Biology subjects

Gravish, N.

Publications and source records attributed to Gravish, N..

9 recordsLinked to original sources

bioRxiv2026

The physiological dynamic clamp allows insect flight muscle to transition between two actuation modes in virtual reality

In most muscles, contraction is initiated by neural activation. Some groups of insects break this rule, flapping at frequencies far exceeding the neural drive to their flight muscles. These insects muscles (termed asynchronous) produce force in response to stretch, enabling flight at faster frequencies than would be possible through the slow calcium-dependent processes associated with neural activation. The first flapping insects lacked stretch-activated physiology, which then evolved on top of neural activation dynamics before likely being reduced again in some groups including moths. Stretch and neural activation can co-exist, but it remains unclear if stretch-activation alone is sufficient to generate asynchronous flapping in insect flight muscle. Building on prior closed-loop muscle physiology platforms, we develop a new way to perform a gain-of-function muscle physiology experiment called the physiological dynamic clamp. Inspired by dynamic clamp experiments in neuroscience, we couple isolated intact flight muscle from a hawkmoth, Manduca sexta, to simulated stretch-activation in virtual reality. Tuning virtual reality parameters allows us to manipulate the degree of stretch-activation in silico while retaining all other physiological properties of the muscle. With artificially enhanced stretch activation, we find that hawkmoth muscle can support stretch-activated work at typical wingbeat frequencies. When simultaneously stimulated at wingbeat frequency, interference between stretch and neural activation results in variable work production. However, this interference disappears when the two activation timescales are close to each other resulting in entrainment to the neural drive. Matching time scales suggests an evolutionary path for smoothly transitioning to stretch-activated, asynchronous flight and back again.

physiology↗

bioRxiv2026

Quasi-static force requirements are not sufficient to explain arolium engagement in climbing Argentine ants

Argentine ants (Linepithema humile) utilize adhesive pads (arolia) to climb smooth surfaces. Previous research found that ants can adjust their individual arolium engagement according to their locomotion mode. However, it remains unclear how they distribute arolium engagement across multiple limbs to climb effectively, and how arolium engagement varies within a climbing step. As the arolium is a well-known adhesive organ, we hypothesized that engagement across different legs is distributed according to the normal forces required for balancing the body during climbing. To test this, we measured Argentine ants arolium engagement on a vertical glass surface using a Frustrated Total Internal Reflection (FTIR) sensor and compared it to the required normal forces from a quasi-static model. Contrary to the required normal force, the measured arolium engagement was asymmetric between upward and downward climbing, and changed over time. Our results indicated that the quasi-static force requirements are not sufficient to explain arolium engagement in climbing Argentine ants, and suggested that other factors, such as body dynamics, ants anatomy and behavioral preferences, should be included.

zoology↗

bioRxiv2025

Supra-resonant wingbeats in insects

Powering small-scale flapping flight is challenging, yet insects sustain exceptionally fast wingbeats with ease. Since insects act as tiny biomechanical resonators, tuning their wingbeat frequency to the resonant frequency of their springy thorax and wings could make them more efficient fliers. But operating at resonance poses control problems and potentially constrains wingbeat frequencies within and across species. Resonance may be particularly limiting for the many orders of insects that power flight with specialized muscles that activate in response to mechanical stretch. Here, we test whether insects operate at their resonant frequency. First, we extensively characterize bumblebees and find that they surprisingly flap well above their resonant frequency via interactions between stretch-activation and mechanical resonance. Modeling and robophysical experiments then show that resonance is actually a lower bound for rapid wingbeats in most insects because muscles only pull, not push. Supra-resonance emerges as a general principle of high-frequency flight across five orders of insects from moths to flies.

zoology↗

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↗

bioRxiv2020

Hawkmoths use wingstroke-to-wingstroke frequency modulation for aerial recovery to vortex ring perturbations

Centimeter-scale fliers that combine wings with springy elements must contend with the high power requirements and mechanical constraints of flapping wing flight. Insects utilize elastic energy exchange to reduce the inertial costs of flapping wing flight and potentially match wingbeat frequencies to a mechanical resonance. Flying at resonance may be energetically favorable under steady conditions, but it is difficult to modulate the frequency of a resonant system. Evidence suggests that insects utilize frequency modulation over long time scales to adjust aerodynamic forces, but it remains an open question the extent to which insects can modulate frequency on the wingstroke-to-wingstroke timescale. If wingbeat frequencies deviate from resonance, the musculature must work against the elastic flight system, thereby potentially increasing energetic costs. To assess how insects address the simultaneous needs for power and control, we tested the capacity for wingstroke-to-wingstroke wingbeat frequency modulation by perturbing free hovering Manduca sexta with vortex rings while recording high-speed video at 2000 fps. Because hawkmoth flight muscles are synchronous, there is at least the potential for the nervous system to modulate frequency on each wingstroke. We observed {+/-} 16% wingbeat frequency modulation in just a few wing strokes. Via instantaneous phase analysis of wing kinematics, we found that over 85% of perturbation responses required active changes in motor input frequency. Unlike their robotic counterparts that explicitly abdicate frequency modulation in favor of energy efficiency, we find that wingstroke-to-wingstroke frequency modulation is an underappreciated control strategies that complements other strategies for maneuverability and stability in insect flight.

biophysics↗

bioRxiv2020

Vision does not impact walking performance in Argentine ants

Many walking insects use vision for long-distance navigation, but the influence of vision in detecting close-range obstacles and directing the limbs to maintain stability remains largely untested. We compared Argentine ant workers in light versus darkness while traversing flat and uneven terrain. In darkness, ants reduced flat-ground walking speeds by only 5%. Similarly, neither the approach speed nor the time to cross a step obstacle was affected by lighting. To determine if tactile sensing might compensate for vision loss, we tracked antennal motion and observed shifts in spatiotemporal activity due to terrain structure but not illumination. Together, these findings suggest that vision does not impact walking performance in Argentine ant workers. Our results help contextualize eye variation across ants, including subterranean, nocturnal, and eyeless species that walk in complete darkness. More broadly, our findings highlight the importance of integrating vision, proprioception, and tactile sensing for robust locomotion in unstructured environments.

animal behavior and cognition↗

bioRxiv2019

Rough substrates constrain walking speed in ants through modulation of stride frequency and not stride length

Natural terrain is rarely flat. Substrate irregularities challenge walking animals to maintain stability, yet we lack quantitative assessments of walking performance and limb kinematics on naturally rough ground. We measured how continually rough 3D-printed substrates influence walking performance of Argentine ants by measuring walking speeds of workers from lab colonies and by testing colony-wide substrate preference in field experiments. Tracking limb motion in over 8,000 videos, we used statistical models that associate walking speed with limb kinematic parameters to compare movement over flat versus rough ground. We found that rough substrates reduced preferred and peak walking speeds by up to 42% and that ants actively avoided rough terrain in the field. Observed speed reductions were modulated primarily by shifts in stride frequency and not stride length, a pattern consistent across flat and rough substrates. Modeling revealed that walking speeds on rough substrates were accurately predicted based on flat walking data for over 89% of strides. Those strides that were not well modeled primarily involved limb perturbations, including missteps, active foot repositioning, and slipping. Together these findings relate kinematic mechanisms underlying walking performance on rough terrain to ecologically-relevant measures under field conditions.

biophysics↗

bioRxiv2019

Indirect actuation reduces flight power requirements in Manduca sexta via elastic energy exchange

In the vast majority of flying insects, wing movements are generated indirectly via the deformations of the exoskeleton. Indirect measurements of inertial and aerodynamic power requirements suggest that elastic energy exchange in spring-like structures may reduce the high power requirements of flight by recovering energy from one wingstroke to the next. We directly measured deformation mechanics and elastic energy storage in a hawkmoth Manduca sexta thorax by recording the force required to deform the thorax over a frequency range encompassing typical wingbeat frequencies. We found that a structural damping model, not a viscoelastic model, accurately describes the thoraxs linear spring-like properties and frequency independent dissipation. The energy recovered from thorax deformations is sufficient to minimize flight power requirements. By removing the passive musculature, we find that the exoskeleton determines thorax mechanics. To assess the factors that determine the exoskeletons spring-like properties, we isolated functional thorax regions, disrupted strain in an otherwise intact thorax, and compared results to a homogeneous hemisphere. We found that mechanical coupling between spatially separated thorax regions improves energy exchange performance. Furthermore, local mechanical properties depend on global strain patterns. Finally, the addition of scutum deformations via indirect actuation provides additional energy recovery without added dissipation.

biophysics↗