Demographic and reproductive patterns in moustached tamarin monkeys (Saguinus mystax) Implications for reconstructing platyrrhine mating systems.код для вставкиСкачать
American Journal of Primatology 29:235-254 (1993) RESEARCH ARTICLES Demographic and Reproductive Patterns in Moustached Tamarin Monkeys (Saguinus mystax): Implications for Reconstructing Platyrrhine Mating Systems P.A. GARBER', F. ENCARNACIbN', L. MOYA3, AND J.D. PRUETZ' 'Department of Anthropology, University of Illinois, Urbana, Illinois; "Proyecto Peruano de Primatologia, Iquitos, Peru; 3Ministerio de Agricultura y Alimentacibn, Iquitos, Peru In this paper we address a series of questions concerning reproductive opportunities, kinship, dispersal, and mating patterns in free-ranging moustached tamarin monkeys (Saguinus mystax). Between 1980 and 1990 information on group size, composition, and migration patterns was collected on marked groups of moustached tamarins inhabiting Padre Isla, an island in the Amazon Basin of northeastern Peru. In 1990, 86% of 114 animals residing in 16 social groups were trapped, examined, and released. Mean group size was 7.0, including 2.2 adult males and 2.0 adult females. None of these groups was characterized by a single adult malefemale pair. In groups with more than one adult female, only the oldest female produced offspring. An examination of dispersal patterns indicates that transfers between groups were common and fell into several categories, including immigration of individual males and females, simultaneous transfer of pairs of subadult and/or adult males (sometimes relatives) into the same social groups, and group fissioning in which males and females of the splinter group join another small social group. We have no unambiguous cases of 2 adulthubadult females migrating together into the same social group. All 6 groups for which reproductive data were available were characterized by either a polyandrous or polygynous (polygyandrous) mating pattern. The results of this study indicate that moustached tamarins reside in small multimale multifemale groups that are likely to contain both related and unrelated adult group members. Kinship and social ties among males appear to be stronger and more longlasting than kinship and social ties among females. We contend that the modal mating system of moustached and many other tamarins is not monogamous, and offer the possibility that cooperative infant care and mating system flexibility in callitrichines evolved from a polygynous mating pattern. 0 1993 Wiley-Liss, Inc. Key words: dispersal, reproduction, demography Received for publication August 19, 1991; revision accepted October 31, 1992. Address reprint requests to Dr. Paul A. Garber, Department of Anthropology, 109 Davenport Hall, University of Illinois, Urbana, IL 61801. 0 1993 Wiley-Liss, Inc. 236 I Garber et al. INTRODUCTION Tamarins and their close relatives the marmosets are unusual among higher primates in the production of twin offspring and the degree to which several adults within a group (helpers) participate in infant care. Among certain species there is evidence that fathers, other adult males, and nonreproductive adult females expend considerable time and effort carrying and exchanging food with the young [Box, 1977; Epple, 1975; Garber, 1986; Garber et al., 1984; Goldizen, 1987a, 1989; Snowdon & Soini, 1988; Stevenson & Rylands, 1988; Tardif et al., 19903. Although in captive settings older siblings frequently participate in infant care, in freeranging groups it remains uncertain the degree to which cooperative caregiving is kin based, and whether male and female helpers are closely related t o the young [Goldizen, 1989; Sussman & Garber, 19871. In callitrichines [sensu Rosenberger, 19811,the evolution of cooperative infant care is associated with a social group composed of 1-4 adult males, 1-4 adult females, and a small number of subadults and young. Regardless of the number of females present in a group, however, only a single female gives birth. Evidence from laboratory investigations indicates that in groups containing more than 1 adult female, generally only a single female exhibits hormonal levels indicative of a normal ovarian cycle [Epple & Katz, 1984; French et al., 19841. Although there are indications that in certain settings the ovarian cycle of daughters may not be suppressed [Abbott, 1984; Tardif, 19841, the ability of an alpha female to control the reproductive opportunities of subordinate females represents a highly specialized behavioral-endocrine mechanism that effectively limits the number of breeding females in the population as well as the number of offspring born into a group a t one time. Traditionally, tamarin and marmoset breeding systems have been described as monogamous extended family social units [Kleiman, 1977; Kleiman et al., 1988; Snowdon & Soini, 19881. This interpretation has been questioned recently in light of more extensive field data on group size and composition, frequency of migration, and evidence of what appears to be a highly variable system of mating [Ferrari & Lopes Ferrari, 1989; Garber et al., 1984; Goldizen, 1987a,b, 1989,1990; Stevenson & Rylands, 1988, Sussman & Garber, 1987; Sussman & Kinzey, 1984; Terborgh & Goldizen, 19851. In particular, long-term field investigations of S. fuscicollis, the saddle-back tamarin, indicate that groups within a single population exhibit mating patterns that are described as functionally monogamous, polyandrous, polygynous, and/or polygynandrous [Goldizen, 1990; Goldizen & Terborgh, 19891. Polyandrous and/or polygynous matings have also been observed in S . mystax [Pruetz & Garber, 1991; Ruth, 19911and Cullithrix humeralifer [Rylands, 1982,19861,and are suspected in other tamarin species including S. imperutor [Goldizen, 1987bl and S. geoffroyi [Garber & Zeigler, in preparation]. A breeding system characterized by intense female competition, reproductive suppression, twinning, and high costs of infant care places severe constraints on individual reproductive opportunities. If the reproductive success of male and female tamarins is dependent on the cooperative rearing efforts of group helpers, then proximate conditions such as the number, age, sex, relatedness, and reproductive condition of animals residing in the same social group, as well as individual opportunities for dispersal into neighboring groups, are likely to regulate the expression and effectiveness of particular mating patterns. In this regard, Goldizen [1990:791has suggested that the mating system of tamarins “appear[sl to be more directly affected by demographic factors . . . than by ecological conditions.” In this paper we present demographic information collected over the course of Mating Patterns in Tamarin Monkeys / 237 10 years on an island population of moustached tamarin monkeys, Saguinus mystax mystax, in Amazonian Peru, and address a series of questions regarding reproductive opportunities, dispersal, patterns of mating, and the role of kinship in primate social interactions. These questions are as follows: 1. What is the demographic structure of the moustached tamarin population on Padre Isla? 2. Is the Padre Isla tamarin population demographically representative of moustached tamarin populations in other areas of Peru? 3. How does the age structure of the population influence male and female reproductive opportunities? 4. To what degree is the ovulatory cycle of subordinate females suppressed, and under what conditions are more than 1 adult female in a group sexually actively? 5. Is there evidence that alloparental behavior is kin based (are the helpers related to the breeding pair)? 6. Is it more likely that cooperative infant rearing and mating flexibility in tamarins evolved from a monogamous or a nonmonogamous breeding system? As used here, the term mating to refers to copulatory behavior. A mating system therefore represents the pool of potential gene donors or the individuals within a group that copulate. In contrast, a breeding system refers only to those individuals that are successful gene donors and produce viable offspring. The term tamarin is restricted to callitrichines of the genus Saguinus. METHODS AND BACKGROUND From June through November 1990, behavioral and demographic information was collected on 16 groups of free-ranging moustached tamarin monkeys inhabiting Padre Isla, a small island (5.2 km2) in the Amazon Basin of northeastern Peru (53"44', W73" 14'). The island is of relatively recent origin, formed approximately 100 years ago from alluvial sediments deposited by the Amazon River. The area is a protected ecological reserve and includes a permanent research station maintained by the Proyecto Peruano de Primatologia. Although mammalian predators, except for domesticated dogs, are absent from the island, constrictors, poisonous snakes, and birds of prey represent significant predatory threats to the tamarins [Heymann, 19871. Moustached tamarins are not native to Padre Isla. In 1977, 1978, and 1980, researchers from the Proyecto Peruano de Primatologia (PPP) and the Ministerio de Agricultura y Alimentaci6n wild-trapped and released 20 S. mystax groups on the island (87 animals) for purposes of research and study. Individuals were sexed, aged, permanently tattooed, and fitted with collars for later field identification. All members of an original wild-trapped group were taken to a particular location on the island, placed in a large outdoor holding cage, and released simultaneously. From 1980 to 1989, the PPP conducted periodic visual and trap censuses of Padre Isla's moustached tamarin population. General information on the vegetation of Padre Ida and the behavior and ecology of the island's tamarins can be found in Moya et al. [19801, Garber et al. [19841, and Norconk [19861. In 1990 we began a study of moustached tamarin mating systems by retrapping and recensusing the population. The procedure used to capture the animals involved habituating an entire group to a baited trap site composed of a single large cage divided into 10 separate compartments, each with its own manually operated door. The compartments were closed by pulling a string that runs from 238 I Garber et al. each door to the blind constructed some 5 meters from the trap. Although more labor intensive than using spring-loaded traps, this method of waiting in a blind and manually closing or opening each door independently has four primary advantages: 1)observation of the group from inside the blind prior to trapping enables the researcher to determine how many animals are in the group and whether all of the animals have entered the traps to feed; 2) the doors are closed silently and other group members are unaware that an individual has been captured; 3) the entire group can be captured in a single day (often in the span of 1-2 hours); and 4) since the animals are unaware of the presence of the researcher, the technique can also be used to monitor changes in the composition of marked groups. Immediately after capture, the group was transported to the field laboratory. Each individual was injected intramuscularly with 0.1-0.15 cc of ketamin HCL (a tranquilizer) and 0.05 cc of torbutrol (an analgesic). The tamarins were examined, measured, weighed, marked with a permanent tattoo, and fitted with an identification collar. Impressions were made of the maxillary and mandibular dentition of each moustached tamarin. Individuals were then assigned to general age categories (i.e., infant, juvenile, subadult, and adult) based on dental development, relative degree of dental wear, and dental stain according t o criteria established by Soini and Soini 119821. Subadults were defined as individuals with all permanent teeth erupted but with canines still not in full occlusion (approximately 12-18 months of age). Adults were defined as individuals with all permanent teeth in full occlusion. The adult category was subdivided into age classes based on the relative amount of stain and wear visible on the incisors and the cusp tips of the canines. Three grades of wear were noted. The Adult 1 (Al) class exhibited unstained (white) teeth and virtually no evidence of dental war, the Adult 2 (A21 class exhibited moderate dental wear (minimal dentin exposure) and slight staining, and the Adult 3 (A3) class was characterized by extreme wear (canines broken, heavy dentin exposure on incisors) and heavy staining. Based on a comparison with 19 animals of known age in the population (e.g., an animal trapped as an infant in 1986 would be 4 years old in 19901, A1 adults are estimated to be 2-4 years of age, A2 adults 4-8 years of age, and A3 adults 8 + years of age. Adult females were scored as pregnant, lactating, or nonreproductive. Pregnancy was determined by uterine palpation. Lactation was determined by the presence of milk in the mammary glands. Age and sex differences in weight and other body measurements were compared using a Student’s t-test. RESULTS Distribution and Population Density of Moustached Tamarins on Padre Isla During the course of the investigation 123 moustached tamarins residing in 17 social groups were encountered on the island. We concentrated our efforts on 16 of these groups and trapped, marked, and released 98 of the 114 animals (86%) associated with these 16 groups. Twenty-six of the animals captured (26%) in 1990 had been captured and tattooed during previous field seasons. For many of these individuals we were able to reconstruct a history of previous group affiliation, previous group partners, and migratory activities. Ten of the tamarins captured were original inhabitants of the island. Five of these were males and five were females. Nine of these “founders” (4 males and 5 females) were released as adults, and thus were at least 12 years of age when recaptured in 1990. All five of these female founders were reproductively active in 1981, and a t least two (#603 and #479) continued to be reproductively Mating Patterns in Tamarin Monkeys I 239 rn I4 d H 2 I+ 60 40 8 i 7; 2o n ADULT SUBADULT JUVENILE INFANT Fig. 1. Age structure of moustached tamarins on Padre Isla, 1990. active in 1990. One of these 12+ year old females was simultaneously lactating and pregnant during our study. The demographic structure of the moustached tamarin population on Padre Isla is presented in Figure 1. The animals trapped included 66 adults, 11 subadults, 6 juveniles, and 15 infants. The ratio of adults to immatures was 2:1, and the number of males and females was approximately equal (1.02:l). Of 31 adult females examined, 7 (22.5%)were pregnant and 7 (22.5%)were lactating. Using dental wear as an indicator of the age structure of the adult population, 38%of the tamarins were classified as young adults (All, 18%as middle-aged adults (A2),and 44% as oldest adults (A3) (Fig. 2). The population density of moustached tamarins on the island is 26 ind/km2. Group Size and Composition Based on a sample of 13 groups in which all or all but one member was trapped, mean group size was 7,including 2.2 adult males and 2.0 adult females (Table I). The largest bisexual group contained 11animals, and the smallest bisexual group contained 4 animals. The number of adult males in these groups ranged from 1-3, and the number of adult females ranged from 1-4. None of the 13 groups was characterized by a single adult male-female pair. Age Structure of the Island Population Using dental wear as an indication of relative age, and assuming that males and females wear their dentition at equal rates, there were considerably more A3 (oldest) males in the population (27% of adults) than A3 females (15% of adults) (Figure 2). Although this disparity is not statistically significant (X2 = 1.6; d.f. = 1;P > .05), and could reflect sampling error or short-term perturbations in malefemale sex ratios at birth, there is some indication that competition for a limited number of breeding opportunities may contribute to increased female dispersal and possibly increased female mortality. Despite the fact that direct acts of aggression between females residing in the same group are infrequent, none of the 13 social groups contained more than 1 A3 or 1 A2 female (Table 11). Apparently females of these older age categories are intolerant of age mates and exclude them from cohabiting in the same social group. This is in marked contrast to the behav- 240 I Garber et al. 30 3 25 20 15 10 5 0 AM3 AF3 AM2 AF2 AM1 AF1 ADULT AGE CATEGORIES Fig. 2. Adult age composition of moustached tamarins on Padre Isla, 1990. TABLE I. Sue and Composition of 13 Moustached Tamarin Groups on Padre Isla, 1990 GI-OUD Adult males Adult females Orange 1 Silver 1 Rosado 1 Copper 2 Green 2 Red 3 Celeste 3 Blue 3 Brown 3 White 3 Purple 3 Beige 4 Orange 4 Total Mean 2 2 3 1 3 3 3 2 2 2 2 2 2 29 2.2 2 2 4 3 1 3 2 1 2 1 2 1 2 26 2.0 Group size 6 6 11 5 6 11 6 4 9 6 9 4 8 91 7.0 ior of adult males. Thirty-eight percent of the groups on Padre Isla were composed of either 2 A3 or 2 A2 males. In virtually all of the groups censused, it is the oldest female that breeds (see below). Our records indicate that 78% of the A3 females and 67% of the A2 females were either pregnant or lactating at the time of capture. In contrast only 21% of the A1 females were pregnant or lactating. Young adult females on Padre Isla rarely produce offspring. Two groups provide exceptions. In the Rosado 3 group (not listed in Tables I and I1 because more than 1 group member was not trapped), the A3 Mating Patterns in Tamarin Monkeys / 241 TABLE 11. Age Structure of Adult Group Members in Moustached Tamarins. Padre Isla. Peru 1990 Adult males Group Orange 1 Silver la Rosado 1 Copper 2 Green 2b Red 3 Celeste 3 Blue 3 Brown 3 White 3 Purple 3 Beige 4 Orange 4" Total' Totald Adult females A3 A2 A1 A3 A2 A1 2 1 0 1 0 2 2 1 1 0 2 0 0 0 1 1 1 1 1 1 0 1 0 1 1 0 0 0 1 0 1 0 0 2 2 8 5 6 0 2 14 18 1 2 0 0 1 0 0 0 2 0 1 0 7 7 0 2 0 1 1 1 0 0 1 0 7 7 11 0 0 1 0 0 1 0 1 0 0 0 2 1 1 0 0 1 1 1 11 13 "A lactating female in this group was observed but not examined. bAn adult male in this group was observed but not examined. 'Groups in which more than 1 member was not trapped are omitted from these calculations. dData from all 16 groups. female died in August and the lone remaining A1 female became pregnant in September. The blue group was the other social unit characterized by a single young adult breeding female. She was the only female in her group and was observed nursing a single infant. This group of four was the smallest bisexual group on the island. We have no examples from the 1990 trapping period of groups with more than 1 adult female in which only the youngest female was reproductively active. Although there was no evidence that more than 1 female in a group was lactating or had recently given birth, 23%(3/13) of the complete groups contained either 2 pregnant or 1 pregnant and 1 lactating female. In each case, these were among the largest groups in the population, averaging 10 animals per group. These groups were also similar in that it was an A3 female that was lactating/ pregnant, and an A2 female that was pregnant but not lactating. These data suggest that when groups size exceeds 9, the ability of the older dominant female to suppress ovulation and reproductive activities in a younger subordinate female is significantly diminished. Although we cannot discount the possibility that in groups with 2 reproductively active females, one of the females was a recent migrant and entered the group already pregnant, given that only l female in a group gives birth (we have no evidence of more than 1 lactating female in any group), reproductive competition in these females appears to result in abortion, expulsion, or group fissioning. Body Size and Reproductive Activity In an attempt to determine whether particular body measurements were correlated with reproductive sovereignty or reproductive condition, we compared body weight, crown-rump length, genital size, nipple length, and suprapublic gland size among adult females. The results (Table 111) indicate that A3 females are not 242 I Garber et al. TABLE 111. Body Size Measurements of Adult Male and Female Moustached Tamarins, Padre Isla. 1990 ~~ Adult females A3 (N Body weight (grams) Body length (cm) Vulva area (mm2) Gland area (mm2) Nipple length" (mm) = A2 (N 10) 585.3 + 55 239 + 7.8 3.69 + 1.0 2.82** + .97 3.66* + 0.92 = A1 (N 6) 564.1 + 56 245 + 6.8 3.44 + 1.0 2.35 + .72 1.57 + 0.43 = 13) 560.8 + 42 239 + 9.9 3.23 + 1.1 2.03 + .74 1.80 + 0.89 Adult males A3 (N = 18) Body weight (grams) Body length (mm) Testes volumeb (mm2) A2 (N = 6) A1 (N = 6) 567.5 + 75 243 + 7.4 544.6 + 34 243 + 6.9 550.4 + 36 243 + 5.0 6.87 + 2.9 5.91 + 2.9 4.78 + 1.4 aLactatingfemales were excluded from the calculations. Sample size includes 6 A3 females, 5 A2 females, and 11 A1 females. bTestes volume was calculated using the equation Vol = 3.14 (xy2Y6. x, testes length; y, testes width. *Significantly greater in Adult 3 females than in either A2 or A1 females (P < ,001). **Significantlygreater in Adult 3 females than in A1 females (P < . O W significantly heavier, longer, or characterized by larger genitalia than either A1 or A2 females. Differences in the size of the suprapublic gland between A3 and A1 females were statistically significant (t = 2.10;P < .05), however, and gland area may provide a general measure of distinguishing older and/or reproductively active females from younger and nonreproductive females. The suprapublic gland, which is reported to play an important role in socio-sexual behavior and perhaps reproductive suppression [Snowdon & Soini, 19881, averaged 2.82 cm2 in A3 females, 2.35 cm2 in A2 females, and 2.03 cm2 in A1 females. In only 1 group in our sample was the area of the suprapublic gland larger in a nonreproductive female than in a reproductive (pregnant or lactating) female. Data on nipple length in nonlactating moustached tamarin females provide additional support for the contention that older adult females are the principal breeders. Mean nipple length in A3 females was 3.6 mm. In A2 and A1 females nipple length was 1.5 mm and 1.8 mm, respectively (Table 111). Differences between A3, A2, and A1 females were significant (P = .001). If nipple size is an indication of previous breeding activity, it appears that in this population A2 females were not significantly more likely to have reproduced successfully than A1 females. A similar analysis of body measurements in male moustached tamarins (Table Mating Patterns in Tamarin Monkeys I 243 TABLE IV. Age and Sex Status of Solitary Migrant Moustached Tamarins on Padre Isla. 1981-1982 ~~ ~ Adult male 1981 1982 TOTAL Subadult male Adult female Subadult female 5 Total no. trapped 2 4 0 41% of animals trapped were solitary migrants 1 0 2 1 14% of animals trapped were solitary migrants 27 1 56 6 2 6 29 111)failed to indicate significant differences in body weight, body length, and testes volume (male moustached tamarins rarely scent mark and have poorly developed suprapubic glands, which are difficult to measure). Based on these body measurements, there was no evidence that any particular age class of adult males had a reproductive advantage or was in better reproductive condition than any other adult age class. Patterns of Migration Field data on several tamarin species indicate that migration is common, and that adults and subadults of both sexes transfer into and out of groups. This same pattern appears to characterize the moustached tamarin population on Padre Isla. Our findings indicate that after their initial introduction onto the island, groups underwent a period of instability. There are several cases in which each of 3 or 4 adults from the same founding group in 1980 individually joined animals from different social groups by 1981. Although the censuses in 1981 and 1982 do not allow us to calculate precise rates of migration or identify the effects of mortality on group stability, one year after being released on the island 41% of the adults/ subadults recaptured had transferred as individual migrants into a new social group (Table IV). These migrants included adult and subadult males, as well as reproductively active and reproductively inactive adult females. Data from the 1982 census indicate that although immigration and emigration were still common, group composition was considerably more stable. Fewer individuals migrated alone (14%), although both adult males and adult females continued to be the principal migrants (Table IV). Combining the census data collected by the PPP between 1980 and 1989 with our most recent trap census in 1990, we were able to identify a set of migration patterns that are recurrent and appear to characterize this moustached tamarin population. These patterns can be distinguished from other migratory events that occur rarely, if a t all. It must be emphasized that the data base used in these reconstructions has several important limitations. Not all of the groups trapped over the 10 year period represent complete groups, there are significant gaps in life histories of most animals, especially between 1983 and 1987, when only a small proportion of the tamarin population was trapped and tattooed, and in 1986, 29 animals were removed from the island for captive study. Although these problems force us t o qualify many of our conclusions and prohibit statistical treatment of the data, a number of common migratory patterns can be identified. These are described as follows: 1. Individual migrations of adult and subadult females. These include both nulliparous and multiparous females. 244 I Garber et al. 2. Individual migrations of adult and subadult males. These include males of all adult age categories. 3. A large established group splitting into 2 smaller bisexual groups. One of these groups remains in the original range and the other, a more transient group, eventually joins another small social group. 4. Two adultlsubadult males migrating together into the same social group. We have 8 unambiguous examples of male-male dispersal. In one case, the migrants were twin A1 brothers. In 2 additional cases the males were of the same age class but of unknown genealogy (1 pair of subadults and 1pair of A1 males). In 3 of the remaining cases the paired migrants were of different age classes (A31A1 or AISA). Our data indicate that these migrants have remained together in their new social group from 4 to over 8 years. 5. Absence of identifiable cases of 2 adult and/or subadult females migrating together into the same social group. We did, however, encounter a stable group of 3 adult females that after a period of several months was joined to 2 immigrant males. 6. An adult offspring remaining in the same group as its mother. We have 2 unambiguous cases of fully adult offspring remaining in their natal group. In the first instance, a 3-year-old female continued to reside in the same group as her A3 mother. Neither female was pregnant or lactating a t the time of capture. In the second example, an adult male has remained in the same breeding group as his mother for a period of 8 years. His mother remains the dominant/breeding female of the group. We have no evidence of whether or not her son is reproductively active. At present our data base is insufficient to identify how many of the young adults in the population are offspring of other adults in their group, and the degree to which adult offspring care for younger siblings. Mating Activities During the 1990 field season we also conducted a detailed 6 month investigation of mating behavior and social interactions in 2 marked moustached tamarin social groups. The copper group was composed of 3 adult females and 2 males (1A3 male and 1subadult) that had immigrated together into the group. The A3 male was observed to copulate with each of the group’s 2 oldest females. The subadult male was observed to copulate only with the oldest female. Given that 2 males and 2 females in this group were sexually active and copulated during a time coinciding with the breeding season, the mating pattern of this group is provisionally described as polygynous (polygynandrous). Our second study group, the green group, consisted of a lactating A3 female, 3 adult males, and 2 infants. Four copulations were observed in the this group over a 5 day period. One male copulated on 2 occasions and the other two males were each observed to copulate once. The mating pattern of this group is described as polyandrous. During copulatory activities there was no evidence of increased levels of intrasexual aggression or behaviors generally associated with mate guarding or consort relationships in either group. 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 composed 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 cen- Mating Patterns in Tamarin Monkeys I 245 sused groups on the island were characterized by a single adult male and a single adult female. Social groups composed of more than 1adult of each sex are reported in many 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, 19851. Based on observations in 2 target study groups and evidence of more than 1 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 August 1990 of polyandrous matings in another group on the island also have been reported [Ruth, 19911. Each of the 3 groups with more than 1 sexually active female contained a t least 2 adult males. Although we lack information on whether more than 1male 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 [19851 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 [19881 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 are 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 be greater than 8 years of age. At 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 [Dawson, 1977; Neyman, 19771, A2 females in this population are no more likely to have successfully produced offspring than A1 females. In social groups of 9 or larger, suppression of subordinate females is less complete, and although more than 1female may conceive only 1female 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, 19901, S . fuscicollis [Goldizen, 19901, and Callithrix flaviceps 246 I Garber et al. [Ferarri & Lopes Ferrari, 19891. Among tamarins and marmosets, variance in female reproductive output appears to be more extreme than 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, 19771, S. oedipus [Neyman, 19771, and in other populations of S. mystax [Ramirez, 1984; Soini & Soini, 19821. A study by Ramirez [19841 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 [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, 1was an A3 male, 2 were A1 males, 1 was an adult male of unknown age, and 1was a subadult male. In both of our study groups there was no indication of intra-group mate guarding, and more than 1male 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 A1 and A2 males in the population have considerably more reproductive opportunities then A1 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  on their main study group of Callithrix flaviceps Mating Patterns in Tamarin Monkeys I 247 TABLE V. Demographic Comparison of Moustached Tamarins on Padre Isla With Other Moustached Tamarin Populations in Northeastern Peru Demographic data No. of groups Mean group size Range group size No. adult male/group No. adult female/group Adult composition of groups (%) Old adult males in populationb(%) Old adult females in populationb (%I Young females that breed"(%) PoDulation densitv ~~ ~ Padre Isla Other sites" 13 7.0 4-11 1-3 1-4 68 19 10 21 26 ind/km2 133 5.3 3-9 1-4 1-4 67 15 10 25 23-32 ind/km2 ~ aData adapted from Soini and Soini [19821 and Snowdon and Soini [19881. Moustached tamarins live-trapped from sites on the Rio Maniti, Rio Tahuayo, and Rio Tapiche, Northeastern Peru. bSoini and Soini [19821 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 119821 criteria (mature adults: canines considerably worn and teeth stained; old adults: canine and other teeth very worn or decayed), our old adult category is analogous to his mature and old adult categories. "Soini and Soini [19821 define these as females up to 5 years of age. We define these as females up to 4 years of age. 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 pygnaea) 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 are 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. 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 [19823 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, 19891, as well as 248 / Garber et a]. populations of Saguinus fuscicollis [Goldizen, 1989, 1990; Goldizen & Terborgh, 19891. 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, 19861, 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, 19851, Saguinus oedipus [Neyman, 19771, and Saguinus geoffroyi [Dawson, 19771. 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, 19771, it is likely that decisions concerning dispersal and dispersal success are strongly influenced by the availability of reproductive opportunities [Goldizen, 19891. In S . fuscicollis migrants are known to disperse into both nearby (44%)and distant (56%) territories [Goldizen, 19891. 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, 19881, 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 boups on the island we were able to identify the presence of a paired set of immigrant males, it is likely that male kinshiphocial 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, 19771. The final question relates t o 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, 19841 and represent the ancestral condition for tamarins and marmosets [Goldizen, 1990; Kinzey, 19871. 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, Mating Patterns in Tamarin Monkeys / 249 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, 19811, 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, 19921, 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:llOl. 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 [19871 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, he 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 but 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) (e.g., 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 et al., 19871 that cannot also be found in species such as Cebus apella [Janson, 1984; Robinson & Janson, 19871, Alouatta seniculus [Crockett, 1984; Crockett & Eisenberg, 1987; Sekulic, 19831, or Alouatta pigra [Bolin, 1981; Horwich, 1983; Neville et al., 19881. 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 1 female breeds [Masataka, 1981; Pook & Pook, 19811. 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 250 I Garber et al. TABLE VI. Comparison of Social and Reproductive Patterns in Select New World Primate Taxa* Behavior Callicebus moloch Aotus Saguinus mystax Cebus apella Alouatta seniculus Alouatta pigra 2-5 2-5 4-13 8-20 4-10 2-10 - - + ++ ++ + ++ ++ + + + + + + + + + + + ? Group size Multimale/ multifemale group Female mates exclusively with a single male Flexible mating and group structure Dispersal of both sexes Adults may remain (temporarily) in natal group Intolerance of same sex adults within the social group Male parental care Alloparenting by nonadults Limited number of female breeding positions Only 1 female Per group gives birth Reproductive twinning Reproductive suppression in subordinate females ~~~~ ++ ++ - ++ ++ ++ + + + ++ ? ++ ++ ++ ++ ++ ++ - - ++ ~~~ - + ++ ~ * + + , 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. 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 matinglbreeding system in other platyrrhine taxa. Mating Patterns in Tamarin Monkeys I 251 CONCLUSIONS 1. Data collected on patterns of mating, dispersal, and reproduction in an island population of moustached tamarin monkeys (Saguinus mystccx) indicate that these callitrichines live in small multimale multifemale social groups. The adult composition of social groups was highly variable, ranging from 1-4 adult females and 1-3 adult males. None of the 13 completely censused groups contained a single adult male and a single adult female at the time of capture or during subsequent censuses. 2. All 6 groups for which data are available were characterized by either a polyandrous or a polygynous (polygyandrous) mating system. 3. In all groups with more than 1 female it is only the oldest female that produces offspring. Most of these females are known or estimated to be a t least 8 years of age. Young (2-4 years of age) and middle (4-8 years of age) aged females rarely reproduce. The mating system of this tamarin species is best described in terms of age-dependent female reproductive sovereignty. Based on both morphological and behavioral information, there was no evidence that reproductive activity in male moustached tamarins was similarly age dependent. 4. In this population migration is common, and adults and subadults of both sexes individually transfer into and out of groups. There is also evidence that males often migrate as pairs into the same social group. Twenty-three percent of the groups on the island contained a paired set of immigrant males. These males remain together in this new group for up to 8 years. We have no unambiguous cases of paired female migration. It is likely that male kinshiphocial bonds form the basis for much of the cooperative infant care exhibited by these tamarins. 5. We conclude that there is no compelling evidence to support the contention that the modal mating system of moustached and other tamarin species is monogamous, and offer the possibility that mating system flexibility and cooperative infant care in callitrichines evolved from a polygynous mating pattern. ACKNOWLEDGMENTS This research was supported in part by grants from the National Geographic Society, The William and Flora Hewlett Foundation, and the Research Board of the University of Illinois. Logistical support and guidance in Peru were provided by Dr. Jaime Moro of the Instituto Veterinario de Investigaciones Tropicales Y de Altura (I.V.I.T.A.). We acknowledge the following people for their valuable assistance in the field: Eriberto Mermao, Walter Mermao, Jose Oscano, Walter Vasquez, Carlos Ique, and Didier Lamy. 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