Muscle architecture dynamics modulate performance of the superficial anterior temporalis muscle during chewing in capuchins

Abstract

Jaw-muscle architecture is a key determinant of jaw movements and bite force. While static lengthforce and force-velocity relationships are well documented in mammals, architecture dynamics of the chewing muscles and their impact on muscle performance are largely unknown. We provide novel data on how fiber architecture of the superficial anterior temporalis (SAT) varies dynamically during naturalistic feeding in tufted capuchins (Sapajus apella). We collected data on architecture dynamics (changes in muscle shape or the architectural gear ratio) during the gape cycle while subjects fed on foods of different mechanical properties. Architecture of the SAT varied with phases of the gape cycle, but gape distance accounted for the majority of dynamic changes in architecture. in addition, lower gear ratios (low muscle velocity relative to fascicle velocity) were observed when animals chewed on more mechanically resistant foods. At lower gear ratios, fibers rotated less during shortening resulting in smaller pinnation angles, a configuration that favors increased force production. Our results suggest that architectural dynamics may influence jaw-muscle performance by enabling the production of higher bite forces during the occlusal phase of the gape cycle and while processing mechanically challenging foods.

Feeding postural behaviors and food geometric and material properties in bearded capuchin monkeys (Sapajus libidinosus)

“…Broadly, behavioral flexibility (sometimes called behavioral plasticity, but see Strier, 2017 ) is the ability to modify behavior for a short time in response to a stimulus, such as a food. Studies of force‐gape tradeoffs, bite and muscle forces, and feeding behaviors in primates suggest behavioral flexibility during primate feeding relates to the biomechanical configuration of the feeding system and the foods (Coiner‐Collier et al, 2016 ; Laird, Granatosky, et al, 2020 ; Laird, Wright, et al, 2020 ; Ross et al, 2016 ; Ross & Iriarte‐Diaz, 2019 ; Taylor & Vinyard, 2009 ; Wright, 2005 ). While the feeding and locomotor systems are infrequently related (but see Granatosky et al, 2019 ), our results suggest both systems are behaviorally flexible in response to food items.…”

“…Food geometric and mechanical properties are thought to influence primate feeding behaviors (Bouvier, 1986a , 1986b ; Coiner‐Collier et al, 2016 ; Daegling, 1992 ; Daegling & McGraw, 2007 ; Hylander, 1975 ; Jolly, 1970 ; Kay, 1975 ; Kinzey, 1974 , 1992 ; Koyabu & Endo, 2009 ; Laird, 2017 ; Laird, Ross, & O'Higgins, 2020 ; Lucas, 2004 ; Rosenberger, 1992 ; Rosenberger & Kinzey, 1976 ; Silverman et al, 2001 ; Taylor, 2006 ; but see Ross et al, 2012 and Ross & Iriarte‐Diaz, 2014 ). Mechanically and size‐challenging foods will be placed at locations along the toothrow that facilitate large gapes, increased muscle force, and maximize jaw mechanical advantage (e.g., Coiner‐Collier et al, 2016 ; Greaves, 1978 ; Laird, Granatosky, et al, 2020 ; Spencer, 1998 ; Spencer, 1999 ; Spencer & Demes, 1993 ; Taylor & Vinyard, 2009 ; Vogel et al, 2009 ; Wright, 2005 ). While much attention has been paid to craniodental feeding behaviors, variation in the postcranial behaviors during feeding is not well understood.…”

“…While the relationship between food properties and feeding behaviors has been investigated in several species of primates (Bouvier, 1986a , 1986b ; Coiner‐Collier et al, 2016 ; Daegling, 1992 ; Daegling & McGraw, 2007 ; Hylander, 1975 ; Jolly, 1970 ; Kay, 1975 ; Kinzey, 1974 , 1992 ; Koyabu & Endo, 2009 ; Laird, 2017 ; Laird, Ross, & O'Higgins, 2020 ; Lucas, 2004 ; Rosenberger, 1992 ; Rosenberger & Kinzey, 1976 ; Silverman et al, 2001 ; Taylor, 2006 ; but see Ross et al, 2012 and Ross & Iriarte‐Diaz, 2014 ), it is unknown whether feeding postural behaviors also reflect differences in geometric properties (specifically food size) and FMPs. Studies of feeding behaviors have indicated that FMPs and food size play a key role in determining the type of feeding behavior, the location of food placement within the mouth, and the amount of bite force (e.g., Herring & Herring, 1974 ; Laird, Granatosky, et al, 2020 ; Lucas, 2004 ; Perry et al, 2011 ; Wright, 2005 ). Studies of primate FMPs have focused on two measures: food toughness and elastic modulus.…”

Differences in muscle mechanics underlie divergent optimality criteria between feeding and locomotor systems

“…Some of these variables are known to vary between the feeding and locomotor systems (e.g., Hoh, 2002; Österlund et al ., 2011; Anderson and Roberts, 2020) and have effects on an individual muscle's ability to generate force or speed (Narici et al ., 1992; Morse et al ., 2005; Knudson, 2007; Eng et al ., 2009; Taylor and Vinyard, 2009; Guimarães et al ., 2013). Furthermore, this study ignores length–tension properties of muscles (Dumont and Herrel, 2003; Eng et al ., 2009; Gidmark et al ., 2013) and muscle architecture dynamics (Laird et al ., 2020). However, such considerations are beyond the scope of this study as it was our intent to simply explore the “anatomical potential” for certain muscle configurations to produces high forces vs. wide excursion.…”

Primate body mass and dietary correlates of tooth root surface area

“…This puzzling finding is likely due to the nature of anatomically derived BF, which is calculated as the summed PCSA of the jaw adductor muscles, and therefore estimates the maximal force which can be generated when all muscles are firing maximally and simultaneously. This is an unrealistic and potentially impossible behavior—for example, we know the masticatory adductors fire at different times during the chewing cycle (e.g., Hylander et al, 1987; Vinyard et al, 2008) and muscle architecture, including PCSA, and therefore the capacity for force generation varies within a given gape cycle and across gape cycles of different velocity (Laird et al, 2020)—but the assumption of maximal contraction is necessary in the absence of sufficient in vivo data, as no direct evidence exists for what percentage of the muscle is being used in any given bite for the vast majority of taxa. In rodent models, habitual BF has been found to be lower than BF predicted based on PCSA (Becerra et al, 2011); thus, it is likely that within primates, myological estimates of BF potential also overestimate actual BFs.…”