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Primate Vocal Communication: A Useful Toolfor Understanding Human Speech and LanguageEvolution?Author(s): Pawel Fedurek and Katie E. SlocombeSource: Human Biology, 83(2):153-173.Published By: Wayne State University PressDOI: http://dx.doi.org/10.3378/027.083.0202URL: http://www.bioone.org/doi/full/10.3378/027.083.0202

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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 andwhy it evolved have been intriguing scientists for years. Nonhuman primates(primates) are our closest living relatives, and their behavior can be used toestimate the capacities of our extinct ancestors. As humans and manyprimate species rely on vocalizations as their primary mode of communica-tion, the vocal behavior of primates has been an obvious target for studiesinvestigating the evolutionary roots of human speech and language. Bystudying the similarities and differences between human and primatevocalizations, comparative research has the potential to clarify the evolu-tionary processes that shaped human speech and language. This reviewexamines some of the seminal and recent studies that contribute to ourknowledge regarding the link between primate calls and human language andspeech. We focus on three main aspects of primate vocal behavior:functional reference, call combinations, and vocal learning. Studies in theseareas 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 vocalplasticity, are not shared with our primate cousins. We conclude thatcomparative research on primate vocal behavior is a very promising tool fordeepening our understanding of the evolution of human speech and lan-guage, but much is still to be done as many aspects of monkey and apevocalizations 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 livingworld. Language enables humans to represent and communicate complexabstract information, and it occurs in verbal, gestural, and written forms. Anevolutionary account for this capacity remains elusive, but this issue is the focusof interdisciplinary research effort. One premise is that many of the cognitivecapacities involved in language processing are much older than language itself,

1Department of Psychology, University of York, YO10 5DD York, United Kingdom.

Human Biology, April 2011, v. 83, no. 2, pp. 153–173.Copyright © 2011 Wayne State University Press, Detroit, Michigan 48201-1309

KEY WORDS: LANGUAGE, VOCAL COMMUNICATION, NONHUMAN PRIMATES, FUNCTIONAL

REFERENCE, VOCAL LEARNING, CALL COMBINATIONS.

with their phylogenetic roots deep in the primate lineage (Hauser et al. 2002).Thus, a promising empirical approach to understanding the origins of languageis to apply a comparative approach (Hauser et al. 2002). In particular, byexamining the capacities of extant primates, whose phylogenetic relationships tomodern humans are known, we can draw inferences about the likely capacities ofour extinct ancestors. Specifically, by investigating primate behavior it ispossible to test the hypothesis that human language built on abilities alreadypresent in the primate lineage before the advent of modern humans. Thiscomparative approach is vital for identifying the homologous, shared elements oflanguage which appear to have evolved gradually from a common primateancestor and those which have no clear evolutionary path and thus may be the“novel” elements which were instrumental to human language evolving into itscurrent uniquely complex state (Hauser et al. 2002). In addition, comparativeresearch can allow researchers to develop and test hypotheses concerning theevolutionary pressures that may have driven the selection of traits required forlanguage.

Whilst the capacity for language is independent of modality of productionand perception, speech is the pervasive and most prevalent way of conveyinglanguage in modern humans. Speech, which relies on the vocal–auditory channel,is characterized by voluntary control and is a culturally shared system forcommunicating within a population. Speech is also combinatorial, with pho-nemes and syllables being combined to form words and phrases. Humans seemto have several adaptations for speech production and perception, including thoserelated to the structure of the vocal tract and neural mechanisms in the brain(Fitch 2000; Pinker 1994). Understanding how these adaptations evolved iscentral to our understanding of how language evolved into its current speech-dominated form. Although no other primate is equipped with speech apparatus assophisticated as the one found in humans, comparative data from nonhumanprimates 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 comparativeperspective it is necessary to focus on the vocal–auditory channel of communi-cation in other species, including primates (Ghazanfar and Hauser 1999). As thecapacity for language is independent of modality, research into any modality ofcommunication in other species could further our understanding of languageevolution: 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.Many primate species live in arboreal, low-visibility environments and individu-als from the same group are often separated as they travel and forage over largedistances. Vocalizations therefore provide an ideal medium for communicatingwith group members who, because of both physical and social constraints, may

154 / FEDUREK AND SLOCOMBE

not be visible. Empirically more research has been conducted on vocal behaviorthan any other type of communication in primates (Slocombe et al. in press) andresearchers are well equipped to conduct meaningful research into vocalizationsand their cognitive underpinnings because of the techniques and methods that canbe applied to vocal behavior. Detailed acoustic analysis of calls in combinationwith observational data allow us to examine the production of calls in greatdetail, and experimental playback techniques crucially allow us to create and testprecise hypotheses regarding listener understanding of vocal signals. In contrastto other modalities, both observational and experimental vocal techniques can beconducted in the wild, meaning that many primate vocal communication studieshave high ecological validity.

It is important to highlight that facial expressions, body postures, manualgestures, and olfaction also play important roles in primate communication andcommunicative signals are often composites of two or more of these differentmodalities. In this way focusing exclusively on vocal communication is tellingonly part of the story, but unfortunately it is out of the scope of this review tocover the other modalities and multimodal signals and how they also make avaluable contribution to our understanding of language evolution.

Comparative data on primate gestural and vocal communication are oftenused to argue whether the origin of human language was vocal or gestural (Arbib2008; Hewes 1973; Riede et al. 2005; Tomasello 2008; Zuberbuhler 2005). Bothmodalities demonstrate some aspects of continuity with language, with great apegestures being learnt, generative and intentional signals (Tomasello 2008) andmonkey vocalizations functioning referentially and being combined into se-quences (Zuberbuhler 2005). Although data on vocal and gestural competenciesare important for furthering this debate, currently we do not have comparabledata in the two modalities to make very meaningful comparisons (Slocombe et al.in press). For example most gestural data are collected from great apes, whereasmost vocal data are collected from monkeys: any conclusions of the relativemerits of one modality over the other are confounded by systematic differencesin the study species, study environment (wild/captive), and focus of the research.Although vocalizations are central to arguments over the origin of language and thisis another example of how primate vocalizations can make a strong contribution todebates 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 differentquestions within the language evolution debate, including the evolutionarypressures that may have led to more complex communication and the modalityin which human language arose (vocal vs. gestural). They can also help usidentify and distinguish between facets of speech and language which areevolutionarily old, shared traits and which are recent novel human adaptations,and it is in this capacity that they are examined in more detail in this review.There are a many aspects of language and speech that could be examined in this

Primate Vocal Communication / 155

manner, but we focus on two key cognitive components of language where therehas been substantial and important evidence collected from primates: we willexamine evidence for potential precursors to human reference and basiccombinatorial rules. In addition, we will examine vocal learning to illustrate howprimate vocalizations can contribute to our understanding of speech evolutionand how discontinuities between primates and humans are just as valuable indeveloping our understanding as evidence for continuities. It is important to notehere that the aim of this paper is to provide a review of seminal and recentliterature in relation to the topics outlined above, to illustrate the value andrelevance 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 forfurthering our understanding of language evolution (e.g., Arbib 2008; Tomasello2008), we believe this review is important for highlighting the contributionprimate vocal behavior can make to the interdisciplinary research effort focusedon language evolution.

Functional Reference

Human language is highly efficient at conveying meaningful messagesbetween communicators. Semantics plays a crucial role in this, as human words,phrases, and sentences all carry meaning. Within the field of semantics, manyhuman words and phrases are referential, in that they refer to an external objector event in the world. The specificity of reference varies greatly in humanlanguage from utterances with many possible referents (mammal) to highlyspecific utterances (my dog). Comparative researchers have identified a processwithin animal vocal communication that shares some of the features of thishuman system, and may represent an important precursor to human linguisticabilities. 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 beentermed “functionally referential communication.”

Evidence for Functional Reference in Primates. The seminal study offunctional reference examined the alarm calls of vervet monkeys. Strushaker(1967) first reported that vervet monkeys produce three acoustically distinctalarm calls when encountering with their three main predators: leopards, eagles,and snakes. Seyfarth et al. (1980) then conducted a playback experiment toexamine whether these calls were meaningful to listeners, in the sense that thesethree calls represented different classes of predators. The results of the play-backexperiment demonstrated that listeners responded in exactly the same, adaptivemanner to playbacks of conspecific alarm calls as they did when they encoun-tered the real predator (Seyfarth et al. 1980). This means that alarm calls alonegenerate appropriate and adaptive escape responses. Such evidence meets theestablished criteria for functional reference, which are, first, from the productionperspective the call must be acoustically distinct from other calls in the vocal


repertoire and produced consistently in response to a specific external stimulus.Second, from the receiver’s perspective, the receiver must react to the call in thesame way as it would react toward the stimulus itself, in the absence of any otherinformation indicating the presence of the stimulus that elicited the call (Marleret al. 1992).

Since the famous study on vervet monkeys, functionally referential alarmcalls have been found in a number of other primate species, such as Dianamonkeys (Zuberbuhler et al. 1997), Campbell monkeys (Zuberbuhler 2001),putty-nosed monkeys (Arnold and Zuberbuhler 2006b), tamarins (Kirchhof andHammerschmidt 2006), and ring-tailed lemurs (Macedonia 1990). The specific-ity of the alarm calling system varies, with some systems that seem to conveyinformation about the presence of an aerial or terrestrial threat (Macedonia andStanger 1994; Oda and Masataka 1996) and other systems being specific to typesof predator, regardless of the location of the predator. For instance the playbackof predator stimuli from different elevations and distances confirmed thatregardless of the urgency to respond or the trajectory of an imminent attack Dianamonkeys did not deviate from labeling the type of predator with their alarm calls(Zuberbuhler 2000b). It has been suggested that the specificity of alarm callsin these animals results from differences in the nature of escape responsesthat are required to avoid different types of predatory threat (Macedonia1990). Selection pressures seem to have favored the evolution of acousticallyspecific calls that generate specific responses in the receivers, if differentialanti-predator responses increase fitness (Donaldson et al. 2007; Macedonia1990; Pereira and Macedonia 1991).

It is not only in urgent predator avoidance contexts that functionalreference has been found. Primates also produce functionally referential calls inresponse to food. Again there is variation in the specificity of these calls, withtufted capuchin monkeys producing calls that simply alert listeners to thepresence of food in the environment (Di Bitetti 1993) and other speciesproducing vocalizations that seem to provide listeners with information about thenature of the discovered food source. Rhesus macaques give different calls tohigh and low value food items (Hauser and Marler 1993) and a habituation-dishabituation experiment showed that listeners behaved as if they extractedmeaning about the value of the food source from these calls (Hauser 1998). Morerecently chimpanzees have been shown to produce acoustically distinct calls tofoods of different values, and in captivity this system even extends to specific callvariants 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 andZuberbuhler 2005b), but whether the food-specific calls (e.g., bread, mango) aremeaningful to listeners still remains to be tested. In a similar vein there are manystudies showing that acoustically distinct calls or different rates of calls areproduced in response to food of different quality (Golden lion tamarind [Benz


1993], cotton-top tamarins [Roush and Snowdon 2000], white-faced capuchins[Gros-Louis 2003], bonobos [Clay and Zuberbuhler 2009], marmosets [Kitzmannand Caine 2009]) or quantity (red bellied tamarins [Caine et al. 1995]). Suchcontext-specific calling is necessary for a functionally referential system, butlistener understanding (i.e., whether listeners act as if they extract informationabout the external event from the call) must be systematically tested before callscan be shown to function referentially.

The complexity of social relationships within primate groups suggests thatfunctional reference may also occur in a variety of other social situations. Insocial situations distinct behavioral responses to different contexts are rare andthe more subtle responses of listeners are often measured by differences inlooking duration / latency to look at the speaker. Although this shows theprimates distinguish between the calls, it is harder to infer what meaning theyextracted from it.

In the social sphere, female Barbary macaques produce acousticallydifferent calls during copulations depending on whether the male has ejaculatedor not (Pfefferle et al. 2008a). The facts that the call begins well beforeejaculation and that the frequencies of call production correlate with ejaculationrates suggests that these calls are signals directed to the mating partner so as toincrease the probability of ejaculation (Pfefferle et al. 2008a). Recent playbackshave shown that listening males can distinguish between these calls and adjusttheir behavior toward the female (such as walking toward the female or the timespent in her vicinity) according to whether she has just had a successful matingwith another male (Pfefferle et al. 2008b). It is therefore possible that these callsalso function to provide male listeners with information about whether thefemale is likely to conceive to increase the likelihood of subsequent mating(Pfefferle et al. 2008b).

Primates often vocalize whilst involved in agonistic interactions, andrhesus macaque monkeys give different screams in response to differing levels ofaggression from opponents of different ranks. A playback experiment showedthat mothers were able to meaningfully distinguish (i.e., they responded to thesecalls as if they extracted some information about the ongoing fight from thesevocalizations) between scream variants given by offspring (Gouzoules et al.1984). More recently chimpanzees have been shown to produce acousticallydistinct screams depending on their social role in the interaction (victim oraggressor; [Slocombe and Zuberbuhler 2005a]). A playback study has shown thatlisteners were able to infer the respective roles and the subsequent direction ofaggression 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 congruouswith the existing social dominance hierarchy, with subjects showing significantlymore interest in the incongruent interactions. Victim screams also systematicallyvary in acoustic structure as a function of the severity of aggression encounteredby the caller (Slocombe and Zuberbuhler 2007), and a playback experiment


conducted in the wild demonstrated that listeners distinguished between thesescreams (Slocombe et al. 2009). Listeners showed significantly more interest inscreams given in response to severe aggression than mild aggression. Theseresponses were not driven by low level responses to the acoustic structure of thedifferent screams, as listeners did not show comparable interest in controltantrum screams, which matched the severe screams in acoustic structure.

Evidence for Functional Reference in Non-Primate Species. Functionalreference has also been demonstrated in a wide variety of nonprimate species.For instance, chickens produce functionally referential food calls (Evans andMarler 1994) and alarm calls that function to refer to aerial and terrestrialpredatory threats (Evans et al. 1993). Meerkats also produce alarm calls that notonly function to denote predator type but also the urgency of response (Manser2001; Manser et al. 2002). Although the surface behavior of these diverse speciesis similar, there is some evidence that primates seem to process these calls in arelatively sophisticated way. For instance, experiments with wild Diana monkeysindicated that listeners attended to the meaning of the call rather than the surfaceacoustics and likely form some kind of mental representation when hearing a call(Zuberbuhler et al. 1999). This study showed that upon hearing a soundindicating the presence of a specific predator, such as leopard growls, Dianamonkeys respond much less intensively if they had been primed by a conspe-cific’s leopard alarm call (Zuberbuhler et al. 1999). The leopard growls and theleopard alarm call are two acoustically different sounds, suggesting that themonkeys were habituating not to the low level acoustic structure of the stimulibut to the referent of the sounds. Unfortunately, comparable experimentsprobing the mechanisms underlying functionally referential signals in nonpri-mates have not been reported, so it is difficult to conclude how the presence ofsimilar behavior in nonprimate species should affect our interpretation of the datain relation to humans. It is likely, however, that similar evolutionary pressureshave lead to the emergence of this kind of signaling in divergent species. Furtherinvestigation of functional reference in other nonprimate species may furthershed light on the selection pressures that favor its emergence and clarifysimilarities and differences in the psychological underpinnings of this behavior indifferent species.

Human Language and Functional Reference. The studies of functionallyreferential calls indicate some continuity between primate and human commu-nication. However, it is important to highlight some crucial differences betweenfunctional reference in animals and reference in humans. First, the referentialcharacter of human language is arbitrary in the sense that humans flexibly attachdifferent meanings to different symbols (words) whereas other primates seem tohave considerable genetic constraints on possible meaning-call mappings.Second, although the surface behavior in humans, primates, and nonprimates canlook similar, we have very limited evidence on whether the psychological


mechanisms underlying communication are similar. This is partly because of apaucity of research tools we have available to examine the cognitive machineryinvolved in nonhuman animal vocal communication (Cheney and Seyfarth 1990).As outlined above, there is some evidence that some primate listeners may formsome kind of mental representation when hearing functionally referential calls(e.g., Zuberbuhler et al. 1999). However, it is very difficult to examine the natureof any mental representation held by a primate. For instance, when a vervetmonkey responds appropriately to a leopard alarm call, it is impossible to tellwhether the calls evoke a declarative representation of a leopard in the mind ofthe listener or whether they interpret the call as an imperative such as “climb thetree.” Although we sometimes use such metaphors as “information,” “message,”and “meaningful,” we might never be sure exactly what happens in the listener’smind. Furthermore, the involvement of such mental representations may not berequired to produce and respond appropriately to referential signals, and moresimple mechanisms may account for these effects (Hauser et al. 2002; Owren andRendall 2001; Seyfarth et al. 2010). Parsimony is strength in science for a goodreason: simple mechanisms are more likely to evolve, and therefore we shouldfirst explore the simplest possible explanations for any behavior, includingfunctionally referential calls, before reaching for more elaborated ones. It is forthese reasons that the term “functionally referential communication” refers to theway 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 andRendall 2001).

The cognitive mechanisms involved in primate vocal behavior remains acontentious issue and a topic of considerable recent debate. Rendall et al. (2009),for example, challenged the view that the concept of information is needed toexplain any aspect of vocal communication in nonhuman animals. Their keyargument is that the mechanisms involved in primate communication differ fromthose characterizing human language mainly as a result of the cognitivelimitation of these animals. The authors claim that nonhuman animals are notcapable of intentional communication and perspective-taking and consequentlyadvocate abandoning any “language-like” expressions such as “information”when dealing with primate vocalizations. In contrast, Seyfarth et al. (2010) claimthat the term “information” applies simply to the process of reducing uncertaintyby learning associations between one stimulus (such as a vocal signal) andanother (such as the presence of a predator), rather than to the elaborate processof encoding and decoding of ideas that occurs in human language. The processof making associations between calls and objects or events in external world isfavored by natural selection as it allows animals predict accurately critical eventsin the environment. The fact that this process is rather simple has prompted someresearchers to argue that terms such as “information transfer” are confusing andshould be abandoned in the studies of nonhuman animal communication, as theyimply the involvement of elaborate cognitive machinery in this process (Carazoand Font 2010).


The role of receivers in animal communication has also been extensivelydiscussed. Rendall et al. (2009) suggest that primate vocalizations function tomanipulate the behaviors of receivers through the direct induction of theirnervous systems. Rendall et al. (2009) along with Owren et al. (in press)characterize listeners as passive receivers and reject the notion that receiversextract and infer information from calls in any way similar to human languageprocessing. Seyfarth et al. (2010) criticize this approach, suggesting that itfocuses too heavily on the interests of senders while neglecting the interests ofreceivers in animal communication. The evolution of communicative signalsrequires the interplay of signalers and receivers, as signals can be ignored by thereceivers if they are costly or fail to provide benefits (Searcy and Nowicki 2005;Zahavi and Zahavi 1997). Therefore, the receivers are not prisoners of themanipulative tactics used by the senders (Seyfarth et al. 2010) and rather play anactive role in communication and the evolution of signals.

Mechanisms Underlying Call Production. Although there are many areas ofdisagreement regarding animal communication, there does seem to be a generalagreement that the motivations and mechanisms that drive call production inprimates likely differ from those involved in human language. Human languageis generally characterized by the producer intending to convey a message to thereceiver, 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 callproduction was contingent on the callers themselves being at the periphery of thegroup, rather than a reflection of a motivation to provide an informative reply toother lost individuals (Cheney et al. 1996). It is argued that the ability todistinguish between others’ and own knowledge is a key prerequisite for suchinformative and intentional communication (Grice 1957), and given the generallypoor performance of monkey species on theory of mind (i.e., the ability toattribute mental stages to others) tests (Heyes 1998; Povinelli et al. 1991), thistype of communication may be impossible. This view is supported by a study inwhich rhesus monkey mothers were given the opportunity to inform ignorantoffspring 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 showsome hallmarks of intentionality (Leavens 2004) such as sensitivity to the visualattention of the recipient (Liebal et al. 2004) and persistence and elaboration ofthe signal if the goal of the signaler is not achieved (Leavens et al. 2005). Recentevidence 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 beable to distinguish what other individuals see and know (Hare et al. 2001; Hareet al. 2006; Kaminski et al. 2008). Although this remains a contentious issue(Penn and Povinelli 2007; Povinelli and Vonk 2003), recent experiments haveshown that chimpanzees understand the goals, intentions, and knowledge of


others (Call and Tomasello 1999). Great apes failed, however, to show anyunderstanding of false belief (Kaminski et al. 2008; Krachun et al. 2009), whichis seen as the pinnacle of a fully fledged set of theory of mind skills that inhumans typically develops at the age of four (de Villiers and Pyers 2002). Theability to understand beliefs of others is argued to have underpinned the evolutionof complex social cognition phenomena in humans, including language, whichrelies on a set of communally shared symbols with arbitrary assigned meanings(Tomasello et al. 2005; Tomasello and Carpenter 2007; Fitch et al. 2010). Insummary, although there are critical differences in theory of mind skillsdemonstrated by apes and humans, it seems that great apes can assign somemental states to others. The extent to which these skills are put to pragmatic usein vocal communication is still to be tested. Research is currently underway toexamine whether the differences between monkeys and apes in terms of theoryof mind skills and gesture use result in great ape species engaging in moreinformative, 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 aresimilar to those in the better-studied monkey species.

Whilst it is unclear what mechanisms and motivations underlie primate callproduction, several lines of evidence indicate that calls are not necessarily rigidand 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 productionboth in terms of the frequency of calling (Caine et al. 1995; Chapman andLefebvre 1990; Di Bitetti 2005; Roush and Snowdon 2000; Slocombe et al.2010b) and the acoustic structure of the call production (Slocombe andZuberbuhler 2007). Finally, there is some evidence that call producers aresensitive to the behavior of others, with male langur monkeys continuing to alarmcall 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 callingin 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 inlanguage evolution. As with functional reference little is known, however, aboutthe cognitive mechanisms that underpin audience effects of call production(Zuberbuhler 2008). The fact that fish and domestic chickens adjust generalsocial 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 presenceof certain individuals is an external stimulus that automatically triggers certainbehaviors. Primates, however, seem to modulate their social communication as afunction of very subtle social cues, such as the attention of others (Liebal et al.2004) and their capacity to help (Slocombe and Zuberbuhler 2007), indicating


that the psychological mechanisms involved in audience effect in primates mightbe more complex that in other animals (Zuberbuhler 2008). More research is,however, needed to explore in detail the cognitive underpinnings of audienceeffects in primates before such conclusions can be reached.

Summary of Functional Reference. The study of functional reference inprimates provides several fruitful avenues for language evolution research.Although there are key differences between human reference and functionalreference, the study of functionally referential signals allows us to assess thetype, complexity, and specificity of information that can be communicatedbetween conspecifics. It has been particularly useful in highlighting the flexibil-ity of the listener in being able to respond appropriately to a wide variety ofsignals (Cheney and Seyfarth 2005), which may shed light on how our owncomprehension skills evolved. In parallel with a broader comparative approach,we can assess the environments and selective pressures that give rise tocommunication of highly specific messages. The current body of work onfunctional reference also lays vital ground work for further investigations whichmay be particularly pertinent to language evolution. For instance researchersmust establish the meaning of single call types before they can examine how andwhy primates may combine their calls, which may provide an insight intoprecursors for human syntax.

Vocal Plasticity and Vocal Learning

Humans are able to imitate a wide range of noises: the ability relies on theengagement of the larynx to generate acoustic variation and to produce novelvocalizations. Such vocal plasticity is a key property of human speech (Fitch2000). Comparative research has revealed such vocal plasticity seems to beshared to some degree with song birds, parrots, dolphins, and seals (Janik andSlater 1997). Recent studies have shown that chimpanzees in captivity use anovel raspberry sound as an attention-getter (Hopkins et al. 2007) and anorang-utan has spontaneously learnt to whistle (Wich et al. 2009), but thesesound innovations crucially do not engage the larynx, which is vital for speechproduction (Fitch 2000). In contrast, there is no good evidence for plasticity inprimate vocalizations (which rely on laryngeal activity). Despite extensivetraining, all attempts to teach a human-raised chimpanzee to speak even a fewwords failed (Hayes 1951). There is a considerable body of evidence that showsthat, in contrast to humans, the vocal repertoire of primates is fixed and geneticallydetermined. For example, from the first days of life a squirrel monkey is able toproduce acoustically adult-like vocalizations (Winter 1969). Early deafness does notstop a squirrel monkey from producing the full vocal repertoire typical of theirspecies (Winter et al. 1973). In addition, monkey infants raised with heterospecificfoster mothers retain the species-specific vocal repertoire (Owren et al. 1992). Themessage generated by these studies is very clear: vocal production in primates isinnately determined, and learning has little or nothing to do with its development.


Despite the inability of primates to generate or develop novel sounds, thereis evidence that they can modify the acoustic structure of existing calls withintheir repertoire (Egnor and Hauser 2004). Baboons modify the temporal featuresof their grunt vocalizations to accommodate differences in sound propagation asthey move through varying habitats (Ey et al. 2009). Subtle vocal learning alsoseems to be particularly prevalent in relation to the social use of vocalizations. Anumber of studies showed that primates adjust the acoustic structure of their callsafter a change in social circumstances. It has been shown, for example, that afterplacing two unfamiliar populations of pygmy marmosets in the same acousticenvironment, the two populations modified the acoustic parameters of theircontact calls making them acoustically more similar to each other (Elowson andSnowdon 1994). A similar convergence of call structure was observed in the trillcalls of newly paired pygmy marmosets (Snowdon and Elowson 1999) andduring the process of pair-bonding in gibbons (Geissmann 1986; Geissmann2002). Whereas these studies show that primates adjust vocal production to newsocial environments on a long-term basis (usually several weeks or more),several studies indicated that primates can also modify their calls in a dynamic,flexible, short-term manner. For instance, if played back coo calls, Japanesemacaques reply with calls that match the acoustic features of the calls they heard(Sugiura 1993; Sugiura 1998). Mitani and Gros-Louis (1998) focused on a singlechimpanzee dyad and found that while producing a joint pant hoot these closesocial partners adjusted the acoustic structure of their calls to match elements oftheir partner’s call.

Further evidence for vocal learning in primates comes from the studies onacoustic variants of calls that occur in different populations. It is assumed thatsuch group-specific variants or dialects in different populations of the samespecies are a result of learning, provided that these populations live in a similarhabitat and are not genetically heterogenic (Mitani et al. 1999). Studies on bothmonkeys and apes provide evidence that dialects do exist in nonhuman primates.It has been shown, for example, that screams among pigtail macaques and coocalls in rhesus macaques could function as matrilineal signature calls as thesevocalizations vary between particular matrilines (Gouzoules and Gouzoules1992; Hauser 1992). Several studies on chimpanzee pant hoots (i.e., longdistance species-specific calls) suggest that dialects also characterize chimpanzeevocalizations. For example, several geographically separated chimpanzee popu-lations produce acoustically different pant hoots (Clark Arcadi 1996; Mitani et al.1992). One study strongly suggests that these differences are the product oflearning as neither genetic differences nor habitat accounted for the acousticdifferences in pant hoot production between three adjacent communities of wildchimpanzees (Crockford et al. 2004). Similar conclusions were obtained from thestudies focused on the acoustic convergence of pant hoots in captive chimpanzeegroups (Marshall et al. 1999). It is very possible that dialects in both humans andprimates evolved in response to the same selection pressure: the need todistinguish between group members and strangers (Nettle 1999).


Primates also exhibit some evidence of learning in vocal usage (e.g., whichcall to give in which situation). Vervet monkey infants use alarm calls much lessselectively than adults do, for example, by giving an “eagle” alarm call afterseeing any kind of bird, or producing a “leopard” alarm call in response to anyterrestrial animal. Juveniles make these “mistakes” less frequently, and the vocalusage becomes substantially more precise when an animal reaches adulthood(Seyfarth and Cheney 1986). Likewise, in rhesus monkeys the usage of certainkinds of grunts and screams in response to particular social contexts also seemsto develop through an individual’s maturation (Gouzoules and Gouzoules 1992;Seyfarth and Cheney 1986). These studies imply that while during primateinfancy there is little learning involved in vocal production, infants seem to learnthe finer details of vocal usage.

In summary, primates seem to have a genetically determined and fixedvocal repertoire. They do seem able to modify some aspects of the acousticstructure of calls already within their repertoire and learning seems to have a rolein correct vocal usage, but this seems to be qualitatively different from the vocallearning abilities of humans. Genetic evidence indicates that the humans have aunique version of the FOXP2 gene, which is crucial for a proper development offine motor control over their oro-facial muscles during ontogeny (Enard et al.2002). Individuals with damage to this gene typically show high levels ofimpairment in oro-facial control and speech (Vargha-Khadem et al. 2005).FOXP2 is a highly conserved gene that is very similar across avian andmammalian species, and the FOXP2 protein is identical in chimpanzee, gorilla,and rhesus macaque species (Enard et al. 2002; Webb and Zhang 2005). Thehuman version of this gene, however, is different. It has been shown that thechimpanzee version of the protein sequence differs from the human version bytwo amino-acids (Enard et al. 2002). A recent study shows that the insertion ofthe human version of FOXP2 into a mouse changes her vocal behavior andactivity in the relevant brain regions, suggesting that small changes in this genemight have been very important for the evolution of speech (Enard et al. 2009).While some believe that changes in the human version of this gene may havebeen vital for speech arising in humans (Enard et al. 2002), other researchers aremore skeptical about this conclusion and suggest the difference between humanand nonhuman primates in terms of vocal abilities might be attributed toregulatory changes at the FOXP2 locus rather than to the changes in the FOXP2gene itself (Carroll 2005).

Given the often small size and fixed nature of primate vocal repertoires,some argue that primates are consequently limited to communicating a verysmall number of simple “messages” and therefore their vocal behavior is not ofinterest for theories of language evolution (Tomasello 2008). In contrast to thiswe would argue that by examining the ways in which primates compensate fortheir small, fixed repertoire to communicate in complex and varied ways, we canlearn about the evolutionary pressures which give rise to more sophisticatedcommunication. Primates face a number of pressures, such as predation, also


encountered by other animals, which seem to have shaped their vocal behaviorin specific ways (Macedonia 1990). However, in contrast to the majority ofanimals, most primate species also live in social groups that are characterized byunusually complex network of relationships with kin and non-kin, where moresophisticated communication could give a fitness advantage. Two mechanismsthat would allow primates to increase the number of messages they can communicateworking with a fixed repertoire, which are highly relevant to speech and languageevolution, are categorical perception and call combinations.

On a phonetic level, there can be substantial grading between humanphonemes (e.g., graded continuum between ba and pa), yet humans perceivethese graded signals categorically (Burling 1993; Rosner and Pickering 1994).Many primates, and particularly apes, have highly graded vocal repertoires, andthere is some evidence that some monkey species also perceive graded callscategorically (May et al. 1989; Fischer 1998; Fischer et al. 2000; Fisher et al.2001). Indeed, nonhuman animals have also been shown to perceive continuumsfrom human speech categorically (e.g., Kuhl and Miller 1975), indicating thatauditory categorical perception is likely to occur in a number of species. Moresystematic research is needed to reveal how different primate species perceiveconspecific calls, as currently we may be underestimating the size of their vocalrepertoires.

Categorical perception of graded repertoires may increase the number ofdistinct calls available to convey different “messages,” but the repertoire is stillfixed because of the very limited vocal plasticity in primates. There are severalways in which this can be overcome. First, primates can use pragmatic strategies,where information from calls is combined with world knowledge to increase therange of “messages” that can be conveyed. We have good evidence that primatelisteners are not simple passive receivers of sound, but they do engage inpragmatic reasoning (Zuberbuhler 2000a), combine information from calls withknowledge 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 combiningexisting calls to create combinations that elicit different responses in listenerscompared with the component calls, the number of “messages” that can becommunicated is increased.

Call Combinations

Humans can convey an infinite amount of messages using a limited numberof words because of the powerful system of grammatical rules that govern thestructure and form of language, including the ordering of words into meaningfulsentences. Although it seems highly unlikely that any other species has syntacticrules as complex as those of humans, primates may provide us with evidence ofprecursors or building blocks to this more complex human ability. Combiningexisting calls to provide different “messages” to listeners is one way in whichprimates may compensate for their fixed repertoire of calls.


It is known that primates often produce call combinations composed of twoor more calls and that these calls are sometimes produced in a nonrandom orderand in specific contexts (Mitani and Marler 1989; Robinson 1984; Snowdon andCleveland 1984). For instance, experiments showed that black and white colobusmonkeys produce specific call combinations in response to specific predators(Schel et al. 2009). Similarly, experimental studies with white-handed gibbonshave suggested that recombination of particular notes within songs, whichnormally function to strengthen pair-bonding and to attract mates, allows theseprimates to communicate about predator-induced danger (Clarke et al. 2006).

Evidence for one call acting as a modifier for another has been provided bysystematic studies of Diana monkey comprehension of Campbell monkey alarm calls(Zuberbuhler 2002). Campbell monkeys produce distinct alarm calls to both leopardsand eagles, but in addition they also produce a “boom” call as a general alert call.Campbell monkeys sometimes produce booms followed by predator specific alarmcalls, and the addition of the boom call seems to modify the meaning of thesubsequent alarm call. For example, in a playback experiment Zuberbuhler showedthat while Diana monkeys typically produce their own “leopard” call upon hearingCampbell’s monkey “leopard” calls, the Diana monkeys do not produce alarm callsupon hearing Campbell’s monkey “boom” call followed by the “leopard” call(Zuberbuhler 2002). This study indicates that the “boom” call modifies the functionalmeaning of the subsequent “leopard” alarm call.

Male putty-nosed monkeys produce sequences of two loud calls that functionto convey at least three different “messages” to listeners (Arnold and Zuberbuhler2006a; Arnold and Zuberbuhler 2006b). Sequences of “pyows” are given to a broadrange of disturbances, including leopards, and sequences of hacks are generally givenin response to eagles. The male monkeys also produce “Pyow-hack” sequences,which initiate group travel. Rigorous playback experiments demonstrated that the“let’s go message” conveyed by the “Pyow-hack” sequence was contingent on thesequence of the calls, not the acoustic structure of the calls themselves (Arnold andZuberbuhler 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 complexsequences, but the extent to which this enables individuals to communicate differentor modified “messages” is unknown because the way listeners respond to thesecombinations has yet to be examined. For example, chimpanzees often combine calltypes in short sequences, and certain call combinations are given in narrowly definedcontexts (Crockford and Boesch 2005). More recently, potentially high levels ofcomplexity within call combinations have been discovered in the systematic study ofCampbell’s monkeys. This species produces numerous combinations of calls inresponse to a wide variety of different events, from trees falling to neighborencounters (Ouattara et al. 2009). Finally, Campbell’s monkeys can transform aspecific “eagle” alarm call into a more general alarm call, indicating arborealdisturbance, by generating acoustic variation in a way functionally similar tosuffixation in human language (Ouattara et al. 2009). If these call combinations are


shown to be meaningful to listeners, these calling systems will represent an excellentexample of how combining existing calls in a repertoire can increase the complexityof information that can be communicated.

Conclusion

In summary, the study of primate communication is a promising avenue toexplore in several ways. First, primate vocalizations can help establish what thephylogenetically old and uniquely human aspects of language and speech mayhave been during the evolutionary process. In particular, this review highlightssome of the areas of continuity within the vocal domain, where the primateability for functional reference, complex comprehension, and combinations ofcalls may represent precursors to linguistic abilities. This review also highlightsdiscontinuity in terms of vocal plasticity and the comparably scant evidence formodification of calls through learning, suggesting that fine vocal control and theability to generate novel calls that are required for speech likely evolved oncehumans split from the rest of the primate lineage. As such, primate communi-cation has much to offer the field of language evolution. However, in manyspecies we know virtually nothing about their vocal behavior. Much moreresearch effort is required to exploit this potentially fruitful way of exploring howand why human language may have evolved.

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

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