Cross-site differences in foraging behavior of white-faced capuchins (Cebus capucinus).код для вставкиСкачать
AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY 119:52– 66 (2002) 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 1 Department Department 3 Department 4 Department 5 Department 6 Department 7 Department 2 of of of of of of of 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 KEY WORDS variation traditions; social learning; New World monkey; tool use; interpopulation ABSTRACT 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© 2002 WILEY-LISS, INC. 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: firstname.lastname@example.org Received 16 July 2001; accepted 5 February 2002. DOI 10.1002/ajpa.10103 Published online in Wiley InterScience (www.interscience.wiley. com). VARIATION IN CAPUCHIN FORAGING BEHAVIOR 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., 1999). 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. WHY CAPUCHINS ARE PREDICTED TO EXHIBIT FORAGING TRADITIONS 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 53 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 conditions. 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., 54 M.A. PANGER 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. METHODS 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 VARIATION IN CAPUCHIN FORAGING BEHAVIOR 55 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- 56 M.A. PANGER ET AL. TABLE 1. Study site information Study site Geographic coordinates Lomas Barbudal 10° 30⬘ N, 85° 22⬘ W Capuchin density 2 3.7/km2 Capuchin adult sex ratio (male to female) Troop size 20–372 1:22 Researchers providing data for this project Contact hours1 Troop(s) studied S. Perry3 7,721 E. Vogel4 J. Gros-Louis5 1,875 2,425 Abby’s Rambo’s Abby’s Abby’s Rambo II’s Lagoon Station Water Hole Cerco de Piedra Los Valles Nacite Cerco de Piedra Los Valles Sendero Palo Verde 10° 19⬘–10° 24⬘ N, 85° 18⬘–85° 25⬘ W 6 9.4/km2 19 (average)6 1:1.26 M. Panger7 1,200 Santa Rosa 10° 45⬘–11° 00⬘N, 85° 30⬘–85° 45⬘ W 8 4.8/km2 18 (average)8 1:1.38 L. Rose9 3,185 K.C. MacKinnon10 1,515 1 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. 2 Information from Chapman et al. (1989). 3 S. Perry has been collecting capuchin data at LB since 1990. 4 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. 5 J. Gros-Louis has worked at LB since 1991. 6 Information from Panger (1997). 7 M. Panger spent 11 continuous months working at PV. 8 Information from Fedigan et al. (1996). 9 L. Rose worked at SR, noncontiguously, over a span of 7 years. 10 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. RESULTS 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. 57 VARIATION IN CAPUCHIN FORAGING BEHAVIOR 1 TABLE 2. List of species (or common name) of food found on food lists of at least two of the main study sites Sites Food species (plants) LB3 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 * * * * * * * * * * * * * * * * * * * * * * * * * * * * * * PV4 2 Sites SR5 Food species (plants) LB * * * * * * * * 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” Snails Bird eggs Automeris spp. caterpillars Other large caterpillars Squirrels and coatis Grasshoppers Polistes nests Polybia nests Termites Butterflies * * * * * * * * * * * * * * * * * * * * * * * * * * * * * * * * * * * * * * * * * * * * * * * * * * * * * * * * * * * * * * * * * PV SR * * * * * * * * * * * * * * * * * * * * * * * * * * * * * * * * * * * * * 1 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). 4 PV food list includes approximately 52 species (Panger, 1997). 5 SR food list includes approximately 100 species (MacKinnon, 1995; L. Rose, personal communication). 2 3 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- 58 M.A. PANGER ET AL. TABLE 3. Description of food processing techniques that varied across study sites Processing technique Description “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” Pound3 Rub3 Tap 1 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). 2 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). 3 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 59 VARIATION IN CAPUCHIN FORAGING BEHAVIOR 1 TABLE 4. Processing techniques that vary across sites and their use patterns Lomas Barbudal Food species Tech. Palo Verde U.P. Tech. Santa Rosa U.P. Acacia spp. (fruit) Acacia spp. (thorns) Annona reticulata Eat Eat Eat (rare) C C H Apeiba tibouru Rub P Bactris minor Cecropia peltata Eat (rare) Eat C C Genipa americana Eat C Mangifera indica Manilkara chicle Pithecellobium saman Pound Rub Tap Eat Tap H H H C P Quercus spp. Randia spp. Eat Pound C H Sloanea terniflora Rub C Stemmandenia donnell-smithii Pound P Pound H Sterculia apetala Tabebuia ochracea Rub (fruit inside of husk) Pound Rub Leaf wrap Rub Tap H H C H C C Rub (husk of fruit) Pound Rub Rub H H H H Pound Rub No H H Pound Tap Eat (rare) H C H Automeris spp. caterpillar Insects in branches4 Vertebrate prey (squirrels and coatis) “Army ant following” *** Eat Pound Rub C H P *** Pound Eat H C *** Rub Tap H H Pound Fulcrum P H *** Pound Rub H P *** No Tech. U.P. Rub Rub Pound Rub Pound Rub *** Pound Rub Pound Rub *** H H H H H H Eat Rub Fulcrum2 Pound Eat H C H H H Leaf wrap Rub Pound Rub Tap *** Eat P C C C C C C C C 3 H Leaf wrap Rub Tap H H H Pound Rub Yes H H H 1 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). 2 This information based on L. Fedigan (personnal communication). 3 This information based on R. O’Malley (personnal communication). 4 “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 60 6.4⬃ Phil, Penny Individuals exhibiting the behavior Proximity score for matched dyad3 1 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. 2 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). 4 ⬃, 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). 0 Gina, Keggy Tabebuia ochracea (pound) Sterculia apetala (rub-husk) Larry, Mac 12⬃ Pithecellobium saman (fulcrum) Keggy, Maury 5.1⬃ Bactris minor (pound) 5.63 4.28 7.11* 3.98 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 7.98* 4.07 KK, Larry, Mac, Maury, Phil, Susie 7.07* 3.78 Randia spp (pound) Mangiferas indica (rub) 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 (pound) KK, Penny, Phil M.A. PANGER ET AL. (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. DISCUSSION 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 VARIATION IN CAPUCHIN FORAGING BEHAVIOR 61 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, 62 M.A. PANGER ET AL. 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 time. VARIATION IN CAPUCHIN FORAGING BEHAVIOR 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., 63 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. 64 M.A. PANGER ET AL. CONCLUSIONS 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. ACKNOWLEDGMENTS 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. LITERATURE CITED Adams-Curtis LE. 1990. Conceptual learning in capuchin monkeys. Folia Primatol (Basel) 54:129 –137. Anderson JR. 1990. Use of objects as hammers to open nuts by capuchin monkeys (Cebus apella). Folia Primatol (Basel) 54: 138 –145. Anderson JR. 1996. Chimpanzees and capuchin monkeys: comparative cognition. In: Russon AE, Bard KA, Parker ST, editors. Reaching into thought: the minds of the great apes. Cambridge: Cambridge University Press. p 23–56. Anderson JR, Henneman MC. 1994. Solutions to a tool-use problem in a pair of Cebus apella. Mammalia 58:351–361. Antinucci F. 1989. Cognitive structure and development in nonhuman primates. Hillsdale, NJ: Erlbaum. Antinucci F, Visalberghi E. 1986. Tool use in Cebus apella: a case study. Int J Primatol 7:351–363. Beck B. 1980. Animal tool behavior: the use and manufacture of tools by animals. New York: Garland Press. Boesch C. 1996a. Three approaches for assessing chimpanzee culture. In: Russon AE, Bard KA, Parker ST, editors. Reaching into thought: the minds of the great apes. Cambridge: Cambridge University Press. p 404 – 429. Boesch C. 1996b. The emergence of cultures among wild chimpanzees. Proc Br Acad 88:251–268. Boesch C, Boesch H. 1990. Tool use and tool making in wild chimpanzees. Folia Primatol (Basel) 54:86 –99. Boesch C, Boesch-Achermann H. 2000. The chimpanzees of the Taı̈ Forest: behavioural ecology and evolution. Oxford: Oxford University Press. Boesch C, Tomasello M. 1998. Chimpanzees and human cultures. Curr Anthropol 39:591– 614. Boesch C, Marchesi P, Marchesi N, Fruth B, Joulian F. 1994. Is nut cracking in wild chimpanzees a cultural behaviour? J Hum Evol 26:325–338. Boinski S. 1988. Use of a club by a wild white-faced capuchin (Cebus capucinus) to attack a venemous snake (Bothrops asper). Am J Primatol 14:177–179. Boinski S, Quatrone R, Swats H. 2000. Substrate and tool use by brown capuchins in Suriname: ecological contexts and cognitive bases. Am Anthropol 102:741–761. Bonner JT. 1980. The evolution of culture in animals. Princeton: Princeton University Press. Byrne RW. 1994. The evolution of intelligence. In: Slater PJB, Halliday TR, editors. Behaviour and evolution. Cambridge: Cambridge University Press. p 223–265. Byrne RW. 1996. The misunderstood ape: cognitive skills of the gorilla. In: Russon AE, Bard KA, Parker ST, editors. Reaching into thought: the minds of the great apes. Cambridge: Cambridge University Press. p 111–130. Chapman CA, Fedigan LM. 1990. Dietary differences between neighboring Cebus capucinus groups: local traditions, food availability, or response to food profitability? Folia Primatol (Basel) 54:177–186. Chapman C, Chapman L, Glander K. 1989. Primate populations in northwestern Costa Rica: potential for recovery. Biotropica 21:148 –152. Chevalier-Skolnikoff S. 1990. Tool use by wild Cebus monkeys at Santa Rosa National Park, Costa Rica. Primates 31:375–383. Coussi-Korbel S, Fragaszy DM. 1995. On the relation between social dynamics and social learning. Anim Behav 50:1441– 1453. Custance D, Whiten A, Fredman T. 1999. Social learning of an artificial fruit task in capuchin monkeys (Cebus apella). J Comp Psychol 113:13–23. de Waal FBM, Luttrell LM, Canfield ME. 1993. Preliminary data on voluntary food sharing in brown capuchin monkeys. Am J Primatol 29:73–78. Fedigan LM, Rose LM, Avila RM. 1996. See how they grow: tracking capuchin monkey populations in a regenerating Costa Rican dry forest. In: Norconck M, Rosenberger A, Garber P, editors. Adaptive radiations of neotropical primates. New York: Plenum Press. p 289 –307. Fernandes MEB. 1991. Tool use and predation of oysters (Crassostrea rhizophorea) by the tufted capuchin, Cebus apella apella, in brackish water mangrove swamp. Primates 32:529 – 531. Fox EA, Sitompul AF, van Schaik CP. 1998. Intelligent tool use in wild Sumatran orangutans. In: Parker ST, Mitchell RW, Miles RL, editors. The mentality of gorillas and orangutans: comparative perspectives. Cambridge: Cambridge University Press. p 99 –116. Fragaszy DM, Adams-Curtis LE. 1991. Generative aspects of manipulation in tufted capuchin monkeys (Cebus apella). J Comp Psychol 105:387–397. Fragaszy DM, Bard K. 1997. Comparison of development and life history in Pan and Cebus. Int J Primatol 18:683–701. Fragaszy DM, Boinski S. 1995. Patterns of individual diet choice and efficiency of foraging in wedge-capped capuchin monkeys (Cebus olivaceus). J Comp Psychol 109:339 –348. Fragaszy DM, Visalberghi E. 1989. Social influences on the acquisition and use of tools in tufted capuchin monkeys (Cebus apella). J Comp Psychol 103:159 –170. Fragaszy DM, Visalberghi E. 1990. Social processes affecting the appearance of innovative behaviors in capuchin monkeys. Folia Primatol (Basel) 54:155–165. Fragaszy DM, Visalberghi E. 1996. Social learning in monkeys: primate “primacy” reconsidered. In: Heyes CM, Galef BG, editors. Social learning in animals: the roots of culture. San Diego: Academic Press. p 65– 84. Fragaszy DM, Robinson J, Visalberghi E. 1990. Variability and adaptability in the genus Cebus. Folia Primatol (Basel) 54:113– 118. Frankie GW, Baker HG, Opler PA. 1974. Comparative phenological studies of trees in tropical wet and dry forests in the lowlands of Costa Rica. J Ecol 62:881–919. Frankie GW, Vinston SB, Newstrom LE, Barthell JF. 1988. Nest site and habitat preferences of Cintris bees in the Costa Rican dry forest. Biotropica 20:301–310. Galef BG. 1992. The question of animal culture. Hum Nat 3:157– 178. Gibson KR. 1986. Cognition, brain size and the extraction of embedded food resources. In: Else JG, Lee PC, editors. Primate ontogeny, cognition and social behaviour. Cambridge: Cambridge University Press. p 93–103. VARIATION IN CAPUCHIN FORAGING BEHAVIOR Gibson KR. 1990. Tool use, imitation, and deception in a captive cebus monkey. In: Parker ST, Gibson KR, editors. “Language” and intelligence in monkeys and apes. Cambridge: Cambridge University Press. p 205–218. Goodall J. 1964. Tool-using and aimed throwing in a community of free-living chimpanzees. Nature 201:1264 –1266. Goodall J. 1986. The chimpanzees of Gombe: patterns of behavior. Cambridge, MA: Belknap Press of Harvard University. p 673. Hall KRL. 1963. Observational learning in monkeys and apes. Br J Psychol 54:201–226. Hartshorn GS. 1983. Plants. In: Janzen DH, editor. Costa Rican natural history. Chicago: University of Chicago Press. p 118 – 157. Heyes CM. 1993. Imitation, culture, and cognition. Anim Behav 46:999 –1010. Heyes CM. 1998. Theory of mind in nonhuman primates. Behav Brain Sci 21:101–114. Huffman MA. 1996. Acquisition of innovative cultural behaviors in nonhuman primates: a case study of stone handling, a socially transmitted behavior in Japanese macaques. In: Heyes CM, Galef BG, editors. Social learning in animals: the roots of culture. San Diego: Academic Press. p 267–289. Inoue-Nakamura N, Matsuzawa T. 1997. Development of stone tool use by wild chimpanzees (Pan troglodytes). J Comp Psychol 111:159 –173. Itani J. 1958. On the acquisition and propagation of new food habits in the troop of Japanese monkeys at Takasakiyama. Primates 1:84 –98. Izawa K, Mizuno A. 1977. Palm-fruit cracking behavior of wild black-capped capuchin (Cebus apella). Primates 18:773–792. Jalles-Filho E. 1995. Manipulative propensity and tool use in capuchin monkeys. Curr Anthropol 36:664 – 667. Janzen D, editor. 1983. Costa Rican natural history. Chicago: University of Chicago Press. Kawamura S. 1959. The process of subculture propagation among Japanese macaques. Primates 2:43– 60. Klüver H. 1933. Behavior mechanisms in monkeys. Chicago: University of Chicago Press. Langer J. 2000. The descent of cognitive development. Dev Sci 3:361–379, 385–388. Lefebvre L, Palameta B. 1988. Mechanisms, ecology, and population difussion of socially learned, food-finding behavior in feral pigeons. In: Zentall T, Galef BG, editors. Social learning: psychological and biological perspectives. Hillsdale, NJ: Erlbaum. p 141–164. MacKinnon KC. 1995. Age differences in foraging patterns and spatial associations of white-faced capuchin monkeys (Cebus capucinus) in Costa Rica. M.A. thesis. Department of Anthropology, University of Alberta. Matsuzawa T, Yamakoshi G. 1996. Comparison of chimpanzee material culture between Bossou and Nimba, West Africa. In: Russon AE, Bard KA, Parker ST, editors. Reaching into thought: the minds of the great apes. Cambridge: Cambridge University Press. p 211–232. McGrew WC. 1992. Chimpanzee material culture: implications for human evolution. Cambridge: Cambridge University Press. McGrew WC. 1993. The intelligent use of tools: twenty propositions. In: Gibson KR, Ingold T, editors. Tools, language and cognition in human evolution. Cambridge: Cambridge University Press. p 151–170. McGrew WC. 1998. Culture in nonhuman primates? Annu Rev Anthropol 27:301–328. McGrew WC, Marchant LF. 1997. Using the tools at hand: manual laterality and elementary technology in Cebus spp. and Pan spp. Int J Primatol 18:787– 810. Mundinger PC. 1980. Animal cultures and a general theory of cultural evolution. Ethol Sociobiol 1:183–223 Nishida T. 1987. Local traditions and cultural transmission. In: Smuts BB, Seyfarth RM, Wrangham RW, Struhsaker TT, editors. Primate societies. Chicago: University of Chicago Press. p 462– 474. Ottoni EB, Mannu M. 2001. Semi-free ranging tufted capuchin monkeys (Cebus apella) spontaneously use tools to crack open nuts. Int J Primatol. 65 Panger MA. 1997. Hand preference and object-use in free-ranging white-faced capuchins (Cebus capucinus) in Costa Rica. Ph.D. thesis. University of California, Berkeley. Panger MA. 1998. Object-use in free-ranging white-faced capuchins (Cebus capucinus) in Costa Rica. Am J Phys Anthropol 106:311–321. Panger MA. 1999. Capuchin object manipulation. In: Dolhinow P, Fuentes A, editors. The nonhuman primates. Mountain View, CA: Mayfield Publishing Co. p 115–120. Parker ST. 1990. Why big brains are so rare: energy costs of intelligence and brain size in anthropoid primates. In: Parker ST, Gibson KR, editors. “Language” and intelligence in monkeys and apes. New York: Cambridge University Press. p 129 – 154. Parker ST. 1996. Apprenticeship in tool-mediated extractive foraging: The origins of imitation, teaching, and self-awareness in great apes. In: Russon AE, Bard KA, Parker ST, editors. Reaching into thought: the minds of the great apes. Cambridge: Cambridge University Press. p 348 –370. Parker ST, Gibson KR. 1977. Object manipulation, tool use and sensorimotor intelligence as feeding adaptations in Cebus monkeys and great apes. J Hum Evol 6:623– 641. Parker ST, McKinney ML. 1999. Origins of intelligence: the evolution of cognitive development in monkeys, apes, and humans. Baltimore: Johns Hopkins University Press. Perry S, Rose LM. 1994. Begging and transfer of coati meat by white-faced capuchin monkeys, Cebus capucinus. Primates 35: 499 – 415. Perry S, Baker M, Fedigan L, Gros-Louis J, Jack K, MacKinnon KC, Manson J, Panger M, Pyle K, Rose L. In preparation. Social Conventions in Wild C. capucinus. Phillips KA. 1998. Tool use in wild capuchin monkeys (Cebus albifrons trinitatis). Am J Primatol 46:259 –261. Rettenmeyer CW. 1983. Eciton burchelli and other army ants (Hormiga arriera, army ants). In: Janzen D, editor. Costa Rican natural history. Chicago: University of Chicago Press. p 716 – 718. Rose LM. 1994. Sex differences in diet and foraging behavior in white-faced capuchins, Cebus capucinus. Int J Primatol 15:63– 82. Rose LM. 1998. Behavioral ecology of white-faced capuchins (Cebus capucinus) in Costa Rica. Ph.D. thesis. Washington University, St. Louis. Russon AE. 1996. Imitation in everyday use: matching and rehearsal in the spontaneous imitation of rehabilitant orangutans (Pongo pygmaeus). In: Russon AE, Bard KA, Parker ST, editors. Reaching into thought: the minds of the great apes. Cambridge: Cambridge University Press. p 152–176. Russon AE, Galdikas BMF. 1992. Imitation in ex-captive orangutans (Pongo pygmaeus). J Comp Psychol 107:147–161. Sakura O, Matsuzawa T. 1991. Flexibility of wild chimpanzee nut-cracking behavior using stone hammers and anvils: an experimental analysis. Ethology 87:237–248. Struhsaker T, Leland L. 1977. Palm-nut smashing by Cebus apella in Columbia. Biotropica 9:124 –126. Sugiyama Y. 1993. Local variation of tools and tool use among wild chimpanzee populations. In: Berthelet A, Chavaillon J, editors. The use of tools by human and non-human primates. Oxford: Claredon Press. p 175–187 Sugiyama Y. 1997. Social tradition and the use of tool-composites by wild chimpanzees. Evol Anthropol 6:23–27. Terborgh J. 1983. Five New World primates: a study in comparative ecology. Princeton: Princeton University Press. Tomasello M. 1990. Cultural transmission in the tool use and communicatory signaling of chimpanzees? In: Parker ST, Gibson KR, editors. “Language” and intelligence in monkeys and apes: comparative developmental perspectives. Cambridge: Cambridge University Press. p 274 –311. Urbani B. 1999. Spontaneous use of tools by wedge-capped capuchin monkeys (Cebus olivaceus). Folia Primatol (Basel) 70:172– 174. van Schaik CP, Fox EA, Sitompul AF. 1996. Manufacture and use of tools in wild Sumatran orangutans: implications for human evolution. Naturwissenschaften 83:186 –188. 66 M.A. PANGER ET AL. van Schaik CP, Deaner RO, Merrill MY. 1999. The conditions for tool use in primates: implications for the evolution of material culture. J Hum Evol 36:719 –741. Visalberghi E. 1987. Acquisition of nut-cracking behaviour by 2 capuchin monkeys (Cebus apella). Folia Primatol (Basel) 49: 168 –181. Visalberghi E. 1988. Responsiveness to objects in two social groups of tufted capuchin monkeys (Cebus apella). Am J Primatol 15:349 –360. Visalberghi E. 1990. Tool use in Cebus. Folia Primatol (Basel) 54:146 –154. Visalberghi E. 1997. Success and understanding in cognitive tasks: a comparison between Cebus apella and Pan troglodytes. Int J Primatol 18:811– 830. Visalberghi E, Fragaszy DM. 1990. Do monkeys ape? In: Parker ST, Gibson KR, editors. “Language” and intelligence in monkeys and apes: comparative developmental perspectives. Cambridge: Cambridge University Press. p 247–273. Visalberghi E, Limongelli L. 1996. Acting and understanding: tool use revisted through the minds of capuchin monkeys. In: Russon AE, Bard KA, Parker ST, editors. Reaching into thought: the minds of the great apes. Cambridge: Cambridge University Press. p 57–79. Visalbeghi E, McGrew WC. 1997. Cebus meets Pan. Int J Primatol 18:677– 681. Visalberghi E, Trinca L. 1989. Tool use in capuchin monkeys: distinguishing between performing and understanding. Primates 30:511–521. Visalberghi E, Vitale AF. 1990. Coated nuts as an enrichment device to elicit tool use in tufted capuchins (Cebus apella). Zoo Biol 9:65–71. Wanatabe K. 1994. Precultural behavior of Japanese macaques: longitudinal studies of the Koshima troops. In: Gardner RA, Gardner BT, Chiarelli B, Plooij FX, editors. The ethological roots of culture. Dordrecht: Kluwer. p 81–94. Westergaard GC. 1995. The stone-tool technology of capuchin monkeys: possible implications for the evolution of symbolic communication in hominids. World Archaeol 27:1–9. Westergaard GC, Fragaszy DM. 1987. The manufacture and use of tools by capuchin monkeys (Cebus apella). J Comp Psychol 101:159 –168. Westergaard GC, Suomi SJ. 1993a. Use of a tool-set by capuchin monkeys (Cebus apella). Primates 34:459 – 462. Westergaard GC, Suomi SJ. 1993b. Hand preference in the use of nut-cracking tools by tufted capuchin monkeys (Cebus apella). Folia Primatol (Basel) 61:38 – 42. Westergaard GC, Suomi SJ. 1994a. Aimed throwing of stones by tufted capuchin monkeys (Cebus apella). Hum Evol 9:323–329. Westergaard GC, Suomi SJ. 1994b.The use and modification of bone tools by capuchin monkeys. Curr Anthropol 35:75–77. Westergaard GC, Suomi SJ. 1994c. Asymmetrical manipulation in the use of tools by tufted capuchin monkeys (Cebus apella). Folia Primatol (Basel) 63:96 –98. Westergaard GC, Suomi SJ. 1995. The manufacture and use of bamboo tools by monkeys: possible implications for the development of material culture among East Asian hominids. J Archaeol Sci 22:677– 681. Westergaard GC, Suomi SJ. 1997. Transfer of tools and food between groups of tufted capuchins (Cebus apella). Am J Primatol 43:33– 41. Westergaard GC, Greene JA, Babitz MA, Suomi SJ. 1995. Pestle use and modification by tufted capuchins (Cebus apella). Int J Primatol 16:643– 651. Westergaard GC, Lundquist AL, Kuhn HE, Suomi SJ. 1997. Ant-gathering with tools by captive tufted capuchins (Cebus apella). Int J Primatol 18:95–103. Whiten A. 1989. Transmission mechanism in primate cultural evolution. Trends Ecol Evol 4:61– 62. Whiten A. 1996. Imitation, pretense, and mindreading: secondary representation in comparative primatology and developmental psychology? In: Russon AE, Bard KA, Parker ST, editors. Reaching into thought: the minds of the great apes. Cambridge: Cambridge University Press. p. 300 –324. Whiten A, Ham R. 1992. On the nature and evolution of imitation in the animal kingdon: reappraisal of a century of research. In: Slater PJB, Rosenblatt JS, Beer C, Milinski M, editors. Advances in the study of behavior, volume 21. San Diego: Academic Press. p 239 –283. Whiten A, Goodall J, McGrew WC, Nishida T, Reynolds V, Sugiyama Y, Tutin CEG, Wrangham RW, Boesch C. 1999. Cultures in chimpanzees. Nature 399:682– 685. Wolfe LD. 1981. Display behavior in three troops of Japanese macaques (Macaca fuscata). Primates 22:24 –32.