New World monkeys II: Marmosets, tamarins, and Goeldi's monkeys

(Callitrichidae)

Class Mammalia

Order Primates

Family Callitrichidae

Thumbnail description
Small-sized monkeys with claws on all digits except large toe; long non-prehensile tails; several species with elongated hairs on crown, ears, or face

Size
Head and body length: 5.5–11.4 in (14–29 cm), tail length: 7.9–15.8 in (20–40 cm); weight: 3.9–21.9 oz (110–620 g)

Number of genera, species
6 genera; 41 species

Habitat
Tropical and subtropical forests

Conservation status
Critically Endangered: 3 species; Endangered: 5 species; Vulnerable: 6 species; Data Deficient: 2 species

Distribution
South and Central America

Evolution and systematics

The family includes six extant genera: tamarins (Saguinus, 15 species), lion tamarins (Leontopithecus, 4 species), Goeldi's monkey (Callimico, 1 species), eastern Brazilian marmosets (Callithrix, 6 species), Amazonian marmosets (Mico, 14 species), and pygmy marmosets (Cebuella, 1 species). Their closest allies among the primates are the capuchins and squirrel monkeys, family Cebidae. The monotypic Goeldi's monkey (Callimico goeldii) has often been classified as a member of its own family Callimiconidae, but genetic studies demonstrate its position within the Callitrichidae as a sister-group to the clade formed by the three marmoset genera. In 2000, the Amazonian marmosets were reconsidered and placed in their own genus, Mico. This classification was based on the recognition that the pygmy marmoset is more closely related to Amazonian marmosets than to eastern Brazilian marmosets. The relative position of tamarins and lion tamarins within the Callitrichidae is still debated, with either of these genera being considered as basal within the family by different authorities.

The evolutionary history of the Callitrichidae is poorly documented. Lagonimico, from the middle Miocene (about 13.5 million years ago) of Colombia, is perhaps the earliest known fossil pertaining to the callitrichids.

Physical characteristics

The extant members of the family Callitrichidae are among the smallest primates and represent the smallest true monkeys (simian primates). Adult body mass ranges between 3.9–21.9 oz (110–620 g), head and body length between 5.5–11.4 in (14–29 cm), and tail length between 7.9–15.8 in (20–40 cm). The non-prehensile tail is always longer than the head and body combined. The head is relatively rounded and the snout only slightly pronounced. Except for lion tamarins and Goeldi's monkeys, females are usually larger than males (in contrast to the general trend in primates where males are larger than females), although to a varying degree. The coloration of the dense, silky fur varies considerably between species. Some, like the golden lion tamarins (Leontopithecus

rosalia), are very conspicuously colored, others, like Graell's black-mantled tamarins (Saguinus graellsi), are rather dull, and still others show contrasting coloration in different regions of the body. The fur may form a kind of a mantle on the shoulders or a mane in some species. Several marmosets possess ear tufts, while in a few tamarins either the beard or the hair on the crown is quite elongated. Males and females are colored alike. Claw-like nails grow on all fingers and toes except the big toe that has a flat nail. Histological studies revealed that these claws are laterally compressed nails, different from the true claws of other mammals. The thumb cannot be opposed to the other fingers, but the big toe is opposable, as in all other primates. The arms are shorter then the legs, but relative length varies between species, depending on the principal mode of locomotion. The third molar is lacking both in the upper and lower jaw; hence the number of teeth is 32. Goeldi's monkey represents the only exception: it possesses small, third molars, and thus 36 teeth. In tamarins, lion tamarins, and Goeldi's monkey the lower canines are higher then the lower incisors (long-tusked callitrichids), while in eastern Brazilian marmosets and pygmy marmosets they attain the same height (short-tusked callitrichids); Amazonian marmosets are intermediate in this character.

Distribution

The Callitrichidae have a wide distribution over tropical and subtropical South and Central America, from the Panamanian isthmus in the north to southeastern Brazil and northern Paraguay in the south. Tamarins occur in western and central Amazonia west of the Rio Madeira (although one sub-species of saddle-back tamarins, Saguinus fuscicollis, has extended its range into a small area east of the Rio Madeira), in the Guyanas and adjacent northern Brazil, and in northwestern Colombia, Panama and southeastern Costa Rica. Lion tamarins have the most restricted distribution of all genera of the family and are endemic to southeastern Brazil. Goeldi's monkey is found in western Amazonia, south of the Rio Japurá, but its exact distribution, particularly the eastern limits, is still poorly known; within the distributional range, its occurrence seems to be very patchy. Pygmy marmosets also occur in western Amazonia, south of the rivers Caquetá and Solimões and west of the Rio Madeira. Amazonian marmosets range in eastern and southern Amazonia, between the Rio Madeira in the west and the rivers Xingu and Tocantins in the east. Eastern Brazilian marmosets are distributed along the Brazilian Atlantic coast and adjacent inland areas.

Habitat

Callitrichids are mainly animals of tropical rainforests; they do, however, occupy a wide range of different habitats. Tamarins and the Amazonian marmosets are typically found in high-ground primary rainforest interspersed with patches of secondary vegetation, caused by natural disturbances (tree falls). Secondary forests provide a different spectrum of fruit and may also bear a higher abundance of insects, making them highly attractive for prey foraging. Some species may also persist in secondary forests with little or no remaining primary vegetation, and close to human settlements. Pygmy marmosets are preferably found in seasonally inundated and riverine forests. Goeldi's monkey mainly ranges in forest with dense undergrowth, such as those found in bamboo forests. Such habitat may occur in widely spaced patches, which is probably one of the reasons why groups and populations of this species may be separated from each other. Tamarins of northwestern Colombia and Central America are also found in relatively dry and semi-deciduous forests. Lion tamarins occur in coastal rainforests and in the often drier inland extensions of the Atlantic forests of eastern Brazil. Eastern Brazilian marmosets live in Atlantic coastal forests, gallery forests, and in forest patches within open habitats like the Cerrado and Caatinga (Brazil) and Chaco (Paraguay and Bolivia).

Behavior

All marmosets and tamarins live in groups. Group sizes range between 3–15 individuals, but most species are typically found in groups of 4–9. Groups of two animals usually represent migrating individuals without a home range or incipient groups. On average, group size is smaller in tamarins and lion tamarins compared to Amazonian and eastern Brazilian marmosets. Large groups of 20 or more individuals reported in the literature most likely represent the temporal association of two or more neighboring groups.

Based on captive findings where keeping an adult pair together with their non-breeding offspring was the most stable situation, marmosets and tamarins have traditionally been classified as living in family groups. However, callitrichid social organization is much more complex in the wild. In the best-studied species—that of the saddleback tamarin—social organization varies within populations, with groups being composed of one adult female plus two or more adult males, one adult female plus one adult male, one adult male plus two or more adult females, and two or more adults of both sexes plus immature individuals. During its existence, a single group may pass through these different forms of organization. Other species for which long-term data are available—like the common marmoset (Callithrix jacchus) and the moustached tamarin (Saguinus mystax)—have also been reported to be highly flexible in their social organization.

All tamarins and marmosets are diurnal and usually leave their sleeping sites at sunrise. The length of their daily activity period is, however, variable between species. Moustached tamarins and saddleback tamarins are active for ten hours and retire on average two hours before sunset, while pygmy marmosets (Cebuella pygmaea) and common marmosets are active for 11–12 hours, almost until dusk. Many species sleep in dense tangles of vines and epiphytes, but the base of palm fronds or the forking of trunks and large branches are also used. Saddleback tamarins and lion tamarins make intensive use of tree hollows, while moustached tamarins have never been observed in this kind of shelter.

Home-range size is highly variable both within and between species. The smallest home ranges are found in pygmy marmosets, which occupy areas of 0.25–1.24 acres (0.1–0.5 hectares). They are centered upon one or a few major sources of plant exudates; once these sources have been exhausted, pygmy marmoset groups shift to another area. In marmosets of the genera Callithrix and Mico, home-range size is related to the relative importance of exudates in their diet: highly exudativorous species usually occupy much smaller ranges (1.2–16.1 acres [0.5–6.5 hectares] in common marmosets, 3.2–11.1 acres [1.3–4.5 hectares] in black tufted-ear marmosets, Callithrix penicillata) compared to the less exudativorous species (27–40 acres [11–16 hectares] in buffy tufted-ear marmosets, Callithrix aurita, and about 69 acres [28 hectares] in the Aripuanã marmoset, Mico intermedius). In tamarins, home-range size varies between 20 acres [8 hectares] and almost 495 acres [200 hectares], but reasons underlying this variation are less well known; it is likely to be related to the productivity of the habitat. The largest home ranges for any callitrichid have been reported for golden-rumped lion tamarins (Leontopithecus chrysopygus) who may range over 682 acres [276 hectares].

The overlap between home ranges of neighbors also varies between species and populations. Home ranges of pygmy marmosets and Goeldi's monkey do not overlap and may not even be contagious, while in golden lion tamarins overlaps of up to 60% have been observed. Neighboring groups meet and interact in these overlap areas regularly, normally during the first hours of the day. Interactions may be aggressive, including chasing and fighting, but may also include friendly interactions like grooming and playing; in common marmosets, saddleback tamarins, and mustached tamarins, individuals from neighboring groups have been observed to be involved in sexual interactions. While the function of these between-group encounters is often seen as resource defense, it also provides the opportunity for immature individuals and non-breeding adults to familiarize with potential mates from neighboring groups. Additionally, during between-group encounters animals may migrate from one group to another without an intervening solitary phase.

Within-group social behavior is characterized by much affiliation. Social grooming is the most frequent interaction and

is usually performed during prolonged resting periods. It is usually the adult and subadult group members who are involved in grooming, and the breeding female of a group can be the primary focus of the grooming activity. One individual laying down in front of another one and presenting the body in a posture not taken during solitary resting often initiates a grooming session. Apart from grooming, animals also huddle together for extended periods. While adults and subadults are grooming, youngsters are involved in social play, which involves chasing each other to-and-fro, grabbling, wrestling, and smooth, inhibited biting. Aggressive behavior between group members is generally rare and limited to threats and displacements. It may occur in small food resources that cannot accommodate several individuals; severe aggression with fighting is extremely rare in the wild.

Callitrichids are highly vocal animals. In the wild, marmosets and tamarins can best be detected by listening to their calls. All species possess a long call, a vocalization of high intensity that is audible to the human ear over a distance of at least 500–650 ft (150–200 m). Long calls are composed of two

or more (up to about 30) notes, and are different between species, populations, and individuals; within an individual, the structure of long calls may also vary according to social context. Long calls function in intragroup cohesion and in the regulation of space between neighboring groups; in tamarin mixed-species troops they also function in the establishment of association. Long calls are most often heard in the early morning and usually precede and accompany encounters between neighboring groups.

Apart from long calls, all marmosets and tamarins possess a diversity of other calls. Specific alarm calls are emitted upon seeing a raptorial bird. Other group members (and even members of other species) "understand" these calls and may react in the appropriate way without seeing the raptor itself. Infant and juvenile tamarins utter squawks when soliciting and stealing food from another group member. Harsh and atonal calls are given during aggressive interactions. Many vocalizations are related to the cohesion of the group and coordination of activity. Pygmy marmosets vary the structure of their trills in relation to the distance to the nearest group member. In golden lion tamarins, different calls provide information about the sender's current location, activity, and intention.

Playback experiments with naturally recorded and with synthesized vocalizations revealed that pygmy marmosets show categorical perception, and that they respond to individual and contextual differences. Learning seems to be involved in the development of the vocal repertoire in marmosets and tamarins, since infants "babble" intensively and use vocalizations out of their proper context.

In contrast to most other simian primates, olfactory communication, that is communication by means of scent signals, plays an important role in the social life of marmosets and tamarins. Most callitrichids are equipped with scent glands in areas on and around the genitals (anogenital or circumgenital glands), on the lower abdomen above the genitals (suprapubic glands), and on the midline of the chest (sternal gland). The secretions of these glands consist of highly complex mixtures of fatty acids and their esters, proteins, and other organic compounds. Alone or mixed with urine, these secretions contain information about species and subspecies, sex, reproductive state, and individual identity of the sender. Scent gland secretions are applied to the environment through ritualized rubbing movements. Depending on the type of gland employed, this behavior is called anogenital, suprapubic, or sternal scent marking. The frequency with which the different types of scent marking behavior are employed varies between species. In most species, anogenital marking is the dominant mode, but in the Aripuanã marmoset suprapubic marking prevails, and black-mantled tamarins, Saguinus nigricollis, most often use sternal marking.

Usually, scent gland secretions are applied to branches, trunks, and lianas, but some species also mark members of their group. In saddleback tamarins this behavior culminates in scent-marking "parties" where most or all group members mark each other and objects of the environment for 2–3 minutes. The sympatric moustached tamarin lacks this kind of performance. Reasons for such interspecific variation are suggested to rest in subtle differences in the social structure and mating strategies.

In tamarins, adult females scent mark significantly more than adult males, while in lion tamarins and marmosets, rates of scent marking are usually balanced between sexes or may be male-biased as in golden-headed lion tamarins, Leontopithecus chrysomelas. In common marmosets, Aripuanã marmosets, saddle-back tamarins, and moustached tamarins scent marking is performed throughout the home range, and the spatial distribution of scent marks usually follows the patterns of home-range use. While this does not completely exclude a territorial function of scent marking, it is more consistent with a function in intragroup communication. In common marmosets scent marking by subordinate females may serve in the attraction of potential mates from neighboring groups.

In a few tamarin species urine washing has been observed, a behavior known from several other New World primates, particularly from squirrel monkeys (Saimiri). The behavior is, however, very rare and its function not known. Another behavior pattern related to olfactory communication is the

anointing of the tail with scent-gland secretions and urine, as observed in Goeldi's monkey.

Marmosets and tamarins also employ visual signals in social communication. When they are aroused, the hair on the head, ears, shoulders, or the whole body is raised. This is particularly notable in species that possess hairy ornaments like the long crown hair of cotton-top tamarins (Saguinus oedipus) and the ear tufts of several marmoset species. Facial expressions like frowning, open mouth threats, and head shaking, are used in agonistic interactions. When threatening another individual—whether in their own group or in another group—several marmoset species turn around, lift their tail, and display their genitals. Lion tamarins and marmosets walk with an arched back and raised hair during agonistic interactions and in situations of social tension.

Due to their small body size, callitrichids are susceptible to a wider array of predators than larger primates. Successful and unsuccessful attacks by raptorial birds—Guianan crested eagles (Morphnus guianensis), ornate hawk eagles (Spizaetus ornatus), bicolored hawks (Accipiter bicolor)—and snakes—anacondas (Eunectes murinus), rainbow boas (Boa constrictor), jararacas (Bothrops jararaca)—have been witnessed. Tayras (Eira barbara) have been seen carrying dead tamarins in their mouths and hairs of tamarins were found in feces of ocelots (Felis pardalis). Callitrichids respond to predators by alarm calling, escaping, and hiding. If a raptor attacks while animals are exposed in an open tree crown and no escape to dense vegetation is possible, they may let themselves drop as a last resort. Once a predator has been detected and can no longer hunt by surprise, marmosets and tamarins may approach and intensively mob the predator with specific vocalizations. Saddleback tamarins have been observed striking at a resting snake, and moustached tamarins were observed attacking a rainbow boa in order to rescue a group member.

As a counterstrategy against being surprised by a predator, marmosets and tamarins are constantly vigilant. They frequently interrupt their ongoing activity to scan the surroundings. Adult male marmosets and tamarins perform such vigilance more often than other group members.

In areas south of the Amazon, saddle-back tamarins form mixed-species troops (interspecific associations) with sympatric congeners, either moustached tamarins, red-bellied tamarins (Saguinus labiatus), or emperor tamarins (Saguinus imperator). In these troops, one group of saddlebacks and one group of the other tamarin species spend much of their active time together and jointly exploit plant resources, and their home ranges overlap almost completely. The species separate for the night, and contact is often re-established the next morning by means of long calls. Although species participating in mixed-species troops use all layers of the forest from the ground to the emergent trees, the smaller saddle-back tamarins range on average at lower heights than the associated larger species. Species forming mixed-species troops also differ in their strategies of foraging for prey. In northern Bolivia, Goeldi's monkeys regularly participate as the third party in associations of saddleback tamarins and red-bellied tamarins. Members of the different species in a mixed-species troop rarely interact directly with each other. If such interactions occur, they are usually agonistic and involve displacements or mild aggression by a member of the larger species

towards a member of the smaller species. Agonistic interactions mainly occur in food resources of limited size. There are also friendly interactions between members of the associated species, and particularly juveniles and subadults have been observed playing intensively.

Major benefits of mixed-species troops are seen in increased safety from predators and increased foraging efficiency. By associating with another species, group size is increased without compromising the social organization and mating patterns. Increased group size may reduce the risk for each individual of being the target of an attacking predator. Studies on associations of moustached and saddleback tamarins on the Urucu River in Brazilian Amazonia have revealed that the two species may also benefit from a "division of labor" with regard to their vigilance: moustached tamarins, which use higher strata of the forest, are more likely to detect aerial threats, while saddleback tamarins use lower strata of the forest and are more likely to detect threats coming from below. Saddleback tamarin may also derive a benefit from the association by capturing prey that has been flushed by and escaped from mustached tamarins.

Like most New World monkeys and unlike Old World monkeys and apes, all callitrichid males and one-third of the females are dichromats, that is, they can only distinguish two colors, while two-thirds of the females are trichromats, that is, they possess normal color vision. While the gene for the short wavelength is located on chromosome 7, the genes coding for the middle and long wavelength are located on chromosome X. Having only one chromosome X, males possess only two different color vision genes. Whether females are dichromat or a trichromat depends on whether they are homozygotous or heterozygotous at the respective gene locus on the chromosome X. The reasons for the maintenance of this polymorphic color vision system are unknown. It has been suggested that trichromats are better at detecting ripe fruits, while dichromats may have an advantage in detecting camouflaged prey and predators.

Feeding ecology and diet

All callitrichids include fruit, gums and other plant exudates, and insects in their diet. Most species also feed on nectar, other arthropods (e.g., butterflies and spiders), and small vertebrates (e.g., frogs, lizards, bird eggs, and nestlings). Leaves and buds are very rarely consumed. The relative proportion of different dietary components varies considerably between species. Eastern Brazilian marmosets and pygmy marmosets rely heavily on plant exudates that they procure by gouging through the bark of trees and lianas, a behavior facilitated by their short-tusked condition. Amazonian marmosets are also able to gouge, but depend on plant exudates much less than the other marmosets. Given their long-tusked condition, tamarins and lion tamarins cannot gouge and rely on exudate flow stimulated by damage of the bark through

such things as windbreak and wood-boring insects. In contrast to marmosets, their diet is dominated by a high diversity of fruits; saddleback tamarins and moustached tamarins may include up to about 150 different fruit species in their diet. The spectrum of fruits ranges from soft, tiny berries of less than 0.2 in (0.5 cm) in diameter to large, leathery legume pods of more than 12 in (30 cm) in length. Tamarins swallow the seeds of many of the plant species whose fruits they consume and void them with their feces after the adhering pulp has been fully or partially digested. These seeds remain viable after gut passage; tamarins thus contribute to seed dispersal and to the natural regeneration of the forest. Many of the swallowed seeds are large (diameter up to 0.4 in [1 cm], length 0.6–0.8 in [1.5–2 cm]) in relation to tamarin body size, and it has been suggested that this habit possesses a curative function (displacement of gastro-intestinal parasites and stimulation of gut motility).

During seasonal shortages in fruit availability, nectar or gum may become the principal dietary alternative for frugivorous species. Goeldi's monkeys exploit fungi as an alternative diet during periods of reduced fruit availability. In contrast, fungi are an important dietary component throughout the year for buffy tufted-ear marmosets. In saddleback tamarins and emperor tamarins nectar may account for 50–75% of all plant food consumed during periods of fruit scarcity.

Strategies for the search and capture of insects and other prey vary between species. Lion tamarins and saddleback tamarins are mainly manipulative foragers. They probe with their hands (which are particularly elongated in lion tamarins) into tree holes and crevices, break up dead bark, turn around leaf litter, and dip into bromeliads to obtain hidden prey. Most other tamarins and the marmosets are "surface gleaners" that obtain camouflaged prey from the surface of leafs and branches; they stealthily approach this prey and then rapidly snatch or grab. For many callitrichids, foraging for prey is the most time-consuming activity, accounting for up to about 45% of the waking hours, and katydids are the top prey for most species. When capturing a katydid, the first bite is directed towards the head; thus they avoid being bitten by the often formidable mandibles.

Differences in prey foraging strategies are an important factor for the sympatric co-existence of different tamarin species and for the formation of mixed-species troops. By searching for and capturing prey at different strata of the forest and with different techniques, saddleback tamarins and moustached tamarins overlap much less in the spectrum of their principal prey items (katydids) in comparison to the plant component of their diet; saddleback tamarins also capture more lizards and other small reptiles, while mustached tamarins feed more often on frogs.

Several marmoset species and saddleback tamarins also forage over swarms of army ants and capture insects and other arthropods that try to escape from the ants.

Reproductive biology

As with social organization, the mating system of callitrichids is quite variable, both within and between species.

In all marmosets and tamarins (once again with the exception of Goeldi's monkey) each group includes only a single breeding (dominant) female, which may mate with a single male (monogamy), or with two or more males (polyandry). While monogamy is found in all callitrichids, polyandry has been observed in saddleback and moustached tamarins, golden lion tamarins, Aripuanã marmosets, and pygmy marmosets. Breeding by multiple females is the norm in Goeldi's monkey, but also occurs in different tamarin species, in golden lion tamarins, and in common marmosets. In golden lion tamarins, secondary breeding females are usually the daughters of the primary breeding female, but their rearing success is much lower. In common marmosets, dominant females have even been observed committing infanticide; that is, actively killing the infants of other breeding females in their group. This behavior has been related to the competition for resources, particularly helpers for infant care.

In captivity, the limitation of breeding to a single female in each group is based on the lack in subordinate females of fertile ovarian cycles in marmosets and tamarins, and the

dominant female's interference with matings between subordinate females and males in golden lion tamarins. It has been suggested that olfactory cues (pheromones) released by breeding females through scent marking "suppress" ovarian cycling in subordinate females. However, the presence of ovarian cycles in subordinate females and of multiple breeding females in groups suggest that the mechanism is much more complex and that subordinate females play an active role in determining whether or not they will breed.

Callitrichid mating behavior is rather inconspicuous. In many species, for example, in moustached tamarins and in pygmy marmosets, copulations are not preceded by any soliciting behavior, while in common marmosets tongue flicking may initiate copulations. There is no external sign of estrus, although some swelling of the vulva during the supposed receptive phase has been observed in wild mustached tamarins. During the receptive period of the female estrus cycle, males are often more closely associated with females than during other times. During this period, males also perform more genital controls by sniffing and licking the genitals and the urine of females. In captivity, pygmy marmoset and cotton-top tamarin males are able to detect the receptive period through olfactory signals, and it is likely that the same is true for other species and in the wild. Golden lion tamarin males increase their body mass in the month before the highest probability that females come into estrus, and mustached tamarin males have larger testes during the months when most conceptions occur.

In captivity, all callitrichids may give birth twice per year. However, in the wild this has been observed regularly only in marmosets and in pygmy marmosets. In most tamarins and in golden lion tamarins normally only one birth per year occurs. In these species, births peak during 2–3 months, mainly in the early and middle wet season. Through this timing of births, the energetically costly lactation and carrying of infants and the critical process of weaning take place during periods of high fruit availability. In golden lion tamarins, a female may give birth a second time only if the first birth took place early in the birth season.

The duration of pregnancy varies between 129 days in golden lion tamarins and 183 days in cotton-top tamarins, but for most marmosets and tamarins it is around 145–150 days. All callitrichids except for Goeldi's monkey give birth to dizygotic twins. Births take place during the night. At birth, the combined body mass of twins accounts for up to 20% of maternal body mass, which is among the highest proportion in mammals and the highest in primates except for tarsiers. The infants are carried on the back, and most or all adult and subadult group members may participate in infant carrying. In

tamarins, it is the adult males who carry the infants most of the time, often from the day of birth on, while in lion tamarins and common marmosets infant carrying is more evenly shared between mothers and fathers or other adult males. In Goeldi's monkey, infants are first carried by group members other than the mother only from about the second week of life on.

Carrying the heavy offspring is a strong, energetic burden. Studies of captive cotton-top tamarins have shown that carrying males may lose up to 10% of body mass in the weeks after the birth of infants, even though they do not have to travel and search for food. It is thus evident that in the wild, where tamarins may have to travel 0.6–1.2 mi (1–2 km) per day to find sufficient food, infant carrying represents a considerable cost to the caregivers. In pygmy marmosets, infants may be "parked" at protected places after the second week of life, and may spend most of their waking hours on their own. This behavior is unique among simian primates (while many lemurs, lorises, and tarsiers park their infants routinely), and only feasible because the activities of pygmy marmosets are usually focused around a single major food resource.

Infant callitrichids make the first short excursions from the back of a carrier and take the first solid food during the third or fourth week of life, but continue to suckle milk from the mother until the end of the third month. Locomotor independence is also attained by the end of the third month, although even at a later age infants may be picked up and carried by an adult group member in threatening situations or when the group has to travel very fast.

Apart from carrying, the cooperative rearing system of callitrichids includes the transfer of food from adults and subadults to infants. Infants approaching another group member and emitting a squawk, and then taking the food item, can initiate this transfer. In a number of species (e.g., golden lion tamarins and in buffy-headed marmosets, Callithrix flaviceps), animals in possession of a food item may also initiate the transfer; that is, a specific chattering vocalization is emitted in order to attract the infant. Items transferred include animal prey or opened fruits that are otherwise difficult for infants to process. The frequency of food transfer and the willingness of the food possessor to concede decrease with increasing age of the offspring and cease after the first year of life. Sexual maturity is attained between 12–24 months of age; marmosets (except pygmy marmosets) and Goeldi's monkey are matured at an earlier age than tamarins and lion tamarins.

Conservation status

The family includes very common and widely distributed species that are not threatened, but also a number of Critically Endangered, Endangered, and Vulnerable species with very restricted and shrinking distributional ranges. With perhaps fewer than 350 individuals remaining, the black-faced lion tamarin (Leontopithecus caissara) is among the 25 most endangered primate species. The principal reason for declining populations is the ongoing destruction of suitable habitats. In the past, several species (e.g., cotton-top tamarins) have also suffered from heavy trapping of wild animals for exportation to the Northern Hemisphere, both as laboratory animals and as pets. While large-scale trade-trapping has been banned, illegal activities continue. For Critically Endangered species like the lion tamarins, even the removal of a few individuals from the already reduced wild populations represents a substantial loss.

Ironically, threats to marmosets and tamarins also emerge from closely related species. The common marmoset expands its range due to introduction by humans, and displaces or interbreeds with resident species. The Critically Endangered pied tamarin (Saguinus bicolor), which lives in a limited area close to the Amazonian city of Manaus, suffers from range expansion by the Midas tamarin (Saguinus midas).

Significance to humans

Common marmosets are one of the most widely used primate species in biomedical research, and cotton-top tamarins are an important primate model for the study of colitis and colon cancer. Other callitrichids like moustached tamarins and red-bellied tamarins are also used in different areas of biomedical research. Today, most marmosets and tamarins in biomedical research are captive bred. In their habitat countries, marmosets and tamarins are appreciated as pet monkeys. In the 1960s and 1970s, several species (e.g., golden lion tamarins and cotton-top tamarins) were heavily trapped and exported to the Northern Hemisphere. Due to their small body size, marmosets and tamarins are rarely hunted for food, quite in contrast to larger primate species.

Recent research has pointed to the possibility that common marmosets may represent a reservoir for rabies in Brazil.

Species accounts

List of Species

Cotton-top tamarin

Saguinus oedipus

taxonomy

Simia oedipus Linnaeus, 1758, Colombia.

other common names

French: Pinché; German: Lisztaffe; Spanish: Tití blanco.

physical characteristics

Weight: 12.4–15.9 oz (350–450 g); head and body length: 7.9–11 in (20–28 cm); tail length: 12.2–16.1 in (31–41 cm); conspicuous long white hair on the crown.

distribution

Northwestern Colombia, between Rio Magdalena and Rio Atrato.

habitat

Tropical rainforest, seasonally dry tropical forest.

behavior

Cotton-top tamarins usually live in groups of 3–10 individuals, including 1–2 adults of each sex and immature offspring of different ages. Both sexes may disperse and join neighboring groups. Home-range areas are 19–25 acres (7.8–10 ha),

and daily path length is 0.9–1.1 mi (1.5–1.7 km). The diverse and complex vocal repertoire includes long calls of much lower frequency (1–1.5 kilohertz) than those of tamarin species distributed in Amazonia. Scent-marking involves the anogenital and suprapubic glands, sternal marking is extremely rare. The conspicuous crown hair is raised when animals are agitated.

feeding ecology and diet

Cotton-top tamarins are primarily frugivorous and insectivorous, but complement their diet with exudates, nectars, and small vertebrates. They use all strata of the forest during feeding and foraging, and may also come down to the ground to feed on fallen fruits.

reproductive biology

Breeding is usually restricted to a single female per group, but groups with two pregnant females have been observed. Whether females mate with more than one adult male is not known. Estrus cycle duration is 23–25 days, and gestation length is 180–185 days (longer than other tamarin species). Usually one birth per year takes place between March and June, if pregnancies fail or if infants die, females may conceive a second time and give birth later in the year. Infants are mainly carried by adult males.

conservation status

Cotton-top tamarins are Critically Endangered due to ongoing habitat destruction and trapping.

significance to humans

Used in biomedical research and popular as pets.

Saddleback tamarin

Saguinus fuscicollis

taxonomy

Midas fuscicollis Spix, 1823, Brazil. Twelve subspecies (some or most of which may represent their own species).

other common names

French: Tamarin à dos brun; German: Braunrückentamarin; Spanish: Bebeleche (Colombia), chichico (Ecuador), pichico (Peru).

physical characteristics

Weight: 10.2–14.8 oz (290–420 g); head and body length: 7.9–10.6 in (20–27 cm); tail length: 11.4–15 in (29–38 cm). It is the smallest member of the genus. Fur occurs on the dorsal side of the head and body tripartite, with an agouti-colored saddle in the middle.

distribution

Central and western Amazonia.

habitat

Tropical rainforest.

behavior

Saddle-back tamarin groups comprise 3–10 individuals, with 1–2 adults of each sex, and immature individuals of different ages. Home-range size varies between 25–495 acres (10–200 ha), according to population. Most or all group members at the same place perform scent marking throughout the home range, often simultaneously. In areas of sympatry, saddle-back tamarins form mixed-species troops with mustached tamarins, red-bellied tamarins, and emperor tamarins. East of the Rio Madeira, saddleback tamarins have also been observed in association with a marmoset species.

feeding ecology and diet

Saddle-back tamarins are primarily frugivorous and insectivorous, but supplement their diet with exudates, nectar, small vertebrates, and soil from arboreal termite mounds. Depending on availability, nectar or exudates may become the dietary staples when fruits are scarce. They search for prey in the leaf litter, and dip into tree holes, crevices, and bromeliads.

reproductive biology

Flexible mating system includes polyandry, monogamy, and polygyny. Reproduction is moderately seasonal, usually one birth per year. Estrus cycle duration averages about 25.7 days, and gestation length is 148–152 days. Adult males are the principal carriers of infants.

conservation status

Not threatened.

significance to humans

They are kept as pets in habitat countries and used as models in biomedical research.

Golden lion tamarin

Leontopithecus rosalia

taxonomy

Simia rosalia Linnaeus, 1766, Rio de Janeiro, Brazil.

other common names

French: Singe lion; German: Goldener Löwenaffe; Portuguese: Micoleãodourado.

physical characteristics

Male weight: 21.9 oz (620 g), female weight: 21.1 oz (598 g); head and body length: 8.9–11 in (22.5–28 cm); tail length: 10.4–15.8 in (26.5–40 cm). Entirely covered with golden fur, except for a naked face.

distribution

Remnants of Atlantic coast forest in the state of Rio de Janeiro, Brazil.

habitat

Mature lowland forest, secondary forest.

behavior

Group size ranges between 2–11 individuals, most often including more than one adult of each sex. Both sexes may migrate, but may also inherit the breeding status in the natal group. Home range comprise 52–180 acres (21–73 ha), overlap with neighboring home ranges is around 60%. Groups travel between 0.8–1 mi (1.3–1.6 km) per day. Males and females scent mark with equal rates. Tree holes are preferred for sleeping.

feeding ecology and diet

Golden lion tamarins are primarily frugivorous and insectivorous, but supplement their diet with nectar, exudates, and small vertebrates; nectar may become the principal food source when fruits are scarce. Forage for prey mainly in epiphytic bromeliads, but also in dead leaves, epiphytes, tree bark, etc., using their long fingers to probe for embedded prey.

reproductive biology

Flexible mating system (monogamy, polyandry, polygyny). In groups with more than one adult male, mate guarding occurs during the receptive phase of the breeding female. Gestation length is 125–130 days and twins are the rule. Females give birth usually once per year, and breeding and births are seasonal. Adult males participate in infant carrying.

conservation status

Critically Endangered due to habitat destruction and fragmentation. Golden lion tamarins are the focus of strong conservation efforts, where protection of natural habitat, captive breeding, and reintroduction of captive-bred animals into the wild are combined.

significance to humans

Golden lion tamarins are kept as pets; one was the famous pet of Madame de Pompadour. They are featured on the back of the Brazilian 20 Reais cash note, and is the flagship species for conservation efforts in the Brazilian Atlantic region.

Golden-headed lion tamarin

Leontopithecus chrysomelas

taxonomy

Midas chrysomelas Kuhl, 1820, Bahia, Brazil.

other common names

French: Singe lion à tête d'or; German: Goldkopf-Löwenaffe; Portuguese: Mico-leão-de-cara-dourada.

physical characteristics

Male weight: 21.9 oz (620 g), female weight: 18.9 oz (535 g); head and body length: 8.7–10.2 in (22–26 cm); tail length: 13.0–15.4 in (33–39 cm). Rump with black fur; arms, part of tail, and fringe around face is golden in color.

distribution

Forest remnants in the southern part of the state of Bahia, Brazil.

habitat

Tropical rainforest in coastal region, semi-deciduous forest further inland.

behavior

Groups of 3–9 individuals, with usually two adult males and one adult female, plus immature individuals. Home-range size is 163–213 acres (66–86 ha), and groups travel 0.9–1.4 mi (1.4–2.2 km) per day. Where living in the same forest with Wied's black-tufted-ear marmoset (Callithrix kuhli), short term associations are formed.

feeding ecology and diet

Golden-headed lion tamarins are mainly frugivorous and insectivorous; the diet is supplemented with flowers, exudates from the pods of a legume, and nectar. Prey is mainly searched in epiphytic bromeliads and includes cryptic or concealed insects, but also small vertebrates and snails.

reproductive biology

Little known, probably a flexible mating system (monogamy, polyandry).

conservation status

Critically Endangered due to ongoing habitat destruction.

significance to humans

Kept as pets.

Goeldi's monkey

Callimico goeldii

taxonomy

Hapale goeldii Thomas, 1904, Acre, Brazil.

other common names

French: Tamarin de Goeldi; German: Springtamarin; Portuguese: Mico-de-Goeldi; Spanish: Chichico diablo (Colombia), supay pichico (Peru).

physical characteristics

Average male weight: 12.9 oz (366 g), female weight: 12.5 oz (355 g) (both in the wild); male weight: 19.5 oz (554 g), female weight 18.6 oz (526 g) (both in captivity); head and body length: 8.4–9.2 in (21.3–23.4 cm); tail length: 10.6–12.8 in (27–32.4 cm). Fur is entirely black; the only callitrichid with 36 teeth.

distribution

Patchily distributed in western Amazonia, south of the Rio Japurá.

habitat

Tropical rainforest with dense undergrowth, bamboo forest.

behavior

Groups include 2–9 individuals; 1–3 adult males and females per group. Home-range size is 198–370 acres (80–150 ha); home ranges of different groups are not contagious. They are frequently found in mixed-species troops with saddle-back tamarins and red-bellied tamarins, often occupying the lowest levels of the forest when in association.

feeding ecology and diet

Goeldi's monkeys are basically frugivorous and insectivorous, but fungus may become the dominant dietary item during several months of fruit scarcity. Prey foraging in the understory on thin branches, but also in the leaf litter; orthopterans are the principal prey item.

reproductive biology

Flexible mating system (monogamy, polyandry). Groups include 1–2 breeding females, each of which gives birth to a single infant. Estrus cycle duration is 23–24 days, gestation length is 147–157 days. Breeding is perhaps seasonal, with possibly two births per year. Mothers are the principal carriers of infants.

conservation status

Vulnerable. Threatened by habitat destruction, at least in the southern part of its geographic range.

significance to humans

Little is known even by local people; they are occasionally kept as pets.

Common marmoset

Callithrix jacchus

taxonomy

Simia jacchus Linnaeus, 1758, Pernambuco, Brazil.

other common names

French: Ouistiti à toupet blanc; German: Weisspinselaffe; Portuguese: Sagüi-do-nordeste.

physical characteristics

Average weight: 11.3 oz (320 g); head and body length: 7.3–9.8 in (18.5–25 cm); tail length: 11.6–13.8 in (29.5–35 cm). They display prominent white ear tufts.

distribution

Northeastern Brazil; introduced in eastern and southeastern Brazil.

habitat

Coastal forest, gallery forest, forest patches in open Caatinga and Cerrado bush land.

behavior

Group size ranges between 3–15, with usually several adults of both sexes plus immature individuals. Home-range size is 1.2–16.1 acres (0.5–6.5 ha), daily path length is 0.3–0.6 mi (0.5–1 km). Home range overlap with neighboring groups is variable. Encounters between neighboring groups are frequent, usually initiated by long calling. Most interactions between members from different groups are hostile, involving chasing and genital displays, but copulations between members from different groups have also been observed during these encounters. Within-group social relations are highly affiliative. Grooming is the major social activity, and breeding adults are most frequently involved in grooming interactions. Aggression

between group members is rare in the wild and usually occurs only during feeding in exudates trees. In the dominance hierarchy, the breeding adults are at the top, and the non-breeding group members are arranged according to age with older individuals ranking higher than younger ones.

feeding ecology and diet

Common marmosets feed primarily on exudates and insects; eating only a little fruit and occasionally small vertebrates. Exudate flow is stimulated through gouging into the tree bark.

reproductive biology

They usually breed in monogamous pairs, but breeding by two females in the same group is quite common in the wild. Genetic data suggest that only one male breeds in a group. Despite observation of copulations between males and females from different groups, no infants seem to be fathered by extra-group males. Estrus cycle duration is 28–29 days, and gestation length is 141–146 days. In captivity, subordinate females do not show an estrus cycle. Two births per year are common both in captivity and in the wild. When two females are breeding simultaneously in the group, rearing success is lower in the subordinate female; even killing of subordinate female infants by the dominant female has been observed in a wild population. Adult males and other group members participate in infant carrying.

conservation status

Not threatened.

significance to humans

One of the most widely used laboratory primates; also kept as pets. They have been introduced to areas outside their natural range.

Buffy-headed marmoset

Callithrix flaviceps

taxonomy

Hapale flaviceps Thomas, 1903, Espírito Santo, Brazil.

other common names

French: Ouistiti à tête jaune; German: Gelbkopfbüschelaffe; Portuguese: Sagüi-da-serra.

physical characteristics

Average weight: 14.3 oz (406 g); head and body length: 8.7–9.8 in (22.2–24.8 cm); tail length: 11.7–13.8 in (29.8–35 cm); Fur appears on the head and ear tufts are buffy-yellowish in color.

distribution

Forest remnants in the states of Espírito Santo and Minas Gerais.

habitat

Seasonal, altitudinal Atlantic coastal forest.

behavior

Group size varies between 5–15; a single group that was monitored over six years living together included 11–15 individuals; 3–6 adult males, and 1–6 adult females. Home-range size is around 88 acres (35.5 ha), and daily path length is about 0.75 mi (1.2 km).

feeding ecology and diet

Buffy-headed marmosets feed primarily on exudates and insects; exudates are procured through gouging on tree bark. However, they often eat more fruit when it becomes more abundant in their highly seasonal habitat.

reproductive biology

Despite the large number of adult females that may live in a group, only one of them breeds. A daughter may inherit the position of the breeding female, while the mother still remains in the group and contributes to infant care, along with other adult and subadult group members. Mating is monogamous, but mating with more than one male (polyandry) is suspected. Two births per year is normal, and probably seasonal.

conservation status

Endangered. Habitat fragmentation and loss are the major threat.

significance to humans

Often captured for the pet trade; this species is also a draw for ecotourists.

Aripuanã marmoset

Mico intermedius

taxonomy

Callithrix humeralifer intermedius Hershkovitz, 1977, Rio Aripuanã, Brazil.

other common names

French: Ouistiti à camail; German: Weissschulterseidenaffe; Portuguese: Sagüi-de-Aripuanã.

physical characteristics

Average head and body length: 9.4 in (24 cm); tail length: 12.6 in (32 cm). The head and upper half of the body is creamy white, while the lower half is brown.

distribution

Brazilian Amazonia, between Rio Aripuanã and Rio Roosevelt.

habitat

Tropical rainforest, both in mature and secondary vegetation.

behavior

Groups are normally between 4–13 individuals, usually including more than one adult of each sex. Home-range size is around 69 acres (28 ha), overlap with neighboring groups is around 22%. Daily path length is 0.5–1.3 mi (0.8–2.1 km). Scent marking performed most frequently with suprapubic gland, but sternal marking is also quite common, and by both sexes with similar rates. Scent marks are distributed throughout home range, but more in peripheral areas, and also more often during encounters with neighboring groups.

feeding ecology and diet

They primarily feed on fruits and arthropods; exudates are much less important than in eastern Brazilian marmosets, and tree gouging rarely employed. Occasionally small vertebrates are taken. They have been observed to forage over swarms of army ants (Eciton burchelli).

reproductive biology

Mating is not confined to a single pair, but several adult males and females have been seen copulating. However, only a single female gives birth. Births occur seasonally, with two peaks at the end of the dry season and the second half of the wet season. Adult males and other group members participate in infant carrying.

conservation status

Not threatened.

significance to humans

None known.

Pygmy marmoset

Cebuella pygmaea

taxonomy

Jacchus pygmaeus Spix, 1823, Tabatinga, Brazil. Two subspecies.

other common names

French: Ouistiti mignon; German; Zwergseidenaffe; Spanish: Leoncito (Peru, Ecuador), mono de bolsillo (Colombia).

physical characteristics

Average male weight: 3.9 oz (110 g), female weight: 4.3 oz (122 g); head and body length: 5.4–6 in (13.6–15.2 cm); tail length: 6.8–9 in (17.2–22.9 cm). Coat is yellow-brown; tail has faint rings. It is the smallest New World monkey.

distribution

Western Amazonia, south of the rivers Caquetá and Solimões and west of the Rio Madeira.

habitat

Tropical rainforest, prefers seasonally inundated and riverine forest.

behavior

Groups include 2–9 individuals, with usually a single adult pair and their offspring. Both sexes disperse from their natal group. They occupy very small home ranges (0.25–1.25 acres; 0.1–0.5 ha), which are shifted once the exudate yield of the principal feeding tree has dropped below a critical level. Neighboring home ranges are usually not contagious. Genital display is used as an aggressive signal towards other individuals (both within and between groups) and human observers.

feeding ecology and diet

They feed mostly on exudates of over 60 plant species and on arthropods; fruits are of little importance. They gouge 0.4–0.8 in (10–20 mm) wide and 0.2–0.7 in (4–18 mm) deep holes into the bark with specialized dentition to stimulate exudate flow. Foraging for prey in the crowns of small-to medium-sized trees often occurs, but occasionally they also forage on the forest floor.

reproductive biology

Usually monogamous. Estrus cycle duration is 27–28 days, gestation length is 135–146 days. Births occur throughout the year, but peak around May-June and October-January. Infants are carried by mothers and other group members, but also parked at safe sites.

conservation status

Not threatened.

significance to humans

Sometimes kept as pets.

Resources

Books

Goldizen, A. W. "Tamarins and Marmosets: Communal Care of Offspring." In Primate Societies, edited by B. B. Smuts, D. L. Cheney, R. M. Seyfarth, R. W. Wrangham, and T. T. Struhsaker. Chicago: University of Chicago Press, 1986.

Hershkovitz, P. Living New World Monkeys (Platyrrhini), Volume 1. Chicago: University of Chicago Press, 1977.

Heymann, E. W. "The Number of Adult Males in Callitrichine Groups and its Implications for Callitrichine Social Evolution." In Primate Males, edited by P. M. Kappeler. Cambridge, U.K.: Cambridge University Press, 2000.

Kleiman, D. G. The Biology and Conservation of the Callitrichidae. Washington, DC: Smithsonian Institution Press, 1977.

Kleiman, D. G., and A. B. Rylands. Lion Tamarins: Biology and Conservation. Washington, DC: Smithsonian Institution Press, 2002.

Mittermeier, R. A., A. B. Rylands, A. F. Coimbra-Filho, and G. A. B. Fonseca. Ecology and Behavior of Neotropical Primates, Volume 2. Washington, DC: World Wildlife Fund, 1988.

Norconk, M. A., A. L. Rosenberger, and P. A. Garber. Adaptive Radiations of Neotropical Primates. New York: Plenum Press, 1996.

Peres, C. A. "Territorial Defense and the Ecology of Group Movements in Small-bodied Neotropical Primates." In On the Move. How and Why Animals Travel in Groups, edited by S. Boinski and P. A. Garber. Chicago, IL: University of Chicago Press, 2000.

Rylands, A. B. Marmosets and Tamarins. Systematics, Behaviour, and Ecology. Oxford, U.K.: Oxford University Press, 1993.

Periodicals

Garber, P. A. "One for All and Breeding for One: Cooperation and Competition as a Tamarin Reproductive Strategy." Evolutionary Anthropology 6 (1997): 187–199.

Goldizen, A. W., J. Mendelson, M. van Vlaardingen, and J. Terborgh. "Saddle-back Tamarin (Saguinus fuscicollis) Reproductive Strategies: Evidence from a Thirteen-year Study of a Marked Population." American Journal of Primatology 38 (1996): 57–83.

Heymann, E. W., and H. M. Buchanan-Smith. "The Behavioural Ecology of Mixed-species Troops of Callitrichine Primates." Biological Reviews 75 (2000): 169–190.

Martin, R. D. "Goeldi and the Dwarfs: The Evolutionary Biology of the Small New World Monkeys." Journal of Human Evolution 22 (1992): 367–393.

Rylands, A. B. "Habitat and the Evolution of Social and Reproductive Behavior in Callitrichidae." American Journal of Primatology 38 (1996): 5–18.

Rylands, A. B., H. Schneider, A. Langguth, R. A. Mittermeier, C. P. Groves, and E. Rodriguez-Luna. "An Assessment of the Diversity of New World Primates." Neotropical Primates 8 (2000): 61–93.

Snowdon, C. T. "Vocal Communication in New World Monkeys." Journal of Human Evolution 18 (1989): 611–633.

Sussman, R. W., and W. G. Kinzey. "The Ecological Role of the Callitrichidae." American Journal of Physical Anthropology 64 (1984): 419–449

Organizations

Golden Lion Tamarin Conservation Program. Rodovia BR 101, Km 214, Casimiro de Abreu, RJ, CEP 28.860-970 Brazil. Phone: +55 22 2778 2025. Fax: +55 22 2778 2025. E-mail: [email protected]. Website: <http://natzoo.si.edu/ConservationAndScience/EndangeredSpecies/GLTProgram/GLTP/AMLD.cfm>.

Eckhard W. Heymann, PhD