Natural History

Cotton-top tamarins (Saguinas oedipus) are New World monkeys that are members of the Callitrichid family. Garber (1993) lists some of the features of the Callitrichidae, including small body size, claw-like nails on all digits excluding the hallux and the consequent ability to cling to vertical supports, reproductive twinning, high birth weight, ability to reproduce twice per year, ovulation suppression in subordinate females, extensive involvement of males in infant care, and communal care for young. The white-haired bare-face tamarins that comprise the endangered S. oedipus species are endemic to northern Colombian neotropical rainforests (Rylands, Coimbra-Filho, & Mettermeier, 1993). Cotton-top tamarins live in small, stable or unstable groups of about five or six monkeys centered around the breeding pair (Snowdon & Soini, 1988). These groups may or may not be based on kinship, but are characterized by extensive cooperation and observable dominance hierarchies. This cooperation is most evident in infant care, feeding, and anti-predator strategies, and probably arose as an adaptive effort in these areas (Caine, 1993).

Tamarins are prey to birds, snakes, and nocturnal predators among other animals, and have evolved cooperative strategies to avoid them. For example, retiring before dusk and choosing roosting sites carefully are two ways of avoiding danger while sleeping. The monkeys are also able to increase their vigilance by living in small cooperative groups. Caine (1993) explains that the avoidance of predation pressure is probably the central factor promoting cooperation among groups in which the degree of relatedness may be relatively low. Since most of the tamarins’ activity is dedicated to feeding and raising young, vigilance becomes a key feature of their existence: a monkey can do only one of these activities at a time, so cooperation is beneficial for all monkeys.

In a given group of tamarins, all adult members contribute to raising young monkeys by carrying the infants for some of the time and providing the infants with food. While carrying an infant, the adult monkey depends on others in the group to be vigilant of predators, and also incurs a great cost to itself in terms of the metabolic expense of carrying extra weight and the decrease suffered in mobility. In addition, monkeys carrying infants tend to eat less, reinforcing the idea that a monkey can only do one thing at a time (Caine, 1993). Infant care is a huge burden on a family group: infants are carried over 90% of the time during the first four weeks, and over 80% of the time between four and six weeks after birth (Tardif, Harrison, & Simek, 1993), and only become young adults around 20 months of age (Yamamoto, 1993). The ovarian cycle of subordinate females is suppressed, especially in daughters of the dominant mother, presumably because it is more adaptive for subordinate females not to leave groups too early. Furthermore, the dominant female needs help raising her own offspring, and the subordinates’ contribution increases the overall fitness of the kin group. Also, young females gain essential experience in caring for young by helping the breeding monkey (Abbott, Barrett, & George, 1993).

The mating system of cotton-top tamarins is flexible, consistent with their cooperative living patterns and the fact that males and females are roughly monomorphic (Garber, 1993). For the most part, the monkeys seem to adopt a monogamous system, though "facultative" (taking place only under certain environmental conditions) polyandry is often observed. Dixson (1993) points to the tamarins’ larger relative testis weight than expected for monogamous monkeys. Caine (1993) explains that in captivity, groups of one female and two male cagemates live well together, and that in the wild, the average male-to-female ratio tends to be greater than one. These researchers hypothesize that the flexibility of the mating system is an adaptation that evolved in the monkeys to cope with variable environmental features and predation pressures. Though paternity is in question, both males in a trio contribute extensively to infant care. Caine (1993) explains that though the degree of relatedness within a group may be low, kinship often underlies polyandrous behavior, contributing to the overall cooperative nature of the group.

In addition to caring for the young, cooperation is also evident in the feeding habits of the monkeys. Due to the small gut and rapid rate of food passage, cotton-top tamarins require a diet with high levels of energy and nutrition. They rely mostly on insects (accounting for 30-77% of total foraging time), fruits and nectar (20-65%), and during some seasons, plant exudates or gums (Garber, 1993). The preferred insects are mostly large orthopterans, and the tamarins use such strategies as stealth, rummaging in small spaces and turning over leaves, and pouncing to catch their prey – largely strategies for independent feeding. The search for fruit – the source of carbohydrates and sugars – however, is primarily a cooperative effort. Tamarins tend to prefer tree species with specific characteristics, including small to moderately sized crowns, intraspecific fruiting synchrony, bearing a small amount of fruit each day, and a scattered and patchy distribution (Garber, 1993). Because of these qualities, the monkeys must exploit a set of temporally predictable fruiting tree species. Therefore, during a day, they will typically exploit one individual tree species, eating fruit from that kind of tree over the entire range (Garber, 1993). The home ranges are moderate to large in size, but the day ranges tend to be extensive relative to other animals with similar body weight. The home ranges typically overlap with major feeding sites, associated with some intergroup aggression. The large range size is related to the scattered distribution of trees (Garber, 1993). The groups travel cohesively when foraging, producing food calls and contact calls to synchronize the feeding effort. Intragroup aggression is diminished in free-ranging tamarins, and injurious aggression is rarely observed (Garber, 1993). Again, intragroup cooperation allows for monkeys to avoid predators, forage and feed, care for the young, and sleep safely; monkeys take turns accomplishing these tasks.

Cooperation is in part accomplished through the tamarin communication system, consisting of nonvocal gestures, vocal calls, and chemical messages (Epple et al., 1993). Females have a circumgenital glandular organ that produces scents. The system consists of large holocrine and apocrine glands in the suprapubic, labial, and perineal areas (Epple et a., 1993). Most of this form of communication is circumgenital marking (or "sit rubbing"). While the point of these messages is unclear, researchers have observed that females tend to do more scent marking than males, and more frequently during estrus. Tamarins can individuate conspecifics by scent (Epple et al., 1993).

Vocal calls include a variety of chirps, chatters, screams, whistles, and long calls (Snowdon, 1993). Chirps occur in a variety of contexts, primarily in response to the discovery of food or during other kinds of exploratory behavior. Chatters and screams are typically evoked by frightening stimuli and given by monkeys in alarm. Long calls, also called contact calls, consist a few long syllables with little or no frequency modulation and a low fundamental frequency that allows for the calls to travel over large distances, a feature adaptive in the neotropical rainforest and necessary for group cohesion (Snowdon, 1993). Snowdon and Soini (1988) describe some of the complexity of the tamarin communication system, observing an "apparent syntax in the sequencing of vocal interactions" during territorial encounters. For example, tamarins’ responses depend on the call they hear; responses to members of the same group escalate encounters while calls to nonmembers are usually just a replication of the original call. Non-auditory visual signals play a lesser role in tamarin communication, probably because of the difficulty tamarins have seeing each other in their habitat (Snowdon & Soini, 1988). Common displays include tongue flicking (appearing in many contexts such as aggression and mating), the hostile frowning display, and piloerection (another aggressive threat; Snowdon & Soini, 1988).

The neuroanatomy of cotton-top tamarins has not been as extensively studied as their behavioral ecology. New World monkeys tend to have the smallest brains among the arthropoid monkeys, on average (Armstrong & Shea, 1997). Brain size relative to body weight is comparable in New and Old World monkeys, but is significantly smaller in the family Callitrichidae, as is the metabolic rate (Armstrong & Shea, 1997). Most differences in the brains of Old and New World monkeys are due to differences in brain size, such as the reduced amount of cortical folding, especially in the occipital lobe, of New World primates. Old and New World monkeys also differ in sulcal patterning and in some connections and anatomical features. Callitrichidae may have larger posterior limbic regions, particularly the hippocampus, relative to other primates (Armstrong & Shea, 1997).

Studies of the visual system indicate the importance of this perceptual modality to the tamarin. As tamarins are diurnal, they have a retina with a well-defined fovea, replete with cones, specialized in discriminating color (Armstrong & Shea, 1997). Most aspects of the visual system of Old and New World monkeys are similar, and Armstrong and Shea conclude that it appears conserved among both kinds of monkeys. Studies of saddleback tamarins (Saguinus fuscicollis) reveal polymorphism for color vision, researchers finding some dichromatic and mostly trichromatic individuals (Jacobs, 1997). Tamarins tend to use visual not olfactory cues when foraging (Kinzey, 1997).

Experimental Subjects

Table 2-1 lists the 13 cotton-top tamarins used in these experiments. These monkeys were acquired from the New England Primate Research Center in Southboro, Massachusetts, and thus have lived in captivity all of their lives. They are housed together in William James Hall, Harvard University, and share a single homeroom. The colony is divided into six families, and each family occupies its own wire cage, 6 ft tall, 4.75 ft wide, and 2.4 ft deep (1.9 m³). All families are comprised of a mated pair; one family (Linguists II) has two pairs of twin offspring (two infants and two juveniles), two families (Linguists I and Anthropologists II) have one infant, and another has one adult daughter (Cognitive Scientists). Each cage contains a wooden roosting box where the tamarins sleep, and branches and platforms on which to climb. While spatially separated, the families can see each other and communicate with olfactory and auditory cues. The colony room is heated and humidified for the comfort of the tamarins.

Monkeys have free access to water, and are fed Zupreem monkey chow, insects, fruit, and nuts. Their weights are kept at their estimated ad libitum feeding levels. The monkeys participate in noninvasive behavioral experiments during the day, from 8 a.m. to 6 p.m., primarily on the weekdays. They have participated in numerous studies on communication and cognition. For example, most monkeys have learned to use simple tools, such as using canes to move food (Hauser, 1997). The tamarins also know how to open small doors (e.g., Hood, Hauser, Anderson, & Santos, 1999) and are very familiar with searching in containers filled with wood shavings (Weiss, personal communication). Other experiments in the lab have demanded that the monkeys associate various colors with different quantities of objects (Hauser, Kralik, & Zimlicki, unpublished data). Studies in our laboratory also show that the tamarins can be successfully tested in an operant paradigm, as in a study where they were able to discriminate faces from nonfaces (Weiss & Kralik, in press). Though the monkeys are not experimentally naïve, this is the first rigorous test of their foraging abilities.

For every experiment, we transport tamarins from the homeroom to experimental rooms in clear Plexiglas transport 1.5 ft³ (0.04 m³) boxes, and thus never directly handle them. After the session is over, experimenters first weigh the monkeys then return them to their home cages. At the weighing station, we record their performance and weight, the current weather conditions, and experimenter’s identity.