It is, however, found only in a small number of species. While many birds have extensive visual fields most have a blind area behind the head leaving them more vulnerable to predator attack Figure 3. The presence of these blind areas and their absence in only certain species is evidence that controlling bill position and the detection of predators are tasks which have different informational demands that are in competition.
Total panoramic vision appears to have evolved independently in just two bird orders which are distantly related Jarvis et al.
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Only a few species in these taxa have totally panoramic vision, but those that do, share a common feature in that their foraging does not require visual control of bill position; foraging relies upon tactile information derived from bill-tip organs Martin, Accurate visual control of bill position seems to place an important constraint of visual field configuration, but when that constraint is removed, it appears that natural selection has driven toward the evolution of comprehensive panoramic visual coverage above and around the head as an aid to predator detection.
However, these birds are able to fly fast even in complex habitats. This suggests that a frontal binocular field of this narrow width is sufficient for the control of flight. Thus, it seems safe to conclude that the function of broader binocular fields is related to the control of bill position, not flight control. There is evidence from both ducks and shorebirds that the gaining of comprehensive vision can evolve relatively rapidly. This is indicated by the finding that there are significant differences in vigilance behavior in two ducks within the same genus, and that these differences are explained by differences in their visual fields.
These differences in vigilance behavior have been observed between the non-visual tactile and filter foraging Northern Shovelers Anas clypeata and the visually guided foraging Eurasian Wigeons A. Penelope Guillemain et al. Wigeons are selective grazers guided by visual cues and have a wider binocular field which embraces the projection of their bill tip, with the result that they have a blind region behind the head. On the other hand Shovelers have comprehensive visual coverage of the celestial hemisphere.
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Thus, these congeneric species, which can be observed exploiting different resources in the same locality, differ in their visual field configurations, foraging technique, and also in their vigilance behavior. This demonstrates that subtle, but behaviorally significant, differences in visual ecology can occur between closely related species. A more recent comparative analysis of binocular field characteristics and estimates of visual acuity in buntings and American sparrows Emebrizidae also showed subtle but functionally significant differences between closely related species.
As in the ducks these differences could be related to differences in foraging and vigilance behavior Moore et al. The above examples indicate that closely related bird species, which employ different perceptual cues visual or tactile for foraging, can differ in their visual field characteristics and that these differences are functionally important. This suggests that visual fields plus the anatomical and optical structures which underpin them are driven primarily by the informational demands of foraging, although similar studies on a wider range of species are necessary to adequately test this hypothesis.
Such evolutionary outcomes regarding the informational demands for the visual control of bill position and timing may be analogous to the more well-studied subtle variations in bill form that are driven by the mechanical demands of foraging Grant and Grant, These examples reinforce the hypothesis that the configuration of visual fields are driven primarily by the informational challenges of foraging which are traded-off against the requirement for predator detection.
Not requiring visual cues to guide foraging is, however, not sufficient to lead to the evolution of comprehensive vision. It is also necessary that the bill does not require fine visual control for any task, not just foraging. Thus comprehensive vision is, in fact, found only among birds which also do not need to position their bills accurately for two other key tasks; nest construction and the provisioning of young. Both the ducks and shorebirds use simple nests which do not require elaborate construction, and their young are precocial. That is their young hatch in an advanced stage of development and self-feed from hatching.
They are never provisioned by their parents; parental care is limited to brooding and protection from predators. Most other birds must use their bills for foraging, for nest building, and for the provisioning of young, all tasks which require accurate position and timing of the bill. A telling example that makes this clear is provided by flamingos Phoenicopteridae Martin et al. They are filter feeders, having highly specialized structures within their bills to remove minute resources from filtered water and mud, yet unlike the filter feeding ducks they do not have comprehensive vision.
Thus, despite their filter feeding, flamingos require vision that allows accurate bill placement so that young can be provisioned. This results in a relatively broad binocular field into which the bill projection falls, and a blind area behind their head. Stereopsis and the perception of relative depth have become regarded as the prime function of binocular vision in humans and other primates, and it has often been assumed that these same functions apply to all instances of binocular vision.
However, it seems unlikely that this is the case among birds. An earlier study demonstrating stereopsis in American Kestrels Falco sparverius Fox et al. There is evidence of binocularly derived relative depth information in Rock Doves Columba livia that is based upon convergence eye movements and accommodation cues. However evidence of retinal disparity neurons of the kind thought to underlie stereopsis in owls and mammals Barlow et al. Binocularly driven neurons have been sought in doves. Hence each eye must have a contralateral projection, that is, each eye must look across the central plane of the head Figure 4.
It is true that this results in a region which is perceived by two eyes simultaneously and so it is labeled a binocular field. However, having two eyes extracting information from the same region is not the same as that region being analyzed with binocular vision in the sense in which it is usually understood in mammals i. For any visual system the most vital information, more important than recognition of an object, is accurate determination of an object's position. Indeed it is argued that the main driver in the early evolution of vision systems was toward increasing accuracy in spatial resolution which meant increasingly accurate determination of the direction in which objects lay with respect to the viewer Nilsson, The next most important piece of information that vision provides is the time it will take to contact an object, that is, when will the object arrive at the observer or when will the observer arrive at the object?
Perception and Motor Control in Birds
The actual identity of an object and its specific distance from a bird is likely to be of less importance than knowing the direction in which it lies, and crucially the length of time before contact will be made with it. This type of information is directly available from optic flow-fields Lee and Lishman, ; Lee, It has been shown convincingly that birds use flow-field information to control apparently exacting tasks.
For example, it has been shown that hummingbirds Tochilidae and Northern Gannets Morus bassanus when carrying out maneuver that require accurate visual information on object location and the time to reach it, employ flow-field information Lee and Reddish, ; Lee et al. Optic flow-field information in mammals is processed in the accessory optic system Giolli et al. A similar accessory system of the visual part of the brain has been identified in birds McKenna and Wallman, ; Pakan and Wylie, Information is potentially available from flow-fields that can be detected in any part of the retina.
Information concerning time-to-contact a target and the direction of travel toward it are, however, extracted most efficiently when vision surrounds the target. This will result in an optical flow-field which expands symmetrically about the image of the target Martin, This is the configuration that applies in the tasks described above as the key drivers of avian vision.
When a bird is lunging or pecking at an object both its position and the time-to-contact need to be determined accurately. The crucial factors is that for a flow-field pattern to expand symmetrically about an object toward which the bill is directed, the visual field of each eye needs to extend across the median sagittal plane of the bird, that is, there must be contralateral vision Figure 4 Martin, Here, the important concept is contralateral vision, not binocular vision. It may be more appropriate to consider that binocular vision per se is the product of the requirement to have eyes that look forward across the median sagittal plane of the head.
Such an arrangement means that movement toward a target by the bill produces a symmetrically expanding optic flow-field. Binocular vision in birds should therefore not be considered an adaptation that evolved to achieve simultaneous views of the same object from slightly different positions which may be the case in mammalian species which have stereopsis. Rather binocularity may be driven by the requirement to place the bill, or the projection of its direction, at the center of a symmetrically expanding flow-field.
What is important is contralateral vision rather than binocular vision as such. It can be hypothesized that binocularity in birds functions to provide information on the direction of travel and time-to-contact a target. Thus, in the majority of birds the function of binocularity would seem to lie in what each eye does independently rather than in what the two eyes might be able to do together. The arguments presented above support the hypothesis that two key tasks drive the configuration of visual fields in birds.
The primary driver appears to be the perceptual challenges of foraging; specifically these are the control of bill or feet position, and timing their arrival at a target Martin, This requires contralateral vision in the frontal field. The second driver appears to be the detection of predators and this requires vision over as wide a sector of space as possible around the head. Thus, these two drivers make competing demands. They can be considered primary and secondary because only under the specific circumstance of bill position not having to be controlled by vision, does the requirement for predator detection result in comprehensive visual coverage.
There is a further important difference between the two key tasks that drive vision. The control of bill position requires information extracted from the world that lies in front of, and relatively close to, the bird. The detection of predators, on the other hand, requires information that lies laterally, or even to the rear of the bird's head, and is concerned with information from locations that are remote from the bird and it is this which probably drives higher spatial resolution in lateral fields.
The regions within the visual field where there is high spatial resolution, indicated by retinal regions of high photoreceptor and ganglion cell density Tyrrell et al. Ever since such retinal topography was first described Wood, these patterns have been correlated with the regions associated specifically with foraging or with the directions from which predators are most likely to attack. Such analyses are reinforced by more recent and detailed descriptions of retinal topography Hughes, ; Fernandez-Juricic et al.
In some species e. There is evidence that predatory birds, such as Peregrine Falcons Falco peregrinus detect their prey at a distance using lateral vision, using the regions of high photoreceptor density which project laterally and slightly forward. When approaching prey Peregrines frequently do so along a curved path which keeps the prey approximately in the central field of view of a single eye and they pass control to the frontal binocular region just prior to prey capture Tucker, ; Tucker et al.
That is, the bird does not usually sight the prey into its binocular frontal field until just before prey capture. Thus distant prey is probably initially detected using lateral high resolution vision while the control of the bill and feet close to the time of prey capture probably employs frontal, lower resolution vision, and this comes into play only at close range.
However, there is evidence that other falcon species may use frontal vision quite early on in the pursuit of prey and switch between the use of the difference foveas during a pursuit flight by turning the head Kane and Zamani, Such use of lateral vision for detecting food items with control passing to forward vision for final prey capture in the bill at close quarters has been reported in other species. For example, in terns foraging over mud flats for crabs Land, , thrushes searching on the ground for earth worms Montgomerie and Weatherhead, , and in domestic chicks when detecting grain from amongst grit Rogers, A reviewer of this paper argued that owls and other nocturnal birds are exceptions to the general argument presented above.
However, no suggestions were made as to what the results of this exception might be. Why should owls and other nocturnally active birds such as, nightjars Caprimulgidae and kiwi Apterygidae be thought to be exceptions to the general thrust of the argument? What might be different about the demands of extracting information at lower light levels that would mean that the primary evolutionary driver of vision is not concerned with control of the positions and timing of the bill or feet toward a target but is rather concerned with the control of flight?
It should be noted that not all owl species are nocturnal in the sense of completing all aspects of their life cycle between dusk and dawn. The sensory adaptations of nocturnal birds and their relationships to the challenges of general mobility and foraging are topics that have been addressed in detail a number of times in the past Martin, , and also recently, Martin These reviews indicate that the frontal visual fields of owls show no special features compared with other raptors.
Their binocular field is similar in width to those of passerines and is not the broadest recorded in birds. As stated above, the broadest binocular fields among birds are found in crows Troscianko et al. The use of acoustic cues to guide owls to prey targets is well established but so also is visual guidance of the feet to take prey items when light levels are sufficiently high. Furthermore, the feet are raised just before prey strike to lie within the binocular field, suggesting that during prey capture, as in diurnal raptors, the feet may be guided by cues from the flow field within the binocular region Martin and Katzir, The visual fields of nightjars Caprimulgidae show high similarity to other non-passerine species.
Although nightjars may trawl blindly for small insects they are also known to take larger individual insects in aerial pursuit and this is highly likely to be under visual control. Oilbirds Steatornis caripensis now regarded as closely related to nightjars are perhaps the most nocturnal of all flying birds.
They roost and nests in caves by day and emerge to forage for fruit in the tree canopy at night. Their eyes are large and have the lowest f-number so far recorded in a terrestrial vertebrate and may also have an exceptionally sensitive retina Martin et al. However, their visual fields are very similar in general configuration to other non-passerine species Martin et al.
The visual fields of the flightless Kiwi are different to the majority of birds but Kiwi are dependent upon non-visual senses to guide their behavior and their vision shows evidence of regressive evolution Martin et al. Kiwi do not appear to be visually guided in their foraging and, of course, they do not use visual cues for the guidance of flight.
That the sensory systems and behavior of Kiwi are so different to other birds means that they cannot be considered as supporting or rejecting the central argument of this review. It should also be noted that there are many instances of nocturnal behaviors in a wide range of bird species beyond the owls, nightjars, and kiwi. For example, many shorebirds, waterfowl, and diving birds forage at night and many passerine species routinely migrate at night. Many birds which seek their food underwater by diving to depths may forage at night, and some species, including penguins and auks, routinely forage at such depths that they can be regarded as nocturnal foragers even if they dive during the day.
To go into detail on the vision and other senses in all such instances of nocturnal behavior in birds or birds which may forage at low light levels would take this review in a very different multisensory direction, but a reader interested in this should consider looking at Chapter 6 of Martin Owls were referred to by the reviewer as an exception among birds although the exact basis of this exceptionality was not spelt out. However, this point is sometimes made when alluding to two particular features of owl vision; first that owls have high absolute sensitivity, and second, that owls may be unique among birds in having stereopsis.
Certainly owls have high absolute visual sensitivity compared to other birds. For example, the absolute sensitivity of Tawny Owls Strix aluco is approximately times greater than in Rock Doves Columba livia Martin, However, high sensitivity is unlikely of itself to have driven the gaining of broad binocularity since as argued above binocular overlap in owls is no greater than in many bird species including passerines and some diurnal raptors, although it is broader than in doves. While there is evidence for stereopsis in owls see section The Function of Binocular Vision in Birds it is not clear how its presence should drive visual field configuration or indeed other general aspects of vision.
Furthermore there is no evidence that stereopsis is used in owls' prey catching behavior. There are, in fact, good reason to believe that stereoscopic cues are not involved in the prey capture by owls. Resolution at low light levels in owls is low Fite, ; Orlowski et al. Stereopsis is usually regarded as a rather slow process because it involves higher order processing, and the high sensitivity of owls may be achieved by relatively long temporal integration, as well as high spatial integration.
These factor are likely to make stereopsis too slow to provide information on changing depth cues during a prey strike. It is also worth noting that even if owls do have access to relative depth cues based upon stereopsis that does not mean that they do not use flow-field information, alongside the direction and distance cues based upon hearing Knudsen and Konishi, After all, humans have stereopsis, and sound location equal in accuracy to that of owls, but are highly dependent upon flow field information for the control of locomotion, especially time to contact a target.
Beyond high absolute sensitivity what is unusual about the vision of owls, compared with other birds, is the large blind area to the rear of the head. This possibly is the result of the elaborate outer ear structures in owls Norberg, which are positioned just behind the eyes, and which are used for sound localization that is considerably more accurate than that of most other bird species Klump, Because of these outer ear structures it would seem impossible for the visual fields of owls to be more extensive to the rear of the head. In essence the evolution of elaborate and large outer ears appears to have prevented owls evolving or perhaps retaining from ancestral forms more extensive visual coverage about their head.
Based upon this brief summary it would seem best not to regard owls, oilbirds, or other instances of nocturnally active bird species as posing a particular challenge to the general arguments presented in this review. The above discussion has argued that there are in fact two key drivers of vision in birds and neither of them are concerned with the perceptual demands of flight. The primary driver is argued to be the control of bill position and the timing of its arrival at a target, the secondary driver is the task of detecting food items and predators.
The control of bill position is based upon information derived from the optic flow-field in the binocular region that encompasses the bill. It is based upon information from the environment relatively close to the bird and depends upon relatively low spatial resolution. The detection of predators and food items is based upon information detected at a greater distance and depends upon regions in the retina with relatively high spatial resolution.
Interplay between these two key drivers of vision appear to be expressed in subtle interspecific variations in the vision of birds. The tasks of detecting predators and of placing the bill accurately, make contradictory demands upon vision and these have resulted in trade-offs in the form of visual fields and in the topography of retinal regions in which spatial resolution is enhanced indicated by foveas and areas of high photoreceptor and ganglion cell densities. The overall driver of frontal visual field characteristics appears to be the demand for the accurate positioning of the bill and the timing of its arrival at a target.
This means that each eye must have a certain portion of its visual field which projects forwards and contralaterally across the median sagittal plane of the head. The result of this is that in most birds there is a blind area behind the head which at any one moment constitutes an area in which predators cannot be detected. It is only in those few bird species which do not have to use vision to achieve precise control of bill position that natural selection has favored full visual coverage about the head.
Interspecific comparisons of visual fields between closely related species of ducks, shorebirds, and among emberizid passerines, have shown that small differences in foraging techniques can give rise to different perceptual challenges and these have resulted in subtle differences in visual fields even within the same genus. This suggests that vision can be subject to continuing and relatively rapid natural selection. This is perhaps not surprising given the inherent flexibility and individual differences in the structure of the optical system, retinal topography, and position in the skull, of vertebrate eyes Figure 1.
It is important to note that patterns of photoreceptor and ganglion cell distribution in the retinas of birds Lisney et al. Together this variation in optics, retinal structure and eye position present a potent source of variation in vision that can be subject to natural selection at short time scales, much in the same way that individual differences in bill morphology can be the source of natural selection that underpin bill shape changes within a bird species over a short time scale Grant and Grant, Among birds there is a strong phylogenetic signal with respect to the maximum width of the binocular field, with passerine species showing broader widths than non-passerines, and within the passerines the broadest fields are found among the Corvidae Troscianko et al.
However, sample size with respect to the total number of passerines is small and more comprehensive species sampling of passerines, as well as non-passerines, may reveal some very interesting examples of the fine tuning of vision in birds. The informational function of binocular vision in birds seems to lie not in binocularity per se i. In conclusion, it is proposed that the task of bill control is the key driver of bird vision, with predator detection also playing a key, but secondary role. The perceptual demands of flight are overshadowed by the demands of these two tasks.
The author confirms being the sole contributor of this work and approved it for publication. The author declares that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest. Alonso, P. The avian nature of the brain and inner ear of Archaeopteryx.
Nature , — Barlow, H. The neural mechanism of binocular depth discrimination. Bhagavatula, P. Optic flow cues guide flight in birds. Bunce, M. The evolutionary history of the extinct ratite moa and New Zealand Neogene paleogeography. Chiappe, L. Hoboken, NJ: John Wiley. Coimbra, J. Topographic specializations in the retinal ganglion cell layer of Australian passerines.
Variations in retinal photoreceptor topography and the organization of the rod-free zone reflect behavioral diversity in Australian passerines. Cresswell, W.
An Ecological Approach
Predation in bird populations. Davies, M. Berlin: Springer-Verlag. Google Scholar. Davies, N.
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An Introduction to Behavioural Ecology, 4th Edn. Oxford: Wiley-Blackwell. Devereux, C. Predator detection and avoidance by starlings under differing scenarios of predation risk. Dolan, T. Retinal ganglion cell topography of five species of ground-foraging birds. Brain Behav. Endler, J. Comparing entire colour patterns as birds see them. Animal visual systems and the evolution of color patterns: sensory processing illuminates signal evolution.
Evolution 59, — Visual perception and social foraging in birds. However, all of these examples have involved a complete loss of vision following colonisation of subterranean habitats devoid of light. In Kiwi, complete regression of the eye and parts of the brain associated with visual information processing has not occurred. However, while Kiwi roost and nest in burrows, their foraging habitats are not completely devoid of light .
Given that other flightless birds have some of the largest eyes among terrestrial vertebrates and that many flying birds of similar or smaller mass have eyes that are larger than those of Kiwi  , it would seem that the higher cost of transport in locomotion of larger eyes is not sufficient to explain eye regression in Kiwi. We propose that regressive evolution of Kiwi vision is the result of the trade-off between the requirement for a large eye to gain information at low light levels, and the metabolic costs of extracting and processing that information .
It seems possible that there is an ambient light level below which the costs of maintaining a large eye and associated visual centres are not balanced by the rate at which information can be gained, and that this occurs in forest floor habitats at night. Kiwi are a group of endangered species protected under New Zealand law. We were able to work on these birds for research purposes only under strict guidelines and permits kindly issued by the New Zealand Department of Conservation and animal ethics approvals from Lincoln University.
Both birds were adults and were not part of any breeding programme.
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To reduce disturbance to the birds, measurements were conducted on the birds' holding premises and the birds were returned to their aviaries immediately after measurements were complete. To ensure comparability of these measurement with those conducted on other birds the same procedures were used as described previously for work with a range of species e. Oilbirds Steatornis  , Flamingos Phoeniconaias .
Each bird was restrained with the body immobilised and the head position fixed by holding the bill. The bill was held in a specially built metal holder coated with cured silicone sealant to produce a non-slip surface. The bill holder was mounted on an adjustable mechanism and the head positioned so that the mid-point of a line joining the corneal vertices was at the approximate centre of a visual perimeter apparatus  that enabled the eyes to be examined ophthalmoscopically from known co-ordinates centred on the head.
The perimeter's co-ordinate system followed conventional latitude and longitude with the equator aligned vertically in the birds' median sagittal plane and this co-ordinate system is used for the presentation of the visual field data Fig. This head position approximated that which the birds adopted spontaneously when held in the hand. The projection of the bill tip when measurements were made was determined accurately from photographs and the visual field data corrected for this.
The eyes were examined using an ophthalmoscope mounted on the perimeter arm. To the rear of the head the limits of retinal visual field were determined at all elevations down to the horizontal. From these data corrected for viewing from a hypothetical viewing point placed at infinity topographical maps of the frontal visual fields and horizontal sections through the visual fields were constructed.
Skins of kiwi were examined and photographed at the collections held by the Natural History Museum Tring, UK , and skeletal materials were examined and photographed at the collections held by the Canterbury Museum Christchurch, New Zealand. Eye size and brain structure were determined from post mortem specimens of A. M Wild lab. Sections were collected in PBS. Every sixth section was mounted serially onto subbed slides, stained with Cresyl Violet, dehydrated and coverslipped. All tectal measurements were obtained from serial sections stained with Cresyl Violet, except for the pigeon where some measurements were taken from A Stereotaxic Atlas of the Brain of the Pigeon .
Measurements were obtained from 11 kiwi, 20 Emu, 14 Barn Owl, and 31 Pigeon sections. Tectal thickness was measured from the midpoint of the midbrain ventricle, orthogonally to the tectal surface. No claims as to the specificity of antibody binding are made and, therefore, we refer to the calretinin-like immunoreactivity as CR-LI. Sections were incubated overnight at room temperature in the primary antibody in the presence of 2.
In some cases, 0. All steps in this and all other incubation procedures were separated by washes in the incubation buffer. The tissue was mounted onto subbed slides, dehydrated, and coverslipped with Permount. The material was photographed on a light table using a standard photographic camera.
The images were processed with Adobe PhotoShop v. Emu brains were kindly provided by R. Pennell at Northland Ostrich and Emu Ltd. We are grateful to N. Duggan for assistance in producing brain photographs. We are also indebted to the New Zealand Department of Conservation for their support during this project and for permits to handle live birds.
In particular we thank C. Gardner and P. Graham for their invaluable assistance in obtaining kiwi specimens. Browse Subject Areas? Click through the PLOS taxonomy to find articles in your field. Abstract Background In vision, there is a trade-off between sensitivity and resolution, and any eye which maximises information gain at low light levels needs to be large. Introduction Flight in birds is guided primarily by vision since, with the exception of high frequency echolocation found only in bats  , no other sensory modality can provide spatial information at sufficient speed and resolution to guide flight .
Download: PPT. Figure 2. Visual processing areas of the brains of four species of birds. Figure 3. Boxplot of normalised tectal thicknesses of the four bird species. Figure 6. Principal sensory trigeminal nucleus and olfactory bulb. Discussion We have presented a range of information suggesting that although Kiwi are apparently free from weight constraints upon eye size that apply to flying birds, and that their nocturnal habits would predict a large eye size, their eyes and visual fields are in fact very small, and the visual centres serving vision are very much reduced while centres processing olfactory and tactile information are relatively large.
Materials and Methods Specimens Kiwi are a group of endangered species protected under New Zealand law. Anatomy Skins of kiwi were examined and photographed at the collections held by the Natural History Museum Tring, UK , and skeletal materials were examined and photographed at the collections held by the Canterbury Museum Christchurch, New Zealand. References 1. New York: Plenum Press. Perception and motor control in birds: an ecological approach. Berlin: Springer-Verlag. Oxford: Oxford University Press. Michigan: Cranbrook Institute of Science.
About this book Being both broad - perception and motor organization - and narrow - just onegroup of animals - at the same time, this book presents a new unified framework for understanding perceptuomotor organization, stressing the importance of an ecological perspective. Show all. Mark N. Show next xx.
Read this book on SpringerLink. Recommended for you. Davies Patrick R.