Muscle tradeoffs 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 tradeoff: muscles can be maximally fast or forceful, but not both. Direct lever systems offer a straightforward manifestation of this tradeoff, yet the fastest organisms use power amplification, not direct lever action. Power-amplified systems typically use slow, forceful muscles to pre-load 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 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 tradeoffs in muscles in the biomechanical, comparative evolutionary framework of power-amplified systems.

以极高速度与加速度运动的动物，应当选用快肌还是慢肌？这一问题的答案取决于一项根本性的权衡：肌肉无法同时实现极致的速度与力量，只能二者择一。直接杠杆系统是这种权衡关系的直观体现，但运动速度最快的生物并非采用直接杠杆机制，而是通过功率放大系统实现运动。功率放大系统通常借助收缩缓慢但力量强劲的肌肉对弹性结构进行预加载，随后快速释放弹性势能以产生极高的速度与加速度。然而，若要对刺激做出快速响应，则可能需要快速完成弹性结构的预加载过程。本研究以22种螳螂虾（Stomatopoda）为研究对象，探讨了肌肉解剖结构与弹性结构力学特性及附肢类型之间的关联。本研究发现，肌肉力量可通过生理横截面积实现最大化，但无法通过肌节（sarcomere）长度达成。伏击型捕食者的肌节长度最短（收缩速度最快），但其攻击速度却最为缓慢。以粉碎外壳为捕食方式的物种（“粉碎型”），则拥有最快的攻击速度、力量最强的弹性结构以及最长的肌节。粉碎型演化支的起源催生了令人惊叹的高加速度，这或许是因为其摆脱了为捕获逃逸猎物而需快速完成弹性预加载的约束。本研究在功率放大系统的生物力学与比较演化框架下，为肌肉力量-速度权衡的动态机制提供了全新的研究视角。