Little is known about the mechanical behavior of skeletal muscle at long lengths, or how these behaviors scale to different hierarchical levels. The purpose of this thesis is to examine the mechanical behavior of skeletal muscle leading up to, and at the point of failure. Failure was defined as a compromise in the muscles’ ability to produce force, as indicated by a decrease in force, during a steady stretch. Stretches were performed in active (i.e. contracting) and passive muscles in three different preparations from the semitendinosus muscle of the frog Rana pipiens – myofibrils, permeabilized fibres, and whole muscles. Stress in active myofibrils was significantly greater than in passive ones with the progression of stretch to failure, and was persistent despite being stretched to lengths beyond overlap of actin and myosin filaments (who’s interactions are responsible for the production of contractile force). This divergence in stress was reduced at the cellular level, and was abolished in whole muscles. It is suggested that higher active compared to passive stress is a result of an increased contribution by the large molecular spring, titin. As higher hierarchical levels are examined, the introduction of other passive elements and connections may break during stretch and mask the divergent behavior observed in myofibrils.

Histology and electron microscopy showed complete loss of regular striation patterns in both active and passive fibres stretched to sarcomere lengths of approximately 5 µm. Whole muscles showed indicators of damage as well, but to a much lesser extent, and with active muscles showing more evidence of damage. Mechanical data and histology suggest that failure in whole muscles occurs outside of the cell, perhaps in the extracellular matrix or at the myotendinous junction.

Finally, it was demonstrated that whole muscles possessing a low passive compliance (in this case, the tibialis anterior from R. pipiens) were more prone to failure at short lengths than muscles having a higher compliance (i.e. semitendinosus). It is suggested that differing muscle compliances represent adaptive strategies to prevent damage according to functional demands of the specific muscle.