Primate Communication

http://www.nature.com/scitable/knowledge/library/primate-communication-67560503

By: Klaus Zuberbuhler (School of Psychology, University of St Andrews and Cognitive Science Centre,

Citation: Zuberbuhler, K. (2012) Primate Communication. Nature Education Knowledge 3(10):83

Why Do Primates Communicate?

Like other animals, primates communicate to satisfy their biological and social needs, such as

avoiding predators, interacting with other group members, or maintaining cohesion during travel.

To this end, they use a range of different signals, many of which have directly evolved as

ritualised abbreviations of more basic behavioural or physiological processes. For example,

chimpanzees sometimes react with pilo-erection (bristling of hair) during conflicts, which makes

them appear bigger and more dangerous and conveys their willingness to escalate (van Hooff

1973). Communication signals have thus evolved partly to be psychologically effective on

receivers (Guilford & Dawkins 1991).

Is Primate Communication More Complex Compared

to Other Groups of Animals?

Most primates live in groups in which members know each other individually and maintain

multifaceted social relations; factors which are thought to favour the evolution of advanced

communication skills (McComb & Semple 2005). However, other animals with complex social

behaviour, such as dolphins, also show sophisticated communication skills, suggesting that

complex communication is not limited to primates (Janik 2009).

Do Primates ‘Cry Wolf’?

Monkeys sometimes produce terrestrial predator alarms when competing over food, even though

no predator is around. As a result, other group members run to safety, which then gives the caller

a foraging advantage (Wheeler 2009). In general, however, primates rarely produce such

dishonest signals, or ‘cry wolf’. Why is dishonest signalling not more common? One solution has

been given by Zahavi’s (1975) ‘handicap principle’, which states that receivers will only attend to

signals that are difficult to fake by low-quality or poorly motivated individuals. It has also been

argued that, in primates, individuals know and need each other and thus gain little from

deception (Silk et al. 2000). Moreover, primates can learn to ignore unreliable signallers (Cheney

& Seyfarth 1988), suggesting that ‘reputation’ acts as a further safeguard against dishonest

signalling. Honest signalling prevails because of sceptical receivers.

Channels of Primate Communication

Primate communication takes place in all major modalities. Olfaction is one of the least

researched modalities, partly because it is difficult to measure and manipulate olfactory cues,

especially in the wild. Nevertheless, probably all primates secrete scents that influence others.

An interesting human example is women apparently influencing each other’s ovulation through

odourless cues (Stern & McClintock 1998). Another remarkable example is the ‘stink fights’ of

male ring-tailed lemurs. During conflicts, males rub their tails across their wrist and chest glands

before waving them at each other (Jolly 1966). Generally, olfactory cues play important roles in

stating claims over resources and displaying individual characteristics, such as reproductive state,

social rank, immuno-compatibility, and other genetic traits (Wedekind et al. 1995). One

difficulty with research on olfactory communication is that it is often unclear whether scent-

bearing substances are actively and strategically released into the environment, or whether they

are mere by-products of general metabolic processes. Active scent marking and self-anointment

(applying scent-bearing substances onto a substrate or body) are notable exceptions, but in many

cases it is unclear whether olfactory cues qualify as proper communication signals.

Figure 1: Gestural communication.

Gestural communication in the Sonso chimpanzee community of Budongo Forest,

Uganda. The young infant ‘Cathy’ reaches out to the older infant ‘Zak’, who interprets

and accepts this gesture as a play invitation. ‘Zak’ responds with a ‘play-face’ and both

begin to wrestle. Primate gestures have been defined as ‘discrete, mechanically

ineffective physical movements of the body observed during periods of intentional

communication’ (Hobaiter & Byrne 2011).

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In the visual domain, primates use a range of facial displays and body part movements as

communication signals, sometimes combined with tactile components. Gorilla chest beating and

Rhesus monkeys bared-teeth displays are examples of how different species express social rank

with visual signals. Current research has focused much on gestures, which are interesting

because of their partly flexible, partly species-specific use in a variety of social contexts.

Gestures have been studied mainly in great apes, where considerable variation between

individuals and groups has been found. Whether some of this variation is socially learned and

thus potentially ‘cultural’ is still an unresolved question. A more established finding is that,

during gesturing, apes take into account each other’s attention and deploy their signals

accordingly (Call & Tomasello 2007; Figure 1). Interestingly, however, there is almost no

evidence that primate gestures, or combinations thereof, carry symbolic meaning by referring to

external entities (Cartmill & Byrne 2010). Instead, they appear to function primarily to facilitate

ongoing social interactions, to bond with others, or to persuade others to behave in a desired way.

For many primates, vocalizations are the main channel of communication. Vocal repertoires tend

to be species-specific, indicating that they develop under strong genetic control. Humans also

possess a specific repertoire of such context-specific calls but, in addition, they also possess

extensive control over vocal production, an ability that develops early and is crucial for the

acquisition of speech. Such high degrees of vocal control is not seen in other primates and one

interesting hypothesis is that it is the product of relatively recent genetic changes during human

evolution (Enard et al. 2002). If this is correct then our hominid ancestors must have relied on a

primate-like communication system.

In sum, primates communicate using all major modalities. Olfactory communication is poorly

researched but is probably widespread, mostly inflexible and contextually confined to basic

biological functions. Within the visual modality, gestures are somewhat of an exception because

of their flexibility and socially targeted use. Finally, vocal communication is based on species-

specific repertoires, with some flexibility in use but little in structure.

The Origins of Syntax and Meaning

What are the evolutionary origins of syntax? A persistent claim has been that human languages

are the product of a genetically endowed, universal grammatical deep structure that — amongst

other things — enables children to acquire language without much help (Chomsky 2005).

Although extremely influential, it has been impossible to find convincing empirical support for

this idea, for example by identifying grammatical features that are shared amongst all the world’s

languages (Evans & Levinson 2009). Nevertheless, humans possess the capacity for syntactic

communication, so what are the biological roots of this ability? At a basic level, various primates

produce utterances that consist of combinations of calls that can be meaningful to others. For

example, male putty-nosed monkeys produce series of two basic loud calls to external threats,

such as eagles and leopards. In addition, males sometimes combine the two calls into a unique

sequence, which conveys its own meaning (‘move away’), regardless of the nature of the external

disturbance (Arnold & Zuberbühler 2006; Figure 2). Similarly, adult male Campbell’s monkeys

produce different loud call types, which they combine into structurally unique context-specific

sequences (Ouattara et al. 2009). Meaning at the sequence level has also been found in ape

vocalisations, including gibbons and more recently bonobos (Clay & Zuberbühler 2011),

suggesting that syntactically organised sequences are widespread in primate communication. In

contrast to human language, there is no evidence that primates use such call combinations in a

generative and creative way to ‘make infinite use of finite means’ (von Humboldt 1836).

Figure 2: Putty-nosed monkeys combine two call types.

Putty-nosed monkeys combine two call types (‘pyows’ and ‘hacks’) into meaningful

sequences. Females travelled further after hearing playbacks of ‘pyow-hack’

combinations of their own male (both real and synthetically composed) compared to his

‘pyow’ series (indicating a disturbance on the ground) or ‘hack’ series (indicating the

presence of a crowned eagle).

Another feature of human communication is that speech acts can be symbolic by referring to

both mental entities and events in the outside world. Furthermore, humans make ample use of

indexical and iconic signals, such as pointing or pantomiming, and from an early age, infants

understand that symbolic and indexical signals complement each other in their capacity to refer

to external objects (Gliga & Csibra 2009). Although laboratory research has shown that great

apes can learn a considerable number of arbitrary symbols and follow indexical signals, there is

little evidence that they use such acquired skills in creative ways or when communicating with

each other (e.g., Savage-Rumbaugh et al. 1986).

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Figure 3: Diana monkeys understand the predator-alarm calls of other monkeys.

Diana monkeys understand the predator-alarm calls of other monkeys, (within and across

species) and perceive them as representations of the corresponding predator class. Top

panel: baseline – eagle alarm calls by female Diana monkeys given in response to

playback of eagle shrieks; intermediate panel: test condition – eagle alarm calls given by

female Diana monkeys in response to a male’s eagle alarm calls followed by eagle

shrieks; bottom panel: control condition – leopard alarm calls given by female Diana

monkeys in response a male’s leopard alarm calls followed by eagle shrieks. Females

only ceased to respond to probe stimuli if they were primed with a semantically

corresponding stimulus (baseline and test conditions).

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In sum, although primates sometimes combine different call types into complex utterances that

are meaningful to others, it is still unclear how this behaviour is related to syntax in human

language. One key difference appears to be that human languages, and their grammars, are

socially learned, while there is no such evidence for primate call sequences. The difference

between human and primate communication is less obvious in the domain of call comprehension.

Both human and non-human primates extract meaning by relating arbitrary sound structures to

real-world events and their mental representations.

Do Primates Actively Inform Each Other?

Another contentious issue in the evolution of language debate is whether primates communicate

to actively inform each other. Humans tend to interpret communicative acts as an underlying

intention to be informative (Grice 1969). Thus, meaning does not solely emerge from the speech

signal, but also from the ‘common ground’ shared by the interlocutors. There is currently no

good evidence that primate communication operates this way, although some key abilities seem

to be present. For example, primates can predict the impact of their signals on others (e.g.,

Hopkins et al. 2007). Similarly, both apes and monkeys have demonstrated considerable

audience awareness that suggest that they have some understanding of the effects of their calls

and gestures (e.g., Wich & de Vries 2006, Laporte & Zuberbühler 2010, Genty et al. 2009;

Crockford et al. 2012; Figure 4).

Humans, however, go a step further, with signallers and receivers communicating in relation to

their shared intentions (Tomasello 2008). As a consequence, human communication is bi-

directional, conversational, and based on conventions as to how intentions are to be

communicated. A particularly interesting example is pointing, which emerges early and

universally during human development, with no direct equivalent in primate communication.

Although the pointing gesture has no independent meaning, it is very effective in triggering

shared attention between signallers and receivers in relation to an external referent. Apes also

produce gestures to request objects, but there is no good evidence that they point for others

solely to be informative. The degree to which primates perceive and share each other’s intentions,

and to communicate as part of this cooperative experience, is the object of much ongoing

research. Results are likely to delineate more clearly the relationship between primate

communication and human language. As such they will provide progress towards one of the

most interesting questions in science. What part of our biology is uniquely human and what is

part of our primate heritage?

Figure 4: Female chimpanzees produce copulation calls during sexual interactions

with males.

Call rates are affected by the social rank of the male partner and the composition of the

nearby audience. Both mating with low-ranking males and the presence of large female

audiences tend to inhibit copulation calls in different females.

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