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ABSTRACT In aquatic species such as fish, the integumentary system, comprising skin and scales, serves as a crucial defense against puncture from high-velocity impacts. While previous studies have focused on quasistatic puncture behavior and constrained targets, here we investigated the less-studied dynamic puncture behavior in both constrained and unconstrained fish integument samples. We used cone snails as a model organism, which utilize a ballistic radular tooth to penetrate and paralyze prey. Our dynamic puncture experiments demonstrate that fish integument effectively mitigates damage from predatory mechanisms at biologically relevant speeds. While higher velocities typically result in deeper penetration, puncture performance is significantly reduced at lower speeds in unconstrained targets. These findings reveal the protective function and biomechanical efficiency of fish integument, with high puncture resistance attributed to material properties, momentum transfer and mobility. Our results highlight the adaptive strategies of cone snails in overcoming these defenses with greater velocity and energy. 

Genital spines are widespread in animals with internal fertilization, and their morphology is diverse. Many hypotheses have been proposed to explain their presence, yet their function has not been tested in most systems. We do not yet have a framework to characterize their morphology and potential function, even to determine if they puncture the vaginal tract (as is often assumed). Here, we examine the morphospace and puncturing ability of genital spines by testing different 3D-printed spines from a diverse sample of μCT-scanned snake hemipenes, which are among the most morphologically variable intromittent genitalia in vertebrates. We performed serial compression tests into polydimethylsiloxane silicone polymer at increments of 10° until puncture was impossible. We found that the range of successful puncture angles differed based on spine curvature and tip sharpness, suggesting that some spines are built to puncture at almost every angle of approach, while others are extremely unlikely to puncture vaginal tissues at all. These results provide a framework for continued study and characterization of the shape and performance of genital spines in other animal groups and help to refine functional hypotheses in the context of copulatory interactions. 

The integumentary system in animals serves as an important line of defence against physiological and mechanical external forces. Over time, integuments have evolved layered structures (scales, cuticle and skin) with high toughness and strength to resist damage and prevent wound expansion. While previous studies have examined their defensive performance under low-rate conditions, the failure response and damage resistance of these thin layers under dynamic biological puncture remain underexplored. Here, we utilize a novel experimental framework to investigate the mechanics of dynamic puncture in both bilayer structures of synthetic tissue-mimicking composite materials and natural skin tissues. Our findings reveal the remarkable efficiency of a thin outer skin layer in reducing the overall extent of dynamic puncture damage. This enhanced damage resistance is governed by interlayer properties through puncture energetics and diminishes in strength at higher puncture rates due to rate-dependent effects in silicone tissue simulants. In addition, natural skin tissues exhibit unique material properties and failure behaviours, leading to superior damage reduction capability compared with synthetic counterparts. These findings contribute to a deeper understanding of the inherent biomechanical complexity of biological puncture systems with layered composite material structures. They lay the groundwork for future comparative studies and bio-inspired applications. 

Living organisms have evolved various biological puncture tools, such as fangs, stingers, and claws, for prey capture, defense, and other critical biological functions. These tools exhibit diverse morphologies, including a wide range of structural curvatures, from straight cactus spines to crescent-shaped talons found in raptors. While the influence of such curvature on the strength of the tool has been explored, its biomechanical role in puncture performance remains untested. Here, we investigate the effect of curvature on puncture mechanics by integrating experiments with finite element simulations. Our findings reveal that within a wide biologically relevant range, structural curvature has a minimal impact on key metrics of damage initiation or the energies required for deep penetration in isotropic and homogeneous target materials. This unexpected result improves our understanding of the biomechanical pressures driving the morphological diversity of curved puncture tools and provides fundamental insights into the crucial roles of curvature in the biomechanical functions of living puncture systems. 

Abstract 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$$\sim$$ $\sim$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. 

Biological puncture systems use a diversity of morphological tools (stingers, teeth, spines etc.) to penetrate target tissues for a variety of functions (prey capture, defence, reproduction). These systems are united by a set of underlying physical rules which dictate their mechanics. While previous studies have illustrated form–function relationships in individual systems, these underlying rules have not been formalized. We present a mathematical model for biological puncture events based on energy balance that allows for the derivation of analytical scaling relations between energy expenditure and shape, size and material response. The model identifies three necessary energy contributions during puncture: fracture creation, elastic deformation of the material and overcoming friction during penetration. The theoretical predictions are verified using finite-element analyses and experimental tests. Comparison between different scaling relationships leads to a ratio of released fracture energy and deformation energy contributions acting as a measure of puncture efficiency for a system that incorporates both tool shape and material response. The model represents a framework for exploring the diversity of biological puncture systems in a rigorous fashion and allows future work to examine how fundamental physical laws influence the evolution of these systems.