Vocal Communication in Primates
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Vocal Communication in Primates
KATIE E. SLOCOMBE
Abstract
Vocal communication is common in the animal kingdom. Researchers often examine
vocal communication in nonhuman primates (primates) with the aim of identifying similarities and differences with human language and speech, in order to trace
the evolutionary origins of our complex communication system. Primates can produce distinct calls in response to specific events, such as the discovery of a certain
predator, and listeners seem to understand what these calls refer to. Although on
the surface there are similarities between this type of communication and human
referential words, the mental processes that underlie them may be very different.
While in general the flexibility shown by primate receivers may demonstrate some
commonalities with humans, there is much more controversy over whether there
are similarities between the production of primate vocalizations and language. It is
widely accepted that primates, unlike humans, lack the ability to generate new vocalizations. Although this means primates have a closed repertoire of calls that cannot
be expanded, primates are capable of combining their existing calls to generate new
messages. The degree of voluntary control and intentionality involved in the use of
calls is also a matter of debate, with recent evidence on both a neural and behavioral
level challenging traditional assumptions that primate vocalizations are used in an
automatic, reflexive manner. More research is needed to examine the mental processes underlying communicative behavior in both the producer and the receiver.
In the future adopting a more holistic, multimodal approach to studying primate
communication is likely to challenge and ultimately improve our understanding of
primate communication and the evolution of human language.
INTRODUCTION
Vocal communication is widespread across the animal kingdom and it has
been well studied in a number of different species. The foci of such research
has been wide ranging, but when studying our closest living relatives, the
nonhuman primates (primates), much research has focussed on identifying
similarities and differences between primate vocal communication and
human language and speech. Such comparative research often aims to help
us trace the phylogenetic history of human communicative abilities and
to further our understanding of how human language may have evolved.
Emerging Trends in the Social and Behavioral Sciences. Edited by Robert Scott and Stephen Kosslyn.
© 2015 John Wiley & Sons, Inc. ISBN 978-1-118-90077-2.
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EMERGING TRENDS IN THE SOCIAL AND BEHAVIORAL SCIENCES
The basic logic underlying this approach is that we can try and identify (i)
elements of language that are shared with other primates and thus likely
evolved in our ancient past, and (ii) elements of language that are uniquely
human and thus likely evolved recently and that may represent the crucial
elements that allowed our communication system to become so complex
and powerful.
While primates, including humans, communicate using vocal, gestural and
facial signals, vocalizations have traditionally been studied in isolation from
other modalities. The vocal modality has been the most extensively studied
in primates (Slocombe, Waller, & Liebal, 2011), and there may be several reasons for this. First, as human language is predominantly expressed through
speech, vocalizations may have been the natural place to start to look for
similarities between communication systems. Second, there are established
methods for identifying, categorzing and analysing vocal behavior from the
perspective of both the producer and the receiver: aspects that are much less
established for gestures for instance. Lastly, given the visually dense habitat
that many primates naturally inhabit, vocalizations seem to be the primary
mode of communication in many species.
This review will examine some key similarities and differences that have
been highlighted between aspects of primate vocal communication and
human language, before outlining some recent cutting edge research which
might challenging these traditional views.
FOUNDATIONAL AND CUTTING EDGE WORK
Researchers have identified several important similarities and differences
between primate vocal communication and features of speech and language.
Perhaps the most famous finding arose from the seminal work of Robert Seyfarth and Dorothy Cheney on vervet monkey alarm calls. Vervet monkeys
face a range of predatory threats and they were observed to produce acoustically different alarm calls to different types of predator (Struhsaker, 1967).
Seyfarth, Cheney, and Marler (1980) built on these observations to show that
listening monkeys acted as if they understood the meaning of the calls. Vervet
monkeys react in qualitatively different ways to their main predators (eagles,
leopards and pythons) and playback experiments showed that monkeys produced the appropriate anti-predator response when a group member’s alarm
call was broadcast: the same response they would give if encountering the
actual predator. Since this seminal work, further examples of alarm call systems that seem to refer to different predators have been found and evidence
that food-associated calls provide listeners with information about the presence or quality of food has been generated (e.g., Hauser, 1998; Slocombe and
Zuberbühler, 2005; Zuberbühler, 2000). Indeed, playback experiments have
Vocal Communication in Primates
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revealed that receivers are highly adept at extracting information about many
aspects of their physical and social world from not only the calls of their own
group members (Pfefferle, Heistermann, Hodges, & Fischer, 2008; Slocombe,
Kaller, Call, & Zuberbühler, 2010), but also those of other species (Seyfarth &
Cheney, 1990; Zuberbühler 2002).
Initially the alarm and food calls that provided listeners with information
about external events were heralded as semantic and referential in similar
way to human words and were seen as an important source of continuity
between human and primate communication. There has since, however, been
the realization that although these systems may appear similar on the surface,
the cognitive mechanisms that underlie them may be very different (Macedonia & Evans, 1993; Rendall, Owren, & Ryan, 2009; Seyfarth & Cheney, 2003;
Wheeler & Fischer, 2012). While human words are produced intentionally
to inform others about events in the world, with both signaller and receiver
sharing the concept associated with the word, this is not necessarily the case
in monkeys. For instance, it could be that monkey alarm calls are a product of
simple stimulus—response mechanisms, and that listeners have learnt to use
these calls as reliable predictors of specific predators and as such are extracting information from calls that the caller may have never intended to provide
(Seyfarth & Cheney, 2003). This highlights the importance of understanding
the proximate mechanism driving a behavior—be it arousal, innate, or learnt
stimulus–response mechanisms, emotional processes, voluntary control and
an intention to change the behavior of another or an intention to change the
mental states of another. Without probing the similarity of the mental processes that produce the behaviors, we may erroneously identify primate traits
as homologous to human traits, when it is in reality two very different mental
processes producing similar surface behavior.
Following the seminal work on referential alarm calls, there has been a
strong focus in vocal research on understanding the informational content of
vocal signals and playback techniques are perfectly designed for pursuing
this line of enquiry. This has lead to a historical emphasis on context-specific
vocalizations, while more flexible signals, that are given in a variety of
contexts and therefore require the receiver to integrate the signal with other
contextual information, may have been overlooked (Wheeler & Fischer,
2012). Such flexible signals have been readily identified in great ape gestural
communication (Tomasello, 2008) and are argued to be more cognitively
demanding on the receiver than signals with a one-to-one mapping between
signal and event. Greater parallels are also drawn between such flexible
communication and human language, which can be highly ambiguous and
requires the receiver to integrate utterances with other contextual knowledge
in order to fully understand the meaning (Carston, 2002). In contrast to
gestures, there are comparatively few studies that focus on vocal signals
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EMERGING TRENDS IN THE SOCIAL AND BEHAVIORAL SCIENCES
being given in a flexible manner across contexts. However, the current lack of
evidence for this kind of vocal communication may well reflect the relative
absence of research effort in this area, rather than a genuine absence of
ability for this type of communication (Liebal, Waller, Burrows, & Slocombe,
2013; Slocombe et al., 2011). Indeed many alarm call systems are relatively
nonspecific and given in response to a variety of events and innovative
experimental field research by Kate Arnold and colleagues has investigated
the processes underlying the interpretation of these more ambiguous calls
by receivers. They have shown that female putty-nosed monkeys integrate
information from different sources to infer the likely cause of a male’s alarm
calls, enabling them to react appropriately to these ambiguous calls (Arnold
& Zuberbühler, 2013). Further research examining the pragmatic strategies
receivers implement to understand flexibly produced calls and the cognitive
processes underlying this behavior could reveal more similarities between
human and primate communication.
One well-established and important difference between primate and
human vocal communication is the ability to generate new vocalizations.
Speech relies on the human ability to generate and imitate new vocalizations,
however, other primates seem to have little or no capacity to generate new
calls. Although reports of whistling orangutans and raspberry blowing
chimpanzees (Hopkins, Taglialatela, & Leavens, 2007; Wich et al., 2009),
have shown that primates can invent new sounds, comparable evidence of
generating new vocalizations that engage the larynx is lacking. Primates, in
contrast to humans, have a relatively limited, genetically determined vocal
repertoire, where the structure and range of calls an individual can produce
is relatively impervious to experience and learning: species typical calls
are produced by monkeys reared in acoustic isolation (Winter, Handley,
Ploog, & Schott, 1973) and cross fostering experiments have shown that
infant macaque monkeys produce calls more similar to their genetic rather
than adoptive parental species (Owren, Dieter, Seyfarth, & Cheney, 1993).
The fine control over orofacial muscles that humans possess that is vital
for the production of the variety of sounds required for speech has been
linked to a certain variant of the FOXP2 gene. Comparative research has
shown that while primates have a highly conserved version of the gene,
humans have a different variant of this gene that stabilized in the human
population relatively recently in our evolutionary past (Enard et al., 2002).
Wider comparative work examining the function of vocal plasticity that is
evident in more distantly related species, such as parrots, passerine birds
and cetaceans (Janik & Slater, 1997) may be enable us to understand the
evolutionary pressures that may have made the recent evolution of vocal
plasticity in humans an adaptive trait.
Vocal Communication in Primates
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The inability of primates to expand their vocal repertoire has lead to
assumptions that primates have a finite number of “messages” that they
can convey and that this limited, closed system is qualitatively different
to the open generative human language system. However, the generative
power of human language does not just derive from our ability to generate
new words: We are able to express an infinite number of messages through
the recombination of words into different utterances (Pinker, 1994). Do
we see any evidence of anything similar in primates? While gibbons are
capable of singing elaborately structured songs (Geissmann, 2002), the
relation between the meaning of individual song elements and sequences of
elements is unknown. More recent work by Arnold and Zuberbühler (2006)
has, however, identified a simple combinatorial system in the forest dwelling
Putty-nosed monkeys. Male Putty-nosed monkeys produce two loud calls,
pyows and hacks, with hacks given primarily as alarm calls to eagles and
pyows given as more general alarm calls to a range of disturbances, including leopards. They also combined these calls into a pyow–hack sequence
which careful observational and experimental work has shown initiates
travel in the group, in contexts unrelated to predation. Thus this simple
combination of meaningful calls allows more messages to be conveyed,
within the constraints of a system where new calls cannot be generated.
More recent observational work has shown Campbell monkeys produce a
number of different call combinations in context-specific ways (Ouattara,
Lemasson, & Zuberbühler, 2009), and this may represent a more complex
combinatorial communication system, however experiments demonstrating
that listeners extract different meanings from these different combinations
are still required.
Although many studies of primate vocal communication aim to elucidate
the cognition underlying communication, comparably few studies have
succeeded in probing the proximate mechanisms underlying the observable
behavior. While playback experiments have proved powerful tools to investigate aspects of monkey cognition, such as understanding of hierarchical
relationships (e.g., Bergman, Beehner, Cheney, & Seyfarth, 2003), relatively
few studies have focussed on understanding the mental processes that
underlie natural communication events. Zuberbühler, Cheney, and Seyfarth
(1999) sought to do exactly this by using a prime-probe experiment to examine the processes underling receiver responses to predator-specific alarm
calls. They tested whether receivers responded to specific acoustic features
of the calls in a relatively inflexible manner or whether their responses were
more likely mediated by some kind of mental representation. Their findings
indicated that Diana monkeys seemed to process the meaning of the sounds
they heard, rather than responding directly to the low level acoustic features
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EMERGING TRENDS IN THE SOCIAL AND BEHAVIORAL SCIENCES
of the sounds they heard, demonstrating an important aspect of continuity
with humans.
In contrast to the cognitive processes identified in call receivers, the
production of vocalizations has traditionally been attributed to emotional
processes. Neurological studies revealed that in squirrel monkeys call
production was triggered by the activity of subcortical brain areas including
the limbic system (Jürgens, 1979) and there was no evidence of the direct
connection between cortical motor areas and the larynx that characterizes
humans. Although some primates have been successfully conditioned to
produce vocalizations in response to arbitrary stimuli (Pierce, 1985), this
often takes a considerable number of trials, indicating it is not an easy
task for them to master. These classic studies have lead to prominent
researchers, such as Michael Tomasello describing primate vocal production
as automatic, unintentional and reflexive and as such it has been viewed as
cognitively uninteresting and very different from human language. More
recent, cutting edge research has, however, challenged this view.
From a neurological perspective, advances in technology have meant
that the brain areas involved in vocal and gestural production in our
closest living relative, the chimpanzee have now been examined and they
seem very different from the results obtained from monkeys. Using PET
scanners, Taglialatela, Russell, Schaeffer, and Hopkins (2011) have been able
to determine that the homologue to Broca’s area, that is critical for language
production in humans, is active during the production of vocal and gestural
signals. Although this cortical activity was present in chimpanzees who
produced both vocal and gestural signals, it was absent in chimpanzees who
just produced gestures, indicating that this cortical activation is critically
associated with the production of vocal signals. The vocal signals studied
here were “attention-getting” signals that have been reported to be novel
signals invented in captivity to communicate with human experimenters
(Hopkins, Taglialatela, & Leavens, 2007). The extent to which these signals
engage the larynx is, however, currently unclear. If these imaging techniques
can also be used to examine the neural areas underlying the production of
species-typical vocalizations that do engage the larynx, it will greatly inform
our understanding of the neural mechanisms involved in vocal production
in our closest relatives: whether we will see more commonalities between the
neural processes in chimpanzees and humans, or chimpanzees and monkeys
is an open question and the answer will have important consequences for
our understanding of how speech and language might have evolved.
From a behavioral perspective, observational studies have shown that
primates are capable of adjusting their vocal production according not only
to the presence of an audience, but the presence of certain individuals. For
instance, vervet monkeys are more likely to alarm call when kin are present
Vocal Communication in Primates
7
(Cheney & Seyfarth, 1990a) and female chimpanzees suppress copulation
calls when in the presence of high ranking females (Townsend, Deschner,
& Zuberbühler, 2008). Recent field experiments have shown that wild male
chimpanzees who are feeding silently on their own will start producing
food calls if a playback simulates the arrival of an individual who is more
dominant and a friend to the feeding male (Schel, Machanda, Townsend,
Zuberbühler, & Slocombe, 2013a). These studies indicate that calls are not
automatic and can be directed at specific individuals, but there is still debate
as to the proximate mechanisms underlying such audience effects. While
they might be indicative of voluntary control, other lower level explanations
based on associative learning and emotional or arousal processes have also
been offered, particularly for the more basic presence/absence audience
effects (Hurford, 2007; Liebal et al., 2013). Anne Marijke Schel and Katie
Slocombe have recently lead a team to rigorously test whether wild chimpanzee alarm call production is intentional (voluntary and goal-directed),
using several established criteria for intentional signal production. These
criteria of social use, gaze alternation and persistence have been extensively
used to identify intentional gesture production in human infants and great
apes, but had never previously been applied to a vocal communication
system. Chimpanzees were presented with a moving python model and two
types of alarm calls met these hallmarks of intentional communicative acts.
These calls were more likely to be given in response to the arrival of friends
rather than nonfriends irrespective of their rank, calls were accompanied
by gaze alternation between the snake and recipient and callers persisted in
vocalizing until all group members were aware of or safe from this ambush
predator (Schel, Townsend, Machanda, Zuberbühler, & Slocombe, 2013b).
There are alternative explanations that do not invoke intentional processes,
for each of these individual criteria, however, obtaining convergent evidence
from multiple criteria provides more robust evidence that these calls may be
produced intentionally (Liebal et al., 2013).
Although chimpanzees may produce some calls intentionally, whether they
are capable of vocalizing with the goal of manipulating others mental states
is an important and open question. While monkeys have failed to inform
ignorant offspring about food or predators (Cheney & Seyfarth, 1990b), chimpanzees have been shown to understand knowledge/ignorance states outside communicative contexts (Hare, Call, & Tomasello, 2001; Kaminski, Call,
& Tomasello, 2008). One recent field experiment aimed to test if chimpanzees
alarm called at a static model snake to warn ignorant, rather than knowledgeable individuals of the danger (Crockford, Wittig, Mundry, & Zuberbühler,
2012). Although callers did call more in the presence of individuals presumed
to be ignorant rather than knowledgeable, in this field setting the researchers
were unable to rigorously rule out the influence of other factors on calling,
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EMERGING TRENDS IN THE SOCIAL AND BEHAVIORAL SCIENCES
such as the caller’s own previous knowledge of the snake and the behavior,
rather than the mental state, of receivers.
To summarize, traditional views of primate vocal usage being inflexible, reflexive and driven by emotional rather than cognitive processes
(Tomasello, 2008) are being undermined by cutting edge neurological
and behavioral research. Neuroimaging techniques have revealed cortical
involvement in the vocal production of our closest living relative and behavioral research has found that vocal production is mediated by complex social
factors and that chimpanzees can produce calls intentionally, potentially to
inform others of external events.
KEY ISSUES FOR FUTURE RESEARCH
While vocalizations are a key mode of communication for many animals,
including primates, studying them in isolation may ultimately limit our
understanding of communication. Communication in primates, including
humans, is inherently multimodal, with gestural, olfactory, facial and
vocal signals frequently being combined (Liebal et al., 2013). Removing
vocalizations from composite multimodal signals to study them in isolation
may lead us to incorrect or incomplete understanding of the signal function
and the proximate mechanisms underlying it. Currently many cross-modal
comparisons are made, particularly between primate gestures and vocalizations, but the different methods, approaches, settings and assumptions that
underpin research in different modalities means that these comparisons are
likely invalid and many of our characterizations of vocal and gestural signals
may be inaccurate (Liebal et al., 2013; Slocombe et al., 2011). Thus it is critical
in the future that there is better integration between researchers focussing
on different modalities and where possible a more holistic approach to
communication is taken and integrated multimodal research is conducted.
More research is also needed to understand the cognitive processes underlying primate communication. When studying our closest living relatives
it is often easy to attribute complex mental processes to the communicative behaviours we observe, without explicitly testing those assumptions.
We need to design rigorous, ecologically valid experiments to directly test the
proximate mechanisms involved and we must actively test alternative explanations. Broader comparative work that identifies communicative behaviour
in less intelligent, distantly related species that is similar to that found in primates (e.g., Scott-Phillips, 2014) is particularly valuable for highlighting the
need for directly testing the complexity of cognitive processes underlying
primate communication. Similar behaviors can be generated by very different proximate mechanisms and so when searching for homologous traits that
Vocal Communication in Primates
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may have acted as precursors to human language, it is vital we are identifying
behaviors that are similar on both the behavioral and cognitive level.
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Wheeler, B. C., & Fischer, J. (2012). Functionally referential signals: A promising
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FURTHER READING
Arnold, K., & Zuberbühler, K. (2006). Language evolution: Semantic combinations
in primate calls. Nature, 441(7091), 303–303.
Cheney, D. L., & Seyfarth, R. M. (1990). How monkeys see the world: Inside the mind of
another species. Chicago, IL: University of Chicago Press.
Fedurek, P., & Slocombe, K. E. (2011). Primate vocal communication: A useful tool
for understanding human speech and language evolution? Human Biology, 83(2),
153–174.
Liebal, K., Waller, B., Burrows, A., & Slocombe, K. E. (2013). Primate communication:
A multimodal approach. Cambridge, England: Cambridge University Press.
Taglialatela, J. P., Russell, J. L., Schaeffer, J. A., & Hopkins, W. D. (2011). Chimpanzee
vocal signaling points to a multimodal origin of human language. PLoS One, 6(4),
e18852.
Zuberbühler, K., Cheney, D. L., & Seyfarth, R. M. (1999). Conceptual semantics in a
nonhuman primate. Journal of Comparative Psychology, 113(1), 33.
KATIE E. SLOCOMBE SHORT BIOGRAPHY
Katie E. Slocombe: I gained a first class BSc in Psychology from the University of Nottingham before joining the Psychology department at the
University of St Andrews as a PhD student in 2002. I worked under the
supervision of Professor Klaus Zuberbühler to study chimpanzee vocal
communication and completed fieldwork in Uganda and captive work at
Edinburgh Zoo. I continued my research work with wild and captive chimpanzees as a post-doctoral researcher before obtaining a faculty position at
the Psychology department at the University of York in 2007. I now lead
a research group examining animal communication and cognition, with
research projects ranging from multimodal communication in chimpanzees
to prosocial behavior in parrots.
http://www.york.ac.uk/psychology/staff/faculty/ks553/
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The Sexual Division of Labor (Anthropology), Rebecca Bliege Bird and Brian
F. Codding
Language, Perspective, and Memory (Psychology), Rachel A. Ryskin et al.
Sexual Behavior (Anthropology), Melissa Emery Thompson
Language and Thought (Psychology), Susan Goldin-Meadow
Food Sharing (Anthropology), Michael Gurven and Adrian V. Jaeggi
Reconciliation and Peace-Making: Insights from Studies on Nonhuman
Animals (Anthropology), Sonja E. Koski
Culture, Diffusion, and Networks in Social Animals (Anthropology), Janet
Mann and Lisa Singh
Evolutionary Perspectives on Animal and Human Personality (Anthropology), Joseph H. Manson and Lynn A. Fairbanks
Gestural Communication in Nonhuman Species (Anthropology), Simone Pika
Class, Cognition, and Face-to-Face Interaction (Sociology), Lauren A. Rivera
Speech Perception (Psychology), Athena Vouloumanos
Behavioral Heterochrony (Anthropology), Victoria Wobber and Brian Hare
-
Vocal Communication in Primates
KATIE E. SLOCOMBE
Abstract
Vocal communication is common in the animal kingdom. Researchers often examine
vocal communication in nonhuman primates (primates) with the aim of identifying similarities and differences with human language and speech, in order to trace
the evolutionary origins of our complex communication system. Primates can produce distinct calls in response to specific events, such as the discovery of a certain
predator, and listeners seem to understand what these calls refer to. Although on
the surface there are similarities between this type of communication and human
referential words, the mental processes that underlie them may be very different.
While in general the flexibility shown by primate receivers may demonstrate some
commonalities with humans, there is much more controversy over whether there
are similarities between the production of primate vocalizations and language. It is
widely accepted that primates, unlike humans, lack the ability to generate new vocalizations. Although this means primates have a closed repertoire of calls that cannot
be expanded, primates are capable of combining their existing calls to generate new
messages. The degree of voluntary control and intentionality involved in the use of
calls is also a matter of debate, with recent evidence on both a neural and behavioral
level challenging traditional assumptions that primate vocalizations are used in an
automatic, reflexive manner. More research is needed to examine the mental processes underlying communicative behavior in both the producer and the receiver.
In the future adopting a more holistic, multimodal approach to studying primate
communication is likely to challenge and ultimately improve our understanding of
primate communication and the evolution of human language.
INTRODUCTION
Vocal communication is widespread across the animal kingdom and it has
been well studied in a number of different species. The foci of such research
has been wide ranging, but when studying our closest living relatives, the
nonhuman primates (primates), much research has focussed on identifying
similarities and differences between primate vocal communication and
human language and speech. Such comparative research often aims to help
us trace the phylogenetic history of human communicative abilities and
to further our understanding of how human language may have evolved.
Emerging Trends in the Social and Behavioral Sciences. Edited by Robert Scott and Stephen Kosslyn.
© 2015 John Wiley & Sons, Inc. ISBN 978-1-118-90077-2.
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EMERGING TRENDS IN THE SOCIAL AND BEHAVIORAL SCIENCES
The basic logic underlying this approach is that we can try and identify (i)
elements of language that are shared with other primates and thus likely
evolved in our ancient past, and (ii) elements of language that are uniquely
human and thus likely evolved recently and that may represent the crucial
elements that allowed our communication system to become so complex
and powerful.
While primates, including humans, communicate using vocal, gestural and
facial signals, vocalizations have traditionally been studied in isolation from
other modalities. The vocal modality has been the most extensively studied
in primates (Slocombe, Waller, & Liebal, 2011), and there may be several reasons for this. First, as human language is predominantly expressed through
speech, vocalizations may have been the natural place to start to look for
similarities between communication systems. Second, there are established
methods for identifying, categorzing and analysing vocal behavior from the
perspective of both the producer and the receiver: aspects that are much less
established for gestures for instance. Lastly, given the visually dense habitat
that many primates naturally inhabit, vocalizations seem to be the primary
mode of communication in many species.
This review will examine some key similarities and differences that have
been highlighted between aspects of primate vocal communication and
human language, before outlining some recent cutting edge research which
might challenging these traditional views.
FOUNDATIONAL AND CUTTING EDGE WORK
Researchers have identified several important similarities and differences
between primate vocal communication and features of speech and language.
Perhaps the most famous finding arose from the seminal work of Robert Seyfarth and Dorothy Cheney on vervet monkey alarm calls. Vervet monkeys
face a range of predatory threats and they were observed to produce acoustically different alarm calls to different types of predator (Struhsaker, 1967).
Seyfarth, Cheney, and Marler (1980) built on these observations to show that
listening monkeys acted as if they understood the meaning of the calls. Vervet
monkeys react in qualitatively different ways to their main predators (eagles,
leopards and pythons) and playback experiments showed that monkeys produced the appropriate anti-predator response when a group member’s alarm
call was broadcast: the same response they would give if encountering the
actual predator. Since this seminal work, further examples of alarm call systems that seem to refer to different predators have been found and evidence
that food-associated calls provide listeners with information about the presence or quality of food has been generated (e.g., Hauser, 1998; Slocombe and
Zuberbühler, 2005; Zuberbühler, 2000). Indeed, playback experiments have
Vocal Communication in Primates
3
revealed that receivers are highly adept at extracting information about many
aspects of their physical and social world from not only the calls of their own
group members (Pfefferle, Heistermann, Hodges, & Fischer, 2008; Slocombe,
Kaller, Call, & Zuberbühler, 2010), but also those of other species (Seyfarth &
Cheney, 1990; Zuberbühler 2002).
Initially the alarm and food calls that provided listeners with information
about external events were heralded as semantic and referential in similar
way to human words and were seen as an important source of continuity
between human and primate communication. There has since, however, been
the realization that although these systems may appear similar on the surface,
the cognitive mechanisms that underlie them may be very different (Macedonia & Evans, 1993; Rendall, Owren, & Ryan, 2009; Seyfarth & Cheney, 2003;
Wheeler & Fischer, 2012). While human words are produced intentionally
to inform others about events in the world, with both signaller and receiver
sharing the concept associated with the word, this is not necessarily the case
in monkeys. For instance, it could be that monkey alarm calls are a product of
simple stimulus—response mechanisms, and that listeners have learnt to use
these calls as reliable predictors of specific predators and as such are extracting information from calls that the caller may have never intended to provide
(Seyfarth & Cheney, 2003). This highlights the importance of understanding
the proximate mechanism driving a behavior—be it arousal, innate, or learnt
stimulus–response mechanisms, emotional processes, voluntary control and
an intention to change the behavior of another or an intention to change the
mental states of another. Without probing the similarity of the mental processes that produce the behaviors, we may erroneously identify primate traits
as homologous to human traits, when it is in reality two very different mental
processes producing similar surface behavior.
Following the seminal work on referential alarm calls, there has been a
strong focus in vocal research on understanding the informational content of
vocal signals and playback techniques are perfectly designed for pursuing
this line of enquiry. This has lead to a historical emphasis on context-specific
vocalizations, while more flexible signals, that are given in a variety of
contexts and therefore require the receiver to integrate the signal with other
contextual information, may have been overlooked (Wheeler & Fischer,
2012). Such flexible signals have been readily identified in great ape gestural
communication (Tomasello, 2008) and are argued to be more cognitively
demanding on the receiver than signals with a one-to-one mapping between
signal and event. Greater parallels are also drawn between such flexible
communication and human language, which can be highly ambiguous and
requires the receiver to integrate utterances with other contextual knowledge
in order to fully understand the meaning (Carston, 2002). In contrast to
gestures, there are comparatively few studies that focus on vocal signals
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EMERGING TRENDS IN THE SOCIAL AND BEHAVIORAL SCIENCES
being given in a flexible manner across contexts. However, the current lack of
evidence for this kind of vocal communication may well reflect the relative
absence of research effort in this area, rather than a genuine absence of
ability for this type of communication (Liebal, Waller, Burrows, & Slocombe,
2013; Slocombe et al., 2011). Indeed many alarm call systems are relatively
nonspecific and given in response to a variety of events and innovative
experimental field research by Kate Arnold and colleagues has investigated
the processes underlying the interpretation of these more ambiguous calls
by receivers. They have shown that female putty-nosed monkeys integrate
information from different sources to infer the likely cause of a male’s alarm
calls, enabling them to react appropriately to these ambiguous calls (Arnold
& Zuberbühler, 2013). Further research examining the pragmatic strategies
receivers implement to understand flexibly produced calls and the cognitive
processes underlying this behavior could reveal more similarities between
human and primate communication.
One well-established and important difference between primate and
human vocal communication is the ability to generate new vocalizations.
Speech relies on the human ability to generate and imitate new vocalizations,
however, other primates seem to have little or no capacity to generate new
calls. Although reports of whistling orangutans and raspberry blowing
chimpanzees (Hopkins, Taglialatela, & Leavens, 2007; Wich et al., 2009),
have shown that primates can invent new sounds, comparable evidence of
generating new vocalizations that engage the larynx is lacking. Primates, in
contrast to humans, have a relatively limited, genetically determined vocal
repertoire, where the structure and range of calls an individual can produce
is relatively impervious to experience and learning: species typical calls
are produced by monkeys reared in acoustic isolation (Winter, Handley,
Ploog, & Schott, 1973) and cross fostering experiments have shown that
infant macaque monkeys produce calls more similar to their genetic rather
than adoptive parental species (Owren, Dieter, Seyfarth, & Cheney, 1993).
The fine control over orofacial muscles that humans possess that is vital
for the production of the variety of sounds required for speech has been
linked to a certain variant of the FOXP2 gene. Comparative research has
shown that while primates have a highly conserved version of the gene,
humans have a different variant of this gene that stabilized in the human
population relatively recently in our evolutionary past (Enard et al., 2002).
Wider comparative work examining the function of vocal plasticity that is
evident in more distantly related species, such as parrots, passerine birds
and cetaceans (Janik & Slater, 1997) may be enable us to understand the
evolutionary pressures that may have made the recent evolution of vocal
plasticity in humans an adaptive trait.
Vocal Communication in Primates
5
The inability of primates to expand their vocal repertoire has lead to
assumptions that primates have a finite number of “messages” that they
can convey and that this limited, closed system is qualitatively different
to the open generative human language system. However, the generative
power of human language does not just derive from our ability to generate
new words: We are able to express an infinite number of messages through
the recombination of words into different utterances (Pinker, 1994). Do
we see any evidence of anything similar in primates? While gibbons are
capable of singing elaborately structured songs (Geissmann, 2002), the
relation between the meaning of individual song elements and sequences of
elements is unknown. More recent work by Arnold and Zuberbühler (2006)
has, however, identified a simple combinatorial system in the forest dwelling
Putty-nosed monkeys. Male Putty-nosed monkeys produce two loud calls,
pyows and hacks, with hacks given primarily as alarm calls to eagles and
pyows given as more general alarm calls to a range of disturbances, including leopards. They also combined these calls into a pyow–hack sequence
which careful observational and experimental work has shown initiates
travel in the group, in contexts unrelated to predation. Thus this simple
combination of meaningful calls allows more messages to be conveyed,
within the constraints of a system where new calls cannot be generated.
More recent observational work has shown Campbell monkeys produce a
number of different call combinations in context-specific ways (Ouattara,
Lemasson, & Zuberbühler, 2009), and this may represent a more complex
combinatorial communication system, however experiments demonstrating
that listeners extract different meanings from these different combinations
are still required.
Although many studies of primate vocal communication aim to elucidate
the cognition underlying communication, comparably few studies have
succeeded in probing the proximate mechanisms underlying the observable
behavior. While playback experiments have proved powerful tools to investigate aspects of monkey cognition, such as understanding of hierarchical
relationships (e.g., Bergman, Beehner, Cheney, & Seyfarth, 2003), relatively
few studies have focussed on understanding the mental processes that
underlie natural communication events. Zuberbühler, Cheney, and Seyfarth
(1999) sought to do exactly this by using a prime-probe experiment to examine the processes underling receiver responses to predator-specific alarm
calls. They tested whether receivers responded to specific acoustic features
of the calls in a relatively inflexible manner or whether their responses were
more likely mediated by some kind of mental representation. Their findings
indicated that Diana monkeys seemed to process the meaning of the sounds
they heard, rather than responding directly to the low level acoustic features
6
EMERGING TRENDS IN THE SOCIAL AND BEHAVIORAL SCIENCES
of the sounds they heard, demonstrating an important aspect of continuity
with humans.
In contrast to the cognitive processes identified in call receivers, the
production of vocalizations has traditionally been attributed to emotional
processes. Neurological studies revealed that in squirrel monkeys call
production was triggered by the activity of subcortical brain areas including
the limbic system (Jürgens, 1979) and there was no evidence of the direct
connection between cortical motor areas and the larynx that characterizes
humans. Although some primates have been successfully conditioned to
produce vocalizations in response to arbitrary stimuli (Pierce, 1985), this
often takes a considerable number of trials, indicating it is not an easy
task for them to master. These classic studies have lead to prominent
researchers, such as Michael Tomasello describing primate vocal production
as automatic, unintentional and reflexive and as such it has been viewed as
cognitively uninteresting and very different from human language. More
recent, cutting edge research has, however, challenged this view.
From a neurological perspective, advances in technology have meant
that the brain areas involved in vocal and gestural production in our
closest living relative, the chimpanzee have now been examined and they
seem very different from the results obtained from monkeys. Using PET
scanners, Taglialatela, Russell, Schaeffer, and Hopkins (2011) have been able
to determine that the homologue to Broca’s area, that is critical for language
production in humans, is active during the production of vocal and gestural
signals. Although this cortical activity was present in chimpanzees who
produced both vocal and gestural signals, it was absent in chimpanzees who
just produced gestures, indicating that this cortical activation is critically
associated with the production of vocal signals. The vocal signals studied
here were “attention-getting” signals that have been reported to be novel
signals invented in captivity to communicate with human experimenters
(Hopkins, Taglialatela, & Leavens, 2007). The extent to which these signals
engage the larynx is, however, currently unclear. If these imaging techniques
can also be used to examine the neural areas underlying the production of
species-typical vocalizations that do engage the larynx, it will greatly inform
our understanding of the neural mechanisms involved in vocal production
in our closest relatives: whether we will see more commonalities between the
neural processes in chimpanzees and humans, or chimpanzees and monkeys
is an open question and the answer will have important consequences for
our understanding of how speech and language might have evolved.
From a behavioral perspective, observational studies have shown that
primates are capable of adjusting their vocal production according not only
to the presence of an audience, but the presence of certain individuals. For
instance, vervet monkeys are more likely to alarm call when kin are present
Vocal Communication in Primates
7
(Cheney & Seyfarth, 1990a) and female chimpanzees suppress copulation
calls when in the presence of high ranking females (Townsend, Deschner,
& Zuberbühler, 2008). Recent field experiments have shown that wild male
chimpanzees who are feeding silently on their own will start producing
food calls if a playback simulates the arrival of an individual who is more
dominant and a friend to the feeding male (Schel, Machanda, Townsend,
Zuberbühler, & Slocombe, 2013a). These studies indicate that calls are not
automatic and can be directed at specific individuals, but there is still debate
as to the proximate mechanisms underlying such audience effects. While
they might be indicative of voluntary control, other lower level explanations
based on associative learning and emotional or arousal processes have also
been offered, particularly for the more basic presence/absence audience
effects (Hurford, 2007; Liebal et al., 2013). Anne Marijke Schel and Katie
Slocombe have recently lead a team to rigorously test whether wild chimpanzee alarm call production is intentional (voluntary and goal-directed),
using several established criteria for intentional signal production. These
criteria of social use, gaze alternation and persistence have been extensively
used to identify intentional gesture production in human infants and great
apes, but had never previously been applied to a vocal communication
system. Chimpanzees were presented with a moving python model and two
types of alarm calls met these hallmarks of intentional communicative acts.
These calls were more likely to be given in response to the arrival of friends
rather than nonfriends irrespective of their rank, calls were accompanied
by gaze alternation between the snake and recipient and callers persisted in
vocalizing until all group members were aware of or safe from this ambush
predator (Schel, Townsend, Machanda, Zuberbühler, & Slocombe, 2013b).
There are alternative explanations that do not invoke intentional processes,
for each of these individual criteria, however, obtaining convergent evidence
from multiple criteria provides more robust evidence that these calls may be
produced intentionally (Liebal et al., 2013).
Although chimpanzees may produce some calls intentionally, whether they
are capable of vocalizing with the goal of manipulating others mental states
is an important and open question. While monkeys have failed to inform
ignorant offspring about food or predators (Cheney & Seyfarth, 1990b), chimpanzees have been shown to understand knowledge/ignorance states outside communicative contexts (Hare, Call, & Tomasello, 2001; Kaminski, Call,
& Tomasello, 2008). One recent field experiment aimed to test if chimpanzees
alarm called at a static model snake to warn ignorant, rather than knowledgeable individuals of the danger (Crockford, Wittig, Mundry, & Zuberbühler,
2012). Although callers did call more in the presence of individuals presumed
to be ignorant rather than knowledgeable, in this field setting the researchers
were unable to rigorously rule out the influence of other factors on calling,
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EMERGING TRENDS IN THE SOCIAL AND BEHAVIORAL SCIENCES
such as the caller’s own previous knowledge of the snake and the behavior,
rather than the mental state, of receivers.
To summarize, traditional views of primate vocal usage being inflexible, reflexive and driven by emotional rather than cognitive processes
(Tomasello, 2008) are being undermined by cutting edge neurological
and behavioral research. Neuroimaging techniques have revealed cortical
involvement in the vocal production of our closest living relative and behavioral research has found that vocal production is mediated by complex social
factors and that chimpanzees can produce calls intentionally, potentially to
inform others of external events.
KEY ISSUES FOR FUTURE RESEARCH
While vocalizations are a key mode of communication for many animals,
including primates, studying them in isolation may ultimately limit our
understanding of communication. Communication in primates, including
humans, is inherently multimodal, with gestural, olfactory, facial and
vocal signals frequently being combined (Liebal et al., 2013). Removing
vocalizations from composite multimodal signals to study them in isolation
may lead us to incorrect or incomplete understanding of the signal function
and the proximate mechanisms underlying it. Currently many cross-modal
comparisons are made, particularly between primate gestures and vocalizations, but the different methods, approaches, settings and assumptions that
underpin research in different modalities means that these comparisons are
likely invalid and many of our characterizations of vocal and gestural signals
may be inaccurate (Liebal et al., 2013; Slocombe et al., 2011). Thus it is critical
in the future that there is better integration between researchers focussing
on different modalities and where possible a more holistic approach to
communication is taken and integrated multimodal research is conducted.
More research is also needed to understand the cognitive processes underlying primate communication. When studying our closest living relatives
it is often easy to attribute complex mental processes to the communicative behaviours we observe, without explicitly testing those assumptions.
We need to design rigorous, ecologically valid experiments to directly test the
proximate mechanisms involved and we must actively test alternative explanations. Broader comparative work that identifies communicative behaviour
in less intelligent, distantly related species that is similar to that found in primates (e.g., Scott-Phillips, 2014) is particularly valuable for highlighting the
need for directly testing the complexity of cognitive processes underlying
primate communication. Similar behaviors can be generated by very different proximate mechanisms and so when searching for homologous traits that
Vocal Communication in Primates
9
may have acted as precursors to human language, it is vital we are identifying
behaviors that are similar on both the behavioral and cognitive level.
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Wheeler, B. C., & Fischer, J. (2012). Functionally referential signals: A promising
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FURTHER READING
Arnold, K., & Zuberbühler, K. (2006). Language evolution: Semantic combinations
in primate calls. Nature, 441(7091), 303–303.
Cheney, D. L., & Seyfarth, R. M. (1990). How monkeys see the world: Inside the mind of
another species. Chicago, IL: University of Chicago Press.
Fedurek, P., & Slocombe, K. E. (2011). Primate vocal communication: A useful tool
for understanding human speech and language evolution? Human Biology, 83(2),
153–174.
Liebal, K., Waller, B., Burrows, A., & Slocombe, K. E. (2013). Primate communication:
A multimodal approach. Cambridge, England: Cambridge University Press.
Taglialatela, J. P., Russell, J. L., Schaeffer, J. A., & Hopkins, W. D. (2011). Chimpanzee
vocal signaling points to a multimodal origin of human language. PLoS One, 6(4),
e18852.
Zuberbühler, K., Cheney, D. L., & Seyfarth, R. M. (1999). Conceptual semantics in a
nonhuman primate. Journal of Comparative Psychology, 113(1), 33.
KATIE E. SLOCOMBE SHORT BIOGRAPHY
Katie E. Slocombe: I gained a first class BSc in Psychology from the University of Nottingham before joining the Psychology department at the
University of St Andrews as a PhD student in 2002. I worked under the
supervision of Professor Klaus Zuberbühler to study chimpanzee vocal
communication and completed fieldwork in Uganda and captive work at
Edinburgh Zoo. I continued my research work with wild and captive chimpanzees as a post-doctoral researcher before obtaining a faculty position at
the Psychology department at the University of York in 2007. I now lead
a research group examining animal communication and cognition, with
research projects ranging from multimodal communication in chimpanzees
to prosocial behavior in parrots.
http://www.york.ac.uk/psychology/staff/faculty/ks553/
12
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