Fishing in the dark: a pursuit-diving seabird modifies foraging behaviour in response to nocturnal light levels

Visual predators tend not to hunt during periods when efficiency is compromised by low light levels. Yet common murres, a species considered a diurnal visual predator, frequently dive at night. To study foraging of murres under different light conditions, we used a combination of archival tagging methods and astronomical models to assess relationships between diving behaviour and light availability. During diurnal and crepuscular periods, murres used a wide range of the water column (2-177 m), foraging across light intensities that spanned several orders of magnitude (10(3)-10(-10) Wm(-2)). Through these periods, they readily dived under conditions equivalent to ambient moonlight (~10(-4) Wm(-2)) but rarely under conditions equivalent to starlight (~10(-8) Wm(-2)). At night, murres readily foraged during both moonlit and starlit periods, and diving depth and efficiency increased with nocturnal light intensity, suggesting that night diving is at least partially visually guided. Whether visually guided foraging is possible during starlit periods is less clear. Given the dense prey landscape available, random-walk simulations suggest that murres could benefit from random prey encounters. We hypothesise that murres foraging through starlit periods rely either on close-range visual or possibly nonvisual cues to acquire randomly encountered prey. This research highlights the flexibility of breeding common murres and raises questions about the strategies and mechanisms birds use to find prey under very low light conditions.     

The neural selection and control of saccades by the frontal eye field

Recent research has provided new insights into the neural processes that select the target for and control the production of a shift of gaze. Being a key node in the network that subserves visual processing and saccade production, the frontal eye field (FEF) has been an effective area in which to monitor these processes. Certain neurons in the FEF signal the location of conspicuous or meaningful stimuli that may be the targets for saccades. Other neurons control whether and when the gaze shifts. The existence of distinct neural processes for visual selection and saccade production is necessary to explain the flexibility of visually guided behaviour.     

Operant control of human eye movements

Saccade and smooth pursuit are the eye movements used by primates to shift gaze. In this article we review evidence for the effects of reinforcement on several dimensions of these responses such as their latencies, velocities or amplitudes. We propose that these responses are operant behaviours controlled by their consequences on performance of visually guided tasks. Studying the conditions under which particular eye movement patterns might emerge from the cumulative effects of reinforcement provides critical insights about how motor responses are attuned to environmental exigencies.     

How Lovebirds Maneuver Rapidly Using Super-Fast Head Saccades and Image Feature Stabilization

Diurnal flying animals such as birds depend primarily on vision to coordinate their flight path during goal-directed flight tasks. To extract the spatial structure of the surrounding environment, birds are thought to use retinal image motion (optical flow) that is primarily induced by motion of their head. It is unclear what gaze behaviors birds perform to support visuomotor control during rapid maneuvering flight in which they continuously switch between flight modes. To analyze this, we measured the gaze behavior of rapidly turning lovebirds in a goal-directed task: take-off and fly away from a perch, turn on a dime, and fly back and land on the same perch. High-speed flight recordings revealed that rapidly turning lovebirds perform a remarkable stereotypical gaze behavior with peak saccadic head turns up to 2700 degrees per second, as fast as insects, enabled by fast neck muscles. In between saccades, gaze orientation is held constant. By comparing saccade and wingbeat phase, we find that these super-fast saccades are coordinated with the downstroke when the lateral visual field is occluded by the wings. Lovebirds thus maximize visual perception by overlying behaviors that impair vision, which helps coordinate maneuvers. Before the turn, lovebirds keep a high contrast edge in their visual midline. Similarly, before landing, the lovebirds stabilize the center of the perch in their visual midline. The perch on which the birds land swings, like a branch in the wind, and we find that retinal size of the perch is the most parsimonious visual cue to initiate landing. Our observations show that rapidly maneuvering birds use precisely timed stereotypic gaze behaviors consisting of rapid head turns and frontal feature stabilization, which facilitates optical flow based flight control. Similar gaze behaviors have been reported for visually navigating humans. This finding can inspire more effective vision-based autopilots for drones.     

The electroretinogram of Drosophila to flickering light: Assessment of the contributions of receptor cells R7 and R8

A method using flickering light of a suitable frequency was devised to assess the contribution of the central photoreceptor cells to the ERG of red-eyed Drosophila. It reveals the function of receptor cells R7 and R8 even in the presence of intact receptor cells R1-6. The method is calibrated using the mutant sev^LY3 and applied to the study of some mutants affected in visually guided behaviour.     

Ravens, Corvus corax, follow gaze direction of humans around obstacles

The ability to follow gaze (i.e. head and eye direction) has recently been shown for social mammals, particularly primates. In most studies, individuals could use gaze direction as a behavioural cue without understanding that the view of others may be different from their own. Here, we show that hand-raised ravens not only visually co-orient with the look-ups of a human experimenter but also reposition themselves to follow the experimenter's gaze around a visual barrier. Birds were capable of visual co-orientation already as fledglings but consistently tracked gaze direction behind obstacles not before six months of age. These results raise the possibility that sub-adult and adult ravens can project a line of sight for the other person into the distance. To what extent ravens may attribute mental significance to the visual behaviour of others is discussed.     

Visual accommodation and active pursuit of prey underwater in a plunge-diving bird: the Australasian gannet

Australasian gannets (Morus serrator), like many other seabird species, locate pelagic prey from the air and perform rapid plunge dives for their capture. Prey are captured underwater either in the momentum (M) phase of the dive while descending through the water column, or the wing flapping (WF) phase while moving, using the wings for propulsion. Detection of prey from the air is clearly visually guided, but it remains unknown whether plunge diving birds also use vision in the underwater phase of the dive. Here we address the question of whether gannets are capable of visually accommodating in the transition from aerial to aquatic vision, and analyse underwater video footage for evidence that gannets use vision in the aquatic phases of hunting. Photokeratometry and infrared video photorefraction revealed that, immediately upon submergence of the head, gannet eyes accommodate and overcome the loss of greater than 45 D (dioptres) of corneal refractive power which occurs in the transition between air and water. Analyses of underwater video showed the highest prey capture rates during WF phase when gannets actively pursue individual fish, a behaviour that very likely involves visual guidance, following the transition after the plunge dive's M phase. This is to our knowledge the first demonstration of the capacity for visual accommodation underwater in a plunge diving bird while capturing submerged prey detected from the air.     

Visual signals in the courtship of Drosophila melanogaster: Mutant analysis

Visual cues are necessary for optimal mating success in Drosophila melanogaster. The male's most important visually guided behaviour is tracking. It is shown here that tracking requires intact visual receptor cells R1–6 and the presence of screening pigments in the eye. Thus flies carrying the mutation ebony as well as wild type flies affected in receptor cell R1–6 are unable to use visual cues when they track females. A similar defect was obseved in white-eyed flies lacking screening pigments. Female receptivity depends on visual signals provided by the male flies. Most important cues are the light reflection from and the shape of the male's eyes. No influence of the light reflected from the thorax could be seen. Absence of eyes in the male, however, does not depress female receptivity as much as white eyes. Some evidence is provided that male courtship behaviour is evaluated visually by the female.     

Cryptic sociality in rattlesnakes (Crotalus horridus) detected by kinship analysis

Research on social behaviour has largely concentrated on birds and mammals in visually active, cooperatively breeding groups (although such systems are relatively rare) and focused much less on species that rarely interact other than for mating and parental care. We used microsatellite markers to characterize relatedness among aggregations of timber rattlesnakes (Crotalus horridus), a putatively solitary reptile that relies heavily on chemical cues, and found that juveniles and pregnant females preferentially aggregate with kin under certain conditions. The ability to recognize kin and enhance indirect fitness thus might be far more widespread than implied by studies of animals whose behaviour is primarily visually and/or acoustically mediated, and we predict that molecular markers will reveal many additional examples of 'cryptic' sociality.     

Nest height is affected by lamppost lighting proximity in addition to nestbox size in urban great tits

Both natural and artificial light have proximate influences on many aspects of avian biology, physiology and behaviour. To date artificial light at night is mostly considered as being a nuisance disrupting for instance sleep and reproduction of diurnal species. Here, we investigate if lamppost night lighting affects cavity‐nesting bird species inside their breeding cavity. Nest height in secondary cavity‐nesting species is the result of trade‐offs between several selective forces. Predation is the prevailing force leading birds to build thin nests to increase the distance towards the entrance hole. A thin nest may also limit artificial light exposure at night. Yet, a minimum level of daylight inside nesting cavities is necessary for adequate visual communication and/or offspring development. Against this background, we hypothesised that avian nest‐building behaviour varies in response to a change in night lighting. We monitored nest height of urban great tits Parus major during six years and found that it varied with artificial light proximity. The birds built thinner nests inside nestboxes of various sizes in response to increasing lamppost night light availability at the nest. In large nestboxes, the nests were also thinner when a lamppost was present in the territory. Whether this relationship between artificial night lighting and nest height reflects a positive or negative effect of urbanisation is discussed in the light of recent experimental studies conducted in rural populations by other research groups.     

Age dynamics of visually guided behavior and visual evoked potentials of altricial nestlings

Comparative study has been carried out of factors of organization of visually guided feeding behaviour (observation method) and the degree of maturity of the visual mechanisms by the criterion of Wulst EPs formation and of their recovery cycles in normally developing and visually deprived nestlings. In has been established that during the period following the opening of the eyes (5-9th day) the feeding behaviour is connected with diffuse photo-sensitivity of visual mechanisms. Diffuse photo-sensitivity fully provides for natural feeding behaviour at the corresponding stage of development of visual functions. Complete visual deprivation during the whole period of diffuse photo-sensitivity does not influence subsequent development of the visual system.     

Speaking and Listening with the Eyes: Gaze Signaling during Dyadic Interactions

Cognitive scientists have long been interested in the role that eye gaze plays in social interactions. Previous research suggests that gaze acts as a signaling mechanism and can be used to control turn-taking behaviour. However, early research on this topic employed methods of analysis that aggregated gaze information across an entire trial (or trials), which masks any temporal dynamics that may exist in social interactions. More recently, attempts have been made to understand the temporal characteristics of social gaze but little research has been conducted in a natural setting with two interacting participants. The present study combines a temporally sensitive analysis technique with modern eye tracking technology to 1) validate the overall results from earlier aggregated analyses and 2) provide insight into the specific moment-to-moment temporal characteristics of turn-taking behaviour in a natural setting. Dyads played two social guessing games (20 Questions and Heads Up) while their eyes were tracked. Our general results are in line with past aggregated data, and using cross-correlational analysis on the specific gaze and speech signals of both participants we found that 1) speakers end their turn with direct gaze at the listener and 2) the listener in turn begins to speak with averted gaze. Convergent with theoretical models of social interaction, our data suggest that eye gaze can be used to signal both the end and the beginning of a speaking turn during a social interaction. The present study offers insight into the temporal dynamics of live dyadic interactions and also provides a new method of analysis for eye gaze data when temporal relationships are of interest.     

Vision: getting to grips with the Ebbinghaus illusion

It is well known that visual illusions can have a dramatic effect upon our visual perception of such properties as an object's size. It remains the subject of much debate, however, whether visual illusions have a similar influence on visually guided actions. Recent studies have thrown new light on this debate.     

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.     

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.     

Larval growth and development of cultured Pacific bonito

A method is described for rearing the offspring of wild-captured Pacific bonito. Six basic stages of post-embryonic development were determined based on ontogenetic changes in morphology and behaviour. Each stage corresponded with a different food source preference, related to the development of new swimming and predatory behaviours. A controlled environment is required to study the processes underlying development of those behaviours adeptly performed by bonito and other scombrids, including high-efficiency swimming and visually guided predation on other advanced species.     

Road exposure and the detectability of birds in field surveys

Road ecology, the study of the impacts of roads and their traffic on wildlife, including birds, is a rapidly growing field, with research showing effects on local avian population densities up to several kilometres from a road. However, in most studies, the effects of roads on the detectability of birds by surveyors are not accounted for. This could be a significant source of error in estimates of the impacts of roads on birds and could also affect other studies of bird populations. Using road density, traffic volume and bird count data from across Great Britain, we assess the relationships between roads and detectability of a range of bird species. Of 51 species analysed, the detectability of 36 was significantly associated with road exposure, in most cases inversely. Across the range of road exposure recorded for each species, the mean positive change in detectability was 52% and the mean negative change was 36%, with the strongest negative associations found in smaller-bodied species and those for which aural cues are more important in detection. These associations between road exposure and detectability could be caused by a reduction in surveyors’ abilities to hear birds or by changes in birds’ behaviour, making them harder or easier to detect. We suggest that future studies of the impacts of roads on populations of birds or other taxa, and other studies using survey data from road-exposed areas, should account for the potential impacts of roads on detectability.     

Zoo behaviour science in the Research Centre for Vertebrate Studies of the Academy of Sciences of the German Democratic Republic (in the Animal Park of Berlin)

This is a report of the results of behaviour science studies in the Animal Park of Berlin and the Academy of Sciences in the German Democratic Republic (G.D.R.). The major goal of this research is to investigate the behaviour of rare animals as a basis for zoological research, systematics and comparative studies in evolution. In addition, further research provided information directly applicable to behavioural management in zoos, farms and wild animal collections. Three main comparative studies dealt with urination and defecation in mammals, allelomimetic behaviour in vertebrates, and audio-visual orientation responses in several species of birds and mammals. Ethograms were created for the Red Woolly Opossum, Maned Wolf, Takin and Giant Eland Antelope. Social and reproductive behaviour studies were conducted on the Wolf, Golden Lion Marmoset, Père David's Deer, Mouflon and Wild Boar. Reports are included on the circadian activity of Pigmy Armadillo and Wild Boar. New information was revealed regarding communication in Mouflon and Père David's Deer, in addition to the new finding that some social behaviour patterns in Wild Boar are dependent on circadian rhythms. Three wolf packs studied consecutively in the same enclosure revealed that each pack differed in its social behaviour and that the dominant female (alpha female) determined the social structure. The problem of animal-human interactions is discussed. Zoos are seen as a medial stage between wilderness and farm management. It is suggested that an important task of zoo behaviour science is to study the ability of wild animals to adapt to purposes such as animal farms, animal husbandry institutes and domestic animal productivity, and to study the behaviour of the original forms of domestic animals in order to better understand and manage them.     

Genetic markers validate using the natural phenotypic characteristics of shed feathers to identify individual northern goshawks Accipiter gentilis

The recognition of individual animals is essential for many types of ecological research, as it enables estimates of demographic parameters such as population size, survival and reproductive rates. A popular method of visually identifying individuals uses natural variations in spot, stripe or scar markings. Although several studies have assessed the accuracy of these methods in mammals, crustaceans and fish, there have been few attempts to determine whether phenotypic characteristics are accurate when used for birds. Furthermore, even less is known about whether shed or moulted body parts can be reliably used to visually identify individuals. Here we assessed the accuracy of using phenotypic characteristics to identify avian individuals using a double‐marking experiment, whereby nine microsatellite genetic markers and natural markings on shed feathers were used to independently identify northern goshawks Accipiter gentilis. Phenotypic and genetic identification of individuals was consistent in 94.4% (51/54) comparisons. Our results suggest that the phenotypic characteristics of shed feathers can be reliably used as a non‐invasive and relatively inexpensive technique to monitor populations of an elusive species, the northern goshawk, without having to physically re‐capture or re‐sight individuals. We posit that using natural markings on shed feathers will also be a reliable method of identifying individuals in avian species with similar phenotypic characteristics, such as other Accipiter species.     

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.