Mothers, not fathers, determine the delayed onset of male carrying in Goeldi's monkey (Callimico goeldii)

In biparental species, females are thought to accept and even to seek male assistance in rearing of the young. In this study, we present data that suggests that Goeldi's monkey females (Callimico goeldii) actually reject male parental care for a certain period. In Callimico, which have biparental care, mothers carry the infant exclusively for the first three weeks despite the fact that fathers are interested in their infants directly after birth. Fathers initiated significantly more body contact with their mates when newborn infants were present and retrieved one-day-old infants that were experimentally presented to them. The onset of paternal carrying in our colony was 27.5 days compared to 11.5 days (medians) observed in the field. However, presentation of a live potential predator induced earlier onset of paternal carrying by about 10 days. Additional costs to maternal carrying such as foraging and predator avoidance are likely factors influencing the decision of the mother as to when to share the cost of infant carrying with the father. We conclude that Goeldi's monkey fathers start carrying their infants so late because they do not get them earlier from the mother. We suggest that one ultimate explanation for that delay might be increased infant mortality when infant transfer starts at an earlier stage.     

Nighttime Wakefulness Associated with Infant Rearing in Callithrix kuhlii

Parent-infant cosleeping occurs in human and nonhuman primates, yet studies on the impact of cosleeping on parental sleep patterns have been limited to human mothers. We examined the effects of cosleeping on the nighttime wakefulness of a biparental New World primate, Wied's black tufted-ear marmoset (Callithrix kuhlii). We compared the sleep patterns of marmoset parents caring for young infants to those without infants, using an 8 mm videocamera and timelapse VCR under infrared illumination. The presence of young infants significantly impacted the sleep of mothers but not fathers. In fact, mothers rearing young infants were awake >3 times as often as mothers without infants. We also examined the nighttime wakefulness of marmoset parents across the first 9 weeks of infant life (birth through weaning). Although callitrichid mothers tend to reduce their daytime investment in offspring very early in infant life by relinquishing the care of infants to fathers and alloparents, increased nighttime wakefulness was not limited to the early postpartum period for the mothers. Instead, mothers exhibited more nighttime wakefulness than fathers did across the first 9 weeks of infant life. Our results indicate that the presence of infants has a greater impact on the sleep patterns of Callithrix kuhlii mothers than fathers, suggesting that mothers are more involved in infant care than previously realized and that fathers are not nearly as involved in nighttime care as their behavior during the day would suggest.     

Contributions to infant care in captive cotton-top tamarins (Saguinus oedipus): The influence of age,sex, and reproductive status

Marmosets and tamarins are characterized by a reproductive strategy that includes twinning, and a communal rearing system in which infant care is shared among all group members, both breeders and nonbreeding helpers (often older offspring). In order to test some predictions about the extent to which different age-sex classes should invest in infants, contributions to infant carrying and food-sharing by all family members were measured in captive groups of cotton-top tamarins (Saquinus oedipus) ranging in size from 2 to 12 independent individuals. Fourteen litters were observed from birth to 12 weeks. Carrying by mothers decreased steadily over the study period, while carrying by fathers and other offspring increased for 3–5 weeks, then declined. Infants spent more time carried by siblings than by either parent, but parents did more carrying than individual siblings and, also, shared more food with infants. Older siblings contributed more care than younger siblings did. Adult sons carried infants more than adult daughters did, but immature daughters carried more than immature sons did. However, adult daughters actively offered food to infants more than any other class of helper did. These results were interpreted in the light of hypotheses concerning the reproductive and dispersal strategies of callitrichid species.     

Costs of infant‐carrying in the cotton‐top tamarin (Saguinus oedipus)

Infant‐carrying behavior among callitrichids seems to be a costly activity. Costs have been related to the physical efforts of carrying the weight of very heavy infants and to the resulting reduction in foraging efficiency. However, the costs of carrying in terms of the physical consequences for carriers have not previously been assessed. In this study, we have regarded weight loss in infant carriers as a measure of costs. We studied five families of cotton‐top tamarins (Saguinus oedipus) during the first 9 weeks following the birth of infants. Captive‐breeding conditions were required so that body weight could be measured frequently. To avoid inflicting undue stress on the subject animals, we used a noninvasive method for weighing the tamarins. Differences in carrying contribution were found amongst fathers and male and female helpers, with female helpers contributing less. We have found that carrying infants in the cotton‐top tamarins is an activity that produces a weight loss. Fathers and male helpers go through a maximal body weight loss. While carrying, the tamarins also decrease food intake. However, no relationship was found between contribution to carrying and feeding time or in energetic intake during feeding observations. Thus, it seems that a direct relation doesn't exist between the observations of feeding and weight loss. Fathers increase their contribution to carrying during mothers' periovulatory periods. In this period, male helpers and especially fathers go through a maximal body weight loss. We found body weight losses of up to 11.3% in one subadult male and 9.1percnt; in a father during the fifth week. No changes occurred in food intake in fathers or other male helpers during this period. During periovulatory periods, mothers carried less frequently but did increase their food intake. They gained weight from the second week after birth onward, especially during the periovulatory period. It seems that the infant‐carrying behavior of fathers and male helpers may contribute to the improvement of the mothers' physical condition after birth and therefore may support a consecutive pregnancy. Am. J. Primatol. 48:99–111, 1999. © 1999 Wiley‐Liss, Inc.     

The development of infant-caregiver relationships in captive common marmosets (Callithrix jacchus)

The growing independence of infant common marmosets from their caregivers is promoted primarily by their caregivers, who increasingly often prevent the infants from climbing onto them and decreasingly often pick the infants up. Infants achieve independence from their mothers, fathers, and older siblings at different rates and develop characteristically different relationships with them. Infants that are most rejected by caregivers spend the least time on them. When rejected by their parents, infants tend to spend their time with their twins, rather than seeking to climb onto other caregivers. Caregivers do not compensate for unduly large or small amounts of care given by other members of the group. It is argued that if we are to understand the development of caregiver-infant relationships in species with multiple caregivers, we must discover the rules by which infants assess the amount of care they perceive themselves to have received and caregivers assess the amount of care they perceive themselves to have offered. The implications of a simple model based on expected levels of caregiving and careseeking are explored, particularly with respect to competition and compensation.     

Variations in care for cottontop tamarin, Saguinus oedipus, infants as a function of parental experience and group size

We examined the effects of parental experience and group size on infant care and development. Ten cottontop tamarin families were followed across three consecutive births of offspring to examine differences in survival, quality of care, developmental maturation and physical development for infants in two experimental conditions: (1) in large groups with previous parenting experience and (2) in small groups with little or no parenting experience. Although we found no differences in infant mortality, parents treated infants differently between conditions. However, when we examined the cumulative care provided by parents and sibling helpers together across experimental conditions, there were no differences in the rates of retrieval or rejection of infants. Overall levels of infant transport and food transfers were similar between conditions, with fathers and sibling helpers contributing the bulk of care. Fathers in small groups carried infants and transferred food with infants much more than helpers but, as group size increased, helpers augmented this role. Infant development varied with the experience of the family both between conditions and within a family. The results indicate that infants receive similar levels of care regardless of group size and parenting experience, although the individual contributions of family members change with both factors. Parental experience with previous infants had effects on early infant development, but only for the first sets of infants. Copyright 2002 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.     

Suppression of prolactin does not reduce infant care by parentally experienced male common marmosets (Callithrix jacchus)

High levels of prolactin have been found to correlate with the expression of paternal care in a variety of taxa. However, in mammals, there is little experimental evidence that prolactin is causally involved in the stimulation or maintenance of paternal care. Here, we suppressed prolactin production in paternally experienced common marmoset fathers in their family groups during the first 2 weeks after their infants were born. Circulating prolactin levels were suppressed using cabergoline (Dostinex: Pfizer), a long acting dopamine (D2) agonist with minimal behavioural side-effects. A within-subject design was used to compare behavioural and hormonal data on 5 paternally experienced fathers during two consecutive births. Cabergoline reduced prolactin to negligible levels in all fathers without effecting testosterone, DHT and cortisol and without adverse side-effects. However, lowering prolactin had no significant effect on the expression of majority of the behaviour patterns associated with paternal care. These included infant carrying, infant grooming and the frequency with which fathers retrieved and rejected infants. The only infant-related behaviour to be affected was the frequency with which fathers touched, licked and investigated infants. We noted a marginally significant increase in this behaviour during cabergoline treatment. Despite the lack of effect on paternal care, cabergoline did exert an effect on the affiliative/sexual behaviour of fathers as there was a significant increase in the grooming behaviour fathers directed at and received from their mates during drug treatment. This study showed that experienced male marmosets can express paternal behaviour in the absence of the high prolactin levels normally seen after infants are born.     

Male investment under changing conditions among chacma baboons at Suikerbosrand.

Male investment in infant baboons was measured by frequency of carrying from 1978 through 1985. A series of hypotheses was generated and tested with the carrying data, based on the assumptions that: male baboons have some capacity to estimate likelihood of paternity; where paternity probability is greater, males will invest more, where potential benefits to males or infants are higher, males will invest more. Carrying was affected by probability of paternity, availability of estrous females, season of conception and season of carrying, infant age, subtrooping, and predation risk. Infants were carried by probable fathers, siblings, mothers' siblings, and unrelated "suitors." Male investment increased female reproductive fitness: carried infants were more likely to survive, and mothers of carried infants had shorter interbirth intervals. Males appeared to estimate paternity both by observed copulations by other males and by the likelihood that copulations could have occurred without being observed. Male care of infant baboons may also be affected by female choice among males, the distribution of probable infants in time, male tenure at alpha rank, the number of males per troop, the probability of infanticide, and energy demands. Subtrooping seems to be historically crucial, by initially creating a situation in which some males have high paternity certainty.     

Social development during the first twenty weeks in the cotton-top tamarin (Saguinus o. oedipus)

Fourteen infant cotton-top tamarins from five captive family groups were studied during the first 20 weeks of life. We examined the roles of parents and of siblings of different ages as caregivers and as social companions for the infants, as well as the effects of group composition and group size on these roles. Parents and adult siblings played similar active roles in infant caregiving during the first few weeks after birth, with males showing a greater involvement than females. In groups without other offspring the two parents showed equal infant caregiving behaviour, whreas fathers carried more than mothers did in groups with offspring present. Although infants received more caregiving from males, they showed a preference for contact and proximity with their mothers. No sex differences were found in infant behaviour or in the direction of behaviour by caregivers toward infants. Twins showed greater amounts of both social and solitary play in weeks 15–20 than did singletons, and there was no effect of the number of older siblings on the amount of play shown by an infant.     

Infant carrying in family groups of goeldi's monkeys (Callimico goeldii)

Goeldi's monkey (Callimico goeldii) is closely related to marmosets and tamarins. Like marmosets and tamarins, C. goeldii lives in family groups, and fathers and older offspring (helpers) participate in infant carrying. In contrast to the typical twin births in marmosets and tamarins, C. goeldii has only single offspring, and paternal carrying is delayed. We studied infant carrying following 26 births in eight groups of C. goeldii, testing hypotheses proposed in the literature on infant carrying in marmosets and tamarins. The infant was carried exclusively by the mother for the first 26.3 days after birth. Afterwards other group members participated in infant carrying. Whereas the C. goeldii mother is always the main carrier, the father does not always carry more than helpers. In contrast to other callitrichids, age and sex of sibling helpers was not found to have an effect on the participation in infant carrying. The participation in infant carrying in Callimico indicated intraindividual consistency, i.e., the amount of infant carrying performed by fathers and helpers following one birth correlated significantly with the amount of infant carrying of the same individuals following the next birth. We found a significant negative correlation between parental infant carrying and group size, indicating that helpers really do help, sharing the carrying burden with their parents. This is attributed to a clear trend for a reduction in maternal carrying in the presence of helpers, whereas fathers did not benefit from helpers. We conclude that the infant-carrying pattern in C. goeldii is different from the infant-carrying pattern in marmosets and tamarins. The main differences were that the mother instead of the father is the main carrier, and that there is a clear time delay between infant birth and when the father and helpers participate in infant carrying.     

Comparison of infant care in family groups of the common marmoset (Callithrix jacchus) and the cotton-top tamarin (Saguinus oedipus)

The involvement of parents and siblings in infant care in similarly composed groups of common marmosets (Callithrix jacchus) and cotton-top tamarins (Saguinus oedipus) was compared during the infants' first 8 weeks of life. The results indicate an earlier infant independence in C. jacchus than in S. oedipus due primarily to a more frequent rejection of carried infants in C. jacchus. There was no species difference in extent of maternal involvment in carrying infants. However, S. oedipus fathers carried infants significantly more often during weeks 5–8 than did C. jacchus fathers. Siblings were generally more involved in infant care at an earlier infant age in C. jacchus than in S. oedipus.     

An investigation into the socioendocrinology of infant care and postpartum fertility in Goeldi’s monkey (Callimico goeldii)

We investigated the existence of interaction between the major behavioral and endocrine events that occur in breeding pairs of Callimicoduring the postpartum period: the reduction in maternal care, the onset of maternal aggression, the onset of paternal care, and the resumption of female fertility. While the frequency of nursing remained constant throughout the 6-week observation period, decreasing amount of time spent nursing generally preceded the onset of paternal carriage. Decreasing nursing duration was not associated with the occurrence of postpartum ovulation. Some mothers frequently acted aggressively toward the infant during the period of first mother-to-father transfer of the infant, while other mothers did not. There is no correlation between the interval to the first transfer and the period to postpartum ovulation. We validated urinary cortisol as a measure of stress and defined the duration of its poststress elevation as approximately 3 hr. There is no consistent relationship between female behavior and endocrine state, or male cortisol values and the onset of infant carrying by fathers. During the peritransfer phase, no significant change in cortisol concentration occurred, while the pre-, peri-, and postovulatory phases appeared to be reflected in urinary cortisol output by some males. Based on these results, we propose an explanatory model for the causal dynamics of infant care in pairs of Callimico.The model stresses the importance of a high reproductive rate to male and female reproductive strategies.     

Reactions of nuclear-family–reared rhesus macaques to the births of younger siblings

A group of juvenile rhesus macaques (Macaca mulatta) living in a nuclear-family laboratory environment was studied to determine their responses to the births of siblings. The frequencies of interactions with family members (mothers, fathers, and new siblings) and nonfamily (peers, unrelated infants, and unrelated adults) were studied over both the year preceding and the year following sibling birth. The frequencies of specific behaviors in each of those interactions and the frequencies of interactions in each area of the nuclear-family unit (home cage, play area, or other families' cage) were also examined. After new siblings arrived, several measures of interactions with mothers, fathers, and new siblings increased significantly; by contrast interactions with peers decreased substantially over the post-birth year. Although the frequency of interactions in home cages remained stable over the 2-year period, interactions outside of the subjects' home cages decreased significantly after siblings were born. An additional subject group whose mothers became pregnant but failed to deliver viable offspring showed no significant changes in total levels of interactions with peers; they did, however, exhibit increases in some interactions with unrelated infants and adults. Female juveniles interacted with new siblings significantly more often than did males when siblings were less than 6 months old, but as siblings grew older (6–12 months), females' levels of interaction with them fell to a level equal to that of males. In the nuclear-family social structure, the birth of a sibling resulted in an increased emphasis on family interactions at the expense of peer interactions.     

Pre- and postpartum sex steroids in female marmosets (Callithrix kuhlii): is there a link with infant survivorship and maternal behavior?

Recent studies in primates have suggested that pre- and peripartum sex steroid hormones may be important determinants of maternal behavior and motivation, since higher levels of prepartum estrogen are associated with maternal competency and infant survivorship. To test the cross-species generality of this finding, we monitored excreted profiles of estradiol (E(2)), progesterone metabolites (pregnanediol glucuronide; PdG), and E(2):PdG ratios throughout pregnancy in black tufted-ear marmosets (Callithrix kuhlii). Additionally, we wanted to determine the extent to which variability in maternal carrying effort was related to hormonal factors and relative levels of maternal experience. For six females, hormonal profiles were determined by enzyme immunoassay for two pregnancies, one in which infants survived at least 2 weeks postpartum and one in which infants did not survive. Our within-subjects analyses revealed significant differences in mean prepartum E(2) levels for females in the different infant survival conditions. In contrast to previous findings, however, females exhibited significantly higher prepartum E(2) levels when their infants did not survive a minimum of 2 weeks postpartum, relative to when their infants did survive. Maternal carrying effort was also negatively and significantly correlated with prepartum E(2) levels. Unlike previous reports in callitrichid primates, then, our data suggest that high concentrations of prepartum E(2) in callitrichid primates are not necessarily associated with competent maternal behavior and may instead be associated with poor infant survivorship and inadequate maternal care. Further, our results appear to be convergent with research focusing on human mothers and may represent a common underlying mechanism linking prepartum estrogen and postpartum affect and behavior in some primates.     

Carrying behaviour in captive and wild marmosets (Callithrix jacchus): A comparison between two colonies and a field site

Data on callitrichids infant carrying is highly variable, and there is some disagreement over the relative involvement of different group members. Considering that variation may result from different social and environmental conditions it is important to compare data from different environments. The purpose of this study was to compare infant carrying in 11Callithrix jacchus groups living in two colonies, in the UK and Brazil, or in a field site in the northeastern Brazil. No differences were found in the amount of time that infants were carried, in the three environmental conditions, during weeks 1 to 4, 7, and 10. Fathers and mothers carried infants for equivalent amounts of time in the three conditions, but helpers from natural groups carried infants more than their captive counterparts. In general, adult helpers carried infants more than subadults and juveniles. The results suggest that carrying is a stable feature inCallithrix jacchus groups, but there is a trend suggestive of an extended carrying period in natural groups. Mothers behaviour were remarkably stable, but fathers behaviour, although comparable, was more conspicuous in captivity than in the field, what may be attributed to paternity certainty. Finally, the greater participation of field helpers in carrying is considered as deriving mostly to age of helpers than to group size.     

Parturition and perinatal behaviour in captive cotton-top tamarins (Saguinus oedipus)

Fourteen births to seven female cotton-top tamarins in a successful breeding colony were observed. All births occurred between 17:50 and 20:40. Behavioural changes indicating the onset of labour are described. Delivery was usually accomplished rapidly, with short intervals between successive infants. One suspected and one verified breech presentation occurred; these deliveries were accompanied by a marked increase in the duration of the interval between infants, and one infant apparently died during expulsion. All other presentations seen were vertex occiput posterior. Fathers, and sometimes older offspring of both sexes, frequently shared with the mother in eating the placenta. Carrying of infants by individuals other than the mother was rare in the hour after birth, and was usually confined to fathers. One primipara rejected her second-born infant, but all other parents showed competent parental behaviour from birth onwards. The results are compared to data from other primates, and their relevance to the successful breeding of this species is discussed.     

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.     

Variable infant care contributions in cooperatively breeding groups of wild saddleback tamarins

Among non-human primates, alloparental infant care is most extensive in callitrichines, and is thought to be particularly costly for tamarins whose helpers may suffer increased energy expenditure, weight loss, and reduced feeding time and mobility. The costs and benefits of infant care likely vary among group members yet very few wild studies have investigated variable infant care contributions. We studied infant care over an 8-month period in four wild groups of saddleback tamarins in Bolivia to evaluate: (a) what forms of infant care are provided, by whom, and when, (b) how individuals adjust their behavior (activity, vigilance, height) while caring for infants, and (c) whether individuals differ in their infant care contributions. We found that infant carrying, food sharing, and grooming varied among groups, and immigrant males—those who joined the group after infants were conceived—participated less in infant care compared to resident males. Adult tamarins fed less, rested more, and increased vigilance while carrying infants. Although we did not detect changes in overall activity budgets between prepartum and postpartum periods, tamarins spent more time scanning their environments postpartum, potentially reflecting increased predation risk to both carriers and infants during this period. Our study provides the first quantitative data on the timing and amount of infant carrying, grooming, and food transfer contributed by all individuals within and among multiple wild groups, filling a critical knowledge gap about the factors affecting infant care, and highlighting evolutionary hypotheses for cooperative breeding in tamarins.     

High paternal testosterone may protect against postpartum depressive symptoms in fathers,but confer risk to mothers and children

Following the birth of an infant, decreases in testosterone and increases in depressive symptoms have been observed in fathers. Paternal testosterone may reflect fathers' investment in pair-bonding and paternal caregiving and, as such, may be associated with maternal and familial well-being. This study tests associations between paternal testosterone, paternal and maternal postpartum depressive symptoms, and subsequent family functioning.Within 149 couples, fathers provided testosterone samples when infants were approximately nine months old and both parents reported on postpartum depressive symptoms at two, nine, and 15 months postpartum. Fathers with lower aggregate testosterone reported more depressive symptoms at two and nine months postpartum. Mothers whose partners had higher evening testosterone reported more depressive symptoms at nine and 15 months postpartum. Maternal relationship satisfaction mediated this effect, such that mothers with higher testosterone partners reported more relationship dissatisfaction, which in turn predicted more maternal depressive symptoms. Higher paternal testosterone and paternal depressive symptoms at nine months postpartum each independently predicted greater fathering stress at 15 months postpartum. Higher paternal testosterone also predicted more mother-reported intimate partner aggression at 15 months postpartum. In addition to linear relationships between testosterone and depression, curvilinear relationships emerged such that fathers with both low and high testosterone at nine months postpartum reported more subsequent (15-month) depressive symptoms and fathering stress.In conclusion, whereas higher paternal testosterone may protect against paternal depression, it contributed to maternal distress and suboptimal family outcomes in our sample. Interventions that supplement or alter men's testosterone may have unintended consequences for family well-being.