International Journal of Primatology, Vol. 18, No. 6, 1997 Infant Carrying Behavior in Callitrichid Primates: Callithrix and Leontopithecus Cristina V. Santos,1-2 Jeffrey A. French,2-3 and Emma Otta1 Received October 29, 1996; accepted May 21, 1997 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. KEY WORDS: Callithrix; Leontopithecus; cooperative rearing; infant care; parental behavior. 'Departamento de Psicologia Experimental, Universidade de So Paulo, So Paulo, SP, Brazil. 2Department of Psychology and Nebraska Behavioral Biology Group, University of Nebraska at Omaha, Omaha, Nebraska 68182. 3To whom correspondence should be addressed at Department of Psychology, University of Nebraska at Omaha, Omaha, Nebraska 68182-0274. 889 0164-0291/97/1200-0889$12.50/0 O 1997 Plenum Publishing Corporation 890 Santos, French, and Otta INTRODUCTION Communal care of dependent offspring by individuals other than the mother is a hallmark of callitrichid primate social biology. Indeed, some have considered communal rearing to be one of the major defining features of callitrichid social systems (Goldizen, 1987; Ferrari and Lopes-Ferrari, 1989; Tardif et al, 1993). Hypotheses accounting for the existence of com- munal care by alloparents in these species have typically relied on arguments based on energetics and the assumption of high costs of repro- duction for breeding females (Goldizen, 1990). Aspects of the reproductive biology of callitrichids that contribute to the high cost of reproduction in- clude the production of twin births with a high neonate maternal weight ratio (Leutenneger, 1973; Ford and Davis, 1992) and, in some species, an immediate postpartum estrus with little or no lactational suppression of fertility (French, 1983; Ziegler et al, 1990). According to the reproductive energetics account, alloparents, which are either retained in or recruited into the group, have several possible effects on the overall reproductive effort of the breeding female. First, al- loparents may reduce the magnitude of parental effort by the breeding female: effort expended specifically on parental behavior (Westneat and Sherman, 1993). This has been traditionally assessed in callitrichid primates measuring the impact of alloparents on energetically demanding tasks such as infant carrying and provisioning of solid food to infants (Feistner and Chamove, 1986; Tardif et al, 1986; McGrew, 1988). Second, the presence of alloparents may increase the opportunity for the breeding female to en- gage in activities such as foraging and feeding, which may increase her likelihood of success in future breeding attempts: somatic effort (Westneat and Sherman, 1993). Price (1992a) hinted at the significance of long-term benefits of alloparents for a breeding pair, and studies on some free-ranging populations (Garber et al, 1984; Baker, 1991) support the notion that groups with more potential alloparents have greater reproductive success than groups with fewer alloparents. Indeed, Goldizen (1987; Terborgh and Goldizen, 1985) suggested that lone breeding pairs of tamarins without al- loparental resources would be unable to rear offspring successfully. However, this hypothesis has not been widely assessed in free-ranging populations, and there is at least one demonstration that helpers may not be critical for offspring survival in captive groups (Rothe et al, 1993). In spite of the ubiquity of communal breeding and alloparental care in the social profile of marmosets and tamarins, there is considerable vari- ability among species in the distribution of parental care among group members. For example, golden lion tamarin infants are first carried by in- dividuals other than the mother at 16 days postpartum (Hoage, 1982). In Infant Carrying in Callitrichids 891 other callitrichid taxa, nonmothers begin to carry infants within the first week, sometimes on the first day postpartum [Saguinus (Cleveland and Snowdon, 1984; Tardif et al, 1990), Callithrix (Ingram, 1977), Cebuella (Christen, 1974)]. The proportion of time that offspring are carried at 8 weeks of age also varies across taxa: Callithrix. jacchus infants are effectively independent of carriers by 8 weeks, while infant Saguinus oedipus and 5. fuscicollis are still being carried 60% of the time (Tardif et al, 1986, 1993). Infant Leontopithecus achieve independence of caregivers even later, and are carried 15% of the time at 12 weeks of age and independent of carriers (carried <5% of the time) only after week 14 (Hoage, 1982). Thus, the profile of parental carrying effort in callitrichid groups differs widely across taxa. This taxonomic variability may reflect specifies differences in the costs of producing infants (and costs of subsequent infant care) or potential dif- ferences in rates of maturation among callitrichid genera or both factors. Thus, the earlier dependence on alloparents and earlier independence of offspring in Callithrix, compared to Saguinus and Leontopithecus, has been attributed to higher neonate:maternal weight ratios in Callithrix (Kleiman, 1977) or the slower maturational rate in the larger-bodied Leontopithecus (Hoage, 1982). We provide quantitative comparisons of infant carrying behavior by breeding males and females and by alloparents in representative species of two genera of callitrichid primates, Callithrix (C. kuhli, C. geoffroyi) and Leontopithecus (L. rosalia, L. chrysomelas, and L. chrysopygus). We evalu- ated the assumption that the effort expended by alloparental helpers reduces the parental burden of any one individual in the social group, es- pecially the breeding adult female or male or both (Emlen, 1991; Price, 1992a), by comparing differences in carrying effort by individuals in small groups, consisting of the breeding pair and no more than two alloparents, with carrying effort in large groups, consisting of the breeding pair and 3 or more potential caregivers. METHODS Subjects and Housing We observed 14 groups of Leontopithecus, including L. rosalia, L. chrysomelas, and L. chrysopygus, and 10 groups of Callithrix, represented by C. kuhli and C. geoffroyi. Details of the demographic constitution of the study groups are in Table I. We observed captive groups at the Rio de Janeiro Primate Center-FEEMA, Brazil; where social groups are housed in large outdoor cages measuring 4 x 3 x 2 m. Each cage contained natural 892 Santos, French, and Otta Infant Carrying in Callitrichids 893 branches, nestboxes, and natural litter on the floor. The groups were visu- ally separated but had auditory contact with other groups. Food and water were supplied twice daily. Morning feeding consisted of bread enriched with vitamins, proteins, cereal, and milk; in the afternoon fruit and mealworms were provided. Further details of this colony are given by Coimbra-Filho and Maia (1977). Procedure We conducted observations during the first 12 weeks of infant life, which we divided into three monthly periods. We divided all social groups in two sizes: small groups (breeders plus no more than two older siblings) and large groups (breeders plus three or more older siblings). Older siblings (=helpers) are in one of three stages of development based on criteria outlined by Yamamoto (1993): juvenile, 5-10 months of age; subadult: 10-15 months old; and young adult, >15 months for Callithrix; and juvenile, 4-9 months; subadult, 9-12 months; and young adult, > 12 months for Leontopithecus. In Leontopithecus, we had eight small groups (8 litters, 15 infants total) and eight large groups (9 litters, 14 infants total). In Callithrix we had four small groups (4 litters, 8 infants) and six large groups (7 litters, 13 infants). After the birth of infants, we observed each group (litter) an average of one observation session per week during the first 12 weeks of infant life. Observation sessions lasted 30 min and were carried out between 0900- 1100 and 1300-1500. We used 1-min instantaneous scan sampling (Altmann, 1974) to record the location of each of the infants in the group. For each scan, we identified and recorded both infants as being on or off a caregiver and noted the identity of the caregiver for each infant as ap- propriate. No