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FIGURE 8 Three mechanisms of dark adaptation in apposition eyes of insects (see text). (Reproduced, with permission, from Land and Nilsson, 2002.)

this is to absorb the wave-guided light that travels just outside the rhabdom. This is replaced with light within the rhabdom, and this is absorbed in turn, so that light is progressively "bled" out of the rhabdom. This mechanism is particularly important in higher Diptera (house flies, etc.) and in butterflies, and it can work in a matter of seconds. (C) The rhabdom dimensions may themselves change, usually over a period of hours. This mechanism may involve the resynthesis of photoreceptive membrane in the dark and its sequestration in the light. In addition to these changes there are electrical and enzymatic changes in the receptors themselves that alter the gain of transduction and increase response time in the dark.

Ecological Variations in Apposition Design

As we have seen, the optical design of apposition eyes means that there is no spare room on the head surface, and what there is needs to be used as efficiently as possible. A survey of the apposition eyes of insects and crustaceans leads to the conclusion that there are three main patterns of acuity distribution that one can identify fairly easily. These are identified in Fig. 9, which illustrates the ecological reasons for these patterns (Figs. 9A-9C) and examples of the distributions themselves (Figs. 9D—9F). Figure 9D shows the pattern related to the motion across the eye encountered in forward locomotion, especially flight. Figure 9E has an "acute zone" associated with predation or sex, these zones sometimes developing into separate components of a double eye. In Fig. 9F the narrow horizontal strip of high resolution is associated with environments such as water surfaces and sand flats, where almost all important activity takes place around the horizon.

THE FORWARD FLIGHT PATTERN When an animal is moving through the world, the objects in the world appear to move backward across the eye. Objects to the sides move faster than those in front, and there is a point in the direction of the animal's travel (the "focus of expansion") where there is no image motion. Objects farther away move more slowly

FIGURE 9 (A—C) Three situations that lead to asymmetries in the distribution of resolution in apposition compound eyes. (A) Flight through vegetation. (B) Chasing mates or prey. (C) Flight close to flat surfaces. (D—F) Plots of the density of ommatidial axes around the eyes of three insects, corresponding to the three situations in A—C. (D) Locust (forward flight pattern). (E) Drone bee (chasing females). (F) Water strider (hunting on water surface). Contours show the numbers of ommatidial axes per square degree of space around the animal. (Reproduced, with permission, from Land and Nilsson, 2002.)

FIGURE 9 (A—C) Three situations that lead to asymmetries in the distribution of resolution in apposition compound eyes. (A) Flight through vegetation. (B) Chasing mates or prey. (C) Flight close to flat surfaces. (D—F) Plots of the density of ommatidial axes around the eyes of three insects, corresponding to the three situations in A—C. (D) Locust (forward flight pattern). (E) Drone bee (chasing females). (F) Water strider (hunting on water surface). Contours show the numbers of ommatidial axes per square degree of space around the animal. (Reproduced, with permission, from Land and Nilsson, 2002.)

than near objects. Clearly, near objects to the side are likely to move so fast across the retina as to cause blurring, and if this is the case it would be economical to use fewer receptors there, as high resolution is not usable. For a bee or butterfly flying half a meter from foliage, the blur streak can be estimated to be about 2.3° long. It follows that there is little point in having lateral-pointing receptors closer together than 2 or 3°, however good the resolution at the front of the eye may be. This seems to be borne out in practice. In the butterfly Heteronympha merope, for example, the horizontal interommatidial angle decreases from 1.4° in front to 2.6° at the side. Bees, butterflies, and acridid grasshoppers are flying insects, and their eyes all show decreasing horizontal interommatidial angles from front to rear, consistent with these ideas. Nonflying insects, e.g., many tettigonid grasshoppers, have more or less spherical eyes, without this gradient. In all the flying groups there is another, separate gradient of vertical interommatidial angles; they are smallest around the eye's equator and increase toward both dorsal and ventral poles. This results in a band around the equator with

FIGURE 10 Eyes in which facet size reflects local resolution. Paradoxically, large facets produce high resolution. (A) Syritta (syrphid male), (B) Dilophus (bibionid male), (C) Aeschna (dragonfly), (D) Hilara (empid fly). See text. (Reproduced, with permission, from Land and Nilsson, 2002.)

enhanced vertical acuity. The most likely reason for this vertical gradient is that the region around the eye's equator contains the highest density of information important to the animal, especially if it is an insect that feeds on flowers.

The combined effects of these two gradients on the overall density of ommatidial axes are shown for a locust in Fig. 9D, in which the contours represent the number of ommatidial axes per square degree on the sphere surrounding the animal. Worker bees and female blow flies (Calliphora) show a similar pattern, although in male flies and drone honey bees, this pattern is distorted to give a more pronounced acute zone concerned with mate capture (also Fig. 9E).

acute zones concerned with prey capture and mating Many insects have a forward- or upward-pointing region of high acuity, related either to the capture of other insect prey or to the pursuit in flight of females by males (Fig. 9E). When both sexes have the specialization (mantids, dragonflies, robber flies), predation is the reason, but more commonly it is only the male that has the acute zone (simuliid black flies, hover flies, mayflies, drone bees), indicating a role in sexual pursuit. The acute zones vary considerably. In male house flies and blow flies, they may involve little more than a local increase in the acuity of the "forward flight" acute zone common to both sexes (see earlier). However, in other insects the acute zone may be in a separate eye, as is the case with the dorsal eyes of male bibionid flies (Fig.10B). In these more extreme double eyes, the upward-pointing part is often specialized for detecting other small animals against the sky.

Good examples of forward-directed acute zones are found in the praying mantids, predators in which both sexes ambush prey. The eyes have large, binocularly overlapping acute zones that are used to center potential prey before it is struck with the spiked forelegs. Mantids provide the only known example in insects in which prey distance is determined by binocular triangulation. The interommatidial angle (A^) in Tenodera australasiae varies from 0.6° in the acute zone center to 2.5° laterally. Facet diameters decrease from 50 |lm in the acute zone to 35 |lm peripherally, but this is less of a decrease than would be expected from diffraction considerations alone.

In many male dipterans an acute zone associated with sexual pursuit is typically situated 20 to 30° above the flight direction. In Calliphora flies it is characterized by a low value for A^ of 1.07° compared with 1.28° in the female. In house flies and probably in other flies there are also anatomical differences at the receptor level that suggest that this region (it has been called the "love spot") is specifically adapted for improved sensitivity. This is no doubt caused by the very fast response times required for high-speed chasing. Male flies also have a number of "male-specific" interneurons in the optic ganglia, which are undoubtedly involved in the organization of pursuit behavior.

In the small hover fly Syritta pipiens the sex difference is particularly striking. In the male's acute zone, A^ is about 0.6°, nearly three times smaller than elsewhere in the eye or anywhere in the female eye (Fig. 10A). Drone bees have a similar anterodorsal acute zone, where the density of ommatidial axes is three to four times greater than anywhere in the female eye (Fig. 9E). They use this region when they chase the queen and can be induced to chase a dummy queen on a string subtending only 0.32°, much smaller than the ommatidial acceptance angle of 1.2°. This implies that the trigger for pursuit is a brief decrease of about 6% in the intensity received by single rhabdoms.

Most of the animals just discussed have to detect their prey or mates against a background of foliage, a far from easy task. However, many insects have simplified the problem by using the sky as a background, against which any non-luminous object becomes a dark spot. Thus, one finds not only upward-pointing acute zones but also double eyes with one component directed skyward (Figs. 10B and 10C). For example, dragonflies hunt other insects on the wing and have acute zones with a variety of configurations. Many in fact have two acute zones, one forward pointing, and presumably concerned with forward flight as discussed above, and another directed dorsally and used to detect prey. The migratory, fast-flying aeschnids have the largest eyes and most impressive acute zones. Exactly 28,672 ommatidia have been counted in one eye of Anax junius, which has the smallest interommatidial angles of any insect (0.24° in the dorsal acute zone) and facets of corresponding size (62 |lm). The dorsal acute zone takes the form of a narrow band of high resolution extending across the upper eye along a great circle, 50 to 60° up from the forward direction. The axis density (five per square degree) is twice that in the forward acute zone and five times higher than in a male blow fly. The dorsal acute zone is easily visible as a wedge of enlarged facets (Fig. 10C). Presumably the great high-acuity stripe in Anax is used to trawl through the air, picking out insects against the sky much as the scan line on a radar set picks up aircraft.

Simuliid flies have divided eyes and use the upper part to detect potential mates against the sky. They can do this at a distance of 0.5 m, when a female subtends an angle of only 0.2°. As in drone bees, this is a small fraction of an acceptance angle. The eyes of male bibionid flies are similarly divided (Fig. 10B), with larger facets and smaller interommatidial angles in the dorsal eye (1.6° compared with 3.7°, in Bibio marci). The upper eyes are used exclusively for the detection of females; movement of stripes around the lower eye evokes a strong optomotor turning response (the almost universal visual behavior used by insects to prevent involuntary rotation) but the dorsal eye is quite unresponsive to this kind of stimulus.

horizontal acute zones As we have seen, many flying insects have a zone of increased vertical acuity around the horizon, no doubt reflecting the visual importance of this part of the surroundings. The visual field of the locust in Fig. 9A shows this clearly. There are environments where this region is even more important.

Insects that fly over water have a similarly narrow equatorial field of interest. Empid flies hunt close to the surfaces of ponds, again looking for stranded insects, and they have a horizontal acute zone that can be recognized by a linear region of enlarged facets around the eye (Fig.10D). In Rhamphomyia tephraea, vertical interommatidial angles are only 0.5° in this 15°-high region, rising to 2° above and below it.

Water surfaces themselves provide a similarly constrained field of view, and water striders (Gerris) that hunt prey stranded in the surface film have a narrow acute band imaging this region, as shown in Fig. 9F. This has a height of only about 10°, centered on the horizon, and within this the vertical interommatidial angle in the frontal region is only 0.55°, which is close to the diffraction limit and impressive in an eye with only 920 ommatidia.

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