In contrast to human phonation, the virtuoso vocalizations of most birds are modulated at the level of the sound generator, the syrinx. We address the hypothesis that syringeal muscles are physiologically capable of controlling the sound-generating syringeal membranes in the ring dove (Streptopelia risoria) syrinx. We establish the role of the tracheolateralis muscle and propose a new function for the sternotrachealis muscle. The tracheolateralis and sternotrachealis muscles have an antagonistic mechanical effect on the syringeal aperture. Here, we show that both syringeal muscles can dynamically control the full syringeal aperture. The tracheolateralis muscle is thought to directly alter position and tension of the vibrating syringeal membranes that determine the gating and the frequency of sound elements. Our measurements of the muscle's contractile properties, combined with existing electromyographic and endoscopic evidence, establish its modulating role during the dove's trill. The muscle delivers the highest power output at cycle frequencies that closely match the repetition rates of the fastest sound elements in the coo. We show that the two syringeal muscles share nearly identical contraction characteristics, and that sternotrachealis activity does not clearly modulate during the rapid trill. We propose that the sternotrachealis muscle acts as a damper that stabilizes longitudinal movements of the sound-generating system induced by tracheolateralis muscle contraction. The extreme performance of both syringeal muscles implies that they play an important role in fine-tuning membrane position and tension, which determines the quality of the sound for a conspecific mate.