American Journal of Primatology 72:122–128 (2010)
Sex Differences in Vocal Patterns in the Northern Muriqui
LUISA F. ARNEDO1Ã, FRANCISCO D.C. MENDES2, AND KAREN B. STRIER1
1Department of Anthropology, University of Wisconsin– Madison, Madison, Wisconsin
2Departamento de Psicologia, Universidade Cato´lica de Goia´s, Goiaˆnia, Brazil
We investigated whether sex differences in spatial dynamics correlate with rates of staccato and neigh
vocalizations in northern muriquis (Brachyteles hypoxanthus) at the Reserva Particular do Patrimo
Natural–Feliciano Miguel Abdala, Minas Gerais, Brazil. A total of 2,727 10 min focal subject samples
were collected on 32 adult females and 31 adult males between April 2007 and March 2008. Compared
with males, females spent a signiﬁcantly lower proportion of their time in proximity to other group
members and gave staccatos at signiﬁcantly higher rates while feeding, resting, and traveling.
Conversely, males emitted neigh vocalizations at signiﬁcantly higher rates than females when feeding
and resting only. Both sexes gave signiﬁcantly more staccatos when feeding than when they were
engaged in other activities, but their respective rates of neighs did not vary across activities. Both
females and males emitted staccato vocalizations at signiﬁcantly higher rates during times of the year
when preferred foods were scarce, but no seasonal differences in the rates of neigh vocalizations were
observed in either sex. Females and males showed a reduction in the number of neighbors following
staccato vocalizations and an increase in the number of neighbors following neigh vocalizations. Our
ﬁndings of sex differences in the rates of staccato and neigh vocalizations and the effects of these
vocalizations on interindividual spacing are consistent with sex differences in spatial dynamics, and
conﬁrm the role of vocal communication in mediating spatial associations in this species. Am. J.
Primatol. 72:122–128, 2010.
r 2009 Wiley-Liss, Inc.
Key words: northern muriqui; spatial dynamics; vocal communication; short-distance call;
other males [Fischer et al., 2004; Kitchen et al.,
2003], whereas females, emit ‘‘grunt’’ vocalizations,
Vocal communication is known to mediate the
which appears to facilitate afﬁliative interactions
spatial distribution of conspeciﬁcs by repelling or
with one another, at higher rates than males
attracting individuals according to social and ecolo-
[Cheney & Seyfarth, 2007; Cheney et al., 1995].
gical conditions [Boinski, 1996]. Proximity is neces-
Efforts to explain sex differences in primate
sary for afﬁliative interactions but can also increase
vocalizations have focused on the beneﬁts and
competition, and the costs and beneﬁts of increasing
costs to the caller [Wich & Nunn, 2002]. The higher
or decreasing the number of neighbors often varies
rates of loud, long-distance calls emitted by males
between sexes and between individuals [Altmann,
compared with females have been attributed to
1980]. Sex differences in interindividual spatial
the greater beneﬁts males gain by broadcasting
patterns might result in corresponding sex differ-
their position to facilitate group re-aggregation
ences in vocalization patterns.
Sex differences in vocal behavior often vary with
the functions of the calls [Rendall et al., 2004]. For
Contract grant sponsor: National Science Foundation Improve-
ment Dissertation Grant; Contract grant number: 0621788;
example, female Diana monkeys (Cercopithecus
Contract grant sponsors: Wenner-Gren Foundation Dissertation
diana) account for most of the vocal activity within
Fieldwork Grant; American Society of Primatologists Research
the social group, whereas male vocalizations are
restricted to the production of long-distance calls
ÃCorrespondence to: Luisa F. Arnedo, Department of Anthro-
that are thought to function mostly as predator-
pology, University of Wisconsin– Madison, 1180 Observatory
Drive, Madison, WI 53706. E-mail: firstname.lastname@example.org
speciﬁc alarm calls [Shultz et al., 2003; Zuberbu
Received 1 July 2009; revised 11 September 2009; revision
et al., 1997]. Similarly, males chacma baboons (Papio
accepted 1 October 2009
cynocephalus) produce loud ‘‘wahoo’’ calls during
dawn choruses, intergroup interactions, when chas-
Published online 2 November 2009 in Wiley InterScience
ing females, and in aggressive interactions with
r 2009 Wiley-Liss, Inc.
Vocal Behavior in Northern Muriquis / 123
[chimpanzees: Wrangham, 1977; spider monkeys,
unity and coordinate group movement because they
Ateles spp: Ramos-Fernandez, 2005; Spehar, 2006],
are often heard when animals are traveling and
maintaining territorial spacing to defend mates or
feeding, but the effects of these calls on spatial
defend resources needed by females [red howler
patterns have not been subjected to quantitative
monkeys, Alouatta seniculus: Sekulic, 1982; black
and white colobus, Colobus guereza: Oates et al.,
If staccatos function to increase interindividual
2000; pig-tailed langurs, Simias concolor: Tenaza,
distances, then we expected that the greater inter-
1989], and attracting mates [Orangutans, Pongo sp:
individual distances maintained by females com-
Mitani, 1985; Thomas’s langurs, Presbitys thomasi:
pared with males would be reﬂected in their higher
Steenbeek et al., 1999; Wich et al., 2002]. The costs of
rates of staccatos, and that this difference would be
increasing the number of neighbors while feeding or
greater when females experience higher levels of
of attracting predators may explain why females,
indirect competition, such as when they are feeding
which have higher energetic requirements and may
and at times of the year when preferred food sources
be more vulnerable to predation when pregnant or
are scarce. Conversely, if neighs function to reunite
lactating, tend to emit long-distance vocalizations at
conspeciﬁcs then the high levels of sociality main-
lower rates than males [Mitani, 1996].
tained by males should be reﬂected in their higher
Short-distance calls, by contrast, are usually less
rates of neighs compared with females, independent
conspicuous than long-distance vocalizations, and
of their activities or seasonal ﬂuctuations in the
are thought to play an important role in mediating
availability of preferred foods.
intragroup social interactions [Palombit et al., 1999;
Snowdon, 1997]. In some species, the higher rates
at which females emit short-distance vocaliza-
tions compared with males facilitate the initiation
of afﬁliative associations, especially between indi-
Study Site and Subjects
viduals with unequal hierarchical positions [e.g.,
Our study was conducted between April 1, 2007
and March 22, 2008 at the Reserva Particular do
Masataka, 1989; and grunts by chacma baboons:
Cheney et al., 1995]. In other species, however, short-
(RPPN-FMA, earlier known as the Estac-a˜o Biologica
distance vocalizations appear to increase the inter-
de Caratinga, 191500S, 411500N) in Minas Gerais,
individual distances among group members. For
Brazil. The study area consists of approximately
example, the higher rates of ‘‘huh’’ calls that adult
957 ha of low, semideciduous montane forest, mostly
female wedge-capped capuchins [Cebus nigrivittatus,
secondary, surrounded by pastures and plantations
Robinson, 1982] and white-faced capuchins [Cebus
[Strier et al., 2006]. The area is characterized by a
capucinus, Boinski & Campbell, 1996] give during
distinct rainy season from October to April, and a dry
foraging have been shown to increase spacing
season from May to September when preferred food
between conspeciﬁcs and reduce feeding competition.
resources are scarce [Strier, 1991].
We investigated the relationship between sex
We collected behavioral and vocal data from
differences in spatial dynamics and vocal behavior in
three of the four groups in the study population:
the northern muriqui (Brachyteles hypoxanthus), a
Nadir group (71 individuals), M2 group (48 indivi-
species in which females tend to avoid each other and
duals) and Jao
´ group (75 individuals). Members of
maintain greater interindividual distances, espe-
these groups were fully habituated and could be
cially while feeding, than philopatric males [Strier,
individually identiﬁed by their distinctive facial
1990; Strier et al., 2002]. Staccatos and neighs are
pigmentation, hair color, and other physical features.
two of the most common vocalizations within the
A subset of 32 females (10–11 per group),
vocal repertoire of northern muriquis [Ades &
including 7 subadults known to have recently
Mendes, 1997; Nishimura et al., 1988]. Staccatos
immigrated into these groups, and 25 long-term
have been deﬁned as short-distance contact calls,
resident adult females, were selected as focal subjects.
commonly produced during short-range exchanges
There were no signiﬁcant differences in the rates of
[Mendes, 1995]. Mendes and Ades  suggested
vocalizations between recent immigrant and long-
that staccatos could function to reduce competition
term resident females, so they have been combined in
by allowing callers to maintain or increase distances
this study. The long-term resident females were
among nearby listeners, but no previous studies have
selected based on the number of behavioral observa-
yet tested this hypothesis.
tions obtained during the ﬁrst 2 months of data
Contrary to staccatos, neighs have been classi-
collection, after conﬁrming that there were no
ﬁed as long-distance contact calls, mainly produced
signiﬁcant differences in the rates of vocalizations
during long-range exchanges when group members
between these females and those not included in the
are widely dispersed [Mendes & Ades, 2004; Strier,
sample. All 31 adult males present in the three
1999]. Nishimura et al.  suggested that neighs
groups at the beginning of this investigation were
are used by northern muriquis to maintain group
also included as focal subjects (10–11 per group).
Am. J. Primatol.
124 / Arnedo et al.
Systematic recordings were made using a
We tested our data set for normality using the
Marantz PMD660 digital recorder and Sennheiser
Shapiro–Wilk test in JMP 7.0.2 software. Because
ME66 shotgun microphone. The Nadir and M2
our data did not ﬁt a normal distribution, we used a
groups were sampled every month throughout the
Box-Cox Power transformation [Box & Cox, 1964;
12-month study period (April 2007 to March 2008),
Peltier et al., 1998] to permit the use of parametric
whereas the Jao
´ group was sampled every month for
6 months between August 2007 and January 2008.
Patterns of spatial associations for the focal
From 8 to 15 days were devoted to locating and
animals were calculated as the proportion of time
collecting data from members of each group depend-
that each individual spent in proximity (i.e., within
ing on whether two or three groups were being
5 m) to at least one independent associate during its
followed that month.
FSS [Strier et al., 2002]. We ran ANOVAs to assess
We collected data on social and vocal behavior on
differences in spatial associations between females
the focal subjects during on-the-minute instanta-
neous samples of 10 min duration [Altmann, 1974;
We also used ANOVAs to determine whether
Paterson, 2001; Possamai et al., 2007]. The daily
rates of staccato and neigh vocalizations differed by
sequence of focal subjects was chosen following a list
sex, activity, or time of the year. In these analyses,
of earlier established criteria for independence, such
we used the number of vocalizations per FSS as the
that no individual was sampled twice in the same
explanatory variable weighted by the FSS length
hour or more than three times on the same day, and
(8–10 min). Sex, activity, and time of the year were
no individual that interacted with the focal animal
entered as ﬁxed factors and individual identity was
was chosen for sampling within 30 min of the
entered as a random effect to account for repeated
interaction [Printes & Strier, 1999]. We attempted
observations of the same subjects and avoid pseudo-
to balance the number of focal subject samples (FSS)
replication. Post-hoc Tukey’s HSD tests were used to
across each of the 63 focal subjects bimonthly. Only
compare average rates of vocalizations between pairs
FSS of Z8 min of observations were included in the
of the three most common activities (feeding, travel-
data analyses, resulting in a total of 2,727 FSS
ing, and resting), and across 2-month periods during
during which focal subjects emitted 2,089 staccato
the study year.
and neigh vocalizations. Table 1 shows the average
To evaluate the effect of the vocalizations on
and standard deviation of FSS collected per indivi-
spatial associations, we calculated the difference in
dual bimonthly for each of the three study groups.
the total number of independent neighbors in
The activity of the focal subject and the
proximity to the focal subject before and after the
identities and activities of all neighbors within a
focal animal emitted a vocalization. To control for
5 m radius of the subject were recorded within the
the effect of vocalizations that could have been
ﬁrst 5 sec of each minute of the sample [Strier et al.,
emitted before the onset of the FSS, and also to
2002]. Activities were classiﬁed as resting, feeding,
allow enough time to observe the possible effect after
traveling, and social behavior, and neighbors in-
a vocalization occurred, we only included those FSS
cluded all adults, subadults, and juveniles traveling
in which the focal individual vocalized between the
independently from their mothers. All neigh and
second and seventh minutes of continuous sampling
staccato vocalizations produced by the focal subjects
in this analysis. To control for the effect of multiple
were recorded when they occurred during their FSS
vocalizations, and to maximize the chances of
and only those vocalizations were used in our
detecting the effects of the focal subject’s vocaliza-
tions on the neighbor’s response, we only used FSS
in which only one vocalization was emitted and in
which the focal subject did not change positions after
TABLE 1. Average Number of Focal Subject Samples
Consistent with previous studies, we found
signiﬁcant differences in the spatial relationships
of females vs. males (ANOVA: F 5 35.41, df 5 1,
Po0.0001). On an average, females spent only
72.2% of their time in proximity to at least
70.9 210 9.671.0 202 8.172.6 163
one independent neighbor, whereas males spent
56.372% of their time in proximity to other
conspeciﬁcs. The average number of neighbors
´ group members were sampled only during half of the sample period
was signiﬁcantly lower when female subjects were
(August 2007 to January 2008), resulting in a smaller number of FSS for
this group. No group differences were found in any of our analyses.
feeding (0.3270.01 neighbors) than when they were
Am. J. Primatol.
Vocal Behavior in Northern Muriquis / 125
resting (0.4770.02 neighbors) or traveling (0.417
df 5 1, Po0.005) and resting (ANOVA: F 5 11.56,
0.02 neighbors; ANOVA: F 5 14.2, df 5 2, Po0.0001),
df 5 1, Po0.005), but not when traveling (ANOVA:
whereas there were no differences in the number of
F 5 0.6, df 5 1, P 5 0.136). Males emitted neighs
at signiﬁcantly higher rates when they were
(0.5470.02 neighbors), resting (0.5070.02 neigh-
feeding (0.1870.02 calls/FSS) and resting (0.207
bors), or traveling (0.5170.02 neighbors; ANOVA:
F 5 2.95, df 5 2, P 5 0.074).
0.02 calls/FSS, ANOVA: F 5 6.54, df 5 2, Po0.005),
Females emitted staccato vocalizations at sig-
but females showed no differences in their rates of
niﬁcantly higher rates (0.6370.04 calls/FSS) com-
neighs between activities (Fig. 1B).
pared with males (0.3770.04 calls/FSS; ANOVA:
Both sexes also showed seasonal variation in the
F 5 19.11, df 5 1, Po0.005), and these sex differ-
rates of staccato vocalizations (females ANOVA:
ences were consistent across all three major activities
F 5 3.68, df 5 5, Po0.05; males ANOVA F 5 3.78,
(ANOVA: feeding F 5 27.03, df 5 1, Po0.0001; rest-
df 5 5, Po0.05). Although females and males emitted
ing F 5 22.51, df 5 1, Po0.0001; traveling F 5 16.8,
signiﬁcantly higher rates of staccatos when feeding
df 5 1, Po0.0001). Both females and males showed
between June and September, with the exception of
signiﬁcantly higher rates of staccatos when feeding
April–May, this difference was more pronounced in
(females 0.4470.02 calls/FSS; males 0.2670.2 calls/
females than in males (Fig. 2). Neither females nor
FSS) than when resting (females 0.2670.02 calls/
males showed seasonal variation in the bimonthly
FSS; males 0.1570.2 calls/FSS) or traveling (females
rates of neigh vocalizations (females ANOVA:
0.2470.02 calls/FSS, ANOVA: F 5 21.13, df 5 2,
F 5 1.76, df 5 5, P 5 0.081; males ANOVA: F 5 1.83,
Po0.0001; males 0.1270.2 calls/FSS, ANOVA:
df 5 5, P 5 0.184).
F 5 13.68, df 5 2, Po0.0001; Fig. 1A).
The average number of neighbors in proximity
In contrast to the female-biased pattern for
to the focal animal consistently decreased following
staccatos, male muriquis emitted neigh vocalizations
staccato vocalizations and increased after neigh
at signiﬁcantly higher rates (0.3470.029 calls/FSS)
vocalizations (Fig. 3). Females and males exhibited
than females (0.1970.027 calls/FSS; ANOVA: F 5 12.28,
similar decreases in the number of neighbors
df 5 1, Po0.005). These sex differences were signiﬁ-
following staccatos (females: À0.6570.04 neighbors,
cant when animals were feeding (ANOVA: F 5 6.73,
males: À0.6170.06 neighbors; ANOVA: F 5 0.23,
df 5 1, P 5 0.62) and similar increases following neighs
(females: 0.4970.07 neighbors, males: 0.5470.06
neighbors; ANOVA F 5 0.29, df 5 1, P 5 0.58).
Sex differences in the vocalization patterns of
northern muriquis appear to correspond to sex
differences in their spatial dynamics. Similar to
previous studies on another group in this population
[Strier, 1990], we found that female muriquis in our
study groups spent a signiﬁcantly lower proportion of
their time in proximity with other group members
than males. Staccato vocalizations were associated
with a similar reduction in the average number of
neighbors of female and male callers, and the higher
rates of these vocalizations by females were consistent
with the greater interindividual distances they main-
tained compared with males. Neighs, by contrast, were
associated with an increase in the average number of
neighbors of both female and male callers, and were
emitted at higher rates by males than females,
consistent with the higher proportion of time males
spent in proximity to other group members.
The higher proportion of time females spent
feeding compared with males, and the higher
proportion of feeding time females devoted to higher
Fig. 1. Rates of (A) staccato and (B) neigh vocalizations by sex
quality foods [Strier, 1987, 1991] suggest that female
and activity. The signiﬁcance levels of Post-hoc Tukey’s HSD
northern muriquis, like many other female primates,
pair wise comparisons are indicated by letters. Bars not
experience higher energetic demands than males.
connected by the same letter are signiﬁcantly different
The greater distances females maintain with close
Am. J. Primatol.
126 / Arnedo et al.
Fig. 2. Seasonal variation in rates of staccato vocalizations when feeding. The signiﬁcance levels of Post-hoc Tukey’s HSD pair wise
comparisons are indicated by letters. Capital letters show the comparisons across months for females, whereas small letters show the
monthly comparisons for males. Bars not connected by the same letter are signiﬁcantly different (Po0.005).
Fig. 3. Effects of vocalizations on the number of neighbors. A positive difference indicates an average increase in number of neighbors,
whereas a negative difference indicates an average reduction. Individuals were ranked separately from the smallest to the greatest
change in neighbor numbers for each vocalization.
neighbors while feeding than while resting also
emitted rates of staccatos as low as those of males
implies that females actively reduce direct competi-
was during April–May, the period of peak production
tion by avoiding each other [Strier, 1990].
of inﬂorescences of Mabea ﬁstulifera, which produces
The higher rates of staccatos emitted by females
conspicuous amounts of nectar and is distributed in
while feeding than while resting and traveling, and
high densities in the study area [Ferrari & Strier,
when preferred foods are scarce, suggests that the
1992]. Contrary to what has been proposed to be the
function of staccato vocalizations in northern mur-
function of other short-distance calls in several
iquis could be linked to changes in spatial relation-
primate species [Snowdon, 1988, 1997] staccatos do
ships associated with avoiding competition over
not appear to facilitate associations among muriqui
access to food. Indeed, the only time when females
Am. J. Primatol.
Vocal Behavior in Northern Muriquis / 127
In contrast to staccatos, the higher rates of
neighs emitted by males compared with females
suggest that neigh vocalizations might permit males
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