Vertical leaping mechanics of the Lesser Egyptian Jerboa reveal specialization for maneuverability rather than elastic energy storage

Abstract

BackgroundNumerous historical descriptions of the Lesser Egyptian jerboa, Jaculus jaculus, a small bipedal mammal with elongate hindlimbs, make special note of their extraordinary leaping ability. We observed jerboa locomotion in a laboratory setting and performed inverse dynamics analysis to understand how this small rodent generates such impressive leaps. We combined kinematic data from video, kinetic data from a force platform, and morphometric data from dissections to calculate the relative contributions of each hindlimb muscle and tendon to the total movement.ResultsJerboas leapt in excess of 10 times their hip height. At the maximum recorded leap height (not the maximum observed leap height), peak moments for metatarso-phalangeal, ankle, knee, and hip joints were 13.1, 58.4, 65.1, and 66.9 Nmm, respectively. Muscles acting at the ankle joint contributed the most work (mean 231.6 mJ / kg Body Mass) to produce the energy of vertical leaping, while muscles acting at the metatarso-phalangeal joint produced the most stress (peak 317.1 kPa). The plantaris, digital flexors, and gastrocnemius tendons encountered peak stresses of 25.6, 19.1, and 6.0 MPa, respectively, transmitting the forces of their corresponding muscles (peak force 3.3, 2.0, and 3.8 N, respectively). Notably, we found that the mean elastic energy recovered in the primary tendons of both hindlimbs comprised on average only 4.4% of the energy of the associated leap.ConclusionsThe limited use of tendon elastic energy storage in the jerboa parallels the morphologically similar heteromyid kangaroo rat, Dipodomys spectabilis. When compared to larger saltatory kangaroos and wallabies that sustain hopping over longer periods of time, these small saltatory rodents store and recover less elastic strain energy in their tendons. The large contribution of muscle work, rather than elastic strain energy, to the vertical leap suggests that the fitness benefit of rapid acceleration for predator avoidance dominated over the need to enhance locomotor economy in the evolutionary history of jerboas.Electronic supplementary materialThe online version of this article (doi:10.1186/s12983-017-0215-z) contains supplementary material, which is available to authorized users.

Why do mammals hop? Understanding the ecology, biomechanics and evolution of bipedal hopping

“…In a recent study of desert kangaroo rats, we showed that while the majority of mechanical work for vertical jumping is delivered at the ankle, approximately 40% of this energy is transferred from proximal muscles (Schwaner et al, 2017), and in a previous study we showed that proximal to distal energy transfer also likely plays an important role in horizontal accelerations by tammar wallabies (McGowan et al, 2005b). The ratio of the moment arms of the ankle extensors at the ankle and knee is approximately 2:1 and is remarkably similar in macropods and bipedal rodents (Alexander and Vernon, 1975;Moore et al, 2017b;Rankin et al, 2018). If the ankle extensor muscle-tendon unit were to act exclusively as a strut, a 4-bar linkage would be created and any torque generated at the knee would be doubled at the ankle.…”

“…A rapid vertical or lateral leap, followed by aerial reorientation, to evade the ballistic strike of a predator is likely under strong selective pressure in many small bipedal hoppers. The morphological adaptions of the hindlimbs are well suited for generating the rapid accelerations and high mechanical power output needed to produce the extreme jumping performance seen in many species, with jumps often reaching as high as 10 times the animal's hip height (Bartholomew and Caswell, 1951;Moore et al, 2017b;Schwaner et al, 2017). The elongated hindlimbs of bipedal hoppers enable them to accelerate the body over longer periods of time (Alexander, 1995), and hoppers tend to have substantially more hindlimb muscle mass relative to similarly sized quadrupeds (Berman, 1980;Grand, 1990).…”

“…For example, during steady-speed hopping, 0.1 kg kangaroo rats operate with relatively high tendon safety factors of ∼10 , whereas kangaroos and wallabies operate with safety factors of 3 or less (Alexander and Vernon, 1975;Biewener, 1998;McGowan et al, 2008b). However, during vertical jumping, the stresses placed on the tendons are significantly higher, and tendon safety factors may drop to as low as 2 in jerboas and kangaroo rats Moore et al, 2017b;Schwaner et al, 2017). And although tendon stress may limit the acceleration capacity of kangaroos (Biewener and Bertram, 1991), relatively large yellow-footed rock wallabies (Petrogale xanthopus, ∼5 kg) are capable of extremely high-powered jumps (McGowan et al, 2005a).…”

“…Another interesting feature of the hindlimb musculoskeletal anatomy of bipedal hoppers is that all the primary ankle extensor muscles (i.e. gastrocnemii, plantaris) are biarticular, and the uniarticular soleus muscle is vestigial (Alexander and Vernon, 1975;Berman, 1980;Moore et al, 2017b;Rankin et al, 2018). This biarticularity creates a direct linkage between the powerful proximal muscles and the distal limb joints where external mechanical work is typically done.…”

Evolutionary loss of foot muscle during development with characteristics of atrophy and no evidence of cell death

“…Muscle is not required for autopod tendon formation or maintenance in mice, but the tendons that develop in a muscleless or a paralyzed mouse are thinner and less well organized (Huang et al, 2015). It is 405 therefore possible that muscle is initially required in the fetus and neonate for tendons to establish sufficient architecture from origin to insertion so that the tendon, after further growth, can withstand high locomotor forces in the adult (Lochner et al, 1980;Moore et al, 2017).…”