The impact of gape on the performance of the skull in chisel-tooth digging and scratch digging mole-rats (Rodentia: Bathyergidae)

Abstract

The African mole-rats (Bathyergidae) are a family of rodents highly adapted for life underground. Previous research has shown that chisel-tooth digging mole-rats (which use their incisors to dig burrows) are clearly distinguishable from scratch diggers (which only use the forelimbs to tunnel) on the basis of morphology of the skull, and that the differences are linked to the production of high bite forces and wide gapes. We hypothesized that the skull of a chisel-tooth digging mole-rat would perform better at wider gapes than that of a scratch digging mole-rat during incisor biting. To test this hypothesis, we created finite-element models of the cranium of the scratch digging Bathyergus suillus and the chisel-tooth digging Fukomys mechowii, and loaded them to simulate incisor bites at different gapes. Muscle loads were scaled such that the ratio of force to surface area was the same in both models. We measured three performance variables: overall stress across the cranium, mechanical efficiency of biting and degree of deformation across the skull. The Fukomys model had a more efficient incisor bite at all gapes, despite having greater average stress across the skull. In addition, the Fukomys model deformed less at wider gapes, whereas the Bathyergus model deformed less at narrower gapes. These properties of the cranial morphology of Fukomys and Bathyergus are congruent with their respective chisel-tooth and scratch digging behaviours and, all other factors being equal, would enable the more efficient production of bite force at wider gapes in Fukomys. However, in vivo measurements of muscle forces and activation patterns are needed to fully understand the complex biomechanics of tooth digging.

Kinematics of chisel-tooth digging by African mole-rats

“…For example, the mean gape angle of Fukomys during digging from the current study has already been used in a study of the mechanical advantages of the jaw adductor muscles of bathyergid rodents (McIntosh and Cox, 2016b). A recent computational modelling study compared the performance of the cranium of a tooth-digging bathyergid species with that of a scratchdigging species during biting (McIntosh and Cox, 2016a). This type of study could be further optimized to better represent a case of digging based on the presented data.…”

“…The latter behaviour is referred to as chisel-tooth digging. It has evolved independently at least once in each of the six extant families of subterranean and fossorial rodents (Stein, 2000;McIntosh and Cox, 2016a). However, due to the technical difficulties with capture, keeping, breeding and monitoring their behaviour (Begall et al, 2007), relatively little is known about the functional morphology and biomechanics of digging in these underground dwellers.…”

The jaw is a second-class lever inPedetes capensis(Rodentia: Pedetidae)

“…The distribution of maximum (ε 1 : predominantly tensile) and minimum (ε 3 : predominantly compressive) principal strains across the skull were examined using contour maps. Geometric morphometric methods were used to analyse deformation patterns across the skull (Cox et al, 2011; Cox, Kirkham & Herrel, 2013; O’Higgins et al, 2011; McIntosh & Cox, 2016). A set of 46 3D landmark co-ordinates (described in Fig.…”

“…To address the hypotheses and to study the function of the springhare skull during biting, finite element analysis (FEA) will be employed. FEA is an engineering technique for predicting stress, strain and deformation in an object during loading (Rayfield, 2007), and is now frequently applied to reconstructions of skulls and other skeletal elements in order to analyse vertebrate biomechanics (e.g., Richmond et al, 2005; Kupczik et al, 2007; Dumont et al, 2011; Ross et al, 2011; Cox et al, 2012; Cox, Kirkham & Herrel, 2013; O’Hare et al, 2013; Porro et al, 2013; Figueirido et al, 2014; Cuff, Bright & Rayfield, 2015; Sharp, 2015; McIntosh & Cox, 2016; McCabe et al, 2017; Tsouknidas et al, 2017). As well as simulating stress and strain distributions, FEA is also able to predict reaction forces, and so will be used here to estimate bite force, jaw joint reaction force and mechanical advantage.…”

In vivo bone strain and finite element modeling of a rhesus macaque mandible during mastication

“…Hypothesized associations between loading regimes, internal stress regimes, and shapes of biological structures are commonly evaluated using either simple beam models (e.g., Preuschoft et al, 1983; Hylander, 1984, 1985; Daegling, 1993, 2001; Hylander and Johnson, 1994; Ravosa, 1996, 2000; Ross and Hylander, 1996; Hylander et al, 1998, 2000; Daegling and Hylander, 2000; Ravosa et al, 2000; Ross, 2001; Metzger et al, 2005; Daegling and McGraw, 2009) or, more recently, complex finite element models (FEMs) (e.g., Ross et al, 2005; Strait et al, 2005; Kupczik et al, 2009; Panagiotopoulou and Cobb, 2011; Porro et al, 2013; Prado et al, 2016; Janovic et al, 2014, 2015; Cox et al, 2011; Smith et al, 2015; Benazzi et al, 2016; Ledogar et al, 2016a; McIntosh and Cox, 2016; Panagiotopoulou et al, 2016a, b; Smith and Grosse, 2016). These modeling methods are especially important for testing hypotheses regarding form–function relationships (design) in skeletons of fossil animals for which in vivo data are not available (e.g., Rayfield et al, 2001; Strait et al, 2009; Berthaume et al, 2010; Grine et al, 2010; Falkingham et al, 2011a,b; Dzialo et al, 2014; Smith et al, 2015; Ledogar et al, 2016b).…”