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Cross-site differences in foraging behavior of white-faced capuchins (Cebus capucinus).

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Cross-Site Differences in Foraging Behavior of WhiteFaced Capuchins (Cebus capucinus)
Melissa A. Panger,1* Susan Perry,2 Lisa Rose,3 Julie Gros-Louis,4 Erin Vogel,5
Katherine C. Mackinnon,6 and Mary Baker7
Anthropology, George Washington University, Washington, DC 20052
Anthropology, University of California at Los Angeles, Los Angeles, California 90095
Anthropology and Sociology, University of British Columbia, Vancouver V6T 1Z1, Canada
Psychology, University of Pennsylvania, Philadelphia, Pennsylvania 19104
Ecology and Evolution, SUNY Stony Brook, Stony Brook, New York 11794
Anthropology, University of California at Berkeley, Berkeley, California 94720
Anthropology, Pomona College, Claremont, California 91711
traditions; social learning; New World monkey; tool use; interpopulation
Researchers have identified a variety of
cross-site differences in the foraging behavior of free-ranging great apes, most notably among chimpanzees (Pan
troglodytes) and more recently orangutans (Pongo pygmaeus), that are not due to obvious genetic or ecological
differences. These differences are often referred to as “traditions.” What is not known is whether this high level of
interpopulation variation in behavior is limited to hominoids. In this study, we use long-term data from three
Costa Rican field sites that are geographically close and
similar ecologically to identify potential foraging traditions in white-faced capuchins (Cebus capucinus). Foraging traditions are predicted in Cebus because of many
behavioral and morphological convergences between this
genus and the great apes. The processing techniques used
Interpopulation variability in behavior, most notably among chimpanzees (Pan troglodytes) and orangutans (Pongo pygmaeus) (Boesch, 1996a,b; Boesch and Boesch-Achermann, 2000; Boesch and
Tomasello, 1998; McGrew, 1992, 1998; van Schaik et
al., 1999; Whiten et al., 1999), has received a great
deal of research attention recently among primatologists. The general tenet of this research is that crosssite variability in behavior not due to obvious genetic or environmental differences is a result of
social learning processes (i.e., such site-specific foraging techniques are “traditions;” Heyes, 1993;
Mundinger, 1980). Although behaviors that are similar across sites and those that occur because of
some environmental influence may be the result of
social learning (Huffman and Hirata, in preparation), identifying cross-site differences in behavior
not readily attributable to environmental or genetic
differences is a valuable “first step” in providing
evidence of potential traditions in free-ranging populations.
Using these criteria, the identified foraging behaviors argued to be traditional in chimpanzees and
orangutans primarily involve difficult-to-access food
resources, and thus entail complex manipulative be©
for the same food species were compared across sites, and
all differences found were classified as present, habitual,
or customary. Proximity data were also analyzed to determine if social learning mechanisms could explain variation in foraging behavior. Of the 61 foods compared, we
found that 20 of them are processed differently by capuchins across sites. The differences involve pound, rub, tap,
“fulcrum,” “leaf-wrap,” and “army ant following.” For most
of the differences with enough data to analyze, the average proximity score of the “matched” dyads (two individuals within a group who shared a “different” processing
technique) was statistically higher than the average proximity score of the remaining “unmatched” dyads. Am J
Phys Anthropol 119:52– 66, 2002. © 2002 Wiley-Liss, Inc.
Grant sponsor: Alberta Heritage Scholarship Fund; Grant sponsor:
Area de Conservación Guanacaste; Grant sponsor: Area de Conservación Tempisque; Grant sponsor: Costa Rican National Park Service;
Grant sponsor: Earthwatch; Grant sponsor: Leakey Foundation;
Grant sponsor: Organization for Tropical Studies; Grant sponsor:
National Geographic Society; Grant sponsor: NIH-MIRT; Grant sponsor: National Science Foundation; Grant sponsor: Natural Sciences
and Engineering Research Council of Canada; Grant sponsor: Royal
Anthropological Institute; Grant sponsor: Sigma Xi; Grant sponsor:
University of Alberta; Grant sponsor: UC-Berkeley Department of
Anthropology; Grant sponsor: UCLA; Grant sponsor: UCLA Council
on Research; Grant sponsor: UC-Riverside Graduate Division; Grant
sponsor: University of Michigan Alumnae Society; Grant sponsor:
University of Michigan Rackham Graduate School; Grant sponsor:
University of Pennsylvania; Grant sponsor: UREP; Grant sponsor:
Center for the Advanced Study of Human Paleobiology; Grant sponsor: George Washington University.
*Correspondence to: Melissa Panger, Department of Anthropology,
2110 G St., NW, George Washington University, Washington, DC
20052. E-mail:
Received 16 July 2001; accepted 5 February 2002.
DOI 10.1002/ajpa.10103
Published online in Wiley InterScience (www.interscience.wiley.
haviors (e.g., object and tool use). For example, in
free-ranging orangutans, probing and scraping tools
are habitually used in some geographic areas, but
are not used in others (Fox et al., 1998; van Schaik
et al., 1996, 1999). Among chimpanzees, behaviors
vary across geographic areas, e.g, the use of hammers and anvils to crack open hard-shelled nuts
(Boesch and Boesch, 1990; Boesch and BoeschAchermann, 2000; Boesch et al., 1994; Inoue-Nakamura and Matsuzawa, 1997; McGrew, 1992; Sakura
and Matsuzawa, 1991); the cracking of hard-shelled
fruits against substrates (Boesch, 1996b; Goodall,
1986; Matsuzawa and Yamakoshi, 1996; Nishida,
1987); and ant dipping and termite fishing (Boesch
and Boesch, 1990; McGrew, 1992, 1998; Sugiyama,
1997). In all, researchers from seven long-term
chimpanzee field sites recently identified 39 behavioral pattern differences among their study populations, 18 of which involved food processing techniques (all entailing object or tool use; Whiten et al.,
These food- and nonfood-related behavioral differences have been argued to be especially important
for lending insight into the evolution of human culture, including material culture (Boesch, 1996b;
Boesch and Tomasello, 1998; McGrew, 1992, 1998;
Sakura and Matsuzawa, 1991; Sugiyama, 1997; van
Schaik et al., 1999). Although cross-site differences
in foraging and other types of behavior have been
found in a variety of animal species (Bonner, 1980;
Galef, unpublished data; Hall, 1963; Huffman, 1996;
Huffman and Hirata, unpublished data; Itani, 1958;
Kawamura, 1959; Lefebvre and Palameta, 1988;
Watanabe, 1994; Wolfe, 1981), the number and
types of differences are argued to be unique to chimpanzees and orangutans (Boesch and Tomasello,
1998; Whiten et al., 1999). What is not currently
known is whether or not this high level of cross-site
variability in foraging behavior is actually unique to
hominoids. The primary aim of this paper was to
determine whether or not capuchins (members of
the New World monkey genus Cebus) exhibit traditions in a foraging context comparable to what has
been described in great apes.
There are many reasons to suspect that capuchins
might exhibit the types of foraging traditions previously only described in great apes. For example,
capuchins have long life-history variables, large
brain size relative to body size, and a high level of
sensorimotor intelligence when compared to other
monkeys; and they have an omnivorous diet (including vertebrate prey), and rely heavily on extractive
foraging techniques (Anderson, 1996; Antinucci,
1989; Fragaszy et al., 1990; Fragaszy and Bard,
1997; Gibson, 1986; Panger, 1998; Parker, 1990;
Parker and Gibson, 1977; Reader, in preparation;
Visalberghi and McGrew, 1997). Furthermore, capuchins (Cebus spp.), along with the great apes, are the
most prolific nonhuman primate tool-users (Anderson, 1996; Boinski et al., 2000; McGrew and Marchant, 1997). Relative to most Old World monkeys,
capuchins are extraordinarily tolerant of others foraging in close proximity, allowing them to sit in
contact with them and even touch and sniff the food
being processed (Perry and Rose, 1994, and unpublished data). Thus capuchins exhibit all of the socioecological features (extractive foraging, dexterous
manipulation, and tolerant gregariousness) that van
Schaik et al. (1999) proposed as necessary precursors to the evolution of material culture in primates.
Tool- and object-use behaviors in capuchins
Capuchins use tools extensively under captive and
semifree-ranging conditions (Anderson, 1990;
Anderson and Henneman, 1994; Antinucci and Visalberghi, 1986; Gibson, 1990; Jalles-Filho, 1995;
Klüver, 1933; Ottoni and Mannu, 2001; Urbani,
1999; Visalberghi, 1987, 1988, 1990; Visalberghi
and Vitale, 1990; Westergaard, 1995; Westergaard
and Fragaszy, 1987; Westergaard and Suomi,
1993a,b, 1994a,b,c, 1995; Westergaard et al., 1995,
1997). Several reports indicate that tool use, along
with a variety of object-use behaviors, is also a likely
part of the normal behavioral repertoire of many
free-ranging capuchins (i.e., use of a club, Boinski,
1988; use of probing tools, Chevalier-Skolnikoff,
1990; hammer and anvil use, Fernandes, 1991;
Boinski et al., 2000; use of leaf containers, Phillips,
1998; and pounding/rubbing objects against a substrate, Boinski et al., 2000; Izawa and Mizuno, 1977;
Panger, 1998; Struhsaker and Leland, 1977; Terborgh, 1983). Although there may be species-level
differences in capuchin tool-using abilities (our
knowledge, especially from captive studies, is
heavily biased towards C. apella), it is clear from
field reports that C. apella, C. capucinus, and C.
albifrons can and do use tools under free-ranging
As with apes (e.g., Boesch and Boesch, 1990;
Goodall, 1964; McGrew, 1992, 1993), most of these
highly manipulative behaviors occur in a foraging
context, and are used to access difficult-to-process
foods (Boinski et al., 2000; Panger, 1998, 1999; Terborgh, 1983). Therefore, capuchins exhibit many of
the foraging behaviors identified as “cultural traditions” in free-ranging chimpanzees and orangutans
(van Schaik et al., 1999; Whiten et al., 1999). In fact,
early reports of complex foraging techniques used by
free-ranging capuchins led Nishida (1987) to state,
“Judging from their sophistication, these techniques
may very probably be cultural behaviors.”
Capuchin social dynamics
In addition to exhibiting types of foraging behaviors that vary across sites in hominoids, capuchins
also exhibit social dynamics conducive to social
learning processes (Boesch and Tomasello, 1998;
Coussi-Korbel and Fragaszy, 1995; van Schaik et al.,
1999). Capuchins live in multimale/multifemale
groups; they engage in high levels of alloparenting,
such that immatures have ready access to a variety
of role models; and they tend to be extraordinarily
tolerant of the close proximity of group members
while foraging (S. Perry, unpublished data). Food
sharing, rare among nonhuman primates, has been
reported in capuchins (de Waal et al., 1993; Perry
and Rose, 1994; Westergaard and Suomi, 1997).
This level of tolerance allows group members to
cofeed in proximity to each other on a regular basis.
Therefore, the social context is ripe and the opportunities exist for capuchins to learn specific foraging
behaviors from other group members.
Social learning processes in capuchins
Specifically regarding social learning processes,
the overriding (although debatable) view in the literature is that monkeys, including capuchins, are
unable to truly imitate (Adams-Curtis, 1990; Byrne,
1994; Fragaszy and Visalberghi, 1989, 1990, 1996;
Galef, 1992; Heyes, 1993; Visalberghi and Fragaszy,
1990; Visalberghi, 1987, 1997; Visalberghi and Limongelli, 1996; Visalberghi and Trinca, 1988;
Whiten, 1989, 1996), while the ability of hominoids
to truly imitate is open for debate (Boesch, 1996a;
Byrne, 1996; Custance et al., 1999; Heyes, 1998;
Inoue-Nakamura and Matsuzawa, 1997; Russon,
1996; Russon and Galdikas, 1992; Tomasello, 1990;
Whiten and Ham, 1992). Both capuchins and great
apes, however, are clearly capable of other forms of
social learning (e.g., at least emulation and simple
imitation; Custance et al. 1999). Thus, although
there appear to be differences in the overall intellectual abilities of hominoids and capuchins, both types
of primates are capable of complex social learning
(Langer, 2000; Parker and McKinney, 1999; Visalberghi and Limongelli, 1996).
Therefore, primarily due to their diet, sensorimotor abilities, foraging behavior, and social dynamics,
capuchins are expected to show levels of cross-site
variability in foraging behavior comparable to the
differences found in chimpanzees and orangutans.
The primary aim of this paper was to determine
whether or not capuchins exhibit such traditions in
a foraging context. Since the data presented here
were not collected specifically for this purpose, we
are not able to address specific questions regarding
the origin of possible traditions within our study
populations. Therefore, conclusions regarding the
social learning processes (e.g., emulation, imitation,
orenvironmental facilitation; see Custance et al.,
1999; Hall, 1963; Heyes, 1993; Parker, 1996; Whiten
and Ham, 1992) responsible for the transmission
and acquisition of potential foraging traditions in
capuchins are beyond the scope of this project, although possible reasons for any differences found
are discussed.
Study sites
Data were compiled by researchers from three
long-term white-faced capuchin (Cebus capucinus)
study sites located in the tropical dry forests of the
Guanacaste Province in Northwestern (NW) Costa
Rica (Lomas Barbudal (LV) Biological Reserve, Palo
Verde (PV) National Park, and Santa Rosa (SR)
National Park; Fig. 1, Table 1). These sites were
chosen because of their geographic proximity to each
other (therefore, capuchins from each site are assumed to be similar genetically) and their ecological
similarity (Janzen, 1983). Supplemental data from
other long-term capuchin sites were used when appropriate; however, unless otherwise stated, the information provided below comes from the three
main dry forest sites just listed.
The tropical dry forests of NW Costa Rica typically
receive 1,000 –2,500 mm of rain per year and experience two distinct seasons annually: a wet season
(June–November) and a dry season (December–
May). During the dry season, little to no rain falls
and temperatures can reach 40°C. Up to 80% of the
trees in these areas are deciduous, and they lose
their leaves completely during the dry season (for
forest phenology and plant composition, see Frankie
et al., 1974). The forests typically lack a clear vertical structure, and the trees are normally no higher
than 25 m. The relatively low canopy and decreased
foliage during the dry season allow for exceptional
visibility. For details on Lomas Barbudal, see
Frankie et al. (1988); for Palo Verde, see Panger
(1997, 1998); and for Santa Rosa, see Fedigan et al.
(1996) and Hartshorn (1983).
Data comparison
Processing techniques. Although the three
study sites are similar ecologically, the diets of even
neighboring capuchin troops can vary (Chapman
and Fedigan, 1990; Rose, 1998). Therefore, comparisons (unless otherwise indicated) were limited to
species that appear on the food lists of at least 2 of
the 3 main study sites (Table 2). This enabled us to
compare how the same food species were processed
across sites. After a list of “overlapping” plant and
animal food species was compiled, brief qualitative
descriptions of how each species is processed by the
capuchins at each site (where it is eaten) were provided by the researchers referred to in Table 1. It
should be noted that detailed data collection on food
processing techniques was only a focus at PV (during Panger’s 1995–1996 study) and at LB (during
Gros-Louis and Vogel’s 2000 field season and Perry’s
2001 field season). Therefore, the descriptions from
the study sites are qualitative, and only broad crosssite differences are noted.
Because only broad differences were noted, most
of the processing differences that we found involve
obvious differences in manipulative behavior, i.e.,
“object-use” behaviors, tool use, and other obvious
Fig. 1. Map of study sites. Individual maps are not to scale. Letters represent core areas of different Cebus capucinus study groups
discussed in this paper. Santa Rosa: Ce, Cerco de Piedra; L, Los Valles; N, Nancite; S, Sendero; Lomas Barbudal: A, Abby; R, Rambo;
Palo Verde: LT, Lagoon; ST, Station; WH, Water Hole.
manipulative behaviors (Table 3). In final comparisons, if a food was not processed in one of these
ways, it was included in the default category “eat”
(Table 4). A processing technique at a particular site
was considered “different” from those at the other
site(s) if it involved one of the “noneat” categories,
and the same food was processed by “eat” at another
site. Thus, for example, if a particular food species
was processed using “pound” at two sites, but was
processed using “eat” at another, the “pound” technique was considered “different.”
We are aware that our data are limited, especially
in regard to the PV data (which are based on the
observations of one researcher, M.A.P., over an 11month period). In light of the old but true adage,
“absence of evidence is not evidence of absence,” we
looked for obvious patterns in our data that might be
due to differential observation time at each site.
Additionally, because geographic proximity has the
potential to influence cross-site variability, we compared our study sites in regard to the number of
between-site differences in food processing techniques.
Use categories. Once broad differences in processing techniques were noted, information on the
number of individuals who exhibited the indicated
behavior at the specific site(s) where it occurred was
provided if possible. Similar categories to those described by Whiten et al. (1999) were used: “customary,” if the behavior is exhibited by all members of at
least one age/sex class; “habitual,” if the behavior is
not customary but is exhibited by more than one
individual; and “present,” if the behavior has been
observed but is neither customary nor habitual. The
data in Results were checked over several times by
all of the authors to insure their accuracy, and supplemental information were provided by additional
capuchin researchers when possible.
Social network data. Because the acquisition of
traditions requires that individuals observe the be-
TABLE 1. Study site information
Study site
Lomas Barbudal
10° 30⬘ N, 85° 22⬘ W
adult sex
ratio (male
to female)
Troop size
providing data for
this project
S. Perry3
E. Vogel4
J. Gros-Louis5
Rambo II’s
Water Hole
Cerco de Piedra
Los Valles
Cerco de Piedra
Los Valles
Palo Verde
10° 19⬘–10° 24⬘ N,
85° 18⬘–85° 25⬘ W
19 (average)6
M. Panger7
Santa Rosa
10° 45⬘–11° 00⬘N,
85° 30⬘–85° 45⬘ W
18 (average)8
L. Rose9
K.C. MacKinnon10
Contact hours refer to total number of hours a researcher spent watching monkeys at respective study sites. Contact hours were not
necessarily distributed equally among study troops.
Information from Chapman et al. (1989).
S. Perry has been collecting capuchin data at LB since 1990.
E. Vogel’s data are from a 6.5-month study in 2000. Food processing data were not collected systematically during all of the contact
hours reported.
J. Gros-Louis has worked at LB since 1991.
Information from Panger (1997).
M. Panger spent 11 continuous months working at PV.
Information from Fedigan et al. (1996).
L. Rose worked at SR, noncontiguously, over a span of 7 years.
K.C. MacKinnon worked a total of 21 months during 3 separate years at SR.
havior of others, we wanted to see if individuals who
exhibited customary or habitual behavior patterns
were also those that shared social networks (or at
least were often found in proximity to each other).
We used proximity scan data that were collected at
the end of 10-min focal periods to indicate potential
social networks. Detailed data regarding proximity
data and specific processing techniques were only
available from the main study troop at PV, which
was composed of 17 individuals (4 adult males, 4
adult females, 2 subadult males, 1 subadult female,
3 juveniles, and 3 infants).
At PV, each individual within 3 m of the focal
animal was recorded during each proximity scan.
There were 91 different dyad combinations possible
for the individuals in this group (excluding infants).
The number of scan samples that each individual
was found in proximity to a specific dyad partner
was divided by the total number of scan samples
collected for both individuals in that dyad (i.e., the
scans for each individual in a dyad were pooled).
These percentages represent each dyad’s proximity
score. We will refer to the dyads composed of two
individuals who share a specific “different” processing technique at PV as “matched dyads.” Note that
the matched dyads differ for each food species compared, depending on the individuals who exhibited
the specific processing technique being analyzed.
Mann-Whitney U-tests were run (using STATISTICA, 1998 edition) to compare the proximity scores
of matched dyads (for each relevant food species) to
the proximity scores of remaining dyads. Alpha was
set at P ⫽ 0.05. The genealogies at PV are not
known, and therefore, proximity measures along
kinship lines could not be explored.
Foraging behaviors
Number and types of differences found. There
was a total of 49 plant (two encompassing different
parts of the same species) and 12 animal foods that
overlapped between at least two sites (see Table 2).
Of the 61 foods that overlapped, 20 (16 plants and 4
animals) were processed differently at minimally
one of the sites by at least one individual (Table 4).
Three of these foods were only eaten rarely at one of
the compared study sites, so processing techniques
may have been missed because of limited observation opportunities.
The processing differences associated with 17
foods involved “pound” and/or “rub;” 2 involved “tool
use” (i.e., wrapping a noxious object in a leaf before
rubbing it against a substrate); 2 involved “tap;” 1
involved “fulcrum,” and 1 involved following army
ants to access flushed-out insects. Seven foods were
processed differently at LB; 8 foods were processed
differently at PV; and 13 foods (two encompassing
different parts of the same species) were processed
differently at SR. In all, 39 different processing techniques were identified from all three sites (i.e., all of
the techniques in bold listed in Table 4). Of these 39
processing technique differences, 5 are “present;” 26
are “habitual;” and 8 fit the “customary” category.
TABLE 2. List of species (or common name) of food found on food lists of at least two of the main study sites
Food species (plants)
Acacia spp. (fruit)
Acacia spp. (adults/larvae in thorns)
Acrocomia vinifera
Allophyllus occidentalis
Annona reticulata
Apeiba tibouru
Ardisia revoluta
Astronium graveolens
Bactris minor
Bauhinia spp.
Bromelia pinguin (fruit)
Bromelia pinguin (pith)
Bursera simaruba
Byrsonima crassifolia
Carica papaya
Casearia spp.
Cassia grandis
Cecropia peltata
Cochlospermum vitifolium (flowers)
Food species (animals)
Combretum farinosum
Curatella americana
Diospyros nicaraguensis
Enterolobium cyclocarpum
Ficus spp.
Genipa americana
Guazuma ulmifolia
Guettarda macrosperma
Jacquinia pungens
Lasiacis ruscifolia
Licania arborea
Luehea candida
Food species (plants)
Luehea speciosa
Maclura tinctoria
Mangifera indica
Manilkara chicle
Muntingia calabura
Passiflora spp.
Pithecellobium saman
Psychotria sp.
Quercus sp.
Randia sp.
Sciadodendron excelsum
Simarouba glauca
Sloanea terniflora
Spondias mombin
Stemmandenia donnell-smithii
Sterculia apetala
Tabebuia ochracea
Trichilia trifolia
Insects in branches
“Army ant following”
Bird eggs
Automeris spp. caterpillars
Other large caterpillars
Squirrels and coatis
Polistes nests
Polybia nests
Detailed descriptions of how each food species is processed at each site are available upon request from the corresponding author.
LB, Lomas Barbudal; PV, Palo Verde; SR, Santa Rosa; *site where food species is eaten by monkeys.
Total LB food list includes approximately 120 species (S. Perry and E. Vogel, personal communication).
PV food list includes approximately 52 species (Panger, 1997).
SR food list includes approximately 100 species (MacKinnon, 1995; L. Rose, personal communication).
Additionally, there were 6 foods that involved minor
variations in processing techniques across at least
two sites. Neither distance between sites nor different observation times at each site seemed to
strongly influence the number of food-processing
technique differences across sites.
It should be noted that “fulcrum” and “tool use”
were not initially included in the processing techniques used by SR capuchins to process Pithecellobium saman and Automeris spp. caterpillars, respectively. However, they were later included based on
information provided by additional researchers.
Linda Fedigan (personal communication) reported
seeing monkeys processing P. saman pods using
“fulcrum” behaviors several years ago at SR (for a
description of the behavior, see Panger, 1998). Additionally, R. O’Malley (personal communication) recently observed a few monkeys using the leaf-wrapping behavior to process Automeris caterpillars at
SR (see below).
Overall, most differences in foraging techniques
across our study sites involved difficult-to-process
foods (e.g., embedded foods and foods protected by
noxious substances). This is somewhat obvious,
since easy-to-eat foods, such as small fruits, can
simply be picked, placed into the mouth, and
chewed; there is not much room for variation (especially at the level of our comparison). However, it
should be noted that not all complex processing techniques varied across the three sites. For example,
accessing seeds from Luehea candida fruits is a complicated task that requires dexterous bimanual coordination (for description, see Panger, 1998). However, the processing technique used with L. candida
varies little across the three main study sites. In all,
8 foods from our list of 61 overlapping food species
that were difficult to process (i.e., they were processed using a “noneat” category) were not processed
differently across sites.
Description of differences found
Object-use behaviors. Most of the foraging techniques that differed across sites involved object-use
behaviors, specifically “pound” and “rub.” Many of
the assumed functions of “pound” and “rub” overlap.
The assumed functions of these behaviors were: to
break into hard fruits or other plant parts (Annona
reticulata, Apeiba tibouru, Manilkara chicle, Quercus spp., Randia armata, Stemmedenia donnellsmithii, Sterculia apetala, and tree branches); to
soften fruits prior to ingestion (Cercropia peltata,
Genipa americana, and Mangifera indica); to (un-
TABLE 3. Description of food processing techniques that varied across study sites
Processing technique
“Army ant following”
Several members of a group closely follow foraging columns of army ants and catch animal prey
(primarily insects and occasionally small vertebrates) flushed out by swarm of traveling ants.
An individual applies force on an object working against a substrate (which was used as a fulcrum). This
is a type of object use.1
An individual wraps an object in a leaf and then rubs the leaf (containing the object) against a fixed
substrate (e.g., tree branch or rock). This is a type of tool use.2
An individual hits an object against a fixed substrate (e.g., tree branch or rock) with either one or two
hands. This is a type of object use.1
An individual slides an object against a fixed substrate (e.g., tree branch or rock) with one or two hands.
This is a type of object use.3
An individual uses its fingertips to tap against an object. A tap normally involves a rhythmic series of
rapid taps on one object with the fingers of one hand.
Fulcrum use
“Leaf wrap”
Object use is defined as any time an individual manipulates (to alter) a detached object relative to a fixed substrate or medium
(Panger, 1998; Parker and Gibson, 1977).
Tool use is defined as “[T]he external employment of an unattached environmental object to alter more efficiently the form, position,
or condition of another object, another organism, or the user itself when the user holds or carries the tool during or just prior to use”
(Beck, 1980).
Although we assign “assumed functions” to the pound and rub behaviors in the text, in reality it is very difficult to determine the
motivation for every pound and rub bout. Both “pound” and “rub” are commonly reported in both captive and free-ranging capuchins
(for captive Cebus, Antinucci and Visalberghi, 1986; Fragaszy and Adams-Curtis, 1991; Visalberghi, 1988; Visalberghi and Vitale,
1990); for free-ranging Cebus, Boinski et al., 2000; Izawa and Mizuno, 1977; Panger, 1998; Struhsaker and Leland, 1977; Terborgh,
1983). There is a possibility that pound and rub are default behaviors that are turned to by capuchins whenever they run into difficulty
processing food (juvenile capuchins will also occasionally pound “inappropriate,” nonfood items against substrates, e.g., stones).
successfully) remove hair from mammalian prey
(squirrels and coatis); to remove noxious substances
or biting insects from foods (Acacia spp. fruits and
thorns, Automeris caterpillar, Sloanea terniflora,
Sterculia apetala, and Tabebuia ochracea); and to
detach fruit from fruit bunches (Bactris minor). In
the case of Sterculia apetala, the monkeys at both
LB and PV rubbed the fruits, but they used the rub
behavior at different stages of the food processing
procedure. At LB, monkeys opened hard-husked
fruits with their teeth, and then rubbed the fruit
within the husks against tree branches. At PV, the
fruit husks themselves were occasionally rubbed
against tree branches; once the husks were opened
(normally using teeth), the monkeys simply ate the
fruit inside without rubbing it.
Fulcrum (see Table 3 for definition) was used to
process Pithecellobium saman fruits at PV and SR.
The fruits are broken open by monkeys to access
bruchid beetle larvae that live inside the fruits.
“Leaf wrap.” Another processing technique that
appears on our list of differences involves monkeys
wrapping objects (Automeris caterpillars and Sloanea terniflora fruits) in leaves before rubbing them
against a substrate (a type of tool use). Both Automeris caterpillars and Sloanea terniflora fruits have
chemical or mechanical defenses that can cause pain
and/or discomfort when touched. Therefore, the
monkeys are most likely using the leaves to protect
their hands when rubbing the objects to remove
noxious substances. At SR, most individuals rub
Sloanea fruits and Automeris caterpillars directly
against a substrate without wrapping them in
leaves first, and the “leaf-wrapping” behavior has
only been seen a few times with each of these foods
(L. Rose, personal observation; R. O’Malley, personal communication).
“Tap.” “Tap” is another foraging technique that
varies among the three main study sites. The behavior is presumably used to check for fruit ripeness (as in
the case of Mangifera indica and Stemmedenia donnell-smithii fruits) and to search for insects in
branches and/or Pithecellobium saman fruits (see Visalberghi and Néel, unpublished findings). The monkeys at LB were only recently seen tapping branches.
Researchers have been looking for “tap” at LB since
1993, although systematic data collection on the behavior started in 2000. “Branch tapping” was not reported at LB before 2000. During the 2000 and 2001
LB field seasons, however, the behavior was exhibited
often by several individuals. The potential for methodological bias makes it difficult to confirm the absence of
“branch tap” at LB prior to 2000, but the behavior has
apparently become more common at the site since
1993. Overall, tapping is seen across all age/sex classes
(excluding infants); however, the highest rate is found
among adult females (MacKinnon, 1995; Panger, unpublished data; S. Perry, unpublished data) whose
total tapping rate averages 1.55 bouts/hr at PV (Panger, unpublished data).
“Army ant following.” The final foraging technique that appears on our list of cross-site differences is “army ant following.” This behavior involves
a troop of capuchins closely following foraging columns of army ants and catching animal prey (primarily insects and occasionally small vertebrates)
flushed out by the swarm of traveling ants (similar
behaviors were reported in a variety of bird genera;
Rettenmeyer, 1983). This behavior is seen often at
SR, and each bout may last for up to an hour. Although army ants are common at both LB and PV,
the monkeys there were never seen to forage in
association with ant swarms. “Army ant following”
was also seen by M. Baker (unpublished data) at her
TABLE 4. Processing techniques that vary across sites and their use patterns
Lomas Barbudal
Food species
Palo Verde
Santa Rosa
Acacia spp. (fruit)
Acacia spp. (thorns)
Annona reticulata
Eat (rare)
Apeiba tibouru
Bactris minor
Cecropia peltata
Eat (rare)
Genipa americana
Mangifera indica
Manilkara chicle
Pithecellobium saman
Quercus spp.
Randia spp.
Sloanea terniflora
Stemmandenia donnell-smithii
Sterculia apetala
Tabebuia ochracea
Rub (fruit inside of husk)
Leaf wrap
Rub (husk of fruit)
Eat (rare)
Automeris spp. caterpillar
Insects in branches4
Vertebrate prey (squirrels and coatis)
“Army ant following”
Leaf wrap
Leaf wrap
Tech., technique; U. P., are patterns. Please see Table 3 and text for definitions of specific processing techniques.*** Foods that do
not appear on site’s food list (species may be present at site); techniques in bold indicate “different” techniques. P, “present;” H,
“habitual;” C, “customary” (see text for definitions).
This information based on L. Fedigan (personnal communication).
This information based on R. O’Malley (personnal communication).
“Tap branch” was only recently seen at LB (see text for discussion).
C. capucinus site in Curú, Costa Rica. At Curú, the
monkeys not only catch the prey flushed out by the
ants, but also occasionally take prey already caught by
the ants (and consume both the ants and their prey).
Social networks
To statistically compare proximity scores of the
dyads who used a unique processing technique
(“matched dyads”) to proximity scores of the remaining dyads, there had to be more than one matched
dyad associated with the specific food species involved in the analysis. There were four food species
from Table 4 at PV that met this criterion. In all four
of these cases, the matched dyads for each food species had a higher average proximity score than the
average proximity score of the remaining dyads
(three of the differences were statistically significant; see Table 5 and Fig. 2). It should be noted that
there is much overlap in the individuals who make
up the “matched” dyads for the different food species
(i.e., KK-PHIL [KK-PH] are associated with all four
of the foods; KK-LARRY [KK-LA] and PH-LA are
associated with three; and KK-PENNY [KK-PN],
LA-PN, and PH-PN are associated with two). Such
redundancies might be expected if social learning
mechanisms play a role in producing shared behavior patterns, e.g., spending a lot of time in close
proximity to another particular individual could allow for several opportunities to learn specific behavior patterns (not just one) from that individual.
However, it is possible that one or more of these
dyads skewed the average proximity scores of the
matched dyads. Nonetheless, the average proximity
score for all of the matched dyads (combined) was
statistically higher than the average proximity score
for the unmatched dyads, indicating a statistical
difference (unmatched dyads: N ⫽ 65; average ⫽ 3.4;
r ⫽ 0 –16.5; SD ⫽ 3.3; matched dyads: N ⫽ 26;
average ⫽ 6.7; r ⫽ 0 –15; SD ⫽ 3.7; U ⫽ 307.5, z ⫽
⫺4.6, P ⬍ 0.001).
There were four food species with only one
matched dyad. Although not statistically analyzed,
the proximity scores for 3 of these 4 matched dyads
were higher than the averages and medians for the
remaining dyads (again, see Table 5). The exception
was for pounding Tabebuia. Two adult females
Phil, Penny
Individuals exhibiting the behavior
Proximity score for matched dyad3
See text for definitions of “matched” and “unmatched” dyads. Selection criteria for “matched dyads” were based on data available as of June 2001. Subsequent data show that Stemm
anderi donnell-smithii is also “pounded” at LB.
Benji (BN, adult male); Gina (GN, adult female); Keggy (KG, adult female); KK (KK, subadult male); Larry (LA, subadult male); Mac (MC, adult male); Maury (MR, adult male);
Penny (PN, juvenile); Phil (PH, juvenile); Susie (SU, adult female).
*Statistically significant difference; A. reticulata (matched dyads: N ⫽ 10; r ⫽ 2–12.5; SD ⫽ 3.88; unmatched dyads: N ⫽ 81; r ⫽ 0 –16.5; SD ⫽ 3.56) (U ⫽ 208.5, z ⫽ ⫺2.50, P ⫽ 0.013);
M. indica (matched dyads: N ⫽ 6; r ⫽ 5.1–12.1; SD ⫽ 2.28; unmatched dyads: N ⫽ 85; r ⫽ 0 –16.5; SD ⫽ 3.66) (U ⫽ 74.0, z ⫽ ⫺2.90, P ⫽ 0.004); Randia spp. (matched dyads: N ⫽
15; r ⫽ 2–15; SD ⫽ 3.65; unmatched dyads: N ⫽ 76; r ⫽ 0 –16.5; SD ⫽ 3.49) (U ⫽ 251.5, z ⫽ ⫺3.41, p ⫽ 0.001); S. donnell-smithii (matched dyads: N ⫽ 3; r ⫽ 3–7.5; SD ⫽ 2.35;
unmatched dyads: N ⫽ 88; r ⫽ 0 –16.5; SD ⫽ 3.75).
⬃, proximity scores higher than total average and median scores for all troop dyads (totals: N ⫽ 91; r ⫽ 0 –16.5; average ⫽ 4.32; median ⫽ 3.2; SD ⫽ 3.71).
Gina, Keggy
Tabebuia ochracea (pound)
Sterculia apetala
Larry, Mac
Pithecellobium saman
Keggy, Maury
Bactris minor (pound)
Average proximity score for matched dyads
Average proximity score for remaining dyads
Comparisons involving one matched dyad
Food species (processing technique)
Gina, KK, Larry, Phil, Penny
Individuals exhibiting the behavior2
KK, Larry, Mac, Maury,
Phil, Susie
Randia spp (pound)
Mangiferas indica
Benji, KK, Larry, Phil
Annona reticulata (pound)
Food species (processing technique)
Comparisons involving more than one matched dyad
TABLE 5. Comparison of proximity scores between matched and unmatched dyads (PV data)*
Stemm anderi donnell-smithii
KK, Penny, Phil
(Gina and Keggy) were the only two individuals at
PV who were observed pounding Tabebuia; these
females, however, were never recorded in proximity
to each other during their scan samples.
Of the 4 troop individuals who did not exhibit any
of the unique processing techniques (excluding infants; Bogie, juvenile; Eric, adult male; Indy, adult
female; and Stoner, subadult female), 3 had the lowest proximity scores of all troop individuals (i.e.,
lowest percent of scans with individuals recorded
within 3 m). Therefore, there was a general pattern
(at least at PV): individuals who spent more time
together shared some of the “different” processing
techniques; those who spent little time around other
troop individuals did not.
What we found in this first systematic attempt to
identify potential intersite differences in the foraging behavior of capuchins is that hominoids are not
unique among primates in regard to their degree of
cross-site differences in foraging behavior. Many of
the same types of differences argued to be “traditional” differences in chimpanzees and orangutans have
now been identified in capuchins (see also Perry et
al., in preparation). Our results indicate that capuchins (specifically Cebus capucinus) vary some of
their complex foraging techniques across geographically close and ecologically similar sites. Of the 61
food species compared, 20 were processed differently
across the three study sites. Many of the differences
involved common behavioral patterns used to process several species (pound, rub, and tap), while
others involved rarer foraging techniques (fulcrum,
“leaf-wrapping,” and “army ant following”). Furthermore, at least at PV, there was a link between proximity scores and individuals who shared different
processing techniques (i.e., in most cases, individuals who shared particular processing techniques had
statistically higher or higher than average proximity scores when compared to the remaining dyads).
There are several parallels between the types of
intersite foraging differences found in capuchins
and those reported for chimpanzees and orangutans.
For example, not only is the high number of differences we found across sites comparable to what was
described for hominoids, but so are the types of
differences observed. Many of the foraging differences identified across chimpanzee and orangutan
populations include tool-use and/or object-use behaviors (e.g., van Schaik et al., 1999; Whiten et al.,
1999). We also found this to be true among the
capuchin populations in our study. Additionally,
many reports of foraging traditions among great
apes involve the absence of a behavior at one site
and its presence at another that cannot be easily
explained by ecological differences. For example,
probing tools are used by orangutans at Suaq Balimbing but not by orangutans at other known sites
(e.g., Fox et al., 1998), and hammers are used by
chimpanzees in some populations but not at others
Fig. 2. Proximity scores for matched and unmatched dyads (a– c). Proximity scores ⫽ percent of total number of scan samples
(collected for both individuals in a dyad) that each individual was found in proximity to the specific dyad partner. Open bars represent
matched dyads for all “different” processing techniques used at PV (see Tables 4 and 5); solid bars represent dyads composed of
individuals at PV who were never observed exhibiting any “different” foraging techniques.
(e.g., Whiten et al., 1999), even though the same
foods processed using these techniques are found at
other sites where the behaviors are absent. In our
study, fulcrum-use, army anting, and leaf-wrapping
were found at some capuchin sites but were absent
at others, and ecological differences cannot easily
account for the variation.
In other cases, the same general foraging behavior
can be found across sites, but the behavior is used to
process different food species. Among chimpanzees,
probing tools are used at many known sites, but they
are not necessarily used to process the same food
species. For example, chimpanzees in some populations use probing tools to access honey, while in
other populations (where probing tools are used to
process other food species), tools are not used for
honey extraction (e.g., McGrew, 1992; Whiten et al.,
1999). For capuchins, an example of this involves
“pound.” Pounding objects against a substrate is
found in all known capuchin populations, but pound
is not universally used for the same food species
(e.g., capuchins pound Cecropia peltata fruits at
some sites, but not at others where the species is
eaten). Additionally, in both capuchins and chimpanzees, a processing technique may be similar
across sites, but its use pattern may be different
(e.g., habitual at one site and customary at another).
An example of this among capuchins is the rubbing
of Tabebuia ochracea fruits, and for chimpanzees,
the use of probing tools to extract fluids (Whiten et
al., 1999).
These similarities suggest several potential hypotheses. One possibility is that the type of interpopulation variation in foraging behavior found previously in great apes and now in capuchins is not
necessarily rare among primates (or other animals),
and that with systematic study, similar types of
foraging traditions could be found in other taxa (e.g.,
Galef, in preparation; Mann and Sargeant, unpublished data). Another possibility is that there are
characteristics shared between capuchins and great
apes (specifically chimpanzees and orangutans) that
allow for, or at least facilitate, foraging traditions.
Some likely candidates (which are not mutually exclusive) are extractive foraging, dexterous manipulation, tolerant gregariousness, long life-history
variables, large brain size relative to body size, a
high level of sensorimotor intelligence, and/or an
omnivorous diet (including vertebrate prey, e.g.,
Boesch and Boesch-Achermann, 2000; Coussi-Korbel and Fragaszy, 1995; Parker and Gibson, 1977;
Reader, unpublished data; van Schaik et al., 1999).
Potential explanations for differences found
Ecological differences. There are several factors
that may help explain the intersite variation found
in the foraging behavior of capuchins, chimpanzees,
and orangutans. For example, ecological differences
across sites may influence foraging patterns. Some
of the foraging differences found among chimpanzee
populations can easily be attributed to ecological
differences between sites (e.g., see Whiten et al.,
1999); many others among chimpanzees, orangutans, and capuchins, however, cannot (e.g., see
McGrew, 1992; van Schaik et al., 1999; Whiten et
al., 1999; this study). Although obvious ecological
differences do not account for many of the differences seen in foraging patterns, subtle ecological
differences could potentially influence foraging behaviors across sites. Differences in soils and microclimates can influence food characteristics (e.g., dif-
ferent growing conditions may make some fruits
tougher or more noxious, thus influencing processing techniques) and forest composition.
Detecting subtle ecological differences across sites
that could influence foraging behaviors is admittedly extremely difficult, but such factors should be
kept in mind in future primate studies attempting to
identify behavioral differences due to social learning
processes. Such data are not currently available for
the three main capuchin sites in this study, so the
effects of subtle ecological differences cannot be specifically addressed here.
Demographic differences. Another potential
factor that may account for cross-site variation in
behavior involves demographic differences. Foraging behavior and diet composition vary across age/
sex classes intraspecifically in many animals, including capuchins, chimpanzees, and orangutans
(for capuchins, Fragaszy and Boinski, 1995; Rose
1994, 1998; Panger, unpublished data; for chimpanzees, Boesch and Boesch-Achermann, 2000; McGrew,
1992; Sugiyama, 1993; Whiten et al., 1999; and for
orangutans, van Schaik et al., 1996, and for orangutans, 1999). These differences have most commonly
been argued to be due to differences in body size
(especially in sexually dimorphic species), which can
lead to differences in predation risk (real or perceived), strength, and ability to socially constrain
others: all these factors can influence foraging patterns (e.g., Fragaszy and Boinski, 1995; Rose, 1994).
Differences in metabolic demands (associated with
such things as gestation and lactation) and variability in foraging skills and efficiency due to age can
also affect an individual’s diet. Such differences in
diet and foraging behavior across age/sex classes
may result in “site-level differences” across research
sites when comparing populations that vary in demographic composition. For example, several studies found that “tap” is largely an adult female behavior in capuchins (e.g., MacKinnon, 1995; Panger,
unpublished data). Therefore, tap may be found in
some groups of capuchins and not others simply as a
result of how many adult females are present.
Demographic differences are not suspected in this
study, however, because troop composition across
the three sites is similar and the pattern of differences across the sites does not support variability in
behavior due to demographic differences (i.e., differences found in the processing techniques involving
pound, rub, tap, tool use, etc. were not skewed toward one site). Furthermore, L. Rose (personal observation) reported that three neighboring groups at
Santa Rosa that varied in troop size and composition
did not differ in their food-processing techniques.
This also appears to be the case at LB, based on
preliminary analyses. Comparative data across
neighboring troops at PV are not available at this
Idiosyncratic behaviors. Individual variation in
behavior may also account for some cross-site differences. Idiosyncratic behaviors exhibited by a single
individual could explain the presence of a behavior
at one site, and its absence at another. For instance, it is possible that the “patterns” that we
see across sites may actually represent coincidentally clustered individual responses to certain
foods. Therefore, when we see a few individuals
processing a particular food in a way different
from the majority of other individuals, we may
simply be detecting individual differences (i.e., independent innovations discovered through trial
and error attempts) that appear clumped because
of sampling error.
This may account for the tool use (i.e., “leaf-wrapping”) observed at LB and at SR. At LB, the individuals who exhibited this behavior were peripheral
individuals who spent very little time together and
hence had few (if any) opportunities to learn tool use
from each other. At SR, the tool-use behavior was
only seen exhibited by one individual and a few
individuals, respectively, for Sloanea terniflora and
caterpillars. Therefore, it is plausible that these individuals learned the behavior independently
through trial and error. Furthermore, individual behavioral differences could explain the other
“present” and “habitual” (if only a few individuals
exhibited the behavior) differences observed, but it
cannot easily account for the remaining customary
and habitual processing techniques that varied
across study sites. Therefore, individual differences
in behavior should be considered in future studies of
this kind, but they cannot easily account for most of
the differences observed in our study.
Social learning mechanisms. Additionally, social learning processes may also explain intersite
variability in behavior. There is a multitude of different social learning processes (all variously defined and interpreted) discussed in the literature.
The main types are local enhancement, response
facilitation, social emulation, and imitation (Custance
et al., 1999; Whiten, 1989). Although debatable, a
growing number of researchers argue that capuchins cannot imitate (e.g., Adams-Curtis, 1990; Byrne, 1994; Fragaszy and Visalberghi, 1989, 1996;
Visalberghi and Fragaszy, 1990; Visalberghi, 1987,
1997; Visalberghi and Limongelli, 1996; Visalberghi
and Trinca, 1988; but see Custance et al., 1999), and
that chimpanzees and orangutans can (e.g., Boesch,
1996a; Custance et al., 1999; Russon, 1996; Russon
and Galdikas, 1992). There is less debate regarding
the argument that capuchins, along with great apes,
are capable of complex forms of social learning (e.g.,
Custance et al., 1999). Social learning processes (including imitation) are the leading potential causes
argued to be responsible for many of the cross-site
differences found among chimpanzee and orangutan
populations (e.g., McGrew, 1992; Boesch and Tomasello, 1998; van Schaik et al., 1999; Whiten et al.,
1999). If it is true that capuchins are not capable of
imitation and that hominoids are, our results suggest that an ability to imitate may not be a necessary precursor to the establishment of foraging traditions, and that simpler types of social learning
processes may be enough to produce intraspecific
differences in foraging behavior across populations.
Arguing for social learning processes requires that
more than one individual exhibit a certain behavior.
Therefore, specifically for capuchins, social learning
processes cannot help explain the differences we
found in the techniques used to process Annona
reticulata, Manilkara chicle, Randia spp., and Sloanea terniflora (because only a single individual was
observed performing the relevant technique). However, social learning processes may help explain
many of the remaining foraging differences that we
identified (those that are customary or habitual).
This is especially true in light of the proximity score
analyses we conducted; there seems to be a fit between social networks and potential learned behavior patterns.
The proximity data from PV, although not conclusive, suggest that at least some of the cross-site
processing differences that we found during the
course of this study are the result of social learning
processes. The apparent spread of branch-tapping at
LB, in addition to the possible disappearance of “fulcrum” to process Pithecellobium saman pods at SR,
indicate that some foraging behaviors may appear,
spread, and then disappear through time in capuchin populations. The pattern of the duration and
spread of certain behaviors over time within and
across groups may provide clues to the social learning mechanism(s) responsible for the transmission
of behaviors (Boesch and Tomasello, 1998). It is impossible, however, at this point to determine which
(if any) social learning processes play a role in the
variability observed in capuchins, because the data
currently available are not detailed enough to resolve this issue. Furthermore, because the genealogies of the capuchins at PV are not known, we cannot at this time address issues regarding the
possible transmission of certain behaviors along kinship lines.
Future research that might elucidate the potential
influence of social learning processes and cross-site
differences in primate behavior includes projects
that focus on the transmission of specific foraging
patterns (e.g., using proximity data to determine
possible transmission of a behavior from a potential
model). An understanding of the association patterns of individuals across age/sex groups would be
vital for this type of research. Studies that focus on
changes in behaviors over time within one population, and projects that focus on the demography of
dispersal and how it might influence the spread of
foraging traditions across groups and study sites,
would also be helpful.
We have identified a wide variety of intersite differences in the foraging behavior of C. capucinus
living in three tropical dry forest sites in Costa Rica,
although specific mechanisms explaining variability
across sites cannot be determined at this time.
These data illustrate that site-specific behaviors not
due to obvious genetic or ecological differences, similar to those found in chimpanzees and orangutans,
can be found in nonhominoid primates. Whether or
not such differences will also be found in other primate and/or nonprimate species will require further
research (but see Galef, unpublished data; Mann
and Sargeant, unpublished data). The results of this
preliminary study are not meant to be definitive;
instead, they are meant to be a springboard for
future systematic research of this kind.
We thank the participants of the conference on
animal traditions organized by Drs. Dorothy Fragaszy and Susan Perry (held November, 2000 in
Athens, GA), especially Dr. Michael Huffman; we
also thank Dr. Russ Greenberg, Dr. Clark Spencer
Larsen, and three anonymous reviewers for valuable
comments on various versions of this manuscript.
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