Functional morphology of the feeding mechanism in aquatic ambystomatid salamanders

This study addresses four questions in vertebrate functional morphology through a study of aquatic prey capture in ambystomatid salamanders: (1) How does the feeding mechanism of aquatic salamanders function as a biomechanical system? (2) How similar are the biomechanics of suction feeding in aquatic salamanders and ray-finned fishes? (3) What quantitative relationship does information extracted from electromyograms of striated muscles bear to kinematic patterns and animal performance? and (4) What are the major structural and functional patterns in the evolution of the lower vertebrate skull? During prey capture, larval ambystomatid salamanders display a kinematic pattern similar to that of other lower vertebrates, with peak gape occurring prior to both peak hyoid depression and peak cranial elevation. The depressor mandibulae, rectus cervicis, epaxialis, hypaxialis, and branchiohyoideus muscles are all active for 40–60 msec during the strike and overlap considerably in activity. The two divisions of the adductor mandibulae are active in a continuous burst for 110–130 msec, and the intermandibularis posterior and coracomandibularis are active in a double burst pattern. The antagonistic depressor mandibulae and adductor mandibulae internus become active within 0.2 msec of each other, but the two muscles show very different spike and amplitude patterns during their respective activity periods. Coefficients of variation for kinematic and most electromyographic recordings reach a minimum within a 10 msec time period, just after the mouth starts to open. Pressure within the buccal cavity during the strike reaches a minimum of ?25 mmHg, and minimum pressure occurs synchronously with maximum gill bar adduction. The gill bars (bearing gill rakers that interlock with rakers of adjacent arches) clearly function as a resistance within the oral cavity and restrict posterior water influx during mouth opening, creating a unidirectional flow during feeding. Durations of electromyographic activity alone are poor predictors of kinematic patterns. Analyses of spike amplitude explain an additional fraction of the variance in jaw kinematics, whereas the product of spike number and amplitude is the best statistical predictor of kinematic response variables. Larval ambystomatid salamanders retain the two primitive biomechanical systems for opening and closing the mouth present in nontetrapod vertebrates: elevation of the head by the epaxialis and depression of the mandible by the hyoid apparatus.     

Morphology and function of the feeding apparatus of the lungfish, Lepidosiren paradoxa (Dipnoi)

The feeding mechanism of the South American lungfish, Lepidosiren paradoxa retains many primitive teleostome characteristics. In particular, the process of initial prey capture shares four salient functional features with other primitive vertebrates: 1) prey capture by suction feeding, 2) cranial elevation at the cranio-vertebral joint during the mouth opening phase of the strike, 3) the hyoid apparatus plays a major role in mediating expansion of the oral cavity and is one biomechanical pathway involved in depressing the mandible, and 4) peak hyoid excursion occurs after maximum gape is achieved. Lepidosiren also possesses four key morphological and functional specializations of the feeding mechanism: 1) tooth plates, 2) an enlarged cranial rib serving as a site for the origin of muscles depressing the hyoid apparatus, 3) a depressor mandibulae muscle, apparently not homologous to that of amphibians, and 4) a complex sequence of manipulation and chewing of prey in the oral cavity prior to swallowing. The depressor mandibulae is always active during mouth opening, in contrast to some previous suggestions. Chewing cycles include alternating adduction and transport phases. Between each adduction, food may be transported in or out of the buccal cavity to position it between the tooth plates. The depressor mandibulae muscle is active in a double-burst pattern during chewing, with the larger second burst serving to open the mouth during prey transport. Swallowing is characterized by prolonged activity in the hyoid constrictor musculature and the geniothoracicus. Lepidosiren uses hydraulic transport achieved by movements of the hyoid apparatus to position prey within the oral cavity. This function is analogous to that of the tongue in many tetrapods.     

The plagiosaurid temnospondyl Plagiosuchus pustuliferus (Amphibia: Temnospondyli) from the Middle Triassic of Germany: anatomy and functional morphology of the skull

The cranial anatomy of the plagiosaurid temnospondyl Plagiosuchus pustuliferus, from the Middle Triassic of Germany, is described in detail on the basis of a newly discovered skull and mandibular material. The highly derived skull is characterized by huge orbitotemporal fenestrae, a reduction of the circumorbital bones – the prefrontal, postfrontal and (probably) postorbital are lost – and the expansion of the jugal to occupy most of the lateral skull margin. Ventrally the extremely long subtemporal vacuities correlate with the elongate adductor fossa of the mandible. The dentition is feebly developed on both skull and mandible. Ossified ?ceratobranchials and ‘branchial denticles’ indicate the presence of open gills clefts in life. The remarkably divergent cranial morphology of P. pustuliferus highlights the extraordinary cranial diversity within the Plagiosauridae, probably unsurpassed within the Temnospondyli. Specific structural aspects of the skull – including an extremely short marginal tooth row, feeble dentition and an elongated chamber for adductor musculature – together with evidence for a hyobranchial skeleton, suggests that P. pustuliferus utilized directed suction feeding for prey capture. © 2009 The Linnean Society of London, Zoological Journal of the Linnean Society, 2009, 155 , 348–373.     

The hyal and ventral branchial muscles in caecilian and salamander larvae: Homologies and evolution

Amphibians (Lissamphibia) are characterized by a bi‐phasic life‐cycle that comprises an aquatic larval stage and metamorphosis to the adult. The ancestral aquatic feeding behavior of amphibian larvae is suction feeding. The negative pressure that is needed for ingestion of prey is created by depression of the hyobranchial apparatus as a result of hyobranchial muscle action. Understanding the homologies of hyobranchial muscles in amphibian larvae is a crucial step in understanding the evolution of this important character complex. However, the literature mostly focuses on the adult musculature and terms used for hyal and ventral branchial muscles in different amphibians often do not reflect homologies across lissamphibian orders. Here we describe the hyal and ventral branchial musculature in larvae of caecilians (Gymnophiona) and salamanders (Caudata), including juveniles of two permanently aquatic salamander species. Based on previous alternative terminology schemes, we propose a terminology for the hyal and ventral branchial muscles that reflects the homologies of muscles and that is suited for studies on hyobranchial muscle evolution in amphibians. We present a discussion of the hyal and ventral branchial muscles in larvae of the most recent common ancestor of amphibians (i.e. the ground plan of Lissamphibia). Based on our terminology, the hyal and ventral branchial musculature of caecilians and salamanders comprises the following muscles: m. depressor mandibulae, m. depressor mandibulae posterior, m. hyomandibularis, m. branchiohyoideus externus, m. interhyoideus, m. interhyoideus posterior, m. subarcualis rectus I, m. subarcualis obliquus II, m. subarcualis obliquus III, m. subarcualis rectus II‐IV, and m. transversus ventralis IV. Except for the m. branchiohyoideus externus, all muscles considered herein can be assigned to the ground plan of the Lissamphibia with certainty. The m. branchiohyoideus externus is either apomorphic for the Batrachia (frogs + salamanders) or salamander larvae depending on whether or not a homologous muscle is present in frog tadpoles. J. Morphol., 2011. © 2011 Wiley‐Liss, Inc.     

Braincase,palatoquadrate and ear region of the plagiosaurid Gerrothorax pulcherrimus from the Middle Triassic of Germany

Abstract: The complete neurocranium plus palatoquadrate of the plagiosaurid temnospondyl Gerrothorax pulcherrimus from the Middle Triassic of Germany is described for the first time, based on outer morphological observations and micro‐CT scanning. The exoccipitals are strong elements with paroccipital processes and well‐separated occipital condyles. Anterolaterally, the exoccipitals contact the otics, which are mediolaterally elongated and have massive lateral walls. The otics contact the basisphenoid, which shows well‐developed sellar processes. Anteriorly, the basisphenoid is continuous with the sphenethmoid region. In its posterior portion, the sphenethmoid gives rise to robust, laterally directed laterosphenoid walls, a unique morphology among basal tetrapods. The palatoquadrate is extensively ossified. The quadrate portion overlaps the descending lamina of squamosal and ascending lamina of pterygoid anteriorly, almost contacting the epipterygoid laterally. The epipterygoid is a complex element and may be co‐ossified with otics and laterosphenoid walls. It has a broad, sheet‐like footplate and a horizontally aligned ascending process that contacts the laterosphenoid walls. The degree of ossification of the epipterygoid, however, is subject to individual variation obviously independent from ontogenetic changes. The stapes of Gerrothorax is a large, blade‐like element that differs conspicuously from the plesiomorphic temnospondyl condition. It has a prominent anterolateral projection which has not been observed in other basal tetrapods. Morphology of neurocranium and palatoquadratum of Gerrothorax most closely resembles that of the Russian plagiosaurid Plagiosternum danilovi, although the elements are less ossified in the latter. The extensive endocranial ossification of Gerrothorax is consistent with the general high degree of ossification in the exo‐ and endoskeleton of this temnospondyl and supports the view that a strong endocranial ossification cannot be evaluated as a plesiomorphic character in basal tetrapods.     

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.     

Metamorphosis of the feeding mechanism in tiger salamanders (Ambystoma tigrinum): the ontogeny of cranial muscle mass

Most previous research on metamorphosis of the musculoskeletal system in vertebrates has focused on the transformation of the skeleton. In this paper we focus on the transformation of the muscles of the head during metamorphosis in tiger salamanders ( Ambystoma tigrinum ) in order (1) to provide new data on changes in myology during ontogeny, and (2) to aid in interpreting previous data on the metamorphosis of function in the head of salamanders.
The physiological cross-sectional area of nine head muscles was calculated by measuring fibre angles, fibre lengths, and muscle mass in two samples of tiger salamanders obtained just before and just after metamorphosis. The major mouth-opening muscles (rectus cervicis and depressor mandibulae) exhibit a significant decrease in estimated maximum tetanic tension (MTT) across metamorphosis of about 36%. The jaw-closing muscles (adductor mandibulae internus and externus) and the head-lifting muscles (epaxials) also decrease in MTT but not significantly. The muscles associated with tongue projection during feeding on land (the subarcualis rectus I, geniohyoideus, interhyoideus and intermandibularis) all show a slight increase in MTT at metamorphosis.
Metamorphic transformation of feeding behaviour in Ambystoma tigrinum involves changes in performance, the design of skeletal elements, changes in muscle force-generating capability, and changes in hydrodynamic design from unidirectional flow in larvae to bidirectional flow during aquatic feeding after metamorphosis. Although muscle activity patterns during aquatic feeding do not change across metamorphosis, tongue-based terrestrial feeding involves a suite of novel muscle activity patterns, morphological characters acquired at metamorphosis, and a metamorphic increase in the masses of muscles important in tongue projection.     

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.     

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.     

Comparative anatomy and evolutionary history of suction feeding in cetaceans

Some odontocetes possess unique features of the hyolingual apparatus that are involved in suction feeding. The hyoid bone and associated musculature generates rapid, piston‐like retraction, and depression of the hyoid and tongue. “Capture” suction feeders (e.g., Globicephala) use suction for capturing and swallowing prey. “Combination” feeders (i.e., Lagenorhynchus) use both raptorial feeding (to capture prey) and suction (to ingest prey). In “capture” suction feeders, features of the hyoid and skull have been attributed to creating suction (i.e., large surface area and mandibular bluntness). In addition to odontocetes, a mysticete, the gray whale (Eschrichtius robustus), is considered a benthic suction feeder. However, anatomical studies of purported suction‐feeding structures of the gray whale are lacking. In addition, few studies have utilized evolutionary approaches to understand the history of suction feeding in cetaceans. This study incorporates quantitative and qualitative hyoid and cranial data from 35 extant and 14 extinct cetacean species into a multivariate principal component analysis and comparative phylogenetic analyses. Conclusions from these analyses are that some commonly attributed features (i.e., ventral throat grooves and mandibular bluntness) and one principal component are significantly correlated with suction feeding. Finally, ancestral state reconstructions indicate that suction feeding likely evolved once, early in cetacean evolutionary history.     

Cranial morphology of an American siphonopid, Microcaecilia unicolor (Amphibia, Gymnophiona) and its functional interpretation

The skull of Microcaecilia unicolor, american Siphonopidae (Amphibia, Gymnophiona), shows 3 notable morphological characteristics: The mandibular shortening, the verticalization of the retroarticular process, and the verticalization of the quadrate. They define a peculiar morphofunctional pattern, which seems to exist in dwarf forms moving in the complex root system of trees. These morphological characters, associated with modifications of the muscle depressor mandibulae, give functional advantages: A wider gaping of the mouth and the ability of the ingestion of preys which have a great cross-section. In keeping its macrophageous habits, Microcaecilia unicolor does not compete with other dwarf vertebrates living in the same environment and feeding on microinvertebrates.     

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.     

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     

Effects of prey type on motor pattern variance in tetraodontiform fishes

It is unclear whether the high variance of electromyographic parameters measured in feeding teleost fishes reflects functionally significant motor variation that is under control of the fish, or functionally insignificant variation characteristic of EMG data. We addressed this issue by examining the effect of three prey, differing in physical characteristics, on the feeding motor pattern in three fishes of the Order Tetraodontiformes: the filefish, Monacanthus hispidus; the triggerfish, Balistes capriscus; and the puffer, Sphoeroides nephelus. EMG recordings were made from subdivisions of the mouth closing adductor mandibulae muscle and the mouth opening levator operculi muscle in four fish from each species feeding on live fiddler crabs, live shrimp, and pieces of cut squid mantle. Analysis of variance was used to test for effects of prey type on the standard deviation of muscle burst duration, burst onset time, and average burst amplitude in the adductor muscles. The filefish exhibited a doubling of standard deviation of burst duration in all muscles when feeding on fiddler crabs; triggerfish showed increased standard deviations in onset times and duration of two muscles when feeding on squid mantle; and the puffer showed no effects of prey on motor variability. The observation that prey type can elicit more than a doubling in the standard deviation of some EMG traits indicates that a large portion of the within-prey type variance is under direct control of the individual fish, suggesting an even greater level of fine motor control in teleost feeding mechanisms than previously recognized.     

Hyobranchial and postcranial ontogeny of the temnospondylOnchiodon labyrinthicus (Geinitz, 1861) from Niederhäslich (Dohlen Basin, Autunian, Saxony)

Hyobranchium, postcranial skeleton, and developmental events during ontogeny of the temnospondylOnchiodon labyrinthicus from the Dohlen Basin (Autunian, Saxony) are described. At a skull length of approximately 20 mm, the scapulocoracoid appeared, but ossified very slowly. The ischium ossified distinctly later than the stout ilium and later than the scapulocoracoid. The stapes can be determined in specimens beyond 26 mm skull length, and the exoccipitals started to ossify probably at 40 mm, followed by the quadrate. Vertebral centra ossified in early juveniles at approximately 50 mm skull length. The larval hyobranchium with ossified basibranchial and ceratobranchials indicates strong suction feeding. The bony ceratobranchials were resorbed after the larval period. The poorly ossified postcranium suggests that juveniles lived semiterrestrially.     

Form and function of the feeding apparatus of Alligator mississippiensis

The architecture of the jaw muscles and their tendons of Alligator mississippiensis is described and their function examined by electromyography. Alligator grabs its prey with forward lunges or rapid lateral movements of the head. It does not engage in regular masticatory cycles. Prey is manipulated by inertial movements and the tongue does not appear to play any role in transport. The Mm. adductor mandibulae externus, adductor mandibulae posterior, and pterygoideus activate bilaterally and simultaneously during rapid closing or crushing. The M. pterygoideus does not act during prey holding whereas the Mm. adductor mandibulae externus, adductor mandibulae posterior continue to be active. The Mm. depressor mandibulae and intramandibularis are variably active during both jaw opening and closing.     

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.     

THE EVOLUTION OF TETRAPOD FEEDING BEHAVIOR: KINEMATIC HOMOLOGIES IN PREY TRANSPORT

One of the major features of the aquatic-to-terrestrial transition in vertebrate evolution was the change in the mechanism used to transport prey from the jaws to the throat. Primarily, vertebrates use hydraulic transport, but the transition to terrestrial life was accompanied by modifications of the hyobranchial apparatus that permit tongue-based transport. Despite an extensive data base on amniote feeding systems and mechanisms of intraoral prey transport, few data are available on the mechanism of prey transport in anamniote tetrapods. Transport cycles of four Ambystoma tigrinum (Amphibia) feeding on worms and crickets were filmed at 150 flames per second to produce quantitative profiles of the intraoral transport cycles for the two prey types. During the transport cycle the head and body remain stationary relative to the background: transport in Ambystoma tigrinum thus does not involve inertial movements of the head or body. Prey type had little effect on the kinematics of prey transport. The process of prey transport may be divided into four phases: preparatory, fast opening, closing, and recovery. The preparatory phase itself is divided into two parts: an extended segment that may include slight slow opening and a static phase prior to mouth opening where no change in gape occurs. The kinematic profile of transport in terrestrial salamanders is extremely similar to that used by fishes during hydraulic (aquatic) prey transport. We hypothesize that the distinct recovery and preparatory phases in the transport cycle of anamniote tetrapods are together homologous to the slow opening phases of the amniote cycle, and that during the evolution of terrestrial prey processing systems the primitive extended preparatory phase has become greatly compressed and incorporated into the amniote gape cycle.     

Functional morphology of tongue projection in Taricha torosa (Urodela: Salamandridae)

The kinematics of tongue projection by terrestrial adult California newts, Taricha torosa (Rathke, 1833), are described based upon high-speed cinematography. Tongue projection results from coupled anterior movements of the ceratohyals and branchial arches. Four distinct periods are defined during a projection sequence: preparation, tongue projection, tongue recovery and mouth closing. Key anatomical correlates of projection are described, with special emphasis on the mobility of the hyoid arch. Adult Taricha (Gray, 1850) have lost the mandibulo-hyoid ligament and reduced additional connective tissues present in larvae. These changes decouple the hyoid arch from mouth opening and release the ceratohyals to participate in a tongue projection system distinct from those of ambystomatids and plethodontids. These phylogenetic differences pose questions about the evolution of tongue projection systems in terrestrial urodeles. Currently available data are consistent with the interpretation that terrestrial urodeles have independently evolved specialized tongue projection systems at least twice: the ceratohyal-stable mode of plethodontids and the ceratohyal-mobile system of newts. In all cases, an essential underlying (= plesiomorphic) feature is the presence of the depressor mandibulae muscle. We regard this pathway for mouth opening as a prerequisite which liberated the hyobranchium for alternative function. Comprehensive studies of the mandibulo-hyoid ligament and depressor mandibulae will be vital to modelling the evolution of specialized tongue projection systems of urodeles.