American Journal of Primatology 70:301–305 (2008)
Mother–Offspring Associations in Northern Muriquis, Brachyteles hypoxanthus
KARYNNA TOLENTINO1, JAMES J. ROPER1, FERNANDO C. PASSOS1, AND KAREN B. STRIER2Ã
1Department of Zoology, Graduate Program in Zoology, Universidade Federal do Parana´, Curitiba, Parana´ Brazil
2Department of Anthropology, University of Wisconsin-Madison, Madison, Wisconsin
Maternal care of offspring is ubiquitous among primates, but its duration varies across species due to
factors such as dispersal patterns and social dynamics, which inﬂuence opportunities for and potential
beneﬁts of maternal investment in older offspring, respectively. We examined mother-offspring
associations in wild northern muriquis (Brachyteles hypoxanthus), in which males are philopatric,
females typically disperse before puberty, and social relationships among and between males and
females are egalitarian. Associations were systematically recorded between ten mothers, each with
two–six offspring in the study group, and all group members from August 2003–May 2004 at the RPPN-
Feliciano Miguel Abdala in Minas Gerais, Brazil. Infants of both sexes received similarly high
percentages of their mothers’ association time. Mothers without infants also maintained strong
associations with their youngest juvenile sons. Mothers did not spend consistently more time
associating with either juvenile or adult sons than daughters. Our ﬁnding of non-preferential
associations between muriqui mothers and their older male offspring suggests that extended maternal
investment in offspring may be of minimal value in their egalitarian society compared with its value for
species living in hierarchical societies. Am. J. Primatol. 70:301–305, 2008.
c 2007 Wiley-Liss, Inc.
Key words: Northern muriquis; Brachyteles hypoxanthus; mother–offspring associations;
maternal support; dispersal; egalitarian society
permit us to examine alternative predictions about
the value of extended maternal investment [Printes
Maternal care is of fundamental importance for
& Strier, 1999; Strier, 1992; Strier & Ziegler, 2000].
the survival and socialization of dependent infants
Muriqui mothers invest heavily in dependent infants
[Altmann, 1980; Harlow et al., 1963; Nicolson,
of both sexes [Odalia-Rı´moli, 1998; Strier, 1996], but
1987,1991]. After weaning, however, mother–off-
whether their associations favor older sons rather
spring relationships vary greatly depending on
than daughters is not known. Male philopatry
whether sons or daughters remain in their natal
provides opportunities for extended mother–son
groups or disperse, and on whether they live in
interactions, which might result in stronger associa-
hierarchical or egalitarian societies. For example, in
tions with sons than daughters. Alternatively,
the matrifocal, hierarchical societies of macaques
extended maternal investment in offspring may be
(Macaca spp.) and baboons (Papio spp.), daughters
of limited, if any, value in their egalitarian society,
beneﬁt from maternal support throughout their
resulting in indiscriminant associations between
lives, and maternal support can be instrumental as
mothers and older offspring of either sex.
maturing daughters establish their position in the
adult hierarchy [Kawai, 1965; Walters, 1980]. In
patrifocal societies, mothers maintain lifelong asso-
ciations with their sons, but only with those
daughters that remain in their natal groups [Pusey
Contract grant sponsors: Margot Marsh Biodiversity Founda-
tion; Liz Claiborne and Art Ortenberg Foundation; Graduate
et al., 1997]. Among patrifocal bonobos (Pan panis-
School of the University of Wisconsin-Madison; CAPES scholar-
cus), maternal support is critical to the establish-
ship; Contract grant sponsor: CNPq; Contract grant number:
ment of their sons’ positions in the adult male
hierarchy [Furuichi, 1997]. Little is known about
ÃCorrespondence to: Karen B. Strier, Department of Anthro-
maternal investment in older offspring in patrifocal,
pology, University of Wisconsin-Madison, 1180 Observatory
Drive, Madison, WI 53706. E-mail: email@example.com
Received 7 June 2007; revised 20 August 2007; revision accepted
We examined mother–offspring associations in
29 August 2007
wild northern muriquis (Brachyteles hypoxanthus),
in which male philopatry and egalitarian relation-
Published online 1 October 2007 in Wiley InterScience (www.
ships among and between adult males and females
r 2007 Wiley-Liss, Inc.
302 / Tolentino et al.
mothers spent more of their time associating with
sons than daughters. Similarly, we tested whether
This study was conducted from August 2003—to
associations of focal females were more frequent
May 2004 at the RPPN-Feliciano Miguel Abdala, in
with offspring than non-offspring for each age–sex
Minais Gerais, Brazil (previously known as the
class with the log-likelihood ratio (G statistic). All
Estac-a˜o Biolo´gica de Caratinga; 1914205000
comparisons were one-tailed and considered signiﬁ-
4114903000 W). Our subjects were members of the
cant when Pr0.05, or Pr0.025 (Bonferroni adjust-
˜o group, one of the four mixed-sex groups in this
ment for multiple comparisons).
forest and studied since 1982 [Strier et al., 2006]. All
individuals were fully habituated to observers and
identiﬁable by their natural markings. During this
study period, the group included 80 individuals,
which we divided into three age classes: ‘‘infants’’
A total of 13,853 min of dyadic associations were
(o2 years) were born between May 2002 and
recorded during the 12,190 min of observation owing
September 2003; ‘‘juveniles’’ (2–7 years) were born
to associations with 41 individual. The 10 focal
between 1997 and 2001 and were not yet sexually
females spent from 841–1,940 min in association
active; and ‘‘adults’’ (47 years in this study) were all
with one or more other group members (Table I).
observed in copulations that ended with ejaculate
Infants accounted for an average of 46.0725.3%
before the onset of this study period. We selected 10
(median 5 55.3%) of the females’ total association
adult females as our focal subjects, each of which had
time, juveniles for 20.6719.2% (median 5 10.9%),
2–6 surviving offspring in the group (Table I).
and adults for 33.478.1% (median 5 33.4%).
Systematic behavioral data were collected from
Although the sample size was small for statis-
07:00–18:00 h using a modiﬁed ‘‘focal-animal’’ method
tical analysis, mothers spent similar amounts of time
[Altmann, 1974], in which all nearest neighbors within
in association with their infant sons (mean7SD,
5 m of the focal female were noted at 1-min intervals
median 5 71.2%)
for up to 10 consecutive minutes. Efforts were made to
median 5 66.8%;
N1 5 5,
N2 5 2,
balance the distribution of observations of each female
U 5 4.0, P40.05). All mothers clearly spent more
over time of day each month, following previously
time associating with their own infant offspring
established protocol [Odalia-Rı´moli, 1998; Printes &
(91.973.3%, median 5 91.0%) than with other in-
Strier, 1999; Strier et al., 2002].
fants of the same sex. Infant sons were slightly less
We examined the dyadic associations between
preferred (87.9–91.9%) than daughters (94.2 and
each focal mother and group member. All associated
98.0%) relative to time spent with all male and
individuals were distinguished by age–sex class and
female infants (N1 5 5, N2 5 2, U 5 10, P 5 0.053).
offspring/non-offspring relationship. Unless other-
The only grandmother (BS) present was never
wise noted, we did not compare older and younger
observed in association with her grandson, and
individuals in the same age–sex class. We used
associated with her granddaughter for only 9 of the
105 min she spent with female infants.
TABLE I. Focal Subjects, Their Offspring, and Sample Sizes
aThere were 14 infants (four females, 10 males), 20 juveniles (11 females, nine males), and 46 adults (26 females, 20 males) in the group during this study.
bAssociation minutes are based on dyadic associations, and exceed the total minutes of systematic observations because of simultaneous dyadic associations.
Analyses compare both percentage of observation time, and time spent with associates in the same age-sex classes.
cBS also had one infant grandson and one infant granddaughter in the group during the study period.
dBS and DD exchanged infants of opposite sexes during their ﬁrst week of life [Martins et al., 2007], and continued to nurse and carry their adopted infants,
which are treated as their offspring except when otherwise noted.
Am. J. Primatol.
Mother–Offspring Associations / 303
Mothers spent an average of 12.6714.3% (med-
[Odalia-Rı´moli, 1998], and with the high infant
ian 5 6.2%) of their time with juvenile sons, and
survivorship attributed to maternal care [Strier,
2.371.4% with juvenile daughters (median 5 2.3%).
1996]. Associations between mothers and their older
Although this difference seems large and as pre-
offspring were more variable. Mothers did not spend
dicted, the comparison is not signiﬁcant (N1 5 8,
more time in association with juvenile sons than
N2 5 6, U 5 15, P40.05) due to the variation in
juvenile daughters, but they did associate more with
mother–juvenile son associations resulting from
juvenile sons than daughters relative to their
three mothers that were not also caring for infants
associations with non-offspring in the same age–sex
and that spent from 23 to 40% of their time with their
class as their own offspring. They also associated
youngest sons. The range of time spent with other
preferentially with adult females over adult males,
juvenile sons (0.1–8.2%, N 5 5) encompassed that
and with adults males that were not their own
spent with all juvenile daughters (0.6–4.4%, N 5 6).
offspring. However, the mothers showed preferences
Comparing juvenile offspring versus non-off-
for particular juveniles and adults of both sexes. This
spring, mothers spent more time in association with
variation may be attributed to factors including
their sons (49.2733.1%, median 5 42.4%, N 5 8)
individual differences in initiating or avoiding
than their daughters (34.7727.7%, median 5 24.9%,
associations, or may be incidental and result from
N 5 6; G 5 6.65, df 5 1, Po0.02). However, mothers
mutual attractions to a third individual. Both these
also favored some juvenile non-offspring as well, and
effects have been observed in the association pat-
there were no consistent biases in favor of juvenile
terns of adult males in this muriqui group [Strier
sons when we examined all possible dyadic associa-
et al., 2002]. Moreover, copulations between muriqui
tions with juvenile males (N 5 90) and juvenile
mothers and their adult sons are extremely rare
females (N 5 110) separately. Twenty-one associa-
[Strier, 1997], and both mothers and adult males
tions with juvenile males (23.3%) and 33 associations
that copulated during the study period may have
with juvenile females (30%) occurred more often
associated more with unrelated individuals as poten-
than expected by chance. Six of the eight (75%)
tial mates [Possamai et al., 2007].
mother–son dyads (including the three mothers
The absence of maternal association biases in
without infants) and four of the six (67%) mother–-
favor of older sons implies that despite the opportu-
daughter dyads associated more often than expected
nities male philopatry provides, extended maternal–-
(Fig. 1A). Four of the ﬁve mothers with two juvenile
son associations may have minimal, if any, value in
offspring spent more time associating with the
this egalitarian society. In contrast to bonobos,
younger regardless of the offspring’s sex. Both of
muriqui males do not compete agonistically for rank
the two mothers that had previously (and atypically)
or access to mates [Strier, 1992], and therefore
exchanged infants [Martins et al., 2007] spent more
probably do not beneﬁt from maternal support like
time than expected with their adopted juvenile
bonobo males [Furuichi, 1997].
offspring, but only one also spent more time than
The tendency of mothers to spend more time
expected with her biological son.
associating with the youngest of juvenile offspring
Mothers spent a small percentage of their time
regardless of sex suggests an ontogeny of mother–off-
in association with their adult sons (range 5 0–2.8%)
spring relationships, which are severed when daugh-
and adult daughters (0.1–1.4%; N1 5 8, N2 5 3,
ters disperse, and mediated by the sexual and
U 5 22.5, P40.05). However, the 10 focal females
reproductive activities of both mothers and their
associated more than expected with adult females
philopatric offspring [MacKinnon, 2007]. Strong
(73.1715.4%, median 5 80.8%) than with adult
maternal associations with older juvenile daughters
(26.9715.3%, median 5 19.2%; G 5 195.1,
did not prevent them from subsequently dispersing.
df 5 1, Po0.02), and all associated more than
Moreover, one mother with adult daughters in the
expected with at least some adult non-offspring. Six
group spent less time associating with them, and
of the 14 mother–adult son dyads were among the 56
more time with other adult females than expected by
(of 200 possible) dyadic associations with adult males
chance, suggesting that factors other than maternal
that occurred more often than expected, and one of
kinship inﬂuence the associations of female mur-
the three mother–adult daughter dyads was among
iquis. To tease apart other maternal association
the 97 (of 250 possible) dyadic associations with adult
preferences will require a further study of paternal
females that occurred more often than expected (Fig.
as well as maternal relatedness among all individuals
1B). All three mothers with more than one adult son
in the group, and of the ways in which current
spent more time associating with the youngest.
associations and other forms of maternal investment
may affect ﬁtness.
The strength of associations between muriqui
mothers and infant offspring of both sexes is
We thank the Brazilian government for permis-
consistent with previous studies of this group
sion to conduct research in Brazil, E. Veado for
Am. J. Primatol.
304 / Tolentino et al.
School of the University of Wisconsin-Madison to
KBS, a CAPES scholarship to KT, and CNPq
for a research grant to FCP (Process 306194/2006-
6). We also appreciate the anonymous reviewers’
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