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Historically, predicting ursid feeding behaviour on the basis of morphometric and mechanical analyses has proven difficult. Here, we apply three‐dimensional finite element analysis to models representing five extant and one fossil species of bear. The ability to generate high bite forces, and for the skull to sustain them, is present in both the gi...
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... finite element models were assembled from computed tomography (CT) data representing five extant species (brown bear, Asian bear, black bear, polar bear and giant panda) and one fossil ursid A. africanum (SI Table S1). For extant taxa, preprocessing followed the previously published protocols Moreno et al., 2008;Wroe, 2008;Degrange et al., 2010;Wroe et al., 2010). ...
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... forces and bite force quotients [i.e. bite forces adjusted for body mass (Wroe et al., 2005)] were derived from the unscaled FEMs (see Table 1). Body masses were estimated for each specimen using an equation presented for ursids based on skull length (Van Valkenburgh, 1990). ...
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... absolute terms, bite force at the canines is greatest in A. af- ricanum (4566 N) and least in the Asian bear (1217 N). Bite force adjusted for body mass (bite force quotient, BFQ) was much higher in A. africanum and the giant panda than in any other species/specimens (Table 1). Lowest values for BFQ were for the Asian bear and the polar bear. ...
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... 4566 N, our 3D bilateral canine bite force estimate for A. africanum is the highest predicted for any mammal, being considerably greater than the equivalent for a very large male African lion (Panthera leo) (Wroe, 2008). A. africanum also had a very powerful bite for its size as indicated by a high BFQ value (Table 1). ...
Citations
... Dumont et al., 2011a;Ledogar et al., 2022;Mitchell et al., 2018;Wroe, 2010). Comparative FEA has been used in this way to great effect across diverse extant and extinct vertebrates, particularly to assess feeding biomechanics of the vertebrate skull (Attard et al., 2011;Cook et al., 2021;Cox et al., 2011Cox et al., , 2015Dumont et al., 2011a,b;Ferrara et al., 2011;Figueirido et al., 2014;Ledogar et al., 2016Ledogar et al., , 2018Ledogar et al., , 2022Mitchell, 2019;Mitchell et al., 2018;Mitchell and Wroe, 2019;Oldfield et al., 2011;Rayfield, 2011;Slater et al., 2009;Smith et al., 2015b;Strait et al., 2009;Tseng, 2008;Tseng et al., 2011;van Heteren et al., 2021;Wroe, 2007;Wroe et al., 2007Wroe et al., , 2013. Through these studies, we have gained valuable insights into the relationship between skull morphology and mechanical performance, with applications towards animal behaviour, conservation, ecology, evolution and palaeontology. ...
... There are two main methods that aim to standardise mechanical advantage. The first is done on models that have been scaled to equivalent size, by rescaling the initial muscle forces to result in a common bite force ( Fig. 1A) (Attard et al., 2011;Oldfield et al., 2011;Wroe et al., 2010). The goal is to ensure that all models are performing an equivalent action, for their size, and the stress and strain magnitudes therefore adequately reflect an equivalent action of the jaw, when adjusted for size. ...
... This method is similar in aim to rescaling the models to the same size and applying muscle forces that result in the same bite reaction force for a given size (e.g. Attard et al., 2011;Oldfield et al., 2011;Wroe et al., 2010); however, we chose this approach because it allows for the same models to be used in all our scaling scenarios. This procedure corrected for the effects mechanical advantage on strain magnitudes during equivalent bites. ...
Comparative finite element analysis involves standardising aspects of models to test equivalent loading scenarios across species. However, regarding feeding biomechanics of the vertebrate skull, what is considered “equivalent” can depend on the hypothesis. Using 13 diversely-shaped skulls of marsupial bettongs and potoroos (Potoroidae), we demonstrate that scaling muscle forces to standardise specific aspects of biting mechanics can produce clearly opposing comparisons of stress or strain that are differentially suited to address specific kinds of hypotheses. We therefore propose three categories of hypotheses for skull biting mechanics, each involving a unique method of muscle scaling to produce meaningful results: those comparing (1) the skull's efficiency in distributing muscle forces to the biting teeth, via standardising input muscle force to skull size, (2) structural biting adaptation through standardising mechanical advantage to simulate size-independent, equivalent bites, and (3) feeding ecology affected by size, such as niche partitioning, via standardising bite reaction force.
... 1c and 3a). Observing how the same relationship between form and function is found in placentals and marsupials (Fig. 6a, b) the latter can be considered replicated "experiments" from this point of viewfurther supports the idea that the force-driven adaptations are constrained biomechanical solutions achieved within a smaller set of available evolutionary pathways as compared to adaptations maximising velocity 66 . ...
Functional trade-offs can affect patterns of morphological and ecological evolution as well as the magnitude of morphological changes through evolutionary time. Using morpho-functional landscape modelling on the cranium of 132 carnivore species, we focused on the macroevolutionary effects of the trade-off between bite force and bite velocity. Here, we show that rates of evolution in form (morphology) are decoupled from rates of evolution in function. Further, we found theoretical morphologies optimising for velocity to be more diverse, while a much smaller phenotypic space was occupied by shapes optimising force. This pattern of differential representation of different functions in theoretical morphological space was highly correlated with patterns of actual morphological disparity. We hypothesise that many-to-one mapping of cranium shape on function may prevent the detection of direct relationships between form and function. As comparatively only few morphologies optimise bite force, species optimising this function may be less abundant because they are less likely to evolve. This, in turn, may explain why certain clades are less variable than others. Given the ubiquity of functional trade-offs in biological systems, these patterns may be general and may help to explain the unevenness of morphological and functional diversity across the tree of life.
... Velociraptor mongoliensis experiences the lowest MWAM strain (360 με) of any modelled dromaeosaurid, and this taxon is suggested to have had regularly engaged in scavenging behaviour [88]. Higher jaw strength is associated with scavenging among extant carnivorous birds [83,89] and mammals [90,91], so it may be that dromaeosaurids with stronger jaws (e.g. Dromaeosaurus albertensis, 399 με) were more reliant on carrion and those with weaker jaws (e.g. ...
Non-avialan theropod dinosaurs had diverse ecologies and varied skull morphologies. Previous studies of theropod cranial morphology mostly focused on higher-level taxa or characteristics associated with herbivory. To better understand morphological disparity and function within carnivorous theropod families, here we focus on the Dromaeosauridae, ‘raptors’ traditionally seen as agile carnivorous hunters.
We applied 2D geometric morphometrics to quantify skull shape, performed mechanical advantage analysis to assess the efficiency of bite force transfer, and performed finite element analysis to examine strain distribution in the skull during biting. We find that dromaeosaurid skull morphology was less disparate than most non-avialan theropod groups. Their skulls show a continuum of form between those that are tall and short and those that are flat and long. We hypothesise that this narrower morphological disparity indicates developmental constraint on skull shape, as observed in some mammalian families. Mechanical advantage indicates that Dromaeosaurus albertensis and Deinonychus antirrhopus were adapted for relatively high bite forces, while Halszkaraptor escuilliei was adapted for high bite speed, and other dromaeosaurids for intermediate bite forces and speeds. Finite element analysis indicates regions of high strain are consistent within dromaeosaurid families but differ between them. Average strain levels do not follow any phylogenetic pattern, possibly due to ecological convergence between distantly-related taxa.
Combining our new morphofunctional data with a re-evaluation of previous evidence, we find piscivorous reconstructions of Halszkaraptor escuilliei to be unlikely, and instead suggest an invertivorous diet and possible adaptations for feeding in murky water or other low-visibility conditions. We support Deinonychus antirrhopus as being adapted for taking large vertebrate prey, but we find that its skull is relatively less resistant to bite forces than other dromaeosaurids. Given the recovery of high bite force resistance for Velociraptor mongoliensis, which is believed to have regularly engaged in scavenging behaviour, we suggest that higher bite force resistance in a dromaeosaurid taxon may reflect a greater reliance on scavenging rather than fresh kills.
Comparisons to the troodontid Gobivenator mongoliensis suggest that a gracile rostrum like that of Velociraptor mongoliensis is ancestral to their closest common ancestor (Deinonychosauria) and the robust rostra of Dromaeosaurus albertensis and Deinonychus antirrhopus are a derived condition. Gobivenator mongoliensis also displays a higher jaw mechanical advantage and lower resistance to bite force than the examined dromaeosaurids, but given the hypothesised ecological divergence of troodontids from dromaeosaurids it is unclear which group, if either, represents the ancestral condition. Future work extending sampling to troodontids would therefore be invaluable and provide much needed context to the origin of skull form and function in early birds. This study illustrates how skull shape and functional metrics can discern non-avialan theropod ecology at lower taxonomic levels and identify variants of carnivorous feeding.
Supplementary Information
The online version contains supplementary material available at 10.1186/s12862-024-02222-5.
... In the past 15 years, the FE method has become a ubiquitous tool in the repertoire of evolutionary biologists (Kolston, 2000;Rayfield, 2007), although it has rarely been used to model the fish (or any other vertebrates') hearing system. FE analysis is notably often used in paleontology to predict the abilities of extinct taxa to withstand loads induced by a biomechanical function, like chewing, for example, or walking (e.g., Macho et al., 2005;Oldfield et al., 2012). As the extinct specimen in focus cannot be tested in vivo, digital versions of the morphology, materials, and loads can be modelled and analysed. ...
Fishes, including elasmobranchs (sharks, rays, and skates), present an astonishing diversity in inner ear morphologies; however, the functional significance of these variations and how they confer auditory capacity is yet to be resolved. The relationship between inner ear structure and hearing performance is unclear, partly because most of the morphological and biomechanical mechanisms that underlie the hearing functions are complex and poorly known. Here, we present advanced opportunities to document discontinuities in the macroevolutionary trends of a complex biological form, like the inner ear, and test hypotheses regarding what factors may be driving morphological diversity. Three-dimensional (3D) bioimaging, geometric morphometrics, and finite element analysis are methods that can be combined to interrogate the structure-to-function links in elasmobranch fish inner ears. In addition, open-source 3D morphology datasets, advances in phylogenetic comparative methods, and methods for the analysis of highly multidimensional shape data have leveraged these opportunities. Questions that can be explored with this toolkit are identified, the different methods are justified, and remaining challenges are highlighted as avenues for future work.
... Rarely documented are its postcranial skeletons, and a complete humerus has never been reported. For an ursid reaching to a body size of 400 kg and with controversial diet (Sorkin 2006a;Oldfield et al., 2012), its limb bones contain much-needed information about its locomotion as well as predatory behaviors. ...
... The reduction of these structures is a factor that limited the effectiveness of Agriotherium for hunting and retention of large prey. These factors influenced the diet of Agriotherium that was not strictly carnivorous (Sorkin, 2006a;Hendey, 1980;Oldfield et al., 2012). ...
A complete humerus referred to Agriotherium is described, collected from early-late Hemphillian deposits from Zacatecas. Agriotherium is widely represented by isolated molars, mandibles, and maxillae in early-late Hemphillian faunas of Eurasia and North America. In the literature, postcranial elements are scarce and briefly described with little detail. The greatest diversity is known from the Langebaanweg quarry in South Africa; however, the only complete specimen is from Mexico. The proximal end is described, and the humerus shares similarities with the description of the distal end from South Africa, in which the medial epicondyle and crest of the lateral epicondyle are reduced, which can be considered as a limitation in the hunting of larger prey for food. This implies that Agriotherium was not strictly carnivorous but was a predator-scavenger with an omnivorous diet that included plants and fruits.
... As routinely employed in FE analyses (e.g. [23][24][25][26][27][28]), we reconstructed or retrodeformed some models of fossil taxa. To assure transparency, a complete description of the various reconstruction and retro-deformation steps undertaken is available in Figures S1-S9. ...
Cat-like carnivorans are a textbook example of convergent evolution with distinct morphological differences between taxa with short or elongated upper canines, the latest being often interpreted as an adaptation to bite at large angles and subdue large prey. This interpretation of the sabretooth condition is reinforced by a reduced taxonomic sampling in some studies, often focusing on highly derived taxa or using simplified morphological models. Moreover, most biomechanical analyses focus on biting scenarios at small gapes, ideal for modern carnivora but ill-suited to test for subduction of large prey by sabre-toothed taxa. In this contribution we present the largest 3D collection-based muscle-induced biting simulations on cat like carnivorans by running a total of 1,074 analyses on 17 different taxa at three different biting angles (30°, 60° and 90°) including both morphologies. While our results show a clear adaptation of extreme sabre-toothed taxa to bite at larger angles in terms of stress distribution, other performance variables display surprising similarities between all forms at the different angles tested, highlighting a continuous rather than bipolar spectrum of hunting methods in cat-like carnivorans and demonstrating a wide functional disparity and nuances of the sabretooth condition that cannot simply be characterized by specialized feeding biomechanics.
... While initially common in engineering, architecture, and orthopaedic sciences, it is now widely used to assess the biomechanics of the human musculoskeletal system, and in recent years it has been a crucial tool in understanding vertebrate biomechanics and evolution (Ross, 2005;Rayfield, 2007). FEA has been used in studies of 2D (Rayfield, 2004;Rayfield, 2005a;Rayfield, 2005b;Pierce, Angielczyk & Rayfield, 2008;Pierce, Angielczyk & Rayfield, 2009;Fletcher, Janis & Rayfield, 2010;Ma et al., 2021) and 3D structures (Moreno et al., 2008;Bell, Snively & Shychoski, 2009;Oldfield et al., 2012;Cost et al., 2019;Rowe & Snively, 2021) to assess patterns and magnitudes of stresses and strain in both extant and extinct organisms, as well as suture morphology in the crania of reptiles (Rayfield, 2005a;Rayfield, 2005b;Jones et al., 2017) and mammals (Bright & Gröning, 2011;Bright, 2012). While studies involving FEA commonly focus on stress and strain occurring in the skull during feeding (Rayfield, 2007), studies may also examine the biomechanics of other vertebrate appendages (Arbour & Snively, 2009;Lautenschlager, 2014;Bishop et al., 2018). ...
Finite element analysis (FEA) is a commonly used application in biomechanical studies of both extant and fossil taxa to assess stress and strain in solid structures such as bone. FEA can be performed on 3D structures that are generated using various methods, including computed tomography (CT) scans and surface scans. While previous palaeobiological studies have used both CT scanned models and surface scanned models, little research has evaluated to what degree FE results may vary when CT scans and surface scans of the same object are compared. Surface scans do not preserve the internal geometries of 3D structures, which are typically preserved in CT scans. Here, we created 3D models from CT scans and surface scans of the same specimens (crania and mandibles of a Nile crocodile, a green sea turtle, and a monitor lizard) and performed FEA under identical loading parameters. It was found that once surface scanned models are solidified, they output stress and strain distributions and model deformations comparable to their CT scanned counterparts, though differing by notable stress and strain magnitudes in some cases, depending on morphology of the specimen and the degree of reconstruction applied. Despite similarities in overall mechanical behaviour, surface scanned models can differ in exterior shape compared to CT scanned models due to inaccuracies that can occur during scanning and reconstruction, resulting in local differences in stress distribution. Solid-fill surface scanned models generally output lower stresses compared to CT scanned models due to their compact interiors, which must be accounted for in studies that use both types of scans.
... This is a computational engineering tool that involves simulating behaviors or actions of interest on digital models rendered from scanned specimens (Richmond et al. 2005;Rayfield 2007;Panagiotopoulou 2009;Bright 2014). Relative performance metrics such as mechanical efficiency (output force/total applied muscle force), stress (force per unit area), and strain ( length/initial length) can be obtained from modeled skulls and are often attributed to known or predicted diets and feeding behaviors across the species examined (e.g., Wroe et al. 2007Wroe et al. , 2013Porro et al. 2011;Ross et al. 2011;Cox et al. 2012;Oldfield et al. 2012;Smith et al. 2015;Tseng and Flynn 2015;Godinho et al. 2018;Lautenschlager et al. 2018;Ledogar et al. 2018;Mitchell et al. 2018;Panagiotopoulou et al. 2020). In order to highlight potential biomechanical deficits introduced by soft diets in captive-reared fauna, we employ the finite element method here to test the influence that contrasting food material properties have on bone deposition, and resulting biting performance, in a single generation of animals raised from weaning. ...
The rescue and rehabilitation of young fauna is of substantial importance to conservation. However, it has been suggested that incongruous diets offered in captive environments may alter craniofacial morphology and hinder the success of reintroduced animals. Despite these claims, to what extent dietary variation throughout ontogeny impacts intrapopulation cranial biomechanics has not yet been tested. Here, finite element models were generated from the adult crania of 40 rats (n = 10 per group) that were reared on 4 different diet regimes and stress magnitudes compared during incisor bite simulations. The diets consisted of (1) exclusively hard pellets from weaning, (2) exclusively soft ground pellet meal from weaning, (3) a juvenile switch from pellets to meal, and (4) a juvenile switch from meal to pellets. We hypothesized that a diet of exclusively soft meal would result in the weakest adult skulls, represented by significantly greater stress magnitudes at the muzzle, palate, and zygomatic arch. Our hypothesis was supported at the muzzle and palate, indicating that a diet limited to soft food inhibits bone deposition throughout ontogeny. This finding presents a strong case for a more variable and challenging diet during development. However, rather than the "soft" diet group resulting in the weakest zygomatic arch as predicted, this region instead showed the highest stress among rats that switched as juveniles from hard pellets to soft meal. We attribute this to a potential reduction in number and activity of osteoblasts, as demonstrated in studies of sudden and prolonged disuse of bone. A shift to softer foods in captivity, during rehabilitation after injury in the wild for example, can therefore be detrimental to healthy development of the skull in some growing animals, potentially increasing the risk of injury and impacting the ability to access full ranges of wild foods upon release. We suggest captive diet plans consider not just nutritional requirements but also food mechanical properties when rearing wildlife to adulthood for reintroduction.
... Here, we use the 'dry-skull' method and the finite element analysis (FEA) to estimate the bite force of Z. varolai and test the bite performances of this extinct macroraptorial sperm whale. FEA has proven to be a powerful tool to investigate form and function of extinct vertebrates (Rayfield et al. 2001;Hassan et al. 2002;McHenry et al. 2007;Wroe et al. 2007;Bell et al. 2009;Oldfield et al. 2012;Foffa et al. 2014;Snively et al. 2015), but such a biomechanical approach has never been used before on a macroraptorial sperm whale. The results obtained from the FEA bite simulations provide informative clues about the palaeoecology of this top predator from the late Miocene, and open new intriguing research horizons concerning the macroraptorial physeteroids and their trophic role in the Miocene global ocean. ...
Differing from the extant physeteroids, macroraptorial sperm whales are currently regarded as apex predators of the Miocene seas based on several morphofunctional observations. Here, we estimate the bite force of Zygophyseter varolai, a macroraptorial physeteroid from lower upper Miocene strata of the Pietra leccese formation (Apulia, Italy) using the finite element analysis (FEA). To explore multiple bite scenarios, we set four different load cases on a 3D model of the cranium obtained via digital photogram-metry, considering the temporalis and masseter muscles as jaw adductors. Our FEA simulations indicate that Z. varolai exerted an anterior bite force of more than 4000 N and a posterior bite force of more than 10000 N. These values are similar to those estimated for other marine predators known for their powerful bite. This suggests that Z. varolai might have fed upon medium-sized marine vertebrates like other odontocetes. Considering the significant difference observed between the anterior and posterior bite forces, Z. varolai likely fed via 'grip-and-shear' feeding, snapping the food items with an anterior bite and then cutting them with a powerful posterior bite. Other macroraptorial sperm whales such as the roughly coeval Acrophyseter from Peru likely employed the same feeding technique. ARTICLE HISTORY
... Finite element analysis (FEA) is an in silico technique that provides an alternative to strain gauge measurements when investigating how the cranium deforms under certain loading conditions. FEA has been used to analyse cranial stresses and strains resulting from masticatory loads in a wide range of taxa [26][27][28][29][30][31][32][33][34][35] . In addition, FEA can be integrated with multi-body dynamic analysis (MDA) to inform the FEA with kinetic data associated with various forms of mastication 29,34,36,37 . ...
... A similar process was also used to determine and visualise the dominant principal strains over all bites. The FE analyses were evaluated by considering von Mises strain because it has been employed previously to assess skull biomechanics 29,31,35,54 . In addition, von Mises strain is convenient because it is a scalar function combining the three principal strains, is related to the von Mises failure criterion, and is useful for comparing the performance of complex three-dimensional geometries. ...
Although a functional relationship between bone structure and mastication has been shown in some regions of the rabbit skull, the biomechanics of the whole cranium during mastication have yet to be fully explored. In terms of cranial biomechanics, the rabbit is a particularly interesting species due to its uniquely fenestrated rostrum, the mechanical function of which is debated. In addition, the rabbit processes food through incisor and molar biting within a single bite cycle, and the potential influence of these bite modes on skull biomechanics remains unknown. This study combined the in silico methods of multi-body dynamics and finite element analysis to compute musculoskeletal forces associated with a range of incisor and molar biting, and to predict the associated strains. The results show that the majority of the cranium, including the fenestrated rostrum, transmits masticatory strains. The peak strains generated over all bites were found to be attributed to both incisor and molar biting. This could be a consequence of a skull shape adapted to promote an even strain distribution for a combination of infrequent incisor bites and cyclic molar bites. However, some regions, such as the supraorbital process, experienced low peak strain for all masticatory loads considered, suggesting such regions are not designed to resist masticatory forces.
