The reproductive success of wild animals usually increases with age before declining at the end of life, but the proximate mechanisms underlying those patterns remain elusive. Young animals are expected to invest less in current reproduction due to high prospects for future reproduction (the "restraint" hypothesis). The oldest animals may also show restraint when conditions are sub-optimal where even a small increase in reproductive investment may lead to death ("terminal restraint"). Alternatively, reproduction may be constrained by lack of experience and senescence (the "constraint" hypothesis). In two species of breeding seabirds, behavioural (time to return the offspring, calmness during restraint) and physiological (metabolism, glucose and corticosterone) parameters responded similarly to stress with advancing age, implying a generalized stress response. Across those parameters, birds were "shy" (high stress response) when young or old, and "bold" (low stress response) when middle-aged. Specifically, free corticosterone, the principal avian glucocorticoid responsible for directing energy away from reproduction and towards immediate survival following stress, was highest in both young and very old stressed birds. All age groups had a similar adrenal capacity to produce corticosterone, implying that middle-aged birds were showing restraint. Because the stress response, was highest at ages when the probability of current reproduction was lowest rather than at ages when the probability of future reproduction was highest we concluded that birds restrained reproductive investment based on current conditions rather than potential future opportunities. In particular, old birds showed terminal restraint when stressed. Hormonal cues promoted investment in adult survival over reproductive output at both the start and end of life consistent with the restraint hypothesis.