Attachment and social preferences in cooperatively-reared cotton-top tamarins

In many primate species a close attachment between mother and infant provides a secure base for the infant when the infant is frightened or under stress. In cooperatively breeding primates infant carrying is divided among several individuals in the group, with the mother often doing little more than nursing. In these species it is not clear which individual would best serve as a secure base for the infant. We studied eight infant cotton-top tamarins from birth through 20 weeks of age, noting who carried the infant during the first 100 days, who transferred food with the infants, and, as infants became independent, with whom they associated during social play and affiliative behavior. From week 9 to week 20, when infants were independent of carriers most of the time, we presented families with six trials (once every 2 weeks) with a threatening stimulus (a human dressed in a lab coat and wearing an animal mask). Infants played primarily with their twin or youngest sibling and had affiliative interactions with many family members. However, in fearful situations, infants ran to those who had carried them and transferred food with them the most-their father or oldest brother (never to the mother). Although adults increased rates of mobbing calls in response to the threat, infants significantly reduced their vocalization rate. For these cooperatively breeding monkeys, the attachment object for infants is the family member that invested the most effort in carrying the infant and transferring food with the infant. These results parallel and extend results from bi-parental infant care species in which the father serves as the primary attachment figure.     

Captive-born cotton-top tamarins (Saguinus oedipus) respond similarly to vocalizations of predators and sympatric nonpredators

What types of cues do callitrichid primates use to detect and respond to predators? Do they respond to predator‐specific cues or to more general cues? The evidence for these questions remains conflicting. We presented captive‐born and reared cotton‐top tamarins with no previous exposure to predators (or predator cues) with vocalizations from three potential predators of cotton‐top tamarin in the wild (white hawk, jaguar, and tayra) and with vocalizations from sympatric nonpredators (black‐faced antthrush and red howler monkey). Vocalizations from predators and from nonpredator mammals elicited equivalent arousal, fear, and vocal responses. Howler monkey roars produced the strongest responses. The results suggest that predator‐naïve cotton‐top tamarins do not recognize specific predator vocalizations, but may respond to vocal qualities (low‐frequency, noisy sounds) that indicate large body size, threat, or aggression. On the other hand, tamarins responded much more strongly to the higher frequency calls from the hawk than the antthrush, suggesting another mechanism must also be involved. The failure of captive‐reared tamarins to distinguish between vocalizations of predators and nonpredator mammals has important implications for reintroduction studies. Am. J. Primatol. 70:707–710, 2008. © 2008 Wiley‐Liss, Inc.     

Factors in the rejection and survival of captive cotton top tamarins (Saguinus oedipus)

Captive colonies of cotton top tamarins experience a high rate of rejection of infants within the 1st week of life. The rates of rejection and survival to maturity (2 or more years) among 659 live colony-born infants were correlated with rearing, birth group, litter size, season of birth, gender, origin of parents, experience of parents raising siblings, parity and age of parents, and experience of parent pairs. The most important factors associated with low rejection rates were family life and parental experience raising infants. Infants born into family groups or reared in families were rejected at a significantly lower rate. Rejection of infants whose sires were raised with siblings was significantly lower. Paternal experience was more important than maternal experience. Litter size had no effect on rejection of infants born to family groups, whereas, rejection of triplets was significantly higher than twins or singles among those born to parents alone. Rejection was significantly higher among primiparous births than multiparous birth. The combined experience of colony-born parents was not related to rejection if there were no sibling helpers in the cage at the time of birth. Rejection was significantly lower if sibling helpers were present. High survival of infants who were not rejected was correlated with rearing by or being born into family groups and higher parity and older age of the sires.     

Developmental changes in food transfers in cotton-top tamarins (Saguinus oedipus)

We investigated the development of food transfer and independent feeding in cotton-top tamarin (Saguinus oedipus) families. We studied the relationship between infant-directed vocalizations and food transfers on the development of independent feeding in infants. We experimentally tested ten infants (eight twins and two singletons) three times a week for 17 weeks from before weaning through 20 weeks. Food transfers and vocalizations made during tests were recorded and analyzed to determine (1) the role of vocalizations (C- and D- chirps and D-chirp series) in food acquisition, (2) the relationship between food transfers and individual food acquisition, and (3) whether, owing to energetic costs of nursing and carrying twins, food is transferred to twins sooner than to singletons. Infants were more successful in acquiring food via begging when adults produced repeated vocalizations than when adults did not vocalize. Adults emitted more food-related vocalizations in rapid series when in the presence of infants, whereas during feeding in the absence of infants only single unit vocalizations were produced. Begging occurred frequently. Changes over infant age were not significant when all infants were included in analysis. However, when twin data were analyzed alone, begging success changed significantly over months, with successful begging peaking in month 3 (week 12). Begging success rate did not differ between twins and singletons, although twins fed independently sooner and at a higher rate than did singletons.     

Affective responses in tamarins elicited by species-specific music

Theories of music evolution agree that human music has an affective influence on listeners. Tests of non-humans provided little evidence of preferences for human music. However, prosodic features of speech (‘motherese’) influence affective behaviour of non-verbal infants as well as domestic animals, suggesting that features of music can influence the behaviour of non-human species. We incorporated acoustical characteristics of tamarin affiliation vocalizations and tamarin threat vocalizations into corresponding pieces of music. We compared music composed for tamarins with that composed for humans. Tamarins were generally indifferent to playbacks of human music, but responded with increased arousal to tamarin threat vocalization based music, and with decreased activity and increased calm behaviour to tamarin affective vocalization based music. Affective components in human music may have evolutionary origins in the structure of calls of non-human animals. In addition, animal signals may have evolved to manage the behaviour of listeners by influencing their affective state.     

Production and perception of sex differences in vocalizations of Wied's black‐tufted‐ear marmosets (Callithrix kuhlii)

Males and females from many species produce distinct acoustic variations of functionally identical call types. Social behavior may be primed by sex‐specific variation in acoustic features of calls. We present a series of acoustic analyses and playback experiments as methods for investigating this subject. Acoustic parameters of phee calls produced by Wied's black‐tufted‐ear marmosets (Callithrix kuhlii) were analyzed for sex differences. Discriminant function analyses showed that calls contained sufficient acoustic variation to predict the sex of the caller. Several frequency variables differed significantly between the sexes. Natural and synthesized calls were presented to male–female pairs. Calls elicited differential behavioral responses based on the sex of the caller. Marmosets became significantly more vigilant following the playback of male phee calls (both natural and synthetic) than following female phee calls. In a second playback experiment, synthesized calls were modified by independently manipulating three parameters that were known to differ between the sexes (low‐, peak‐, and end‐frequency). When end‐frequency‐modified calls were presented, responsiveness was differentiable by sex of caller but did not differ from responses to natural calls. This suggests that marmosets did not use end‐frequency to determine the sex of the caller. Manipulation of peak‐and low‐frequency parameters eliminated the discrete behavioral responses to male and female calls. Together, these parameters may be important features that encode for the sex‐specific signal. Recognition of sex by acoustic cues seems to be a multivariate process that depends on the congruency of acoustic features. Am. J. Primatol. 71:324–332, 2009. © 2008 Wiley‐Liss, Inc.     

Sexual communication between breeding male and female cotton-top tamarins (Saguinus oedipus), and its relationship to infant care

Male cotton-top tamarins have been shown to be responsive to female scent cues of ovulation, and are known to actively participate in infant care during the time when their mates are fertile. We measured urinary androgen levels and glucocorticoids in seven father tamarins for the first month following the birth of infants to determine 1) whether male tamarins showed an androgen response to their mate's postpartum ovulation, 2) when androgens rise relative to ovulation, 3) whether there is a glucocorticoid response, and 4) whether males alter their parenting behavior during their mate's receptive period. All of the males showed a significant increase in urinary androgens prior to the female's postpartum LH peak, which indicated ovulation. The hormonal increase, which included estradiol, occurred 3-7 days prior to the female's LH peak at a time that coincided with the female's follicular period. Corticosterone levels also peaked during that time, but did not correlate with androgen changes. Fathers did not alter their daily infant-carrying patterns relative to the androgen increase or at the time of the mate's LH peak. We conclude that male cotton-top tamarins experience an increase in androgens that coincides with their mate's postpartum ovulation, which ensures optimal fertility. However, this sexual communication does not alter father-infant interactions, which already occur at a high rate in this species.     

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.     

Reconciliation in captive cotton‐top tamarins (Saguinus oedipus), a cooperative breeding primate

Reconciliation has been demonstrated in all primate species in which the phenomenon has been studied. However, reconciliation has been studied in only two species of callitrichids, and conclusions remain controversial. The first aim of this study has been to find out whether captive cotton‐top tamarins (Saguinus oedipus) reconcile, since this is the first such study on this species. We examined 227 conflicts in three family groups (N=19). Instances in which individuals remained together in t=0 (29; 12.8%) were not analyzed. The cotton‐top tamarins showed heightened affiliation between opponents in the postconflict periods (PC) compared with matched control (MC) periods (39.88±5.12% and 3.18±1.27%, respectively), with a corrected conciliatory tendency of 37.17±5.37%, and a “time window” that included the first 180 sec of the PC period. Former opponents were the most likely recipient of affiliative behaviors during the PC periods: 39.83±4.26% vs. 11.36±5.33% during MC periods. The proportion of attracted pairs (47.13±6.25%) was significantly higher than those of dispersed pairs for male–male conflicts (3.79±1.79), but not for male–female conflicts (27.31±9.32 and 4.82±2.9, respectively). In cooperative‐breeding species, specific sex‐class dyads might differ in how they resolve conflicts. Am. J. Primatol. 71:895–900, 2009. © 2009 Wiley‐Liss, Inc.     

The ontogeny of sex differences in the behavior of patas monkeys

Many studies of sex differences in primates have been based on small experimental groups of peers in which only a limited range of social behavior could be expressed. In addition, the first few months of life are often the focus of such studies, with relatively little attention paid to older juveniles. In this study, 11 male and 9 female juvenile patas monkeys, living in a captive social group with all age-sex classes available, were observed between 1 and 4 years of age. A subset of seven patas monkeys was also observed between birth and 1 year of age. Here, we report the development of sex differences in independence, play, grooming, positioning behavior, and aggression over the juvenile period. Juvenile male patas monkeys played more and in longer bouts than females, but wrestling (rough-and-tumble play) was not more common among males. There were few differences in behaviors directed to male and female juveniles by other group members. Distinct differences emerged only in the behaviors of the juveniles themselves, with females being more active participants in social and aggressive interactions than males. In general, sex differences in patas monkeys show a mixture of patterns, some of which are predictive of adult sex differences and some of which appear to be specific to the particular demands of the juvenile period in this species     

Sex differences in the vocal repertoire of adult red‐capped mangabeys (Cercocebus torquatus): a multi‐level acoustic analysis

Sex differences in the vocal behavior of nonhuman primates can take various forms: sex‐specific call types, differential production of shared call types, or sex discrepancy in phonation. Also, a growing literature is evidencing that systematically analyzing the vocal repertoires of primates at the call level might lead to underestimating their communicative abilities. Here, we present an extensive multi‐level analysis of the still unknown vocal repertoire of adult red‐capped mangabeys (Cercocebus torquatus), with a special emphasis on sex differences. We collected recordings from seven adult males and seven adult females housed in captivity. We present a structurally‐based classification of mangabey calls that we cross‐validated by an analysis of the associated contexts of emission. We found 12 sound units (including six sex‐specific) that were concatenated to form eight call types (including four sex‐specific), which were produced either singularly or in sequences composed of one (“repetition”) or several (“combination”) call types. We extracted organizational principles that ruled call composition and calling patterns. This revealed a high degree of potentially meaningful variability in terms of semantics and syntax. Male–female discrepancy in terms of phonation could be related to morphological dimorphism and would enable listeners to behave appropriately according to the sex of the caller. Sex differences in repertoire size, structural gradation, and call usage could reflect specificities of male–female social roles. We discuss the pertinence of these sex differences according to social system and habitat quality. Am. J. Primatol. 72:360–375, 2010. © 2010 Wiley‐Liss, Inc.     

Sex differences in vocal patterns in the northern muriqui (Brachyteles hypoxanthus)

We investigated whether sex differences in spatial dynamics correlate with rates of staccato and neigh vocalizations in northern muriquis (Brachyteles hypoxanthus) at the Reserva Particular do Patrimônio Natural–Feliciano Miguel Abdala, Minas Gerais, Brazil. A total of 2,727 10 min focal subject samples were collected on 32 adult females and 31 adult males between April 2007 and March 2008. Compared with males, females spent a significantly lower proportion of their time in proximity to other group members and gave staccatos at significantly higher rates while feeding, resting, and traveling. Conversely, males emitted neigh vocalizations at significantly higher rates than females when feeding and resting only. Both sexes gave significantly more staccatos when feeding than when they were engaged in other activities, but their respective rates of neighs did not vary across activities. Both females and males emitted staccato vocalizations at significantly higher rates during times of the year when preferred foods were scarce, but no seasonal differences in the rates of neigh vocalizations were observed in either sex. Females and males showed a reduction in the number of neighbors following staccato vocalizations and an increase in the number of neighbors following neigh vocalizations. Our findings of sex differences in the rates of staccato and neigh vocalizations and the effects of these vocalizations on interindividual spacing are consistent with sex differences in spatial dynamics, and confirm the role of vocal communication in mediating spatial associations in this species. Am. J. Primatol. 72:122–128, 2010. © 2009 Wiley‐Liss, Inc.     

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.     

Leaders of progressions in wild mixed-species troops of saddleback (Saguinus fuscicollis) and mustached tamarins (S. mystax), with emphasis on color vision and sex

Leadership of travel progression is an important aspect of group living. It is widely believed that trichromacy evolved to facilitate the detection and selection of fruit in the dappled light of a forest. Further, it has been proposed that in New World primate species, which typically contain a range of color vision phenotypes, at least one female in a group will be trichromatic (i.e., having three types of visual pigment, in contrast to the two types of pigment found in dichromatic individuals) and will lead the group to fruiting trees. We examine progression leadership within two wild mixed-species troops of saddleback (Saguinus fuscicollis) and mustached (Saguinus mystax) tamarins over a complete year. As whole units, the mixed-species troops were most frequently led by a mustached tamarin. This is the first time that mixed-species group leadership and individual leadership have been quantified in these tamarin species. In terms of single-species intragroup leadership, neither the visual status (dichromatic or trichromatic) nor the sex of individuals had a consistent effect across species. Saddleback tamarin groups were led by males more frequently than females, while evidence suggests that mustached tamarins may be female-led. The notion that all groups contain at least one trichromatic female that leads the troop to feeding trees was not supported.     

Predation-associated differences in sex linkage of wild guppy coloration

Evolutionary theory predicts that the sex linkage of sexually selected traits can influence the direction and rate of evolutionary change, and also itself be subject to selection. Theory abounds on how sex-specific selection, mate choice, or other phenomena should favor different types of sex-linked inheritance, yet evidence in nature remains limited. Here, we use hormone assays in Trinidadian guppies to explore the extent to which linkage of male coloration differs among populations adapted to varying predation regimes. Results show there is consistently higher degree of X- and autosomal linkage in body coloration among populations adapted to low-predation environments. More strikingly, analyses of an introduced population of guppies from a high- to a low-predation environment suggest that this difference can change in 50 years or less.     

Dual Function of Chip Calls Depending on Changing Call Rate Related to Risk Level in Territorial Pairs of White‐Eared Ground‐Sparrows

Different mechanisms have been proposed for encoding information into vocalizations: variation of frequency or temporal characteristics, variation in the rate of vocalization production, and use of different vocalization types. We analyze the effect of rate variation on the dual function of chip calls (contact and alarm) produced by White‐eared Ground‐sparrows (Melozone leucotis). We conducted an acoustic playback experiment where we played back 1 min of four chip call rates (12, 36, 60, 84 calls/min). We measured the response of territorial pairs using behavioral responses, and fine structural features of calls produced in response to those playbacks. White‐eared Ground‐sparrows showed more intense behavioral responses to higher than lower call rate playbacks. Both individuals of the pair approached the source of the playback stimulus faster, produced the first vocalization faster, produced more vocalizations, and spent more time close to the stimulus in higher call rate than in lower call rate playbacks. Frequency and duration characteristics of calls (chip and tseet) were similar in response to all call rate playbacks. Our playback experiment elicited different intensity of behavioral responses, suggesting that risk‐based information is encoded in call rate. Our results suggest that variation in the rate of chip call production serves a dual function in this species; calls are used at lower rates for pair contact and at higher rates for alarm/mobbing signals.     

Aggression, sex and individual differences in cerebral lateralization in a cichlid fish

Cerebral lateralization is an evolutionarily ancient adaptation, apparently ubiquitous among vertebrates. Despite demonstrated advantages of having a more lateralized brain, substantial variability in the strength of lateralization exists within most species. The underlying reasons for the maintenance of this variation are largely unknown. Here, we present evidence that the strength of lateralization is linked to a behavioural trait, aggressiveness, in the convict cichlid (Archocentrus nigrofasciatus), and that this relationship depends on the sex of the fish. This finding suggests that individual variation in behaviour may be linked to variation in cerebral lateralization, and must be studied with regard to the sex of the animal.