Mantises Exchange Angular Momentum between Three Rotating Body Parts to Jump Precisely to Targets

Flightless animals have evolved diverse mechanisms to control their movements in air, whether falling with gravity or propelling against it. Many insects jump as a primary mode of locomotion and must therefore precisely control the large torques generated during takeoff. For example, to minimize spin (angular momentum of the body) at takeoff, plant-sucking bugs apply large equal and opposite torques from two propulsive legs [1]. Interacting gear wheels have evolved in some to give precise synchronization of these legs [2, 3]. Once airborne, as a result of either jumping or falling, further adjustments may be needed to control trajectory and orient the body for landing. Tails are used by geckos to control pitch [4, 5] and by Anolis lizards to alter direction [6, 7]. When falling, cats rotate their body [8], while aphids [9] and ants [10, 11] manipulate wind resistance against their legs and thorax. Falling is always downward, but targeted jumping must achieve many possible desired trajectories. We show that when making targeted jumps, juvenile wingless mantises first rotated their abdomen about the thorax to adjust the center of mass and thus regulate spin at takeoff. Once airborne, they then smoothly and sequentially transferred angular momentum in four stages between the jointed abdomen, the two raptorial front legs, and the two propulsive hind legs to produce a controlled jump with a precise landing. Experimentally impairing abdominal movements reduced the overall rotation so that the mantis either failed to grasp the target or crashed into it head first.</p

Mantises Exchange Angular Momentum between Three Rotating Body Parts to Jump Precisely to Targets

Flightless animals have evolved diverse mechanisms to control their movements in air, whether falling with gravity or propelling against it. Many insects jump as a primary mode of locomotion and must therefore precisely control the large torques generated during takeoff. For example, to minimize spin (angular momentum of the body) at takeoff, plant-sucking bugs apply large equal and opposite torques from two propulsive legs [1]. Interacting gear wheels have evolved in some to give precise synchronization of these legs [2, 3]. Once airborne, as a result of either jumping or falling, further adjustments may be needed to control trajectory and orient the body for landing. Tails are used by geckos to control pitch [4, 5] and by Anolis lizards to alter direction [6, 7]. When falling, cats rotate their body [8], while aphids [9] and ants [10, 11] manipulate wind resistance against their legs and thorax. Falling is always downward, but targeted jumping must achieve many possible desired trajectories. We show that when making targeted jumps, juvenile wingless mantises first rotated their abdomen about the thorax to adjust the center of mass and thus regulate spin at takeoff. Once airborne, they then smoothly and sequentially transferred angular momentum in four stages between the jointed abdomen, the two raptorial front legs, and the two propulsive hind legs to produce a controlled jump with a precise landing. Experimentally impairing abdominal movements reduced the overall rotation so that the mantis either failed to grasp the target or crashed into it head first.</p

Compensatory plasticity at an identified synapse tunes a visuomotor pathway

We characterized homeostatic plasticity at an identified sensory-motor synapse in an insect, which maintains constant levels of motor drive as locusts transform from their solitarious phase to their gregarious swarming phase. The same mechanism produces behaviorally relevant changes in response timing that can be understood in the context of an animal's altered behavioral state. For individual animals of either phase, different looming objects elicited different spiking responses in a visual looming detector interneuron, descending contralateral movement detector (DCMD), yet its synaptic drive to a leg motoneuron, fast extensor tibiae (FETi), always had the same maximum amplitude. Gregarious locust DCMDs produced more action potentials and had higher firing frequencies, but individual postsynaptic potentials (PSPs) elicited in FETi were half the amplitude of those in solitarious locusts. A model suggested that this alone could not explain the similarity in overall amplitude, and we show that facilitation increased the maximum compound PSP amplitude in gregarious animals. There was the same linear relationship between times of peak DCMD firing before collision and the size/velocity of looming objects in both phases. The DCMD-FETi synapse transformed this relationship nonlinearly, such that peak amplitudes of compound PSPs occurred disproportionately earlier for smaller/faster objects. Furthermore, the peak PSP amplitude occurred earlier in gregarious than in solitarious locusts, indicating a differential tuning. Homeostatic modulation of the amplitude, together with a nonlinear synaptic transformation of timing, acted together to tune the DCMD-FETi system so that swarming gregarious locusts respond earlier to small moving objects, such as conspecifics, than solitarious locusts

RNAi of the elastomeric protein resilin reduces jump velocity and resilience to damage in locusts

Resilin, an elastomeric protein with remarkable physical properties that outperforms synthetic rubbers, is a near-ubiquitous feature of the power amplification mechanisms used by jumping insects. Catapult-like mechanisms, which incorporate elastic energy stores formed from a composite of stiff cuticle and resilin, are frequently used by insects to translate slow muscle contractions into rapid-release recoil movements. The precise role of resilin in these jumping mechanisms remains unclear, however. We used RNAi to reduce resilin deposition in the principal energy-storing springs of the desert locust (Schistocerca gregaria) before measuring jumping performance. Knockdown reduced the amount of resilin-associated fluorescence in the semilunar processes by 44% and reduced the cross-sectional area of the tendons of the hind leg extensor-tibiae muscle by 31%. This affected jumping in three ways: first, take-off velocity was reduced by 15% in knockdown animals, which could be explained by a change in the extrinsic stiffness of the extensor-tibiae tendon caused by the decrease in its cross-sectional area. Second, knockdown resulted in permanent breakages in the hind legs of 29% of knockdown locusts as tested by electrical stimulation of the extensor muscle, but none in controls. Third, knockdown locusts exhibited a greater decline in distance jumped when made to jump in rapid succession than did controls. We conclude that stiff cuticle acts as the principal elastic energy store for insect jumping, while resilin protects these more brittle structures against breakage from repeated use.</p

Transverse frozen sections from a series taken through the right half of the thorax of <i>Philaenus</i> at the planes indicated in <b>Figure 1D</b> and viewed from their anterior surfaces.

<p>Dorsal is to the top and ventral to the bottom of each image. A. Superimposed images of the same sections taken with UV and with bright field illumination. Intense blue fluorescence occurs in the pleural arch (energy store) within the thorax. Weaker blue fluorescence is present in the exoskeleton. B. The same sections in which antibody labelling is superimposed on the bright field image. The immuno-signal is restricted to the fluorescent regions with a much weaker signal in parts of the exoskeleton.</p

Combined fluorescence and antibody staining of the pleural arches (energy stores) in transverse sections of the thorax of <i>Delphacodes</i>.

<p>Combined images of bright field and UV fluorescence are shown on the left and of UV fluorescence and antibody labelling on the right.</p

Preadsorption controls to show the specificity of the antibody.

<p>A. Transverse section of the thorax of <i>Philaenus</i> illuminated with bright field and UV light. Blue fluorescence is restricted to the pleural arch (energy store). The large muscles that power depression of the hind legs in jumping occupy most of the volume of the thorax. B. Incubation in the antibody after preadsorption with the antigen now fails to label the pleural arch. Only some weak immunolabelling is still present in the exoskeleton.</p

Location of the thoracic energy stores in the pleural arch.

<p>A. Cartoon of the froghopper <i>Philaenus</i> as viewed from the side. B. Ventral view of the posterior part of the thorax of <i>Philaenus</i>. The right hind leg is shown partly depressed and the left hind leg levated with its femoro-tibial joint between the ventral surface of the body and the femur of the left middle leg, held as in preparation for a jump. C. Ventral view of the right half of the metathorax of <i>Philaenus</i> (area indicated by box in B) dissected to reveal the massive pleural arch (tinted grey-blue) which with its counterpart on the other side of the body forms the energy store for jumping. D. Photograph of a ventral view of the metathorax of <i>Delphacodes</i> in which images illuminated with white and UV light have been superimposed to show the blue fluorescence of the pleural arches. The horizontal lines indicate the region from which the transverse sections shown in subsequent figures were taken.</p

Data contact area Aphrodes platellae

Platellae contact area data from high-speed close-up recordings of the hind tarsi for 12 jumps of 5 Aphrodes leafhoppers

Data force measurements Philaenus and Aphrodes

Friction force data of the hind tarsi of 4 Aphrodes leafhoppers and 5 Philaenus froghoppers on glass