Raymond Nowak

Mother-young relationships in sheep: a model for a multidisciplinary approach of the study of attachment in mammals.

The onset of maternal responsiveness and the development of mother–young attachment in sheep are under the combined influence of hormonal and sensory stimulations. In the mother, the prepartum rise in oestrogen and vaginocervical stimulation caused by expulsion of the foetus act on the main olfactory system and on hypothalamic regions. This induces maternal care through the central release of oxytocin, modulated by opiates and corticotrophin‐releasing hormone. In parallel, activation of the main olfactory network enables the learning of individual lamb odour and maternal attachment. In the neonate, the first suckling episodes and the concomitant activation of the cholecystokinin, opioids and oxytocin systems facilitate the development of a preference for the mother. Gastrointestinal signals activate the brain stem, the hypothalamus and the amygdala. Within 72 h of parturition, the mother–young attachment shifts from proximal to distal recognition based on visual and auditory cues after which vocal cues become more salient. Although olfaction remains a key element in the display of selective maternal nursing, maternal attachment relies on a multisensory mental image of the lamb. These findings support the view that sheep are amongst the most appropriate animal models for the study of maternal and filial attachment in mammals.

Perinatal visceral events and brain mechanisms involved in the development of mother-young bonding in sheep.

In sheep the onset of maternal responsiveness and the development of the mutual mother-young bond are under the combined influence of hormonal and visceral somatosensory stimulations. These stimuli are provided in the mother by parturition (via steroids and vaginocervical stimulation) and in the neonate by the first suckling episodes (via cholecystokinin and oro-gastro-intestinal stimulation). In addition, each partner relies on specific chemosensory stimulation for reciprocal attraction: amniotic fluids for the mother, colostrum for the young. In the ewe parturition activates several brain structures to respond specifically to sensory cues emanating from the young. The main olfactory bulbs undergo profound neurophysiological changes when exposed to offspring odors at parturition. Additional activations in the hypothalamus - preoptic area - and the amygdala - medial and cortical nuclei - also contribute to maternal responsiveness and memorization of lamb odors. In the neonate, post-ingestive stimulations activate the brain stem via vagal afferents. Like in the ewe, several regions of the hypothalamus and the amygdala respond to colostrum ingestion suggesting common ground for the integrative neural processes involved in early learning and bonding. This leads to rapid visual and auditory recognition in both partners although olfaction remains important in the ewe to display selective nursing. It is concluded that the biological basis for the development of maternal and filial bonding in sheep presents striking similarities.

Do Lambs Perceive Regular Human Stroking as Pleasant? Behavior and Heart Rate Variability Analyses

Stroking by humans is beneficial to the human-animal relationship and improves welfare in many species that express intraspecific allogrooming, but very few studies have looked at species like sheep that do not express such contact except around parturition. This study investigated the way lambs perceive regular human tactile contact using behavioral and physiological responses. Twenty-four lambs were reared and bucket-fed in groups of four. All were stroked daily by their familiar caregiver. At 8 weeks of age, the lambs were individually tested in their home pen but in a 1×1m open-barred pen after a 15h period of habituation to physical separation from peers while remaining in visual and auditory contact. Half of the lambs received stroking by their caregiver for 8min and half were exposed to their caregiver’s immobile presence. Heart rate and heart rate variability were recorded and analyzed by 2-min slots over the same interval based on three measures: mean heart rate value (HR), root mean square of successive differences (RMSSD) and standard deviation of all intervals measured between consecutive sinus beats (SDNN). Behavioral responses (ear postures of the lamb and time spent in contact with the familiar caregiver, on the knees of the familiar caregiver, and moving) were recorded throughout the test. Lamb HR decreased continuously while in the presence of their caregiver. Lambs being stroked showed slower HR and higher RMSSD which reflected positive emotional states compared to lambs left unstroked. All behavioral variables were highly correlated with the main component axis of the PCA analyses: the more the animals stayed in contact with their caregiver, the less they moved and the more their ears were hanging. This first component clearly differentiates lambs being stroked or not. Behavioral and physiological observations support the hypothesis that gentle physical contact with the caregiver is perceived positively by lambs.

Effect of one week of stress on emotional reactivity and learning and memory performances in Japanese quail

Chronic stress is known to induce long term alterations of emotional behaviours as well as cognitive performances leading thereby to welfare or husbandry problems. These stress-induced consequences are observed following long periods of stress lasting from several weeks to several years. The current study examined whether a shorter period of stress (one week) produced similar impairing effects. Two-week old Japanese quail were either submitted to a series of aversive events over consecutive 8 days, at unpredictable times each day (treated animals) or left undisturbed (controls). Following the treatment period, animals were weighed and basal as well as aversive events-induced levels of plasma corticosterone were quantified. Quail were also tested for emotional reactivity in three tests (the tonic immobility test, the hole-in-the-wall and novel object tests) and for spatial reference memory. Although there was no difference in corticosterone levels between the two groups, the treated animals had lower body weight than controls. Behavioural investigations after the treatment period did not reveal any difference between the groups in the three emotional reactivity tests. In the spatial task, treated quail displayed enhanced behavioural flexibility as revealed by their higher performances during the reversal phase of the task. The alteration of growth suggests that a short period of repetitive exposures to unpredictable aversive events can be perceived by quail as stressful. Such a stress period can improve spatial learning performances in quail supporting the critical role played by the duration of the stress period on cognitive performance.

Suckling, Milk, and the Development of Preferences Toward Maternal Cues by Neonates: From Early Learning to Filial Attachment?

Publisher Summary The aim of this chapter is to show how repeated sensory information provided by the mother concomitantly with the occurrence of suckling gains signal value for the neonate. This sensory information then becomes selectively sought for by the neonate and elicits preferential behaviors. This point is illustrated by considering several contrasting species that have been studied in detail, with the rat and the rabbit pup, as examples of altricial mammals, the lamb as a precocial mammal, and the human baby as an intermediate type. Information on other species will only be included to emphasize converging (or diverging) points or to provide information that is not available for the species cited above. Because suckling is the most intimate form of contact with the maternal body, it is at the root of the relationship with the mother. The importance of suckling in developing a preference is unique to the neonatal phase as preventing lambs from suckling at a later stage is void of effect. Nursing–suckling interactions are the result of physiological, morphological, and behavioral changes that ensure extrauterine survival at a time when the young is entirely dependent on its mother for the provision of food. In mammals, the newborn is entirely dependent on its mother for the provision of food. Stimuli associated with suckling shape the behavior of the neonate in diverse manners. In particular, they induce calming, facilitate learning, and are common to a wide range of species—including rats, rabbits, dogs, sheep, and humans.

Temperament does not affect the overall establishment of mutual preference between the mother and her young in sheep measured in a choice test

Temperament influences maternal behavior and lamb survival in Merino sheep selected for calm or nervous temperament. The impact of this selection on mother-young recognition and early expression of temperament in lambs is unknown. We tested the ability of multiparous ewes selected for calm (n = 16) or nervous (n = 18) temperament to recognize their own lambs 6 hr after parturition, the ability of the lambs to display a preference for their own mother at 18 hr, and the temperament of the lambs at 1 and 16 weeks of age. Ewes and lambs from both genotypes showed a similar preference for their familiar kin. In contrast, differences in temperament were detectable at 1 and 16 weeks of age. Nervous lambs showed higher vocal and locomotor activity than calm lambs. Thus, temperament did not affect the early process of ewe-lamb bonding but might affect the quality of the mother-young relationship under more challenging situations.

Amniotic fluid is important for the maintenance of maternal responsiveness and the establishment of maternal selectivity in sheep

Amniotic fluid (AF) is important for the establishment of maternal behaviour in inexperienced ewes, but its role in experienced mothers remains to be studied. Here, the maintenance of post-partum maternal responsiveness and the establishment of exclusive bonding was investigated in multiparous ewes when AF was removed from the neonate or/and physical contact with the young was precluded for the first 4 h post partum. Maintenance of maternal responsiveness and establishment of exclusive bonding were measured by the proportion of mothers accepting their own lamb and alien lambs that had been either washed or not washed, and by comparing an acceptance score for each type of lamb. The acceptance score was computed by summing standardised variables of acceptance (low bleats, acceptance at udder, nursing and licking time) and subtracting standardised variables of rejection (high-pitched bleats, rejection at the udder and aggressive behaviour). Washing the neonate reduced its acceptance score, but the proportion of mothers rejecting their own lamb was reduced only when washing the neonate and prevention of physical contact for 4 h were combined (7/15 v. 0/10 in controls, P = 0.02). In addition, washing the neonate increased the acceptance score of the washed alien lamb, but not of the unwashed alien. However, washing and privation of physical contact did not increase significantly the proportion of mothers accepting an alien lamb at 4 h post partum. We conclude that AF is important in experienced ewes for the establishment of maternal responsiveness, as already found in primiparous mothers. In addition, our results indicate that AF also carries some chemosensory information facilitating exclusive bonding.

Behavioral differentiation during collective building in wild mice Mus spicilegus

Although well documented in social insects, the possibility of behavioral differentiation during collective building has been poorly studied in mammals. In this context, the mound-building mouse Mus spicilegus is an interesting model. Under natural conditions, juveniles from different litters gather vegetal material and build a sophisticated structure, the mound, under which the mice will spend winter. The first steps of this complex building process may be elicited under laboratory conditions by offering cotton balls as building material. Spatio-temporal distribution of both animals and cotton balls was automatically recorded by RFID (Radio-Frequency Identification Device) technique. Our results revealed a behavioral differentiation during a collective building task. In a group of six individuals, only two mice (called carriers) transported 80% of the building material whereas the contribution of the remaining mice was weak or even non-existent. The proportion of carriers was constant in all of the six groups studied. This behavioral differentiation was implemented immediately after the building material was made available and remained stable during the 4 days of experiment. The high contribution level of carriers did not result from resource monopolization, nor did it depend on the gender or parental origin of the mice.

Olfactory preference for own mother and litter in 1-day-old rabbits and its impairment by thermotaxis.

We investigated the ability of rabbit pups to display preferences towards various elements of their postnatal environment during the stage of confinement in the nest. Subjects were submitted to a two-choice test during the first week after birth to assess if they could detect and discriminate between does, litters of pups, or nesting materials of the same developmental stage. On D1 and D7, pups were attracted to any lactating doe, litter, or nest when compared to an empty compartment. When two stimuli were opposed, pups preferred their own nest to an alien one on D1 and D7 but not their mother nor their siblings when opposed to alien does or pups. However, additional tests indicated that this lack of preference for kin conspecifics resulted from a predominant attraction to thermal cues over individual odors. Indeed, pups were strongly attracted to a warm compartment (37 degrees C) than to a cooler one (20 degrees C) and once thermal cues were controlled for in the testing situation, the pups were specifically attracted to odors of their own mothers hair and of their siblings. No preference was observed towards the mothers uterine secretions. In conclusion, pups can recognize olfactory cues emanating from their mother and their siblings the day after birth. The preference for nesting materials would reflect in major part the combined attraction to maternal and sibling odors present in the nest.

Colostrum quality of ewes of calm temperament is not responsible for low lamb mortality

Perinatal lamb mortality is a serious issue for the sheep industries. Starvation is implicated in many of these lamb deaths. Ewes with a calm temperament lose significantly fewer lambs than ewes with nervous temperament, particularly in the critical first 3 days after birth. Colostrum provides essential nutrition to neonatal lambs. This research set out to determine whether ewe temperament affects the quantity and quality of colostrum that ewes produce. Calm temperament was found to have an influence on the viscosity of colostrum 6 h after birth. High variability in all aspects of colostrum production were found in the study and may be a limiting factor in lamb survival in certain circumstances. There is little evidence, however, to suggest a strong association with ewe temperament and is therefore unlikely to explain the lower lamb mortality that is reported to occur among calm ewes.