Predicting bite force and cranial biomechanics in the largest fossil rodent using finite element analysis

Josephoartigasia monesi, from the Pliocene of Uruguay, is the largest known fossil rodent, with an estimated body mass of 1000 kg. In this study, finite element analysis was used to estimate the maximum bite force that J. monesi could generate at the incisors and the cheek teeth. Owing to uncertainty in the model inputs, a sensitivity study was conducted in which the muscle forces and orientations were sequentially altered. This enabled conclusions to be drawn on the function of some of the masticatory muscles. It was found that J. monesi had a bite of 1389 N at the incisors, rising to 4165 N at the third molar. Varying muscle forces by 20% and orientations by 10° around the medio‐lateral aspect led to an error in bite force of under 35% at each tooth. Predicted stresses across the skull were only minimally affected by changes to muscle forces and orientations, but revealed a reasonable safety factor in the strength of the skull. These results, combined with previous work, lead us to speculate that J. monesi was behaving in an elephant‐like manner, using its incisors like tusks, and processing tough vegetation with large bite forces at the cheek teeth.

[1]  I. R. Grosse,et al.  Predicting bite force in mammals: two-dimensional versus three-dimensional lever models , 2010, Journal of Experimental Biology.

[2]  A. Grandal-d’Anglade.  Bite force of the extinct Pleistocene Cave bear Ursus spelaeus Rosenmüller from Europe , 2010 .

[3]  Ian R Grosse,et al.  Finite-element analysis of biting behavior and bone stress in the facial skeletons of bats. , 2005, The anatomical record. Part A, Discoveries in molecular, cellular, and evolutionary biology.

[4]  A. Rinderknecht,et al.  The largest fossil rodent , 2008, Proceedings of the Royal Society B: Biological Sciences.

[5]  Patricia W. Freeman,et al.  A simple morphological predictor of bite force in rodents , 2008 .

[6]  Anthony Herrel,et al.  Masticatory biomechanics of the Laotian rock rat, Laonastes aenigmamus, and the function of the zygomaticomandibularis muscle , 2013, PeerJ.

[7]  Todd C. Pataky,et al.  Functional Evolution of the Feeding System in Rodents , 2012, PloS one.

[8]  F C van Ginkel,et al.  Comparison of Jaw-muscle Bite-force Cross-sections Obtained by Means of Magnetic Resonance Imaging and High-resolution CT Scanning , 1989, Journal of dental research.

[9]  Philip Clausen,et al.  Finite element analysis of ursid cranial mechanics and the prediction of feeding behaviour in the extinct giant Agriotherium africanum , 2012 .

[10]  J. Thomason,et al.  Cranial dimensions and forces of biting in the domestic dog , 2009, Journal of anatomy.

[11]  J. Downing,et al.  CRC Handbook of Mammalian Body Masses , 1995 .

[12]  E. Rayfield.  Finite Element Analysis and Understanding the Biomechanics and Evolution of Living and Fossil Organisms , 2007 .

[13]  N Jeffery,et al.  Finite element modelling of squirrel, guinea pig and rat skulls: using geometric morphometrics to assess sensitivity , 2011, Journal of anatomy.

[14]  L. Hautier,et al.  Masticatory muscle architecture in the Laotian rock rat Laonastes aenigmamus (Mammalia, Rodentia): new insights into the evolution of hystricognathy , 2009, Journal of anatomy.

[15]  Jia Liu,et al.  The application of muscle wrapping to voxel-based finite element models of skeletal structures , 2012, Biomechanics and modeling in mechanobiology.

[16]  A. Lappin,et al.  Insights into the Ecology and Evolutionary Success of Crocodilians Revealed through Bite-Force and Tooth-Pressure Experimentation , 2012, PloS one.

[17]  Stuart O. Landry,et al.  Turnbull, William D. Mammalian Masticatory apparatus. Fieldiana: Geol., 18:149–356, 1970 , 1971 .

[18]  V. Millien.  The largest among the smallest: the body mass of the giant rodent Josephoartigasia monesi , 2008, Proceedings of the Royal Society B: Biological Sciences.

[19]  W. Greaves,et al.  The jaw lever system in ungulates: a new model , 2009 .

[20]  Julian L. Davis,et al.  Finite element analysis of performance in the skulls of marmosets and tamarins , 2011, Journal of anatomy.

[21]  J. Thomason.  Cranial strength in relation to estimated biting forces in some mammals , 1991 .

[22]  K R Williams,et al.  Orthodontic tooth movement analysed by the Finite Element Method. , 1984, Biomaterials.

[23]  G. C. Gorniak.  Feeding in golden hamsters, Mesocricetus auratus , 1977, Journal of morphology.

[24]  Laura C Fitton,et al.  The Impact of Simplifications on the Performance of a Finite Element Model of a Macaca fascicularis Cranium , 2015, Anatomical record.

[25]  Weijs Wa.  MORPHOLOGY OF MUSCLES OF MASTICATION IN ALBINO-RAT, RATTUS-NORVEGICUS (BERKENHOUT, 1769) , 1973 .

[26]  L. Hautier.  Masticatory muscle architecture in the gundi Ctenodactylus vali (Mammalia, Rodentia) , 2010 .

[27]  W. Weijs.  Morphology of the muscles of mastication in the albino rat, Rattus norvegicus (Berkenhout, 1769). , 1973, Acta morphologica Neerlando-Scandinavica.

[28]  K. Bates,et al.  Estimating maximum bite performance in Tyrannosaurus rex using multi-body dynamics , 2012, Biology Letters.

[29]  A. Rinderknecht,et al.  The bite force of the largest fossil rodent (Hystricognathi, Caviomorpha, Dinomyidae) , 2012 .

[30]  C. Woods,et al.  Adaptive Radiation of Capromyid Rodents: Anatomy of the Masticatory Apparatus , 1979 .

[31]  C. Woods.  Comparative myology of jaw, hyoid, and pectoral appendicular regions of New and Old World hystricomorph rodents. Bulletin of the AMNH ; v. 147, article 3 , 1972 .

[32]  S. Wroe,et al.  Effects of Gape and Tooth Position on Bite Force and Skull Stress in the Dingo (Canis lupus dingo) Using a 3-Dimensional Finite Element Approach , 2008, PloS one.

[33]  K. Hiiemae.  The structure and function of the jaw muscles in the rat (Rattus norvegicus L.) , 1971 .

[34]  Michael Nies,et al.  Bite force measurement in awake rats. , 2004, Brain research. Brain research protocols.

[35]  A. E. Wood.  GRADES AND CLADES AMONG RODENTS , 1965 .

[36]  Philip G Cox,et al.  Reviewing the Morphology of the Jaw‐Closing Musculature in Squirrels, Rats, and Guinea Pigs with Contrast‐Enhanced MicroCt , 2011, Anatomical record.

[37]  R. Druzinsky.  Functional Anatomy of Incisal Biting in Aplodontia rufa and Sciuromorph Rodents – Part 2: Sciuromorphy Is Efficacious for Production of Force at the Incisors , 2010, Cells Tissues Organs.

[38]  S. Wroe,et al.  Bite forces and evolutionary adaptations to feeding ecology in carnivores. , 2007, Ecology.

[39]  Stephen Wroe,et al.  Supermodeled sabercat, predatory behavior in Smilodon fatalis revealed by high-resolution 3D computer simulation , 2007, Proceedings of the National Academy of Sciences.

[40]  Philip Clausen,et al.  Computer simulation of feeding behaviour in the thylacine and dingo as a novel test for convergence and niche overlap , 2007, Proceedings of the Royal Society B: Biological Sciences.

[41]  D T Davy,et al.  Anisotropic yield behavior of bone under combined axial force and torque. , 1985, Journal of biomechanics.

[42]  J. Hermanson,et al.  Myology of Hystricognath Rodents: An Analysis of Form, Function, and Phylogeny , 1985 .

[43]  Don E. Wilson,et al.  The Mammal Species of the World , 2009 .

[44]  S. Wroe,et al.  Bite club: comparative bite force in big biting mammals and the prediction of predatory behaviour in fossil taxa , 2005, Proceedings of the Royal Society B: Biological Sciences.

[45]  K. Byrd.  Mandibular movement and muscle activity during mastication in the guinea pig (Cavia porcellus) , 1981, Journal of morphology.