Muscle trade-offs in a power-amplified prey capture system

Should animals operating at great speeds and accelerations use fast or slow muscles? The answer hinges on a fundamental trade-off: muscles can be maximally fast or forceful, but not both. Direct lever systems offer a straightforward manifestation of this trade-off, yet the fastest organisms use power amplification, not direct lever action. Power-amplified systems typically use slow, forceful muscles to preload springs, which then rapidly release elastic potential energy to generate high speeds and accelerations. However, a fast response to a stimulus may necessitate fast spring-loading. Across 22 mantis shrimp species (Stomatopoda), this study examined how muscle anatomy correlates with spring mechanics and appendage type. We found that muscle force is maximized through physiological cross-sectional area, but not through sarcomere length. Sit-and-wait predators (spearers) had the shortest sarcomere lengths (fastest contractions) and the slowest strike speeds. The species that crush shells (smashers) had the fastest speeds, most forceful springs, and longest sarcomeres. The origin of the smasher clade yielded dazzlingly high accelerations, perhaps due to the release from fast spring-loading for evasive prey capture. This study offers a new window into the dynamics of force-speed trade-offs in muscles in the biomechanical, comparative evolutionary framework of power-amplified systems.