Animal locomotion: Wing-like femoral lobes help orchid mantid nymphs glide.

The femoral lobes of the orchid mantis give this fierce predator a flower-like appearance, but they also assist in gliding, showing that form can match function in more ways than one.

Dynamic gap crossing in Dendrelaphis, the sister taxon of flying snakes.

Arboreal animals commonly use dynamic gap-crossing behaviors such as jumping. In snakes, however, most species studied to date only employ the quasi-static cantilever crawl, which involves a whole-body reach. One exception is the paradise tree snake (Chrysopelea paradisi), which exhibits kinematic changes as gap distance increases, culminating in dynamic behaviors that are kinematically indistinguishable from those used to launch glides. Because Chrysopelea uses dynamic behaviors when bridging gaps without gliding, we hypothesized that such dynamic behaviors evolved ancestrally to Chrysopelea. To test this predicted occurrence of dynamic behaviors in closely related taxa, we studied gap bridging locomotion in the genus Dendrelaphis, which is the sister lineage of Chysopelea. We recorded 20 snakes from two species (D. punctulatus and D. calligastra) crossing gaps of increasing size, and analyzed their 3D kinematics. We found that, like C. paradisi, both species of Dendrelaphis modulate their use of dynamic behaviors in response to gap distance, but Dendrelaphis exhibit greater inter-individual variation. Although all three species displayed the use of looped movements, the highly stereotyped J-loop movement of Chrysopelea was not observed in Dendrelaphis. These results support the hypothesis that Chrysopelea may have co-opted and refined an ancestral behavior for crossing gaps for the novel function of launching a glide. Overall, these data demonstrate the importance of gap distance in governing behavior and kinematics during arboreal gap crossing.

A Year at the Forefront of Gliding Locomotion.

This review highlights the largely understudied behavior of gliding locomotion, which is exhibited by a diverse range of animals spanning vertebrates and invertebrates, in air and in water. The insights in the literature gained from January 2022 to December 2022 continue to challenge the previously held notion of gliding as a relatively simple form of locomotion. Using advances in field/lab data collection and computation, the highlighted studies cover gliding in animals including seabirds, flying lizards, flying snakes, geckos, dragonflies, damselflies, and dolphins. Altogether, these studies present gliding as a sophisticated behavior resulting from the interdependent aspects of morphology, sensing, environment, and likely selective pressures. This review uses these insights as inspiration to encourage researchers to revisit gliding locomotion, both in the animal's natural habitat and in the laboratory, and to investigate questions spanning gliding biomechanics, ecology, sensing, and the evolution of animal flight.

Air-to-land transitions: from wingless animals and plant seeds to shuttlecocks and bio-inspired robots.

Recent observations of wingless animals, including jumping nematodes, springtails, insects, and wingless vertebrates like geckos, snakes, and salamanders, have shown that their adaptations and body morphing are essential for rapid self-righting and controlled landing. These skills can reduce the risk of physical damage during collision, minimize recoil during landing, and allow for a quick escape response to minimize predation risk. The size, mass distribution, and speed of an animal determine its self-righting method, with larger animals depending on the conservation of angular momentum and smaller animals primarily using aerodynamic forces. Many animals falling through the air, from nematodes to salamanders, adopt a skydiving posture while descending. Similarly, plant seeds such as dandelions and samaras are able to turn upright in mid-air using aerodynamic forces and produce high decelerations. These aerial capabilities allow for a wide dispersal range, low-impact collisions, and effective landing and settling. Recently, small robots that can right themselves for controlled landings have been designed based on principles of aerial maneuvering in animals. Further research into the effects of unsteady flows on self-righting and landing in small arthropods, particularly those exhibiting explosive catapulting, could reveal how morphological features, flow dynamics, and physical mechanisms contribute to effective mid-air control. More broadly, studying apterygote (wingless insects) landing could also provide insight into the origin of insect flight. These research efforts have the potential to lead to the bio-inspired design of aerial micro-vehicles, sports projectiles, parachutes, and impulsive robots that can land upright in unsteady flow conditions.

3D X-ray analysis of the subterranean burrowing depth and pupal chamber size of Laricobius (Coleoptera: Derodontidae), a specialist predator of Adelges tsugae (Hemiptera: Adelgidae).

The non-native hemlock woolly adelgid (HWA), Adelges tsugae Annand (Hemiptera: Adelgidae), has caused a significant decline of eastern hemlock, Tsuga canadensis L. (Pinales: Pinaceae), and Carolina hemlock, Tsuga caroliniana Engelmann (Pinales: Pinaceae), in eastern North America. Biological control of HWA has focused on the use of 2 Laricobius spp. (Coleoptera: Derodontidae), natural predators of HWA, which require arboreal and subterranean life phases to complete their development. In its subterranean phase, Laricobius spp. are subject to abiotic factors including soil compaction or soil-applied insecticides used to protect hemlock from HWA. This study used 3D X-ray microcomputed tomography (micro-CT) to identify the depth at which Laricobius spp. burrows during its subterranean lifecycle, characterize pupal chamber volume, and determine whether soil compaction had a significant effect on these variables. The mean burrowing depth in the soil of individuals was 27.0 mm ± 14.8 (SD) and 11.4 mm ± 11.8 (SD) at compaction levels of 0.36 and 0.54 g/cm3, respectively. The mean pupal chamber volume was 11.15 mm3 ± 2.8 (SD) and 7.65 mm3 ± 3.5 (SD) in soil compacted at 0.36 and 0.54 g/cm3, respectively. These data show that soil compaction influences burrowing depth and pupal chamber size for Laricobius spp. This information will help us better identify the effect of soil-applied insecticide residues on estivating Laricobius spp. and soil-applied insecticide residues in the field. Additionally, these results demonstrate the utility of 3D micro-CT in assessing subterranean insect activity in future studies.

Air sacs are a key adaptive trait of the insect respiratory system.

Air sacs are a well-known aspect of insect tracheal systems, but have received little research attention. In this Commentary, we suggest that the study of the distribution and function of air sacs in tracheate arthropods can provide insights of broad significance. We provide preliminary phylogenetic evidence that the developmental pathways for creation of air sacs are broadly conserved throughout the arthropods, and that possession of air sacs is strongly associated with a few traits, including the capacity for powerful flight, large body or appendage size and buoyancy control. We also discuss how tracheal compression can serve as an additional mechanism for achieving advection in tracheal systems. Together, these patterns suggest that the possession of air sacs has both benefits and costs that remain poorly understood. New technologies for visualization and functional analysis of tracheal systems provide exciting approaches for investigations that will be of broad significance for understanding invertebrate evolution.

Transient use of hemolymph for hydraulic wing expansion in cicadas.

Insect wings must be flexible, light, and strong to allow dynamic behaviors such as flying, mating, and feeding. When winged insects eclose into adults, their wings unfold, actuated hydraulically by hemolymph. Flowing hemolymph in the wing is necessary for functioning and healthy wings, both as the wing forms and as an adult. Because this process recruits the circulatory system, we asked, how much hemolymph is pumped into wings, and what happens to the hemolymph afterwards? Using Brood X cicadas (Magicicada septendecim), we collected 200 cicada nymphs, observing wing transformation over 2 h. Using dissection, weighing, and imaging of wings at set time intervals, we found that within 40 min after emergence, wing pads morphed into adult wings and total wing mass increased to ~ 16% of body mass. Thus, a significant amount of hemolymph is diverted from body to wings to effectuate expansion. After full expansion, in the ~ 80 min after, the mass of the wings decreased precipitously. In fact, the final adult wing is lighter than the initial folded wing pad, a surprising result. These results demonstrate that cicadas not only pump hemolymph into the wings, they then pump it out, producing a strong yet lightweight wing.

Complex hemolymph circulation patterns in grasshopper wings.

An insect's living systems-circulation, respiration, and a branching nervous system-extend from the body into the wing. Wing hemolymph circulation is critical for hydrating tissues and supplying nutrients to living systems such as sensory organs across the wing. Despite the critical role of hemolymph circulation in maintaining healthy wing function, wings are often considered "lifeless" cuticle, and flows remain largely unquantified. High-speed fluorescent microscopy and particle tracking of hemolymph in the wings and body of the grasshopper Schistocerca americana revealed dynamic flow in every vein of the fore- and hindwings. The global system forms a circuit, but local flow behavior is complex, exhibiting three distinct types: pulsatile, aperiodic, and "leaky" flow. Thoracic wing hearts pull hemolymph from the wing at slower frequencies than the dorsal vessel; however, the velocity of returning hemolymph (in the hindwing) is faster than in that of the dorsal vessel. To characterize the wing's internal flow mechanics, we mapped dimensionless flow parameters across the wings, revealing viscous flow regimes. Wings sustain ecologically important insect behaviors such as pollination and migration. Analysis of the wing circulatory system provides a template for future studies investigating the critical hemodynamics necessary to sustaining wing health and insect flight.

Mallard landing behavior on water follows a -constant braking strategy.

Many flying animals use optic flow to control their flight. During landing maneuvers, pigeons, hummingbirds, bats, Draco lizards and bees use the -constant braking strategy. This strategy regulates the approach by keeping the ratio of distance to an object and the rate of change of that distance constant. In keeping this ratio, , constant, a variety of deceleration profiles can lead to different collision avoidance behaviors. The landing behaviors listed above all qualify as controlled collisions, where the animal is decelerating into the object. We examined whether the same regulatory strategy is employed by mallards when landing on water. Video of mallard landing behavior was recorded at a local pond and digitized. Kinematic and τ parameters were calculated for each landing (N=177). The Pearson correlation coefficient for τ with respect to time to land was 0.99±0.02, indicating mallards employ a controlled-collision strategy. This result implies regulation by the birds to fix as constant while landing (on average, 0.90±0.13). In comparison with other active flyers, mallards use a higher value of when landing (0.775±0.109, 0.710±0.132 and 0.702±0.052 for pigeons, hummingbirds and bats, respectively). This higher may reflect physical differences in substrate from solid to liquid. The higher compliance of water in comparison to a solid substrate may reduce impact forces that could be injurious on a solid substrate, thereby enabling mallards to approach faster and expend less energy for costly, slow flight.

Reconsidering tympanal-acoustic interactions leads to an improved model of auditory acuity in a parasitoid fly.

Although most binaural organisms locate sound sources using neurological structures to amplify the sounds they hear, some animals use mechanically coupled hearing organs instead. One of these animals, the parasitoid flyOrmia ochracea(O. ochracea), has astoundingly accurate sound localization abilities. It can locate objects in the azimuthal plane with a precision of 2°, equal to that of humans, despite an intertympanal distance of only 0.5 mm, which is less than1/100th of the wavelength of the sound emitted by the crickets that it parasitizes.O. ochraceaaccomplishes this feat via mechanically coupled tympana that interact with incoming acoustic pressure waves to amplify differences in the signals received at the two ears. In 1995, Mileset aldeveloped a model of hearing mechanics inO. ochraceathat represents the tympana as flat, front-facing prosternal membranes, though they lie on a convex surface at an angle from the flies' frontal and transverse planes. The model works well for incoming sound angles less than±30∘but suffers from reduced accuracy (up to 60% error) at higher angles compared to response data acquired fromO. ochraceaspecimens. Despite this limitation, it has been the basis for bio-inspired microphone designs for decades. Here, we present critical improvements to this classic hearing model based on information from three-dimensional reconstructions ofO. ochracea's tympanal organ. We identified the orientation of the tympana with respect to a frontal plane and the azimuthal angle segment between the tympana as morphological features essential to the flies' auditory acuity, and hypothesized a differentiated mechanical response to incoming sound on the ipsi- and contralateral sides that depend on these features. We incorporated spatially-varying model coefficients representing this asymmetric response, making a new quasi-two-dimensional (q2D) model. The q2D model has high accuracy (average errors of under 10%) for all incoming sound angles. This improved biomechanical model may inform the design of new microscale directional microphones and other small-scale acoustic sensor systems.

Material properties of skin in the flying snake Chrysopelea ornata.

In snakes, the skin serves for protection, camouflage, visual signaling, locomotion, and its ability to stretch facilitates large prey ingestion. The flying snakes of the genus Chrysopelea are capable of jumping and gliding through the air, requiring additional functional demands: its skin must accommodate stretch in multiple directions during gliding and, perhaps more importantly, during high-speed, direct-impact landing. Is the skin of flying snakes specialized for gliding? Here, we characterized the material properties of the skin of Chrysopelea ornata and compared them with two nongliding species of colubrid snakes, Thamnophis sirtalis and Pantherophis guttatus, as well as with previously published values. The skin was examined using uniaxial tensile testing to measure stresses, and digital image correlation methods to determine strains, yielding metrics of strength, elastic modulus, strain energy, and extensibility. To test for loading orientation effects, specimens were tested from three orientations relative to the snake's long axis: lateral, circumferential, and ventral. Specimens were taken from two regions of the body, pre- and pos-tpyloric, to test for regional effects related to the ingestion of large prey. In comparison with T. sirtalis and P. guttatus, C. ornata exhibited higher post-pyloric and lower pre-pyloric extensibility in circumferential specimens. However, overall there were few differences in skin material properties of C. ornata compared to other species, both within and across studies, suggesting that the skin of flying snakes is not specialized for gliding locomotion. Surprisingly, circumferential specimens demonstrated lower strength and extensibility in pre-pyloric skin, suggesting less regional specialization related to large prey.

Isometric spiracular scaling in scarab beetles-implications for diffusive and advective oxygen transport.

The scaling of respiratory structures has been hypothesized to be a major driving factor in the evolution of many aspects of animal physiology. Here, we provide the first assessment of the scaling of the spiracles in insects using 10 scarab beetle species differing 180× in mass, including some of the most massive extant insect species. Using X-ray microtomography, we measured the cross-sectional area and depth of all eight spiracles, enabling the calculation of their diffusive and advective capacities. Each of these metrics scaled with geometric isometry. Because diffusive capacities scale with lower slopes than metabolic rates, the largest beetles measured require 10-fold higher PO2 gradients across the spiracles to sustain metabolism by diffusion compared to the smallest species. Large beetles can exchange sufficient oxygen for resting metabolism by diffusion across the spiracles, but not during flight. In contrast, spiracular advective capacities scale similarly or more steeply than metabolic rates, so spiracular advective capacities should match or exceed respiratory demands in the largest beetles. These data illustrate a general principle of gas exchange: scaling of respiratory transport structures with geometric isometry diminishes the potential for diffusive gas exchange but enhances advective capacities; combining such structural scaling with muscle-driven ventilation allows larger animals to achieve high metabolic rates when active.

The impact of sampling frequency on ground reaction force variables.

New portable and low-cost technologies for assessing limb loading may be useful in non-laboratory environments, but have relatively low sampling frequencies. The lowest recommended sampling frequency for impact kinetics has not been investigated. The purpose of this study was to determine the effect of sampling frequency on metrics of impact kinetics during landing, walking, and running. This was a retrospective analysis of bilateral drop vertical jumps, unilateral drop landings, treadmill running, and flat, inclined, and declined treadmill walking. Landing data were collected at 1920 Hz while walking and running data were collected at 1440 Hz. Impact kinetics were computed at the highest possible sampling frequency, and then data were continuously down-sampled to determine the impact on the following computed metrics: peak impact force, average LR, and impulse. The minimum sampling frequency to compute each outcome with 90%, 95%, and 99.5% accuracy when compared to the original sampling frequency were determined. To achieve 90% of the true value of impact force, a sampling frequency of 180 Hz was needed for running, 62 Hz for bilateral landing, and 48 Hz for remaining tasks. For average LR, a sampling frequency of 1440 Hz was need for running, 63 Hz for inclined walking, 192 Hz for bilateral landing, and 48 Hz for the remaining tasks. For impulse, 48 Hz was required for all tasks. The results of this study provide future researchers with a guide for selecting the sampling frequency required to accurately assess impact kinetics during walking, landing, or running.

Dynamic movements facilitate extreme gap crossing in flying snakes.

In arboreal habitats, direct routes between two locations can be impeded by gaps in the vegetation. Arboreal animals typically use dynamic movements, such as jumping, to navigate these gaps if the distance between supports exceeds their reaching ability. In contrast, most snakes only use the cantilever crawl to cross gaps. This behavior imposes large torques on the animal, inhibiting their gap-crossing capabilities. Flying snakes (Chrysopelea), however, are known to use dynamic behaviors in a different arboreal context: they use a high-acceleration jump to initiate glides. We hypothesized that flying snakes also use jumping take-off behaviors to cross gaps, allowing them to cross larger distances. To test this hypothesis, we used a six-camera motion-capture system to investigate the effect of gap size on crossing behavior in Chrysopelea paradisi, and analyzed the associated kinematics and torque requirements. We found that C. paradisi typically uses cantilevering for small gaps (<47.5% snout-vent length, SVL). Above this distance, C. paradisi were more likely to use dynamic movements than cantilevers, either arching upward or employing a below-branch loop of the body. These dynamic movements extended the range of horizontal crossing to ∼120% SVL. The behaviors used for the largest gaps were kinematically similar to the J-loop jumps used in gliding, and involved smaller torques than the cantilevers. These data suggest that the ability to jump allows flying snakes to access greater resources in the arboreal environment, and supports the broader hypothesis that arboreal animals jump across gaps only when reaching is not mechanically possible.

The aerodynamics of flying snake airfoils in tandem configuration.

Flying snakes flatten their body to form a roughly triangular cross-sectional shape, enabling lift production and horizontal acceleration. While gliding, they also assume an S-shaped posture, which could promote aerodynamic interactions between the fore and the aft body. Such interactions have been studied experimentally; however, very coarse models of the snake's cross-sectional shape were used, and the effects were measured only for the downstream model. In this study, the aerodynamic interactions resulting from the snake's posture were approximated using two-dimensional anatomically accurate airfoils positioned in tandem to mimic the snake's geometry during flight. Load cells were used to measure the lift and drag forces, and flow field data were obtained using digital particle image velocimetry (DPIV). The results showed a strong dependence of the aerodynamic performance on the tandem arrangement, with the lift coefficients being generally more influenced than the drag coefficients. Flow field data revealed that the tandem arrangement modified the separated flow and the wake size, and enhanced the lift in cases in which the wake vortices formed closer to the models, producing suction on the dorsal surface. The downforce created by the flow separation from the ventral surface of the models at 0 deg angle of attack was another significant factor contributing to lift production. A number of cases showing large variations of aerodynamic performance included configurations close to the most probable posture of airborne flying snakes, suggesting that small postural variations could be used to control the glide trajectory.

Frequency-specific, valveless flow control in insect-mimetic microfluidic devices.

Inexpensive, portable lab-on-a-chip devices would revolutionize fields like environmental monitoring and global health, but current microfluidic chips are tethered to extensive off-chip hardware. Insects, however, are self-contained and expertly manipulate fluids at the microscale using largely unexplored methods. We fabricated a series of microfluidic devices that mimic key features of insect respiratory kinematics observed by synchrotron-radiation imaging, including the collapse of portions of multiple respiratory tracts in response to a single fluctuating pressure signal. In one single-channel device, the flow rate and direction could be controlled by the actuation frequency alone, without the use of internal valves. Additionally, we fabricated multichannel chips whose individual channels responded selectively (on with a variable, frequency-dependent flow rate, or off) to a single, global actuation frequency. Our results demonstrate that insect-mimetic designs have the potential to drastically reduce the actuation overhead for microfluidic chips, and that insect respiratory systems may share features with impedance-mismatch pumps.

Nonlinear elasticity and damping govern ultrafast dynamics in click beetles.

Many small animals use springs and latches to overcome the mechanical power output limitations of their muscles. Click beetles use springs and latches to bend their bodies at the thoracic hinge and then unbend extremely quickly, resulting in a clicking motion. When unconstrained, this quick clicking motion results in a jump. While the jumping motion has been studied in depth, the physical mechanisms enabling fast unbending have not. Here, we first identify and quantify the phases of the clicking motion: latching, loading, and energy release. We detail the motion kinematics and investigate the governing dynamics (forces) of the energy release. We use high-speed synchrotron X-ray imaging to observe and analyze the motion of the hinge's internal structures of four Elater abruptus specimens. We show evidence that soft cuticle in the hinge contributes to the spring mechanism through rapid recoil. Using spectral analysis and nonlinear system identification, we determine the equation of motion and model the beetle as a nonlinear single-degree-of-freedom oscillator. Quadratic damping and snap-through buckling are identified to be the dominant damping and elastic forces, respectively, driving the angular position during the energy release phase. The methods used in this study provide experimental and analytical guidelines for the analysis of extreme motion, starting from motion observation to identifying the forces causing the movement. The tools demonstrated here can be applied to other organisms to enhance our understanding of the energy storage and release strategies small animals use to achieve extreme accelerations repeatedly.

Validity of Using Automated Two-Dimensional Video Analysis to Measure Continuous Sagittal Plane Running Kinematics.

Two-dimensional video analysis is commonly used to assess kinematics when three-dimensional motion capture is unavailable. However, videos are often assessed using manual digitization, which limits the ability to extract outcomes that require continuous data. Here, we introduced a method to collect continuous kinematic data in 2D using an inexpensive camera and an open-source automated marker tracking program. We tested the validity of this method by comparing 2D video analysis to 3D motion capture for measuring sagittal-plane running kinematics. Twenty uninjured participants ran on a treadmill for 1-min while lower extremity kinematics were collected simultaneously in 3D using a motion capture system and in 2D using a single digital camera, both at 120 Hz. Knee, ankle, and foot angle at contact, peak knee flexion, knee flexion excursion, and knee-ankle flexion vector coding variability were computed using both the 3D and 2D kinematic data, and were compared using intraclass correlation coefficients and Bland-Altman plots. The agreement between collection methods was excellent for foot angle at contact and knee flexion excursion, good for ankle and knee angle at contact and knee-ankle vector coding variability, and moderate for peak knee flexion. However, Bland-Altman plots revealed significant differences between the 2D and 3D collection methods, which varied across study participants. These low-cost methods could be useful for collecting continuous sagittal plane running kinematics in non-laboratory settings.

Visual acuity in the flying snake, Chrysopelea paradisi.

Visual control during high-speed aerial locomotion requires a visual system adapted for such behaviors. Flying snakes (genus: Chrysopelea) are capable of gliding at speeds up to 11 m s-1 and perform visual assessments before take-off. Determining nuances of control requires a closed-loop experimental system, such as immersive virtual arenas. To characterize vision in the flying snake Chrysopelea paradisi, we used digitally reconstructed models of the head to determine a 3D field of vision. We also used optokinetic drum experiments and compared slowphase optokinetic nystagmus (OKN) speeds to calculate visual acuity and conducted preliminary experiments to determine whether snakes would respond to closed-loop virtual stimuli. Visual characterization showed that C. paradisi likely has a large field of view (308.5 ± 6.5° azimuthal range), with a considerable binocular region (33.0 ± 11.0° azimuthal width) that extends overhead. Their visual systems are broadly tuned and motion-sensitive, with peak OKN response gains of 0.50 ± 0.11 seen at 46.06 ± 11.08 Hz, and a low spatial acuity, with peak gain of 0.92 ± 0.41 seen at 2.89 ± 0.16 cpd (cycles per degree). These characteristics were used to inform settings in an immersive virtual arena, including framerate, brightness, and stimulus size. In turn, the immersive virtual arena was used to reproduce the optokinetic drum experiments. We elicited OKN in open-loop experiments, with a mean gain of 0.21 ± 0.9 seen at 0.019 ± 6x10-5 cpd and 1.79 ± 0.01 Hz. In closed-loop experiments, snakes did not exhibit OKN, but held the image fixed, indicating visual stabilization. These results demonstrate for that C. paradisi responds to visual stimuli in a digital virtual arena. The accessibility and adaptability of the virtual setup make it suitable for future studies of visual control in snakes and other animals in an unconstrained setting.