Signals use by leaders in Macaca tonkeana and Macaca mulatta: group-mate recruitment and behaviour monitoring.

Anim Cogn (2010) 13:239–248
DOI 10.1007/s10071-009-0261-9ORIGINAL PAPER
Signals use by leaders in Macaca tonkeana and Macaca mulatta:
group-mate recruitment and behaviour monitoring
Cédric Sueur · Odile Petit
Received: 11 August 2008 / Revised: 29 June 2009 / Accepted: 30 June 2009 / Published online: 14 July 2009
© Springer-Verlag 2009
Abstract Animals living in groups have to make consen-
sus decisions and communicate with each other about the
time, or the direction, in which to move. In some species,
the process relies on the proposition of a single individual,
i.e. a Wrst individual suggests a movement and the other
group members decide whether or not to join this individ-
ual. In Tonkean (Macaca tonkeana) and rhesus macaques
(Macaca mulatta), it has been observed that this Wrst indi-
vidual displays speciWc signals at departure. In this paper,
we aimed to explore the function of such behaviours, i.e. if
these behaviours were recruitment signals or only cues
about the motivation of the Wrst departed individual. We
carried out temporal analyses and studied the latencies of
the Wrst departed individual’s behaviours and of the joining
of other group members. We also assessed whether the
social style of a species in terms of dominance and kinship
relationships inXuenced the patterns of signal emissions.
We then analyzed how the Wrst departed individual decided
to make a pause or to stop it according to the identities of
group members that joined the collective movement.
Results showed that Tonkean macaques and rhesus
macaques seemed to use back-glances to monitor the join-
ing of other group members and pauses to recruit such indi-
viduals. This was especially the case for highly socially
aYliated individuals in Tonkean macaques and kin-related
individuals in rhesus macaques. Moreover, back-glances
and pauses disappeared when such individuals joined the
Wrst departed individual. From these results, we suggested
that such behaviour could be considered intentional. Such
Wndings could not be highlighted without temporal analyses
and accurate observations on primate groups in semi-free
ranging conditions.
Keywords Decision-making · Collective movement ·
Intention · Macaque · Social style · Kinship
Introduction
Most animals have to move to speciWc areas for drinking,
resting or foraging. For group-living species, these move-
ments need to be collective in order to keep the advantages
of sociality for group members (Alexander 1974; Wrangham
1980). This synchronization requires communication and
consensus between individuals so that collective decisions
can be made about the time and the direction of movement
(Conradt and Roper 2005; Krause and Ruxton 2002). The
processes underlying these consensuses may vary across
species. In Hamadryas baboons (Papio hamadryas hama-
dryas) and African buValo (Syncerus caVer), voting behav-
iours seem to occur before the departure of the group;
several individuals may suggest diVerent choices and the
group then decides to move in the direction for which the
majority of individuals displayed such voting behaviour
(Conradt and Roper 2005; Kummer 1968; Prins 1996).
However, in some species the process relies on the proposi-
tion of a single individual, the leader or initiator (Leca
et al. 2003; Couzin et al. 2005; Sueur and Petit 2008b;
Stueckle and Zinner 2008). This Wrst departed individual
suggests the time or the direction to move (Hall and
C. Sueur · O. Petit (&)
Departement d’Ecologie, Physiologie et Ethologie,
Centre National de la Recherche ScientiWque & Université de
Strasbourg, 23 rue Becquerel, 67087 Strasbourg, France
e-mail: odile.petit@c-strasbourg.fr
C. Sueur
e-mail: cedric.sueur@c-strasbourg.fr123

240 Anim Cogn (2010) 13:239–248DeVore 1965; Kummer 1968; Sueur and Petit 2008a) and
the other group members decide whether or not to join this
individual (Leca et al. 2003; Stueckle and Zinner 2008).
Signals used by this individual may be visual, acoustic and/
or odorous and may depend on environmental conditions,
such as vegetation density (Boinski and Garber 2000). In
the Mountain gorilla (Gorilla gorilla berengei), the silver-
back walks quickly in the direction of the future movement
(Watts 2000), whereas common chimpanzees (Pan troglo-
dytes) seem to use drumming on buttressed trees (Boesch
1991) and Barbary macaques (Macaca sylvanus) seem to
use branch shaking (Mehlman 1996) to signal the departure
of a collective movement. Authors have observed that
acoustic signals, such as a ‘deep hoarse cluck’ in the howler
monkey (Alouatta palliata, Carpenter 1934) and ‘coo’
vocalization in Japanese macaques (Macaca fuscata, Itani
1963) and ‘trill’ in the white-faced capuchin monkey
(Cebus capucinus, Boinski and Campbell 1995) are also
given before groups depart. Similarly, a ‘loud call’ was
reported in Sulawesi macaques in the context of collective
movements (Riley 2005; Thierry et al. 2000). A more
empirical study on semi-free ranging white-faced capuchin
monkeys showed that the Wrst departed individual dis-
played recruitment and monitoring behaviour during the
onset of a collective movement (Meunier et al. 2007).
Moreover in capuchin monkeys, the behaviour of other
group members seemed to aVect the behaviour of the Wrst
departed individual (as a feedback): when the numbers of
joiners increased, the number of signals the Wrst individual
displayed decreased (Meunier et al. 2007). Similarly in
Tonkean (Macaca tonkeana) and rhesus macaques
(Macaca mulatta), the Wrst departed individual displayed
pauses and back-glances at departure (Sueur and Petit
2008a). However, we did not investigate the eVect of such
behaviour on other group members in this previous study.
In this current study, we performed temporal analyses to
explore the function of such behaviours and whether they
diVered between both species. We aimed to assess whether
the behaviours displayed by the Wrst departed individual
were recruitment and/or monitoring’ signals. Moreover, we
aimed to verify if the social style of a species (de Waal and
Luttrell 1989), especially in terms of nepotism, may inXu-
ence the emission of signals—as is the case for the organi-
zation of joining (Sueur and Petit 2008b). Rhesus macaques
are more nepotistic than Tonkean macaques: many behav-
iours, such as grooming, reconciliation and social play are
constrained by kinship in rhesus macaques but not in Tonk-
ean macaques (Thierry 2004, 2007). Therefore, we
assumed that rhesus macaques would stop displaying sig-
nals after kin-related individuals have joined. Conversely,
Tonkean macaques should display signals to recruit strong
aYliated individuals, whatever their degree of kinship
might be.
Methods
Subjects and study area
The groups under investigation were bred in the Centre of
Primatology at the Strasbourg University, in semi-natural
conditions. All group members were born in captivity. The
group of rhesus macaques composed of two matrilines. At
the time of the study (May 2006 to August 2006) the group
consisted of 22 individuals: two adult males (17 and
8-years-old), 11 adult females (16, 14, 12, 11, 11, 11, 8, 7,
7, 7 and 6-years-old), two sub-adult females (both 4-years-
old) and 7 infants (<1-year-old). The group of Tonkean
macaques composed of Wve matrilines. At the time of the
study (November 2005 to March 2006), the group consisted
of 10 individuals: one adult male (10-years-old), Wve adult
females (10, 9, 7, 6 and 5-years-old), one subadult male
(3-years-old) and three juveniles (2, 1 and 1-year-old). The
composition of the two groups was comparable to wild
groups (Makwana 1978; Supriatna et al. 1992; Whitten
et al. 1987). Maternal kin relationships are known for both
groups. We did not analyze the infants’ behaviour as their
discrimination was impossible. The study was based on 15
rhesus macaque individuals and on 10 Tonkean macaque
individuals. Each group lived in a park (fenced Weld of
0.5 ha) with trees, bushes and grassy areas. The area had an
inside shelter (20 m2), where commercial pellets and water
were provided ad libitum. Fruit and vegetables were dis-
tributed once a week, outside of observation sessions. For
both species, groups were cohesive and moved collectively
(as a whole group or in sub-groups) between areas devoted
to speciWc activities (for details, see Sueur and Petit 2008a).
DeWnitions
The beginning of a collective movement was deWned by the
departure of a single Wrst individual (Wrst departed individ-
ual) walking more than 10 m in <40 s (Leca et al. 2003;
Sueur and Petit 2008a, b). Any individual walking for more
than 5 m in a direction that formed an angle smaller than
45° with the direction of the Wrst departed individual and
within 5 min after the departure of the Wrst departed indi-
vidual was labelled a joiner (Sueur and Petit 2008a, b). This
time window was determined by the mean latency separat-
ing the joining of two direct participants; mean =
27.9 § 1.1 s for Tonkean macaques; mean = 64.1 § 2.7 s
for rhesus macaques; where joining is the moment at which
an individual starts to follow (Sueur and Petit 2008a).
We deWned the departure latency, of every joiner, as the
time elapsed between its departure and the time of the Wrst
departed individual.
The duration of a collective movement is the time
elapsed between the departure of the Wrst individual from123

Anim Cogn (2010) 13:239–248 241the start point and the arrival of the last individual at the
end point (Sueur and Petit 2008a).
Individual behaviours were recorded when exhibited at
departure or during the progress of the movement. The fol-
lowing represents a list of deWnitions of behaviours that
have been used for the current study and were identical to
those described by Meunier et al. (2007) and Sueur and
Petit (2008a):
– Speed of each individual: in m s¡1, the time an individ-
ual needed to cover the Wrst 10 m after its departure.
– Back-glance the individual looks in the direction of other
group members, measured as a frequency throughout the
movement (i.e. as long as the individual moves). In the
cases, where eyes of animals could not be observed, we
used the direction of the head (with an angle wider than
135° with the direction of the movement) to determine a
back-glance (Fig. 1).
– Pause the individual stops moving for at least 2 s. The
frequency of pauses throughout the movement was
recorded. A pause was qualiWed as a distinct event when
it was separated by more than 2 s from a preceding one.
– Loud call a high-pitched vocalization composed of
phrases consisting of frequency modulated units (Thierry
et al. 2000).
We considered only pauses that were longer than 2 s in
order to discard pauses due to the display of other behav-
iours (back-glances or loud call). Nevertheless, when a
back-glance was emitted simultaneously with a pause
longer than 2 s, we considered the two events as indepen-
dent. For analyses, we considered “a pause after a back-
glance” as a pause occurring at least 2 s after the end of the
preceding back-glance. We considered “a back-glance after
a pause”, a back-glance occurring at least 2 s after the end
of the preceding pause.
Observation procedure
Groups were observed and Wlmed continuously by two
observers (simultaneously in order that all individuals were
always seen), 4 h per day between 10:00 and 16:00 hours.
Each collective movement was recorded onto videotape
and these videotapes were analyzed only by one person
(C·S.). Participants (Wrst departed individual and joiners)
were observed one by one using video scoring. Movements
for which data about behaviours were missing were not
taken into account in the analyses. For example, we dis-
carded cases in which an individual had not been continu-
ously observed, since we could not determine whether
behaviours, such as pause or back-glance might have been
displayed. Movements occurring in context of conXict or
sexual consort were discarded. Collective movements were
taken into account only if more than 2/3 of group members
were present in the starting zone (·10 m from the point
where the Wrst departed individual started, Sueur and Petit
2008a, b). With this criterion, both groups were not dis-
persed in the majority of cases (the diameter was inferior to
10 m in both groups). The departure of the Wrst departed
individual over a distance of more than 10 m was an obvi-
ous signal for other group members (Leca et al. 2003;
Sueur and Petit 2008a). We drew a plan of each park allow-
ing us to measure the distance walked by group members
(Sueur and Petit 2008a).
We observed 131 collective movements for the rhesus
macaques and 146 movements for the Tonkean macaques.
Data scoring
We scored the identity and the behaviour (speed, back-
glance, pause and loud call, see deWnitions above) of the
Wrst departed individual and of every joiner.
We scored the departure latency of every joiner. Using
these latencies, we determined the order of individuals at
each collective movement. At departure, we attributed rank
0 to the Wrst departed individual and rank j to the individual
that joined the movement when j individuals were already
participating. Thus, jmax = n ¡ 1, where n is the number of
individuals of each group (except infants).
In the same way, we recorded the start time and the end
time of each back-glance and of each pause. These data
allowed us to study the dynamics of the collective move-
ment and to assess whether behavioural changes implied
changes in the joining of group members (or the
converse).
To determine these times and latencies, we used the time
indicated on the video-tape.
Fig. 1 Illustrations of one back-glance for one Tonkean macaque
(left) and for two rhesus macaques (right). The arrows indicate individ-
uals displaying back-glance123

242 Anim Cogn (2010) 13:239–248Social relationships
Kinship
We considered two individuals as related when belonging
to the same matriline regardless of their degree of related-
ness and addressed a coeYcient equalled 1 to the dyad.
Then, in order to make results of both species comparable,
we corrected the coeYcient of kinship for each individual
by the number of its kin-related individuals.
AYliation
AYliative relationships were quantiWed by calculating the
number of events when two individuals were observed
within body contact out of moving context. This was car-
ried out, using instantaneous scan sampling every 5 min
(Altmann 1974). We kept only scans, where all group
members could be observed. We collected 88 scans for rhe-
sus macaques and 111 for Tonkean macaques. For subse-
quent analyses, we used the “ratio of contacts” that was the
number of scans for which two individuals were in contact
per the total number of scans. Thus, aYliative relationships
represented preferential relationships between group mem-
bers (including kin and non-kin related partners).
Statistical analysis
The majority of group members, whatever the species, can
be the Wrst departed individual of a movement. This Wrst
departed individual was any group member in Tonkean
macaques whereas only adults initiated a collective move-
ment in rhesus macaques (Sueur and Petit 2008a). Rates of
initiations were not diVerent among initiators whatever the
species (Sueur and Petit 2008a) was. Moreover, ranks are
not tied to individuals (as found by Sueur and Petit 2008b).
As a consequence, we analyzed the behaviour of the Wrst
departed individual and other ranks in the movement,
regardless of their identities (Leca et al. 2003; Sueur and
Petit 2008a; Stueckle and Zinner 2008).
We tested correlations between rank at departure and
mean number of signals using the Spearman rank correla-
tion test and analyzed the curves using curve estimation
tests. We tested inter-rank diVerences using Kruskall-Wal-
lis tests followed by post-hoc Dunn’s multiple comparisons
test. We carried out these tests using SPPS 10.0 and Graph-
Pad Prism 4.03. We then carried out matrices correlations
using Socprog2.3 (Whitehead 1997, 2009) with Kr test tak-
ing into account missing values of a matrix and allowing to
compare the values of each row with all other values in the
row (Hemelrijk 1990; Whitehead 1997, 2009). This row
wise matrix correlation method is suited for the evaluation
of these types of covariance between behaviours and is
appropriate for small-sized matrices (de Vries et al. 1993).
We set the number of permutations at 10,000 for each cor-
relation matrices test (Whitehead 1997, 2009). Permuta-
tions of the rows and columns of one of the two matrices
were generated and for each permutation, statistical values
were calculated. This method provided more accurate and
stable p values (Hemelrijk 1990; de Vries et al. 1993;
Whitehead 1997). Mean values are represented as §SE.
� = 0.05.
Results
How did behavioural patterns vary according to ranks
at departure?
The mean group stationary time before moving was
1,161 § 210 s (19.35 § 3.5 min) for Tonkean macaques
and 868 § 84 s (14.47 § 1.4 min) for rhesus macaques. In
both species, no loud calls occurred during collective
movements. For each collective movement, at least one
individual carried out pauses and back-glances. In Tonkean
macaques, the Wrst departed individual emitted at least one
pause or back-glance in 109 cases out of 146 collective
movements. In rhesus macaques, the Wrst departed individ-
ual emitted at least one pause or back-glance in 92 cases out
of 131 collective movements.
Pauses and back-glances are correlated for Tonkean
macaques (Spearman rank correlation: N = 146, r = 0.25,
p = 0.002) and for rhesus macaques (Spearman rank corre-
lation: N = 131, r = 0.43, p < 0.0001). Indeed, it seems that
the Wrst departed individual emitted back-glances when it
made pauses. However, even if these two variables are cor-
related, they are not collinear (collinearity diagnostics,
VIF · 1.272 for both species; collinearity is a high correla-
tion between two variables: the variance inXation factor
(VIF) has to equal at least 5 to consider two variables as
collinear and thus as dependent (Pallant 2007)). We can
therefore consider the number of pauses and the number of
back-glances as independent variables.
These behaviours might reXect a willingness of staying
cohesive. Then, their frequencies should decrease when the
number of joiners increased and also, with the rank. So, we
assessed if mean frequencies of pauses and back-glances
and mean speed decreased according to the rank of an indi-
vidual at the departure of a collective movement as has
been observed in white-faced capuchins (Meunier et al.
2007, Table 1).
Back-glances
The mean frequency of back-glances and rank were nega-
tively correlated for Tonkean macaques (N = 10, rs = ¡0.75,123

Anim Cogn (2010) 13:239–248 243p = 0.012) and rhesus macaques (N = 15, rs = ¡0.71,
p = 0.04). For Tonkean macaques, we found that mean fre-
quency of back-glances diVered between ranks (Kruskall-
Wallis test, H = 94.32, df = 9, p < 0.0001) with only rank 0
having a higher frequency than other ranks (Dunn’s multi-
ple comparison test, p < 0.001). For rhesus macaques, mean
frequency of back-glances also diVered between ranks
(H = 65.67, df = 14, p < 0.00001) with only rank 0 having a
higher frequency than ranks 1 to 6 and rank 8 (Dunn’s mul-
tiple comparison test, p < 0.01). The Wrst departed individ-
ual displayed 71% of all recorded back-glances in Tonkean
macaques and 56% in rhesus macaques.
Pauses
The mean frequency of pauses and rank were negatively
correlated for Tonkean macaques (N = 10, rs = ¡0.65,
p = 0.042) and rhesus macaques (N = 15, rs = ¡0.72,
p = 0.002). In Tonkean macaques, ranks did not diVer in
their frequencies of pauses (Kruskall-Wallis test,
H = 15.32, df = 9, p = 0.08). However, in rhesus macaques,
mean frequency of pauses diVered between ranks
(H = 65.67, df = 9, p < 0.0001), with only rank 0 having a
higher frequency than ranks 1 to 6 (Dunn’s multiple com-
parison test, p < 0.001). The Wrst departed individual dis-
played 19% of all recorded pauses in Tonkean macaques
and 34% in rhesus macaques.
Speed
If the speed is a recruitment signal, then the Wrst departed
individual and the Wrst joiners should have a speed higher
than the last joiners. However, the mean speed and rank
were not correlated in Tonkean macaques (N = 10,
rs = ¡0.08, p = 0.830) and in rhesus macaques (N = 15,
rs = ¡0.40, p = 0.22). We found that mean speed did not
diVer between ranks in Tonkean macaques (Kruskall-Wal-
lis test, H = 14, df = 14, p = 0.120) and in rhesus macaques
(Kruskall-Wallis test, H = 14.52, df = 9, p = 0.153).
How did the number of joiners inXuence the behaviour
of the Wrst departed individual?
Based on the previous results, we analyzed further pauses
and back-glances for the Wrst departed individual only.
If pauses or back-glances are used by the Wrst departed
individual to recruit and/or monitor joiners as in white-
faced capuchins (Meunier et al. 2007), their frequencies
should decrease when the number of joiners increases. Fre-
quencies of pauses should also decrease if pauses reXected
some uncertainty. Indeed, the Wrst departed individual
would express its hesitation by waiting for other group
members to join the movement. Thus when no individuals
joined the Wrst departed individual, it seems logical that this
latter one tried to recruit group members by emitting sig-
nals and/or waited their joining. When the Wrst individual is
joined by a majority of individuals, it did not need to fur-
ther use signals or wait.
Back-glances
The mean frequency of back-glances and the number of
joiners were negatively correlated in Tonkean macaques
(N = 10, rs = ¡0.63, p = 0.04, Fig. 2a) and in rhesus
macaques (N = 15, rs = ¡0.77, p = 0.006, Fig. 2c). For
Tonkean macaques, we found that mean frequency of back-
glances diVered according to the number of joiners (Kruskall-
Wallis test, H = 48.2, df = 9, p < 0.00001). The Wrst
departed individual displayed more back-glances when no
individual had joined the movement than when 2 or more
individuals had joined it (Dunn’s multiple comparison test,
Table 1 Intensity of signals per collective movement (mean number
of back-glances, mean number of pauses, mean speed in m/s;
mean § SE) according to the rank at departure for collective move-
ments in the Tonkean macaques group and the rhesus macaques group
Rank 0 corresponds to the Wrst departed individual, rank 1 to the Wrst
joiner, etc
Rank Mean no. of
back-glances
Mean no. of
pauses
Mean speed
Tonkean
macaques
0 0.53 § 0.12 3.02 § 0.28 0.62 § 0.02
1 0.10 § 0.04 2.91 § 0.34 0.52 § 0.03
2 0.03 § 0.02 2.51 § 0.33 0.55 § 0.04
3 0.07 § 0.04 2.48 § 0.31 0.62 § 0.06
4 0.07 § 0.07 1.77 § 0.21 0.70 § 0.10
5 0 2.17 § 0.28 0.59 § 0.07
6 0 2.6 § 0.37 0.63 § 0 .09
7 0 2.40 § 0.32 0.54 § 0.04
8 0.03 § 0.03 2.43 § 0.47 0.48 § 0.05
9 0 2.17 § 0.50 0.66 § 0.10
Rhesus
macaques
0 0.94 § 0.12 1.19 § 0.11 0.58 § 0.03
1 0.41 § 0.10 0.75 § 0.13 0.58 § 0.03
2 0.27 § 0.08 0.72 § 0.12 0.57 § 0.04
3 0.15 § 0.08 0.87 § 0.14 0.58 § 0.05
4 0.27 § 0.09 0.81 § 0.15 0.24 § 0.04
5 0.05 § 0.03 0.55 § 0.13 0.49 § 0.06
6 0.11 § 0.08 0.59 § 0.32 0.52 § 0.07
7 0.21 § 0.12 0.95 § 0.35 0.40 § 0.07
8 0 0.46 § 0.27 0.52 § 0.07
9 0.40 § 0.30 0.8 §0. 41 0.45 § 0.09
10 0.28 § 0.28 0.28 § 0.19 0.62 § 0.12
11 0 0 0.45 § 0.05
12 0 0 0.5
13 0 0.50 § 0.50 0.6
14 0 0.50 § 0.50 0.5123

244 Anim Cogn (2010) 13:239–248p < 0.01, Fig. 2a). For rhesus macaques, we found that
mean frequency of back-glances diVered according to the
number of joiners (Kruskall-Wallis test, H = 83.6, df = 14,
p < 0.00001). The Wrst departed individual displayed more
back-glances when no individual had joined the movement
than when 1 to 9 individuals joined it (Dunn’s multiple
comparison test, p < 0.01, Fig. 2c). When it was not joined,
the Wrst departed individual displayed 83% of its back-
glances in Tonkean macaques and 92% in rhesus macaques.
Pauses
The mean frequency of pauses and the number of joiners
were not correlated in Tonkean macaques (N = 10,
rs = ¡0.38, p = 0.248, Fig. 2b) whereas these were nega-
tively correlated in rhesus macaques (N = 15,
rs = ¡0.89, p = 0.0002, Fig. 2d). However, we found in
Tonkean macaques that mean frequency of pauses
diVered according to the number of joiners (Kruskall-
Wallis test, H = 72.2, df = 9, p < 0.00001). Indeed, the
Wrst departed individual displayed more pauses when no
individual had joined the movement than when 2 to 8
individuals had joined it (Dunn’s multiple comparison
test, p < 0.01, Fig. 2b). In rhesus macaques, mean fre-
quency of pauses diVered according to the number of
joiners (Kruskall-Wallis test, H = 107.7, df = 14,
p < 0.00001). The Wrst departed individual displayed
more pauses when no individual had joined the move-
ment than when 1 to 13 individuals had joined it (Dunn’s
multiple comparison test, p < 0.05, Fig. 2d). When it
was not joined by any individuals, the Wrst departed indi-
vidual displayed 50% of pauses in Tonkean macaques
and 90% in rhesus macaques. This result seems to show
that the Wrst departed individual might want to be joined
and that pauses may be used to recruit and/or to wait for
group-mates.
The link between the number of behaviours of the Wrst
departed individual and the number of joiners may be due
to an inXuence of the time (the more elapsed time, the more
the Wrst departed individual can display behaviours and the
more the other individuals can join the movement). How-
ever, the number of joiners was not correlated to the dura-
tion of a collective movement in Tonkean macaques
(Spearman rank correlation, N = 10, rs = 0.333, p = 0.347)
nor in rhesus macaques (N = 15, rs = 0.482, p = 0.058).
This result suggests that the behaviours of the Wrst departed
individual probably have a direct inXuence on the number
of joiners.
The relationship between the mean frequencies of pauses
and back-glances displayed by the Wrst departed individual
and the number of joiners is not linear (Fig. 2a–d). More-
over, the Wrst departed individual appeared to stop display-
ing these behaviours after 2–3 group members have joined.
A curve estimation test shows that the best predictor of
observed curve is an inverse curve for behaviours both in
Tonkean macaques (back-glances: R2 = 0.90, df = 9,
p < 0.00001; pauses: R2 = 0.89, df = 9, p < 0.00001) and
rhesus macaques (back-glances: R2 = 0.92, df = 14,
p < 0.00001; pauses: R2 = 0.73, df = 14, p < 0.0007). If the
curve would be linear, this may suggest that the Wrst
departed individual wanted to recruit/to wait all group
members. However, as the curve was not linear, it seems
that the Wrst departed individual did not recruit/wait for the
whole group but only for some individuals.
Fig. 2 Mean number of back-
glances and of pauses per collec-
tive movement of the Wrst de-
parted individual according to
the number of joiners. a, b Tonk-
ean macaques; c, d Rhesus
macaques123

Anim Cogn (2010) 13:239–248 245Did the Wrst departed individual modify its behaviour
according to the number of joiners?
We checked whether the frequency of pauses decreased
after a back-glance according to the number of joiners in
the movement. Indeed, we believed that the Wrst departed
individual used back-glances to monitor conspeciWcs and
thus estimate the number of joiners, whereas it used pauses
as an encouragement for them to join, i.e. to recruit them.
According to this assumption, the number of pauses after a
back-glance would decrease with the number of joiners
while the number of back-glances after a pause would not
decrease with this number. An alternative explanation
could be that these behaviours reXected internal motiva-
tional state of the Wrst departed animal, like a hesitation or
an uncertainty for going alone. According to this assump-
tion, we would predict that both the number of pauses after
a back-glance and the number of back-glances after a pause
should decrease with the number of joiners.
Back-glances were not displayed always. As mentioned
in the previous section, the Wrst departed individual seemed
to stop emitting signals after the joining of 2–3 joiners to
the movement. They occurred only when there were 0, 1, 2,
4, 6, 7 and 8 joiners in Tonkean macaques (N = 7) and for
0, 1, 2, 4 and 7 joiners in rhesus macaques (N = 5). The fol-
lowing analysis will be conducted on these numbers. We
checked whether the absence of signals for 3 and 5 joiners
was due to an identity eVect of the Wrst departed individual,
of the 3rd or of the 5th joiner. Results showed that the
majority of individuals occupied each of these ranks and
that there was no diVerence between individuals in both
Tonkean macaques (Chi square test, df = 10, �² · 6.810,
p ¸ 0.500) and rhesus macaques (Chi square test, df = 14,
�² · 15.532, p ¸ 0.353).
Pauses after a back-glance
The frequency of pauses after a back-glance decreased with
the number of joiners in Tonkean macaques (N = 7,
rs = ¡0.78, p = 0.038) and in rhesus macaques (N = 5,
rs = ¡0.89, p = 0.04).The mean number of pauses after a
back-glance is reduced by half when one individual has
joined the movement (whatever the species) and was nil
when there were 6 joiners in Tonkean macaques and 7 join-
ers in rhesus macaques.
Back-glances after a pause
To ensure that the relationship between pauses and number
of joiners was not an artefact due to a link with the duration
of movement, we tested if the converse conWguration i.e.
frequency of back-glances after a pause and the number of
joiners were also correlated. Such correlation was not found
in Tonkean macaques (Spearman rank correlation, N = 10,
rs = ¡0.43, p = 0.208, pauses were displayed for any num-
ber of joiners), and in rhesus macaques (N = 7, rs = ¡0.05,
p = 0.806, pauses were only displayed for 0, 1, 2, 3, 4, 7
and 8 joiners). The mean number of back-glances after a
pause was 0.13 § 0.06 from 0 to 8 joiners in Tonkean
macaques and 0.59 § 0.19 from 0 to 7 joiners in rhesus
macaques.
From these results, we suggested that the Wrst departed
individual used back-glances to monitor the number of
joiners and then adapted its number of pauses according to
this number or more particularly according to the presence
of speciWc individuals (kin-related or aYliated) among
these joiners instead of only waiting its conspeciWcs.
Did the Wrst departed individual recruit speciWc group
members?
When monitoring its group-mates, the Wrst departed indi-
vidual may not only monitor the number of joiners but also
their identities. In the following section, the identities of
participants are considered. We assessed if the relationships
a Wrst departed individual a had with a joiner b inXuenced it
restarting after a pause. During a pause of a, if an individual
b joins the movement, a can restart or stay in pause. For
each a–b dyad, we scored the number of times a Wrst
departed individual restarted after a joining (n1) and the
number of times it stayed in pause (n2). For both groups,
the matrix of the ratios n1/(n1 + n2)ab was compared to the
matrix of kinship and the matrix of aYliation using matri-
ces correlation tests (Hemelrijk 1990).
In Tonkean macaques, the matrix of the ratios n1/
(n1 + n2)ab correlated with the matrix of aYliation
(Kr = 0.45, p = 0.0004) but not with the one of kinship
(Kr = 0.21, p = 0.087). Conversely, in rhesus macaques, the
matrix of the ratios n1/(n1 + n2)ab correlated with the
matrix of kinship (Kr = 0.28, p = 0.004) but not with the
matrix of aYliation (Kr = ¡0.15, p = 0.593).
These results conWrm that the Wrst departed individual
speciWcally recruited and/or waited for some individuals,
the highly aYliated ones in Tonkean macaques and the kin-
related ones in rhesus macaques. Thus, it ceased its waiting
and/or its recruitment as soon as these particular individuals
had joined.
Discussion
Our study was conducted in semi-free ranging conditions,
where the visibility was higher and inter-individual dis-
tances lower than in natural conditions (Judge and de Waal
1997). Animals might thus rely only on visual signals
(Gros-Louis 2004; Mitani and Nishida 1993). This may123

246 Anim Cogn (2010) 13:239–248explain why we did not hear any loud calls in our studied
group contrary to Riley (2005), who reported the use of a
‘loud call’ to initiate group movements and keep cohesion
in Tonkean macaques. In both groups, results seemed to
show that the Wrst departed individual seemed to use pauses
to recruit its conspeciWcs. Another explanation could be
that pauses reXected internal motivational state of the Wrst
departed animals, such as hesitation, uncertainty or solely
waiting for its conspeciWcs. On the other hand, Wrst
departed individuals seemed to use back-glances to monitor
the number and/or the identity of joiners. The use of these
behaviours is also similar for other species (chimpanzees,
Menzel 1971; white-faced capuchins, Leca et al. 2003;
Meunier et al. 2007; hyenas (Crocuta crocuta), Holekamp
et al. 2000) and in another group of Tonkean macaques
(Sueur and Petit 2008a).
The Wrst departed individual seemed to modify its num-
ber of pauses according to the number of joiners evaluated
by monitoring. The more the Wrst departed individual dis-
played pauses, the more numerous were the joiners. The
Wrst departed animal might pause because it could feel
reluctant to go alone and pauses could express animal’s
uncertainty; when other individuals joined the movement,
the uncertainty of the Wrst departed individual probably
decreased and it displayed fewer pauses. However, the
duration of a collective movement did not depend on the
number of joiners. This result suggests that the behaviours
of the Wrst departed individual may have a direct inXuence
on the number of joiners and that making a pause does not
mean merely waiting but is certainly a cue in itself for
joiners. This result does not imply that the Wrst departed
individual should be conscious of the eVect of its pause. In
a second step, the Wrst departed individual diminished its
number of pauses. This feedback loop favoured group
coordination. Sueur and Petit (2008a) suggested that the
speed of the Wrst departed individual could be a recruit-
ment signal, as its intensity was positively correlated to the
joiners’ number. In the same way, Leca et al. (2003) found
that a low speed in white-faced capuchins favoured the
joining of group members. However, in the present study,
the speed of the Wrst departed individual was not higher
than the one of other group members, a result already
found by Meunier et al. (2007) for white-faced capuchins.
It has been suggested that a high speed of movement of an
individual may rather be a cue of its goal-directed-move-
ment or of its motivation (Altmann and Altmann 1974;
Garber 1988; Noser and Byrne 2007; Pochron 2001; Sigg
and Stolba 1981) than a real recruitment signal, even if
speed seemed to favour the joining process. Indeed, Tonk-
ean macaques are able to use cues conveyed by group-
mates to localize food sources (Chauvin and Thierry 2005;
Drapier et al. 2002; Ducoing and Thierry 2004) and may
use speed as a simple cue.
We showed that pause seemed to be a cue for joiners but
from the Wrst departed individual’s point of view, a pause
may be a recruitment signal or the expression of its uncer-
tainty. Nevertheless, we found that the Wrst departed indi-
vidual ceased to display pauses when some particular
individuals had joined. This Wnding seemed to go beyond
the uncertainty hypothesis. If the Wrst departed individual
hesitated to go alone, then it should cease emitting pauses
when joined whatever the identities of the joiners might be.
However, it stopped displaying pause solely when some
speciWc individuals joined it. According to this result, we
suggested that pause would be more a recruitment signal
than uncertainty index.
Recruitment may be a mechanism as simple as a thresh-
old function, dependent on the number of joiners. However,
we found that the recruitment process was not only depen-
dent on the joiners’ number but also on their identities.
Indeed, the Wrst departed individual seemed willing to
recruit mostly kin-related individuals in rhesus macaques
and highly aYliated ones in Tonkean macaques and
stopped displaying signals when this goal was reached.
This diVerence between rhesus and Tonkean macaques reX-
ects their diVerent social styles (de Waal and Luttrell 1989;
Thierry 2007). Rhesus macaques are more nepotistic than
Tonkean macaques, as found in many of their daily interac-
tions (Thierry 2004). As a consequence, rhesus macaques
formed kin-related sub-groups during collective move-
ments contrary to Tonkean macaques, for which associa-
tions during collective movements are based on aYliative
relationships (Sueur and Petit 2008b). Such inXuence of
social style is also found in the current study.
Tomasello and Call (1997) deWned behaviour as inten-
tional if it implies a goal and some Xexibility in the means
for attaining it. Ducoing and Thierry (2003) found such
Xexibility in Tonkean macaques, where informed subordi-
nate individuals used tactical manoeuvres in order to
reach a food source alone. Flack and de Waal (2007)
found a similar result with context modulating domi-
nance-related signal meaning in pig-tailed macaques
(Macaca nemestrina). In the same way, loud calls are
used to initiate movements in wild groups (Riley 2005)
and when a pig-tailed macaque mother used the pucker
behaviour to encourage its infant to join it, this behaviour
has also been considered as intentional (Maestripieri
1996a, b). In this study, we suggested that the Wrst
departed individual used pauses to recruit speciWc group
members. We previously reported that when not joined,
the Wrst departed individual went back to the group and
started a new start attempt (Sueur and Petit 2008a). More-
over, Tonkean and rhesus macaques seemed to show their
intention to move. Indeed, they indicated with their body
position the direction in which they were willing to go
before the departure of a collective movement (Sueur and123

Anim Cogn (2010) 13:239–248 247Petit 2008a). So, macaques seemed to use diVerent signals
to recruit other group members: loud calls, pucker behav-
iour, intention movements, a new start attempt and maybe
pauses. We may suggest that these behaviours are inten-
tional (Tomasello and Call 1997). We are aware that our
results came from two semi-free ranging groups and that
further observations or experiments are needed to test the
intentionality of this kind of behaviours in macaques.
However, these conditions were essential to record the
behaviour of each individual during observation sessions.
Moreover, comparing two groups of two diVerent species
in the same environmental conditions allowed us to Wnd
similar rules explaining group cohesion during collective
movements and gave robustness to our Wndings. This fact
is corroborated by the interspeciWc diVerences we found
in the identity of recruited congeners. Such diVerences are
easily understandable by considering social styles of both
species, as has been previously shown for conciliatory
tendencies (Thierry et al. 2008), social play (Petit et al.
2008) and many other social behaviours (Thierry et al. 2004).
Acknowledgments The authors are grateful to J. Dubosq, V. Wyss,
H. Roger-Bérubet and A. Coulon for their help, P. Uhlrich, for techni-
cal assistance, N. Poulin for statistical advices and R. Knowles for En-
glish corrections. This work was supported by the French Research
Ministry (EGIDE), the French Foreign Ministry (Lavoisier Excellence
Scholarship) and the European Doctoral College of Strasbourg Univer-
sities. Thanks are extended to J. L. Deneubourg and B. Thierry for sci-
entiWc discussions. These experiments comply with the current laws of
the country in which they were performed.
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