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Web Topic 5.2
Perception of Polarized Light

A beam of pure polarized light consists of a population of electromagnetic waves with parallel electric vectors. The natural world contains complex patterns of polarized light that humans cannot perceive but which are very useful for animals that can distinguish different electric vectors of light. In Web Topic 4.1, we described some of the basic sources of natural polarized light from scattering and reflection. In this section we shall first clarify how polarized light is quantified and measured and then describe the patterns of polarized light in nature. Next, we show how photoreceptors can be made sensitive to the planes of polarized light and outline some of the uses animals make of polarized light.

Quantifying light polarization

Natural polarized light is rarely pure (i.e., comprised of 100% parallel e-vectors). Instead, it is partially polarized to varying degrees because it contains some fraction of e-vectors oriented in other directions. Four components are needed to completely describe polarized light are:

I = the overall intensity of the light beam
p = the degree of linear polarization, or the fraction of the overall light intensity that is linearly polarized parallel to a reference plane, which can range from 0–100%
α = the angle of strongest linear polarization, expressed in angles from 0–180º
ε = the fraction of circularly polarized light

Circularly polarized light is relatively rare in nature and often ignored, but later in this unit we describe some examples of animals that do in fact reflect circularly polarized light. The other three parameters are essential components for describing a beam of polarized light. The photoelectric device for measuring and computing these components is called a polarimeter. It consists of a radiometer that measures light intensity (in watts or photon flux per unit time, see Web Topic 4.2) with a rotating linear polarizer in front of the light-receiving lens. Three simultaneous or rapidly sequential measurements of light intensity must be made at three independent angles of rotation, typically 0, 60, and 120º. Using these values, one can compute the three essential components as follows:

I = 2(I0 + I60 + I120)/3
p = (Q2 + U2)1/2/I
α = 0.5 arctan(U/Q)

Here, Q = 2(2I0 + I60 + I120)/3 and U = –2(I120I60) 3–1/2. These three components—intensity, degree of polarization, and angle of polarization—are analogous to the color components of brightness, saturation, and hue, respectively. Also analogous to color measurements, polarized light can be measured for a very small point in space using a narrow light acceptor, called point-source polarimetry, or globally over a very large area, called imaging polarimetry. In presenting the results of imaging polarimetry, it is best to provide separate images of the three components (Figure 1). Overall intensity is typically displayed with a normal color image of a scene, degree of polarization is displayed with a grayscale image of the same scene where white may represent either 0% or 100% polarization depending on the situation, and angles of polarization are depicted with different hues (Horváth and Varjú 2004).

Figure 1: Imaging polarimetry. (A) Normal color image of a shiny black plastic sheet laid on an asphalt road. (B) Same subject showing degree of polarization, where darker areas are more strongly polarized. (C) Same subject showing angle of polarization. These patterns were measured by Gabor Horváth with imaging polarimetry.

Environmental patterns of polarized light

There are two main sources of polarized light in nature— reflection off of smooth surfaces and scattering in the sky by atmospheric particles. In both cases, the degree of polarization is very high at certain viewing angles, but the fraction of light that is polarized decreases gradually as the viewer or the light source moves away from this angle, and may become essentially nonpolarized at other angles. Figure 2 illustrates this concept for scattering in the sky.

Figure 2: Polarization of scattered light. Light from the sun, depicted by yellow arrows, is scattered by small particles (black point in center) in the atmosphere (note: The sun is not visible, but is located beyond the upper left corner of this illustration). This scattered light is vertically polarized when viewed from an angle of 90º relative to the sun. The plane of polarization of the scattered light is perpendicular to the plane defined by the incident and the scattered ray. Light that is scattered at an angle of 0º is nonpolarized and at intermediate angles it is partially polarized. (After Wehner 2001.)

Scattering creates a band of strongly polarized light across the sky that changes position as the sun moves (Figure 3). At sunrise and sunset the polarized band arcs across the middle of the sky with respect to the observer and can reach a maximum of 90% polarization on a clear day, but is usually less than this value. At noon the band is close to the horizon. Wavelengths in the middle of the visual range (blue and green) exhibit the strongest polarization intensity. The polarization intensity of red wavelengths is reduced by dust in the atmosphere, and UV intensity is reduced by multi-path scattering of the short wavelengths. Hazy and overcast skies increase this secondary scattering and may completely obliterate the polarization cues. However, conditions of patchy clouds with at least some open areas of sky will still retain their polarization pattern with respect to the sun and enable animals that rely on sky polarization to continue their activities (Wehner 1976, 2001; Cronin and Marshall 2011).

Figure 3: Pattern of polarized light in the sky. (A) Noon. (B) Sunrise. The blue dashed lines show the orientation of the e-vectors within the strongly polarized band. Less strong bands of polarized light form concentric circles around the sun. (After Wellington 1974; Wehner 1976.)

A similar pattern persists when the sky is viewed from underwater, but the degree of polarization is lower (maximum p of about 70%) because of multi-path scattering of light by the water. Figure 4 illustrates the pattern of polarized light entering through Snell’s window (see Web Topic 4.1) for a viewer within about 15 m of the surface. The position of the band is tilted at lower sun angles as a result of refraction of light at the air–water boundary. Outside of Snell’s window and at increasing depths, there is still a considerable amount of polarized light from extensive scattering in the water, but the sky pattern is attenuated and the e-vector orientation is primarily horizontal. At depths between 100–200 m below the surface, light is still linearly polarized at about 30% at noon, and long (red) and short (blue) wavelengths are more strongly polarized than middle wavelengths (Cronin and Shashar 2001; Sabbah et al. 2006; Cronin and Marshall 2011.)

Figure 4: Pattern of polarized light underwater. (A) Noon. (B) Sunrise. The band of maximum polarization forms a ring around the observer. The e-vector within the band is perpendicular to the scattering plane and parallel to the band. Snell’s window is defined by a viewing angle of 48.7º to either side of the vertical normal, beyond which light is internally reflected. (After Hawryshyn 1992.)

Light that is reflected off of the smooth surface of a dielectric material is completely horizontally polarized at Brewster’s angle of incidence and becomes increasingly less polarized at incident angles above and below Brewster’s angle. In nature, this source of polarized light arises from the reflection of light off of a smooth water surface such as a pond or lake (Figure 5A), and from specular reflection off of silvery scales (Figure 5B, C).

Figure 5: Polarization of reflected light. (A) Light incident on a smooth dielectric surface such as water is horizontally polarized (Wehner 2001). (B) Cross-section of a fish’s body. Downwelling light reflecting off of silvery fish scales containing guanine crystals is polarized at certain viewing angles where Brewster’s angle conditions are met. (C) Underwater photo of a fish with normal lens (top) and with an imaging polarizer (bottom), where white regions indicate stronger degree of polarization. Dorsal side of fish reflects 70–95% horizontally polarized light (upper arrow), whereas side flanks reflect 30–50% polarized light (lower arrow) (Denton and Rowe 1994; Shashar et al. 2000.)

Receptor sensitivity to polarized light

Sensitivity to polarized light has evolved many times independently and is found in a wide range of animals, including many orders of insects, spiders, crustaceans, cephalopods, fish, amphibians, reptiles, and birds (see Roberts et al. 2011 for a phylogenetic tree of taxa showing polarization sensitivity). Humans can perceive the linear polarization of light but this ability is believed to be a byproduct of the ocular media or foveal region and has no biological function. Species with well-developed polarization vision possess specialized sets of receptors sensitive to different e-vectors of polarized light. The neural output from several differently-angled cells or units are combined in additive and subtractive ways in higher-level neurons that comprise a polarization-opponent system, analogous to the color-opponent system. Thus different e-vectors of polarized light may be analyzed and perceived as if they were different colors. Behavioral experiments and neurophysiological studies support the view that the degree and orientation of polarized light is perceived as a graded stimulus (Horváth and Varjú 2004).

The visual pigment rhodopsin is inherently sensitive to the plane of polarized light. The crucial double bond of the retinal chromophore must be aligned in the same direction as the plane of polarization (e-vector) of the light for the molecule to absorb a photon. Dichroism is the general term for molecules or photoreceptor cells with selective sensitivity to the angle of polarization. Rhabdomeric photoreceptors are inherently more sensitive to polarized light than ciliary receptors, but both types of photoreceptor cells possess mechanisms to make them more dichroic (Roberts et al. 2011).

In a normal rod or cone cell, the long axes of the retinal molecules are maintained in a fixed horizontal position parallel to the plane of the disc membrane and perpendicular to the direction of incoming (axial) light shining on the photoreceptor (Figure 6A). The opsin molecules are relatively free to move along the disc membrane and can rotate around at random compass angles when viewed from above. No matter what the orientation of the e-vector of polarized light is, a similar number of retinal chromophores will be oriented parallel to it, and the response of the cell will be the same. However, if one were to shine light transversely from the side of the rod or cone, the response of the cell would become dependent on the polarization angle of the light—horizontally polarized light would be absorbed by retinal molecules oriented perpendicular to the ray’s direction, but vertically polarized light would not be absorbed by any retinal molecules. The cell is now selectively sensitive to just one plane of polarized light, i.e., it is dichroic.

Rhodopsin molecules are anchored on the tubular membranes of microvilli in rhabdomeric photoreceptors. Even if the rhodopsin molecules were randomly oriented on this rolled surface, as on a ciliary cell disc (Figure 6B), the cell would respond more strongly to axial light polarized in a direction parallel to the microtubules. Rhodopsin molecules on the sides of the tubules are more likely to be properly oriented to absorb this e-vector of light, compared to rhodopsin molecules on the tops and bottoms of the tubules, which are equally likely to respond to all e-vector orientations. The theoretical dichroic ratio of the cell’s response to parallel versus perpendicular polarized light is around 2. In fact, many rhabdomeric cells have dichroic ratios much higher than this value, up to 15. The orientation of rhodopsin molecules in specialized polarization-sensitive receptors is often strongly aligned parallel to the tubules, as shown in Figure 6C. This alignment is caused by connections between rhodopsin molecules and the cytoskeleton within the tubules, and by linkages between rhodopsin molecules on adjacent tubules (Roberts et al. 2011).

Figure 6: Sensitivity to polarized light in rhabdomeric and ciliary photoreceptors. (A) Ciliary receptors do not respond differently to light of different polarization orientations when shone from above (axial rays), but they will selectively absorb horizontally polarized light shone from the side (transverse rays). (B) Rhabdomeric receptors with rhodopsin chromophore molecules oriented randomly on the plasma surface, as shown here, would respond more strongly to axial rays polarized parallel to the microtubules than to rays polarized perpendicular to the microtubules. (C) Rhabdomeric cells specialized for polarized light detection contain retinal chromophores oriented parallel to the tubules, resulting in strong absorption of parallel polarized light.

The fine structure of polarization-sensitive rhabdomeric receptors has been studied most extensively in terrestrial insects (field crickets, honey bees, desert ants, and house flies) that detect the oscillation plane of polarized skylight with a group of specialized ommatidia situated at the dorsal rim area (DRA) of the compound eye. The dorsal rim ommatidia have properties that make them especially suitable for polarization vision. All of the ommatidia in the DRA, as well as the individual rhabdomere cells within each ommatidium, are sensitive to the same wavelength of light so that true color analysis is not compromised. Various adaptations are employed to make the visual field (light acceptance angle) of each ommatidium (or group of ommatidia) very broad for viewing a large portion of the sky. Each ommatidium contains two sets of strongly polarization-sensitive photoreceptors with orthogonally-arranged orientations. Neural outputs from the two sets are compared antagonistically so that each cell reports the intensity of incident polarized light of a given angle. Within the DRA, the main microvillar directions of adjacent ommatidia are rotated from front to back in a fan-shaped pattern. It is believed that output from at least three ommatidia types sensitive to different angles are combined and compared in polarization-opponent neurons to provide the insect’s brain with information on the orientation of celestial polarization, much like the measurement procedure of a polarimeter (Labhart and Meyer 1999; Horváth and Varjú 2004). Figure 7 shows cross sections through the specialized ommatidia compared to the regular ommatidia for these major groups of polarization-sensitive insects.

Figure. 7: Optical, spectral, and structural characteristics of the specialized ommatidia in the dorsal rim area of six insect species. Top row: these optical specializations generally increase the visual field of the ommatidium. Second row: polarization-sensitive ommatidia are often associated with a single hue type. Third row: the number of rhabdomeres in each ommatidium that contribute to polarization sensitivity. Fourth row: the ratio of these that are oriented in the two orthogonal positions. Fifth row: cross-sections through specialized dorsal rim ommatidia, colors approximate the hue sensitivity of the receptor (violet represents UV). Sixth row: regular dorsal ommatidia, which are used for color and spatial analysis; they lack the strict orthogonal orientation, and have other adaptations such as long and twisted rhabdoms, misaligned microvilli, and/or randomly oriented retinal chromophores so they are not differentially sensitive to the e-vector of light. (Labhart and Meyer 1999.)

Sensitivity to polarized light has been documented in vertebrates, primarily teleost fish, but also in some amphibian and reptile species (Horváth and Varjú 2004). How can ciliary photoreceptor cells become differentially sensitive to polarized light? Four mechanisms have been proposed. The most evident mechanism is to tilt the outer segment of the cone cell receptor on its side, so that the flat surfaces of the discs are parallel to the direction of incoming light cells (Fineran and Nicol 1978; Novales Flamarique and Hawryshyn 1998; Novales Flamarique 2011). This adaptation has been well-documented in anchovy fish (Figure 8). The same strategy has been employed in the extraocular polarized light detectors of amphibians and reptiles; the intracranial pineal body and frontal organ of amphibians contains cone-like receptors with longitudinal disc orientation, and the parietal eye of reptiles contains a ring of cone-like receptors lying on their sides (Hamasaki and Eder 1977; Adler 1976). Coho salmon (Oncorhynchus kisutch) have achieved a degree of polarization sensitivity by partially tilting the discs within the cones (Roberts et al. 2004).

Figure 8: Anchovy fish cones specialized for polarization sensitivity. (A) Side-on view of bay anchovy (Anchoa mitchilli) cones. Cones are arranged in rows of alternating long cones (LC, pink) and short cones (SC, blue) with bilobed outer segments. The disc stacks in the outer segments of these cones are tilted longitudinally so they are parallel to the incoming light direction (upward from the bottom). The discs in the two cone types are oriented orthogonal to each other, as shown in the top-down view in (B). This view also shows their flat-sided shape, which facilitates orthogonal packing. The cross-hatched areas are zones in which the discs of the two cone types overlap. Several mechanisms ensure that the long cones respond selectively to perpendicular e-vectors (Eperp, perpendicular to the plane of the page and indicated by the dot-filled circle; the orthogonal e-vector Epar is parallel to the plane of the page and indicated by double-headed arrows). Unpolarized incident light undergoes dichroic absorption when it passes through the bilobed outer segments of the short cells, and is further perpendicularly polarized as it reflects off the multilayered guanine platelets (yellow) and on to the lone cone outer segments. Likewise, light passing through the dichroic-absorbing short cones is further polarized as it reflects off the multilayered tapetum and back to the long cones. (After Novales Flamarique and Hárosi 2002.)

A second mechanism for making vertebrate cone cells dichroic is to guide light transversally onto adjacent cone cells by scattering or reflection. This idea arose from the observation that the polarization sensitivity in some species is found in double cones. In fish such as trout, the cones for color vision are arranged in highly regular mosaics with a square arrangement of red and green double cones, UV cones between them, and a blue cone in the middle, as shown in Figure 9A, B. The partitioning membrane between the red and green cones has a bulge that directs light transversally to the red cone and on to the UV cone, which is the primary polarized light sensor (Novales Flamarique, Hawryshyn and Hárosi 1998). Birds also possess double cones, which are arranged in orderly mosaic patterns of four or six double cones surrounding one or two single cones. The principle cone contains clear oil droplets and there is no screening pigment between the two cones, leading to the possibility that sideways scattering from the droplets could direct polarized light transversely to the secondary cone (Young and Martin 1984; Waldvogel 1990). However, this proposal is by no means proven (Muheim 2011).

Figure 9: Reflection and scattering in double cones. (A) Side view and (B) top view of the cone mosaics of the rainbow trout (Oncorhynchus mykiss), showing UV-, blue-, green- and red-sensitive cones. Axial incident light is reflected from the tilted partitioning membrane surface in two directions (single-headed arrows). The UV receptor receives transverse rays. The quadrilateral arrangement of four double cone units in a square mosaic leads to orthogonal e-vector reception; double-headed arrows in (B) indicate the dominant plane of polarization of the reflected light (Eh = horizontal e-vector, Ev = vertical e-vector). (A, B after Novales Flamarique, Hawryshyn and Hárosi 1998.)

A third possible mechanism that could facilitate selective e-vector absorption in vertebrate, as well as invertebrate, photoreceptors is to provide each receptor with a polarizing filter. Invertebrates with a cuticular carapace can produce surface structures that selectively reflect or transmit certain e-vectors of light (dichroism or birefringence, respectively). The lenses of ommatidia may contain polarizing filters that either enhance the selectivity or the polarization sensors, or act like polariod glasses to filter out glare in insects that hunt on the water’s surface (Horváth and Varjú 2004). Birds, reptiles, and amphibians can detect the Earth’s magnetic field by optical means with specialized photoreceptors (Philips et al. 2001; Wiltschko and Wiltschko 2006). The design of these receptors could make them simultaneously sensitive to the plane of polarized light if they cause the alignment of rhodopsin molecules within discs, but the true mechanism for polizarized light detection remains unknown (Muheim 2011). Birds appear to primarily use their sensitivity to polarized light to recalibrate their magnetic detectors before they fly at night, taking advantage of the strong overhead arch of polarized light at sunset (Moore and Phillips 1988; Phillips and Moore 1992; Muheim et al. 2006).

Finally, some recent research has suggested that cone cells might be able to align adjacent rhodopsin molecules in a parallel fashion using underlying protein–protein interactions, similar to the protein–cytoskeleton interactions demonstrated in rhabdomeric photoreceptors (Nair et al. 2002; Roberts and Needham 2007; Elliott et al. 2008). These interactions allow rhodopsin to oligomerize and form rafts of parallel chromophores, which would make the photoreceptor cell potentially sensitive to axially oriented polarized light (Roberts et al. 2011).

Functions of polarized light vision

The functions of polarized light vision include celestial cues for compass orientation, detection of aquatic habitat, reduction of flare from the water surface, increased contrast and prey detection underwater, and social communication. We take these up in turn.

Bees, ants, crickets, burrowing beetles, spiders, and probably many other arthropods that routinely return to the points of departure of their foraging journeys (e.g., nests, burrows, webs) use the patterns of polarized light in the sky for navigation. The natural sky patterns provide the animal with a compass if it knows the time of day, and with the time of day if it knows the direction. In fact, receivers can infer any particular compass direction from any particular sector of the sky at any time of day (Rossel 1993; Wehner 2001). Experimental evidence has recently been obtained demonstrating that honeybees truly use polarized light information to navigate to a food source (Kraft et al. 2011). The point to emphasize is that the polarization sensors do not provide the animal with individual e-vector directions, but with the compass direction of head orientation derived from global processing of e-vector gradients in the sky (Heinze and Homberg 2007). Behavioral and neurophysiological studies on the desert ant Cataglyphis suggest how this compass might work. Output from the polarization-sensitive photoreceptors in the dorsal rim area of the eye converge onto sets of at least three large-field polarization-sensitive interneurons, called POL neurons, located within a restricted area of the second visual ganglion. Each point of the compass is characterized by a particular response ratio of three POL neurons. There is some kind of neural network translating the broadband compass responses of the POL neurons into narrowly tuned responses of particular ‘compass neurons.’ A particular compass neuron should be activated whenever the animal is heading in a particular compass direction. Figure 10 illustrates the proposed compass model based on neurophysiological data. For further details on the neurophysiological basis of polarization analysis, see the review by Homberg et al. 2011.

Figure 10: Proposed mechanism for the e-vector compass in insects. (A) The e-vector pattern in the sky with sun (yellow point) at 60º elevation; orientation and size of the blue bars represent the angle and degree of polarization. (B) Array of polarization detectors in the dorsal rim area (DRA), showing left (L) and right (R) visual fields. The position of the pink bars shows the fan-like orientation of tuned e-vector sensors; only a few of the 55–75 polarization (POL) detectors per eye are shown here. Each detector consists of a pair of orthogonally arranged photoreceptors (see Figure 7). The dashed line in the center indicates the animal’s longitudinal body axis. (C) Response ratios of three large-field POL neurons, represented here by false colors. If the animal rotates relative to the skylight pattern (see (B), black arrow), different false colors show up (see (C), white arrow). (D) Hypothetical compass neurons arranged in a circular array. Each compass neuron encodes a particular response ratio based on input from the broadly tuned POL neurons. The filled pink circle indicates the compass neuron that is maximally excited when the animal faces the solar azimuth. (From Wehner 2001. Reproduced with permission from the Journal of Experimental Biology.)

Insects such as water beetles, bugs, dragonflies, and butterflies that seek water for breeding can make use of the polarized light reflected off the water’s surface during dispersal flights to detect aquatic habitat. Because light reflected off of water is horizontally polarized, these insects are especially attracted to horizontally polarized light sources on the ground and may possess photoreceptors that are selectively sensitive to this plane of polarization. Backswimmers Notonecta glauca are a prime example, as well as dragonflies, mayflies, and waterstriders. Similarly, butterflies may take advantage of reflection off of smooth, shiny leaves to detect optimal oviposition sites. Insects that hunt on the water’s surface, such a Dolichopodid flies and waterstriders, have vertical polarizers to reduce glare (Horváth and Varjú 2004).

Another major function of polarization sensitivity is improved underwater vision and foraging. The marine environment imposes a greater challenge for visual predators and prey than the terrestrial environment because of the strong scattering and absorption of light by the water. Maximum beam attenuation length in water is approximately 15 meters, compared to 6 kilometers in air. Scattering degrades the contrast between objects and the background by interposing veiling light between the observer and the object, much like a dense fog (Lythgoe 1979). As we saw above, the ocean is also characterized by partially polarized light. The plane of polarization is mostly horizontal, but the pattern of polarized light varies greatly as a function of time of day and viewing angle. A vertically polarized visual analyzer reduces the amount of scattered light perceived and greatly increases visibility and contrast (Figure 11). This effect is analogous to the benefit we obtain by wearing Polaroid glasses to reduce street glare (horizontally polarized reflections).

Figure 11: Contrast enhancement with polarization-sensitive vision. Photos of a school of small silvery fish (Caesio suevica), taken with no polarizing filter (left), a horizontal filter (middle) and a vertical filter (right). Notice how much more visible the fish are with the vertical filter, which removes the horizontally polarized veiling and background light. (Courtesy of N. Shashar.)

Underwater visual animals can gain much more than haze reduction if they possess sensitivity to the full range of e-vectors with a polarization-opponent system. Biological tissues reflect and scatter light with different polarization characteristics. Just as with color, animals that are able to perceive polarization differences have additional contrast cues they can use to detect objects (Wehner 2001; Cronin et al. 2003; Sabbah and Shashar 2006). Two particular cryptic strategies by marine prey organisms—transparency and mirrored reflection—can be broken by predators with polarization sensitivity. Transparent animals are never completely transparent, although they can be very difficult to see from a distance. However, transparent tissues may modify the light transmitted through the body. Some tissues are birefringent, in which the refractive index varies with the plane of polarized light and light waves are split into unequally reflected or transmitted waves. Other materials, called quarter-wave retarders, are able to depolarize incident waves that are initially polarized. Thus some objects in the ocean medium may be less polarized along some vector than the background, while other objects may be more polarized. In addition, transparent animals may reflect and scatter some of the unpolarized downwelling light so that the prey animal stands out against the horizontally polarized background light (Figure 12) (Johnsen et al. 2011). The squid Loglio pealei is a polarization-sensitive visual predator that can detect zooplankton prey at 70% greater distance under partially polarized lighting than under nonpolarized lighting (Shashar et al. 1998). Moreover, under normal lighting, the squid were far more likely to attack transparent glass beads that were made polarization-active by heat stressing compared to transparent beads that were not polarization-active. Similar studies have also discovered polarization sensitivity in predatory crayfish (Tuthill and Johnsen 2006).

Figure 12: Polarization breaks transparency. Two views of a transparent prawn (Lucifer spp.). The photo on the left shows the prawn under normal lighting with no polarizing filters on the lens. The photo on the right shows the same animal viewed through cross-polarizers. Two orthogagonal filters are positioned in front of the lens so that the background illumination is minimized. The animal is bright because it is scattering unpolarized light at other angles. The transparent tissues (cuticle and muscles) are also birefringent and modify the horizontally polarized transmitted light to various oblique angles. (Photo courtesy of N. Shashar.)

The logic behind the crypticity strategy of mirrored reflection is to match the background illumination. Many pelagic fish use silvery specular reflectance from guanine crystals in their scales as camouflage to reduce detection. The schooling fish in Figure 11 are attempting to use mirrored reflection to match their brightness to the background, but because they scatter more unpolarized light relative to the background, they become more visible when viewed through a vertical polarizing filter. In addition, silvery fish produce strong horizontally polarized specular reflectance at certain viewing angles (see Figure 2B,C), and a polarization-sensitive predator can perceive this reflection along the dorsal side of the prey (Shashar et al. 2000). Schooling fish may also be able to detect each other’s complex polarization reflections and use this information along with other senses to maintain school integrity (Rowe and Denton 1997).

The final function of polarization-sensitive vision is social signaling to conspecifics. A dramatic example occurs in the cuttlefish (Sepia officinalis) which uses controlled reflection of polarized light to produce species-specific signals on the arms, eyes, and forehead (Figure 13) (Shashar et al. 1996; Boal et al. 2004; Mäthger et al. 2009a). In contrast to the nonpolarized achromatic visual signals which are used in aggressive and courtship contexts, the polarized signals appear to be general indicators of sex and species identity. Females in particular respond differentially to images of conspecifics with and without the polarized signals. The patterns are turned on during normal alert activities, but disappear when the animal lies camouflaged in the sand and when it is is engaged in aggressive interactions, attacking prey, copulation, and egg-laying. The signals arise from reflecting iridophores in a chromatophore organ. Iridophores contain flat guanine platelets that produce partially polarized reflections. Groups of iridophores are oriented at different angles so the patterns are visible under a range of horizontal viewing angles (Chiou et al. 2007). As in other cephalopods, these iridophores are dynamic cells, capable of undergoing ultrastructural changes on neural command (Cooper et al. 1990; Shashar et al. 2001; Cronin et al. 2003; Mäthger et al. 2009b). Such changes shift the iridophores between organized and disorganized alignments, which enables the animals to change their polarization reflectances on time scales of a second or less. Cuttlefish eyes, like those of many other cephalopods, have a horizontal band of specialized orthogonal polarization-sensitive photoreceptors (Talbot and Marshall 2011). As mentioned previously, cuttlefish also use their polarization sensitivity while foraging to break the prey camouflage strategies of transparency and specular reflectance.

Figure 13: Frontal display of a cuttlefish, Sepia officinalis. The left panel shows an alert animal under normal white light illumination with no camera filter. The right panel shows the same photo with a horizontal polarizing light filter, which reveals a striking polarized light pattern on the forehead, eyes, and arms. (From Cronin et al. 2003. Reproduced with permission from the Journal of Experimental Biology.)

As we saw in the main text, mantis shrimp possess eyes with phenomenal color discrimination abilities. One possible reason for their system of many narrow but overlapping photoreceptor absorbance curves is their need for color constancy given the large changes in light quality at different water depths (Cheroske et al. 2009). They seem to have one more backup system for visual communication under conditions of variable light quality: the use of polarization signals. Polarization is much more predictable and stable with increasing depth then spectral quality. A large fraction of their compound eyes—the dorsal and ventral hemispheres—are devoted to spatial resolution and achromatic brightness contrast, and these ommatidia are polarization-sensitive. The color receptors are located in rows 1–4 of the midband, while midband rows 5–6 all have the same photopigment and are specialized for polarization detection. Their location adjacent to the wavelength detectors, paired arrangement with receptors having perpendicular e-vectors, and neural wiring similar to the color detectors suggests that they are specialized for a polarization-opponent system. Many stomatopod species have body parts that are obviously specialized for the reflection of strongly polarized light and are used in behavioral contexts that seem clearly linked to intraspecific communication (Figure 14). Species-specific patterns based on differential reflection of partially linearly polarized light could be unusually direct and easy to interpret since no other objects in the scene are likely to have a similar appearance. They would also be private and invisible to animals lacking polarization sensitivity. The polarization of specific body parts must be produced structurally in the carapace, as they do not change over time and are even present in the molt casts (Marshall et al. 1999; Kleinlogel et al. 2003; Cronin and Marshall 2004).

Figure 14: Potential polarized-light signal in the mantis shrimp Haptosquilla trispinosa. Successive frames captured on digital video through a polarization-switching, liquid crystal filter that rotates the plane of a polarization analyzer 90º between frames; the e-vector plane transmitted by the filter in each frame is shown by the white line (H, horizontal; V, vertical). The shrimp is sitting at its burrow entrance displaying its antennae, claws, and maxillipeds. Only the maxillipeds differentially reflect horizontally polarized light (arrows). These structures are powder blue under white light illumination (Cronin et al. 2003).

Polarized-light signaling has been found in terrestrial forest environments, where the intensity and spectral composition of light varies greatly (see Figure 5.4 in the main text). Although natural polarization is limited because of strong filtering by the canopy, contrasting polarized light reflectance can provide a more consistent pattern for species recognition than colored signals. The butterfly Heliconius cydno reflects iridescent colors from the wings. The reflected light is both chromatically saturated and 90% polarized (Sweeney et al. 2003). Males of this species appear to recognize females based on this polarization. When the reflected light from females is artificially depolarized, males approach them much less frequently. A survey of the presence of polarized light reflectance from 144 species of nymphalid butterflies found 75 species with polarized patterns. These species were significantly more likely to inhabit forest habitats than open habitats (Douglas et al. 2007).

Finally, a few animal taxa have been found to reflect circularly polarized light, in which the electric vector rotates either clockwise (right-handed) or counterclockwise (left-handed) while the wave travels. Although very rare in the natural environment (starlight becomes partially circularly polarized, as well as underwater backscattered light outside of Snell’s window), it is not difficult to produce with manmade materials, and circularly polarized reflection (CPR) is widespread among scarab beetles. In a survey of 16,650 species from 1320 genera, 89% showed some level of CPR ranging from very low degrees of polarization up to a maximum of 97% (Pye 2010). Most cases had left-handed rotation. These beetles are generally green in color, but they can change in appearance from brilliant, metallic green to black when viewed with left- and right-handed polarizing filters (Hegedüs et al. 2006; Goldstein 2006; Pye 2010). The fine structure of the exoskeleton consists of tightly packed hexagon cells with a cone structure (Jewell et al. 2007; Sharma et al. 2009). Under the light microscope, the cones appear yellow in the center with a green surround. Concentric nested arcs encircle the cones to form a helical structure (Figure 15). Behavioral tests demonstrate that the beetles respond selectively to objects of different degrees and rotations of CPR (Brady and Cummings 2010).

Visual reception mechanisms for CPR have not been studied in the beetles yet, but in another group that also shows CPR, the mantis shrimps (stomatopods), a potential visual mechanism has been described (Chiou et al. 2008). In a linearly polarized light wave, the x and y vibrational e-vector components are in phase; when these vectors are out of phase, an elliptical wave results, and when the vectors are 90º out of phase, a circular wave results. If a circularly polarized light wave travels through a birefringent material with a thickness and refractive index that slows the wave in one e-vector orientation by 1/4 of a wavelength (called a quarter-wave retarder), the two vectors are brought back into phase, and the wave becomes linearly polarized. A few species of stomatopods (Odontodactylus) with the usual midband linear-polarized light detectors have placed such quarter-wave retarders in a layer over these photoreceptor cells to filter the incoming light. These species have been shown to distinguish behaviorally between left-CPR and right-CPR objects. Moreover, three species were found to have sex-specific circular reflectance patterns on body parts used for behavioral displays in males (Chiou et al. 2008). Circularly polarized light signals thus create a private communication channel in both scarab beetles and stomatopods.

Figure 15: Reflection of circularly polarized light from the scarab beetle Crysina gloriosa. (A, B) Photo of a beetle under unpolarized light illumination using a left-hand and right-hand circular polarizing filter. (C) Light microscope photo of the same beetle’s exoskeleton showing the packed, conical cells, approximately 10 mm in diameter, with yellow centers and green surrounds. (D) An x-y section of a confocal microscope image showing concentric rings that form the helical reflective surface (Sharma et al. 2009).

Further reading

Horváth, G. and D. Varjú. 2004. Polarized Light in Animal Vision. Berlin: Springer-Verlag.

The entire July 2001 issue of the Journal of Experimental Biology contains excellent review articles from the “Second Workshop on Ultraviolet and Polarization Vision.”

The March 2011 issue of Philosophical Transactions of the Royal Society of London – B contains a series of articles on “New directions in the detection of polarized light” stimulated by a small international meeting in 2008 on Heron Island, Australia.

Useful websites

http://polarization.com/

http://www.colorado.edu/physics/2000/polarization/index.html

http://micro.magnet.fsu.edu/primer/java/scienceopticsu/polarizedlight/filters/

http://hyperphysics.phy-astr.gsu.edu/hbase/phyopt/polarcon.html

http://en.wikipedia.org/wiki/Circularly_polarized_light

http://web.qbi.uq.edu.au/ecovis/index.html

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