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Primate Vocal Communication: A Useful Tool forUnderstanding Human Speech and Language Evolution?

PAWEL FEDUREK1

AND KATIE E. SLOCOMBE1

Abstract Language is a uniquely human trait, and questions of how and

why it evolved have been intriguing scientists for years. Nonhuman primates

(primates) are our closest living relatives, and their behavior can be used to

estimate the capacities of our extinct ancestors. As humans and many

primate species rely on vocalizations as their primary mode of communica-

tion, the vocal behavior of primates has been an obvious target for studies

investigating the evolutionary roots of human speech and language. By

studying the similarities and differences between human and primate

vocalizations, comparative research has the potential to clarify the evolu-

tionary processes that shaped human speech and language. This review

examines some of the seminal and recent studies that contribute to our

knowledge regarding the link between primate calls and human language and

speech. We focus on three main aspects of primate vocal behavior:

functional reference, call combinations, and vocal learning. Studies in these

areas indicate that despite important differences, primate vocal communica-

tion exhibits some key features characterizing human language. They alsoindicate, however, that some critical aspects of speech, such as vocal

plasticity, are not shared with our primate cousins. We conclude that

comparative research on primate vocal behavior is a very promising tool for

deepening our understanding of the evolution of human speech and lan-

guage, but much is still to be done as many aspects of monkey and ape

vocalizations remain largely unexplored.

Tools for Tackling Language and Speech Evolution

Language is an exceedingly complex and intricate behavior and is one ofthe capacities that appears to distinguish humans from the rest of the living

world. Language enables humans to represent and communicate complex

abstract information, and it occurs in verbal, gestural, and written forms. An

evolutionary account for this capacity remains elusive, but this issue is the focus

of interdisciplinary research effort. One premise is that many of the cognitive

capacities involved in language processing are much older than language itself,

1

Department of Psychology, University of York, YO10 5DD York, United Kingdom.

Human Biology, April 2011, v. 83, no. 2, pp. 153173.

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with their phylogenetic roots deep in the primate lineage (Hauser et al. 2002).

Thus, a promising empirical approach to understanding the origins of language

is to apply a comparative approach (Hauser et al. 2002). In particular, by

examining the capacities of extant primates, whose phylogenetic relationships to

modern humans are known, we can draw inferences about the likely capacities of

our extinct ancestors. Specifically, by investigating primate behavior it is

possible to test the hypothesis that human language built on abilities already

present in the primate lineage before the advent of modern humans. This

comparative approach is vital for identifying the homologous, shared elements of

language which appear to have evolved gradually from a common primate

ancestor and those which have no clear evolutionary path and thus may be the

novel elements which were instrumental to human language evolving into its

current uniquely complex state (Hauser et al. 2002). In addition, comparative

research can allow researchers to develop and test hypotheses concerning the

evolutionary pressures that may have driven the selection of traits required for

language.

Whilst the capacity for language is independent of modality of production

and perception, speech is the pervasive and most prevalent way of conveying

language in modern humans. Speech, which relies on the vocalauditory channel,

is characterized by voluntary control and is a culturally shared system for

communicating within a population. Speech is also combinatorial, with pho-

nemes and syllables being combined to form words and phrases. Humans seem

to have several adaptations for speech production and perception, including those

related to the structure of the vocal tract and neural mechanisms in the brain

(Fitch 2000; Pinker 1994). Understanding how these adaptations evolved is

central to our understanding of how language evolved into its current speech-

dominated form. Although no other primate is equipped with speech apparatus as

sophisticated as the one found in humans, comparative data from nonhuman

primates have been central to furthering our understanding of speech evolution

(Fitch 2000; Ghazanfar and Hauser 1999; Riede et al. 2005).

Why Vocalizations?

To investigate the evolution of human speech from a comparative

perspective it is necessary to focus on the vocalauditory channel of communi-

cation in other species, including primates (Ghazanfar and Hauser 1999). As the

capacity for language is independent of modality, research into any modality of

communication in other species could further our understanding of language

evolution: so what contribution can primate vocalizations make?

Vocalizations are an important mode of communication for most primates,as in general they are well suited to both their social and physical environments.

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not be visible. Empirically more research has been conducted on vocal behavior

than any other type of communication in primates (Slocombe et al. in press) and

researchers are well equipped to conduct meaningful research into vocalizations

and their cognitive underpinnings because of the techniques and methods that can

be applied to vocal behavior. Detailed acoustic analysis of calls in combination

with observational data allow us to examine the production of calls in great

detail, and experimental playback techniques crucially allow us to create and test

precise hypotheses regarding listener understanding of vocal signals. In contrast

to other modalities, both observational and experimental vocal techniques can be

conducted in the wild, meaning that many primate vocal communication studies

have high ecological validity.

It is important to highlight that facial expressions, body postures, manual

gestures, and olfaction also play important roles in primate communication and

communicative signals are often composites of two or more of these different

modalities. In this way focusing exclusively on vocal communication is telling

only part of the story, but unfortunately it is out of the scope of this review to

cover the other modalities and multimodal signals and how they also make a

valuable contribution to our understanding of language evolution.

Comparative data on primate gestural and vocal communication are often

used to argue whether the origin of human language was vocal or gestural (Arbib

2008; Hewes 1973; Riede et al. 2005; Tomasello 2008; Zuberbuhler 2005). Both

modalities demonstrate some aspects of continuity with language, with great ape

gestures being learnt, generative and intentional signals (Tomasello 2008) and

monkey vocalizations functioning referentially and being combined into se-

quences (Zuberbuhler 2005). Although data on vocal and gestural competencies

are important for furthering this debate, currently we do not have comparable

data in the two modalities to make very meaningful comparisons (Slocombe et al.

in press). For example most gestural data are collected from great apes, whereas

most vocal data are collected from monkeys: any conclusions of the relative

merits of one modality over the other are confounded by systematic differences

in the study species, study environment (wild/captive), and focus of the research.

Although vocalizations are central to arguments over the origin of language and this

is another example of how primate vocalizations can make a strong contribution to

debates surrounding language evolution, it is not the focus of this review.

Precursors to Human Language and Speech?

Primate vocalizations can be useful tools in examining many different

questions within the language evolution debate, including the evolutionary

pressures that may have led to more complex communication and the modalityin which human language arose (vocal vs. gestural). They can also help us

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manner, but we focus on two key cognitive components of language where there

has been substantial and important evidence collected from primates: we will

examine evidence for potential precursors to human reference and basic

combinatorial rules. In addition, we will examine vocal learning to illustrate how

primate vocalizations can contribute to our understanding of speech evolution

and how discontinuities between primates and humans are just as valuable in

developing our understanding as evidence for continuities. It is important to note

here that the aim of this paper is to provide a review of seminal and recent

literature in relation to the topics outlined above, to illustrate the value and

relevance of primate vocalizations to the debate surrounding language evolution,

rather than to offer new insights or hypotheses regarding the reviewed topic.

Given that recent works have questioned the utility of primate vocalizations for

furthering our understanding of language evolution (e.g., Arbib 2008; Tomasello

2008), we believe this review is important for highlighting the contribution

primate vocal behavior can make to the interdisciplinary research effort focused

on language evolution.

Functional Reference

Human language is highly efficient at conveying meaningful messages

between communicators. Semantics plays a crucial role in this, as human words,

phrases, and sentences all carry meaning. Within the field of semantics, many

human words and phrases are referential, in that they refer to an external object

or event in the world. The specificity of reference varies greatly in human

language from utterances with many possible referents (mammal) to highly

specific utterances (my dog). Comparative researchers have identified a process

within animal vocal communication that shares some of the features of this

human system, and may represent an important precursor to human linguistic

abilities. In animals this ability to produce calls that function to convey a

message to conspecifics about an object or event in the external world has been

termed functionally referential communication.

Evidence for Functional Reference in Primates. The seminal study of

functional reference examined the alarm calls of vervet monkeys. Strushaker

(1967) first reported that vervet monkeys produce three acoustically distinct

alarm calls when encountering with their three main predators: leopards, eagles,

and snakes. Seyfarth et al. (1980) then conducted a playback experiment to

examine whether these calls were meaningful to listeners, in the sense that these

three calls represented different classes of predators. The results of the play-back

experiment demonstrated that listeners responded in exactly the same, adaptivemanner to playbacks of conspecific alarm calls as they did when they encoun-

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repertoire and produced consistently in response to a specific external stimulus.

Second, from the receivers perspective, the receiver must react to the call in the

same way as it would react toward the stimulus itself, in the absence of any other

information indicating the presence of the stimulus that elicited the call (Marler

et al. 1992).

Since the famous study on vervet monkeys, functionally referential alarm

calls have been found in a number of other primate species, such as Diana

monkeys (Zuberbuhler et al. 1997), Campbell monkeys (Zuberbuhler 2001),

putty-nosed monkeys (Arnold and Zuberbuhler 2006b), tamarins (Kirchhof and

Hammerschmidt 2006), and ring-tailed lemurs (Macedonia 1990). The specific-

ity of the alarm calling system varies, with some systems that seem to convey

information about the presence of an aerial or terrestrial threat (Macedonia and

Stanger 1994; Oda and Masataka 1996) and other systems being specific to types

of predator, regardless of the location of the predator. For instance the playback

of predator stimuli from different elevations and distances confirmed that

regardless of the urgency to respond or the trajectory of an imminent attack Diana

monkeys did not deviate from labeling the type of predator with their alarm calls

(Zuberbuhler 2000b). It has been suggested that the specificity of alarm calls

in these animals results from differences in the nature of escape responses

that are required to avoid different types of predatory threat (Macedonia

1990). Selection pressures seem to have favored the evolution of acousticallyspecific calls that generate specific responses in the receivers, if differential

anti-predator responses increase fitness (Donaldson et al. 2007; Macedonia

1990; Pereira and Macedonia 1991).

It is not only in urgent predator avoidance contexts that functional

reference has been found. Primates also produce functionally referential calls in

response to food. Again there is variation in the specificity of these calls, with

tufted capuchin monkeys producing calls that simply alert listeners to the

presence of food in the environment (Di Bitetti 1993) and other species

producing vocalizations that seem to provide listeners with information about thenature of the discovered food source. Rhesus macaques give different calls to

high and low value food items (Hauser and Marler 1993) and a habituation-

dishabituation experiment showed that listeners behaved as if they extracted

meaning about the value of the food source from these calls (Hauser 1998). More

recently chimpanzees have been shown to produce acoustically distinct calls to

foods of different values, and in captivity this system even extends to specific call

variants being produced in response to different high value food items (bread,

mango, banana) that remain stable over feeding events (Slocombe and Zuber-

buhler 2006). A playback study showed that listeners can extract informationabout quality of food from the calls of group members (Slocombe and

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1993], cotton-top tamarins [Roush and Snowdon 2000], white-faced capuchins

[Gros-Louis 2003], bonobos [Clay and Zuberbuhler 2009], marmosets [Kitzmann

and Caine 2009]) or quantity (red bellied tamarins [Caine et al. 1995]). Such

context-specific calling is necessary for a functionally referential system, but

listener understanding (i.e., whether listeners act as if they extract information

about the external event from the call) must be systematically tested before calls

can be shown to function referentially.

The complexity of social relationships within primate groups suggests that

functional reference may also occur in a variety of other social situations. In

social situations distinct behavioral responses to different contexts are rare and

the more subtle responses of listeners are often measured by differences in

looking duration / latency to look at the speaker. Although this shows the

primates distinguish between the calls, it is harder to infer what meaning they

extracted from it.

In the social sphere, female Barbary macaques produce acoustically

different calls during copulations depending on whether the male has ejaculated

or not (Pfefferle et al. 2008a). The facts that the call begins well before

ejaculation and that the frequencies of call production correlate with ejaculation

rates suggests that these calls are signals directed to the mating partner so as to

increase the probability of ejaculation (Pfefferle et al. 2008a). Recent playbacks

have shown that listening males can distinguish between these calls and adjusttheir behavior toward the female (such as walking toward the female or the time

spent in her vicinity) according to whether she has just had a successful mating

with another male (Pfefferle et al. 2008b). It is therefore possible that these calls

also function to provide male listeners with information about whether the

female is likely to conceive to increase the likelihood of subsequent mating

(Pfefferle et al. 2008b).

Primates often vocalize whilst involved in agonistic interactions, and

rhesus macaque monkeys give different screams in response to differing levels of

aggression from opponents of different ranks. A playback experiment showedthat mothers were able to meaningfully distinguish (i.e., they responded to these

calls as if they extracted some information about the ongoing fight from these

vocalizations) between scream variants given by offspring (Gouzoules et al.

1984). More recently chimpanzees have been shown to produce acoustically

distinct screams depending on their social role in the interaction (victim or

aggressor; [Slocombe and Zuberbuhler 2005a]). A playback study has shown that

listeners were able to infer the respective roles and the subsequent direction of

aggression between two screaming individuals from these calls (Slocombe et al.

2010a). Listeners were thus able to distinguish between sequences of calls thatsimulated agonistic interactions which were either incongruous or congruous

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conducted in the wild demonstrated that listeners distinguished between these

screams (Slocombe et al. 2009). Listeners showed significantly more interest in

screams given in response to severe aggression than mild aggression. These

responses were not driven by low level responses to the acoustic structure of the

different screams, as listeners did not show comparable interest in control

tantrum screams, which matched the severe screams in acoustic structure.

Evidence for Functional Reference in Non-Primate Species. Functional

reference has also been demonstrated in a wide variety of nonprimate species.

For instance, chickens produce functionally referential food calls (Evans and

Marler 1994) and alarm calls that function to refer to aerial and terrestrial

predatory threats (Evans et al. 1993). Meerkats also produce alarm calls that not

only function to denote predator type but also the urgency of response (Manser

2001; Manser et al. 2002). Although the surface behavior of these diverse species

is similar, there is some evidence that primates seem to process these calls in a

relatively sophisticated way. For instance, experiments with wild Diana monkeys

indicated that listeners attended to the meaning of the call rather than the surface

acoustics and likely form some kind of mental representation when hearing a call

(Zuberbuhler et al. 1999). This study showed that upon hearing a sound

indicating the presence of a specific predator, such as leopard growls, Diana

monkeys respond much less intensively if they had been primed by a conspe-cifics leopard alarm call (Zuberbuhler et al. 1999). The leopard growls and the

leopard alarm call are two acoustically different sounds, suggesting that the

monkeys were habituating not to the low level acoustic structure of the stimuli

but to the referent of the sounds. Unfortunately, comparable experiments

probing the mechanisms underlying functionally referential signals in nonpri-

mates have not been reported, so it is difficult to conclude how the presence of

similar behavior in nonprimate species should affect our interpretation of the data

in relation to humans. It is likely, however, that similar evolutionary pressures

have lead to the emergence of this kind of signaling in divergent species. Furtherinvestigation of functional reference in other nonprimate species may further

shed light on the selection pressures that favor its emergence and clarify

similarities and differences in the psychological underpinnings of this behavior in

different species.

Human Language and Functional Reference. The studies of functionally

referential calls indicate some continuity between primate and human commu-

nication. However, it is important to highlight some crucial differences between

functional reference in animals and reference in humans. First, the referentialcharacter of human language is arbitrary in the sense that humans flexibly attach

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mechanisms underlying communication are similar. This is partly because of a

paucity of research tools we have available to examine the cognitive machinery

involved in nonhuman animal vocal communication (Cheney and Seyfarth 1990).

As outlined above, there is some evidence that some primate listeners may form

some kind of mental representation when hearing functionally referential calls

(e.g., Zuberbuhler et al. 1999). However, it is very difficult to examine the nature

of any mental representation held by a primate. For instance, when a vervet

monkey responds appropriately to a leopard alarm call, it is impossible to tell

whether the calls evoke a declarative representation of a leopard in the mind of

the listener or whether they interpret the call as an imperative such as climb the

tree. Although we sometimes use such metaphors as information, message,

and meaningful, we might never be sure exactly what happens in the listeners

mind. Furthermore, the involvement of such mental representations may not be

required to produce and respond appropriately to referential signals, and more

simple mechanisms may account for these effects (Hauser et al. 2002; Owren and

Rendall 2001; Seyfarth et al. 2010). Parsimony is strength in science for a good

reason: simple mechanisms are more likely to evolve, and therefore we should

first explore the simplest possible explanations for any behavior, including

functionally referential calls, before reaching for more elaborated ones. It is for

these reasons that the term functionally referential communication refers to the

way signals are used and the way responses are generated, but not in any senseto the cognitive mechanisms that are involved (Marler et al. 1992; Owren and

Rendall 2001).

The cognitive mechanisms involved in primate vocal behavior remains a

contentious issue and a topic of considerable recent debate. Rendall et al. (2009),

for example, challenged the view that the concept of information is needed to

explain any aspect of vocal communication in nonhuman animals. Their key

argument is that the mechanisms involved in primate communication differ from

those characterizing human language mainly as a result of the cognitive

limitation of these animals. The authors claim that nonhuman animals are notcapable of intentional communication and perspective-taking and consequently

advocate abandoning any language-like expressions such as information

when dealing with primate vocalizations. In contrast, Seyfarth et al. (2010) claim

that the term information applies simply to the process of reducing uncertainty

by learning associations between one stimulus (such as a vocal signal) and

another (such as the presence of a predator), rather than to the elaborate process

of encoding and decoding of ideas that occurs in human language. The process

of making associations between calls and objects or events in external world is

favored by natural selection as it allows animals predict accurately critical eventsin the environment. The fact that this process is rather simple has prompted some

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The role of receivers in animal communication has also been extensively

discussed. Rendall et al. (2009) suggest that primate vocalizations function to

manipulate the behaviors of receivers through the direct induction of their

nervous systems. Rendall et al. (2009) along with Owren et al. (in press)

characterize listeners as passive receivers and reject the notion that receivers

extract and infer information from calls in any way similar to human language

processing. Seyfarth et al. (2010) criticize this approach, suggesting that it

focuses too heavily on the interests of senders while neglecting the interests of

receivers in animal communication. The evolution of communicative signals

requires the interplay of signalers and receivers, as signals can be ignored by the

receivers if they are costly or fail to provide benefits (Searcy and Nowicki 2005;

Zahavi and Zahavi 1997). Therefore, the receivers are not prisoners of the

manipulative tactics used by the senders (Seyfarth et al. 2010) and rather play an

active role in communication and the evolution of signals.

Mechanisms Underlying Call Production. Although there are many areas of

disagreement regarding animal communication, there does seem to be a general

agreement that the motivations and mechanisms that drive call production in

primates likely differ from those involved in human language. Human language

is generally characterized by the producer intending to convey a message to the

receiver, but to date we have no evidence to suggest that such intentionalcommunication exists in monkeys. Indeed, in the case of baboon contact barks,

although calls are exchanged between individuals, it was found that call

production was contingent on the callers themselves being at the periphery of the

group, rather than a reflection of a motivation to provide an informative reply to

other lost individuals (Cheney et al. 1996). It is argued that the ability to

distinguish between others and own knowledge is a key prerequisite for such

informative and intentional communication (Grice 1957), and given the generally

poor performance of monkey species on theory of mind (i.e., the ability to

attribute mental stages to others) tests (Heyes 1998; Povinelli et al. 1991), thistype of communication may be impossible. This view is supported by a study in

which rhesus monkey mothers were given the opportunity to inform ignorant

offspring about food, or a danger in the environment, and they failed to do so

(Cheney and Seyfarth 1990).

Great apes, in contrast to monkeys, produce manual gestures that show

some hallmarks of intentionality (Leavens 2004) such as sensitivity to the visual

attention of the recipient (Liebal et al. 2004) and persistence and elaboration of

the signal if the goal of the signaler is not achieved (Leavens et al. 2005). Recent

evidence also indicates that great apes may have a superior level of theory ofmind skills, and when they are tested in competitive paradigms they seem to be

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others (Call and Tomasello 1999). Great apes failed, however, to show any

understanding of false belief (Kaminski et al. 2008; Krachun et al. 2009), which

is seen as the pinnacle of a fully fledged set of theory of mind skills that in

humans typically develops at the age of four (de Villiers and Pyers 2002). The

ability to understand beliefs of others is argued to have underpinned the evolution

of complex social cognition phenomena in humans, including language, which

relies on a set of communally shared symbols with arbitrary assigned meanings

(Tomasello et al. 2005; Tomasello and Carpenter 2007; Fitch et al. 2010). In

summary, although there are critical differences in theory of mind skills

demonstrated by apes and humans, it seems that great apes can assign some

mental states to others. The extent to which these skills are put to pragmatic use

in vocal communication is still to be tested. Research is currently underway to

examine whether the differences between monkeys and apes in terms of theory

of mind skills and gesture use result in great ape species engaging in more

informative, intentional vocal communication than monkeys (K. Slocombe,

unpublished data). Until evidence is forthcoming, however, it is most parsimo-

nious to assume that the cognitive mechanisms involved in ape vocalizations are

similar to those in the better-studied monkey species.

Whilst it is unclear what mechanisms and motivations underlie primate call

production, several lines of evidence indicate that calls are not necessarily rigid

and automatic responses. Call producers seem sensitive to the presence of anaudience and for instance, vervet monkeys rarely produce alarm calls when alone

(Cheney and Seyfarth 1990).

In addition, the composition of the audience also affects call production

both in terms of the frequency of calling (Caine et al. 1995; Chapman and

Lefebvre 1990; Di Bitetti 2005; Roush and Snowdon 2000; Slocombe et al.

2010b) and the acoustic structure of the call production (Slocombe and

Zuberbuhler 2007). Finally, there is some evidence that call producers are

sensitive to the behavior of others, with male langur monkeys continuing to alarm

call until all members of the group call (Wich and de Vries 2006) and male bluemonkeys taking into account the danger faced by group members during calling

in response to eagle predation (Papworth et al. 2008).

Primate call production thus seems sensitive to subtle social variables,

indicating that social complexity may have been an important pressure in

language evolution. As with functional reference little is known, however, about

the cognitive mechanisms that underpin audience effects of call production

(Zuberbuhler 2008). The fact that fish and domestic chickens adjust general

social behavior according to the audience composition (Grosenick et al. 2007;

Herb et al. 2003; Marler et al. 1986) means that complex cognitive tools may notbe required for audience effects to take place: it might just be that the presence

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that the psychological mechanisms involved in audience effect in primates might

be more complex that in other animals (Zuberbuhler 2008). More research is,

however, needed to explore in detail the cognitive underpinnings of audience

effects in primates before such conclusions can be reached.

Summary of Functional Reference. The study of functional reference in

primates provides several fruitful avenues for language evolution research.

Although there are key differences between human reference and functional

reference, the study of functionally referential signals allows us to assess the

type, complexity, and specificity of information that can be communicated

between conspecifics. It has been particularly useful in highlighting the flexibil-

ity of the listener in being able to respond appropriately to a wide variety of

signals (Cheney and Seyfarth 2005), which may shed light on how our own

comprehension skills evolved. In parallel with a broader comparative approach,

we can assess the environments and selective pressures that give rise to

communication of highly specific messages. The current body of work on

functional reference also lays vital ground work for further investigations which

may be particularly pertinent to language evolution. For instance researchers

must establish the meaning of single call types before they can examine how and

why primates may combine their calls, which may provide an insight into

precursors for human syntax.

Vocal Plasticity and Vocal Learning

Humans are able to imitate a wide range of noises: the ability relies on the

engagement of the larynx to generate acoustic variation and to produce novel

vocalizations. Such vocal plasticity is a key property of human speech (Fitch

2000). Comparative research has revealed such vocal plasticity seems to be

shared to some degree with song birds, parrots, dolphins, and seals (Janik and

Slater 1997). Recent studies have shown that chimpanzees in captivity use a

novel raspberry sound as an attention-getter (Hopkins et al. 2007) and anorang-utan has spontaneously learnt to whistle (Wich et al. 2009), but these

sound innovations crucially do not engage the larynx, which is vital for speech

production (Fitch 2000). In contrast, there is no good evidence for plasticity in

primate vocalizations (which rely on laryngeal activity). Despite extensive

training, all attempts to teach a human-raised chimpanzee to speak even a few

words failed (Hayes 1951). There is a considerable body of evidence that shows

that, in contrast to humans, the vocal repertoire of primates is fixed and genetically

determined. For example, from the first days of life a squirrel monkey is able to

produce acoustically adult-like vocalizations (Winter 1969). Early deafness does notstop a squirrel monkey from producing the full vocal repertoire typical of their

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encountered by other animals, which seem to have shaped their vocal behavior

in specific ways (Macedonia 1990). However, in contrast to the majority of

animals, most primate species also live in social groups that are characterized by

unusually complex network of relationships with kin and non-kin, where more

sophisticated communication could give a fitness advantage. Two mechanisms

that would allow primates to increase the number of messages they can communicate

working with a fixed repertoire, which are highly relevant to speech and language

evolution, are categorical perception and call combinations.

On a phonetic level, there can be substantial grading between human

phonemes (e.g., graded continuum between ba and pa), yet humans perceive

these graded signals categorically (Burling 1993; Rosner and Pickering 1994).

Many primates, and particularly apes, have highly graded vocal repertoires, and

there is some evidence that some monkey species also perceive graded calls

categorically (May et al. 1989; Fischer 1998; Fischer et al. 2000; Fisher et al.

2001). Indeed, nonhuman animals have also been shown to perceive continuums

from human speech categorically (e.g., Kuhl and Miller 1975), indicating that

auditory categorical perception is likely to occur in a number of species. More

systematic research is needed to reveal how different primate species perceive

conspecific calls, as currently we may be underestimating the size of their vocal

repertoires.

Categorical perception of graded repertoires may increase the number of

distinct calls available to convey different messages, but the repertoire is still

fixed because of the very limited vocal plasticity in primates. There are several

ways in which this can be overcome. First, primates can use pragmatic strategies,

where information from calls is combined with world knowledge to increase the

range of messages that can be conveyed. We have good evidence that primate

listeners are not simple passive receivers of sound, but they do engage in

pragmatic reasoning (Zuberbuhler 2000a), combine information from calls with

knowledge of social relationships (Cheney et al. 1995; Slocombe et al. 2010a),

and may even perform basic inferential reasoning (Arnold and Zuberbuhler,

submitted) to respond appropriately to the calls they hear. Second, by combining

existing calls to create combinations that elicit different responses in listeners

compared with the component calls, the number of messages that can be

communicated is increased.

Call Combinations

Humans can convey an infinite amount of messages using a limited number

of words because of the powerful system of grammatical rules that govern the

structure and form of language, including the ordering of words into meaningfulsentences. Although it seems highly unlikely that any other species has syntactic

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It is known that primates often produce call combinations composed of two

or more calls and that these calls are sometimes produced in a nonrandom order

and in specific contexts (Mitani and Marler 1989; Robinson 1984; Snowdon and

Cleveland 1984). For instance, experiments showed that black and white colobus

monkeys produce specific call combinations in response to specific predators

(Schel et al. 2009). Similarly, experimental studies with white-handed gibbons

have suggested that recombination of particular notes within songs, which

normally function to strengthen pair-bonding and to attract mates, allows these

primates to communicate about predator-induced danger (Clarke et al. 2006).

Evidence for one call acting as a modifier for another has been provided by

systematic studies of Diana monkey comprehension of Campbell monkey alarm calls

(Zuberbuhler 2002). Campbell monkeys produce distinct alarm calls to both leopards

and eagles, but in addition they also produce a boom call as a general alert call.

Campbell monkeys sometimes produce booms followed by predator specific alarm

calls, and the addition of the boom call seems to modify the meaning of the

subsequent alarm call. For example, in a playback experiment Zuberbuhler showed

that while Diana monkeys typically produce their own leopard call upon hearing

Campbells monkey leopard calls, the Diana monkeys do not produce alarm calls

upon hearing Campbells monkey boom call followed by the leopard call

(Zuberbuhler 2002). This study indicates that the boom call modifies the functional

meaning of the subsequent leopard alarm call.Male putty-nosed monkeys produce sequences of two loud calls that function

to convey at least three different messages to listeners (Arnold and Zuberbuhler

2006a; Arnold and Zuberbuhler 2006b). Sequences of pyows are given to a broad

range of disturbances, including leopards, and sequences of hacks are generally given

in response to eagles. The male monkeys also produce Pyow-hack sequences,

which initiate group travel. Rigorous playback experiments demonstrated that the

lets go message conveyed by the Pyow-hack sequence was contingent on the

sequence of the calls, not the acoustic structure of the calls themselves (Arnold and

Zuberbuhler 2008). This study illustrates how combining calls can enable a greaterflexibility in terms of the functional usage of calls.

There is more evidence of primates combining calls in potentially complex

sequences, but the extent to which this enables individuals to communicate different

or modified messages is unknown because the way listeners respond to these

combinations has yet to be examined. For example, chimpanzees often combine call

types in short sequences, and certain call combinations are given in narrowly defined

contexts (Crockford and Boesch 2005). More recently, potentially high levels of

complexity within call combinations have been discovered in the systematic study of

Campbells monkeys. This species produces numerous combinations of calls inresponse to a wide variety of different events, from trees falling to neighbor

(O l 2009) Fi ll C b ll k f


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shown to be meaningful to listeners, these calling systems will represent an excellent

example of how combining existing calls in a repertoire can increase the complexity

of information that can be communicated.

Conclusion

In summary, the study of primate communication is a promising avenue to

explore in several ways. First, primate vocalizations can help establish what the

phylogenetically old and uniquely human aspects of language and speech may

have been during the evolutionary process. In particular, this review highlights

some of the areas of continuity within the vocal domain, where the primate

ability for functional reference, complex comprehension, and combinations of

calls may represent precursors to linguistic abilities. This review also highlightsdiscontinuity in terms of vocal plasticity and the comparably scant evidence for

modification of calls through learning, suggesting that fine vocal control and the

ability to generate novel calls that are required for speech likely evolved once

humans split from the rest of the primate lineage. As such, primate communi-

cation has much to offer the field of language evolution. However, in many

species we know virtually nothing about their vocal behavior. Much more

research effort is required to exploit this potentially fruitful way of exploring how

and why human language may have evolved.

Received 1 April 2010; revision accepted for publication 20 September 2010.

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