Generative Aspects of Manipulation in Tufted ...

Copyright 1991 by the American Psychological Association, Inc. 0735-7036/91/S3.00

Journal of Comparative Psychology 1991, Vol. 105, No. 4, 387-397

Generative Aspects of Manipulation in Tufted Capuchin Monkeys (Cebus apelld) Leah E. Adams-Curtis Washington State University

Dorothy M. Fragaszy University of Georgia

Evaluating the cognitive and ontogenetic bases of tool use in primates requires comparative data on the generative nature of manipulation, including the frequency and variety of combinations of actions and objects. Thirty-one tufted capuchins (Cebus apelld) of 3 age groups devoted significant proportions of time to interaction with objects and substrates. Activity that combined an object with a substrate occurred often; activities that combined 2 portable objects were less frequent. Predictions drawn from neo-Piagetian theory of an ontogenetic link between combinatorial behaviors and the onset of tool use were not supported. The frequency and generative nature of capuchins' manipulative activity, particularly acts combining objects and substrates, could account for their proclivity to use tools. The use of tools by capuchins need not involve the representational abilities proposed by neo-Piagetian theory.

We describe interactions with objects in tufted capuchins (Cebus apella), with an emphasis on those characteristics of the species-normal manipulative repertoire expected to contribute to tool use. Such characteristics include the variety of acts directed to objects, the frequency with which the same act is directed toward different objects, and the absolute and relative frequencies of acts that place an object in relation to another object or to a substrate. These characteristics reflect the generativity of manipulation. We argue that comparative study of generativity of manipulation will provide insight into the behavioral processes supporting tool use. Tool use has rarely been reported in New World monkeys other than Cebus, but it has been reported more frequently in a variety of Old World primates (see Beck, 1980, for a review). We rely on Beck's definition of tool use: In essence, a detached object must be used in the achievement of an effect on another object or on a substrate. Recent reports from the field of tool use by primates include, for example, Hohmann's (1988) report of a case of simple tool-use in 3 lion-tailed macaques (Macaco silenus), which used a leaf to roll an irritating insect chrysalis. Several investigators, most recently Westergaard (1988), have reported that baboons in captivity use sticks. Lion-tailed macaques in captivity have been observed to use sticks as probes (Westergaard, 1988), to

insert long branches into wire mesh and then to use the sticks as perches, and to prop sticks against walls and then use them as ladders (Westergaard & Lindquist, 1987). Whether creation of new support surfaces (perches and ladders) may be considered tool use is debatable, but the actions nevertheless indicate a capability for creative manipulation. Given their phylogenetic status as New World monkeys, it is anomalous that no other genus of monkey rivals Cebus in the number and diversity of tool-using reports (Anderson, 1990; Antinucci & Visalberghi, 1986; Chevalier-Skolnikoff, 1989; Fragaszy & Visalberghi, 1989; Westergaard & Fragaszy, 1985, 1987; see Beck, 1980, S. Parker & Gibson, 1977, and Visalberghi, 1990, for reviews). For example, capuchins have used hard objects to pound open nuts, sticks as rakes, probes, clubs, and levers, boxes to stack and climb on, soft material as sponges, and cups to hold liquids and small objects. It appears that capuchins use tools in captivity more frequently than any other genus except chimpanzees and in more situations than Old World monkeys. No Old World monkey has been reported to use a tool to pound something open or to use sponges, cups, or clubs. Moreover, a link between toolusing capacity and manipulative variety, especially relational and combinatorial actions, seems more obvious in capuchins than in Old World monkeys. Capuchins have been seen to perform manipulative acts rarely or never seen in other species, such as pounding hard foods on a substrate to crack them open, and banging two objects together (Fragaszy, 1986; Izawa, 1979; Izawa & Mizuno, 1977; Struhsaker & Leland, 1977). The variety of manipulative and tool-using behaviors expressed by capuchins and the occurrence of relational and combinatorial behaviors in their manipulative activity led S. Parker and Gibson (1977) to suggest that capuchins' toolusing behaviors, like those of chimpanzees, indicate the use of cognitive abilities falling into Stage 5 and 6 in a modified Piagetian scheme of sensorimotor intelligence. That is, these behaviors indicate the presence of representational capacities and the occurrence of deliberate experimentation to discover means-ends relations (see also Chevalier-Skolnikoff, 1989). Actions involving the combination of two portable objects

This work was supported by National Science Foundation Grant 85-03603 and National Institutes of Health Grant MH-41543 to Dorothy M. Fragaszy. Preparation of the article was supported by a Research Scientist Development Award from the Public Health Service to Dorothy M. Fragaszy. We thank J. Whipple for statistical advice, J. Teberg for programming assistance, and G. Giesick and G. Canul for assistance with data tabulation. A. Fristensky, J. Baer, A. Tedeschi, A. Marquis, P. Smith, M. Hackney, and D. Nylan all assisted with data collection. We thank W. London of the National Institutes of Health for the loan of the adult core of the breeding colony. This work was conducted in accord with all regulations for the humane treatment of laboratory animals. Correspondence concerning this article should be addressed to Dorothy M. Fragaszy, Psychology Department, University of Georgia, Athens, Georgia 30602. 387

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DOROTHY M. FRAGASZY AND LEAH E. ADAMS-CURTIS

with each other are viewed by these authors as particularly relevant to tool-using. The same or similar cognitive abilities underlying tool use are critically involved, in the neo-Piagetian scheme, with imitation of novel behaviors, prelinguistic communication, and many other cognitive accomplishments of human children in the 2nd and 3rd years of life (Bates & Snyder, 1987; Harding, 1984; Sugarman, 1984). The coherent neo-Piagetian interpretation proposed by S. Parker and Gibson (1977) to link tool-using behaviors in primates with other manifestations of Stages 5 and 6 tertiary sensorimotor intelligence requires careful empirical evaluation. It produces, after all, a rather strong and startling (phylogenetically) hypothesis that capuchins possess qualitatively different cognitive structures than all other monkeys. However, the presence of tool-using behaviors in an animal or a species cannot, by itself, serve as evidence that these behaviors require the cognitive processes attributed to them by their classification according to a neo-Piagetian framework. Data from outside the classificatory scheme are needed for this purpose. Experimental data on tool-using skills in various revealing contexts (Visalberghi & Trinca, 1989), observations of the acquisition of tool-using behaviors (Fragaszy & Visalberghi, 1989; Visalberghi, 1987; Westergaard & Fragaszy, 1987), and data on the species-normal patterns of manipulation outside of tool-using contexts can all be used to test various predictions drawn from neo-Piagetian theory. An alternative, behavioristic formulation to relate manipulative activity to tool use must also be evaluated. Certain characteristics of manipulative activity might be strongly correlated across species or across ages within species with observed differences in the frequency and forms of tool use because they affect the probability that an object's use as a tool will be discovered (e.g., Baldwin, 1989). Characteristics of the manipulative repertoire we expect may affect the probability of a discovery of tool use include (a) the variety of acts directed toward the same object, (b) the frequency with which the same act is directed toward different objects (c) the frequency and proportion of acts that place an object in relation to another, and (d) the frequency or proportion of activity in which an object is placed in relation to a substrate. These can all be considered creative recombinations, or generative properties, in the motor domain (Bruner, 1974). We refer to acts described in (c) and (d) as combinatorial. The primary comparative hypothesis to which this view leads is that the generative characteristics of manipulation are sufficient, and in fact the best, predictors of species differences in the use of tools. This hypothesis is not in conflict with neoPiagetian predictions that link manipulative variety and discovery of means-ends relations, as it makes no claims in regard to the cognitive bases for these behaviors. Rather, it places greater emphasis on normative features of manipulation than on the occasional specific action. We favor this hypothesis for several reasons. First, the neo-Piagetian perspective, as used by Chevalier-Skolnikoff (1989), for example, reclassifies behaviors in terms of their (inferred) requisite cognitive structures. However, the behaviors themselves are the only evidence for the existence of the inferred structures. This reasoning is circular (Adams-Curtis, 1989; Baldwin, 1989). Second, because there are subjective components to

the classification of tool-using behavior (such as the subject's intentions), the method is difficult to standardize across species or laboratories. An approach that relies strictly on overt features of behavior is more readily applied across species and by different investigators. The behaviorist advantages of parsimony and objectivity would be offset, however, if neoPiagetian theory had greater powers to explain variation in other aspects of manipulation. We take this up later in regard to ontogenetic explanations. In this report, we present data on the generative features of normal manipulation in capuchin monkeys. These data will serve as a starting point for comparisons of the capuchins' manipulative repertoire with those of other species, needed for an empirical comparative evaluation of the behavioral and neo-Piagetian hypotheses about the correlates of tool use. We predicted that capuchins would exhibit higher levels of generative manipulation than other species of monkeys, in keeping with their status as common users of tools. We do not yet have a basis for predicting the relative importance of each of the four distinctive aspects of generativity listed earlier. Comparative data are available on some aspects of the manipulative repertoire in primates from C. E. Parker (1974) and from Torigoe (1985). Torigoe's study was an explicit replication of C. E. Parker's original study with many more species and more animals for many species. These authors both studied animals housed in rather barren settings (cages fitted only with benches, a water source, and food). In both studies, one or two simple experimental manipulanda (a tethered length of knotted nylon rope in C. E. Parker's study and an untethered, knotted length of nylon rope and a wooden block small enough to be held in one hand in Torigoe's study) were presented for short periods, and data were collected on activity with these objects. In C. E. Parker's study, with 4 adult capuchins (C. capucinus), the animals did not vary significantly from other species of monkeys in the frequency of response, number of body parts used, or number of actions performed. Torigoe studied many more capuchins (N = 20, 3-7 animals of each of four species in the genus; ages were not reported). These monkeys shared with apes a more varied use of actions and body parts than other monkeys and more frequent use of actions that did not involve the substrate, such as drop, drape, swing, and throw (see Torigoe, 1985, Figure 4). The manipulanda presented, however, did not lend themselves to activity that combined two portable objects. Understandably, Torigoe's discussion on the complexity of manipulation is limited to a comparison of reliance on the substrate (floor, wall, wire mesh, or water pan) in a global sense (primary manipulation) and use of the substrate in a more specific relation to the manipulandum (secondary manipulation). Capuchins were similar to macaques, guenons, mangabeys, baboons, and the great apes in the number of distinctive forms of secondary manipulations performed (see Torigoe, 1985, Figure 6). In sum, the comparative data concern the form of activity with simple novel manipulanda by otherwise manipulandadeprived animals. Torigoe's (1985) data, but not C. E. Parker's (1974), suggest greater productivity among capuchins than other monkeys. Given the limited circumstances of the testing procedure, the data from these studies cannot speak to the

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GENERATIVITY OF MANIPULATION IN CAPUCHINS

normal frequency of manipulation, the normal distribution of actions, the form or frequency of actions that combine two portable objects, or the productive character of manipulation with various objects and surfaces. In a recent study with social groups of capuchins housed similarly to those studied by C. E. Parker (1974) and Torigoe (1985; i.e., lacking manipulanda other than food), Visalberghi (1988) used wooden blocks as experimental objects. She presented many wooden blocks simultaneously, left them in for long periods, and noted the identities of animals that manipulated them. Actions that combined one block with another were observed occasionally but were not a prominent feature of behavior. However, vigorous interactions combining the object and a substrate, such as pounding and rubbing, were frequent. Visalberghi's (1988) data show that capuchins engage in combinatorial activity outside of tool-using contexts, and they provide the best data yet on within-species variability in capuchins in the frequency of exploratory manipulative activity. They are limited, however, in the same way that C. E. Parker's and Torigoe's data are limited, by the focus on rather simple experimental manipulanda, and the possibility that the results reflect the chronic absence of other objects which Visalberghi's (1988) subjects experienced. Fragaszy and Visalberghi also presented wooden blocks, like those used by Visalberghi (1988), to other animals, which largely ignored the wooden blocks in favor of manipulating other objects routinely present in their cages (Fragaszy & Visalberghi, personal observation, November 1986). To return to ontogenetic issues, neo-Piagetian theory leads to two predictions about the appearance of tool use and combinatorial behavior that we can address with our data. First, tool use and the appearance of combinatorial behavior ought to be roughly coincidental, as both are supported initially by Stage 5 and later Stage 6 sensorimotor intelligence. For example, in Stage 5, infants are said to explore the potentials of objects through experimentation, such as discovering that an object can be used to act on another object or a surface. This activity can lead to the discovery that an object can be used as a tool. Experimentation with objects and their use as tools both involve a specific cognitive structure (Chevalier-Skolnikoff, 1989). Once combinatorial behaviors appear in the repertoire, the use of tools ought to be close behind. From our point of view, in contrast, discovery of tool use is probabilistic and therefore more sensitive to the frequency of combinatorial activity than to its onset. We looked for evidence to support one of these competing hypotheses by comparing monkeys' age at onset of tool use observed in other studies with the age of appearance of combinatorial behaviors in this study. The second prediction we draw from neo-Piagetian theory is that when combinatorial activities appear, they ought to be associated with a blossoming of combinatorial behaviors, as the young animal uses its cognitive skills in the service of experimentation and discovery (Chevalier-Skolnikoff, 1989). Therefore, soon after the appearance of combinatorial behaviors in the repertoire, young animals ought to (a) combine objects in several actions, (b) use a wide variety of objects in combinations, and (c) perform these combinations at a relatively greater rate than older juveniles. Older juveniles, having

accommodated these skills, ought to have a lower rate of combinatorial actions. This prediction is examined by comparing animals' frequency of acts with two objects or acts of placing an object in relation to a substrate in the months after their appearance (months 6 to 9) with the frequency of the same actions among 33- to 36-month-old juveniles. Methodologically, our study is unlike previous efforts to describe manipulation in monkeys (Joubert & Vauclair, 1986; C. E. Parker, 1974; Torigoe, 1985; Visalberghi, 1988) in that we observed monkeys housed in rather rich social and physical environments, which support a great variety of actions, including combinatorial actions, and and that we scored semicontinuously all actions with all objects by focal animals, rather than restrict our interest to specific manipulanda or to a subset of manipulative acts. This was done so that we were able to examine the absolute and relative frequency of specific actions, including acts with two objects or with an object and a substrate (combinatorial behaviors). Consequently, we were able to determine how likely an animal is to do any specific act and the proportion of its activity made up of behaviors most often linked to discovery of novel properties and tool use. Method Design Thirty-one animals were observed undisturbed in the home cage for 10-min periods at regular intervals over 13 months. Objectdirected activities were scored according to form of the acts and the targets involved. A total of 727 observation sessions (average of 23 per subject, total of 121 hr of observation) constitutes the data set presented in this article.

Subjects and Housing Two breeding groups of tufted capuchins (Cebus apella), established in 1982 and 1984, served as subjects in the study. The membership of the groups changed somewhat over the course of the study, but the general composition of the groups did not. Each group was composed of an adult male, 5-6 adult females, and juveniles and infants born to females in the group. Each group had 2-8 immature animals. Twelve adult females, 3 adult males, 8 juveniles (13-39 months, 5 males and 3 females), and 8 infants (0-12 months, 6 females and 2 males) were observed. All the immature subjects were reared in our laboratory. One adult male was wild caught as a young adult; others were raised in captivity. None of the immature animals contributed data to both the infant and the juvenile age groups. The subjects were housed in double-room indoor cages (2.5 m wide x 2.5 m high x 6.0 m deep and 2.5 x 2.5 x 3.0 m) at the Washington State University Primate Center. Each set of rooms was equipped with perches, water sources, straw bedding, tree cuttings, and various manipulanda selected to encourage varied manipulative activity (e.g., washers strung on bolts and chain and small wheels threaded on wire cable). A rubber tire, plastic hangers, and a large climbing rope were suspended from the ceiling to provide locomotor opportunities. Small foods (seeds, diced vegetables, and cut fruit) were strewn into the straw a few times a week. Commercial monkey chow and water were available ad lib.

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Procedure Data were collected with a semicontinuous recording method by an observer seated behind a one-way silvered window. A subject was selected for observation on a rotating schedule, with balanced representation of animals within the same age group. An observational session consisted of 10 consecutive 1-min sampling periods. During each 1-min period, alternating 5-s intervals were devoted to observing and to recording. Each unique combination of an act and object observed during the 5-s interval was recorded according to the categories listed in Tables 1 and 2. Although the act does not involve

Table 1 Vocabulary Used for Acts Act Directed look

Hit, slap, or bang Bite or masticate

Push, pull, or tear

Directed reach

Insert or extract Lick, sniff, or mouth

Scratch, pick, or tap Handle Sift

Hold or carry

Rub, roll, or smear

Drink or soak Unknown

Table 2 Vocabulary Used for Objects Object Cage Browse Toys

Feces Self

Usage

Look at an object or another animal for 3 seconds or more from less than 1 meter away. Scored only when there was no contact. Vigorous hit of any target with the hands, whether or not the subject held an object. Vigorous contact with the mouth, including use of the teeth. Simultaneous contact by a hand was not required. Push or pull an object along a substrate, or use opposing force. An object torn or broken could be held in both hands or by the hands and mouth. Chow was never scored as torn or broken. Scored only for infants less than 4 months old. Reach toward an object, but make only passing or no contact. Insert an object or an arm, hand, or fingers into a substrate. Sniff, place in the mouth, or lick an object to investigate it. Distinguished from bite or masticate by the vigor of the act and by the lack of use of the teeth. Use the fingers to investigate an object in gentle tactile exploration. Manipulate an object bimanually, turning or changing the object's orientation in some way. Search through the straw bedding by sweeping motions, by lifting and moving the bedding, or by moving the hands through the straw. Hold an object while stationary or moving, including carrying objects in the mouth. The distinguishing feature is lack of movement of the object while in the hand or mouth. Rub an item or the hand along a surface in continuous contact. Distinguished from push, pull, or tear by the hand's being placed flat on the surface. Drink water or wet objects by placing them beneath running water. Act that cannot be identified.

Food Unknown

Definition

All parts of the home cage, including walls, perches, floor, light covers, visual barriers, and tethers. Straw and tree branches Tethered but moveable locomotor surfaces (plastic hangers, tires, and ropes) and smaller objects (wheels and bolts), and their tethers. Also, loose objects in the cage not defined by other object types. Self-explanatory Any part of the subject's body. Scored when the body part was used as a substrate (for example, lick chow from self) or when the body was used to act on a substrate (for example, rub hand on wall). Selfmaintenance behaviors, such as grooming, were not scored. Self-explanatory Scored when the object could not be identified by the observer.

direct manual contact, close visual inspection (identified as directed look) was scored to encompass exploratory activity of infants and also to make these data comparable to data on foraging activities obtained in field studies. At the end of 6 consecutive cycles of observation and recording of the focal animal, a record was made of each animal within 1 m of the focal animal. The activity and identity of each neighbor were recorded with the same vocabulary as for the focal animal. Observations were made between 0900 hr and 1900 hr, at times when the groups were undisturbed. Only the focal data are treated here. The observational method was developed over a period of several months before the collection of these data. New observers were trained in the method to acceptable levels of interobserver reliability before they collected data. We calculated reliability in two ways, as a percentage of intervals with one or more acts in agreement and as percentage of intervals with perfect agreement. Observers attained greater than 90% on the former and greater than 80% on the latter in at least two consecutive observation periods before commencing data collection. Reliability observations used animals between 10 months and 4 years of age as focal animals, as these were the most active subjects and recording their activity was the most demanding. New observers were trained during the course of the study and achieved reliability with the original and secondary observers. In this way, observer drift was prevented.

Analysis The frequency of specific acts, act-object pairings, combinations of two particular objects, and use of specific objects singly over all observations per subject served as the raw data. Activity was also classified post hoc with loosely functional criteria linking acts and objects into five categories: food-directed, browse-directed, surfaceexploratory, social, and variable manipulation (see Table 3). Five categories of relational actions were defined by the relation between the object and substrate, as shown in Table 4.

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Objects Involved in Manipulation

Table 3 Functional Activity Category Surface exploration Food-directed

Browse-directed

Social

Variable manipulation

Distinguishing features Lick, sniff, mouth, scratch, pick, or tap the cage or toys. Any act in which food was acted on, including acts in which food was combined in some way with a substrate, such as bang chow on the wall. Any act in which browse was acted on, including acts in which browse was combined in some way, such as rub browse on the wall. Any act in which another animal was acted on. This consists primarily of directed look and directed reach. Any activity not classified above.

To examine differences across age groups, multivariate analyses of variance (MANOVAs) were run for each variable, transformed to an hourly rate and into the proportion of total acts in which the variable of interest was scored, with age group as the single independent variable. MANOVAs of rates used untransformed values; analyses of proportions used logit transformations in which the most frequently occurring variable served as the denominator. Wilks's lambda (approximate F) was used in determinations of statistical significance. Subsequently, one-way analyses of variance (ANOVAs) were run with age as the independent variable and with the subject within the group as the error term for specific acts and act-target classes. Arcsin transformations were used for proportional data for ANOVAs; untransformed data were used for ANOVAs of rates. Post hoc pairwise comparisons were made between age groups with least significant difference (LSD) tests. The ANOVA model explained .50 of the variance or better for most variables and somewhat less (.20-.30) for some of the rarer single acts, combinations of objects, and act classes.

Results Frequency of Manipulation Manipulation occurred on 51 % of all intervals of observation. Two hundred eleven unique actions were observed (actions in which a subject contacted another animal were scored only once, regardless of the identity of the other animal). Multiple acts often occurred within a 5-s interval, so that for some animals the overall frequency of acts exceeded the number of intervals in which manipulation was scored. The number of intervals of occurrence per hr for all acts is presented for each age group in Table 5. Overall, bite occurred in 28% of all actions, twice as often as any other act. Three acts (scratch, hold, and lick) that generally involve a simple orientation of body to surface or object were the next most frequent, and each occurred in 13%-14% of actions. All other acts occurred in 5% or less of total acts scored. The vigorous acts of hit, push, and rub occurred in 5%, 5%, and 4% of all actions scored, respectively.

All acts were performed with a variety of objects (except sift, which by definition could occur only with straw). In short, there was no evidence for specialized acts used only for specific objects. Actions with only one object or the cage alone dominated manipulative activity (see Table 6). The cage was contacted on 37% of all acts and was the only contact (i.e., no objects were placed in relation to the cage) for 23% of all acts. Food was manipulated in 32% of all acts and in 45% of acts in which only one object was contacted. Browse accounted for 26% of actions with a single object, toys for 17%, social for 6%, and self, feces, and unknown made up the balance. Actions with an object placed in relation to the cage occurred 16 times per hr and accounted for 57% of all acts that involved placing an object in relation to something else (see Table 7). These acts included pounding an object on the wall, inserting straw into holes in the wall, rubbing an object against the wall, and licking or picking food off of the wall. All portable objects (food, browse, toys, and feces) were placed in relation to the cage. Thus, not only was the action of placing an object in relation to the cage common, it was variable as well. Manipulation of a part of the body on a substrate with a particular orientation, such as inserting a hand through the wire mesh or rubbing a hand down a bar, was the next most common relational act (32% of the total), followed by an object in combination with a part of the body (7%), for which the body serves more or less as the substrate. Portable objects combined with each other or with toys, which were tethered, accounted for 3% of all relational acts.

Action Classes As a second means of examining the form of manipulative activity, we classed actions into five broad functional cate-

Table 4 Categories of Combinations of Objects With Other Objects or in Relation to a Substrate Category Object to enclosure

Self to substrate

Object to body

Object to toy Object to object

Definition Place an object in relation to the cage. Examples: Bang chow on the wall, insert straw into wire mesh. Place the hand or arm in relation to the cage. Example: Insert finger into a hole in the wall. Manipulate an object in relation to the body. These actions involve using the body as a substrate. Examples: Lick food from self, pick straw from self. Place an object in relation to a toy. Example: Insert straw through a hanger. Place an object in relation to another. Example: Hit food against food.

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Table 5 Mean Occurrences per Hour for Acts Act Infants Juveniles Adults 72 202 108 Single object 13 65 Cage only 61 9 11 33 Object with the cage Object with object' 0.5 7.40, ps < .003,

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Figure 1. Acts as proportions of each age group's activities. (The sloping line shows the distribution of activity in adults.)

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ison of these data with data on capuchins in natural environments and offer a suggestion as to why tool use is observed more rarely in natural environments than in captivity. Infants

Generativity in Manipulation and Its Relation to Tool Use Enclosure Browse Toys Food

Juveniles

Feces Self Social Unknown

As the most common relational act performed by capuchins was placing an object in relation to a surface, a model of tool use based on generativity would suggest that tool use in this species is most likely where the tool is used in relation to a substrate. The data are consistent with this interpretation. For example, capuchins learn fairly readily to dip or probe into an enclosure with an object (Visalberghi, 1990; Westergaard & Fragaszy, 1987). Other object-substrate combinations that are not classed as tool use, such as washing sand off food by placing it into water (Visalberghi & Fragaszy, 1990b), also occur readily in capuchins. Pounding an object with another (e.g., in cracking nuts), observed repeatedly in captive capuchins (Anderson, 1990; Antinucci & Visalberghi, 1986; Fragaszy & Visalberghi, 1989; Visalberghi, 1987) and the only form of tool use observed in wild capuchins (Boinski, 1988), also involves a substrate (against which the second object is broken).

Adults

Figure 2. Proportions of each age group's acts that involved a specific single object.

Infants

Discussion This study has demonstrated that capuchins perform a wide variety of actions with the full assortment of objects available. Manipulation is frequent in all animals past a few months of age, and a measurable proportion of it involves two objects or an object and a surface. Hence, considerable generativity was evident in four dimensions: the variety of actions with the same objects, the variety of objects to which the same act is directed, and the frequency and proportion of relational behaviors. As comparative data are not yet available for these measures, it is premature to claim that capuchins exceed other species of monkeys in the generativity of their manipulation. Nevertheless, the available data (Torigoe, 1985) suggest this is the case, especially with respect to relational behaviors. We also suspect that capuchins exceed other species of monkeys (including the manipulative omnivores, such as baboons) in the sheer frequency of any form of manipulative activity. Are these characteristics sufficient to account for the discovery of tool use, and the types of tools discovered, in captive capuchins? To provide an initial answer to this important question, we consider the relation between generativity and the forms of tool use seen in capuchins, the age differences in generative characteristics, and the relation between the onset of relational behaviors and tool use. We close with a compar-

Juveniles

Explore FoodDirected BrowseDirected Social Other

Adults

Figure 3. Categories of activities as proportions of each age group's activity.


Other

Social

I Adults E3 Juveniles

Browse

H Infants Food

Explore

20

40

60

80

100

120

Number of occurrences per hour

Figure 4. Number of occurrences per hr for each age group for each category of activity.

In many cases in which the acquisition of tool use or another form of useful manipulative innovation has been closely followed, exploratory or playful actions either precede or accompany first instances (e.g., Fragaszy & Visalberghi, 1989; Visalberghi & Fragaszy, 1990b). In this respect, tool use in capuchins follows Bruner's (1974) conception that creative recombination underlies the acquisition of novel behaviors. This view is congenial to both neo-Piagetian and behaviorist conceptions of innovation. A more telling characteristic, with respect to neo-Piagetian views of tool use, is that improvement in skill follows the pattern observed in associative learning, that is, gradual extinction of inefficient behaviors (Visalberghi, 1987). Moreover, when new tasks are presented, behaviors that succeeded with previous tasks are often the first attempted with the new task. These features are consistent with models of behavioral innovation based on behaviorist principles presented by Epstein (1987; Epstein & Medalie, 1983). Epstein referred to the reappearance of previously successful behaviors as resurgence and also described the interconnection of repertoires, which logically contribute to the discovery of tool use when sequences of actions are necessary (such as moving a box to the appropriate place and then mounting it to reach an object). Both of these phenomena can be translated into Piagetian concepts of assimilation and accommodation, but in our view they are more parsimoniously interpreted as aspects of generativity present in manipulation than of cognitive structures mediating the use of objects.

Age Differences in Manipulation With Respect to Generativity The frequency of maintenance activities (feeding and drinking) did not differ between adults and juveniles, which indicates that the time the capuchins used to feed themselves was about the same for the two age groups. However, juveniles were more active manipulators than were adults, and they devoted a greater proportion of their manipulative activity to nonmaintenance. For example, juveniles manipulated substrates and toys more frequently and in a greater proportion of acts than did adults. Furthermore, juveniles performed all relational acts more frequently than adults. Last, juveniles performed vigorous acts (hit, push, and rub) at a significantly

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higher rate than adults. In short, juveniles exhibited the greatest degree of generativity in their manipulation, and most of their manipulation involved objects other than food. Manipulation in juveniles often had a distinctly playful character and was sometimes incorporated into whole-body play sequences. For example, juveniles sometimes swing 360° around a bar while holding an object, banging the object against the substrate on each pass-by (Adams-Curtis, Jeffers, & Brumfield, 1990). We point out, however, that juveniles in our groups do not devote significantly more time to locomotion, play, and acrobatics (which together constitute the overwhelming majority of energetic activities) than do adults (Adams-Curtis, 1990). Adults devote 14% of daytime activity to locomotion and other motorically energetic pursuits; the figure for animals between 1 and 4 years old is 19%.

Ontogeny of Manipulation and Tool Use Compared The earliest reported age of first tool use in capuchins is at 9 months for a dipping task that required inserting a stick or straw to obtain syrup (Westergaard & Fragaszy, 1987). Five infants born into our groups were present during extensive presentation of tool-using tasks: Between the ages of birth to 6 months, a task that involved the insertion of a rod, similar to the task in Westergaard and Fragaszy (1987), was introduced, and between the ages of 6-10 months, a task that involved pounding a metal object on a substrate (Fragaszy & Visalberghi, 1989) was introduced. None of the infants solved these tasks or attempted solution, whereas 2 juveniles out of 4 in the age range of 18 months to 2 years did use the tools. When a dipping task and a pounding task were presented to the groups over a year later, 4 of the same 5 animals, now between 20 and 24 months of age, exhibited tool use, but neither of the 2 subjects aged 6-12 months did (Fragaszy, Vitale, & Ritchie, 1990). In all these tasks, use of the tool involved placing an object in relation to a substrate, a category of action which appears at about 6 months of age. Moreover, by 6 months, infants are competent at independent locomotion and spend more than 50% of their day off a carrier (Fragaszy, Baer, & AdamsCurtis, in press). Thus motor competence and relational actions are present months before the appearance of tool use. These data suggest that tool use does not appear concurrently with the first appearance of the relevant form of relational behaviors. They do not support the simplest prediction drawn from neo-Piagetian theory of coincidental occurrence of tool use and topologically similar relational actions. To preserve an association between the ontogeny of relational actions and tool use, one must propose that other forms of relational actions, which appear at the end rather than in the middle of the 1st year, are diagnostic of cognitive development related to tool use. The proposition seems weak, however, because the appearance of tool use is still delayed in most animals in relation to the appearance of all forms of relational behaviors. Moreover, the finding that relational behaviors are not more frequent in 6- to 9-month-olds than in 33- to 36-month-olds further weakens the explanatory power of neo-Piagetian models that link cognitive development and tool use.

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Comparison With Capuchins in Natural Environments The rate with which manipulation occurred, the proportion of it that constituted vigorous activity, and the dominance of interest in object-substrate combinations are in line with observations on capuchins in natural settings (Fragaszy, 1986; Robinson & Janson, 1986). Manipulations of an object against the substrate (such as hitting) were the most common combinatorial actions in this study and are so in nature. In captivity, actions with a single object were far and away more common than combinatorial actions. Comparable quantitative field data are not available, but informal observations suggest this is also true in natural settings (Fragaszy, 1986). Adult males and females interacted with objects at equivalent rates in this study, in contrast to Visalberghi's (1988) findings. In nature, female capuchins devote more time than males to foraging activities and, particularly, more time than males to persistent manipulation of woody substrates (Fragaszy, 1990). The sex difference for males in manipulative activity in Visalberghi's (1988) study probably reflected the competitive circumstances present in her subjects' social groups in the presence of introduced manipulanda. Thus, age differences apparent in this study between adults and juveniles are not due to the differences in the sexual composition of the two age groups. Neither have sex differences in success at tool-using tasks been found (Fragaszy & Visalberghi, 1989). Two characteristics of manipulation seem quite different between wild and captive capuchins. The first is the relative frequency of actions with two portable objects. Relational actions of this type occurred at a rate of 3 times per hr per juvenile (and less frequently in adults or infants) in the captive monkeys. Such actions were observed only a few times in free-ranging monkeys over several hundred hr of observation (Fragaszy, 1981). The second characteristic of manipulation that differs for captive and free-ranging capuchins is the frequency with which insertions of objects into crevices occur. Our captive monkeys (especially juveniles) routinely probe into holes in the wall, the wire mesh, introduced objects, and any appropriate opening with sticks, straw, pieces of food, or any other object of an appropriate size, as well as their hands. Insertion of an object into a crevice has not been reported for wild capuchins, although reaching into tree boles and mud banks has (Izawa, 1979; Boinski, personal communication, July 18, 1988). Although most of these acts are not identified as tool use because there is no specific outcome, insertion of an object into a surface can lead to the discovery of tool use under the right circumstances. Insertion is a prominent feature in several of the tool-using tasks presented to our groups (Fragaszy & Visalberghi, 1989; Westergaard & Fragaszy, 1987). These findings suggest that some aspect of the captive environment supports greater expression of manipulative potential than has been observed in natural environments. Observers in the field have often detected tool-using behaviors and other unusual manipulative activities in other species (see Beck, 1980, for a review), so we cannot blame the absence of such observations on the rigors of field conditions. The nearabsence of tool-using behaviors in capuchins in the field, in

comparison to the diversity and facility of spontaneous toolusing in captive capuchins (reviewed in Visalberghi, 1990), also suggests innovative behaviors are more frequent in captivity (see also Kummer & Goodall, 1985). Why might this be? We have no basis for proposing fundamental differences in cognitive operations between captive and wild monkeys. Social influences that increase the frequency of certain behaviors may play a stronger facilitating role in captivity, given the enforced proximity among group members (Box & Fragaszy, 1986), although direct imitation seems unlikely (Fragaszy & Visalberghi, 1989; Visalberghi & Fragaszy, 1990a). Physical features of the environment that affect generativity, such as the relative proximity between objects and substrates, familiarity of the objects and substrate, and an increase in leisure time, are likely to be more important for the contrast between captive and wild groups of capuchins. In short, the interaction of generativity with setting appears more likely to be responsible for the difference in tool-using behaviors in these populations than do differences in cognitive operations. We have described features of manipulative generativity in capuchins and argued that these will be useful in predicting the presence or absence of tool-using across species and age groups. Obviously, further work is needed to evaluate our hypothesis that generativity in manipulation is sufficient for the discovery of tool use, independent of representational capacities. The hypothesis leads to other directions of inquiry as well, such as elucidating the organizational properties of behavior that lead to generativity. To be sure, it is desirable to compare the ontogenies of manipulation and tool use in humans with those of other species. Unfortunately, observations of tool-using behaviors in human infants and toddlers have been restricted to interactions with a small set of objects in specific tasks (e.g., Case, 1985; Connolly & Dalgleish, 1989) or are accounts of the appearance of specific skills in natural settings (Rogoff, 1990). To our knowledge, the relevant data to test these predictions on manipulation and tool use do not exist for humans.

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Received May 15, 1990 Revision received January 28, 1991 Accepted January 31, 1991 •