Wold, E. | bioRxiv Science

bioRxiv2024

Moth resonant mechanics are tuned to wingbeat frequency and energetic demands.

An insects 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 insects 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.

physiology↗

bioRxiv2022

Structural damping renders the insect exoskeleton mechanically insensitive to non-sinusoidal deformations

Muscles act through elastic and dissipative elements to mediate movement, but these elements can introduce dissipation and filtering which are important for energetics and control. The high power requirements of flapping flight can be reduced by the insects exoskeleton, which acts as a structurally damped spring under purely sinusoidal deformation. However, this purely sinusoidal dynamic regime does not encompass the asymmetric wing strokes of many insects or non-periodic deformations induced by external perturbations. As such, it remains unknown whether a structural damping model applies broadly and what implications it has for control. We used a vibration testing system to measure the mechanical properties of isolated Manduca sexta thoraces under symmetric, asymmetric, and band-limited white noise deformations. We measured a thoracic stiffness of 2980 Nm-1 at 25 Hz and physiological peak-to-peak amplitude of 0.92 mm. Power savings and dissipation were indistinguishable between symmetric and asymmetric conditions, demonstrating that no additional energy is required to deform the thorax non-sinusoidally. Under white noise conditions, stiffness and damping were invariant with frequency, which is consistent with a structural damping model and suggests the thorax has no frequency-dependent filtering properties. A simple flat frequency response function fits our measured frequency response. This work demonstrates the potential of structurally damped materials to simplify motor control by eliminating any velocity-dependent filtering that viscoelastic elements usually impose between muscle and appendage.

biophysics↗