Multi-layered bird beaks: a finite-element approach towards the role of keratin in stress dissipation

Soons, Joris; Herrel, Anthony; Genbrugge, Annelies; Adriaens, Dominique; Aerts, Peter; Dirckx, Joris J.J.

doi:10.1098/rsif.2011.0910

Cited by 33 publications

(47 citation statements)

References 32 publications

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“…An earlier study on Padda oryzivora [23] showed that changing the bone modulus value also had a linear effect, albeit small, on safety factor values (SFs changed from 2.5 to 3.0 if bone modulus changed from 6.7 to 7.9 GPa). Also, variation in the keratin modulus within its measured interval (Eker = 1.3 till 2.1 GPa) had a little effect on SF.…”

Section: Discussionmentioning

confidence: 99%

Is Beak Morphology in Darwin’s Finches Tuned to Loading Demands?

et al. 2015

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One of nature's premier illustrations of adaptive evolution concerns the tight correspondence in birds between beak morphology and feeding behavior. In seed-crushing birds, beaks have been suggested to evolve at least in part to avoid fracture. Yet, we know little about mechanical relationships between beak shape, stress dissipation, and fracture avoidance. This study tests these relationships for Darwin's finches, a clade of birds renowned for their diversity in beak form and function. We obtained anatomical data from micro-CT scans and dissections, which in turn informed the construction of finite element models of the bony beak and rhamphotheca. Our models offer two new insights. First, engineering safety factors are found to range between 1 and 2.5 under natural loading conditions, with the lowest safety factors being observed in species with the highest bite forces. Second, size-scaled finite element (FE) models reveal a correspondence between inferred beak loading profiles and observed feeding strategies (e.g. edge-crushing versus tip-biting), with safety factors decreasing for base-crushers biting at the beak tip. Additionally, we identify significant correlations between safety factors, keratin thickness at bite locations, and beak aspect ratio (depth versus length). These lines of evidence together suggest that beak shape indeed evolves to resist feeding forces.

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Section: Discussionmentioning

confidence: 99%

Is Beak Morphology in Darwin’s Finches Tuned to Loading Demands?

et al. 2015

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“…Validation experiments on the beaks of extant finches have shown that these assumptions yield high correlations between ex vivo experimental displacements and displacements from skull and beak FE models (R 2 = 0.97 for loading at the anterior rostrum, R 2 = 0.89 loading elsewhere along the beak). Thereby our methodology for FE model construction can be considered valid and biologically realistic (10).…”

Section: Methodsmentioning

confidence: 99%

“…Apparently freed from functional constraints associated with a carnivorous diet, this permitted diversification of skull and beak shapes, particularly among extant and extinct birds (9). Biomechanical studies on extant birds have indicated a functional benefit of rhamphothecae and beaks other than weight reduction (10,11). However, the functional role of edentulism and (keratinous) beaks in the evolution of herbivory from a macropredaceous heritage is still unclear.…”

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confidence: 99%

Edentulism, beaks, and biomechanical innovations in the evolution of theropod dinosaurs

Lautenschlager

Witmer

Altangerel

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

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Maniraptoriformes, the speciose group of derived theropod dinosaurs that ultimately gave rise to modern birds, display a diverse and remarkable suite of skeletal adaptations. Apart from the evolution of flight, a large-scale change in dietary behavior appears to have been one of the main triggers for specializations in the bauplan of these derived theropods. Among the different skeletal specializations, partial or even complete edentulism and the development of keratinous beaks form a recurring and persistent trend in from the evolution of derived nonavian dinosaurs. Therizinosauria is an enigmatic maniraptoriform clade, whose members display these and other osteological characters thought to be correlated with the shift from carnivory to herbivory. This makes therizinosaurians prime candidates to assess the functional significance of these morphological characters. Based on a highly detailed biomechanical model of Erlikosaurus andrewsi, a therizinosaurid from the Upper Cretaceous of Mongolia, different morphological configurations incorporating soft-tissue structures, such as a keratinous rhamphotheca, are evaluated for their biomechanical performance. Our results indicate that the development of beaks and the presence of a keratinous rhamphotheca would have helped to dissipate stress and strain, making the rostral part of the skull less susceptible to bending and displacement, and this benefit may extend to other vertebrate clades that possess rhamphothecae. Keratinous beaks, paralleled by edentulism, thus represent an evolutionary innovation developed early in derived theropods to enhance cranial stability, distinct to postulated mass-saving benefits associated with the origin of flight.functional morphology | computer modelling | finite element analysis T he evolution from nonavian to avian theropods (birds) is defined by a plethora of anatomical and functional specializations, many of which have been linked to the evolution of flight (1-3). However, several skeletal traits and adaptations, gradually acquired within distinct clades of Maniraptoriformes, appear to have been induced by or sparked dietary diversification (4). Many of these morphological characters are now thought to be closely associated with a trophic shift from carnivory to omnivory or herbivory (5-7) and are regarded as the result of correlated character evolution, occurring independently in three or perhaps as many as five lineages of Maniraptoriformes, suggesting a role of these characters in the functional acquisition of herbivory (4). Most obvious is the trend toward tooth reduction, which ultimately leads to partial or complete edentulism, and is paralleled by the appearance of a beak-like keratinous rhamphotheca. Edentulism has occurred independently multiple times in tetrapod history, usually accompanied by the abandonment of obligate carnivory (8). Apparently freed from functional constraints associated with a carnivorous diet, this permitted diversification of skull and beak shapes, particularly among extant and extinct birds (9). B...

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“…This allows the mechanical function of complex structures, such as the skull and the masticatory apparatus, to be studied in a non‐invasive way. The FE method has been used to investigate cranial morphology and feeding biomechanics in many taxa, including mammals, reptilian sauropsids, birds, and dinosaurs (e.g., Rayfield, ; Dumont et al, ; McHenry et al, ; Jasinoski et al, ; Tseng and Wang, ; Attard et al, ; Dumont et al, ; Cox et al, ; Oldfield et al, ; Soons et al, ; Young et al, ; Piras et al, ; Figueirido et al, ; Gill et al, ;).…”

Section: Introductionmentioning

confidence: 99%

Comparative finite element analysis of the cranial performance of four herbivorous marsupials

Sharp

2015

Journal of Morphology

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Marsupial herbivores exhibit a wide variety of skull shapes and sizes to exploit different ecological niches. Several studies on teeth, dentaries, and jaw adductor muscles indicate that marsupial herbivores exhibit different specializations for grazing and browsing. No studies, however, have examined the skulls of marsupial herbivores to determine the relationship between stress and strain, and the evolution of skull shape. The relationship between skull morphology, biomechanical performance, and diet was tested by applying the finite element method to the skulls of four marsupial herbivores: the common wombat (Vombatus ursinus), koala (Phascolarctos cinereus), swamp wallaby (Wallabia bicolor), and red kangaroo (Macropus rufus). It was hypothesized that grazers, requiring stronger skulls to process tougher food, would have higher biomechanical performance than browsers. This was true when comparing the koala and wallaby (browsers) to the wombat (a grazer). The cranial model of the wombat resulted in low stress and high mechanical efficiency in relation to a robust skull capable of generating high bite forces. However, the kangaroo, also a grazer, has evolved a very different strategy to process tough food. The cranium is much more gracile and has higher stress and lower mechanical efficiency, but they adopt a different method of processing food by having a curved tooth row to concentrate force in a smaller area and molar progression to remove worn teeth from the tooth row. Therefore, the position of the bite is crucial for the structural performance of the kangaroo skull, while it is not for the wombat which process food along the entire tooth row. In accordance with previous studies, the results from this study show the mammalian skull is optimized to resist forces generated during feeding. However, other factors, including the lifestyle of the animal and its environment, also affect selection for skull morphology to meet multiple functional demands.

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Multi-layered bird beaks: a finite-element approach towards the role of keratin in stress dissipation

Cited by 33 publications

References 32 publications

Is Beak Morphology in Darwin’s Finches Tuned to Loading Demands?

Is Beak Morphology in Darwin’s Finches Tuned to Loading Demands?

Edentulism, beaks, and biomechanical innovations in the evolution of theropod dinosaurs

Comparative finite element analysis of the cranial performance of four herbivorous marsupials

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