Mother–infant relationships and maternal estrogen metabolites changes in macaques (Macaca fuscata, M. mulatta)

Abstract

This research assessed mother-infant relationships in rhesus and Japanese macaques living in analogous captive social groups, and monitored changes in the levels of excreted estrogen metabolites during the peripartum period. Each mother-infant pair was focally observed 3 h per week during the first 12 weeks of life of newborns. Fecal samples were collected twice a week from each mother, starting 4 weeks before delivery and ending 4 weeks after delivery. Infant-directed behaviors appeared to be consistently less protective/controlling and more rejecting in rhesus macaques than in Japanese macaques. Estrogen metabolite levels during the perinatal period were, on average, 3-fold higher in Japanese macaques and showed a sharp increase during the last weeks of pregnancy only in the Japanese macaque group. Considering the ecological and behavioral similarities between Japanese and rhesus macaques, the divergence between the two species in the onset and maintenance of maternal behavior was unexpected. This was possibly linked to the difference in the overall body size and life history, and to the striking divergence in estrogen metabolite variation during the peripartum period. Group size, social relationships, and average age of individuals in the two captive groups were not clearly involved in the recorded differences in maternal behavior.Keywords Japanese macaque AE Rhesus macaque AE Maternal behavior AE Estrogen metabolites AE Enzyme immunoassays Primates (2003) 44: 91-98

Maternal behavior and maternal stress are associated with infant behavioral development in macaques

“…This confirms the importance of taking into consideration inter-specific variability when assessing the role played by mothers during infant development, even for species sharing very close ecological and behavioral characteristics (Bardi et al, 2003b;Fa, 1989;Maestripieri, 1994;Thierry, 1985). As a species, Japanese macaque infants show higher levels of social contact toward other group members even if they experience less overall rejection episodes (Bardi et al, 2003c;Hiraiwa, 1981), and stay longer in contact with their mothers (Collinge, 1991;Hiraiwa, 1981;Mason, Long, & Mendoza, 1993;Tanaka, 1989). This indicates that species-specific effects may be as important, if not more important, as inter-specific mechanisms of mother-infant regulation.…”

“…Mother-infant interactions were recorded during the first 3 months of the infant's life. Due to the difference in mothering style between the two species, with rhesus usually characterized as both rejecting and controlling, while Japanese macaques as more laissez-faire (Bardi, Shimizu, Barrett, Borgognini-Tarli, & Huffman, 2003b;Bardi, Shimizu, & Borgognini-Tarli, 2003c;Bardi, Shimizu, Fujita, Borgognini-Tarli, & Huffman, 2001;Gomendio, 1995;Maestripieri, 1994), we are also expected to be able to discern different developmental trajectories in these two groups. Comparative studies carried out in similar environments are largely missing from the literature (Maestripieri, 1994;Bardi et al, 2003c), and considering the diversity of parental behavioral characteristics even in closely related species (Young & Insel, 2002), and the variability in behavioral propensities at the intra-specific level (Strier, 2003), more comparative studies are needed to fully realize the opportunity to assess how species-specific differences in behavior are associated with differences in neurondocrine organizations.…”

Mother–infant interactions in free-ranging rhesus macaques: Relationships between physiological and behavioral variables

“…For example, recent studies have investigated the relation between physiological changes accompanying pregnancy and lactation and changes in maternal motivation [29–32], the physiological correlates of individual differences in mothering style [33–41], and the physiological mechanisms through which early exposure to variable mothering style affects offspring behavioral development [19,21,23,28,42]. Research on the physiological substrates of maternal motivation and mothering style has focused on hormones of the hypothalamic-pituitary-gonadal (HPG) and the hypothalamic-pituitary-adrenal (HPA) axes, such as estrogen, progesterone, prolactin, and cortisol [31–33,36,37,43], as well as on endogenous opioids [44,45] and brain monoamines [28,39,46–48]. Although studies of rodents and sheep have implicated oxytocin in maternal motivation and behavior [49–51], there is limited research on oxytocin and maternal behavior in primates [52–54].…”

Emotions, stress, and maternal motivation in primates

“…Rhesus macaque females whose ovaries had been removed increased significantly their frequency of interactions with other females' infants after the administration of estradiol in doses similar to those of middle‐late pregnancy [Maestripieri & Zehr, 1998]. Further correlational evidence of a relation between infant handling and periparturitional changes in estrogen, progesterone, and also cortisol has been obtained in Japanese macaques and in baboons [Bardi et al, 2001, 2003a, b, c, 2004; Ramirez et al, 2004]. These findings obtained with Old World monkeys confirmed previous results obtained with common marmosets, in which nonpregnant females treated with estrogen and progesterone in concentrations similar to those of late pregnancy showed a significantly higher motivation to interact with infant stimuli (they pressed a bar in order to simultaneously gain visual access to a replica of an infant and turn off an audio recording of infant distress vocalizations) than nontreated females [Pryce et al, 1993; see also Pryce et al, 1988].…”