close

Вход

Забыли?

вход по аккаунту

?

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 [1989] 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. We thank Jim and Lois Bresedine, owners
of Breezy’s Tattoo Parlor in Rantoul, Illinois, for providing instruction on how to
build and run a battery-operated tattoo machine. Comments on earlier drafts of
this manuscript were provided by Dr. Lynette Norr, Dr. MaryLou Harrison, Dr.
Suzette Tardif, and 3 anonymous reviewers. We also thank Lynette, Sara, and
Jenni for letting me spend a summer with the tamarins.
REFERENCES
Abbott, D.H. Behavioral and physiological
suppression of fertility in subordinate marmoset monkeys. AMERICAN JOURNAL
OF PRIMATOLOGY 61169-186,1984.
Bolin, I. Male parental behavior in black
howler monkeys ( Alouatta palliata pigra)
in Belize and Guatemala. PRIMATES 22:
349-360,1981.
Box, H.O. Quantitative data on the carrying
of young captive monkeys (Callithrixjacchus) by other members of their captive
SOUP. PRIMATES 181475-484, 1977.
Buchanan-Smith, H. Polyspecific association of two tamarins species, Saguinus labiatus and Saguinus fuscicollis,in Bolivia.
AMERICAN JOURNAL OF PRIMATOLOGY 22:205-214,1990.
Crockett, C.M. Emigration by female red
252 I Garber et al.
howler monkeys and the case for female
competition.
159-173 in FEMALE
PRIMATES: STUDIES BY WOMEN PRIMATOLOGISTS. M. Small, ed. New York,
Alan R. Liss, 1984.
Crockett, C.M.; Eisenberg, J.F. Howlers:
Variations in group size and demography.
Pp.54-68 in PRIMATE SOCIETIES. B.B.
Smuts, D.L. Cheney, R.M. Seyfarth, R.W.
Wrangham, T.T. Struhsaker, eds. Chicago,
The University of Chicago Press, 1987.
Dawson, G.A. Composition and stability of
social groups of the tamarins, Saguinus oedipus geoffroyi, in Panama. Pp. 23-38 in
BIOLOGY AND CONSERVATION OF
THE CALLITRICHIDAE. D.G. Kleiman,
ed. Washington, DC, Smithsonian University Press, 1977.
Eisenberg, J.F. THE MAMMALIAN RADIATIONS: AN ANALYSIS OF TRENDS IN
EVOLUTION, ADAPTATION, AND BEHAVIOR. Chicago, University of Chicago
Press, 1981.
Epple, G. Parental behavior in Saguinus
fuscicollis ssp. (Callitrichidae). FOLIA
PRIMATOLOGICA 241221-238,1975.
Epple, G.; Katz, Y. Social influences on estrogen excretion and ovarian cyclicity in
saddle back tamarins (Saguinus fuscicolZis). AMERICAN JOURNAL OF PRIMATOLOGY 61155-168,1984.
Ferarri, S.F.;Lopes Ferrari, M.A. A re-evaluation of the social organization of the Callitrichidae, with reference to the ecological
differences between genera. FOLIA PRIMATOLOGICA 52:132-147, 1989.
Ford, S.M.; Davis, L.C. Systematics and
body size: Implications for feeding adaptations in New World monkeys. AMERICAN
JOURNAL OF PHYSICAL ANTHROPOLOGY 88~415-468,1992.
French, J.A.; Abbott, D.H.; Snowdon, C.T.
The effect of social environment on estrogen excretion, scent marking and sociosexual behavior in tamarins (Saguinus
oedipus). AMERICAN JOURNAL OF PRIMATOLOGY 6:155-168, 1984.
Garber, P.A. Social organization and patterns of infant transport in Saguinus mystax in Amazonian Peru. PRIMATE REPORT 14:78 (abstract), 1986.
Garber, P.A. Diet, foraging patterns, and resource defense in a mixed species troop of
Saguinus mystax and Saguinus fuscicollis
in Amazonian Peru. BEHAVIOUR 105:
18-34,1988.
Garber, P.A.; Moya, L.; Malaga, C. A preliminary field study of the moustached tamarin monkey (Saguinus mystax) in northeastern Peru: Questions concerned with
the evolution of a communal breeding system. FOLIA PRIMATOLOGICA 42:17-32,
1984.
h.
Goldizen, A.W. Facultative polyandry and
the role of infant-carrying in wild saddleback tamarins (Saguinus fuscicollis) BEHAVIORAL ECOLOGY AND SOCIOBIOLOGY 20:99-109,1987a.
Goldizen, A.W. Tamarins and marmosets:
Communal care of offspring. PP. 34-43 in
PRIMATE SOCIETIES. B.B. Smuts, D.L.
Chenes, R.M. Sevfarth. R.W. Wrangham.
T.T. St-ruhsaker, ids. Chicago, The Ukver;
sity of Chicago Press, 1987b.
Goldizen, A.W. Social relationships in a cooperatively polyandrous group of tamarins
(Saguinus fuscicollis). BEHAVIORAL
ECOLOGY AND SOCIOBIOLOGY 24:7989, 1989.
Goldizen, A.W. A comparative perspective
on the evolution of tamarin and marmoset social systems. INTERNATIONAL
JOURNAL OF PRIMATOLOGY 11:6383, 1990.
Goldizen, A.W.; Terborgh, J . Demography
and dispersal patterns of a tamarin population: Possible causes of delayed breeding.
AMERICAN NATURALIST 134208-224,
1989.
Harrison, M.L.; Tardif, S.D. Kin preference
in marmosets and tamarins: Suguinus oedipusi and Callithrix jucchus (Callitrichidae, Primates). AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY
77:377-384, 1988.
Hevmann. E.W. A field observation of medhtion on a moustached tamarin (Supuz&
mystax) by an anaconda (Eunectes-murinus). INTERNATIONAL JOURNAL OF
PRIMATOLOGY 8:193-195, 1987.
Horwich, R.H. Breeding behaviors in the
black howler monkey (Alouattu pigra) of
Belize. PRIMATES 24:222-230, 1983.
Izawa, K. A field study of the ecology and
behavior of the black-mantle tamarin
(Saguinus nigricollis). PRIMATES 19:
241-274, 1978.
Janson, C.H. Female mate choice and mating system of the brown capuchin monkey
Cebus apella (Primates: Cebidae). ZEITSCHRIFT FUR TIERPSYCHOLOGIE 65:
177-200, 1984.
Kinzev. W.G. A wimate model for human
mating systems: Pp. 105-114 in THE EVOLUTION OF HUMAN BEHAVIOR. PRIMATE MODELS. W.G. Kinzey, ed. Albany, NY, State University of New York
Press, 1987.
Kleiman, D.G. Monogamy in mammals.
QUARTERLY REVIEW OF BIOLOGY 52:
39-69,1977.
Kleiman, D.G.; Hoage, R.J.; Green, K.M.
The lion tamarins, genus Leontopithecus
Pp. 299-347 in ECOLOGY AND BEHAVIOR OF NEOTROPICAL PRIMATES, Vol.
2. R.A. Mittermeier, A.B. Rylands, A.
Mating Patterns in Tamarin Monkeys I' 253
Coimbra-Filho, G.A.B. Fonseca, eds. Washington, DC, World Wildlife Fund, 1988.
Masataka, N. A field study of the social behavior of Goeldi's monkeys (Callimico goeldii) in North Bolivia. I. Group composition,
breeding cycle, and infant development.
KYOTO UNIVERSITY OVERSEAS RESEARCH REPORT OF NEW WORLD
MONKEYS, 23-32,1981.
Moya, L.; Trigoso, M.; Heltne, P.G. Manejo
de Fauna Silvestre en Semicautiverio en la
Isla de Iquitos y Padre Isla. An0 1980. INFORME ORDELORETO DIRECCION REGIONAL DE AGRICULTURA Y DIRECCION FORESTAL Y DE FAUNA. Iquitos,
Peru, 1980.
Moynihan, M. THE NEW WORLD PRIMATES: ADAPTIVE RADIATION AND
THE EVOLUTION OF SOCIAL BEHAVIOR, LANGUAGE, AND INTELLIGENCE. Princeton, NJ, Princeton University Press, 1976.
Neville, M.K.; Glander, K.E.; Braza, F.; Rylands, A.B. The howling monkeys, genus
Alouattu. Pp. 349-453 in ECOLOGY AND
BEHAVIOR OF NEOTROPICAL PRIMATES, Vol. 2. R.A. Mittermeier, A.B. Rylands, A. Coimbra-Filho, G.A.B. Fonseca,
eds. Washington, DC, World Wildlife Fund,
1988.
Neyman, P.F. Aspects of the ecology and social organization of free ranging cotton-top
tamarins Suguinus oedipus and the conservation status of the species. Pp. 39-71 in
BIOLOGY AND CONSERVATION OF
THE CALLITRICHIDAE. D.G. Kleiman,
ed. Washington, DC, Smithsonian University Press, 1977.
Norconk, M.A. INTERACTIONS BETWEEN PRIMATE SPECIES IN A NEOTROPICAL FOREST MIXED-SPECIES
TROOPS OF Saguinus mystax AND Suguinus fuscicollis (CALLITRICHIDAE).
Ph.D. thesis, University of California, Los
Angeles, 1986.
Pook, A.G.; Pook, G. A field study of the socioecology of the Goeldi's monkey (Cullimico goeldii) in northern Bolivia. FOLIA
PRIMATOLOGICA 35288-312,1981.
Pruetz, J.D.; Garber, P.A. Patterns of resource utilization, home range overlap, and
intergroup encounters in moustached tamarin monkeys. AMERICAN JOURNAL OF
PHYSICAL ANTHROPOLOGY (Suppl)
12:146, 1991.
Ramirez, M. Population recovery in the
moustached tamarin (Suguinus mystar):
Management strategies and mechanisms
of recovery. AMERICAN JOURNAL OF
PRIMATOLOGY 7~245-259,1984.
Ramirez, M. FEEDING ECOLOGY AND
DEMOGRAPHY OF THE MOUSTACHED TAMARIN Saguinus mystar IN
NORTHEASTERN PERU. Ph.D. thesis,
City University of New York, New York,
1989.
Robinson, J.G.; Janson, C.H. Capuchins,
squirrel monkeys, and atelines: Socioecological convergence with Old World Primates. Pp. 69-82 in PRIMATE SOCIETIES. B.B. Smuts, D.L. Cheney, R.M.
Seyfarth, R.W. Wrangham, T.T. Struhsaker, eds. Chicago, The University of Chicago Press, 1987.
Robinson, J.G.; Wright, P.C.; Kinzey, W.G.
Monogamous cebids and their relatives: Intergroup calls and spacing. Pp. 44-53 in
PRIMATE SOCIETIES. B.B. Smuts, D.L.
Cheney, R.M. Seyfarth, R.W. Wrangham,
T.T. Struhsaker, eds. Chicago, The University of Chicago Press, 1987.
Rosenberger, A.L. Systematics: The higher
taxa. Pp. 9-28 in ECOLOGY AND BEHAVIOR OF NEOTROPICAL PRIMATES, Vol. 1. A.F. Coimbra-Filho, R.A.
Mittermeier, eds. Rio de Janeiro, Academia Brasileria de Ciencias, 1981.
Ruth, B. Observation of polyandrous mating
in a wild-living callitrichid Saguinus mystax. AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY (SUDD~)
12:156
.
(abstract), 1991.
Rvlands. A.B. THE BEHAVIOUR AND
ECOLOGY OF THREE SPECIES OF
MARMOSETS AND TAMARINS (CALLITRICHIDAE, PRIMATES) IN BRAZIL.
Ph.D. thesis, University of Cambridge,
Cambridge, UK, 1982.
Rylands, A.B. Infant-carrying in a wild marmoset group, Cullithrix humeralifer: Evidence of a polyandrous mating system. Pp.
131-144 in A PRIMATOLOGIA NO BRASIL-2. M.T. de Mello, ed. Brasilia, Sociedade Brasileira de Primatologia, 1986.
Savage, A. THE REPRODUCTIVE BIOLOGY OF THE COTTON-TOP TAMARIN
(Saguinus oedipus oedipus) IN COLOMBIA. Ph.D. thesis, University of WisconsinMadison, 1990.
Sekulic, R. Male relationships and infant
deaths in red howler monkeys (Alouattu
seniculus). ZEITSCHRIFT FUR TIERPSCHYOLOGIE 61:185-202,1983.
Snowdon, C.T.; Soini, P. The tamarins, Genus Suguinus. Pp.223-298 in ECOLOGY
AND BEHAVIOR OF NEOTROPICAL
PRIMATES, Vol. 2. R.A. Mittermeier, A.B.
Rylands, A. Coimbra-Filho, G.A.B. Fonseca, eds. Washington, DC, World Wildlife
Fund, 1988.
Soini, P. Ecology of the saddle-back tamarin
Saguinus fuscicollis illigeri on the Rio Pacaya, Northeastern Peru. FOLIA PRIMATOLOGICA 49~11-32,1987.
Soini, P. The pygmy marmoset, genus Cebuella. Pp. 79-129 in ECOLOGY AND BE&.
~
254 I Garber et al.
HAVIOR OF NEOTROPICAL PRIMATES, Vol. 2. R.A. Mittermeier, A.B.
Rylands, A. Coimbra-Filho, G.A.B. Fonseca, eds. Washington, DC, World Wildlife
Fund, 1988.
Soini, P.; Soini, M. Distribucion geografica y
ecologia poblacional de Saguinus mystax
(PRIMATES, Callitrichidae). INFORME
DE PACAYA NO. 6 ORDELORETO, DIRECCION REGIONAL DE ARGICUTURA Y DIRECCION FORESTAL Y DE
FAUNA. Iquitos, Peru, 1982.
Stevenson, M.F.; Rylands A.B. The marmosets, Genus Callithrix. F’D. 131-222 in
ECOLOGY AND BEHAVIOR OF NEOTROPICAL PRIMATES. Vol. 2. R.A. Mittermeier, A.B. Rylands, A. Coimbra-Filho,
G.A.B. Fonseca, eds. Washington, DC,
World Wildlife Fund, 1988.
Sussman, R.W.; Garber, P.A. A new interpretation of the social organization and
mating system of the Callitrichidae. INTERNATIONAL JOURNAL OF PRIMATOLOGY 8:73-92, 1987.
Sussman, R.W.; Kinzey, W.G. The ecological
role of the Callitrichidae: A review.
AMERICAN JOURNAL OF PHYSICAL
ANTHROPOLOGY 64419-449,1984.
Tardif, S.D. Social influences on sexual maturation of female Saguinus oedipus oediP U S . AMERICAN JOURNAL OF PRIMATOLOGY 6:199-210, 1984.
Tardif, S.D.; Carson, R.L.; Gangaware, B.L.
Infant-care behavior of mothers and fathers in a communal-care primate, the
cotton-top tamarin (Saguinus oedipus).
AMERICAN JOURNAL OF PRIMATOLOGY 22:73-85, 1990.
Terborgh, J.; Goldizen, A.W. On the mating
system of cooperatively breeding saddleback tamarins (Saguinus fuscicollis). BEHAVIORAL ECOLOGY AND SOCIOBIOLOGY 16:293-299, 1985.
Wright, P.C. Biparental care in Aotus triuirigatus and Callicebus moloch. Pp.59-76
in FEMALE PRIMATES: STUDIES BY
WOMEN PRIMATOLOGISTS. M. Small,
ed. New York, ALan R. Liss, 1984.
Документ
Категория
Без категории
Просмотров
8
Размер файла
1 458 Кб
Теги
implications, tamarix, mating, platyrrhine, system, demographic, mystax, moustached, patterns, monkey, saguinus, reproduction, reconstruction
1/--страниц
Пожаловаться на содержимое документа