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Tiny flying insects, such as Drosophila melanogaster , fly by flapping their wings at frequencies faster than their brains are able to process. To do so, they rely on self-oscillation: dynamic instability, leading to emergent oscillation, arising from muscle stretch-activation. Many questions concerning this vital natural instability remain open. Does flight motor self-oscillation necessarily lead to resonance—a state optimal in efficiency and/or performance? If so, what state? And is self-oscillation even guaranteed in a motor driven by stretch-activated muscle, or are there limiting conditions? In this work, we use data-driven models of wingbeat and muscle behaviour to answer these questions. Developing and leveraging novel analysis techniques, including symbolic computation, we establish a fundamental condition for motor self-oscillation common to a wide range of motor models. Remarkably, D. melanogaster flight apparently defies this condition: a paradox of motor operation. We explore potential resolutions to this paradox, and, within its confines, establish that the D. melanogaster flight motor is probably not resonant with respect to exoskeletal elasticity: instead, the muscular elasticity plays a dominant role. Contrary to common supposition, the stiffness of stretch-activated muscle is an obstacle to, rather than an enabler of, the operation of the D. melanogaster flight motor.
Tiny flying insects, such as Drosophila melanogaster , fly by flapping their wings at frequencies faster than their brains are able to process. To do so, they rely on self-oscillation: dynamic instability, leading to emergent oscillation, arising from muscle stretch-activation. Many questions concerning this vital natural instability remain open. Does flight motor self-oscillation necessarily lead to resonance—a state optimal in efficiency and/or performance? If so, what state? And is self-oscillation even guaranteed in a motor driven by stretch-activated muscle, or are there limiting conditions? In this work, we use data-driven models of wingbeat and muscle behaviour to answer these questions. Developing and leveraging novel analysis techniques, including symbolic computation, we establish a fundamental condition for motor self-oscillation common to a wide range of motor models. Remarkably, D. melanogaster flight apparently defies this condition: a paradox of motor operation. We explore potential resolutions to this paradox, and, within its confines, establish that the D. melanogaster flight motor is probably not resonant with respect to exoskeletal elasticity: instead, the muscular elasticity plays a dominant role. Contrary to common supposition, the stiffness of stretch-activated muscle is an obstacle to, rather than an enabler of, the operation of the D. melanogaster flight motor.
In many insect species, the thoracic exoskeletal structure plays a crucial role in enabling flight. In the dipteran indirect flight mechanism, thoracic cuticle acts as a transmission link between the flight muscles and the wings, and is thought to act as an elastic modulator: improving flight motor efficiency thorough linear or nonlinear resonance. But peering closely into the drivetrain of tiny insects is experimentally difficult, and the nature of this elastic modulation is unclear. Here, we present a new inverse-problem methodology to surmount this difficulty. In a data synthesis process, we integrate literature-reported rigid-wing aerodynamic and musculoskeletal data into a planar oscillator model for the fruit fly Drosophila melanogaster, and use this integrated data to identify several surprising properties of the fly's thorax. We find that fruit flies likely have an energetic need for motor resonance: absolute power savings due to motor elasticity range from 0-30% across literature-reported datasets, averaging 16%. However, in all cases, the intrinsic high effective stiffness of the active asynchronous flight muscles accounts for all elastic energy storage required by the wingbeat. The D. melanogaster flight motor should be considered as a system in which the wings are resonant with the elastic effects of the motor’s asynchronous musculature, and not with the elastic effects of the thoracic exoskeleton. We discover also that D. melanogaster wingbeat kinematics show subtle adaptions that ensure that wingbeat load requirements match muscular forcing. Together, these newly-identified properties suggest a novel conceptual model of the fruit fly's flight motor: a structure that is resonant due to muscular elasticity, and is thereby intensely concerned with ensuring that the primary flight muscles are operating efficiently. Our inverse-problem methodology sheds new light on the complex behaviour of these tiny flight motors, and provides avenues for further studies in a range of other insect species.
An insect’s wingbeat frequency is a critical determinant of its flight performance and varies by multiple orders of magnitude across Insecta. Despite potential energetic and kine-matic benefits for an insect that matches its wingbeat frequency to its resonant frequency, recent work has shown that moths may operate off of their resonant peak. We hypothesized that across species, wingbeat frequency scales with resonance frequency to maintain favorable energetics, but with an offset in species that use frequency modulation as a means of flight control. The moth superfamily Bombycoidea is ideal for testing this hypothesis because their wingbeat frequencies vary across species by an order of magnitude, despite similar morphology and actuation. We used materials testing, high-speed videography, and a “spring-wing” model of resonant aerodynamics to determine how components of an insect’s flight apparatus (thoracic properties, wing inertia, muscle strain, and aerodynamics) vary with wingbeat frequency. We find that the resonant frequency of a moth correlates with wingbeat frequency, but resonance curve shape (described by the Weis-Fogh number) and peak location vary within the clade in a way that corresponds to frequency-dependent biomechanical demands. Our results demonstrate that a suite of adaptations in muscle, exoskeleton and wing drive variation in resonant mechanics, reflecting potential constraints on matching wingbeat and resonant frequencies.
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