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Senin, 26 Januari 2009

Common marmoset (Callithrix jacchus)


Though they have been studied in captive settings since the 1960s, the social structure of wild common marmosets is less well known than other reproductive and behavioral characteristics (Digby 1995; Ferrari & Digby 1996). Long thought to be monogamous, evidence from recent field studies shows that they have a social structure that revolves around a stable, extended family unit with a few dominant breeding individuals and flexible mating behavior (Digby & Barreto 1993; Digby 1995; Ferrari & Digby 1996; Sussman 2000). Groups of common marmosets range in size from three to 15 animals, but usually have about nine members (Stevenson & Rylands 1988; Ferrari & Lopes Ferrari 1989). Within the group, three generations are often encompassed including one or two breeding females with one breeding male and related adults (possibly parents or siblings) and the breeding pairs' offspring (Ferrari & Digby 1996). Using genetic evidence to tease apart the relationships within a group of common marmosets, it has been demonstrated that females within a group are closely related (as close as mother/daughter or sisters) while breeding males are distantly related, and probably immigrated from another group. When males are closely related to breeding females, they do not breed with them (Nievergelt et al. 2000). Unlike many other primate species, emigration does not occur during adolescence in common marmosets. Instead, they remain in their group until they are adults and then the males leave the group to find breeding females. Emigration by adults is balanced by recruitment through births, keeping the group size relatively stable over time, though very little is known about when and why adult common marmosets leave their groups (Ferrari & Digby 1996). Group stability is compromised in the wild because the death of a breeding adult will cause a group to break up and separate into new groups (Lazaro-Perea 2001).

Social status within the group is linked to breeding status, and while the breeding pair is usually codominant, if there is more than one breeding female, one of the breeding females is dominant over the other. For nonbreeding individuals, the dominance hierarchy is age-graded and sex is not a factor (Digby 1995). Dominant individuals displace others at feeding sites and exhibit a variety of postures, vocalizations, and behaviors that include open-mouth threats, nips, cuffs, lunges, grabs, ear-tuft flicks, genital presenting, chasing, and biting (Abbott 1984; Digby 1995). They are the center of social life in the group and subordinate animals favor being in proximity with dominant individuals and groom them preferentially (Digby 1995).

Photo: Ludwig Miller

One of the defining social behaviors of common marmosets is their system of cooperative breeding and infant care (Digby & Barreto 1993; Digby 1995; Sussman 2000). The breeding adults in the group depend on the cooperation of their adult siblings and offspring to care for their new infants to ensure their survival. This requires behavioral and physiological reproductive suppression of adult and developing females and behavioral reproductive suppression of adult and developing males in the group by the breeding pair, a phenomenon that has been well studied among captive common marmosets (Saltzman et al. 1997; Baker et al. 1999). In response to a dominant, unrelated, female, submissive common marmosets become anovulatory while her daughters may continue to cycle (Ziegler &de Sousa 2002). Rather than dispersing, finding a breeding partner, and forming a new group, subordinate marmosets that are sexually mature and could otherwise mate stay within the family unit. This strategy may be beneficial under certain ecological conditions. For example, where marmosets live in extremely high population densities, dispersal may not be possible because of lack of available territory and hostile encounters with other marmoset groups in the area or high chance of predation if ranging solitarily (Dietz 2004). Staying within the group, at least for a while, to help raise their nieces and nephews or siblings may be the best choice to maximize fitness. Because these helpers are likely related to the dominant female, it is within their interest to ensure the survival of her offspring because they are also related to them and the survival of the infants increases the related caregiver's inclusive fitness (Saltzman et al. 1997).


Sexual behavior and reproductive parameters are often skewed in captivity compared to natural conditions and as such, data from laboratory settings often must be substantiated by observations and tests from wild animals. The common marmoset is no exception, though recently there have been advances in hormonal monitoring techniques resulting in data from wild common marmosets (Albuquerque et al. 2001).

Photo: Gustl Anzenberger

The mating patterns of wild common marmosets are exceptionally complex and vary over time. While monogamy was long thought to be rule among common marmosets because of captive studies, there have been observations of polygyny, polyandry, and monogamy in the wild (Digby 1995; Nievergelt et al. 2000). Field data support that most mating is monogamous and when two females are pregnant within a group, it is because the subordinate female, the daughter of the dominant female, mated with a male from a neighboring group. The non-dominant female is not fully reproductively suppressed, but her pregnancy does not result in viable offspring (Digby 1999; Nievergelt et al. 2000; Arruda et al. 2005). Even though the subordinate females lose their infants, this pattern of mating with extra-group males may be a strategy to identify potential future mates. This is supported because subordinate females that mated successfully but did not produce viable offspring emigrated from their natal groups shortly after and joined another group, assuming a breeding position (Arruda et al. 2005).

Menarche occurs between nine and 14 months of age but common marmosets do not menstruate nor are there any external signs of ovulation. The ovarian cycle lasts between 24 and 30 days, but averages 28 days (Hearn 1982; Kendrick & Dixson 1983). In captivity, in the presence of a dominant female, unrelated young female marmosets generally will not ovulate and though they are sexually mature, they do not cycle and are unable to breed, but the dominant female's daughters do exhibit ovarian cyclicity even if they do not mate (Abbott 1984; Ziegler &Sousa 2002). Under natural conditions, the presence of two breeding females has been observed, but the females are always closely related, either mother and daughter or sisters (Digby & Barreto 1993; Nievergelt et al. 2000; Arruda et al. 2005). For females, the mechanism by which this occurs is both behavioral and physiological but variations in reproductive suppression are not well understood. That is, it is unclear why in most but not all circumstances only one female breeds while in other instances there are two breeding females (Saltzman et al. 1997). One factor that contributes to the suppression of ovulation in subordinate female common marmosets is the presence of a related male. In laboratory studies, young adult females do not ovulate or exhibit sexual behavior in the presence of their fathers, probably a defense against inbreeding, but if the biological father is replaced by another adult male, within a few weeks ovulation occurs coupled with sexual solicitations and an increase in aggressive behavior towards their mothers (Abbott 1984; Saltzman et al. 1997). One explanation for this is daughters are trying to displace their mothers as the dominant breeding female in their group and have more opportunities to mate and increase their overall fitness.

Once the social conditions are suitable for a female to begin breeding, common marmosets reproduce consistently over the remainder of their adult lives. Females solicit mating by tongue-flicking displays directed at males. Common marmosets mate throughout their ovarian cycle but the majority of mating occurs in a three- to four-day window on either side of ovulation (Kendrick & Dixson 1983). Gestation lasts about five months (143 to 153 days) and soon after parturition (within 10 days), female marmosets begin to cycle again and shortly thereafter become pregnant (Lunn & McNeilly 1982; Sussman 2000). The interbirth interval exhibited by common marmosets is five months and they give birth twice each year (Stevenson & Rylands 1988). Common marmosets exhibit a high degree of birth seasonality in the wild and have two birth peaks during the year; during September, October, and November as well as April, May, and June (Stevenson & Rylands 1988). One of the major factors thought to influence this strict seasonality is rainfall, which directly affects food availability (Di Bitetti & Janson 2000). Common marmosets give birth at the end of the dry season and at the end of the rainy season to maximize food availability. Because nursing is so energetically costly, females need to minimize the nutritional stress they experience by rearing their infants during periods of relative food abundance (Di Betetti & Janson 2000). Additionally, the pattern of habitual twinning among common marmosets means nursing and rearing infants is even more energetically taxing. Common marmosets do not always give birth to twins; they also have single births and triplets. The reproductive patterns of common marmosets would not be possible if there were not special adaptations to infant rearing and parental care.


Group support for developing infants is necessary among common marmosets. Twins are often 20 to 27% of the mother's total body weight; this is the equivalent of a 135-pound woman giving birth to two 16-pound babies. A female would not be able to care for infants alone because of the high demands of pregnancy and lactation as well as the mechanical difficulties of carrying two heavy infants, therefore all age-sex classes contribute to infant survival and development among common marmosets (Stevenson & Rylands 1988; Rothe et al. 1993; Tardif et al. 1993; Kinzey 1997). As discussed previously, compliance with cooperative rearing is probably linked to kin selection and fitness. The non-reproductive helpers in the group are probably related to the infants because they are related to the breeding female. It is within their interest to ensure the survival of her offspring because this increases the helper's inclusive fitness (Rothe et al. 1993; Saltzman et al. 1997). Studies on captive marmosets indicate that survival rate increases as number of non-reproductive helpers increases, up to a point. The highest survival rate of infants (95.7%) is found in groups of 10 common marmosets (the breeding pair and eight helpers) (Rothe et al. 1993). Interestingly, the average group size in the wild is about nine members.

Photo: Gustl Anzenberger

From birth, common marmosets have a very strong cling reflex and do not voluntarily leave their carrier's back for the first two weeks of life. They are very active starting in the second week, crawling on their carrier's back and investigating their surroundings (Stevenson & Rylands 1988). Immediately after birth, the breeding male and presumptive father of the infants begins to carry the twins and caregiving by offered by the father, mother, or other members of the group (Yamamoto 1993). Over the following weeks, time off the backs of carriers gradually increases and the infants develop locomotory behaviors and coordination and begin to exhibit play behavior (Stevenson & Rylands 1988). By about three months of age, the infants are almost completely weaned and are capable of self-feeding, though they do not gnaw their own holes to feed on gum but rather lick the holes created by older individuals (Stevenson & Rylands 1988). The infancy stage lasts until about five months of age and is followed by the juvenile period, which lasts between five and 10 months (Stevenson & Rylands 1988; Yamamoto 1993). By five months, common marmoset juveniles are 75% of their adult weight. Interaction with other group members besides parents is emphasized and play becomes rougher as future status is worked out. During the juvenile period, another set of infants is usually born and carrying and play with infants also characterizes this period of development (Yamamato 1993). Between nine and 14 months, the sub-adult stage begins, characterized by the full repertoire of adult behaviors as well as puberty. By 15 months, common marmosets have reached their adult weight and are capable of reproduction but do not reproduce until social conditions are adequate (Yamamato 1993).


Like all primates, vocal and visual communication is important to common marmosets. Facial expressions and vocalizations convey information about social status, emotional state, and intent to other individuals (Stevenson & Rylands 1988). Because of their small size and the natural habitats they are found in, visual signals are important in close-range communication while vocal communication is more important over longer distances (Jones 1997). Some expressive facial and postural positions include the "partial open mouth stare," "frown," and "slit-stare" which are used to signify alarm, aggression, and submission. When common marmosets flatten their ear-tufts close to their heads in "tuft-flatten" position, this signifies submission, fear, and sometimes curiosity of new objects (Stevenson & Rylands 1988).

Photo: Ludwig Miller

Common marmosets use vocal signals in a variety of situations including in response to unexpected movements and in threatening situations (Jones 1997). Alarm calls in response to sudden movement include "staccatos," which are a series of short ascending calls, and "tsiks," that are brief descending calls given either alone or in a series. Alarm calls are brief, high-pitched vocalizations that elicit fleeing behavior from other group members and are given in response to threatening situations (Lazaro-Perea 2001). There are some calls that are generally used and which lack obvious contextual connection including "phee" and "trill" calls (Jones 1997). "Phee" calls have high sound intensity and sound like very loud, high pitched whistles. They are usually given in a series of one to five notes that last about two seconds each. They are important for long-range vocal contact and play a role in mate attraction, maintenance of group cohesion, territorial defense, and location of lost group members (Jones 1997). "Trill" calls are also generic vocalizations, but sound much different from "phees." They have lower pitch and have cyclic frequency fluctuations that give them a distinctive vibrato sound. These calls are given by all animals of any age, sex, and status and their main purpose probably is to monitor group members by identifying and locating their position in low visibility areas (Jones 1997).

Unlike the apes and Old World monkeys, smell is very important to New World monkeys. They have a specialized organ in their nasal cavity called the vomeronasal organ that allows them to process chemical signals in a focused manner and discern information about other animals (Evans 2003). Because of the presence of this "second nose," scents are very important tools of communication in New World monkeys, and common marmosets convey information by marking objects with secretions from specialized scent glands on their chests and around their anus and genitals (Lazaro-Perea et al. 1999). The main information conveyed by scent-marking includes demarcating home range and resources within that range, signifying social status, and advertising reproductive status (Stevenson & Rylands 1988; Lazaro-Perea et al. 1999; Ziegler et al. 2005).

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