Chemical olfactory signals and parenthood in mammals

This article is part of a Special Issue “Chemosignals and Reproduction”.In mammalian species, odor cues emitted by the newborn are essential to establish maternal behavior at parturition and coordinate early mother–infant interactions. Offspring odors become potent attractive stimuli at parturition promoting the contact with the young to ensure that normal maternal care develops. In some species odors provide a basis for individual recognition of the offspring and highly specialized neural mechanisms for learning the infant signals have evolved. Both the main and the accessory olfactory systems are involved in the onset of maternal care, but only the former contributes to individual odor discrimination of the young. Electrophysiological and neurochemical changes occur in the main olfactory bulb leading to a coding of the olfactory signature of the familiar young. Olfactory neurogenesis could also contribute to motherhood and associated learning. Parturition and interactions with the young influence neurogenesis and some evidence indicates a functional link between olfactory neurogenesis and maternal behavior. Although a simple compound has been found which regulates anogenital licking in the rat, studies identifying the chemical nature of these odors are lacking. Neonatal body odors seem to be particularly salient to human mothers who are able to identify their infant's odors. Recent studies have revealed some neural processing of these cues confirming the importance of mother–young chemical communication in our own species.     

Olfactory regulation of maternal behavior in mammals

In mammals, olfactory cues are extensively used in many aspects of maternal care to ensure the coordination of mother-infant interactions and consequently the normal development of the offspring. Outside the period of parturition and lactation, when the young are not a behavioral priority, olfactory cues play an inhibitory role on maternal responsiveness since in most mammalian species studied so far, nonpregnant females find the odor of young aversive. On the contrary at the time of parturition, a shift in the hedonic value of infantile odors occurs so that the young now become a very potent stimulus and this sensorial processing constitutes an important part of the maternal motivational system. Moreover, infants' odors provide a basis for individual recognition by their mothers and some species (ungulates) have developed highly specialized mechanisms for processing of the infant signals. Perception of the smell of the young also regulates various aspects of maternal behavior. Dodecyl propionate, a compound released by of pup's preputial glands, has been shown to influence anogenital licking behavior, a fundamental pattern of maternal behavior in rodents. While there is no functional specificity of either the main or the accessory olfactory systems in the development of maternal behavior amongst species, it appears that only the main olfactory system is implicated when individual odor discrimination of the young is required. Neural structures, such as the main olfactory bulb, undergo profound changes when exposed to offspring odors at parturition. These changes in synaptic circuitry contribute both to maternal responsiveness to these odors, to their memorization, and to effects of long-term maternal experience.     

Maternal behaviour and peripartum levels of oestradiol and progesterone show little difference in Merino ewes selected for calm or nervous temperament under indoor housing conditions

Temperament influences the expression of maternal behaviour in sheep under experimental field conditions. We investigated whether maternal behaviour between ewes selected for a calm or nervous temperament is independent from environmental conditions. In addition, the level of maternal behaviour expressed by mothers is correlated with the concentration of hormones during the peripartum period. Therefore, we investigated whether the selection for temperament had resulted in hormonal differences between the two lines with regard to the hormones that could be involved in the onset of maternal behaviour. Oestradiol, progesterone and cortisol concentrations from 4 days before parturition to 24 h after parturition were determined from blood samples collected from 10 calm and 12 nervous ewes. Behavioural interactions between ewe and lamb were also recorded for 2 h starting at parturition. Mothers of both temperament lines showed adequate maternal behaviour under the controlled conditions of the study. Therefore, the results of the study do not suggest that selection for a calm or nervous temperament has profoundly affected the intrinsic ability of mothers to display adequate maternal behaviour. Hormonal differences between the two temperament lines were generally small and their possible influence on the display of maternal behaviour in the two temperament lines would have to be demonstrated.     

Affinity towards maternal odour and offspring dispersal in the common lizard

Kin competition is known to strongly influence the spacing behaviour of juveniles in the common lizard, a species which is only weakly social and has no parental care. We examined whether variation in offspring dispersal propensity was associated with variation in their ability to discriminate odours of their mothers versus unknown females. We caught pregnant females in two populations and reared them in the laboratory until parturition. Just after birth, we recorded the juvenile response to the odour of either their mother or an unrelated female. Mothers and offspring were then released at the mother's last capture point, and juvenile movement was monitored by recapture for 2 years. Philopatric individuals were more attracted to the odour of their mother and more repulsed by the odour of an unrelated female than dispersers. In this species, ability to discriminate maternal cues appears to be implied in the spacing behaviour of juveniles. Since juvenile males and females reacted in the same way, the main role of mother discrimination is likely to be the avoidance of kin competition by promoting juvenile dispersal. This does not necessary require mother discrimination to imply mother recognition, or not to be implied in other functions such as inbreeding avoidance. Further research is needed to clarify these points. We suggest that context-dependent kin discrimination may be involved in the spacing behaviour of a large number of species, even for those species where other social functions for kin discrimination have been proposed.     

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.     

Post‐birth separation affects the affiliative behaviour of kin in a pitviper with maternal attendance

The relatedness of individuals can have pronounced effects on behavioural interactions, as engaging in mutually beneficial behaviours with kin can increase inclusive fitness. Parental care can be particularly important for kin discrimination in birds and mammals, but similar studies have not been conducted on species exhibiting more rudimentary forms of care. Maternal attendance of young is ubiquitous among viviparous temperate pitvipers, but the adaptive value of this behaviour has received little attention. We sought to determine if being deprived of a maternal attendance period as neonates altered how cottonmouths (Agkistrodon piscivorus Lacépède), a common North American pitviper, responded to kin vs. non‐kin. We measured the affiliative behaviour of related and unrelated juvenile–juvenile and mother–juvenile pairs that had been allowed a maternal attendance period or had been separated since birth. We found that maternal attendance was not required for sibling or mother–offspring recognition, but did enhance female affiliative behaviour overall, and particularly that of sisters. In contrast, related juveniles that were separated at birth showed a reversal of the sex‐specific affiliative behaviour observed in maternally attended juveniles. Post‐birth separation had only a modest effect on mother–juvenile affiliative behaviour, and no effect on the strong affiliation between mothers and daughters. The patterns of affiliative behaviour observed in maternally attended snakes corresponded to patterns that have emerged from previous captive and field studies of pitvipers; however, the behaviour of juveniles separated at birth was atypical. Thus, it is possible that maternal attendance plays some role in the development of adaptive sex‐specific and kin‐directed affiliative behaviour in pitvipers.     

Sensory and physiological determinants of maternal behavior in the goat (Capra hircus)

Maternal behavior in the goat appears at the time of parturition, partly under the activating influence of vaginocervical stimulation. Mothers actively lick their neonate and rapidly establish a selective bond with their kid through olfactory recognition. They also develop visual and acoustic recognition of the kid within 4 h following birth. Acoustic recognition is present at 48 h. The establishment of maternal recognition can be impaired by underfeeding during the second half of pregnancy. There is no indication that the mechanisms controlling the onset of maternal behavior and bonding are different from those reported in sheep, despite the fact that lambs start to follow their mother within a few hours after birth and kids hide for about a week. During lactation, the cues provided by the kid are necessary for the maintenance of maternal responsiveness, but suckling itself does not appear of primary importance. The presence of the kid also modulates the hormonal response to udder stimulation and influences recovery of postpartum sexual activity when kidding (i.e. birthing) takes place in autumn. Finally, the rapid establishment of mutual attachment between mother goats (does) and their kids offers the possibility to investigate an aspect of mother-young affiliation that is not present in many laboratory species.     

Maternal care and foal social relationships in a herd of Sorraia horses: Influence of maternal rank and experience

The influence of maternal rank and experience on patterns of maternal care and social relationships of foals were investigated in a managed herd of Sorraia horses, Equus caballus. Social interactions and spatial relationships of 13 foals (seven females and six males) born to seven mares were examined from birth to 10 months of life, within the three major periods of foal development. Conflict over suckling between dam and foal was not generally affected by rank and experience, but higher-ranking mothers allowed more suckling during late lactation than lower-ranking mothers. Foals of higher-ranking mares spent more time in proximity to the mother during socialization. Maternal rank and experience did not significantly affect maternal protectiveness, foal independence from the mother or the development of affiliative relationships between foals and group members. Foals of higher-ranking mares received lower frequencies of aggression from other horses only in the first month of life. Dominance relationships among foals depended mainly on aggressiveness and were not associated with maternal rank. The large variability in maternal behaviour, the absence of a significant association between maternal rank and body condition at parturition and the stable social environment within this herd may partly account for the reported results.     

The influence of phenotypic and genetic effects on maternal provisioning and offspring weight gain in mice

Close interactions between mother and offspring are said to result in a coevolution of parental and offspring genotypes such that offspring are adapted in their solicitation behaviour to obtain maternal provisioning that maximizes their fitness. Few empirical studies have been conducted in this field and it remains unclear whether maternal provisioning and offspring weight gain are influenced by the same set of maternal and offspring phenotypic and genotypic factors. Using a cross-foster, split-litter design in mice, we found that overall maternal provisioning and offspring weight gain are significantly correlated but are affected by a different set of parameters, except for the effect of maternal bodyweight. While the level of maternal provisioning was influenced by both offspring and foster mother genotype, offspring weight gain was only affected by the number of males in the mixed litter. We suggest that this disparity may hint at the inefficiency of offspring solicitation behaviour or effects of sibling competition.     

A pheromone to behave, a pheromone to learn: the rabbit mammary pheromone

Birth is part of a continuum and is a major developmental change. Newborns need to adapt rapidly to the environment in terms of physiology and behaviour, and ability to locate the maternal source of milk is vital. Mechanisms have evolved resulting in the emission of olfactory cues by the mother and the processing of these cues by the young. Here, we focus on some sensory, cognitive and behavioural strategies developed by the European rabbit (Oryctolagus cuniculus) that optimize the early development of offspring. In this species, chemosensory communication between the mother and young plays a critical role in eliciting adaptive neonatal responses. In particular, lactating females release a molecule, the mammary pheromone, which has several functional impacts. It triggers orocephalic responses involved in the quick localization of nipples and sucking. Moreover, this unconditioned signal promotes rapid appetitive learning of novel odorants, acting as a potent organizer of neonatal cognition. The mammary-pheromone-induced odour memory requires consolidation/reconsolidation processes to be maintained in the long term. Finally, as this mode of conditioning also promotes learning of mixtures of odorants, it supports investigations related to the capacity of neonatal olfaction to extract biological value from the complex environment.     

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.     

Direct Exposure to Corticosterone During Embryonic Development Influences Behaviour in an Ovoviviparous Lizard

It is becoming increasingly clear that conditions experienced during embryonic development can be of major importance for traits subsequent to parturition or hatching. For example, in mammals, offspring from stressed mothers show a variety of changes in behavioural, morphological, and life‐history traits. The effects of maternal stress on trait development are believed to be mediated via transfer of glucocorticoids, the main hormones released during the stress response, from mother to offspring. However, also other physiological maternal responses during stress could be responsible for changes in offspring phenotype. We investigated the direct effects of corticosterone on offspring development, without other confounding factors related to increased maternal stress, by injection of corticosterone in eggs of the ovoviviparous lizard Lacerta vivipara. Corticosterone‐manipulated offspring did not show impaired development, reduced body size or body condition at parturition. However, corticosterone‐treated offspring showed altered anti‐predator behaviour, as measured by the time required to emerge from shelter after a simulated predator attack. Differential steroid exposure during development, possibly mediated by maternal stress response, may explain some of the variation in behaviour among individuals in natural populations.     

Behavioural interactions of dairy cows with their newborn calves and the effects of parity

Continuous observations of 82 individually penned Friesian cows and their calves were made during the first 6 h post partum. The behaviour observed was similar to that described for wild ungulates of the ‘hider’ type. Cows showed a marked decrease in calf-directed activities with time after parturition. This was more pronounced in older animals, which recommenced ingestive behaviour sooner. The incidence of licking and other maternal behaviour depends upon the characteristics of the calf and upon the state of the mother. Close proximity between cow and calf was maintained, in small calving pens, by the mother at the first three calvings but by the calf after these. The eating of the afterbirth is considered to be anti-predator behaviour. Calves of primiparous dams spent more time suckling and suckled from more quarters than did calves of older cows. Primiparous dams showed a higher incidence of abnormal maternal behaviour.     

Communication in bacteria: an ecological and evolutionary perspective

Individual bacteria can alter their behaviour through chemical interactions between organisms in microbial communities - this is generally referred to as quorum sensing. Frequently, these interactions are interpreted in terms of communication to mediate coordinated, multicellular behaviour. We show that the nature of interactions through quorum-sensing chemicals does not simply involve cooperative signals, but entails other interactions such as cues and chemical manipulations. These signals might have a role in conflicts within and between species. The nature of the chemical interaction is important to take into account when studying why and how bacteria react to the chemical substances that are produced by other bacteria.     

Mother-offspring bonding in farmed red deer: accuracy of visual observation verified by DNA analysis

The accuracy of a maternity assessment based on visual observation was tested during the post parturient phase in farmed red deer. The mother of the calf was determined using visual observation of the hind's peri-parturient and early maternal behaviour during the first week of the calf's life. This assessment was compared with genetic analysis based on DNA microsatellite polymorphism. Data for 48 new-born calves and 50 hinds were compared. The visual assessment of maternity was correct in 43 of the 48 cases (89.58%). In the five remaining cases the mother was identified by DNA testing whereas adoptive mother was determined by visual observation. Altogether 14 cases of adoption were seen in this study and in 9 cases the biological mother was correctly determined by visual observation. Detailed observation of the hind-calf interactions during calving and the first week after the parturition allowed an accurate prediction of maternity. However, such observation is technically demanding.     

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.     

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.     

Reduced progesterone metabolites in human late pregnancy

In this review, we focused on the intersection between steroid metabolomics, obstetrics and steroid neurophysiology to give a comprehensive insight into the role of sex hormones and neuroactive steroids (NAS) in the mechanism controlling pregnancy sustaining. The data in the literature including our studies show that there is a complex mechanism providing synthesis of either pregnancy sustaining or parturition provoking steroids. This mechanism includes the boosting placental synthesis of CRH with approaching parturition inducing the excessive synthesis of 3beta-hydroxy-5-ene steroid sulfates serving primarily as precursors for placental synthesis of progestogens, estrogens and NAS. The distribution and changing activities of placental oxidoreductases are responsible for the activation or inactivation of the aforementioned steroids, which is compartment-specific (maternal and fetal compartments) and dependent on gestational age, with a tendency to shift the production from the pregnancy-sustaining steroids to the parturition provoking ones with an increasing gestational age. The fetal and maternal livers catabolize part of the bioactive steroids and also convert some precursors to bioactive steroids. Besides the progesterone, a variety of its 5alpha/beta-reduced metabolites may significantly influence the maintenance of human pregnancy, provide protection against excitotoxicity following acute hypoxic stress, and might also affect the pain perception in mother and fetus.     

Maternal Care and Infanticide by Males in Helvibis longicauda (Araneae: Theridiidae)

Maternal care in spiders varies from just the construction of a protective silken structure for the eggs and the selection of a safe site to place them, to a long period of association between the mother and spiderlings. Such extended care may involve the active protection from predators and parasitoids, food regurgitation, the production of trophic eggs and even matriphagy. In this study, we describe extended maternal care in Helvibis longicauda (Theridiidae) and evaluate the effectiveness of maternal protection against predators of eggs and spiderlings. We conducted experiments comparing the frequency of egg sac destruction and mortality of spiderlings in the presence and absence of mothers. We also observed the behaviour of the mother and spiderlings during prey capture events and interactions with possible predators. Helvibis longicauda females guard their egg sacs until the emergence of the young and guard the spiderlings for several instar stages, fighting possible predators, including conspecifics. We found that aggressive behaviour by females increased the survival of both eggs and spiderlings in our experiments. Intruder males were the main source of mortality in the absence of females. The benefits of maternal care for the young also include the acquisition of prey items that are captured, immobilized and pre‐digested by the mother. Effective maternal protection and the extended period of supplying food to juveniles probably contribute to the late dispersal of offspring in H. longicauda.     

A method for encouraging maternal care in the giant panda

We developed a method to facilitate maternal care in a giant panda (Ailuropoda melanoleuca) female that rejected her cub immediately after parturition. After removal of the cub, the female was systematically exposed to a regime of infant‐related stimuli, including a surrogate toy panda, accompanied by infant vocalizations and urine, and the mother's own milk. The female displayed several measures of maternal behavior toward the surrogate, for example, spending 61% of her time holding the surrogate in positions typical for the species. There was some evidence that maternal proficiency increased across the 4 weeks of the experiment. Results also indicate that the female was responsive to both infant vocalizations and urine, but not milk. After a transitional period in which we assisted the female in her efforts to nurse and groom the infant, all maternal care‐giving responsibilities were returned to the mother. Over the next 3 months, the pattern of maternal care followed the species‐typical course of declining mother‐infant contact, grooming, overall interaction time, and responsiveness to the cub's vocalizations. This study marks the first successful reunification of a giant panda mother with an infant separated at birth and, it is hoped, will serve as a model for similar efforts elsewhere. Zoo Biol 19:53–63, 2000. © 2000 Wiley‐Liss, Inc.