Vis 1--invertebrates-vision

Vision: InvertebratesE. Warrant, University of Lund, Lund, Sweden

ã 2010 Elsevier Ltd. All rights reserved.

Introduction

Invertebrates – animals without backbones – constitutethe vast majority of all known species of animal life onEarth. From a giant squid swimming in the dark colddepths of the sea to a tiny ant foraging in the leaf litterof a rainforest floor, invertebrates have conquered almostevery imaginable habitat. This extraordinary adaptabilityis in no small part due to their sense organs, and particu-larly their eyes, which help them to find food, locatemates, escape predators, and migrate to new habitats.Even though most invertebrates do not see as sharply aswe do, many see much better in dim light, can experiencemany more colors, can see polarized light, and can clearlydistinguish extremely rapid movements. Moreover, theydo all this with eyes and brains a fraction the size of ourown. It is this small size – and comparative simplicity – thathave allowed scientists to unravel many of vision’s mostfundamental principles, as equally applicable to a dragonflyas they are to us. Due to their small size, invertebrates oftenrely on comparatively simple circuits of cells to efficientlydecipher complex visual information.Manyof these circuits –and the computations they perform – seem ingenious to ahuman observer. Indeed, many have already been usedwith great success to create artificial visual systems forrobots, aircraft, and autonomous vehicles.

This short review explores the most important func-tional modalities of visual sensation in invertebrates andhow vision is used in daily life, from the capture of lightand its neural processing to the ways invertebrates usevision to orient, to navigate, to avoid predators, and to findfood and mates.

Invertebrate Visual Systems

Light is a highly physical stimulus, with an intensity, adirection, a color, and sometimes a plane of polarization.All these properties of light are detectable, to a greateror lesser extent, by the eyes of all animals. This detectionrelies on the conversion of light energy into an electricalsignal, a chemical process that involves rhodopsin, a light-absorbing protein found in the photoreceptor cells of theretina. These electrical signals are then processed by highervisual centers (in the optic lobes and brain) to allow inver-tebrates a visual impression of the world that is probablynot unlike that experienced by vertebrates.

Invertebrate Eye Designs

Ten distinct types of visual organs have been identified inthe animal kingdom (Figures 1 and 2). Vertebrates pos-sess only one of them, whereas invertebrates possess allten, from simple assemblies of photoreceptors that under-lie phototaxis to advanced compound and camera eyesthat support a sophisticated range of visual behaviors.Some invertebrates even possess several eyes of morethan one type.

Eye spots and pit eyes

The simplest type of visual organ – found in many smallerinvertebrates and larvae (notably of worms and insects) –is an aggregation of one or more photoreceptors on thebody surface, shielded on one side by a pigment cellcontaining screening pigment granules. Such ‘eye spots’are unable to detect the direction from which light isincident (i.e., they do not possess spatial vision) and aretherefore little more than simple detectors of light inten-sity. Since spatial vision, no matter how crude, is consid-ered to be the hallmark of a ‘true eye,’ eye spots are notconsidered true eyes. But for those invertebrates thatpossess them, eye spots are able to detect the presenceor absence of light and compare its intensity sequentiallyin different directions, thus allowing animals to avoid orto move toward it.

Pit eyes, formed by a number of photoreceptors lininga pigmented invagination – or ‘pit’ – in the epidermis, arecommon in turbellarian worms. Since the photoreceptorseach occupy different positions in the pigment-lined pit,they are each able to receive light from a different direc-tion in space. As a result, pit eyes are capable of crudespatial vision and are thus considered to be true eyes.

Pinhole eyes

One evolutionary route from a pit-eyed ancestor resultedin the eyes of the abalone Haliotis and the cephalopodmollusc Nautilus (Figure 2(a)). In these eyes, the pit hasdeveloped a spherical shape, with a small ‘pinhole’ pupilthat admits light to the underlying retina. However, unlikethe eyes of other cephalopods (squids and octopuses), theNautilus eye has no lens. Its pinhole eye works like apinhole camera: the small pupil creates a dim image onthe retina. However, compared to camera eyes of the samesize – like those found in other cephalopods – the pinhole

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Figure 1 Invertebrate eyes. Row 1, left to right: the camera(two larger eyes) and pigment cups eyes (two smaller eyes) that

equip a single rhopalium of the box jellyfish Tripedalia cystophora

(courtesy of D.E. Nilsson); three of the many compound eyes thatline themantle edge of the ark clamBarbatia cancellaria (courtesy

of D.E. Nilsson); two of the many concave-mirror eyes that line

the mantle edge of the scallop Pecten (courtesy of D.E. Nilsson);

the pinhole eye of the cephalopodmolluscNautilus. Row 2, left toright: the camera eyes of an unknown species of conch; the

camera eyes of an unknown species of cuttlefish; the apposition

compound eyes of a crab zoea (larva) (courtesy of D.E. Nilsson);

the apposition compound eyes of an unknown species of fiddlercrab. Row 3, left to right: the apposition compound eyes of an

unknown species of mantis shrimp; the apposition compound

eyes of the nocturnal bee Megalopta genalis; the refracting

superposition compound eyes of the mayfly Baetis (courtesy ofD.E. Nilsson); the apposition compound eyes of an unknown

species of katydid. Row 4, left to right: the apposition compound

eyes of an unknown species of robber fly; the appositioncompound eyes of an unknown species of dragonfly; the camera

eyes of an unknown species of jumping spider; the camera eyes

of the net-casting spider Dinopis subrufus.

512 Vision: Invertebrates

eye has rather poor sensitivity and resolution, whichprobably explains its rarity in nature. Nevertheless, thepinhole eye is a great improvement over a regular pit eye.

Concave-mirror eyes

Scallops, clams, and a few ostracods have another inter-esting eye type: the ‘concave-mirror eye’ (Figures 1 and 2(b)).In this design, light weakly focused by the cornea passesthrough the retina, and is then reflected from a hemi-spherical concave mirror (m in Figure 2(b)) lining theback of the eye. This reflected light is focused intothe retina, but since the retina has already absorbed partof the weakly focused light on the way in, the image contrastis rather poor. With its large pupil, its potential for lightcapture, on the other hand, is excellent. Indeed, one of

the most sensitive eyes in nature is of this design andfound in the deep-sea ostracod Gigantocypris. Many scallopsand clams have hundreds of concave-mirror eyes liningthe edges of both shells, and these are optimized as ‘burglaralarms’ for the rapid detection of shadows cast by predatorsattempting to enter the shell.

Compound eyes

By far, the most widespread eye design in the animalkingdom is the ‘compound eye’ design, possessed by insects(75% of the world’s animal species), most crustaceans,myriapods, and even some clams and polychaetes. Compoundeyes are composed of identical units called ‘ommatidia’(Figure 3(a)), each consisting of a lens element – the‘corneal lens’ and ‘crystalline cone’ – that focuses lightincident from a narrow region of space onto the ‘rhabdom,’ aphotoreceptive structure composed of membranousmicrovillithat house the rhodopsin molecules (Figure 3(b), 3(c), 3(e),and 3(f )). In all eyes, the rhodopsin molecules absorbphotons of light and trigger the chain of biochemicalevents that leads to the generation of an electrical signal,a process known as ‘phototransduction.’ In most compoundeyes, the rhabdom is built by fusing the photoreceptivesegments (or ‘rhabdomeres’) of several photoreceptorcells (or ‘retinula cells’: rc in Figure 3(a)). A compoundeye may contain as many as 30 000 ommatidia, as in largedragonflies, or as few as 1, as in some ants. Each ommatidiumis responsible for reading the average intensity, color, and(in some cases) plane of polarization within the smallregion of space that they each view. Two neighboringommatidia view two neighboring regions of space. Thus,each ommatidium supplies a ‘pixel’ of information to alarger image of pixels that the entire compound eye con-structs. Larger compound eyes with more ommatidia thushave the potential for greater spatial resolution. Compoundeyes come in two main forms: ‘apposition eyes’ and ‘super-position eyes.’

Apposition eyes (Figure 2(d)) are typical of (but notrestricted to) animals living in bright habitats. Eachommatidium in an apposition eye is isolated from itsneighbors by a sleeve of light-absorbing screening pig-ment, thus preventing light reaching the photoreceptorsfrom all but its own small corneal lens. This tiny lens –typically about 30 mm across – represents the pupil of theapposition eye. Such a tiny pupil only allows very littlelight to be captured. Not surprisingly, apposition eyes arebest suited to bright habitats. Day-active insects withapposition eyes include butterflies, bees, wasps, ants, dra-gonflies, and grasshoppers. Many crabs also have apposi-tion eyes.

There are two types of apposition eye known: thewidespread ‘focal’ type (Figure 2(d)) and the less com-mon ‘afocal’ type. In focal apposition eyes, the crystallinecone has a homogeneous refractive index, and light isfocused by the curved exterior surface of the corneal

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cz

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Figure 2 The main optical designs of invertebrate eyes. (a) The pinhole eye, possessed by the cephalopod mollusc Nautilus, lacks

a lens: the small pupil creates a dim and blurred image on the retina in much the same way that a pinhole camera does. (b) The

concave-mirror eye, possessed by many scallops, clams, and ostracods, relies on a hemispheric reflective mirror m (or ‘tapetum’)

that lines the back of the eye. Light first passes unfocused through the retina, and is then focused into the retina upon reflection.(c) The camera eye, possessed by all vertebrates, cephalopod and gastropod molluscs, and most arachnids. Light is focused by the

cornea (air only) and lens to form an image on the retina. (d) The focal apposition compound eye. Light reaches the photoreceptors

exclusively from the small corneal lens located directly above. This eye design is thus rather insensitive to light, and is typical of

day-active insects and many crustaceans. (e) The refracting superposition compound eye. A large number of corneal facets andbullet-shaped crystalline cones collect and focus light – across the clear zone of the eye (cz) – toward single rhabdoms in the retina.

Several hundred, or even thousands, of facets service a single rhabdom. Not surprisingly, many nocturnal and deep-sea animals – for

example, nocturnal insects and krill – have refracting superposition eyes, and benefit from the significant improvement in sensitivity.Diagrams courtesy of Dan-Eric Nilsson.

Vision: Invertebrates 513

facet lens onto the distal tip of the rhabdom. In flies, therhabdom is ‘open,’ meaning that its eight rhabdomeres areseparated rather than fused. In fly eyes – called ‘neuralsuperposition eyes’ – each point in space is imaged byseven rhabdomeres in each of seven neighboring omma-tidia. The axons of six of these rhabdomeres superimposeon a neural cartridge under the central ommatidium, inthe lamina, the first optic neuropil of the brain. Thus,compared with a conventional focal apposition eye, thisrewiring arrangement allows a sixfold increase in sensi-tivity for no loss in spatial resolution.

Afocal apposition eyes are only known in papilionoidbutterflies and differ from the focal type by having astrong gradient of refractive index in the extreme proxi-mal end (or ‘cone stalk’) of the crystalline cone. Rays arebrought to an intermediate focus at the entrance of thecone stalk and are then recollimated by the refractive-index gradient, which acts like a powerful second lens,

an adaptation that improves both spatial resolution andsensitivity.

Superposition eyes (Figure 2(e)) – of which there arethree different types – are typical for (but not restrictedto) animals living in dimmer habitats. In superpositioneyes the pigment sleeve is withdrawn, and a wide opticallytransparent area, the clear zone, is interposed between thelenses and the retina. This clear zone (cz in Figure 2(e)) –and specially modified crystalline cones – allow light froma narrow region of space to be collected by a large numberof ommatidia (comprising the superposition aperture) andfocused onto a single rhabdom. Unlike the crystallinecones of apposition eyes, those of superposition eyeshave evolved refractive index gradients or reflecting sur-faces, that allow as many as 2000 lenses to collect the lightfor a single photoreceptor (as in some nocturnal moths).This represents a massive improvement in sensitivitywhile still producing a reasonably sharp image.

c

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Figure 3 Compound eyes. (a) A schematic longitudinal section (and an inset of a transverse section) through a generalized

Hymenopteran ommatidium, showing the corneal lens (c), the crystalline cone (cc), the primary pigment cells (pc), the secondary

pigment cells (sc), the rhabdom (rh), the retinula cells (rc), the basal pigment cells (bp), and the basement membrane (bm). The left half of

the ommatidium shows screening pigment granules in the dark-adapted state, while the right half shows them in the light-adapted state.(b) A schematic transverse section through the open rhabdom of a higher fly, showing the seven distal retinula cells with their separated

rhabdomeres. (c) A schematic transverse section through the fused rhabdom of the Collembolan Orchesella, showing the eight retinula

cells with their apposed rhabdomeres. (d) A schematic longitudinal section through nine neighboring ommatidia in a focal apposition

eye. The interommatidial angle △f is the divergence angle between two adjacent ommatidia. co: corneal lens; c.c.: crystalline cone.(e, f) Transverse sections of rhabdoms in the dorsal rim area (DRA, (e)), and remainder of the eye (f), in the dung beetle Scarabaeus

zambesianus. In the dorsal rim, the rhabdomeres each have one of two possible perpendicular microvillar directions (white

perpendicular bars), whereas in the remainder of the eye the rhabdoms are flower-shaped and the rhabdomeres havemicrovilli orientedin one of several possible directions. Scale bar for both parts: 5 mm. Adapted from Warrant EJ, Kelber A, and Frederiksen R (2007)

Ommatidial adaptations for spatial, spectral and polarisation vision in arthropods. In: North G and Greenspan R (eds.) Invertebrate

Neurobiology, pp. 123–154. Woodbury, NY: Cold Spring Harbor Laboratory Press.


In the ‘refracting superposition eye’ (Figure 2(e)) –found in many beetles, moths, and some crustaceans suchas krill – there is a powerful gradient of refractive indexfrom the axis to the edge of each crystalline cone (which iscircular in cross-section). There is also a weak gradientpresent in the corneal lens. These gradients turn thecorneal and crystalline cone lenses into an afocal tele-scope: light rays focused by the corneal facet to an inter-mediate focus in the cone are then recollimated into aparallel bundle before exiting proximally toward the tar-get rhabdom. The superposition image is formed from theincidence of all such bundles on the retina. In the ‘reflect-ing superposition eye’ – found in aquatic and marineMacruran crustaceans – the crystalline cone is square incross-section, has a homogeneous refractive index, and iscoated in reflective pigment. Parallel light rays arefocused across the clear zone by reflection within thecrystalline cones, each of which acts as a mirror box.

The clear zone, however, is not optically homogeneous(as in the refracting design) but is instead crossed bytapering cone tracts that connect the crystalline cones tothe retina. These tracts have a shallow gradient of refrac-tive index along their length. For rays well away from theommatidial axis, reflection takes place in the crystallinecones, whereas for those nearer the axis, reflection occurswithin the cone tract. This unique arrangement allows fora superposition image on the retina. A third type – the‘parabolic superposition eye’ – is so far only known insome swimming and hermit crabs, and works using acombination of refraction and reflection.

Camera eyes

In camera-type simple eyes (Figure 2(c)), light is focusedonto the retina by a single optical system comprising alens and in some cases an overlying cornea. All vertebrateshave camera eyes, including ourselves. So do many


invertebrates, including many molluscs (including squidsand octopuses), some annelid worms and various arthro-pods including spiders, and many insect larvae and cope-pods. Despite their functional similarity, the camera eyesof vertebrates and invertebrates have very different devel-opmental origins. The vertebrate retina derives from thefrontal part of the brain, whereas the lens derives fromthe skin. In invertebrates, both the retina and the lens derivefrom the skin. In nonarthropod invertebrates – such ascephalopod and gastropod molluscs – the lens is inside theeye, beneath an external cornea. In arthropods, the lens isformed by a thickening of the corneal cuticle. The cameraeyes of deep-sea animals – particularly those of squids –can reach enormous size. The largest eyes known in theanimal kingdom are the camera eyes of the giant deep-seasquid (Architeuthis dux) that can reach a diameter of over30 cm! Camera eyes have better resolution and sensitivitythan any other eye type of comparable size.

Higher Visual Centers

Just as in vertebrates, which have a visual cortex and severalother brain areas for the higher processing of visual infor-mation, visual signals leaving the retina of invertebrates areprocessed sequentially, and along several parallel informa-tion pathways, in a number of higher visual centers locatedin the cephalic ganglion (the brain: Figure 4). In the well-studied insects, visual information is first processed by theretinotopically organized neuropils of the optic lobe: thelamina, medulla, lobula, and in some species (notably flies,butterflies, and beetles), a subdivision of the lobula knownas ‘the lobula plate.’ The lamina optimizes the signalscoming from the retina, and after receiving these signals,the medulla – which remains little understood – makeselementary analyses of the fundamental modalities of thevisual signal (space, time, color, and polarization). Thelobula, which receives retinotopic input from the medulla,plays an important role in the analysis of color, the discrim-ination of line orientation, and the detection of movingsmall-field targets. The lobula plate, which receives retino-topic input from both the medulla and the lobula, houseslarge wide-field motion-sensitive cells that are responsiblefor analyzing optic flow induced during locomotion. Theoptic lobes of other invertebrates are less well understood,but they contain similar neuropils. The optic lobes ofcephalopods are particularly well developed. In Octopusvulgaris, it has been estimated that the optic lobes alonecontain about 75% of the total number of neurons found inthe central nervous system.

An identical optic lobe connects each eye to the supra-and subesophageal ganglia, and permits tracts of visualinformation leaving the lobula and lobula plate to beprocessed further in the brain. The tract (or pathway)for polarization vision in a locust is shown in Figure 4(b).This visual information is integrated with information

derived from other senses, after which it is relayed bygiant descending fibers that carry highly specific sensoryinformation to the motor circuitry of the thoracic gangliathat control the wings and legs (and thus locomotion). Insome species, some visual information is also carried tothe abdominal ganglia. Several important areas of visualprocessing have now been identified in the insect brain.The mushroom bodies – paired structures located in bothhalves of the central brain region – are important inintegrating information from several sensory modalities,and for their role in learning and memory. The centralcomplex – a highly columnar neuropil in the center of thebrain – seems to be involved in the spatial organization oflocomotion (and possibly spatial organization in general).

The Modalities of Vision

Like vertebrates, invertebrates have the ability to detectand analyze the main properties of light, namely its inten-sity, its direction, its color, and its polarization. Theseproperties define the modalities of vision, and togetherthese provide the information necessary for invertebratesto interpret the visual world.

Sensitivity to Light

The greatest challenge for an eye that views a dimlyilluminated scene is to absorb sufficient photons of lightto reliably discriminate it. Certainly, ever since the pio-neering studies of Yeandle in the horseshoe crab Limulusin the late 1950s, we have known that photoreceptors canrespond to single photons with small but distinct electri-cal responses known as ‘bumps.’ Such responses are foundin both vertebrates and invertebrates, and seem to indi-cate that animal eyes are exquisitely sensitive to light.While this is certainly true, the visual response is alsoinherently noisy, due to the unpredictable and randomnature of photon arrivals as well as to sources of neuralnoise in the photoreceptors themselves. The effects ofthese sources of noise are minimized by capturing morelight: the greater the number of photons captured, thegreater the signal relative to the noise and the more reliableis visual discrimination. In regard to light capture, the eyesof invertebrates living in dim light are among the mostsensitive found in the animal kingdom. Indeed, the hugeeyes of giant deep-sea squids (with a diameter of up to30–40 cm) are likely to be the most sensitive eyes thathave ever existed.

Eyes of high absolute sensitivity to extended scenestend to have (relative to eye size) large pupils, short focallengths, and large photoreceptors. A frequently usedparameter to describe the light-gathering capacity of animaging system is its ‘F-number,’ the ratio of its focallength f to the diameter of its entrance pupil A (i.e., f/A).

ca

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lar

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500 μm

DRMe

ALo2Ca

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MO LALIL

LU

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Figure 4 Visual neuropils and pathways in the insect brain. (a) A frontal section of the entire bee brain. The retina r and various

neuropils of the optic lobe (lamina, la; medulla, me; and lobula, lo) are shown with neuropils of the brain: the mushroom body(comprising the calyx, ca; the peduncle, pe; and the b-lobe of the peduncle, b), and the antennal lobe al. Section courtesy of Wulfila

Gronenberg. Reproduced from Ehmer B and GronenburgW (2002) Segregation of visual input to the mushroom bodies in the honeybee

(Apis mellifera). The Journal of Comparative Neurology 451: 362–373. (b) A schematic drawing of the optic lobes and brain of the locust

Schistocerca gregaria, with the polarization pathways shown in dark gray. Me: medulla; DRMe: dorsal rim area in the medulla; ALo1–2:layers 1 and 2 of the anterior lobe of the lobula; OLo: outer lobe of the lobula; Ca and P: calyces and penduncles of the mushroom

bodies; CB: central body; LAL: lateral accessory lobe; PB: protocerebral bridge; OL and IL: outer and inner lobes of the upper unit of the

anterior optic tubercle; LU: lower unit of the anterior optic tubercle; LT and MO: lateral triangle and median olive of the lateral accessorylobe. Scale bar¼200mm. Diagram courtesy of Uwe Homberg. Reproduced from Homberg U, Hofer S, Pfeiffer K, and Gebhardt S (2003)

Organization and neural connections of the anterior optic tubercle in the brain of the locust, Schistocerca gregaria. The Journal of

Comparative Neurology 462: 415–430.


This is a useful and easy metric for comparing the light-gathering capacities of different eyes, with a lowerF-number indicating a brighter image. The huge cameraeyes of the nocturnal net-casting spider Dinopis subrufushave an F-number of < 0.6, a much lower value than inthe anterior-median (AM) eyes of the diurnal jumpingspider Phidippus johnsoni (F-number¼ 2.0). The dark-adapted human eye has an F-number of around 2.1.Thus, the eyes of Dinopis are clearly constructed for highsensitivity. Among compound eyes, the superposition eyes

of the nocturnal hawkmoth Deilephila elpenor have anF-number of around 0.7.

This high sensitivity to light has permitted manyinvertebrates to have remarkably good vision in dimlight. Nocturnal hawkmoths and bees can see the colorsof flowers and negotiate dimly illuminated obstacles dur-ing flight. Nocturnal bees can also home using learnedterrestrial landmarks, while moths and dung beetles cannavigate using constellations of stars or the dim pattern ofpolarized light formed around the moon.


Temporal Vision

The ability of animals to see things that move at differentspeeds is a reflection of their temporal vision, that is, how‘fast’ they are able to see. A human observer is unable todiscriminate a bullet fired from a rifle simply because itmoves too rapidly to be seen. The fastest objects that canbe seen by an animal depend on many factors, includingthe physiological properties of the photoreceptors and theambient light intensity. Moreover, the speed of visionvaries from species to species, with some species havingvery fast vision (like the fast-flying aerobatic diurnalinsects) and others having very slow vision (like sedentarynocturnal toads). This indicates that the speed of vision,like every other aspect of vision, is matched to the ecol-ogies of animals: those that move rapidly, or need to detectfast-moving objects (e.g., mates or prey in full flight), tendto have fast vision, while those that are sedentary orslowly moving tend to have slow vision.

The speed of vision varies widely between animalsbecause the dynamics of phototransduction, and the iden-tities and proportions of ion channels present in the photo-receptors (and the membrane kinetics they thus establish),differ substantially from species to species, and these dif-ferences have evolved in response to the various ecologicalneeds of animals. In fact, the cell membrane, via its electri-cal properties, acts as a ‘matched filter’ that is able to matchthe response properties of the eye to the lifestyle that theanimal possesses, such as its locomotion speed or its pre-ferred light intensity niche. In addition to these ecologicalinfluences, the filtering properties of the photoreceptormembrane and the transduction cascade are influencedby the state of adaptation and the temperature.

The fastest visual systems found in the animal king-dom are possessed by invertebrates, and the fastest arelikely to be those of calliphorid flies, which in a light-adapted state are able distinguish light stimuli that flickerat rates of up to around 300Hz (for humans, in compari-son, the limit is around 50Hz). These flies engage in high-speed pursuit and interception of mates, a behavior thatinvolves rapid and unpredictable changes in flight trajec-tory and which requires a rapid visual response. For allspecies, vision slows down as light levels fall (due toadaptive changes in the physiological properties of thephotoreceptors), and nocturnal and deep-sea species tendto have intrinsically slower vision than species active inbright sunshine. Slower vision in dim light significantlyimproves the reliability of vision because it filters outfaster visual details that tend to be inherently noisy anddegrade visual performance.

Spatial Vision

Most visual scenes viewed by animals on land or in theupper depths of the ocean are extended in nature, meaning

that light reaches the eye from many different directionsat once. The spatial details of such a scene – defined bylocal contrast differences between areas of light and dark –are imaged by the eye onto the underlying retina. Thefinest spatial details that can be seen by an eye are deter-mined by two main factors: (1) the quality of the opticalsystem that images the scene (i.e., the cornea and lens(es))and (2) the density and visual fields of the photoreceptorsthat receive the image. Both these factors are in turnsubservient to the amount of light that the eye can collectfrom the scene. As observed earlier, as light levels fall,visual reliability declines because of a decreasing signal-to-noise ratio. This is particularly true for the smallercontrast differences typical of finer spatial details, whichtend to be lost in the noise as intensity falls, a limitationthat is equally problematic for all eyes, irrespective of theiroptical quality or photoreceptor density. Thus, in general,spatial resolution declines with light intensity.

The optical quality of an imaging system depends onthe extent it suffers from various aberrations, particularlyspherical and chromatic aberrations. Moreover, in verysmall lenses such as those found in compound eyes, it alsodepends on diffraction of light waves entering the aper-ture. The effect of all these optical imperfections is to blurthe image formed on the retina, that is, to reduce itscontrast. Even though there are many invertebrate specieswhose eyes lack an imaging system altogether (e.g., thecephalopod Nautilus), those that do possess one very fre-quently have surprisingly crisp optics and good opticalimage resolution. For example, among the single lenses ofcamera eyes, those of tiny cubozoan jellyfish eyes areremarkably sharp, as are those of most gastropod andcephalopod molluscs and most arachnids. What is typicalfor most of these lenses is the presence of a powerfulradial (and often parabolic) gradient of refractive indexfrom the center to the edge of the lens, which tends toalmost exactly cancel spherical aberration. The lenses ofjumping spiders are an excellent example, which togetherwith a densely packed retina, allow jumping spider eyes tohave among the best spatial vision for their size in theanimal kingdom. In compound eyes, the small ommatidiallenses are typically only 20–100 times wider than thewavelength of visible light, a fact that invariably leads toimage degradation due to diffraction. In superpositioneyes, optical image quality is additionally limited by theaccuracy of superposition of light rays on the target rhab-dom, and in species where the rhabdoms are not shieldedby screening pigments or a tapetal sheath, by the spread ofmore steeply incident rays through neighboring rhab-doms (which blurs the image neurally).

Once the image is focused on the retina, the underly-ing matrix of photoreceptors must reconstruct it. Likethe pixels of a digital camera, the density of photorecep-tors in an eye sets the finest spatial detail that can bereconstructed: more densely packed photoreceptors can


reconstruct finer details. Ideally, the density of photore-ceptors should be matched to the finest spatial detail thatcan be passed by the optics, but often this is not the case.For example, in many gastropod mollusc camera eyes –such as those in the giant queen conch – the lens suppliesmuch sharper images than the retina can resolve, and inthe tiny camera eyes of cubozoan jellyfishes, the retina islocated distal to the focal plane of the lens, which meansthat the photoreceptors do not receive the sharply focusedimage that the lens supplies. It would seem that eventhough the eyes are capable of providing a sharp image,these animals do not require the spatial acuity their lensesafford. To exploit this acuity, a larger number of visualcells would undoubtedly be needed to process the addi-tional spatial information, bringing with it an energy costthat the animal might not be able to afford. Ultimately, theeye that evolves in a particular animal is the result ofnatural selection, whereby an optimal balance is foundbetween the costs of maintaining the eye and the ecologi-cal benefits it bestows upon the animal. This reasoning isequally true for the evolution of all sensory organs.

In other camera eyes – particularly those of spiders andcephalopods – the matrix of photoreceptors is usuallywell matched to the optical quality of the image focusedby the lens. As an example, we can consider the AM eyesof diurnal jumping spiders. In the jumping spider Portiafimbriata, the AM eyes are among the sharpest known ininvertebrates, with the potential to discriminate spatialdetails subtending as little as 2.4min of arc, a performanceapproaching that of our own eyes. Just as amazing is thatmuscles connected to the internal structure of the eyeallow the sharpest region of the retina to be scannedacross the visual field. This outstanding spatial resolutioncan be explained by both optical and neural adaptations.In Portia, the AM eyes are almost 1mm wide and almost2mm deep, with a retina divided into four distinct layersof receptors (I–IV) arranged proximally to distally. Distalto the receptors, the retina forms a pit aligned with theocular axis, the curved surface of which forms an interfacewith the lower refractive index internal vitreous of theeye. This interface acts as a diverging lens, increasing thefocal length of the system and magnifying the image byabout one-and-a-half times. This is analogous to thetelephoto system employed in falconiform birds of preyand almost doubles visual acuity. Spatial resolution isfurther improved by the presence of a gradient of refrac-tive index in the lens that corrects for spherical aberrationin the image. However, the lens also suffers from chro-matic aberration: light of shorter wavelength is focused toa position closer to the lens than light of longer wave-length, thus blurring the image. This has also been cor-rected in a most remarkable manner: receptors withmaximum sensitivity to the shorter wavelengths are placedmore distally in layer IV (found to be ultraviolet-sensitivecells), whereas those with maximum sensitivity to the

longer wavelengths are placed more proximally in layersI and II (found to be green-sensitive cells).

In compound eyes, spatial vision is highly dependenton the number of ommatidia present in each eye andon their packing density. The number of ommatidia ina single eye can vary from as few as one, as found in someprimitive ants, to as many as 30 000, as found in some speciesof large dragonfly. Since each ommatidium essentiallyaccounts for a single ‘pixel’ of the image, eyes with moreommatidia have the potential for higher spatial resolution.The density of ommatidia – specified by their interom-matidial angle △f (Figure 3(d)) – is also important. Theinterommatidial angle is a measure of how tightly packedthe ommatidia are within an eye or a specific eye region:the smaller this angle, the more tightly packed the omma-tidia and the more finely sampled the visual scene. Theinterommatidial angle (in radians) is also related to thecorneal facet diameter (D) and the local radius of curvatureof the eye (R) by △f¼D/R, showing that a larger localeye radius, or a smaller facet, produces a smaller inter-ommatidial angle and greater spatial resolution. A smallerfacet, however, collects less light and invariably suffersfrom the image-degrading effects of diffraction. A largereye radius means a larger eye, and this has limits too: animalswith compound eyes are generally rather small and thereis a limit to how big an eye they can carry. Apart fromanything else, the metabolic cost of having a larger eyeis quite enormous and sets a serious limit to how big aparticular eye can be. Instead, a wonderful compromisehas evolved that maintains eye size. Rather than enlargingthe whole eye, some animals have ‘enlarged’ a small part oftheir eye, and thus a small part of their visual field. A localincrease in eye radius may not only allow an increase inlens size (which reduces diffraction and improves lightcapture) but if eye radius is increased sufficiently, it mighteven allow a simultaneous reduction in△f (thus sharpeningspatial resolution). Unfortunately, any benefits gained inone eye region necessarily come at the cost of other regions.Despite this, it turns out that these specialized eye regions –known as ‘acute zones’ – are quite common, especially inapposition eyes. The presence of an acute zone impliesthat one region of the visual world is more important to ananimal than others. Exactly which region depends onseveral factors, many reflecting transient needs, such asthe need to find a mate or prey, or the need to detect theadvance of a predator. Others reflect more permanentneeds, not the least of which is the structure of the habitatswhere animals live.

As an example of the latter, consider the appositioneyes of animals adapted for life in a flat habitat: a desertant that runs across a salt pan or a fiddler crab that scans aflat intertidal beach for mates. All experience a brightworld dominated by the horizon, and all possess eyeshaving an elongated horizontal acute zone of enhancedresolution known as a ‘visual streak.’ Because most objects

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Figure 5 Sexual dimorphism in the apposition eyes of the

hoverfly Volucella pellucens. (a) Female and (b) male. The visualfields of the left eyes of the two sexes, and interommatidial

angles shown by isolines, are projected onto spheres, where

A: anterior; M: medial; L: lateral; V: ventral; and D: dorsal. Bothsexes possess acute zones directed frontally, an adaptation for

processing optic flow during forward flight. Compared to the

female, however, the male has a much larger acute zone directed

20�–30� dorsally (shaded regions, where △f < 1.1�). The male’sacute zone is used for fixating females during sexual pursuit.

Reproduced from Warrant EJ (2001) The design of compound


of interest for these animals occur either at or very nearthe horizon, visual streaks concentrate the majority of theeye’s sampling stations – and thereby visual capacity – atthe same locations. In fiddler crabs, the apposition eyesare vertically elongated, almost cylindrical, and located onlong stalks above the carapace. The shape of the eyemeans that the radius of curvature in the vertical eyeplane is much greater than in the horizontal eye plane,resulting in the vertical interommatidial angles (△fv)being much smaller (by up to a factor of 4) than thehorizontal ones. △fv steeply narrows toward the horizon(from both above and below) becoming smallest (0.3�) justalong the eye’s equator.

Acute zones have also evolved in the context of matedetection. Female brachyceran flies, like blowflies andhoverflies, have their eyes spaced well apart, but inmales the eyes are joined at the top of the head. Thisextra area of eye constitutes a frontal-dorsal acute zoneused by the males to keep sight of females during high-speed pursuits. Amusingly, these acute zones are oftenreferred to as ‘love spots.’ They are clearly seen in themale hoverfly Volucella pellucens, which has large love spotslocated frontally, 20� above the equator (Figure 5). Theinterommatidial angle here falls to just 0.7� . The size ofthe acute zone (the eye region where, say, △f< 1.1�)occupies 2230 deg2 of the visual field (shaded area inFigure 5). In females there is also an acute zone, directedexactly frontally and probably used for controlling flight.In females,△f only falls to 0.9�, and the area of the acutezone (△f< 1.1�) is a mere 23% as large as that of males(510 deg2: shaded area in Figure 5). The acute zones ofmale flies are not restricted to the eye surface. Below theeye, there is an intricate neural pathway that is specific tomales. First, the connections of photoreceptor axons tothe lamina are quite different in the acute zone comparedto both the female’s eye and the rest of the male’s eye.Higher up the brain, in the lobula, large male-specificvisual cells respond maximally to small dark objects thatmove across a bright background in the frontal-dorsalvisual field, an ideal physiology for detecting silhouettedfemales flying against the sky!

eyes and the illumination of natural habitats. In: Barth FG and

Schmid A (eds.) Ecology of Sensing, pp. 187–213. Berlin:Springer Verlag.

Color Vision

Many invertebrates experience a richly colored world,some much more richly than we ourselves experience it.The reason for this is that color is important in a variety ofbehavioral contexts including phototaxis and orientation,camouflage, object detection and recognition, the detec-tion of host plants for oviposition, the recognition offlowers and other food sources, the detection and inter-pretation of colored signals during sexual and social inter-actions, and the location of new shelters and recognizinglearned landmarks.

The sensation of color requires the presence of at leasttwo ‘spectral types’ of photoreceptor that view the sameregion of space, followed by a neural comparison of thesignals generated in these photoreceptors (usually via aneural opponency mechanism) at a subsequent (higher)level of the visual system. The spectral type of a photore-ceptor is defined by its spectral sensitivity, that is, itssensitivity to different wavelengths (or colors) of light.For example, a UV spectral type absorbs primarily inthe ultraviolet part of the spectrum, whereas a green


spectral type absorbs primarily in the green part of thespectrum. Exactly which band of wavelengths a receptorabsorbs, and how sensitive it is to individual wavelengthswithin that band, depends mainly on the nature of its‘visual pigment’ rhodopsin. Rhodopsin molecules –which absorb photons of light and trigger the generationof an electrical signal – are composed of two parts: a large‘opsin’ molecule, a protein consisting of a chain of around350 amino acids embedded in the photoreceptor mem-brane, and a small ‘chromophore,’ a molecule (typicallyretinal, hydroxyretinal or dehydroretinal) that is coupledto the opsin. The band of wavelengths absorbed by therhodopsin molecule depends on the exact sequence ofamino acids present in the opsin molecule and the iden-tity of the chromophore.

Even though the absorption spectrum of the residentrhodopsin molecule is the main determinant of the photo-receptor’s spectral sensitivity (and thus its spectral type),it is also affected by the concentration of rhodopsin, thepresence or absence of sensitizing or filtering pigments,the photoreceptor’s length and placement, and the absor-bance and reflectance of structures within the eye. Forinstance, if the rhabdom of a UV spectral type lies distal tothat of a green spectral type (i.e., if the rhabdoms are‘tiered’), the spectrum of light received by the green-sensitive photoreceptor will be filtered because of itspartial absorption by the overlying UV-sensitive photore-ceptor. This filtering will tend to narrow the spectralsensitivity of the underlying green-sensitive photorecep-tor and often shift its peak. Filtering resulting in spectralsensitivity changes also occurs if a colored filter (e.g., amembrane-bound vesicle of colored pigment) is located atthe distal entrance to the rhabdom, or between two tieredrhabdoms (a common arrangement in the apposition eyesof mantis shrimps), or if colored pigment granules arelocated within or around the photoreceptor cells (asfound in a variety of insect and crustacean species). Theeffect of all filtering mechanisms is to sharpen and tunethe spectral sensitivities of the resident spectral types ofphotoreceptors, to maximize and optimize the range and/or numbers of colors seen. Of course, the colors thatanimals need to see in order to survive and reproducevary dramatically from species to species according totheir ecology. In fact, the number of photoreceptor spec-tral types and the nature of any filtering that evolves in aneye are ultimately driven by the ecological needs of itsowner (Figure 6).

Most invertebrate rhabdoms contain at least two pho-toreceptor spectral types that share the same receptivefield, thus fulfilling the first precondition of color vision.However, in the deep sea, where the spectrum of down-welling daylight is almost monochromatically blue(around 480 nm), there is almost no need for color vision,and with few exceptions, deep-sea animals are mono-chromats, possessing only one photoreceptor spectral

type (e.g., deep-sea crustaceans and cephalopods). More-over, in the same eye, there can be regions of the retinawhere only one photoreceptor spectral type is present,whereas in other retinal areas, two or more types can bepresent. This allows monochromatic vision in one part ofthe visual field and the potential for color vision inanother part. A good example of this is the camera eyeof the firefly squidWatasenia scintillans (Figure 6(g)). Mostof the retina contains only one photoreceptor spectraltype with peak absorption at 484 nm (and allowing mono-chromatic vision), whereas a small region of the ventralretina (which views the dorsal visual field) contains twofurther photoreceptor spectral types (peaking at 470 and500 nm) and the possibility of dichromatic color vision(which may be useful for detecting and analyzing the twocolors of bioluminescence produced by the squid duringcourtship).

Many invertebrates have evolved two photoreceptorspectral types throughout the retina (e.g., many spiders,crustaceans, cockroaches, and ants), with the potentialfor dichromatic color vision. Trichromacy, based on threephotoreceptor spectral types with peak absorptions in theUV (�350 nm), blue (450–480nm), and green (500–550 nm),is also common and found in many clams (Figure 6(h)),spiders (Figure 6(e)), crustaceans (e.g., isopods), and insects(e.g., grasshoppers, bugs, bees, wasps, moths: Figure 6(a)).As a comparison, our own trichromacy is based on threephotoreceptor spectral types (blue, green, and yellow-red)with peak absorptions at around 420, 530, and 560 nm.Some invertebrates – notably some jumping spiders,water fleas, and butterflies – have extended their spectralrange from the UV to the red by adding a fourth photore-ceptor spectral type. Others have five photoreceptor spec-tral types (e.g., some dragonflies (Figure 6(b)) and flies),while yet others have six (some butterflies of the genusPapilio : Figure 6(c)). Remarkably, the eyes of mantisshrimps (Stomatopoda) have 12 photoreceptor spectraltypes (Figure 6(f )) – the largest number known in theanimal kingdom – each narrowly tuned as the result ofspectral filtering. These 12 types evenly sample the spec-trum from the deep UV to the far red but are only foundin a narrow band of ommatidia stretched across the centerof each eye (which is scanned across objects of interest).Whether or not these colorful reef-dwelling crustaceanshave 12-dimensional color vision remains unknown, buteven if an animal possesses a certain number of photore-ceptor spectral types, this does not necessarily imply thatall interact to create the maximal dimension of colorvision possible.

Polarization Vision

In addition to its particulate (photon) nature, light canalso be physically described as an electromagnetic wave,an electric field and a magnetic field that oscillate in

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Figure 6 Photoreceptor spectral sensitivities in selected invertebrates. UV: ultraviolet; V: violet; B: blue; G: green; R: red. (a) The

trichromatic visual system of the nocturnal hawkmoth Deilephila elpenor (based on opsin templates). (b) The spectral sensitivities of five

spectral receptor classes of photoreceptors in the dragonfly Hemicordulia tau (based on intracellular recordings). (c) Six spectralclasses of photoreceptors in the butterfly Papilio xuthus. Dashed line: receptor with broad sensitivity caused by expression of two

opsins within one cell. (d) Photoreceptors in the primary and secondary retinae of the annelid worm Torrea candida. (e) The

three spectral classes of photoreceptors found in the nocturnal spider Cupiennius salei (based on intracellular recordings). (f) The

multiple spectral classes of photoreceptors found in midband ommatidial rows of the stomatopod apposition eye (based on MSPand intracellular recordings). Dashed line: a receptor with broad sensitivity outside the midband rows. (g) The firefly squid Watasenia

scintillans. Solid lines: photoreceptors in the ventral part of the retina (the 550-nm receptor results from a 500-nm pigment filtered by a

distal 470-nm pigment). Dashed line: a photoreceptor in the larger dorsal retina. (h) Three spectral classes of photoreceptors in the giant

clam Tridacna maxima. Adapted with permission from Kelber A (2006) Invertebrate color vision. In: Warrant EJ and Nilsson D-E (eds.)Invertebrate Vision, pp. 83–126. Cambridge: Cambridge University Press.


unison at the same frequency, but are perpendicular toeach other. The polarization properties of the wave can bedescribed by its electric field component, and particularlyby the electric field’s phase relationships, which deter-mine whether the light wave is linearly (or plane) polar-ized or whether it is elliptically or circularly polarized.Remarkably, invertebrates are able to see both plane andcircularly polarized light, and to use it in several impor-tant behavioral contexts, notably navigation, orientation,prey detection, and for interactions between individuals ofthe same species. Except for a few controversial cases(notably among the birds and fishes), polarization visionis unknown in vertebrates.

The most common polarization vision in invertebratesinvolves the detection and analysis of linearly (plane)polarized light, since this is the most common form ofpolarized light found in Nature. The plane of polarizationis defined as the plane in which the electric field wave (ore-vector) oscillates. Most sources of light (both naturaland artificial) emit an immense number of such electro-magnetic waves, and commonly these waves are collectivelyplane unpolarized: the planes of polarization of individualwaves are randomly distributed in the light beam. How-ever, natural sources of light are quite often plane polar-ized, meaning that all individual light waves more or lessshare the same plane of polarization.

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Figure 7 Polarization vision in arthropods. (a–c) Schematic cross-sections through rhabdoms in the ommatidia of arthropod

compound eyes (not to scale). (a) Dorsal rim areas (DRAs) of various groups of insects. (b) Typical ommatidium in the retina of decapod

crustaceans; the two mutually perpendicular microvillar arrangements alternate in regular intervals along the rhabdom. (c) Ventral POL

area of the backswimmer. Color indicates the spectral type of receptors mediating polarization vision (pink, UV); receptors notcontributing to polarization vision are given in white; rhabdoms in gray indicate that the spectral range of polarization vision is unknown.

(d) Principle of polarization opponency. Left, two analyzer channels (represented by the two receptors 1 and 2) act antagonistically on a

POL neuron. Right, e-vector response functions of photoreceptors and POL neuron. (e, f) POL1 neuron in the optic lobe of the cricket,

Gryllus campestris. (e) Morphology reconstructed by neurobiotin staining. Input region (ipsilateral) receiving inputs from the POL area is



The dome of the sky is an excellent example of such asource. Light from the sun (or the moon) is scattered byair molecules in the Earth’s atmosphere to produce acircularly symmetric pattern of linearly polarized lightcentered on the disk of the sun (or moon). Each point inthe sky emits light polarized in only one direction, and thedirection of polarization shifts systematically from onepoint in the sky to the next (which produces the pattern).The degree of polarization is greatest along a circularlocus that is 90� from the sun or moon (and centered onit). If an invertebrate has the possibility to unravel the180� directional ambiguity inherent in the circularly sym-metric pattern (which they do, by analyzing spectral gra-dients in the sky), then they can use the pattern as agigantic compass cue for extracting directional informa-tion while navigating, either to simply keep a straight-linecourse (e.g., ball-rolling dung beetles) or to use as acomponent of an advanced path integration system usedfor homing (e.g., the well-studied desert ant Cataglyphisbicolor). Polarized skylight is even seen underwater, partic-ularly at shallower depths (down to about 200m). The factthat water has a higher refractive index than air meansthat the entire 180� dome of the sky is compressed to a 97�

cone of light underwater. This circular window of light –called ‘Snell’s window’ – allows the polarized skylightpattern to remain visible underwater, but turbid waterand the presence of waves can degrade it significantly.Nevertheless, some species (e.g., grass shrimps and juve-nile trout) can apparently use the underwater skylightpattern to maintain a straight swimming course. OutsideSnell’s window, the space light is strongly polarized in thehorizontal direction because of scattering from suspendedparticles. Near the shore, the degree of horizontal polari-zation is greater toward the open water, and some inverte-brates (notably the branchiopod Daphnia) use this fact toorient away from the shore (and danger). Some inverte-brates also use the aquatic backdrop of horizontally polar-ized light to detect transparent prey. Many transparentplanktonic organisms are highly birefringent, whichmeans that they are opaque (and highly visible) whenseen against a polarized background by a polarization-sensitive visual system (as found in squids). In terrestrialhabitats, horizontally plane-polarized light is formed byreflection from horizontal surfaces, notably water surfacesand shiny waxy leaves. Many flying insects – such as thebackswimmer Notonecta – search for new bodies of waterby looking for bright areas of horizontally polarized light

shown to the right. L, lamina; M, medulla; AM, accessory medulla; O

ipsilateral (right) and the contralateral part (left) of POL1 neurons whilrotated by 360�. In the ipsilateral recording, the baseline undulates as

the dark, demonstrating spontaneous spiking activity; the white trian

frequency modulates as a function of e-vector orientation. Ipsilateraldifferent e-vector tuning axes. Adapted with permission from Wehne

Nilsson D-E (eds.) Invertebrate Vision, pp. 83–126. Cambridge: Camb

in the ventral visual field. In combination with appropri-ate color cues, some papilionid butterflies also detectsuitable oviposition sites on the basis of horizontallypolarized light reflected from the leaves of their hostplants. Finally, some heliconid butterflies, squids, andmantis shrimps use polarized light signals reflected fromtheir integuments in intraspecific communication.

The reason why most invertebrates can see plane-polarized light is due to the structure of their rhabdoms,which are formed from tube-like membranous microvilli.These microvilli – which are all highly aligned – eachconstrain the orientation of their resident rhodopsinmolecules, so that they are aligned along the microvillaraxis. Since each rhodopsin molecule is a linear absorptiondipole, and the dipole orientation is constrained by themicrovillus (and is identical to that for every other rho-dopsin molecule), the rhabdom as a whole becomes highlypolarization sensitive. To actively remove polarizationsensitivity requires that the microvilli become disoriented(e.g., by the rhabdom being twisted along its length, asfound in certain eye regions of many insects). In contrast,the photoreceptors of vertebrates have a structure unsuit-able to the detection of polarized light. The flat disk-likemembranes of their photoreceptor outer segments allowrhodopsin molecules to diffuse in any random direction:the crystalline alignment of rhodopsin molecules neces-sary to detect polarized light is thus impossible.

Just as with color vision, the analysis of plane-polarizedlight requires two ‘polarization classes’ of photoreceptorthat view the same region of space, followed by a neuralcomparison of the signals generated in each (usually via aneural opponency mechanism) at a subsequent (higher)level of the visual system. Our understanding of thisprocess is almost entirely due to decades of research indesert ants (Catalglyphis bicolor), crickets (Gryllus campes-tris), and locusts (Schistocerca gregaria), all of which have aspecialized ‘dorsal rim area’ (or DRA), a narrow strip ofommatidia along the dorsal-most margin of the compoundeye. The ommatidia of the DRA house the polarization-sensitive photoreceptors, all of which have a dorsal field ofview. Outside the DRA, the rhabdoms are deliberatelytwisted to eliminate their polarization sensitivity. The twopolarization classes of photoreceptor found in the DRAhave microvilli oriented in only one of two possible per-pendicular directions (Figure 7(a)–7(c)). Within a rhabdomof (say) eight rhabdomeres, at least one rhabdomere hasmicrovilli oriented in one direction, while all others have

T, optic tract; S, cell soma. (f) Intracellular recordings from the

e the e-vector orientation of a strongly polarized stimulus wasa result of EPSP summation. The contralateral recording starts in

gle marks the onset of the stimulus. In both recordings, the spike

and contralateral recordings are from two POL1 neurons withr R and Labhart T (2006) Polarisation vision. In: Warrant EJ and

ridge University Press.


microvilli oriented in the perpendicular direction (thusforming two orthogonal analysis components for any direc-tion of plane-polarized light). The signals generated in thesetwo classes form two analyzer channels, each of which canact antagonistically (Figure 7(d)) on a polarization-sensitiveinterneuron (known as ‘a POL neuron’) that arises in themedulla (Figure 7(d)–7(f)). A well-studied POL neuronis POL1 (found in crickets), a cell that sends its outputs toboth the central brain and to the contralateral medulla inthe optic lobe of the other eye (Figure 7(e)). In crickets,three types of POL1 neurons have been found, eachhighly sensitive and each having a very large receptivefield (>60� across). The three types differ only in theirpreferred orientation of polarized light relative to the longaxis of the head – 10�, 60�, and 130� – directions thatroughly correspond to the combined directional prefer-ence of the pool of 200 DRA ommatidia that feed eachreceptive field of each of the three POL1 neurons (thereare approximately 600 ommatidia in the cricket DRA).These three classes of POL1 neurons are believed toindirectly feed an array of ‘compass neurons’ (probablylocated in the central brain), each of which represents acertain body orientation relative to the symmetry plane ofthe celestial polarization pattern. The pattern of responsesin the array of compass neurons, due to the inputs of thethree-axis system of POL1 neurons (10�, 60�, and 130�), isthen thought to code body orientation exactly. Evidencefor the existence of compass-like neurons is beginning toemerge in the central complex of the locust brain (seeFigure 4(b) for the visual pathways of the brain involvedin polarization vision).

While much less common than linearly polarized light,circularly polarized light can be produced by reflectionfrom certain natural surfaces, notably the cuticle of somearthropods. Many scarab beetles – particularly those thatare brilliantly iridescent – have exactly the type of cuticlenecessary. To become circularly polarized, the two per-pendicular components of the electric field wave of lightmust become 90� out of phase (i.e., by a quarter of awavelength). Certain materials – such as the cuticle ofsome beetles – induce this phase shift upon reflection.Even though circularly polarized cuticular reflectionshave been known for some time, their visual and behavioralfunctions (if any) were unknown. Very recently, however,certain species of mantis shrimps (stomatopods) have beenshown to not only reflect circularly polarized light, butalso to visually detect it and to react to it behaviorally.

The physiological basis for this ability lies within therhabdoms of a specialized band of ommatidia in the com-pound eye: the eighth rhabdomere, which sits on top of theother seven, has a thickness and microvillar orientation thatremoves the 90� phase difference between the two perpen-dicular components of the electric field of the incomingcircularly polarized light (i.e., it acts as a ‘quarter-waveretarder’), thereby converting it to linearly polarized light.This linearly polarized light is then detected and analyzedin the conventional manner by the seven underlying rhab-domeres, but in this case, as a code for the presence ofcircularly polarized light.

Conclusions

The invertebrates – constituting nearly all species ofanimal life on Earth – have conquered almost all knownhabitats. Not surprisingly, their sensory organs, and par-ticularly their eyes, have adapted to a remarkable range ofsensory environments and sensory stimuli. Among theinvertebrates are found all known optical designs ofeyes, endowing these animals with visual abilities that inmany cases rival, and occasionally even exceed, those ofhumans. Compared with our own visual impression, manyspecies see much better in dim light, experience a fasterand more colorful world, and are able to distinguish thesubtleties of polarized light, a visual modality foreverbeyond our perceptual limits.

See also: Crabs and Their Visual World; Insect Naviga-

tion; Nervous System: Evolution in Relation to Behavior;

Vision: Vertebrates; Visual Signals.

Further Reading

Chiou TH, Kleinlogel S, Cronin T, et al. (2008) Circular polarization visionin a stomatopod crustacean. Current Biology 18: 429–434.

Krapp HG and Wiklein M (2008) Central processing of visual informationin insects. In: Albright T and Masland RH (eds.) The Senses:A Comprehensive Reference, vol. 1, Basbaum AI, Kaneko A,Shepherd GM, andWestheimer G (series eds.) Vision I, pp. 131–203.Oxford: Academic Press.

Land MF and Nilsson DE (2002) Animal Eyes. Oxford: Oxford UniversityPress.

Warrant EJ and Nilsson DE (2006) Invertebrate Vision. Cambridge:Cambridge University Press.

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