Iron-coated Komodo dragon teeth and the complex dental enamel of carnivorous reptiles.

Komodo dragons (Varanus komodoensis) are the largest extant predatory lizards and their ziphodont (serrated, curved and blade-shaped) teeth make them valuable analogues for studying tooth structure, function and comparing with extinct ziphodont taxa, such as theropod dinosaurs. Like other ziphodont reptiles, V. komodoensis teeth possess only a thin coating of enamel that is nevertheless able to cope with the demands of their puncture-pull feeding. Using advanced chemical and structural imaging, we reveal that V. komodoensis teeth possess a unique adaptation for maintaining their cutting edges: orange, iron-enriched coatings on their tooth serrations and tips. Comparisons with other extant varanids and crocodylians revealed that iron sequestration is probably widespread in reptile enamels but it is most striking in V. komodoensis and closely related ziphodont species, suggesting a crucial role in supporting serrated teeth. Unfortunately, fossilization confounds our ability to consistently detect similar iron coatings in fossil teeth, including those of ziphodont dinosaurs. However, unlike V. komodoensis, some theropods possessed specialized enamel along their tooth serrations, resembling the wavy enamel found in herbivorous hadrosaurid dinosaurs. These discoveries illustrate unexpected and disparate specializations for maintaining ziphodont teeth in predatory reptiles.

Understanding trophic interactions in a warming world by bridging foraging ecology and biomechanics with network science.

Climate change will disrupt biological processes at every scale. Ecosystem functions and services vital to ecological resilience are set to shift, with consequences for how we manage land, natural resources, and food systems. Increasing temperatures cause morphological shifts, with concomitant implications for biomechanical performance metrics crucial to trophic interactions. Biomechanical performance, such as maximum bite force or running speed, determines the breadth of resources accessible to consumers, the outcome of interspecific interactions, and thus the structure of ecological networks. Climate change-induced impacts to ecosystem services and resilience are therefore on the horizon, mediated by disruption of biomechanical performance and, consequently, trophic interactions across whole ecosystems. Here, we argue that there is an urgent need to investigate the complex interactions between climate change, biomechanical traits and foraging ecology to help predict changes to ecological networks and ecosystem functioning. We discuss how these seemingly disparate disciplines can be connected through network science. Using an ant-plant network as an example, we illustrate how different data types could be integrated to investigate the interaction between warming, bite force and trophic interactions, and discuss what such an integration will achieve. It is our hope that this integrative framework will help to identify a viable means to elucidate previously intractable impacts of climate change, with effective predictive potential to guide management and mitigation.

Optimal Gearing of Musculoskeletal Systems.

Movement is integral to animal life, and most animal movement is actuated by the same engine: striated muscle. Muscle input is typically mediated by skeletal elements, resulting in musculoskeletal systems that are geared: at any instant, the muscle force and velocity are related to the output force and velocity only via a proportionality constant G, the "mechanical advantage". The functional analysis of such "simple machines" has traditionally centred around this instantaneous interpretation, such that a small vs large G is thought to reflect a fast vs forceful system, respectively. But evidence is mounting that a comprehensive analysis ought to also consider the mechanical energy output of a complete contraction. Here, we approach this task systematically, and deploy the theory of physiological similarity to study how gearing affects the flow of mechanical energy in a minimalist model of a musculoskeletal system. Gearing influences the flow of mechanical energy in two key ways: it can curtail muscle work output, because it determines the ratio between the characteristic muscle kinetic energy and work capacity; and it defines how each unit of muscle work is partitioned into different system energies, i.e., into kinetic vs. "parasitic" energy such as heat. As a consequence of both effects, delivering maximum work in minimum time and with maximum output speed generally requires a mechanical advantage of intermediate magnitude. This optimality condition can be expressed in terms of two dimensionless numbers that reflect the key geometric, physiological, and physical properties of the interrogated musculoskeletal system, and the environment in which the contraction takes place. Illustrative application to exemplar musculoskeletal systems predicts plausible mechanical advantages in disparate biomechanical scenarios; yields a speculative explanation for why gearing is typically used to attenuate the instantaneous force output (Gopt < 1); and predicts how G needs to vary systematically with animal size to optimise the delivery of mechanical energy, in superficial agreement with empirical observations. A many-to-one-mapping from musculoskeletal geometry to mechanical performance is identified, such that differences in G alone do not provide a reliable indicator for specialisation for force vs speed-neither instantaneously, nor in terms of mechanical energy output. The energy framework presented here can be used to estimate an optimal mechanical advantage across variable muscle physiology, anatomy, mechanical environment and animal size, and so facilitates investigation of the extent to which selection has made efficient use of gearing as degree of freedom in musculoskeletal "design".

The effect of muscle ultrastructure on the force, displacement and work capacity of skeletal muscle.

Skeletal muscle powers animal movement through interactions between the contractile proteins, actin and myosin. Structural variation contributes greatly to the variation in mechanical performance observed across muscles. In vertebrates, gross structural variation occurs in the form of changes in the muscle cross-sectional area : fibre length ratio. This results in a trade-off between force and displacement capacity, leaving work capacity unaltered. Consequently, the maximum work per unit volume-the work density-is considered constant. Invertebrate muscle also varies in muscle ultrastructure, i.e. actin and myosin filament lengths. Increasing actin and myosin filament lengths increases force capacity, but the effect on muscle fibre displacement, and thus work, capacity is unclear. We use a sliding-filament muscle model to predict the effect of actin and myosin filament lengths on these mechanical parameters for both idealized sarcomeres with fixed actin : myosin length ratios, and for real sarcomeres with known filament lengths. Increasing actin and myosin filament lengths increases stress without reducing strain capacity. A muscle with longer actin and myosin filaments can generate larger force over the same displacement and has a higher work density, so seemingly bypassing an established trade-off. However, real sarcomeres deviate from the idealized length ratio suggesting unidentified constraints or selective pressures.

Large deformation diffeomorphic mapping of 3D shape variation reveals two distinct mandible and head capsule morphs in Atta vollenweideri leaf-cutter worker ants.

Ants are crucial ecosystem engineers, and their ecological success is facilitated by a division of labour among sterile "workers". In some ant lineages, workers have undergone further morphological differentiation, resulting in differences in body size, shape, or both. Distinguishing between changes in size and shape is not trivial. Traditional approaches based on allometry reduce complex 3D shapes into simple linear, areal, or volume metrics; modern approaches using geometric morphometrics typically rely on landmarks, introducing observer bias and a trade-off between effort and accuracy. Here, we use a landmark-free method based on large deformation diffeomorphic metric mapping (LDDMM) to assess the co-variation of size and 3D shape in the mandibles and head capsules of Atta vollenweideri leaf-cutter ants, a species exhibiting extreme worker size-variation. Body mass varied by more than two orders of magnitude, but a shape atlas created via LDDMM on µ-CT-derived 3D mesh files revealed only two distinct head capsule and mandibles shapes-one for the minims (body mass < 1 mg) and one for all other workers. We discuss the functional significance of the identified 3D shape variation, and its implications for the evolution of extreme polymorphism in Atta.

Dynamic similarity and the peculiar allometry of maximum running speed.

Animal performance fundamentally influences behaviour, ecology, and evolution. It typically varies monotonously with size. A notable exception is maximum running speed; the fastest animals are of intermediate size. Here we show that this peculiar allometry results from the competition between two musculoskeletal constraints: the kinetic energy capacity, which dominates in small animals, and the work capacity, which reigns supreme in large animals. The ratio of both capacities defines the physiological similarity index Γ, a dimensionless number akin to the Reynolds number in fluid mechanics. The scaling of Γ indicates a transition from a dominance of muscle forces to a dominance of inertial forces as animals grow in size; its magnitude defines conditions of "dynamic similarity" that enable comparison and estimates of locomotor performance across extant and extinct animals; and the physical parameters that define it highlight opportunities for adaptations in musculoskeletal "design" that depart from the eternal null hypothesis of geometric similarity. The physiological similarity index challenges the Froude number as prevailing dynamic similarity condition, reveals that the differential growth of muscle and weight forces central to classic scaling theory is of secondary importance for the majority of terrestrial animals, and suggests avenues for comparative analyses of locomotor systems.

replicAnt: a pipeline for generating annotated images of animals in complex environments using Unreal Engine.

Deep learning-based computer vision methods are transforming animal behavioural research. Transfer learning has enabled work in non-model species, but still requires hand-annotation of example footage, and is only performant in well-defined conditions. To help overcome these limitations, we developed replicAnt, a configurable pipeline implemented in Unreal Engine 5 and Python, designed to generate large and variable training datasets on consumer-grade hardware. replicAnt places 3D animal models into complex, procedurally generated environments, from which automatically annotated images can be exported. We demonstrate that synthetic data generated with replicAnt can significantly reduce the hand-annotation required to achieve benchmark performance in common applications such as animal detection, tracking, pose-estimation, and semantic segmentation. We also show that it increases the subject-specificity and domain-invariance of the trained networks, thereby conferring robustness. In some applications, replicAnt may even remove the need for hand-annotation altogether. It thus represents a significant step towards porting deep learning-based computer vision tools to the field.

Biomechanics of cutting: sharpness, wear sensitivity and the scaling of cutting forces in leaf-cutter ant mandibles.

Herbivores large and small need to mechanically process plant tissue. Their ability to do so is determined by two forces: the maximum force they can generate, and the minimum force required to fracture the plant tissue. The ratio of these forces determines the relative mechanical effort; how this ratio varies with animal size is challenging to predict. We measured the forces required to cut thin polymer sheets with mandibles from leaf-cutter ant workers which vary by more than one order of magnitude in body mass. Cutting forces were independent of mandible size, but differed by a factor of two between pristine and worn mandibles. Mandibular wear is thus likely a more important determinant of cutting force than mandible size. We rationalize this finding with a biomechanical analysis, which suggests that pristine mandibles are ideally 'sharp'-cutting forces are close to a theoretical minimum, which is independent of tool size and shape, and instead solely depends on the geometric and mechanical properties of the cut tissue. The increase of cutting force due to mandibular wear may be particularly problematic for small ants, which generate lower absolute bite forces, and thus require a larger fraction of their maximum bite force to cut the same plant. This article is part of the theme issue 'Food processing and nutritional assimilation in animals'.

Three-dimensional kinematics of leaf-cutter ant mandibles: not all dicondylic joints are simple hinges.

Insects use their mandibles for a variety of tasks, including food processing, material transport, nest building, brood care, and fighting. Despite this functional diversity, mandible motion is typically thought to be constrained to rotation about a single fixed axis. Here, we conduct a direct quantitative test of this 'hinge joint hypothesis' in a species that uses its mandibles for a wide range of tasks: Atta vollenweideri leaf-cutter ants. Mandible movements from live restrained ants were reconstructed in three dimensions using a multi-camera rig. Rigid body kinematic analyses revealed strong evidence that mandible movement occupies a kinematic space that requires more than one rotational degree of freedom: at large opening angles, mandible motion is dominated by yaw. But at small opening angles, mandibles both yaw and pitch. The combination of yaw and pitch allows mandibles to 'criss-cross': either mandible can be on top when mandibles are closed. We observed criss-crossing in freely cutting ants, suggesting that it is functionally important. Combined with recent reports on the diversity of joint articulations in other insects, our results show that insect mandible kinematics are more diverse than traditionally assumed, and thus worthy of further detailed investigation. This article is part of the theme issue 'Food processing and nutritional assimilation in animals'.

Developmental biomechanics and age polyethism in leaf-cutter ants.

Many social insects display age polyethism: young workers stay inside the nest, and only older workers forage. This behavioural transition is accompanied by genetic and physiological changes, but the mechanistic origin of it remains unclear. To investigate if the mechanical demands on the musculoskeletal system effectively prevent young workers from foraging, we studied the biomechanical development of the bite apparatus in Atta vollenweideri leaf-cutter ants. Fully matured foragers generated peak in vivo bite forces of around 100 mN, more than one order of magnitude in excess of those measured for freshly eclosed callows of the same size. This change in bite force was accompanied by a sixfold increase in the volume of the mandible closer muscle, and by a substantial increase of the flexural rigidity of the head capsule, driven by a significant increase in both average thickness and indentation modulus of the head capsule cuticle. Consequently, callows lack the muscle force capacity required for leaf-cutting, and their head capsule is so compliant that large muscle forces would be likely to cause damaging deformations. On the basis of these results, we speculate that continued biomechanical development post eclosion may be a key factor underlying age polyethism, wherever foraging is associated with substantial mechanical demands.

Strong positive allometry of bite force in leaf-cutter ants increases the range of cuttable plant tissues.

Atta leaf-cutter ants are the prime herbivore in the Neotropics: differently sized foragers harvest plant material to grow a fungus as a crop. Efficient foraging involves complex interactions between worker size, task preferences and plant-fungus suitability; it is, however, ultimately constrained by the ability of differently sized workers to generate forces large enough to cut vegetation. In order to quantify this ability, we measured bite forces of Atta vollenweideri leaf-cutter ants spanning more than one order of magnitude in body mass. Maximum bite force scaled almost in direct proportion to mass; the largest workers generated peak bite forces 2.5 times higher than expected from isometry. This remarkable positive allometry can be explained via a biomechanical model that links bite forces with substantial size-specific changes in the morphology of the musculoskeletal bite apparatus. In addition to these morphological changes, we show that bite forces of smaller ants peak at larger mandibular opening angles, suggesting a size-dependent physiological adaptation, probably reflecting the need to cut leaves with a thickness that corresponds to a larger fraction of the maximum possible gape. Via direct comparison of maximum bite forces with leaf mechanical properties, we demonstrate (i) that bite forces in leaf-cutter ants need to be exceptionally large compared with body mass to enable them to cut leaves; and (ii), that the positive allometry enables colonies to forage on a wider range of plant species without the need for extreme investment in even larger workers. Our results thus provide strong quantitative arguments for the adaptive value of a positively allometric bite force.

A theory of physiological similarity in muscle-driven motion.

Muscle contraction is the primary source of all animal movement. I show that the maximum mechanical output of such contractions is determined by a characteristic dimensionless number, the "effective inertia," Γ, defined by a small set of mechanical, physiological, and anatomical properties of the interrogated musculoskeletal complex. Different musculoskeletal systems with equal Γ may be considered physiologically similar, in the sense that maximum performance involves equal fractions of the muscle's maximum strain rate, strain capacity, work, and power density. It can be demonstrated that there exists a unique, "optimal" musculoskeletal anatomy which enables a unit volume of muscle to deliver maximum work and power simultaneously, corresponding to Γ close to unity. External forces truncate the mechanical performance space accessible to muscle by introducing parasitic losses, and subtly alter how musculoskeletal anatomy modulates muscle performance, challenging canonical notions of skeletal force-velocity trade-offs. Γ varies systematically under isogeometric transformations of musculoskeletal systems, a result which provides fundamental insights into the key determinants of animal locomotor performance across scales.

Multilevel dynamic adjustments of geckos (Hemidactylus frenatus) climbing vertically: head-up versus head-down.

Many climbing animals use direction-dependent adhesives to attach to vertical or inclined surfaces. These structures adhere when activated via a pull but detach when pushed. Therefore, a challenge arises when a change in climbing direction causes external forces such as gravity to change its acting orientation upon the lizard. To investigate how specialized climbers adjust, we studied kinematics and dynamics of six Hemidactylus frenatus geckos climbing head-up and head-down a vertical racetrack. We found that limbs functionally swap their adhesive role: feet above the centre of mass (COM) generated adhesive forces, feet below the COM compressive forces, both equal in magnitude across directions. To investigate how lizards perform this swap, despite the constraint of their direction-dependent adhesives, we analysed kinematic adjustments across multiple smaller levels of hierarchy: limbs, feet and toes. All levels contributed: the hindfoot angle was reoriented realigning the adhesive structure, the hindlimb centre range of motion was further protracted and the hindfoot toe spreading was reduced. Notably, all three variables were adjustments of hindlimbs, suggesting that they make a more flexible contribution in upward versus downward climbing, while forelimbs may be anatomically or functionally constrained. The relevance of multilevel dynamic adjustments might inform the development of performant gaits for legged climbing robots.

A biomechanical model for the relation between bite force and mandibular opening angle in arthropods.

Bite forces play a key role in animal ecology: they affect mating behaviour, fighting success, and the ability to feed. Although feeding habits of arthropods have a significant ecological and economical impact, we lack fundamental knowledge on how the morphology and physiology of their bite apparatus controls bite performance, and its variation with mandible gape. To address this gap, we derived a biomechanical model that characterizes the relationship between bite force and mandibular opening angle from first principles. We validate this model by comparing its geometric predictions with morphological measurements on the muscoloskeletal bite apparatus of Atta cephalotes leaf-cutter ants, using computed tomography (CT) scans obtained at different mandible opening angles. We then demonstrate its deductive and inductive utility with three examplary use cases: Firstly, we extract the physiological properties of the leaf-cutter ant mandible closer muscle from in vivo bite force measurements. Secondly, we show that leaf-cutter ants are specialized to generate extraordinarily large bite forces, equivalent to about 2600 times their body weight. Thirdly, we discuss the relative importance of morphology and physiology in determining the magnitude and variation of bite force. We hope that a more detailed quantitative understanding of the link between morphology, physiology, and bite performance will facilitate future comparative studies on the insect bite apparatus, and help to advance our knowledge of the behaviour, ecology and evolution of arthropods.

The physical properties of the stick insect pad secretion are independent of body size.

Many insects use adhesive organs to climb. The ability to cling to surfaces is advantageous but is increasingly challenged as animals grow, due to the associated reduction in surface-to-volume ratio. Previous work has demonstrated that some climbing animals overcome this scaling problem by systematically altering the maximum force per area that their adhesive pads can sustain; their adhesive organs become more efficient as they grow, an observation which is also of substantial relevance for the design of bioinspired adhesives. What is the origin of this change in efficiency? In insects, adhesive contact is mediated by a thin film of a liquid, thought to increase adhesive performance via capillary and viscous forces. Here, we use interference reflection microscopy and dewetting experiments to measure the contact angle and dewetting speed of the secretion of pre-tarsal adhesive pads of Indian stick insects, varying in mass by over two orders of magnitude. Neither contact angle nor dewetting speed change significantly with body mass, suggesting that the key physical properties of the pad secretion-its surface tension and viscosity-are size-invariant. Thus, the observed change in pad efficiency is unlikely to arise from systematic changes of the physical properties of the pad secretion; the functional role of the secretion remains unclear.

Elastic energy storage and the efficiency of movement.

Movement is an integral part of animal biology. It enables organisms to escape from danger, acquire food, and perform courtship displays. Changing the speed or vertical position of a body requires mechanical energy. This energy is typically provided by the biological motor, striated muscle. Striated muscle uses chemical (metabolic) energy to produce force, to move this force over a distance to do work, and to do this work within some time to generate power. The metabolic energy consumed in producing these mechanical outputs is a major component of an organism's energy budget, particularly during repetitive, cyclical movements. This energy could otherwise be used for maintenance, growth, and reproduction. Hence, fitness may be enhanced by improving locomotor efficiency - the ratio between work done and metabolic energy consumed. This may be achieved by reducing the need for muscle to do work, and by increasing the efficiency with which muscle does work.

Morphological determinants of bite force capacity in insects: a biomechanical analysis of polymorphic leaf-cutter ants.

The extraordinary success of social insects is partially based on division of labour, i.e. individuals exclusively or preferentially perform specific tasks. Task preference may correlate with morphological adaptations so implying task specialization, but the extent of such specialization can be difficult to determine. Here, we demonstrate how the physical foundation of some tasks can be leveraged to quantitatively link morphology and performance. We study the allometry of bite force capacity in Atta vollenweideri leaf-cutter ants, polymorphic insects in which the mechanical processing of plant material is a key aspect of the behavioural portfolio. Through a morphometric analysis of tomographic scans, we show that the bite force capacity of the heaviest colony workers is twice as large as predicted by isometry. This disproportionate 'boost' is predominantly achieved through increased investment in muscle volume; geometrical parameters such as mechanical advantage, fibre length or pennation angle are likely constrained by the need to maintain a constant mandibular opening range. We analyse this preference for an increase in size-specific muscle volume and the adaptations in internal and external head anatomy required to accommodate it with simple geometric and physical models, so providing a quantitative understanding of the functional anatomy of the musculoskeletal bite apparatus in insects.

scAnt-an open-source platform for the creation of 3D models of arthropods (and other small objects).

We present scAnt, an open-source platform for the creation of digital 3D models of arthropods and small objects. scAnt consists of a scanner and a Graphical User Interface, and enables the automated generation of Extended Depth Of Field images from multiple perspectives. These images are then masked with a novel automatic routine which combines random forest-based edge-detection, adaptive thresholding and connected component labelling. The masked images can then be processed further with a photogrammetry software package of choice, including open-source options such as Meshroom, to create high-quality, textured 3D models. We demonstrate how these 3D models can be rigged to enable realistic digital specimen posing, and introduce a novel simple yet effective method to include semi-realistic representations of approximately planar and transparent structures such as wings. As a result of the exclusive reliance on generic hardware components, rapid prototyping and open-source software, scAnt costs only a fraction of available comparable systems. The resulting accessibility of scAnt will (i) drive the development of novel and powerful methods for machine learning-driven behavioural studies, leveraging synthetic data; (ii) increase accuracy in comparative morphometric studies as well as extend the available parameter space with area and volume measurements; (iii) inspire novel forms of outreach; and (iv) aid in the digitisation efforts currently underway in several major natural history collections.

Disentangling the role of surface topography and intrinsic wettability in the prey capture mechanism of Nepenthes pitcher plants.

Nepenthes pitcher plants capture prey with leaves specialised as pitfall traps. Insects are trapped when they 'aquaplane' on the pitcher rim (peristome), a surface structured with macroscopic and microscopic radial ridges. What is the functional significance of this hierarchical surface topography? Here, we use insect pad friction measurements, photolithography, wetting experiments and physical modelling to demonstrate that the ridges enhance the trap's efficacy by satisfying two functional demands on prey capture: Macroscopic ridges restrict lateral but enhance radial spreading of water, thereby creating continuous slippery tracks which facilitate prey capture when little water is present. Microscopic ridges, in turn, ensure that the water film between insect pad and peristome remains stable, causing insects to aquaplane. In combination, the hierarchical ridge structure hence renders the peristome wettable, and water films continuous, so avoiding the need for a strongly hydrophilic surface chemistry, which would compromise resistance to desiccation and attract detrimental contamination.