Reliable quantification of bite-force performance requires use of appropriate biting substrate and standardization of bite out-lever

Bite-force performance is an ecologically important measure of whole-organism performance that shapes dietary breadth and feeding strategies and, in some taxa, determines reproductive success. It also is a metric that is crucial to testing and evaluating biomechanical models. We reviewed nearly 100 published studies of a range of taxa that incorporate direct in vivo measurements of bite force. Problematically, methods of data collection and processing vary considerably among studies. In particular, there is little consensus on the appropriate substrate to use on the biting surface of force transducers. In addition, the bite out-lever, defined as the distance from the fulcrum (i.e. jaw joint) to the position along the jawline at which the jaws engage the transducer, is rarely taken into account. We examined the effect of bite substrate and bite out-lever on bite-force estimates in a diverse sample of lizards. Results indicate that both variables have a significant impact on the accuracy of measurements. Maximum bite force is significantly greater using leather as the biting substrate compared with a metal substrate. Less-forceful bites on metal are likely due to inhibitory feedback from mechanoreceptors that prevent damage to the feeding apparatus. Standardization of bite out-lever affected which trial produced maximum performance for a given individual. Indeed, maximum bite force is usually underestimated without standardization because it is expected to be greatest at the minimum out-lever (i.e. back of the jaws), which in studies is rarely targeted with success. We assert that future studies should use a pliable substrate, such as leather, and use appropriate standardization for bite out-lever.

[1]  M. Fagan,et al.  The Biomechanical Function of Periodontal Ligament Fibres in Orthodontic Tooth Movement , 2014, PloS one.

[2]  A. Lappin,et al.  Bite‐force performance of the last rhynchocephalian (Lepidosauria: Sphenodon) , 2009 .

[3]  D. Irschick,et al.  An analysis of the relative roles of plasticity and natural selection in the morphology and performance of a lizard (Urosaurus ornatus) , 2007, Oecologia.

[4]  E. Kalko,et al.  All You Can Eat: High Performance Capacity and Plasticity in the Common Big-Eared Bat, Micronycteris microtis (Chiroptera: Phyllostomidae) , 2011, PloS one.

[5]  F. Hertel,et al.  In vivo bite and grip forces, morphology and prey-killing behavior of North American accipiters (Accipitridae) and falcons (Falconidae) , 2010, Journal of Experimental Biology.

[6]  P. Fitze,et al.  An ecomorphological analysis of the determinants of mating success , 2013 .

[7]  A. Herrel,et al.  Scaling of morphology, bite force, and feeding kinematics in an iguanian and a sclerosglossan lizard , 2002 .

[8]  D. Irschick,et al.  The Evolution of Performance‐Based Male Fighting Ability in Caribbean Anolis Lizards , 2007, The American Naturalist.

[9]  Neil Curtis,et al.  The importance of accurate muscle modelling for biomechanical analyses: a case study with a lizard skull , 2013, Journal of The Royal Society Interface.

[10]  Patricia W. Freeman,et al.  Measuring Bite Force in Small Mammals with a Piezo-resistive Sensor , 2008 .

[11]  P. O’Higgins,et al.  Hard tissue anatomy of the cranial joints in Sphenodon (Rhynchocephalia): sutures, kinesis, and skull mechanics , 2011 .

[12]  K. Tolley,et al.  Morphology, ornaments and performance in two chameleon ecomorphs: is the casque bigger than the bite? , 2009, Zoology.

[13]  Melissa L. Wynn,et al.  Sex-specific trade-offs and compensatory mechanisms: bite force and sprint speed pose conflicting demands on the design of geckos (Hemidactylus frenatus) , 2013, Journal of Experimental Biology.

[14]  A. Herrel,et al.  Does dewlap size predict male bite performance in Jamaican Anolis lizards , 2005 .

[15]  Richard F. Martin,et al.  Physiological properties of intradental mechanoreceptors , 1985, Brain Research.

[16]  A. Herrel,et al.  Evolution of bite performance in turtles , 2002 .

[17]  V. H. Hutchison,et al.  LIGHT VERSUS HEAT: THERMOREGULATORY BEHAVIOR IN A NOCTURNAL LIZARD (GEKKO GECKO) , 1988 .

[18]  P. Aerts,et al.  The functional significance of the lower temporal bar in Sphenodon punctatus , 2008, Journal of Experimental Biology.

[19]  A. Herrel,et al.  Performance capacity, fighting tactics and the evolution of life–stage male morphs in the green anole lizard (Anolis carolinensis) , 2004, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[20]  G. Ortí,et al.  Mega-Bites: Extreme jaw forces of living and extinct piranhas (Serrasalmidae) , 2012, Scientific Reports.

[21]  A. Casinos,et al.  Bite force and jaw biomechanics in the subterranean rodent Talas tuco-tuco (Ctenomys talarum) (Caviomorpha: Octodontoidea) , 2011 .

[22]  P. Gignac,et al.  Ontogenetic scaling of cranial morphology and bite-force generation in the loggerhead musk turtle , 2010 .

[23]  A. Herrel,et al.  Biting Performance in Teeth‐Digging African Mole‐Rats (Fukomys, Bathyergidae, Rodentia)* , 2008, Physiological and Biochemical Zoology.

[24]  K. Holekamp,et al.  Ontogeny of feeding performance and biomechanics in coyotes , 2011 .

[25]  Susan E. Evans,et al.  Predicting muscle activation patterns from motion and anatomy: modelling the skull of Sphenodon (Diapsida: Rhynchocephalia) , 2010, Journal of The Royal Society Interface.

[26]  A. Herrel,et al.  Effects of testosterone on morphology, performance and muscle mass in a lizard. , 2010, Journal of experimental zoology. Part A, Ecological genetics and physiology.

[27]  J W Osborn,et al.  Effects on human maximum bite force of biting on a softer or harder object. , 1998, Archives of oral biology.

[28]  A. Herrel,et al.  Push and bite: trade-offs between burrowing and biting in a burrowing skink (Acontias percivali) , 2011 .

[29]  J. Mead,et al.  Early Pliocene Crotaphytus and Gambelia (Squamata: Crotaphytidae) from the Panaca Formation of Southeastern Nevada , 2006 .

[30]  J W Osborn,et al.  The effect of pressure on a maximum incisal bite force in man. , 1997, Archives of oral biology.

[31]  K. Fanson,et al.  Sex, androgens, and whole‐organism performance in an Australian lizard , 2014 .

[32]  P. Motta,et al.  Analysis of the bite force and mechanical design of the feeding mechanism of the durophagous horn shark Heterodontus francisci , 2005, Journal of Experimental Biology.

[33]  J. Kieser,et al.  Structure and compositional characteristics of caniniform dental enamel in the tuatara Sphenodon punctatus (Lepidosauria: Rhynchocephalia). , 2011, The New Zealand dental journal.

[34]  A. Herrel,et al.  Temperature effects on snapping performance in the common snapper Chelydra serpentina (Reptilia, Testudines). , 2011, Journal of experimental zoology. Part A, Ecological genetics and physiology.

[35]  R. Mark French,et al.  DESIGN VALIDATION AND TESTING OF WOLF BITE METER , 2005 .

[36]  A. Lappin,et al.  The fitness advantage of a high‐performance weapon , 2009 .

[37]  A. Herrel,et al.  Diet, morphology and performance in two chameleon morphs : do harder bites equate with harder prey? , 2011 .

[38]  M. Yamaguchi,et al.  Mechanoreceptors, Nociceptors, and Orthodontic Tooth Movement , 2012 .

[39]  Jonathan B. Losos,et al.  Ecomorphology, Performance Capability, and Scaling of West Indian Anolis Lizards: An Evolutionary Analysis , 1990 .

[40]  P. Aerts,et al.  Built to bite: feeding kinematics, bite forces, and head shape of a specialized durophagous lizard, Dracaena guianensis (teiidae). , 2012, Journal of experimental zoology. Part A, Ecological genetics and physiology.

[41]  E. Dumont,et al.  Connecting behaviour and performance: the evolution of biting behaviour and bite performance in bats , 2009, Journal of evolutionary biology.

[42]  Kathleen K. Smith Mechanical significance of streptostyly in lizards , 1980, Nature.

[43]  A. Herrel,et al.  Functional basis for sexual differences in bite force in the lizard Anolis carolinensis , 2007 .

[44]  S. Goldstein,et al.  Elastic modulus and hardness of cortical and trabecular bone lamellae measured by nanoindentation in the human femur. , 1999, Journal of biomechanics.

[45]  A. Herrel,et al.  Parentage analyses suggest female promiscuity and a disadvantage for athletic males in the colour-polymorphic lizard Podarcis melisellensis , 2014, Behavioral Ecology and Sociobiology.

[46]  A. Lappin,et al.  A comparative analysis of ontogenetic bite‐force scaling among Crocodylia , 2014 .

[47]  D. Kemp,et al.  Gaping Displays Reveal and Amplify a Mechanically Based Index of Weapon Performance , 2006, The American Naturalist.

[48]  Natasha I. Bloch,et al.  Are morphology-performance relationships invariant across different seasons? A test with the green anole lizard (**Anolis carolinensis**) , 2006 .

[49]  Simple predictors of bite force in bats: the good, the better and the better still , 2010 .

[50]  J. Husak,et al.  Bite-Force Performance Predicts Dominance in Male Venerable Collared Lizards (Crotaphytus antiquus) , 2006, Copeia.

[51]  A. Herrel,et al.  Insularity affects head morphology, bite force and diet in a Mediterranean lizard , 2014 .

[52]  D. Sustaita,et al.  The anatomy of a shrike bite: bill shape and bite performance in Loggerhead Shrikes , 2014 .

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

[54]  Justin P. Henningsen,et al.  An experimental test of the effect of signal size and performance capacity on dominance in the green anole lizard , 2012 .

[55]  A. Herrel,et al.  Ecomorphological analysis of trophic niche partitioning in a tropical savannah bat community , 2002, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[56]  Relationships between head morphology, bite performance and ecology in two species of Podarcis wall lizards , 2012, Evolutionary Ecology.

[57]  D. Irschick,et al.  No Evidence for Female Association with High-Performance males in the Green Anole Lizard, Anolis carolinensis , 2006 .

[58]  Anthony Herrel,et al.  The effects of gape angle and bite point on bite force in bats , 2003, Journal of Experimental Biology.

[59]  A. Herrel,et al.  Relationships between head size, bite force, prey handling efficiency and diet in two sympatric lacertid lizards , 2002 .

[60]  Anthony Herrel,et al.  Sexual dimorphism of head size in Gallotia galloti: testing the niche divergence hypothesis by functional analyses , 1999 .

[61]  P O'Higgins,et al.  Comparison between in vivo and theoretical bite performance: using multi-body modelling to predict muscle and bite forces in a reptile skull. , 2010, Journal of biomechanics.

[62]  A. Herrel,et al.  A biomechanical analysis of intra- and interspecific scaling of jumping and morphology in Caribbean Anolis lizards , 2003, Journal of Experimental Biology.

[63]  Anthony Herrel,et al.  Aggressive Behavior and Performance in the Tegu Lizard Tupinambis merianae , 2009, Physiological and Biochemical Zoology.

[64]  E. Brainerd,et al.  Bite force is limited by the force–length relationship of skeletal muscle in black carp, Mylopharyngodon piceus , 2013, Biology Letters.

[65]  R. German,et al.  Ontogeny of feeding function in the gray short-tailed opossum Monodelphis domestica: empirical support for the constrained model of jaw biomechanics , 2003, Journal of Experimental Biology.

[66]  R Phillips,et al.  Masticatory loading and bone adaptation in the supraorbital torus of developing macaques. , 2009, American journal of physical anthropology.

[67]  R. Orchardson,et al.  The effect of local periodontal anaesthesia on the maximum biting force achieved by human subjects. , 1980, Archives of oral biology.

[68]  Lance D. McBrayer,et al.  Bite force in vertebrates: opportunities and caveats for use of a nonpareil whole-animal performance measure , 2008 .

[69]  J. Kieser,et al.  Microstructure of dental hard tissues and bone in the Tuatara dentary, Sphenodon punctatus (Diapsida: Lepidosauria: Rhynchocephalia). , 2009, Frontiers of oral biology.

[70]  R McN Alexander,et al.  Modelling approaches in biomechanics. , 2003, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[71]  J. Losos,et al.  Cautionary comments on the measurement of maximum locomotor capabilities , 2002 .

[72]  M. Angilletta,et al.  Temperature preference in geckos: Diel variation in juveniles and adults , 1999 .

[73]  A. Herrel,et al.  Bite performance and morphology in a population of Darwin's finches: implications for the evolution of beak shape , 2005 .

[74]  A. Lappin,et al.  Comparison of bite‐force performance between long‐term captive and wild American alligators (Alligator mississippiensis) , 2004 .

[75]  Lance D. McBrayer,et al.  Bite Force, Behavior, and Electromyography in the Teiid Lizard, Tupinambis teguixin , 2002, Copeia.

[76]  D. Rödder,et al.  Living on the edge? – On the thermobiology and activity pattern of the large herbivorous desert lizard Uromastyx aegyptia microlepis Blanford, 1875 at Mahazat as-Sayd Protected Area, Saudi Arabia , 2011 .

[77]  A. Casinos,et al.  Biting performance and skull biomechanics of a chisel tooth digging rodent (Ctenomys tuconax; Caviomorpha; Octodontoidea). , 2013, Journal of experimental zoology. Part A, Ecological genetics and physiology.

[78]  A. Manns,et al.  Bite force measurements with hard and soft bite surfaces. , 2013, Journal of oral rehabilitation.

[79]  B. Kingsbury Thermoregulatory Set Points of the Eurythermic Lizard Elgaria multicarinata , 1993 .

[80]  Jerry F Husak,et al.  Weapon Performance, Not Size, Determines Mating Success and Potential Reproductive Output in the Collared Lizard (Crotaphytus collaris) , 2005, The American Naturalist.

[81]  B. Valkenburgh,et al.  Development of bite strength and feeding behaviour in juvenile spotted hyenas (Crocuta crocuta) , 2000 .

[82]  P. Gignac,et al.  Ontogenetic changes in jaw-muscle architecture facilitate durophagy in the turtle Sternotherus minor , 2011, Journal of Experimental Biology.

[83]  L. McBrayer,et al.  The relationship between skull morphology, biting performance and foraging mode in Kalahari lacertid lizards , 2004 .

[84]  P. Motta,et al.  Bite force and performance in the durophagous bonnethead shark, Sphyrna tiburo. , 2009, Journal of experimental zoology. Part A, Ecological genetics and physiology.

[85]  M. V. D. van der Meij,et al.  Seed husking time and maximal bite force in finches , 2006, Journal of Experimental Biology.

[86]  A. Hannam The response of periodontal mechanoreceptors in the dog to controlled loading of the teeth. , 1969, Archives of oral biology.

[87]  P. O’Higgins,et al.  Feedback control from the jaw joints during biting: an investigation of the reptile Sphenodon using multibody modelling. , 2010, Journal of biomechanics.

[88]  A. Herrel,et al.  Rotational feeding in caecilians: putting a spin on the evolution of cranial design , 2006, Biology Letters.

[89]  R. A. Anderson,et al.  Sexual Size Dimorphisms and Bite Force in The Northern Alligator Lizard, Elgaria Coerulea , 2007 .

[90]  R. Hackert,et al.  Proximate determinants of bite force capacity in the mouse lemur , 2013 .

[91]  M. V. D. van der Meij,et al.  Scaling of jaw muscle size and maximal bite force in finches , 2004, Journal of Experimental Biology.

[92]  Julian L. Davis,et al.  Mechanics of bite force production and its relationship to diet in bats , 2010 .

[93]  R. Jacobs,et al.  Comparison between implant-supported prostheses and teeth regarding passive threshold level. , 1993, The International journal of oral & maxillofacial implants.

[94]  Laura B. Porro,et al.  In vivo cranial bone strain and bite force in the agamid lizard Uromastyx geyri , 2014, Journal of Experimental Biology.

[95]  S. Wroe,et al.  The Effects of Biting and Pulling on the Forces Generated during Feeding in the Komodo Dragon (Varanus komodoensis) , 2011, PloS one.

[96]  X. Ji,et al.  Selected body temperature, thermal tolerance and thermal dependence of food assimilation and locomotor performance in adult blue-tailed skinks, Eumeces elegans , 2000 .

[97]  N. Ananjeva,et al.  Characteristics of dentition in gekkonid lizards of the genus Teratoscincus and other Gekkota (Sauria, Reptilia) , 2009, Biology Bulletin.

[98]  Katsufumi Sato,et al.  The ontogenetic scaling of bite force and head size in loggerhead sea turtles (Caretta caretta): implications for durophagy in neritic, benthic habitats , 2012, Journal of Experimental Biology.

[99]  A. Herrel,et al.  It is all in the head : morphological basis for differences in bite force among colour morphs of the Dalmatian wall lizard , 2008 .

[100]  A. Lappin,et al.  Bite-force performance and head shape in a sexually dimorphic crevice-dwelling lizard, the common chuckwalla [Sauromalus ater (= obesus)] , 2006 .

[101]  A. Herrel,et al.  Cranial morphology and bite force in Chamaeleolis lizards--adaptations to molluscivory? , 2008, Zoology.

[102]  B. Siemers,et al.  An integrative approach to detect subtle trophic niche differentiation in the sympatric trawling bat species Myotis dasycneme and Myotis daubentonii , 2014, Molecular ecology.

[103]  A. Herrel,et al.  Sex-specific evolution of bite performance in Liolaemus lizards (Iguania: Liolaemidae): the battle of the sexes , 2010 .

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

[105]  D. Dessem,et al.  Jaw‐muscle activity in ferrets, Mustela putorius furo , 1992, Journal of morphology.

[106]  E. Chudler,et al.  Static and dynamic responses of periodontal ligament mechanoreceptors and intradental mechanoreceptors. , 1993, Journal of neurophysiology.

[107]  A. Lappin,et al.  The ontogeny of bite-force performance in American alligator (Alligator mississippiensis) , 2003 .

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

[109]  A. Herrel,et al.  Microhabitat use, diet, and performance data on the Hispaniolan twig anole, Anolis sheplani: pushing the boundaries of morphospace. , 2007, Zoology.

[110]  A. Herrel,et al.  Impact of temperature on performance in two species of South African dwarf chameleon, Bradypodion pumilum and B. occidentale , 2013, Journal of Experimental Biology.