Appendicular Muscle Physiology and Biomechanics inCrocodylus niloticus

Abstract

Archosaurian reptiles (including living crocodiles and birds) had an explosive diversification of locomotor form and function since the Triassic ∼250 million years ago. Their limb muscle physiology and biomechanics are pivotal to our understanding of how their diversity and evolution relate to locomotor function. Muscle contraction velocity, force and power in extinct archosaurs such as early crocodiles, pterosaurs or non-avian dinosaurs is not available from fossil material, but is needed for biomechanical modelling and simulation. However, an approximation or range of potential parameter values can be obtained by studying extant representatives of the archosaur lineage. Here, we study the physiological performance of three appendicular muscles in Nile crocodiles (Crocodylus niloticus). Nile crocodile musculature showed high power and velocity values—the flexor tibialis internus 4 muscle, a small “hamstring” hip extensor and knee flexor actively used for terrestrial locomotion, performed particularly well. Our findings demonstrate some physiological differences between muscles, potentially relating to differences in locomotor function and muscle fibre type composition. By considering these new data from a previously unstudied archosaurian species in light of existing data (e.g., from birds), we can now better bracket estimates of muscle parameters for extinct species and related extant species. Nonetheless, it will be important to consider the potential specialization and physiological variation among muscles, because some archosaurian muscles (such as those with terrestrial locomotor function) may well have close to double the muscle power and contraction velocity capacities of others.

Musculoskeletal modelling of the Nile crocodile (Crocodylus niloticus) hindlimb: Effects of limb posture on leverage during terrestrial locomotion

“…DDNC04 provided information on muscle architectural properties, comprising standard measurements (Allen et al, 2014 ; Martin et al, 2020 ) of (1) muscle mass (electronic balance ±0.001 g); (2) optimal isometric fascicle length (ℓo) which was assumed equal to dissected resting fibre length (digital callipers, ±0.1 mm; 1–10 measurements/muscle depending on the size and variation of architecture); and (3) pennation θ (protractor, ±5°; 1−5 measurements/muscle under dissecting microscope). These data were used to estimate each muscle's maximum isometric force (henceforth F max ; calculated following Alexander et al, 1979 ; Lieber & Boakes, 1988 ; Hutchinson et al, 2015 ; Allen et al, 2014 ): where m is the muscle mass, σ is the muscle's stress with a value of 300 kN/m 2 used (Medler, 2002 ; Michel et al, 2020 ) and p is the tissue density with a density of 1060 kg/m 3 (Hutchinson et al, 2015 ; Mendez & Keys, 1960 ).…”

“…where m is the muscle mass, σ is the muscle's stress with a value of 300 kN/m 2 used (Medler, 2002;Michel et al, 2020) and p is the tissue density with a density of 1060 kg/m 3 (Hutchinson et al, 2015;Mendez & Keys, 1960).…”

Anatomically grounded estimation of hindlimb muscle sizes in Archosauria

“…We also compared our PCSA estimates with the results of Bishop, Cuff, et al ( 2021 ), who used normalised muscle architecture data (muscle masses, and then fibre lengths estimated from musculotendon length changes; Sellers et al, 2013 , 2017 ) from extant archosaurs to estimate PCSAs (their ‘variant 3’ musculoskeletal model). As in the latter study, the maximal isometric force ( F max ) of muscles was estimated as (PCSA * 0.3 N mm −2 ) (Medler, 2002 ; Michel et al, 2020 ). Furthermore, we predicted the total single‐hindlimb muscle mass and PCSA from body mass (of Coelophysis bauri ) using the phylogenetically generalised least squares regressions using the dataset of Bishop, Wright, et al ( 2021 ) in R Studio ( https://www.r‐project.org/ ).…”

“…The maximal isometric force that these skeletal muscles can generate is directly proportional to the physiological‐cross‐sectional area (PCSA) of the muscles (e.g. Medler, 2002 ; Michel et al, 2020 ; Powell et al, 1984 ). Hence information on PCSAs of muscles, and other ‘muscle architecture’ data such as muscle fibre or fascicle lengths and pennation angles, are valuable for relating form to function in the musculoskeletal system (for reviews see Bishop, Wright, et al, 2021 ; Martin et al, 2020 ).…”