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Food processing refers to any form of mechanical breakdown of food prior to swallowing. Variations of this behaviour are found within all major gnathostome groups. Chewing is by far the most commonly used intraoral processing mechanism and involves rhythmic mandibular jaw and hyobranchial (tongue) movements. Chewing occurs in chondrichthyans (sharks and rays), actinopterygians (rayfinned fishes), dipnoi (lungfishes) as well as amniotes and involves similarities in the patterns of muscle activity and movement of the feeding apparatus. It has been suggested that amniote chewing, which involves the interaction of movements of the mandibular jaw and the muscular tongue, has evolved as part of the tetrapod land invasion. However, little is known about food-processing mechanisms in lissamphibians, which might have retained many ancestral tetrapod features. Here, we identified a processing mechanism in the salamandrid newt, Triturus carnifex, which after prey capture displays cyclic head bobbing in concert with rhythmic jaw and tongue movements. We used high-speed fluoroscopy, anatomical reconstructions and analyses of stomach contents to show that newts, although not using their mandibular jaws, deploy a derived processing mechanism where prey items are rasped rhythmically against the dentition on the mouth roof, driven by a loop motion of the tongue. We then compared patterns and coordination of jaw and tongue movements across gnathostomes to conclude that food processing in this newt species shares traits with processing mechanisms in fish as well as amniotes. This discovery casts salamanders as promising models for reconstructing the evolution of intraoral processing mechanisms at the fish-tetrapod split.

It is generally accepted that most non-mammal tetrapods have a hinge-like jaw operation restricted to vertical opening and closing movements. Many mammal jaw joints, by contrast, operate in more complex, three-dimensional ways, involving not only vertical, but also propalinal (rostro-caudal) and transverse (lateral) movements. Data on intraoral food processing in lissamphibians and sauropsids has prompted a generally accepted view that these groups mostly swallow food unreduced, and that in those cases where lissamphibians and sauropsids chew, they mostly use simple vertical jaw movements for food processing. The exception to that generally accepted view being some propalinal chewing in sauropsids. We combined 3D kinematics and morphological analyses from biplanar high-speed video fluoroscopy and micro-CT to determine how the paedomorphic salamander Siren intermedia treats captured food. We discovered that S. intermedia not only uses intraoral food processing, but that the elaborated morphology of its jaw joint facilitates mandibular motions in all three planes, resulting in complex three-dimensional chewing. Thus, our data challenge the commonly held view that complex three-dimensional chewing movements are exclusive to mammals, by suggesting that complex chewing mechanisms might evolved early in tetrapod evolution.

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Background The feeding apparatus of salamanders consists mainly of the cranium, mandible, teeth, hyobranchial apparatus and the muscles of the cranial region. The morphology of the feeding apparatus in turn determines the boundary conditions for possible food processing (i.e., intraoral mechanical reduction) mechanisms. However, the morphology of the feeding apparatus changes substantially during metamorphosis, prompting the hypothesis that larvae might use a different food processing mechanism than post-metamorphic adults. Salamandrid newts with facultative metamorphosis are suitable for testing this hypothesis as adults with divergent feeding apparatus morphologies often coexist in the same population, share similar body sizes, and feed on overlapping prey spectra. Methods We use high-speed videography to quantify the in vivo movements of key anatomical elements during food processing in paedomorphic and metamorphic Alpine newts (Ichthyosaura alpestris). Additionally, we use micro-computed tomography (μCT) to analyze morphological differences in the feeding apparatus of paedomorphic and metamorphic Alpine newts and sort them into late-larval, mid-metamorphic and post-metamorphic morphotypes. Results Late-larval, mid-metamorphic and post-metamorphic individuals exhibited clear morphological differences in their feeding apparatus. Regardless of the paedomorphic state being externally evident, paedomorphic specimens can conceal different morphotypes (i.e., late-larval and mid-metamorphic morphotypes). Though feeding on the same prey under the same (aquatic) condition, food processing kinematics differed between late-larval, mid-metamorphic and post-metamorphic morphotypes. Conclusions The food processing mechanism in the Alpine newt changes along with morphology of the feeding apparatus during ontogeny, from a mandible-based to a tongue-based processing mechanism as the changing morphology of the mandible prevents chewing and the tongue allows enhanced protraction. These results could indicate that early tetrapods, in analogy to salamanders, may have developed new feeding mechanisms in their aquatic environment and that these functional innovations may have later paved the way for terrestrial feeding mechanisms.