While the normal function of tendons is critical for daily activity and a high quality of life, the specific micro-structural mechanisms underlying their function and their ability to bear load remain unknown. A central unresolved question is whether collagen fibrils in tendon bear load independently or if the applied load is transferred across fibrils through interfibrillar forces. The objectives of this dissertation were to determine the effects of interfibrillar sliding on tendon fascicle macroscale mechanics, quantify the magnitude of the associated interfibrillar shear stresses, and identify the possible physical structures that transmit loads between fibrils. Multiscale experimental testing using confocal microscopy was conducted to investigate the relationship between interfibrillar sliding and the uniaxial macroscale mechanics of rat tail tendon fascicles. Additionally, a shear lag model was used to test whether load transfer between fibrils through interfibrillar shear could explain the experimental data. Microscale notch tension testing was performed to confirm the existence of such interfibrillar shear forces and measure their magnitude. Finally, serial block-face scanning electron microscopy (SBF-SEM) and enzymatic removal of the extrafibrillar tissue components were used to identify the possible structures that transmit load between fibrils.

Multiscale experimental testing demonstrated that greater interfibrillar sliding was associated with a decrease in the macroscale tissue modulus and increased stress relaxation. The shear lag model demonstrated that load transfer between discontinuous fibrils via shearing of a plastic interfibrillar matrix uniquely explains the observed experimental data. Additionally, the magnitude of the interfibrillar shear stress obtained from notch tension testing was comparable to that predicted by the shear lag model. The SBF-SEM images showed smaller diameter fibrils weaving around and fusing with larger diameter fibrils, suggesting that these smaller diameter fibrils, and not extrafibrillar tissue components, may be the structural origin of interfibrillar shear forces in tendon. This hypothesis was supported by trypsin digestions, which successfully removed the extrafibrillar proteins but did not change the fascicle mechanical behavior. Collectively, these data strongly suggest that fibrils are discontinuous and that interfibrillar sliding and shear load transfer are the mechanisms underlying tendon fascicle multiscale mechanics.