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

Abstract

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’.