Chewing or not? Intraoral food processing in a salamandrid newt

Abstract

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.

Ontogenetic plasticity in cranial morphology is associated with a change in the food processing behavior in Alpine newts

“…2B). This secondary tongue protractor complex allows the tip of the tongue to be ejected out of the mouth which has been described for post-metamorphic salamandrids [33] and in turn is the functional basis for tongue-palate rasping [21]. Our data suggest that aquatic salamandrid larvae begin to use their tongue for processing ( Fig.…”

“…As a result, the tongue is likely to lose the ability to forcefully press a food against the palatal dentition, possibly reducing the effectiveness of tongue-palate rasping. It had been hypothesized that the coordination between hyolingual motion and depression of the skull may aid food processing e cacy in post-metamorphic salamandrids [21]. Coordinated head and hyolingual movement patterns also appear in post-metamorphic Alpine newts (Fig.…”

“…It was recently shown that metamorphosed salamandrid newts use loop-like movements of their hyobranchial apparatus (i.e., tongue) to translate food across the palatal dentition (i.e., tongue-palate rasping) [21]. It has also been suggested that salamandrids with a larval morphology cannot employ the same processing mechanism as metamorphic animals because of morphological constraints, including the lack of a exible tongue with su cient internal movement-potential and diverging dentition patterns in larval morphotypes [15,16].…”

“…However, further observations showed that the LLM chewed its food because the prey occasionally protruded from the mouth and therefore made clear how the jaws act upon the prey (Video 4). We could distinguish the post-ingestion behavior (i.e., jaw and hyobranchial movements) into prey transport (characterized by hyobranchial depression during gape opening [17-19]) and rhythmic food processing (characterized by hyobranchial elevation throughout or during some of the gape opening cycle [21,23]). Food-processing kinematics in the LLM involved the highest mean gapeclosure acceleration (Fig.…”

“…Food processing in salamanders involves a mix of structural and functional traits seen in shes and amniotes [21]. Salamanders, being lissamphibians, are especially interesting from an evolutionary point of view because of their phylogenetic position near the base of the tetrapod radiation, with lissamphibians being considered the extant sister-group of amniotes.…”