Populations of independently oscillating agents can sometimes synchronize. In the context of animal societies, conspicuous synchronization of activity is known in some social insects. However, the causes of variation in synchrony within and between species have received little attention. We repeatedly assessed the short-term activity cycle of ant colonies (Temnothorax rugatulus) and monitored the movements of individual workers and queens within nests. We detected persistent differences between colonies in the waveform properties of their collective activity oscillations, with some colonies consistently oscillating much more erratically than others. We further demonstrate that colony crowding reduces the rhythmicity (i.e., the consistent timing) of oscillations. Workers in both erratic and rhythmic colonies spend less time active than completely isolated workers, but workers in erratic colonies oscillate out of phase with one another. We further show that the queen's absence can impair the ability of colonies to synchronize worker activity and that behavioral differences between queens are linked with the waveform properties of their societies.