Low achromatic contrast sensitivity in birds: a common attribute shared by many phylogenetic orders.

Vision is an important sensory modality in birds, which can outperform other vertebrates in some visual abilities. However, sensitivity to achromatic contrasts - the ability to discern luminance difference between two objects or an object and its background - has been shown to be lower in birds compared with other vertebrates. We conducted a comparative study to evaluate the achromatic contrast sensitivity of 32 bird species from 12 orders using the optocollic reflex technique. We then performed an analysis to test for potential variability in contrast sensitivity depending on the corneal diameter to the axial length ratio, a proxy of the retinal image brightness. To account for potential influences of evolutionary relatedness, we included phylogeny in our analyses. We found a low achromatic contrast sensitivity for all avian species studied compared with other vertebrates (except small mammals), with high variability between species. This variability is partly related to phylogeny but appears to be independent of image brightness.

Ontogenetic exposure to light influences seabird vulnerability to light pollution.

Light pollution critically affects fledglings of burrow-nesting seabirds, leading to massive mortality events. The successful management of this pollutant depends upon a comprehensive understanding of the factors influencing visual sensitivity and corresponding behaviours towards light. Factors shaping the development of the visual system could account for variation in seabirds' vulnerability to light pollution. We investigated how Cory's shearwater chicks respond to selected contrasting artificial light stimuli. Chicks were subjected to blue and red light treatments, and repeatedly tested throughout the nestling period. We analysed behavioural responses (number, timing and orientation of reactions) to determine how age, exposure to experimental light stimuli and spectra influenced the onset of visually guided behaviours, thus inferring drivers of vulnerability to light pollution. Repetitive exposure to light significantly increased the number of reactions, and chicks predominantly displayed light avoidance behaviour. We did not find differences in the number of reactions, timing and orientation between blue and red light treatments. The responses did not differ across different age groups. These results provide empirical evidence for the contribution of the light available in the rearing environment to seabird visual development. They support the hypothesis that differential exposure to light during the growth period influences responses to artificial light, and that the state of visual development at fledging could be a main driver of the age bias observed during seabird fallout events. It is thus important to evaluate lighting schemes in both urban and natural areas, and determine the as yet unknown consequences that may be affecting the populations.

Retinal Ganglion Cell Topography and Spatial Resolution in Three Indian Pteropodid Bats.

Pteropodidae is the only phytophagous bat family that predominantly depends on visual and olfactory cues for orientation and foraging. During daytime, pteropodids of different species roost in sites with varying light exposure. Pteropodids have larger eyes relative to body size than insectivorous bats. Retinal topography has been studied in less than 10% of the approximately 200 pteropodid species, a behavioural estimation of spatial resolution is available only for Pteropus giganteus, and little is known about the relationship between their roost site preference and visual ecology. We present retinal ganglion cell topographic maps and anatomical estimates of spatial resolution in three southern Indian pteropodid species with different roosting preferences. Ganglion cell densities are between 1,000 and 2,000 cells/mm2 in the central retina and lower in the dorsal and ventral periphery. All three species have a temporal area in the retina with peak ganglion cell densities of 4,600-6,600 cells/mm2. As a result, the foliage-roosting Cynopterus sphinx and the cave-roosting Rousettus leschenaultii have similar anatomical resolution (2.7 and 2.8 cycles/degree, respectively). The anatomical estimate for the larger tree-roosting P. giganteus (4.0 cycles/degree) is higher than the spatial resolution determined earlier in behavioural tests. Like other pteropodids and unlike other vertebrates, all three species have choroidal papillae. Based on 15 pteropodid species studied to date, we find no relationship between roost type and eye size or visual acuity. For a general understanding of the sensory ecology of pteropodids that perform key ecosystem services in the tropics, it will be essential to study additional species.

Visual adaptations of diurnal and nocturnal raptors.

Raptors have always fascinated mankind, owls for their highly sensitive vision, and eagles for their high visual acuity. We summarize what is presently known about the eyes as well as the visual abilities of these birds, and point out knowledge gaps. We discuss visual fields, eye movements, accommodation, ocular media transmittance, spectral sensitivity, retinal anatomy and what is known about visual pathways. The specific adaptations of owls to dim-light vision include large corneal diameters compared to axial (and focal) length, a rod-dominated retina and low spatial and temporal resolution of vision. Adaptations of diurnal raptors to high acuity vision in bright light include rod- and double cone-free foveae, high cone and retinal ganglion cell densities and high temporal resolution. We point out that more studies, preferably using behavioural and non-invasive methods, are desirable.

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.

High resolution of colour vision, but low contrast sensitivity in a diurnal raptor.

Animals are thought to use achromatic signals to detect small (or distant) objects and chromatic signals for large (or nearby) objects. While the spatial resolution of the achromatic channel has been widely studied, the spatial resolution of the chromatic channel has rarely been estimated. Using an operant conditioning method, we determined (i) the achromatic contrast sensitivity function and (ii) the spatial resolution of the chromatic channel of a diurnal raptor, the Harris's hawk Parabuteo unicinctus The maximal spatial resolution for achromatic gratings was 62.3 c deg-1, but the contrast sensitivity was relatively low (10.8-12.7). The spatial resolution for isoluminant red-green gratings was 21.6 c deg-1-lower than that of the achromatic channel, but the highest found in the animal kingdom to date. Our study reveals that Harris's hawks have high spatial resolving power for both achromatic and chromatic vision, suggesting the importance of colour vision for foraging. By contrast, similar to other bird species, Harris's hawks have low contrast sensitivity possibly suggesting a trade-off with chromatic sensitivity. The result is interesting in the light of the recent finding that double cones-thought to mediate high-resolution vision in birds-are absent in the central fovea of raptors.

Development of the Visual System in a Burrow-Nesting Seabird: Leach's Storm Petrel.

Little is known about the development of vision in wild birds. It is unknown, for example, whether the ability to see can be predicted by the level of prenatal growth or whether the eyes are open at hatching in a particular species. In this study, we investigated the growth of eyes, the formation of retinal ganglion cell topography, and the appearance of simple, visually guided behaviours in chicks of a small procellariiform seabird, Leach's storm petrel (Oceanodroma leucorhoa). This semi-precocial species, which has a well-developed sense of smell, nests in underground burrows where adults provision chicks for 6-8 weeks in the dark before fledging. Retinal ganglion cell topographic maps revealed that fine-tuning of cell distribution does not happen early in development, but rather that the ganglion cell layer continues to mature throughout provisioning and probably even after fledging. While the olfactory bulbs reached adult size around 7 weeks after hatching, the eyes and telencephalon continued to grow. Optokinetic head response and artificial burrow finding experiments indicated that chicks in the 2nd week after hatching lack even the most basic visually guided behaviours and are probably blind. Thus, vision in Leach's storm petrel chicks starts to function sometime around the 3rd week after hatching, well after the eyes have opened and the olfactory system is functional.

Eye Size, Fovea, and Foraging Ecology in Accipitriform Raptors.

Birds with larger eyes are predicted to have higher spatial resolution because of their larger retinal image. Raptors are well known for their acute vision, mediated by their deep central fovea. Because foraging strategies may demand specific visual adaptations, eye size and fovea may differ between species with different foraging ecology. We tested whether predators (actively hunting mobile prey) and carrion eaters (eating dead prey) from the order Accipitriformes differ in eye size, foveal depth, and retinal thickness using spectral domain optical coherence tomography and comparative phylogenetic methods. We found that (1) all studied predators (except one) had a central and a temporal fovea, but all carrion eaters had only the central fovea; (2) eye size scaled with body mass both in predators and carrion eaters; (3) predators had larger eyes relative to body mass and a thicker retina at the edge of the fovea than carrion eaters, but there was no difference in the depth of the central fovea between the groups. Finally, we found that (4) larger eyes generally had a deeper central fovea. These results suggest that the visual system of raptors within the order Accipitriformes may be highly adapted to the foraging strategy, except for the foveal depth, which seems mostly dependent upon the eye size.

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.

Vision on the high seas: spatial resolution and optical sensitivity in two procellariiform seabirds with different foraging strategies.

Procellariiform or 'tubenosed' seabirds are challenged to find prey and orient over seemingly featureless oceans. Previous studies have found that life-history strategy (burrow versus surface nesting) was correlated to foraging strategy. Burrow nesters tended to track prey using dimethyl sulphide (DMS), a compound associated with phytoplankton, whereas surface-nesting species did not. Burrow nesters also tended to be smaller and more cryptic, whereas surface nesters were larger with contrasting plumage coloration. Together these results suggested that differences in life-history strategy might also be linked to differences in visual adaptations. Here, we used Leach's storm petrel, a DMS-responder, and northern fulmar, a non-responder, as model species to test this hypothesis on their sensory ecology. From the retinal ganglion cell density and photoreceptor dimensions, we determined that Leach's storm petrels have six times lower spatial resolution than the northern fulmars. However, the optical sensitivity of rod photoreceptors is similar between species. These results suggest that under similar atmospheric conditions, northern fulmars have six times the detection range for similarly sized objects. Both species have extended visual streaks with a central area of highest spatial resolution, but only the northern fulmar has a central fovea. The prediction that burrow-nesting DMS-responding procellariiforms should differ from non-responding species nesting in the open holds true for spatial resolution, but not for optical sensitivity. This result may reflect the fact that both species rely on olfaction for their nocturnal foraging activity, but northern fulmars might use vision more during daytime.

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.

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.

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.

Inter-individual differences in foveal shape in a scavenging raptor, the black kite Milvus migrans.

Birds, and especially raptors, are believed to forage mainly using visual cues. Indeed, raptors (scavengers and predators) have the highest visual acuity known to date. However, scavengers and predators differ in their visual systems such as in their foveal configuration. While the function of the foveal shape remains unknown, individual variation has never been quantified in birds. In this study, we examined whether foveal shape differs among individuals in relation to eye size, sex, age, eye (left or right) and genetic proximity in a scavenging raptor, the black kite Milvus migrans. We assessed foveal shape in 47 individuals using spectral domain optical coherence tomography (OCT) and geometric morphometric analysis. We found that foveal depth was significantly related to eye size. While foveal width also increased with eye size, it was strongly related to age; younger individuals had a wider fovea with a more pronounced rim. We found no relationship between foveal shape and genetic proximity, suggesting that foveal shape is not a hereditary trait. Our study revealed that the shape of the fovea is directly linked to eye size and that the physical structure of the fovea may develop during the entire life of black kites.

Retinal topography in two species of flamingo (Phoenicopteriformes: Phoenicopteridae).

In this study, we assessed eye morphology and retinal topography in two flamingo species, the Caribbean flamingo (Phoenicopterus ruber) and the Chilean flamingo (P. chilensis). Eye morphology is similar in both species and cornea size relative to eye size (C:A ratio) is intermediate between those previously reported for diurnal and nocturnal birds. Using stereology and retinal whole mounts, we estimate that the total number of Nissl-stained neurons in the retinal ganglion cell (RGC) layer in the Caribbean and Chilean flamingo is ~1.70 and 1.38 million, respectively. Both species have a well-defined visual streak with a peak neuron density of between 13,000 and 16,000 cells mm-2 located in a small central area. Neurons in the high-density regions are smaller and more homogeneous compared to those in medium- and low-density regions. Peak anatomical spatial resolving power in both species is approximately 10-11 cycles/deg. En-face images of the fundus in live Caribbean flamingos acquired using spectral domain optical coherence tomography (SD-OCT) revealed a thin, dark band running nasotemporally just dorsal to the pecten, which aligned with the visual streak in the retinal topography maps. Cross-sectional images (B-scans) obtained with SD-OCT showed that this dark band corresponds with an area of retinal thickening compared to adjacent areas. Neither the retinal whole mounts, nor the SD-OCT imaging revealed any evidence of a central fovea in either species. Overall, we suggest that eye morphology and retinal topography in flamingos reflects their cathemeral activity pattern and the physical nature of the habitats in which they live.

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.

Specialized photoreceptor composition in the raptor fovea.

The retinae of many bird species contain a depression with high photoreceptor density known as the fovea. Many species of raptors have two foveae, a deep central fovea and a shallower temporal fovea. Birds have six types of photoreceptors: rods, active in dim light, double cones that are thought to mediate achromatic discrimination, and four types of single cones mediating color vision. To maximize visual acuity, the fovea should only contain photoreceptors contributing to high-resolution vision. Interestingly, it has been suggested that raptors might lack double cones in the fovea. We used transmission electron microscopy and immunohistochemistry to evaluate this claim in five raptor species: the common buzzard (Buteo buteo), the honey buzzard (Pernis apivorus), the Eurasian sparrowhawk (Accipiter nisus), the red kite (Milvus milvus), and the peregrine falcon (Falco peregrinus). We found that all species, except the Eurasian sparrowhawk, lack double cones in the center of the central fovea. The size of the double cone-free zone differed between species. Only the common buzzard had a double cone-free zone in the temporal fovea. In three species, we examined opsin expression in the central fovea and found evidence that rod opsin positive cells were absent and violet-sensitive cone and green-sensitive cone opsin positive cells were present. We conclude that not only double cones, but also single cones may contribute to high-resolution vision in birds, and that raptors may in fact possess high-resolution tetrachromatic vision in the central fovea.