Avoidance of Skeletal Muscle Atrophy in Spontaneous and Facultative Hibernators

Abstract

Smooth and skeletal muscle changes were compared from overwintering white-tailed prairie dogs, spontaneous hibernators that undergo regular, low-temperature torpor bouts, and black-tailed prairie dogs, facultative hibernators that use sporadic, moderate-temperature torpor bouts. The objectives were to assess the abilities of these two species with dramatically different torpor patterns (1) to conserve skeletal muscle morphology, protein, and strength and (2) to use labile protein in the small intestine and liver during the winter season of reduced activity and food intake. Mass and protein concentration of the extensor digitorum longus (EDL), soleus, liver, and small intestine, as well as skeletal muscle strength and fiber morphology for the EDL and soleus, were compared before and after hibernation in both species. Both species appeared to be similar to overwintering black bears and underwent very little strength and protein loss, as compared with euthermic models of immobility and long-term fasting. Although the two species used vastly different hibernation strategies, none of the changes in parameters related to muscle atrophy and labile-protein use during the hibernation season differed significantly between them. Therefore, it appears that regardless of the phenotypic expressions of hibernation, the outcome is the conservation of skeletal muscle.

Daily torpor reduces mass and changes stress and power output of soleus and EDL muscles in the Djungarian hamster, Phodopus sungorus

“…Therefore, there appears to have been significant skeletal muscle atrophy and reduction of body fat in response to torpor conditions. Some previous studies on hibernation have also found significant skeletal muscle atrophy; for example, 13 to 30% skeletal muscle mass loss in a number of species of hibernating mammals (Musacchia et al, 1989;Rourke et al, 2004;Cotton and Harlow, 2010). However, in other previous work, there was no evidence of skeletal muscle atrophy during hibernation (Rourke et al, 2004;Lohuis et al, 2007a;Lee et al, 2008;Cotton and Harlow, 2010).…”

“…Some previous studies on hibernation have also found significant skeletal muscle atrophy; for example, 13 to 30% skeletal muscle mass loss in a number of species of hibernating mammals (Musacchia et al, 1989;Rourke et al, 2004;Cotton and Harlow, 2010). However, in other previous work, there was no evidence of skeletal muscle atrophy during hibernation (Rourke et al, 2004;Lohuis et al, 2007a;Lee et al, 2008;Cotton and Harlow, 2010). Muscle atrophy can be caused by reductions in the load or activity experienced by the muscle (Musacchia et al, 1988;Narici and Maganaris, 2007;Phillips et al, 2009).…”

“…More than 3months of hibernation in black bears caused a relatively small (15%) decrease in skeletal muscle protein concentration (Tinker et al, 1998), a 29% loss of absolute isometric force in tibialis anterior muscle, and a significant reduction in fatigue resistance, but no significant changes in twitch force generation times or relaxation times (Lohuis et al, 2007b). Hibernation in golden hamsters and prairie dogs also had limited effects on isometric muscle performance (Vyskocil and Gutmann, 1977;Cotton and Harlow, 2010). Maintenance of skeletal muscle performance during periods of natural dormancy is desirable to enable animals to undertake fitness-related activities, such as those behaviours related to prey capture, predator avoidance or reproduction, as soon as they arouse from torpor.…”

Mechanisms underlying inhibition of muscle disuse atrophy during aestivation in the green-striped burrowing frog, Cyclorana alboguttata

“…Whereas hibernating U. americanus lower their body temperature by only 2-5°C (Lohuis et al, 2007b), ground squirrels in deep torpor reduce core temperature to near ambient (approximately 4°C), yet both species show minimal muscle atrophy despite months of inactivity. Furthermore, a study examining two species of prairie dogs found no difference in the extent of muscle or strength loss between the two despite differences in their hibernation strategies (one experiencing normal torpor cycles with very low core temperatures, the other being facultative hibernators that use sporadic, moderate-temperature torpor cycles) (Cotton and Harlow, 2010).…”

“…However, recent investigations have examined the structure, function and plasticity of muscles in organisms that experience natural periods of muscle disuse or immobilisation, such as aestivating frogs and hibernating mammals (Cotton and Harlow, 2010;Harlow et al, 2001;Hudson and Franklin, 2002a;Mantle et al, 2009;Nowell et al, 2011;Symonds et al, 2007;Young et al, 2011). These studies have shown that animals which undertake extended bouts of natural immobility (i.e.…”