Honeybee odometry: performance in varying natural terrain

Recent studies have shown that honeybees flying through short, narrow tunnels with visually textured walls perform waggle dances that indicate a much greater flight distance than that actually flown. These studies suggest that the bee's “odometer” is driven by the optic flow (image motion) that is experienced during flight. One might therefore expect that, when bees fly to a food source through a varying outdoor landscape, their waggle dances would depend upon the nature of the terrain experienced en route. We trained honeybees to visit feeders positioned along two routes, each 580 m long. One route was exclusively over land. The other was initially over land, then over water and, finally, again over land. Flight over water resulted in a significantly flatter slope of the waggle-duration versus distance regression, compared to flight over land. The mean visual contrast of the scenes was significantly greater over land than over water. The results reveal that, in outdoor flight, the honeybee's odometer does not run at a constant rate; rather, the rate depends upon the properties of the terrain. The bee's perception of distance flown is therefore not absolute, but scene-dependent. These findings raise important and interesting questions about how these animals navigate reliably.     

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.     

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.     

Common principle of guidance by echolocation and vision

1. Using echolocation, bats move as gracefully as birds through the cluttered environment, suggesting common principles of optic and acoustic guidance. We tested the idea by analysing braking control of bats (Macroderma gigas) flying through a narrow aperture with eyes covered and uncovered. 2. Though braking control would seem to require rapid detection of distance and velocity and computation of deceleration, simpler control is possible using the tau function of any sensory variable S that is a power function of distance to aperture. Tau function of S is tau (S) = S/S (the dot means time derivative). Controlled braking is achievable by keeping tau (S) constant. 3. Previous experiments indicated the tau (S) constant procedure is followed by humans and birds in visually controlling braking. Analysis of the bats' flight trajectories indicated they too followed the braking procedure using echolocation. 4. The tau function of echo-delay or of echo-intensity or of angle subtended by directions of echoes from two points on the approach surface could be used to control braking. Aperture size was modulated during flight on some trials in an attempt to test between these possibilities, but the results were inconclusive.     

The scaling of eye size with body mass in birds

We developed a simple method that uses skulls to estimate the diameter, and hence the mass, of birds'' eyes. Allometric analysis demonstrated that, within five orders (parrots, pigeons, petrels, raptors and owls) and across 104 families of flying birds, eye mass is proportional to (body mass)^0.68 over a range of body masses (6 g to 11.3 kg). As expected from their habits and visual ecology, raptors and owls have enlarged eyes, with masses 1.4 and 2.2 times greater than average birds of the same weight. Taking existing relationships for flight speed on body mass, we find that resolution increases close to (flight speed)^1.333. Consequently, large birds resolve objects at a longer time to contact than small birds. Eye radius and skull size co-vary in strict proportion, suggesting common physiological, aerodynamic and mechanical constraints. Because eye mass scales close to brain mass, metabolic rate and information processing could also be limiting, but the precise factors determining the scaling of eye to body have not been identified.     

Wind estimation based on thermal soaring of birds

The flight performance of birds is strongly affected by the dynamic state of the atmosphere at the birds' locations. Studies of flight and its impact on the movement ecology of birds must consider the wind to help us understand aerodynamics and bird flight strategies. Here, we introduce a systematic approach to evaluate wind speed and direction from the high‐frequency GPS recordings from bird‐borne tags during thermalling flight. Our method assumes that a fixed horizontal mean wind speed during a short (18 seconds, 19 GPS fixes) flight segment with a constant turn angle along a closed loop, characteristic of thermalling flight, will generate a fixed drift for each consequent location. We use a maximum‐likelihood approach to estimate that drift and to determine the wind and airspeeds at the birds' flight locations. We also provide error estimates for these GPS‐derived wind speed estimates. We validate our approach by comparing its wind estimates with the mid‐resolution weather reanalysis data from ECMWF, and by examining independent wind estimates from pairs of birds in a large dataset of GPS‐tagged migrating storks that were flying in close proximity. Our approach provides accurate and unbiased observations of wind speed and additional detailed information on vertical winds and uplift structure. These precise measurements are otherwise rare and hard to obtain and will broaden our understanding of atmospheric conditions, flight aerodynamics, and bird flight strategies. With an increasing number of GPS‐tracked animals, we may soon be able to use birds to inform us about the atmosphere they are flying through and thus improve future ecological and environmental studies.     

Visually induced height orientation of the fly Musca domestica

The visually controlled height orientation of fixed flying flies (Musca domestica) was investigated. The flight lift force measured by a transducer drives the vertical motion of a panorama. The dynamical conditions of the free flight are electronically simulated for the fly with respect to this degree of freedom of motion. In most of the experimentally investigated cases the panorama consists of a horizontally oriented narrow dark stripe on a bright background. The fly orientates with respect to the stripe, transporting it into a stable fixation position just below the equatorial plane of its compound eyes. It is experimentally demonstrated that the formalism of the linearized theory of the pattern induced flight orientation — Poggio and Reichardt (1973a) — can be applied to describe the height orientation of the fly. The experimental evidence concerning the simultaneous perception of stripes moving in a well defined manner in front of each of the two compound eyes is consistent with the hypothesis that the two halves of the visual system are perceptually additive.     

Maximal horizontal flight performance of hummingbirds: effects of body mass and molt

Hovering and fast forward flapping represent two strenuous types of flight that differ in aerodynamic power requirement. Maximal capabilities of ruby-throated hummingbirds (Archilochus colubris) in hovering and forward flight were compared under varying body mass and wing area. The capability to hover in low-density gas mixtures was adversely affected by body mass, whereas the capability to fly in a wind tunnel did not show any adverse mass effect. Molting birds that lost primary flight feathers and reduced wing area also displayed mass loss and loss of aerodynamic power and flight speed. This suggests that maximal flight speed is insensitive to short-term perturbations of body mass but that molting is stressful and reduces the birds' speed and capacity for chase and escape. Hummingbirds' flight behavior in confined space was also investigated. Birds reduced their speeds flying through a narrow tube to approximately one-fifth of that in the wind tunnel and did not display differences under varying body mass and wing area. Hence, performance in the flight tube was submaximal and did not correlate with performance variation in the wind tunnel. For ruby-throated hummingbirds, both maximal mass-specific aerodynamic power derived from hovering performance in low-density air media and maximal flight velocity measured in the wind tunnel were invariant with body mass.     

Influence of flight time and flight environment on distance communication by dancing honey bees

Forager honey bees communicate the distance of food sources to nest mates through waggle dances, but how do bees measure these distances? Recent work suggests that bees measure distance flown in terms of the extent of image motion (integrated optic flow) that is experienced during flight. However, it is known that optic flow also regulates the speed of flight. Therefore, the duration of the flight to a destination is likely to co-vary with the optic flow that is experienced en route. This makes it difficult to tease apart the potential roles of flight duration and optic flow as cues in estimating distance flown. Here we examine whether flight duration alone can serve as an indicator of distance. We trained bees to visit feeders at two sites located in optically different environments, but positioned such that the flight durations to the two sites were similar. The distance estimates for the two sites, as reported in the waggle dance, were compared. We found that dances differed significantly between the two sites, even though flight times were similar. Flight time perse was a poor predictor of waggle dance behaviour. We conclude that foraging bees do not simply signal flight time as their measure of distance in the waggle dance; the environment through which they fly plays a dominant role. Received 11 April 2005; revised 16 May 2005; accepted 3 June 2005.     

Metabolism during flight in two species of bats, Phyllostomus hastatus and Pteropus gouldii.

The energetic cost of flight in a wind-tunnel was measured at various combinations of speed and flight angle from two species of bats whose body masses differ by almost an order of magnitude. The highest mean metabolic rate per unit body mass measured from P. hastatus (mean body mass, 0.093 kg) was 130.4 Wkg-1, and that for P. gouldii (mean body mass, 0.78 kg) was 69.6 Wkg-1. These highest metabolic rates, recorded from flying bats, are essentially the same as those predicted for flying birds of the same body masses, but are from 2.5 to 3.0 times greater than the highest metabolic rates of which similar-size exercising terrestrial mammals appear capable. The lowest mean rate of energy utilization per unit body mass P. hastatus required to sustain level flight was 94.2 Wkg-1 and that for P. gouldii was 53.4 Wkg-1. These data from flying bats together with comparable data for flying birds all fall along a straight line when plotted on double logarithmic coordinates as a function of body mass. Such data show that even the lowest metabolic requirements of bats and birds during level flight are about twice the highest metabolic capabilities of similar-size terrestrial mammals. Flying bats share with flying birds the ability to move substantially greater distance per unit energy consumed than walking or running mammals. Calculations show that P. hastatus requires only one-sixth the energy to cover a given distance as does the same-size terrestrial mammal, while P. gouldii requires one-fourth the energy of the same-size terrestrial mammal. An empirically derived equation is presented which enables one to make estimates of the metabolic rates of bats and birds during level flight in nature from body mass data alone. Metabolic data obtained in this study are compared with predictions calculated from an avian flight theory.     

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.     

Visual ground pattern modulates flight speed of male Oriental fruit moth Grapholita molesta

Insects flying in a horizontal pheromone plume must attend to visual cues to ensure that they make upwind progress. Moreover, it is suggested that flying insects will also modulate their flight speed to maintain a constant retinal angular velocity of terrestrial contrast elements. Evidence from flies and honeybees supports such a hypothesis, although tests with male moths and beetles flying in pheromone plumes are not conclusive. These insects typically fly faster at higher elevations above a high‐contrast ground pattern, as predicted by the hypothesis, although the increase in speed is not sufficient to demonstrate quantitatively that they maintain constant visual angular velocity of the ground pattern. To test this hypothesis more rigorously, the flight speed of male oriental fruit moths (OFM) Grapholita molesta Busck (Lepidoptera: Tortricidae) flying in a sex pheromone plume in a laboratory wind tunnel is measured at various heights (5–40 cm) above patterns of different spatial wavelength (1.8–90°) in the direction of flight. The OFM modulate their flight speed three‐fold over different patterns. They fly fastest when there is no pattern in the tunnel or the contrast elements are too narrow to resolve. When the spatial wavelength of the pattern is sufficiently wide to resolve, moths fly at a speed that tends to maintain a visual contrast frequency of 3.5 ± 3.2 Hz rather than a constant angular velocity, which varies from 57 to 611° s^?1. In addition, for the first time, it is also demonstrated that the width of a contrast pattern perpendicular to the flight direction modulates flight speed.     

Visual control of navigation in insects and its relevance for robotics

Flying insects display remarkable agility, despite their diminutive eyes and brains. This review describes our growing understanding of how these creatures use visual information to stabilize flight, avoid collisions with objects, regulate flight speed, detect and intercept other flying insects such as mates or prey, navigate to a distant food source, and orchestrate flawless landings. It also outlines the ways in which these insights are now being used to develop novel, biologically inspired strategies for the guidance of autonomous, airborne vehicles.     

Flight dynamics of Cory’s shearwater foraging in a coastal environment

Flight dynamics theories are influenced by two major topics: how birds adapt their flight to cope with heterogeneous habitats, and whether birds plan to use the wind field or simply experience it. The aim of this study was to understand the flight dynamics of free-flying Cory’s shearwaters in relation to the wind characteristics on the coastal upwelling region of continental Portugal. We deployed recently miniaturised devices—global positioning system loggers to collect precise and detailed information on birds’ positions and motions. Prevalent winds were blowing from the north-east and adults used those winds by adjusting their flight directions mainly towards north-west and south-west, flying with cross and tail winds, respectively, and avoiding head winds. This is confirmation that Cory’s shearwaters use a shear soaring flying strategy while exploiting the environment for food: adults foraged mainly with cross winds and their ground speed was not constant during all foraging trips as it changed dynamically as a result of the ocean surface shear winds. During travelling phases, ground speed was strongly influenced by the position of the bird with regard to the wind direction, as ground speed increased significantly with increasing tail wind component (TWC) values. Adults appear to choose foraging directions to exploit ambient wind, in order to improve shear soaring efficiency (cross winding) and exploit diurnal changes in tail wind strength to maximise commuting efficiency. We report, for the first time, precise ground speed values (GPS-derived data) and computed actual flight speed values (using TWC analysis) for Cory’s shearwater.     

Estimating flight height and flight speed of breeding Piping Plovers

Collisions with wind turbines are an increasing conservation concern for migratory birds that already face many threats. Existing collision‐risk models take into account parameters of wind turbines and bird flight behavior to estimate collision probability and mortality rates. Two behavioral characteristics these models require are the proportion of birds flying at the height of the rotor swept‐zone and the flight speed of birds passing through the rotor swept‐zone. In recent studies, investigators have measured flight height and flight speed of migrating birds using fixed‐beam radar and thermal imaging. These techniques work well for fixed areas where migrants commonly pass over, but they cannot readily provide species‐specific information. We measured flight heights of a nesting shorebird, the federally threatened Piping Plover (Charadrius melodus), using optical range finding and measured flight speed using videography. Several single‐turbine wind projects have been proposed for the Atlantic coast of the United States where they may pose a potential threat to these plovers. We studied Piping Plovers in New Jersey and Massachusetts during the breeding seasons of 2012 and 2013. Measured flight heights ranged from 0.7 to 10.5 m with a mean of 2.6 m (N = 19). Concurrent visually estimated flight heights were all within 2 m of measured heights and most within 1 m. In separate surveys, average visually estimated flight height was 2.6 m (N = 1674) and ranged from 0.25 m to 40 m. Average calculated flight speed was 9.30 m/s (N = 17). Optical range finding was challenging, but provided a useful way to calibrate visual estimates where frames of reference were lacking in the environment. Our techniques provide comparatively inexpensive, replicable procedures for estimating turbine collision‐risk parameters where the focus is on discrete nesting areas of specific species where birds follow predictable flight paths.     

Visual flight control in naturalistic and artificial environments

Although the visual flight control strategies of flying insects have evolved to cope with the complexity of the natural world, studies investigating this behaviour have typically been performed indoors using simplified two-dimensional artificial visual stimuli. How well do the results from these studies reflect the natural behaviour of flying insects considering the radical differences in contrast, spatial composition, colour and dimensionality between these visual environments? Here, we aim to answer this question by investigating the effect of three- and two-dimensional naturalistic and artificial scenes on bumblebee flight control in an outdoor setting and compare the results with those of similar experiments performed in an indoor setting. In particular, we focus on investigating the effect of axial (front-to-back) visual motion cues on ground speed and centring behaviour. Our results suggest that, in general, ground speed control and centring behaviour in bumblebees is not affected by whether the visual scene is two- or three dimensional, naturalistic or artificial, or whether the experiment is conducted indoors or outdoors. The only effect that we observe between naturalistic and artificial scenes on flight control is that when the visual scene is three-dimensional and the visual information on the floor is minimised, bumblebees fly further from the midline of the tunnel. The findings presented here have implications not only for understanding the mechanisms of visual flight control in bumblebees, but also for the results of past and future investigations into visually guided flight control in other insects.     

Nocturnal insects use optic flow for flight control

To avoid collisions when navigating through cluttered environments, flying insects must control their flight so that their sensory systems have time to detect obstacles and avoid them. To do this, day-active insects rely primarily on the pattern of apparent motion generated on the retina during flight (optic flow). However, many flying insects are active at night, when obtaining reliable visual information for flight control presents much more of a challenge. To assess whether nocturnal flying insects also rely on optic flow cues to control flight in dim light, we recorded flights of the nocturnal neotropical sweat bee, Megalopta genalis, flying along an experimental tunnel when: (i) the visual texture on each wall generated strong horizontal (front-to-back) optic flow cues, (ii) the texture on only one wall generated these cues, and (iii) horizontal optic flow cues were removed from both walls. We find that Megalopta increase their groundspeed when horizontal motion cues in the tunnel are reduced (conditions (ii) and (iii)). However, differences in the amount of horizontal optic flow on each wall of the tunnel (condition (ii)) do not affect the centred position of the bee within the flight tunnel. To better understand the behavioural response of Megalopta, we repeated the experiments on day-active bumble-bees (Bombus terrestris). Overall, our findings demonstrate that despite the limitations imposed by dim light, Megalopta-like their day-active relatives-rely heavily on vision to control flight, but that they use visual cues in a different manner from diurnal insects.     

Effects of host-odour plume altitude and changing wind velocity on upwind flight manoeuvres of a specialist braconid parasitoid

Abstract. Females of the specialist parasitoid, Microplitis croceipes (Cresson) (Hymenoptera: Braconidae), were released in a wind tunnel into host-odour plumes dispersed by winds of three velocities and winds whose speed was changed while the wasps were engaged in upwind flight. In steady winds of 61, 122 and 183 cms-^-1, wasps maintained similar 'preferred' ground speeds by adjusting their airspeed, while turning to a lesser degree as wind velocity increased. In winds of changing velocity (either increasing or decreasing within a 60–100 cm s-¹ range), wasps lowered their rate of upwind progress, leading to more tortuous tracks. During changing wind speeds longitudinal image flow decreased. Wasps flying in host-odour plumes 10 cm and 20 cm above the flight tunnel floor in a 122 cm s-¹ wind had similar ground speeds; thus their rate of ventral visual image flow varied two-fold. M.croceipes may 'aim' upwind by comparing how changes in the course angle vary with the direction of visual image flow. During changing wind velocities the relationship between changes in visual and flight muscle generated torque is ambiguous. Under these conditions most wasps cast, a manoeuvre characterized by wide lateral excursions across the wind without upwind progress. Once wind speed stabilizes, flight straightens out and upwind flight resumes.     

Flight Energetics in Birds

SYNOPSIS. Some birds can fly for more than 1000 kilometers withoutfeeding. Are these distances compatible with the fuel reservesand the power requirements that flying birds are thought tohave? The fuel for flight is primarily fat, which can make up50% of the total body mass of a bird prior to a long distanceflight. As the bird uses up fuel during the flight and becomeslighter, the power requirements of flight probably decrease.However, a constant power requirement can be assumed throughoutthe flight without introducing serious errors into the estimateof maximum flight distance at a given flight speed. Variousmethods that have been used to estimate the power requirementsof flight are reviewed. Estimates based on indirect calorimetryindicate that the maximum flight distances of birds, when agiven proportion of body mass is used as fuel, are directlyproportional to body mass raised to the 0.227 power. Calculatedvalues of range suggest that birds have small margins of safelyin long, over-water flights unless they are aided by winds orvertical air currents.     

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.