1. Vision: Invertebrates
E. Warrant, University of Lund, Lund, Sweden
ã 2010 Elsevier Ltd. All rights reserved.
Introduction
Invertebrates – animals without backbones – constitute
the vast majority of all known species of animal life on
Earth. From a giant squid swimming in the dark cold
depths of the sea to a tiny ant foraging in the leaf litter
of a rainforest floor, invertebrates have conquered almost
every imaginable habitat. This extraordinary adaptability
is in no small part due to their sense organs, and particu-
larly their eyes, which help them to find food, locate
mates, escape predators, and migrate to new habitats.
Even though most invertebrates do not see as sharply as
we do, many see much better in dim light, can experience
many more colors, can see polarized light, and can clearly
distinguish extremely rapid movements. Moreover, they
do all this with eyes and brains a fraction the size of our
own. It is this small size – and comparative simplicity – that
have allowed scientists to unravel many of vision’s most
fundamental principles, as equally applicable to a dragonfly
as they are to us. Due to their small size, invertebrates often
rely on comparatively simple circuits of cells to efficiently
decipher complex visual information. Manyof these circuits –
and the computations they perform – seem ingenious to a
human observer. Indeed, many have already been used
with great success to create artificial visual systems for
robots, aircraft, and autonomous vehicles.
This short review explores the most important func-
tional modalities of visual sensation in invertebrates and
how vision is used in daily life, from the capture of light
and its neural processing to the ways invertebrates use
vision to orient, to navigate, to avoid predators, and to find
food and mates.
Invertebrate Visual Systems
Light is a highly physical stimulus, with an intensity, a
direction, a color, and sometimes a plane of polarization.
All these properties of light are detectable, to a greater
or lesser extent, by the eyes of all animals. This detection
relies on the conversion of light energy into an electrical
signal, a chemical process that involves rhodopsin, a light-
absorbing protein found in the photoreceptor cells of the
retina. These electrical signals are then processed by higher
visual centers (in the optic lobes and brain) to allow inver-
tebrates a visual impression of the world that is probably
not unlike that experienced by vertebrates.
Invertebrate Eye Designs
Ten distinct types of visual organs have been identified in
the animal kingdom (Figures 1 and 2). Vertebrates pos-
sess only one of them, whereas invertebrates possess all
ten, from simple assemblies of photoreceptors that under-
lie phototaxis to advanced compound and camera eyes
that support a sophisticated range of visual behaviors.
Some invertebrates even possess several eyes of more
than one type.
Eye spots and pit eyes
The simplest type of visual organ – found in many smaller
invertebrates and larvae (notably of worms and insects) –
is an aggregation of one or more photoreceptors on the
body surface, shielded on one side by a pigment cell
containing screening pigment granules. Such ‘eye spots’
are unable to detect the direction from which light is
incident (i.e., they do not possess spatial vision) and are
therefore 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 not
considered true eyes. But for those invertebrates that
possess them, eye spots are able to detect the presence
or absence of light and compare its intensity sequentially
in different directions, thus allowing animals to avoid or
to move toward it.
Pit eyes, formed by a number of photoreceptors lining
a pigmented invagination – or ‘pit’ – in the epidermis, are
common in turbellarian worms. Since the photoreceptors
each 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 crude
spatial vision and are thus considered to be true eyes.
Pinhole eyes
One evolutionary route from a pit-eyed ancestor resulted
in the eyes of the abalone Haliotis and the cephalopod
mollusc Nautilus (Figure 2(a)). In these eyes, the pit has
developed a spherical shape, with a small ‘pinhole’ pupil
that admits light to the underlying retina. However, unlike
the eyes of other cephalopods (squids and octopuses), the
Nautilus eye has no lens. Its pinhole eye works like a
pinhole camera: the small pupil creates a dim image on
the retina. However, compared to camera eyes of the same
size – like those found in other cephalopods – the pinhole
511

2. eye has rather poor sensitivity and resolution, which
probably explains its rarity in nature. Nevertheless, the
pinhole 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 passes
through the retina, and is then reflected from a hemi-
spherical concave mirror (m in Figure 2(b)) lining the
back of the eye. This reflected light is focused into
the retina, but since the retina has already absorbed part
of the weakly focused light on the way in, the image contrast
is rather poor. With its large pupil, its potential for light
capture, on the other hand, is excellent. Indeed, one of
the most sensitive eyes in nature is of this design and
found in the deep-sea ostracod Gigantocypris. Many scallops
and clams have hundreds of concave-mirror eyes lining
the edges of both shells, and these are optimized as ‘burglar
alarms’ for the rapid detection of shadows cast by predators
attempting to enter the shell.
Compound eyes
By far, the most widespread eye design in the animal
kingdom is the ‘compound eye’ design, possessed by insects
(75% of the world’s animal species), most crustaceans,
myriapods, and even some clams and polychaetes. Compound
eyes are composed of identical units called ‘ommatidia’
(Figure 3(a)), each consisting of a lens element – the
‘corneal lens’ and ‘crystalline cone’ – that focuses light
incident from a narrow region of space onto the ‘rhabdom,’ a
photoreceptive structure composed of membranous microvilli
that house the rhodopsin molecules (Figure 3(b), 3(c), 3(e),
and 3(f )). In all eyes, the rhodopsin molecules absorb
photons of light and trigger the chain of biochemical
events that leads to the generation of an electrical signal,
a process known as ‘phototransduction.’ In most compound
eyes, the rhabdom is built by fusing the photoreceptive
segments (or ‘rhabdomeres’) of several photoreceptor
cells (or ‘retinula cells’: rc in Figure 3(a)). A compound
eye may contain as many as 30 000 ommatidia, as in large
dragonflies, or as fewas 1, as in some ants. Each ommatidium
is responsible for reading the average intensity, color, and
(in some cases) plane of polarization within the small
region of space that they each view. Two neighboring
ommatidia view two neighboring regions of space. Thus,
each ommatidium supplies a ‘pixel’ of information to a
larger image of pixels that the entire compound eye con-
structs. Larger compound eyes with more ommatidia thus
have the potential for greater spatial resolution. Compound
eyes come in two main forms: ‘apposition eyes’ and ‘super-
position eyes.’
Apposition eyes (Figure 2(d)) are typical of (but not
restricted to) animals living in bright habitats. Each
ommatidium in an apposition eye is isolated from its
neighbors by a sleeve of light-absorbing screening pig-
ment, thus preventing light reaching the photoreceptors
from all but its own small corneal lens. This tiny lens –
typically about 30 mm across – represents the pupil of the
apposition eye. Such a tiny pupil only allows very little
light to be captured. Not surprisingly, apposition eyes are
best suited to bright habitats. Day-active insects with
apposition 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: the
widespread ‘focal’ type (Figure 2(d)) and the less com-
mon ‘afocal’ type. In focal apposition eyes, the crystalline
cone has a homogeneous refractive index, and light is
focused by the curved exterior surface of the corneal
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 that
line the mantle edge of the ark clam Barbatia 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 cephalopod mollusc Nautilus. Row 2, left to
right: 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 fiddler
crab. 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 of
D.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 apposition
compound 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

3. facet lens onto the distal tip of the rhabdom. In flies, the
rhabdom is ‘open,’ meaning that its eight rhabdomeres are
separated rather than fused. In fly eyes – called ‘neural
superposition eyes’ – each point in space is imaged by
seven rhabdomeres in each of seven neighboring omma-
tidia. The axons of six of these rhabdomeres superimpose
on a neural cartridge under the central ommatidium, in
the lamina, the first optic neuropil of the brain. Thus,
compared with a conventional focal apposition eye, this
rewiring arrangement allows a sixfold increase in sensi-
tivity for no loss in spatial resolution.
Afocal apposition eyes are only known in papilionoid
butterflies and differ from the focal type by having a
strong gradient of refractive index in the extreme proxi-
mal end (or ‘cone stalk’) of the crystalline cone. Rays are
brought to an intermediate focus at the entrance of the
cone stalk and are then recollimated by the refractive-
index gradient, which acts like a powerful second lens,
an adaptation that improves both spatial resolution and
sensitivity.
Superposition eyes (Figure 2(e)) – of which there are
three different types – are typical for (but not restricted
to) animals living in dimmer habitats. In superposition
eyes the pigment sleeve is withdrawn, and a wide optically
transparent area, the clear zone, is interposed between the
lenses and the retina. This clear zone (cz in Figure 2(e)) –
and specially modified crystalline cones – allow light from
a narrow region of space to be collected by a large number
of ommatidia (comprising the superposition aperture) and
focused onto a single rhabdom. Unlike the crystalline
cones of apposition eyes, those of superposition eyes
have evolved refractive index gradients or reflecting sur-
faces, that allow as many as 2000 lenses to collect the light
for a single photoreceptor (as in some nocturnal moths).
This represents a massive improvement in sensitivity
while still producing a reasonably sharp image.
(a) (b)
(d) (e)
(c)
cz
m
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 and
bullet-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

4. In the ‘refracting superposition eye’ (Figure 2(e)) –
found in many beetles, moths, and some crustaceans such
as krill – there is a powerful gradient of refractive index
from the axis to the edge of each crystalline cone (which is
circular in cross-section). There is also a weak gradient
present in the corneal lens. These gradients turn the
corneal 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 a
parallel bundle before exiting proximally toward the tar-
get rhabdom. The superposition image is formed from the
incidence of all such bundles on the retina. In the ‘reflect-
ing superposition eye’ – found in aquatic and marine
Macruran crustaceans – the crystalline cone is square in
cross-section, has a homogeneous refractive index, and is
coated in reflective pigment. Parallel light rays are
focused across the clear zone by reflection within the
crystalline 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 by
tapering cone tracts that connect the crystalline cones to
the retina. These tracts have a shallow gradient of refrac-
tive index along their length. For rays well away from the
ommatidial axis, reflection takes place in the crystalline
cones, whereas for those nearer the axis, reflection occurs
within the cone tract. This unique arrangement allows for
a superposition image on the retina. A third type – the
‘parabolic superposition eye’ – is so far only known in
some swimming and hermit crabs, and works using a
combination of refraction and reflection.
Camera eyes
In camera-type simple eyes (Figure 2(c)), light is focused
onto the retina by a single optical system comprising a
lens and in some cases an overlying cornea. All vertebrates
have camera eyes, including ourselves. So do many
c
cc
pc
sc
rh
rc
bp
bm
(a) Δφ(d)
(b)
(c)
1
2
3
45
c.c.
co.
6
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8
7
1
2
34
5
6
(f)
(e)
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 have microvilli oriented
in 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.
514 Vision: Invertebrates

5. invertebrates, including many molluscs (including squids
and octopuses), some annelid worms and various arthro-
pods including spiders, and many insect larvae and cope-
pods. Despite their functional similarity, the camera eyes
of vertebrates and invertebrates have very different devel-
opmental origins. The vertebrate retina derives from the
frontal part of the brain, whereas the lens derives from
the skin. In invertebrates, both the retina and the lens derive
from the skin. In nonarthropod invertebrates – such as
cephalopod and gastropod molluscs – the lens is inside the
eye, beneath an external cornea. In arthropods, the lens is
formed by a thickening of the corneal cuticle. The camera
eyes of deep-sea animals – particularly those of squids –
can reach enormous size. The largest eyes known in the
animal kingdom are the camera eyes of the giant deep-sea
squid (Architeuthis dux) that can reach a diameter of over
30 cm! Camera eyes have better resolution and sensitivity
than any other eye type of comparable size.
Higher Visual Centers
Just as in vertebrates, which have a visual cortex and several
other brain areas for the higher processing of visual infor-
mation, visual signals leaving the retina of invertebrates are
processed sequentially, and along several parallel informa-
tion pathways, in a number of higher visual centers located
in the cephalic ganglion (the brain: Figure 4). In the well-
studied insects, visual information is first processed by the
retinotopically organized neuropils of the optic lobe: the
lamina, medulla, lobula, and in some species (notably flies,
butterflies, and beetles), a subdivision of the lobula known
as ‘the lobula plate.’ The lamina optimizes the signals
coming from the retina, and after receiving these signals,
the medulla – which remains little understood – makes
elementary analyses of the fundamental modalities of the
visual signal (space, time, color, and polarization). The
lobula, 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 moving
small-field targets. The lobula plate, which receives retino-
topic input from both the medulla and the lobula, houses
large wide-field motion-sensitive cells that are responsible
for analyzing optic flow induced during locomotion. The
optic lobes of other invertebrates are less well understood,
but they contain similar neuropils. The optic lobes of
cephalopods are particularly well developed. In Octopus
vulgaris, it has been estimated that the optic lobes alone
contain about 75% of the total number of neurons found in
the central nervous system.
An identical optic lobe connects each eye to the supra-
and subesophageal ganglia, and permits tracts of visual
information leaving the lobula and lobula plate to be
processed 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 by
giant descending fibers that carry highly specific sensory
information to the motor circuitry of the thoracic ganglia
that control the wings and legs (and thus locomotion). In
some species, some visual information is also carried to
the abdominal ganglia. Several important areas of visual
processing have now been identified in the insect brain.
The mushroom bodies – paired structures located in both
halves of the central brain region – are important in
integrating information from several sensory modalities,
and for their role in learning and memory. The central
complex – a highly columnar neuropil in the center of the
brain – seems to be involved in the spatial organization of
locomotion (and possibly spatial organization in general).
The Modalities of Vision
Like vertebrates, invertebrates have the ability to detect
and analyze the main properties of light, namely its inten-
sity, its direction, its color, and its polarization. These
properties define the modalities of vision, and together
these provide the information necessary for invertebrates
to interpret the visual world.
Sensitivity to Light
The greatest challenge for an eye that views a dimly
illuminated scene is to absorb sufficient photons of light
to reliably discriminate it. Certainly, ever since the pio-
neering studies of Yeandle in the horseshoe crab Limulus
in the late 1950s, we have known that photoreceptors can
respond to single photons with small but distinct electri-
cal responses known as ‘bumps.’ Such responses are found
in 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 also
inherently noisy, due to the unpredictable and random
nature of photon arrivals as well as to sources of neural
noise in the photoreceptors themselves. The effects of
these sources of noise are minimized by capturing more
light: the greater the number of photons captured, the
greater the signal relative to the noise and the more reliable
is visual discrimination. In regard to light capture, the eyes
of invertebrates living in dim light are among the most
sensitive found in the animal kingdom. Indeed, the huge
eyes of giant deep-sea squids (with a diameter of up to
30–40 cm) are likely to be the most sensitive eyes that
have ever existed.
Eyes of high absolute sensitivity to extended scenes
tend to have (relative to eye size) large pupils, short focal
lengths, and large photoreceptors. A frequently used
parameter to describe the light-gathering capacity of an
imaging system is its ‘F-number,’ the ratio of its focal
length f to the diameter of its entrance pupil A (i.e., f/A).
Vision: Invertebrates 515

6. This is a useful and easy metric for comparing the light-
gathering capacities of different eyes, with a lower
F-number indicating a brighter image. The huge camera
eyes of the nocturnal net-casting spider Dinopis subrufus
have an F-number of < 0.6, a much lower value than in
the anterior-median (AM) eyes of the diurnal jumping
spider Phidippus johnsoni (F-number ¼ 2.0). The dark-
adapted human eye has an F-number of around 2.1.
Thus, the eyes of Dinopis are clearly constructed for high
sensitivity. Among compound eyes, the superposition eyes
of the nocturnal hawkmoth Deilephila elpenor have an
F-number of around 0.7.
This high sensitivity to light has permitted many
invertebrates to have remarkably good vision in dim
light. Nocturnal hawkmoths and bees can see the colors
of flowers and negotiate dimly illuminated obstacles dur-
ing flight. Nocturnal bees can also home using learned
terrestrial landmarks, while moths and dung beetles can
navigate using constellations of stars or the dim pattern of
polarized light formed around the moon.
ca
pe
β
al
lo
me
la
r
(a)
(b)
500 μm
DRMe
ALo2
Ca
P
PB
CB
MO LAL
IL
LU
OLo
OL
∗ ∗
LT
ALo1
OLoMe
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 Gronenburg W (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 accessory
lobe. Scale bar ¼ 200 mm. 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.
516 Vision: Invertebrates

7. Temporal Vision
The ability of animals to see things that move at different
speeds is a reflection of their temporal vision, that is, how
‘fast’ they are able to see. A human observer is unable to
discriminate a bullet fired from a rifle simply because it
moves too rapidly to be seen. The fastest objects that can
be seen by an animal depend on many factors, including
the physiological properties of the photoreceptors and the
ambient light intensity. Moreover, the speed of vision
varies from species to species, with some species having
very fast vision (like the fast-flying aerobatic diurnal
insects) and others having very slow vision (like sedentary
nocturnal 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 detect
fast-moving objects (e.g., mates or prey in full flight), tend
to have fast vision, while those that are sedentary or
slowly moving tend to have slow vision.
The speed of vision varies widely between animals
because 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 ecological
needs of animals. In fact, the cell membrane, via its electri-
cal properties, acts as a ‘matched filter’ that is able to match
the response properties of the eye to the lifestyle that the
animal possesses, such as its locomotion speed or its pre-
ferred light intensity niche. In addition to these ecological
influences, the filtering properties of the photoreceptor
membrane and the transduction cascade are influenced
by the state of adaptation and the temperature.
The fastest visual systems found in the animal king-
dom are possessed by invertebrates, and the fastest are
likely to be those of calliphorid flies, which in a light-
adapted state are able distinguish light stimuli that flicker
at rates of up to around 300 Hz (for humans, in compari-
son, the limit is around 50 Hz). These flies engage in high-
speed pursuit and interception of mates, a behavior that
involves rapid and unpredictable changes in flight trajec-
tory and which requires a rapid visual response. For all
species, vision slows down as light levels fall (due to
adaptive changes in the physiological properties of the
photoreceptors), and nocturnal and deep-sea species tend
to have intrinsically slower vision than species active in
bright sunshine. Slower vision in dim light significantly
improves the reliability of vision because it filters out
faster visual details that tend to be inherently noisy and
degrade visual performance.
Spatial Vision
Most visual scenes viewed by animals on land or in the
upper depths of the ocean are extended in nature, meaning
that light reaches the eye from many different directions
at once. The spatial details of such a scene – defined by
local contrast differences between areas of light and dark –
are imaged by the eye onto the underlying retina. The
finest spatial details that can be seen by an eye are deter-
mined by two main factors: (1) the quality of the optical
system that images the scene (i.e., the cornea and lens(es))
and (2) the density and visual fields of the photoreceptors
that receive the image. Both these factors are in turn
subservient to the amount of light that the eye can collect
from 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 smaller
contrast differences typical of finer spatial details, which
tend to be lost in the noise as intensity falls, a limitation
that is equally problematic for all eyes, irrespective of their
optical quality or photoreceptor density. Thus, in general,
spatial resolution declines with light intensity.
The optical quality of an imaging system depends on
the extent it suffers from various aberrations, particularly
spherical and chromatic aberrations. Moreover, in very
small lenses such as those found in compound eyes, it also
depends on diffraction of light waves entering the aper-
ture. The effect of all these optical imperfections is to blur
the image formed on the retina, that is, to reduce its
contrast. Even though there are many invertebrate species
whose eyes lack an imaging system altogether (e.g., the
cephalopod Nautilus), those that do possess one very fre-
quently have surprisingly crisp optics and good optical
image resolution. For example, among the single lenses of
camera eyes, those of tiny cubozoan jellyfish eyes are
remarkably sharp, as are those of most gastropod and
cephalopod molluscs and most arachnids. What is typical
for most of these lenses is the presence of a powerful
radial (and often parabolic) gradient of refractive index
from the center to the edge of the lens, which tends to
almost exactly cancel spherical aberration. The lenses of
jumping spiders are an excellent example, which together
with a densely packed retina, allow jumping spider eyes to
have among the best spatial vision for their size in the
animal kingdom. In compound eyes, the small ommatidial
lenses are typically only 20–100 times wider than the
wavelength of visible light, a fact that invariably leads to
image degradation due to diffraction. In superposition
eyes, optical image quality is additionally limited by the
accuracy of superposition of light rays on the target rhab-
dom, and in species where the rhabdoms are not shielded
by screening pigments or a tapetal sheath, by the spread of
more 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. Like
the pixels of a digital camera, the density of photorecep-
tors in an eye sets the finest spatial detail that can be
reconstructed: more densely packed photoreceptors can
Vision: Invertebrates 517

8. reconstruct finer details. Ideally, the density of photore-
ceptors should be matched to the finest spatial detail that
can 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 supplies
much sharper images than the retina can resolve, and in
the tiny camera eyes of cubozoan jellyfishes, the retina is
located distal to the focal plane of the lens, which means
that the photoreceptors do not receive the sharply focused
image that the lens supplies. It would seem that even
though the eyes are capable of providing a sharp image,
these animals do not require the spatial acuity their lenses
afford. To exploit this acuity, a larger number of visual
cells would undoubtedly be needed to process the addi-
tional spatial information, bringing with it an energy cost
that the animal might not be able to afford. Ultimately, the
eye that evolves in a particular animal is the result of
natural selection, whereby an optimal balance is found
between the costs of maintaining the eye and the ecologi-
cal benefits it bestows upon the animal. This reasoning is
equally true for the evolution of all sensory organs.
In other camera eyes – particularly those of spiders and
cephalopods – the matrix of photoreceptors is usually
well matched to the optical quality of the image focused
by the lens. As an example, we can consider the AM eyes
of diurnal jumping spiders. In the jumping spider Portia
fimbriata, the AM eyes are among the sharpest known in
invertebrates, with the potential to discriminate spatial
details subtending as little as 2.4 min of arc, a performance
approaching that of our own eyes. Just as amazing is that
muscles connected to the internal structure of the eye
allow the sharpest region of the retina to be scanned
across the visual field. This outstanding spatial resolution
can be explained by both optical and neural adaptations.
In Portia, the AM eyes are almost 1 mm wide and almost
2 mm deep, with a retina divided into four distinct layers
of receptors (I–IV) arranged proximally to distally. Distal
to the receptors, the retina forms a pit aligned with the
ocular axis, the curved surface of which forms an interface
with the lower refractive index internal vitreous of the
eye. This interface acts as a diverging lens, increasing the
focal length of the system and magnifying the image by
about one-and-a-half times. This is analogous to the
telephoto system employed in falconiform birds of prey
and almost doubles visual acuity. Spatial resolution is
further improved by the presence of a gradient of refrac-
tive index in the lens that corrects for spherical aberration
in the image. However, the lens also suffers from chro-
matic aberration: light of shorter wavelength is focused to
a 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 with
maximum sensitivity to the shorter wavelengths are placed
more distally in layer IV (found to be ultraviolet-sensitive
cells), whereas those with maximum sensitivity to the
longer wavelengths are placed more proximally in layers
I and II (found to be green-sensitive cells).
In compound eyes, spatial vision is highly dependent
on the number of ommatidia present in each eye and
on their packing density. The number of ommatidia in
a single eye can vary from as few as one, as found in some
primitive ants, to as many as 30 000, as found in some species
of large dragonfly. Since each ommatidium essentially
accounts for a single ‘pixel’ of the image, eyes with more
ommatidia have the potential for higher spatial resolution.
The density of ommatidia – specified by their interom-
matidial angle △f (Figure 3(d)) – is also important. The
interommatidial angle is a measure of how tightly packed
the 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. The
interommatidial angle (in radians) is also related to the
corneal facet diameter (D) and the local radius of curvature
of the eye (R) by △f ¼ D/R, showing that a larger local
eye radius, or a smaller facet, produces a smaller inter-
ommatidial angle and greater spatial resolution. A smaller
facet, however, collects less light and invariably suffers
from the image-degrading effects of diffraction. A larger
eye radius means a larger eye, and this has limits too: animals
with compound eyes are generally rather small and there
is a limit to how big an eye they can carry. Apart from
anything else, the metabolic cost of having a larger eye
is quite enormous and sets a serious limit to how big a
particular eye can be. Instead, a wonderful compromise
has evolved that maintains eye size. Rather than enlarging
the whole eye, some animals have ‘enlarged’ a small part of
their eye, and thus a small part of their visual field. A local
increase in eye radius may not only allow an increase in
lens size (which reduces diffraction and improves light
capture) but if eye radius is increased sufficiently, it might
even allowa simultaneous reduction in △f (thus sharpening
spatial resolution). Unfortunately, any benefits gained in
one 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 in
apposition eyes. The presence of an acute zone implies
that one region of the visual world is more important to an
animal than others. Exactly which region depends on
several factors, many reflecting transient needs, such as
the need to find a mate or prey, or the need to detect the
advance of a predator. Others reflect more permanent
needs, not the least of which is the structure of the habitats
where animals live.
As an example of the latter, consider the apposition
eyes of animals adapted for life in a flat habitat: a desert
ant that runs across a salt pan or a fiddler crab that scans a
flat intertidal beach for mates. All experience a bright
world dominated by the horizon, and all possess eyes
having an elongated horizontal acute zone of enhanced
resolution known as a ‘visual streak.’ Because most objects
518 Vision: Invertebrates

9. of interest for these animals occur either at or very near
the horizon, visual streaks concentrate the majority of the
eye’s sampling stations – and thereby visual capacity – at
the same locations. In fiddler crabs, the apposition eyes
are vertically elongated, almost cylindrical, and located on
long stalks above the carapace. The shape of the eye
means that the radius of curvature in the vertical eye
plane 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 the
horizontal ones. △fv steeply narrows toward the horizon
(from both above and below) becoming smallest (0.3
) just
along the eye’s equator.
Acute zones have also evolved in the context of mate
detection. Female brachyceran flies, like blowflies and
hoverflies, have their eyes spaced well apart, but in
males the eyes are joined at the top of the head. This
extra area of eye constitutes a frontal-dorsal acute zone
used by the males to keep sight of females during high-
speed pursuits. Amusingly, these acute zones are often
referred to as ‘love spots.’ They are clearly seen in the
male hoverfly Volucella pellucens, which has large love spots
located frontally, 20
above the equator (Figure 5). The
interommatidial angle here falls to just 0.7
. The size of
the acute zone (the eye region where, say, △f 1.1
)
occupies 2230 deg2
of the visual field (shaded area in
Figure 5). In females there is also an acute zone, directed
exactly frontally and probably used for controlling flight.
In females, △f only falls to 0.9
, and the area of the acute
zone (△f 1.1
) is a mere 23% as large as that of males
(510 deg2
: shaded area in Figure 5). The acute zones of
male flies are not restricted to the eye surface. Below the
eye, there is an intricate neural pathway that is specific to
males. First, the connections of photoreceptor axons to
the lamina are quite different in the acute zone compared
to both the female’s eye and the rest of the male’s eye.
Higher up the brain, in the lobula, large male-specific
visual cells respond maximally to small dark objects that
move across a bright background in the frontal-dorsal
visual field, an ideal physiology for detecting silhouetted
females flying against the sky!
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 of
behavioral contexts including phototaxis and orientation,
camouflage, object detection and recognition, the detec-
tion of host plants for oviposition, the recognition of
flowers 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 recognizing
learned landmarks.
The sensation of color requires the presence of at least
two ‘spectral types’ of photoreceptor that view the same
region of space, followed by a neural comparison of the
signals generated in these photoreceptors (usually via a
neural 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, its
sensitivity to different wavelengths (or colors) of light.
For example, a UV spectral type absorbs primarily in
the ultraviolet part of the spectrum, whereas a green
L
D
D
V
Male
A
L
Female
V
A
1.3Њ
1.3Њ
1.2Њ
1.2Њ
1.1Њ
1.3Њ
1.4Њ
1.0Њ
0.9Њ
0.8Њ
0.7Њ
0.9Њ
1.1Њ
1.0Њ
1.4Њ
1.4Њ
1.5Њ
1.5Њ
1.6Њ
1.6Њ
1.3Њ
1.4Њ
1.5Њ
1.6Њ
Figure 5 Sexual dimorphism in the apposition eyes of the
hoverfly Volucella pellucens. (a) Female and (b) male. The visual
fields 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. Both
sexes 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’s
acute zone is used for fixating females during sexual pursuit.
Reproduced from Warrant EJ (2001) The design of compound
eyes and the illumination of natural habitats. In: Barth FG and
Schmid A (eds.) Ecology of Sensing, pp. 187–213. Berlin:
Springer Verlag.
Vision: Invertebrates 519

10. spectral type absorbs primarily in the green part of the
spectrum. Exactly which band of wavelengths a receptor
absorbs, and how sensitive it is to individual wavelengths
within that band, depends mainly on the nature of its
‘visual pigment’ rhodopsin. Rhodopsin molecules –
which absorb photons of light and trigger the generation
of an electrical signal – are composed of two parts: a large
‘opsin’ molecule, a protein consisting of a chain of around
350 amino acids embedded in the photoreceptor mem-
brane, and a small ‘chromophore,’ a molecule (typically
retinal, hydroxyretinal or dehydroretinal) that is coupled
to the opsin. The band of wavelengths absorbed by the
rhodopsin molecule depends on the exact sequence of
amino acids present in the opsin molecule and the iden-
tity of the chromophore.
Even though the absorption spectrum of the resident
rhodopsin 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, the
presence or absence of sensitizing or filtering pigments,
the photoreceptor’s length and placement, and the absor-
bance and reflectance of structures within the eye. For
instance, if the rhabdom of a UV spectral type lies distal to
that 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 its
partial absorption by the overlying UV-sensitive photore-
ceptor. This filtering will tend to narrow the spectral
sensitivity of the underlying green-sensitive photorecep-
tor and often shift its peak. Filtering resulting in spectral
sensitivity changes also occurs if a colored filter (e.g., a
membrane-bound vesicle of colored pigment) is located at
the distal entrance to the rhabdom, or between two tiered
rhabdoms (a common arrangement in the apposition eyes
of mantis shrimps), or if colored pigment granules are
located within or around the photoreceptor cells (as
found in a variety of insect and crustacean species). The
effect of all filtering mechanisms is to sharpen and tune
the spectral sensitivities of the resident spectral types of
photoreceptors, to maximize and optimize the range and/
or numbers of colors seen. Of course, the colors that
animals need to see in order to survive and reproduce
vary dramatically from species to species according to
their ecology. In fact, the number of photoreceptor spec-
tral types and the nature of any filtering that evolves in an
eye are ultimately driven by the ecological needs of its
owner (Figure 6).
Most invertebrate rhabdoms contain at least two pho-
toreceptor spectral types that share the same receptive
field, 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 retina
where only one photoreceptor spectral type is present,
whereas in other retinal areas, two or more types can be
present. This allows monochromatic vision in one part of
the visual field and the potential for color vision in
another part. A good example of this is the camera eye
of the firefly squid Watasenia scintillans (Figure 6(g)). Most
of the retina contains only one photoreceptor spectral
type with peak absorption at 484 nm (and allowing mono-
chromatic vision), whereas a small region of the ventral
retina (which views the dorsal visual field) contains two
further photoreceptor spectral types (peaking at 470 and
500 nm) and the possibility of dichromatic color vision
(which may be useful for detecting and analyzing the two
colors of bioluminescence produced by the squid during
courtship).
Many invertebrates have evolved two photoreceptor
spectral types throughout the retina (e.g., many spiders,
crustaceans, cockroaches, and ants), with the potential
for dichromatic color vision. Trichromacy, based on three
photoreceptor spectral types with peak absorptions in the
UV (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 three
photoreceptor 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 spectral
range 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 genus
Papilio : Figure 6(c)). Remarkably, the eyes of mantis
shrimps (Stomatopoda) have 12 photoreceptor spectral
types (Figure 6(f )) – the largest number known in the
animal kingdom – each narrowly tuned as the result of
spectral filtering. These 12 types evenly sample the spec-
trum from the deep UV to the far red but are only found
in a narrow band of ommatidia stretched across the center
of each eye (which is scanned across objects of interest).
Whether or not these colorful reef-dwelling crustaceans
have 12-dimensional color vision remains unknown, but
even if an animal possesses a certain number of photore-
ceptor spectral types, this does not necessarily imply that
all interact to create the maximal dimension of color
vision possible.
Polarization Vision
In addition to its particulate (photon) nature, light can
also be physically described as an electromagnetic wave,
an electric field and a magnetic field that oscillate in
520 Vision: Invertebrates

11. unison at the same frequency, but are perpendicular to
each other. The polarization properties of the wave can be
described by its electric field component, and particularly
by 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 and
circularly polarized light, and to use it in several impor-
tant behavioral contexts, notably navigation, orientation,
prey detection, and for interactions between individuals of
the same species. Except for a few controversial cases
(notably among the birds and fishes), polarization vision
is unknown in vertebrates.
The most common polarization vision in invertebrates
involves the detection and analysis of linearly (plane)
polarized light, since this is the most common form of
polarized light found in Nature. The plane of polarization
is defined as the plane in which the electric field wave (or
e-vector) oscillates. Most sources of light (both natural
and artificial) emit an immense number of such electro-
magnetic waves, and commonly these waves are collectively
plane unpolarized: the planes of polarization of individual
waves 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 less
share the same plane of polarization.
Watasenia
Deilephila
Papilio
1.0
0.5
0.0
Wavelength (nm)
Torrea
Primary
retina
Secondary
retina
Tridacna
Cupiennius
RelativesensitivityRelativesensitivity
1.0
0.5
0.0
1.0
0.5
0.0
1.0
0.5
0.0
1.0
0.5
0.0
1.0
0.5
0.0
1.0
0.5
0.0
1.0
0.5
0.0
Hemi-
cordelia
(a)
(b)
(c)
(d)
(e)
(f)
(g)
(h)
G
G
G
G
R
R
B
B
B
B
V
V
UV
UV
GBUV
UV
UV
RelativesensitivityRelativesensitivity
300 300
Wavelength (nm)
700600500400700600500400
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 spectral
classes 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 MSP
and 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.
Vision: Invertebrates 521

12. Time (s)
360Њ
20mV
20mV
250 μm
0Њ
360Њ
0Њ 90Њ
0Њ
2 4 6 8 10 12 14 16 4 6
AM
AM S
OTOT
−1
1
1
0
0
11
(a)
(b)
(d)
(e)
(c)
(f)
Retinula
POL neuron
Relativeresponse
Leptograpsus
(crustacea)
Gryllus
(orthoptera)
Melolontha
(coleoptera)
Cataglyphis
(hymenoptera)
Apis
(hymenoptera)
Danaus
(lepidoptera)
Notonecta
(hemiptera)
2–1
22
MM
LL
8 10 12 14
Time (s)
φ
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 not
contributing 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
522 Vision: Invertebrates

13. The dome of the sky is an excellent example of such a
source. Light from the sun (or the moon) is scattered by
air molecules in the Earth’s atmosphere to produce a
circularly symmetric pattern of linearly polarized light
centered on the disk of the sun (or moon). Each point in
the sky emits light polarized in only one direction, and the
direction of polarization shifts systematically from one
point in the sky to the next (which produces the pattern).
The degree of polarization is greatest along a circular
locus that is 90
from the sun or moon (and centered on
it). If an invertebrate has the possibility to unravel the
180
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 a
gigantic compass cue for extracting directional informa-
tion while navigating, either to simply keep a straight-line
course (e.g., ball-rolling dung beetles) or to use as a
component of an advanced path integration system used
for homing (e.g., the well-studied desert ant Cataglyphis
bicolor). Polarized skylight is even seen underwater, partic-
ularly at shallower depths (down to about 200 m). The fact
that water has a higher refractive index than air means
that 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 skylight
pattern to remain visible underwater, but turbid water
and the presence of waves can degrade it significantly.
Nevertheless, some species (e.g., grass shrimps and juve-
nile trout) can apparently use the underwater skylight
pattern to maintain a straight swimming course. Outside
Snell’s window, the space light is strongly polarized in the
horizontal direction because of scattering from suspended
particles. 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 to
orient away from the shore (and danger). Some inverte-
brates also use the aquatic backdrop of horizontally polar-
ized light to detect transparent prey. Many transparent
planktonic organisms are highly birefringent, which
means that they are opaque (and highly visible) when
seen against a polarized background by a polarization-
sensitive visual system (as found in squids). In terrestrial
habitats, horizontally plane-polarized light is formed by
reflection from horizontal surfaces, notably water surfaces
and shiny waxy leaves. Many flying insects – such as the
backswimmer Notonecta – search for new bodies of water
by looking for bright areas of horizontally polarized light
in the ventral visual field. In combination with appropri-
ate color cues, some papilionid butterflies also detect
suitable oviposition sites on the basis of horizontally
polarized light reflected from the leaves of their host
plants. Finally, some heliconid butterflies, squids, and
mantis shrimps use polarized light signals reflected from
their 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 – each
constrain the orientation of their resident rhodopsin
molecules, so that they are aligned along the microvillar
axis. Since each rhodopsin molecule is a linear absorption
dipole, and the dipole orientation is constrained by the
microvillus (and is identical to that for every other rho-
dopsin molecule), the rhabdom as a whole becomes highly
polarization sensitive. To actively remove polarization
sensitivity requires that the microvilli become disoriented
(e.g., by the rhabdom being twisted along its length, as
found 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-like
membranes of their photoreceptor outer segments allow
rhodopsin 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-polarized
light requires two ‘polarization classes’ of photoreceptor
that view the same region of space, followed by a neural
comparison of the signals generated in each (usually via a
neural opponency mechanism) at a subsequent (higher)
level of the visual system. Our understanding of this
process is almost entirely due to decades of research in
desert ants (Catalglyphis bicolor), crickets (Gryllus campes-
tris), and locusts (Schistocerca gregaria), all of which have a
specialized ‘dorsal rim area’ (or DRA), a narrow strip of
ommatidia along the dorsal-most margin of the compound
eye. The ommatidia of the DRA house the polarization-
sensitive photoreceptors, all of which have a dorsal field of
view. Outside the DRA, the rhabdoms are deliberately
twisted to eliminate their polarization sensitivity. The two
polarization classes of photoreceptor found in the DRA
have microvilli oriented in only one of two possible per-
pendicular directions (Figure 7(a)–7(c)). Within a rhabdom
of (say) eight rhabdomeres, at least one rhabdomere has
microvilli oriented in one direction, while all others have
shown to the right. L, lamina; M, medulla; AM, accessory medulla; OT, optic tract; S, cell soma. (f) Intracellular recordings from the
ipsilateral (right) and the contralateral part (left) of POL1 neurons while the e-vector orientation of a strongly polarized stimulus was
rotated by 360
. In the ipsilateral recording, the baseline undulates as a result of EPSP summation. The contralateral recording starts in
the dark, demonstrating spontaneous spiking activity; the white triangle marks the onset of the stimulus. In both recordings, the spike
frequency modulates as a function of e-vector orientation. Ipsilateral and contralateral recordings are from two POL1 neurons with
different e-vector tuning axes. Adapted with permission from Wehner R and Labhart T (2006) Polarisation vision. In: Warrant EJ and
Nilsson D-E (eds.) Invertebrate Vision, pp. 83–126. Cambridge: Cambridge University Press.
Vision: Invertebrates 523

14. microvilli oriented in the perpendicular direction (thus
forming two orthogonal analysis components for any direc-
tion of plane-polarized light). The signals generated in these
two classes form two analyzer channels, each of which can
act antagonistically (Figure 7(d)) on a polarization-sensitive
interneuron (known as ‘a POL neuron’) that arises in the
medulla (Figure 7(d)–7(f)). A well-studied POL neuron
is POL1 (found in crickets), a cell that sends its outputs to
both the central brain and to the contralateral medulla in
the optic lobe of the other eye (Figure 7(e)). In crickets,
three types of POL1 neurons have been found, each
highly sensitive and each having a very large receptive
field (60
across). The three types differ only in their
preferred orientation of polarized light relative to the long
axis of the head – 10
, 60
, and 130
– directions that
roughly correspond to the combined directional prefer-
ence of the pool of 200 DRA ommatidia that feed each
receptive field of each of the three POL1 neurons (there
are approximately 600 ommatidia in the cricket DRA).
These three classes of POL1 neurons are believed to
indirectly feed an array of ‘compass neurons’ (probably
located in the central brain), each of which represents a
certain body orientation relative to the symmetry plane of
the celestial polarization pattern. The pattern of responses
in the array of compass neurons, due to the inputs of the
three-axis system of POL1 neurons (10
, 60
, and 130
), is
then thought to code body orientation exactly. Evidence
for the existence of compass-like neurons is beginning to
emerge in the central complex of the locust brain (see
Figure 4(b) for the visual pathways of the brain involved
in polarization vision).
While much less common than linearly polarized light,
circularly polarized light can be produced by reflection
from certain natural surfaces, notably the cuticle of some
arthropods. Many scarab beetles – particularly those that
are brilliantly iridescent – have exactly the type of cuticle
necessary. To become circularly polarized, the two per-
pendicular components of the electric field wave of light
must become 90
out of phase (i.e., by a quarter of a
wavelength). Certain materials – such as the cuticle of
some beetles – induce this phase shift upon reflection.
Even though circularly polarized cuticular reflections
have been known for some time, their visual and behavioral
functions (if any) were unknown. Very recently, however,
certain species of mantis shrimps (stomatopods) have been
shown to not only reflect circularly polarized light, but
also to visually detect it and to react to it behaviorally.
The physiological basis for this ability lies within the
rhabdoms of a specialized band of ommatidia in the com-
pound eye: the eighth rhabdomere, which sits on top of the
other seven, has a thickness and microvillar orientation that
removes the 90
phase difference between the two perpen-
dicular components of the electric field of the incoming
circularly polarized light (i.e., it acts as a ‘quarter-wave
retarder’), thereby converting it to linearly polarized light.
This linearly polarized light is then detected and analyzed
in the conventional manner by the seven underlying rhab-
domeres, but in this case, as a code for the presence of
circularly polarized light.
Conclusions
The invertebrates – constituting nearly all species of
animal life on Earth – have conquered almost all known
habitats. Not surprisingly, their sensory organs, and par-
ticularly their eyes, have adapted to a remarkable range of
sensory environments and sensory stimuli. Among the
invertebrates are found all known optical designs of
eyes, endowing these animals with visual abilities that in
many cases rival, and occasionally even exceed, those of
humans. Compared with our own visual impression, many
species see much better in dim light, experience a faster
and more colorful world, and are able to distinguish the
subtleties of polarized light, a visual modality forever
beyond 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 vision
in a stomatopod crustacean. Current Biology 18: 429–434.
Krapp HG and Wiklein M (2008) Central processing of visual information
in insects. In: Albright T and Masland RH (eds.) The Senses:
A Comprehensive Reference, vol. 1, Basbaum AI, Kaneko A,
Shepherd GM, and Westheimer G (series eds.) Vision I, pp. 131–203.
Oxford: Academic Press.
Land MF and Nilsson DE (2002) Animal Eyes. Oxford: Oxford University
Press.
Warrant EJ and Nilsson DE (2006) Invertebrate Vision. Cambridge:
Cambridge University Press.
524 Vision: Invertebrates