? 2008 by The Wenner-Gren Foundation for Anthropological Research. All rights reserved. 0011-3204/2008/4906-0004$10.00. DOI: 10.1086/593015
Current Anthropology Volume 49, Number 6, 20081053
Primate Vocalization, Gesture, and the
Evolution of Human Language
Michael A. Arbib, Katja Liebal, and Simone Pika
CA? Online-Only Material: Supplements A–D
The performance of language is multimodal, not confined to speech. Review of monkey and ape
communication demonstrates greater flexibility in the use of hands and body than for vocalization.
Nonetheless, the gestural repertoire of any group of nonhuman primates is small compared with the
vocabulary of any human language and thus, presumably, of the transitional form called protolan-
guage. We argue that it was the coupling of gestural communication with enhanced capacities for
imitation that made possible the emergence of protosign to provide essential scaffolding for pro-
tospeech in the evolution of protolanguage. Similarly, we argue against a direct evolutionary path
from nonhuman primate vocalization to human speech. The analysis refines aspects of the mirror
system hypothesis on the role of the primate brain’s mirror system for manual action in evolution
of the human language-ready brain.
In looking for the evolutionary roots of human speech, many
researchers turned to the vocal signals of nonhuman primates
(e.g., Seyfarth 1987; Snowdon, Brown, and Petersen 1982) as
opposed to a “gestural origins” view of how language might
have evolved. However, children use gestures for communi-
cation before their first spoken words, and adult speakers
normally accompany all their speech with expressive manual
gestures (cospeech gestures; McNeill 1992, 2005), while hu-
man signed languages are full-blown languages that do not
use speech. Thus, any theory of language origins mustaddress
the fact that gestures form a crucial part of the human “lan-
guage performance system.” Hewes (1973) argued that our
ancestors were able to voluntarily control gestures long before
speech emerged. Corballis (1991, 2002) suggestedthatmanual
gestures paved the way for the evolution of handedness linked
to cerebral lateralization and—exploiting the “generativity”
of manual action—for the evolution of human language.
Armstrong and Wilcox (2007) support a crucialroleforiconic
gestures in language evolution and suggest that signed lan-
guages are the original and prototypical languages.
Our “modified gestural origins” theory charts a possible
Michael A. Arbib is Professor of Computer Science and Neurosci-
ence at the University of Southern California (Los Angeles, CA
90089-2520, U.S.A. [email@example.com]). Katja Liebal has a research
position at the Max Planck Institute for Evolutionary Anthropology,
Leipzig, and is an honorary lecturer at the psychology department,
the University of Portsmouth. Simone Pika is a lecturer in Evolu-
tionary Psychology at the School of Psychological Sciences at the
University of Manchester. This paper was submitted 14 XII 06 and
accepted 4 VI 08.
evolutionary course from brain mechanisms for manual
praxis (practical actions such as those involved in manipu-
lating objects) to those supporting language. It does not deny
the importance of vocalization but suggests that gesture and
then pantomime offered a path to an open semantics that
vocalization could not provide without this scaffolding. In
what follows, it will be important to distinguish imitation of
praxic actions from pantomime. In the early stages of our
observed actions to achieve some goal with respect to an
object. Pantomime, which we see, in evolutionary terms, as
building on imitation, involves (in the early stages) the rep-
etition of some of the movements of a praxic action, but
thing about the action, object, or event concerned.
Our theory is grounded in evidence from brain imaging
(e.g., Grafton et al. 1996) that there is a human mirror system
for grasping—i.e., a brain region activated for both grasping
and observation of grasping—in or near Broca’s area. Such
findings raised the following question: Why might a mirror
system for grasping be associated with an area commonly
seen as involved in speech production? The fact that aphasia
of signed and spoken languages may result from lesions to
Broca’s area (Emmorey 2002; Poizner, Klima, and Bellugi
1987) supports the view that one should associate Broca’s
area with multimodal language production rather than with
speech alone. Such considerations led to the formulation of
the mirror system hypothesis (Arbib and Rizzolatti 1997; Riz-
zolatti and Arbib 1998): the evolutionary basis for language
parity (the more or less alignment between the meaning in-
tended by the “speaker” and the meaning understood by the
1054 Current Anthropology Volume 49, Number 6, December 2008
“hearer”) is provided by the evolution of brain mechanisms
that support language atop the mirror system for grasping,
rooting speech in communication based on manual gesture.
In more detail, Arbib (2005a) argues that an ability for
complex imitation unique to the human line made possible
the evolution of brain mechanisms for pantomimeandthence
protosign, a system of conventional gestures used to formalize,
disambiguate, and extend pantomime. It was further hy-
pothesized that, once protosign has established an ability for
the free creation of arbitrary gestures to support an open-
ended semantics, the capacity to use conventionalized manual
communicative gestures (protosign) and the capacity to use
vocal communicative gestures (protospeech) evolved together
in an expanding spiral(Arbib2005b)tosupportprotolanguage
(Arbib 2008; Bickerton 2008), an open-ended multimodal
of nonhuman primates lack compositionality, a crucial prop-
erty of modern human languages. This is the notion that
language gets its power not only from having an open-ended
lexicon but also from having a grammar that allows words to
be combined into phrases, with the results open to further
combination, but also enables the hearer to infer the meaning
of the overall utterance from the meaning of its parts and
the constructions used to assemble them.
In this article, we will consider data from neuroscience only
briefly. Instead, we address a glaring weakness of most writing
on the mirror system hypothesis: too little attention is paid
to research on the communication systems of nonhuman pri-
mates as a source of comparative data. This article is written
to rectify this omission, especially with reference to the debate
over whether the emergence of protosign did indeed provide
essential scaffolding for the emergence of protolanguage.
The most debated topics in regard to the use of gestures,
facial expressions, and vocalizations by nonhuman primates
include (1) whether they are used intentionally or are simply
side effects of emotional states, (2) how flexibly they are used
(even gestures produced unintentionally may involve context
specificity and audience effects), (3) whether they have an
inherent meaning or whether the meaning is conveyed by the
social context, (4) whether they are inherited or learned, and
(5) whether they are used referentially.
The following sections review the existing literature on vo-
cal communication, facial expressions, and gestural com-
munication of nonhuman primates. We then compare com-
munication systems in monkeys and apes and gestural
communication in apes and prelinguistic or just-linguistic
human children. Finally, we discuss the implications of these
data for theories of language evolution.
Vocal Communication of Nonhuman
There are many studies on vocalizations of a range of monkey
species (e.g., Gouzoules 1995; Kudo 1987; Seyfarth, Cheney,
and Marler 1980; Zuberbu ¨hler 2002), whereas studies of ape
vocalizations focused mainlyonchimpanzees(Pantroglodytes;
e.g., Clark and Wrangham 1993; Crockford and Boesch 2003;
Mitani and Gros-Louis 1998; Slocombe and Zuberbu ¨hler
Production of Vocalizations
Monkeys reared in social isolation produce basically all their
species-typical call types from soon after birth.Althoughthere
is evidence of some flexibility in the way a given monkey
vocalization is produced (for a recent review, see Ham-
merschmidt and Fischer 2008), no new vocal signals are in-
vented by individuals (for a review, see Snowdon and Haus-
berger 1997). Cross-fostering of rhesus monkeys (Macaca
mulatta) and Japanese macaques (Macaca fuscata) produces
no significant changes in their species-specific vocalizations
(Owren et al. 1992), while gibbon hybrids produce songs
composed of phrases from both parental species (Geissmann
1984). Concerning apes, chimpanzee males in the wild show
a positive association between the amount of time spent with
another individual and call similarity in their “pant-hoots”
(Mitani and Brandt 1994). However, males who chorus often
with others produce more variable calls than individuals who
chorus less often or call alone. Humans (Homo sapiens) also
display a variety of involuntary vocal behaviors, but these are
to be distinguished from speech (e.g., Burling 1993).
Higher degrees of flexibility are present in the “audience
effect” of vocalizations (Tomasello and Zuberbu ¨hler 2002).
For example, tamarins (Saguinus labiatus) produce food calls
when discovering food, but the rates depend on whetherother
group mates are present (Caine, Addington, and Windfelder
1995). Vervet monkey females (Cercopithecus aethiops) adjust
the rate of alarm calling depending on whether their own
offspring are present, while males call more often when fe-
males are present (Cheney and Seyfarth 1985). Seyfarth and
Cheney (2003), however, conclude that nonhuman primates
may lack the human ability to represent the mental states of
others and involve simply the recipients’ presence or absence.
Concerning great apes, Mitani and Nishida (1993) reported
that male chimpanzees use pant-hoots more frequently in
traveling contexts when their alliance partners are nearby.
Wilson, Hauser, and Wrangham (2001) showed that, in re-
sponse to the playback of the pant-hoot call of a single ex-
tragroup male, parties with three or more males consistently
joined in a chorus of pant-hoots and approached the loud-
speaker together, while parties with fewer adult males usually
stayed silent and approached the loudspeaker less often. Slo-
combe and Zuberbu ¨hler (2007) reported that chimpanzees in
the wild seemed to modify the acoustic structure of their
screams during a severe attack if at least one listener in the
audience matched or surpassed the aggressor in rank. This
suggests that chimpanzees understand third-party relation-
ships and adjust their vocal production in relation to the rank
relationship of aggressor and listener. In addition, Hopkins,
Arbib, Liebal, and Pika Primate Vocalization, Gesture, and the Evolution of Human Language1055
Taglialatela, and Leavens (2007; but see also Hostetter, Can-
tero, and Hopkins 2001) found that chimpanzees in captivity
were more likely to produce two so-called attention-getting
sounds, the “raspberry” and the “extended grunt,” when a
human was present in conjunction with a preferred food item
than when either stimulus (human, food) was presented
alone. They thus suggest that chimpanzees may produce these
Referential Use of Vocalizations
It has been argued that an animal vocalization qualifies as
referential if the signal (a) has a distinct acoustic structure,
(b) is produced in response to a particular external object or
event, and (c) elicits a response in nearby listeners similar to
that which the external object or event normally elicits (Zu-
berbu ¨hler 2000b). Point b asserts that referential communi-
cation is triadic, involving a sender, a receiver, and a third
entity. To date, most of the evidence for referential signals in
nonhuman primates stems from monkey species. For in-
and Campbell’s monkeys (Cercopithecus campbelli) allusedis-
tinct alarm calls for different predators, eliciting appropriate
escape responses in other group members (Cheney and Sey-
farth 1990; Zuberbu ¨hler 1999, 2001). Although the degree of
context specificity varies across species (Evans 1997), these
results suggest thatreferentialcommunicationisawidespread,
perhaps universal, characteristic of primate communication.
However, referential alarm calls are present in various mam-
mals such as squirrels (Spermophilus beecheyi; Owings and
Virginia 1978), marmots (Blumstein 1995a, 1995b), and even
chickens (Gyger, Marler, and Pickert 1987). Such findings
argue against the view that this form of the capacity to assign
meaning to sound utterances constitutes a primate referential
ability that could be pivotal to language. Language cannot
rest on a small, fixed repertoire of such utterances.
The majority of referential calls in monkeys is linked to
predation (Gouzoules and Gouzoules 2000; Gouzoules, Gou-
zoules, and Marler 1984; Hauser 1998). Chimpanzees in the
wild produce vocalizations that are context specific and not
limited to predation, crucial prerequisites for calls to function
referentially (Crockford and Boesch 2003; Uhlenbroek 1996).
In addition, captive chimpanzees use acoustically distinct
“grunt” variants as response to different food preference clas-
ses (Slocombe and Zuberbu ¨hler 2006), and a playback ex-
periment showed that a single chimpanzee seemed to use the
information encoded in the calls to guide his search for food
(Slocombe and Zuberbu ¨hler 2005b).
Several hypotheses may explain the difference betweenapes
and monkeys. First, there may be a paucity of data rather
than a lack of referential abilities in apes in the wild. Second,
there may be evolutionary pressure for monkeys but not great
apes to develop a repertoire of predator-specific alarm calls.
Third, differences in social systems might account for differ-
ences in vocal behavior. Finally, great apes might have “lost”
a referential vocal system present in their ancestors because
they might have become specialized for a different kind of
referential skill based on the flexible use of manual gestural
signals (see “Repertoire and Use”). These hypotheses need
not be mutually exclusive. For example, the lack of high pred-
ator pressure in apes may have allowed them to develop a
more flexible and open gestural communicative system not
tied to predation.
Acquisition of Vocalizations
Vocal production, vocal usage, and responses to vocalizations
develop at different rates in primates, with vocal production
being mostly innate, though the motor patterns change with
maturation, and with usage conditions being affected more
than the motor pattern by learning (Seyfarth and Cheney
1997). For example, the grunts of infant vervetmonkeysdiffer
from those of adults. Only later do the acoustic features of
their grunts gradually come to resemble those of adults, with
the grunts used appropriately (e.g., correct usage requires that
an animal distinguish between dominant and subdominant
individuals). The genetically determined acoustic structure of
certain call types can also change as a consequence of changes
in the social environment, as described for pygmy marmosets
(Cebuella pygmaea; Snowdon and de la Torre 2002), chacma
baboons (Papio ursinus; Fischer et al. 2004), and Campbell’s
monkeys (Lemasson, Hausberger, and Zuberbu ¨hler 2005).
Further evidence for the influence of the social environment
on a genetically determined “basic pattern” of a given vo-
calization is that “coo” calls of rhesusmonkeysareacoustically
more similar within than between matrilines (Hauser 1992).
Furthermore, Japanese macaques show population-level dif-
ferences in their use of food and contact calls (Green 1975;
Sakura 1989), and population-specific “dialects” have been
described for saddle-backed tamarins (Saguinus fuscicollis;
Hodun, Snowdon, and Soini 1982) and chimpanzees (Mitani
et al. 1992).
Facial Expressions of Nonhuman
Few studies address repertoires of facial expressions in non-
human primates (Van Hooff 1962, 1967). Moreover, defini-
tions differ widely. Facial expressions may be considered ges-
tures (Maestripieri 1997; Zeller 1980) and also orofacial
actions (Ferrari et al. 2003) if their production is connected
to particular mouth movements such as “teeth chatter” or
“lip smacks.” Some authors consider facial expressions a sep-
arate category of communicative meansinadditiontomanual
and bodily gestures (Liebal, Pika, and Tomasello 2006; Van
Hooff 1962). To complicate matters further, facial expressions
are often graded, and some are closely linked to the produc-
tion of vocalizations, such as “horizontal pout face” in chim-
panzees (linked to whimpering) or “full open grin” (linked
to scream; Goodall 1986).
1056 Current Anthropology Volume 49, Number 6, December 2008
As for vocalizations, it is a matter of debate whether facial
expressions are simply affective expressions of emotional
states or whether they are intentional signals (see Caldecott
1986; Tomasello and Call 1997). A possible function of facial
expressions is to serve as “metacommunicative” signals. For
example, orangutans and chimpanzees use a “play face” when
approaching others to make sure that a hitting gesture or
wrestling is perceived as intention to play and not as an ag-
gressive approach (Bekoff and Allen 1997; Chevalier-Skolni-
koff 1994; Rijksen 1978).
A variety of facial expressions has been described for Old
World monkeys, such as macaques and baboons (Hinde and
Rowell 1962; Kummer 1957; Kummer and Kurt 1965), with
some of them being present also in great apes (Van Hooff
1962, 1967). However, because few studies investigatethevar-
iability and frequency of facial expressions, it is unclear
whether there are systematic differences in the use of facial
expressions among great apes, gibbons, and monkeys. In ad-
dition, little is known about whether and how facial expres-
sions are learned. Because rhesus macaques reared inisolation
still produce their species-specific facial expressions, there
seems to be a strong genetic component (Brandt, Stevens, and
Mitchell 1971). The question of whether these facial expres-
sions are produced voluntarily to influence others’ behavior
remains open. In humans, the motor systems controlling af-
fective facial expressions appear different from those con-
trolling voluntary facial expressions, so perhaps only the af-
fective system is operative in nonhuman primates (Gazzaniga
and Smylie 1990; Rinn 1984). Tanner and Byrne (1993) ob-
served a gorilla female who tried to hide her “play face” by
covering it with her hand, consistent with the idea that the
facial expression is less voluntary than the manual gesture.
Too little is known about how facial expressions may relate
to simultaneous gestures; this should be an object of future
Gestural Communication in Apes
The use of manual and bodily gestures to communicate with
other conspecifics has been reported for several species of
nonhuman primates. Classic studies include those of Goodall
(1986), Kummer (1968), and Van Hooff (1973; see also Hinde
and Rowell 1962; Rijksen 1978), who provided detailed de-
scriptions of different gestures (in addition to other com-
municative behaviors) used by monkeys and apes. More re-
cent studies focus on the individual variability of gestural
repertoires and the cognitive mechanisms underlying gestural
communication (for a review, see Call and Tomasello 2007).
We next focus on ape gestures and show that (1) use of
communicative gestures is common across species, (2) there
is considerable variability in gesture repertoires from group
to group, and (3) gestures are used flexibly in different con-
texts, with use depending on the behavior of the recipient.
This flexibility seems attributabletolearning.Wewillcompare
studies on gestural communication of apes both in captivity
and in the wild, including all great apes and siamangs (as
representative of the small apes or gibbons). We consider
behaviors to be gestures only if they serve to reach a recurrent
social goal and are directed at a particular recipient (for cri-
teria of gesture definition, see CA? online supplement A).
Manual and bodily gestures can be clustered into three signal
categories—auditory, tactile, and visual—depending on the
perceptual system used to receive them. Auditory gestures
generate sound (but not with vocal cords) while tactile ges-
tures include physical contact with the recipient and visual
gestures generate a mainly visual effect with no physical
Repertoire and Use
A variety of gestures is reported for gibbons and great apes
in both captive and wild populations. For siamangs, at least
20 different gestures, comprising both tactile and visual ges-
tures, were observed in different captive groups (Liebal, Pika,
and Tomasello 2004; see also Fox 1977; Orgeldinger 1999),
with similar gestures such as “embrace ” or “offer body part”
also reported for white-handed gibbons (Baldwin and Teleki
1976; Ellefson 1974). For orangutans, another arboreal spe-
cies, approximately 10 gestures are reported from wild pop-
ulations (Mackinnon 1974; Rijksen 1978), and up to 30 dif-
ferent gestures are described in captive groups (Liebal, Pika,
and Tomasello 2006; see also Becker 1984; Jantschke 1972;
Maple 1980). For gorillas, little is known about gestural com-
munication in wild populations (Fossey 1983; Schaller 1963;
Schaller 1964), but captive gorillas utilize a variety of at least
30 different tactile, visual, and, particularly, auditory gestures
(Pika, Liebal, and Tomasello 2003; Tanner 1998). Similar
numbers are reported for captive chimpanzees (Tomasello et
al. 1997, 1985; Van Hooff 1971), and Goodall(1986)mentions
a repertoire of about a dozen gestures used in a wild popu-
lation. Little is known about gestures of wild bonobos (Bad-
rian and Badrian 1984; Ingmanson 1996; Kano 1980; Kuroda
1980, 1984). The few existing studies on individuals in cap-
tivity focus on either young individuals (performing around
20 gestures; Pika, Liebal, and Tomasello 2005)orgesturesused
in particular contexts, such as sex (variety of around 20 ges-
tures; Savage-Rumbaugh, Wilkerson,andBakeman1977;Sav-
age and Bakeman 1978). De Waal (1988) found that bonobos
develop gestural repertoires (size around two dozen gestures)
similar to those of chimpanzees but described functional dif-
ferences between the two species. Play seems to be the dom-
inant context for gesture use across captive apes (if offspring
are present in a group), with the exception of orangutans,
who gesture mostly in the food context (Call and Tomasello
2007; for some examples of gestures, see CA? online sup-
plement B; for more information and recent publications
about primate gestures, see http://www.primate-gesture-
Arbib, Liebal, and Pika Primate Vocalization, Gesture, and the Evolution of Human Language1057
Variability of Gestural Repertoires
The numbers and kinds of gestures reported so far refer to
the total observed in a particular population or group. How-
ever, gestural repertoires may vary depending on the individ-
ual’s age and sex, as well as its group affiliation. For example,
Tomasello et al. (1994, 1997) observed 30 gestures in two
chimpanzee groups, but, on average, each individual used less
than one-third of this repertoire. The number of gestures
initially increases with age and then decreases again in adult-
hood (Tomasello et al. 1997). A similar pattern is found in
other ape species, including siamangs (Call and Tomasello
2007). There are also group-specific gestures performed by
the majority of individuals in one group but not in another
(Pika, Liebal, and Tomasello 2003). “Offer arm with food
pieces” in orangutans (Liebal, Pika, and Tomasello, 2006; for
an example, see CA? online supplement C), “arm shake” in
gorillas (Pika, Liebal, and Tomasello 2003), and “punch” in
bonobos (Pika, Liebal, and Tomasello 2005) are examples
reported from captive groups, while “leaf clipping” (Nishida
1980) and “grooming hand clasp” (McGrew and Tutin 1978)
are described as group-specific gestures of wild chimpanzees.
A higher degree of conformity between the gestures used
by individuals is found in siamangs and gorillas livinginsmall
and stable groups, compared with species living in a more
based fission-fusion system) and chimpanzees and bonobos
(fission-fusion system), which exhibit a considerable vari-
ability of individual gestural repertoires both within and be-
tween groups (for a detailed overview of these results, see Call
and Tomasello 2007). Although these results refer to captive
groups, they seem consistent with the hypothesisthataspecies
with more complex and negotiated social interactions should
exhibit more variability in gesture use than a species living
in small groups and/or a despotic social organization (Maes-
We next consider audience effects, in regard not only to the
presence/absence of a recipient but also to how gestures are
adjusted depending on the attentional state or behavior of
the recipient. In captivity, all apes use their visual gestures
rarely, unless the recipient is visually attending (Call and To-
masello 2007). Surprisingly, they also perform at least half of
their tactile gestures toward an attending audience, although
this was still significantly less than for visual gestures. How-
ever, both wild and captive populations use tactile and—in
case of the African great apes—auditory gestures to attract
the attention of someone who is not looking at them (Nishida
1980; Tanner 2004; Tomasello et al. 1994). Orangutans adjust
their begging gestures toward humans as a function of how
well the humans respond (Kirk et al. 2003). If great apes have
the choice of where to position themselves in relation to the
orientation of a human experimenter to produce their ges-
tures, they walk in front of the humaninsteadofmanipulating
his or her state of attention by using gestures behind him or
her (Liebal et al. 2004).
Referential Use of Gestures
There are few data on the referential use of gestures, and most
of the existing literature concerns “pointing” gestures of cap-
tive chimpanzees (Leavens, Hopkins, and Thomas 2004). In
a recent study,Pika andMitani(2006)describethewidespread
use of a gesture, the “directed scratch,” in chimpanzees in the
wild. This gesture involved one chimpanzee making a rela-
tively loud and/or exaggerated scratching movementonapart
of his body that could be seen by his grooming partner. In
the majority of the cases, the indicated spot was groomed
directly by the recipient. These observations suggest that this
gesture is understood by receivers as referential(althoughself-
referential) because it indicates a certain spot on the body
and therefore creates a triadic communication (for an ex-
ample, see CA? online supplement D).
Iconic gestures relate to their referent by some actual phys-
ical resemblance such as a desired motion in space or the
form of an action (Bates et al. 1979). Although iconic gestures
have been reported in one bonobo and one gorilla (Tanner
and Byrne  reported that an adult gorilla male seemed
to signal with his hand, arm, or head to a playmate the di-
rection in which he wanted her to move or the action he
wanted her to perform), these observations have not been
observed in other groups of bonobos or gorillas.
Acquisition of Gestures
Different mechanisms have been suggested for how nonhu-
man primates acquire their gestures during ontogeny, in-
cluding genetic determination, ontogenetic ritualization, and
social learning. Isolation experiments with rhesus macaques
show that they still perform species-typical gestures and pos-
tures (Mason 1963), suggesting that the basic form of these
communicative behaviors is geneticallypreprogrammed.Sim-
ilarly, “chest beat” is reported for two gorillas that had never
seen another gorilla perform these gestures (Redshaw and
Locke 1976). Berdecio and Nash (1981) observed that chim-
panzees from peer groups that have essentiallynoopportunity
to observe older conspecifics develop many of the same play
gestures as individuals from groups with more natural group
composition. Thus, the production of at least some species-
typical gestures seems to be due to genetic predisposition,
triggered by commonly available individual learning condi-
tions, as in Seyfarth and Cheney’s (1997) model of vocal
However, there is good evidence that great apes can also
invent or individually learn new gestures. Idiosyncratic ges-
tures, used only by single individuals within a group and
which therefore could not have been either genetically deter-
mined or socially learned, are reported for all great apespecies
1058 Current Anthropology Volume 49, Number 6, December 2008
in captivity (Liebal, Pika, and Tomasello 2006; Pika, Liebal,
and Tomasello 2003, 2005; Tomasello et al. 1997) and also
for chimpanzees in the wild (Goodall 1986). Moreover, these
gestures were used to achieve a certain social goal and most
often caused a response of the recipient (Pika, Liebal, and
Tomasello 2003). Thus, these individual gestures can be in-
tegrated into the group’s gestural repertoire.
Tomasello and Call (1997) argue that the majority of novel
gestures are learned via an individual learning process called
ontogenetic ritualization. Here, a communicativesignaliscre-
ated by two individuals shaping each other’s behavior in re-
peated instances of an interaction over time. For example,
play hitting is an important part of the rough-and-tumble
play of chimpanzees, and many individuals come to use a
stylized “arm-raise” to indicate that they are about to hit the
other and thus initiate play (Tomasello et al. 1997). Thus, a
behavior that was not at first a communicative signal would
become one over time. However, there are also group-specific
gestures that are widely used within groups, leaving room for
social learning to complement ontogenetic ritualizationinthe
acquisition of some gestures in great apes in the wild and
captivity. Unfortunately, there are no longitudinal studies in-
vestigating the ontogeny of gesture use in nonhuman pri-
mates, and existing data seem to indicate a mix of different
One needs to be cautious about overgeneralizing the pat-
terns observed in captive versus wild individuals. However,
some studies report that gestural repertoires are comparable
between wild and captive individuals (for siamangs, see Fox
1977), although captive individuals, compared withwildones,
might use their gestures with a higher frequency (Kummer
and Kurt 1965). Even if gestures might be less significant in
the wild, it is striking that in captivity gestures can be found
in such a variety and a high degree of variability in relatively
small groups of apes, proving that gestures provide very flex-
ible and effective communicative means thatcandevelopeven
within short time spans.
Comparing Communication Systems in
Monkeys and Apes
Little is known about gestural communication in monkeys.
Although there are a few studies describing gestures in hama-
dryas baboons and rhesus macaques (Hinde and Rowell 1962;
Kummer 1957), the only systematic studies on monkey ges-
tural communication concern macaques (Macaca nemestrina,
Macaca arctoides, Macaca mulatta [Maestripieri 1996a, 1996b,
1997, 1999], and Macaca sylvanus [Hesler and Fischer 2007]).
Each species uses a variety of manual gestures and postures;
the kinds of gestures individuals produce vary as a function
of social context and rank (Maestripieri 1999), and they are
used flexibly across a number of different contexts (Hesler
and Fischer 2007). However, these studies alsoshowthatfacial
expressions seem to be important communicative means in
monkeys. Thus, although many facial expressions are shared
by monkeys and apes (Van Hooff 1962, 1967), it seems that
facial expressions in monkeys are more prominent than in
great apes (Liebal 2005). When comparing the kinds of ges-
tures used in captive monkeys and apes, there seems to be a
trend toward manual gestures in apes compared with the
predominant use of postures in monkeys (Call and Tomasello
2007). However, more systematic studies are needed to ad-
dress monkey gestural communication.
Facial expressions accompany both spoken and signed lan-
guages in humans but have never served to form a fully ex-
pressive language of their own. Thus, while facial expressions
are important in communication (e.g., as expressions of emo-
tional states) and in “modulating” language, their study is
secondary to the primary aim of this article—namely,toassess
whether nonhuman primate vocalizations or manual gestures
are evolutionarily closer to the conventionalized symbol use
of human language. Therefore, we set aside further consid-
eration of facial expressions.
There is an ongoing debate about whether and to what
extent nonhuman primate vocalizations are intentional, vol-
untarily controlled communicativemeans(TomaselloandZu-
berbu ¨hler 2002). Although vocalizations seem to be largely
innate, with a limited number of vocalizations in an individ-
ual’s repertoire, there is flexibility in regard to the usage and
comprehension of vocalizations, with some species even com-
prehending the calls of other species, which requires learning
(Zuberbu ¨hler 2000a). In addition, there is some variation in
certain calls as a function of population-specific dialects (Mi-
tani, Hunley, and Murdoch 1999) or affiliation to a particular
matriline (Hauser 1992).
Gestures are used intentionally and flexibly in the sense
that they are directed to a specific recipient; they are adjusted
to the behavior of the recipient, and one gesture can be used
to achieve different goals in different contexts. Both gestures
and vocalizations do occur as part of combinations or se-
quences (Crockford and Boesch 2005; Liebal, Call, and To-
masello 2004; Tanner 2004), with evidence that different types
of combinations of vocalizations—but not gestures—convey
different meanings. However, as we will discuss, such com-
binations are few and lack the generativity of the syntax of
For us, the crucial differences between gestures and vo-
calizations are that (1) gestural repertoires are open to in-
corporation of new gestures at both an individual and a pop-
ulation level; (2) there is a high degree of individual variability
of gestural repertoires not only regarding age classes (asmight
also be the case for vocalizations) but also between different
groups or populations, due to both ontogenetic ritualization
and, to a lesser extent, social learning and emergence of id-
iosyncratic gestures; and (3) gestures are used to address one
particular recipient rather than being broadcast, as is the case
for most vocalizations. We thus argue that these gestures dis-
play a flexibility lacking in nonhuman primate vocalizations.
This is supported by a recent study (Pollick and De Waal
2007) showing that gestures are used more flexiblythanfacial/
Arbib, Liebal, and Pika Primate Vocalization, Gesture, and the Evolution of Human Language1059
vocal signals in captive chimpanzees and bonobos. Homol-
by both ape species.
Comparing Gestural Communication in
Apes and Humans
We stressed in the introduction to this article that gesture is
an important part of language use in humans, with speech
often accompanied by facial gestures that add emotional ex-
pression, as well as the hand movements known as cospeech
gestures. Both of these facts seem to comport better with a
view of language evolution that sees an important role for
gesture than with one that seeks to trace a “voice-only” path
from nonhuman primatevocalizationstolanguageconsidered
solely as speech. However, we postpone further development
of this argument until “Implications for the Evolution of
Language.” “Comparison of Ape Gestures with Gestures in
Prelinguistic Human Children” offers a comparison of the
use of gestures in apes with the gestural communication of
prelinguistic or just-linguisticchildren—cospeechgesturesare
not discussed—and a perspective on gesture by distinguishing
dyadic from triadic gestures. Then in “Teaching ‘Language’
to Apes,” we turn to attempts to teach “language” (speech
and gestures) to apes and show that enculturation with hu-
mans gives apes a different gestural repertoire than that ex-
hibited by wild individuals or even by individuals raised in
captivity without human fostering. The discussion will there-
fore help us understand how much of complex behavior re-
quires not only a brain with appropriate capabilities but also
an environment that enables specific capabilities to develop
in specific ways.
Comparison of Ape Gestures with Gestures in Prelinguistic
Gestures of children can be differentiated with respect to the
direction and type of gesture used (Bates 1976). The direction
of gestures includes both dyadic and triadic interactions. Dy-
adic gestures are exchanged between two individualsandserve
to attract the recipient’s attention toward the acting individ-
ual, whereas triadic gestures incorporate an external object or
event into the interaction of two individuals and are used to
attract the attention of the partner to this outside entity. Tri-
adic gestures may be classified as referentialgestures(see“Ref-
erential Use of Vocalization”forvocalizationsand“Referential
Use of Gestures” for gestures) and begin to appear in human
children by the age of 12 months (Liszkowski et al. 2004).
The use of referential gestures has been linked with cog-
nitive capacities, such as mental state attribution (Camaioni
1993; Tomasello 1995), because the recipient must infer the
signaler’s meaning. Triadic gestures include both imperative
and declarative gestures. Imperative gestures are used to get
another individual to help in attaining a goal (Pika 2008a),
whereas declarative gestures are used to draw another’s at-
tention to an outside entity to share attention (e.g., holding
up an object and showing it; Pika 2008b). Plooij (1979, 1987)
observed mother-infant dyads of wild chimpanzees and ar-
gued that only between the ages of 9 and 12.5 months does
the chimpanzee infant start to initiate interactions with its
mother by intentionally directing signals to her, for example,
by using gestures such as “initiating tickling,” “grooming,”
and “approach.” Only then does the chimpanzee infant act
as if it understands its mother and conspecifics as social
agents. This developmental stage marks the onset of the use
of imperative gestures and the developmental shift from per-
locutionary acts (where communication occurs only because
the receiver is adept at interpreting the behavior of the sig-
naler, in this case, the infant) to illocutionary acts in which
the signaler directs his or her behavior toward a recipient.
As opposed to gestures of prelinguistic human children,
the majority of gestures used in interactions between great
apes can be defined as dyadic (Pika et al. 2005). Thus, asender
directs a certain gesture toward a particular recipient, with
the gesture not involving an object or another outside entity.
Some of the gestures apes use to attract the attention of others
are “slapping the ground” in front of the recipient and “pok-
ing at” or “throwing” things at the desired partner when they
want to initiate play (Tomasello, Gust, and Frost 1989). These
gestures are of a triadic nature but draw, similarly to human
utterances such as “Hey,” the attention to oneself and not to
a third entity or an object (Pika et al. 2005). Moreover, chim-
panzees do not use gesture combinations as a strategy to
manipulate the attentional state of a recipient (Liebal, Call,
and Tomasello 2004). Thus, the majority of gestures used
between great apes in their natural communicationaredyadic
rather than triadic (Pika et al. 2005). Exceptions are the ges-
tures “food-begging” (an animal holds out the hand, palm
up to obtain food from another; for orangutans, see Bard
1992; for chimpanzees, see Tomasello et al. 1994),“foodoffer”
(an animal offers food placed on its hand to another animal),
and “present object” (an individual holds an object in front
of another animal; Liebal, Pika, and Tomasello 2006). These
gestures are clearly triadic. Another example is pointing, but
as opposed to the previously mentioned gestures, it is de-
ployed mainly by apes when interacting with humans (Leav-
ens, Hopkins, and Bard 1996, 2005; Leavens, Hopkins, and
Thomas 2004) or by language-trained apes (e.g., Gardner and
Gardner 1969; Miles 1990; Patterson 1978a; Woodruff and
Premack 1979). There are also few reports of pointing for
conspecifics in captive and wild chimpanzees (de Waal 1982;
Inoue-Nakamura and Matsuzawa 1997) and wild bonobos
(Vea and Sabater-Pi 1998). It is important to note that apes
in captivity usually point with their whole hand, not with
their index finger (Leavens and Hopkins 1999). According to
Leavens, Hopkins, and Thomas (2004), this behavior serves
a communicative function rather than a mere reaching for
food that is out of reaching distance, as argued by Povinelli
and Davis (1994). (Note that pointing in humans varies be-
tween different cultures and is not restricted to index finger
1060 Current AnthropologyVolume 49, Number 6, December 2008
pointing but can include pointing involving other body parts,
such as lip pointing; Enfield 2001; Kita 2003).
Teaching “Language” to Apes
Leavens, Hopkins, and Bard (2005) argued that pointing in
captive apes is attributable to environmental influences on
their communicative development. Another suggestion isthat
apes do not point for conspecifics because they do not have
the motive to help or inform others or to share attention and
information (Tomasello et al. 2005). The discussion makes
clear that the communicative capacities of wild apes can be
augmented by raising them with humans in part because
humans respond in ways that apes do not. But what kinds
of attempts have been made to teach apes to use human
language? This bears on the issue of to what extent human
language is a biological inheritance and to what extent it
reflects the cumulative effects of a society’s history.
Attempts to teach apes to speak have failed repeatedly (e.g.,
Hayes and Hayes 1951; Kellog and Kellog 1933). Gardner and
Gardner (1969) tried to overcome nonhuman primates’ dif-
ficulties in speech production by teaching AmericanSignLan-
guage (ASL) to a chimpanzee, Washoe (but see also Fouts
and Budd 1979). Washoe did indeed learn a number of such
signs, and this success led to similar projects with a gorilla,
Koko (Patterson 1978b), and an orangutan, Chantek (Miles
1990). Other attempts to overcome the speech barrier were
made by Premack (1976), who used plastic tokens to stand
for spoken words in communicating with the chimpanzee
Sarah. In addition, Rumbaugh (1977) created a visual lan-
guage based on graphic symbols (lexigrams) depicted on a
computerized keyboard for the chimpanzee Lana. Impressive
results have come from the bonobo Kanzi, who spent the first
2.5 years of his life observing his mother, Matata, while she
was interacting with humans around the computerized key-
board (e.g., Greenfield and Savage-Rumbaugh 1990; Savage-
Rumbaugh and Brakke 1992; Savage-Rumbaugh, Shanker,
and Taylor 1998). Kanzi learned many of the lexigrams that
his mother had not, which implied that he had acquired them
spontaneously by observing others without any specific train-
ing. A similar process is known from human children (Bruner
1983; Lock 1978), who also acquire most of their early lin-
guistic abilities without explicit training but rather as a result
of highly predictable, routine interactions with adults. Kanzi’s
early vocabulary resembled that of human children, including
names for individuals; labels for common objects; words for
actions, locations, and properties; and even a few function
words such as “no” and “yes.” His ability to understand En-
glish is comparable to that of a 2-year-old (but not older)
human child (Savage-Rumbaugh et al. 1993), and he under-
stands lexigrams as symbols in the sense that he uses them
in absence of a particular referent and in a decontextualized
manner. Referential abilities and increasing decontextualiza-
tion are also reported for a sign language–trained orangutan,
Chantek (Miles 1990).
In regard to the combinatorial aspect of symbolic com-
munication, Fouts (1974) and Gardner and Gardner (1969)
describe the spontaneous nonrandom combination of signs
in ASL-using chimpanzees. However, this is not sufficient for
grammar. The relationship between the symbols must be
meaningful and reliable, a rule must specify the relations be-
tween categories of symbols across combinations, and the
rules must be creative and productive (Terrace et al. 1979).
About 10% of Kanzi’s utterances at age 5.5 years consisted
of combinations of two or three lexigrams or a lexigram plus
a gesture (Greenfield and Savage-Rumbaugh 1990), and he
not only ordered actions but also invented his own rules.
Greenfield and Savage-Rumbaugh argue that the capacity of
Kanzi for some “grammatical” rules represents a “protogram-
mar,” indicating an evolutionary continuity with certain lin-
guistic skills. However, compared with human children, apes
acquire symbols at a much slower rate and also have a much
smaller repertoire (Bonvillian and Patterson 1999; Greenfield
and Savage-Rumbaugh 1990). In addition, many of their ut-
terances represent requests and not statements or indicatives
(Bonvillian and Patterson 1999). Rivas (2005) concludes that
chimpanzees using ASL predominantly performed object and
action signs, with no evidence for semantic or syntactic struc-
ture in combinations of signs. Some authors conclude that
differences between the linguistic skills of nonhuman and
human primates are quantitative rather than qualitative (Gib-
son 1990). However, “ape language” lacks the open-ended
ability to build sentences hierarchically with a compositional
semantics—that is, in such a way that the meaning of the
sentence can be reconstructed from the meaning of its com-
ponents by inferring how the sentence was put together. With
this background, we can return to our discussion of the evo-
lution of language.
Implications for the Evolution of
In the introduction to this article, we noted that many re-
searchers turned to the vocal signals of nonhuman primates
as the direct basis for the evolution of human speech. How-
ever, we stressed that human language use is multimodal, so
that any theory of language origins must include gestures as
a crucial part of the human “language performance system.”
We briefly recalled a number of theories laying out a gestural
origin for human language, including our own “modified
gestural origins” theory, the mirror system hypothesis. The
aim of this article has been to provide a thorough review of
the data on vocal, facial, and gestural communication in non-
human primates as the basis for an examination of the light
they shed on such theories and the standing of such theories
with respect to the “direct path from vocalization” theories.
As such, we aim for a focused analysis of just a few issues in
Arbib, Liebal, and Pika Primate Vocalization, Gesture, and the Evolution of Human Language1061
the debate on language origins rather than a comprehensive
From Imitation to Pantomime: The Roots of Syntax
Despite the ability of enculturated apes to combine signs to-
gether in an “utterance,” there is no evidence that they have
the ability to employ syntax to create and re-create novel
utterances that inherit their new, overall meaning from their
parts via a compositional semantics. The current version of
the mirror system hypothesis (Arbib 2005a)rootstheessential
difference in a change in skills in imitation. Where this hy-
pothesis sees increased skill in imitation of manipulative skills
as the basis for generalizationto communicativeskills,Donald
(1991) places more emphasis on a general mimetic ability. In
any case, we distinguish (i) “simple” imitation (shared with
apes) that allows single actions to be acquired (more or less)
in around 15 trials (Myowa-Yamakoshi and Matsuzawa 1999)
and complex skills, such as strategies for feeding on nettles,
to be acquired only after months of exposure to the behavior
(Byrne 1999a; for related discussion, see Custance, Whiten,
and Bard 1995; Russon 1996; Whiten 1998) from (ii) “com-
plex” imitation (Arbib 2002), the capacity for recognizing
novel actions as approximated by a combination of variants
of known goal-directed actions. The overall action can thus
be imitated immediately, though probably not skillfully at
first. Wohlschla ¨ger, Gattis, and Bekkering (2003) enrich this
characterization with their notion of goal-directed imitation.
In their view, imitation is the result of perceiving an action
in terms of a (possibly incomplete, possibly erroneous) hi-
erarchical structuring of subgoals. Through these processes of
successive approximation, a complex action can be repro-
duced with increasing accuracy by increased attention being
paid to its subparts. This increased attention may result in a
finer-scaled decomposition of the observed movement, re-
sulting in execution of a more congruent behavior.
Complex actions, then—and producing a sentence in a
modern human language is a complex action—involve sub-
actions as well as actions, subgoals as well as goals.Thehuman
capacity for complex, goal-directed imitation exhibitstwoim-
portant properties: (a) humans can get aroughunderstanding
of the structure of the behavior in a single exposure, with the
overall program being “debugged” on subsequent exposures,
rather than taking months, as in gorillas learning feeding
behaviors (Byrne 1999b), and (b) humans can do it for all
sorts of behaviors rather than a limited set of feeding behav-
iors. Wohlschla ¨ger, Gattis, and Bekkering (2003) attribute dif-
ferences in imitative abilities across species to differences in
working memory capacity. However, differences in imitative
ability could also involve differences in the mechanism(s) of
hierarchical decomposition of observed performances as well
as working memory for the results (whether in planning or
The version of the mirror system hypothesis given byArbib
(2005a) posits an evolutionary progression of neural systems
from simple imitation of manual praxic actions (shared with
the great apes but not monkeys) to complex imitation of man-
ual praxic actions (unique to the human line) and only then
turns to the evolution of communication via pantomime to
protosign and beyond. However, the data reviewed in this
article suggest that simple imitation in apes should be ex-
tended from manual praxic actions to include manual com-
municative gestures but not, to any great extent, vocalizations.
(While some imitation-like behaviors have been observed in
monkeys [Voelkl and Huber 2000, 2007], they seem toinvolve
facilitation of use of effectors—e.g., the use of the mouth
rather than the hand to remove a lid—rather than the imi-
tation of specific [combinations of] actions.) In short, non-
human primates have little or no capacity for vocal imitation,
but apes can indeed acquire novel gestures through some
combination of ontogenetic ritualization and a form of social
learning akin to what we have called simple imitation (Byrne
and Tanner 2006). However, whereas the demands of praxic
action lead to inherently hierarchical behaviors as targets for
imitation by behavior parsing, the use of gesturebyapesoffers
little in the way of compound gestures—beyond those cases
where an ape performs gestures one after the other when the
recipient does not react.
Our analysis of the data on communication in nonhuman
primates thus suggests that it is gesture rather than vocali-
zation that extended the ability for simple imitation in apes
into the communicative realm. This insight, missing in Arbib
(2005a), yields theopeningforgreatlyexpandedgesturalcom-
munication once complex imitation had evolved for practical
manual skills. We posit an evolutionary progression of neural
systems unique to the human line that build on those sup-
porting complex imitation to yield (following the numbering
adopted in Arbib 2005a): (S5a) pantomime of grasping and
manual praxic actions; (S5b) pantomime of actions outside
the pantomimic’s own behavioral repertoire (e.g., flapping
the arms to mime a flying bird); (S5c) protosign, conventional
gestures used to formalize, disambiguate, and extend pan-
tomime (e.g., to distinguish “bird” from “flying”) that estab-
lish an ability for the free creation of arbitrary gestures to
support an open-ended semantics; and, finally, (S6) protolan-
guage, a multimodal system created once protosign, after hav-
ing achieved some critical mass, and protospeech (the capacity
to use vocal communicative gestures) evolve together in an
The argument for the utility of pantomime (Arbib 2002;
Stokoe 2001) is that it provides an “open semantics,” allowing
a large set of novel meanings to be communicated, especially
as stage S5b expands on stage S5a. However, such pantomime
is inefficient, both in the time taken to produce it and in the
likelihood of misunderstanding. This motivates the postula-
tion of stage S5c, as a group uses conventionalized signs to
extend and exploit more efficiently the semantic richness
opened by pantomime. Here, processes such as ontogenetic
1062 Current Anthropology Volume 49, Number 6, December 2008
ritualization convert elaborate pantomimes into a conven-
Vocalization versus Gesture in the Evolution of Language
We have argued that the successful use of gesture, via pan-
tomime and an ability for complex imitation, was essential
to the evolution of a protohuman brain that could support
the open-ended expression of meaning by the compounding
of gestures and that this capability provided the essential scaf-
folding for protospeech and the evolution of the human lan-
guage-ready brain. However, we must now see how well this
stands up against the argument that elaborations purely in-
trinsic to the core vocalization systems could have provided
the basis for the evolution of brain mechanisms supporting
speech. We focus our attention on a few of the strongest
arguments for this view.
Cheney and Seyfarth (2005) argue that brain mechanisms
for language evolved from the call systems of nonhuman pri-
mates without involvementofmanualgesturebecause(i)even
though nonhuman primate vocal repertoires contain several
different call types that grade acoustically into one another,
nonhuman primates produce and perceive their calls as more
or less discretely different signals; (ii) different call types are
given in different social contexts and listeners respond ap-
propriately; and (iii) the grunts used by baboons (and prob-
ably many other nonhuman primates) differ according to the
placement of vowel-like formants. However, our view is that
these data may be relevant to the evolution of the articulatory
apparatus rather than that of language.
Cheney and Seyfarth (2007), using controlled playback ex-
periments, have also established that various calls are related
to the social dominance hierarchy: baboons react more
strongly to splices of calls of individuals who are not in the
appropriate dominance relationship. Noting parallelsbetween
social structure and language structure, Cheney and Seyfarth
(2005) hypothesize that enrichment of vocalizations for social
communication provides the path to speech. However, rec-
ognizing the calls of individuals is a far cry (so to speak) from
developing vocalized names for individuals or for expressing
explicitly the relations between them. Nonhuman primates
can explicitly express through their system of shared com-
municative signals only a small fraction of whattheirbehavior
demonstrates that they understand, whereas humans can ex-
press vastly more aspects of how and why they behave and
can also communicate about situations and abstractions far
beyond the here and now.
But perhaps monkey vocalizations share more properties
with language than our review makes clear. Although most
monkey calls are emitted with no particular order but rather
as the context demands, there is some evidence for limited
combinations (but not combinatory rules) in monkey vocal
utterances. Zuberbu ¨hler (2002) demonstrated that in Diana
monkeys in the wild, one specific call may act as a semantic
modifier of another. They respond to the “eagle” alarm call
of Campbell’s monkeys with their own alarm calls. In situ-
ations that are less dangerous, Campbell’s monkeys combine
the eagle alarm call with a so-called boom. Zuberbu ¨hler
their eagle or “leopard” alarm calls and played them back to
Diana monkeys. These calls no longer elicited alarm calls in
Diana monkeys, indicating that the booms had affected the
“meaning” of the subsequent alarm calls. When the booms
preceded the alarm calls of Diana monkeys, however, they
were no longer effective as semantic modifiers, indicating that
the semantic modification is specific to Campbell’s monkey
Arnold and Zuberbu ¨hler (2006a, 2006b) found that male
putty-nosed monkeys regularly combine “pyow” and “hack”
calls into “pyow-hack” sequences, which usually consist of
one, two, or three pyows followed by up to four hacks. They
demonstrated that this combination is linked to specific ex-
ternal events, such as the imminent movement of the group.
The authors argue that “combining existing calls into mean-
ingful sequences increases the variety of messages that can be
generated” and suggest that nonhuman primatescancombine
calls into higher-order sequences that have a particular mean-
ing (Arnold and Zuberbu ¨hler 2006b, 303). However, there is
no evidence of the compositionality essential to language—
having a few sequences with a well-defined meaning does not
qualify as syntax.
With this, let us return to our study of nonhuman primate
gestures. We provided evidence that apes use more manual
gestures than monkeys (e.g., Maestripieri 1999). However,
apes do not seem to have a more varied repertoire of orofacial
gestures. Indeed, monkeys (in particular macaques and ba-
boons) have a variety of facial expressions, and some of them
cannot be found in great apes (Van Hooff 1967). If we con-
sider the close relationship between apes and humans, the
increased use of the hands in apes compared with body pos-
tures and facial expressions in monkeys might be due to a
shift from facial expressions (under less voluntary control) to
more manual gestures (under voluntary control) over the
course of evolution. Therefore, manual gestures may have
played a role in the common ancestor of apes and humans
as well. An alternative is that the use of manual gestures in
apes presents a trait independent of the use of orofacial ges-
tures and is irrelevant to human multimodal communicative
behavior. However, because manual gestures still play an im-
portant role in human communication (McNeill 1992), this
seems less likely. Thus, we argue that it is enrichment of the
manual rather than the orofacial repertoire, exploiting the
extended capability for complex imitation, that grounded the
foundational semantics for an open-ended set of protosign
utterances (stage S5c) and that the dramatic changes in vocal
apparatus and its control (stage S6) were secondary devel-
opments in hominid evolution, driving rather than driven by
expansion of the monkey orofacial repertoire.
Manual gestures in humans can have an effect on vocali-
Arbib, Liebal, and Pika Primate Vocalization, Gesture, and the Evolution of Human Language1063
zations made at the same time, thus creating certain natural
vocal concomitants of manual efforts (Gentilucci et al. 2004a,
2004b). Chimpanzees execute sympatheticmouthmovements
during fine motor manipulations (Waters and Fouts 2002).
These results suggest that the emergence of voice modulation
and thus of an articulatory movement repertoire could have
been associated with or even prompted by the preexisting
manual action repertoire (for further discussion, see Roy and
Arbib 2005). Such mechanisms may have played an evolu-
tionary role in enabling the development of intentional vocal
communication atop a base of gestural communication (Gen-
tilucci and Corballis 2006).
With this, we leave aside considerations that may anchor
stage S6 and turn to what may have been communicated in
protosign. Recall that apes use their gestures mainly imper-
atively (Pika et al. 2005), whereas human children gesture for
declarative purposes and to direct the attention of others to
an outside object or event (Bates, Camaioni, and Volterra
1975; Liszkowski et al. 2004). We saw in “Teaching ‘Language’
to Apes” that the communicative capacities of apes in the
wild can be augmented by raising them with humans in part
because humans respond in ways that apes do not. The com-
munication about outside entities may be central to the use
a crucial difference between natural ape communication and
the communication between humans and of apes with hu-
mans. We may also note the cognitive ability of humans to
understand other persons as intentional agents with whom
they may share a goal (Tomasello et al. 2005), an ability that
is still highly debated in nonhuman primates (e.g., Heyes
1998; Pika and Zuberbu ¨hler 2007; Povinelli and Vonk 2003;
Seyfarth and Cheney 2008; Tomasello, Call, and Hare 2003).
Conversely, an ability to communicate a wider range of im-
peratives symbolically might have increased the need to com-
municate about more objects to which the desired actions
should be directed. Imagine that there were protowords like
the English “punch” and “kick.” The transition we are hinting
at here would be discovering the general construction “hit
with your x” and developing new words “x” for “hand” and
“foot” and then many more besides. These x’s could then be
used in turn with other predicates. This in turn would en-
courage triadic, referential communication that could then
be expanded for purely declarative purposes. This propensity
might also express the need to create a medium for the eval-
uation of social bonds in humans, to testandstrengthensocial
relationships, and thus to share experiences as part of a social
relationship. In our closest relatives, bonobos and chimpan-
zees, social grooming permeatesvirtuallyeveryaspectofsocial
life. It might therefore represent their medium to evaluate
and to invest into social relationships (Dunbar 1996; Pika
2008b). We are back to the importance that Cheney and Sey-
farth (2005) ascribe to social structure for the emergence of
language structure—but now with gesture rather than vocal-
ization being the prime vehicle for this emergence.
For lively discussion and/or comments on earlier drafts, we
thank K. Arnold, D. Haun, H. Lyn, R. Seyfarth, and K. Zu-
berbu ¨hler. We also thank all of the anonymous reviewers for
a range of helpful criticism and suggestions.
Michael C. Corballis
Department of Psychology, University of Auckland, Private
Bag 92019, Auckland 1142, New Zealand (m.corballis@
auckland.ac.nz). 12 VIII 08
The article by Arbib, Liebal, and Pika adds to the growing
evidence and opinion that human language evolved from
manual gestures and not from vocal calls. The authors have
provided an especially thorough and pertinent review of pri-
mate vocalization, facial gestures, and manual gestures. Iron-
ically, this review suggests more flexibility and learning in
primate vocalizations than hitherto recognized, even to the
point of giving at least some encouragement to those, such
as Cheney and Seyfarth (2005), who still argue that language
evolved from primate calls. Perhaps the clinching argument
for the gestural hypothesis, though, is the at least moderate
success in teaching great apes forms of gestural language,
whether through signing or through pointing to visual sym-
bols, compared with the almost total failure of teaching them
The gestural theory is further supported by evidence as to
the nature and timing of anatomical changes in hominin evo-
lution. According to most accounts, the hominins were dis-
tinguished from the other great apes by being bipedal (but
see Thorpe, Holder, and Crompton 2007), which must surely
have enhanced the possibilities of communicating through
manual gesture more than it would have influenced the vocal
repertoire. The early hominins, though, were facultative bi-
peds, and Donald (1991) proposed thatthepantomimicphase
probably originated with the genus Homo from around 2
million years ago, when bipedalism switched from facultative
to obligate. At this time, too, brain size began its dramatic
increase. In contrast, anatomical and neurophysiological ad-
aptations for articulate vocalization probablyarosemuchlater
and possibly only within the past 200,000 years, with the
emergence of Homo sapiens. In a recent review, Lieberman
(2007, 39) suggests an even more extreme scenario: “fully
human speech anatomy first appears in the fossil record in
the Upper Paleolithic (about 50,000 years ago) and is absent
in both Neanderthals and earlier humans.”
Some have argued that language itself emerged only in our
own species (e.g., Bickerton 1995; Crow 2002). If we consider
the complexity of human language, the more likely scenario
is that it evolved gradually over the past 2 million years,
1064Current Anthropology Volume 49, Number 6, December 2008
perhaps originating in a predominantly gestural form but
gradually incorporating vocal elements, with vocal speech as-
suming dominance only in our own species. This, in turn,
would have released the hands from involvement in vocali-
zation, leading to an enhancement of manufacture and ped-
agogy. Speech rather than language per se might then explain
how our species progressed to what has been termed “mo-
dernity” (e.g., Stringer 2002), perhaps through the release of
the hands from primary involvement in communication. The
rise of what hasbeentermed“modernity”inourspeciesmight
then be attributed not to language per se but to the emergence
of autonomous speech (Corballis 2004).
The authors do not consider the question of what actually
drove language beyond simple pantomime or protolanguage
to compositional structure. At one point, though, they refer
to communication “about situations and abstractions far be-
yond the here and now.” This may relate to the suggestion
that grammatical language may have coevolved with mental
time travel, also perhaps a uniquely human capacity (Sud-
dendorf and Corballis 2007). Mental time travel includes ep-
isodic memory and the construction of possible future epi-
sodes, both of which have compositional structure. Language
seems purpose built for the communication of episodes, even
fictional ones, with its corresponding structure, mechanisms
for coding time (e.g., tense), and use of symbols to represent
episodic elements (actors, acts, patients, etc.; Corballis 2008).
The emergence of compositional structure, I suggest, co-
evolved with mental time travel during the Pleistocene and
preceded the emergence of speech as the dominant language
Department of Social Sciences, Media, and Cultural
Studies, University of East London, London E16 2RD, UK
(firstname.lastname@example.org). 26 VIII 08
Arbib, Liebal, and Pika provide an excellent—and long over-
due—comparative survey of the incidence of gestural versus
vocal communication in nonhuman primates. I like theirpro-
posal that the primate mirror neuron system underpinning
gestural imitation played a key role in enabling language par-
ity. I am also persuaded by their more general argument that
the emergence of vocal speech in our ancestors in some way
presupposed the scaffolding provided by gesture and then
Unfortunately, the article ends rather abruptly, having of-
fered little that merits description as an actual theory. The
authors address a range of “what,” “when,” and “how” ques-
tions yet never ask the crucial question “Why?” Yes, apes in
general do lack volitional control over their vocal signals. Yes,
they do seem to have much greater control over their manual
gestures. And, yes, manual gestures in humans “can have an
effect on vocalizations made at the same time, thus creating
certain natural vocal concomitants of manual efforts.” It
would therefore follow logically that one way an intelligent
primate might enhance cognitive control over its vocal sig-
naling would be by intentionallyjumpingaroundorotherwise
manipulating its body so as to influence any sounds being
emitted at the same time.
But all this strikes me as a strangely mechanistic approach
to the theoretical difficulties—as if no ape or monkey ever
thought to modulate its vocal signals by deploying the equip-
ment it already has. There must surely be some moreplausible
reason why these animals in fact do not play around creatively
or imaginatively with vocal communication. After all, young
primates can be strikingly creative and imaginative in their
playful antics. In the interests of masticatory efficiency, more-
over, they possess jaws, lips, and tongues that are subject to
fine motor control. Little effort is needed to activate the rel-
evant mouth muscles. If greater signal flexibility would be
adaptive, why notusesuch ready-made,highlyefficientequip-
ment to modulate sounds in the way humans do?
Instead of restricting ourselves to yet another description
and classification of signaling modalities and corresponding
mechanisms, we surely need some Darwinian thinking here.
Among nonhuman primates, what selection pressures might
have rendered it adaptive for vocal communication to be so
strikingly insulated from cognitive control? What fitness ad-
vantages might accrue to an intelligent ape from its inability
to play around with its vocal signals? Such questions cry out
for an answer. If we do not even address them, we are unlikely
to get far in elucidating the evolutionary relationships among
primate vocalization, primate gesture, and speech-based hu-
The ability to engage in pantomime is, by definition, an
ability to fake one’s bodily signals and displays. For patent
fakes to be accepted as valid currency for purposes of com-
munication, unusually high levels of social cooperation and
corresponding trust must be assumed. This presents a the-
to deploy such potentially deceptive strategies will also be
clever enough to competitively exploit the trust presupposed
by their habitual use (Knight 1998). This could explain why,
despite their quite developed capacities for deploying and
comprehending symbolic conventions when in captivity,non-
human primates apparently find so little use for symbolic
communication in the wild (Ulbaek 1998).
What would happen if a Machiavellian mutant monkey did
discover that it could freely substitute one predator alarm call
for another, regardless of the presence of any actual threat?
Insofar as the fakes were exploited for purposes of tactical
deception, they would lose their former status as reliable—
hence meaningful—signals. To the extent that salient aspects
of any signal can be intentionally faked, conspecifics will sim-
ply ignore those variable aspects in favor of any hard-to-fake
acoustic features that might prove unintentionally significant.
In a Darwinian social world, selection pressures will in this
way drive signalers to persuade receivers of the reliability of
Arbib, Liebal, and Pika Primate Vocalization, Gesture, and the Evolution of Human Language1065
their signals by demonstrating precisely that they are not sub-
ject to cognitive control.
This will apply in particular to vocal signaling,whichworks
at a distance, often in contexts that do not allowopportunities
for immediate verification. Sound signals go around corners,
work in the dark, operate over distances, and leave signalers
free to continue with noncommunicative manual tasks. Such
advantages make it especially important to protect the vocal-
auditory modality from deceptive abuse. Lack of volitional
control acts like the watermark on a banknote—it proves that
the owner was not the printer. The need to guarantee reli-
ability applies less to visual signals used in face-to-face in-
teractions because such contexts generally offer little scope
Facial and manual gesture work best at close quarters, in
intimate contexts where immediate verification should be rel-
atively easy. Opportunities for deception are correspondingly
few. For example, when one chimpanzee informs a grooming
partner at which point on its body it needs to be scratched
(Pika and Mitani 2006), what could it possibly gain from a
deceptive signal? It is surely no coincidence that nonhuman
primates get closest to volitional referential signaling in those
restricted social contexts that offer the least scope for decep-
But this is precisely the theoretical problem: human lan-
guage is not used primarily as an aid to ongoing physical
activities such as grooming. Its distinctive function is “dis-
placed reference”—communication about things not cur-
rently within sensory range. No mechanistic approach of the
kind exemplified by Arbib and his colleagues can measure up
to the challenge of explaining how this kind of language could
possibly have evolved.
David A. Leavens
Department of Psychology, School of Life Sciences,
University of Sussex, Falmer, East Sussex BN1 9QH, UK
(email@example.com). 27 VIII 08
Arbib, Liebal, and Pika have produced an ambitious and
origins. In their review, apes stand out among primates in
their capacities for intentional communication with manual
gestures. To the degree that the last common ancestor (LCA)
of (the other) apes and humans displayed flexibilityinmanual
signaling, over and above that seen in facial expressions and
vocalizations, is the degree to which manual signaling gains
allure as a prelinguistic substrate for the later complex story
of language evolution. Their review concludes that great apes
have moderately flexible, typically dyadic gestural commu-
nicative habits, whereas modern humans have extraordinary
flexibility in triadic signaling in numerous domains. Here, I
will elaborate on the significance of pointing and symbol ac-
quisition by apes for reconstructing the triadic competencies
of the LCA.
Arbib and colleagues frequently invoke the notion of flex-
ibility in signaling. But what does “flexibility” mean in this
context? In one sense, it means that an individual can use a
number of different communicative tacticstowardattainment
of a goal and can use the same signal to different ends (To-
masello and Call 1997, 243). An example of this kind of
flexibility is that chimpanzees communicate in different sen-
sory modalities depending on whether an observer can see
them (e.g., Hostetter, Cantero, and Hopkins 2001; Leavens et
al. 2004). In this sense, signalers are seen as tacticians.
In a second sense, flexibility is a characteristic of dyads. In
ontogenetic ritualization, pairs of social partnersdeveloptheir
own pair-specific patterns of nonverbal communication (To-
masello and Call 1997, 301). An example of thiskindofdyadic
flexibility occurs when infants ritualize their signals for being
picked up: no longer strainingwiththeirwholebodies,bounc-
ing rhythmically on their substrates, reaching with both arms
fully extended, raising their arms while looking at the care-
giver. Examples from adulthood include dancing and love-
making—in these and other contexts, couples develop dyad-
specific repertoires of nonverbal signals. Here, signalers are
seen as dancers.
In a third sense, flexibility means that signals are acquired
during development and shaped through common social ex-
periences of signal consequences (Tomasello and Call 1997,
243). Whether humans typically point with their lips or fin-
gers, for example, is a function not so much of individual
tactics or dyadic accommodations but of cultural traditions
(Wilkins 2003). This flexibility is manifested in patterns of
within-cultural similarities as contrasted with systematic
cross-cultural differences. Here, signalers are seen as being
plastic in an ontogenetic sense.
According to many theorists, including Arbib and others,
this third kind of ontogenetic flexibility requires sophisticated
mimetic abilities. However, consideration of the distribution
of pointing among apes reveals a striking pattern of group
differences: wild apes almost never point manually, about half
of laboratory apes point (usually with their whole hands), and
virtually all language-trained apes point (usually with their
index fingers; Leavens, Hopkins, and Bard 2005, 2008). Arbib
(2005a, 150) noted that “chimpanzees raised in a human
environment can exhibit far more ‘protolanguage’ than their
wild cousins—observing animals in the wild does not define
the limits of complexity of their behavior.” Apes raised by
humans assume the mannerisms of their caregivers to some
degree: to a lesser degree among captive apes with relatively
infrequent daily interactions with caregivers and to a much
greater degree among home-raised or language-trained apes.
The significance of these empirical patterns is clear when
one considers that virtually everything we know about human
communicative development derives from the study of hu-
mans raised in artificial urban or suburban caregiving envi-
ronments that are without precedent in the prehistory of our
species (e.g., Leavens, Hopkins, and Bard 2005, 2008). There
is a widespread contemporary belief that, somehow, “natural”
1066 Current Anthropology Volume 49, Number 6, December 2008
patterns of human parenting survive, in essence, through the
maelstrom of cultural evolution that characterizes a kalei-
doscope of human histories. But all appeals to essence are
logically antagonistic to the practice of natural history, so the
mirror system hypothesis can benefit only if we acknowledge
how unrepresentative any contemporary human rearing en-
vironment is of those of our prelinguistic ancestors. When
we study communicative development in our own species,
we see particular ontogenetic patterns only in contemporary
(pre)historical events, both biologically and culturally. The
flexibility in signal repertoires developed by apes in diverse
rearing environments highlights the relevance of animalmod-
els for understanding human communicative development
(Bard and Leavens 2008). In particular, every one of the many
thousands of linguistic signs acquired by language-trained
apes entails a triadic, referential episode. These animals cor-
rectly solved the binding problem hundreds or thousands of
times, and they can be characterized as habituallytriadiccom-
municators who belie classifications of apes as predominantly
dyadic signalers. Human environments foster triadic com-
munication in both humans and apes.
Department of Comparative Human Development,
University of Chicago, 5730 South Woodlawn Avenue,
Chicago, IL 60637, U.S.A. (firstname.lastname@example.org).
26 VIII 08
Many anatomical, physiological, behavioral, and cognitive
traits possessed by modern humans have been produced by
natural selection through a gradual process of modification
of biological structures and their functional properties over
a long period of time. The fact that the same traits, or similar
ones, are also possessed by closely related species of apes and
monkeys suggests that these traits originated long before the
birth of our species, Homo sapiens. Our ability to use and
understand language likely originated through the same nat-
ural selection process that produced other human adaptive
traits. Whether language abilities are unique to humans or
also shared by other primate species depends in large part on
how language is defined.
Equating language with speech would make language
unique to humans and reduce the usefulness of comparative
primate research in understanding languageevolution.Speech
clearly evolved after the evolutionary split between H. sapiens
and the other apes, so that studying the extant nonhuman
primate species would not tell us much about why and how
language evolved. Defining language in a way that emphasizes
its relation with thought rather than communication would
also reduce the usefulness of comparative primate research.
Complex human thought processes were likely made possible
by the substantial increase in brain size and complexity that
occurred during the evolution of our hominid lineage. If lan-
guage originated as a by-product of hominid large brain size
and complex cognitive skills, studying the communicative be-
havior of other primate species will be of limited value in
understanding language evolution.
Comparative research with nonhuman primates will be
most useful to understanding language evolution if language
is viewed as a complex system of communication. In this case,
comparative research can potentially make two types of con-
tributions. First, it can help us identify the environmental
(e.g., social or ecological) selective pressures responsible for
the evolution of complex communication and possibly also
the pressures responsible for the evolution of particular func-
tional properties of language. Second, comparative research
could help us identify possible precursors of human language
in the communication systems of the ancestors we share with
extant primate species. For example, human language may
have evolved from the vocalizations of our primate ancestors,
which presumably resembled those of extant nonhuman pri-
mates, or from their manual gestures, or both.
I am sympathetic to definitions of language that emphasize
its functional properties and its evolutionary continuity with
animal communication systems. I do believe, however, that
the main contribution of comparative primate research is in
the identification of the selective pressures driving the evo-
lution of complex communication rather than the identifi-
cation of language precursors in other animals’ signals. The
question of whether language precursors can be found among
nonhuman primate vocalizations or gestures cannot be ad-
dressed with standard scientific methods and is therefore des-
tined to remain unanswered. Moreover, neither the vocali-
zations nor the gestures of any extant nonhuman primates
show any clear evidence of an incipient process of evolution-
ary modification that may have turned these signals into lan-
guage. As pointed out by Arbib, Liebal, and Pika, primate
vocalizations are no more complex than the vocalizations of
other mammals or birds in terms of their structure,functional
properties, or usage. The manual gestures of the great apes
are equally unimpressive. Most, if not all, of the spontaneous
gestures observed in naturalistic studies of ape behavior in-
volve arm or hand movements displayed by juveniles or sub-
adults in the context of social play. Although great apes ex-
posed to humans in captivity acquire new humanlikegestures,
these gestures are limited largely to requests for food. Arguing
for a direct evolutionary continuity between human language
and the play signals of juvenile apes or the food-begging
behavior of captive apes seems unwarranted.
The mirror system hypothesis presented by Arbib and col-
leagues argues that the brain mechanisms for multimodal
language production evolved from the mirror neuron system
for grasping, a brain region activated for both grasping move-
ments and observation of grasping. According to this hy-
pothesis, increased skill in imitation of manipulative skills
such as grasping led to an evolutionary increase in the role
of imitation in the acquisition and transmission of manual
gestures, which in turn resulted in greater complexity of com-
Arbib, Liebal, and Pika Primate Vocalization, Gesture, and the Evolution of Human Language1067
munication and, ultimately, in language. Although the hy-
pothesis that language evolved from the mirrorneuronsystem
is plausible, the hypothesized evolutionary links between ma-
nipulative skills and manual gestures and between manual
gestures and language are not directly supported by the pri-
mate behavioral data reviewed by Arbib and colleagues. The
observations that social play between immature great apes
involves hand gestures and that great apes can potentially use
their hands to beg for food are interesting. However, the
argument that these gestures may be associated with the mir-
ror neuron system and served as evolutionary precursors of
human language is far from compelling.
Joanne E. Tanner
3071 Dover Drive, Santa Cruz, CA 95065, U.S.A.
(email@example.com). 15 VIII 08
Like Arbib, Liebal, and Pika, I find that the existence of a
mirror neuron system and knowledge of its workings have
supported our understanding of the gestural aspect of lan-
guage. However, more exploration is needed of terms central
to the authors’ conclusions:imitation,pantomime,andgesture.
Definitions of gesture in apes are not only not in agreement
between investigators but also have morphed within the same
research teams in their ongoing series of papers. Here, the
physical nature of “gesture” goes undescribed,andtheauthors
simply say “we consider behaviors to be gestures only if they
serve to reach a recurrent social goal and are directed at a
can identify an animal’s social goals—which arequitepossibly
in constant flux and subject to changing circumstances, con-
text, and unknown previous social history. There have been
recent attempts to compare gesture repertoires of the same
species (Pika 2007), but because of disparity in definitions,
synthesis is far from complete. Gesture for some scholars is
any kind of body movement at all and for others only “in-
tentional” movement of the upper limbs or actions lacking
mechanically effective force. Actions incorporating objects,
held or thrown, are gesture in some studies and excluded by
others. Some lump gesture types in nomenclature; othersslice
in fine detail.
A focus in my own studies has been the iconic aspect of
some gesture. Borrowing from the authors’ definition of pan-
tomime, iconic gesture involves the repetition of parts of
practical action without acting on objects, as communication.
The authors categorize pantomime of grasping and manual
praxic actions as part of an “evolutionary progression of neu-
ral systems unique to the human line.” I would not want to
relegate pantomime exclusively to the human line. Example:
a male gorilla reaches out and taps a female on the shoulder,
nods his head, and swings the arm that touched her to be-
tween his legs. The consistent result of such sequences was
initiation of contact by the female (Tanner and Byrne 1999;
see also Savage-Rumbaugh, Wilkerson, and Bakeman 1977
and examples from symbol-taught apes). The iconic gestures
I describe in gorillas are not classic “intention movement”;
they minimize force and appear to portray intentions for
another animal, not the gesturer. This kind of gesture, un-
derstood instantly by others, is exactly what one would expect
in a mirror system. There are also hints of “compositionality”
in ape phrases such as the above. Gorillas negotiate mutual
activity with gestures that function disparately as attention
getters, motion depictors, location indicators, or negations
(see Tanner 2004; http://www.gorillagestures.info/).
Facial expression, yet another form of gesture (Armstrong,
Stokoe, and Wilcox 1995), needs to be studied asfoundwithin
streams of gestural action. The facial expressions of gorillas
in particular are an untapped area. Though they have been
called less flexible than those of chimpanzees, my videotape
suggests that they can be rich and varied. Further, gorillas
may be aware, if not completely in control, of the commu-
nicative significance of the face (Tanner and Byrne 1993).
Early-stage imitation is distinguished from pantomime as
involving the achievement of goals regarding objects. The
authors also make a distinction between “simple” and “com-
plex” (human-only) imitation that appears to be their own,
though “simple imitation” seems to correspond with Byrne’s
(1999a, 2003) “behaviour parsing” and “complex” with Ger-
gely, Bekkering, and Kiraly’s (2002) “rational imitation” of
children. Simple imitation requires repeated viewing of ac-
tions over time; complex imitation is immediate but not al-
ways wholly accurate.Thus, both categories allow practice ef-
fects, and there is overlap in categories. Tomaselloetal.(1993)
found enculturated chimpanzees highly successful overall in
immediately reproducing both means and ends of two-step
functional actions on objects with which they had been only
briefly familiarized. Data on rehabilitant orangutans describe
previously unfamiliar camp activities that were copied almost
immediately. Though many reproductions occurred after
multiple viewings of common activities, one orangutan im-
mediately copied a rare event, axe sharpening. In an exper-
imental setting, an orangutan copied a novel compound hi-
erarchical action on a first trial (Russon 1996, 1999).
Complex imitation is attributed to a solely human ability
to recognize a compound action as a goal-directed whole.The
statement “complex imitation unique to the humanlinemade
possible the evolution of brain mechanism for pantomime”
seems, in light of this discussion, (literally) out of order. Ape
have primed the brain’s capacity to hold in memory longer
and longer sequences of action and led to increasingly com-
plex imitative skills.
The authors review skills of human-enculturated apes but
drop them from their discussion of evolutionary progression
of neural systems. Tanner, Patterson, and Byrne (2006, 87)
have applied Arbib and colleagues’ proposed stages of evo-
lutionary development of language to performance of sign-
taught gorilla Koko in terms of her invented (not taught)
signs and found that she progresses into stages reserved. Ape
1068 Current Anthropology Volume 49, Number 6, December 2008
potential, like thatof humans,isnotlimitedtobehaviorfound
in native settings but influenced by the culture of their up-
bringing; learned or invented behavior should be recognized
as part of their essential ape-ness rather than untypical.
Our article surveyed data on communication systems in
present-day nonhuman primates as a basis for assessing the
relative merits of a “vocalization only” versus an “essential
role of gesture” path from the communicative systems of our
common ancestors to human language. We concluded that
ape gestures show much more variation from group to group
than do primate vocalizations and suggested that this ability
to create new communicative signals within groups favors the
latter view. In addition, we briefly discussed the pros and cons
of a specific evolutionary model (the mirror system hypoth-
esis) associated with this view. It goes far beyond what can
be learned from comparative primatology but is nonetheless
consistent with the constraints of data sets from a variety of
We thus divide this reply to our commentators into two
parts. The first part focuses on data on nonhuman primates,
whereas the second part turns to language evolution consid-
ered more generally.
Analysis and Interpretation of Data on Nonhuman Primates.
Tomasello and Zuberbu ¨hler (2002) proposed that vocaliza-
tions are used usually in “evolutionarily urgent”contextssuch
as predation or aggression and therefore must be specific in
their meaning. However, as Corballis noted, we ascribe more
flexibility and learning to primate vocalizations than hitherto
recognized. This is in part because researchers of primate
vocalizations have focused mainly on alarm calls and only
now begin to investigate, for example, contact calls and food
calls. Even factoring in these new data, we stillseetheevidence
as favoring the “essential role of gesture” model—but not a
“gesture only” model. We also want to stress that it is im-
portant to integrate research on different modes of com-
munication instead of focusing on just one modality alone.
The only potentially referential gesture described so far for
apes in the wild is used during grooming (Pika and Mitani,
forthcoming), a context suggested as the precursor to human
gossip and thus language (Dunbar 1996). Knight counters
that “human language is not used primarily as an aid to
ongoing physical activities such as grooming” but asdisplaced
reference. While we agree that language today is used to direct
the attentional and mental states of receivers to outside en-
tities, its evolutionary precursors may have aided such on-
going activities. As group size increased(primatesocialgroups
∼50–55 individuals; human social network ∼150 individuals),
multiplying the number of relationships each individual has
to monitor, servicing relationships through grooming be-
comes impractical (Dunbar 1996). Humans may thus have
filled the “grooming gap” by developing different commu-
nicative means—vocal and/or gestural “grooming”—which
flowed later into linguistic communication (Pika 2008b).
Given his own contributions, Maestripieri seemed surpris-
ingly negative about the whole field of comparative prima-
tology of communication. Moreover, he dismissed the ma-
jority of gestures studied in apes communicating with
conspecifics as juvenilia. However, we (Liebal, Pika, and To-
masello 2004, 2006) found that both young and adult sia-
mangs and orangutans use a range of different gestures, and
although all gesture types are found during play, they are also
used in other contexts. Gestural repertoires decrease with age,
but adults may use “new” gestures not observedinyoungsters,
and they may perform previously used gestures in different
contexts. Further, many gestures observed in different species
occur in the context of reconciliation, within the establish-
ment or maintenance of group structure (Maestripieri 1999;
Nishida et al. 1999), or during affiliative interactions and sex
(Savage-Rumbaugh, Wilkerson, and Bakeman 1977; Savage-
Rumbaugh and Wilkerson 1978).
Maestripieri stresses that whether language abilities are
unique to humans depends in large part on how language is
defined. However, we have been careful (Arbib 2005a) to set
forth several characteristics of language that are unique to
humans but are neither specific to speech nor based on the
characteristics of thought.
Concerning Leavens’s discussion of pointing, the crucial
question is no longer whether apes point (Leavens and col-
leagues have shown this convincingly) but why they point.
Apes gesture mainly for imperative purposes, while humans
from an early age on also gesture for declarative purposes,
directing the attention of others to an outside object or event
to share interest or comment on it (Bates, Camaioni, and
Volterra 1975; Liszkowski 2005; Pika 2008b).
Tanner asks for more clarification of the term “gesture.”
Moreover, she considers facial expressions as a type of gesture.
While some researchers do considerfacialexpressionsgestures
(e.g., Maestripieri 1997; Zeller 1980), it remains unclear
whether they are simply affective expressions of emotional
states or whether they should, at least in some cases, be clas-
sified as intentional signals (e.g., Caldecott 1986; Tomasello
and Call 1997). Facial expressions of emotion may be differ-
entiated from orofacial gestures linked to ingestion (Fogassi
and Ferrari 2007). However, motor linkages between arm/
hand movements and speech in humans (Gentilucci, Dalla
Volta, and Gianelli 2008) may have important implications
for language evolution (Gentilucci and Corballis 2006).
Tanner suggests that pantomime is not exclusive to the
human line and draws attention to iconic gestures, which
bear some physical resemblance to their referent (Bates et al.
1979) and thus share features with pantomime (but may be
highly conventionalized). However, iconic gestures have so
far been described in only a single bonobo and a single gorilla
(e.g., Savage-Rumbaugh, Wilkerson, and Bakeman 1977; Tan-
ner and Byrne 1999), so the evidence is rather thin and may
Arbib, Liebal, and Pika Primate Vocalization, Gesture, and the Evolution of Human Language1069
hold only in the eyes of the human observer. Tanner rejects
the view that complex imitation is unique to the human,
arguing that ape pantomime with a goal of movement for a
social partner could have primed the brain’s capacity to hold
in memory longer and longer sequences of action and led to
increasingly complex imitative skills. However, given the pau-
city of data on nonhuman primate pantomime, the “could”
here seems to us more a factor of human evolution than the
development of nonhuman primates. Indeed, we distinguish
the ability of apes to create and share a relatively small rep-
ertoire of gestures from the immense richness of a modern
human sign language. Thus, even were it demonstrated that
apes could create a few iconic gestures, these might better be
seen as an evolutionary precursor to pantomime rather than
pantomime in the human sense. Nonetheless, Tanner’s ob-
servations make it clear that further research is needed on
the comparative primatology of the diverse forms of
General Considerations on LanguageEvolution.Knightasked
why vocalizations are still so limited in monkeys and explains
this with mechanisms to avoid deception when communi-
cating over larger distances and therefore being out of view.
He suggests that selection pressures might have rendered it
adaptive for vocal communication to be insulated from cog-
nitive control and asks what fitness advantages might accrue
to an intelligent ape from its inability to play around with its
vocal signals. Knight sees the ability to engage in pantomime
as an ability to fake one’s bodilysignalsanddisplays.However,
we should not conflate “honest pantomime” (or the ape ges-
tures for which ontogenetic ritualization might be one path)
with faking. Our account stresses the role of simple and then
complex imitation as having a payoff in praxis that then pro-
vides opportunities for exaptation for communication. A
greater emphasis on social structure would, however, usefully
enrich the mirror system hypothesis by teasing out an “ex-
panding spiral” between imitation for praxic communication
and imitation for social gestures. This might in turn yield a
basis for the brain structures underlying general mimesis
(Donald 1998). Note, too, the advantages posited for moving
from pantomime of hand gestures to pantomime of all man-
ner of events, actions, and objects, not just actions of hominid
agents as part of the move from instrumental to declarative.
Corballis asks what actually drove language beyond simple
pantomime or protolanguage to compositional structure. We
have argued that the ability for complex imitation enabled
the evolution of brain mechanisms that provided the starting
point for an open-ended spiral leading to pantomime, pro-
tosign, protolanguage, and thence compositional structure
(Arbib 2008). However, we do not see language as an all-or-
none system but rather suggest that any language is the result
of a long process of invention, importation from other
(proto)languages, and grammaticalization. Consider, then,
Corballis’s suggestion that the ability to travel mentally in
time and space drove language from pantomime to compo-
sitional structure (Suddendorf and Corballis 2007). Certainly,
one cannot talk of the past or possible future unless one has
episodic memory (which may reflect an evolutionary devel-
opment from processes involving hippocampal place cells;
Mizumori 2006) and the ability to weigh alternative plans of
action (which, in its more sophisticated forms, may rest on
integrated activity in prefrontal and parietal cortices; see, e.g.,
Newman 2003). However, recent studies on birds (e.g., Clay-
ton and Dickinson 1998; Raby et al. 2007) and apes (e.g.,
Schwartz, Hoffmann, and Evans 2005) show that these crea-
tures exhibit at least some aspects of episodic memory, so not
all “mental time travel” is uniquely human. Moreover, it is
one thing to have episodic memory or planning ability; it is
quite another to communicate those memories or plans to
others. We thus have a chicken and egg problem. It may be
that compositionality emerged first to more flexibly describe
increasingly complex episodes in the here and now (Arbib
2009) and that this made possible adding markers to descrip-
tions of here-and-now events to indicate some form of tem-
poral aspect. De Villiers and Pyers (2002) argue that the un-
derstanding of false beliefs supports the development of
complex syntax. We have already noted the transition in hu-
man evolution from instrumental pointing to pointing for
sharing interests. Any modern language is the product of
bricolage, melding a large variety of different communicative
and cognitive skills.
Leavens argues that the communicative development seen
in humans raised in modern caregiving environments is un-
representative of that of our prelinguistic ancestors. He also
stresses the need to define the kind of flexibility involved in
communicative systems. In addition to the types he mentions,
flexible use can involve combining single components into
larger combinations. Wehavesuggestedthatthecombinations
seen in nonhuman primates are qualitatively different from
those afforded by the grammars of human languages. This
fits with our view (the mirror system hypothesis) that the
brain mechanisms that support language integrate those that
evolved in turn to support complex imitation, then panto-
mime, and then protosign and protospeech, with the richness
of languages emerging much later as the result of “cultural
evolution.” Because most of our knowledge of triadic com-
munication of apes stems from thoseraisedinartificialcaptive
environments by modern humans, it might be argued that it
does not provide a useful tool to infer the communicative
and cognitive skills that were available during the dawn of
human language—but it does inform us about what apes are
potentially capable of. Nonetheless, we are convinced that it
is essential to study the impact of social and ecological factors
on ape gestures in the “natural” environment as a basis for
hypotheses about the role such factors might have played in
the evolution of human gestural communication and lan-
guage. Indeed, we emphasize the importance of combining
as much as possible of the available comparative knowledge
zle of what makes us human.
—Michael A. Arbib, Katja Liebal, and Simone Pika
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