Olle Lind

Avian colour vision: Effects of variation in receptor sensitivity and noise data on model predictions as compared to behavioural results

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.

Bird colour vision: behavioural thresholds reveal receptor noise.

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 Webers law. Below this intensity, signal-to-noise ratio decreases and Webers law is violated because photon-shot noise limits colour discrimination. In very dim light (below 0.05cd 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 vision in birds: the importance of transparent eye media

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.

The spatial tuning of achromatic and chromatic vision in budgerigars.

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.

Ultraviolet sensitivity and colour vision in raptor foraging

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.

Limits of colour vision in dim light

Humans and most vertebrates have duplex retinae with multiple cone types for colour vision in bright light, and one single rod type for achromatic vision in dim light. Instead of comparing signals from multiple spectral types of photoreceptors, such species use one highly sensitive receptor type thus improving the signal‐to‐noise ratio at night. However, the nocturnal hawkmoth Deilephila elpenor, the nocturnal bee Xylocopa tranquebarica and the nocturnal gecko Tarentola chazaliae can discriminate colours at extremely dim light intensities. To be able to do so, they sacrifice spatial and temporal resolution in favour of colour vision. We review what is known about colour vision in dim light, and compare colour vision thresholds with the optical sensitivity of the photoreceptors in selected animal species with lens and compound eyes.

Chromatic and achromatic vision: parameter choice and limitations for reliable model predictions

Many animals use vision to detect, discriminate, or recognize important objects such as prey, predators, homes, or mates. These objects may differ in color and brightness-having chromatic and achromatic contrast to the background or to other objects. Visual models are powerful tools to investigate contrast detection, but need to be calibrated by experimental data to provide robust predictions. The most critical parameter of current models-receptor noise-is usually estimated from a small number of behavioral tests on chromatic contrast thresholds, while equivalent tests of achromatic thresholds in a wide range of animals have often been ignored. We suggest that both chromatic and achromatic contrasts in studies of visual ecology should be examined using calibrated model parameters, and we provide a compilation of what is currently known on visual thresholds and corresponding noise estimates. Besides the need for careful parameter estimation, we discuss how the robustness of model predictions depends on assumptions about overall light intensity, background color and brightness, object size, and behavioral context. (Less)

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. DOI: http://dx.doi.org/10.7554/eLife.15675.001

Brightness discrimination in budgerigars (Melopsittacus undulatus).

Birds have excellent spatial acuity and colour vision compared to other vertebrates while spatial contrast sensitivity is relatively poor for unknown reasons. Contrast sensitivity describes the detection of gratings of varying spatial frequency. It is unclear whether bird brightness discrimination between large uniform fields is poor as well. Here we show that budgerigars (Melopsittacus undulatus) need a Michelson contrast of 0.09 to discriminate between large spatially separated achromatic fields in bright light conditions. This is similar to the peak contrast sensitivity of 10.2 (0.098 Michelson contrast) for achromatic grating stimuli established in earlier studies. The brightness discrimination threshold described in Weber fractions is 0.18, which is modest compared to other vertebrates.

Visual modelling suggests a weak relationship between the evolution of ultraviolet vision and plumage coloration in birds

Birds have sophisticated colour vision mediated by four cone types that cover a wide visual spectrum including ultraviolet (UV) wavelengths. Many birds have modest UV sensitivity provided by violet‐sensitive (VS) cones with sensitivity maxima between 400 and 425 nm. However, some birds have evolved higher UV sensitivity and a larger visual spectrum given by UV‐sensitive (UVS) cones maximally sensitive at 360–370 nm. The reasons for VS–UVS transitions and their relationship to visual ecology remain unclear. It has been hypothesized that the evolution of UVS‐cone vision is linked to plumage colours so that visual sensitivity and feather coloration are ‘matched’. This leads to the specific prediction that UVS‐cone vision enhances the discrimination of plumage colours of UVS birds while such an advantage is absent or less pronounced for VS‐bird coloration. We test this hypothesis using knowledge of the complex distribution of UVS cones among birds combined with mathematical modelling of colour discrimination during different viewing conditions. We find no support for the hypothesis, which, combined with previous studies, suggests only a weak relationship between UVS‐cone vision and plumage colour evolution. Instead, we suggest that UVS‐cone vision generally favours colour discrimination, which creates a nonspecific selection pressure for the evolution of UVS cones.