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  1. 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$$\sim$$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.

     
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    Free, publicly-accessible full text available December 1, 2024
  2. ABSTRACT

    When designing experimental studies, it is important to understand the biological context of the question being asked. For example, many biological puncture experiments embed the puncture tool to a standardized depth based on a percentage of the total tool length, to compare the performance between tools. However, this may not always be biologically relevant to the question being asked. To understand how definitions of penetration depth may influence comparative results, we performed puncture experiments on a series of venomous snake fangs using the venom pore location as a functionally relevant depth standard. After exploring variation in pore placement across snake phylogeny, we compared the work expended during puncture experiments across a set of snake fangs using various depth standards: puncture initiation, penetration to a series of depths defined by the venom pore and penetration to 15% of fang length. Contrary to our hypothesis, we found almost no pattern in pore placement between clades, dietary groups or venom toxicity. Rank correlation statistics of our experimental energetics results showed no difference in the broad comparison of fangs when different puncture depth standards were used. However, pairwise comparisons between fangs showed major shifts in significance patterns between the different depth standards used. These results imply that the interpretation of experimental puncture data will heavily depend upon which depth standard is used during the experiments. Our results illustrate the importance of understanding the biological context of the question being addressed when designing comparative experiments.

     
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    Free, publicly-accessible full text available September 1, 2024
  3. 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. 
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  4. Abstract

    Phenotypic diversity is influenced by physical laws that govern how an organism's morphology relates to functional performance. To study comparative organismal biology, we need to quantify this diversity using biological traits (definable aspects of the morphology, behavior, and/or life history of an organism). Traits are often assumed to be immutable properties that need to be measured only a single time in each adult. However, organisms often experience changes in their biotic and abiotic environments that can alter trait function. In particular, structural traits represent the physical capabilities of an organism and may be heavily influenced by the rate at which they are exposed to physical demands (“loads”). For instance, materials tend to become more brittle when loaded at faster rates which could negatively affect structures trying to resist those loads (e.g., brittle materials are more likely to fracture). In the following perspective piece, we address the dynamic properties of structural traits and present case studies that demonstrate how dynamic strain rates affect the function of these traits in diverse groups of organisms. First, we review how strain rate affects deformation and fracture in biomaterials and demonstrate how these effects alter puncture mechanics in systems such as snake strikes. Second, we discuss how different rates of bone loading affect the locomotor biomechanics of vertebrates and their ecology. Through these examinations of diverse taxa and ecological functions, we aim to highlight how rate-dependent properties of structural traits can generate dynamic form–function relationships in response to changing environmental conditions. Findings from these studies serve as a foundation to develop more nuanced ecomechanical models that can predict how complex traits emerge and, thereby, advance progress on outlining the Rules of Life.

     
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  5. Abstract

    Muscle fatigue can reduce performance potentially affecting an organism's fitness. However, some aspects of fatigue could be overcome by employing a latch-mediated spring actuated (LaMSA) system where muscle activity is decoupled from movement. We estimated the effects of muscle fatigue on different aspects of mandible performance in six species of ants, two whose mandibles are directly actuated by muscles and four that have LaMSA “trap-jaw” mandibles. We found evidence that the LaMSA system of trap-jaw ants may prevent some aspects of performance from declining with repeated use, including duration, acceleration, and peak velocity. However, inter-strike interval increased with repeated strikes suggesting that muscle fatigue still comes into play during the spring loading phase. In contrast, one species with directly actuated mandibles showed a decline in bite force over time. These results have implications for design principles aimed at minimizing the effects of fatigue on performance in spring and motor actuated systems.

     
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  6. Synopsis

    We develop a model of latch-mediated spring actuated (LaMSA) systems relevant to comparative biomechanics and bioinspired design. The model contains five components: two motors (muscles), a spring, a latch, and a load mass. One motor loads the spring to store elastic energy and the second motor subsequently removes the latch, which releases the spring and causes movement of the load mass. We develop freely available software to accompany the model, which provides an extensible framework for simulating LaMSA systems. Output from the simulation includes information from the loading and release phases of motion, which can be used to calculate kinematic performance metrics that are important for biomechanical function. In parallel, we simulate a comparable, directly actuated system that uses the same motor and mass combinations as the LaMSA simulations. By rapidly iterating through biologically relevant input parameters to the model, simulated kinematic performance differences between LaMSA and directly actuated systems can be used to explore the evolutionary dynamics of biological LaMSA systems and uncover design principles for bioinspired LaMSA systems. As proof of principle of this concept, we compare a LaMSA simulation to a directly actuated simulation that includes either a Hill-type force-velocity trade-off or muscle activation dynamics, or both. For the biologically-relevant range of parameters explored, we find that the muscle force-velocity trade-off and muscle activation have similar effects on directly actuated performance. Including both of these dynamic muscle properties increases the accelerated mass range where a LaMSA system outperforms a directly actuated one.

     
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  7. ABSTRACT Some host species of avian obligate brood parasites reject parasitic eggs from their nest whereas others accept them, even though they recognize them as foreign. One hypothesis to explain this seemingly maladaptive behavior is that acceptors are unable to pierce and remove the parasitic eggshell. Previous studies reporting on the force and energy required to break brood parasites' eggshells were typically static tests performed against hard substrate surfaces. Here, we considered host nest as a substrate to simulate this potentially critical aspect of the natural context for egg puncture while testing the energy required to break avian eggshells. Specifically, as a proof of concept, we punctured domestic chicken eggs under a series of conditions: varying tool shape (sharp versus blunt), tool dynamics (static versus dynamic) and the presence of natural bird nests (of three host species). The results show a complex set of statistically significant interactions between tool shapes, puncture dynamics and nest substrates. Specifically, the energy required to break eggs was greater for the static tests than for the dynamic tests, but only when using a nest substrate and a blunt tool. In turn, in the static tests, the addition of a nest significantly increased energy requirements for both tool types, whereas during dynamic tests, the increase in energy associated with the nest presence was significant only when using the sharp tool. Characterizing the process of eggshell puncture in increasingly naturalistic contexts will help in understanding whether and how hosts of brood parasites evolve to reject foreign eggs. 
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  8. Synopsis The field of comparative biomechanics strives to understand the diversity of the biological world through the lens of physics. To accomplish this, researchers apply a variety of modeling approaches to explore the evolution of form and function ranging from basic lever models to intricate computer simulations. While advances in technology have allowed for increasing model complexity, insight can still be gained through the use of low-parameter “simple” models. All models, regardless of complexity, are simplifications of reality and must make assumptions; “simple” models just make more assumptions than complex ones. However, “simple” models have several advantages. They allow individual parameters to be isolated and tested systematically, can be made applicable to a wide range of organisms and make good starting points for comparative studies, allowing for complexity to be added as needed. To illustrate these ideas, we perform a case study on body form and center of mass stability in ants. Ants show a wide diversity of body forms, particularly in terms of the relative size of the head, petiole(s), and gaster (the latter two make-up the segments of the abdomen not fused to thorax in hymenopterans). We use a “simple” model to explore whether balance issues pertaining to the center of mass influence patterns of segment expansion across major ant clades. Results from phylogenetic comparative methods imply that the location of the center of mass in an ant’s body is under stabilizing selection, constraining the center of mass to the middle segment (thorax) over the legs. This is potentially maintained by correlated rates of evolution between the head and gaster on either end. While these patterns arise from a model that makes several assumptions/simplifications relating to shape and materials, they still offer intriguing insights into the body plan of ants across ∼68% of their diversity. The results from our case study illustrate how “simple,” low-parameter models both highlight fundamental biomechanical trends and aid in crystalizing specific questions and hypotheses for more complex models to address. 
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  9. Abstract

    An organism’s ability to control the timing and direction of energy flow both within its body and out to the surrounding environment is vital to maintaining proper function. When physically interacting with an external target, the mechanical energy applied by the organism can be transferred to the target as several types of output energy, such as target deformation, target fracture, or as a transfer of momentum. The particular function being performed will dictate which of these results is most adaptive to the organism. Chewing food favors fracture, whereas running favors the transfer of momentum from the appendages to the ground. Here, we explore the relationship between deformation, fracture, and momentum transfer in biological puncture systems. Puncture is a widespread behavior in biology requiring energy transfer into a target to allow fracture and subsequent insertion of the tool. Existing correlations between both tool shape and tool dynamics with puncture success do not account for what energy may be lost due to deformation and momentum transfer in biological systems. Using a combination of pendulum tests and particle tracking velocimetry (PTV), we explored the contributions of fracture, deformation and momentum to puncture events using a gaboon viper fang. Results on unrestrained targets illustrate that momentum transfer between tool and target, controlled by the relative masses of the two, can influence the extent of fracture achieved during high-speed puncture. PTV allowed us to quantify deformation throughout the target during puncture and tease apart how input energy is partitioned between deformation and fracture. The relationship between input energy, target deformation and target fracture is non-linear; increasing impact speed from 2.0 to 2.5 m/s created no further fracture, but did increase deformation while increasing speed to 3.0 m/s allowed an equivalent amount of fracture to be achieved for less overall deformation. These results point to a new framework for examining puncture systems, where the relative resistances to deformation, fracture and target movement dictate where energy flows during impact. Further developing these methods will allow researchers to quantify the energetics of puncture systems in a way that is comparable across a broad range of organisms and connect energy flow within an organism to how that energy is eventually transferred to the environment.

     
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