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Some aspects of role taking behaviour in captive family groups of the cotton-top tamarin Saguinus oedipus oedipus
... Adult males both in captive and in wild groups of cottontop tamarins and other callitrichines are especially involved in infant carrying (e.g. Epple 1975;Goldizen 1987;Garber 1997;Tardif et al. 2002; but see Schradin & Anzenberger 2001) and in providing vigilance and protection particularly when vulnerable infants are present (Wolters 1978;Savage et al. 1996;Koenig 1998), and lose weight during the period of infant dependency (Sá nchez et al. 1999;Achenbach & Snowdon 2002). Caretaking, carrying effort and weight loss are reduced in adult cottontop tamarin males with the presence of additional helpers (Wolters 1978;McGrew 1988;Tardif et al. 1990;Price 1992b;Savage et al. 1996;Achenbach & Snowdon 2002;Washabaugh et al. 2002). ...
... Epple 1975;Goldizen 1987;Garber 1997;Tardif et al. 2002; but see Schradin & Anzenberger 2001) and in providing vigilance and protection particularly when vulnerable infants are present (Wolters 1978;Savage et al. 1996;Koenig 1998), and lose weight during the period of infant dependency (Sá nchez et al. 1999;Achenbach & Snowdon 2002). Caretaking, carrying effort and weight loss are reduced in adult cottontop tamarin males with the presence of additional helpers (Wolters 1978;McGrew 1988;Tardif et al. 1990;Price 1992b;Savage et al. 1996;Achenbach & Snowdon 2002;Washabaugh et al. 2002). Evidence suggests that infant survival in wild callitrichine groups increases with the number of available helpers and corresponds with the presence of adult males in particular (Garber et al. 1984;Koenig 1995;Savage et al. 1996;Bales et al. 2000). ...
... We reasoned that in a biparental species, general sex-specific social patterns may govern what behavioural modality is used by male or female breeders to maintain cooperative alloparenting services. For example, tamarin fathers engage in higher levels of aggressive behaviour with their adult sons and other family members than do mothers (Wolters 1978;Ginther 2008). Whereas mothers may actively groom to maintain alloparenting services, fathers may instead modulate aggression to show more tolerance to sons that have proven themselves better helpers. ...
In the biparental, cooperatively breeding cottontop tamarin, Saguinus oedipus oedipus, adult sons provide an energetically and reproductively valuable service to their breeding parents by helping to carry infants. Other species may use aggressive coercion or punishment to enforce alloparenting. Yet, affiliation in primates is important in negotiating social relationships and may be exchanged for services. We hypothesized that the rewards of grooming might be used by expectant parents to cultivate strong relationships with and maintain the services of adult son alloparents. We tested for an interchange trade of aggression or grooming for infant carrying according to a biological market. Individual rates of grooming, but not aggression, received by sons were explained by previously demonstrated levels of alloparental infant carrying. However, the direction of the interaction differed according to the sex of the parent. Mothers groomed better carriers at a higher rate, whereas fathers groomed poorer carriers at a higher rate. This sex difference in parental behaviour may reflect differential benefits that male and female breeders receive with increasing help. Market predictions based on alloparent availability were not supported, but results indicated a connection between affiliation and cooperative service. The rates of huddling and contact affiliation between fathers and adult sons suggest a sex-specific set of social relationship traits conducive to both affiliation and infant carrying. These may be necessarily tied to the particular form of infant care by males in this cooperatively breeding species. Fathers may condition sons for the social aspects of carrying, which involve socially coordinated efforts and close physical proximity between adult males. © 2009 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.
... In Leontopithecus rosalia, there seems to be no significant effect of the presence of "helpers" on carrying behavior by the mother or father (Kleiman, unpublished), suggesting that the juveniles and subadults do not change the pattern of parental carrying. By contrast, significant carrying frequencies by other group members do seem to result in reduced parental care activities in Callithrix and Saguinus species (Epple, 1975;Box, 1977;Wolters, 1978). ...
... Interestingly, there does seem to be a relationship between group size and the role of "helpers." In Callithrix, Saguinus and Leontopithecus, with multiple young in litters, older juveniles and subadults individually become substantially involved in parental care while in the singleton-producing Aotus, Callicebus, and Callimico, older juveniles and subadults contribute little to the care of young infants (Epple, 1975;Box, 1977;Wolters, 1978;Dixson and Fleming, 1981;Fragaszy et al, 1982;Cleveland and Snowdon, 1984;Wright, 1984;Beck, Rettberg, Warneke, Ramer, and Sodaro, personal communication). Thus, the total number of available "helpers" appears to affect the behavior of each individual "helper," suggesting either major inborn phylogenetic differences or a social facilitation effect in species with more "helpers" (i.e., a larger group size). ...
... A number of factors deriving from differences in the background of the parents influence parental care behavior in New World primates. Previous experience of parental care is one major variable which has been shown to be important in Callithrix, Saguinus, and Leontopithecus (Epple, 1975;Hoage, 1977;Ingram, 1978;Wolters, 1978). Individuals without previous experience of caring for infants while still living in the parental group, may be abusive or ignore new offspring once they have been paired and reproduce for the first time. ...
Extensive parental care is well developed in several genera of New World primates (genera aCallicebus, Aotus, Callimico, Calltthrix, Cebuella, Leontopithecus, Saguinus) including most of the indirect and direct paternal care behaviors described by Kleiman and Malcolm (1981). Paternal care is correlated with a monogamous (and perhaps polyandrous) mating system and a small group size. Additionally, in genera (e.g., Callithrix) which have a higher reproductive rate and tolerate a larger group size, subadult and juvenile offspring of the breeding pair and perhaps unrelated individuals may contribute substantially to the rearing of infants.
Both within and across genera, there is considerable variability in the type, quantity, and distribution of care provided by the mother, father, and other individuals in the family group. The purpose of this presentation is to examine the basis of this variability and to evaluate the degree to which we can make statements about the evolution of paternal care in this primate radiation.
There are few field studies of those species of monogamous New World primates which exhibit extensive paternal care. Thus, it is currently impossible to correlate the observed variability in paternal care with ecological factors. Also, the taxonomy of the New World primates is in flux which makes phylogenetic interpretation difficult (Rosenberg, 1981). As a result, the following discussion will be based mainly on results from captive studies, and will be concerned with defining those factors that create variability in observed levels of paternal care, both within and across genera.
... The results of at least one other study of captive cotton-top tamarins are inconsistent with the data presented here: Wolters (1978) found that fathers did 90% of the food-sharing in cotton-top tamarin families. ...
... Furthermore, while mothers' contributions to carrying declined steadily from birth onwards, fathers' contributions tended to increase over the first few weeks. Although in groups with few or no helpers, increases in carrying by the father over the first few weeks could be compensation for decreased carrying by the mother, this pattern of paternal carrying persists even in studies of larger groups, both in captivity (Wolters, 1978;Cleveland and Snowdon, 1984) and in the wild (Rylands, 1985). Consequently, other explanations are likely to be necessary here, particularly given that males in large families will even compete to carry infants (Price, 1991b). ...
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.
... In the wild, callitrichids live in family groups from which older siblings migrate as they reach sexual maturity (Dawson 1978;Neyman 1978). Intra-group conflicts between adult animals of the same sex have been observed in captivity to result in the exclusion of one animal from a group or a change in dominance within the group (Wolters 1978;Kleiman 1979;J. Cleveland, personal observation (Dawson 1978;Neyman 1978). ...
... All tamarins of the genus Saguinus that have been studied fit this category; the saddle-back tamarin, Saguinus fuscicollis (Epple 1975;Vogt et al. 1978). the cotton-top tamarin, Saguinus o. oedipus (Hampton et al. 1966;Wolters 1978) and Geoffroy's tamarin, Saguinus o. geoffroyi (Muckenhirn 1967;Moynihan 1970). In all of the species of callitrichids studied, siblings have also been observed to take part in infant care some of the time, although the sample sizes of many studies are so small that the precise degree and timing of sibling involvement is unclear. ...
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.
... Third, methodological differences may account for some of the contradictory findings in the literature. In most FS studies, food is presented in a monopolizable food bowl to the entire group (Price, 1992;Wolters, 1978), henceforth referred to as the standard method. This setup differs significantly from more naturalistic situations in callitrichids where especially rare and highly preferred food items, such as insects, are scattered and captured by single individuals. ...
Food sharing (FS) in cooperatively breeding callitrichids is unusual among nonhuman primates because they regularly share significant amounts of preferred food with immatures and engage in proactive FS. However, it is still unclear which classes of individuals (males or females, breeders or helpers) engage most in FS, and whether differences exist among callitrichid species. In the first part of this study, we characterized general FS patterns in common marmosets (Callithrix jacchus). We found substantial adult–immature FS, and female breeders shared the least with immatures. This conflicts with previously published studies, where data were collected with the prevailing standard method of providing a food bowl to the entire group. In the second part, a comparison of our access-bias-free method and the standard method suggested that previous findings are likely the result of access bias. In the third part, we investigated species differences in adult–adult FS among common marmosets, golden-headed lion tamarins (Leontopithecus chrysomelas), and red-handed tamarins (Saguinus midas). As common marmosets show lower levels of interdependence within groups, we expected more adult–adult FS in tamarins compared with marmosets. Adult–adult FS was indeed more prevalent in tamarins and not exclusively directed from male breeders to female breeders. Therefore, our results suggest that adult–adult FS in marmosets mostly reflects the high energetic demands of female breeders, whereas in the more interdependent tamarins, it may be used to reinforce cooperative bonds between adult group members.
... The pronounced sex differences in scentmarking behaviour in the cotton-top tamarin appear to be greater than among other Callitrichids (see also Wolters 1978). There is apparently no sexual dimorphism in scentmarking among common marmosets (Sutcliffe & Poole 1978), pygmy marmosets (Cebuella pygmaea; C. T. Snowdon & A. Vertovec, personal communication), and golden lion tamarins (Mack & Kleiman 1978). ...
Aspects of social structure in group-living species can be inferred by observing the responses of individuals to unfamiliar animals. This study examined the responses of mated pairs of cotton-top tamarins (Saguinus oedipus oedipus) to presentation of either unfamiliar conspecifics or members of a related tamarin species, the saddle-back tamarin (Saguinus fuscicollis fuscicollis). Male and female responses to intruders differed: resident males threatened, displayed piloerection, approached, and attacked intruders, especially males, while resident females showed increases in suprapubic scentmarking in the presence of intruders. Both males and females discriminated between the species of intruders, exhibiting more threats, scent-marking, piloerection, and approaches in the presence of conspecific intruders. There are pronounced sex differences in the signals and behaviour patterns that are elicited in an aggressive or territorial encounter with unfamiliar conspecifics in this monogamous primate.
... In addition, high levels of intrasexual aggression toward unfamiliar conspecifics has been observed in common marmosets (Callithrix jacchus jacchus; Evans, 1983;Sutcliffe & Poole, 1984) and in saddleback (Epple, 1975(Epple, , 1977, cotton-top (Saguinus oedipus oedipus; French & Snowdon, 1981), and golden lion tamarins . Both male and female common marmosets display intrasexual aggression (Evans, 1983;Sutcliffe & Poole, 1984); however, in tamarins this intrasexual aggression appears to be sexually dimorphic (Epple, 1975;French & lnglett, 1989;French & Snowdon, 1981;Wolters, 1978). In all eases the aggression is sufficiently intense that it effectively prevents other potential mates from emigrating into or permanently residing in a social group as a breeding animal. ...
We investigated the role of mutual and circumstantial factors in maintaining exclusive social relationships in a New World primate. Four breeding pairs of golden lion tamarins (Leontopithecus rosalia rosalia) were allowed to interact with their mate or an unfamiliar, opposite-sex adult in each of 4 different social contexts: in view of the mate, out of the mate's view, with only the mate present, and with only the unfamiliar animal present. Males and females were in proximity to, approached, and sniffed their mates significantly more often than they did unfamiliar tamarins. These behaviors suggest a preference for the familiar mate. However, when mates were absent, tamarins demonstrated significantly higher levels of approach and sniffs toward unfamiliar animals. These patterns of behavior indicate that circumstantial factors, such as social context, may regulate social interactions between paired tamarins and unfamiliar, opposite-sex conspecifics.
Nonhuman primates are among the most expensive, complex, and demanding of species used in biomedical research. Their high cost, scarcity, and high level of sentience demand a specialized infrastructure and level of care that differs from other species used in research. Veterinary care must be balanced between colony management (colony health) and individualized care in such a way that individual animals are treated as patients within the animal care program. With the growing emphasis on translational science, nonhuman primates are often considered the ultimate translational research model due to their close phylogenetic relationship to human primates. Considering the high cost to carry out research using nonhuman primates, research must be vigorously justified based on the probability that the primate model will most closely recapitulate what would be observed in human beings. Their susceptibility to human infectious agents, similarities in physiological responses, developmental biology, and response to experimentally induced diseases are critically important to the advancement of biomedicine. Nonhuman primates are also among the most scarce, costly, and sentient of animal models used in research. During the past 40 years, there has been a significant increase in our knowledge of the biology and care of these valuable animals. This chapter is intended to provide veterinarians, colony managers, and research scientists with an overview of the natural history, biology, clinical management, husbandry, and diseases of the eight most commonly used primate genera.
Intrauterine gestation and the physiological adaptations of females that have allowed them to nourish neonates characterize the class Mammalia, and these characteristics have had revolutionary consequences on the evolution of social organization and mating patterns (Trivers, 1972; Brown, 1975; Maynard Smith, 1977; Wittenberger and Tilson, 1980; Williams, 1966; Gubernick and Klopfer, 1981). This physiological mechanism that allowed a female to solely and direcdy support her offspring also had dramatic effects on parent/offspring bonds (Trivers, 1972), such that the relationships between mother and child are cardinal to all mammalian social systems. An evolutionary consequence of this female capacity has been the diminution of the role of males in parental duties; indeed, so pervasive is the bond between mammalian mother and child that the term “parental behavior” has become equated with mothering. So reduced has been the role of males that the term “biparental” care has been coined to denote explicitly some parenting role for them. For example, in more than 90% of bird species, the male plays an equal role to the female in offspring nurturing, but only a very small percentage of mammals show analogous parenting behavior (Brown, 1985). However maternocentric investigations of mammalian social structure may have been historically, a new focus on the male’s role was inaugurated with the publication of Trivers’s (1972) provocative analysis of parental investment and sexual selection.
For many decades, various species of marmosets and tamarins, members of the family Callitrichidae, have been kept in captivity. Early on these animals were mostly kept as pets or were exhibited in zoological gardens1. Although early attempts to maintain and breed marmosets and tamarins for extended periods of time under captive conditions met with limited success, they have gradually increased our knowledge of the behavior and of the dietary and environmental requirements of callitrichids. More recently, biomedical and behavioral researchers have become interested in these small monkeys and in their potential as laboratory primates. As a result of their studies, our expertise in the maintenance of callitrichids in captivity has increased considerably2–8.
Research on chemical communication in mammals has expanded rapidly, since the classical studies by Bruce (1959) and Whitten (1956) directed attention to this field about 25 years ago. However, most of our knowledge on how chemical signals influence behavioral and endocrine events, their chemical nature and the sensory processes involved in mediating them, has been gained from the study of laboratory rodents. Research on primates is still in its infancy, partly because most primates are exotic and expensive laboratory animals, and partly because the complexity of primate behavior greatly complicates experimental studies. However, there are several groups of primates which provide clear morphological and behavioral evidence that chemical communication is of great importance in their social and sexual behaviors. One of these is the family Callitrichidae, the South American marmosets and tamarins.
The first chemical analysis of the volatile components of scent material from the cotton-top tamarin,Saguinus o. oedipus is presented. In contrast to our previous findings in saddle-back tamarins (Saguinus fuscicollis), the chemical composition of the scent marks is quite variable. Analysis of secretion expressed manually from different areas of the scent pads of sedated animals shows individual and regional variability. Only three components (squalene, cholesterol, andp-methoxybenzaldehyde) were found in all scent mark samples analyzed. However, suprapubic secretions obtained from one sedated female contained, in addition, 12 butyrate esters as well as five acetate esters which were homologous to the butyrates. The butyrate esters have been previously identified in scent material fromSaguinus fuscicollis. The variability of the composition of the scent material is discussed in relation to the scent-marking behavior of the cotton-top tamarins. Behavioral studies tested the ability of the cotton-top tamarins to discriminate between scent marks from conspecifics and scent marks from saddle-back tamarins. The group of 12 subjects discriminated between the scent marks from both species in choice tests during which they could freely contact the scent samples. However, when scent marks were presented under a screen, so that the subjects could smell but not contact the stimuli, no discrimination was shown. Four individuals displayed more interest in the screened scent stimuli than all other subjects. When these animals were tested in a second experiment for their ability to discriminate between material from the two species on the basis of only volatile cues, it became evident that they were able to do so. These results indicate that volatile cues alone enable the tamarins to recognize scent marks from conspecifics, but that additional cues perceived during contact with the scent are important for its full attractiveness and/or informational content.
The ability of cotton-top tamarins to discriminate between scents from conspecifics and those from other tamarin species, and between scents from conspecific individuals was tested. Cotton-tops scent mark with specialized skin glands in the circumgenital area. Females possess larger glands than males and show more scent-marking behavior. In the first experiment, subjects were presented with a glass rod scented with either material collected from the surface of the scent glands of a conspecific female, with scent material from a female of a related species, or with an unscented rod. Glass rods carrying scent from conspecifics were sniffed more frequently than rods carrying scent from related tamarin species or unscented rods. A second experiment offered a choice between two glass rods, one scent marked by aSaguinus o. oedipus female, the second one scent marked by aSaguinus fusdcollis female. Shelves carrying rods that had been scent marked by conspecifics were contacted more frequently than those carrying rods marked by heterospecific females. Scent marks from conspecific females were also sniffed more frequently. A third experiment compared the level of responses to rods carrying material collected from the scent glands of female individuals to which the subjects had been habituated with their responses to rods carrying scent from females to which they had not been habituated. Contacting and sniffing responses to the scents of novel females were higher than those to the scents of females to which the subjects had been habituated.
This chapter discusses the food transfer in nonhuman primates and compares the data with predictions that stem from various functional explanations of food transfer. The transfers among adult primates are described and investigate whether patterns of food transfer may be explained in terms of trade or reciprocity, or whether alternative explanations provide a better fit to the data. The transfer of solid food to infant primates from parents and alloparents are described, the inter- and intraspecific evidence that food transfer reduces time to weaning, increases the infant's growth rate, or increases the infant's chance of survival are reviewed in the chapter. The transfer of food to infants may ensure that infants receive nutrients during the critical transition to independent foraging (nutritional hypotheses), and/or learn about diet breadth or food-processing techniques (informational hypotheses). It is suggested that interactions between mothers and infants may result in the transmission of tool-using skills. The chapter also investigates whether there is any evidence that adults actively use food transfer to direct offspring learning, and discuss potential directions for future research.
Monogamy is a relatively rare mating system among the mammals, probably because of the ability of the mammalian female to rear offspring in the absence of any parental investment by a male. Females both gestate and lactate, and they can typically ensure their offsprings’ survivorship to the point of weaning and independence (Kleiman, 1977). Monogamy has evolved in diverse mammals, and the basis for its evolution appears to have differed in different groups. Some of the selective forces that may have influenced the evolution of monogamy in mammals include high rates of intrasexual aggression among females, limited polygyny potential in males, and nonshareable indispensable male parental care (Kleiman, 1977; Wittenberger & Tilson, 1980).
Possession of objects was studied in a captive group of kin-related brown capuchin monkeys (Cebus apella). Following introduction of an object by the experimenter, social interactions around the object were recorded during 15 min, focussing on takeovers, taking at distance and forced relinquishments. Results showed that individuals behaved according to tactical factors such as value and portability of objects. However, possession by subordinates could remain unchallenged by higher-ranking individuals and the latter tolerated some takeovers by subordinates. To account for such patterns, it is assumed that the dominants' behaviour is sometimes limited by the risk of altering the current state of their social relationships.
The effect of the presence of a familiar social partner on the interactions of saddle back tamarins with unfamiliar conspecifics was studied. Fifteen adult male-female pairs, of which six were composed of a castrated male and an intact female, served as subjects. All subject pairs were given two social encounters during which both mates met a strange male and two encounters during which they met a strange female. In addition, all subjects were given four encounters during which they met the same strangers while their own pair mates were absent. As a group, the subjects showed higher intensities of injurious aggression and of agonistic displays when they met strangers in the presence of their own pair mates. Females and castrated males, as subgroups, showed significant increases in most agonistic responses when they met strangers in the presence of their pair mates. Intact males, however, did not.
To assess the important aspects of a large area for environmental enrichment, the behavior of families of common marmosets Callithrix jacchus and cotton-top tamarins Saguinus oedipus when in laboratory cages and when in much larger outside areas was compared. All animals avoided areas with little cover. The two tamarin families preferred an indoor cage to a large open area with little cover and consequently only showed a limited range of behavior when outside. When dense cover was provided to the marmoset family, they used this area extensively, showing a wider range of behavior than when in cages and shifting to less active behavior patterns. By feeding marmosets in a central area, it was possible to allow unlimited access to the outside while effectively containing them.
Food transfer between adults and infants is common in many marmoset and tamarin monkeys, and is often accompanied by vocalizations. We hypothesized that vocalizations by adults in a food transfer context creates an opportunity for infants to learn not only what foods are appropriate but what vocalizations are appropriate in feeding contexts. We studied the development of feeding behavior and food-associated vocalizations in 10 infant cotton-top tamarins through the first 20 wks of life. Infants obtained solid food through transfers from older group members, primarily the adult male, beginning at weeks 5–6. Both adults and infants vocalized during food transfers with adults, producing rapid sequences of the call types adults normally give when feeding. Infants were usually successful in obtaining food primarily when the adult was vocalizing. The sooner infants were active participants in food transfers, the sooner they began to feed independently. In the early weeks, infants produced a large number of vocal types during food transfers, but with increasing age there was a steady increase in the number of adult-form food calls and a reduction in other, non-food-associated calls. Infants that fed independently at an early age produced fewer non-food-associated calls by the last month of observation. Infants called at higher rates to their most preferred food. Food transfers accompanied by vocalizations may provide an opportunity for infants to learn about appropriate foods as well as the vocalizations that accompany feeding in adults, and may represent a form of ‘coaching’ or information donation by adults.
A survey of severe aggression occurring over the 20 year history of a cotton-top tamarin (Saguinus oedipus) colony indicated that most aggression was between same-sex individuals, with fights among siblings more common than parent-offspring conflict. Males engaged in severe aggression more often than females did, paralleling the dimorphic aggressive response to same-sex intruders in this species. Female-female aggression occurred at larger group sizes than male-male aggression, suggesting a higher threshold for female aggression. Much sibling aggression was directed by postpubertal subadults toward prepubertal siblings. Only 17% of aggression occurred in association with infant births, and these cases rarely involved parents and offspring suggesting that aggression was not used by reproductive animals to defend their breeding position. Severe aggression was often associated with attempts to introduce stepparents or movement of individuals in and out of the group. The mean group sizes when aggression is observed in captivity are close to the maximum group sizes observed in wild tamarins, which suggests that severe aggression in captive groups may reflect processes related to dispersal in wild tamarins.
Observations of several aspects of the behavior of the tamarin Saguinus labiatus labiatusin the laboratory are presented. Some patterns of the behavioral repertoire emphasize areas of contrasting pelage;the leg standaccompanied by piloerectiondisplays the orange coloration of the ventrum. Several facial expressions (possibly rare in other species of callitrichid)
emphasize the contrast between the white circumbuccal area and the black face. The behavior of three mated pairs was compared.
Agonistic and sexual behaviors were rare. Males allogroomed their mates more than females did. Females performed the most
scent marking. In two of the three pairs, one animal (the male in one case, the female in the other) determined the amount
of contact and proximity between the mates. Experimental introductions of unfamiliar tamarins resulted in small amounts of
both amicable and agonistic behavior. The tendency of adults to attack familiar same-sex conspecifics, reported in other callitrichids,
was not evident in these experiments, although the presence of the mate stimulated social interaction between unfamiliar tamarins.
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.
The predator avoidance behaviour of a free-ranging group of buffy-headed marmosets,Callithrix flaviceps, was recorded in detail during the course of a long-term study of behavioural ecology at the Fazenda Montes Claros, southeastern
Brazil. Four distinct patterns of predator avoidance behaviour, each with specific vocalisations, were recognised and are
described here. The selection and use of sleeping sites by the study group are also described. An analysis of the records
indicates that these small monkeys are generally most vulnerable to predation by aerial raptors. Variations in the frequency
of alarm calls also indicate that the marmosets tend to be more vigilant at higher levels in the forest and when the leaf
cover is less extensive. The implications of group size and social structure for both the evolution and the efficacy of the
anti-predator behaviour of marmosets are also discussed.
Female marmosets and tamarins typically give birth to twins, and appear to need considerable assistance from the male and from other group members if they are to rear the young successfully. To ensure that male help is available, females would be expected to increase the time they devote to the pair relationship shortly before birth. Males, however, should devote most time to their relationship with the female after birth, when she is most likely to conceive. These predictions were tested in a study of five captive pairs of cotton-top tamarins for 3 months before and 3 months after the birth of infants, a period covering the second half of pregnancy, lactation and postpartum oestrus. Female investment in the pair relationship, measured by grooming and promotion of proximity, was greatest shortly before birth, while male investment in terms of promotion of proximity and affiliative behaviour such as nuzzling was greatest during the first weeks postpartum. Females showed more proceptive behaviour and were more receptive to males' mounts before they gave birth than after, but were more attractive to the male after birth. These results confirmed the predictions, and suggested that female tamarins use strategies aimed at gaining male assistance in rearing infants, while males, in addition to investing in their current offspring, adopt strategies for maximizing their chances of fathering future offspring.
Many mammalian species which exhibit scent-marking behaviour show a pronounced sexual dimorphism in marking behaviour and scent gland morphology. However, several species of marmosets and tamarins do not show dimorphism in these traits. We examined sex differences in scent-marking structures and behaviour in cotton-top tamarins (Saguinus o. oedipus; Primates: Callitrichidae). While body size and weight were virtually identical in adult males and females, there were pronounced sex differences in scent gland size and in rates of marking behaviour. Females possessed larger anogenital and suprapubic glands and showed 10-fold higher rates of anogenital marking and slightly higher rates of suprapubic marking than males. Observations on the development of anogenital marking revealed a lack of dimorphism during the first 2 years. Adult rates of anogenital marking in females were only observed in females housed separately from their natal family group. The onset of adult levels of marking behaviour corresponds with the adoption of the role of a breeding adult female, suggesting that anogenital marking plays a role in sexual communication.
In order to explore whether or not adult motivation influences transfer of food to infants in cotton-top tamarins (Saguinus oedipus oedipus), 2 experiments were carried out with 3 large captive family groups. Examination of (a) natural changes in food motivation during feeding, and (b) elevated motivation toward food by giving highly preferred items, showed that the adult monkeys shared food more when their own level of motivation was high. This suggests that food-transfer is not merely a consequence of adult satiation, but that matching sharing with high adult motivation is a mechanism which ensures that infants receive ample food, the best items, and also rare items of high quality.
The effects of callitrichid primate helpers (allocare-givers other than an infant's father) on the survival, reproduction or behavior of infants and parents are reviewed, using both published studies and data from free-ranging golden lion tamarins (Leontopithecus rosalia). Three lines of evidence suggest that helpers may increase their own inclusive fitness: (1) The number of adult males acting as helpers in free-ranging groups is correlated with the number of surviving infants in 3 callitrichid species. However, the lack of a negative correlation with number of infants dying suggests that activities other than direct infant care (e.g. territory defense) may be more important, especially in newly formed groups. (2) In 2 species, captive groups with helpers carry infants for longer periods of time than do groups without helpers. Whether such differences would translate into meaningful survival differences in free-ranging groups is unclear. (3) Helpers reduce the energetic burden of parents by reducing the amount of time they spend transporting or provisioning infants in at least 4 species. Reproductive males are more likely than reproductive females to benefit from the presence of helpers, reducing their investment in infant care activities as the number of helpers in the group increases. In free-ranging golden lion tamarins, the reproductive tenure of males, but not females, increases with the number of helpers in the group, suggesting that a reduction in energetic investment may translate into increased survival. 'Decisions' made by helpers to participate in infant transport are weighed against competing needs for foraging, vigilance, territory defense and, in some cases, prospecting for breeding opportunities. Given this complexity, a sophisticated model may be required to answer the question of how helpers 'decide' to participate in infant care versus other activities.
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