Do salamanders chew? An X-ray reconstruction of moving morphology analysis of ambystomatid intraoral feeding behaviours.

Chewing is widespread across vertebrates, including mammals, lepidosaurs, and ray-finned and cartilaginous fishes, yet common wisdom about one group-amphibians-is that they swallow food whole, without processing. Earlier salamander studies lacked analyses of internal kinematics of the tongue, analyses of muscle function, and sampled few individuals, which may have caused erroneous conclusions. Specifically, without tongue and food kinematics, intraoral behaviours are difficult to disambiguate. We hypothesized that ambystomatid salamanders use diverse intraoral behaviours, including chewing, and tested this hypothesis with biplanar videofluoroscopy, X-ray reconstruction of moving morphology, and fluoromicrometry. We generated musculoskeletal kinematic profiles for intraoral behaviours in Axolotls (Ambystoma mexicanum), including three-dimensional skeletal kinematics associated with feeding, for gape, cranial and pectoral girdle rotations, and tongue translations. We also measured muscle fibre and muscle-tendon unit strains for six muscles involved in generating skull, jaw and tongue kinematics (adductor mandibulae, depressor mandibulae, geniohyoid, sternohyoid, epaxialis and hypaxialis). A principal component analysis recovered statistically significant differences between behaviour cycles, classified based on food movements as either chewing or transport. Thus, our data suggest that ambystomatid salamanders use a previously unrecognized diversity of intraoral behaviours, including chewing. Combined with existing knowledge, our data suggest that chewing is a basal trait for tetrapods and jaw-bearing vertebrates. This article is part of the theme issue 'Food processing and nutritional assimilation in animals'.

Rhythmic chew cycles with distinct fast and slow phases are ancestral to gnathostomes.

Intra-oral food processing, including chewing, is important for safe swallowing and efficient nutrient assimilation across tetrapods. Gape cycles in tetrapod chewing consist of four phases (fast open and -close, and slow open and -close), with processing mainly occurring during slow close. Basal aquatic-feeding vertebrates also process food intraorally, but whether their chew cycles are partitioned into distinct phases, and how rhythmic their chewing is, remains unknown. Here, we show that chew cycles from sharks to salamanders are as rhythmic as those of mammals, and consist of at least three, and often four phases, with phase distinction occasionally lacking during jaw opening. In fishes and aquatic-feeding salamanders, fast open has the most variable duration, more closely resembling mammals than basal amniotes (lepidosaurs). Across ontogenetically or behaviourally mediated terrestrialization, salamanders show a distinct pattern of the second closing phase (near-contact) being faster than the first, with no clear pattern in partitioning of variability across phases. Our results suggest that distinct fast and slow chew cycle phases are ancestral for jawed vertebrates, followed by a complicated evolutionary history of cycle phase durations and jaw velocities across fishes, basal tetrapods and mammals. These results raise new questions about the mechanical and sensorimotor underpinnings of vertebrate food processing. This article is part of the theme issue 'Food processing and nutritional assimilation in animals'.

Thermal Sensitivity of Axolotl Feeding Behaviors.

Musculoskeletal movement results from muscle contractions, recoil of elastic tendons, aponeuroses, and ligaments, or combinations thereof. Muscular and elastic contributions can vary both across behaviors and with changes in temperature. Skeletal muscles reach peak contraction speed at a temperature optimum with performance declining away from that optimum by approximately 50% per 10°C, following the Q10 principle. Elastic recoil action, however, is less temperature sensitive. We subjected Axolotls (Ambystoma mexicanum) to changes from warm (23°C), via medium (14°C), to cold (6°C) temperature across most of their thermal tolerance range, and recorded jaw kinematics during feeding on crickets. We sought to determine if suction feeding strikes and food processing chews involve elastic mechanisms and, specifically, if muscular versus elastic contribution vary with temperature for gape opening and closing. Measurements of peak and mean speed for gape opening and closing during strikes and chews across temperature treatments were compared with Q10-based predictions. We found that strike gape speed decreased significantly from warm and medium to cold treatments, indicating low thermal robustness, and no performance-enhancement due to elastic recoil. For chews, peak, and mean gape closing speeds, as well as peak gape opening speed, also decreased significantly from warm to cold treatments. However, peak gape opening and closing speeds for chews showed performance-enhancement, consistent with a previously demonstrated presence of elastic action in the Axolotl jaw system. Our results add to a relatively small body of evidence suggesting that elastic recoil plays significant roles in aquatic vertebrate feeding systems, and in cyclic food processing mechanisms.