Ontogenetic allometry and architectural properties of the paravertebral and hindlimb musculature in Eastern cottontail rabbits (Sylvilagus floridanus): functional implications for developmental changes in locomotor performance

Abstract

Due to small body size, an immature musculoskeletal system, and other growth-related limits on performance, juvenile mammals frequently experience a greater risk of predation than their adult counterparts. As a result, behaviorally precocious juveniles are hypothesized to exhibit musculoskeletal advantages that permit them to accelerate rapidly and evade predation. This hypothesis was tested through detailed quantitative evaluation of muscle growth in wild Eastern cottontail rabbits (Sylvilagus floridanus). Cottontail rabbits experience high rates of mortality during the first year of life, suggesting that selection might act to improve performance in growing juveniles. Therefore, it was predicted that muscle properties associated with force and power capacity should be enhanced in juvenile rabbits to facilitate enhanced locomotor performance. We quantified muscle architecture from 24 paravertebral and hindlimb muscles across ontogeny in a sample of n = 29 rabbits and evaluated the body mass scaling of muscle mass (MM), physiological cross-sectional area (PCSA), isometric force (F max ), and instantaneous power (P inst ), along with several dimensionless architectural indices. In contrast to our hypothesis, MM and PCSA for most muscles change with positive allometry during growth by scaling at M 1:3 b and M 1:1 b , respectively, whereas F max and P inst generally scale indistinguishably from isometry, as do the architectural indices tested. However, scaling patterns indicate that the digital flexors and ankle extensors of juvenile S. floridanus have greater capacities for force and power, respectively, than those in adults, suggesting these muscle properties may be a part of several compensatory features that promote enhanced acceleration performance in young rabbits. Overall, our study implies that body size constraints place larger, more mature rabbits at a disadvantage during acceleration, and that adults must develop hypertrophied muscles in order to maintain mechanical similarity in force and power capacities across development. These findings challenge the accepted understanding that juvenile animals are at a performance detriment relative to adults. Instead, for prey-predator interactions necessitating short intervals of high force and power generation relative to body mass, as demonstrated by rapid acceleration of cottontail rabbits fleeing predators, it may be the adults that struggle to keep pace with juveniles.

Only the Good Die Old? Ontogenetic Determinants of Locomotor Performance in Eastern Cottontail Rabbits (Sylvilagus floridanus)

“…Nevertheless, ontogenetic scaling analysis showed that hindimb P musc scaled to body mass at a rate needed to maintain “mechanical similarity” (i.e., maintenance of functional capacities across growth-related increases in size; Carrier 1983 ) ( Fig. 7 E; P musc = 2.2M b 1.32 [1.240, 1.404] , R 2 : 0.98; mechanical similarity prediction = M b 1.33 ; also see Butcher et al. (2019) ), indicating that the superior mass-specific power capacities of juvenile rabbits were more likely due to their smaller overall size than more powerful muscles per se .…”

“…7 E), the superior performance of juveniles is most likely due to their absolutely smaller body size. Seen in this light, the ontogenetic allometry of the S. floridanus musculoskeletal system may be more indicative of the need for adults to keep pace with juveniles, rather than the converse ( Butcher et al. 2019 ).…”

“…All procedures were approved by the Northeast Ohio Medical University (NEOMED) Institutional Animal Care and Use Committee (Protocols 10-032 and 13-026, to JWY) and the Ohio Department of Natural Resources Division of Wildlife (Permits 14-310, 15-173, and 16-128 to GAS) prior to this research. Details of our data collection procedures have been published previously ( Butcher et al. 2019 ; Foster et al.…”

“…We used architectural measurements of several hip, knee, and ankle extensor muscles to estimate how growth affected total available peak instantaneous hindlimb muscle power (P musc ) during S. floridanus ontogeny (see Table 1 for a list of the specific muscles in our sample). Following our previously published protocol ( Butcher et al. 2019 ), muscles were individually excised from the hindlimb and with their tendons removed, muscle belly mass (MM) was measured with an electronic balance.…”

Ontogeny of effective mechanical advantage in Eastern cottontail rabbits (Sylvilagus floridanus)

“…Owing to variation in animal condition and motivation, and occasional equipment malfunction, we were only able to collect locomotor performance data in 42 rabbits. Of the animals contributing locomotor performance data, we euthanized 14 animals for detailed anatomical study, including measurements of r for several hindlimb extensor muscles and fiber architecture (see below; Butcher et al, 2019). The sample for the present study consists of a subset of 13 individuals for whom we obtained sufficient kinematic and morphological data to calculate EMA.…”