Abstract During the periodic moult of the plumage of birds, a fast regrowth of feathers would shorten the time of reduced plumage functionality. However, it has long been known that feather growth-rate is limited and that long feathers take disproportionally longer to grow than small feathers, which has severe consequences on moult duration and the completeness of moult in large birds. The reasons for the limitations of feather-growth must be related to the size and/or functions of the feather follicle, but are largely unknown. Here we measured the size of the feather follicle (taking calamus width as a proxy) and related it to parameters of feather growth (feather growth-rate by mass and by length) and feather structure (feather length, mass, massiveness [mass of feather material per mm feather-length]). We used three independent datasets which allowed for interspecific analyses, and for intraspecific comparisons of differently structured feathers within the framework of biological scaling. We found that the cross-sectional area of the calamus (as a proxy of feather follicle size) was directly proportional to feather growth-rate by mass. Hence, factors acting at a two-dimensional scale (possibly nutrient supply to the growing feather) determines feather growth rate by mass, rather than the linear arrangement of stem cells (in a circular configuration) as had previously been assumed. Feather follicle size was correlated with both feather length and massiveness, hence it seems to be adapted to some extent to feather structure. Feather growthrate by length was dependent on both the feather material produced per unit time (growthrate by mass) and the amount of material deposited per unit feather-length. Follicle size not only determines feather growth-rate by mass, but also directly the structural design (shape, number of barbs, etc.) of a feather. Therefore, feather growth-rate is severely constrained by the requirements imposed by the structural feather design.