The mechanism by which fibrous tissues adapt upon alterations in their mechanical environment remains unresolved. Here, we determine that periosteum in chick embryos resides in an identical mechanical state, irrespective of the developmental stage. This state is characterized by a residual tissue strain that corresponds to the strain in between the pliant and stiffer region of the force-strain curve. We demonstrate that periosteum is able to regain that mechanical equilibrium state in vitro, within three days upon perturbation of that equilibrium state. This adaptation process is not dependent on protein synthesis, because the addition of cycloheximide did not affect the response. However, a functional actin filament network is required, as is illustrated by a lack of adaptation in the presence of cytochalasin D. This led us to hypothesize that cells actively reduce collagen fiber crimp after tissue shortening, i.e. that in time the number of recruited fibers is increased via cell contraction. Support for this mechanism is found by visualization of fiber crimp with multiphoton microscopy before the perturbation and at different time points during the adaptive response.