Meaningful call combinations in a non-human primate

Human speech is based on rule-governed assemblage of morphemes into more complex vocal expressions. Free-ranging putty-nosed monkeys (Cercopithecus nictitans) provide an interesting analogy, because males combine two loud alarm calls, ‘hacks’ and ‘pyows’, into different call series depending on external events [1]. Series consisting of ‘pyows’ are a common response to leopards, while ‘hacks’ or ‘hacks’ followed by ‘pyows’ are regularly given to crowned eagles [2,3]. Sometimes, males produce a further sequence, consisting of 1–4 ‘pyows’ followed by 1–4 ‘hacks’. These ‘pyow–hack’ (P–H) sequences can occur alone, or they are inserted at or near the beginning of another call series. Regardless of context, P–H sequences reliably predict forthcoming group progression [4]. In playback experiments, we tested the monkeys' reactions to ‘pyows’, ‘hacks’ and P–H sequences and found that responses matched the natural conditions. Specifically, females started group progressions after hearing P–H sequences and responded appropriately to the other call series. In a second experiment, we tested artificially composed P–H sequences, and found that they were also effective in eliciting group progressions. In a third experiment, we established that group movement could only be triggered by the calls of the group's own male, not those of a stranger. We conclude that, in this primate, meaning is encoded by call sequences, not individual calls. Many birds and primates are limited by small vocal repertoires [5,6], and this constraint may have favored the evolution of such combinatorial signaling