Natural History of the Rufous-naped Tamarin (Saguinus geoffroyi)
An Adult Male Rufous-Naped Tamarin
Saguinus geoffroyi, is the smallest monkey found in Panama, with a weight of a little more than a half kilogram and a body length averaging around 24 cm (Table 1). When seen from a distance running along the top of a branch, this monkey appears about the size of a squirrel. This monkey has many common names including Rufous-Naped Tamarin, Geoffroy's Tamarin, and, locally, Mono Titi. Here we'll refer to them as Rufous-Naped tamarins. The Rufous-Naped tamarin is the most Northern of all species found in its family, the Callitrichidae. We conducted research on tamarins at the former Primate Refuge and Santuary of Panama in the Tiger Islands of Gatun Lake, and at Agua Clara, a peninsula located between Barro Colorado Island and Escobal.
Rufous-Naped tamarins have a variegated brown and black body, an almost bare black face, and a triangular crown of short white fur on a brown and black head. The tail and neck are mahogany red, and the tail has a black tip (Rowe, 1996). The hair on the underside of the body from neck to groin are white to cream in color. The Rufous-Naped tamarin does not have a prehensile tail, so you will never see one hanging by its tail. They can and do coil their tails and use their tails to balances.
|this picture accurately shows the size of a Rufous-Naped tamarin's tail relative to its body length|
We have found no significant differences between the sexes in weights, body lengths or tail lengths when pregnant females are excluded from these measures. Even with the aid of high powered binoculars, the sexes can only rarely be determined in the field. From a distance the genitals are difficult to distinguished, since the vulva of the females are only slightly narrower in width than the male's scrotum and has the same dark pigmentation.
1. All measures were made on live-trapped and live-released tamarins at our field site on Agua Clara Bay, located about 5 kilometers west of Barro Colorado island on a peninsula in Gatun Lake. SFS, The University of California Research Expeditions Program, The L. S. B. Leakey Foundation, The World Wildlife Fund, and the U.S. National Institutes of Mental Health provided the funds permitting this research. My fellow faculty, Drs. Carter, Garber, Ramirez, Sharpe, and Skinner and nearly 100 students have provided essential assistance in the collection of these data.
2. *524.2 is the mean; 47.5, is the Standard Deviation; 28, is the number of subjects upon which this measurement was made, the same order of presentation of descriptive statistics is followed for all other sets ofmeasurements in this table.
3. Two tailed T test for independent samples between adult males and all adult females except those pregnant (rows 1 and 2). *** P <0.001 ** P <0.003
Hershkovitz (1977) documented that the range of this species in the 1930s extended from the Rio Atrato in Northern Colombia to the Coto Region on the Pacific side of Costa Rica near the Panamanian border. Unfortunately, there have been no verified sightings of the species in Costa Rica since Carter (1935) reported them present but rare at his field site.
The closely related Cotton Top tamarins, Saguinus oedipus, are found on the southern side of the Rio Atrato in Colombia. Because of similarities between the Cotton Top and Rufous-Naped tamarin, some taxonimists consider them to be subspecies (Rufus-Naped tamarins being Saguinus oedipus geoffroyi; Cotton Top tamarins being Saguinus oedipus oedipus) while others consider them separate species, Saguinus geoffroyi and Saguinus oedipus (Moore & Cheverud, 1992). We had one female tamarin, Abril, who had a particularly large tuft of white hair on her head, so she looked somewhat intermediate between a Cotton Top and a Rufous-Naped tamarin. Currently we follow Moore & Cheverud and consider them to be separate species but we feel more observations should be collected in areas where the two species occur together.
typical adult female Rufous-Naped tamarin
an adult female Rufous-Naped tamarin with
typical adult cotton-top tamarin
Distribution in Panama
In Panama, it seems likely that the majority of the extant population of the tamarins are in central Panama around the Panama Canal, in the San Blas province on the Atlantic coast and in the Darien Province. I have also seen them at Boca Brava near to Costa Rica on the Pacific Coast and saw several groups in 1982 in Cerro Campana, west and north of Capira. We hope more remnant pockets of this species will be found in Panama. They occur in Panama City at the Metropolitan Nature Park and in a few pockets of the city, including San Francisco area, Albrook, Clayton and Ancon Hill. A few groups in San Francisco and Albrook are confined to the back yards of several homes where the neighbors appreciate the tamarins and enjoy their visits.
Rufous-Naped tamarins thrive in secondary growth forests, forests that have been cleared and then have regenerated for 10-40 years. Forest clearings occur naturally when giant trees fall in primary forests and at the edges between forests and rivers, lakes or oceans. Secondary growth may also occur as a result of forest fires. The clearing of land for agriculture and then abandoning that land, a frequent pattern in tropical areas, is by far the most common source of secondary growth. The tamarins' preference for secondary growth has led to speculation that they have lived in a close association with human agricultural activities for centuries. Agricultural activities may have been an important selective factor in their recent evolution. Certainly their appetite for common agricultural pests such as grasshoppers and locusts would seem to have made them a useful human co-habitant.
Complete protection of an area from any disturbance will eventually lead to a decrease in tamarin population density and perhaps to their eventual elimination since they thrive in secondary growth. For example, Moynihan (1970) reported that tamarins were abundant on Barro Colorado 50 years ago. At that time there was considerable secondary growth on the island. As a result of the careful protection of the island, most of the secondary growth is gone. Decreased secondary growth has been paralleled by decreased numbers of tamarins. Skinner (1985) found there were only 14 tamarins remaining on the entire island as of 1983; eventually even this tiny population may disappear. Complete protection of an area, as in a National Park, would eventually cause a decline in the number of tamarins present. Management of areas to foster continual secondary growth is necessary for maintenance of a population.
The Rufous-Naped tamarin does thrive if given a suitable habitat. In areas of ideal secondary growth it may even reach population densities as great as 70 per square kilometer; this local abundance can give the false impression that the species does not need protection. The IUCN (2011) correctly recognizes the population of the Rufous-Naped tamarin is decreasing, but we feel it incorrectly classifies them as not endangered. We have watched their habitat and and their numbers decrease at an alarming rate over the past 20 years. Probably only those living along the Panama Canal could be falsely led into the belief that this species is not seriously imperilled in the Republic of Panama. If refuges are created and managed to assure there would be adequate secondary growth, there would be considerable grounds to believe that tamarins will survive and may even be reintroduced into areas where they have been eliminated. Increased awareness of the role of the tamarin in the control of agricultural pests, as well as aesthetic appreciation of this attractive creature, may eventually allow it to live in closer association with people, much as do squirrels in parks and residential areas in more temperate regions. For example, public education about the tamarins living in the new Metropolitan Nature Park in Panama City could help increase appreciation for this unique and attractive monkey. This appreciation is what allows the small groups of tamarins to survive in urban Panama City.
The most common form of locomotion consist of quadrupedal (using four limbs for locomotion) walking and running, bounding or galloping along horizontal and diagonal supports, combined with leaping between terminal branches. Most typically a tamarin is seen walking or running on top of horizontal branches. Rufous-Naped tamarins avoid vertical supports during travel, but spent about 20% of the total feeding time clinging to large vertical supports (Mittermeier, 1988). Rufous-Naped tamarins can suspend themselves from branches with just their hind limbs (Rowe, 1996). Occasionally they make dramatic, gliding leaps between trees, leaps of 5 meters or more. Typically a tamarin will spread all four limbs wide with its tail out behind it when making these dramatic leaps. The sound of tamarins making these leaps while running away from an observer may be the first, and last, notice that the observer has disturbed an unhabituated group.
The diet of free ranging tamarins has been includes lizards, frogs, nestling birds, bird's eggs, snail, insects (including caterpillars, larvae and pupae), arachnids, centipedes, millipedes, galls, honey, fruits, flowers, leaves, petioles. leaf buds, nectar, exude (gum or sap), bark, and fungi (Mittermeier, 1988). Rowe (1966) estimated fruit makes up 60% of the diet and animal prey 30%, the remaining 10% consisted of flowers, gums, and buds. Large grasshoppers are the most important insect prey, comprising over 70 percent of the diets animal component (Dawson, 1976). The relative nutrient contents of the diet of Saguinus geoffroyi were estimated to be 16% animal proteins, 5% vegetable proteins, 9% lipids, 29% reducing sugars, 7% cellulose, and 34% complementary fraction of mainly indigestible elements (Mittermeier, 1988). Females eat exudates during gestation and lactation for calcium (Rowe, 1996). The scarcity of both insects and fruits during the dry season and the latter part of the wet season is reflected in the loss of fat reserves and weight by the tamarins. The animal/plant proportion in the diet shows seasonal changes that respond mainly to seasonal changes in insect abundance. In the dry season animal prey comprise 44% of the diet, in the first half of the rainy season 64%, and in the second half of the rainy season 36% (Mittermeier, 1988).
Fruit is the most important plant source of food for most of the year. During the driest months of the year, fruit may become scarce, and feeding on such secondary resources as nectar and exudate increase and may even overpass that of fruit (Mittermeier, 1988). Tamarins shift from a preponderance of plant foods during the dry season, to insect prey during the early wet season. Both fruit and insects are at their yearly peak of abundance at this time of year, and tamarins prefer insects when they are easily available (Dawson, 1976). Most fruits eaten are ripe succulent drupes or berries of rather small size and they are usually cropped directly with the mouth. Medium-size fruits are detached and held in the hand while the tamarin is clinging to the fruit. Fallen fruits are occasionally picked up from the ground. Feeding on nuts appears to be relatively rare in tamarins. The seeds are either dropped or, if small, often swallowed intact. (Mittermeier, 1988).
animal prey are usually found while in transit between plant food
sources or while feeding on plant foods. Fruits we have observed to
be among those most favored at our field site, include those of
and Annona spraguei
Spikes of Piper
also favored food sources.
Garber (1984) believes exudates (sap, gum and resins), particularly
those from Anacardium
excelsum to be
important for the nutrition of tamarins and found that they accounted
for a 14% of their diet at a study site on the Pacific side of the
canal. At our field site on the Atlantic side of the canal, Garber
(pers. com.) observed very few instances of exudate feeding. He feels
this may be due to the presence of relatively few mature Anacardium
On the Pacific side of the Panama Canal, Dawson (1976) found tamarins in groups with an average size of 6.93 individuals. Two groups had home ranges of 26 hectares and greater than 32 hectares. At Agua Clara, we found tamarins in slightly smaller groups containing an average of 5.27 individuals. During the wet season, groups occupyied ranges of 8.16 to greater than 15 hectares. Rufous-Naped tamarins have been observed in groups or aggregations of two to about 40 animals. However, the usual size of social groups ranges from 2 to 8 or 9 individuals, the modal or 'average' group size is 5-6 individuals. The available data suggest that 12-13 individuals marks the upper limit for natural, free-ranging, stable social groups. The size of a given stable group may fluctuate considerably over time. Most of this fluctuation results from sub-adult/adult movements into and out from the group. Migrations of individuals between groups is a regular phenomenon in free-ranging populations. Dawson (1976) found a 1:1 male/female sex ratio.
The average daily activity cycle is estimated to be 10.4 to 11.6 hours (Mittermeier, 1988). The daily activities usually cease well before sunset. The principal daily activities of free-ranging tamarin groups include insect foraging, feeding on fruit and other plant resources, resting and grooming, and travel (Mittermeier, 1988). Levels of activity are not constant throughout the day, but rather follow a definite pattern. The daily group activity pattern of Saguinus geoffroyi starts with mainly the visit of one or a few major fruit sources, the first morning hour, and is followed by a period of predominant insect-foraging. A brief resting and grooming bout is often observed in late morning and a major resting and grooming period, usually lasting 1-3 hours, takes place in the early afternoon. This is followed by an other major period of insect foraging and by a few visits to fruit sources, particularly short before settling for the night (Mittermeier, 1988). Activity, in the form of both foraging and travel, increases dramatically just prior to entering the roost tree. The day's activity was often climaxed with rapid, silent, and direct travel of 200 meters or more to a roost tree (Dawson, 1976). If you want to see tamarins, probably the best time to find them in the field is from dawn to 10 AM and from 2 to 3 PM, periods when they are on the move and you are likely to be able to see their small bodies moving in the dense vegetation where they live.
Rufous-Naped tamarins sleep in trees that are either densely foliated and/or covered with vines. The mean height of sleeping trees at our Agua Clara study site was 11.8 meters and the tamarins sleep at a mean height of 9.7 meters. Tamarins frequently sleep in "nests"; no observations have been made of tamarins making these nests so it seems likely that they have been made by squirrels (Sciurus granatensis), other animals, or are accumulated debris. The roost is a basal part of a branch, or a tangle of vines or twigs and leaf debris, located in the middle crown. Rufous-Naped tamarins have not been observed to sleep in cavities in trees as do many other Callitrichids.
Sleeping trees tend to be characterized by isolation from others by virtue of height or absence of connecting branches and often by a particularly good vantage point of the surrounding area. Choice of these trees may increase the tamarins' ability to detect the approach of a nocturnal predator. Sleeping trees are not necessarily near the center of a territory: they may be found at the junction between territories. A sleeping tree near territorial boundaries may be used due to the tendency for tamarins to visit the border of their territories in the morning; we have found territorial encounters often last longer when such a sleeping site has been used the previous night. Sleeping sites are changed frequently.
Rufous-Naped tamarins scent-mark the tree branches that are used as regular trails where their range overlaps with another group’s (Rowe, 1996). Tamarins tongue-flick appears before copulation and in highly aggressive contexts. Scowling is another facial display that is common during aggressive interactions. Piloerection is an important display in Saguinus geoffroyi (Mittermeier, 1988).
Ten different calls have been recognized by Saguinus geoffroyi. A long whistle is a long distance intragroup call. Trills are given in hostile situations and at potential predators. Long rasps are heard when there is a violent agonistic encounter (Rowe, 1996). Loud long calls are being used for territory defense and soft long calls are used in intragroup cohesion (Mittermeier, 1988). The long call is of a much lower frequency (1.0-1.5kHz) than that of other callitrichids (5.0-10.0kHz) (Rowe, 1996).
We have found tamarins to be territorial; they tend to visit the border of their range between 7 and 9 am every day and mark trees there with their large suprapubic scent glands. While at the border, the tamarins frequently make bird-like Normal Long Whistles and Soft Long Whistles, vocalizations that have been quantitatively described in the laboratory for the Cotton top tamarin by Snowdon et al. (1983). Our field data suggest the Normal Long Whistle usually occurs between groups or between widely separated members of the same group. The Soft Long Whistle seems to mostly occur within groups just before contact is made with another group; it thus seems to alert group members of the presence of another group. In the field, the 2 to 4 ascending notes of the Normal Long Whistle are often one's first cue that tamarins are nearby.
Males in the groups most closely and most frequently approach the border of their territory. Chasing back and forth across the border occurs between males in neighboring territories. While involved in territorial interactions with members of another group, individuals may frequently flick their tongues at each other. Females in both the field and laboratory seem to engage in more frequent marking with their large suprapubic glands. We have observed them to often stay 15 or 20 meters away from the territorial boundary when males are interacting at the border. During the main period of breeding, November to February, fighting may frequently occur between groups. Injuries occur during this fighting: we have often seen tamarins fall 20 meters or more to the forest floor and observed broken tails, nails ripped from fingers and toes, and large bleeding lacerations after a fight.
There is thus considerable differentiation of sex roles during territorial disputes; males engage more frequently in active aggressive behavior with the other group and females more frequently scent mark. Greater scent marking by females is associated with their significantly larger suprapubic glands (Table 1). Greater scent marking by females and more aggression by males in intergroup interactions has been observed in captive Cotton Top tamarins (French & Cleveland, 1984).
In a group of tamarins with a home range of more than 32 hectares, Dawson (1979) found overlapping and shared ranges of groups instead of territoriality. In many species that form territories, it has been found that once a range becomes so large that borders cannot be frequently visited, the territorial pattern gives way to temporal segregation in use of the range; when an encounter does take place, one group supplants the other from preferred resource areas. It seems likely that when ranges are small and population density high, tamarins will be found to display territorial behavior whereas when ranges are large and population density low, they have overlapping home ranges.
We have found that tamarins frequently move between groups and that entire groups may coalesce and then disband over a period of a few weeks. A similar pattern of frequent movement between groups was observed in groups of tamarins on the Pacific side of the canal by Dawson (1979). Males and females may sometimes join a group with minimal agonistic behavior and then leave again after a few days. Alternatively, a newcomer may face exceptional aggressive behavior. We have seen solitary individuals, or pairs without a territory, knocked out of trees and chased for several hundred meters when they attempt to approach a group. The exceptional frequency of movements between groups has led us to believe that, within a given area, many of the tamarins are known to each other.
Experimental evidence and extensive experience in forming groups for release suggest adult females meet with most resistance when transferring between groups: We have introduced of tamarins in cages into the ranges of wild groups to assess the reactions of these groups to different ages and sexes of individuals. Our tentative results suggest that adult female tamarins are approached most and receive more aggression than adult males, and adult males receive more approaches and aggression than juveniles of either sex. These observations are consistent with Dawson's finding that adult females emigrate, immigrate or disappear least followed by males, then immature females and then immature males (1978). The high frequency of transfer between groups suggests that adults in groups who do not reproduce will not always be grown offspring of the reproductives in the group.
Table 2: Life development of Saguinus geoffroyi.
2-3 months (Rowe, 1996)
24 months (Rowe, 1996)
140-180 days (Rowe, 1996)
13 years (Rowe, 1996)
January till February (Rowe, 1996)
March till June (Dawson, 1976)
Most tamarin births occur from March through June, a district birth peak is from late April to early June. Pregnant females and/or newly born young can be encountered in every month of the year (Dawson, 1978).
An important part of reproductive success in tamarins concerns the care of infants. Infant tamarins need to be carried for the first 6-8 weeks of life. One striking aspect of tamarins is the extent to which animals other than the mother are involved in caring for infants. This extramaternal care is provided not only by the adult male, but frequently by other family members (Mittermeier, 1988). We have not however, observed adult females, other than the mother, carrying infants.
Infants of Saguinus geoffroyi can move about independently of their parents, even in the first week of life. Even when moving independently, the infants are rarely more than a few inches from another group member. Adults carrying infants move a bit more slowly. Adults would just sit when tired and wait for another group member to approach to take the infant (Mittermeier, 1988). We have observed infants to totter away from their carriers at times and have observed that if they are not quickly retrieved that they can fall, sometimes to their death.
|Adult female with her infant. Note her claw like nails allows her to vertically cling to the tree trunk even while carrying the extra weight of her infant.||Adult
male eating a mango while carrying two infants.
Running from tree to tree with these two large young hanging on his back is an energetic challenge.
|Adult male with infant|
Data from the field and laboratory suggest that only one female in the group bears offspring, a trait shared with other members of the family Callitrichidae. Laboratory data suggest that the presence, probably the smell, of this reproductive female, is often sufficient to prevent other adult females in the group from having normal ovulatory cycles during which conception is possible. Field observations of two closely related species of tamarins indicate that, on rare occasions, two females may give birth in the same group: Ramirez (1984) recorded the birth of young to two adult females in one group of Moustached tamarins (Saguinus mystax) and Terborgh & Goldizen (1985) observed a group of Saddle Backed tamarins (Saguinus fuscicollis) containing two females who showed signs of having given birth and two litters of young who were separated by less than 5 months in age.
gestation length of tamarins
seems likely to be similar to the 183 day gestation period of Cotton
Top tamarins reported by Ziegler et al. (1987). Rufous-Naped tamarins
twins, but in the wild groups may not succeed in raising both.
Leutenegger (1980) has documented the unusually large weight of the
fetuses compared to that of mothers in the Callitrichidae. The large
size of offspring and the presence of twins may provide a proximate
explanation for other group members carrying the infants. We have
found one of the adult males in the group usually does most of the
carrying of the infant or infants. The more frequent carrying
infants by males rather than by the
mother is a very unusual trait among nonhuman primates.
Our observations indicate one adult male tends to invest the most in the care of offspring. This investment can be quite be quite extensive: the adult male who carries the infant will approach more closely to the observers (undoubtedly perceived as a potential danger) than any group member would hazard under other circumstances. Terborgh & Goldizen (1985) report more than one adult male in a group sometimes carry infants in Saddle Back tamarins. Adult and juvenile group members may help in carrying the offspring since those offspring are siblings; by helping, they increase the likelihood that their genetic relatives will survive in future generations (Ingram, 1977) . There is also substantial evidence from studies on captive tamarins by Skinner (1985) and on Cotton Top tamarins Tardiff et al.(1986) that experience in the care of offspring by juveniles increases their later likelihood of successfully raising offspring when they become reproductive adults.
Another very unusual trait found in the Callitrichidae is the actual sharing of food with young initiated by the possessor of the food. So far this trait has only been documented in captive Cotton Top tamarins, where it has been carefully described by Psychologists working at the University of Stirling. While we have not yet observed food sharing with infants initiated by adults, we have observed tamarins to frequently give Normal Long Whistles when they find an abundant food source, seemingly to alert the other group members of its presence. Two tamarins will also frequently eat from the same food source, for example, from a single mango. We have watched adults passively permit juveniles to approach and take food from their grasp. Sometimes the adults protest the taking of the food, so the juveniles' behavior becomes food stealing.
It seems likely that raptors are currently the most frequent predators of the tamarin. As such, they may be an important selective factor influencing their behavioral ecology. In 1982 we observed a hawk swoop down and attempt to grasp a juvenile tamarin in its talons. The juvenile tamarin escaped and fell to the forest floor, apparently receiving no injuries. In response to the close fly by of a raptor or other large bird we have observed tamarins to rapidly swing themselves under the tree branch they were previously sitting on, thereby interposing the branch between themselves and the potential source of danger. Lindsay (1979) also reported this behavior in tamarins on the Atlantic coast of Panama. Raptors have been observed to kill other species of tamarins by Izawa et al. (1988).
Indirect lines of evidence indicate raptors may be frequent predators of tamarins. We have found tamarins tend to scan more frequently when high in the canopy and thus when more exposed to raptors; we have also found tamarins scan more frequently when in areas with low cover density compared to when in areas with dense cover that would shield them from the view of raptors. These observations of increased scanning are consistent with Caine's (1986) observation that Red-Bellied tamarins, Saguinus labiatus, tend to frequently visually scan threatening objects in captive colonies. We have also found that play back of tape recordings of tamarin vocalizations significantly increase the number of raptors visible on the horizon. The approach of raptors to tamarin vocalizations may indicate raptors seek out tamarins as potential prey.
Potential mammalian predators include tayras (Eira barbara), ocelots (Felis pardalis), margays (Felis wiedii) jaguarundis (Felis yagouroundi) and coati mundi (Nasua nasua). Moynihan (1970) observed a tayra carrying a dead tamarin and Ramirez (1984) observed them chasing Saddle Backed tamarins. Most mammalian predators are less common now in Panama than they were previously, so they may have had a stronger selective influence on tamarins in the past. Human observers frighten away these small predators much more than they do the tamarins who are habituated to their presence; many of these potential predators are nocturnal hunters. As a result, observers are unlikely to witness their attacks on tamarins. Mammalian predators may therefore have a currently greater selective influence on tamarins than suggested by available data.
Large boas are also potential predators. We have observed tamarins alarm calling and orienting towards boas when they are present, but we have not seen a boa attempt or succeed in killing a tamarin. Cayman and crocodiles may occasionally catch an unwary tamarin, one tamarin we were observing was eaten by a cayman.
Because of the small size of tamarins their main defense against predators are vigilance, crypticity and escape. While large numbers of individuals may more successfully detect a predator, the greater number of individuals present, the less capable they are of concealing their presence. The balance of these two factors may be partially responsible for the relatively small group size of tamarins.
The fact that there is usually only one reproductive female per group and that one male tends to most frequently carry the offspring suggests that the tamarin may have a monogamous breeding structure. Our observations of sexual behavior also suggest a monogamous breeding pattern: We have observed many instances of males mounting females in free-ranging groups and all copulations have occurred between the same pairs of animals. While a given female may be observed to only copulate with one male in the group for months or years, we have seen pair-bonds change and the female switch to another male in the group. Free-ranging tamarins we have observed might thus be classified as serially monogamous. These observations contrast with our observations of a captive group: In that group composed of 3 adult males and 3 adult females, every adult group member repeatedly mounted the reproductive female.
Clutton-Brock et al. (1977) have demonstrated species of nonhuman primates with a monogamous breeding system are characterized by an absence of difference between the body and canine sizes of adult males and females. In polygynous species, where males have greater variance in reproductive success than females, males tend to have larger body sizes and/or larger canines since these traits are selected by their greater competition with each other over females. Greater size in males may also be selected by a greater role in active defense against predators.
Observations in the field and the laboratory on other species in the family Callitrichidae suggest that sometimes the female in a group may copulate with more than one male during the same time period, that is, the breeding structure may sometimes be polyandrous. Terborgh & Goldizen (1985) observed that, in four of five groups of Saddle Backed tamarins containing two adult males, both of the males copulated.Hubrecht (1985) has observed copulations between an adult female in one group and one or more adult males in another group in the common marmoset (Callithrix jacchus), another member of the family Callitrichidae. Such extragroup breeding may be responsible for our observations of males aggressively chasing the female members of their group away from the border of their territory after intergroup interactions.
Promiscuous matings are frequently observed in laboratory colonies of Callitrichidae and there is some evidence that groups composed of one adult female and two adult males may sometimes more successfully breed than those composed of monogamous pairs. We usually released groups back into the wild with more than one adult male. Even in species where mating almost exclusively takes place between a pair of animals, such as the Lion tamarin, a second male may sometimes copulate with the breeding female. Evidence available from the field and laboratory has led Sussman & Garber (1987) to conclude that Callithrichid social structure is characterized by a polyandrous breeding system. If Rufous-naped tamarins are polyandrous, we feel it is a mild form in which the reproductive female may copulate with more than one male, but one male has a much higher certainty of paternity than the others.
In Rufous-Naped tamarins there is little or no sexual dimorphism in body and canine size. We would anticipate females to have either a larger body size and/or larger canines if they experience greater variance in reproductive success than do the males, a potential consequence of a polyandrous breeding system. Perhaps the greater size of the females' suprapubic glands is an indicator of greater competition in scent marking and this physical trait is of greater competitive value in tamarins than either canine or body size.
Population-Dependent Social Organization
The social organization of the Rufous-Naped tamarin seems adapted to opportunistically exploit their secondary growth habitat. The capacity to produce twins and the care of the offspring by others in the group, primarily one of the adult males, permits a very high rate of reproduction when tamarins move into an area of new secondary growth. The male and other group members free the reproductive female to put all of her energies into obtaining food necessary for lactation and for nurture of the new fetuses she may have conceived soon after giving birth. In areas of secondary growth with low population densities, Ramirez (1984) found Mustached tamarins to have fewer adult females in groups. Given the usual reproductive inhibition of all but one adult female in each group, this group composition would allow for the maximum rate of reproduction when population density is low, as would be the case when tamarins move into a new area of secondary growth. As population density in the area increases, food availability may decrease and the likelihood of raising both twins would also decrease. The number of adult females per group might also increase and this too, would lower the number of offspring produced. At high population densities, it may be advantageous for the reproductive female to put most effort into the care and production of only one offspring per year since food resources, increased competition with other adult females, and decreased opportunities for rapid reproduction of her offspring would make intensive investment in only one offspring more advantageous. Surplus adults in an area with a high population density would await a new area of secondary growth to open up.
The characterizations of the tamarin in this paper are tentative, as much remains to be learned about the social organization and ecology of this unusual species. Of particular importance is a long term study of individually recognized individuals where kinship between group members and neighboring group members is known, length of tenure of reproductive females is determined, and the biological paternity of offspring is identified.
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