Gross morphology and topographical relationships of the hyobranchial apparatus and laryngeal cartilages in the ostrich (Struthio camelus)

The ostrich hyobranchial apparatus consists of the centrally positioned paraglossalia and basiurohyale and paired caudo‐lateral elements (horns), each consisting of the ceratobranchiale and epibranchiale. The paraglossalia lie within the tongue parenchyma and consist of paired, flat, caudo‐laterally directed cartilages joined rostrally. The basiurohyale forms a single dorso‐ventrally flattened unit composed of an octagonal‐shaped body from which extend rostral (the rostral process) and caudal (the urohyale) projections. The laryngeal skeleton consists of cricoid, procricoid and paired arytenoid cartilages. The large ring‐shaped cricoid cartilage displays a body and paired wings which articulate with each other and with the procricoid. The blunt, ossified, rostral projection of the cricoid and the scalloped nature of the arytenoid cartilages are unique to the ostrich. The procricoid is a single structure which links the paired arytenoids and wings of the cricoid. The hyobranchial apparatus is firmly attached to the tongue parenchyma and to the larynx and proximal trachea. In contrast to previous reports in this species, the horns of the hyobranchial apparatus are not related to the skull. Ossification of the body of the basihyale, the ceratobranchials and the rostral process and body of the cricoid cartilage of the larynx lends stability to these structures.     

Tongue evolution in the lungless salamanders,family plethodontidae. II. Function and evolutionary diversity

A recently presented model of tongue projection dynamics is used to generate a series of predictions concerning morphologies to be expected under selection for increased distance of projection, increased speed of projection, and increased directional versatility. A general understanding of biomechanical events and the model are used as points of departure for making specific predictions concerning details of structure in skeletal, muscular and connective tissue components of the tongue and associated structures. Comparative methods are used to examine these predictions in the genera of plethodontid salamanders. These salamanders are known to project their tongues to different degrees, and this knowledge is used to test the hypotheses concerning morphological specialization. Three distinct groups of plethodontid salamanders have evolved specializations for long distance projection, and these genera differ from one another in important ways in respect to specific character complexes. For example, the tropical genera and Hydromantes use CBII as the major force transmission element in the skeleton, while Eurycea and its allies use CBI in this role. Hydromantes differs from both in having a uniquely proportioned and structured hyobranchial skeleton and associated musculature. Less extreme specializations for tongue projection are found in different combinations in three other groups. Finally, two distinct groups of generalized species having only limited tongue projection capabilities are recognized, each having a unique complex of inter-related features. Each of these eight groups is recognized and characterized as a functional mode, and hypotheses concerning the biomechanical meaning of the character complexes of each are formulated.     

A complex hyobranchial apparatus in a Cretaceous dinosaur and the antiquity of avian paraglossalia

The highly specialized feeding apparatus of modern birds is characterized in part by paraglossalia, triangular bones or cartilages in the tongue that constitute part of the rarely fossilized hyobranchial apparatus. Here, we report on a new, juvenile specimen of the ankylosaurid dinosaur Pinacosaurus grangeri Gilmore, 1933 that provides the first evidence of paraglossalia outside of crown group Aves. The specimen is remarkable in preserving a well‐ossified hyobranchial apparatus, including paired paraglossalia, first and second ceratobranchials, epibranchials, and evidence of a median cartilaginous basihyal. Reassessment of Edmontonia, another ankylosaur, also reveals evidence of bony paraglossalia. Ankylosaur paraglossalia closely resemble those of birds, but are relatively larger and bear prominent muscle scars, supporting the hypothesis that ankylosaurs had fleshy, muscular tongues. The other hyobranchial elements, surprisingly, resemble those of terrestrially feeding salamanders. Ankylosaurs had reduced, slowly replacing teeth, as evidenced from dental histology, suggesting that they relied greatly on their tongues and hyobranchia for feeding. Some curved, rod‐like elements of other dinosaur hyobranchia are reinterpreted as second ceratobranchials, rather than first ceratobranchials as commonly construed. Ankylosaurs provide rare fossil evidence of deep homology in vertebrate branchial arches and expose severe biases against the preservation and collection of the hyobranchial apparatus. In light of these biases, we hypothesize that paraglossalia were present in the common ancestor of Dinosauria, indicating that some structures of the highly derived avian feeding apparatus were in place by the Triassic Period. © 2015 The Linnean Society of London     

Experimental morphology of the feeding mechanism in salamanders

The subarcualis rectus I muscle (SAR) in the feeding mechanism of four tiger salamanders (Ambystoma tigrinum) was removed early in ontogeny and these individuals were allowed to complete metamorphosis. This procedure resulted in postmetamorphic tiger salamanders which differed from control individuals in the size (and thus force generating capacity) of the SAR muscle. The experimental manipulation of muscle ontogeny allowed a test of previous hypotheses of SAR function in postmetamorphic individuals. Multivariate analysis of variance for kinematic variables measured from high-speed video records of feeding revealed that experimentally modified tiger salamanders did not protract the hyobranchial apparatus or project the tongue from the mouth during feeding. Removal of the SAR muscle resulted in significantly reduced hyobranchial elevation in the buccal cavity and reduced maximum tongue projection distance.     

Metamorphosis of cranial design in tiger salamanders (Ambystoma tigrinum): A morphometric analysis of ontogenetic change

While ontogenetic analyses of skull development have contributed to our understanding of phylogenetic patterns in vertebrates, there are few studies of taxa that undergo a relatively discrete and rapid change in morphology during development (metamorphosis). Morphological changes occurring in the head at metamorphosis in tiger salamanders (Ambystoma tigrinum) were quantified by a morphometric analysis of cranial osteology and myology to document patterns of change during metamorphosis. We employed a cross-sectional analysis using a sample of larvae just prior to metamorphosis and a sample of transformed individuals just after metamorphosis, as well as larvae undergoing metamorphosis. There were no differences in external size of the head among the larval and transformed samples. The hyobranchial apparatus showed many dramatic changes at metamorphosis, including shortening of ceratobranchial 1 and the basibranchial. The subarcualis rectus muscle increased greatly in length at metamorphosis, as did hypobranchial length and internasal distance. A truss analysis of dorsal skull shape showed that at metamorphosis the snout becomes wider, the maxillary and squamosal triangles rotate posteromedially, and the neurocranium shortens (while maintaining its width), resulting in an overall decrease in skull length at metamorphosis. These morphometric differences are interpreted in light of recent data on the functional morphology of feeding in salamanders. Morphological reorganization of the hyobranchial apparatus and shape changes in the skull are related to the acquisition of a novel terrestrial feeding mode (tongue projection) at metamorphosis. Metamorphic changes (both internal and external) that can be used to judge metamorphic condition are discussed.     

Kinetics of tongue projection in Ambystoma tigrinum: Quantitative kinematics,muscle function,and evolutionary hypotheses

The projectile tongue of caudate amphibians has been studied from many perspectives, yet a quantitative kinetic model of tongue function has not yet been presented for generalized (nonplethodontid) terrestrial salamanders. The purposes of this paper are to describe quantitatively the kinnematics of the feeding mechanism and to present a kinetic model for the function of the tongue in the ambystomatid salamander Ambystoma tigrinum. Six kinematic variables were quantified from high-speed films of adult A. tigrinum feeding on land and in the water. Tongue protrusion reaches its maximum during peak gape, while peak tongue height is reached earlier, 15 ms after the mouth starts to open. Tongue kinematics change considerably during feeding in the water, and the tongue is not protruded past the plane of the gape. Electrical stimulation of the major tongue muscles showed that tongue projection in A. tigrinum is the combined result of activity in four muscles: the geniohyoideus, Subarcualis rectus 1, intermandibularis posterior, and interhyoideus. Stimulation of the Subarcualis rectus 1 alone does not cause tongue projection. The kinetic model produced from the kinematic and stimulation data involves both a dorsal vector (the resultant of the Subarcualis rectus 1, intermandibularis posterior, and interhyoideus) and a ventral vector (the geniohyoideus muscle), which sum to produce a resultant anterior vector that directs tongue motion out of the mouth and toward the prey. This model generates numerous testable predictions about tongue function and provides a mechanistic basis for the hypothesis that tongue projection in salamanders evolved from primitive intraoral manipulative action of the hyobranchial apparatus.     

A comparative study of the hyobranchial apparatus in Hynobiidae (Amphibia: Urodela)

The morphology of the adult hyobranchial apparatus has played an important role in understanding the systematics and evolution of urodeles, but the hyobranchial apparatus of hynobiid salamanders has received little attention so far. In this study, the hyobranchial apparatus of eight hynobiid salamanders (Hynobius leechii, Onychodactylus zhangyapingi, Ranodon sibiricus, Batrachuperus pinchonii, Salamandrella keyserlingii, Liua shihi, Pachyhynobius shangchengensis and Pseudohynobius flavomaculatus) is described and compared based on the clearing and double-staining method. The basic elements of the hyobranchial apparatus of the eight species are similar, including one basibranchial, cornua, one pair of radial loops, one pair of ceratohyals, one pair of hypobranchials II, one pair of ceratobranchials II, one urohyal (absent in O. zhangyapingi), one pair of the complex of hypobranchial I and ceratobranchial I (separated in certain species). Although the hyobranchial apparatus is similar among hynobiid salamanders and shows a unique morphological pattern, there are also certain species-specific distinctions that may be used for specific or generic diagnosis. The results of an ancestral state reconstruction of five traits showed that the ossified basibranchial, the presence of a separated hypobranchial I and ceratobranchial I, the absence of a urohyal, the ossified hypobranchial I and the partially ossified ceratohyal are derived traits. The state shown by the traits of each species is consistent with the phylogenetic position of each species. Compared with other Urodela, the hyobranchial apparatus of this group shows certain distinctive features that may represent the diagnostic characters of the family Hynobiidae. The partially ossified ceratohyal is correlated with the habitat and represents an ecological adaptation.     

Jaw and hyolingual movements during prey transport in varanid lizards: effects of prey type

The ability to modulate feeding kinematics in response to prey items with different functional properties is likely a prerequisite for most organisms that feed on a variety of food items. Variation in prey properties is expected to reveal variation in feeding function and the functional role of the different phases in a transport cycle. Here we describe the kinematics of prey transport of two varanid species, Varanus niloticus and Varanus ornatus. These species were selected for analysis because of their highly specialised hyolingual system and food transport mechanism (inertial food transport). In these animals, tongue and hyoid movements are expected to make no, or only a minor, contribution to prey transport. We observed statistically significant prey type effects that could be associated with prey properties such as mass, size and mobility. These data show that both species are capable of modulating the kinematics of food transport in response to different prey types. Moreover, not only the kinematics of the jaws were modulated in response to prey characteristics but also the anterior/posterior movements of the tongue and hyoid. This suggests a more important role of the tongue and hyolingual movements in these animals than previously suspected. In contrast, head movements were rather stereotyped and were not modulated in response to changes in prey type.     

Tongue evolution in the lungless salamanders, family plethodontidae. I. Introduction, theory and a general model of dynamics.

Plethodontid salamanders capture prey by projecting the tongue from the mouth. An analysis of theoretical mechanics of the hyobranchial skeleton is used to formulate a working hypothesis of tongue movements. Predictions that the skeletal elements of the tongue are included in the projectile and that the hyobranchial skeleton is folded during projection are central to the analysis. When decapitated in a particular way, salamanders project the tongue, and it is not retracted. When these heads are fixed and sectioned, examination confirms the predications. In turn, these observations are used to refine the working hypothesis and to generate a general model of tongue dynamics for plethodontids. Muscles performing the major roles of projection (subarcualis rectus I) and retraction (rectus cervicis profundus) are identified. The skeleton is folded passively along a morphological track having the form of a tractrix. Predictions concerning the shape of the track and the exact configuration of the folded skeleton are confirmed by study of sectioned material. The skeleton unfolds along the track during retraction and is spread into the resting state. The model developed herein will be used as a basis for predictions concerning selection patterns in the family and for analytical purposes in comparative and evolutionary studies.     

The larval hyobranchial apparatus of discoglossoid frogs: its structure and bearing on the systematics of the Anura (Amphibia: Anura)

The morphology of the larval hyobranchial apparatus of discoglossoid frog species representing the genera Ascaphus, Alytes, Bombina, and Discoglossus is described and the resulting characters were analysed cladistically. Seven species representing seven major lineages of frogs were included in the cladistic analysis of characters. Several changes in the terminology of the musculature are introduced, and a new interpretation of the subarcualis-muscle system is presented. The phylogenetic analysis suggest that the hyobranchial apparatus was substantially altered in the lineages leading to and within the Pipanura. This notably involved fusion, reduction and loss of skeletal structures and muscles, and splitting of certain muscles into muscle groups. The result confirm previous hypotheses based on the study of adults: discoglossoid species retain the most numlerous plesiomorphic characters among extant ianurans. The larval hyobranchial apparatus is in many features structrually similar to that of urodeles. Many of their character states were most likely present in the most recent common ancestor of all living forgs. The cladistic analysis of 31 characters of ithe larval hyobranchial apparatus supports major clades: Anura, Bombinanura, Pipanura, and Pelobatoidea + Neobatrachia. The cladiostic analysis and interpretation of larval characters is in part compatible with phylogenetic hypotheses based on characters of adults and rRNA sequences, but is in conflict with the Mesobatrachia and Archaeobatrachia concepts of other authors.     

Hyobranchial skeleton and hypobranchial muscles of rhipidistians

The hyobranchial skeleton of the porolepiform rhipidistian Laccognathus panderi Gross is described. The double composition of the ceratohyal in crossopterygians is proposed. The urohyal of porolepiforms, like that of Latimeria, consists of cartilaginous axial and membranous peripheral portions. The differences between porolepiforms and osteolepiforms in the structure of the hyobranchial skeleton, particularly, in the shape of the urohyal are attributable to different arrangements of the hypobranchial muscles. Porolepiforms and coelacanths have retained the coracomandibularis muscle inherited from early gnathostomes, whereas the same muscle of osteolepiforms was transformed into the geniohyoideus muscle. This transformation is accounted for by functional changes in the hyobranchial apparatus.     

Patterns of peripheral innervation of the tongue and hyobranchial apparatus in caecilians (Amphibia: Gymnophiona).

The innervation of the musculature of the tongue and the hyobranchial apparatus of caecilians has long been assumed to be simple and to exhibit little interspecific variation. A study of 14 genera representing all six families of caecilians demonstrates that general patterns of innervation by the trigeminal, facial, glossopharyngeal, and vagus nerves are similar across taxa but that the composition of the "hypoglossal" nerve is highly variable. Probably in all caecilians, spinal nerves 1 and 2 contribute to the hypoglossal. In addition, in certain taxa, an "occipital," the vagus, and/or spinal 3 appear to contribute fibers to the composition of the hypoglossal nerve. These patterns, the lengths of fusion of the contributing elements, and the branching patterns of the hypoglossal are assessed according to the currently accepted hypothesis of phylogenetic relationships of caecilians, and of amphibians. An hypothesis is proposed that limblessness and a simple tongue, with concomitant reduced complexity of innervation of muscles associated with limbs and the tongue, has released a constraint on pattern of innervation. As a consequence, a greater diversity and, in several taxa, greater complexity of neuroanatomical associations of nerve roots to form the hypoglossal are expressed.     

Metamorphosis and evolution of feeding behaviour in salamanders of the family Plethodontidae

Plethodontid salamanders capture prey with enhanced tongue protraction relative to other salamander taxa, yet metamorphosing plethodontids are hypothesized to be constrained relative to direct-developing plethodontids in their degree of tongue evolution (protraction length and velocity) by the presence of a larval stage in development. In this biphasic life history the hyobranchial apparatus serves the conflicting functions of larval suction feeding and adult tongue protraction. The deletion of the larval stage removes one of the conflicting functions and has thus permitted direct-developing plethodontids to circumvent this constraint and evolve extremely long tongues, which in some species can be projected to 80% of body length. To evaluate this constraint hypothesis and explore taxonomic diversity of feeding behaviours, we studied feeding in larvae, adults and metamorphosing individuals of seven species of metamorphosing plethodontids from the basal taxa Desmognathinae and Hemidactyliini using direct observations, high-speed videography and kinematic analysis. We found that larval plethodontids suction feed, but feeding is suspended entirely during metamorphosis, and aquatic adults do not suction feed. Adults have exapted the terrestrial modes of tongue and jaw prehension for aquatic prey capture. These findings substantiate the premise that suction feeding and tongue protraction are conflicting functions, and thus our results support the constraint hypothesis. Plethodontid adults have evolved their extreme tongue protraction ability at the expense of adult suction feeding. The rapid metamorphosis that characterizes plethodontids may be an adaptation that minimizes the non-feeding period imposed by the evolution of derived tongue protraction in adults. © 2002 The Linnean Society of London, Zoological Journal of the Linnean Society , 2002, 134 , 375–400.     

挂榜山小鲵成体和亚成体舌器的形态特征

以透明骨骼双色法对挂榜山小鲵(Hynobius guabangshanensis)成体和亚成体舌器的形态特征进行观察和详细描述。结果表明,在成体中,下舌软骨中部交叉;角舌软骨末端被第一下鳃骨和第一角鳃骨的愈合体遮盖;具有基鳃软骨角状突;第二角鳃骨骨化;尾舌骨骨化,呈"一"字形。在亚成体中,下舌软骨中部未交叉;第一下鳃骨和第一角鳃骨单独存在;无基鳃软骨角状突;第二角鳃骨未骨化;具有第三、第四对角鳃骨,且均为软骨;尾舌骨未骨化,成"1"字形。这些形态特征的改变可能由舌器在成体和亚成体阶段的功能所引起。     

The mechanism of frill erection in the bearded dragon Amphibolurus barbatus with comments on the jacky lizard A. muricatus (Agamidae)

Amphibolurus barbatus has a threat display which includes the erection of the gular regions as a frill and may also include wide opening of the mouth to display a yellow mouth lining. Frill erection involves protraction, depression, and lateral expansion of the hyoid apparatus. Electrical stimulation of the hyoid muscles and dissection of the hyoid apparatus were used to examine specializations for producing frill erection. Specializations of the hyoid skeleton include the absence of a ceratobranchial II, presence of a synovial joint between the ceratohyal and body of the hyoid, and combined shortening of the entoglossal process and lengthening of the posterior arches. The only apparent specialization of the hyoid musculature is the anterior displacement of the origin of m. hyomandibularis. All of the hyoid muscles are involved in some way in frill erection and the actions of each muscle is described. The characteristic frill erection in the threat display of Amphibolurus barbatus is possible because of the 1:2 ratio of the anterior and posterior parts of the apparatus and the absence of the ceratobrnchial II.     

Gross anatomical features of the tongue, lingual skeleton and laryngeal mound of Rhea americana (Palaeognathae, Aves): morpho-functional considerations

The tongue body of Rhea americana is triangular and partially pigmented with each caudo-lateral margin displaying a round, sub-divided lingual papilla. The tongue root is a smooth, non-pigmented tract of mucosa. The tongue body is supported by the paraglossum and distal half of the rostral projection of the basihyal (RPB), and the tongue root by the proximal half of the RPB, body of the basihyal and proximal ceratobranchials. An urohyal is absent; however, peculiar to R. americana, the caudal margin of the cricoid body displays a median projection, which may represent the remnant of the urohyal incorporated into the cricoid. The laryngeal mound is less elevated, the arytenoid cartilages are smaller than in other ratites, and the caudal margin displays pharyngeal papillae that vary in shape and number. The unique morphology of the lingual skeleton and its positioning within the tongue of R. americana, the rostral insertion of the M. ceratoglossus, the absence of the urohyal (enhanced ventroflexion) and the caudal positioning and mobile attachment of the ensheathed basihyal to the paraglossum would appear to allow independent movement of the tongue body relative to the hyobranchial apparatus. Additionally, the deeply indented base and rostral oval opening in the paraglossum limits the length of cartilage present in the midline of the tongue body. This may allow the tongue the necessary flexibility for the lingual papillae to clean the choana. The cleaning action of the tongue would occur simultaneously with the previously described role of this organ and associated structures during feeding. Thus, the so-called reduced, ancestral tongue of R. americana may be structurally and functionally more complex than previously believed.     

Neuromuscular control of prey capture in frogs.

While retaining a feeding apparatus that is surprisingly conservative morphologically, frogs as a group exhibit great variability in the biomechanics of tongue protraction during prey capture, which in turn is related to differences in neuromuscular control. In this paper, I address the following three questions. (1) How do frog tongues differ biomechanically? (2) What anatomical and physiological differences are responsible? (3) How is biomechanics related to mechanisms of neuromuscular control? Frog species use three non-exclusive mechanisms to protract their tongues during feeding: (i) mechanical pulling, in which the tongue shortens as its muscles contract during protraction; (ii) inertial elongation, in which the tongue lengthens under inertial and muscular loading; and (iii) hydrostatic elongation, in which the tongue lengthens under constraints imposed by the constant volume of a muscular hydrostat. Major differences among these functional types include (i) the amount and orientation of collagen fibres associated with the tongue muscles and the mechanical properties that this connective tissue confers to the tongue as a whole; and (ii) the transfer of intertia from the opening jaws to the tongue, which probably involves a catch mechanism that increases the acceleration achieved during mouth opening. The mechanisms of tongue protraction differ in the types of neural mechanisms that are used to control tongue movements, particularly in the relative importance of feed-forward versus feedback control, in requirements for precise interjoint coordination, in the size and number of motor units, and in the afferent pathways that are involved in coordinating tongue and jaw movements. Evolution of biomechanics and neuromuscular control of frog tongues provides an example in which neuromuscular control is finely tuned to the biomechanical constraints and opportunities provided by differences in morphological design among species.     

Neurobehavioral specializations for respiratory movements and rapid escape from predators in posterior segments of the tubificid Branchiura sowerbyi

The posterior end of the aquatic oligochaete, Branchiura sowerbyi (Tubificidae) protrudes above the sediments and is specialized to carry out several rhythmic respiratory movements. These include 1) waves of flexion by paired gill filaments on each posterior segment, 2) body undulations, and 3) rectal water pumping. Since execution of these behaviors renders the worm's posterior end vulnerable to predation, appropriate neurobehavioral mechanisms have evolved that permit extremely rapid escape of tail segments into the sediments. Some of these mechanisms include 1) highly sensitive sensory apparatus for detecting substrate vibrations, water displacements, or touch, 2) large diameter and rapidly conducting lateral giant nerve fibers, and 3) adequacy of a single lateral giant fiber impulse for evoking an all-or-none longitudinal muscle contraction. The significance of these posterior respiratory and escape reflex specializations are discussed in relation to possible predator foraging strategies.