ANIMAL BEHAVIOUR, 2004, 67, 655e661
doi:10.1016/j.anbehav.2003.08.006
Emergence of individual recognition in young macaques
JULIA FI SC HER
Department of Comparative and Developmental Psychology, Max-Planck-Institute for Evolutionary Anthropology
(Received 8 May 2003; initial acceptance 19 June 2003;
final acceptance 3 August 2003; MS. number: 7710)
Few studies have addressed the development of nonhuman primate infants’ responses to conspecific
vocalizations. Previous studies showed that the appropriate response to alarm, intergroup and longdistance contact calls emerged at about 6 months of age. It remained unclear whether this age constitutes
a watershed in terms of infants’ sociocognitive development or whether it was due to the types of stimuli
used in the experiments. I therefore examined the development of infant Barbary macaque, Macaca
sylvanus, responses to maternal calls, under the assumption that recognition of the mother is one of the
tasks that infants should master as early as possible. I presented infants of different age categories with
short bouts of screams recorded from their mothers or another female of the same social group.
Experiments on yearlings confirmed the suitability of the experimental approach: yearlings responded
significantly more strongly to maternal calls than to calls from unrelated females. Infants were tested at 4,
10 and 16 weeks of age. In the youngest age group, they failed to respond to the playbacks, whereas from
10 weeks of age on they responded significantly more strongly to maternal calls, suggesting that by this age
they recognized their mothers by voice. These results suggest that the developmental trajectories in the
domain of comprehension learning may be flexible, in the sense that infant responses may depend on the
salience of, and the exposure to, the call type under study. The experiments also show that screams may
transmit individual-specific characteristics that are perceptually salient to the listeners.
Ó 2004 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.
Attempts to understand the roots of human language
have fuelled the majority of studies about the vocal
communication of nonhuman primates (Cheney &
Seyfarth 1990; Hauser 1996). One of the hallmarks of
language is that it is learned, in terms of both its
production and comprehension. This has led to the
question to what extent nonhuman primates show vocal
learning. While addressing this issue, it is important to
distinguish between the developmental trajectories of
vocal production, call usage and comprehension of calls
(Seyfarth & Cheney 1997; Janik & Slater 2000). Whereas
there is little evidence that nonhuman primates (hereafter
‘primates’) learn to produce their sounds through imitation, learning does seem to play a role in the usage and
comprehension of calls (Fischer 2002).
Only a handful of studies have addressed the development of primate infant responses to conspecific
vocalizations and sounds in their environment. Seyfarth
& Cheney (1986) investigated whether wild vervet,
Chlorocebus aethiops, infants’ responses to different alarm
calls appeared fully formed at birth or changed during
Correspondence: J. Fischer, Department of Comparative and Developmental Psychology, Max-Planck-Institute for Evolutionary Anthropology, Deutscher Platz 6, 04103 Leipzig, Germany (email:
fischer@eva.mpg.de).
0003e3472/03/$30.00/0
ontogeny. The alarm calls of vervet monkeys are acoustically distinct and elicit qualitatively different responses.
For instance, upon hearing an ‘eagle alarm’, vervets look
up into the air or run into a bush (Struhsaker 1967;
Seyfarth et al. 1980). After playback of the different alarm
calls, infants of 3e4 months of age typically ran to their
mothers, no matter which call was broadcast. Between 4
and 6 months, infants more and more often behaved like
adults; however, in a considerable number of instances,
they responded to calls with a ‘wrong’ (i.e. maladaptive)
behavioural strategy. From the age of 6e7 months on,
most infants responded to alarm calls as adults did,
suggesting that experience plays a role in the formation
of the appropriate response (Seyfarth & Cheney 1986).
Hauser (1989) showed in a playback study that infant
vervets first responded to the intergroup call (‘wrr’) at
about 6 months of age. Prior to that, they showed no
apparent responses to the call. One factor that seemed to
play a role in the acquisition of call meaning was the rate
of exposure. Vervets attend to the alarm calls of the superb
starling, Spreo superbus. These alarm calls occur at different
rates in different habitats. Hauser (1988) showed that
infant vervets who were exposed to the alarm calls at
a higher rate responded to these calls appropriately at an
earlier age than infants who were exposed to these calls at
a lower rate.
655
Ó 2004 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.
656
ANIMAL BEHAVIOUR, 67, 4
Whereas previous studies examined responses to calls
that were acoustically distinct, Fischer et al. (2000)
examined when free-ranging infant chacma baboons,
Papio cynocephalus ursinus, begin to discriminate between
variants of the same general call type, the loud call or
‘bark’ of female baboons, which grade from clear harmonic into more harsh and noisy variants. The clear
variants are typically given when subjects have lost
contact with the troop or a particular subject, whereas
the noisy variants are typically given when the caller has
spotted a predator (Fischer et al. 2001). Results of playback
experiments indicated that infant baboons gradually
develop the ability to discriminate between calls that fall
along a graded acoustic continuum. At 2.5 months of age,
infants failed to orient to the speaker after playbacks of
either alarm or contact barks; at 4 months, they responded
to playback of both alarm and contact barks indiscriminately, and, at 6 months, they responded strongly to alarm
barks, but failed to orient to contact barks. By this age,
therefore, infants reliably discriminated between typical
variants of alarm and contact barks.
In both vervet and chacma baboon infants, the
appropriate response to, and hence the correct classification of, alarm and contact calls emerges at about 6 months
of age (Seyfarth & Cheney 1986; Hauser 1988, 1989;
Fischer et al. 2000). It remains unclear, however, whether
6 months constitutes a watershed in terms of the infants’
cognitive development or whether some types of calls
might be discriminated at even younger ages. Longdistance calls present the infant with a demanding
problem, both because they are relatively rare and because
it is often difficult for the infant to identify the causes that
elicited them. I therefore initiated the present study to
examine the development of Barbary macaque, Macaca
sylvanus, infants’ responses to maternal calls, under the
assumption that recognition of the mother is one of the
tasks that infants should master as early as possible.
Furthermore, lack of exposure to the stimuli can also be
excluded, because infants spend most of their time with
their mothers. The development of maternal recognition
in infants should therefore provide insight into early
learning abilities in the vocal domain. Individually
distinctive calls and differential responses to specific
individuals’ calls have been shown in a number of primate
species, including Barbary macaques (Hammerschmidt &
Todt 1995 and references therein). Individual differences
in vocalizations are also widespread in many other
mammals and birds (Allenbacher et al. 1995; Peake et al.
1998; Tyack 2000; Charrier et al. 2003).
I studied a population of Barbary macaques living in the
20-ha enclosure ‘La Forêt des Singes’ at Rocamadour,
France. Barbary macaques are especially suited to addressing the question of early recognition because they have an
extended alloparental care system in which infants spend
considerable time away from their mothers in the care of
an adult male or other caretakers (Paul et al. 1992, 1996). In
such situations, infants are typically held by the ankle and
are prevented from returning to their mothers (Riechelmann et al. 1994). Thus, infants are away from their
mothers without human interference for long periods.
Although the animals in this study were clearly not living
under natural conditions and were hence not subject to,
for instance, predation pressure or times of food shortage,
the experimental conditions are comparable to the studies
mentioned above, as animals were not constrained and
were free to walk away from the experimental scene.
One potential confounding factor of any study that
attempts to investigate the onset of maternal recognition
by infants is that the failure to demonstrate such an ability
might be due to flaws in the experimental protocol rather
than to subjects’ incompetence. To assess the suitability of
the experimental protocol, therefore, I first conducted
a set of experiments on yearlings. As playback stimuli, I
used short screams recorded either from the mother or
from an unrelated female from the same social group.
Screams occur frequently either in attempts to recruit
support from allies and relatives (Gouzoules & Gouzoules
1995) or to repel aggressors (Todt 1988) and are
individually distinct (Hammerschmidt & Todt 1995;
Hammerschmidt & Fischer 1998a).
METHODS
Study Site and Subjects
I conducted this study between May and September of
2001 and 2002. ‘La Forêt des Singes’ is a visitor park where
monkeys range freely while visitors are restricted to a path.
The macaques are well habituated to human observers and
are tattooed with an individual code on the inside of the
thigh. They are provisioned with monkey chow provided
in feeder huts, and with apples, grain and seeds, which are
spread throughout the park. Visitors are allowed to feed
them with popcorn provided by the park management.
The vegetation consists mainly of oak (Quercus spp.) and
juniper ( Juniperus spp.). Details of the park management
are given in Turckheim & Merz (1984). At the beginning of
the study, the population consisted of 128 macaques and
was divided into three stable social groups consisting of
37, 52 and 39 animals, excluding newborns (Table 1).
Table 1. Subject codes, sex, birth date, ID of mother, ID of unrelated
female and group membership of subjects in the experiments
ID infant
Sex
Birth date
m D370
f D371
m D371
f D370
m D372
f D372
m E380*
f E380*
m E381*
m F390
f F390
f F391
m F391
i330
f F392
Male
Female
Male
Female
Male
Female
Male
Female
Male
Male
Female
Female
Male
Male
Female
8 April 2000
24 April 2000
25 April 2000
5 May 2000
21 May 2000
13 June 2000
18 April 2001
15 May 2001
11 June 2001
18 April 2002
23 April 2002
21 May 2002
30 May 2002
12 June 2002
16 June 2002
ID
ID
unrelated
mother female Group
T268
T269
P223
Z320
X300
P224
M189
O200
Z324
Y311
M192
O208
B352
A330
A332
L170
K144
R250
B331
H90
Y311
T267
R253
H90
P224
O200
T269
A331
Z320
Z324
PB
VOL
VOL
PB
VOL
GB
PB
GB
VOL
GB
GB
VOL
PB
PB
VOL
*These subjects were tested both as infants and as yearlings.
FISCHER: EARLY INDIVIDUAL RECOGNITION
Barbary macaques are seasonal breeders with a birth
season in spring and a mating season in autumn (Paul
1984; Small 1990). I conducted experiments on three
infants born in 2001 and on six infants born in 2002
(Table 1). The study was somewhat hampered by high
infant mortality: over the study period, eight infants died
shortly after birth. Experiments on yearlings were conducted in 2001 on six subjects born the year before, and in
2002 on the three subjects that had participated as infants
(Table 1). These three subjects were included to augment
the sample size and to allow for the inclusion of possible
confounding factors in the statistical analysis (see below).
Call Selection
I recorded calls used for playback using a SONY WM
TCD-100 DAT recorder and a Sennheiser directional
microphone (K6 power module and ME66 recording head
with MZW66 pro windscreen). The distance between the
caller and the microphone ranged between 3 and 10 m.
Whenever an animal vocalized, I spoke on to the tape
recorder a detailed description of the context before and
after calling. Selected call sequences were then uploaded
on to an IBM compatible notebook using the 24-bit U2A
waveterminal USB audio interface (Ego-Sys, Seoul, Korea)
for subsequent editing of the playback stimuli.
Playback stimuli for each subject consisted of screams
recorded from two adult females: the subject’s mother
(‘maternal’ condition) and an unrelated female of the
same social group (‘unrelated’ condition). The calls were
extracted from longer, naturally occurring scream sequences and edited using CoolEdit 2000 (Syntrillium,
Phoenix, AZ, U.S.A.). Each playback stimulus consisted of
two short screams separated by 300 ms of silence, which
removed any individual distinctiveness in the temporal
patterning of the calls. The interval corresponds to the
average intercall interval G SD of 296G100 ms determined from 19 scream bouts recorded from 19 females. I
aimed to match calls in terms of acoustic structure as
assessed by auditory impression and inspection of spectrograms, and also in terms of the caller’s age. The
average scream duration G SD was 195G69 ms in the
maternal condition and 201 G 66 ms in the unrelated
condition. A pairwise comparison of the scream pairs
revealed no significant differences in average scream
lengths in the maternal and the unrelated condition (sign
test: P ¼ 0:6). Five of the calls that were used in the
maternal condition were used as stimuli in the unrelated
condition for other subjects.
Figure 1 shows spectrograms of the calls used for two of
the subjects. After editing, playback stimuli were dubbed
back on to the DAT recorder, while amplitude was
controlled: the average sound pressure level (SPL) was
78:9G0:7 dB in the maternal condition and 78:8G0:5 dB
in the unrelated condition, measured at 70 cm from the
speaker under laboratory conditions (dB SPL re 20 mPa;
C-weighting, SPL meter Rion NL-05, Rion Co., Tokyo,
Japan). In the field, the amplitude range was 55e60 dB
SPL measured at 7 m, with background sound pressure
Figure 1. Spectrograms of calls used in the playback experiments for two of the subjects. Each infant was presented with two short screams,
recorded either from the mother or from an unrelated female.
657
658
ANIMAL BEHAVIOUR, 67, 4
levels of 50e60 dB SPL on a calm day. Behavioural
observations showed that screams occur frequently: on
average, we noted 10.6 scream bouts per h and group
(range 0e27 bouts/h). Bouts typically consisted of several
consecutive calls (XGSD ¼ 11:7G9:3; measured from
N ¼ 28 recorded bouts, range 4e41 calls). However, single
screams may also occur. I used only two screams in each
trial to avoid strong responses from other animals, such as
approaching the speaker. The presentation of the playback
stimuli did not noticeably augment the rate of delivery of
these calls.
Experimental Protocol
Five of the nine yearlings were presented with the
maternal calls first, and the remaining four with the
unrelated calls first. Infants were tested at 4, 10 and 16
weeks of age. At each age category, they were presented
with calls recorded from their mothers and from unrelated females. In the youngest age category, four of the
nine infants were presented with the maternal calls first,
and five with the unrelated calls. In the next age
category, the order of presentation was reversed. For
logistical reasons and because situations suitable for
playback arose much less frequently than anticipated,
infants could be tested only every 6 weeks, and infant
mortality meant that not all infants could be tested at
each age category. All infants were tested at an average
age of 4 weeks; six of these infants were tested again at an
average age of 10 weeks, and five were tested at an
average age of 16 weeks. Each infant was tested only once
per condition and age category.
Playback stimuli were marked with a random code so
that I did not know whether the mother’s or another
female’s calls would be presented to the infant when I
conducted the experiments. Trials were conducted with
the help of a second observer who was responsible for
running the playback device and hiding the speaker
behind bushes or tall grass (SONY DAT TCD-D100
recorder and NAGRA DSM powered loudspeaker) while I
recorded the subject’s behaviour on videotape (SONY DCR
PC 100 digital video camera) and determined the onset of
the trial. We searched for a target infant and initiated
a playback trial opportunistically when the alloparent and
infant were foraging or resting. I ensured that the mother
and the other female whose call might be played were out
of sight. Since at the two youngest age categories, infants
were typically held by the alloparent at the ankle,
orienting towards the speaker was all that could be scored
in response to playbacks.
We placed the speaker approximately at a right angle to
the subject, at a mean distance of 7.6 m (range 6e9 m)
from the subject. The playback was initiated when the
subject had been looking away from the loudspeaker, so
that no baseline looking time had to be taken into
account. I filmed the behaviour of the subject for
approximately 20 s before the playback and 20 s thereafter. I also noted the subject’s behaviour, as well as date,
time, location of the playback, and the number and
identity of individuals in the vicinity. For the yearlings,
2e11 days passed between consecutive playbacks. Within
each age category, each infant was tested within 2 days
(median; range 1e5 days).
Data Analysis
Video recordings were uploaded to an IBM compatible
notebook computer and analysed on a frame-by-frame
basis with the Adobe Premiere Software version 5.1
(25 frames/s), still blind to the experimental condition. I
measured the latency to respond (time between onset of
call and onset of response) and scored only responses that
occurred within 2 s of the onset of any given call. When
subjects looked at the speaker, I determined the duration
of responses that involved a head turn of at least
approximately 45( to the loudspeaker. When subjects
began to approach the speaker, I also noted the time spent
travelling to the loudspeaker and added it to the looking
time to yield a compound measure of response duration.
To assess observer reliability, a second observer also blind
to the experimental design scored the looking time for 13
randomly selected trials. Kendall’s coefficient of concordance was 0.99 (P!0:05).
I used GLMM (general linear mixed-effect model;
maximum likelihood estimation) to assess which factors
affected infant responses to the playback, testing both
response duration and latency to respond. GLMM analyses are an extension to GLM, which allow the incorporation of ‘subjects’ as random effects to control for
replicated observations (Pinheiro & Bates 2000). For the
yearlings, I used subject ID as a random factor, the
experimental condition (maternal or unrelated) and
speaker placement (left or right) as fixed factors, and
speaker distance and number of subjects in the vicinity as
covariates. For the infants, I used infant ID as a random
factor, and the age category, the experimental condition
and speaker placement as fixed factors; speaker distance
and the number of subjects in the vicinity were entered as
covariates. For the infants, I considered only the looking
time duration, not overall response duration. I first
calculated the initial model with all factors and then
examined different models using Akaike’s information
criterion (Pinheiro & Bates 2000) to identify the best
model. SPSS v. 11.5 was used for all analyses (SPSS Inc.,
Chicago, U.S.A.).
RESULTS
Yearlings responded more strongly to the playback of
maternal screams than to the calls of unrelated females
(Fig. 2). In two of the trials in which the screams from an
unrelated female were presented, subjects showed no
apparent responses. In contrast, in two of the trials in
which the mother’s screams were broadcast, yearlings
interrupted their prior activity and approached the
speaker. In one case, the yearling showed affiliative facial
gestures (lip smacking and teeth chattering) as he walked
towards the bush behind which the speaker was hidden.
The final model contained only the experimental condition as an independent variable (F1;18 ¼ 4:51, P!0:05), as
FISCHER: EARLY INDIVIDUAL RECOGNITION
Response duration (s)
6
*
5
4
3
2
1
0
Maternal
Unrelated
Figure 2. Response duration (X þ SD) of yearlings after playback of
screams recorded from their mother or an unrelated female.
)P!0:05 (GLMM analysis).
none of the possibly confounding variables had a significant effect on response duration (speaker placement:
P > 0:6; number of subjects in the vicinity: P > 0:2;
distance to the speaker: P > 0:8). The average latency to
respond G SD was 0:38G0:25 s, and was not affected by
any of the factors in the analysis. Thus, the experiments
on yearlings showed that this experimental paradigm was
suitable to uncover differences in responses to maternal
versus unrelated females’ screams by infants.
Infants’ responses changed with age and varied in
relation to the experimental condition (Fig. 3). In the
youngest age category, infants rarely responded to the
playback of any female screams. From the age of 10 weeks
on, they consistently responded to playbacks of maternal
calls. In contrast, they often failed to respond to the
playback of the unrelated female’s calls. In those few cases
where infants responded to the playback of calls recorded
from an unrelated female, they spent less time looking at
the speaker. The statistical analysis revealed a significant
interaction between age category and condition (F2;29:6 ¼
3:99, P!0:05). Neither speaker placement (P > 0:4), nor
number of subjects in the vicinity (P > 0:8), nor distance
to the speaker (P > 0:8) had a significant effect on looking
time duration, and were therefore not part of the final
Looking time (s)
8
*
7
*
6
5
4
NS
3
2
1
0
M
UF
4
M
UF
10
Age of infant (weeks)
M
UF
16
Figure 3. Looking time duration (XCSD) for infants in the different
age classes after playback of screams recorded from their mother (M)
or an unrelated female (UF). )P!0:05 (GLMM analysis).
model. The latency to respond was influenced only by the
infants’ age: as infants grew older, latency to respond
decreased significantly (F2;18:2 ¼ 5:696, P!0:05). The
mean G SD latency to respond decreased from
0:82G0:48 s in the first age category to 0:72G0:40 s in
the second and 0:43G0:32 s in the third. Post hoc tests
revealed significant or marginally significant differences in
the latency to respond between the first versus third
(P!0:01) and the second versus third (P!0:1) age
categories.
It would have been desirable to include in the regression
model the degree to which infants’ responses were
influenced by responses of other adults nearby, specifically
those of adults that held them by the ankle. However, as
infants grow older, they spend more and more time alone
or with other infants and juveniles, so that the consideration of this factor would have reduced the sample size. As
a first attempt to resolve this question, I therefore simply
examined whether infant responses occurred more frequently when the caretakers also responded by looking
towards the speaker. Results suggested that infants’
responses were not related to their caretakers’ responses
(log likelihood ratio: c21 ¼ 0:3, N ¼ 32, P > 0:8).
DISCUSSION
From as early as 10 weeks of age, Barbary macaque infants
responded significantly more strongly to playbacks of
their mothers’ calls than to playbacks of unrelated females
from the same social group. Apparently, infants were able
to recognize their mothers by voice from this early age
onwards. A prerequisite for the recognition of different
individuals is the discrimination of individually distinctive screams. Thus, at the very least, infants are able to
distinguish between their mother’s and other females’
voices by the age of 10 weeks. In the youngest age
category, infants showed few responses to the playback of
any female’s screams, supporting the view that in nonhuman primates, vocal production and comprehension
unfold along very different developmental trajectories.
Barbary macaque infants produce a variety of screams and
also ‘geckers’ from the first day of life (Hammerschmidt &
Todt 1995). By contrast, the comprehension of calls sets in
later and develops gradually. This finding corroborates the
assumption that the structure of the vocalizations is
largely innate, whereas call comprehension is based on
learning (Seyfarth & Cheney 1997).
When assessing infant responses it is important to
distinguish between the different components that underlie correct responses to calls. First, infants must attend
to the calls; second, they must attach the correct meaning
to the calls in the sense that they must associate the calls
with the stimulus that elicits the calling. Third, they must
be able to produce an adequate response (Fischer et al.
2000). The lack of responses at the youngest age category
cannot simply be attributed to a motor inability to turn
the head: Paul (1984) reported that in their first week of
life, Barbary macaque infants turned towards moving
objects in their vicinity and produced chewing jaw
movements in response to animals who lip-smacked at
659
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ANIMAL BEHAVIOUR, 67, 4
them. Thus, from a very early age, infants attend to the
gestures and social behaviour of conspecifics nearby.
Possibly, the lack of responses at the youngest age category
is due to the fact that sounds that are not paired with
visual stimuli fail to elicit the infants’ attention. It is also
possible that the infants in fact discriminated between
their mother’s and other females’ voices before differences
in response became apparent; that is, the response assay
was insensitive to possible changes in heart rate or other
variables that may indicate differential responses. Human
infants prefer their mother’s voice within a few days of
birth, presumably because of experience in the womb (for
an overview, see Locke 1993). However, the point of my
study was to elucidate what the animals ‘do do’, not what
they ‘can do’ (Nelson & Marler 1990). Therefore, the
possibility of an earlier discrimination does not influence
my conclusions.
The lack of responses at the youngest age class replicates
the findings from the study on infant baboons reported
above (Fischer et al. 2000) in which the youngest subjects
failed to show any responses. One may therefore conclude
that this initial lack of response is irrespective of the call
type. Subantarctic fur seal pups, Arctocephalus tropicalis,
begin to distinguish between their mother’s and other
females’ vocalizations within the first week of life, before
the mother takes off for her first extended foraging trip
(Charrier et al. 2001). In this social system, reunification is
based on mutual calling, and, therefore, natural selection
has probably posed a high premium on pups’ early ability
to respond differentially to their mothers. In primates, in
contrast, it is the mother who is mainly responsible for reestablishing contact with the infant when it is still very
young (Altmann 1980).
In contrast to previous work on baboons (Fischer et al.
2000), in which infants responded indiscriminately to
different call variants before they began to distinguish
them, no such pattern became apparent among the
Barbary macaque infants. This might be because infants
were tested at intervals too large to detect such a phase, or
because, once infants attended to the calls, they immediately began to discriminate between their mother’s and
other females’ calls. Unfortunately, more frequent testing
was not possible to address this question. Nevertheless,
the present findings suggest that the development of
infant responses may depend both on the call type and on
exposure to the call, that is, the infants’ experience with
a certain call category. It would be desirable to study in
more detail the effects of rate of exposure and salience of
the call type on the development of infant responses.
However, this is probably feasible only under more
controlled conditions.
This study showed that Barbary macaque infants are
able to associate specific calls with a specific individual
(their mother) at a much earlier age than 6 months, the
age at which baboon infants distinguish between different
long-distance calls. Notably, at the age of 10 weeks, when
Barbary macaque infants responded significantly more
strongly to their mothers’ than to other females’ calls,
baboon infants failed to show any responses to the
playbacks of alarm or contact calls from unrelated females.
The Barbary macaque infants’ development cannot be
compared directly with the development observed in
vervet infants because vervets develop distinct escape
responses, whereas Barbary macaque infants simply show
prolonged looking time after presentation of the mothers’
calls. However, my experiments add to the body of
evidence (Hammerschmidt & Fischer 1998b) that individual differences in Barbary macaque scream vocalizations (Hammerschmidt & Todt 1995) are meaningful
and evoke adaptive responses from listeners, even when
they are very young.
My results suggest that infant responses, looking
towards the speaker, were not influenced by the behaviour
of their alloparental caretakers, that is, whether he or she
looked towards the speaker. Several studies show that
nonhuman primates regularly follow the gaze of others
(Tomasello et al. 1998, 1999). Fewer studies have systematically examined the ontogeny of gaze following in
nonhuman primates. Tomasello et al. (2001) investigated
the age at which rhesus macaque, Macaca mulatta, and
chimpanzee, Pan troglodytes, infants began to follow the
gaze of the human experimenter. In rhesus macaques,
subjects followed the gaze of the experimenter at 5.5
months of age. Possibly, however, gaze following among
conspecifics sets in at an earlier age. Clearly, there is still
a need to develop a better understanding of the mechanisms that mediate auditory comprehension learning in
nonhuman primates. To date, there is only indirect and
partly contradictory evidence on how much infant
responses to calls are influenced by adult behaviour. For
instance, Seyfarth & Cheney (1986) reported that vervet
infants were more likely to respond correctly to the
different alarm calls when they had first looked at an
adult. In contrast, infant baboons responded to intermediate alarm and contact barks which were typically
ignored by adults, suggesting that infants did not copy
adult behaviour (Fischer et al. 2000). Similarly, after
playback of conspecific alarm calls, infant and juvenile
Barbary macaques more frequently ran away or climbed
on to trees than adults did (Fischer et al. 1995; Fischer &
Hammerschmidt 2001). It remains unclear, however, how
much infant responses are influenced by juvenile behaviour. Similarly, we need to investigate whether nonhuman
primate infants have a predisposition to attend to their
own species’ calls over other sounds, and whether the
attachment of ‘meaning’ to particular calls involves
general associative mechanisms that mediate the classification of sounds in general or special processes that are
dedicated to species-specific sounds.
Acknowledgments
I thank Ellen Merz and Gilbert de Turckheim for
permission to conduct this study at ‘La Forêt des Singes’
at Rocamadour, Kurt Hammerschmidt for support and
discussion throughout the study, and Christoph Teufel,
Catherine Crockford and Simone Pika for helping with the
experiments. I am grateful to Dorothy Cheney, Robert
Seyfarth, Catherine Crockford and Elena Lieven for
discussion and comments on the manuscript. Daniel
Stahl provided valuable statistical advice; and the helpful
FISCHER: EARLY INDIVIDUAL RECOGNITION
suggestions of two anonymous referees are gratefully
acknowledged. This research was supported by the
German Science Foundation (Fi707/4).
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