American Journal of Primatology 70:301–305 (2008)
BRIEF REPORT
Mother–Offspring Associations in Northern Muriquis, Brachyteles hypoxanthus
KARYNNA TOLENTINO1, JAMES J. ROPER1, FERNANDO C. PASSOS1, AND KAREN B. STRIER2

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
INTRODUCTION
Maternal care is of fundamental importance for
the survival and socialization of dependent infants
[Altmann, 1980; Harlow et al., 1963; Nicolson,
1987,1991]. After weaning, however, mother–off-
spring relationships vary greatly depending on
whether sons or daughters remain in their natal
groups or disperse, and on whether they live in
hierarchical or egalitarian societies. For example, in
the matrifocal, hierarchical societies of macaques
(Macaca spp.) and baboons (Papio spp.), daughters
benefit from maternal support throughout their
lives, and maternal support can be instrumental as
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
et al., 1997]. Among patrifocal bonobos (Pan panis-
cus), maternal support is critical to the establish-
ment of their sons’ positions in the adult male
hierarchy [Furuichi, 1997]. Little is known about
maternal investment in older offspring in patrifocal,
egalitarian societies.
We examined mother–offspring associations in
wild northern muriquis (Brachyteles hypoxanthus),
in which male philopatry and egalitarian relation-
ships among and between adult males and females
permit us to examine alternative predictions about
the value of extended maternal investment [Printes
& Strier, 1999; Strier, 1992; Strier & Ziegler, 2000].
Muriqui mothers invest heavily in dependent infants
of both sexes [Odalia-Rı´moli, 1998; Strier, 1996], but
whether their associations favor older sons rather
than daughters is not known. Male philopatry
provides opportunities for extended mother–son
interactions, which might result in stronger associa-
tions with sons than daughters. Alternatively,
extended maternal investment in offspring may be
of limited, if any, value in their egalitarian society,
resulting in indiscriminant associations between
mothers and older offspring of either sex.
Published online 1 October 2007 in Wiley InterScience (www.
interscience.wiley.com).
DOI 10.1002/ajp.20488
Received 7 June 2007; revised 20 August 2007; revision accepted
29 August 2007
Contract grant sponsors: Margot Marsh Biodiversity Founda-
tion; Liz Claiborne and Art Ortenberg Foundation; Graduate
School of the University of Wisconsin-Madison; CAPES scholar-
ship; Contract grant sponsor: CNPq; Contract grant number:
Process 306194/2006-6.

Correspondence to: Karen B. Strier, Department of Anthro-
pology, University of Wisconsin-Madison, 1180 Observatory
Drive, Madison, WI 53706. E-mail: kbstrier@wisc.edu
r 2007 Wiley-Liss, Inc.

METHODS
This study was conducted from August 2003—to
May 2004 at the RPPN-Feliciano Miguel Abdala, in
Minais Gerais, Brazil (previously known as the
Estac- a˜o Biolo´gica de Caratinga; 1914205000 S;
4114903000 W). Our subjects were members of the
Mata˜o group, one of the four mixed-sex groups in this
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’’
(o2 years) were born between May 2002 and
September 2003; ‘‘juveniles’’ (2–7 years) were born
between 1997 and 2001 and were not yet sexually
active; and ‘‘adults’’ (47 years in this study) were all
observed in copulations that ended with ejaculate
before the onset of this study period. We selected 10
adult females as our focal subjects, each of which had
2–6 surviving offspring in the group (Table I).
Systematic behavioral data were collected from
07:00–18:00h using a modified ‘‘focal-animal’’ method
[Altmann, 1974], in which all nearest neighbors within
5m of the focal female were noted at 1-min intervals
for up to 10 consecutive minutes. Efforts were made to
balance the distribution of observations of each female
over time of day each month, following previously
established protocol [Odalia-Rı´moli, 1998; Printes &
Strier, 1999; Strier et al., 2002].
We examined the dyadic associations between
each focal mother and group member. All associated
individuals were distinguished by age–sex class and
offspring/non-offspring relationship. Unless other-
wise noted, we did not compare older and younger
individuals in the same age–sex class. We used
Mann–Whitney U-tests to determine whether
mothers spent more of their time associating with
sons than daughters. Similarly, we tested whether
associations of focal females were more frequent
with offspring than non-offspring for each age–sex
class with the log-likelihood ratio (G statistic). All
comparisons were one-tailed and considered signifi-
cant when Pr0.05, or Pr0.025 (Bonferroni adjust-
ment for multiple comparisons).
RESULTS
A total of 13,853min of dyadic associations were
recorded during the 12,190min of observation owing
to associations with 41 individual. The 10 focal
females spent from 841–1,940min in association
with one or more other group members (Table I).
Infants accounted for an average of 46.0725.3%
(median5 55.3%) of the females’ total association
time, juveniles for 20.6719.2% (median5 10.9%),
and adults for 33.478.1% (median5 33.4%).
Although the sample size was small for statis-
tical analysis, mothers spent similar amounts of time
in association with their infant sons (mean7SD,
64.2711.1%, median5 71.2%) and daughters
(66.871.8%, median5 66.8%; N15 5, N25 2,
U5 4.0, P40.05). All mothers clearly spent more
time associating with their own infant offspring
(91.973.3%, median5 91.0%) than with other in-
fants of the same sex. Infant sons were slightly less
preferred (87.9–91.9%) than daughters (94.2 and
98.0%) relative to time spent with all male and
female infants (N15 5, N25 2, U5 10, P5 0.053).
The only grandmother (BS) present was never
observed in association with her grandson, and
associated with her granddaughter for only 9 of the
105min she spent with female infants.
TABLE I. Focal Subjects, Their Offspring, and Sample Sizes
Infantsa Juvenilesa Adultsa
Total minutes
observed
Total association
minutesbFocal F M F M F M N offspring
BSc 1d 1 2 1 5 1,219 1,907
CH 1 2 1 4 1,311 1,940
DD 1d 1 2 4 1,338 1,068
FE 1 1 1 3 1,167 1,324
HE 2 1 3 1,217 841
IZ 1 1 1 1 4 1,220 1,719
JU 1 1 2 1,197 1,470
NY 1 1 4 6 1,151 1,503
PL 1 1 1 3 1,099 970
TZ 2 2 4 1,271 1,111
Total 2 5 6 8 3 14 38 12,190 13,853
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.
302 / Tolentino et al.

Mothers spent an average of 12.6714.3% (med-
ian5 6.2%) of their time with juvenile sons, and
2.371.4% with juvenile daughters (median5 2.3%).
Although this difference seems large and as pre-
dicted, the comparison is not significant (N158,
N256, U5 15, P40.05) due to the variation in
mother–juvenile son associations resulting from
three mothers that were not also caring for infants
and that spent from 23 to 40% of their time with their
youngest sons. The range of time spent with other
juvenile sons (0.1–8.2%, N55) encompassed that
spent with all juvenile daughters (0.6–4.4%, N56).
Comparing juvenile offspring versus non-off-
spring, mothers spent more time in association with
their sons (49.2733.1%, median5 42.4%, N5 8)
than their daughters (34.7727.7%, median5 24.9%,
N5 6; G5 6.65, df5 1, Po0.02). However, mothers
also favored some juvenile non-offspring as well, and
there were no consistent biases in favor of juvenile
sons when we examined all possible dyadic associa-
tions with juvenile males (N5 90) and juvenile
females (N5 110) separately. Twenty-one associa-
tions with juvenile males (23.3%) and 33 associations
with juvenile females (30%) occurred more often
than expected by chance. Six of the eight (75%)
mother–son dyads (including the three mothers
without infants) and four of the six (67%) mother–-
daughter dyads associated more often than expected
(Fig. 1A). Four of the five mothers with two juvenile
offspring spent more time associating with the
younger regardless of the offspring’s sex. Both of
the two mothers that had previously (and atypically)
exchanged infants [Martins et al., 2007] spent more
time than expected with their adopted juvenile
offspring, but only one also spent more time than
expected with her biological son.
Mothers spent a small percentage of their time
in association with their adult sons (range5 0–2.8%)
and adult daughters (0.1–1.4%; N15 8, N25 3,
U5 22.5, P40.05). However, the 10 focal females
associated more than expected with adult females
(73.1715.4%, median5 80.8%) than with adult
males (26.9715.3%, median5 19.2%; G5 195.1,
df5 1, Po0.02), and all associated more than
expected with at least some adult non-offspring. Six
of the 14 mother–adult son dyads were among the 56
(of 200 possible) dyadic associations with adult males
that occurred more often than expected, and one of
the three mother–adult daughter dyads was among
the 97 (of 250 possible) dyadic associations with adult
females that occurred more often than expected (Fig.
1B). All three mothers with more than one adult son
spent more time associating with the youngest.
DISCUSSION
The strength of associations between muriqui
mothers and infant offspring of both sexes is
consistent with previous studies of this group
[Odalia-Rı´moli, 1998], and with the high infant
survivorship attributed to maternal care [Strier,
1996]. Associations between mothers and their older
offspring were more variable. Mothers did not spend
more time in association with juvenile sons than
juvenile daughters, but they did associate more with
juvenile sons than daughters relative to their
associations with non-offspring in the same age–sex
class as their own offspring. They also associated
preferentially with adult females over adult males,
and with adults males that were not their own
offspring. However, the mothers showed preferences
for particular juveniles and adults of both sexes. This
variation may be attributed to factors including
individual differences in initiating or avoiding
associations, or may be incidental and result from
mutual attractions to a third individual. Both these
effects have been observed in the association pat-
terns of adult males in this muriqui group [Strier
et al., 2002]. Moreover, copulations between muriqui
mothers and their adult sons are extremely rare
[Strier, 1997], and both mothers and adult males
that copulated during the study period may have
associated more with unrelated individuals as poten-
tial mates [Possamai et al., 2007].
The absence of maternal association biases in
favor of older sons implies that despite the opportu-
nities male philopatry provides, extended maternal–-
son associations may have minimal, if any, value in
this egalitarian society. In contrast to bonobos,
muriqui males do not compete agonistically for rank
or access to mates [Strier, 1992], and therefore
probably do not benefit from maternal support like
bonobo males [Furuichi, 1997].
The tendency of mothers to spend more time
associating with the youngest of juvenile offspring
regardless of sex suggests an ontogeny of mother–off-
spring relationships, which are severed when daugh-
ters disperse, and mediated by the sexual and
reproductive activities of both mothers and their
philopatric offspring [MacKinnon, 2007]. Strong
maternal associations with older juvenile daughters
did not prevent them from subsequently dispersing.
Moreover, one mother with adult daughters in the
group spent less time associating with them, and
more time with other adult females than expected by
chance, suggesting that factors other than maternal
kinship influence the associations of female mur-
iquis. To tease apart other maternal association
preferences will require a further study of paternal
as well as maternal relatedness among all individuals
in the group, and of the ways in which current
associations and other forms of maternal investment
may affect fitness.
ACKNOWLEDGMENTS
We thank the Brazilian government for permis-
sion to conduct research in Brazil, E. Veado for
Am. J. Primatol.
Mother–Offspring Associations / 303

logistical support, the Abdalla family for their
collaboration and permission to work in their forest,
and J. Gomes, F. Mendes, J. Rı´moli, A. O. Rı´moli, F.
Neri, P. Coutinho, A. Carvalho, L. Oliveira, C.
Nogueria, S. Neto, W. Teixeira, R. Printes, M.
Maciel, C. Costa, A. Oliva, L. Dib, D. Carvalho,
N. Bejar, L.G. Dias, W. P. Martins, V. O. Guimara˜es,
J. C. da Silva, C. B. Possamai, R. C. Romanini, F. P.
Paim, M. F. Iurck, and V. Souza for their contribu-
tions to long-term demographic data. Financial
support was provided by grants from the Margot
Marsh Biodiversity Foundation, the Liz Claiborne
and Art Ortenberg Foundation, and the Graduate
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’
comments.
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Percentages of time in association for two of the mother–adult
son dyads (TZ–TH and NY–NI) were similar to that of a
mother–adult daughter dyad (DD–DB), but the male dyads did
not differ from expectations because there were fewer adult
males than adult females (N5 20 vs. 25) available as potential
associates. Note that one of the mother–adult son dyads (NY–NE)
was never observed to associate during this study.
Mother–offspring dyads that associated at greater frequencies
than expected from the number of individuals in the offspring’s
age–sex class.
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