Developmental

7 Modifications in the Vocal

Behavior of Non-Human
Primates
Julia Fischer

CONTENTS

I. Introduction
II. Impact of Methodological Advances
III. Plasticity in the Usage and Comprehension of Calls
A. The Case of Pygmy Marmoset Babbling
B. Dialects and the Question of Vocal Convergence
C. Infants’ Responses to Acoustic Gradation
IV. Future Research
Acknowledgments
References

I. INTRODUCTION
Understanding the roots of human language is a fascinating topic that has generated
as much interest as controversy (see References 1 to 3 for some recent contributions).
A key feature of human language is that it is learned, in terms of both its production
and comprehension. From a comparative perspective, this raises the question of
whether and to what extent other primate species exhibit vocal learning. One of the
earliest studies in this field involved an attempt to teach a chimpanzee to speak.4,5
Vicki, the chimpanzee raised with the Hayeses, for instance, in fact learned to utter
a few “words,” but the difficulties she had in mastering this task were apparently
more striking than her successes.4
The finding that apes or monkeys have difficulties acquiring human speech,
however, does not refute the possibility that learning plays an important role in the
development of their own species-typical vocalizations. Most of the evidence accu-
mulated about vocal development comes from studies on monkeys,6,7 while hardly
anything is known about the vocal development of apes.8 In contrast, numerous

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studies have explored apes’ ability to employ signs or linguistic symbols,9 as well
as gestures.10 Thus, there is a serious imbalance in what we know about monkeys
vs. apes in these different domains of communication.8
Much of the original research on primate vocal development focused on whether
the ability to produce certain vocalizations was a learned vs. an innate process.11–13
More recently, primatologists have realized that it is important to distinguish among
the developmental trajectories of the ontogeny of vocal production, call usage, and
comprehension of calls.14,15 In a nutshell, whereas there is little evidence that non-
human primates learn to produce their sounds through imitation,16 learning does
seem to play an important role in the usage and comprehension of calls. An extensive
review of these earlier studies is given in Seyfarth and Cheney.14
The occurrence and possible function of small-scale variability in monkey and
ape vocalizations have recently attracted increased attention. The goal of this chapter
is to review some recent studies that have targeted such vocal variability during
development, as they apply to both production and perception. First, we will examine
whether methodological advances in the field of acoustic analyses have altered the
assessment of the degree of vocal modification during ontogenetic development.
This will be followed by an examination of the occurrence of increased vocal activity
(“babbling”) in young non-human primates, as well as the extent of and possible
mechanisms underlying variation in call production at the group or population level
(“dialects”). These studies may shed some light on the functional significance of
modifiability in monkey and ape calls. They also provide an opportunity to discuss
the distinction between usage and production of calls. The next section turns to
recent studies of the development of the comprehension of calls and examines the
question of how the ability to attach different meanings to similar sounding calls
develops with age.

II. IMPACT OF METHODOLOGICAL ADVANCES

In their 1997 review of vocal development in non-human primates, Seyfarth and
Cheney14 reported that the majority of studies published before 1987 supported the
notion that non-human primate calls appear fully formed at birth and show no
developmental modification. The majority of studies published after 1987, however,
provide evidence of more substantial modification in vocal production. They hypoth-
esized that this shift may be related to the advent of computer-based digital process-
ing of sounds.
Two recent studies in which an earlier investigation was replicated provide a
good opportunity to test this hypothesis. In the first such study, Hammerschmidt
and colleagues17 analyzed recordings of young squirrel monkeys, Saimiri sciureus.
This data set had been gathered in an attempt to replicate the classic paper by
Winter et al.12 on the ontogenetic development of squirrel monkey calls. Winter
and colleagues investigated whether species-specific auditory input is necessary
for the proper development of the species’ vocal repertoire. In this earlier study,
squirrel monkey infants raised normally were compared with infants raised in
social isolation. A qualitative description of the vocal repertoire yielded no dif-
ferences between the two groups of infants, suggesting that hearing conspecific

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vocalizations is not necessary for developing the full range of normal vocalizations.
Quantitative analyses of some temporal and spectral characteristic of two call types
(“isolation peep” and “cackling”) also failed to reveal significant differences in
relation to rearing condition. Furthermore, Winter and colleagues12 found no
structural differences in the vocalizations from normally hearing squirrel monkeys
and ones deafened shortly after birth. Based on these findings, the authors con-
cluded that all but two call types appear fully formed at birth and do not change
during development. Only the isolation peep and twitter exhibited structural
changes with age that were probably due to changes in body size.
More recently, Hammerschmidt and colleagues17 analyzed recordings from four
normally raised squirrel monkeys, one Kaspar–Hauser animal reared in social iso-
lation, and one animal that was congenitally deaf. The study investigated changes
in 12 different call types over a period of 2 years, using a state-of-the-art acoustic
analysis in which a large set of acoustic variables was measured and then submitted
to multivariate statistical analysis. With the aid of these more sensitive analytical
tools, Hammerschmidt and colleagues found some ontogenetic changes in all of the
call types studied, with some calls showing more pronounced changes with age than
others. As the call repertoire of the squirrel monkey is extremely diverse, it is not
surprising that, for each call type, different sets of acoustic features showed different
patterns of developmental modification.17 However, many of the changes could
simply be attributed to growth, such as changes in resonant frequencies or in call
duration, a variable that — at least in loud calls — is presumed to be related to lung
volume.18 The majority of changes occurred in the first 4 months of life. Vocal
development seemed to be completed at the age of about 10 months. The authors
found no substantial differences in the vocalizations of the isolated or the deaf
subject, and in this regard confirmed the earlier findings of Winter et al.12,17 Most
importantly, though, results indicated that calls did not become more stereotyped
with age but that all calls maintained a high degree of inter- and intra-individual
variation. The authors argued that such variation could be the substrate for modifi-
cations later in life, a claim that remains to be tested.
In a second similar study, Hammerschmidt and colleagues19 traced the develop-
mental modification in the “coo” calls of the rhesus macaque (Macaca mulatta) and
compared their findings to the results of an earlier study by Newman and Symmes.20
This earlier study reported that young rhesus monkeys reared in isolation produced
abnormal-sounding coo calls as adults. In their more recent study, Hammerschmidt
et al.19 recorded 20 subjects from the first week of life until 5 months of age. The
animals were raised under two different rearing conditions. Some were housed with
their mothers and other animals, whereas others were nursery reared with only age-
matched peers and were thus deprived of adult vocalizations to use as potential vocal
models. Figure 7.1 shows spectrograms of calls recorded from three subjects at three
different ages, illustrating the findings of the acoustic analysis. The analysis revealed
a drop in fundamental frequency and more consistent amplitude across the duration
of the coo call as the animals grew older. The amplitude consistency reflects whether
and to what degree a coo call may reveal gaps during the course of the fundamental
frequency. The occurrence of such gaps decreased with age. Whereas a drop in the
fundamental frequency correlated significantly with an increase in weight (which in

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 1-2 weeks 3-4 weeks 4-5 months
16
subject 1
8

16
frequency [kHz]

subject 2

16
subject 3

time [ms]

FIGURE 7.1 Spectrograms of coo calls recorded from rhesus macaques at three different
ages. Frequency is depicted on the y-axis; time on the x-axis. (Unpublished material courtesy
of Kurt Hammerschmidt.)

turn is related to size), the increase in amplitude consistency indicated that some
practice might be required before the mature version of a call can be produced.
Whether or not auditory feedback plays a role in producing coos with a stable
fundamental frequency remains an open question. Rearing conditions did not affect
the acoustic structure of the coo call, suggesting that exposure to an adult model
is not a prerequisite for the formation of species-typical call characteristics. This
finding stands in contrast to Newman and Symmes’ earlier study.20 However, these
authors lumped coo calls with a tonal structure with others that graded into
screaming. The differences in vocal output could therefore rather be related to
differences in social experience instead of auditory input, as it seems likely that
the recording conditions (social isolation) were perceived differently by isolates
and normally reared infants. The results of both the original study and the more
recent one suggest that auditory feedback is not a prerequisite. The increase in
constancy could either be due to increased experience or to maturation of the
neuronal substrate controlling motor output. Interestingly, like the squirrel monkey
study described above, the current study also failed to find a significant increase
in call stereotypy over time. Instead, throughout the study period, animals exhibited
marked intra-individual variation.
To summarize, two recent studies using modern techniques of acoustic and
statistical analysis offer conclusions that deviate from earlier claims. In the squirrel
monkey study, Hammerschmidt et al.17 reported a larger degree of acoustic variation

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than found in previous work, whereas in the rhesus monkey study19 authors were
unable to replicate the finding that rearing conditions affected call structure. Both
recent studies support the view that the vast majority of the motor patterns underlying
vocal production are largely innate and in place at least from birth, while some
features may change in relation to age and practice or maturation. Both studies also
suggest that a high degree of variability is maintained throughout development.
It is therefore unclear whether the application of sophisticated analytical tools
will fundamentally change current views on vocal development. It is possible that
some of these divergent statements can be reconciled if earlier studies are put into
their proper historical perspective. For instance, those researchers who described
calls as being “adult-like from birth on and showing no signs of modification”14
would probably have had no trouble estimating the age of a caller just on the basis
of the call characteristics, despite the fact that, essentially, the call types are the
same across different age classes. At a time when comparatively little evidence had
been accumulated yet, the extent as to which vocal production appears to be innate
may have come as a surprise, particularly in light of the close relatedness of humans
and non-human primates. When it became clear that monkeys neither go through
sensitive phases (in terms of their vocal production) nor gradually acquire the
structure of their vocalizations, subtle changes became more interesting.

III. PLASTICITY IN THE USAGE

AND COMPREHENSION OF CALLS
A. THE CASE OF PYGMY MARMOSET BABBLING
Whereas the previous studies addressed the issue of whether non-human primate
calls exhibit plasticity in terms of their acoustic structure, less is known about
plasticity in terms of the usage of calls. Several studies suggest that infants vocalize
more frequently than adults (reviewed by Snowden and Elowson21). Whereas some
of this vocal activity may be related to the weaning process,22,23 other studies suggest
that this increased vocal activity may provide vocal practice. One outstanding case
is the vocal activity of young pygmy marmosets, Cebuella pygmaea. Elowson,
Snowdon, and colleagues24,25 observed that infant pygmy marmosets go through a
phase of intense vocal output during which they produce long bouts of calls, most
of which resemble calls of the species’ repertoire. These call bouts consist of
rhythmic and repetitive strings of syllables which occur within the first 2 weeks of
life. Vocal activity peaks just prior to weaning at the age of 7 to 8 weeks. The authors
likened this behavior to human infant babbling.24 Human infant babbling typically
begins between 6 and 10 months of age and also consists of repetitive strings of
syllables.26,27 Unlike human words, which typically have an external referent, human
babbling seems to be content free and is thought to promote control over one’s vocal
output via auditory feedback. Elowson and colleagues pointed out that both human
and pygmy marmoset babbling lack apparent meaning, promote interactions with
caregivers, and might provide vocal practice.21,24
It may be worth noting that some important differences exist between pygmy
marmoset and human infant babbling. For one, human infant babbling can be clearly

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differentiated from earlier vocal behavior. Furthermore, children assemble the parts
that make up their early words from their prelinguistic phonetic repertoire (i.e., from
the syllables that form part of the babbling).27,28 In other words, whereas babbling
in children is a crucial part of the child’s development of speech, pygmy marmosets,
after their babbling phase, decrease the amount of their vocal activity, while the
structure of the elements largely remains the same. Finally, not only the pygmy
marmoset babbling but also the large majority of adult vocalizations fail to provide
information about external objects or events and are, in this sense, content free.
Doubtless, numerous parallels do exist between pygmy marmoset and human infant
babbling, yet some important differences remain.

B. DIALECTS AND THE QUESTION OF VOCAL CONVERGENCE

As noted earlier, vocalizations of at least some primate species retain a high degree
of variability throughout adult life, and it was hypothesized that this variability may
be the substrate for modifications of the call structure later in life. This issue has
been addressed at two levels: first, whether animals tend to converge at a group or
population level, and, second, whether dyads tend to produce calls that are similar
to each other. If meaningful variation within the range of a species’ vocalizations
occurs between different populations or groups, a key question is whether they
constitute dialects in the sense that the variation can be attributed to experience and
not simply to genetic variation. One of the earliest such reports came from Green,29
who observed that three different populations of Japanese macaques, Macaca fus-
cata, had differences in the acoustic structure of a call produced during feeding
times. He suggested that these differences were due to a “behavioral founder effect,”
where a given subject responded to the food provisioning with a spontaneous vocal-
ization that was subsequently imitated by other group members. In an attempt to
document this process in more detail, Sugiura30 conducted a playback study in which
he compared the acoustic structure of calls that were given in response to playbacks
of contact calls with those that were given spontaneously. He found that female
Japanese macaques in one population (but not another) responded to playback of
coo calls by calling back with similar sounding coo calls; that is, these coo calls
were acoustically more similar to the playback coo than to coo calls produced
spontaneously by the subjects.30 He concluded that these monkeys must have some
control over their output and be able to adjust it accordingly.
But, what exactly is meant by the phrase “control over the vocal output”? On
the one hand, animals could truly be imitating one another; that is, they store the
auditory input as a sound model and adjust their vocal output so that it matches the
model. The acoustic structure of non-human primate calls is determined by oscilla-
tion of the vocal folds and sometimes the vocal lip,31 articulatory gestures that
influence the filtering characteristics of the vocal tract,32–34 and respiration.35 Current
evidence suggests that, in non-human primates, the anterior cingulate cortex serves
to control the initiation of vocalizations, facilitating voluntary control over call
emission and onset.36 However, the motor coordination of the vocalization appears
to take place in the reticular formation of the lower brainstem,37 suggesting little
voluntary control over the precise structure of the vocal pattern. Following this line

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of argument, it is difficult to see how such precise control could be achieved. On
the other hand, animals may differ in the activation of different motor patterns. Far
too little is known about the representation and activation of these motor patterns38
to resolve this question. In any case, it turns out to be more difficult to distinguish
between call usage and call production than it appears at first glance.
Another example for acoustic differences at the group level comes from Barbary
macaques, Macaca sylvanus. Fischer and colleagues39 reported that the alarm calls
given by members of two populations of Barbary macaques revealed significant
variation between sites. Whereas the general structure was the same at both sites, a
fine-grained acoustic analysis revealed significant differences between calls from
the two populations. Playback experiments in which calls from their own or the
other population were broadcast suggested that this observed variation was percep-
tually salient.39 Because neither genetic differences nor habitat structure could
account for the observed differences between groups, Fischer and colleagues con-
cluded that the general acoustic structure of calls is fixed whereas there is restricted
potential for acoustic modification. Again, it remains unclear which mechanisms
underlie this observation.
While the evidence for dialects in macaques remains rather weak, and the
mechanisms opaque, it could still be the case that apes provide more compelling
evidence for modifiability of their vocalizations. Mitani and colleagues40 examined
the differences in the acoustic structure of chimpanzee (Pan troglodytes) “pant-
hoots” between two different populations. Pant-hoots comprise a series of several
elements (dubbed the build-up phase), culminating in a climax element. The authors
found differences both in the temporal characteristics of the call and in the frequency
characteristics of the climax element. Although genetic or anatomical differences
between populations could not be ruled out, the authors assumed that the differences
in pant-hoots between groups were mediated by learning. Similarly, Mitani and
Gros-Louis41 investigated the occurrence of call convergence in wild chimpanzees
during joint chorusing. In one anecdotal case, they found that calls produced by a
pair of closely affiliated male chimpanzees were more similar to each other when
they called together than when they called with others. In a recent study, Mitani and
colleagues42 reassessed the evidence for dialects. They recorded pant-hoots from
two populations of wild chimpanzees in East Africa. As the structure of pant-hoots
varies as a function of the age and sex of the caller,43 the analysis was restricted to
the calls of adult males. This study failed to identify significant variation in the
climax elements; however, based on the combination of a number of variables that
are related to the duration and the number of elements in the build-up phase, it was
possible to assign the majority of calls to their proper populations. In contrast to
earlier studies, Mitani and co-workers42 assumed that this acoustic variation could
be related to differences in habitat acoustics and body size of the chimpanzees.
To eliminate genetic relatedness as a variable in chimpanzee call convergence,
Marshall and colleagues44 initiated a study in which they investigated whether two
groups of captive chimpanzees differed with regard to the acoustic structure of the
pant-hoots. Because the animals came from diverse origins, the influence of a genetic
component could be ruled out. The authors found an overall similarity among pant-
hoots recorded in captivity and in the wild, suggesting a strong innate component

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of the call type. Nevertheless, they found significant variation between two captive
groups. They also reported that a male in one enclosure introduced a novel element
to his pant-hoot that subsequently was also used by five other males from the same
colony. This novel element (dubbed a “Bronx cheer”) is produced by blowing air
through pursed lips. The observation suggests that chimpanzees have some control
over their respiratory activity and their lips. However, it is perhaps not surprising
that this novel element was not voiced, as studies of the neural control of the vocal
apparatus suggest that the control of the tongue and the lips is under voluntary
control, while the control over the laryngeal muscles is less developed.45
To summarize, several studies suggested that non-human primates have the
potential for minor modifications of their call structure. To establish the putative
function of these vocal modifications, it is necessary to distinguish between within-
group44,46 and within-dyad convergence.30,41 Within-group similarity in call struc-
ture should be the result of a longer term process, possibly taking place within
weeks or months, and could function as a social badge for group recognition.47
This would facilitate the identification of members in neighboring groups. Iden-
tifying members in one’s own group could be mediated via knowledge of individual
characteristics in call structure, but if groups exceed a certain size then call
convergence could also assist in identifying members in one’s own group. As far
as dyads are concerned, Sugiura30 proposed that vocal matching functions to
indicate that the “matched” coos are given in response to a particular individual’s
calling. A similar function has been suggested for the matching of signature
whistles in dolphins, for which it is believed that vocal matching functions to
address a particular individual.48
As far as the mechanisms are concerned, several authors suggested that the
process of call convergence can be attributed to vocal accommodation.39,49,50 In
speech, humans make minor adjustments in their vocal output so that it sounds
more like the speech of the individual with whom they are talking. This subcon-
scious process is called speech accommodation.51 Speech accommodation includes
a wide range of subtle adaptations, such as altering the speed at which people
talk, the length of pauses and utterances, and the kind of vocabulary and syntax
used, as well as intonation and voice pitch. Locke28 observed similar adjustments
in the speech acquisition process of infants and termed it vocal accommodation.
However, the concept of vocal accommodation has a more descriptive than explan-
atory value, as the mechanisms underlying both vocal accommodation and match-
ing remain unclear.
In light of the finding that non-human primates have only limited voluntary
control over the vocal apparatus,45,52–54 it remains puzzling how accommodation is
accomplished. If vocal accommodation accounts for the observed modification in
call structure, then auditory feedback must somehow play a role, despite the fact
that it does not seem to be a prerequisite to developing the species-specific reper-
toire.55 More precisely, matching requires that the model be rapidly stored, and an
individual’s own motor output be planned in accordance with the stored template.56
With regard to long-term effects of call convergence, an alternative mechanism to
vocal accommodation has been suggested by Marler,57 who proposed that some call
variants are selectively reinforced by social stimulation (action-based learning). In

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this case, contextual learning (sensu Janik and Slater58) would account for the
observed changes in call characteristics. Again, however, the precise mechanisms
mediating action-based learning are not known.

C. INFANTS’ RESPONSES TO ACOUSTIC GRADATION

The previous sections on modifications in the production and/or usage of calls
showed that non-human primates apparently exhibit only little, albeit significant,
plasticity in some of their calls. In contrast, studies that examined the development
of the comprehension of, and correct responses to calls, indicated that subjects
undergo pronounced changes in development. Most of the earlier work59,60 has
focused on the development of vervet (Cercopithecus aethiops) infants’ responses
to different alarm calls given in response to their main predators, leopards, martial
eagles, and pythons.61,62 Vervet alarm calls are acoustically distinct and elicit
different, adaptive responses. For instance, upon hearing an eagle alarm, group
members look up into the sky. Playback experiments conducted on a small sample
of infants showed that after playback of the different alarm calls, infants 3 to 4
months of age typically ran to their mothers, no matter which call was broadcast.
At 4 to 5 months of age, many infants produced an incorrect behavioral strategy;
for example, they scanned the ground after hearing an eagle alarm. Detailed
inspection of film footage revealed that infants were more likely to respond
correctly when they had first looked at an adult. At the age of 6 to 7 months, most
infants responded to alarm calls as adults did.59
Vervets also attend to the alarm calls of other species, such as the alarm calls
of the superb starling (Spreo superbus), which are given in response to ground
predators such as leopards.63 Starling alarm calls occur at different rates in different
habitats, and playback experiments showed that vervet infants begin to attend to
these calls by looking in the direction of the loudspeaker at an age of 6 to 7 weeks.60
Vervet infants in an area with higher rates of starling alarm calling responded to
playbacks of these calls at an earlier age than did infants living in areas with lower
rates of starling alarm calling.60 Additional experiments on a smaller sample of older
infants revealed that they responded appropriately to starling alarm calls by running
up into a tree at 4 to 5 months of age.60
These previous studies have focused on calls that are acoustically distinct;
however, the vocal repertoires of many primate species typically consist of a mixture
of acoustically graded and discrete calls. Discrete repertoires contain signals with
no intermediates between call types, whereas graded signal systems are characterized
by continuous acoustic variation between and/or within signal types, with no obvious
distinct boundaries that allow a listener to discriminate easily between one signal
type and another.64 For instance, adult Barbary macaques give acoustically different
variants of the shrill bark call in response to different predator classes.65 Typical
subtypes of the shrill bark exist, but intermediate variants between these subtypes
also occur. Subsequent playback experiments showed that listeners categorized the
calls according to the stimulus that elicited the calling. Thus, adult subjects were
able to partition the continuous acoustic variation into different categories66 in a
manner that resembled the categorical perception (CP) found in human speech.67

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 kHz
5
4
3
2
1

200 ms

FIGURE 7.2 Spectrograms of female chacma baboon barks recorded from one subject. From
left to right: typical alarm bark, intermediate alarm bark, intermediate contact bark, and typical
alarm bark. (Redrawn from Reference 69.)

Does the ability to discriminate between variants of the same general call type
develop with age? This issue is particularly interesting in light of the suggestion that
CP in human speech relies on an innate component.68 Fischer and colleagues69
investigated whether a primate’s ability to dissect an acoustic continuum into discrete
categories is in place from birth on or whether it emerges with experience and age.
As the Barbary macaque population currently is under a strict birth-control regime,
Fischer et al.70 extended their studies to baboons (Papio cynocephalus ursinus). As
an example, they used the bark of adult female baboons. These barks grade from
clear, harmonically rich calls into calls with a noisier, harsh structure (Figure 7.2).71
The clear version is usually given when a caller finds herself in a situation where
she is apparently separated from the group or her offspring (contact bark),72,73
whereas the harsher variant is usually given when a female spots a potential predator
(alarm bark). However, there are also intermediate forms between the two subtypes,
and these acoustically intermediate calls can occur in both contexts.71
Results indicate that infant baboons gradually develop the ability to discriminate
between calls that fall along a graded acoustic continuum. The time spent looking
toward the (concealed) speaker was measured following playbacks. At 2.5 months
of age, infants failed to orient to the speaker after playbacks of either alarm or
contact barks. At 4 months of age, infants responded to playback of both alarm and
contact barks indiscriminately. At 6 months of age, infants responded strongly to
alarm barks but failed to orient to contact barks (Figure 7.3a,b). By this age, there-
fore, infants reliably discriminate between typical variants of alarm and contact
barks. Further experiments showed that infants 6 months and older exhibit a graded
series of responses to intermediate call variants (Figure 7.3c). They responded most
strongly to typical alarm barks, less strongly to intermediate alarm calls, less strongly
still to intermediate contact barks, and hardly at all to typical contact barks. Due to
the small sample size, these results remain somewhat equivocal. They may indicate
that infants respond in a continuous fashion to continuous variation in perceived
urgency in the calls. Alternatively, because infants only responded to intermediate
alarm barks, but not to intermediate contact barks, with startle responses, it might
also be the case that infants place intermediate contact and alarm barks into two

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FIGURE 7.3 Response duration (median ± IQR) in the different age classes after playback of (a) typical alarm barks and (b) typical
contact barks. Bars indicate differences between treatments (p < 0.1). (c) Response duration after presentation of single exemplars of
baboons barks (A, typical alarm bark; B, intermediate alarm bark; C, intermediate contact bark; D, typical contact bark). Bars indicate
significant differences (p < 0.05) between treatments. (Redrawn from Reference 69.)
different categories.69 Further experiments showed that a lack of responses to clear
contact barks was not simply due to habituation to their frequent occurrence; infants
responded strongly to the playback of contact barks recorded from their mothers.
Some of the infants even interrupted their activity and began to approach the
speaker.69 The finding that infant baboons were able to discriminate between the
different call types at about 6 months of age complements the results of the studies
mentioned above on vervet infants’ responses to different alarm calls.74
In sum, the baboon study showed that infants discriminate among graded
variants within a call type, and, at the very least, that they can distinguish maternal
contact barks from other females’ barks. The experiments suggest that infants
proceed through a number of different stages. First, they must learn to attend to
barks in general; that is, they must distinguish the barks from other sounds. Next,
they must associate a particular call type with the external stimulus that evoked
it. Presumably, the typical variants of particular call types serve as prototypes
because they occur more frequently. If typical variants do indeed function as
prototypes, they could then serve as perceptual anchors in the process of dissecting
the acoustic continuum into different categories.75 Whereas the association of a
given call with the context of its occurrence clearly forms part of the infant’s
general cognitive development, the latter should be viewed as part of the infant’s
perceptual development in the narrower sense.
The view that experience, and not simply maturation, mediates the development
of infants’ responses is supported by the observations that both vervets and baboons
respond to the alarm calls of birds, ungulates, and other primate species.6,60,63,76 It
seems unlikely that these responses have a genetic basis. Finally, in a cross-fostering
experiment in which Japanese and rhesus macaque infants were raised by members
of the other species, adoptive mothers learned to attend to the calls of their foster
offspring even though the infant was a member of another species.77
How do infants learn the appropriate responses to a given vocalization? On the
one hand, the observation that young vervets who first looked at an adult were more
prone to respond appropriately suggests that they may mimic the adult’s behavior.
On the other hand, juvenile Barbary macaques much more frequently ran away or
climbed into trees after playbacks of conspecific alarm calls than adults.65,78 To date,
the evidence for “teaching” and other forms of active information transmission
remains anecdotal (for a discussion, see Hauser7). McCowan and colleagues79 sug-
gested that the reason(s) why juveniles respond more readily than adults could be
due to infant error or, more plausibly, because it is adaptive to do so. Young monkeys
are more vulnerable to dangers because they are smaller and possibly less attentive
to their surroundings;79 thus, not responding to an alarm call could be more costly
for young monkeys than for adults.

IV. FUTURE RESEARCH

Compared to the vast amount of information that has accumulated about the devel-
opment of song in Passerine birds,80 little is known about early developmental
dispositions of non-human primates. In part, this is because social isolation disrupts
much of the sociocognitive development in monkeys and is therefore problematic

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on ethical as well as scientific grounds (this is not to say that social isolation would
not disrupt bird social behavior). Nevertheless, even for socially reared infants, there
is a conspicuous dearth of information on their early auditory development. For
instance, do infant monkeys and apes have a predisposition to attend to their own
species’ calls over other sounds? When infants learn to attach meaning to particular
calls, does this involve general associative mechanisms that mediate the classification
of sounds in general, or are special processes at work?
As far as vocal production is concerned, it is the author’s belief that we need to
develop a better understanding of the relatively strong constraints operating on vocal
communication in non-human primates. Why have animals such as dolphins or
parrots, but not non-human primates, evolved the ability to imitate vocally? What
is the adaptive value of vocal imitation, and what is its function? We know from
studies on dolphins that imitation plays a role in the social context,16 but are there
other functions? Finally, we need to develop a better understanding of the co-
evolution of caller and listener. For instance, given the relative small degree of
modifiability on the caller’s side, and the apparent plasticity on the listener’s side,
could it be the case that smart listeners effectively lift off selective pressure from
the caller? This question is of interest with regard to the need to communicate
effectively, as well in terms of manipulating one another’s behavior.
Many of these issues touch upon the question of the evolution of human lan-
guage. Clearly, identifying similarities between the vocal behavior of humans and
non-human primates is intriguing. In the long term, however, it may be more
rewarding to put a thorough understanding of a given species’ communicative system
first and questions into the similarity to other species’ communication second. In
other words, animal communication is fascinating in its own right, not only as a
road to human linguistic accomplishments.

ACKNOWLEDGMENTS
I gratefully acknowledge funding by the Deutsche Forschungsgemeinschaft (Fi
707/2–1, Fi 707/4–1), and I would like to thank Kurt Hammerschmidt, Mike Toma-
sello, and Robert Seyfarth for discussion and helpful comments on the manuscript.
I am indebted to Asif Ghazanfar for inviting me to contribute to this volume and
his careful editing of the chapter.

REFERENCES
1. Jackendoff, R., Possible stages in the evolution of the language capacity, Trends Cogn.
Sci., 3, 272, 1999.
2. Fitch, W.T., The evolution of speech: a comparative review, Trends Cogn. Sci., 4,
258, 2000.
3. Tomasello, M., Language is not an instinct, Cogn. Dev., 10, 131, 1995.
4. Hayes, K.J.þand Hayes, C., The intellectual development of a home-raised chimpan-
zee, Proc. Am. Philos. Soc., 95, 105, 1951.

© 2003 by CRC Press LLC

 5. Kellogg, W.N., Communication and language in home-raised chimpanzee: gestures,
words, and behavioral signals of home-raised apes are critically examined, Science,
162, 423, 1968.
6. Cheney, D.L. and Seyfarth, R.M., How Monkeys See the World, University of Chicago
Press, 1990.
7. Hauser, M.D., The Evolution of Communication, MIT Press, Cambridge, MA, 1996.
8. Tomasello, M. and Zuberbuhler, K., Primate vocal and gestural communication, in
The Cognitive Animal, A. Allen, M. Bekoff, and G.M. Burghardt, Eds., MIT Press,
Cambridge, MA, 2002, p. 293.
9. Wallman, J., Aping Language, Cambridge University Press, Cambridge, U.K., 1992.
10. Tomasello, M., Call, J., Warren, J., Frost, G.T., Carpenter, M., and Nagell, K., The
ontogeny of chimpanzee gestural signals: a comparison across groups and genera-
tions, Evol. Comm., 1, 223, 1997.
11. Winter, P., Ploog, D., and Latta, J., Vocal repertoire of the squirrel monkey (Saimiri
sciureus), its analysis and significance, Exp. Brain Res., 1, 359, 1966.
12. Winter, P.P., Handley, D., Ploog, D., and Schott, D., Ontogeny of squirrel monkey
calls under normal conditions and under acoustic isolation, Behaviour, 47, 230, 1973.
13. Talmage-Riggs, G., Winter, P., Mayer, W., and Ploog, D., Effect of deafening on vocal
behaviour of squirrel monkey (Saimiri sciureus), Folia Primatol., 17, 404, 1972.
14. Seyfarth, R.M. and Cheney, D.L., Some features of vocal development in nonhuman
primates, in Social Influences on Vocal Development, C.T. Snowdon and M. Haus-
berger, Eds., Cambridge University Press, Cambridge, U.K., 1997, chap. 13.
15. Hauser, M.D., Vocal communication in macaques: causes of variation, in Evolutionary
Ecology and Behavior of Macaques, J.E. Fa and D. Lindburg, Eds., Cambridge
University Press, Cambridge, U.K., 1996.
16. Janik, V.M. and Slater, P.J., Vocal learning in mammals, Adv. Stud. Behav., 26, 59,
1997.
17. Hammerschmidt, K., Freudenstein, T., and Jürgens, U., Vocal development in squirrel
monkeys, Ethology, 138, 1179.
18. Fitch, W.T. and Hauser, M.D., Vocal production in nonhuman primates: acoustics,
physiology, and functional constraints on “honest” advertisement, Am. J. Primatol.,
37, 191, 1995.
19. Hammerschmidt, K., Newman, J.D., Champoux, M., and Suomi, S.J., Changes in
rhesus macaque coo vocalizations during early development, Ethology, 106, 873,
2000.
20. Newman, J.D. and Symmes, D., Vocal pathology in socially deprived monkeys, Dev.
Psychobiol., 7, 351, 1974.
21. Snowdon, C.T. and Elowson, A.M., ‘Babbling’ in pygmy marmosets: development
after infancy, Behaviour, 138, 1235, 2001.
22. Hammerschmidt, K. and Todt, D., Individual differences in vocalizations of young
Barbary macaques (Macaca sylvanus): a multi-parametric analysis to identify critical
cues in acoustic signalling, Behaviour, 132, 381, 1995.
23. Hammerschmidt, K., Ansorge, V., Fischer, J., and Todt, D., Dusk calling in Barbary
macaques (Macaca sylvanus): demand for social shelter, Am. J. Primatol., 32, 277,
1994.
24. Elowson, A.M., Snowdon, C.T., and Lazaro-Perea, C., Infant ‘babbling’ in a nonhu-
man primate: complex vocal sequences with repeated call types, Behaviour, 135, 643,
1998.
25. Elowson, A.M., Snowdon, C.T., and Lazaro-Perea, C., ‘Babbling’ and social context
in infant monkeys: parallels to human infants, Trends Cogn. Sci., 2, 31, 1998.

© 2003 by CRC Press LLC

 26. Oller, D.K., The Emergence of the Speech Capacity, Lawrence Erlbaum, Mahwah,
NJ, 2000.
27. Vihman, M.M., Phonological Development: The Origins of Language in the Child,
Blackwell Publishers, Oxford, 1996.
28. Locke, J.L., The Child’s Path to Spoken Language, Harvard University Press, Cam-
bridge, MA, 1993.
29. Green, S., Dialects in Japanese monkeys: vocal learning and cultural transmission of
locale-specific vocal behavior?, Z. Tierpsychol., 38, 304, 1975.
30. Sugiura, H., Matching of acoustic features during the vocal exchange of coo calls by
Japanese macaques, Animal Behav., 55, 673, 1998.
31. Mergell, P., Fitch, W.T., and Herzel, H., Modeling the role of nonhuman vocal
membranes in phonation, J. Acoust. Soc. Am., 105, 2020, 1999.
32. Brown, C.H. and Cannito, M.P., Modes of vocal variation in Sykes monkeys (Cer-
copithecus albogularis) squeals, J. Comp. Psychol., 109, 398, 1995.
33. Hauser, M.D., Evans, C.S., and Marler, P., The role of articulation in the production
of rhesus monkey, Macaca mulatta, vocalizations, Animal Behav., 45, 423, 1993.
34. Hauser, M.D. and Schön Ybarra, M., The role of lip configuration in monkey vocal-
izations: experiments using xylocaine as a nerve block, Brain Lang., 46, 232, 1994.
35. Häusler, U., Vocalization-correlated respiratory movements in the squirrel monkey,
J. Acoust. Soc. Am., 108, 1443, 2000.
36. Jürgens, U., Neuronal control of non-human and human primates, in Current Topics
in Primate Vocal Communication, E. Zimmermann, J.D. Newman, and U. Jürgens,
Eds., Plenum, New York, 1995.
37. Jürgens, U., Neurobiology of primate vocal communication, Adv. Ethol., 36, 17, 2001.
38. Düsterhoft, F., Häusler, U., and Jürgens, U., On the search for the vocal pattern
generator: a single-unit recording study, NeuroReport, 11, 2031, 2000.
39. Fischer, J., Hammerschmidt, K., and Todt, D., Local variation in Barbary macaque
shrill barks, Animal Behav., 56, 623, 1998.
40. Mitani, J.C., Hasegawa, T., Gros-Louis, J., Marler, P., and Byrne, R.W., Dialects in
wild chimpanzees?, Am. J. Primatol., 27, 233, 1992.
41. Mitani, J.C. and Gros-Louis, J., Chorusing and call convergence in chimpanzees: tests
of three hypotheses, Behaviour, 135, 1041, 1998.
42. Mitani, J.C., Hunley, K.L., and Murdoch, M.E., Geographic variation in the calls of
wild chimpanzees: a reassessment, Am. J. Primatol., 47, 133, 1999.
43. Marler, P. and Hobbett, L., Individuality in a long-range vocalization of wild chim-
panzee, Z. Tierpsychol., 38, 97, 1975.
44. Marshall, A.J., Wrangham, R.T., and Arcadi, A.C., Does learning affect the structure
of vocalizations in chimpanzees?, Animal Behav., 58, 825, 1999.
45. Jürgens, U., On the neurobiology of vocal communication, in Nonverbal Vocal Com-
munication, H. Papousek, U. Jürgens, and M. Papousek, Eds., Springer–Verlag, Ber-
lin, 1992.
46. Arcadi, A.C., Phrase structure of wild chimpanzee pant hoots: patterns of production
and interpopulation variability, Am. J. Primatol., 39, 159, 1996.
47. Guildford, T. and Stamp Dawkins, M., Receiver psychology and the evolution of
animal signals, Animal Behav., 42, 1, 1991.
48. Janik, V.M., Whistle matching in wild bottlenose dolphins (Tursiops truncatus),
Science, 289, 1355, 2000.
49. Mitani, J.C. and Brandt, K.L., Social factors influence the acoustic variability in the
long-distance calls of male chimpanzees, Ethology, 96, 233, 1994.

© 2003 by CRC Press LLC

 50. Snowdon, C.T. and Elowson, A.M., Pygmy marmosets modify call structure when
paired, Ethology, 105, 893, 1999.
51. Giles, H., The dynamics of speech accommodation, Int. J. Sociol. Lang., 46, 1–155,
1984.
52. Deacon, T.W., The neuronal circuitry underlying primate calls and human language,
in Language Origin: A Multidisciplinary Approach, J. Wind, B. Chiarelli, B. Bichaka-
jian, and A. Nocentini, Eds., Kluwer, Dordecht, Netherlands, 1992.
53. Alipour, M., Chen, Y., and Jürgens, U., Anterograde projections of the cortical tongue
area of the tree shrew (Tupaia belangeri), J. Brain Res., 38, 405, 1997.
54. Sutton, D., Larson, C., Taylor, E.M., and Lindeman, R.C., Vocalizations in rhesus
monkeys: conditionability, Brain Res., 52, 225, 1973.
55. Fichtel, C., Hammerschmidt, K., and Jürgens, U., On the vocal expression of emotion:
a multiparametric analysis of different states of aversion in the squirrel monkey,
Behaviour, 138, 97, 2001.
56. Heyes, C.M., Causes and consequences of imitation, Trends Cogn. Sci., 5, 253, 2001.
57. Marler, P., Song-learning behaviour: the interface with neuroethology, Trends Neu-
rosci., 14, 199, 1991.
58. Janik, V.M. and Slater, P.J., The different roles of social learning in vocal communi-
cation, Animal Behav., 60, 1, 2000.
59. Seyfarth, R.M. and Cheney, D.L., The ontogeny of vervet monkey alarm calling
behavior: a preliminary report, Z. Tierpsychol., 54, 37, 1980.
60. Hauser, M.D., How infant vervet monkeys learn to recognize starling alarm calls: the
role of experience, Behaviour, 105, 187, 1988.
61. Seyfarth, R.M., Cheney, D.L., and Marler, P., Vervet monkey alarm calls: semantic
communication in a free-ranging primate, Animal Behav., 28, 1070, 1980.
62. Seyfarth, R.M., Cheney, D.L., and Marler, P., Monkey responses to three different
alarm calls: evidence of predator classification and semantic communication, Science,
210, 801, 1980.
63. Cheney, D.L. and Seyfarth, R.M., Social and nonsocial knowledge in vervet monkeys,
Philos. Trans. Roy. Soc. London Ser. B, 308, 187, 1985.
64. Marler, P., Social organization, communication and graded signals: the chimpanzee
and the gorilla, in Growing Points in Ethology, P.P.G. Bateson and R.A. Hinde, Eds.,
Cambridge University Press, Cambridge U.K., 1976.
65. Fischer, J., Hammerschmidt, K., and Todt, D., Factors affecting acoustic variation in
Barbary macaque (Macaca sylvanus) disturbance calls, Ethology, 101, 51, 1995.
66. Fischer, J., Barbary macaques categorize shrill barks into two call types, Animal
Behav., 55, 799, 1998.
67. Harnad, S., Categorical Perception, Cambridge University Press, Cambridge, U.K.,
1987.
68. Eimas, P.D., Siqueland, E.R., Jusczyk, P., and Vigorito, J., Speech perception in
infants, Science, 171, 303, 1971.
69. Fischer, J., Cheney, D.L., and Seyfarth, R.M., Development of infant baboons’
responses to graded bark variants, Proc. Roy. Soc. London Ser. B, 267, 2317, 2000.
70. Hall, K.R. L. and DeVore, I., Baboon social behavior, in Primate Behavior: Field
Studies of Monkeys and Apes, I. DeVore, Ed., Holt, Rinehart & Winston, New York,
1965, chap. 3.
71. Fischer, J., Hammerschmidt, K., Cheney, D.L., and Seyfarth, R.M., Acoustic features
of female chacma baboon barks, Ethology, 107, 33, 2001.
72. Cheney, D.L., Seyfarth, R.M., and Palombit, R., The function and mechanisms under-
lying baboon ‘contact’ barks, Animal Behav., 52, 507, 1996.

© 2003 by CRC Press LLC

 73. Rendall, D., Cheney, D.L., and Seyfarth, R.M., Proximate factors mediating ‘contact’
calls in adult female baboons and their infants, J. Comp. Psychol., 114, 36, 2000.
74. Seyfarth, R.M. and Cheney, D.L., Vocal development in vervet monkeys, Animal
Behav., 34, 1640, 1986.
75. Kuhl, P.K., Human adults and human infants show a ‘perceptual magnet effect’ for
the prototypes of speech categories, monkeys do not, Percep. Psychophys., 50, 93,
1991.
76. Zuberbuhler, K., Interspecies semantic communication in two forest primates, Proc.
Roy. Soc. London Ser. B, 267, 713, 2000.
77. Owren, M.J., Dieter, J.A., Seyfarth, R.M., and Cheney, D.L., Vocalizations of rhesus
(Macaca mulatta) and Japanese (M. fuscata) macaques cross-fostered between species
show evidence of only limited modification, Dev. Psychobiol., 26, 389, 1993.
78. Fischer, J.þand Hammerschmidt, K., Functional referents and acoustic similarity
revisited: the case of Barbary macaque alarm calls, Animal Cogn., 4, 29, 2001.
79. McCowan, B., Franceschini, N.V., and Vicino, G.A., Age differences and develop-
mental trends in alarm peep responses by squirrel monkeys (Saimiri sciureus), Am.
J. Primatol., 53, 19, 2001.
80. Catchpole, C.K. and Slater, P.J., Bird Song, Cambridge University Press, Cambridge,
U.K., 1995.

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