No abstract

Birds have impressive physiological adaptations for colour vision, including tetrachromacy and coloured oil droplets, yet it is not clear exactly how well birds can discriminate the reflecting object colours that they encounter in nature. With behavioural experiments, we determined colour discrimination thresholds of chickens in bright and dim light. We performed the experiments with two colour series, orange and green, covering two parts of chicken colour space. These experiments allowed us to compare behavioural results with model expectations and determine how different noise types limit colour discrimination. At intensities ranging from bright light to those corresponding to early dusk (250-10 cd m −2 ), we describe thresholds accurately by assuming a constant signal-to-noise ratio, in agreement with an invariant Weber fraction of Weber's law. Below this intensity, signal-to-noise ratio decreases and Weber's law is violated because photon-shot noise limits colour discrimination. In very dim light (below 0.05 cd m −2 for the orange series or 0.2 cd m −2 for the green series) colour discrimination is possibly constrained by dark noise, and the lowest intensity at which chickens can discriminate colours is 0.025 and 0.08 cd m −2 for the orange and green series, respectively. Our results suggest that chickens use spatial pooling of cone outputs to mitigate photon-shot noise. Surprisingly, we found no difference between colour discrimination of chickens and humans tested with the same test in bright light.

Ultraviolet (UV)-sensitive visual pigments are widespread in the animal kingdom but many animals, for example primates, block UV light from reaching their retina by pigmented lenses. Birds have UV-sensitive (UVS) visual pigments with sensitivity maxima around 360–373 nm (UVS) or 402–426 nm (violet-sensitive, VS). We describe how these pigments are matched by the ocular media transmittance in 38 bird species. Birds with UVS pigments have ocular media that transmit more UV light (wavelength of 50% transmittance, λT0.5, 323 nm) than birds with VS pigments (λT0.5, 358 nm). Yet, visual models predict that colour discrimination in bright light is mostly dependent on the visual pigment (UVS or VS) and little on the ocular media. We hypothesize that the precise spectral tuning of the ocular media is mostly relevant for detecting weak UV signals, e.g. in dim hollow-nests of passerines and parrots. The correlation between eye size and UV transparency of the ocular media suggests little or no lens pigmentation. Therefore, only small birds gain the full advantage from shifting pigment sensitivity from VS to UVS. On the other hand, some birds with VS pigments have unexpectedly low UV transmission of the ocular media, probably because of UV blocking lens pigmentation.

Bird colour vision is mediated by single cones, while double cones and rods mediate luminance vision in bright and dim light, respectively. In daylight conditions, birds use colour vision to discriminate large objects such as fruit and plumage patches, and luminance vision to detect fine spatial detail and motion. However, decreasing light intensity favours achromatic mechanisms and eventually, in dim light, luminance vision outperforms colour vision in all visual tasks. We have used behavioural tests in budgerigars (Melopsittacus undulatus) to investigate how single cones, double cones and rods contribute to spectral sensitivity for large (3.4°) static monochromatic stimuli at light intensities ranging from 0.08 to 63.5 cd/m². We found no influences of rods at any intensity level. Single cones dominate the spectral sensitivity function at intensities above 1.1 cd/m², as predicted by a receptor noise-limited colour discrimination model. Below 1.1 cd/m², spectral sensitivity is lower than expected at all wavelengths except 575 nm, which corresponds to double cone function. We suggest that luminance vision mediated by double cones restores visual sensitivity when single cone sensitivity quickly decreases at light intensities close to the absolute threshold of colour vision.

Colour vision models require measurement of receptor noise and the absorbance of visual pigments, oil droplets, and ocular media. We have studied how variation in these parameters influences colour matching, spectral sensitivity, and colour discrimination predictions in four bird species. While colour match predictions are sensitive to variation in visual pigment and oil droplet absorbance data, discrimination predictions are mostly sensitive to variation in receptor noise. Ocular media transmittance influences only modelled spectral sensitivities at short wavelengths. A comparison between predicted and measured spectral sensitivities in domestic fowl and duck revealed large discrepancies, likely because of influences from achromatic mechanisms.

Birds are assumed to use half of their cones (double cones) to detect fine spatial detail while their other half (single cones) is used for color vision. However, the spatial resolution of the color pathway in birds has never been studied. We determined the spatial contrast sensitivity to achromatic and isoluminant red-green and blue-green color gratings in budgerigars (Melopsittacus undulatus). Contrast sensitivity to achromatic gratings has band-pass characteristics while that for red-green and blue-green gratings has low-pass properties. Maximum sensitivity is lower to blue-green than to red-green gratings and the acuity for both color gratings is less than half (ca. 4.5 cycles/degree) of that for achromatic gratings (ca. 10 cycles/degree). This suggests that achromatic vision in birds, as in humans and bees, is tuned for detecting fine detail while chromatic vision is tuned for viewing larger fields. Similar to humans, blue-sensitive cones contribute little to spatial vision. Moreover, budgerigars detected gratings having both achromatic and chromatic contrasts more reliably at high spatial frequencies than gratings with either of these contrasts, suggesting that the single and double cone pathways are incompletely separated. The study demonstrates the importance of the spatial dimension of color vision; fine patterns remain unresolved even if they present large color contrasts.

SUMMARY Raptors have excellent vision, yet it is unclear how they use colour information. It has been suggested that raptors use ultraviolet (UV) reflections from vole urine to find good hunting grounds. In contrast, UV plumage colours in songbirds such as blue tits are assumed to be ‘hidden’ communication signals, inconspicuous to raptors. This ambiguity results from a lack of knowledge about raptor ocular media transmittance, which sets the limit for UV sensitivity. We measured ocular media transmittance in common buzzards (Buteo buteo), sparrowhawks (Accipiter nisus), red kites (Milvus milvus) and kestrels (Falco tinnunculus) so that, for the first time, raptor UV sensitivity can be fully described. With this information, and new measurements of vole urine reflectance, we show that (i) vole urine is unlikely to provide a reliable visual signal to hunting raptors and (ii) blue tit plumage colours are more contrasting to blue tits than to sparrowhawks because of UV reflectance. However, as the difference between blue tit and sparrowhawk vision is subtle, we suggest that behavioural data are needed to fully resolve this issue. UV cues are of little or no importance to raptors in both vole and songbird interactions and the role of colour vision in raptor foraging remains unclear.

SUMMARY We have used behavioural tests to determine the intensity thresholds of colour vision in Bourke's parrots (Neopsephotus bourkii) and budgerigars (Melopsittacus undulatus). We have also examined the relationship between these thresholds and the optical sensitivities of single photoreceptors using morphological methods. Bourke's parrots lose colour vision in brighter light (0.4 cd m–2) than budgerigars (0.1 cd m–2) and both birds lose colour vision in brighter light(`end of civil twilight') than humans (0.02 cd m–2,`moonlight'). The optical sensitivities of single cones are similar in both birds (budgerigar 0.27 μm2 sr, Bourke's parrot 0.25μm2 sr) but Bourke's parrots have more (cone to rod ratio,1.2:1.0), thinner (2.8 μm) and longer rods (18.5 μm) than budgerigars(2.1:1.0, 3.4 μm, 13.3 μm). Bourke's parrots thus have an eye type that,with a flexible pooling mechanism, allows for high resolution or high absolute sensitivity depending on the light conditions. The results nicely agree with the activity patterns of the birds, Bourke's parrots being active during the day and in twilight while budgerigars are not normally active before sunrise and after sunset. However, Bourke's parrots have fewer cones than budgerigars,which implies that a smaller number of cones are pooled within each retinal integration area. That could explain why Bourke's parrots have a higher intensity threshold of colour vision than budgerigars. Furthermore, the study emphasises the need to expand the sensitivity measure so that photoreceptor integration units are used rather than single receptors.