Differences in foraging ecology determine variation in visual fields in ibises and spoonbills (Threskiornithidae)

Variations in visual field topography among birds have been interpreted as adaptations to the specific perceptual challenges posed by the species’ foraging ecology. To test this hypothesis we determined visual field topography in four bird species which have different foraging ecologies but are from the same family: Puna Ibis Plegadis ridgwayi (probes for prey in the soft substrates of marsh habitats), Northern Bald Ibis Geronticus eremita (surface pecks for prey in dry terrestrial habitats), African Spoonbill Platalea alba and Eurasian Spoonbill Platalea leucorodia (bill‐sweeps for prey in shallow turbid waters). All four species employ tactile cues provided by bill‐tip organs for prey detection. We predicted that the visual fields of these species would show general features similar to those found in other birds whose foraging is guided by tactile cues from the bill (i.e. bill falling outside the frontal binocular field and comprehensive visual coverage of the celestial hemisphere). However, the visual fields of all four species showed general features characteristic of birds that take food directly in the bill under visual guidance (i.e. a narrow and vertically long binocular field in which the projection of the bill tip is approximately central and with a blind area above and behind the head). Visual fields of the two spoonbills were very similar but differed from those of the ibises, which also differed between themselves. In the spoonbills, there was a blind area below the bill produced by the enlarged spatulate bill tip. We discuss how these differences in visual fields are related to the perceptual challenges of these birds’ different foraging ecologies, including the detection, identification and ingestion of prey. In particular we suggest that all species need to see binocularly around the bill and between the opened mandibles for the identification of caught prey items and its transport to the back of the mouth. Our findings support the hypothesis that sensory challenges associated with differences in foraging ecology, rather than shared ancestry or the control of locomotion, are the main determinants of variation in visual field topography in birds.     

White‐headed Vulture Trigonoceps occipitalis shows visual field characteristics of hunting raptors

The visual fields of the Aegypiinae vultures have been shown to be adapted primarily to meet two key perceptual challenges of their obligate carrion‐feeding behaviour: scanning the ground and preventing the sun's image falling upon the retina. However, field observations have shown that foraging White‐headed Vultures Trigonoceps occipitalis are not exclusively carrion‐feeders; they are also facultative predators of live prey. Such feeding is likely to present perceptual challenges that are additional to those posed by carrion‐feeding. Binocularity is the key component of all visual fields and in birds it is thought to function primarily in the accurate placement and time of contact of the talons and bill, especially in the location and seizure of food items. We determined visual fields in White‐headed Vultures and compared them with those of two species of carrion‐eating Gyps vultures. The visual field of White‐headed Vultures has more similarities with those of predatory raptors (e.g. accipitrid hawks) than with the taxonomically more closely related Gyps vultures. Maximum binocular field width in White‐headed Vultures (30°) is significantly wider than that in Gyps vultures (20°). The broader binocular fields in White‐headed Vultures probably facilitate accurate placement and timing of the talons when capturing evasive live prey.     

Vision and the foraging technique of Great Cormorants Phalacrocorax carbo: pursuit or close‐quarter foraging?

Predatory diving birds, such as cormorants (Phalacrocoracidae), have been generally regarded as visually guided pursuit foragers. However, due to their poor visual resolution underwater, it has recently been hypothesized that Great Cormorants do not in fact employ a pursuit-dive foraging technique. They appear capable of detecting typical prey only at short distances, and primarily use a foraging technique in which prey may be detected only at close quarters or flushed from a substratum or hiding place. In birds, visual field parameters, such as the position and extent of the region of binocular vision, and how these are altered by eye movements, appear to be determined primarily by feeding ecology. Therefore, to understand further the feeding technique of Great Cormorants we have determined retinal visual fields and eye movement amplitudes using an ophthalmoscopic reflex technique. We show that visual fields and eye movements in cormorants exhibit close similarity with those of other birds, such as herons (Ardeidae) and hornbills (Bucerotidae), which forage terrestrially typically using a close-quarter prey detection or flushing technique and/or which need to examine items held in the bill before ingestion. We argue that this visual field topography and associated eye movements is a general characteristic of birds whose foraging requires the detection of nearby mobile prey items from within a wide arc around the head, accurate capture of that prey using the bill, and visual examination of the caught prey held in the bill. This supports the idea that cormorants, although visually guided predators, are not primarily pursuit predators, and that their visual fields exhibit convergence towards a set of characteristics that meet the perceptual challenges of close-quarter prey detection or flush foraging in both aquatic and terrestrial environments.     

Visual fields and foraging ecology of Blacksmith Lapwings Vanellus armatus

The visual fields of Blacksmith Lapwings Vanellus armatus show the characteristics of visual guided foragers that use precision pecking for prey capture – a binocular field of narrow width and limited vertical extent, with the projection of the bill close to its centre and a large blind area above and behind the head. The topography of the total field, particularly the binocular field, is similar to that of European Golden Plovers Pluvialis apricaria. We suggest that the ‘foot‐trembling’ behaviour associated with foraging in Plovers is not under visual guidance but forces the escape of hidden prey, which is detected when the prey item moves into the binocular field to enable its capture in the bill. Foot‐trembling thus functions to extend the effective foraging area of a bird beyond the limits of its visual field.     

Vision and the foraging technique of skimmers (Rynchopidae)

In birds, the position and extent of the region of binocular vision appears to be determined primarily by feeding ecology. Of prime importance is the degree to which vision is used for the precise control of bill position when foraging. Skimmers (Rynchops, Rynchopidae, Charadriiformes) exhibit a unique foraging behaviour and associated structural adaptations. When foraging they fly low and straight over water with the mouth open and the mandible partially submerged. Items that are hit by the lower mandible are grasped by a rapid reflex bill closure. It is believed that this unique ‘skimming’ foraging technique is guided by tactile rather than visual cues. It is predicted therefore that the visual fields of skimmers will have similar topography to those of other tactile feeding birds. We determined retinal visual fields in Black Skimmers Rynchops niger using an ophthalmoscopic reflex technique. Contrary to expectation the visual fields of Black Skimmers are not like those of other tactile feeders. They show high similarity with those of birds that feed by precision‐pecking. The projection of the bill tip when the mouth is closed and when open (as in skimming) falls within the frontal binocular field and there is an extensive blind area above and behind the head. We argue that this visual field topography functions to achieve accurate bill positioning with respect to the water surface when skimming and, because foraging skimmers cannot determine the identity of what they are seizing as they skim, to permit the visual identification of prey items held between the mandibles after they have been taken from the water surface. When skimming, only a small portion of the binocular field, approximately 5° wide and extending 5° above the horizontal, looks in the direction of travel. The small size of this forward‐facing region of binocularity in skimmers suggests that control of locomotion in birds does not necessarily require extensive binocularity in the direction of travel.     

The subtlety of simple eyes: the tuning of visual fields to perceptual challenges in birds

Birds show interspecific variation both in the size of the fields of individual eyes and in the ways that these fields are brought together to produce the total visual field. Variation is found in the dimensions of all main parameters: binocular region, cyclopean field and blind areas. There is a phylogenetic signal with respect to maximum width of the binocular field in that passerine species have significantly broader field widths than non-passerines; broadest fields are found among crows (Corvidae). Among non-passerines, visual fields show considerable variation within families and even within some genera. It is argued that (i) the main drivers of differences in visual fields are associated with perceptual challenges that arise through different modes of foraging, and (ii) the primary function of binocularity in birds lies in the control of bill position rather than in the control of locomotion. The informational function of binocular vision does not lie in binocularity per se (two eyes receiving slightly different information simultaneously about the same objects from which higher-order depth information is extracted), but in the contralateral projection of the visual field of each eye. Contralateral projection ensures that each eye receives information from a symmetrically expanding optic flow-field from which direction of travel and time to contact targets can be extracted, particularly with respect to the control of bill position.     

The visual fields of two ground‐foraging birds,House Finches and House Sparrows,allow for simultaneous foraging and anti‐predator vigilance

In birds, differences in the extent and position of the binocular visual field reflect adaptations to varying foraging strategies, and the extent of the lateral portion of the field may reflect anti‐predator strategies. The goal of this study was to describe and compare the visual fields of two ground‐foraging passerines, House Finch Carpodacus mexicanus and House Sparrow Passer domesticus. We found that both species have a binocular field type that is associated with the accurate control of bill position when pecking. Both species have eye movements of relatively large amplitude, which can produce substantial variations in the configuration of the binocular fields. We propose that in these ground foragers, their relatively wide binocular fields could function to increase foraging efficiency by locating multiple rather than single food items prior to pecking events. The lateral fields of both species are wide enough to facilitate the detection of predators or conspecifics while head‐down foraging. This suggests that foraging and scanning are not mutually exclusive activities in these species, as previously assumed. Furthermore, we found some slight, but significant, differences between species: House Sparrow binocular fields are both wider and vertically taller, and the blind area is wider than in House Finches. These differences may be related to variations in the degree of eye movements and position of the orbits in the skull.     

Eye structure and foraging in King Penguins Aptenodytes patagonicus

Anterior eye structure and retinal visual fields were determined in King Penguins Aptenodytes patagonicus using keratometry and an ophthalmoscopic reflex technique. The cornea is relatively flat (radius 32.9 mm) and hence of low refractive power (10.2 dioptres in air) and this may be correlated with the amphibious nature of penguin vision. The large size of the eye and of the fully dilated pupil may be correlated with activity at low light levels. In air, the binocular field is long (vertical extent 180̀) and narrow (maximum width 29̀), with the bill placed approximately centrally—a topography found in a range of bird species which employ visual guidance of bill position when foraging. Upon immersion in water, the optical power of the cornea is abolished, with the effect that the monocular fields decrease and binocularity is lost. King Penguins have a pupil type which has not hitherto been recorded in birds. In daylight it contracts to a square-shaped pinhole but dilates to a large circular aperture in darkness. This change alters retinal illumination by 300-fold (2.5 log₁₀ units). When diving, this permits the retina to be pre-adapted to the low ambient light levels that the birds encounter upon reaching mesopelagic depths. These penguins also forage at depths where ambient light levels, even during the day, can fall below the equivalent of terrestrial starlight. Under these conditions, the birds must rely upon the detection of light from the photophores of their prey. In this they are aided by their absolutely large pupil size and broad cyclopean visual field.     

Visual fields in Blue Ducks Hymenolaimus malacorhynchos and Pink-eared Ducks Malacorhynchus membranaceus: visual and tactile foraging

Blue Ducks Hymenolaimus malacorhynchos (Anatidae), an IUCN Red Listed Endangered species, reside in headwaters of New Zealand rivers and feed primarily on aquatic invertebrates. However, whether such food items are detected by tactile or visual cues is unknown. That Blue Ducks may use tactile cues when foraging is suggested by the presence of specialized flaps of thickened, keratinized epidermis containing Herbst's corpuscles along the ventral margins of the upper mandibles near the bill tip. Similar bill flaps are found only in one other duck species, Pink-eared Ducks Malacorhynchus membranaceus , that surface filter-feed on a range of planktonic organisms. Using an ophthalmoscopic reflex technique we determined the visual fields of both species. In Blue Ducks the eyes are frontally placed resulting in a relatively wide binocular field into which the narrow tapering bill intrudes. There is a large blind area to the rear of the head. This visual field topography is similar to that of other visually guided foragers including those that take mobile prey from the water column, e.g. penguins (Spheniscidae). By contrast, Pink-eared Duck visual fields show features found in other tactile feeding ducks: a narrow frontal binocular field with the bill falling at the periphery, and comprehensive visual coverage of the celestial hemisphere. We conclude that although Blue Ducks may take prey from rock surfaces they are primarily visual feeders of the water column and we suggest therefore that their foraging may be significantly disrupted by changes in water clarity. This introduces a previously unconsidered factor into the selection of sites for population enhancement or re-introductions, a current conservation focus.     

Visual fields in woodcocks Scolopax rusticola (Scolopacidae; Charadriiformes)

Woodcocks, Scolopax rusticola, are long-billed terrestrial wading birds (Scolopacidae; Charadriiformes) which forage primarily by probing in soft substrates for invertebrates. Visual field topography in restrained alert birds was investigated using an ophthalmoscopic reflex technique.

1. Eye movements of significant amplitude are absent.
2. The retinal binocular field is long and narrow. It extends through 190° in the median sagittal plane. When the head adopts a normal posture (bill at an angle of 40° below the horizontal) the binocular field stretches from 25° above the bill to 5° above the horizontal behind the head. Thus, woodcocks have comprehensive visual coverage of the hemisphere above them but the bill falls outside the visual field. Maximum binocular field width equals 12° and occurs perpendicular to the line of the bill. To the rear of the head binocular field width is less than 5° except in an area 40° above the horizontal where it increases to 7°.
3. Monocular retinal fields in the horizontal plane are 182° wide. There is no blind sector at the margin of the optical fields.
4. The general structure of woodcock skulls facilitates panoramic vision in a horizontal plane.
5. Interspecific comparisons are consistent with the hypothesis that visual field topography among birds is closely associated with the role of vision in foraging. Comprehensive visual coverage of the celestial hemisphere probably occurs only in species, such as woodcocks, which rely primarily upon senses other than vision to guide foraging.

     

Eye structure and amphibious foraging in albatrosses

Anterior eye structure and retinal visual fields were determined in grey-headed and black-browed albatrosses, Diomedea melanophris and D. chrysostoma (Procellariiformes, Diomedeidae), using keratometry and an ophthalmoscopic reflex technique. Results for the two species were very similar and indicate that the eyes are of an amphibious optical design suggesting that albatross vision is well suited to the visual pursuit of active prey both on and below the ocean surface. The corneas are relatively flat (radius ca. 14.5 mm) and hence of low absolute refractive power (ca. 23 dioptres). In air the binocular fields are relatively long (vertical extent ca. 70 degrees) and narrow (maximum width in the plane of the optic axes 26–32 degrees), a topography found in a range of bird species that employ visual guidance of bill position when foraging. The cyclopean fields measure approximately 270 degrees in the horizontal plane, but there is a 60 degrees blind sector above the head owing to the positioning of the eyes below the protruding supraorbital ridges. Upon immersion the monocular fields decrease in width such that the binocular fields are abolished. Anterior eye structure, and visual field topography in both air and water, show marked similarity with those of the Humboldt penguin.     

Visual configuration of two species of Falconidae with different foraging ecologies

Significant interspecific differences in avian vision occur, even in congeneric species, and these have been correlated with differences in the perceptual challenges associated with foraging. Although diurnal raptors are assumed to be mainly visually guided in their foraging, they differ markedly in their foraging tactics and this may result in different visual demands. Among the Falconidae (Falconiformes), most falcons forage mainly on the wing for highly mobile prey, whereas caracaras forage on the ground for carrion and insects. We assessed whether Saker Falcon Falco cherrug and Southern Caracara Caracara plancus differ in their visual abilities by determining the visual fields and foveal characteristics of both species. Using an ophthalmoscopic reflex technique, we found a higher degree of binocular overlap in the caracaras than in the falcons. The high binocular overlap (47°) of the Southern Caracara may facilitate object manipulation (e.g. moving rocks) when foraging. We used an ultra‐high resolution spectral‐domain optical coherence tomography to determine foveal characteristics. We found two foveas (depressions in the retina where high visual resolution is expected) in the falcons (one central and one temporal) but only a central fovea in the caracaras. The presence of a shallower temporal fovea in Saker Falcons may help to fixate visually upon a highly mobile prey item during pursuit. We conclude that these differences in visual field configurations and foveal characteristics reflect different foraging demands, suggesting that the extraction of visual information is finely tuned to the demands of their foraging tactics.     

Visual fields in hornbills: precision-grasping and sunshades

Retinal visual fields were determined in Southern Ground Hornbills Bucorvus leadbeateri and Southern Yellow-billed Hornbills Tockus leucomelas (Coraciiformes, Bucerotidae) using an ophthalmoscopic reflex technique. In both species the binocular field is relatively long and narrow with a maximum width of 30° occurring 40° above the bill. The bill tip projects into the lower half of the binocular field. This frontal visual field topography exhibits a number of key features that are also found in other terrestrial birds. This supports the hypothesis that avian visual fields are of three principal types that are correlated with the degree to which vision is employed when taking food items, rather than with phylogeny. However, unlike other species studied to date, in both hornbill species the bill intrudes into the binocular field. This intrusion of the bill restricts the width of the binocular field but allows the birds to view their own bill tips. It is suggested that this is associated with the precision-grasping feeding technique of hornbills. This involves forceps-like grasping and manipulation of items in the tips of the large decurved bill. The two hornbill species differ in the extent of the blind area perpendicularly above the head. Interspecific comparison shows that eye size and the width of the blind area above the head are significantly correlated. The limit of the upper visual field in hornbills is viewed through the long lash-like feathers of the upper lids and these appear to be used as a sunshade mechanism. In Ground Hornbills eye movements are non-conjugate and have sufficient amplitude (30–40°) to abolish the frontal binocular field and to produce markedly asymmetric visual field configurations.     

Visual fields in the Black-crowned Night Heron Nycticorax nycticorax: nocturnality does not result in owl-like features

Compared with diurnally active species, the eyes of nocturnally active herons (Ardeidae) are relatively larger and more widely separated. These features are found in comparisons between the nocturnally foraging Black-crowned Night Heron Nycticorax nycticorax and the diurnally active Cattle Egret Bubulcus ibis. Casual viewing of the Black-crowned Night Heron gives the impression of a somewhat owl-like appearance, with an apparently wide degree of binocular overlap. Visual fields and eye movements were determined in two alert, restrained Black-crowned Night Herons with the use of an ophthalmoscopic technique. A wide degree of binocular overlap was not confirmed, and the Black-crowned Night Heron's visual field closely resembles those of diurnally foraging herons (Western Reef Heron Egretta gularis schistacea , Squacco Heron Ardeola ralloides , Cattle Egret). The Black-crowned Night Heron's binocular field is vertically long and narrow (maximum width 22̀), with the bill placed approximately at the centre. Monocular and cyclopean field widths in the horizontal plane equal 171̀ and 320̀, respectively. Retinal binocular overlap can be abolished by eye movements. There is a blind sector (10–13̀ wide) at the margin of each eye's optical field, and this results in the functional retinal binocular field being much narrower than the optical binocular fields. It is these blind sectors which give rise to the appearance of a much wider binocular field. The visual field characteristics of this heron species may be best understood in relation to the foraging technique of capturing agile, evasive prey directly in the bill. The comparatively large size of the Black-crowned Night Herons' eyes may be associated with activity over a wide range of natural light levels but does not give rise to binocular fields larger than those of diurnal heron species.     

Visual coverage and scanning behavior in two corvid species: American crow and Western scrub jay

Inter-specific differences in the configuration of avian visual fields and degree of eye/head movements have been associated with foraging and anti-predator behaviors. Our goal was to study visual fields, eye movements, and head movements in two species of corvids: American crow (Corvus brachyrhynchos) and Western scrub jay (Aphelocoma californica). American crows had wider binocular overlap, longer vertical binocular fields, narrower blind areas, and higher amplitude of eye movement than Western scrub jays. American crows can converge their eyes and see their own bill tip, which may facilitate using different foraging techniques (e.g., pecking, probing) and manufacturing and handing rudimentary tools. Western scrub jays had a higher head movement rate than American crows while on the ground, and the opposite between-species difference was found when individuals were perching. Faster head movements may enhance the ability to scan the environment, which may be related to a higher perceived risk of predation of Western scrub jays when on the ground, and American crows when perching. The visual field configuration of these species appears influenced mostly by foraging techniques while their scaning behavior, by predation risk.     

Vision, touch and object manipulation in Senegal parrots Poicephalus senegalus

Parrots are exceptional among birds for their high levels of exploratory behaviour and manipulatory abilities. It has been argued that foraging method is the prime determinant of a bird's visual field configuration. However, here we argue that the topography of visual fields in parrots is related to their playful dexterity, unique anatomy and particularly the tactile information that is gained through their bill tip organ during object manipulation. We measured the visual fields of Senegal parrots Poicephalus senegalus using the ophthalmoscopic reflex technique and also report some preliminary observations on the bill tip organ in this species. We found that the visual fields of Senegal parrots are unlike those described hitherto in any other bird species, with both a relatively broad frontal binocular field and a near comprehensive field of view around the head. The behavioural implications are discussed and we consider how extractive foraging and object exploration, mediated in part by tactile cues from the bill, has led to the absence of visual coverage of the region below the bill in favour of more comprehensive visual coverage above the head.     

Vision and touch in relation to foraging and predator detection: insightful contrasts between a plover and a sandpiper

Visual fields were determined in two species of shorebirds (Charadriiformes) whose foraging is guided primarily by different sources of information: red knots (Calidris canutus, tactile foragers) and European golden plovers (Pluvialis apricaria, visual foragers). The visual fields of both species showed features that are found in a wide range of birds whose foraging involves precision pecking or lunging at food items. Surprisingly, red knots did not show comprehensive panoramic vision as found in some other tactile feeders; they have a binocular field surrounding the bill and a substantial blind area behind the head. We argue that this is because knots switch to more visually guided foraging on their breeding grounds. However, this visual field topography leaves them vulnerable to predation, especially when using tactile foraging in non-breeding locations where predation by falcons is an important selection factor. Golden plovers use visually guided foraging throughout the year, and so it is not surprising that they have precision-pecking frontal visual fields. However, they often feed at night and this is associated with relatively large eyes. These are anchored in the skull by a wing of bone extending from the dorsal perimeter of each orbit; a skeletal structure previously unreported in birds and which we have named 'supraorbital aliform bone', Os supraorbitale aliforme. The larger eyes and their associated supraorbital wings result in a wide blind area above the head, which may leave these plovers particularly vulnerable to predation. Thus, in these two shorebirds, we see clear examples of the trade-off between the two key functions of visual fields: (i) the detection of predators remote from the animal and (ii) the control of accurate behaviours, such as the procurement of food items, at close quarters.     

Visual fields in the Stone-curlew Burhinus oedicnemus

The Stone-curlew Burhinus oedicnemus is a short-billed terrestrial wading bird (Burhinidae; Charadriiformes) which forages primarily for surface living invertebrates in open, sparsely vegetated habitats during twilight and nighttime. Visual field topography in restrained alert birds was investigated using an ophthalmoscopic reflex technique. The visual fields have the following features: (1) Eye movements of significant amplitude appear to be absent. (2) The retinal binocular field is relatively small, with the bill placed near its centre. It extends vertically through 80° in the median sagittal plane with a maximum width of 18° occurring 5° above the bill. (3) With the head in a typical posture (eye-bill-tip angle approximately 15° below the horizontal), the binocular field stretches from 60° below to 20° above the horizontal. (4) The blind area behind the head is relatively narrow (15° at the horizontal), giving the bird near panoramic vision in the horizontal plane, but the widest blind area (32°) occurs directly above the head. (5) Monocular retinal fields in the horizontal plane are 182° wide and are asymmetric about the optic axis. (6) There is a blind sector of 7–12° at the margin of the optical fields, indicating that binocular field widths are not maximized. Interspecific comparisons of these visual field features suggest that the foraging of Stone-curlews is guided primarily by visual cues.     

Dissimilar bill shapes in new world tropical versus temperate forest foliage-gleaning birds

Summary The bill shape of foliage-gleaning birds in temperate and tropical new world forests is dissimilar. Tropical species have longer and narrower bills than their temperate zone counterparts. In addition, their bills are longer for a given body size. These differences cannot be readily explained as phylogenetic artifacts. I suggest that the distinct bill morphology of the two assemblages is determined by the type of insects that comprise the largest size classes of potential prey. These large insects are particularly important since they generally comprise the bulk of the nestling diet for insectivorous birds. In tropical forests Orthoptera are probably the most abundant large soft-bodied arthropods; they form an important resource for foliage-gleaning birds during the breeding (rainy) seasons. Most temperate zone foliage-gleaning birds rely almost entirely upon caterpillars when breeding. Long, narrow bills are thought to close more rapidly than shorter, broader bills. These long, fast bills may be required to efficiently harvest active Orthoptera. Migrant warblers may face morphological constraints from breeding successfully in lowland tropical forests. While the short-billed temperate zone birds can survive the tropical dry season by foraging on small arthropods, they may be inefficient at handling large Orthoptera to feed to nestlings.