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First published online October 31, 2008
Journal of Experimental Biology 211, 3554-3562 (2008)
Published by The Company of Biologists 2008
doi: 10.1242/jeb.016055
Mother–young vocal communication and acoustic recognition promote preferential nursing in sheep
1 Equipe Comportement, Neurobiologie Adaptation, Unite de Physiologie de la
Reproduction et des Comportements UMR 6175 CNRS INRA Universite de Tours Haras
Nationaux, 37380 Nouzilly, France
2 Equipe Communications Acoustiques, NAMC CNRS UMR 8620, Université
Paris-Sud, Bât. 446, 91405 Orsay Cedex, France
* Author for correspondence (e-mail: sebefrederic{at}gmail.com)
Accepted 4 September 2008
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Summary |
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 TOP Summary INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Key words: mother–young interactions, motivation, suckling, bleats, maternal behaviour, selectivity, playback, ewe, lamb
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INTRODUCTION |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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;
Clutton-Brock, 1991). This is
particularly true in gregarious species in which reproduction is highly
synchronised and many young are born within a limited time of the year; if the
mother provides milk to non-kin young she may reduce her investment in her own
offspring (González-Mariscal and
Poindron, 2002; Poindron et
al., 2007). In such situations, mother–young recognition at
the time of suckling is critical to maximise maternal investment. Sheep
constitute a good example of mammals living in large groups with synchronised
seasonal breeding, in which mutual mother–young recognition ensures
exclusive care of their own progeny (Lynch
et al., 1992; Poindron et al.,
2007).
In this species, olfaction has long been recognized as the critical sensory
modality controlling exclusive acceptance of the mother's own lamb at nursing
(Bouissou, 1968;
Alexander, 1978;
Kendrick et al., 1997;
Lévy and Fleming,
2006). The process of parturition facilitates ewes' rapid
familiarisation with the individual smell of their neonates
(Kendrick et al., 1997;
Lévy et al., 2004),
which in turn ensures selective access to the udder as early as 2 h postpartum
in the large majority of mothers (Poindron
et al., 1980; Keller et al.,
2003). Nonetheless, despite the critical role of maternal
olfactory recognition and selective nursing of the newborn lamb in early
maternal investment, several other factors in the mother, but also in the
lamb, may contribute further to preferential maternal investment. First,
maternal olfactory recognition is functional only at a very short distance
(<0.25 m) (Alexander and Shillito,
1977a; Alexander,
1978) and discrimination of young at greater distances necessarily
involves visual and/or acoustic modalities. Second, recognition of the mother
by her lamb is also important for its survival and hence for maternal
reproductive success (Nowak and Lindsay,
1992), and this depends on visual and acoustic cues
(Nowak, 1991;
Terrazas et al., 2002).
Therefore, visual and acoustic distance recognition by both ewes and lambs are
likely to facilitate preferential suckling and maternal investment.
While it is well established that ewes and lambs recognise each other
through both visual and acoustic cues
(Lindsay and Fletcher, 1968;
Poindron and Carrick, 1976;
Alexander and Shillito, 1977a;
Alexander and Shillito, 1977b;
Alexander and Shillito-Walser,
1978; Terrazas et al.,
1999), vocal recognition is likely to play a primary role at a
distance, since it can take place at much greater distances than allowed by
visual recognition (Hinch et al.,
1987) or when mother and young cannot see each other
(Shillito, 1975;
Poindron and Carrick, 1976;
Shillito-Walser et al., 1981).
Also, vocal communication is an important component regulating early
mother–young interactions (Vince,
1993), when both the mother and her neonate show an intense peak
of vocal activity in the first 3 h following the birth of the lamb
(Sèbe et al., 2007).
Furthermore, ewes and lambs display a preference for each other based solely
upon vocal cues soon after parturition (at 24 h in ewes and 48 h in lambs)
(Sèbe et al., 2007) and
recognise the individual acoustic signature of their kin soon afterwards
(Searby and Jouventin,
2003).
Taken together, these results suggest that mutual vocal recognition plays a
significant role in the development of preferential nursing by ewes of their
own lambs and that this may occur quite rapidly after parturition. Moreover,
early suckling activity is critical for the lamb to develop a preference for
its mother, which also depends on mother–young vocal communication and
recognition (Nowak, 1990;
Nowak, 1991;
Terrazas et al., 2002;
Sèbe et al., 2007).
Therefore, our hypothesis was that vocal communication and the display of
acoustic recognition by ewes and their lambs would be closely associated with
nursing. To investigate this possibility we carried out two separate studies
to analyse the establishment of acoustic communication between the ewe and her
lamb and the conditions under which mutual ewe–lamb vocal recognition
occurs during the first 2 weeks after birth.
In the first study, we tested the hypothesis that if vocal communication plays a role in preferential suckling, some pattern of association between these two components of the mother–young relationship should emerge within a few days of parturition. To this end, we recorded and analysed spontaneous nursing behaviour and vocal activity of mother–young dyads during the first 2 weeks of lactation, to see whether vocal behaviour in ewes and lambs would peak just before nursing.
In the second study, we investigated further the role of acoustic
recognition at the time of nursing, by testing the response of ewes and lambs
to the playback of bleats of their own or an alien partner. This was performed
at 2 weeks postpartum, as the results of the first study indicated that at
this time we could reliably assume vocal communication to be established. In
addition, we took into account the time at which the tests were carried out
relative to the last nursing bout, because the context in which a sensory
signal is emitted, such as the motivational state of the receiver, can
influence the display of the receiver's behavioural response
(Snowdon and Hausberger, 1997;
McGregor, 2005a;
Engh et al., 2006). The role
of the motivational context of the receiver in the display of
mother–young vocal recognition has not been documented in sheep.
Therefore, we tested the response of ewes and lambs to the playback of bleats
either 5 or 30 min after a nursing episode. We considered that these two
intervals represented a sufficient difference in motivation to suckle because
in the first study we found that most nursing occurred at intervals ranging
from 30 to 60 min at 2 weeks postpartum. The second study also clarified the
causal relationships between vocal behaviour and nursing.
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MATERIALS AND METHODS |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Behavioural observations
Ewes and lambs emit basically two categories of bleats
(Dwyer et al., 1998;
Hersher et al., 1963;
Lévy et al., 1996;
Sèbe et al., 2007),
easily distinguishable by the human ear and by the opening of the mouth: (1)
low-pitched bleats (quiet vocalisations emitted with the mouth closed); and
(2) high-pitched bleats (loud calls emitted with the mouth open). These two
types of vocalisation were both taken into account in the present study. The
time and number of vocalisations of the 14 ewes and their 16 lambs were
directly recorded by an observer during six observation sessions, each lasting
3 h, from the time of lambing until day 15 postpartum (see
Fig. 1 for details). All
animals were observed at 0–3, 3–6, 12–15 and 24–27 h
postpartum. However, due to some overlapping with the last parturitions, only
11 ewes were observed at 6 and 15 days. For all sessions, the vocal activity
was recorded by focal observations of each mother–young unit separately
on video. Therefore, during each session of observation, the behaviour of ewes
and their lambs was video recorded and thereafter analysed in the laboratory,
using Observer Video-Pro XT software
(Noldus et al., 2000). In all
sessions and for all subjects, nursing episodes were identified (at least 1
min of sucking by the lamb in one suckling bout or several bouts separated by
a maximum interval of 5 s). No other such episodes occurred within a period
ranging from 25 min prior to a target suckling bout until 10 min after it
ended. In this paper, we use the terms nursing and suckling to refer to the
feeding of the lamb by the dam according to the definitions of Hall and
colleagues (Hall et al.,
1988). During these 35 min, vocalisations of the ewe and her lamb
were quantified in windows of 2.5 min of focal sampling, each separated by 2.5
min intervals (Fig. 1), in
order to obtain an accurate estimation of vocalisation timing in relation to
the feeding of the lamb. The vocal behaviour of each animal was then analysed
over the 35 min period. In addition, the global vocal activity of the
mother–young dyad during this time was assessed by summing the vocal
activity of the ewe and her lamb.
Statistical analyses
The results are presented as medians and lower and upper quartiles. Because
of the lack of normality of the data and small sample size, non-parametric
statistical tests were used (Siegel and
Castellan, 1988). Since the vocal behaviour of singles and twins,
or of their mothers, did not differ, they were combined to form a single group
of lambs.
Within each 35 min period, the vocal activity in the various 2.5 min windows was compared by the Friedman test, followed by the Wilcoxon signed-ranks test for pairwise comparisons, with Bonferroni correction for multiple comparisons. In addition, separate comparisons were carried out, on the one hand between the five 2.5 min windows of the 25 min before nursing, and on the other hand between the 2.5 min window just before nursing and the two 2.5 min windows after nursing. Comparisons between the various times of the study were carried out by a Friedman test, taking the percentage of bleats emitted in the last 2.5 min before nursing relative to the total number of bleats emitted in the 25 min before nursing. The significance level was set at P=0.05, with bilateral probabilities. Statistica V.6.0 software (2002; StatSoft, Tulsa, OK, USA) was used for the statistical analyses.
Study 2: experimental responses of ewes and their lambs at 15 days postpartum to the playback of bleats relative to suckling
Animals and management conditions
Animals were drawn from a total flock of 80 Ile-de-France ewes and their
110 lambs maintained in the grounds of INRA Research Centre of Nouzilly,
France. Ovulations had been synchronised so that all experimental ewes gave
birth within a period of 1 week each year. Subjects were tested at 15 days
postpartum over a period of 2 years. Ewes were kept permanently indoors in
pens at a density of 30 animals per 100 m2. They were fed
dehydrated lucerne, maize, straw and vitamin and mineral supplement, and had
free access to water. Recording of bleats and playback experiments were
performed 2 weeks after lambing.
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Only high-pitched bleats (i.e. loud calls emitted with the mouth open; see
Fig. 2) were recorded
(Dwyer et al., 1997;
Dwyer et al., 1998), as this
is the main type of vocalisation emitted by ewes and lambs at this stage of
the mother–young relationship
(Sèbe et al., 2007).
Sound files were then transferred to a computer for subsequent broadcast.
Playback procedure
Ewe calls were played back to 37 lambs and lamb calls to 31 ewes in their
living pen in the barn. Mothers and offspring were not separated from each
other or from the other ewes and lambs of the same group. Animals were studied
focally (i.e. one dyad at a time). Tests were performed after 16:00 h, when
the daily routine maintenance of the animals had ceased.
Three different bleats, from the same animal, separated by 2.5 s of silence
were played back. Selected recordings were free of bleats from other animals
and had a signal (dB) to noise (dB) ratio higher than 25 in all cases. The
recordings were played at a volume and tone similar to that of the natural
voices of lambs as controlled by a sound level meter. A computer connected to
a unidirectional loudspeaker (TANNOY coaxial 80 W/6 
Tannoy Ltd,
Coatbridge, UK) was used for the playback. The loudspeaker was placed 1 m
outside a corner of the animals' pen and playback was carried out when
subjects were 3–6 m from the loudspeaker. In addition, the following
conditions had to be met for the test to occur. (1) Subjects involved in the
test (kin or non-kin) had to be visually separated and at least 2 m away from
each other. (2) The subject to be tested must not have been eating or lying
with eyes closed. (3) The exact time of the last nursing (>5 s) had to be
known, since it was one of the experimental parameters studied.
Each tested individual was subjected to two playback sessions: bleats of
the kin mother or young (hereafter referred to as `kin bleats') and bleats of
another unrelated ewe or lamb from the same living pen (hereafter referred to
as `non-kin bleats'). To avoid habituation
(McGregor, 1992), each lamb
was never tested more than twice, with a minimum of 1 h between the two
playback sessions. Half of the animals were tested with kin bleats first and
the other half with non-kin bleats first. The non-kin bleats used in the test
came from animals from the same group. Hence, bleats from non-kin mothers came
from ewes that were at the same stage of lactation as the mother of the lamb
to be tested, and bleats from non-kin lambs came from lambs of the same age as
the lamb of the ewe to be tested. For each tested subject, the two playback
sequences were carried out on the same day and they were separated by at least
1 h and one suckling. To test the effect of the interval between suckling and
playback of the vocalisations on the response by the tested subject, we
performed the playback either 5 or 30 min after suckling. The intervals of 5
and 30 min were chosen because in study 1 we had found that ewes nurse their
lambs generally between one and two times per hour at 2 weeks of lactation,
which is also consistent with the literature
(Ewbank, 1964;
Fletcher, 1971;
Schirar et al., 1989). We
therefore inferred that comparing the responses of ewes and lambs to acoustic
playback 5 or 30 min after a suckling episode would offer a substantial
difference regarding the motivation to nurse (mother) and suck (lamb). Each
lamb and ewe was then allocated at random to one of four experimental groups
and observed under the following stimulus conditions. Group 1: behavioural
responses of mothers to bleats of lambs 30 min after nursing (N=16);
group 2: behavioural responses of mothers to bleats of lambs 5 min after
nursing (N=15); group 3: behavioural responses of lambs to bleats of
ewes 30 min after sucking (N=19); and group 4: behavioural responses
of lambs to bleats of ewes 5 min after sucking (N=18).
All groups were independent of each other, while the condition for the type of bleat (kin or non-kin) was tested with the same subjects.
Criteria of response
Under natural conditions, when recognised, a call can elicit various
responses from the receiver: interruption of ongoing activity, vocalisations,
orientation towards the source (head or head and body), approaching the source
(McGregor, 1992;
Charrier et al., 2002a;
Searby and Jouventin, 2003;
Ligout et al., 2004;
Sèbe et al., 2007) and
eventually reunion of the two members of the dyad, as subjects were in the
same pen at the time of testing. We took into account these five response
categories during the playback and the minute following the last played-back
bleat. The responses of each subject were quantified by allocating points each
time the tested animal displayed one of the following behaviours. (i)
Interruption of behaviour within 2 s after the emission of a bleat: 1 point.
(ii) Looking towards loudspeaker within 2 s after the emission of a bleat: 1
point. `Looking' was defined as the rear-front axis of the head of the animal
being oriented directly towards the loudspeaker. (iii) Approaching the
loudspeaker (>1 m) during the playback or the following minute of
observation: 1 point. (iv) Bleats emitted during the playback or the following
minute of observation. The number of allocated points for this variable ranged
from 0 to 4. Each time the subject vocalised within 2.5 s after the playback
of one bleat, it was given 1 point. Thus, an animal could obtain a total of 3
points for immediate `response' to the playback of the three bleats. In
addition, if the subject emitted more bleats during the rest of the test (1
min after playback of the third bleat), he was given one additional point. A
major weight was given to this variable because, in other studies
(Shillito-Walser et al., 1981;
Searby and Jouventin, 2003),
the bleating rate has been shown to be positively correlated with recognition.
(v) Reunion of mother and young during the playback or the following minute of
observation, ending with sucking: 1 point. 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.
Statistical analyses
The results are presented as medians and lower and upper quartiles. Because
of the discontinuous nature of the data and their lack of normality,
non-parametric statistical tests were used.
In each group, Wilcoxon tests were used to compare the behavioural responses of subjects to kin versus non-kin bleats. Mann–Whitney U-tests were used for comparisons of responses between groups.
In all cases, the significance level was set at P=0.05, with bilateral probabilities.
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RESULTS |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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During the period 3–6 h after parturition, the number of bleats differed significantly between the various windows of sampling (Friedman: N=14, d.f.=6, P<0.001; Fig. 3). The vocal activity was significantly higher just before nursing than 25 and 20 min before nursing (Wilcoxon: N=14, P<0.05), while no difference was found between the period just before nursing and the two periods after (Friedman: N=14, d.f.=2, P=0.8). Similar results were found at 12 h and 24 h postpartum (Friedman tests, total: N=14, d.f.=6, P<0.001; before nursing: N=14, d.f.=4, P<0.001; after nursing: N=14, d.f.=6, P>0.076; Fig. 3).
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In contrast, at all other observation times (3–6 h, 12 h, 24 h, day 6 and day 15) the number of bleats differed significantly between all the various 2.5 min windows of each 35 min period (Friedman: N=14, d.f.=6, P<0.001). The vocal activity was highest just before nursing in all cases (Friedman: N=14, d.f.=4, P<0.01), but this activity just before nursing did not differ from that in the two windows after nursing at 3–6 h, 12 h and 24 h (Friedman: N=14, d.f.=2, P>0.18). Nonetheless, at day 6 and day 15 the number of bleats by the mother after nursing decreased significantly relative to the last 2.5 min before nursing (Friedman test, total: N=14, d.f.=2, P<0.05).
Relationship between the vocal activity of lambs and nursing
As for the mothers, between birth and 3 h after birth, the vocal activity
of newborn lambs did not differ between the various 2.5 min windows of the 35
min period around nursing (Friedman: N=14, d.f.=6,
P=0.24).
At 3–6 h, 12 h, day 6 and day 15 after parturition, the number of bleats differed significantly between the various 2.5 min windows of each 35 min period (Friedman: N=14 or 11, d.f.=6, P<0.01), whereas this was not the case at 24 h (Friedman: N=14, d.f.=6, P=0.37). At 3–6 h, 12 h, day 6 and day 15 after parturition the vocal activity increased significantly before nursing (Friedman: N=14 or 11, d.f.=4, P<0.05) and decreased significantly after nursing (Friedman test: N=14 or 11, d.f.=2, P<0.05).
Study 2: experimental responses of ewes and their lambs at 15 days postpartum to the playback of bleats relative to suckling
Behaviour of ewes following the playback of lambs' bleats (groups 1 and 2)
When playback was performed 30 min after suckling, kin lamb bleats elicited
significantly higher scores than non-kin lamb bleats (Wilcoxon test:
N=16, P<0.001; Fig.
5A) and in the former case, playback was followed by
mother–young reunion in 37% of tests with kin bleats, usually ending
with sucking, versus 0% with non-kin bleats (Fisher's exact test,
P=0.009). In contrast, when playback of the bleats of the kin lamb
was carried out 5 min after suckling, it did not result in higher scores than
the playback of bleats of a non-kin lamb (Wilcoxon test, N=16,
P=0.29; Fig. 5A). The
mothers' scores resulting from the playback of non-kin lamb bleats 30 min
after suckling did not differ from those obtained 5 min after suckling
(Mann–Whitney: P=0.76). In addition, mother–young reunion
was never observed with non-kin bleats.
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Behaviour of lambs following the playback of kin or non-kin mothers' bleats (groups 3 and 4)
The playback of the kin mother's bleats at both 30 and 5 min after suckling
elicited higher scores in lambs than the playback of bleats from non-kin
mothers at the same times (Wilcoxon: N=19 or 18, P<0.005;
Fig. 5B). In addition,
playbacks of kin mother's bleats 30 min after suckling resulted in
significantly higher scores than playback of kin mother's bleats 5 min after
suckling (Mann–Whitney: P<0.001). However, the proportion of
mother–young reunions following playback of the kin mother's bleats 30
min after nursing (20%) did not differ significantly from that following
playback 5 min after nursing (38%). Finally, following the playback of bleats
from a non-kin mother, the scores of the lambs were significantly higher 30
min after suckling than 5 min after suckling (Mann–Whitney:
P<0.005; Fig. 5B)
although we never observed mother–young reunion in this experimental
situation. Also, the proportion of mother–young reunions following
playback of bleats of the kin mother differed from that following playback of
bleats of non-kin mothers (30 min after nursing: 20% versus 0%,
Fisher's exact test, P=0.052; 5 min after nursing: 38%
versus 0%, Fisher's exact test, P=0.004).
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DISCUSSION |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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;
Poindron, 1976;
Poindron et al., 1980). While
it is well established that vocalisations represent an important element of
mother–young interactions (Nowak,
1990; Vince, 1993;
Dwyer et al., 1998), this is
the first experimental evidence demonstrating its biological significance for
preferential maternal investment.
Early postpartum association of mother–young vocal communication with nursing
The development of a preference for the mother is entirely dependent on
suckling in sheep (Nowak et al.,
1997). The association of vocal activity by the mother and her
lamb with nursing, which was marked at 2 weeks of lactation, develops very
soon after parturition. Evidence for nursing-dependent structuring of vocal
behaviour in ewes and lambs was present at 3–6 h after parturition,
indicating that acoustic communication has already started to develop at that
time. This is likely to be the result of a number of converging factors. Both
ewes and lambs display intense vocal activity that peaks during the first 3 h
following parturition (Poindron et al.,
1980; Shillito-Walser et al.,
1984; Dwyer et al.,
1998; Sèbe et al.,
2007) thus providing a propitious context for the establishment of
vocal communication and hearing recognition. Since the lamb starts to suck
within the first hour after birth, it is likely that nursing begins to play a
reinforcing role in vocal activity very early on, thus providing a basis for
the two members of the dyad to learn each other's vocal identity. In the lamb,
this is likely to depend on the well-established reinforcing influence of
colostrum intake on the development of a preference for the mother
(Nowak et al., 1997;
Val-Laillet et al., 2004;
Nowak and Poindron, 2006). The
reinforcement of vocal activity by nursing is also consistent with the shaping
of neonatal behaviour by stimuli associated with sucking, which can have a
calming effect and facilitate learning, as reported in a wide range of
species, including rats, rabbits, dogs, sheep and humans
(Nowak, 2006). Also, it must
be kept in mind that the bleating activity of the mother in the early
postpartum period has a very high frequency of occurrence, more than 10 times
higher than that of the lamb (Sèbe
et al., 2007). Consequently it is likely to play a driving and
determinant role in the association between nursing and vocal communication
between the mother and her young. Hence, nursing may facilitate lambs'
learning of the vocal signature of the mother, as has been shown for olfactory
or acoustic cues in human babies (Alegria
and Noirot, 1978; Noirot and
Alegria, 1983; Nowak,
2006). This is the first evidence that an early postpartum
relationship exists between mother–young vocal communication and both
recognition and nursing. Thus, the results suggest that nursing and the natal
context may play an important role in vocal learning between lambs and their
mothers.
Interestingly, a pattern of association between vocal activity and nursing
was also present within 6 h postpartum in ewes and their lambs. This implies
that in the ewe the initial activation of vocal behaviour by intrinsic factors
associated with parturition (Dwyer et al.,
1998; Sèbe et al.,
2007) gives precedence to factors provided by the lamb and by
nursing itself. Therefore, nursing appears to be reinforcing not only in the
neonate but also in the mother. This is supported further by the results of
study 2, showing that mothers responded to the playback of their lamb's bleats
30 min after nursing but not just after, when their motivation to nurse was
likely to be low. Together with the early increase of vocalisations by the
lamb observed before nursing, the rewarding effect of nursing appears to
rapidly promote the reinforcement of vocal communication between the mother
and her neonate and the establishment of mutual acoustic recognition and
preferences.
The association of an increased peak of vocal activity with the imminence
of nursing is not limited to the initial postpartum hours: our results suggest
that the first coupling of vocal activity with nursing during the 6 h
immediately postpartum is followed by a second increase of this coupling
between 6 and 15 days postpartum, as illustrated in
Fig. 4. This dynamic probably
reflects the establishment of nursing behaviour within the context of the
mother–young vocal relationship or/and the change in the
mother–young spatial relationship, which increases with the age of the
lambs and their motor activity. Within a few days after birth, lambs tend to
form play groups, thus reducing the contact with their dam
(Lynch et al., 1992). In
addition, an important change in maternal behaviour takes place by the end of
the first week postpartum. During the first week postpartum, lambs are allowed
to suck whenever and for as long as they want, generally staying close to
their dams (Ewbank, 1964;
Hess et al., 1974;
Graves et al., 1977;
Lynch et al., 1992). Then, at
about 7 days of lactation, mothers begin to control the duration of nursing
bouts, and this becomes the rule within a few days
(Gordon and Siegmann, 1991).
It is therefore likely that this increasing limitation of access to the udder
imposed by the dam, combined with increasing mother–young distance and
independent activity of the lamb (Lynch et
al., 1992), reinforces the advantage of and need for vocal
communication to promote nursing.
Importance of nursing for the display of mother–young vocal recognition in ewes and lambs
The results of study 2 provide important information regarding the factors
controlling mother–young vocal communication. The difference in the
responses to each other's played-back bleats by the mother and the lamb before
and after suckling indicates that vocal communication depends strongly on the
motivational state of the receiver, as suggested by the results of study 1 on
spontaneous communication and nursing. Both mothers and young responded better
to playback performed 30 min after nursing than when it was performed just
after nursing. In fact, mothers totally failed to respond to the bleats of
their lambs just after a nursing episode, indicating that the motivation to
nurse must be a primary determinant of vocal communication in mothers under
undisturbed conditions. This is also partly true for lambs, as they responded
significantly more to playback 30 min after suckling than 5 min later.
Nonetheless, their response 5 min after suckling was still higher than that
for playback of non-kin mother's bleats. This may suggest that the lambs are
not fully satiated after a nursing episode and/or that it is easier for lambs
to find their way back to their mothers only 5 min after having been in
contact with them. This is especially likely in the case of twins, when
maternal milk production may not be sufficient to meet the needs of two lambs
(Treacher, 1983;
Hinch, 1989). Another
non-exclusive explanation for the persistence of some response of lambs
immediately after nursing is that the oral stimulation provided by sucking is
rewarding independently of the intake of milk
(Nowak, 2006). It contributes
to the psychobiological attachment of the lamb to its mother, and this may be
another strong motivation for the lamb to reunite with its mother,
independently of its prandial state. The level of satiety also appears to
modulate the response to non-kin bleats, as at 30 min the response of lambs to
non-kin mother bleats was higher than at 5 min. While this response remained
lower than that to kin bleats, it underlines the major role played by context
and the fact that the response depends not only on recognition of the signal
but also on motivational state.
The results of study 2 also demonstrate that one important function of
vocal communication is to allow inter-individual recognition before nursing.
Mothers and lambs responded very specifically to the bleats of their kin, thus
reducing the probability of nursing between non-kin subjects before olfactory
identification of the lamb had taken place. In other words, preferential
maternal investment at nursing is already conditioned by vocal communication
and mutual acoustic recognition before the animals come in contact. Although
the actual rejection of an alien lamb at the udder depends on olfactory
inspection by the ewe when the animals are in physical contact
(Lévy et al., 2004),
the present results indicate that acoustic recognition does play an active
role in promoting preferential nursing between ewes and their own lambs in
spontaneously occurring mother–young interactions, at least at the age
of 2 weeks. Further studies are warranted to investigate the exact time at
which acoustic recognition starts to play such a role. Nonetheless, the
emergence of some association between vocal activity and nursing as early as 6
h postpartum (study 1), together with the early acoustic recognition existing
between ewes and their lambs (Dwyer et
al., 1998; Searby and
Jouventin, 2003; Sèbe
et al., 2007), suggests that it is probably already functional
long before 2 weeks postpartum. This function of acoustic recognition for
preferential maternal investment is likely to be even more important when
animals are at pasture, where inter-individual distances between animals are
much greater than in the present study. This probably also applies to other
domestic and wild species in which mother–young acoustic recognition has
been documented [e.g. goats (Ruiz-Miranda
et al., 1993; Terrazas et al.,
2003); reindeer (Espmark,
1971); red deer (Vankova and
Malek, 1997; Torriani et al.,
2006); fur seals (Charrier et
al., 2001; Charrier et al.,
2002a); wolves (Goldman et
al., 1995); and bats (Balcombe,
1990; Balcombe and McCracken,
1992)].
Conclusion
Mother–young vocal communication and recognition in sheep is well
structured and biologically significant at the time of nursing, ensuring
effective maternal care that is selectively directed towards the mother's own
young, a function that had not been considered previously for this sensory
modality in sheep. Like olfactory cues in sheep and other species
(Poindron et al., 1980;
Montigny et al., 2006;
Nowak and Poindron, 2006),
bleats serve as an organising signal anticipatory of feeding rhythm. The
present study demonstrates the importance of nursing and of motivational
context in the display of vocal mother–young communication and
recognition in sheep. These results suggest that mother–young vocal
communication and nursing are associated, and that this association may
facilitate the development of mutual vocal recognition. In addition, these
results highlight the major role played by context learning in the development
of filial and maternal bonding. The behavioural response of the recipient
depends not only on the signal itself but also on a rapid periodic change of
motivational context in both the transmitter and the recipient. This is
somewhat similar to results reported in other species, such as the seal,
although it occurs over a much longer period in seals. Thus, the
responsiveness of fur seal pups to maternal calls during the mother's absence
varies according to their motivational state, which is itself related to
internal nutritional balance (Charrier et
al., 2001; Charrier et al.,
2002b). More generally, this is congruent with the social
modelling theory that suggests that input must be referentially and
contextually applicable to elicit a socially appropriate response
(Bandura, 1977;
McGregor, 2005b). The
motivational context associated with nursing appears fundamental to a full
understanding of the communication network at play in mother–young
relationships.
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Acknowledgments |
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References |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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