A three‐dimensional placoderm (stem‐group gnathostome) pharyngeal skeleton and its implications for primitive gnathostome pharyngeal architecture

The pharyngeal skeleton is a key vertebrate anatomical system in debates on the origin of jaws and gnathostome (jawed vertebrate) feeding. Furthermore, it offers considerable potential as a source of phylogenetic data. Well‐preserved examples of pharyngeal skeletons from stem‐group gnathostomes remain poorly known. Here, we describe an articulated, nearly complete pharyngeal skeleton in an Early Devonian placoderm fish, Paraplesiobatis heinrichsi Broili, from Hunsrück Slate of Germany. Using synchrotron light tomography, we resolve and reconstruct the three‐dimensional gill arch architecture of Paraplesiobatis and compare it with other gnathostomes. The preserved pharyngeal skeleton comprises elements of the hyoid arch (probable ceratohyal) and a series of branchial arches. Limited resolution in the tomography scan causes some uncertainty in interpreting the exact number of arches preserved. However, at least four branchial arches are present. The final and penultimate arches are connected as in osteichthyans. A single median basihyal is present as in chondrichthyans. No dorsal (epibranchial or pharyngobranchial) elements are observed. The structure of the pharyngeal skeleton of Paraplesiobatis agrees well with Pseudopetalichthys from the same deposit, allowing an alternative interpretation of the latter taxon. The phylogenetic significance of Paraplesiobatis is considered. A median basihyal is likely an ancestral gnathostome character, probably with some connection to both the hyoid and the first branchial arch pair. Unpaired basibranchial bones may be independently derived in chondrichthyans and osteichthyans.     

A novel pharyngeal expansion mechanism in the yellow-spotted fanray, Platyrhina tangi (Elasmobranchii: Batoidea), with special reference to the function of the fifth ceratobranchial cartilage in batoids

Expansion of the ‘pharynx’ during breathing or capturing prey in fishes generally involves posteroventral retraction of the hyoid arch. However, the hyoid arch structure of batoid fishes (skates, rays, guitarfishes, and sawfishes) is unique, and how they expand the pharyngeal cavity is poorly understood. To investigate the mechanism of pharyngeal expansion during breathing in the yellow-spotted fanray, Platyrhina tangi, we conducted anatomical and kinematic investigations of the pharyngeal region. Our study revealed that the yellow-spotted fanray and sharks have different skeletal linkage systems for pharyngeal expansion. During pharyngeal expansion in the yellow-spotted fanray, the hyoid bar and branchial apparatus rotate ventrally around the hinge joint between the fifth ceratobranchial cartilage and the pectoral girdle. This pharyngeal expansion mechanism appears to be widespread among batoid fishes and is unique among cartilaginous fishes (sharks, batoids, and holocephalans). Batoid fishes possibly developed this pharyngeal expansion mechanism during early batoid evolution.     

Hyoid and pharyngeal arch function during ventilation and feeding in elasmobranchs: Conservation and modification in function

The hypothesis that the mandibular and hyoid arches evolved from anterior pharyngeal arches to increase ventilation performance and subsequently became adapted for feeding is widely accepted. As jaws evolved, the morphology of the hyoid arch changed notably from that of a pharyngeal arch. Furthermore, hyoid arch morphology varies considerably among elasmobranch taxa and has been shown to be related to feeding style. The goal of this study is to determine whether the function (direction of movement or change in cavity cross‐section) of the hyoid arch is altered from that of the pharyngeal arch, and whether function is altered between ventilation, the basal behavior, and feeding, the derived behavior. Similar effects and associations of the pharyngeal arches by orientation to feeding or ventilation are also investigated. The kinematics of the hyoid and second pharyngeal arch during ventilation and feeding are quantified using sonomicrometry and hyomandibular angle measured in five shark and one skate species representing widely divergent hyomandibular morphologies. Hyoid and pharyngeal cavity width follows the same pattern of movement during ventilation; therefore the hyoid arch retains the ancestral function of the pharyngeal arches. The orientation of the hyomandibular cartilage appears to influence the pattern of arch movement during ventilation: anterior directed elements decrease in cavity width; laterally directed elements increase in cavity width; while posterior directed elements increase in cavity width or do not change; while cavity depth increases in all species. Hyoid and pharyngeal cavity width movement differs among the species during feeding and also appears to be related to hyoid arch orientation as well as feeding style. There appears to be a division between those species with hyomandibular angles less than 110° from those that are greater between feeding mode and hyoid cavity width movement. Primarily suction feeding species decrease hyoid cavity width whereas primarily bite feeding species increase hyoid cavity width during feeding while all species increase hyoid cavity depth.     

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.     

Vascularization of the osteostracan and antiarch (Placodermi) pectoral fin: similarities, and implications for placoderm relationships

Phylogenetic analyses frequently resolve the extinct group Placodermi at the base of the clade of jawed fishes (traditionally known as the Gnathostomata), with the jawless fish group Osteostraci as sister taxon to this clade. Both gnathostomes and osteostracans possess pectoral fins supported by a radial(s) articulating on a cartilaginous scapulocoracoid. Blood vessels and nerves pass by or through the scapulocoracoid to supply the musculature of the pectoral fin, and in the Osteostraci also pass through the postbranchial lamina backing the gill chamber before reaching the scapulocoracoid. This course also characterizes the placoderm group Antiarchi. Other placoderms retain the condition typical of other jawed fishes in which the scapulocoracoid, as well as the subclavian veins and arteries, are entirely posterior to the back wall of the gill chamber, lying within the internal region of the trunkshield. These observations suggest that these placoderm groups are more closely related to other jawed fishes than are the Antiarchi, challenging the monophyly of the Placodermi.     

Evolution of muscle activity patterns driving motions of the jaw and hyoid during chewing in Gnathostomes

Although chewing has been suggested to be a basal gnathostome trait retained in most major vertebrate lineages, it has not been studied broadly and comparatively across vertebrates. To redress this imbalance, we recorded EMG from muscles powering anteroposterior movement of the hyoid, and dorsoventral movement of the mandibular jaw during chewing. We compared muscle activity patterns (MAP) during chewing in jawed vertebrate taxa belonging to unrelated groups of basal bony fishes and artiodactyl mammals. Our aim was to outline the evolution of coordination in MAP. Comparisons of activity in muscles of the jaw and hyoid that power chewing in closely related artiodactyls using cross-correlation analyses identified reorganizations of jaw and hyoid MAP between herbivores and omnivores. EMG data from basal bony fishes revealed a tighter coordination of jaw and hyoid MAP during chewing than seen in artiodactyls. Across this broad phylogenetic range, there have been major structural reorganizations, including a reduction of the bony hyoid suspension, which is robust in fishes, to the acquisition in a mammalian ancestor of a muscle sling suspending the hyoid. These changes appear to be reflected in a shift in chewing MAP that occurred in an unidentified anamniote stem-lineage. This shift matches observations that, when compared with fishes, the pattern of hyoid motion in tetrapods is reversed and also time-shifted relative to the pattern of jaw movement.     

Histological structure of the cancellous bone layer in Bothriolepis canadensis (Antiarchi, Placodermi)

The Placodermi are extinct basal gnathostomes which had extensive dermal and perichondral bone, but which lacked the endochondral bone which characterizes the more derived bony fishes. Thin sections of bone from a specimen of the antiarch placoderm Bothriolepis canadensis, from the Escuminac Formation (Frasnian, Upper Devonian), Québec, Canada, reveal that part of the cancellous layer in its dermal and endoskeletal bone formed from perichondral bone trabeculae growing around cartilage spheres. The resultant structure mimics that of osteichthyan endochondral bone. The layout and dimensions of this polygonal mosaic patterning of the bone trabeculae and flattened cartilage spheres resemble those of the prismatic layers of calcified cartilage in chondrichthyans. If the lack of endoskeletal bone in chondrichthyans is a derived character, then the structure identified in B. canadensis could represent a 'template' for the formation of prismatic calcified cartilage in the absence of bone.     

A fish that uses its hydrodynamic tongue to feed on land

To capture and swallow food on land, a sticky tongue supported by the hyoid and gill arch skeleton has evolved in land vertebrates from aquatic ancestors that used mouth-cavity-expanding actions of the hyoid to suck food into the mouth. However, the evolutionary pathway bridging this drastic shift in feeding mechanism and associated hyoid motions remains unknown. Modern fish that feed on land may help to unravel the physical constraints and biomechanical solutions that led to terrestrialization of fish-feeding systems. Here, we show that the mudskipper emerges onto land with its mouth cavity filled with water, which it uses as a protruding and retracting ‘hydrodynamic tongue’ during the initial capture and subsequent intra-oral transport of food. Our analyses link this hydrodynamic action of the intra-oral water to a sequence of compressive and expansive cranial motions that diverge from the general pattern known for suction feeding in fishes. However, the hyoid motion pattern showed a remarkable resemblance to newts during tongue prehension. Consequently, although alternative scenarios cannot be excluded, hydrodynamic tongue usage may be a transitional step onto which the evolution of adhesive mucosa and intrinsic lingual muscles can be added to gain further independence from water for terrestrial foraging.     

Respiratory function of hyoid muscles and hyoid arch

The position of the hyoid arch suggests that it supports soft tissue surrounding the upper airway (UA) and can act to maintain UA patency. We also suspected that muscles inserting on the hyoid arch might show respiratory patterns of activity that could be affected by respiratory stimuli. To test these possibilities, we moved the hyoid arch ventrally in six anesthetized dogs either by traction on it or by stimulation of hyoid muscles. UA resistance was decreased 73 +/- (SE) 6% and 72 +/- 6% by traction and stimulation during expiration and 57 +/- 15% and 52 +/- 8% during inspiration. Moving averages of the geniohyoid (GH) and thyrohyoid (TH) obtained in six other dogs breathing 100% O2 showed phasic respiratory activity while the sternohyoid (SH) showed phasic respiratory activity in only two of these animals and no activity in four. With progressive hypercapnia, GH and TH increased as did SH when activity was already present. Airway occlusion at end expiration augmented and prolonged inspiratory activity in the hyoid muscles but did not elicit SH activity if not already present. Occlusion at end inspiration suppressed phasic activity in hyoid muscles for as long as in the diaphragm. After vagotomy activity increased and became almost exclusively inspiratory. Activity appeared in SH when not previously present. Duration and amplitude of hyoid muscle activity were increased with negative UA pressure and augmented breaths. We conclude that the hyoid arch and muscles can strongly affect UA flow resistance. Hyoid muscles show responses to chemical, vagal, and negative pressure stimuli similar to other UA muscles.     

Development of the mandibular, hyoid arch and gill arch skeleton in the Chinese barb Puntius semifasciolatus: comparisons of ossification sequences among Cypriniformes

The morphogenesis and sequence of ossification and chondrification of skeletal elements of the jaws, and hyoid arch and gill arches of Puntius semifasciolatus are described. These data provide a baseline for further studies and enable comparisons with other described cypriniforms. Some general patterns of ossification in the hyoid arch and branchial arches in cypriniforms were notable. First, the overall development is from anterior to posterior, with the exception of the fifth ceratobranchial bone, which ossifies first. Second, where ossification of iterated elements is sequential, it tends to proceed from posterior to anterior, even when more posterior chondrifications are the smallest in the series. Ossification of the ceratobranchial, epibranchial and pharyngobranchial bones tends to proceed from ventral to dorsal. The comparisons revealed small sets of skeletal elements whose ossification sequence appears to be relatively conserved across cyprinid cypriniforms. Several potentially key timing changes in the ossification sequence of the jaws, hyoid arch and gill arches were identified, such as the accelerated timing of ossification of the fifth ceratobranchial bone, which may be unique to cypriniforms.     

Evolution and development of the synarcual in early vertebrates

The synarcual is a structure incorporating the anterior vertebrae of the axial skeleton and occurs in vertebrate taxa such as the fossil group Placodermi and the Chondrichthyes (Holocephali, Batoidea). Although the synarcual varies morphologically in these groups, it represents the first indication, phylogenetically, of a differentiation of the vertebral column into separate regions. Among the placoderms, the synarcual of Cowralepis mclachlani Ritchie, 2005 (Arthrodira) shows substantial changes during ontogeny to produce an elongate, spool-shaped structure with a well-developed dorsal keel. Because the placoderm synarcual is covered in perichondral bone, the ontogenetic history of this Cowralepis specimen is preserved as it developed anteroposteriorly, dorsally and ventrally. As well, in the placoderm Materpiscis attenboroughi Long et al., 2008 (Ptyctodontida), incomplete fusion at the posterior synarcual margin indicates that both neural and haemal arch vertebral elements are added to the synarcual. A survey of placoderm synarcuals shows that taxa such as Materpiscis and Cowralepis are particularly informative because perichondral ossification occurs prior to synarcual fusion such that individual vertebral elements can be identified. In other placoderm synarcuals (e.g. Nefudina qalibahensis Lelièvre et al., 1995; Rhenanida), cartilaginous vertebral elements fuse prior to perichondral ossification so that individual elements are more difficult to recognize. This ontogenetic development in placoderms can be compared to synarcual development in Recent chondrichthyans; the incorporation of neural and haemal elements is more similar to the holocephalans, but differs from the batoid chondrichthyans.     

Patterns of Evolution in the Feeding Mechanism of Actinopterygian Fishes

SYNOPSIS. Structural and functional patterns in the evolutionof the actinopterygian feeding mechanism are discussed in thecontext of the major monophyletic lineages of ray-finned fishes.A tripartite adductor mandibulae contained in a maxillary-palatoquadratechamber and a single mechanism of mandibular depression mediatedby the obliquus inferioris, sternohyoideus, and hyoid apparatusare primitive features of the Actinopterygii. Halecostome fishesare characterized by having an additional mechanism of mandibulardepression, the levator operculi—opercular series coupling,and a maxilla which swings anteriorly during prey capture. Theseinnovations provide the basis for feeding by inertial suctionwhich is the dominant mode of prey capture throughout the halecostomeradiation. A remarkably consistent kinematic profile occursin all suction-feeding halecostomes. Teleost fishes possessa number of specializations in the front jaws including a geniohyoideusmuscle, loss of the primitive suborbital adductor component,and a mobile premaxilla. Structural innovations in teleost pharyngealjaws include fusion of the dermal tooth plates with endoskeletalgill arch elements, the occurrence of a pharyngeal retractormuscle, and a shift in the origin of the pharyngohyoideus. Thesespecializations relate to increased functional versatility ofthe pharyngeal jaw apparatus as demonstrated by an electromyographicstudy of pharyngeal muscle activity in Esox and Ambloplites.The major feature of the evolution of the actinopterygian feedingmechanism is the increase in structural complexity in both thepharyngeal and front jaws. Structural diversification is a functionof the number of independent biomechanical pathways governingmovement.     

Very low pressures drive ventilatory flow in chimaeroid fishes

Chimaera (Holocephali) are cartilaginous fishes with flexible operculi rather than external gill slits, suggesting ventilation occurs in a manner different from other fishes. We examined holocephalan ventilation morphology, behavior, and performance by anatomical investigations, high‐speed video, and in vivo pressure measurements from the buccal and parabranchial cranial cavities in Hydrolagus colliei and Callorhinchus callorynchus. Ventilatory modes ranged from quiet resting breathing to rapid “active” breathing, yet external cranial movements—excepting the passive movement of the opercular flap—were always extremely subtle, and pressures generated were one to two orders of magnitude lower than those of other fishes. To explain ventilation with such minimal pressure generation and cranial motion, we propose an “accordion” model, whereby rostrocaudal movement of the visceral arches drives pressure differentials, albeit with little lateral or ventral movement. Chimaeroids have comparatively large oropharyngeal cavities, which can move fluid with a smaller linear dimension change than the comparatively smaller cavities of other fishes. Orobranchial pressures are often less than parabranchial pressures, suggesting flow in the “wrong” direction; however, the long gill curtains of chimaeroids may passively restrict backflow. We suggest that constraints on holocephalan jaw and hyoid movements were compensated for evolutionarily by novel visceral arch mechanics and kinematics. J. Morphol., 2012. © 2011 Wiley Periodicals, Inc.     

Double-mouth deformity in a trout (Salmo trutta) and its cause

Gudger (1930) ends an article on this deformity by stating that double-mouth deformity in fishes is always due to injury so far as our present knowledge goes. The feature common to all cases is displacement of the lower end of the hyoid arch downwards and backwards through a gap in the mouth floor. This occurs because the protractor muscles of the arch have been put out of action, usually by severe accidental injury. The retractor muscles, thus left unopposed, pull the lower end of the arch into the deformed position. It is difficult to imagine how accidental wound could produce the condition seen in the Shetland trout. Here is only a cleft like a clean cut in the midline of the mouth floor ending at the displaced arch. There is neither irregular scarring nor obvious tissue loss, the head retaining its bilateral symmetry. In it the protractors of the arch must also have been destroyed, but probably by some other kind of damage than wound from without. With this possibility in mind I wrote to the managers of several trout-farms, enclosing a sketch of the deformity. Each was asked if he had come across anything like it when grading his stock. One letter in the affirmative suggested that air trapped in the floor of the mouth might be the cause. Later the writer sent me two young trout, radiographs of which confirmed this statement and led me to think that obstruction of the pneumatic duct might account for the trapped air. The consequences of extirpation of the swimbladder in physostomes explains how the trapped air is permanently at increased pressure, and supports this hypothesis.     

Functional morphology of the feeding apparatus,feeding constraints,and suction performance in the nurse shark Ginglymostoma cirratum

The nurse shark, Ginglymostoma cirratum, is an obligate suction feeder that preys on benthic invertebrates and fish. Its cranial morphology exhibits a suite of structural and functional modifications that facilitate this mode of prey capture. During suction‐feeding, subambient pressure is generated by the ventral expansion of the hyoid apparatus and the floor of its buccopharyngeal cavity. As in suction‐feeding bony fishes, the nurse shark exhibits expansive, compressive, and recovery kinematic phases that produce posterior‐directed water flow through the buccopharyngeal cavity. However, there is generally neither a preparatory phase nor cranial elevation. Suction is generated by the rapid depression of the buccopharyngeal floor by the coracoarcualis, coracohyoideus, and coracobranchiales muscles. Because the hyoid arch of G. cirratum is loosely connected to the mandible, contraction of the rectus cervicis muscle group can greatly depress the floor of the buccopharyngeal cavity below the depressed mandible, resulting in large volumetric expansion. Suction pressures in the nurse shark vary greatly, but include the greatest subambient pressures reported for an aquatic‐feeding vertebrate. Maximum suction pressure does not appear to be related to shark size, but is correlated with the rate of buccopharyngeal expansion. As in suction‐feeding bony fishes, suction in the nurse shark is only effective within approximately 3 cm in front of the mouth. The foraging behavior of this shark is most likely constrained to ambushing or stalking due to the exponential decay of effective suction in front of the mouth. Prey capture may be facilitated by foraging within reef confines and close to the substrate, which can enhance the effective suction distance, or by foraging at night when it can more closely approach prey. J. Morphol., 2008. © 2008 Wiley‐Liss, Inc.