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Prokinesis, a mode of avian cranial kinesis involving motion between the neurocranium and upper beak, has long been investigated in biomechanical analyses of avian feeding and drinking. However, the modern avian beak is also used for non-feeding functions. Here, we investigate the dual function of prokinesis in the feeding and locomotor systems of the rosy-faced lovebird (Agapornis roseicollis). Lovebirds and other parrots utilize their beak both during feeding and as a third limb during vertical climbing. Thus, we experimentally measured both force-generating potential and movement of the rosy-faced lovebird mandible and maxilla (via prokinetic flexion of the craniofacial hinge) during tripedal climbing and mandibular/maxillary adduction. We found that whereas the maxilla is primarily responsible for generating force during locomotion, the mandible is primarily responsible for generating force during forceful jaw adduction, hinting at a remarkable capacity to alter prokinetic function with differing neuromuscular control. The ability of the prokinetic apparatus to perform functions with competing optimality criteria via modulation of motor control illustrates the functional plasticity of the avian cranial kinesis and sheds new light on the adaptive significance of cranial mobility.

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The value of birds' ability to move the upper beak relative to the braincase has been shown in vital tasks like feeding and singing. In woodpeckers, such cranial kinesis has been thought to hinder pecking as delivering forceful blows calls for a head functioning as a rigid unit. Here, we tested whether cranial kinesis is constrained in woodpeckers by comparing upper beak rotation during their daily activities such as food handling, calling and gaping with those from closely related species that also have a largely insectivorous diet but do not peck at wood. Both woodpeckers and non-woodpecker insectivores displayed upper beak rotations of up to 8 degrees. However, the direction of upper beak rotation differed significantly between the two groups, with woodpeckers displaying primarily depressions and non-woodpeckers displaying elevations. The divergent upper beak rotation of woodpeckers may be caused either by anatomical modifications to the craniofacial hinge that reduce elevation, by the caudal orientation of the mandible depressor muscle forcing beak depressions, or by both. Our results suggest that pecking does not result in plain rigidification at the upper beak's basis of woodpeckers, but it nevertheless significantly influences the way cranial kinesis is manifested.

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The independent movements and flexibility of various parts of the skull, called cranial kinesis, are an evolutionary innovation that is found in living vertebrates only in some squamates and crown birds and is considered to be a major factor underpinning much of the enormous phenotypic and ecological diversity of living birds, the most diverse group of extant amniotes. Compared to the postcranium, our understanding of the evolutionary assemblage of the characteristic modern bird skull has been hampered by sparse fossil records of early cranial materials, with competing hypotheses regarding the evolutionary development of cranial kinesis among early members of the avialans. Here, a detailed three-dimensional reconstruction of the skull of the Early Cretaceous enantiornithine Yuanchuavis kompsosoura allows for its in-depth description, including elements that are poorly known among early-diverging avialans but are central to deciphering the mosaic assembly of features required for modern avian cranial kinesis. Our reconstruction of the skull shows evolutionary and functional conservation of the temporal and palatal regions by retaining the ancestral theropod dinosaurian configuration within the skull of this otherwise derived and volant bird. Geometric morphometric analysis of the palatine suggests that loss of the jugal process represents the first step in the structural modifications of this element leading to the kinetic crown bird condition. The mixture of plesiomorphic temporal and palatal structures together with a derived avialan rostrum and postcranial skeleton encapsulated in Yuanchuavis manifests the key role of evolutionary mosaicism and experimentation in early bird diversification.

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Background: The leporid lagomorphs (rabbits and hares) are adapted to running and leaping (some more than others) and consequently have unique anatomical features that distinguish them from ochotonid lagomorphs (pikas) and from their rodent relatives. Two traits that have received some attention are fenestration of the lateral wall of the maxilla and facial tilting. These features are known to correlate with specialised locomotory form in that the faster running species will generally have fenestration that occupies the dorsal and the anteroventral surface of the maxillary corpus and a more acute facial tilt angle. Another feature is an intracranial joint that circumscribes the back of the skull, thought to facilitate skull mobility. This joint separates the anterior portion of the cranium (including the dentition, rostrum and orbit) from the posterior portion of the cranium (which encompasses the occipital and the auditory complex). Aside from the observation that the intracranial joint is absent in pikas (generalist locomotors) and appears more elaborate in genera with cursorial and saltatorial locomotory habits, the evolutionary history, biomechanical function and comparative anatomy of this feature in leporids lacks a comprehensive evaluation. Methodology: The present work analysed the intracranial joint, facial tilting and lateral fenestration of the wall of the maxilla in the context of leporid evolutionary history using a Bayesian inference of phylogeny (18 genera, 23 species) and ancestral state reconstruction. These methods were used to gather information about the likelihood of the presence of these three traits in ancestral groups. Results: Our phylogenetic analyses found it likely that the last common ancestor of living leporids had some facial tilting, but that the last common ancestor of all lagomorphs included in the dataset did not. We found that it was likely that the last common ancestor of living leporids had fenestration that occupies the dorsal, but not the anteroventral, surface of the maxillary corpus. We also found it likely that the last common ancestor of living leporids had an intracranial joint, but that the last common ancestor of all living lagomorphs did not. These findings provide a broader context to further studies of evolutionary history and will help inform the formulation and testing of functional hypotheses.

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The skull of a woodpecker is hypothesized to serve as a shock absorber that minimizes the harmful deceleration of its brain upon impact into trees1-11 and has inspired the engineering of shock-absorbing materials12-15 and tools, such as helmets.16 However, this hypothesis remains paradoxical since any absorption or dissipation of the head's kinetic energy by the skull would likely impair the bird's hammering performance4 and is therefore unlikely to have evolved by natural selection. In vivo quantification of impact decelerations during pecking in three woodpecker species and biomechanical models now show that their cranial skeleton is used as a stiff hammer to enhance pecking performance, and not as a shock-absorbing system to protect the brain. Numerical simulations of the effect of braincase size and shape on intracranial pressure indicate that the woodpeckers' brains are still safe below the threshold of concussions known for primate brains. These results contradict the currently prevailing conception of the adaptive evolution of cranial function in one of nature's most spectacular behaviors. VIDEO ABSTRACT.

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Changes to feeding structures are a fundamental component of the vertebrate transition from water to land. Classically, this event has been characterized as a shift from an aquatic, suction-based mode of prey capture involving cranial kinesis to a biting-based feeding system utilizing a rigid skull capable of capturing prey on land. Here we show that a key intermediate, Tiktaalik roseae, was capable of cranial kinesis despite significant restructuring of the skull to facilitate biting and snapping. Lateral sliding joints between the cheek and dermal skull roof, as well as independent mobility between the hyomandibula and palatoquadrate, enable the suspensorium of T. roseae to expand laterally in a manner similar to modern alligator gars and polypterids. This movement can expand the spiracular and opercular cavities during feeding and respiration, which would direct fluid through the feeding apparatus. Detailed analysis of the sutural morphology of T. roseae suggests that the ability to laterally expand the cheek and palate was maintained during the fish-to-tetrapod transition, implying that limited cranial kinesis was plesiomorphic to the earliest limbed vertebrates. Furthermore, recent kinematic studies of feeding in gars demonstrate that prey capture with lateral snapping can synergistically combine both biting and suction, rather than trading off one for the other. A "gar-like" stage in early tetrapod evolution might have been an important intermediate step in the evolution of terrestrial feeding systems by maintaining suction-generation capabilities while simultaneously elaborating a mechanism for biting-based prey capture.

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The extinct nonavian dinosaur Tyrannosaurus rex, considered one of the hardest biting animals ever, is often hypothesized to have exhibited cranial kinesis, or, mobility of cranial joints relative to the braincase. Cranial kinesis in T. rex is a biomechanical paradox in that forcefully biting tetrapods usually possess rigid skulls instead of skulls with movable joints. We tested the biomechanical performance of a tyrannosaur skull using a series of static positions mimicking possible excursions of the palate to evaluate Postural Kinetic Competency in Tyrannosaurus. A functional extant phylogenetic bracket was employed using taxa, which exhibit measurable palatal excursions: Psittacus erithacus (fore-aft movement) and Gekko gecko (mediolateral movement). Static finite element models of Psittacus, Gekko, and Tyrannosaurus were constructed and tested with different palatal postures using anatomically informed material properties, loaded with muscle forces derived from dissection, phylogenetic bracketing, and a sensitivity analysis of muscle architecture and tested in orthal biting simulations using element strain as a proxy for model performance. Extant species models showed lower strains in naturally occurring postures compared to alternatives. We found that fore-aft and neutral models of Tyrannosaurus experienced lower overall strains than mediolaterally shifted models. Protractor muscles dampened palatal strains, while occipital constraints increased strains about palatocranial joints compared to jaw joint constraints. These loading behaviors suggest that even small excursions can strain elements beyond structural failure. Thus, these postural tests of kinesis, along with the robusticity of other cranial features, suggest that the skull of Tyrannosaurus was functionally akinetic. Anat Rec, 303:999-1017, 2020. © 2019 Wiley Periodicals, Inc.

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Most living birds exhibit cranial kinesis-movement between the rostrum and braincase-in which force is transferred through the palatal and jugal bars. The palate alone distinguishes the Paleognathae from the Neognathae, with cranial kinesis more developed in neognaths. Most previous palatal studies were based on 2D data and rarely incorporated data from stem birds despite great interest in their kinetic abilities. Here we reconstruct the vomer of the Early Cretaceous stem bird Sapeornis and the troodontid Sinovenator, taxa spanning the dinosaur-bird transition. A 3D shape analysis including these paravians and an extensive sampling of neornithines reveals their strong similarity to paleognaths and indicates that morphological differences in the vomer between paleognaths and neognaths are intimately related to their different kinetic abilities. These results suggest the skull of Mesozoic paravians lacked the kinetic abilities observed in neognaths, a conclusion also supported by our identification of an ectopterygoid in Sapeornis here. We conclude that cranial kinesis evolved relatively late, likely an innovation of the Neognathae, and is linked to the transformation of the vomer. This transformation increased palatal mobility, enabling the evolution of a diversity of kinetic mechanisms and ultimately contributing to the extraordinary evolutionary success of this clade.

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The planar, one degree of freedom (1-DoF) four-bar linkage is an important model for understanding the function, performance and evolution of numerous biomechanical systems. One such system is the opercular mechanism in fishes, which is thought to function like a four-bar linkage to depress the lower jaw. While anatomical and behavioral observations suggest some form of mechanical coupling, previous attempts to model the opercular mechanism as a planar four-bar have consistently produced poor model fits relative to observed kinematics. Using newly developed, open source mechanism fitting software, we fitted multiple three-dimensional (3D) four-bar models with varying DoF to in vivo kinematics in largemouth bass to test whether the opercular mechanism functions instead as a 3D four-bar with one or more DoF. We examined link position error, link rotation error and the ratio of output to input link rotation to identify a best-fit model at two different levels of variation: for each feeding strike and across all strikes from the same individual. A 3D, 3-DoF four-bar linkage was the best-fit model for the opercular mechanism, achieving link rotational errors of less than 5%. We also found that the opercular mechanism moves with multiple degrees of freedom at the level of each strike and across multiple strikes. These results suggest that active motor control may be needed to direct the force input to the mechanism by the axial muscles and achieve a particular mouth-opening trajectory. Our results also expand the versatility of four-bar models in simulating biomechanical systems and extend their utility beyond planar or single-DoF systems.

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Archosaurs, like all vertebrates, have different types of joints that allow or restrict cranial kinesis, such as synovial joints and fibrous joints. In general, synovial joints are more kinetic than fibrous joints, because the former possess a fluid-filled cavity and articular cartilage that facilitate movement. Even though there is a considerable lack of data on the microstructure and the structure-function relationships in the joints of extant archosaurs, many functional inferences of cranial kinesis in fossil archosaurs have hinged on the assumption that elongated condylar joints are (i) synovial and/or (ii) kinetic. Cranial joint microstructure was investigated in an ontogenetic series of American alligators, Alligator mississippiensis All the presumably synovial, condylar joints found within the head of the American alligator (the jaw joint, otic joint and laterosphenoid-postorbital (LS-PO) joint) were studied by means of paraffin histology and undecalcified histology paired with micro-computed tomography data to better visualize three-dimensional morphology. Results show that among the three condylar joints of A. mississippiensis, the jaw joint was synovial as expected, but the otherwise immobile otic and LS-PO joints lacked a synovial cavity. Therefore, condylar morphology does not always imply the presence of a synovial articulation nor mobility. These findings reveal an undocumented diversity in the joint structure of alligators and show that crocodylians and birds build novel, kinetic cranial joints differently. This complicates accurate identification of synovial joints and functional inferences of cranial kinesis in fossil archosaurs and tetrapods in general.

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The evolution of avian cranial kinesis is a phenomenon in part responsible for the remarkable diversity of avian feeding adaptations observable today. Although osteological, developmental and behavioral features of the feeding system are frequently studied, comparatively little is known about cranial joint skeletal tissue composition and morphology from a microscopic perspective. These data are key to understanding the developmental, biomechanical and evolutionary underpinnings of kinesis. Therefore, here we investigated joint microstructure in juvenile and adult mallard ducks (Anas platyrhynchos; Anseriformes). Ducks belong to a diverse clade of galloanseriform birds, have derived adaptations for herbivory and kinesis, and are model organisms in developmental biology. Thus, new insights into their cranial functional morphology will refine our understanding of avian cranial evolution. A total of five specimens (two ducklings and three adults) were histologically sampled, and two additional specimens (a duckling and an adult) were subjected to micro-computed tomographic scanning. Five intracranial joints were sampled: the jaw joint (quadrate-articular); otic joint (quadrate-squamosal); palatobasal joint (parasphenoid-pterygoid); the mandibular symphysis (dentary-dentary); and the craniofacial hinge (a complex flexion zone involving four different pairs of skeletal elements). In both the ducklings and adults, the jaw, otic and palatobasal joints are all synovial, with a synovial cavity and articular cartilage on each surface (i.e. bichondral joints) ensheathed in a fibrous capsule. The craniofacial hinge begins as an ensemble of patent sutures in the duckling, but in the adult it becomes more complex: laterally it is synovial; whereas medially, it is synostosed by a bridge of chondroid bone. We hypothesize that it is chondroid bone that provides some of the flexible properties of this joint. The heavily innervated mandibular symphysis is already fused in the ducklings and remains as such in the adult. The results of this study will serve as reference for documenting avian cranial kinesis from a microanatomical perspective. The formation of: (i) secondary articular cartilage on the membrane bones of extant birds; and (ii) their unique ability to form movable synovial joints within two or more membrane bones (i.e. within their dermatocranium) might have played a role in the origin and evolution of modern avian cranial kinesis during dinosaur evolution.

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The zygoma (called jugal bar) in modern birds accounts for a large portion of the ventral margin of the cranium. As a delicate and rod-like element, the jugal bar is functionally integrated into the avian cranial kinesis, a unique property that allows the beak to be elevated or depressed with respect to the braincase and thus distinguishes birds from all other modern vertebrates. Developmental studies show that the jugal bar of modern birds is formed by the fusion of the jugal and quadratojugal that are ossified from separated centers. However, those two bones are unfused and exhibit complicated morphological variations in basal birds and their dinosaurian relatives. Moreover, the jugal and quadratojugal form rigid articulations with the postorbital and squamosal, respectively, consequently hindering the movement of the upper jaw in most non-avian dinosaurs and some basal birds. A comparative study of the jugal and quadratojugal morphology of basal birds and their close relatives such as dromaeosaurids and oviraptorids elucidates how modern birds has achieved its derived jugal bar morphology, and sheds light on the evolution of the postorbital configuration of birds. We propose that numerous morphological modifications of those two elements (morphology changes and reduced articulation with other elements) took place in early bird history, and some of them pertinent to the refinement of the cranial kinesis. Anat Rec, 300:62-75, 2017. © 2016 Wiley Periodicals, Inc.

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Chewing, characterized by shearing jaw motions and high-crowned molar teeth, is considered an evolutionary innovation that spurred dietary diversification and evolutionary radiation of mammals. Complex prey-processing behaviours have been thought to be lacking in fishes and other vertebrates, despite the fact that many of these animals feed on tough prey, like insects or even grasses. We investigated prey capture and processing in the insect-feeding freshwater stingray Potamotrygon motoro using high-speed videography. We find that Potamotrygon motoro uses asymmetrical motion of the jaws, effectively chewing, to dismantle insect prey. However, CT scanning suggests that this species has simple teeth. These findings suggest that in contrast to mammalian chewing, asymmetrical jaw action is sufficient for mastication in other vertebrates. We also determined that prey capture in these rays occurs through rapid uplift of the pectoral fins, sucking prey beneath the ray's body, thereby dissociating the jaws from a prey capture role. We suggest that the decoupling of prey capture and processing facilitated the evolution of a highly kinetic feeding apparatus in batoid fishes, giving these animals an ability to consume a wide variety of prey, including molluscs, fishes, aquatic insect larvae and crustaceans. We propose Potamotrygon as a model system for understanding evolutionary convergence of prey processing and chewing in vertebrates.

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Many musculoskeletal systems, including the skulls of birds, fishes, and some lizards consist of interconnected chains of mobile skeletal elements, analogous to linkage mechanisms used in engineering. Biomechanical studies have applied linkage models to a diversity of musculoskeletal systems, with previous applications primarily focusing on two-dimensional linkage geometries, bilaterally symmetrical pairs of planar linkages, or single four-bar linkages. Here, we present new, three-dimensional (3D), parallel linkage models of the skulls of birds and fishes and use these models (available as free kinematic simulation software), to investigate structure-function relationships in these systems. This new computational framework provides an accessible and integrated workflow for exploring the evolution of structure and function in complex musculoskeletal systems. Linkage simulations show that kinematic transmission, although a suitable functional metric for linkages with single rotating input and output links, can give misleading results when applied to linkages with substantial translational components or multiple output links. To take into account both linear and rotational displacement we define force mechanical advantage for a linkage (analogous to lever mechanical advantage) and apply this metric to measure transmission efficiency in the bird cranial mechanism. For linkages with multiple, expanding output points we propose a new functional metric, expansion advantage, to measure expansion amplification and apply this metric to the buccal expansion mechanism in fishes. Using the bird cranial linkage model, we quantify the inaccuracies that result from simplifying a 3D geometry into two dimensions. We also show that by combining single-chain linkages into parallel linkages, more links can be simulated while decreasing or maintaining the same number of input parameters. This generalized framework for linkage simulation and analysis can accommodate linkages of differing geometries and configurations, enabling novel interpretations of the mechanics of force transmission across a diversity of vertebrate feeding mechanisms and enhancing our understanding of musculoskeletal function and evolution. J. Morphol. 277:1570-1583, 2016. © 2016 Wiley Periodicals, Inc.

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Cranial kinesis of the avian beak is complex; particularly in birds with prokinetic beak movement, such as psittacine birds. A number of diseases can result in damage to the bony and soft tissue structures of the beak and can lead to secondary pathology, such as beak deviation, abnormal rhamphothecal growth and wear, and opportunistic infections. A solid understanding of species-specific anatomic variations is essential before attempting rhamphothecal restoration or surgical repair. Many diseases of the oral cavity can appear similar on initial clinical evaluation and therefore warrant appropriate diagnostic testing.

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Background. Syngnathid fishes produce three kinds of sounds, named click, growl and purr. These sounds are generated by different mechanisms to give a consistent signal pattern or signature which is believed to play a role in intraspecific and interspecific communication. Commonly known sounds are produced when the fish feeds (click, purr) or is under duress (growl). While there are more acoustic studies on seahorses, pipefishes have not received much attention. Here we document the differences in feeding click signals between three species of pipefishes and relate them to cranial morphology and kinesis, or the sound-producing mechanism. Methods. The feeding clicks of two species of freshwater pipefishes, Doryichthys martensii and Doryichthys deokhathoides and one species of estuarine pipefish, Syngnathoides biaculeatus, were recorded by a hydrophone in acoustic dampened tanks. The acoustic signals were analysed using time-scale distribution (or scalogram) based on wavelet transform. A detailed time-varying analysis of the spectral contents of the localized acoustic signal was obtained by jointly interpreting the oscillogram, scalogram and power spectrum. The heads of both Doryichthys species were prepared for microtomographical scans which were analysed using a 3D imaging software. Additionally, the cranial bones of all three species were examined using a clearing and double-staining method for histological studies. Results. The sound characteristics of the feeding click of the pipefish is species-specific, appearing to be dependent on three bones: the supraoccipital, 1st postcranial plate and 2nd postcranial plate. The sounds are generated when the head of the Dorichthyes pipefishes flexes backward during the feeding strike, as the supraoccipital slides backwards, striking and pushing the 1st postcranial plate against (and striking) the 2nd postcranial plate. In the Syngnathoides pipefish, in the absence of the 1st postcranial plate, the supraoccipital rubs against the 2nd postcranial plate twice as it is pulled backward and released on the return. Cranial morphology and kinesis produce acoustic signals consistent with the bone strikes that produce sharp energy spikes (discrete or merged), or stridulations between bones that produce repeated or multimodal sinusoidal waveforms. Discussion. The variable structure of the sound-producing mechanism explains the unique acoustic signatures of the three species of pipefish. The differences in cranial bone morphology, cranial kinesis and acoustic signatures among pipefishes (and seahorses) could be attributed to independent evolution within the Syngnathidae, which warrants further investigation.