Mechanical similarity across ontogeny of digging muscles in an Australian marsupial (Isoodon fusciventer)

Abstract

Many mammals dig, either during foraging to access subsurface food resources, or in creating burrows for shelter. Digging requires large forces produced by muscles and transmitted to the soil via the skeletal system; thus fossorial mammals tend to have characteristic modifications of the musculoskeletal system that reflect their digging ability. Bandicoots (Marsupialia: Peramelidae) scratch‐dig mainly to source food, searching for subterranean food items including invertebrates, seeds, and fungi. They have musculoskeletal features for digging, including shortened, robust forelimb bones, large muscles, and enlarged muscle attachment areas. Here, we compared changes in the ontogenetic development of muscles associated with digging in the Quenda (Isoodon fusciventer). We measured muscle mass (m m), pennation angle, and fiber length (FL) to calculate physiological cross‐sectional area (PCSA; a proxy of maximum isometric force) as well as estimate the maximum isometric force (Fmax) for 34 individuals ranging in body size from 124 to 2,390 g. Males grow larger than females in this bandicoot species, however, we found negligible sex differences in mass‐specific m m, PCSA or FL for our sample. Majority of the forelimb muscles PCSA showed a positive allometric relationship with total body mass, while m m and FL in the majority of forelimb muscles showed isometry. Mechanical similarity was tested, and two thirds of forelimb muscles maximum isometric forces (Fmax) scaled with isometry; therefore the forelimb is primarily mechanical similar throughout ontogeny. PCSA showed a significant difference between scaling slopes between main movers in the power stroke, and main movers of the recovery stroke of scratch‐digging. This suggests that some forelimb muscles grow with positive allometry, specially these associated with the power stroke of digging. Intraspecific variation in PCSA is rarely considered in the literature, and thus this is an important study quantifying changes in muscle architectural properties with growth in a mammalian model of scratch‐digging.

Covariation between forelimb muscle anatomy and bone shape in an Australian scratch‐digging marsupial: Comparison of morphometric methods

“…The species displays adaptations of both muscle and bone anatomy associated with scratch‐digging (Warburton et al, ). This study builds on previous findings that showed Quenda force generation capacity (PCSA) showed differential growth between main movers of the recovery stroke and the power stroke of scratch‐digging (Martin, Warburton, Travouillon, & Fleming, ). We therefore predicted that muscles associated with the power‐stroke of digging will have disproportionate influence on shape change of the long bones.…”

“…Quenda are sexually dimorphic in body mass (Warburton & Travouillon, ) and we therefore predicted that there may be some sex differences in forelimb musculature or bone shape. Despite these differences, we previously identified that Quenda forelimb muscle anatomy (muscle mass, PCSA, and fiber length) showed no significant difference between the sexes (Martin et al, ). Furthermore, there were only minor sex differences in a single forelimb bone in the Quenda in the present study; the third metacarpal showed shape differences between the sexes, with males having a smaller, less elongated proximal end.…”

“…Muscles were dissected and measured for mass and PCSA; these data have been fully analyzed and published separately (Martin et al, ) (Table ). Muscle mass is a representation of overall muscle size, while PCSA is a representation of maximum isometric force production for individual muscles.…”

Comparative forelimb myology and muscular architecture of a juvenile Malayan tapir (Tapirus indicus)

“…; Martin et al. ). Unfortunately, no data is presently available for ontogenetic variation or scaling in muscle architecture for perissodactyls, and therefore scaling of juvenile Tapirus data to an adult size was not performed.…”

“…As equids are much larger than juvenile tapirs, direct comparison of muscle mass was considered unsuitable. Ontogenetic studies of mammalian and avian muscle and tendon anatomy suggest that limb muscles can scale both allometrically and isometrically through ontogeny, dependent upon the muscle and the taxon (Miller et al 2008;Olson et al 2018;Martin et al 2019). Unfortunately, no data is presently available for ontogenetic variation or scaling in muscle architecture for perissodactyls, and therefore scaling of juvenile Tapirus data to an adult size was not performed.…”