Food Sharing in Pied Bare-Faced Tamarins (Saguinus bicolor bicolor): Development and Individual Differences

We investigated food sharing behavior in 5 litters of pied bare-faced tamarins (Saguinus bicolor bicolor)—8 infants, from 3 families—from 5 to 26 weeks of age. The frequency of sharing by parents in response to infant begging increased steadily from the age of 5 weeks to 16 weeks, and then declined. Offering of food by adults without prior infant begging occurred at very low frequencies throughout observations (1.5% of total items transferred). On average, infants received approximately equal amounts of food from transfers from others and by self feeding until about 20 weeks, after which self feeding began to predominate. Begging success—the proportion of infant begs which resulted in food sharing—remained relatively constant over time, at 60–70%. Overall, therefore, the frequency of food sharing seemed to be governed by changes in infant rather than adult behavior. There were individual differences between adults in their response to infant begging, but two of three fathers transferred significantly more food to infants than mothers did. The results of this study emphasize the existence of specific and individual differences in food-sharing behavior, which must be taken into account in explaining its importance in the reproductive strategies of the Callitrichidae.     

Associations Between Golden-Headed Lion Tamarins and the Bird Community in the Atlantic Forest of Southern Bahia

We examined the presence of birds accompanying and foraging in proximity to golden-headed lion tamarins at Una Biological Reserve, Bahia, Brazil. We followed 3 groups of golden-headed lion tamarins over 3 yr. We noted all birds ≤5 m of a lion tamarin during 20-min observation periods. We found 11 different bird species in the presence of the lion tamarins. We most often found insectivores, such as woodcreepers and nunbirds, in association with them, eating prey the tamarins flushed. Associations were most frequent in mature and shade-cocoa forests. The group that spent most of its time in mature and shade-cocoa forest was also the group that foraging birds followed most frequently. Differences in resource availability among forest types, such as the abundance of microforaging environments, may affect the frequency and diversity of birds seen in association with golden-headed lion tamarins.     

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.     

Food sharing in lion tamarins: Tests of three hypotheses

Infant marmosets and tamarins (Callitrichidae) frequently receive food from older group members. Three possible functions of food sharing in lion tamarins were examined experimentally. The first hypothesis, that food sharing ensures that infants receive sufficient food even if it is difficult for them to acquire it themselves, was tested by varying the ease with which infants could reach a food source. When access to food was restricted, infants fed themselves less, received more food from others, and had a higher success rate in begging attempts. The second hypothesis, that food sharing helps teach infants an appropriate diet, was tested by presenting fruits that were novel to infants. Although infants fed themselves less under these conditions, adults were less likely to share novel foods than familiar foods. The final experiment compared food sharing when food was abundant with behavior when food items were presented singly. Infants fed themselves less and received more food from others when food items were rare. These results suggest that food sharing in lion tamarins helps to ensure that infants receive adequate amounts of food which is difficult to locate or acquire, but that it is not involved in teaching infants which foods they should eat. © 1993 Wiley-Liss, Inc.     

Tutoring in Wild Golden Lion Tamarins

Among most nonhuman primates, juveniles must acquire most of their solid food independently. Information gleaned from adults results from efforts initiated by the juveniles. Donation of food or foraging information by adults to immatures is rare among apes and virtually unknown among monkeys. We report 3 observations in which wild adult golden lion tamarins appear to have directed their immature offspring to a location where a hidden prey item was located. According to the definition of Caro and Hauser (1992), the tamarins were tutoring their young.     

Color Vision in <Emphasis Type="Italic">Leontopithecus chrysomelas</Emphasis>: A Behavioral Study

We assessed the color discriminations by golden-headed lion tamarins (Leontopithecus chrysomelas) via a series of tasks involving a behavioral paradigm that maximizes the naturalness of the stimuli. The stimuli were pairs of Munsell color chips used in earlier experiments with human dichromats. We tested 3 male and 3 female monkeys with stimuli of random brightness values in order to assure that discriminations were based on color rather than brightness cues. Results indicate that each male and one female presented random performances for stimuli resembling hue conditions under which tamarins forage: oranges vs. greens. Two females exhibited discriminations consistent with allelic trichromacy. Findings indicate the presence of an M/L cone opsin polymorphism, a condition of most platyrrhines that is characterized by dichromatic and/or trichromatic females and dichromatic males. Interspecific differences in allelic frequency among lion tamarins raises the possibility that habitat fragmentation is affecting heterozygous frequencies, a trend that could impact tamarin foraging efficiency.     

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.     

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.     

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.     

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.     

Endocrine Correlates of Reproductive Status in Breeding and Nonbreeding Wild Female Moustached Tamarins

In callitrichid primates, reproduction is usually restricted to a single female per group. Reproductive rate is high and the occurrence of a postpartum estrus can lead to simultaneous lactation and pregnancy. In contrast, nonreproductive females often show ovarian inactivity. However, most studies on callitrichid reproductive physiology have been conducted in captivity, where conditions differ considerably from those in the wild, so that reproductive conditions may be strongly modified. Using fecal estrogen and progestogen measurements to monitor female reproductive status in 2 groups of wild moustached tamarins (Saguinus mystax), we examined 1) whether reproductive females in free-ranging groups also show postpartum estrus and 2) whether nonreproductive females demonstrate signs of ovarian activity. In both reproductive females, clear changes in the excretion pattern of progestogen and estrogen metabolites over time in combination with information on parturition dates allowed us to differentiate between pregnancy, a period of postpartum ovarian inactivity lasting for 54 and 64–82 days, and a period of ovarian activity before conception. Nonreproductive females demonstrated temporal fluctuations in hormone concentrations and absolute hormone levels that were similar to ones in the breeding females during the phase of ovarian activity. The results suggest that, in contrast to most captive female tamarins, reproductive females in wild groups of moustached tamarins do not have a postpartum estrus and that nonreproductive females show ovarian activity despite the presence of a breeding female. We therefore conclude that findings from captivity should be only carefully compared to the situation in the wild.     

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.     

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.     

Sex Differences in Olfactory Communication in Saguinus labiatus

We assessed behaviors involved with depositing and receiving scent in three captive heterosexual pairs of red-bellied tamarins (Saguinus labiatus). The frequencies of scent deposition and scent investigatory behaviors differed between the sexes. Females scent marked exclusively by the anogenital gland. Males deposited 95.8% of scent marks via the anogenital gland and 4.2% via the sternal gland. Females scent marked at a significantly higher rate than that of males (0.9 ± 0.1 versus 0.3 ± 0.1 per 20 min, respectively). Males investigated the scent of their opposite-sex partners whereas females investigated no male scent. Mean ± SEM latency for males to investigate female scent was 208.7 ± 65.0 sec. Around 9% of all scent marks were overmarked within 8 min and there was a nonsignificant trend for males to overmark the scent of their female partners than vice versa. We discuss the sex differences in olfactory communication in red-bellied tamarins in terms of sexual selection theory.     

Comparison of affiliative behaviors between old and recently established pairs of golden lion tamarin,Leontopithecus rosalia

To evaluate the changes in the relationship between male and femaleLeontopithecus rosalia over time, I compared the interactions in four well established pairs at the National Zoological Park, Washington, D.C., to those in four newly established pairs at the Conservation and Research Center of the National Zoological Park, Front Royal, Virginia, U.S.A. I recorded the frequency of approaches, withdrawals, food offerings, food takings, and resisting food transfers. Male and female adults were the focal animals and the observations totaled 206.5 hr. Males of newly established pairs interacted more with females than males of old established pairs. While males generally began and maintained the interactions significantly more than females, females of recently formed pairs were initiators of affiliative behaviors significantly more than females of old pairs. These results demonstrate a qualitative difference in the relationship between males and females when old and new pairs are compared.     

Sibling Age and Intragroup Aggression in Captive Saguinus midas midas

Different species of Callitrichidae show a consistent pattern in intragroup aggression. Aggression is more frequent between same-sex individuals, with males and older siblings being more aggressive. These findings have been associated with reproductive competition and dispersal events. However, the few studies dealing with intragroup aggression have not fully explored the effects of food availability on aggression or the relationship between age and aggression. I observed 3 family groups of Saguinus midas for 50 weeks and recorded all occurrences of aggression. A total of 138 agonistic events occurred at an average of 1.16 aggressive acts/hour per group, and 52.2% of aggressive acts occurred during a food shortage condition, which accounted for about 12% of all meals in the groups. During the food shortage, aggression was significantly higher, which suggests that food competition promoted an increase in aggression levels. Aggression amongst siblings accounted for 65.2% of all aggressive acts. Aggression from brothers to sisters was significantly more frequent than aggression between brothers. Aggression rates were significantly different between age classes. Young siblings were significantly more aggressive toward old ones than the reverse. Age and aggression received followed a linear relationship, while age and aggression initiated tended to follow a curvilinear relationship. Higher rates of aggression in young siblings probably were prompted by puberty and associated hormonal changes.     

A New Subspecies of <Emphasis Type="Italic">Saguinus fuscicollis</Emphasis> (Primates,Callitrichidae)

Saddleback tamarins (Saguinus fuscicollis, S. melanoleucus, and S. tripartitus) occur in the upper Amazon, west of the rios Madeira and Mamoré–Guaporé to the Andes. They currently comprise 13 species and subspecies in Bolivia, Brazil, Colombia, Ecuador, and Peru. Here we report on a previously undescribed subspecies of Saguinus fuscicollis from the interfluvium of the lower rios Madeira and Purus in the central Amazon of Brazil. It is a distinct form with a very pronounced mottling on the back giving the appearance of a saddle, a characteristic shared by the 3 species, and the reason for their collective common name. The lack of a white superciliary chevron and its highly mottled ochraceous-dark brown to black saddle that extends from the scapular region to the base of the tail distinguish the new taxon from Saguinus fuscicollis weddelli. The latter characteristic also distinguishes it from another saddleback tamarin (Saguinus fuscicollis ssp.) that has been reported immediately to the south of its range in the same interfluvium. We compare pelage coloration, external characters and craniometric measurements with its geographically closest relatives, Saguinus fuscicollis weddelli and S. f. avilapiresi, and indicate its probable geographic distribution in a small area between the rios Madeira and Purus, just south of the Rio Amazonas.     

灵长类动物的食物分享行为

食物分享是灵长类动物的一种重要社会交往行为,主要发生在成体-幼体间和成体-成体之间。本文从这两个方面对灵长类动物食物分享的行为表现、特点以及功能进行总结,着重比较了无亲缘关系的成年个体间食物分享的互惠解释和骚扰解释。通过对以上内容的综合分析,进一步提出了食物分享行为的未来研究方向以及对人类合作行为演化的启示。     

Seed Swallowing in Tamarins: Evidence of a Curative Function or Enhanced Foraging Efficiency?

Nonhuman primates represent a major component of the frugivore biomass in several rain-forest communities. Although there is considerable evidence that prosimians, monkeys, and apes serve as dispersal agents for many tropical trees, little attention has been paid to the more basic questions of why certain species of primates swallow and void seeds, and what, if any, are the advantages to an animal of having a large, hard, bolus pass through its digestive tract. We examine patterns of fruit-eating and seed-swallowing in two species of free-ranging tamarins: Saguinus mystax and Saguinus geoffroyi. Fruits commonly eaten by tamarins contain large seeds surrounded by a fibrous and adhesive pulp or arilate seed coat. They generally swallow seeds and pulp together. Intact seeds are voided over a 1- to 3-h period. Measurements of 132 seeds naturally voided by Panamanian tamarins average 11.2 mm in length and 0.3 g. The greatest number of large seeds contained in the digestive tract of a single animal at one time was 13. In the case of moustached tamarins, we collected 220 seeds. Average seed length is 11.9 mm and average seed weight is 0.3 g. At the time of capture, one animal had 26 seeds in its digestive tract. In both tamarin species, there is evidence of sex-based differences in feeding behavior. Adult female moustached and Panamanian tamarins swallowed and voided seeds of larger size than adult males did. Seed size is positively correlated with pulp weight (p <. 001), therefore females were selecting food items with higher nutritional rewards than adult males did. Given their small body size and relatively short digestive tract, why do tamarins swallow such large seeds? Although several explanations are possible, we propose that the large number and size of undigested seeds continuously passing through the tamarin gut serve a curative role in mechanically dislodging and expelling intestinal parasites—Ancanthocephala (spiny-headed worms)—from their digestive tracts.