Chewed out: an experimental link between food material properties and repetitive loading of the masticatory apparatus in mammals

Abstract

Using a model organism (rabbits) that resembles a number of mammalian herbivores in key aspects of its chewing behaviors, we examined how variation in dietary mechanical properties affects food breakdown during mastication. Such data have implications for understanding phenotypic variation in the mammalian feeding apparatus, particularly with respect to linking jaw form to diet-induced repetitive loading. Results indicate that chewing frequency (chews/s) is independent of food properties, whereas chewing investment (chews/g) and chewing duration(s), which are proportional to repetitive loading of the jaws, are positively related to food stiffness and toughness. In comparisons of displacement-limited and stress-limited fragmentation indices, which respectively characterize the intraoral breakdown of tough and stiff foods, increases in chewing investment and duration are linked solely to stiffness. This suggests that stiffer foods engender higher peak loads and increased cyclical loading. Our findings challenge conventional wisdom by demonstrating that toughness does not, by itself, underlie increases in cyclical loading and loading duration. Instead, tough foods may be associated with such jaw-loading patterns because they must be processed in greater volumes owing to their lower nutritive quality and for longer periods of time to increase oral exposure to salivary chemicals.

Betwixt and Between: Intracranial Perspective on Zygomatic Arch Plasticity and Function in Mammals

“…Stiffness characterizes resistance to elastic deformation and is quantified via the stress/strain ratio at small deformations otherwise known as the elastic, or Young's, modulus (E); toughness is an energetic property describing the work performed to propagate a crack through an item. Indeed, rabbits use approximately three times more chewing cycles per unit food mass when processing hay vs. pellets (2.95 times more chews per g), which results in longer chewing durations averaging 3.22 times longer (Ravosa et al, ). The singular importance of cyclical loading for our analyses is further underscored by the similarity in mandibular peak‐strain levels during hay and pellet processing (Weijs and de Jongh, ).…”

Toughness of the Virunga mountain gorilla (Gorilla beringei beringei) diet across an altitudinal gradient

“…This, coupled with the observation that mountain gorillas spend 55% of their day feeding (Watts, ), suggests that the robust masticatory apparatus of gorillas may have evolved for repetitive mastication of foods that are not extremely high in toughness rather than for the production of high‐magnitude bite forces. Along these lines, Ravosa et al () argue that the relationship between food toughness and masticatory robusticity exists because tough foods require extensive oral processing resulting in repetitive loading of the jaws.…”

“…With the advent of microwear and isotopic analyses, however, dietary reconstructions have become more contentious as the results using different methodologies often do not yield the same dietary signal (e.g., Cerling et al, ; Smith et al, ; Ungar, Grine, & Teaford, ; Ungar & Sponheimer, ). Furthermore, while shape differences in the adult mandibular corpus have been linked to the mechanical demands of different diets (e.g., Bouvier & Hylander, ; Hylander, , ; Ravosa, ; Ravosa et al, ; Ross et al, ; Scott et al, ), comparative studies of primates do not support a consistent relationship between mandibular morphology and diet (Ross et al, ). Collecting data on specific feeding behaviors (e.g., whether items are prepared with any part of the dentition prior to mastication or disposal, the frequency of ingestion and preparation) for foods that vary in material properties is also necessary to gain a deeper understanding of dento‐gnathic adaptations to specific diets (McGraw et al, ; Ross et al, ).…”

“…The morphology of the masticatory system is often used to make inferences about dietary adaptations of fossil primate taxa (e.g., Bock & von Wahlert, ; Demes & Creel, ; Kay & Cartmill, ; Lucas, Constantino, & Wood, ; Robinson, , ; Smith et al, ; Strait et al, ; Teaford & Ungar, ; Ungar & Sponheimer, ). Specifically, the material properties of foods are thought to influence the morphology of the masticatory system such that animals that feed on mechanically challenging foods should possess robust jaws that can withstand high magnitude bite forces and/or prolonged loading (e.g., Bouvier & Hylander, ; Hylander, , ; Ravosa, Scott, McAbee, Veit, & Fling, ; Ravosa, Vinyard, Gagnon, & Islam, ; Ross et al, ; Scott, McAbee, Eastman, & Ravosa, ; Taylor, ; Taylor, Vogel, & Dominy, ; Vogel et al, ). Many studies have reported on the material properties of primate foods (e.g., Coiner‐Collier et al, ; Dominy, Lucas, Osorio, & Yamashita, ; Dunham & Lambert, ; Elgart‐Berry, ; Hill & Lucas, ; Lucas, ; Teaford, Lucas, Ungar, & Glander, ; Venkataraman et al, ; Vogel et al, , ; Williams, Wright, Truong, Daubert, & Vinyard, ; Wright et al, ; Yamashita, ; Yamashita, Vinyard, & Tan, ), yet linking these data directly with masticatory morphology in a primate‐wide comparative context has proven difficult, largely due to the complex interactions among factors that produce adult masticatory morphology (e.g., feeding behavior, food mechanical and geometric properties, and loading regimes; Ross, Iriarte‐Diaz, & Nunn, ).…”

Ontogenetic and functional modularity in the rodent mandible

“…The material properties of food items are understood to influence jaw adductor activity, jaw kinematics, and feeding behaviors (Crompton, 1986;Weijs et al, 1989;Hylander et al, 1992Hylander et al, , 2000Hylander et al, , 2005. Increased jaw muscle activity associated with mechanically resistant food items results in elevated peak and cyclical strains in the craniomandibular skeleton (Weijs and de Jongh, 1977;Hylander, 1979Hylander, , 1988Hylander, , 1992Hylander et al, 1992;Herring and Teng, 2000;Ravosa et al, 2007Ravosa et al, , 2008bRavosa et al, , 2015 and, in turn, differential growth and remodeling of hard and soft tissues in the cranium and mandible (Beecher and Corruccini, 1981;Bouvier andHylander, 1981, 1996;Beecher et al, 1983;Bouvier and Zimny, 1987;Bouvier, 1988;Yamada and Kimmel, 1991;Kiliaridis et al, 1996;Nicholson et al, 2006;Ravosa et al, 2007Ravosa et al, , 2008bRavosa et al, , 2010Menegaz et al, 2009Menegaz et al, , 2010Scott et al, 2014a;Franks et al, 2016Franks et al, , 2017Ravosa et al, 2016).…”