Quality vs. Quantity: the Consequences of Elevated CO2 on Wood Biomaterial Properties.

Since the late 1800s, anthropogenic activities such as fossil fuel consumption and deforestation have driven up the concentration of atmospheric CO2 around the globe by more than 45%. Such heightened concentrations of carbon dioxide in the atmosphere are a leading contributor to global climate change with estimates of a 2-5 degree increase in global air temperature by the end of the century. While such climatic changes are mostly considered detrimental, a great deal of experimental work has shown that increased atmospheric CO2 will actually increase growth in various plants, which may lead to increased biomass for potential harvesting or CO2 sequestration. However, it is not clear whether this increase in growth or biomass will be beneficial to the plants, as such increases may lead to weaker plant materials. In this review, I examine our current understanding of how elevated atmospheric CO2 caused by anthropogenic effects may influence plant material properties focusing on potential effects on wood. For the first part of the review, I explore how aspects of wood anatomy and structure influence resistance to bending and breakage. This information is then used to review how changes in CO2 levels may later these aspects of wood anatomy and structure in ways that have mechanical consequences. The major pattern that emerges is that the consequences of elevated CO2 on wood properties is highly dependent on species, and environment, with different tree species showing contradictory responses to atmospheric changes. In the end, I describe a couple avenues for future research into better understanding the influence of atmospheric CO2 levels on plant biomaterial mechanics.

How venom pore placement may influence puncture performance in snake fangs.

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.

Morphological variation in the vomer of aquatic and terrestrial spelerpini salamanders.

The vomer is an important tooth-bearing cranial bone in the lungless salamanders (Caudata: Plethodontidae) that serves different functional roles in aquatic versus terrestrial feeding. Vomerine tooth rows that run parallel with the maxillary teeth are thought to help grasp prey while expelling water from the mouth, while posterior extensions of the tooth row may help terrestrial taxa bring prey down the throat. We hypothesize that these two general morphological types will correlate with the habitat (aquatic vs. terrestrial) of adult salamanders. Alternatively, variation in form may be due to taxonomic effects, such that closely related species will have similar vomer morphology regardless of adult habitat. To test this hypothesis, we examined vomer shape on a set of species of the morphologically diverse tribe Spelerpini, in which two of the five genera (Eurycea and Gyrinophilus) include both aquatic and terrestrial species. Data were collected using micro computed tomography (micro-CT) scans from specimens from the Field Museum of Natural History and the Illinois Natural History Survey; additional data was obtained from public online repositories including Morphosource.org. Two-dimensional geometric morphometric analyses were performed to capture shape variation of both the vomer and the vomerine tooth row. We found clear separation between aquatic and terrestrial taxa, with most of the variation due to differences in the vomerine tooth row. Differences ascribed to habitat use likely correspond to feeding behavior, and the functional role of the vomer in prey processing warrants further investigation in this species-rich salamander family.

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.

Modelling biological puncture: a mathematical framework for determining the energetics and scaling.

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.

A Tunable, Simplified Model for Biological Latch Mediated Spring Actuated Systems.

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.

Shifts in morphological covariation and evolutionary rates across multiple acquisitions of the trap-jaw mechanism in Strumigenys.

A long-standing question in comparative biology is how the evolution of biomechanical systems influences morphological evolution. The need for functional fidelity implies that the evolution of such systems should be associated with tighter morphological covariation, which may promote or dampen rates of morphological evolution. I examine this question across multiple evolutionary origins of the trap-jaw mechanism in the genus Strumigenys. Trap-jaw ants have latch-mediated, spring-actuated systems that amplify the power output of their mandibles. I use Bayesian estimates of covariation and evolutionary rates to test the hypotheses that the evolution of this high-performance system is associated with tighter morphological covariation in the head and mandibles relative to nontrap-jaw forms and that this leads to shifts in rates of morphological evolution. Contrary to these hypotheses, there is no evidence of a large-scale shift to higher covariation in trap-jaw forms, while different traits show both increased and decreased evolutionary rates between forms. These patterns may be indicative of many-to-one mapping and/or mechanical sensitivity in the trap-jaw LaMSA system. Overall, it appears that the evolution of trap-jaw forms in Strumigenys did not require a correlated increase in morphological covariation, partly explaining the proclivity with which the system has evolved.

Muscle fatigue in the latch-mediated spring actuated mandibles of trap-jaw ants.

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 system (LaMSA) 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.

Different traits at different rates: The effects of dynamic strain rate on structural traits in biology.

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 only be measured 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.

Increasing morphological disparity and decreasing optimality for jaw speed and strength during the radiation of jawed vertebrates.

The Siluro-Devonian adaptive radiation of jawed vertebrates, which underpins almost all living vertebrate biodiversity, is characterized by the evolutionary innovation of the lower jaw. Multiple lines of evidence have suggested that the jaw evolved from a rostral gill arch, but when the jaw took on a feeding function remains unclear. We quantified the variety of form in the earliest jaws in the fossil record from which we generated a theoretical morphospace that we then tested for functional optimality. By drawing comparisons with the real jaw data and reconstructed jaw morphologies from phylogenetically inferred ancestors, our results show that the earliest jaw shapes were optimized for fast closure and stress resistance, inferring a predatory feeding function. Jaw shapes became less optimal for these functions during the later radiation of jawed vertebrates. Thus, the evolution of jaw morphology has continually explored previously unoccupied morphospace and accumulated disparity through time, laying the foundation for diverse feeding strategies and the success of jawed vertebrates.

Linking ecomechanical models and functional traits to understand phenotypic diversity.

Physical principles and laws determine the set of possible organismal phenotypes. Constraints arising from development, the environment, and evolutionary history then yield workable, integrated phenotypes. We propose a theoretical and practical framework that considers the role of changing environments. This 'ecomechanical approach' integrates functional organismal traits with the ecological variables. This approach informs our ability to predict species shifts in survival and distribution and provides critical insights into phenotypic diversity. We outline how to use the ecomechanical paradigm using drag-induced bending in trees as an example. Our approach can be incorporated into existing research and help build interdisciplinary bridges. Finally, we identify key factors needed for mass data collection, analysis, and the dissemination of models relevant to this framework.

Nest substrate and tool shape significantly affect the mechanics and energy requirements of avian eggshell puncture.

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.

Ecological opportunity and the rise and fall of crocodylomorph evolutionary innovation.

Understanding the origin, expansion and loss of biodiversity is fundamental to evolutionary biology. The approximately 26 living species of crocodylomorphs (crocodiles, caimans, alligators and gharials) represent just a snapshot of the group's rich 230-million-year history, whereas the fossil record reveals a hidden past of great diversity and innovation, including ocean and land-dwelling forms, herbivores, omnivores and apex predators. In this macroevolutionary study of skull and jaw shape disparity, we show that crocodylomorph ecomorphological variation peaked in the Cretaceous, before declining in the Cenozoic, and the rise and fall of disparity was associated with great heterogeneity in evolutionary rates. Taxonomically diverse and ecologically divergent Mesozoic crocodylomorphs, like marine thalattosuchians and terrestrial notosuchians, rapidly evolved novel skull and jaw morphologies to fill specialized adaptive zones. Disparity in semi-aquatic predatory crocodylians, the only living crocodylomorph representatives, accumulated steadily, and they evolved more slowly for most of the last 80 million years, but despite their conservatism there is no evidence for long-term evolutionary stagnation. These complex evolutionary dynamics reflect ecological opportunities, that were readily exploited by some Mesozoic crocodylomorphs but more limited in Cenozoic crocodylians.

Testing the influence of crushing surface variation on seed-cracking performance among beak morphs of the African seedcracker Pyrenestes ostrinus.

Extreme phenotypic polymorphism is an oft-cited example of evolutionary theory in practice. Although these morphological variations are assumed to be adaptive, few studies have biomechanically tested such hypotheses. Pyrenestes ostrinus (the African seedcracker finch) shows an intraspecific polymorphism in beak size and shape that is entirely diet driven and allelically determined. Three distinct morphs feed upon soft sedge seeds during times of abundance, but during lean times switch to specializing on three different species of sedge seeds that differ significantly in hardness. Here, we test the hypothesis that beak morphology is directly related to consuming seeds of different hardness. We used a novel experimental analysis to test how beak morphology affects the efficiency of cracking sedge seeds of variable hardness, observing that neither mandibular ramus width nor crushing surface morphology had significant effects on the ability to crack different seed types. It is likely that feeding performance is correlated with other aspects of beak size and shape, such as beak depth and strength, muscle force or gape. Our results highlight how even seemingly straightforward examples of adaptive selection in nature can be complex in practice.

"Simple" Biomechanical Model for Ants Reveals How Correlated Evolution among Body Segments Minimizes Variation in Center of Mass as Heads Get Larger.

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.

Taking a Stab at Quantifying the Energetics of Biological Puncture.

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.

Making a point: shared mechanics underlying the diversity of biological puncture.

A viper injecting venom into a target, a mantis shrimp harpooning a fish, a cactus dispersing itself via spines attaching to passing mammals; all these are examples of biological puncture. Although disparate in terms of materials, kinematics and phylogeny, all three examples must adhere to the same set of fundamental physical laws that govern puncture mechanics. The diversity of biological puncture systems is a good case study for how physical laws can be used as a baseline for comparing disparate biological systems. In this Review, I explore the diversity of biological puncture and identify key variables that influence these systems. First, I explore recent work on biological puncture in a diversity of organisms, based on their hypothesized objectives: gripping, injection, damage and defence. Variation within each category is discussed, such as the differences between gripping for prey capture, gripping for dispersal of materials or gripping during reproduction. The second half of the Review is focused on specific physical parameters that influence puncture mechanics, such as material properties, stress, energy, speed and the medium within which puncture occurs. I focus on how these parameters have been examined in biology, and how they influence the evolution of biological systems. The ultimate objective of this Review is to outline an initial framework for examining the mechanics and evolution of puncture systems across biology. This framework will not only allow for broad biological comparisons, but also create a baseline for bioinspired design of both tools that puncture efficiently and materials that can resist puncture.

Strong biomechanical relationships bias the tempo and mode of morphological evolution.

The influence of biomechanics on the tempo and mode of morphological evolution is unresolved, yet is fundamental to organismal diversification. Across multiple four-bar linkage systems in animals, we discovered that rapid morphological evolution (tempo) is associated with mechanical sensitivity (strong correlation between a mechanical system's output and one or more of its components). Mechanical sensitivity is explained by size: the smallest link(s) are disproportionately affected by length changes and most strongly influence mechanical output. Rate of evolutionary change (tempo) is greatest in the smallest links and trait shifts across phylogeny (mode) occur exclusively via the influential, small links. Our findings illuminate the paradigms of many-to-one mapping, mechanical sensitivity, and constraints: tempo and mode are dominated by strong correlations that exemplify mechanical sensitivity, even in linkage systems known for exhibiting many-to-one mapping. Amidst myriad influences, mechanical sensitivity imparts distinct, predictable footprints on morphological diversity.

Herbivorous dinosaur jaw disparity and its relationship to extrinsic evolutionary drivers.

Morphological responses of nonmammalian herbivores to external ecological drivers have not been quantified over extended timescales. Herbivorous nonavian dinosaurs are an ideal group to test for such responses, because they dominated terrestrial ecosystems for more than 155 Myr and included the largest herbivores that ever existed. The radiation of dinosaurs was punctuated by several ecologically important events, including extinctions at the Triassic/Jurassic (Tr/J) and Jurassic/Cretaceous (J/K) boundaries, the decline of cycadophytes, and the origin of angiosperms, all of which may have had profound consequences for herbivore communities. Here we present the first analysis of morphological and biomechanical disparity for sauropodomorph and ornithischian dinosaurs in order to investigate patterns of jaw shape and function through time. We find that morphological and biomechanical mandibular disparity are decoupled: mandibular shape disparity follows taxonomic diversity, with a steady increase through the Mesozoic. By contrast, biomechanical disparity builds to a peak in the Late Jurassic that corresponds to increased functional variation among sauropods. The reduction in biomechanical disparity following this peak coincides with the J/K extinction, the associated loss of sauropod and stegosaur diversity, and the decline of cycadophytes. We find no specific correspondence between biomechanical disparity and the proliferation of angiosperms. Continual ecological and functional replacement of pre-existing taxa accounts for disparity patterns through much of the Cretaceous, with the exception of several unique groups, such as psittacosaurids that are never replaced in their biomechanical or morphological profiles.

Common evolutionary trends underlie the four-bar linkage systems of sunfish and mantis shrimp.

Comparative biomechanics offers an opportunity to explore the evolution of disparate biological systems that share common underlying mechanics. Four-bar linkage modeling has been applied to various biological systems such as fish jaws and crustacean appendages to explore the relationship between biomechanics and evolutionary diversification. Mechanical sensitivity states that the functional output of a mechanical system will show differential sensitivity to changes in specific morphological components. We document similar patterns of mechanical sensitivity in two disparate four-bar systems from different phyla: the opercular four-bar system in centrarchid fishes and the raptorial appendage of stomatopods. We built dynamic linkage models of 19 centrarchid and 36 stomatopod species and used phylogenetic generalized least squares regression (PGLS) to compare evolutionary shifts in linkage morphology and mechanical outputs derived from the models. In both systems, the kinematics of the four-bar mechanism show significant evolutionary correlation with the output link, while travel distance of the output arm is correlated with the coupler link. This common evolutionary pattern seen in both fish and crustacean taxa is a potential consequence of the mechanical principles underlying four-bar systems. Our results illustrate the potential influence of physical principles on morphological evolution across biological systems with different structures, behaviors, and ecologies.