Call function and meaning

Black-fronted titi monkeys (Callicebus nigrifrons) produced vocalizations in response to all predator models and to the control. All groups reliably uttered call A as a first response to the raptor (caracara) in the canopy and call B in response to all other species of predators (snakes, oncilla, puma and tayra) and to the control (deer) on the ground. In later parts of the sequence, groups produced other call types, especially in response to mammalian terrestrial predators. However, call A was never produced to any of the models presented on the ground, but only in response to the caracara in the canopy.

Vocal sequences in response to a perched caracara were composed only, or almost exclusively of call A, and monkeys usually went to a hidden place or left the area. During raptor presentations, only two individuals from two different groups approached the model after looking and calling at it for some time. It is reasonable to assume that encountering a motionless raptor represents an unusual event, while the continued lack of movement may influence the caller to approach for further inspection. This reaction was not observed in response to live raptors, possibly because monkeys can differentiate between still and moving animals. Another observation to support this interpretation comes from the two trials in which the caracara model was moved by the experimenter. In both cases, the caller, which was closest to the model, was affected by the movement and escaped quickly. The same behaviour was observed during all natural observations of raptor encounters and attacks. Listeners looked upwards and stayed still, probably in order to avoid being detected by the predator.

Vocal responses to predator models presented on or close to the ground, especially oncilla, puma and tayra, were longer and more complex than other responses. They contained several additional call types, including loud and low-pitched calls. The first caller always initiated the vocal sequence with call B, which seems to be produced primarily to inform or attract conspecifics‘ attention to a disturbance on the ground. Subsequently, the other listeners usually approached and also called towards the model. This behaviour, along with the production of loud calls, seems to be directed at the predator to inform that it has been detected (Zuberbühler et al., 1997, Zuberbühler et al., 1999ab, Clarke et al., 2006). This hypothesis is supported by the increase in production of low pitched and loud calls throughout the time and the mobbing behaviour performed towards these predator models by several individuals. Digweed et al. (2005) have suggested that capuchin alarm calls may also recruit conspecifics to mob. It seems also likely that once the group is together they try to intimidate the predator (Zuberbühler et al, 1999ab). Moreover, the use of different call variants and sometimes low-pitched calls may be important to inform group members the degree of threat they are facing. Another possible explanation for recruitment and mobbing would be an increase in the caller‘s fitness when a younger individual later recognizes a predator and alarms, thereby warning the original caller (Curio, 1978, revised in Wheeler, 2008).

Some calls produced in response to models on the ground, especially call B, are also produced in other contexts. In other studies, it has been reported that most of the major call types of C. cupreus occur in a wide range of social circumstances, including both hostile and non-hostile situations (Moynihan, 1966; Robinson, 1979a). However, it seems likely that some calls can be context-specific if the caller and listener are able to extract the relevant information from the event. For instance, some calls produced in long distance sequences consist of different vocal combinations that can have different functions if uttered separately (Marler, 1977). Robinson (1979) has also shown that in response to abnormal sequences C. cupreus produced more ―moans‖, which are uttered in more disturbing situations. During this study, I recorded subjects uttering call B while

descending or foraging near the ground, when a human (the observer) was in their way, or in response to human observers by unhabituated animals (chapter four). This suggests that this call is also triggered by non-predatory events, a pattern common in other primate species (Wheeler, 2008, Arnold and Zuberbühler, 2006a). The loud calls given only to oncilla and tayra (and puma, not analysed) were observed during duets and other loud sequences during some intergroup encounters. Whether or not these calls produced in different contexts have a different meaning will have to be tested in the future.

Although monkeys are using the same call in different contexts, it may be possible that subtle differences, in acoustic features of the same call or call variation, are sufficient to inform others about the ongoing contexts or level of threat. For instance, while coding vocal responses I noticed that monkeys often produced multiples (such as doubles and triplets) of call B in response to terrestrial predators. However, due to overlap between different callers I could not reliably code this vocal behaviour as a unique call variant, which was rare or absent during non-predatory contexts. Variation in syllable number may be associated with particular predator types (Schell et al, 2009) and/or the caller‘s risk urgency (e.g. Templeton et al 2005), which may also explain titi‘s behavioural responses after hearing the presence of a predator. In contrast, there is no evident behavioural response from the rest of the group when a caller was descending, when human observers were in its way, or when it was foraging in the lower canopy. In those cases, listeners only looked towards the caller and continued with their current activities. In some cases, for example when the caller was feeding, other group members followed the first individual and fed in the same tree or bush, usually by producing call B (cheep) and other high-pitched calls, such as whistles and food calls (C. Cäsar, personal observation). In response to a human observer, unhabituated subjects seem to produce the same call types as habituated subjects give in response to predator models on the ground. However, their vocal sequences are usually shorter and the animals retreated more quickly (Cäsar, personal observation).

Context-specific information can be also conveyed in subtypes of a general alarm call (Fichtel et al, 2005). The acoustic differences I found in call B produced in response to predators and the control (tables 5.6, 5.7 and figures 5.10, 5.12) may convey information about different types of terrestrial threats. For instance, call B with high frequency at the call end and less number of harmonics may inform of a presence of puma, while a shorter version would indicate the presence of tayra. Unfortunately, I did not measure any suitable independent variables that would allow me to address this hypothesis more systematically; and at this point my results showed no behavioural differences (e.g. all monkeys approached and mobbed) in response to puma, oncilla and tayra, even though the calls were apparently context-specific. One possibility to explain this would be that the acoustic variants within call B do not provide sufficient evidence for a communicative function. In a playback study with meerkats (Suricata suricatta), for instance, Townsend et al (2010) showed that receivers did not perceive the group signature present in their ‗close calls‘, possibly because they used other sensory systems to identify non-group members. Whether or not titi monkeys can discriminate between the acoustic differences present in their B calls is still unclear and will require further investigation. Nonetheless, the data presented here indicate that monkeys may be able to extract the meaning from the subtle differences in the acoustic structure of call B and/or by examining the behaviour of the caller (e.g. Fisher and Hammerschmidt, 2001). While still not apparent how these differences may or may not be understood by the listeners, some evidence suggests monkeys may be able to cue in one or more of these differences (e.g. during encounters with terrestrial predators monkeys approach and mob the models; during encounters with deer model, monkeys look and call while monitoring the model; and during foraging monkeys look and continue with their activities).

An important additional point is that all contexts in which B-calls were given are conceptually similar. They all relate to situations in which the caller is vulnerable to threats from the ground.