Int J Primatol (2007) 28:801–817
DOI 10.1007/s10764-007-9162-4
Social Aspects of Fur-rubbing in Cebus
capucinus and C. apella
Jean-Baptiste Leca & Noëlle Gunst & Odile Petit
Received: 16 June 2005 / Revised: 20 January 2006 / Accepted: 9 June 2006 /
Published online: 7 August 2007
# Springer Science + Business Media, LLC 2007
Abstract Capuchins rub particular plant materials into their pelage, a behavior for
which most authors have proposed a medicinal function (Baker in American Journal of
Primatology 38:263–270, 1996, Baker, M. (1998). Fur Rubbing as Evidence for
Medicinal Plant Use by Capuchin Monkeys (Cebus capucinus): Ecological, Social,
and Cognitive Aspects of the Behavior. Dissertation thesis. University of California
Riverside; DeJoseph et al. in Journal of the American Academy of Dermatology
46:924–925, 2002). Individuals fur-rub solitarily or in groups, but researchers have not
conducted studies to understand the differences. We investigated the link between the
form of fur-rubbing and other social variables in 2 capuchin species. We supplied 2
captive groups —white-faced capuchins and tufted capuchins— with citrus fruit and
onions and explored the behavioral processes and social aspects underlying the
activity. We documented the occurrence, number of participants, and effect of
recruitment behaviors in fur-rubbing subgroups. We investigated the role of kinship,
affiliation, and dominance relationships in accounting for fur-rubbing groups. There is
a significant difference in the form of fur-rubbing between white-faced and tufted
capuchins. White-faced capuchins fur-rubbed mainly in subgroups and performed a
particular behavior to recruit prospective participants, whereas tufted capuchins furrubbed mainly alone, and showed no particular motivation to be joined by other group
members. White-faced capuchins could fur-rub together frequently, whatever their
degree of kinship, affiliation, or dominance interval. In tufted capuchins, fur-rubbing
appeared to be significantly affected by kinship and dominance.
Keywords capuchins . covariation . fur-rubbing . social organization
J.-B. Leca : O. Petit (*)
Ethologie des Primates, Département Ecologie, Physiologie et Ethologie, Institut Pluridisciplinaire
Hubert Curien, UMR 7178 CNRS ULP, 67087 Strasbourg cedex 2, France
e-mail: [email protected]
N. Gunst
Institute of Ecology, University of Georgia, Athens GA 30602–2202, USA
802
J.-B. Leca, et al.
Introduction
Some wild and captive primate species apply or rub various odoriferous or pungent
materials or arthropods into their pelage. Depending on whether they use plant materials
(fruit, leaves, or stems), peat, millipedes, or ants, the behavior is referred to as furrubbing (Baker 1996, 1998; Campbell 2000, Quinn 2004), peat-bathing (Ludes and
Anderson 1995), self-anointing (Birkinshaw 1999; Valderrama et al. 2000; Zito et al.
2003; Evans et al. 2004), or anting (Longino 1984; Falotico et al. 2004), respectively.
Researchers have mentioned ≥4 hypotheses to explain fur-rubbing in primates (cf.
Baker 1996, 1998; Campbell 2000). 1) Fur-rubbing may be a form of medicinal plant
use, like leaf-swallowing in chimpanzees (Huffman et al. 1996). The pharmacological
properties of the plants used are supposed to deter or remove ectoparasites and
condition the fur (DeJoseph et al. 2002). 2) Fur-rubbing may be a form of group scentmarking behavior, just as urine-washing or fecal-marking presumably are in some
primate species (Ueno 1991). 3) Given that several individuals sometimes interact with
each other while fur-rubbing, the behavior may reinforce social bonds, and could be a
form of social convention like handclasp grooming in chimpanzees (McGrew and
Tutin 1978) or handsniffing in white-faced capuchins (Perry et al. 2003). 4) The
capuchins may simply enjoy the interaction with the plant material, and apparent
pleasurable feedback potentially gained from the activity may be an immediate
reinforcement.
Most studies on the topic focused on the first hypothesis. Researchers considered
rubbing pungent material into fur to be mainly for its medicinal benefits (Baker 1996;
DeJoseph et al. 2002; Ludes and Anderson 1995; Valderrama et al. 2000). The only
source of behavioral variation they studied was the type of plant material selected for
fur-rubbing (Baker 1997, 2000). In capuchins, social fur-rubbing occurred, with ≥2
individuals in physical contact during fur-rubbing episodes (Quinn 2004), and ≤10
participants huddled together while performing the behavior (Baker 1996; Ludes and
Anderson 1995). However, little is known about the possible proximate mechanisms
that may underlie the form of the behavior. Until now, no one investigated the
behavioral processes, social factors, and possible social function of fur-rubbing in
capuchin groups. Though all capuchin species (Cebus spp.) engage in fur-rubbing,
researchers have conducted no interspecific comparison.
White-faced capuchins (Cebus capucinus) and tufted capuchins (C. apella) are
different in their social organizations. White-faced capuchins are a highly social
species, characterized by strong affiliative bonds and cooperative relationships during
hunting (Perry 1996; Rose 1997). Individuals show a high rate of bidirectional
aggression and intense conciliatory behaviors (Leca et al. 2002; Perry 1998; Rose
1994). According to the studied troops, relationships among males are qualified
neutral, tolerant, or highly affiliative (Jack 2003). Males are protective toward infants
(Rose 1994), and α-males show relative tolerance of other males having access to
females (Fedigan 1993). While foraging, white-faced capuchins tend to be tolerant of
the close proximity and even body contact with group members. An individual may
even touch and sniff the food being processed by another group member (Panger et al.
2002; Perry and Rose 1994). As for the decision-making process underlying initiation
of group movement, leadership is not concentrated on a single high-ranking
individual. White-faced capuchins show distributed leadership: any individual could
Fur-rubbing in 2 Cebus spp.
803
initiate group travels regardless of their age, sex, and dominance status (Boinski 1993;
Boinski and Campbell 1995; Leca et al. 2003).
By contrast, proper long-term studies on the social organization of tufted capuchins
are lacking. They seem to have a more rigid social organization, even though authors
have different opinions about its rigidity (Izawa 1980; Janson 1986a,b; van Schaik and
van Noordwijk 1989; Welker et al. 1990). Like white-faced capuchins, tufted
capuchins show interindividual tolerance. However, in the latter, social interactions
are more conditioned by dominance relationships, and affiliative bonds are less evenly
distributed among all group members. In tufted capuchins, social interactions are better
explained by the similarity principle (cf. de Waal 1991; de Waal and Luttrell 1986):
individuals of similar age, sex, and dominance rank spend a lot of time grooming,
playing, and supporting one another during conflicts and therefore may reach similar
rank (Parr et al. 1997). Tufted capuchins are characterized by the central role of the
higher-ranking male, which is the main recipient of grooming bouts, which may
aggressively control access to resources, and whose behavior is closely monitored by
other group members (Di Bitetti 1997; Janson 1985, 1990).
Marked differences also occur between tufted capuchins and white-fronted
capuchins (Cebus albifrons) in foraging strategies, mating behaviors, social
interactions, and dominance hierarchies (Janson 1986a, b). However, researchers
have not investigated a possible covariation among social variables in Cebus.
Researchers have demonstrated covariation only in macaques, finding, via the
comparative method, similar differences in social organizations in most macaque
species. In Macaca, there is covariation among many social variables, such as the
form of aggressive and postconflict interactions, strictness of dominance hierarchy,
and group cohesiveness (Petit et al. 1997; Thierry 2000; Thierry et al. 1997). For
example, the emergence of cooperation in an instrumental task has been possible in a
tolerant species such as Tonkean macaques (Macaca tonkeana) while the strictness
of the dominance prevent 2 rhesus macaques (M. mulatta) from being present on the
same spot simultaneously and hence keeping cooperative behaviors from emerging
(Petit et al. 1992). The characteristics of the social organizations are likely to
condition the contrasting behavioral styles of macaques (Thierry 1990, 2000, 2004).
To our knowledge, we are first to investigate the link between the form of furrubbing and other social variables in 2 capuchin species.
Because fur-rubbing can involve close interactions among several partners, we
assumed that the behavior can reflect social cohesion in capuchins. Our objective
was to examine covariation between the form of fur-rubbing and different
sociodemographic variables, such as kinship, dominance, and affiliative relationships, in white-faced and tufted capuchins. White-faced capuchins exhibit social
dynamics conducive to a communal form of fur-rubbing, characterized by close and
intense interactions, distributed among all group members. By contrast, we expected
a rather solitary form of fur-rubbing in tufted capuchins, with an important influence
of dominance relationships. We collected data on fur-rubbing and social relationships
in the 2 capuchin species and tested the following 4 predictions: 1) fur-rubbing in
subgroups should be much more frequent than fur-rubbing alone in white-faced
capuchins, while the converse is expected in tufted capuchins; 2) fur-rubbing should
involve intense and effective recruitment behaviors in white-faced capuchins, i.e.,
behavioral patterns involving physical contacts and that result in longer social fur-
804
J.-B. Leca, et al.
rubbing episodes, whereas few, if any, recruitment behaviors are expected in tufted
capuchins; 3) when left alone after the departure of the last in-contact participant in a
fur-rubbing bout, the initiator should stop fur-rubbing quite rapidly in white-faced
capuchins, whereas it could continue for a long time in tufted capuchins; 4) in whitefaced capuchins, individuals should be able to fur-rub together, whether they are kin
or not, close-ranking or far-ranking, and strongly or poorly affiliated, whereas kin and
dominance relationships should be more important to account for fur-rubbing
subgroups in tufted capuchins.
Methods
Subjects and Housing
During the study, the group of white-faced capuchins contained 13 individuals of 3
separate lineages. There were 9 mother-offspring dyads and 16 dyads including
siblings, half-siblings, and grandmother-grandchildren. We sampled 3 adult males, 5
adult females (>5 yr), 2 immature males, and 3 immature females (2–5 yr). The
group of tufted capuchins —Cebus apella per Groves (2001; Fragaszy et al. 2004)—
contained 16 individuals of 3 separate lineages. There were 13 mother-offspring
dyads and 26 dyads including siblings, half-siblings, and grandmother-grandchildren. We sampled 3 adult males, 5 adult females, 3 immature males, and 5
immature females.
Both groups lived at the Primatology Center of the Louis Pasteur University,
Strasbourg, France. The white-faced capuchins were in a 1-acre outdoor park with
natural vegetation. A 25-m2 connected indoor compartment had concrete floor and
metal sitting perches. During observations, the group was outdoor and did not have
access to the indoor compartment. The tufted capuchins occupy a 70-m2 indooroutdoor enclosure with 3 compartments (a 40-m2 outdoor compartment, 30-m2 and
20-m2 indoor compartments). The enclosure contained wooden bars, platforms, and
chains. During observations, the monkeys were confined to the 40-m2 outdoor
compartment. For both groups, commercial primate pellets and water were available
ad libitum. Fresh fruit and vegetables were available to them once a week but not
during observations. Oranges were part of the weekly fruit diet, whereas we gave
subjects lemons and onions only very occasionally.
Procedure
Leca and Gunst carried out a series of video-recorded experiments between 0900 and
1200 h and between 1400 and 1700 h, from May to August 2001 for the white-faced
capuchins, and from February to May 2002 for the tufted capuchins. Because both
capuchin species showed different degrees of interest in the materials used to fur-rub (cf.
Baker 1996, 1997; Quinn 2004), we supplied them with 2 types of plant materials:
fruit of Citrus sp. (oranges and lemons) and bulbs of Allium sp. (onions), cut into
pieces. We provided citrus fruit in 35 sessions with white-faced capuchins and 9
Fur-rubbing in 2 Cebus spp.
805
sessions with tufted capuchins. We provided onions in 15 sessions with white-faced
capuchins and 9 sessions with tufted capuchins. From video recordings, we defined
fur-rubbing episodes in terms of sessions, bouts, and phases.
A fur-rubbing session is the time elapsed between plant material provisioning and
the moment that occurred 20 min after the last individual involved in fur-rubbing
stopped performing the behavior. A session generally consists of several fur-rubbing
bouts. A fur-rubbing bout started when an initiator began fur-rubbing. Several
partners might join the initiator, engage in social fur-rubbing, finally break up, and stop
fur-rubbing. If the same initiator started fur-rubbing again ≤1 min after breaking up, then
we considered the 2 episodes as a single bout. A bout may consist of several fur-rubbing
phases: periods of time during which the number of individuals involved in a fur-rubbing
subgroup remained unchanged. When an individual joined or left a fur-rubber or a furrubbing subgroup, a new phase began.
Data Analysis
To obtain directly comparable data, we drew lots for 9 sessions with citrus fruit and 9
sessions with onions in the sample of the white-faced capuchins. In the comparative
analysis, we used 9 sessions for each capuchin species and each plant species.
We ranked individuals >5 yr in a dominance hierarchy according to the direction of
avoidances and unidirectional aggressions. We quantified affiliation by the frequency
of body contacts among all identified group members recorded via instantaneous
sampling every 5 min (Altmann 1974). We collected 808 scans in each group, but not
during fruit provisioning. The surface of the physical environment was much larger
in white-faced than in tufted capuchins. Therefore, for the white-faced capuchins, we
collected scans only while the group was rather clumped in a particular area of the
outdoor park. The surface of the area is comparable with that of the indoor-outdoor
enclosure of the tufted capuchins. We assessed the affiliation score within each dyad
by the number of scans during which the 2 partners were in body contact.
Regarding the number of participants simultaneously involved in fur-rubbing
activity, we distinguished 4 types of phases (cf. Baker 1996): an individual fur-rubbed
alone, with no other group members involved in fur-rubbing (individual phases); an
individual fur-rubbed alone, not in physical contact with other group member(s)
involved in simultaneous fur-rubbing (solitary phases); an individual fur-rubbed in
body contact with another which was not involved the activity (accompanied
phases); ≥2 individuals, ≤9, fur-rubbed in contact with one another (social phases).
Likewise, we defined 4 types of bouts: individual bouts (including only individual
phases), solitary bouts (including ≥1 solitary phase, and possibly individual phases),
accompanied bouts (≥1 accompanied phase and no social phase), and social bouts
(≥1 social phase).
During preliminary observations of social fur-rubbing subgroups, we noticed that
capuchins sometimes coiled their semiprehensile tails around the body of other
participants while rubbing the plant material into their fur. We hypothesized that it
may result in recruiting group members for longer social fur-rubbing. To investigate
the level of motivation of the initiator of a fur-rubbing bout to be joined by other
participants, and to test a possible effect of recruitment of tail-coiling, we
Cebus apella
Citrus fruit
Cebus capucinus
Citrus fruit
Onion
Food item
Species
Individual
Solitary
Accompanied
Social (2 ind.)
Social (3 ind.)
Social (4 ind.)
Social (5 ind.)
Social (6–9 ind)
Total social (2–9 ind.)
TOTAL
Individual
Solitary
Accompanied
Social (2 ind.)
Social (3 ind.)
Social (4 ind.)
Social (5 ind.)
Social (6–9 ind)
Total social (2–9 ind.)
TOTAL
Individual
Solitary
Accompanied
Social (2 ind.)
Social (3 ind.)
Social (4 ind.)
Social (5 ind.)
Social (6–9 ind)
Total social (2–9 ind.)
TOTAL
Type bout/phase
10
17
11
16
4
5
8
4
37
75
30
16
5
3
5
1
0
0
9
60
8
0
1
0
0
0
0
0
0
9
61
39
48
98
70
46
32
27
273
454
76
18
14
12
7
1
0
20
0
128
8
0
1
0
0
0
0
0
0
9
2.9
8.9
15.4
25.2
11.3
24.3
25.7
36.4
122.9
150.2
14.9
17.1
6.6
3.4
11.0
3.0
0.0
0.0
17.4
56.0
3.5
0.0
0.2
0.0
0.0
0.0
0.0
0.0
0.0
3.7
19.1
21.8
11.8
36.7
18.7
13.0
9.8
10.4
88.6
141.3
22.5
18.0
3.8
3.1
2.3
0.4
0.0
0.0
5.8
50.2
3.5
0.0
0.2
0.0
0.0
0.0
0.0
0.0
0.0
3.7
Phases
Bout
Bout
Phases
Total duration (min)
Number
0.3
0.5
1.4
1.6
2.8
4.9
3.2
9.1
3.3
2.0
0.5
1.1
1.3
1.1
2.2
3.0
0.0
0.0
1.9
0.9
0.4
0.0
0.2
0.0
0.0
0.0
0.0
0.0
0.0
0.4
Bout
0.3
0.6
0.2
0.4
0.3
0.3
0.3
0.4
0.3
0.3
0.3
1.0
0.3
0.3
0.3
0.4
0.0
0.0
0.3
0.4
0.4
0.0
0.2
0.0
0.0
0.0
0.0
0.0
0.0
0.4
Phases
Mean duration (min)
0.2
0.4
0.9
1.0
1.3
1.2
0.9
4.3
2.2
1.8
0.4
1.0
0.5
0.9
1.6
0.0
0.0
0.0
1.3
0.8
0.3
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.3
Bout
0.2
0.5
0.2
0.3
0.2
0.2
0.2
0.3
0.2
0.3
0.2
0.9
0.2
0.2
0.3
0.0
0.0
0.0
0.3
0.3
0.3
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.3
Phases
SEM (min)
0.8/0.1
2.6/0.1
4.2/0.2
6.4/0.3
5.5/0.8
7.8/3.1
4.7/1.7
16.2/2.4
16.2/0.3
16.2/0.1
2.2/0.1
5.3/0.1
2.6/0.5
2.4/0.3
6.3/0.4
3.0/3.0
0.0/0.0
0.0/0.0
6.3/0.3
6.3/0.1
1.5/0.2
0.0/0.0
0.2/0.2
0.0/0.0
0.0/0.0
0.0/0.0
0.0/0.0
0.0/0.0
0.0/0.0
1.5/0.2
Bout
2.1/0.1
5.9/0.1
0.9/0.1
2.9/0.1
1.8/0.1
0.9/0.1
1.0/0.1
1.7/0.1
2.9/0.1
5.9/0.1
1.4/0.1
4.6/0.1
1.1/0.1
1.1/0.1
1.3/0.1
0.4/0.4
0.0/0.0
0.0/0.0
1.3/0.1
4.6/0.1
1.5/0.2
0.0/0.0
0.2/0.2
0.0/0.0
0.0/0.0
0.0/0.0
0.0/0.0
0.0/0.0
0.0/0.0
1.5/0.2
Phases
Range dur. (max/min)
Table I Number, total duration, mean duration, and duration range of fur-rubbing bouts and phases, according to the food items used in white-faced and tufted capuchins
806
J.-B. Leca, et al.
Onion
Individual
Solitary
Accompanied
Social (2 ind.)
Social (3 ind.)
Social (4 ind.)
Social (5 ind.)
Social (6–9 ind)
Total social (2–9 ind.)
TOTAL
27
27
45
4
0
0
0
0
4
103
95
72
98
5
0
0
0
0
5
270
15.3
34.2
161.6
56.4
0.0
0.0
0.0
0.0
56.4
267.4
80.8
111.3
63.1
2.5
0.0
0.0
0.0
0.0
2.5
257.7
0.6
1.3
3.6
14.1
0.0
0.0
0.0
0.0
14.1
2.6
0.9
1.5
0.6
0.5
0.0
0.0
0.0
0.0
0.5
1.0
0.5
1.2
3.0
12.0
0.0
0.0
0.0
0.0
12.0
2.7
0.8
1.3
0.5
0.3
0.0
0.0
0.0
0.0
0.3
0.9
2.2/0.1
6.4/0.1
20.1/0.1
38.1/0.7
0.0/0.0
0.0/0.0
0.0/0.0
0.0/0.0
38.1/0.7
38.1/0.1
6.5/0.1
10.4/0.1
5.7/0.1
1.0/0.1
0.0/0.0
0.0/0.0
0.0/0.0
0.0/0.0
1.0/0.1
10.4/0.1
Fur-rubbing in 2 Cebus spp.
807
808
J.-B. Leca, et al.
distinguished 2 types of fur-rubbing bouts, according to the behavioral patterns the
initiator performed when already fur-rubbing: 1) bouts during which the initiator
came into body contact with another group member and coiled its tail around its
body and 2) bouts during which the initiator merely came into body contact with
another group member but did not tail-coil. In both categories, we compared the
duration of body contact between the 2 partners.
Statistics
We conducted analyses via nonparametric statistical tests: Spearman rank correlation
coefficient test, Wilcoxon signed ranks test, Mann-Whitney U test, Kruskal-Wallis H
test, χ2 test with Yate’s continuity correction (Siegel and Castellan 1988). We tested
matrix correlations via Matman (de Vries et al. 1993). We set the number of automatic
permutations of matrices at 10,000 and used the Pearson’s correlation coefficient.
Results
We based the analysis of fur-rubbing on 135 bouts in white-faced capuchins and 112
bouts in tufted capuchins.
Food Item Preference When Fur-rubbing
When provided with citrus fruit, white-faced capuchins spent much more time furrubbing, and showed many more bouts and phases than tufted capuchins did (total
duration of fur-rubbing phases for all individuals=141.3 and 3.7 min, respectively;
total number of bouts=75 and 9, respectively; total number of phases=454 and 9,
respectively) (Table I). When provided with onions, tufted capuchins spent more time
fur-rubbing in more bouts and phases than white-faced capuchins did (total duration
of fur-rubbing phases for all individuals=257.7 and 50.2 min, respectively; total
number of bouts=103 and 60, respectively; total number of phases=270 and 128,
respectively). The longest fur-rubbing bout with citrus fruit lasted 16.2 min in whitefaced capuchins and only 1.5 min in tufted capuchins. The longest fur-rubbing bout
with onions lasted 38.1 min in tufted capuchins and 6.3 min in white-faced capuchins.
When fur-rubbing, white-faced capuchins showed a strong preference for citrus fruit,
whereas tufted capuchins highly preferred onions. Though both species exhibited a
preference in the plant material used, it did not affect significantly the general form of
fur-rubbing. White-faced capuchins performed social fur-rubbing involving >2
individuals with citrus fruit and onions. Tufted capuchins never performed social
fur-rubbing involving >2 individuals with both food items. We pooled the data on
both plant materials for the 2 species.
Duration of Fur-rubbing and Number of Participants
To distinguish quantitatively the social vs. nonsocial forms of fur-rubbing in both
species, we compared the total duration of fur-rubbing among the different types of
Fur-rubbing in 2 Cebus spp.
809
phases (Fig. 1). In white-faced capuchins, social phases pooled together were 6 times
longer than accompanied phases (94.4 vs. 15.7 min, respectively), and twice longer
than individual and solitary phases (94.4 vs. 41.6 and 39.8 min, respectively). The
maximum duration for individual phases was 2.1 min, 5.9 min for solitary phases,
and 1.1 min for accompanied phases. Social phases involved ≤9 partners and
presented a high turnover (495 phases in 157.7 min, 3.1 phases/min out of 55
accompanied and social bouts) because individuals joined or left a fur-rubber or a
fur-rubbing subgroup quite rapidly. There is a statistically significant difference in
the duration of the 4 types of bouts: individual, solitary, accompanied, and social
(Kruskal-Wallis H test: N1=40, N2=33, N3=16, N4=46, median=0.3, 0.3, 1.1, and
2.2 min, respectively, H=57.1, p<0.001). Multiple comparisons showed that
accompanied bouts lasted significantly longer than individual bouts, and social
bouts lasted significantly longer than individual or solitary bouts (p<0.05). The
longest social bout lasted 16.2 min and involved ≤9 individuals.
Considering the number of participants in social bouts, there are significant
differences in the duration of the following 8 bouts: individuals, solitary, accompanied,
social with 2, 3, 4, 5, and 6–9 individuals (Kruskal-Wallis H test: N1=40, N2=33, N3=
16, N4=19, N5=9, N6=6, N7=8, N8=4, median=0.3, 0.3, 1.1, 1.2, 1.9, 4.2, 3.5, and
8.9 min, respectively, H=66.7, p<0.001). Multiple comparisons showed that bouts are
individual or are significantly shorter than accompanied bouts and than social bouts
with 2, 3, 4, 5, and 6–9 individuals. Solitary bouts are significantly shorter than social
bouts with 4, 5, and 6–9 individuals (p<0.05). However, the duration of fur-rubbing
bouts did not increase significantly with the number of participants.
In tufted capuchins, solitary phases were twice longer than accompanied phases,
and longer than individual phases (111.6 vs. 63.3 and 84.3 min, respectively; Fig. 1).
The maximum duration for solitary phases was 10.4 min, 5.7 min for accompanied
phases, and 6.5 for individual phases. Social phases were virtually absent. In total,
Total duration of fur rubbing phases (min)
120,0
White-faced capuchin
Tufted capuchin
100,0
80,0
60,0
40,0
20,0
0,0
Individual
Solitary
Accompanied
Social (2 ind.)
Social (3 ind.)
Social (4 ind.)
Social (5 ind.) Social (6-9 ind.)
Type of phases
Fig. 1 Total duration of fur-rubbing according to the type of phase in white-faced and tufted capuchins.
810
J.-B. Leca, et al.
we recorded only 2.5 min of social phases, distributed as follows: 2 phases of 6 sec,
1 of 30 sec, 1 of 48 sec, and 1 of 1 min. Each of them involved only 2 partners, a fur
rubbing adult female in body contact with an immature individual. The turnover was
3 times lower than in white-faced capuchins (220 phases in 205.8 min, 1.1 phases/
min out of 38 accompanied and social bouts). We could not statistically compare the
duration of the 4 types of bouts because the social bouts were too few. However, the
very few times we observed social fur-rubbing, they were very long bouts (N=4,
median=8.8 min). There is a statistically significant difference in the duration of the
3 other types of bouts: individual, solitary, and accompanied (Kruskal-Wallis H test:
N1=35, N2=27, N3=46, median=18 sec, 30 sec, and 1.8 min, respectively, H=27.5,
p<0.001). Multiple comparisons showed that accompanied bouts lasted significantly
longer than individual or solitary bouts did (p<0.05).
Recruitment Process in Fur-rubbing
Body contact with another group member occurred in 10% of bouts (14 of 135
bouts) in white-faced capuchins, and in no bout (0 of 103 bouts) in tufted capuchins.
Coiling the tail around the body of another group member occurred in 20% of bouts
(27 of 135 bouts) in white-faced capuchins, and no bout (0 of 103 bouts) in tufted
capuchins. In all accompanied and social fur-rubbing bouts in tufted capuchins, the
initiator never came into body contact with others. Instead, another group member
joined the initiator.
To quantify a possible recruitment effect of tail coiling in white-faced capuchins
we considered randomly 10 fur-rubbing bouts during which the initiator coiled its
tail around another group member and 10 bouts when the initiator did not. We
compared in both categories, the duration of body contact between the 2 partners.
The behavior correlates significantly with an increase in the duration of body contact
(Mann-Whitney U test: N1=N2=10, median=1.2 min and 12 sec, respectively; U=
7.5, p=0.001). The result showed that the behavior consisting of coiling the tail
around the body of another group member can be considered a method of prolonging
social fur-rubbing activity in white-faced capuchins. One could argue that tail-coiling
is less about recruitment per se, and more about the quality of the social relationship
between 2 partners. We compared the affiliation scores among dyads that performed
tail-coiling vs. dyads that performed only body contact. There is no significant effect
of affiliation on tail-coiling (Mann-Whitney U test: N1=23, N2=12, medians=20.2
and 20.0, respectively; U=135.5, p=0.930).
To assess the motivation of the initiator to continue fur-rubbing when it remains
the only one performing it, we compared in each capuchin species, 2 types of furrubbing durations: 1) the duration of the initiator’s fur-rubbing before the last
individual in body contact with him had stopped fur-rubbing and left and 2) the
duration the initiator’s fur-rubbing after the departure of the last in-contact individual.
There is a significant difference in both species (white-faced capuchins: first duration
mean ± SEM=1.8±1.3 min, second duration mean=18±12 sec, Wilcoxon signed ranks
test, N=27, Z=−4.4, p < 0.001; tufted capuchins: first duration mean±SEM=6.0±
5.1 min, second duration mean=1.6±1.2 min, Wilcoxon signed ranks test, N=20, Z=
−2.4, p=0.014). There is an effect of the departure of the last in-contact
individual on the duration of fur-rubbing of the initiator left alone. However,
Fur-rubbing in 2 Cebus spp.
811
the effect is stronger in tufted capuchins than in white-faced capuchins. There is
a statistically significant difference between the 2 capuchin species in the mean
duration of the initiator’s fur-rubbing activity after the departure of the last incontact individual (χ2 test: N1=27, N2=20; mean=0.3 and 1.6 min, respectively;
χ2 =12.8, p<0.001). After the departure of the last individual, the initiator
continued to fur-rub alone significantly longer in tufted capuchins than in whitefaced capuchins.
The results are consistent with the fact that the recruitment process in fur-rubbing
was much more important in white-faced than in tufted capuchins.
Effect of Sociodemographic Variables on the Duration of Fur-rubbing
Age We compared the duration of fur-rubbing according to 2 age classes (immature
and adult). There is no significant difference in white-faced capuchins (MannWhitney U test: N1=5, N2=8, median=38.6 and 26.2 min, min/max=21.5/56.6 and
12.8/61.6 min, respectively; U=10.0, p=0.171) or in tufted capuchins (N1=N2=8,
median=0.6 and 2.0 min, min/max=0.0/19.7 and 0.0/113.6 min, respectively; U=
25.5, p=0.505).
Sex We compared the duration of fur-rubbing according to sex. There is no significant
difference between males and females in white-faced capuchins (Mann-Whitney U test:
N1=5, N2=8, median=32.1 and 23.9 min, min/max=26.1/61.6 and 12.8/56.6 min,
respectively; U=12.5, p=0.284) or in tufted capuchins (N1=6, N2=10, median=1.2
and 1.3 min, min/max=0.0/19.7 and 0.0/113.6 min, respectively; U=28.0, p=0.875).
Kinship We investigated whether kinship could favor body contact in fur-rubbing
subgroups. We assessed the degree of closeness in maternal kin relationships by
distinguishing 3 types of dyads: nonkin, far kin (siblings, half-siblings, and
grandmother-grandchildren), and close kin (mother-offspring) dyads. We tested the
effect of kinship closeness on the duration of accompanied and social fur-rubbing.
In a first matrix, we implemented the degree of kinship in the 3 types of kin
dyads. In a second matrix, we entered for each dyad the duration of presence in
the same fur-rubbing subgroups. There is a significant positive correlation in tufted
capuchins (Pearson’s correlation coefficient=0.269, p=0.004). Close-kin dyads
spent more time fur-rubbing in body contact than far-kin dyads did, and the 2 types
of dyads spent more time fur-rubbing in contact than nonkin dyads did (mean ±
SEM=1.1±1.1 min, 12±12 sec, and 6±6 sec, respectively). There is no significant
correlation in white-faced capuchins (Pearson’s correlation coefficient=0.153,
p=0.126).
Hierarchical rank We carried out hierarchical rank order analysis with the aid of
Matman, (de Vries et al. 1993). We verified the linearity of the dominance hierarchy,
h′=1.00 (p<0.001) for the white-faced capuchins, and h′=0.98 (p<0.001) for the
tufted capuchins (cf. de Vries 1995). We compared the duration of fur-rubbing
according to hierarchical rank. There is no significant correlation in white-faced
capuchins (Spearman rank correlation coefficient test: N=8, Rs =−0.395, p=0.333)
or in tufted capuchins (N=8, Rs =0.386, p=0.346).
812
J.-B. Leca, et al.
Dominance interval We investigated whether dominance interval could influence
body contact in fur-rubbing subgroups. We distinguished 2 types of dyads according
to the dominance interval between 2 partners: close-ranking dyads (dominance
interval=1–3, N1=18 for both groups) and far-ranking dyads (dominance interval=
4–7, N2=10 for both groups). In a first matrix, we implemented the dominance
interval within each dyad. In a second matrix, we entered for each dyad, the duration
of presence in the same fur-rubbing subgroups. There is no significant correlation in
white-faced capuchins (Pearson’s correlation coefficient=−0.214, p=0.124). Conversely, there is a significant correlation in tufted capuchins (Pearson’s correlation
coefficient=−0.294, p=0.048). For both species, the mean duration of presence in
the same fur-rubbing subgroups was superior in close-ranking dyads than in farranking dyads (Fig. 2). However, the difference is significant only in tufted
capuchins.
Affiliation Out of 808 scans, we recorded 2629 body contacts in the white-faced
capuchins and 671 in the tufted capuchins. Individual frequency of body contact is 5
times superior in white-faced capuchins (0.25 body contact/individual/scan) than in
tufted capuchins (0.05 body contact/individual/scan). Based on dyads, body contacts
are significantly more frequent in white-faced than in tufted capuchins (MannWhitney U test: N1=78, N2=120, median=30 and 1, respectively; U=729.0, p<
0.001).
From the contrasted results between the 2 groups, we distinguished 3 types of dyads
according to the affiliation score: poorly affiliated dyads (white-faced capuchins:
affiliation score=2–19, N1=24; tufted capuchins: affiliation score=0, N1=46),
moderately affiliated dyads (white-faced capuchins: affiliation score=20–40, N2=27;
tufted capuchins: affiliation score=1–10, N2=28), and strongly affiliated dyads
(white-faced capuchins: affiliation score=41–100, N3=27; tufted capuchins: affiliation
score=11–56, N3=20). We investigated whether affiliation score could influence body
7
close-ranking
far-ranking
Mean duration of presence in the same
fur-rubbing subgroups (min)
6
5
4
3
2
1
0
white-faced capuchins
tufted capuchins
Fig. 2 Effect of dominance on the duration of presence in the same fur-rubbing subgroups. *p<0.05.
Fur-rubbing in 2 Cebus spp.
813
contact in fur-rubbing subgroups. In a first matrix, we implemented the affiliation
score within each dyad. In a second matrix, we entered for each dyad, the duration of
presence in the same fur rubbing subgroups. Though there is no statistically significant
result in either species, the positive correlation in tufted capuchins approaches
statistical significance (white-faced capuchins: Pearson’s correlation coefficient=
0.139, p=0.116; tufted capuchins: Pearson’s correlation coefficient=0.188, p=
0.064). In tufted capuchins, strongly affiliated dyads tended to fur-rub together longer
than moderately or poorly affiliated dyads.
Discussion
There is a significant difference in the form of fur-rubbing between white-faced and
tufted capuchins, which confirms our predictions. White-faced capuchins spent much
more time fur-rubbing in subgroups than alone. Fur-rubbing subgroups involved 2–9
partners and had a high participant turnover. In 30% of cases (41 out 135 bouts), the
initiator of a bout tried to recruit more partners by entering into body contact with
prospective participants or coiling its tail around their bodies. The latter seemed to be
effective in the recruitment of additional fur-rubbers. When left alone, the initiator
stopped fur-rubbing quite rapidly. Conversely, tufted capuchins mainly fur-rubbed
alone. About 75% of the actual time spent fur-rubbing involved individual or solitary
phases. Occasionally, another individual might enter and simply stay in body contact for
a while with the only fur-rubber (24% of the total duration spent fur-rubbing). Furrubbing subgroups were very seldom seen (5 out of 279 phases), lasted a very short
period of time (1% of the total time), and involved ≤2 partners. The initiator performed
no recruitment behavior, which could be regarded as a lack of motivation in being joined
by other participants. While fur-rubbing, the initiator sometimes avoided being
approached by other group members (personal observation). When left alone, the
initiator could continue fur-rubbing much longer than in white-faced capuchins.
The difference in the form of fur-rubbing (social vs. individual and solitary)
between the 2 capuchin species might be due to the physical properties of the food
item used. White-faced and tufted capuchins might be stimulated in different ways
by different plant substances. Citrus fruit are much juicier than onions, and it is
easier to spread its juice among fur-rubbers than perhaps the juice in most onions,
which could partly explain the fact that white-faced capuchins, which used mainly
citrus fruit, were much more social fur-rubbers than tufted capuchins, which used
principally onions. However, different plant materials can result in the same form of
fur-rubbing in a capuchin species. When using onions, white-faced capuchins
displayed social fur-rubbing (12 phases involving 2 participants, and 7 phases
involving 3 participants, and 1 phase involving 4 participants, which lasted 3.1, 2.4,
and 0.4 min, respectively). When using citrus fruit, the tufted capuchins never
displayed social fur-rubbing. Other reports showed that white-faced capuchins exhibit
social fur-rubbing via other materials, such as loose peat (Ludes and Anderson 1995).
In long-term observations at Raleighvallen, Suriname, wild tufted capuchins furrubbed alone, via rotten bamboo leaves; very occasional fur-rubbing subgroups
involved 2 individuals at the most (N. Gunst, pers. obs.). Second, one may not
814
J.-B. Leca, et al.
consider citrus fruit and onions so different in terms of pungency, stickiness, and
capacity to be sprayed and to stimulate the skin. Consequently, though the food items
the 2 capuchin species mainly used are not the same, they are unlikely to account for a
difference in the form of fur-rubbing.
Based on our data, we could not rule out a possible seasonal effect on the
observed differences in fur-rubbing between the 2 species. However, the following
arguments are not consistent with a major impact of weather conditions on the form
of fur-rubbing in capuchins. First, Baker (1996) showed an effect of the season on
the frequency (not the duration or the form) of fur-rubbing in wild white-faced
capuchins. Second, reports from the wild and the captivity suggested that the form of
fur-rubbing in tufted capuchins is in agreement with our results, even in hot weather.
In Raleighvallen, Suriname, individual fur-rubbing occurred during the rainy and the
dry seasons (S. Boinski, pers. com.). In a captive group of tufted capuchins in an
outdoor enclosure during summer in Southern California, individuals mainly furrubbed alone, and the very rare social fur-rubbing bouts (3 out of 260 bouts)
involved 2 participants at the most (Quinn 2004).
When considering the influence of social factors on the distribution of fur-rubbing
subgroups, our results showed that in tufted capuchins, close-kin and close-ranking
individuals fur-rubbed together much longer than far-kin, nonkin, and far-ranking
group members. Fur-rubbing subgroups were highly shaped by kinship, dominance,
and to some extent affiliation. In other words, we demonstrated that the individuals
that often interacted during fur-rubbing in tufted capuchins were also ones that share
close social relationships. By contrast, in white-faced capuchins, individuals were
able to fur-rub together frequently, whatever their degree of kinship, affiliation, or
dominance interval.
There seems to be a covariation between the form of rub-rubbing and some variables
of social organization in capuchins. White-faced capuchins had much more frequent
body contacts, in a general social context, than those of tufted capuchins. In white-faced
capuchins, affiliative postconflict behaviors appeared more frequent and more intense
than in tufted capuchins (Leca et al. 2002; Verbeek and de Waal 1997). Second, other
studies showed that white-faced capuchins are characterized by high levels of
interindividual tolerance in social interactions (Fedigan 1993; Perry 1996), protectiveness toward infants (Rose 1994), access to females (Fedigan 1993), feeding
competition (Phillips 1995; Rose 1994), food-sharing (Panger et al. 2002; Perry and
Rose 1994), and group movement organization (Boinski 1993; Boinski and Campbell
1995; Leca et al. 2003). By contrast, the social organization of tufted capuchins appears
less tolerant, more despotic, and mainly based on dominance relationships, including an
α-male with a pivotal role (Di Bitetti 1997; Janson 1985, 1990; Parr et al. 1997).
According to the findings, positive social interactions seem to be more frequent and
more distributed among all group members in white-faced capuchins than in tufted
capuchins. Consequently, one can characterize social relationships in white-faced
capuchins as more open and more tolerant than those of tufted capuchins. At least for
some particular behavioral patterns, white-faced capuchins may be more prone to
negotiation and social exchange than tufted capuchins. Via the comparative method,
researchers documented strong differences in social organizations in several macaque
species (Petit et al. 1997; Thierry 2000; Thierry et al. 1997). According to the
covariation hypothesis, there are numerous constraints liable to link the characters of a
Fur-rubbing in 2 Cebus spp.
815
social organization, and any significant variation in a single character induces a set of
correlated changes in the social organization (Thierry 2004). Likewise, in capuchin
species, the form of fur-rubbing appears to covary with some social variables. The social
form and distributed process of fur-rubbing in white-faced capuchins might be related to
their open social relationships and tolerant gregariousness. By contrast, the solitary form
of fur-rubbing and the roles of dominance and kinship during accompanied phases in
tufted capuchins could be connected to their less frequent and distributed positive
interactions, and their decision process mainly based on power asymmetry.
Like grooming, social fur-rubbing might reinforce social bonds (Baker 1996).
Given the difference in social styles between the 2 capuchin species, one can assume
that if social fur-rubbing can enhance social cohesion among group members, the
trait is more likely to evolve in white-faced than in tufted capuchins. We hypothesize
that social fur-rubbing might be a means to test the strength of social ties among
individuals in white-faced capuchins (cf. Zahavi 1977). First, it could account for the
high motivation of the initiator to be joined by other participants, and its low
motivation to continue fur-rubbing when left alone. Second, the fact that social furrubbing involves frequent turn-taking and role reversals makes the behavior a strong
candidate for testing the strength of social bonds. Third, Zahavi (1977) argued that
physical stress is a condition for the assessment of the strength of a social tie. An
individual that is not interested in testing the strength of the bond may not be ready
to sustain the stress, whereas one that is motivated to test and maintain the bond will
probably do so. Researchers recently have found odd behaviors in some troops of
wild white-faced capuchins, such as handsniffing, sucking body parts, and games
(Perry et al. 2003). They qualify as social conventions because they involve a certain
amount of risk to one or both protagonists, as in any social interaction, which is also
true in our study of fur-rubbing. Though conflicts often occurred among the
participants of fur-rubbing bouts (personal observation), several individuals risked
interacting in close physical contact for long periods of time. We can regard furrubbing in white-faced capuchins as a social index, a way to go thoroughly into the
quality of social relationships among group members. Our main conclusion is that
fur-rubbing might be part and parcel of the social behavioral repertoire in whitefaced capuchins but not in tufted capuchins.
Finally, to reach a comprehensive assessment of such specific differences, one
should consider not only mechanisms but also functional aspects of fur-rubbing. For
example, there might be differences in the type of ectoparasitical infections the 2
capuchin species experience. For self-medicative reasons, evolution may have
favored a social form of fur-rubbing in white-faced capuchins, whereas a more
individual or solitary form may have prevailed in tufted capuchins. However, further
dermatological analyses are needed to explore the issue.
Acknowledgments A fellowship from the Ministère de l’Education Nationale, de la Recherche, et de la
Technologie supported the work. During the preparation of the manuscript, a Lavoisier grant, Ministry of
Foreign Affairs, France supported J.-B. Leca; a grant from the National Science Foundation (BCS0352035) supported N. Gunst. We thank Camille Chandès, Sandra Colas, Nadia Daki, Pavine Lefebvre,
Hélène Meunier, and Delphine Penant for occasional assistance in data collection. We also thank Michael
A. Huffman for his fruitful suggestions, and 2 anonymous reviewers for their very constructive comments
on previous versions of the manuscript. We thank Sue Boinski and Josephine P. Quinn for providing
valuable information and Ana M. Ducoing for correcting the English.
816
J.-B. Leca, et al.
References
Altmann, J. (1974). Observational study of behaviour: Sampling methods. Behaviour, 49, 227–265.
Baker, M. (1996). Fur rubbing: Use of medicinal plants by capuchin monkeys (Cebus capucinus).
American Journal of Primatology, 38, 263–270.
Baker, M. (1997). Identification and selection of fur rubbing materials by white-faced capuchin monkeys
(Cebus capucinus). American Journal of Primatology, 42, 93.
Baker, M. (1998). Fur Rubbing as Evidence for Medicinal Plant Use by Capuchin Monkeys(Cebus
capucinus): Ecological, Social, and Cognitive Aspects of the Behavior. Dissertationthesis.University
of California Riverside.
Baker, M. (2000). Cognitive components of plant selection for fur rubbing in white-faced capuchin
monkeys, Cebus capucinus. American Journal of Primatology, 51, 39–40.
Birkinshaw, C. R. (1999). Use of millipedes by black lemurs to anoint their bodies. Folia Primatologica,
70, 170–171.
Boinski, S. (1993). Vocal coordination of group movement among white-faced capuchin monkeys, Cebus
capucinus. American Journal of Primatology, 30, 85–100.
Boinski, S., & Campbell, A. F. (1995). Use of trill vocalizations to coordinate troop movement among
white-faced capuchins: A second field test. Behaviour, 132, 875–901.
Campbell, C. J. (2000). Fur rubbing behavior in free-ranging black-handed spider monkeys (Ateles
geoffroyi) in Panama. American Journal of Primatology, 51, 205–208.
DeJoseph, M., Taylor, R. S. L., Baker, M., & Aregullin, M. (2002). Fur-rubbing behaviour of capuchin
monkeys. Journal of the American Academy of Dermatology, 46, 924–925.
de Vries, H. (1995). An improved test of linearity in dominance hierarchies containing unknown or tied
relationships. Animal Behavior, 50, 1375–1389.
de Vries, H., Netto, W. J., & Hanegraaf, P. L. H. (1993). Matman: A program for the analysis of
sociometric matrices and behavioural transition matrices. Behaviour, 125, 157–175.
de Waal, F. B. M. (1991). Rank distance as a central feature of rhesus monkey social organization: A
sociometric analysis. Animal Behavior, 41, 383–395.
de Waal, F. B. M., & Luttrell, L. M. (1986). The similarity principle underlying social bonding among
female rhesus monkeys. Folia Primatologica, 46, 215–234.
Di Bitetti, M. S. (1997). Evidence for an important social role of allogrooming in a Platyrrhine primate.
Animal Behavior, 54, 189–211.
Evans, S., Weldon, P., Giovanetti, J., Moody, C., & Vicaria, E. (2004). Anointing in owl monkeys. Folia
Primatologica, 75, 259.
Falotico, T., Verderane, M. P., Resende, B. D., Labruna, M. B., Izar, P., & Ottoni, E. B. (2004). Anting in a
semi-free ranging group of brown capuchin monkeys (Cebus apella). Folia Primatologica, 75, 372.
Fedigan, L. M. (1993). Sex differences and intersexual relations in adult white-faced capuchins, Cebus
capucinus. International Journal of Primatology, 14, 853–877.
Fragaszy, D. M., Visalberghi, E., & Fedigan, L. M. (2004). The Complete Capuchin: The Biology of the
Genus Cebus. Cambridge University Press, Cambridge, UK.
Groves, C. P. (2001). Primate Taxonomy. Smithsonian Institution Press, Washington, D.C.
Huffman, M. A., Page, J. E., Sukhdeo, M. V. K., Gotoh, S., Kalunde, M. S., Chandrasiri, T., et al. (1996).
Leaf-swallowing by chimpanzees: A behavioral adaptation for the control of strongyle nematode
infections. International Journal of Primatology, 17, 475–503.
Izawa, K. (1980). Social behavior of the wild black-capped capuchin (Cebus apella). Primates, 21, 443–467.
Jack, K. M. (2003). Explaining variation in affiliative relationships among male white-faced capuchins
(Cebus capucinus). Folia Primatologica, 74, 1–16.
Janson, C. H. (1985). Aggressive competition and individual food consumption in wild brown capuchin
monkeys (Cebus apella). Behavioral Ecology and Sociobiology, 18, 125–138.
Janson, C. H. (1986a). The mating system as a determinant of social evolution in capuchin monkeys
(Cebus). In J. G. Else, & P. C. Lee (Eds.), Primate Ecology and Conservation (pp. 169–179).
Cambridge University Press, Cambridge, UK.
Janson, C. H. (1986b). Capuchin counterpoint: Divergent mating and feeding habits distinguish two
closely related monkey species of the Peruvian forest. Natural History, 95, 45–52.
Janson, C. H. (1990). Social correlates of individual spatial choice in foraging groups of brown capuchin
monkeys, Cebus apella. Animal Behavior, 40, 910–921.
Leca, J.-B., Fornasieri, I., & Petit, O. (2002). Aggression and reconciliation in Cebus capucinus.
International Journal of Primatology, 23, 979–998.
Fur-rubbing in 2 Cebus spp.
817
Leca, J.-B., Gunst, N, Thierry, B., & Petit, O. (2003). Distributed leadership in semi-free ranging whitefaced capuchin monkeys. Animal Behavior, 66, 1045–1052.
Longino, J. T. (1984). True anting by the capuchin, Cebus capucinus. Primates, 25, 243–245.
Ludes, E., & Anderson, J. R. (1995). Peat-bathing by captive white-faced capuchin monkeys, Cebus
capucinus. Folia Primatologica, 65, 38–42.
McGrew, W. C., & Tutin, C. E. G. (1978). Evidence for a social custom in wild chimpanzees? Man, 13,
243–251.
Panger, M. A., Perry, S., Rose, L., Gros-Louis, J., Vogel, E., McKinnon, K. C., et al. (2002). Cross-site
differences in foraging behavior of white-faced capuchins (Cebus capucinus). American Journal of
Physical Anthropology, 119, 52–66.
Parr, L. A., Matheson, M. D., Bernstein, I. S., & de Waal, F. B. M. (1997). Grooming down the hierarchy:
Allogrooming in captive brown capuchin monkeys, Cebus apella. Animal Behavior, 54, 361–367.
Perry, S. (1996). Female-female social relationships in wild white-faced capuchin monkeys, Cebus
capucinus. American Journal of Primatology, 40, 167–182.
Perry, S. (1998). A case report of male rank reversal in a group of wild white-faced capuchins (Cebus
capucinus). Primates, 39, 51–69.
Perry, S., Baker, M., Fedigan, L., Gros-Louis, J., Jack, K., McKinnon, K. C., et al. (2003). Social
conventions in wild white-faced capuchin monkeys. Current Anthropology, 44, 241–268.
Perry, S., & Rose, L. M. (1994). Begging and transfer of coati meat by white-faced capuchin monkeys.
Cebus capucinus. Primates, 35, 409–415.
Petit, O., Abegg, C., & Thierry, B. (1997). A comparative study of aggression and conciliation in
three Cercopithecine monkeys (Macaca fuscata, Macaca nigra, Papio papio). Behaviour, 134,
415–432.
Petit, O., Desportes, C., & Thierry, B. (1992). Differential probability of “coproduction” in two species of
macaque (Macaca tonkeana, M. mulatta). Ethology, 90, 107–120.
Phillips, K. A. (1995). Resource patch size and flexible foraging in white-faced capuchins (Cebus
capucinus). International Journal of Primatology, 16, 509–519.
Quinn, J. P. (2004). Fur Rubbing Behavior in a Captive Group of Cebus apella apella Monkeys. Master’s
thesis. California State University, Fullerton.
Rose, L. M. (1994). Sex differences in diet and foraging behavior in white-faced capuchins (Cebus
capucinus). International Journal of Primatology, 15, 95–114.
Rose, L. M. (1997). Vertebrate predation and food-sharing in Pan and Cebus. International Journal of
Primatology, 18, 727–765.
Thierry, B. (1990). Feedback loop between kinship and dominance: The macaque model. Journal of
Theoretical Biology, 145, 511–521.
Thierry, B. (2000). Covariation of conflict management patterns in macaque societies. In F. Aureli, & F. B.
M. de Waal (Eds.), Natural Conflict Resolution (pp. 106–128). University of California Press,
Berkeley.
Thierry, B. (2004). Social epigenesis. In B. Thierry, M. Singh, & W. Kaummans (Eds.), Macaque
societies: A model for the study of social organization (pp. 267–294). Cambridge University Press.
Thierry, B., Aureli, F., de Waal, F. B. M., & Petit, O. (1997). Variation in reconciliation patterns and social
organization across nine species of macaques. Advances in Ethology, 32, 39.
Ueno, Y. (1991). Urine-washing in tufted capuchins (Cebus apella): Discrimination between groups by
urine-odor. In A. Ehara, T. Kimura, O. Takenaka, & M. Iwamonto (Eds.) (pp. 297–300). Primatology
today. Elsevier, Amsterdam.
Valderrama, X., Robinson, J. G., Attygale, A. B., & Eisner, T. (2000). Seasonal anointment with
millipedes in a wild primate: A chemical defense against insects? Journal of Chemical Ecology, 26,
2781–2790.
van Schaik, C. P., & van Noordwijk, M. A. (1989). The special role of male Cebus monkeys in
predation avoidance and its effect on group composition. Behavioral Ecology and Sociobiology, 24,
265–276.
Verbeek, P., & de Waal, F. B. M. (1997). Post-conflict behavior of captive brown capuchins in the
presence and absence of attractive food. International Journal of Primatology, 18, 703–725.
Welker, C., Hoehmann, H., & Schaefer-Witt, C. (1990). Significance of kin relations and individual
preferences in the social behavior of Cebus apella. Folia Primatologica, 54, 166–170.
Zahavi, A. (1977). The testing of a bond. Animal Behavior, 25, 246–247.
Zito, M., Evans, S., & Weldon, P. J. (2003). Owl monkeys (Aotus spp.) self-anoint with plants and
millipedes. Folia Primatologica, 74, 159–161.