Intra-Community Coalitionary Lethal Attack of an Adult Male Southern Muriqui (Brachyteles arachnoides)

American Journal of Primatology 71:860–867 (2009)
RESEARCH ARTICLE
Intra-Community Coalitionary Lethal Attack of an Adult Male Southern Muriqui
(Brachyteles arachnoides)
M.G. TALEBI1,2Ã, R. BELTRA
˜ O-MENDES 2,3, AND P.C. LEE4
1Biological Sciences Faculty, Federal University of Sa˜o Paulo, Diadema, Estado de Sa˜o Paulo, Brazil
2Pro´-Muriqui Association, Behavioral Biology and Conservation, Sa˜o Paulo, Sa˜o Paulo, Brazil
3Department of Conservation & Ecology, Federal University of Sergipe, Sa˜o Cristova˜o, Sergipe, Brazil
4Department of Psychology, University of Stirling, Stirling, Scotland
We report on the first evidence of intra-community coalitionary lethal aggression in muriquis
(Brachyteles). The event occurred in southern muriquis (Brachyteles arachnoides) during a long-term
study (415 years) of two social groups inhabiting mostly pristine Atlantic forest habitat in the Parque
Estadual Carlos Botelho, southern Sa
˜o Paulo State, Brazil. The attack took place deep in the core area
of the Group Caete
ˆ home range. Tense agonistic behaviors and vocalizations preceded the lethal
coalitionary attack, and the tension increased over a 36–48 hr period. One adult female and two
unidentified individuals also took part in a coalition led by six adult males. The members of the coalition
collectively approached, embraced, immobilized and repeatedly bit the entire body of an adult male,
resulting in severe bleeding injuries and the victim’s death in less than 1 hr after the attack
commenced. Combined ecological, behavioral and spatial data related to the event indicate that this was
an intra-community attack and suggest social tensions related to mating competition as the proximate
trigger of the coalitionary killing. The attack resembled those reported for chimpanzees, with clear
numeric superiority and a low risk of injury to aggressors, resulting in the death of a lone conspecific
victim. This observation (n 5 1) is suggestive of a capacity for escalated aggression in muriquis and
reinforces arguments for the potential adaptive significance of intra-community aggression in male
philopatric societies, as reported for spider monkeys and chimpanzees. These characteristics challenge
the view of the muriquis as a peaceful primate and support the general hypothesis that imbalances of
power contribute to intra-specific killing in primates, such as chimpanzees and humans. Am. J.
Primatol. 71:860–867, 2009.
r 2009 Wiley-Liss, Inc.
Key words: aggression; coalitions; male–male competition; muriquis; B. arachnoides
INTRODUCTION
dynamics, male philopatry, female dispersal and high
levels of both male–male cooperation and high levels
Fatal wounding during contests between adult
of male–male competition. In chimpanzees, disputes
individuals, especially males, is widespread in mam-
for
food,
females
and
fertilizations
[Wrangham,
mals. Episodes of intra-specific killing have been
1987] have repeatedly resulted in coalitionary lethal
reported for 132 mammal species in nine genera
attacks [Fawcett & Muhumuza, 2000; Watts, 2004;
[Byers, 1997; Clutton-Brock et al., 1982]. Coalition-
ary lethal attacks involving several individuals are,
however, relatively rare, and are known from social
Contract grant sponsor: CNPq, Brazilian National Research
carnivores [Mech, 1994] and some primate taxa:
Council; Contract grant number: 20025699-8; Contract grant
sponsors: WWF-IIE, Support for postgraduate studies; Conser-
humans, chimpanzees, [Boesch et al., 2007; Watts,
vac-a˜o International (Brazil); ATBC Clifford Evans Grant;
2004; Wrangham, 1999], gorillas, red colobus, capu-
Margot Marsh Biodiversity Foundation; Primate Action Fund
of Conservation International; MetroParks Zoo Cleveland, Idea
chins [Grous-Louis et al., 2004] and spider monkeys
Wild, Conservation Food and Health Foundation (USA);
[Campbell, 2006; Valero et al., 2006]. Intra-specific
Manfred Hermsen Stiftung Foundation (Germany); Fauna &
lethal coalitionary aggression has been related to
Flora International, DEFRA and Bromley Trust (UK).
both inter-community and intra-community compe-
ÃCorrespondence to: M. G. Talebi, Rua Luis Gois 1902 apto 73,
tition and though a number of events have been
Mirandopolis, Sa
˜o Paulo, CEP 04043-200, Brazil.
E-mail: talebi@promuriqui.org.br, talebi@pq.cnpq.br
described, relatively little is yet known about the
Received 11 November 2008; revised 27 April 2009; revision
causation or functions of such nonhuman primate
accepted 27 April 2009
aggression [Boesch et al., 2007].
DOI 10.1002/ajp.20713
Chimpanzees live in multi-male multi-female so-
Published online 1 June 2009 in Wiley InterScience (www.
cieties characterized by a high degree of fission–fusion
interscience.wiley.com).
r 2009 Wiley-Liss, Inc.

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Intra-Community Coalitionary Lethal Attack in Muriquis / 861
Wrangham, 1999] and intra-specific violence is a
resources [Wrangham & Peterson, 1996] and mur-
significant cause of mortality [Wilson et al., 2004]. In
iquis are commonly referred as the authentic ‘‘hippie
contrast, similar behaviors have only rarely been
monkey’’ [Strier, 1992b]. On the other hand, there is
observed in Neotropical species, e.g. capuchins [Grous-
slight sexual dimorphism in body and canine tooth
Louis et al., 2004; Valderrama et al., 1990] and spider
size in southern muriquis [Lemos de Sa et al., 1993;
monkeys [Campbell, 2006; Valero et al., 2006]. Adult
Zingeser, 1973] compared with northern muriquis,
males are the main initiators of attacks, and adolescent
which may suggest different aggressive tactics
or adult males, the main targets of attacks [Watts, 2004].
[Plavcan et al., 1995].
Fission–fusion social dynamics create opportu-
In this paper we present information on inter-
nities for large male parties from a given community
individual aggressive interactions and describe one
to surprise and attack smaller parties or lone
violent intra-community coalitionary lethal attack
individuals within and/or between communities,
against
a
lone
wild
southern
muriqui
male
with little risk. This is referred to as ‘‘the imbalance
(B. arachnoides) in the continuous forest of the
of power’’ hypothesis [Manson & Wrangham, 1991].
Parque Estadual Carlos Botelho (PECB), Sa
˜o Paulo
Boundary patrols create opportunities for low-risk
State, Brazil. We compare available ecological and
attacks, but similar power imbalances can also occur
behavioral information about muriquis and their
during encounters between foraging parties from
habitats in light of current functional explanations of
neighboring communities [Watts, 2006]. Several
primate coalitionary killings. These observations are
functional explanations for the occurrence of inter-
the first available evidence of aggressiveness and
community coalitionary killings have been proposed,
coalitionary lethal aggression for wild muriquis.
although it is controversial whether they apply
[Watts, 2004]. In chimpanzees, a positive relation-
ship between territory size and female reproductive
METHODS
success supports the idea that the dominance over
The observations reported here are part of an
neighboring communities provides indirect pay offs
ongoing long-term study (415 years) of the behavior
to males because it increases food availability for
and ecology of southern muriquis in continuous
their mates and offspring. Territory expansion and
Atlantic forest. Observations commenced in 1993 in
the elimination of neighboring males can result in
the northern section of PECB (37,644 ha; 24144–15
´S,
the incorporation of more females into the commu-
47
´46–10 W, 760 MASL), southern region of Sao Paulo
nity and increased mating opportunities [Watts,
State. The topography is characterized by hills,
2004; Wrangham, 1999]. In addition, killing danger-
valleys and mountains at altitudes ranging from
ous neighbors can eventually increase survivorship
50–810 m ASL [Custo
´dio-Filho et al., 1992]. Capu-
for all community members [Wrangham, 1999].
chins (Cebus nigritus) and howler monkeys (Alouatta
Thus, aggression is a strategic option employed when
clamitans) also occur at the field site [Talebi, 2008].
assessment of expected costs and benefits indicates
Additional details on the field site and the muriqui
that the attack will yield net benefits for the
groups can be found elsewhere [Custo
´dio-Filho et al.,
attackers [Wilson et al., 2004].
1992; Moraes et al., 1998; Talebi & Soares, 2005;
To date, most studies on Brachyteles have
Talebi et al., 2005].
focused on the northern muriqui inhabiting isolated
The PECB harbors the largest population of
forest fragments, whereas less is known of the
muriquis in Brazil and two social groups have been
southern muriqui in remnants of undisturbed con-
habituated to human observers, systematically fol-
tinuous Atlantic forest [Talebi et al., 2005]. Earlier
lowed and studied using an extensive trail system in
behavioral
observations
on
northern
muriquis
a total area of approximately 20 km2. These two
(B. hypoxanthus) [Strier, 1986] revealed that, similar
groups (Group Caete
ˆ, hereafter GC; Group Guaca
´,
to spider monkeys and chimpanzees, muriquis live in
hereafter GG) have been followed since 1993. The
a fission–fusion social system with multi-male, multi-
total number of individuals in GC is 48 individuals,
female communities and male philopatry in a highly
including 8 adult males and 10 adult females who can
fragmented habitat. These studies also revealed a
be individually identified. GC and GG are similar in
peaceful society, characterized by males and females
overall size and composition (Table I), including 5
maintaining
outwardly
egalitarian
relationships
adult males and 6 adult females who can be
with an absence of males territorially patrolling
individually identified in GG.
boundaries in a highly fragmented habitat [Strier,
Data on inter-individual aggression have been
1992a]. This unusual social peacefulness was paral-
collected from GC and GG since 1993, whereas
leled by similarities in body mass and body length
the coalitionary killing was a unique event seen on
between sexes in northern muriquis [Lemos de Sa
05/01/08 in GC. Since 2000, GC has been followed
et al., 1993]. A combination of behavioral and cranial
systematically for 15 days per month, whereas GG
features thus suggested that muriquis are the most
has been the subject of opportunistic monthly observa-
extreme example of a peaceful primate. It is the only
tions. Observations include party size, party activity
primate taxa that does not aggressively compete for
and composition and spatial location. Behavior of
Am. J. Primatol.

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862 / Talebi et al.
TABLE I. Illustration of group sizes and composition of the two study groups of southern muriquis (Brachyteles
arachnoides) in P.E. Carlos Botelho during the study period
2001
2007
Size
Composition
Size
Composition
Group 1 (GC)
38–44
14 M, 15 F, 9 Juv/ Inf
39–48
14 M, 14 F, 11 Juv/ Inf
Group 2 (GG)
Z28
14 M, 14 F
34–40
14 M, 14 F, 6 Juv
M, male; F, Female; Juv, Juveniles; Inf, Infants [Talebi, 2005].
TABLE II. Aggressive episodes observed in the PECB southern muriquis
Date
Time
Duration (min)
Emitter
Receiver
Agonistic behavior
Context
25.07.93
8.00 am
o10
3 M
1 M
CH,VOC
SS
26.07.93
8.01 am
15o20
4 M
1 M
CH, HG, AB, VOC
SS–FS
19.09.94
7.59 am
o10
7 M
1 M
CH, HG, AB, ACB, VOC
FS
24.04.97
9.12 am
o5
5 M
1 M
CH, BG, VOC
FSÃ
14.03.01
6.36 am
20425
7 M
1 M
CH, VOC
SS
14.03.04
7.12 am
o5
1 F
1 YF
ACB, VOC
?
1993–2005
n 5 35
–
M
M
CH, DIS, SUP, VOC
RF
M, male; F, female; YF, young female; RF, receptive female; Agonistic Behaviors: CH, chasing; HG, hand grabbing; BG, body grabbing; AB, attempt to bite;
ACB, actual bite; DIS, displacements/avoids; SUP, suplantation; VOC, threatening vocalizations (see text for behavioral definitions); SS, sleeping site;
FS, feeding site; FSÃ, abundant fruiting feeding site; ?, unknown.
individuals was recorded during instantaneous scan
of the targeted animal and pulled it violently for
samples, using 10 min sampling periods and 5 min
o10 sec, body grabbing where one animal violently
sampling intervals [Altmann, 1974]. Whenever inter-
grabbed another’s body foro20 sec, attempts to bite
group encounters were detected, observers documen-
(unsuccessful), actual biting (successful and directed
ted the location, context and sequence of events.
at any part of another animal’s body), sequential
Observation distance ranged from 10–30 m, using
supplantations where one individual avoided an-
10 Â 40 binoculars. Vocalizations described below
other, who took over its resource or space and/or
follow
prior
descriptions
for
northern
muriquis
threatening
vocalizations
(loud
neighs,
shouts,
[Mendes & Ades, 2004]. All research reported in
barks).
this manuscript is in agreement with the appro-
These
behaviors
were
considered
agonistic
priate national and institutional guidelines and applic-
rather than affiliative or neutral. They occurred
able laws.
primarily among males in contexts that suggest some
degree
of
competition
over
limited
resources
RESULTS
(Table II). These contexts could be divided into three
main types: (a) when a male was agonistically
Previous Observations of General Agonistic
intercepted in a coalitionary fashion by several males
Behavior in Southern Muriquis
as he attempted to join a male party that was chasing
Southern muriquis inhabiting dense forest of
a sexually receptive female; (b) when a male
PECB engage in social interactions infrequently,
approached a fruiting tree containing females and
averaging less than 2% of individual daily time
their offspring; (c) when a male was intercepted by a
[Talebi, 2005]. Inter-community interactions are
coalition of males and evicted as he was trying to
also relatively rare. Inter-community encounters
enter a sleeping site in the late afternoon. As
occurred on average 0.6 times per month from
muriquis are generally not aggressive or competitive,
1999–2009, but increased to 2.6 per month during
all such agonistic behavioral events, although rare,
the last 3 years. It is likely that the increased rate of
were unexpected. These sporadic, qualitative beha-
these encounters was an effect of enhanced habitua-
vioral observations provide the context for the
tion of both groups after 2000.
escalated and lethal coalitionary attack that we
Agonistic behavior occurred at very low frequen-
report on here.
cies of 2–3 events/yr and these appeared to opportu-
nistically target lone individuals when parties
encountered such individuals (Table II). Behavior
Specific Agonistic Behavior
observed during these events included inter-indivi-
As muriquis rarely engage in escalated aggres-
dual chasing over relatively large distances (o50 m),
sion, we detail the nature of all male–male aggressive
hand grabbing where one animal grabbed the hand
episodes seen between 1993 and 2004 during
Am. J. Primatol.

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Intra-Community Coalitionary Lethal Attack in Muriquis / 863
observations of both study groups (GC and GG). On
25/07/93 at 08.00 am, three adult males of CG
persistently and aggressively evicted a single adult
male from the group’s sleeping site. The following
day, at the same time and place, four adult southern
muriquis males vigorously chased an adult male who
approached the core feeding group’s location for
more than 20 min: they succeeded in hand–body
grabbing while not succeeding to bite the lone male.
All aggressive behavior was initiated by one or more
males toward a single approaching male.
On 19/09/94, 7.59 am, seven adult males persis-
tently chased an adult male. Two males succeeded in
body grabbing and one male succeeded in biting of
the upper leg of the arriving male. On 24/04/97 at
09.12 am, five males chased one adult male and body-
grabbing behavior was observed. On 14/03/01 at 6.36
pm, seven males acted together to block an adult
Fig. 1. Home ranges of muriqui GC (darker area) and GG (white
male from joining the group’s sleeping site. Although
area) groups were calculated from long-term observations using
male–male encounters have been sporadically ob-
the minimum convex polygon method. The location of the
observed attack (white circle) is depicted in relation to the
served throughout 15 years and 1,000s of hours of
previous observed inter-group encounters (black dots). Buffer
observation (n 5 17 on 11 different days), only once
zone was calculated as the prevalent location for behavioral
an adult female has been observed to firmly bite the
observation of both groups in any temporal scale.
leg of a young adult female (14/03/04) (Table II).
In addition to these rare, sustained male–male
interactions we also recorded 35 observations of male
General Description of the Lethal Attack
parties chasing a sexually receptive female. During
At dawn on 05/01/08, the 22 male and female
these episodes, males exhibited aggression among
adults, sub-adults and dependent offspring were
themselves: fast converging inter-individual displa-
clearly visible to three observers at 15–20 m above
cements, suplantation and tense-loud vocalizations
the ground. The identified individuals of CG group
(Table II).
that had been observed on the previous day were
again present with the same other group members.
Loud barking vocalizations commenced. A mixture of
males and presumably females all participated in
Behavioral Observations Prior to the Lethal
vocalizing. Seven adult males rapidly initiated an
Attack
upside-down collective embrace, suspended by their
Unusual interactions and sounds were first
tails. These individuals started to embrace and
noticed deep in GC core home range on 3rd January
vocalize in a tense agonistic manner, with arms
2008 at 09.49 am–approximately 48 hours prior to
pulling forcefully rather than the usual relaxed
the lethal attack. No inter-group encounters have
contacts. Other individuals tried to join this persist-
been previously recorded in this area (Fig. 1). Loud
ing and tense collective embrace but were excluded
vocalizations of shouting, barking and repeated
by two participating males. After 12 min, one adult
neighs [sensu Mendes & Ades, 2004] were heard.
male within the embrace was simultaneously at-
The next morning, on 04/01/08, the party consisted of
tacked by at least six adult males and two unidenti-
10 adult males, 12 adult females including three
fied adults, with sequential bites being directed at
females with dependent offspring, several sub-
the ventral, dorsal, genital and facial regions. The
adults, juveniles and infants. In addition, four
victim started to bleed profusely; meanwhile, other
identified individuals of CG were seen on 04/01/08
individuals including a female with a dependent
and none of the identified individual of Group GG
offspring joined the attack, biting the victim’s tail
were detected. Atypically, GC individuals were
and testicles. Juvenile individuals tried to join but
agitated, making repeated barking vocalizations
were expelled by adult males. The victim became
and fast movements or displacements through the
weak and faint, and stopped reacting, being held up
trees. Uncharacteristically, they vocalized loudly all
by his tail by another adult male. Adult males
day long (04/01/2008). Group behavior appeared
continued to bite for 7 min until the victim was
markedly tense. These frequent and loud vocaliza-
released and fell from the high canopy onto the
tions were similar to alarm calls and contrasted with
ground. The victim tried to move, but was immobile
previously observed more ‘‘relaxed’’ inter-groups
and appeared in pain and distress. He died 50 min
encounters. The party remained together overnight
after falling to the ground. After the attack,
at the same location (Fig. 1).
the muriquis who had attacked the male briefly
Am. J. Primatol.

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864 / Talebi et al.
descended to approximately 10 m above the ground
and under certain circumstances can exhibit the
to observe the male on the ground, and then resumed
aggressive patterns of other primates [Wrangham &
normal foraging activities without any further
Peterson, 1996].
aggressive behavior (Fig. 2) (see Appendix A for a
Such a conspicuous coalitionary attack has never
detailed description of the attack).
been previously observed in long-term field studies of
northern or southern muriquis. It is highly unlikely
that attacks were ‘‘missed’’ by observers at the
Examination of the Carcass
600 ha Caratinga Private Reserve (CTGA) [Strier
During an external macro-examination of the
et al., 2006] as northern muriquis have been followed
carcass, the following wounds were identified: (1)
at that field site daily for 201years. At PECB,
lacerations covered with blood on the left shoulder;
however, the larger study area (2,000 ha) combined
on the ventral base of the tail; both left and right
with fewer observers may account for why there
portions of the scrotal sack; (2) a 4 cm cut on the
were no previous observations of attacks. In addition,
middle-left temporal area of the head; (3) a 3 cm cut
as observers are rarely able to follow more than one
on the upper left lip of the corner of the mouth; (4) a
party at a time, many events such as inter-group
deep puncture wound in the area between the anus
interactions may go undetected. Southern muriquis
and the base of the tail surrounded by fresh blood;
live at low densities in PECB, and the fission–fusion
(5) lacerations in the ventrum across the lower
nature of their society contributes to reduced
abdominal region, descending to the genital area
numbers of observations: animals split into small
and (6) a laceration produced by biting at the base,
travelling parties of variable composition, scattered
middle and top of the penis. Inspection of the dead
across a large home range [Coles et al., 2008].
male’s teeth indicated that he was an elderly
Finally, a similar logic to that applied to chimpanzees
individual; five of the teeth were missing and his
[Wilson et al., 2004], where lethal attacks are
remaining teeth were heavily worn or worn down
expected to occur infrequently owing to the slow life
close to, or below, the gum line. No further
history and therefore reduced likelihood of extreme
postmortem osteological analyses were performed.
events in any animal’s lifespan, may apply to
muriquis: these are also long-lived animals (430
DISCUSSION
years)
[Strier,
2005],
reproducing
only
slowly
(7 years for sexual maturation, 7 months for
This report is the first observation of an intra-
gestation, and one offspring every 2.5–3.0 years)
specific coalitionary lethal attack for Brachyteles sp.,
[Strier & Ziegler, 2000]. These combined factors are,
a Neotropical primate genus recognized as the
to the best of our knowledge, the main suggestions as
most—and only—peaceful extant genus within the
to why there have been no prior observations of
Primate Order. Our observation adds one more case
coalitionary killing in southern muriquis.
to the database of coalitionary killings in primates. It
The lack of previous data on the aggressive
also demonstrates that southern muriquis are able to
capacities of muriquis in the context of male–male
gather into coalitions, collectively immobilize, attack
competition [Strier & Ziegler, 2000], combined with
and kill conspecifics. This unexpected coalitionary
infrequent episodes of inter-individual aggression
killing corroborates the suggestion that aggressive-
(e.g. Table II) and the lethal attack (n 5 1), compli-
ness is a general characteristic of the Primate Order.
cates efforts to test causal hypotheses related to the
Thus, muriquis do not innately lack aggressiveness
observed coalitionary killing.
It has been argued that coalitionary killings,
whether within or between groups/communities may
not be an evolved strategy but a rare and aberrant
behavior associated with unusual circumstances
[Wilson et al., 2004]. Yet, accumulating data from
long-term studies on chimpanzees [see Boesch et al.,
2007 for a review] and many other primates includ-
ing Neotropical species [see Watts, 2006 for a
review], demonstrates widespread inter- and intra-
community violence. This growing body of evidence
argues against the likelihood of these killings being
aberrant behaviors.
Could southern muriqui fission–fusion sociality
favor coalitionary killings during inter-community
encounters? Inter-communities encounters are rare.
These encounters, which occasionally lasted for
Fig. 2. During the lethal coalitionary attack, the southern
several days, were easily detected by frequent and
muriqui male received body and facial injuries resulting in
profuse bleeding.
repeated loud vocalizations associated with group
Am. J. Primatol.

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Intra-Community Coalitionary Lethal Attack in Muriquis / 865
cohesion [neighs, sensu Mendes & Ades, 2004] and by
1999] and spider monkey [Valero et al., 2006]
an atypically large party-size (44–70 individuals) and
attacks. Reproductive competition is a function of
probably with individual belonging to the same
the availability of cycling females relative to num-
community engaging in interactions such as play
bers of males. A male-biased sex-ratio and a low
and
embracing
more
frequently
than
usual.
number of receptive females enhances intra-commu-
Although occasional and infrequent chasing and
nity male tension and may trigger coalitionary
behavioral displays did occur among males, most
killing [Valero et al., 2006]. Both study groups at
likely between males belonging to different commu-
PECB have an equal adult (1:1) sex-ratio, although
nities, physical contact has never been observed
the effective sex ratio (given a 3-year interval
during these relaxed inter-community encounters. It
between reproductive events) is 3M:1F. Despite an
is therefore unlikely that observers simply missed
increase in northern muriqui group size over the last
many inter-communities encounters when they
20 years at CTGA [Strier et al., 2006] social tension
occurred. During the attack, however, vocalizations
owing to reproductive competition is absent among
(neighs) and group size were not typical of previously
males, who patiently wait in line without signs of
observed inter-community encounters. In addition,
aggression to copulate with a receptive female.
no inter-community encounters had ever been
A female will copulate with several males in a short
observed in the attack area (Fig. 1). Thus, the
period of time in order to maximizing her fertiliza-
combined evidence of our long-term observations of
tion chances [Strier, 1992b]. By contrast, no multi-
the spatial location and behavioral circumstances
male copulations have yet been observed in southern
strongly suggest that the lethal attack did not
muriquis. Moreover, male–male agonistic behaviors
happen during an inter-community encounter.
in the presence of receptive females have previously
If an inter-community attack is excluded, then
been observed in PECB (see Table II) [Talebi, 2005].
the coalitionary killing resulted from an intra-
The combination of enhanced sexual dimorphism in
community attack. This attack, where several in-
canine size [Lemos de Sa et al., 1993] with discrete
dividuals acted collectively and violently against a
mating tactics [Talebi, 2005] may suggest the
single individual, raises the possibility of intra-
occurrence of alternative aggressive tactics between
community rejection. One explanation for rejections
the two muriquis species.
associated with challenges for alpha rank status
In chimpanzees, Watts [2004] proposed that
[Wrangham, 1999] seems unlikely here, as no specific
though killing community individuals could result
intra-individual contest was observed, and the male
in fewer allies for inter-community conflicts, it would
was too old to be a possible challenger. The northern
still be advantageous to target individuals so as to
muriquis egalitarian society suggests that linear
reduce intra-community mating competition and
dominance relationships are absent and that mutual
‘‘sacrifice the weakest link or individual whose
ecological and social net benefits arise from collective
contribution to the system of male–male relation-
cooperation [Mendes, 1987; Strier, 1992a].
ships was the lowest’’ [Valero et al., 2006]. This
Another functional explanation for male–male
functional explanation would fit with the elimination
hostility includes priority of access to feeding
of an elderly male in this southern muriqui group.
resources and/or mating partners. Feeding and
Chimpanzees, spider monkeys and muriquis all
reproductive competition have been suggested as
have multi-male, multi-female societies character-
underlying factors for increased male tension, and
ized by a high degree of fission–fusion dynamics,
such aggression may trigger coalitionary attacks
male philopatry, female dispersal and high levels of
[Campbell, 2006; Valero et al., 2006; Watts, 2004;
male–male cooperation. Our observations challenge
Wrangham, 1999]. Food availability is high in PECB,
the view of the muriqui as the peaceful one among
fruit food patch sizes are large and productive
this group of species, and broadly support the
[Moraes et al., 1998] and preferential muriqui
hypothesis that imbalances of power contribute to
fruiting foods [Strier, 1991] are available—and
intra-specific killing in primates, as in chimpanzees
eaten—year round [Talebi et al., 2005]. Scarcity of
and humans. Thus, this unique observation in
preferred foods has not been observed at PECB
southern muriquis has the potential to reinvigorate
[Talebi et al., 2006; Talebi & Lee, 2008]. If social
discussions about the precursors of egalitarian and
tension owing to food scarcity triggered coalitionary
despotic societies, with potential implications for
killings, one might expect lethal attacks to occur at
understanding the functions and causes of escalated
CTGA, where there is higher muriqui density [Strier
inter-group aggression.
et al., 2006] and proportionally less food available in
smaller and less productive patches. Thus, we
suggest that feeding competition is unlikely to be
ACKNOWLEDGMENTS
an underlying factor initiating the coalitionary kill-
Sa
˜o Paulo State Forestry Institute & Parque
ing at PECB.
Estadual Carlos Botelho (Process permit SMA 41513/
Reproductive competition has been proposed as
99). Financial support has been provided by the
causal for chimpanzee [Watts, 2004; Wrangham,
CNPq, Brazilian National Research Council, Process
Am. J. Primatol.

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866 / Talebi et al.
20025699-8, WWF-IIE, Support for postgraduate
muscle; large blood stains were observed in the fur of
studies; Conservac-a˜o International (Brazil); ATBC
the victim in the regions of the lower and upper back,
Clifford Evans Grant, Margot Marsh Biodiversity
arms and legs. At least eight adult animals, including
Foundation, Primate Action Fund of Conservation
six adult males and two unidentified adults, were
International, MetroParks Zoo Cleveland, Idea Wild,
attacking the victim simultaneously; the attackers
Conservation Food and Health Foundation (USA);
were now reaching and biting simultaneously other
Manfred Hermsen Stiftung Foundation (Germany);
regions of the victim’s body such as feet, hands, tail,
Fauna & Flora International, DEFRA and Bromley
head, arm-pit, groin and genital area (scrotum and
Trust (UK). We are most grateful for the support of
penis); 08.31–08.33 (Very good visibility): The victim
Pedro Soares, Camila Freitas, Shormila Roy Choudh-
started to show tiredness and was less reactive to the
ury, Rebecca C. Coles, and Peter W. Lucas. All
attack; the victim was emitting low-frequency and
research reported in this manuscript is in agreement
low-amplitude vocalizations; The victim was still
with the appropriate national and institutional
suspended by his tail while the attackers continued
guidelines and applicable laws.
to inflict bites but the victim was no longer
vocalizing; 08.34 (Very good visibility): The victim
was no longer responding; he was totally without
APPENDIX A: DETAILED DESCRIPTION OF
movement and at this moment another adult male
THE ATTACK
was holding him only by his tail as the victim was
06.15 am (Good visibility): GC is located and
without any motor reaction; 08.35 (Good visibility):
whole-day group observation started. Group compo-
The victim was released and fell from the middle
sition: adults, sub-adults and youngsters male and
height canopy (15–20 m height) onto the ground;
females; 08.10 am (Good visibility): Tense and loud
when the victim reached the ground, without
vocalizations start, including shouting, barking and
emitting any further sounds, the participating
grinning by several individuals simultaneously;
attackers descended to approximately 10 m height
08.11–8.22 am (Very good visibility): Several indivi-
above the ground to observe the victim; 08.36 (Good
duals simultaneously and repeatedly emitted intense
visibility): The attacking muriquis moved away and
barking and shouting; some chaos is observed with
resumed their daily activities. They moved quickly
individuals moving fast and converging together;
away from the place of the agonistic attack; 08.40:
inter-individual spatial displacements and repeated
Human observers approached the victim on forest
episodes of suplantation were observed. It is a
floor, who is found bleeding profusely in a ventral
somewhat tense situation that leads to a ‘‘cacho,’’
position and is experiencing severe breathing diffi-
where several individuals embrace upside down
culties; 09.18: The victim remained lying down
suspended by their tails [Strier, 1994], but this time
ventrally and he appeared to be in agonizing pain
in an agitated, violent and more tense manner than
when he tried to move laterally by positioning his left
is usually observed during frequent cachos; 08.23
shoulder for body support. This action failed and he
(Very good visibility): Within this continued collec-
returned to the same ventral position; 09.20: The
tive embrace, loud shouts and barks were repeatedly
victim tried to move again, but again failed; 09.22:
heard; other individuals were continuously trying to
The victim was breathing deeply and adopted a
join the collective embrace of 48 muriquis but were
ventral position with his right hand holding a large
continuously repelled by the adult males, and loud
foliage shrub on the forest floor, whereas his left
barking episodes continued; 08.23–08.24 (Very good
hand supported his body on the forest floor. The
visibility): An adult male was being attacked as he
plantar face of the left foot was touching the forest
was squashed among the tense embraces performed
floor and his right foot was folded backwards; 09.27:
by at least seven males. The adult victim male was
The victim was no longer moving or emitting any
immobilized in the upside down position; individuals
sound; 09.28: The victim was no longer breathing
start to repeatedly bite and shout while the victim
and bugs and mosquitoes arrived at his carcass;
reacted with loud screaming. Concomitantly, addi-
09.32: The victim was declared dead and removed by
tional individuals were still trying to join the action
human observers.
but were again repelled by participating adult males;
08.25–08.27 (Good visibility): The collective tense
embrace continued with loud vocalizations, stressful
movements and nonstop repeated bites to all body
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