Why ruminating ungulates chew sloppily: Biomechanics discern a phylogenetic pattern

• Published in: PloS one Vol. 14; no. 4; p. e0214510
• Main Authors: Zhou, Zupeng, Winkler, Daniela E, Fortuny, Josep, Kaiser, Thomas M, Marcé-Nogué, Jordi
• Format: Journal Article
• Language: English
• Published: United States Public Library of Science 17.04.2019; Public Library of Science (PLoS)
• Subjects: Adaptation; Analysis; Animals; Artiodactyla; Artiodactyla - anatomy & histology; Biology and Life Sciences; Biomechanical engineering; Biomechanical Phenomena; Biomechanics; Bite Force; Biting; Buffalo; Camelids; Ceratotherium simum; Chewing; Cluster Analysis; Comminution; Computer and Information Sciences; Diet; Disintegration; Endangered & extinct species; Evolution, Molecular; Female; Fermenters; Finite Element Analysis; Finite element method; Food; Force; Hindgut; Imaging, Three-Dimensional; Ingestion; Jaw; Male; Mandible; Mandible - physiology; Mastication; Mastication - physiology; Mechanical properties; Medicine and Health Sciences; Methods; Models, Anatomic; Morphology; Perissodactyla; Perissodactyla - anatomy & histology; Phylogenetics; Phylogeny; Physical Sciences; Reproducibility of Results; Reptiles & amphibians; Research and Analysis Methods; Rhinoceroses; Ruminants - physiology; Rumination; Species Specificity; Stress; Stress concentration; Taxa; Three dimensional analysis; Ungulates; Values; Germany; Spain
• ISSN: 1932-6203; 1932-6203
• DOI: 10.1371/journal.pone.0214510

There is considerable debate regarding whether mandibular morphology in ungulates primarily reflects phylogenetic affinities or adaptation to specific diet. In an effort to help resolve this debate, we use three-dimensional finite element analysis (FEA) to assess the biomechanical performance of mandibles in eleven ungulate taxa with well-established but distinct dietary preferences. We found notable differences in the magnitude and the distribution of von Mises stress between Artiodactyla and Perissodactyla, with the latter displaying lower overall stress values. Additionally, within the order Artiodactyla the suborders Ruminantia and Tylopoda showed further distinctive stress patterns. Our data suggest that a strong phylogenetic signal can be detected in biomechanical performance of the ungulate mandible. In general, Perissodactyla have stiffer mandibles than Artiodactyla. This difference is more evident between Perissodactyla and ruminant species. Perissodactyla likely rely more heavily on thoroughly chewing their food upon initial ingestion, which demands higher bite forces and greater stress resistance, while ruminants shift comminution to a later state (rumination) where less mechanical effort is required by the jaw to obtain sufficient disintegration. We therefore suggest that ruminants can afford to chew sloppily regardless of ingesta, while hindgut fermenters cannot. Additionally, our data support a secondary degree of adaptation towards specific diet. We find that mandibular morphologies reflect the masticatory demands of specific ingesta within the orders Artiodactyla and Perissodactyla. Of particular note, stress patterns in the white rhinoceros (C. simum) look more like those of a general grazer than like other rhinoceros' taxa. Similarly, the camelids (Tylopoda) appear to occupy an intermediate position in the stress patterns, which reflects the more ancestral ruminating system of the Tylopoda.