Spatial patterning of bone stiffness in the anterior mandibular corpus of Macaca fascicularis: Implications for models of bone adaptation

Abstract

Elastic modulus of bone from the anterior mandibular corpus was determined via microindentation in a mixed-sex ontogenetic sample (N = 14) of Macaca fascicularis. This investigation focused on the hypothesis that material heterogeneity in the macaque mandibular symphysis-provided an accounting of age and sex variation-is explicable as a means to homogenize strains in this region. Experimental data and theoretical models of masticatory loading indicate that in the absence of material compensation, large strain gradients exist in the anterior mandibular corpus of macaques, particularly between lingual and labial cortical plates owing to the effects of lateral transverse bending. Microindentation data indicate that juvenile macaques possess less stiff bone than their subadult and adult counterparts; however, sex differences in elastic modulus are not apparent. Anisotropy variation is idiosyncratic; that is, there is not a common pattern of variation in stiffness sampled among orthogonal planes across individuals. Similarly, differences in stiffness between lingual and labial cortical plates, as well as differences among alveolar, midcorpus, and basal regions are inconsistently observed. Consequently, we find little evidence in support of the hypothesis that spatial variation in bone stiffness functions to homogenize strains in the anterior corpus; in fact, in some individuals, this spatial variation serves to exacerbate, rather than to minimize, strain gradients. The mechanical benefit of elastic modulus variation in the macaque mandibular symphysis is unclear; this variation may not confer adaptive benefit in terms of structural integrity despite the fact that such variation has discernible functional consequences.

Biomechanical implications of cortical elastic properties of the macaque mandible

“…Our results show significant regional variations in elastic properties of the macaque mandible as has been found in the mandibles of other mammals (Dechow et al, 1992(Dechow et al, , 1993Dechow, 2002, 2003;Rapoff et al, 2008Rapoff et al, , 2017Daegling et al, 2009Daegling et al, , 2011aDaegling et al, ,b, 2014Daegling et al, , 2015Wang et al, 2010;Zapata et al, 2010;Lad et al, 2016;Le et al, 2016;Dechow, 2017). Of the parameters studied, cortical thickness, density, elastic moduli, shear moduli, and anisotropy exhibited distinct properties within and among regions.…”

“…This is evident from ultrasonic three-dimensional studies of elastic properties of cortical bone in mandibles of various species including humans (Dechow et al, 1993;Dechow, 2002b, 2003;Dechow, 2017), baboons (Wang et al, 2010), alligators (Zapata et al, 2010, and pigs (Dechow, 2017). Microindentation techniques that have also been used to determine elastic moduli of cortical bone from mandibles of several Old World and New World monkey species have demonstrated heterogeneity on a micro scale (; Rapoff et al, 2008Rapoff et al, , 2017Daegling et al, 2009Daegling et al, , 2011aDaegling et al, ,b, 2014Daegling et al, , 2015Lad et al, 2016;Le et al, 2016). Overall, studies of elastic properties suggest that variations in the different anatomical regions correspond to morphofunctional partitions and can show similarities between species with close phylogenetic relationships.…”

Spatial variation in mandibular bone elastic modulus and its effect on structural bending stiffness: A test case using the Taï Forest monkeys

“…There is no necessary mechanical benefit to material heterogeneity in the mandible if it is recognized that metabolic activity in bone will create material heterogeneity whether or not the activity was instigated by mechanical stimuli. For instance, the finding of material variation in the macaque mandibular symphysis did not necessarily support the idea that spatial variation functions to mitigate stress under wishboning loads (Daegling et al, ). Neither does the fact that there is no common pattern of heterogeneity among the species sampled signify an absence of benefit in terms of structural integrity.…”

“…Each indentation was referenced to a Cartesian coordinate system for calculation of structural mechanical properties (area moments of inertia) as well as spatial autocorrelation statistics (Moran's I) as developed below. Indentation protocol followed Daegling, Granatosky, et al (2011) and Daegling et al (). This study was approved by IACUC (approval number 201301261, valid through December 2016).…”

“…Bone is not homogeneous in material composition, and consideration of the heterogeneous distribution of material stiffness in bone will presumably lead to improved understanding of biomechanical performance. Existence of stiffness variation in mandibular bone is well established (e.g., Daegling, Granatosky, & McGraw, ; Daegling, Hotzman, McGraw, & Rapoff, ; Dechow & Hylander, ; Rapoff et al, ; Schwartz‐Dabney & Dechow, ; Wang et al, ). It is clear that the structural integrity of bone is influenced by its macrostructural properties (e.g., cortical thickness and trabecular density) and its microstructural properties (e.g., porosity, secondary bone distribution), such that an assumption of homogeneity yields an inaccurate assessment of structural stiffness (e.g., Augat & Schorlemmer, ; Bhatavadekar et al, ; Fratzl, Gupta, Fischer, & Kolednik, ; Harrison et al, ; Jaasma, Bayraktar, Niebur, & Keaveny, ; MacNeil & Boyd, ; Rapoff et al, ; Rho, Zioupos, Currey, & Pharr, ; Roy, Rho, Tsui, Evans, & Pharr, ; Sansalone et al, ; Wachter et al, ).…”