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ABSTRACT Hydrostatic skeletons, such as an elephant trunk or a squid tentacle, permit the transmission of mechanical work through a soft body. Despite the ubiquity of these structures among animals, we generally do not understand how differences in their morphology affect their ability to transmit muscular work. Therefore, the present study used mathematical modeling, morphometrics, and kinematics to understand the transmission of force and displacement in the tube feet of the juvenile six-rayed star (Leptasterias sp.). An inverse-dynamic analysis revealed that the forces generated by the feet during crawling primarily serve to overcome the submerged weight of the body. These forces were disproportionately generated by the feet at more proximal positions along each ray, which were used more frequently for crawling. Owing to a combination of mechanical advantage and muscle mass, these proximal feet exhibited a greater capacity for force generation than the distal feet. However, the higher displacement advantage of the more elongated distal feet offer a superior ability to extend the feet into the environment. Therefore, the morphology of tube feet demonstrates a gradient in gearing along each ray that compliments their role in behavior. 

A hydrostatic skeleton allows a soft body to transmit muscular force via internal pressure. A human's tongue, an octopus' arm and a nematode's body illustrate the pervasive presence of hydrostatic skeletons among animals, which has inspired the design of soft engineered actuators. However, there is a need for a theoretical basis for understanding how hydrostatic skeletons apply mechanical work. We therefore modeled the shape change and mechanics of natural and engineered hydrostatic skeletons to determine their mechanical advantage (MA) and displacement advantage (DA). These models apply to a variety of biological structures, but we explicitly consider the tube feet of a sea star and the body segments of an earthworm, and contrast them with a hydraulic press and a McKibben actuator. A helical winding of stiff, elastic fibers around these soft actuators plays a critical role in their mechanics by maintaining a cylindrical shape, distributing forces throughout the structure and storing elastic energy. In contrast to a single-joint lever system, soft hydrostats exhibit variable gearing with changes in MA generated by deformation in the skeleton. We found that this gearing is affected by the transmission efficiency of mechanical work (MA×DA) or, equivalently, the ratio of output to input work. The transmission efficiency changes with the capacity to store elastic energy within helically wrapped fibers or associated musculature. This modeling offers a conceptual basis for understanding the relationship between the morphology of hydrostatic skeletons and their mechanical performance. 

ABSTRACT Latch-mediated spring actuation (LaMSA) is used by small organisms to produce high acceleration movements. Mathematical models predict that acceleration increases as LaMSA systems decrease in size. Adult mantis shrimp use a LaMSA mechanism in their raptorial appendages to produce extremely fast strikes. Until now, however, it was unclear whether mantis shrimp at earlier life-history stages also strike using elastic recoil and latch mediation. We tested whether larval mantis shrimp (Gonodactylaceus falcatus) use LaMSA and, because of their smaller size, achieve higher strike accelerations than adults of other mantis shrimp species. Based on microscopy and kinematic analyses, we discovered that larval G. falcatus possess the components of, and actively use, LaMSA during their fourth larval stage, which is the stage of development when larvae begin feeding. Larvae performed strikes at high acceleration and speed (mean: 4.133×105 rad s−2, 292.7 rad s−1; 12 individuals, 25 strikes), which are of the same order of magnitude as for adults – even though adult appendages are up to two orders of magnitude longer. Larval strike speed (mean: 0.385 m s−1) exceeded the maximum swimming speed of similarly sized organisms from other species by several orders of magnitude. These findings establish the developmental timing and scaling of the mantis shrimp LaMSA mechanism and provide insights into the kinematic consequences of scaling limits in tiny elastic mechanisms.