Pascal Poindron

Learning of olfactory cues is not necessary for early lamb recognition by the mother

Ewes identify their young through the use of different sensory modalities. Olfactory recognition, which mediates selective acceptance at the udder, is established at 4 h postpartum (pp). Visual and auditory cues are involved in recognition at a distance, which is evident at 12 h pp. This study investigates whether anosmic ewes are able (a) to develop visual and auditory recognition and (b) to restore selective acceptance of their lamb at the udder. Visual and auditory recognition was assessed in anosmic and intact ewes at 12 h and 24 h pp by a test of two choices: their own and an alien lamb. Selectivity at allowing suckling was tested by presenting successively an alien and the familiar lamb at 4 h, 3 days, and 1 month pp. In the two-choice recognition test, at both 12 h and 24 h pp, anosmic as well as intact ewes showed a preference for their familiar lamb. Although anosmic ewes showed no difference in their acceptance of alien and familiar lambs for suckling at 4 h and 3 days pp, they nursed the alien lamb less at 1 month pp and showed more rejection behaviors toward it. Thus, visual, auditory, or both those types of recognition can be rapidly established, independent of olfactory recognition. Moreover, differential behavior of anosmic ewes toward their own versus an alien lamb at the udder at 1 month suggests that vision and audition may compensate to some extent for the loss of olfaction.

Do ewes recognize their lambs within the first day postpartum without the help of olfactory cues

Two studies were carried out to test the ability of Préalpes du Sud x Lacaune (Study 1) and Rambouillet ewes (Study 2) to recognize their lambs during the first 24 h postpartum. Ewes were given the choice between their own and an alien lamb of approximately the same age, in a triangular pen of 10 m×10 m×10 m. A lamb was placed in each of the two corners while the mother was released from the third corner. Direct access to the lambs was prevented by an open barrier located at 1 m from the pens in which the lambs were kept. Ewes were studied at 8 h (n=10, 12), 12 h (n=20, 10) and 24 h postpartum (n=29, 9; Study 1 and Study 2 respectively). Tests lasted 3 and 5 min in Study 1 and 2, respectively. Although the first choice of the ewes did not differ from random, in both studies mothers spent significantly more time near their own lamb than near the alien. In both breeds a significant preference for the own lamb was already present at 8 h (P<0.05). We conclude that ewes are very likely to recognize their lamb without the aid of olfactory cues as early as 8 h postpartum, which is much sooner than thought from previous studies.

Estradiol receptor-α expression in hypothalamic and limbic regions of ewes is influenced by physiological state and maternal experience

The influence of estrus, pregnancy, parturition, and maternal experience on the expression of estrogen receptor-alpha (ERalpha) was investigated in hypothalamic and limbic regions of the sheep brain, using immunocytochemistry. Four days before parturition, previous maternal experience was associated with a higher density of ERalpha-labeled neurons in the paraventricular and supraoptic nuclei, the medial preoptic area, and the medial amygdala, but not in the mediobasal hypothalamus. Furthermore, an interaction was found between physiological state and experience in the peripartum period as the effect of experience existing 4 days prepartum was not found at parturition, when densities were lowest both in primiparous and in multiparous ewes. An additional effect of physiological state was also observed between parturition and estrus, densities being significantly lower at parturition than at estrus in the SON, PVN, and MPOA, but not in the medial amygdala. These results indicate that in sheep ERalpha expression is influenced by previous physiological and/or maternal experience at specific times of the reproductive cycle. They are also congruent with the higher ability of multiparous than nulliparous ewes to show maternal behavior several days prepartum.

Maternal Olfaction Differentially Modulates Oxytocin and Prolactin Release during Suckling in Goats

In postparturient goats, olfactory recognition of the young allows the establishment of a selective bond between the mother and her kids. Once this bond is formed, the mother rejects alien young that attempt to suckle. We tested whether the development of the maternal selective bond in goats modulates prolactin (PRL) and oxytocin (OT) release in response to suckling. On day 37 of lactation, serial blood samples were taken during nursing of the mothers own or alien kid(s) in 10 intact/selective goats and in 10 goats rendered anosmic/nonselective through prepartum peripheral ZnSO(4) irrigation. Spontaneous nursing behavior was also studied weekly from day 7 to 30 of lactation, at which time milk production was measured. Maternal selectivity had no effect on PRL release, in contrast to OT release, which was significantly affected by this factor. Intact mothers released OT only when nursing their own kids, but not with aliens, while anosmic/nonselective dams showed an increase in OT levels regardless of the identity of the kids. In addition to these effects on maternal selectivity, the amplitude of the response of both hormones was lower in anosmic mothers than in intact mothers. Finally, nursing behavior and milk production were not significantly affected by anosmia. We conclude that maternal selective behavior in goats, which relies on the individual olfactory signature of the kid, modulates the OT, but not the PRL, response to suckling. In addition, perception of the smell of the young appears to have a general facilitatory effect, independent of the kids identity, on the release of both hormones.

Maternal selectivity suppression through peripheral anosmia affects neither overall nursing frequency and duration, nor lactation performance in ewes

The effects of prepartum peripheral anosmia on nursing activity, milk production and growth of the lambs, were assessed by comparing intact (n=10) and anosmic (n=10) multiparous Columbia and Rambouillet ewes and their single lamb during the first 2 months of lactation. Intact mothers only nursed their own lamb (98%) while most of the nursing activity in anosmic mothers concerned alien lambs (78%). On the other hand, the total duration and the frequencies of nursing did not differ significantly between groups (P>0.05). Nevertheless, the total percentage of nursing of own lamb by anosmic mothers (22%) was higher than expected at random (10%). Milk production or lambs weights did not differ between groups. We conclude that prepartum anosmia resulted in the failure of ewes to develop true selective nursing up to the 8th week of lactation, although some preferential mother-young relationship yet developed. On the other hand, it did not affect significantly overall nursing activity.

Differential effects of undernutrition during pregnancy on the behaviour of does and their kids at parturition and on the establishment of mutual recognition

We investigated whether undernutrition during the second half of pregnancy impaired the behaviour of does and their kids at parturition and early mutual recognition. Twenty-two control and 22 underfed mixed-breed, multiparous dairy goats were used, together with their respective kids (control, n = 31: nine singles, 16 twins and six triplets; underfed, n = 32: 11 singles, 18 twins and three triplets). Undernutrition involved limiting protein and energy intake at 70% of the nutritional requirements for maintenance and foetal growth from day 70 of pregnancy until birth. The behaviour of mothers and their two first-born kids was observed for 90 min from the birth of each kid. Maternal olfactory recognition of the kid was assessed at 4 h post partum by testing selective nursing behaviour. Non-olfactory recognition was assessed at 8 h in a two-choice test excluding olfactory cues. In kids, preference for the mother was assessed in a two-choice test at either 12 or 24 h post partum. Bodyweight of does and kids were lower in the underfed group up to 2 weeks post partum. At parturition, licking, maternal bleating frequency and latency to nursing did not differ between nutritional groups. Control kids were faster than underfed kids to stand, search for and reach the udder, but underfed kids bleated more and tended to spend more time at the udder. Both control and underfed does accepted their own kid and rejected the alien in the selectivity test at 4 h. In contrast, at 8 h post partum, only control goats showed a significant preference for their own kid in the non-olfactory recognition test. Both control and underfed kids showed a preference for their own mother at 12 and 24 h and undernutrition during pregnancy had little influence on the performance of kids. However, 12 h-old underfed kids tended to be less active than control kids and visited their own mothers less than control kids. There were no significant correlations between the behaviour of the mother or of the kid at parturition and their performance in the discrimination tests. Overall, undernutrition in the second half of pregnancy appears to be more detrimental for the behaviour of the mother than for the kid. Furthermore, it has more impact on the establishment of maternal non-olfactory recognition than on maternal care at parturition or the establishment of maternal selectivity.

Effects of restricted nursing on milk production and collection, kid growth and plasma prolactin and growth hormone concentrations in dairy goats

The milk production of dairy goats under various regimes of mother-young contact from day 4 post partum were studied during the first 2 months of lactation, together with the prolactin (PRL) and growth hormone (GH) responses to udder stimulation. In the control group, 13 goats and their kids were left in permanent contact and did not undergo milking. In two additional groups, goats were machine milked once a day in the morning (at 0800xa0h) and kids were allowed 10 hours (from 1000 to 2000xa0h; 10H group, nxa0=xa011) or 5xa0h (from 1000 to 2000xa0h; 5H group, nxa0=xa011) of mother-young interaction per day. In the last group (MO, nxa0=xa010), mothers were permanently separated from their kids on day 4 post partum and milked once a day. Milk production during a 24-h period at 37 days post partum performed by controlled nursing and weighing of the kids (groups with kids) or by two machine milking 12xa0h apart (milking only group) revealed a higher production in the three groups with some mother-young contact than in the MO group. Total milk collected by milking over the 2 months of the study did not differ between the three groups that underwent milking. Kid weights at 2 months were 3.4 to 4.8xa0kg. lighter in the groups that underwent milking than in the control group. Hormonal profiles were significantly affected by restricted mother-young contact, with highest pre-stimulation concentrations of PRL and GH in the 5H group. Restricting mother-young contact from the first week postpartum can permit an early collection of milk without major effects on kid growth, when compared with one daily milking in goats totally separated from their young.

Preference of 12-h-old kids for their mother goat is impaired by pre-partum-induced anosmia in the mother

We investigated whether kids were able to discriminate their own mother from an alien one in a two-choice test on the day of birth when they had access to acoustic, visual and olfactory cues from their mother, and whether this discrimination depended on the selective maternal behaviour of the mother (i.e. exclusive nursing of own kids). When given the choice between their own mother and an alien equivalent dam, 8-h-old kids did not show a significant preference for their dam, whereas 12- and 24-h-old kids did. When given the choice between their own and an alien mother that were both non-selective because they had been rendered peripherally anosmic by irrigation of the nostrils with zinc sulphate, 12-h-old kids did not show a significant preference for their mother. These results are similar to those reported in sheep and may suggest that the contrast of behaviour between their own and an alien mother existing in normosmic does is important for discrimination of dams by kids at this age. Finally, testing 8-h-old kids in a smaller enclosure resulted in some improvement of their performance, although they still failed to display a significant preference for their mother. On the whole, kids are able to discriminate between their own and an alien mother goat as early as previously reported in lambs. The impairment of this ability when mothers are anosmic and not selective suggests that acceptance behaviours displayed by the mother may serve as one of the cues orientating the choice of the kid when given the choice between intact mothers. Finally, the present results do not suggest the existence of fundamental differences in the establishment of a preference for the mother between lambs, which are followers, and kids, which are hiders.

Parental Care in Mammals

Publisher Summary This chapter is concerned with the immediate control of parental behavior. When considering the many different forms by which parental care is expressed in mammals and the variety of control mechanisms involved, it becomes quite evident that no general model can be proposed to explain this complex behavior. Even in species occupying the same ecological niches, producing neonates that share the same characteristics, and expressing similar patterns of parental care, the mechanisms that control this behavior are quite different. Typical examples of this are rats and mice: Whereas the former are highly dependent on internal factors (i.e., hormones) for the facilitation of maternal behavior at the first parturition and olfactory cues tonically inhibit maternal responsiveness in virgins, in mice olfactory cues appear to be mostly facilitatory, and endocrine factors are not essential for the rapid display of parental care.