Jaw movement kinematics and jaw muscle (EMG) activity during drinking in the pigeon (Columba livia)

Summary Movements of the maxilla and mandible were recorded during drinking in the head-fixed pigeon and correlated with electromyographic activity in representative jaw muscle groups. During drinking, each jaw exhibits opening and closing movements along both the dorso-ventral and rostro-caudal axes which may be linked with or independent of each other. All subjects showed small but systematic increases in cycle duration over the course of individual drinking bouts. Cyclic jaw movements during drinking were correlated with nearly synchronous activity in the protractor (levator) of the upper jaw and in several jaw closer muscles, as well as with alternating activity in tongue protractor and retractor muscles. No EMG activity was ever recorded in the lower jaw opener muscle, suggesting that lower jaw opening in this preparation is produced, indirectly, by the contraction of other muscles. The results clarify the contribution of the individual jaws to the generation of gape variations during drinking in this species.Abbreviations AMEM adductor mandibulae externus muscle - DM depressor mandibulae muscle - EMG electromyographic - GENIO geniohyoideus muscle - LB lower beak - LED light-emitting diode - PQP protractor quadrati et pterygoidei muscle - PVL pterygoideus ventralis muscle, pars lateralis - SeH/StH serpihyoideus or stylohyoideus muscle - UB upper beak     

Morphology of the cranial skeleton and musculature in the obligate carnivorous tadpole of Lepidobatrachus laevis (Anura: Ceratophryidae)

Ziermann, J.M., Infante, C., Hanken, J. and Olsson, L. 2011. Morphology of the cranial skeleton and musculature in the obligate carnivorous tadpole of Lepidobatrachus laevis (Anura: Ceratophryidae). —Acta Zoologica (Stockholm) 00 :1–12. Lepidobatrachus laevis (Ceratophryidae: Ceratophryinae) is a bizarre frog endemic to the Chacoan desert of central South America. Its tadpole is an obligate carnivore that can catch and consume live prey nearly its own size. Morphological adaptations associated with this unique feeding mode, including the larval skull anatomy and associated cranial musculature, have only been partly described. We studied the head of Stages 26–27 larvae using gross dissection, immunohistochemistry, and standard histology. Derived features of this tadpole compared to the microphagous, herbivorous larvae of most other anurans include simplified chondrocranial cartilages and very robust jaw muscles. The mm. suspensorio‐ et quadratoangularis do not take their origin from the processus muscularis of the palatoquadrate, as in most other tadpoles, but instead originate from the corpus of the palatoquadrate caudal to this process. The jaw levators are unusually large. The tadpole of Ceratophrys, another member of the ceratophryine clade, also consumes large animal prey, but its morphology is very different. It probably has evolved independently from a generalized, mainly herbivorous tadpole similar to the larva of Chacophrys, the third ceratophryine genus. Most specialized features of the larval head of Lepidobatrachus laevis are adaptations for ‘megalophagy’—ingestion of whole, very large animal prey.     

Anatomy of the feeding apparatus of the nurse shark,Ginglymostoma cirratum

The anatomy of the feeding apparatus of the nurse shark, Ginglymostoma cirratum, was investigated by gross dissection and computer axial tomography. The labial cartilages, jaws, jaw suspension, muscles, and ligaments of the head are described. Palatoquadrate cartilages articulate with the chondrocranium caudally by short, laterally projecting hyomandibulae and rostrally by ethmoorbital articulations. Short orbital processes of the palatoquadrates are joined to the ethmoid region of the chondrocranium by short, thin ethmopalatine ligaments. In addition, various ligaments, muscles, and the integument contribute to the suspension of the jaws. When the mouth is closed and the palatoquadrate retracted, the palatine process of the palatoquadrate is braced against the ventral surface of the nasal capsule and the ascending process of the palatoquadrate is in contact with the rostrodorsal end of the suborbital shelf. When the mandible is depressed and the palatoquadrate protrudes slightly rostroventrally, the palatoquadrate moves away from the chondrocranium. A dual articulation of the quadratomandibular joint restricts lateral movement between the mandible and the palatoquadrate. The vertically oriented preorbitalis muscle spans the gape and is hypothesized to contribute to the generation of powerful crushing forces for its hard prey. The attachment of the preorbitalis to the prominent labial cartilages is also hypothesized to assist in the retraction of the labial cartilages during jaw closure. Separate levator palatoquadrati and spiracularis muscles, which are longitudinally oriented and attach the chondrocranium to the palatoquadrate, are hypothesized to assist in the retraction of the palatoquadrate during the recovery phase of feeding kinematics. Morphological specializations for suction feeding that contribute to large subambient suction pressures include hypertrophied coracohyoideus and coracobranchiales muscles to depress the hyoid and branchial arches, a small oral aperture with well‐developed labial cartilages that occlude the gape laterally, and small teeth. J. Morphol. 241:33–60, 1999. © 1999 Wiley‐Liss, Inc.     

Suboccipital muscle of sharpnose sevengill shark Heptranchias perlo and its possible role in prey dissection

Skull and head muscles of Heptranchias perlo were studied. Its distinctive features include the suboccipital muscles, described for the first time, the absence of the palatoquadrate symphysis, a longitudinally extended mouth, and teeth unsuited for dissecting prey in typical method of modern sharks, which is cutting motions powered by head shaking from side to side. The palatoquadrate cartilages of H. perlo and closely related Hexanchidae articulate with the neurocranium via orbital and postorbital articulations, which together allow for lateral expansion of the jaws, but restrict retraction and protraction. We interpret these features as an adaptation to a different method of prey dissection, that is, ripping in a backward pull. It employs the specific postorbital articulation together with the suboccipital muscles as force-transmitting devices, and is powered by swimming muscles which produce a rearward thrust of the tail. During this type of dissection, the anterior part of the vertebral column should experience a tensile stress which explains the replacement of rigid vertebral bodies by a collagenous sheath around the notochord in H. perlo. The backward-ripping dissection could have been common among ancient Elasmobranchii based on the similarly developed postorbital articulation, a longitudinally extended mouth, and the absence of the palatoquadrate symphysis. A biomechanical comparison with the extinct Pucapampella indicates that ancient elasmobranchs could be also specialized in the backward-ripping prey dissection, but their mechanism was different from that inferred for H. perlo. We suggest that in the early evolution of sharks this mechanism was replaced by head-shaking dissection and then later was restored in H. perlo on a new morphological basis. A new position of the postorbital articulation below the vertebral axis is fraught with the braincase elevation when backward ripping the prey, and as a counter-mean, requires formation of suboccipital portions of the axial musculature unknown in other sharks. Homology and origin of these portions is considered.     

Comment on ‘Stable isotopes challenge the perception of ocean sunfish Mola mola as obligate jellyfish predators'

Muscle development in the bamboo sole Heteromycteris japonicus was investigated, focusing primarily on the cranial muscles, using an improved whole mount immunohistochemical staining method with potassium hydroxide, hydrogen peroxide and trypsin. Larvae of H. japonicus had branchial levators, but not all of them were retained in adults, a condition also seen in the Japanese flounder Paralichthys olivaceus. In particular, larval branchial levators II and III disappeared during development, while I and IV remained to become the levator internus I and levator posterior, which were well‐defined muscles in adults. In place of the atrophied muscles, levatores externi and levator internus II developed and regulated the branchial arches. The results showed that the muscle composition in the dorsal branchial arches changed to the adult form before metamorphosis in H. japonicus, as seen in P. olivaceus, and this transformation may be common to all members of that group.     

Tooth and cranial disparity in the fossil relatives of Sphenodon (Rhynchocephalia) dispute the persistent ‘living fossil’ label

The tuatara (Sphenodon punctatus) is the only living representative of Rhynchocephalia, a group of small vertebrates that originated about 250 million years ago. The tuatara has been referred to as a living fossil; however, the group to which it belongs included a much greater diversity of forms in the Mesozoic. We explore the morphological diversity of Rhynchocephalia and stem lepidosaur relatives (Sphenodon plus 13 fossil relatives) by employing a combination of geometric morphometrics and comparative methods. Geometric morphometrics is used to explore cranium size and shape at interspecific scale, while comparative methods are employed to test association between skull shape and size and tooth number after taking phylogeny into account. Two phylogenetic topologies have been considered to generate a phylomorphospace and quantify the phylogenetic signal in skull shape data, the ancestral state reconstruction as well as morphological disparity using disparity through time plots (DTT). Rhynchocephalia exhibit a significant phylogenetic signal in skull shape that compares well with that computed for other extinct vertebrate groups. A consistent form of allometry has little impact on skull shape evolution while the number of teeth significantly correlates with skull shape also after taking phylogeny into account. The ancestral state reconstruction demonstrates a dramatic shape difference between the skull of Sphenodon and its much larger Cretaceous relative Priosphenodon. Additionally, DTT demonstrates that skull shape disparity is higher between rather than within clades while the opposite applies to skull size and number of teeth. These results were not altered by the use of competing phylogenic hypotheses. Rhynchocephalia evolved as a morphologically diverse group with a dramatic radiation in the Late Triassic and Early Jurassic about 200 million years ago. Differences in size are not marked between species whereas changes in number of teeth are associated with co‐ordinated shape changes in the skull to accommodate larger masticatory muscles. These results show that the tuatara is not the product of evolutionary stasis but that it represents the only survivor of a diverse Mesozoic radiation whose subsequent decline remains to be explained.     

Cranial muscles of the anurans leiopelma hochstetteri and ascaphus truei and the homologies of the mandibular adductors in lissamphibia and other gnathostomes

The frogs Ascaphus truei and Leiopelma hochstetteri are members of the most basal lineages of extant anurans. Their cranial muscles have not been previously described in full and are investigated here by dissection. Comparison of these taxa is used to review a controversy regarding the homologies of the jaw adductor muscles in Lissamphibia, to place these homologies in a wider gnathostome context, and to define features that may be useful for cladistic analysis of Anura. A new muscle is defined in Ascaphus and is designated m. levator anguli oris. The differences noted between Ascaphus and Leiopelma are in the penetration of the jaw adductor muscles by the mandibular nerve (V³). In the traditional view of this anatomy, the paths of the trigeminal nerve branches define homologous muscles. This scheme results in major differences among frogs, salamanders, and caecilians. The alternative view is that the topology of origins, insertions, and fiber directions are defining features, and the nerves penetrate the muscle mass in a variable way. The results given here support the latter view. A new model is proposed for Lissamphibia, whereby the adductor posterior (levator articularis) is a separate entity, and the rest of the adductor mass is configured around it as a folded sheet. This hypothesis is examined in other gnathostomes, including coelacanth and lungfish, and a possible sequence for the evolution of the jaw muscles is demonstrated. In this system, the main jaw adductor in teleost fish is not considered homologous with that of tetrapods. This hypothesis is consistent with available data on the domain of expression of the homeobox gene engrailed 2, which has previously not been considered indicative of homology. Terminology is discussed, and “adductor mandibulae” is preferred to “levator mandibulae” to align with usage in other gnathostomes. J. Morphol., 2011. © 2011 Wiley‐Liss, Inc.     

Cephalic muscle development in the Australian lungfish,Neoceratodus forsteri

Lungfishes are the extant sister group of tetrapods. As such, they are important for the study of evolutionary processes involved in the water to land transition of vertebrates. The evolution of a true neck, that is, the complete separation of the pectoral girdle from the cranium, is one of the most intriguing morphological transitions known among vertebrates. Other salient changes involve new adaptations for terrestrial feeding, which involves both the cranium and its associated musculature. Historically, the cranium has been extensively investigated, but the development of the cranial muscles much less so. Here, we present a detailed study of cephalic muscle development in the Australian lungfish, Neoceratodus forsteri, which is considered to be the sister taxon to all other extant lungfishes. Neoceratodus shows several developmental patterns previously described in other taxa; the tendency of muscles to develop from anterior to posterior, from their region of origin toward insertion, and from lateral to ventral/medial (outside‐in), at least in the branchial arches. The m.protractor pectoralis appears to develop as an extension of the most posterior m.levatores arcuum branchialium, supporting the hypothesis that the m.cucullaris and its derivatives (protractor pectoralis, levatores arcuum branchialium) are branchial muscles. We present a new hypothesis regarding the homology of the ventral branchial arch muscles (subarcualis recti and obliqui, transversi ventrales) in lungfishes and amphibians. Moreover, the morphology and development of the cephalic muscles confirms that extant lungfishes are neotenic and have been strongly influenced via paedomorphosis during their evolutionary history.     

Ontogeny of the cranial musculature in Corydoras aeneus Callichthyidae,Siluriformes

A complete study of the early ontogeny of the cranial muscles of Corydoras aeneus (Callichthyidae) was undertaken and results were compared with those for the loricariid Ancistrus cf. triradiatus. This comparison reveals a high degree of similarity in the ontogeny of both species' cranial muscles. Both species lack a musculus protractor hyoidei, and the musculus intermandibularis posterior is divided into two different parts that have partly obtained a novel function (serving the lower lip) in A. cf. triradiatus. A similar increase in muscular complexity in this species is found in the dorsal constrictor of the hyoid muscle plate. This constrictor gives rise to the same muscles in both C. aeneus and A. cf. triradiatus, but in A. cf. triradiatus the musculus levator operculi later hypertrophies. In C. aeneus the musculus extensor tentaculi forms a single muscle diverging posteriorly, whereas in A. cf. triradiatus the musculus extensor tentaculi differentiates into two separate bundles. Also, a loricariid neoformation is present called the musculus levator tentaculi.     

Development of the muscles associated with the mandibular and hyoid arches in the Siberian sturgeon,Acipenser baerii (Acipenseriformes: Acipenseridae)

The skeleton of the jaws and neurocranium of sturgeons (Acipenseridae) are connected only through the hyoid arch. This arrangement allows considerable protrusion and retraction of the jaws and is highly specialized among ray‐finned fishes (Actinopterygii). To better understand the unique morphology and the evolution of the jaw apparatus in Acipenseridae, we investigated the development of the muscles of the mandibular and hyoid arches of the Siberian sturgeon, Acipenser baerii. We used a combination of antibody staining and formalin‐induced fluorescence of tissues imaged with confocal microscopy and subsequent three‐dimensional reconstruction. These data were analyzed to address the identity of previously controversial and newly discovered muscle portions. Our results indicate that the anlagen of the muscles in A. baerii develop similarly to those of other actinopterygians, although they differ by not differentiating into distinct muscles. This is exemplified by the subpartitioning of the m. adductor mandibulae as well as the massive m. protractor hyomandibulae, for which we found a previously undescribed portion in each. The importance of paedomorphosis for the evolution of Acipenseriformes has been discussed before and our results indicate that the muscles of the mandibular and the hyoid may be another example for heterochronic evolution.     

Comparative study on the cranial morphology of Gymnallabes typus (Siluriformes: Clariidae) and their less anguilliform relatives,Clariallabes melas and Clarias gariepinus

We compare the cranial morphology of four fish species with an increasing anguilliformism in the following order: Clarias gariepinus, Clariallabes melas, Gymnallabes typus, and Channallabes apus. The main anatomical‐morphological disparities are the stepwise reduction of the skull roof along with the relative enlargement of the external jaw muscles, which occurred in each of them. Gymnallabes typus and C. apus lack a bony protection to cover the jaw muscles. The neurocranial bones of C. gariepinus, however, form a closed, broad roof, whereas the width of the neurocranium in C. melas is intermediate. Several features of the clariid heads, such as the size of the mouth and the bands of small teeth, may be regarded as adaptations for manipulating large food particles, which are even more pronounced in anguilliform clariids. The jaw musculature of G. typus is hypertrophied and attached on a higher coronoid process of the lower jaw, causing a larger adductive force. The hyomandibula interdigitates more strongly with the neurocranium and its dentition with longer teeth is posteriorly extended, closer to the lower jaw articulation. The anguilliform clariids also have their cranial muscles modified to enable a wider gape. The adductor mandibulae and the levator operculi extend more posteriorly, and the anterior attachment site of the protractor hyoidei dorsalis shifts toward the sagittal plane of the head. A phylogenetic analysis of the Clariidae, which is in progress, could check the validity of Boulenger's hypothesis that predecessors of the primitive fishes, such as Heterobranchus and most Clarias, would have evolved into progressively anguilliform clariids. J. Morphol. 240:169–194, 1999. © 1999 Wiley‐Liss, Inc.     

Muscle development in the Japanese flounder,Paralichthys olivaceus,with special reference to some of the larval‐specific muscles

We investigated muscle development in the Japanese flounder Paralichthys olivaceus, focusing primarily on the cranial muscles, using a whole mount immunohistochemical staining method. It is well established that during the very early stages of morphogenesis, until 4 days post hatching (dph), muscles required for feeding develop. Later, between 8 and 16 dph, the muscle composition in the dorsal branchial arches changes to the adult form. We discovered the presence of larval‐specific muscles in this ontogenetic period, termed the larval branchial levators 2 and 3, located in the dorsal branchial arches. The larval branchial levators 2 and 3 disappear during the course of development, whereas the others remain as levator internus 1 and levator posterior, which have also been described in adult fish. In place of these regressed muscles, the levatores externi and levator internus 2 develop and regulate the branchial arches. In addition, we found that the levator posterior, which is thought to represent the fifth levator externus, and the levatores externi exhibit different origins. We also found that at least a part of the caudal fin musculature develops from the trunk myotome. J. Morphol. 2010. © 2010 Wiley‐Liss, Inc.