traversed by crystalline tracts. These are thought to act as wave-guides that direct light to the photoreceptors.
The eyes of some insects feature a tracheal tapetum, as shown in a figure. Tracheal tapeta are known from several Lepidoptera. Small tracheae run parallel with the longer cells of the ommatidia. It has been suggested that these structures function as interference reflector filters.
Light sensitivity of insect eyes varies according to the state of light- adaptation or dark-adaptation of the eyes. In bright light, the eye is less sensitive to light, and the eye is regarded as light-adapted. Maximum sensitivity occurs in darker conditions, when the eye is fully dark-adapted. Some insect eyes can change light sensitivity by about three orders of magnitude within a few minutes of changing light conditions.
There are a number of mechanisms of adaptation to light and dark conditions. One mechanism relates to the biochemistry of vision. The visual pigment is broken down by interaction with light. In daylight the breakdown rate can equal or exceed the replacement rate. This leads to decreased light sensitivity, and partly explains light adaptation. In the dark, the visual pigment accumulates, and the insect becomes dark adapted.
A second mechanism of adaptation is the movement of screening pigments. Screening pigments are located in the retinula cells. In light-adapted eyes granules of screening pigments surround the rhabdom. These pigments absorb light, and they have the effect of optically isolating individual ommatidia. The endoplasmic reticulum of dark-adapted eyes forms large, clear vesicles. This forms a clear space around the rhabdom, so that a greater amount of light falls upon the rhabdom.
Vision involves the transduction of light energy into a bioelectric signal within the nervous system. The first events in this process take place in the retinula cells. The fine structure of rhabdomeres consists of thousands of closely packed tubules. These tubules are about 500 A in diameter and one micron long. They are aligned at right angles to the long axis of the rhabdom. The visual pigments occur mainly in these rhabdomeric microvilli. It has been suggested that the small diameter of each microvillus inhibits free rotation of visual pigments. This specific orientation may be the molecular basis of insects' sensitivity to polarized light. Photobiological processes occur in a narrow band of the electromagnetic spectrum between 300 and 700 nm. Photons in this region of the spectrum have enough energy for photochemical interactions, but not enough energy to disrupt macromolecules. Visual pigments initiate vision by absorbing light in this region. These pigments are a class of membrane bound proteins known as opsins that are conjugated with a chromophore. Visual pigments whose chromophore is retinal are called rhodopsins. The visual pigments of all invertebrates, including insects, crustaceans and squids, are all rhodopsins.
There are a number of geometric isomers of retinal. The 11-cis isomer is the chromophore of native rhodopsin. Free retinal absorbs light strongly at about 380 nm. When 11-cis-retinal is linked to opsin to form rhodopsin, the main absorption peak is shifted. The maximum absorption values of different rhodopsins range from about 345 nm (ultraviolet) to as high as 610 nm (red). The absorbing properties of any given rhodopsin is related to the disposition of charged opsin groups around the chromophore. These interactions between the side-groups of the amino acids within the opsins and the chromophores are thought to modify thep electron orbital of the chromophores, and thereby modify the absorbance spectra of rhodopsins.
When the chromophore of rhodopsin absorbs a photon, the chromophore undergoes an isomerization from the 11-cis to the all-trans configuration. The rhodopsins of insects and other invertebrates differ from vertebrate rhodopsins on the point of the chemical events that follow the isomerization step. Vertebrate rhodopsins go through a series of spectrally distinct intermediates. The process is called bleaching because the absorption shifts from visible to ultraviolet wavelengths, which we can not see. The vertebrate process can lead to hydrolysis of the opsin and chromophore. Invertebrate rhodopsins generally do not bleach. Light transforms the rhodopsins to a stable intermediate. The isomerized 11-cis chromophore stays in place in the microvilli. The stable intermediates have spectral properties similar to metarhodopsin I of vertebrates, which has earned them the term metarhodopsins.
The mechanism of transducing light-induced chemical changes in rhodopsins into electrical signals remains the major unresolved issue in understanding the physiology of light receptors. Several milliseconds are required before the absorption of light can be recorded as electrical activity in the receptor cell membrane. Certainly, the phototransduction event occurs during the transition from rhodopsin to metarhodopsin. We can not say much more about the detailed mechanisms of transducing light into bioelectrical signals.
A key requirement in the chemistry of vision is that metarhodopsin, or the bleached pigment of vertebrates, must be reconverted to rhodopsins. In the eyes of vertebrates, this regeneration is the product of a complex biochemical pathway. The pathway involves isomerization back to the 11-cis configuration and assembly with the opsins. Again, invertebrates differ from vertebrates on this aspect of photochemistry. Light is absorbed by rhodopsin and metarhodopsin in invertebrates. Absorption of light transforms metarhodopsin back to rhodopsin. The pigments exist in two stable conformations, and light causes them to switch back and fro from one state to the other. This regeneration is essential because conformational changes in rhodopsin, but not in metarhopsin, leads to phototransduction.
Experiments on insect behavior indicate that many insect species can distinguish colors. Color vision depends on the ability to discriminate between light of different wavelengths. Such discrimination is possible because compound eyes have photopigments with differing spectral properties. Many insects have two rhodopsins, one with maximum absorption in ultraviolet wavelengths and one with maximum absorption in green wavelengths. Some species have a third pigment that absorbs maximally in the blue region. A few Lepidoptera have four visual pigments.
Dorsal ocelli occur in larvae of hemimetabolous insects and in nearly all adults. Here is the structure of a dorsal ocellus. Although there are variations in structure, a typical ocellus has a single lens that is usually rather thickened. Most ocelli feature a large number, often hundreds, of retinula cells. Rhabdomeres of several cells combine to form a number of rhabdoms. Axons project from the retinula cells through the basement membrane and they end in a synaptic plexus behind the eye. Light causes a sustained depolarization of the retinula cells, however, the biological roles of ocelli remain unknown. It is generally agreed that ocelli allow only poor, if any, perception of form. In some orthopterans the ocelli are active in orientation to a light source.
The larvae of holometabolous insects have stemmata on the sides of the head capsule. Many larvae have a single stemma (singular of stemmata) on either side, but the number can be as many as six on a side. Here is a sketch of a section through a stemma. Each stemma has a cuticular lens and a crystalline cone distal to the sense cells. Stemmata generally do not produce clear images, but most caterpillars can discriminate some shapes and they can orientate themselves with respect to boundaries.