Quantitative studies of animal colour constancy:using the chicken as a model

Colour constancy is the capacity of visual systems to keep colour perception constant despite changes in the illumination spectrum. Colour constancy has been tested extensively in humans and has also been described in many animals. In humans, colour constancy is often studied quantitatively, but besides humans, this has only been done for the goldfish and the honeybee. In this study, we quantified colour constancy in the chicken by training the birds in a colour discrimination task and testing them in changed illumination spectra to find the largest illumination change in which they were able to remain colour-constant. We used the receptor noise limited model for animal colour vision to quantify the illumination changes, and found that colour constancy performance depended on the difference between the colours used in the discrimination task, the training procedure and the time the chickens were allowed to adapt to a new illumination before making a choice. We analysed literature data on goldfish and honeybee colour constancy with the same method and found that chickens can compensate for larger illumination changes than both. We suggest that future studies on colour constancy in non-human animals could use a similar approach to allow for comparison between species and populations

Achromatic cues are important for flower visibility to hawkmoths and other insects

Studies on animal colour vision typically focus on the chromatic aspect of colour, which is related to the spectral distribution, and disregard the achromatic aspect, which is related to the intensity (“brightness”) of a stimulus. Although the chromatic component of vision is often most reliable for object recognition because it is fairly context independent, the achromatic component may provide a reliable signal under specific conditions, for example at night when light intensity is low. Here we make a case for the importance of achromatic cues in plant-pollinator signalling, based on experimental data on naïve Deilephila elpenor and Macroglossum stellatarum hawkmoths, optical modelling and synthesising published experiments on bees, flies, butterflies and moths. Our experiments show that in ecologically relevant light levels hawkmoths express a strong preference for brighter stimuli. Published experiments suggest that for flower-visiting bees, butterflies, moths and flies, achromatic cues may be more important for object detection than often considered. Our optical modelling enabled disentangling the contribution of pigments and scattering structures to the flower’s achromatic contrast, and illustrates how flower anatomy and background are important mediating factors. We discuss our findings in the context of the often-assumed dichotomy between detection and discrimination, chromatic versus achromatic vision, and the evolution of floral visual signals

The Absolute Threshold of Colour Vision in the Horse

Arrhythmic mammals are active both during day and night if they are allowed. The arrhythmic horses are in possession of one of the largest terrestrial animal eyes and the purpose of this study is to reveal whether their eye is sensitive enough to see colours at night. During the day horses are known to have dichromatic colour vision. To disclose whether they can discriminate colours in dim light a behavioural dual choice experiment was performed. We started the training and testing at daylight intensities and the horses continued to choose correctly at a high frequency down to light intensities corresponding to moonlight. One Shetland pony mare, was able to discriminate colours at 0.08 cd/m2, while a half blood gelding, still discriminated colours at 0.02 cd/m2. For comparison, the colour vision limit for several human subjects tested in the very same experiment was also 0.02 cd/m2. Hence, the threshold of colour vision for the horse that performed best was similar to that of the humans. The behavioural results are in line with calculations of the sensitivity of cone vision where the horse eye and human eye again are similar. The advantage of the large eye of the horse lies not in colour vision at night, but probably instead in achromatic tasks where presumably signal summation enhances sensitivity

Spatial summation improves bird color vision in low light intensities

Color guides many important behaviors in birds. Previously we have shown that the intensity threshold for color discrimination in the chicken depends on the color contrast between stimuli and their brightness. The birds could discriminate larger color contrasts and brighter colors in lower light intensities. We suggested that chickens use spatial summation of cone signals to maintain color vision in low light levels. Here we tested this hypothesis by determining the intensity thresholds of color discrimination using similar stimuli, patterns of grey tiles of varying intensity interspersed with color tiles, adjusted for this specific aim. Chickens could discriminate stimuli with a larger single color tile, or with a larger proportion of small color tiles, in lower light intensities. This is in agreement with the hypothesis that spatial summation improves color discrimination in low light levels. There was no difference in the intensity threshold for discrimination of stimuli with a single 6 × 6 mm color tile, stimuli with 30% colored tiles and stimuli in which color filled the whole pattern. This gives a first indication to the degree of spatial summation that can be performed. We compare this level of spatial summation to predictions from mathematical model calculations

The dual rod system of amphibians supports colour discrimination at the absolute visual threshold

The presence of two spectrally different kinds of rod photoreceptors in amphibians has been hypothesized to enable purely rod-based colour vision at very low light levels. The hypothesis has never been properly tested, so we performed three behavioural experiments at different light intensities with toads (Bufo) and frogs (Rana) to determine the thresholds for colour discrimination. The thresholds of toads were different in mate choice and prey-catching tasks, suggesting that the differential sensitivities of different spectral cone types as well as task-specific factors set limits for the use of colour in these behavioural contexts. In neither task was there any indication of rod-based colour discrimination. By contrast, frogs performing phototactic jumping were able to distinguish blue from green light down to the absolute visual threshold, where vision relies only on rod signals. The remarkable sensitivity of this mechanism comparing signals from the two spectrally different rod types approaches theoretical limits set by photon fluctuations and intrinsic noise. Together, the results indicate that different pathways are involved in processing colour cues depending on the ecological relevance of this information for each task. This article is part of the themed issue 'Vision in dim light'.Peer reviewe

Optics of cone photoreceptors in the chicken (Gallus gallus domesticus)

Vision is the primary sensory modality of birds, and its importance is evident in the sophistication of their visual systems. Coloured oil droplets in the cone photoreceptors represent an adaptation in the avian retina, acting as long-pass colour filters. However, we currently lack understanding of how the optical properties and morphology of component structures (e.g. oil droplet, mitochondrial ellipsoid and outer segment) of the cone photoreceptor influence the transmission of light into the outer segment and the ultimate effect they have on receptor sensitivity. In this study, we use data from microspectrophotometry, digital holographic microscopy and electron microscopy to inform electromagnetic models of avian cone photoreceptors to quantitatively investigate the integrated optical function of the cell. We find that pigmented oil droplets primarily function as spectral filters, not light collection devices, although the mitochondrial ellipsoid improves optical coupling between the inner segment and oil droplet. In contrast, unpigmented droplets found in violet-sensitive cones double sensitivity at its peak relative to other cone types. Oil droplets and ellipsoids both narrow the angular sensitivity of single cone photoreceptors, but not as strongly as those in human cones

Chromatic Signals Control Proboscis Movements during Hovering Flight in the Hummingbird Hawkmoth Macroglossum stellatarum

Most visual systems are more sensitive to luminance than to colour signals. Animals resolve finer spatial detail and temporal changes through achromatic signals than through chromatic ones. Probably, this explains that detection of small, distant, or moving objects is typically mediated through achromatic signals. Macroglossum stellatarum are fast flying nectarivorous hawkmoths that inspect flowers with their long proboscis while hovering. They can visually control this behaviour using floral markings known as nectar guides. Here, we investigate whether this is mediated by chromatic or achromatic cues. We evaluated proboscis placement, foraging efficiency, and inspection learning of naïve moths foraging on flower models with coloured markings that offered either chromatic, achromatic or both contrasts. Hummingbird hawkmoths could use either achromatic or chromatic signals to inspect models while hovering. We identified three, apparently independent, components controlling proboscis placement: After initial contact, 1) moths directed their probing towards the yellow colour irrespectively of luminance signals, suggesting a dominant role of chromatic signals; and 2) moths tended to probe mainly on the brighter areas of models that offered only achromatic signals. 3) During the establishment of the first contact, naïve moths showed a tendency to direct their proboscis towards the small floral marks independent of their colour or luminance. Moths learned to find nectar faster, but their foraging efficiency depended on the flower model they foraged on. Our results imply that M. stellatarum can perceive small patterns through colour vision. We discuss how the different informational contents of chromatic and luminance signals can be significant for the control of flower inspection, and visually guided behaviours in general

Complementary shifts in photoreceptor spectral tuning unlock the full adaptive potential of ultraviolet vision in birds

Color vision in birds is mediated by four types of cone photoreceptors whose maximal sensitivities (λmax) are evenly spaced across the light spectrum. In the course of avian evolution, the λmax of the most shortwave-sensitive cone, SWS1, has switched between violet (λmax > 400 nm) and ultraviolet (λmax < 380 nm) multiple times. This shift of the SWS1 opsin is accompanied by a corresponding short-wavelength shift in the spectrally adjacent SWS2 cone. Here, we show that SWS2 cone spectral tuning is mediated by modulating the ratio of two apocarotenoids, galloxanthin and 11',12'-dihydrogalloxanthin, which act as intracellular spectral filters in this cell type. We propose an enzymatic pathway that mediates the differential production of these apocarotenoids in the avian retina, and we use color vision modeling to demonstrate how correlated evolution of spectral tuning is necessary to achieve even sampling of the light spectrum and thereby maintain near-optimal color discrimination