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Behavioral strategies and hormonal profiles of dominant and subordinate common marmoset (Callithrix jacchus) females in wild monogamous groups.

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American Journal of Primatology 67:37–50 (2005)
RESEARCH ARTICLE
Behavioral Strategies and Hormonal Profiles of Dominant
and Subordinate Common Marmoset (Callithrix jacchus)
Females in Wild Monogamous Groups
MARIA BERNARDETE CORDEIRO SOUSA1,2n, ANA CLAUDIA SALES DA ROCHA
ALBUQUERQUE3, FABIOLA DA SILVA ALBUQUERQUE1, ARRILTON ARAUJO1,
MARIA EMILIA YAMAMOTO1, and MARIA DE FATIMA ARRUDA1
1
Curso de Pós-graduação em Psicobiologia, Departamento de Fisiologia, Universidade
Federal do Rio Grande do Norte, Natal, Brazil
2
Curso de Pós-graduação em Cieˆncias da Saúde, Departamento de Fisiologia,
Universidade Federal do Rio Grande do Norte, Natal, Brazil
3
Departamento de Cieˆncias Biológicas, Universidade Estadual do Rio Grande do Norte,
Mossoró, Brazil
New insights into the mating systems of common marmosets suggest that
they are mainly monogamous, although polygyny and polyandry
occasionally occur. Long-term monitoring of wild common marmosets
has shown that some reports of polygynous groups (i.e., groups that
contain more than one reproducing female) in fact indicate an
unbalanced reproductive output associated with extragroup copulation.
In this study we describe the behavioral and hormonal profiles of common
marmoset (Callithrix jacchus) females living in three wild monogamous
groups (Q, PBf, and T), varying from five to 11 individuals, at Nı́sia
Floresta field station, RN, Brazil. The mating system of the groups was
previously characterized in terms of affiliative, sexual, and mate-guarding
behaviors. Behavioral data were collected once a week, and fecal samples
were collected at least twice a week for 10–16 months, depending on the
group. A preferential allogrooming relationship was recorded between
dominant males and females. Under field conditions the reproductive
inhibition of subordinate females appears to be more behavioral than
hormonal, since subordinate females of the three groups ovulated
and two conceived during the study. In these cases, the subordinate
and dominant females reproduced 1 month apart, and infanticide
(one case confirmed and one suspected) appeared to be part of the
reproductive strategy of dominant females. Following the infanticide,
ovarian inhibition (group T) or emigration and return to the natal group
(group PBf) were observed. In the third group (Q) the subordinate female
Contract grant sponsor: CNPq; Contract grant numbers: 464103/00-2; 52.1186/1997; 305216/20035; 470601/2003-1; 524409/96; Contract grant sponsor: CAPES; Contract grant number: 864/91-11.
n
Correspondence to: Maria B.C. Sousa, Universidade Federal do Rio Grande do Norte,
Departamento de Fisiologia, Caixa Postal, 1511, 59078-970 Natal, RN, Brazil.
E-mail: mdesousa@cb.ufrn.br
Received 28 September 2004; revised 3 February 2005; revision accepted 3 February 2005
DOI 10.1002/ajp.20168
Published online in Wiley InterScience (www.interscience.wiley.com).
r
2005 Wiley-Liss, Inc.
38 / Sousa et al.
showed hormonal profiles compatible with pregnancy, but no infants
were seen. These findings reflect the different alternatives that wild
subordinate common marmoset females use to reproduce. Am. J.
r 2005 Wiley-Liss, Inc.
Primatol. 67:37–50, 2005.
Key words: wild common marmosets; monogamy; sexual strategies;
dominance; steroid hormones
INTRODUCTION
The various mating systems of neotropical primates (Callitrichidae
family), such as monogamy, polygyny, and polyandry, have been described
by numerous authors (e.g., C. jacchus [Digby & Ferrari, 1994; Roda & Pontes,
1998], C. humeralifer [Rylands, 1986], C. aurita [Coutinho & Correia, 1995], and
L. rosalia [Dietz & Baker, 1993]). However, recent data regarding the
reproductive output of dominant and subordinate females from nine wild groups,
including two that were analyzed in the present study, have revealed two
profiles: 1) both dominant and subordinate females reproduce and their offspring
survive in almost the same proportion, and 2) although both females give
birth a few days apart, only the offspring of the dominant survive [Arruda et al.,
2005].
Common marmosets are one of the most widely studied neotropical primate
species. They are considered to be singular cooperative breeders [Snowdon, 1996],
with females competing to reproduce [Abbott, 1984]. The hormonal profiles of
dominant and subordinate females living in captive groups were fully described in
previous studies [e.g., Abbott et al., 1984, 1987, 1998; Alencar et al., 1995;
Saltzman et al., 1997a]. These studies demonstrated that dominant females
inhibit the ovarian cycling of subordinate females, probably by means of odor
signaling [Abbott et al., 1993; Smith & Abbott, 1998]. Captive studies have also
shown that reproductive inhibition of subordinate females occurs mainly when
the females are not related [Saltzman et al., 1997a,b; Ziegler & Sousa, 2002].
However, although a wide range of information has been collected from captive
groups, few data are available for wild groups.
To better understand the dynamics of the social relationship between
breeding males and dominant and subordinate common marmoset females in wild
monogamous groups, we performed a long-term field study in northeastern
Brazil, addressing three main questions: 1) what are the differences in social
dynamics among dominant and subordinate females and breeding males, 2) are
subordinate females hormonally inhibited in monogamous groups, and 3) what
strategies are used by subordinate females to reproduce?
MATERIALS AND METHODS
Study Area
This study was undertaken at the National Forest Station (FLONA) in Nı́sia
Floresta county, 45 km from Natal, Brazil, which includes open areas and
secondary forest [Santee & Arruda, 1994]. We studied three groups that occupied
two different areas within the field station. One group occupied an experimental
plantation area [Albuquerque et al., 2001], and the remaining two groups used
previously described areas [Santee & Arruda, 1994].
Monogamy in Wild Common Marmosets / 39
Animals
In this study we examined wild monogamous groups of common marmosets
(Callithrix jacchus). The mating system of the groups was previously characterized
with the use of long-term data from studies based on affiliative, sexual, and mateguarding behaviors, as well as female reproductive output. These groups were
monitored from December 1997 to October 2000. In each group we followed the
breeding male and two females (one dominant and one subordinate). Dominant
status was determined based on the relationship with the breeding male (dominant
females copulated and spent more time interacting with breeding males compared
to subordinates). Identification of the breeding male was based on either long-term
records or the results of a 2-month pilot study in which affiliative, sexual, and mateguarding behaviors were recorded. During the pilot study all individuals were
habituated to the presence of an observer, captured, and marked with collars.
Specific areas of the body were painted with picric acid for identification. In some
animals, trichotomy of the tail was also used to help with individual identification.
Behavioral and Hormonal Data Collection
We observed each group from 5:00 a.m. to 2:00 p.m. using on-the-minute
samples for 15 min each hour for the breeding male and the dominant and
subordinate females. No data were recorded without a 40-min minimum interval
between recordings. Ad libitum records were also obtained for qualitative data,
such as intra- or extragroup copulations and aggressive displays. The analyzed
data did not include information obtained during acute changes in the group’s
routine, such as intergroup encounters. Observation sessions took place once a
week, and the order of observations of focal individuals was randomly established
before data collection began. The behavioral and hormonal sampling both lasted
10–16 months, depending on the group. Table I shows additional information about the groups. The behaviors recorded during the study included
grooming, scent-marking, agonism (vocalization and chasing), and sexual
activities (copulation and attempts). The behavioral definitions followed those
used by Lazaro-Perea [2001] and Lazaro-Perea et al. [2004].
TABLE I. Summary Information About Group Composition, Reproductive Performance of
Females and Study Duration of the Three Monitored Groups
Groups
Q
Total of
individuals
Monitored
females/no. of
parturition
6–5
D (Grécia)/2
Study duration
September 1999 to
October 2000
No. 1-minute
records
No. fecal
samples
by females
8,533
D=62
S (Glenda)a/0
PBf
5–9
D (Patricia)/1
S=66
December 1997 to
April 1999
12,537
S (Paloma)/2
T
9–11
D (Tereza)/2
S (Tina)/1
a
Daughter of dominant female.
D, Dominant females; S, subordinate females.
D=69
S=102
October 1999 to
October 2000
9,266
D=68
S=49
40 / Sousa et al.
Fecal samples were collected from adult females twice a week [Sousa et al.,
2002], and assays were performed as described in Sousa and Ziegler [1998], with
solvolysis used to break up conjugates in the samples [Ziegler et al., 1996].
Enzyme conjugates and antibodies for both hormones were provided by the
University of California–Davis. The intra- and interassay coefficients of variation
for cortisol and progesterone were 11.5% and 23.6%, and 13.6% and 20.3%,
respectively. Hormone values are provided as ng/g of feces.
Data Analysis
All data were examined for normality before the parametric tests were
conducted, and the data were found to be normal. We used the software Statistics
version 5.5 (Statsoft Inc., 1999). Student’s t-test and an analysis of variance
(ANOVA) one-way post hoc Tukey test were used to compare the frequency of
allogrooming and scent-marking behaviors performed by focal animals. For
allogrooming, all interactions performed and received by the focal animals were
analyzed. For both behaviors, hourly frequencies were grouped according to social
status (dominant or subordinate).
The criteria used to characterize ovarian functioning were as follows:
cycling=increase of progesterone during the length of the luteal phase of ovarian
cycle (by what increase, i.e., 50% or higher?); noncycling=progesterone levels
continuously low (or ovarian cycles and pregnancies were determined as
described in Ziegler and Sousa [2002]).
Spearman’s test was used to correlate the cortisol fecal concentrations in
dominant and subordinate females. Significance was pre-established at Po0.05
for all tests.
RESULTS
Behavioral Profiles
The pooled data (from three groups) of allogrooming interactions between
the focal animals (dominant and subordinate females and breeding males) are
shown in Fig. 1. As illustrated in Fig. 1A, the frequencies of grooming performed
by dominant females on both subordinate females and males did not differ. On
the other hand, the amount of grooming received by dominants from males was
significantly higher than that received from subordinates (t-test(1,48)=3.877,
Po0.001). No differences were recorded in the frequency of allogrooming
performed by subordinate females on dominant females and breeding males
(Fig. 1B). Subordinate females also received an equal amount of grooming from
both dominant individuals. Males displayed the highest frequency of grooming
behavior in comparison with the values recorded for females, regardless of
whether they were dominants or subordinates (ANOVA(2,20)=2.326, Po0.05). As
illustrated in Fig. 1C, the mean values of allogrooming performed by males were
preferentially directed to the dominant females, and allogrooming received from
the breeding male by dominant females was significantly higher than that
received by subordinate females (t-test(1,52)=3.423, Po0.01).
Scent-marking behavior did not show significant differences between
dominant and subordinate females living in monogamous groups, although the
mean frequencies for subordinates were higher (Fig. 2). It is interesting to point
out that although n is small (n=2), the mean scent-mark frequencies for the
subordinate females from group Q (Glenda) and group T (Tina) were higher when
they were not cycling compared to those recorded during ovarian cycling (Glenda
Monogamy in Wild Common Marmosets / 41
A
BM
SF
Mean frequency
20
15
*
10
5
0
Performed
Received
B
Mean frequency
20
DF
BM
15
10
5
0
Performed
Received
C
DF
SF
Mean frequency
20
15
*
10
5
0
Performed
Received
Fig. 1. Mean hourly frequency (+SEM) of grooming behavior performed on and received from (A)
dominant females (DF), (B) subordinate females (SF), and (C) breeding males (BM) in monogamous
wild groups of common marmosets. n ANOVA, Po0.05.
42 / Sousa et al.
(noncycling)=5.4071.02; (cycling)=3.2071.30; Tina (noncycling)=11.4377.02;
(cycling)=5.4473.26).
Agonistic behaviors between dominant and subordinate females (i.e.,
vocalization toward the other individual, and chasing behavior) and sexual
behaviors were recorded opportunistically (Q=6; PBf=4; T=5 episodes). Nevertheless, in all recorded instances of agonism between the two females, it was
exclusively directed by the dominant toward the subordinate.
We also recorded all occurrences of sexual behavior (Fig. 3). In groups Q and
T, the dominant females were seen copulating and attempting to copulate with
the breeding male (intragroup copulations). Subordinate females, on the other
hand, were never seen copulating with the breeding male. However, they were
10
Mean frequency
8
6
4
2
0
Dominants
Subordinates
Fig. 2. Mean hourly frequency (+SEM) of scent-marking behavior by dominant (white bar) and
subordinate (black bar) females living in monogamous groups of wild common marmosets.
IGC or attempts BM
6
IGC or attempts SM
Frequency
EGC or attempts
4
2
0
D
Group Q
S
D
S
Group PBf
D
S
Group T
Fig. 3. Total frequency of sexual behaviors (copulation and attempts to copulate) directed by males
to dominant (D) and subordinate (S) females in three monogamous groups of common marmosets.
IGC=intragroup copulation; EGC=extragroup copulation; BM=breeding male; SM=subordinate
male.
Monogamy in Wild Common Marmosets / 43
observed copulating with extragroup males (extragroup copulations) or, in the
case of Q group, also with a nonbreeding male of the same group. In group PBf,
both females were seen copulating and attempting to copulate with the breeding
male, but only the subordinate was seen copulating with extragroup males.
Hormonal Profiles of Dominant and Subordinate Females
Progesterone.
Group Q. Prior to this study, group Q had been hormonally monitored
[Albuquerque et al., 2001] from August 1996 to March 1997, when another
subordinate female (Graça) showed an ovulatory cycle during the pregnancy of
the breeding female (Grécia). Hormonal data from this group were also collected
from April 1998 to May 1999. Another subordinate female (Gertrudes) gave birth
in the natal group, but the offspring was a victim of infanticide by the dominant.
In the current study, dominant and subordinate females from group Q were
monitored from 4 September 1999 to 8 October 2000. As shown in Fig. 4A, the
progesterone profiles of the dominant (Grécia) and subordinate (Glenda) females
fluctuated, and during this period we observed two births from the dominant
female (12 March and 15 August 2000). An increase in progesterone levels for the
subordinate female was recorded during this period, which was compatible with
ovarian cyclicity. Although fecal progesterone remained high for 5 months (from
8 December 1999 to 3 May 2000, as shown in Fig. 4A, which corresponds to the
duration of a full pregnancy), no infants were seen in the group. As previously
presented (Fig. 3), sexual interactions between the subordinate female and an
extragroup male and another male within her group were recorded. The
subordinate female showed a new increase in progesterone 2 months later. From
that time on, fecal collection became discontinuous and most of the Q-group
members disappeared, including the dominant female, breeding male, and
subordinate female. Immediately before the dissolution of the group, this
subordinate female gave birth to two live infants, which, along with their
mother, were not seen afterward. A positive correlation between the cortisol
levels of the dominant and subordinate females (r=0.54, Po0.01) was found
during gestation #1 of the dominant, which was coincident with the maintained
increase in progesterone of the subordinate.
Group PBf. This group was formed by fission from group PB after the
reproductive female died in April 1997 (see Lazaro-Perea [2000] for a full
description). Between April and November 2000, two females bred, but one of the
infants of the subordinate (Paloma) was killed by the dominant female (Patricia),
who gave birth 1 month later. The data presented here correspond to the
monitoring carried out from December 1997 to March 1999. These are the same
two females that were previously studied [Lazaro-Perea, 2000]. Figure 4B shows
fecal progesterone levels in the dominant and subordinate females of the PBf
group. During this time, the subordinate female reproduced twice, whereas the
dominant female reproduced once. Six days after parturition the subordinate
female’s infants were killed by the dominant female, which gave birth 1 month
after the subordinate. Both females remained cycling in the following period until
the subordinate emigrated 4 months later (August 1997). The dominant female
died in September 1997, and only 2–3 days afterward the subordinate female
returned to the group and remained as the breeding female. She gave birth again
in February 1999.
44 / Sousa et al.
Q
2000
D
S
1500
1000
500
10/4/2000
9/4/2000
8/4/2000
7/4/2000
6/4/2000
5/4/2000
4/4/2000
3/4/2000
2/4/2000
1/4/2000
12/4/1999
11/4/1999
10/4/1999
0
9/4/1999
Fecal progesterone (ng/g)
A
Date
B
PBf
*
1500
1000
+
500
36246
36218
36195
36173
36148
36117
36099
36074
36042
36021
35991
35965
35941
35916
35895
35874
35847
35817
0
35782
Fecal progesterone (ng/g)
2000
Date
C
*
1500
1000
500
36825
36787
36763
36739
36720
36697
36677
36658
36645
36627
36601
36575
36559
36539
36512
36497
36481
36468
0
36449
Fecal Progesterone (ng/g)
T
2000
Date
Fig. 4. Fecal progesterone profile of dominant and subordinate females in groups Q, PBf, and T
during monitoring. The dotted vertical line indicates parturition of the subordinate female, and
the full line indicates that of the dominant females. The asterisk (n) indicates the occurrence of
confirmed (group PBf) or suspected (group T) infanticides. The arrow corresponds to the date
when a subordinate emigrated from her natal group, and + corresponds to the death of the
dominant female.
Group T. Group T was monitored for a total of 12 months, from 16 October
1999 to 16 October 2000. Similarly to observations made in group PBf, the
subordinate female gave birth twice, and her first birth (8–9 February)
occurred only 1 month before the parturition of the dominant (9 March), as
Monogamy in Wild Common Marmosets / 45
illustrated in Fig. 4C. The offspring of the subordinate were likely killed, and
although no newborn infanticide was witnessed, aggressive episodes from the
dominant male and female directed toward the subordinate female suggest
the occurrence of infanticide. Another finding that suggests infanticide was a
cortisol increase in both females around that time, as was noted in group
PBf when infanticide occurred. The subordinate female of group T remained
in the group without any apparent sign of pregnancy until April 2001 (when
she was last seen in the field station area, a month before the entire
group disappeared).
Cortisol
The mean values for cortisol excreted in feces were similar for dominant
(129.12722.09 ng/g) and subordinate (116.97720.02 ng/g) females. The mean
values for cortisol when subordinate females were cycling were higher than when
they were not cycling (193.117476.91 ng/g, and 47.69790.78 ng/g, respectively).
Also the values for fecal cortisol were higher during gestation #2 (30.92757.32
ng/g) compared to gestation #1 (298.607381.38 ng/g) for the subordinate female
of PBf group, but not for the two successive pregnancies of the dominant females
in the Q and T groups (173.467349.11 ng/g, and 122.357345.27 ng/g,
respectively).
During the two episodes of infanticide perpetrated by dominant females
toward subordinate offspring in groups T and PBf, acute increases in cortisol
were recorded in both dominant and subordinate females, as shown for group PBf
in Fig. 5. For subordinate females, the increase was about twice that observed
for dominants.
Fecal cortisol (ng/g)
2000
*
+
1500
1000
500
3/13/1999
2/10/1999
1/16/1999
12/19/1998
11/13/1998
10/24/1998
9/19/1998
8/19/1998
7/22/1998
6/19/1998
5/22/1998
4/24/1998
3/31/1998
3/1/1998
1/25/1998
12/18/1997
0
Date
Fig. 5. Concentration of fecal cortisol excreted by dominant (-’-) and subordinate (–J–) females of
group PBf during the monitoring. The dotted line indicates parturition (n=2) of the subordinate
female, and the full line shows the parturition of the dominant. The arrow corresponds to the date
when a subordinate emigrated from her natal group, + corresponds to the death of the dominant
female, and n corresponds to the infanticide episode.
46 / Sousa et al.
DISCUSSION
The findings of our study show that a preferential relationship between
breeding males and females occurs in wild monogamous common marmoset
groups, even when more than one female gives birth. We found that allogrooming
reciprocity within the dominant pair was significantly higher than that observed
between breeding males and subordinate females, and between dominant and
subordinate females. Also, males were the main groomers in all three groups, as
recorded for six groups (group Q in a different period, and five other groups) in
the same field area [Lazaro-Perea et al., 2004].
Although we found high mean values for scent-marking behavior performed
by subordinates, they were not significantly different from those of dominant
females. Our results are similar to those recorded for five groups of common
marmosets living in the same field station, including group Q (prior to our study)
[Lazaro-Perea et al., 1999]. This study found no strict correlation between scentmarking and reproductive dominance or territoriality. Higher scent-marking
during the noncycling periods for subordinates may indicate avoidance of agonism
from dominant females, since scent-marking during the cycling period may be
seen as a challenge to the dominant’s status. Complete suppression of scentmarking by subordinates was not observed, given the importance of this behavior
for attracting potential mates from neighboring groups, as suggested by LazaroPerea et al. [1999]. Other evidence from the literature points out the flexibility of
this behavior in common marmosets, which frequently varies according to social
context [Epple, 1970; Lazaro-Perea et al., 1999], light/dark cycle [Nogueira et al.,
2001], and reproductive condition [Evans & Poole, 1983, Nogueira et al., 2001],
among other factors.
The mean dominant and subordinate female cortisol fecal levels were similar;
however, we were unable to analyze basal levels because the females all
experienced different reproductive conditions during the study, including
noncycling, cycling, pregnancy, and postpartum phases. Consequently, since
cortisol levels depend on the physiological condition of the female, these data
could not be properly interpreted. However, cortisol levels increased dramatically
during infanticide, and this may safely be regarded as an indication of extreme
stress in both dominant and subordinate females (but mainly in the subordinates
whose offspring were killed).
Aggression was mostly low in the wild groups we monitored. Nevertheless, on
the few occasions that we witnessed it (infanticide episodes included), it was
directed from the dominant toward the subordinate female. This is in line with
a previous study in which aggression between a mother and daughter was mild
and infrequent [Saltzman et al., 2004]. The restricted cortisol peaks we recorded
for wild females are likely related to specific conditions. This suggests that
subordinate females are able to thwart potential aggression by the dominant
female using mechanisms that have not yet been identified.
In general, the progesterone fecal profiles during pregnancy showed a
regular, repeated fluctuation pattern similar to that of plasma. However, the
expected maintained progesterone increase, from the 12th week until shortly
before parturition, was not well characterized on all occasions (for instance,
during Tina’s pregnancy). In these cases, we used the pregnancy duration to
estimate the beginning of the gestation period [Hearn, 1983].
Sexual activity (copulations and copulation attempts) by the dominant
females in all three groups was observed exclusively with the breeding male.
Subordinate females from all three groups were seen copulating with extragroup
Monogamy in Wild Common Marmosets / 47
males. We recorded five births by dominant females and three by subordinate
females in groups Q, PBf, and T, but only the infants born to the dominant
females survived.
Breeding vacancies are rare and unpredictable for female common
marmosets. Therefore, nonbreeding females have to decide among many
alternatives, such as delaying reproduction and remaining in their natal group,
contesting the dominant female and attempting to breed in her natal group
(which may open the way for inheriting the breeding position) with either an
extragroup male or the breeding male (if he is not her father), filling in a breeding
vacancy in a neighboring group, or migrating and trying to find a breeding
vacancy [Arruda et al., in press]. All of these alternatives imply costs, and their
potential for success is varied.
Subordinate common marmoset females may or may not escape reproductive
suppression. Data from captive groups show that up to 50% of subordinate
females escape this suppression in family groups [Abbott, 1984; Saltzman et al.,
1997a]. Recent hormonal data from wild groups suggest there is usually more
than one ovulating female in every group [Albuquerque et al., 2001, 2004].
Alencar et al. [1995] suggested that the ability to escape reproductive suppression
is related to the type of dominant relationship that exists between dominant and
subordinate females. Our results suggest that at least one subordinate female in
each wild group is able to escape reproductive suppression. Although Emlen
[1991] considered that this may demonstrate increased tolerance by dominant
individuals, allowing for limited breeding by subordinates, Clutton-Brock [1998]
offered a critique of this model and suggested that subordinates breed simply
because dominants are unable to prevent it. Saltzman et al. [2004] found that the
replacement of the breeding male by an unrelated male in captive family groups
may favor reproduction by subordinate females (daughters), depending on their
relationship with their mothers, because only nonsubmissive, cycling subordinates were able to breed in the presence of a new, nonrelated male.
Both our behavioral and hormonal data are in agreement with the
conclusions drawn by Clutton-Brock [1998] and Saltzman et al. [2004]. The
allogrooming and aggression between females, and the differential relationship of
grooming and sexual behavior between the breeding male and the two females
suggest that there is a hierarchy between the females, and also that the bond
between the male and the dominant female is stronger than that with the
subordinate female. Nevertheless, subordinate females in all groups bred (in
group Q, the subordinate female gave birth to two infants a few months after
hormonal monitoring had ceased). This suggests that the dominant female was
not able to prevent subordinates from either cycling or breeding.
Subordinate females face another constraint, which is finding a suitable
mate. In some groups, the breeding male may be related to subordinates (as the
father or a brother) [Araújo, 1996]. Extragroup males could fit the role of
unrelated mate, which would explain the extragroup copulations observed in the
current study and by Arruda et al. [in press] in these and other groups from the
same population. In fact, extragroup males are the likely source of social cues that
induce the activation of the reproductive function in subordinate females, as
suggested by Saltzman et al. [1997b, 2004]. The idea of extragroup males as
potential or, occasionally, actual mates would also explain the higher levels of
scent-marking by subordinate females that have also been reported for the same
population [Lazaro-Perea et al., 1999].
However, group PBf does not fit this model. In contrast to the other two
groups, the subordinate female received more grooming from the breeding male
48 / Sousa et al.
compared to the dominant female, and was seen copulating with the breeding
male, as well as with extragroup males. This group was formed after another
group (PB) dissolved when the breeding female died. Group PB split [LazaroPerea, 2000] into two groups: all females in one group (PBf), and all males in the
other (PBm). When we initiated this study, the PBf group was restructuring and
both females were likely kin and competing for the breeding position. Paloma, the
subordinate female, gave birth twice, and on both occasions her offspring were
killed by Patricia, the dominant female [Arruda et al., 2005].
The infanticide witnessed in the PBf group shows that escaping reproductive
suppression and finding a suitable mate are only the first steps toward successful
breeding. Offspring survival depends on the type of relationship the subordinate
mother has with the dominant female, and to what extent the latter will tolerate a
second breeder in the group. Polygyny has been reported in wild C. jacchus
[Arruda et al., 2005; Barreto, 1996; Digby & Ferrari, 1994], but if its costs are so
high that infants’ survival is highly unlikely, other alternatives must be sought.
This was the case for these three females. Paloma, the PBf subordinate female,
tried unsucessfully to gain a breeding position. After two failed attempts to breed,
she left the group. Shortly afterward the breeding female, Patricia, died, and
Paloma returned to the PBf group. There she reproduced successfully with the
same breeding male.
The other two subordinate females left their groups after they lost their
infants, and we have no further information regarding them. This outcome
suggests that the main reason for migration is competition with the breeding
female, even if this competition is not reflected in agonism levels. The likely costs
of remaining in the group without breeding opportunities are higher than the
possible costs of migrating. Data from other subordinate females from the same
population suggest that migrating females may eventually find a breeding
position in groups that have lost the breeding female, or groups that split and
form two new groups [Arruda et al., 2005].
In conclusion, in response to the three questions posed in this study, our
results show that the social dynamics of dominant and subordinate females were
different in monogamous groups because the dominant females and breeding
males spent more time on reciprocal grooming, and in at least two of the groups
maintained exclusive sexual interactions, suggesting a preferential relationship
between them in comparison with breeding males and subordinate females. We
also found that under field conditions, the subordinate females’ reproductive
inhibition appeared to be more behavioral than hormonal, since all monitored
subordinate females showed ovarian functioning over the course of the study. In
two groups (PBf and T) the subordinate females were able to reproduce, although
their infants did not survive. We identified three different reproductive strategies
used by subordinate female common marmosets living in wild monogamous
groups: 1) staying in the natal group as nonreproductive members for a period of
time and waiting for a more favorable opportunity to reproduce, 2) attempting to
reproduce as a second female and emigrating unsuccessfully, and 3) eventually
returning to the natal social group to occupy the breeding-female vacancy.
ACKNOWLEDGMENTS
We thank Herbert M. Santos, Maria Carla Lopes do Nascimento, and Patricia
Guilhermino Ledo for their help with the fecal collection and hormone assays. We
also thank the Brazilian Institute for the Environment and Renewable Resources
(IBAMA) for permission to conduct this research at Flona, Nisia Floresta, RN. We
Monogamy in Wild Common Marmosets / 49
are grateful to two anonymous referees for suggestions that improved the
manuscript. This work was supported by grants from CNPq to A. Araujo (464103/
00-2), M.B.C. Sousa (52.1186/1997, 305216/2003-5, and 470601/2003-1), and M.E.
Yamamoto (524409/96), and from CAPES to A.C.S.R. Albuquerque and A. Araujo
(864/91-11).
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strategia, dominantly, group, monogamous, common, subordinate, wild, hormonal, marmoset, callithrix, profiler, behavior, jacchus, female
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