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.

Effect of Substrates' Compliance on the Jumping Mechanism of Locusta migratoria

“…To better understand, Figure 6 provides some schematic representations of locusts' anatomy and cinematic. In particular, Figure 6A (Rogers et al, 2016) shows a representation of the internal anatomy of a hind femur, characterized by a massive, pennate extensor tibiae muscle and a very small flexor tibiae FIGURE 6 | (A) Mechanical diagram of the interactions between the extensor tibiae muscle, its apodeme and the semilunar processes: during the contraction just before jumping, the apodeme pulls on and distorts the front part of the femoro-tibial joint, bending the semi-lunar processes (Rogers et al, 2016); (B) configuration's variation from the steady stare to the jumping state (Rogers et al, 2016); (C) theoretical model of locust jumping cinematics (Mo et al, 2019); (D) lumped parameter model of muscles' arrangement in locust jump (Rogers et al, 2016). muscle, while Figure 6B (Rogers et al, 2016) shows how the leg configuration varies from the steady phase to the jumping phase.…”

“…In particular, Figure 6A (Rogers et al, 2016) shows a representation of the internal anatomy of a hind femur, characterized by a massive, pennate extensor tibiae muscle and a very small flexor tibiae FIGURE 6 | (A) Mechanical diagram of the interactions between the extensor tibiae muscle, its apodeme and the semilunar processes: during the contraction just before jumping, the apodeme pulls on and distorts the front part of the femoro-tibial joint, bending the semi-lunar processes (Rogers et al, 2016); (B) configuration's variation from the steady stare to the jumping state (Rogers et al, 2016); (C) theoretical model of locust jumping cinematics (Mo et al, 2019); (D) lumped parameter model of muscles' arrangement in locust jump (Rogers et al, 2016). muscle, while Figure 6B (Rogers et al, 2016) shows how the leg configuration varies from the steady phase to the jumping phase. Figure 6C (Mo et al, 2019) represents a theoretical model of locust jumping cinematic: the body is simplified as rigid; the centroid is located in point S; femur is connected with the body by means of joint C. Femur and tibiae were simplified as rigid bars and the knee joint was simplified as hinge B. Tarsus and ground are simplified as one part and the joint between tarsus and tibiae is simplified as hinge A. θ 1 , θ 2 , θ 3 represent the angles between the links separately, l 1 , l 2 , l 3 represent the length of femur bar AB, tibiae bar BC and the length between point C and centroid S, respectively.…”

“…The pattern for jumping in animals that exploit catapult mechanism always present two fundamental phases: in the first phase elastic energy is accumulated in the muscle fibers; in the second phase the elastic energy is explosively released to power the jump. In the specific case of locusts ( Figure 6 ), the jumping motor pattern consists of three phases (Rogers et al, 2016 ): the cocking phase, the co-contraction phase and the jump phase (or triggering phase). During the cocking phase, the hind tibiae are totally flexed and blocked into position against the hind femora.…”

Impact of Different Developmental Instars onLocusta migratoriaJumping Performance

“…A sharp improvement of velocity and energy in adults is reported to be a result of the combination of a bigger mean crosssectional area of the femur muscle [28,63,64] coupled with the fact that a rather long life span gives adult locusts longer time to stiffen their semilunar process and extensor cuticle [27,32,40,65,66]. A stiffer spring system in adults was also estimated by the abovementioned modeling, where the elasticity of the hind legs of locusts was supposed to be modeled as a torsional spring located at the femur-tibiae joint [56], neglecting other elastic contributions [67,68]. The results showed that the stiffness of fourth instar and third instar locusts are close, and rather smaller than that of adults, differing by orders of magnitude.…”

JumpDetector: An automated monitoring equipment for the locomotion of jumping insects

“…Jumping is the main form of locomotion for juvenile locusts with low power output and high endurance as a marathoner (Kirkton & Harrison, ). The difference of velocity performance in a single jump has been reported between solitary and gregarious locusts (Rogers et al ., ). The properties, kinematics, influencing factors, and related physiological mechanisms of the locusts’ jumping behavior have been extensively investigated (Bennet‐Clark, ; Snelling et al ., ; Beck et al ., ) by using various manual methods or traditional observations.…”