The Role of Non-reproductive Helpers in Infant Care in Captive Callithrix jacchus

Callitrichids have been proposed as communal breeders, with non-reproductive animals acting as helpers. Reports in the literature attest to the high variability in the behaviour of helpers. The present study assessed four proximate factors involved in helping in captive Callithrix jacchus: age, gender and experience of helpers and composition of their groups. Forty-eight helpers from 15 families from Natal (Brazil) and Reading (UK) colonies were observed during the first 4 weeks of life of new-born twins. Infant carrying, transfers and retrieval, and duration of carrying bouts were registered. Results showed that the presence of helpers decreased the costs of infant carrying, with a negatively significant correlation between group size and mean percentage of carrying. Age, but not gender, was a significant factor for infant carrying, transfers and retrieval, and mean duration of carrying bouts, with older helpers contributing more than younger ones. Singletons and oldest non-reproductive offspring carried infants more, and longer, than twins and offspring with older siblings present in the group. Experience decreased motivation and actual carrying time, but not to a significant level. Age, experience and group composition appeared important factors in the display of infant care by helpers in captive Callithrix jacchus.     

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.     

Long-term study of infant-carrying behavior in captive common marmosets (Callithrix jacchus): Effect of nonreproductive helpers on the parents' carrying performance

Infant-carrying behavior in four families ofCallithrix jacchus was investigated over a period covering six to eight litters. We evaluated the effect of the total number of helpers and the number of adult helpers on the parents' carrying performance for the total carrying period and for three age stages of the infants. The carrying performance of the parents reached an asymptote beginning with litters 3 to 5. In two groups, the carrying performance of the parents was significantly negatively correlated with group size. However, considerable differences existed within each group and between the groups. The mother was the primary caregiver in the early weeks of the infants' lives. In this phase the helpers' contribution to carrying was less than might be expected. The relief of the parents from infant-carrying was greatest when the infants were 4 to 7 weeks old. Breeding males benefited most and from every helper, while breeding females benefited most from adult helpers, i.e., the carrying performance of the breeding female was considerably reduced until the respective group had grown to 8 to 10 members (infants not included). This group size is considered to be ideal for maximal relief of the parents from infant carrying. An increasing number of adult nonreproductive helpers (>4 or 5) does not induce a further reduction of the parents' carrying performance. Infant-rearing experience of nonreproductive helpers seems to be more important for the parents' and, especially, the breeding female's relief from infant-carrying than the overall number of helpers is. The data also strongly evidence that a group member's participation in infant-carrying is influenced by housing conditions and the demographic history of the group.     

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.     

Social relationships and individual contribution to cooperative behaviour in captive common marmosets (Callithrix jacchus)

The social relationships between the members of a family consisting of eight captive common marmosets (Callithrix jacchus) are here examined, as well as the participation of individual family members in infant carrying and defensive behaviour against non-related intruders (adolescent males). Within the social relationships, a clear division of the family into three subgroups (parents, adult offspring, non-adult offspring) could be determined, whereby the adult offspring, especially with respect to the parents, occupy a peripheral position. In the types of cooperative behaviour examined here, substantial participation in infant carrying could be observed in only four family members (parents, adult son, one subadult daughter), and in defence against intruders in only two family members (adult son, one subadult daughter). Participation in infant carrying remained stable throughout the study period. Conversely, individual changes in participation in defence against intruders could be determined, dependent upon the presence of infants carried. The advantages and disadvantages of social substructuring observed are discussed here, in particular the peripheral position of adult offspring, possible connections in individually varied participation in cooperative behaviour, and possible regulative mechanisms. In view of past studies on cooperative behaviour among marmosets, it is here presumed that pronounced individual differences result from a division of labour within the family with respect to various aspects of cooperative behaviour.     

Family composition and the characteristics of parental care during the nursing phase of captive common marmosets (Callithrix jacchus)

Cooperative care of the young by the father, older siblings, and unrelated group members is observed in a number of species, but inCallithrix jacchus parental care by the father is considered to be part of the reproductive behavior of the species. Nevertheless, the way the presence of potential helpers influences the costs of caring for the parents is not well understood. In this study we describe the suckling phase of youngC. jacchus, in families with and without older siblings, assessing the effect of siblings on the amount of care given by the father and mother. Six family groups were observed: three consisting of the mated pair and two newborn infants, and three with one or two additional sub-adult siblings. Our results suggest that the presence of older siblings as helpers affects the parents' participation in caregiving by altering maternal investment through the control of nursing and by reducing the costs of carrying for the father.     

Infant survival and number of helpers in captive groups of common marmosets (Callithrix jacchus)

In a colony of captive marmoset monkeys (Callithrix jacchus), the survival rate of infants up to the age of 90 days after birth was analyzed with special reference to the number of members in the group. The number of group members (newborns excluded) varied between two (parents only) and 18 (parents plus non-reproductive helpers); the number of adult group members varied between two and 15. Five hundred ninety-two live-born, parent-reared infants of 263 litters from 56 breeding females were included in the analysis. The greatest reproductive success was observed in groups of ten to 11 members or four to five adults, including the parents. However, the survival rate was fairly constant over group size at approximately 80% of an expected maximum value and no significant correlation was observed between the total number of group members and infant survival rate, or between the number of adult members and infant survival. While helpers may be necessary to increase the survival rate of infants in wild groups, help of non-reproductive animals is not required in captivity, where energetic demands are comparatively low and ecological constraints absent. Under laboratory conditions the parents' skill in infant handling and the mother's physical condition, i.e., the ability to provide enough milk for the infants, is likely to be the most important factor for infant survival. © 1993 Wiley-Liss, Inc.     

Infant-caregiver interactions in common marmosets (Callithrix jacchus): Consequences of rejections and rub-offs of infants by caregivers

Interactions between common marmoset infants (Callithrix jacchus) and their fathers, mothers, older siblings and twins were examined in captive family groups. The aim was to record infants' behaviour after being rejected in their attempts to get on to caregivers and after being rubbed off by caregivers who had been carrying them. The results showed that infants' behaviour differed according to which caregiver was involved and that behaviours following rejections differed from those following rub-offs. These differences in infants' behaviour had been predicted from previous work which showed that caregivers have a limit to the amount of time they are prepared to devote to infants and that different caregivers give different amounts of care to infants of specific ages.     

Maternal care and infant development in <Emphasis Type="Italic">Callimico goeldii</Emphasis> and <Emphasis Type="Italic">Callithrix jacchus</Emphasis>

Callimico goeldii gives birth to single offspring, whereas other callitrichids, including Callithrix jacchus, twin. This study compares maternal effort and infant development in C. goeldii and C. jacchus; it is the first study to look at nursing frequency. Infants were observed from birth for 7 weeks in two captive groups each of C. goeldii and C. jacchus. C. goeldii mothers physiologically invested the same or less than C. jacchus mothers. C. goeldii mothers gained the same amount of weight during pregnancy in absolute terms as did the smaller C. jacchus. This results in a smaller gain in proportion to maternal weight but an equivalent proportional gain on a per fetus basis. C. goeldii mothers nursed their infants less based on duration of nursing bouts compared with C. jacchus mothers. C. goeldii mothers transported their infants exclusively through the first 2 weeks of life, which is longer than C. jacchus mothers, who exclusively transported infants only during the first week of life. As maternal infant carriage declined, other group members transported offspring in both species. C. goeldii infants engaged in independent locomotive sequences later in development and tasted solid foods less frequently than C. jacchus infants when compared at equivalent ages. A single, opportunistic milk sample obtained from a C. goeldii mother when her infant was 48 days old indicates that C. goeldii milk contains gross energy from crude protein within the range of variation observed in Callithrix milk. Despite the similarities in milk quality and prenatal effort in individual fetuses, C. goeldii infants gain weight faster from 0 to 18 months than do C. jacchus infants. A reduction in litter size allows C. goeldii mothers to spend more time carrying their infant and to delay weaning, thereby allowing accelerated infant and juvenile growth rates compared with C. jacchus.     

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.     

Interactions between infant growth and survival: Evidence for selection on age-specific body weight in captive common marmosets (Callithrix jacchus)

The objective of this study is to investigate factors influencing infant survival in captive common marmosets. We investigated the influence of age-specific weight, litter size, caging, and the presence of helpers on survival to 6 months of age in 189 Callithrix jacchus infants. Infant survival was analyzed using Cox Proportional Hazards regression, and fitness functions were plotted to explore the relationship between survival and growth. Results indicate that weights at birth and 120 days significantly affect future survival probability. Litter size significantly influences survival prior to 60 days of age with larger litters having poorer survival. Males and females did not have significantly different survival and the presence of helpers in the group did not influence survival probability. Patterns of survival with respect to age-specific weights suggest stabilizing selection on birth weight and directional selection on weight at 120 days of age. Am. J. Primatol. 42:269–280, 1997. © 1997 Wiley-Liss, Inc.     

Interactions between parents and infants,and infants-father separation in the common marmoset (Callithrix jacchus)

The New World monkey,Callithrix jacchus, diversely from most Old World primates, shares infant care among all family members. This paper intends to describe a pattern of infant care in the common marmoset, and to verify if the infant-father separation induces a depression reaction, such as found in other separation studies. In Experiment 1, 11 families (mother, father, and twin newborn infants) ofCallithrix jacchus were observed from 1st to 36th days of infants' life. It was noted that infants were carried most of the time in the beginning of life, and that from the 4th day on this care came mostly from the father. In Experiment 2, nine families were divided in three separation groups (15, 30, and 45 days of infants' life). Each group had a control and two experimental families. Removal of the father was done for three days, beginning at the indicated infants' ages. Results showed that upon removal of the father, the mother assumes the infants' care, and no depression reaction appeared.     

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.     

Balancing contest competition,scramble competition,and social tolerance at feeding sites in wild common marmosets (Callithrix jacchus)

Models of primate sociality focus on the costs and benefits of group living and how factors such as rank, feeding competition, alliance formation, and cooperative behavior shape within‐group social relationships. We conducted a series of controlled field experiments designed to investigate how resource distribution (one or three of four reward platforms) and amount of food on a reward platform affected foraging strategies and individual feeding success in four groups of wild common marmosets (Callithrix jacchus) living in the Caatinga of northeastern Brazil. At our field site, common marmoset groups are characterized by a single breeding female who can produce twin litters twice per year, strong social cohesion, and cooperative infant care provided principally by several adult male helpers. We found that except for the dominant breeding female, rank (based on aggression) was not a strong predictor of feeding success. Although the breeding female in each group occupied the highest rank position and obtained the greatest daily feeding success, all other group members, including adults and juveniles experienced relatively equal feeding success across most experimental conditions. This was accomplished using a balance of behavioral strategies related to contest competition, scramble competition (associated with a finder's advantage), and social tolerance (sharing the same feeding platform). Based on these results, the social structure of common marmosets is best described as “single female dominance,” with the breeding female maximizing food intake needed to offset the energetic costs associated with reproductive twinning and the ability to produce two litters per year. Cooperative infant caregiving, in which the number of helpers is positively correlated with offspring survivorship, requires a set of behavioral strategies that serve to reduce contest competition and promote prosocial behaviors at feeding sites.     

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.     

The caregiving/care-seeking balance in captive common marmosets (Callithrix jacchus)

A hypothesis to explain differences in infant social development in species with multiple caregivers is described. The hypothesis states that the distribution of an infant's time and activities amongst the individuals in its group is determined by the balance between the relative amounts of care-seeking by the infant and caregiving by the other members of the group. This generates several predictions that are investigated by experimentally reducing the care available to a group of infant common marmosets (Callithrix jacchus), and comparing their interactions with caregivers with those of a control group of infants that experienced normal levels of care. The results bear out several of the predictions. Infants receiving less care than usual spend less time in non-care-seeking activities and there are some increases in care-seeking behaviour. Infants continue to seek care differentially from different caregivers, and no compensation among caregivers in their behaviour towards infants is found.     

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.     

Social implications of gummivory in marmosets

Gummivory or exudate feeding is a major dietary specialization which has received relatively little attention in the literature. While plant exudates contribute to the diet of many primate species, we suggest that the callitrichid species Cebuella pygmaea and Callithrix jacchus are obligate exudate feeders under free-ranging conditions. Callithrix jacchus provides an excellent model for examining the effects of exudate feeding and foraging upon social behavior, since other callitrichid species of similar body size do not share this dietary specialization. We review the effects of exudate foraging on specific social behaviors observed both in field and laboratory populations of C. jacchus. By comparing this species to closely related species, exudate foraging is seen to (1) be retained under laboratory conditions, (2) increase the frequency of territorial marking behavior while decreasing the frequency of overt aggression in males, (3) decrease the duration of infant care, and (4) increase the number of nonadults in social groups but not affect group size. The evidence presented supports the hypothesis that the consequences of exudate foraging in C. jacchus are fundamental and socially complex. © 1994 Wiley-Liss, Inc.     

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.