Variation in limb loading magnitude and timing in tetrapods.

Comparative analyses of locomotion in tetrapods reveal two patterns of stride cycle variability. Tachymetabolic tetrapods (birds and mammals) have lower inter-cycle variation in stride duration than bradymetabolic tetrapods (amphibians, lizards, turtles and crocodilians). This pattern has been linked to the fact that birds and mammals share enlarged cerebella, relatively enlarged and heavily myelinated Ia afferents, and γ-motoneurons to their muscle spindles. Both tachymetabolic tetrapod lineages also possess an encapsulated Golgi tendon morphology, thought to provide more spatially precise information on muscle tension. The functional consequence of this derived Golgi tendon morphology has never been tested. We hypothesized that one advantage of precise information on muscle tension would be lower and more predictable limb bone stresses, achieved in tachymetabolic tetrapods by having less variable substrate reaction forces than bradymetabolic tetrapods. To test this hypothesis, we analyzed hindlimb substrate reaction forces during locomotion of 55 tetrapod species in a phylogenetic comparative framework. Variation in species means of limb loading magnitude and timing confirm that, for most of the variables analyzed, variance in hindlimb loading and timing is significantly lower in species with encapsulated versus unencapsulated Golgi tendon organs. These findings suggest that maintaining predictable limb loading provides a selective advantage for birds and mammals by allowing energy savings during locomotion, lower limb bone safety factors and quicker recovery from perturbations. The importance of variation in other biomechanical variables in explaining these patterns, such as posture, effective mechanical advantage and center-of-mass mechanics, remains to be clarified.

Joint angular excursions during cyclical behaviors differ between tetrapod feeding and locomotor systems.

Tetrapod musculoskeletal diversity is usually studied separately in feeding and locomotor systems. However, comparisons between these systems promise important insight into how natural selection deploys the same basic musculoskeletal toolkit - connective tissues, bones, nerves and skeletal muscle - to meet the differing performance criteria of feeding and locomotion. In this study, we compare average joint angular excursions during cyclic behaviors - chewing, walking and running - in a phylogenetic context to explore differences in the optimality criteria of these two systems. Across 111 tetrapod species, average limb-joint angular excursions during cyclic locomotion are greater and more evolutionarily labile than those of the jaw joint during cyclic chewing. We argue that these findings reflect fundamental functional dichotomies between tetrapod locomotor and feeding systems. Tetrapod chewing systems are optimized for precise application of force over a narrower, more controlled and predictable range of displacements, the principal aim being to fracture the substrate, the size and mechanical properties of which are controlled at ingestion and further reduced and homogenized, respectively, by the chewing process. In contrast, tetrapod limbed locomotor systems are optimized for fast and energetically efficient application of force over a wider and less predictable range of displacements, the principal aim being to move the organism at varying speeds relative to a substrate whose geometry and mechanical properties need not become more homogeneous as locomotion proceeds. Hence, the evolution of tetrapod locomotor systems has been accompanied by an increasing diversity of limb-joint excursions, as tetrapods have expanded across a range of locomotor substrates and environments.

A comparative study of single-leg ground reaction forces in running lizards.

The role of different limbs in supporting and propelling the body has been studied in many species with animals appearing to have either similarity in limb function or differential limb function. Differential hindlimb versus forelimb function has been proposed as a general feature of running with a sprawling posture and as benefiting sprawled postured animals by enhancing maneuvering and minimizing joint moments. Yet only a few species have been studied and thus the generality of differential limb function in running animals with sprawled postures is unknown. We measured the limb lengths of seven species of lizard and their single-limb three-dimensional ground reaction forces during high-speed running. We found that all species relied on the hindlimb for producing accelerative forces. Braking forces were forelimb dominated in four species and equally distributed between limbs in the other three. Vertical forces were dominated by the hindlimb in three species and equally distributed between the forelimb and hindlimb in the other four. Medial forces were dominated by the hindlimb in four species and equally distributed in the other three, with all Iguanians exhibiting hindlimb-biased medial forces. Relative hindlimb to forelimb length of each species was related to variation in hindlimb versus forelimb medial forces; species with relatively longer hindlimbs compared with forelimbs exhibited medial forces that were more biased towards the hindlimbs. These results suggest that the function of individual limbs in lizards varies across species with only a single general pattern (hindlimb-dominated accelerative force) being present.

Landing in basal frogs: evidence of saltational patterns in the evolution of anuran locomotion.

All frogs are assumed to jump in a similar manner by rapidly extending hindlimbs during the propulsive phase and rotating the limbs forward during flight in order to land forelimbs first. However, studies of jumping behavior are lacking in the most primitive living frogs of the family Leiopelmatidae. These semi-aquatic or terrestrial anurans retain a suite of plesiomorphic morphological features and are unique in using an asynchronous (trot-like) rather than synchronous "frog-kick" swimming gait of other frogs. We compared jumping behavior in leiopelmatids to more derived frogs and found that leiopelmatids maintain extended hindlimbs throughout flight and landing phases and do not land on adducted forelimbs. These "belly-flop" landings limit the ability for repeated jumps and are consistent with a riparian origin of jumping in frogs. The unique behavior of leiopelmatids shows that frogs evolved jumping before they perfected landing. Moreover, an inability to rapidly cycle the limbs may provide a functional explanation for the absence of synchronous swimming in leiopelmatids.

Breathing with your belly: abdominal exhalation, loco-ventilatory integration and size constraints on locomotion in small mammals.

In mammals, diaphragmatic contractions control inhalation while contraction of some thoracic hypaxial muscles and the transversus abdominis muscle contribute to exhalation. Additional thoracic hypaxial muscles are recruited as accessory ventilatory muscles to improve inhalation and exhalation during locomotion. However, the contribution of abdominal hypaxial muscles to resting and locomotor ventilation is little understood in mammals and loco-ventilatory integration has not been studied in small basal mammals. We show for the first time that all of the abdominal hypaxial muscles actively contribute to both resting and locomotory ventilation in mammals but in a size-dependent manner. In large opossums (Didelphis), hypaxial muscles exhibit uniform mild tonus during resting ventilation (pressurizing the gut to aid in exhalation) and shift to phasic bursts of activity during each exhalation during locomotion. Smaller opossums (Monodelphis) actively exhale by firing the abdominal hypaxial muscles at approximately 10Hz at both rest and at preferred locomotor speeds. Furthermore, the large opossums entrained ventilation to limb cycling as speed increased while the small opossums entrained limb cycling to the resting ventilation rate during locomotion. Differences in these species are related to size effects on the natural frequency of the ventilatory system and increasing resting ventilation rates at small size. Large mammals, with lower resting ventilation rates, can increase ventilatory rates during locomotion, while the high resting ventilation rates of small mammals limits their ability to increase ventilation rates during locomotion. We propose that increase in mammalian body size during the Cenozoic may have been an adaptation or exaptation to overcome size effects on ventilation frequency.

Posture, gait and the ecological relevance of locomotor costs and energy-saving mechanisms in tetrapods.

A reanalysis of locomotor data from functional, energetic, mechanical and ecological perspectives reveals that limb posture has major effects on limb biomechanics, energy-saving mechanisms and the costs of locomotion. Regressions of data coded by posture (crouched vs. erect) reveal nonlinear patterns in metabolic cost, limb muscle mass, effective mechanical advantage, and stride characteristics. In small crouched animals energy savings from spring and pendular mechanisms are inconsequential and thus the metabolic cost of locomotion is driven by muscle activation costs. Stride frequency appears to be the principal functional parameter related to the decreasing cost of locomotion in crouched animals. By contrast, the shift to erect limb postures invoked a series of correlated effects on the metabolic cost of locomotion: effective mechanical advantage increases, relative muscle masses decrease, metapodial limb segments elongate dramatically (as limbs shift from digitigrade to unguligrade designs) and biological springs increase in size and effectiveness. Each of these factors leads to decreases in the metabolic cost of locomotion in erect forms resulting from real and increasing contributions of pendular savings and spring savings. Comparisons of the relative costs and ecological relevance of different gaits reveal that running is cheaper than walking in smaller animals up to the size of dogs but running is more expensive than walking in horses. Animals do not necessarily use their cheapest gaits for their predominant locomotor activity. Therefore, locomotor costs are driven more by ecological relevance than by the need to optimize locomotor economy.

Tuataras and salamanders show that walking and running mechanics are ancient features of tetrapod locomotion.

The lumbering locomotor behaviours of tuataras and salamanders are the best examples of quadrupedal locomotion of early terrestrial vertebrates. We show they use the same walking (out-of-phase) and running (in-phase) patterns of external mechanical energy fluctuations of the centre-of-mass known in fast moving (cursorial) animals. Thus, walking and running centre-of-mass mechanics have been a feature of tetrapods since quadrupedal locomotion emerged over 400 million years ago. When walking, these sprawling animals save external mechanical energy with the same pendular effectiveness observed in cursorial animals. However, unlike cursorial animals (that change footfall patterns and mechanics with speed), tuataras and salamanders use only diagonal couplet gaits and indifferently change from walking to running mechanics with no significant change in total mechanical energy. Thus, the change from walking to running is not related to speed and the advantage of walking versus running is unclear. Furthermore, lumbering mechanics in primitive tetrapods is reflected in having total mechanical energy driven by potential energy (rather than kinetic energy as in cursorial animals) and relative centre-of-mass displacements an order of magnitude greater than cursorial animals. Thus, large vertical displacements associated with lumbering locomotion in primitive tetrapods may preclude their ability to increase speed.

Functional evolution of jumping in frogs: Interspecific differences in take-off and landing.

Ancestral frogs underwent anatomical shifts including elongation of the hindlimbs and pelvis and reduction of the tail and vertebral column that heralded the transition to jumping as a primary mode of locomotion. Jumping has been hypothesized to have evolved in a step-wise fashion with basal frogs taking-off with synchronous hindlimb extension and crash-landing on their bodies, and then their limbs move forward. Subsequently, frogs began to recycle the forelimbs forward earlier in the jump to control landing. Frogs with forelimb landing radiated into many forms, locomotor modes, habitats, and niches with controlled landing thought to improve escape behavior. While the biology of take-off behavior has seen considerable study, interspecific comparisons of take-off and landing behavior are limited. In order to understand the evolution of jumping and controlled landing in frogs, data are needed on the movements of the limbs and body across an array of taxa. Here, we present the first description and comparison of kinematics of the hindlimbs, forelimbs and body during take-off and landing in relation to ground reaction forces in four frog species spanning the frog phylogeny. The goal of this study is to understand what interspecific differences reveal about the evolution of take-off and controlled landing in frogs. We provide the first comparative description of the entire process of jumping in frogs. Statistical comparisons identify both homologous behaviors and significant differences among species that are used to map patterns of trait evolution and generate hypotheses regarding the functional evolution of take-off and landing in frogs.

Functional morphology of feeding and gill irrigation in the anuran tadpole: electromyography and muscle function in larval Rana catesbeiana.

This study provides the first data on muscle activity patterns during active feeding in a larval anuran. Data regarding muscle function during gill irrigation and hyperexpiration are also provided. Electromyographic and kinematic data were recorded from six mandibular and hyoid muscles in unanesthetized, unrestrained larvae of Rana catesbeiana. Only three (hyoangularis, orbitohyoideus, anterior interhyoideus) of the six muscles examined are active during gill irrigation. Feeding cycles are characterized by the recruitment of three additional muscles: intermandibularis, suspensorioangularis, and levator mandibulae longus superficialis. The latter two contribute, respectively, to wide opening and forceful closing of the mouth during feeding. Hyperexpiration is characterized by a reversal of water flow anteriorly out of the mouth. This hydrodynamic change occurs due to modulation of the timing of firing of the anterior interhyoideus, as well as recruitment of the posterior interhyoideus, which is only active during hyperexpiration. Both regions of the interhyoideus, which are responsible for evacuation of the buccal cavity, are active during the opening phase of hyperexpiration. Kinematically, transitioning from gill irrigation to feeding involves both an overall shortening of the gape cycle and a shift in the relative length of opening phase vs. closing phase. Our results corroborate many of the findings of Gradwell ([1972] Can J Zool 50:501-521) regarding muscle function during gill irrigation and hyperexpiration. Furthermore, we demonstrate that in larval anurans the transition from gill irrigation to feeding involves modulation of gape cycle kinematics, changes in the level of activity of muscles, and recruitment of muscles that are not active during irrigation. In light of new data presented here, a review of muscle function in tadpoles is also provided.

Testing amniote models of prey transport kinematics: a quantitative analysis of mouth opening patterns in lizards.

Two models have been proposed to describe the prey transport kinematics of terrestrial vertebrates (Bramble and Wake, 1985; Reilly and Lauder, 1990). The critical difference between the models is the presence or absence of a slow open-II phase (SO-II) in the gape profile during mouth opening. Each of these models has been applied to lizards, however to date, lizard feeding kinematics have not been adequately quantified to assess the utility of these models for this clade. Neither model has been sufficiently tested due to the lack of a methodology to assess the specific differences between the models. We describe a method that uses explicit mathematical criteria to define the kinematic phases in tetrapod feeding. This "slope analysis& is used to precisely quantify and compare the transport kinematics of seven lizard species. Lizard transport kinematics were highly variable both within and across taxa. However, several common gape cycle patterns were identified. The predominant patterns were slow-fast opening (37.3%), fast opening only (22.9%) and slow opening only (21.2%). The most common pattern explicitly fits the prediction of the Reilly and Lauder model while the other two are similar to patterns observed in salamanders. Thus, lizards possess both the slow opening-fast opening pattern predicted for amniotes and the more primitive, simple opening pattern characteristic of more basal tetrapods. Plateau phases were found in only 12.8% of the profiles and only a fourth of these (3.4% of the total) explicitly fit the Bramble and Wake model (slow opening, plateau, fast opening) and two species never exhibited plateaus in their gape cycles. Thus, it is clear that the Bramble and Wake model is not supported as a generalized model for lizards or generalized tetrapods.

Symmetrical gaits and center of mass mechanics in small-bodied, primitive mammals.

Widely accepted relationships between gaits (footfall patterns) and center of mass mechanics have been formulated from observations for cursorial mammals. However, sparse data on smaller or more generalized forms suggest a fundamentally different relationship. This study explores locomotor dynamics in one eutherian and five metatherian (marsupials) mammals-all small-bodied (<2 kg) with generalized body plans that utilize symmetrical gaits. Across our sample, trials conforming to vaulting mechanics occurred least frequently (<10% of all trials) while bouncing mechanics was obtained most commonly (60%); the remaining trials represented mixed mechanics. Contrary to the common situation in large mammals, there was no evidence for discrete gait switching within symmetrical gaits as speed increased. This was in part due to the common practice of grounded running. The adaptive advantage of different patterns of center-of-mass motion and their putative energy savings remain questionable in small-bodied mammals.

The evolution of jumping in frogs: morphological evidence for the basal anuran locomotor condition and the radiation of locomotor systems in crown group anurans.

Our understanding of the evolution of frog locomotion follows from the work of Emerson in which anurans are proposed to possess one of three different iliosacral configurations: 1) a lateral-bending system found in walking and hopping frogs; 2) a fore-aft sliding mechanism found in several locomotor modes; and 3) a sagittal-hinge-type pelvis posited to be related to long-distance jumping performance. The most basal living (Ascaphus) and fossil (Prosalirus) frogs are described as sagittal-hinge pelvic types, and it has been proposed that long-distance jumping with a sagittal-hinge pelvis arose early in frog evolution. We revisited osteological traits of the pelvic region to conduct a phylogenetic analysis of the relationships between pelvic systems and locomotor modes in frogs. Using two of Emerson's diagnostic traits from the sacrum and ilium and two new traits from the urostyle, we resampled the taxa originally studied by Emerson and key paleotaxa and conducted an analysis of ancestral-character state evolution in relation to locomotor mode. We present a new pattern for the evolution of pelvic systems and locomotor modes in frogs. Character analysis shows that the lateral-bender, walker/hopper condition is both basal and generally conserved across the Anura. Long-distance jumping frogs do not appear until well within the Neobatrachia. The sagittal-hinge morphology is correlated with long-distance jumping in terrestrial frogs; however, it evolved convergently multiple times in crown group anurans with the same four pelvic traits described herein. Arboreal jumping has appeared in multiple crown lineages as well, but with divergent patterns of evolution involving each of the three pelvic types. The fore-aft slider morph appears independently in three different locomotor modes and, thus, is a more complex system than previously thought. Finally, it appears that the advent of a bicondylar sacro-urostylic articulation was originally related to providing axial rigidity to lateral-bending behaviors rather than sagittal bending.

Abdominal muscle and epipubic bone function during locomotion in Australian possums: insights to basal mammalian conditions and Eutherian-like tendencies in Trichosurus.

Mammals have four hypaxial muscle layers that wrap around the abdomen between the pelvis, ribcage, and spine. However, the marsupials have epipubic bones extending anteriorly into the ventral hypaxial layers with two additional muscles extending to the ventral midline and femur. Comparisons of South American marsupials to basal eutherians have shown that all of the abdominal hypaxials are active bilaterally in resting ventilation. However, during locomotion marsupials employ an asymmetrical pattern of activity as the hypaxial muscles form a crosscouplet linkage that uses the epipubic bone as a lever to provide long-axis support of the body between diagonal limb couplets during each step. In basal eutherians, this system shifts off the femur and epipubic bones (which are lost) resulting in a shoulder to pelvis linkage associated with shifts in both the positions and activity patterns of the pectineus and rectus abdominis muscles during locomotion. In this study, we present data on hypaxial function in two species (Pseudocheirus peregrinus and Trichosurus vulpecula) representing the two major radiations of possums in Australia: the Pseudocheiridae (within the Petauroidea) and the Phalangeridae. Patterns of gait, motor activity, and morphology in these two Australian species were compared with previous work to examine the generality of 1) the crosscouplet lever system as the basal condition for the Marsupialia and 2) several traits hypothesized to be common to all mammals (hypaxial tonus during resting ventilation, ventilation to step synchrony during locomotion, and bilateral transversus abdominis activity during locomotor expiration). Our results validate the presence of the crosscouplet pattern and basic epipubic bone lever system in Australian possums and confirm the generality of basal mammalian patterns. However, several novelties discovered in Trichosurus, reveal that it exhibits an evolutionary transition to intermediate eutherian-like morphological and motor patterns paralleling many other unique features of this species.

Abdominal muscle function in ventilation and locomotion in new world opossums and basal eutherians: Breathing and running with and without epipubic bones.

All tetrapods have the same four basic abdominal hypaxial muscle layers that wrap around the abdomen between the pelvis, ribcage, and spine. However, the marsupials and our immediate mammalian ancestors have epipubic bones extending anteriorly into the ventral hypaxial layers with two additional muscles connecting them to the ventral midline and femur. Studies of two marsupials have shown that all of the abdominal hypaxials play a part bilaterally in resting ventilation and during locomotion there is an asymmetrical pattern of activity as the hypaxial muscles form a cross-couplet linkage that uses the epipubic bone as a lever to provide long-axis support of the body between diagonal limb couplets during each step. The cross-couplet epipubic lever system defines the earliest mammals and is lost in placental mammals. To expand our understanding of the evolution of mammalian abdominal muscle function and loco-ventilatory integration we tested the generality of the cross-couplet system in marsupials and conducted the first formal studies of hypaxial abdominal motor patterns in generalized placental mammals focusing on a representative rodent and insectivore. These new data reveal 1) that continuous abdominal muscle tonus during resting ventilation and a 1:1 breath to step cycle during locomotion appear to be the basal condition for mammals, 2) that the loss of epipubic bones in eutherians is associated with a shift from the cross-couplet dominated motor pattern of marsupials to a shoulder-to-pelvis system with unilateral activation of abdominal muscles during locomotion and 3) that hypaxial function in generalized eutherians is more similar to marsupials than cursorial mammals.

The correlated evolution of biomechanics, gait and foraging mode in lizards.

Foraging mode has molded the evolution of many aspects of lizard biology. From a basic sit-and-wait sprinting feeding strategy, several lizard groups have evolved a wide foraging strategy, slowly moving through the environment using their highly developed chemosensory systems to locate prey. We studied locomotor performance, whole-body mechanics and gaits in a phylogenetic array of lizards that use sit-and-wait and wide-foraging strategies to contrast the functional differences associated with the need for speed vs slow continuous movement during foraging. Using multivariate and phylogenetic comparative analyses we tested for patterns of covariation in gaits and locomotor mechanics in relation to foraging mode. Sit-and-wait species used only fast speeds and trotting gaits coupled with running (bouncing) mechanics. Different wide-foraging species independently evolved slower locomotion with walking (vaulting) mechanics coupled with several different walking gaits, some of which have evolved several times. Most wide foragers retain the running mechanics with trotting gaits observed in sit-and-wait lizards, but some wide foragers have evolved very slow (high duty factor) running mechanics. In addition, three evolutionary reversals back to sit-and-wait foraging are coupled with the loss of walking mechanics. These findings provide strong evidence that foraging mode drives the evolution of biomechanics and gaits in lizards and that there are several ways to evolve slower locomotion. In addition, the different gaits used to walk slowly appear to match the ecological and behavioral challenges of the species that use them. Trotting appears to be a functionally stable strategy in lizards not necessarily related to whole-body mechanics or speed.

Correlation of symmetrical gaits and whole body mechanics: debunking myths in locomotor biodynamics.

Independent maturation of gait (Hildebrand) and whole body mechanics (Cavagna et al.) traditions in locomotor analyses has led to conflicting terminology. Re-evaluation of these traditions yields three primary insights. First, walking and running should be recognized by their fundamentally different mechanics. Because duty factor fails to consistently distinguish these mechanics, its use in discriminating walks from runs should be abandoned in preference to parameters that more accurately reflect the movements of the center of mass (COM; phase difference in external mechanical energy or Froude number). Second, "trot" should be reserved as a descriptor of a particular footfall pattern. This and all gait terms lack explicit information about limb compliance and thus COM movements. Third, symmetrical gait definitions should be broadened to reflect the four primary footfall patterns: the lateral-couplet dominated pattern of the pace, the diagonal-couplet dominated pattern of the trot and the more independent sequencing of footfalls of the two singlefoots. Intermediate gaits (perennially confusing and a mouthful to pronounce) are thereby subsumed by these four discrete gaits. Confusion between gait terminologies would be avoided if limb phase were consistently reported.

Hindlimb function in the alligator: integrating movements, motor patterns, ground reaction forces and bone strain of terrestrial locomotion.

Alligator hindlimbs show high torsional loads during terrestrial locomotion, in sharp contrast to the bending or axial compressive loads that predominate in animals that use parasagittal limb movements. The present study integrates new data on hindlimb muscle function with previously obtained data on hindlimb kinematics, motor patterns, ground reaction forces and bone strain in order to (1) assess mechanisms underlying limb bone torsion during non-parasagittal locomotion in alligators and (2) improve understanding of hindlimb dynamics during terrestrial locomotion. Three dynamic stance phase periods were recognized: limb-loading, support-and-propulsion, and limb-unloading phases. Shear stresses due to torsion were maximized during the limb-loading phase, during which the ground reaction force (GRF) and caudofemoralis (CFL) muscles generated opposing moments about the femur. Hindlimb retraction during the subsequent stance-and-propulsion phase involves substantial medial rotation of the femur, powered largely by coordinated action of the GRF and CFL. Several muscles that actively shorten to flex and extend limb joints during stance phase in sprawling and erect quadrupeds act in isometric or even eccentric contraction in alligators, stabilizing the knee and ankle during the support-and-propulsion phase. Motor patterns in alligators reveal the presence of local and temporal segregation of muscle functions during locomotion with muscles that lie side by side dedicated to performing different functions and only one of 16 muscles showing clear bursts of activity during both stance and swing phases. Data from alligators add to other recent discoveries that homologous muscles across quadrupeds often do not move joints the same way as is commonly assumed. Although alligators are commonly considered models for early semi-erect tetrapod locomotion, many aspects of hindlimb kinematics, muscle activity patterns, and femoral loading patterns in alligators appear to be derived in alligators rather than reflecting an ancestral semi-erect condition.

Ontogeny of the hyobranchial apparatus in the salamanders Ambystoma talpoideum (Ambystomatidae) and Notophthalmus viridescens (Salamandridae): The ecological morphology of two neotenic strategies.

Comparison of metamorphosis of skull and hyobranchial system in two species of neotenic salamanders reveals two different types of neoteny. Ambystoma talpoideum is completely neotenic owing to delayed metamorphosis. Notophthalmus viridescens exhibits limited neoteny as a result of incomplete metamorphosis. Morphological details of neoteny are compared to life history in both species in order to discuss the ecological morphology of the two neotenic strategies. Comparisons to Taricha granulosa, Triturus vulgaris, and Ambystoma gracile indicate that these two strategies are widely employed and may represent familial patterns.

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.

Atavisms and the homology of hyobranchial elements in lower vertebrates.

The homology of branchial arch segments in salamanders has been a matter of controversy since the last century. Many investigators term the most medial paired elements of salamander branchial arches "ceratobranchials" and the next distal paired elements "epibranchials." This suggests that the first two segmental elements of the salamander branchial arch are not homologous with elements occupying the same position in ray-finned fishes, Latimeria, "rhipidistians," and lungfishes, in which these bones are called hypobranchials and ceratobranchials, respectively. Three lines of evidence suggest that it is more parsimonious to interpret urodele branchial arch segments as being homologous with those of other vertebrate clades-(1) comparative osteology, (2) comparative myology, and (3) the discovery of cartilaginous structures forming a third segmental unit that we interpret as atavistic epibranchials of the branchial arch in one population of the salamander Notophthalmus viridescens. These structures possess all the defining attributes of atavisms, and illustrate the special role that atavistic features play in resolving questions of homology recognition.