Interactions
Between Third Parties and Consortship Partners
in Tonkean Macaques
(Macaca
tonkeana)
Arianna De Marco Roberto Cozzolino
Francesco Dessi-Fulgheri Bernard
Thierry
Abstract
Sexual competition is potentially disruptive
for the cohesion of social groups because stress
and conflicts can extend to other group members.
The displays and interactions of sexual partners
are liable to influence the behavior of
groupmates, which may need to observe them to
anticipate possible consequences. We studied 2
captive groups of Tonkean macaques (Macaca
tonkeana) to test whether group-mates pay more
attention to consort partners, modify their
activities and social interactions, and exhibit
signs of stress during periods of sexual
consortships. We found that group-mates
approached the top-ranking male more frequently
and were more frequently oriented toward the
consort pair at the time of consortship than at
other times. Group-mates spent less time
sleeping, and devoted less time to manipulating
the environment and more time to monitoring
during consortship. This indicates that
consortships may incur costs in individuals not
involved in sexual competition. However, Tonkean
macaques did not exhibit any signs of increased
stress during consortship periods, as their
rates of scratching and yawning did not
differ between consortship and nonconsortship
periods. This study shows that not only direct
competitors but also other individuals monitor
the behavior of sexual partners. It is likely
that group-mates obtain information this way
about ongoing action, and take decisions
accordingly.
Introduction
In group-living animals, sexual competition
is potentially disruptive for the cohesion of
social groups. With their large body size and
large canines, males can compete overtly for
access to females (Plavcan 2004). Not only can
they fight and wound each other or attack the
female (Clutton-Brock and Parker 1995; Huffman
1987; Manson 1994), but conflicts can also
extend to other group members, increasing social
tension and inducing energy loss (Smuts and
Smuts 1993; van Schaik et al. 2004). The
majority of researchers have focused on the
behavior of sexual partners and competitors, and
little is known about their influence on
group-mates. Recent studies have shown that the
outburst of conflicts influences the behavior
not only of opponents but also of uninvolved
individuals; in hamadryas baboons (Papio
hamadryas hamadryas) and Tonkean macaques
(Macaca tonkeana), bystanders are more likely to
affiliate with one another to cope with social
tension after fights (De Marco et al. 2010;
Judge and Mullen 2005). In several species,
individuals use social grooming to reduce the
tension generated when group members anticipate
the competition induced by a forthcoming food
distribution (Macaca arctoides: Mayagoitia et
al. 1993; Pan troglodytes: Koyama and Dunbar
1996; Cebus apella: Polizzi di Sorrentino et al.
2010).
Given the cognitive abilities of monkeys, it
is expected that bystanders acquire information
by following the interactions occurring between
sexual partners. Not only do monkeys know their
own affiliative bonds and dominance
relationships with others, but they are also
aware of the social relationships linking their
group-mates (Bergman et al. 2003; Bovet and
Washburn 2003; Cheney and Seyfarth 1990; Dasser
1988). They can take relative ranks between
their opponents and potential allies into
account when recruiting support (Silk 1999).
They also track the gaze of others and predict
their behavior from subtle gestures and vocal
cues (Bergman et al. 2006; Tomasello et al.
1998; Wood et al. 2007). In Tonkean macaques,
for instance, individuals orient their food
search using visual and olfactory cues conveyed
by group-mates (Drapier et al. 1999 2002).
In several Old World monkeys, the swelling
of the perineal skin conspicuously signals
female sexual receptivity (Dixson 1998; Higham
et al. 2008). Males react to changes in genital
swelling and are more likely to mate when it is
particularly large and brightly colored (Dixson
1998; Domb and Pagel 2001). Females can utter
specific vocalizations during the reproductive
period (Maestripieri and Roney 2005; Pradhan et
al. 2006). The finding that males inspect and
smell the perineal area of estrous females
suggests that they exploit olfactory signals to
monitor a female's reproductive condition
(Hausfater 1975; Hdry and Whitten 1987). There
are hints that olfactory cues indicate fertility
in macaques (Cerda-Molina et al. 2006; Michael
and Keverne 1968), but their importance in
catarrhines remains questionable (Dixson 1998;
Snowdon 2004).
Whether sexual displays are reliable
indicators of female fitness (Pagel 1994) or
intracycle signals of the distribution of
ovulation (Nunn 1999), it is certain that they
convey information to competing males about the
fertility of a potential mate (Deschner et al.
2003; Emery and Whitten 2003; Higham et al.
2008). The information provided by sexual
displays is available not only to dominant males
but also to other group members, albeit probably
in different ways according to the distance
between individuals (Higham et al. 2009).
Signaling interactions represent an additional
source of information about relative features
that can be used by conspecifics to direct their
behavior (McGregor 2005). In chacma baboons
(Papio hamadryas ursinus), higherranking males
monopolize mating by remaining close to sexually
receptive females. Using playback experiments,
Crockford et al. (2007) have demonstrated that
lowerranking males specifically react when
informed that dominant males and estrous females
are temporarily apart, indicating that they can
track changes in the status of consortship and
quickly identify mating opportunities. In
Barbary macaques (Macaca sylvanus), males
respond more strongly to playbacks of copulatory
calls uttered by females during ejaculatory
copulations than after those recorded during
nonejaculatory copulations, meaning that they
eavesdrop on mating outcome (Pfefferle et al.
2008). Tonkean macaques originate from the
island of Sulawesi, Indonesia, and form
multimale, multifemale groups. Females show
clear behavioral, morphological, and endocrine
changes throughout the ovarian cycle (Aujard et
al. 1998; Thierry et al. 1996). Around the
ovulatory period they display brightly colored
and voluminous genital swelling, and emit a
specific estrus call (Masataka and Thierry 1993;
Thierry et al. 1996). Reproduction occurs all
year round. There is usually only one
periovulatory female available at any one time,
and the top-ranking male is able to monopolize
sexual access to her over several days in a
sexual consortship (Thierry 2010).
We investigated changes in the behaviors of
group-mates at the time of sexual consortship in
2 groups of Tonkean macaques. Because periods of
sexual competition correspond to heightened
levels of conflicts between males (Thierry,
unpubl. data), group-mates may need to follow
the interactions occurring around sexual
partners to anticipate better their potential
consequences even if this imposes a load on
their activity budget. On the other side, the
top-ranking male has to maintain his monopoly
over the estrous female by keeping other
individuals at a distance. We predicted that
during consortship 1) group-mates should pay
more attention to sexual partners and possibly
approach them; 2) the top-ranking male should
prevent the approaches of group members,
increasing his rate of conflicts with other
males; 3) group-mates should spend more time
monitoring at the expense of other activities;
and 4) group-mates should exhibit signs of
stress in relation to the context of sexual
competition.
Discussion
This is the first study demonstrating that
the behavior of group members is modified at the
time of sexual consortship in primates. The
close association between sexual partners
influenced the social interactions, activities,
and interindividual distances of group-mates
significantly. As found in a previous study
(Aujard et al. 1998), topranking males also
spent more time in contact-sitting with
receptive females and more frequently copulated
with them.
Our first prediction was supported, i.e.,
that group-mates would pay special attention to
sexual partners. Not only was the proportion of
affiliative interferences in mating between the
top-ranking male and the estrous female higher
during consortship than in control periods, but
also the consort pair attracted the attention of
other group members. In general, group-mates
were more frequently oriented toward the
top-ranking male and the female at the time of
consortship and they approached the top-ranking
male more often. Different individuals could
have different motivations for paying attention
to sexual partners. For instance, adult males
could be waiting for mating opportunities if the
female escapes the attention of the topranking
male. On the other hand, group-members
interfered in mounts more often at the time of
consortship than at other times. It is known
that immature individuals interfere more often
than older group members, especially when their
mother is involved (Thierry 1986). Here they
watched and followed the behaviors of sexual
partners, being in a position to learn about
mate guarding and mating. The previous results
are particularly interesting in view of the fact
that the topranking male performed mate guarding
by spending more time positioned between the
female and group-mates during consortship, and
by actively interposing himself between her and
approaching group-mates, especially when the
latter were males. Rates of conflicts between
him and other males remained relatively low at
the time of consortship, but they increased in 1
of the 2 groups, consistent with our second
prediction.
It is a general finding that females
increase their locomotory activity and reduce
foraging during the periovulatory period (Aujard
et al. 1998; Bercovitch 1983; Dixson 1998). Mate
guarding and aggression are also associated with
costs for dominant males in terms of time and
energy expenditure, as reported in savannah
baboons (Papio sp.: Alberts et al. 1996;
Bercovitch 1983). Although the amount of sexual
effort in lower-raking males is weaker than
those of the top-ranking one in Japanese
macaques (Macaca fuscata: Matsubara, 2003), our
results in captive Tonkean macaques show that
the daily activities of other group
members&emdash;adults and subadults&emdash;can
be significantly affected regardless of their
sex. In accordance with our third prediction,
group-mates spent less time sleeping or
manipulating the environment, and they devoted
more time to monitoring during consortship.
Thus, the consort period could incur costs for
other group members, even those not directly
involved in sexual competition.
Contrary to our fourth prediction,
group-mates did not exhibit signs of stress
during sexual consortship. Because the rates of
conflict remained relatively low, and thus the
likelihood of injuries, it may be that mate
guarding did not make groupmates more anxious
than usual. In a previous study in Tonkean
macaques, we found higher rates of affiliation
between group-mates having observed a conflict,
although they display low levels of scratching
and yawning (De Marco et al. 2010).
Compared to other macaque species, Tonkean
macaques are characterized by relaxed dominance
(Thierry 2010; Thierry et al. 1994). Agonistic
interactions usually remain at low levels of
intensity, third parties can stop aggression by
addressing appeasement signals to opponents, and
a majority of conflicts are followed by
reconciliation (Demaria and Thierry 2001; Petit
and Thierry 1994; Thierry 1985). An alternative
explanation would be that scratching and
yawning are not reliable indices of
anxiety in Tonkean macaques. Different measures
of anxiety will be necessary to know whether
Tonkean macaque group-mates are particularly
able to cope with the stressful situation
induced by sexual competition.
In chacma baboons and Barbary macaques,
listening to vocalizations emitted by sexual
partners provides adult males with information
about their interactions (Crockford et al. 2007;
Pfefferle et al. 2008). Our study in Tonkean
macaques adds that not only direct competitors
but also other conspecifics closely monitor the
behaviors of sexual partners. Given the
cognitive abilities of monkeys, it is likely
that bystanders can pick up on multiple cues
through observation and take decisions
accordingly (McGregor 2005; Valone 2007). The
present results are drawn from 2 small groups,
and further sampling will be needed to increase
statistical power. Future research should
investigate whether the present conclusions are
applicable to wild animals, and determine which
behavioral cues are informative for
bystanders.
