http://www.nature.com/scitable/knowledge/library/primate-communication-67560503
Primate Communication
By: Klaus Zuberbuhler (School of Psychology, University of St Andrews and Cognitive Science Centre,
University of Neuchatel) © 2012 Nature Education
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).
© 2012 Nature Education Courtesy of C. Hobaiter. All rights reserved.
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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).
© 2012 Nature Education Data from Arnold & Zuberbühler (2008). All rights reserved.
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).
© 2012 Nature Education Data from Zuberbühler et al. (1999). All rights reserved.
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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.
© 2012 Nature Education Data from Townsend et al. (2008). All rights reserved.
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References and Recommended Reading
Arnold, K. & Zuberbühler, K. Language evolution: Semantic combinations in primate calls.
Nature 441, 303 (2006).
———— Meaningful call combinations in a non-human primate. Current Biology 18, R202-
R203 (2008).
Call, J. & Tomasello, M. eds. The Gestural Communication of Apes and Monkeys. Mahwah, NJ
and London, UK: Lawrence Erlbaum Associates, 2007.
Cartmill, E. A. & Byrne, R. W. Semantics of primate gestures: Intentional meanings of
orangutan gestures. Animal Cognition 13, 793-804 (2010).
Cheney, D. L. & Seyfarth, R. M. Assessment of meaning and the detection of unreliable signals
by vervet monkeys. Animal Behaviour 36, 477-486 (1988).
Chomsky, N. Three factors in language design. Linguistic Inquiry 36, 1-22 (2005).
Clay, Z. & Zuberbühler, K. Bonobos extract meaning from call sequences. PLoS ONE 6, e18786
(2010).
Crockford, C. et al.. Wild chimpanzees inform ignorant group members of danger. Current
Biology 22, 142-146 (2012).
Enard, W. et al. Molecular evolution of FOXP2, a gene involved in speech and language. Nature
418, 869-872 (2002).
Evans, N. & Levinson, S. C. The myth of language universals: Language diversity and its
importance for cognitive science. Behavioral and Brain Sciences 32, 429-448 (2009).
Genty, E. et al. Gestural communication of the gorilla (Gorilla gorilla): Repertoire, intentionality
and possible origins. Animal Cognition 12, 527-546 (2009).
Gliga, T. & Csibra, G. One-year-old infants appreciate the referential nature of deictic gestures
and words. Psychological Science 20, 347-353 (2009).
Grice, H. P. Utterers’ meaning and intentions. Philosophical Review 78, 147-177 (1969).
Guilford, T. & Dawkins, M. S. Receiver psychology and the evolution of animal signals. Animal
Behaviour 42, 1-14 (1991).
Hobaiter, C. & Byrne, R. W. The gestural repertoire of the wild chimpanzee. Animal Cognition
14, 745-767 (2011).
Janik, V. M. Acoustic communication in delphinids. Advances in the Study of Behavior 40, 123-
157 (2009).
Jolly, A. Lemur social behavior and primate intelligence. Science 153, 501-506 (1966).
Laporte, M. N. C. & Zuberbühler, K. Vocal greeting behaviour in wild chimpanzee females.
Animal Behaviour 80, 467-473 (2010).
McComb, K. & Semple, S. Coevolution of vocal communication and sociality in primates.
Biology Letters 1, 381-385 (2005).
Ouattara, K., Lemasson, A. & Zuberbühler, K. Campbell’s monkeys concatenate vocalizations
into context-specific call sequences. Proceedings of the National Academy of Sciences of the
United States of America 106, 22026-22031 (2009).
Savage-Rumbaugh, S. et al. Spontaneous symbol acquisition and communicative use by pygmy
chimpanzees (Pan paniscus). Journal of Experimental Psychology: General 115, 211-235 (1986).
Seyfarth, R. M., Cheney, D. L. & Marler, P. Monkey responses to three different alarm calls:
Evidence of predator classification and semantic communication. Science 210, 801-803 (1980).
Silk, J. B., Kaldor, E. & Boyd, R. Cheap talk when interests conflict. Animal Behaviour 59, 423-
432 (2000).
Stern, K. & McClintock, M. K. Regulation of ovulation by human pheromones. Nature 392, 177-
179 (1998).
Tomasello, M. Origins of Human Communication. Cambridge, MA: MIT Press, 2008.
Townsend, S. W., Deschner, T. & Zuberbühler, K. Female chimpanzees use copulation calls
flexibly to prevent social competition. PLoS ONE 3, e2431 (2008).
van Hooff, J. “A structural analysis of the social behavior of a semi-captive group of
chimpanzees” in Social Communication and Movement: Studies of Interaction and Expression in
Man and Chimpanzee, eds. M. von Cranach & I. Vine (London, UK: Academic Press, 1973) 75-
162.
von Humboldt, K. W. Über die Verschiedenheit des menschlichen Sprachbaues und ihren
Einfluss auf die geistige Entwickelung des Menschengeschlechts. Berlin, Germany: Druckerei
der Königlichen Akademie der Wissenschaften, 1836/1935.
Wedekind, C. et al. MHC-dependent mate preferences in humans. Proceedings of the Royal
Society B: Biological Sciences 260, 245-249 (1995).
Wheeler, B. C. Monkeys crying wolf? Tufted capuchin monkeys use anti-predator calls to usurp
resources from conspecifics. Proceedings of the Royal Society B: Biological Sciences 276, 3013-
3018 (2009).
Wich, S. A. & de Vries, H. Male monkeys remember which group members have given alarm
calls. Proceedings of the Royal Society B: Biological Sciences 273, 735-740 (2006).
Zahavi, A. Mate selection: A selection for a handicap. Journal of Theoretical Biology 53, 205-
214 (1975).
Zuberbühler, K., Cheney, D. L. & Seyfarth, R. M. Conceptual semantics in a nonhuman primate.
Journal of Comparative Psychology 113, 33-42 (1999).
