Effects of food properties on chewing in pigs: Flexibility and stereotypy of jaw movements in a mammalian omnivore

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© 2020 Montuelle et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Chewing is a rhythmic oral behavior that requires constant modifications of jaw movements in response to changes in food properties. The food-specific kinematic response is dependent on the potential for kinematic flexibility allowed by morphology and modulation of motor control. This study investigates the effects of food toughness and stiffness on the amplitude and variability of jaw movements during chewing in a typical omnivorous mammalian model (pigs). Jaw movements were reconstructed using X-ray Reconstruction Of Moving Morphology (XROMM) and kinematic data associated with the amplitude of jaw pitch (opening-closing) and jaw yaw (mediolateral rotation) were extracted for each cycle. Between-food differences were tested for the amplitude of jaw movements during each phase of the gape cycle, as well as in their respective within-food variability, or stereotypy, as indicated by coefficients of variation. With increasing toughness, jaw pitch amplitude is decreased during fast close, larger and more stereotyped during slow close, smaller but more variable during slow open, and more variable during fast open. In addition, when chewing on tougher foods, the amplitude of jaw yaw during slow close only increases in a subset of individuals, but all become less variable (i.e., more stereotyped). In contrast, increasing food stiffness has no effect on the amplitude or the variability of jaw pitch, whereas jaw yaw increases significantly in the majority of individuals studied. Our data demonstrate that food stiffness and toughness both play a role in modulating gape cycle dynamics by altering the trajectory of jaw movements, especially during the slow-close phase and tooth-food-tooth contact, albeit differently. This highlights how a generalist oral morphology such as that of pigs (e.g., bunodont teeth lacking precise occlusion, permissive temporomandibular joint allowing extensive condylar displacements in 3 dimensions) enables organisms to not only adjust chewing movements in their amplitude, but also in their variability.