Quasi-steady aerodynamic theory under-predicts glide performance in flying snakes.

Flying snakes (genus Chrysopelea) glide without the use of wings. Instead, they splay their ribs and undulate through the air. A snake's ability to glide depends on how well its morphing wing-body produces lift and drag forces. However, previous kinematics experiments under-resolved the body, making it impossible to estimate the aerodynamic load on the animal or to quantify the different wing configurations throughout the glide. Here, we present new kinematic analyses of a previous glide experiment, and use the results to test a theoretical model of flying snake aerodynamics using previously measured lift and drag coefficients to estimate the aerodynamic forces. This analysis is enabled by new measurements of the center of mass motion based on experimental data. We found that quasi-steady aerodynamic theory under-predicts lift by 35% and over-predicts drag by 40%. We also quantified the relative spacing of the body as the snake translates through the air. In steep glides, the body is generally not positioned to experience tandem effects from wake interaction during the glide. These results suggest that unsteady 3D effects, with appreciable force enhancement, are important for snake flight. Future work can use the kinematics data presented herein to form test conditions for physical modeling, as well as computational studies to understand unsteady fluid dynamics effects on snake flight.

Skittering locomotion in cricket frogs: a form of porpoising.

Multiple species of frogs in the Ranidae family have been observed to 'skitter' across the water surface, but little is understood about the biomechanical or physical mechanisms that underlie this behavior. All documented descriptions are anecdotal, asserting simply that the frogs can cross the water surface without sinking. To study this form of interfacial locomotion, we recorded high speed video of the northern cricket frog Acris crepitans and quantified its kinematics. We also compared its semi-aquatic behavior with the frogs' terrestrial locomotion. Contrary to expectations based on anecdotal knowledge, we found that cricket frogs do not maintain an above-surface position throughout the locomotor cycle. Instead, the frogs are completely submerged during both the launching and landing phase of a jump cycle, similar to porpoising in other animals. It is possible that leg-retraction time constrains these frogs from performing true surface-only locomotion.

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.

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.

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.

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.

Physiological responses to gravity in an insect.

Gravity is one of the most ubiquitous environmental effects on living systems: Cellular and organismal responses to gravity are of central importance to understanding the physiological function of organisms, especially eukaryotes. Gravity has been demonstrated to have strong effects on the closed cardiovascular systems of terrestrial vertebrates, with rapidly responding neural reflexes ensuring proper blood flow despite changes in posture. Invertebrates possess open circulatory systems, which could provide fewer mechanisms to restrict gravity effects on blood flow, suggesting that these species also experience effects of gravity on blood pressure and distribution. However, whether gravity affects the open circulatory systems of invertebrates is unknown, partly due to technical measurement issues associated with small body size. Here we used X-ray imaging, radio-tracing of hemolymph, and micropressure measurements in the American grasshopper, Schistocerca americana, to assess responses to body orientation. Our results show that during changes in body orientation, gravity causes large changes in blood and air distribution, and that body position affects ventilation rate. Remarkably, we also found that insects show similar heart rate responses to body position as vertebrates, and contrasting with the classic understanding of open circulatory systems, have flexible valving systems between thorax and abdomen that can separate pressures. Gravitational effects on invertebrate cardiovascular and respiratory systems are likely to be widely distributed among invertebrates and to have broad influence on morphological and physiological evolution.

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.

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.

How temperature influences the viscosity of hornworm hemolymph.

Hemolymph is responsible for the transport of nutrients and metabolic waste within the insect circulatory system. Circulation of hemolymph is governed by viscosity, a physical property, which is well known to be influenced by temperature. However, the effect of temperature on hemolymph viscosity is unknown. We used Manduca sexta larvae to measure hemolymph viscosity across a range of physiologically relevant temperatures. Measurements were taken from 0 to 45°C using a cone and plate viscometer in a sealed environmental chamber. Hemolymph viscosity decreased with increasing temperature, showing a 6.4-fold change (11.08 to 1.74 cP) across the temperature range. Viscosity values exhibited two behaviors, changing rapidly from 0 to 15°C and slowly from 17.5 to 45°C. To test the effects of large particulates (e.g. cells) on viscosity, we also tested hemolymph plasma alone. Plasma viscosity also decreased as temperature increased, but did not exhibit two slope regimes, suggesting that particulates strongly influence low-temperature shifts in viscosity values. These results suggest that as environmental temperatures decrease, insects experience dramatic changes in hemolymph viscosity, leading to altered circulatory flows or increased energetic input to maintain similar flows. Such physical effects represent a previously unrecognized factor in the thermal biology of insects.

Dogs lap using acceleration-driven open pumping.

Dogs lap because they have incomplete cheeks and cannot suck. When lapping, a dog's tongue pulls a liquid column from the bath, suggesting that the hydrodynamics of column formation are critical to understanding how dogs drink. We measured lapping in 19 dogs and used the results to generate a physical model of the tongue's interaction with the air-fluid interface. These experiments help to explain how dogs exploit the fluid dynamics of the generated column. The results demonstrate that effects of acceleration govern lapping frequency, which suggests that dogs curl the tongue to create a larger liquid column. Comparing lapping in dogs and cats reveals that, despite similar morphology, these carnivores lap in different physical regimes: an unsteady inertial regime for dogs and steady inertial regime for cats.

Patterns of Tracheal Compression in the Thorax of the Ground Beetle, Platynus decentis.

Insects breathe using a system of tracheal tubes that ramify throughout the body. Rhythmic tracheal compression (RTC), the periodic collapse and reinflation of parts of the system, has been identified in multiple taxa, but little is known about the precise dynamics of tube deformation cycles. It has been hypothesized that during RTC, compression occurs synchronously throughout the body, but specific kinematic patterns along the length of individual tracheae may vary. Tube collapse or reinflation that proceeds unidirectionally along the length of a tube may function as a pump to transport air, augmenting gas exchange. This study aims to characterize patterns of tracheal compression in one species of carabid beetle, Platynus decentis, to test the hypothesis of directional compression. The internal tracheae of living beetles were visualized using synchrotron x-ray phase contrast imaging at the Advanced Photon Source, Argonne National Laboratory. X-ray video results show that tracheal compression is characterized by the formation of discrete, buckled regions in the tube wall, giving the appearance of "dimpling." Dimple formation in the main dorsal tracheal trunks of the prothorax occurred as two semi-circular fronts that spread symmetrically or directionally along the longitudinal tube axis. In the transverse axis, the main ventral trunks collapsed in the lateral direction, whereas the dorsal trunks collapsed dorsoventrally. Along the length of the ventral thoracic tracheal trunks, collapse and reinflation occurred synchronously in the majority of cycles (75 percent), not sequentially. Synchronous longitudinal compression and consistent dimple formation kinematics within an animal suggest that Platynus decentis employs a stereotyped mechanism to produce cycles of tracheal collapse and reinflation, but such compression does not function as a unidirectional pump, at least along the length of the local trachea. Further data on spiracle opening and closing patterns and internal pressures within the tracheal system are required to determine actual airflow patterns within the body.

Multigenerational Effects of Rearing Atmospheric Oxygen Level on the Tracheal Dimensions and Diffusing Capacities of Pupal and Adult Drosophila melanogaster.

Insects are small relative to vertebrates, and were larger in the Paleozoic when atmospheric oxygen levels were higher. The safety margin for oxygen delivery does not increase in larger insects, due to an increased mass-specific investment in the tracheal system and a greater use of convection in larger insects. Prior studies have shown that the dimensions and number of tracheal system branches varies inversely with rearing oxygen in embryonic and larval insects. Here we tested whether rearing in 10, 21, or 40 kPa atmospheric oxygen atmospheres for 5-7 generations affected the tracheal dimensions and diffusing capacities of pupal and adult Drosophila. Abdominal tracheae and pupal snorkel tracheae showed weak responses to oxygen, while leg tracheae showed strong, but imperfect compensatory changes. The diffusing capacity of leg tracheae appears closely matched to predicted oxygen transport needs by diffusion, perhaps explaining the consistent and significant responses of these tracheae to rearing oxygen. The reduced investment in tracheal structure in insects reared in higher oxygen levels may be important for conserving tissue PO2 and may provide an important mechanism for insects to invest only the space and materials necessary into respiratory structure.

Tracheal compression in pupae of the beetle Zophobas morio.

Insects that are small or exhibit low metabolic rates are considered to not require active ventilation to augment diffusive gas exchange. Some pupae with low metabolic rates exhibit abdominal pumping, a behaviour that is known to drive tracheal ventilation in the adults of many species. However, previous work on pupae suggests that abdominal pumping may serve a non-respiratory role. To study the role of abdominal pumping in pupa of the beetle Zophobas morio, we visualized tracheal dynamics with X-rays while simultaneously measuring haemolymph pressure, abdominal movement, and CO2 emission. Pupae exhibited frequent tracheal compressions that were coincident with both abdominal pumping and pulsation of pressure in the haemolymph. However, more than 63% of abdominal pumping events occurred without any tracheal collapse and hence ventilation, suggesting that the major function of the abdominal pump is not respiratory. In addition, this study shows that the kinematics of abdominal pumping can be used to infer the status of the spiracles and internal behaviour of the tracheal system.

How locusts breathe.

Insect tracheal-respiratory systems achieve high fluxes and great dynamic range with low energy requirements and could be important models for bioengineers interested in developing microfluidic systems. Recent advances suggest that insect cardiorespiratory systems have functional valves that permit compartmentalization with segment-specific pressures and flows and that system anatomy allows regional flows. Convection dominates over diffusion as a transport mechanism in the major tracheae, but Reynolds numbers suggest viscous effects remain important.

Aerodynamics of the flying snake Chrysopelea paradisi: how a bluff body cross-sectional shape contributes to gliding performance.

A prominent feature of gliding flight in snakes of the genus Chrysopelea is the unique cross-sectional shape of the body, which acts as the lifting surface in the absence of wings. When gliding, the flying snake Chrysopelea paradisi morphs its circular cross-section into a triangular shape by splaying its ribs and flattening its body in the dorsoventral axis, forming a geometry with fore-aft symmetry and a thick profile. Here, we aimed to understand the aerodynamic properties of the snake's cross-sectional shape to determine its contribution to gliding at low Reynolds numbers. We used a straight physical model in a water tunnel to isolate the effects of 2D shape, analogously to studying the profile of an airfoil of a more typical flyer. Force measurements and time-resolved (TR) digital particle image velocimetry (DPIV) were used to determine lift and drag coefficients, wake dynamics and vortex-shedding characteristics of the shape across a behaviorally relevant range of Reynolds numbers and angles of attack. The snake's cross-sectional shape produced a maximum lift coefficient of 1.9 and maximum lift-to-drag ratio of 2.7, maintained increases in lift up to 35 deg, and exhibited two distinctly different vortex-shedding modes. Within the measured Reynolds number regime (Re=3000-15,000), this geometry generated significantly larger maximum lift coefficients than many other shapes including bluff bodies, thick airfoils, symmetric airfoils and circular arc airfoils. In addition, the snake's shape exhibited a gentle stall region that maintained relatively high lift production even up to the highest angle of attack tested (60 deg). Overall, the cross-sectional geometry of the flying snake demonstrated robust aerodynamic behavior by maintaining significant lift production and near-maximum lift-to-drag ratios over a wide range of parameters. These aerodynamic characteristics help to explain how the snake can glide at steep angles and over a wide range of angles of attack, but more complex models that account for 3D effects and the dynamic movements of aerial undulation are required to fully understand the gliding performance of flying snakes.

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.

Dynamics of tracheal compression in the horned passalus beetle.

Rhythmic patterns of compression and reinflation of the thin-walled hollow tubes of the insect tracheal system have been observed in a number of insects. These movements may be important for facilitating the transport and exchange of respiratory gases, but observing and characterizing the dynamics of internal physiological systems within live insects can be challenging due to their size and exoskeleton. Using synchrotron X-ray phase-contrast imaging, we observed dynamical behavior in the tracheal system of the beetle, Odontotaenius disjunctus. Similar to observations of tracheal compression in other insects, specific regions of tracheae in the thorax of O. disjunctus exhibit rhythmic collapse and reinflation. During tracheal compression, the opposing sides of a tracheal tube converge, causing the effective diameter of the tube to decrease. However, a unique characteristic of tracheal compression in this species is that certain tracheae collapse and reinflate with a wavelike motion. In the dorsal cephalic tracheae, compression begins anteriorly and continues until the tube is uniformly flattened; reinflation takes place in the reverse direction, starting with the posterior end of the tube and continuing until the tube is fully reinflated. We report the detailed kinematics of this pattern as well as additional observations that show tracheal compression coordinated with spiracle opening and closing. These findings suggest that tracheal compression may function to drive flow within the body, facilitating internal mixing of respiratory gases and ventilation of distal regions of the tracheal system.