P. Poindron

Genital, olfactory, and endocrine interactions in the development of maternal behaviour in the parturient ewe

This article reviews current understanding of the physiological control of maternal behaviour in parturient ewes. Estradiol is an important endocrine factor which stimulates maternal responsiveness, both in nonpregnant and in parturient ewes. However, its action depends on previous maternal experience, and other factors are also necessary for the rapid manifestation of maternal behaviour. Olfactory cues play a major role in the normal development of the mother-young relationship. Genital stimulation (GS) is a key factor influencing various aspects of maternal responsiveness in sheep. GS acts in synergy with peripheral hormones to induce the rapid onset of licking and immediate acceptance of a neonate at the udder in nonpregnant ewes. It also influences the attraction of amniotic fluid at parturition and reduces aggressive behaviour towards lambs. Deprivation of GS by peridural anesthesia disturbs maternal behaviour in parturient ewes, especially in primiparae. And, additional GS in postparturient ewes allows the formation of a new bond with an alien neonate in mothers which had already established a selective relationship with their own lambs. Some of these positive effects of GS are mediated through modifications of olfactory function (attraction of amniotic fluid, establishment of a selective bond), whereas this may not be the case for other effects (stimulation of licking, reduction of aggressive behaviour). Studies of the neural mechanisms involved will be necessary to specify the modes of action of GS. The first results suggest GS may act in at least two ways at the level of the brain. Stimulation of maternal behaviour could depend on the liberation of oxytocin within the brain, since intracerebroventricular injections of this hormone facilitate maternal responses. Also, GS can influence olfactory function through the activation of afferent noradrenergic pathways in the olfactory bulbs. Further studies need to be developed to specify the relationships between the various structures involved as well as the level at which estradiol exerts its facilitatory action.

Peridural anesthesia disturbs maternal behavior in primiparous and multiparous parturient ewes

Several experiments were carried out to study the effects of peridural anesthesia (Sylvocaine, 6 ml between sacrum and 1st caudal vertebra) performed either at the first signs of birth (early peridural: EP), or little before expulsion (late peridural: LP). When performed late, peridural anesthesia altered maternal behavior only slightly when compared with controls. By contrast severe deficits were observed in the case of EP. Seven out of 8 primiparae failed to show interest for their lamb within 30 min of the birth of the young (vs. 1/9 in LP group, p less than 0.01). In multiparae these proportions were 8/27 and 0/22 respectively (p less than 0.01). Within the EP group the effects of the peridural were more marked in primiparous than in multiparous mothers (p less than 0.05). Even in EP multiparous ewes becoming maternal within 5 min after giving birth a reduction in duration of licking was noted, when compared with the LP group (p less than 0.05). On the other hand, these same ewes established normally a selective bond within 2 hours after giving birth, as did the LP or control ewes. These results confirm the importance of genital stimulation for the rapid onset of maternal behavior in parturient ewes. They failed however to clarify the role played by genital stimulation in the establishment of a selective maternal bond.

Ability of 12-hour-old Merino and crossbred lambs to recognise their mothers

The ability of 12-h-old Merino (M) and Border-Leicester × Merino lambs (BL×M) to be attracted to post-parturient ewes and to recognise their own mothers was tested using a 2-choice situation. When released at 6 m from two ewes placed next to each other, most lambs reached a ewe before the end of the 5-min test (2428). Amongst lambs spending more than 3 min close to the ewes, 79% (1924) spent at least two-thirds of this time next to their own dam. On the other hand, the proportion of lambs reaching their mothers first (1124) did not differ significantly from a choice at random. Also, the proportion of BL×M lambs reaching a ewe (1515) or spending more than two-thirds of their time with their own dams (1415) was higher than in pure M lambs (913 and 59, respectively; P<0.05 in both cases). It is concluded that 12-h-old lambs are able to recognise their mothers at close quarters, but not from a distance of 6 m. These results also suggest that in these tests, BL×M lambs perform better than M lambs.

Ontogeny of social awareness in domestic herbivores

Abstract It is now well established that domestic animals construct responses to their environment that depend on experience and on integration of several features of the environment, including social partners. This ability to be aware of the environment is not fully developed at birth but improves and varies through the animals life. This topic is discussed on the basis of social processes in sheep and cattle. Social relationships of an animal with its conspecifics develop with age; they do not merely depend on pre-programmed behaviours but rely at least in part on learning of characteristics of the partners. Soon after birth, a strong preferential bond establishes with the dam then to a lesser extent, the young associates to other members of the flock, especially other young. The attractiveness of the group varies later in life due to external events or to physiological state: the abrupt separation from the dam at artificial weaning strengthens bonds between peers, whereas around parturition, females are less disturbed by isolation from the group. More recently, the awareness of social partners has been described in non-social contexts: the animal modifies its responses to events according to the presence of partners, and also to their emotional state and behaviour. The effects of partners seem to depend on their relationship with the animal and also on the social motivation of that animal, which both vary during its life. We recommend study of the ontogeny of awareness using the model of social influences.

Influence of breed on reactivity of sheep to humans.

Ewe lambs from 2 breeds (M6rinos d’Arles and Romanov) and their crossbreds, from M6rinos ewes sired by Romanov rams, were observed during 5 individual tests. During the first 3 tests there were no other sheep in sight and animals were alone, with concentrate or with a human. During the last 2 tests, some penmates were in sight and the experimental animal was alone or with a human. Romanov animals were much more reactive than the M6rinos. They eliminated more, ate less and avoided the human more. For most of the criteria, crossbreds were closer to the Romanov than to the M6rinos purebreds. This seemed to be due to genetic differences and not to direct maternal influence.

Comparaison du comportement maternel en bergerie à la parturition chez des brebis primipares ou multipares de race Romanov, Préalpes du Sud et Ile-de-France

Le comportement maternel au cours des 3 premières heures de la vie de l’agneau a été comparé chez des brebis Ile-de-France (IF), Préalpes du Sud (PA) et Romanov (R). L’étude a porté à la fois sur des femelles primipares et multipares dont la reproduction était synchronisée par l’utilisation d’éponges vaginales imprégnées de FGA suivies d’une injection de PMSG, et dont la parturition était induite par une injection de dexaméthasone (IF : 16 mg à J 144 de gestation ; PA : 12 mg à J 143 ; R : 16 mg à J 140). Chez les brebis multipares, aucune différence très marquée n’a été observée entre les 3 races, à l’exception du léchage de l’agneau, qui a débuté plus tardivement chez les IF que chez les R et les PA (P < 0,05 dans les 2 cas). Par contre, les différences entre races ont été beaucoup plus marquées chez les femelles agnelant pour la première fois. Les troubles du léchage ou de l’acceptation à la mamelle ont été moins fréquents chez les R (10 p. 100) que chez les IF (50 p. 100) ou les PA (35 p. 100). Le comportement agressif a été plus fréquent chez les PA (29 p. 100 des mères) que chez les IF (7 p. 100, P < 0,05) ou les R (19 p. 100, ns). 60 p. 100 des mères R n’ont manifesté aucun trouble de comportement dès la parturition et 3 heures plus tard, 90 p. 100 avaient adopté leur agneau. Chez les brebis IF, ces proportions étaient respectivement de 35 et 61 p. 100 (P < 0,05 dans les 2 cas). Les performances des brebis PA étaient intermédiaires (34 p. 100 et 84 p. 100 respectivement). Donc, d’une façon générale, les brebis primipares manifestent plus fréquemment des troubles de comportement maternel que les brebis multipares. Par ailleurs, les brebis Romanov ont eu un comportement maternel mieux adapté que les 2 autres races, et les Ile-de-France sont apparues comme étant les moins bonnes mères. Il faut souligner aussi que dans les 3 races, de grandes variations individuelles ont été notées : certains animaux ont très bien accepté leur agneau alors que d’autres l’on refusé jusqu’à la fin de l’étude.

Influence of the blood concentration of prolactin on the length of the sensitive period for establishing maternal behavior in sheep at parturition.

Abstract The fading of postpartum maternal interest for the neonate (sensitive period) in ewes separated from their young at lambing is delayed when parturition is induced with 20 mg of estradiol benzoate (EB). An experiment was carried out to investigate the role of prolactin in this phenomenon. The sensitive period was studied in three groups of parturient ewes. In all groups lambs were removed at birth and reintroduced to their mothers 24 hr later. Maternal acceptance was tested at this time. In group 1 (dexamethasone D), ewes were induced to lamb with dexamethasone (15 mg im). In group 2 (EB), ewes were treated with 20 mg of estradiol benzoate (im). In group 3 (EB + CB 154) ewes received 20 mg of EB as in group 2 and 1 mg of CB 154 (sc) every 12 hr to prevent the enhanced secretion of prolactin which normally occurs after EB injection. The concentration of prolactin was highest in group 2 (EB), lowest in group 3 (EB + CB), and intermediate in group 1 (D) (p ⩽ 0.001 between groups). By contrast, the proportion of ewes showing maternal behavior was similar in groups 2 and 3 ( 15 23 and 17 22 ), both of which differed from group 1 ( 3 22 ; p ⩽ 0.005 ). It is concluded that the lengthening of the sensitive period for establishing maternal behavior in sheep following EB induced parturition is not related with high levels of prolactin in the peripheral circulation.

Genital stimulation facilitates maternal behavior in estrous ewes

Only a small proportion of ewes at estrus have been found to respond maternally to newborn lambs, and this low maternal responsiveness may be partially attributable to the absence of the genital stimulation which occurs at parturition. Therefore, the effect of artificial genital stimulation on maternal behavior of estrous ewes was investigated. Estrus was synchronized in 33 ewes by placement and withdrawal of progestin-saturated vaginal sponges. Estrous ewes were divided into two groups, a control group and a group receiving 5 min of artificial genital stimulation, and observed following presentation of newborn lambs. Significantly more stimulated ewes licked the lamb and emitted low-pitched bleats in a 30-min test. When genital stimulation was subsequently administered to control ewes, more of them also became maternal so that the two groups were no longer significantly different. These results indicate that absence of genital stimulation is one of the factors contributing to the low maternal responsiveness of estrous ewes. They also demonstrate for the first time that artificial genital stimulation is effective in eliciting maternal behavior in nonpregnant ewes even at physiological concentrations of estradiol.