DISCUSSION

Moustached tamarins on Padre Isla live in small multimale multifemale social groups (group size 4-11 individuals) that appear to, contain both related and unrelated adults. The adult composition of groups was highly variable and included social units conposed of 1 adult male with 3 adult females, 3 adult males with 1 adult female, 3 adult males with 3 adult females, 3 adult males with 4 adult females, and 2 adult males with 2 adult females. None of the 13 completely censused groups on the island were characterized by a single adult male and a single adult female. Social groups composed of more than I adult of each sex are reported in man) if' not all tamarin species studied in the wild. These include Saguinus oedipus, S. geoffroyi, S. labiatus, S. fuscicollis, S. imperator, S. mystax, and S. nigricollis [Buchanan-Smith, 1990; Dawson, 1977; Goldizen, 1987a,b, 1990; Izawa, 1978; Moynihan, 1976 Neyman, 1977; Soini, 1987; Sussman & Garber, 1987; Terborgh & Goldizen, 1985].

Based on observations in 2 target study groups and evidence of more than I reproductively active female in 3 additional groups, the modal mating pattern of Saguinus mystax on Padre Isla cannot be considered functionally or obligatorily monogamous. We have direct evidence of polyandrous matings in the green group and polygynous (polygynandrous) matings in the copper group. Observations during Aug7ast 1990 of polyandrous matings in another group on the island also have been reported [Ruth, 1991].

Each of the 3 groups with more than 1 sexually active female contained at least 2 adult males. Although we lack information on whether more than I male copulated with these females, the mating patterns of these groups must provisionally be considered polygynous. Thus, at least 6 of the complete groups on the island exhibited a nonmonogamous mating system Polyandrous and/or polygynous matings have also been reported in 4 of 5 groups of saddle-back tamarins studied by Terborgh and Goldizen [1985] in southern Peru. Although it is possible that some of the remaining groups on Padre Isla may be monogamous, given that their adult age and sex composition do not differ markedly from our other study groups, we feel that monogamy is not a common mating pattern in this population.

Snowdon and Soini [1988] report that in northeastern Peru, Saguinus mystax is characterized by an annual birth peak from November through March. Births, however, do occur during all months of the year. On Padre Isla the majority of infants Ere born during the period of June through October. A second and more limited birth period occurs in February and March. Based on information we collected on 28 lactating females between 1981 and 1990, 93% were nursing young infants during the June through October birth period. Given that our 1990 study coincided with this primary birth peak, the absence of 2 lactating females in any social group on the island supports the contention that in this and other callitrichine species, at any single point in time, there is only 1 successfully reproducing female in each group.

The age structure of the moustached tamarin breeding population indicates that, in general, it is the oldest female in each group that produces offspring. These are principally A3 females, and are known or estimated to he greater than 8 years of age. Ai least 2 of 5 A3 females that were successful breeders in 1981 continue to breed in 1990. These females are at least 12 years of age. If we assume that they were A2 or A3 females in 1981, then it is likely that some moustached tamarin females have a reproductive period that may span 10 or more years and can continue to breed even as they approach the age of 20 In contrast, young and middle aged adult females residing in multifemale groups appear to be reproductively suppressed. Using nipple length as a measure of previous reproductive activity (D 1977; Neyman, 19771, A2 females in this population are no more likely to have successfully produced offspring than Al females.

In social groups of 9 or larger, suppression of subordinate females is less complete, and although more than 1 female may conceive only 1 female is reproductively successful. Groups containing two pregnant, but not two lactating, females have also been reported in Saguinus geoffroyi [Garber & Zeigler, in preparation], S. oedipus [Savage, 1990], S. fuscicollis [Goldizen, 1990], and Callithrix flaviceps [Ferarri & Lopes Ferrari, 1989]. Among tamarins and marmosets, variance in female reproductive output appears to be more extreme thin is reported for any other primate taxa. Opportunities to ascend into an alpha breeding position or to maintain reproductive sovereignty are limited by the number of older females in the population, as well as the ability of a female to attract helpers and establish and defend a home range. Given that none of the social groups on the island contained either 2 A3 females or 2 A2 females, nonbreeding females attempt to enhance their breeding status by 1) migrating into or remaining in a group that does not contain a similarly aged or older female, 2) maintaining a beta social position until the breeding female dies or reaches reproductive senescence, or 3) migrating into or remaining in a large social group, and during group fission attempting to establish reproductive sovereignty in the splinter or transient group. Although an adult daughter may remain in her natal group and act to increase the kinship component of her inclusive fitness through helping to care for her mother's offspring, it is unlikely that in this moustached tamarin population such a strategy will consistently enhance a young female's chances of attaining reproductive dominance.

A similar pattern of age-related reproductive sovereignty has been reported in S. geoffroyi [Dawson, 1977], S. oedipus [Neyman, 1977], and in other populations of S. mystax [Ramirez, 1984; Soini & Soini, 1982]. A study by Ramirez [1984] provides strong support for an age-related female dominance reproductive pattern. At the Yarapa River Site in northern Peru, 66% of a local population of moustached tamarins was removed. Examination of the population prior to trapping indicated that older females were the principal breeders. Three years after the removal of these older, socially dominant females, most of the adult females in the population were young (65-85%), and virtually all were breeding successfully I Ramirez, 19841. These data indicate that in the wild, adult females under 4 years of age are reproductively competent and sufficiently mature to reproduce and nurse their young. The fact that they normally do not breed underscores the degree to which young females are reproductively suppressed and supports the contention that age is a critical factor determining female reproductive opportunities in moustached tamarins. Limitations in this study prohibit us from calculating the average length of time a dominant female retains her sovereign breeding position, or identifying if and under what conditions adult females alternate their breeding positions in the group. The present evidence, however, leads us to conclude that the mating system of Saguinus mystax and perhaps other tamarin species is best described in terms of age-dependent female reproductive sovereignty.

Based on both morphological and behavior information there is no evidence that reproductive activity in male moustached tamarins is similarly age dependent. Of the 5 males that we observed to copulate, 1 was an A3 male, 2 were Al males, 1 was an adult male of unknown age, and 1 was a subadult male. In both of our study groups there was no indication of intra-group mate guarding, and more than 1 male was observed to copulate with the same female within a 24 hour period (in one case within a period of 42 minutes). Although at present we have no information regarding paternity or male reproductive success, given that testes volume was not correlated significantly with adult age, and that males of young, older, and even subadult age classes copulate, it appears that Al and A2 males in the population have considerably more reproductive opportunities then Al and A2 females.

The age-dependent female breeding system described for Saguinus mystax appears to differ from that reported in certain marmoset species. Data presented by Ferrari and Lopes Ferrari (19891 on their main study group of Callithrix flaviceps indicate that young daughters may remain in their natal group and ascend into their mother's breeding position. However, as in the case of tamarins, considerable mating and breeding variability exists among marmosets. For example, information collected by Soini [19881 on 115 live-trapped pygmy marmosets (Cebuella pygmaea) reveals that whereas all of the oldest females in the population were reproductively active, only 50% of the middle aged females and 25% of the youngest adult females were found to be pregnant or lactating. Thus, despite differences in the size and age structure of tamarin and marmoset groups (marmoset groups art generally larger and contain a greater proportion of nonadult to adult group members than do tamarin groups), in the pygmy marmoset female age is an important factor in reproductive success.

TABLE V. Demographic Comparison of Moustached Tamarins on
Padre Isla With Other Moustached Tamarin Populations in
Northeastern Peru

^a Data adapted from Soini and Soini [1982] and Snowdon and Soini [1988]. Moustached tamarins live-trapped from sites on the Rio Maniti, Rio Tahuayo, and Rio Tapiche, Northeastern Peru,
^b Soini and Soini [1982J divided adults into 4 age categories young adult, middle adult, mature adult, and old adult, We divided adults into 3 age categories: young, middle, and old. Using Soini and Soini's [1982] criteria (mature adults: mines considerably worn and teeth stained; old adults: canine and other teeth very won or decayed), our old adult category is analogous to his mature and old adult categories.
^c Soini and Soini [1982] define these as females up to 5 years of age. We define these as females up to 4 years of age.

Given our description of moustached tamarin social and mating patterns on Padre Isla, 3 additional questions need to be addressed. First, is the Padre Isla tamarin population demographically representative of moustached tamarin populations in other areas of Peru? A comparison of the Padre Isla population with data collected by Soini and Soini [19821 on several other moustached tamarin populations in northeastern Peru is presented in Table V. Using measures of group size, number of adult males and females per group, proportion of adults to nonadults in groups, percentage of old adult males and females in the population, and population density, the Padre Isla population is demographically indistinguishable from other moustached tamarin populations live-trapped in Amazonian Peru. Although certain characteristics of the island (absence of natural mammalian predators and potentially competing nonhuman primates, closed population) and aspects of tamarin ecology (smaller home ranges and day ranges) differ from that reported in other populations, these factors appear to have had little direct effect on overall patterns of mating and social organization. Mating patterns and social organization of moustached tamarins on Padre Isla are comparable to those reported for other moustached tamarin populations [Garber, 1988; Ramirez, 1989], as well as populations of Saguinus fuscicollis [Goldizen, 1989, 1990; Goldizen & Terborgh, 1989]. Given, however, the limited comparative data presently available on most of the remaining 10 Saguinus species, generalizing from the Padre Isla population must be done with caution.

Given that all or most adult group members are observed to participate in infant care [Garber, 1986], the second question is whether alloparental behavior in moustached tamarins is kin based. This question is difficult to answer in the absence of precise information on the genetic relatedness of group members (we are presently using DNA fingerprinting techniques to determine kinship in this population). Based on our reconstruction of migration patterns we offer the following possibilities. As is the case with other tamarin species individual migrations of adult and subadults of each sex commonly occur. Such regular migrations have been documented in marked populations of Saguinus fuscicollis [Goldizen, 1990, Soini, 1987; Terborgh & Goldizen, 1985], Saguinus oedipus [Neyman, 1977], and Saguinus geoffroyi [Dawson, 1977]. Given that successful emigration generally occurs without noticeably increased levels of intragroup aggression, and that unsuccessful migrants have been observed to both return to their former group or enter several established groups over a period of months [Neyman, 1977], it is likely that decisions concerning dispersal and dispersal success are strongly influenced by the availability of reproductive opportunities [Goldizen, 1989]. In S. fuscicollis migrants are known to disperse into both nearby (44%) and distant (56%) territories [Goldizen, 1989]. Thus, although it is possible that individuals migrate into groups containing close kin [for a discussion of kin, recognition in tamarins, see Harrison and Tardif, 1988], it also is probable that many migrants spend at least some period of their life in groups with unrelated adults.

We also have evidence of a second pattern of migration in which a pair of males simultaneously transfers into the same social group. Although our present data base does not allow us to calculate the rate of such migratory behavior or the effect of paired emigration in reducing migrant mortality, we feel that our 8 unambiguous cases indicate that this is a common and important pattern. In 3 of these cases the migrants were of the same age class, and possibly litter mates. In other cases these males were of different age classes. The strength of these social ties between the males is extremely strong, with some paired males remaining together in the same nonnatal group for 4 to 8+ years Given that we have no unambiguous evidence of paired female migration, and that in 23% (3 of 13 complete groups) of the current groups on the island we were able to identify the presence of a paired set of immigrant males, it is likely that male kinship/social bonds form the basis of much of the cooperative infant care exhibited by these tamarins. Nevertheless, unlike previous suggestions that male helpers are caring for their younger siblings, we argue that the more common pattern in these and perhaps other callitrichines is one of fraternal and possibility patriphilial (father-son) polyandry and polygyny. We have no information regarding the conditions under which females might migrate as pairs; however, such migrations have been noted in Saguinus oedipus [Neyman, 1977].

The final question relates to the evolution of cooperative infant care and mating system variability in tamarins. Many researchers have argued that monogamous breeding and a nuclear family social system are primitive in Platyrrhini [Eisenberg, 1981; Kinzey, 1987; Wright, 1984] and represent the ancestral condition for tamarins and marmosets [Goldizen, 1990; Kinzey, 1987]. Much of the evidence in support of monogamy in the earliest platyrrhines is the absence of pronounced sexual dimorphism in body size in many taxa, and the fact that all species of Aotus and Callicebus, considered by many the most primitive genera, live in monogamous nuclear family groups. Moreover, since among New World primates monogamous, pair-bonded, nuclear-family social groups are found only in the subfamily Pitheciinae [Kinzey, 1987, Rosenberger, 1981], it remains uncertain whether this particular breeding and social pattern is a shared derived feature of pithecines or whether it is primitive for Ceboidea.

Given the general concensus that tamarins and marmosets represent a highly derived and specialized radiation of small bodied primates, and the absence of postcranial, dental, cranial, or fossil evidence directly linking callitrichines with either Callicebus or Aotus [Ford & Davis, 1992], monogamy cannot simply be assumed to be the ancestral callitrichine condition. In fact, Kinzey [1987:105] notes that whereas in nonhuman primates "monogamy is correlated with relative behavioral and ecological inflexibility," the callitrichine mating and social system is extremely complex and characterized by what he terms "organizational plasticity of behavior" [Kinzey, 1987:110]. Behavioral plasticity allows tamarins and marmosets to exhibit a variety of mating and migration patterns. These patterns function to enhance reproductive opportunities and to ensure the presence of an adequate number of helpers within the social group. Helpers may be kin, nonkin, breeders, or nonbreeders. Although Kinzey [1987] explains this paradox between inflexibility in monogamous nonhuman primates and flexibility in tamarins by arguing that many species of modern tamarins and marmosets are not monogamous, be fails to pose the question of whether such a flexible mating system could have evolved from a nonmonogamous ancestral pattern.

Could the multimale multifemale cooperative breeding system of Saguinus mystax and other tamarin species have evolved from a polygynous breeding pattern? Although we cannot provide a definitive answer to this question, it is possible to identify several aspects of tamarin social and reproductive behavior (using S. mystax as an example) that are 1) present in polygynous New World primates but absent in monogamous forms (e.g., individuals may temporarily or permanently remain in their natal group as adults; flexible mating and group structure), 2) present in monogamous species and tamarins bit generally absent in polygynous taxa (e.g., only a single female in each group gives birth), and 3) unique to the tamarins (and marmosets excluding Callimico) (eg., reproductive twinning; reproductive suppression in subordinate adult females). These are outlined in Table VI. Although this list is neither complete nor exhaustive, it does cast reasonable doubt on a monogamous ancestry for tamarins. In particular, S. mystax shares few traits in common with Aotus or Callicebus [Robinson A al., 1987] that cannot also be found in species such as Cebus apella [Janson, 1984; Robinson & Janson, 1987], Alouatta seniculus [Crockett, 1984; Crockett & Eisenberg, 1987; Sekulic, 1983], or Alouatta pigra [Bolin, 1981; Horwich, 1983; Neville et al., 1988]. Moreover, although the mating system of Callimico is not well known, this primate, which in many aspects of its morphology and behavior may represent the early callitrichine condition, is reported to live in polygynous multimale multifemale groups in which more than I female breeds [Masataka, 1981; Pook & Pook, 1981]. Developing a S. mystax-like mating system from a Callicebus-like or Aotus-like mating system would require changes in group structure, mating pattern, mating flexibility, retention of adults in the natal group, and tolerance of the same sex adults, along with the evolution of reproductive twinning and reproductive suppression. In contrast, developing a S. mystax-like mating system From a Cebus apella or Alouatta pigra-like system would also require reproductive twinning and reproductive suppression, plus the addition of increased levels of alloparental care. These 3 traits are closely linked, however, and may represent part of a single adaptive complex. Thus, we conclude by offering the possibility that ancestral callitrichines were not monogamous and that mating flexibility in tamarins is likely to have evolved from a polygynous mating pattern. It is hoped that many of the questions and ideas raised in this paper will stimulate additional research into the nature of cooperative infant care and reproductive behavior in tamarins and marmosets, as well as provide a framework for reconstructing the ancestral mating/breeding system in other platyrrhine taxa.

TABLE VI. Comparison of Social and Reproductive Patterns in Select New World Primate Taxa*

*++, trait that is highly developed in the species; +, trait that is present but variable in the species; -, not
present or rarely present in the species.