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Biology subjects

Muijres, F. T.

Publications and source records attributed to Muijres, F. T..

10 recordsLinked to original sources

Catch me if you can: wild Morpho butterflies trade speed for erraticity in escape flight

Predator-prey interactions shape the evolution of escape behavior in prey, including different combinations of evasive movements, that may enhance unpredictability in fleeing directions and trajectories. So-called protean motion can enhance survival of flying prey in the wild, but quantifying such behaviors under natural conditions remains challenging. Here we used stereoscopic high-speed videography to record the escape flight behavior of wild males of the butterfly species Morpho menelaus in the Amazonian rainforest, and reconstructed 3D flight trajectories using artificial-neural-network-based tracking. During the experiments, we used a lure to attract freely patrolling male butterflies and elicited escape flights by intercepting their trajectory with a looming insect net swing. We then compared the escape flight kinematics to the pre-attack patrolling behavior. Attacks first induced a rapid upward maneuvering, directly followed by an unpredictable horizontal turn. The following escape flight trajectories showed increased horizontal erraticity and greater intra-individual heading variability, as compared to the pre-attack flight. Surprisingly, the mean speed decreased in the escape phase, notably in the horizontal plane. A significant negative association between horizontal trajectory complexity and flight speed was detected, indicating a speed-erraticity trade-off. These results show that wild Morpho butterflies respond to attacks by combining a climbing maneuver with an unpredictable heading change, followed by a protean escape flight; this increased escape erraticity comes at the expense of reduced escape flight speed. Because these large and relatively slow-flying butterflies display bright iridescent blue coloration on their dorsal wing side, erraticity during flight might enhance the dynamic flash coloration, likely limiting accurate targeting by predators.

animal behavior and cognition↗

Attachment performance of cuttlefish (Sepia officinalis) suckers depends on the interaction between papillae and substrate topography

Cephalopods are versatile predators, with many species using suckers to capture prey. These suckers attach to substrates ranging from the stiff, rough exoskeletons of crustaceans to the soft, smooth tissues of other cephalopods. Despite generating higher suction pressures than octopuses, less attention has been given to the biomechanics of cuttlefish suckers. Cuttlefish suckers exhibit a stiff, rough papillated rim that acts as a seal. We hypothesise that these papillae have evolved to attach to rough substrates matching their rugosity to expel water at the contact interface. To test this hypothesis, we investigated the passive attachment performance of common cuttlefish (Sepia officinalis) suckers ex vivo on a variety of artificial substrates that differed in stiffness and roughness. We found that sucker attachment forces varied significantly with substrate roughness, with the highest forces occurring on roughnesses that coincided with the average sucker papillae height (root-mean-square [~] 6.84 {micro}m). Additionally, attachment forces were higher on stiffer substrates. We developed a mathematical model for predicting leakage across the sucker rim that qualitatively agrees with our experimental results. These findings indicate that the papillae may aid attachment performance, particularly to natural prey, and could inform the design and development of versatile bioinspired suction cups.

biophysics↗

The complex swarming dynamics of malaria mosquitoes emerges from simple minimally-interactive behavioral rules

Swarming is a widespread collective behavior in animals, often thought to emerge from complex interactions among individuals. Here, we show that mating swarms of malaria mosquitoes can emerge from simple behavioral rules with minimal interaction between individuals. We analyzed two published experimental datasets with three-dimensional flight tracks of Anopheles coluzzii mosquitoes swarming above a visual marker under simulated sunset conditions. We found that individuals alternate between straight flight and rapid turning maneuvers known as saccades. These saccades are triggered at the edge of the swarm, and their directions are biased along the sunset direction. This behavior was found consistent between both datasets and across swarm sizes, including solitary individuals, indicating that inter-individual interactions play a limited role within the studied size range. We developed a simple agent-based model incorporating three behavioral rules: attraction to the swarm center, alignment normal to the sunset horizon, both driven by environmental cues, and repulsion through short-range collision avoidance. The model reproduced key features of natural mosquito swarms, including looping flight paths, central density peaks, and directional alignment. Even in the absence of direct inter-individual interactions, the model generated realistic emergent swarm dynamics, demonstrating that social coordination is not required for swarm emergence. Our findings suggest that mosquito swarming is primarily guided by environmental perception rather than social interaction. This minimal framework offers a new perspective on insect swarming and may apply broadly to the many other insect species that form mating swarms. Understanding these rules could inform strategies for vector control and improve the effectiveness of interventions targeting mosquito reproduction. Author SummaryMosquito swarms are a familiar sight in many parts of the world, but the rules that govern their movement have remained mysterious. In our study, we investigated how male malaria mosquitoes behave in mating swarms. Using high-speed videography and computer simulations, we discovered that these swarms do not rely on complex social interactions. Instead, each mosquito follows a few simple rules based on visual cues from the environment, like the position of the sunset and a ground marker. These rules are enough to produce the looping flight patterns and dense swarms observed in nature. Surprisingly, even a single mosquito can perform this behavior in isolation. This minimal approach challenges the idea that swarming requires strong social coordination. It also opens new possibilities for controlling malaria mosquito populations by targeting the environmental factors that influence mating behavior. Since many insects rely on swarming to reproduce, our findings may help explain similar behaviors across species and inform broader strategies for insect population management.

animal behavior and cognition↗

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.

neuroscience↗

Spatial and temporal characteristics of laboratory-induced Anopheles coluzzii swarms: shape, structure and flight kinematics

Anopheles mosquitoes mate at sunset in aerial swarms. The development of mating-based methods for effective malaria vector control requires a good knowledge of the flight behaviour of Anopheles species in mating swarms. However, the process of how swarms are formed and maintained remains poorly understood. Here, we characterized the three-dimensional spatial and temporal flight kinematics of Anopheles coluzzii males swarming above a ground marker. We observed that the location, shape and volume of swarms were highly stereotypic, consistent over the swarming duration, regardless of the number of individuals in the swarm. The swarm had an elliptical cone shape, and we observed a differential spatial distribution of flight kinematics parameters within the swarm volume. Among these parameters, only swarm density varied with swarm size. Using a sensory system-informed model, we show that swarm location and shape can accurately be modelled based on visual perception of the marker. To control swarm height, swarming individuals maintain an optical angle of the marker ranging from 24{degrees} to 55{degrees}. Limiting the viewing angle deviation to 4.5% of the maximum value results in the observed elliptical cone swarm shape. We discuss the implications of these finding in mating success, speciation and for vector control.

animal behavior and cognition↗

Flight performance, activity and behaviour of breeding pied flycatchers in the wild, revealed with accelerometers and machine learning

Flight behaviours have been extensively studied from different angles such as their kinematics, aerodynamics and more general their migration pattern. Nevertheless, much is still unknown about the daily flight activity of birds, in terms of their performance, behaviour and the potential differences between males and females. The recent development of miniaturized accelerometers allows us a glimpse into the daily life of a songbird. Here, we tagged 26 pied flycatchers (Ficedula hypoleuca) with accelerometers and analysed using machine learning approaches their flight performance, activity and behaviour during their chick rearing period. We found that during two hours of foraging chick-rearing pied flycatchers were flying 13.7% of the time. Almost all flights (>99%) were short flights lasting less than 10s. Flight activity changed throughout the day and was highest in the morning and lowest in the early afternoon. Male pied flycatcher had lower wing loading than females, and peak flight accelerations were inversely correlated with wing loading. Despite this, we found no significant differences in flight activity and performance between sexes. This suggests that males possess a higher potential flight performance, which they not fully utilized during foraging flights. Our results thus suggest that male and female pied flycatcher invest equally in parental care, but that this comes at a reduced cost by the male, due to their higher flight performance potential.

animal behavior and cognition↗

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

To detect and escape from a looming threat, night-flying insects must rely on other senses than vision alone. Nocturnal mosquitoes have been described to escape looming objects in the dark, but how they achieve this is still unknown. Here, we show how night-active female malaria mosquitoes escape from a rapidly looming object that simulates the defensive action of a blood-host. By combining videography-based automatic tracking with numerical simulations of the attacker-induced airflow, we first show that night-flying mosquitoes use airflow-sensing to detect the danger and trigger their escape. Secondly, by combining these data with mechanistic movement modelling, we unravelled how mosquitoes control their escape manoeuvres: they actively steer away from the danger, and passively travel with the bow-wave produced by the attacker. Our results demonstrate that night-flying mosquitoes escaping from a looming object use the object-induced airflow both to detect the danger, and as fluid medium to move with for avoiding collision. This shows that the escape strategy of flying insects is more complex than previous visually-induces escape flight studies suggest. As mosquitoes are average-sized insects, a combined airflow-induced and visual-induced escape strategy is expected to be common amongst millions of flying insect species. Also, our research helps explain the high escape performance of mosquitoes from counterflow-based odour-baited mosquito traps. It can therefore provide new insights for the development of novel trapping techniques for integrative vector management.

zoology↗

Bumblebees actively 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 strategy, sensorimotor control, and landing performance of foraging bumblebees (Bombus terrestris). For this, we trained a hive of bumblebees to forage in a wind tunnel, and used high-speed stereoscopic videography to record 19,421 landing flight 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 duration from free flight was not increased by wind. We then tested how bumblebees adjusted their landing control to compensate for the adverse effects of sidewind on landing. This showed that the landing strategy in sidewind was similar to that in still air, but with important adaptations. In the highest windspeeds, more hover phases occurred than during landings in still air. The rising hover frequency did not increase landing duration because bumblebees flew faster in between hover phases. Hence, they negated the adverse effects of increased hovering in high windspeeds. Using control theory, we revealed how bumblebees integrate information from the wind-mediated mechanosensory modality with their vision-based sensorimotor control loop. The proposed multi-sensory flight control system may be commonly used by insects landing in windy conditions and it may inspire the development of landing control strategies onboard man-made flying systems. Summary statementBumblebees foraging in strong sidewinds can still land precisely on artificial flowers, allowing them to be efficient and robust pollinators in these adverse environmental conditions.

animal behavior and cognition↗

Gliding in the Amazonian canopy: adaptive evolution of flight in Morpho butterflies

The diversity of flying animals suggests that countless combinations of morphologies and behaviors have evolved with specific lifestyles, thereby exploiting diverse aerodynamic mechanisms. Elucidating how morphology, flight behavior and aerodynamic properties together diversify with contrasted ecologies remains however seldom accomplished. Here, we studied the adaptive co-divergence 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 modelling. 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 strikingly distinct combinations of flight behavior, wing shape and aerodynamic mechanisms, highlighting the multiple pathways of adaptive evolution. One Sentence SummaryBy combining high-speed videography, geometric morphometrics and computational aerodynamic modelling, our study of wild Amazonian Morpho butterflies reveals a strong contrast between the efficient gliding flight of canopy species and the powerful flapping flight of understory species, pointing at a combined adaptive divergence of wing shape and flight behavior among sympatric species flying in different forest strata.

evolutionary biology↗

Reorientation and propulsion in fast-starting zebrafish larvae: an inverse dynamics analysis

Most fish species use fast starts to escape from predators. Zebrafish larvae perform effective fast starts immediately after hatching. They use a C-start, where the body curls into a C-shape, and then unfolds to accelerate. These escape responses need to fulfil a number of functional demands, under the constraints of the fluid environment and the larvas body shape. Primarily, the larvae need to generate sufficient escape speed in a wide range of possible directions, in a short-enough time. In this study, we examined how the larvae meet these demands. We filmed fast starts of zebrafish larvae with a unique five-camera setup with high spatiotemporal resolution. From these videos, we reconstructed the three-dimensional swimming motion with an automated method and from these data calculated resultant hydrodynamic forces and, for the first time, 3D torques. We show that zebrafish larvae reorient mostly in the first stage of the start by producing a strong yaw torque, often without using the pectoral fins. This reorientation is expressed as the body angle, a measure that represents the rotation of the complete body, rather than the commonly used head angle. The fish accelerates its centre of mass mostly in stage 2 by generating a considerable force peak while the fish \"unfolds\". The escape direction of the fish correlates strongly with the amount of body curvature in stage 1, while the escape speed correlates strongly with the duration of the start. This may allow the fish to independently control the direction and speed of the escape.\n\nSummary statementFish larvae can independently adjust the direction and speed of their fast start escape response, a manoeuvre crucial for survival.

biophysics↗