Developmental Changes in Manipulation in Tufted ...

Copyright 1997 by the American Psychological Association, Inc. 0735-7036V97/I3.00

Journal of Comparative Psychology 1997, Vol. 111. No. 2, 201-211

Developmental Changes in Manipulation in Tufted Capuchins (Cebus apella) From Birth Through 2 Years and Their Relation to Foraging and Weaning Leah E. Adams-Curtis Washington State University

Dorothy M. Fragaszy University of Georgia

This study examined the contributions of physical and sensorimotor development to manipulation in capuchins (Cebus apella) from birth to 2 years. Between months 1-6 and 7-12, manipulation increased significantly in frequency, in the proportion that was vigorous or required fine motor control, and in the proportion directed at portable objects. Rne motor control, moving objects in relation to the body, and stamina are largely in place by 12 months, after which little changed. All elements of the manipulative repertoire have appeared, and vigorous and dexterous activities have peaked before fully independent foraging. Emergence of permanent dentition and achievement of approximately half of adult body size accompany the attainment of fully independent foraging at 15 months. Thereafter, increasing strength and specific knowledge probably contribute more to changing foraging competence in young capuchins than do stamina and sensorimotor development.

This report analyzes developmental changes in spontaneous manipulation over the course of the first 2 years of life in captive tufted capuchins (Cebus apella). We also consider the relation of manipulation to the appearance of species-typical foraging behaviors and the emergence of independent foraging. Capuchins are prototypical of nonhuman primates that engage in extractive foraging (removing foods from enclosing matrices, whether wood, soil, rind, husk, shell, or other dense covering; Parker & Gibson, 1977). Their extractive techniques typically involve strenuous manual and oral activity. They pull and bite open tough plant materials; break apart husked fruits, nuts, snails, and bivalves by banging them against a hard surface; dig through soil or plant debris; and reach into deep holes (Brown & Zunino, 1990; Fragaszy, 1986; Janson & Boinski, 1992). Extractive foraging also involves finely controlled movements, fine eye-hand coordination, haptic per-

ception, and multilimb and multidigit coordination. Such actions impose considerable motoric and perceptual demands (Gibson, 1986). In the wild, extractive actions during foraging are uncommon through the first year to 18 months of life but very evident in older animals (Fragaszy & Boinski, 1995). Juveniles perform similar actions as adults on substrates and eat the same foods. However, young capuchins are less efficient foragers than adult capuchins for several years after weaning (Fragaszy & Boinski, 1995; Janson & van Schaik, 1993). Capuchins grow more slowly after weaning than before (Fragaszy & Bard, in press) and appear vulnerable to starvation during periods of food scarcity that adult capuchins can weather without permanent ill effects (Janson & van Schaik, 1993). Together, these findings suggest that development of efficiency at extractive foraging is a demanding problem for the young capuchin. The reliance on extractive foraging is likely to increase the magnitude of the problem for capuchins, compared with species that forage in other ways (such as squirrel monkeys; Boinski & Fragaszy, 1989). Allometrically larger brain size has been singled out as a correlate of reliance on extractive foraging in certain primate groups, including capuchins (Gibson, 1986). Capuchins are noted to have relatively large brains for their body size. Their brains are relatively immature (by weight) at birth (Harvey & Clutton-Brock, 1985). They also have long interbirth intervals in relation to their size, as a function of the lengthy period of lactation and associated amenorrhea (radier than a long gestation; Fedigan & Rose, 1995; Ross, 1991). Weaning in tufted capuchins (calculated as interbirth interval minus 160 days, the duration of gestation) is estimated as 416 days (fifteen 28-day months) in captivity (Fragaszy & Adams-Curtis, 1994) and 16.5 months in a

Dorothy M. Fragaszy, Department of Psychology, University of Georgia; Leah E. Adams-Curtis, Department of Psychology, Washington State University (now at Department of Behavioral Sciences, Millikin University). This work was supported by grants from the National Science Foundation (BNS 85-03603) and the National Institute of Mental Health (R01-41543) and by a Research Scientist Development Award from the National Institute of Mental Health. Additional support was provided by a Dissertation Support Award from the Graduate School of Washington State University. Preparation of the manuscript was supported by a grant from the National Institute of Child Health and Human Development (2P01-HD6016). We thank Irwin Bernstein for commenting on an earlier draft of the manuscript. Correspondence concerning this article should be addressed to Dorothy M. Fragaszy, Department of Psychology, University of Georgia, Athens, Georgia 30602. Electronic mail may be sent via Internet to [email protected].

201

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FRAGASZY AND ADAMS-CURTIS

natural population (Janson & van Schaik, 1993). In short, having an immature brain at birth and a large brain in adulthood is associated in capuchins with an extended duration of suckling and a vigorous and extractive foraging style after weaning. The link among brain size, duration of nursing, and extractive foraging suggests that neural development, sensorimotor development, and cognitive reorganization may pace the development of foraging competence and the termination of nursing. Development of sensorimotor abilities that are necessary for competent extractive foraging, such as bimanual coordination and fine motor control of the digits, reflects in part maturation of the brain. For example, Lemon (1996) showed that corticospinal projections are not yet adultlike at 11 months of age in rhesus monkeys (Macaco mulatto), although species-normal functional dexterity has been achieved months earlier. Synaptic connections of this type contribute directly to manual dexterity. Capuchins exhibit as dense a field of direct corticospinal synapses to the hands as do rhesus monkeys (Bortoff & Strick, 1993). The developmental timetable for these synapses is unknown, but extrapolating from rhesus monkeys, the process would continue well past the first year of life. It may also take time to master the procedural knowledge used in foraging (i.e., selection of appropriate actions or refinement of motor skill) and the declarative knowledge (i.e., knowing where and when to forage; Altmann & Samuels, 1992; King, 1994). Some have even posited that cognitive development involving the reorganization of motor activity is important to foraging and that extractive foraging requires further (and therefore later) organization than less manipulative foraging styles (Gibson, 1983; Parker & Gibson, 1977). Of course, muscular, skeletal, and dental growth and development co-occur with individual experience and brain development. These also contribute to foraging competence. An alternative view of the relation between the development of foraging and the duration of nursing is that the latter reflects the length of time needed to grow a sufficiently large and strong body to forage competently. It is difficult to disentangle the contributions of neural maturation, sensorimotor development, cognitive development, and physical growth to increasing foraging efficiency in natural settings. Indeed, probably all these factors contribute to foraging competence. Moreover, they affect one another reciprocally and dynamically. Examining behavioral and physical development of captive populations is one way to parse out the contributions of particular factors. Captive populations afford a chance to examine behavioral development under conditions of optimal nutrition and food abundance for both mother and infant (i.e., where foraging efficiency does not constrain infant growth or maternal condition). Under these conditions, we can expect (a) physical growth and fecundity to achieve species-typical maximums and (b) age at achievement of self-sufficiency in foraging to achieve species-typical minimums. Adams-Curtis and Fragaszy (1994) described the development of manipulation in captive capuchins over the first 6 months of life. Infants attempt to reach, touch, and lick or sniff objects and surfaces near them as they cling to the

mother or other carrier during the first 8 weeks of life. Manipulative activity increases rapidly after 8 weeks as infants attain postural control and (he strength to reach out from the mother or other carrier and begin to locomote independently. By the end of the first 6 months of life, infant capuchins display all major elements of the adult manipulative repertoire, including precision grips (Costello & Fragaszy, 1989) and bimanual activity. At this age they begin to eat solid foods and are spending more than half of the daytime hours off a carrier. However, they will nurse for nearly a year longer. In this article, we analyze how manipulation changes after the first 6 months in these monkeys. We focus particularly on variables in which changes with age should reflect stamina and strength on the one hand and neural maturation, sensorimotor development, or cognitive change on the other. Stamina and strength should most affect the frequency of manipulation and the portion of it involving strenuous activities. Neural, sensorimotor, or cognitive development should most affect the patterns of activity and the frequency of actions involving dexterity or combination of objects. These are not mutually exclusive hypotheses. The strength of support for each one, and identifying at what ages each type of development appears relevant, can provide further direction for thinking about their specific contributions to the attainment of competence in foraging.

Method

Design Eight capuchins were observed in the home cage under normal environmental conditions over the first 25 months of life. A focal animal method was used (Altmann, 1974). The form of manipulation and the objects contacted during manipulation were recorded using an interval sampling scheme. This study follows previous studies by Fragaszy and Adams-Curtis (1991) and Adams-Curtis and Fragaszy (1994). We focus here on behavioral changes across four significant phases of foraging competence, which we signify by 6-month blocks. The first 6 months constitute early infancy: The infant has limited independent mobility and limited ability to feed itself. During the second 6 months, the infant is mobile but still substantially dependent on the mother for nutrition. In the third 6 months, the infant assumes increasing responsibility for feeding itself. In the fourth 6 months, the infant is fully independent nutritionally. This study has two features that serve to minimize potential confounds inherent in longitudinal research. First, subjects in this study were born at different times and were drawn from two different social groups, thus reducing cohort effects. Second, a number of observers, trained by both the original observers and later observers, collected the data. This procedure served to minimize changes in scoring as a function of who trained and established reliability with new observers.

Subjects and Housing The subjects (4 male, 4 female) were members of two groups of captive capuchins (Cebus apella). Each group consisted of 1 adult male, 3 to 5 adult females, and their offspring. Except for 2 males, all subjects for this study were born into the groups. The latter 2

DEVELOPMENT OF MANIPULATION IN CAPUCHINS

203

lary for acts and for surfaces and objects contacted is listed in Table 1. The vocabulary was chosen to reflect behaviors seen in foraging (Fragaszy, 1990) and to include the simple manipulations first seen in infants. Directed look, an act which does not involve direct manual contact with an object or surface, was included in the vocabulary to encompass exploratory activity of infants and also to make these data comparable with data on foraging activities obtained in field studies. At the end of each minute of observation (six 10-s cycles), the identities and behaviors of all animals within 1 m of the focal animals were recorded, using the same procedure (5-s watch, 5-s record) for each neighbor. The behavior of the neighbors is not analyzed here. Each subject was observed first within an observation session until all subjects in that group had been first; order of observation of subjects within session was randomized after the first subject. Observations were made between 9:00 a.m. and 7:00 p.m. Most of the observations occurred between 1:00 and 5:00 p.m. The number of observations per subject varied as a function of the availability of reliable observers. Each subject was observed during a 10-min observation period at least two times per month for 5 of the first 6 months (Block 1). For Blocks 2 (Months 7-12), 3 (Months 13-18), and 4 (Months 19-24), the subject was observed at least twice per month for 4 of

male subjects entered the groups with their mothers before the age of 6 months. Each group was housed in a two-room pen (over 153 cubic meters of space). Each room contained perches, hanging barriers, and various locomotor surfaces, including a tire swing, plastic hangers and a climbing rope, and straw bedding. The monkeys were fed Purina Monkey Chow each morning in sufficient quantities so that biscuits were available throughout the day. Water was available ad libitum. The diet of monkey chow was supplemented by fresh fruit, frozen vegetables, and yogurt. Small items of food, such as peanuts and sunflowers, were intermittently strewn on the floor to provide foraging opportunities. Other small objects (e.g., small plastic cups) were also provided intermittently.

Procedure Data were collected by paper-and-pencil format or by computer keyboard. During an observational session, each subject was observed for sixty 10-s sampling periods. During each 10-s period, the subject was observed for 5 s, then during the next 5 s, each combination of act and object or surface was recorded. This method produced 360 samples per hour per subject. The vocabu-

Table 1 Vocabulary Used for Acts and Targets Definition

Category Acts Directed look Bang/hit/slap Bite/masticate Push/pull, tear/break

Directed reach Insert/extract Lick/sniff/mouth Scratch/pick/tap Handle Sift Hold/carry Rub/roll/smear Drink/soak Unknown

Look at an object or another animal for 3 s or more from S i m away. Scored only when there was no contact. Vigorous hit of any target with the hand(s), whether or not they 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 to tear or break an object. The 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 a target but make only passing contact or no contact. Insert an object or the arm, hand, or finger(s) into or through a substrate. Common insert/extract actions involved placing straw into holes in the enclosure and reaching through the cage mesh. Investigation of a target by sniffing, placing in the mouth, or licking. Distinguished from bite/masticate by the vigor of the act and by the lack of use of the teeth. Investigation of the target using the fingers. Gentle tactile or fingertip exploration. Bimanually manipulate an object by turning the object or changing the object's orientation in some way. Search through the straw bedding with sweeping motions, lifting and moving the bedding, or by moving the hands through the straw. Hold an object while stationary or locomoting, including carrying objects in the mouth. The distinguishing feature is lack of manipulation. Rub an item or the hand along a surface in continuous contact. Distinguished from push/pull by the hand being placed flat on the surface. Drink water or wet objects by placing them beneath running water. Act that cannot be identified. Targets

Enclosure Browse Toys Feces Self Unknown Social

All parts of the home cage, includes walls, perches, floor, light covers, visual barriers and their tethers. All straw and tree branches. All tethered locomotor surfaces (plastic hangers, tires, etc.), all introduced objects, and tethered items for manipulation. Toys include the tethers for the toys. Self-explanatory. Any part of the subject's body. Scored only when there are two targets (e.g., lick chow from self, rub hand on wall). Self-maintenance behaviors such as grooming were not scored. Scored when the target could not be identified by the observer. Target is another animal. Scored only for directed reach and directed look, and for acts with two targets in which one target is another animal.

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FRAGASZY AND ADAMS-CURTIS

Table 2 Number of Observations per Subject for Each 6-Month Block Subject Block

Br

Fe

Lo

Vi

Wi

Xa

Yv

Zo

21 20 . 24 31 (5) (5) (5) (5) 32 2 33 25 35 38 (4) (6) (6) (6) (6) 3 12 15 23 18 25 (4) (4) (4) (5) (4) 4 14 13 30 25 12 25 (5) (6) (4) (4) (5) (5) Note. Numbers in parentheses indicate number of months represented by two or more observations. Subjects' names were as follows: Br = Bruce; Fe = Felicia; Lo = Louisa; Vi = Viola; Wi = Willy; Xa = Xavier; Yv = Yves; Zo = Zola.

1

29 (6) 17 (5)

30 (5) 13 (4) 12 (4)

the 6 months. This rule produced a minimum per subject of 10 observations distributed over the first 6-month block, and 8 observations over each of the second through the fourth block. Every subject had 12 or more observations in each block. The number of observations per subject is shown in Table 2.

Reliability We restricted calculation of reliability to active lines. A line was considered active if either of the two observers scored any activity. This procedure prevented biasing of reliability estimates by agreement on inactivity. To determine interobserver reliability, we calculated two percentages: the percentage of active lines in which at least one act agreed and the percentage of active lines with perfect agreement. Observers were considered reliable when the value for the former was greater than 90% and the value for the latter was greater than 80%. The reliability of new observers was assessed with both the original observers and secondary observers. Reliability data were collected from subjects of all ages used in this analysis.

Analysis

showed overlap of the sexes for all behaviors. Thus, male and female subjects were analyzed together. Age-related changes in the rate of manipulating particular kinds of objects were analyzed in the same manner. In addition, six categories of relational actions were defined by the relation between the object and the substrate or between the object and other objects (see Table 3). A final analysis involved the post hoc grouping of act and object combinations into five broadly defined functional classes (see Table 4). Because the largest amount of change occurred between Blocks 1 and 2 (i.e., during the first year), we also analyzed changes over smaller units of time (2-month periods) for Months 5-6, 7-8, 9-10, and 11-12 to produce a finer grained picture. The format of analyses was identical to that used for blocks. Each subject contributing to these analyses had two observations per month for each month in a 2-month period. A larger number of subjects contributed to these analyses (n = 10 to 11). Detailed analyses of Months 1-6 are presented elsewhere (Adams-Curtis & Fragaszy, 1994).

Results

Changes Evident From Block 1 to Block 2 (Months 1-6 to Months

7-12)

The overall rates of activity for each 6-month block ranged from 140 to 280 samples per hour (out of 360 possible; see Figure 1). The rate of activity increased significantly from the first block to the second block (Af first block = 1 3 2 acts per hour, M second block = 239 acts per hour), F(l, 5) = 15.10, p < .05. Rates of 7 out of 14 acts increased significantly from the first block to the second block (see Figure 2). One action, directed reach, showed a significant decline. As a consequence of differential changes in frequency, two acts that comprised a large proportion of activity in the first block (directed look and directed reach) were significantly smaller proportions of activity in the second block.

Table 3 Combinations of Objects and Surfaces

The data were treated in 6-month blocks. Dependent variables of rare and proportion were derived from the raw frequency data for each variable. To arrive at a rate score, we determined the total number of actions for each animal for each age in months (28 days). This value was then divided by the number of 10-min samples of observation for each animal for that month and then multiplied by 6 to produce an "hourly" rate per variable. The mean of the months contributing to each block was then computed. Thus each subject contributed one value to each block per variable. A within-subjects repeated measures analysis of variance comparing adjacent blocks was done for each variable, with n (of subjects) = 6 for comparisons of Blocks 1 and 2 and Blocks 2 and 3, and n = 5 for Blocks 3 and 4. Age was the quasi-independent variable and rate per hour was the dependent variable in one set of analyses; proportion was the dependent variable in another set of analyses. Results of these two analyses were compared informally to determine if changes in the proportional contribution of a particular activity reflected primarily changes in the rate per hour for that activity or a shift in the rate of other activities. Preliminary analysis

Combination

Definition

Object to enclosure

Place an object in relation to the enclosure. Example: Bang chow on the wall. Manipulate an object in relation to the body. Examples: Lick food from self, pick straw from self. Place an object in relation to a toy. Example: Insert a straw through a hanger. Place an object in relation to another. Example: Hit food against food. Place the hand or arm in relation to the enclosure. Example: Insert finger into a hole in the wall. Place the body in relation to an object. Example: Rub hand on food.

Object to body

Object to toy

Object to object Self to enclosure

Self to object

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DEVELOPMENT OF MANIPULATION IN CAPUCHINS Table 4 Functional Classes of Activity Definition

Class

Lick/sniff/mouth and scratch/pick/tap directed toward the enclosure or toys. Scored only if there was one surface or item contacted. Any act in which food was the first item contacted. Includes acts involving two items such as bang chow on the wall. Any act in which browse was the first item contacted. Includes acts involving two items such as rub straw on the wall. Any act in which another animal was the first object contacted. Consists primarily of directed look and directed reach. Any activity not classified as any of the classes described above. Includes all vigorous activity and all acts involving two objects or surfaces, unless directed toward food or browse.

Exploratory Food directed Browse directed Social Other

Lick/sniffVmouth remained about 20% of all activity; scratch/pick/tap declined about 5 percentage points, from 23 to 18 (ns). All those acts classed as vigorous or dexterous (slap/hit/bang, push/pull/tear, insert/extract, rub/roll/smear, and handle) increased in both rate and proportional representation (see Figures 2 and 3). Proportionally, the enclosure was contacted most frequently in both blocks. However, the distribution of actions to various targets (surfaces and objects contacted) changed significantly from Block 1 to Block 2, F(l, 5) = 19.63, p < .007 (see Table 5). Browse and food were both manipulated for a significantly greater proportion of actions in Block 2 than in Block 1, and the enclosure was manipulated a significantly lesser proportion. The distribution of activity across the five functional classes of acts varied significantly across Blocks 1 and 2. Infants devoted proportionally significantly less time to social activity (manual contact with other animals) and more time to investigating food and browse in the second block than in the first block. Although activity in which one object is combined with another or with a substrate is always a minority of all capuchins' actions, such actions are still relatively common (see Figure 4). The frequency of these actions increased significantly between Block 1 and Block 2, nearly doubling

from 13/hr to 24/hr, and the proportion increased from 5% to 15% (see Table 5).

Changes Evident Within Block 2 Significant changes over 2-month periods after 6 months are limited to two actions: lick/sniff/mouth and slap/hit/ bang. The proportional contribution of lick/sniff/mouth declined significantly from Months 5-6 to Months 7-8, F(l, 9) = 7.48, p < .03, and declined again from Months 7-8 to 9-10, F(l, 10) = 5.41, p < .05. The later decline in proportional contribution for lick/sniff/mouth was accompanied by a corresponding decline in rate per hour (from 51/hr to 34/hr). From Months 9-10 to 10-12, the proportional contribution of lick/sniff/mouth remained between 10% and 15%, and it occurred at a rate of 28 to 42 times/hr. The rate of slap/hit/bang increased significantly from Months 5-6 to 7-8 (from 7 to 15 times/hr), F(l, 9) = 11.09, p < .01. The corresponding proportional increase was not significant.

Changes Evident After 12 Months Overall rate of activity did not vary significantly across Blocks 2-3 or Blocks 3-4 (see Figure 1). The greatest rate

350 a

300

250'

200 150 100

a

T 1

1

I 1 J.

T 1

50

ft -

Figure I.

First

Second

Third

Six

Six

Six

Fourth Six

Months

Months

Months

Months

Number of acts per hour per 6-month age block. Bars show standard deviations.

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FRAGASZY AND ADAMS-CURTIS

90

Gentle Acts

80 70 60

ab

50 40 30 20

1st Six Months 12nd Six Months 13rd Six Months J 4th Six Months

I-JH 0

D.L.

S/P/T

L/S/M

D.R.

Dexterous Acts

B/H/S

B/C

P/P/T

I/E

H

R/R/S

Figure 2. Rate per hour of gentle acts (top) and dexterous acts (bottom) per 6-month age block. Bars show standard deviations. Small letters above the bars indicate significant changes across blocks (a = Block 1 to Block 2; b = Block 2 to Block 3; c = Block 3 to Block 4). For gentle acts, D.L. = directed look; D.R. = directed reach; L/S/M = lick/sniff/mouth; and S/P/T = scratch/pick/ tap. For dexterous acts, B/H/S = bang/hit/slap; B/C = bite/chew; P/P/T = push/pull/tear; I/E = insert/extract; H = handle; and R/R/S = rub/roll/smear.

in any block for any subject was 354 acts/hr. Proportionally, the distribution of activity across functional classes shifted between Blocks 2 and 3, F(l, 4) = 7.23, p < .05. The only class to show a statistically significant change was explore, which declined, F(l, 4} = 16.08, p < .02 (see Figure 3). The enclosure was targeted proportionally less frequently, F(l, 4) = 5.96, p < .071, and lick became absolutely less frequent. These findings reveal a coordinated shift in activity away from gentle exploration of a fixed surface between 6-12 months and 13-18 months. Statistically significant changes in the frequency or proportion of activities between Blocks 3 and 4 were limited to declines in the rate and proportion of bite/chew (from 70/hr to 50/hr), Fs(l, 4) > 9.00, ps < .05, and the rate of scratch/pick/tap, which declined from 35/hr to 26/hr, F(l, 4) = 8.27, p < .05. The overall rate of activity did not change, nor did the frequency or distribution of combinatorial actions or functional classes.

Discussion Age-Related Changes in Manipulation and Their Relation to Foraging Competence The present study has documented that spontaneous manipulation in capuchins changes rapidly during the first year of life but that changes thereafter are relatively minor. Although all adult forms of manipulation (e.g., uses of digits) are seen in the first 6 months (Adams-Curtis & Fragaszy, 1994), changes between the first and second half of the first year affected virtually all other aspects of manipulation. The proportion of activity that was vigorous and dexterous increased, portable objects were manipulated proportionately more often, and combinatorial actions were produced more frequently. Infants proportionally decreased manipulation of others* bodies and increased manipulation of browse and food. The changes occurred gradually in the

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DEVELOPMENT OF MANIPULATION IN CAPUCHINS

Gentle Acts

1st Six Months 2nd Six Months 3rd Six Months 4th Six Months

Dexterous Acts

B/H/S

B/C

P/P/T

I/E

H

R/R/S

Figure 3. Proportion of manipulative activity represented by gentle and dexterous acts per 6-month age block. Bars show standard deviations. Small letters above the bars indicate significant changes across blocks (a = Block 1 to Block 2; b = Block 2 to Block 3; c = Block 3 to Block 4). For gentle acts, L/S/M = lick/sniff/mouth; S/P/T = scratch/pick/tap; D.L. = directed look; and D.R. = directed reach. For dexterous acts, B/H/S = bang/hit/slap; B/C = bite/chew; P/P/T = push/pull/tear; I/E - insert/extract; H = handle; and R/R/S = rub/roll/smear.

second 6 months. Taken together, these changes produce a pattern of manipulation that supports foraging in a speciestypical fashion. The frequency of manipulation also increased dramatically. Below we consider the implications of these findings for the development of competent foraging. Changes in manipulation between 7-12 and 13-18 months of age concerned the redistribution of activity away from gentle exploratory activity (e.g., by licking) and away from inspection of fixed cage surfaces (walls, perches, etc.). These changes probably have implications for the selection of materials to manipulate and probably reflect in part changes in postural stability and physical stamina. Yearlings can move all around the cage more securely compared with younger infants and can more readily pick up objects. Consequently, they are better able to select varied and portable objects to manipulate. No changes were observed between these age groups that would affect foraging in other ways. Change after 18 months was restricted to a decline in the frequency of bite/chew, which probably reflects teething

activity in Months 13-18. Six permanent teeth on each side erupt in this age block (mandibular and maxillary Ml, II, and 12; Galliari, 1985). Like the changes occurring between 6-12 and 13-18 months, these changes do not have strong implications for the manner of foraging by the young animal, although the arrival of permanent teeth is probably important for success in processing hard foods. Overall, the most striking feature of manipulation in young capuchins older than 6 months is its sheer frequency. Frequency of manipulation rose rapidly through 12 months and remained stable thereafter among juveniles; it was much higher among juveniles 13 to 39 months than among adults in me same groups (cf. Fragaszy & Adams-Curtis, 1991). That high rates of manipulation are present among juveniles in the absence of any contingency between such manipulation and obtaining food indicates that this activity is inherently attractive to young monkeys. The high frequency of unrewarded spontaneous manipulation in young monkeys translates into persistent foraging activity in natural settings, even when foraging efficiency is low. Wild

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Table 5 Proportion of Activity Directed to Different Objects and Surfaces in Each 6-Month Block, Expressed as a Percentage Block Activity Acts with a single target Enclosure Browse Toy Food Feces Self Unknown Social Sum Acts combining one object (Obj) with another object or surface Obj/enclosure Obj/self Obj/toy Obj/obj Self/substrate Self/obj Social combination Sum Grand total

48.6

7.4 6.8 5.4 0.0 1.3 2.9 22.5 94.9

2.1 0.3 0.1 0.0 2.5 0.0 0.1 5.1 100

25.0 18.5

85.2

28.4b 12.4 12.0 23.6 0.3 0.0 5.6 1.7 84.0

7.4 1.7 0.1 0.1 5.2 0.1 0.2

7.2 2.4 0.2 0.1 6.0 0.0 0.0

11.0

35.2" 14.2° 12.4 15.7"

0.2 0.1 a

5.2

2.2

14.8

100

"Significant change between Blocks 1-2. between Blocks 2 and 3.

15.9

100

9.7 18.2

0.2 0.2 5.1 1.3 77.8

4.6 0.3 0.2 5.6 0.1 0.1 22.2

100

Significant change

juvenile capuchins spend much more time foraging than do adult capuchins (Fragaszy & Boinski, 1995). The extent to which this is because they are inefficient foragers and therefore need to spend more time foraging or because they prefer manipulation over other activity cannot be determined from field observations. Our data suggest that sometimes they may be engaging in these activities for reasons other than solely to find food. Taken together, these findings indicate that the manipulative patterns relevant to species-typical foraging have appeared by 13 months of age in young capuchins. Speciesnormal sensorimotor development must be largely achieved, even if not mature, by 1 year, as subsequent changes in manipulative activity are minor indeed. Moreover, young capuchins persist in manipulative activity that is identified in natural settings as foraging, even when the immediate activity bears no immediate consequences for feeding (as was generally the case in captivity). Sex differences in these patterns are not evident. Thus, capuchins of both sexes are equipped well before the appearance of permanent teeth to benefit from practice of foraging elements in nonfunctional situations. How does this timetable relate to the attainment of independent foraging? Foraging Activity by Infant and Juvenile

Capuchins

in a Natural Setting Foraging activity in infant wedge-capped capuchins (Cebus olivaceus) ranging from approximately 6 months to 18

months of age, and juveniles in the same group from 2 years to 4 or 5 years, has been described by Fragaszy and Boinski (1995). Infant capuchins foraged in ways that were largely similar to those seen in adults and juveniles, picking fruits and taking surface invertebrates, and banging and biting branches and twigs, although they devoted less time to this activity than did adult or juvenile capuchins. They engaged in some activities at which they were patently ineffective (such as banging snails against tree trunks) but that are prominent features of foraging in older animals. Unlike juvenile capuchins, they engaged in strenuous foraging less often than did adult capuchins. There were no differences between infant capuchins and other capuchins in the rate of producing unusual action-object combination, although infant capuchins were more diverse than older capuchins in foraging on parts of certain plants. For example, only infant capuchins were observed to bite limbs of fig trees. However, infant capuchins' foraging efficiency was extremely low, and often their foraging activities looked playful rather than purposeful. Much more of their foraging activity involved mastication without evidence of ingestion, which may have been prompted by teething. Juvenile capuchins presented a different picture from infant capuchins, spending more time foraging than adult capuchins and engaging in strenuous foraging activity more than adult capuchins. Their foraging rarely involved mastication without ingestion, and although they were inefficient at some activities (such as smashing open snail shells), they were at least partially competent at all adult foraging tasks. On the whole, then, the pattern of foraging in infant and juvenile capuchins follows the pattern of manipulation observed in the captive study. One difference is that in the captive setting, adult capuchins reduce time devoted to manipulation, so that juvenile capuchins appear more different from them than in the wild population. Although observation conditions in the field did not permit identification of specific manual actions, it seemed that infant capuchins were not handicapped by sensorimotor abilities in their foraging efforts, but rather by postural instability and relative weakness. They were also quite timid, a characteristic that seems adaptive in relation to avoidance of predation but that can inhibit foraging at certain rich sites. Juvenile capuchins were less timid and also larger and posturally stronger.

Physical Growth and Its Relation to Foraging Competence The aspects of physical growth with the most immediate relevance to improving foraging competence for young capuchins are probably jaw musculature and skeletal anatomy, as these affect bite strength. Bite strength is a function of both the biomechanical properties of the jaw and the muscular apparatus (Cole, 1992). The appearance of permanent teeth, particularly molars, and muscular development are probably important additions to the young monkey's ability to produce a bite force large enough to crack open hard foods, a behavior that is an important feature of for-

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] 1st Six Months 2nd Six Months 3rd Six Months 4th Six Months JIBT nrn 0-E

O-S

O-T

-r

0-0

S-S

T

S-O

Figure 4. Rate per hour of actions combining contact with an object and a substrate, or an object and another object. Bars show standard deviations. O-E = object-enclosure; O-S = object-self; O-T = object-toy; O-O = object-object; S-S = self-substrate; and S-O = self-object.

aging in capuchins. In captive tufted capuchins, permanent dentition begins to emerge at 14-16 months with the first molar and first incisor (in close succession), the second incisor at 16-19 months, the second molar at 26-28 months, and the last two molars after 30 months (Galliari, 1985). This schedule may be delayed in natural populations, however. For example, Phillips-Conroy and Jolly (1988) reported that eruption of the permanent incisors and first molar in baboons (Papio hamadryas cynocephalits) occurred 6 to 13 months sooner in a captive population than in a wild population (16% to 24% earlier). If a delay of similar magnitude occurs in wild capuchins in relation to their captive counterparts, the first permanent teeth would not appear until 17 to 20 months. In natural populations, then, completion of weaning may occur just about the time the permanent two incisors and the permanent first molar appear. Incisors are used to tear, and molars, along with the premolars, are used to bite open hard foods (Izawa, 1979; Izawa & Mizuno, 1977; personal observation) that figure so largely in the foraging specializations of capuchins. Increasing skeletal and muscular growth also impart greater strength. Weight gain can serve as a general index of muscular growth. In captive tufted capuchins, females reach 50% of their mother's adult nonpregnant weight at 61 weeks (15.2 months) of age, on average (Fragaszy & AdamsCurtis, 1994). This timetable is probably advanced compared with wild populations, but we can only guess by how much—probably a few months at least. As muscle growth occurs more quickly than skeletal growth in the mandibles (Cole, 1992), young monkeys can gain bite force more quickly than their skeletal growth would suggest. Thus by late in the second year, the young capuchin has gained half its adult weight (and presumably an even larger proportion of its adult bite force), as well as one permanent molar and two permanent incisors. The changes may be sufficient to put the young monkey over the threshold for self-feeding.

Comparison With Saimiri The squirrel monkey (Saimiri) provides an instructive comparison for the developmental pattern described for capuchins. Saimiri is in the same family as Cebus (Cebidae) and shares with Cebus an omnivorous diet and a reliance on animal sources of protein. However, weaning is completed at an earlier age and the gradual nature of weaning seen in capuchins is absent in Costa Rican squirrel monkeys (Saimiri oerstedi; Boinski & Fragaszy, 1989). Weaning in 5. oerstedi occurs relatively rapidly by 5 months of age, just about as soon as infants exhibit the basic adult repertoire of manipulative and locomotor skills. This is also about the age that (captive) infant female squirrel monkeys (S. sciureus) reach 50% of their adult weight (between 21 and 26 weeks; Kaack, Walker, & Brizzee, 1979). In captive squirrel monkeys, permanent molars begin to erupt at about the age of weaning (19 weeks; Galliari & Colillas, 1985). Thus in terms of physical milestones in relation to adult size and dentition, they are at about the same point at 5 months as capuchins are about a year later. Behavioral abilities are less discrepant in timing; capuchins display the adult repertoire of actions by 6 months as well (Adams-Curtis & Fragaszy, 1994). However, squirrel monkeys are less reliant than capuchins upon extraction and biting hard objects to obtain food; visual detection of fruits and small invertebrates characterizes their predatory strategy (Janson & Boinski, 1992). Physical size and bite force are not especially relevant to this foraging strategy, as they are to the capuchins. An important point for this discussion is that ontogenetic timing of motor, perceptual, and physical development is rather close in squirrel monkeys. This is a major point of difference with capuchins, in which physical development is delayed, even under nutritionally ideal circumstances, but sensorimotor development, reflecting basic development of sensory and motor tracts, is on a timetable that is much more similar to the squirrel monkeys'. This is apparently an

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instance of heterochronic differentiation between capuchins and squirrel monkeys (McKinney & McNamara, 1991), wherein neuromotor or perceptual development is not linked so closely to physical development in one species as another. Later offset of physical growth, a primary process increasing body size in evolution, is associated with larger brains but not necessarily with a matched delay in the offset of growth of the brain. Instead, the trend toward a later offset in physical development carries with it a trend toward what McKinney and McNamara termed "organizational heterochrony" (1991, p. 309) in the development of the brain. Brain development involves more than volumetric growth; it involves myelination, selective cell death, and the formation of branching connections. These processes take considerable time even after brain mass has stopped increasing, and the larger the brain, the longer it seems to take. It is unknown whether capuchins exhibit a longer period of neural development in these terms than do squirrel monkeys, but we would predict so, on the basis of the duration of skeletal growth, dental eruption patterns, the size of the brain, and the pattern of attainment of independent foraging in each species. Certainly data bearing on myelination and patterns of connectivity would be a welcome addition to our understanding of growth and development in both these genera. Even so, to salvage the hypothesis that delayed onset of independent foraging reflects increasing behavioral complexity, in turn requiring a complexly organized brain, one must demonstrate that developmental changes in brain function are linked with changes in foraging. A finer resolution of measurement of foraging activity than we have used here will be needed for that purpose. In summary, we would argue from our findings on manipulation, the patterns of dental eruption and weight gain in captive monkeys, and foraging efficiency and interbirth intervals in wild monkeys that capuchins become fully self-sufficient at foraging at just about the time that size and dentition permit processing foods that require strength to obtain. Self-sufficiency in foraging occurs long after development of motor abilities used in foraging and seems not to depend on any noticeable change in these abilities as weaning proceeds. Other taxa that may show the same pattern include the aye-aye (Daubentonia madagascariensis). Ayeayes exhibit unique percussive and extractive foraging techniques that require both strong bite force of the incisors and fine motor coordination of the digits (Erickson, 1994). The details of physical and motor development in this species await description, but a preliminary report of development in one captive-born infant noted that the infant frequently displayed the species-typical digital actions used in adult foraging (tapping, scraping with one digit) at 7 to 8 months of age but was still suckling at a year (Feistner & Ashbourne, 1994). We would predict that eruption of permanent incisors would occur about the tune of completion of weaning, after 12 months, and that infants would achieve a fair proportion of their adult body weight before weaning (to support sufficient bite force). Brain development in ayeayes is completely unstudied but will be fascinating to learn about, as this genus also has an anomalously large brain (Bauchot, 1984; Gibson, 1986).

This view of the relation among motor development, physical development, and self-sufficiency in foraging does not preclude a significant role for experience in fashioning an individual's foraging behavior. To be sure, skill takes time to develop, and many aspects of foraging can benefit from skill (see King, 1994). It does, however, suggest that the parameters controlling achievement of independent foraging are related to physical development at least as much as to increasing motor skill or changing motor competence. Motorically, capuchins are ready to self-feed months before they do so. During the second year of life, strength seems to limit their foraging success more than stamina, cognition, perception, or motor skill.

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