The effect of optic flow cues on honeybee flight control in wind

To minimize the risk of colliding with the ground or other obstacles, flying animals need to control both their ground speed and ground height. This task is particularly challenging in wind, where head winds require an animal to increase its airspeed to maintain a constant ground speed and tail winds may generate negative airspeeds, rendering flight more difficult to control. In this study, we investigate how head and tail winds affect flight control in the honeybee Apis mellifera, which is known to rely on the pattern of visual motion generated across the eye—known as optic flow—to maintain constant ground speeds and heights. We find that, when provided with both longitudinal and transverse optic flow cues (in or perpendicular to the direction of flight, respectively), honeybees maintain a constant ground speed but fly lower in head winds and higher in tail winds, a response that is also observed when longitudinal optic flow cues are minimized. When the transverse component of optic flow is minimized, or when all optic flow cues are minimized, the effect of wind on ground height is abolished. We propose that the regular sidewards oscillations that the bees make as they fly may be used to extract information about the distance to the ground, independently of the longitudinal optic flow that they use for ground speed control. This computationally simple strategy could have potential uses in the development of lightweight and robust systems for guiding autonomous flying vehicles in natural environments.     

If a bird flies in the forest,does an insect hear it?

Birds are major predators of many eared insects including moths, butterflies, crickets and cicadas. We provide evidence supporting the hypothesis that insect ears can function as ‘bird detectors’. First, we show that birds produce flight sounds while foraging. Eastern phoebes (Sayornis phoebe) and chickadees (Poecile atricapillus) generate broadband sounds composed of distinct repetitive elements (approx. 18 and 20 Hz, respectively) that correspond to cyclic wing beating. We estimate that insects can detect an approaching bird from distances of at least 2.5 m, based on insect hearing thresholds and sound level measurements of bird flight. Second, we show that insects with both high and low frequency hearing can hear bird flight sounds. Auditory nerve cells of noctuid moths (Trichoplusia ni) and nymphalid butterflies (Morpho peleides) responded in a bursting pattern to playbacks of an attacking bird. This is the first study to demonstrate that foraging birds generate flight sound cues that are detectable by eared insects. Whether insects exploit these sound cues, and alternatively, if birds have evolved sound-reducing foraging tactics to render them acoustically ‘cryptic’ to their prey, are tantalizing questions worthy of further investigation.     

Biomechanics and biomimetics in insect-inspired flight systems

Insect- and bird-size drones—micro air vehicles (MAV) that can perform autonomous flight in natural and man-made environments are now an active and well-integrated research area. MAVs normally operate at a low speed in a Reynolds number regime of 10⁴–10⁵ or lower, in which most flying animals of insects, birds and bats fly, and encounter unconventional challenges in generating sufficient aerodynamic forces to stay airborne and in controlling flight autonomy to achieve complex manoeuvres. Flying insects that power and control flight by flapping wings are capable of sophisticated aerodynamic force production and precise, agile manoeuvring, through an integrated system consisting of wings to generate aerodynamic force, muscles to move the wings and a control system to modulate power output from the muscles. In this article, we give a selective review on the state of the art of biomechanics in bioinspired flight systems in terms of flapping and flexible wing aerodynamics, flight dynamics and stability, passive and active mechanisms in stabilization and control, as well as flapping flight in unsteady environments. We further highlight recent advances in biomimetics of flapping-wing MAVs with a specific focus on insect-inspired wing design and fabrication, as well as sensing systems.This article is part of the themed issue ‘Moving in a moving medium: new perspectives on flight’.     

To what extent can the tiny parasitoid wasps,Eretmocerus mundus,fly upwind?

Body miniaturization in insects is predicted to result in decreased flight speed and therefore limited ability of these insects to fly upwind. Therefore, tiny insects are often regarded as relying on passive dispersal by winds. We tested this assumption in a wind tunnel by measuring the burst speed of Eretmocerus mundus (Mercet), a beneficial parasitoid wasp with body length <1 mm. Insects were filmed flying upwind towards a UV light source in a range of wind speed 0–0.5 m/s. The Insects flew towards the UV light in the absence and presence of wind but increased their flight speed in the presence of wind. They also changed flight direction to be directly upwind and maintained this body orientation even while drifted backwards relative to the ground by stronger winds. Field measurements showed that the average flight speed observed in the wind tunnel (0.3 m/s) is sufficient to allow flying between plants even when the wind speed above the vegetation was 3–5 folds higher. A simulation of the ability of the insects to control their flight trajectory towards a visual target (sticky traps) in winds show that the insects can manipulate their progress relative to the ground even when the wind speed exceeds their flight speed. The main factors determining the ability of the insects to reach the trap were trap diameter and the difference between insect flight speed and wind speed. The simulation also predicts the direction of arrival to the sticky target showing that many of the insects reach the target from the leeward side (i.e. by flight upwind). In light of these results, the notion that miniature insects passively disperse by winds is misleading because it disregards the ability of the insects to control their drift relative to the ground in winds that are faster than their flight speed.     

Orientation Cues for High-Flying Nocturnal Insect Migrants: Do Turbulence-Induced Temperature and Velocity Fluctuations Indicate the Mean Wind Flow?

Migratory insects flying at high altitude at night often show a degree of common alignment, sometimes with quite small angular dispersions around the mean. The observed orientation directions are often close to the downwind direction and this would seemingly be adaptive in that large insects could add their self-propelled speed to the wind speed, thus maximising their displacement in a given time. There are increasing indications that high-altitude orientation may be maintained by some intrinsic property of the wind rather than by visual perception of relative ground movement. Therefore, we first examined whether migrating insects could deduce the mean wind direction from the turbulent fluctuations in temperature. Within the atmospheric boundary-layer, temperature records show characteristic ramp-cliff structures, and insects flying downwind would move through these ramps whilst those flying crosswind would not. However, analysis of vertical-looking radar data on the common orientations of nocturnally migrating insects in the UK produced no evidence that the migrants actually use temperature ramps as orientation cues. This suggests that insects rely on turbulent velocity and acceleration cues, and refocuses attention on how these can be detected, especially as small-scale turbulence is usually held to be directionally invariant (isotropic). In the second part of the paper we present a theoretical analysis and simulations showing that velocity fluctuations and accelerations felt by an insect are predicted to be anisotropic even when the small-scale turbulence (measured at a fixed point or along the trajectory of a fluid-particle) is isotropic. Our results thus provide further evidence that insects do indeed use turbulent velocity and acceleration cues as indicators of the mean wind direction.     

Flying bats use serial sampling to locate odour sources

Olfactory tracking generally sacrifices speed for sensitivity, but some fast-moving animals appear surprisingly efficient at foraging by smell. Here, we analysed the olfactory tracking strategies of flying bats foraging for fruit. Fruit- and nectar-feeding bats use odour cues to find food despite the sensory challenges derived from fast flight speeds and echolocation. We trained Jamaican fruit-eating bats (Artibeus jamaicensis) to locate an odour reward and reconstructed their flight paths in three-dimensional space. Results confirmed that bats relied upon olfactory cues to locate a reward. Flight paths revealed a combination of odour- and memory-guided search strategies. During ‘inspection flights’, bats significantly reduced flight speeds and flew within approximately 6 cm of possible targets to evaluate the presence or absence of the odour cue. This behaviour combined with echolocation explains how bats maximize foraging efficiency while compensating for trade-offs associated with olfactory detection and locomotion.     

Further Explorations of the Facing Bias in Biological Motion Perception: Perspective Cues,Observer Sex,and Response Times

The human visual system has evolved to be highly sensitive to visual information about other persons and their movements as is illustrated by the effortless perception of point-light figures or ‘biological motion’. When presented orthographically, a point-light walker is interpreted in two anatomically plausible ways: As ‘facing the viewer’ or as ‘facing away’ from the viewer. However, human observers show a ‘facing bias’: They perceive such a point-light walker as facing towards them in about 70-80% of the cases. In studies exploring the role of social and biological relevance as a possible account for the facing bias, we found a ‘figure gender effect’: Male point-light figures elicit a stronger facing bias than female point-light figures. Moreover, we also found an ‘observer gender effect’: The ‘figure gender effect’ was stronger for male than for female observers. In the present study we presented to 11 males and 11 females point-light walkers of which, very subtly, the perspective information was manipulated by modifying the earlier reported ‘perspective technique’. Proportions of ‘facing the viewer’ responses and reaction times were recorded. Results show that human observers, even in the absence of local shape or size cues, easily pick up on perspective cues, confirming recent demonstrations of high visual sensitivity to cues on whether another person is potentially approaching. We also found a consistent difference in how male and female observers respond to stimulus variations (figure gender or perspective cues) that cause variations in the perceived in-depth orientation of a point-light walker. Thus, the ‘figure gender effect’ is possibly caused by changes in the relative locations and motions of the dots that the perceptual system tends to interpret as perspective cues. Third, reaction time measures confirmed the existence of the facing bias and recent research showing faster detection of approaching than receding biological motion.     

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.     

Moving in a moving medium: new perspectives on flight

One of the defining features of the aerial environment is its variability; air is almost never still. This has profound consequences for flying animals, affecting their flight stability, speed selection, energy expenditure and choice of flight path. All these factors have important implications for the ecology of flying animals, and the ecosystems they interact with, as well as providing bio-inspiration for the development of unmanned aerial vehicles. In this introduction, we touch on the factors that drive the variability in airflows, the scales of variability and the degree to which given airflows may be predictable. We then summarize how papers in this volume advance our understanding of the sensory, biomechanical, physiological and behavioural responses of animals to air flows. Overall, this provides insight into how flying animals can be so successful in this most fickle of environments.This article is part of the themed issue ‘Moving in a moving medium: new perspectives on flight’.     

Egomotion estimation with optic flow and air velocity sensors

We develop a method that allows a flyer to estimate its own motion (egomotion), the wind velocity, ground slope, and flight height using only inputs from onboard optic flow and air velocity sensors. Our artificial algorithm demonstrates how it could be possible for flying insects to determine their absolute egomotion using their available sensors, namely their eyes and wind sensitive hairs and antennae. Although many behaviors can be performed by only knowing the direction of travel, behavioral experiments indicate that odor tracking insects are able to estimate the wind direction and control their absolute egomotion (i.e., groundspeed). The egomotion estimation method that we have developed, which we call the opto-aeronautic algorithm, is tested in a variety of wind and ground slope conditions using a video recorded flight of a moth tracking a pheromone plume. Over all test cases that we examined, the algorithm achieved a mean absolute error in height of 7% or less. Furthermore, our algorithm is suitable for the navigation of aerial vehicles in environments where signals from the Global Positioning System are unavailable.     

Small or far away? Size and distance perception in the praying mantis

Stereo or ‘3D’ vision is an important but costly process seen in several evolutionarily distinct lineages including primates, birds and insects. Many selective advantages could have led to the evolution of stereo vision, including range finding, camouflage breaking and estimation of object size. In this paper, we investigate the possibility that stereo vision enables praying mantises to estimate the size of prey by using a combination of disparity cues and angular size cues. We used a recently developed insect 3D cinema paradigm to present mantises with virtual prey having differing disparity and angular size cues. We predicted that if they were able to use these cues to gauge the absolute size of objects, we should see evidence for size constancy where they would strike preferentially at prey of a particular physical size, across a range of simulated distances. We found that mantises struck most often when disparity cues implied a prey distance of 2.5 cm; increasing the implied distance caused a significant reduction in the number of strikes. We, however, found no evidence for size constancy. There was a significant interaction effect of the simulated distance and angular size on the number of strikes made by the mantis but this was not in the direction predicted by size constancy. This indicates that mantises do not use their stereo vision to estimate object size. We conclude that other selective advantages, not size constancy, have driven the evolution of stereo vision in the praying mantis.This article is part of the themed issue ‘Vision in our three-dimensional world’.     

Nutritional biology: a neglected basic discipline of nutritional science

On the basis of a scientific-philosophical analysis, this paper tries to show that the approaches in current nutritional science—including its subdisciplines which focus on molecular aspects—are predominantly application-oriented. This becomes particularly evident through a number of conceptual problems characterized by the triad of ‘dearth of theoretical foundation,’ ‘particularist research questions,’ and ‘reductionist understanding of nutrition.’ The thesis presented here is that an interpretive framework based on nutritional biology is able to shed constructive light on the fundamental problems of nutritional science. In this context, the establishment of ‘nutritional biology’ as a basic discipline in research and education would be a first step toward recognizing the phenomenon of ‘nutrition’ as an oecic process as a special case of an organism–environment interaction. Modern nutritional science should be substantively grounded on ecological—and therefore systems biology as well as organismic—principles. The aim of nutritional biology, then, should be to develop near-universal ‘law statements’ in nutritional science—a task which presents a major challenge for the current science system.     

Fine-scale flight strategies of gulls in urban airflows indicate risk and reward in city living

Birds modulate their flight paths in relation to regional and global airflows in order to reduce their travel costs. Birds should also respond to fine-scale airflows, although the incidence and value of this remains largely unknown. We resolved the three-dimensional trajectories of gulls flying along a built-up coastline, and used computational fluid dynamic models to examine how gulls reacted to airflows around buildings. Birds systematically altered their flight trajectories with wind conditions to exploit updraughts over features as small as a row of low-rise buildings. This provides the first evidence that human activities can change patterns of space-use in flying birds by altering the profitability of the airscape. At finer scales still, gulls varied their position to select a narrow range of updraught values, rather than exploiting the strongest updraughts available, and their precise positions were consistent with a strategy to increase their velocity control in gusty conditions. Ultimately, strategies such as these could help unmanned aerial vehicles negotiate complex airflows. Overall, airflows around fine-scale features have profound implications for flight control and energy use, and consideration of this could lead to a paradigm-shift in the way ecologists view the urban environment.This article is part of the themed issue ‘Moving in a moving medium: new perspectives on flight’.     

Odour boosts visual object approach in flies

Multisensory integration is synergistic—input from one sensory modality might modulate the behavioural response to another. Work in flies has shown that a small visual object presented in the periphery elicits innate aversive steering responses in flight, likely representing an approaching threat. Object aversion is switched to approach when paired with a plume of food odour. The ‘open-loop’ design of prior work facilitated the observation of changing valence. How does odour influence visual object responses when an animal has naturally active control over its visual experience? In this study, we use closed-loop feedback conditions, in which a fly''s steering effort is coupled to the angular velocity of the visual stimulus, to confirm that flies steer toward or ‘fixate’ a long vertical stripe on the visual midline. They tend either to steer away from or ‘antifixate’ a small object or to disengage active visual control, which manifests as uncontrolled object ‘spinning’ within this experimental paradigm. Adding a plume of apple cider vinegar decreases the probability of both antifixation and spinning, while increasing the probability of frontal fixation for objects of any size, including a normally typically aversive small object.     

Sexual deception in a cannibalistic mating system? Testing the Femme Fatale hypothesis

Animal communication theory holds that in order to be evolutionarily stable, signals must be honest on average, but significant dishonesty (i.e. deception) by a subset of the population may also evolve. A typical praying mantid mating system involves active mate searching by males, which is guided by airborne sex pheromones in most species for which mate-searching cues have been studied. The Femme Fatale hypothesis suggests that female mantids may be selected to exploit conspecific males as prey if they benefit nutritionally from cannibalism. Such a benefit exists in the false garden mantid Pseudomantis albofimbriata—females use the resources gained from male consumption to significantly increase their body condition and reproductive output. This study aimed to examine the potential for chemical deception among the subset of females most likely to benefit from cannibalism (poorly fed females). Females were placed into one of four feeding treatments (‘Very Poor’, ‘Poor’, ‘Medium’ and ‘Good’), and males were given the opportunity to choose between visually obscured females in each of the treatments. Female body condition and fecundity varied linearly with food quantity; however, female attractiveness did not. That is, Very Poor females attracted significantly more males than any of the other female treatments, even though these females were in significantly poorer condition, less fecund (in this study) and more likely to cannibalise (in a previous study). In addition, there was a positive correlation between fecundity and attractiveness if Very Poor females were removed from the analysis, suggesting an inherently honest signalling system with a subset of dishonest individuals. This is the first empirical study to provide evidence of sexual deception via chemical cues, and the first to provide support for the Femme Fatale hypothesis.     

Flights of fear: a mechanical wing whistle sounds the alarm in a flocking bird

Animals often form groups to increase collective vigilance and allow early detection of predators, but this benefit of sociality relies on rapid transfer of information. Among birds, alarm calls are not present in all species, while other proposed mechanisms of information transfer are inefficient. We tested whether wing sounds can encode reliable information on danger. Individuals taking off in alarm fly more quickly or ascend more steeply, so may produce different sounds in alarmed than in routine flight, which then act as reliable cues of alarm, or honest ‘index’ signals in which a signal''s meaning is associated with its method of production. We show that crested pigeons, Ocyphaps lophotes, which have modified flight feathers, produce distinct wing ‘whistles’ in alarmed flight, and that individuals take off in alarm only after playback of alarmed whistles. Furthermore, amplitude-manipulated playbacks showed that response depends on whistle structure, such as tempo, not simply amplitude. We believe this is the first demonstration that flight noise can send information about alarm, and suggest that take-off noise could provide a cue of alarm in many flocking species, with feather modification evolving specifically to signal alarm in some. Similar reliable cues or index signals could occur in other animals.     

Social calls used by a leaf-roosting bat to signal location

Social calls in bats have many functions, including mate attraction and maintaining contact during flight. Research suggests that social calls may also be used to transfer information about roosts, but no studies have yet demonstrated that calls are used to actively attract conspecifics to roosting locations. We document the social calls used by Spix''s disc-winged bat (Thyroptera tricolor) to actively recruit group members to roosts. In acoustic trials, we recorded two sets of calls; one from flying individuals termed ‘inquiry calls’, and another from roosting bats termed ‘response calls’. Inquiry calls were emitted by flying bats immediately upon release, and quickly (i.e. 178 ms) elicited production of response calls from roosting individuals. Most flying bats entered the roost when roosting individuals responded, while few bats entered the roost in the absence of a response. We argue that information transfer concerning roost location may facilitate sociality in T. tricolor, given the ephemeral nature of roosting structures used by this species.     

Honeybee navigation: critically examining the role of the polarization compass

Although it is widely accepted that honeybees use the polarized-light pattern of the sky as a compass for navigation, there is little direct evidence that this information is actually sensed during flight. Here, we ask whether flying bees can obtain compass cues derived purely from polarized light, and communicate this information to their nest-mates through the ‘waggle dance’. Bees, from an observation hive with vertically oriented honeycombs, were trained to fly to a food source at the end of a tunnel, which provided overhead illumination that was polarized either parallel to the axis of the tunnel, or perpendicular to it. When the illumination was transversely polarized, bees danced in a predominantly vertical direction with waggles occurring equally frequently in the upward or the downward direction. They were thus using the polarized-light information to signal the two possible directions in which they could have flown in natural outdoor flight: either directly towards the sun, or directly away from it. When the illumination was axially polarized, the bees danced in a predominantly horizontal direction with waggles directed either to the left or the right, indicating that they could have flown in an azimuthal direction that was 90° to the right or to the left of the sun, respectively. When the first half of the tunnel provided axial illumination and the second half transverse illumination, bees danced along all of the four principal diagonal directions, which represent four equally likely locations of the food source based on the polarized-light information that they had acquired during their journey. We conclude that flying bees are capable of obtaining and signalling compass information that is derived purely from polarized light. Furthermore, they deal with the directional ambiguity that is inherent in polarized light by signalling all of the possible locations of the food source in their dances, thus maximizing the chances of recruitment to it.     

Ecological fitness, genomic islands and bacterial pathogenicity. A Darwinian view of the evolution of microbes

The compositions of bacterial genomes can be changed rapidly and dramatically through a variety of processes including horizontal gene transfer. This form of change is key to bacterial evolution, as it leads to ‘evolution in quantum leaps’. Horizontal gene transfer entails the incorporation of genetic elements transferred from another organism—perhaps in an earlier generation—directly into the genome, where they form ‘genomic islands’, i.e. blocks of DNA with signatures of mobile genetic elements. Genomic islands whose functions increase bacterial fitness, either directly or indirectly, have most likely been positively selected and can be termed ‘fitness islands’. Fitness islands can be divided into several subtypes: ‘ecological islands’ in environmental bacteria and ‘saprophytic islands’, ‘symbiosis islands’ or ‘pathogenicity islands’ (PAIs) in microorganisms that interact with living hosts. Here we discuss ways in which PAIs contribute to the pathogenic potency of bacteria, and the idea that genetic entities similar to genomic islands may also be present in the genomes of eukaryotes.