Colour discrimination thresholds vary throughout colour space in a reef fish (Rhinecanthus aculeatus).

Animals use colour vision in a range of behaviours. Visual performance is limited by thresholds, which are set by noise in photoreceptors and subsequent neural processing. The receptor noise limited (RNL) model of colour discrimination is widely used for modelling colour vision and accounts well for experimental data from many species. In one of the most comprehensive tests yet of colour discrimination in a non-human species, we used Ishihara-style stimulus patterns to examine thresholds for 21 directions at five locations in colour space for the fish Rhinecanthus aculeatus. Thresholds matched RNL model predictions most closely for stimuli near the achromatic point, but exceeded predictions (indicating a decline in sensitivity) with distance from this point. Thresholds were also usually higher for saturation than for hue differences. These changes in colour threshold with colour space location and direction may give insight into photoreceptor non-linearities and post-receptoral mechanisms of colour vision in fish. Our results highlight the need for a cautious interpretation of the RNL model - especially for modelling colours that differ from one another in saturation (rather than hue), and for highly saturated colours distant from the achromatic point in colour space.

An Ishihara-style test of animal colour vision.

Colour vision mediates ecologically relevant tasks for many animals, such as mate choice, foraging and predator avoidance. However, our understanding of animal colour perception is largely derived from human psychophysics, and behavioural tests of non-human animals are required to understand how colour signals are perceived. Here, we introduce a novel test of colour vision in animals inspired by the Ishihara colour charts, which are widely used to identify human colour deficiencies. In our method, distractor dots have a fixed chromaticity (hue and saturation) but vary in luminance. Animals can be trained to find single target dots that differ from distractor dots in chromaticity. We provide MATLAB code for creating these stimuli, which can be modified for use with different animals. We demonstrate the success of this method with triggerfish, Rhinecanthus aculeatus, which quickly learnt to select target dots that differed from distractor dots, and highlight behavioural parameters that can be measured, including success of finding the target dot, time to detection and error rate. We calculated discrimination thresholds by testing whether target colours that were of increasing colour distances (ΔS) from distractor dots could be detected, and calculated discrimination thresholds in different directions of colour space. At least for some colours, thresholds indicated better discrimination than expected from the receptor noise limited (RNL) model assuming 5% Weber fraction for the long-wavelength cone. This methodology could be used with other animals to address questions such as luminance thresholds, sensory bias, effects of sensory noise, colour categorization and saliency.

Contrast sensitivity and behavioural evidence for lateral inhibition in octopus.

Behavioural contrast sensitivity in Octopus tetricus was measured in the range of 0.05-12 cycles per degree (cpd) using a fixation reflex. We show that the contrast sensitivity reaches its maximum (between 1 and 4%) at 0.3 cpd, and decreases to approximately half of the maximum value at the lowest spatial frequency. Reduction of sensitivity at low spatial frequency is a signature of lateral inhibition in visual systems. In vertebrates and insects, lateral inhibition helps to overcome the bottleneck of encoding information into spikes. In octopus, photoreceptors generate spikes themselves and are directly connected to the brain through their axons. Therefore, the neural processing occurring in the octopus brain cannot help overcome the bottleneck of encoding information into spikes. We conclude that, in octopus, either the lateral inhibition occurs in the brain after information has been encoded into spikes, or photoreceptors inhibit each other. This is the first time behavioural contrast sensitivity has been measured in a cephalopod.

Unexpectedly low UV-sensitivity in a bird, the budgerigar.

Photoreceptor adaptation ensures appropriate visual responses during changing light conditions and contributes to colour constancy. We used behavioural tests to compare UV-sensitivity of budgerigars after adaptation to UV-rich and UV-poor backgrounds. In the latter case, we found lower UV-sensitivity than expected, which could be the result of photon-shot noise corrupting cone signal robustness or nonlinear background adaptation. We suggest that nonlinear adaptation may be necessary for allowing cones to discriminate UV-rich signals, such as bird plumage colours, against UV-poor natural backgrounds.

Visual acuity in a species of coral reef fish: Rhinecanthus aculeatus.

Coral reef fish present the human observer with an array of bold and contrasting patterns; however, the ability of such fish to perceive these patterns is largely unexamined. To understand this, the visual acuity of these animals - the degree to which they can resolve fine detail - must be ascertained. Behavioural studies are few in number and anatomical analysis has largely focused on estimates of ganglion cell density to predict the visual acuity in coral reef fish. Here, we report visual acuity measures for the triggerfish Rhinecanthus aculeatus. Acuity was first assessed using a series of behavioural paradigms and the figures were then contrasted with those obtained anatomically, based on photoreceptor and ganglion cell counts. Behavioural testing indicated an upper behavioural acuity of 1.75 cycles·degree(-1), which is approximately the same level of acuity as that of the goldfish (Carassiusauratus). Anatomical estimates were then calculated from wholemount analysis of the photoreceptor layer and Nissl staining of cells within the ganglion cell layer. Both of these anatomical measures gave estimates that were substantially larger (7.75 and 3.4 cycles·degree(-1) for the photoreceptor cells and ganglion cells, respectively) than the level of acuity indicated by the behavioural tests. This indicates that in this teleost species spatial resolution is poor compared to humans (30-70 cycles·degree(-1)) and it is also not well indicated by anatomical estimates.

Depolymerization of actin facilitates memory formation in an insect.

In mammals, memory formation and stabilization requires polymerization of actin. Here, we show that, in the honeybee, inhibition of actin polymerization within the brain centres involved in memory formation, the mushroom bodies (MBs), enhances associative olfactory memory. Local application of inhibitors of actin polymerization (Cytochalasin D or Latrunculin A) to the MBs 1 h before induction of long-term memory increased memory retention 2 and 24 h after the onset of training. Post-training application of Cytochalasin D also enhanced retention, indicating that memory consolidation is facilitated by actin depolymerization. We conclude that certain aspects of memory mechanisms could have been established independently in mammals and insects.

Angular dependence of polarisation contrast sensitivity in octopus.

Cephalopod photoreceptors are polarisation-sensitive, giving them an ability to discriminate between lights of different angle and degree of polarisation. While colour vision is achieved by comparison of signals of photoreceptors tuned to different parts of light spectra, polarisation vision is achieved by comparison of signals of photoreceptors tuned to different orientations of e-vector. Therefore, from a theoretical point of view, polarisation vision is similar to colour vision. In particular, detection of polarised light against an unpolarised background is analogous to detection of chromatic light against grey. The dependence of polarisation contrast sensitivity on the angle of polarisation can be theoretically predicted using a receptor noise limited model in much the same way as it has been done for predicting the shape of the increment threshold spectral sensitivity in animals with colour vision. Here we report angular dependence of polarisation contrast sensitivity in octopus (O. tetricus, Gould 1852) and compare the theoretical predictions of polarisation contrast with the experimental results. Polarisation gratings were generated using LCD screens with removed polarisers and the orientation of polarisation was changed by rotating the screen. Reaction to the stimulus was recorded using a fixation reflex. We show that, in agreement with the theoretical predictions, the maximum contrast sensitivity is achieved at horizontal and vertical orientations of polarisation. Our results demonstrate that the dependence of polarisation contrast sensitivity on the angle of polarisation can be analysed in the same way as the dependence of colour thresholds on wavelength of monochromatic light added to a grey background.

The Colours of Octopus: Using Spectral Data to Measure Octopus Camouflage.

No animal can so effectively camouflage in such a wide range of environments as the octopus. Thanks to their highly malleable skin, they are capable of adapting their body patterns to the brightness and texture of their immediate environment, and they often seemingly match the colour of background objects. However, octopuses are colour-blind as their eyes have only one type of visual pigment. Therefore, chromatophores in their skin are likely to respond to changes in brightness, not chromaticity. To determine whether octopuses actually match background colours, we used a SpectraScan® PR-655 spectroradiometer to measure the reflectance spectra of Octopus tetricus skin in captivity. The spectra were compared with those of green algae, brown algae, and sponges-all of these being colourful objects commonly found in the octopus's natural environment. Even though we show that octopuses change both lightness and chromaticity, allowing them to potentially camouflage in a wide range of backgrounds in an effective manner, the overall octopus colours did not reach the same level of saturation compared to some background objects. Spectra were then modelled under the visual systems of four potential octopus predators: one dichromatic fish (Heller's barracuda), two trichromatic fish (blue-spotted stingray and two-spotted red snapper), and one tetrachromatic bird (wedge-tailed shearwater). We show that octopuses are able to match certain background colours for some visual systems. How a colour-blind animal is capable of colour-matching is still unknown.

The role of colour patterns for the recognition of flowers by bees.

Bees discriminate between many different colours of flower petals, but it is not well understood how they perceive and learn patterns frequently found in flowers with colourful structures. We used multi-spectral imaging to explore chromatic cues in concentric flower patterns as they are seen through the low-resolution eyes of the honeybee. We find a diversity of colour combinations, which suggests that plants might exploit the sensory capabilities of pollinators, like bees, that learn colours easily. A consistent feature is that the surround of the pattern has a stronger chromatic contrast to the foliage background than the centre. This can potentially facilitate the fast identification of floral objects within colourful scenes when a foraging bee moves through a flower patch. In behavioural experiments we trained and tested bees with three types of concentric patterns. They recognized and discriminated patterns accurately in most tests, relying flexibly on both chromatic and spatial cues. Only rarely, depending on the training stimulus, chromatic cues determined their choices whilst pattern cues were ignored. The variability of floral designs and the bees' flexibility in recalling colour and spatial information suggest a role for colour vision in pattern processing. Implications for the signalling strategies of flowers are discussed. This article is part of the theme issue 'Understanding colour vision: molecular, physiological, neuronal and behavioural studies in arthropods'.

Selected ocular dimensions of three penguin species.

Penguins (Spheniscidae) are a diverse clade of flightless, marine birds. Their eyes, likely a primary driver of behaviour, have been noted to have anatomic adaptations to their amphibious lifestyle. In particular, they have a relatively flat cornea, which would make the transition from a subaerial to a submarine environment require less accommodative effort. However, the ocular dimensions are not known for many penguin species, despite the diversity within the family, and their accommodative abilities have been the source of some dispute. In this study we undertook to establish the basic dimensions of the eye of the smallest, a mid-sized penguin and the second largest penguin. The power of the front surface of the cornea was inversely related to the size of both the eye and penguin, being 41.3 D in the little penguin (Eudyptula minor), a power greater than previously measured in any other penguin species, 26.3 D in the gentoo (Pygoscelis papua) and 19.1 D in the king penguin (Aptenodytes patagonicus). All other dimensions increased or decreased in line with the size of the eye. All penguins were able to achieve emmetropia in air. The gentoo appeared to be emmetropic underwater. A finding of central corneal thickening in some penguins may be artefactual. Calculations using the ocular dimensions demonstrated that the mean retinal illumination of an extended source of light in the little penguin eye is less than that of its larger, deeper-diving relatives.

Approach Direction Prior to Landing Explains Patterns of Colour Learning in Bees.

Gaze direction is closely coupled with body movement in insects and other animals. If movement patterns interfere with the acquisition of visual information, insects can actively adjust them to seek relevant cues. Alternatively, where multiple visual cues are available, an insect's movements may influence how it perceives a scene. We show that the way a foraging bumblebee approaches a floral pattern could determine what it learns about the pattern. When trained to vertical bicoloured patterns, bumblebees consistently approached from below centre in order to land in the centre of the target where the reward was located. In subsequent tests, the bees preferred the colour of the lower half of the pattern that they predominantly faced during the approach and landing sequence. A predicted change of learning outcomes occurred when the contrast line was moved up or down off-centre: learned preferences again reflected relative frontal exposure to each colour during the approach, independent of the overall ratio of colours. This mechanism may underpin learning strategies in both simple and complex visual discriminations, highlighting that morphology and action patterns determines how animals solve sensory learning tasks. The deterministic effect of movement on visual learning may have substantially influenced the evolution of floral signals, particularly where plants depend on fine-scaled movements of pollinators on flowers.

Double cones are used for colour discrimination in the reef fish, Rhinecanthus aculeatus.

Double cones (DCs) are the most common cone types in fish, reptiles and birds. It has been suggested that DCs are used for achromatic tasks such as luminance, motion and polarization vision. Here we show that a reef fish Rhinecanthus aculeatus can discriminate colours on the basis of the difference between the signals of individual members of DCs. This is the first direct evidence that individual members of DCs are used in colour vision as independent spectral channels.

Numerical modeling of light propagation in a hexagonal array of dielectric cylinders.

To model the light-guiding properties of a hexagonal array of dielectric cylinders, we have numerically solved Maxwell's equations with the finite-difference time-domain technique. The sizes and refractive indices of the cylinders are representative of those of the outer segments of the cone photoreceptors in the human central retina. In the array, light propagates predominantly as a "slow" mode, with a noticeable contribution of a "fast" mode, with the optical field localized in the intra- and inter-cylinder spaces, respectively. Interference between these modes leads to substantial (up to approximately 60%) axial oscillations in optical power within the cylinders. Our numerical model offered approximate dependence of the optical intensity distribution within the cylinders on their radii and separations.

Spatial Contrast Sensitivity to Polarization and Luminance in Octopus.

While color vision is achieved by comparison of signals of photoreceptors tuned to different parts of light spectra, polarization vision is achieved by comparison of signals of photoreceptors tuned to different orientations of the electric field component of visible light. Therefore, it has been suggested that polarization vision is similar to color vision. In most animals that have color vision, the shape of luminance contrast sensitivity curve differs from the shape of chromatic contrast sensitivity curve. While luminance contrast sensitivity typically decreases at low spatial frequency due to lateral inhibition, chromatic contrast sensitivity generally remains high at low spatial frequency. To find out if the processing of polarization signals is similar to the processing of chromatic signals, we measured the polarization and luminance contrast sensitivity dependence in a color-blind animal with well-developed polarization vision, Octopus tetricus. We demonstrate that, in Octopus tetricus, both luminance and polarization contrast sensitivity decrease at low spatial frequency and peak at the same spatial frequency (0.3 cpd). These results suggest that, in octopus, polarization and luminance signals are processed via similar pathways.

Enhanced UV-Reflection Facilitated a Shift in the Pollination System of the Red Poppy, Papaver rhoeas (Papaveraceae).

Evolutionary change is considered a major factor influencing the invasion of new habitats by plants. Yet, evidence on how such modifications promote range expansion remains rather limited. Here we investigated flower color modifications in the red poppy, Papaver rhoeas (Papaveraceae), as a result of its introduction into Central Europe and the impact of those modifications on its interactions with pollinators. We found that while flowers of Eastern Mediterranean poppies reflect exclusively in the red part of the spectrum, those of Central European poppies reflect both red and ultraviolet (UV) light. This change coincides with a shift from pollination by glaphyrid beetles (Glaphyridae) to bees. Glaphyrids have red-sensitive photoreceptors that are absent in bees, which therefore will not be attracted by colors of exclusively red-reflecting flowers. However, UV-reflecting flowers are easily detectable by bees, as revealed by visual modeling. In the North Mediterranean, flowers with low and high UV reflectance occur sympatrically. We hypothesize that Central European populations of P. rhoeas were initially polymorphic with respect to their flower color and that UV reflection drove a shift in the pollination system of P. rhoeas that facilitated its spread across Europe.

Flower patterns are adapted for detection by bees.

We have demonstrated previously that honeybees use brightness vision mediated by green (or L-) receptor to detect targets from a long distance. They detect circular targets having a dim, for the L-receptor, centre and bright surround from a longer distance than targets having bright centre and dim surround. Here we show that a majority of bee-pollinated flowers have a centre that, for the L-receptor, is dim with bright surround, i.e. have patterns that are easy for a bee to detect. Flowers with dim for the L-receptor surrounds tend to be larger than those with bright surrounds, indicating that flowers compensate for the impaired visibility of their patterns by increasing the size of their displays.

A contractile cochlear frame is a common feature of the hearing organs in Gekkota (sauria, Squamata): a comparative study.

Geckos are the most vocalizing animals among Squamata. Previously we discovered a contractile segment (the NAL, noncartilaginous abneural limbus), within the rigid periotic cochlear frame of the gecko Teratoscincus scincus [Ganeshina and Vorobyev, 2003]. Because this unusual cochlear specialization has not previously been described in the vertebrate hearing organs, we have hypothesized that the NAL has evolved within Gekkota as a specialization associated with vocalization and sound communication. Here we show that the NAL is present in ten other species belonging to four major Gekkota clades: Gekkoninae, Diplodactylinae, Eublepharinae and Pygopodidae. The NAL exhibits similar structural organization among the Gekkota species. It is composed of large, tightly packed cells enriched with a filamentous cytoskeleton and extensively interconnected via putative gap junctions. No relationship is found between the extent of development of the NAL and degree of vocalization. However, the species with relatively large body dimensions show larger absolute NAL area and structural peculiarities of the NAL that might affect its mechanical properties. A representative of the non-gekkonoid, non-vocalizing lizard, Pogona barbata (Iguania, Agamidae), possesses a similar cochlear specialization. This provides evidence that the NAL is not the exclusive feature of the Gekkota hearing organs. Our data are compatible with the hypothesis that the NAL appeared before the Gekkota separated from other Squamata groups as a mechanism involved in maintenance of the cochlear mechanical or ionic homeostasis.

Tetrachromacy in a butterfly that has eight varieties of spectral receptors.

This paper presents the first evidence of tetrachromacy among invertebrates. The Japanese yellow swallowtail butterfly, Papilio xuthus, uses colour vision when foraging. The retina of Papilio is furnished with eight varieties of spectral receptors of six classes that are the ultraviolet (UV), violet, blue (narrow-band and wide-band), green (single-peaked and double-peaked), red and broad-band classes. We investigated whether all of the spectral receptors are involved in colour vision by measuring the wavelength discrimination ability of foraging Papilio. We trained Papilio to take nectar while seeing a certain monochromatic light. We then let the trained Papilio choose between two lights of different wavelengths and determined the minimum discriminable wavelength difference Deltalambda. The Deltalambda function of Papilio has three minima at approximately 430, 480 and 560nm, where the Deltalambda values approximately 1nm. This is the smallest value found for wavelength discrimination so far, including that of humans. The profile of the Deltalambda function of Papilio can be best reproduced by postulating that the UV, blue (narrow-band and wide-band), green (double-peaked) and red classes are involved in foraging. Papilio colour vision is therefore tetrachromatic.

Visual ecology of the Australian lungfish (Neoceratodus forsteri).

BACKGROUND: The transition from water to land was a key event in the evolution of vertebrates that occurred over a period of 15-20 million years towards the end of the Devonian. Tetrapods, including all land-living vertebrates, are thought to have evolved from lobe-finned (sarcopterygian) fish that developed adaptations for an amphibious existence. However, while many of the biomechanical and physiological modifications necessary to achieve this feat have been studied in detail, little is known about the sensory adaptations accompanying this transition. In this study, we investigated the visual system and visual ecology of the Australian lungfish Neoceratodus forsteri, which is the most primitive of all the lungfish and possibly the closest living relative to the ancestors of tetrapods. RESULTS: Juvenile Neoceratodus have five spectrally distinct retinal visual pigments. A single type of rod photoreceptor contains a visual pigment with a wavelength of maximum absorbance (lambdamax) at 540 nm. Four spectrally distinct single cone photoreceptors contain visual pigments with lambdamax at 366 (UVS), 479 (SWS), 558 (MWS) and 623 nm (LWS). No double cones were found. Adult lungfish do not possess UVS cones and, unlike juveniles, have ocular media that prevent ultraviolet light from reaching the retina. Yellow ellipsoidal/paraboloidal pigments in the MWS cones and red oil droplets in the LWS cones narrow the spectral sensitivity functions of these photoreceptors and shift their peak sensitivity to 584 nm and 656 nm, respectively. Modelling of the effects of these intracellular spectral filters on the photoreceptor colour space of Neoceratodus suggests that they enhance their ability to discriminate objects, such as plants and other lungfishes, on the basis of colour. CONCLUSION: The presence of a complex colour vision system based on multiple cone types and intracellular spectral filters in lungfishes suggests that many of the ocular characteristics seen in terrestrial or secondarily aquatic vertebrates, such as birds and turtles, may have evolved in shallow water prior to the transition onto land. Moreover, the benefits of spectral filters for colour discrimination apply equally to purely aquatic species as well as semi-aquatic and terrestrial animals. The visual system of the Australian lungfish resembles that of terrestrial vertebrates far more closely than that of other sarcopterygian fish. This supports the idea that lungfishes, and not the coelacanth, are the closest living relatives of the ancestors of tetrapods.

Are fruit colors adapted to consumer vision and birds equally efficient in detecting colorful signals?

Reproduction in plants often requires animal vectors. Fruit and flower colors are traditionally viewed as an adaptation to facilitate detection for pollinators and seed dispersers. This longstanding hypothesis predicts that fruits are easier to detect against their own leaves compared with those of different species. We tested this hypothesis by analyzing the chromatic contrasts between 130 bird-dispersed fruits and their respective backgrounds according to avian vision. From a bird's view, fruits are not more contrasting to their own background than to those of other plant species. Fruit colors are therefore not adapted toward maximized conspicuousness for avian seed dispersers. However, secondary structures associated with fruit displays increase their contrasts. We used fruit colors to assess whether the ultraviolet and violet types of avian visual systems are equally efficient in detecting color signals. In bright light, the chromatic contrasts between fruit and background are stronger for ultraviolet vision. This advantage is due to the lesser overlap in spectral sensitivities of the blue and ultraviolet cones, which disappears in dim light conditions. We suggest that passerines with ultraviolet cones might primarily use epigamic signals that are less conspicuous to their avian predators (presumably with violet vision). Possible examples for such signals are carotenoid-based signals.