A seabird's eye view: visual fields of some seabirds (Laridae and Procellariidae) from tropical latitudes.

The visual field of a bird defines the amount of information that can be extracted from the environment around it, using the eyes. Previous visual field research has left large phylogenetic gaps, where tropical bird species have been comparatively understudied. Using the ophthalmoscopic technique, we measured the visual fields of seven tropical seabird species, to understand what are the primary determinants of their visual fields. The visual field topographies of the seven seabird species were relatively similar, despite the two groups of Terns (Laridae) and Shearwaters (Procellariidae) being phylogenetically distant. We propose this similarity is due to their largely similar foraging ecology. These findings support previous research that foraging ecology rather than relatedness is the key determining factor behind a bird's visual field topography. Some bird species were identified to have more limited binocular fields, such as Brown Noddies (Anous stolidus) where binocularity onsets lower down within the visual field, resulting in a larger blind area about the head.

Anomalous binocular vision in African Harrier-Hawks.

An animal's visual field is the three-dimensional space around its head from which it can extract visual information at any instant1. Bird visual fields vary markedly between species, and this variation is likely to be driven primarily by foraging ecology1,2,3. The binocular visual field is the region in which the visual fields of the two eyes overlap; thus, objects in the binocular field are imaged by both eyes simultaneously. The binocular field plays a pivotal role in the detection of symmetrical optic flow-fields, providing almost instantaneous information on the direction of travel and the time to contact a target towards which the head or feet is travelling; thus, information from the binocular field is crucial in guiding key foraging behaviours2,3. Here, we demonstrate an unusual visual field and binocular extent above the head in African Harrier-Hawks, also known as Gymnogenes (Polyboroides typus) compared to 18 other members of the Accipitridae4,5. We argue that the observed visual field can be attributed to the unusual and specific foraging behaviour of African Harrier-Hawks.

Binocular field configuration in owls: the role of foraging ecology.

The binocular field of vision differs widely in birds depending on ecological traits such as foraging. Owls (Strigiformes) have been considered to have a unique binocular field, but whether it is related to foraging has remained unknown. While taking into account allometry and phylogeny, we hypothesized that both daily activity cycle and diet determine the size and shape of the binocular field in owls. Here, we compared the binocular field configuration of 23 species of owls. While we found no effect of allometry and phylogeny, ecological traits strongly influence the binocular field shape and size. Binocular field shape of owls significantly differed from that of diurnal raptors. Among owls, binocular field shape was relatively conserved, but binocular field size differed among species depending on ecological traits, with larger binocular fields in species living in dense habitat and foraging on invertebrates. Our results suggest that (i) binocular field shape is associated with the time of foraging in the daily cycle (owls versus diurnal raptors) and (ii) that binocular field size differs between closely related owl species even though the general shape is conserved, possibly because the field of view is partially restricted by feathers, in a trade-off with auditory localization.

Binocular vision and foraging in ducks, geese and swans (Anatidae).

Wide variation in visual field configuration across avian species is hypothesized to be driven primarily by foraging ecology and predator detection. While some studies of selected taxa have identified relationships between foraging ecology and binocular field characteristics in particular species, few have accounted for the relevance of shared ancestry. We conducted a large-scale, comparative analysis across 39 Anatidae species to investigate the relationship between the foraging ecology traits of diet or behaviour and binocular field parameters, while controlling for phylogeny. We used phylogenetic models to examine correlations between traits and binocular field characteristics, using unidimensional and morphometric approaches. We found that foraging behaviour influenced three parameters of binocular field size: maximum binocular field width, vertical binocular field extent, and angular separation between the eye-bill projection and the direction of maximum binocular field width. Foraging behaviour and body mass each influenced two descriptors of binocular field shape. Phylogenetic relatedness had minimal influence on binocular field size and shape, apart from vertical binocular field extent. Binocular field differences are associated with specific foraging behaviours, as related to the perceptual challenges of obtaining different food items from aquatic and terrestrial environments.

Avian vision.

The primary reliance of birds on vision is readily and frequently asserted. Casual observations of birds completing their everyday behaviours is sufficient to convince most observers that birds are using vision to control their key behaviours. This assertion is supported by evidence that in most bird species relatively large portions of their brains are devoted to the analysis of information from vision. Also, the so-called intelligent behaviours of birds seem to be based primarily upon visual information. Thus, gaining information from vision, and using it to guide sophisticated behaviours, is seen as a vital component of what makes birds so fascinating.

What Drives Bird Vision? Bill Control and Predator Detection Overshadow Flight.

Although flight is regarded as a key behavior of birds this review argues that the perceptual demands for its control are met within constraints set by the perceptual demands of two other key tasks: the control of bill (or feet) position, and the detection of food items/predators. Control of bill position, or of the feet when used in foraging, and timing of their arrival at a target, are based upon information derived from the optic flow-field in the binocular region that encompasses the bill. Flow-fields use information extracted from close to the bird using vision of relatively low spatial resolution. The detection of food items and predators is based upon information detected at a greater distance and depends upon regions in the retina with relatively high spatial resolution. The tasks of detecting predators and of placing the bill (or feet) 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, areas, and high ganglion cell densities. The informational function of binocular vision in birds does not lie in binocularity per se (i.e., two eyes receiving slightly different information simultaneously about the same objects) but in the contralateral projection of the visual field of each eye. This ensures that each eye receives information from a symmetrically expanding optic flow-field centered close to the direction of the bill, and from this the crucial information of direction of travel and time-to-contact can be extracted, almost instantaneously. Interspecific comparisons of visual fields between closely related species have shown that small differences in foraging techniques can give rise to different perceptual challenges and these have resulted in differences in visual fields even within the same genus. This suggests that vision is subject to continuing and relatively rapid natural selection based upon individual differences in the structure of the optical system, retinal topography, and eye position in the skull. From a sensory ecology perspective a bird is best characterized as "a bill guided by an eye" and that control of flight is achieved within constraints on visual capacity dictated primarily by the demands of foraging and bill control.

Visual abilities in two raptors with different ecology.

Differences in visual capabilities are known to reflect differences in foraging behaviour even among closely related species. Among birds, the foraging of diurnal raptors is assumed to be guided mainly by vision but their foraging tactics include both scavenging upon immobile prey and the aerial pursuit of highly mobile prey. We studied how visual capabilities differ between two diurnal raptor species of similar size: Harris's hawks, Parabuteo unicinctus, which take mobile prey, and black kites, Milvus migrans, which are primarily carrion eaters. We measured visual acuity, foveal characteristics and visual fields in both species. Visual acuity was determined using a behavioural training technique; foveal characteristics were determined using ultra-high resolution spectral-domain optical coherence tomography (OCT); and visual field parameters were determined using an ophthalmoscopic reflex technique. We found that these two raptors differ in their visual capacities. Harris's hawks have a visual acuity slightly higher than that of black kites. Among the five Harris's hawks tested, individuals with higher estimated visual acuity made more horizontal head movements before making a decision. This may reflect an increase in the use of monocular vision. Harris's hawks have two foveas (one central and one temporal), while black kites have only one central fovea and a temporal area. Black kites have a wider visual field than Harris's hawks. This may facilitate the detection of conspecifics when they are scavenging. These differences in the visual capabilities of these two raptors may reflect differences in the perceptual demands of their foraging behaviours.

Associations between Resting, Activity, and Daily Metabolic Rate in Free-Living Endotherms: No Universal Rule in Birds and Mammals.

Energy management models provide theories and predictions for how animals manage their energy budgets within their energetic constraints, in terms of their resting metabolic rate (RMR) and daily energy expenditure (DEE). Thus, uncovering what associations exist between DEE and RMR is key to testing these models. Accordingly, there is considerable interest in the relationship between DEE and RMR at both inter- and intraspecific levels. Interpretation of the evidence for particular energy management models is enhanced by also considering the energy spent specifically on costly activities (activity energy expenditure [AEE] = DEE - RMR). However, to date there have been few intraspecific studies investigating such patterns. Our aim was to determine whether there is a generality of intraspecific relationships among RMR, DEE, and AEE using long-term data sets for bird and mammal species. For mammals, we use minimum heart rate (fH), mean fH, and activity fH as qualitative proxies for RMR, DEE, and AEE, respectively. For the birds, we take advantage of calibration equations to convert fH into rate of oxygen consumption in order to provide quantitative proxies for RMR, DEE, and AEE. For all 11 species, the DEE proxy was significantly positively correlated with the RMR proxy. There was also evidence of a significant positive correlation between AEE and RMR in all four mammal species but only in some of the bird species. Our results indicate there is no universal rule for birds and mammals governing the relationships among RMR, AEE, and DEE. Furthermore, they suggest that birds tend to have a different strategy for managing their energy budgets from those of mammals and that there are also differences in strategy between bird species. Future work in laboratory settings or highly controlled field settings can tease out the environmental and physiological processes contributing to variation in energy management strategies exhibited by different species.

The sub-annual breeding cycle of a tropical seabird.

Breeding periodicity allows organisms to synchronise breeding attempts with the most favourable ecological conditions under which to raise offspring. For most animal species, ecological conditions vary seasonally and usually impose an annual breeding schedule on their populations; sub-annual breeding schedules will be rare. We use a 16-year dataset of breeding attempts by a tropical seabird, the sooty tern (Onychoprion fuscatus), on Ascension Island to provide new insights about this classical example of a population of sub-annually breeding birds that was first documented in studies 60 years previously on the same island. We confirm that the breeding interval of this population has remained consistently sub-annual. By ringing >17,000 birds and re-capturing a large sample of them at equivalent breeding stages in subsequent seasons, we reveal for the first time that many individual birds also consistently breed sub-annually (i.e. that sub-annual breeding is an individual as well as a population breeding strategy). Ascension Island sooty terns appear to reduce their courtship phase markedly compared with conspecifics breeding elsewhere. Our results provide rare insights into the ecological and physiological drivers of breeding periodicity, indicating that reduction of the annual cycle to just two life-history stages, breeding and moult, is a viable life-history strategy and that moult may determine the minimum time between breeding attempts.

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.

Sublingual fistula in a masked booby (Sula dactylatra) and possible role of ectoparasites in its etiology.

A sublingual fistula is an opening through the ventral skin of the buccal cavity through which the tongue can protrude. The cause is unknown. Masked Boobies (Sula dactylatra) are the third avian species to be reported with this condition. We argue that ectoparasite infestation of hatchlings may be an initial cause.

Extreme binocular vision and a straight bill facilitate tool use in New Caledonian crows.

Humans are expert tool users, who manipulate objects with dextrous hands and precise visual control. Surprisingly, morphological predispositions, or adaptations, for tool use have rarely been examined in non-human animals. New Caledonian crows Corvus moneduloides use their bills to craft complex tools from sticks, leaves and other materials, before inserting them into deadwood or vegetation to extract prey. Here we show that tool use in these birds is facilitated by an unusual visual-field topography and bill shape. Their visual field has substantially greater binocular overlap than that of any other bird species investigated to date, including six non-tool-using corvids. Furthermore, their unusually straight bill enables a stable grip on tools, and raises the tool tip into their visual field's binocular sector. These features enable a degree of tool control that would be impossible in other corvids, despite their comparable cognitive abilities. To our knowledge, this is the first evidence for tool-use-related morphological features outside the hominin lineage.

Metabolic rate throughout the annual cycle reveals the demands of an Arctic existence in great cormorants.

Aquatic endotherms living in polar regions are faced with a multitude of challenges, including low air and water temperatures and low illumination, especially in winter. Like other endotherms from cold environments, Great Cormorants (Phalacrocorax carbo) living in Arctic waters were hypothesized to respond to these challenges through a combination of high daily rate of energy expenditure (DEE) and high food requirements, which are met by a high rate of catch per unit effort (CPUE). CPUE has previously been shown in Great Cormorants to be the highest of any diving bird. In the present study, we tested this hypothesis by making the first measurements of DEE and foraging activity of Arctic-dwelling Great Cormorants throughout the annual cycle. We demonstrate that, in fact, Great Cormorants have surprisingly low rates of DEE. This low DEE is attributed primarily to very low levels of foraging activity, particularly during winter, when the cormorants spent only 2% of their day submerged. Such a low level of foraging activity can only be sustained through consistently high foraging performance. We demonstrate that Great Cormorants have one of the highest recorded CPUEs for a diving predator; 18.6 g per minute submerged (95% prediction interval 13.0-24.2 g/min) during winter. Temporal variation in CPUE was investigated, and highest CPUE was associated with long days and shallow diving depths. The effect of day length is attributed to seasonal variation in prey abundance. Shallow diving leads to high CPUE because less time is spent swimming between the surface and the benthic zone where foraging occurs. Our study demonstrates the importance of obtaining accurate measurements of physiology and behavior from free-living animals when attempting to understand their ecology.

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.

Does food supplementation really enhance productivity of breeding birds?

Food availability influences multiple stages of the breeding cycle of birds, and supplementary feeding has helped in its understanding. Most supplementation studies have reported advancements of laying, whilst others, albeit less numerous, have also demonstrated fitness benefits such as larger clutches, shorter incubation periods, and greater hatching success. Relatively few studies, however, have investigated the effects of supplementary feeding for protracted periods across multiple stages of the breeding cycle. These effects are important to understand since long-term food supplementation of birds is recommended in urban habitats and is used as a tool to increase reproductive output in endangered species. Here, we compare the breeding phenology and productivity of blue tits Cyanistes caeruleus and great tits Parus major breeding in food-supplemented and non-supplemented blocks in a broadleaf woodland in central England over three seasons (2006-2008). Supplementation was provided continuously from several weeks pre-laying until hatching, and had multiple significant effects. Most notably, supplementation reduced brood size significantly in both species, by half a chick or more at hatching (after controlling for year and hatching date). Reduced brood sizes in supplemented pairs were driven by significantly smaller clutches in both species and, in blue tits, significantly lower hatching success. These are novel and concerning findings of food supplementation. As expected, supplementary feeding advanced laying and shortened incubation periods significantly in both species. We discuss the striking parallels between our findings and patterns in blue and great tit reproduction in urban habitats, and conclude that supplementary feeding may not always enhance the breeding productivity of birds.

Local affine image matching and synthesis based on structural patterns.

A general purpose block-to-block affine transformation estimator is described. The estimator is based on Fourier slice analysis and Fourier spectral alignment. It shows encouraging performance in terms of both speed and accuracy compared to existing methods. The key elements of its success are attributed to the ability to: 1) locate an arbitrary number of affine invariant points in the spectrum that latch onto significant structural features; 2) match the estimated invariant points with the target spectrum by the slicewise phase-correlation; and 3) use affine invariant points to directly compute all linear parameters of the full affine transform by spectral alignment. Experimental results using a wide range of textures are presented. Potential applications include affine invariant image segmentation, registration, affine symmetric image coding, and motion analysis.

An affine symmetric image model and its applications.

Natural images contain considerable redundancy, some of which is successfully captured using recently developed directional wavelets. In this paper, an affine symmetric image model is considered. It provides a flexible scheme to exploit geometric redundancy. A patch of texture from an image is rotated, scaled and sheared to approximate other similar parts in the image, revealing the self-similarity relation. The general scheme is derived as follows. A texture model is required that identifies structural patterns. Then the affine symmetry is exploited between structural textures at a local level, the objective being to find the minimum residual error by estimating the affine transform relating two patches of texture. Having developed a local model, the methodology is extended to the whole image to estimate the global affine relation. This global model is further developed in a multiresolution framework for multiscale analysis, by which the self similarity of the image is exploited across space and scale. The multiresolution model can be applied to a series of practical problems. Experimental evaluation demonstrates the effectiveness of the approach in affine invariant texture segmentation and image approximation.

What is binocular vision for? A birds' eye view.

It is proposed that with the possible exception of owls, binocularity in birds does not have a higher order function that results in the perception of solidity and relative depth. Rather, binocularity is a consequence of the requirement of having a portion of the visual field that looks in the direction of travel; hence, each eye must have a contralateral projection that gives rise to binocularity. This contralateral projection is necessary to gain a symmetrically expanding optic flow-field about the bill. This specifies direction of travel and time to contact a target during feeding or when provisioning chicks. In birds that do not need such control of their bill, binocular field widths are very small, suggesting that binocular vision plays only a minor role in the control of locomotion. 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 wider binocular fields of owls may be the product of an interaction between enlarged eyes and enlarged outer ears, which may simply prevent more lateral placement of the eyes.

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.

Pedestrian locomotion energetics and gait characteristics of a diving bird, the great cormorant, Phalacrocorax carbo.

Great cormorants Phalacrocorax carbo are foot propelled diving birds that seem poorly suited to locomotion on land. They have relatively short legs, which are presumably adapted for the generation of high forces during the power stroke of aquatic locomotion, and walk with a pronounced "clumsy waddle". We hypothesise (1) that the speed, independent minimum cost of locomotion (C min, ml O2 m(-1)) will be high for cormorants during treadmill exercise, and (2) that cormorants will have a relatively limited speed range in comparison to more cursorial birds. We measured the rate of oxygen consumption (V02) of cormorants during pedestrian locomotion on a treadmill, and filmed them to determine duty factor (the fraction of stride period that the foot is in contact with the ground), foot contact time (tc), stride frequency (f), swing phase duration and stride length. C min was 2.1-fold higher than that predicted by their body mass and phylogenetic position, but was not significantly different from the C min of runners (Galliformes and Struthioniformes). The extrapolated gamma-intercept of the relationship between V02 and speed was 1.9-fold higher than that predicted by allometry. Again, cormorants were not significantly different from runners. Contrary to our hypothesis, we therefore conclude that cormorants do not have high pedestrian transport costs. Cormorants were observed to use a grounded gait with two double support phases at all speeds measured, and showed an apparent gait transition between 0.17 and 0.25 m s(-1). This transition occurs at a Froude number between 0.016 and 0.037, which is lower than the value of approximately 0.5 observed for many other species. However, despite the use of a limited speed range, and a gait transition at relatively low speed, we conclude that the pedestrian locomotion of these foot propelled diving birds is otherwise generally similar to that of cursorial birds at comparable relative velocities.