The International Journal of Animal Sound and its Recording, 2011, Vol. 20, pp. 341–356
© 2011 AB Academic Publishers
HOW AND WHEN DO LAMBS RECOGNIZE THE
BLEATS OF THEIR MOTHERS?
, THIERRY AUBIN
, RAYMOND NOWAK
, OLIVIER SÈBE
AND PASCAL POINDRON
Equipe Comportements, Neurobiologie et Adaptation, UMR 6175 INRA/CNRS/
Université de Tours/Haras Nationaux, 37380 Nouzilly, France.
Equipe Communications Acoustiques, NAMC CNRS UMR 8620, Université Paris-
Sud, Bât. 446, 91405 Orsay Cedex, France
Geophysical Institute, Universtät Karlsruhe (TH), Hertzstrasse 16, D-76187
Karlsruhe, Germany now at CEA¬DASE-LDG,BP12, 91680 Bruyères-le-Châtel,
In domestic sheep Ovis aries, the mother and the young display a preferential bond
for each other that relies on multimodal inter-individual recognition. Lambs show
a preference for their own dam shortly after birth, and this is important for their
survival. The role of acoustic cues in this early preference for the mother is not clear.
The aim of the present work was to analyze the timing of acoustic recognition of the
mother and to identify the physical parameters used in the recognition of maternal
bleats by the lamb.
In a rst study, we investigated the ability of lambs to discriminate between
the bleats of their own mother and an alien equivalent mother in a two-choice
test. Both ewes were hidden behind a canvas sheet and lambs were not allowed
to approach the dams closer than 1 m, thus preventing visual as well as olfactory
perception. Tests were conducted 12 hr, 24 hr or 48 hr after birth (n=19 or 20/group).
An indication of vocal discrimination was already present at 24 hr and at 48 hr lambs
spent signicantly more time near their mother than near the alien dam.
In a second step, we investigated which physical parameters of the bleats were
important for recognition. For this, we conducted playback experiments with modied
bleats at two weeks postpartum. Ours results show that lambs pay attention to a
combination of various time, energy and frequency parameters: timbre (distribution of
energy within the spectrum), amplitude and frequency modulations appear to be the
most important parameters encoding the individual signature.
We conclude that vocal recognition between the ewe and her lamb plays an
important role in the display of preferential mother-young bond from very early on.
Our studies also demonstrate that the encoding of the individual signature is not
limited to the frequency domain but rather involves a multiparametric encoding
Key words: vocal recognition, sheep, bleats, playback, maternal behaviour
In mammals, maternal investment is a key determinant of reproductive
tness, as young are unable to survive without milk and adequate
maternal care (Walser 1978; Clutton Brock 1991). This is particularly
true in gregarious species, in which mother-young recognition ensures
exclusive care of their own progeny (Lynch et al. 1992; Poindron et al.
2007). The sheep is a good experimental animal model for the study
of maternal behaviour and selective bonding because the maternal
behaviour of ewes is characterized by the development of an exclusive
bond with the newborn (González-Mariscal & Poindron 2002; Poindron
et al. 2007). Sheep are mostly synchronized, seasonal breeders and
therefore, many young may be born within a very short period of time.
Also, ewes give birth to precocial young that are relatively mature
and mobile at birth. Therefore, mothers must be able to recognize
their offspring selectively to avoid separation which may be fatal to
their young (Lent 1974) and to avoid allosuckling. After becoming
selective, the ewe begins to show aggressive responses to alien young
that attempt to suck her (Poindron et al. 1993). As a consequence
maternal selectivity demands that the lambs recognize their mother
very quickly after birth for access to milk (Vince 1993).
The dynamics and mechanisms involved in recognition vary
depending on whether we consider the mother or the young. Keller
et al. (2003) showed that most ewes showed selectivity at suckling
as early as 30 min after parturition and that they can discriminate
between own and alien lambs from a distance after 6 hr of contact.
Lambs, on the other hand, are lower than their dams; they can
readily identify their mother between 12 and 24 hr of age but only
at close quarters (less than 50 cm: Nowak 1990; Nowak & Lindsay
1990). By 3 days old they can recognize their dam at a distance of
several meters (Nowak 1990; Nowak 1990). .Mutual recognition also
relies on various sensory cues (olfaction, vision or hearing) and on
whether recognition occurs at long or short distances. For example,
for both ewe and lamb, recognition from a distance mainly depends
on visual and acoustic cues (Lindsay & Fletcher 1968; Alexander &
Shillito 1977). At very close range, recognition is mainly based on
olfactory cues even though visual and acoustic cues may also be
used (Alexander 1977; Alexander & Shillito 1977; Lynch et al. 1992).
Recognition of the mother by her lamb is important for its survival,
and this depends mainly on visual and acoustic cues (Nowak 1991;
Terrazas et al. 2002).
Visual recognition has been shown (Shillito 1975; Alexander &
Shillito 1977; Kendrick et al. 1996) but acoustic cues appear to be
more fundamental in longer range recognition, since the efciency of
visual cues can be reduced by distance, particularly when lambs and
ewes congregate into large groups. For example, Searby and Jouventin
(2003) showed, in playback experiments, that lambs recognise their
own mother from three days to two weeks after birth. Moreover, lambs
that were the most vocal at birth also had the best performances in a
test of the lamb’s ability to discriminate the mother at the age of 12
hr postpartum (Nowak 1990; Nowak & Lindsay 1990). This suggests
that vocal communication is more important than rst thought and
that lambs must establish acoustic discrimination early on after
Very few studies have focused on the acoustic parameters that
provide information about the mother’s identity. Using playback
experiments, Searby & Jouventin (2003) have shown that the mother’s
call constitutes a vocal signature recognized by the lambs. These
authors pointed out in sheep a simple signature system that relies
only on the frequency domain. This contrast with results obtained
on other animals breeding in large colonies or in extremely confusing
context (many individuals using vocal communication in the same
time attempting to recognize), showing that young rely on several
acoustic parameters, belonging not only to the frequency but also
to the amplitude domain (Lengagne et al. 1997; Aubin & Jouventin
2002). Thus, even though the importance of the mean fundamental
frequency is well established for individual acoustic recognition in
ewes and lambs, the role of other acoustic parameters still needs to
The aim of the present work was to specify when and how lambs
recognize the bleats of their mother. In a rst study, we determined
the timing of development of the early acoustic discrimination, by
comparing the behaviour of lambs in a two-choice test at 12 hr, 24
hr and 48 hr after birth. Lambs were individually exposed to bleats
from their own and an alien mother hidden behind a canvas sheet. In
a second study, the objective was to identify the acoustic parameters
of mother’s bleats that are relevant for recognition by her lamb. By
playing back maternal bleats that were acoustically modied we
wanted to clarify whether vocal identication depends on single or
MATERIALS AND METHODS
Animals and Management Conditions
The Ile-de-France ewes and their lambs used in the two studies
presented in this article were kept indoors under the same general
conditions. All the lambs were born at the INRA Research Centre
located in Nouzilly, France, where the experiments were conducted.
When a ewe was about to give birth, she was penned individually and
kept there with her lambs for 6 hr to allow adequate development
of the mother-young relationship. At 6 hr postpartum, mothers and
their offspring were transferred into another communal pen with
others ewes and lambs. This allowed interactions with other animals
and thus presumably stimulated the establishment of discrimination
between individuals (Val-Laillet & Nowak 2006).
Study 1: Vocal Discrimination by Lambs during the First
Two Postpartum Days
Discrimination of ewes by their lambs: experimental groups and
The full details of the experimental materials and methods have been
reported elsewhere (Sèbe et al. 2007) and are only briey described
here. Three independent groups of lambs were tested at 12 hr (n =
20), 24 hr (n = 19), or 48 hr (n = 19) after birth, using as stimuli
their mother (hereafter called “own” ewe) and another ewe that had
lambed at about the same time (hereafter called “alien” ewe). Lambs
were not tested before 12 hr of age, as there is no evidence that they
can display a preference for their mother earlier in a two choice test
procedure (Nowak et al. 1987; Nowak 1991; Terrazas et al. 2002).
The testing procedure was similar to the one used in previous
studies by Ferreira et al. (2000) and Terrazas et al. (1999). Lambs
were tested in a 7 m x 5 m x 5 m triangular testing enclosure (see
Figure 2 in Sèbe et al. 2007). Each of the two stimulus mothers (the
‘own’ and the alien mother) was placed in one of the two holding
pens that were located at the two corners of the testing enclosure
(Terrazas et al. 1999; Ferreira et al. 2000; Sèbe et al. 2007). Mothers
were hidden by an opaque canvas, and two sets of hurdles spaced 1
m apart prevented the lambs from approaching the ewes at less than
1 m, a distance too big to allow olfactory identication of the mothers
(Alexander & Shillito 1977; Alexander 1978; see also Poindron et al.
2003 in goats).
The position of the own mother alternated for each test. In
all the tests, each stimulus mother vocalized at least ten times and
the lambs reached at least one of the two proximity zones. In all
instances, the alien stimulus mothers were from the same communal
rearing pen as the tested lamb, so that they were not totally
unknown to it. The total time spent (s) in the proximity zone near
each stimulus animal (1-2 m to hidden ewes) was recorded during the
3-minute test by two trained observers. Neither of the observers who
recorded the behaviour in the test knew the identity and side of each
stimulus animal. At the end of the test, the ewes and their lambs
were immediately reunited and returned to their home pen.
Study 2: Playback experiments with modied calls
The study was performed on 15 day-old lambs (± 1 day). At this age,
lambs are still suckling and dependant on their mothers. Each lamb
was caught and placed in a small pen inside the barn while its mother
was kept 1 m away, so that visual contact was always maintained.
Vocalisations exchanged between mothers and lambs were recorded
1 day before the playback tests, using a Marantz PMD 670 digital
recorder (sampling frequency: 32,000 Hz) connected to a Beyer dynamic
microphone M88 TG (frequency response: ± 2.5 dB within the range
20-20,000 Hz). The distance between the microphone and the head of
the recorded animal was 1 m. Only high-pitched bleats were recorded,
i.e. loud calls emitted with the mouth open (Dwyer et al. 1997; Dwyer
et al. 1998), since it is the main type of vocalisations emitted by ewes
and lambs at this stage of the mother-young relationship (Sèbe et
al. 2007) and also because they represented the great majority of
bleats emitted during this type of separation or during a two-choice
preference test as in study 1. Sound les were then transferred into
a computer, and the mothers’ bleats were selected for subsequent
manipulation and broadcast.
Ewe calls were played back to 134 lambs in their living pen inside the
barn, without mother-young separation and in the presence of ewes
and lambs of the same group. Eight independent groups of lambs
were tested (≈18 dyad/pen in 60 m²). Animals were studied using focal
watches (i.e. one dyad or mother-lamb couple at a time). We played-
back three types of series made of control (unmodied mother bleats),
modied mother or alien bleats. One experimental series played back
consisted of three different bleats of the same mother separated by
2.5 s of silence. To avoid habituation (McGregor 1992), each lamb was
not tested more than twice, with the control in each test and with a
minimum of two hours between two playback sessions. The order of
presentation of the series was randomised for each lamb. The series
were played at an intensity level similar to that of the natural voices
of ewes as controlled by a sound level meter. A computer connected
to a unidirectional loudspeaker (TANNOY coaxial 80 W/6 Ohms) was
used for the playback. The loudspeaker was placed in a corner of the
pen, one metre outside and the playback was carried out when subjects
were at 3-6 m from the loudspeaker and away from the mother. In
addition, we performed the playback 30 min after suckling, a stage
when lambs are motivated to respond to their mother’s call. The
interval of 30 min was chosen because we had found in a previous
study that, at two weeks of lactation, ewes nurse their lamb between
once and twice per hour (Sèbe et al. 2008), consistent with other
observations (Ewbank 1964; Fletcher 1971; Schirar et al. 1989).
● Control experiment: do lambs respond selectively to their own
mother’s voice? To conrm the ability of lambs to discriminate their
mother among others, we played back to lambs a series of three
‘control calls’ (non-modied) from their own mother and a series
of three calls from an alien mother. The presentation of the two
series was randomized for each lamb (n = 19).
● Experimental signals
We created experimental signals by modifying the frequency and
temporal domains of the mothers’ control calls (Figure 1A). We
were interested in the process of recognition of the mother’s voice
by their lambs, so each lamb was tested with experimental signals
prepared from its mother’s calls. Modications of the control calls
were performed using Syntana (Aubin 1994), Avisoft (Avisoft-
Figure 1. Spectrograms of mother bleats and bleats modied in temporal and
frequency domains and used in playback experiments to lambs. (A) Non-mod-
ied mother’s bleat (control); (B) Low-pass Q50%; (C) Low-pass Q75%; (D)
high-pass Q50%; (E) Linear frequency shifts +50 Hz; (F) Linear frequency
shifts +100 Hz; (G) Linear frequency shifts +200 Hz; (H) without amplitude
SASLab Pro 2006), Matlab and Goldwave packages (Craig 1996).
For each experimental signal, we compared the lambs’ response
obtained with alien or own mother’s control calls.
● Experiment 1: is the whole spectrum necessary?
The mother’s bleats were ltered by high-pass or low- pass digital
lters. The cut-off frequencies of these lters were chosen to remove
a certain percent of the total energy of the signal. We dened the
50% quartiles and 75% quartiles corresponding to the frequency
where the cumulative energy from the starting frequency (0Hz)
represents respectively 50% or 75% of the total signal energy.
Three kinds of experimental signals were created. In the rst case
(n = 15), the control bleat was high-pass-ltered at Quartile 50%,
(1,680 Hz ± 3%, Figure 1D); in the second case (n = 15), it was
low-pass-ltered Q50% (Figure 1B) and the other (n = 16) low-pass-
ltered Q75% (2,600 Hz ± 3.6%, Figure 1C). Route mean square
(RMS) values, representing the mean intensity of the entire call,
of both experimental signals were adjusted to those of the natural
● Experiment 2: do mothers rely on precise frequency values of the
We performed positive linear shifts (Charrier et al. 2003; Randal
& Tech 1987.). This was done by picking a data record through
a square window, applying short-term overlapping (50%) Fast
Fourier Transform (FFT), followed by a linear positive shift of each
spectrum, and by a short-term inverse Fast Fourier Transform
(FFT-1, Randal & Tech 1987). The window size was 4,096 points
(precision in frequency 7-8 Hz). The values were +50 (n=18), +100
(n = 17), +200 Hz (n = 17); see Figure 1E, F, G. For these modied
signals, the natural frequency and amplitude modulations of the
original bleats were unchanged.
● Experiment 3: is amplitude pattern an important cue?
We prepared experimental signals (n = 17 lambs tested) without
any amplitude modulation (quavering bleats) but with the natural
frequency modulation kept (Figure 1H). To build this signal, we
used the analytical signal concept, which allows demodulation
of amplitude using a Hilbert transformation (Seggie 1987; Mbu-
Nyamsi et al. 1994).
Criteria of response
Under natural conditions, when recognized, a call elicits various
responses from the receiver: interruption of ongoing activity,
vocalisations, orientation towards the source (head or head and body),
approach to the source (McGregor 1992; Searby & Jouventin 2003;
Ligout et al. 2004; Sèbe et al. 2007; Sèbe et al. 2008), and eventually
reunion of the two members of the dyad. Here, we took into account
these ve response categories during the playback and the minute
following the last played back bleat. The response of each subject was
quantied by allocating points each time the tested animal displayed
one of the above behaviours. When none of these behaviours were
recorded during the testing session, the subject obtained a score of
0 points. Thus, the score of an individual could range from 0 to 8
points (Table 1).
The results are presented as medians and lower and upper quartiles
[LQ-HQ]. Because of the discontinuous nature of the data and its
lack of normality, nonparametric statistical tests were used.
In each group, Wilcoxon tests were used to compare the
behavioural responses of subjects to own versus alien bleats and of
non-modied mother’s bleats versus modied mother’s bleats. Mann-
Whitney U tests were used for comparisons of responses between
groups, and particularly, to compare the behavioural responses
of subjects to modied mother’s bleats versus alien bleats. The
signicance level was set at p = 0.05, with bilateral probabilities.
Software used for statistical analysis was Statistica V.6.0 (StatSoft,
Behavioural responses to playback and score obtained by lambs (Sèbe et al., 2008).
Scores Behavioural response
Interruption of ongoing behaviour within 2s after the emission
from 0 to 4
Bleats emitted during the playback. Each time the subject vocalised
within 2.5 s after the playback of a played back bleat, he was given
Looking towards loudspeaker within 2s after the emission of a bleat
Approach toward the loudspeaker (> 1 m) during the playback
Reunion of mother and young during the playback
Study 1: Vocal discrimination by lambs during the rst two
During the tests, twelve-hour-old lambs did not spend signicantly
more time in the proximity zone near their hidden mother than they
did near the hidden alien ewe (Table 2). At 24 hr, lambs tended to
spend more time near their mother than near the alien ewe (Table 2)
and at 48 hr the difference was statistically signicant (Table 2).
Study 2: Playback experiments with modied calls
Control experiment: Lambs respond specically to their own mother’s
The playback of the own mother’s bleats at 30 min after suckling
elicited higher scores in lambs than the playback of the alien mother’s
bleats at the same time (Wilcoxon, n = 19, p = 0.0004; Table 3). This
experience shows that mother’s bleats elicit more responses than alien
bleats and conrms that lambs are able to discriminate the calls of
Experiment 1: a too truncated spectrum does not allow recognition
Low and high-pass-ltered Q50% signals elicited a lower response in
the majority of the tested lambs compared to their response to non-
modied bleats from their mothers (Low pass Q50% : p = 0.014; high-
pass : p = 0.0004; Table 3). In contrast, most lambs identied the
Time (s) spent by lambs near their own or an alien hidden ewe, (median, [LQ, HQ]),
in a 3 min two-choice test according to the age of the lamb (12, 24 or 48 hr).
N = numbers of individuals. Lambs had no access to visual or individual olfactory
cues from their mother. Table adapted from Sèbe et al. (2007).
Groups N Time spent near to p-level Time spent near
own ewe Z to alien ewe
12 hr 20 28 p = 0.54 29.5
[0-61] Z = 0.60 [10–43]
24 hr 19 48 p = 0.084 15
[13.5–87] Z = 1.73 [0–31.5]
48 hr 19 63
p = 0.006 4
[30–117.5] Z = 2.74 [0–26]
low-pass-ltered signals with the Q75% lter and their response to
this signal did not differ from that to the non modied signal.
Experiment 2: the precise frequency values of the harmonics are
important features for individual recognition
Most of the positive frequency-shifted signals did not trigger
recognition of the mother’s call by the lamb. Only the +50 Hz signals
elicited responses that did not differ signicantly from those elicited
by the control signal (Table 3).
Results of playback experiments to lambs. N = number of lambs tested, (ns p>0.5,
*p<0.05, **p<0.01, ***p<0.01, Wilcoxon test for comparisons with the positive control
and Mann-Whitney U tests for comparisons between experimental and alien signals).
Low-pass Q50%; Low-pass Q75%; High-pass Q50%: signals low-pass and high-pass-
ltered. Shift +50Hz; +100Hz; +200Hz: positive frequency-shifted signals. Without
AM: signal with no amplitude modulation.
Playback experiments N Ethological Comparison Comparison
score with the with the
control bleats alien's bleats
non-modied mother’s 19 4 [3–5] – –
Alien Mother’s bleat 19 1 [0–2] ***
Low-pass Q50% 15 1 [0–3] * ns
Low-pass Q75% 16 3.5 [3–4] ns ***
Shifts +50Hz 18 5 [4–5] ns ***
Shifts +100Hz 17 3 [2–4] * **
Shifts +200Hz 17 0 [0–1] *** ns
Without AM 17 0 [0–0] *** ns
Experiment 3: lambs rely on amplitude modulation pattern to
identify their mother
The absence of the amplitude pattern (quavering bleats) impairs the
recognition process: all lambs tested were unable to recognize their
mother’s calls with such modication (Table 3).
Early vocal discrimination
In a double-choice test situation, lambs displayed a preference for
the bleats of their own mother 48 hr after birth. This indicates that
lambs are able to discriminate their mother on the basis of acoustic
cues (high-pitched bleats in the present study) earlier than what had
previously been reported in the literature of vocal recognition (Shillito
& Alexander 1975; Alexander 1977; Searby & Jouventin 2003). There
is no doubt that the discrimination reported here depends only on
acoustic cues. Indeed, the lambs displayed a preference for the bleats
of their own mother hidden behind a canvas screen at a distance of 1
m, excluding thus the involvement of visual and olfactory cues, these
latter cues being not perceived at more than 0.25 cm (Alexander 1978;
Alexander & Shillito 1978; Ferreira et al. 2000). Considering that ewes
are also able to recognize their lamb by hearing at 24 hr postpartum
(Sèbe et al. 2007), this highlights that acoustic communication plays
an important role in mother-young recognition in sheep at a very
For lambs, the failure to express a preference between the own
mother and an alien one at 12 hr does not necessarily mean that
they are unable to discriminate their mother at an earlier age. In
fact, in the present study, lambs displayed discrimination later than
reported in the literature of multimodal recognition (Nowak et al.
1987; Nowak 1990; Val-Laillet et al. 2004), but in these studies visual
cues were available at 12 to 24 hr postpartum. This indicates that
visual cues also play an important facilitating role in early mother-
young recognition (Terrazas et al. 2002).As already suggested by Sèbe
et al. (2007), the ability of ewes and lambs to rapidly establish vocal
discrimination of their kin and a preference for them, is consistent
with the vocal behaviour that animals of this species display at the
time of parturition. Both the ewes and the lambs showed an intense
peak of vocal activity just after the birth of the lamb, thus providing
a propitious context for the establishment of vocal recognition.
A multiparametric decoding process
Our hypothesis that the acoustic encoding of maternal individuality
involves other acoustic parameters than solely the mean fundamental
frequency was supported by the results of the present study. We
established that the recognition process appears to be multiparametric,
relying on several cues in the frequency and temporal domains.
Concerning the acoustic parameters involved in the encoding
of maternal identity, our playback experiments have shown that the
mother’s call presents individual characteristics in the frequency
domain and also that the whole frequency spectrum was not required
for the identication of the emitter. Nevertheless, playback of less
than 50% of the energy spectrum, both at low or high frequencies,
was insufcient to trigger recognition of the mother call by the lamb.
Moreover, the use of the frequency shifted signals showed that lambs
take into account the precise frequency values of the harmonics. In
the temporal domain, amplitude modulations or quavering bleats
are essential for recognition. Thus, our results have demonstrated
that the encoding of the individual signature is not limited to the
frequency domain as suggested by Searby and Jouventin (2003), but
is rather based on a multiparametric encoding process. In a crowd,
the environment is noisy and mother and young can be separated
by a relative great distance. In such a context, a multiparametric
encoding process can more efciently convey information for individual
recognition (Aubin & Jouventin 1998; Aubin & Jouventin 2002).
To conclude, it appears that vocal recognition of the ewe by her
lamb plays an important role for the maintenance of mother-young
contact very soon after parturition. It is interesting to point out that
our results are quite similar to those reported in another gregarious
mammal living in similar conditions (many young, synchronize and
seasonal breeders, maternal selectivity), the fur seal Arctocephalus
tropicalis: in this species, recognition of the mother’s call by the pup
is effective from the age of 2 days, and involves also a multiparametric
encoding process (Charrier et al. 2001; Charrier et al. 2003). This
mutual vocal recognition process in mammals which live in large
and/or moving groups, may be of primary importance when the dyad
(sheep) or one of its members (seals) starts to move from the birth
site, especially given the very short range at which olfactory and visual
discriminations are possible. These observations of early discrimination
and multiparametric encoding in mother-lamb recognition supports
the hypothesis of convergent systems of recognition related to the
social, biological breeding and environmental context. This pattern
seems to occur independently of domestication or of phylogeny.
The authors are grateful to D. Lindsay, F. Lévy, A. Boissy, M.
Hausberger and F. Rybak for suggestions, participation and technical
support; to F. Dupont, E. Archer and the shepherds from the
experimental farm of the INRA of Nouzilly, for the care of the animals.
This work was supported by a Ph.D. scholarship from I.N.R.A. and
GDR 2822 d’Éthologie.
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