Monitoring muscle over three orders of magnitude: Widespread positive allometry among locomotor and body support musculature in the pectoral girdle of varanid lizards (Varanidae)

Abstract

There is a functional trade-off in the design of skeletal muscle. Muscle strength depends on the number of muscle fibers in parallel, while shortening velocity and operational distance depend on fascicle length, leading to a trade-off between the maximum force a muscle can produce and its ability to change length and contract rapidly. This trade-off becomes even more pronounced as animals increase in size because muscle strength scales with area (length 2) while body mass scales with volume (length 3). In order to understand this muscle trade-off and how animals deal with the biomechanical consequences of size, we investigated muscle properties in the pectoral girdle of varanid lizards. Varanids are an ideal group to study the scaling of muscle properties because they retain similar body proportions and posture across five orders of magnitude in body mass and are highly active, terrestrially adapted reptiles. We measured muscle mass, physiological cross-sectional area, fascicle length, proximal and distal tendon lengths, and proximal and distal moment arms for 27 pectoral girdle muscles in 13 individuals across 8 species ranging from 64 g to 40 kg. Standard and phylogenetically informed reduced major axis regression was used to investigate how muscle architecture properties scale with body size. Allometric growth was widespread for muscle mass (scaling exponent >1), physiological cross-sectional area (scaling exponent >0.66), but not tendon length (scaling exponent >0.33). Positive allometry for muscle mass was universal among muscles responsible for translating the trunk forward and flexing the elbow, and nearly universal among humeral protractors and wrist flexors. Positive allometry for PCSA was also common among trunk translators and humeral protractors, though less so than muscle mass. Positive scaling for fascicle length was not widespread, but common among humeral protractors. A higher proportion of pectoral girdle muscles scaled with positive allometry than our previous work showed for the pelvic girdle, suggesting that the center of mass may move cranially with body size in varanids, or that the pectoral girdle may assume a more dominant role in locomotion in larger species. Scaling exponents for physiological cross-sectional area among muscles primarily associated with propulsion or with a dual role were generally higher than those associated primarily with support | 1115 CIERI Et al.

The scaling of ground reaction forces and duty factor in monitor lizards: implications for locomotion in sprawling tetrapods

“…Femoral adduction and knee and ankle joint angles did not vary significantly with size (40 g-8 kg) in a previous study on varanids [9]. Larger varanids have previously been shown to compensate for the predicted sizedependent loss of muscle force by possessing pelvic [17] and pectoral muscles [19] of greater mass and physiological cross-sectional area, reduced locomotor speeds [20], increased duty factors and modest changes in femoral kinematics [9].…”

The Evolution of Appendicular Muscles During the Fin-to-Limb Transition: Possible Insights Through Studies of Soft Tissues, a Perspective

“…Concerning tetrapods, we excluded all birds from our dataset since they have highly derived forelimbs specialized for flight, but we covered a diversity of tetrapods that use quadrupedal locomotion. We included the data on the alligator Alligator mississippiensis (Allen et al, 2010), varanid lizards (Dick and Clemente, 2016;Cieri et al, 2020), and several mammals (Payne et al, 2005a;Ercoli et al, 2013Ercoli et al, , 2015Moore et al, 2013;Rupert et al, 2015;Warburton et al, 2015;Olson et al, 2016;Martin et al, 2019). The publications on the coelacanth (Huby et al, 2021), the alligator (Allen et al, 2010), the varanids (Dick and Clemente, 2016;Cieri et al, 2020), the short-nosed bandicoot Isoodon (Warburton et al, 2015;Martin et al, 2019) and the grison Galictis (Ercoli et al, 2013(Ercoli et al, , 2015 include both the pectoral and pelvic appendages.…”

“…We included the data on the alligator Alligator mississippiensis (Allen et al, 2010), varanid lizards (Dick and Clemente, 2016;Cieri et al, 2020), and several mammals (Payne et al, 2005a;Ercoli et al, 2013Ercoli et al, , 2015Moore et al, 2013;Rupert et al, 2015;Warburton et al, 2015;Olson et al, 2016;Martin et al, 2019). The publications on the coelacanth (Huby et al, 2021), the alligator (Allen et al, 2010), the varanids (Dick and Clemente, 2016;Cieri et al, 2020), the short-nosed bandicoot Isoodon (Warburton et al, 2015;Martin et al, 2019) and the grison Galictis (Ercoli et al, 2013(Ercoli et al, , 2015 include both the pectoral and pelvic appendages. The data for the American badger, Taxidea taxus (Moore et al, 2013), the nine-banded armadillo, Dasypus novemcinctus (Olson et al, 2016), and the marmot Marmota monax (Rupert et al, 2015) pertain only to the forelimb, whereas the data for the horse Equus caballus (Payne et al, 2005a) pertain only to the hind limb.…”

The evolutionary biomechanics of locomotor function in giant land animals

“…Scaling of supportive non-skeletal tissues reinforces what the skeletal scaling data reveal – yet the data are more sparse and based on limited sample sizes, and there is underexplored potential for phylogenetic biases. Limb muscles of most mammals, birds and lizards scale with overall allometry of strength-related geometry (>mass 0.67 ; Alexander et al, 1979b , 1981 ; Bennett, 1996 ; Cieri et al, 2020 ; Dick and Clemente, 2017 ; Maloiy et al, 1979 ; Pollock and Shadwick, 1994a ), despite a constant capacity of muscle to produce isometric force per unit area ( Close, 1972 ; Medler, 2002 ; Rospars and Meyer-Vernet, 2016 ). In contrast, amniote tendon geometry scales isometrically or with negative allometry, rendering the relatively thinner leg tendons of larger mammals and birds more likely to act in a spring-like fashion; as muscle force/tendon area generally increases with size.…”

“…That variation is analogous to patterns described by Dick and Clemente (2017) for felid mammals and varanid lizards, two groups with broad size ranges. Felids are less crouched (have an apparently higher EMA) than varanid lizards, which maintain safe tissue stresses via allometrically larger muscles ( Dick and Clemente, 2016 ; Cieri et al, 2020 ). Felids, then, may simply cope with being weaker at larger sizes and reducing relative athletic capacity more steeply with increases in size, but neither felids nor varanids abandon whole gaits as their size increases.…”