Objectively identifying landmark use and predicting flight trajectories of the homing pigeon using Gaussian processes

Pigeons home along idiosyncratic habitual routes from familiar locations. It has been suggested that memorized visual landmarks underpin this route learning. However, the inability to experimentally alter the landscape on large scales has hindered the discovery of the particular features to which birds attend. Here, we present a method for objectively classifying the most informative regions of animal paths. We apply this method to flight trajectories from homing pigeons to identify probable locations of salient visual landmarks. We construct and apply a Gaussian process model of flight trajectory generation for pigeons trained to home from specific release sites. The model shows increasing predictive power as the birds become familiar with the sites, mirroring the animal''s learning process. We subsequently find that the most informative elements of the flight trajectories coincide with landscape features that have previously been suggested as important components of the homing task.     

Interaction rules underlying group decisions in homing pigeons

Travelling in groups gives animals opportunities to share route information by following cues from each other''s movement. The outcome of group navigation will depend on how individuals respond to each other within a flock, school, swarm or herd. Despite the abundance of modelling studies, only recently have researchers developed techniques to determine the interaction rules among real animals. Here, we use high-resolution GPS (global positioning system) tracking to study these interactions in pairs of pigeons flying home from a familiar site. Momentary changes in velocity indicate alignment with the neighbour''s direction, as well as attraction or avoidance depending on distance. Responses were stronger when the neighbour was in front. From the flocking behaviour, we develop a model to predict features of group navigation. Specifically, we show that the interactions between pigeons stabilize a side-by-side configuration, promoting bidirectional information transfer and reducing the risk of separation. However, if one bird gets in front it will lead directional choices. Our model further predicts, and observations confirm, that a faster bird (as measured from solo flights) will fly slightly in front and thus dominate the choice of homing route. Our results explain how group decisions emerge from individual differences in homing flight behaviour.     

Vision-based flight control in the hawkmoth Hyles lineata

Vision is a key sensory modality for flying insects, playing an important role in guidance, navigation and control. Here, we use a virtual-reality flight simulator to measure the optomotor responses of the hawkmoth Hyles lineata, and use a published linear-time invariant model of the flight dynamics to interpret the function of the measured responses in flight stabilization and control. We recorded the forces and moments produced during oscillation of the visual field in roll, pitch and yaw, varying the temporal frequency, amplitude or spatial frequency of the stimulus. The moths’ responses were strongly dependent upon contrast frequency, as expected if the optomotor system uses correlation-type motion detectors to sense self-motion. The flight dynamics model predicts that roll angle feedback is needed to stabilize the lateral dynamics, and that a combination of pitch angle and pitch rate feedback is most effective in stabilizing the longitudinal dynamics. The moths’ responses to roll and pitch stimuli coincided qualitatively with these functional predictions. The moths produced coupled roll and yaw moments in response to yaw stimuli, which could help to reduce the energetic cost of correcting heading. Our results emphasize the close relationship between physics and physiology in the stabilization of insect flight.     

昆虫飞行信息自动化采集装置的设计

针对现有昆虫飞行信息采集方法中存在的采集数据量大、采集效率低和束缚实验对象等问题,设计了一种基于视觉检测技术的自动化采集装置。该装置主要包括障碍通道模块、运动触发采集模块、飞行轨迹信息模块和自动采集控制系统。首先,根据控制功能的需求设计了间隙控制器,采用激光测距传感器和步进电机等硬件实现了闭环控制;其次,采用STM32微控制器为控制终端,并结合运动方向检测算法触发Blackfly S USB3高速相机,实现昆虫在指定运动方向的序列图像采集;然后,利用开源计算机视觉库OpenCV分析采集的序列图像,获取昆虫的飞行轨迹信息;最后,通过嵌入式控制系统协调各模块之间的通信,以达到高效、稳定获取昆虫飞行信息的设计要求。为了验证该装置的适用性和准确率,选取中华蜜蜂进行穿越间隙的实验,实验结果表明：在静态环境中,该装置能获取完整、清晰的飞行序列图像,平均准确率达到73.24%,采集性能稳定,有效提升了采集效率。通过分析蜜蜂的飞行轨迹信息,推断出其识别间隙的机制与横向运动的幅度和速度存在联系,这为深度研究蜜蜂的飞行机制提供了支持。     

Frequency response of lift control in Drosophila

The flight control responses of the fruitfly represent a powerful model system to explore neuromotor control mechanisms, whose system level control properties can be suitably characterized with a frequency response analysis. We characterized the lift response dynamics of tethered flying Drosophila in presence of vertically oscillating visual patterns, whose oscillation frequency we varied between 0.1 and 13 Hz. We justified these measurements by showing that the amplitude gain and phase response is invariant to the pattern oscillation amplitude and spatial frequency within a broad dynamic range. We also showed that lift responses are largely linear and time invariant (LTI), a necessary condition for a meaningful analysis of frequency responses and a remarkable characteristic given its nonlinear constituents. The flies responded to increasing oscillation frequencies with a roughly linear decrease in response gain, which dropped to background noise levels at about 6 Hz. The phase lag decreased linearly, consistent with a constant reaction delay of 75 ms. Next, we estimated the free-flight response of the fly to generate a Bode diagram of the lift response. The limitation of lift control to frequencies below 6 Hz is explained with inertial body damping, which becomes dominant at higher frequencies. Our work provides the detailed background and techniques that allow optomotor lift responses of Drosophila to be measured with comparatively simple, affordable and commercially available techniques. The identification of an LTI, pattern velocity dependent, lift control strategy is relevant to the underlying motion computation mechanisms and serves a broader understanding of insects'' flight control strategies. The relevance and potential pitfalls of applying system identification techniques in tethered preparations is discussed.     

Predicting power-optimal kinematics of avian wings

A theoretical model of avian flight is developed which simulates wing motion through a class of methods known as predictive simulation. This approach uses numerical optimization to predict power-optimal kinematics of avian wings in hover, cruise, climb and descent. The wing dynamics capture both aerodynamic and inertial loads. The model is used to simulate the flight of the pigeon, Columba livia, and the results are compared with previous experimental measurements. In cruise, the model unearths a vast range of kinematic modes that are capable of generating the required forces for flight. The most efficient mode uses a near-vertical stroke–plane and a flexed-wing upstroke, similar to kinematics recorded experimentally. In hover, the model predicts that the power-optimal mode uses an extended-wing upstroke, similar to hummingbirds. In flexing their wings, pigeons are predicted to consume 20% more power than if they kept their wings full extended, implying that the typical kinematics used by pigeons in hover are suboptimal. Predictions of climbing flight suggest that the most energy-efficient way to reach a given altitude is to climb as steeply as possible, subjected to the availability of power.     

Embodied linearity of speed control in Drosophila melanogaster

Fruitflies regulate flight speed by adjusting their body angle. To understand how low-level posture control serves an overall linear visual speed control strategy, we visually induced free-flight acceleration responses in a wind tunnel and measured the body kinematics using high-speed videography. Subsequently, we reverse engineered the transfer function mapping body pitch angle onto flight speed. A linear model is able to reproduce the behavioural data with good accuracy. Our results show that linearity in speed control is realized already at the level of body posture-mediated speed control and is therefore embodied at the level of the complex aerodynamic mechanisms of body and wings. Together with previous results, this study reveals the existence of a linear hierarchical control strategy, which can provide relevant control principles for biomimetic implementations, such as autonomous flying micro air vehicles.     

Apparent power-law distributions in animal movements can arise from intraspecific interactions

Lévy flights have gained prominence for analysis of animal movement. In a Lévy flight, step-lengths are drawn from a heavy-tailed distribution such as a power law (PL), and a large number of empirical demonstrations have been published. Others, however, have suggested that animal movement is ill fit by PL distributions or contend a state-switching process better explains apparent Lévy flight movement patterns. We used a mix of direct behavioural observations and GPS tracking to understand step-length patterns in females of two related butterflies. We initially found movement in one species (Euphydryas editha taylori) was best fit by a bounded PL, evidence of a Lévy flight, while the other (Euphydryas phaeton) was best fit by an exponential distribution. Subsequent analyses introduced additional candidate models and used behavioural observations to sort steps based on intraspecific interactions (interactions were rare in E. phaeton but common in E. e. taylori). These analyses showed a mixed-exponential is favoured over the bounded PL for E. e. taylori and that when step-lengths were sorted into states based on the influence of harassing conspecific males, both states were best fit by simple exponential distributions. The direct behavioural observations allowed us to infer the underlying behavioural mechanism is a state-switching process driven by intraspecific interactions rather than a Lévy flight.     

Visual guidance during bicycle steering through narrow lanes: A study in children

Recently, Vansteenkiste et al. (2013) explored how visual behaviour guides bicycle steering when cycling at different speeds through 15 m long lanes of 10, 25 and 40 cm wide. Participants were found to shift their gaze direction towards the end of the lanes at higher speeds, towards the near pathway on narrow lanes and more towards irrelevant areas on wider lanes. To investigate to what extent young learner bicyclists adapt their visual behaviour in a similar way as adults, the experiment was repeated with seven eight-year-old children, and results were compared to the adult data. Children were found to cycle slower through narrow lanes than adults. However, with increasing lane width and cycling speed, children made the same shifts of visual gaze direction as the adults. These results suggest that for a simple precision steering task, children are able to adopt a similar visual-motor strategy as adults, provided that they cycle at their own pace.     

Predator confusion is sufficient to evolve swarming behaviour

Swarming behaviours in animals have been extensively studied owing to their implications for the evolution of cooperation, social cognition and predator–prey dynamics. An important goal of these studies is discerning which evolutionary pressures favour the formation of swarms. One hypothesis is that swarms arise because the presence of multiple moving prey in swarms causes confusion for attacking predators, but it remains unclear how important this selective force is. Using an evolutionary model of a predator–prey system, we show that predator confusion provides a sufficient selection pressure to evolve swarming behaviour in prey. Furthermore, we demonstrate that the evolutionary effect of predator confusion on prey could in turn exert pressure on the structure of the predator''s visual field, favouring the frontally oriented, high-resolution visual systems commonly observed in predators that feed on swarming animals. Finally, we provide evidence that when prey evolve swarming in response to predator confusion, there is a change in the shape of the functional response curve describing the predator''s consumption rate as prey density increases. Thus, we show that a relatively simple perceptual constraint—predator confusion—could have pervasive evolutionary effects on prey behaviour, predator sensory mechanisms and the ecological interactions between predators and prey.     

Mapping the stereotyped behaviour of freely moving fruit flies

A frequent assumption in behavioural science is that most of an animal''s activities can be described in terms of a small set of stereotyped motifs. Here, we introduce a method for mapping an animal''s actions, relying only upon the underlying structure of postural movement data to organize and classify behaviours. Applying this method to the ground-based behaviour of the fruit fly, Drosophila melanogaster, we find that flies perform stereotyped actions roughly 50% of the time, discovering over 100 distinguishable, stereotyped behavioural states. These include multiple modes of locomotion and grooming. We use the resulting measurements as the basis for identifying subtle sex-specific behavioural differences and revealing the low-dimensional nature of animal motions.     

Leading to distraction: Driver distraction,lead car,and road environment

Driver distraction is strongly associated with crashes and near-misses, and despite the attention this topic has received in recent years, the effect of different types of distracting task on driving performance remains unclear. In the case of non-visual distractions, such as talking on the phone or other engaging verbal tasks that do not require a visual input, a common finding is reduced lateral variability in steering and gaze patterns where participants concentrate their gaze towards the centre of the road and their steering control is less variable. In the experiments presented here, we examined whether this finding is more pronounced in the presence of a lead car (which may provide a focus point for gaze) and whether the behaviour of the lead car has any influence on the driver's steering control. In addition, both visual and non-visual distraction tasks were used, and their effect on different road environments (straight and curved roadways) was assessed. Visual distraction was found to increase variability in both gaze patterns and steering control, non-visual distraction reduced gaze and steering variability in conditions without a lead car; in the conditions where a lead car was present there was no significant difference from baseline. The lateral behaviour of the lead car did not have an effect on steering performance, a finding which indicates that a lead car may not necessarily be used as an information point. Finally, the effects of driver distraction were different for straight and curved roadways, indicating a stronger influence of the road environment in steering than previously thought.     

Downstroke and upstroke conflict during banked turns in butterflies

For all flyers, aeroplanes or animals, making banked turns involve a rolling motion which, due to higher induced drag on the outer than the inner wing, results in a yawing torque opposite to the turn. This adverse yaw torque can be counteracted using a tail, but how animals that lack tail, e.g. all insects, handle this problem is not fully understood. Here, we quantify the performance of turning take-off flights in butterflies and find that they use force vectoring during banked turns without fully compensating for adverse yaw. This lowers their turning performance, increasing turn radius, since thrust becomes misaligned with the flight path. The separation of function between downstroke (lift production) and upstroke (thrust production) in our butterflies, in combination with a more pronounced adverse yaw during the upstroke increases the misalignment of the thrust. This may be a cost the butterflies pay for the efficient thrust-generating upstroke clap, but also other insects fail to rectify adverse yaw during escape manoeuvres, suggesting a general feature in functionally two-winged insect flight. When lacking tail and left with costly approaches to counteract adverse yaw, costs of flying with adverse yaw may be outweighed by the benefits of maintaining thrust and flight speed.     

Raptor wing morphing with flight speed

In gliding flight, birds morph their wings and tails to control their flight trajectory and speed. Using high-resolution videogrammetry, we reconstructed accurate and detailed three-dimensional geometries of gliding flights for three raptors (barn owl, Tyto alba; tawny owl, Strix aluco, and goshawk, Accipiter gentilis). Wing shapes were highly repeatable and shoulder actuation was a key component of reconfiguring the overall planform and controlling angle of attack. The three birds shared common spanwise patterns of wing twist, an inverse relationship between twist and peak camber, and held their wings depressed below their shoulder in an anhedral configuration. With increased speed, all three birds tended to reduce camber throughout the wing, and their wings bent in a saddle-shape pattern. A number of morphing features suggest that the coordinated movements of the wing and tail support efficient flight, and that the tail may act to modulate wing camber through indirect aeroelastic control.     

Experiments and theory of undulatory locomotion in a simple structured medium

Undulatory locomotion of micro-organisms through geometrically complex, fluidic environments is ubiquitous in nature and requires the organism to negotiate both hydrodynamic effects and geometrical constraints. To understand locomotion through such media, we experimentally investigate swimming of the nematode Caenorhabditis elegans through fluid-filled arrays of micro-pillars and conduct numerical simulations based on a mechanical model of the worm that incorporates hydrodynamic and contact interactions with the lattice. We show that the nematode''s path, speed and gait are significantly altered by the presence of the obstacles and depend strongly on lattice spacing. These changes and their dependence on lattice spacing are captured, both qualitatively and quantitatively, by our purely mechanical model. Using the model, we demonstrate that purely mechanical interactions between the swimmer and obstacles can produce complex trajectories, gait changes and velocity fluctuations, yielding some of the life-like dynamics exhibited by the real nematode. Our results show that mechanics, rather than biological sensing and behaviour, can explain some of the observed changes in the worm''s locomotory dynamics.     

Use of multiple modes of flight subsidy by a soaring terrestrial bird,the golden eagle Aquila chrysaetos,when on migration

Large birds regularly use updrafts to subsidize flight. Although most research on soaring bird flight has focused on use of thermal updrafts, there is evidence suggesting that many species are likely to use multiple modes of subsidy. We tested the degree to which a large soaring species uses multiple modes of subsidy to provide insights into the decision-making that underlies flight behaviour. We statistically classified more than 22 000 global positioning satellite–global system for mobile communications telemetry points collected at 30-s intervals to identify the type of subsidized flight used by 32 migrating golden eagles during spring in eastern North America. Eagles used subsidized flight on 87% of their journey. They spent 41.9% ± 1.5 (, range: 18–56%) of their subsidized northbound migration using thermal soaring, 45.2% ± 2.1 (12–65%) of time gliding between thermals, and 12.9% ± 2.2 (1–55%) of time using orographic updrafts. Golden eagles responded to the variable local-scale meteorological events they encountered by switching flight behaviour to take advantage of multiple modes of subsidy. Orographic soaring occurred more frequently in morning and evening, earlier in the migration season, and when crosswinds and tail winds were greatest. Switching between flight modes allowed migration for relatively longer periods each day and frequent switching behaviour has implications for a better understanding of avian flight behaviour and of the evolution of use of subsidy in flight.     

The entropic basis of collective behaviour

We identify a unique viewpoint on the collective behaviour of intelligent agents. We first develop a highly general abstract model for the possible future lives these agents may encounter as a result of their decisions. In the context of these possibilities, we show that the causal entropic principle, whereby agents follow behavioural rules that maximize their entropy over all paths through the future, predicts many of the observed features of social interactions among both human and animal groups. Our results indicate that agents are often able to maximize their future path entropy by remaining cohesive as a group and that this cohesion leads to collectively intelligent outcomes that depend strongly on the distribution of the number of possible future paths. We derive social interaction rules that are consistent with maximum entropy group behaviour for both discrete and continuous decision spaces. Our analysis further predicts that social interactions are likely to be fundamentally based on Weber''s law of response to proportional stimuli, supporting many studies that find a neurological basis for this stimulus–response mechanism and providing a novel basis for the common assumption of linearly additive ‘social forces’ in simulation studies of collective behaviour.     

Mechanistic analysis of the search behaviour of Caenorhabditis elegans

A central question in movement research is how animals use information and movement to promote encounter success. Current random search theory identifies reorientation patterns as key to the compromise between optimizing encounters for both nearby and faraway targets, but how the balance between intrinsic motor programmes and previous environmental experience determines the occurrence of these reorientation behaviours remains unknown. We used high-resolution tracking and imaging data to describe the complete motor behaviour of Caenorhabditis elegans when placed in a novel environment (one in which food is absent). Movement in C. elegans is structured around different reorientation behaviours, and we measured how these contributed to changing search strategies as worms became familiar with their new environment. This behavioural transition shows that different reorientation behaviours are governed by two processes: (i) an environmentally informed ‘extrinsic’ strategy that is influenced by recent experience and that controls for area-restricted search behaviour, and (ii) a time-independent, ‘intrinsic’ strategy that reduces spatial oversampling and improves random encounter success. Our results show how movement strategies arise from a balance between intrinsic and extrinsic mechanisms, that search behaviour in C. elegans is initially determined by expectations developed from previous environmental experiences, and which reorientation behaviours are modified as information is acquired from new environments.     

The visual control of bicycle steering: The effects of speed and path width

Although cycling is a widespread form of transportation, little is known about the visual behaviour of bicycle users. This study examined whether the visual behaviour of cyclists can be explained by the two-level model of steering described for car driving, and how it is influenced by cycling speed and lane width. In addition, this study investigated whether travel fixations, described during walking, can also be found during a cycling task. Twelve adult participants were asked to cycle three 15 m long cycling lanes of 10, 25 and 40 cm wide at three different self-selected speeds (i.e., slow, preferred and fast). Participants’ gaze behaviour was recorded at 50 Hz using a head mounted eye tracker and the resulting scene video with overlay gaze cursor was analysed frame by frame. Four types of fixations were distinguished: (1) travel fixations, (2) fixations inside the cycling lane (path), (3) fixations to the final metre of the lane (goal), and (4) fixations outside of the cycling lane (external). Participants were found to mainly watch the path (41%) and goal (40%) region while very few travel fixations were made (<5%). Instead of travel fixations, an OptoKinetic Nystagmus was revealed when looking at the near path. Large variability between subjects in fixation location suggests that different strategies were used. Wider lanes resulted in a shift of gaze towards the end of the lane and to external regions, whereas higher cycling speeds resulted in a more distant gaze behaviour and more travel fixations. To conclude, the two-level model of steering as described for car driving is not fully in line with our findings during cycling, but the assumption that both the near and the far region is necessary for efficient steering seems valid. A new model for visual behaviour during goal directed locomotion is presented.