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1.  Long-term Memory for Calls of Relatives in Cotton-top Tamarins (Saguinus oedipus) 
Recognition of relatives is important for dispersing animals to avoid inbreeding and possibly for developing cooperative, reciprocal relationships between individuals after dispersal. We demonstrate under controlled captive conditions that cotton-top tamarins (Saguinus oedipus) have a long-term memory for long calls of relatives from which they had been separated for periods ranging from 4 to 55 months. Tamarins responded with lower levels of arousal behavior to playbacks of long calls from current mates and from separated relatives compared to calls of unfamiliar, unrelated tamarins. Four animals had been out of contact with relatives for more than 4 years and still showed recognition as evidenced by low levels of arousal. Results could not be explained in terms of proximity to former relatives. Long-term memory for vocal signatures of relatives is adaptive and may be much more common than has been demonstrated.
doi:10.1037/a0023149
PMCID: PMC3191862  PMID: 21574684
cotton-top tamarins; vocalizations; long-term memory; relatives
2.  Conditioned Sexual Arousal in a Nonhuman Primate 
Hormones and behavior  2010;59(5):696-701.
Conditioning of sexual arousal has been demonstrated in several species from fish to humans, but has not been demonstrated in nonhuman primates. Controversy exists over whether nonhuman primates produce pheromones that arouse sexual behavior. Although common marmosets copulate throughout the ovarian cycle and during pregnancy, males exhibit behavioral signs of arousal, demonstrate increased neural activation of anterior hypothalamus and medial preoptic area and have an increase in serum testosterone after exposure to odors of novel ovulating females suggestive of a sexually arousing pheromone. Males also have increased androgens prior to their mate’s ovulation. However, males presented with odors of ovulating females demonstrate activation of many other brain areas associated with motivation, memory and decision making. In this study we demonstrate that male marmosets can be conditioned to a novel, arbitrary odor (lemon) with observation of erections, and increased exploration of the location where they previously experienced a receptive female, and increased scratching in postconditioning test without a female present. This conditioned response was demonstrated up to a week after the end of conditioning trials, a much longer lasting effect of conditioning than reported in studies of other species. These results further suggest that odors of ovulating females are not pheromones, strictly speaking, and that marmoset males may learn specific characteristics of odors of females providing a possible basis for mate identification.
doi:10.1016/j.yhbeh.2010.10.009
PMCID: PMC3043118  PMID: 21029736
Sexual conditioning; sexual arousal; pheromones; common marmosets; pair-bonding
3.  Prosocial behaviour emerges independent of reciprocity in cottontop tamarins 
The cooperative breeding hypothesis posits that cooperatively breeding species are motivated to act prosocially, that is, to behave in ways that provide benefits to others, and that cooperative breeding has played a central role in the evolution of human prosociality. However, investigations of prosocial behaviour in cooperative breeders have produced varying results and the mechanisms contributing to this variation are unknown. We investigated whether reciprocity would facilitate prosocial behaviour among cottontop tamarins, a cooperatively breeding primate species likely to engage in reciprocal altruism, by comparing the number of food rewards transferred to partners who had either immediately previously provided or denied rewards to the subject. Subjects were also tested in a non-social control condition. Overall, results indicated that reciprocity increased food transfers. However, temporal analyses revealed that when the tamarins' behaviour was evaluated in relation to the non-social control, results were best explained by (i) an initial depression in the transfer of rewards to partners who recently denied rewards, and (ii) a prosocial effect that emerged late in sessions independent of reciprocity. These results support the cooperative breeding hypothesis, but suggest a minimal role for positive reciprocity, and emphasize the importance of investigating proximate temporal mechanisms underlying prosocial behaviour.
doi:10.1098/rspb.2010.0879
PMCID: PMC2992700  PMID: 20630886
reciprocal altruism; prosocial behaviour; negative reciprocity; punishment; cooperative breeding
4.  Variation in Oxytocin is Related to Variation in Affiliative Behavior in Monogamous, Pairbonded Tamarins 
Hormones and behavior  2010;58(4):614-618.
Oxytocin plays an important role in monogamous pairbonded female voles, but not in polygamous voles. Here we examined a socially-monogamous cooperatively breeding primate where both sexes share in parental care and territory defense for within species variation in behavior and female and male oxytocin levels in 14 pairs of cotton-top tamarins (Saguinus oedipus), In order to obtain a stable chronic assessment of hormones and behavior, we observed behavior and collected urinary hormonal samples across the tamarins’ three week ovulatory cycle. We found similar levels of urinary oxytocin in both sexes. However, basal urinary oxytocin levels varied ten-fold across pairs and pair-mates displayed similar oxytocin levels. Affiliative behavior (contact, grooming, sex) also varied greatly across the sample and explained more than half the variance in pair oxytocin levels. The variables accounting for variation in oxytocin levels differed by sex. Mutual contact and grooming explained most of the variance in female oxytocin levels whereas sexual behavior explained most of the variance in male oxytocin levels. The initiation of contact by males and solicitation of sex by females were related to increased levels of oxytocin in both. This study demonstrates within-species variation in oxytocin that is directly related to levels of affiliative and sexual behavior. However, different behavioral mechanisms influence oxytocin levels in males and females and a strong pair relationship (as indexed by high levels of oxytocin) may require the activation of appropriate mechanisms for both sexes.
doi:10.1016/j.yhbeh.2010.06.014
PMCID: PMC2933949  PMID: 20600045
Oxytocin; affiliative behavior; cotton-top tamarins; monogamy; cooperative breeding; sex differences
5.  Affective responses in tamarins elicited by species-specific music 
Biology Letters  2009;6(1):30-32.
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.
doi:10.1098/rsbl.2009.0593
PMCID: PMC2817256  PMID: 19726444
music evolution; vocal communication; affective responses; tamarins; species-specific music
6.  Exposure to infant scent lowers serum testosterone in father common marmosets (Callithrix jacchus) 
Biology Letters  2008;4(6):603-605.
Common marmoset (Callithrix jacchus) males are bi-parental non-human primates that show extensive paternal behaviour. Fathers are in direct sensory contact with their infants during the natal period. We found that fathers exposed to isolated scents of their infant displayed a significant drop in serum testosterone levels within 20 min after exposure, whereas parentally naive males did not. These data suggest that infant's scent may have a causal role in regulating paternal testosterone in their fathers. This is the first study to demonstrate that olfactory cues have an acute effect on paternal care.
doi:10.1098/rsbl.2008.0358
PMCID: PMC2614150  PMID: 18755659
paternal care; testosterone; infant scent; parenting; olfactory
7.  The Effects of Unequal Reward Distributions on Cooperative Problem Solving by Cottontop Tamarins (Saguinus oedipus) 
Animal behaviour  2008;75(1):245-257.
Cooperation among non-human animals has been the topic of much theoretical and empirical research, but few studies have examined systematically the effects of various reward payoffs on cooperative behaviour. Here, we presented heterosexual pairs of cooperatively breeding cottontop tamarins with a cooperative problem solving task. In a series of four experiments, we examined how the tamarins’ cooperative performance changed under conditions in which (a) both actors were mutually rewarded, (b) both actors were rewarded reciprocally across days, (c) both actors competed for a monopolizable reward and (d) one actor repeatedly delivered a single reward to the other actor. The tamarins demonstrated sensitivity to the reward structure, exhibiting the greatest percentage of trials solved and shortest latency to solve the task in the mutual reward experiment and the lowest percentage of trials solved and longest latency to solve the task in the experiment in which one actor was repeatedly rewarded. However, even in the experiment in which the fewest trials were solved, the tamarins still solved 46 ± 12% of trials and little to no aggression was observed among partners following inequitable reward distributions. The tamarins did, however, exhibit selfish motivation in each of the experiments. Nevertheless, in all experiments, unrewarded individuals continued to cooperate and procure rewards for their social partners.
doi:10.1016/j.anbehav.2007.04.032
PMCID: PMC2390931  PMID: 19122748
cognition; competition; cooperation; cottontop tamarin; mutualism; reciprocity; reciprocal altruism; Saguinus oedipus
8.  Cooperative breeders do cooperate 
Behavioural processes  2007;76(2):138-141.
Bergmüller et al. (2007) make an important contribution to studies of cooperative breeding and provide a theoretical basis for linking the evolution of cooperative breeding with cooperative behavior. We have long been involved in empirical research on the only family of nonhuman primates to exhibit cooperative breeding, the Callitrichidae, which includes marmosets and tamarins, with studies in both field and captive contexts. In this paper we expand on three themes from Bergmüller et al. (2007) with empirical data. First we provide data in support of the importance of helpers and the specific benefits that helpers can gain in terms of fitness. Second, we suggest that mechanisms of rewarding helpers are more common and more effective in maintaining cooperative breeding than punishments. Third, we present a summary of our own research on cooperative behavior in cotton-top tamarins (Saguinus oedipus) where we find greater success in cooperative problem solving than has been reported for non-cooperatively breeding species.
doi:10.1016/j.beproc.2007.01.016
PMCID: PMC2080785  PMID: 17703900
9.  Grooming as a reward? Social function of grooming between females in cooperatively breeding marmosets 
Animal behaviour  2004;67(4):627-636.
Classical models of grooming predict that subordinate primates will direct grooming towards dominants to receive coalitionary support from them. In contrast, recent reviews suggest that grooming asymmetries can change with social system and ecological conditions and should reflect asymmetries in services provided by different members of the dyad. We studied grooming patterns between females in six wild groups of common marmosets, Callithrix jacchus, to investigate the relation between social structure and grooming between females in a cooperatively breeding species. We observed grooming frequently and consistently in all study groups. Breeding females groomed nonbreeding females more than vice versa, and grooming between breeding and nonbreeding females was not related to agonistic behaviour. Our results provide some support to the hypothesis that grooming asymmetries are related to differences in services provided by different group members. We suggest that, in cooperatively breeding systems, breeding females may use grooming as an incentive for helper females to stay in the group.
doi:10.1016/j.anbehav.2003.06.004
PMCID: PMC1761567  PMID: 17237884
10.  The role of social context and individual experience in novel task acquisition in cottontop tamarins, Saguinus oedipus 
Animal behaviour  2006;71(4):933-943.
In socially tolerant settings, naïve individuals may have opportunities to interact jointly with knowledgeable demonstrators and novel tasks. This process is expected to facilitate social learning. Individual experience may also be important for reinforcing and honing socially acquired behaviours. We examined the role of joint interaction and individual experience in the acquisition of a novel foraging task in captive cottontop tamarins. The task involved learning how to locate and access two hidden food rewards from among 10 differently cued forage sites. Tamarins were tested in three different conditions: (1) individually, (2) while interacting with a naïve mate, and (3) while interacting with a mate trained as a knowledgeable demonstrator. For tamarins tested with mates present, we interspersed social input test days with exposure to the task while alone. Tamarins were tested again 17 months after their last exposure to the task, to assess long-term memory. All tamarins tested with knowledgeable demonstrators solved the task. In contrast, tamarins tested alone or with naïve mates had similarly high levels of neophobia and low levels of task acquisition. We conclude that joint interaction occurs in mated pairs of cottontop tamarins and facilitates the spread of novel behaviour. Interspersing test days with a knowledgeable demonstrator present and test days alone with the task helped tamarins to achieve the ultimate goal of the task: obtaining food rewards. Tamarins performed similarly when tested 17 months later, regardless of their initial learning environment. Tamarins had memory deficits for the location of hidden food rewards, but retained memory of the necessary motor actions and solved the task.
doi:10.1016/j.anbehav.2005.09.007
PMCID: PMC1540457  PMID: 16912811
11.  Activation of Neural Pathways Associated with Sexual Arousal in Non-Human Primates 
Purpose
To evaluate brain activity associated with sexual arousal, fully conscious male marmoset monkeys were imaged during presentation of odors that naturally elicit high levels of sexual activity and sexual motivation.
Material and Methods
Male monkeys were lightly anesthetized, secured in a head and body restrainer with a built-in birdcage resonator and positioned in a 9.4-Tesla spectrometer. When fully conscious, monkeys were presented with the odors of a novel receptive female or an ovariectomized monkey. Both odors were presented during an imaging trial and the presentation of odors was counterbalanced. Significant changes in both positive and negative BOLD signal were mapped and averaged.
Results
Periovulatory odors significantly increased positive BOLD signal in several cortical areas: the striatum, hippocampus, septum, periaqueductal gray, and cerebellum, in comparison with odors from ovariectomized monkeys. Conversely, negative BOLD signal was significantly increased in the temporal cortex, cingulate cortex, putamen, hippocampus, substantia nigra, medial preoptic area, and cerebellum with presentation of odors from ovariectomized marmosets as compared to periovulatory odors. A common neural circuit comprising the temporal and cingulate cortices, putamen, hippocampus, medial preoptic area, and cerebellum shared both the positive BOLD response to periovulatory odors and the negative BOLD response to odors of ovariectomized females.
Conclusion
These data suggest the odor-driven enhancement and suppression of sexual arousal affect neuronal activity in many of the same general brain areas. These areas included not only those associated with sexual activity, but also areas involved in emotional processing and reward.
doi:10.1002/jmri.10456
PMCID: PMC1525212  PMID: 14745749
BOLD technique; approach/avoidance; magnetic resonance imaging; functional imaging; common marmoset; cerebellum; neural circuit; sexual motivation; suppressed sexual activity
12.  Cooperative problem solving in a cooperatively breeding primate (Saguinus oedipus) 
Animal behaviour  2005;69(1):133-142.
We investigated cooperative problem solving in unrelated pairs of the cooperatively breeding cottontop tamarin, Saguinus oedipus, to assess the cognitive basis of cooperative behaviour in this species and to compare abilities with other apes and monkeys. A transparent apparatus was used that required extension of two handles at opposite ends of the apparatus for access to rewards. Resistance was applied to both handles so that two tamarins had to act simultaneously in order to receive rewards. In contrast to several previous studies of cooperation, both tamarins received rewards as a result of simultaneous pulling. The results from two experiments indicated that the cottontop tamarins (1) had a much higher success rate and efficiency of pulling than many of the other species previously studied, (2) adjusted pulling behaviour to the presence or absence of a partner, and (3) spontaneously developed sustained pulling techniques to solve the task. These findings suggest that cottontop tamarins understand the role of the partner in this cooperative task, a cognitive ability widely ascribed only to great apes. The cooperative social system of tamarins, the intuitive design of the apparatus, and the provision of rewards to both participants may explain the performance of the tamarins.
doi:10.1016/j.anbehav.2004.02.024
PMCID: PMC1483064  PMID: 16804561
13.  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.
doi:10.1023/A:1013210226793
PMCID: PMC1483063  PMID: 16804560
cotton-top tamarin; Saguinus; cooperative breeding; weight loss; infant care
14.  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.
doi:10.1002/ajp.20061
PMCID: PMC1482834  PMID: 15356858
cotton-top tamarin; androgens; glucocorticoids; chemical signaling; ovulation; parenting behavior
15.  Attachment and Social Preferences in Cooperatively-Reared Cotton-Top Tamarins 
American journal of primatology  2002;57(3):131-139.
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.
doi:10.1002/ajp.10040
PMCID: PMC1482833  PMID: 12111679
infant attachment; secure base; response to threats; cooperative breeding; cotton-top tamarins (Saguinus oedipus)
16.  Neonatal and Pubertal Development in Males of a Cooperatively Breeding Primate, the Cotton-Top Tamarin (Saguinus oedipus oedipus)1 
Biology of reproduction  2002;66(2):282-290.
In cooperatively breeding groups of mammals, reproduction is usually restricted to a small number of individuals within the social group. Sexual development of mammals can be affected by social environment, but we know little regarding effects of the cooperative-breeding system on males. Cotton-top tamarin (Saguinus oedipus oedipus) offspring typically do not reproduce in their natal group, even though they may be physically mature. We examined neonatal and pubertal development in captive male cotton-top tamarins as an example of reproductive development within a cooperative-breeding system and to compare cotton-top tamarins with the general primate model. Puberty was characterized using both hormonal and physical measures. Data were collected on urinary levels of LH, testosterone (T), dihydrotestosterone (DHT), cortisol, and the ratio of DHT to T; testicular development; body weight; and breeding age. We determined that 1) pubertal LH secretion began at Week 37, 2) a surge of T secretion followed at Weeks 41–44, and 3) an increase in the metabolism of T to DHT may have occurred at an average age of 48.6 wk. Most of the rapid weight gain was completed by Week 24, before hormonal increases and rapid scrotal growth. We concluded that rapid pubertal testicular growth in captive cotton-top males was completed by an average 76 wk, but that completion of the individual pubertal spurt can occur between 56 and 122 wk. In a cooperative-breeding system, the opportunity for successful reproduction is dictated by the social environment, but we found no evidence that male offspring were developmentally suppressed in their natal social groups. Our findings suggest that puberty in male New World callitrichid primates occurs more quickly than puberty in Old World primates, even though both have similar patterns of development.
PMCID: PMC1482832  PMID: 11804940
developmental biology; luteinizing hormone; puberty; steroid hormones; testis
17.  Pregnancy weight gain: marmoset and tamarin dads show it too 
Biology letters  2006;2(2):181-183.
Paternal behaviour is critical for the survival of offspring in many monogamous species. Common marmoset (Callithrix jacchus) and cotton-top tamarin (Saguinus oedipus) fathers spend as much or more time caring for infants than mothers. Expectant males of both species showed significant increases in weight across the pregnancy whereas control males did not (five consecutive months for marmoset males and six months for cotton-top tamarin males). Expectant fathers might be preparing for the energetic cost of fatherhood by gaining weight during their mate’s pregnancy.
doi:10.1098/rsbl.2005.0426
PMCID: PMC1483903  PMID: 16810338
weight gain; paternal care; couvades; primates
18.  Social odours, sexual arousal and pairbonding in primates 
We describe the role of social odours in sexual arousal and maintaining pairbonds in biparental and cooperatively breeding primates. Social odours are complex chemical mixtures produced by an organism that can simultaneously provide information about species, kinship, sex, individuality and reproductive state. They are long lasting and have advantages over other modalities. Both sexes are sensitive to changes in odours over the reproductive cycle and experimental disruption of signals can lead to altered sexual behaviour within a pair. We demonstrate, using functional magnetic resonance imaging (fMRI), that social odours indicating reproductive state directly influence the brain areas responsible for sexual behaviour. Social odours also influence other brain areas typically involved in motivation, memory and decision making, suggesting that these signals have more complex functions in primates than mere sexual arousal. We demonstrate a rapid link between social odours and neuroendocrine responses that are modulated by a male's social status. Recent work on humans shows similar responses to social odours. We conclude with an integration of the importance of social odours on sexual arousal and maintaining pairbonds in socially biparental and cooperatively breeding species, suggesting new research directions to integrate social behaviour, neural activation and neuroendocrine responses.
doi:10.1098/rstb.2006.1932
PMCID: PMC1764847  PMID: 17118925
social odours; sexual arousal; pairbonds; primates; functional magnetic resonance imaging; neuroendocrine responses
19.  Pregnancy weight gain: marmoset and tamarin dads show it too 
Biology Letters  2006;2(2):181-183.
Paternal behaviour is critical for the survival of offspring in many monogamous species. Common marmoset (Callithrix jacchus) and cotton-top tamarin (Saguinus oedipus) fathers spend as much or more time caring for infants than mothers. Expectant males of both species showed significant increases in weight across the pregnancy whereas control males did not (five consecutive months for marmoset males and six months for cotton-top tamarin males). Expectant fathers might be preparing for the energetic cost of fatherhood by gaining weight during their mate's pregnancy.
doi:10.1098/rsbl.2005.0426
PMCID: PMC1483903  PMID: 16810338
weight gain; paternal care; couvade; primates

Results 1-19 (19)