Individual recognition is critical in social animal communication, but it has not been demonstrated for a complete vocal repertoire. Deciphering the nature of individual signatures across call types is necessary to understand how animals solve the problem of combining, in the same signal, information about identity and behavioral state. We show that distinct signatures differentiate zebra finch individuals for each call type. The distinctiveness of these signatures varies: contact calls bear strong individual signatures while calls used during aggressive encounters are less individualized. We propose that the costly solution of using multiple signatures evolved because of the limitations of the passive filtering properties of the birds' vocal organ for generating sufficiently individualized features. Thus, individual recognition requires the memorization of multiple signatures for the entire repertoire of conspecifics of interests. We show that zebra finches excel at these tasks.