Martin J. How

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.

Claw waving display changes with receiver distance in fiddler crabs, Uca perplexa

Effective communication is critically dependent on the successful transfer of information and, because environmental and social conditions can affect signal transmission, animals should be able to adjust their signals to optimize reliability. We show, apparently for the first time in a movement-based signal, that visual displays are adjusted with respect to the distance of signal receivers. Not only does this show the ability of the fiddler crab to judge distance, but this also shows that signalling is context dependent on surprisingly fine spatial and temporal scales. We elicited courtship behaviour in the crabs with tethered females and simultaneously recorded the displays of males from above and from crab-eye level. As females approached, males increased signal intensity by shortening display duration and altered signal form by reducing the lateral movement component of the waving signal. We suggest that males tune their waving display depending on receiver distance (a) to balance energetic costs with reproductive benefits, (b) to alter the information content of the signal and (c) to avoid signal misinterpretation. Such fine-scale context sensitivity is likely to be far more widespread in animal communication than hitherto recognized from similar signal modifications in auditory communication.

Cyp27c1 Red-Shifts the Spectral Sensitivity of Photoreceptors by Converting Vitamin A1 into A2

Some vertebrate species have evolved means of extending their visual sensitivity beyond the range of human vision. One mechanism of enhancing sensitivity to long-wavelength light is to replace the 11-cis retinal chromophore in photopigments with 11-cis 3,4-didehydroretinal. Despite over a century of research on this topic, the enzymatic basis of this perceptual switch remains unknown. Here, we show that a cytochrome P450 family member, Cyp27c1, mediates this switch by converting vitamin A1 (the precursor of 11-cis retinal) into vitamin A2 (the precursor of 11-cis 3,4-didehydroretinal). Knockout of cyp27c1 in zebrafish abrogates production of vitamin A2, eliminating the animals ability to red-shift its photoreceptor spectral sensitivity and reducing its ability to see and respond to near-infrared light. Thus, the expression of a single enzyme mediates dynamic spectral tuning of the entire visual system by controlling the balance of vitamin A1 and A2 in the eye.

High-resolution polarisation vision in a cuttlefish

Summary For animals that can see it, the polarisation of light adds another dimension to vision, analogous to adding colour to a black and white image [1,2]. Whilst some animals use the orientation of the electric field vector (e-vector) for navigation and orientation [3], the ability to discriminate angular differences in e-vector has been implicated in object recognition for predator/prey detection [4,5] as well as signalling and communication [6]. In all animals previously tested, however, the resolution of e-vector angle discrimination has been found to be in the range 10–20° [5,7,8], which is inadequate for the typical e-vector differences measured in relevant natural visual scenes [9]. In this study, we found that mourning cuttlefish ( Sepia plangon ) are able to detect differences between e-vector orientations as small as 1°. Not only is this the most acute e-vector angle discrimination measured behaviourally in any animal, but it provides a high enough resolution to be relevant to real world visual tasks. We analysed natural underwater scenes using computer based polarisation imaging. When we increased the resolution of our system, we discovered information not detected using normal-resolution imaging polarimetry and invisible to animals lacking fine e-vector angle discrimination. For example, we found that high-resolution e-vector discrimination provides a new way of breaking typical intensity-based background matching. S. plangon lacks colour vision, like most other cephalopods, and high-resolution polarisation vision may provide an alternative source of contrast information that is just as fine-scale.

To Be Seen or to Hide: Visual Characteristics of Body Patterns for Camouflage and Communication in the Australian Giant Cuttlefish Sepia apama

It might seem obvious that a camouflaged animal must generally match its background whereas to be conspicuous an organism must differ from the background. However, the image parameters (or statistics) that evaluate the conspicuousness of patterns and textures are seldom well defined, and animal coloration patterns are rarely compared quantitatively with their respective backgrounds. Here we examine this issue in the Australian giant cuttlefish Sepia apama. We confine our analysis to the best-known and simplest image statistic, the correlation in intensity between neighboring pixels. Sepia apama can rapidly change their body patterns from assumed conspicuous signaling to assumed camouflage, thus providing an excellent and unique opportunity to investigate how such patterns differ in a single visual habitat. We describe the intensity variance and spatial frequency power spectra of these differing body patterns and compare these patterns with the backgrounds against which they are viewed. The measured image statistics of camouflaged animals closely resemble their backgrounds, while signaling animals differ significantly from their backgrounds. Our findings may provide the basis for a set of general rules for crypsis and signals. Furthermore, our methods may be widely applicable to the quantitative study of animal coloration.

High e-vector acuity in the polarisation vision system of the fiddler crab Uca vomeris

SUMMARY Polarisation vision is used by a variety of species in many important tasks, including navigation and orientation (e.g. desert ant), communication and signalling (e.g. stomatopod crustaceans), and as a possible substitute for colour vision (e.g. cephalopod molluscs). Fiddler crabs are thought to possess the anatomical structures necessary to detect polarised light, and occupy environments rich in polarisation cues. Yet little is known about the capabilities of their polarisation sense. A modified polarisation-only liquid crystal display and a spherical rotating treadmill were combined to test the responses of fiddler crabs to moving polarisation stimuli. The species Uca vomeris was found to be highly sensitive to polarised light and detected stimuli differing in e-vector angle by as little as 3.2 deg. This represents the most acute behavioural sensitivity to polarised light yet measured for a crustacean. The occurrence of null points in their discrimination curve indicates that this species employs an orthogonal (horizontal/vertical) receptor array for the detection of polarised light.

Variability of a dynamic visual signal: the fiddler crab claw-waving display

Fiddler crabs use elaborate, species-specific claw-waving displays to communicate with rivals and mates. However, detailed comparative studies of fiddler crab signal structure and structural variations are lacking. This paper provides an analysis of the claw-waving displays of seven Australian species of fiddler crab, Uca mjoebergi, U. perplexa, U. polita, U. seismella, U. signata, U. elegans and U. vomeris. We used digital video to record and analyse the fine-scale spatiotemporal properties of these movement-based visual signals. We found that the structure and timing of the displays is species-specific, exhibiting inter-specific differences that follow phylogenetic relationships. The displays showed intra-specific variation according to individual identity, geographic location and fine-scale behavioural context. The observed differences and variations are discussed in the light of the evolutionary forces that may shape their design.

Circularly Polarized Light as a Communication Signal in Mantis Shrimps

Animals that communicate using conspicuous body patterns face a trade-off between desired detection by intended receivers and undesired detection from eavesdropping predators, prey, rivals, or parasites. In some cases, this trade-off favors the evolution of signals that are both hidden from predators and visible to conspecifics. Animals may produce covert signals using a property of light that is invisible to those that they wish to evade, allowing them to hide in plain sight (e.g., dragonfish can see their own, otherwise rare, red bioluminescence). The use of the polarization of light is a good example of a potentially covert communication channel, as very few vertebrates are known to use polarization for object-based vision. However, even these patterns are vulnerable to eavesdroppers, as sensitivity to the linearly polarized component of light is widespread among invertebrates due to their intrinsically polarization sensitive photoreceptors. Stomatopod crustaceans appear to have gone one step further in this arms race and have evolved a sensitivity to the circular polarization of light, along with body patterns producing it. However, to date we have no direct evidence that any of these marine crustaceans use this modality to communicate with conspecifics. We therefore investigated circular polarization vision of the mantis shrimp Gonodactylaceus falcatus and demonstrate that (1) the species produces strongly circularly polarized body patterns, (2) they discriminate the circular polarization of light, and (3) that they use circular polarization information to avoid occupied burrows when seeking a refuge.

Polarization distance: a framework for modelling object detection by polarization vision systems.

The discrimination of polarized light is widespread in the natural world. Its use for specific, large-field tasks, such as navigation and the detection of water bodies, has been well documented. Some species of cephalopod and crustacean have polarization receptors distributed across the whole visual field and are thought to use polarized light cues for object detection. Both object-based polarization vision systems and large field detectors rely, at least initially, on an orthogonal, two-channel receptor organization. This may increase to three-directional analysis at subsequent interneuronal levels. In object-based and some of the large-field tasks, the dominant e-vector detection axes are often aligned (through eye, head and body stabilization mechanisms) horizontally and vertically relative to the outside world. We develop Bernard and Wehners 1977 model of polarization receptor dynamics to apply it to the detection and discrimination of polarized objects against differently polarized backgrounds. We propose a measure of ‘polarization distance’ (roughly analogous to ‘colour distance’) for estimating the discriminability of objects in polarized light, and conclude that horizontal/vertical arrays are optimally designed for detecting differences in the degree, and not the e-vector axis, of polarized light under natural conditions.

Surveying noctural cuttlefish camouflage behaviour using an AUV

This paper describes a recent study in which an Autonomous Underwater Vehicle (AUV) with a high resolution stereo-imaging system was used to document nocturnal camouflage behaviour in cuttlefish at a well known spawning site in Whyalla, South Australia. The AUVs ability to fly at low altitude during day and night while closely following a desired survey pattern provided improved data collection compared to divers and previous work with a small ROV. Over the course of the week long expedition, the AUV Sirius was deployed on 38 dives at three sites in the survey area and collected tens of thousands of stereo images. Of these, nearly a thousand were seen to contain cuttlefish during post cruise analysis, with a large proportion showing evidence of camouflage. The distribution of images containing cuttlefish suggest that the animal concentrations were substantially higher closer in to shore in shallow waters, where the flat rocky substrate occurs; females lay their eggs on the underside of these rocks. Results demonstrate the strengths of using an AUV for surveying near-shore benthic habitats of ecological interest, with a particular emphasis on the ability to operate during both day and night time operations.