Multisensory integration in Anopheles mosquito swarms: The role of visual and acoustic information in mate tracking and collision avoidance.

Male mosquitoes form aerial aggregations, known as swarms, to attract females and maximize their chances of finding a mate. Within these swarms, individuals must be able to recognize potential mates and navigate the dynamic social environment to successfully intercept a mating partner. Prior research has almost exclusively focused on the role of acoustic cues in mediating the ability of male mosquitoes to recognize and pursue flying females. However, the role of other sensory modalities in this behavior has not been explored. Moreover, how males avoid collisions with one another in the dense swarm while pursuing females remains poorly understood. In this study, we combined free-flight and tethered flight simulator experiments to demonstrate that swarming Anopheles coluzzii mosquitoes integrate visual and acoustic information to track conspecifics and avoid collisions. Our tethered experiments revealed that acoustic stimuli gated mosquito steering responses to visual objects simulating nearby mosquitoes, especially in males that exhibited attraction to visual objects in the presence of female flight tones. Additionally, we observed that visual cues alone could trigger changes in wingbeat amplitude and frequency of mosquitoes. These findings were corroborated by our free-flight experiments, which revealed that mosquitoes modulate their flight responses to nearby conspecifics in a similar manner to tethered animals, allowing for collision avoidance within swarms. Together, these results demonstrate that both males and females integrate multiple sensory inputs to mediate swarming behavior, and for males, the change in flight kinematics in response to multimodal cues allows them to simultaneously track females while avoiding collisions.

Bumblebees compensate for the adverse effects of sidewind during visually guided landings.

Flying animals often encounter winds during visually guided landings. However, how winds affect their flight control strategy during landing is unknown. Here, we investigated how sidewind affects the landing performance and sensorimotor control of foraging bumblebees (Bombus terrestris). We trained bumblebees to forage in a wind tunnel, and used high-speed stereoscopic videography to record 19,421 landing maneuvers in six sidewind speeds (0 to 3.4 m s-1), which correspond to winds encountered in nature. Bumblebees landed less often in higher windspeeds, but the landing durations from free flight were not increased by wind. By testing how bumblebees adjusted their landing control to compensate for adverse effects of sidewind on landing, we showed that the landing strategy in sidewind resembled that in still air, but with important adaptations. Bumblebees landing in a sidewind tended to drift downwind, which they controlled for by performing more hover maneuvers. Surprisingly, the increased hover prevalence did not increase the duration of free-flight landing maneuvers, as these bumblebees flew faster towards the landing platform outside the hover phases. Hence, by alternating these two flight modes along their flight path, free-flying bumblebees negated the adverse effects of high windspeeds on landing duration. Using control theory, we hypothesize that bumblebees achieve this by integrating a combination of direct aerodynamic feedback and a wind-mediated mechanosensory feedback control, with their vision-based sensorimotor control loop. The revealed landing strategy may be commonly used by insects landing in windy conditions, and may inspire the development of landing control strategies onboard autonomously flying robots.

Mosquitoes escape looming threats by actively flying with the bow wave induced by the attacker.

To detect and escape looming threats, night-flying insects must rely on other senses than vision alone. Nocturnal mosquitoes can evade looming objects in the dark, but how they achieve this is still unknown. Here, we show how night-active female malaria mosquitoes escape from rapidly looming objects that simulate defensive actions of blood-hosts. First, we quantified the escape performance of flying mosquitoes from an event-triggered mechanical swatter, showing that mosquitoes use swatter-induced airflow to increase their escape success. Secondly, we used high-speed videography and deep-learning-based tracking to analyze escape flights in detail, showing that mosquitoes use banked turns to evade the threat. By combining escape kinematics data with numerical simulations of attacker-induced airflow and a mechanistic movement model, we unraveled how mosquitoes control these banked evasive maneuvers: they actively steer away from the danger, and then passively travel with the bow wave produced by the attacker. Our results demonstrate that night-flying mosquitoes can detect looming objects when visual cues are minimal, suggesting that they use attacker-induced airflow both to detect the danger and as a fluid medium to move with away from the threat. This shows that escape strategies of flying insects are more complex than previous visually induced escape flight studies suggest. As most insects are of similar or smaller sizes than mosquitoes, comparable escape strategies are expected among millions of flying insect species. The here-observed escape maneuvers are distinct from those of mosquitoes escaping from odor-baited traps, thus providing new insights for the development of novel trapping techniques for integrative vector management.

Edge computing in wildlife behavior and ecology.

Modern sensor technologies increasingly enrich studies in wildlife behavior and ecology. However, constraints on weight, connectivity, energy and memory availability limit their implementation. With the advent of edge computing, there is increasing potential to mitigate these constraints, and drive major advancements in wildlife studies.

Visual guidance of honeybees approaching a vertical landing surface.

Landing is a critical phase for flying animals, whereby many rely on visual cues to perform controlled touchdown. Foraging honeybees rely on regular landings on flowers to collect food crucial for colony survival and reproduction. Here, we explored how honeybees utilize optical expansion cues to regulate approach flight speed when landing on vertical surfaces. Three sensory-motor control models have been proposed for landings of natural flyers. Landing honeybees maintain a constant optical expansion rate set-point, resulting in a gradual decrease in approach velocity and gentile touchdown. Bumblebees exhibit a similar strategy, but they regularly switch to a new constant optical expansion rate set-point. In contrast, landing birds fly at a constant time to contact to achieve faster landings. Here, we re-examined the landing strategy of honeybees by fitting the three models to individual approach flights of honeybees landing on platforms with varying optical expansion cues. Surprisingly, the landing model identified in bumblebees proved to be the most suitable for these honeybees. This reveals that honeybees adjust their optical expansion rate in a stepwise manner. Bees flying at low optical expansion rates tend to increase their set-point stepwise, while those flying at high optical expansion rates tend to decrease it stepwise. This modular landing control system enables honeybees to land rapidly and reliably under a wide range of initial flight conditions and visual landing platform patterns. The remarkable similarity between the landing strategies of honeybees and bumblebees suggests that this may also be prevalent among other flying insects. Furthermore, these findings hold promising potential for bioinspired guidance systems in flying robots.

Designing a Generic Videography Experiment for Studying Mosquito Behavior.

In this protocol, we describe the basic design considerations and general method to set up a videography system to study mosquito behavior. A basic videography system to study mosquito behavior requires one or more cameras with an optical lens, camera lighting, a calibration setup, and a system to record the video data or otherwise control the camera. Here, we define two types of systems: (1) a real-time videography-based tracking system for determining the position of multiple moving (flying) mosquitoes, and (2) a high-fidelity videography system that can track the detailed movements of body, wings, and legs of a single mosquito at high spatial and temporal resolutions. These high-fidelity trackers are divided into single-camera systems for studying two-dimensional (2D) movements, and multicamera systems that can reconstruct three-dimensional (3D) movements of the mosquito.

Using Videography to Study the Biomechanics and Behavior of Freely Moving Mosquitoes.

Female mosquitoes of most species require a blood meal for egg development. When biting a human host to collect this blood meal, they can spread dangerous diseases such as malaria, yellow fever, or dengue. Researchers use videography to study many aspects of mosquito behavior, including in-flight host-seeking, takeoff, and landing behaviors, as well as probing and blood feeding, and more. Here, we introduce protocols on how to use videography to capture and analyze mosquito movements at high spatial and temporal resolution, in two and three dimensions.

Quantifying and Analyzing Mosquito Movement from Video Tracking Results.

After tracking the kinematics of a moving mosquito from video, one needs to convert the tracking output into the kinematics data needed to answer the research question. Here, we provide general guidelines for how to do this by discussing how to quantify body position and orientation in the world reference frame and wing and leg orientation in the mosquito body reference frame. These guidelines should be adapted based on the goal of your research. To answer your research question, the resulting kinematics data must then be further analyzed. Because the nature of this analysis depends strongly on your specific research question, we refer to literature for designing these postprocessing routines.

Real-Time Tracking of Multiple Moving Mosquitoes.

Tracking mosquitoes in real time, as opposed to recording video files and performing the tracking step later, is useful for two reasons. The first is efficiency. Real-time tracking requires less storage because video images do not need to be saved and followed by a tracking step. The second is that tracking data can be used to interact with the animal in some way, such as triggering the approach of a looming object. In this protocol, we discuss the use of Braid, free software for performing real-time, multicamera, multianimal tracking. We describe a setup with four cameras capable of tracking the three-dimensional (3D) position of mosquitoes at 100 frames per second in a volume of 30 cm × 30 cm × 60 cm with millimeter accuracy. The specific hardware configuration is flexible and can be substituted using different or additional components to adjust the tracking parameters as needed.

Tracking the Body, Wing, and Leg Kinematics of Moving Mosquitoes.

In this protocol, we discuss general techniques for tracking the three-dimensional (3D) locations of the mosquito body, wings, legs, or other features of interest using videos. Tracking data must be acquired to produce detailed kinematics of moving mosquitoes. The software of focus for this protocol, DLTdv, was chosen for its widespread use and excellent support and because it is open-source. In addition, DLTdv allows both manual and automatic tracking. The automatic tracking can be done using a classic machine vision or machine-learning algorithm. The software supports both single-camera analysis and multicamera systems and can take advantage of sophisticated calibration algorithms, both for intrinsic lens distortion correction and for 3D DLT-based reconstruction. For this protocol, we assume all kinematic data is acquired post hoc through video analysis.

Bumblebees land rapidly by intermittently accelerating and decelerating toward the surface during visually guided landings.

Many flying animals parse visual information to control their landing, whereby they can decelerate smoothly by flying at a constant radial optic expansion rate. Here, we studied how bumblebees (Bombus terrestris) use optic expansion information to control their landing, by analyzing 10,005 landing maneuvers on vertical platforms with various optic information, and at three dim light conditions. We showed that bumblebees both decelerate and accelerate during these landings. Bumblebees decelerate by flying at a constant optic expansion rate, but they mostly accelerate toward the surface each time they switched to a new, often higher, optic expansion rate set-point. These transient acceleration phases allow bumblebees to increase their approach speed, and thereby land rapidly and robustly, even in dim twilight conditions. This helps explain why bumblebees are such robust foragers in challenging environmental conditions. The here-proposed sensorimotor landing control system can serve as bio-inspiration for landing control in unmanned aerial vehicles.

Flying Into the Wind: Insects and Bio-Inspired Micro-Air-Vehicles With a Wing-Stroke Dihedral Steer Passively Into Wind-Gusts.

Natural fliers utilize passive and active flight control strategies to cope with windy conditions. This capability makes them incredibly agile and resistant to wind gusts. Here, we study how insects achieve this, by combining Computational Fluid Dynamics (CFD) analyses of flying fruit flies with freely-flying robotic experiments. The CFD analysis shows that flying flies are partly passively stable in side-wind conditions due to their dorsal-ventral wing-beat asymmetry defined as wing-stroke dihedral. Our robotic experiments confirm that this mechanism also stabilizes free-moving flapping robots with similar asymmetric dihedral wing-beats. This shows that both animals and robots with asymmetric wing-beats are dynamically stable in sideways wind gusts. Based on these results, we developed an improved model for the aerodynamic yaw and roll torques caused by the coupling between lateral motion and the stroke dihedral. The yaw coupling passively steers an asymmetric flapping flyer into the direction of a sideways wind gust; in contrast, roll torques are only stabilizing at high air gust velocities, due to non-linear coupling effects. The combined CFD simulations, robot experiments, and stability modeling help explain why the majority of flying insects exhibit wing-beats with positive stroke dihedral and can be used to develop more stable and robust flapping-wing Micro-Air-Vehicles.

Diurnal and nocturnal mosquitoes escape looming threats using distinct flight strategies.

Flying insects have evolved the ability to evade looming objects, such as predators and swatting hands. This is particularly relevant for blood-feeding insects, such as mosquitoes that routinely need to evade the defensive actions of their blood hosts. To minimize the chance of being swatted, a mosquito can use two distinct strategies-continuously exhibiting an unpredictable flight path or maximizing its escape maneuverability. We studied how baseline flight unpredictability and escape maneuverability affect the escape performance of day-active and night-active mosquitoes (Aedes aegypti and Anopheles coluzzii, respectively). We used a multi-camera high-speed videography system to track how freely flying mosquitoes respond to an event-triggered rapidly approaching mechanical swatter, in four different light conditions ranging from pitch darkness to overcast daylight. Results show that both species exhibit enhanced escape performance in their natural blood-feeding light condition (daylight for Aedes and dark for Anopheles). To achieve this, they show strikingly different behaviors. The enhanced escape performance of Anopheles at night is explained by their increased baseline unpredictable erratic flight behavior, whereas the increased escape performance of Aedes in overcast daylight is due to their enhanced escape maneuvers. This shows that both day and night-active mosquitoes modify their flight behavior in response to light intensity such that their escape performance is maximum in their natural blood-feeding light conditions, when these defensive actions by their blood hosts occur most. Because Aedes and Anopheles mosquitoes are major vectors of several deadly human diseases, this knowledge can be used to optimize vector control methods for these specific species.

Great tits do not compensate over time for a radio-tag-induced reduction in escape-flight performance.

The use of biologging and tracking devices is widespread in avian behavioral and ecological studies. Carrying these devices rarely has major behavioral or fitness effects in the wild, yet it may still impact animals in more subtle ways, such as during high power demanding escape maneuvers. Here, we tested whether or not great tits (Parus major) carrying a backpack radio-tag changed their body mass or flight behavior over time to compensate for the detrimental effect of carrying a tag. We tested 18 great tits, randomly assigned to a control (untagged) or one of two different types of a radio-tag as used in previous studies in the wild (0.9 g or 1.2 g; ~5% or ~6-7% of body mass, respectively), and determined their upward escape-flight performance 1, 7, 14, and 28 days after tagging. In between experiments, birds were housed in large free-flight aviaries. For each escape-flight, we used high-speed 3D videography to determine flight paths, escape-flight speed, wingbeat frequency, and actuator disk loading (ratio between the bird weight and aerodynamic thrust production capacity). Tagged birds flew upward with lower escape-flight speeds, caused by an increased actuator disk loading. During the 28-day period, all groups slightly increased their body mass and their in-flight wingbeat frequency. In addition, during this period, all groups of birds increased their escape-flight speed, but tagged birds did so at a lower rate than untagged birds. This suggests that birds may increase their escape-flight performance through skill learning; however, tagged birds still remained slower than controls. Our findings suggest that tagging a songbird can have a prolonged effect on the performance of rapid flight maneuvers. Given the absence of tag effects on reproduction and survival in most songbird radio-tagging studies, tagged birds in the wild might adjust their risk-taking behavior to avoid performing rapid flight maneuvers.

Adaptive evolution of flight in Morpho butterflies.

The diversity of flying animals suggests that countless combinations of flight morphologies and behaviors have evolved with specific lifestyles, thereby exploiting diverse aerodynamic mechanisms. How morphology, flight behavior, and aerodynamic properties together diversify with contrasting ecology remains to be elucidated. We studied the adaptive codivergence in wing shape, flight behavior, and aerodynamic efficiency among Morpho butterflies living in different forest strata by combining high-speed videography in the field with morphometric analyses and aerodynamic modeling. By comparing canopy and understory species, we show that adaptation to an open canopy environment resulted in increased glide efficiency. Moreover, this enhanced glide efficiency was achieved by different canopy species through distinct combinations of flight behavior, wing shape, and aerodynamic mechanisms, highlighting the multiple pathways of adaptive evolution.

Bumblebees land rapidly and robustly using a sophisticated modular flight control strategy.

When approaching a landing surface, many flying animals use visual feedback to control their landing. Here, we studied how foraging bumblebees (Bombus terrestris) use radial optic expansion cues to control in-flight decelerations during landing. By analyzing the flight dynamics of 4,672 landing maneuvers, we showed that landing bumblebees exhibit a series of deceleration bouts, unlike landing honeybees that continuously decelerate. During each bout, the bumblebee keeps its relative rate of optical expansion constant, and from one bout to the next, the bumblebee tends to shift to a higher, constant relative rate of expansion. This modular landing strategy is relatively fast compared to the strategy described for honeybees and results in approach dynamics that is strikingly similar to that of pigeons and hummingbirds. The here discovered modular landing strategy of bumblebees helps explaining why these important pollinators in nature and horticulture can forage effectively in challenging conditions; moreover, it has potential for bio-inspired landing strategies in flying robots.

Varroa destructor infestation impairs the improvement of landing performance in foraging honeybees.

The parasitic mite Varroa destructor is an important contributor to the high losses of western honeybees. Forager bees from Varroa-infested colonies show reduced homing and flight capacity; it is not known whether flight manoeuvrability and related learning capability are also affected. Here, we test how honeybees from Varroa-infested and control colonies fly in an environment that is unfamiliar at the beginning of each experimental day. Using stereoscopic high-speed videography, we analysed 555 landing manoeuvres recorded during 12 days of approximately 5 h in length. From this, we quantified landing success as percentage of successful landings, and assessed how this changed over time. We found that the forager workforce of Varroa-infested colonies did not improve their landing success over time, while for control bees landing success improved with approximately 10% each hour. Analysis of the landing trajectories showed that control bees improved landing success by increasing the ratio between in-flight aerodynamic braking and braking at impact on the landing platform; bees from Varroa-infested colonies did not increase this ratio over time. The Varroa-induced detriment to this landing skill-learning capability might limit forager bees from Varroa-infested colonies to adapt to new or challenging conditions; this might consequently contribute to Varroa-induced mortality of honeybee colonies.

Lure, retain, and catch malaria mosquitoes. How heat and humidity improve odour-baited trap performance.

BACKGROUND: When seeking a human for a blood meal, mosquitoes use several cues to detect and find their hosts. From this knowledge, counter-flow odour-baited traps have been developed that use a combination of CO2, human-mimicking odour, visual cues and circulating airflow to attract and capture mosquitoes. Initially developed for monitoring, these traps are now also being considered as promising vector control tools. The traps are attractive to host-seeking mosquitoes, but their capture efficiency is low. It has been hypothesized that the lack of short-range host cues, such as heat and increased local humidity, often prevent mosquitoes from getting close enough to get caught; this lack might even trigger avoidance manoeuvres near the capture region. METHODS: This study investigated how close-range host cues affect the flight behaviour of Anopheles female malaria mosquitoes around odour-baited traps, and how this affects trap capture performance. For this, a novel counter-flow odour-baited trap was developed, the M-Tego. In addition to the usual CO2 and odour-blend, this trap can provide the short-range host cues, heat and humidity. Systematically adding or removing these two cues tested how this affected the trap capture percentages and flight behaviour. First, capture percentages of the M-Tego with and without short-range host cues to the BG-Suna trap were compared, in both laboratory and semi-field testing. Then, machine-vision techniques were used to track the three-dimensional flight movements of mosquitoes around the M-Tego. RESULTS: With heat and humidity present, the M-Tego captured significantly more mosquitoes as capture percentages almost doubled. Comparing the flight behaviour around the M-Tego with variable close-range host cues showed that when these cues were present, flying mosquitoes were more attracted to the trap and spent more time there. In addition, the M-Tego was found to have a better capture mechanism than the BG-Suna, most likely because it does not elicit previously observed upward avoiding manoeuvres. CONCLUSIONS: Results suggest that adding heat and humidity to an odour-baited trap lures more mosquitoes close to the trap and retains them there longer, resulting in higher capture performance. These findings support the development of control tools for fighting mosquito-borne diseases such as malaria.

Experimental-numerical method for calculating bending moments in swimming fish shows that fish larvae control undulatory swimming with simple actuation.

Most fish swim with body undulations that result from fluid-structure interactions between the fish's internal tissues and the surrounding water. Gaining insight into these complex fluid-structure interactions is essential to understand how fish swim. To this end, we developed a dedicated experimental-numerical inverse dynamics approach to calculate the lateral bending moment distributions for a large-amplitude undulatory swimmer that moves freely in three-dimensional space. We combined automated motion tracking from multiple synchronised high-speed video sequences, computation of fluid dynamic stresses on the swimmer's body from computational fluid dynamics, and bending moment calculations using these stresses as input for a novel beam model of the body. The bending moment, which represent the system's net actuation, varies over time and along the fish's central axis due to muscle actions, passive tissues, inertia, and fluid dynamics. Our three-dimensional analysis of 113 swimming events of zebrafish larvae ranging in age from 3 to 12 days after fertilisation shows that these bending moment patterns are not only relatively simple but also strikingly similar throughout early development and from fast starts to periodic swimming. This suggests that fish larvae may produce and adjust swimming movements relatively simply, yet effectively, while restructuring their neuromuscular control system throughout their rapid development.

Bumblebees land remarkably well in red-blue greenhouse LED light conditions.

Red-blue emitting LEDs have recently been introduced in greenhouses to optimise plant growth. However, this spectrum may negatively affect the performance of bumblebees used for pollination, because the visual system of bumblebees is more sensitive to green light than to red-blue light. We used high-speed stereoscopic videography to three-dimensionally track and compare landing manoeuvres of Bombus terrestris bumblebees in red-blue light and in regular, broad-spectrum white light. In both conditions, the landing approaches were interspersed by one or several hover phases, followed by leg extension and touchdown. The time between leg extension and touchdown was 25% (0.05 s) longer in red-blue light than in white light, caused by a more tortuous flight path in red-blue light. However, the total landing duration, specified as the time between the first hover phase and touchdown, did not differ between the light conditions. This suggests that the negative effects of red-blue light on the landing manoeuvre are confined to the final phase of the landing.This article has an associated First Person interview with the first author of the paper.