G. P. Sutton

Resilin and chitinous cuticle form a composite structure for energy storage in jumping by froghopper insects

BackgroundMany insects jump by storing and releasing energy in elastic structures within their bodies. This allows them to release large amounts of energy in a very short time to jump at very high speeds. The fastest of the insect jumpers, the froghopper, uses a catapult-like elastic mechanism to achieve their jumping prowess in which energy, generated by the slow contraction of muscles, is released suddenly to power rapid and synchronous movements of the hind legs. How is this energy stored?ResultsThe hind coxae of the froghopper are linked to the hinges of the ipsilateral hind wings by pleural arches, complex bow-shaped internal skeletal structures. They are built of chitinous cuticle and the rubber-like protein, resilin, which fluoresces bright blue when illuminated with ultra-violet light. The ventral and posterior end of this fluorescent region forms the thoracic part of the pivot with a hind coxa. No other structures in the thorax or hind legs show this blue fluorescence and it is not found in larvae which do not jump. Stimulating one trochanteral depressor muscle in a pattern that simulates its normal action, results in a distortion and forward movement of the posterior part of a pleural arch by 40 μm, but in natural jumping, the movement is at least 100 μm.ConclusionCalculations showed that the resilin itself could only store 1% to 2% of the energy required for jumping. The stiffer cuticular parts of the pleural arches could, however, easily meet all the energy storage needs. The composite structure therefore, combines the stiffness of the chitinous cuticle with the elasticity of resilin. Muscle contractions bend the chitinous cuticle with little deformation and therefore, store the energy needed for jumping, while the resilin rapidly returns its stored energy and thus restores the body to its original shape after a jump and allows repeated jumping.

The mechanics of elevation control in locust jumping

How do animals control the trajectory of ballistic motions like jumping? Targeted jumps by a locust, which are powered by a rapid extension of the tibiae of both hind legs, require control of the take-off angle and speed. To determine how the locust controls these parameters, we used high speed images of jumps and mechanical analysis to reach three conclusions: (1) the extensor tibiae muscle applies equal and opposite torques to the femur and tibia, which ensures that tibial extension accelerates the centre of mass of the body along a straight line; (2) this line is parallel to a line drawn from the distal end of the tibia through the proximal end of the femur; (3) the slope of this line (the angle of elevation) is not affected if the two hind legs extend asynchronously. The mechanics thus uncouple the control of elevation and speed, allowing simplified and independent control mechanisms. Jump elevation is controlled mechanically by the initial positions of the hind legs and jump speed is determined by the energy stored within their elastic processes, which allows us to then propose which proprioceptors are involved in controlling these quantities.

Interacting Gears Synchronize Propulsive Leg Movements in a Jumping Insect

Joint Action Many small insects are impressive jumpers, but large leaps and small bodies pose biomechanical challenges. Burrows and Sutton (p. 1254) show that the nymphal planthopper Issus has interlocking gears on their hindleg trochanters that act together to cock the legs synchronously before triggering forward jumps. At the final molt, the gears are swapped for a high-performance friction-based mechanism because the risk of breaking a gear is high, the options for repair during molting are gone, and, moreover, the animal is bigger and stronger. Functional gears are involved in the ballistic jumping movements of the flightless planthopper insect, Issus. Gears are found rarely in animals and have never been reported to intermesh and rotate functionally like mechanical gears. We now demonstrate functional gears in the ballistic jumping movements of the flightless planthopper insect Issus. The nymphs, but not adults, have a row of cuticular gear (cog) teeth around the curved medial surfaces of their two hindleg trochantera. The gear teeth on one trochanter engaged with and sequentially moved past those on the other trochanter during the preparatory cocking and the propulsive phases of jumping. Close registration between the gears ensured that both hindlegs moved at the same angular velocities to propel the body without yaw rotation. At the final molt to adulthood, this synchronization mechanism is jettisoned.

The effect of leg length on jumping performance of short- and long-legged leafhopper insects.

SUMMARY To assess the effect of leg length on jumping ability in small insects, the jumping movements and performance of a sub-family of leafhopper insects (Hemiptera, Auchenorrhyncha, Cicadellidae, Ulopinae) with short hind legs were analysed and compared with other long-legged cicadellids (Hemiptera, Auchenorrhyncha, Cicadellidae). Two species with the same jumping characteristics but distinctively different body shapes were analysed: Ulopa, which had an average body length of 3 mm and was squat, and Cephalelus, which had an average body length of 13 mm with an elongated body and head. In both, the hind legs were only 1.4 times longer than the front legs compared with 1.9–2.3 times in other cicadellid leafhoppers. When the length of the hind legs was normalised relative to the cube root of their body mass, their hind legs had a value of 1–1.1 compared with 1.6–2.3 in other cicadellids. The hind legs of Cephalelus were only 20% of the body length. The propulsion for a jump was delivered by rapid and synchronous rotation of the hind legs about their coxo-trochanteral joints in a three-phase movement, as revealed by high-speed sequences of images captured at rates of 5000 s–1. The hind tarsi were initially placed outside the lateral margins of the body and not apposed to each other beneath the body as in long-legged leafhoppers. The hind legs were accelerated in 1.5 ms (Ulopa) and 2 ms (Cephalelus) and thus more quickly than in the long-legged cicadellids. In their best jumps these movements propelled Ulopa to a take-off velocity of 2.3 m s–1 and Cephalelus to 2 m s–1, which matches that of the long-legged cicadellids. Both short-legged species had the same mean take-off angle of 56° but Cephalelus adopted a lower angle of the body relative to the ground (mean 15°) than Ulopa (mean 56°). Once airborne, Cephalelus pitched slowly and rolled quickly about its long axis and Ulopa rotated quickly about both axes. To achieve their best performances Ulopa expended 7 μJ of energy, generated a power output of 7 mW, and exerted a force of 6 mN; Cephalelus expended 23μ J of energy, generated a power output of 12 mW and exerted a force of 11 mN. There was no correlation between leg length and take-off velocity in the long- and short-legged species, but longer legged leafhoppers had longer take-off times and generated lower ground reaction forces than short-legged leafhoppers, possibly allowing the longer legged leafhoppers to jump from less stiff substrates.

Locusts use a composite of resilin and hard cuticle as an energy store for jumping and kicking

SUMMARY Locusts jump and kick by using a catapult mechanism in which energy is first stored and then rapidly released to extend the large hind legs. The power is produced by a slow contraction of large muscles in the hind femora that bend paired semi-lunar processes in the distal part of each femur and store half the energy needed for a kick. We now show that these energy storage devices are composites of hard cuticle and the rubber-like protein resilin. The inside surface of a semi-lunar process consists of a layer of resilin, particularly thick along an inwardly pointing ridge and tightly bonded to the external, black cuticle. From the outside, resilin is visible only as a distal and ventral triangular area that tapers proximally. High-speed imaging showed that the semi-lunar processes were bent in all three dimensions during the prolonged muscular contractions that precede a kick. To reproduce these bending movements, the extensor tibiae muscle was stimulated electrically in a pattern that mimicked the normal sequence of its fast motor spikes recorded in natural kicking. Externally visible resilin was compressed and wrinkled as a semi-lunar process was bent. It then sprung back to restore the semi-lunar process rapidly to its original natural shape. Each of the five nymphal stages jumped and kicked and had a similar distribution of resilin in their semi-lunar processes as adults; the resilin was shed with the cuticle at each moult. It is suggested that composite storage devices that combine the elastic properties of resilin with the stiffness of hard cuticle allow energy to be stored by bending hard cuticle over only a small distance and without fracturing. In this way all the stored energy is returned and the natural shape of the femur is restored rapidly so that a jump or kick can be repeated.

A buckling region in locust hindlegs contains resilin and absorbs energy when jumping or kicking goes wrong

SUMMARY If a hindleg of a locust slips during jumping, or misses its target during kicking, energy generated by the two extensor tibiae muscles is no longer expended in raising the body or striking a target. How, then, is the energy in a jump (4100–4800 μJ) or kick (1700 μJ) dissipated? A specialised buckling region found in the proximal hind-tibia where the bending moment is high, but not present in the other legs, buckled and allowed the distal part of the tibia to extend. In jumps when a hindleg slipped, it bent by a mean of 23±14 deg at a velocity of 13.4±9.5 deg ms–1; in kicks that failed to contact a target it bent by 32±16 deg at a velocity of 32.9±9.5 deg ms–1. It also buckled 8.5±4.0 deg at a rate of 0.063±0.005 deg ms–1 when the tibia was prevented from flexing fully about the femur in preparation for both these movements. By experimentally buckling this region through 40 deg at velocities of 0.001–0.65 deg ms–1, we showed that one hindleg could store about 870 μJ on bending, of which 210 μJ was dissipated back to the leg on release. A band of blue fluorescence was revealed at the buckling region under UV illumination that had the two key signatures of the elastic protein resilin. A group of campaniform sensilla 300 μm proximal to the buckling region responded to imposed buckling movements. The features of the buckling region show that it can act as a shock absorber as proposed previously when jumping and kicking movements go wrong.

The mechanics of azimuth control in jumping by froghopper insects

SUMMARY Many animals move so fast that there is no time for sensory feedback to correct possible errors. The biomechanics of the limbs participating in such movements appear to be configured to simplify neural control. To test this general principle, we analysed how froghopper insects control the azimuth direction of their rapid jumps, using high speed video of the natural movements and modelling to understand the mechanics of the hind legs. We show that froghoppers control azimuth by altering the initial orientation of the hind tibiae; their mean angle relative to the midline closely predicts the take-off azimuth. This applies to jumps powered by both hind legs, or by one hind leg. Modelling suggests that moving the two hind legs at different times relative to each other could also control azimuth, but measurements of natural jumping showed that the movements of the hind legs were synchronised to within 32 μs of each other. The maximum timing difference observed (67 μs) would only allow control of azimuth over 0.4 deg. to either side of the midline. Increasing the timing differences between the hind legs is also energetically inefficient because it decreases the energy available and causes losses of energy to body spin; froghoppers with just one hind leg spin six times faster than intact ones. Take-off velocities also fall. The mechanism of azimuth control results from the mechanics of the hind legs and the resulting force vectors of their tibiae. This enables froghoppers to have a simple transform between initial body position and motion trajectory, therefore potentially simplifying neural control.

Pygmy mole crickets jump from water

Summary Animals that live or repeatedly alight on the surface of water often need to escape from predators or return to land. We show that flightless pygmy mole crickets use a new strategy to jump rapidly from water. Their powerful hind legs are moved so quickly that they penetrate the surface and as they move through the water, unique arrays of spring-loaded paddles and spurs fan out to increase surface area. This enables these insects to propel a large volume of water downwards in a laminar flow, so that they are launched upwards into the air.

Increased muscular volume and cuticular specialisations enhance jump velocity in solitarious compared with gregarious desert locusts, Schistocerca gregaria.

ABSTRACT The desert locust, Schistocerca gregaria, shows a strong phenotypic plasticity. It can develop, depending upon population density, into either a solitarious or gregarious phase that differs in many aspects of behaviour, physiology and morphology. Prominent amongst these differences is that solitarious locusts have proportionately longer hind femora than gregarious locusts. The hind femora contain the muscles and energy-storing cuticular structures that propel powerful jumps using a catapult-like mechanism. We show that solitarious locusts jump on average 23% faster and 27% further than gregarious locusts, and attribute this improved performance to three sources: first, a 17.5% increase in the relative volume of their hind femur, and hence muscle volume; second, a 24.3% decrease in the stiffness of the energy-storing semi-lunar processes of the distal femur; and third, a 4.5% decrease in the stiffness of the tendon of the extensor tibiae muscle. These differences mean that solitarious locusts can generate more power and store more energy in preparation for a jump than can gregarious locusts. This improved performance comes at a cost: solitarious locusts expend nearly twice the energy of gregarious locusts during a single jump and the muscular co-contraction that energises the cuticular springs takes twice as long. There is thus a trade-off between achieving maximum jump velocity in the solitarious phase against the ability to engage jumping rapidly and repeatedly in the gregarious phase. Highlighted Article: Larger muscles and more elastic cuticular springs allow solitarious locusts to jump 25% faster than gregarious locusts, but they require double the energy and time to operate the spring mechanism.

Biomechanics: An Army Marching with Its Stomach

A novel X-ray technique shows that the internal organs of crawling caterpillars slide past the body walls like pistons in a new kind of legged locomotion.