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Using short duration perturbations, previous attempts to measure the intrinsic ankle stiffness during human standing have revealed a substantial stabilizing contribution (65–90% normalized to load stiffness ‘mgh’). Others regard this method as unsuitable for the low-frequency conditions of quiet standing and believe the passive contribution to be small (10–15%). This latter view, consistent with a linear Hill-type model, argues that during standing, the contractile portion of the muscle is much less stiff than the tendon. Here, for upright subjects, we settle this issue by measuring the stiffness of the contractile portion of the passive calf muscles using low-frequency ankle rotations. Using ultrasound we tracked the changes in muscle contractile length and partitioned the ankle rotation into contractile and extra-contractile (series elastic) portions. Small ankle rotations of 0.15 and 0.4 deg show a contractile to series elastic stiffness ratio (Kce/Kse) of 12 ± 9 and 6.3 ± 10, respectively, with both elements displaying predominantly elastic behaviour. Larger, 7 deg rotations reveal the range of this ratio. It declines in a non-linear way from a high value (Kce/Kse= 18 ± 11) to a low value (Kce/Kse= 1 ± 0.4) as rotation increases from 0.1 to 7 deg. There is a marked transition at around 0.5 deg. The series elastic stiffness (Kse/mgh) remains largely constant (77 ± 13%) demonstrating the contractile component origin of passive, short range stiffness. The linear Hill-type model does not describe the range-related stiffness relevant to the progression from quiet standing to perturbed balance and movement and can lead to inaccurate predictions regarding human balance.