Fast visual adaptation to dim light in a cavity-nesting bird.

Many birds move fast into dark nest cavities forcing the visual system to adapt to low light intensities. Their visual system takes between 15 and 60 min for complete dark adaptation, but little is known about the visual performance of birds during the first seconds in low light intensities. In a forced two-choice behavioural experiment we studied how well budgerigars can discriminate stimuli of different luminance directly after entering a darker environment. The birds made their choices within about 1 s and did not wait to adapt their visual system to the low light intensities. When moving from a bright facility into an environment with 0.5 log unit lower illuminance, the budgerigars detected targets with a luminance of 0.825 cd m-2 on a black background. When moving into an environment with 1.7 or 3.5 log units lower illuminance, they detected targets with luminances between 0.106 and 0.136 cd m-2. In tests with two simultaneously displayed targets, the birds discriminated similar luminance differences between the targets (Weber fraction of 0.41-0.54) in all light levels. Our results support the notion that partial adaptation of bird eyes to the lower illumination occurring within 1 s allows them to safely detect and feed their chicks.

Lens and cornea limit UV vision of birds - a phylogenetic perspective.

Most vertebrates have UV-sensitive vision, but the UV sensitivity of their eyes is limited by the transmittance of the ocular media, and the specific contribution of the different media (cornea, lens) has remained unclear. Here, we describe the transmittance of all ocular media (OMT), as well as that of lenses and corneas of birds. For 66 species belonging to 18 orders, the wavelength at which 50% of light is transmitted through the ocular media to the retina (λT0.5) ranges from 310 to 398 nm. Low λT0.5 corresponds to more UV light transmitted. Corneal λT0.5 varies only between 300 and 345 nm, whereas lens λT0.5 values are more variable (between 315 and 400 nm) and tend to be the limiting factor, determining OMT in the majority of species. OMT λT0.5 is positively correlated with eye size, but λT0.5 of corneas and lenses are not correlated with their thickness when controlled for phylogeny. Corneal and lens transmittances do not differ between birds with UV- and violet-sensitive SWS1 opsin when controlling for eye size and phylogeny. Phylogenetic relatedness is a strong predictor of OMT, and ancestral state reconstructions suggest that from ancestral intermediate OMT, highly UV-transparent ocular media (low λT0.5) evolved at least five times in our sample of birds. Some birds have evolved in the opposite direction towards a more UV-opaque lens, possibly owing to pigmentation, likely to mitigate UV damage or reduce chromatic aberration.

Chicken colour discrimination depends on background colour.

How well can a bird discriminate between two red berries on a green background? The absolute threshold of colour discrimination is set by photoreceptor noise, but animals do not perform at this threshold; their performance can depend on additional factors. In humans and zebra finches, discrimination thresholds for colour stimuli depend on background colour, and thus the adaptive state of the visual system. We have tested how well chickens can discriminate shades of orange or green presented on orange or green backgrounds. Chickens discriminated slightly smaller colour differences between two stimuli presented on a similarly coloured background, compared with a background of very different colour. The slope of the psychometric function was steeper when stimulus and background colours were similar but shallower when they differed markedly, indicating that background colour affects the certainty with which the animals discriminate the colours. The effect we find for chickens is smaller than that shown for zebra finches. We modelled the response to stimuli using Bayesian and maximum likelihood estimation and implemented the psychometric function to estimate the effect size. We found that the result is independent of the psychophysical method used to evaluate the effect of experimental conditions on choice performance.

Use of the effluent from biogas production for cultivation of Spirulina.

The effluent from the biogas process was tested as a nutrient source during cultivation of the protein-rich and edible microalgae Spirulina (Arthrospira platensis) and compared with conventional Spirulina medium. Equal biomass production was observed until late exponential phase and no significant differences could be observed between the treatments in protein amount, amino acid composition, and total lipid concentration. The concentration of the pigment phycocyanin differed significantly between Spirulina medium and the effluent-based medium (63.3 ± 11.7 and 86.2 ± 1.9 mg g-1, respectively). Slightly higher concentrations of saturated fatty acids, mainly palmitic acid, were observed in the biomass produced in Spirulina medium than in that produced in the effluent-based medium. In the biomass produced in the effluent-based medium, the cadmium concentration was 0.07 ± 0.05 mg kg-1 of dry weight, whereas it was below the detection limit in the biomass produced in Spirulina medium. There is a need to identify new food and feed resources and a possible future scenario is to integrate Spirulina production into the biogas plant for protein production as it contains more than 60% of protein on dry weight basis. In that scenario, it is important to control heavy metal concentrations in the biogas slurry fed to Spirulina.

Change of ultraviolet light transmittance in growing chicken and quail eyes.

The ocular media transmittance (OMT), the amount of light transmitted by the ocular media (the cornea, aqueous humour, lens and vitreous humour) to the retina, determines the sensitivity of vertebrate eyes to short-wavelength light, such as ultraviolet (UV). Earlier, we have measured the OMT of adult birds from a range of species and found that smaller eyes transmitted more UV-light to the retina than larger eyes. In the current study we measured OMT during post-hatch development in Japanese quails and domestic chickens. We show that in both species, OMT decreases as the eye size increases similarly to that what was found across various species, but that quails have lower OMT than expected from eye size. In both species, lens transmittance decreases linearly with lens thickness suggesting that UV-transmittance through the lenses is not actively controlled, but instead determined by UV-absorbance and scattering that occur in all biological tissues. Contrary to earlier assumptions of high cornea transmittance, we found that cornea transmittance is more variable, substantially influencing whole eye transmittance in all age groups of quail and in young chickens. It seems that additional absorbing pigments are used to more actively control cornea transmittance and thereby also overall OMT.

No response to linear polarization cues in operant conditioning experiments with zebra finches.

Many animals can use the polarization of light in various behavioural contexts. Birds are well known to use information from the skylight polarization pattern for orientation and compass calibration. However, there are few controlled studies of polarization vision in birds, and the majority of them have not been successful in convincingly demonstrating polarization vision. We used a two-alternative forced choice conditioning approach to assess linear polarization vision in male zebra finches in the 'visible' spectral range (wavelengths >400 nm). The birds were trained to discriminate colour, brightness and polarization stimuli presented on either one of two LCD-screens. All birds were able to discriminate the colour and brightness stimuli, but they were unable to discriminate the polarization stimuli. Our results suggest that in the behavioural context studied here, zebra finches are not able to discriminate polarized light stimuli.

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 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 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, λ(T0.5), 323 nm) than birds with VS pigments (λ(T0.5), 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 contribution of single and double cones to spectral sensitivity in budgerigars during changing light conditions.

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.

Retinal ganglion cell topography and spatial resolution of two parrot species: budgerigar (Melopsittacus undulatus) and Bourke's parrot (Neopsephotus bourkii).

Retinal ganglion cell (RGC) isodensity maps indicate important regions in an animal's visual field. These maps can also be combined with measures of focal length to estimate the theoretical visual acuity. Here we present the RGC isodensity maps and anatomical spatial resolving power in three budgerigars (Melopsittacus undulatus) and two Bourke's parrots (Neopsephotus bourkii). Because RGCs were stacked in several layers, we modified the Nissl staining procedure to assess the cell number in the whole-mounted and cross-sectioned tissue of the same retinal specimen. The retinal topography showed surprising variation; however, both parrot species had an area centralis without discernable fovea. Budgerigars also had a putative area nasalis never reported in birds before. The peak RGC density was 22,300-34,200 cells/mm(2) in budgerigars and 18,100-38,000 cells/mm(2) in Bourke's parrots. The maximum visual acuity based on RGCs and focal length was 6.9 cyc/deg in budgerigars and 9.2 cyc/deg in Bourke's parrots. These results are lower than earlier behavioural estimates. Our findings illustrate that retinal topography is not a very fixed trait and that theoretical visual acuity estimations based on RGC density can be lower than the behavioural performance of the bird.

Out of the blue: the spectral sensitivity of hummingbird hawkmoths.

The European hummingbird hawkmoth Macroglossum stellatarum is a diurnal nectar forager like the honeybee, and we expect similarities in their sensory ecology. Using behavioural tests and electroretinograms (ERGs), we studied the spectral sensitivity of M. stellatarum. By measuring ERGs in the dark-adapted eye and after adaptation to green light, we determined that M. stellatarum has ultraviolet (UV), blue and green receptors maximally sensitive at 349, 440 and 521 nm, and confirmed that green receptors are most frequent in the retina. To determine the behavioural spectral sensitivity (action spectrum) of foraging moths, we trained animals to associate a disk illuminated with spectral light, with a food reward, and a dark disk with no reward. While the spectral positions of sensitivity maxima found in behavioural tests agree with model predictions based on the ERG data, the sensitivity to blue light was 30 times higher than expected. This is different from the honeybee but similar to earlier findings in the crepuscular hawkmoth Manduca sexta. It may indicate that the action spectrum of foraging hawkmoths does not represent their general sensory capacity. We suggest that the elevated sensitivity to blue light is related to the innate preference of hawkmoths for blue flowers.

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.

Ultraviolet sensitivity and colour vision in raptor foraging.

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.

Luminance-dependence of spatial vision in budgerigars (Melopsittacus undulatus) and Bourke's parrots (Neopsephotus bourkii).

Budgerigars (Melopsittacus undulatus) and Bourke's parrots (Neopsephotus bourkii) are closely related birds with different activity patterns. Budgerigars are strictly diurnal while Bourke's parrots are active in dim twilight. Earlier studies show that the intensity threshold of colour vision is similar in both species while Bourke's parrots have larger eyes with a higher density of rods than budgerigars. In this study, we investigate whether this could be an adaptation for better spatial vision in dim light. We used two alternative forced-choice experiments to determine the spatial acuity of both species at light intensities ranging from 0.08 to 73 cd/m(2). We also determined the spatial contrast sensitivity function (CSF) for bright light in Bourke's parrots and compare it to existing data for budgerigars. The spatial acuity of Bourke's parrots was found to be similar to that of budgerigars at all light levels. Also the CSF of Bourke's parrots is similar to that of budgerigars with a sensitivity peak located between 2.1 and 2.6 cycles/degree. Our findings do not support the hypothesis that Bourke's parrots have superior spatial acuity in dim light compared to budgerigars and the adaptive value of the relatively rod-rich and large eyes of Bourke's parrots remains unclear.

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.

Visual acuity of budgerigars for moving targets.

For a bird, it is often vital to visually detect food items, predators, or individuals from the same flock, i.e. moving stimuli of various shapes. Yet, behavioural tests of visual spatial acuity traditionally use stationary gratings as stimuli. We have behaviourally tested the ability of budgerigars (Melopsittacus undulatus) to detect a black circular target, moving semi-randomly at 1.69 degrees s-1 against a brighter background. We found a detection threshold of 0.107±0.007 degrees of the visual field for a target size corresponding to a resolution of a grating with a spatial frequency of 4.68 cycles degree-1. This detection threshold is lower than the resolution limit for gratings but similar to the threshold for stationary single objects of the same shape. We conclude that the target acuity of budgerigars for moving single targets, just as for stationary single targets, is lower than their acuity for gratings.

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.

The intensity threshold of colour vision in two species of parrot.

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 microm(2) sr, Bourke's parrot 0.25 microm(2) sr) but Bourke's parrots have more (cone to rod ratio, 1.2:1.0), thinner (2.8 microm) and longer rods (18.5 microm) than budgerigars (2.1:1.0, 3.4 microm, 13.3 microm). 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.

Pterin-pigmented nanospheres create the colours of the polymorphic damselfly Ischnura elegans.

Animal colours commonly act as signals for mates or predators. In many damselfly species, both sexes go through a developmental colour change as adults, and females often show colour polymorphism, which may have a function in mate choice, avoidance of mating harassment and camouflage. In the blue-tailed damselfly, Ischnura elegans, young males are bright green and turn blue as they reach maturity. Females are red ( rufescens) or violet ( violacea) as immatures and, when mature, either mimic the blue colour of the males ( androchrome), or acquire an inconspicuous olive-green ( infuscans) or olive-brown ( obsoleta). The genetic basis of these differences is still unknown. Here, we quantify the colour development of all morphs of I. elegans and investigate colour formation by combining anatomical data and reflectance spectra with optical finite-difference time-domain simulations. While the coloration primarily arises from a disordered assembly of nanospheres in the epidermis, morph-dependent changes result from adjustments in the composition of pterin pigments within the nanospheres, and from associated shifts in optical density. Other pigments fine-tune hue and brilliance by absorbing stray light. These mechanisms produce an impressive palette of colours and offer guidance for genetic studies on the evolution of colour polymorphism and visual communication.

Single target acuity is not higher than grating acuity in a bird, the budgerigar.

We examined the capacity of budgerigars (Melopsittacus undulatus) to visually detect dark single targets against a brighter background and established their spatial resolution limit for such targets. While the sampling density of the retina limits the resolution of gratings, target detection is theoretically limited by contrast sensitivity. This allows many animals to detect single targets smaller than their visual resolution limit, but this is not the case for budgerigars. The budgerigars were able to detect a high contrast circular target with a luminance profile of a single period of a sine wave subtending 0.065 degrees of their visual field, corresponding to a spatial acuity of 7.7 cycles degree-1, a measurement in line with the previously measured grating acuity of budgerigars (7.7 and 10 cycles degree-1). This result is different from findings on the spatial acuity of humans, who can detect single targets much smaller than predicted by their acuity for gratings. The low contrast sensitivity of budgerigar vision might be one of the reasons why the single target acuity is not higher than grating acuity. Adding a bright surround to the target did not influence detection threshold significantly. However, the threshold was slightly higher for a target with a square-wave luminance profile than for a target with a sinusoidal luminance profile.