The visual field of an animal determines what part of its surrounding environment can influence its behaviour at any one instant (Martin 2007
). Visual fields need to serve two key functions: (i) the detection of predators, conspecifics, potential prey and obstacles, which are remote from the animal, and (ii) 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 (Fernández-Juricic et al. 2004
). This antagonism is well illustrated in birds.
In species that employ visual information for the guidance of the bill position when taking food items, the projection of the bill falls approximately centrally within the frontal binocular section of the visual field (Martin 2007
). This arrangement facilitates the accurate determination of direction of travel towards, and time to contact, an object by the bill. This information is derived primarily from the radially symmetrical linear optic flow field that is generated during forward motion (Gibson 1986
; Davies & Green 1994
; Martin & Katzir 1999
). However, this more forward position of the eyes that is necessary to achieve a binocular field surrounding the projection of the bill always results in a blind area behind the head, rendering the animal more vulnerable to predation (Guillemain et al. 2002
; Fernández-Juricic et al. 2004
; Martin 2007
The importance of reducing vulnerability to predator attack is indicated by examples of birds in which non-visual information is used to guide foraging. These birds no longer need to derive accurate information about the direction and speed of travel of the bill relative to a target, and in these species the bill falls at the very periphery or entirely outside the visual field. Often, the eyes are placed high in the skull giving comprehensive panoramic vision around and above the head (Martin 2007
). Such visual field topography is found, for example, in the tactile-feeding Eurasian woodcocks Scolopax rusticola
) and a number of filter-feeding duck species: mallards, Anas platyrhynchos
; northern shovelers, Anas clypeata
; and pink-eared ducks, Malacorhynchus membranaceus
; Guillemain et al. 2002
; Martin et al. 2007a
). Thus, among birds, when accurate visual guidance of the bill position is not necessary, natural selection seems to have favoured comprehensive visual coverage of the hemisphere above and around the head to aid the detection of predators (Guillemain et al. 2002
; Martin 2007
). However, tactile or filter feeding does not necessarily lead to the evolution of panoramic vision. In black skimmers (Rynchops niger
), tactile feeding requires the visual inspection of prey items after they have been caught while ‘blind trawling’ (Martin et al. 2007a
), and, in filter-feeding lesser flamingos (Phoeniconaias minor
), accurate bill positioning under the control of visual cues is required for the feeding of young with oesophageal milk (Martin et al. 2005
). Neither species has comprehensive panoramic vision and the projections of their bills fall centrally within a frontal binocular field.
The general principles outlined above have been based upon comparisons between relatively few species that have quite separate evolutionary origins. Here, we describe differences in visual field topography between species with similar ecologies and within a single avian order. We show that differences in visual fields can be attributed to subtle differences in foraging ecology, indicating an evolutionary trade-off between the demands of using vision for accurate guidance during foraging and the detection of predators.
Among the Charadriiformes are two taxa of shorebirds that forage in similar open habitats but are divided into short-billed forms (plovers, Charadriidae), which primarily take surface-living or shallow-dwelling invertebrates, and a separate radiation of longer billed forms (sandpipers and their allies, Scolopacidae), which take invertebrate prey, often buried in soft substrates (Piersma & Wiersma 1996
; Piersma et al. 1996
). The foraging of plovers is regarded as guided primarily by visual, and possibly auditory (Fallet 1962
), cues, while foraging sandpipers are guided primarily by tactile information derived from receptors (Herbst and Grandry corpuscles) located within sensory pits in the bone around the bill tips (Bolze 1968
; Piersma et al. 1998
; Nebel et al. 2005
). Species of both families have precocial chicks, and therefore do not need to employ visual cues for the accurate placement of the bill when provisioning chicks.
We hypothesized that the visual fields and eye positions within the skull of birds from these two families would reflect their differential use of visual and tactile information in the guidance of their foraging. Here, we have compared two species: red knots (Calidris canutus
), which can locate buried prey using exclusively tactile cues (Piersma et al. 1998
), and European golden plovers (Pluvialis apricaria
), which are regarded as visually guided foragers (Barnard & Thompson 1985
). We predicted that red knots would have their eyes located high in the skull, resulting in visual fields with similar topography to that of the tactile-foraging Eurasian woodcocks, i.e. a narrow binocular field (less than 10° maximum width) extending throughout the median sagittal plane above the head providing total panoramic vision of the celestial hemisphere, and the projection of their bill falling outside the visual field (Martin 1994
). By contrast, golden plovers were predicted to have visual field topography similar to those of other visually guided foraging birds in which the bill projects centrally within a broader binocular field (15–25° wide), and the more frontal placement of the eyes results in a blind area above and to the rear of the head.