Title: Meaningful call combinations in a non-human primate
Abstract: 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 [1Eckardt W. Zuberbühler K. Cooperation and competition in two forest monkeys.Behav. Ecol. 2004; 15: 400-411Crossref Scopus (69) Google Scholar]. Series consisting of ‘pyows’ are a common response to leopards, while ‘hacks’ or ‘hacks’ followed by ‘pyows’ are regularly given to crowned eagles [2Arnold K. Zuberbühler K. The alarm-calling system of adult male putty-nosed monkeys, Cercopithecus nictitans martini.Anim. Behav. 2006; 72: 643-653Crossref Scopus (85) Google Scholar, 3Arnold K. Pohlner Y. Zuberbühler K. A forest monkey's alarm call series to predator models.Behav. Ecol. Sociobiol. 2008; 62: 549-559Crossref Scopus (52) Google Scholar]. 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 [4Arnold K. Zuberbühler K. Language evolution: semantic combinations in primate calls.Nature. 2006; 441: 303Crossref PubMed Scopus (215) Google Scholar]. 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 [5Catchpole C.K. Slater P.J.B. Bird Song: Biological Themes and Variations. Cambridge Univ. Press, Cambridge1995Google Scholar, 6Zuberbühler K. Referential signaling in non-human primates: Cognitive precursors and limitations for the evolution of language.Adv. Study Behav. 2003; 33: 265-307Crossref Scopus (76) Google Scholar], and this constraint may have favored the evolution of such combinatorial signaling.