Forelimb muscle architecture and myosin isoform composition in the groundhog (Marmota monax)

Abstract

Scratch-digging mammals are commonly described as having large, powerful forelimb muscles for applying high force to excavate earth, yet studies quantifying the architectural properties of the musculature are largely unavailable. To further test hypotheses about traits that represent specializations for scratch-digging, we quantified muscle architectural properties and myosin expression in the forelimb of the groundhog (Marmota monax), a digger that constructs semi-complex burrows. Architectural properties measured were muscle moment arm, muscle mass (MM), belly length (ML), fascicle length (l F ), pennation angle and physiological cross-sectional area (PCSA), and these metrics were used to estimate maximum isometric force, joint torque and power. Myosin heavy chain (MHC) isoform composition was determined in selected forelimb muscles by SDS-PAGE and densitometry analysis. Groundhogs have large limb retractors and elbow extensors that are capable of applying moderately high torque at the shoulder and elbow joints, respectively. Most of these muscles (e.g. latissimus dorsi and pectoralis superficialis) have high l F /ML ratios, indicating substantial shortening ability and moderate power. The unipennate triceps brachii long head has the largest PCSA and is capable of the highest joint torque at both the shoulder and elbow joints. The carpal and digital flexors show greater pennation and shorter fascicle lengths than the limb retractors and elbow extensors, resulting in higher PCSA/MM ratios and force production capacity. Moreover, the digital flexors have the capacity for both appreciable fascicle shortening and force production, indicating high muscle work potential. Overall, the forelimb musculature of the groundhog is capable of relatively low sustained force and power, and these properties are consistent with the findings of a predominant expression of the MHC-2A isoform. Aside from the apparent modifications to the digital flexors, the collective muscle properties observed are consistent with its behavioral classification as a lessspecialized burrower and these may be more representative of traits common to numerous rodents with burrowing habits or mammals with some fossorial ability.

Functional Morphology of the Forelimb of the Nine-Banded Armadillo (Dasypus novemcinctus): Comparative Perspectives on the Myology of Dasypodidae

“…The relatively higher expression of the MHC-2A isoform in the digital flexor muscles seems most appropriate for this functional role in scratch-digging. Future studies of additional species of armadillos are needed verify the significance of MHC-2A expression in the distal limbs; however, these findings are consistent with recent observations in the carpal/ digital flexors of burrowing M. monax (Rupert et al 2015).…”

“…Similar to other terrestrial scratch-diggers studied (e.g., Gambaryan 1974;Moore et al 2013;Warburton et al 2013;Rupert et al 2015), forelimb muscle mass in D. novemcinctus is concentrated in the limb retractor, elbow extensor, and digital flexor muscle groups. These functional groups combined accounted for over 80 % of total forelimb muscle mass.…”

“…Moreover, the digital flexors of D. novemcinctus are 13.8 % of intrinsic forelimb muscle mass (see Supplemental Data Figure), a value that is intermediate to that of T. taxus [17.7 % (Moore et al 2013)] and the groundhog, Marmota monax [10.9 % (Rupert et al 2015)]. During scratch-digging, these muscles are expected to initially flex the digits and carpus, causing the robust claws to pierce and dislodge the substrate, and then maintain this flexed position for substrate displacement during the power stroke (Stalheim-Smith 1984;Thewissen and Badoux 1986;Moore et al 2013).…”

“…In addition, available myology and morphological characters from other species of dasypodids will be evaluated to help remedy gaps in our knowledge of comparative muscle structure and digging function in armadillos. This work will also build on our previous studies of muscle architectural properties (Moore et al 2013;Rose et al 2013;Rupert et al 2015) to improve understanding of muscle traits that indicate specialization for fossorial habit as observed across diverse orders of mammals.…”

Muscle architecture of the forelimb of the Golden Pheasant (Chrysolophus pictus) (Aves: Phasianidae) and its implications for functional capacity in flight

“…However, more than any other factor, muscle architecture predicts muscle function (Lieber and Fridén 2000;Ward et al 2009;Lieber and Ward 2011). The importance of muscle fiber architecture has long been recognized and related studies have been widely reported in human and other mammals (Sacks and Roy 1982;Payne et al 2005Payne et al , 2006Williams et al 2007Williams et al , 2008Eng et al 2008;Channon et al 2009;Rupert et al 2014), but seldom in birds. Report on the hind limb of an ostrich by Smith et al (2006) may have been the first comprehensive research on avian muscle architecture.…”