Vision is both complex and multidimensional, so considerable ingenuity, involving a range of anatomical, physiological and behavioural techniques, has been used to isolate particular capacities and their underlying mechanisms in birds and other animals. Not all aspects of visual capacity are equally well understood but there are four key areas that are important to consider when attempting to understand the vulnerability of birds to collisions.
The function of colour vision is to enhance the detection of objects by extracting information about their differential reflection in the spectrum. It is sobering to realise that colour, which appears such an important part of our world view, is not a property of the physical world but a construct of the visual system that analyses it (Wright 1963). It has long been recognized that the colour vision mechanism of avian retinas differs in quite fundamental ways from that of mammals, and its mechanisms have been summarized a number of times as knowledge has grown (Walls 1942, Jacobs 1981, Bowmaker et al. 1997, Land & Nilsson 2002, Martin & Osorio 2008, Hunt et al. 2009). Although there are differences among bird species, the fundamental property of avian colour vision compared with mammals, and particularly primates, lies in the extent of the visible spectrum and the subtlety of colour discrimination that can be made within that spectrum. It was first recognized that birds have colour vision which extends into the ultraviolet, thus broadening (compared with humans) the range of stimuli to which the avian eye can respond, through behavioural studies of Rock Pigeons Columba livia (Wright 1972, Emmerton & Delius 1980) and later of hummingbirds (Trochilidae) (Goldsmith 1980). Subsequently, behavioural and physiological work has shown that vision in the UV or near-UV part of the spectrum is widespread among avian families (Cuthill et al. 2000, Hunt et al. 2009). In view of the wide taxonomic distribution of vision in the UV region among birds, it would now seem safe to assume that the visible spectrum of most birds extends into the UV and that vision in this part of the spectrum should no longer be viewed as exceptional.
The few detailed psychophysical studies of colour discrimination in birds suggest that birds are capable of subtle discriminations throughout their visible spectrum, including the UV and near-UV (Wright 1979). This has been supported by general models of how the different types of retinal cone photoreceptors in birds mediate colour discrimination (Vorobyev & Osorio 1998, Vorobyev 2003, Endler & Mielke 2005).
Resolution (the precision with which an eye splits up light according to its direction of origin) is usually referred to as acuity. It is tempting to characterize this with a single value of best performance for a particular species. This value describes the smallest spatial detail that can be resolved under high light levels using stimuli of high contrast, giving a basis for interspecific comparisons and allowing estimates to be made of the finest details or smallest object that can be detected at a certain distance under ideal viewing conditions. However, natural stimuli are often of lower contrast and a full characterization of spatial resolution requires the determination of a spatial contrast function which characterizes visual thresholds across a range of contrasts and spatial frequencies (Ghim & Hodos 2006). As with colour vision, there are few behavioural studies of contrast sensitivity or even acuity in birds, but it has been possible to estimate acuity from knowledge of the structure of the retina in a number of species. Two key findings come from these studies. First, acuity in birds is high compared with those in other vertebrates with eyes of similar size, suggesting that the eyes of the majority of diurnally active birds can be characterized as adapted to maximize resolution rather than sensitivity (Land & Nilsson 2002). However, despite earlier claims based upon anecdotal observations, the highest known acuity in birds is not exceptionally superior to that of humans. For example, earlier claims of exceptional acuity in falcons and eagles have been more recently revised downwards to suggest that the highest acuity of falcons (0.4–0.75 min of arc) is approximately equal to that of the eye of a young human (0.4–1.0 min of arc: Fox et al. 1976, Hirsch 1982, Reymond 1987, Land & Nilsson 2002, Gaffney & Hodos 2003), while that of the largest eagles (0.2 min of arc) is perhaps 2.5 times higher than that of human eyes (Reymond 1985). For many bird species, acuity is below that of the human fovea at similar light levels, for example Rock Pigeon, 1.7 min of arc; Rook Corvus frugilegus, 1.0 min of arc; domestic fowl Gallus domesticus, 3.4 min of arc (Hodos 1993).
Secondly, acuity varies markedly within the visual field of an eye. In humans, there is a single region of high acuity vision which projects directly forwards, typically in the direction of travel. This region is of small angular size (≈ 2° diameter) compared with the total visual field (≈ 160°) and is mediated by the foveal region of the retina (Westheimer 1972). Acuity decreases rapidly towards the periphery of the eye’s visual field. In birds there may be two areas of high acuity in each eye (Meyer 1977). One typically projects laterally with respect to the axis of the head, approximately along the optical axis of the eye, but there may be other frontal or ventrally projecting areas of higher acuity, or even an area of higher acuity that extends in a band across the field of view. There have been a number of attempts to explain the occurrence and visual projection of these areas of high acuity by reference to the visual challenges that life in different habitat types present (Meyer 1977, Martin 1985). Typically, the regions of highest acuity occur laterally, not frontally, with respect to the head and when behavioural techniques are used in assessments of a bird’s acuity, a bird usually chooses to use its lateral field of view. Anatomical evidence also corroborates the use of these laterally projecting regions for tasks involving the determination of the highest visual acuity by freely moving birds (Reymond 1985, 1987).
Relative depth, distance and time to contact
Determination of the position of an object in relative depth from an animal, as well as its absolute distance, is a complex perceptual process for any visual system (Goldstein 1984, Bruce et al. 2003). However, it is clearly a process that is central to understanding collisions.
Estimation of depth and distance are not a property of the eye alone, but a perception based upon higher order processing by the brain. In humans, relative depth close to the observer is usually analysed by reference to the process of stereopsis (Bruce et al. 2003). Perception of the distance of objects further away depends upon cues that are available in each eye alone but which also require a high degree of cognitive processing. Stereopsis is based upon the small differences in the images of the same object produced on the retinas of the two eyes, which occur because of the lateral displacement of the eyes in the skull. Human eyes are relatively far apart compared with birds and even in humans the process of stereopsis provides relative depth information for only a few metres ahead and is typically employed for tasks conducted closer to the eyes (e.g. manipulation of objects by the hands). Whether birds whose eyes are relatively close together (typically, avian eyes almost touch in the median sagittal plane of the skull) are able to employ stereopsis to gain relative depth information is uncertain. An early behavioural demonstration of stereopsis in a falcon (Fox et al. 1977) has not been replicated or extended more generally among bird species, although McFadden (1994) found some behavioural evidence of stereopsis for close objects in pigeons. More recently, Martin (2009) has argued that birds, with perhaps the exception of some owl species (Strigidae, Tytonidae), do not have stereopsis and that the function of binocular vision lies primarily in the control of the bill (and/or feet in some species) towards objects at close range, and not for the control of locomotion towards more remote targets. Martin (2009) also argues that for any bird, the most vital visual information beyond recognition of an object is the object’s position and, if there is relative speed between the object and the observer, information on time to contact. The actual distance of an object from a bird may be of little importance compared with its direction and the time it may take to make contact with it.
Such information is available from optic flow-fields (Lee & Lishman 1977, Lee 1980, Warren 2008) and it has been shown that Northern Gannets Morus bassanus and hummingbirds, when carrying out manoeuvres that require accurate visual information regarding time to contact a target, appear to employ optic flow-field information (Lee & Reddish 1981, Lee et al. 1991). The informational properties of optic flow-fields were first analysed in detail by Gibson (1966) and derive directly from the way images of objects flow across the retina as they move relative to the observer (Warren 2008). They can specify very accurately both the direction of travel and the time to contact with an object that is being approached and they may underpin many tasks undertaken by humans, such as driving, cycling, running, jumping and ball-catching: tasks in which the observer has to adjust speed of approach to achieve accurate timing of arrival at a given point (Lee 1980). However, the information extracted from the optic flow-field across the retina is contained not in highly detailed spatial information but in information extracted from moving images at relatively low resolution.
Fields of view
Visual fields and the variation of visual capacities within them are likely to have a direct impact on collision susceptibility. This is because, regardless of the ways in which visual information is processed, visual fields determine what part of an animal’s environment can influence its behaviour at any one instant (Martin 2007, 2009) and because visual capacities can vary markedly within the visual field (Martin & Osorio 2008). This is true of humans, where there are marked changes in visual capacity from central to peripheral vision within an eye, but such differences appear to be more extreme within avian eyes. Especially important are the characteristics of that section of a bird’s visual field that are used to detect and analyse objects of interest, and the characteristics and general functions of the section of the visual field that projects forward and hence ‘looks’ in the direction of travel.
In humans, that section of the visual field that is used for detailed analysis of objects looks directly forward, and there is a very extensive region of forward binocular vision that constitutes the major portion of the total visual field (Fig. 2). However, this is not the case in most, perhaps all, birds. For humans, the detailed world lies ahead, whereas for the majority of birds the detailed world lies laterally. Furthermore for birds (indeed any animals with eyes placed laterally in the skull), forward/binocular vision is achieved through the peripheral vision of the each eye; in other words vision at the edge of the visual field of an individual eye, away from the optical axis (Fig. 2). In contrast, in most manufactured optical systems, such as binoculars, the quality of optics in the periphery is always inferior to the quality of optics along the optical axis of the system. As little is known about the quality of peripheral optics in bird eyes, it is not possible to be sure that when birds look forward with their binocular field, which is typically a very small portion of the total visual field (Fig. 2), they are employing the best quality optics.
Figure 2. Visual fields in Kori Bustards, humans and White Storks. The differences between a ‘human eye view’ and a ‘birds’ eye view’ are readily apparent from these diagrams. Bustards are particularly prone to collisions with power lines of the kind depicted in Figure 1. Storks, although vulnerable to collisions with such power lines, are more likely to be electrocuted by low-tension power wires (because their wide wing span is sufficient to earth between two current-carrying wires in low-tension power transmission systems). The figure is a matrix that allows interspecific comparison of the same information across rows, while columns show information for each species. Row (a): perspective views of orthographic projections of the boundaries of the retinal fields of the two eyes and in the birds the line of the eye–bill tip projections (indicated by a white triangle). The direction of the optic axes of the eyes is indicated by a white pentagon. The diagrams use conventional latitude and longitude coordinate systems with the equator aligned vertically in the median sagittal plane of the head. The grid is at 20° intervals. It should be imagined that in each diagram the head is positioned at the centre of a transparent sphere with the field boundaries and optic axes projected onto the surface of the sphere with the heads in the orientations shown in row (c). Green areas, binocular sectors; pink areas, monocular sectors; blue areas, blind sectors. Row (b): horizontal sections through the visual fields in a horizontal plane defined by the straight line running through the middle of each of the visual field projections shown in row (a). Dashed lines indicate the directions of the optic axes. In the birds, the axis of each eye projects laterally, in humans, the optic axes of each eye project forward and coincide (colour coding of each sector of the visual fields as in row (a)). Row (c): vertical sections through the binocular fields (green) in the median sagittal plane defined by the vertically oriented equators of the diagrams in row (a). The line drawings of the heads of the birds show them in the approximate orientations typically adopted by the species in flight. In humans, the head is in a typical upright posture. The visual fields are presented with respect to these typical head positions. Key features of visual fields in birds that forage using visual guidance are shown in the case of the bustards and storks. These are features typical of the majority of bird species (Martin 2007). The eyes project laterally and the best optical quality and the direction of best resolution projects laterally. The binocular field is narrow and vertically long with the bill projecting approximately centrally; there is extensive visual coverage by each eye to the side and behind the head, resulting in a small blind sector above and to the rear of the head. In humans the visual field is arranged very differently from those of the two birds. The eyes project forwards and almost the whole of the visual field is binocular, there is a large blind area behind the head and the best optical quality and highest resolution lie directly ahead. One crucial difference between the two bird species depicted here lies in the vertical extent of their binocular fields and the effect of moving the head on visual coverage of the frontal hemisphere. In bustards, a relatively small forward head pitch of 25° (rows a and c) is sufficient to bring the extensive blind area above the head to project forwards in the direction of forward travel. However, in storks, visual coverage of the frontal field is not abolished until the head has pitched forward by 55°, which would mean that the bill is pointing vertically downwards. This amplitude of head movement that is necessary to abolish forward vision is similar to that required for the same effect in humans. The visual field of bustards is similar to those found in cranes and eagles, which are also highly vulnerable to collisions with artefacts. The visual field of storks is similar to those found in other members of the Ciconiformes and in duck species (Martin 2007). The figure is based upon Martin and Shaw (2010).
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The visual field of an animal is a function of the optics of the eyes and of their placement in the head, and among birds a number of visual field arrangements have been described (Martin 2007) (Fig. 2). Visual fields need to serve two key functions: (1) the detection of predators, conspecifics, obstacles and potential food sources that are remote from the animal, and (2) the control of accurate behaviours, such as the procurement of food items, at close quarters. Both functions are potent sources of natural selection but they are potentially antagonistic (Fernandez-Juricic et al. 2008, Martin & Piersma 2009). While there is evidence that some birds have optical systems that keep both distant and close objects in focus without the need to change the refractive state of the eye, this occurs in the laterally projecting visual field, not the frontal projection of the field (Martin 1986b, Hodos & Erichsen 1990). The human eye, with its frontal orientation, has continuously to accommodate for objects that lie ahead at different distances.
In bird species that employ visual information for the guidance of bill position when taking food items, the projection of the bill falls approximately centrally within the binocular (frontal) section of the visual field, and in the majority of birds that feed in this way, the binocular field is relatively narrow, between 15° and 30° in maximum width, and vertically long (Martin 2007) (Fig. 2). However, the vertical extent of the binocular field varies markedly. For example, in herons (Ardeidae) and storks (Ciconiidae), it extends through 180°, so that these birds have comprehensive visual coverage of the hemisphere in front of the head (Martin & Katzir 1994), while in eagles, bustards and cranes it extends through only 80°, vertically giving these birds extensive blind areas both above and below the head in the frontal hemisphere (Martin & Katzir 1999, Martin & Shaw 2010) (Fig. 2). In birds that do not employ visual information to guide bill position (e.g. some duck species which filter-feed, and some long-billed shorebirds which feed by probing in soft substrates guided by tactile cues), the bill falls at the very periphery or outside the visual field. In these cases the eyes are positioned high in the skull, giving comprehensive visual coverage of the hemisphere around and above the head such that there are no blind areas in their visual field except that produced by their own body (Martin 2007, Martin et al. 2007).
Eye movements are present in many bird species and these are typically independent complex rotations of the eyes that can have markedly different effects on visual coverage around the head. In a number of species (e.g. herons, hornbills and cormorants; Martin & Katzir 1994, Martin & Coetzee 2004, Martin et al. 2008), it has been shown that binocularity to the front of the head can be abolished by eye movements. Such abolition of binocularity occurs frequently when birds are held in the hand, suggesting that they switch spontaneously between binocular coverage of frontal field and its abolition. The function of such abolition of frontal binocular vision is unclear but it may be an incidental consequence of using the region of an eye’s best optical quality, which projects along the optic axis laterally, to examine an object or track its movement (Martin et al. 2008).
In birds, the function of binocular vision appears primarily to be the control of behaviours requiring the accurate positioning and timing of bill-opening towards objects close to the animal (particularly the control of bill position for food procurement and/or chick provisioning); the control of locomotion with respect to more distant objects is a less important determinant of binocular field characteristics (Martin 2009). Indeed, for birds such as the filter-feeding ducks or probing shorebirds, the binocular field can be very narrow (≈ 5°) in the direction of travel when flying. Furthermore, it seems likely that in many birds the detection of food items is primarily under the control of lateral vision, with control of item procurement transferred to forward vision just prior to seizure (Montgomerie & Weatherhead 1997, Land 1999, Tucker 2000, Tucker et al. 2000, Rogers 2008).