Landing strategies in honeybees, and possible applications to autonomous airborne vehicles

Insects, being perhaps more reliant on image motion cues than mammals or higher vertebrates, are proving to be an excellent organism in which to investigate how information on optic flow is exploited to guide locomotion and navigation. This paper describes one example, illustrating how bees perform grazing landings on a flat surface. A smooth landing is achieved by a surprisingly simple and elegant strategy: image velocity is held constant as the surface is approached, thus automatically ensuring that flight speed is close to zero at touchdown. No explicit knowledge of flight speed or height above the ground is necessary. The feasibility of this landing strategy is tested by implementation in a robotic gantry, and its applicability to autonomous airborne vehicles is discussed.     

Do foraging bumblebees scent-mark food sources and does it matter?

Summary The foraging of worker bees of Bombus terrestris visiting artificial feeders in a climatic test chamber was investigated. The behaviour of worker bees visiting rewarding and unrewarding feeders is completely different. Of all flower visits to rewarding feeders 94% are probing-visits, i.e. the bees land on the flower and probe for nectar. In contrast, only 0.3% of all visits to unrewarding feeders are probing-visits, whereas 47% are approach-visits, i.e., the bees approach the feeders without landing. Exchanging feeder discs proves that the signal used for discrimination must be associated with the plastic disc used as landing platform. Most probably it involves scent-marking of the rewarding feeders with components of high and low volatility. The mean foraging efficiency of bees in a scent-marked foraging arena is 5.7 mg sugar/min and drops to 2.8 mg sugar/min after the scent marked discs are replaced by clean ones. Three components generate this drop in foraging efficiency: (1) the between-flower flight time increases, i.e. the bees search for a longer time before landing on flowers, (2) the bees no longer discriminate between rewarding and unrewarding feeders, and (3) the bees probe empty feeders longer than necessary; obviously they expect to find nectar.     

The need for muscle co-contraction prior to a landing

In landings from a flight phase the mass centre of an athlete experiences rapid decelerations. This study investigated the extent to which co-contraction is beneficial or necessary in drop landings, using both experimental data and computer simulations. High speed video and force recordings were made of an elite martial artist performing drop landings onto a force plate from heights of 1.2, 1.5 and 1.8 m. Matching simulations of these landings were produced using a planar 8-segment torque-driven subject-specific computer simulation model. It was found that there was substantial co-activation of joint flexor and extensor torques at touchdown in all three landings. Optimisations were carried out to determine whether landings could be effected without any co-contraction at touchdown. The model was not capable of landing from higher than 1.05 m with no initial flexor or extensor activations. Due to the force–velocity properties of muscle, co-contraction with net zero joint torque at touchdown leads to increased extensor torque and decreased flexor torque as joint flexion velocity increases. The same considerations apply in any activity where rapid changes in net joint torque are required, as for example in jumps from a running approach.     

Intensity contrast as a crucial cue for butterfly landing

Papilio butterflies use a tetrachromatic color vision to discriminate a rewarding flower, approach, land and take nectar from the flower. In the course of further analyzing their foraging behavior in a laboratory condition, we found that some butterflies could not land on the target flower even they discriminated and tried to land on it, especially when the target was dark. This phenomenon, which we call “landing suppression”, indicates that the cue for landing differs from the cue for visually locating a flower. We hypothesized that a possible cue for landing was intensity contrast between the target and background, and have initiated to test this hypothesis. We tested the butterflies’ landing behavior to targets of various colors and intensities presented on background of black or various densities of gray. As a result, the landing was most strongly suppressed when the intensity contrast was close to zero irrespective of the target colors, suggesting that the butterflies used the target-background intensity contrast when landing.     

Tetragonisca guard bees interpret expanding and contracting patterns as unintended displacement in space

Guard bees of the stingless bee Tetragonisca angustula (Apidae: Meliponinae) hover in stable positions in front of the nest to protect the flight corridor leading to the nest entrance against insect intruders. To unravel the visual control of station keeping, we exposed these hovering guards to expanding and contracting patterns at the nest front. The bees fly away from an expanding pattern and towards the centre of a contracting pattern along a line connecting their initial position and the centre of expansion regardless of where in the visual field they view the pattern. The response of bees to a spinning radial pattern is different: they fly parallel to the pattern, up and down or forward and backward depending on whether they initially hover to the side, above or below the centre of rotation. The bees respond to horizontal and to vertical expansion and contraction. They also adjust their distance relative to a rotating spiral which produces a realistic flow field and thus allowed us to test to what extent the bees minimize image motion speed. We find that guard bees indeed move in the appropriate direction to minimize the image motion speed they experience. A comparison of bees hovering at different distances from the nestfront at the onset of pattern motion and experiencing very different image velocities shows that the dynamics of the reaction is quite uniform. At the pattern velocities tested, we did not find evidence that guard bees use image motion to control their flight speed. The bees' response rather suggests that the underlying mechanism might be insensitive to the size of motion vectors. Accepted: 2 April 1997     

Individual bumblebees vary in response to disturbance: a test of the defensive reserve hypothesis

Bees may leave their nest in the event of an attack, but this is not their only response. Here, we examine the behavior of those individuals that remain inside the nest during a disturbance. Specifically, we test the hypothesis that bee workers usually exhibiting high levels of inactivity (i.e., ‘lazy’ bees) may function as defensive reserves that are more likely to respond when the colony is disturbed. We explore this hypothesis by simulating vertebrate attacks by vibrating or blowing carbon dioxide into two colonies on alternating days and measuring the movements and tasks performed by bees inside the nest. Our results show that regardless of the disturbance type, workers increase guarding behavior after a disturbance stops. Although previously inactive bees increased their movement speed inside the nest when the disturbance was vibration, they were not more likely to leave the nest (presumably to attack the simulated attacker) or switch to guarding behavior for any disturbance type. We therefore reject the hypothesis that inactive Bombus impatiens bumblebees act as defensive reserves, and propose alternative hypotheses regarding why many workers remain inactive inside the nest.     

Variability of the thermal behavior of honeybees on a feeding place

Summary The thermoregulation of honeybees (Apis mellifera carnica) was investigated under field conditions, on a feeding place 335 m away from the hive, where 0.25M or 0.5M sucrose solution was offered. By means of real-time tele-thermography, contactless body surface temperature measurements of undisturbed animals were made.The foraging bees showed highly developed individual thermoregulatory abilities. Complex behavioral patterns such as food uptake, active body temperature regulation, and preparation for flight were performed simultaneously. However, body temperature was more variable than expected. When bees drank 0.5M sucrose solution, they generally had a higher thoracic surface temperature (T _Ths) and showed smaller temperature fluctuations (e.g., cooling down after landing) than with 0.25M solution. Given 0.5M sucrose they stayed for shorter periods at the feeding place. The highest (maximum)T _Ths during the stop was positively (linearly) correlated with the ambient temperature (T _a=18–30°C) for both 0.25M and 0.5M sucrose feeding. At aT _a of 19°C the mean (interpolated) maximum values forT _Ths were 37.2°C (0.25M) and 38.5°C (0.5M); at aT _a of 27°C they were 39.2°C (0.25M) and 40.9°C (0.5M). The minimumT _Ths was correlated withT _a only with 0.5M feeding, whereas with 0.25M feeding a great variability was observed. Similarly as the maximumT _Ths,T _Ths upon landing and taking off were positively (linearly) correlated withT _a and were higher during 0.5M feeding.The quality (concentration) of the food offered to the bees obviously influenced their thermal behavior at the feeding place.Abbreviations T _a ambient temperature - T _Ths thoracic surface temperature - IR infra-red     

Nurse bees support the physiological development of young bees (Apis mellifera L.)

Newly emerged worker honeybees (focal bees) were caged individually for 8 days either isolated or together with one companion bee of known age (2–30 days) taken from a colony. The companion bee was replaced every 2nd day. After 8 days, various parameters were investigated in the focal bees as indicators of the level of development. Focal bees which had been caged with 6-day-old companion bees were better developed than isolated focal bees, newly emerged bees, or focal bees caged with almost all other ages of companion bees. They had hypopharyngeal glands that were larger and contained more protein, their thoraces had a higher protein content, and they had a higher rate of proteolytic activity in the midgut. Although the focal bees were supplied with pollen as well as honey, they consumed only small amounts of pollen. We attribute their better development to their having been fed worker jelly by the accompanying companion bees. The 6-day-old companion bees consumed high quantities of pollen and spent more time (18.7 ± 11.85 s/h) feeding focal bees than 12-day-old bees (6.5 ± 4.09 s/h) or foragers (no feeding of focal bees). The results show that even under such artificial conditions, the exchange of food (trophallaxis) promotes the development of young honeybee workers. Accepted: 26 February 1999     

Transfers ofVarroa mites from newly emerged bees: Preferences for age- and function-specific adult bees (Hymenoptera: Apidae)

Movements of the parasitic honey bee mite,Varroa jacobsoni (Oud.) were monitored in several assays as they moved among adult host honey bees,Apis mellifera. We examined the propensity of mites to leave their hosts and to move onto new bee hosts. We also examined their preference for bees of different age and hive function. Mites were standardized by selecting mites from newly emerged worker bees (NEWs). In closed jars, 50% ofVarroa left NEWs irreversibly when no physical path was present for the mites to return to the NEWs; about 90% of mites left newly emerged drones in identical assays. In petri dish arenas, mites were rarely seen off NEW hosts when monitored at 15-min intervals for 4 h; this was the case for single NEWs with one mite (NEWs+) and when a NEW+ and a NEW− (no mites) were placed together in a petri dish. When a NEW+ was held with either a nurse beeor a pollen forager, 25% of the mites moved to the older bees. When both a nurseand a pollen forager were placed in a petri dish with a NEW+, about 50% of the mites transferred to older bees; nurse bees received about 80% of these mites, whereas pollen foragers received significantly fewer mites (about 20%,P < 0.05). Most mite transfers occurred during the first 30 min after combining NEWs+ and test bees. When NEWs+ were combined with bees of known ages, rather than function, mites transferred more often to young bees than to older bees (1- and 5-day-old bees vs. 25-day-old bees,P < 0.05; 1-day-old vs. 13- and 25-day-old bees;P < 0.05). No differences in proportions of transferring mites were seen when the range of bee ages was ≤ 8 days (P > 0.05), implying that the factors mediating the mites’ adult-host preference change gradually with bee age. A possible chemical basis for host choice byVarroa is indicated by their greater propensity to move onto freezer-killed nurse bees than onto freezer-killed pollen foragers (P < 0.05) and by their lower movement onto heat-treated bees than onto control bees (P < 0.05). Bee age, hive function, and directional changes in cuticular chemistry are all correlated. Movements of newly emerged mites in relation to these variables may provide insights into their reproductive success inApis mellifera colonies.     

Costs of diving by wing and foot propulsion in a sea duck,the white-winged scoter

Most birds swim underwater by either feet alone or wings alone, but some sea ducks often use both. For white-winged scoters (Melanitta fusca), we measured costs of dives to 2 m with descent by feet only versus wings + feet (only feet are used at the bottom). Dive costs repaid during the recovery period after a dive bout were an important fraction (27–44%) of total dive costs, and removing costs of extraneous surface behaviors increased resolution of differences between dive types. Scoters using wings + feet had 13% shorter descent duration, 18% faster descent speed, 31% fewer strokes/m, and 59% longer bottom duration than with feet only. The cost of time underwater for dives using wings + feet was 32–37% lower than with feet only (P = 0.09 to 0.15). When indirect methods were used to partition descent costs from costs of ascent and bottom phases, using wings + feet lowered descent cost by an estimated 34%. Thus, using wings + feet increases descent speed and lowers descent cost, leaving more time and energy for bottom foraging. For birds in cold water, the large savings may result from both biomechanical and thermoregulatory factors.     

Behavioural and physical reactions of the Colorado potato beetle, Leptinotarsa decemlineata (Say) (Coleoptera: Chrysomelidae) walking on a slanted surface

 A natural reaction of the adult Colorado potato beetle [Leptinotarsa decemlineata (Say)] is to walk uphill on sloped surfaces. The geotaxis reaction of the beetle was observed on slopes of 20° or steeper. It was demonstrated that the uphill orientation behaviour was not a consequence of physical limitation for across-slope locomotion. The walking speed of insects deviating from the fall line did not change within the range of slope angles tested. The speed of adult beetles decreased with an increase in the slope of the substrate as a reaction to the increased gravitational force vector opposing uphill movement. The larger size of the hind legs might make uphill locomotion more efficient than traversing a sloped surface. As the angle of the slope increased, the gait changed from a 3/3 to a 5/1, as did the posterior and anterior extreme position of the legs. This behaviour might be triggered by the need to maintain balance on slanted surfaces as the vertical projection of the centre of mass on the substrate moved outside the support base pattern at the steeper angles. In one experiment beetles were made to pull a load when walking over a horizontal surface. The loads pulled were equivalent to the gravitational loads opposing forward motion when walking up a slope. No differences in forward speed or gait were observed at the lower-angle equivalent compared to beetles walking on slopes. Differences in speed were noted at slope angles higher than 40° indicating that adaptation of the walking strategy might be needed on steeply slanted surfaces. Received: 2 May 2000 / Accepted in revised form: 11 September 2000     

How long to stay on a plant: the response of bumblebees to encountered nectar levels

This field study shows that the number of flowers visited per bee per plant (Anchusa officinalis) increases with the instantaneous nectar level at the plant. Observations during the season showed that a bee visits more flowers per plant of given nectar level, the lower the overall mean nectar level in the study area. These results agree with predictions from a model based on the ‘marginal value theorem’, but with assumptions and constraints adapted for nectar-foraging bees. It suggests that bumblebees assess the nectar level at a plant by sampling one or a few flowers, which is possible because within-plant nectar volumes are correlated. The bees compare encountered gains to an optimal plant switching threshold equal to the overall mean nectar level and leave an unrewarding plant as soon as possible, but continue to visit the flowers on a rewarding plant. However, the bees leave before having visited all flowers due to a searching constraint. The bees’ response to plant nectar levels results in systematic flower visitation, because visitation to recently depleted flowers is reduced, which reduces the variation of the inter-visit time per flower. Systematic flower visitation implies that the overall mean encountered gain per flower is higher than the overall mean standing crop, as predicted by a model of systematic foraging. However, the sampling and searching constraints on the bees’ response to plant nectar levels increase the variation of the inter-visit time per flower, and thereby limit the degree of systematic flower visitation and the effect on the mean encountered gain.     

Alteration in community-dwelling older adults' level walking following perturbation training

While perturbation training is promising in reducing fall-risk among older adults, its impact on altering their spontaneous gait pattern has not been investigated. The purpose of this study was to determine to what extent older adults' gait pattern would be affected by exposure to repeated slips. Seventy-three community-dwelling older adults (age: 72.6±5.4 years) underwent 24 repeated-slip exposure induced by unannounced unlocking and relocking of low-friction sections of a 7-m pathway upon which they walked. Full body kinematics and kinetics were recorded during the training. The gait parameters and the center of mass (COM) stability against backward balance loss were compared before and after the training. The results revealed that the training reduced fall incidence from 43.8% upon the novel slip to 0 at the end of training. After the training, subjects significantly improved gait stability by forward positioning of their COM relative to the base of support without altering gait speed. This forward COM shift resulted from a shortened step at the end of single stance and forward trunk leaning during double stance. They also adopted flat foot landing with knee flexed at touchdown (with an average change of 6.9 and 4.1 degrees, respectively). The perturbation training did alter community-dwelling older adults' spontaneous gait pattern. These changes enabled them to improve their volitional control of stability and their resistance to unpredictable and unpreventable slip-related postural disturbance.     

The role of receptivity in the courtship behavior of Podocnemis erythrocephala in captivity

The courtship behavior of Podocnemis erythrocephala (Red-headed Amazon River Turtle) in captivity was studied to examine female receptivity and male response to female rejection. We observed 20 females and 39 males in 150 sessions (3–6 h/day for a total of 450 h). In 36% of the trials, there was no interaction between males and females, and 20% of the trials resulted in copulations. All males introduced into tanks approached females, and eventually there was aggression among the males. In 48% of the experiments, females also searched for or approached males. When males initially approached females, they either accepted the male’s advances (14%), rejected the male passively (38%), or rejected the male aggressively (48%). In 86% of the cases where males were rejected, 4% attempted to approach females again, and in 51% they were ultimately successful.     

Landmark orientation during the approach to the nest in the stingless beeTrigona (Tetragonisca) angustula (Apidae,Meliponinae)

Summary We displaced a small nest box containing stingless bees (Trigona (Tetragonisca)angustula) over distances of up to 1.6 meters in different directions and counted the numbers of returning foragers to measure the effects of this manipulation on the homing ability of bees. Bees find it hard to locate the nest box when it was displaced more than about 1 m backwards, forwards or sideways relative to the direction into which the nest entrance pointed. They do not find the nest when its height above ground is changed. The bees use landmarks in the vicinity of the nest to locate it: When the nest box is displaced and landmark positions are changed so that their angular position at the new nest site is the same as at the normal nest position their homing ability is less impaired than it is without changes in landmark positions. Our results show that the bees do not use the nest box itself as a landmark until they have approached the nest position to within about 1 meter with the aid of surrounding landmarks.     

Oil-Gathering Bees Visit Flowers of Eglandular Morphs of the Oil-Producing Malpighiaceae1

The visiting behaviour of oil-gathering, anthophorid bees on eglandular morphs of two Malpighiaceae species was observed in southeastern Brazil. The bees landed on eglandular flowers apparently by mistake, as suggested by their making one to a few scraping movements on landing, and behaving in the same way as they scrape oil glands on glandular flowers. After perceiving their mistake the bees either left the flower, making one to a few additional visits to other eglandular flowers before leaving the plant, or switched to pollen collecting. Large and medium-sized species of Centris, and some Epicharis, left the flowers after mistake visits, thus wasting time and energy, whereas small Centris and larger Epicharis switched to pollen harvesting, thus turning a mistake into a rewarding visit. Eglandular flowers of both Banisteriopsis muricata and Heteropterys aceroides attracted oil-gathering bees by deceit and probably acted as mimics of glandular flowers of their own species (automimicry). The pollination of eglandular morphs of these two Malpighiaceae species seems dependent mainly on the opportunistic, mixed oil-pollen gathering behaviour of deceived bees such as Epicharis schrottkyi. We suggest that some showy, eglandular species such as Banisteriopsis lutea may act as general mimics of other, oil-rewarding Malpighiaceae species.     

Anti-predator Fan-blowing in Guard Bees, <Emphasis Type="Italic">Apis mellifera capensis</Emphasis> Esch

Honeybees employ different defensive strategies depending on the nature of potential predators. The Cape honeybee, Apis mellifera capensis, exhibits a unique fan-blowing behaviour to repel ants and similar sized insects at the nest entrance. Guard bees turn in alternating clockwise and anticlockwise circles on a fixed vertical axis and fan their wings when encountering tramp ants (Pheidole megacephala), aphids (Myzus persicae) and termites (Trinervitermes trinovoides) on the landing board of a hive. The blowing force was constant and was driven by fanning with a wing-beat frequency of 274.8 ± 16.3 Hz, which exceeds that of flight. On the contrary, small hive beetles (Aethina tumida) were removed by mauling and expulsion whereas larvae of the greater waxmoth (Galleria mellonella) and the mealworm (Tenebrio molitor) were seized with mandibles and thrown from the nest area.     

Responses of Metapopulation Dynamics to Two Different Kinds of Habitat Destruction Caused by Human Activities

Habitat destruction can be classified into instantaneous destruction and continuous destruction by the different ways of human destroying habitat. Previous studies, however, always focused on instantaneous destruction. In this study, we develop a universal model, Multi-time scale N-species model, to study and compare the responses of metapopulation dynamics to both kinds of habitat destruction. The model explores that: (1) under instantaneous habitat destruction, species extinction is determined by the proportion of habitat destruction (D) and the structure of metapopulation (q). When D>q, species will go extinct ranked from the best competitor to the worst. When D≤ q, no species will go extinct, but the equilibrium abundances of odd-ranked competitors will decrease, and the equilibrium abundances of even-ranked competitors will increase; (2) under continuous destruction, species extinction is dependent on the speed of habitat destruction and the metapopulation structure. The higher the speed of habitat destruction and the bigger q are, the earlier species go extinct. Usually, there are two possible mechanisms of species extinction: one is that all species go extinct collectively following complete destruction, and the other is that species go extinct in ranked competitive order from best to worst, and the survivals, if they exist, will go extinct collectively following complete destruction. The oscillation amplitudes of inferior competitors are so large as to increase the probability of stochastic extinction under instantaneous destruction. Therefore, it is relatively propitious for the persistence of rare species under slow and continuous destruction, especially when continuous destruction stops.     

Object detection by honeybees: Why do they land on edges?

Behavioural experiments using a variety of experimental situations (Figs. 1, 3, 6, 7, 9) were conducted to investigate the visual cues which bees use in the task of object-ground discrimination. The bees' flight and landing behaviour was video-filmed throughout the experiments. The evaluation of the video data shows that bees trained to find a randomly textured figure raised above a similarly textured ground land mainly on the boundaries of the figure, facing its inner surface (Fig. 2a, b). Bees can also be trained to find a hole, i.e. a low texture viewed through a window cut in a raised texture, but these bees are not attracted to the edges of the hole (Fig. 5a, b). Bees trained to a single edge between a low and a raised random texture land at the edge mainly facing the raised side (Table 1). Bees approaching the edge from the high side cross the edge in most cases without landing on it (Table 1). Bees trained to an edge between 2 striped patterns, one raised above the other, again land on the edge facing the raised pattern, regardless of whether the stripes on the 2 patterns run parallel or perpendicular to each other or to the edge (Fig. 8). In this case, the bees acquire range information by flying in oblique directions with respect to the orientation of the stripes (Fig. 10). All of the results suggest that the edge elicits landings when the bee perceives a local increase in the speed of image motion, signalling an abrupt decrease in range. This is corroborated by the results of further experiments in which artificial motion was used to simulate range differences between the two sides of an edge (Table 2). We conclude that image speed is a powerful cue in range discrimination as well as object detection. Dedicated to G. Adrian Horridge on the occasion of his retirement     

Role of stability and limb support in recovery against a fall following a novel slip induced in different daily activities

The purpose of this study was to determine whether stability and limb support play a similar role in governing slip outcome in gait-slip as in sit-to-stand-slip, and whether such prediction could also be derived based on measures of these variables during regular, unperturbed movements. Fifty-three and forty-one young subjects all took one recovery step following an unannounced, novel, forward slip induced in gait and in sit-to-stand, respectively. Logistic regression was used to predict recovery outcome based on preslip and reactive measures of stability and limb support across tasks. Following slip onset, all subjects in both tasks experienced rapid decay in stability and limb support (indicated by a hip descent), leading to some actual falls that could not have been predicted from regular, preslip walking. Immediately before recovery step touchdown, stability and limb support could together best predict 88.9% and 100% falls, respectively, for gait-slip and sit-to-stand-slip. Because of differences in the execution of the recovery step, stability became a better predictor of fallers in sit-to-stand-slip than in gait-slip after recovery limb touchdown. Recovery steps were highly effective in restoring stability, regardless of outcome and task. The predictive strength of stability diminished in gait-slip or reduced in sit-to-stand-slip after recovery touchdown, while limb support remained able to differentiate fallers from those who recovered in both tasks. When slip-induced instability was combined with inadequate limb support, falls were nearly inevitable in both tasks.