Tracheal hyperallometry and spatial constraints in a large beetle.

Insects exchange respiratory gases with their environment through their gas-filled tracheal system, a branched tracheal tree extending from segmental openings and terminating at fine tissue penetrating tracheoles. It was shown that the tracheal volume increases hyperallometrically with insect body size (Mb), both interspecifically and across developmental stages. In this study, we used the sixfold Mb variation in adult Batocera rufomaculata(Cerambicidae; Coleoptera) examining the allometry of adult tracheal volume (Vtr). We further explored the effect of sex and sexual maturity on tracheal gas conductance, testing the hypotheses that (i) larger body size and (ii) egg volume in gravid females would result in lower safety margins for tracheal oxygen transport due to structural restriction. We report a hyperallometric tracheal growth in both sexes of adult B. rufomaculata(mean mass exponent of 1.42 ± 0.09), similar in magnitude to previously reported values. Tracheal gas conductance was independent of Mb and reproductive state, but was significantly higher in females compared with males. We suggest that females may have pre-adapted a higher tracheal conductance required for the higher flight power output while gravid. Lack of compliant air sacs and rigid trachea may explain how gravid females retain their Vtr. However, we show that Vtr outgrows thoracic dimensions with increased B. rufomaculatasize. Hyperallometric growth of the giant cerambycid thoracic trachea could explain the previously reported hypometric scaling of flight muscles in B. rufomaculata, and the compromised long-distance flight performance of larger compared with smaller conspecifics.

Intraspecific scaling and early life history determine the cost of free-flight in a large beetle (Batocera rufomaculata).

The scaling of the energetic cost of locomotion with body mass is well documented at the interspecific level. However, methodological restrictions limit our understanding of the scaling of flight metabolic rate (MR) in free-flying insects. This is particularly true at the intraspecific level, where variation in body mass and flight energetics may have direct consequences for the fitness of an individual. We applied a 13C stable isotope method to investigate the scaling of MR with body mass during free-flight in the beetle Batocera rufomaculata. This species exhibits large intraspecific variation in adult body mass as a consequence of the environmental conditions during larval growth. We show that the flight-MR scales with body mass to the power of 0.57, with smaller conspecifics possessing up to 2.3 fold higher mass-specific flight MR than larger ones. Whereas the scaling exponent of free-flight MR was found to be like that determined for tethered-flight, the energy expenditure during free-flight was more than 2.7 fold higher than for tethered-flight. The metabolic cost of flight should therefore be studied under free-flight conditions, a requirement now enabled by the 13C technique described herein for insect flight.

The hydrodynamic performance of duck feet for submerged swimming resembles oars rather than delta-wings.

Waterfowl use webbed feet to swim underwater. It has been suggested that the triangular shape of the webbed foot functions as a lift-generating delta wing rather than a drag-generating oar. To test this idea, we studied the hydrodynamic characteristics of a diving duck's (Aythya nyroca) foot. The foot's time varying angles-of-attack (AoAs) during paddling were extracted from movies of ducks diving vertically in a water tank. Lift and drag coefficients of 3D-printed duck-foot models were measured as a function of AoA in a wind-tunnel; and the near-wake flow dynamics behind the foot model was characterized using particle image velocimetry (PIV) in a flume. Drag provided forward thrust during the first 80% of the power phase, whereas lift dominated thrust production at the end of the power stroke. In steady flow, the transfer of momentum from foot to water peaked at 45° < AoA < 60°, due to an organized wake flow pattern (vortex street), whereas at AoAs > 60° the flow behind the foot was fully separated, generating high drag levels. The flow characteristics do not constitute the vortex lift typical of delta wings. Rather, duck feet seem to be an adaptation for propulsion at a wide range of AoAs, on and below the water surface.

Metabolic cost of flight and aerobic efficiency in the rose chafer, Protaetia cuprea (Cetoniinae).

Rose chafer beetles (Protetia cuprea) are pollinators as well as agricultural pests, flying between flowers and trees while foraging for pollen and fruits. Calculating the energy they expend on flying during foraging activity faces the challenge of measuring the metabolic rate (MR) of free-flying insects in an open space. We overcame this challenge by using the bolus injection of 13 C Na-bicarbonate technique to measure their metabolic energy expenditure while flying in a large flight arena. Concurrently, we tracked the insects with high-speed cameras to extract their flight trajectory, from which we calculated the mechanical power invested in flying for each flight bout. We found that the chemical (metabolic) energy input converted to mechanical flight energy output at a mean efficiency of 10.4% ± 5.2%, with a trend of increased efficiency in larger conspecifics (efficiency scaled with body mass to the power of 1.4). The transition in the summer from a diet of pollen to that of fruits may affect the energy budget available for foraging. Starved P. cuprea, feeding on apples ad libitum, increased their body mass by an average of 6% in 2 h. According to our calculations, such a meal can power a 630-m flight (assuming a carbohydrate assimilation efficiency of 90%). Pollen, with a low water and carbohydrate content but rich in proteins and lipids, has a higher caloric content and should assimilate differently when converting food to flight fuel. The high cost of aerial locomotion is inherent to the foraging behavior of rose chafers, explaining their short flight bouts followed by prolonged feeding activity.

The relationship between body size and flight power output in the mango stem borer (Batocera rufomaculata).

Adult body size in insects can be influenced by environmental conditions during larval growth. The effect of such intraspecific variation in body mass on flight performance is poorly understood. In Batocera rufomaculata, a large tree boring beetle, adults emerging from larvae that developed in a dying host tree, and therefore, under nutrient-deprived diet conditions, are smaller but have an elevated long-distance flight capability compared to larger conspecifics that developed in viable host trees. The improved endurance for long-distance flight in the smaller individuals appears to contradict the interspecific trend in flying animals of a decrease in Cost of Transport (CoT) with increased body mass. To explore the relationship between intraspecific variation in body size and power expended during steady forward flight, we flew these beetles tethered in a wind tunnel and compared the flapping kinematics and power output of individuals varying in body mass (1-7 gr). Concurrently, we measured the forces the insects applied on the tether allowing us to evaluate the tethering effects and correct for them. From the flapping kinematics we estimated the mechanical power expended using a quasi-steady blade-element model. We found that muscle mass-specific power did not differ between small and large individuals flying at the same wind (flight) speed in the tunnel. Consequently, the CoT of B. rufomaculata does not vary with body mass. Such invariance of mass-specific power with body mass may aid the dispersal of smaller individuals from deteriorating host trees to new ones.

Insect flight metabolic rate revealed by bolus injection of the stable isotope 13C.

Measuring metabolic rate (MR) poses a formidable challenge in free-flying insects who cannot breathe into masks or be trained to fly in controlled settings. Consequently, flight MR has been predominantly measured on hovering or tethered insects flying in closed systems. Stable isotopes such as labelled water allow measurement of MR in free-flying animals but integrates the measurement over long periods exceeding the average flight duration of insects. Here, we applied the 'bolus injection of isotopic 13C Na-bicarbonate' method to insects to measure their flight MR and report a 90% accuracy compared to respirometry. We applied the method on two beetle species, measuring MR during free flight and tethered flight in a wind tunnel. We also demonstrate the ability to repeatedly use the technique on the same individual. Therefore, the method provides a simple, reliable and accurate tool that solves a long-lasting limitation on insect flight research by enabling the measurement of MR during free flight.

Elastic wing deformations mitigate flapping asymmetry during manoeuvres in rose chafers (Protaetia cuprea).

To manoeuvre in air, flying animals produce asymmetric flapping between contralateral wings. Unlike the adjustable vertebrate wings, insect wings lack intrinsic musculature, preventing active control over wing shape during flight. However, the wings elastically deform as a result of aerodynamic and inertial forces generated by the flapping motions. How these elastic deformations vary with flapping kinematics and flight performance in free-flying insects is poorly understood. Using high-speed videography, we measured how contralateral wings elastically deform during free-flight manoeuvring in rose chafer beetles (Protaetia cuprea). We found that asymmetric flapping during aerial turns was associated with contralateral differences in chord-wise wing deformations. The highest instantaneous difference in deformation occurred during stroke reversals, resulting from differences in wing rotation timing. Elastic deformation asymmetry was also evident during mid-strokes, where wing compliance increased the angle of attack of both wings, but reduced the asymmetry in the angle of attack between contralateral wings. A biomechanical model revealed that wing compliance can increase the torques generated by each wing, providing higher potential for manoeuvrability, while concomitantly contributing to flight stability by attenuating steering asymmetry. Such stability may be adaptive for insects such as flower chafers that need to perform delicate low-speed landing manoeuvres among vegetation.

Insect-inspired jumping robots: challenges and solutions to jump stability.

Some insects can jump to heights that are several times their body length. At smaller scales, jumping mechanisms are constrained by issues relating to scaling of power generation, which insects have resolved over the course of their evolution. These solutions have inspired the design of small jumping robots. However, the insect' solution for the power constraint came at a price of instability and limited control over jump performance and these drawbacks were inherited by the jumping robots inspired by them. This review focuses on the jumping mechanisms of insects and robots, the challenges it imposes on control and stability and possible solutions. Although jump stability might not be a critical problem for insects, it poses substantial challenges for engineers of small jumping robots, who hope to develop autonomous devices with improved mobility over rough terrain.

Can electrostatic fields limit the take-off of tiny whiteflies (Bemisia tabaci)?

Electrostatic fields are abundant in the natural environment. We tested the idea that electrostatic attraction forces between tiny whiteflies (Bemisia tabaci) and the substrate could be substantial to the point of limiting their take-off. These insects are characterized by a very small body mass and powerful take-offs that are executed by jumping into the air with the wings closed. Wing opening and transition to active flight occur after the jump distanced the insect several body lengths away from the substrate. Using high-speed cameras, we captured the take-off behavior inside a uniform electrostatic field apparatus and used dead insects to calculate the electric charge that these tiny insects can carry. We show that electrostatic forces stimulate the opening of the insect's wings and can attract the whole insect toward the opposite charge. We also found that whiteflies can carry and hold an electrical charge of up to 3.5 pC. With such a charge the electrostatic field required to impede take-off is much stronger than those typically found in the natural environment. Nevertheless, our results demonstrate that artificial electrostatic fields can be effectively used to suppress flight of whiteflies, thus providing options for pest control applications in greenhouses.

The Aerodynamics and Power Requirements of Forward Flapping Flight in the Mango Stem Borer Beetle (Batocera rufomaculata).

The need for long dispersal flights can drive selection for behavioral, physiological, and biomechanical mechanisms to reduce the energy spent flying. However, some energy loss during the transfer of momentum from the wing to the fluid is inevitable, and inherent to the fluid-wing interaction. Here, we analyzed these losses during the forward flight of the mango stem borer (Batocera rufomaculata). This relatively large beetle can disperse substantial distances in search of new host trees, and laboratory experiments have demonstrated continuous tethered flights that can last for up to an hour. We flew the beetles tethered in a wind tunnel and used high-speed videography to estimate the aerodynamic power from their flapping kinematics and particle image velocimetry (PIV) to evaluate drag and kinetic energy from their unsteady wakes. To account for tethering effects, we measured the forces applied by the beetles on the tether arm holding them in place. The drag of the flying beetle over the flapping cycle, estimated from the flow fields in the unsteady wake, showed good agreement with direct measurement of mean horizontal force. Both measurements showed that total drag during flight is ∼5-fold higher than the parasite drag on the body. The aerodynamic power estimated from both the motion of the wings, using a quasi-steady blade-element model, and the kinetic energy in the wake, gave mean values of flight-muscle mass-specific power of 87 and 65 W kg muscle-1, respectively. A comparison of the two values suggests that ∼25% of the energy is lost within the fluid due to turbulence and heat. The muscle mass-specific power found here is low relative to the maximal power output reported for insect flight muscles. This can be attributed to reduce weight support during tethered flight or to operation at submaximal output that may ensure a supply of metabolic substrates to the flight muscles, thus delaying their fatigue during long-distance flights.

Loaded flight in male Ischnura elegans and its relationship to copulatory flight.

Copulation in the blue-tailed damselfly (Ischnura elegans) can last several hours, during which the pair may fly together in the 'wheel position' with both insects flapping their wings. Previous studies have suggested that during flight in copula, the male increases its power output while the female decreases it. Consequently, the male must support some of the female's body weight in the air. We tested the hypothesis that female body mass places a biomechanical constraint on the ability of smaller males to mate with larger females by attaching weights to male damselflies and analyzing their wing motion and force exerted using high-speed cameras. Males flying with an added load exerted extra forces equivalent to 157% of their body weight. Males flying in the mating wheel position with females whose wings were clipped bore a similar weight and were barely able to fly. To fly with an added load, males increased their wing-flapping frequency and amplitude, reaching values of mean wing tip flapping speed that were 1.9-fold higher than that in solitary flight. Our experiments indicate that although males would be able to fly briefly with the added weight of a non-responsive female, the flight performance of the pair would be severely compromised without the female contributing effort to the joint flight.

Life in the flow: unique adaptations for feeding on drifting zooplankton in garden eels.

A major challenge faced by sessile animals that feed in the flow is to maintain effective feeding postures while enduring hydrodynamic forces. Garden eels exhibit an exceptional lifestyle: feeding on drifting zooplankton while being 'anchored' in a burrow they dig in the sand. Using underwater observations, sampling and three-dimensional video recording, we measured the feeding rates and characterized feeding postures of garden eels under a wide range of current speeds. We show that the eels behaviorally resolve the trade-off between adverse biomechanical forces and beneficial fluxes of food by modulating their body postures according to current speeds. In doing so, the eels substantially reduce drag forces when currents are strong, yet keep their head well above bottom in order to effectively feed under conditions of high prey fluxes. These abilities have allowed garden eels to become one of the rare oceanic fishes that live in sandy, predation-rich habitats and feed on zooplankton while being attached to the bottom.

Role of side-slip flight in target pursuit: blue-tailed damselflies (Ischnura elegans) avoid body rotation while approaching a moving perch.

Visually guided flight control requires processing changes in the visual panorama (optic-flow) resulting from self-movement relative to stationary objects, as well as from moving objects passing through the field of view. We studied the ability of the blue-tailed damselfly, Ischnura elegans, to successfully land on a perch moving unpredictably. We tracked the insects landing on a vertical pole moved linearly 6 cm back and forth with sinusoidal changes in velocity. When the moving perch changed direction at frequencies higher than 1 Hz, the damselflies engaged in manoeuvres that typically involved sideways flight, with minimal changes in body orientation relative to the stationary environment. We show that these flight manoeuvres attempted to fix the target in the centre of the field of view when flying in any direction while keeping body rotation changes about the yaw axis to the minimum. We propose that this pursuit strategy allows the insect to obtain reliable information on self and target motion relative to the stationary environment from the translational optic-flow, while minimizing interference from the rotational optic-flow. The ability of damselflies to fly in any direction, irrespective of body orientation, underlines the superb flight control of these aerial predators.

The effect of air resistance on the jump performance of a small parasitoid wasp, Anagyrus pseudococci (Encyrtidae).

The distance a small insect moves through the air during a jump is limited by the launch velocity at take-off and by air resistance. The launch velocity is limited by the length of the jumping legs and the maximum power that the jump apparatus can provide for pushing against the ground. The effect of air resistance is determined by the insect mass-to-area ratio. Both limitations are highly dependent on body size, making high jumps a challenge for smaller insects. We studied both effects in the tiny Encyrtid wasp Anagyrus pseudococci. Males are smaller than females (mean body length 1.2 and 1.8 mm, respectively), but both sexes take off in a powerful jump. Using high-speed cameras, we analyzed the relationship between take-off kinematics and distance traveled through the air. We show that the velocity, acceleration and mass-specific power when leaving the ground places A. pseudococci among the most prominent jumpers of the insect world. However, the absolute distance moved through the air is modest compared with other jumping insects, as a result of air resistance acting on the small body. A biomechanical model suggests that air resistance reduces the jump distance of these insects by 49% compared with jumping in the absence of air resistance. The effect of air resistance is more pronounced in the smaller males, resulting in a segregation of the jumping performance between sexes. The limiting effect of air resistance is inversely proportional to body mass, seriously constraining jumping as a form of moving through the air in these and other small insects.

Allometry of wing twist and camber in a flower chafer during free flight: How do wing deformations scale with body size?

Intraspecific variation in adult body mass can be particularly high in some insect species, mandating adjustment of the wing's structural properties to support the weight of the larger body mass in air. Insect wings elastically deform during flapping, dynamically changing the twist and camber of the relatively thin and flat aerofoil. We examined how wing deformations during free flight scale with body mass within a species of rose chafers (Coleoptera: Protaetia cuprea) in which individuals varied more than threefold in body mass (0.38-1.29 g). Beetles taking off voluntarily were filmed using three high-speed cameras and the instantaneous deformation of their wings during the flapping cycle was analysed. Flapping frequency decreased in larger beetles but, otherwise, flapping kinematics remained similar in both small and large beetles. Deflection of the wing chord-wise varied along the span, with average deflections at the proximal trailing edge higher by 0.2 and 0.197 wing lengths compared to the distal trailing edge in the downstroke and the upstroke, respectively. These deflections scaled with wing chord to the power of 1.0, implying a constant twist and camber despite the variations in wing and body size. This suggests that the allometric growth in wing size includes adjustment of the flexural stiffness of the wing structure to preserve wing twist and camber during flapping.

The aerodynamics of flight in an insect flight-mill.

Predicting the dispersal of pest insects is important for pest management schemes. Flight-mills provide a simple way to evaluate the flight potential of insects, but there are several complications in relating tethered-flight to natural flight. We used high-speed video to evaluate the effect of flight-mill design on flight of the red palm weevil (Rynchophorous ferruginneus) in four variants of a flight-mill. Two variants had the rotating radial arm pivoted on the main shaft of the rotation axis, allowing freedom to elevate the arm as the insect applied lift force. Two other variants had the pivot point fixed, restricting the radial arm to horizontal motion. Beetles were tethered with their lateral axis horizontal or rotated by 40°, as in a banked turn. Flight-mill type did not affect flight speed or wing-beat frequency, but did affect flapping kinematics. The wingtip internal to the circular trajectory was always moved faster relative to air, suggesting that the beetles were attempting to steer in the opposite direction to the curved trajectory forced by the flight-mill. However, banked beetles had lower flapping asymmetry, generated higher lift forces and lost more of their body mass per time and distance flown during prolonged flight compared to beetles flying level. The results indicate, that flapping asymmetry and low lift can be rectified by tethering the beetle in a banked orientation, but the flight still does not correspond directly to free-flight. This should be recognized and taken into account when designing flight-mills and interoperating their data.

Effect of larval growth conditions on adult body mass and long-distance flight endurance in a wood-boring beetle: Do smaller beetles fly better?

The tropical fig borer, Batocera rufomaculata De Geer, is a large beetle that is a pest on a number of fruit trees, including fig and mango. Adults feed on the leaves and twigs and females lay their eggs under the bark of the tree. The larvae bore into the tree trunk, causing substantial damage that may lead to the collapse and death of the host tree. We studied how larval development under inferior feeding conditions (experienced during development in dying trees) affects flight endurance in the adult insect. We grew larvae either in their natural host or on sawdust enriched with stale fig tree twigs. Flight endurance of the adults was measured using a custom-built flight-mill. Beetles emerging from the natural host were significantly larger but flew shorter distances than beetles reared on less favourable substrates. There was no difference in the allometric slope of wing area with body mass between the beetles groups; however flight muscle mass scaled with total body mass with an exponent significantly lower than 1.0. Hence, smaller beetles had proportionally larger flight muscles. These findings suggest that beetles that developed smaller as a result from poor nutritional conditions in deteriorating hosts, are better equipped to fly longer distances in search of a new host tree.

Flying with eight wings: inter-sex differences in wingbeat kinematics and aerodynamics during the copulatory flight of damselflies (Ischnura elegans).

Copulation in the blue-tailed damselfly, Ischnura elegans, can last over 5 hours, during which the pair may fly from place to place in the so-called "wheel position". We filmed copulatory free-flight and analyzed the wingbeat kinematics of males and females in order to understand the contribution of the two sexes to this cooperative flight form. Both sexes flapped their wings but at different flapping frequencies resulting in a lack of synchronization between the flapping of the two insects. Despite their unusual body posture, females flapped their wings in a stroke-plane not significantly different to that of the males (repeated-measures ANOVA, F1,7 = 0.154, p = 0.71). However, their flapping amplitudes were smaller by 42 ± 17 %, compared to their male mates (t test, t 7 = 9.298, p < 0.001). This was mostly due to shortening of the amplitude at the ventral stroke reversal point. Compared to solitary flight, males flying in copula increased flapping frequency by 19 %, while females decreased flapping amplitude by 27 %. These findings suggest that although both sexes contribute to copulatory flight, females reduce their effort, while males increase their aerodynamic output in order to carry both their own weight and some of the female's weight. This increased investment by the male is amplified due to male I. elegans being typically smaller than females. The need by smaller males to fly while carrying some of the weight of their larger mates may pose a constraint on the ability of mating pairs to evade predators or counter interference from competing solitary males.

Whiteflies stabilize their take-off with closed wings.

The transition from ground to air in flying animals is often assisted by the legs pushing against the ground as the wings start to flap. Here, we show that when tiny whiteflies (Bemisia tabaci, body length ca. 1 mm) perform take-off jumps with closed wings, the abrupt push against the ground sends the insect into the air rotating forward in the sagittal (pitch) plane. However, in the air, B. tabaci can recover from this rotation remarkably fast (less than 11 ms), even before spreading its wings and flapping. The timing of body rotation in air, a simplified biomechanical model and take-off in insects with removed wings all suggest that the wings, resting backwards alongside the body, stabilize motion through air to prevent somersaulting. The increased aerodynamic force at the posterior tip of the body results in a pitching moment that stops body rotation. Wing deployment increases the pitching moment further, returning the body to a suitable angle for flight. This inherent stabilizing mechanism is made possible by the wing shape and size, in which half of the wing area is located behind the posterior tip of the abdomen.