Evidence for semantic communication in titi monkey alarm calls Cristiane Cäsar a, b , Richard W. Byrne a , William Hoppitt c , Robert J. Young b , Klaus Zuberbühler a, d, * a School of Psychology, University of St Andrews, St Andrews, U.K. b Department of Post-Graduate Studies in Zoology, Pontifícia Universidade Católica de Minas Gerais, Belo Horizonte, Brazil c School of Biology, University of St Andrews, St Andrews, U.K. d Institute of Biology, University of Neuchâtel, Neuchâtel, Switzerland article info Article history: Received 6 February 2012 Initial acceptance 20 March 2012 Final acceptance 25 April 2012 Available online 22 June 2012 MS. number: 12-00089 Keywords: Callicebus functional reference New World monkey playback experiment predation Black-fronted titi monkeys, Callicebus nigrifrons, produce acoustically distinct vocalizations in response to several predator species. Compared to other primates, the calls are remarkably quiet, high-pitched and structurally simple, suggesting that they may not function uniquely as predator-specific warning calls. To address this, we investigated whether conspecifics were able to respond to these calls in adaptive ways, by playing back call series originally given to a perched raptor (caracara) and terrestrial predatory mammals (oncilla and tayra). Monkeys responded strongly and in predator-specific ways. Specifically, listeners preferentially looked upwards when hearing raptor-related calls, and towards the presumed caller when hearing terrestrial predator-related calls. Locomotor responses were generally uncommon, but if they occurred then they were always in the expected direction. We concluded that black-fronted titi monkeys discriminated between calls given to different predators on the basis of their acoustic features and were able to make inferences about the type or likely location of the predator. Ó 2012 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved. Numerous animal studies have shown that vocal signals alone can be sufficient to elicit appropriate responses from listeners in the absence of the natural events that normally elicit them (Seyfarth et al. 1980a, b; Macedonia & Evans 1993; Evans & Marler 1995; Zuberbühler et al. 1997; Zuberbühler 2001; Manser et al. 2001; Templeton et al. 2005). It has become customary to refer to such signals as ‘functionally referential’, provided they are produced in context-specific ways and elicit specific adaptive responses in listeners. The use of this terminology is further sup- ported by evidence that the ‘referent’ (e.g. a predator type) may be mentally represented as a natural concept, the ‘reference’ (Ogden & Richards 1923; Seyfarth & Cheney 1980; Macedonia & Evans 1993; Zuberbühler et al. 1999). The classic example is the vervet monkey, Chlorocebus aethiops, alarm call system. In this species, individuals produce several acoustically distinct alarm calls, each tightly associated with the detection of a distinct predator type, such as a python, eagle or leopard (Struhsaker 1967). Playback experiments have demonstrated that these different alarm call types trigger specific locomotor behaviour that is generally appropriate to the hunting technique of the predator, as if the listeners had spotted the predator itself. Upon hearing an alarm call originally given to an eagle, for instance, monkeys respond by running into dense vegetation, whereas in response to calls originally given to a leopard they might climb a nearby tree (Seyfarth et al. 1980a, b). This and similar studies have caught the attention of a wider field because of the apparent parallels with symbolic reference, a key feature of human language (e.g. Seyfarth et al. 1980a). More recent examples have come from Diana monkeys, Cercopithecus diana (Zuberbühler 2000a, b), Campbell’s monkeys, Cercopithecus camp- belli (Zuberbühler 2001) and Guereza colobus monkeys, Colobus guereza (Schel et al. 2010). However, it is unlikely that functional reference is a unique feature of simian primates. Evidence for comparable phenomena has come from several other taxa, including birds (Rainey et al. 2004; Templeton et al. 2005), prairie dogs, Cynomys gunnisoni (Slobodchikoff et al. 1991), suricates, Suricata suricatta (Manser et al. 2001) and ring-tailed lemurs, Lemur catta (Macedonia 1990). Some of the nonprimate examples have matched or surpassed the primate ones in sophistication and complexity. For example, chickadees, Poecile atricapilla, and sur- icates possess systems by which referential and urgency informa- tion is combined in ways not yet described for primates (Manser et al. 2001; Templeton et al. 2005). Despite this wealth of research, evidence of functional reference is conspicuously sparse in New World monkeys, with few excep- tions. Kirchhof & Hammerschmidt (2006) found that two sympatric species of tamarins (Saguinus fuscicollis and Saguinus mystax) responded with appropriate antipredator reactions after hearing playbacks of calls originally given to aerial and terrestrial * Correspondence: K. Zuberbühler, School of Psychology, University of St Andrews, St Andrews KY16 9JP, U.K. E-mail address: kz3@st-and.ac.uk (K. Zuberbühler). Contents lists available at SciVerse ScienceDirect Animal Behaviour journal homepage: www.elsevier.com/locate/anbehav 0003-3472/$38.00 Ó 2012 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved. doi:10.1016/j.anbehav.2012.05.010 Animal Behaviour 84 (2012) 405e411