Spatial Facilitation in a Probing Task in Wedge-Capped Capuchins (Cebus olivaceus)

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International Journal of Primatology [ijop] PP244-302154 August 31, 2001 5:8 Style file version Nov. 19th, 1999

International Journal of Primatology, Vol. 22, No. 6, December 2001( c© 2001)

Spatial Facilitation in a Probing Task inWedge-Capped Capuchins (Cebus olivaceus)

Michel Dubois,1 Jean-Francois Gerard,2,3 Elineuza Sampaio,1

Olavo de Faria Galvao,1 and Colette Guilhem2

Received December 10, 1999; revised February 29, 2000; accepted May 6, 2000

Activities ordinarily performed by an animal in a given place may influencethe way it behaves towards an object newly found there. We examined the useof probing tools in a group of 4 wedge-capped capuchins (Cebus olivaceus),in the home cage into which we simultaneously introduced two identical ap-paratuses, one at a site ordinarily used to manipulate objects, and the otherat a site mainly used for visual monitoring. We expected that spatial facilita-tion would occur, i.e., the subjects would be more efficient at the site wheremanipulative behaviors were more frequently performed. Two monkeys usedprobing tools to extract syrup from the openings of the apparatuses. Tool useefficiency was higher with the apparatus located at the site where they hadperformed more manipulative and combinative behaviors. These results areconsistent with the hypothesis of spatial facilitation and illustrate the fact thatspatial context can be an overwhelming variable that should not be neglectedin behavioral research dealing with instrumental tasks.

KEY WORDS: Cebus olivaceus; probing behavior; spatial facilitation; tool use.

INTRODUCTION

Capuchins (Cebus spp) complete omnivorous foraging activities by re-moving food from enclosing matrices (Parker and Gibson, 1977). Theirextractive foraging techniques involve not only vigorous actions but also,

1Departamento de Psicologia Experimental, Universidade Federal do Para, Para, Brazil.2Institut de Recherche sur les Grands Mammiferes, Castanet Tolosan Cedex, France.3To whom correspondence should be addressed; e-mail: [email protected].

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0164-0291/01/1200-0993$19.50/0 C© 2001 Plenum Publishing Corporation

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994 Dubois, Gerard, Sampaio, Galvao, and Guilhem

in many instances, finely-elaborated multidigit coordination (Costello andFragaszy, 1988). These finely-controlled sensorimotor skills allow capuchinsto be proficient tool users in a great variety of situations (Beck, 1980; Urbani,1999; Visalberghi, 1990; Westergaard et al., 1999). In particular, use probingtools (Fragaszy and Adams-Curtis, 1991), an activity well-documented inother primates (Beck, 1980; Westergaard, 1991; Westergaard and Fragaszy,1987; Westergaard and Suomi, 1994). However, only chimpanzees (Pantroglodytes) consistently use such tools in the wild, notably for termite orant-fishing and honey dipping (McGrew, 1992; McGrew and Marchant, 1992;Nishida and Hiraiwa, 1982; Van Lawick-Goodall, 1970).

Dubois et al. (2000) found that the way captive wedge-capped capuchins(Cebus olivaceus) behave towards a new object introduced to a given placewithin their cage greatly reflects the activities ordinarily performed in thisparticular place. This location-specific effect in individual’s responsivenessstyle predicts spatial facilitation, if an apparatus designed to improve tool useis introduced into an area where capuchins perform manipulative behaviors.Indeed, as noted by Fragaszy and Adams-Curtis (1991, p. 389), ”discoveryof tool use is probabilistic and therefore more sensitive to the frequency ofcombinatorial activity than to its onset.”

We designed an experiment to test the existence of spatial facilita-tion. We examined the use of probing tools in a group of wedge-cappedcapuchins confronted with two identical apparatuses, one at a site mainlyused for object manipulations, the other at a site used for other behav-iors. We expected the monkeys to be more efficient in syrup extraction atthe site where they ordinarily performed manipulative and combinatorialactivities.

METHODS

Subjects and Home Cage

The subjects were four unrelated wedge-capped capuchins: a wild-bornmale of 13 years (Neositu), and captive-born males of 8 years (Lagace),7 years (Curumim), and 4 years of age (Henein). They lived within the sameoutdoor cage, in the National Primatological Center of Ananindeua (Brazil).Located at the edge of a secondary neotropical forest, the cage was 14 m long,8 m wide, and 5.7 m high. Water was available ad libitum and food (monkeychow, vegetables, local fruits, and sometimes eggs) was provided on a dailybasis at 2:00 p.m. Results from tests conducted in order to evaluate thedominance hierarchy (Dubois et al., 2000) indicated the following ranking:Neositu > Lagace > Henein > Curumim.

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Spatial Facilitation in a Probing Task in Wedge-Capped Capuchins 995

Table I. Relative frequencies (in %) of the behavioral categories recorded in sites Aand B for each subject

Location A Location B(Manipulative behaviors) (Visual monitoring)

N L H C N L H C

Social 4.76 1.47 5.61 7.00 8.86 3.60 17.19 19.66Manipulative 67.35 58.82 38.32 67.00 2.53 1.44 7.03 12.82Rest 1.36 1.47 2.80 0.00 8.86 17.26 5.47 5.13Locomotion 12.93 20.59 25.23 18.00 5.70 11.51 7.03 18.80Feed 2.04 8.82 16.82 2.00 0.00 1.44 7.81 0.86Visual monitoring 10.88 6.62 10.28 4.00 70.25 63.31 53.91 40.17Other 0.68 2.21 0.94 2.00 3.80 1.44 1.56 2.56n 147 136 107 100 158 139 128 117

Notes: N – Neositu; L – Lagace; H – Henein; C – Curumim.

Choice of the Sites for the Apparatuses

In order to identify sites usually supporting contrasting behaviors withinthe home cage, we first drafted a detailed map of the cage and recordedactivities and locations of all subjects at 2-min intervals over a 6 mo period.We recorded behavior in 7 categories: social, manipulative, rest, locomotion,feeding, visual monitoring, and other.

The 3604 scans performed during this preliminary phase allowed us toidentify two squares of 1× 1 m, intensively used and supporting contrastingkinds of behaviors. One of the squares—site A—was mainly used to performmanipulative behaviors, while the other—site B—was characterized by vi-sual monitoring and, to a lesser extent, social behaviors (Table I). Nothingin the two sites, located at 12.6 m from each other, could account for theirdifferent use.

Apparatus

We built two identical apparatuses designed to accommodate the useof probing tools to obtain sweet syrup . Each apparatus (Fig. 1) was a closedwooden box with three square openings of 3× 3 cm on the top. The box waslarge enough to allow the simultaneous presence of several subjects on itsroof. Each opening corresponded to a container, whose bottom was filledwith syrup. In order to gain access to the syrup the subjects could use threesteel sticks (0.7 cm in diameter and 25 cm long) that were chained by oneend to the box. The other end was fitted with a 2.8× 2.8-cm bolt that themonkeys had to insert through an opening to the bottom of the container inorder to obtain the syrup. A colored tag on each stick allowed us to determine

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Fig. 1. Apparatus: a steel bolt had to be inserted into a container to reach the syrup, thenextracted.

whether the tool reached the bottom. The proper insertion of the steel boltsrequired the use of both hands.

Procedure and Data Recording

We simultaneously placed the two apparatuses in the home cage, onein site A, the other in site B, about 1 mo after completing site identifica-tion observations. Both locations allowed the subjects to interact with theapparatuses in the same way. We recorded data during twenty-four 60-minsessions each morning over a 2-mo period. At the onset of each session, wecleaned the containers, then filled them with 8 cc of sweet syrup from a sy-ringe. Between sessions, the apparatuses remained in the outdoor cage, withtheir tops covered with an aluminum sheet in order to protect them fromrain and to prevent functional tool use between experimental sessions bythe monkeys. The boxes were only removed from the enclosure 2 h a weekfor cleaning.

During each 60-min session, we filmed each site by a video camera lo-cated 2 m from the focal apparatus. A bout began when a monkey climbed

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up an apparatus, and ended when he moved away and did not come backwithin 10 s. All recorded bouts a included in the analysis. We scored a prob-ing attempt when a subject tried to insert a tool into an opening. We scoredan appropriate use of tools to probe into and to extract liquid from the ap-paratus when a steel bolt was correctly inserted to the colored mark andextracted. We distinguished two kinds of error. Type 1 errors were all at-tempts using the wrong-end of the steel bolts and type 2 errors encompassedall inefficient attempts where subjects used the right end of the steel bolts butfailed to insert the bolt far enough to obtain the syrup. We recorded actionsfor (a) inserting and thrusting the tool into the apparatus, (b) removing thetool from the apparatus, and (c) bringing the bolt to mouth. The non-solversoften found a tool standing in a container, and we recorded every episodeof licking syrup-coated bolts by the non-solvers. The vocabulary used todesignate the behaviors other than those involved in a probing attempt asdescribed above, e.g. insertion attempts using material other than the pro-vided tools, is in Table II. We scored acts by one-zero sampling of occurrencewithin a bout interval. In order to assess possible interference from socialfactors, we scored all occurrences and durations of apparatus-sharing andall cases of avoidance, where in a subject moved away from the apparatus asa direct result of the approach from, or aggression of peers. Interobserverreliabilities determined from 4 random sessions were about 95% for probingattempts, and 86% for all other acts.

Table II. Terms and definitions for acts

Category Definition

SocialWatching Look at another subject for 3 s or moreConflict Aggressive movements toward another subjectPositive social behavior Play, grooming and gentle directed reach where the

target is another animalManipulative

Poke Insert the right or the left hand, or finger(s) into an openingManipulate Manipulate a tool by turning or changing

the object’s orientationShake Vigorous activity consisting shaking the apparatusStrike Vigorous hit of the apparatus with the hand(s) or a

detached objectObject Insert into an opening another object than the

provided toolsRest At rest on the apparatus and self-directed behaviors

as self-groomingVisual monitoring Visual monitoring of the surroundings for ≥3 sOther Any activity not classified as any of the acts described

above and acts that cannot be identified

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Statistical Analysis

We compared, frequencies via the log-likelyhood G-test. We used onlynonparametric tests (Wilcoxon T-test, Mantel Z-test, Kendall rank correla-tion coefficient τ ) for statistical inferences based on quantitative variables.P values correspond to two-tailed probabilities. We calculated the durationthat each subject could be expected to spent in a given site, in the absense ofeffect of the introduced apparatus, based on the proportion of scans show-ing the subject in the site during the preliminary phase of observation. Forinstance, we calculated the duration expected in A for Neositu during each60-min observation session as 60 min× 147/3604= 2 min 27 s.

RESULTS

Overall Interest for the Apparatuses

The subjects use each of the two apparatuses intensively: on average8 min 31 s per subject and 60-min session at site A, 11 min 32 s per sub-ject and 60-min session at site B. Nevertheless, introduction of a box had amore consistent effect in B than in A (Fig. 2): while all the subjects spentmore time at site B than they spent there before the introduction of theapparatus (Wilcoxon T-test: P < 0.001 for each subject), only Neositu andCurumim significantly increased the time spent at site A (Neositu: T = 3,n = 24, P = 0.0001; Curumim: T = 1, n = 24, P = 0.0001; Lagace: T = 99,n = 24, P = 0.15; Henein: T = 131, n = 24, P = 0.59). Apparatuses weretotally neglected during some sessions by Lagace (n = 1 for A) and Henein(n = 5 for A; n = 2 for B).

Behaviors Performed at the Apparatuses

The introduction of the apparatuses had a strong effect on behavior,even when the acts directly related to syrup extraction by means of thetools are excluded from the analysis. At site B, in particular, manipulativebehaviors became the predominant activity, while visual monitoring behav-iors strongly decreased in frequency (Table III). Accordingly, the behavioralcontrast which had initially been recorded between sites A and B (Table I)almost vanished.

The subjects differed in their activity pattern, especially with referenceto manipulative behaviors. Henein and Lagace frequently poked their fingersinto the openings, while the two other subjects rarely did so (Henein: 27% out

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Fig. 2. Distribution of the time spent by the four subjects at sites A and B, over thetwenty-four 60-min sessions of observation. Each box plot shows median (inner hori-zontal line), first and third quartiles (upper and lower edges of the box), as well as 10thand 90th percentiles (ends of the whiskers) of the distribution. Black points correspondto the values expected in the lack of effect of the apparatus introduction.

of the 1,364 manipulative acts recorded; Lagace: 15%, n = 1, 820; Neositu:1%, n = 4, 813; Curumim: 1%, n = 7, 680; G3 = 1542.5, P = 0.0001; fre-quencies computed by excluding the acts involved in syrup extraction bymeans of the tools). Moreover, the manipulative behaviors performed byLagace included a higher proportion of vigorous acts, such as striking andshaking, than those performed by the other subjects (29% vs. <4% for theother subjects, G-test: P < 0.0001 in each case).

Table III. Relative frequencies (in %) of behaviors other than those involved in probingattempts, recorded in sites A and B for each of the subjects

Neositu Lagace Henein Curumim

A B A B A B A B

Social 8.4 13.7 3.3 7.2 17.8 13.5 5.8 6.0Manipulative 58.3 56.0 64.4 47.8 47.7 53.2 73.4 80.8Rest 0.1 2.2 0.0 3.2 0.0 1.0 0.1 0.0Visual monitoring 25.1 24.7 22.6 34.7 24.4 25.9 13.4 12.1Other 8.1 3.4 9.7 7.1 10.1 6.4 7.3 1.1n 2700 5750 713 2825 825 1813 2170 7531

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Task Component Dynamics

Only Curumim and Neositu, i.e., the lowest and the highest-ranked sub-jects, respectively, obtained syrup by inserting the steel bolts into openingsin the apparatus, removing them, and licking off syrup. Curumim dippedsuccessfully with a tool as soon as session 1, in 22 instances at site A, and 11instances at site B. Neositu’s first attempts occurred at site A during the firstsession when alone, and at site B during session 7 when he encountered asteel bolt that Curumim had left inserted in an opening. On the 10th sessionhe successfully probed at site A (in 10 instances) while sharing the apparatuswith Curumim. Alone, he successfully probed the apparatus (in 10 instances)at site B during the 13th session, but failed to extract syrup during the 14thsession.

After the first successful attempts, use of probing tools became a regularactivity for Curumim and Neositu. Neositu made consistently more attemptsat site A than at site B (T = 34, n = 19, P = 0.015). This was not the casefor Curumim (T = 117, n = 24, P > 0.30) because although he initially fa-vored site A, he changed to site B as soon as Neositu began to make severalattempts at site A (Fig. 3). Indeed, the number of attempts performed in Aby Curumim was negatively correlated with the number of attempts madethere by Neositu (τ = −0.440, n = 24, P = 0.0026).

The probing attempts by both Neositu and Curumim were more fre-quently successful at site A than at site B (Neositu: 40.7% vs. 26.4%, T = 1,n = 14, P = 0.001; Curumim: 50.2% vs. 27.4%, T = 11, n = 24, P = 0.0001).For Neositu, the occurrence frequency of type 1 error was 100% at both sitesduring his first attempts, but reached 0% at site A and 5.2% at site B dur-ing the final session. For Curumim, this frequency was 38.5% at site A and57.1% at site B during the first session, 1.4% at site A and 2.3% at site Bduring the final session. Type 2 error occurred frequently for both subjectsuntil the end of the observations, especially at site B (final session: 30% atsite A, and 61% at site B for Neositu; 18% at site A, and 84% at site B forCurumim).

Although Lagace and Henein never attempted to probe the appara-tuses, they showed interest in them, obtaining small amounts of syrup bylicking the apparatus, poking their fingers into the openings, and lickingsyrup-coated bolts obtained from the apparatus, or by taking the tools awayfrom the lower-ranked Curumim. They sometimes encountered steel boltspartly or fully inserted (Lagace: n = 25; Henein: n = 12). However, episodesthat involved bolt-handling were not followed by probing attempts. Further-more, they did not use tools or objects appropriately when attempting toobtain syrup; instead they usually shook the apparatus, and struck it withtools, their hands, or with other objects.

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Fig. 3. Number of probing attempts performed by the two solvers at apparatuses A (full line)and B (dashed line) during the entire study.

Simultaneous Presence at the Apparatuses

The time the individuals spent together at the same apparatus differedbetween pairs of subjects (Fig. 4). In general, the nearer two subjects werein the hierarchy, the less time they were together at the apparatuses (site A:Z= 6.34, P = 0.0833; site B: Z= 14.82, P = 0.0833; overall probability thatthe difference in social status had no effect on the time spent together:P = 0.0069). In practice, we never observed a subject climb onto an appa-ratus when a dominant capuchin of immediately higher-ranking status wasalready there. In contrast, a subordinate was rather frequently disturbed by adominant, either slightly higher or much higher in the hierarchy. In this way,Curumim had about 40% of his bouts interrupted (39.5%, n = 177, at siteA; 40.2%, n = 189, at site B), while Neositu, the highest-ranked individual,had none (n = 140 at site A; n = 188 at site B).

Difference in social status was not the only factor influencing the time ofapparatus sharing. With the exception of Curumim and Henein, which werenever observed together at either site, all pairs of subjects spent more time

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Fig. 4. Time spent together at sites A and B by the different pairs of indi-viduals, during the overall experiment. The subjects are ordered accordingto their hierarchical rank.

together at site B than site A (Fig. 4; T = 0; n = 5; P = 0.0625). The enhancedsocial tolerance at site B is further supported by the fact that Curumim andNeositu simultaneously performed probing activities 6 times at site B, whilethey did so on only once at site A. Due to apparatus sharing at Site B, Lagaceand Henein actually spent non-negligible amounts of time with either of thesubjects that probed the boxes. Lagace spent a total of 29 min with Curumim,and Henein a total of 59 min with Neositu, as compared to the 66 minNeositu spent with Curumim before performing his first successful probingattempt.

DISCUSSION

Subject’s Proficiency in the Task

In contrast with other Cebus species, few tool use experiments havebeen carried out with C. olivaceus (Urbani, 1999). We have documentedthe use of tools to probe syrup by wedge-capped capuchins. In contrast to

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Fragaszy and Adams-Curtis (1991), we observed no spontaneous probingin holes with sticks before introducing the apparatus, i.e., during the 6-mopreliminary phase of observation. The two tool-users differed from the non-users in terms of presence and in the types of activity performed on theapparatuses (Fragaszy and Visalberghi, 1989).

Results from this task illustrate the need to master the motor skills andspatial and temporal components involved in tool use. Monkeys learnedhow to operate their tools by manipulating the end part which fits into theopenings of the apparatus. There was a gradual extinction of wrong end er-rors (type 1 errors) and, to a lesser extent, of other errors (type 2 errors).This finding follows the pattern typical of associative learning in skill im-provement (Visalberghi, 1987). Nevertheless, the fact that until the end ofthe study, the solvers continued intermittently to use the wrong end of thetools, and tried to solve the task by pounding (striking), indicates that theydid not achieve a causal understanding of the task and effective/ineffectivemanipulative properties of the tools (Visalberghi and Limongelli, 1994).

Although Lagace was proficient in nut cracking with hammers, hefailed to channel the action into correct use of the probing tools. Lagaceattempted to repeat actions that proved successful in previous tasks thatinvolved pounding and exhibited a greater number of vigorous actions to-wards the apparatus than the others. Striking an object (the apparatus) withsteel bolts may seem an appropriate foraging activity. Moreover, Lagaceand Henein were proficient in actions involving finely controlled movementssuch as raking with sticks in order to get at out-of-reach food. Perhaps notbeing able to see the target (syrup) when manipulating probing tools hin-dered the fine eye-hand coordination necessary to complete this task andprevented their tool acquisition. In any case the subjects that used sticks inother contexts did not understand that the polyvalent nature of this standardtool could be used in the present task.

Observation of Group Members

The inclination to observe others is a prerequisite for the social trans-mission of novel motor behaviors, and monkeys are potentially able tolearn from being around others (Visalberghi and Fragaszy, 1996). PerhapsNeositu’s success was facilitated by his close and extended observation ofCurumim’s actions, and stimulated by access to the syrup that Curumimobtained when sharing the apparatus with him. However, Lagace attendedCurumim’s activities and Henein attended Neositu’s without becoming pro-ficient in tool use. While monkeys may be sensitive to the activities of others,there is no evidence that they comprehend the dynamics of what they see

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happening. Neositu learned more quickly at site A whereas he attended morefrequently to Curumim’s activities at site B than at site A (as illustrated bythe frequency of watching behaviors). These findings do not indicate thatdirect social transmission plays a major role in the acquisition of the instru-mental behavior in this group. In any case, there was no imitation of themanual procedure itself: Curumim used his right hand to hold the proximalend of the stick and his left hand to guide the distal end, while Neositu alwaysdid the reverse. In fact, a blend of spatial facilitation, observational patternsand generalization appears to have stimulated the first successful attemptsof Neositu. Tool use is usually limited to a subset of subjects, each apparentlylearning independently through a trial-and-error process (Byrne and Suomi,1996; Fragaszy and Visalberghi, 1989). Our data are consistent with the factthat subjects appear to acquire tool-using skills via their own investigativeactivities.

Social factors are essential constraints, and in the particular case of Cu-rumim it was obvious that he went from site A to site B, and vice versa,depending on the presence of others. For all subjects site B (visual moni-toring) was more attractive than site A. The reason for such a discrepancyis apparently due to the fact that subjects were more social at site B, whichis consistent with the results obtained in the preliminary phase of observa-tion, and experienced the two spatial contexts (A and B) differently. Resultsare consistent with the influence of social enhancement: when at site B, thesubjects showed greater tolerance for the presence of each other, and wereattracted by each others activities. Conversely, social enhancement that cancontribute to learning a new contingency (Visalberghi and Fragaszy, 1990)did not appear to play this role, given that subjects were more successful atsite A. It appears that the influence of social enhancement is likely to varynot only across individuals within a social group (Fragaszy et al., 1994) butalso across different spatial contexts.

Spatial Facilitation

Rate of success differs at sites A and B: Neositu and Curumim weremore efficient in probing actions in A (manipulation) than in B (visual mon-itoring). Neositu was more frequently present at site B but performed alower number of probing attempts than at site A. He only succeeded atsite B three sessions after having completed his first success in A. Moreover,the occurence of type 1 errors was more persistent in B than in A.

This finding could be interpreted as evidence that the activity elicitedby an instrumental task is spatial-context-dependent. This fact, which con-strains knowledge about the affordances of a spatial context (Turvey et al.,

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1981), may indicate a limitation in terms of controlling and exploiting whatis available in the surrounding environment, and this for even the other-wise skillful capuchins. In order to explain spatial influences on skillfulnessin tool-using behavior, we assume that monkeys, that do not experience ageometrical space but instead a broading of psychological perspective, areable, by virtue of their ability to create a meaningful space on their own, toimpose a structure on this space and by doing so, elicit the emergence ofspatial affordances (object meaning and function). Our results highlight theimportant role played by spatial location in the solution of an instrumentaltask, and the influence of spatial context in constraining the degree to whichskills may be acquired.

ACKNOWLEDGMENTS

This research was supported by the CAPES Agencies (Grant No. CDI728-11). Subjects were housed at the National Primatological Center(CENP) in Ananindeua, Para, Brazil. Thanks to William L. Martin andBonnie Brusky who checked the English text, and to two anonymous refer-ees for comments on an earlier version of the manuscript.

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Spatial Facilitation in a Probing Task in Wedge-Capped Capuchins (Cebus olivaceus)