Parturition and perinatal behaviour in captive cotton-top tamarins (Saguinus oedipus)

Fourteen births to seven female cotton-top tamarins in a successful breeding colony were observed. All births occurred between 17:50 and 20:40. Behavioural changes indicating the onset of labour are described. Delivery was usually accomplished rapidly, with short intervals between successive infants. One suspected and one verified breech presentation occurred; these deliveries were accompanied by a marked increase in the duration of the interval between infants, and one infant apparently died during expulsion. All other presentations seen were vertex occiput posterior. Fathers, and sometimes older offspring of both sexes, frequently shared with the mother in eating the placenta. Carrying of infants by individuals other than the mother was rare in the hour after birth, and was usually confined to fathers. One primipara rejected her second-born infant, but all other parents showed competent parental behaviour from birth onwards. The results are compared to data from other primates, and their relevance to the successful breeding of this species is discussed.     

Changes in the activity of captive cotton-top tamarins (Saguinus oedipus) over the breeding cycle

The energetic costs of reproduction are likely to be particularly high in the Callitrichidae (marmosets and tamarins), which characteristically produce twin litters. The activity of five captive breeding pairs of cotton-top tamarins (Saguinus oedipus) was investigated for a 6-month period covering the second half of pregnancy and lactation. Breeding males showed few major changes in activity over this period, but breeding females reduced their levels of locomotion during late pregnancy, and during lactation they spent up to twice as much time feeding and foraging as they did during pregnancy. These results support the hypothesis that the costs that callitrichid females incur when reproducing are likely to have been an important factor in the evolution of these species' communal rearing systems.     

Philopatry and dispersion in the cotton-top tamarin,Saguinus (o.) oedipus: An attempted laboratory simulation

Cotton-top tamarins [Saguinus (o.) oedipus,Callitrichidae] living in cooperatively breeding, mature families in a captive colony were given the chance to explore a new living area. The aim was to simulate choices of philopatry versus dispersion. Breeding adults tended to stay home, as did eldest sons and still-dependent young offspring, but eldest daughters tended to go prospecting. The latter also spent more time in the new area and did more looking around while there. This confirms impression of female dispersion gained from records of “evictions” of daughters by other family members. These findings agree with those from field study and show noteworthy parallels with an avian cooperative breeder, the Florida scrub jay, Aphelocoma coerulescens.     

Birth seasonality in cotton-top tamarins (saguinus oedipus) despite constant food supply and body weight

Goldizen et al. (1988) reported that wild saddle-back tamarins (Saguinus fuscicollis, Callitrichidae) show birth seasonality that is correlated with food supply and body weight. They suggested a sequence of ultimate causality in which shortage of food leads to reduced body weight which leads to timing of weaning and lactation when resources are more abundant. Cotton-top tamarins in captivity show birth seasonality despite constant food supply and body weight. Although natural availability of fruit and insects (which are key foods for tamarins) is related to rainfall, birth seasonality and body weight in captive cotton-top tamarins are unrelated to rainfall. The most likely proximate mechanism for seasonality of births in tamarins is photo-period, given existing data on populations living in natural and artificial lighting.     

Quantitative genetic analysis of cranial morphology in the cotton-top (Saguinus oedipus) and saddle-back (S. fuscicollis) tamarins

Patterns of morphological variation play an important role in evolutionary diversification and are critical to an informed interpretation of interspecific differences. When patterns of genetic variation have not diverged substantially, it is possible to reconstruct the differences in selection which gave rise to morphological differences among extant species. Morphological variation patterns are compared between two tamarin species, the cotton-top tamarin (Saguinus oedipus) and the saddle-back tamarin (S. fuscicollis illigeri). Genetic, phenotypic, and environmental variance/covariance and correlation matrices were obtained for a series of 39 cranial characters in each species (cotton-top tamarin, N = 328; saddle-back tamarin, N = 209) and for the species combined using crania from individuals of known genealogical relationship. After accounting for the effects of estimation error on measures of matrix similarity, patterns of phenotypic, genetic, and environmental variation and correlation were found to be very similar across species and among the types of variance within species. Taking the saddle-back tamarins as the standard, cotton-top tamarins have been selected for an enlarged anterior temporalis attachment area and increased facial prognathism. In primates, an enlarged anterior temporalis muscle is associated with incisive food preparation, especially at wide gape.     

Visual encounters between families of cotton-top tamarins,Saguinus oedipus

Territorial, cooperatively-breeding, incest-avoiding organisms have various options for securing mates and resources for breeding. Both philopatry and dispersal have many costs and benefits, but all are likely to include assessment of neighbours. Five families of cotton-top tamarins,Saguinus oedipus, in a laboratory colony were allowed to watch each other through a peephole. These encounters took place in a naturalistic, neutral zone outwith their home room or cage. Parents looked more at neighbours than did offspring. Older monkeys looked more than younger. Females looked more than males. The clearest effect was ofseniority: eldest offspring regardless of age were more eager lookers than were second-eldest than were third-eldest. The results make sense in terms of the monitoring of potential candidates for mate-recruitment or resource-acquisition, or for defense against outsiders with the same interests.     

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.     

Vigilance,vocalizations, and cryptic behavior at retirement in captive groups of red-bellied tamarins (Saguinus labiatus)

Frequent references are made to presumed antipredator adaptations exhibited by callitrichids, but there are very few systematic investigations of these behaviors. One set of untested presumptions stems from observations that callitrichids become especially vigilant and cryptic prior to retirement each evening. This hypothesis was tested in the current study by quantifying the rates of vocalizations and extragroup behavior at various times of the day. Using two groups of captive red-bellied tamarins, it was demonstrated that these primates do become relatively more quiet and more attentive to the nonsocial environment prior to retirement each evening, culminating in virtual silence once the nest box has been entered. While the adaptive significance of these phenomena has not yet been tested, it is likely that the behaviors reduce vulnerability to predation.     

A retrospective study of infant mortality of cotton-top tamarins (Saguinus oedipus) in captive breeding

Fifty of 156 (32%) colony bred cotton-top tamarins were stillborn, and 31 (20%) died within the first week after birth. The stillbirth rate was related to litter size and parity in captivity. A higher percent of single births were stillborn (69%) compared to those of twin births (26%) (p less than 0.005). A higher percent of infants born of the first litter in captivity (42%) were stillborn than those of subsequent litters (23%) (p less than 0.025). Stillbirths were not related to season of birth or sex of infant. Survival of live infants was unrelated to season of birth, sex, litter size, or number of litters.     

Demography,group composition,and dispersal in wild cotton-top tamarin (Saguinus oedipus) groups

Groups of individually marked cotton-top tamarins (Saguinus oedipus), located in La Reserva Forestal Protectora Serranía de Coraza-Montes de María in Colosó Colombia, were studied over a period of 5 years. Data on group composition, stability, birthing seasons, and dispersal patterns are used to examine the reproductive strategies and tactics used by males and females. Both monogamous groups and groups containing two pregnant females have been observed. All groups contained at least one adult female and male, with several groups containing several adult males and females. Both males and females dispersed to neighboring groups, and there were no sex differences in rates of emigration. Males were more likely to immigrate into a new group following the death/emigration of a resident male. Females appeared to tolerate immigrating females but would actively defend their breeding position during fertile periods. © 1996 Wiley-Liss, Inc.     

The benefits of helpers: Effects of group and litter size on infant care in tamarins (Saguinus oedipus)

The Callitrichidae (marmosets and tamarins) typically give birth to twins, and infant care is shared by all group members. The potential benefits to callitrichids of having helpers were investigated in a study of 21 captive cotton-top tamarin (Saguinus oedipus) infants, living in groups with two to 12 older members. Time carried and suckled and amount of food received from other family members were recorded for each infant during the first 12 weeks of life. The results showed that infants in larger groups were carried more and received more food than those in smaller groups. Twin infants in larger families were less likely to be on the same carrier. Singleton infants were carried more than twins but did not receive more food. On average, individual caretakers in larger groups carried less and shared less food with infants than those in smaller groups. When parental contributions to care were analyzed, no effects of group size were found on mothers' contributions to carrying or food sharing, but fathers in larger groups both carried infants less and shared less food with them. There appear to be several benefits of a communal rearing system to cotton-top tamarins. 1) Infants may receive more care in larger families, thus increasing their chances of survival. 2) The burden of care is spread over several animals, reducing the costs to a given individual. 3) The parents, particularly fathers, may benefit most from reducing the costs of investing in the present litter and increasing their ability to invest in future litters.     

The effect of social environment on estrogen excretion,scent marking,and sociosexual behavior in tamarins (Saguinus oedipus)

The influence of various social environments on estrogen excretion, scent marking, and the expression of sociosexual behavior was examined in cotton-top tamarins (Sanguinus o. oedipus). Behavioral observations and urine collections were conducted on five females while first housed in their natal family group or in the presence of another cycling adult female and then while housed with an unrelated adult male in a separate cage. Behavioral observations only were conducted on males in natal family groups and while housed with an unrelated adult female. Levels of urinary estrone and estradiol for females were measured by specific radioimmunoassays. Females housed in family groups or in the presence of an adult cycling female showed low and noncyclic patterns of estrogen excretion. Removal from these environments resulted in a rapid increase in urinary estrone and estradiol and three of five females demonstrated cyclic patterns of estrone excretion. Rates of anogenital marking in females were elevated after the social change, and sexual interactions, virtually absent in the original environments, were observed in all five females. In males, similar manipulations of the social environment affected the expression of sexual behavior, but not scent marking. The social environment, therefore has a profound impact on fertility and sociosexual behavior in cotton-top tamarin groups, with implications for callitrichid social structure and behavior.     

Fertility status,dominance, and scent marking behavior of family-housed female cotton-top tamarins (Saguinus oedipus) in absence of their mothers

The effect of the mother's absence on the fertility status and expression of scent marking behavior was examined in 12 sexually mature female cotton-top tamarins (Saguinus oedipus) living in four motherless families. Behavioral data and urine samples were collected on an average of five times per week and levels of estrone-glucuronide (E1G) were quantified directly by radioimmunoassay to establish whether the females showed ovarian cyclicity. Of the 12 females investigated only the dominant female in each motherless group exhibited regular E1G cycles. By contrast, low and acyclic hormonal profiles were found for subordinate sisters. In addition to differences in the patterns and levels of E1G, scent gland morphology and rates of scent marking differed between females: dominant, cycling females had elaborate glands and significantly higher rates of scent marking than subordinates. These results indicate that the presence of the mother (breeding female) is one important factor regulating ovarian function in cotton-top tamarin daughters. The findings also show that dominance status is a vital determinant of each female's subsequent physiological reproductive competence, with only the dominant female obtaining complete fertility and probably inhibiting ovulatory activity in her subordinate sisters. Scent marking behavior seems to be involved in the regulation of this phenomenon of intrasexual reproductive competition.     

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.     

Proposed nutritional importance of plant exudates in the diet of the Panamanian Tamarin,Saguinus oedipus geoffroyi

Data collected on the feeding behavior of Saguinus oedipus geoffroyi(Panamanian tamarin) in Panama show that plant exudates, as well as insects and fruits, are a major component of the diet. During the months of May, June, and July, tamarins were observed clinging to the trunks of Anacardium excelsum(Anacardiaceae) while feeding on exudates. These observations accounted for greater than 14% of the total feeding time of this primate. Nutritional analyses indicate that Anacardiumexudates provide these tamarins with a rich source of the mineral calcium as well as protein, carbohydrates, and water. The seasonal pattern of exudate feeding observed in S. oedipusappears to coincide with certain nutritionally sensitive periods of the reproductive cycle and may serve to offset a potential mineral imbalance incurred during the terminal phase of gestation and lactation.     

Reactions of wild tamarins,Saguinus mystax andSaguinus fuscicollis to avian predators

During a field study in northeastern Peru, the reactions of a group ofSaguinus mystax on Padre Isla and of a mixed-species troop ofS. mystax andSaguinus fuscicollis at the Río Blanco to raptorial and other birds were observed. Alarms that are specific to flying stimuli were elicited by birds of prey, but other birds that do not represent a threat to the tamarins also caused alarm calls. Alarm events (i.e., instances when one or more alarm calls were given) were observed at rates of 0.3/hr (Padre Isla) and 0.5/hr (Río Blanco). Rates of alarm events significantly increased after the birth of an infant in the Padre Isla group and after the attack of an ornate hawk-eagle (Spizaetus ornatus) on the Río Blanco group. Reactions to alarming stimuli/alarm calls ranged from looking up to falling down from trees. The modification of the tamarins' behavior by the potential presence of aerial predators indicates that raptors represent an important predatory threat to tamarins.     

Social influences on estrogen excretion and ovarian cyclicity in saddle back tamarins (Saguinus fuscicollis)

The effects of different social living conditions on estrogen excretion and on the ovarian cycle of saddle back tamarins were investigated. Urinary estrogens were monitored as indices of ovarian cyclicity in groups of adult females living under the following experimental conditions: (1) five parous females, each living with an adult castrated male (in one of the females plasma estradiol and progesterone were also measured); (2) five adult daughters living with their families. Each daughter was then removed from her family and paired with a vasectomized male. After pairing, scent marks collected from the family were introduced daily to one of the daughters and her mate. Scent exposure was then discontinued and hormone excretion measured for several weeks. The remaining four daughters were not exposed to family scent. The females living with castrated males showed urinary estrogen cycles of an average length of 17.5 ± 1.0 days. The plasma estrogen cycle was of the same length. The females studied under condition 2 showed low, noncycling estrogen levels while living in their families. They responded to pairing with an increase in the level of urinary estrogens, and four out of five showed regular estrogen cyclicity. The fifth female exposed to family scent marks after pairing also showed an increase in urinary estrogens. However, as long as scent transfer was maintained, no cycle was observed. Estrogen excretion increased again, and cyclicity commenced when scent transfer was discontinued. It is concluded that ovarian estrogen production is suppressed and cyclicity does not occur as long as daughters live in their families. Release from suppression and perhaps stimulation by the male cause a rapid increase in estrogen levels and the onset of cyclicity. Chemical stimuli produced by the family, perhaps particularly by the mother, may be involved in reproductive suppression.     

Reproduction in captive lion tamarins (Leontopithecus): Seasonality,infant survival,and sex ratios

Diversity in reproductive and social systems characterizes the primate family Callitrichidae. This paper contributes to our appreciation of this diversity by presenting the first detailed comparative analysis of captive breeding in three species of lion tamarins (Leontopithecus chrysomelas, L. chrysopygus, and L. rosalia) housed at the Centro de Primatologia do Rio de Janeiro. The annual pattern of reproduction in all three species of Leontopithecus was markedly seasonal, with births occurring during the spring, summer, and fall months from August through March. While modal number of litters produced per female per year was 1, approximately 20% of breeding females produced two litters per year. The onset of breeding activity in years when two litters are produced was significantly earlier than in years when only one litter was produced. The cumulative number of offspring surviving to 3 months of age did not differ between years with one vs. two breeding attempts. Like other callitrichids, postnatal mortality was highest during the first week of life, and there were pronounced species differences in offspring survival through 1 year, with significantly lower survivorship in L. chrysomelas. Infant survivorship was affected by a number of experiential factors. Survivorship up to 30 days of life was higher in groups in which the breeding female had previous experience with infants as a nonbreeding helper than in groups in which the female lacked previous helping experience. Likewise, survivorship to 30 days of life was higher for infants born to multiparous females than for infants born to primiparous females. When parity and previous helping experience were analyzed concurrently, the lowest survivorship was associated with offspring produced by inexperienced primiparous females. Genus-wide, there was no significant departure from a 50:50 sex ratio at any point during the first year of life, nor was there evidence for differential mortality for male and female infants. However, L. chrysopygus produced significantly more male infants at birth (65:44) and had male-biased litters (approximately 60% males) throughout the first year of life, while L. chrysomelas showed a nonsignificant tendency toward female-biased litters. © 1996 Wiley-Liss, Inc.     

Campylobacter-induced enteritis and diarrhea in captive cotton-top tamarins (Saguinus oedipus) during the first year of life

A prospective study of 43 cotton-top tamarins, from infancy to 6 to 17 months of age, was conducted to determine the epidemiology of Campylobacter spp. infection. Nine infants followed for one year in an isolation unit, where attendants wore protective clothing, did not become infected. In the main facility where 32 of 34 animals had repeated infections with C. coli, 6% of the infections developed initially in incubators, 66% in the nursery room, and 28% after transfer to the main colony. Fifteen of these tamarins also were infected with C. jejuni. Twenty percent of the infections developed initially in the nursery room and 80% in the colony. Polyacrylamide gel electrophoresis analysis of C. jejuni cultures revealed multiple reinfections with different strains. Both types of infections were most prevalent between 3 and 9 months of age. Campylobacterjejuni infection developed most frequently between April and June and C. coli infection developed between October and December. In the nursery, diarrhea developed most frequently at times when there was no infection with Campylobacter spp. Forty percent of animals with diarrhea in the nursery had C. coli and none had C. jejuni, whereas, in the colony, 49% had C. jejuni and 11% had C. coli infections. There was no association between these infections and diet or idiopathic colitis.     

Social and seasonal influences on reproductive biology in male moustached tamarins (Saguinus mystax)

In several primate taxa there is evidence that the social and physical environment can exert a significant effect on reproductive behavior and biology. In this paper we examine social and physiological factors influencing group composition and reproduction in free-ranging moustached tamarin monkeys (Saguinus mystax mystax). This species is characterized by cooperative care of the young and a breeding system that includes both polyandrous and polygyandrous matings. Body measurements collected on adult males residing in multimale groups indicate marked within-group differences in testes volume. In 12 of 17 groups examined, testes volume of at least two resident adult males differed by 21–174%. Among these males, testes volume was not correlated with either body weight or adult age class. We also examine whether factors such as time of year had an effect on reproductive condition. An analysis of body measurements of 128 adult male and 127 adult female moustached tamarins, wild-trapped and released in northeastern Peru, indicates cyclic changes in genital size. For males, mean monthly testes volume in July (712 mm³) was twice that recorded in June (351 mm³). Females exhibited a similar pattern. Although endocrine information on intra- and intersexual social effects on fertility are unavailable for S. mystax, given the high degree of social cooperation and lack of overt aggression among adult male group members, we offer the possibility that resident male moustached tamarins compete for access to the groups' lone breeding female through socially induced reproductive suppression and sperm competition. © 1996 Wiley-Liss, Inc.