Social dynamics and individual plasticity of infant care behavior in cooperatively breeding cotton‐top tamarins

Individual variation in infant caretaking behavior is prevalent among marmoset and tamarin monkeys. Although most group members participate in infant care, the timing and amount provided differs greatly. In this study, we quantified general trends in infant carrying behavior by using a longitudinal database that included 11 years of instantaneous scan observations following 80 births of cotton‐top tamarins. Using detailed focal observations on a subset of the same families (10 births) we identified influences that affected expression of infant care at the group and individual levels. Fathers were the primary carriers and paternal carry time gradually decreased with increasing infant age. Paternal carry time also decreased significantly with an increasing number of older sibling helpers. Most fathers began to carry on the first day postpartum. However, we report circumstances in which fathers delayed carrying until almost a month postpartum. Fathers retrieved infants the most, although adult brothers' rates of retrievals peaked and surpassed fathers' rates during week 4 postpartum. Fathers delayed rejection of infants until week 4, whereas mothers rejected infants immediately and throughout the eight weeks. Nonetheless, infants climbed onto their mothers more than onto any other family member. Mothers showed a high initial investment in carrying during the first two weeks, decreasing quickly thereafter. Maternal contributions to infant carrying remained low and relatively consistent regardless of group size. However, mothers dramatically increased their infant carrying behavior in families in which fathers were absent. Older siblings cared for infants more than did younger siblings, and brothers retrieved and carried infants more than did sisters. Individual expression of infant care changed to accommodate infant needs and changed according to varying social dynamics and circumstances across litters. Am. J. Primatol. 72:296–306, 2010. © 2009 Wiley‐Liss, Inc.     

Effect of the enclosure on carriers' body weight loss in the cotton-top tamarin (Saguinus oedipus)

Infant carrying in cotton-top tamarins is a costly activity that results in weight loss by the fathers and helpers. However, to date, measures of carrying costs have been obtained in small indoor enclosures. We studied body weight changes in adult and subadult individuals from eight large groups (n > 5) for 9 weeks after the birth of infants. Four groups were housed in large indoor/outdoor enclosures (42 m(2) x 3.3 m high), and four were housed in small indoor enclosures (12 m(2) x 2.4 m high). All of the individuals were weighed regularly at least three times a week. Reproductive males lost more weight in the big indoor/outdoor enclosures (mean=6.51%) than in the small indoor ones, as did male adult helpers (mean=5.59%) and female adult helpers (mean=4.4%). Still-growing subadult individuals also lost weight in the big indoor/outdoor enclosures (mean=3.17%), although the differences did not reach significance (P=0.07). These results support the hypothesis that cotton-top tamarins living in more natural settings experience higher weight loss than those housed under less-natural conditions.     

Costs of Caregiving: Weight Loss in Captive Adult Male Cotton-Top Tamarins (Saguinus oedipus) Following the Birth of Infants

We examined changes in weight for 10 captive adult male cotton-top tamarins (Saguinus oedipus) from before the birth of infants through the first 16 weeks of infant life. Compared to before birth, males weighed significantly less in Weeks 1–4, 5–8, and 9–12 following the birth. Weights in Weeks 13–16 did not differ significantly from prebirth weights. Maximum weight loss for individual males ranged from 1.3 to 10.8% of prebirth body weight. Males in groups with fewer helpers lost significantly more weight than ones in groups with more helpers. For the 3 males that had no helper other than their mates, weight loss was particularly striking, ranging from 10.0 to 10.8% of their prebirth body weight. These results suggest that caring for infants is energetically costly, and that in this cooperatively breeding species, the presence of more individuals to share the burden of infant carrying reduces the cost to individual caregivers.     

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.     

The benefits of helpers: Effects of group and litter size on infant care in tamarins (Saguinus oedipus)

The Callitrichidae (marmosets and tamarins) typically give birth to twins, and infant care is shared by all group members. The potential benefits to callitrichids of having helpers were investigated in a study of 21 captive cotton-top tamarin (Saguinus oedipus) infants, living in groups with two to 12 older members. Time carried and suckled and amount of food received from other family members were recorded for each infant during the first 12 weeks of life. The results showed that infants in larger groups were carried more and received more food than those in smaller groups. Twin infants in larger families were less likely to be on the same carrier. Singleton infants were carried more than twins but did not receive more food. On average, individual caretakers in larger groups carried less and shared less food with infants than those in smaller groups. When parental contributions to care were analyzed, no effects of group size were found on mothers' contributions to carrying or food sharing, but fathers in larger groups both carried infants less and shared less food with them. There appear to be several benefits of a communal rearing system to cotton-top tamarins. 1) Infants may receive more care in larger families, thus increasing their chances of survival. 2) The burden of care is spread over several animals, reducing the costs to a given individual. 3) The parents, particularly fathers, may benefit most from reducing the costs of investing in the present litter and increasing their ability to invest in future litters.     

Prolactin levels of fathers and helpers related to alloparental care in common marmosets, Callithrix jacchus

Previous studies have suggested that prolactin may play a role in regulating allocare behaviour in cotton-top tamarins, Saguinus oedipus. In this study, we investigate the prolactin profile of 3 groups of captive common marmosets, Callithrix jacchus. Carrying behaviour in this species was observed after parturition. Prolactin assays of blood samples of both fathers and helpers (sub-adult non-fathers) in 3 family groups were taken for 8 weeks before and after birth of the infants. The after-birth condition was divided into 2 groups: carrying and non-carrying animals. The results suggest a relationship between prolactin levels and allocare behaviour, with carrying behaviour being associated with increased prolactin in both fathers and helpers. This suggests that extra prolactin is produced in response to physical contact, and may be associated with carrying behaviour. Also, prolactin production may be related to learning parental skills in Neotropical primates.     

Infant Carrying Behavior in Callitrichid Primates: Callithrix and Leontopithecus

Care of offspring by individuals other than the mother is ubiquitous in callitrichid primates. In spite of its widespread occurrence, however, there is considerable taxonomic variation in the timing and intensity of parental effort by breeding males and nonbreeding juvenile group members. These differences may be attributable to generic and specifies differences in the costs of reproduction for females or in ecological constraints on travel and foraging. We present data on patterns of infant carrying in social groups of two taxa of callitrichid primates (Callithrix and Leontopithecus) throughout the first 3 months of infant life. We evaluated patterns of care in small groups (two or fewer juvenile or subadult helpers) and in large groups (three or more helpers in addition to the breeding adult male and female). Group size had little effect on levels of maternal carrying effort in either marmosets or lion tamarins, and mothers ceased carrying infants by 3 months of age. Carrying efforts by fathers were significantly reduced in groups with many helpers relative to small groups. Helpers carried at consistent rates during the second and third months of infant life in Leontopithecus, while in Callithrix, carrying by helpers peaked during the second month. These results suggest that if helpers reduce energetic demands on lactating females, the mechanism by which helpers reduce these burdens is independent of maternal carrying effort.     

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.     

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.     

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.     

Infant-care Behavior of Non-reproductive Helpers in a Communal-care Primate,the Cotton-top Tamarin (Saguinus oedipus)

Infant-care behavior patterns of captive cotton-top tamarins were examined to assess factors defining participation by non-reproductive helpers. The time spent carrying infants and characteristics of infant transfers were examined for 47 helpers in a total of 18 groups. We predicted that age, previous experience, and carrying opportunity would all affect participation of non-reproductive helpers. Our results confirm that carrying by non-reproductive helpers was related to age, with older helpers carrying more often. However, this difference declined with increasing infant age, suggesting that body size of the carrier was not the only factor determining participation in carrying. When observations were classified relative to type of interaction with infants, older juveniles were found to both investigate and harass infants more often than subadults or younger juveniles. There was no effect of gender on carrying. The carrying behavior of subadults was not affected by their previous experience; that is, subadults with no previous exposure to infants carried as often as those with previous experience. Inter-individual variation among helpers was high; within 11 twin litters of helpers, one animal usually carried significantly more than the other.     

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.     

Change in weight‐for‐length status during the first three months: Relationships to birth weight and implications for metabolic risk

Weight‐for‐length during the early postnatal period is a critical predictor of subsequent body composition and metabolic risk. This study was designed to analyze change in weight‐for‐length status according to birth weight in early infancy. Data were collected for 267 infants enrolled in the Jackson County Women, Infants, and Children (WIC) program. Postnatal measurements were collected at a clinic visit between birth and 12 weeks of age (mean = 5.7 weeks). Changes inWHO z‐scores (weight, length, weight‐for‐length) between birth and the clinic visit were calculated. Infants were classified as exclusively breastfed or as formula‐fed. Ethnicity was coded as Hispanic or non‐Hispanic. Infants were classified based on birth weight z‐score as lower ( +1 SD). Multiple regression models tested birth weight, demographic factors, and feeding as predictors of z‐score change measures. Demographic factors and feeding were also tested as moderators of the effects of birth weight. Lower birth weight infants displayed an increase in weight‐for‐length z‐score between birth and the clinic visit. Change in weight‐for‐length was associated with significant increase in weight z‐score but not in length z‐score. Higher birth weight predicted decrease in weight and length z‐scores but did not predict change in weight‐for‐length. Hispanic ethnicity predicted decrease in length z‐score and increase in weight‐for‐length z‐score but did not moderate effects of birth weight. Increase in weight‐for‐length among lower birth weight infants and persistence of high weight‐for‐length among higher birth weight infants may reflect phenotypic adjustments that are maladaptive in adverse dietary environments. Am J Phys Anthropol, 2013. © 2012 Wiley Periodicals, Inc.     

Influence of maternal pregravid weight, height and body mass index on birth weight of male and female newborns

The study included 2300 healthy couples and their healthy newborns delivered vaginally from singleton, normal term (37-42 weeks) pregnancies in Sibenik, Zadar and Split (Croatia). Both fathers and mothers of male newborns were older and had a higher weight than those of female newborns (p < 0.05). Gestational age and birth weight were higher in male than female newborns (p < 0.001). Increasing maternal pregravid weight led to increasing birth weight of both male and female newborns (p < 0.001). Furthermore, increasing maternal height and body mass index resulted in increasing birth weight of male and female newborns (p < 0.001). Thus, the fathers and mothers of male infants were older than those of female infants (p < 0.05), and increasing pre-gravid body weight, body height and body mass index were associated with a higher birth weight in both male and female newborns.     

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.     

The costs of infant carrying in captive cotton-top tamarins

Marmosets and tamarins have a communal rearing system in which all group members help to care for the twin infants characteristic of this family of primates. Helpers are likely to incur time and energy costs by contributing to infant care. Predictions that cotton-top tamarin (Saguinus oedipus) helpers would change their behavior when carrying infants because of reduced mobility and/or a need for increased vigilance were tested in a captive colony. Tamarins carrying an infant spent significantly less time feeding, foraging, moving, or engaging in social activities such as grooming than they did when not carrying. Frequencies of scratching, autogrooming, and scent marking were significantly reduced in carriers, suggesting that their mobility was reduced. However, carriers were significantly less likely to be vigilant (measured by direction of gaze) than when not carrying. Further observations showed that carriers spent more time in concealed areas than they did when not carrying and were probably therefore adopting a cryptic strategy to reduce predation risks to themselves and to infants. These results demonstrate that tamarin helpers pay costs by carrying infants. Some possible compensating benefits are indicated.     

Maternal and paternal controlling feeding practices: reliability and relationships with BMI

Objective: This study aimed to examine the interrelationships between mothers' and fathers' reports on the child‐feeding questionnaire (CFQ), the BMI of parents and their children, and observations of parents' controlling feeding practices at mealtimes. Methods and Procedures: Twenty‐three mothers and twenty‐three fathers of children aged between 18 and 67 months reported on their child‐feeding practices, on their child's height and weight, and were observed during a normal family mealtime at home. Results: No associations were found between mothers' reported and observed feeding practices. Fathers' reported pressure to eat and restriction were associated with more controlling observed mealtime feeding practices. Mothers and fathers did not significantly differ in their reported or observed child‐feeding practices. Children's BMI was not related to maternal or paternal reported or observed feeding practices. More mealtime pressure was observed in parents with a higher BMI. Discussion: Fathers' self‐reports of their mealtime practices are reliable. Mothers' feeding practices may differ when fathers are present and further work should examine mothers at mealtimes with and without fathers. Although children's BMI was not related to parents' use of reported or observed control, parents with a higher BMI were more controlling, highlighting the importance of considering parents' own weight in future studies.     

Why do cotton‐top tamarin female helpers carry infants? A preliminary study

Shortly after giving birth, cotton-top tamarin mothers frequently attack the eldest female helpers [Snowdon et al., American Journal of Primatology 31:11-21, 1993]. Sometimes this aggression leads to the eviction of the eldest daughters from their natal groups 3-4 months after the birth of infants [Price & McGrew, Folia Primatologica 57:16-27, 1991]. We propose that daughters, during the act of carrying infants, may receive less aggression from mothers than when they are not carrying. On the other hand, given that mothers benefit from having others carry their infants, overall aggression received by female helpers from their mothers might be lower in those female helpers with a larger relative contribution to this activity. Four groups were observed during the first 9 weeks following the birth of infants, and aggression received was recorded for symmetrical as well as nonsymmetrical interactions. We found a positive correlation between contribution to infant carrying of female helpers and the overall aggression received from their mothers. Furthermore, the two eldest daughters with highest values of carrying contribution were evicted from their natal groups 3-4 months after the birth of infants. Although mothers do not appear to be more tolerant of female helpers that contribute the most to infant carrying, daughters do benefit from reduced aggression during the act of carrying, and remain in their natal group during the time period when infants must be carried.     

Preparental hormone levels and parenting experience in male cotton-top tamarins, Saguinus oedipus

Male cotton-top tamarins, Saguinus oedipus, display hormonal changes associated with parenting prior to the birth of their infants. Here we examined the hormonal changes that occurred in experienced and inexperienced fathers during the postconception period, prior to the birth of infants. Noninvasive techniques were used to collect urine from 10 male cotton-top tamarins (5 experienced and 5 inexperienced breeders) three times weekly during the 6-month gestation period. Samples were analyzed for prolactin, testosterone, dihydrotestosterone (DHT), and cortisol, averaged by gestational month. Experienced males showed elevated prolactin during the mate's 3rd gestational month, and the elevation correlated with the number of infants surviving from the previous birth (0, 1, and 2) but not with outcome of the current pregnancy. However, an experienced male with no infants present still showed elevated prolactin and some inexperienced males showed elevated prolactin just before parturition, suggesting noninfant cues are also important. While prolactin levels were influenced by the male's prior infant experience, testosterone levels did not differ between experienced and inexperienced males. Testosterone levels were significantly elevated for all males during the 3rd, 4th and 5th months but had no relationship with number of infants present or with outcome of current pregnancy. DHT decreased during the second half of pregnancy compared with testosterone but this finding was not consistent for every male. No significant changes occurred in cortisol levels. These results suggest that infant-rearing experience affected the hormonal responsitivty of the male to his mate's current pregnancy.