Scaling and development of elastic mechanisms: the tiny strikes of larval mantis shrimp

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.

Methods
Larval mantis shrimp raptorial appendage strikes were collected using high speed video (20,000 frames s-1; 25 strikes, 12 individuals, 1-6 strikes per individual). Kinematics were determined by manually tracking the raptorial appendage over the course of a strike using MTrackJ plug-in (V1.5.1, Meijering et al., 2012) in ImageJ (v2.0.0, Schneider et al, 2012). Strike kinematics (angular and linear velocity and acceleration) were compared to a previously compiled dataset of adult mantis shrimp strike kinematics (McHenry et al., 2016). The speed of the larval mantis shrimp strike was compared to a newly compiled dataset collected from the literature of swimming and feeding speeds from other larval aquatic organisms.