Tsyr Huei Chiou

Circular polarization vision in a stomatopod crustacean.

We describe the addition of a fourth visual modality in the animal kingdom, the perception of circular polarized light. Animals are sensitive to various characteristics of light, such as intensity, color, and linear polarization [1, 2]. This latter capability can be used for object identification, contrast enhancement, navigation, and communication through polarizing reflections [2-4]. Circularly polarized reflections from a few animal species have also been known for some time [5, 6]. Although optically interesting [7, 8], their signal function or use (if any) was obscure because no visual system was known to detect circularly polarized light. Here, in stomatopod crustaceans, we describe for the first time a visual system capable of detecting and analyzing circularly polarized light. Four lines of evidence-behavior, electrophysiology, optical anatomy, and details of signal design-are presented to describe this new visual function. We suggest that this remarkable ability mediates sexual signaling and mate choice, although other potential functions of circular polarization vision, such as enhanced contrast in turbid environments, are also possible [7, 8]. The ability to differentiate the handedness of circularly polarized light, a visual feat never expected in the animal kingdom, is demonstrated behaviorally here for the first time.

Polarization Vision and Its Role in Biological Signaling

Abstract Visual pigments, the molecules in photoreceptors that initiate the process of vision, are inherently dichroic, differentially absorbing light according to its axis of polarization. Many animals have taken advantage of this property to build receptor systems capable of analyzing the polarization of incoming light, as polarized light is abundant in natural scenes (commonly being produced by scattering or reflection). Such polarization sensitivity has long been associated with behavioral tasks like orientation or navigation. However, only recently have we become aware that it can be incorporated into a high-level visual perception akin to color vision, permitting segmentation of a viewed scene into regions that differ in their polarization. By analogy to color vision, we call this capacity polarization vision. It is apparently used for tasks like those that color vision specializes in: contrast enhancement, camouflage breaking, object recognition, and signal detection and discrimination. While color is very useful in terrestrial or shallow-water environments, it is an unreliable cue deeper in water due to the spectral modification of light as it travels through water of various depths or of varying optical quality. Here, polarization vision has special utility and consequently has evolved in numerous marine species, as well as at least one terrestrial animal. In this review, we consider recent findings concerning polarization vision and its significance in biological signaling.

A Different Form of Color Vision in Mantis Shrimp

One of the most complex eyes in the animal kingdom can be found in species of stomatopod crustaceans (mantis shrimp), some of which have 12 different photoreceptor types, each sampling a narrow set of wavelengths ranging from deep ultraviolet to far red (300 to 720 nanometers) (1–3). Functionally, this chromatic complexity has presented a mystery (3–5). Why use 12 color channels when three or four are sufficient for fine color discrimination? Behavioral wavelength discrimination tests (Δλ functions) in stomatopods revealed a surprisingly poor performance, ruling out color vision that makes use of the conventional color-opponent coding system (6–8). Instead, our experiments suggest that stomatopods use a previously unknown color vision system based on temporal signaling combined with scanning eye movements, enabling a type of color recognition rather than discrimination. Stomatopods use multiple photoreceptors to allow rapid color recognition rather than color discrimination. [Also see Perspective by Land and Osorio] Living Technicolor Color vision is generally carried out through the number of photoreceptor types found in the retina. The mantis shrimps (stomatopods) can have up to 12 photoreceptors, far more than needed for even extreme color acuity. Thoen et al. (p. 411; see the Perspective by Land and Osorio) conducted paired color discrimination tests with stomatopods and found that their ability to discriminate among colors was surprisingly low. Instead, stomatopods appear to use a color identification approach that results from a temporal scan of an object across the 12 photoreceptor sensitivities. This entirely unique form of vision would allow for extremely rapid color recognition without the need to discriminate between wavelengths within a spectrum.

Light habitats and the role of polarized iridescence in the sensory ecology of neotropical nymphalid butterflies (Lepidoptera: Nymphalidae)

SUMMARY The exploitation of polarized light may increase perceived visual contrast independent of spectrum and intensity and thus have adaptive value in forest habitats, where illumination varies greatly in brightness and spectral properties. Here we investigate the extent to which Costa Rican butterflies of the family Nymphalidae exhibit polarized wing reflectance and evaluate the types of habitats in which the trait is commonly found. We also examine the degree of polarized reflectance of wing patterns in representative species belonging to the nymphalid subfamilies Charaxinae, Heliconiinae, Morphinae and Nymphalinae. Polarized reflectance was evaluated using museum specimens illuminated with a light source that simulated the spectrum of ambient sunlight and viewed through a polarized filter. Of the 144 species examined, 75 species exhibited polarized reflectance patterns. These species were significantly more likely to occupy forest habitats than open habitats. A concentrated changes test performed on a phylogeny of the Nymphalidae, with the Papilionidae as an outgroup, provides further support for the correlated evolution of polarized iridescence and life in a forest light environment. These results are consistent with the hypothesis that the production and detection of polarized light may have adaptive communicative value in those species inhabiting forest habitats with complex light conditions. The potential utility of polarized iridescence and iridescent wing coloration within differing ambient spectral environments is discussed to provide a basis for future investigation of the polarized light ecology of butterflies.

Spectral and spatial properties of polarized light reflections from the arms of squid (Loligo pealeii) and cuttlefish (Sepia officinalis L.).

SUMMARY On every arm of cuttlefish and squid there is a stripe of high-reflectance iridophores that reflects highly polarized light. Since cephalopods possess polarization vision, it has been hypothesized that these polarized stripes could serve an intraspecific communication function. We determined how polarization changes when these boneless arms move. By measuring the spectral and polarizing properties of the reflected light from samples at various angles of tilt and rotation, we found that the actual posture of the arm has little or no effect on partial polarization or the e-vector angle of the reflected light. However, when the illumination angle changed, the partial polarization of the reflected light also changed. The spectral reflections of the signals were also affected by the angle of illumination but not by the orientation of the sample. Electron microscope samples showed that these stripes are composed of several groups of multilayer platelets within the iridophores. The surface normal to each group is oriented at a different angle, which produces essentially constant reflection of polarized light over a range of viewing angles. These results demonstrate that cuttlefish and squid could send out reliable polarization signals to a receiver regardless of arm orientation.

Behavioural relevance of polarization sensitivity as a target detection mechanism in cephalopods and fishes

Aquatic habitats are rich in polarized patterns that could provide valuable information about the environment to an animal with a visual system sensitive to polarization of light. Both cephalopods and fishes have been shown to behaviourally respond to polarized light cues, suggesting that polarization sensitivity (PS) may play a role in improving target detection and/or navigation/orientation. However, while there is general agreement concerning the presence of PS in cephalopods and some fish species, its functional significance remains uncertain. Testing the role of PS in predator or prey detection seems an excellent paradigm with which to study the contribution of PS to the sensory assets of both groups, because such behaviours are critical to survival. We developed a novel experimental set-up to deliver computer-generated, controllable, polarized stimuli to free-swimming cephalopods and fishes with which we tested the behavioural relevance of PS using stimuli that evoke innate responses (such as an escape response from a looming stimulus and a pursuing behaviour of a small prey-like stimulus). We report consistent responses of cephalopods to looming stimuli presented in polarization and luminance contrast; however, none of the fishes tested responded to either the looming or the prey-like stimuli when presented in polarization contrast.

Changes in light-reflecting properties of signalling appendages alter mate choice behaviour in a stomatopod crustacean Haptosquilla trispinosa

Stomatopod crustaceans have complex visual systems capable of excellent spatial, colour and polarization vision. Accordingly, visual signals are used widely in their intraspecific communication behaviour. We tested the role of a particular visual signal thought to be important in mate choice in a stomatopod crustacean Haptosquilla trispinosa, by manipulating the ability of a brightly blue coloured, polarized light reflecting region on their first maxillipeds to reflect light. Depriving male H. trispinosa of their ability to produce bright blue polarized light signals did not affect their overall chances of being accepted by females. However, in comparison with control males, they had to signal significantly longer before being accepted by females, had briefer mating durations and received more aggressive responses from females before mating. These data show that males without coloured and polarized maxilliped reflections find it more difficult to be accepted by females than normal males, indicating that these light signals play an important role in mate selection in H. trispinosa. Our experiments show that highly regionalized, specific visual stimuli can be used in intraspecific signalling in a marine crustacean group known for its visual competence.

A novel function for a carotenoid: astaxanthin used as a polarizer for visual signalling in a mantis shrimp

SUMMARY Biological signals based on color patterns are well known, but some animals communicate by producing patterns of polarized light. Known biological polarizers are all based on physical interactions with light such as birefringence, differential reflection or scattering. We describe a novel biological polarizer in a marine crustacean based on linear dichroism of a carotenoid molecule. The red-colored, dichroic ketocarotenoid pigment astaxanthin is deposited in the antennal scale of a stomatopod crustacean, Odontodactylus scyllarus. Positive correlation between partial polarization and the presence of astaxanthin indicates that the antennal scale polarizes light with astaxanthin. Both the optical properties and the fine structure of the polarizationally active cuticle suggest that the dipole axes of the astaxanthin molecules are oriented nearly normal to the surface of the antennal scale. While dichroic retinoids are used as visual pigment chromophores to absorb and detect polarized light, this is the first demonstration of the use of a carotenoid to produce a polarizing signal. By using the intrinsic dichroism of the carotenoid molecule and orienting the molecule in tissue, nature has engineered a previously undescribed form of biological polarizer.

Spectral Sensitivities and Color Signals in a Polymorphic Damselfly

Animal communication relies on conspicuous signals and compatible signal perception abilities. Good signal perception abilities are particularly important for polymorphic animals where mate choice can be a challenge. Behavioral studies suggest that polymorphic damselflies use their varying body colorations and/or color patterns as communication signal for mate choice and to control mating frequencies. However, solid evidence for this hypothesis combining physiological with spectral and behavioral data is scarce. We investigated this question in the Australian common blue tail damselfly, Ischnura heterosticta, which has pronounced female-limited polymorphism: andromorphs have a male-like blue coloration and gynomorphs display green/grey colors. We measured body color reflectance and investigated the visual capacities of each morph, showing that I. heterosticta have at least three types of photoreceptors sensitive to UV, blue, and green wavelength, and that this visual perception ability enables them to detect the spectral properties of the color signals emitted from the various color morphs in both males and females. We further demonstrate that different color morphs can be discriminated against each other and the vegetation based on color contrast. Finally, these findings were supported by field observations of natural mating pairs showing that mating partners are indeed chosen based on their body coloration. Our study provides the first comprehensive evidence for the function of body coloration on mate choice in polymorphic damselflies.

Polarization signals in mantis shrimps

While color signals are well known as a form of animal communication, a number of animals communicate using signals based on patterns of polarized light reflected from specialized body parts or structures. Mantis shrimps, a group of marine crustaceans, have evolved a great diversity of such signals, several of which are based on photonic structures. These include resonant scattering devices, structures based on layered dichroic molecules, and structures that use birefringent layers to produce circular polarization. Such biological polarizers operate in different spectral regions ranging from the near-UV to medium wavelengths of visible light. In addition to the structures that are specialized for signal production, the eyes of many species of mantis shrimp are adapted to detect linearly polarized light in the ultraviolet and in the green, using specialized sets of photoreceptors with oriented, dichroic visual pigments. Finally, a few mantis shrimp species produce biophotonic retarders within their photoreceptors that permit the detection of circularly polarized light and are thus the only animals known to sense this form of polarization. Mantis shrimps use polarized light in species-specific signals related to mating and territorial defense, and their means of manipulating lights polarization can inspire designs for artificial polarizers and achromatic retarders.