Testing the function of dromaeosaurid (Dinosauria, Theropoda) ‘sickle claws’ through musculoskeletal modelling and optimization

Abstract

Dromaeosaurids were a clade of bird-like, carnivorous dinosaurs that are well known for their characteristic morphology of pedal digit II, which bore an enlarged, sickle-shaped claw and permitted an extreme range of flexion–extension. Proposed functions for the claw often revolve around predation, but the exact manner of use varies widely. Musculoskeletal modelling provides an avenue to quantitatively investigate the biomechanics of this enigmatic system, and thereby test different behavioural hypotheses. Here, a musculoskeletal model of the hindlimb and pes of Deinonychus was developed, and mathematical optimization was used to assess the factors that maximize production of force at the claw tip. Optimization revealed that more crouched hindlimb postures (i.e., more flexed knees and ankles) and larger flexor muscle volumes consistently increased claw forces, although the optimal degree of digit flexion or extension depended on assumptions of muscle activity and fibre operating range. Interestingly, the magnitude of force capable of being produced at the claw tip was relatively small, arguing against regular transmission of a large proportion of body weight into a substrate principally via the claw tip. Such transmission would therefore likely have needed to occur via more proximal parts of the foot. Collectively, the results best support a grasping function for digit II (e.g., restraint of prey smaller than the dromaeosaurid’s own body size), although other behaviours involving flexed hindlimbs cannot be excluded.

How to build a dinosaur: Musculoskeletal modeling and simulation of locomotor biomechanics in extinct animals

“…Here, MTU paths in OpenSim were created to run between the approximate centroids of origin and insertion. As in many previous studies of extinct archosaurs (Hutchinson et al 2005, 2008; Bates and Schachner 2012; Bates et al 2012a,b; Brassey et al 2017; Otero et al 2017; Sellers et al 2017; Bishop et al 2018c; Bishop 2019), these paths were constrained to follow anatomically realistic lines of action across the full ROM of each joint, using a combination of “via points” and “wrapping surfaces.” Representative examples of these in the Coelophysis model are illustrated in Figure 6. Via points are points in space through which the MTU must pass, and wrapping surfaces are geometric primitives (available shapes in OpenSim are spheres, ellipsoids, cylinders, and tori) around which a given MTU is constrained to pass, following the shortest route to do so (Delp et al 1990; Garner and Pandy 2000; Sherman et al 2013).…”

“…Both are key determinants of F max (eq. 2) and previous sensitivity analyses have demonstrated their important effects on biomechanical inferences in extinct taxa (Hutchinson 2004b;Bates et al 2010;Bates and Falkingham 2018;Bishop 2019). Variants 3 and 4 were derived on the basis (to one degree or another) of comparative data for extant species, but this does not account for the real possibility that extinct species such as nonavian theropods may have been structurally arranged in a markedly different fashion to any extant species: different sizes, shapes, proportions, postures, and (presumably) functions of the underlying skeleton may lead to muscle anatomy in an extinct species being adapted or "tuned" in ways that differ from those observed in any extant species (Bishop 2019).…”

“…Here, MTU paths in OpenSim were created to run between the approximate centroids of origin and insertion. As in many previous studies of extinct archosaurs (Hutchinson et al 2005(Hutchinson et al , 2008Bates and Schachner 2012;Bates et al 2012a,b;Brassey et al 2017;Otero et al 2017;Sellers et al 2017;Bishop et al 2018c;Bishop 2019), these paths were constrained to follow anatomically realistic lines of action across the full ROM of each joint, using a combination of "via points" and "wrapping surfaces." Representative examples of these in the Coelophysis model are illustrated in Figure 6.…”

“…Then, given body mass and MTU length for an extinct focal species (derived from models built in the steps outlined earlier), muscle-specific estimates of mass and fiber length, and in turn F max , are back-calculated. It should be noted that neither of the two methods covered here directly estimate muscle pennation, which in certain systems may have an important influence on system behavior (Zajac 1989;Bishop 2019) and could potentially be estimated by other means such as phylogenetic character mapping. Additionally, many animals possess muscles in which fiber pennation angle varies throughout a muscle belly, and hence a single value, as used in modeling, will not capture the (potentially important) internal heterogeneity in architecture (Dickinson et al 2018;Sullivan et al 2019;Martin et al 2020).…”

Computational modelling of muscle fibre operating ranges in the hindlimb of a small ground bird (Eudromia elegans), with implications for modelling locomotion in extinct species

“…The relevance of fibre length to understanding organismal function, performance and ecology extends beyond just extant species. Attempts to better understand the behaviour and function of enigmatic extinct species, such as non-avian dinosaurs [ 54 , 59 – 68 ], early hominids [ 69 – 71 ] or mammal ancestors [ 72 ], have often employed musculoskeletal models of varying complexity. A central issue for each of these studies is the fact that various biomechanically relevant parameters remain unknown for fossil species, especially aspects pertaining to soft tissues such as muscle size (strength) and ℓ o .…”