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.

Anomalous binocular vision in African Harrier-Hawks.

An animal's visual field is the three-dimensional space around its head from which it can extract visual information at any instant1. Bird visual fields vary markedly between species, and this variation is likely to be driven primarily by foraging ecology1,2,3. The binocular visual field is the region in which the visual fields of the two eyes overlap; thus, objects in the binocular field are imaged by both eyes simultaneously. The binocular field plays a pivotal role in the detection of symmetrical optic flow-fields, providing almost instantaneous information on the direction of travel and the time to contact a target towards which the head or feet is travelling; thus, information from the binocular field is crucial in guiding key foraging behaviours2,3. Here, we demonstrate an unusual visual field and binocular extent above the head in African Harrier-Hawks, also known as Gymnogenes (Polyboroides typus) compared to 18 other members of the Accipitridae4,5. We argue that the observed visual field can be attributed to the unusual and specific foraging behaviour of African Harrier-Hawks.

Binocular field configuration in owls: the role of foraging ecology.

The binocular field of vision differs widely in birds depending on ecological traits such as foraging. Owls (Strigiformes) have been considered to have a unique binocular field, but whether it is related to foraging has remained unknown. While taking into account allometry and phylogeny, we hypothesized that both daily activity cycle and diet determine the size and shape of the binocular field in owls. Here, we compared the binocular field configuration of 23 species of owls. While we found no effect of allometry and phylogeny, ecological traits strongly influence the binocular field shape and size. Binocular field shape of owls significantly differed from that of diurnal raptors. Among owls, binocular field shape was relatively conserved, but binocular field size differed among species depending on ecological traits, with larger binocular fields in species living in dense habitat and foraging on invertebrates. Our results suggest that (i) binocular field shape is associated with the time of foraging in the daily cycle (owls versus diurnal raptors) and (ii) that binocular field size differs between closely related owl species even though the general shape is conserved, possibly because the field of view is partially restricted by feathers, in a trade-off with auditory localization.

Binocular vision and foraging in ducks, geese and swans (Anatidae).

Wide variation in visual field configuration across avian species is hypothesized to be driven primarily by foraging ecology and predator detection. While some studies of selected taxa have identified relationships between foraging ecology and binocular field characteristics in particular species, few have accounted for the relevance of shared ancestry. We conducted a large-scale, comparative analysis across 39 Anatidae species to investigate the relationship between the foraging ecology traits of diet or behaviour and binocular field parameters, while controlling for phylogeny. We used phylogenetic models to examine correlations between traits and binocular field characteristics, using unidimensional and morphometric approaches. We found that foraging behaviour influenced three parameters of binocular field size: maximum binocular field width, vertical binocular field extent, and angular separation between the eye-bill projection and the direction of maximum binocular field width. Foraging behaviour and body mass each influenced two descriptors of binocular field shape. Phylogenetic relatedness had minimal influence on binocular field size and shape, apart from vertical binocular field extent. Binocular field differences are associated with specific foraging behaviours, as related to the perceptual challenges of obtaining different food items from aquatic and terrestrial environments.

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.

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.

How fast can raptors see?

Birds, and especially raptors, are highly visual animals. Some of them have the highest spatial resolving power known in the animal kingdom, allowing prey detection at distance. While many raptors visually track fast-moving and manoeuvrable prey, requiring high temporal resolution, this aspect of their visual system has never been studied before. In this study, we estimated how fast raptors can see, by measuring the flicker fusion frequency of three species with different lifestyles. We found that flicker fusion frequency differed among species, being at least 129 Hz in the peregrine falcon, Falco peregrinus, 102 Hz in the saker falcon, Falco cherrug, and 81 Hz in the Harris's hawk, Parabuteo unicinctus We suggest a potential link between fast vision and hunting strategy, with high temporal resolution in the fast-flying falcons that chase fast-moving, manoeuvrable prey and a lower resolution in the Harris's hawk, which flies more slowly and targets slower prey.

Sight or smell: which senses do scavenging raptors use to find food?

Raptors are usually considered to be mainly visually dependent, and the use of other sensory modalities has rarely been studied in these birds. Here, we investigated experimentally which senses (vision and/or olfaction) Turkey vultures (Cathartes aura) and Southern caracaras (Caracara plancus) use to find hidden food. First, two identical stainless-steel perforated balls, one containing a putrefied piece of meat and the other an odorless control, were presented to birds in binary choice experiments. Both species interacted more with the smelling ball than with the control, suggesting that they were attracted by the odor of the hidden meat. In a second experiment, individuals were accustomed to eat in one specifically colored ball (blue or green). In the test phase, the meat was hidden in the opposite color with respect to the one each bird had become accustomed to. Vultures still interacted more with the smelly ball disregarding the color, while caracaras interacted equally with the two balls. The prevalence of olfaction in Turkey vultures may partly explain why they are the first raptors to find carcasses in tropical forests. In contrast, caracaras forage on the ground opportunistically, a strategy where both olfaction and sight may be involved. Our experiments suggest that both species are able to use olfactory cues for foraging. However, olfaction could be the predominant sense in Turkey vultures while olfaction and sight could play an equivalent role in Southern caracaras.

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.

Visual field shape and foraging ecology in diurnal raptors.

Birds, particularly raptors, are believed to forage primarily using visual cues. However, raptor foraging tactics are highly diverse - from chasing mobile prey to scavenging - which may reflect adaptations of their visual systems. To investigate this, we studied the visual field configuration of 15 species of diurnal Accipitriformes that differ in such tactics, first focusing on the binocular field and blind area by using a single-traits approach, and then exploring the shape of the binocular field with a morphometric approach. While the maximum binocular field width did not differ between species with different foraging tactics, the overall shape of their binocular fields did. In particular, raptors chasing terrestrial prey (ground predators) had a more protruding binocular field and a wider blind area above the head than did raptors chasing aerial or aquatic prey and obligate scavengers. Ground predators that forage on mammals from above have a wide but short bill - which increases ingestion rate - and a large suborbital ridge to avoid sun glare. This may explain the protruding binocular field and the wide blind area above the head. By contrast, species from the two other groups have long but narrow bills used to pluck, flake or tear food and may need large visual coverage (and reduced suborbital ridges) to increase their foraging efficiency (e.g. using large visual coverage to follow the escaping prey in three dimensions or detect conspecifics). We propose that binocular field shape is associated with bill and suborbital ridge shape and, ultimately, foraging strategies.

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.

Visual abilities in two raptors with different ecology.

Differences in visual capabilities are known to reflect differences in foraging behaviour even among closely related species. Among birds, the foraging of diurnal raptors is assumed to be guided mainly by vision but their foraging tactics include both scavenging upon immobile prey and the aerial pursuit of highly mobile prey. We studied how visual capabilities differ between two diurnal raptor species of similar size: Harris's hawks, Parabuteo unicinctus, which take mobile prey, and black kites, Milvus migrans, which are primarily carrion eaters. We measured visual acuity, foveal characteristics and visual fields in both species. Visual acuity was determined using a behavioural training technique; foveal characteristics were determined using ultra-high resolution spectral-domain optical coherence tomography (OCT); and visual field parameters were determined using an ophthalmoscopic reflex technique. We found that these two raptors differ in their visual capacities. Harris's hawks have a visual acuity slightly higher than that of black kites. Among the five Harris's hawks tested, individuals with higher estimated visual acuity made more horizontal head movements before making a decision. This may reflect an increase in the use of monocular vision. Harris's hawks have two foveas (one central and one temporal), while black kites have only one central fovea and a temporal area. Black kites have a wider visual field than Harris's hawks. This may facilitate the detection of conspecifics when they are scavenging. These differences in the visual capabilities of these two raptors may reflect differences in the perceptual demands of their foraging behaviours.

Visual acuity in an opportunistic raptor, the chimango caracara (Milvago chimango).

Raptors are always considered to have an extraordinary resolving power of their eyes (high visual acuity). Nevertheless, raptors differ in their diet and foraging tactics, which could lead to large differences in visual acuity. The visual acuity of an opportunist bird of prey, the Chimango caracara (Mivalgo chimango) was estimated by operant conditioning. Three birds were trained to discriminate two stimuli, a positive grey uniform pattern and a negative grating pattern stimulus. The visual acuity range from 15.08 to 39.83 cycles/degrees. When compared to other birds, they have a higher visual acuity than non-raptorial birds, but they have the lowest visual acuity found in bird of prey so far. We discuss this result in the context of the ecology of the bird, with special focus on it is foraging tactic.