The temporal ligaments and their bearing on cranial kinesis in lizards

In the lateral temporal opening of the lacertilian skull there are three main types of ligaments: quadratojugal, jugomandibular, and quadratopostfrontal. The quadratojugal and ventral jugomandibular ligaments transmit the retraction force from the lower jaw to the rhinal unit of the maxillary segment. The dorsal jugomandibular ligament causes the coupled kinesis, that results in the protraction of the whole maxillary segment (in the amphikinetic skull with simple streptostyly) or in the protraction of the quadrate-mandibular complex (in the hyperstreptostylic skull), when opening the mouth.     

The role of cranial kinesis in birds.

In birds, the ability to move the upper beak relative to the braincase has been the subject of many functional morphological investigations, but in many instances the adaptive significance of cranial kinesis remains unclear. Alternatively, cranial kinesis may be considered a consequence of the general design of the skull, rather than an adaptive trait as such. The present study reviews some results related to the mechanism and functional significance of cranial kinesis in birds. Quantitative three-dimensional X-ray has shown that in skulls morphologically as divers as paleognaths and neognaths the mechanism for elevation of the upper beak is very similar. One of the mechanisms proposed for avian jaw movement is a mechanical coupling of the upper and the lower jaw movement by the postorbital ligament. Such a mechanical coupling would necessitate upper beak elevation. However, independent control of upper and lower jaw has been shown to occur during beak movements in birds. Moreover, kinematic modeling and force measurements suggests that the maximum extensibility of collagen, in combination with the short distance of the insertion of the postorbital ligament to the quadrato-mandibular articulation do not constitute a block to lower jaw depression. The lower jaw ligaments serve to limit the maximal extension of the mandibula. It is suggested here that cranial kinesis in avian feeding may have evolved as a consequence of an increase in eye size. This increase in size led to a reduction of bony bars in the lateral aspect of the skull enabling the transfer of quadrate movement to the upper jaw. The selective forces favoring the development of a kinetic upper beak in birds may be subtle and act in different ecological contexts. Simultaneous movement of the upper and lower jaw not only increases the velocity of beak movements, but with elevated upper beak also less force is required to open the lower jaw. However, the penalty of increased mobility of elements in a lightweight skull and a large eye is potential instability of skull elements during biting, smaller bite forces and limitations on joint reaction forces. Such a lightly built, kinetic skull may have evolved in animals that feed on small plant material or insects. This type of food does not require the resistance of large external forces on the jaws as in carnivores eating large prey.     

Cranial kinesis in the amphibia: a review

All extant orders of amphibians are characterized by kinetic skulls. Main type of intracranial movability in amphibians is pleurokinetism, that is supplemented in different amphibian groups by various types of rhyncho- and prokinetism. The most primitive pattern of cranial kinesis is revealed in the stegocrotaphic gymnophions. More paedomorphic species retain general cranial flexibility that is characteristic of larval skull. That is unfavourable for evolution of well-regulated (adult) cranial kinesis and related feeding adaptations. Kinetism is also reduced in the species with heavily ossified skulls. Adaptive role and evolution of cranial kinesis in amphibians are discussed.     

Nonlinear dynamical model and response of avian cranial kinesis

All modern birds have kinetic skulls in which the upper bill can move relative to the braincase, but the biomechanics and motion dynamics of cranial kinesis in birds are poorly understood. In this paper, we model the dynamics of avian cranial kinesis, such as prokinesis and proximal rhynchokinesis in which the upper jaw pivots around the nasal-frontal (N-F) hinge. The purpose of this paper is to present to the biological community an approach that demonstrates the application of sophisticated predictive mathematical modeling tools to avian kinesis. The generality of the method, however, is applicable to the advanced study of the biomechanics of other skeletal systems. The paper begins with a review of the relevant biological literature as well as the essential morphology of avian kinesis, especially the mechanical coupling of the upper and lower jaw by the postorbital ligament. A planar model of the described bird jaw morphology is then developed that maintains the closed kinematic topology of the avian jaw mechanism. We then develop the full nonlinear equations of motion with the assumption that the M. protractor pterygoideus and M. depressor mandibulae act on the quadrate as a pure torque, and the nasal frontal hinge is elastic with damping. The mechanism is shown to be a single degree of freedom device due to the holonomic constraints present in the quadrate-jugal bar-upper jaw-braincase-quadrate kinematic chain as well as the quadrate-lower jaw-postorbital ligament-braincase-quadrate kinematic chain. The full equations are verified via simulation and animation using the parameters of a Grey Heron (Ardea cinerea). Next we develop a simplified analytical model of the equations by power series expansion. We demonstrate that this model reproduces the dynamics of the full model to a high degree of fidelity. We proceed to use the harmonic balance technique to develop the frequency response characteristics of the jaw mechanism. It is shown that this avian cranial kinesis model exhibits the characteristics of a hardening Duffing oscillator. Beyond the identification of the characteristics of the underlying dynamics, which provides insight into the behavior of the system, the model and methodology presented here provides other potential benefits. A framework has been developed that could be utilized to study the biomechanics of feeding and bite force as well the effects of cranial kinesis on the frequency and modulation of bird songs.     

The trigeminal jaw adductors of primitive snakes and their homologies with the lacertilian jaw adductors

The trigeminal jaw adductor musculature of anilioid snakes is analysed. The group is characterised by primitive characters, viz. the presence of an extensive bodenaponeurosis and of a quadrate aponeurosis. A temporal tendon gives rise to superficial (lb) fibres which are not observed in other snakes: this may be a primitive or a derived feature.
Jaw adductor muscles in snakes are usually subdivided following their relative position in an antero–posterior direction. Lacertilian jaw adductors are subdivided in a transverse plane. A detailed comparison of the anilioid and primitive lacertilian jaw adductors establishes correspondences (homologies) of parts in the transverse plane in both groups. These homologies are corroborated by innervational patterns.
Platynotan lizards are widely accepted as potential snake ancestors. A comparison of homologue jaw adductors shows different evolutionary trends to characterise platynotan lizards and snakes. Theoretically, these findings do not rule out primitive platynotan lizards as snake ancestors. On the basis of the structure of jaw adductors, snakes are to be derived from a primitive lacertilian pattern, be it platynotan or not.     

On the structural adaptations of the bill, skull-elements, tongue, and hyoid of some Indian insect-eating birds

The study of the functional morphology of the feeding apparatus of some Indian insect-eating birds reveals suitable adaptational changes in the structure of their bill, skull-elements, tongue, and byoid in different degrees, depending on the nature of their partial adaptation to secondary food-habits. The hooked tip of the upper beak in Muscicapa and Dicrurus, sharp tomial edges of both the beaks in Turdoides and the long, gradually curved bill in Merops are some of the suitable adaptations of the bill for food-getting. The dimensional variations of the skull and its kinetic elements may be correlated not only with the food-habits of birds studied, but also with the patterns of jaw and tongue muscles possessed by them. A comparatively greater width of the cranium and height of the lower jaw in Turdoides and Dicrurus provide wider areas for the origins and insertions of the adductor muscles. The skull in all the birds studied is pro-kinetic. The kinesis of the upper jaw, however, depends on several factors of which the angles of placement of the quadrate-pterygoid-palatine components, the nature of the naso-frontal hinge and the resultant "torques" produced by differential forces of muscles are very significant. The upper jaw kinesis is best developed in Merops and Orthotomus. The variations in the structure of the tongue and hyoid may also be correlated with various movements of the tongue in both primary and secondary food-adaptations.     

The loss of the lower temporal arcade in diapsid reptiles

The fossil record of diapsid reptiles does not provide conclusive evidence that the loss of the lower temporal arcade is correlated with the development of streptostyly. Analysis of the structure of the external jaw adductor in extant lizards results in the formulation of an alternative hypothesis to explain the loss of the lower temporal arcade in lepidosaurs. Extant lizards show the development of a posteroventral portion of the superficialis layer (lb) of the external adductor, which invades the lateral surface of the lower jaw, thus escaping the original confines of the external adductor. The development and expansion of a posteroventral lb muscle would have to be correlated with the loss of at least the posterior portion of the lower temporal arcade. Fossil lepidosaurs such as Clevosaurus, Prolacerta and Macrocnemus show the reduction of the lower temporal arcade from back to front, which is consistent with the hypothesis of the development of a posteroventral lb muscle.     

Biomechanics of cranial kinesis in birds: Testing linkage models in the white-throated sparrow (Zonotrichia albicollis)

Cranial kinesis in sparrows refers to the rotation of the upper jaw around its kinetic joint with the braincase. Avian jaw mechanics may involve the coupled motions of upper and lower jaws, in which the postorbital ligament transfers forces from the lower jaw, through the quadrate, pterygoid, and jugal bones, to the upper jaw. Alternatively, jaw motions may be uncoupled, with the upper jaw moving independently of the lower jaw. We tested hypotheses of cranial kinesis through the use of quantitative computer models. We present a biomechanical model of avian jaw kinetics that predicts the motions of the jaws under assumptions of both a coupled and an uncoupled mechanism. In addition, the model predicts jaw motions under conditions of force transfer by either the jugal or the pterygoid bones. Thus four alternative models may be tested using the proposed model (coupled jugal, coupled pterygoid, uncoupled jugal, uncoupled pterygoid). All models are based on the mechanics of four-bar linkages and lever systems and use morphometric data on cranial structure as the basis for predicting cranial movements. Predictions of cranial motions are tested by comparison to kinematics of white-throated sparrows (Zonotrichia albicollis) during singing. The predicted relations between jaw motions for the coupled model are significantly different from video observations. We conclude that the upper and lower jaws are not coupled in white-throated sparrows. The range of jaw motions during song is consistent with a model in which independent contractions of upper and lower jaw muscles control beak motion. © 1996 Wiley-Liss, Inc.     

A new stem craniate from the Ordovician of Morocco and the search for the sister group of the craniata

The investigation of the development of the trigeminal jaw adductor musculature in the turtle Chelydra serpentina documents the early aggregation of muscle rudiments around the innervating nerve branches, probably a consequence of inductive interaction. This may explain the early continuity of the intramandibularis with the intermandibularis muscle. Several aspects of muscle development differ in the turtle as compared to lizards. These differences highlight the fact that conjectures of homology, based on a static topographical correspondence of adult structures, cannot capture the dynamics of the developmental process. The intramandibularis muscle of turtles, comparable to that of crocodiles, represents a plesiomorphous structure which is not homologous to the intramandibularis muscle of lacertoid lizards, a derived feature of the Lacertoidea. A derived feature of the chelonian jaw adductor musculature is the posterodorsal expansion of the external adductor along a supraoccipital crest, developing according to a pattern of Haeckelian recapitulation. Muscle development serves to corroborate the concept of a monophyletic Eureptilia, including diapsids and synapsids, as opposed to the (paraphyletic) Anapsida. The impact of the differentiation of the external adductor into a pulley system on cranial kinesis is analysed in biomechanical terms.     

The structure and development of the jaw adductor musculature in the turtle Chelydra serpentina

The investigation of the development of the trigeminal jaw adductor musculature in the turtle Chelydra serpentina documents the early aggregation of muscle rudiments around the innervating nerve branches, probably a consequence of inductive interaction. This may explain the early continuity of the intramandibularis with the intermandibularis muscle. Several aspects of muscle development differ in the turtle as compared to lizards. These differences highlight the fact that conjectures of homology, based on a static topographical correspondence of adult structures, cannot capture the dynamics of the developmental process. The intramandibularis muscle of turtles, comparable to that of crocodiles, represents a plesiomorphous structure which is not homologous to the intramandibularis muscle of lacertoid lizards, a derived feature of the Lacertoidea. A derived feature of the chelonian jaw adductor musculature is the posterodorsal expansion of the external adductor along a supraoccipital crest, developing according to a pattern of Haeckelian recapitulation. Muscle development serves to corroborate the concept of a monophyletic Eureptilia, including diapsids and synapsids, as opposed to the (paraphyletic) Anapsida. The impact of the differentiation of the external adductor into a pulley system on cranial kinesis is analysed in biomechanical terms.     

THE ONTOGENY OF THE CRANIAL BONES, CRANIAL PERIPHERAL AND CRANIAL PARASYMPATHETIC NERVES, TOGETHER WITH A STUDY OF THE VISCERAL MUSCLES OF STRUTHIO

Abstract The skull of Struthio is typically avian. There are, however, many cranial features that are neotenic in relation to the other Dromaeognathae and Neognathae. The premaxillary-vomer arthrosis is present in the embryo of Struthio but is absent in the adult; it is present in the adults of the other Dromaeognathae; the trabeculo-capsular entity is uninterrupted: therefore, there is no mesokinetic joint; kinesis, as a result, is limited. No orbitosphenoid present; septum ossifies as mesethmoid which appears on the dorsal surface. There are only two circumorbital bones present: the lacrimal and the jugal. The auditory region has only two centres of ossification: the prootic and opisthotic. The quadrate has a single elongated condyle of the processus oticus which articulates with the prootic and squamosal. The cranial base is ossified as the basioccipital and basisphenoid, the latter being of mixed origin. There are five dermal bones in the lower jaw of Struthio ; the gonial is present. The trigeminus musculature is reduced and shows very definite neotenic features. The peripheral cranial nerves are typically avian. The cranial parasympathetic nerves are well developed in the embryo but show definite signs of resorption in the later stages of development. The hyoid apparatus is mainly cartilaginous; the hyoid musculature is reduced.     

Variation in the cranium shape of wall lizards (Podarcis spp.): effects of phylogenetic constraints, allometric constraints and ecology

We used geometric morphometrics to explore the influence of phylogenetic and allometric constraints as well as ecology on variation in cranium shape in five species of monophyletic, morphologically similar Podarcis lizards (Podarcis erhardii, Podarcis melisellensis, Podarcis muralis, Podarcis sicula and Podarcis taurica). These species belong to different clades, they differ in their habitat preferences and can be classified into two distinct morphotypes: saxicolous and terrestrial. We found (i) no phylogenetic signal in cranium shape, (ii) diverging allometric slopes among species, and (iii) a significant effect of habitat on cranium shape. The saxicolous species (P. erhardii and P. muralis) had crania with elongated parietals, elongated cranium bases, shortened anterior parts of the dorsal cranium, reduced chambers of the jaw adductor muscles and larger subocular foramina. These cranial features are adaptations that compensate for a flattened cranium, dwelling on vertical surfaces and seeking refuge in crevices. The crania of the terrestrial species (P. melisellensis, P. sicula and P. taurica) tended to be more elongate and robust, with enlarged chambers of the jaw adductor muscle, reduced skull bases and shortened parietals. Terrestrial species exhibited more variation in cranium shape than saxicolous species. Our study suggests that shape variation in Podarcis sp. lizards is largely influenced by ecology, which likely affects species-specific patterns of static allometry.     

A new psittacosaur from Inner Mongolia and the parrot-like structure and function of the psittacosaur skull

We describe a new species of psittacosaur, Psittacosaurus gobiensis, from the Lower Cretaceous of Inner Mongolia and outline a hypothesis of chewing function in psittacosaurs that in many respects parallels that in psittaciform birds. Cranial features that accommodate increased bite force in psittacosaurs include an akinetic skull (both cranium and lower jaws) and differentiation of adductor muscle attachments comparable to that in psittaciform birds. These and other features, along with the presence of numerous large gastroliths, suggest that psittacosaurs may have had a high-fibre, nucivorous (nut-eating) diet.Psittacosaurs, alone among ornithischians, generate oblique wear facets from tooth-to-tooth occlusion without kinesis in either the upper or lower jaws. This is accomplished with a novel isognathous jaw mechanism that combines aspects of arcilineal (vertical) and propalinal (horizontal) jaw movement. Here termed clinolineal (inclined) jaw movement, the mechanism uses posteriorly divergent tooth rows, rather than kinesis, to gain the added width for oblique occlusion. As the lower tooth rows are drawn posterodorsally into occlusion, the increasing width between the upper tooth rows accommodates oblique shear. With this jaw mechanism, psittacosaurs were able to maintain oblique shearing occlusion in an akinetic skull designed to resist high bite forces.     

Myological variability in a decoupled skeletal system: Batoid cranial anatomy

Chondrichthyans (sharks, batoids, and chimaeras) have simple feeding mechanisms owing to their relatively few cranial skeletal elements. However, the indirect association of the jaws to the cranium (euhyostylic jaw suspension) has resulted in myriad cranial muscle rearrangements of both the hyoid and mandibular elements. We examined the cranial musculature of an abbreviated phylogenetic representation of batoid fishes, including skates, guitarfishes and with a particular focus on stingrays. We identified homologous muscle groups across these taxa and describe changes in gross morphology across developmental and functional muscle groups, with the goal of exploring how decoupling of the jaws from the skull has effected muscular arrangement. In particular, we focus on the cranial anatomy of durophagous and nondurophagous batoids, as the former display marked differences in morphology compared to the latter. Durophagous stingrays are characterized by hypertrophied jaw adductors, reliance on pennate versus fusiform muscle fiber architecture, tendinous rather than aponeurotic muscle insertions, and an overall reduction in mandibular kinesis. Nondurophagous stingrays have muscles that rely on aponeurotic insertions onto the skeletal structure, and display musculoskeletal specialization for jaw protrusion and independent lower jaw kinesis, relative to durophagous stingrays. We find that among extant chondrichthyans, considerable variation exists in the hyoid and mandibular muscles, slightly less so in hypaxial muscles, whereas branchial muscles are overwhelmingly conserved. As chondrichthyans occupy a position sister to all other living gnathostomes, our understanding of the structure and function of early vertebrate feeding systems rests heavily on understanding chondrichthyan cranial anatomy. Our findings highlight the incredible variation in muscular complexity across chondrichthyans in general and batoids in particular. J. Morphol. 275:862–881, 2014. © 2014 Wiley Periodicals, Inc.     

Sexual dimorphism of skull shape in a lacertid lizard species (Podarcis spp., Dalmatolacerta sp., Dinarolacerta sp.) revealed by geometric morphometrics

Geometric morphometric techniques were used to examine allometric and non-allometric influences on sexual shape dimorphism (SShD) in the ventral cranium (skull base, palate and upper jaw) of four species of lacertid lizards (Podarcis muralis, Podarcis melisellensis, Dalmatolacerta oxycephala, Dinarolacerta mosorensis). These species differ in body shape, ecology and degree of phylogenetic relatedness. The structures of the ventral cranium that were studied are directly involved in the mechanics of feeding and are connected to the jaw musculature; these structures are potentially subject to both sexual and natural selection. Allometry accounted for a considerable degree of cranial shape variation between the sexes. Allometric shape changes between individuals with smaller cranium size and individuals with larger cranium size are mostly related to changes in the skull base showing pronounced negative allometry. The rostral part, however, either scaled isometrically or showed less pronounced negative allometry than the skull base. Non-allometric intersexual shape variation predominantly involved changes related to the jaw adductor muscle chamber, i.e., changes that are associated with biomechanically relevant traits of the jaw system in females and males. Both allometric and non-allometric shape changes appeared to be species-specific. Our results indicate that natural and sexual selection may be involved in the evolution of SShD.     

Evolutionary patterns of shape and functional diversification in the skull and jaw musculature of triggerfishes (Teleostei: Balistidae)

The robust skull and highly subdivided adductor mandibulae muscles of triggerfishes provide an excellent system within which to analyze the evolutionary processes underlying phenotypic diversification. We surveyed the anatomical diversity of balistid jaws using Procrustes‐based geometric morphometric analyses and a phylomorphospace approach to quantifying morphological transformation through evolution. We hypothesized that metrics of interspecific cranial shape would reveal patterns of phylogenetic diversification that are congruent with functional and ecological transformation. Morphological landmarks outlining skull and adductor mandibulae muscle shape were collected from 27 triggerfish species. Procrustes‐transformed skull shape configurations revealed significant phylogenetic and size‐influenced structure. Phylomorphospace plots of cranial shape diversity reveal groupings of shape between different species of triggerfish that are mostly consistent with phylogenetic relatedness. Repeated instances of convergence upon similar cranial shape by genetically disparate taxa are likely due to the functional demands of shared specialized dietary habits. This study shows that the diversification of triggerfish skulls occurs via modifications of cranial silhouette and the positioning of subdivided jaw adductor muscles. Using the morphometric data collected here as input to a biomechanical model of triggerfish jaw function, we find that subdivided jaw adductors, in conjunction with a unique cranial skeleton, have direct biomechanical consequences that are not always congruent with phylomorphospace patterns in the triggerfish lineage. The integration of geometric morphometrics with biomechanical modeling in a phylogenetic context provides novel insight into the evolutionary patterns and ecological role of muscle subdivisions in triggerfishes. J. Morphol. 277:737–752, 2016. © 2016 Wiley Periodicals, Inc.