Gape drives regional variation in temporalis architectural dynamics in tufted capuchins

Abstract

Dynamic changes in jaw movements and bite forces depend on muscle architectural and neural factors that have rarely been compared within the same muscle. Here we investigate how regional muscle architecture dynamics—fascicle rotation, shortening, lengthening and architectural gear ratio (AGR)—vary during chewing across a functionally heterogeneous muscle. We evaluate whether timing in architecture dynamics relates to gape, food material properties and/or muscle activation. We also examine whether static estimates of temporalis fibre architecture track variation in dynamic architecture. Fascicle-level architecture dynamics were measured in three regions of the superficial temporalis of three adult tufted capuchins ( Sapajus apella ) using biplanar videoradiography and the XROMM workflow. Architecture dynamics data were paired with regional fine-wire electromyography data from four adult tufted capuchins. Gape accounted for most architectural change across the temporalis, but architectural dynamics varied between regions. Mechanically challenging foods were associated with lower AGRs in the anterior region. The timing of most dynamic architectural changes did not vary between regions and differed from regional variation in static architecture. Collectively these findings suggest that, when modelling temporalis muscle force production in extant and fossil primates, it is important to account for the effects of gape, regionalization and food material properties. This article is part of the theme issue ‘Food processing and nutritional assimilation in animals’.

Rhythmic chew cycles with distinct fast and slow phases are ancestral to gnathostomes

“…Fortunately, X-ray-based data on gape kinematics are rapidly becoming available from a swath of lepidosaurs and mammals (e.g. [69][70][71]), which will facilitate future velocity-based analyses of chew cycle partitioning into phases.…”

Energetic costs of feeding in 12 species of small-bodied primates

“…Alternatively for H3B 0 , if tough/stiff foods incur higher feeding costs compared to soft/elastic foods regardless of jaw-adductor mass, then we expect that foods with high FMPs will have intercepts that are elevated above those foods with lower FMPs. Alternatively for H4A 0 and H4B 0 , large diameter foods may incur higher feeding costs compared to smaller foods (due, for example, to the gape/bite force trade-off due to relatively poor muscle performance at larger gapes [8]). For H4A 0 , if large foods incur higher feeding costs than small foods and these costs increase as jaw-adductor mass increases, then large diameter foods will have higher slopes than small diameter foods.…”

“…Understanding the role of energetic costs in the feeding system is important for relating selective pressures to morphology and behaviour and facilitates broader comparisons between biomechanical systems. While feeding energetics have been the subject of numerous studies [1][2][3][4][5][6][7][8][9][10][11][12][13][14], there are no comparative, empirical studies of the energetic costs of feeding in mammals. Here, we test how the energetic costs of feeding vary in relation to body mass and jawadductor muscle mass and with food properties in a comparative sample of 12 non-human primate species ranging in size from 0.08 to 4.2 kg.…”

Introduction: food processing and nutritional assimilation in animals

“…However, studies relating food material properties to oral processing in vertebrates are limited outside of primates (but see, [44,77,81]). In this special issue, Stilson et al [21], Laird et al [32], Wall et al [61] and Panagiotopoulou et al [56] all explore effects of varying food substrates during oral processing. Despite the importance of understanding the physics of a food substrate, this element of oral processing has thus far had a relatively limited effect on linking diet and morphology within primates [14].…”

“…However, our ability to visualize and measure complex movements inside the oral cavity and pharynx has been revolutionized by development of the three-dimensional high-speed X-ray-based XROMM workflow [18]. Its technological advances, which include marker-less bone motion-reconstruction and measurements of soft tissue dynamics (strain and pennation angle changes), have accelerated the accumulation of data on how the vertebrate skull functions during feeding [19][20][21], how the tongue and its skeleton function during feeding [22][23][24][25][26], and on how muscles drive feeding apparatus function in general [27][28][29][30][31][32][33]. The resulting advances in our understanding of feeding significantly broaden our perspective on food processing biomechanics and support integration with physiology to explore processes occurring deep inside the organism, and not just between the jaws.…”