Gaze Strategy in the Free Flying Zebra Finch (Taeniopygia guttata)

Fast moving animals depend on cues derived from the optic flow on their retina. Optic flow from translational locomotion includes information about the three-dimensional composition of the environment, while optic flow experienced during a rotational self motion does not. Thus, a saccadic gaze strategy that segregates rotations from translational movements during locomotion will facilitate extraction of spatial information from the visual input. We analysed whether birds use such a strategy by highspeed video recording zebra finches from two directions during an obstacle avoidance task. Each frame of the recording was examined to derive position and orientation of the beak in three-dimensional space. The data show that in all flights the head orientation was shifted in a saccadic fashion and was kept straight between saccades. Therefore, birds use a gaze strategy that actively stabilizes their gaze during translation to simplify optic flow based navigation. This is the first evidence of birds actively optimizing optic flow during flight.     

Variable fortunes in a patchy landscape —The habitat templet of an insect migrant

Migration by flight is essential for insects living in patchy landscapes and knowledge about variability in habitat patch structure and quality is important for the development of theory concerning insect dispersal polymorphisms. However, few studies provide more than anecdotal evidence about habitat change in time and space and its effects on insect survival and reproduction. Here I show how habitats and resource density of a lygaied bug,Lygaeus equestris, change in a patchy landscape over a seventeen year period. Although habitat patches per se are very stable, there are large temporal fluctuations in per capita food resources. Food seems to be limiting only in some years, and there may be periods of several years when populations change due to weather disturbance. Between-patch variation in reproductive success is large. Furthermore, the relative favourability of patches changes between years. There are also distance effects; in some years distances to suitable hibernation sites affect reproductive success. Long fliers experience more variable success, and sometimes extreme success, when compared with short fliers. The importance of movements from outlying areas also changes with time. The insect is thus faced with a habitat templet which varies strongly on many temporal and spatial scales.     

Visual gaze control during peering flight manoeuvres in honeybees

As animals travel through the environment, powerful reflexes help stabilize their gaze by actively maintaining head and eyes in a level orientation. Gaze stabilization reduces motion blur and prevents image rotations. It also assists in depth perception based on translational optic flow. Here we describe side-to-side flight manoeuvres in honeybees and investigate how the bees’ gaze is stabilized against rotations during these movements. We used high-speed video equipment to record flight paths and head movements in honeybees visiting a feeder. We show that during their approach, bees generate lateral movements with a median amplitude of about 20 mm. These movements occur with a frequency of up to 7 Hz and are generated by periodic roll movements of the thorax with amplitudes of up to ±60°. During such thorax roll oscillations, the head is held close to horizontal, thereby minimizing rotational optic flow. By having bees fly through an oscillating, patterned drum, we show that head stabilization is based mainly on visual motion cues. Bees exposed to a continuously rotating drum, however, hold their head fixed at an oblique angle. This result shows that although gaze stabilization is driven by visual motion cues, it is limited by other mechanisms, such as the dorsal light response or gravity reception.     

Motion and vision: why animals move their eyes

Nearly all animals with good vision have a repertoire of eye movements. The majority show a pattern of stable fixations with fast saccades that shift the direction of gaze. These movements may be made by the eyes themselves, or the head, or in some insects the whole body. The main reason for keeping gaze still during fixations is the need to avoid the blur that results from the long response time of the photoreceptors. Blur begins to degrade the image at a retinal velocity of about 1 receptor acceptance angle per response time. Some insects (e.g. hoverflies) stabilise their gaze much more rigidly than this rule implies, and it is suggested that the need to see the motion of small objects against a background imposes even more stringent conditions on image motion. A third reason for preventing rotational image motion is to prevent contamination of the translational flow-field, by which a moving animal can judge its heading and the distances of objects. Some animals do let their eyes rotate smoothly, and these include some heteropod molluscs, mantis shrimps and jumping spiders, all of which have narrow linear retinae which scan across the surroundings. Hymenopteran insects also rotate during orientation flights at speeds of 100–200° s⁻¹. This is just consistent with a blur-free image, as are the scanning speeds of the animals with linear retinae. Accepted: 29 April 1999     

A Bio-inspired Collision Avoidance Model Based on Spatial Information Derived from Motion Detectors Leads to Common Routes

Avoiding collisions is one of the most basic needs of any mobile agent, both biological and technical, when searching around or aiming toward a goal. We propose a model of collision avoidance inspired by behavioral experiments on insects and by properties of optic flow on a spherical eye experienced during translation, and test the interaction of this model with goal-driven behavior. Insects, such as flies and bees, actively separate the rotational and translational optic flow components via behavior, i.e. by employing a saccadic strategy of flight and gaze control. Optic flow experienced during translation, i.e. during intersaccadic phases, contains information on the depth-structure of the environment, but this information is entangled with that on self-motion. Here, we propose a simple model to extract the depth structure from translational optic flow by using local properties of a spherical eye. On this basis, a motion direction of the agent is computed that ensures collision avoidance. Flying insects are thought to measure optic flow by correlation-type elementary motion detectors. Their responses depend, in addition to velocity, on the texture and contrast of objects and, thus, do not measure the velocity of objects veridically. Therefore, we initially used geometrically determined optic flow as input to a collision avoidance algorithm to show that depth information inferred from optic flow is sufficient to account for collision avoidance under closed-loop conditions. Then, the collision avoidance algorithm was tested with bio-inspired correlation-type elementary motion detectors in its input. Even then, the algorithm led successfully to collision avoidance and, in addition, replicated the characteristics of collision avoidance behavior of insects. Finally, the collision avoidance algorithm was combined with a goal direction and tested in cluttered environments. The simulated agent then showed goal-directed behavior reminiscent of components of the navigation behavior of insects.     

A test of spatial memory and movement patterns of bumblebees at multiple spatial and temporal scales

Naive bumblebee foragers appear to use movement rules at smallspatial and temporal scales, but it is not clear whether theserules determine movement patterns as the scales increase. Onestrategy for efficient foraging used by bumblebees is near-farsearch, involving short flights when in good patches of flowersand longer flights when in poor patches. Bumblebees also demonstratethe use of a spatial memory strategy by returning repeatedlyto patches of flowers, and even following the same route betweenflowers, over periods of days. We attempted to determine atwhat spatial scales bumblebees use spatial memory while foragingwithin a patch and after how many flower visits spatial memoryoutweighs near-far search. Bumblebees in the laboratory foragedon a 4 x 4 array of artificial flowers with distances rangingfrom 10 to 80 cm between flowers in two simple spatial patterns.The proportion of visits to flowers containing a sucrose rewardwas monitored for either 100 or 400 flower visits in two separateexperiments, after which the locations of the rewarding andnonrewarding flowers were interchanged, producing a mirror image.A drop in accuracy after the mirror image switch would indicatethat the bees had memorized the location of rewarding flowers.Mirror image tests, and comparisons to a simulation model ofnear-far search based on actual flight distances, indicate thatnaive bumblebees used near-far search on flowers 10 cm apartbut increasingly used spatial memory as experience and spatialseparation increased. Bumblebees thus have multiple tacticsavailable to forage efficiently in different environments.     

Saccadic flight strategy facilitates collision avoidance: closed-loop performance of a cyberfly

Behavioural and electrophysiological experiments suggest that blowflies employ an active saccadic strategy of flight and gaze control to separate the rotational from the translational optic flow components. As a consequence, this allows motion sensitive neurons to encode during translatory intersaccadic phases of locomotion information about the spatial layout of the environment. So far, it has not been clear whether and how a motor controller could decode the responses of these neurons to prevent a blowfly from colliding with obstacles. Here we propose a simple model of the blowfly visual course control system, named cyberfly, and investigate its performance and limitations. The sensory input module of the cyberfly emulates a pair of output neurons subserving the two eyes of the blowfly visual motion pathway. We analyse two sensory–motor interfaces (SMI). An SMI coupling the differential signal of the sensory neurons proportionally to the yaw rotation fails to avoid obstacles. A more plausible SMI is based on a saccadic controller. Even with sideward drift after saccades as is characteristic of real blowflies, the cyberfly is able to successfully avoid collisions with obstacles. The relative distance information contained in the optic flow during translatory movements between saccades is provided to the SMI by the responses of the visual output neurons. An obvious limitation of this simple mechanism is its strong dependence on the textural properties of the environment.     

Temporal Structure of Human Gaze Dynamics Is Invariant During Free Viewing

We investigate the dynamic structure of human gaze and present an experimental study of the frequency components of the change in gaze position over time during free viewing of computer-generated fractal images. We show that changes in gaze position are scale-invariant in time with statistical properties that are characteristic of a random walk process. We quantify and track changes in the temporal structure using a well-defined scaling parameter called the Hurst exponent, H. We find H is robust regardless of the spatial complexity generated by the fractal images. In addition, we find the Hurst exponent is invariant across all participants, including those with distinct changes to higher order visual processes due to neural degeneration. The value we find for H of 0.57 shows that the gaze dynamics during free viewing of fractal images are consistent with a random walk process with persistent movements. Our research suggests the human visual system may have a common strategy that drives the dynamics of human gaze during exploration.     

To keep on track during flight,fruitflies discount the skyward view

When small flying insects go off their intended course, they use the resulting pattern of motion on their eye, or optic flow, to guide corrective steering. A change in heading generates a unique, rotational motion pattern and a change in position generates a translational motion pattern, and each produces corrective responses in the wingbeats. Any image in the flow field can signal rotation, but owing to parallax, only the images of nearby objects can signal translation. Insects that fly near the ground might therefore respond more strongly to translational optic flow that occurs beneath them, as the nearby ground will produce strong optic flow. In these experiments, rigidly tethered fruitflies steered in response to computer-generated flow fields. When correcting for unintended rotations, flies weight the motion in their upper and lower visual fields equally. However, when correcting for unintended translations, flies weight the motion in the lower visual fields more strongly. These results are consistent with the interpretation that fruitflies stabilize by attending to visual areas likely to contain the strongest signals during natural flight conditions.     

Impacts of dispersal on rapid adaptation and dynamic stability of Daphnia in fluctuating environments

Prior ecological research has shown that spatial processes can enhance the temporal stability of populations in fluctuating environments. Less explored is the effect of dispersal on rapid adaptation and its concomitant impact on population dynamics. For asexually reproducing populations, theory predicts that dispersal in fluctuating environments can facilitate asynchrony among clones and enhance stability by reducing temporal variability of total population abundance. This effect is predicted when clones exhibit heritable variation in environmental optima and when fluctuations occur asynchronously among patches. We tested this in the field using artificial ponds and metapopulations composed of a diverse assemblage of Daphnia pulex clones. We directly manipulated dispersal presence/absence and environmental fluctuations in the form of nutrient pulses. Consistent with predictions, dispersal enhanced temporal asynchrony among clones in the presence of nutrient pulses; this in turn stabilized population dynamics. This effect only emerged when patches experienced spatially asynchronous nutrient pulses (dispersal had no effect when patches were synchronously pulsed). Clonal asynchrony was driven by strong positive selection for a single clone that exhibited a performance advantage under conditions of low resource availability. Our work highlights the importance of dispersal as a driver of eco-evolutionary dynamics and population stability in variable environments.     

Visuomotor Response to Object Expansion in Free-Flying Bumble Bees

The flight control systems of flying insects enable many kinds of sophisticated maneuvers, including avoidance of midair collisions. Visuomotor response to an approaching object, received as image expansion on insects’ retina, is a complex event in a dynamic environment where both animals and objects are moving. There are intensive free flight studies on the landing response in which insects receive image expansion by their own movement. However, few studies have been conducted regarding how freely flying insects respond to approaching objects. Here, using common laboratory insects for behavioral research, the bumblebee Bombus ignitus, we examined their visual response to an approaching object in the free-flying condition. While the insect was slowly flying in a free-flight arena, an expanding stripe was projected laterally from one side of the arena with a high-speed digital mirror device projector. Rather than turning away reported before, the bumble bees performed complex flight maneuvers. We synchronized flight trajectories, orientations and wing stroke frequencies with projection parameters of temporal resolution in 0.5 ms, and analyzed the instantaneous relationship between visual input and behavioral output. In their complex behavioral responses, we identified the following two visuomotor behaviors: increasing stroke frequency when the bumble bees confront the stripe expansion, and turning towards (not away) the stripe expansion when it is located laterally to the bee. Our results suggested that the response to object expansion is not a simple and reflexive escape but includes object fixation, presumably for subsequent behavioral choice.     

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.     

Through a barn owl’s eyes: interactions between scene content and visual attention

In this study we investigated visual attention properties of freely behaving barn owls, using a miniature wireless camera attached to their heads. The tubular eye structure of barn owls makes them ideal subjects for this research since it limits their eye movements. Video sequences recorded from the owl’s point of view capture part of the visual scene as seen by the owl. Automated analysis of video sequences revealed that during an active search task, owls repeatedly and consistently direct their gaze in a way that brings objects of interest to a specific retinal location (retinal fixation area). Using a projective model that captures the geometry between the eye and the camera, we recovered the corresponding location in the recorded images (image fixation area). Recording in various types of environments (aviary, office, outdoors) revealed significant statistical differences of low level image properties at the image fixation area compared to values extracted at random image patches. These differences are in agreement with results obtained in primates in similar studies. To investigate the role of saliency and its contribution to drawing the owl’s attention, we used a popular bottom-up computational model. Saliency values at the image fixation area were typically greater than at random patches, yet were only 20% out of the maximal saliency value, suggesting a top-down modulation of gaze control.     

Behavioral states help translate dispersal movements into spatial distribution patterns of floaters

Within the field of spatial ecology, it is important to study animal movements in order to better understand population dynamics. Dispersal is a nonlinear process through which different behavioral mechanisms could affect movement patterns. One of the most common approaches to analyzing the trajectories of organisms within patches is to use random-walk models to describe movement features. These models express individual movements within a specific area in terms of random-walk parameters in an effort to relate movement patterns to the distributions of organisms in space. However, only using the movement trajectories of individuals to predict the spatial spread of animal populations may not fit the complex distribution of individuals across heterogeneous environments. When we empirically tested the results from a random-walk model (a residence index) used to predict the spatial equilibrium distribution of individuals, we found that the index severely underestimated the spatial spread of dispersing individuals. We believe this is because random-walk models only account for the effects of environmental conditions on individual movements, completely overlooking the crucial influence of behavior changes over time. In the future, both aspects should be accounted for when predicting general rules of (meta)population abundance, distribution, and dynamics from patterns of animal movements.     

Mechanisms and implications of animal flight maneuverability

Accelerations and directional changes of flying animals derivefrom interactions between aerodynamic force production and theinertial resistance of the body to translation and rotation.Anatomical and allometric features of body design thus mediatethe rapidity of aerial maneuvers. Both translational and rotationalresponsiveness of the body to applied force decrease with increasedtotal mass. For flying vertebrates, contributions of the relativelyheavy wings to whole-body rotational inertia are substantial,whereas the relatively light wings of many insect taxa suggestthat rotational inertia is dominated by the contributions ofbody segments. In some circumstances, inertial features of wingdesign may be as significant as are their aerodynamic propertiesin influencing the rapidity of body rotations. Stability inflight requires force and moment balances that are usually attainedvia bilateral symmetry in wingbeat kinematics, whereas bodyroll and yaw derive from bilaterally asymmetric movements ofboth axial and appendicular structures. In many flying vertebrates,use of the tail facilitates the generation of aerodynamic torquesand substantially enhances quickness of body rotation. Geometricalconstraints on wingbeat kinematics may limit total force productionand thus accelerational capacity in certain behavioral circumstances.Unitary limits to animal flight performance and maneuverabilityare unlikely, however, given varied and context-specific interactionsamong anatomical, biomechanical, and energetic features of design.     

Optic flow-based collision-free strategies: From insects to robots

Flying insects are able to fly smartly in an unpredictable environment. It has been found that flying insects have smart neurons inside their tiny brains that are sensitive to visual motion also called optic flow. Consequently, flying insects rely mainly on visual motion during their flight maneuvers such as: takeoff or landing, terrain following, tunnel crossing, lateral and frontal obstacle avoidance, and adjusting flight speed in a cluttered environment. Optic flow can be defined as the vector field of the apparent motion of objects, surfaces, and edges in a visual scene generated by the relative motion between an observer (an eye or a camera) and the scene. Translational optic flow is particularly interesting for short-range navigation because it depends on the ratio between (i) the relative linear speed of the visual scene with respect to the observer and (ii) the distance of the observer from obstacles in the surrounding environment without any direct measurement of either speed or distance. In flying insects, roll stabilization reflex and yaw saccades attenuate any rotation at the eye level in roll and yaw respectively (i.e. to cancel any rotational optic flow) in order to ensure pure translational optic flow between two successive saccades. Our survey focuses on feedback-loops which use the translational optic flow that insects employ for collision-free navigation. Optic flow is likely, over the next decade to be one of the most important visual cues that can explain flying insects' behaviors for short-range navigation maneuvers in complex tunnels. Conversely, the biorobotic approach can therefore help to develop innovative flight control systems for flying robots with the aim of mimicking flying insects’ abilities and better understanding their flight.     

Effects of long-term space flights on the organization of the horizontal gaze fixation reaction

The results of the Russian-Austrian space experiment Monimir, which was a part of the international space program Austromir, are presented. The characteristics of the horizontal gaze fixation reaction (hGFR) to the visual targets were studied during long-term space flights. Seven crewmembers of the space station Mir participated in our experiment. The subjects were tested four times before the flight, five times during the flight, and three to four times after landing. During the flight and after accomplishing, the characteristics of gaze fixation reaction changed regularly: the reaction time and coefficient of the gain of vestibular-ocular reflex increased; the velocities of eye-head movements increased and decreased. These changes were indicative of a disturbed control of the vestibular-ocular reflex under microgravity conditions because of variability of the vestibular input activity. The cosmonauts that had flight and non-flight professional specializations differed in strategies of their adaptation to the microgravity conditions. In the former, exposure to microgravity was accompanied by gaze hypermetry and inhibition of head movements; conversely, in the latter, the velocity of head movements increased, whereas that of saccades decreased.     

Scanning image correlation spectroscopy

Molecular interactions are at the origin of life. How molecules get at different locations in the cell and how they locate their partners is a major and partially unresolved question in biology that is paramount to signaling. Spatio-temporal correlations of fluctuating fluorescently tagged molecules reveal how they move, interact, and bind in the different cellular compartments. Methods based on fluctuations represent a remarkable technical advancement in biological imaging. Here we discuss image analysis methods based on spatial and temporal correlation of fluctuations, raster image correlation spectroscopy, number and brightness, and spatial cross-correlations that give us information about how individual molecules move in cells and interact with partners at the single molecule level. These methods can be implemented with a standard laser scanning microscope and produce a cellular level spatio-temporal map of molecular interactions.     

Home Range,Movement, and Distribution Patterns of the Threatened Dragonfly Sympetrum depressiusculum (Odonata: Libellulidae): A Thousand Times Greater Territory to Protect?

Dragonflies are good indicators of environmental health and biodiversity. Most studies addressing dragonfly ecology have focused on the importance of aquatic habitats, while the value of surrounding terrestrial habitats has often been overlooked. However, species associated with temporary aquatic habitats must persist in terrestrial environments for long periods. Little is known about the importance of terrestrial habitat patches for dragonflies, or about other factors that initiate or influence dispersal behaviour. The aim of this study was to reveal the relationship between population dynamics of the threatened dragonfly species Sympetrum depressiusculum at its natal site and its dispersal behaviour or routine movements within its terrestrial home range. We used a mark–release–recapture method (marking 2,881 adults) and exuviae collection with the Jolly–Seber model and generalized linear models to analyse seasonal and spatial patterns of routine movement in a heterogeneous Central European landscape. Our results show that utilisation of terrestrial habitat patches by adult dragonflies is not random and may be relatively long term (approximately 3 mo). Adult dragonflies were present only in areas with dense vegetation that provided sufficient resources; the insects were absent from active agricultural patches (p = 0.019). These findings demonstrate that even a species tightly linked to its natal site utilises an area that is several orders of magnitude larger than the natal site. Therefore, negative trends in the occurrence of various dragonfly species may be associated not only with disturbances to their aquatic habitats, but also with changes in the surrounding terrestrial landscape.     

Effects of long-term space flights on organization of horizontal gaze fixation reaction

Results of Russian-Austrian space experiment "Monimir" which was a part of international space program "Austromir" are presented in this paper. Characteristics of horizontal gaze fixation reaction (hGFR) to visual targets were analyzed. Seven crewmembers of "Mir" space station expeditions took part in the experiment. Experiments were carried out 4 times before space flight, 5 times in flight and 3-4 times after landing. There were revealed significant alterations in characteristics of gaze fixation reaction during flight and after its accomplishing, namely: an increase of the time of gaze fixation to the target, changes of eye and head movements' velocity and increase of the gain of vestibular-ocular reflex, that pointed out to the disturbances of the control mechanisms of vestibular-ocular reflex in weightlessness caused by changes of vestibular input's activity. There was discovered also the difference in the strategies of adaptation to microgravity conditions among the cosmonauts of flight and non-flight occupation: in the first group exposure to weightlessness was accompanied by gaze hypermetry and inhibition of head movements; in the second one--on the contrary--by increase of head movement velocity and decrease of saccades' velocity.