Investigation of the rate-mediated form-function relationship in biological puncture.

Puncture is a vital mechanism for survival in a wide range of organisms across phyla, serving biological functions such as prey capture, defense, and reproduction. Understanding how the shape of the puncture tool affects its functional performance is crucial to uncovering the mechanics underlying the diversity and evolution of puncture-based systems. However, such form-function relationships are often complicated by the dynamic nature of living systems. Puncture systems in particular operate over a wide range of speeds to penetrate biological tissues. Current studies on puncture biomechanics lack systematic characterization of the complex, rate-mediated, interaction between tool and material across this dynamic range. To fill this knowledge gap, we establish a highly controlled experimental framework for dynamic puncture to investigate the relationship between the puncture performance (characterized by the depth of puncture) and the tool sharpness (characterized by the cusp angle) across a wide range of bio-relevant puncture speeds (from quasi-static to [Formula: see text] 50 m/s). Our results show that the sensitivity of puncture performance to variations in tool sharpness reduces at higher puncture speeds. This trend is likely due to rate-based viscoelastic and inertial effects arising from how materials respond to dynamic loads. The rate-dependent form-function relationship has important biological implications: While passive/low-speed puncture organisms likely rely heavily on sharp puncture tools to successfully penetrate and maintain functionalities, higher-speed puncture systems may allow for greater variability in puncture tool shape due to the relatively geometric-insensitive puncture performance, allowing for higher adaptability during the evolutionary process to other mechanical factors.