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.     

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.     

The visual fields of Common Guillemots Uria aalge and Atlantic Puffins Fratercula arctica: foraging,vigilance and collision vulnerability

Significant differences in avian visual fields are found between closely related species that differ in their foraging technique. We report marked differences in the visual fields of two auk species. In air, Common Guillemots Uria aalge have relatively narrow binocular fields typical of those found in non‐passerine predatory birds. Atlantic Puffins Fratercula arctica have much broader binocular fields similar to those that have hitherto been recorded in passerines and in a penguin. In water, visual fields narrow considerably and binocularity in the direction of the bill is probably abolished in both auk species. Although perceptual challenges associated with foraging are similar in both species during the breeding season, when they are piscivorous, Puffins (but not Guillemots) face more exacting perceptual challenges when foraging at other times, when they take a high proportion of small invertebrate prey. Capturing this prey probably requires more accurate, visually guided bill placement and we argue that this is met by the Puffin's broader binocular field, which is retained upon immersion; its upward orientation may enable prey to be seen in silhouette. These visual field configurations have potentially important consequences that render these birds vulnerable to collision with human artefacts underwater, but not in air. They also have consequences for vigilance behaviour.     

Disentangling olfactory and visual information used by field foraging birds

Foraging strategies of birds can influence trophic plant–insect networks with impacts on primary plant production. Recent experiments show that some forest insectivorous birds can use herbivore‐induced plant volatiles (HIPVs) to locate herbivore‐infested trees, but it is unclear how birds combine or prioritize visual and olfactory information when making foraging decisions. Here, we investigated attraction of ground‐foraging birds to HIPVs and visible prey in short vegetation on farmland in a series of foraging choice experiments. Birds showed an initial preference for HIPVs when visual information was the same for all choice options (i.e., one experimental setup had all options with visible prey, another setup with hidden prey). However, if the alternatives within an experimental setup included visible prey (without HIPV) in competition with HIPV‐only, then birds preferred the visual option over HIPVs. Our results show that olfactory cues can play an important role in birds’ foraging choices when visual information contains little variation; however, visual cues are preferred when variation is present. This suggests certain aspects of bird foraging decisions in agricultural habitats are mediated by olfactory interaction mechanisms between birds and plants. We also found that birds from variety of dietary food guilds were attracted to HIPVs; hence, the ability of birds to use plant cues is probably more general than previously thought, and may influence the biological pest control potential of birds on farmland.     

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.     

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.     

Interspecific differences in the visual system and scanning behavior of three forest passerines that form heterospecific flocks

Little is known as to how visual systems and visual behaviors vary within guilds in which species share the same micro-habitat types but use different foraging tactics. We studied different dimensions of the visual system and scanning behavior of Carolina chickadees, tufted titmice, and white-breasted nuthatches, which are tree foragers that form heterospecific flocks during the winter. All species had centro-temporally located foveae that project into the frontal part of the lateral visual field. Visual acuity was the highest in nuthatches, intermediate in titmice, and the lowest in chickadees. Chickadees and titmice had relatively wide binocular fields with a high degree of eye movement right above their short bills probably to converge their eyes while searching for food. Nuthatches had narrower binocular fields with a high degree of eye movement below their bills probably to orient the fovea toward the trunk while searching for food. Chickadees and titmice had higher scanning (e.g., head movement) rates than nuthatches probably due to their wider blind areas that limit visual coverage. The visual systems of these three species seem tuned to the visual challenges posed by the different foraging and scanning strategies that facilitate the partitioning of resources within this guild.     

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.     

Understanding bird collisions with man‐made objects: a sensory ecology approach

Sensory ecology investigates the information that underlies an animal’s interactions with its environment. A sensory ecology framework is used here to seek to assess why flying birds collide with prominent structures, such as power lines, fences, communication masts, wind turbines and buildings, which intrude into the open airspace. Such collisions occur under conditions of both high and low visibility. It is argued that a human perspective of the problems posed by these obstacles is unhelpful. Birds live in different visual worlds and key aspects of these differences are summarized. When in flight, birds may turn their heads in both pitch and yaw to look down, either with the binocular field or with the lateral part of an eye’s visual field. Such behaviour may be usual and results in certain species being at least temporarily blind in the direction of travel. Furthermore, even if birds are looking ahead, frontal vision may not be in high resolution. In general, high resolution occurs in the lateral fields of view and frontal vision in birds may be tuned for the detection of movement concerned with the extraction of information from the optical flow field, rather than the detection of high spatial detail. Birds probably employ lateral vision for the detection of conspecifics, foraging opportunities and predators. The detection of these may be more important than simply looking ahead during flight in the open airspace. Birds in flight may predict that the environment ahead is not cluttered. Even if they are facing forward, they may fail to see an obstacle as they may not predict obstructions; perceptually they have no ‘prior’ for human artefacts such as buildings, power wires or wind turbines. Birds have only a restricted range of flight speeds that can be used to adjust their rate of gain of visual information as the sensory challenges of the environment change. It is argued that to reduce collisions with known hazards, something placed upon the ground may be more important than something placed on the obstacle itself. Foraging patches, conspecific models or alerting sounds placed a suitable distance from the hazard may be an effective way of reducing collisions in certain locations. However, there is unlikely to be a single effective way to reduce collisions for multiple species at any one site. Warning or diversion and distraction solutions may need to be tailored for particular target species.     

An Experimental Analysis of Spatial Position Effects on Foraging and Vigilance in Brown-Headed Cowbird flocks

Several observational studies have found that the costs and benefits of social foraging vary as a function of spatial position in the group. However, it is difficult to make mechanistic inferences because several confounding factors, such as food deprivation levels, food availability, neighbor distance, and group size can mask or amplify spatial position effects. We attempted to address experimentally the effect of spatial position on foraging and vigilance in a group, controlling for many confounding factors. We used enclosures that restricted physical but not visual interactions between brown-headed cowbirds and manipulated spatial position, flock size, and neighbor distance. Pecking rate (number of pecks per trial duration) was not related with position, but instantaneous pecking rate (number of pecks per foraging bout duration) was higher at the edge. The proportion of time spent head-up (scanning and food-handling) was also higher at the edge. For pecking rate and proportion of time spent scanning, changes in neighbor distance influenced the behavior of edge birds to a lesser extent than central birds. These results suggest that cowbirds at the edge perceived greater predation risk and that during the limited foraging time available, edge birds tried to compensate by foraging at a faster rate.     

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.     

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.     

When Parasitoid Males Make Decisions: Information Used when Foraging for Females

Optimal foraging models predict how an organism allocates its time and energy while foraging for aggregated resources. These models have been successfully applied to organisms such as predators looking for prey, female parasitoids looking for hosts, or herbivorous searching for food. In this study, information use and patch time allocation were investigated using male parasitoids looking for mates. The influence of the former presence of females in absence of mates and the occurrence of mating and other reproductive behaviours on the patch leaving tendency was investigated for the larval parasitoid Asobara tabida. Although males do not modify their patch residence time based on the number of females that visited the patch, they do show an increase in the patch residence time after mating a virgin female and performing courtship behaviour such as opening their wings. These results are in concordance with an incremental mechanism, as it has been described for females of the same species while foraging for hosts. The similarities between males and females of the same species, and the conditions under which such a patch-leaving decision rule is fitted are discussed. This is the first study describing an incremental effect of mating on patch residence time in males, thus suggesting that similar information use are probably driving different organisms foraging for resource, regardless of its nature.     

Group Size in Foraging African Penguins (Spheniscus demersus)

Diving synchrony was examined for varying group sizes of African penguins (Spheniscus demersus) travelling to their foraging grounds from their breeding islands. Groups of fewer than 12 birds always dived synchronously, whereas groups of more than 17 birds always dived asynchronously. Since travelling penguins do not dive deeply, large groups of birds can remain together irrespective of diving synchronization. Observations from boats showed that foraging penguins rarely occurred in groups of more than 17 birds. We suggest that groups of penguins that do not have synchronized dives cannot forage effectively, because foraging penguins dive deeply.     

Foraging strategy and predator avoidance behaviour: an intraspecific approach

Relationships between predator avoidance behaviour (scanning and flocking) and foraging were studied in Calidris alpina, to test predictions regarding the effect of foraging techniques on such behaviours. The scanning hypothesis predicts that individuals with a tactile hunting technique and individuals with a visual hunting technique (both continuous searchers) do not differ in any variable related to scanning behaviour. The flocking hypothesis predicts that visually hunting individuals witl tend to form smaller flocks than tactile-foraging individuals. The two continuous feeding strategies did not differ among individuals in vigilance rate, nor in vigilance time or mean scan duration. However, with respect to flocking behaviour, visual foragers differed from tactile foragers in foraging flock size. The relationships between flocking behaviour and foraging strategy are discussed. The pattern found at the intraspecific level are the same as those found at interspecific level.     

Behavior of Buff-Breasted Sandpipers (Tryngites subruficollis) during Migratory Stopover in Agricultural Fields

Background

Understanding the behavior of birds in agricultural habitats can be the first step in evaluating the conservation implications of birds'' use of landscapes shaped by modern agriculture. The existence and magnitude of risk from agricultural practices and the quality of resources agricultural lands provide will be determined largely by how birds use these habitats. Buff-breasted Sandpipers (Tryngites subruficollis) are a species of conservation concern. During spring migration large numbers of Buff-breasted Sandpipers stopover in row crop fields in the Rainwater Basin region of Nebraska. We used behavioral observations as a first step in evaluating how Buff-breasted Sandpipers use crop fields during migratory stopover.

Methodology/Principal Findings

We measured behavior during migratory stopover using scan and focal individual sampling to determine how birds were using crop fields. Foraging was the most frequent behavior observed, but the intensity of foraging changed over the course of the day with a distinct mid-day low point. Relative to other migrating shorebirds, Buff-breasted Sandpipers spent a significant proportion of their time in social interactions including courtship displays.

Conclusions/Significance

Our results show that the primary use of upland agricultural fields by migrating Buff-breasted Sandpipers is foraging while wetlands are used for maintenance and resting. The importance of foraging in row crop fields suggests that both the quality of food resources available in fields and the possible risks from dietary exposure to agricultural chemicals will be important to consider when developing conservation plans for Buff-breasted Sandpipers migrating through the Great Plains.     

Incompletely informed shorebirds that face a digestive constraint maximize net energy gain when exploiting patches

Foragers that feed on hidden prey are uncertain about the intake rate they can achieve as they enter a patch. However, foraging success can inform them, especially if they have prior knowledge about the patch quality distribution in their environment. We experimentally tested whether and how red knots (Calidris canutus) use such information and whether their patch-leaving decisions maximized their long-term net energy intake rate. The results suggest that the birds combined patch sample information with prior knowledge by making use of the potential value assessment rule. We reject five alternative leaving rules. The potential encounter rate that the birds choose as their critical departure threshold maximized their foraging gain ratio (a modified form of efficiency) while foraging. The high experimental intake rates were constrained by rate of digestion. Under such conditions, maximization of the foraging gain ratio during foraging maximizes net intake rate during total time (foraging time plus digestive breaks). We conclude that molluscivore red knots, in the face of a digestive constraint, are able to combine prior environmental knowledge about patch quality with patch sample information to obtain the highest possible net intake over total time.     

Do Insectivorous Birds use Volatile Organic Compounds from Plants as Olfactory Foraging Cues? Three Experimental Tests

Some insectivorous birds orient towards insect‐defoliated trees even when they do not see the foliar damage or the herbivores. There are, however, only a few studies that have examined the mechanisms behind this foraging behaviour. Previous studies suggest that birds can use olfactory foraging cues (e.g. volatile organic compounds (VOCs) emitted by defoliated plants), indirect visual cues or a combination of the two sensory cues. VOCs from insect‐defoliated plants are known to attract natural enemies of herbivores, and researchers have hypothesized that VOCs could also act as olfactory foraging cues for birds. We conducted three experiments across a range of spatial scales to test this hypothesis. In each experiment, birds were presented with olfactory cues and their behavioural responses or foraging outcomes were observed. In the first experiment, two different VOC blends, designed to simulate the volatile emissions of mountain birch (Betula pubescens ssp. czerepanovii) after defoliation by autumnal moth (Epirrita autumnata) larvae, were used in behavioural experiments in aviaries with pied flycatchers (Ficedula hypoleuca). The second experiment was a field‐based trial of bird foraging efficiency; the same VOC blends were applied to mountain birches, silver birches (B. pendula) and European white birches (B. pubescens) with plasticine larvae attached to the trees to serve as artificial prey for birds and provide a means to monitor predation rate. In the third experiment, the attractiveness of silver birch saplings defoliated by autumnal moth larvae versus intact controls was tested with great tits (Parus major) and blue tits (Cyanistes caeruleus) in an aviary. Birds did not orient towards either artificial or real trees with VOC supplements or towards herbivore‐damaged saplings when these saplings and undamaged alternatives were hidden from view. These findings do not support the hypothesis that olfactory foraging cues are necessary in the attraction of birds to herbivore‐damaged trees.     

Visual scanning behaviours and their role in the navigation of the Australian desert ant Melophorus bagoti

Ants are excellent navigators, using a combination of innate strategies and learnt information to guide habitual routes. The mechanisms underlying this behaviour are little understood though one avenue of investigation is to explore how innate sensori-motor routines are used to accomplish route navigation. For instance, Australian desert ant foragers are occasionally observed to cease translation and rotate on the spot. Here, we investigate this behaviour using high-speed videography and computational analysis. We find that scanning behaviour is saccadic with pauses separated by fast rotations. Further, we have identified four situations where scanning is typically displayed: (1) by naïve ants on their first departure from the nest; (2) by experienced ants departing from the nest for their first foraging trip of the day; (3) by experienced ants when the familiar visual surround was experimentally modified, in which case frequency and duration of scans were proportional to the degree of modification; (4) when the information from visual cues is at odds with the direction indicated by the ant’s path integration system. Taken together, we see a general relationship between scanning behaviours and periods of uncertainty.