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.

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.

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.

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.

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.

Owls lack UV-sensitive cone opsin and red oil droplets, but see UV light at night: Retinal transcriptomes and ocular media transmittance.

Most diurnal birds have cone-dominated retinae and tetrachromatic colour vision based on ultra-violet/violet-sensitive UV/V cones expressing short wavelength-sensitive opsin 1 (SWS1), S cones expressing short wavelength-sensitive opsin 2 (SWS2), M cones expressing medium wavelength-sensitive opsin (RH2) and L cones expressing long wavelength-sensitive opsin (LWS). Double cones (D) express LWS but do not contribute to colour vision. Each cone is equipped with an oil droplet, transparent in UV/V cones, but pigmented by carotenoids: galloxanthin in S, zeaxanthin in M, astaxanthin in L and a mixture in D cones. Owls (Strigiformes) are crepuscular or nocturnal birds with rod-dominated retinae and optical adaptations for high sensitivity. For eight species, the absence of functional SWS1 opsin has recently been documented, functional RH2 opsin was absent in three of these. Here we confirm the absence of SWS1 transcripts for the Long-eared owl (Asio otus) and demonstrate its absence for the Short-eared owl (Asio flammeus), Tawny owl (Strix aluco) and Boreal owl (Aegolius funereus). All four species had transcripts of RH2, albeit with low expression. All four species express all enzymes needed to produce galloxanthin, but lack CYP2J19 expression required to produce astaxanthin from dietary precursors. We also present ocular media transmittance of the Eurasian eagle owl (Bubo bubo) and Short-eared owl and predict spectral sensitivities of all photoreceptors of the Tawny owl. We conclude that owls, despite lacking UV/V cones, can detect UV light. This increases the sensitivity of their rod vision allowing them, for instance, to see UV-reflecting feathers as brighter signals at night.

High visual acuity revealed in dogs.

Humans have selectively bred and used dogs over a period of thousands of years, and more recently the dog has become an important model animal for studies in ethology, cognition and genetics. These broad interests warrant careful descriptions of the senses of dogs. Still there is little known about dog vision, especially what dogs can discriminate in different light conditions. We trained and tested whippets, pugs, and a Shetland sheepdog in a two-choice discrimination set-up and show that dogs can discriminate patterns with spatial frequencies between 5.5 and 19.5 cycle per degree (cpd) in the bright light condition (43 cd m-2). This is a higher spatial resolution than has been previously reported although the individual variation in our tests was large. Humans tested in the same set-up reached acuities corresponding to earlier studies, ranging between 32.1 and 44.2 cpd. In the dim light condition (0.0087 cd m-2) the acuity of dogs ranged between 1.8 and 3.5 cpd while in humans, between 5.9 and 9.9 cpd. Thus, humans make visual discrimination of objects from roughly a threefold distance compared to dogs in both bright and dim light.

Visual cues of oviposition sites and spectral sensitivity of Cydia strobilella L.

We investigated whether the spruce seed moth (Cydia strobilella L., Tortricidae: Grapholitini), an important pest in seed orchards of Norway spruce (Picea abies (L.) Karst.), can make use of the spectral properties of its host when searching for flowers to oviposit on. Spectral measurements showed that the flowers, and the cones they develop into, differ from a background of P. abies needles by a higher reflectance of long wavelengths. These differences increase as the flowers develop into mature cones. Electroretinograms (ERGs) in combination with spectral adaptation suggest that C. strobilella has at least three spectral types of photoreceptor; an abundant green-sensitive receptor with maximal sensitivity at wavelength λmax=526nm, a blue-sensitive receptor with λmax=436nm, and an ultraviolet-sensitive receptor with λmax=352nm. Based on our spectral measurements and the receptor properties inferred from the ERGs, we calculated that open flowers, which are suitable oviposition sites, provide detectable achromatic, but almost no chromatic contrasts to the background of needles. In field trials using traps of different spectral properties with or without a female sex pheromone lure, only pheromone-baited traps caught moths. Catches in baited traps were not correlated with the visual contrast of the traps against the background. Thus, visual contrast is probably not the primary cue for finding open host flowers, but it could potentially complement olfaction as a secondary cue, since traps with certain spectral properties caught significantly more moths than others.

Coevolution of coloration and colour vision?

The evolutionary relationship between signals and animal senses has broad significance, with potential consequences for speciation, and for the efficacy and honesty of biological communication. Here we outline current understanding of the diversity of colour vision in two contrasting groups: the phylogenetically conservative birds, and the more variable butterflies. Evidence for coevolution of colour signals and vision exists in both groups, but is limited to observations of phenotypic differences between visual systems, which might be correlated with coloration. Here, to illustrate how one might interpret the evolutionary significance of such differences, we used colour vision modelling based on an avian eye to evaluate the effects of variation in three key characters: photoreceptor spectral sensitivity, oil droplet pigmentation and the proportions of different photoreceptor types. The models predict that physiologically realistic changes in any one character will have little effect, but complementary shifts in all three can substantially affect discriminability of three types of natural spectra. These observations about the adaptive landscape of colour vision may help to explain the general conservatism of photoreceptor spectral sensitivities in birds. This approach can be extended to other types of eye and spectra to inform future work on coevolution of coloration and colour vision.This article is part of the themed issue 'Animal coloration: production, perception, function and application'.

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.

Colour vision and background adaptation in a passerine bird, the zebra finch (Taeniopygia guttata).

Today, there is good knowledge of the physiological basis of bird colour vision and how mathematical models can be used to predict visual thresholds. However, we still know only little about how colour vision changes between different viewing conditions. This limits the understanding of how colour signalling is configured in habitats where the light of the illumination and the background may shift dramatically. I examined how colour discrimination in zebra finch (Taeniopygia guttata) is affected by adaptation to different backgrounds. I trained finches in a two-alternative choice task, to choose between red discs displayed on backgrounds with different colours. I found that discrimination thresholds correlate with stimulus contrast to the background. Thresholds are low, and in agreement with model predictions, for a background with a red colour similar to the discs. For the most contrasting green background, thresholds are about five times higher than this. Subsequently, I trained the finches for the detection of single discs on a grey background. Detection thresholds are about 2.5 to 3 times higher than discrimination thresholds. This study demonstrates close similarities in human and bird colour vision, and the quantitative data offer a new possibility to account for shifting viewing conditions in colour vision models.

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.

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.

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.

Stimulus motion improves spatial contrast sensitivity in budgerigars (Melopsittacus undulatus).

Birds are generally thought to have excellent vision with high spatial resolution. However, spatial contrast sensitivity of birds for stationary targets is low compared to other animals with similar acuity, such as mammals. For fast flying animals body stability and coordination are highly important, and visual motion cues are known to be relevant for flight control. We have tested five budgerigars (Melopsittacus undulatus) in behavioural discrimination experiments to determine whether or not stimulus motion improves contrast sensitivity. The birds were trained to distinguish between a homogenous grey field and sine-wave gratings of spatial frequencies between 0.48 and 6.5 cyc/deg, and Michelson contrasts between 0.7% and 99%. The gratings were either stationary or drifting with velocities between 0.9 and 13 deg/s. Budgerigars were able to discriminate patterns of lower contrast from grey when the gratings were drifting, and the improvement in sensitivity was strongest at lower spatial frequencies and higher drift velocities. Our findings indicate that motion cues can have positive effects on visual perception of birds. This is similar to earlier results on human vision. Contrast sensitivity, tested solely with stationary stimuli, underestimates the sensory capacity of budgerigars flying through their natural environments.

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.