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True imitation in marmosets
ANIMAL BEHAVIOUR, 2000, 60, 195–202 doi:10.1006/anbe.2000.1457, available online at http://www.idealibrary.com on
True imitation in marmosets BERNHARD VOELKL & LUDWIG HUBER
Institute of Zoology, University of Vienna (Received 20 September 1999; initial acceptance 29 October 1999; final acceptance 1 April 2000; MS. number: 6359R)
Marmosets, Callithrix jacchus, observed a demonstrator removing the lids from a series of plastic canisters to obtain a mealworm. When subsequently allowed access to the canisters, marmosets that observed a demonstrator using its hands to remove the lids used only their hands. In contrast, marmosets that observed a demonstrator using its mouth also used their mouth to remove the lids. Since hand and mouth demonstrators brought about identical changes in the canisters, the differential test behaviour of the observer groups suggests that they learned about the demonstrator’s behaviour. Furthermore, marmosets that had not been given the opportunity to observe a demonstrator prior to testing had a low probability of mouth opening, even if the canisters were previously opened by a mouth-opening demonstrator in an olfactory control experiment. Corroborating Bugnyar & Huber’s (1997, Animal Behaviour, 54, 817–831) earlier findings, our results provide further evidence that marmosets can imitate.
agreement among researchers on the conclusion that recent evidence has not supported the existence of imitation in monkeys’ (Custance et al. 1999, page 14). To our knowledge, Bugnyar & Huber (1997) were the first to claim true movement imitation by monkeys, using marmosets as experimental subjects. However, their procedure had weaknesses (see below) and only two of the five observers tested matched the action sequence of the demonstrator. Furthermore, it has been suggested that these animals may not be able to learn anything more demanding from a demonstrator’s behaviour than to attend to either the relevant location (local enhancement, Thorpe 1963) or the relevant stimulus (stimulus enhancement, Spence 1937; see Visalberghi & Fragaszy 1990; Whiten & Ham 1992; Fragaszy & Visalberghi 1996; Moore 1996). Only recently have methods been designed that control for nonimitative social learning, irrespective of the cognitive complexity of these processes (Akins & Zentall 1996, 1998; Kaiser et al. 1997; Campbell et al. 1999). Early experiments on imitation in animals used a nonexposed control (Heyes et al. 1992) and compared the performance of animals allowed to observe a demonstrator peforming an action on an object for food (observers) with that of animals never given this opportunity (nonobservers). If the observers acquired the target response faster or more efficiently than the nonobservers (Zentall et al. 1996), it was concluded that they had imitated the demonstrator’s behaviour. To control for nonimitative factors such as motivational, perceptual and species-specific effects on the observer, experimentalists have used or recommended the two-action procedure (Dawson & Foss 1965; Galef
Over the last decade, the adoption of a cognitive approach to the study of animal behaviour has considerably improved our understanding of the processes underlying social learning. Researchers have investigated to which aspects of a conspecific’s instrumental behaviour animals attend, and which they understand, in particular contexts (reviews in Zentall & Galef 1988; Whiten & Ham 1992; Heyes 1994; Heyes & Galef 1996, 1998). In addition, a comparative approach has widened our knowledge of the taxonomic distribution of social learning processes. For example, some researchers have suggested that great apes are the only animals capable of learning a behaviour by seeing it done (‘true imitation’), at least ‘in the limited sense of copying for its own sake divorced from normal behaviour’ (Byrne & Tomasello 1995, page 1419; see also Byrne & Russon 1998). However, others have suggested that imitation is widely scattered among species (see, for instance, comments by Fishbein, Heimann, Huber, Roitblat, Vogt & Carey and Zentall on Byrne & Russon 1998). Although humans and great apes are the most prolific imitators, dolphins (Tayler & Saayman 1973), some birds such as parrots, Psittacus erithacus (Moore 1992), pigeons, Columba livia (Zentall et al. 1996; Kaiser et al. 1997) and Japanese quail, Coturnix japonica (Akins & Zentall 1996, 1998) show some evidence of imitative learning as well. Nevertheless, although improved procedures have ‘indicated that a range of species can imitate’ (Heyes & Galef 1998, page 74), ‘there has been a relatively high amount of Correspondence: L. Huber, Department of Theoretical Biology, Institute of Zoology, University of Vienna, Biocenter, Althanstrasse 14, A-1090 Vienna, Austria (email: [email protected]). 0003–3472/00/080195+08 $35.00/0
2000 The Association for the Study of Animal Behaviour
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et al. 1986; Galef 1988; Whiten & Ham 1992). In this procedure, groups of animals are compared after they observed a conspecific demonstrator performing one of two or more alternative actions on a single manipulandum. For example, Dawson & Foss (1965) allowed budgerigars, Melopsittacus undulatus, to observe demonstrators removing the lid from a bowl by either pushing or twisting it off with the beak, or twisting it off with a foot. True imitation may be said to have occurred if the observer groups differ significantly in the proportion of the two actions performed during their initial attempts to manipulate the test object; that is, if they show a bias towards the demonstrator’s response (see Galef et al. and Tomasello in Heyes & Galef 1996). The two-action procedure may be contrasted with the two-object procedure (Campbell et al. 1999), in which the performances of two observer groups are compared after they witnessed a demonstrator manipulating one of two different objects or parts of an object. In this procedure, the information acquired by the observers may consist of knowing what parts of the physical environment are relevant for a task or where to begin manipulating an object. A clear separation of the two types of learning is not easy to achieve. Campbell et al. (1999) allowed starlings, Sturnus vulgaris, to observe demonstrators removing a plug from a hole in the lid of a food container either by pulling on a loop of string attached to the plug or by pushing the plug down. As the authors admitted, these two actions may have rendered different regions of the plug attractive (Lefebvre et al. 1997). The two groups of observers may also have learned different affordances of the plug (i.e. dynamic properties, potential uses; Gibson 1966; Tomasello et al. 1987), for example, that the plug moved up and out of the food canister when lifted, and down and into the canister when pushed. Therefore, to determine whether animals learn by observation about responses or about changes of state in the environment, a two-action/one-outcome procedure is preferable. Zentall and colleagues ruled out observed differences in the movement of a manipulandum by comparing naïve pigeons (Zentall et al. 1996) and quail (Akins & Zentall 1996) that had observed a demonstrator either pecking at or stepping on a treadle for food. In both studies, a significant correlation was found between the observers’ performance and the demonstrated behaviour even though only the demonstrators’ response topographies (pecking versus stepping) differed but not the effects on the environment. A further methodological complication emerges when one attempts to determine whether the copied action was elicited by nonimitative processes such as contagion (Thorpe 1963), rather than acquired as a result of learning a novel or improbable motor act (Thorpe 1956, 1963; Meltzoff 1988; Zentall 1988; Whiten & Custance 1996). For example, if a specific response is part of the animal’s behavioural repertoire for approaching an object, such as pecking is in pigeon or quail, the observation of a pecking demonstrator may have acted as an innate releaser of pecking in the observer (Akins & Zentall 1996, 1998; Zentall et al. 1996). In combination with stimulus enhancement, or increased attention towards the demon-
strator’s manipulandum, contagion may be sufficient to explain demonstrator-consistent responding in observers (Campbell et al. 1999). Huber (1998) argued that novelty should be used more carefully as a means of identifying cases of true imitation for two reasons. First, there is little agreement as to how novelty should be defined. Second, it is difficult to see how the emergence of novel behaviours could be identified. However, Thorpe’s (1963, page 135) definition of imitation ‘as the copying of a novel or otherwise improbable act or utterance’ makes these problems more manageable. The probability that an action will be performed could be determined by using a group of nonobservers and measuring the frequency of occurrence of the target action. Using this method, Bugnyar & Huber (1997) showed that the exact reproduction of a sequence of actions used by a demonstrator to open a pendulum door was improbable. Therefore, the exact reproduction of the demonstrator’s sequence by two of the observers was interpreted as evidence of imitation. We permitted two groups of marmosets, Callithrix jacchus, to observe a demonstrator using one of two alternative techniques and compared their initial test responses with one another and with a third group of marmosets that were never given the opportunity to observe a demonstrator. The particular requirement of our experiment was that the two opening techniques (pulling with a hand versus pulling with the mouth) have the same effect on the environment, that is, the lid to be opened would ‘behave’ identically if moved automatically. Furthermore, one technique consisted of a behavioural ‘peculiarity’ (mouth opening), that is, mouth opening was neither common in the animals under investigation nor necessary for lid removal. This requirement ensured that if the technique was performed by the observers, then they were most probably influenced by what they witnessed (Whiten & Custance 1996; Whiten et al. 1996; Custance et al. 1999). Mouth opening was occasionally found in one female marmoset out of five animals and occurred as a by-product of a previous experiment on associative learning. We expected that observation of a mouth-opening demonstrator would affect the probability of other monkeys showing this behaviour. On the other hand, we predicted that observation of hand opening would have no effect on the probability of mouth opening by the monkeys. We tested this by making the removal of the lid more difficult (and perhaps mouth opening more efficient). We also used a nonexposed control group to control for nonsocial factors and to assess the baseline probability of the mouth-opening response. Finally, given the current concern in the literature with the potential role of olfactory cues in promoting demonstrator-consistent responding, we included an olfactory control group. METHODS
Subjects The subjects were 36 adult common marmosets, of which two were demonstrators and 11 were observers. We
VOELKL & HUBER: TRUE IMITATION IN MARMOSETS
used 11 subjects (including the two models) for the nonexposed control and 14 for the olfactory control. The animals were maintained in four family groups at the Institute of Zoology of Vienna University, Austria, two family groups at the Konrad Lorenz Institute for Evolution and Cognition-Research, Altenberg, Austria, and three family groups at the Instituto Superiore di Sanita, Rome, Italy. All animals were born in captivity. At the Institute of Zoology two groups lived in indoor cages (250250250 cm) that were attached to outdoor cages of the same size and two groups lived in indoor cages (12080 cm and 180 cm high and 260260 cm and 250 cm high, respectively). At the Konrad Lorenz Institute both groups lived in indoor cages (200350 cm and 300 cm high). At the Instituto Superiore di Sanita the groups lived in indoor cages (15050 cm and 220 cm high). All cages were equipped with branches, ropes and living plants. All animals were fed fruits, vegetables, monkey pellets and protein supplements. The temperature was 26–30C during the day and 21–23C at night. The humidity was ca. 70–80%. In summer daylight was the main source of lighting, while in winter additional UV-fluorescent tubes were used to maintain a 12:12 h light:dark cycle.
Apparatus The apparatus consisted of a wooden board (1033 cm) with five black plastic film canisters for 35-mm Kodak slide films attached to it with screws. The board and the lids of the film canisters were painted blue. In each session the subjects were given three identical boards (with a total of 15 canisters). The canisters were each filled with one mealworm as a reward. In the observer sessions and in the first test session the lids of the canisters were half shut (only one half of the lid was firmly attached to the canister, whereas the other half did not click into place and therefore left a gap between the lid and the upper end of the canister) while in the second test session the lids were completely shut. At the laboratories in Altenberg and Rome the experiments were conducted in the home cage of the subjects, while the subjects in Vienna were tested in an experimental cage (12070 cm and 260 cm high) adjoined to the home cage.
Procedure Group Mouth In a previous experiment, female BI was the only one of five subjects that opened the canisters by removing the lids with its mouth (Fig. 1a). This animal was selected as the mouth-opening demonstrator. The other subjects in this previous experiment were not used in the present one. In six training sessions BI was separated from the other group members and we confirmed its original preference for the mouth-opening technique by offering completely shut canisters, which could only be opened by this technique. After the subject performed the task well (making only correct responses within three
Figure 1. Schematic representation of the two opening techniques performed by (a) the mouth-opening demonstrator and (b) the hand-opening demonstrator.
successive sessions and needing less than 2 min for each session), we gave BI two more sessions with half-shut canisters. After we confirmed that BI continued with this technique (only mouth opening in two sessions), we used it as demonstrator for six subjects (observers) of its neighbouring group (group Mouth). During the observation sessions, the other animals of BI’s group were locked out and we placed the three boards 25 cm from the wire-mesh partition that separated BI’s cage from the observers’ cage. The demonstrator (BI) was then allowed to open the canisters while all the observers had the opportunity to observe it. We conducted two observation sessions each day. The sessions were terminated as soon as the demonstrator had opened all the canisters. Immediately after the fifth observation session all the observers were tested individually in two successive test sessions. For this purpose we removed all but one subjects of the observer group from the observers’ cage and placed the boards into that cage. In the first test session the canisters were half shut and the subjects had a maximum of 10 min to open them. If the subjects needed less than 10 min to open the 15 canisters, the session was terminated earlier. After the first
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test session the subjects immediately had a second test session, in which the canisters were completely shut. The session was again limited to 10 min.
the subjects were tested individually in their home cages. The sessions were terminated after 15 min. In this experiment we gave all the subject two boards with a total of 10 canisters in each session.
Group Hand A male subject (GR) was separated from its group and confronted with the apparatus with half-shut canisters. GR spontaneously started to open the canisters using its hand (Fig. 1b). To confirm that GR opened the canisters in this manner we repeatedly offered only half-shut canisters. Unlike the first demonstrator (BI), GR was not given completely shut canisters, but it had seven successive training sessions with half-shut canisters. During these training sessions the experimental cage was visually isolated from the home cage by a cardboard partition. After GR had shown only correct responses within the last three sessions, it was used as a demonstrator. We removed the cardboard screen and placed the demonstrator in the experimental cage while the other group members (group Hand) could observe it. Again we conducted five sessions. The sessions were terminated as soon as the demonstrator had opened all the canisters. After these observation sessions every observer was separately tested in the experimental cage as described above.
Nonexposed control group To assess the frequency of spontaneous mouth opening we conducted a control experiment. The control group consisted of 11 individuals that had access to the boards without having the opportunity to observe a social model. As in the previous experiments, the subjects were tested individually in their home cages. The sessions were terminated after 15 min. If the subjects did not succeed in opening at least three canisters in one session, further sessions were added on subsequent days.
Olfactory control group Odour cues may have influenced our marmosets’ behaviour. The mouth-opening demonstrator (BI) may have left saliva containing food particles on the lids of the canisters, making its observers more likely to sniff at the lids than the marmosets that observed the hand-opening demonstrator. If this is correct, scent-mediated local enhancement instead of, or in addition to, response learning by observation might have been responsible for demonstrator-consistent responding in the mouth-opening observers. To determine whether differences in the opening techniques used by the two groups of observers resulted from a tendency for mouth-opening observers to approach the lid with their head and/or mouth, we analysed videotapes of these approaches in detail. We also conducted a second control experiment to determine more directly whether olfactory or visual cues, that is saliva or scratches, that the previous mouthopening animal might have left on the canisters’ lids, influence the subjects’ behaviour. This control group consisted of 14 subjects that had access to canisters that were previously opened by another animal by mouth. The subjects could not see the other animal opening the canisters, so this was again a nonexposed control. Again,
Data Analysis All sessions were videotaped with a DV camcorder (Sony VX 1000). We classified the behaviour at the apparatus as either mouth opening or hand opening. An action was called mouth opening when the subject bit into the lid and raised its head while still keeping a firm hold on the lid with its teeth (Fig. 1a). An act was called hand opening when a subject inserted one or more fingers at the edge of the lid and lifted the lid by stretching its forearm (Fig. 1b). As in studies with pigeons and quail in which stepping and pecking responses were compared (Akins & Zentall 1996, 1998; Zentall et al. 1996; Kaiser et al. 1997), the two response topographies contrasted here (mouth versus hand opening) were easily distinguished by the experimenter. Here, too, the postures and body parts involved in the two responses were different (compare Fig. 1a and b). Sometimes a subject opened the lid only half way by hand or mouth, then put its head into the gap between the lid and the canister, which caused the lid to open. If such a sequence was started by one of the two actions (mouth opening or hand opening) we accordingly classified it as mouth opening or hand opening. If a subject did not open the canister with the first movement and repeatedly used the same technique several times in succession, we counted this as one action. If a subject did not open the canister with the first movement (i.e. hand opening) and switched to the other opening technique (i.e. mouth opening) and opened the lid, we recorded this as mouth opening, because only full actions entered into the analysis. We defined a full action as an opening action where the lid was removed completely from the canister. The subjects could reach the reward only if the lid was completely removed. As every canister was filled with a mealworm, each full action was rewarded. The entire database was coded from videotape by B.V. To measure observer reliability we selected two short video sequences: one with 10 opening acts of an observer of group Hand and one with seven opening acts of an observer of group Mouth. We asked 11 independent persons to classify the opening acts as hand opening’, ‘mouth opening’ or ‘not visible’ (when the opening act was not clearly visible on the videotape). The persons did not know that one of the subjects had a mouth-opening demonstrator and the other a hand-opening demonstrator. They coded 99.42.2% (XSD) of the 17 actions in the same way that B.V. did. This indicates that these actions were clear and easy to distinguish and therefore the coding bias was negligible. RESULTS
Observation Phase While being observed, both demonstrators showed perfect discrimination between the two opening techniques.
VOELKL & HUBER: TRUE IMITATION IN MARMOSETS
Number of subjects
Hand opening
Mouth opening
8 NS 6 * 4
2
Mouth
Hand
Mouth
Hand
Group Figure 2. Number of observers that opened the canisters at least once by hand (Hand opening) or by mouth (Mouth opening) during the first test session. Six observers saw a mouth-opening demonstrator (group Mouth) and five saw a hand-opening demonstrator (group Hand). *P<0.05.
Both were presented with 75 canisters. The demonstrator for group Mouth (BI) opened all 75 canisters (100%) using its mouth. The demonstrator for group Hand (GR) opened 74 out of 75 canisters (98.7%) with its hand. One lid accidentally opened when GR jumped on to the board. GR opened the lid only half way by hand 12 times and removed the lid by putting its head into the canister.
Test Phase: First Test Session In both groups, all the subjects opened at least one canister with their hand, but opening the canisters with the mouth was shown by four out of six subjects from
group Mouth while none of the five subjects in group Hand opened a canister with its mouth (Fig. 2). Despite the small group size this difference was statistically significant (Fisher’s exact test: N=11, P=0.045). To compare the performance of the two groups we calculated a discrimination ratio for each subject by dividing the number of hand-opening acts performed during the first test session by the total number of opening acts during that session. The mean discrimination ratioSD was 0.640.34 (N=6) for group Mouth, and 1.000 (N=5) for group Hand (Table 1). We computed the standardized deviates (Sokal & Rohlf 1995) separately for each subject’s discrimination ratio, pooled the resulting deviates and tested them for normality by a Kolmogorov–Smirnov test for goodness of fit. The observed data did not depart significantly from a normal distribution (Z=0.754, P=0.62) and heterogeneous variances were assumed. Therefore we used Welch’s t test (Sokal & Rohlf 1995) to compare the means of the two groups. The discrimination ratios for groups Hand and Mouth were significantly different (t4.5 =2.33, P=0.033, one tailed).
Test Phase: Second Test Session In the second test session the canisters were completely shut and could only be opened by mouth. This session was conducted to investigate if the subjects that used only their hands in the first session were also able to open canisters with the mouth. From the two subjects from group Mouth that did not use the mouth in the first session, one immediately began to open the canisters with its mouth, whereas none of the subjects from group Hand managed to open a canister with its mouth. Thus in the second test session five out of six subjects from group Mouth opened the canisters with their mouth and one
Table 1. Opening behaviour of the observers and control subjects during the first and second test sessions Session 1
Group Mouth
Hand
Control
Subject DV MO WI SQ NI MA Mean KL SU VI GI SH Mean Mean
Nose-near-lid approaches
Mouth opening
Hand opening
Opened canisters
Discrimination ratio
Session 2 Opened canisters
3 2 4 5 7 0 3.5 2 2 3 5 5 3.4
0 6 13 11 2 0 5.3 0 0 0 0 0 0 1.0
15 8 2 4 13 15 9.5 15 15 15 15 14 14.8 10.9
15 14 15 15 15 15 14.8 15 15 15 15 14 14.8 13.0
1.00 0.57 0.13 0.27 0.87 1.00 0.64 1.00 1.00 1.00 1.00 1.00 1.00 0.92
0 15 15 15 6 15 11 0 0 0 0 0 0 1.6
The total numbers of nose-near-lid approaches, mouth-opening and hand-opening actions and opened canisters and the discrimination ratio (the number of hand-opened canisters divided by the total number of opened canisters) are shown for session 1. For session 2 only the total number of opened canisters is shown, as all canisters were opened by mouth. For the nonexposed control group (N=11) only the mean values are shown.
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subject failed to open at least one canister within 10 min, while none of the five subjects from group Hand succeeded in opening a canister (Fisher’s exact test: N=11, P=0.013).
mouth opening. The mean discrimination ratioSD was 0.850.34. The subjects opened the canisters significantly more often with their hands (Wilcoxon signed-ranks test: Z=2.128, P=0.033, two tailed).
Olfactory Exploration
Olfactory Control Group
Animals of both groups typically sniffed at the canisters, especially during the first test session. This behaviour was clearly part of their olfactory exploration at the onset of the test. We counted all approaches where an animal’s nose touched the lid of a canister, or came very close (to within 5 mm) to the lid (nose-near-lid). The mean number of nose-near-lid bouts until the first canister was openedSD was 3.52.4 for group Mouth and 3.41.5 for group Hand and the number of nose-near-lid bouts during the entire first session was 13.75.6 for group Mouth and 13.23.3 for group Hand. The mean latency to the first nose-near-lid boutSD was 45.844.2 s for group Mouth and 21.02.6 s for group Hand. Again we used the standardized values of both groups to test them for normality by a Kolmogorov–Smirnov test for goodness of fit. The observed data did not depart significantly from a normal distribution for the number of bouts until the first canister was opened (Z=0.463, N=11, P=0.983), for the number of bouts during the first session (Z=0.537, N=11, P=0.935) and for the latency to the first bout (Z=0.754, N=11, P=0.621). Therefore we used a two-tailed t test to compare the number of bouts until the first canister was opened and the number of bouts during the first session. To compare the latencies to the first bout a Welch’s t test was used after Levene’s test for equality of variances found heterogeneous variances between the two groups (F5,4 =5.998, P=0.037). No significant differences were found between group Hand and group Mouth in the number of nose-near-lid bouts until the first canister was opened (t test: t9 =0.08, P=0.938), the number of nose-near-lid bouts during the entire first test session (t test: t9 =0.16, P=0.874) and the latency to the first nose-near-lid bout (Welch’s t test: t4.5 =1.37, P=0.228). These data cannot exclude the possibility that the observers smelled some deposits on the lid without being influenced in the way they approached the canisters; the same is true for visual cues such as saliva droplets on the lid. But the argument that such cues promoted the approach with the head towards the lid and thus facilitated the probability of mouth opening is not supported by our data.
This control group consisted of 14 subjects. Five did not open any canister within the 15 min of the test session. Of the remaining nine subjects, eight opened the canisters with their hands and only one opened them with its mouth. The mean discrimination ratioSD was 0.89 0.33. The subjects opened the canisters significantly more often with their hands (Wilcoxon signed-ranks test: Z=2.433, P=0.015, two tailed). A comparison of the mean discrimination ratio with the nonexposed control group showed no significant difference (Mann–Whitney U test: U=41.5, N1 =11, N2 =14, P=0.652) whereas a comparison of the mean discrimination ratio with group Mouth was significant (Mann–Whitney U test: U=10.0, N1 =6, N2 =14, P=0.016) even when we applied a Bonferroni method (Sokal & Rohlf 1995) to evaluate the experimentwise error rate, which reduced the critical P value to 0.025. Thus the subjects from group Mouth opened the canisters significantly more often with their mouth than the subjects from the olfactory control group, which were given canisters previously mouth-opened by another monkey. On the other hand no difference could be found between the olfactory control group and the nonexposed control group, where the subjects were given canisters that were not previously mouth-opened. Therefore visual or olfactory cues on the lids of the canisters were not sufficient to promote mouth opening in naïve monkeys.
Nonexposed Control Group The nonexposed control group consisted of 11 subjects, including BI and GR, the two models. Two subjects did not open even one canister within the first test session and two opened fewer than three canisters. However, these four subjects successfully opened canisters in the second test session. To assess the discrimination ratio of these animals, we pooled the data from the first and second test sessions. Only two of 11 subjects showed
DISCUSSION Common marmosets copied the response topography of a conspecific demonstrator to open a Kodak film canister and obtain a desired food item. More specifically, marmosets that had observed a demonstrator using its mouth to remove the lid from a film canister were more likely to use this technique during a subsequent test session than marmosets that had observed a demonstrator using exclusively its hand. In fact, mouth opening was rare in 30 subjects that had never seen a mouth-opening demonstration or any opening demonstration before. These results are consistent with a previous study of imitative learning in marmosets (Bugnyar & Huber 1997) and raise doubts about the claim that the ability to imitate is unique to great apes, including humans (Tomasello & Call 1997; Byrne & Russon 1998). This effect cannot be accounted for by either enhancement effects or object movement re-enactment (learning how an object moves; Heyes 1998), since the lid of the canisters moved in the same way for both observer groups. Contagion is also an unlikely explanation, since the observers were tested in the absence of a demonstrator. Finally, it is also unlikely that olfactory cues influenced the direction and strength of the observers’ approach behaviour. A control experiment showed that
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deposits left by the demonstrators on the lids of the canisters did not increase the probability of mouth opening. Observers of hand-opening demonstrators also sniffed the lid as frequently and closely as observers of mouth-opening demonstrators. After decades of refining both methods and terminology, the future of social learning will inevitably involve attempts to extend the range of species comparisons. Not only will questions of how animals become proficient imitators achieve heuristic value, but also questions about what conditions promote social learning in contrast, or in addition, to individual learning. As suggested by Caldwell et al. (1999), the all-or-none approach to imitation is being superseded by an approach that recognizes the complex concatenations of the processes and circumstances of social learning. The repeated failure to find robust imitative effects in animals other than apes may be due to either an overestimation of the species’ manipulative abilities or an underestimation of the species’ other capacities that render the task more manageable. For example, marmosets experienced difficulty in turning a handle in order to open a plastic box with a hinged lid (Caldwell et al. 1999) and olfactory cues played a greater role than visual cues in the rat’s exploratory behaviour (Mitchell et al. 1999). To identify the conditions under which robust imitative effects occur, we need some understanding of the species’ ecological niche and the natural context in which movement imitation appears. In humans, and probably in some great apes and dolphins, faithful copying of a demonstrator’s behaviour is part of a social game. Learning to exploit hidden food sources may be well established in highly explorative and manipulative mammals (e.g. chimpanzees, Pan troglodytes: Whiten et al. 1996) and birds (e.g. ravens, Corvus corax: Fritz & Kotrschal 1999; keas, Nestor notabilis: L. Huber, S. Rechberger & M. Taborsky, unpublished data). Vocal mimicry is widespread among birds and common in humans, but occurs rarely, if ever, in great apes and other mammals (Moore 1996). Furthermore, the occurrence of social-learning mechanisms may also be influenced by the species’ group size (Boyd & Richerson 1996) and social tolerance (Coussi-Korbel & Fragaszy 1995). In tolerant primate groups, such as the marmoset family, individuals often follow one another, exploring the forest canopy and approaching others busy with interesting objects. In these situations, copying behaviour is likely to occur, especially if an individual cannot understand the causal structure of the task. Recently, Huber (1998) argued that copying fidelity would be especially high if it was not affected by an insight into the causal relationships of the task (programme imitation; Byrne & Byrne 1993), the affordances of the objects (emulation or affordance learning; Tomasello 1996) or the goal and intentions of the demonstrator (goal emulation; Whiten & Ham 1992). If all of these types of information are beyond the cognitive capacity of the species, then slavish copying is a valuable alternative. Behavioural peculiarities, unnecessary extensions and even errors in performance can be used to determine the degree and type of behavioural matching. In the present experiment, we were able to benefit from a peculiar
opening technique shown by a single female during a pilot study. We further profited from the fact that this behavioural peculiarity involved an action that differed on a large scale from the default action in that it involved a different body part. Thus, we avoided a problem common to studies of social learning in great apes (see Tomasello 1996 and Whiten & Custance 1996 for reviews), in which a complex object or a tool is manipulated with the hands in one of two or more different ways, only one of which is demonstrated to a subject. A further advantage of our two-action/one-peculiarity approach is that copying of a peculiar behaviour qualifies as being truly imitative. According to Thorpe (1963), one should consider only motor acts that do not pre-exist in the animal’s behavioural repertoire at the onset of the experiment, otherwise socially mediated behaviour (contagion) would be sufficient to result in behavioural matching. We were able to show that the probability of spontaneous mouth-opening behaviour was low; in the two nonobserver control groups mouth opening was rare and in the hand-opening observer group it never occurred. Although mouth opening may not be completely novel at the level of motoric execution, it is a rather novel technique for opening plastic film canisters (see Akins & Zentall 1996 for a similar argument on ‘novelty’). To conclude, our findings support the suggestion that basic forms of imitative learning occur not only in humans and great apes but also in monkeys. Regardless of the mechanism responsible for behavioural matching, it seems plausible that social learning allows the experience of one individual to be acquired by others more efficiently than would be the case with trial-and-error learning (Boyd & Richerson 1988). As we saw here, and also in Bugnyar & Huber (1997), even faithful copying in the absence of insight may help to solve a task that otherwise could not be solved. Those monkeys in our study that did not have the opportunity to observe a mouth-opening demonstrator failed to open canisters, and hence to obtain a highly nutritious food, when the canisters were completely closed (second test session). This is especially interesting in the case of the hand-opening observers, which had extensive experience with the canisters. Thus, our findings also provide some support for the hypothesis that social learning may be adaptive. Acknowledgments This experiment was conducted by B.V. in partial fulfillment of the requirements for the Master degree in Zoology at the University of Vienna. Ruth Sonnweber built the apparatus and conducted a pilot study. Augusto Vitale, Armelle Queyras and Michela Zanzony helped conduct the control experiment. Financial support was provided by the Austrian Science Foundation (FWF-grant P 12011-BIO). We thank Celia Heyes for comments and Fiona Campbell for improving the English. References Akins, C. K. & Zentall, T. R. 1996. Imitative learning in male Japanese quail (Coturnix japonica) using the two-action method. Journal of Comparative Psychology, 110, 316–320.
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Akins, C. K. & Zentall, T. R. 1998. Imitation in Japanese quail: the role of reinforcement of demonstrator responding. Psychonomic Bulletin and Review, 5, 694–697. Boyd, R. & Richerson, P. J. 1988. An evolutionary model of social learning: the effect of spatial and temporal variation. In: Social Learning: Psychological and Biological Perspectives (Ed. by T. R. Zentall & B. G. Galef, Jr), pp. 29–48. Hillsdale, New Jersey: L. Erlbaum. Boyd, R. & Richerson, P. J. 1996. Why culture is common, but cultural evolution is rare. In: Evolution of Social Behaviour Patterns in Primates and Man (Ed. by W. G. Runciman, J. Maynard Smith & R. I. M. Dunbar), pp. 77–93. Oxford: Oxford University Press. Bugnyar, T. & Huber, L. 1997. Push or pull: an experimental study on imitation in marmosets. Animal Behaviour, 54, 817–831. Byrne, R. W. & Byrne, J. M. E. 1993. Complex leaf-gathering skills of mountain gorillas (Gorilla g. beringei): variability and standardization. American Journal of Primatology, 31, 241–261. Byrne, R. W. & Russon, A. E. 1998. Learning by imitation: a hierarchical approach. Behavioral and Brain Sciences, 21, 667–721. Byrne, R. W. & Tomasello, M. 1995. Do rats ape? Animal Behaviour, 50, 1417–1420. Caldwell, C. A., Whiten, A. & Morris, K. D. 1999. Observational learning in the marmoset monkey (Callithrix jacchus). In: AISB Convention: Symposium on Imitation in Animals and Artifacts (Ed. by K. Dautenhahn & C. Nehaniv), pp. 27–31. Edinburgh: The Society for the Study of Artificial Intelligence and the Simulation of Behaviour. Campbell, F. M., Heyes, C. M. & Goldsmith, A. R. 1999. Stimulus learning and response learning by observation in the European starling, in a two-object/two-action test. Animal Behaviour, 58, 151–158. Coussi-Korbel, S. & Fragaszy, D. M. 1995. On the relation between social dynamics and social learning. Animal Behaviour, 50, 1441– 1453. Custance, D., Whiten, A. & Fredman, T. 1999. Social learning of an artificial fruit task in capuchin monkeys (Cebus apella). Journal of Comparative Psychology, 113, 13–23. Dawson, B. V. & Foss, B. M. 1965. Observational learning in budgerigars. Animal Behaviour, 13, 470–474. Fragaszy, D. M. & Visalberghi, E. 1996. Social learning in monkeys: primate ‘primacy’ reconsidered. In: Social Learning in Animals: the Roots of Culture (Ed. by C. M. Heyes & B. G. Galef, Jr), pp. 65–84. San Diego: Academic Press. Fritz, J. & Kotrschal, K. 1999. Social learning in common ravens, Corvus corax. Animal Behaviour, 57, 785–793. Galef, B. G. Jr. 1988. Imitation in animals: history, definition and interpretation of data from the psychology laboratory. In: Social Learning: Psychological and Biological Perspectives (Ed. by T. R. Zentall & B. G. Galef, Jr), pp. 207–223. Hillsdale, New Jersey: L. Erlbaum. Galef, B. G. Jr, Manzig, L. A. & Field, R. M. 1986. Imitation learning in budgerigars: Dawson and Foss (1965) revisited. Behavioural Processes, 13, 191–202. Gibson, J. J. 1966. The Senses Considered as Perceptual Systems. Boston: Houghton Mifflin. Heyes, C. M. 1994. Social learning in animals: categories and mechanisms. Biological Review, 69, 207–231. Heyes, C. M. 1998. Theory of mind in nonhuman animals. Behavioral and Brain Sciences, 21, 101–148. Heyes, C. M. & Galef, B. G. Jr (Eds) 1996. Social Learning in Animals: the Roots of Culture. San Diego: Academic Press. Heyes, C. M. & Galef, B. G. Jr. 1998. The Napoli social learning conference. Introduction. International Journal of Comparative Psychology, 11, 73–92. Heyes, C. M., Dawson, G. R. & Nokes, T. 1992. Imitation in rats: initial responding and transfer evidence. Quarterly Journal of Experimental Psychology, 45B, 229–240.
Huber, L. 1998. Movement imitation as faithful copying in the absence of insight (comment on Byrne & Russon). Behavioral and Brain Sciences, 21, 694. Kaiser, D. H., Zentall, T. R. & Galef, B. G. Jr. 1997. Can imitation in pigeons be explained by local enhancement together with trialand-error learning? Psychological Science, 8, 459–460. Lefebvre, L., Templeton, J., Brown, K. & Koelle, M. 1997. Carib crackles imitate conspecific and Zenaida dove tutors. Behaviour, 134, 1003–1017. Meltzoff, A. N. 1988. Imitation, objects, tools, and the rudiments of language in human ontogeny. Human Evolution, 3, 45–64. Mitchell, C. J., Heyes, C. M., Gardner, M. R. & Dawson, G. R. 1999. Limitations of a bidirectional control procedure for the investigation of imitation in rats: odour cues on the manipulandum. Quarterly Journal of Experimental Psychology, 52B, 193– 202. Moore, B. R. 1992. Avian movement imitation and a new form of mimicry: tracing the evolution of a complex form of learning. Behaviour, 122, 231–263. Moore, B. R. 1996. The evolution of imitative learning. In: Social Learning in Animals: the Roots of Culture (Ed. by C. M. Heyes & B. G. Galef, Jr), pp. 245–265. San Diego: Academic Press. Sokal, R. R. & Rohlf, F. J. 1995. Biometry. New York: W. H. Freeman. Spence, K. W. 1937. Experimental studies of learning and higher mental processes in infra-human primates. Psychological Bulletin, 34, 806–850. Tayler, C. K. & Saayman, G. S. 1973. Imitative behaviour by Indian Ocean bottlenose dolphins (Tursiops aduncus) in captivity. Behaviour, 44, 286–298. Thorpe, W. H. 1956. Learning and Instinct in Animals. London: Methuen. Thorpe, W. H. 1963. Learning and Instinct in Animals. 2nd edn. London: Methuen. Tomasello, M. 1996. Do apes ape? In: Social Learning in Animals: the Roots of Culture (Ed. by C. M. Heyes & B. G. Galef, Jr), pp. 319–346. San Diego: Academic Press. Tomasello, M. & Call, J. 1997. Primate Cognition. New York: Oxford University Press. Tomasello, M., Davis-Dasilva, M., Camak, L. & Bard, K. 1987. Observational learning of tool-use by young chimpanzees. Human Evolution, 2, 175–183. Visalberghi, E. & Fragaszy, D. M. 1990. Do monkeys ape? In: ‘Language’ and Intelligence in Monkeys and Apes. Comparative Developmental Perspectives (Ed. by S. T. Parker & K. R. Gibson), pp. 247–273. Cambridge: Cambridge University Press. Whiten, A. & Custance, D. 1996. Studies in imitation in chimpanzees and children. In: Social Learning in Animals: the Roots of Culture (Ed. by C. M. Heyes & B. G. Galef, Jr), pp. 291–318. San Diego: Academic Press. Whiten, A. & Ham, R. 1992. On the nature and evolution of imitation in the animal kingdom: reappraisal of a century of research. In: Advances in the Study of Behavior (Ed. by P. J. B. Slater, J. S. Rosenblatt, C. Beer & M. Milinski), pp. 239–283. New York: Academic Press. Whiten, A., Custance, D. M., Gomez, J.-C., Teixidor, P. & Bard, K. A. 1996. Imitative learning of artificial fruit processing in children (Homo sapiens) and chimpanzees (Pan troglodytes). Journal of Comparative Psychology, 110, 3–14. Zentall, T. R. 1988. Experimentally manipulated imitative behavior in rats and pigeons. In: Social Learning: Psychological and Biological Perspectives (Ed. by T. R. Zentall & B. G. Galef, Jr), pp. 191–206. Hillsdale, New Jersey: L. Erlbaum. Zentall, T. R. & Galef, B. G. Jr (Eds) 1988. Social learning: Psychological and Biological Perspectives. Hillsdale, New Jersey: L. Erlbaum. Zentall, T. R., Sutton, J. E. & Sherburne, L. M. 1996. True imitative learning in pigeons. Psychological Science, 7, 343–346.
True imitation in marmosets BERNHARD VOELKL & LUDWIG HUBER
Institute of Zoology, University of Vienna (Received 20 September 1999; initial acceptance 29 October 1999; final acceptance 1 April 2000; MS. number: 6359R)
Marmosets, Callithrix jacchus, observed a demonstrator removing the lids from a series of plastic canisters to obtain a mealworm. When subsequently allowed access to the canisters, marmosets that observed a demonstrator using its hands to remove the lids used only their hands. In contrast, marmosets that observed a demonstrator using its mouth also used their mouth to remove the lids. Since hand and mouth demonstrators brought about identical changes in the canisters, the differential test behaviour of the observer groups suggests that they learned about the demonstrator’s behaviour. Furthermore, marmosets that had not been given the opportunity to observe a demonstrator prior to testing had a low probability of mouth opening, even if the canisters were previously opened by a mouth-opening demonstrator in an olfactory control experiment. Corroborating Bugnyar & Huber’s (1997, Animal Behaviour, 54, 817–831) earlier findings, our results provide further evidence that marmosets can imitate.
agreement among researchers on the conclusion that recent evidence has not supported the existence of imitation in monkeys’ (Custance et al. 1999, page 14). To our knowledge, Bugnyar & Huber (1997) were the first to claim true movement imitation by monkeys, using marmosets as experimental subjects. However, their procedure had weaknesses (see below) and only two of the five observers tested matched the action sequence of the demonstrator. Furthermore, it has been suggested that these animals may not be able to learn anything more demanding from a demonstrator’s behaviour than to attend to either the relevant location (local enhancement, Thorpe 1963) or the relevant stimulus (stimulus enhancement, Spence 1937; see Visalberghi & Fragaszy 1990; Whiten & Ham 1992; Fragaszy & Visalberghi 1996; Moore 1996). Only recently have methods been designed that control for nonimitative social learning, irrespective of the cognitive complexity of these processes (Akins & Zentall 1996, 1998; Kaiser et al. 1997; Campbell et al. 1999). Early experiments on imitation in animals used a nonexposed control (Heyes et al. 1992) and compared the performance of animals allowed to observe a demonstrator peforming an action on an object for food (observers) with that of animals never given this opportunity (nonobservers). If the observers acquired the target response faster or more efficiently than the nonobservers (Zentall et al. 1996), it was concluded that they had imitated the demonstrator’s behaviour. To control for nonimitative factors such as motivational, perceptual and species-specific effects on the observer, experimentalists have used or recommended the two-action procedure (Dawson & Foss 1965; Galef
Over the last decade, the adoption of a cognitive approach to the study of animal behaviour has considerably improved our understanding of the processes underlying social learning. Researchers have investigated to which aspects of a conspecific’s instrumental behaviour animals attend, and which they understand, in particular contexts (reviews in Zentall & Galef 1988; Whiten & Ham 1992; Heyes 1994; Heyes & Galef 1996, 1998). In addition, a comparative approach has widened our knowledge of the taxonomic distribution of social learning processes. For example, some researchers have suggested that great apes are the only animals capable of learning a behaviour by seeing it done (‘true imitation’), at least ‘in the limited sense of copying for its own sake divorced from normal behaviour’ (Byrne & Tomasello 1995, page 1419; see also Byrne & Russon 1998). However, others have suggested that imitation is widely scattered among species (see, for instance, comments by Fishbein, Heimann, Huber, Roitblat, Vogt & Carey and Zentall on Byrne & Russon 1998). Although humans and great apes are the most prolific imitators, dolphins (Tayler & Saayman 1973), some birds such as parrots, Psittacus erithacus (Moore 1992), pigeons, Columba livia (Zentall et al. 1996; Kaiser et al. 1997) and Japanese quail, Coturnix japonica (Akins & Zentall 1996, 1998) show some evidence of imitative learning as well. Nevertheless, although improved procedures have ‘indicated that a range of species can imitate’ (Heyes & Galef 1998, page 74), ‘there has been a relatively high amount of Correspondence: L. Huber, Department of Theoretical Biology, Institute of Zoology, University of Vienna, Biocenter, Althanstrasse 14, A-1090 Vienna, Austria (email: [email protected]). 0003–3472/00/080195+08 $35.00/0
2000 The Association for the Study of Animal Behaviour
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et al. 1986; Galef 1988; Whiten & Ham 1992). In this procedure, groups of animals are compared after they observed a conspecific demonstrator performing one of two or more alternative actions on a single manipulandum. For example, Dawson & Foss (1965) allowed budgerigars, Melopsittacus undulatus, to observe demonstrators removing the lid from a bowl by either pushing or twisting it off with the beak, or twisting it off with a foot. True imitation may be said to have occurred if the observer groups differ significantly in the proportion of the two actions performed during their initial attempts to manipulate the test object; that is, if they show a bias towards the demonstrator’s response (see Galef et al. and Tomasello in Heyes & Galef 1996). The two-action procedure may be contrasted with the two-object procedure (Campbell et al. 1999), in which the performances of two observer groups are compared after they witnessed a demonstrator manipulating one of two different objects or parts of an object. In this procedure, the information acquired by the observers may consist of knowing what parts of the physical environment are relevant for a task or where to begin manipulating an object. A clear separation of the two types of learning is not easy to achieve. Campbell et al. (1999) allowed starlings, Sturnus vulgaris, to observe demonstrators removing a plug from a hole in the lid of a food container either by pulling on a loop of string attached to the plug or by pushing the plug down. As the authors admitted, these two actions may have rendered different regions of the plug attractive (Lefebvre et al. 1997). The two groups of observers may also have learned different affordances of the plug (i.e. dynamic properties, potential uses; Gibson 1966; Tomasello et al. 1987), for example, that the plug moved up and out of the food canister when lifted, and down and into the canister when pushed. Therefore, to determine whether animals learn by observation about responses or about changes of state in the environment, a two-action/one-outcome procedure is preferable. Zentall and colleagues ruled out observed differences in the movement of a manipulandum by comparing naïve pigeons (Zentall et al. 1996) and quail (Akins & Zentall 1996) that had observed a demonstrator either pecking at or stepping on a treadle for food. In both studies, a significant correlation was found between the observers’ performance and the demonstrated behaviour even though only the demonstrators’ response topographies (pecking versus stepping) differed but not the effects on the environment. A further methodological complication emerges when one attempts to determine whether the copied action was elicited by nonimitative processes such as contagion (Thorpe 1963), rather than acquired as a result of learning a novel or improbable motor act (Thorpe 1956, 1963; Meltzoff 1988; Zentall 1988; Whiten & Custance 1996). For example, if a specific response is part of the animal’s behavioural repertoire for approaching an object, such as pecking is in pigeon or quail, the observation of a pecking demonstrator may have acted as an innate releaser of pecking in the observer (Akins & Zentall 1996, 1998; Zentall et al. 1996). In combination with stimulus enhancement, or increased attention towards the demon-
strator’s manipulandum, contagion may be sufficient to explain demonstrator-consistent responding in observers (Campbell et al. 1999). Huber (1998) argued that novelty should be used more carefully as a means of identifying cases of true imitation for two reasons. First, there is little agreement as to how novelty should be defined. Second, it is difficult to see how the emergence of novel behaviours could be identified. However, Thorpe’s (1963, page 135) definition of imitation ‘as the copying of a novel or otherwise improbable act or utterance’ makes these problems more manageable. The probability that an action will be performed could be determined by using a group of nonobservers and measuring the frequency of occurrence of the target action. Using this method, Bugnyar & Huber (1997) showed that the exact reproduction of a sequence of actions used by a demonstrator to open a pendulum door was improbable. Therefore, the exact reproduction of the demonstrator’s sequence by two of the observers was interpreted as evidence of imitation. We permitted two groups of marmosets, Callithrix jacchus, to observe a demonstrator using one of two alternative techniques and compared their initial test responses with one another and with a third group of marmosets that were never given the opportunity to observe a demonstrator. The particular requirement of our experiment was that the two opening techniques (pulling with a hand versus pulling with the mouth) have the same effect on the environment, that is, the lid to be opened would ‘behave’ identically if moved automatically. Furthermore, one technique consisted of a behavioural ‘peculiarity’ (mouth opening), that is, mouth opening was neither common in the animals under investigation nor necessary for lid removal. This requirement ensured that if the technique was performed by the observers, then they were most probably influenced by what they witnessed (Whiten & Custance 1996; Whiten et al. 1996; Custance et al. 1999). Mouth opening was occasionally found in one female marmoset out of five animals and occurred as a by-product of a previous experiment on associative learning. We expected that observation of a mouth-opening demonstrator would affect the probability of other monkeys showing this behaviour. On the other hand, we predicted that observation of hand opening would have no effect on the probability of mouth opening by the monkeys. We tested this by making the removal of the lid more difficult (and perhaps mouth opening more efficient). We also used a nonexposed control group to control for nonsocial factors and to assess the baseline probability of the mouth-opening response. Finally, given the current concern in the literature with the potential role of olfactory cues in promoting demonstrator-consistent responding, we included an olfactory control group. METHODS
Subjects The subjects were 36 adult common marmosets, of which two were demonstrators and 11 were observers. We
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used 11 subjects (including the two models) for the nonexposed control and 14 for the olfactory control. The animals were maintained in four family groups at the Institute of Zoology of Vienna University, Austria, two family groups at the Konrad Lorenz Institute for Evolution and Cognition-Research, Altenberg, Austria, and three family groups at the Instituto Superiore di Sanita, Rome, Italy. All animals were born in captivity. At the Institute of Zoology two groups lived in indoor cages (250250250 cm) that were attached to outdoor cages of the same size and two groups lived in indoor cages (12080 cm and 180 cm high and 260260 cm and 250 cm high, respectively). At the Konrad Lorenz Institute both groups lived in indoor cages (200350 cm and 300 cm high). At the Instituto Superiore di Sanita the groups lived in indoor cages (15050 cm and 220 cm high). All cages were equipped with branches, ropes and living plants. All animals were fed fruits, vegetables, monkey pellets and protein supplements. The temperature was 26–30C during the day and 21–23C at night. The humidity was ca. 70–80%. In summer daylight was the main source of lighting, while in winter additional UV-fluorescent tubes were used to maintain a 12:12 h light:dark cycle.
Apparatus The apparatus consisted of a wooden board (1033 cm) with five black plastic film canisters for 35-mm Kodak slide films attached to it with screws. The board and the lids of the film canisters were painted blue. In each session the subjects were given three identical boards (with a total of 15 canisters). The canisters were each filled with one mealworm as a reward. In the observer sessions and in the first test session the lids of the canisters were half shut (only one half of the lid was firmly attached to the canister, whereas the other half did not click into place and therefore left a gap between the lid and the upper end of the canister) while in the second test session the lids were completely shut. At the laboratories in Altenberg and Rome the experiments were conducted in the home cage of the subjects, while the subjects in Vienna were tested in an experimental cage (12070 cm and 260 cm high) adjoined to the home cage.
Procedure Group Mouth In a previous experiment, female BI was the only one of five subjects that opened the canisters by removing the lids with its mouth (Fig. 1a). This animal was selected as the mouth-opening demonstrator. The other subjects in this previous experiment were not used in the present one. In six training sessions BI was separated from the other group members and we confirmed its original preference for the mouth-opening technique by offering completely shut canisters, which could only be opened by this technique. After the subject performed the task well (making only correct responses within three
Figure 1. Schematic representation of the two opening techniques performed by (a) the mouth-opening demonstrator and (b) the hand-opening demonstrator.
successive sessions and needing less than 2 min for each session), we gave BI two more sessions with half-shut canisters. After we confirmed that BI continued with this technique (only mouth opening in two sessions), we used it as demonstrator for six subjects (observers) of its neighbouring group (group Mouth). During the observation sessions, the other animals of BI’s group were locked out and we placed the three boards 25 cm from the wire-mesh partition that separated BI’s cage from the observers’ cage. The demonstrator (BI) was then allowed to open the canisters while all the observers had the opportunity to observe it. We conducted two observation sessions each day. The sessions were terminated as soon as the demonstrator had opened all the canisters. Immediately after the fifth observation session all the observers were tested individually in two successive test sessions. For this purpose we removed all but one subjects of the observer group from the observers’ cage and placed the boards into that cage. In the first test session the canisters were half shut and the subjects had a maximum of 10 min to open them. If the subjects needed less than 10 min to open the 15 canisters, the session was terminated earlier. After the first
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test session the subjects immediately had a second test session, in which the canisters were completely shut. The session was again limited to 10 min.
the subjects were tested individually in their home cages. The sessions were terminated after 15 min. In this experiment we gave all the subject two boards with a total of 10 canisters in each session.
Group Hand A male subject (GR) was separated from its group and confronted with the apparatus with half-shut canisters. GR spontaneously started to open the canisters using its hand (Fig. 1b). To confirm that GR opened the canisters in this manner we repeatedly offered only half-shut canisters. Unlike the first demonstrator (BI), GR was not given completely shut canisters, but it had seven successive training sessions with half-shut canisters. During these training sessions the experimental cage was visually isolated from the home cage by a cardboard partition. After GR had shown only correct responses within the last three sessions, it was used as a demonstrator. We removed the cardboard screen and placed the demonstrator in the experimental cage while the other group members (group Hand) could observe it. Again we conducted five sessions. The sessions were terminated as soon as the demonstrator had opened all the canisters. After these observation sessions every observer was separately tested in the experimental cage as described above.
Nonexposed control group To assess the frequency of spontaneous mouth opening we conducted a control experiment. The control group consisted of 11 individuals that had access to the boards without having the opportunity to observe a social model. As in the previous experiments, the subjects were tested individually in their home cages. The sessions were terminated after 15 min. If the subjects did not succeed in opening at least three canisters in one session, further sessions were added on subsequent days.
Olfactory control group Odour cues may have influenced our marmosets’ behaviour. The mouth-opening demonstrator (BI) may have left saliva containing food particles on the lids of the canisters, making its observers more likely to sniff at the lids than the marmosets that observed the hand-opening demonstrator. If this is correct, scent-mediated local enhancement instead of, or in addition to, response learning by observation might have been responsible for demonstrator-consistent responding in the mouth-opening observers. To determine whether differences in the opening techniques used by the two groups of observers resulted from a tendency for mouth-opening observers to approach the lid with their head and/or mouth, we analysed videotapes of these approaches in detail. We also conducted a second control experiment to determine more directly whether olfactory or visual cues, that is saliva or scratches, that the previous mouthopening animal might have left on the canisters’ lids, influence the subjects’ behaviour. This control group consisted of 14 subjects that had access to canisters that were previously opened by another animal by mouth. The subjects could not see the other animal opening the canisters, so this was again a nonexposed control. Again,
Data Analysis All sessions were videotaped with a DV camcorder (Sony VX 1000). We classified the behaviour at the apparatus as either mouth opening or hand opening. An action was called mouth opening when the subject bit into the lid and raised its head while still keeping a firm hold on the lid with its teeth (Fig. 1a). An act was called hand opening when a subject inserted one or more fingers at the edge of the lid and lifted the lid by stretching its forearm (Fig. 1b). As in studies with pigeons and quail in which stepping and pecking responses were compared (Akins & Zentall 1996, 1998; Zentall et al. 1996; Kaiser et al. 1997), the two response topographies contrasted here (mouth versus hand opening) were easily distinguished by the experimenter. Here, too, the postures and body parts involved in the two responses were different (compare Fig. 1a and b). Sometimes a subject opened the lid only half way by hand or mouth, then put its head into the gap between the lid and the canister, which caused the lid to open. If such a sequence was started by one of the two actions (mouth opening or hand opening) we accordingly classified it as mouth opening or hand opening. If a subject did not open the canister with the first movement and repeatedly used the same technique several times in succession, we counted this as one action. If a subject did not open the canister with the first movement (i.e. hand opening) and switched to the other opening technique (i.e. mouth opening) and opened the lid, we recorded this as mouth opening, because only full actions entered into the analysis. We defined a full action as an opening action where the lid was removed completely from the canister. The subjects could reach the reward only if the lid was completely removed. As every canister was filled with a mealworm, each full action was rewarded. The entire database was coded from videotape by B.V. To measure observer reliability we selected two short video sequences: one with 10 opening acts of an observer of group Hand and one with seven opening acts of an observer of group Mouth. We asked 11 independent persons to classify the opening acts as hand opening’, ‘mouth opening’ or ‘not visible’ (when the opening act was not clearly visible on the videotape). The persons did not know that one of the subjects had a mouth-opening demonstrator and the other a hand-opening demonstrator. They coded 99.42.2% (XSD) of the 17 actions in the same way that B.V. did. This indicates that these actions were clear and easy to distinguish and therefore the coding bias was negligible. RESULTS
Observation Phase While being observed, both demonstrators showed perfect discrimination between the two opening techniques.
VOELKL & HUBER: TRUE IMITATION IN MARMOSETS
Number of subjects
Hand opening
Mouth opening
8 NS 6 * 4
2
Mouth
Hand
Mouth
Hand
Group Figure 2. Number of observers that opened the canisters at least once by hand (Hand opening) or by mouth (Mouth opening) during the first test session. Six observers saw a mouth-opening demonstrator (group Mouth) and five saw a hand-opening demonstrator (group Hand). *P<0.05.
Both were presented with 75 canisters. The demonstrator for group Mouth (BI) opened all 75 canisters (100%) using its mouth. The demonstrator for group Hand (GR) opened 74 out of 75 canisters (98.7%) with its hand. One lid accidentally opened when GR jumped on to the board. GR opened the lid only half way by hand 12 times and removed the lid by putting its head into the canister.
Test Phase: First Test Session In both groups, all the subjects opened at least one canister with their hand, but opening the canisters with the mouth was shown by four out of six subjects from
group Mouth while none of the five subjects in group Hand opened a canister with its mouth (Fig. 2). Despite the small group size this difference was statistically significant (Fisher’s exact test: N=11, P=0.045). To compare the performance of the two groups we calculated a discrimination ratio for each subject by dividing the number of hand-opening acts performed during the first test session by the total number of opening acts during that session. The mean discrimination ratioSD was 0.640.34 (N=6) for group Mouth, and 1.000 (N=5) for group Hand (Table 1). We computed the standardized deviates (Sokal & Rohlf 1995) separately for each subject’s discrimination ratio, pooled the resulting deviates and tested them for normality by a Kolmogorov–Smirnov test for goodness of fit. The observed data did not depart significantly from a normal distribution (Z=0.754, P=0.62) and heterogeneous variances were assumed. Therefore we used Welch’s t test (Sokal & Rohlf 1995) to compare the means of the two groups. The discrimination ratios for groups Hand and Mouth were significantly different (t4.5 =2.33, P=0.033, one tailed).
Test Phase: Second Test Session In the second test session the canisters were completely shut and could only be opened by mouth. This session was conducted to investigate if the subjects that used only their hands in the first session were also able to open canisters with the mouth. From the two subjects from group Mouth that did not use the mouth in the first session, one immediately began to open the canisters with its mouth, whereas none of the subjects from group Hand managed to open a canister with its mouth. Thus in the second test session five out of six subjects from group Mouth opened the canisters with their mouth and one
Table 1. Opening behaviour of the observers and control subjects during the first and second test sessions Session 1
Group Mouth
Hand
Control
Subject DV MO WI SQ NI MA Mean KL SU VI GI SH Mean Mean
Nose-near-lid approaches
Mouth opening
Hand opening
Opened canisters
Discrimination ratio
Session 2 Opened canisters
3 2 4 5 7 0 3.5 2 2 3 5 5 3.4
0 6 13 11 2 0 5.3 0 0 0 0 0 0 1.0
15 8 2 4 13 15 9.5 15 15 15 15 14 14.8 10.9
15 14 15 15 15 15 14.8 15 15 15 15 14 14.8 13.0
1.00 0.57 0.13 0.27 0.87 1.00 0.64 1.00 1.00 1.00 1.00 1.00 1.00 0.92
0 15 15 15 6 15 11 0 0 0 0 0 0 1.6
The total numbers of nose-near-lid approaches, mouth-opening and hand-opening actions and opened canisters and the discrimination ratio (the number of hand-opened canisters divided by the total number of opened canisters) are shown for session 1. For session 2 only the total number of opened canisters is shown, as all canisters were opened by mouth. For the nonexposed control group (N=11) only the mean values are shown.
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subject failed to open at least one canister within 10 min, while none of the five subjects from group Hand succeeded in opening a canister (Fisher’s exact test: N=11, P=0.013).
mouth opening. The mean discrimination ratioSD was 0.850.34. The subjects opened the canisters significantly more often with their hands (Wilcoxon signed-ranks test: Z=2.128, P=0.033, two tailed).
Olfactory Exploration
Olfactory Control Group
Animals of both groups typically sniffed at the canisters, especially during the first test session. This behaviour was clearly part of their olfactory exploration at the onset of the test. We counted all approaches where an animal’s nose touched the lid of a canister, or came very close (to within 5 mm) to the lid (nose-near-lid). The mean number of nose-near-lid bouts until the first canister was openedSD was 3.52.4 for group Mouth and 3.41.5 for group Hand and the number of nose-near-lid bouts during the entire first session was 13.75.6 for group Mouth and 13.23.3 for group Hand. The mean latency to the first nose-near-lid boutSD was 45.844.2 s for group Mouth and 21.02.6 s for group Hand. Again we used the standardized values of both groups to test them for normality by a Kolmogorov–Smirnov test for goodness of fit. The observed data did not depart significantly from a normal distribution for the number of bouts until the first canister was opened (Z=0.463, N=11, P=0.983), for the number of bouts during the first session (Z=0.537, N=11, P=0.935) and for the latency to the first bout (Z=0.754, N=11, P=0.621). Therefore we used a two-tailed t test to compare the number of bouts until the first canister was opened and the number of bouts during the first session. To compare the latencies to the first bout a Welch’s t test was used after Levene’s test for equality of variances found heterogeneous variances between the two groups (F5,4 =5.998, P=0.037). No significant differences were found between group Hand and group Mouth in the number of nose-near-lid bouts until the first canister was opened (t test: t9 =0.08, P=0.938), the number of nose-near-lid bouts during the entire first test session (t test: t9 =0.16, P=0.874) and the latency to the first nose-near-lid bout (Welch’s t test: t4.5 =1.37, P=0.228). These data cannot exclude the possibility that the observers smelled some deposits on the lid without being influenced in the way they approached the canisters; the same is true for visual cues such as saliva droplets on the lid. But the argument that such cues promoted the approach with the head towards the lid and thus facilitated the probability of mouth opening is not supported by our data.
This control group consisted of 14 subjects. Five did not open any canister within the 15 min of the test session. Of the remaining nine subjects, eight opened the canisters with their hands and only one opened them with its mouth. The mean discrimination ratioSD was 0.89 0.33. The subjects opened the canisters significantly more often with their hands (Wilcoxon signed-ranks test: Z=2.433, P=0.015, two tailed). A comparison of the mean discrimination ratio with the nonexposed control group showed no significant difference (Mann–Whitney U test: U=41.5, N1 =11, N2 =14, P=0.652) whereas a comparison of the mean discrimination ratio with group Mouth was significant (Mann–Whitney U test: U=10.0, N1 =6, N2 =14, P=0.016) even when we applied a Bonferroni method (Sokal & Rohlf 1995) to evaluate the experimentwise error rate, which reduced the critical P value to 0.025. Thus the subjects from group Mouth opened the canisters significantly more often with their mouth than the subjects from the olfactory control group, which were given canisters previously mouth-opened by another monkey. On the other hand no difference could be found between the olfactory control group and the nonexposed control group, where the subjects were given canisters that were not previously mouth-opened. Therefore visual or olfactory cues on the lids of the canisters were not sufficient to promote mouth opening in naïve monkeys.
Nonexposed Control Group The nonexposed control group consisted of 11 subjects, including BI and GR, the two models. Two subjects did not open even one canister within the first test session and two opened fewer than three canisters. However, these four subjects successfully opened canisters in the second test session. To assess the discrimination ratio of these animals, we pooled the data from the first and second test sessions. Only two of 11 subjects showed
DISCUSSION Common marmosets copied the response topography of a conspecific demonstrator to open a Kodak film canister and obtain a desired food item. More specifically, marmosets that had observed a demonstrator using its mouth to remove the lid from a film canister were more likely to use this technique during a subsequent test session than marmosets that had observed a demonstrator using exclusively its hand. In fact, mouth opening was rare in 30 subjects that had never seen a mouth-opening demonstration or any opening demonstration before. These results are consistent with a previous study of imitative learning in marmosets (Bugnyar & Huber 1997) and raise doubts about the claim that the ability to imitate is unique to great apes, including humans (Tomasello & Call 1997; Byrne & Russon 1998). This effect cannot be accounted for by either enhancement effects or object movement re-enactment (learning how an object moves; Heyes 1998), since the lid of the canisters moved in the same way for both observer groups. Contagion is also an unlikely explanation, since the observers were tested in the absence of a demonstrator. Finally, it is also unlikely that olfactory cues influenced the direction and strength of the observers’ approach behaviour. A control experiment showed that
VOELKL & HUBER: TRUE IMITATION IN MARMOSETS
deposits left by the demonstrators on the lids of the canisters did not increase the probability of mouth opening. Observers of hand-opening demonstrators also sniffed the lid as frequently and closely as observers of mouth-opening demonstrators. After decades of refining both methods and terminology, the future of social learning will inevitably involve attempts to extend the range of species comparisons. Not only will questions of how animals become proficient imitators achieve heuristic value, but also questions about what conditions promote social learning in contrast, or in addition, to individual learning. As suggested by Caldwell et al. (1999), the all-or-none approach to imitation is being superseded by an approach that recognizes the complex concatenations of the processes and circumstances of social learning. The repeated failure to find robust imitative effects in animals other than apes may be due to either an overestimation of the species’ manipulative abilities or an underestimation of the species’ other capacities that render the task more manageable. For example, marmosets experienced difficulty in turning a handle in order to open a plastic box with a hinged lid (Caldwell et al. 1999) and olfactory cues played a greater role than visual cues in the rat’s exploratory behaviour (Mitchell et al. 1999). To identify the conditions under which robust imitative effects occur, we need some understanding of the species’ ecological niche and the natural context in which movement imitation appears. In humans, and probably in some great apes and dolphins, faithful copying of a demonstrator’s behaviour is part of a social game. Learning to exploit hidden food sources may be well established in highly explorative and manipulative mammals (e.g. chimpanzees, Pan troglodytes: Whiten et al. 1996) and birds (e.g. ravens, Corvus corax: Fritz & Kotrschal 1999; keas, Nestor notabilis: L. Huber, S. Rechberger & M. Taborsky, unpublished data). Vocal mimicry is widespread among birds and common in humans, but occurs rarely, if ever, in great apes and other mammals (Moore 1996). Furthermore, the occurrence of social-learning mechanisms may also be influenced by the species’ group size (Boyd & Richerson 1996) and social tolerance (Coussi-Korbel & Fragaszy 1995). In tolerant primate groups, such as the marmoset family, individuals often follow one another, exploring the forest canopy and approaching others busy with interesting objects. In these situations, copying behaviour is likely to occur, especially if an individual cannot understand the causal structure of the task. Recently, Huber (1998) argued that copying fidelity would be especially high if it was not affected by an insight into the causal relationships of the task (programme imitation; Byrne & Byrne 1993), the affordances of the objects (emulation or affordance learning; Tomasello 1996) or the goal and intentions of the demonstrator (goal emulation; Whiten & Ham 1992). If all of these types of information are beyond the cognitive capacity of the species, then slavish copying is a valuable alternative. Behavioural peculiarities, unnecessary extensions and even errors in performance can be used to determine the degree and type of behavioural matching. In the present experiment, we were able to benefit from a peculiar
opening technique shown by a single female during a pilot study. We further profited from the fact that this behavioural peculiarity involved an action that differed on a large scale from the default action in that it involved a different body part. Thus, we avoided a problem common to studies of social learning in great apes (see Tomasello 1996 and Whiten & Custance 1996 for reviews), in which a complex object or a tool is manipulated with the hands in one of two or more different ways, only one of which is demonstrated to a subject. A further advantage of our two-action/one-peculiarity approach is that copying of a peculiar behaviour qualifies as being truly imitative. According to Thorpe (1963), one should consider only motor acts that do not pre-exist in the animal’s behavioural repertoire at the onset of the experiment, otherwise socially mediated behaviour (contagion) would be sufficient to result in behavioural matching. We were able to show that the probability of spontaneous mouth-opening behaviour was low; in the two nonobserver control groups mouth opening was rare and in the hand-opening observer group it never occurred. Although mouth opening may not be completely novel at the level of motoric execution, it is a rather novel technique for opening plastic film canisters (see Akins & Zentall 1996 for a similar argument on ‘novelty’). To conclude, our findings support the suggestion that basic forms of imitative learning occur not only in humans and great apes but also in monkeys. Regardless of the mechanism responsible for behavioural matching, it seems plausible that social learning allows the experience of one individual to be acquired by others more efficiently than would be the case with trial-and-error learning (Boyd & Richerson 1988). As we saw here, and also in Bugnyar & Huber (1997), even faithful copying in the absence of insight may help to solve a task that otherwise could not be solved. Those monkeys in our study that did not have the opportunity to observe a mouth-opening demonstrator failed to open canisters, and hence to obtain a highly nutritious food, when the canisters were completely closed (second test session). This is especially interesting in the case of the hand-opening observers, which had extensive experience with the canisters. Thus, our findings also provide some support for the hypothesis that social learning may be adaptive. Acknowledgments This experiment was conducted by B.V. in partial fulfillment of the requirements for the Master degree in Zoology at the University of Vienna. Ruth Sonnweber built the apparatus and conducted a pilot study. Augusto Vitale, Armelle Queyras and Michela Zanzony helped conduct the control experiment. Financial support was provided by the Austrian Science Foundation (FWF-grant P 12011-BIO). We thank Celia Heyes for comments and Fiona Campbell for improving the English. References Akins, C. K. & Zentall, T. R. 1996. Imitative learning in male Japanese quail (Coturnix japonica) using the two-action method. Journal of Comparative Psychology, 110, 316–320.
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