Published in Current Zoology, Vol. 58, Issue 5, 2012, p. 680-697 which should be used for any reference to this work 1 Referential alarm calling behaviour in New World primates Cristiane CÄSAR1,2, Klaus ZUBERBÜHLER1,3* 1 Scottish Primate Research Group, School of Psychology, University of St Andrews. St Mary’s Quad, St Andrews, Fife, Scotland, UK, KY16 9JP 2 Conservation, Ecology and Animal Behaviour Group, Department of Post-Graduate Studies in Zoology, Prédio 41, Pontifícia Universidade Católica de Minas Gerais, Av. Dom José Gaspar 500, Coração Eucarístico, 30535-610, Belo Horizonte, Minas Gerais, Brazil 3 Cognitive Science Centre, Rue Emile Argand 11, University of Neuchâtel, Neuchâtel, Switzerland Abstract There is relatively good evidence that non-human primates can communicate about objects and events in their envi- ronment in ways that allow recipients to draw inferences about the nature of the event experienced by the signaller. In some spe- cies, there is also evidence that the basic semantic units are not individual calls, but call sequences and the combinations gener- ated by them. These two findings are relevant to theories pertaining to the origins of human language because of the resemblances of these phenomena with linguistic reference and syntactic organisation. Until recently, however, most research efforts on the primate origins of human language have involved Old World species with comparatively few systematic studies on New World monkeys, which has prevented insights into the deeper phylogenetic roots and evolutionary origins of language-relevant capaci- ties. To address this, we review the older primate literature and very recent evidence for functionally referential communication and call combinations in New World primates. Within the existing literature there is ample evidence in both Callitrichids and Ce- bids for acoustically distinct call variants given to external disturbances that are accompanied by distinct behavioural responses. A general pattern is that one call type is typically produced in response to a wide range of general disturbances, often on the ground but also including inter-group encounters, while another call type is produced in response to a much narrower range of aerial threats. This pattern is already described for Old World monkeys and Prosimians, suggesting an early evolutionary origin. Second, recent work with black-fronted titi monkeys has produced evidence for different alarm call sequences consisting of acoustically distinct call types. These sequences appear to encode several aspects of the predation event simultaneously, notably predator type and location. Since meaningful call sequences have already been described in Old World primates, we suggest that basic combi- natorial vocal communication has evolved in the primate lineage long before the advent of language. Moreover, it is possible that some of these communicative abilities have evolved even earlier, or independently, as there is comparable evidence in other taxonomic groups. We discuss these findings in an attempt to shed further light on the primate stock from which human language has arisen [Current Zoology 58 (5): 680−697, 2012]. Keywords Primate alarm calls, Functionally referential calls, Call combinations, New World monkeys, Old World monkeys 1 Primate Alarm Calls colobus monkeys Colobus guereza; Schel et al., 2009), the rates of call delivery (Campbell’s monkeys; Lemas- Alarm calls are a common component of the son et al., 2010), the acoustic features and intensity of anti-predator strategies employed by many species of calls (chacma baboons Papio cynocephalus ursinus; birds and mammals. They usually function to announce Fischer et al., 2001a, b), or certain combinations of calls threats to conspecifics and to communicate directly to (putty-nosed monkey Cercopithecus nictitans martini; the predator (Caro, 2005). Multiple explanations have Arnold and Zuberbühler, 2006a, b). Many of these ut- been offered to understand the evolution and mecha- terances are elicited by specific external events, the nisms of this potentially costly behaviour (see review in ‘referents’ (e.g. eagles, leopards, snakes), and there ap- Wheeler, 2008). Some species, for instance, produce pears to be some mediation by corresponding underly- several acoustically distinct alarm calls in response to ing mental concepts (Zuberbühler et al., 1999), the ‘ref- different predator types (vervet monkeys; Seyfarth et al., erences’, a process that can take place even in the ab- 1980a, b), but in others the nature of the danger is re- sence of contextual information (Seyfarth et al., 1980; flected by the number of calls per sequence (Guereza Macedonia and Evans, 1993; Evans and Marler, 1995). 2 Another interesting phenomenon is the bewildering 2002; Fichtel and van Schaik, 2006) and Old World range of acoustic structures that serve as alarm calls. monkeys (Arnold and Zuberbühler, 2006). Table 1 pro- One relevant factor here seems to be the perceptual vides an overview of all Neotropical primates known to abilities of the predators. Marler (1955) has proposed produce at least one type of alarm call. This list is not that low-pitched, broadband calls are conspicuous and exhaustive as there are further reports of predation on easier to localise for predators than cryptic high-pitched, Neotropical primates (see for instance Boinski et al., narrowband calls. Thus, prey animals that defend them- 2000; Ferrari, 2009; Miller and Treves, 2011) and it is selves by avoiding detection are likely to produce biased towards species that have been the subject of high-pitched calls that alert others to the danger without long-term research projects (Boinski et al., 2000; Miller putting themselves at risk of detection (Wilson and Hare, and Treves, 2011). Table 1 illustrates how little is cur- 2006; Campbell and Snowdon, 2007). However, primate rently known about the type and function of alarm calls alarm calls are often conspicuously loud, especially the in Neotropical species. ones given by adult males, suggesting that they are also Aotus, for instance, was first described to possess directed at neighbouring groups or directly at the nine distinct vocalisations (Moynihan, 1964), including predator, for instance to signal detection, an adaptive generalized alarms to alert group members of danger strategy if the predator relies on surprise hunting (Wright, 1981). To our knowledge, however, no further (Zuberbühler et al., 1997; Zuberbühler, 1999a). Con- studies have been carried out to investigate these calls in spicuous calling in the presence of predators is often more detail. Chiropotes is also known to have alarm related to mobbing behaviour, a behaviour that is fairly vocalizations (Silva and Ferrari, 2008), but it is not clear common in New World monkeys (Bartecki and Hey- how these signals are deployed to predators, which is mann, 1987; Fichtel et al., 2005; Digweed et al., 2005; partially explained by the fact that this genus is one of Campbell and Snowdon, 2007; Clara et al., 2008). the most difficult primates to study (Pinto et al., in Mobbing behaviour is usually defined in terms of indi- press). Other studies have generated vocal repertoires in viduals making repeated and aggressive advances on a some species but detailed information on alarm calling predator, typically while vocalizing and displaying in a is typically missing. For captive cotton-top tamarins conspicuous manner, which appears to distract or repel Saguinus oedipus oedipus, Cleveland and Snowdon predators (e.g., Schel et al., 2010). (1982) identified eight context-specific acoustic variants Predator-specific alarm calls are well described in of ‘chirp’ calls, one of which was used during mobbing Old World monkeys (see Zuberbühler, 2009 for a re- behaviour. In a playback study, Bauers and Snowdon view), but this is not the case for New World monkeys, (1990) investigated two variants of the chirp call, one an independent radiation within the primate lineage with given to unfamiliar groups and another given during its own life history and socio-ecological characteristics within-group call exchanges, and found contextually (Strier, 2011). Therefore, discovering whether and how appropriate responses by recipients. Interestingly, the other Neotropical monkeys use vocal behaviour when chirp variant produced during mobbing behaviour was interacting with predators has implications for evolu- also uttered to preferred foods by some groups, but it is tionary theories of primate communication and under- currently not known whether listeners can discriminate lying cognitive processes. these variants. There is evidence for alarm calls in almost all New Other reports have indicated that individuals do not World monkey species that have been studied in the always produce alarm calls in response to predators, wild. However, most records are from anecdotal obser- while some calls that function in long-distance commu- vations with little or no systematic information on the nication are also given to predators, similar to what has types and function of calls and most reports are on re- been found in some African forest monkeys (e.g. Schel sponses to raptors (Digweed et al., 2005; Fichtel et al., et al., 2010; Zuberbühler et al., 1997). Alouatta’s roar- 2005; Kirchhof and Hammerschmidt, 2006; Wheeler, ing vocalizations, for instance, are used during predator 2010). Aerial alarm calls are usually very specific encounters (Eason, 1989), for example by A. palliata in (given to a few species of dangerous raptors)