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.     

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.     

Inactivation of the medial preoptic area or the bed nucleus of the stria terminalis differentially disrupts maternal behavior in sheep

The present study was designed to investigate the role of the medial preoptic area (MPOA) and the bed nucleus of the stria terminalis (BNST) in the onset and maintenance of maternal behavior in sheep. In a first experiment, the MPOA or BNST were transiently inactivated during the first 2 h postpartum in primiparous ewes with the use of the anaesthetic lidocaine. MPOA inactivation greatly impaired the display of maternal behavior whereas inactivation of BNST or of adjacent sites (septum or diagonal band of Broca) or infusion of cerebrospinal fluid did not. In a separation/reunion lamb test (S/R) performed at 2 h postpartum, ewes with MPOA inactivation exhibited little reaction after separation of their lambs and did not show any motivation to reunite with them. Ewes with BNST inactivation showed intermediate performances in the S/R test. Moreover, in control ewes that were maternal for the first 2 h postpartum, MPOA or BNST inactivation performed in the following 12 h induced deficits in the S/R test, indicating that the MPOA and to a lesser extent BNST are also involved in the maintenance of maternal behavior. A second experiment showed that, in multiparous ewes, MPOA inactivation at parturition induced less deficit in the display of maternal behavior and in the S/R test than in primiparous mothers. These findings indicate that the MPOA and, to some extent, the BNST are functionally involved in the initiation and in the maintenance of maternal behavior in sheep, but this involvement is influenced by maternal experience.     

Mother–young bonding in prolific D’man and Romanov sheep

The effect of prolificacy on mother–young mutual recognition is still largely unknown in sheep. The aim of the present study was to investigate the ability of prolific ewes to develop an exclusive bond with their neonate and to recognize each other from alien subjects. Observations were performed on 11 D’man and 16 Romanov ewes with, respectively, 19 and 37 of their lambs. Maternal selectivity was tested at 24 h postpartum during two consecutive periods of 3 min. All mothers accepted their own lambs at suckling, while 21 out of 27 (78%) rejected the alien, thus displaying mostly selective nursing. To assess mother–young recognition, a two-choice test was performed at 36 h postpartum. Ewes clearly preferred their own lambs to an alien lamb and behavioral differences were not found between mothers of small (singletons and twins) and large litters (triplets and quadruplets). Romanov ewes reached their own lambsmore rapidly and spent more time near them than D’man ewes. Lambs from small litters, in particular light lambs, clearly preferred their mothers to an alien dam; however, both light and heavy lambs in large litters did not discriminate between the two stimulus ewes. D’man lambs clearly preferred their mothers to an alien dam; in contrast, such a preference was not as clearly demonstrated in Romanov lambs.     

The effects of twinning and maternal experience on maternal-filial social relationships in confined beef cattle

The objective of this investigation was to assess the maternal-filial social relationships of Hereford beef cattle as influenced by maternal experience of the dam (primiparous vs. multiparous) and number of offspring (one vs. two calves). Calves were temporarily separated from their dams during the first week after parturition, and the behavioral responses of mother and young were noted during and following separation.Contact and contact-seeking behaviors between twins and their mothers began to decline by the 5th or 6th day post-partum. Over the same period, contact behaviors exhibited by single calves and their dams remained stable or increased in frequency. Mothers of twins were less responsive to their calves than mothers of singles both during and following separation, and twins interacted with alien females more frequently than single-born young. It is proposed that insufficient milk production by Hereford dams bearing two calves provides an incentive for twins to parasitize the milk supply of alien mothers and, thus, become less dependent on their natural mothers. Social feedback between mother and twins may be further reduced by dams dividing their maternal attentiveness between two offspring.In general, experienced cows were more responsive to separation from their offspring than inexperienced heifers. Cows and their calves exhibited more frequent contact and contact-seeking behavior than heifers and their young.     

The importance of amniotic fluids for the establishment of maternal behaviour in experienced and inexperienced ewes

Maternal behaviour at parturition was studied in multiparous and primiparous ewes whose lambs had been washed to remove amniotic fluids from their coats. In multiparous ewes, washing of the newborn with soap or water decreased licking of the neonate but did not significantly affect other parameters of maternal behaviour (aggressive behaviour, maternal bleats, or acceptance at udder). By contrast, in primiparous ewes, washing of the neonate with only water dramatically reduced licking behaviour and acceptance at udder, while the incidence of aggressive behaviour towards the neonate was increased (P<0·05 in all cases). It is concluded that for inexperienced ewes amniotic fluid on the lamb's coat is necessary for the normal development of maternal behaviour at parturition. For experienced ewes amniotic fluids also play a facilitatory role, but other sensory information can substitute for this cue.     

Primiparous females do not exhibit reduced maternal care in gray seals (Halichoerus grypus)

We compared the behaviors of primiparous and multiparous gray seal (Halichoerus grypus) females over the course of lactation to examine whether poorly developed maternal behaviors may play a role in the reduced lactation performance observed in primiparous females. Overall, primiparous females spent as much time interacting with their pups as multiparous females. The proportion of time spent nursing their pup increased significantly between early and peak lactation in both primiparous and multiparous females. Although there was no significant difference in the duration of nursing bouts as a function of reproductive status, primiparous females nursed significantly more frequently (bouts/hour) and, therefore, spent a significantly greater proportion of time nursing than multiparous females throughout lactation. Primiparous gray seal females were also significantly more active than multiparous females, however, the difference in activity represented only a small proportion of the overall time budget. We conclude that poorly developed maternal behaviors resulting from a lack of prior reproductive experience are unlikely to account for lower levels of milk energy transfer to pups in primiparous gray seals.     

Pen size and parity effects on maternal behaviour of Small-Tail Han sheep

The aim of this experiment was to study the effects of pen size and parity on maternal behaviour of twin-bearing Small-Tail Han ewes. A total of 24 ewes were allocated to a 2×2 design (six per pen), with parity (primiparous or multiparous) and pen size (large: 6.0×3.0 m; small: 6.0×1.5 m) as main effects at Linyi University, Shandong Province, China. Behaviour was observed from after parturition until weaning. All ewes were observed for 6 h every 5 days from 0700 to1000 h and from 1400 to 1700 h. Continuous focal animal sampling was used to quantify the duration of maternal behaviours: sucking, grooming and following as well as the frequency of udder accepting, udder refusing and low-pitched bleating. Oestradiol and cortisol concentrations in the faeces (collected in the morning every 5 days) were detected using EIA kits. All lambs were weighed 24 h after parturition and again at weaning at 35 days of age. The small pen size significantly reduced following (P<0.005), grooming (P<0.001) and suckling durations (P<0.05), as well as the frequency of udder refusals (P<0.001). However, there was a significant interaction with ewe parity, with decreased grooming and suckling in the small pen largely seen in the multiparous ewes (P<0.001). Independent of pen size, multiparous ewes accepted more sucking attempts by their lambs (P<0.05) and made more low-pitched bleats than primiparous ewes (P<0.001). Multiparous ewes had higher faecal oestradiol concentrations than primiparous ewes (P<0.001), and ewes in small pens had higher faecal cortisol levels compared with ewes in larger pens (P<0.001). As lambs increased in age, the duration of maternal grooming, following and suckling as well as frequency of udder acceptance and low-pitched bleating all declined, and the frequency of udder refusing increased (P<0.001 for all). Ewe parity, but not pen size, affected lamb weight gain during the period of observation (P<0.001). This is the first study to show that pen size, interacting with parity, can affect the expression of maternal behaviour in sheep during lactation. The study is also the first to report on the maternal behaviour of Chinese native sheep breeds (Small-Tail Han sheep), with implications for the production of sheep in China.     

Distance recognition in ewes and lambs kept permanently indoors or at pasture

We tested the ability of Merino and Merino × Romanov ewes and lambs to recognise each other at a distance when given the choice between an alien partner and their own. Two groups of animals were studied. In the first group, multiparous ewes and their lambs were housed permanently indoors at a stocking-rate of 1 ewe/2 m². In the second group, ewes and lambs were run permanently outside in a paddock at a stocking rate of 1 ewe/500 m². Of animals living outside, 87% of ewes recognised their own lamb (100% of multiparous dams versus 84% of primiparous ones, P = 0.02). This differed significantly from a random choice. By contrast, the proportion of correct choices by ewes living inside (all multiparous) was significantly lower (64%) and did not differ from a random choice at the 5% level. Lambs reared outside recognised their dam in 95% of cases, versus 72% in lambs reared indoors (P = 0.01). Both frequencies differed significantly from a choice at random. It is concluded that the environmental conditions in which ewes and lambs are maintained can influence their ability to select their partners at a distance with the help of auditory and visual cues.     

A comparison of primiparous and multiparous mother-infant dyads inMacaca mulatta

The relationships of 42 rhesus monkey mother-infant dyads were examined to investigate the effects of the mothers' parity. Primiparous mothers were found to be younger, more excitable and less confident than the multiparous mothers. They also received more aggression from other adult females living in their social group and were more anxious about their infants, approaching and leaving them more frequently. The primiparous mothers protected their daughters more than the multiparous mothers and their daughters correspondingly spent more time in the ventro-ventral position and more time on the nipple. Their sons however spent less time in contact with their mothers than did the sons of the multiparous mothers. Although the primiparous mothers protected their daughters more than their sons, for the multiparous mothers the converse was true and sons received more maternal protection. It is suggested that the greater protectiveness of the multiparous mothers towards male infants may be a consequence of the interest siblings have in males, whereas the greater protectiveness of primiparous mothers to daughters may stem from their greater vulnerability to attacks from adult females. The importance of mother-mediated sibling influences may explain the lack of strong parity differences in previous studies.     

Role of the vomeronasal organ in neonatal offspring recognition in sheep

Twenty-five pregnant Dorsett ewes were randomly divided into three groups to test if ewes use their vomeronasal organs for offspring recognition during nursing. One group of eight ewes (procaine) were made anosmic by irrigation of the nasal olfactory apparatus with a zinc sulphate procaine solution. The second group of nine ewes (cauterized) had their vomeronasal organs rendered nonfunctional by cauterization of the nasoincisive duct. The third group of eight ewes were the controls. Parturition was synchronized in all ewes with betamethasone on Day 145 of gestation. Maternal responsiveness was tested two separate times with 1- to 2-day-old alien lambs. Each alien lamb trial was conducted 24 h apart. Cauterized ewes allowed alien lambs to suckle and they were unable to distinguish alien lambs from their own lambs, whereas the ewes in both groups with functional vomeronasal organs (procaine and control) violently rejected any alien lamb's attempt to suckle. Thus, female sheep use their vomeronasal organs for neonatal offspring recognition.     

The effects of ablation of the olfactory bulbs on parturition and maternal behaviour in Soay sheep

Eight pregnant Soay ewes were made anosmic by ablation of the olfactory bulbs before their lambs were born. They were observed during parturition and in the following few days. Four out of five ewes seen during parturition did not show pre-natal lip licking which is normally seen in Soays. Four ewes did not lick their lambs properly after birth, and in six there was a lack of specific response to their own lambs, so that strange lambs were often fed. Post-mortem examination showed that olfactory tracts were absent in all except one of the ewes examined. It is suggested that the importance of olfaction in maternal care is concerned with identification of the lamb at close quarters and in forming the ewe-lamb relationship.     

Differences in fertility and suckling patterns between primiparous and multiparous rhesus mothers (Macaca mulatta)

Primiparous females gave birth around the same time as multiparous nonlactating females, and earlier than did multiparous lactating females. No differences in birth sex ratio were found between primiparous and multiparous females. During the breeding season following birth, primiparous mothers returned to oestrus later than did multiparous mothers, and while few primiparous mothers conceived successfully during that season, most multiparous mothers did. Primiparous females suckled their infants more frequently than did multiparous females at all ages; infants of primiparous females also made more nipple contacts per bout, and had shorter sucking bouts. When mothers came into oestrus, suckling frequency drastically increased for primiparous females, but not for multiparous females, magnifying the differences between the two groups. After the first oestrus, suckling frequency declined for all mothers, but multiparous mothers had consistently lower suckling frequencies than did primiparous mothers. The high suckling frequency, and numerous nipple contacts per bout, found among primiparous mothers are likely to be related to the low reproductive chances that these females faced during the breeding season. Multiparous mothers seemed to compensate for their low suckling frequency by lengthening the suckling bouts, and this suckling pattern did not hinder their reproduction. It is argued that primiparous mothers might have to suckle their infants more frequently because they can only produce milk at slow rates, being in this way forced into a reproductively inhibiting suckling pattern. However, the delay in subsequent reproduction could be ultimately advantageous for primiparous mothers if it enhanced infant survival, and allowed the mothers to regain physical condition before reproducing again.     

Maternal ‘imprinting’ or maternal ‘labelling’ in goats?

The present study on maternal ‘imprinting’ in goats initially failed to replicate previous findings that mothers discriminate between their own and alien young, accepting their own kid and rejecting alien kids. Rather, 62% of the mothers accepted both their own and alien kid. This disparity was not due to breed differences, age, or behaviour of the aliens but to length of time the alien kids had been with their own mother. When behaviour was eliminated through anaesthesia or left intact, older aliens that had had no contact with their mother were accepted by other mothers, while those aliens with more than 8 h of contact with their own mothers were rejected (whether anaesthetized or not) by other mothers. Maternal ‘imprinting’ in goats may take longer than previously reported, and mothers may ‘label’ their kids and learn to recognize the labels.     

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.     

Estradiol receptor-alpha 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.     

Hormonal and experiential predictors of infant survivorship and maternal behavior in a monogamous primate (Callicebus cupreus)

To better understand the roles that hormones and experience play in infant survival and maternal behavior in a biparental primate species, we analyzed urinary estrone (E(1)C) and pregnanediol glucuronide (PdG) from 24 socially housed titi monkey (Callicebus cupreus) females over 54 pregnancies (N = 1,430 samples). Pregnancies were categorized according to whether the infant survived (N = 35) or not (N = 19), and by maternal parity (primiparous: N = 9; multiparous: N = 45). Mothers of infants that survived had a significantly greater drop in PdG from the third trimester to the first week postpartum than mothers of infants that did not survive. Multiparous mothers had a greater increase in PdG from the first to the third trimester as well as greater increases in the E(1)C:PdG ratio from the first to the third trimester and from the third trimester to the first week postpartum. There were positive relationships between third trimester PdG and maternal carrying and nursing during the first week postpartum, and between maternal age and carrying during the infant's first month of life. There was a negative correlation between maternal age and PdG during the third trimester. These results suggest that elevated progesterone during late pregnancy followed by progesterone withdrawal immediately following parturition is associated with greater probability of infant survivorship and maternal behavior in this species, and that older females engage in more postpartum maternal care.     

Maternal behaviour and lamb survival: from neuroendocrinology to practical application

Parental care promotes offspring survival and, for livestock species, this care is provided solely by the mother. Maternal behaviour in the sheep has been exceptionally well-studied compared with other species and many of the underpinning biological processes leading to the expression of maternal care are known. In this review the current state of play with regard to the biology of maternal care will be reviewed, and its application to provide practical solutions to reduce lamb mortality considered. For maternal care to be elicited at birth the ewe requires elevated circulating oestradiol in late gestation, which stimulates the expression of oxytocin receptors in both peripheral and central areas (particularly the hypothalamic and limbic areas of the brain). At birth stretching of the vaginocervical canal elicits a spinal reflex which triggers the release of oxytocin primarily from neurones within the paraventricular nucleus of the hypothalamus. Oxytocin release causes an increase in the neurotransmitters noradrenaline, acetylcholine, glutamate and γ-aminobutyric acid (GABA) in the olfactory bulb, and other brain regions important for maternal behaviour. Finally, sensory cues provided by the lamb, in particular the amniotic fluids surrounding it, lead to the expression of maternal behaviours (licking, low-pitched bleats, acceptance of the lamb at the udder and suckling). This allows the expression of the two facets of maternal behaviour in the ewe: nurturance of the young and maternal selectivity, whereby a specific olfactory memory for the ewes own lamb is formed and the expression of maternal care is restricted to this lamb. Variation in the expression of maternal care has been demonstrated in primiparous ewes compared with multiparous, in different sheep genotypes, with undernutrition, stress in pregnancy, following a difficult delivery, and may occur with variation in ewe temperament. An understanding of the importance of the timing of various events in late pregnancy and during parturition, as well as the factors that can disrupt these events, can help to design management activities to minimise risks to the successful onset of maternal behaviour. Management practices that work with the biology of the ewe will be the most successful in ensuring that maternal care is expressed, so improving the welfare of the ewe and lamb, and the profitability of the farm.     

Evidence for Sex-Biased Behavioral Maternal Investment in the Gray Mouse Lemur (Microcebus murinus)

To study sex-differential allocation of maternal behavior in Microcebus murinus, I recorded behavioral patterns on 21 litters from parturition to the weaning period. After a pregnancy of 61.5 ± 0.9 days, females may produce from one to four young per litter. Litters were weaned in 40 days by mothers. Behavioral observations at the beginning of the nocturnal activity period demonstrated that close contacts between mothers and infants were more frequent in multiparous mothers than in primiparous ones (p < .01). Time in close contact with offspring aged >15 days old compared to contacts with neonates is significantly lower only in single-sex litters and is more marked for all-female litters (p < .01). Mother's approaches toward mixed litters or all-male litters were always significantly greater than approaches toward all-female litters (p = .04). However, mother's approaches within mixed sex litters were not biased toward either sex (p = .7). Males in a litter may be interpreted as a stimulator of maternal behavior. Similarly, using retrieving tests of 15-min duration, a significant maternal preference for male neonates is evident. Latency to first retrieval is significantly shorter in multiparous females than in primiparous ones (p < .05) independent of size and sex ratio of the litter. For multiparous females only, male neonates were chosen first for retrieval more often than females (p < .05). Finally, the calls of young played a stimulator effect on maternal retrieving (p < .001). Accordingly multiparous mothers exhibit more interest in their young, which appears to be biased toward male neonates.     

Paternal levels of DNA damage in spermatozoa and maternal parity influence offspring mortality in an endangered ungulate

Understanding which factors influence offspring mortality rates is a major challenge since it influences population dynamics and may constrain the chances of recovery among endangered species. Most studies have focused on the effects of maternal and environmental factors, but little is known about paternal factors. Among most polygynous mammals, males only contribute the haploid genome to their offspring, but the possibility that sperm DNA integrity may influence offspring survival has not been explored. We examined several maternal, paternal and individual factors that may influence offspring survival in an endangered species (Gazella cuvieri). Levels of sperm DNA damage had the largest impact upon offspring mortality rates, followed by maternal parity. In addition, there was a significant interaction between these two variables, so that offspring born to primiparous mothers were more likely to die if their father had high levels of sperm DNA damage, but this was not the case among multiparous mothers. Thus, multiparous mothers seem to protect their offspring from the deleterious effects of sperm DNA damage. Since levels of sperm DNA damage seem to be higher among endangered species, more attention should be paid to the impact of this largely ignored factor among the viability of endangered species.